Open Journal of Animal Sciences, 2020, 10, 64-133
https://www.scirp.org/journal/ojas
ISSN Online: 2161-7627
ISSN Print: 2161-7597
Wild Mammal Translocations: A Public Health
Concern
João Carlos Araujo Carreira1*, Cecilia Bueno2, Alba Valeria Machado da Silva3
1
Public Health Researcher/IOC, Fiocruz, Brazil
Universidade Veiga de Almeida, Rio de Janeiro, Brazil
3
Rio de Janeiro, Brazil
2
How to cite this paper: Carreira, J.C.A.,
Bueno, C. and da Silva, A.V.M. (2020) Wild
Mammal Translocations: A Public Health
Concern. Open Journal of Animal Sciences,
10, 64-133.
https://doi.org/10.4236/ojas.2020.101006
Received: September 23, 2019
Accepted: December 28, 2019
Published: December 31, 2019
Copyright © 2020 by author(s) and
Scientific Research Publishing Inc.
This work is licensed under the Creative
Commons Attribution International
License (CC BY 4.0).
http://creativecommons.org/licenses/by/4.0/
Open Access
Abstract
With regard to wildlife translocations and the assessment of potential risk of
disease transmission, several advances have been made in conservative
projects. However, other factors like the large number of species received at
screening centers from different locations, rescued after being hit by vehicles,
taken by the public or confiscated from illegal trade by the authorities, have
increased the risk of spreading, emergence or reemergence of zoonosis. Besides the notorious importance of the procedure improvement for managing
wildlife, the access to as much as possible information about the occurrence
of potential infections on each particular species can be a tool of great value
for mitigating the disease risk. In the present paper, it was showed the evolution of processes for wildlife translocations mostly related to mammals, we
also discussed some aspects related to sylvatic animals as reservoir host of
zoonosis and finally were presented several tables recording numerous
mammals hosts and their respective parasitic protozoa.
Keywords
Mammals, Wildlife Translocations, Zoonosis, Parasitic Protozoa
1. Introduction
Zoonosis can be defined as diseases or infections that are naturally transmitted
between animals and humans. The diverse kinds of potential infectious organisms encompassing viruses, fungi, bacteria as well as parasites they can produce
zoonotic infections and seventy-five per cent of the emerging human diseases
were determined as zoonosis [1].
Consequently, it should be considered as a significant warning for global pubDOI: 10.4236/ojas.2020.101006 Dec. 31, 2019
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lic health.
Among the causal factors for the emerging or re-emerging of zoonosis is the
increase in human-assisted movement of animals and anthropogenic changes
that alter the distribution of wild hosts and vectors promoting the spreading of
infectious agents.
The knowledge about the jeopardy of microorganism transmission involving
the wildlife relocation has been progressing substantially since the last century.
Unfortunately, in spite of the great advancement in the procedures to avoid
that kind of microorganisms, transmission, the achievement of effective measures in many countries is still incipient and the lack of information about those
infectious agents and their wild hosts still represents a gap.
In the present paper, we presented firstly a review from bibliography related
to disease risk and wildlife translocations, principally related to wild mammals.
After, it was discussed some results from the literature and finally, based on
the molecular classification of placentals proposed by Tarver et al. [2], a table
was presented showing infection records of several wild host mammal species
and their respective parasitic protozoa, most of them with medico-veterinary
importance.
One of the first reports about the risk of microorganism transmission involving the wildlife relocation was presented by Jirovec [3].
He showed that an avirulent microorganism that causes imperceptible infection in wild animal hosts could sometimes become virulent after the passage
through a new host in a new environment.
The author mentioned one case of rabbits (Lepus cuniculus), translocated
from England to South Africa. Some of the animals in England (5.7%) were infected by an avirulent strain of Toxoplasma. After arriving in South Africa, the
parasite infected local rats (Rattus natalensis) and in these new hosts, a virulent
form of the parasite selected.
Later, Jacobson et al. [4], from the investigation on the epizootiology of an
outbreak of cerebrospinal nematodiasis in cottontail rabbits and woodchucks in
USA, triggered by the introduction of racoons.
They concluded that because of the potential consequences of this disease in
small mammal populations, the raccoons should be examined, prior to relocation.
Moreover, the authors underlined the public health aspect, of potential parasite translocation through those animals.
May and Lyles [5] analyzed a reintroduction program of captive tamarins in
the native habitat in Poço das Antas Biological Reserve, Brazil, according to the
authors after about two years, out of the 26 animals only five were alive with
diseases as the leading cause of death.
Nettles [6] introduced the term “biological package” referring that a translocated animal is not a representative of a single species, but it is considerably a set
of viruses, bacteria, protozoa, helminths and arthropods.
Rosatte and Maclnnes [7] studied one group of raccoons from Toronto (CA),
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translocated to either rural areas or a town.
They argued as not recommending the relocation of those animals, because
their high exploratory movements and a potential risk for disease transmission.
Griffith et al. [8] presented a review of terrestrial vertebrate animals from 1973
to 1986, in Australia, Canada, New Zealand and the USA, analyzing the geographical distribution and relative frequency of translocations methods that had
disease transmission implications.
They related that translocations probably exceed 700 per year and more than
50% of assessed agencies have translocated some species each year.
On average, 26% were captive-reared animals, 29 were released to areas on the
periphery or outside of the species ranges.
Only 32% provided post-release follow up and in 24%, there were no checkups
carried out by professionals related to the occurrence of parasite infections, diseases or any kind of wound.
The authors stated that a suitable valuation on the effect of disease on translocation success would require multivariate analyses.
Viggers et al. [9] discussed the importance of disease in reintroduction programs. They pointed out that disease could play a significant role in the reduction or extinction of small isolated animal populations.
Furthermore, a remaining wild population could be strongly reduced by a
disease co-introduced with relocated animals. Conversely, endemic diseases in
wild animal populations could be deadly for those immunologically naive reintroduced individuals.
Munson and Cook [10] indicated the necessity of conservation programs for
captive breeding and reintroducing of threatened and endangered species, for
assessing the risk of introducing infectious disease into or acquiring diseases
from the reintroduction environment.
The authors pointed that risk evaluation was seriously disadvantaged by insufficient knowledge about the disease. Thus, it was suggested that integrating
information from diverse sources would be greatly simplified by establishing
standards for data collection. Guideline instructions for monitoring and investigating the infectious diseases would provide essential information for a disease
database.
It was also proposed, the creation of a method for categorizing infectious diseases by degree of threat to a species or environment, for the limited resources in
support of disease investigations being appropriately allocated. Furthermore,
these methods would meaningfully increase the understanding of disease epidemiology in nondomestic species.
Woodford and Rossiter [11] described some subjects of the disease risks attending wildlife translocation projects they also suggested the development of
systematic procedures to reduce these risks both at the source of the founder
animals and at the proposed release site.
The same authors in 1994, working in the above-mentioned projects, they
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presented one of the first attempts to establish guidelines for assessing disease
risk in wildlife translocations.
The following topics were proposed:
1) Types of disease risk.
2) Diseases introduced by translocated animals.
3) Diseases encountered by translocated animals at the release site.
4) Minimizing the risks.
5) Interpretation of survey and screening results.
6) Vaccination of founders.
7) Post-release health monitoring.
8) Disease transmission hazards with cryopreserved germplasm.
In our view, the cryopreservation of microorganism samples corresponds to a
very important measure, because isolate and preserve biological samples from
sylvatic animals is fundamental for studies in diverse approaches like biology,
pathology, genetics, proteomics and many others.
These samples could be fundamental permitting identify, characterize and
studding potential pathogenic organisms, for the animals but also with potential
risk to public health.
Mihok et al. [12], recorded some health consequences related to the translocations of endangered species in Africa, specifically associated with cases of Try-
panosoma infections in rhinoceros.
The survey included both, black (Diceros bicornis) and white (Ceratotherium
simum) rhinoceros that had lived before in areas free from T. brucei and were
translocated to low lands characteristically associated to the occurrence of tsetse
flies, the insect vectors of different species of trypanosomes.
In both mammal species there were deaths because the parasite infections and
although previous examinations from blood smears revealed low infections incidence, posterior serological tests demonstrated that most animals presented
subpatent infections.
Particularly concerning to the white rhinoceros the authors concluded that
this species would be a good sylvatic host to T. brucei, likewise it was highlighted
the potential serious consequences for management plans involving this species
into or out the areas with human sleeping sickness and the possibility of spreading the disease to new areas.
Karesh and Cook [13] pondered about the importance of the incorporation of
veterinary medicine on a multidisciplinary approach for assessment the elaboration and execution of conservation projects.
Besides their expertise for immobilizing animals, they could contribute on the
follow up the health of sylvatic animals, as well as in the training of others for
working and supervising wildlife.
It was stated that, wildlife health care should include six steps.
The first step proposed, was identifying critical health-related factors that
could affect wildlife populations, recognizing the role of diseases in the dynamics
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of those populations.
According the authors, the host-parasite relationship should be considered as
very complex condition, including multivariate factors like bacterial, viral and
fungal infections besides nutritional, metabolic, genetic and toxicological problems.
In function of that, wide-ranging health surveys comprising all those factors
should be implemented for most threatened and endangered species and those
studies should include even probably involved sympatric species.
Like other authors have already proposed, that survey should be carried out
for a multidisciplinary team for assembling overall health profiles related to
wildlife populations.
The second step proposed by Karesh and Cook [13], was the monitoring the
health status of wildlife populations over time, because those information could
be employed on future conservation strategies.
Moreover, the following premises were proposed in respect to programs of
disease-monitoring:
1) Function as signs of environmental degradation showing potential threats
and alterations in the health of populations, because they normally precede the
variations in population size or structure.
2) Provide qualitative and quantitative data for population viability analysis
(PVA) programs. Taking into account that the inclusion of the health was supposed to be fundamental for a comprehensive assessment of population viability.
3) Support on the definition of the aptness of wildlife populations for translocation, restocking, reintroduction or restoration ecology projects. By the evaluation of area or the animals to be introduced, in function of the diseases they
could be harboring and for their immunity to agents to which they could be exposed during the process.
Both, the animals as well as the selected areas for receiving them should be
evaluated for the occurrence of diseases or the risk of new pathogens introduction.
The other promises in summary comprised of: a) Crisis intervention, b) Animal handling and welfare and c) New technologies. Concerning respectively to,
diagnosis during a health crisis or wildlife die off; handling of wildlife, specifying
equipment; and practices for reducing possible animal wounds.
In conclusion, the authors indicated the veterinary sciences could supply conservation programs in respect to the several points above mentioned and their
function in conservation efforts would need to increase for encountering the requirements of governmental and nongovernmental programs around the world.
Cunninghan [14] discussed the possible adverse effects on the evolution of
ecosystems because disease transmission resulting from wildlife translocations.
Revising the literature, he referred several authors to highlight that certain
diseases can cause on the fauna severe negative effects such as, increased of susceptibility to predation, lower reproductive capacity and death.
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It was also recorded the great effect of diseases on individual fitness, considered an important factor in the maintenance of biodiversity. Those effects
could also present more complex situation, like diseases that cause a decline on
the population of a determined species that is a staple prey of some predator,
consequently it may trigger a selective pressure causing reductions on the predator number.
On the other wise, the author remembered that diseases are important to the
maintenance of biodiversity, because it influences the species complement within established ecosystems.
Indeed, Cunninghan [14] stressed that although the mechanisms involving
parasite infections on community structures within ecosystems were poorly understood, it should not be overlooked when wildlife translocation programs are
developed.
Another important question raised by Cunninghan [14] was about keeping
time of sylvatic animals in captivity.
He suggested that animals in captivity would be at risk of infection with parasites that are foreign respectively to, a particular species, the area of origin, the
area where will be introduced or a combination of the three. Besides, the risks of
outbreaks of disease increase while an animal has been kept in captivity and further away from its natural habitat.
For reducing the risks, the author suggested the adopting of very important
measures, for caught animals as well as whose progeny that would be further
reintroduced:
1) The animals must be maintained in captivity as near as possible to the site
of capture.
2) The animals should be held captive for as short a time as possible.
3) Avoid direct or indirect contacts between the animals from different
sources or species.
4) The animals should be Kept and managed under hygienic conditions to
minimize the risk of parasites being passed from the keepers to them.
5) Control of foodstuff for avoiding transmission of parasites to the animals.
The author reasoned it would seem desirable for animals in captivity to be
kept parasite-free, but the parasites they could harbor were those they would be
exposed to in their natural territory.
The maintenance of such parasite burden and consequently the continuation
of genetic and other adaptations to these parasites could be an advantage for
ensuring the survival of animals once they are reintroduced to the wild.
It also could allow the conserving the parasites biodiversity, in spite of the necessity for controlling the infections to avoid probable deleterious effects produced by captivity.
Completing, Cunninghan [14] presented five more points: 1) Specimens with
no registered disease, does not mean that they are not susceptible to the disease.
2) Animals of any age can carry, or be susceptible to pathogenic organisms. 3)
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Clinically healthy animals should not be considered as free of parasites; thus,
equal attention and prerequisites should be requested to all animals in each
stages of the life; but the methods applied for parasites detection would depend
on the species, stage of the life cycle, as well as the methodology of the reintroduction program. 4) Translocation of animals to areas lacking of related species
would reduce the risk of interspecific transmission of the disease. 5) If evaluation
and reduction of risk would be not possible, the program should only be continued in cases that the conservation risk for not having been made was greater
in order to avoid the introduction of parasites into new areas.
Likewise, it is accepted that the introduction of other exotic species, usually
into new habitats, should be avoided.
Among the conclusions, the author indicated that previously of making a
wildlife translocation the disease risks should be correctly evaluated and preventive measures should be taken to reduce the risks.
In 1998 The International Union for Conservation of Nature and Natural Resources (IUCN) [15], published one of their first comprehensive guidelines that
were considered as necessary to make available a more comprehensive coverage
of the several factors related to re-introduction.
The background for that guidelines, was relating to policies directed to biodiversity conservation and sustainable management of natural resources.
It was highlighted the procedures should represent useful tools for re-introduction
programs and do not a rigid code of conduct.
Among diverse themes mentioned, the restoring of ecosystems regarding to
re-introduction of species was discussed and considered a very common practice
around the world. Thus, the IUCN Species Survival Commission’s Re-introduction
Specialist Group developed those guidelines.
They were based on reviews and case-histories and were thought that could
institute more thoroughness into the elaboration of concepts, design, feasibility
and in implementation of re-introductions.
The definition of the terms “re-introduction”, “translocation”, “reinforcement/supplementation” and “conservation/benign introductions” were presented.
The aims and objectives were correspondingly related to the long-term survival or re-establishing of important species, for preserving and/or restoration of
natural biodiversity, producing long-term economic benefits and stimulating
conservation consciousness.
It was remembered the need of a multidisciplinary approach to support
re-introduction projects including governmental natural resource management
agencies, non-governmental organizations, funding bodies; universities; veterinary institutions; zoos, etc.
Some statements related to re-introduction projects, were presented including:
1) pre-project activities, 2) planning, preparation and release stages and 3)
post-release activities. In the two firsts, was related the concerning about the acDOI: 10.4236/ojas.2020.101006
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quisition and/or spreading of diseases.
Composing Pre-project activities, in the feasibility study and background research, it was suggested the application of detailed surveys on the status and biology of wild animal populations. Disease was included among several factors to
identify the critical needs of the species like, habitat preferences, intraspecific
variation, home range size, shelter, feeding behavior, predators etc.
In the planning, preparation and release stages, the choice of release site and
type, it should be within the historic range of the species and for a re-introduction,
no remnant population could exist to prevent disease spreading, social disruption and introduction of alien genes.
