Comparison of Gastrointestinal Parasite Communities in Vervet
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Integrative Zoology 2017; 12: 512–520 doi: 10.1111/1749-4877.12270 1 SHORT COMMUNICATION 1 2 2 3 3 4 4 5 5 6 6 7 Comparison of gastrointestinal parasite communities in vervet 7 8 8 9 monkeys 9 10 10 11 11 12 Kim VALENTA,1 Dennis TWINOMUGISHA,2 Kathleen GODFREY,1 Cynthia LIU,1 Valérie A. M. 12 13 3 2,4 1,2,5 13 14 SCHOOF, Tony L. GOLDBERG and Colin A. CHAPMAN 14 15 1McGill School of Environment, McGill University, Montreal, Quebec, Canada, 2Makerere University Biological Field Station, 15 16 Kampala, Uganda, 3Bilingual Biology Program, Department of Multidisciplinary Studies, Glendon Campus, York University, 16 17 Toronto, Ontario, Canada, 4Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin- 17 18 5 18 Madison, Madison, Wisconsin, USA and Wildlife Conservation Society, Bronx, New York, USA 19 19 20 20 21 21 22 Abstract 22 23 23 Globally, habitat degradation is accelerating, especially in the tropics. Changes to interface habitats can increase 24 24 environmental overlap among nonhuman primates, people, and domestic animals and change stress levels in 25 25 wildlife, leading to changes in their risk of parasite infections. However, the direction and consequences of 26 26 these changes are unclear, since animals may benefit by exploiting human resources (e.g., improving nutrition- 27 27 al health by eating nutritious crops) and decreasing susceptibility to infection, or interactions with humans may 28 28 lead to chronic stress and increased susceptibility to infection. Vervet monkeys are an excellent model to under- 29 29 stand parasitic disease transmission because of their tolerance to anthropogenic disturbance. Here we quantify 30 30 the gastrointestinal parasites of a group of vervet monkeys (Chlorocebus aethiops) near Lake Nabugabo, Ugan- 31 31 da, that frequently overlaps with people in their use of a highly modified environment. We compare the parasites 32 32 found in this population to seven other sites where vervet monkey gastrointestinal parasites have been identi- 33 33 fied. The vervets of Lake Nabugabo have the greatest richness of parasites documented to date. We discuss how 34 34 this may reflect differences in sampling intensity or differences in the types of habitat where vervet parasites 35 35 have been sampled. 36 36 37 Key Words: anthropogenic disturbance, disease, gastrointestinal parasite, habitat degradation, Nabugabo, 37 38 vervet, zoonotic disease 38 39 39 40 40 41 41 42 INTRODUCTION Nunn & Altizer 2006). For example, the number of para- 42 43 site eggs in the environment is lower in hot, dry months 43 44 Parasitism is fundamentally linked to the environ- compared to wetter months, and increased environmen- 44 45 ment and the condition of the host (Holt et al. 2003; tal moisture is positively related to prevalence and in- 45 46 tensity of infections (Appleton & Henzi 1993; Apple- 46 47 ton & Brain 1995; Larsen & Roepstorff 1999; Chapman 47 48 Correspondence: Kim Valenta, McGill School of Environment, et al. 2010, 2015). Environmental conditions also affect 48 49 McGill University, 3534 University St. H3A 2A7 Montreal, the host, altering susceptibility to parasite infections. 49 50 Quebec, Canada. Marginal environmental conditions can cause physio- 50 51 Email: [email protected] logical stress, and chronic stress can suppress the im- 51 512 © 2017 The Authors. Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Parasite communities in vervet monkeys 1 mune system leading to greater risk of infections (Black pogenically-modified landscape neighboring Lake Nab- 1 2 1994; Coe & Erickson 1997; Padgett & Glaser 2003). ugabo, Uganda. Vervet monkeys are extremely flexible 2 3 For example, in free-ranging chamois (Rupicapra rupi- in terms of diet and habitat use. Vervets are often found 3 4 capra), stress hormone levels and gastrointestinal and living in urban, peri-urban or agricultural environments, 4 5 lung helminth counts were found to co-vary through- sometimes co-existing with humans, as well as in undis- 5 6 out the year (Hoby et al. 2006). Similarly, primates ex- turbed savanna, and woodland, riverine systems. Vervet 6 7 periencing chronically elevated stress and depressed im- monkeys are considered pests because they frequent- 7 8 mune function have increased parasite burden and are ly crop raid or steal human food (Boulton et al. 1996; 8 9 at a higher risk of acquiring parasites than those that ex- Saj et al. 2001; Gillingham & Lee 2003; Chapman et al. 9 10 perience less stress (Muehlenbein 2006; Chapman et al. 2016). Because of their proximity to (and frequent inter- 10 11 2015). Such host–parasite-environment linkages mean action with) humans and their ability