Physiological and social consequences of gastrointestinal nematode infection in a nonhuman primate

Müller‐Klein, Nadine; Heistermann, Michael; Strübe, Christina; Morbach, Zina M; Lilie, Navina D.; Franz, Mathias; Schülke, Oliver; Ostner, Julia

doi:10.1093/beheco/ary168

Cited by 19 publications

(34 citation statements)

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“…The standard deviation (σ), percentages of variance explained (% of σ 2 ) and p-values for random effects in each model are given below (from ranova in lmerTest, Kuznetsova et al, 2016). 2010; Müller- Klein et al, 2018). Furthermore, a recent experimental study on free-ranging mangabeys found that parasite removal led to a reduction in host GC levels (Friant et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…The physiological costs associated with helminth infection may be reflected in hormones that indicate host energetic expenditure, such as glucocorticoids (GCs). Several studies, both experimental and observational in the wild, have found significant positive correlations between host GC levels and patterns of helminth infection (Friant, Ziegler, & Goldberg, 2016;Muehlenbein & Watts, 2010;Müller-Klein et al, 2018;Sures, Knopf, & Kloas, 2001).…”

Section: Introductionmentioning

confidence: 99%

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Costs and drivers of helminth parasite infection in wild female baboons

Akinyi

Jansen

Habig

et al. 2019

Journal of Animal Ecology

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Helminth parasites can have wide‐ranging, detrimental effects on host reproduction and survival. These effects are best documented in humans and domestic animals, while only a few studies in wild mammals have identified both the forces that drive helminth infection risk and their costs to individual fitness. Working in a well‐studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya, we pursued two goals, to (a) examine the costs of helminth infections in terms of female fertility and glucocorticoid hormone levels and (b) test how processes operating at multiple scales—from individual hosts to social groups and the population at large—work together to predict variation in female infection risk. To accomplish these goals, we measured helminth parasite burdens in 745 faecal samples collected over 5 years from 122 female baboons. We combine these data with detailed observations of host environments, social behaviours, hormone levels and interbirth intervals (IBIs). We found that helminths are costly to female fertility: females infected with more diverse parasite communities (i.e., higher parasite richness) exhibited longer IBIs than females infected by fewer parasite taxa. We also found that females exhibiting high Trichuris trichiura egg counts also had high glucocorticoid levels. Female infection risk was best predicted by factors at the host, social group and population level: females facing the highest risk were old, socially isolated, living in dry conditions and infected with other helminths. Our results provide an unusually holistic understanding of the factors that contribute to inter‐individual differences in parasite infection, and they contribute to just a handful of studies linking helminths to host fitness in wild mammals.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Costs and drivers of helminth parasite infection in wild female baboons

Akinyi

Jansen

Habig

et al. 2019

Journal of Animal Ecology

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“…Anthelmintic treatment was administered orally by distributing food items containing ivermectin (approximately 0.4 mg/kg body weight). All individuals of group C received treatment on 5 August 2014; 21 individuals of group H were treated on 17 August 2015, 20 individuals served as an untreated control group for other studies (Müller, Heistermann, Strube, Schülke, & Ostner, ; Müller‐Klein et al, ). Control individuals were included for construction of social variables, but excluded from reinfection analysis.…”

Section: Methodsmentioning

confidence: 99%

“…Faecal samples were collected immediately after defecation 0–4 times per individual per week for parasite analysis, with separate aliquots stored for fGCM analyses if possible as described previously (Müller et al, ; Müller‐Klein et al, ). Over the six weeks prior to anthelminthic treatment, 2.0 ± 0.8 urine samples were collected opportunistically from 40 of the subjects as described previously (Müller et al, , see Supporting Information Appendix S2).…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2019

