The impact of food provisioning on parasite infection in wild black capuchin monkeys: a network approach
- 239 Downloads
Nonhuman primates host a variety of gastrointestinal parasites that infect individuals through different transmission routes. Social contact among group members (e.g., body contact, grooming) brings the risk of parasite infection, especially when the pathogen infection is directly transmitted. Along with this, accidental provisioning (i.e., food provisioning occurring during close tourist–wildlife interactions) is also considered to increase the risk of infection, as aggregation during feeding can cause higher exposure to parasite infective stages. However, while some attention has been paid to the relationship between social behavior and parasites, the link between accidental food provisioning and characteristics of parasite infection in primates has thus far received less attention. This study examines the potential effect of accidental provisioning on patterns of inter-individual spatial association, and in turn on parasite infection risk in a wild group of black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. To do so, we simulated events of accidental provisioning via researcher-managed provisioning experiments and tested whether experimental provisioning affects the inter-individual spatial distribution within groups. In addition, we determined whether patterns of parasite infection were better predicted by naturally occurring spatial networks (i.e., spatial association during natural observations) or by provisioning spatial networks (i.e., spatial interactions during experimental provisioning). We found a significant increase in network centrality that was potentially associated with an overall increase in individual connections with other group members during experimental trials. However, when assessing the effects of natural and provisioning network metrics on parasite characteristics, we did not observe a significant effect of centrality measures (i.e., closeness and betweenness) on parasite richness and single infection by Filariopsis sp. Taken together, our findings suggest that alterations of within-group spatial networks due to accidental provisioning may have a limited influence in determining the characteristics of parasite infections in black capuchin monkeys.
KeywordsSociospatial networks Co-feeding networks Gastrointestinal parasite richness Filariopsis sp. Sapajus nigritus
We thank Cedric Sueur, Ivan Puga, and Sebastian Sosa for their invitation to participate in this special issue. We particularly thank Ivan Puga for statistical advice. We thank the Delegación Tecnica of the Argentine Administration of National Parks, the Centro de Investigaciones Ecologicas Subtropicales for research permission and logistical support (permit numbers: NEA 158 bis Rnv 5). We thank Ezequiel Vanderhoeven and Juliana Notarnicola at the Instituto Nacional de Medicina Tropical (INMeT) for help with running parasite analyses. We thank also Charles H. Janson, who initiated the long-term project on black capuchins in Iguazú National Park. Julie Duboscq and an anonymous reviewer provided constructive comments on the manuscript. Fieldwork was carried out with the valuable assistance of many, especially Ester Bernaldo de Quiros and Martin Fahy.
Compliance with ethical standards
Conflict of interest
This study was approved by the Animal Welfare Officer at the German Primate Center (DPZ) and by the Argentine Administration of National Parks (permit number: NEA 158 bis Rnv 5), and adhered to the legal requirements of Argentina. The authors declare no conflict of interest.
- Agostini I, Vanderhoeven E, Beldomenico PM, Pfoh R, Notarnicola J (2018) First coprological survey of helminths in a wild population of black capuchin monkeys (Sapajus nigritus) in northeastern Argentina. Mastozool Neotrop. https://doi.org/10.31687/saremmn.22.214.171.124.11
- Becker DJ, Streicker DG, Altizer S (2018) Using host species traits to understand the consequences of resource provisioning for host–parasite interactions. J Anim Ecol 87:511–525Google Scholar
- Carne C, Semple S, MacLarnon A et al (2017) Implications of tourist–macaque interactions for disease transmission. EcoHealth 14:704–717Google Scholar
- Cox DD, Todd AC (1962) Survey of gastrointestinal parasitism in Wisconsin dairy cattle. J Am Vet Med Assoc 141:706–709Google Scholar
- Crespo JA (1982) Ecología de la comunidad de mamíferos del Parque Nacional Iguazú, Misiones. Rev Mus Argent Cienc Nat Ecol 3:1–172Google Scholar
- Csardi G, Nepsz T (2006) The igraph software package for complex network research. InterJournal 1695:1–9Google Scholar
- Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, CambridgeGoogle Scholar
- Gillespie TR, Nunn CL, Leendertz FH (2008) Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health. Am J Phys Anthropol 137:53–69Google Scholar
- Janson CH, Baldovino MC, Di Bitetti MS (2012) The group life cycle and demography of brown capuchin monkeys (Cebus apella nigritus) in Iguazú National Park, Argentina. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin, pp 185–212Google Scholar
- Nunn C, Altizer SM (2006) Infectious diseases in primates: behavior. Ecology and evolution. OUP, OxfordGoogle Scholar
- Parr NA, Fedigan LM, Kutz SJ (2013) Predictors of parasitism in wild white-faced capuchins (Cebus capucinus). Int J Primatol 34:1137–1152Google Scholar
- Santa Cruz A, Borda J, Gómez L, de Rott M (2000) Endoparasitosis in captive Cebus apella. Lab Primate Newslett 39:10–13Google Scholar
- Wheeler BC, Tiddi B, Heistermann M (2014) Competition-induced stress does not explain deceptive alarm calling in tufted capuchin monkeys. Anim Behav 93:49–58Google Scholar