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 , 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 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 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 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

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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. feces. Parasites were photographed and identified based 4 5 Samples were examined for helminth eggs, larvae on morphological traits, including egg size, color, shape 5 6 and large protozoan cysts using a modified ethyl acetate and contents. Measurements were made to the nearest 0.1 6 7 sedimentation method, in which 5 slides of the sediment µm ± SD using an ocular micrometer fitted to the com- 7 8 were examined for each sample (Sloss et al. 1994; Bow- pound microscope; parasites were photographed using 8 9 man 1999; Garcia 1999; Greiner & McIntosh 2009). Infinity camera software for further identification and 9 10 To identify protozoans, we used the hematocrit stain- documentation. 10 11 ing procedure to identify species (Bowman 1999) and We plotted the frequency of eggs or larvae at differ- 11 12 examined trichrome-stained slides. We used a Leica ent size classes (0.1 mm bins) to examine variation in 12 13 13 14 14 15 15 16 Table 1 Parasites identified in different wild vervet populations 16 17 This Mahale Rubondo Rural Sodore Wondo Loskop Hawassa 17 18 study Kenya 18 19 Cestodes Cestode (unidentified) X X 19 20 Anatrichosoma X 20 21 Ascaris spp. X X 21 22 Hyostrongylus spp. X 22 23 23 Mammonogamus spp. X 24 24 X 25 25 Necator (, likely this genus) X X 26 26 Oesophogostomum X X X 27 27 Spirurid X X 28 28 Streptophargus X 29 29 X X X 30 30 Strongyloides (possibly fuelleborni) X X X X X X X 31 31 Subulura X X 32 32 Toxocara X 33 33 Trichuris X X X X X X X X 34 34 35 Trematode Trematode (unidentified) X 35 36 Fasciola X 36 37 Dicrocoeliida X 37 38 mansoni X 38 39 Protist Balantidium coli X X 39 40 Blastocystis hominis X X 40 41 Coccida X 41 42 Cryptosporidium X X 42 43 Cyclospora X X 43 44 Entamoeba coli X X X X X X 44 45 Entamoeba histolytica/dispar X X X X 45 46 Giardia spp. X X 46 47 Iodomoeba spp. X X 47 48 Sample 403 72 111 123 25 16 272 140 48 49 number 49 50 Richness Excluding Protozoans 11 6 6 3 2 1 6 6 50 51 X indicates that parasites are present. 51

514 © 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 Parasite communities in vervet monkeys

1 egg size, but no evidence was found for any subdivision N 1 2 of a taxonomic group that we considered for any type 2 3 3

of parasite. Parasites were identified to the genus level 75% 4 wherever possible, but for some parasites identification 4 5 at a higher taxonomic level was necessary (Greiner & Unknown spp. 5 21% 21% 25% 20% 21% 6 McIntosh 2009; Ghai et al. 2014a,b). An individual was 6 7 7

considered infected if at least one helminth egg or 13%

8 was identified. We aggregated data to calculate parasite Trichuris 8

9 richness (the number of parasite species or types found Percent of samples with >1 parasite species present 9 10 in the population). When interpreting results based on 10

11 richness, it should be cautioned that if host communities 92% 11 12 have a high species richness index, this does not neces- Trematode 12 13 sarily imply that the animals in the community are less 13

14 12 43 21 34 55 14

healthy, as the parasite species are not all equivalent and 17%

15 different parasite infections have different effects. Toxocara 15 16 To determine whether there were age class or sex dif- 16 17 ferences in parasite occurrence, we compared the num- 17 Number of samples with >1 parasite species present 18 ber of fecal samples positive for parasites divided by the 29% 18 19 19

total number of fecal samples collected for each group Strongyloides = 24 monkeys), and excluded from the male/female analysis (

20 for all juveniles and subadults (N = 10), to all adults (N N 20 21 = 14), and all males (N = 9) to all females (N = 13) us- 21 1.26 1.29 1.34 1.26 1.29 22 ing a χ2-test (IBM SPSS Statistics, V 23). To determine 25% 22 Strongyle 23 parasite prevalence in the community, we calculated the 23

24 number of hosts infected with each parasite, then divid- Mean parasites per sample 24 25 ed this number by the total number of vervets sampled (N 25 26 26 = 24) (Margolis et al. 1982). 8% 27 = 24 monkeys 27

We compared our results with published results of N

28 68% 64% 67% 64% 65% 28 parasite richness in other vervet monkey populations 29 Oesophogostomum 29 (Table 1). These included the Mahale Mountains Na- 30 30 tional Park, Tanzania (Kooriyama et al. 2012); Rubon- Percent of positive samples

31 4% 31 do Island, Tanzania (Petrasova et al. 2010); rural Kenya Unknown 32 Protozoan 32