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Increased risk of infectious disease transmission has been proposed as one major cost of group living. While factors corresponding to transmission via exposure to infectious stages and susceptibility to contracting infections upon contact are relatively well understood, both aspects are rarely investigated simultaneously. Here, we assessed the influence of exposure and susceptibility measures on strongyle nematode reinfection after experimental deworming of Barbary macaques (Macaca sylvanus) (n = 57). We investigated impacts of behaviour (social bonds, grooming and ground use) and physiology (faecal glucocorticoids, urinary C‐Peptides, urinary neopterin, gastrointestinal [GI] helminth coinfection) on the likelihood of reinfection, using patch occupancy modelling and information theoretic model selection to determine the best models predicting reinfection patterns. Coinfection was the most consistent risk factor, spending time on presumably contaminated soil, interacting with many partners and forming strong same‐sex bonds also tended to increase infection risk. In contrast, strong social bonds with opposite‐sex partners had a consistently protective effect. Our results indicate that coinfections could serve as an integrative measure of individual disease susceptibility. Furthermore, we show that social contact contributes to both exposure and susceptibility to environmentally transmitted parasites, with the outcome depending on specific interaction patterns. A plain language summary is available for this article.

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“…First, the facilitated transmission of parasites and other pathogens constitutes one of the major costs of group living (Côté and Poulin 1995;Altizer et al 2003;Kappeler et al 2015;Müller-Klein et al 2018). Several meta-analyses revealed that group size and parasite transmissions are generally positively correlated, but their relationship turns out to be rather variable and complex Rifkin et al 2012;Patterson and Ruckstuhl 2013).…”

Section: Introductionmentioning

confidence: 99%

One size fits all? Relationships among group size, health, and ecology indicate a lack of an optimal group size in a wild lemur population

Rudolph

Fichtel

Schneider

et al. 2019

Behav Ecol Sociobiol

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Group size is a key component of sociality and can affect individual health and fitness. However, proximate links explaining this relationship remain poorly understood, partly because previous studies neglected potential confounding effects of ecological factors. Here, we correlated group size with various measures of health while controlling for measures of seasonality and habitat quality, to explore trade-offs related to group living in a mainly folivorous primate-Verreaux's sifakas (Propithecus verreauxi). Over a course of 2 years, we studied 42 individuals of 7 differently sized groups (range 2-10) and combined measures of faecal glucocorticoid metabolites (n > 2300 samples), parasitism (n > 500 samples), ranging and activity patterns, together with estimates of habitat quality (measures of~7000 feeding trees). None of our measures was correlated with group size, while seasonality, but not habitat quality, impacted almost all examined variables. We conclude that group size alone might be insufficient to explain patterns in the sociality-health nexus or that the small range of group sizes in this species does not induce effects suggested for species living in larger groups. An optimal group size balancing the advantages and disadvantages of living in differently sized groups may not exist for Verreaux's sifakas. Our results do not support predictions of the ecological constraints hypothesis or the optimal group size hypothesis as they may only account for species limited in group size by ecological factors-a condition that may not apply to the majority of folivorous mammals, which seem to be limited by social factors. Communicated by M. A. van NoordwijkSignificance statement Group size is a key component of group living and can crucially impact individual health. Ecological variables may modulate this relationship, but they were often neglected in previous studies. To better understand the links between sociality and health, we, for the first time in a mammal, simultaneously examined variation in ranging patterns, daily activities, glucocorticoid concentrations, and parasitism as a function of group size and under consideration of measures of seasonality and habitat quality in wild Verreaux's sifakas (Propithecus verreauxi). Group size had no impact on individual health indicators, while seasonal variation in food availability and temperature differences, but not habitat quality, affected the majority of variables. We demonstrate strong impacts of environmental factors on socio-ecological traits and conclude that group size on its own might be insufficient to explain patterns in the sociality-health nexus.

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Physiological and social consequences of gastrointestinal nematode infection in a nonhuman primate

Cited by 19 publications

References 100 publications

Costs and drivers of helminth parasite infection in wild female baboons

Costs and drivers of helminth parasite infection in wild female baboons

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

One size fits all? Relationships among group size, health, and ecology indicate a lack of an optimal group size in a wild lemur population

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