Abstract
Epidemiological studies have identified numerous environmental and individual characteristics underlying the heterogeneity of gastrointestinal parasitism within host populations. However, the contribution of anti-parasite behaviors remains understudied, although recent studies revealed individual variation in their expression. Here, we explored the relationship between individual tendency to exhibit fecal avoidance during feeding tests and gastrointestinal nematode infections in 17 semi-free ranging female woolly monkeys (Lagothrix lagotricha poeppigii). We also investigated how parasitism varied with individual age, social connectedness and level of terrestriality, and across seasons. We focused on Strongyloides sp. and Trichuris sp., the two main nematode taxa observed in the population. We found that individual tendency to avoid fecally contaminated food was negatively correlated with Strongyloides sp. infection only. Individual social connectedness was also related to infection status, but while Strongyloides sp. infection increased with the level of spatial proximity, Trichuris sp. infection increased with the rate of body contacts. Furthermore, Strongyloides sp. and Trichuris sp. infections both increased with individual frequency of ground use and decreased with age. Finally, Strongyloides sp. infection showed a seasonal pattern, with females being more parasitized during the dry than the humid season. Differences in parasite life cycles and transmission strategies may have generated the contrasted patterns of infection between Strongyloides sp. and Trichuris sp. We argue that considering individual tendency to avoid parasites among the potential determinants of gastrointestinal parasitism within populations could help to better understand disease dynamics and improve parasite control strategies, which has become a major concern for animal conservation.
Significance statement
Hosts have evolved behavioral strategies to avoid gastrointestinal parasites, such as fecal avoidance, and their expression varies among individuals. We studied the relationship between nematode infections and individual tendency to avoid feces in a feeding context, social connectedness, level of terrestriality, age and season in female woolly monkeys. Our results revealed that the more females avoided feces, the less they were parasitized, suggesting the efficiency of anti-parasite behavioral strategies. We further found that high social connectedness, intense ground use, young age and dry season were associated with increased parasitism. This study highlights the importance of considering host behaviors in epidemiological models and suggests that hosts can actively mitigate parasite risk by adopting specific anti-parasite behaviors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data used in analyses are available as Supplementary Information.
References
Akinyi MY, Jansen D, Habig B, Gesquiere LR, Alberts SC, Archie EA (2019) Costs and drivers of helminth parasite infection in wild female baboons. J Anim Ecol 88:1029–1043. https://doi.org/10.1111/1365-2656.12994
Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9:467–484. https://doi.org/10.1111/j.1461-0248.2005.00879.x
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. CABI Publishing, Wallingford
Anderson RM, Schad GA (1985) Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Trans R Soc Trop Med Hyg 79:812–825. https://doi.org/10.1016/0035-9203(85)90128-2
Appleton CC, Henzi SP (1993) Environmental correlates of gastrointestinal parasitism in montane and lowland baboons in Natal, South Africa. Int J Primatol 14:623–635. https://doi.org/10.1007/BF02215451