On the evaluation of re-introduction site, several actions were suggested for
the detection, diminution or removal, of causes of population decline such as
diseases, over-hunting, over-collection, pollution, poisoning, competition with
or predation by introduced species and habitat loss.
The availability of suitable release stock for minimizing infectious disease risk
should be implemented, seeing that grave diseases could occur during shipment.
When considered wild-caught release stock, attention to ensuring that animals
were non-infected with contagious pathogens and parasites before shipment and
not be exposed to vectors of disease agents which may be present at the release
site to which they would have no acquired immunity.
The immunization, against diseases of wild or domestic animals of the release
site, should be done during “Preparation Stage” at enough time for the immunity
development.
Woodford [16] was one the first authors that compiled data concerning quarantine and health screening procedures for wildlife prior to translocation and
release into the wild. It was also suggested treatment and immunization protocols for mammals, birds, reptiles, amphibians and fish.
The author reinforces the idea that translocation from one wild population, or
introduction of captive-borne animals in the wild as well as the return of convalesced animals after some time in captivity, should be taken into account as a
risk of disease transfer.
It was reminded the concept proposed by Nettles [6] of biological package besides aiming the possibility of certain organisms become pathogenic under host
stressful situations, affecting as the released specimen as well as the other animals but principally putting human population under risk.
Woodford [16] presented very useful information related to the measures
for caught animals as well as whose progeny that would be further reintroduced, including several animal groups from fish to Primates as follows: Artiodactyla, Perissodactlya, Primates, Carnivora, marine Mammalia, Rodentia,
Lagomorpha, Marsupialia, Monotremata, Chiroptera, Birds, Reptilia, Amphibia and Piscidae.
Corn and Nettles [17] presented health protocol for translocation of free-ranging
elk (Cervus elaphus).
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The protocol was based on five components:
1) Evaluation of the health status of source populations.
2) Quarantines.
3) Physical examination.
4) Restrictions on translocation.
5) Prophylactic treatment.
They suggested that wildlife managers should assess the positive and negative
elements of translocation before initiate a restoration plan.
A selected set of epidemiologic factors related to infectious agents and ectoparasites were evaluated through a qualitative analysis for determining its potential to be introduced and to become established.
Infectious agents and ectoparasites of unknown risks were classified as: Anap-
lasma marginale, Anaplasma ovis, Mycobacterium paratuberculosis, Pasteurella
multocida serotype 3, Elaphostrongylus cervi, Dicrocoelium dendriticum, Fascioloides magna, Echinococcus granulosus, Dermacentor albipictus, and Otobius
megnini.
Of high risk were: Chronic wasting disease, Brucella abortus, Mycobacterium
bovis, Parelaphostrongylus tenuis, Elaeophora schneideri, Babesia sp. and Dermacentor andersoni, Ixodes pacificus and Psoroptes sp.
Lafferty and Gerber [18] presented a very interesting approach concerning the
intersection of epidemiology and conservation theory.
They stated that infectious disease would be a concern for diverse features of
conservation biology such as, the determining threats species, estimating population viability, designing reserves, captive breeding, and recovery programs.
The authors showed some correlation between infectious diseases and population density, susceptibility and pathogen exposure.
Actually, infectious-disease transmission usually increases when the density of
the host species augment.
On the other hand, species with a decreasing number of individuals would be
more susceptible for host-specific infectious diseases. Nonetheless, conditions
like habitat fragmentation or captivity that cause in increased contact facilitate
disease spread among individuals even in a declining species.
It was also supposed, that there was no a linear correlation between the outcome of infectious diseases and pathology in individual hosts. So infectious
agents that kill fast their hosts, present a tendency to become locally extinct,
consequently organisms with intermediate pathogenicity would be responsible
for the highest negative effects on a host population density.
Several records of infectious diseases of hosts considered as of conservation
concern were tabulated for providing evidence that infectious agents could reduce population density or inhibit the species recovering.
Table 1 was based on the results of Lafferty and Gerber [18] where were included only the results related to mammals, recording the host, infectious agent,
source of the infection and consequences of the disease on the population.
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Table 1. Infectious diseases that have caused negative effects on mammal host species of conservation concern.
Host
Disease agent
Transmission
Origin
Consequences
Koala (Phascolarctos cinereus)
Chlamydia
STD
Native
Birth rate declined
Red squirrel (Sciurus vulgaris)
Parapoxvirus
Direct
Introduced grey squirrel
90% population reduction
wolf (Canis lupus)
Rabies
Direct
Arctic fox (Vulpes lagopus)
60% population reduction
African ungulates
Rinderpest
Direct
Domestic cattle
80% population reduction
Bighorn sheep (Ovis canadensis)
Scabies Psoroptes ovis
Cholera V. colarae
Direct
Arthropod
Domestic sheep
80% population reduction
Local extinction
Sea otter (Enhydralutrisnereis)
Acanthocephalan
Native birds
Trophic
Increased mortality
Allegheny wood rat
(Neotoma magister)
Larval migrans
Subsidized raccoons
Trophic
Local extinction
African lion (Panthera leo)
Canine distemper
Domestic dogs
Direct
33% reduction
African wild dog (Lycaon pictus)
.Canine distemper
Rabies
Domestic dogs/jackal
Direct
Local extinction
Black-footed ferret (Mustela nigripes)
Canine distemper
Live vaccine
Direct
90% reduction
Wolf (Canis lupus)
Parvovirus
Domestic dogs
Direct
Reduced recovery
Ethiopian wolf (Canis simensis)
Rabies
Domestic dogs
Direct
50% density
Koala (P.cinereus)
Chlamydia ssp
STD
Native
Birth rate declined
Red squirrel (S. vulgaris)
Parapoxvirus
Direct
Introduced grey squirrel
90% population reduction
wolf (C. lupus)
Rabies
Direct
Arctic fox (V. lagopus)
60% population reduction
African ungulates
Rinderpest
Direct
Domestic cattle
80% population reduction
Bighorn sheep (O. canadensis)
Scabies Psoroptes ovis
Direct
Arthropod
80% population reduction
Bighorn sheep (O.canadensis)
Cholera
Domestic sheep
Direct
Local extinction
Sea otter (E. nereis)
Acanthocephalan
Native birds
Trophic
Increased mortality
Subsidized raccoons
Trophic
Local extinction
Allegheny wood rat (N. magister)
Larva migrans
B. procyonis
African lion (P. leo)
Canine distemper
Morbillivirus
Domestic dogs
Direct
33% reduction
African wild dog (L. pictus)
Canine distemper
Morbillivirus
Domestic dogs/jackal
Direct
Local extinction
Black-footed ferret (M. nigripes)
Canine distemper
Morbillivirus
Live vaccine
Direct
90% reduction
Wolf (C. lupus)
Parvovirus
Domestic dogs
Direct
Reduced recovery
Ethiopian wolf (C. simensis)
Rabies
Domestic dogs
Direct
50% density
African wild dog (L.pictus)
Rabies
Domestic dogs/jackal
Direct
Local extinction
Based on the results of Lafferty K.D. and Gerber L.R. [18]. STD: sexually transmitted diseases.
In Conclusion, Lafferty and Gerber [18] emphasized the importance of making an interaction between conservation biology and epidemiology. It was suggested that probable important infectious diseases for threatened species could
be those with wide-ranging host species. Therefore disease investigation besides
crowding decrease, avoiding inbreeding and selection for susceptibility, they
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could support conservation biologists on the understanding of disease risks.
Gaydos and Gilardi [19], addressed disease risks when recovering species at
risk.
They maintained that diseases have great influences on free-ranging wildlife
populations, and could be especially important in the case of recovering species
at risk.
In the need of translocation or captive breeding, which could enhance the risk
of disease impacts, it was suggested a process comprised of steps for deal with
species at risk, summarized below:
1) Disease should be considered as a reason that could affect the success of
recovery efforts of a species.
2) Potential important diseases should be assessed.
3) The third step presented by the authors must be considered of great importance because highlighted the awareness regarding the risk of introducing
diseases when translocating or propagating species at risk in captivity. Besides, it
should be cogitated the probable existence of new diseases not yet recorded for
the species in question.
4) Treatment or vaccinations of individuals besides manipulating the pathogen or toxin, the population, the environment, and/or human activities, should
be considered accessible strategies for disease management.
5) Checking disease management strategies is important to assess effectiveness.
In conclusion, Gaydos and Gilardi [19] agreed that diseases are potential risk
to the continuing viability of recovery of threatened or endangered species.
Thus, it should be the first action, the prevention of disease-related problems.
They highlighted the necessity to continuous appraisal of disease risks and
impacts throughout the recovery process. Considering disease is one the main
ecological force, the detection and the diminishing of risks could be a significant
component for wildlife recovering.
Gerber et al. [20] argued about the exposing pathogens to a population and
the analysis of extinction risk, besides questioning if disease is simply one more
example of density dependence.
They pointed out as an important measure, the development of population
viability analyses (PVA) as a legal requirement in the United States and several
other countries, being mandatory the applying of PVA in any plan elaborated for
threatened and endangered species.
Nevertheless, regardless of the significance of the pathogens effects on the native populations, according to the authors insufficient attention was given to
host–pathogen dynamics concerning PVA.
They reviewed the relevance on the host-pathogen interaction on the extinction risk and estimated through PVA the potential impact of infectious diseases
on host population.
Furthermore, a density-dependent host-parasite stochastic model was created
to examine the consequences of disease on the preservation of endangered popDOI: 10.4236/ojas.2020.101006
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ulations.
It was also showed that the model developed converged on a Ricker model of
density dependence under a set of constraining suppositions, comprised a high
probability that epidemics would arrive and occur.
Note: The Ricker model, constitutes in a classic discrete population mathematical model which presents an expected number Nt+1 (or density) of individuals in generation t + 1 as a function of the number of individuals in the previous
generation.
Through that approach, they observed:
1) Distinctions between time series produced by disease and Ricker processes.
2) Probabilities of quasi-extinction for populations exposed to disease or
self-limitation.
3) A tendency in quasi-extinction chances estimated by density-independent
PVAs when populations undergone any type of density dependence.
Concerning the relationships among disease, PVA and dealing with endangered species, the authors proposed two hypothetical situations.
1) Disease more strongly increased variability in host abundance and, thus,
the probability of quasi-extinction than did self-limitation.
2) Estimates of quasi extinction were more often overly optimistic for populations experiencing disease than for those subject to self-limitation.
According the authors population density is an important factor for both PVA
and the host-pathogen theory.
A fundamental principle of epidemiology lies on the concept that the dispersion of an infectious disease within a population is a function of the density of
the susceptible as well as the infectious hosts.
Consequently, in the cases where infectious agents would be tolerable by the
host species, the pathogen effect on declining population would probably drop
with the host population decreasing.
In addition, the authors mentioned that a pathogen would be able to spread
when it was competent to be transmitted to another host before the current host
dies or eliminates the infection.
Thus, when parasites influences the host reproduction or mortality, or the
host is able to control the infection, the parasite population could eventually be
reduced because of the decrease on the number of susceptible hosts, eventually
stopping infection incidence.
Likewise, epidemiological models generally show the existence of a host density limit or native population size, restraining the parasite ability to infect new
hosts. It would imply that some concerned species should be less exposed to
host-specific disease.
In conclusion, the authors suggested that while the results of density-independent
PVAs would be relatively robust to some specific statements in relation to density dependence, they would be less consistent in relation to endangered populations susceptible to disease.
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Nevertheless, managing schedules for endangered species should involve
working with pathogens to decrease the threat of extinction and PVA including
disease explicitly would be indispensable for enhancing the population persistence.
Chipman et al. [21] in an article entitled “Downside Risk of Wildlife Translocation”, were among the first to indicate that in addition to translocations for
conservation purposes, various other forms and means of actions involving
translocations of wild mammals were increasing, producing negative consequences.
They reviewed and argued the challenges about restrictive normalizing for
translocations in the USA, targeting the animals originated from the public
nuisance wildlife control, and wildlife rehabilitators.
The authors questioned the practice of translocation in function of several
negative outcomes such as, stress and death of relocated animals besides effects
on resident fauna, conflicts with human interests and diseases spreading.
In addition it was highlighted that some types of translocations practices
would make vulnerable the control or eradication of important wildlife diseases
in North America, like the rabies in raccoons, coyotes, and foxes.
The different types of wildlife translocation described, included:
1) Unintentional:
Where animals that feed on human-generated waste could be transported inadvertently in garbage trucks from city to city or interstate.
For an example of unintentional translocation, it was referred the spreading of
an enzootic raccoon variant of the rabies virus covering several states from
United States caused by garbage relocation.
2) Interstate to supplement hunting:
Practiced by private hunt clubs of the United States that had been traditionally
imported and released mesocarnivores coyote (Canis latrans), red fox (Vulpes
vulpes), gray fox (Urocyon cinereoargenteus) and raccoons to enhance hunting
opportunities.
As an example, cases of raccoon rabies enzootic were mentioned relating it
spreading from North America north and southern portions of Ontario, reaching Quebec and New Brunswick, Canada.
In addition another case related to the translocation of coyotes from Texas to
Florida for the same reason, could have resulted in a substantial geographic
spread of a canine variant rabies.
3) By the public:
It was related that despite of the especially scarce information about the public
handle wildlife without professional assistance.
It was mentioned a study carried out in 1990-91 that observed about 25% of
the asked people had solved nuisance wildlife problems by themselves being 26%
through live traps.
In addition, an informal inspection in the United States during 2004 and 2007
involving the cage trap market, it have showed a sales increasing from 10% DOI: 10.4236/ojas.2020.101006
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100% in five years.
4) By nuisance control operators:
Considering the United States translocation have been commonly enjoyed to
the control of both pest and nuisance wildlife.
According to the authors, this type of industry had grown substantially since
the 1990s, accounting for most translocations of mesocarnivores in the country.
Table 2 was based on the results of two tables that were presented showing
the top ten animals treated by Nuisance Wildlife Control Operators in Connecticut and New York respectively in 2000 and 2001-2002. Only mammalian species
were included but even so, it shows how impacting that kind of translocation
can be.
5) By rehabilitators:
The rehabilitators or custodians are unpaid authorized helpers who assist injured animals for further release after their recovery.
Although the effect of this practice on populations is undetermined, it could
result in the release of animals in regions other than those in which they were
rescued.
Besides, the effect of the release of animals after maintenance for several
weeks in captivity could be comparable to the geographical translocation, even if
the release had been made in the same place they were caught.
In relation to that topic number five, we presented Table 3 that was based on
the results of Chipman et al. [21] and presents a list of the mammal species handled by Wildlife Rehabilitators in Connecticut in 2000, or by Nuisance Wildlife
Control Operators in New York, October 200 I-September 2002 with their respective number of specimens.
Table 2. Mammals moved by Nuisance Wildlife Control Operators in Connecticut in
2000 as well as handled by Nuisance Wildlife Control Operators in New York, October
200 I-September 2002. Based on the results of Chipman R. et al. (2008) [21].
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Rank
Animals
Number of animals
1
Squirrel (“other”) (Rodentia spp.)
4.569
2
Skunk (Mephitis mephitis)
2.297
3
Raccoon (Procyon lotor)
1.864
4
Woodchuck (Marmota monax)
1.217
5
Bats (Chiroptera spp.)
924
6
Opossum (Didelphis virginiana)
507
7
Moles (Insectivora spp.)
165
8
Chipmunk (Tamias striatus)
68
9
Feral cat (Felis catus)
64
10
Gray fox (Urocyon cinereoargenteus)
24
11
Coyote (Canis latrans)
22
12
Red fox (Vulpes vulpes)
7
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Table 3. Mammals species handled by Wildlife Rehabilitators in Connecticut in 2000, or
Nuisance Wildlife Control Operators in New York, October 2001-September 2002 and
the respective numbers of specimens.
