LEMUR NEWS
LEMUR NEWS
TheNewsletteroftheMadagascarSectionoftheIUCN/SSCPrimateSpecialistGroup
Vol.15,2010 ISSN1608-1439
Editors
ChristophSchwitzer(Editor-in-chief)
BristolConservationandScienceFoundation,BristolZooGardens,UK;cschwitzer@bcsf.org.uk
ClaudiaFichtel
GermanPrimateCenter,Göttingen,Germany;claudia.fichtel@gwdg.de
JörgU.Ganzhorn
UniversityofHamburg,Germany;ganzhorn@biologie.uni-hamburg.de
RodinM.Rasoloarison
GermanPrimateCenter,Göttingen,Germany;kirindy@simicro.mg
JonahRatsimbazafy
GERP,Antananarivo,Madagascar;gerp@wanadoo.mg
AnneD.Yoder
DukeUniversityLemurCenter,Durham,USA;anne.yoder@duke.edu
IUCN/SSCPrimateSpecialistGroup
ChairmanRussellA.Mittermeier,ConservationInternational,Arlington,VA,USA
DeputyChairAnthonyB.Rylands,ConservationInternational,Arlington,VA,USA
Coordinator–SectiononGreatApesLizWilliamson,StirlingUniversity,Stirling,Scotland,UK
RegionalCoordinators–Neotropics
Mesoamerica–LilianaCortés-Ortiz,MuseumofZoology&DepartmentofEcologyandEvolutionary
Biology,UniversityofMichigan,AnnArbor,MI,USA
AndeanCountries–ErwinPalacios,ConservationInternationalColombia,Bogotá,Colombiaand
EckhardW.Heymann,DeutschesPrimatenzentrum,Göttingen,Germany
BrazilandtheGuianas–M.CecíliaM.Kierulff,InstitutoparaaConservaçãodosCarnívoros
Neotropicais–Pró-Carnívoros,Atibaia,SãoPaulo,Brazil,FabianoRodriguesdeMelo,Universidade
FederaldeGoiás,Jataí,Goiás,Brazil,andMaurícioTalebi,UniversidadeFederaldeSãoPaulo,Diadema,
SãoPaulo,Brazil
RegionalCoordinators–Africa
WestAfrica–W.ScottMcGraw,TheOhioStateUniversity,Columbus,OH,USA
RegionalCoordinators–Madagascar
JörgU.Ganzhorn,HamburgUniversity,Hamburg,Germany,andChristophSchwitzer,BristolConservation
andScienceFoundation,BristolZooGardens,Bristol,UK
RegionalCoordinators–Asia
China–LongYongcheng,TheNatureConservancy,China
SoutheastAsia–JatnaSupriatna,ConservationInternationalIndonesiaProgram,Jakarta,Indonesia,and
ChristianRoos,DeutschesPrimatenzentrum,Göttingen,Germany
IndoBurma–BenRawson,ConservationInternational,Hanoi,Vietnam
SouthAsia–SallyWalker,ZooOutreachOrganization,Coimbatore,TamilNadu,India,andSanjayMolur,
WildlifeInformationLiaisonDevelopment,Coimbatore,TamilNadu,India
Editorialassistants
NicolaDavies,RoseMarieRandrianarison
Layout
HeikeKlensang,AnnaFrancis
Frontcover:TheEndangeredgolden-crownedsifaka(Propithecustattersalli)attheedgeofanareadevastated
bygoldminingactivitiesintheDarainaregionofnorth-easternMadagascar.©PeteOxford/naturepl.com
Addressesforcontributions
ChristophSchwitzer
BristolConservationandScienceFoundation
BristolZooGardens
Clifton,BristolBS83HA
UnitedKingdom
Fax:+44(0)1179736814
Email:cschwitzer@bristolzoo.org.uk
JonahRatsimbazafy
GERP
34,CitédesProfesseurs
Antananarivo101
Madagascar
Email:gerp@wanadoo.mg
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All15volumesareavailableonlineatwww.primate-sg.org,www.aeecl.organdwww.dpz.eu
ThisvolumeofLemurNewswaskindlysupportedbytheMargotMarshBiodiversityFoundation
(throughConservationInternational’sPrimateActionFund)andbyWWFMadagascar.
PrintedbyGoltzeGmbH&Co.KG,Göttingen,Germany
Lemur News Vol. 15, 2010
Editorial
I am writing this Editorial only a couple of days after another
attempted (and failed) Coup d’Etat in Madagascar, in which a
faction of the army tried to topple the Transition Government. For nearly two years now, since the start of the political crisis in early 2009,the country has not seen a week without demonstrations, tensions between different political
parties and attempts from international mediators to get
power-sharing agreements signed by all sides. Most donors,
governments and multinational organisations alike, have
frozen all non-humanitarian aid for Madagascar,which has led
to severe funding shortages in the environmental and conservation sector. The political crisis has thus quickly turned
into a full-blown environmental crisis, with large-scale illegal
logging taking place mainly in eastern Madagascar (Marojejy,
Masoala, Makira), and unseen levels of lemur poaching all
across the island. To keep people aware of the seriousness of
the situation we have decided to run another feature on
Madagascar’s environmental crisis in this issue of Lemur News,
with an excellent update on illegal logging by Erik Patel as
well as a case study of ongoing threats to lemurs and their
habitat in Sahamalaza National Park by Melanie Seiler and
colleagues.
The conservation situation of lemurs has also been a big concern in several presentations given at the most recent 23rd
Congress of the International Primatological Society in
Kyoto, Japan. The talk that I remember best was by Lemur
News co-editor Jonah Ratsimbazafy, who reminded the audience in a very emotional way that scientists and conservationists working in Madagascar had a moral responsibility to
respond to the "cries of the lemurs", as otherwise these
would remain unheard by the Malagasy and international
community. In the biennial discussion session of "Primates in
Peril", the list of the world’s top 25 most endangered primates, issued jointly by the IUCN/SSC Primate Specialist
Group and IPS, lemurs remained a very high priority and will
again make up 20% of the 25 listed species in the next biennium. Sadly,Madagascar thus retains its first place (along with
Vietnam) as the country harbouring the highest number of
the top 25. It can only be hoped that the political classes of
Madagascar come to agree a way out of the current crisis
sooner rather than later, as otherwise we run the very serious risk,during the UN Decade of Biodiversity 2011-2020,of
losing a substantial proportion of the endemic biodiversity of
this amazing megadiversity country.
Alison Jolly with Russ Mittermeier at the IPS Lifetime Achievement Award 2010 ceremony in Kyoto. (Photo: R. Mittermeier)
Page 1
For a change, on a very positive note, I am thrilled to say that
Alison Jolly was awarded the IPS Lifetime Achievement
Award for her long-term commitment to lemur conservation and environmental education in Madagascar (see News
and Announcements). My two daughters (now 4 and 2 years
old) and I particularly enjoy reading Alison’s children’s book
on Bitika,the mouse lemur,as,I am sure,do lots of children in
Madagascar and elsewhere in the world.
It is encouraging to see that this volume of Lemur News is
again full of articles and short reports not only on lemur species red-listed in one of the Threatened categories (VU, EN
or CR), but also on Data Deficient nocturnal species such as
Mirza zaza, Lepilemur leucopus and the recently rediscovered
Cheirogaleus sibreei (see the articles by Rode et al., Fish, and
Blanco, respectively). As Johanna Rode and colleagues point
out in their short report on Mirza zaza, Madagascar is in the
unusual situation that 45 % of its primate species are redlisted as Data Deficient, which is a far higher percentage than
in any other primate habitat country and mainly derived
from the discovery of dozens of cryptic species in the genera
Lepilemur and Microcebus over the last couple of years. Many
of those species are only known from their type localities
and may in fact be highly endangered. The more research is
conducted and published on them, the easier it will become
to assign them a conservation status and target them with
conservation measures. It will require a concerted effort of
the lemur research and conservation community over the
next decade or so to to reduce the number of Data Deficient
species to a level comparable to other regions (or, ideally, to
zero).
Another encouraging development is the frenzy of research
and conservation activities now under way for Prolemur simus
at various locations both south and north of the Mangoro
River,reported by Dolch et al.as well as Rajaonson et al.in this
volume. The greater bamboo lemur undoubtedly remains
one of the most endangered of Madagascar’s lemurs. However, with several additional populations having been discovered over the last two years, workshops having been conducted that have led to a joint-up approach to this species’
conservation,and the ex situ population having been included
as an integral part of conservation efforts, I now think that
we stand a real chance of saving Prolemur simus from extinction.
As Jörg Ganzhorn announced in his editorial to Lemur News
14, I have taken over the coordination of this newsletter
from him after the 2009 volume, hence this is now the first
volume that I have helped produce (which is my humble excuse for its slightly late publication). Jörg has been involved
with Lemur News since its inception in 1993,first as a member
of its Editorial Board and from volume 3 (1998) as its Editor.I
am thus pleased to say that we will not lose his experience
and backing,as he has kindly agreed to remain part of the editorial team. Likewise, Jonah Ratsimbazafy and Rodin Rasoloarison, who have been the newsletter’s Malagasy coordinators since 2006, and Anne Yoder, who represents the Duke
Lemur Center, will carry on as editorial team members, for
which I am grateful.I am indebted to Heike Klensang,who has
been doing the layout for Lemur News now for more than a
decade and is still not tired of it,and to Anna Francis,who has
designed the beautiful new logo and front cover. Very many
thanks also to Stephen D. Nash for the wonderful lemur silhouettes that we printed on the inside back cover.
This volume of Lemur News was kindly supported by the
Margot Marsh Biodiversity Foundation through Conservation International’s Primate Action Fund, and by the WWF
Madagascar and West Indian Ocean Programme Office.
Page 2
I very much look forward to helping to take Lemur News into
the UN Decade of Biodiversity together with the editorial
team and with its base of loyal contributors and readers,and I
will do my best to ensure that the newsletter will continue to
help promote the conservation of lemurs as it has done for
the last 17 years.
Christoph Schwitzer
Feature: Madagascar’s
Environmental Crisis
Madagascar’s illegal logging crisis: an update and discussion of possible solutions
Erik R. Patel
Cornell University, 211 Uris Hall, Ithaca, NY 14850, USA,
patel.erik@gmail.com
How sure are you that your favorite rosewood or ebony
acoustic guitar was not made from rare, illegally logged trees
in Madagascar; an exceptional biodiversity hotspot with desperately little original forest remaining? What is the origin of
the wood in the expensive oriental-style rosewood furniture
which is heavily advertised for sale on the internet? Unfinished rosewood boards from Madagascar are openly sold
even in the United States (www.gilmerwood.com/boards_
rosewood-exotic_unique.htm) and the United Kingdom (www.
exotichardwoods.co.uk/Woods_List/Madagascar_Rosewood.asp).
Can such vendors prove that the rosewood was legally (and
ethically) obtained? The answer is usually "no". These can be
difficult questions for consumers to answer, but purchasing
these products can prolong the ongoing logging crisis in
northeastern Madagascar in some of the most unique and biologically diverse forests in the world.
Consumers should be suspicious since none of these rapidly
disappearing Madagascan rosewood and ebony species are
yet protected under CITES,the Convention on International
Trade in Endangered Species. In November of last year, Gibson Guitars, one of the two largest U.S. stringed-instrument
companies,came under federal investigation for violating the
Lacey Act by allegedly using illegal rosewood from Madagascar which had first been shipped to Germany and then the
United States (Michaels, 2009). Most of the illegally logged
rosewood in Madagascar is used for the manufacture of furniture in China. Some of this is known to be sold in China as
luxurious "Ming Dynasty style" furniture (Global Witness
and Environmental Investigation Agency, 2009). Some may
well be exported to western countries. China is the world’s
leading exporter of furniture. According to the Office of the
United States Trade Representative, the United States imported 16 billion dollars of Chinese furniture in 2009,making
it the USA’s fifth largest import from China.
Illegal logging of rosewood (Dalbergia spp.) and ebony (Diospyros spp.) has emerged as the most severe threat to Madagascar’s dwindling northeastern rainforests. In 2009, a year
of political upheaval in Madagascar due to an undemocratic
change of power, approximately 100,000 of these trees were
illegally cut in the UNESCO World Heritage Sites of Masoala
National Park,Marojejy National Park,the Makira Conservation Site, and Mananara Biosphere Reserve (also a national
park).Needless to say,the wood is extremely valuable.Rosewood can sell for US$5,000 per cubic meter,more than double the price of mahogany. Several hundred million dollars of
Lemur News Vol. 15, 2010
these precious hardwoods were cut in 2009 in protected
areas. The overwhelming majority of these profits are taken
by a rosewood mafia of a few dozen organizing individuals,
many of whose identities are well known.Few others benefit.
Harvesting these extremely heavy hardwoods is a labor intensive activity requiring coordination between local residents who manually cut the trees, but receive little profit
(about US$5/day), and a criminal network of exporters, domestic transporters, and corrupt officials who initiate the
process and reap most of the enormous profits. This is a
"tragedy with villains" unlike habitat disturbance from subsistence slash-and-burn agriculture which has been well described as a "tragedy without villains" (Barrett et al., 2010;
Débois, 2009; Global Witness and Environmental Investigation Agency,2009;Patel, 2007,2009;Randriamalala and Liu,in
press; Schuurman and Lowry, 2009; Schuurman, 2009; Wilme
et al., 2009; Wilme et al., in press).
Globally, illegal logging results in an estimated US$10 billion
lost per year to the economies of timber producing countries (Furones, 2006). In addition to depriving the government of Madagascar of millions of dollars of taxable revenue,
illegal logging of this precious wood has decimated tourism
in northeastern Madagascar, which had become a growing
source of local income. Although selective logging results in
less absolute forest loss than clear-cutting, it is often
accompanied by substantial peripheral damage such as decreases in genetic diversity and increases in the susceptibility
of the impacted areas to burning and bushmeat hunting.
Documented long-term ecological consequences of selective logging in Madagascar include invasion of persistent,
dominant non-native plant species, impaired faunal habitat,
and a diminution of endemic mammalian species richness
(Gillies, 1999; Cochrane and Schultze, 1998; Brown and
Gurevitch, 2004; Stephenson, 1993). In actual practice, rosewood logging has turned out to be far less "selective" than
originally believed. Often rafts made of a lighter species of
wood (Dombeya spp.) are constructed to float the much
more dense rosewood logs down rivers. Approximately five
Dombeya trees are cut as "raft wood" for every one rosewood tree (Randriamalala and Liu,in press).Tall adult trees of
a variety of species, that simply happen to be very close to
rosewood trees, must often be cut simply to gain access to
cut down a rosewood tree. This has been observed in
Marojejy (pers. obs.).
Red ruffed lemurs (Varecia rubra) are probably the most negatively impacted lemur since many were hunted by these loggers and this species is known to feed on ebony trees
(Diospyros spp.) as well as pallisandre (Dalbergia spp.) in
Masoala (Vasey, pers. comm.). Varecia rubra probably also
feeds on the fruits and leaves of the logged "raft wood"
Dombeya spp. trees like Varecia v. editorium in Manombo Forest in southeastern Madagascar (Ratsimbazafy, 2007). In
Mantadia National Park, Indri indri and Propithecus diadema
consume young leaves of one species of actual rosewood
(Dalbergai baronii) which is also consumed by Milne-Edwards’
sifakas (Propithecus edwardsi) in Ranomafana National Park
(Powzyk and Mowry, 2003; Arrigo-Nelson, 2007). Propithecus
diadema at Tsinjoarivo consume the unripe fruit of ebony
trees (Irwin, 2006). In Marojejy, silky sifakas (Propithecus
candidus) not uncommonly feed on the young leaves of pallisandre (Dalbergia chapelieri) which is also a preferred sleeping tree (pers. obs.).
When discussing the impacts of precious wood logging, it is
important not to forget how damaging all this has been to local communities as well. Local residents have suffered as foreign and domestic elites have corrupted the forest service,
leading to losses of sustainable employment in tourism, re-
Page 3
Lemur News Vol. 15, 2010
search, and conservation. In some cases, community life has
suddenly changed as gambling, prostitution, and crime have
increased in rural communities. Moreover, the risks of local
food shortages and nutritional deficiencies mount when
farmers abandon subsistence agriculture for temporary,physically dangerous illegal logging work (Global Witness and
Environmental Investigation Agency, 2009;Patel, 2007, 2009).
Moreover,illegal loggers trample on the beliefs and taboos of
local people. In traditional Sakalava culture, ebony is a sacred
wood only cut by priests who conduct traditional ceremonies with ebony staffs. The chief of Ankalontany, a Sakalava
Malagasy village in the northeast, explained that "Some
strangers from outside our village came here. They started
cutting ebony and they clearly had no right. We asked for
their authorization but they said they didn’t have to show us
papers.They said they had police clearance and we can’t stop
them." Laurent Tutu, president of the forest association of
Ankalontany, remarked "It hurts us to see our trees cut like
this. The forest loses its personality" (Cocks, 2005).
Although illegal logging in Madagascar has received some media attention recently, confusion still remains regarding a
number of key facts. The aim of this report is to provide an
update (at the time of writing: May 25, 2010), dispel a few
myths, discuss some of the possible solutions to this ongoing
crisis, and present a comprehensive bibliography of articles,
photos, films, and videos related to this topic.
Four myths about illegal logging in Madagascar
Myth #1: "Plenty of Madagascar rosewood is harvested legally…" says Bob Taylor, founder of Taylor Guitars. Quote
from Gill, C. (2010). Log Jam. Guitar Aficionado. Spring Issue.
P. 68
This is simply not true. A vast amount of published evidence
clearly shows that very very little,if any,of the rosewood logging in Madagascar is legal.The overwhelming majority of exported Madagascar rosewood is illegally logged within Masoala National Park and Marojejy National Park (which are part
of a UNESCO World Heritage Site) as well as Mananara Biosphere Reserve (also a national park) and the vast Makria
Conservation Site (Barrett et al., 2010; Débois, 2009; Global
Witness and Environmental Investigation Agency,2009;Patel,
2007, 2009; Randriamalala and Liu, in press; Schuurman and
Lowry, 2009; Schuurman, 2009; Wilme et al., 2009; Wilme et
al., in press).
Myth #2: The current ban has stopped illegal logging.
In late March, the government of Madagascar announced a
new two to five year ban on export and cutting of ebony and
rosewood. The decree #2010-141 officially passed on April
14, 2010. Clearly this was an important and large step forward. However, the decree does not apparently include
pallisandre, a precious hardwood in the same genus (Dalbergia) as rosewood. Illegal logging of pallisandre has heavily
impacted some reserves such as Betampona Natural Reserve (Kett, 2005; Bollen, 2009). At the time of writing (May
25, 2010), there have been no new exports since the recent
ban.However,illegal rosewood and ebony logging still continues inside Mananara Biosphere Reserve and the Makira Conservation Site according to reliable anonymous informants.
The clearest information has come from Mananara where at
least several hundred, recently cut, rosewood logs were observed.
Myth #3: Illegal logging was never a big problem in Madagascar until the recent political crisis.
Illegal logging in Madagascar of rosewood (Dalbergia spp.) and
ebony (Diospyros spp.) did not begin with the culmination of
the political crisis in March 2009.A major illegal logging crisis
in World Heritage Sites (Masoala National Park and Marojejy
National Park) took place during 2004-2005, a time of political stability. The earliest documented case of rosewood logging in Madagascar and foreign export dates to 1902.Foreign
exports of Madagascar rosewood occurred at "low" levels
(1000 to 5000 tonnes) between 1998 and 2007. In 2008, exports jumped to 13,000 tonnes, and jumped again in 2009 to
more than 35,000 tonnes (Botokely,1902;Randriamalala and
Liu,in press;Global Witness and Environmental Investigation
Agency, 2009).
Myth #4: There are 43 species of rosewood trees in Madagascar.
Some recent reports had mistakenly made this statement. It
is not entirely clear exactly how many rosewood species are
found in Madagascar. More botanical research is needed.
However, currently, there are believed to be 10 species of
rosewood in Madagascar in the genus Dalbergia which contains 48 total species. The rosewood species are presumed
to be Dalbergia baronii [VU], D. bathiei [EN], D. davidii [EN], D.
louvelii [EN], D. mollis [NT], D. monticola [VU], D. normandii
[EN], D. purpurascens [VU], D. tsiandalana [EN], and D. viguieri
[VU] (Barrett et al., 2010).
Rosewood stockpile solutions?
Approximately 10,280 tonnes of illegally logged rosewood
remain stockpiled in numerous locations in northeastern
Madagascar, such as the ports of Vohemar and Antalaha as
well as private residences in those cities and Sambava,
Ampanifena,Ambohitralalana,and others.Each 150 kg log has
an approximate market value of US$1,300 usd. As unfinished
logs, the value of the current stockpile is therefore approximately US$90 million.Value increases dramatically,of course,
after being constructed, for example, into high-end Ming
Dynasty style furniture in China. A single armoire composed
of only a few logs can sell for US$20,000 or more.It’s a horrid
contrast to the annual income in Madagascar (about
US$400) or the daily wage provided to loggers (US$5) for
the dangerous and physically debilitating work (Randriamalala and Liu, in press; Global Witness and Environmental
Investigation Agency, 2009; anonymous local informants).
If the export ban holds (numerous other bans did not), what
should be done with these stockpiles? Several ideas have
been suggested.
1. The "Forest Counterpart Fund" (Wilme et al., 2009) aims
to create a conservation and charitable works fund to assist
local communities and forests damaged by the illegal logging.
The logs are not sold on the open market as in the second
proposal below.Rather,philanthropists,conservation organizations, and international aid agencies pay to "adopt" a log.
Each log can be "adopted" for its market value (about
US$1,300). The logs themselves are given to (carefully selected) local residents who are victims of the illegal logging.
The logs would then be carved,engraved,and customized for
public display as symbols. If sufficient donors can be found,
this proposal offers a win-win solution for Madagascar’s forests as well as people.
2. The Moratorium-Conservation-Amnesty-Reforestation
(MCAR) program (Butler, 2009). This is essentially a one-off
actual sale with conservation benefits. Logs would be auctioned via a transparent market system in which the price
and the log code would be recorded, publicly available, and
digitally traceable.Funds generated would mainly go towards
Page 4
conservation programs such as reforestation and forest
monitoring. Criminal traders would receive amnesty from
prosecution as well as a very small percentage of the funds.
An export moratorium would be required. There is always a
danger that one-off sales can encourage further logging; a
topic which has been extensively debated with respect to
confiscated elephant ivory stockpiles. An impressive recent
review paper in Science (Wasser et al., 2010):
www.sciencemag.org/cgi/content/short/327/5971/1331)
argued that no one-off ivory sales should be approved even if
the funds go towards conservation.
3. Destroy the stockpile. This was recently reiterated by
Global Witness (GW) and Environmental Investigation
Agency (EIA). Andrea Johnson, Director of Forest Campaigns at EIA explained that "To end the cycle of illegal harvest and corruption, the government should take the step of
destroying all stocks that are not contained in the latest official inventories…Traders, who are currently stockpiling illegal timber, hoping for another ‘exceptional’ export authorization, must receive a clear signal that it will be impossible to
profit from the illegal trade in the future." Numerous examples can be found from around the world of simple and effective destruction of stockpiles of contraband such as small
arms,drugs,and ivory.Destruction also eliminates the not insignificant expense of storing and guarding the items.Burning
the rosewood stockpiles would create a lot of pollution, it
has been argued, and might be dangerous given the high volume. Other ways of destroying the wood are possible however. The wood could be hacked into tiny unusable pieces.
This is already done sometimes by park rangers in Madagascar. This would take a very long time, but would be a fitting
punishment of hard labor for members of the rich rosewood
mafia! Of course, destruction of the wood, whatever the
method,would contribute no money for any conservation or
community development funds.
Any of these possibilities are better than what has happened
in the past:seized wood was auctioned off to the highest bidder.Foreign export remains a possibility too,despite the ban.
French shipping company CMA-CGM Delmas exported
rosewood from Madagascar several times in 2009 and 2010.
Long-term solutions?
Thinking long-term, what can be done to prevent another illegal logging crisis in Madagascar?
Some may argue that so little rosewood and ebony remains,
logging on this scale could never happen again. However, this
had been claimed before 2009 too. More surveys are clearly
needed. One hopes that some of the more impenetrable regions of mountainous Marojejy National Park may still have
rosewood. But because rosewood tends to be harvested at
lower elevations, near rivers (where the largest individuals
are found), it is less protected by the physical challenges of
the massif than some other tree species. It is encouraging
that some Dalbergia and Diospyros species can form stump
sprouts which can grow into a new tree over many many
years. Unfortunately, some entire rosewood stumps are removed either to hide evidence of logging or for wood for
small, locally made rosewood vases. Rosewood trees are
known to be some of the oldest trees in the eastern Malagasy
humid forests. They can live to be more than 400 years old,
according to local guides. Traders explain that they can be
harvested after 50 years (Patel 2007, 2009).
1. CITES
The surest way to reduce the likelihood of another illegal
logging crisis in Madagascar, is to list all species in the genera
Lemur News Vol. 15, 2010
of Dalbergia and Diospyros on CITES Appendix 1. Currently
none of Madagascar’s ebony or rosewood species are protected under any appendices within the Convention on International Trade in Endangered Species (CITES). Globally,
only one species of rosewood,Brazilian rosewood (Dalbergia
nigra), is listed under CITES Appendix 1. This is the most
stringent category, and prohibits all commercial trade of that
wood from the date of listing. This has generally been effective.Guitars in the United States made of Brazilian rosewood
are known to have risen in price and are harder to find since
Appendix 1 listing. Similarly, Appendix 1 listing of Alerce
(Fitzroya cupressoides), a heavily logged South American conifer, has significantly reduced logging and trade (Barrett et al.,
2010; Keong, 2006).
A few other Brazilian and Central American rosewood species are listed under CITES Appendix 2 and 3. These lower
appendices aim to regulate trade,not prohibit it.Just this year,
another species of Brazilian rosewood (Aniba rosaeodora),exported extensively as fragrant oil, was listed under CITES
Appendix 2. Two additional species of Central American
rosewood (D. retusa and D. stevensonii) are listed under Appendix 3. Appendix 2, unlike Appendix 3, does require that
the CITES authorities in the export nation determine that
the species were legally obtained and that their export will
not be detrimental to species survival. There seem to be few
cases where Appendix 3 listing was sufficient, except as a
means to Appendix 2 or higher listing. The well examined
case-studies of big-leaf mahogany (Swietenia macrophylla) and
ramin (Gonystylus spp.) both began as Appendix 3 species
(which only requires unilateral listing by a habitat country)
and were later voted in as Appendix 2 species by the CITES
parties (Keong, 2006).
To what degree can CITES regulations be implemented and
enforced? The need for more officially trained import inspectors has been suggested numerous times. The agency
chosen as the CITES management authority should be free
of corruption and have experience in forest management.
Insufficient trained staff has also hindered the ability of export authorities to determine whether an Appendix 2 species was legally obtained and non-detrimental to species survival.Range countries often require assistance in this respect.
An unusually good example comes from Indonesia where biological data for ramin has been used in non-detriment findings to examine sustainability. Missing "certificates of origin"
have been a problem for some Appendix 3 species. While
ramin and big-leaf mahogany were listed on Appendix 3, the
required ‘certificates of origin’ were not consistently issued
by exporting nations; while importing countries were not always diligent about confirming that shipments arrived with
such certificates (Blundell, 2007; Keong, 2006).
2. Independent forest monitoring (IFM)
In addition to CITES,actual improvements in forest monitoring on the ground are needed. A new system called independent forest monitoring (IFM) may be needed in order
stop illegal logging, monitor implementation of REDD (Reducing Emissions from Deforestation and Forest Destruction) programs, restore the confidence of international donors, and ultimately to save Madagascar’s precious forests as
well as attain social justice for Madagascar’s impoverished
population. IFM has been defined as "the use of an independent third party that,by agreement with state authorities,provides an assessment of legal compliance, and observation of
and guidance on official forest law enforcement systems"
p. 18 (Global Witness,2005). IFM is similar in principle to unbiased international election observers. Local and international expertise is utilized, and monitoring teams operate
Page 5
Lemur News Vol. 15, 2010
independently but with the consent of the host government.
Independent forest monitors are strictly observers, law enforcement remains the responsibility of local officials and
governments.
Of course other nations have been faced with similar forest
monitoring problems.IFM has already been used successfully
in several African and Central American nations seeking to
improve the effectiveness of their forest monitoring. Since it
was first introduced in 1999, IFM has been established in
Cameroon, Cambodia, and Honduras. Smaller scale feasibility and pilot studies have been conducted in Ghana, Peru,
Mozambique, Republic of Congo, Tanzania, and Democratic
Republic of Congo. In Cambodia and Cameroon, donor
countries have been the impetus behind IFM.Though in Honduras, the incentive for IFM was domestic, and hosted by the
Honduran Commission for Human Rights (CONADEH).
Furones (2006) and Young (2007) review the results of IFM in
these nations, and consider them to be "broadly positive".
Specific examples of the impact of IFM in these nations include: documentation of hundreds of forest crimes, cancellation of logging concessions,moratoriums on logging and timber transport,and creation of new "forest crimes monitoring
units" in the forestry administrations. In some cases, IFM has
earned money for these governments by identifying violations which led to large fines against logging companies and
individuals breaching the law and forest management regulations.
3. Update IUCN Red List assessments
The approximately 10 Madagascar rosewood species listed
above have not had their official conservation status evaluated by the IUCN since 1998. At that time, all were threatened except for D. mollis. Five of the ten were already classified as ‘endangered’ then. Given the extreme logging since
that time, it is likely that their Red List categories should be
reassessed (IUCN, 2010).
4. UNESCO World Heritage Sites "in danger"
The majority of the illegally logged rosewood in Madagascar
comes from two UNESCO World Heritage Sites: Masoala
National Park and Marojejy National Park.Why have Masoala
and Marojejy not been placed on the World Heritage Sites
"In Danger" List? After all, 2010 is the United Nations "International Year of Biodiversity". Nine national parks and seven
other protected natural areas are currently on this danger
list, mainly for extensive anthropogenic disturbance such as
poaching, logging, and war. The extent of the logging damage
in Masoala National Park, in particular, over the past 5 years,
must rival that of some of the other national parks "in danger". Placing a site on the UNESCO "danger list" is not utter
de-listing. It is a reversible process meant to draw attention
to and attract possible resources which can alleviate the crisis. There are specific funds that can become available if a site
is placed on the danger list. One can only speculate that the
reasons for no change in status may well be political and
practical. Perhaps it complicates matters that eight national
parks (which include these two) comprise the single Atsinanana World Heritage Site Complex. Perhaps there are
fears of triggering an even greater loss of tourism. Whatever
the reasons may be, it is odd that UNESCO has not been
more vocal or active in its support of these two national
parks which are the biodiversity jewels of the Atsinanana
World Heritage Site Complex (IUCN, 2007).
5. DNA fingerprinting
DNA fingerprinting has recently been used on confiscated
ivory to determine which populations of African elephants
were slaughtered. Similar genetic techniques would be of
great assistance in determining which populations of Madagascar rosewood are being logged the most,and in identifying
species. DNA testing has already been used to track timber,
but not yet in Madagascar.One of the biggest methodological
challenges is extracting DNA from the heartwood of dead
tree trunks (e.g., rosewood stockpiles), which consist of
dead cells with partly degraded DNA. In living trees, it is a
routine process to obtain DNA from the cambium just beneath the bark or leaves or buds. Nevertheless, several new
techniques have successfully extracted DNA from dry wood
of ramin (Gonystylus spp.) and other woods including 1000
year old beech (Fagus spp.) (Nielson and Kjaer, 2008).
References and rosewood logging resources
Barrett, M.A.; Brown, J.L.; Morikawa, M.K.; Labat, J-N.; Yoder,
A.D. In press. CITES designation for endangered rosewood in Madagascar. Science.
Blundell, A.G. 2007. Implementing CITES regulations for timber. Ecological Applications 17: 323-330.
Bohannon, J. 2010. Madagascar’s forests get a reprieve – But
for how long? Science 328: 23-25.
Bollen, A. 2009. Eighth continent quarterly. The Newsletter
of the Madagascar Fauna Group.Autumn Issue.
Bosser, J.; Rabevohitra, R. 1996. Taxa et noms nouveaux dans
le genre Dalbergia (Papilionaceae) à Madagascar et aux
Comores. Bulletin du Museum national d'Histoire Naturelle, 4e sér., 18: 171-212.
Bosser,J.;Rabevohitra,R.2005.espèces nouvelles dans le genre Dalbergia (Fabaceae, Papilionoideae) à Madagascar.
Adansonia, Sér. 3, 27, 2: 209-216.
Botokely (Marc Clique).1902.Chronique commerciale,industrielle et agricole. Revue de Madagascar 4: 356-365.
Braun, D. 2009. Lemurs, rare forests, threatened by Madagascar
strife. NatGeo News Watch.
blogs.nationalgeographic.com/blogs/news/chiefeditor/
2009/03/lemurs-threatened-by-madagascar-strife.html.
Downloaded on 23 March 2009.
Braun, D. 2010. Conservationists applaud renewed ban on
Madagascar rosewood. NatGeo News Watch.
blogs.nationalgeographic.com/blogs/news/chiefeditor/2010/
03/madagascar-rosewood-ban-reaction.html. Downloaded on
31 March 2010.
Brown, K.A.; Gurevitch, J. 2004. Long-term impacts of logging
on forest diversity in Madagascar. Proceedings of the National Academy of Sciences 101: 6045-6049.
Butler, R. A. 2010. How to end Madagascar’s logging crisis.
news.mongabay.com/2010/0211-madagascar.html. Downloaded on 10 February 2010.
Cochrane,M.A.;Schulze,M.D.1998.Forest fires in the Brazilian Amazon. Conservation Biology 12: 948-950.
Cocks, T. 2005. Loggers cut madagascan rainforest with impunity. Reuters. July 4.
Débois, R. 2009. La fièvre de l’or rouge saigne la forêt malgache. Univers Maoré 13: 8-15.
Du Puy, D. J.; Labat, J.-N.; Rabevohitra, R.; Villiers, J.-F.; Bosser,
J.; Moat, J. 2002. The Leguminosae of Madagascar. Royal
Botanic Gardens, Kew, U.K.
Furones, L. 2006. Independent forest monitoring: Improving
forest governance and tackling illegal logging and corruption. Trócaire Development Review 135-148.
Gerety, R.M. 2010. Major international banks, shipping companies, and consumers play key role in Madagascar’s logging crisis.
news.mongabay.com/2009/1215-rowan_madagascar.html.
Downloaded on 16 December 2010.
Gill, C. 2010. Log Jam. Guitar Aficionado. Spring Issue.
Gillies, A.C.M. 1999. Genetic diversity in Mesoamerican populations of mahogany (Swietenia macrophylla), assessed
using RAPDs. Heredity 83: 722-732.
Global Witness and Environmental Investigation Agency.
2009.Investigation into the illegal felling,transport and export of precious wood in SAVA Region Madagascar. Unpublished report to the Government of Madagascar.
Page 6
www.illegal-logging.info/uploads/madagascarreportrevi
sedfinalen.pdf. Downloaded on 20 November 2010.
Irwin, M. T. 2006. Ecological impacts of forest fragmentation
on diademed sifakas (Propithecus diadema) at Tsinjoarivo,
Eastern Madagascar:Implications for conservation in fragmented landscapes. Ph.D. thesis, Stony Brook University,
New York, USA.
IUCN. 2007. World heritage nomination. IUCN technical
evaluation. Rainforests of the Atsinanana (Madagascar).
IUCN Evaluation Report. ID No. 1257.
IUCN. 2010. IUCN Red List of Threatened Species. Version
3.1. www.iucnredlist.org. Downloaded on 25 May 2010.
Keong, C.H. 2006. The role of CITES in combating illegal logging: Current and Potential. Traffic Online Report Series,
No. 13. www.illegal-logging.info/item_single. php? it_id=
504&it=document. Downloaded on 20 November 2010.
Kett, G. 2005. Checking the reserve. Monthly from Madagascar. March. Madagascar Fauna Group.
Labat, J.N.; Moat, J. 2003. Leguminosae (Fabaceae). Pp. 346373. In: S.M. Goodman; J.P. Benstead (eds.) The Natural
History of Madagascar. University of Chicago Press, Chicago, USA.
Michaels, S. 2009. Gibson guitars raided for alleged use of
smuggled wood. www.guardian.co.uk/music/2009/nov/
20/gibson-guitars-raided. Downloaded on 20 November
2009.
Nielsen, L.R.; KjFr, E.D. 2008. Tracing timber from forest to
consumer with DNA markers. Danish Ministry of the
Environment, Forest and Nature Agency.
www.skovognatur.dk/udgivelser. Electronic Publication.
Office of the United States Trade Representative. 2010. USChina trade facts. www.ustr.gov/countries-regions/china.
Downloaded on 23 May 23 2010.
Patel, E.R. 2007. Logging of rare rosewood and pallisandre
(Dalbergia spp.) within Marojejy National Park, Madagascar. Madagascar Conservation and Development 2(1):
11-16.
www.erikpatel.com/Logging_of_Rosewood_Patel_2007.pdf.
Electronic Publication.
Patel, E.R. In press. A tragedy with villains: Severe resurgence
of selective rosewood logging in Marojejy National Park
leads to temporary park closure. Lemur News.
Patel, E.R.;Rasarely,E.;Tegtmeter,R.;Furones,N.;Fritz-Vietta,
N.; Malan, S.; Waeber, P. In Prep. Beyond Ecological Monitoring: A proposal for "Independent Forest Monitoring"
in Madagascar. Madagascar Conservation and Development.
Randriamalala,H.;Liu,Z.In press.Bois de rose de Madagascar:
Entre democratie et protection. Madagascar Conservation and Development.
Ratsimbazafy, J. 2006. Diet composition, foraging, and feeding
behavior in relation to habitat disturbance: Implications
for the adaptability of ruffed lemurs (Varecia v. editorium)
in Manombo forest, Madagascar. Pp. 403-422. In L. Gould;
M.L.Sauther,(eds.) Lemurs:ecology and adaptation.Springer, New York.
Rubel, A.; Hatchwell, M.; Mackinnon, J.; Ketterer, P. 2003. Masoala–L’oeil de la Forêt. Zoo Zurich.
Schuurman, D.; Lowry, P.L. 2009. The Madagascar rosewood
massacre. Madagascar Conservation and Development
4(2): 98-102. www.mwc-info.net. Electronic Publication.
Schuurman,D.2009.Illegal logging of rosewood in the rainforests of northeast Madagascar. TRAFFIC Bulletin 22(2):
49.
Stasse, A. 2002. La Filière Bois de Rose. Région d’Antalaha –
Nord-est de Madagascar. Thèse de mastère non publiée,
Université de Montpellier, France.
Stephenson, P.J. 1993. The small mammal fauna of Reserve
Speciale d’Analamazaotra, Madagascar: The effects of
human disturbance on endemic species diversity. Biodiversity and Conservation 2: 603-615.
Wasser, S.; Poole, J.; Lee, P.; Lindsay, K.; Dobson, A.; Hart, J.;
Douglas-Hamilton, I.; Wittemyer, G.; Granli, P.; Morgan, B.;
Gunn,J.;Alberts,S.;Beyers,R.;Chiyo,P.;Croze,H.;Estes,R.;
Gobush,K.;Joram,P.;Kikoti,A.;Kingdon,J.;King,L.;Macdonald, D.; Moss, C.; Mutayoba, B.; Njumbi, S.; Omondi, P.;
Nowak, K. 2010. Elephants, ivory, and trade. Science 327
(5971): 1331-1332.
Lemur News Vol. 15, 2010
Wilmé,L.;Schuurman,D.;Lowry II,P.P.In Press.A forest counterpart fund:Madagascar’s wounded forests can erase the
debt owed to them while securing their future, with support from the citizens of Madagascar. Lemur News.
Wilmé, L.; Schuurman, D.; Lowry II, P.P.; Raven, P.H. 2009. Precious trees pay off – but who pays? Poster prepared for
the World Forestry Congress in Buenos Aires, Argentina.
www.mwc-info.net/en/services/Journal_PDF%27s/
Issue4-2/MCD_2009_vol4_iss2_rosewood_massacre_
Supplementary_Material.pdf. Downloaded on 23 October
2009.
Young, D. 2007. Independent forest monitoring: Seven years
on. International Forestry Review 9(1): 563-574.
Rosewood logging photos
Photographer Toby Smith:
www.telegraph.co.uk/culture/photography/7625511/
Madagascar-undercover-slideshow.html
Photographer Chris Maluszynsk:
www.photoshelter.com/c/moment/gallery/ Rosewood-loggingin-Madagasar-by-Chris- Maluszynski/ G0000JWMAJa78LJ0/
Rosewood logging films
Dan Rather Reports:Treasure Island.Episode 437.A detailed
investigation of the impact of the recent political crisis in
Madagascar on the unique biodiversity of this island continent. Filmed in high-definition, active rosewood logging
camps are shown. The impact of such habitat disturbance on
the silky sifaka and the World Heritage Sites of Marojejy NP
and Masoala NP are discussed. The debates surrounding the
Ambatovy nickel mine adjacent to Andasibe-Mantadia NP
are also discussed. The mine may be endangering one of the
rarest animals on earth, the greater bamboo lemur (Prolemur
simus) which is being protected there by the NGO Mitsinjo.
Aired on HD-NET cable television November 2009. Purchasable and downloadable on I-Tunes in the United States.
DVDs can be purchased online:
hdnet-store.stores.yahoo.net/danrare437.html
Sample Clip 1:
www.facebook.com/video/video.php?v= 600388589544
Sample Clip 2: www.youtube.com/watch?v= dEi-yRlJ-mk
Carte Blanche: Madagascar (Part 1 and Part 2). Two short
films examining illegal rosewood logging in Madagascar and
the impact on the critically endangered silky sifaka. They
were produced by Neil Shaw and commissioned and funded
by Carte Blanche which is one of the most respected television news programs in the Southern Hemisphere. Aired on
South African Television in April,2010,and streams freely online here:
Carte Blanche: Madagascar Part 1:
beta.mnet.co.za/carteblanche/Article.aspx?Id= 3919&ShowId=1
Carte Blanche: Madagascar Part 2:
beta.mnet.co.za/mnetvideo/browseVideo.aspx?vid=25570
506: Bois de Rose. A Documentary Film by Joseph Areddy.
2003. RSI, Comano/Signe, Genve/GAP, Antananarivo.
Rosewood logging videos
Madagascar Rainforest Massacre (English):
www.youtube.com/watch?v=FzWNPHBRrAc
Madagascar Rainforest Massacre (French):
www.youtube.com/watch?v=KtjmFWpGNKs&feature=related
Madagascar Rainforest Massacre (Malagasy):
www.youtube.com/watch?v=rHYYhhLHeQw&feature=related
Lemur News Vol. 15, 2010
Global Witness – Environmental Investigation Agency - Illegal logging in Madagascar – Part 1
www.youtube.com/watch?v=T1hPviSbRcU
Global Witness – Environmental Investigation Agency - Illegal logging in Madagascar – Part 2
www.youtube.com/watch?v=LBtsNBpWW0E
Global Witness – Environmental Investigation Agency - Illegal logging in Madagascar – Part 3
www.youtube.com/watch?v=payUUJed0dc
Global Witness – Environmental Investigation Agency - Illegal logging in Madagascar – Part 4
www.youtube.com/watch?v=lm6a6Hrat3o
Rosewood logging radio programs
BBC World Service – Africa. September 17, 2009.
www.bbc.co.uk/worldservice/africa/2009/09/090917_
madge_rosewood2.shtml
Ongoing threats to lemurs and their habitat inside the Sahamalaza - Iles Radama
National Park
Melanie Seiler1,2, Guy H. Randriatahina3, Christoph
Schwitzer1*
1Bristol Conservation and Science Foundation, Bristol Zoo
Gardens, Clifton, Bristol BS8 3HA, UK
2University of Bristol, School of Biological Sciences, Woodland Road, Bristol BS8 1UG, UK
3Association Européenne pour l’Etude et la Conservation
des Lémuriens (AEECL), Lot: IVH 169 N Ambohimanandray,
Ambohimanarina, Antananarivo 101, Madagascar
*Corresponding author: cschwitzer@bcsf.org.uk
The Sahamalaza - Iles Radama National Park,officially inaugurated in July 2007 and managed by Madagascar National
Parks (MNP), includes both marine and terrestrial ecosystems and is the first park that was created under the
"Programme Environnemental III" of the Malagasy government and the World Bank. In addition to the few remaining
forest fragments of the Southern Sambirano ecoregion, the
park is home to extensive mangrove forests, which harbour
their own highly endangered fauna, and also includes offshore coral reefs. In 2003, researchers from the Cologne
Zoo, funded by AEECL, undertook an expedition to Sahamalaza to explore the opportunities for the establishment of
a permanent field station in order to study and protect the
Critically Endangered blue-eyed black lemur (Eulemur flavifrons) and its habitat. In 2004 and 2005,the field station in the
Ankarafa Forest became reality (Schwitzer et al.,2006),and it
has since been used by both European and Malagasy scientists as a basis for research on E. flavifrons and other lemur
species, especially the Sahamalaza sportive lemur (Lepilemur
sahamalazensis) and the northern giant mouse lemur (Mirza
zaza), occurring on the Sahamalaza Peninsula (Schwitzer and
Randriatahina, 2009).
Sahamalaza - Iles Radama National Park lies within a transition zone between the Sambirano region in the north and
the western dry deciduous forest region in the south, harbouring semi-humid forests with tree heights of up to 30m
(Schwitzer et al.,2006).The forests include a mixture of plant
species typical of both domains (Birkinshaw, 2004), and the
remaining primary and secondary forest fragments vary in
their degree of degradation. There are no larger connected
areas of intact primary forest left on the Sahamalaza Penin-
Page 7
sula, and the remaining fragments all show some degree of
anthropogenic disturbance and/or edge effects (Schwitzer et
al., 2007). The forests and forest fragments are separated by
grass savannah and shrubs. Sahamalaza is the only protected
area that harbours the blue-eyed black lemur,the Sahamalaza
sportive lemur and the northern giant mouse lemur. Other
lemur species in the park include the aye-aye (Daubentonia
madagascariensis), the western bamboo lemur (Hapalemur
occidentalis),and an as yet unidentified species of dwarf lemur
(Cheirogaleus spec.).
The remaining forest of the Sahamalaza Peninsula and its
unique fauna are in grave danger of disappearing. The habitat
is already extremely degraded, nonetheless bush fires and
tree-felling are activities that are routinely pursued and accepted within the local society (Ruperti et al., 2008). During
the first field season of a study on the impact of habitat degradation and fragmentation on the ecology and behaviour of
the Sahamalaza Peninsula sportive lemur (Lepilemur sahamalazensis), conducted by MS in 2009, local people from the
villages surrounding the protected area were found logging
trees in the already small forest fragments almost on a daily
basis. Logging activities mainly occurred in forest fragments
where no researchers had been present in previous years.
During walks through different forest fragments, in addition
to large numbers of logged trees, two places where trees
were processed for further use were found. Trees were
felled mainly in the early morning hours, on the one hand because of the high temperatures later in the day, on the other
hand probably because of the assumption that the researchers started observing animals later in the day and therefore
would not realise the illegal logging activities. Nonetheless,
trees were sometimes also felled in the afternoons. Because
locals immediately fled when becoming aware of researchers’ presence, we believe that the presence of researchers
and/or field guides, park authorities or park rangers is a crucial factor in stopping illegal logging in the remaining fragments. For the next field season (2010) we therefore plan to
expand the observations of Lepilemur to other, not yet used
forest fragments to help prevent their destruction. Of
course this cannot be a long-term solution to this problem.
The presence of park rangers and further environmental education of the local people will thus be extremely important
to save the Sahamalaza forests from further degradation.
About five times between August and October 2009, fires
occurred near the Ankarafa field station, three times in the
savannah and twice in the forest itself. After having extinFig. 1: Lepilemur sahamalazensis
poached
and roasted by locals in
Sahamalaza - Iles Radama National Park“.
Page 8
guished these fires it became obvious that they had all
started right beside the fire breaks that are frequently used
as paths by people on their way between villages. The Ankarafa field guides, all of them locals from the surrounding villages, assumed that the fires were set by villagers to show
their dissatisfaction with the recently established national
park that prohibits the use of the forests for collecting building material for their dwellings. As we followed the smoke
that was coming from another fire, we found an area inside
one of the core zones of the national park that was inhabited
by a young couple. They harvested a rice field and regularly
burned undergrowth around it. Additionally, they kept cattle
and goats and had built 2 houses at this site,one for the cattle
and one for themselves. As we talked to them, they claimed
that they were allowed to stay on this site and that MNP had
sold this part of the forest to them.They affirmed that,if they
set fire on this site, they would keep an eye on it and would
prevent the fire from expanding into the forest. Unfortunately this was not the case, however, as we later observed a
fire around this site without anyone near it. Overall, it
seemed that there were various people living inside the national park on permits given to them by what they claimed to
have been MNP agents;we were told that there was a map of
the park showing all the "excluded" areas available for housing and agriculture, which could be seen in the village of
Marovato. If that was indeed the case (we did not have the
opportunity to verify the information), it would be a massive
problem for protecting Sahamalaza’s unique wildlife and forests. If people claiming to be MNP staff illegally sold permits
for activities inside the national park, the destruction of the
small forest fragments will continue rapidly.
Another big problem comes with cattle; every day zebu cattle were observed in all forest fragments and on the savannah
in Ankarafa, as people from nearby villages let their cattle
roam freely.The abundance of zebu themselves and their excrements indicated that they frequently used the forest fragments as grazing grounds, especially those with remaining
primary forest parts. When zebu were grazing in the forest
rather than on the savannah, their movements were accompanied by crashing and breaking sounds; they were undoubtedly hindering the growth of many saplings,if not eating them.
This is an additional threat to the forest fragments, and furthermore, the abundance of the excrements of local zebu
has been found to negatively correlate with the density of L.
sahamalazensis (Ruperti, 2007). Additionally, the introduced
bush pig is responsible for considerable habitat destruction
due to digging up large areas, thus hindering the growth of
saplings. Unfortunately, the bush pig is reproducing wildly as
it is regarded as fady (taboo) by the local people and therefore not hunted.
Not only the activities of local people seem to be a threat to
the endangered wildlife on the Sahamalaza Peninsula. One of
the Ankarafa field guides encountered a foreigner,probably a
resident living in Madagascar (since he spoke Malagasy fluently), with a 4x4 car and two local guides about 1 km from
the researchers’ camp. These people had set up a tent and
told the Ankarafa field guide that they were visiting all villages
on the Sahamalaza Peninsula to look for fish. As we checked
their camp site the next day, the three men were gone, but
signs of a fire, logged branches and feathers of a harrier hawk
were found,indicating that they had caught and killed this endangered bird of prey. We wrote a report about this event
and handed it over, together with feathers of the bird, to
MNP in Maromandia. However, as long as there are no signs,
borders or fences indicating the national park area and its
restrictions, these problems will continue.
Lemur News Vol. 15, 2010
The ongoing political crisis is a further big concern that hinders the effective protection not only of the biodiversity of
the Sahamalaza Peninsula, but of Madagascar and its national
parks system as a whole. Only 10 years ago, Madagascar was
notorious for its environmental degradation and deforestation, but that began to change in 2003 when then President
Marc Ravalomanana, working with international conservation organizations and local groups, set aside 10 % of the
country’s surface area as national parks and started supporting ecotourism, which slowed deforestation and helped to
safeguard biodiversity.After the political events in early 2009
that saw the ousting of the President and the installation of a
transitional government, the majority of donor funds, which
provided half the government’s annual budget, have been
withdrawn, leading to major funding gaps that have affected
protected areas and their management. There currently is
almost no money to employ park rangers or to implement
other measures to protect the forests inside Madagascar’s
national parks, and forest degradation is going on without
noticeable resistance from the relevant authorities. Despite
the political crisis that affects most of the social and environmental activities of numerous NGOs, AEECL is still carrying
out its research activities and support to the villagers surrounding the Sahamalaza - Iles Radama National Park. Since
the establishment of the protected area in 2007, AEECL has
been conducting, besides its research programme, different
projects that aim to reduce the excessive environmental exploitation inside and around the park.As the major activity of
the local population surrounding the Sahamalaza Peninsula
National Park is rice-growing, every year AEECL organizes a
rice-growing training course and rice-growing competition,
using modern techniques in order to increase yield per ha
and to decrease the use of slash and burn agriculture.To stop
the ongoing overexploitation of the environment, environmental education is another important part of AEECL´s
work.As many villages in Sahamalaza are unable to pay teachers, AEECL subsidizes teachers’ salaries to ensure the primary education of the local children. Additionally, leaflets
about the Sahamalaza biodiversity and its importance are
distributed. They inform and educate villagers about the importance of lemurs and other species for their forest ecosystem. To minimise bush fires and to protect the forest against
uncontrolled fires, AEECL organizes firebreak programs
around the Ankarafa Forest, close to the research camp,
where during three days, hundreds of local people remove
the grasses on a 7m wide strip around the forest fragments.
Furthermore, several reforestation campaigns have been
conducted, where villagers, including many teachers and
their pupils, have planted trees around their villages with the
help of AEECL.
Because of all the factors described here, the protection of
Sahamalaza’s unique flora and fauna continues to be a major
challenge that has to be faced by the local human population
with the help of Madagascar National Parks and foreign partners. Two essential parts of AEECL’s efforts to help meeting
this challenge are to stimulate further scientific study of
endangered lemurs and other wildlife at its research station
in the Ankarafa Forest, especially by Malagasy students, and
to enable the local human population around the Sahamalaza
- Iles Radama National Park to sustainably use their natural
resources.
Acknowledgements
We would like to thank Madagascar National Parks (MNP),
especially the director of Sahamalaza - Iles Radama National
Park, M. ISAIA Raymond, for their continuing collaboration.
Page 9
Lemur News Vol. 15, 2010
Thank you also to the DGEF and CAFF/CORE for granting
us research permits for our work in Sahamalaza, and to Prof.
RABARIVOLA Clément for his ongoing help. Tantely Ralantoharijaona and Bronwen Daniel,along with all Ankarafa field
guides, contributed substantially to fighting forest fires and
other environmental threats in Ankarafa in 2009. MS was
funded by Bristol Conservation and Science Foundation,
AEECL, Conservation International Primate Action Fund,
Margot Marsh Biodiversity Foundation, Mohamed bin Zayed
Species Conservation Fund, International Primatological Society and Christian-Vogel-Fonds.
References
Birkinshaw, C.R. 2004. Priority areas for plant conservation.
Ravintsara 2(1): 14-15.
Ruperti, F. 2007. Population density and habitat preferences
of the Sahamalaza sportive lemur (Lepilemur sahamalazensis) at the Ankarafa research site, NW Madagascar.
Unpublished MSc thesis, Oxford Brookes University, UK.
82 p.
Ruperti, F.; Smith, J.; Ratovonasy, L.; Thorn, J. 2008. Sahamalaza
Conservation Action Plan (SCAP).Unpublished report to
the Association Européenne pour l’Etude et la Conservation des Lémuriens (AEECL). 17 p.
Schwitzer, C.; Randriatahina, G.H. 2009. AEECL: Update on
activities. Lemur News 14: 11-12.
Schwitzer, N.; Randriatahina, G.H.; Kaumanns, W.; Hoffmeister, D.; Schwitzer, C. 2007. Habitat utilization of blue-eyed
black lemurs,Eulemur macaco flavifrons (Gray,1867),in primary and altered forest fragments. Primate Conservation
22: 79-87.
Schwitzer, C.; Schwitzer, N.; Randriatahina, G.H.; Rabarivola,
C.; Kaumanns, W. 2006. "Programme Sahamalaza": New
perspectives for the in situ and ex situ study and conservation of the blue-eyed black lemur (Eulemur macaco flavifrons) in a fragmented habitat.Pp.135-149.In:C.Schwitzer;
S.Brandt;O.Ramilijaona;M.Rakotomalala Razanahoera;D.
Ackermand; T. Razakamanana; J. U. Ganzhorn (eds.). Proceedings of the German-Malagasy Research Cooperation
in Life and Earth Sciences. Berlin: Concept Verlag.
News and Announcements
Madagascar conservationist wins international environmental prize
Mr Rabary Desiré has been awarded the 2010 Seacology
Prize (www.seacology.org/prize/index.htm) for his his tireless
efforts to further forest conservation in northeastern Madagascar. Mr Desiré will receive the US$10,000 Prize on October 7, 2010 at a ceremony in Berkeley, California.
Rabary Desiré is recognized by many as a major conservation leader in northeastern Madagascar, and is a highlysought-after research and eco-tourism guide. With the money he makes from guiding, he buys forested land in order to
protect it. Years of work have finally culminated in the establishment of his own small private nature reserve called
Antanetiambo (antanetiambo.marojejy.com/Intro_e.htm),
which means "on the high hill". It is perhaps the only reserve
in northern Madagascar that has been entirely created from
start to finish by a single local resident.
According to Mr Desiré, "I am very happy to receive this
award and I feel very lucky for myself and Madagascar. After
many years of hard work and political instability,finally we are
having some local conservation success. I plan to use these
funds for such projects as reforestation, developing tourist
Fig. 1: Rabary Desiré next to the sign for the Antanetiambo
Nature Reserve he created.
infrastructure and purchasing the land around Antanetiambo
Nature Reserve to increase the size of the reserve and the
amount of protected land in this region. This award will help
preserve the precious biodiversity and high endemism of
Madagascar,as well as fight the ongoing battle against massive
deforestation and possible extinction of many beloved species... Thanks Seacology for giving me this prize. The whole
region will never forget it."
Read the full press release:
www.seacology.org/news/display.cfm?id=4238
Célébration du quinzième anniversaire
du GERP (1994-2009)
Jonah Ratsimbazafy*, Rose Marie Randrianarison,
Muriel Nirina Maeder
GERP, 34, Cité des Professeurs, Antananarivo 101,
Madagascar
*Corresponding author: gerp@wanadoo.mg
Quinze ans se sont écoulés depuis la création, en 1994, de la
Société de Primatologie malgache ou Groupe d’Etude et de
Recherche sur les Primates de Madagascar (GERP). Elle fut
fondée par dix Primatologues dont le Professeur Berthe
Rakotosamimanana qui occupait à la fois le poste de Secrétaire Général du GERP et le Co-éditeur de la revue Lemur
News jusqu’à sa disparition en 2005. De son vivant, elle
désirait ardemment passer le flambeau au Docteur Jonah
Ratsimbazafy pour le poste de Secrétaire Général du GERP
qui, en 2006, a été mandaté à l’unanimité par les membres
nationaux et internationaux du GERP au titre de Leader du
GERP.
L’Association compte aujourd’hui 169 membres et 20 d’entre eux sont de nationalité étrangère. La multidisciplinarité
des membres du groupe (Primatologues, Anthropologues,
Paléontologues, Ornithologues, Herpétologues, Spécialistes
de Micromammifères et Mammifères, Parasitologistes, Botanistes, Géographes, Vétérinaires, Agro-forestiers, Biochimis-
Page 10
tes, Dessinateur, Financiers) apporte une importante potentialité dans l’accomplissement de la mission du GERP: transférer les compétences nécessaires à la préservation de la
biodiversité pour les générations futures. Par ailleurs, les actions du GERP comprennent également la formation des
pépinières de Primatologues, la mise en œuvre du plan de
conservation des lémuriens, la contribution à l’amélioration
des activités génératrices de revenu des communautés de
base liées à la conservation,sans oublier l’éducation environnementale de la population cible.