Arlet ME, Chapman CA, Isbell LA, Molleman F, Mänd R, Hõrak P, Carey JR (2015) Social and ecological correlates of parasitic infections in adult male gray-cheeked mangabeys (Lophocebus albigena). Int J Primatol 36:967–986. https://doi.org/10.1007/s10764-015-9866-9
Bakuza JS, Nkwengulila G (2009) Variation over time in parasite prevalence among free-ranging chimpanzees at Gombe National Park, Tanzania. Int J Primatol 30:43–53. https://doi.org/10.1007/s10764-008-9329-7
Behringer DC, Butler MJ, Shields JD (2006) Avoidance of disease by social lobsters. Nature 441:421. https://doi.org/10.1038/441421a
Brambilla A, von Hardenberg A, Kristo O, Bassano B, Bogliani G (2013) Don’t spit in the soup: faecal avoidance in foraging wild Alpine ibex, Capra ibex. Anim Behav 86:153–158. https://doi.org/10.1016/j.anbehav.2013.05.006
Briard L, Ezenwa VO (2021) Parasitism and host social behaviour: a meta-analysis of insights derived from social network analysis. Anim Behav 172:171–182. https://doi.org/10.1016/j.anbehav.2020.11.010
Buck JC, Weinstein SB, Young HS (2018) Ecological and evolutionary consequences of parasite avoidance. Trends Ecol Evol 33:619–632. https://doi.org/10.1016/j.tree.2018.05.001
Budischak SA, O’Neal D, Jolles AE, Ezenwa VO (2018) Differential host responses to parasitism shape divergent fitness costs of infection. Funct Ecol 32:324–333. https://doi.org/10.1111/1365-2435.12951
Callinan APL, Arundel JH (1982) Population dynamics of the parasitic stages of Ostertagia spp. in sheep. Int J Parasitol 12:531–535. https://doi.org/10.1016/0020-7519(82)90048-0
Cartagena-Matos B, Gasnier T, Cravo-Mota M, Bezerra BM (2017) Activity budget and social interactions in semi-captive gray woolly monkeys (Lagothrix lagotricha cana) living in an ex situ conservation area in Central Amazonia. Zoo Biol 36:21–29. https://doi.org/10.1002/zoo.21333
Coop RL, Holmes PH (1996) Nutrition and parasite interaction. Int J Parasitol 26:951–962. https://doi.org/10.1016/S0020-7519(96)80070-1
Coop RL, Kyriazakis I (2001) Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends Parasitol 17:325–330. https://doi.org/10.1016/s1471-4922(01)01900-6
Coulson G, Cripps JK, Garnick S, Bristow V, Beveridge I (2018) Parasite insight: assessing fitness costs, infection risks and foraging benefits relating to gastrointestinal nematodes in wild mammalian herbivores. Phil Trans R Soc B 373:20170197. https://doi.org/10.1098/rstb.2017.0197
Daly EW, Johnson PTJ (2011) Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission. Oecologia 165:1043–1050. https://doi.org/10.1007/s00442-010-1778-y
Debeffe L, Mcloughlin PD, Medill SA, Stewart K, Andres D, Shury T, Wagner B, Jenkins E, Gilleard JS, Poissant J (2016) Negative covariance between parasite load and body condition in a population of feral horses. Parasitology 143:983–997. https://doi.org/10.1017/S0031182016000408
Deere JR, Schaber KL, Foerster S et al (2021) Gregariousness is associated with parasite species richness in a community of wild chimpanzees. Behav Ecol Sociobiol 75:87. https://doi.org/10.1007/s00265-021-03030-3
di Fiore A, Fleischer RC (2005) Social behavior, reproductive strategies, and population genetic structure of Lagothrix poeppigii. Int J Primatol 26:1137–1173. https://doi.org/10.1007/s10764-005-6462-4
Dobson AP, Hudson PJ (1992) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse II. Population models. J Anim Ecol 61:487–498. https://doi.org/10.2307/5339
Ezenwa VO (2004) Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. Int J Parasitol 34:535–542. https://doi.org/10.1016/j.ijpara.2003.11.012
Forresteer JE, Scott ME (1990) Measurement of Ascaris lumbricoides infection intensity and the dynamics of expulsion following treatment with mebendazole. Parasitology 100:303–308. https://doi.org/10.1017/S003118200006131X