Order
Animals
Number of animals
1
Squirrel (Rodentia spp.)
3.298
2
Rabbits
2.628
3
Opossum (Didelphis virginiana)
1.005
4
Raccoon (Procyon lotor)
602
5
White-tailed deer (Odocoileus virginianus)
342
6
Skunk (Mephitis mephitis)
167
7
Red fox (Vulpes vulpes)
59
8
Gray fox (Urocyon cinereoargenteus)
32
9
Coyote (Canis latrans)
10
Based on the results of Chipman R. et al. [21].
In conclusion, the authors indicated the great importance of Wildlife to the
United States as resource and highlighted that the majority of translocated animals by people or public agents were because human-wildlife worries in urban
and suburban habitats.
In function of anthropic action, the augmented accessibility of foodstuff and
shelter would cause the increasing of certain animal species populations in those
areas with high demographic density, aggravating nuisance wildlife problems
and resulting in translocations.
Finally, it was suggested that because the risk of spreading diseases like rabies,
chronic wasting disease, West Nile virus, and avian influenza, the euthanasia of
nuisance animals instead of translocation would be an important alternative for
protecting people, endangered species or pets as well as additional problems for
homeowners neighboring the release places.
Emslie et al. [22] presented the First Edition of Guidelines for the in situ
Re-introduction and Translocation of African and Asian Rhinoceros.
The scope of the guidelines was focused on translocations for conservation
and rescue of rhinoceros species. The global objectives were growth and lifelong
viability of those animals.
The guidelines were organized sequentially in four sections.
In the Section 1, was presented several points related to a pre-translocation
phase.
So during the Pre-translocation, the actions that should be progressed included,
Planning and Management, Biological and Socio-Economic and Legal engagement. Encompassing the general viability and assessment, plans for promoting source populations growth, selection of donor and recipient areas as well
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ments, translocation, mortality risk, veterinary cares, socio-political considerations, costing etc.
Section 2 considered the execution of the translocation including, logistical
and operational aspects of the capture, veterinary monitoring equipment for the
captures and transportation, etc.
Section 3, the post-release period involved, intensive post-release follow up,
veterinary care, continuing protection, monitoring and supervision, etc.
Finally, in Section 4 that would comprise an inventory of the mistakes and information acquired from previous translocations.
In addition, two annexes were also presented related to protocols for basic
pre-reintroduction/translocation health screening and prophylaxis as well as the
veterinary role in the investigation and post mortem procedures.
Considering the problem related to the disease risk and translocations, the
authors stated the importance of veterinary knowledge for the planning and implementation of captures and translocations.
It was pointed out that the risks associated with transmission of infectious
agents due to translocations existed and the health of the animals should be a
priority.
Among the few available studies showing the risk of trypanosome infections
on the rhinoceros from Africa, some were coincidently performed during translocations. Nevertheless, it was assumed that death risk would always be present
nonetheless; it could be reduced using applicable procedures, medicines and
knowledge.
The use of translocation could amplify population growth rates, maintaining
long-term genetic conservation, increase range and number of populations. It
could also have “strategic advantages”, like expanding the capability of the wildlife populations to persist on natural disasters such as a Tsunami, disease etc. as
well as avoiding subspecies extinction.
In the topic, identification of recipient areas as well as the dissimilarities in the
conditions of donor and recipient places. It was stated that black rhino would
apparently present a certain trypano-tolerance, nevertheless could develop disease under stress and/or immunosuppression conditions. It also could occur
when they were precipitously exposed to infected vectors after they had been
living in areas free of the parasite for long time.
According to the authors, regardless of the origin of the animals, they could
adapt in a few weeks and show resistance to infection. This would be achieved by
controlling the level of the host’s exposure to the vector. Initially they should be
exposed to low numbers of fly vectors and they would be never be introduced in
areas with a high density of glossinid flies.
Based on the occurrence of differences in the susceptibility to Trypanosoma
brucei infections observed in populations of white rhinoceros living in two distinct geographical areas of Africa, was suggested that these species would tend to
adapt to subpopulations of the parasite where they had been living together for
some time.
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Conversely, it was highlighted that there was no indication that reducing the
infection challenge would induce resistance. Besides it was also mentioned a case
of translocated animals that had died because Trypanosoma infections, even after months of previous controlled exposure.
In the topic concerning wild vs. captive or semi-captive breeding, based on
previous studies and on some data describing problems that occurred in intensive breeding programs for captive or semi-captive rhinos in Africa and the information that wild populations were more successful and less expensive, principally for Asian species.
It was proposed the fence using and protection of a suitable area that would
promote better growth rate with possible lower cost. Disease risks should be
considered on a case by case.
Some animals that intermittently leaved the protected areas invading adjacent
farmland named stray-rhinos, they were common in the South Asia and consequently were potential targets for translocations and reintroduction into new
areas. The authors showed the high risk of those animals carrying diseases, because their behavior frequent stress situations increased the risk.
In veterinary considerations, they were stated few general points around potential problems related health and disease.
It was considered that the knowledge on horse veterinary proceedings could
mean as opportunities for the understanding of rhino diseases because their
close relationship in the physiology, parasites, disease, response to drugs among
others.
The term “biological package” introduced by Nettles in 1988 was remembered, so it was considered the translocation of an animal could be a movement
of biological elements including endo- and ectoparasites possibly dangerous to
other rhino populations and herbivores.
The problems related to the possibility of introducing microorganisms in the
releasing site, as well as the risks of introduced animals acquire infections by local pathogens were reminded.
The use of healthy animals was pointed as prerequisite for a successful
re-introduction, because they would have more possibilities of surviving in cases
of stress, besides supposedly being more capable to adapt to their new habitat.
The necessity of qualified veterinarian assessing the translocation of captive or
wild animals was stated for an effective evaluation of possible disease risks.
Thought the scarce information of rhino infections at that time, it was suggested that any chance to examine live and dead animals should include systematic studies and a complete biological sampling.
Trypanosomosis has been mentioned as a problem for rhino exposed through
translocation into tsetse fly zones.
Considering anterior records about the higher pathogenicity of some Trypanosoma species in white rhinos when compared to black rhinos, it was indicated
that this first species should not be translocated to areas of occurrence of those
parasites.
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Some records about the susceptibility of rhinos to Babesia and Theileria were
also mentioned and one case of translocation after the animals have been vaccinated against Babesia was recorded as seemingly have been challenged with no
side effect.
With respect to the two annexes above mentioned, in the first one entitled
“Basic pre-reintroduction/translocation health screening protocols and prophylaxis”. Several actions were proposed including: risk assessment, clinical evaluation, haematocrit, blood smear thick and thin and serum collection for stocking,
occurrence disease, presence or absence of pathogens in source and recipient
populations including sympatric species, endo- and ecto-parasitic load documenting and treating only if mandatory by international protocols or if absent in
the recipient place, serology, vaccination for tetanus and other diseases, necropsy of any dead rhinos, eventual treatment of endo- and ecto-parasites with
avermectin group of anthelmintics, enteric pathogen culture, T. brucei test.
In the second annex named “Summary protocol for veterinary investigation
and post mortem of a rhino carcass” it was recorded a very important point the
use of appropriate precautionary measures for contagious agents. In addition, it
included some other conventional proceedings like, take capillary blood smear
and serum collection if feasible, record the presence of ectoparasites, take
complete series of tissue samples among others.
Hartley and Gill [23] published a study entitled “Assessment and mitigation
processes for disease risks associated with wildlife management and conservation interventions”.
The study described methods approved according the English laws for disease
risk evaluation on wildlife conservation interventions.
They were sorted into four categories that could result respectively in five licensing categories: 1) no additional license conditions, 2) additional license conditions imposed by a wildlife advisor; 3) additional license conditions imposed
by a government wildlife veterinarian; 4) a request for a qualitative veterinary
risk assessment and 5) refusal of the license.
The Category 1 included the following premises: licensed killing of the animals with appropriate carcasses disposal, keeping animals into captivity inaccessible from free-ranging species and relocation of animals in the interior of
their home range.
Rearing or trading captive animals with the purpose of not release were also
considered to pose a negligible disease risk.
In the Category 2, it was showed some actions related to the capture of wild
animals with subsequent releasing into their initial home range after short interval of captivity. Thus, activities like biological sampling and telemetry studies
using wild caught animals and the liberation of recovered wildlife from the veterinary hospital were included in that category.
The time in captivity and the exposure to disease in the course of the intervention should be utilized for determining the disease risk.
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The emphasis according the authors was hygiene and biosecurity, or veterinarian assertion that the animal is free of clinical signs of infectious diseases.
In regarding to that, we would suggest procedures more detailed, because for
several parasites, when infecting their sylvatic hosts, the infections are subclinical in many cases being detected only by molecular tests.
The Category 3 encompassed interventions considered of likely high risk of
disease introduction.
These should be forwarded to a government wildlife veterinarian for further
appraisal. They would include solicitations for moving animals beyond their
home range or species which specific concerns of disease.
In those cases, it should be proposed veterinary participation to ensure health
assessments for quarantine, biosecurity and necropsy.
Apply, respectively, in cases of transfer of an animal far from its area of origin,
the release of imported wildlife, as well as species with specific concerns related
to diseases.
The probable impacts of diseases introduced by translocated or released wildlife on local wildlife populations, livestock or human beings should be considered to establish the diseases of concerns.
Although the UK was thought free of a number of important pathogens with
wildlife reservoirs, according the authors the importance of the diseases of concern should be recorded to those that would have the highest impact on wildlife
populations as well as in the human health or on the economy.
When possible routes of exposure and the most troubling diseases associated
with the proposed licensed action would have been identified, the veterinarian
would consider mitigation measures.
It was mentioned that frequently just simple generic precautions such as biosecurity and hygiene practices or clinical inspection were performed by
veterinarian before release and sporadically specific pathogen assays were demanded.
The Category 4 of disease risk should be applied just in extraordinary situations principally in advance of licensing official reintroduction programs. It
should have been requested a full veterinary risk assessment, containing risk
managing methods and the course of action should be borne by the entrants.
It was stimulated that any such project should have experienced veterinary
supervision during quarantine regimes, animal naming, pre- and post-release
disease surveillance, postmortem examination procedures and medical records.
The entire process should also conform to the International Union for Conservation of Nature and Natural Resources (IUCN) Guidelines for Re-introductions
(IUCN/Species Survival Commission [SSC] Re-introduction Specialist Group 1998)
Any demands should be considered by a review panel of senior officials from
Natural England and Defra as well as by an autonomous veterinary review.
Kock et al. [24] described some disease risks associated with the translocation
of wildlife, reminded the definition of translocation in field of conservation as
the intentional transfer of living organisms from one geographic area to a new,
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meaning the establishing, re-establishing or supplementing a population.
They pointed that the risk of disease introduction because wildlife trade or
translocation for the companion animal would be possibly of greater than the
risk posed by animals translocated for sporting or conservation purposes.
It was remembered that the risks involved on translocations, would depend on
a variety of factors including the epidemiological conditions in the area where
the animals came as well as in the destination or release place.
According the authors, the animals born or raised in captivity like zoological
gardens, farms and breeding centers could represent the greatest risk, because
under natural conditions the epidemiological processes besides the natural selection would decrease the probability of pathogen survival.
Nevertheless an important point was also mentioned, those animals could
present asymptomatic infections including with latent pathogens to other species.
It was also recorded that the risk of a translocated animal introduce different
pathogens into the release area affecting the immunologically naïve fauna in
addition the concept proposed Nettles in 1988 that “a translocated animal is not
the representative of a single species but is rather a biological package”.
We presented further down Table 4 and Table 5 based on the results of Kock
et al. [24] and showing respectively examples of wild mammal diseases introduced or encountered in release areas after wildlife translocations.
Subsequently, a proposal of available measures to be applied in actions related
to wildlife translocations was presented.
Those measures included, schedules for minimizing the risks, through veterinary intervention at the source of the release or among founder stock comprehending of laboratory detection procedures, clinical haematology, screening for
Table 4. Wild mammals species origin and places where diseases have been introduced after their translocation.
Species
Origin
Disease
Microorganism
Destination
Concerned species
Zebra
(Equus burchelli)
Namibia
African horse
sickness
Orbivirus
Spain
Domestic equids
Racoon
(Procyon lotor)
Texas
Parvoviral enteritis
parvovirus
West Virginia
Local raccoons
(Procyon lotor)
Racoon
(Procyon lotor)
Florida
Rabies
lyssavirus
Pennsylvania,
Skunks
(Mephitis mephitis),
Skunks
(Mephitis mephitis),
Florida
Rabies
lyssavirus
Virginia and Maryland
local racoons
Wapiti
(Carves elaphus)
United States
Giant liver fluke
Fascioloides magna
Italy
European ungulates
Bighorn sheep
(Ovis canadensis)
Arizona
Viral pneumonia
RSV
New Mexico
Local bighorns
Plains bison
(Bison bison)
Montana
Tuberculosis,
brucellosis
Brucella abortus
Mycobacterium bovis
Canada
Wood bison
(B. bison athabascae)
Hare
(Lepus europaeus)
Hungary and former
Czechoslovakia
Brucellosis
Brucella suis biovar
Switzerland and Italy
Domestic animals,
humans
Based on the results of Kock et al. [24].
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Table 5. Diseases encountered at release areas by translocated wild mammals. Based on the results of Kock R.A. et al. [24].
Species
Origin
Disease
Microorganism
Destination
Concerned species
Bongo (Tragelaphus
eurycerus isaaci)
United States
Babesiosis
Babesia spp
Kenya
Local artiodactyls
Roan antelope
(Hippotragus equinus)
Namibia
Theileriosis
Theileria spp
Swaziland
Tick vectors
Sable antelope
(Hippotragus niger)
Namibia
Babesiosis
Babesia spp
South Africa
Tick vectors
Bighorn sheep
(Ovis canadensis)
United States
Babesiosis
Babesia spp
United States
Tick vectors
mule deer (Odocoileus
hemionus)
United States
Babesiosis
Babesia spp
United States
Tick vectors
Bighorn sheep
(Ovis canadensis
United States
Pasteurellosis
Pasteurella spp
United States
Sheep
Eastern woodrats
(Neotoma floridana)
United States
Baylisascaris
infestation
Baylisascaris procyonis
New York
Racoons
Black rhino
(Diceros bicornis)
white rhino
(Ceratotherium simum)
Koala
(Phascolarctos cinereus)
South Africa, Kenya
Babesiosis, theileriosis, Babesia, Theileria and
trypanosomosis
Trypanosoma
Masai Mara, Tsavo, Meru,
Kenya; Meru, Kenya;
Ngorongoro, Tanzania
Tick and tsetse
vectors
South Africa, Kenya
Babesiosis, theileriosis, Babesia, Theileria and
trypanosomosis
Trypanosoma
Masai Mara, Tsavo, Meru,
Kenya; Meru, Kenya;
Ngorongoro, Tanzania
Tick and tsetse
vectors
Toxic agent in the
saliva
Victoria, Australia
Tick paralysis
Ixodes spp.
Victoria, Australia
Eastern United States
and Quebec
Cerebrospinal
nematodosis
Elaphostrongylus
rangiferi
Ontario and Nova Scotia
Canada
Arabian oryx
(Oryx leucoryx)
United States
Botulism
Clostridium
Oman
Enzootic in Oman
Muskrat (Ondatra
zibethicus)
United States Canada
Tularemia
Francisella tularensis
Soviet Union
Water voles
(Arvicola terrestris
Brush-tailed possum
(Trichosurus vulpecula)
Tasmania
Bovine tuberculosis
Mycobacterium bovis
New Zealand
Deer, wild pigs, etc
Golden lion tamarin
(Leontopithecus rosalia)
United States
American
trypanosomiasis
Trypanosoma cruzi
South-eastern Brazil
Local fauna
Caribou
(Rangifer tarandus)
White-tailed deer
(Odocoileus
virginianus
haemoparasites through blood smear for haemoparasites identification, analyses
of antibody detection among others.