(Muriuki et al. 1998); Sodore, Ethiopia, a recreation- 84 33 319 125 267 403 33 al area where vervets roam on hotel premises; Wondo 34 Sample number 34 Grenet, Ethiopia, where vervets are found on the Wabe 35 35

Shebele Hotel premises (Legesse & Erko 2004); Lake 17% 36 36 Hawassa in southern Ethiopia (Amenu et al. 2015); 37 37 Metastrongylus

and the protected area of Loskop Dam Nature Reserve, 57 84 38 205 170 262 38 South Africa (Wren et al. 2015). 39 39

40 Number of positive samples 40 41 RESULTS 4% 41 42 42 In total, 65% of fecal samples were positive for at Hyostrongylus

43 9 43 least one parasite (262/403), and no differences were 10 14 13 24 44 detected between parasite infections by age or sex class- 44 38%

45 Number of individuals 45 es (Table 2); 68% of subadult and juvenile fecal sam- Fasciola 46 ples, and 64% of adult fecal samples had at least 1 46 47 47

parasite species present, and the difference was not sig- 38% 48 nificant χ( 2 = 0.38, P = 0.54). Sex also did not have an Cestode 48 49 effect on parasite presence in the vervets studied here: Fecal sample numbers, positive samples and parasites per fecal for 24 monkeys, by age sex class Percent of individual monkeys found to have parasite species or types. 49 50 50 64% of female fecal samples had at least 1 parasite spe- 33% Ascaris Age/Sex Class Subadults and juveniles Adults All males All females All individuals

51 2 Table Note: Sex is unknown for 2 juveniles. They are included in the adult versus subadult/juvenile analysis ( = 22 monkeys). 3 Table 51

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1 cies present and 65% of male fecal samples had at least of vervet parasites, 3 were conducted in holiday resorts 1 2 1 parasite species present, and the difference was not in Ethiopia, where tourists are known to interact closely 2 3 significant χ( 2 = 0.47, P = 0.50). with vervets (Sodore, Wondo Genet, and Lake Hawassa 3 4 Trematodes were the most prevalent, occurring in [Legesse & Erko 2004; Amenu et al. 2015]), and in one, 4 5 92% of individuals at least once, followed by Fascio- vervet samples were collected from village sites in Ken- 5 6 la spp. (38%), cestodes (38%), Ascaris spp. (33%) and ya, where interactions with humans are likely to have 6 7 Strongyloides spp. (29%). All other parasites were found occurred (Muriuki et al. 1998). Of the 3 studies that 7 8 in less than 25% of the individuals (Table 3). Many fe- took place in protected habitats, all 3, nonetheless, had 8 9 cal samples (21%) had only 1 parasite present (55/403), long-term researcher presence, one had long-term re- 9 10 and, overall, fecal samples had a mean of 1.29 parasite search presence and tourism (Mahale Mountains, Tanza- 10 11 species per sample. nia [McGrew et al. 1996]), and one was notable for the 11 12 12 In total, 11 identifiable parasite taxa were found in release of many captive-bred primates into the ecosys- 13 13 the Lake Nabugabo vervet population (Table 1). Of tem (Lake Hawassa, Ethiopia [Amenu et al. 2015]). The 14 14 these, 3 have not been found in other vervet populations number of individual variables contributing to anthropo- 15 15 sampled: Metastrongylus, Toxocara and Fasciola. Of genic disturbance at these sites highlights the difficulty 16 16 these 3, 1 is associated with the ingestion of intermedi- of establishing anthropogenic drivers behind differences 17 17 ate hosts (e.g. , Metastrongylus), 1 is direct- among populations in parasite infections. 18 18 ly ingested in contaminated soil or vegetation (Fasciola), While continental-wide comparisons of vervet par- 19 19 and 1 can be ingested directly or through an intermedi- asite species contribute to a broader picture of ver- 20 20 ate host (Toxocara, Cheng 1973). vet-parasite interactions, caution should be used in in- 21 21 When compared to the results of 7 other studies, terpreting comparisons between populations for at least 22 4 reasons: (i) the methods and ability to identify para- 22 23 non-protozoan vervet parasite species richness at Lake 23 Nabugabo (N = 11) was almost double that of the next sites vary among studies which produces variance for 24 which we cannot determine the magnitude; (ii) the sam- 24 25 highest studies (N = 6, Mahale, Rubondo, and Hawas- 25 sa). Some component of this difference in parasite spe- ple size is not the same at each site and species richness 26 may at least partly result from the number of samples 26 27 cies richness between studies likely results from varia- 27 tion in sampling intensity, which ranged from a low of assessed; (iii) it is difficult to control for habitat-specific 28 factors that could influence the parasites that infect host 28 29 16 fecal samples at Wondo Genet, Ethiopia, to 403 fecal 29 samples (this study). Across all studies, a mean of 4.8% populations (e.g. soil moisture, frequency of intra-group 30 interactions); and (iv) it is difficult to assess the regional 30 31 of samples were positive for non-protozoan parasites 31 (SD = 2.8%, range = 1.9–8.3%). pool of parasites in a rigorous quantitative manner. The 32 regional parasite pool will be a function of vervet mon- 32 33 key population size and composition and for parasite 33 34 DISCUSSION species that are host generalists, the community of host 34 35 35 Compared to 7 other sites where vervet monkey gas- species present in the region and their respective abun- 36 36 trointestinal parasites have been described, the ver- dance. 37 37 vets of Lake Nabugabo have the greatest parasite rich- Without genetic analysis of parasites, it is not possi- 38 38 ness. This finding is likely the result of a number of ble to ascertain if human to nonhuman primate parasite 39 39 factors. To some degree, the increased parasite richness transmission is occurring (de Gruijter et al. 2005; Ghai 40 40 observed in this study may be due to our larger sam- et al. 2014a,b). Genetic analysis of transmission is valu- 41 41 ple size. It is also possible that the higher parasite rich- able. For example, research based only on coproscopic 42 42 ness observed in the Lake Nagubabo population results analysis concluded that nodular (Oesophagosto- 43 43 from the highly anthropogenically disturbed nature of mum spp.) could be transmitted from nonhuman pri- 44 44 the study group’s habitat: vervets at Lake Nabugabo mates to people and thus primates posed a health risk to 45 45 have frequent interactions with humans, dogs and live- humans (Polderman & Blotkamp 1995). However, ad- 46 46 stock (Chapman et al. 2016). However, living in a high- ditional genetic analyses determined that the nodular 47 47 ly disturbed habitat does not alone explain the higher worms found in human and nonhuman primates were 48 48 parasite species richness observed in this study, as 4 of in fact genetically distinct (Gasser et al.2006). Similar- 49 49 the 7 other vervet populations sampled also live in high- ly, researchers identified 3 genetically distinct groups 50 50 ly disturbed habitats (Table 4). Of the 7 extant studies of whipworms that could not be distinguished by mi- 51 51