Freeland WJ (1980) Mangabey (Cerocebus albigena) movement patterns in relation to food availability and fecal contamination. Ecology 61:1297–1303. https://doi.org/10.2307/1939037
Friant S, Ziegler TE, Goldberg TL (2016) Primate reinfection with gastrointestinal parasites: behavioural and physiological predictors of parasite acquisition. Anim Behav 117:105–113. https://doi.org/10.1016/j.anbehav.2016.04.006
Galvani AP (2003) Immunity, antigenic heterogeneity, and aggregation of helminth parasites. J Parasitol 89:232–241. https://doi.org/10.1645/0022-3395(2003)089[0232:IAHAAO]2.0.CO;2
Garnick SW, Elgar MA, Beveridge I, Coulson G (2010) Foraging efficiency and parasite risk in eastern grey kangaroos (Macropus giganteus). Behav Ecol 21:129–137. https://doi.org/10.1093/beheco/arp162
Geissler PW, Mwaniki D, Thiong'o F, Friis H (1998) Geophagy as a risk factor for geohelminth infections: a longitudinal study of Kenyan primary schoolchildren. Trans R Soc Trop Med Hyg 92:7–11. https://doi.org/10.1016/s0035-9203(98)90934-8
Goldizen AW, Terborgh J, Cornejo F, Porras DT, Evans R (1988) Seasonal food shortage, weight loss, and the timing of births in saddle-back tamarins (Saguinus fuscicollis). J Anim Ecol 57:893–901. https://doi.org/10.2307/5099
González-Hernández M, Rangel-Negrín A, Schoof VAM, Chapman CA, Canales-Espinosa D, Dias PAD (2014) Transmission patterns of pinworms in two sympatric congeneric primate species. Int J Primatol 35:445–462. https://doi.org/10.1007/s10764-014-9751-y
Gonzalez-Moreno O, Hernandez-Aguilar RA, Piel AK, Stewart FA, Gracenea M, Moore J (2013) Prevalence and climatic associated factors of Cryptosporidium sp. infections in savanna chimpanzees from Ugalla Western Tanzania. Parasitol Res 112:393–399. https://doi.org/10.1007/s00436-012-3147-8
Grear DA, Luong LT, Hudson PJ (2013) Network transmission inference: host behavior and parasite life cycle make social networks meaningful in disease ecology. Ecol Appl 23:1906–1914. https://doi.org/10.1890/13-0907.1
Gulland FMD (1992) The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105:493–503. https://doi.org/10.1017/S0031182000074679
Habig B, Archie EA (2015) Social status, immune response and parasitism in males: a meta-analysis. Phil Trans R Soc B 370:20140109. https://doi.org/10.1098/rstb.2014.0109
Habig B, Doellman MM, Woods K, Olansen J, Archie EA (2018) Social status and parasitism in male and female vertebrates: a meta-analysis. Sci Rep 8:3629. https://doi.org/10.1038/s41598-018-21994-7
Habig B, Jansen DAWAM, Akinyi MY, Gesquiere LR, Alberts SC, Archie EA (2019) Multi-scale predictors of parasite risk in wild male savanna baboons (Papio cynocephalus). Behav Ecol Sociobiol 73:134. https://doi.org/10.1007/s00265-019-2748-y
Holmes JC (1996) Parasites as threats to biodiversity in shrinking ecosystems. Biodivers Conserv 5:975–983. https://doi.org/10.1007/BF00054415
Holmstad PR, Hudson PJ, Skorping A (2005) The influence of a parasite community on the dynamics of a host population: a longitudinal study on willow ptarmigan and their parasites. Oikos 111:377–391. https://doi.org/10.1111/j.0030-1299.2005.13640.x
Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258. https://doi.org/10.1126/science.282.5397.2256
Hutchings MR, Kyriazakis I, Anderson DH, Gordon IJ, Coop RL (1998) Behavioural strategies used by parasitized and non-parasitized sheep to avoid ingestion of gastro-intestinal nematodes associated with faeces. Anim Sci 67:97–106. https://doi.org/10.1017/S1357729800009838
Johnson PTJ, Hoverman JT (2014) Heterogeneous hosts: how variation in host size, behaviour and immunity affects parasite aggregation. J Anim Ecol 83:1103–1112. https://doi.org/10.1111/1365-2656.12215