En 2007, l’attribution par le GERP du nom de Microcebus macarthurii à une nouvelle espèce découverte dans la forêt de
Makira représentait un témoignage de reconnaissance au
dévouement de la Fondation MacArthur. De plus, le GERP a
depuis 2008 officiellement été mandaté par le MEFT/DGEF/
DSAP comme Gestionnaire de la forêt de Maromizaha, pour
que cette dernière devienne une Nouvelle Aire Protégée
(NAP). Plus récemment encore, en février 2010, le prix "lifetime" décerné par l’IPS a été attribué à un membre scientifique du GERP en la personne du Docteur Alison Jolly.
A l’occasion de son quinzième anniversaire, le GERP aura
l’honneur d’organiser une conférence scientifique sur les
lémuriens, à Antananarivo en novembre 2010.
Conservation International’s Primate
Action Fund: Projects funded March 2009
to March 2010
Anthony Rylands
Conservation International, 2011 Crystal Drive, Suite 500,
Arlington, VA 22202, USA, a.rylands@conservation.org
Conservation International’s Primate Action Fund awards
small grants (up to $5,000) to support projects and initiatives
promoting the conservation of primates worldwide,focusing
on Critically Endangered and Endangered species in their
natural habitats (and most especially those included in the biennial listing of the World’s 25 Most Endangered Primates).
Projects should contribute to at least one of the following
themes: (1) enhancement of scientific understanding/knowledge of the target species/ecosystem; (2) improved protection of a key species, habitat, or a reserved area; (3) demonstration of economic benefits achieved through conservation of a species and its habitat,as compared to its loss;(4) increased public awareness or educational impact resulting
from the project in question; (5) improved local capacity to
carry out future conservation efforts through training or
practical experience obtained through project participation;
and (6) modification of inappropriate policies or legislation
that previously led to species or habitat decline. Awards are
given most frequently for population and distribution surveys, and ecological and behavioral studies pertinent to conservation initiatives for threatened species. Grants are also
given that support genetic and taxonomic studies, publications, workshops for action plans and suchlike, and primate
field courses. Some awards are given to help primate habitat-country primatologists attend the biennial congresses of
the International Primatological Society. The fund does not
support participation in academic courses.
The Primate Action Fund comes from an annual award to
Conservation International, Arlington, Virginia, USA, made
by the Margot Marsh Biodiversity Foundation. It is managed
jointly by Ms Ella Outlaw and Dr Anthony B. Rylands, both of
CI’s Office of the President. Guidelines for application can be
Lemur News Vol. 15, 2010
obtained by writing to Anthony Rylands (see Funding and
Training section in this issue).
Five grants were awarded to benefit lemur conservation in
the March 2009 – March 2010 funding cycle. They were as
follows: (1) Halting politically-induced deforestation in the
short term to preserve the unique primate community of
Tsinjoarivo, eastern central Madagascar–Mitchell T. Irwin,
Fanomezantsoa, Jean-Luc Raharison and Marina Blanco; (2)
Rapid survey and assessment of the northern sportive lemur,
Lepilemur septentrionalis, in the Sahafary Region, Madagascar–Edward Louis Jr, Jean
Ranaivoarisoa, John Zaonarivelo and Steig Johnson; (3) Support for the publication of the IUCN/SSC Primate Specialist
Group newsletter and journal Lemur News, volume 14–Jörg
U. Ganzhorn and Christoph Schwitzer; (4) Student training
course “Field Methods in the Study of Primate Behavior and
Ecology”, Kirindy forest, 2010–Melanie Dammhahn, Peter M.
Kappeler, Claudia Fichtel, Cornelia Kraus and Rodin Rasoloarison; and (5) Comparison of habitat requirements of the
Data Deficient northern giant mouse lemur (Mirza zaza) in
two differently degraded habitats, in Sahamalaza, northwestern Madagascar–Johanna Rode and Christoph Schwitzer.
International Technical Meeting on Prolemur simus, 26-28 January 2010, Antananarivo, Madagascar
The greater bamboo lemur Prolemur simus has long been considered to be one of the rarest primate species in the world.
Up to 2007 only 60 individuals were known from the wild,
and another 22 were in captivity (Wright et al.,2008;Primate
Conservation 23: 5-17). Once widespread across Madagascar, more recent confirmed sightings were exclusively from
south-eastern Madagascar, which led to the assumption that
the species was extinct on the rest of the island. In 2008,
Dolch et al. (Lemur News 13: 14-17) rediscovered P. simus in
the Torotorofotsy wetlands, north of the Mangoro River.
Since then, several extensive surveys have been conducted
north and south of the Mangoro, and evidence of greater
bamboo lemurs was found at several sites in the Ankeniheny-Zahamena Corridor, in the central region of the eastern rainforest (King and Chamberlan, 2010; Oryx 44: 167).
In the context of developing a conservation action plan for
the greater bamboo lemur, the Madagascar Fauna group organised, from 26-28 January 2010 at the motel d’Antananarivo, Anosy, an international technical meeting with the
theme "Conservation of the critically endangered greater
bamboo lemur Prolemur simus: What we know now, what we
need to know and potential conservation strategies".Several
members of the PSG contributed to this.
The objectives of the meeting were 1) to share information
about the current situation of the various groups/populations of Prolemur simus in the wild and in captivity; 2) to discuss the threats, the solutions and the conservation strategies for three groups - north of the Mangoro River (Torotorofotsy and the Ankeniheny-Zahamena corridor CAZ),
south of the Mangoro River (south-east and the FandrianaVondrozo corridor COFFAV), and in captivity (Madagascar
and Europe); and 3) to make a plan, short to long term, to
move towards a conservation action plan for the species.
With 28 participants,the meeting was well attended.Presentations were given by researchers studying P. simus in the wild
and in captivity, representatives from the Ambatovy, Madagascar National Parks, the University of Antananarivo and
Lemur News Vol. 15, 2010
conservation NGOs. While other potential P. simus sites still
need to be explored, results from the most recent surveys
suggest the total estimated size of the known population is
between 221-346 individuals. Another 20 individuals are
housed in one Malagasy (Parc Ivoloina Zoo) and several European zoos and and managed under the umbrella of an EEP.
The following recommendations for the conservation of P.
simus came out of the meeting:
· We need to achieve official/formal protection for all currently known P. simus habitat (using whatever status is appropriate to the site);
· Animals of the northern and southern populations (wild
or captive) should not be mixed until the taxonomic situation is clarified;
· Faecal samples should be collected from all sites using a
standard protocol (meeting participants agree to collaborate to achieve this);
· When animals are caught/immobilised the opportunity
should be used to maximise the collection of samples;
· Bamboo plot data should be collected from all sites using
a standard protocol (meeting participants agree to collaborate to achieve this);
· A health screening protocol should be applied whenever
the opportunity arises;
· Sites in the Ankeniheny-Zahamena Corridor (CAZ) recently shown to harbour P. simus should be evaluated by
2011 at the latest to assess population size;
· Maromiza and Lakato need to be evaluated for the presence of P. simus, and protected to ensure connectivity;
· We agree that assuring connectivity between Torotorofotsy and CAZ is a high priority,and that the area needs an
integrated conservation plan involving all stakeholders –
CI to drive the process under supervision of the AlaotraMangoro Forestry Commission;
· It is important to make P. simus a priority (conservation
target) for the CAZ;
· Improved communication using a mailing list will be established, the "Prolemur Conservation Working Group";
· There are other sites that need to be surveyed for P.simus
(a list of sites has already been identified);
· Maximising connectivity between P. simus sites is important;
· Local communities should be directly involved in P. simus
conservation wherever possible;
· In case of a crisis scenario involving potential translocation, a technical strategy is needed consistent with IUCN
guidelines;
· The EEP-Ivoloina exchange of P. simus is important to
strengthen the global captive population;
· For the time being, it is not recommended that additional
wild P. simus be added to the global captive programme,
except in emergency;
· In the case of emergency, we recommend that animals go
to PBZT if upgraded facilities have been installed; if not
then they should go to Ivoloina;
· Based on the development of the global captive programme, integrated (metapopulation) management of P. simus
should be considered;
· Another technical meeting should be held in January
2011.
The workshop was financially and technically supported by
the Madagascar Fauna Group with additional contributions
from Conservation International Madagascar.
Page 11
Lemur presentations at the 23rd Congress of the International Primatological
Society, Kyoto, Japan
Jonah Ratsimbazafy
GERP, 34, Cité des Professeurs, Antananarivo 101, Madagascar, gerp@wanadoo.mg
The 23rd Congress of the International Primatological Society (IPS) was held in Kyoto (Yoshida Main Campus), Japan on
12th-18th September, 2010. This congress brought together
more than 1,000 delegates from 56 countries. Twenty-eight
talks and three posters were presented on lemur studies
during that congress.
I am also pleased to share with you the good news that the
winner of the 2010 IPS Lifetime Award is Professor Alison
Jolly who is an active member of GERP (Groupe d’Etude et
de Recherche sur les Primates de Madagascar). The lemur
lady,Prof.Jolly,has devoted her life to the conservation of the
world’s primates. Education is one of the main activities that
she never stops to discuss, as she found that the only chance
to save the endangered lemurs of Madagascar is to provide
the Malagasy children with tools enabling them to learn and
love the creatures that exist in their backyards.
I hope that even more lemur researchers will present the
results of their work at the 24th IPS Congress in Mexico.
Short Communications
Preliminary conservation status assessment for the Data Deficient northern
giant mouse lemur Mirza zaza
Eva Johanna Rode1,2, K. Anne-Isola Nekaris2, Christoph Schwitzer1*
1Bristol Conservation and Science Foundation, c/o Bristol
Zoo Gardens, Clifton, Bristol BS8 3HA, UK
2Nocturnal Primate Research Group, School of Social Sciences and Law, Oxford Brookes University, OX3 0BP, UK
*Corresponding author: cschwitzer@bcsf.org.uk
Madagascar is one of the world’s most important biodiversity hotspots, underpinned by its large proportion of endemic species and high rates of deforestation.During the last
decade, species diversity of Madagascar’s endemic lemurs
has increased dramatically due to new discoveries and taxonomic revisions. This has resulted in the unusual situation of
45 % of all Malagasy primate species being Red-Listed as Data
Deficient (DD) by the IUCN. This is by far the highest such
figure for any primate habitat country (by comparison, 13 %
of all primates and 15 % of all mammals are Red-Listed as
DD). The lack of species-specific knowledge makes it impossible to design effective conservation measures targeting
these taxa. To help assign a conservation status to the DD
northern giant mouse lemur Mirza zaza, described in 2005
due to distinctive features in morphology, behaviour and
genetics (Kappeler et al., 2005; Primate Report, 71, 3-26), we
examined space requirements and group size of this small
nocturnal lemur species during a three-month study (MayJuly 2010) and extrapolated our results to the taxon’s area of
Page 12
occupancy in order to estimate the size of its remaining
population.
Mirza zaza lives in dry forests of north-western Madagascar,
one of the fastest declining habitats of the island, with a decrease in forest cover of 40 % from 1975 to 2000.The area of
occurrence of the species is limited by the Maeverano River
in the south and the Mahavavy River in the north. Combining
forest cover data collected by the Madagascar Vegetation
Mapping Project (www.vegmad.org) with data on group home
range size and group size calculated from our study and additional literature, we calculated minimum and maximum estimates of total remaining population size. Since data for the
Madagascar Vegetation Mapping Project were collected several years ago,we lowered the estimate of total available habitat according to the estimated annual rate of decline.Habitat
decline may have accelerated since the onset of the political
crisis in Madagascar in early 2009, which is not yet reflected
in our estimates. Since a previous survey failed to detect Mirza zaza in several regions within the species’ area of occurrence, we applied different estimates of the percentage of
suitable habitat actually inhabited by the species.Our calculations yielded the following estimates:
· Maximum estimate: The total area covered in dry forest
within the area of occupancy of M. zaza is approximately
1,650 km2. Assuming an occupancy of 80 %, group home
ranges of 2 ha and group size of 4 individuals there would
be max. 177,500 animals left in total.
· Minimum estimate: In order to reflect the long-term survival of the species in a very fragmented area, only fragments < 1 km2 and smaller fragments closer than 500 m to
other, larger fragments (total area: 955 km2) were considered.We chose 1 km2 to allow a minimum viable population of 250 animals. If only 30 % of the habitat is inhabited,
animals use group home ranges of 4 ha and live in groups
of on average 2.3 animals, this leads to an estimate of
16,500 individuals left.
Mirza zaza should be assessed as Vulnerable (VU B2ab) since
its area of occupancy in both estimates is lower than 2,000
km2. With several sites within the species’ distribution area
found to be unoccupied, the remaining habitat being extremely fragmented with the smallest fragments unsuitable
to support a viable population, and habitat vanishing quickly,
M. zaza may become Endangered (EN B2ab) in the near
future if its area of occupancy shrinks below 500 km2.
Our preliminary conservation status assessment used the
best available data for Mirza zaza. More accurate estimates
will be possible if more data become available, especially on
percentage of occupancy. This method might be applied to
other DD lemur species in order to gain initial assessments
of their conservation status.
Lemur News Vol. 15, 2010
2Field
Museum of Natural History, 1400 South Lake Shore
Drive, Chicago, Illinois 60605, USA, and Association Vahatra,
BP 3972, Antananarivo 101, Madagascar
*Corresponding author: sgoodman@vahatra.mg
Although a few decades ago the hairy-eared dwarf lemur
(Allocebus trichotis) was considered "unquestionably the rarest of surviving lemurs" (Tattersall,1982,p.131),more recent
field work has found this species to be widely distributed
across portions of the eastern humid forests of Madagascar
(e.g., Meier and Albignac, 1991; Rakotoarison, 1998; Schütz
and Goodman, 1998; Goodman and Raselimanana, 2002).
Since more than a decade, there have been numerous records of this species from the central portion of the eastern
humid forests, and information is now available on aspects of
its ecology and natural history (e.g. Rakotoarison et al., 1997;
Garbutt,2000;Biebouw,2009;Ralison,2010).Here we add an
additional record from the region of Lakato, an area from
where this species had not been previously recorded.
From 22-28 October 2010 we were part of a research group
that conducted a biological inventory of a forest block in the
Lakato area and in the southern portion of the ZahamenaAnkeniheny forest corridor. The specific study site was centered at the following locality,which served as the base camp
for all inventory activities: Province de Toamasina, AlaotraMangoro Region, 14.5 km SW of Andasibe (Périnet) village,
Ampasipotsy-Anivonimaro/Ambalafary Forest, 19°02’38"S,
48°20’55"E, 995 m elevation.
During a nocturnal survey on 28 October 2010, the first author observed and photographed an individual of A. trichotis.
The animal appeared not to be accompanied by any conspecifics. The distinctive ear-tufts, characteristic of Allocebus,
were clearly visible (Fig.1).The lemur was observed at 21h58
and for about five minutes. The site was in partially disturbed
lower montane forest, about 200 m away from the research
camp and within a few meters of the dirt road connecting the
RN 2 (connecting Antananarivo-Toamasina) and the village
of Lakato. The animal was not particularly active and rested
in the upper portion of a 4 m tall tree. As it was photographed, including the use of flash, the individual remained
largely stationary, until it finally turned and moved off into
another tree and into dense vegetation.
During the course of nocturnal observations of forest animals within the study site, this was the only observation of A.
trichotis. Each night numerous individuals of Microcebus cf.
An observation of the hairy-eared dwarf
lemur, Allocebus trichotis, in the Lakato
region, eastern Madagascar
Erwan Lagadec1, Steven M. Goodman2*
de Recherche et de Veille sur les maladies émergentes dans l’Océan Indien (CRVOI),GIP Cyclotron Réunion
Océan Indien, 2 rue Maxime Rivière, 97492 Sainte Clotilde,
Ile de la Réunion, France, and Centre National de la Recherche Scientifique, UMR5557 Ecologie Microbienne, Bât A.
Forel, 43 bd du 11 novembre 1918, 69622 Villeurbanne
CEDEX, France
1Centre
Fig. 1: Photo of Allocebus trichotis taken during the night of 28
October 2010 in a forest block approximately halfway between the turn-off of RN 2 and the village of Lakato. The
ear-tufts of this animal, diagnostic of this species, are readily
visible in the photo.
Lemur News Vol. 15, 2010
Page 13
lehilahytsara were observed in close proximity. Although A.
trichotis is now known to have a broad distribution across a
good portion of the eastern humid forests, from lowland to
montane forests (up to about 1,000 m), it occurs in low densities (Mittermeier et al., 2006).This factor might account for
its absence in other forested sites surveyed within the
Zahamena-Ankeniheny forest corridor (e.g., Schmid et al.,
1999; Randrianabinina and Rasoloharijaona, 2006). However,
continued surveying efforts at these sites will probably result
in the finding that it occurs across the forest corridor.
Acknowledgements
The survey of the Lakato region was financed by a grant from
the Volkswagen Foundation.We are grateful to the Département de Biologie Animale, Université d’Antananarivo and
the Direction du Système des Aires Protégées, Direction
Générale de l’Environnement et des Forêts for permits to
conduct this research.
References
Biebouw,K.2009.Home range size and use in Allocebus trichotis in Analamazaotra Special Reserve, central eastern Madagascar. Int. J. Primatol. 30: 367-386.
Garbutt, N. 2000. Brief observations of hairy-eared dwarf lemur (Allocebus trichotis) in Analamazaotra Special Reserve,
eastern Madagascar. Lemur News 6: 37.
Goodman, S.M.; Raselimanana, A.P. 2002. The occurrence of
Allocebus trichotis in the Parc National de Marojejy. Lemur
News 7: 21-22.
Meier, B.; Albignac, R. 1991. Rediscovery of Allocebus trichotis
Günther 1875 (Primates) in northeast Madagascar. Folia
Primatol. 56: 57-63.
Mittermeier, R.A.; Konstant, W.R.; Hawkins, A.F.A.; Louis, E.E.;
Langrand, O.; Ratsimbazafy, J.; Rasoloarison, R.M.; Ganzhorn, J.U.; Rajaobelina, S.; Tattersall, I.; Meyers, D.M. 2006.
Lemurs of Madagascar. Second edition. Conservation International, Washington, D.C.
Rakotoarison,N.1998.Recent discoveries of the hairy-eared
dwarf lemur (Allocebus trichotis). Lemur News 3: 21.
Rakotoarison, N.; Zimmermann, H.; Zimmermann, E. 1997.
First discovery of the hairy-eared dwarf lemur (Allocebus
trichotis) in a highland rain forest of Eastern Madagascar.
Folia Primatol. 68: 86-94.
Ralison,J.M.2010.The lemurs of the Ambatovy-Analamay region. Malagasy Nature 3: 178-191.
Randrianambinina, B.; Rasoloharijaona, S. 2006. Inventaires
des lémuriens nocturnes dans la forêt pluviale de Maromizaha (Est de Madagascar). Lemur News 11: 9-11.
Schmid,J.;Fietz,J.;Rakotobe,Z.L.R.1999.Lémuriens du corridor Mantadia-Zahamena, Madagascar. In: J. Schmid, L.E.
Alonso (eds.). Une évaluation biologique rapide du corridor Mantadia-Zahamena, Madagascar. Bulletin of Biological Assessment 32: 61-72.
Schütz, H; Goodman, S.M. 1998. Photographic evidence of Allocebus trichotis in the Reserve Speciale d’AnjanaharibeSud. Lemur News 3: 21-22.
Tattersall,I.1982.The primates of Madagascar.Columbia University Press, New York.
When big lemurs swallow up small ones:
Coquerel’s dwarf lemur as a predator of
grey mouse lemurs and endemic rodents
Schliehe-Diecks1,
Markolf2,
Susanne
Matthias
Elise
Huchard2*
1Courant Research Center "Evolution of Social Behavior",
Georg-August-University of Göttingen, Kellnerweg 6, 37077
Göttingen, Germany
2Abteilung Verhaltensökologie and Soziobiologie, Deutsches
Primatenzentrum,Kellnerweg 4,37077 Göttingen,Germany
*Corresponding author: ehuchard@gmail.com
Predation has probably played a major role in the evolutionary history of lemurs, and specifically affects small nocturnal
lemurs, which are heavily predated upon by a wide range of
vertebrates, including carnivores (e.g., viverrid or domestic
carnivores), birds (e.g. raptors, owls) or reptiles (e.g. Boidae)
(Goodman, 2003). In contrast, lemur predation by other lemur species appears exceptional and highly opportunistic,
with one observed case of predation of an infant Lemur catta
by Eulemur fulvus (Pitts, 1995). However, such events might
occur more regularly in other lemur species. Two indirect
lines of evidence suggest that Coquerel’s dwarf lemur (Mirza
coquereli) predates on closely related smaller mouse lemurs
(Microcebus sp.) (Kappeler and Rasoloarison, 2003). The first
report is based on events where the partially eaten carcass of
a gray mouse lemur (M. murinus) was found together with a
live M. coquereli in a trap (Goodman, 2003). The second observation consists of an experimental confrontation of M.
murinus with M. coquereli, both being kept in separate cages
that were temporarily placed next to each other. In most
experiments, mouse lemurs started alarm-calling at the
Coquerel’s dwarf lemur and moved around in their cage in an
agitated fashion (Fichtel, 2009). Here, we present the first direct evidence of predation by wild M. coquereli upon gray
mouse lemurs and endemic rodents (western tuft-tailed rats,
Elliurus myoxinus).
Study animals, study site and methods
Coquerel’s dwarf lemurs (300 g;mean home range size: 4 ha)
occur in the western lowland forests and gray mouse lemurs
(60 g;mean home range size: 1.5 ha) can be found in most remaining forests in southern and western Madagascar (Kappeler and Rasoloarison,2003;Rasoloarison et al., 2000). Both
species share several features.Both are nocturnal and omnivorous solitary foragers. They mainly feed on primary resources (fruits, gum, flowers, young leaves), insect secretions,
small invertebrates and occasionally vertebrates (chameleons and lizards). Their diet displays seasonal fluctuation, as
well as interspecific variation (Goodman, 1993, 2003), and
the Coquerel’s dwarf lemur is reported to be slightly more
carnivorous than the gray mouse lemur (Petter et al., 1977).
In captivity, both species have been observed eating young
rodents (Petter et al., 1977) although this has never been reported in the wild. Both species occur sympatrically in central western Madagascar with western tuft-tailed rats, a nocturnal, frugi- and granivorous and partially arboreal rodent
(average body mass: 66 g) (Carleton, 2003).
All following observations were made in the Forêt de
Kirindy, a 12,500 ha forestry concession of the C.N.F.E.R.E.F.
(formerly C.F.P.F.) Morondava. This dry deciduous forest is
situated 60 km northeast of Morondava (44°39´E, 20°03´S).
The predation of the western tufted-tail rat was witnessed
during a focal observation of a Coquerel’s dwarf lemur which
was equipped with a radio collar (Biotrack TW3). The observed mouse lemurs were similarly equipped with radio
collars (Holohil Systems Ltd., BD-2C, 1.8 g), permitting behavioural observations of focal animals.
Results and discussion
The first observation reports the predation of a western
tuft-tailed rat by an adult male M.coquereli in November 2006
(Fig. 1). The Coquerel’s dwarf lemur was found sitting on the
ground at 20h17, feeding on a tufted-tail rat, and changed its
position only to climb-up the vegetation from 1-3 m height
and to recover the carcass when it fell to the ground. It devoured the whole carcass, including (cracked) bones. After
finishing eating,the M.coquereli groomed its face and hands.
Page 14
The second observation
reports an unsuccessful
attack on an adult female
gray mouse lemur (55 g,
approx. age: 1 year and 9
months) by a Coquerel’s
dwarf lemur in October
2009.At 21h24,the mouse
lemur had been foraging
high up in the vegetation
(between 6 and 15 m) for
at least 10 minutes, licking
sugary insect secretions
off leaves, when a M.coquereli, adult size, was spotted
at the same height, about
10m from the focal subFig. 1: An adult Coquerel’s ject, slowly and silently
towards
the
dwarf lemur (Mirza coquereli) moving
in the Foret de Kirindy, Mada- mouse lemur. Marking
brief and frequent pauses
gascar.
in an apparently easy progression into the canopy, its whole attitude strongly recalled
the hunting cat, with a low head and a flexible body, apparently entirely focused on its prey. In less than 30 seconds, the
Mirza was within 5 m of the mouse lemur,who kept feeding in
the same location. While the Mirza approached within 2 m,
the mouse lemur suddenly disappeared in an eclipse, quickly
fleeing among the top and tiniest branches,and jumping from
one slim branch to the next. The Coquerel’s dwarf lemur did
not try to chase it.After 2 minutes out of sight,the mouse lemur was retrieved quietly feeding on tree exudates, 25 m
away from its previous localization in its fleeing direction,and
15 m away from a frequently used sleeping site. Less than 10
minutes later, the female was joined by a related female and
both entered the tree hole together (21h37).
Finally, an adult Coquerel’s dwarf lemur was observed feeding on a young male gray mouse lemur (body mass: 37 g;
approx. age: 2-3 months) in June 2010. The predation was recorded at 22h10,about two hours after behavioural data had
been collected from the predated mouse lemur, which at the
time showed no signs of injuries and displayed normal behaviour. The body of the gray mouse lemur was almost complete when the observer spotted the M. coquereli feeding on
it, suggesting that the mouse lemur was killed shortly before.
The Coquerel’s dwarf lemur was sitting with its prey in a tree
of about 10m height, which stood 25 m away from the position where the grey mouse lemur was last spotted alive. It
took about one hour to finish the entire carcass, interrupted
by occasional vigilance scans of the surroundings.
The frequency of such events is probably relatively low, and
all reported observations happened during, or at the end of,
the dry season in Kirindy. It is thus possible that predation
pressure by M. coquereli increases at times of food scarcity,
when alternative resources like fruits and invertebrates are
rare or absent. However, it is also important to note that
most observations took place during the dry season, when
vegetation density is low in this dry, deciduous forest. This
means that the timing of events reported here might simply
reflect study methods. Nevertheless, this suit of anecdotal
observations represents the first direct and unambiguous
evidence for predation by the Coquerel’s dwarf lemur upon
small nocturnal lemurs, as well as other mammals. Predation
among other primate species is relatively rare. So far, only
chimpanzees, orangutans, baboons, blue monkeys and capuchins have been observed preying upon other primates
(Fichtel, in press). Our report provides evidence for the first
Lemur News Vol. 15, 2010
case where a lemur species might commonly predate upon
other lemurs.
References
Carleton,M.D.2003.Eliurus,Tufted-tailed rats.Pp.1373-1380.
In: S. M. Goodman; J. Benstead (eds.). The Natural History
of Madagascar.The University of Chicago Press,Chicago.
Fichtel, C. 2009. Costs of alarm calling: lemur alarm calls
attract fossas. Lemur News 14: 53-54.
Fichtel,C.in press.Predation.In:J.Mitani:J.Call;P.M,Kappeler;
R.Palombit;J.B.Silk;(eds.) The Evolution of Primate Societies. The University of Chicago Press, Chicago.
Goodman, S.M.; O’Connor, S.; Langrand, O. 1993. A review of
predation on lemurs: implications for the evolution of
social behavior in small, nocturnal primates. Pp. 51-66. In:
P.M.Kappeler;J.U.Ganzhorn (eds.).Lemur social systems and
their ecological basis. Plenum Press, New York.
Goodman,S.M.2003.Predation on Lemurs. Pp 1221-1228.In:
S. M. Goodman: J. Benstead (eds.). The Natural History of
Madagascar. The University of Chicago Press, Chicago.
Kappeler,P.M.;Rasoloarison,R.M.2003.Microcebus,mouse lemurs, tsidy. Pp 1310-1315. In: S. M. Goodman: J. Benstead
(eds.). The Natural History of Madagascar. The University
of Chicago Press, Chicago.
Petter, J-J.; Albignac, R.; Rumpler, Y. 1977. Mammifères lémuriens (primates prosimiens). In: Faune de Madagascar,
Paris.
Pitts, A. 1995. Predation by Eulemur fulvus on an infant Lemur
Catta at Berenty, Madagascar. Folia Primatol. 65: 169-71.
Rasoloarison, R.M.; Goodman, S.; Ganzhorn, J.U. 2000. Taxonomic revision of mouse lemur (Microcebus) in the western portions of Madagascar.Int.J.Primatol.21:963-1019.
Collective mobbing of a boa by a group of
red-fronted lemurs (Eulemur fulvus rufus)
Lennart Pyritz1,2*, Tianasoa Andrianjanahary1
1Behavioral Ecology & Sociobiology Unit, German Primate
Center, Kellnerweg 4, 37077 Göttingen, Germany
2CRC "Evolution of Social Behavior", University of Göttingen, Germany
*Corresponding author: LennartPyritz@gmx.net
Key words: red-fronted lemurs, boa, predation, mobbing,
anti-predator behaviour
Introduction
Collective anti-predator behaviour is one of the principal advantages of group-living (for mammals, e.g., Janzen, 1970; van
Schaik, 1983). It can be broadly divided into two strategies
and tactics employed before and after predator encounters
(Caro, 2005; Rahlfs and Fichtel, 2010; Fichtel, in press). While
the former include predator-sensitive foraging and increased
vigilance, mobbing occurs in several mammal species after
detecting a predator (e.g., Tamura, 1989). Why animals
engage in mobbing and who benefits from it in which way
remains an unresolved question in animal behaviour (for
reviews see Curio et al., 1978; Shields, 1984). Until today,
published field observations of group-living lemurs mobbing
a predator are rare (summarised in Scheumann et al., 2007).
Regarding snakes, only three interactions have been described so far (Colquhoun,1993;Rakotondravony,1998;Burney, 2002). Here, we report a prolonged mobbing display
against a Madagascar ground boa (Acrantophis madagascariensis) by a group of red-fronted lemurs (Eulemur fulvus rufus)
in Kirindy Forest. Observations like this may help to elucidate fundamental mechanisms of collective anti-predator behaviour by contributing to a pool of data on mobbing by particular pairs of prey and predators.
Lemur News Vol. 15, 2010
Observations
The event was observed during regular behavioural observations of red-fronted lemurs in Kirindy Forest,60 km north of
Morondava. It was the only snake-lemur interaction observed during the entire study period from November 2007
to April 2010, in which four lemur groups were followed
daily by one or two observers, respectively (> 4,000 h of observation data). Red-fronted lemurs live in multi-male, multifemale groups of 5-12 individuals (Pereira and Kappeler,
1997;Wimmer and Kappeler,2002).The study group (B) that
encountered the boa included 9 individually marked animals
at the time (2 adult females, 5 adult males, 1 juvenile male, 1
male infant).
On March 1,2010,at 7.19 h,sudden alarm calls of several redfronted lemurs were heard in the study area known as CS7.
Six individuals (2 adult females, 2 adult males, 1 juvenile male,
1 male infant) could be identified after approaching the group
to within 10 m. Three of them (2 adult females, 1 adult male)
emitted "Woofs" and "Huvvs", vocalisations typically uttered
during predator encounters (Fichtel and Kappeler, 2002).
The 5 individuals surrounded an approximately 2 m long
Madagascar ground boa (Fig. 1) that was lying motionless on
the ground. The lemurs sat at a height of 1-2 m, each about
3 m away from the snake, wagging their tails vigorously, ex-
Fig. 1: Madagascar ground boa in Kirindy. (Photo: Lennart
Pyritz)
cept the infant that kept a distance of 5 m during the entire
event and did not display any vocalisations or tail-wagging.
During the next 4 min,one of the adult males approached the
front end of the boa twice, getting as close as 1-2 m. After 5
min, he left the scene. During this time, one of the adult females also approached the snake up to within 2 m.When the
male left,the second female started to quickly circuit the boa
for 4 min,maintaining a distance of 2-3 m.After 14 min of several approaches and continuous alarm calls by 3-5 individuals,
the boa moved for the first time,heading slowly away.The remaining adult male approached the moving snake also within
2 m; also at its front end. About 1 min later, the boa had
moved 15 m away, and the lemurs left in the opposite direction, still uttering grunts continuously. Once the boa was out
of sight, the mobbing stopped and the lemurs` behaviour returned to baseline levels.
Discussion
The mobbing reaction of the group was strong and prolonged and included most of the group members.This is similar to the behaviour of a black lemur (Eulemur macaco
macaco) group encountering a Madagascar boa at Ambato
Massif, where the group mobbed the snake for 15-20 min,
Page 15
and some individuals approached it as close as 1 m before
finally leaving the location (Colquhoun, 1993). It is also noteworthy that females and males mobbed and approached the
snake in equal measure as observed in a number of other
species (e.g., Tamura, 1989; Ferrari and Ferrari, 1990; Tello et
al., 2002). The infant maintained a larger distance to the boa
and did not engage in the mobbing displays, however. Similar
infant behaviour has also been reported for other primates
(e.g., Ferrari and Ferrari, 1990) and might be due to a higher
susceptibility to an attack due to smaller body size or a lack
of innate experience regarding predator encounters and
mobbing strategies (Curio et al., 1978; Fichtel, in press).
The strong mobbing reaction of the lemurs might be explained by the hunting strategy of the snake.Boas are ambush
hunters that usually abandon an attack as soon as they have
been detected (Montgomery and Rand, 1978; Slip and Shine,
1988). Therefore, it seems beneficial for prey animals to signal the ambush hunter quickly and distinctly that it has been
detected. As boas do not pursue their prey after an unsuccessful attack, it is also unsurprising that the lemurs’ behaviour returned to baseline levels of anxiety shortly after departing the site of the predator encounter. In contrast,
groups of red-fronted lemurs showed increased vigilance behaviour for at least 30-60 min after encountering a fossa
(Cryptoprocta ferox;pers. comm. Jean-Pierre Tolojanahary and
pers. observation by LP), which is probably due to the higher
agility and climbing abilities of the largest mammalian carnivore.Furthermore,fossas have been observed to hunt cooperatively and pursue prey up to 45 min (Lührs and Dammhahn, 2009).
There are no quantitative data on predation rates of lemurs
by snakes in Kirindy, only opportunistic observations (e.g.,
Schülke, 2001; Eberle and Kappeler, 2008) that are biased by
several factors, however. The low observation rate of boalemur interactions could be due to the reptiles` nocturnal
lifestyle (Raxworthy,2003),so that most of the attacks would
occur at night when no or only few observers are working in
the forest. Furthermore, boas at Kirindy are only active during the rainy season from January to April, when observations are often limited by dense foliage and frequent rainfalls.
Five of the six individuals taking part in the mobbing were related (1 adult female and her 4 offspring from the last 4
years), while it is currently unknown whether the second
adult male sired one of the two youngest group members.
However, due to the small number of detailed observations
of predator encounters it remains impossible to identify the
ultimate causes of collective mobbing (kin defence/parental
care, self-/group defence or cultural transmission of enemy
recognition; Curio et al., 1978) in this species for the time
being.
Acknowledgements
LP was supported financially by the Deutsche Forschungsgemeinschaft (DFG; KA 1082/16-1, FuE). We thank field assistant Jean-Pierre Tolojanahary for sharing his long-term observation experiences with us. We are also grateful to Peter
Kappeler, Claudia Fichtel and Moritz Rahlfs for constructive
and helpful comments on earlier drafts of the manuscript.
References
Burney, D.A. 2002. Sifaka predation by a large boa. Folia Primatologica 73: 144-145.
Caro, T. 2005. Antipredator defenses in birds and mammals.
The University of Chicago Press, Chicago, London.
Colquhoun, I.C. 1993. The socioecology of Eulemur macaco:
A preliminary report. Pp. 11-23. In: P.M. Kappeler; J.U.
Ganzhorn (eds.). Lemur social systems and their ecological basis. Plenum Press, New York and London.
Page 16
Curio, E.; Ernst, U.; Vieth, W. 1978. Cultural transmission of
enemy recognition: one function of mobbing. Science 202:
899-901.
Eberle, M.; Kappeler, P.M. 2008. Mutualism, reciprocity, or kin
selection? Cooperative rescue of a conspecific from a boa
in a nocturnal solitary forager the gray mouse lemur.
American Journal of Primatology 70: 410-414.
Ferrari, S.F.; Ferrari, M.A.L. 1990. Predator avoidance behaviour in the buffy-headed marmoset, Callithrix flaviceps.
Primates 31: 323-338.
Fichtel, C. In press. Predation on primates. In: J.C. Mitani; J.
Call; P. Kappeler;R. Palombit; J. Silk (eds.). The evolution of
primate societies. University of Chicago Press, Chicago.
Fichtel, C.; Kappeler, P.M. 2002. Anti-predator behaviour of
group-living Malagasy primates: mixed evidence for a
referential alarm call system. Behavioral Ecology and
Sociobiology 51: 262-275.
Janzen, D. 1970. Altruism by coatis in the face of predation by
boa constrictor. Journal of Mammalogy 51: 387-389.
Lührs, M.L.; Dammhahn, M. 2009. An unusual case of cooperative hunting in a solitary carnivore. Journal of Ethology
DOI: 10.1007/s10164-009-0190-8.
Montgomery, G.G.; Rand, A.S. 1978. Movements, body temperature and hunting strategy of a Boa constrictor. Copeia
3: 532-533.
Pereira, M.E.; Kappeler, P.M. 1997. Divergent system of agonistic behaviour in lemurid primates.Behavior 34:225-74.
Rahlfs, M.; Fichtel, C. 2010. Anti-predator behaviour in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Ethology 116: 429-439.
Rakotondravony, D.; Goodman, S.M.; Soarimalala, V. 1998.
Predation on Hapalemur griseus griseus by Boa manditra
(Boidae) in the Littoral Forest of Eastern Madagascar.
Folia Primatologica 69: 405-408.
Raxworthy, C.J. 2003. Boidae, Boas. Pp. 993–997. In: S.M.
Goodman; J.P. Benstead (eds.). The Natural History of
Madagascar. University of Chicago Press, Chicago.
Scheumann, M.; Rabesandratana, A.; Zimmermann, E. 2007.
Predation, communication, and cognition in lemurs. Pp.
100-126. In: S. Gursky; K.A.I. Nekaris (eds.). Primate antipredator strategies. Springer, New York.
Schülke, O. 2001. Social anti-predator behaviour in a nocturnal lemur. Folia Primatologica 72: 332-334.
Shields,W.1984.Barn swallow mobbing:self-defence,collateral kin defence, group defence, or parental care? Animal
Behaviour 32: 132-148.
Slip, D.; Shine, R. 1988. Feeding habits of the diamond python,
Morelia s. spilota: ambush predation by a Boid snake. Journal of Herpetology 22: 323-330.
Tamura, N. 1989. Snake-directed mobbing by the Formosan
squirrel Callosciurus erythraeus thaiwanensis. Behavioral
Ecology and Sociobiology 24: 175-180.
Tello, N.S.; Huck, M.; Heymann, E.W. 2002. Boa constrictor attack and successful group defence in moustached tamarins, Saguinus mystax. Folia Primatologica 73: 146-148.
Van Schaik, C. 1983. Why are diurnal primates living in
groups? Behaviour 88: 120-143.
Wimmer,B.;Kappeler,P.M.2002.The effects of sexual selection and life history on the genetic structure of redfronted
lemur, Eulemur fulvus rufus, groups. Animal Behaviour 64:
557-68.
Lemur News Vol. 15, 2010
ation, and cryptic movements to remain hidden from predators were considered anti-predator adaptations among
nocturnal primates while diurnal primates used large group
size to enhance their ability to detect and defend against
predators, give alarm calls to warn conspecifics of the presence of a predator, and flee from predators (Hill and Dunbar,
1998;Isbell,1994;Stanford,2002).As research into nocturnal
primate behavior expanded,results revealed that,like diurnal
primates, nocturnal primates display a range of anti-predator
behaviors upon encountering a predator (Fichtel, 2007).
Nocturnal primates vary in the type of response (mobbing,
alarm calling), height in the canopy, proximity to other
individuals, and vigilance levels in the presence of different
predators (Fichtel, 2007; Gursky, 2002, 2003, 2005, 2006;
Schuemann et al., 2007; Schulke, 2001). In particular, mobbing
behaviors are well- documented in tarsiers (Tarsius sp.),
mouse lemurs (Microcebus spp.), and fork-marked lemurs
(Phaner furcifer) (Gursky, 2007; Eberle and Kappeler, 2008;
Schulke, 2001). Mobbing includes close approach, touching,
sniffing, and pouncing on the predator (Gursky, 2007). Interspecies mobbing of a predator occurs as well. Fork-marked
lemurs and coquerel’s dwarf lemurs (Mirza coquereli) together mobbed a snake (Boa manditra) (Schulke, 2001).
Several hypotheses have been put forth to explain the evolution of mobbing behavior (Eberle and Kappeler, 2008): 1) byproduct mutualism in which individuals defend others in the
process of defending themselves, 2) reciprocity where animals obtain higher fitness by cooperating with others, and 3)
kin selection whereby animals cooperate when they share
common genes. A fourth hypothesis known as perception
advertisement was developed as an explanation for the
evolution of alarm calling and other mobbing behaviors in
birds (Curio et al., 1978; Zuberbuhler et al., 1999) but has
been extended to account for the presence of mobbing behaviors in primates (Gursky,2005).According to this hypothesis, alarm calling and mobbing are signals to the predator
that the element of surprise has been lost. Snakes, leopards,
and other animals that hunt by crypticity and rely on the element of surprise to capture prey are common recipients of
alarm calling and mobbing.Research on both diurnal and nocturnal primates suggests that alarm calling and mobbing by
these primates results in predators leaving an area (Zuberbuhler et al.,1999;Gursky,2006).Here I report the divergent
responses of two species of nocturnal primates (Microcebus
murinus and Lepilemur leucopus) to the same potential predator- a nocturnal boiidae snake (Sanzinia madagascariensis)
and discuss implications for the above hypotheses based on
these observations.
Krista Fish
Department of Anthropology, The Colorado College, 14 E
Cache La Poudre, Colorado Springs, CO 80903, USA,
krista.fish@coloradocollege.edu
Methods
The observations reported here were made in the Ankoba
gallery forest of Berenty Private Reserve in southern Madagascar. The encounters between the snake and primates
were observed in the course of a six month study investigating the ecology of Microcebus murinus. During this study,
trails within the reserve were walked to locate unhabituated
mouse lemurs.When encountered,the time at which the encounter began, height, location, and activity of the mouse lemur were recorded continuously until the mouse lemur was
out of sight for more than five minutes. The time, height, and
activity of potential predators were also noted when they
were encountered, but predators were not followed unless
they were within proximity to a primate.
Primates display an array of responses to predators, and
differences in these responses were once thought to exist
based on activity pattern. Solitary foraging, cryptic color-
Results
While conducting walks to locate mouse lemurs in May 2009,
a sportive lemur alarm call at 20:52 alerted me to the pres-
Response of two nocturnal lemurs (Microcebus murinus and Lepilemur leucopus)
to a potential boiidae (Sanzinia madagascariensis) predator
Lemur News Vol. 15, 2010
ence of a boiidae snake later identified as Sanzinia madagascariensis. I saw two white-footed sportive lemurs (Lepilemur leucopus),one located at 4m height and the other at 5m
height in a tree over the trail.The sportive lemurs were barking and looking at the snake. The snake was moving at
approximately 4 m high in a tree and was attempting to cross
a gap and move into a tree nearer to the tree in which the
sportive lemurs were located. The attempt was unsuccessful
as the snake slipped and almost fell out of the thin, terminal
branches. The snake then moved down to 3.5 m height and
began crossing the canopy gap along thicker branches. The
sportive lemurs continued to alarm bark at the snake until
21:02 when the snake turned away from the gap in the
canopy and began moving lower down in the tree and away
from the sportive lemurs. The sportive lemur alarm calling
ended by 21:04 when the snake had traveled down the tree
trunk to 3m in height. The sportive lemur lowest in the tree
continued to watch the snake while the other sportive lemur
moved to 8m height in its tree and began feeding.
At 21:15, I was preparing to leave the area when I noticed a
mouse lemur at 0.5 m in the same tree as the snake. The
snake was at 3 m height in the tree and moving down the
main trunk of the tree. The mouse lemur looked at me as it
walked up the main trunk of the tree in the direction of the
snake. The snake faced the mouse lemur, but the mouse
lemur did not appear to notice the snake as it alternated
looking in my direction with looking around its immediate
area while foraging for insects. The mouse lemur continued
to move up the tree until it was within 0.25 m of the snake
where it paused and looked intently at the spot where the
snake was located and then jumped backwards away from
the snake. The mouse lemur then began moving around the
tree at the same height (3 m) as the snake, jumping to terminal branches, and running along main branches while pausing
to look at the snake. The mouse lemur’s movements took it
from 1m to only a few cms in distance from the snake. The
mouse lemur continued this pattern of running and pausing
to examine the snake for 7 mins. The mouse lemur then began foraging for insects in a neighboring tree at 3-4 m height
and within 1-2 m of the snake. While foraging, the mouse
lemur would pause to look in the direction of the snake
which remained motionless.The mouse lemur foraged in this
manner for 4 mins until a sportive lemur alarm called. Prior
to the alarm call, the mouse lemur was foraging approximately 1m from the snake and the snake began moving down
the tree trunk. At the sound of the sportive lemur alarm call,
the mouse lemur jumped to 2 m distance from the snake and
paused in its foraging to watch the snake. The snake remained motionless.A minute later the sportive lemurs alarm
called again. The snake began moving down the trunk of the
tree again and the mouse lemur moved to forage insects in
trees that were approximately 3-5 m from the snake and at
5m height. After 5 mins of foraging at this increased distance
from the snake, the mouse lemur moved back into the tree
where it was initially observed and foraged within 1m of the
snake for 2 mins. The mouse lemur then moved close to the
snake coming within less than 1m of the boa and running and
jumping around the snake while pausing to watch it while
standing bipedally. After 3 mins of remaining motionless
while the mouse lemur ran, jumped and watched the snake,
the snake began moving back up into the dense crown of the
tree. The mouse lemur continued running and jumping
around the snake and watching it at a distance of 0,5-1 m
away as the snake moved into the crown of the tree. 8 mins
later, the mouse lemur began foraging insects at 3-4 m height
in the canopy and within 0,5-1 m from the snake with occasional glances in the direction of the snake.The mouse lemur
Page 17
then moved further away from the snake and foraged insects
at 5m in height and approximately 5 m distance from the
snake.At 21:46 the mouse lemur was out of sight and did not
return by 21:51 when I left and continued the mouse lemur
walk.A return visit to the location at 10:05 for species identification of the species revealed the presence of no mouse lemurs or Lepilemur in the vicinity.
Discussion
Eberle and Kappeler (2008) describe the successful mobbing
of a Sanzinia madagascariensis by two female and one male
mouse lemur (Microcebus murinus). The mobbing caused the
snake to release a captured male mouse lemur. Subsequent
genetic analysis revealed that the mobbing females were related to the attempted victim (Eberle and Kappeler, 2008).
Additional encounters between mouse lemurs and snakes
without captured prey did not elicit mobbing behaviors from
the mouse lemurs (Eberle and Kappeler, 2008). Instead, the
mouse lemurs sat approximately 2 m from the snake and
watched it. (Eberle and Kappeler, 2008). The mobbing of the
snake by relatives of a captured mouse lemur and the lack of
mobbing behaviors by solitary mouse lemurs in Eberle and
Kappeler’s study support the kin selection hypothesis for the
evolution of mobbing behaviors. However, the solitary
mouse lemur observed in this study displayed mobbing-like
behaviors in the absence of kin or other individuals. Additionally, under experimental conditions, solitary mouse lemurs monitored model snakes and even locomoted towards
the model predators (Rahlfs and Fichtel,2010).The presence
of mobbing-like behaviors in solitary animals lends support
to the by-product mutualism hypothesis. Mouse lemurs may
display mobbing-like behaviors as an individual strategy and
then when larger numbers of mouse lemurs contact a predator, the appearance of a group-defense strategy may result
from multiple individuals pursuing the same strategy.
The observations here also lend support to the perception
advertisement hypothesis. The mouse lemur may have benefited by displaying mobbing behaviors toward the snake to let
the snake know that it was being monitored and would not
surprise the lone mouse lemur as it foraged. However, a prediction of the perception-advertisement hypothesis is that
cryptic predators should flee when faced with alarm calls and
mobbing as they cannot surprise prey in their vicinity. The
alarm calling by the sportive lemurs and the mobbing-like
behaviors of the mouse lemur observed in this study did not
cause the snake to flee. Instead, the snake remained in the
area while both the sportive lemurs and mouse lemur left
the area. Size of the mobbing and alarm-calling group may be
important. Tarsiers were more likely to retreat first if their
mobbing group consisted of four or fewer individuals (Gursky,2007).The small group sizes here may have not caused the
predator to flee,but may have served as an adequate warning
that it had lost the element of surprise and should not
expend energy in an attack.
Of particular interest in these observations was the opportunity to view the responses of two different nocturnal primate species to the same predator. Such observations are
infrequent in the literature. Schulke (2001) observed Phaner
and dwarf lemur (Mirza coquereli) together mobbed Boa
manditra. In the case of the sportive and mouse lemurs,
neither showed the same behavioral response to the Sanzinia madagascariensis. The pair of Lepilemurs maintained a
larger distance between themselves and the snake than did
the mouse lemur. The mouse lemur did not vocalize in the
vicinity of the snake, however, the sportive lemurs vocalized
during their encounter with the snake.Mouse lemurs seldom
respond to predator models with alarm calls in experimental
Page 18
conditions (Rahlfs and Fichtel,2010).Nocturnal primates and
other mammals may not rely on alarm calls as an anti-predator strategy (Rahlfs and Fichtel, 2010) because early detection of predators at night is more difficult and solitary foraging may limit the usefulness of this strategy. The sportive
lemurs however did alarm call in the presence of the snake.
Alarm calls in nocturnal primates may function as a deterrent
to the predator or to recruit conspecifics in defense against
the predator (Rahlfs and Fichtel, 2010).The exact function of
the sportive lemur alarm calls in this study cannot be determined, but they do reveal a need for future studies to examine potential variation in alarm call behaviors between nocturnal species. Given variation in body size, diet, and sociality
in nocturnal primates, we might expect variation in antipredator behaviors such as alarm calling among nocturnal
species.
The possibility exists that the mouse lemur may have recognized the alarm calls of the sportive lemur because it increased its distance from the snake, ceased foraging, and
monitored the snake following an alarm call. Recognition of
the alarm calls of other species has been documented for
birds, small mammals, and primates including diurnal lemurs
(Fichtel,2004;Rainey et al.,2004;Shriner,1998).However,the
suggestion that mouse lemurs recognize sportive lemur
alarm calls needs to be further investigated with field experiments. The ability of nocturnal primate species to recognize
the alarm calls of other sympatric species would be beneficial
to animals that frequently forage away from conspecifics.
The few encounters documented between nocturnal primates and their predators describe a range of anti-predator
responses that vary depending on the type of predator,proximity of conspecifics,and available vegetative cover.Such flexibility is interesting because nocturnal primates- especially
mouse lemurs- are often used as living models for the ancestral primate. The anti-predator behaviors of nocturnal primates such as mouse lemurs may reflect the primitive
primate or even primitive mammal condition (Stanford,
2002). The range of anti-predator behavior described for
nocturnal primates in this and other studies implies that the
flexibility in anti-predator behaviors observed in primates
have a more ancient origin than originally suspected or that
mouse lemurs and sportive lemurs have developed divergent
anti-predator behaviors that may not have been present in
early mammals and primates. Wider use of experiments to
explore the differing conditions which elicit variable responses to predators within and between nocturnal species
will be necessary to develop a more complete understanding
of ancestral versus derived anti-predator behaviors. Additionally, comparative research exploring variation in antipredator behaviors in other nocturnal mammal species will
be needed.
Acknowledgements
I would like to thank Dr.Alison Jolly for her facilitation of this
research project and the de Heaulme family for their permission to work at Berenty and their support of the project.I am
grateful also to the staff of MICET (Madagascar Institut pour
la Conservations des Ecosystèmes Tropicaux) for their assistance in travel and obtaining research permits and visas.
Funding for this project was provided by Sigma Xi, The University of Colorado Museum, the University of Colorado
Graduate Student Grants, and the American Society of
Primatologists.
References
Curio,E.;Ernst,U.;Vieth,W.1978.The adaptive significance of
avian mobbing.II. Cultural transmission of enemy recogni-
Lemur News Vol. 15, 2010
tion in blackbirds: effectiveness and some constraints. Z.
Tierpsychol. 48: 184-202.
Eberle, M.; Kappeler, P.M. 2008. Mutualism, reciprocity, or kin
selection? Cooperative rescue of a conspecific from a boa
in a nocturnal solitary forager the gray mouse lemur.Am.J.
Primatol. 70: 410-414.
Fichtel, C. 2004. Reciprocal recognition of sifaka (Propithecus
verreauxi verreauxi) and redfronted lemur (Eulemur fulvus
rufus) alarm calls. Anim. Cogn. 7: 45-52.
Fichtel, C. 2007. Avoiding predators at night: antipredator
strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus). Am. J. Primatol. 69: 611-624.
Gursky, S. 2002. The behavioral ecology of the spectral tarsier, Tarsius specturn. Evol. Anth. 11: 226-234.
Gursky, S. 2003. Predation experiments on infant spectral
tarsiers (Tarsius spectrum) Folia. Primatol. 74: 272-284.
Gursky, S. 2005. Predator mobbing in Tarsius spectrum. Internat. J. Primatol. 26(1): 207-221.
Gursky, S. 2006. Function of snake mobbing in spectral tarsiers. Am. J. Phys. Anth. 129:601-608.
Gursky, S. 2007. The Spectral Tarsier. Upper Saddle River, NJ:
Pearson/Prentice Hall.
Hill, R.A.; Dunbar, R.I.M. 1998. An evaluation of the roles of
predation rate and predation risk as selective pressures
on primate grouping behavior.Behaviour 135(4):411-430.
Isbell, L.A. 1994. Predation in primates: ecological patterns
and evolutionary consequences. Evol. Anth. 3(2): 61-71.
Rahlfs, M.; Fichtel, C. 2010. Anti-predator behavior in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Ethology 116: 429-439.
Rainey HJ, Zuberbuhler K, Slater PJB. 2004. Hornbills can distinguish between primate alarm calls. Proc R Soc Lond B
271: 755-759.
Scheumann, M.; Rabesandratana, A.; Zimmermann, E. 2007.
Predation, communication, and cognition in lemurs. Pp.
100-126. In: S. Gursky; K.A.I Nekaris (eds.). Primate AntiPredator Strategies. Springer.
Schulke, O. 2001. Social anti-predator behaviour in a nocturnal lemur. Folia Primatol. 72: 332-334.
Shriner,W.M.1998.Yellow-bellied marmot and golden-mantled ground squirrel responses to heterospecific alarm
calls. Anim. Behav. 55: 529-536.
Stanford, C.B. 2002. Avoiding predators: expectations and
evidence in primate antipredator behavior. Int J Primatol
23(4): 741-757.
Zuberbuhler, K.; Jenny, D.; Bshary, R. 1999. The predator deterrence function of primate alarm calls. Ethology105:
477-490.
Effective predation defence in Cheirogaleus medius
Kathrin H. Dausmann
Animal Ecology & Conservation, Biocentre Grindel, University Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg,
Germany, kathrin.dausmann@uni-hamburg.de
Besides one’s own death, the predation of offspring is the
most severe loss of fitness possible. In species that invest significantly in their offspring it is therefore natural that this "expensive" offspring should be guarded to avoid predation.
Nonetheless, and particularly in small animals, it is uncertain
whether an adult can effectively defend its offspring when it
is attacked by a larger predator.
The fat-tailed dwarf lemur (Cheirogaleus medius) is a small
(130 g), strictly nocturnal primate that occurs in the dry,
deciduous woodlands of western Madagascar, and lives in
social monogamous small family groups consisting of a reproductive male-female pair and their offspring from one or
more breeding seasons. Males and females maintain lifelong
pair bonds and usually separate only when one partner dies
(Fietz, 1999; Müller, 1999; Fietz and Dausmann, 2003). The
Lemur News Vol. 15, 2010
diet of C.medius consists mainly of fruits and varying proportions of arthropods depending on the season (Fietz and
Ganzhorn, 1999). C. medius is unique among primates because it spends seven months hibernating during the cooler
dry-season of the southern winter (April to October), when
food and water availability are low (Petter, 1978; Hladik et al.,
1980; Dausmann et al., 2004). When resting during the day
and when hibernating, the dwarf lemurs occupy tree hollows
either alone or with members of the family group (Dausmann et al., 2005). In the wild, female C. medius usually give
birth to twins and in most cases reproduction only takes
place every second year (Fietz and Dausmann, 2006). C.
medius only reproduce after delayed emigration from their
family and successful occupation of their own territory (thus
in their third year at the earliest;Fietz et al.,2000).In addition,
their life span is restricted by their size and is usually
between 4 and 11 years for territory holders, and so opportunities to reproduce are limited (for most animals between
one and three). Therefore, every young is a costly and valuable investment. Avoiding predation of their young should
therefore be a critical part of parental care.
Predators of C. medius include raptors (Madagascar harrier
hawk Polyboroides radiatus, Madagascar buzzard Buteo brachypterus, Madagascar long-eared owl Asio madagascariensis),
mammals (Fossa Cryptoprocta ferox, Narrow-striped mongooses Mungodictis decemlineata), and snakes (Madagascar
Ground Boa Acrantophis madagascariensis, Madagascar Tree
Boa Sanzinia madagascariensis, Malagasy Cat-eyed Snake Madagascarophis colubrinus) (Dausmann, submitted). The choice
of an appropriately sized tree hollow in which to give birth
can reduce attacks from many of these predators with the
exception of snakes which are able to enter any hollow that
can be used by C. medius.
C. medius leave their tree hollows at sunset to forage alone
but both sexes defend their shared territory. After the birth
of their offspring, both parents take turns in guarding the
young in the tree hollow throughout the night, while the
other one forages. As the young get older, the proportion of
time that parents spend guarding them gradually declines
(Fietz and Dausmann, 2003). At the age of about two weeks,
both parents leave the hollow and return only occasionally.
During this time, the young are particularly vulnerable to
predation, since they are unguarded. Later, the young accompany the parents during their nightly excursions.
In this note, I want to describe evidence that adult C. medius
can repel larger predators and therefore guarding or at least
remaining within hearing range of the tree hollow is an effective measure against predation of their offspring. I report an
observation in which a snake (Madagascarophis colubrinus)
tried to attack two C. medius young within a tree hollow but
was successfully repelled by the mother.
Our observation occurred in the Kirindy C.F.P.F. forest, a dry
deciduous forest near the west coast of Madagascar (60 km
north east of Morondava) during a focal animal survey of a
female C. medius on January 31st. For a more detailed description of the area see Ganzhorn and Sorg (1996).