Furthermore, for verifying if some animal would be probably infected with a
specific pathogen an assortment of more specific tests like, ELISA, PCR and
immunohistochemistry they should be carried out.
A group of more actions completed the proposal such as, veterinary supervising at the supposed release site, pre-release planning, interpretation of survey
and screening results, prophylactic vaccination, post-release health intensive
care and cryopreserved germplasm, among others.
The authors concluded that whatsoever the objective of translocation there
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could be at all times a substantial disease risk and vectors or pathogens could be
transmitted among translocated animals or to recipient fauna.
The human behavior was pointed as an underestimated threat because of the
great quantity of mammal species moved with minor or no health constraints all
over the world.
Moreover in 2010, the IUCN [25] published a very useful Training Manual on
Wildlife Diseases and Surveillance, produced from the Workshop for OIE National Focal Points for Wildlife by the World Organization for Animal Health
(OIE).
Different from the above mentioned IUCN Training Manual published in
2009, in that last one it was addressed specific points related to the wildlife pathogens and diseases.
It started with a definition of “Wildlife” concerned with pathogens and diseases of mammals and birds described as wild animals.
Then were presented some aspects related to socio-economic significance of
pathogens and diseases of those wild animals that could affect the health of human and domestic animals, but also could produce significant impact on the
populations of wild animals.
In this section were listed some wildlife zoonotic diseases or pathogens and
those the related to mammals were the following: HIV, Rabies, Hanta viruses,
Chagas’ disease, Yellow fever, Leishmaniasis, Brucellosis, Tuberculosis, Leptospirosis, Anthrax, Plague, Trichinellosis, Nipah virus, Ebola virus and Monkeypox.
In that list we could include some others important zoonosis like, Toxoplasmose, angiostrogiliasis, Shistosomosis, chikungunya, Mayaro virus, dengue,
Rocky Mountain spotted fever, Bartonella, Lyme disease and others.
Among the examples of pathogens in wild animals may affect the health of
domestic mammals were included: Anthrax, Bovine tuberculosis, Foot-and-mouth
disease, Leptospirosis, Rabies, Myxomatosis, Chronic waste disease, Classical
and African swine fevers, Brucellosis, Venezuelan equine encephalitis, Blue
tongue and Epizootic hemorrhagic disease.
It was also presented considerations about the ecology of pathogens and diseases, emerging diseases and wildlife, pathogen transmission, reservoirs of infectious pathogens, measure of pathogen transmission, manage pathogens and diseases in wild animals, national wildlife disease programs and surveillance.
In the section “Reservoirs of infectious pathogens”, the definition for pathogen reservoir was “one or more epidemiologically connected populations or environments in which the pathogen can be permanently maintained and from
which infection is transmitted to the defined target population”.
Nevertheless, it is important to highlight that several epidemiological studies
have been considering also the concept of reservoir hosts in relation to mammal
species and some parasitic protozoa, because certain particular species of hosts
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voir hosts and the parasites, in general presents an equilibrium, the infections
are in general sub-patent and sub-clinical. So, those species particularly serve as
sources of infection for the vectors. Ex: Trypanosoma cruzi and Leishmania
when infecting the opossum.
In the components of national wildlife disease programs, a very important
point was referred in relation to governmental policies, regulations and programs. It would be fundamental to make possible suitable achievement issues in
relation to wild animals and pathogens. It was highlighted that countries not
prepared to deal which that situations could be at risk of the negative effects
from those health and disease concerns.
They considered wild animal pathogen assessment essential to animal health
management and proposed a constant search and vigilance for pathogens in
wildlife and potential diseases they could cause, collecting data and achieving
systematic analysis.
That surveillance results should comprises communication of the information
gathered to the people, agencies and institutes that could need information.
Accordingly, those surveillance programs should have a number of different
actions, like, the detection of dead or diseased wild animals, collection of samples from wild populations, pathogens characterization and diseases diagnosis
through laboratory assays, data computerized treatment, analysis and reporting
as well as the production of maps, statistics and conferences.
They stated that wide-ranging surveillance for wildlife pathogens should starts
with the detection of those microorganisms in sick or dead wild animals. Such
work should be implemented by a network of qualified professionals, for collecting and processing biological samples for further diagnostic tests.
Finally they showed two appendices respectively related to “Terms of Reference for the OIE National Focal Point on Wildlife” and a suggestion of Project
for small groups for wildlife pathogen and disease surveillance.
The authors stated that wide-ranging surveillance for wildlife pathogens
should starts with the detection of those microorganisms in sick or dead wild
animals. Nevertheless, we think that before starts any fieldwork, broad reviews
on the scientific literature should be of great importance, seeing that actually for
most zoonosis there is great number of publications.
We agree that the collection of biological samples for further utilization in diagnostic tests is notoriously important and in respect to that, we have been suggesting that animals hit by vehicles on the roads could represent a very a
significant source of biological samples.
Campbell and VerCauteren [26] in a study entitled “Diseases and Parasites of
White-tailed Deer” they presented a panel with the objective of providing a
synopsis encompassing, parasites, prion, viral, bacterial and rickettsial diseases.
Among parasites were included protozoan of the genera Toxoplasma, Babesia
and Theileria, Helminths were liver fluke, large lungworm, large stomach worm,
meningeal worm, arterial worm, abdominal worm and larval tap worm.
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The prion sickness was the Chronic wasting disease (CWD), rickettsial
disease was anaplasmosis and the bacterial were anthrax, dermatophilosis,
brain/intracranial abscesses, bovine tuberculosis, Johne’s Disease/paratuberculosis,
leptospirosis, salmonella and Lyme disease.
The viral diseases were hemorrhagic disease, cutaneous fibroma and other viruses including some arboviruses.
It was highlighted the concerning in relation to the presence of CWD in both
captive and free-ranging white-tailed deer and other cervids.
It could mean a critical management problem because of the long incubation
period, negligible early clinical signs, life-threatening infectious agent, environmental contamination, multiple modes of transmission and a 100% mortality.
The measures suggested for decelerating the spreading were localized population reduction, regulating translocation and prohibition of baiting and feeding.
According the authors the meningeal worms should be also considered a concerning subject for natural resource managers and biologists that would assume
translocation activities. The life cycle complexity of the Parelaphostrongylus te-
nuis with mollusks as intermediate hosts could be an additional aggravating factor and a significant threat to all native cervids.
Finally, they suggested the adoption of the guidelines of Corn and Nettles
(2001) by biologists and managers that could be involved in cervids translocation.
Trinkel et al. [27] recorded a very interesting experimental test where translocations were proceeded for combating bovine tuberculosis (BT) in a lion population with increased susceptibility to for that disease caused by inbreeding.
They demonstrated that while 15% of the native population died because BT,
on the other hand less than 2% of the translocated animals died for the same
reason.
Besides, they also recorded there were no significant differences on the antibody prevalence to six feline viruses among native and translocated lions, as well
as offspring. It was suggested that these feline viruses likely presented no effect
on the clinical health of the animals.
The authors concluded that the translocation of those animals without prior
studying of their health status could give rise to unexpected results and management of population genetics through supplementation could effectively prevent pressures on the population’s persistence.
Nevertheless, it was stated that the absence of BT deaths in the translocated
animals and their offspring could be because of the long incubation period of the
microorganism that can remain dormant for years and eventually reactivate.
Although they have been recorded, there were no significant differences on
the antibody prevalence to six feline viruses among native and translocated lions.
Based on the results presented it is very likely that on cases of feline coronavirus
as well as feline calicivirus the differences were significant. Considering that for
coronavirus the percentage of positives on the natives were 3% and among the
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translocated ones was 13% and 21% and for calicivirus, the group translocated in
2006 none of the animals had specific antibodies to Calicivirus.
In 2013, the IUCN [28] published new “Guidelines for Reintroductions and
Other Conservation Transactions”, they were comprised of nine sections, ranging from introduction and scope of guidelines, deciding when translocation is an
acceptable option, until Monitoring and continuing management and dissemination of information.
In relation to disease and translocations, in the section 6 named risk assessment, one of the main categories was the disease risk.
Considered that no translocated organisms could not be entirely free of infections and the risk of disease spreading would ever exist. It should be assessed at
the beginning of the planning stage, evaluating expected probability of occurrence and gravity of negative effects of pathogens as well as the risk of spreading
and should be reviewed periodically.
One important aspect presented was related to the idea that viability valuation
should incorporate the balance of the conservation benefit against the costs and
risks of both the translocation and different conservation actions.
Translocation would interchange with human interests, than socio-economic
and political factors should be essential to translocation achievability and planning. These actions would need efficient multi-disciplinary staff, with technical
and social knowledge that could act for all interests.
In 2014, OIE and IUCN [29] co-published guidelines directed to diseases risk
analysis of the wildlife.
Disease risk analysis (DRA) was pointed as a tool for investigating the risks of
introduction, emergence or re-emergence of a disease in a population. It could
also help the assessing the risk of disease transmission between different species.
According the authors that tool had been used based on the concept that the
disease risk could be triggered by a new or probable action, such as the movement of species into a new territory. Besides it was suggested the aim of DRA
was provide effective and low cost prevention and mitigation plans.
DRA has been progressively applied, in agronomic business, species reintroduction or translocation, but also in human-wildlife and domestic animal interactions with a quite broader applicability.
Five steps in the process of disease risk analysis were proposed as summarized
below:
1) Problem description for defining the circumstances and determine the objectives of the DRA as well as make query, assert conjectures and restrictions and
stipulate the adequate risk degree.
One of the questions proposed was about the type DRA that would be needed
for applying to solve each specific situation.
2) Hazard identification for classifying the health hazards in “infectious” or
“noninfectious”. Categorize each threat taking into account the likely of direct
and indirect outcomes indicating which hazards should be of full risk appraisal.
The issues raised were related to what could cause the disease, how it might
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happen and the likely extent of the problem.
3) Risk assessment for ranking the hazards in a descending order of precedence and evaluate each risk individually for the probability of disease introduction in the new area, the possible level of the species exposition and the probable
consequences in case of disease dispersion.
In this case, the question presented was about the probability and also the effects of a detected threat happen in a recognized pathway or event.
4) Risk management for reconsidering the possibilities of potential risk reduction or controlling as well as appraise the probable consequences.
The questioning has been related to the probable actions for reducing the
probability of occurring a risky incident and diminishing the consequences if it
would have happen.
5) Implementation and review for preparing a strategy of action and contingency as well as ascertain the procedure and schedules for the supervising, assessing and assessment of risk management.
That action should result in a well-defined knowledge about the question for
supporting the DRA improvement.
The questions were about the criteria of selection of risk management actions
that should be applied, their assessment considering if the objectives were
reached and the possibilities of its improvement.
Besides the five interconnected steps, in a schematic view occupying a central
point, the “Risk communication” makes bridges interconnecting all the components together.
One more aspect addressed was the representation of the eco-epidemiological
picture of Ebola and Nipah viruses and Chytridiomycosis in addition to the impact of Diclofenac using. The scheme showed the relationship among, humans,
peri-domestic wildlife and livestock inside the human landscape and participation of the neighboring wildlife, composing the natural environment.
They concluded proposing that, disease risk analysis of wildlife should work
in concert with other agencies and that different presentations of DRA have been
used by various areas like, public health, agriculture, trade, the pharmaceutical industry and wildlife conservation.
The IUCN highlighted that DRA should be applied in all segments related to
wildlife disease, strengthening the concept of “One Health” that acknowledges
the interconnection among the health of people, animals and the environment.
Still in 2014, Jakob-Hoff et al. [30] in an OIE and IUCN co-publication prepared a “Manual of Procedures for Wild Animal Disease Risk Analysis”. In the
first part of this manual, the stages of the process of disease risk analysis (DRA)
were presented; in fact, this subject was also stated in the “Guidelines for Risk
Analysis of Wildlife Diseases.
After the introduction and a brief history of disease risk analysis, were presented key concepts for wildlife disease risk analysis including, risk, disease, disease causes and impacts, objectivity, proportionality, the ‘precautionary principle and others.
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In following, a detailed description about the planning and conducting a wildlife disease risk analysis was presented showing several practical situations.
Were included statements about collaboration, technical, social and political
considerations, challenges in wildlife disease risk analysis, etc.
Among other topics asserted were comprised, risk of communication, problem description, hazard identification, risk assessment, risk management, implementation and review and to close a checklist for conducting a wildlife translocation disease risk analysis.
It is important to highlight, in spite of a very well elaborated manual, the authors even so they signaled the impossibility to reverse habitat loss and extinction or preventing the emergence or resurgence of diseases in such globalized
world.
Therefore, the integration among biodiversity conservation, biosecurity, domestic animal health as well as public health, is fundamental when addressing in
conditions when wildlife disease is a human life-threatening issue.
In relation to the public health, a very important point presented was the suggestion of inclusion of doctors belonging that area on the DRAs. In function
their expertise in diseases prevention and promotion of human health besides
the possibility of instructing medical and veterinary practitioners.
Because the increasing contacts between people and wildlife, they suggested
that DRAs should include the possibility of zoonotic disease transfer and doctors
in public health could give recommendation on measures for the risks management.
Finally, twenty-two very useful tools for wildlife disease risk analysis were
presented.
They were: Disease Risk Assessment Tool (DRAT), Visual system-level simulation modeling: Stella and Vensim, Disease Risk Analysis Worksheet (DRA
Worksheet), Paired ranking for hazard Prioritizing, Graphical models, Decision
trees, Influence diagrams, Fault trees, Concept Maps (Cmap), Geographic Information Systems (GIS), OIE Handbook, @Risk, OUTBREAK, PopTools, Formal elicitation of expert opinion, Netica, Precision Tree, Vortex, RAMAS and
Risk communication plan template.
Additionally, it was also exemplified the use of some those tools and incorporated eight appendices, ten boxes, fifty-one figures and nineteen tables showing
how complex could be the DRA and the importance of a multidisciplinary approaching to carry it out.
In 2015, the OIE World Organization for Animal Health published a fact
sheet entitled “Wildlife Diseases” [31] that was produced basically for presenting
the WAHIS interface, a World Animals Health Information Database produced
through information mostly obtained from veterinary services.
Based on that wild animals could be targets or reservoirs for microorganisms
able of infecting other animals and human, it was considered that the wildlife
disease monitoring, prevention and control were decisive aspects for biodiversity
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preservation as well as for public and animal health.
According the authors an increased spreading of pathogenic organisms had
been occurring in function of several factors including anthropic action, climate
change, globalization, demographic evolution and new human social behaviors.
Intensified trade around the world had provided more chances of infectious
agents combine, circulate in different species and exchange genetic material with
the potential development of new killer pathogens.
In relation of the WAHIS in our view, it may considered a very important tool
for the world animals health, nevertheless as already above mentioned, it is a
health information database basically produced through information obtained
from veterinary services.
We think the WAHIS should also include information from other sources besides the veterinary services. In the scientific literature, there is vast number of
papers from diverse groups that have been studding diseases from a great number of animal species.
Additionally, the information should be more contextualized, for example: in
the WAHIS wild interface, the section affected species, where it should be observed
disease/infection presence occurrence by codes for a chosen family (ies) and species. The diseases related to Didelphidae in the table related to disease/infection
presence by species from 2008 to 2018, it show only one case of infection with
Leptospira interogans ssp and other of salmonellosis caused by S. enterica, respectively in Didelphis virginiana (Virginia Opossum) in Colombia and Didelphis aurita (Big-eared Opossum) in Netherlands.
