Gastrointestinal parasites in captive and free-ranging Cebus albifrons in the Western Amazon, Ecuador

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Abstract

Currently, there is a lack of surveys that report the occurrence of gastrointestinal parasites in the white-headed capuchin monkey ( Cebus albifrons). We therefore assessed the presence and richness (= number of different parasite genera) of parasites in C. albifrons in wildlife refuges (n = 11) and in a free-ranging group near a human village (n = 15) in the Ecuadorian Amazon. In the 78 samples collected (median of 3 samples per animal), we identified a total of 6 genera of gastrointestinal parasites, representing protozoa, nematodes, acanthocephalans and cestodes. We observed a high prevalence (84%) across the 26 individuals, with the most prevalent parasite being Strongyloides sp. (76.9%), followed by Hymenolepis sp. (38.5%) and Prosthenorchis elegans (11.5%). We found Entamoeba histolytica/dispar/moskovskii/nuttalli and Capillaria sp. in only a minority of the animals (3.8%). In addition, we observed unidentified strongyles in approximately one-third of the animals (34.6%). We found a total of 6 parasite genera for the adult age group, which showed higher parasite richness than the subadult age group (5) and the juvenile age group (3). Faecal egg/cyst counts were not significantly different between captive and free-ranging individuals or between sexes or age groups. The free-ranging group had a higher prevalence than the captive group; however, this difference was not significant. The only genus common to captive and free-ranging individuals was Strongyloides sp. The high prevalence of gastrointestinal parasites and the presence of Strongyloides in both populations support results from previous studies in Cebus species. This high prevalence could be related to the high degree of humidity in the region. For the free-ranging group, additional studies are required to gain insights into the differences in parasite prevalence and intensity between age and sex groups. Additionally, our study demonstrated that a serial sampling of each individual increases the test sensitivity.

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Highlights

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This study brings new information about primate parasites to Ecuador.
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We analyse the prevalence, richness and FECC among the two habitats, sex and age.
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Adults harbour more genera of parasites than subadults and juveniles.
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Sampling effort was essential to find a good number of parasites genera.
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E. histolytica/dispar and P. elegans were found only in captive individuals.

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Most cited references 88

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Comparative tests of parasite species richness in primates.

Menna Jones, Sonia Altizer, Charles Nunn … (2003)

Some hosts harbor diverse parasite communities, whereas others are relatively parasite free. Many factors have been proposed to account for patterns of parasite species richness, but few studies have investigated competing hypotheses among multiple parasite communities in the same host clade. We used a comparative data set of 941 host-parasite combinations, representing 101 anthropoid primate species and 231 parasite taxa, to test the relative importance of four sets of variables that have been proposed as determinants of parasite community diversity in primates: host body mass and life history, social contact and population density, diet, and habitat diversity. We defined parasites broadly to include not only parasitic helminths and arthropods but also viruses, bacteria, fungi, and protozoa, and we controlled for effects of uneven sampling effort on per-host measures of parasite diversity. In nonphylogenetic tests, body mass was correlated with total parasite diversity and the diversity of helminths and viruses. When phylogeny was taken into account, however, body mass became nonsignificant. Host population density, a key determinant of parasite spread in many epidemiological models, was associated consistently with total parasite species richness and the diversity of helminths, protozoa, and viruses tested separately. Geographic range size and day range length explained significant variation in the diversity of viruses.

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Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis).

Brenda McCowan, Lynne Isbell, Edward Atwill … (2013)

Although network analysis has drawn considerable attention as a promising tool for disease ecology, empirical research has been hindered by limitations in detecting the occurrence of pathogen transmission (who transmitted to whom) within social networks. Using a novel approach, we utilize the genetics of a diverse microbe, Escherichia coli, to infer where direct or indirect transmission has occurred and use these data to construct transmission networks for a wild giraffe population (Giraffe camelopardalis). Individuals were considered to be a part of the same transmission chain and were interlinked in the transmission network if they shared genetic subtypes of E. coli. By using microbial genetics to quantify who transmits to whom independently from the behavioural data on who is in contact with whom, we were able to directly investigate how the structure of contact networks influences the structure of the transmission network. To distinguish between the effects of social and environmental contact on transmission dynamics, the transmission network was compared with two separate contact networks defined from the behavioural data: a social network based on association patterns, and a spatial network based on patterns of home-range overlap among individuals. We found that links in the transmission network were more likely to occur between individuals that were strongly linked in the social network. Furthermore, individuals that had more numerous connections or that occupied 'bottleneck' positions in the social network tended to occupy similar positions in the transmission network. No similar correlations were observed between the spatial and transmission networks. This indicates that an individual's social network position is predictive of transmission network position, which has implications for identifying individuals that function as super-spreaders or transmission bottlenecks in the population. These results emphasize the importance of association patterns in understanding transmission dynamics, even for environmentally transmitted microbes like E. coli. This study is the first to use microbial genetics to construct and analyse transmission networks in a wildlife population and highlights the potential utility of an approach integrating microbial genetics with network analysis. © 2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society.