Karvonen A, Seppälä O, Valtonen ET (2004) Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129:159–164. https://doi.org/10.1017/s0031182004005505
Kiesecker JM, Skelly DK, Beard KH, Preisser E (1999) Behavioral reduction of infection risk. P Natl Acad Sci USA 96:9165–9168. https://doi.org/10.1073/pnas.96.16.9165
Knezevich M (1998) Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta). Am J Primatol 44:71–82. https://doi.org/10.1002/(SICI)1098-2345(1998)44:1<71::AID-AJP6>3.0.CO;2-U
Koprivnikar J, Forbes MR, Baker RL (2006) On the efficacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis. Can J Zool 84:1623–1629. https://doi.org/10.1139/z06-158
Koski KG, Scott ME (2001) Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annu Rev Nutr 21:297–321. https://doi.org/10.1146/annurev.nutr.21.1.297
Lello J, Boag B, Hudson PJ (2005) The effect of single and concomitant pathogen infections on condition and fecundity of the wild rabbit (Oryctolagus cuniculus). Int J Parasitol 35:1509–1515. https://doi.org/10.1016/j.ijpara.2005.06.002
Lilly AA, Mehlman PT, Doran D (2002) Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. Int J Primatol 23:555–573. https://doi.org/10.1023/A:1014969617036
Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359. https://doi.org/10.1038/nature04153
MacIntosh AJJ, Hernandez AD, Huffman MA (2010) Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51:353–364. https://doi.org/10.1007/s10329-010-0211-9
MacIntosh AJJ, Jacobs A, Garcia C, Shimizu K, Mouri K, Huffman MA, Hernandez AD (2012) Monkeys in the middle: parasite transmission through the social network of a wild primate. PLoS One 7:e51144. https://doi.org/10.1371/journal.pone.0051144
Masi S, Chauffour S, Bain O, Todd A, Guillot J, Krief S (2012) Seasonal effects on great ape health: a case study of wild chimpanzees and western gorillas. PLoS One 7:e49805. https://doi.org/10.1371/journal.pone.0049805
McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10:190–194. https://doi.org/10.1016/S0169-5347(00)89050-3
Miterpáková M, Dubinský P, Reiterová K, Stanko M (2006) Climate and environmental factors influencing Echinococcus multilocularis occurrence in the Slovak Republic. Ann Agric Environ Med 13:235–242
Morand S, Harvey PH (2000) Mammalian metabolism, longevity and parasite species richness. Proc R Soc Lond B 267:1999–2003. https://doi.org/10.1098/rspb.2000.1241
Muehlenbein MP, Watts DP (2010) The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc Med 4:21. https://doi.org/10.1186/1751-0759-4-21
Müller-Graf CDM, Collins DA, Woolhouse MEJ (1996) Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112:489–497. https://doi.org/10.1017/s0031182000076952
Nishimura A (1994) Social interaction patterns of woolly monkeys (Lagothrix lagotricha): a comparison among the Atelines. Sci Eng Rev Doshisha Univ 35:235–254
Nunn C, Altizer S (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, Oxford
Nunn CL, Craft ME, Gillespie TR, Schaller M, Kappeler PM (2015) The sociality–health–fitness nexus: synthesis, conclusions and future directions. Phil Trans R Soc B 370:20140115. https://doi.org/10.1098/rstb.2014.0115
Nwosu CO, Ogunrinade AF, Fagbemi BO (1996) Prevalence and seasonal changes in the gastro-intestinal helminths of Nigerian goats. J Helminthol 70:329–333. https://doi.org/10.1017/s0022149x00015625
Oppliger A, Richner H, Christe P (1994) Effect of an ectoparasite on lay date, nest-site choice, desertion, and hatching success in the great tit (Parus major). Behav Ecol 5:130–134. https://doi.org/10.1093/beheco/5.2.130
Parr NA, Fedigan LM, Kutz SJ (2013) Predictors of parasitism in wild white-faced capuchins (Cebus capucinus). Int J Primatol 34:1137–1152. https://doi.org/10.1007/s10764-013-9728-2