As there is no additional information in the table, it could be assumed that
those data were originated from zoo animals, because the species Didelphis vir-
giniana do not occur in Colombia neither the Didelphis aurita (the Black-eared
Opossum) in Netherlands.
The Didelphidae is a family of New World marsupials and the unique representative belonging that family of the genus Didelphis that occurs in Colombia is
the D. marsupialis.
In addition to those significant reports that showed seemingly cases of accidental infections with Leptospira and Salmonella, there are numerous records
equally relevant that could be included in the table.
There are many studies relating to several genera of the Didelphidae family
and their close relationship with some representative of the Trypasomatidae
family.
A number of species of the Didelphis genus have been fully described as important reservoir hosts of Trypanosoma and Leishmania, playing essential roles
on the eco-epidemiology of the diseases caused by those parasitic protozoa in
both sylvatic and peridomestic transmission cycles.
The Didelphis (common opossum) for example, it is the unique mammal host
described until now where the Trypanosoma cruzi can complete its whole biological cycle presenting all developmental forms observed in both, the mammals
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reservoirs and the triatomine insect vectors. Soon the parasite in the Didelphis
can develop inside of muscle and nerve cells as normally do in all mammals or
extracellularly in the lumen of scent glands, performing the cycle correspondent
to that occur in the insect gut.
It is important to highlight that the forms of the parasite may be eliminated
together the scent glands content what the animal do under stress situations.
Actually, like the metacyclic forms excreted by the triatomine bugs those expelled by the opossum can equally be potentially infective to other mammals included man.
In 2017 Hartley and Sainsbury [32] in a paper entitled “Methods of Disease
Risk Analysis in Wildlife Translocations for Conservation Purposes” they presented results related to the Zoological Society of London’s Disease Risk Analysis
and Health Surveillance (DRAHS) project.
It has been operating for 25 years, in partnership with Natural England and
non-governmental organizations, to assess and respond to disease risks associated with interventions undertaken for the national species recovery program
for native wildlife.
They recalled the risks of wildlife translocations and the inherent disease impacts that could cause broad effects involving government, farmers, local residents and businesses.
It was exemplified by the case of an unofficial introduction of European beavers and the risk of introducing of the Echinococcus multilocularis to the UK.
They also pointed different aspects related to translocations of species from ex
situ populations and the potential disease risks. Those aspects included, animals
with asymptomatic infections carrying pathogenic microorganisms to the new
habitat, the exposition to exotic infective agents and the mixture of species from
unrelated geographic regions, the potential stress resulting in immunosuppression and the absence of acquired immunity or resistance to the infectious.
As examples for those potential disease risks were mentioned the cases of hazel dormice that were exposed to a supposed novel cestode species in captivity
prior to reintroduction and red squirrels (Sciurus vulgaris) reintroduced that
were exposed to a squirrel poxvirus (harboured by an alien invasive grey squirrel, (Sciurus carolinensis) resulting in a severe squirrelpox disease outbreak.
Both cases occurred in England.
Afterward, were made several considerations about the meaning of disease
risk analysis, its development, different approaches and modifications for wildlife translocation, expertise involved, information required, quantitative versus
qualitative analysis, uncertainty and subjectivity, disease risk management and
finally the risk analysis as a tool for decision making.
Among to different approaches and modifications for wildlife translocation it
was indicated that even when concentrated only on threatened species, there
were several possibilities for making use of disease risk analysis like, preceding
the reintroduction program, because a specific disease diagnosed in the course of
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a project or an epidemiological search of unidentified disease concentrated in a
determined species.
A table was presented showing several examples of how DRA, disease risk
management (DRM), and post-release health surveillance (PRHS) had been incorporated into monitoring disease health and translocation of species covered
by the DRAHS project.
Concerning the expertise involved, as already stated in previous studies, a
necessity of a multidisciplinary team was indicated as very important.
In quantitative versus qualitative analysis, according the authors in function of
the great scarcity of numerical data related to wildlife populations, like prevalence
of infection, incubation period, duration of infection, and the size and distribution. The qualitative risk assessment could be probably as accurate as the quantitative method in wildlife translocation.
The advantage of the risk assessment when presented under a qualitative approach was the possibility of working with plain language and logic to be more
comprehensible by a wider range of participants and decision makers.
Concerning to the uncertainty and subjectivity, it was highlighted the importance of stating the areas and the range of the uncertainty as well estimates risks,
mainly in the early phases of assessment when supposedly the uncertainties
could be large and the data scarce.
Based on the lack of mathematical or modelling studies directed to uncertainty,
it was suggested the use of the information gap theory proposed by Ben-Haim
(2001), which comprises mathematical development model, performance constraint and a model for uncertainty.
Disease risk management was described as a process of identifying measures
that could be applied to the problem that would reduce the risk of disease.
Schedules of risk management also would support the classifying of threats and
redefine the suitable risk levels.
In risk analysis as a tool for decision-making, Hartley and Sainsbury mentioned Wooldridge 2000 when considering it as a progressive assignment employing facts and records combined with the thoughts and assessments from a
wide-ranging of standpoints.
According to the authors, the determining of what could be considered as an
acceptable risk constitutes one of the most difficult problems faced by decision-makers. Because some level of risk could be always predictable and the
choice usually would involves societal or political decision.
Thus in respect to wildlife translocation, besides the disease risk analysis, financial costs, public support, political approval and stakeholder endorsement
could be other providers.
In conclusion, they related that Wildlife disease risk analysis processes have
been developing but even so, there were many questions for addressing yet.
In 2018, Mengak [33] in a paper entitled “Wildlife Translocation” discussed a
very important point related to translocations and the risk of disease spreading,
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the fate of animals implicated in human-wildlife conflicts.
It was recorded the concerns of scientists, wildlife managers, and public health
professionals in relation the spread of disease and translocation of wild animals.
Once again, it was remembered that animals moved could carrier worms,
ticks, fleas, viruses, bacteria, and other parasites. As an example was recorded,
the case of a raccoon strain of rabies virus originated from raccoons from Florida (USA) and were introduced into the Mid-Atlantic and Northeastern states
after translocations. Actually, even when moving the animals for short distances
the concern would be well founded.
Other diseases including, plague, chronic wasting disease, pneumonia, tuberculosis and brucellosis, tick paralysis, botulism, tularemia, bovine tuberculosis,
and trypanosomiasis were also associated to wildlife translocations.
Human exposure to diseases, for example, homeowners or others who would
transport wildlife by exposing themselves and others at risk was also considered
a concern.
In conclusion, Mengak [33] asserted that both professional and public opinion
about managing wildlife and wildlife nuisance problems have been changed because certain wild animal species have been becoming more abundant.
Translocation in spite of usually been considered as humanitarian, harmless
and effective, the wildlife professionals would not agree with the use of that
technics, with exception of large carnivores where management options are limited to either translocation or euthanasia.
Actually, translocation for solving wildlife nuisance problems should be seldom proposed because several reasons like, animal stress, potential handler lesion, risk of moving a disease among others.
Instead, other measures should be taken and wildlife professionals should assist enlightening the public about alternative control measures, such as habitat
alteration, exclusion, scare devices, repellents, and euthanasia.
They would be perceptive to changing public feelings and clarify why euthanasia would be the most reasonable choice when nonlethal methods are not
achievable.
In 2019, one of the most recent and significant publication related to disease
risk on wildlife translocations are the “Guidelines for the management of confiscated live organisms presented by IUCN, edited by Neil Maddison [34].
These guidelines presented a broad approach, including plants and animals,
considering the importance of effective management methods to make the best
use of the role of conservation and individual well-being.
Due to the need to promote a policy formulation process for wildlife management. It was emphasized, the importance of preventing the extinction of species in addition to safeguarding the health of each single animal prioritizing risk
assessment for both, confiscated animals and for the wildlife that lives in areas
where they could be translocated.
The spread of diseases from released animals caused by incorrect management
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was considered as one of the primary risks for preventing of biodiversity loss.
A very important aspect was also presented related to taking of a proactive
approach in order to make sure necessary information for the decision-making.
It was suggested the development of consultative networks by the confiscating
authorities that should comprise experts including:
1) Specialists in taxonomy to enable rapid and accurate identification to species/subspecies level.
2) Medical and veterinary team on human and animal health, and quarantine.
3) Professionals in wildlife rescue, husbandry and animal behavior.
4) Legal skill.
5) Logistical for advising on holding and transport.
6) Wildlife rescue/rehabilitation centers.
7) Zoo consultants and associations, and sanctuaries.
8) World Organization for Animal Health (OIE) focal points.
9) Government/university veterinary departments.
10) In-country CITES Management and Scientific Authorities.
11) In-country wildlife crime enforcement and border authorities.
The Guidelines In respect to action planning among the immediate short-term
cares, it is emphasized the importance of confiscated organisms being immediately placed into quarantine that may vary depending on the species and situations.
Another important point stated was the disease transmission risks to humans
and other organisms belonging the same or different species while in transit,
holding or translocation.
The risks of disease transmission to humans and other organisms belonging
the same or different species while in transit, holding or translocation were considered as well as the euthanasia that was referred as “the humane ending of an
animal’s life for the intention of preventing further suffering of an injured
and/or sick animal.”
In those cases of euthanasia, we suggest that all the material derived from the
animals should be available for research. It would contribute directly to a pool of
records about important species and the major infectious agents related to them.
It could be of great importance, taking into account that in several situations
euthanasia is unfortunately the only option even for animals included in the extinction risk list. Actually, any sample collected from those animals may contribute with valuable information.
One more aspect mentioned directly associated risks of disease transmission,
was the wildlife trading in view of a direct correlation between the increasing of
wildlife confiscation and illegal trade in addition to a better knowledge and understanding on the part of the competent authorities.
It was assumed these guidelines are offered to help confiscation authorities
make decisions in view of the notorious impossibilities of preventing the illegal
trade in wild animals and the difficult decisions that they have to take concerning this problem.
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Concerning to the wildlife trade, Can et al. [35] also highlighted the potential
for spreading of zoonotic diseases.
Zoonosis are causing millions of deaths and just look at known cases of Ebola
or Severe acute respiratory syndrome (SARS) that have been provoking global
impacts.
Actually, wildlife trade either legal or not, it may represent risks to human
health seeing that pathogens in their host they do not care about the way they
are negotiated, legally or illegally.
There are several motives associated to, conservation, animal health and ethics
to be concerned about the regulation of wildlife trade. Nevertheless, the pathogens responsible for emerging zoonosis, they should not be underestimated.
2. Discussion
Indeed, after presented how the procedures related to wildlife translocation and
disease risk assessing have being evolving with the production of several protocols and guidelines.
Noticeably, the rules directed to conservation purpose are at present the best
stablished.
Nevertheless as recorded by Chipman et al. [21] there are other types of actions involving translocations, including, by the public, nuisance control operators, rehabilitators and others.
In reality the relocation of wildlife have been needed more and more due to
wildlife captured illegally and seized by authorities, sick or hit on roads, victims
of anthropogenic environmental disasters and rescued from areas disturbed by
major engineering projects, such as highways or power plants.
All those factors together with the scanty actions developed in some places
directed to avoid disease spreading through wildlife translocation make that
problem much more complex.
Even in conservation actions, it may be very difficult preventing adverse effects.
In fact, reintroducing an animal in the wild, ensuring its health, and further
avoiding the introduction of some exotic species of parasites, can be a very difficult task.
There are several parasites such as the Trypanosoma cruzi that present different lineages that can circulate individually with different geographical distribution patterns, even in close fragments of the same forest [36].
As well Leishmania that can perform a discontinuous transmission pattern
and even in circumscribed habitats may exist small areas corresponding to “hot
spots” where the risk of parasite transmission is very high, surround by low risk
places [37].
In addition, in several situations it is difficult the determining of what diseases
must be tested for each species, because it can, change depending on the place
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eases.
It must also be taken into account that in many diseases there is not enough
information about the evolution and potential pathogenicity for a great number
of species.
In addition, there is no available reagent to proceed diagnostic test for several
of them. Even in those infections that could be easily diagnosed by a dipstick
test, the data on the treatment or prevention, are either scarce or nonexistent.
It is important to highlight that a great number of microorganisms related to
infectious diseases, have been co-evolving with their natural host species since
millions of years ago, like Trypanosoma or Leishmania that have being evolving
with their sylvatic mammal hosts since the existence of Gondwana supercontinent.
Indeed, it must be expected that sylvatic animals will probably be infected
with a great number of parasites, which in many cases are also responsible for
pathogenic human diseases.
As an example, we could mention the lion tamarins they are small New World
primates belonging the genus Leontopithecus that is composed of four species:
L. rosalia, L. chrysomelas, L. chrysopygus and L. caissara.
This genus is endemic from Brazil living in the Atlantic rain forest, in 2003
the golden lion tamarin (Leontopithecus rosalia) was down listed to endangered
from Critically Endangered on the IUCN Red List following the black lion tamarin (Leontopithecus chrysopygus). It was achieved after three decades of conservation efforts involving numerous institutions.
It was considered by IUCN that populations of both animals have been considered well-protected but continue very small, indicating a necessity for reforestation to provide new habitat.
According to May and Lyles [5] of the 26 animals reintroduced in the native
habitat in Poço das Antas Biological Reserve (Brazil), after about two years, only
five were alive and disease was the leading cause of death.
Correspondingly, several other studies where carried out on the same place
involving Trypanosoma cruzi infection on the populations of lion tamarins that
are considered as one of the species that are reservoir hosts of this protozoan, the
etiological agent of Chagas’ disease. [38]
Lisboa et al. [39] analyzed the Trypanosoma cruzi infection in Leontopithecus
rosalia.
From 118 lion tamarins composing 21 groups varying to three to eleven animals respectively, 52% presented positive serological titers and the parasite was
isolated from 38 specimens. No patent parasitemia have been observed indicating that the indirect diagnostic methods would be more effective in similar cases.
Nevertheless, some animals formerly free from T. cruzi infection, in a period
of some months showed serum conversion and positive hemoculture, indicating
the occurrence of a sylvatic cycle and active transmission.
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ferent populations of L. rosalia and concluded that the parasitaemia of infected
tamarins from the above mentioned reserve, is higher than that of tamarins from
the other studied forest fragments.
They winnowed three hypotheses for explaining it: 1) reinfection, 2) concomitant infection by other parasites and 3) improper management conditions of
this forest fragment. Nevertheless, the possibilities reinfection were considered
irrelevant based on haemocultures and experimental infections.
In our opinion, it is likely that has occurred insect vectors dispersion, from
surrounding areas of the Reserve. Then, some tamarins from neighboring forest
fragments could already be infected with Tc II and, after their blood-feeding the
triatomines have flew to the neighboring habitat [40].
Several of those areas are located within a radius of 5 km that could be
reached by the triatomines that have a considerable flight range [41].
Besides, a specimen of Triatoma vitticeps captured in one of those places was
described posteriorly as infected with T. cruzi II, the same lineage isolated of the
golden lion tamarins living in Poço das Antas Biological Reserve.
There are several records about the T. vitticeps with high percentages of natural infection by T. cruzi in the Atlantic rainforest, southeast Brazil.
In addition, it was capable to maintain long term infection by the same lineage
of the parasite, and have been frequently described in natural infection, with
corroborates with the possibility of vector dispersion [42].
It is likely, that because the tamarins of the Poço das Antas Biological Reserve
were living isolated as referred by the authors, that population would be naïve to
Tc II lineage of T. cruzi, consequently they presented the infection patterns correspondent to recently infected animals, confirmed by some cases of seroconversions recorded.
Following the studies with T. cruzi infections, Monteiro et al. [43] presented
clinical, biochemical, and electrocardiographic aspects of T. cruzi infection in
free-ranging golden lion tamarins (L. rosalia).
