Temporal and demographic blood parasite dynamics in two free-ranging neotropical primates

Abstract

Parasite-host relationships are influenced by several factors intrinsic to hosts, such as social standing, group membership, sex, and age. However, in wild populations, temporal variation in parasite distributions and concomitant infections can alter these patterns. We used microscropy and molecular methods to screen for naturally occurring haemoparasitic infections in two Neotropical primate host populations, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, in the lowland tropical rainforests of southeastern Peru. Repeat sampling was conducted from known individuals over a three-year period to test for parasite-host and parasite-parasite associations. Three parasites were detected in L. weddelli including Trypanosoma minasense, Mansonella mariae, and Dipetalonema spp., while S. imperator only hosted the latter two. Temporal variation in prevalence was observed in T. minasense and Dipetalonema spp., confirming the necessity of a multi-year study to evaluate parasite-host relationships in this system. Although callitrichids display a distinct reproductive dominance hierarchy, characterized by single breeding females that typically mate polyandrously and can suppress the reproduction of subdominant females, logistic models did not identify sex or breeding status as determining factors in the presence of these parasites. However, age class had a positive effect on infection with M. mariae and T. minasense, and adults demonstrated higher parasite species richness than juveniles or sub-adults across both species. Body weight had a positive effect on the presence of Dipetalonema spp. The inclusion of co-infection variables in statistical models of parasite presence/absence data improved model fit for two of three parasites. This study verifies the importance and need for broad spectrum and long-term screening of parasite assemblages of natural host populations.

A multiyear survey of helminths from wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins

“…Our hypothesis that larger groups would show higher parasite species richness was not supported. This finding is consistent with observations of blood parasites in these primates (Erkenswick, Watsa, Gozalo, et al, 2017), and may be a consequence of low group size variation (3-8 inds.). Some callitrichids can occur in larger groups, for example, Callithrix at 15 members (Pontes & da Cruz, 1995;Watsa et al, 2017), but it is also possible that group size and parasite diversity cannot be linked within the Callitrichidae.…”

“…Consistent with the pattern of prevalence of blood parasites in this population (Erkenswick, Watsa, Gozalo, et al, 2017), age class predicted the presence of two trophically transmitted parasites, though we obtained both positive and negative relationship estimates from our models. We suspect that differences in diet and foraging efficiency between younger and older individuals underlie different parasite encounter rates, but differences in immune status, and cumulative parasite exposure as animals age are also possibilities.…”

“…Since the range of factors that can explain parasite-host patterns in nature is large (Clough, Heistermann, & Kappeler, 2010;Gillespie, Barelli, & Heistermann, 2013;Gillespie et al, 2010;MacIntosh, Hernandez, & Huffman, 2010;MacIntosh et al, 2012;Monteiro, Dietz, Raboy, et al, 2007;Muehlenbein & Watts, 2010;Nunn, Brezine, Jolles, & Ezenwa, 2014;Telfer et al, 2008) and often dependent on the environment and time (Clough et al, 2010;Gillespie et al, 2010), it may be best approached through longitudinal monitoring of individuals in host communities (Clutton-Brock & Sheldon, 2010;Erkenswick, Watsa, Gozalo, Dmytryk, & Parker, 2017;Stuart et al, 1998). A primary challenge has been that research on wild primates usually requires habituation to observers, which often constrains sample sizes, making it difficult to adequately analyze many of these factors (Williamson & Feistner, 2011).…”

“…As a result of greater social burdens placed on females to compete for dominant breeding opportunities, we predicted that an age-sex interaction would influence prevalence and parasite species richness. We also analyzed infection data for nonrandom associations between all pairwise parasite combinations, on the basis that blood parasite associations were detected previously in the same populations (Erkenswick, Watsa, Gozalo, et al, 2017). Lastly, prior studies have detected a potential pattern between primate group size and parasite species richness (Cote & Poulin, 1995;Nunn, Altizer, Jones, & Sechrest, 2003;Rifkin, Nunn, & Garamszegi, 2012;Vitone, Altizer, & Nunn, 2004), but this association has not been considered within the Callitrichidae, at small taxonomic scales.…”

A multi-year survey of helminths from the gastrointestinal tract of wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins

“…Host behavior in combination with parasite mode of dispersal can also structure parasite populations (MacIntosh et al, 2010;Nunn & Heymann, 2005). Influences of concomitant parasite infections are not routinely analyzed, but when they are, their impacts may be comparable to those exerted by host or environmental factors (Erkenswick, Watsa, Gozalo, Dmytryk, & Parker, 2017a;Monteiro, Dietz, Raboy, et al, 2007b;Nunn, Brezine, Jolles, & Ezenwa, 2014;Telfer et al, 2008). Also, meta-analyses find general support for increasing parasite species richness as social group size increases (Cote & Poulin, 1995;Nunn, Altizer, Jones, & Sechrest, 2003;Rifkin, Nunn, & Garamszegi, 2012;Vitone, Altizer, & Nunn, 2004), but the spatial and taxonomic scales at which this pattern will hold true (e.g.…”