The female was a mother of two young aged two weeks. The
male of the pair was also being observed. The female left the
tree hollow after sunset at 18:57 hours and the male
followed at 19:01 hours.The two young were left alone in the
hollow within a dead tree (Malagasy name: Mapingo). The
entrance of the hollow was 3 m above ground. The female
started her regular patrol of the territory border, but suddenly abandoned the patrol at 19:29 hours when about 80 m
from the hollow. She returned quickly to the hollow in
almost a straight line.On approach to the hollow,it was clear
Page 19
that the two young who had been left alone within the
hollow were making loud and constant distress calls. On a
branch of the same tree at a height of about 1.5 m above
ground was a large M. colubrinus (> 1 m length) eying the
hollow. Even though this crepuscular or nocturnal snake is
mainly terrestrial, scansorial behaviour is possible. The female approached the snake to within a few centimetres and
actively attacked it, and the snake responded by striking
towards the female. Both the adult female and the juvenile C.
medius were loudly vocalizing constantly.After three min,the
female seized the tail of the snake with both hands and bit it
about 10 cm from the end. The snake tried to drop to the
ground, but remained dangling in the female’s teeth. After
10 s of wriggling and repeated attempts to strike the female
the snake fell to the ground and moved away quickly. The
female descended to about 1 m, observed the ground for a
few minutes and then spent 15 min agitatedly observing the
surroundings at a height of about 3 m and inspecting the tree
hollow containing the young,who were still loudly vocalizing.
For the next 3.5 hours the female was moving rapidly around
within the territory, which is very unusual for a C. medius,
frequently returning and checking the tree hollow with the
young.She finally carried leaves into a new tree hollow about
50 m away and separately carried both young to the new tree
hollow. She did not return to sleep in the original tree hole
for the next two months, even though it had been used
frequently prior to this encounter. It seems puzzling that the
male of the pair did not come to help during the attack.Since
the male was followed simultaneously we know that at the
time of the attack he was less than 20 m from the tree hollow,
and clearly within hearing range of the distress calls. He
returned about 30 min after the attack where he met the
female and groomed her while she and the young continued
making distress calls. Since reproduction in this species is a
fairly rare event even including extra pair copulations, the
possibility of siring offspring is restricted, and the male
should have been highly motivated to defend his young in
order to increase his fitness. Considering the high (obligate)
paternal investment in guarding the young and the life-long
pair bond, C. medius have a surprisingly high rate (ca 40 %) of
extra pair young (Fietz et al., 2000; Schwensow et al., 2007). It
is thought that the male cannot discriminate between intra
pair and extra pair young and therefore cares for any offspring of his pair-partner, so as not to jeopardize the survival
of his own young. Alternatively, paternal care of extra pair
young could be an indicator for male quality or simply a tactic
to maintain his bond with the female and so securing future
mating possibilities in such a long-lasting relationship (Fietz
and Dausmann, 2003). Genetic analyses showed that the
male ("social father") of our observation was indeed only the
genetic father of one offspring, but not the other (Schwensow et al., 2007). However, even if he was able to distinguish
kin from non-kin, he should still have defended the tree hollow in order to protect his one own offspring.Interestingly,in
the weeks before these observations, the male and the
female had always spent the daily resting period together in
the same tree hollow. However, the day after the predation
attempt they slept apart, the male in the old, and the female
together with the offspring in the new tree hollow. We
cannot judge whether the male was unable to find the female
in the new tree hollow, whether he chose to rest in the old
hollow,or was prevented from entering the new tree hollow.
Conclusion
Clearly,the surveillance of offspring either directly within the
tree hollow (additionally offering thermoregulatory advan-
Page 20
tages simultaneously; Fietz and Dausmann, 2003), or by staying within hearing range, does offer protection from attack
by at least some predators even in this small species of primate.
Acknowledgements
This study was carried out under the "Accord de Collaboration" between Madagascar National Parks (MNP, formerly
ANGAP), the University of Antananarivo and the University
of Hamburg. We thank MNP, Chantal Andrianarivo, Jocelyn
Rakotomala, Domoina Rakotomalala, the late Olga Ramilijaona and Daniel Rakotondravony for their collaboration and
support. We acknowledge the authorization and support of
this study by the Ministère de l’Environnement, des Eaux et
Forêts et du Tourisme, MNP and the University of Antananarivo.C.Thurner was an invaluable observation companion.
The study was financed by DFG (Ga 342/14) and DAAD.
References
Dausmann, K.H. submitted. Spoilt for choice – Choice of
hibernacula and its influence on predation and energy expenditure during hibernation in Cheirogaleus medius. In: J.
Masters; F. Génin (eds.). Leaping Ahead.
Dausmann, K.H.; Glos, J.; Ganzhorn, J.U.; Heldmaier, G. 2004.
Hibernation in a tropical primate. Nature 429: 825-826.
Dausmann, K.H.; Glos, J.; Ganzhorn, J.U.; Heldmaier, G. 2005.
Hibernation in the tropics:lessons from a primate.J Comp
Physiol B 175: 147-155.
Fietz, J. 1999. Monogamy as a rule rather than exception in
nocturnal lemurs: The case of the fat-tailed dwarf lemur,
Cheirogaleus medius. Ethology 105: 259-272.
Fietz,J.;Dausmann,K.H.2003.Costs and potential benefits of
parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatol 74: 246-258.
Fietz, J.; Dausmann, K.H. 2006. Big is beautiful: fat storage and
hibernation as a strategy to cope with marked seasonality
in the fat-tailed dwarf lemus (Cheirogaleus medius). Pp.
97-111. In: L. Gould; Sauther, M. L. (eds.). Lemurs: Ecology
and Adaptation. Springer, Berlin Heidelberg New York.
Fietz, J; Ganzhorn, J. U. 1999. Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat?
Oecologia 121: 157-164.
Fietz, J.; Zischler, H.; Schwiegk, C.; Tomiuk, J.; Dausmann, K.H.;
Ganzhorn, J. U. 2000. High rates of extra-pair young in the
pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49: 8-17.
Ganzhorn, J.U.; Sorg,J. P. 1996. Ecology and economy of a tropical dry forest in Madagascar. Primate Report 46-1, Göttingen.
Hladik, C.M.; Charles-Dominique, P.; Petter, J. J. 1980. Feeding
strategies of five nocturnal prosimians in the dry forest of
the west coast of Madagascar. Pp. 41-73. In: P. Charles-Dominique;H.M.Cooper;A.Hladik;C.M.Hladik;E.Pages;G.F.
Pariente;A.Petter-Rousseaux;J.J.Petter;A.Schilling (eds.).
Nocturnal Malagasy Primates: ecology, physiology and behaviour. Academic Press, New York.
Müller, A.E. 1999. Social organization of the fat-tailed dwarf
lemur (Cheirogaleus medius) in North-western Madagascar. Pp. 139-157. In: B. Rakotosamimanana; H. Rasaminanana; J.U. Ganzhorn; S.M. Goodman (eds.). New Directions
in Lemur Studies. Kluwer Academic/Plenum Publishers,
New York.
Petter, J.J. 1978. Ecological and physiological adaptations of
five sympatric nocturnal lemurs to seasonal variations in
food production. Pp. 211-223. In: D.J. Chivers; J. Herbert
(eds.). Recent Advances in Primatology. Academic Press,
New York.
Schwensow, N.; Fietz, J.; Dausmann, K.H.; Sommer, S. 2007.
Neutral versus adaptive variation in parasite resistance:
importance of MHC-supertypes in a free-ranging primate.
Heredity 99: 265-277.
Lemur News Vol. 15, 2010
Lepilemur feeding observations from
Northern Madagascar
Andrew J. Lowin
Society for Environmental Exploration / Frontier, 50-52
Rivington Street, London EC2A 3QP, United Kingdom,
research@frontier.ac.uk
Lepilemur ankaranensis is the most northerly distributed
member of the genus Lepilemur, with a range that extends
south from Montagne d’Ambre National Park (Mittermeier
et al.,2008).The behaviour and ecology of Lepilemur is poorly
understood (Ratsirarson et al.,1987);this report summarises
some preliminary observations of L. ankaranensis.
Observations took place in a forest fragment (09°23.6E,
46°07.3’S) 70km south of Antsiranana (Diego Suarez), near
the town of Anivorano, west of the Route Nationale 6. The
site is situated approximately 4 km south of the Mt. d’Ambre
Park limit (Fig. 1). The area is heavily degraded, with only
pockets of secondary dry deciduous forest remaining.
Fig. 1: Study site in northern Madagascar.
Casual feeding observations of L. ankaranensis took place
from August 2009 to March 2010 (excluding the month of
December). Observations were made in the first hour after
sun set, with animals located using a flashlight. They were
then followed,and any feeding bouts were recorded,with the
plant species and food item noted. During this time, 32 % of
all observations were of L. ankaranensis feeding on fruits,
whereas all other observations were of leaf feeding. Five
plant families were utilized for their fruits during the study:
Moraceae, Verbenaceae, Rubiaceae, Pittosporaceae, and one
that was not identified.
As Lepilemur are thought to be predominantly folivorous
(Ganzhorn et al., 2004; Thalmann and Ganzhorn, 2003), this
proportion of fruit consumption seems to be high as compared to other Lepilemur species. For example, Thalmann
(2001) found that during their study of L. edwardsi, only 0.3 %
of 229 feeding bouts were feeding on fruits.
Also during this study, L. ankaranensis was observed feeding
on fruits with both Eulemur coronatus and Eulemur sanfordi in
the same tree, also feeding on the same fruit, with no signs of
aggression shown between any of the animals. A second
study took place in June 2010, six dusk-till-dawn follows
were carried out on consecutive nights, for a total of 64.3
hours. Again, animals were located at dusk with a flashlight
and followed until they returned to their sleeping sites in the
Lemur News Vol. 15, 2010
morning.During this time,175 feeding observations were recorded,and no fruit was consumed.During this second study,
a focal animal was observed to be chased out of a feeding
tree by a female E. coronatus. The female E. coronatus then began eating the unripe fruits of the tree.It thus seems that during times of fruit abundance L. ankaranensis utilize fruits as a
food resource along with several other lemur species occurring in the area. However, when food resources were not
abundant in the dry season, only leaves were eaten and
interspecific competition appears to be higher.
On several occasions during this second study, leaf stems
were snapped from trees and white tree exudates were consumed. Latex exudates are thought to be a toxic defence
mechanism and therefore usually avoided by primates (Glander, 1994), but latex feeding by Colobus spp. has also been observed (Mckey, 1978). Other lemur species, such as Phaner
furcifer (Petter et al., 1975; Petter, 1978; Thalmann, 2006) and
Mirza coquereli (Hladik,1979),are also known to feed on tree
exudates. A review of the literature on exudate feeding in
primates by Coimbra-Filho and Mittermeier (1977) suggested that tree exudates, in addition to simple sugars, protein,
and minerals, may also provide a source of calcium. However,
the latter authors also suggested that for most primates
exudate feeding was rare and of little nutritional importance.
This short report highlighted some behaviors of Lepilemur
ankaranensis, a relatively poorly studied member of the Lepilemur genus. Further field work is required to examine in detail the previously discussed observations and to improve
our knowledge of this species.
References
Coimbra-Filho, A.F.; Mittermeier, R.A. 1977. Tree-gouging,
exudate-eating and the "short-tusked" condition in Callithrix and Cebuella. Pp. 105-115. In: D.G. Kleiman (ed.). The
Biology and Conservation of the Callitrichidae. Smithsonian Institution Press, Washington, D. C.
Ganzhorn, J.U.; Pietsch, T.; Fietz, J.; Gross, S.; Schmid, J; Steiner,
N. 2004. Selection of food and ranging behavior in a sexually monomorphic folivorous lemur: Lepilemur ruficaudatus. Journal of Zoology 263: 393-399.
Glander, K.E. 1994. Nonhuman primate self-medication with
wild plant foods. Pp. 239-256. In: N.L. Etkin (ed.). Eating on
the wild side: The Pharmacologic, Ecologic, and Social Implications of Using Nncultigens. University of Arizona
Press, Tuscon.
Hladik, C.M. 1979. Diet and ecology of prosimians. Pp. 307357. In: A. Doyle; R.D. Martin (eds.). The Study of Prosimian Behavior. Academic Press, New York and London.
Mckey,D.1978.Plant Chemical Defences and the Ranging Behaviour of Colobus Monkeys in African Rainforests. Ph.D.
thesis, University of Michigan, Ann Arbor.
Mittermeier,R.A.;Ganzhorn,J.U.;Konstant,W.R.;Glander,K.;
Tattersall, I.; Groves, C.P.; Rylands, A.B.; Hapke, A.; Ratsimbazafy, J.; Mayor, M.I.; Louis, E.E.; Rumpler, Y.; Schwitzer, C.;
Rasoloarison, R.M. 2008. Lemur diversity in Madagascar.
International Journal of Primatology 29: 1607-1656.
Petter, J.J. 1978. Ecological and physiological adaptations of
five sympatric nocturnal lemurs to seasonal variations in
food production. Pp. 211-223. In: D.J. Chivers; J. Herbert
(eds.). Recent Advances in Primatology, Vol. 1: Behavior.
Academic Press, New York and London.
Petter,J.J.;Schilling,A.;Pariente,G.1975.Observations on the
behavior and ecology of Phaner furcifer. Pp. 209-218. In: I.
Tattersall; R.W. Sussman (eds.). Lemur Biology. Plenum
Press, New York.
Ratsirarson, J.; Anderson, J.; Warter, S.; Rumpler, Y. 1987. Notes on the Distribution of Lepilemur septentrionalis and Lepilemur mustelinus in Northern Madagascar. Primates 28:
119-122.
Thalmann, U. 2001. Food resource characteristics in two
nocturnal lemurs with different social behavior: Avahi
occidentalis and Lepilemur edwardsi.International Journal of
Primatology 22: 287-324.
Page 21
Thalmann, U.; Ganzhorn, J.U. 2003. The Sportive Lemurs, genus Lepilemur.In:S.M.Goodman;J.Benstead (eds.).Natural
History of Madagascar. The University of Chicago Press,
Chicago.
Thalmann, U. 2006. Lemurs - Ambassadors for Madagascar.
Madagascar Conservation and Development 1: 4-8.
Hypotheses on ecological interactions
between the aye-aye (Daubentonia madagascariensis) and microhylid frogs of the
genus Platypelis in Tsaratanana bamboo
forest
Andolalao Rakotoarison1*, Solohery A. Rasamison1,
Emile Rajeriarison2,David R.Vieites3,Miguel Vences4
1Département de Biologie Animale, Université d’Antananarivo, BP 906, Antananarivo 101, Madagascar
2Research assistant, Ranomafana National Park, BP 2, Fivondronana, Ifanadiana, Ranomafana 312, Madagascar
3Museo Nacional de Ciencias Naturales-CSIC, C/José Gutiérrez Abascal 2, 28006 Madrid, Spain
4Zoological Institute, Technische Universität Braunschweig,
Spielmannstr. 8, 38106 Braunschweig, Germany
*Corresponding author: andomailaka@gmail.com
The aye-aye (Daubentonia madagascariensis) is the most distinctive of all lemurs. It is the only known living species of the
Daubentoniidae (Simon and Meyer, 2001). The hands of the
aye-aye are highly specialised, with long and slender third fingers that are used for precise grooming, mainly at face level,
to get food into the mouth with rapid movements, and to tap
on the bark of tree trunks to detect insect larvae or other
arthropods (Goix, 1993). When an aye-aye locates a cavity, it
will anchor the upper incisors into the wood and then gnaw
away at the wood with the lower incisors to make a pit
(Erickson, 1995a, 1994). This unique manner of foraging for
arthropods leaves traces of biting on the wood cover which
are often used to ascertain the presence of the species even
without an actual sighting (Duckworth,1993 and own observations of one of us, ER). During a recent herpetological inventory on the Tsaratanana massif in northern Madagascar,
we noticed bamboo holes that were possibly caused or enlarged by foraging aye-aye,and we observed frogs living inside
these cavities. Here we report these observations and posit
a number of hypotheses on the possible ecological interactions among these species, with the goal of stimulating further studies.
During a herpetological inventory in Tsaratanana (the highest mountain massif of Madagascar, which rises up to 2876 m
above sea level) one of us (AR) carried out an ecological
study on frogs of the genus Platypelis (Mycrohylidae: Cophylinae), from the 9th to the 22nd of June 2010. Specifically, we
worked in a mountain forest bordering the temporary pond
locally called Matsabory Maiky (S 14°09’04.09"- E 48°57’
26.06" – 2,066 m elevation) - corresponding to campsite 2 on
the trail from Mangindrano to the Maromokotro peak. The
observed Platypelis occupy a specific microhabitat: the species live and breed inside the bamboo internodes which contain water and are accessible through small external holes.
These frogs have endotrophic development: their non-feeding tadpoles develop inside the water retained in the tree
holes and bamboo internodes. Based on a comparison with
type material and DNA barcoding, we ascertained that the
encountered Platypelis belong to two species described from
Page 22
the Tsaratanana massif: P. tsaratananaensis (most common)
and the much larger P. alticola (more rare). Detailed data on
the ecology and reproductive biology of these frogs will be
published elsewhere. Approximately 754 bamboo trunks, at
five different study sites, were inspected around the campsite. These sites each had four plots of 10 x 10 m areas. Out
of the 754 trunks, we discovered in 162 of them, a total number of 204 internode segments; small rounded holes that
were most probably made by insects like Dinoderus minutus
(Delobel and Tran, 1993). According to these authors,
Dinoderus minutus deposit eggs in bamboo internodes in
which their larvae develop (Fig. 1d).
At one of the sites (ca. 600 m east of the pond), we discovered some bamboo stems with remarkably different kinds of
holes which allowed access to the hollow cavity of the
internodes. Parts of the bamboo had been damaged in an irregular way. This appeared similar to what has already been
described as typical damage caused by the gnawing activity of
the aye-aye, whereby a freshly ripped-back piece is still attached and solid (Duckworth, 1993) (Fig. 1a-b).
On 20 of the 281 bamboo trunks at this study site, we found
similar damages,with a total of 71 holes which were more or
less oval and measured 5.2-29.7 mm vertically and 1.58.2 mm horizontally. The diameter measurements of the
non-damaged bamboo trunks were 5.3-54.2 mm, and those
with holes were 5.3-48.9 mm. On several bamboo trunks we
observed such holes in various internodes (1-6 m above the
Fig. 1: Traces of animals on the trunks of bamboo at the study
site: (a) bamboo internode segment with an upper and a
lower node attributed to the aye-aye; (b) segments of two
bamboo trunks with a hole attributed to the aye-aye on the
right and bite traces on the left; (c) traces attributed to
aye-aye upper and lower incisors on a "virgin" bamboo trunk
segment; (d) typical regular-shaped hole in a bamboo segment attributed to insects.
Lemur News Vol. 15, 2010
Fig. 2: Animals observed within bamboo segments: (a) frogs:
various specimens of Platypelis tsaratananaensis in one segment; (b) spider; (c) myriapod; (d) insect (cockroach).
ground),and some internodes had an upper and a lower hole.
Most importantly for the hypotheses drawn below, on some
of the trunks without holes, we observed clear traces of
gnawing that probably represent the upper and lower incisors of the aye-aye (Fig. 1b). According to our observations,
80 % of all the holes found in the study site were caused by
the activity of insects, and 20 % by the aye-aye.
Bamboo internodes accessible by both kinds of holes were
populated by Platypelis frogs as well as a variety of insects,spiders and centipedes (Fig. 2). At the study site where the bite
traces ascribed to the aye-aye were discovered, the altogether 282 holes (putatively made by insects) contained: 61
Platypelis distributed in 24 different holes, 12 insects in 8 different holes, and 2 myriapods in 2 holes. In the 71 holes
ascribed to the activity of the aye-aye, we observed 30
Platypelis in 11 holes, 4 insects in 3 holes, and 0 centipedes.
Based on these observations, we posit the following (partly
alternative) hypotheses which require verification and further study:
(1) We are confident that the observed marks at one of our
study sites, similar to those noted by Duckworth (1993), are
indeed caused by the activity of the aye-aye. Fresh bamboo
stems are externally smooth and very strong, and it seems
unlikely that any other mammal or even a bird could cause
such damage. However, the possibility that these holes may
be made by rats (such as Rattus rattus (which we collected at
Matsobory Maiky), or Brachytarsomys) needs to be excluded
by direct observations.
(2) We assume that the aye-aye will typically search for bamboo internodes which already have small holes made by insects. This is because in such internodes there is a high likelihood of finding prey.In addition to insect larvae and other arthropods, tree-hole breeding frogs like Platypelis may also be
consumed. In areas with high bamboo density, these frogs
may constitute an import part of the aye-aye diet. If proven,
this fact - that aye-ayes may eat frogs in addition to invertebrates - would be an interesting discovery in terms of
Primatology.
(3) Alternatively, the aye-aye may also gnaw holes into previously untouched bamboo segments. The bite traces we en-
Lemur News Vol. 15, 2010
countered in such "virgin" internodes support this hypothesis. Reasons for this might either be a search for drinking water, or the search and detection of insect larvae which develop inside these internodes and which have not yet made a
hole to emerge.
(4) As a fourth and highly speculative hypothesis, the aye-aye
may gnaw holes into "virgin" bamboo segments (or increase
the size of pre-existing holes) as part of a long-term feeding
strategy in which such holes are produced to make the bamboo segment suitable for colonization by arthropods and
frogs. This would enable the aye-aye to "harvest" its food
during a subsequent visit to the site several days later. Obviously, such a foresighted feeding strategy in a basal primate
would be of extreme interest, but we are aware that alternative and more probable explanations exist.
Detailed testing of these hypotheses will require long-term
observations in an area of dense growth of large bamboo,
probably including the deployment of a large number of camera traps and possibly hair traps to obtain evidence of aye-aye
activity. Carrying out such studies at the site in Matsabory
Maiky is difficult. It should be noted that the Tsaratanana
massif is difficult to access. However, alternative sites, e.g. at
Marojejy (Duckworth, 1993) might contain a large population of Platypelis (albeit other species) as well, and could be
surveyed more systematically.
Acknowledgements
A warm thanks to the Directorate of Waters and Forests
and the Head of the Offices of Madagascar National Parks at
Mangindrano and Ambanja for the research permits on
Tsaratanana. We are also indebted to the many people who
have logistically assisted in our expedition, especially to the
local guides (Faly and Levaovao) from Mangindrano.
References
Delobel, A.; Tran, M. 1993. Les coléoptères des denrées alimentaires entreposées dans les regions chaudes. Faune
tropical XXXII: 98-99.
Duckworth, J.W. 1992. Feeding damage left in bamboos, probably by aye-ayes (Daubentonia madagascariensis). International Journal of Primatology 14: 927-931.
Erickson, C.J. 1994. Tap-scanning and extractive foraging in
aye-ayes, Daubentonia madagascariensis. Folia Primatologica 62: 125-135.
Erickson, C.J. 1995a. Feeding sites for extractive foraging by
the aye-aye,Daubentonia madagascariensis.American Journal of Primatology 35: 235-240.
Goix, E. 1993. L’utilisation de la main chez le aye-aye en captivité (Daubentonia madagascariensis) (Prosimiens, Daubentoniidés). Mammalia 57: 171-188.
Milliken, G.W.; Ward, J.P.; Erickson, C.J. 1991. Independent digit control in foraging by the aye-aye (Daubentonia madagascariensis). Folia Primatologica 56: 219-224.
Simon,E.L.;Meyer,D.,2001.Folklore and beliefs about the aye
aye (Daubentonia madagascarienis) Lemur News 6:11-16.
Discovery of crowned sifaka (Propithecus
coronatus) in Dabolava, Miandrivazo, Menabe Region
Josia Razafindramanana1*, Rija Rasamimanana2
d’Etude et de Recherche sur les Primates de Madagascar (GERP), Lot 34 Cité des Professeurs Fort Duchesne,
Ankatso, Antananarivo 101, Madagascar.
2Pan African Mining Madagascar (PAMM), Lot 137 II AN
Analamahitsy, Antananarivo 101, Madagascar.
*Corresponding author: r_josia@hotmail.com
1Groupe
Page 23
Key words: Propithecus coronatus, Dabolava, distribution,
lemurs, Indridae
The crowned sifaka Propithecus coronatus was until recently
regarded as one of four subspecies of P. verreauxi, family
Indridae, which occur throughout western and southern
Madagascar (Muller et al., 2000; Mittermeier et al., 1994; Tattersall, 1986; Wilmé and Callmander, 2006). Recent taxonomic revisions (Mittermeier et al., 2008) have promoted all
four subspecies to full species status (Mittermeier et al.,
2006). However, there is considerable debate about the validity of P. coronatus, and especially its relationship with P.
deckeni (Mittermeier et al.,2008),due to the physical similarities and close geographical distributions of these taxa,including apparent sympatry at some sites (e.g. Tattersall, 1986;
Curtis et al.,1998;Muller et al.,2000;Groves,2001;Thalmann
et al., 2002).
P. coronatus was previously assigned to the IUCN conservation rating "Critically Endangered",but has since been moved
into the "Endangered" category; nevertheless, the distribution range and the ecology of this species are not yet well
understood (IUCN, 2008). Crowned sifakas are diurnal, and
their habitat is characterised by dry deciduous forests and
mangroves (Petter and Andriatsarafara, 1987). They live in
groups of two to eight individuals, with home ranges from
1.2–1.5 ha.They feed mainly on buds,green fruits and mature
leaves (Muller,1997).It is known that they reproduce seasonally, with females giving birth every 2-3 years (Curtis et al.,
1998; Mittermeier et al., 2006). Compared to other lemurs,
their reproduction rate is very slow, making recovery of
small populations even more problematic.
The newly discovered crowned sifaka population is situated
at Amboloando (UTM WGS 84,N 7822351 E 580189) in the
Commune of Dabolava in central Madagascar,and is the most
southerly record of the species.Amboloando lies about 4 km
from Dabolava village, and 40 km to the southeast of Miandrivazo. Amboloando comprises 7 ha of dry semi-deciduous,
secondary forest that exhibits the characteristics of riverine
forests, consisting of deciduous as well as evergreen trees
such as Acacia sp.,Nastus sp.and Macaranga sp.The altitude is
about 600 m above sea level, and the area is characterized by
a clearly defined wet and dry season. The sifaka population is
composed of a single group, which constituted six adults and
one juvenile when first discovered in June 2009 (Razafindramanana, 2009). One of the adult males disappeared later in
the year, presumed dead, leaving six individuals remaining.
The animals appear to be classic P.coronatus (Fig.1),but some
individuals show pelage colour variation, with dark fur on
their back and arms (Fig. 2). Behavioural studies of the group
are underway,and a preliminary community-based conservation program has been established at the site, involving several organisations including GERP, The Aspinall Foundation,
SAHA and Pan-African Mining Madagascar. Forests in Amboloando and the surrounding area are heavily degraded. Different factors threaten the survival of this species in Madagascar: in contrast to the other sites such as Anjamena (Muller, 2000), hunting does not occur in Amboloando, partly due
to the sifaka being regarded as holy by the local people.
Therefore,other threats such as habitat destruction through
slash-and-burn agriculture to make way for pasture for livestock,charcoal production,and mining exploitation affect the
sifaka group.
Surveys in the vicinity of Dabolava suggest that this is the
only group of P. coronatus remaining in that area, despite local
people claiming that other groups were present between 5
and 10 years ago. Therefore, it appears that habitat destruc-
Page 24
Lemur News Vol. 15, 2010
The Mahajilo is a tributary of the Tsiribihina River, which is considered to
represent the north-western limit of P.
verreauxi (Mittermeier et al., 2006). P.
coronatus is therefore unlikely to be
found much further south or southwest than Dabolava. Only 80 km
south-west of Dabolava, a population
of P. verreauxi is known from Ambatolahy (SAHA, 2009), which lies within
the Ambararata/Londa protected area
complex (Fig. 3). Another tributary of
the Mahajilo, the Mania River, lies between Ambatolahy and Dabolava and
may therefore represent the distributional limit of P. coronatus and P. verreauxi in the south of Madagascar. A
conservation programme and restoration of the remaining habitat with
the local people are needed to save
this population of P. coronatus.
Fig.1:Crowned sifaka in the Amboloando
Forest (top).
Fig. 2: Crowned sifaka with dark colour
on its arms (right).
Acknowledgments
I thank GERP – Groupe d’Etude et de
Recherche sur les Primates de Madagascar, The Aspinall Foundation, Cotswold Wildlife Park, SECAS, Belfast
Zoo, Besancon Museum and Parc
Zoologique de Paris for funding this
research. Many thanks to Dr Jonah
Ratsimbazafy and Tony King for discussions about the project implementation.I am grateful for permission and
assistance in the field from the Direction Régionale de l’Environnement et
des Forêts and the Commune of
Dabolava.I also thank Pan African Mining Madagascar for providing accommodation in their lovely camp site.
Fig. 3: Map showing the area of discovery and survey in Dabolava.
tion for local livelihoods has resulted in the almost complete
extirpation of crowned sifaka in the area, probably due to a
combination of habitat loss and food scarcity.
Some studies describe the range of P.coronatus as broadly restricted to the region between the rivers Betsiboka and
Mahavavy (Muller et al., 2000; Wilmé and Callmander, 2006),
with a population density of 173 individuals/km² at Anjamena
(Muller, 2000). In an analysis of the distribution of lemurs in
central western Madagascar, Thalman and Rakotoarison
(1994) suggested that the faunal region bounded by the
Betsiboka, the central highlands, the river Tsiribihina and the
Mozambique Channel can be divided into four sub regions.
These sub regions are separated by the three rivers: Mahavavy, Manambaho and Manambolo, but are interconnected
with the Bongolava Massif.The discovery of a crowned sifaka
population in Dabolava, which is located in the south of the
central highlands sub region, confirms the hypothesis that
the historical range of this species might spread along the
central highlands of Madagascar. The record of a group of
crowned sifaka in Andranotonga, slightly north of the Mahajilo River, was cited by Tattersall (1986). The present report
appears to be the first location of P. coronatus to the south of
this river.
References
Curtis, D.J.; Velo, E.-O.; Raheliarisoa; Zaramody, A.; Muller, P.
1998. Surveys on Propithecus verreauxi deckeni, a melanistic
variant, and P.v. coronatus in Northwest Madagascar. Oryx
32: 157-163. Groves, C.P. 2001. Primate taxonomy. Smithsonian Institution Press, Washington, D.C.
Hawkins, A.F.A.;Durbin, J.C.;Reid, D.B. 1998.The primates of
the Baly Bay area, north-western Madagascar. Folia Primatologica 69: 337-345.
IUCN. 2008. 2008 IUCN Red list of threatned species.
www.iucnredlist.org.
Mittermeier, R.A.; Tattersall, I.; Konstant, W.R.; Meyers, D.M.;
Mast,R.1994.Lemurs of Madagascar.1st ed.Conservation
International, Washington, D.C.
Mittermeier, R.A.; Konstant, W.R.; Hawkins, F.; Louis E.E.;
Langrand, O.; Ratsimbazafy, J.; Rasoloarison, R.; Ganzhorn,
J.U.; Rajaobelina, S.; Tattersall, I.; Meyers, D.M. 2006.
Lemurs of Madagascar. 2nd ed. Conservation International, Washington, D.C.
Mittermeier,R.A.;Ganzhorn,J.U.;Konstant,W.R.;Glander,K.;
Tattersall, I.; Groves, C.P.; Rylands, A.B.; Hapke, A.; Ratsimbazafy, J.; Mayor, M.I.; Louis Jr., E.E.; Rumpler, Y.; Schwitzer,
C.; Rasoloarison, R.M. 2008. Lemur diversity in Madagascar. International Journal of Primatology 29 (6): 16071656.
Muller,P.1997.The behaviour and ecology of the crowned sifaka (Propithecus verreauxi coronatus) in north west Madagascar. Unpublished Ph.D. thesis, University of Zurich.
Lemur News Vol. 15, 2010
Muller,P.A.;Velo,E.-O.;Raheliarisoa;Zaramody A.;Curtis.D.J.
2000. Surveys of five sympatric lemurs at Anjamena,
northwest Madagascar. African Journal of Ecology 38:
248-257.
Petter, J.-J.; Andriatsarafara. F. 1987. Conservation Status and
distribution of lemurs in the west and northwest of Madagascar. Primate Conservation 8: 169-171.
Razafindramanana, J. 2009. Propithecus coronatus on the verge
of extinction: Help to save them: GERP, Antananarivo, Madagascar, 6.
SAHA. 2009. Crèation de Nouvelle Aire Protegee pour le
complexe Ambararata/Londa.
Tattersall,A.I.1986.Notes on the distribution and taxonomic
status of some species of Propithecus in Madagascar. Folia
Primatologica 46: 51-63.
Thalmann, U.; Rakotoarison, N. 1994. Distribution of lemurs
in central western Madagascar, with a regional distribution hypothesis. Folia Primatologica 63: 156-161.
Thalmann, U.; Kümmerli, R.; Zaramody, A. 2002. Why Propithecus verreauxi deckeni and P. v. coronatus are valid taxa –
quantitative and qualitative arguments. Lemur News 7:
11-16.
Wilme, L.; Callmander M.W. 2006. Les populations reliques
de primates: les Propithèques. Lemur News 11: 24-31.
Inferences about the distant past in Madagascar
Elwyn L. Simons
Duke Lemur Center, Division of Fossil Primates, Dept. Evol.
Anthropology, Duke University, 3705 Erwin Road, Durham,
NC 27705, USA, esimons@duke.edu
From Etienne de Flacourt (1658), the following is an English
translation, from the original French, of an entry in his book
"Histoire de la Grande Isle Madagascar:"
"Tretretretre or Tratratratra. It is a large animal like a calf of
two years old, with a round head and the face of a man: the
fore feet are like those of a monkey (or ape),and the hind feet
also.It has curly (or frizzy) hair,a short tail and ears like those
of a man. It resembles the "Tanacht" described by Ambroise
Paré. It can be seen near the pond of the Lipomami [tribe]
and in that region is where it can be found. It is a highly
solitary animal,the people of that country have a great fear of
it and flee from it as it also does from them." From this context,it is not clear whether Flacourt actually had seen this animal.
It is well known that in Madagascar village people tend to
name lemurs after the sounds they make, following a sort of
onomatopoeic pattern for animal names such as occurs in
the case of the cuckoo bird in English. For instance, the
ground predator alarm call of species of genus Propithecus is a
loud "si-i-fak!" cry and so the name of this animal in the Malagasy language is "Sifaka".The mouse lemur makes a chittering
alarm call and has the name "T’sit-sihy".The Avahi,a nocturnal
lemur, has one call that sounds like the word "avahi!" In the
case of Flacourt’s animal the name Tretretretre or Tratratratra is definitely onomatopoeic and sounds like an alarm
bark–it is not unlike the bark alarm call of the southeastern
Madagascan lemur Propithecus edwardsi,or that of another lemur related to it, Indri indri, or even the alarm bark of the
chimpanzee.
Hence, I have often considered this term, or name, to be a
"fossil" sound and it seems likely that it would have been a
replication, by members of the Lipomami tribe of the alarm
call of this giant lemur when they told Flacourt about the animal. The location of the Lipomami region in southeastern
Madagascar is known today (Tattersall,1982).Thus Flacourt’s
name for the animal may be the only known "fossil" sound.
Page 25
There are frequent references by various scientists all agreeing that Flacourt must have been describing,in the above passage, one of the giant extinct lemurs; but which one? All lemurs have hands and feet like those of monkeys, but wavy
hair is more restricted–mainly to members of the Indriid
group or taxonomic family [this family includes only species
of the extant genera Propithecus, Indri, and Avahi] and incidentally they all have rounded ears–like those of a man. One
large giant extinct lemur of the south and southwest of the
island is known as Palaeopropithecus ingens and taxonomists
generally agree that genus Palaeopropithecus is related to the
family Indriidae (Orlando et al., 2008), where curly or frizzy
hair occurs. A number of scientists have speculated that
Flacourt’s Tretretretre lemur belonged to the genus Megaladapis (Tattersall, 1982; Mittermeier et al., 1994), which also
occurs as fossils from the southern part of the island, but
species of this genus have a large snout and could never be
described as having a round head. Moreover, the distal ends
of the nasal bones in species of this genus are elongated and
expanded and, in life, there must have been an expanded or
bulbous nose or even a trunk. Hence, one could never say
that the creature had "a face of a man." Differing from Megaladapis, Palaeopropithecus ingens does have a rounded humanlike head with forward directed eyes and a small face.In addition to all these other features, the living species Indri indri or
babacoot,is the only lemur that has a short tail.In addition to
this, the most complete skeleton of Palaeopropithecus, recovered by a Duke expedition in 1983, and the only associated
skeleton of this animal ever found includes a sacrum that diminishes posteriorly and could only hold a very small and
short tail.In opposition to all these conclusions,it can be said
that Palaeopropithecus ingens could not possibly be construed
to have been the size of a calf of two years in age–nor, in fact,
would any of the extinct giant lemurs have been that large.
Nevertheless, it is well known that exaggeration surrounds
stories about such little known animals, and also Malagasy
cattle tend to be small. For these reasons it would appear
that the Tretretretre was a Palaeopropithecus species–a conclusion also implied by Godfrey and Jungers (2002). A year
later these authors reconfirm the same position (Godfrey
and Jungers, 2003).
Between 1994 and the year 2003 teams from the Duke
Lemur Center excavated fossils at two caves called Akomaka
and Ankilitelo in southwestern Madagascar on the Mikoboka
Plateau north of Tulear. This region is Madagascar’s most
extensive and stratigraphically thickest calcareous plateau.
Discoveries made at both of these caves show that the
southwestern part of the island was inhabited comparatively
recently by several giant lemurs including Palaeopropithecus
ingens and Megaladapis edwardsi. More importantly, these
species lived relatively recently (Godfrey and Jungers, 2002),
as evidenced by radiocarbon dating based on specimens
from Ankilitelo (Megaladapis at 630 ± 50 years B.P. and
Palaeopropithecus, 510 ± 80 years B.P. The latter of these
dates (calculated in 1996) ranged from 1406 to 1566 years
AD and falls into historic times. These are relatively recent
ages,not so far from the date of Flacourt’s observation of the
Tretretretre which could have been at any time after he was
named Governor of Ft.Dauphin Madagascar in 1648;approximately 350 years ago. A more recent date determined in
2008 on a Cryptoprocta bone from Ankilitelo gives a similar
age to that of the Palaeopropithecus, estimated as between
1408 and 1488 (Simons, 1997; Muldoon et al., 2009; Muldoon
and Simons, 2007). This suggests that the small mammals
accumulated more or less contemporaneously with the giant
lemurs. [The cave name, Ankilitelo, means "at the three kili
(tamarind) trees" but no such trees grow there now. Mala-
Page 26
Fig. 1: Harpagophytum grandidieri burr or "hitchhiker" from
southern Madagascar. These barbs are approximately 9.5 cm
across.
gasy caves can be named for a nearby settlement or village.At
present there is no nearby hamlet with such a name but in
the past there could have been. Kili trees often grow in
villages there.]
At this point another speculation can be introduced.Pastoral
grass burning has reduced present day forests on the Mahafaly Plateau, north of Tulear, to the ridges of hills and many
present day plant species occurring in them must be the
same as those of 500-1000 years ago. The remaining forests
near Ankilitelo represent both spiny thicket and succulent
woodland regions and examples of the dry deciduous forest
are nearby (Simons, 1997; Muldoon et al., 2009). In general,
grass burning in that region, near the Ankilitelo cave, is arrested from spreading by outcrops of limestone on the
slopes of hills. In addition, it would appear that surviving forests on hilltops of the Ankilitelo region remain as they were a
few hundred years ago.The surface finds of small mammals in
Ankilitelo (34 species) do reflect those of a few hundred
years ago–when the giant lemurs existed and when the cave
was serving as a natural trap–these environmental conditions were similar to those of the present.The fauna suggests
that, perhaps, the region then was slightly more humid, and
definitely the forests of the region have undergone fragmentation (Simons, 1997; Muldoon and Simons, 2007). Each such
natural trap cave serves as a window in time because, as the
solution cavities open mainly from below,the fauna that fall in
will only begin to collect when there is a surface opening.
More dates are being determined for fossils from Ankilitelo
but the window concerned here did not open long enough
ago that the 34 small mammal species are different from
those now extant in the region or relatively nearby.The commonest giant lemur at Ankilitelo is the awkwardly constructed Palaeopropithecus that presumably could not support itself on all fours on the ground. Once having fallen to
earth it would have been restricted to swimming, sloth-like
motions and this perhaps explains why so many P. ingens fell
into the pit. Also, Godfrey and Jungers (2003) report a Malagasy tradition (p. 258) that an "ogre with the body of an animal but the face of a human" could be made helpless on
smooth rock surfaces. Such clumsiness of the sloth-like
Palaeopropithecus would account both for its abundance in
Ankilitelo and its presumed inabilities on the ground. Whatever the pelage of this animal was like,or indeed that of any of
the giant lemurs, their fur could not have resisted picking up
burrs and other hitchhikers from the southwestern forests
as has been noted with modern lemurs (personal observa-
Lemur News Vol. 15, 2010
tions of Michelle Sauther). A present day student of behavior,
Sauther,has observed individual Lemur catta that had become
entangled with the large seeds of what is often called Uncarina grandidieri–but more properly, because of an earlier date
of description, this species should be assigned to genus Harpagophytum–meaning "snatcher plant". This plant of southwestern Madagascar has amazing "hitchhikers" about 2.5 to 3
inches across each of which has 30/35 protruding spines
approximately 1.5 inches long (see Fig.l).Each of these spines
is, in turn, tipped by 4 recurving fishhook-like projections.
This huge seed pod is something that it seems would only
have evolved to be transported by a much larger animal than
any now extant on the Island–presumably a giant lemur like
species of such southern genera as Palaeopropithecus, Megaladapis, or Archaeolemur or even transportation by the elephant bird (see below).
Modern botanists report that the pasty pollen of this plant is
spread by pollen-eating beetles, who, after feeding on pollen
from the anthers, get it all over themselves and when covered by pollen fly from flower to flower where pollen is
transmitted from them to the stigma. This sort of pollination
may be the principal fertilization process, but lemur transport of these seed burrs does occur today (personal observations of Michelle Sauther), and must have also done so in
the past. Working at the Beza Mahfaly Special Reserve, in
southwestern Madagascar,Sauther has seen Lemur catta individuals with Harphagophytum burrs stuck on the face, feet,
and tail. However, she has not seen them attached to Propithecus verreauxi; a second larger, diurnal lemur species which
occurs at Beza but is more arboreal than L. catta. These dry
seed pods would naturally attach to the skin, not necessarily
fur, of any passing animals and be carried while attached until
its spines were broken enough for the seed to drop off.It was
recently suggested that dispersal of these seed pods might
have been carried out primarily by the extinct elephant birds
of Madagascar (Midgley and Illing, 2009). The authors presenting this view argue that the mature fruit more often accumulate on the ground as "trample burrs" and so are more
likely to stick to the feet of these extinct giant ratites than to
fur of arboreal animals. I suspect, however, that the giant lemurs did not always stay high up in trees but were often on
or near to the ground. The mature terminal hooks of the
Harpagophytum (Uncarina) burr have evolved so as to attach
to any extremity, not necessarily fur. Also it is of interest that
these plants are often called the "Mouse-trap tree" or "Grapple tree". These species belong in the sesame family (Pedaliaceae) and typically constitute shrubs or small trees. It is
told that Malagasy people sometimes collect and put together bunches of these seeds and place cheese or other attractants at the center of the bunch. They then use this device to trap rats and mice: Hence, the origin of the common
name.
References
Etienne de Flacourt.1658.Histoire de la grande Isle Madagascar, 2 vols. Chez G. de Lvyne, Paris.
Godfrey, L. R.; Jungers, W. L. 2002. Quaternary fossil lemurs.
Pp. 1-530. In W.C. Hartwig (ed.). The Primate Fossil
Record:Cambridge Studies in Biological and Evolutionary
Anthropology No. 33. Cambridge Univ. Press, Cambridge,
UK.
Godfrey,L.R.;Jungers,W.L.2003.The Extinct Sloth Lemurs of
Madagascar. Evol. Anth. 12: 252-263.
Midgley, J. J; Illing, N. 2009. Were Malagasy Uncarina fruits dispersed by the extinct elephant bird? So. Af. J. Sci. 105
(11/12): 467-499.
Mittermeier, R.A.; Tattersall, I.; Konstant, W.R.; Meyers, D.M.;
Mast, R.B. 1994. Lemurs of Madagascar. Conservation
International, Washington, D.C., USA.
Page 27
Lemur News Vol. 15, 2010
Muldoon, K.M.; de Blieux, D.D.; Simons, E.L.; Chatrath, P.S.
2009. The subfossil occurrence and paleoecological significance of small mammals at Ankilitelo cave,southwestern
Madagascar. Journ. Mammology 90 (5): 1111-1131.
Muldoon,K.M.;Simons,E.L.2007.Ecogeographic Size Variation in Small-Bodied Subfossil Primates From Ankilitelo,
Southwestern Madagascar.Am.J.Phys.Anth.134:152-161.
Orlando, L.; Calvignac, S.; Schnebelen, C.; Douady, C.J.; Godfrey, L.R.; Hänni, C. 2008. DNA from extinct giant lemurs
links archaeolemurids to extant indriids.BMC Evolutionary Biology 8: 121.
Simons,E.L.1997.Lemurs:Old and New.In S.M.Goodman;B.
D.Patterson (eds.). Natural Change and Human Impact in
Madagascar. Smithsonian Inst. Press, Washington, D.C.
Tattersall, I. M. 1982. The Primates of Madagascar. Columbia
Univ. Press.
Husbandry guidelines for mouse lemurs
at Paris Zoo
Delphine Roullet
Parc Zoologique de Paris, MNHN, 53 avenue de Saint Maurice, 75012 Paris, France, roullet@mnhn.fr
There are two species of mouse lemur in captivity in Europe:
the grey mouse lemur, Microcebus murinus, and the Goodman’s mouse lemur, Microcebus lehilahytsara (Pes, 2009). The
European captive population of grey mouse lemurs was
established at the end of the 1960s and is now composed of
165 individuals (778.77.10; Pes, 2009), distributed in 29 institutions. The population of this species is of unknown origin.
According to recent morphological measurements (Pes,
2009) and preliminary results of mtDNA studies (Roos,
2008, in Pes, 2009), this population can be divided into two
pure lineages: one composed of pure breed animals from the
region of Vohimena (SW Madagascar), and the other of pure
breed animals from the region of Mandena (SE Madagascar).
A third lineage is composed of hybrids between the two pure
lineages (Pes, 2009).
The European captive population of Goodman’s mouse lemurs was established in 2005 and is currently composed of
62 individuals (33.29; Pes, 2009) distributed in two institutions. The first animals were imported from the area of
Andasibé, Madagascar. They were recognized as a new species when they arrived in Europe (Rübel, pers. comm.).
The Parc Zoologique de Paris has a success story with the
grey mouse lemurs. The most important group arrived in
December 1990 and was composed of 79 individuals. The
origin of the animals that arrived in the 1980s is unknown.
According to the analysis of the European captive population
(conducted by Tomas Pes for the ESB), the animals coming
from Paris appear to be hybrids between the two pure lineages described above (Pes, pers. comm.).
The first births occurred in 1991 only a few months after the
arrival of the first animals.During the period of 1991 to 2004,
when the last grey mouse lemurs eventually left the zoo after
the closing of the nocturnal area, there had been a total of
224 successful births (young surviving longer than two
months), with an 86.5 % birth success rate. 1994 was the
most prolific year with 56 successful births. The colony of
grey mouse lemurs in Paris occasionally reached more than
150 individuals.
Before 2001, we didn’t know much about the animals, especially the composition of the groups.Eleven females were the
founders of the colony in Paris. Since the identity of the fathers was not recorded, the filiations were only built from
the females. Potentially, 28 males could have been the founders of the colony.
Before 2002, most of the females lived alone in small cages
and were introduced to males (of various group sizes) only
during the few days of oestrus. The females were kept isolated again afterwards. The young were separated from their
mothers just after their weaning to join a young animals
group.
In 2002 we decided to implement some changes in the management of the colony in order to improve the wellbeing of
the animals: to increase the space available to them, to rearrange the enclosures according to the wild habitat of the animals, to carry out enclosure enrichment, and to re-constitute the groups to make them more similar to the ones observed in the wild. The following husbandry guidelines were
established according to the new management of the colony
set up in 2002.
Only single sex groups could be seen by the public.The breeding groups were kept in a separated building. Moreover,
from 2002 onwards,we limited the number of births (around
10 per year) in order to be able to keep all the animals in
good conditions (and no longer in small cages as had been
done in the past).
Facility standards
1. Enclosure
Size: The enclosure should have a minimum total floor size
of 4 m² with a minimum height of 2 m for both male and female groups.For a mother with her young,the enclosure can
be smaller during the first month.After this period,the young
start to explore their environment and need more space.
Temperature: 20°C (18-22° C). Not below 18° C. Below
this temperature, the animals enter torpor. Torpor can also
be provoked by intense stress such as prolonged capture of
an animal.
Inside Humidity: 50-70 %.
Lighting and photoperiod: Similar to that found in Madagascar or Europe but the photoperiod must vary during the
year for breeding.
Furniture: Dense environment with thin branches and
leaves. The animals need to have many places to hide from
people and also from each other when they live in groups,especially when the animals are unrelated.
Nest box (see Fig. 1):
· Size: 12x12x12 cm
· Entry diameter: 5 cm
· It’s very important to provide one nest box per animal, in
different places, even if they sleep together. This allows
them to be alone if they want to be.
Fig.1:Grey mouse lemurs (Microcebus murinus) in nest box at
Paris Zoo. (Photo: F.-G. Grandin, MNHN)
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Lemur News Vol. 15, 2010
2. Feeding and watering
Two feeding spots are needed if there are more than two
adults in the group. Additional feeding spots are required according to the size of the group. If there are not enough nest
boxes or feeding spots,the animals can be very aggressive towards one another, sometimes causing serious wounds,
mostly to the tail. One water bottle per enclosure is sufficient.
Diet for 1 animal/day:
Monday: 1 tea-spoon of gruel* + 3 folivorous pellets
Tuesday: 1/8 of apple + 2 slices of carrot + 3 folivorous pellets
Wednesday:1/8 of apple + 1/8 of pear + 3 folivorous pellets
Thursday: 1 tea-spoon of gruel* + 3 folivorous pellets
Friday:1/8 of apple + 2 slices of carrot + 3 folivorous pellets
Saturday: 1 tea-spoon of gruel* + 3 folivorous pellets
Sunday: 1 slice of banana + 1/8 of mango + 5 mealworms + 3
folivorous pellets
*Gruel composition: folivorous pellet powder + milk
powder + baby cereals + yolks + cottage-cheese + juice of
squeezed oranges + vitamins (every Monday).
For overweight animals (weight >100 g):from Tuesday to Saturday we provide only 2 slices of carrot and 3 folivorous pellets. No change for Sunday and Monday.
For underweight animals (weight <70 g): we add 5 mealworms and one piece (~2 cm²) of gingerbread every day in
the diet.
It is important to give more food to lactating females. If they
don’t have enough food, they will eat their young: we add 5
mealworms and one piece (~2 cm²) of gingerbread every day
in the diet.
Social grouping
During the non-breeding season, we separate males from females.
Male groups: the best groups are composed of individuals
of the same litter.If the males are unrelated,it is important to
know the dominance relations between them in order to determine which one will be the breeding male (probably the
dominant one). From 2002, studies of the hierarchy in the
male groups were systematically conducted to allow us to
determine the young’s fathers. The male groups are composed of 2 to 5 individuals (Fig. 2). Note that we managed to
keep a group of up to 10 males together as a non-breeding
group.
Female groups:they are only composed of related females
(mother-daughter-sister). The female groups are composed
of 2 to 4 individuals.But more important groups can be maintained in more spacious enclosures. Note that it was impossible to keep unrelated females together for more than one
breeding season. These groups are very unstable and the females can be very aggressive towards one another.Moreover,
the old unrelated females are very anti-social and do not tolerate each other.
The breeding groups are established in March, before the
beginning of the breeding season. The best way to do this is
to introduce the females of a same group to the males’ enclosure.
Reproduction
Oestrus observation: When the females are with the
males, it is important to check their vulvas regularly in order
to follow the oestrus evolution (vulva opened 2-3 days every
month during the breeding season;until 3 oestrus per breeding season). If a female does not develop a second oestrus
(probable pregnancy, length: 2 months), she is removed from
Fig.2:Group of male grey mouse lemurs (Microcebus murinus)
at Paris Zoo. (Photo: F.-G. Grandin, MNHN)
the breeding group and kept alone until her young are
weaned. The females, even if they are related, can be very
aggressive to one another during this period. At the end of
the oestrus most females develop a white cap on their vulva.
The females can have a baby from 8 months old. This means
that they can have their first oestrus at 6 months. It is better
to remove females from a breeding situation after 6 years,
but it is important to keep them in related female groups.
The size of the male’s testes increases at the time of oestrus.
Except for the oestrus period, testes are usually almost invisible.
Parturition observation: The nest boxes are checked
every day for several days before the parturition. Before
opening a nest box, we softly tap on it: it allows the female to
exit without having a baby hanging on to her nipples (between 1-3 young). The nest box is opened every day for several days after the parturition, to check if the young are still
alive (but we don’t touch them of course!).The births can occur from March to October but most of them appeared from
April to June in Paris where we follow the Malagasy photoperiod.
Splitting of the young: It is better to wait 4-5 months after
the parturition before doing any changes in the motheryoung group (even if the young are weaned at 2 months).
Then, the daughter(s) stay with their mother and all are introduced back into the female group that they originated
from before the breeding season.The young male(s) are separated from their mother and sister(s).If there is only 1 male,
he is introduced to a group of males of the same age. If there
are several brothers, they stay together and compose a new
male group.
Enrichment
In Paris, a study showed that the females use feeding enrichments more often than the males.This could be explained by
the ecology and behaviour of this species; by the fact that the
Page 29
Lemur News Vol. 15, 2010
females may be more interested in food during the breeding
season than the males which,in turn,may be more interested
in the females (Roullet, 1998).
The enrichment made with a branch covered in fruit juice
was the most used by the animals: This is a branch (diameter
of around 5 cm, length of 30-40 cm) in which two trenches
are dug along its length. The branch is fixed onto the mesh
roof. We apply the fruit juice in the trenches with a brush
(Roullet,1998).The animals spend their time licking the juice
out of the branch as they would do with sap in wild (Martin,
1973).
Mixed-species exhibits
Paris Zoo experienced 2 successful combinations: with ayesayes (Daubentonia madagascariensis) and greater tenrecs
(Tenrec ecaudatus). We tried to put the mouse lemurs in with
slow lorises (Nycticebus coucang), but without success:
wounds were observed on the mouse lemurs’ tails, so they
were removed from the exhibit.
Introduction
Background
The Biosphere Reserve of Mananara-Nord was created in
1989. It is one of 533 UNESCO (the United Nations Educational, Scientific, and Cultural Organization) Biospheres
around the world.The Biosphere Reserve of Mananara Nord
covers 144,000 ha, with 23,000 ha being devoted to a terrestrial park, and another 1,000 ha to a marine park. The terrestrial national park is split into three separate parcels. Going
from north to south these parcels are: Ivontaka Nord,
Ivontaka Sud, and Verezanantsoro. The parcel of Ivontaka
Nord covers an area of only 827 ha.This is small compared to
the other two parcels; Ivontaka Sud and Verezanantsoro,
which are 1,300 ha and 20,685 ha respectively (Fig. 1). These
parcels are connected by forest sections that are not protected by the national park system (ANGAP, 2005).
References
Martin, R.D. 1973. A review of the behaviour and ecology of
the lesser mouse lemur (Microcebus murinus). Pp. 1-68. In:
R.P. Michael; J.H. Crook (eds.). Comparative ecology and
behaviour of primates. Academic Press, London, UK.
Pes, T. 2009. The European Studbook of Grey Mouse Lemur
(Microcebus murinus). Zoo and Botanical Garden Plzen.
Roullet, D. 1998. Effet d’un enrichissement physique sur les
comportements agonistiques et exploratoires de plusieurs groupes de microcèbes murins (Microcebus murinus)
en captivité. DESS d’Ethologie Appliquée et de Chronobiologie du Comportement. Université Paris XI.
Articles
Diurnal lemur density in the national
park parcel Ivontaka Nord, UNESCO
Biosphere Reserve of Mananara-Nord
Marta Polasky Lyons
School for International Training, Fort Dauphin, Madagascar;
and Carleton College, Northfield, Minnesota, USA,
marta.lyons@gmail.com
Abstract
Here I present a recent diurnal lemur density study performed in the Biosphere Reserve of Mananara Nord, conducted between the dates of November 9 and 22, 2008 in
Ivontaka Nord; part of Mananara-Nord National Park. Densities were calculated using transect walks, and other information was gathered through interviews with local people
and national park staff. The density of Eulemur fulvus albifrons
appears to be over twice that recorded in other areas
(Table 1), while the density of Varecia variegata variegata
appears to be low, perhaps due to the latter’s preference for
undisturbed habitat and past problems with overhunting. In
addition, Eulemur rubriventer was found to inhabit the park,
though its range was previously thought not to extend east
into the biosphere. Having been, in the past, under strong
pressures from local inhabitants, Ivontaka Nord represents a
disturbed low altitude rainforest;however this report shows
that the lemur populations within the parcel may be recovering.
Fig.1:National Park of Mananara-Nord.Three parcels in dark
shade, going from north to south: Ivontaka Nord (where this
survey was carried out), Ivontaka Sud, Verezanantsoro.
Source: MNP.
Threats
It is estimated that approximately 1.9 to 2.2 % of the primary
forest within the biosphere is cleared every year, usually for
rice cultivation through tavy (slash and burn agriculture)
(ANGAP, 2005). Besides just destroying necessary habitat,
this deforestation further splits already extremely fragmented sections of primary forest.Another concern is illegal
(and legal) selective extraction. The population within the
biosphere relies on wood for constructing their houses and
fuel for cooking. In the villages most cooking is done over an
open flame using collected wood. The wood does not simply
go to the villages on the periphery of a forest, but is also collected for sale in urban centers and areas farther away from
the forest.
Page 30
Another large concern in the biosphere has to do with
poaching. Until recently, hunting was thought to not be of
great concern in Madagascar, being far below the menace
caused by deforestation (Goodman et al., 2003); however,
that is quickly proving incorrect. Unlike in other areas of the
country where eating lemurs is considered fady (taboo), the
Betsimisaraka ethnic group that makes up the majority of inhabitants within the biosphere reserve is only known to have
fady related to the eating of Indri indri,and even this taboo has
been shown not to be universal (Mittermeier et al., 2006). In
the area people have classically used laly (traditional lemur
traps) and firearms in order to hunt lemurs for consumption
(ANGAP, 2005). Lemurs within the reserve have been a traditional source of protein for villagers whose diets are based
on the staple rice.
Site
The field camp was situated within the town of Ambodivoandrozana approximately 17 km south of Mananara Nord. The
village is inaccessible by vehicle but rests less than 2 km from
the national park parcel of Ivontaka Nord.Between the town
and the national park lies another forest managed by the
COBA (communaute de base) for conservation and local subsistence needs. This forest is split into three zones; Beantohiravina (21.7 ha), Betsingiala (11.52 ha), and Ambahinkarabo (41.06 ha). These zones are separated by areas of
agricultural land and secondary forest. A Gestion Contractualisée des forêts (GCF) in 2005 transferred certain management and use rights to the local community. It is mostly
low altitude primary growth rainforest, intermixed with
zones of savoka (secondary growth). The parcel of Ivontaka
Nord is made up of both primary forest and disturbed habitat.From past species inventories,it was believed that two diurnal lemur species (Eulemur albifrons and Varecia v. variegata)
and multiple nocturnal species, including Microcebus rufus,
Lepilemur mustelinus, Avahi laniger, and Daubentonia madagascariensis among others inhabited this national park.
