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

Studies on parasites infecting non-human primates are essential to better understand the potential threat to humans of zoonoses transmission, particularly under the current processes of pervasive land use change and biodiversity loss. The natural ecosystems in the Middle Magdalena river basin in Colombia have suffered a dramatic reduction and transformation into pastures and agroindustrial monocultures, threatening their biodiversity, and probably affecting the dynamics between parasites and their hosts, as well as altering the disease transmission cycles between wild populations and humans. This study evaluated seasonality, prevalence and richness of intestinal parasites in three species of neotropical primates: Cebus versicolor, Ateles hybridus and Alouatta seniculus, in a fragmented forest in the Middle Magdalena river valley, Colombia. One hundred and eighty five faecal samples were collected between 2010 and 2015. Direct faecal smears were performed with saline solution (0.85%) and iodine solution (1%), in order to identify larvae and eggs based on their morphology. A large proportion of the samples examined (72.9%) was positive for intestinal parasites; seven families of nematodes were identified: Trichuridae, Trichostrongylidae, Oxyuridae, Strongyloididae, Ancylostomatidae, Ascarididae and Gnathostomatidae, two of protozoans: Entamoebidae and Balantiididae, as well as some eggs of trematodes, cestodes and acanthocephalans. Additionally, DNA extraction and sequencing were conducted on 30 faecal samples in order to identify Giardia sp. and Blastocystis hominis, two parasite species also present in humans. Molecular testing for Giardia sp. was negative and Blastocystis hominis was identified in a single sample of Alouatta seniculus. No clear patterns were observed for prevalence of intestinal parasites according to the season; nonetheless, parasite species richness was higher during the dry season. This study builds on our current understanding of intestinal parasites infecting wild neotropical primates and provides novel information on the patterns of intestinal parasites in primate communities exposed to anthropogenic disturbance.

Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics.

Elevated risk of disease transmission is considered a major cost of sociality, although empirical evidence supporting this idea remains scant. Variation in spatial cohesion and the occurrence of social interactions may have profound implications for patterns of interindividual parasite transmission. We used a social network approach to shed light on the importance of different aspects of group-living (i.e. within-group associations versus physical contact) on patterns of parasitism in a neotropical primate, the brown spider monkey (Ateles hybridus), which exhibits a high degree of fission-fusion subgrouping. We used daily subgroup composition records to create a 'proximity' network, and built a separate 'contact' network using social interactions involving physical contact. In the proximity network, connectivity between individuals was homogeneous, whereas the contact network highlighted high between-individual variation in the extent to which animals had physical contact with others, which correlated with an individual's age and sex. The gastrointestinal parasite species richness of highly connected individuals was greater than that of less connected individuals in the contact network, but not in the proximity network. Our findings suggest that among brown spider monkeys, physical contact impacts the spread of several common parasites and supports the idea that pathogen transmission is one cost associated with social contact.

Effects of logging, hunting, and forest fragment size on physiological stress levels of two sympatric ateline primates in Colombia.

Habitat fragmentation and anthropogenic disturbances are of major concern to the conservation of endangered species because of their potentially negative impact on animal populations. Both processes can impose physiological stress (i.e. increased glucocorticoid output) on animals, and chronically elevated stress levels can have detrimental effects on the long-term viability of animal populations. Here, we investigated the effect of fragment size and human impact (logging and hunting pressure) on glucocorticoid levels of two sympatric Neotropical primates, the red howler monkey (Alouatta seniculus) and the critically endangered brown spider monkey (Ateles hybridus). These two species have been reported to contrast strongly in their ability to cope with anthropogenic disturbances. We collected faecal samples from eight spider monkey groups and 31 howler monkey groups, living in seven and 10 different forest fragments in Colombia, respectively. We measured faecal glucocorticoid metabolite (FGCM) levels in both species using previously validated methods. Surprisingly, fragment size did not influence FGCM levels in either species. Spider monkeys showed elevated FGCMs in fragments with the highest level of human impact, whereas we did not find this effect in howler monkeys. This suggests that the two species differ in their physiological responsiveness to anthropogenic changes, further emphasizing why brown spider monkeys are at higher extinction risk than red howler monkeys. If these anthropogenic disturbances persist in the long term, elevated FGCM levels can potentially lead to a state of chronic stress, which might limit the future viability of populations. We propose that FGCM measurements should be used as a tool to monitor populations living in disturbed areas and to assess the success of conservation strategies, such as corridors connecting forest fragments.

Diet of the critically endangered brown spider monkey (Ateles hybridus) in an inter-Andean lowland rainforest in Colombia.

Brown spider monkeys (Ateles hybridus) are one of the least known and more threatened primates in the Neotropics. Recognized as a species about a decade ago, field studies on these endangered primates have mainly focused on estimating local population densities. Since 2006, we habituated a group of wild brown spider monkeys at Serranía de Las Quinchas, Colombia, and studied their feeding ecology during 2.5 years using focal "subgroup" sampling, and conducted phenological surveys in order to estimate habitat-wide fruit availability. Based on 847 hr of behavioral follows, brown spider monkeys spent approximately 25% of their time in feeding activities, and fed from fruits and leaves on at least 123 plant species. Ripe fruits were the most important item in the diet of A. hybridus at Las Quinchas comprising 92% of their feeding time. Probably due to the minor variation in the monthly proportion of fruits in brown spider monkey's diet throughout this study, there was no relation between habitat-wide fruit availability and the proportion of fruit included in their monthly diet. The diet of brown spider monkeys at Las Quinchas is toward the high end of fruit intake, even within other wild spider monkeys' populations, suggesting that these endangered primates might also be facing the challenges of being a large bodied fruit specialist under a regional scenario of habitat loss and fragmentation.

Patterns of mineral lick visitation by spider monkeys and howler monkeys in Amazonia: are licks perceived as risky areas?

Mineral licks--also known as "salados," "saladeros," or "collpas"--are specific sites in tropical and temperate ecosystems where a large diversity of mammals and birds come regularly to feed on soil. Although the reasons for vertebrate geophagy are not completely understood, animals are argued to obtain a variety of nutritional and health benefits from the ingestion of soil at mineral licks. We studied the temporal patterns of mineral lick use by white-bellied spider monkey (Ateles belzebuth) and red howler monkey (Alouatta seniculus) in a lowland rain forest in Amazonian Ecuador. Using camera and video traps at four different mineral licks, combined with behavioral follows of one group of spider monkeys, we documented rates of mineral lick visitation by both primate species and the relative frequency and intensity of mineral lick use by spider monkeys. On the basis of 1,612 days and 888 nights of mineral lick monitoring, we found that A. belzebuth and A. seniculus both visit mineral licks frequently throughout the year (on average ∼14% of days for both species), and mineral lick visitation was influenced by short-term environmental conditions (e.g. sunny and dry weather). For spider monkeys, the area surrounding the lick was also the most frequently and most intensively used region within the group's home range. The fact that spider monkeys spent long periods at the lick area before coming to the ground to obtain soil, and the fact that both species visited the lick preferentially during dry sunny conditions (when predator detectability is presumed to be relatively high) and visited simultaneously more often than expected by chance, together suggest that licks are indeed perceived as risky areas by these primates. We suggest that howler and spider monkeys employ behavioral strategies aimed at minimizing the probability of predation while visiting the forest floor at risky mineral lick sites.