They concluded that given the similarities of human disease and T. cruzi infection in tamarins, mortality rates of near 13% could expect because associated
cardiac problems.
An overall death rate from 4% to 7% for tamarins from the Poço das Antas,
was estimated based on the prevalence of T. cruzi that varied from 32% to 52%.
The death of sick animals was suggested as also increasing by indirect factors
such as predation, considering that it has been responsible for a reduction of the
size tamarin population by 40% in the area.
In the same year, the above-mentioned authors [44] examined the correlation
of Trypanosoma cruzi and intestinal helminths infections in wild golden lion tamarins Leontopithecus rosalia and golden-headed lion tamarins L. chrysomelas
(Callitrichidae, L., 1766).
They observed high percentages of Trypanosoma cruzi seroprevalence ranging from 13% to 47%. In addition, it was suggested that the increase in helminth
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prevalence associated with T. cruzi infection was apparently related to the type
of helminth pathogenic action.
In addition, the increased helminth prevalence associated with T. cruzi
infection, was suggested as apparently related to a type of helminth pathogenic
action.
It showed how one determined species of parasite could influence on the behavior of a different one, affecting its pathogenicity.
Lisboa et al. [45] presented the results from an 11-year follow-up investigating
the infection with Trypanosoma cruzi in lion tamarins (Leontopithecus spp).
It was concluded, that the infectivity competence of the golden lion tamarin
fluctuates presenting peak every other year. Furthermore, both golden and golden-headed lion tamarins were able to maintain long-lasting infections by different sub-populations of Trypanosoma cruzi.
Those above information suggest that Trypanosoma cruzi probably could already exist before in these areas utilized for reintroduction of the animals.
Finally, Kerr et al. [38] through lineage-specific serology, verified that Atlantic
forest lion tamarins, Leontopithecus chrysomelas and Leontopithecus rosalia,
were reservoir hosts of Trypanosoma cruzi II (TcII), a lineage that has been
commonly associated with severe Chagas disease in South America.
Actually, those observations also show how complex can be the biological interactions involving parasites, vectors and hosts, mainly with those parasites
species with diverse vectors and hosts like the T. cruzi.
In fact, Trypanosoma cruzi, besides of being a causative agent of Chagas disease, which is still a serious health problem without a vaccine, and drug
treatment, produces several side effects. It is a very common parasite infecting a
great quantity of different sylvatic mammal species in many countries from
Central to South America but even so, in a relatively small area inside of a forest,
the behavior of the parasite can vary drastically affecting the hosts in different
ways.
Here one important aspect must be highlighted concerning rescuing of sylvatic animals, this have to be considered firstly a potential public health issue.
So, all the professionals that will work in contact with the animals, or biological samples they must be properly trained and utilize the required personal protection equipment in agreement with biosecurity standards.
3. Conclusions
In conclusion, all the above information shows how indispensable is the searching of parasite infection among rescued sylvatic animals, before releasing it back
into the wild.
Another important point mentioned in the literature above was the geo referencing of the places where the animals were found. It would be a very useful
tool for digitally mapping the points where sylvatic cycles of various infectious
microorganisms occur, showing the potential risks of infection from each reDOI: 10.4236/ojas.2020.101006
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gion. It would also determine possible dangerous parasite interactions, even
considering groups of forest fragments. It also would determine possible hazardous parasite interactions.
Actually all those records systematically assembled also could be very helpful
on the choice of probable places for a species relocation.
It also showed the necessity of the creation of one easily reached system integrating a multidisciplinary databank where one professional could utilize information of each specific biome. The information could include scientific records
about ecology and ethology of a great number of species, besides all the knowledge related to infectious diseases and the biological cycles of each autochthonous etiological agent, containing natural hosts and sylvatic vectors.
The importance of returning sylvatic animals to the wild is undeniable, nevertheless to make it reasonably, as already stated it is necessary deploying animal
health bases exclusively committed with wildlife protection but also combined
with a public health conscience.
Those centers would minimize the likelihood of disease spreading related to
reintroduction of sylvatic animals and the transmission of these infectious
agents to the resident fauna but also mitigate effects of potential emerging and
re-emerging zoonosis.
In fact, it will also provide important information for preventing emerging
zoonosis.
The formation of a net of multidisciplinary teams of specialists integrating the
information is fundamental, besides of helping the assessment for each specific
situation, it could enable the collecting of biological samples from those animals
for a great number of research fields such as DNA sequencing, biology of parasite, taxonomy, production of medicines and vaccines, among others.
Moreover, the formation of a Banc constituted by Tissue samples from sylvatic specimens could signify a valuable reserve for the genetic inheritance of many
determined ecosystems.
It could also represent an important opportunity to study the role of various wild
animals as hosts of infectious agents, including vulnerable and endangered species.
In reality, sometimes it is very difficult for the detection of parasites in animals with subpatent infections or symptomless, often requiring specific tests. On
the other hand, multiple infections among sylvatic animal hosts involving different parasites species or even different strains from the same species may be
very common [46] [47].
Essentially, every single biome presents an intricate pattern of niches sustaining an immense diversity of species, and each individual presenting an even
more significant range of parasites.
Among the several points related to wildlife, translocations and the risk of
disease transmission above remarked. One of that currently still represents a gap
is the lack of information about sylvatic hosts of a great number of infectious
agents. In function of that, we presented below several tables showing records of
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wild mammal infections with several parasitic protozoan.
The order of the mammal species showed in the tables followed the molecular
studies based on DNA analysis proposed by Tarver et al. [2].
In spite of the incongruences on the literature in relation to molecular phylogenetic analyses, some studies of DNA sequencing have supported that approach but
even so, the criterion utilized was just for a didactic purpose for assembling the data.
Indeed all the animals were identified at least at genus level.
Monotremata
Monotremes belong the subclass Prototheria and are one of the three living
groups of mammals, together with marsupials (Metatheria) and placentals (Eutheria).
Characteristically they lay eggs instead of giving birth to pups, but like all
other mammals, nurse their young with milk (Figure 1, Table 6).
Marsupialia
Marsupials are any members of the mammalian infraclass Marsupialia (from
Latin marsupium pouch). All extant marsupials are endemic to Australasia and
the Americas.
Figure 1. Tachyglossus aculeatus.
Table 6. Records of infections of Monotremata with parasitic protozoa, including the
host and parasite species as well as the place and reference numbers.
Monotremata
Host
Platypus
Ornithorhynchus anatinus
Short-beaked echidna
Tachyglossus aculeatus
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Disease agent
Place
Ref. number
Theileria ornithorhynchi
Australia
[48] [49]
Trypanosoma binneyi
Australia
[50]
Theileria tachyglossi
Australia
[48]
Coccidia
Australia
[51]
Hepatozoon tachyglossi
Australia
[52]
Eimeria echidnae
Australia
[53]
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A distinctive characteristic common to those animals is that the offspring are
born while they are still in the embryonic stage, and they crawl to a pouch or
abdominal skin folds for completing their development (Figure 2, Table 7).
Figure 2. Marmosops incanus.
Table 7. Records of infections of marsupials with parasitic protozoa, including the host
and parasite species as well as the place and reference numbers.
Marsupialia
Australian Marsupials
Host
Southern brown bandicoot
Isoodon obesulus
Northern brown bandicoot
Isoodon macrourus
Long-nosed bandicoot
Perameles nasuta
Long-nosed potoroo
Potorous tridactylus
Gilbert’s Potoroo Potorous gilbertii
Woylie or brush-tailed bettong
Bettongia penicillata
Quokka Setonix brachyurus
Eastern Grey Kangaroos
Macropus giganteus
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Disease agent
Place
Ref. number
Theileria perameles
Australia
[54]
Trypanosoma vegrandis
Australia
[55]
Trypanosoma copemani
Australia
[55]
Trypanosoma thylacis
Australia
[55]
Theileria perameles
Australia
[54]
Theileria perameles
Australia
[54]
Theileria gilberti
Australia
[56]
Trypanosoma copemani
Australia
[55]
Theileria penicillata
Australia
[57]
Trypanosoma copemani
Australia
[55]
Trypanosoma vegrandis
Australia
[55]
Trypanosoma sp H25
Australia
[55]
Theileria brachyuri
Australia
[57]
Trypanosoma copemani
Australia
[55]
Babesia macropus
Australia
[58]
Eimeria hestermani
Australia
[59]
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Continued
Red Kangaroo Macropus rufus
Western grey kangaroo
Macropus fuliginosus
Common wallaroo
Macropus robustus
Red-necked wallaby
Macropus rufogriseus
Black-striped wallaby
Macropus dorsalis
Tammar wallaby Macropus eugenii
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Eimeria toganmainensis
Australia
[59]
Eimeria wilcanniensis
Australia
[59]
Eimeria macropodis
Australia
[59]
Eimeria marsupialium
Australia
[59]
Eimeria gungahlinensis
Australia
[59]
Eimeria yathongensis
Australia
[59]
Trypanosoma sp. H25
Australia
[55]
Toxoplasma gondii
Australia
[60]
Eimeria toganmainensis
Australia
[59]
Eimeria wilcanniensis
Australia
[59]
Eimeria macropodis
Australia
[59]
Leishmania spp
Australia
[61]
Toxoplasma gondii
Australia
[60]
Eimeria toganmainensis
Australia
[59]
Eimeria hestermani
Australia
[59]
Theileria fuliginosa
Australia
[57]
Eimeria wilcanniensis
Australia
[59]
Eimeria macropodis
Australia
[59]
Eimeria marsupialium
Australia
[59]
Eimeria gungahlinensis
Australia
[59]
Eimeria yathongensis
Australia
[59]
Trypanosoma vegrandis
Australia
[55]
Toxoplasma gondii
Australia
[60]
Eimeria wilcanniensis
Australia
[59]
Leishmania spp
Australia
[61]
Eimeria hestermani
Australia
[59]
Eimeria toganmainensis
Australia
[59]
Eimeria macropodis
Australia
[59]
Eimeria flindersi
Australia
[59]
Eimeria prionotemni
Australia
[59]
Eimeria desmaresti
Australia
[59]
Eimeria hestermani
Australia
[59]
Eimeria macropodis
Australia
[59]
Eimeria prionotemni
Australia
[59]
Eimeria hestermani
Australia
[59]
Eimeria toganmainensis
Australia
[59]
Eimeria macropodis
Australia
[59]
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Continued
Western brush wallaby
Macropus irma
Whip-tailed wallaby
Macropus parryi
Parma wallaby Macropus parma
Antilopine wallaroo
Macropus antilopinus
Agile wallaby Macropus agilis
black wallaroo
Macropus bernardus
Chuditch Western quoll
Dasyurus geoffroii
Tiger quoll Dasyurus maculatus
Northern Quoll
Dasyurus hallucatus
Northern brownbandicoot
Isoodon macrourus
Pearson Island rock-wallaby
Petrogale lateralis pearsoni
Quokka Setonix brachyurus
Tasmanian pademelon
Thylogale billardierii
Swamp wallaby Wallabia bicolor
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Eimeria flindersi
Australia
[59]
Eimeria prionotemni
Australia
[59]
Trypanosoma vegrandis
Australia
[55]
Eimeria macropodis
Australia
[59]
Eimeria macropodis
Australia
[59]
Eimeria mykytowyczi
Australia
[59]
Eimeria prionotemni
Australia
[59]
Eimeria parryi,
Australia
[59]
Eimeria macropodis
Australia
[59]
Eimeria parma
Australia
[59]
Eimeria flindersi
Australia
[59]
Eimeria mykytowyczi
Australia
[59]
Eimeria prionotemni
Australia
[59]
Eimeria mykytowyczi
Australia
[59]
Leishmania spp
Australia
[61]
Trypanosoma evansi
Australia
[55]
Leishmania spp
Australia
[61]
Trypanosoma vegrandis
Australia
[50]
Trypanosoma vegrandis
Australia
[55]
Trypanosoma copemani
Australia
[50]
Trypanosoma copemani
Australia
[55]
Babesia thylacis
Australia
[62]
Trypanosoma thylacis
Australia
[50]
Eimeria petrogale
Australia
[63]
Eimeria sharmani
Australia
[63]
Eimeria godmani
Australia
[63]
Eimeria inornata
Australia
[63]
Eimeria setonocis
Australia
[64]
Eimeria volckertzooni
Australia
[64]
Eimeria quokka
Australia
[64]
Eimeria thylogale
Australia
[64]
Eimeria obendorfi
Australia
[64]
Eimeria ringaroomaensis
Australia
[64]
Eimeria wallabiae
Australia
[64]
Eimeria bicolor
Australia
[64]
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Continued
Hare-wallabies
Lagorchestes conspicillatus
Eimeria lagorchestis
Australia
[64]
Tree-kangaroo
Dendrolagus lumholtzi
Eimeria lumholtzi
Australia
[64]
Eimeria dendrolagi
Australia
[64]
Toxoplasma gondii
Australia
[65]
Toxoplasma gondii
Australia
[65]
Toxoplasma gondii
Australia
[65]
Toxoplasma gondii
Australia
[65]
Toxoplasma gondii
Australia
[65]
Toxoplasma gondii
Australia
[65]
Trypanosoma copemani
Australia
[55]
Trypanosoma irwini
Australia
[55]
Trypanosoma copemani
Australia
[55]
Trypanosoma gillett
Australia
[55]
Trypanosoma vegrandis
Australia
[66]
Trypanosoma gilletti
Australia
[66]
Sarcocystis spp
Brazil
[67]
Trypanosoma cruzi
Brazil
[68]
Trypanosoma cruzi
*(in scent glands)
Brazil
[68]
Leishmania forattinii
Brazil
[61]
Leishmania infantum
Brazil
[61]
Leishmania amazonensis
Brazil
[61]
Trypanosoma freitasi
Brazil
[69]
Trypanosoma cruzi
Brazil
[68]
Leishmania amazonensis
Brazil
[61]
Leishmania guyanensis
Brazil
[61]
Leishmania mexicana
Brazil
[61]
Leishmania infantum
Colombia
[61]
Kultarr-“Jerboa-marsupial”
Antechinomys spenceri
Antechinus spp
Crest-tailed mulgara
Dasycercus cristicauda
Kowari Dasyuroides byrnei
Fat-tailed dunnart
Sminthopsis crassicaudata
White-footed dunnart
Sminthopsis leucopus
Common wombat
Vombatus ursinus
Koala Phascolarctos cinereus
New World Marsupials
Didelphis spp
Black eared opossum
Didelphis aurita
Common opossum
Didelphis marsupialis
Common opossum
White-eared opossum
Didelphis albiventris
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Leishmania infantum
Venezuela
[61]
Leishmania braziliensis
Colombia
[61]
Leishmania braziliensis
Venezuela
[61]
Leishmania (Viannia )spp
Colombia
[61]
Leishmania mexicana
Honduras
[61]
Trypanosoma rangeli
Brazil
[70]
Trypanosoma cruzi
Brazil
[68]
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Continued
Andean white-eared opossum
Didelphis pernigra
Northern red-sided opossum
Monodelphis brevicaudata
Grey short-tailed opossum
Monodelphis domestica
Southeastern four-eyed opossum
Philander frenatus
Gray four-eyed opossum
Philander opossum
Bare-tailed woolly opossum
Caluromys philander
Brown four-eyed opossum
Metachirus nudicaudatus
Murine mouse opossum
Marmosa murina
Long-furred woolly Mouse
Opossum Marmosa demerarae
Robinson’s mouse opossum
Marmosa robinsoni
Mexican mouse opossum
Marmosa mexicana
Grey Slender Opossum
Marmosops incanus
Trypanosoma cruzi
Paraguay
[71]
Leishmania infantum
Brazil
[61]
Leishmania braziliensis
Brazil
[61]
Leishmania amazonensis
Brazil
[61]
Leishmania guyanensis
Brazil
[61]
Leishmania peruviana
Peru
[61]
Trypanosoma cruzi
Brazil
[68]
Trypanosoma cruzi
Paraguay
[71]
Leishmania (Viannia) spp
Brazil
[61]
Trypanosoma cruzi
Brazil
[68]
Trypanosoma cruzi
Brazil
[68]
Leishmania amazonensis
Brazil
[61]
Trypanosoma cruzi
Brazil
[68]
Leishmania spp
Trinidad
[61]
Leishmania braziliensis
Trinidad
[61]
Leishmania garnhami
Trinidad
[61]]
Trypanosoma cruzi
Brazil
[68]
Leishmania amazonensis
Brazil
[61]
Leishmania amazonensis
Brazil
[61]
Leishmania braziliensis
Brazil
[61]
Leishmania amazonensis
Brazil
[61]
Leishmania braziliensis
Colombia
[61]
Leishmania spp
Trinidad
[61]
Leishmania mexicana
Panamá
[61]
Leishmania mexicana
Mexico
[61]
Leishmania guyanensis
Brazil
[61]
Leishmania braziliensis
Dusky slender opossum
(Marmosops fuscatus)
The agile gracile opossum
Gracilinanus agilis
Elegant fat-tailed mouse opossum
Thylamys elegans
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[61]
Leishmania spp
Colombia
[61]
Leishmania spp
Brazil
[61]
Sarcocystis
Chile
[72]
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Afrotheria
Afrotheria is a clade of mammals, of which include groups that are currently
living either in Africa or of African origin.