Methods
A survey of diurnal lemur species was conducted in the low
altitude (between 250 and 300 m above sea level) rainforest
in the national park of Ivotaka Nord and adjoining community-managed forest (GCF). The survey was conducted from
November 9-22,2008.Within the national park parcel,a preestablished 2 km transect set up by ANGAP was followed, in
addition to other transects along preexisting paths throughout the two forests. Additional permanent transects were
not established because of time constraints and the desire to
limit the impact on the habitat. Instead, distance was measured by walking at a constant pace along preexisting paths
(approximately 900 m per hour). This pace was calculated
using the 2 km transect, and variation in speed was used to
create a range for densities. The total of 17 transects were
walked, ranging from 600-2,500 m in length, with a total distance walked of approximately 30 km.
For each transect the date, start and end time, weather, and
location were recorded.When a lemur was spotted,the species was noted along with the group size,time of day,distance
on transect, distance from path, habitat type, and the GPS
coordinates. Density was then calculated by the number of
individual lemurs/area. Area was based on the total length of
transects walked multiplied by double the average perpendicular distance of lemur from the path (Whitesides et al.,
1988; Norscia et al., 2006). Common methods for this type
of primate study include using a 50 % criterion for falloff
distance based on histograms (Whitesides et al., 1988; John-
Lemur News Vol. 15, 2010
son and Overdorff, 1999; Erhart and Overdorff, 2008) or the
program DISTANCE (Quemere et al., 2010). However, given
time constraints it was not possible to collect an adequate
amount of data to perform these tests.Based on earlier studies on similar species in similar habitats we used a falloff distance of 20 m (Irwin, 2001). In addition to transect walks,
interviews were conducted with employees of the ANGAP
office of Mananara Nord and local people of the town of Ambodivoandrozana. Within the village, the interviews were
done with prominent members of the community including
members of Slow Food (an agriculture movement within the
biosphere) and the COBA.
Results
The observed population density for Eulemur albifrons was
46.13 ± 2.32 individuals/km2 within the park (Tab.1).The average group size observed was 7 individuals. Multiple groups
were observed with females carrying babies on their back,
and overall this species was found in a variety of different
habitats, both dense and sparse primary forest, and even on
the edge of secondary growth. Through a combination of
data collected in the forest and interviews with local people,
we found that though Eulemur albifrons frequents multiple
habitats, even leaving the forest to eat crops, they mainly rest
within the National Park.
Two other diurnal lemur species were observed within the
parcel, Varecia variegata variegata and Eulemur rubriventer. V. v.
variegata was observed to have a density of 1.06 ± 0.02 individuals/km2 (Tab. 1). This species was only observed on one
occasion and only one individual was seen. According to the
local guide and vice president of the COBA, eight individuals
of this species exist within the parcel, a group of five and a
group of three (F. Frejes, personal communication). This implies a density of 0.97 individuals/km2. From traces observed
on the ground (eaten fruit) and calls heard,it seems clear that
this lemur spends the majority of its time within the limits of
the parcel as it prefers deep valleys with tall trees; a habitat
not found in the more disrupted community managed forest.
Tab.1:Density of diurnal lemurs within the parcel of Ivontaka
Nord. Densities were calculated of the three species observed within the parcel, Eulemur albifrons, Eulemur rubriventer,and Varecia v.variegata.A 50 % falloff distance was used
for perpendicular distances over 20 m (Whitesides et al.,
1988; Irwin et al., 2000) Error bars represent the error in
pace of transect walked and error in observation of animals
from path.
Species
Eulemur
albifrons
Eulemur
rubriventer
Varecia v.
variegata
Number of
Number of Calculated density
individuals
groups
(individuals/km2)
encountered encountered
31
5
46.13 ± 2.32
3
1
6.40 ± 0.38
1
1
1.06 ± 0.02
Eulemur rubriventer, being a species believed to live west of
the biosphere in higher altitude rainforest, was thus not on
the initial list of lemurs to be found in the area. From the one
sighting of three individuals in a dense part of the primary
forest, the calculated density is 6.40 ± 0.38 individuals/km2
for the parcel (Tab. 1). No sightings were made of this individual outside of the parcel, and as its eating habits closely mirror that of E.albifrons,it was not possible to tell the difference
between traces found on the ground.
Lemur News Vol. 15, 2010
Discussion
The parcel of Ivontaka Nord is considered to be an example
of disturbed primary forest. Anthropogenic effects are much
stronger in Ivontaka Nord than in other parcels, because it is
the smallest of the three, and the closest to the town of
Mananara. Before the creation of the national park, the area
of Ivontaka Nord was frequently used as a place to grow
crops through tavy,harvest wood for construction and cooking,and hunt lemurs.For these reasons,the lemur population
of the parcel was at one time diminished to the point of localized extinction of the critically endangered Varecia v.variegata,
in addition to the localized extinctions of Indri indri and Hapalemur griseus (J. Betsiahilika, personal communication). Yet,
because it is connected through a corridor of community
managed forest to the less disturbed parcel of Ivontaka Sud
(Fig. 1), in 2002, V. v. variegata migrated into the GCF corridor
between Ivontaka Sud and Ivontaka Nord, and in 2005 these
lemurs could again be found within the parcel. However, the
species of Indri indri and Hapalemur griseus are not believed to
currently inhabit the parcel, though they can be found in the
other two parcels within the biosphere (J. Betsiahilika, personal communication).
Within the parcel, there was convincing evidence to suggest
that the lemurs might be recovering even more than previously known. During the two weeks of transects, Eulemur
rubriventer was observed within the parcel, even though its
recorded range ends west of the biosphere reserve. In addition, traces of the distinct eating habits (shredding the stems
of tall plants whilst stripping off foliage) of Hapalemur griseus
were found within the savoka. Additionally, there were reports of Indri indri spending time in the corridor between
Ivontaka Sud and Ivontaka Nord (J. Betsiahilika, personal
communication).
Through field observations, E. albifrons was found to have a
population twice that found in other areas such as Masoala
(Mittermeier et al., 2006). They frequent both the parcel and
community forest. During the season in which this study
took place,when most of the fruit within the parcel is not yet
ripe, many Eulemur albifrons were reported by local villagers
to be exiting the parcel in search of other cultivated fruits
like lychee and banana. V. v. variegata on the other hand
appeared to not leave the protected parcel. It is possible that
they adapt their feeding habits based on the season and thus
do not eat cultivated fruits (Ratsimbazafy, 2002).
The observed density of V. v. variegata was not congruent
with the report of the local guide (F.Frejes,personal communication). This species, like Eulemur rubriventer, was observed
on only one occasion. Because of time constraints, surveys
had to be conducted over a two week period and with only
the use of one field team. For more complete and definitive
findings, a survey needs to be done over a longer period of
time, possibly across different seasons. Also, it would be
beneficial to conduct the same type of study after dark.
Finally, it would be helpful to determine lemur densities in
the other two parcels, and the community managed forests
in-between.
Conclusion
It is currently of the utmost importance to make sure that
the integrity of forested sections outside the realm of the
parcel remains protected. These areas represent a buffer between the fragile low altitude rainforest and an ever expanding human population. The corridor formed by these community-managed forests, between the three national park
parcels, is a priority area. It has already been shown to provide a bridge to facilitate migration between the three parcels,which is critical in a country where forest fragmentation
Page 31
is proving detrimental to the gene flow of lemurs (Louis et al.,
2006).
Through the work of the biosphere reserve, significant steps
have already been taken to encourage conservation. Both
government officials and villagers appear to be working together to promote a healthy ecosystem. Already with the
promotion of crops such as vanilla,cloves,and coffee,as an alternative to other more environmentally negative livelihoods, villagers say they have seen an improvement both in
their lives and the forest health (Desana and Berger,personal
communication). However, people have needs; the agricultural inhabitants of these rural areas need both to grow their
food and to have wood and other materials for performing
everyday tasks. It is possible to improve both the lives of the
people in the area and decrease their negative impact on
their environment through simple strategies such as rice intensification and promoting more efficient cooking methods.
Maybe then populations of Indri indri, Hapalemur griseus, and
Propithecus diadema,all species that at one time inhabited the
area, will return to the parcel of Ivontaka Nord.
Acknowledgements
This study was carried out under a Memorandum of Understanding between SIT and ANGAP Mananara for an internship for the author in November 2008. SIT thanks the Ministry of Higher Education and Scientific Research and the University of Antananarivo for the ongoing collaboration under
which SIT Study abroad operates. This study could not have
been possible without the help of Barry Ferguson and Jim
Hansen of SIT in addition to the staff in the ANGAP office of
Mananara, including Willy Mora, Jocelyn Bezara, Justin Besiahilika, and Jean Cristophe Josoa.
References
ANGAP. 2005. Plan de Gestion de la Conservation-Parc
National Mananara Nord.
COBA FMAA. 2005. Fifanekena Famindra-Pitantanana ny
Atiala sy ny Harena Voajanahary azo Havaozina ao Ambodivoandrozana.
Erhart, E.M.; Overdorff, D.J. 2008. Population demography
and social structure changes in Eulemur fulvus rufus from
1988 to 2003. American Journal of Physical Anthropology
136: 183-193.
Goodman, S.; Raselimanana, A. 2003. Hunting of wild animals
by Sakalava of the Menabe region: a field report from
Kirindy-Mite. Lemur News 8: 4-6.
Irwin, M.T.; Samonds, K.E.; Raharison, J. 2001. A biological inventory of the lemur community of Réserve Spéciale de
Kalambatritra, south-central Madagascar. Lemur News 6:
24-28.
Johnson, S.E.; Overdorff, D.J. 1999. Census of brown lemurs
(Eulemur fulvus sspp.) in southeastern Madagascar:
Methods-testing and conservation implications. American Journal of Primatology 47: 51-60.
Louis, E.E. jr.; Coles, M.S.; Andriantompohavana, R.; Sommer,
J.A.; Engberg, S.E.; Zaonarivelo, J.R.; Mayor, M.I.; Brenneman, R.A. 2006. Revision of the mouse lemurs (Microcebus) of Eastern Madagascar. International Journal of
Primatology 27: 347-389.
Mittermeier, R.; Tattersall, I.; Konstant, W.R.; Nash, S.D. 2006.
Lemurs of Madagascar. Conservation International, Washington D.C.
Norscia,I.;Rahanitriniaina,O.G.;Jolly,A.;Donati G.2006.Preliminary survey of lemur density in the semimontane rainforest of Anka, Fort-Dauphin region. Lemur News 11: 1416.
Quemere, E.; Champeau, J.; Besolo, A.; Rasolondraibe, E.;
Rabarivola,C.;Crouau-Roy,B.;Chikhi,L.2010.Spatial Variation in Density and Total Size Estimates in Fragmented
Primate Populations: The Golden-Crowned Sifaka (Propithecus tattersalli). American Journal of Primatology 72:
72-80.
Page 32
Ratsimbazafy, J.H.; Ramarosandratana, H.V.; Zaonarivelo, R.J.
2002. How do black-and-white ruffed lemurs still survive
in highly disturbed habitat? Lemur News 7: 7-10.
Sur le Commerce International des Especes de Faune et de
Flore Sauvage. 2005. Loi N 2005-018.
Whitesides, G.H.; Oates, J.F.; Green, S.M.; Kluberdanz, R.P.
1988. Estimating primate densities from transects in a
West African rain forest; a comparison of techniques.
Journal of Animal Ecology 57: 345-367.
Lemur News Vol. 15, 2010
that villagers brought to our attention, and from anecdotal
evidence in existing literature. The ten localities from where
information was available included (from south to north) the
Marolambo area, the Brickaville area, the western parts of
the Ankeniheny-Zahamena Corridor (CAZ), Zahamena, the
Soanierana-Ivongo area, Ambatovaky, Marotandrano, Mananara, Makira, and Marojejy (Fig. 1).
Distribution of Prolemur simus north of
the Mangoro-Nosivolo River – how far
north do we really have to look?
Rainer Dolch1*, Erik R. Patel2, Jonah H. Ratsimbazafy3,4, Christopher D. Golden5, Tianasoa Ratolojanahary1, Jean Rafalimandimby1, Jonathan L. Fiely1
1Association MITSINJO, Lot 104 A, Andasibe 514, Madagascar
2Cornell University, 211 Uris Hall, Ithaca, NY 14850, USA
3Durrell Wildlife Conservation Trust,BP 8511,Antananarivo
101, Madagascar
4GERP, 34 Cité des Professeurs, Fort Duchesne, Antananarivo 101, Madagascar
5University of California, Department of Environmental
Science, Policy and Management, Mulford Hall #3114, Berkeley, CA 94720, USA
*Corresponding author: rdolch@gmx.de
Introduction
While the Mangoro-Nosivolo river system is a recognized
biogeographical divide for several lemur species (Goodman
and Ganzhorn, 2004), this pattern does not hold for the
Greater Bamboo Lemur (Prolemur simus). Findings from
numerous subfossil sites indicate that the historical distribution of P. simus, now one of the rarest Malagasy primates
(Wright et al.,2008,2009),once encompassed most of Madagascar (Godfrey and Vuillaume-Randriamanantena, 1986).
During the last 150 years, documented sightings of the species became more and more scarce and by the middle of the
last century it was already feared extinct (e.g. Napier and
Napier, 1967).
More recent discoveries came solely from southeastern
Madagascar (Petter et al., 1977; Meier and Rumpler, 1987),
which led to the unspoken assumption that P. simus had been
extirpated from the rest of the island. Despite the fact that
the last collected specimen of P. simus had come from
Mananara in 1876 (Godfrey and Vuillaume-Randriamanantena, 1986), not a single individual had been found north of
the Mangoro river for more than 130 years, before Dolch et
al. (2004, 2008) rediscovered the species in Torotorofotsy, in
the commune of Andasibe.
In order to investigate further into the distribution and abundance of P. simus north of the Mangoro, several extensive
surveys have recently been, and are currently being, conducted (King and Chamberlan, 2010). As preliminary results
of these surveys are trickling in, accounts of P. simus from
inhabitants of these regions also multiply rapidly and await
verification.
We do not aspire to anticipate survey results, but we believe
that summarizing our current knowledge of P. simus north of
the Mangoro is crucial for the planning of future surveys and
conservation strategies.
Methods
We gathered and compiled information on P. simus north of
the Mangoro deduced from our own research, from reports
Fig. 1: Localities from where information on P. simus was collected.
Results
Results of our compilation are summarized in Tab.1.Of all localities north of the Mangoro examined, two (Brickaville and
western CAZ) have steadfast records of P.simus based on independently confirmed sightings. One locality (SoanieranaIvongo) has a record based on a single observation, whereas
for four others (Marolambo, Zahamena, Ambatovaky, Makira) evidence is only based on reports of villagers. The final
three (Marotandrano, Mananara, Marojejy) do not have any
records. Details are given below.
Tab. 1: Potential localities for P. simus north of the NosivoloMangoro.
Region
Marolambo area
Brickaville area
Western CAZ
Zahamena
Soanierana-Ivongo area
Ambatovaky
Marotandrano
Mananara
Makira
Marojejy
evidence based on
reports by villagers
sightings, confirmed
sightings, confirmed
reports by villagers
sightings, unconfirmed
reports by villagers
(no evidence)
(mo evidence)
reports by villagers
(no evidence)
Marolambo area. A hotspot of endemic fish species richness, the Nosivolo and lower Mangoro rivers have recently
received increased attention by researchers and conservationists alike. While working in this area, we received several
accounts of villagers on P. simus from 2006-2009. Reports
claiming the occurrence of P. simus come from 4 communes
along the Nosivolo-Mangoro river, and focus (from west to
east) on Ambohimilanja, Betampona, Marolambo and Ambinanidilana. In order to verify these accounts, a preliminary
survey is currently being conducted within The Aspinall
Foundation’s "Saving Prolemur simus" project (Ratsimbazafy,
2010).
Lemur News Vol. 15, 2010
Brickaville area. A similar survey has already been conducted for the Brickaville area. A total of 6 sites in isolated
fragments in the communes (from west to east) of Fanasana,
Anivorano and Fetraomby have been found containing P.
simus. Details are given by Ravaloharimanitra et al. (2010).
Western CAZ.In the course of the same survey, 12 sites in
the western parts of the Ankeniheny-Zahamena corridor
have been found containing P. simus (Ravaloharimanitra et al.,
2010). These findings follow earlier reports from villagers
that had claimed its presence (e.g. Schmid and Alonso, 2005).
The communes where P. simus has been confirmed include
(from south to north) Andasibe, Morarano-Gare, Fierenana,
and Didy.
Zahamena. Ganzhorn (2004) states that a report of the
presence of P. simus in the PN Zahamena was brought to his
attention in 1995, but that it "was questioned and eventually
withdrawn". Information on a possible occurrence of P. simus
in Zahamena, obviously derived from that report, is mentioned in Godfrey et al. (1997).
Soanierana-Ivongo area. In their little noticed bulletin,
the Association de Défense de la forêt d’Ambodiriana report that trainee Coralie Ebert, while studying the woolly
lemurs (Avahi laniger) of this forest, claims to have observed
an individual of Prolemur simus (ADEFA, 2009). An earlier
lemur survey of the area (Beaucent and Fayolle, 2008) has
not yielded evidence of P.simus.The forêt d’Ambodiriana lies
just 30 km to the north of Soanierana-Ivongo,a region where,
according to Mittermeier et al. (2006), halogodro and bokombolobe are still used as local names for P. simus.
Ambatovaky.Ambatovaky is an area that has received only
little attention due to its difficult accessibility. In the early
1990s, a lemur survey was conducted by Evans et al. (19931994). They did not find tangible evidence for P. simus, but
state that "local people indicated that there existed until recently a lemur which fed on giant bamboo along the Sandrangato and/or Marimbona rivers,known as alakoto or halokoto".
Marotandrano.Lying to the northwest of Ambatovaky,Marotandrano has even received less attention than the former.
A lemur survey by Ralison (2006) did not indicate presence
of P. simus.
Mananara. The last specimen of P. simus to be collected
from north of the Nosivolo-Mangoro river came from an
area close to Mananara (Godfrey and Vuillaume-Randriamanantena,1986).Although the exact collection locality can not
be traced (due to unsuited transcription of its name by the
collector J. P. Audebert), the assumption that P. simus may still
occur in the forests around Mananara was still put forward
by Nicoll and Langrand (1989). No evidence for P. simus in
Mananara has been produced since.
Makira. Being Madagascar’s largest continuous rainforest
(317,000 ha), lemur surveys in Makira are not easy to conduct. Two years of intensive surveys by Rasolofoson et al.
(2007) and Ratelolahy and Raivoarisoa (2007) have not uncovered any evidence of P. simus. Similarly, during seven years
of relying on trusting relationships with hunters, Golden
(2009) has not come across P. simus among the 23 mammal
species hunted for consumption throughout southern,western, northern, and eastern Makira. However, villagers living
adjacent to the newly discovered Antohaka Lava forest at the
edge of northeastern Makira (20 km south of Andrakata on
Marojejy’s southeastern border) have reported recent sightings of a large bamboo lemur with ear tufts known locally as
bokombolobe.Unfortunately,several months of systematic lemur surveying of the Antohaka Lava forest between August
and December 2009 did not confirm these reports, despite
an exceptional primate diversity documented inthat area
(Patel, 2009).
Page 33
Marojejy. A lemur survey by Sterling and McFadden (2000)
found no evidence of P. simus. Alleged observations of bamboo lemurs other than Hapalemur griseus by tourists may be
attributed to the possible presence of H. occidentalis, rather
than P. simus (R. Mittermeier, pers. comm.). Moreover, during
nine years of research on Propithecus candidus in Marojejy, no
local reports or sightings of P.simus have been received (Patel,
2009).
Discussion
Despite the scarcity of information, growing evidence supports that P. simus may still be widespread in Madagascar
north of the Mangoro river. Since the species occupies large
home ranges (Dolch et al., unpubl. data), appears to travel at
night due to possible cathemerality (Santini-Palka, 1994), is
cryptic, and often silent when unhabituated, it is conceivable
that it has been overlooked in the past.However,because the
P.simus vocal repertoire is distinct and extensive (Bergey and
Patel,2008) and its feeding traces on giant bamboo (Cathariostachys madagascariensis) are unmistakable, attention to such
indirect evidence of P. simus presence should be focused
upon in all surveys.
The report from Makira, if confirmed, is especially interesting, since the northernmost former record for the species
(other than from subfossils) comes from Antongil Bay
(Schwarz, 1931).
Our experience shows that accounts of villagers are mostly
reliable, and that people usually have a good sense of what
animal species do or do not occur in their vicinity.Therefore,
integrating local people is crucial for further studies into
Prolemur distribution. Logically, collaboration with local people is one conservation recommendation given by the Prolemur Conservation Working Group (Madagascar Fauna
Group, 2010).
Based on information compiled,we tentatively conclude that
P. simus is still more widespread than previously thought.
Without sufficient data, given persisting threats to the habitats in which it occurs and our incomplete understanding of
habitat requirements for the species, we do not dare say that
a larger distribution area contributes in any way to relieving
the species from extinction pressure. Unfortunately, P. simus
still has to be considered one of the most threatened primates in the world.
Acknowledgements
We thank Tokiniaina Hobinjatovo for helping with literature
research and Coralie Ebert for additional information. We
thank all individuals that have shared their observations and
made available the information presented here. We would
also like to thank the Margot Marsh Biodiversity Fund, and
the National Geographic Society Conservation Trust Award
#C135-08.
References
ADEFA. 2009. Stages. Bulletin d’Information de l’Association
de Défense de la forêt d’Ambodiriana 25: 1-2.
Beaucent, S.; Fayolle, M. 2008. Etude de la communauté de lémuriens de la forêt d’Ambodiriana,NE Madagascar.Lemur
News 13: 28-32.
Bergey, C.; Patel. E.R. 2008. A preliminary vocal repertoire of
the Greater Bamboo Lemur (Prolemur simus): classification and contexts. Nexus 1: 69-84.
Dolch, R.; Fiely, J.L.; Ndriamiary, J.N.; Rafalimandimby, J.; Randriamampionona,R.;Engberg,S.E.;Louis,E.E.Jr.2008.Confirmation of the greater bamboo lemur, Prolemur simus,
north of the Torotorofotsy wetlands, eastern Madagascar.
Lemur News 13: 14-17.
Dolch, R.; Hilgartner, R.D.; Ndriamiary, J.N.; Randriamahazo,
H.2004.The grandmother of all bamboo lemurs:evidence
Page 34
for the occurrence of Hapalemur simus in fragmented
rainforest surrounding the Torotorofotsy marshes, central eastern Madagascar. Lemur News 9: 24-26.
Evans, M.I.; Thompson, P.M.; Wilson, A. 1993-1994. A survey
of the lemurs of Ambatovaky special reserve, Madagascar.
Primate Conservation 14/15: 13-21.
Ganzhorn, J. U. 2004. Editorial. Lemur News 9: 1.
Godfrey, L. R.; Vuillaume-Randriamanantena, M. 1986. Hapalemur simus: endangered lemur once widespread. Primate
Conservation 7: 92-96.
Godfrey,L.R.;Jungers, W.L.;Reed, K.E.; Simons, E.L.;Chatrath,
P.S. 1997. Subfossil lemurs: Inferences about past and present primate communities. Pp.218-256.In: S.M.Goodman;
B. Patterson (eds.). Natural Change and Human Impact in
Madagascar. Smithsonian Institution Press, Washington
D.C.
Golden, C. D. 2009. Bushmeat hunting and use in the Makira
Forest, north-eastern Madagascar: a conservation and
livelihoods issue. Oryx 43: 386-392.
Goodman,S.M.;Ganzhorn,J.U.2004.Biogeography of lemurs
in the humid forests of Madagascar:the role of elevational
distribution and rivers. J. Biogeography 31: 47-55.
King, T., Chamberlan, C. 2010. Conserving the critically endangered Greater Bamboo Lemur. Oryx 44: 165-170.
Madagascar Fauna Group.2010.Conservation of the critically endangered greater bamboo lemur Prolemur simus:
What we know now,what we need to know and potential
conservation strategies. International Technical Meeting
Final Report, Antananarivo 26-28 January 2010. Madagascar Fauna Group.
Meier, B.; Rumpler, Y. 1987. Preliminary survey of Hapalemur
simus and of a new species of Hapalemur in eastern Betsileo, Madagascar. Primate Conservation 8: 40-43.
Mittermeier, R.A.; Konstant, W.R.; Hawkins, F.; Louis, E. E.;
Langrand, O.; Ratsimbazafy, J.; Rasoloarison, R.; Ganzhorn,
J.U.; Rajaobelina, S.; Tattersall, I.; Meyers, D.M. 2006. Lemurs of Madagascar.Tropical Field Guide Series.Washington DC, Conservation International.
Napier, J. R.; Napier, P. H. 1967. A Handbook of Living Primates. Academic Press, New York.
Patel, E.R. 2009. Silky Sifaka, Propithecus candidus. Pp. 84. In:
R.A. Mittermeier; J. Wallis; A.B. Rylands; J.U. Ganzhorn; J.F.
Oates; E.A. Williamson; E. Palacios; E.W. Heymann;M.C.M.
Kierulff; Y. Long;J. Supriatna; C. Roos;S. Walker; L. CortésOrtiz;C.Schwitzer (eds.). Primates in peril: the world’s 25
most endangered primates, 2008-2010. IUCN/SSC
Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation International (CI),
Arlington, VA.
Petter, J.J.; Albignac, R.; Rumpler, Y. 1977. Mammiferes Lémuriens (Primates Prosimiens). Faune de Madagascar 44.
Paris: Office de la Recherche Scientifique et Technique
d’Outre-Mer (ORSTOM)/Centre National de la Recherche Scientifique (CNRS).
Ralison,J. M.2006.A lemur survey of the Réserve Spéciale de
Marotandrano, Madagascar. Lemur News 11: 35-37.
Rasolofoson, D.; Rakotondratsimba, G.; Rakotonirainy, O.;
Rasolofoharivelo, T.; Rakotozafy, L.; Ratsimbazafy, J.; Ratelolahy, F.; Andriamaholy, V.; Sarovy, A. 2007. Le bloc forestier de Makira charnière de Lémuriens. Lemur News 12:
49-53.
Ratelolahy, F.J.; Raivoarisoa, F.M.J. 2007. Distribution et statut
de population de Propithèque Soyeux (Propithecus candidus) dans la forêt de Makira, région d’Anjanaharibe, Nord
Est de Madagascar.Report,Wildlife Conservation Society,
Antananarivo.
Ratsimbazafy,J.2010.Identification des sites prioritaires pour
la conservation de Prolemur simus dans le Bassin versant
de Nosivolo/Marolambo. Proposition de recherche, Projet Varibolomavo, The Aspinall Foundation.
Ravaloharimanitra, M.; Ratolojanahary, T.; Rafalimandimby, J.;
Rajaonson, A.; Rakotonirina, L.; Rasolofoharivelo, T.; Ndriamiary, J.N.; Andriambololona, J.; Nasoavina, C.; Fanomezantsoa, P.; Rakotoarisoa, J.C.; Youssouf, M.; Ratsimbazafy,
J.; Dolch, R.; King, T. 2010. Gathering indigenous knowledge in Madagascar results in a major increase in the
known range and number of sites for the critically endangered Greater Bamboo Lemur (Prolemur simus). Int. J. Primat. (in review).
Lemur News Vol. 15, 2010
Santini-Palka, M.E. 1994. Feeding behaviour and activity patterns of two Malagasy bamboo lemurs, Hapalemur simus
and Hapalemur griseus, in captivity. Folia Primatologica 63:
44-49.
Schmid, J.; Alonso, L.E. 2005. A rapid biological assessment of
the Mantadia-Zahamena Corridor, Madagascar. RAP Bulletin of Biological Assessment No. 32. Washington DC,
Conservation International.
Schwarz, E. 1931. A revision of the genera and species of
Madagascar Lemuridae. Proceedings of the Zoological
Society of London 1931: 399-428.
Sterling,E.;McFadden,K.2000.Rapid census of lemur populations in the Parc National de Marojejy, Madagascar. Fieldiana Zoology 97: 265-274.
Wright,P.C.;Johnson,S.E.;Irwin,M.T.;Jacobs,R.;Schlichting,P.;
Lehman, S.; Louis, E.E. Jr.; Arrigo-Nelson, S.J.; Raharison, J.
L.; Rafalirarison, R.R.; Razafindratsita, V.; Ratsimbazafy, J.;
Ratelolahy,F.J.; Dolch, R.;Tan,C.2008.The crisis of the critically endangered Greater Bamboo Lemur (Prolemur
simus). Primate Conservation 23: 5-17.
Wright, P.C.; Larney, E.; Louis, E.E. Jr., Dolch, R.; Rafaliarison,
R.R. 2009. Greater bamboo lemur, Prolemur simus (Gray,
1871). In: R.A. Mittermeier; J. Wallis; A.B. Rylands; J.U.
Ganzhorn; J.F. Oates; E.A. Williamson; E. Palacios; E.W.
Heymann; M.C.M. Kierulff; Y. Long; J. Supriatna; C. Roos; S.
Walker; L. Cortés-Ortiz; C. Schwitzer (eds.). Primates in
peril: the world’s 25 most endangered primates, 20082010. IUCN/SSC Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation
International (CI), Arlington, VA.
Enquête préliminaire de la distribution
des lémuriens de bambou dans et autour
du Corridor forestier Fandriana-Vondrozo, Madagascar
Andry Rajaonson1,2, Maherisoa Ratolojanahary2,
Jonah Ratsimbazafy1, Anna Feistner3, Tony King2*
1Groupe d’Etude sur les Primates de Madagascar (GERP),
Lot 34 Cité des Professeurs, Fort Duchesne, Ankatso, Antananarivo 101, Madagascar
2The Aspinall Foundation, BP 7170 Andravoahangy, Antananarivo 101, Madagascar
3Centre ValBio, BP 33 Ranomafana, Ifanadiana 312, Madagascar (present address: anna@feistner.com)
*Corresponding author: tonyk@aspinallfoundation.org
Mots-clés: Prolemur simus, Hapalemur aureus, Varecia variegata editorum, bambou
Introduction
Le Grand Hapalémur (Prolemur simus) mangeur de bambou,
est classé comme étant "gravement menacé CR" sur la liste
rouge de l’Union Internationale pour la Conservation de la
Nature (UICN, 2009).Il est aussi l’une des quatre espèces de
Madagascar faisant partie des 25 primates considérés
comme les plus menacés au monde (Mittermeier et al., 2007,
2009). Des individus capturés dans les années 1800 venaient
d’une région plus étendue, ce qui laisse supposer que son
habitat a diminué.Les sites de subfossiles avec des squelettes
identiques à celui de P. simus sont nombreux, impliquant une
distribution encore plus vaste à une époque très ancienne
(Godfrey et Vuillaume-Randriamanantena, 1986; Godfrey et
al., 2004).
Actuellement, la distribution géographique de l’espèce semble très étroite. On pense que P.simus est seulement présent
dans quelques fragments de forêt tropicale humide près de la
côte Est de Madagascar (Mittermeier et al.,2006 ;Dolch et al.,
2008;Wright et al.,2008).Wright et al.(2008) résume la crise
Lemur News Vol. 15, 2010
actuelle de l’espèce: sur les 70 localités étudiées, la présence
de P.simus est confirmée seulement sur 11 d’entre elles,à une
altitude comprise entre 121 et 1600 m.
La plupart des sites connus abritant P. simus se trouvent dans
ou autour du Corridor Fandriana-Vondrozo, dans le Sud-Est
du pays (Andriaholinirina et al.,2003;Meier et Rumpler,1987;
Sterling et Ramaroson, 1996; Wright et al., 1987, 2008; Mittermeier et al., 2009). Deux autres espèces de lémuriens de
bambou vivant dans le corridor, Hapalemur aureus et H.
griseus, sont aussi menacées (Mittermeier et al., 2006; IUCN,
2009).Notons que P. simus est le plus grand des lémuriens de
bambou,avec un pelage gris brun (comme H. griseus).Il se distingue facilement des deux autres espèces par des touffes de
poils blancs sur les oreilles. Sa face est aussi plus allongée, et
on le trouve souvent au sol, alors que les autres espèces y
sont rarement (Wright et al., 1987). Selon l’étude de Tan
(1999) à Ranomafana, le régime alimentaire de P. simus est
constitué à 95 % d’une seule espèce de bambou Cathariostachys sp. (ou volohosy dans le dialecte local malgache), 3 %
d’autres espèces de bambous et de graminées,0,5 % de fruits
et 1,5 % d’autres éléments (principalement de la terre et des
champignons).
La présente étude a été organisée dans le cadre du Projet
Varibolomavo proposé par The Aspinall Foundation (TAF).
Ce projet veut mettre en place des actions rapides, efficaces
et collaboratives pour sauver Prolemur simus. Plus précisément, le deuxième objectif du projet est d’organiser une
étude de la distribution et de l’abondance de P. simus (TAF,
2008, 2009; King and Chamberlan, 2010). Par conséquent, le
but de cette étude était de contribuer à réaliser ces objectifs,
dans et autour du corridor Fandriana-Vondrozo, par a) la
récolte des connaissances indigènes locales sur les distributions des lémuriens; et b) la recherche des signes de présence des lémuriens de bambou. Nous présentons ici un
résumé des résultats de l’étude, exposés de façon plus
détaillée par Ratolojanahary et al. (2009).
Méthodes
Entre les 27 novembre 2008 et 25 mai 2009, nous avons enquêté dans 14 zones situées dans et autour du Corridor
Fandriana-Vondrozo (Tab. 1, Fig. 1). Pour chaque commune,
des entretiens avec les autorités locales ont eu lieu. Des collaborations avec ces personnes ont permis d’organiser les
réunions villageoises pour mener les enquêtes participatives,
à l’aide de photos des espèces de lémuriens supposées
coexister dans ce couloir forestier (Prolemur simus, Hapalemur aureus, H. griseus, Eulemur rufus, E. rubriventer, Propithecus edwardsi, Varecia variegata editorum, Microcebus rufus,
Cheirogaleus major, Avahi laniger, Lepilemur microdon, Daubentonia madagascariensis). Les appellations locales des différentes espèces connues par les communautés villageoises
ont été relevées lors de chaque enquête.De plus,nous avons
utilisé la méthode de cartographie participative (Jones et al.,
2005) durant la réunion dans les communes de Mahazoarivo,
Iandraina, Sahamadio et Evato. Suite aux résultats des enquêtes villageoises, nous avons visité des forêts et sites
intéressants dans la région, toujours accompagnés par un
guide local et des agents de recherche du Centre ValBio de
Ranomafana. Nous nous arrêtions tous les 25 mètres pour
relever la localisation des bambous et des espèces de lémuriens, ainsi que les signes de présence de ces dernières.
La présence des espèces de lémuriens était révélée soit par
l’observation directe (animal vu), soit par l’observation indirecte (signes de nourrissage,excréments ou vocalisation).La
recherche des signes de nourrissage des lémuriens de bambou était faite dans les zones de bambous, et les signes
Page 35
Tab. 1: Les zones visitées pendant l’enquête.
Zone
Sites visités
Zones situées dans le corridor forestier
Ambendrana
1
Amindrabe
1
Ambodiara
1
Antarehimamy
1
Dates
27-28 nov 2008
29 nov - 1 déc 2008
11-13 déc 2008
14-16 déc 2008
29 jan - 6 fév 2009 (dont TsiaAntaranjaha
4
nivoho et Ambolomadinika)
Manambolo
1
9-11 mai 2009
Zones situées autour du corridor forestier
Mananjary
4
14-16 jan 2009
Sahalanona
9
17-23 jan 2009
Manakara
1
25 jan 2009
Mahazoarivo
2
18-19 mai 2009 (dont Ifasy)
Iandraina
1
21 mai 2009
Sahamadio
1
22-23 mai 2009
Evato
0
24-25 mai 2009
Mahafasa
0
25 mai 2009
14 zones
27 sites
27 nov 2008 - 25 mai 2009
Fig. 1: Les sites visités lors de l’enquête dans et autour du
Corridor forestier Fandriana-Vondrozo.
étaient examinés précautionneusement afin d’identifier l’espèce qui en était responsable. Prolemur simus préfère surtout
les bambous de grand diamètre, et les parties de bambou
privilégiées varient avec les saisons.Entre juillet et novembre,
P. simus consomme principalement la moelle tendre de
bambou géant (Tan, 1999), après avoir ouvert la tige en deux
et l’avoir déchirée en petits morceaux (Wright et al., 1987).
Ainsi, l’échantillon à rechercher devrait être des tiges déchirées sans ou avec peu de moelle.Par contre,entre novembre
et avril, il se concentre sur les jeunes pousses (Tan, 1999),
donc les échantillons devraient être des bouts de jeunes
pousses de bambou géant. Avec de l’expérience, il est égale-
Page 36
ment possible de distinguer les signes laissés sur les feuilles
de bambou. P. simus se nourrit des jeunes feuilles matures et
ne consomme pas la partie tranchante de la feuille. Par
contre, Hapalemur aureus et H. griseus consomment uniquement la base de la feuille, H. aureus déchirant la gaine de
chaume à l’aide de ses dents avant de manger les branches.
Lemur News Vol. 15, 2010
rissage et émis des cris. La présence de huit autres espèces
de lémuriens a également été constatée (Tab. 2). L’une d’entre elles, Varecia variegata editorum, est une sous-espèce
gravement menacée selon l’UICN (2009), et les détails de
toutes les observations de cette espèce sont présentés dans
le Tab. 4.
Résultats par zone située dans le corridor forestier de FandrianaVondrozo
Ambendrana: Le village d’Ambendrana (S21°22’44.9" E 047°
Espèces de lémuriens recensées
18’31.0",altitude 1121 m) est placé sous l’autorité de la comLes populations locales ont souvent des noms vernaculaires
mune rurale d’Androy et situé à une vingtaine de kilomètres
distincts pour les différentes espèces de lémuriens. En outre,
au sud du Parc National de Ranomafana. Ce village est ennous avons remarqué qu’ils ne pouvaient pas toujours identitouré de rizières localisées tout autour du corridor. La forêt
fier les espèces sur les photos, alors qu’ils pouvaient les red’Ambendrana a une superficie de 1.496 hectares et est
connaître dans la nature. Les informations récoltées lors des
gérée par la communauté de base depuis 2003. Au cours de
enquêtes villageoises doivent donc être utilisées avec prél’enquête, les villageois n’ont reconnu que 3 espèces de
caution et sont toujours à vérifier sur le terrain. Durant les
lémuriens des 12 présentées sur les photos, notamment
vérifications, nous n’avons trouvé qu’un seul site présentant
l’espèce Hapalemur griseus. D’après nos observations, la
des signes de nourrissage de Prolemur simus (Tab. 2). Par
forêt d’Ambendrana est perturbée. Cependant, nous avons
contre, nous avons effectué 39 observations (directes et
pu localiser quelques groupes de lémuriens, dont un groupe
indirectes) de Hapalemur griseus, dans 10 des 12 zones viside H. griseus, et des signes de nourrissage.
tées (Tab. 2), et huit observations (indirectes) de H. aureus
Amindrabe: La forêt d’Amindrabe a une superficie de 5.800
(Tab.3).Toutes ces observations ont été faites dans les zones
hectares et est également gérée par la communauté de base
situées au sein du corridor forestier, mais aucune dans ses
depuis 2003. Cette forêt est située à 5,7 km du village d’Amalentours (Tab. 2). Cette espèce a laissé des signes de nourbendrana. Le Fokontany Amindrabe (S21°
23’14.8" E047°21’ 46.4", altitude 1096 m)
Tab. 2: Espèces de lémuriens rencontrées dans chaque zone.
fait également partie de la commune rurale d’Androy et comprend plusieurs vilZone
Hapalemur Hapalemur Prolemur
Autres espèces
griseus
aureus
simus
lages. Durant l’enquête, les villageois ont
Zones situées dans le corridor forestier
reconnu 5 espèces de lémuriens, dont H.
E rubriventer (vu)
griseus. Pendant l’expédition dans le site
Ambendrana
vu & signes
signe
Microcebus sp. (nid)
d’Amindrabe, deux anciens signes de
P. edwardsi (vu et entendu)
signe
Amindrabe
vu & signes
signe
nourrissage (vieux d’environ un an d’après
(environ 1 an) D. madagascariensis (signes)
nos constatations) de P.simus ont été trouAmbodiara
V. variegata (entendu)
signes
signes
vés sur le tronc d’une espèce de bambou
Antarehimamy
V. variegata (entendu)
signes
signes
localement appelé Volotsangana (S21º24’
V. variegata (entendu)
signes &
Antaranjaha
signes
E. rufus (vu)
entendus
22.5", E047º23’07.2", altitude 1055 m).
Manambolo
E. rufus (vu) E. rubriventer (vu)
signes
Nous avons également trouvé deux
Zones situées autour du corridor forestier
groupes de H. griseus, des Propithecus edSahalanona
M. rufus et A. laniger à vendre
vus & signes
wardsi et des signes d’alimentation de DauMicrocebus sp. (nid)
bentonia madagascariensis, attestant de la
Mananjary
vus & signes
Cheirogaleus sp. (signes)
grande diversité de ce site en espèces de
Manakara
E. rufus (vu) A. laniger (vu)
lémuriens.
Mahazoarivo
vus
Ambodiara: Le Fokontany d’Ambodiara
Iandraina
signes
(S21°54’41.3", E047°23’29.2, altitude
Sahamadio
signes
346 m) existe depuis 1910 et est composé
de 8 villages. Le village d’Ambodiara est
Tab. 3: Observations de Hapalemur aureus faites pendant l’étude.
situé à 5,9 km, c’est-à-dire à environ 3
heures de marche à l’ouest d’Ikongo. Au
Zone
Remarque
Latitude
Longitude
Altitude (m)
cours de l’enquête, les villageois ont reAmbendrana
signe de nourrissage S 21º 22’ 22.7" E 047º 20’ 46.5"
1182
connu 9 espèces de lémuriens, dont HapaAmindrabe
signe de nourrissage S 21º 24’ 13.1" E 047º 22’ 47.7"
1070
lemur aureus, H. griseus et également ProAmbodiara
signe de nourrissage S 21º 53’ 27.0" E 047º 21’ 18.9"
825
lemur simus. D’après nos observations, la
Antarehimamy signe de nourrissage S 21º 54’ 47.5" E 047º 20’ 38.4"
1074
forêt d’Ambodiara est perturbée. Nous
Antaranjaha
signe de nourrissage S 21º 58’ 20.3" E 047º 20’ 16.7"
828
n’avons pas trouvé P. simus sur ce site, mais
Antaranjaha
entendu des cris
S 21º 58’ 25.3" E 047º 20’ 17.7"
783
nous avons constaté la présence de CathaAntaranjaha
signe de nourrissage S 21º 58’ 39.1" E 047º 19’ 43.8"
786
riostachys sp. Par contre, Varecia variegata
Manambolo
signes de nourrissage S 22º 04’ 06.2" E 046º 59’ 27.5"
1238
editorum abonde dans cette localité, et
nous avons trouvé des signes de nourTab. 4: Observations de Varecia variegata faites pendant l’étude.
rissage de H. aureus et H. griseus.
Antarehimamy: Situé dans le district
Zone
Remarque
Latitude
Longitude
Altitude (m)
Ambodiara
entendu des cris
S 21º 53’ 17.4" E 047º 21’ 42.3"
500
d’Ikongo, le village d’Antarehimamy (S21°
Ambodiara
entendu des cris
S 21º 53’ 17.7" E 047º 21’ 34.5"
825
55’59.2", E047°22’17.6", altitude 410 m) se
Antarehimamy
entendu des cris
S 21º 55’ 00.4" E 047º 22’ 10.3"
489
situe à 3,16 km au Nord-Est d’Ambodiara
Antaranjaha
entendu des cris
S 21º 58’ 23.6" E 047º 20’ 15.4"
828
et à 9,01 km à l’ouest de la commune
Antaranjaha
entendu des cris
S 21º 58’ 31.5" E 047º 20’ 13.6"
743
rurale d’Ikongo.Lors de l’enquête,les villaRésultats et Interprétations
Lemur News Vol. 15, 2010
geois ont reconnu 7 espèces de lémuriens, mais aucun lémurien de bambou.Néanmoins,nous avons trouvé des signes de
nourrissage de Hapalemur aureus et H. griseus. Nous avons
également remarqué l’abondance de Varecia variegata editorum sur le site.
Antaranjaha/Ambolomadinika/Tsianivoho:Située dans le district d’Ikongo, la commune d’Ambolomadinika gère 12
Fokontany, dont Antaranjaha et Tsianivoho. Le Fokontany
Antaranjaha (S21°59’42.3", E047°25’40.2") est situé à 3,7 km
au Sud-Ouest d’Ambolomadinika. Dans ce site, les villageois
n’ont pas reconnu de lémuriens de bambou. Cependant, des
cris de Hapalemur aureus ont été entendus dans la forêt à
150 m environ de notre campement, c’est-à-dire à Ankazondrano.A Marofototra,situé à 30 minutes du Fokontany d’Antaranjaha, toutes les jeunes pousses de bambou Cathariostachys sp.étaient coupées.Ce sont des signes de nourrissage de
H. griseus. De plus, un villageois a confirmé avoir trouvé un
groupe de H. griseus comprenant 12 individus à cet endroit.
Nous avons également entendu des cris de Varecia variegata
editorum, vu un groupe de Eulemur rufus, et trouvé un piège à
lémuriens dans la forêt. Dans la commune rurale d’Ambolomadinika, on remarque beaucoup de zones agricoles déboisées. Malheureusement, les lémuriens de bambou sont menacés à cause de la coupe massive de bambous dans ces
zones et la chasse pratiquée par les habitants de la Commune.
Manambolo:Située dans la région de Fianarantsoa,la forêt de
Manambolo (S22°04’06.2",E046°59’27.5",1238 m) se trouve
dans le Fokontany de Morafeno, commune rurale de Sendrisoa. La gestion de la forêt est assurée par le FI.TE.MA
(FIkambanan’ny TEraky MAnambolo) et concerne cinq villages: Mandamako, Mahavita, Ambinda, Ankazobe, Ampidira.
La survie de la population locale dépend largement de l’agriculture, l’élevage et la production du rhum traditionnel.
Cependant, la culture sur brûlis est encore pratiquée sur la
lisière forestière. Lors de l’enquête, les villageois ont reconnu 4 espèces de lémuriens, dont Hapalemur griseus et H.
aureus. La vérification en forêt nous a révélé des signes de
nourrissage de H. aureus, et nous avons vu directement Eulemur rufus et E. rubriventer.
Résultats par zone située autour du corridor forestier de Fandriana-Vondrozo
Mananjary: Notre campement à Tsararivotra (S21°10’41.8",
E048°13’19.6", altitude 39 m) était situé à 23 km au nordouest de la ville de Mananjary. Le site de Tsararivotra est
inclus dans le Fokontany de Volomborona Asakatara et fait
partie de la commune de Morafeno Mananjary.Nous n’avons
trouvé que Hapalemur griseus, Cheirogaleus major et Microcebus rufus dans cette zone.
Sahalanona: La commune de Sahalanona fait partie du
District d’Ikongo et inclut 9 Fokontany (Sahalanona, Mahaly,
etc.). La population est composée d’agriculteurs, d’éleveurs
et de pêcheurs. Le village de Sahalanona (S22°03’19.2"
E047°37’ 12.2", altitude 129 m) existe depuis environ 300
ans. Malgré l’abondante présence de bambous, dont le
bambou géant Cathariostachys sp., nous n’avons trouvé que
Hapalemur griseus dans cette zone. Cette espèce est menacée par la chasse que pratiquent les villageois. D’autres
espèces de lémuriens sont également en danger car elles
sont aussi chassées et vendues par les villageois, notamment
Avahi laniger (chassé pour l’alimentation et l’usage domestique) et Microcebus rufus (dont le prix est de 5.000 Ariary
par individu).
Manakara: Le village d’Ambila se trouve à 17 km au nord de
Manakara. Le Fokontany Ambila fait partie de la commune
Page 37
d’Ambila (S22°00’11.6", E047°58’19.9") de la région de Manakara. Notre observation a été effectuée directement dans
la forêt de Tsiazombazaha située à 10 km du village d’Ambila.
L’enquête n’a pas eu lieu dans ce site car il n’y avait plus de
village (principalement notre cible) autour de la forêt. Cette
forêt est gérée par la communauté de base du Fokontany
d’Ambila. A cet endroit, nous n’avons pas trouvé de bambou,
et avons trouvé seulement deux espèces de lémuriens, Avahi
laniger et Eulemur rufus, après vérification dans la forêt.
Mahazoarivo/Ifasy: Située dans la région de Farafangana, la
commune de Mahazoarivo (S22°39’49.0", E047°18’42.4",
222 m) fait partie du corridor forestier, et la population pratique l’agriculture et l’élevage. L’exploitation des ressources
minières, surtout des pierres précieuses, représente une
source de revenus importante pour la population. Lors de
l’enquête, les villageois n’ont reconnu que deux espèces de
lémuriens, Hapalemur griseus et Microcebus rufus. Nous avons
visité deux forêts dans cette commune,à Mitimboto (Fokontany de Mahazoarivo) et Ifasy ou Mahafasy (Fokontany Mahatsara) où deux groupes de H. griseus ont été vus sur chaque
site. A Ifasy (S22°39’13.0", E47°14’56.1"), des individus de H.
griseus de très grande taille ont été localisés, similaires à
Prolemur simus, mais l’absence des touffes de poils blancs sur
les oreilles nous a permis de faire la distinction. Nous avons
également remarqué que le nom local de H. griseus était
différent à Mitimbato et Ifasy, respectivement Varibolo madinika et Varibolo vaventy.
Iandraina: Le Fokontany d’Iandraina fait partie de la commune Rurale de Vohimasy. Il se situe à 15 km au nord-ouest
de Farafangana. La forêt de Befoza et celle d’Ambolosy
(S22°46’07.0", E047°41’07.0", 53 m) se trouvent dans ce
fokontany. Les populations sont constituées principalement
d’agriculteurs et d’éleveurs. La pratique des cultures vivrières constitue l’activité principale. Contrairement aux
autres sites que nous avons visités dans le sud de la zone
d’étude, nous avons trouvé une population de Cathariostachys sp. à Ambolosy.
Sahamadio: Située dans la région de Farafangana, cette zone
est plus ou moins enclavée (absence d’infrastructure routière) et même la circulation et le transport de produits
locaux s’effectuent toujours par pirogue.La commune rurale
de Sahamadio (S22°31’13.4", E047°35’02.8", altitude 27 m)
dépend beaucoup de l’agriculture. L’existence de signes de
nourrissage dans la forêt de Sahamadio nous a permis d’établir que Hapalemur griseus,localement appelé "varibolo" y est
présent.L’enquête effectuée au niveau de la commune rurale
d’Ambalatany a également confirmé la présence de lémuriens de bambou de grande taille dans la forêt d’Ambalakazaha.
Evato:Dans la commune d’Evato (S 22°36’42",E 047°41’20"),
dans la région de Farafangana, le développement des différentes infrastructures est remarquable,citons comme exemple les hôpitaux, écoles, marchés et routes en bon état. Un
bloc de forêt primaire se trouve à Iaboloha dans cette
commune. Notre enquête nous a donné des informations
sur la présence de plusieurs espèces de lémuriens dans cette
forêt. Ce site mérite donc d`être visité pour une prochaine
vérification.
Mahafasa: Dans cette zone située également dans la région
de Farafangana, ce qui reste de forêt primaire est en général
la forêt de bambou,un endroit où se trouvent des tombeaux.
Etant donné la situation actuelle de sécurité, nous n’avons
pas obtenu la permission de visiter cette forêt sacrée de
bambou. Cette dernière recouvre une grande surface, environ 3 km de longueur et jusqu’à 100 m de largeur,et pourrait
être importante en tant qu’habitat de lémuriens.
Page 38
Discussion
La série d’expéditions menée le long du Corridor forestier
Fandriana - Vondrozo nous a permis d’évaluer provisoirement la répartition des lémuriens de bambou. Concernant
Prolemur simus, un seul signe de nourrissage a été identifié, et
ce signe remontait à un an, confirmant les résultats des
études précédentes qui indiquent que l’espèce a une distribution fragmentée dans la région (Wright et al., 2008). Pour
Hapalemur aureus (espèce menacée EN), la découverte de
l’évidence de sa présence sur six zones, toutes dans le corridor forestier, est encourageante car cela implique une large
distribution dans celui-ci, bien que l’espèce ne semble pas
exister en-dehors.Hapalemur griseus (espèce vulnérable VU)
a été trouvé dans presque toutes les zones visitées, dans le
corridor forestier mais également dans des zones éloignées
de ce dernier.
La menace principale pour les espèces de bambou dans la
région du corridor Fandriana-Vondrozo est la destruction
des habitats naturels et leur conversion en champs de culture.Cette technique est appelée "agriculture sur brûlis".Par
conséquent, cette pression entraîne la raréfaction et même
la disparition des espèces autochtones de bambous. Malgré
la présence de bambous à l’intérieur du corridor, la persistance de la pratique du tavy, les coupes de bambous en permanence et surtout la chasse aux lémuriens mettent en péril
la survie des espèces de lémuriens. En outre, la taille de la
forêt du Corridor Fandriana-Vondrozo est petite par rapport aux autres corridors forestiers du pays. Sa largeur est
très réduite surtout dans sa partie sud, et sur la photo
aérienne, la voûte forestière apparaît très ouverte. Tous ces
facteurs menacent la viabilité des populations de lémuriens
vivant dans le corridor, et tout particulièrement les espèces
présentant une distribution fragmentée telles que P. simus.
Actuellement, beaucoup de lémuriens sont chassés et vendus par les villageois (exemple: Sahalanona,Antaranjaha). Les
forêts de bambous sont fragmentées et isolées les unes des
autres, ce qui laisse à penser que ces lémuriens de bambou
sont réellement en danger. En outre, les utilisations des
bambous dans la région sont nombreuses. La population locale utilise les différentes espèces de bambou suivant leur
taille pour la construction des maisons, particulièrement
pour les toitures, les murs, et des clôtures. Les bambous
servent également à fabriquer du matériel pour les usages
quotidiens, parmi lesquels les paniers à fruits, volailles, écrevisses et anguilles. Enfin, ils permettent de transporter des
bagages. Aussi, les espèces de bambous de plus grand diamètre sont utilisées comme récipient pour transporter de
l’eau. La conséquence négative de l’utilisation des bambous
est minime par rapport à la destruction des habitats. Exemple: le Corridor d’Ampitsinjovabe (site d’Antarehimamy) est
une bonne localité pour trouver H. griseus, H. aureus et V.
variegata editorum, mais ces trois espèces sont menacées à
cause de la chasse et des coupes sélectives de bois pratiquées par les habitants résidant autour du corridor.
Pour la conservation de Prolemur simus,il faudrait accroître la
taille des aires protégées en y incluant les forêts de bambous,
et restaurer les fragments d’habitats isolés au sein d’un
paysage agricole déboisé, afin d’équilibrer la valence écologique, c’est-à-dire la zone supportable pour l’espèce (en
pratiquant une reforestation de bambou). Cependant, d’une
façon générale, il y a un besoin immédiat de sensibilisation,
pour conscientiser la population aux problèmes de coupe de
bambous,de tavy et de chasse des lémuriens, afin d’assurer la
survie d’espèces de lémuriens dans et autour du Corridor
Fandriana-Vondrozo. Finalement, les sites d’Ambodiara, Mahazoarivo (Alafady, Ranomena), Ambalakazaha et Mahafasa
Lemur News Vol. 15, 2010
sont recommandés pour une nouvelle vérification de la présence ou non des lémuriens de bambou. En effet, la population locale semble être convaincue d’avoir trouvé P. simus à
ces endroits.
Remerciements
Nos vifs remerciements vont: au Ministère de l’Environnement, des forêts et du Tourisme, à la Direction Générale de
l’Environnement et des forêts, et à la Direction du Système
des Aires Protégées, Madagascar, pour leur accord et la
délivrance de l’autorisation de recherche (permis n°279/08/
MEFT/SG/DGEF/DSAP/SSE); à The Aspinall Foundation, GB,
pour le financement de l’enquête dans le cadre du Projet
"Sauver Prolemur simus"; au Groupe d’Etude et de Recherche
sur les Primates de Madagascar (G.E.R.P) et son personnel
administratif; au Centre International de Formation pour la
Valorisation de la Biodiversité (Centre ValBio) et son personnel administratif; à l’ICTE et Conservation International,
Antananarivo,pour leurs conseils et entire collaboration;aux
communes, Fokontany, et COBAS des zone visitées pour
leurs amabilité et collaboration; et enfin, aux assistants de
recherche du Centre ValBio à Ranomafana, Justin Rakotonjatovo, Dominique Razafindraibe, Jean-Guy Razafindraibe,
Aime-Victor Tombotiana et Telo Albert, et au chauffeur de
The Aspinall Foundation,Mohamad Mbaraka,pour leur assistance sur le terrain.
Références
Andriaholinirina, V.N.; Fausser J.L.; Rabarivola, J.C. 2003. Etude comparative de Hapalemur simus (Gray, 1870) de deux
sites de la province autonome de Fianarantsoa, Madagascar:forêt dégradée d’Ambolomavo et forêt secondaire de
Parc National de Ranomafana. Lemur News 8: 9-13.
Dolch, R.; Fiely, J.L.; Ndriamiary, J.N.; Rafalimandimby, J.; Randriamampionona, R.;Engberg,S.E.;Louis,E.E.Jr.2008.Confirmation of the greater bamboo lemur, Prolemur simus,
north of the Torotorofotsy wetlands, eastern Madagascar.
Lemur News 13: 14-17.
Godfrey, L.; Vuillaume-Randriamanantena, M. 1986. Hapalemur simus: endangered lemur once widespread. Primate
Conservation 7: 92-96.
Godfrey, L.R.; Simons, E.L.; Jungers, W.L.; DeBlieux, D.D.;
Chatrath, P.S.2004.New discovery of subfossil Hapalemur
simus, the greater bamboo lemur, in western Madagascar.
Lemur News 9: 9-11.
Jones,J.P.G.;Andriahajaina,F.B.;Hockley,N.J.;Balmford,A.;Ravoahangimala, O.R. 2005. A multidisciplinary approach to
assessing the sustainability of freshwater crayfish harvesting in Madagascar.Conservation Biology 19:1863-1871.
King, T.; Chamberlan, C. 2010. Conserving the critically endangered greater bamboo lemur Prolemur simus. Oryx 44:
167.
Meier, B.; Rumpler, Y. 1987. Preliminary survey of Hapalemur
simus and of a new species of Hapalemur in eastern Betsileo, Madagascar. Primate Conservation 8: 40-43.
Mittermeier, R.A.; Konstant, W.R.; Hawkins, F.; Louis E.E.;
Langrand, O.; Ratsimbazafy, J.; Rasoloarison, R.; Ganzhorn,
J.U.; Rajaobelina, S.; Tattersall, I.; Meyers, D.M. 2006. Lemurs of Madagascar. 2nd ed. Conservation International,
Washington, D.C.
Mittermeier, R.A.; Ratsimbazafy, J.; Rylands, A.B.; Williamson,
L.;Oates,J.F.;Mbora,D.;Ganzhorn,J.U.;Rodriguez-Luna,E.;
Palacios, E.; Heymann, E.W.; Cecilia, M.; Kierfull, M.; Yongcheng,L.;Supriatna,J.;Roos,C.;Walker,S.;Aguiar,J.M.2007.
Primates in Peril: The World’s 25 Most Endangered Primates 2006-2008. Primate Conservation 22: 1-40.
