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.

Keywords: Blood parasites; Callitrichidae; Co-infection; Cooperative breeding; Longitudinal sampling.

Graphical abstract

Supplementary Fig. S4

Agarose gel image and chromatogram of COI gene. (a) Gel bands of individuals with infection with either Dipetalonema spp. (not indicated), M. mariae (indicated), or both (indicated). (b) Co-infection is confirmed on a chromatogram by the presence of double-peaks.

Fig. 1

Annual prevalence of single- and co-infections by species. Prevalence indicated for each parasite (dark gray), and each pairwise combination of parasites (light gray). Numbers near the top of each bar show the exact prevalence; black lines indicate 95% confidence intervals; dots indicate expected levels of co-infection (refer to Section 3.2). M-D is co-occurrence of M. mariae and Dipetalonema spp., D-T is Dipetalonema spp. and T. minasense, and M-T is M. mariae and T. minasense.

Fig. 2

Individual infection status by parasite by year. Strength and thickness of lines are scaled to the number of individuals that took a given infection trajectory from one year to the next. Two diagonal lines span 2012–2014 because those individuals were not sampled in 2013. The + symbols represent every infection or non-infection found across all individuals in the study.

Fig. 3

Parasite species richness by species, age class and sex. Colors represent females (black) and males (gray).