Most of afrotheres present slight or no morphological likeness, and their relationships have only become known not long in function of genetics and molecular studies.
Among the groups of Afrotheria, those which currently live out of Africa, include animals of the Family Trichechidae represented by two species in the order
Sirenia, the Amazonian manatee (Trichechus inunguis) and the West Indian
manatee (Trichechus manatus) (Figure 3, Table 8).
Xenarthra
Xenarthra is a group of placental mammals from the New World represented
by anteaters, tree sloths and armadillos.
It currently has 13 genera with 30 species, mostly native to South and Central
America, except the nine-band armadillo (Dasypus novencinctus) that occurs in
North America. The radiation of xenarthrans occurred during the Tertiary Period when South America was an island continent (Figure 4, Table 9).
Figure 3. Procavia capensis.
Table 8. Records of infections of afrotherian with parasitic protozoa, including the host
and parasite species as well as the place and reference numbers.
Afrotheria
Host
Rock Hyraxes
Procavia capensis
Bush hyrax
Heterohyrax brucei
Southern tree hyrax
Dendrohyrax arboreus
Amazonian manatee
Trichechus inunguis
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Ref. number
Disease agent
Place
Leishmania tropica
Israel
[73]
Leishmania aethiopica
Ethiopia
[74]
Leishmania aethiopica
Kenya
[74]
Leishmania aethiopica
Africa
[74]
Cryptosporidium spp.
Brazil
[75]
Giardia sp.
Brazil
[75]
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Figure 4. Dasypus novemcictus.
Table 9. Records of infections of Xenarthra with parasitic protozoa, including the host
and parasite species as well as the place and reference numbers.
Xenarthra
Host
Nine-banded armadillo
Dasypus novemcinctus
Six-banded armadillo
Euphractus sexcinctus
Hairy armadillo
Chaetophractus spp.
Two-toed sloth
Choloepus didactylus
Hoffmann’s two-toed sloth
Choloepus hoffmanni
Maned sloth
Bradypus torquatus
Brown-throated sloth
Bradypus variegatus
Collared anteater
Tamandua tetradactyla
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Disease agent
Place
Ref. number
Leishmania spp
Brazil
[76]
Trypanosoma cruzi
Paraguay
[71]]
Trypanosoma cruzi
Bolivia
[77]
Trypanosoma cruzi
Colombia
[77]
Leishmania naiffi
Brazil
[78]
Trypanosoma cruzi
Paraguay
[71]
Trypanosoma cruzi
Paraguay
[71]
Trypanosoma preguici
Brazil
[71]
Trypanosoma leeuwenhoeki
Panama
[71]
Endotrypanum schaudinni
Brazil
[79]
Leishmania shawi
NS
[74]
Leishmania guyanensis
NS
[74]
Leishmania panamensis
NS
[74]
Leishmania colombiensis
NS
[74]
Trypanosoma cruzi
Brazil
[80]
Leishmania shawi
NS
[74]
Trypanosoma legeri
Brazil
[71]
Leishmania amazonensis
Brazil
[74]
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Euarchonta
The Euarchonta have been proposed as encompassing three extant orders: the
Scandentia or treeshrews, the Dermoptera or colugos, and the Primates (Figure
5, Table 10).
Figure 5. Leontopithecus rosalia.
Table 10. Records of infections of Euarchonta with parasitic protozoa, including the host
and parasite species as well as the place and reference numbers.
Euarchonta
Host
Common squirrel monkey
Saimiri sciureus
Pygmy marmoset
Cebuella pygmaea
White-lipped tamarin
Saguinus labiatus
Brown-mantled tamarin
Saguinus fuscicollis
Red-handed tamarin
Saguinus midas
Pied tamarin
Saguinus bicolor
Ochraceus bare-face tamarin
Saguinus ochraceus
Red-bellied titi monkey Callicebus
maloch cripeus
Red-bellied titi monkey Callicebus
maloch
Purus red howler
Alouatta p. stramineus
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Disease agent
Place
Ref. number
Trypanosoma rangeli
Brazil
[70]
Trypanosoma saimiri
Brazil
[70]
Toxoplasma gondii
London
[81]
Trypanosoma rangeli
Brazil
[70]
Trypanosoma rangeli
Brazil
[70]
Trypanosoma rangeli
Brazil
[70]
Trypanosoma cruzi
Brazil
[80]
Trypanosoma cruzi
Brazil
[80]
Trypanosoma cruzi
Brazil
[80]
Trypanosoma rangeli
Brazil
[70]
Trypanosoma cruzi
Brazil
[80]
Trypanosoma rangeli
Brazil
[70]
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Continued
Black titi
Callicebus lugens
Gracile capuchin monkeys
Cebus spp
White-fronted capuchin
Cebus albifrons
Tufted capuchin
Cebus apella
Golden-headed lion tamarin
Leontopithecus chrysomelas
Golden lion tamarin
Leontopithecus rosalia
Black lion tamarin
Leontopithecus chrysopygus
Black bearded saki
Chiropotes satanas
Black-striped capuchin
Sapajus libidinosus
Red-handed howler
Alouatta belzebul
Night monkeys
Aotus sp.
Black-headed night monkey
Aotus nigriceps
Black-tufted marmoset
Callithrix penicillata
Gold-and-white marmoset
Callithrix chrysoleuca
Bornean orangutan
Pongo pygmaeus
Blue monkey
Cercopithecus mitis
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Trypanosoma rangeli
Brazil
[70]
Leishmania shawi
Brazil
[79]
Trypanosoma cruzi
Brazil
[80]
Leishmania shawi
NS
[74]
Trypanosoma cruzi
Brazil
[38]
Trypanosoma cruzi
Brazil
[38]
Trypanosoma cruzi
Brazil
[80]
Leishmania shawi
NS
[74]
Trypanosoma cruzi
Brazil
[38]
Trypanosoma cruzi
Brazil
[38]
Trypanosoma cruzi
Bolivia
[77]
Trypanosoma cruzi
Brazil
[80]
Trypanosoma minasense
Brazil
[82]
Trypanosoma cruzi
Brazil
[80]
Plasmodium pitheci
Malaysia
[83]
Plasmodium silvaticum
Malaysia
[83]
Leishmania infantum
Spain
[84]
Entamoeba histolytica
Indonesia
[85]
Entamoeba coli
Indonesia
[85]
Entamoeba hartmanni
Indonesia
[85]
Endolimax nana
Indonesia
[85]
Iodamoeba buetschlii
Indonesia
[85]
Blastocystis spp
Indonesia
[85]
Balantidium spp
Indonesia
[85]
Giardia spp
Indonesia
[85]
Entamoeba histolytica
Africa
[85]
Entamoeba coli
Africa
[85]
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Continued
Grivet
Cercopithecus aethiops
Mantled guereza
Colobus guereza
Angola colobus
Colobus angolensis
Ugandan red colobus
Piliocolobus tephrosceles
Balantidium spp
Africa
[85]
Entamoeba histolytica
Africa
[85]
Entamoeba coli
Africa
[85]
Balantidium spp
Africa
[85]
Leishmania major
Africa
[74]
Entamoeba histolytica
Uganda
[85]
Entamoeba coli
Uganda
[85]
Entamoeba histolytica
Uganda
[85]
Entamoeba coli
Uganda
[85]
Entamoebahistolytica
Uganda
[85]
Entamoeba coli
Uganda
[85]
Glires
Glires is a clade comprised by rodents and lagomorphs (rabbits, hares, and
pikas) forming a monophyletic group. It is a very diverse group with a worldwide distribution (Figure 6, Table 11).
Eulipotyphla
Eulipotyphla was suggested by molecular methods of phylogenetic reconstruction and includes the hedgehogs and gymnures, solenodons, the desmans,
moles, and shrew-like moles and true shrews (Figure 7, Table 12).
Chiroptera
The chiropterans group is composed by the bats, they present the forelegs
adapted to wings being the only mammals naturally able of flying.
After the rodents, they are the biggest mammals order, consisting of about
20% of all known species (Figure 8, Table 13).
Cetartiodactyla
Cetartiodactyla is the taxon that includes all even hoofed mammals including
deer, camels, pigs and others. The cetaceans are also included, containing more
than 450 terrestrial species, three semiaquatic, as well as close eighty aquatic
representatives (Figure 9, Table 14).
Perissodactyla
The Perissodactyla are hoofed animals known commonly as odd-toed ungulates, it is composed of herbivorous terrestrial mammals, which the number of
toes has been reduced from the ancestral with five to one in horses, three in rhinoceroses, and in the tapirs, four on the front feet and three on the hind feet.
They have been classified into three extant families the Equidae and Tapiridae
comprised of one genus with respectively nine and four species, and the Rhinocerotidae with four genera and five species (Figure 10, Table 15).
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Figure 6. Eliomys quercinus.
Figure 7. Sorex araneus.
Figure 8. Desmodus rotundus.
Figure 9. Dama dama.
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Figure 10. Ceratotherium simum.
Table 11. Records of infections of Glires with parasitic protozoa, including the host and
parasite species as well as the place and reference numbers.
Glires
Host
Drab Atlantic tree-rat
Phyllomys dasythrix
South American water rat
Nectomys squamipes
Common punaré
Thrichomys apereoides
Garden dormouse
Eliomys quercinus
Sumichrast’s vesper rat
Nyctomys sumichrasti
Disease agent
Place
Ref. number
Trypanosoma rangeli
Brazil
[70]
Trypanosoma cruzi
Brazil
[80]
Leishmania infantum
Brazil
[86]
Leishmania infantum
Brazil
[86]
Trypanosoma blanchardi
France
[70]
Leishmania mexicana
NS
[74]
Leishmania amazonensis
NS
[74]
Leishmania major
Iran
[87]
Leishmania major
Central Asia
[74]
Leishmania turanica
Iran
[87]
Leishmania gerbilli
Mongolia
[74]
Leishmania gerbilli
China
[74]
Leishmania major
Africa
[74]
Leishmania major
Iran
[87]
Leishmania spp
Nigeria
[88]
Leishmania major
Africa
[74]
Leishmania major
Africa
[74]
Large-headed rice rat
Hylaeamys megacephalus *referred as
Oryzomys capito
Great gerbil
Rhombomys opimus
Greater Egyptian gerbil
Gerbillus pyramidum
Indian gerbil
Tatera indica
Tatera gambiana
Emin’s gerbil
Taterillus emini
Fringe-tailed gerbil
Gerbilliscus robustus
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Continued
Indian desert gerbil
Meriones hurrianae
Libyan jird
Meriones libycus
Shaw’s jird
Meriones shawi
Sundevall’s jird
Meriones crassus
Desmarest’s spiny pocket mouse
Heteromys desmarestianus
Short-tailed bandicoot rat
Nesokia indica
Fat sand rat
Psammomys obesus
Unstriped grass mice
Arvicanthis spp
Multimammate mouse
Mastomys spp
Natal multimammate mouse
Mastomys natalensis
Guinea multimammate mouse
Mastomys erythroleucus
Fat sand rat
Psammomys obesus
Bank vole
Myodes glareolus
Northern short-tailed shrew
Blarina brevicauda
Wood mouse
Apodemus sylvaticus
Yellow-necked mouse
Apodemus flavicollis
Gambian pouched rat
Cricetomys gambianus
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Leishmania major
Iran
[87]
Leishmania major
India
[74]
Leishmania major
Iran
[87]
Leishmania major
Central Asia
[74]
Leishmania major
Morocco
[74]
Leishmania major
NS
[74]
Leishmania mexicana
NS
[74]
Leishmania panamensis
NS
[74]
Leishmania major
Iranian
Khuzestan
[74]
Leishmania major
Saudi Arabia
[74]
Leishmania major
Africa
[74]
Leishmania major
Africa
[74]
Leishmania major
Nigeria
[88]
Leishmania major
Africa
[74]
Leishmania major
Libya
[74]
Leishmania major
Tunisia
[74]
Trypanosoma evotomys
Hungary
[89]
Hepatozoon erhardovae
Hungary
[89]
Eimeria brevicauda
USA
[90]
Isospora brevicauda
USA
[90]
Cryptosporidium parvum
UK
[91]
Trypanosoma grosi
Hungary
[89]
Hepatozoon sylvatici
Hungary
[89]
Cryptosporidium parvum
Poland
[89]
Trypanosoma grosi
Hungary
[89]
Hepatozoon sylvatici
Hungary
[89]
Leishmania aethiopica
Africa
[74]
Open Journal of Animal Sciences
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Continued
Fat sand rat
Psammomys obesus
Kaiser’s rock rat
Aethomys kaiseri
European hamster
Cricetus cricetus
Short-tailed vole
Microtus agrestis
Leishmania major
Algeria
[74]
Leishmania major
Africa
[74]
Trypanosoma
rabinowitschae
France
[70]
Trypanosoma microti
England
[70]
Cryptosporidium parvum
Finland
[91]
Cryptosporidium parvum
Poland
[91]
Cryptosporidium parvum
Finland
[91]
Cryptosporidium parvum
UK
[91]
Leishmania deanei
Brazil
[79]
Leishmania panamensis
Panama
[74]
Leishmania hertigi
Panama
[79]
Leishmania mexicana
USA
[74]
Leishmania mexicana
Belize
[74]
Leishmania mexicana
Belize
[74]
Leishmania infantum
Bolivia
[86]
Leishmania enriettii
Brazil
[79]
Trypanosoma cruzi
Brazil
[77]
Trypanosoma cruzi
Brazil
[80]
Leishmania panamensis
NS
[74]
Leishmania braziliensis
Brazil
[74]
NS
[74]
Leishmania amazonensis
Brazil
[74]
Leishmania amazonensis
French Guyana
[74]
Leishmania infantum
Colombia
[86]
Leishmania guyanensis
NS
[74]
Bank vole
Myodes glareolus *referred as
Clethrionomys glareolus
Prehensile-tailed porcupines
Coendou spp
Southern Plains woodrat
Neotoma micropus
Desmarest’s spiny pocket mouse
Heteromys desmarestianus
Big-eared climbing rat
Ototylomys phyllotis
Brazilian porcupine
Coendou prehensilis
Guinea pigs
Cavia spp
Common agouti
Dasyprocta aguti
Brazilian marsh rat
Holochilus brasiliensis
South American grass mice
Akodon spp
Montane grass mouse
Akodon montensis
Hispid cotton rat
Leishmania mexicana
Sigmodon hispidus
South American spiny rats
Proechimys spp
Colombian spiny-rat
Proechimys canicollis
Cuvier’s spiny-rat
Proechimys cuvieri
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Continued
Guyenne spiny-rat
Proechimys guyannensis
Tome’s spiny rat
Proechimys semispinosus
Ihering’s Atlantic spiny-rat
Trinomys iheringi
Red squirrel
Sciurus vulgaris
Eastern gray squirrel
Sciurus carolinensis
Capybara
Hydrochoerus hydrochaeris
Capybara
Hydrochoerus hydrochaeris
Capybara
Hydrochoerus hydrochaeris
Capybara
Hydrochoerus hydrochaeris
Lowland paca
Cuniculus paca
Unstriped ground squirrel
Xerus rutilus
European rabbit
Oryctolagus cuniculus
Leishmania amazonensis
NS
[74]
Leishmania amazonensis
NS
[74]
Leishmania guyanensis
NS
[74]
Leishmania panamensis
NS
[74]
Leishmania braziliensis
Brazil
[74]
Leishmania amazonensis
NS
[74]
Cryptosporidium parvum
USA
[91]
Trypanosoma evansi
Brazil
[92]
Trypanosoma evansi
Colombia
[93]
Trypanosoma evansi
Peru
[94]
Trypanosoma evansi
Venezuela
[95]
Leishmania lainsoni
Brazil
[74]
Leishmania major
Africa
[74]
Cryptosporidium parvum
Mainland
Britain
[91]
Table 12. Records of infections of Eulipotyphla with parasitic protozoa, including the
host and parasite species as well as the place and reference numbers.
