The relative effects of reproductive condition, stress, and seasonality on patterns of parasitism in wild female black howler monkeys (Alouatta pigra)

Abstract

Parasitic infections in wildlife are shaped by host-related traits including individual reproductive condition. It has been argued that female primates are more susceptible to infectious diseases during pregnancy due to short-term changes in immune function that result in reduced ability to combat infections. Likewise, lactation, which is the most energetically expensive state, may affect immunity and infection risk due to tradeoffs between milk production and maintenance of immune function. Here, we examine the degree to which parasite prevalence and parasite richness are affected by female reproductive condition and stress levels in wild female black howler monkeys (Alouatta pigra). Over the course of one year, we collected fresh fecal samples from 15 adult females belonging to seven black howler groups living in Escárcega, Mexico. Fecal samples were used for parasitological analysis and for measuring fecal glucocorticoid metabolites (i.e., stress biomarker). We found that the prevalence of intestinal parasites and parasite richness did not differ among non-pregnant, pregnant, and lactating females. Fecal glucocorticoid metabolite levels increased significantly during pregnancy and during the first month of lactation, and positively predicted the probability of Controrchis biliophilus infection. Parasite prevalence and richness decreased during the months of increased rainfall. We conclude that reproductive physiology has limited consequences on intestinal parasitic infection risk in female black howler monkeys and that seasonal environmental fluctuations have greater effects.

Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum

“…A lack of association could be due to the sampling method since sex and reproductive condition of individuals were unknown [80]. However, our findings showing no association between FGC and parasite infection may still suggest that the interaction between immune- and endocrine functions of the host are activated independently as also suggested in other primate (lemurs [19]; gibbons [30]; howler monkeys [32]; colobines [78]) and non-primate species (mouse [81]; raccoons [82]; African ungulates [83]). Moreover, it is possible that the lack of association is an artefact of our sampling design, since more frequent longitudinal sampling would be required to firmly establish both parasite infection and stress levels.…”

“…Forests within the Udzungwas are currently fragmented into numerous blocks, widely different in habitat structure and exposure to anthropogenic disturbance (from national park to forest reserve or completely unprotected). Because the climate of the area shows seasonal variations and the study sites vary widely in altitude gradient (within and among study sites), natural environmental factors need to be also taken into account when predicting parasite infections [28–32]. Hence, we here explore the variation in parasite prevalence and richness in the endemic and endangered Udzungwa red colobus living in natural and modified habitats.…”

Seasonality, richness and prevalence of intestinal parasites of three neotropical primates (Alouatta seniculus, Ateles hybridus and Cebus versicolor) in a fragmented forest in Colombia

“…Likewise, deteriorated health status of animals can lead to negative impacts on their reproduction ( Panayotova-Pencheva, 2013 ) and survival. Although intestinal parasitosis is a major cause of morbidity and mortality in New World monkeys ( Guerrero et al., 2012 ), and some studies have been carried out in the last years ( Trejo-Macías et al., 2007 , Vitazkova and Wade, 2007 , Chinchilla et al., 2010 , Maldonado-López et al., 2014 , Behie et al., 2014 , Martínez-Mota et al., 2017 , Rimbach et al., 2015 , Solórzano-García and Pérez-Ponce de León, 2017 ) further research is required to better understand disease dynamics on New World primates. Currently, environmental changes and land use transformation are globally affecting the dynamics of disease transmission among wild populations of non-human primates and humans ( Goldberg et al., 2008 , Gottdenker et al., 2014 ), raising the importance and relevance of better recognizing and monitoring the current health status of wild non-human primates in their natural ecosystems.…”

“…Such studies tend to be selectively made in species with economic interest such as horses and sheep ( Arece, 2007 , Fusé et al., 2013 ), or pets like cats and dogs ( Barutzki and Schaper, 2011 ). However, some studies have also been conducted in primates ( Chapman et al., 2009 , Behie et al., 2014 , Duboscq et al., 2016 , Martínez-Mota et al., 2017 ), without finding a general pattern of parasite prevalence in correlation with seasonality. Martínez-Mota et al.…”

“…However, some studies have also been conducted in primates ( Chapman et al., 2009 , Behie et al., 2014 , Duboscq et al., 2016 , Martínez-Mota et al., 2017 ), without finding a general pattern of parasite prevalence in correlation with seasonality. Martínez-Mota et al. (2017) found lower parasite richness during rainy seasons, while Chapman et al.…”