516 © 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 Parasite communities in vervet monkeys

1 Table 4 Descriptions of vervet parasite sampling locations: Habitat type, degree of disturbance and observed direct human interac- 1 2 tions 2 3 Location Habitat type Degree of anthropogenic habitat Direct human Source 3 4 disturbance interactions 4 5 observed 5 6 6 Lake Nabugabo, Anthropogenic landscape, adjacent High Yes Personal 7 Uganda to large lake. Mixed use recreational observations 7 8 areas, hotel compounds, small- 8 9 scale subsistence agricultural plots, 9 10 village, small patches of secondary 10 11 forest. 11 12 Mahale Mountains Tropical semi-evergreen forest, Low. Protected as a national No McGrew et. al. 12 13 National Park, adjacent to large lake. park. Ecotourism and permanent (1996) 13 14 Tanzania researcher presence. Nearest 14 15 village is 20 km away from 15 16 research site. 16 17 Rubondo Island Mixed evergreen forest, semi- Low. Protected as a game reserve No Petrasova et al. 17 18 National Park, deciduous forest, grassland. since 1928, and later as a national (2010) 18 19 Tanzania Protected as game reserve since park. Researcher presence, and 19 20 1928. Island within a large lake captive-bred primates released 20 (Lake Victoria). onto island. 21 21 22 Various locations Villages Presumed high No Muriuki et al. 22 23 throughout Kenya (1998) 23 24 Sodere Resort, Anthropogenic – a resort. High Yes. Frequent Legesse and Erko 24 25 Ethiopia interactions with (2004) 25 26 tourists reported. 26 27 Wondo-Genet Anthropogenic – a resort. High Yes Legesse and Erko 27 28 Resort, Ethiopia (2004) 28 29 Lake Hawassa, Anthropogenic – various resorts and High Yes. Frequent Amenu et al. 29 30 Ethiopia recreation areas, including hotels. interactions with (2015) 30 31 tourists reported. 31 32 Loskop Dam Mixed bushveld and woodland. Moderate No, though Wren et al. (2015, 32 33 Nature Reserve, Protected reserve, but with tourist sometimes 2016) and B. 33 34 South Africa resorts and facilities. followed by Wren (personal 34 35 researchers. communication) 35 36 36 37 37 38 38 39 croscopic examination of their eggs (Ghai et al. 2014b). In this study, we observed no significant differences in 39 40 One of these genetically unique groups was found in all parasite species richness between age and sex classes. 40 41 9 species of primates examined, including humans, but As well, when compared to other studies of vervet par- 41 42 the other 2 Trichuris groups were not. Some parasites asites from areas ranging from highly anthropogenical- 42 43 are transmissible between humans and nonhuman pri- ly disturbed to relatively pristine, differences in sample 43 44 mates, while others are not, which emphasizes the need size do not allow us to draw conclusions about the role 44 45 for genetic studies when examining inter-species trans- of environmental factors in the likelihood of parasite 45 46 mission. transmission. With respect to the condition of the host, 46 47 Previous studies have found that variations in par- while stress is known to be a factor influencing para- 47 48 asite infection among individuals, age/sex categories, sitic infection (Chapman et al. 2006), host condition is 48 49 and populations are linked to the environment and the difficult to quantify and compare. Our study group was 49 50 condition of the host (Holt et al. 2003; Padgett & Gla- likely chronically stressed by frequent interactions with 50 51 ser 2003; Ekanayake et al. 2006; Nunn & Altizer 2006). humans - who are known to chase and kill group mem- 51