Mittermeier, R.A.; Wallis, J.; Rylands, A.B.; Ganzhorn, J.U.;
Oates, J.F.; Williamson, E.A.; Palacios, E.; Heymann, E.W.;
Kierulff, M.C.M.;Yongcheng,L.;Supriatna,J.;Roos,C.;Walker, S.; Cortés-Ortiz, L.; Schwitzer, C. 2009. Primates in
Peril: The World’s 25 Most Endangered Primates 20082010. Primate Conservation 24: 1-57.
Ratolojanahary,M.;Rajaonson,A.;Ratsimbazafy,J.;Feistner,A.;
King, T. 2009. Identification des sites prioritaires pour la
Lemur News Vol. 15, 2010
conservation de Prolemur simus par la récolte des connaissances indigènes locales sur les distributions respectives
du bambou et des hapalémurs dans et autour du corridor
Fandriana-Vondrozo: Rapport Final. GERP / The Aspinall
Foundation / Centre ValBio, Madagascar. 25 pp.
Sterling E.J.; Ramaroson, M.G. 1996. Rapid assessment of the
primate fauna of the eastern slopes of the Réserve Naturelle Intégrale d’Andringitra, Madagascar. In: S.M. Goodman (ed.), A Floral and Faunal Inventory of the Eastern
Slopes of the RPserve Naturelle Intégrale d’Andringitra,
Madagascar, with Reference to Elevational Variation. Fieldiana Zoology 85: 293-305.
TAF 2008. Projet Varibolomavo: Sauver Prolemur simus - Objectifs et actions proposées. The Aspinall Foundation,
Port Lympne Wild Animal Park, Kent, GB. 4 pp.
TAF 2009. Projet Varibolomavo: Sauver Prolemur simus - Premiers résultats et actions immédiates. The Aspinall Foundation, Antananarivo, Madagascar. 6 pp.
Tan, C.L, 1999.Group Composition, Home Range Size, and
Diet of Three Sympatric Bamboo lemur species (genus
Hapalemur) in Ranomafana National Park, Madagascar.
International Journal of Primatology 20(4): 547-566.
UICN 2009. IUCN Red List of Threatened Species. Version
2009.2. www.iucnredlist.org.
Wright P.C.; Daniels P.S.; Meyers, D.M.; Overdorff, D.J.; Rabesoa, J.A. 1987. Census and study of Hapalemur and Propithecus in Southeastern Madagascar.Primate Conservation
8: 84-88
Wright,P.C.;Johnson,S.E.;Irwin,M.T.;Jacobs,R.;Schlichting,P.;
Lehman, S.; Louis, E.E. Jr.; Arrigo-Nelson, S.J.; Raharison,
J.-L.; Rafalirarison, R.R.; Razafindratsita, V.; Ratsimbazafy, J.;
Ratelolahy, F.J; Dolch, R.; Tan, C. 2008. The Crisis of the
Critically Endangered GreaterBamboo Lemur (Prolemur
simus). Primate Conservation 23: 5-17.
Effect of red ruffed lemur gut passage on
the germination of native rainforest plant
species
Onja H. Razafindratsima1,2*, Emilienne Razafimahatratra1
1Department of Animal Biology, University of Antananarivo,
Madagascar
2Department of Ecology and Evolutionary Biology, Rice University – MS 170, 6100 Main St., Houston, TX 77005, USA
(current affiliation)
*Corresponding author: ohr1@rice.edu, onjhar@hotmail.com
Key words: seed dispersal, germination success, Varecia
rubra, primate, corridor restoration, Masoala
Abstract
Like much of Madagascar’s remaining rainforest, the forest of
Masoala National Park is facing severe threats from deforestation and fragmentation. The remaining fragmented areas
are connected by degraded corridors which are important
for biological exchange. Frugivorous animals such as lemurs
may have an important role in the restoration of such degraded areas through seed dispersal. Unfortunately, no studies have been carried out before concerning the role lemurs
play in the restoration of the largest corridor in Masoala,
Ambatoledama. This study explores the effect of seed passage inside the gut of the frugivorous red-ruffed lemur
(Varecia rubra) on the germination of some native tropical
plants with the aim to understand the capacity of V. rubra to
help in the restoration of the Ambatoledama corridor. We
planted seeds of nine plant species that we collected from V.
rubra’s fresh feces in a nursery to compare with seeds that
we extracted manually from corresponding fruits. The germination of seeds was monitored each month after planting
Page 39
them. Results showed that defecated seeds had overall a significantly higher germination rate than non-passed seeds.
Thus, lemur ingestion of seeds has the capacity to improve
seed germination of several species and some plants require
the physiological treatment inside the gut to germinate. Results suggested that restoration projects in the area including
the Ambatoledama corridor should take into account the
important role Varecia rubra plays in the regeneration of the
forest and corridor.Management actions that increase movement and protection of animals moving into and out of the
corridor will be important for the long term success of the
project.
Introduction
The rainforest of the Masoala Peninsula suffers greatly from
loss and fragmentation caused by the human population
living around the area. The forest is subdivided into different
fragments, connected by corridors of degraded habitat
which are Ambatoledama,Analambolo and Ilampy (Holloway,
1997). Corridors are vital for enabling gene flow and dispersal of wildlife among habitat fragments (Mech and Hallett,
2001). The largest of these is the Ambatoledama corridor,
which connects two large parcels of the forest (Fig. 1). The
restoration of this corridor is critical for safeguarding wildlife
populations in the fragments and for preserving gene flow
between fragments (Mech and Hallett, 2001; Haddad et al.,
2003). To restore this degraded corridor, it is necessary to
plant native trees or to encourage zoochory (biological dispersal of seeds through animal defecation) (Duncan and
Chapman, 2002; Neilan et al., 2006). Since 1997, Madagascar
National Parks (MNP) and the Wildlife Conservation Society (WCS) have established a restoration project in the Ambatoledama corridor by planting native fruiting trees (Holloway,1997) with the aim of attracting frugivorous vertebrates
which will in turn carry seeds into the degraded parts of the
forest and into forest clearings. Unfortunately, no studies
have previously been carried out to shed light on the importance of frugivorous animals, especially lemurs, in the reforestation of the Ambatoledama corridor.Unlike the majority of
tropical forests, the diversity of the frugivorous bird community in Madagascar is impoverished, and therefore primates
are the principal dispersers of its tropical trees (Goodman,
1997; Dew and Wright, 1998; Ganzhorn et al., 1999; Bleher
and Böhning-Gaese, 2001). Ten lemur species are indentified
as living in the Masoala Forest (Mittermeier et al., 2006); one
of which (Varecia rubra) is endemic to this region and has Endangered status (IUCN, 2008), and can be found in both the
corridor habitat and adjacent forest fragments (Razakamaharavo et al., 2010). Previous studies demonstrated that
Varecia variegata is an effective disperser in the southeastern
rainforests (Dew and Wright,1998).However,we know very
little about the potential role of V. rubra for regeneration and
restoration of the corridor habitat in Ambatoledama.
In this study, we explored the germination success of seeds
defecated by Varecia rubra in order to understand their capacity for seed dispersal and potential impact on the restoration of the degraded rainforest corridor at Ambatoledama.
Our objective was to shed light on the role of this species in
forest regeneration. Understanding their influence on tree
germination is particularly important given the threatened
status of this species. This paper tested the hypothesis that
gut passage of seeds by Varecia rubra facilitates seed germination. Our prediction was that lemur-gut-passed seeds have a
higher germination rate than non-passed seeds because of
the physiological treatment affecting the seed coat inside the
gut.
Page 40
Materials and methods
Field site
This study was carried out at the Ambatoledama corridor
(S15°27’ E050°01’) on the north-eastern part of the Masoala
Peninsula. Ambatoledama connects Masoala National Park
with Makira National Forest to the West. Its forest has undergone significant deforestation but restoration projects
have augmented Ambatoledama such that it now forms a 1
km wide corridor of secondary forest (Hekkala et al., 2007;
Razakamaharavo et al.,2010).It consists of a dense evergreen
rainforest with an altitude ranging from 300 to 700 m. The
forest is mostly characterized by the presence of tree species of the Pandanacea, Ebenaceae, Clusiaceae, Euphorbiaceae, Sapotaceae and Rubiaceae families (Martinez, unpublished).
Study species
Varecia rubra belongs to the family Lemuridae (Gray, 1821)
and is one of two species recognized within the genus (Mittermeier et al., 2006). V. rubra is only found on the Masoala
peninsula and it is classified by the World Conservation Union (IUCN) as Endangered (IUCN, 2008). V. rubra is a largesized diurnal species with a body length ranging from 43 to
57 cm (Vasey, 2003) and has a typically frugivorous diet
(Rigamonti, 1993; Vasey, 1997). They currently inhabit both
the corridor habitat and the adjacent protected areas (Razakamaharavo et al., 2010) and are thus potentially important
for regeneration of the corridor habitat.
Field experiment
Focal animals were followed for 3-5 days per week from
dawn to dusk (from 0600 hours to 1800 hours) to collect
fresh fecal samples (Dew and Wright,1998;Kaplin and Moermond,1998;Stevenson,2000;Poulsen et al.,2001;Link and Di
Fiore, 2006). Each fecal sample was washed and filtered
through a 1-mm sieve (Stevenson, 2000). Seeds were extracted and then identified with the help of local research guides
and an expert local botanist familiar with the Masoala flora.
We planted gut-passed seeds and control seeds that were
extracted manually from fruits in an outdoor nursery adjacent to the corridor at Ambatoledama. The nursery consisted of two "flower beds" of 11.2 m2: one for defecated
Fig. 1: Location of the Ambatoledama corridor.
Lemur News Vol. 15, 2010
seeds and the other one for non-passed seeds. Following
methods used by the conservation agents of MNP in Ambatoledama, a sunshade of 80 cm height, composed of Longoza
leaves (Afromomum angustifolium) was placed above each
flower bed to imitate the closed canopy of the forest. Also,
the soil of the nursery was mixed with fertile soil from cultivated field. Seeds were placed in the soil mixture and
covered by 1 mm-thick river sand to keep a constant temperature.
An equal number of seeds were planted within each species
per treatment. However, the numbers varied between species depending on how many seeds were collected from
lemur feces. The germination of seeds was assessed each
month after planting.
Data analysis
We performed a paired t-test to test for differences between the germination rate of lemur-gut-passed and nonpassed seeds, an ANOVA analysis to test if the two factors
(seed species and treatment) had effects on the germination
rate of the seeds and to determine whether there was interaction between these factors. We analyzed the germination
of each species in order to assess the influence by lemur gut
passage, with Pearson test using contingency tables, which
was adjusted with Bonferroni correction for multiple comparisons (Sokal and Rohlf, 1995).
Results
In total, 268 fresh fecal samples from three individuals of
red-ruffed lemur were collected during 58 days of observation. The fecal samples contained fleshy fruit parts, stalks,
leaves, soil and fecal liquid. 95.52 % of these contained seeds,
to some of which fleshy fruit parts were still attached. 906
seeds of more than 1mm size were extracted. A majority of
them were intact with minor scarification. They represented
34 different plant species that belong to 15 Families.Based on
our collected sample, the most common seed species found
in lemur defecations were the nine species we chose to
study here (Tab. 1). In the nursery, we planted a total of 390
defecated seeds and compared them with 398 non-passed
seeds.
Lemur-gut-passed seeds had significantly higher germination
rates overall than non-passed seeds (t=3.284,df=8,p=0.011).
Passed seeds had a germination rate
of 64.61 %, whereas non-passed
seeds had a rate of 39.69 %.For each
species, seeds that had been defecated had a higher germination rate
than non-passed seeds, except for
Tsilaitra (Tab. 1). This pattern was
driven primarily by four species, including Antaivaratra,Matahobaratra,
Tsilaitra, and Vongobe species.
In a two factor analysis of variance
for seed germination, there was a
significant interaction between the
species of seeds and their treatment
(passed or non-passed) (F= 4.2004,
p<0.0001). When the analysis was
repeated excluding the interaction,
seed germination differed significantly both between seed species
(F=23.268, p<0.0001) and between
their origins (F= 58.706, p<0.0001).
For some species, gut passage might
only be important for dispersal away
Lemur News Vol. 15, 2010
Page 41
Tab. 1: List of species studied with their germination rate. Sample sizes are represented in The results presented here sugbrackets. The star on p-values corresponds to their significance (Pearson test) after a gest that V. rubra may be vital to
Bonferroni correction for multiple tests.
corridor restoration, which is
important for maintaining the
# Malagasy
Scientific
Family
Germination rate
Pearson test
biotic exchange between the
name
name
gut-passed non-passed
ChiPforested blocks of the Masoala
seeds
seeds
square value
Peninsula. Ambatoledama is vul1 Antaivaratra
Potameia sp. Lauraceae
41.67 (n = 48) 17.86 (n = 56) 7.139 0.0075*
nerable and currently facing sig2 Hazondronono Sideroxylon
Sapotaceae
80.00 (n = 10) 60.00 (n = 10) 0.952
0.3291
nificant fragmentation (Doko3 Karaka
Pandanus
Pandanaceae 40.00 (n = 20) 15.00 (n = 20) 3.135
0.0766
lahy,2005;Razakamaharavo et al.,
4 Matahobaratra Garcinia sp.
Clusiaceae
58.06 (n = 31) 00.00 (n = 31) 25.364 <0.0001*
2010). Thus, the existence of
5 Rotro Beravina Eugenia sp.
Myrtaceae
60.61 (n = 33) 42.42 (n = 33) 2.184
0.1394
such dispersers in this site is
Tavolo
6
Cryptocarya sp. Lauraceae
51.25 (n = 80) 26.25 (n = 80) 1.043
0.307
likely to be very important for
madinidravina
quickly facilitating seed dissemi7 Tsilaitra
Norhonia sp. Oleaceae
91.67 (n = 12) 100.0 (n = 12) 10.533 0.0012*
nation. A potential loss of the
Uapaca
8 Vapakafotsy
Euphorbiaceae 75.00 (n = 56) 25.00 (n = 56) 1.17
0.2795
floral diversity will occur if this
silvestris
lemur species goes extinct or
Garcinia
84.00
78.00
9 Vongobe
Clusiaceae
28
<0.0001*
verrucosa
(n = 100)
(n = 100)
moves into other forest blocks.
Recent increases in both
from the parent tree; for others, it is also important for their
bushmeat hunting for lemurs and tree poaching in the area
(Hatchwell, 1999; Barrett and Ratsimbazafy, 2009; Golden,
germination success. The difference of germination rate
2009; Into, 2009; Schuurman and Lowry, 2009) may have dire
within each species showed that for four species, the germiconsequences for forest regeneration and future habitat resnation rate of defecated-seeds was higher than for nontoration efforts. Loss of the floral diversity and change in
passed seeds (Tab. 1).
community structure of the vegetation is expected to occur
in the absence of these lemurs which may be critical for disDiscussion
persal
of many larger-seeded species. Decline or loss of this
As we predicted, our results showed that lemur-gut-passed
species may also limit successful forest regeneration and
seeds had a higher germination rate than non-passed seeds.
habitat restoration of the corridor. Thus the conservation of
Based on our collected fecal samples, our study confirmed
V.rubra is likely to be key for an effective restoration program
that V. rubra has a mainly frugivorous diet. The nine species
at Ambatoledama.
(Tab. 1) studied here represented the most common species
in V. rubra’s diet during the humid hot season. Its frugivorous
Acknowledgments
diet and passing of intact seeds suggest that V. rubra is predisWe would like to thank the Ministère des Eaux et Forets,
posed to be a beneficial seed disperser. Frugivorous animals
University of Antananarivo,Wildlife Conservation Society in
are, in general, categorized into three classes (Kaplin and
Moermond, 1998; Bollen et al., 2004; Gosper et al., 2005): (1)
Madagascar, and all MNP Maroantsetra staff for their permit
seed dispersers which have the capacity to carry seeds from
to work in Masoala National Park and for their logistical help.
one place to another, (2) those who drop seeds under the
We also thank the local guides in Ambatoledama and Leon, a
parent tree without ingesting them, and (3) seed predators
MNP Conservation Agent. We are grateful to Dr Barbara
which digest seeds. Our results showed that V. rubra may be
Martinez, Dr Amy Dunham, and Dr Thomas Jones for their
an effective seed disperser of several tropical rainforest
advice, and to Jeffrey Kloppenburg and Jenny Schmitt for
plants in the Ambadoledama corridor through endozootheir assistance in the field.Funding was provided by the Unichory.The passage of seeds in V.rubra’s gut improved the gerversity of Minnesota Graduate Program in Conservation
mination of several species in this study (Chapman and
Biology. Razafindratsima received support from Rice UniverChapman, 1996; Poulsen et al., 2001). It appears that some
sity and a fellowship from the Philanthropic Educational
plant taxa in particular, require a chemical scarification proOrganization during writing and analysis.
cess inside the lemur gut to acquire a high level of germination capacity,like the majority of vertebrate-dispersed plants
(McKey, 1975; Dew and Wright, 1998), as they may not be
able to germinate without the removal of their aril by a frugivore (Howe, 1986). Moreover, the plant species making up
the majority of the diet appeared to be primarily large-sized
seeds (10-30 mm;Razafindratsima and Martinez,unpublished
data), and are therefore difficult to swallow by frugivorous
birds.
As a seed vector, V. rubra may play an important role in maintaining forest diversity by affecting the spatial distribution
and dynamics of plants (Bleher and Böhning-Gaese, 2001;
Clark et al., 2001; Brodie et al., 2009). Endozoochory by this
species is an important strategy for the plant to increase its
fitness because seeds can minimize the time they spend in
the embryogenesis phase (Dew and Wright, 1998), which is
likely to reduce the rate of seed predation by rodents and
other granivores (Wehncke and Dalling, 2005). Also, it helps
plants to avoid disproportionate seed and seedling mortality
near the parent, and to be deposited in a microhabitat suitable for their establishment and growth (Howe and Smallwood, 1982).
References
Barrett, M.A.; Ratsimbazafy, J. 2009. Luxury bushmeat trade
threatens lemur conservation. Nature 461: 470.
Bleher,B.;Böhning-Gaese,K.2001.Consequences of frugivore diversity for seed dispersal, seedling establishment and
the spatial pattern of seedlings and trees. Oecologia 129:
385-394.
Bollen, A.; Elsacker, L.V.; Ganzhorn, J.U. 2004. Relations between fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach.Journal of Tropical
Ecology 20: 599-612.
Brodie, J.F.; Helmy, O.E.; Brockelman, W.Y.; Maron, J.L. 2009.
Functional differences within a guild of tropical mammalian frugivores. Ecology 90: 688-698.
Chapman, C.A.; Chapman, L.J. 1996. Frugivory and the fate of
dispersed and non-dispersed seeds of six African tree
species. Journal of Tropical Ecology 12(4): 491-504.
Clark,C.J.;Poulsen,J.R.;Parker.V.T.2001.The role of arboreal
seed dispersal groups on the seed rain of a lowland tropical forest. Biotropica 33: 606-620.
Dew, J.L.; Wright, P. 1998. Frugivory and seed dispersal by
four species of primates in Madagascar’s eastern rain forest. Biotropica 30: 425-437.
Page 42
Dokolahy, J. 2005. Etude de la régénération naturelle des
savoka du pont forestier d’Ambatolaidama en vue d’une
restauration forestiere.Unpubl.DEA thesis, ESSA University of Antananarivo, Madagascar.
Duncan,R.S.;Chapman,C.A.2002.Limitations of animal seed
dispersal for enhancing forest succession on degraded
lands. Pp. 437-450. In: D.J. Levey; W.R. Silva; M. Galetti
(eds.). Seed Dispersal and Frugivory: Ecology, Evolution
and Conservation. CABI Publishing, Oxford, UK.
Ganzhorn, J.U.; Fietz, J.; Rakotovao, E.; Schwab, D.; Zinner, D.
1999. Lemurs and the regeneration of dry deciduous forest in Madagascar.Conservation Biology 13(4):794-804.
Golden, C.D. 2009. Bushmeat hunting and use in the Makira
Forest, north-eastern Madagascar: a conservation and livelihoods issue. Oryx 43: 386-392.
Goodman,S.M.1997.Observations at a Ficus tree in Malagasy
humid forest. Biotropica 29: 480-488.
Gosper,C.R.;Stansbury,C.D.;Vivian-Smith,G.2005.Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Diversity and Distributions 11: 549.
Haddad, N.M.; Bowne, D.R.; Cunningham, A.; Danielson, B.J.;
Levey,D.J.;Sargent,S.;Spira,T.2003.Corridor use by diverse taxa. Ecology 84: 609-615.
Hatchwell, M. 1999. Plan de gestion de complexe des Aires
Protégées de Masoala. Unpubl. Wildlife Conservation
Society report.
Hekkala, E.R.; Rakotondratsima, M.; Vasey, N. 2007. Habitat
and distribution of the ruffed lemur, Varecia, north of the
Bay of Antongil in northeastern Madagascar. Primate
Conservation 22: 89-95.
Holloway, L. 1997. Catalysing natural regeneration of rainforest: Masoala corridors. Unpublished report presented
to Wildlife Conservation Society, Madagascar.
Howe, H.F. 1986. Seed dispersal by fruit-eating birds and
mammals. Pp.123-189. In: D.R. Murray (ed.). Seed Dispersal. Academic Press, Sydney.
Howe, H.F.; Smallwood, J. 1982. Ecology of seed dispersal.
Annual Review of Ecology and Systematics 13: 201-228.
Into,I.2009.Investigation into the illegal felling, transport and
export of precious wood in the SAVA region of Madagascar. Global Witness and the Environmental Investigation
Agency, Inc. Report.
IUCN. 2008. Red List of Threatened Species.
www.iucnredlist.org.
Kaplin, B.A.; Lambert, J.E. 2002. Effectiveness of Seed Dispersal by Cercopithecus Monkeys: Implications for Seed Input
into Degraded Areas. Pp. 351-364. In: D.J. Levey;W.R. Silva;
M. Galetti (eds.). Seed Dispersal and Frugivory: Ecology,
Evolution and Conservation. CABI Publishing, Oxford,
UK.
Kaplin, B.A.; Moermond, T.C. 1998. Variation in seed handling
by two species of forest monkeys in Rwanda. American
Journal of Primatology 45: 83-101.
Link, A.; Di Fiore, A. 2006. Seed dispersal by spider monkeys
and its importance in the maintenance of neotropical
rain-forest diversity. Journal of Tropical Ecology 22: 235246.
McKey,D.1975.The ecology of coevolved seed dispersal systems.Pp.159-191.In:L.E.Gilbert,P.H.Raven (eds.).Coevolution of Animals and Plants. University of Texas Press,
Austin, TX, USA.
Mech, S.G.; Hallett, J.G. 2001. Evaluating the effectiveness of
corridors: a genetic approach. Conservation Biology 15:
467-474.
Mittermeier, R.A.; Konstant, W.R.; Hawkins, F.; Louis, E.E.;
Langrand, O.; Ratsimbazafy, J.; Rasoloarison, R.; Ganzhorn,
J.U.; Rajaobelina, S.; Tattersall, I. 2006. Conservation International Tropical Field Guide Series: Lemurs of Madagascar. Conservation International, Washington, DC, USA.
Neilan, W.; Catterall, C.P.; Kanowski, J.; McKenna, S. 2006. Do
frugivorous birds assist rainforest succession in weed
dominated old field regrowth of subtropical Australia?
Biological Conservation 129: 393-407.
Poulsen, J.R.; Clark, C.J.; Smith, T.B. 2001. Seed dispersal by a
diurnal primate community in the Dja Reserve, Cameroon. Journal of Tropical Ecology 17: 787-808.
Razakamaharavo, V.R.; McGuire, S.M.; Vasey, N.; Louis, E.E.;
Brenneman, R.A. 2010. Genetic architecture of two red
Lemur News Vol. 15, 2010
ruffed lemur (Varecia rubra) populations of Masoala National Park. Primates 51: 53-61.
Rigamonti, M.M. 1993. Home range and diet in red ruffed
lemurs (Varecia variegata rubra) on the Masoala Peninsula,
Madagascar. Pp. 25-40. In: P.M. Kappeler; J.U. Ganzhorn
(eds.). Lemur social systems and their ecological basis.
Plenum Press, New York, USA.
Schupp, E.W. 1993. Quantity, quality and the effectiveness of
seed dispersal by animals. Plant Ecology 107: 15-29.
Schuurman, D.; Lowry, I.I. 2009. The Madagascar rosewood
massacre. Madagascar Conservation & Development 4
(2): 98-102.
Sokal,R.R;Rohlf,F.J.1995.Biometry:the principles and practice of statistics in biological research. WH Freeman, New
York, USA.
Stevenson, P.R. 2000. Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia:
dispersal distance, germination rates, and dispersal quantity. American Journal of Primatology 50(4): 275-289.
Vasey, N. 1997. Community ecology and behavior of Varecia
variegata rubra and Lemur fulvus albifrons on the Masoala
Peninsula, Madagascar. Unpubl. Ph.D. thesis, Washington
University, St. Louis, USA.
Vasey, N. 2003. Varecia, ruffed lemurs. Pp. 1332-1336. In: S.M.
Goodman; J.P. Benstead (eds.). The Natural History of
Madagascar. Chicago University Press, Chicago, USA.
Wehncke, E.V.; Dalling, J.W. 2005. Post-dispersal seed removal and germination of selected tree species dispersed by
Cebus capucinus on Barro Colorado Island, Panama. Biotropica 37: 73-80.
Feeding ecology of the crowned sifaka
(Propithecus coronatus) in a coastal dry
forest in northwest Madagascar (SFUM,
Antrema)
Claire Pichon1*, Rivo Ramanamisata2, Laurent Tarnaud1, Françoise Bayart1, Annette Hladik1, Claude
Marcel Hladik1, Bruno Simmen1
1UMR 7206, Eco-anthropologie et Ethnobiologie, Centre
National de la Recherche Scientifique, and Museum National
d’Histoire Naturelle, 4 avenue du Petit Château, 91800 Brunoy, France
2Département de Biologie Animale,Faculté des Sciences, B.P.
906, Université d’Antananarivo, Antananarivo (101), Madagascar
*Corresponding author: cpichon@mnhn.fr
Key words: diet, primate, activity budget, forest composition
The crowned sifaka (Propithecus coronatus; Milne-Edwards,
1871) inhabits dry forests, riparian forests and mangroves of
northwest Madagascar. Originally believed to occur in a restricted area between the Mahavavy River in the southwest
(where it overlaps with P.deckenii) and the Betsiboka River in
the northeast (which separates it from P. coquereli), sightings
west of the Mahavavy River and along the Bongolava Massif
suggest that the distribution of this medium-sized species is
wider (Tattersall, 1986; Thalmann et al., 2002). The distribution and the taxonomic status of crowned sifakas have long
been debated, but the combination of morphological and
biogeographic evidence supports considering it as a valid
species (Thalmann et al., 2002; Mittermeier et al., 2006;
Groves and Helgen, 2007; Mittermeier et al., 2008). Considered as Endangered (A2 c,d) by the IUCN (2010), populations of crowned sifakas were estimated not to exceed 1,000
individuals in the wild. However, recently discovered populations in restricted fragmented forests extend the species’
Lemur News Vol. 15, 2010
distribution range farther towards the Southwest. A "Biocultural Project" was therefore initiated at Antrema (a site
located in the Mahajanga region) in 2000 to promote sustainable management (Gauthier et al., 2001). The project aims at
preserving a coastal environment in which crowned sifakas
occur in high densities while allowing villagers, mainly fishermen, to use natural products of the environment with parsimony and to benefit from technical and economical help.The
project also aims at promoting local socio-cultural rules and
a way of life that tends to respect the forest environment, including useful plants and several sympatric lemur species
(Propithecus coronatus, Eulemur fulvus, Eulemur mongoz, Lepilemur sp., Microcebus murinus). The site contains three of the
Northwest’s typical ecosystems (dry semi-deciduous forest,
mangrove swamp, savanna), which suffer moderate anthropogenic pressure (Gauthier et al., 2001). Owing to local
beliefs, especially the sacred (“masina”) nature of sifakas, the
Sakalava community plays a central role in this conservation
process (Harpet et al.,2000,2008).In this context,a few studies started investigating the behavior in relation to habitat
and food supply of the lemur species of Antrema (Gauthier et
al., 1999; Razafimahefa, 2001; Ramanikirahina, 2004). However,a detailed analysis of the feeding ecology and population
densities of P. coronatus is still lacking. We present here preliminary data on the plant species composition of the whitesand coastal forest inhabited by a dense population of sifakas
(among other prosimian species) and on the feeding ecology
of sifaka groups censused since 2008.
Methods
Study site
The Antrema station is a coastal area of 12,300 ha located on
the left riverside of the Betsiboka estuary, northwestern
Madagascar (15°42’-15°50’S, 46°-46°15’E; Gauthier et al.,
2001). The region undergoes a distinct dry season of 7
months from April to October. The mean annual rainfall (n =
9 years) in the Mahajanga region is 1,410 mm (with a peak in
January-February), with irregular rainfall during the dry season. With an annual mean of 27° C, temperature is highest in
October and lowest between June and August (Airport of
Mahajanga, 2000-2009).
Although the Antrema area has been traditionally protected
by the local Sakalava beliefs, forest areas where studies are
conducted are fragmented. After two first surveys in November 2007 and April-May 2008, we decided to establish
the study site at Badrala (15°45.665’S, 46°12.300’E). With
about 24 ha just behind the littoral dune,this non-sacred forest site offers suitable conditions to study the socioecology
of sifakas and the dynamics of a dry forest in Madagascar.The
forest there is partly split by a sandy open dune that sifaka
groups can cross easily. Tree logging occurs at low intensity
(with few selected species for defined use, e.g. for boats or
coffins) and small trees are sporadically cut for fences and
house building. We studied floristic composition by inventorying trees along four North/South-oriented line transects,
10 m-wide each, that were roughly perpendicular to the sea
front.Within this 0.73 ha,we tagged each tree > 10 cm diameter at breast height (DBH) with plastic labels, recorded
their DBH, the number of stems and their vernacular name.
Likewise, we counted woody lianas and herbaceous vines
> 1 m high within eight 10 x 10 m (800 m2) plots regularly
spaced along the transects. Plant species were sampled and
dried for later botanical identification.
Sifaka population density
In order to locate and identify groups of P. coronatus in
Badrala, we initially mapped groups encountered during
Page 43
repeated transect walks. We drew individuals’ facial masks
for each of the followed groups, noted their sex from visual
inspection of the genitalia and other external characteristics
(cysts, scars, damaged ears, fur colour), and took pictures.
Knowledge gained progressively of groups and individuals
allowed us to provide a preliminary estimate of population
density for the Badrala site.
Behavioral data collection
We collected behavioral data during 4 periods (06 to 21 July
2008; 11 November to 12 December 2008; 05 April to 06
June 2009; 17 October to 22 November 2009). Most groups
were already accustomed to the sporadic presence of local
people. Once we could observe animals at close distances,
we followed each group successively over 2 to 5-day periods,
from 06:30 to 18:30 hours.
We used the instantaneous scan-sampling method (Altmann,
1974) to study group activity budget. Every 5 minutes, we recorded the individuals’ activity using one of the following categories:resting (immobile,with eyes open or closed),moving
(more than 0.5 m), foraging (searching for a food item), feeding (processing or chewing a food item), social activity (displaying agonistic and affiliation behaviors with other individuals) and other miscellaneous behaviors. We noted the plant
part and species eaten by individuals.
Besides recording activity budgets, we determined diet from
mouthful counts converted into weight of ingested matter
(Hladik, 1977) for 2 periods: April-June 2009 and OctoberNovember 2009. We estimated food intake in focal individuals that were followed continuously for 30 minutes each.
Observations were alternated across males and females (excluding juveniles) within groups.
Results
Forest composition
Plant families occurring at Badrala are presented separately
for trees and lianas/vines in Fig.1.To date,91 tree and liana or
vine species have been identified at least at the family level,
and taxonomic identification of 15 more putative species is
still in progress.The 5 richest families in terms of the number
of species are Fabaceae, Sapindaceae, Ebenaceae, Euphorbiaceae and Apocynaceae.The most dominant tree species are
Strychnos decussata, Vitex beraviensis, Mimusops occidentalis,
Baudouinia fluggeiformis and Macphersonia gracilis that represent almost one third of total basal area and tagged trees.
Combretum coccineum, Hypoestes sp., Landolphia perrieri and
Reissantia sp. accounted for more than one third of the lianas
and vines.
Density of trees inventoried on the 4 transects (n=486) corresponds to 666 inds. ha1 with a total basal area of 14.5 m²
ha-1.We found a high density of woody lianas and herbaceous
vines in the 800m² plots (n=373).
Sifaka population density and group composition
Groups at Badrala have 1-3 breeding adult males, 1-4 breeding adult females, and 1-4 immature offspring. We encountered between 15 and 20 groups at this site. Based on current recognition of individuals within these groups, a minimum estimate of 300 inds. km2 was calculated. Mean size of
focal groups was 4.3 ± 1.8 individuals (n=16).
Diet and activity pattern
Sifakas consumed at least 60 plant species from 32 families.
Tab. 1 lists major food species eaten. During the dry season,
14 plant species represented 75 % of the diet whereas only 7
species were the main food resource in the wet season.
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Lemur News Vol. 15, 2010
Tab. 1: Food species accounting for 50 and 75 % of the diet of Propithecus coronatus during the dry season and the wet season.
Eaten plant species are listed in decreasing order and their abundance in transects and plots (see text) is indicated.
Family
Species
Lamiaceae
Fabaceae
Sapotaceae
Anacardiaceae
Sapindaceae
Oleaceae
Moraceae
Sphaerosepalaceae
Melastomataceae
Burseraceae
Fabaceae
Olacaceae
Moraceae
Unidentified
Vitex beraviensis
Baudouinia fluggeiformis
Mimusops occidentalis
Operculicarya gummifera
Majidea zanguebarica
Noronhia boinensis
Trilepisium occidentalis
Rhopalocarpus lucidus
Warneckea sp.
Commiphora sp.
Bussea perrieri
Olax dissitiflora
Ficus pyrifolia
-
Anacardiaceae
Anacardiaceae
Fabaceae
Sapotaceae
Apocynaceae
Combretaceae
Anacardiaceae
Abrahamia deflexa
Abrahamia sp.
Chadsia flammea
Capurodendron gracilifolium
Landolphia perrieri
Terminalia sp.
Operculicarya gummifera
Vernacular name
Dry season
Mojiro
Manjakabentany
Natofotsy
Atokonjo
Tsipopoka
Tsilaitra beravina
Kililo
Hazondringitra
Voatrotrokoala
Arofy
Morango
Ambiotsy
Nonika
RR80
Wet season
Motsovavy
Manavodrevo
Fanamohazo
Natoboay
Vahipira
Taly
Atokonjo
Items
Abundance (%)
yl
yl ml
yl stems
ml buds
yl ml fl
yl
ml
yl fr
yl
fr buds
ml
ml
fr
ml
10,7
4.7
3.9
3.5
2.3
1.9
1.2
1.0
0.6
0.4
0.2
0.2
yl fl
buds yl fl
buds yl fl
buds yl fr
yl
buds yl
yl
3,1
1.2
0.8
0.2
6.8
3.1
3.5
50 %
75 %
50 %
75 %
yl: young leaves; ml: mature leaves; fl: flowers; fr: fuits
Fig.1:Abundance of plant families plotted in
decreasing number of individuals among a)
trees with DBH>10cm (based on transects;
0.73 ha) and b) woody lianas and herbaceous vines >1 m height (based on plots;
0.08 ha).Striped bars refer to the plant families with the highest number of species.
Page 45
Lemur News Vol. 15, 2010
folivorous during our study,its diet changed
with seasons. Young leaves were the pre9% 1%
ferred food type in the early wet season,
11%
57%
2%
Young leaves
30%
while mature leaves were the dominant one
6%
in the beginning of the dry season. In addiMature leaves tion, P. coronatus ate a higher proportion of
liana and vine parts during the wet season.
Flowers
Crowned sifakas also followed the typical
activity pattern of other sifaka species
25%
Fruits
(Norscia et al.,2006;Patel,2006;Charrier et
58%
al., 2007), spending most of their time restOther
1%
ing and devoting a substantial amount of
time to feeding activities and locomotion.
Fig.2:Food categories in the diet of Propithecus coronatus during the dry season Activity budget nevertheless changed with
(a) and the wet season (b).
seasons. It is generally suggested that the
cool dry season represents a period of food
scarcity for animals,which they compensate
(b) Wet season
(a) Dry season
for by reducing their energy expenditure,
travelling less and resting more. In a recent
5,9%
5,3%
0,8%
3,9%
46,6%
50,0%
joint research project, the content of litter
Resting
traps regularly distributed along the trans29,4%
35,8%
Locomotion ects was collected and weighted every two
weeks throughout one year. It was found
Foraging
that plant species could be grouped according to their temporal pattern of leaf loss
Feeding
(Ranaivoson et al., 2010; see also RazakaniSocial
rina, 2010). Several trees, lianas and vines
lost their leaves more or less regularly
6,8%
Other
7,1%
3,6% 4,8%
throughout the dry season while others
Fig. 3: Activity budget of Propithecus coronatus during the dry season (a) and the were characterized by delayed leaf loss or
on the contrary by precocious leaf fall. One
wet season (b).
consequence is that leaves are available
Sifakas were highly folivorous during both seasons, supplethroughout the year, although as different sets of species
menting their diet with flowers, fruits, vegetative buds, and
varying in quantity,diversity,and presumably,nutritional qualsometimes young stems (Fig. 2). They consumed more maity.This at least could explain why sifakas are able to increase
ture leaves and fruits in the dry season and more flowers in
the diversity of consumed plants (and adopt a more opporthe wet season.
tunistic strategy) during the dry season, a period normally
described by the scarcity of food resources.
The activity budget of the sifakas is presented in Fig. 3. AlFuture work on seasonal variations in the diet’s nutritional
though ‘resting’ predominated throughout the study,
and chemical content will allow us to examine the role of
individuals rested more in the dry season than in the wet seaqualitative aspects in food choices (Moss,1991;Dearing et al.,
son. Inversely,they travelled less and engaged in feeding activ2000) and further examine potential differences between
ities more often during the wet season.
genders with regard to the importance of energy conservation for female sifakas (Wright, 1999; Charrier et al., 2007).
Discussion
The sifaka density was found to be high in the dry forest of
Conclusion
Antrema, with a minimum estimate far above the 173 inds.
Better knowledge of the ecology and the villagers’ social perkm2 found in the riparian forest of Anjamena (Muller et al.,
ception of this flagship species may contribute to conserva2000) or for other sifaka species in dry or wet forests
tion of other diurnal lemurs, by incorporating the villagers’
(O’Connor, 1988; Ganzhorn, 1992). This high density might
symbolic perception of their natural environment. Investibe related to some peculiar characteristics of the forest in
gating the interactions between this species and plants of the
terms of food quantity and/or food quality available to this
coastal dry forest ecosystem will undoubtedly result in
prosimian species. However, tree basal area was not particubetter conservation decisions for Antrema. From an evolularly high compared with other dry forests in Madagascar
tionary ecology standpoint, the studies we have planned for
and Mayotte (Hladik, 1980; Simmen et al., 2005). It is not yet
the next years at Antrema will also contribute to better
clear also whether high density is related to a putative low
predation pressure.To our knowledge,no sightings or traces
identify the selective pressures that have been driving the
of viverrid carnivores have been reported; large raptors and
evolution of prosimian typical life-history traits such as
boas would be the only predators that could affect the
reproductive synchronization or dominance-based feeding
demography of the Antrema sifaka population (Garbutt,
priority of females over males in gregarious species (Wright,
2007; Sinclair and Legrand, 2008).
1999; Dewar and Richard, 2007).
As regards their feeding behavior, crowned sifakas fed primarily on leaves from a few tree, liana and vine species, and
Acknowledgements
supplemented their diet with a wide range of secondary
We thank the Malagasy Institutions that authorized to colitems as commonly occurs in other Propithecus species
lect and export the plant samples,the Ministère de l’Environ(Meyers and Wright, 1993; Simmen et al., 2003; Lehman and
nement, des Eaux et forêts et du Tourisme. We also thank
Mayor, 2004; Irwin, 2008). Although this species remained
Antrema’s project staff for assistance with the field work as
(a) Dry season
(b) Wet season
Page 46
well as Master degree students S.Razakanirina,T.Ranaivoson,
V. Randriantoposon and L. Razafindramahatra for helping
with data collection. Special thanks to the specialists of the
Dept of Phanerogamy,J.N.Labat,P.Phillipson and Pete Lowry,
for helping with plant identification. Finally, we thank C.A.
Gauthier, E. Roger, D. Rakotondravony and H. Razafindraibe
for logistic support and collaborative work, and E.G. Leigh
for helpful comments on an earlier draft. This study was
funded by the UMR 7206 - CNRS, and was conducted under
the "Convention cadre de cooperation" between the Université d’Antananarivo and the Museum National d’Histoire
Naturelle, Paris.
References
Altmann, J. 1974. Observational study of behavior. Sampling
methods. Behavior 49: 227-267.
Charrier,A.;Hladik,A.;Simmen,B.2007.Feeding strategy and
social dominance in female sifakas (Propithecus v.verreauxi)
living in a Didiereaceae forest in southern Madagascar.
Rev. Ecol. (Terre Vie). 62: 257-263.
Dearing, M.D.;Mangione,A.M.;Karasov,W.H. 2000.Diet breadth of mammalian herbivores:nutrient versus detoxification constraints. Oecol. 123: 397-405.
Dewar,R.E.;Richard,A.F.2007.Evolution in the hypervariable
environment of Madagascar.Proc.Nat.Acad.Sci.USA 104:
13723-13727.
Ganzhorn, J.U. 1992. Leaf chemistry and the biomass of folivorous primates in tropical forests. Test of a hypothesis.
Oecol. 91: 540-547.
Garbutt, N. 2007. Mammals of Madagascar: A Complete Guide. Yale University Press, New Haven.
Gauthier,C.A.;Deniaud,J.L.;Leclerc-Cassan,M.;Rakotomalala, M.;Razafindramanana,S.;Renson, G. 1999. Proc. 2nd Int.
Symp. Biogeography, diversity and endemism in Madagascar, Paris.
Gauthier,C.A.;Huguet,S.;Rakotondravony,D.;Roger,E.2001.
Diagnostic physico éco-biologique de la station forestière
à usages multiples d’Antrema (péninsule de Katsepy).Parc
Zoologique de Paris, Muséum national d’Histoire naturelle, Paris.
Groves, C.P.; Helgen, K.M. 2007. Craniodental characters in
the taxonomy of Propithecus.Int.J.Primatol.28:1363-1383.
Harpet,C.;Jeannoda,V.;Hladik,C.M.2000.Sacred lemur sites
in the Sakalava region of North-West Madagascar: updated data and implications for sustained development
and conservation programs. Rev. Ecol. (Terre Vie) 55:
291-295.
Harpet,C.;Navarro,L.;Ramanankirahana,R.2008.Rôle et implications des croyances et des savoir-faire locaux dans les
programmes de conservation: exemple d’un site à lémuriens sacrés au cœur de la Station Forestière à Usages
Multiples d’Antrema (Pays Sakalava, Madagascar). Rev.
Ecol. (Terre Vie) 63: 289-292.
Hladik,A.1980.The dry forest of the West coast of Madagascar: climate, phenology, and food available for Prosimians.
Pp.3-40.In:P.Charles-Dominique; H.M.Cooper;A.Hladik;
C.M.Hladik;E.PagPs;G.F.Pariente;A.Petter-Rousseaux;J.J.
Petter; A. Schilling (eds.). Nocturnal Malagasy Primates.
Ecology, Physiology, and Behavior. Academic Press, New
York.
Hladik, C.M. 1977. Field methods for processing food samples. Pp. 595-601. In: T.H. Clutton-Brock (ed.). Primate
Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys, and Apes. Academic Press, London.
Irwin, M.T. 2008. Feeding ecology of Propithecus diadema in
forest fragments and continuous forest. Int. J. Primatol. 29:
95-115.
Lehman, S.M.; Mayor, M. 2004. Dietary patterns in Perrier’s
sifakas (Propithecus diadema perrieri): A preliminary study.
Am. J. Primatol. 62: 115-122.
Meyers,D.M.;Wright,P.C.1993.Resource tracking:food availability and Propithecus seasonal reproduction. Pp. 179-92.
In: P.M. Kappeler; J.U. Ganzhorn (eds.). Lemur social systems and their ecological basis.Plenum Press,New York.
Mittermeier, R.A; Ganzhorn, J.U.; Konstant, W.R.; Glander, K.;
Tattersall, I.; Groves, C.P.; Rylands, A.B.; Hapke, A.; Ratsim-
Lemur News Vol. 15, 2010
bazafy, J.; Mayor, M.I; Louis Jr., E.E.; Rumpler, Y.; Schwitzer,
C.; Rasoloarison, R.M. 2008. Lemur diversity in Madagascar. Int. J. Primatol. 29: 1607-1656.
Mittermeier, R.A; Ganzhorn, J.U.; Konstant, W.R.; Glander, K.;
Tattersall, I.; Groves, C.P.; Rylands, A.B.; Hapke, A.; Ratsimbazafy, J.; Mayor, M.I; Louis Jr., E.E.; Rumpler, Y.; Schwitzer,
C.; Rasoloarison, R.M. 2006. Lemurs of Madagascar. Conservation International, Washington.
Moss,R.1991.Diet selection.An ecological perspective.Proc.
Nutr. Soc. 50: 71-75.
Muller,P.;Velo,A.;Raheliarisoa,E.O.;Zaramody,A.;Curtis,D.J.
2000. Surveys of sympatric lemurs at Anjamena, NorthWest Madagascar. Afr. J. Ecol. 38: 248-257.
Norscia, I.; Carrai, V.; Borgognini-Tarli, S.M. 2006. Influence of
dry season and food quality and quantity on behavior and
feeding strategy of Propithecus verreauxi in Kirindy, Madagascar. Int. J. Primatol. 27: 1001-1022.
O’Connor, S. 1988. Une revue des différences écologiques
entre deux forêts galeries, une protégée et une dégradée,
au centre sud de Madagascar.Pp.216-227.In:L.Rakotovao;
V. Barre; J. Sayer (eds.). L’équilibre des écosystèmes forestiers à Madagascar. Actes d’un séminaire international.
UICN, Gland.
Patel, E.R. 2006. Activity budget, ranging, and group size in
silky sifakas (Propithecus candidus). Lemur News 11: 4.
Ramanikirahina, R. 2004. Rythme d’activité et régime alimentaire de Propithecus verreauxi coronatus et d’Eulemur mongoz dans la Station Forestière d’Antrema. Mémoire de
DEA, Univ. Antananarivo, Faculté des Sciences, Dept Biologie Animale.
Ranaivoson, T.N.; Razakanirina, H.; Roger, E.; Rajeriarison, C.;
Hladik, A. 2010. Structure de l’habitat de Propithecus coronatus et disponibilités alimentaires dans la station forestière a usage multiple d’Antrema: Application de la méthode des tris de litière et interprétations des adaptations
des espèces arborescentes et lianescentes. AETFAT Congress April 25-30. Antananarivo, Madagascar.
Razafimahefa, M.A. 2001. Caractérisation des habitats de Propithecus verreauxi coronatus dans la station forestière à usages multiples d’Antrema (Katsepy): cartographie, typologie, étude ethnobotanique. Mémoire de DEA, Univ. Antananarivo, Faculté des Sciences, Dept Biologie et Ecologie
Végétale.
Razakanirina, H. 2010. Suivi phénologique global et statut de
conservation de 4 espèces végétales (Strychnos decussata,
Diospyros ferrea,Gardenia decaryi et Capurodendron gracilifolium) consommées par Propithecus verreauxi coronatus dans
la forêt de Badrala (Antrema). Mémoire de DEA, Univ.
Antananarivo, Faculté des Sciences, Dept Biologie et Ecologie Végétale.
Simmen, B.; Hladik, A.; Ramasiarisoa, P. 2003. Food intake and
dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, southern
Madagascar. Int. J. Primatol. 24: 948-967.
Simmen, B.; Tarnaud, L.; Bayart, F.; Hladik, A.; Thiberge, A.L.;
Jaspart, S.; Jeanson, M.; Marez, A. 2005. Richesse en métabolites secondaires des forêts de Mayotte et de Madagascar et incidence sur la consommation de feuillages chez
deux espèces de lémurs (Eulemur spp.). Rev. Ecol. (Terre
Vie) 60: 297-324.
Sinclair, I.; Langrand, O. 2008. Birds of the Indian Ocean
islands. Struik, Cape Town.
Tattersall, I. 1986. Notes on the distribution and taxonomic
status of some subspecies of Propithecus in Madagascar.
Folia Primatol. 46: 51-63.
Thalmann, U.; Kümmerli, R.; Zaramody, A. 2002. Why Propithecus verreauxi deckeni and P. v. coronatus are valid taxa.
Quantitative and qualitative arguments. Lemur News 7:
11-16.
Wright, P.C. 1999. Lemur traits and Madagascar ecology:
Coping with an island environment.Yrbk Phys.Anthropol.
42: 31-72.
Lemur News Vol. 15, 2010
Effet de la dégradation de l’habitat sur la
consommation alimentaire d’Eulemur
rubriventer dans deux sites: Talatakely et
Vatoharanana, du Parc National de Ranomafana
Laingoniaina H. Rakotonirina1,2*, Germain J. Spiral1,2,
Jonah H. Ratsimbazafy1,2, Soanorolalao Ravelonjanahary1,Raharizelina Ralaiarison1,2,Stacey Tecot3,Alex
Hall4, Tricia Calhoon4, Gisèle R. Randria1,2
1Département de Paléontologie et d’Anthropologie Biologique, Faculté des Sciences, B.P. 906, Université d’Antananarivo, Madagascar
2Groupe d’Etudes et de Recherche sur les Primates de Madagascar (GERP)
3Department of Anthropology, University of Stony Brook,
USA
4Voluntary field assistant
*Contact de l’auteur principal: laingoniaina2000@yahoo.fr
Mots clés:Eulemur rubriventer,dégradation,habitat,consommation alimentaire, Ranomafana, Madagascar
Introduction
La grande île est potentiellement riche en matière de biodiversité et est par conséquent renommée pour sa remarquable richesse écologique, biologique et génétique (Ganzhorn et al., 2001). Cette richesse qui est gravement menacée
par la diminution et la destruction immuables des habitats
naturels de nombreuses espèces fait de Madagascar un des
huit "hotspots" les plus considérés de notre planète (Ganzhorn et al., 2001).
A l’échelle mondiale, la menace la plus grave pour la population des primates est la destruction et la dégradation de leur
habitat, notamment les forêts tropicales qui hébergent aujourd’hui environ 90 % des primates non humains du monde
(Mittermeier et al., 2006, 2010). Les lémuriens malgaches ne
font pas exception à cette constatation. La dégradation des
forêts affecte la biologie générale des lémuriens car non
seulement elles leur fournissent des abris et de la nourriture,
mais aussi elles servent de supports à la locomotion et aux
différentes activités de ces animaux (Razafimahazo, 2001).
Selon Randriatahina en 2001, la fragmentation de l’habitat
affecte en premier lieu la distribution et la dispersion de la
nourriture.Certains facteurs influencent le rythme d’activité
et le budget-temps des primates:il s’agit surtout des facteurs
écologiques majeurs tels que la structure de l’habitat, le type
d’alimentation (Zaonarivelo, 1999). Par ailleurs, Dunbar
(1988) affirme que les primates pourraient augmenter leur
déplacement journalier pour trouver de la nourriture ou
inversement en vue d’économiser leur énergie.
Notre présent travail est axé sur la corrélation entre l’habitat et l’alimentation des lémuriens. Les lémuriformes montrent un degré de variabilité en ce qui concerne la spécialisation aux régimes alimentaires. La plupart d’entre-eux (les
Lémuridés, les Mégaladapidés, les Indridés) se spécialisent au
régime végétarien. Cependant, la proportion de feuilles, de
fleurs, et de fruits consommés varie suivant les espèces et
sous-espèces,d’une région à une autre,et de saison en saison
(Richard, 1978). Selon Zaonarivelo (1999), des facteurs écologiques influencent les comportements des lémuriens et la
perturbation de leur habitat affecte leur organisation sociale
et l’exploitation des ressources alimentaires.
En tenant compte de toutes ces observations, nous avons
effectué une étude concernant l’effet de la dégradation de
Page 47
l’habitat sur la consommation alimentaire d’Eulemur rubriventer dans deux sites: Talatakely et Vatoharanana du Parc National de Ranomafana, dans la province de Fianarantsoa.
Il y a lieu de souligner qu’Eulemur rubriventer, une espèce
hautement frugivore (Overdorff, 1993), dispose d’une haute
importance écologique car elle participe activement à la dispersion des graines dans la région du Sud-Est de Madagascar,
en particulier dans le Parc National de Ranomafana. A cet
égard, bien que l’animal soit encore classé dans la catégorie
vulnérable selon la liste rouge de l’UICN (Mittermeier et al.,
1994,2006,2010),il a besoin d’ une action de conservation.
C’est la raison pour laquelle le parc national de Ranomafana a
été choisi comme notre station de recherche car par rapport aux autres régions de l’île, les lémurs à ventre roux y
sont les plus répandus (Mittermeier et al.,2006);et leur habitat présente un degré variable de dégradation.
Compte tenu de cette variation du degré de dégradation et
de perturbation du milieu de vie d’Eulemur rubriventer dans le
Parc National de Ranomafana, nous pouvons avancer une
hypothèse selon laquelle la consommation alimentaire n’est
pas statistiquement différente entre celle de Vatoharanana
et celle de Talatakely.
Ce projet a été réalisé dans le cadre de la collaboration interdépartementale entre l’Université d’Antananarivo, l’ICTE/
MICET, le MNP et l’Université de Texas. Ainsi, le présent travail qui vise en la conservation des lémurs à ventre roux a
comme objectifs d’inventorier les différentes espèces de
plantes consommées par Eulemur rubriventer, de comparer le
régime alimentaire adopté dans chaque site d’étude, de
déterminer les caractéristiques des plantes consommées
dans les deux sites d’études à dégradations différentes.
Site d’études
Le parc National de Ranomafana se trouve dans le Sud Est de
Madagascar.Sa superficie est de 41.600 ha.Ce parc se localise
au Nord-Est de Fianarantsoa, à 70 km à l’Ouest de l’Océan
Indien et à 400 km d’Antananarivo. Il est situé entre 47°18’ à
47°37’ Est de longitude et 21°2’ à 21°25’ Sud de latitude. La
température moyenne annuelle est de l’ordre de 21°C selon
Turk en 1995. Quant à la pluviosité, Overdorff a affirmé en
1996 que la pluie y est saisonnière avec une précipitation
moyenne de 2000 mm. Deux sites ont été choisis pour
effectuer notre travail de recherche. Il s’agit de:
Talatakely:milieu perturbé et plus dégradé.Il est situé à environ 10 mn de marche de la poste de garde et de contrôle
du Parc d’Ambodiamontana. Ce site de 1020 m d’altitude
(Brady et al., 1996), est caractérisé par une visite fréquente
de touristes. Notons également que, à cause des abattages
intensifs des arbres par les bûcherons (Kremen, 1992), la
forêt de Talatakely se trouve fortement dégradée.
Vatoharanana: un milieu moins perturbé et moins dégradé. Cet endroit est à 1090 m d’altitude et se trouve à 2
heures de marche de Talatakely. Ce champ de forêt était exploité par les bûcherons il y a 25 ans (Brady et al., 1996). Mais,
la dégradation était moins intense que celle de Talatakely
(Kremen, 1992). La visite des touristes dans cette station
d’études est également moins fréquente. Vatoharanana est
donc un site moins perturbé par rapport à Talatakely.
Les deux stations de recherche sont représentées dans la
figure 1.
Espèces étudiées
Afin de répondre à toutes nos questions, une espèce hautement frugivore, qui participe activement à la dispersion des
graines (Overdorff,1993),a fait l’objet de notre étude.Il s’agit
du Lémur à ventre roux ou Eulemur rubriventer. Généralement,cette espèce de taille moyenne vit en petit groupe de 2
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Lemur News Vol. 15, 2010
· Heure d’observation (Début et fin);
· Temps dépensé (Début et fin) à la consommation alimen-
taire et aux autres activités;
· Nom de chaque espèce consommée (plantes ou autres);
· Parties consommées des plantes: fruit, feuille, fleur;
· Etat des parties comsommées (fruit immature ou mûr,
jeune feuille, feuille mature, fleur ouverte ou fermée);
· Piste la plus proche.
Analyses statistiques
Test de similarité entre deux échantillons
Ce test sert à vérifier la similarité entre le régime alimentaire
adopté par les lémurs à ventre roux de Talatakely et celui de
Vatoharanana.Il se base sur la valeur du coefficient de Jaccard
(Brower et al., 1990). Ce coefficient est donné par la formule
suivante:
Fig. 1: Localisation des deux sites d’études dans le Parc
National de Ranomafana.
à 5 individus. Elle consomme également des feuilles, des
fleurs, de la terre, des mille-pattes. Selon Overdorff (1996),
l’animal mange beaucoup plus de fruits et moins de feuilles.
Eulemur rubriventer présente un dimorphisme sexuel au
niveau de la morphologie. En effet, le ventre des femelles est
clair; tandis que la poitrine et la partie inférieure du corps du
mâle sont visiblement colorées en marron roux. Le mâle
diffère également de la femelle par la présence de tâche
blanche sur le coin interne des yeux (Dague et Petter, 1988).
En ce qui concerne notre étude, nous avons suivi cinq
groupes de lémurs à ventre roux dont trois à Talatakely et
deux à Vatoharanana.
Suivi écologique
Le suivi écologique proprement dit était précédé de la familiarisation de tous les groupes d’études. A ce propos, durant
cinq mois d’études sur terrain,du mois de décembre 2003 au
mois d’avril 2004, la fréquence d’observation était de cinq
jours par semaine. L’observation s’étale de sept à douze
heures dans la matinée et de treize à quinze heures dans
l’après midi. Au total, l’équipe a suivi cinq groupes pour les
sites de Talatakely et de Vatoharanana, pendant 588 heures
45 minutes et 54 secondes.
La méthode d’enregistrement continu de données a été
adoptée.Elle nous donne des informations plus fiables et plus
pratiques par rapport à une méthode d’enregistrement instantané (Martin et Bateson, 1986). En outre, nous avons
collecté les données sur l’alimentation en suivant la méthode
de "focal animal sampling" (Altmann, 1974). Durant ces observations,nous avons enregistré les informations suivantes:
Site d’études: Talatakely ou Vatoharanana;
· Groupe d’étude;
· Focal animal;
· Date de l’observation;
CC: Coefficient de Jaccard
S1: Effectif d’espèces végétales, animales et autres dans le
régime de l’espèce de Talatakely (ET);
S2: Effectif d’espèces végétales, animales et autres dans le
régime d’Eulemur rubriventer de Vatoharanana (EV);
C: Effectif d’espèces végétales, animales et autres communes
(ET et EV)
Par souci de conformité, nous avons adopté les échelles
suivantes:
0-40 %: faible similarité entre les deux régimes;
40-60 %: similarité moyenne entre les deux régimes;
60-80 %: grande similarité entre les deux régimes;
80-100 %: forte similarité entre les deux régimes.