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Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda.

Innocent B. Rwego, Gilbert Isabirye-Basuta, Thomas R Gillespie … (2008)

Habitat overlap can increase the risks of anthroponotic and zoonotic pathogen transmission between humans, livestock, and wild apes. We collected Escherichia coli bacteria from humans, livestock, and mountain gorillas (Gorilla gorilla beringei) in Bwindi Impenetrable National Park, Uganda, from May to August 2005 to examine whether habitat overlap influences rates and patterns of pathogen transmission between humans and apes and whether livestock might facilitate transmission. We genotyped 496 E. coli isolates with repetitive extragenic palindromic polymerase chain reaction fingerprinting and measured susceptibility to 11 antibiotics with the disc-diffusion method. We conducted population genetic analyses to examine genetic differences among populations of bacteria from different hosts and locations. Gorilla populations that overlapped in their use of habitat at high rates with people and livestock harbored E. coli that were genetically similar to E. coli from those people and livestock, whereas E. coli from gorillas that did not overlap in their use of habitats with people and livestock were more distantly related to human or livestock bacteria. Thirty-five percent of isolates from humans, 27% of isolates from livestock, and 17% of isolates from gorillas were clinically resistant to at least one antibiotic used by local people, and the proportion of individual gorillas harboring resistant isolates declined across populations in proportion to decreasing degrees of habitat overlap with humans. These patterns of genetic similarity and antibiotic resistance among E. coli from populations of apes, humans, and livestock indicate that habitat overlap between species affects the dynamics of gastrointestinal bacterial transmission, perhaps through domestic animal intermediates and the physical environment. Limiting such transmission would benefit human and domestic animal health and ape conservation.

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Author and article information

Contributors

Sarah Martin-Solano

Gabriel A. Carrillo-Bilbao

William Ramirez

Maritza Celi-Erazo

Marie-Claude Huynen

Bruno Levecke

Washington Benitez-Ortiz

Bertrand Losson

Journal

Journal ID (nlm-ta): Int J Parasitol Parasites Wildl

Journal ID (iso-abbrev): Int J Parasitol Parasites Wildl

Title: International Journal for Parasitology: Parasites and Wildlife

Publisher: Elsevier

ISSN (Electronic): 2213-2244

Publication date PMC-release: 19 June 2017

Publication date Collection: December 2017

Publication date (Electronic): 19 June 2017

Volume: 6

Issue: 3

Pages: 209-218

Affiliations

[a ]Primatology Research Group, Behavioural Biology Unit, Department of Biology, Ecology and Evolution, Faculty of Science, University of Liège, Quai van Beneden 22, 4020 Liège, Belgium

[b ]Instituto de Salud Pública y Zoonosis - CIZ, Universidad Central del Ecuador, PO BOX: 17-03-100, Quito, Ecuador

[c ]Estación Científica Juri Juri Kawsay, Universidad Central del Ecuador, Ciudadela Universitaria, UCE, Quito, Ecuador

[d ]Departamento Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Av. General Rumiñahui s/n, PO BOX. 171-5-231B, Sangolquí, Ecuador

[e ]Carrera de Ciencias Naturales y del Ambiente, Biología y Química, Universidad Central del Ecuador, Ciudadela Universitaria, UCE, Quito, Ecuador

[f ]Primate Behavior Program, Central Washington University, 400 E University Way, Ellensburg, WA 98926, USA

[g ]Laboratory of Parasitology, Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Salisburylaan 133, B-9820 Merelbeke, Ghent University, Belgium

[h ]Department for Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, Boulevard de Colonster 20, 4000 Liège, University of Liège, Belgium

Author notes

[∗ ]Corresponding author. Primatology Research Group, Behavioural Biology Unit, Department of Biology, Ecology and Evolution, Faculty of Science, University of Liège, Quai van Beneden 22, 4020 Liège, Belgium.Primatology Research GroupBehavioural Biology UnitDepartment of Biology, Ecology and EvolutionFaculty of ScienceUniversity of LiègeQuai van Beneden 22Liège4020Belgium sarahmartinsolano@ 123456gmail.com sarah.martin@ 123456doct.ulg.ac.be ssmartin@ 123456espe.edu.ec

Article

Publisher ID: S2213-2244(17)30064-0

DOI: 10.1016/j.ijppaw.2017.06.004

PMC ID: 5544475

PubMed ID: 28808619

SO-VID: 5213041e-d6f1-4e02-aace-e916dccb65e5

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

History

Date received : 19 June 2015

Date revision received : 9 June 2017

Date accepted : 16 June 2017

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Gastrointestinal parasites in captive and free-ranging Cebus albifrons in the Western Amazon, Ecuador

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Abstract

Graphical abstract

Highlights

Related collections

Parasite

Most cited references 88

Comparative tests of parasite species richness in primates.

Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis).

Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda.

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Cited by 8

Most referenced authors 815