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1 bers–and dogs, which are a known predator of vervets comparative perspective–quantifying both habitat dis- 1 2 in this population (Chapman et al. 2016). However, this turbance, and levels of human and domestic in- 2 3 stress may have been mitigated by the year-round avail- teraction by vervet monkeys. As well, consistent sam- 3 4 ability of food sources, namely crops planted by hu- pling intensity and lab methods for parasite detection 4 5 mans. Determining how physiological stress and diet in- should be employed across studies. Given the abun- 5 6 teract to influence parasite infection in this population dance of vervet monkeys in many human modified hab- 6 7 could contribute to a growing body of literature about itats, they are a useful species for such investigations. 7 8 the complex effects of environmental variation on par- Furthermore, anthropogenically-disturbed habitats are 8 9 asite infection in primates (Gulland 1992; Pride 2005; ubiquitous, thus it is vital that we understand animal be- 9 10 Snaith et al. 2008). havioral and ecological responses to these environments 10 11 Because of the lack of detailed data on environmental to better understand and predict future changes in wild- 11 12 variables, host condition, and vervet stress in multiple life populations, and for the construction of informed 12 13 sites, it is impossible at present to robustly delineate the conservation plans. Vervet monkeys are an excellent 13 14 role of these factors in parasite infection. However, our model for understanding the role of anthropogenic hab- 14 15 study did uncover 3 parasite genera previously undocu- itat change on behavioral and ecological responses, and 15 16 mented in vervets – Metastrongylus, Toxocara and Fas- on parasite transmission to wildlife. 16 17 ciola. The presence of these parasites in our study pop- 17 18 ulation may reflect the increased sampling effort in this REFERENCES 18 19 study, or their presence may reflect the proximity of the Amenu K, Tesaye D, Tilahun G, Mekibib B (2015). 19 20 vervets in this population to villages, small-scale farms Gastrointestinal parasites of vervet monkeys around 20 21 (Metastrongylus, Toxocara), and a lakeshore (Fasciola) Lake Hawassa recreational sites, southern Ethiopia. 21 22 – features not present in other studies of vervet parasites Comparative Clinical Pathology 24, 1491–6. 22 23 (Table 4). Metastrongylus spp. is a lung that fre- Appleton CC, Brain C (1995). 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What conser- 32 33 habitats, or areas with high monkey–human interactions, vationists need to know about farming. Proceedings 33 34 they tended to also be areas without small-scale farm- of the Royal Society of London B 279, 2714–24. 34 35 ing (Table 4). Similarly, while diverse in its life cycle Black PH (1994). Central nervous system-immune sys- 35 36 based on species, Toxocara spp. often develop to sec- tem interactions – Psychoneuroendocrinology of 36 37 ond-stage larvae in intermediate hosts including cock- stress and its immune consequences. Antimicrobial 37 38 roaches, chickens, mice, dogs, and cats, all of which Agents and Chemotherapy 38, 1–6. 38 39 are common in the villages occurring within the home Boulton AM, Horrocks JA, Baulu J (1996). The Bar- 39 40 range of the Lake Nabugabo vervet monkeys (Cheng bados vervet monkey (Cercopithecus aethiops sa- 40 41 1973). Fasciola spp., the liver flukes discovered for the baens): Changes in population size and crop damage, 41 42 first time in this population of vervets, may reflect their 1980–1994. International Journal of Primatology 17, 42 43 foraging along the lake shore, particularly on vegetation 831–44. 43 44 overhanging water, where vervets are safe from pred- Bowman DD (1999). Georgis’ for Veteri- 44 45 atory dogs (see also James et al. 1983). Fasciola spp. narians, 7th edn. Elsevier, St Louis. 45 reach their infective larval stage on aquatic plants, on 46 Chapman CA, Wasserman MD, Gillespie T et al. (2006). 46 which vervets in our study population frequently forage 47 Do nutrition, parasitism, and stress have synergis- 47 (Chapman, pers. obs.). In contrast, other vervet popula- 48 tic effects on red colobus populations living in forest 48 tions may not have associated as closely with water and 49 fragments? 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