Test de Chi-deux:
Cette méthode sert à comparer la durée moyenne journalière (en minute) consacrée à la consommation alimentaire
des lémurs à ventre roux de Talatakely et de Vatoharanana.A
cet effet, les variables utilisées sont les durées moyennes
journalières dépensées à la consommation des fruits, des
feuilles, des fleurs et autres (sol, eau, champignon, insectes,…); et ce dans des intervalles de temps bien déterminés;
c’-est-à-dire, entre 7 et 8h, 8 et 9h, 9 et 10h, 10 et 11h, 11 et
12h, 13 et 14h et finalement entre 14 et 15h. Plus précisément, elle nous permet de vérifier si la différence entre la
consommation de ces aliments est statistiquement significative ou non dans les deux milieux.
Résultats
Temps dédié à l’activité alimentaire
Fig. 2 montre l’allure générale de la durée moyenne journalière en ce qui concerne la consommation alimentaire
générale des lémurs à ventre roux du milieu plus dégradé de
Talatakely et celle du site moins dégradé de Vatoharanana.
Selon cette figure,la prise de nourriture débute entre 7 et 8h.
Concernant le site de Talatakely,elle dessine un pic entre 9 et
10h. Cette activité diminue jusqu’à 12h, puis remonte pour
atteindre le maximum vers 14 à 15h. Quant à l’Eulemur rubriventer de Vatoharanana,le pic de l’alimentation se situe entre
8 et 9h. La courbe diminue jusqu’à 12h environ. Ensuite, une
légère remontée de l’activité est constatée jusqu’à 15h envi-
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Lemur News Vol. 15, 2010
Durée en minute
ron. L’hypothèse nulle est acceptée car l’analyse statistique
(À2= 9,95 ;avec ddl=6,et p>0,05) indique une différence non
significative concernant la prise de la nourriture entre
chaque intervalle de temps.
20
18
16
14
12
10
8
6
4
2
0
Nom
malagasy
Genre
Famille
Fr Fe Fl
Faritraty
Memecylon sp.
Melastomataceae
+
MaranitratoVernonia sp.
raka
Mendoncia
Vahivoraka
avani
Fatsikahitra Alberta humblotii
Albizia
Albizia chinensis
Rotra fotsy
Syzygium sp.
Tongoalahy
7-8h
8-9h
9-10h
10-11h 11-12h
13-14h 14-15h
Intervalle de temps
Talatakely
Vatoharanana
Fig. 2: Temps consacré à la consommation alimentaire pour
Eulemur rubriventer dans les deux sites d’étude: Talatakely et
Vatoharanana.
Similarité entre les régimes alimentaires d’Eulemur rubriventer du
site dégradé de Talatakely et de celui de la station moins dégradée
de Vatoharanana
L’inventaire des espèces consommées par les lémurs à
ventre roux dans les deux sites nous a permis de calculer le
coefficient de Jaccard afin de tester s’il existe ou non une
similarité de régimes dans les deux milieux. Nous avons
recensé 52 espèces de plantes qui sont utilisées comme
source de leur nourriture pour le site de Talatakely. En
revanche, 60 espèces sont inventoriées dans le site de
Vatoharanana.Il est à noter que 35 d’entre elles sont à la fois
consommées à Talatakely et à Vatoharanana. La liste des
espèces végétales utilisées par ces animaux comme source
de leur nourriture (avec la durée de consommation correspondante) est résumée dans le tableau récapitulatif suivant.
Tab. 1: Liste des espèces végétales consommées (61) par
Eulemur rubriventer, avec la durée de consommation correspondante, dans les deux sites d’étude.
Nom
malagasy
Genre
Ramy
Canarium
Burseraceae
madagascariensis
+
Oncostemum sp.
+
Kalafambakaka
Vakoana
Nonoka
Pandanus sp.
Ficus sp.
Strongylodon c
Vahimberana
raveniae
Voara
Ficus sp.
Voara rano
Ficus botryoides
Sandramy
Protorhus sp.
Famille
Myrsinaceae
Fr Fe Fl
+
+
23,57
242,55
Pandanaceae +
Moraceae
+
+
+
24,02
21,40
269,75
Fabaceae
+
2,03
189,72
70,08
23,13
39,45
36,15
Moraceae
Moraceae
Anacardiaceae
+
+
+
+
+
Voandavenona
Famakilela
Moraceae
+
Tavolo malady
Lauraceae
+
Ficus sp.
Cryptocarya
acuminata
Vahitamboro Danais sp.
Streblus
Mahanoro
dimepate
Tsirika
Pandanus sp.
Rotra
Syzygium sp.
Apana
Ficus sp.
Sira
Neodypsis sp.
Rotra mena Syzygium sp.
Aphloia
Fandramanana
theaeformis
Velatra spécial Ruellia sp.
Durée (en mn)
Tala
Vato
Bakerella sp.
Oncostemum
Kalafana
botryoides
spécial
Hafipotsy
Grewia sp.
Fanalamangidy
Melanophylla
Vavaporetaka
crenata
Kaboka
Voacanga sp.
Sandramy fotProtorhus sp.
sy
Apaliala
Treculia africana
Ramandriona Dilobeia thouarsii
Andriambo.
lamena
Bararata
Gaertnera sp.
Mammea
Nato jabo
vatoensis
Tavilona
Vernonia sp.
Apodytes
Malanimanta
thouvenotii
Voantsosoka
Lambinanala Nuxia sp.
Chrysophyllum
Rahiaka
boivinianum
Ficus lutea
Amontana
Psidium
Goavy
cattleianum
Asteraceae
Mendonciaceae
Rubiaceae
Leguminosae
Myrtaceae
Loranthaceae
+
+
+
+
+
+
+
+
101,57
68,40
+
+
Myrsinaceae
Clusiaceae
16,83
+
Tiliaceae
Melanophyllaceae
Apocynaceae
Anacardiaceae
Moraceae
Proteaceae
Menispermaceae
Rubiaceae
Durée (en mn)
Tala
Vato
169,48
9,03
425,63
29,67
30,97
+
3,25
25,68
+
7,67
130,45
35,92
+
+
26,05
16,58
+
86,73
66,30
+
20,32
+
+
7,15
14,85
15,28
+
138,73
+
26,75
+
Asteraceae
11,62
69,60
+
4,07
Icacinaceae
+
3,52
Loganiaceae
+
+
45,08
17,88
Sapotaceae
+
6,30
Moraceae
+
22,42
Myrtaceae
+
589,02
663,50
EuphorbiaFanorafa
+
173,10
ceae
Kimba spécial Symphonia sp.
Clusiaceae
+
3,23
Terminalia tetrano- CombretaVeso
+
2,02
ra
ceae
Vahirano
Cissus sp.
Vitaceae
+
15,73
104,17
Fohaninasity Psychotria sp.
Rubiaceae
+
260,93
Rohindambo Smilax anceps
Smilacaceae +
5,67
Potameia
Sary
Lauraceae
+
36,60
chartacea
Embelia madaKalamasina
Myrsinaceae
+
10,43
gascariensis
Tambourissa
Ambora
Monimiaceae
+
10,85
thouvenotii
Harungana madaHarongana
Clusiaceae
+
21,45
gascariensis
Nato spécial Sideroxylon sp.
Sapotaceae
+
1,82
Holatra
Champignon
+
Decarydendron heMonimiaceae
+
10,33
Amboralahy
lenae
Sandramy
Anacardia+
1,50
Protorhus sp.
ceae
Mena
Inconnue
1,37
8,82
Champignon
6,60
Tala = site de Talatakely; Vato = site de Vatoharanana; Fr = fruits; Fe = feuilles ;
Fl = fleurs.; *: consommé
17,08
+
+
12,70
87,63
3,65
7,55
98,32
Rubiaceae
+
Moraceae
+
+
62,58
Pandanaceae
Myrtaceae
Moraceae
Arecaceae
Myrtaceae
Flacourtiaceae
Acanthaceae
+
+
+
+
+
38,00
27,28
8,070
36,30
9,020
+
19,10
12,97
1,67
135,15
21,47
17,32
127,82
+
68,68
27,05
Le calcul du coefficient de Jaccard offre une valeur de 0,45;
soit 45 %. Il en découle que le régime alimentaire d’Eulemur
rubriventer des deux sites présente une similarité moyenne.
Aussi, la différence entre le régime d’Eulemur rubriventer des
deux milieux peut être révélée par la constatation de la
durée consacrée à la consommation de chaque catégorie
alimentaire telle que les fruits, les fleurs, les feuilles et bien
d’autres (Cf. Tab. 2 et Fig. 2).
En se basant sur ce tableau récapitulatif (Tab.2) et sur la Fig.2,
nous constatons que dans le milieu dégradé de Talatakely, la
consommation des fruits s’avère très importante par rapport à celle du milieu moins dégradé de Vatoharanana. De
plus en comparant avec l’espèce du site de Talatakely,celle de
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Lemur News Vol. 15, 2010
la station de Vatoharanana comble beaucoup plus sa nourriture avec des fleurs, des feuilles, et d’autres types d’aliments.
Tab. 2: Comparaison de la consommation journalière de
chaque catégorie alimentaire d’Eulemur rubriventer dans les
deux sites durant la période d’observation (en minute).
Fruit
Fleur
Talatakely
80,80
Vatoharanana
72,58
Durée de la consommation
(en minute)
Sites
Feuille
Autres
0,52
4,54
0,12
8,32
11,16
1,63
90
80
70
60
50
40
30
20
10
0
Fruit
Fleur
Feuille
Catégorie alimentaire
Talatakely
Autres
Vatoharanana
Fig.3:Allure de la consommation journalière de chaque catégorie alimentaire d’Eulemur rubriventer dans les deux sites
durant la période d’observation.
Discussion
Eulemur rubriventer est un lémurien hautement frugivore.
Mais la proportion des fruits qu’il consomme varie suivant le
degré de perturbation,de dégradation,de l’altitude du milieu,
ainsi que de la saison. Notons également que la consommation des différentes catégories alimentaires dépend de la
disponibilité des ressources alimentaires (Rasolofonirina,
2001). Lors de notre étude, nous constatons que dans le
milieu dégradé de Talatakely, la consommation des fruits
s’avère très importante que dans le milieu moins dégradé de
Vatoharanana.De plus,en comparant avec l’espèce du site de
Talatakely, celle de la station de Vatoharanana comble beaucoup plus sa nourriture avec des fleurs, des feuilles, et d’autres types d’aliments. Ceci est dû certainement à la saison
cyclonique durant laquelle le vent est violent. Comme le site
de Vatoharanana est beaucoup plus élevé par rapport à Talatakely, il s’avère logique qu’il est beaucoup plus affecté par ce
vent violent.En effet,les fruits deviennent rares car beaucoup
d’entre eux tombent par terre. Selon Zaonarivelo (1999),
pendant la période de crise, Varecia variegata variegata augmente le taux de folivorie même si les feuilles sont des aliments de compensation.Cette stratégie adoptée par l’animal
lors de la période de crise est également observée chez
d’autres espèces de lémuriens de la forêt dense humide
(Ganzhorn, 1988) entre-autres l’Eulemur rubriventer, le Eulemur mongoz qui se nourrissent de fleurs en plus des fruits et
des feuilles durant la période de floraison (Sussman, 1975).
Par ailleurs, Garbutt (1999) argumente que les fruits constituent la majeure partie de l’alimentation d’Eulemur rubriventer.
Mais quand ils ne sont pas disponibles, les feuilles et les fleurs
sont aussi consommées (Rasolofonirina, 2001). Notons à la
même occasion que les primates adoptent différentes stratégies pour affronter le manque de nourriture de base (le
fruit pour notre cas) soit en augmentant le temps de la
recherche de nourriture en se déplaçant beaucoup, soit en
acceptant de consommer des aliments de basse qualité
(Zaonarivelo, 1999).
Par rapport au milieu dégradé, l’abondance des fruits dans le
milieu moins dégradé est évidente.Mais en tenant compte de
l’étude phénologique mensuelle des plantes recensées, ce
n’est pas toujours le cas; car plusieurs facteurs pourraient
agir sur ce milieu.Ainsi le climat,en particulier la pluviosité et
le cyclone, influence la qualité et la quantité de la nourriture
disponible (Dajoz, 1985). En effet, durant la période cyclonique, l’altitude de la station joue un rôle important sur les
arbres à semences. Autrement dit, plus l’altitude d’un milieu
est élevée, plus le vent agit directement sur les arbres et plus
les fruits tombent. Par conséquent, les arbres portent moins
de fruits. L’animal est obligé de se rabattre sur d’autres
catégories alimentaires comme les feuilles, les fleurs, les
champignons, les insectes pour pouvoir combler l’insuffisance de nourriture de base.Ce cas se rencontre dans le site
de Vatoharanana qui est considéré comme milieu moins
dégradé et qui est situé à une altitude plus élevée (1090 m)
par rapport au site dégradé de Talatakely qui se trouve à une
altitude de 1020 m (Brady et al, 1996). Concernant le site de
Talatakely, la dispersion des fruits dans l’espace est insuffisante à cause de la dégradation de ce milieu. Ainsi,au lieu de
combler sa nourriture par d’autres types d’aliments, il est
contraint à se déplacer loin afin de consommer de la nourriture de haute qualité qui lui apporte beaucoup plus d’énergie
comme le glucide, le lipide et les protéines (Zaonarivelo,
1999).
Finalement, en se basant sur les données phénologiques,
nous avons constaté que la consommation de chaque catégorie alimentaire varie suivant leur disponibilité mensuelle
dans chaque mileu. Au mois de décembre, par exemple,
l’Eulemur rubriventer de Vatoharanana consomme beaucoup
plus de fleurs que de fruits par rapport à celui de Talatakely
car pendant ce mois, les fleurs y sont disponibles. Remarquons également que l’espèce de la station de Talatakely ne
consomme que des fruits durant la fructification de l’espèce
introduite de goyave (Psidium cattleianum). Ce type de fruit
est très apprécié par l’animal.
Le régime alimentaire d’Eulemur rubriventer est moyennement similaire dans les deux milieux étudiés.
Cependant, quelques espèces de plantes consommées par
l’animal sont propres à chaque site. L’espèce introduite de
goyave Psidium cattleianum se rencontre uniquement à Talatakely. Notons que l’introduction de cette espèce marque la
dégradation de cette station. Par contre, l’animal de Vatoharanana a l’opportunité de consommer, par exemple, l’espèce Mammae vatoensis qui est endémique à ce site. Cette
similarité moyenne entre les deux régimes implique que la
dégradation du site de Talatakely n’est pas encore poussée à
l’extrême (Randriamahaleo,2005).En effet,il est classé parmi
les sites moyennement dégradés. Selon Tam-Alkis (1997), le
site de Talatakely est séparé de Vatoharanana par une barrière biogéographique (rivière Fompohonona). Il paraît que
la dispersion des graines de part et d’autre de cette rivière
est empêchée. Voilà pourquoi certaines espèces de plantes,
utilisées comme source alimentaire, caractérisent uniquement l’un de ces sites. Par conséquent son régime varie
suivant le site.
Conclusion
Cette étude nous a permis de fournir plus d’informations sur
la relation entre la dégradation de l’habitat d’Eulemur rubriventer et sa consommation alimentaire. L’investigation révèle
une similarité moyenne entre le régime alimentaire adopté
par l’animal de Talatakely et celui de Vatoharanana. L’espèce
semble être principalement frugivore quelque soit le site.
Cependant, la proportion de consommation varie suivant le
milieu. A Talatakely, par exemple, ce lémur à ventre roux se
Lemur News Vol. 15, 2010
nourrit beaucoup plus de fruits par rapport à celui de Vatoharanana où il comble sa nourriture avec des fleurs, des
feuilles, et bien d’autres catégories alimentaires. Ceci est dû
sans doute au passage des deux cyclones (Elita et Gafilo)
dans la région durant la période d’étude. En fait, Vatoharanana se trouve à une altitude très élevée par rapport à Talatakely.En effet, les vents violents agissent directement sur les
arbres fruitiers, conduisant ainsi l’insuffisance des fruits.
Aussi, la consommation de Psidium cattleianum (Myrtaceae),
qui est une espèce introduite propre à Talatakely semble être
très importante dans ce milieu. Par contre, Chrysophillum
boivinianum s’avère être la plus appréciée par l’animal de
Vatoharanana. Toutes ces constatations nous conduisent à
dire que la consommation alimentaire d’Eulemur rubriventer
paraît être conditionnée par la disponibilité de la nourriture
dans chacun des sites visités et par l’état de l’habitat.
Remerciements
Nous tenons à remercier le Centre Valbio, le MICET représentés respectivement par le Professeur Patricia Wright et le
Docteur Benjamin Andriamihaja pour leur soutien et leur
collaboration durant la longue haleine de travail dans le Parc
National de Ranomafana. Nos vifs remerciements s’adressent également à tous les guides de recherche pour leur
assistance (Telo Albert, Victor, Koto, Nirina) et à tout ce qui
contribue, de près ou de loin à la réalisation de ce projet.
Références bibliographiques
Altmann, J. 1974. Observational study of behavior: Sampling
methods. Behavior 49: 227-267.
Brady, L.H.; Jenkens, R.; Kauffmann, J.; Rabearivony, J.; Raveloson, G.; Rowcliffe, M. 1996. Madagascar Expedition 93.
Final Report. Univ. East Anglia. Norwich, U.K.
Brower,J.E.;Zar,J.H.;von Ende,C.N.1990.Field and laboratory methods for general ecology. Kevin Kane, ed. Wm C.
Brown publishers, Dubuque.
Dague, C.; Petter, J.J. 1988. Observations sur le Lemur rubriventer dans son milieu naturel.Pp.78-89.In:L.Rakotovao,V.
Barre,et J.Sayer (eds.), l’Equilibre des Ecosystèmes Forestiers à Madagascar: Acte d’un séminaire international.
IUCN, Gland, Switzerland and Cambridge U.K.
Dajoz 1985. Précis de l’écologie. 5ème edition. Dunod University. Paris. Pp. 135.
Dunbar,R.I.M. 1988.Prosimiens. Primate adaptation and evolution. Academic Press. Harcourt Brace Jovanic. Pp. 67110.
Ganzhorn, J.U. 1988. Food partitioning among Malagasy Primates. Oecologia (Berlin) 75: 436-450.
Ganzhorn, J.U.; Lowry II, P.P.; Schatz, G.E.; Sommer, S. 2001.
The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx 35 (4): 346-348.
Garbutt, N. 1999. Mammals of Madagascar. Yale University
Press, New Haven.
Kremen, C. 1992. Assessing the indicator properties of species assemblages for natural areas monitoring. Ecological
Applications. 2(2): 203-217.
Martin, P.; Bateson, P. 1986. Measuring behavior. Cambridge
University Press. Cambridge.
Mittermeier, R.A.; Louis, E.E.; Schwitzer, C.; Langrand, O.;
Konstant, W.; Rylands, A.B.; Hawkins, F.; Rajaobelina, S.;
Ratsimbazafy, J.H.; Rasoloarison, R.; Roos, C.; Kappeler,
P.M.;MacKinnon,J.2010.Lemurs of Madagascar.Third edition. CI Field Guide Series. Washington, DC, USA.
Mittermeier, R.A.; Konstant, W.R.; Hawkins, F.; Louis, E.E.;
Langrand, O.; Ratsimbazafy, J.H.; Rasoloarison, R.; Ganzhorn, J.U.; Rajaobelina, S.; Tattersall, I.; Meyers, D.M. 2006.
Lemurs of Madagascar. Second edition. CI Field Guide
Series. Washington, DC, USA.
Mittermeier, R.A.; Tattersall, I.; Konstant, W.R.; Meyer, D.;
Mast, R. 1994. Lemurs of Madagascar. Conservation International, Washington, D.C, USA.
Overdorff, D.J. 1993. Ecological and reproductive correlates
to range use in red-bellied lemurs (Eulemur rubriventer)
Page 51
and rufous lemurs (Eulemur fulvus rufus). Pp. 167-178. In:
Kappeler, P.M.; Ganzhorn, J.U., Lemur Social Systems and
their Ecological Basis. New York.
Overdorff, D.J. 1996. Ecological correlates to activity and habitat use in two prosimian primates: Eulemur rubriventer
and Eulemur fulvus rufus in Madagascar. American Journal
of Primatology 40: 327-342.
Randriamahaleo, S.I. 2005. Effets de la dégradation de la forêt
et impacts sur les activités sociales de Propithecus diadema
edwardsi dans deux sites Talatakely et Valohoaka du Parc
National de Ranomafana. Mémoire de DEA d’Anthropologie Biologique. DPAB, Faculté des Sciences, Université
d’Antananarivo.
Randriatahina,G.H.2001.Etude des intéractions sociales des
femelles de Varecia variegata variegata, dans la forêt perturbée de Manombo, Farafangana, Madagascar. Mémoire
de DEA d’Anthropologie Biologique. DPAB, Faculté des
Sciences, Université d’Antananarivo.
Rasolofonirina 2001. Contribution à l’étude comparative du
comportement chez Eulemur rubriventer et Eulemur fulvus
rufus femelles pendant la lactation dans la forêt dense
humide de Ranomafana. Mémoire de DEA. Département
de Paléontologie et d’Anthropologie Biologique, Faculté
des Sciences, Université d’Antananarivo.
Razafimahazo, J.C. 2001. Contribution à l’étude saisonnière
dans l’utilisation verticale de l’habitat par deux lémuriens
Hapalemur aureus et Hapalemur simus dans la forêt dense
humide de Ranomafana Ifanadiana. Mémoire de DEA.
Département de Paléontologie et d’Anthropologie Biologique, Faculté des Sciences, Université d’Antananarivo.
Richard 1978. Behavioral variation: Case of a Malagasy lemur.
Freeman, New York, USA.
Sussman, R.W. 1975. A preliminary study of the behavior and
ecology of Lemur fulvus rufus. Pp. 237-258. In: I. Tattersall
and R.W. Sussman (eds), Lemur Biology. Plenum Press,
New York.
Tam-Alkis, J. 1997. Factors affecting the distribution and
abundance of a Chameleon assemblage in Ranomafana
National Park, Madagascar. DICE, University of Kent and
Canterbury.
Turk, D. 1995. A guide of trees of Ranomafana National Park
and Central eastern Madagascar. Pp. 330.
Zaonarivelo, Z.R. 1999. Analyse des modalités d’adaptation
de Varecia variegata variegata à un milieu perturbé. Cas de
Manombo, Farafangana. Mémoire de DEA. Département
de Paléontologie et d’Anthropologie Biologique, Faculté
des Sciences, Université d’Antananarivo.
Observations of terrestrial latrine behaviour by the southern gentle lemur Hapalemur meridionalis in the Mandena littoral
forest, southeast Madagascar
Timothy M. Eppley* and Giuseppe Donati
Nocturnal Primate Research Group,Department of Anthropology and Geography, Oxford Brookes University, Gipsy
Lane, OX3 0BP, Oxford, UK
*Corresponding author: eppleyti@gmail.com
Key words: southern gentle lemur, Hapalemur meridionalis,
defecation, latrines, Mandena
Latrine behaviour is defined as the non-random selection of
a specific defecation site,and although it is rarely described in
primates it is well known among other mammalian species as
a form of olfactory communication (Irwin et al., 2004).Olfactory compounds, which convey chemical signals, are transmitted via scent-producing skin gland secretions, saliva, and/
or waste products (Epple, 1986). Olfaction signals may be
advantageous as they are not limited spatially and temporally,
allowing individuals of a predominately visual communication
Page 52
to receive signals when distant from the source (Schilling,
1979;Irwin et al., 2004). Olfactory signals may transmit information pertaining to environmental familiarisation (Schilling,
1979), reproductive behaviour and condition (Epple, 1986),
territorial demarcation (Mertl-Milhollen, 1979),and inter- or
intra-group spacing (Schilling, 1979; Epple, 1986).
Previous literature has discussed latrines by varying in location (arboreal, terrestrial, or subterranean), and being further analysed by volume of faeces and spatial distribution
(Schilling, 1980; Boonstra et al., 1996; Irwin et al., 2004; Pouvelle et al., 2009). This behaviour appears to be well studied
within other mammals but for primates, especially strepsirhines, latrine use is only sparsely mentioned within much
broader scope research (Irwin et al., 2004). In this report we
present our observations of this peculiar behaviour exhibited by the southern gentle lemur, Hapalemur meridionalis, a
threatened primate that occurs in southeast Madagascar.We
will use our observations to review the hypotheses offered
thus far to explain latrine use,i.e.advertisement of sexual cycle,predation avoidance,intra- group and inter-group spacing
in the context of the fragmented littoral forest.
Methods
This research was conducted from May to July 2008, on the
southern gentle lemur within the Mandena littoral forest
(24°95’S 46°99’E), a coastal forest in southeast Madagascar.
The littoral forest is among the most endangered ecosystems in Madagascar (Bollen and Donati, 2006) and Mandena
is a protected conservation zone encompassing 230 hectares of fragmented and partially degraded littoral forest
interspersed with marsh and swamp. Three groups of H.
meridionalis (mean = 5.7 ind/group) were habituated and
followed daily from dawn to dusk with 62 hours of observation recorded (Eppley and Donati, in press). These lemurs
are of particular interest, as they do not subsist exclusively
on bamboo like the majority of their congeners. Rather, the
southern gentle lemur exhibits a dietary predilection for
terrestrial (turf) grasses while displaying a unique grazing
behaviour (Eppley and Donati, in press). Although the main
research being conducted focused on the feeding ecology of
these animals, opportunistic observations of latrine behaviour were collected ad libitum. In addition to habitat characteristics and GPS waypoints taken at the feeding and resting
sites of three groups, latrine locations were also recorded.
Spatial analyses were carried out with ArcMap version 9.3,
with the outermost feeding and resting site waypoints for
each group being used to create the minimum polygon for
their respective ranging areas.
Results
On three separate occasions an entire group of foraging H.
meridionalis were witnessed descending to the ground and
defecating in succession either near or under a high-rooted
tree of different species. Latrine bouts were recorded ad libitum on a single occasion for Group B (four individuals) and
twice for Group C (seven individuals). Observations took
place within the forest fragment, and were never witnessed
in open canopy areas. The three occurrences of this terrestrial latrine behaviour were observed shortly after individuals had awoken from a midday resting bout (between 11:00
and 14:00) at distances approx. 20 m from the resting site.
The three locations where the latrine behaviour was exhibited are shown in Figure 1.Little overlap between the ranging
areas of the three groups was observed with 0.92 ha (7.74 %)
calculated to exist between groups A and B, 0.18 ha (1.68 %)
between groups A and C, and 0.06 ha (0.73 %) between
Lemur News Vol. 15, 2010
groups B and C. After an individual had defecated, they
ascended three to four meters and continued feeding.Subsequently, the group followed an order of sequential defecation, where by one conspecific would defecate and the next
would rapidly follow.The individuals remaining at an elevated
height always appeared vigilant, scanning the surrounding
area and sometimes continuing to forage, while the conspecific was on the ground. Upon inspection of two of the
defecation sites, accumulations of hardened faecal matter
were identified. Dissimilarly, the third site consisted of only
fresh faeces with no sign of old faecal matter.
Fig. 1: Ranging areas of the three observed H. meridionalis
groups within the northeast corner of the Mandena littoral
forest. The three latrine sites were observed within the territorial boundary buffer zones of Groups A & C and B & C.
Discussion
Among primates,latrine behaviour has been recorded (Table
1) in Alouatta seniculus (Gilbert, 1997; Feeley, 2005; Neves et
al., 2009; Pouvelle et al., 2009), Ateles geoffroyi (Notman et al.,
2009), as well as the strepsirhines: Cheirogaleus major, C.
medius, Lepilemur leucopus (Charles-Dominique and Hladik,
1971; Russell, 1977), L. microdon, L. ruficaudatus, Hapalemur
aureus, H. griseus, Prolemur simus, and Lemur catta (Irwin et al.,
2004). With the exception of Neotropical primates, however,minimal research has been conducted to understand its
function within primates and latrine utilisation is often a matter of debate. In Ranomafana National Park, for example, H.
griseus have been observed to occasionally use the same
resting/sleeping sites and since they often defecate very soon
after they wake up (Tan,pers.comm.),an accumulation of faecal material under these trees may appear inadvertently
latrine-like (Notman et al., 2009; Pouvelle et al., 2009). Thus,
latrine use by H. griseus may be anecdotal within this population.
Irwin et al. (2004) presented four non-mutually exclusive
hypotheses for the possible adaptive function of primate
latrines: 1) advertisement of sexual cycle,2) predation avoidance, 3) intra-group spacing, 4) and inter-group spacing.
The conveyance of scent-marks is well known to advertise
sexual activity and receptivity (Asa, 2008). If this holds true
for H. meridionalis, latrines should be used more frequently
during the breeding seasons. It has been reported that H.
griseus mate between June and July, experiencing a gestation
length of approximately 137 days (Tan, 2006). Though our
research potentially overlapped with the mating season, we
made no observations of mating during the study period.
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Lemur News Vol. 15, 2010
Thus, we had no possibilities to compare the mating season
with pre- or post-mating periods, as the hypothesis testing
would require. However, since two of the latrines at Mandena appeared to be utilized long-term, similar to the findings of Irwin et al.(2004),we conclude that the advertisement
of sexual receptivity is unlikely the sole function of lemur
latrines.
Tab. 1: Observed primates that have exhibited terrestrial
latrine behaviour. Adapted from Irwin et al. (2004).
Species
Hapalemur
meridionalis
Hapalemur
griseus
Prolemur
simus
Localities
Mandena Conservation Zone
Analamazaotra
Special Reserve
Ranomafana
National Park
Lemur catta
Isalo National Park
J. Jernvall and P. Wright
(in Irwin et al., 2004)
Lepilemur
leucopus
Lepilemur
microdon
Lepilemur sp.
(?microdon)
Lepilemur
ruficaudatus
Ateles
geoffroyi
Alouatta
seniculus
Beza Mahafaly
Special Reserve
Manombo Special
Reserve
Kalambatritra
Special Reserve
J. Ratsimbazafy (in Irwin et al.,
2004)
Kirindy Forest
References
This study
Irwin et al. (2004)
P. Wright (in Irwin et al., 2004)
L. Nash (in Irwin et al., 2004)
Irwin et al. (2004)
J.U. Ganzhorn (in Irwin et al.,
2004)
Runaway Creek NaNotman et al. (2009)
ture Preserve, Belize
Nouragues Reserve,
Pouvelle et al. (2009)
French Guiana
Gentle lemurs have a particularly effective predator avoidance strategy including camouflage from cryptic pelage, rapid flight behaviour,and potential cathemeral activity pattern
(Mutschler et al., 1999; Curtis et al., 2006; Tan, 2006). Several
potential predators of Hapalemur exist in the littoral forest.
There have been documented cases of fossa Cryptoprocta
ferox preying on H. griseus (Goodman and Pidgeon, 1999;
Sterling and McFadden, 2000). The Madagascar tree boa Sanzinia madagascariensis (= Boa manditra) also prey on Hapalemur spp.(Goodman et al.,1993;Rakotandravany et al.,1998),
and several aerial predators (Madagascar harrier hawk Polyboroides radiatus, Frances’s sparrowhawk Accipiter francesii,
Henst’s goshawk Accipiter henstii, common barn owl Tyto alba,
and the Madagascar long-eared owl Asio madagascariensis)
represent a threat to medium-sized lemurs (Goodman et al.,
1993; Wright, 1997; Karpanty and Goodman 1999). In fact,
the concealment of Hapalemur faeces under large high-rooted trees may theoretically act as a safeguard against predation by impairing the ability of a predator to detect the prey
population (Boonstra et al.,1996;Irwin et al.,2004).Although
these observations are in accord with the anti-predator idea,
single faecal deposits were also detected at indiscriminate
locations. Thus, more data are necessary to test the hypothesis of latrine behaviour as an anti-predator strategy.
Intra-group spacing has also been suggested to advertise
proximal resource use and assist in inter-individual spacing
(Kruuk, 1992).In accord with Irwin et al.(2004),however,it is
unlikely that Hapalemur latrine behaviour is used for intragroup spacing, as they live in cohesive family units.
The territorial demarcation hypothesis suggests that scentmarks are placed around home range boundaries to act as a
delineation of the territory, i.e. inter-group spacing (MertlMillhollen, 1979; Lewis, 2005). In fact, it is evident from our
observations that H.meridionalis chose defecation sites in the
narrow areas of overlap with neighbouring conspecifics
groups (Fig. 1). If this adaptive function holds true, latrine
behaviour might be even more common in areas of dense
population (Irwin et al.,2004),such as the forest fragments of
Mandena (Eppley and Donati, in press).
Although the exhibition of preferred, non-random defecation sites is most likely multifactorial, latrines in Mandena appear to best fulfil the function of inter-group spacing. Therefore, latrines may be a low-energy behavioural response to
the ecological challenge of defending resources with minimal
rates of agonism (Irwin et al.,2004).In the future,more quantitative studies should focus on seasonal and spatial exhibition of latrine use to verify whether this behaviour is intrinsically linked to territorial delineation and resource defence in
lemurs.
Acknowledgements
We would like to thank the Commission Tripartite of the
Malagasy government, Ministère de l’Environnement, des
Eaux et forêts of the Malagasy government, the University of
Antananarivo, and CAFF/CORE for permission to conduct
research, as well as the Malagasy Institute for the Conservation of Tropical Environments (MICET) for all of their logistical assistance. Financial support was provided partly by the
Chester Zoo (NEZS) and QMM.We would also like to thank
the QMM Environmental Team, most especially Manon Vincelette, Jean-Baptiste Ramanamanjato, Johny Rabenantoandry, Faly Randriatafika, and Christophe Rambolamanana for
all of their advice and logistical help. We are grateful to Jörg
Ganzhorn for all of his continuous support and scientific advice.Thank you to the entire staff of the Oxford Brookes Primate Conservation MSc program, especially Simon Bearder,
Anna Nekaris, and Vincent Nijman. We greatly appreciate
the GIS assistance of Maureen Mullen. My sincere gratitude
goes to my field guide Robertin "Tintin" Ravelomanantsoa
and research assistant Abi Coleman for their companionship
and tireless help in the marecage.
References
Asa, C.S. 2008. Scent and the single male: ring-tailed lemurs
produce honest signals.Molecular Ecology 17:3223-3224.
Bollen,A.;Donati,G.2006.Conservation status of the littoral
forest of south-eastern Madagascar: a review. Oryx 40:
57-66.
Boonstra,R.;Krebs,C.J.;Kenney,A.1996.Why lemmings have
indoor plumbing in summer. Canadian Journal of Zoology
74: 1947-1949.
Charles-Dominique,P.;Hladik,C.M.1971.Le Lepilemur de sud
de Madagascar: ecologie, alimentation, et vie sociale.
Revue d’Écologie (La Terre et la Vie) 25: 3-66.
Curtis, D.; Donati, G.; Rasmussen, M. 2006. Cathemerality.
Folia Primatologica 77: 5-6.
Epple, G. 1986. Communication by chemical signals. Pp.
531-580. In: G. Mitchell; J. Erwin (eds.), Comparative
Primate Biology, Volume 2A: Behavior, Conservation and
Ecology. Alan R. Liss, New York.
Feeley, K. 2005. The role of clumped defecation in the spatial
distribution of soil nutrients and the availability of nutrients for plant uptake. Journal of Tropical Ecology 21:
99-102.
Gilbert, K.A. 1997. Red howling monkey use of specific defecation sites as a parasite avoidance strategy. Animal Behaviour 54: 451-455.
Goodman, S.M.; Pidgeon, M. 1999. Carnivora of the Réserve
Naturelle Intégrale d’Andohahela, Madagascar. Fieldiana:
Zoology 94: 256-68.
Goodman, S.M.; O’Connor, S.; Langrand, O. 1993. A review of
predation on lemurs: implications for the evolution of
social behavior in small, nocturnal primates. Pp. 51-66. In:
P.M. Kappeler; J.U. Ganzhorn (eds.). Lemur Social Systems
and their Ecological Basis. Plenum Press, New York.
Irwin, M.T.; Samonds, K.E.; Raharison, J.-L.; Wright, P.C. 2004
Lemur latrines: observations of latrine behavior in wild
Page 54
primates and possible ecological significance. Journal of
Mammalogy 85: 420-427.
Lewis, R.J. 2005. Sex differences in scent-marking in sifaka:
mating conflict or male services? American Journal of Physical Anthropology 128: 389 98.
Karpanty, S.M.; Goodman, S.M. 1999. Diet of the Madagascar
harrier-hawk, Polyboroides radiatus, in southeastern Madagascar. Journal of Raptor Research 33: 313-316.
Kruuk, H. 1992. Scent marking by otters (Lutra lutra): signalling the use of resources. Behavioral Ecology 3: 133-140.
Mertl-Millhollen, A.S. 1979. Olfactory demarcation of territorial boundaries by a primate-Propithecus verreauxi. Folia
Primatologica 32: 35 2.
Mutschler, T. 1999. Folivory in a small-bodied lemur: the
nutrition of the Alaotran gentle lemur (Hapalemur griseus
alaotrensis). Pp. 221-239. In: H. Rasaminanana; B. Rakotosamimanana; J.U. Ganzhorn; S.M. Goodman (eds.). New
Directions in Lemur Studies. Kluwer Academic / Plenum
Publishing, New York.
Neves, N.D.S.; Feer, F.; Salmon, S.; Chateil, C.; Ponge, J.-F. 2009.
The impact of red howler monkey latrines on the distribution of main nutrients and on topsoil profiles in a tropical rain forest. Austral Ecology doi:
10.1111/j.1442-9993.2009.02066.x
Notman, H.; Hartwell, K.; Pavelka, M.S. 2009. Spider monkey
"latrine sites" at Runaway Creek Nature Reserve, Belize.
American Journal of Primatology 71(Suppl 1): 91.
Pouvelle, S.; Jouard, S.; Feer, F.; Tully, T.; Ponge, J.-F. 2009. The
latrine effect: impact of howler monkeys on the distribution of small seeds in a tropical rain-forest soil. Journal
of Tropical Ecology 25: 239-248.
Rakotondravony, D.; Goodman, S.M.; Soarimalala, V. 1998.
Predation on Hapalemur griseus griseus by Boa manditra
(Boidae) in the littoral forest of eastern Madagascar. Folia
Primatologica 69: 405 08.
Russell, R.J. 1977. The behavior, ecology, and environmental
physiology of a nocturnal primate, Lepilemur mustelinus
(Strepsirhini, Lemuriformes, Lepilemuridae). Unpubl. Ph.
D. thesis, Duke University, Durham, North Carolina.
Schilling, A. 1979. Olfactory communication in primates. Pp.
461-542. In: G.A. Doyle; R.D. Martin (eds.). The Study of
Prosimian Behavior. Academic Press, New York.
Schilling, A. 1980. Seasonal variation in the fecal marking of
Cheirogaleus medius in simulated climatic conditions. Pp.
181-190. In: P. Charles-Dominique; H.M. Cooper; A.
Hladik; C.M. Hladik; E. Pages; G.F. Pariente; A. Petter-Rousseaux; A. Schilling (eds.). Nocturnal Malagasy Primates:
Ecology, Physiology, and Behavior. Academic Press, New
York.
Sterling, E.J.; McFadden, K. 2000. Rapid census of lemur population in the Parc National de Marojejy, Madagascar. A
floral and faunal inventory of the Parc National de Marojejy, Madagascar: with reference to elevation variation. Fieldiana: Zoology 97: 265-274.
Tan, C.L. 2006. Behavior and ecology of gentle lemurs (genus
Hapalemur). Pp. 369-381. In: L. Gould; M. Sauther (eds.).
Lemurs: Ecology and Adaptation. Springer, New York.
Wright, P.C. 1997. Impact of predation risk on the behaviour
of Propithecus diadema edwardsi in the rain forest of Madagascar. Behaviour 135: 483-512.
Wright, P.C. 1999. Lemur traits and Madagascar ecology:
coping with an island environment. Yearbook of Physical
Anthropology 42: 31-72.
Lemur News Vol. 15, 2010
Conservation des lémuriens via la protection de leurs habitats et le développement communautaire dans les corridors
de Betaolana et Tsaratanana-Betaolana,
région de SAVA
Lala Razafy Fara1*, Iarilanto Andriamarosolo2
Madagascar & Western Indian Ocean PO, BP 738
Antananarivo 101, Madagascar
2WWF Andapa, BP 28, Andapa 205, Madagascar
*Corresponding author: frazafy@wwf.mg
1WWF
Contextes
Ecologique:
Madagascar est connu pour sa haute valeur en biodiversité.
Sa flore et sa faune ont une valeur d’endémicité très élevée
(au dessus de 80 %) due entre autres à son insularité. Madagascar est donc plus riche en espèces endémiques comparées à d’autres continents du monde.Le microclimat de l’île a
permis que d’une région à une autre, la flore et la faune constituent une richesse spectaculaire à part.
Pour la partie Nord de Madagascar, la flore luxuriante, avec
des espèces endémiques du genre Dalbergia, est encore à
découvrir.Le WWF a travaillé dans la région de SAVA pour la
mise en place de deux Aires Protégées (AP),Parc National de
Marojejy et Réserve Spéciale d’Anjanaharibe Sud, actuellement sous gestion du Madagascar National Parks. Pour le
WWF,la conservation du flux génétique implique le maintien
et la restauration de la connectivité écologique. Ce maintien
peut être le plus important paramètre le long des pentes
altitudinales car cette connectivité est actuellement très
rare au sein de l’écorégion de l’Est.De plus,il peut constituer
un refuge pour la biodiversité vu les changements du climat
(Erdmann et al., 2005).
Eu égard aux efforts déjà investis dans la protection des deux
AP (Parc de Marojejy et de la Réserve Spéciale d’Anjanaharibe Sud), le WWF a continué ses efforts de conservations
dans les deux corridors forestiers (Betaolana et Tsaratanana-Betaolana). Dans ces localités, les espèces endémiques
sont aussi très remarquables comme le palmier Marojejya
insignis et la fougère Asplenium marojyense. La forêt dense et
humide de cette partie de l’île abrite une multitude de faune
à découvrir et à protéger.
La forêt occupe encore 35,60 % de la région de SAVA (données images satellites de 2000),ce taux est élevé par rapport
à d’autres régions de Madagascar. La richesse en biodiversité
de cette zone est démontrée par de nombreuses études, sur
la flore et sur la faune, conduites dans cette zone.
Pour ces deux corridors Betaolana et Tsaratanana-Betaolana, les inventaires effectués par Rajaonson et Rakotonirina
(2007) pour le WWF ont montré l’existence de 10 espèces
de lémuriens pour le corridor Betaolana, et de sept espèces
pour le corridor Tsaratanana Betaolana, 84 espèces d’oiseaux pour l’ensemble des deux corridors. En comparaison
avec les inventaires des lémuriens effectués par Goodman et
al. (2003), la région d’Andapa, incluant les AP de Marojejy et
d’Anjanaharibe-Sud et le corridor forestier de Betaolana,
possèdent une richesse spécifique en communautés de lémuriens et tient une place importante en biodiversité à Madagascar.La synthèse des études déjà effectuées dans la zone a
recensé 12 espèces de lémuriens dont: Microcebus rufus,
Cheirogaleus major, Allocebus trichotis, Phaner furcifer, Avahi
laniger, Lepilemur mustelinus, Daubentonia madagascariensis,
Hapalemur griseus griseus, Eulemur rubriventer, Eulemur fulvus
Page 55
Lemur News Vol. 15, 2010
albifrons, Propithecus candidus, Indri indri. Parmi ces espèces
citées, celles non rencontrées dans les deux corridors sont:
Indri indri et Phaner furcifer (pour les deux corridors Betaolana et Tsaratanana-Betaolana) et Allocebus trichotis pour le
corridor Tsaratanana Betaolana).
Parmi les espèces de lémuriens, le Simpona (Propithecus candidus) est une des 25 espèces de primates les plus menacées
dans le monde (Mittermeier et al., 2005), d’où l’intérêt de se
focaliser sur sa conservation. Certains auteurs (Petter et al.,
1979; Tattersall, 1982) pensent que l’habitat du Simpona
pourrait éventuellement s’étendre vers le Sud jusqu’aux
forêts de la péninsule de Masoala. Il est par contre prouvé
que le versant Ouest de Anjanaharibe-Sud, actuellement
sans statut de protection, héberge une population importante de Simpona. La population de Simpona de la région
Andapa et donc mondiale est estimée à une valeur comprise
entre 100-1000 individus (Mittermeier et al., 1994). Des
inventaires effectués par le WWF vers la fin 2006 ont relevé
que le Simpona se rencontre aussi vers le Nord du Corridor
de Betaolana en allant vers le Nord Ouest du côté du massif
de Tsaratanana.
Social et économique:
Les deux corridors forestiers, Betaolana et Tsaratanana
Betaolana, couvrent approximativement une superficie respective de 16 500 ha et de 130 900 ha et sont très riches en
forêt. En se référant aux délimitations sur la carte 1, les deux
corridors renferment encore jusqu’à 90 % de forêts. Situées
sur des sols ferralitiques, les forêts des deux corridors sont
localisées entre les altitudes 850 et 1600 m pour Betaolana
et 800 à 2280 m d’altitude pour Tsaratanana-Betaolana. Les
deux corridors jouissent encore du climat humide de la
région de SAVA.
Les deux corridors appartiennent aux districts d’Andapa
(pour le Corridor de Betaolana) et de Bealanana (pour le
corridor de Tsaratanana-Betaolana). Les populations des
communes locales vivant à la périphérie de ces corridors
sont estimées, en 2009, à 72 521 pour le corridor Betaolana
et à 41 333 pour le corridor Tsaratanana-Betaolana (à partir
des données d’INSTAT 1993).
Dans la région de SAVA, les forêts dans les deux corridors
Betaolana et Tsaratanana Betaolana font partie des domaines forestiers de l’Etat. Ils n’ont de ce fait pas de statuts
particuliers (Garreau et Manantsara, 2003). Toutefois, le
WWF, connaissant l’importance de la flore et la faune dans
cette zone, a mis en œuvre de 2005 à 2008 deux projets
spécifiques pour la conservation des lémuriens et de leurs
habitats dans la région de SAVA. Dans le cadre des projets
mis en œuvre par le WWF qui se sont succédés dans la région de SAVA, celui-ci a travaillé avec les populations locales
pour mettre ces deux corridors sous statuts de Nouvelles
Aires Protégées. Pour le Corridor Betaolana, huit communautés de bases ayant reçu des contrats de transferts de gestion des lots de forêts ont déjà déposé leur manifestation
d’intérêt dans ce sens en 2008. Les différentes étapes et procédures à respecter suivent actuellement normalement leur
cours.
Cet article, eu égard à tous les acquis dans le cadre des
projets du WWF, est une capitalisation des expériences de
WWF Madagascar pour les projets de conservation des
lémuriens et de leurs habitats dans le Nord de Madagascar.
L’un des deux projets est connu sous son appellation courte,
projet Simpona. Son but est en effet de mettre en exergue
cette espèce phare bien qu’elle ne soit pas la seule à être
protégée dans le cadre des projets du WWF.
Approche de conservation
Les sites des deux projets
La région de SAVA se trouve dans l’ex Province d’Antsiranana au Nord de Madagascar. Les deux projets du WWF
dans cette localité ont été conduits dans deux corridors
forestiers entre les Aires Protégées Tsaratanana (Réserve
Naturelle Intégrale), Marojejy (Parc National) et Anjanaharibe Sud (Réserve Spéciale). La carte suivante montre la situation générale de ces localités.
Les objectifs de conservation
A partir de la connaissance des richesses de cette localité,
des pressions et menaces sur les espèces cibles,la finalité des
deux projets était de freiner l’utilisation irrationnelle de la
forêt tout en construisant un environnement où les populations locales pourront vivre en harmonie avec la nature.
Découlant de cette finalité, les objectifs des deux projets ont
été de: 1) Mieux connaître le niveau de menace sur les
lémuriens et sur leurs habitats; 2) Elaborer des scénario de
zonages et de gestion; 3) Conscientiser et éduquer les
communautés locales concernant les menaces et la protection des lémuriens; 4) Initier de nouveaux transferts de
gestion des forêts auprès des communautés locales de base
(sur la partie Ouest du Corridor de Betaolana); 5) Protéger
et/ou restaurer les habitats des lémuriens; 6) Renforcer la
protection des lémuriens par l’extension et la création de
nouvelles aires protégées; 7) Vulgariser et promouvoir les
produits de substitution des principaux produits forestiers;
8) Procéder au suivi d’évaluation des méthodes et procédures de gestion internes des associations des forêts; 9)
Restaurer les terrains défrichés de la périphérie du corridor.
En bref, les deux projets essaient de renforcer les conditions
requises pour la conservation à long terme de la biodiversité
via la conservation des fonctions écologiques des deux corridors (Betaolana et Tsaratanana-Betaolana) de manière participative.
Diagnostic participatif: Mieux connaitre pour mieux
protéger
Cartographie
A partir des connaissances issues de la littérature, une cartographie simplifiée basée sur des cartes topographiques
(échelles 1/100 000) et des interprétations des images satellites 2000 a été élaborée. L’objectif est de partir des limites
des forêts à partir de ces images pour délimiter des zones où
les inventaires forestiers vont être réalisés. De même,de par
cette technique, des zonages forestiers et des cartes d’occupation des sols sont élaborés.Le zonage forestier se base sur
les états de dégradations des forêts. Les unités semblables
ont été groupées dans une même catégorie définie pour un
objectif spécifique (conservation, enrichissement / restauration, droit d’usage).
Inventaire des lémuriens par des primatologues
Pour mieux intégrer les populations locales dans l’importance de la conservation des lémuriens, elles ont été invitées
à participer aux inventaires des lémuriens.Leur connaissance
de base, combinée aux connaissances scientifiques de deux
primatologues recrutés ont été pour renforcer les acquis
dans le cadre de la littérature. Cette approche a aussi permis
d’élaborer des documents de base pour le suivi des lémuriens et de choisir des espèces pour la restauration
forestière.
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Lemur News Vol. 15, 2010
Fig. 1: Carte de localisation générale des sites.
Etudes des pressions et menaces sur les lémuriens et leurs
habitats
Les études sur les pressions et menaces ont été conduites
selon des enquêtes informelles et formelles et selon des observations directes.Les enquêtes informelles servent à la fois
à gagner la confiance des populations locales et à recueillir le
maximum d’informations. Les enquêtes formelles sont utilisées par les consultants primatologues pour une meilleure
représentativité des réponses. Les membres de l’équipe de
WWF, à mesure de l’avancement de la conduite des activités
dans le cadre des deux projets, ne cessent de faire des
recoupements entre toutes les réponses obtenues.
La participation des membres des communautés de base est
indispensable dans les deux types d’enquêtes pour qu’ils se
sentent responsables et pour confronter les réponses au fur
et à mesure que des biais sont observés. Les méthodes
classiques de recherches participatives utilisées sont du
genre MARP: Méthode Accélérée de Recherche Participative et PALM: Participatory Learning Methods ou Méthode
d’apprentissage Participatives. Les membres de l’équipe du
WWF ont reçu auparavant des formations sur ces méthodes. Dans le cadre de leur travail, ces méthodes sont
conduites lors des premières approches au sein d’une nouvelle communauté demandant à gérer une ressource naturelle dans leur terroir.
Responsabilisation sous forme de transfert de
gestion
Inventaire forestier et zonage
Dans chaque localité de travail avec une communauté, des
inventaires forestiers ont été conduits. La finalité est de connaitre les potentialités des différents types de forêts en
produits forestiers ligneux et non ligneux. Une uniformisation des méthodes de relevés a été réalisée. A partir des
cartes de zonages élaborées, les inventaires ont été concentrés dans les zones de conservations et des droits
d’usage. Des parcelles imbriquées sont définies. Elles ont des
surfaces de 100 x 100 m pour des diamètres de 1,30 m (dhp)
supérieur ou égal à 30 cm; deux parcelles de 25 x 25 m pour
les arbres de dhp compris entre 10 cm à 30 cm; et deux
parcelles de 5 x 5 m.Les dimensions de ces parcelles peuvent
varier en fonction du relief (si le terrain est trop accidenté, la
réduction des dimensions est préconisée) et leur nombre
varié. Mais quelques soient les variantes, une moyenne de un
hectare par type de forêt est requise pour les gros diamètres.
Elaboration de plan d’aménagement
En vue de l’obtention des contrats de transfert de gestion
des forêts auprès du Ministère des forêts, chaque communauté devrait établir des plans d’aménagement des forêts.
Lemur News Vol. 15, 2010
Les plans d’aménagement suivent les directives proposées
par la Direction Générale des forêts. Le WWF, pour l’élaboration de ces plans,a surtout veillé à ce que les prélèvements
respectent le principe de la durabilité à savoir: ne prélever
que le volume correspondant aux accroissements moyens
annuels. Pour un meilleur équilibre entre les besoins des
populations locales, des reboisements en espèces introduites sont aussi proposés dans ces plans d’aménagement,
mais dans des parcelles en dehors des forêts naturelles.
Appropriation sous forme de contrôle
L’approche d’appropriation sous forme de contrôle a aussi
été développée pour atteindre les objectifs des deux projets.
Elle consiste à encourager les membres des communautés à
l’établissement de parcelles d’observation en forêt en se
basant sur les pistes existantes et sur les signes visibles de
pressions (coupe, pièges). Des représentants dynamiques au
sein de chaque communauté sont ainsi élus et font des visites
(contrôles) régulières, parfois inattendues, en forêts. Ces
visites sont organisées pour observer la biodiversité
(floraison des plantes, augmentation du nombre des groupes
de lémuriens observés, passage d’un oiseau ou autre type
d’animal faisant la particularité de leur forêt etc.) et pour
constater si des pressions sur les lémuriens et la forêt sont
encore présentes. Ces membres notent leurs observations
dans des cahiers réservés pour ces observations et tout
autre évènement qu’ils jugent importants (rencontre avec
d’autres personnes, etc.).
Mesures d’accompagnement
Le WWF défini les mesures d’accompagnement de toute
activité développée pour contribuer à l’amélioration des
conditions de vie des populations locales. Ces activités doivent à la fois réduire les pressions sur la biodiversité en générale et sur les cibles de conservation en particulier (forêt
naturelle et lémurien) et compenser les efforts de conservations entrepris. L’approche consiste d’abord à analyser les
résultats de toutes les études préalables aux transferts de
gestion des forêts. A partir de ces analyses, les potentialités
de chaque terroir (à partir des cartes d’occupation des sols
et des rendements obtenus pour chaque spéculation engagée) dans lesquels vivent les communautés sont dégagées.
Les mesures à développer cherchent ainsi à augmenter les
sources de revenus des paysans et à améliorer leur alimentation pour une meilleure santé.
Résultats et discussions
Inventaires forestiers et zonages
Au total, 14 inventaires forestiers (correspondants au nombre de transfert de gestion des forêts) ont été effectués dans
la région de SAVA. La potentialité des forêts est variable. Le
nombre des arbres de dhp > 30 varie de 200 à 400/ha. Au
total, 200 espèces de plantes (ligneuses et non ligneuses)
sont inventoriées. D’un site à l’autre, le nombre des espèces
ligneuses inventoriées varie de 45 à 87.
Les espèces les plus fréquemment rencontrées sont: Tambourissa religiosa,Weinmannia rutembergii,Zantoxyllon mananarense, Chrysophyllum boivinianum, Canarium madagascariensis,
Symphonia fasciculata, Diospyros aff.ambilensis, Macaranga
decaryana, Erythroxylum sphaeranthum, Brachylaena merana,
Syzygium emirnense, Uapacca densiflora, Ocotea cymosa…
En fonction de l’éloignement des forêts par rapport aux villages, leur état de dégradation diffère. Cette observation a
permis de faire trois grande classifications: forêt naturelle
plus ou moins intacte,classée à protéger ou à conserver (for-
Page 57
mant donc le noyau dur); forêt partiellement dégradée, localisée encore en plein cœur de la forêt, classée comme forêt à
restaurer; forêt naturelle à faible potentialité, due à un degré
d’écrémage localisée à la périphérie des lisières, classée
comme zone de cantonnement de droit d’usage.
Transfert de gestion des forêts
Le WWF a pu mettre en place dans le cadre de ces deux projets 14 transferts de gestion. Pour chaque communauté, la
surface totale des forêts dans ces transferts varie de 300 à
5000 ha (dépendant du taux de couverture forestière dans le
territoire de chaque village d’appartenance de la communauté). Les zonages des forêts sont décrits précédemment.
En principe, les contrats sont établis pour trois ans. Ensuite
une évaluation devra se faire par le Service Forestier en partenariat avec les communes d’appartenance des communautés gestionnaires des forêts. Etablis à partir de 2007, certains
contrats nécessitent ainsi une évaluation à partir de cette
année ou au plus tard en début de l’année prochaine.
Au total,les 14 transferts de gestion des forêts ont permis de
sécuriser sous la gestion des COBA,27 000 ha de forêts.Ces
forêts incluent tous les types de forêts à différents usages définis auparavant (conservation, restauration, droit d’usage).
Les valeurs de la restauration pour le WWF sont présentées
dans son document de la vision de la biodiversité (Erdmann
et al., 2005) qui a défini 40 aires comme Aires Prioritaires de
conservation de par leur valeur en biodiversité. Les études
sur leur état de dégradation ont relevé aussi que 23 de ces aires auront probablement besoin d’importante restauration
(< 20 % de forêt), si elles doivent entièrement concourir à la
conservation de la biodiversité. Dans tous les sites de transferts de gestion des forêts, le WWF met ainsi l’accent sur
l’importance de la restauration. Les communautés avec l’encadrement du WWF, des observations sur terrain et des
inventaires effectués définissent ainsi des zones de restauration dont la superficie varie d’une communauté à une
autre.Les espèces utilisées pour ces restaurations des forêts
dégradées sont essentiellement des essences autochtones.
Leur choix est justifié par leur emplacement (héliophile pour
les zones très ouverts et/ou périphérie de la forêt; nomade
pour les zones sous couvert des espèces héliophiles) ou par
leur utilisation (construction, nourriture des lémuriens).
Suivis et contrôles
Le WWF, pour faciliter l’uniformisation des suivis et contrôle en matière des lémuriens, a élaboré un livret sur les
lémuriens avec la photo des espèces et une description
sommaire des espèces. L’idée de départ était d’exploiter ces
livrets peu avant la fin des projets pour les analyser. Il a
pourtant été constaté que les représentants des communautés n’ont pas utilisé les livrets, mais les a bien classés dans
leur valise. Leur explication est que le livret (en couleur) est
trop beau pour être amené et abimé en forêt à cause de
l’humidité. Néanmoins, les suivis et contrôles ont été effectivement effectués par les communautés. De plus, les données ont été stockées soit dans des cahiers à part, soit dans
leur tête.
Dans le cadre des suivis et contrôles instaurés de manière
participative, des suivis et contrôles à part doivent aussi être
faits par les organismes techniques d’appuis des communautés. En effet, à travers les expériences de l’élaboration du
livret, il a été constaté que les instructions et formations
n’ont pas été suivies correctement. Les agents des deux projets, ne se sont donc rendus compte qu’un peu tardivement
de la nécessité de faire aussi des suivis et contrôles rapprochés.