Pearson RD (2002) An update on the geohelminths: Ascaris lumbricoides, hookworms, Trichuris trichiura, and Strongyloides stercoralis. Curr Infect Dis Rep 4:59–64. https://doi.org/10.1007/s11908-002-0068-1
Pedersen AB, Greives TJ (2008) The interaction of parasites and resources cause crashes in a wild mouse population. J Anim Ecol 77:370–377. https://doi.org/10.1111/j.1365-2656.2007.01321.x
Petrželková KJ, Uwamahoro C, Pafčo B et al (2021) Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei). Sci Rep 11:10869. https://doi.org/10.1038/s41598-021-89283-4
Philippon J, Serrano-Martínez E, Poirotte C (2021) Environmental and individual determinants of fecal avoidance in semi-free ranging woolly monkeys (Lagothrix lagotricha poeppigii). Am J Phys Anthropol 176:614–624. https://doi.org/10.1002/ajpa.24352
Phillips SR, Goldberg TL, Muller MN et al (2020) Faecal parasites increase with age but not reproductive effort in wild female chimpanzees. Phil Trans R Soc B 375:20190614. https://doi.org/10.1098/rstb.2019.0614
Poirotte C, Basset D, Willaume E, Makaba F, Kappeler PM, Charpentier MJE (2016) Environmental and individual determinants of parasite richness across seasons in a free-ranging population of Mandrills (Mandrillus sphinx). Am J Phys Anthropol 159:442–456. https://doi.org/10.1002/ajpa.22888
Poirotte C, Benhamou S, Mandjembe A, Willaume E, Kappeler PM, Charpentier MJE (2017a) Gastrointestinal parasitism and recursive movements in free-ranging mandrills. Anim Behav 134:87–98. https://doi.org/10.1016/j.anbehav.2017.10.013
Poirotte C, Kappeler PM (2019) Hygienic personalities in wild grey mouse lemurs vary adaptively with sex. Proc R Soc B 286:20190863. https://doi.org/10.1098/rspb.2019.0863
Poirotte C, Massol F, Herbert A, Willaume E, Bomo PM, Kappeler PM, Charpentier MJE (2017b) Mandrills use olfaction to socially avoid parasitized conspecifics. Sci Adv 3:e1601721. https://doi.org/10.1126/sciadv.1601721
Poirotte C, Sarabian C, Ngoubangoye B, MacIntosh AJJ, Charpentier MJE (2019) Faecal avoidance differs between the sexes but not with nematode infection risk in mandrills. Anim Behav 149:97–106. https://doi.org/10.1016/j.anbehav.2019.01.013
Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134:763–776. https://doi.org/10.1017/S0031182006002150
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org. Accessed 13 Sept 2022
Ramirez M (1988) The woolly monkeys, genus Lagothrix. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, da Fonseca GAB (eds) Ecology and behavior of neotropical primates. World Wildlife Fund, Washington, DC, pp 539–575
Reckardt K, Kerth G (2007) Roost selection and roost switching of female Bechstein’s bats (Myotis bechsteinii) as a strategy of parasite avoidance. Oecologia 154:581–588. https://doi.org/10.1007/s00442-007-0843-7
Rimbach R, Bisanzio D, Galvis N, Link A, di Fiore A, Gillespie TR (2015) Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Phil Trans R Soc B 370:20140110. https://doi.org/10.1098/rstb.2014.0110
Rinaldi L, Veneziano V, Morgoglione ME, Pennacchio S, Santaniello M, Schioppi M, Musella V, Fedele V, Cringoli G (2009) Is gastrointestinal strongyle faecal egg count influenced by hour of sample collection and worm burden in goats? Vet Parasitol 163:81–86. https://doi.org/10.1016/j.vetpar.2009.03.043
Roldán WH, Cavero YA, Espinoza YA, Jiménez S, Gutiérrez CA (2010) Human toxocariasis: a seroepidemiological survey in the Amazonian city of Yurimaguas, Peru. Rev Inst Med Trop Sao Paulo 52:37–42. https://doi.org/10.1590/s0036-46652010000100006
Rowe N (1996) The pictorial guide to the living primates. Pogonias Press, Charlestown, RI
Sapolsky RM (2004) Social status and health in humans and other animals. Annu Rev Anthropol 33:393–418. https://doi.org/10.1146/annurev.anthro.33.070203.144000
Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652. https://doi.org/10.1126/science.1106477
Sarabian C, Belais R, MacIntosh AJJ (2021) Avoidance of contaminated food correlates with low protozoan infection in bonobos. Front Ecol Evol 9:651159. https://doi.org/10.3389/fevo.2021.651159
Sarabian C, MacIntosh AJJ (2015) Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biol Lett 11:20150757. https://doi.org/10.1098/rsbl.2015.0757
Sato M, Sanguankiat S, Pubampen S, Kusolsuk T, Maipanich W, Waikagul J (2009) Egg laying capacity of Haplorchis taichui (Digenea: Heterophyidae) in humans. Korean J Parasitol 47:315–318. https://doi.org/10.3347/kjp.2009.47.3.315
Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113. https://doi.org/10.1111/j.2041-210X.2010.00012.x
Schmitt CA, di Fiore A (2014) Life history, behavior, and development of wild immature lowland woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. In: Defler TR, Stevenson PR (eds) The woolly monkey: behavior, ecology, systematics, and captive research. Springer, New York, pp 113–146. https://doi.org/10.1007/978-1-4939-0697-0_8
Schwenke RA, Lazzaro BP, Wolfner MF (2016) Reproduction–immunity trade-offs in insects. Annu Rev Entomol 61:239–256. https://doi.org/10.1146/annurev-ento-010715-023924
Seivwright LJ, Redpath SM, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78:69–76. https://doi.org/10.1079/JOH2003220
Shanee S, Stevenson PR, de la Torre S, Moscoso P, Ravetta AL, Muniz CC (2021) Lagothrix lagothricha ssp. poeppigii. The IUCN Red List Threat Species 2021:e.T39927A192308336. https://www.iucnredlist.org/species/39927/192308336. Accessed 22 Mar 2023
Shaw AK, Sherman J, Barker FK, Zuk M (2018) Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration. Proc R Soc B 285:20182147. https://doi.org/10.1098/rspb.2018.2147
Shaw DJ, Dobson AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111:S111–S133. https://doi.org/10.1017/S0031182000075855
Shaw DJ, Grenfell BT, Dobson AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117:597–610. https://doi.org/10.1017/S0031182098003448
Shearer CL, Ezenwa VO (2020) Rainfall as a driver of seasonality in parasitism. Int J Parasitol Parasites Wildl 12:8–12. https://doi.org/10.1016/j.ijppaw.2020.04.004
Stear MJ, Bishop SC, Duncan JL, McKellar QA, Murray M (1995) The repeatability of faecal egg counts, peripheral eosinophil counts, and plasma pepsinogen concentrations during deliberate infections with Ostertagia circumcincta. Int J Parasitol 25:375–380. https://doi.org/10.1016/0020-7519(94)00136-C
Stevenson PR, Quiñones MJ (1993) Vertical stratification of four New World primates, at Tinigua National Park, Colombia. Field Stud New World Monkeys, La Macarena, Colombia 8:11–18
Stoner KE, González di Pierro AM (2006) Intestinal parasitic infections in Alouatta pigra in tropical rainforest in Lacandona, Chiapas, Mexico: implications for behavioral ecology and conservation. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of mesoamerican primates: distribution, ecology, behavior, and conservation. Springer US, Boston, MA, pp 215–240. https://doi.org/10.1007/0-387-25872-8_10
Teichroeb JA, Kutz SJ, Parkar U, Thompson RCA, Sicotte P (2009) Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng-Fiema, Ghana: possible anthropozoonotic transmission. Am J Phys Anthropol 140:498–507. https://doi.org/10.1002/ajpa.21098
Thompson RCA, Lymbery AJ, Smith A (2010) Parasites, emerging disease and wildlife conservation. Int J Parasitol 40:1163–1170. https://doi.org/10.1016/j.ijpara.2010.04.009
Thurber MI, O’Connell-Rodwell CE, Turner WC, Nambandi K, Kinzley C, Rodwell TC, Faulkner CT, Felt SA, Bouley DM (2011) Effects of rainfall, host demography, and musth on strongyle fecal egg counts in African elephants (Loxodonta africana) in Namibia. J Wildlife Dis 47:172–181. https://doi.org/10.7589/0090-3558-47.1.172