Eulipotyphla
Host
European hedgehog
Erinaceus europaeus
Common shrew
Sorex araneus
Pygmy shrew
Sorex minutus
Cinereous shrew
Sorex cinereus
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Disease agent
Place
Ref. number
Cryptosporidium parvum
Mainland Britain
[91]
Cryptosporidium parvum
Mainland Britain
[91]
Hepatozoon spp
Hungary
[89]
Cryptosporidium parvum
Poland
[91]
Trypanosoma spp
England
[96]
Cryptosporidium parvum
Mainland Britain
[91]
Trypanosoma spp
Hungary
[89]
Eimeria palustris
USA
[90]
Eimeria palustris
Canada
[90]
Open Journal of Animal Sciences
J. C. A. Carreira et al.
Continued
Maryland shrew
Sorex fontinalis
Smoky shrew
Sorex fumeus
Prairie shrew
Sorex haydeni
Southeastern shrew
Sorex longirostris
Ornate shrew
Sorex ornatus
Pacific shrew
Sorex pacificus
American water shrew
Sorex palustris
Inyo shrew
Sorex tenellus
Trowbridge’s shrew
Sorex trowbridgii
Long-clawed shrew
Sorex unguiculatus
Vagrant shrew
Sorex vagrans
Eimeria palustris
USA
[90]
Eimeria palustris
USA
[90]
Eimeria fumeus
USA
[90]
Eimeria vagrantis
USA
[90]
Eimeria palustris
USA
[90]
Eimeria palustris
USA
[90]
Eimeria palustris
USA
[90]
Eimeria palustris
USA
[90]
Eimeria fumeus
USA
[90]
Eimeria palustris
USA
[90]
Isospora palustris
USA
[90]
Eimeria palustris
USA
[90]
Eimeria inyoni
USA
[90]
Eimeria palustris
USA
[90]
Eimeria vagrantis
USA
[90]
Eimeria fumeus
Japan
[90]
Isospora palustris
Japan
[90]
Eimeria palustris
USA
[90]
Eimeria vagrantis
USA
[90]
Eimeria fumeus
USA
[90]
Isospora palustris
USA
[90]
Table 13. Records of infections of Chiroptera with parasitic protozoa, including the host
and parasite species as well as the place and reference numbers.
Chiroptera
Host
Little red flying-fox
Pteropus scapulatus
White-lined broad-nosed bat
Platyrrhinus lineatus
Brazilian brown bat
Eptesicus brasiliensis
Free-tailed bat
Tadarida spp
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Disease agent
Place
Ref. number
Trypanosoma teixeirae
Australia
[97]
Trypanosoma rangeli
Brazil
[97]
Trypanosoma dionisii
Brazil
[97]
Trypanosoma erneyi
Mozambique
[97]
Open Journal of Animal Sciences
J. C. A. Carreira et al.
Continued
Common pipistrelle
Pipistrellus pipistrellus
Lander’s horseshoe bat
Rhinolophus landeri
Sundevall’s roundleaf bat
Hipposideros caffer
Yellowish myotis
Myotis levis
Seba’s short-tailed bat
Carollia perspicillata
Greater spear-nosed bat
Phyllostomus hastatus
Pale spear-nosed bat
Phyllostomus discolor
Fringe-lipped bat
Trachops cirrhosus
White-winged vampire bat
Diaemus youngi
Common vampire bat
Desmodus rotundus
Tailed tailless bat
Anoura caudifera
Pallas’s long-tongued bat
Glossophaga soricina
Trypanosoma vespertilionis
England
[97]
Trypanosoma livingstonei
Mozambique
[97]
Trypanosoma livingstonei
Mozambique
[97]
Trypanosoma cruzi Tcbat
Brazil
[97]
Trypanosoma cruzi marinkellei
Brazil
[97]
Leishmania infantum
Venezuela
[86]
Trypanosoma cruzi
Peru
[98]
Leishmania braziliensis
Brazil
[99]
Trypanosoma cruzi
Peru
[98]
Trypanosoma cruzi
Peru
[98]
Trypanosoma cruzi
Peru
[98]
Trypanosoma cruzi marinkellei
Brazil
[99]
Leishmania braziliensis
Brazil
[99]
Trypanosoma cruzi marinkellei
Brazil
[99]
Trypanosoma dionisii
Brazil
[99]
Trypanosoma wauwau
Brazil
[99]
Trypanosoma cruzi marinkellei
Brazil
[99]
Table 14. Records of infections of cetartiodactylan with parasitic protozoa, including the
host and parasite species as well as the place and reference numbers.
Cetartiodactyla
Host
White-tailed deer
Odocoileus virginianus
European roe deer
Capreolus capreolus
Peters’s duiker
Cephalophus callipygus
Fallow deer
Dama dama
Reeves’s muntjac
Muntiacus reevesi
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Disease agent
Place
Ref. number
Toxoplasma gondii
USA
[26]
Babesia odocoilei
USA
[26]
Theileria cervi,
USA
[26]
Cryptosporidium parvum
Denmark
[91]
Haemosporidian
Africa
[100]
Cryptosporidium parvum
Mainland Britain
[91]
Cryptosporidium parvum
Mainland Britain
[91]
Open Journal of Animal Sciences
J. C. A. Carreira et al.
Continued
Black-fronted duiker
Cephalophus nigrifrons
Blue duiker
Cephalophus monticola
Bay duiker
Cephalophus dorsalis
Blue whale
Balaenoptera musculus
Sei whale
Balaenoptera borealis
Fin Whale
Balaenoptera physalus
killer whale
Orcinus orca
Common bottlenose dolphin
Tursiops truncatus
Pygmy sperm whale
Kogia breviceps
Dwarf sperm whale
Kogia sima
Guiana dolphin
Sotalia guianensis
Amazonian manatee
Trichechus inunguis
West Indian manatee
Trichechus manatus
Haemosporidian
Africa
[100]
Haemosporidian
Africa
[100]
Haemosporidian
Africa
[100]
Entamoeba
Atlantic Ocean
[101]
Giardia
Atlantic Ocean
[101]
Entamoeba
Atlantic Ocean
[101]
Giardia
Atlantic Ocean
[101]
Entamoeba
Atlantic Ocean
[101]
Balantidium
Atlantic Ocean
[101]
Toxoplasma gondii
Brazil
[102]
Toxoplasma gondii
Pacific Ocean
[103]
Toxoplasma gondii
Brazil
[102]
Giardia
Brazil
[75]
Giardia
Brazil
[75]
Giardia sp.
Brazil
[75]
Toxoplasma gondii
Brazil
[102]
Cryptosporidium spp.
Brazil
[75]
Cryptosporidium spp.
Brazil
[75]
Giardia sp.
Brazil
[75]
Cryptosporidium spp.
Brazil
[75]
Giardia sp.
Brazil
[75]
Pholidota
The Pholidota is commonly known as pangolins or scaly anteaters. This group
of mammals is composed by just seven living species, four in Africa and three in
Southeast Asia.
They look like armadillos or anteaters that like them also eat insects, have long
tongues, strong digging limbs, and reduced or missing teeth.
The pangolins have already been clustered with armadillos and anteaters in
Edentata; however, their similarities are now considered as a result of convergent evolution (Figure 11, Table 16).
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Table 15. Records of infections of Perissodactyla with parasitic protozoa, including the
host and parasite species as well as the place and reference numbers.
Perissodactyla
Host
South American tapir
Tapirus terrestris
Black rhinoceros
Diceros bicornis
White rhinoceros
Ceratotherium simum
Sumatran rhinoceros
Dicerorhinus sumatrensis
Disease agent
Place
Ref. number
Trypanosoma terrestris
Brazil
[104]
Theileria equi
Brazil
[105]
Trypanosoma congolense
Kenia
[106]
Trypanosoma brucei
Tanzania
[107]
Trypanosoma godfreyi
Kenia
[106]
Trypanosoma simiae
Kenia
[106]
Theileria spp
Kenia
[106]
Trypanosoma vivax
Kenia
[108]
Theileria spp
Kenia
[106]
Theileria bicornis
South Africa
[109]
Theileria equi
South Africa
[109]
Trypanosoma evansi
Malaysia
[110]
Table 16. Records of infections of Pholidota with parasitic protozoa, including the host
and parasite species as well as the place and reference numbers.
Pholidota
Host
Pangolin
Phataginus tricuspis
Javan pangolin
Manis javanica
African Tree Pangolin
Phataginus tricuspis
Indian pangolin
Manis crassicaudata
Long-tailed pangolin
Manis tetradactyla
Temminck’s ground pangolin
Manis temminckii
Disease agent
Place
Ref. number
Haemosporidian
Africa
[100]
Eimeria tenggilingi
Singapore
[111]
Eimeria nkaka
Angola
[111]
Trypanosoma brucei
Cameroon
[112]
Trypanosoma vivax
Cameroon
[112]
Toxoplasma gondii
Belgium
[112]
Trypanosoma brucei
Cameroon
[112]
Trypanosoma vivax
Cameroon
[112]
Piroplasma spp
London
[112]
Carnivora
The Carnivora compound the most varied in size mammalian order, they
have teeth and claws evolved for predation.
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Figure 11. Manis spp.
Figure 12. Leopardus pardalis.
Table 17. Records of infections of Carnivora with parasitic protozoa, including the host
and parasite species as well as the place and reference numbers.
Host
Bush dog
Speothos venaticus
Gray fox
Urocyon cinereoargenteus
Crab-eating fox
Cerdocyon thous
Maned wolf
Chrysocyon brachyurus
Maned wolf
Hoary fox
Lycalopex vetulus
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Disease agent
Place
Ref. number
Leishmania infantum
Brazil
[89]
Toxoplasma gondii
USA
[113]
Trypanosoma cruzi
Brazil
[114]
Leishmania infantum
Brazil
[89]
Trypanosoma cruzi
Brazil
[114]
Leishmania infantum
Brazil
[89]
Trypanosoma cruzi
Brazil
[114]
Open Journal of Animal Sciences
J. C. A. Carreira et al.
Continued
Andean fox
Lycalopex culpaeus
South American gray fox
Lycalopex griseus
Golden jackal
Canis aureus
Grey wolf
Canis lupus
Corsac fox
Vulpes corsac
Red fox
Vulpes vulpes
Fennec fox
Vulpes zerda
Pampas fox
Lycalopex gymnocercus
Raccoon dog
Nyctereutes procyonoides
European badger
Meles meles
Ocelot
Leopardus pardalis
Cougar
Puma concolor
Ring-tailed coati
Nasua nasua
Leishmania infantum
Brazil
[89]
Trypanosoma cruzi
Colombia
[114]
Trypanosoma cruzi
Argentina
[114]
Trypanosoma cruzi
Colombia
[114]
Leishmania infantum
Algeria
[115]
Leishmania infantum
Iran
[89]
Leishmania infantum
Central Asia
[74]
Leishmania infantum
NS
[74]
Cryptosporidium parvum
Mainland Britain
[91]
Leishmania infantum
Africa
[74]
Trypanosoma cruzi
Argentina
[114]
Leishmania donovani
NS
[74]
Leishmania infantum
NS
[74]
Cryptosporidium parvum
Mainland Britain
[91]
Trypanosoma cruzi
Brazil
[114]
Trypanosoma cruzi
Brazil
[114]
Trypanosoma cruzi
Brazil
[114]
Trypanosoma evansi
Brazil
[116]
Leishmania shawi
Iberian lynx
Leishmania infantum
Lynx pardinus
Serval
Leptailurus serval (*)
Egyptian mongoose
Herpestes ichneumon
Raccoon
Procyon lotor
Crab-eating raccoon
Procyon cancrivorus
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Leishmania donovani
NS
Spain
NS
[74]
[89]
[74]
Leishmania infantum
Spain
[89]
Toxoplasma gondii
USA
[113]
Trypanosoma cruzi
USA
[77]
Trypanosoma cruzi
Brazil
[114]
Open Journal of Animal Sciences
J. C. A. Carreira et al.
Continued
Striped skunk
Mephitis mephitis
Common genet
Genetta genetta
Molina’s hog-nosed skunk
Conepatus chinga
American mink
Neovison vison
Tayra
Eira barbara
Neotropical river otter
Lontra longicaudis
Giant river otter
Pteronura brasiliensis
Lesser grison
Galictis cuja
Greater grison
Galictis vittata
Kinkajou
Potos flavus
Kuril harbour seal
Phoca vitulina
Spotted seal
Phoca largha
Mediterranean monk seal
Monachus monachus
Toxoplasma gondii
USA
[113]
Leishmania infantum
Spain
[89]
Leishmania donovani
NS
[74]
Trypanosoma cruzi
Argentina
[114]
Toxoplasma gondii
USA
[113]
Trypanosoma cruzi
Brazil
[114]
Trypanosoma cruzi
Argentina
[114]
Cryptosporidium spp.
Brazil
[75]
Giardia sp.
Brazil
[75]
Cryptosporidium spp
Brazil
[75]
Giardia sp.
Brazil
[75]
Trypanosoma cruzi
Argentina
[114]
Trypanosoma cruzi
Brazil
[114]
Trypanosoma cruzi
Brazil
[114]
Trypanosoma cruzi
Colombia
[114]
Leishmania amazonensis
NS
[74]
Toxoplasma gondii
Japan
[117]
Neospora caninum
Japan
[117]
Toxoplasma gondii
Japan
[117]
Neospora caninum
Japan
[117]
Leishmania infantum
Turkey
[118]
NS: Not specified, (*) Referred as Felix serval.
Generally, the term carnivore is applied to members of this group as
meat-eating animals.
Although several carnivorans like in felids the diet is composed almost exclusively of meat, it may vary, bears for example are omnivorous and the giant
panda is mainly herbivore. Many hunt in groups and present a social behavior
and with some exceptions, they have six incisors and two narrowed canines in
each jaw (Figure 12, Table 17).
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Conflicts of Interest
The authors declare no conflicts of interest regarding the publication of this
paper.
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