Page 58
Lemur News Vol. 15, 2010
développée pour le long terme. Toutefois, le WWF s’est rendu comte
Localités
Andrakengy
Andasipiro
Ambodivoara Ambodimandresy
qu’avec l’isolement de chaque localité,
Période
20 Novembre 6 Décembre 19 Novembre 5 Décembre les réponses instantanées et directes
d’observation 3 Décembre 2006 17 Décembre 2006 3 Décembre 2006 17 Décembre 2006
des membres aux intéressés via le site
Coordonnées S 14° 18’ 53.4’’
S 14° 12’ 10.0’’
S 14° 32’ 05.0’’
S 14° 32’ 05.0’’
web sont très limités et précaires. En
géographiques E 049< 16’ 38.3’’ E 049< 22’ 34.8’’
E 049< 26’ 42.1’’ E 049< 30’ 21.1’’
effet, pour se connecter, les élèves doivent aller à Andapa; et même si cerLes suivis et contrôles effectués par les paysans ont quand
tains élèves d’Andapa sont concernés, le reflexe avec cette
même permis de localiser des sites d’observations de l’eshaute technologie nécessite encore un encadrement rappèce Propithecus candidus (Simpona). Patel, en échangeant les
proché pour être efficace.
Pour mieux unir les efforts,une Union Régionale des Associdonnées avec l’équipe des projets du WWF a publié en 2009
ations de gestion des forêts, appelée aussi "Gestion Unie du
que l’espèce Propithecus candidus est aussi rencontrée dans le
Corridor de Betaolana" a aussi été créé. Malgré les efforts
Corridor de Betaolana et de Tsaratanana-Betaolana. Quelinvestis pour créer cette Union, elle est restée au stade de
ques caractéristiques des localités où les inventaires ont été
constitution (dépôt de dossier) au moment où les phases des
effectués et où cette espèce a été observée sont synthétideux projets sont terminées. Toutefois, elle est engagée et
sées dans le tableau 1.
sera reprise dans les autres projets du WWF dans cette
localité. Il est donc souligné ici l’importance des encadreLes alternatives aux pressions et menaces
ments par des organismes promoteurs dans le long terme ou
Les pressions sont définies comme étant les activités causant
du moins à moyen terme pour obtenir de meilleurs impacts
des impacts négatifs aussi bien sur les forêts que sur les
dans les phases du projet.
lémuriens. Ces activités peuvent être légales ou illégales. Par
Les parties prenantes définies dans ce document
contre, les menaces sont des activités pouvant apparaître
sont composées par les partenaires techniques et les autres
dans le futur et pouvant avoir des impacts négatifs sur les
organismes et/ou associations travaillant dans les domaines
cibles (dans le cadre de ce projet les cibles sont les lémuriens
de l’environnement, les communautés de base, les organes
et leur habitat).
de décentralisation et de déconcentration de l’Etat (les
Les analyses,effectuées dans le cadre de ces deux projets ont
régions, les communes, les districts et les Fokontany).
montré que les pressions et les menaces sur les cibles sont
principalement constituées de: la déforestation causée esConclusions
sentiellement par les cultures sur brûlis, la dégradation des
La capitalisation des deux projets du WWF dans le Nord a
forêts engendrée par les prélvements diverses (bois de conpermis de comprendre les efforts encore à fournir dans le
struction ou autre matériels pour la construction tels que les
cadre de la conservation des lémuriens et de leur habitat.Les
lianes et les bambous, cueillette de miel), la chasse moderne
deux projets conduits dans la région de SAVA sont compléet le piège traditionnel. La déforestation tue à la fois les
mentaires, ceci a permis une uniformisation des approches
lémuriens et détruit leur habitat. Il en est de même des
techniques et scientifiques. Les deux projets ont enrichis les
pièges traditionnels mais à un degré moindre.
données sur la diversité de la zone en flore et en faune.Ils ont
Pour arrêter les pressions sur les forêts, les deux projets du
pu se réaliser de manière participative. En effet, ils ont été
WWF ont donc analysé les activités pouvant remplacer
très bien accueillis par les populations locales du fait que ces
celles formant une pression et constituant une menace dans
projets étaient majoritairement axés sur les activités de
le futur. En bref les activités développées sont: l’amélioration
développement pour atteindre leurs objectifs de conserde l’exploitation de l’espace par l’agroforesterie; la promovation.
tion des cultures maraichères, l’amélioration des cultures de
En conclusion, les défis à lancer doivent se concentrer sur
riz sur les bas fonds étroits par les Systèmes de Riziculture
deux aspects.
Améliorés (SRA),la promotion des briques pour la construcAspect technique: des études plus poussées sur la flore et la
tion des maisons et le reboisement des espèces à croissance
faune sont à conduire. En effet, les découvertes à faire sont
rapide; l’apiculture, la pisciculture et l’amélioration de l’éleencore immenses vu l’étendue du massif forestier.
vage des volailles.
Aspect développement: des activités sont engagées et n’en
sont qu’au début de leur mise en œuvre. Il serait nécessaire
Elaboration d’une stratégie régionale pour la conservation des
dans le futur de faire des évaluations de ces projets en
lémuriens
termes d’impact sur la conservation des habitats et des
Les principales cibles de conservations des deux projets sont
lémuriens ainsi que sur l’amélioration des conditions de vie
la forêt humide et les lémuriens. A part les transferts de
de la population locale.
gestion,les deux projets ont aussi été conduits pour éduquer,
Ces deux projets ne sont pas des projets de recherches.
informer et sensibiliser les populations locales (partant des
Toutefois, ils ont pu être enrichis par les interventions des
élèves dans les écoles primaires aux écoles secondaires mais
scientifiques consultants d’une part et des équipes du WWF
aussi l’ensemble des populations concernées dans les comd’autre part.
munes).
Pour la sauvegarde des lémuriens, les engagements des parRemerciements
ties prenantes sont recherchés à travers l’élaboration et la
Nos vifs remerciements s’adressent aux bailleurs qui ont
mise en œuvre d’une stratégie régionale pour la conservafinancés les projets du WWF Madagascar dans la région de
tion des lémuriens. Dans cette stratégie, les activités de
SAVA. Ils ont permis de conduire à la fois des études scienchaque partie sont définies de manière à minimiser les
tifiques et des activités de développement.Ces bailleurs sont:
dépenses monétaires afin de les rendre réalisables.
WWF Allemagne, WWF Suède et la Conservation InterPour une meilleure intégration ou engagement de chaque
nationale. Bien qu’à faible volume en terme de fonds, nous
entité, une Association des Amis des lémuriens a été créée.
tenons aussi à remercier le WWF Danemark pour des fonds
Cette association est mise en réseau via un site web aux
spécifiquement alloués à l’élaboration des support de comamoureux des lémuriens dans le monde. La vision a été
Table 1: Caractéristiques des localités d’observation des lémuriens.
Page 59
Lemur News Vol. 15, 2010
munication (poster, teeshirt, banderoles etc.) pour une meilleure compréhension des aspects de la conservation auprès
des paysans en particulier et des parties prenantes en
général.
Bibliographie
Erdmann, T.K.; Rambeloarisoa, G.; Ratsifandrihamanana, N.;
Ranaivomanantsoa,A.F.;Abraham,A.;Powell, G.;Allnutt, T.
2005. Vision sur la Biodiversité de l’Ecorégion de la forêt
Humide de Madagascar. Rapport interne pour le WWFInternational et le WWF Madagascar and West Indian
Ocean Programme Office.
Patel, E.R.2009.Silky Sifaka,Propithecus candidus,1871.In: R.A.
Mittermeier, J. Wallis, A.B. Rylands, J.U. Ganzhorn, J.F.
Oates, E.A. Williamson, E. Palacios, E.W. Heymann, M.C.M.
Kierulff, Y. Long, J. Supriatna, C. Roos, S. Walker, L. CortésOrtiz, C. Schwitzer (eds.). Primates in Peril: The World’s
25 Most Endangered Primates 2008-2010. IUCN/ SSC
Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation International (CI),
Arlington, VA. 84pp.
Garreau, J.M.; Manantsara, A. 2003. The protected-area complex of the Parc National de Marojejy and the Reserve
Speciale d’Anjanaharibe-Sud. Pp. 1451-1458. In: S.M.
Goodman, J.P. Benstead (eds.). The Natural History of
Madagascar. University of Chicago Press, Chicago, USA.
Goodman, S.M.; Raherilalao, M.J.; Rakotomalala, D.; Raselimanana,A.;Schütz,H.;Soarimalala,V.2003.Les Lémuriens.Pp.
279-286.In:S.M.Goodman,L.Wilmé (eds.). Nouveaux résultats d’inventaires biologiques faisant référence à l’altitude dans la région des massifs montagneux de Marojejy
et d’Anjanaharibe-Sud. Recherches pour le Développement, série sciences biologiques no. 19. Centre d’Information et de Documentation Scientifique et Technique,
Antananarivo, Madagascar.
Mittermeier, R.A.; Tattersall, I.; Konstant, W.R.; Meyer, D.;
Mast, R. 1994. Lemurs of Madagascar. Conservation International, Washington, D.C., USA.
Mittermeier, R.A.; Valladares-Padua, C.; Rylands, A.B.; Eudey,
A.A.; Butynski, T.M.; Ganzhorn, J.U.; Kormos, R.; Aiguiar, J.
M.; Walker, S. 2005. The World’s 25 Most Endangered
Primates 2004-2005. Lemur News 10: 3-6.
Petter, J.J.; Charles-Dominique, P. 1979. Vocal communication
in prosimians. Pp. 247-305. In: G.A. Doyle and R.D. Martin
(eds.).The Study of Prosimian Behavior.Academic Press.
Rajaoson,A.;Rakotonirina,L.H.2007.Rapport pour le WWF;
Inventaire des lémuriens et des forêts dans le Corridor de
Betaolana et le Corridor Tsaratanana-Marojejy. 89p.
Tattersall, I. 1982. The Primates of Madagascar. Columbia
University Press, New York, USA.
Genetic diversity in ten Indri (Indri indri)
populations compared to other lemur
species
John Zaonarivelo1, Rick Brenneman2*, Rambinintsoa
Andriantompohavana3, Edward E. Louis, Jr.2,3
1University of North Madagascar, Antsiranana, Madagascar
2Center for Conservation and Research, Omaha’s Henry
Doorly Zoo,3701 South 10th Street,Omaha,NE 68107,USA
3Madagascar Biodiversity Partnership, Antananarivo, 101
Madagascar.
*Corresponding author: rabr@omahazoo.com
Genetic diversity is considered by most to be the key to long
term survival and the maintenance of the evolutionary trajectory of a species. Genetic variation at loci under selection
gives the species as a whole the mechanisms with which to
respond or adapt to environmental changes.Lemurs in general are poorly studied with respect to establishing baseline
parameter estimates for genetic diversity.Only limited popu-
lation genetics studies exist on the genera Propithecus, Avahi,
Varecia, Eulemur, Microcebus, and Mirza (Tab. 1). To date, the
genus Indri is depauperate of population genetic data that
would help better understand the genetic diversity harbored
in its populations.
Tab.1:Lemur studies using multilocus microsatellite suites to
estimate genetic diversity as observed (HO) and expected
(HE) heterozygosity levels.
Species
Popu- Sam- Loci HO
lations ples
HE Reference
Zaonarivelo
0.654 0.766 et al., 2007b
Indri indri
2
20
20
Propithecus
deckeni
P. deckeni
2
20
14* 0.790 0.851 Lei et al., 2008a
1
10
P. coquereli
1
25
P. candidus
P. coronatus
2
1
18
10
P. diadema
2
20
P. edwardsi
2
20
P. verreauxi
3
30
P. tattersalli
2
20
P. tattersalli
**3
75
P. tattersalli
9
224
Avahi laniger
5
37
A. occidentalis
Varecia
rubra
V. variegata
variegata
Eulemur
cinereiceps
1
7
2
32
18* 0.776 0.776 Lei et al., 2008b
Rakotoarisoa
20 0.635 0.771 et al., 2006a
17* 0.648 0.614 McGuire et al., 2009
18* 0.771 0.774 Lei et al., 2008b
Ramarokoto
13* 0.818 0.814 et al., 2008
12* 0.681 0.618 Bailey et al., 2009
Rakotoarisoa
13 0.670 0.712 et al., 2006b
Razafindrakoto
16* 0.673 0.683 et al., 2008
Quéméré et al.,
13 0.699 0.682 2009
Quéméré et al.,
13 0.690 0.660 2010
Andriantompoha22 0.640 0.838 vana et al., 2004
Andriantompoha22 0.514 0.586 vana et al., 2004
Razakamaharavo
15 0.616 0.618 et al., 2010
4
35
25
0.337 0.506 Louis et al., 2005
Tokiniaina et al.,
16* 0.598 0.641 2009
Ranaivoarisoa
E. collaris
4
40 10* 0.617 0.576 et al., 2010
Ramanamahefa
E. sanfordi
5
54 11* 0.562 0.567 et al., 2010a
Ramanamahefa
E. coronatus
6
80 11* 0.636 0.673 et al., 2010b
E. rubriAndriantompoha2
12
20 0.531 0.643 vana et al., 2007
venter
Zaonarivelo et al.,
Lemur catta
1
24
7* 0.837 0.838 2006
Microcebus
Olivieri et al.,
8
205
7 0.615 0.605 2007
ravelobensis
M. raveloRadespiel et al.,
12
187
8 0.708 0.734 2008
bensis
M. bongoOlivieri et al.,
3
45
8 0.557 0.565 2008
lensis
M. danfossi
7
78
8 0.628 0.662 Olivieri et al., 2008
Mirza
Markolf et al.,
***1
69
7
0.712 0.799 2008
coquereli
* Heterozygosity averages calculated using loci with null allele
frequency estimates less than 0.10.
** Estimated over genetic clusters, not actual populations
*** Samples taken from 1993-2006.
2
21
The Indri (Indri indri, Gmelin, 1788), or Babakoto as it is
known in most of eastern Madagascar,is the largest extant lemur (Powzyk and Thalmann, 2003). Indri are primarily midlevel forest folivores preferentially feeding on immature
leaves and somewhat also on mature leaf matter, flowers,
fruits,seeds and even bark when necessary (Britt et al.,2002).
The Babakoto is currently threatened by the rapid reduction
Page 60
of forest cover and fragmentation of suitable habitat (Harper
et al., 2007) which limits the species’ density and range
(Glessner and Britt, 2005). Although protected, the Babakoto is also threatened by subsistence hunting pressure and
bush meat trade (Golden, 2005). Designated as Endangered
according to the IUCN Red List of Threatened Species
(IUCN, 2008), I. indri is currently split into two subspecies,
Indri indri indri (Gmelin, 1788) and Indri i. variegatus (Gray,
1872). Here, we present population genetic parameter estimates from populations along the entire range of the species
analyzed from nuclear microsatellite multilocus genotypes.
Methods
Samples were collected from 106 Indri from 10 sites across
the geographical range of the species (Fig. 1). From north to
south,the forests represented in the collection were Anjanaharibe-Sud Special Reserve, Marotandrano Special Reserve,
Ambatovaky Special Reserve,Zahamena Special Reserve and
National Park, Betampona Nature Reserve, Anjozorobe
Regional Forest Reserve, Mantadia National Park, Analamazoatra Special Reserve (Andasibe),Maromizaha Classified
Forest, and Anosibe an’ala Classified Forest. The elevations
of the sampling sites ranged from lowland forests (Anosibe
An’ala, 125 m asl) to highland forests (Anjozorobe, 1358 m
asl).
Fig. 1: Map of Madagascar indicating the study areas.
Immobilization and collection
All lemurs investigated in this study were free-ranging and
were immobilized with a CO2 powered DAN-INJECT (Brrkop, Denmark) Model JM rifle propelling Pneu-Darts (Williamsport, PA) loaded with 10 mg/kg estimated body weight
of Telazol® (Fort Dodge).We recorded the location (within 6
m accuracy) of all of the immobilized lemurs using a global
positioning system (GPS) device. Each individual was transported back to the base camp where complete morphometric data were taken (Zaonarivelo et al., 2007a). Whole
Lemur News Vol. 15, 2010
blood (1.0 cc per kilogram) from the femoral artery and
2.0 mm skin biopsies from the ear pinnae were collected
from each sedated lemur (Junge and Louis, 2002). A Home
Again® (Home Again Pet Recovery Service, East Syracuse,
NY) microchip was placed subcutaneously between the scapulae of each lemur to positively identify individuals re-captured during any future immobilizations. Following data and
sample collection, an injection of lactated Ringer’s solution
was administered subcutaneously to support maintenance
requirements and to dissipate the effect of the Telazol®. Animals were monitored for three hours post recovery then
released according to the capture GPS coordinates.
Data generation
Ear punches were dissected into quarters and DNA was
extracted using standard PCI/Chloroform procedures (Sambrook et al., 1989). Approximately 50 ng of genomic DNA
was used for each PCR reaction. Multilocus genotypes were
generated from a suite of 20 Indri-specific microsatellite loci
as described in Zaonarivelo et al. (2007b). The genotype file
was checked for typographical errors, scoring errors, stutter
bands and allele dropout with Micro-Checker (van Oosterhout et al., 2004) and Microsatellite Analyser (MSA; Dieringer and Schlötterer, 2002). We used CERVUS (version 2.0,
Marshall et al., 1998;Slate et al., 2000) to identify loci with excessive null allele frequency estimates (nf > 0.10) and to estimate polymorphic information content of the loci.Moderate
(0.05 < nf < 0.20) and high (0.20 < nf) null allele frequencies
can have significant effects on population genetics parameter
estimates (Chapuis and Estoup, 2007). The process of redesigning primer pairs is both costly and time consuming;
therefore,we opted to delete problematic loci from the data
set. We deleted eight loci with moderate null allele frequencies (nf > 0.1) to reduce the bias from misclassification of null
heterozygotes as homozygotes (Callen et al., 1993; Hoffman
and Amos, 2005) and to control the variance of parameter
estimates (Chapuis and Estoup, 2007). The accepted loci
were verified for independence of linkage disequilibrium
(with Bonferroni-adjusted P-values) in FSTAT (Goudet,1995,
2001).
Hardy-Weinberg exact tests (Guo and Thompson, 1992)
were performed by locus and population in Genepop (version 4.0, Raymond and Rousset, 1995). Initially, we used the
default settings for the MCMC estimation of HWE then
increased the batch size from 100 to 250 to reduce the standard error of the P-value to below 0.01. Genetic diversity
was measured as observed heterozygosity (HO) and expected heterozygosity (HE). In addition, the number of effective
migrants was estimated globally and pair-wise using the private allele method. We used FSTAT to calculate the total
number of alleles (k), mean number of alleles (MNA), and
rarefacted allelic richness (AR; Leberg, 2002) by locus and
population. Allelic richness estimates the allelic diversity in a
data set based on the population with the fewest number of
individuals contributing genotypes by locus. This is an unbiased comparison of allelic diversity since populations with
more contributors provide a greater opportunity to capture
more alleles from lower frequency occurrences. Wright’s Fstatistics were estimated in FSTAT for within population
similarity (FIS) and between population differences (FST)
according to Weir and Cockerham (1984).
The effective population sizes were estimated with the linkage disequilibrium (LD) option in NeEstimator (Peel et al.,
2004; Hill, 1981; Waples, 1991). We tested all populations
having met the minimum statistical threshold required (n =
20 genes or 10 individuals) for the presence of bottleneck
events using Bottleneck (version 2.0, Cornuet and Luikart,
Page 61
Lemur News Vol. 15, 2010
55DD
.90
.80
Y
1996; Luikart et al., 1998; Piry et al., 1999) under the Infinite
Alleles Model (IAM; Kimura and Crow, 1964), the Stepwise
Mutation Model (SMM;Ohta and Kimura,1973),and the Two
Phase Model (TPM;di Rienzo et al.,1995).We varied the proportion of the single step contribution to the TPM to identify
the P < 0.05 threshold of significance. The program identifies
populations with an excess of heterozygosity relative to
mutation-drift equilibrium which is indicative of a reduction
in the effective population size (Maruyama and Fuerst,1985).
An estimate of relationships among all individuals sampled at
each forest was done in SPAGeDi (Hardy and Vekemans,
2002),then compared to a simulation of known pedigreed individuals. The analysis was performed to calculate the relationship coefficients described in Queller and Goodnight
(1989) in the absence of spatial data.
.70
.60
Y
A B C D E F G H I
J
Results
X
Genetic diversity as mean number of alleles ranged from
Fig. 2: Ranges of expected heterozygosities with 95 % confi6.08-8.92 per population. Using the rarefacted allelic richdence intervals: A) Anjanaharibe Sud; B) Marotandrano; C)
ness, the range lowered to 5.87-7.67. The expected heteroAmbatovaky; D) Zahamena; E) Betampona; F) Anjozorobe;
zygosity ranged from 0.77-0.86 (P > 0.05;Fig.2) with an averG) Mantadia;H) Andasibe;I) Maromizaha; J) Anosibe an’ala.
age of 0.81, while the observed heterozygosity ranged from
4DF4
0.65-0.84 (P < 0.05; Fig. 3) with an average of 0.74. The number of effective breeders in the sampled populations averaged between 12.6 and 39.6 per population (Tab. 2).
.90
Results from Bottleneck showed that none of the 10 populations deviated from a mutation-drift equilibrium under the
SMM.Three populations, Anjanaharibe Sud,Ambatovaky and
.85
Anjozorobe did not show evidence of population bottleneck
under the IAM either.The rest of the populations were significant for bottleneck events under the IAM and varying pro.80
portions of single step contributions under the TPM.
The frequencies of the relationship coefficients estimated
using SPAGeDi were overlaid upon a simulation generated
.75
from known pedigreed data so that each of the population’s
relative distribution of relationships could be compared with
parent offspring, full sibling, half sibling and unrelated relationship coefficient distributions (Fig. 4). The data indicated
A B C D E F G H I
J
that the sampling was from individuals that were somewhat
X
related more than the unrelated individuals in the reference
Fig. 3: Ranges of observed heterozygosities with 95 % confisimulation. Inbreeding can also be due to background relatdence intervals: A) Anjanaharibe Sud; B) Marotandrano; C)
edness where an increased allelic identity by descent is a reAmbatovaky; D) Zahamena; E) Betampona; F) Anjozorobe;
sult from bottleneck events in the population’s history. RelaG) Mantadia;H) Andasibe;I) Maromizaha; J) Anosibe an’ala.
tionship coefficient distributions support the assumption that the individ- Tab. 2: Population genetic parameter estimates for 10 populations comprised of n
uals sampled were often from family samples each derived from 12 microsatellite loci for number of alleles (k), the mean
groups. All of these sources may po- number of alleles (MNA), allelic richness (AR), probability of satisfying Hardy-Weintentially be due to the effects of habi- berg Equilibrium (HWE), observed (HO) and expected (HE) heterozygosities, intat fragmentation which is certainly breeding estimate (FIS), the number of effective breeders (Neb) estimated with the
the case in the Anosibe an’ala popula- linkage disequilibrium method and 95 % confidence interval,and results from the Bottion where the habitat is so frag- tleneck test under the infinite allele model (IAM) and the two phased model (TPM)
mented that although multiple family with proportion of multistep mutations contributing to the P < 0.05 significance level.
groups were encountered, they were
found in isolated forest fragments.
n
k MNA AR HWE HO HE
FIS Neb 95% CI IAM TPM
Discussion
Of the 10 Indri populations sampled,
six (Anjanaharibe Sud, Ambatovaky,
Zahamena, Betampona, Mantadia, and
Anosibe an’ala) deviated from HWE
with an excess of homozygotes. Considering inbreeding as potential cause,
five of the populations (Anjanaharibe
Sud, Ambatovaky, Betampona, Mantadia, and Andasibe) had relatively
high FIS and one (Anosibe an’ala) had
ANJ
10 80 6.67 6.41
*
0.67 0.77 0.135 23.0 16.2-37.8 NS
NS
TAND
10 73 6.08 5.87 NS 0.75 0.77 0.024 21.9 15.1-36.9 **
70
VAK
11 76 6.33 5.92 NS 0.69 0.77 0.121 20.1 14.7-30.4 NS
NS
ZAH
14 107 8.92 7.65 NS 0.81 0.86 0.060 39.6 28.8-61.3 **
10
BET
10 79 6.58 6.37
**
0.73 0.80 0.093 18.3 13.5-27.1 **
20
ANJZ
10 83 6.92 6.70 NS 0.84 0.79 -0.066 20.9 15.1-32.5 NS
NS
TAD
10 96 8.00 7.67 NS 0.75 0.85 0.120 20.1 15.3-28.3 **
70
DASI
11 81 6.75 6.40 NS 0.73 0.81 0.095 12.6 10.2-16.2 **
5
MIZA
10 89 7.42 7.17 NS 0.83 0.84 0.021 15.9 12.4-21.3 **
5
ANOSIBE 10 92 7.67 7.38
*
0.65 0.85 *0.236 28.8 19.9-49.3 **
NS
* P < 0.05, ** P < 0.001; Anjanaharibe-Sud(ANJ), Marotandrano (TAND), Ambatovaky (VAK),
Zahamena (ZAH), Betampona (BET), Anjozorobe (ANJZ), Mantadia (TAD), Andasibe (DASI).
Maromizaha (MIZA), Anosibe an’ala (ANOSIBE).
Page 62
Lemur News Vol. 15, 2010
Anjanaharibe-Sud
0,4
Frequency
Frequency
0,4
0,3
0,2
0,1
0
-0,3
-0,1
0,1
0,3
0,5
Relationship Coefficients
0,7
0,1
0,9
-0,5
Morontandrano
-0,3
0,3
0,2
0,1
0
-0,3
0,4
-0,1
0,1
0,3
0,5
Relationship Coefficients
0,7
0,9
0,7
0,9
0,1
Frequency
0,1
-0,3
-0,1
0,1
0,3
0,5
Relationship Coefficients
Anosibe an'ala
0,4
0,2
0,3
0,2
0,1
0
-0,3
-0,1
0,1
0,3
0,5
Relationship Coefficients
0,7
0,9
-0,5
-0,3
Parent-Offspring
0,4
Frequency
0,7
0,2
-0,5
Ambatovaky
0,3
-0,5
Zahamena
Unrelated
0,3
-0,1
0,1
0,3
0,5
Relationship Coefficients
Full Sibling
Half Sibling
All Populations
Fig. 4: Distributions of relationship coefficients estimated in
each population overlaid on a simulation of 10,000 known
genotypes and pedigreed relationships (Queller and Goodnight, 1989).
0,2
0,1
0
-0,5
-0,3
-0,1
0,1
0,3
0,5
Relationship Coefficients
0,7
0,9
Betampona
0,4
Frequency
0,9
0,3
0,9
0
0,3
0,2
0,1
0
-0,5
-0,3
0,4
Frequency
0,7
0
-0,5
-0,1
0,1
0,3
0,5
Relationship Coefficients
0,7
0,9
0,7
0,9
0,7
0,9
Anjozorobe
0,3
0,2
0,1
0
-0,5
0,4
Frequency
-0,1
0,1
0,3
0,5
Relationship Coefficients
Maromizaha
0,4
Frequency
0,4
Frequency
0,2
0
-0,5
Frequency
Andasibe
0,3
-0,3
-0,1
0,1
0,3
0,5
Relationship Coefficients
Mantadia
0,3
0,2
0,1
0
-0,5
-0,3
-0,1
0,1
0,3
0,5
Relationship Coefficients
a significantly high FIS estimate. Considering relationship
among the samples as one manner of capturing inbreeding,all
populations show some degree of relationship above what
would be expected if the sampled individuals were unrelated.
This is not surprising since samples were collected as found
and this could include individuals that are members of a family group which is supported by the relationship coefficient
distributions in Fig. 2.
All populations demonstrated some degree of recent reduction in the effective population sizes.The bottlenecks did not
appear to have been a single global event as different populations showed differing degrees to which the bottlenecks
were detected. Using Lawler’s (2008) 4*Neb*generations,
the bottlenecks detected would have had an expected window of occurrence of up to 250 to 800 years ago, within the
timeframe of human encroachment. Hence, we postulate
that among other things, anthropogenic disturbances,
whether habitat destruction or subsistence hunting, may
have influenced the demographic reduction that we detected
in the bottleneck test. These baseline values could be useful
in long-term or future studies to determine genetic health
trends over time under various forest or habitat conditions.
Genetic diversity is considered to be the most important
factor in determining the genetic health of a species or population.Among the lemurs,there is little information in the literature that addresses the genetic diversity estimations for
multiple populations of a given species. Ranaivoarisoa et al.
(2010) found the observed heterozygosity in three of four
Eulemur collaris populations to be higher than the expected
heterozygosity. In E. coronatus, Ramanamahefa et al. (2010a)
Page 63
Lemur News Vol. 15, 2010
found the expected heterozygosity to be higher in five out of
six populations, one comparison was significantly higher (P <
0.01). In E. sanfordi, Ramanamahefa et al. (2010b) found that in
all populations sampled, the observed heterozygosities were
higher than the expected heterozygosities. Lastly, Quéméré
et al. (2009), found that their study estimated the expected
heterozygosity level for several populations of P. tattersalli to
be higher than the estimate found by Razafindrakoto et al.
(2008) using a different marker suite in different populations.
Other studies (included in Tab. 2) have estimated heterozygosity levels for one or two populations of various lemur
species in recent years. While these estimates provide some
general sense of genetic diversity, they are not standardized
(e.g. not the same markers were used in each study) so the
estimates are contingent on the polymorphic information
content and amplification quality in each independent study.
What we do see is a relative trend that the observed
heterozygosities are in general lower, but usually not significantly, than the expected heterozygosities under the assumptions of HWE.
In this study on I. indri, we found the differences among the
HO estimates to differ but not significantly and the differences among the HE estimates to differ with low significance
(P < 0.05). The average estimates for heterozygosity, thus
genetic diversity, were in the upper range of those found in
limited population studies on other lemur species. These
estimate trends provide the basis for future and integrative
studies where multiple species might be considered in sympatric zones to investigate the overall genetic health of the
biodiversity and to better understand the effects that humans may be having on the evolutionary potential of lemurs.
Acknowledgements
We acknowledge the Ministry of Environment and Eaux &
Forets, Madagascar National Parks, U.S. Fish & Wildlife Service, Professor Gisele and the Department of Paleontology
and Anthropology, University of Antananarivo for their help.
This project would not have been possible without the support of the staff, guides, and drivers of Henry Doorly Zoo
and the Madagascar Biodiversity Partnership. We also wish
to thank the Theodore F.and Claire M.Hubbard Family Foundation, Bill and Berniece Grewcock, the Ahmanson Foundation, the James Family Foundation and the Hawks Family
Foundation for their support of this project.
References
Andriantompohavana, R.; Randrianamanana, J.C.; Sommer,
J.A.; Brenneman, R.A.; Louis, E.E. Jr. 2004. Characterization
of twenty-two microsatellite loci developed from the
genome of the Woolly Lemur (Avahi laniger). Mol. Ecol.
Notes 4(3): 400-403.
Andriantompohavana, R.; Morelli, T.L.; Behncke, S.M.; Engberg, S.E.; Brenneman, R.A.; Louis, E.E. Jr. 2007. Characterization of twenty Eulemur-specific microsatellite loci characterized in two populations of the Red-Bellied Brown
Lemur, Eulemur rubriventer. Mol. Ecol. Notes 7(6): 11621165.
Bailey, C.A.; Lei, R.; Brenneman, R.A.; Louis, E.E. Jr. 2009. Characterization of 21 microsatellite loci in the Milne-Edwards sifaka (Propithecus edwardsi). Conserv. Genet. 10:
1389-1392.
Britt,A.;Randriamandratonirina,N.J.;Glasscock,K.D.;Iambana, B.R. 2002. Diet and feeding behaviour of Indri indri in a
low-altitude rain forest. Folia Primatol. 73: 225-39.
Callen, D.F.; Thompson, A.D.; Shen, Y.; Phillips, H.A.; Richards,
R.I.; Mulley, J.C.; Sutherland, G.R. 1993. Incidence and
origin of "null" alleles in the (AC)n microsatellite markers.
Am. J. Hum. Genet. 52: 922-927.
Chapuis, M.-P.; Estoup, A. 2007. Microsatellite null alleles and
estimation of population differentiation. Mol. Biol. Evol.
24(3): 621-631.
Cornuet, J.M.;Luikart,G.1996.Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 20012014.
Di Rienzo,A.;Peterson, A.C.;Garza,J.C.;Valdes, A.M.;Slatkin,
M.; Freimer, N.B. 1994. Mutational processes of simplesequence repeat loci in human populations. Proc. Nat.
Acad. Sci. USA. 91: 3166-3170.
Dieringer, D.; Schlötterer, C. 2002. Microsatellite analyser
(MSA): a platform independent analysis tool for large
microsatellite data sets. Mol. Ecol. Notes 1(3): 167-169.
Glessner, K.D.G.; Britt, A.2005. Population density and home
range size of Indri indri in a protected low altitude rain
forest. Int. J. Primatol. 26(4): 855-872.
Gmelin, J.F. 1788. Caroli a Linné systema naturae per regna
tria naturae, secundum classes, ordines, genera, species,
cum characteribus, differentiis, synonymis, locis. Tomus I.
Editio decima tertia,aucta,reformata.42:1-500.Lipsiae,G.
E. Beer.
Golden, C. 2005. Eaten to Endangerment: Mammal hunting
and the bushmeat trade in Madagascar’s Makira forest.
M.S. Thesis: Accession 17105 Box 1, Harvard University
Library, Cambridge, MA.
Goudet, J. 1995. FSTAT, a computer program to test F-statistics. J. Hered. 86: 485-486.
Goudet, J. 2001. FSTAT, a program to estimate and test gene
diversities and fixation indices (version 2.9.3). Updated
from Goudet (1995).
Guo,S.W.;Thompson,E.A.1992.Performing the exact test of
Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361-372.
Gray, J.E. 1872. On the varieties of Indris and Propithecus.
Annals and Magazine of Natural History, London, British
Museum Trustees.
Hardy, O.J.; Vekemans, X. 2002. SPAGeDi: a versatile computer program to analyse spatial and genetic structure at the
individual level. Mol. Ecol. Notes 2: 618-620.
Harper, G.J.; Steininger, M.K.; Tucker C.J.; Juhn, D.; Hawkins, F.
2007. Fifty years of deforestation and forest fragmentation in Madagascar. Environ. Conserv. 34(4): 1-9.
Hill, W.G. 1981. Estimation of effective population size from
data on linkage disequilibrium. Genet. Res. 38: 209-216.
Hoffman, J.J.; Amos, W. 2005. Microsatellite genotyping
errors: detection approaches, common sources, and consequences for paternal exclusion. Mol. Ecol. 14: 599-612.
IUCN. 2008. IUCN Red List of threatened species.
www.iucnredlist.org. Downloaded on 17 April 2009.
Junge,R.E.;Louis,E.E.2002.Medical evaluation of free-ranging
primates in Betampona Reserve, Madagascar. Lemur
News 7:23-25.
Kimura,M.;Crow J.F. The number of alleles that can be maintained in a finite population. Genetics 49: 725-738.
Lawler, R. 2008. Testing for a historical bottleneck in wild
Verreaux’s sifaka (Propithecus verreauxi verreauxi) using
microsatellite data. Am. J. Primatol. 70: 990-994.
Leberg, P.L. 2002. Estimating allelic richness: Effects of ample
size and bottlenecks. Mol. Ecol. 11: 2445-2449.
Lei, R.; McGuire, S.M.; Shore, G.D.; Louis, E.E. Jr.; Brenneman,
R.A. 2008a. Characterization of twenty-one microsatellites developed from Propithecus deckeni deckeni. Mol. Ecol.
Res. 8(4): 773-776.
Lei, R.; McGuire, S.M.; Shore, G.D.; Louis, E.E. Jr.; Brenneman,
R.A. 2008b. Characterization of twenty microsatellites
developed from Propithecus deckeni coronatus with crossamplification in Propithecus deckeni deckeni. Conserv.
Genet. 9(4): 999-1002.
Louis, E.E. Jr.; Ratsimbazafy, J.H.; Razakamaharavo, V.R.; Pierson, D.J.; Barber, R.C.; Brenneman, R.A. 2005. Conservation genetics of black and white ruffed lemurs (Varecia variegata variegata) from southeastern Madagascar. Animal
Conservation 8: 105-111.
Luikart, G.; Allendorf, F.W.; Cornuet, J.-M.; Sherwin, W.B.
1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J. Hered. 89:
238-247.
Markolf, M.; Roos, C.; Kappeler, P. 2008. Genetic and demographic consequences of a rapid reduction in population
size in a solitary lemur (Mirza coquereli). Open Conserv.
Biol. J. 2: 21-29.
1964.
Page 64
Marshall, T.C.; Slate, J.; Kruuk, L.E.B.; Pemberton, J.M. 1998.
Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7(5): 639-655.
Maruyama, T.; Fuerst, P.A. 1985. Population bottlenecks and
non equilibrium models in population genetics.II.Number
of alleles in a small population that was formed by a recent
bottleneck. Genetics 111: 675-689.
McGuire, S.M.; Emodi, G.P.; Shore, G.D.; Brenneman, R.A.;
Louis, E.E. Jr. 2009. Characterization of 21 microsatellite
marker loci in the silky sifaka (Propithecus candidas). Conserv. Genet. 10(4): 985-988.
Ohta, T.; Kimura, M. 1973. Simulation studies on genetic electrophoretically genetic variability in a finite population.
Genetics 76: 615-624.
Olivieri,G.;Zimmermann,E.;Randrianambinina,B.;Rasoloharijaona, S.; Rakotondravony, D.; Guschanski, K.; Radespiel,
U. 2007. The ever-increasing diversity in mouse lemurs:
three new species in north and northwestern Madagascar.
Mol. Phylogenet. Evol. 43(1): 309-27.
Olivieri, G.I.; Sousa, V.; Chikhi, L.; Radespiel, U. 2008. From
genetic diversity and structure to conservation: genetic
signature of recent population declines in three mouse
lemur species (Microcebus spp.). Biol. Conserv. 141: 12571271.
Peel, D.; Ovenden, J.R.; Peel, S.L. 2004. NeEstimator: software
for estimating effective population size, Version 1.3.
Queensland Government, Department of Primary Industries and Fisheries.
Piry, S.; Luikart, G.; Cornuet, J.M. 1999. BOTTLENECK: A
computer program for detecting recent reductions in the
effective population size using allele frequency data. J.
Hered. 90: 502-503.
Powzyk, J.; Thalmann, U. 2003. Indri indri, Indri. Pp. 1342-1345.
In: S.M. Goodman; J.P. Benstead (eds.). The Natural History of Madagascar. University of Chicago Press.
Queller, D.C.; Goodnight, K.F. 1989. Estimating relatedness
using genetic markers. Evolution 43: 258-275.
Quéméré, E.;Louis,E.E.Jr.;Ribéron,L.;Chikhi,L.;Crouau-Roy,
B. 2009. Non-invasive conservation genetics of the critically endangered golden-crowned sifaka (Propithecus
tattersalli): high diversity and significant genetic differentiation over a small range. Conserv. Genet. DOI:
10.1007/s10592-009-9837-9.
Quéméré, E.; Crouau-Roy, B.; Rabarivola, C.; Louis, E.E. Jr.;
Chikhi, L. 2010. Landscape genetics of an endangered
lemur (Propithecus tattersalli) within its entire fragmented
range. Conserv. Genet.
DOI:10.1007/s10592-009-9837-9.
Radespiel, U.; Rakotondravony, R.; Chikhi, L. 2008. Natural
and anthropogenic determinants of genetic structure in
the largest remaining population of the endangered
golden-brown mouse lemur, Microcebus ravelobensis. Am. J.
Primatol. 70: 860-870.
Rakotoarisoa, G.; Shore, G.D.; McGuire, S.M.; Engberg, S.E.;
Louis, E.E. Jr.; Brenneman, R.A. 2006a. Characterization of
20 microsatellite marker loci in the Coquerel’s Sifaka (Propithecus coquereli). Mol. Ecol. Notes. 6(4): 1119-1121.
Rakotoarisoa, G.; Shore, G.D.; McGuire, S.M.; Engberg, S.E.;
Louis, E.E. Jr.; Brenneman, R.A. 2006b. Characterization of
13 microsatellite marker loci in the Verreaux’s Sifaka (Propithecus verreauxi). Mol. Ecol. Notes. 6(4): 1122-1125.
Ramanamahefa, R.; McGuire, S.M.; Louis, E.E. Jr.; Brenneman,
R.A. 2010a. Population genetic parameter estimates for
five populations of Sanford’s lemur, Eulemur sanfordi
(Archbold, 1932), from northern Madagascar. Lemur
News 14: 26-31.
Ramanamahefa, R.; McGuire, S.M.; Louis, E.E. Jr.; Brenneman,
R.A. 2010b. Population genetic parameter estimates for
six populations of crowned lemurs, Eulemur coronatus
(Gray, 1842), from northern Madagascar. Lemur News 14:
21-26.
Ramarokoto,R.;Lei,Runhua,R.;Vincent,J.;Day,S.;Shore,G.D.;
Brenneman, R.A.; Louis, E.E. Jr. 2008. Characterization of
twenty-one microsatellites developed from Propithecus
diadema. Conserv. Genet. 9(5): 1377-1380.
Ranaivoarisoa, J.-F.; McGuire, S.M.; Lei, R.; Ravelonjanahary,
S.S.;Engberg,S.E.;Bailey,C.;Kimmel,L.;Razafimananjato,T.;
Rakotonomenjanahary, R.; Brenneman, R.A.; Louis, E.E. Jr.
Lemur News Vol. 15, 2010
2010. Population genetic study of the Brown Collared
Lemur (Eulemur collaris) in Southeastern Madagascar.
Online Conserv. Biol. J. 4: 1-8.
Raymond,M.;Rousset,F.1995.GENEPOP (Version3.1):Population genetics software for exact tests and ecumenicism.
J. Hered. 86: 248-249.
Razafindrakoto A.; Quéméré, E.; Shore, G.D.; McGuire, S.M.;
Louis, E.E. Jr.; Brenneman, R.A. 2008. Characterization of
20 microsatellites marker loci in the golden-crowned
sifaka (Propithecus tattersalli). Conserv. Genet. 9(4): 10271031.
Razakamaharavo, V.; McGuire, S.M.; Louis, E.E. Jr.; Brenneman,
R.A. 2010. Genetic architecture of regional red ruffed
lemur (Varecia rubra) populations in Masoala National
Park of Madagascar. Primates 51(1): 53-61.
Sambrook,J.;Fritch,E.F.;Maniatus,T.1989.Molecular Cloning:
a Laboratory Manual. 2 edn. Cold Spring Harbor Press,
New York.
nd
Slate, J.; Marshall, T.C.; Pemberton, J.M. 2000. A retrospective
assessment of the accuracy of the paternity inference program CERVUS. Mol. Ecol. 9(6): 801-808.
Tokiniaina, H.; Bailey, C.A.; Shore, G.D.; Delmore, K.E.;
Johnson, S.E.; Louis, E.E. Jr.; Brenneman R.A. 2009. Characterization of 18 microsatellite marker loci in the whitecollared lemur (Eulemur cinereiceps). Conserv. Genet. 10:
1459- 1462.
Van Oosterhaut, C.; Hutchinson, W.F.; Wills, D.P.M.; Shipley, P.
2004. MICRO-CHECKER: software for identifying and
correcting genotyping errors in microsatellite data. Mol.
Ecol. Notes 4: 535-538.
Waples, R.S. 1991. Genetic methods for estimating the effective size of Cetacean populations.Pp.279-300.In:A.R.Hoelzel (ed.). Genetic Ecology of Whales and Dolphins, Special Issue 13.International Whaling Commission,London.
Weir, B.; Cockerham, C.C. 1984. Estimating F-statistics for
the analysis of population structure. Evolution 38(6):
1358-1370.
Zaonarivelo, J.R.; Andriantompohavana, R.; Engberg, S.E.; Kelley, S.G.; Randriamanana, J.-C.; Louis, E.E. Jr.; Brenneman,
R.A. 2007a. Morphometric data for Indri (Indri indri) collected from 10 forest fragments in eastern Madagascar.
Lemur News 12: 17-21.
Zaonarivelo, J.R.; Sommer, J.A.; McGuire, S.M.; Engberg, S.E.;
Brenneman,R.A.;Louis,E.E.Jr.2007b.Isolation and characterization of twenty microsatellite marker loci from the
Indri (Indri indri) genome. Mol. Ecol. Notes 7: 25-28.
Zaonarivelo, J.R.; Andriantompohavana, R.; Shore G.D.; Engberg, S.E.; McGuire, S.M.; Louis, E.E. Jr.; Brenneman, R.A.
2006. Characterization of 21 microsatellite marker loci in
the ring-tailed lemur (Lemur catta). Conserv. Genet. 8(5):
1209-1212.
Verreaux’s sifaka fur condition in the
spiny forest of southern Androy
Ivan Norscia1*, Jean Lambotsimihampy2, Elisabetta
Palagi1,3
1Natural History Museum, UniversitB di Pisa, Via Roma, 79,
56011, Calci (PI), Italy
2Berenty Village, Antandroy, Madagascar
3Unit of Cognitive Primatology and Primate Center, Institute
of Cognitive Sciences and Technologies, The National Research Council (CNR), Rome, Italy
*Corresponding author: norscia@hotmail.com
Résumé
Les conditions du pelage des animaux peuvent représenter
un moyen fiable et un indicateur non invasif pour comprendre l’état de santé d’une population et distinguer des segments différents de la même population. En 2008 nous avons
effectué un recensement de sifaka (Propithecus verreauxi)
dans les forêts riveraines de la réserve de Berenty (foret
galerie et de transition de Malaza et forêt secondaire aux
Lemur News Vol. 15, 2010
espèces allochtones de Ankoba) et dans six portions de
forêt épineuse qui sont inclues dans le domaine privé de
Berenty. Nous avons relevé l’état du pelage des animaux
selon trois conditions: fourrure intègre (niveau 1), fourrure
faiblement endommagée (ponctuée par des petites zones,
sans pelage, couvrant moins de 30 % du corps; niveau 2),
fourrure fortement endommagée (pelage manquant sur une
surface supérieure à 30 %; niveau 3). Nous avons aperçu seulement quatre sifaka au niveau de pelage 3 et, par conséquence, nous avons pu évaluer statistiquement les différences seulement entre les niveaux de pelage 1 et 2, en comparant forêt épineuse et les forêts riveraines, soi au niveau
des groups d’animaux (n= 41) soi au niveau des zones recensée (n= 9). Même si avons détecté un nombre significativement plus haut de sifaka avec la fourrure faiblement
endommagée dans le domaine épineuse, la nature et surtout
l’entité du dommage indiquent que les conditions du pelage
n’arrivent pas vraiment à différentier des segments distincts
dans la population de sifaka de Berenty.
Introduction
An index of coat condition can be a non-invasive tool for
tracking health and stress at the population level (Jolly,
2009a). In fact, pelage growth can be directly influenced by
the proximate stimulus of light (acting through neuro-endocrine pathways), by the nutritional status, and indirectly by
temperature and behavior (Ling, 1970). Two main functions
of fur are a) insulation, which allows conservation of body
heat, thus reducing energy expenditure and food requirements; and b) shielding, which protects day-active mammals
from excessive heat load from solar radiation (Scott et al.,
2001; Kenagy and Pearson, 2000).
Here, we considered coat condition of Propithecus verreauxi
(Verreaux’s sifaka) as a possible indicator of the "health status" of animals in different habitats and investigated whether
it could provide information on possible population stress in
the poorly investigated spiny forest of south Madagascar.
The dry spiny forest of southern Madagascar is a thorny environment,both metaphorically and literally speaking.Listed as
one of the 200 most important ecological regions in the
world, it harbors the highest level of plant endemism in Madagascar (Elmqvist et al., 2007). In spite of its importance, the
spiny forest is underrepresented in terms of protection and
conservation programs (Fenn, 2003; Ganzhorn et al., 2003;
Seddon et al., 2000). To fill, at least in part, this gap, we investigated sifaka fur condition in different spiny forest parcels
inside the Berenty Estate (Androy region,south Madagascar)
and compared it with sifaka inhabiting the riverine forest
areas inside the Berenty Reserve, a habitat much richer in
staple food for lemurs.
Methods
Study site, survey technique, and fur condition evaluation
In March-April 2008, a comprehensive sifaka survey was conducted in the Berenty Estate, covering 134 ha of spiny forest
and 60 ha of non-spiny forest areas. The Berenty Estate is located in the semi-arid Androy Region (rainfall averages less
than 500 mm per year). The spiny forest is usually 3 to 6 m in
height with dwarf and xerophyte plants,and emerging trees of
the Family Didieraceae that may reach more than 10 m in
height,such as the keystone species Allouadia procera (Elmqvist
et al., 2007). We performed the survey in all accessible spiny
forest parcels (sacred areas, used as a cemetery, cannot be
accessed by anyone except for local family clans) and in three
riverine areas of the Berenty Reserve (on the Mandrare river),
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comprising a northern section (occupied by the 40 ha secondary forest of Ankoba dominated by the exotic legume species
Pithecellobium dulce; S 24.99°; E 46.29°) and a southern section
(Malaza: S 25.01°; E 46,31°) (Fig. 1 shows study locations). Inside Malaza we considered the 7 ha gallery forest (dominated
by tamarinds;Tamarindus indica) and the front-transitional forest (13 ha) (Jolly et al., 2006). In all the areas considered in this
study,logging and hunting are prohibited,and the fossa (Cryptoprocta ferox) is absent.
Fig. 1: Study site location: Berenty reserve (solid outline; white
area:scrub;diagonal lines:Ankoba and Malaza riverine forests)
and spiny forest fragments (black areas): 1 = Spiny Malaza; 2 =
Spiny Reserve 1;3 = Spiny Reserve 2;4 = West Rapily;5 = Fragment X; 6 = Anjapolo, about 13 km north-west of Berenty.
Dashed outlines include degraded spiny and/or scrub areas.
The rest of the territory (white) is covered by pasture and
sisal fields. (Map based on Google Earth satellite view).
We performed the survey via walking, at a speed of about 1
km/h, along preexisting trails and through forest paths chosen
ad hoc to have visibility of at least 50 m to the right and left (to
avoid pseudoreplication we followed Norscia and Palagi,
2008).
During the census we evaluated the fur condition of each individual lemur.We scored coat condition on a 3-point scale:coat
undamaged, with fur fully covering the body (level 1); ruffled
coat,with fur punctuated by small areas of reduced/missing fur
(on less than 30 % of the body, especially on elbows and/or
knees;level 2);patchy coat,usually with black skin areas clearly
visible due to reduced/missing fur (on more than 30 % of the
body, especially on elbows/knees, external sides of forearms
and thighs, fingers and toes; level 3) (Fig. 3).
Statistics
We performed the analyses at group or at forest site level.
Owing to the small sample size (n<10 for forest sites) or deviation from normality (when n$10,in the analyses per group;
Kolmogorov-Smirnov, p<0.05), we applied non-parametric
tests (Siegel and Castellan, 1988) and considered exact pvalues according to Mundry and Fischer (1998).
Results
In total we counted 183 sifaka adults and 25 infants (less than
1 y old, not included in the analyses). In the riverine forest
areas we counted 81 adult males and 57 adult females
whereas in the spiny forest we counted 45 individuals and
were able to sex 21 adult males and 19 adult females.Overall,
we observed level 3 fur condition only in four subjects (two
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Lemur News Vol. 15, 2010
in the spiny and two in the non-spiny forest areas). Thus, we
considered only level 1 (undamaged coat) and 2 (moderately
missing fur) for the analyses and found that the proportion of
individuals with level-1 fur was significantly higher in the nonspiny than in the spiny areas both in the analysis per forest
site (Exact Mann-Whitney U test, nnon-spiny=3, nspiny=6, Z=
-2.35, p=0.024) (Fig. 2) and in the analysis per group (MannWhitney U test, nnon-spiny=31, nspiny=11, Z=-3.26, p=0.001).
0.90
FUR CONDITION
0.80
0.70
0.60
0.50
0.40
0.30
0.20
SPINY FOREST
AREAS
RIVERINE
FOREST AREAS
Fig. 2: Difference in fur condition (proportion of individuals
showing level-1 fur) between the spiny and riverine forest areas. The difference is significant (p<0.05). Black lines: median;
box: 25-75%; whiskers: non-outlier range.
Discussion
Monitoring coat condition in an apparently healthy population can yield a baseline of data for climate changes (being
influenced by climatic factors such as temperature and
amount of solar radiation) and eventual pathology,and reveal
differences between population segments, and in forest fragments can track progressive degradation or improvement
over time (Jolly, 2009a).
For the sifaka, we found that fur condition was better in the
riverine forest areas than in the spiny forest domain (Fig. 2),
reflecting the fact that riverine forest areas are richer than
spiny forest areas in terms of staple food for lemurs. However, the comparison had to be restricted to individuals with
full coat and moderately missing fur (level 1 and 2, respectively) because only four sifaka showed fur in truly bad condition (level 3;Fig.3 shows the worst fur - and animal - condition
observed in the forest).
In the Lemur catta of Berenty,serious fur loss was due to the alopecia syndrome, associated with the consumption of the
toxic plant Leucaena leucocephala (Jolly, 2009b). Although consumed also by P. verreauxi in the past (Simmen et al., 2003), L.
leucocephala was not present in the spiny forest and removed
from Berenty when this study was performed (H Rambeloarivony, pers. comm.).
Lemurs in the non-spiny forest domain are characterized by
a good nutritional status (due to accessibility of protein-rich
food) (Jolly et al., 2006), which positively reflects on pelage.
The sifaka of the spiny forest,which is characterized by an entirely open canopy, are exposed to high temperatures and
need to save energy, and this situation positively influences
pelage growth as well.Although different in nature,these two
pressures (food availability and heavy exposure to light) both
Fig. 3: Sifaka male (probably old and/or sick) in the spiny forest
showing fur in very bad condition (level 3). (Photo: Ivan Norscia)
act positively on pelage,probably dampening the differences in
fur conditions between spiny and non-spiny forest sifaka.Considering the type of coat "damage" in the spiny forest (ruffled
fur and/or missing/reduced fur in small areas), the most likely
and obvious correlate is the "unfriendly" vegetation, forming
an open canopy that oblige the sifaka to travel through (and
hide in) the thorny undergrowth.
Whilst sifaka density plummets when moving away from the
riverine to the spiny forest areas, following the sharp gradient
generated by water availability decrease (Norscia and Palagi,
2010),it seems that fur condition can only slightly differentiate
sifaka segments of population inhabiting riverine forests and
adjacent or close spiny forest areas.
Acknowledgements
Thanks are due to Monsieur Jean de Heaulme, the de
Heaulme family for the possibility of working at Berenty;
Alison Jolly for encouraging us in investigating fur conditions
of sifaka at Berenty; Danny Randriamanantena and the forest
manager Haja Rambeloarivony for logistic help at Berenty;
Jean Lambotsimihampy for its guidance; Mara Hozonbolo,
guardian of Anjapolo; Mosa Tsifary and Solosoa Alisoa, guardians of West Rapily, for assistance; Daniela Antonacci and
Chandra Brondi for helping with sifaka census.Special thanks
to Paolo Cavicchio (Giardino Zoologico di Pistoia), Iole
Palanca (Parco Zoo Falconara), and Maria Rodeano (Parco
Zoo Punta Verde, Lignano Sabbiadoro), who funded this
research.
References
Elmqvist, T.;Pyykönen, M.;Tengö,N.;Rakotondrasoa,F.;Rabakonandrianina, E.; Radimilahy, C. 2007. Patterns of loss and
regeneration of tropical dry forest in Madagascar: the social institutional context. Plos One 2(5), e402, DOI 10.
1371/journal.pone.0000402.
Lemur News Vol. 15, 2010
Fenn, M.D. 2003. The spiny forest ecoregion. Pp. 1525-1530.
In: S.M. Goodman; J.P. Benstead (eds.). The Natural History of Madagascar. University of Chicago Press, Chicago.
Ganzhorn, J.U.; Goodman, S.M.; Dehgan, A. 2003. Effects of
forest fragmentation on small mammals and lemurs. Pp.
1228-1234. In: S.M. Goodman; J.P. Benstead (eds.). The
Natural History of Madagascar. University of Chicago
Press, Chicago.
Jolly, A. 2009a. Coat conditions of ringtailed lemurs, Lemur
catta, at Berenty Reserve, Madagascar: I. Differences by
age, sex, density and tourism, 1996-2006. Am. J. Primatol.
71: 191-198.
Jolly, A. 2009b. Coat conditions of ringtailed lemurs, Lemur
catta, at Berenty Reserve, Madagascar: II. Coat and tail
alopecia associated with Leucaena leucocephala. Am. J.
Primatol. 71: 199-205.
Jolly, A; Koyama, N; Rasamimanana, H; Crowley, H; Williams,
G. 2006. Berenty Reserve: a research site in southern Madagascar.Pp.32-42.In:A.Jolly,R.W.Sussman,N.Koyama,H.
Rasamimanana (eds.). Ringtailed Lemur Biology: Lemur
catta in Madagascar. Springer Verlag, New York.
Kenagy, G.J.; Pearson, O.P. 2000. Life with fur and without:
experimental field energetics and survival of naked meadow voles. Oecologia 122: 220-224.
Ling, J.K. 1970. Pelage and molting in wild mammals with
special reference to aquatic forms.Q.Rev.Biol.45:16-54.
Mundry, R; Fischer, J. 1998. Use of statistical programs for
nonparametric tests of small samples often leads to
incorrect P values: examples from Animal Behaviour.
Anim. Behav. 56: 256-259.
Norscia, I.; Palagi, E. 2010. Fragment quality and distribution
of the arboreal primate Propithecus verreauxi in the spiny
forest of south Madagascar. J. Trop. Ecol. DOI:
10.1017/S0266467410000519.
Norscia, I.; Palagi E. 2008. Berenty 2006: census of Propithecus
verreauxi and possible evidence of population stress. Int. J.
Primatol. 29: 1099-1115.
Scott, D.W.; Miller, W.H.; Griffin, C.E. 2001. Structure and
function of skin. Muller and Kirk’s Small Animal Dermatology, 6 ed. W.B. Saunders, Philadelphia.
Seddon, N.; Tobias, J; Yount, J; Ramanampamonjy, J.M.;
Butchart,S;Randrianizahana H.2000.Conservation issues
and priorities in the Mikea forest of south-western Madagascar. Oryx 34: 287-304.
Siegel, S.; Castellan, N.J. Jr. 1988. Nonparametric Statistics for
the Behavioral Sciences, Second edition. MacGraw-Hill,
New York.
th
Rediscovery of Sibree’s dwarf lemur in
the fragmented forests of Tsinjoarivo,
central-eastern Madagascar
Marina B. Blanco
Department of Anthropology, University of Massachusetts,
240 Hicks Way, Amherst, MA 01003, USA,
mbblanco@anthro.umass.edu
The recent genetic confirmation of a rare dwarf lemur
species, C. sibreei, at Tsinjoarivo is bitter-sweet. The excitement of reporting the first known living population of this
species is tainted by conservation concerns, as the forest
fragment in which Sibree’s dwarf lemurs were captured is
highly disturbed and targeted for illicit logging. This species,
like many others inhabiting rapidly degrading forests, faces
the serious threat of extinction.
Taxonomic background of the genus, first field discovery, and subsequent recognition of C. sibreei
During the 19th century,the small nocturnal lemurs of Madagascar were clumped in a chaotic array of species and genera.
For most of the 20th century,however,dwarf lemurs (Cheirogaleus) were classified in only two species: the eastern C.