Turner WC, Getz WM (2010) Seasonal and demographic factors influencing gastrointestinal parasitism in ungulates of Etosha National Park. J Wildlife Dis 46:1108–1119. https://doi.org/10.7589/0090-3558-46.4.1108
van Schaik CP, Terborgh JW, Wright SJ (2003) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377. https://doi.org/10.1146/annurev.es.24.110193.002033
VanderWaal KL, Obanda V, Omondi GP, McCowan B, Wang H, Fushing H, Isbell LA (2016) The “strength of weak ties” and helminth parasitism in giraffe social networks. Behav Ecol 27:1190–1197. https://doi.org/10.1093/beheco/arw035
Warburton EM, Vonhof MJ (2018) From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions. Int J Parasitol 48:309–318. https://doi.org/10.1016/j.ijpara.2017.10.005
White LA, Forester JD, Craft ME (2017) Using contact networks to explore mechanisms of parasite transmission in wildlife. Biol Rev 92:389–409. https://doi.org/10.1111/brv.12236
Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife disease. Oxford University Press, Oxford, pp 6–44
Wren BT, Remis MJ, Camp JW, Gillespie TR (2016) Number of grooming partners is associated with hookworm infection in wild vervet monkeys (Chlorocebus aethiops). Folia Primatol 87:168–179. https://doi.org/10.1159/000448709
Zajac AM, Conboy GA (2012) Veterinary clinical parasitology. John Wiley & Sons, Ames, IA
Acknowledgments
We thank the directors of the NGO Ikamaperu for allowing this study to be carried out in their primate rehabilitation center, the caretakers and volunteers of the NGO Ikamaperu for their help in performing feeding tests, behavioral observations, fecal sample collection and coproscopic analyses and the reviewers for their comments and suggestions.
Funding
This study was supported by a Ph.D. grant from the Franco-Peruvian Doctoral School in Life Sciences of the Cayetano Heredia Peruvian University (UPCH) of Lima, the National Council of Science, Technology and Innovation (CONCYTEC) of Peru, the Ministry of Higher Education and Research (MESR) of France, the Ministry of Foreign Affairs (MAE) of France and the Institute for Research for Development (IRD) of France.
Author information
Authors and Affiliations
Contributions
Conceptualization: JP, CP; Methodology: JP, ES-M, CP; Formal analysis and investigation: JP; Resources: JP, ES-M; Data curation: JP; Supervision: ES-M, CP; Validation: JP; Visualization: JP; Writing - original draft preparation: JP; Writing - review and editing: JP, ES-M, CP; Project administration: ES-M; Funding acquisition: JP.
Corresponding author
Ethics declarations
Ethics approval
Experimental procedures were conducted in compliance with both the American Society of Primatologists Principles for the Ethical Treatment of Non-Human Primates and the rehabilitation and veterinary protocols of the NGO Ikamaperu and approved by both the Institutional Ethics Committee for the use of Animals (CIEA) of the Cayetano Heredia Peruvian University of Lima and the Regional Management of Forestry and Wildlife Development of Loreto, Peru (permit number: N°139-2019-GRL-GGR-GRDFFS-ODPAA-Yurimaguas). Research permissions were granted by the NGO Ikamaperu.
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by K. Langergraber
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(XLSX 36 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Philippon, J., Serrano-Martínez, E. & Poirotte, C. Fecal avoidance and gastrointestinal parasitism in semi-free ranging woolly monkeys (Lagothrix lagotricha poeppigii). Behav Ecol Sociobiol 77, 41 (2023). https://doi.org/10.1007/s00265-023-03317-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-023-03317-7