to live in habitats 11 12 that when people cause environmental change it can ranging from old-growth forest to cities, vervet mon- 12 13 have cascading effects on parasitism and the health of keys are a good model for understanding parasitic infec- 13 14 nonhuman hosts in those environments. tions in wildlife populations inhabiting highly anthro- 14 15 The effects on wild animals living in habitats mod- pogenic habitats. Here we present data on the largest 15 16 ified by humans are complex. However, given cur- sample of vervet gastrointestinal parasites collected to 16 17 rent trends in forest loss, cropland expansion and hu- date, and discuss our findings in light of anthropogenic 17 18 man population growth (Foley et al. 2011; Balmford et and habitat variables that may influence vervet parasite 18 19 al. 2012; Estrada 2013; Hansen et al. 2013; Phalan et richness. 19 20 al. 2013), it is reasonable to expect increasing effects 20 21 of environmental change on wildlife, including chang- MATERIALS AND METHODS 21 22 es in the nature of parasite infection. For example, pri- 22 23 mates that frequent areas heavily used by humans and The study took place on the shores of Lake Nab- 23 24 domesticated animals may be exposed to a higher di- ugabo, Masaka District, Central Uganda (0°22′–12°S, 24 25 versity of parasites than primates in undisturbed hab- 31°54′E) near McGill’s Lake Nabugabo Research Sta- 25 26 itats. Furthermore, primates in such anthropogenical- tion. Lake Nabugabo is a satellite lake of Lake Victo- 26 27 ly-disturbed locations may be chronically stressed due ria and lies at an elevation of 1136 m. The lake is most- 27 28 to frequent conflict with people and their domesticat- ly surrounded by wetlands, grasslands and patches of 28 29 ed animals, thereby increasing their susceptibility to in- swamp forest; however, a portion to the west side of 29 30 fection (Chapman et al. 2006). Alternatively, suscepti- the lake consists of farmers’ fields, degraded forest and 30 31 bility to parasites may decrease as primates gain access a few buildings. The area receives an average of 1348 31 32 to nutritional crops, decreasing nutritional stress (Wal- mm of rain annually, and precipitation is primarily in- 32 33 lis 2000; Hahn et al. 2003). Ekanayake et al. (2006) fluenced by the north–south migration of the Intertropi- 33 34 showed higher prevalence of Cryptosporidium sp. infec- cal Convergence Zone (ITCZ), causing a bimodal rain- 34 35 tions in toque macaques (Macaca sinica), gray langurs fall pattern consisting of 2 rainy seasons (March through 35 36 (Semnopithecus priam) and purple-faced langurs (Tra- mid-May and November through early December), sep- 36 37 chypithecus vetulus) in areas used by humans than in ar- arated by 2 dry seasons (late December through Feb- 37 38 eas not used by humans. Furthermore, a greater preva- ruary and mid-May through October) (Stampone et al. 38 39 lence of Enterobius sp., Strongyloides sp., Trichuris sp., 2011). 39 40 strongyle-type eggs, Entamoeba coli and E. hystolyti- We assessed parasite infection non-invasively, by 40 41 ca/dispar were found in the macaques that ranged in ar- collecting feces from a single habituated group of ver- 41 42 eas used by humans (Ekanayake et al. 2006). Similarly, vets that has been studied since May 2011. The group 42 43 Chapman et al. (2006) found that red colobus (Procolo- contained on average 24 individuals (2 adult males, 5 43 44 bus rufomitratus) in forest fragments who were feeding adult females, 3 subadult males, 3 subadult females, and 44 45 on crops had higher levels of stress and greater parasite 11 juveniles and infants), all of which were individual- 45 46 infections than red colobus in continuous old-growth ly identifiable based on scars, markings and variation in 46 47 forest. pelage. Two of the juveniles that were sampled died be- 47 48 48 The objective of the present study was to identify the fore sex could be determined. Overall, we obtained 403 49 49 gastrointestinal parasites in a population of vervet mon- samples between May 2011–June 2014, and January– 50 50 keys (Chlorocebus aethiops) living in a highly anthro- February 2015. Fecal samples were labeled with the in- 51 51 © 2017 The Authors. Integrative Zoology published by International Society of Zoological Sciences, 513 Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd K. Valenta et al. 1 dividual, date, location and time of collection. At the DM2500 light microscope (71 Four Valley Drive, Con- 1 2 end of each day, observers weighed 1.0 g of wet fecal cord, Ontario, L4K 4V8 Canada) under 10–100× mag- 2 3 matter from each sample and stored it in 2.0 mL of 10% nification to examine thin preparations of sedimented 3 4 formalin solution for parasite identification.