Number of Grooming Partners Is Associated with Hookworm Infection in Wild Vervet Monkeys (Chlorocebus aethiops)

Abstract

There are many known benefits of social grooming among primates, including maintenance of social relationships, removal of ectoparasites, and improved physiological condition. Recently, however, researchers have noted that social grooming and social contact may also present a significant cost by facilitating transmission of some parasites and pathogens. We investigated whether the number of social grooming partners varied based on infection status for gastrointestinal parasites. We used focal animal sampling and continuous recording to collect data on the number of grooming partners for known individual vervet monkeys (Chlorocebus aethiops). We collected non-invasive faecal samples and examined them using faecal flotation, faecal sedimentation, and immunofluorescence microscopy. We detected 6 parasites: Trichuris sp. (92%), hookworm (71%), spirurids (68%), Oesophagostomum sp. (84%), Strongyloides sp. (24%), and Entamoeba coli (92%). The number of grooming partners varied significantly based on infection with hookworm and sex. No significant relationships were detected for other parasites. Associations between host behavioural variation and some parasite taxa (specifically Trichuris, Oesophagostomum, and Entamoeba spp.) were impossible to explore due to an extremely high prevalence among hosts. This is the first report that we are aware of that has detected an association between social grooming behaviours and infection with hookworm.

Exposure and susceptibility drive reinfection with gastrointestinal parasites in a social primate

“…Parasite transmission often has a social component (Balasubramaniam et al, ; Drewe, ; MacIntosh et al, ), but is not always linked to direct contact (Friant et al, ; Grear, Luong, & Hudson, ), suggesting parasite‐specific patterns, for example different transmission pathways in parasites with mobile (free‐living larvae) versus immobile (embryonated eggs) infective stages (MacIntosh et al, ). In vervet monkeys and our study, grooming many different partners increased infection risk with GI nematodes (Wren et al, ), indicating a social component of transmission. Both transmission pathways contributed to individual reinfection risk, highlighting the importance to consider both components of transmission even in predominantly environmentally transmitted pathogens and possibly explaining the dual effect of sociality as both a protective and risk factor.…”

“…Parasite transmission often has a social component (Balasubramaniam et al, 2016;Drewe, 2009;MacIntosh et al, 2012), but is not always linked to direct contact (Friant et al, 2016;Grear, Luong, & Hudson, 2013), suggesting parasite-specific patterns, for example different transmission pathways in parasites with mobile (freeliving larvae) versus immobile (embryonated eggs) infective stages (MacIntosh et al, 2012). In vervet monkeys and our study, grooming many different partners increased infection risk with GI nematodes (Wren et al, 2016), Several predictors emerged in a few selected models, indicating a link to parasite transmission. In accordance with numerous previous studies (Habig & Archie, 2015), males had a markedly higher risk of reinfection.…”

“…While for directly transmitted diseases, direct physical contact carries infection risks (Drewe, 2009;Hamede, Mccallum, & Jones, 2008), spatial association patterns predict transmission of environmentally transmitted parasites (Altizer et al, 2003;Nunn, Jordan, McCabe, Verdolin, & Fewell, 2015). In primates, for example, being socially central and directly interacting with many partners increases the risk of gastrointestinal (GI) parasite infections (MacIntosh et al, 2012;Wren, Remis, Camp, & Gillespie, 2016), suggesting a social component of transmission. While direct and indirect transmission via contact or shared space are often studied in combination (Friant, Ziegler, & Goldberg, 2016;Rimbach et al, 2015), the role of environmental contamination is more difficult to measure and consequently assessed less frequently.…”

Individual behavioral differences and health of golden‐headed lion tamarins (Leontopithecus chrysomelas)

“…We also used the sociogram software version 1.0 (Lewejohann, 2005) to obtain the network diagrams of social grooming for each group. From such network diagrams, we obtained the number of grooming partners of each individual allowing us to test the correlation of this parameter with the parasite load following Wren et al (2016).…”

“…In addition, as adult female tamarins spend more time searching for food and feeding than males, which is positively related to the birth and survival of twin offspring (Bicca‐Marques, 2003; Box, 1997), we hypothesized differences in foraging and feeding behavior between adult female and male golden‐headed lion tamarins that may result in differences between female and male tamarins in some clinical measures. Finally, if exploratory behavior and social interactions through grooming influence endoparasite transmission (Barber & Dingemanse, 2010; MacIntosh et al, 2012; Wren, Remis, Camp, & Gillespie, 2016), we hypothesized that more exploratory and more sociable individuals performing more grooming contact would show higher endoparasite loads compared with less exploratory individuals and those less involved in grooming.…”