Page 67
major and the western C.medius (Schwarz,1931).Around the
turn of the century, Groves (2000) conducted a taxonomic
revision of the genus on the basis of morphological analysis
of museum specimens and increased the species number to
seven: C. medius, C. adipicaudatus, C. major, C. ravus, C. crossleyi,
C. minusculus and C. sibreei. This last species, in fact, had been
originally described by the Swiss naturalist Forsyth Major in
1896 during one of his expeditions to Madagascar (Forsyth
Major, 1896). He had named it Chirogale sibreei in honor of
fellow naturalist James Sibree, who had spent more than fifty
years in Madagascar and had written extensively about its
people, fauna, flora and geology. Forsyth Major published
measurements of an individual "obtained from the neighbourhood of Ankeramadinika," a locality vaguely described
by its discoverer as "one day’s journey to the east of Antananarivo",but in fact a well-known village at the time,located in
the central high plateau on the road that connected Antananarivo to Mahatsara on the east coast (Capitaine "X",
1901). In his taxonomic revision, Groves (2000) included as
Cheirogaleus sibreei not only the holotype from Ankeramadinika (currently housed at the Natural History Museum in
London) but also three additional specimens (3 skins and 1
skull), two of which came from Ampasindava, northwestern
Madagascar, and one from an unclear provenance (Imerina,
which refers to a region of the central highlands around
Antananarivo).
The taxonomic shrinkage of Cheirogaleus
The increase in the number of species within the genus
Cheirogaleus was not surprising because dwarf lemurs occupy
a wide variety of habitats in Madagascar, and their close relatives, the mouse lemurs (Microcebus), had undergone a taxonomic explosion of their own with more than 10 species
described during the past 15 years (Louis et al., 2008;Olivieri
et al., 2007; Radespiel et al., 2008). However, Groves’ 2000
revision of dwarf lemur taxonomy did not escape criticism,
not least of which had to do with the criteria that he used to
define species, the lack of reliable locality information from
museum specimens, and the absence of on-the-ground surveys to assess geographic boundaries and variation among
species (Blanco et al., 2009; Tattersall, 2007). A recent and
more comprehensive revision of dwarf lemur taxonomy was
carried out by Groeneveld and colleagues, who compiled
genetic and morphometric data from field as well as museum
specimens from a variety of localities across Madagascar,
including some of the specimens studied by Groves (Groeneveld et al., 2009; 2011). This research showed overall consistency between morphological and genetic data in recognizing only three Cheirogaleus species: C. medius, C. major
and C. crossleyi. Individuals that previously had been assigned
to C. adipicaudatus fell within the C. medius clade, and those
named as C. ravus grouped with C. major. Results were inconclusive for C.minusculus and C.sibreei because holotype specimens were not available for sampling and their genetic affiliation could not be determined. Genetic data from one of the
C. sibreei museum specimens from Ampasindava linked this
specimen to C. medius. Nevertheless, the C. sibreei holotype
from Ankeramadinika was larger and did not group morphologically with other C. medius. This suggested that the individuals from Ampasindava may have been misclassified by
Groves as C. sibreei (Groeneveld et al., 2010). The status of
this species remained equivocal.
Second field discovery of C. sibreei, at last
The story of a dwarf lemur named "May" told by Mitchell
Irwin (2002) turned out to be rather prophetic. Irwin’s
research team rescued this dwarf lemur badly burned in a
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Lemur News Vol. 15, 2010
human-induced fire nearby Andasivodihazo,one of the forest
fragments at Tsinjoarivo (Fig. 1). At the time, "May" was believed to be, as were all eastern rainforest dwarf lemurs, C.
major. Unfortunately, this female could not fully recover and
died soon after the salvage, but her skeletal remains were
carefully preserved and stored at the University of Antananarivo by Irwin’s team. Seven years later this specimen came
to play a key role in our morphological analysis of dwarf
lemurs at Tsinjoarivo.
Fig.2: Sibree’s dwarf lemur captured at Andasivodihazo, one
of the forest fragments at Tsinjoarivo.
Fig.1: Map showing Tsinjoarivo and other localities associated with Sibree’s dwarf lemurs; see text for details.
In 2006, with the logistic help of Mitchell Irwin and Jean-Luc
Raharison, I began a survey of nocturnal lemurs at Tsinjoarivo. My assistants and I successfully trapped dwarf lemurs
at two study sites: in one of the forest fragments (Andasivodihazo, 19º41’15"S, 47º46’25"E, 1660 m) and within continuous forest (Vatateza, 19º43’15"S, 47º51’25"E, 1396 m)
(Blanco et al., 2009). Even to an inexperienced eye, fragment
dwarf lemurs looked different from continuous forest individuals, in that they were overall smaller, with grayer fur,
marked eye rings and significantly larger female genitalia (Fig.
2). Our morphological and dental analyses determined that
of all the species described by Groves,C.sibreei was the most
similar to forest fragment dwarf lemurs (Blanco et al., 2009).
(Hopefully, sampling of C. sibreei’s holotype will be allowed in
the near future to definitely determine whether or not there
is a genetic match between this specimen and fragment
dwarf lemurs from Tsinjoarivo.) Recent genetic analyses
have confirmed not only that dwarf lemurs from Andasivodihazo constitute a different clade (and therefore an independent phylogenetic lineage), but also that the fragment
dwarf lemur species had branched off first and was ancestral
to the other dwarf lemur species (Groeneveld et al., 2010).
To date, no other living population of C. sibreei has been
reported in the wild and more intensive surveys around the
Tsinjoarivo area (including possibly remaining forests nearby
Ankeramadinika, ~100 km from Tsinjoarivo) are warranted
to assess geographic boundaries and population density.
Conservation concerns
The genetic confirmation of three clades corresponding to C.
medius, C. major and C. crossleyi, each of which has broad
geographic distributions, implied that dwarf lemurs might be
less threatened than previously thought (Groeneveld et al.,
2009). However, the situation for C. sibreei is radically different. Tsinjoarivo’s unique geographic setting, continuous
with the central plateau on the west and the steep escarpment of rainforest in the east, may harbor a unique array of
animal communities. To date, C. sibreei has been captured in
sympatry with C. crossleyi at one forest fragment, Andasivodihazo,and at one intermediate location,Ankadivory.Both of
these areas are subjected to illicit logging and heavy deforestation (Fig.3).Furthermore,these forest sites are located towards Tsinjoarivo’s western boundary which reaches some
of the highest altitudes (up to ~1650 m) known in eastern
Fig. 3: Example of logging near Ankadivory, one of the forest
sites where Sibree’s dwarf lemurs were captured.
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Lemur News Vol. 15, 2010
rainforests in Madagascar.So far,only C.crossleyi has been captured at Vatateza, a lower altitude site located within continuous and less disturbed forest. Virtually everything has to be
learned about the "ancestral" C. sibreei, including how to prevent its extinction through habitat loss.Concerted efforts by
organizations such as Sadabe (www.sadabe.org) are instrumental in raising awareness of endangered species and promoting research and educational programs in the Tsinjoarivo
area.
Acknowledgements
I am particularly thankful to the research team in Madagascar: Malagasy students Vololonirina Rahalinarivo and Mamihasimbola Rakotondratsima, and local assistants Noel Rakotoniaina, Edmond and Nirina Razanadrakoto. Additional
thanks to Jean-Luc Raharison and Mitchell Irwin for providing logistical support and assistance in the field. I am also
grateful to Laurie Godfrey, Stacy Gebo and Christoph
Schwitzer for their comments. This research was supported
by funds from the Rufford Foundation, MMBF/Conservation
International Primate Action Fund and Primate Conservation Inc. I would like to thank the Ministère de l’Environnement et des forêts of the Malagasy government and the University of Antananarivo for permission to conduct this research.The project in Madagascar was facilitated by the Institute for the Conservation of Tropical Environments (ICTE,
Patricia C. Wright) and the Madagascar Institute pour la
Conservation des Ecosystèmes Tropicaux (MICET), especially Benjamin Andriamihaja.
References
"X." 1901. Voyage du Général Gallieni: cinq mois autour de
Madagascar, progrès de l’agriculture, développement
commercial, ressources industrielles, moyens de colonisation. Hachette, Paris.
Blanco, M. B.; Godfrey, L.R.; Rakotondratsima, M.; Rahalinarivo, V.; Samonds, K. E.; Raharison, J-L.; Irwin, M. T. 2009.
Discovery of sympatric dwarf lemur species in the high
altitude forest of Tsinjoarivo, eastern Madagascar: implications for biogeography and conservation.Folia Primatol.
80: 1-17.
Forsyth Major, C. I. 1896. Diagnosis of new mammals from
Madagascar. Ann. Mag. Nat. Hist. 6: 318-325.
Groeneveld, L. F.; Weisrock, D. W.; Rasoloarison, R. M.; Yoder,
A. D.; Kappeler, P. M. 2009. Species delimitation in lemurs:
multiple genetic loci reveal low levels of species diversity
in the genus Cheirogaleus. BMC Evol. Biol. 9: 30.
Groeneveld, L. F.; Blanco, M. B.; Raharison. J-L.; Rahalinarivo, V.;
Kappeler, P. M.; Godfrey, L. R.; Irwin, M. T. 2010. MtDNA and
nDNA corroborate existence of sympatric dwarf lemur species at Tsinjoarivo,eastern Madagascar.Mol. Phylogenet. Evol.
55: 833-845.
Groeneveld, L. F.; Rasoloarison, R. M.; Kappeler, P. M. 2011
Morphometrics confirm taxonomic deflation in dwarf
lemurs (Primates: Cheirogaleidae) as suggested by genetics. Zool. J. Linn. Soc. 161: 229-244.
Groves, C. P. 2000. The genus Cheirogaleus: unrecognized biodiversity in dwarf lemurs. Int. J. Primatol. 21: 943-962.
Irwin, M.T.2002.The story of May,a courageous dwarf lemur.
IPPL News April: 12-14.
Louis, E. E.; Engberg, S. E.; McGuire, S. M.; McCormick, M. J.;
Randriamampionona, R.; Ranaivoarisoa, J. F.; Bailey, C. A.;
Mittermeier, R. A.; Lei, R. 2008. Revision of the mouse
lemurs,Microcebus (Primates, Lemuriformes),of northern
and northwestern Madagascar with descriptions of two
new species at Montagne d’Ambre National Park and
Antafondro Classified Forest. Primate Conservation 23:
19- 38.
Mullens, J. 1875. Twelve Months in Madagascar. James Nisbet
& Co., London.
Olivieri,G.;Zimmermann,E.;Randrianambinina,B.;Rasoloharijaona, S.; Rakotondravony, D.; Guschanski, K.; Radespiel,
U. 2007. The ever-increasing diversity in mouse lemurs:
Three new species in north and northwestern Madagascar. Mol. Phylogenet. Evol. 43: 309-327.
Radespiel, U.; Olivieri, G.; Rasolofoson, D. W.; Rakotondratsimba, G.; Rakotonirainy, O.; Rasoloharijaona, S.; Randrianambinina, B.; Ratsimbazafy, J. H.; Ratelolahy, F.; Randriamboavonjy, T.; Rasolofoharivelo, T.; Craul, M.; Rakotozafy, L.;
Randrianarison,R.M.2008.Exceptional diversity of mouse
lemurs (Microcebus spp.) in the Makira region with the
description of one new species. Am. J. Primatol. 70: 10331046.
Schwarz, E. 1931. A revision of the genera and species of Madagascar Lemuridae.Proc.Zool.Soc.Lond.1931:399-426.
Tattersall, I. 2007. Madagascar’s lemurs: Cryptic diversity or
taxonomic inflation? Evol. Anthropol. 16: 12-23.
Funding and Training
AEECL Small Grants
Since 2009, AEECL awards two small grants of up to € 1,000
each year to graduate students, qualified conservationists
and/or researchers to study lemurs in their natural habitat.
Priority is given to proposals covering conservation-relevant
research on those species red-listed as Vulnerable, Endangered, Critically Endangered or Data Deficient by the IUCN.
We support original research
that helps with establishing
conservation action plans for
the studied species. Grants
are normally given to recent
graduates from Malagasy universities to help building local
capacity.
We may also, in special circumstances, support studies on
Malagasy species other than lemurs if the proposal provides
satisfactory information as to how lemurs or the respective
habitat/ecosystem as a whole will benefit from the research.
All proposals will be assessed by the Board of Directors of
AEECL and/or by external referees.The deadline for applications is February 15th of each year. Successful applicants will
be notified by June 1st.More information can be found on the
AEECL website, www.aeecl.org.
The Mohamed bin Zayed Species Conservation Fund
Announced at the World Conservation Congress in Barcelona in 2008,The Mohamed bin Zayed Species Conservation
Fund is a significant philanthropic endowment established to
do the following:
Provide targeted grants to individual species conservation
initiatives;
Recognize leaders in the field of species conservation;and Elevate the importance of species in the broader conservation
debate.
Page 70
The fund’s reach is truly global,and its species interest is nondiscriminatory. It is open to applications for funding support
from conservationists based in all parts of the world, and will
potentially support projects focused on any and all kinds of
plant and animal species, subject to the approval of an independent evaluation committee.
Details on this important new source for species conservation initiatives and research can be found at
www.mbzspeciesconservation.org
CI Primate Action Fund
The principal objective of Conservation International’s Primate Action Fund is to contribute to global biodiversity
conservation by providing strategically targeted, catalytic
support for the conservation of endangered nonhuman
primates and their natural habitats.
Projects submitted to the foundation should have one or
more of the following characteristics:
· A focus on critically endangered and endangered nonhuman primates (and most especially those included in the
biennial listing of the World’s 25 Most Endangered Primates) living in their natural habitats;
· Location in areas of high overall biodiversity and under great
threat (e.g., "threatened hotspots", "megadiversity" countries) - to ensure maximum multiplier effect for each project;
· Direction and management by nationals from the tropical
countries,to help increase local capacity for implementing
biodiversity conservation;
· The ability to strengthen international networks of fieldbased primate specialists and enhance their capacity to be
successful conservationists; and
· Projects that result in publication of information on endangered primate species in a format that is useful both to
experts and the general public.
Applications for support are considered throughout the year
with no deadlines for submittal. Proposals should be sent by
electronic mail to:
Anthony B. Rylands, Primate Action Fund, Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA
22202, USA, a.rylands@conservation.org
Recent Publications
Lemurs of Madagascar, 3rd edition, by Russell A. Mittermeier, Edward E. Louis Jr., Matthew Richardson, Christoph
Schwitzer, Olivier Langrand, Anthony B. Rylands, Frank Hawkins, Serge Rajaobelina, Jonah Ratsimbazafy, Rodin Rasoloarison, Christian Roos, Peter M. Kappeler and James Mackinnon. Illustrated by Stephen D. Nash. Conservation International, Tropical Field Guide Series, Arlington, VA, 2010. 762
pp. ISBN: 978-1-934151-23-5. US$55.00.
In 2006,Madagascar was making significant progress towards
conservation by expanding the protection of its natural treasures. At the same time, the second edition of Conservation
Lemur News Vol. 15, 2010
International’s Tropical Field Guide Series, Lemurs of Madagascar, had just come off the press, a full twelve years after its
much-celebrated predecessor. A lot has changed in four
years. Political and economic instability has imperiled both
the Malagasy people and their unique wildlife. Conservation
has taken drastic steps backwards as the desperation of the
masses and greed of a few elites and international profiteers
has exacerbated the conflict between the domains of humans and wildlife. CI has answered the call to action by releasing a new third edition of its lemur field guide, dwarfing
previous editions in both size and its depth of research and
detail. With nearly 1,100 references to support it–up from
approximately 500 references in the second edition–the
third edition stands as more than just a complete compendium of our knowledge about lemurs, but the perfect guide
for appreciating the history, diversity, uniqueness, and pure
beauty of our strepsirrhine cousins.
According to CI’s Jill Lucena, from early 2009, the 13 authors
and dozens of contributors have worked tirelessly on the
third edition, dedicating thousands of hours towards its production. Authors Matthew
Richardson and Anthony B.
Rylands, as well as illustrator Stephen D. Nash and
graphic designer Paula K.
Rylands, labored exclusively
on the project for nine
months. The end result is a
field guide that will leave
other academic fields envious! This new volume is 247
pages longer than the previous edition, with 767 pages
of carefully organized maps,
photos, and colorful illustrations, in addition to all
the details lemur enthusiasts and researchers have
come to expect from this
book.The content is so rich
that the book’s dimensions
have increased from 7.5" x
4.5" x 1" to slightly more than 9.25" x 6.25" x 1.25" just to accommodate everything.And herein lies what may be the only
problem with this new edition. Reviews of the previous two
editions had lavished praise for not only the content and
scope, but also the portability of the books. Although it will
fit comfortably in a backpack, it will add more weight and
consume more space than its predecessors. But given the
content, that may be a small price to pay.
The layout of the book has not changed much since the last
edition. An enthralling chapter on Madagascar’s ancient geological history has been added, providing tantalizing details
about the mysteries of Madagascar’s ancient past,while a few
familiar chapters and appendices have been reordered. Each
lemur family has now been assigned its own chapter.The section entitled "How to Use This Field Guide" still walks new
readers through the layout of the book. The "Quick Visual
Reference" and colored tabs facilitate speedy navigation and
help to satiate an ecotourists’ spontaneous hunger for specific information. The "Lemur Life-list" returns in a more
readable table format to help ecotourists record their first
sightings of the numerous lemur species. Even the maps of
the island have been revamped and are easier to read in this
larger format.
Introductory chapters discuss ancient geology,lemur origins,
the extinct subfossil (giant) lemurs, the history of lemur re-
Lemur News Vol. 15, 2010
search, and lemur conservation. Each chapter contains significant updates from the second edition. The ancient geology
of Madagascar is covered in meticulous detail, while the theories of lemur origins are explored in depth, leaving both
reader and researcher alike desperate for more definitive
answers.The chapter on the extinct subfossil lemurs is beautifully illustrated with new peer-reviewed artwork from
award-winning illustrator Stephen D. Nash, and has new details about their biology and extinction. The history of lemur
research and discovery expands greatly upon the work from
the last half century–a topic greatly underrepresented in the
previous edition. Additionally, the chapter is loaded with
newly added artwork from the 1700s and 1800s. The lemur
conservation chapter provides a critical update on the newest emerging threats faced by lemurs and their habitat,
namely the logging of precious hardwoods and bushmeat
hunting. Additional detail is also provided about other important threats that received little mention previously, such
as invasive species, cattle-raising, and mining.
The bulk of the book details the description, geographic
range,natural history,conservation status,and best locations
to observe each of the 101 species and subspecies of lemur.
(This total is up from the 71 taxa detailed in the second edition,yet the authors note that upcoming research may reveal
as many as 110 to 125 lemur taxa!) Each species section
sports a portrait photo, detailed range map, and other photos to enrich the lavish textual content. Once again,the third
edition sets itself apart from the previous editions with its
encyclopedic coverage of details from the lemur research literature.Species,such as the silky sifaka (Propithecus candidus),
are discussed in significantly greater detail,bringing everyone
from bright-eyed ecotourists to veteran lemur researcher
up to speed on the latest findings.
The second edition of Lemurs of Madagascar sold out quickly,
leaving shelves empty as early as February 2008. The third
edition is poised to do the same. With a print run of 10,000
copies,nearly two-thirds are already spoken for according to
Jill Lucena.To help promote conservation education in Madagascar, CI is generously donating 3,000 copies to its partner
in the field, NGO Fanamby. CI hopes that the remaining copies will spark the public’s interest in Madagascar’s ecological
gems and spur a new wave of ecotourism to bolster conservation efforts.
Once again, CI has provided an invaluable tool for a diverse
audience, which includes ecotourists, Malagasy tour guides,
students,lemur researchers,and lemur enthusiasts.Although
larger and not quite as portable as its predecessors, the increased size of the third edition hosts a wealth of enhanced
encyclopedic detail, new and stunning artwork by Stephen D.
Nash, and additional color photos and illustrations. With a
copy of this printing in hand, the only things missing are a
backpack full of supplies and an airline ticket to Madagascar.
So what are you waiting for?
Alex Dunkel
Theses Completed
Blanco, M.B. 2010. Reproductive biology of mouse and dwarf
lemurs of eastern Madagascar,with an emphasis on brown
mouse lemurs (Microcebus rufus) at Ranomafana National
Park,a southeastern rainforest.PhD Dissertation.University of Massachusetts, Amherst.
This dissertation investigates reproductive schedules of
brown mouse lemurs at Ranomafana,using intensive trap-
Page 71
ping techniques. The reproductive condition of female
mouse lemurs was recorded on the basis of vaginal morphology,vaginal smears,body mass gain profiles and nipple
development. Testis size was measured in males throughout the reproductive season. The timing of the first seasonal estrus was determined in frequently captured females over multiple years and it showed individual periodicities close to 365 days,consistent with endogenous regulation and entrainment by photoperiod. The timing of
estrus did not correlate with female age or body mass.
Males showed testicular regression during the rainy season, although there was high inter-individual variation in
testes size at any given point during the reproductive season. Furthermore, some individuals completed testicular
regression earlier than others. Implications for polyestry
are discussed.
For comparative purposes, mouse lemurs were also trapped at two study sites in the Tsinjoarivo area: one in a forest fragment and the other within continuous forest.
These forests are higher in altitude than the main study
area at Ranomafana. Trapping success for mouse lemurs
was lower at Tsinjoarivo than Ranomafana.Albeit preliminary, data from Tsinjoarivo suggest that females have lower reproductive success than do females at Ranomafana.
Nevertheless, mouse lemurs in the Tsinjoarivo forest
fragment did not appear to be in "poorer" condition than
those in the continuous forest.It had been reported in the
literature that western gray mouse lemurs captured in secondary forests have lower body masses and lower recapture rates than those captured in primary forest; in fact,
the opposite was true of the mouse lemurs at Tsinjoarivo.
I additionally collected data on a larger member of the
family Cheirogaleidae, the dwarf lemurs (Cheirogaleus),
which live in sympatry with Microcebus at Ranomafana and
Tsinjoarivo. I analyzed the patterns of growth, development and reproduction in Cheirogaleus and Microcebus and
compared dwarf and mouse lemurs to other similarlysized prosimians which do not undergo torpor or hibernation. These comparisons draw attention to the unusual
reproductive and metabolic strategies employed by cheirogaleids to cope with Madagascar’s unpredictable environments, which ultimately define their very unique life
histories.
Key words: Cheirogaleus, Madagascar, Microcebus, Mouse
lemurs, Rainforest, Ranomafana, Reproduction, Tsinjoarivo.
Bonaventure, R.T.A.R. 2010. Ecologie et comportement de
Propithecus verrreauxi dans les zones d’extension de la
Réserve Spéciale de Bezà Mahafaly. Engineer in agronomy,
option Eaux et forêts.Eaux et forêts,Ecole Supérieure des
Sciences Agronomiques de l’Université d’Antananarivo
(ESSA), Madagascar.
The population of Propithecus verreauxi in the special
reserve of Bezà Mahafaly is one of the conservation targets of the site which is the subject of a long-term follow.
Natural destruction of their habitat and the pressure of
hunting which is exerted on this species outside of the
current reserve are the origin of the sifakas’ decline.With
the park extension project under way, furthering the
knowledge on behavior and ecology of Propithecus verreauxi in disturbed areas outside the current reserve is essential for decision-making regarding conservation measures for this species. Thus, a study of behavior and ecology
of the sifakas was carried out in the extension area of the
special reserve of Bezà Mahafaly in gallery and transition
forest at the end of the dry period. The study was centered on 3 focal groups including one in the gallery forest
and two in the transition forest. The method of focal animal sampling was chosen to study their behavior. A floristic inventory according to the Gentry method, which
includes transects of 2 x 50 m, was carried out to study
the habitat. On the whole, 120h of observations of sifaka
behavior were carried out and 12 transects were walked.
In disturbed areas, the sifakas still consumed preferred
plants.This resulted in a high intake of 2 or 3 easily digestible plant species while at the same time a large variety of
other species was consumed.Thus,the disturbance of the
sites did not influence food intake of the sifakas.Moreover,
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Lemur News Vol. 15, 2010
it was the group of sifakas in the gallery forest which was
the most affected by resource scarcity in the dry period,
necessitating a priorisation of the sifaka groups in this forest formation in the extension of the reserve.In addition,
the availability of nutritional resources influenced spacial
dispersion of group members as well as group size. With
the current park extension project different access restrictions will be implemented, having as an objective the
conservation of the sifaka groups as well as other conservation targets outside of the current reserve, while introducing a range of alternative income-generating activities
and sustainable resource management practices for the
local communities.
Key words: Lemur, Propithecus verreauxi, Ecology, Behavior,
Conservation, Special reserve, BezB Mahafaly, Madagascar.
Delmore,K. 2009.Maintenance of stability in the Andringitra
brown lemur hybrid zone.M.A.thesis,University of Calgary, Calgary, Alberta, Canada.
Two models of hybrid zone stability have been proposed:
1) the tension zone model, which predicts that intrinsic
selection acts against hybrids but is counteracted by dispersal of parentals into the zone and 2) the bounded superiority model, which predicts that exogenous selection
favours hybrids within transitional habitats and parentals
outside the zone.I used morphological,genetic and ecological data to evaluate these models in a stable hybrid zone
between Eulemur rufifrons and E.cinereiceps in southeastern Madagascar. This zone appears to conform to the
bounded superiority model: it was relatively wide and
composed mostly of hybrids that were equally as fit as
parentals.Gene flow between parental and hybrid populations was also limited, clines in multiple characters were
non-coincident and significant ecological correlates were
identified. Results suggest that hybridization can serve as
an important evolutionary force and need not always be
considered a conservation risk for endangered taxa.
Hobinjatovo, T. 2009. Etude morphométrique et génétique
de conservation d’Eulemur cinereiceps (Milne-Edwards et
Grandidier, 1890) dans les forêts de Mahabo, de Manombo et de Vevembe, Madagascar. Mémoire de DEA en Biologie,Ecologie et Conservation Animale,Département de
Biologie Animale,Faculté des Sciences,Université d’Antananarivo.
Cette étude a pour but, d’une part, de connaître et de
comparer la morphométrie d'Eulemur cinereiceps de la forêt de Mahabo,de Manombo et de Vevembe - Madagascar,
ainsi donc de voir le degré du dimorphisme sexuel et
d’autre part, d’établir des données de bases génétiques
pour avoir de plus amples informations en vue de la conservation de cette espèce en danger critique. La descente
sur le terrain et la collecte des données ont été effectuées
pendant deux semaines du mois de mai 2006 et le travail
au laboratoire pour l’étude génétique a été fait du mois de
Février au mois de Mai 2007.Ce lémurien pése en moyenne 2,04 kg avec une longueur moyenne de la couronne de
la tête de 10,84 cm,celle du corps de 33,31 cm et est doté
d’une queue de 50,44 cm. La comparaison de la morphométrie des individus des sites d’étude, par le test U de
Mann-Whitney montre que le Lémurien à Collier Blanc
de Vevembe est de plus grande taille que ceux des 2 autres sites. La différence de taille entre le mâle et la femelle
n’est pas significative. Chez cette espèce, le dimorphisme
sexuel est très marqué concernant la couleur du pelage et
la dimension de la canine supérieure,considérable chez le
mâle.Le testicule droit du mâle est plus long,large et volumineux que le gauche.14 marqueurs génétiques polymorphiques ont été sélectionnés pour effectuer le génotypage par l’utilisation de la technologie moléculaire et à l’aide
de la réaction en chaîne polymérasique. Les programmes
de Cervus, GenePop, Fstat, Structure et Bottleneck ont
été utilisés pour déterminer la structure et la nature génétique de la population d’Eulemur cinereiceps. Ces analyses ont permis de déterminer que la valeur de la diversité
des gènes des populations est pareille et modérée, oscillant autour de 57 % ;la divergence génétique est comprise
’
entre 0,05 à 0,15 et est qualifiée de modérée; la richesse
allélique varie de 2,928 à 3,632;une migration entre la population de Mahabo et de Vevembe, d’une part et celle de
Manombo et de Vevembe d’autre part, a été identifiée; un
certain degré de consanguinité a été constaté à Mahabo.
La population de Manombo subit un goulot démographique et aucune structure distincte ni sous - structure n’a
été observée au sein des populations de ces 3 sites.Même
si cette espèce est en danger critique, sa santé génétique
est modérée.Elle pourrait être bonne si les solutions adéquates sur la conservation génétique étaient appliquées.
Dans le cas contraire, elle deviendrait désastreuse. La prise immédiate de mesures de conservation efficientes est
donc nécessaire afin de préserver les populations pures
d’E. cinereiceps et de protéger ses habitats.
Mots-clés: Eulemur cinericeps, Mahabo, Manombo, Vevembe, Madagascar, Morphométrie, Mensuration, Génétique,
Population, Conservation.
Ingraldi, C. 2010. Forest fragmentation and edge effects on
eight sympatric lemur species in southeast Madagascar.
M.A. thesis, University of Calgary, Calgary, Alberta, Canada.
Extensive slash-and-burn agriculture in southeastern Madagascar has led to the fragmentation of forests in this region, creating a constricted available habitat area and increasing the proportion of forest edge. I investigated the
response to forest fragmentation and edge effects in eight
lemur species through comparisons of species density
and diversity between fragments, as well as correlation
analyses including population distribution patterns,ecological variables,and distance from forest edge.I also include
a more detailed focus on the behavioural response of Eulemur cinereiceps. Results were highly varied, with no species showing strong aversion to forest edge but with higher overall densities in larger, more connected fragments.
Eulemur cinereiceps spent significantly more time near the
forest edge while resting, but edge did not affect feeding
patterns or food availability. These results suggest that
conservation management should focus on maintaining
large, complex fragments and improving connectivity
through forest corridors.
Mihaminekena,T.H.2010. Etude de la relation entre la dégradation de l’habitat et les activités de Propithecus edwardsi
du Parc National de Ranomafana Ifanadiana, Madagascar.
Mémoire de DEA en Paléontologie et évolution biologique, Biologie Evolutive, Primatologie, Département de
Paléontologie et d’Anthropologie biologique, Faculté des
Sciences, Université d’Antananarivo.
Une étude sur le comportement et l’habitat de Propithecus edwardsi a été réalisée dans le Parc National de Ranomafana. Elle a été réalisée dans trois sites ayant chacun un
degré de perturbation inégal: Talatakely (fortement perturbé); Sakaroa (moyennement perturbé) et Valohoaka
(non perturbé). Sa finalité est d’analyser le type de comportement biologique adopté par l’espèce en réponse à la
dégradation de son habitat et de le comparer entre les
trois sites. La méthode adoptée est celle décrite par Altmann en 1974 qui consiste à déterminer l’activité du focal
animal toutes les dix minutes et celle de tous les groupes
toutes les cinq minutes. Pour toutes les activités, sauf le
déplacement, la différence est toujours significative pour
les trois sites. Le repos est plus élevé dans le site intact
(36.6%) par rapport à l’alimentation.Inversement le repos
est moins fréquent (28.9 %) que l’alimentation (53.6 %)
dans le site fortement perturbé. La fréquence des activités de l’espèce dans le site moyennement perturbé est
toujours comprise entre les deux sites perturbés et non
perturbés. Pour ses activités, l’espèce utilise certains niveaux de strates, spécialement ceux compris entre 10 et
15 et 15 et 20 m. Néanmoins, l’espèce habitant le site intact se place à un niveau plus haut que celle de la forêt perturbée. Les grands arbres sont plus abondants à Valohoaka qu’à Sakaroa et à Talatakely: respectivement la hauteur
varie de 10.80, 9.53 et 9.47 m; celui du DHP est de 13.59
cm;12.17 et 11.09 cm.Les épaisseurs de la couronne sont
respectivement 4.42,4.28 et 3.91 m.Les parties de plantes
Lemur News Vol. 15, 2010
consommées pour chaque site sont significativement très
différentes. La corrélation entre la consommation de jeunes
feuilles et les activités exercées est toujours positive et significative quel que soit le site. Les femelles choisissent un niveau plus haut des arbres que les mâles à Valohoaka et à Talatakely par contre à Sakaroa c’est l’inverse. La cohésion du
groupe est plus observée dans le site intact par rapport à celui dégradé. Bref, la perturbation influe les activités générales
et la structure de l’habitat de Propithecus edwardsi.
Mots-clés: Propithecus edwardsi, Lémuriens, Degré de perturbation, Habitat, Activités, Parc National de Ranomafana, Madagascar.
Polowinsky, S.Y. 2009. Nutrition of captive Sclater’s lemurs
(Eulemur macaco flavifrons GRAY, 1867) and crowned
lemurs (Eulemur coronatus GRAY, 1842), with special emphasis on the problem of obesity. PhD dissertation, Biology and Geography, University of Duisburg-Essen, Germany.
This study was concerned with the obesity problem of blueeyed black lemurs and crowned lemurs in captivity. Its aims
were to optimize the species’ diet in captivity by combining
data obtained from individuals kept at different European
zoos as well as from wild blue-eyed black lemurs to gain a
better understanding of the ecological and nutritional needs
of Eulemur macaco flavifrons in order to prevent individuals
from becoming obese and to assist planned conservation
measures.
The captive part of the study was conducted in two European zoos:Cologne Zoo (Germany) and Parc Zoologique
et Botanique de Mulhouse, Sud-Alsace (France). A longterm study with one group of blue-eyed black lemurs
(1.3) and one group of crowned lemurs (1.2) was carried
out at Cologne Zoo.In addition,three groups of blue-eyed
black lemurs (2.1; 1.1; 1.1) and three groups of crowed
lemurs (2.2; 2.1; 3.2) were studied at Mulhouse Zoo. The
body weight development of captive individuals was registered and compared to body weight data of wild individuals. The obesity rate in captivity was recorded. An obese
animal was identified as one weighing more than two standard deviations over the mean wild weight. Moreover,
nutrient and energy intake of Eulemur macaco flavifrons
and Eulemur coronatus at Cologne Zoo and Mulhouse Zoo
were registered. In addition, digestibility trials were conducted. Samples of feeds and faeces were analyzed using
Weende analysis and detergent analysis. In Madagascar,
four groups of Eulemur macaco flavifrons in two forest fragments, one mainly primary forest and the other predominantly secondary forest,were observed.Samples of plants
utilized by free-ranging blue-eyed black lemurs were collected. They were botanically classified and analyzed using
Weende analysis and detergent analysis.
The mean body weights of Eulemur macaco flavifrons as well
as Eulemur coronatus in captivity were significantly higher
than the mean body weight of free-ranging individuals.100
% of the Eulemur macaco flavifrons sample and 33.3 % of
the Eulemur coronatus sample were obese.Significant body
weight differences were found between the groups studied at Cologne Zoo and Mulhouse Zoo, which could be
explained by different feeding regimes. Comparing the
diet of free-ranging blue-eyed black lemurs to the zoo
diets that were based mainly on fruits and vegetables at
Cologne Zoo and Mulhouse Zoo, considerable differences were found with respect to NDF,ADF,ADL and crude
protein content, whereas ash and crude lipid content varied only slightly. The NFC and energy content in the zoo
diets were almost twice as high as those in the diet of wild
blue-eyed black lemurs. The high NFC, crude protein and
metabolizable energy content and low fibre content of
the zoo diets as compared to the wild diet,combined with
a relatively high apparent digestibility of ~80 % for Eulemur
macaco flavifrons and ~84 % for Eulemur coronatus, respectively, and in combination with lemurs’ typically low basal
metabolic rates, all clearly contribute to the obesity problem of captive Eulemur macaco flavifrons.
The presented data of food consumed by Eulemur macaco
flavifrons in captivity and in the wild reveals elementary
differences concerning nutrient and energy composition.
Although a bright variety of fruits and vegetables could
Page 73
protect animals in captivity from stereotypic behaviour, a
systematic reassessment of the zoo diet is suggested:
increasing fibre content and decreasing energy density by
feeding vegetables,and whenever possible,fresh plant material in appropriate quantities instead of energy-rich
fruits, gruel or commercial feeds. Although the utilization
of the food fibre content by a generalist frugivore like Eulemur macaco flavifrons or Eulemur coronatus is limited, fibre content plays an important role in the maintenance of
physiological health. A zoo diet corresponding to the natural requirements of lemurs guarantees an optimization
of breeding programmes and presents a valuable and necessary contribution to the preservation of these highly
endangered species.
Key words: Eulemur macaco flavifrons, Eulemur coronatus,
Nutrition, Digestibility, Obesity, Captivity, Energy intake.
Rafaliarison R.R. 2010. Activité générale du Prolemur simus:
transition saison sèche - saison de pluies et activité de la
femelle avant et après mise bas dans le Parc National
Ranomafana.Département de Paléontologie et d’Anthropologie Biologique, Université d’Antananarivo, Madagascar.
Cette étude a été réalisée dans la parcelle 3 du parc national Ranomafana qui abrite le seul groupe du parc.Elle nous
aidera à mieux comprendre les variations de l’activité générale du Prolemur simus pendant la transition de la saison
sèche à la saison de pluie ainsi que la variation de l’activité
de la femelle avant et après mise bas. Les résultats ont
montré que le Prolemur simus a dépensé la moitié de leur
temps à l’alimentation suivi du repos. Les variations de la
fréquence de l’activité sont en relation avec la partie consommée (tige, moelle ou jeunes pousses), la disponibilité
alimentaire, la température et la pluie ainsi que la disponibilité en eau.La strate la plus utilisée est comprise entre 0
à 5 m. La présence d’un nouveau né a une influence sur
l’activité et la proximité des individus du groupe. Pour la
femelle, il y a une diminution de la fréquence de l’alimentation après la mise bas. Il y a aussi une augmentation très
marquée de la fréquence du repos après la mise bas.Le juvénile s’éloigne de la femelle après mise bas tandis que le
mâle reste toujours près de la femelle.
Mots clés: Prolemur simus, Activités, Mise bas, Parc National Ranomafana, Madagascar.
This study was carried out in Parcel 3 of Ranomafana National Park, where the only group of Prolemur simus within
the park is present.It concerns the variation in the general
activities of P.simus during the transition from the dry season to the rainy season as well as the activity of the female
before and after giving birth. The results showed that P. simus spent half of their time feeding, followed by resting.
The variation in frequency of activities was related to the
consumed plant parts (trunk,culm pith or bamboo shoot),
availability of food,temperature,rain and the availability of
water. The most frequently used forest stratum was between 0 and 5 m of height. The presence of the new-born
had an influence on the activity and the spacing of the individuals in the group.For the female,there was a reduction
of the frequency of feeding after giving birth. There was
also a very marked increase in the frequency of resting after birth. The juvenile stayed away from the female after
she had given birth,but the male always remained close to
the female.
Key words: Prolemur simus, Activity, New born, Ranomafana National Park, Madagascar.
Raharivololona, B.M. 2010. Intestinal parasite infection of the
gray mouse lemur (Microcebus murinus, J.F. Miller, 1777) in
the south-eastern littoral forest of Madagascar. PhD Dissertation, Hamburg University, Hamburg, Germany.
Madagascar’s plants and animals belong to one of the most
unique and threatened biotas of the world. Lemurs are
the flagship species associated with the biological crisis of
the island and notably vulnerable to habitat degradation.
While most studies on the effect of habitat destruction
on species survival have focused on population reduction
and forest degradation, indirect effects, such as altered
parasite loads have received little attention. Parasitologi-
Page 74
cal studies have concentrated on large primates, such as
apes and monkeys.This is probably due to epidemiological
interest in apes, which are genetically closer to humans
and are known to be a reservoir of certain pests and
diseases fatal to humans. Prosimians’ gastrointestinal parasites are less studied.
The goal of this project was to assess and describe the
gastrointestinal parasites of the lemur species Microcebus
murinus (Family Cheirogaleidae), also known as the gray
mouse lemur, from the littoral forest fragments of Mandena in extreme southeastern Madagascar. In addition, I
wanted to evaluate the utility of determining gastrointestinal parasite loads based on fecal samples. From April
2003 to October 2005, 427 fecal samples obtained
from169 different individuals of M. murinus from five forest fragments were analyzed to assess the parasite species richness of this animal based on parasite egg morphology. Three individuals of M. murinus were also sacrified in
order to look for adult worms for identification and confirmation of parasite species, and to localize their gastrointestinal parasites in the digestive tract. Screening all
fecal samples by using the modified technique of the
McMaster flotation, I noted that M. murinus harbored at
least nine different intestinal parasites, which included 1)
six Nemathelminthes:a member of the family Ascarididae,
one species of the family Subuluridae represented by the
genus Subulura, an unidentified Strongylida, a species of the
genus Trichuris (Trichuridae), two species of the family
Oxyuridae: the first belongs to the genus Lemuricola and
the second is still unidentified; 2) two Plathelminthes: two
cestodes of the genus Hymenolepis (Hymenolepididae); 3)
one Protozoa: belonging to the order Coccidia.
These gastrointesinal parasites of M.murinus from Mandena
have not been previously described from this primate.
The cestode infection deserves special attention, as these
parasites have not been previously reprted from lemurs.
Adult worms of Trichuris species were found in the caecum, as well as Lemuricola worms in the caecum and large
intestine.Subulura worms were more abundant in the caecum than in the small and large intestine. A large number
of Subulura larvae were observed in the caecum.As exemplified by the data on Subulura sp. worms in the digestive
tract of M.murinus,the number of nematode parasite eggs
and larvae found in the feces are correlated with the intensity of infection in the digestive tract.
To assess effects of forest fragmentation and degradation, fecal samples from the first captureof 169 individuals of Micro-
cebus murinus living in five littoral forest fragments were
analyzed for gastrointestinal parasites. The fragments differed in size and forest quality. In good quality forest
blocks, lemurs from a smaller fragment had higher prevalences and intensities of infection of gastrointestinal nematodes and protozoans than animals from a larger forest
fragment. In larger forest blocks, excretion of eggs from
Ascarididae and tapeworms was higher in a degraded forest fragment than in a better quality forest fragment.This
situation was reversed in small forest fragments with fewer eggs of Subulura nematodes and protozoans shed by
lemurs in the degraded fragment than by lemurs from the
good quality fragment. The analyses are hampered by the
fact that only one forest fragment was available per type
of treatment. Keeping this limitation in mind, the results
are consistent with other studies and indicate that forest
degradation and fragmentation have marked effects on
the level of parasitism of Madagascar’s lemurs.
To assess seasonal effects on the excretion of gastrointetinal parasites I screened fecal samples from M. murinus
caught during monthly trapping sessions for eggs and
larvae of intestinal parasites. Parasite excretions changed
seasonally when analyzed at the level of individual hosts.
The number of parasite species and the abundance of parasite eggs and larvae in Microcebus feces were higher during the hot season than the cold season. Reduced parasite excretion during the cold season could be due to environmental factors or due to the ability of M. murinus to
enter torpor and hibernation during the cold season
which might lead to reduced metabolism of intestinal parasites and results in reduced shedding of parasite eggs.
Lemur News Vol. 15, 2010
No such seasonal variation was found on the level of the
lemur population when the analyses were based on samples of unknown origin.
The study revealed noticeable effects of forest fragmentation on parasite loads as measured via the excretion of
parasites. The disadvantageous consequences of increased parasite infections on the health of these animals is due
to changes in habitat conditions and is a factor that needs
to receive more attention when developing conservation
plans.
Key words: Microcebus murinus, Parasites, Habitat degradation, Fragmentation, Forest quality, Hymenolepis.
Randrianarimanana, H.L. 2009. Etude comparative de l’alimentation et du comportement des deux espèces sympatriques d’Indriidés :Propitecus diadema et Indri indri dans
le Réserve Naturelle Intégrale n°1 de Betampona (Tamatave).Mémoire de DEA en Paléontologie et évolution biologique,Biologie Evolutive,Primatologie,Département de
Paléontologie et d’Anthropologie biologique, Faculté des
Sciences, Université d’Antananarivo.
Des études comportementales et nutritionnelles des
deux espèces sympatriques d’Indriidés (Propithecus diadema et Indri indri) ont été réalisées pendant les mois de
mars,avril,juin et juillet 2008 dans la Réserve Naturelle Intégrale numéro un de Betampona (Tamatave). Les données comportementales et nutritionnelles, la hauteur fréquentée et la nature des supports et des coordonnées
géographiques ont été enregistrés toutes les 10 minutes.
Des analyses statistiques ont été réalisées pour étudier
comment ces deux plus grands lémuriens partagent leurs
nourritures et habitats. Même si les deux espèces ont la
même fréquence d’alimentation et sont toutes deux considérées folivores, Propithecus diadema consomme un peu
plus de fruit qu’Indri indri (respectivement 33,6 et 9,4 %) et
utilise beaucoup plus d’espèces végétales comme source
de nourriture. Propithecus diadema fréquente des hauteurs beaucoup plus basses qu’Indri indri durant ses activités (8,3071et 10,208 m). De plus, cette dernière espèce
utilise beaucoup de petits supports (respectivement 3,80
et 5,38 cm) et peu inclinés (40,32° et 47,79°). Propithecus
diadema se déplace beaucoup tandis qu’Indri indri se repose davantage. Malgré le chevauchement de leur territoire,
ces deux espèces montrent une séparation de leur niche
écologique.
Mots-clés: Propithecus diadema, Indri indri, Alimentation,
Comportement, Comparaison.
Razafindratsima, O.H. 2009. Rôle écologique de Varecia rubra
et d’Eulemur albifrons dans le Corridor Ambatolaidama du
Parc National Masoala.Mémoire de DEA en Biologie,Ecologie et Conservation Animale, Département de Biologie Animale, Faculté des Sciences, Université d’Antananarivo.
Une étude a été effectuée sur deux espèces de lémuriens
sympatriques dans les forêts tropicales humides du corridor Ambatolaidama du Parc National Masoala - Varecia
rubra (Geoffroy, 1812) et Eulemur albifrons (Geoffroy,
1796). Le but est d’étudier les rôles écologiques de ces
espèces dans la reforestation du corridor en tant que disséminatrices de graines. Ceci afin de mettre en évidence
leur importance au niveau de ce site et par conséquent,
d’élaborer une stratégie de conservation. Un groupe d’E.
albifrons et trois groupes de V.rubra ont été suivis.Trois femelles de V.rubra,choisies comme animaux focaux,ont été
munies de colliers à radio émetteur. Ces espèces ont fait
l’objet de suivis quotidiens, de novembre 2006 à janvier
2007, afin de collecter des informations sur leur régime
alimentaire et leur défécation. Pour E. albifrons, aucune
donnée sur son alimentation n’a été obtenue de part la
difficulté de son suivi dû à l’absence de collier. Les fèces
collectées sont analysées afin d’en extraire des graines qui
ont été, ensuite, inventoriées, mesurées et identifiées. La
viabilité de ces graines a été étudiée par un test d’immersion dans l’eau, puis par la mise en terre dans une pépinière des graines déféquées comparées avec celles extraites
manuellement des fruits. Afin de comprendre le devenir
de ces graines après leur dépôt, une étude de l’habitat où
Lemur News Vol. 15, 2010
Page 75
les fèces ont été déposées a été réalisée. Les résultats de
cette étude ont démontré que V.rubra a une frugivore élevée (86.1 %). Aussi, ces deux espèces participent activement à la dissémination des graines de la majorité des
espèces végétales du corridor, avec 16 graines par jour
disséminées par V. rubra représentées par 34 espèces végétales appartenant à 15 familles, et 10 graines par jour
pour E. albifrons réparties dans 8 familles avec 11 espèces.
De plus, après leur passage au niveau du tube digestif de
ces animaux, les graines sont viables (x = 107,283, ddl = 2,
p = 0,0001) et ont une germination plus élevée que les
graines témoin (x = 55,680, ddl = 1, p = 0,0001). Très peu
d’entre elles ont subi des dommages (seulement de 3,8 %
et 0,7 % respectivement pour les graines déféquées par V.
rubra et E. albifons). L’étude de l’habitat démontre une
réussite de germination malgré une forte pente.Ces deux
espèces de lémuriens sont donc d’importantes disséminatrices de graines de la forêt humide du corridor Ambatolaidama. Elles jouent un rôle important dans le maintien
de l’équilibre écologique et contribuent à la reforestation
du corridor.
Mots-clés: Varecia rubra, Eulemur albifrons, Primates, Régime alimentaire, Dispersion des graines, Parc National
Masoala, Corridor, Ambatolaidama, Madagascar.
which proposes that reproductive females form special
relationships with males to improve foraging success and
offset the energetic costs of reproduction.Data were collected on two small groups in Mahabo forest, on the southeastern coast of Madagascar. Analysis of social structure
data suggested central male structure when resources
were scarce and central female structure during the period of relative resource abundance. The resource defence
hypothesis was not supported by foraging data.
2
2
Razakanirina H. 2010. Suivi phénologique global et statut de
conservation de 4 espèces végétales (Strychnos decussata,
Diospyros ferrea,Gardenia decaryi et Capurodendron gracilifolium) consommées par Propithecus verreauxi coronatus dans
la forêt de Badrala (Antrema - Région Boeny). Mémoire
de DEA en Biologie et Ecologie Végétale, option Ecologie
végétale, Département de Biologie et Ecologie Végétale,
Faculté des Sciences, Université d’Antananarivo.
La Station Forestière à Usage Multiple d’Antrema constitue un des habitats de Propithecus verreauxi coronatus.Dans
cette région, ces Lémuriens sont vénérés comme étant
les représentants des ancêtres des "Sakalava". Cette culture leur offre donc un haut niveau de protection mais
est- ce que la forêt peut leur fournir la nourriture dont ils
ont besoin?
Des études sur la phénologie et une évaluation du statut
de conservation des quelques espèces consommées par
ce lémurien ont été réalisées dans la forêt sèche sur dune
de Badrala (partie Nord de la station),afin de faire ressortir les différents types phénologiques et la saisonnalité des
différentes phénophases des arbres de cette forêt. Trois
(3) plots de 2000 m ont été montés dans la forêt et dans
chaque plot, tous les arbres à DHP > $10 cm sont numérotés et des paniers collecteurs de litières sont installés
suivant un transect de 200 m. La phénologie des arbres a
été suivie pendant une année grâce à des observations directes de chaque individu et à l’analyse des litières qui
sont collectées tous les 15 jours. La période de floraison
maximale des espèces se produit au début de la saison humide, avant l’apparition des feuilles et la défeuillaison est
assez importante au milieu de la saison sèche. Strychnos
decussata, Diospyros ferrea, Gardenia decaryi et Capurodendron gracilifolium sont classées en danger d’extinction
(EN). Ainsi, des mesures de conservation sont à entreprendre afin de protéger ces espèces et les habitats de ce
lémurien.
Mots-clés: Suivi phénologique, Statut de conservation,
Plantes consommées,Propithecus verreauxi coronatus,forêt
sèche, Badrala, Station Forestière à Usage Multiple d’Antrema, Madagascar.
2
Rued, A.C. 2009. Social structure and female foraging strategies in white-collared lemurs (Eulemur cinereiceps). M.A.
thesis, University of Calgary, Calgary, Alberta, Canada.
This thesis examines the nature of male-female affiliation
in Eulemur cinereiceps, specifically whether it consists of
special relationships or a central male social structure. A
special relationship includes an unrelated male and female
adult who preferentially associate and affiliate with each
other over all other individuals within the group. I also
examine the flexibility of female foraging strategies in
response to changes in resource availability and energy
requirements. I tested the resource defence hypothesis,
Solomon,S.K.2010.Living on the edge:a preliminary dry season study of crowned lemur (Eulemur coronatus, Gray
1842) and Sanford’s lemur (E.sanfordi,Archbold 1932),responses to anthropogenic habitat changes in northern
Madagascar. M.A., Anthropology (Environment & Sustainability),University of Western Ontario,London,Canada.
Habitat fragmentation through anthropogenic disturbance is a significant threat to primates in all biogeographic
areas. Recent research has shown that primates have
non-patterned responses to this disturbance and that general models of changing primate behaviour are not effective conservation tools. Previous research on primates in
fragments is concentrated in the Neotropics demonstrating a need to investigate species-specific responses in other areas of the world. This study examined two sympatric lemur species, the crowned lemur (Eulemur coronatus)
and Sanford’s brown lemur (Eulemur sanfordi) and their responses to anthropogenic habitat fragmentation in northern Madagascar. Although habitat generalists, Sanford’s
lemur was extirpated at the study site while crowned lemur density was low but viable; they were restricted to
forest fragments on the periphery and top of limestone
massifs. Conservation initiatives in these fragments are
reliant on preserving fruit trees located in the remaining
forest flatlands and the commitment of a community conservation group.
Key words: Northern Madagascar, Crowned lemur, Sanford’s brown lemur,Forest fragmentation,Edge effects,Lemur density, Community conservation, Dry season, Deciduous forest.
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Schwitzeretal.,2010;KaumannsandSchwitzer,2001).Thereferencelistshouldbearrangedalphabeticallybyfirstauthor'ssurname.
Examplesaregivenbelow.
Journalarticle
Ranaivoarisoa,J.F.;Ramanamahefa,R.;Louis,Jr.,E.E.;Brenneman,R.A.2006.RangeextensionofPerrier’ssifaka,Propithecusperrieri,in
theAndrafiamenaClassifiedForest.LemurNews11:17-21.
Bookchapter
Ganzhorn,J.U.1994.Leslémuriens.Pp.70-72.In:S.M.Goodman;O.Langrand(eds.).Inventairebiologique;ForêtdeZombitse.
RecherchespourleDéveloppement,SérieSciencesBiologiques,n°Spécial.Centred’InformationetdeDocumentationScientifique
etTechnique,Antananarivo,Madagascar.
Book
Mittermeier,R.A.;Konstant,W.R.;Hawkins,A.F.;Louis,E.E.;Langrand,O.;Ratsimbazafy,H.J.;Rasoloarison,M.R.;Ganzhorn,J.U.;
Rajaobelina,S.;Tattersall,I.;Meyers,D.M.2006.LemursofMadagascar.Secondedition.ConservationInternational,Washington,DC,
USA.
Thesis
Freed,B.Z.1996.Co-occurrenceamongcrownedlemurs
(Lemurcoronatus)andSanford’slemur(Lemurfulvussanfordi)
ofMadagascar.Ph.D.thesis,WashingtonUniversity,St.Louis,USA.
Website
IUCN.2008.IUCNRedListofThreatenedSpecies.
<www.iucnredlist.org>.Downloadedon21April2009.
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DrawingbyStephenD.Nash
Lemur News Vol. 15, 2010
ISSN1608-1439
Table of contents
Editorial.................................................................................1
Articles
Feature:Madagascar’sEnvironmentalCrisis
Diurnallemurdensityinthenationalpark
parcelIvontakaNord,UNESCOBiosphere
ReserveofMananara-Nord
MartaPolaskyLyons..............................................................29
Madagascar’sillegalloggingcrisis:Anupdate
anddiscussionofpossiblesolutions
ErikR.Patel...............................................................................2
Ongoingthreatstolemursandtheirhabitat
insidetheSahamalaza-IlesRadamaNational
Park
MelanieSeiler,GuyH.Randriatahina,
ChristophSchwitzer.................................................................7
NewsandAnnouncements..........................................9
ShortCommunications
Preliminaryconservationstatusassessmentfor
theDataDeficientnortherngiantmouselemur
Mirzazaza
EvaJohannaRode,K.Anne-IsolaNekaris,
ChristophSchwitzer...............................................................11
Anobservationofthehairy-eareddwarflemur,
Allocebustrichotis,intheLakatoregion,eastern
Madagascar
ErwanLagadec,StevenM.Goodman..................................12
Whenbiglemursswallowupsmallones:
Coquerel’sdwarflemurasapredatorofgrey
mouselemursandendemicrodents
SusanneSchliehe-Diecks,MatthiasMarkolf,
EliseHuchard.........................................................................13
Collectivemobbingofaboabyagroupof
red-frontedlemurs(Eulemurfulvusrufus)
LennartPyritz,TianasoaAndrianjanahary..........................14
Responseoftwonocturnallemurs(Microcebus
murinusandLepilemurleucopus)toapotential
boiidae(Sanziniamadagascariensis)predator
KristaFish...............................................................................16
EffectivepredationdefenceinCheirogaleus
medius
KathrinH.Dausmann...........................................................18
LepilemurfeedingobservationsfromNorthern
Madagascar
AndrewJ.Lowin......................................................................20
Hypothesesonecologicalinteractionsbetween
theaye-aye(Daubentoniamadagascariensis)
andmicrohylidfrogsofthegenusPlatypelisin
Tsaratananabambooforest
AndolalaoRakotoarison,SoloheryA.Rasamison,
EmileRajeriarison,DavidR.Vieites,MiguelVences............21
Discoveryofcrownedsifaka(Propithecus
coronatus)inDabolava,Miandrivazo,Menabe
Region
JosiaRazafindramananaandRijaRasamimanana............23
InferencesaboutthedistantpastinMadagascar
ElwynL.Simons......................................................................25
HusbandryguidelinesformouselemursatParis
Zoo
DelphineRoullet....................................................................27
DistributionofProlemursimusnorthofthe
Mangoro-NosivoloRiver-howfarnorthdowe
reallyhavetolook?
RainerDolch,ErikR.Patel,JonahH.Ratsimbazafy,
ChristopherD.Golden,TianasoaRatolojanahary,
JeanRafalimandimby,JonathanL.Fiely................................32
Enquêtepréliminairedeladistributiondes
lémuriensdebamboudansetautourdu
CorridorforestierFandriana-Vondrozo,
Madagascar
AndryRajaonson,MaherisoaRatolojanahary,
JonahRatsimbazafy,AnnaFeistner,TonyKing....................34
Effectofredruffedlemurgutpassageonthe
germinationofnativerainforestplantspecies
OnjaH.Razafindratsima,EmilienneRazafimahatratra.....39
Feedingecologyofthecrownedsifaka
(Propithecuscoronatus)inacoastaldryforest
innorthwestMadagascar(SFUM,Antrema)
ClairePichon,RivoRamanamisata,LaurentTarnaud,
FrançoiseBayart,AnnetteHladik,ClaudeMarcel
Hladik,BrunoSimmen..........................................................42
Effetdeladégradationdel'habitatsurla
consommationalimentaired'Eulemur
rubriventerdansdeuxsites:Talatakelyet
Vatoharanana,duParcNationaldeRanomafana
LaingoniainaH.Rakotonirina,GermainJ.Spiral,
JonahH.Ratsimbazafy,SoanorolalaoRavelonjanahary,
RaharizelinaRalaiarison,StaceyTecot,AlexHall,
TriciaCalhoon,GisèleR.Randria..........................................47
Observationsofterrestriallatrinebehaviourby
thesoutherngentlelemurHapalemur
meridionalisintheMandenalittoralforest,
southeastMadagascar
TimothyM.Eppley,GiuseppeDonati....................................51
Conservationdeslémuriensvialaprotectionde
leurshabitatsetledéveloppementcommunautaire
danslescorridorsdeBetaolanaetTsaratananaBetaolana,régiondeSAVA
LalaRazafyFara,IarilantoAndriamarosolo.........................54
GeneticdiversityintenIndri(Indriindri)
populationscomparedtootherlemurspecies
JohnZaonarivelo,RickBrenneman,Rambinintsoa
Andriantompohavana,EdwardE.Louis,Jr............................59
Verreaux’ssifakafurconditioninthespinyforest
ofsouthernAndroy
IvanNorscia,JeanLambotsimihampy,ElisabettaPalagi.....64
RediscoveryofSibree’sdwarflemurinthe
fragmentedforestsofTsinjoarivo,central-eastern
Madagascar
MarinaB.Blanco....................................................................67
FundingandTraining.....................................................69
RecentPublications........................................................70
ThesesCompleted..........................................................71
Melanie Seiler
Guy Randriatahina