Comparative Stress Response of Black and Gold Howler Monkey (Alouatta caraya) in Urban and Rural Environments of Northern Argentina.

The expansion of human populations associated with urbanization results in extensive modification of natural habitats. While many species cannot persist in these highly modified environments, some species adopt new strategies, which contribute to their survival. Several primate species have persisted in altered habitats, including members of the genus Alouatta. To improve our understanding of this interplay, we compared glucocorticoid (GCC) levels in male and female black and gold howler monkeys (Alouatta caraya) in urban and rural areas in northeastern Argentina. Fecal samples (n = 60) were collected from adults and hormone extracts were analyzed by enzyme immunoassays (EIA). Monkeys living in urban areas (females: 109.15 ± 18.83; males: 106.15 ± 10.48) had lower GCClevels than monkeys living in rural areas (females: 152.01 ± 19.50; males:139,82 ± 10.85). Interestingly, males living in urban areas had lower GCC levels compared to those living in rural areas, whereas no differences were observed in GCC levels between females living in urban and rural areas. While these results suggest that urban areas may provide a release from intergroup competition for male howler monkeys, future work is needed to better understand the dynamics of this association to best inform management and conservation of this vulnerable species.

Social play among black and gold howler monkey (Alouatta caraya) immatures during intergroup encounters.

We studied intergroup social play (IGSP) among immatures in wild black and gold howler monkeys (Alouatta caraya) in northeastern Argentina. IGSP events are one form of affiliative interaction that can occur during intergroup encounters. The main goal of this study was to analyze IGSP in A. caraya immatures and assess how intrinsic (e.g., age and sex) and extrinsic (e.g., seasonality) factors can influence the development of this type of social behavior. We followed 12 groups between 2008 and 2015 and recorded 182 encounters and 61 events of IGSP. Considering the composition of play partners, most IGSP events occurred among juveniles of both sexes (33%), followed by juveniles that were only-male (31%), and finally between mixed-sex juveniles and infants (20%) interactions. Additionally, most IGSP events occurred mainly in summer (56%), followed by spring (29%), with fewer events occurring in autumn (15%) and no IGSP events recorded in winter. Our results suggest that IGSP constitutes a beneficial activity in wild A. caraya that promotes behavioral flexibility, where immatures acquire social skills, such as tolerance, by interacting with unknown individuals. Moreover, the higher participation of young males in IGSP is consistent with the fact that adult black and gold howler males tend to be more actively involved in group encounters than females, supporting the hypothesis that social play provides benefits in the development of motor and social skills. Finally, seasonality in the frequencies of IGSP might be related to availability of foods with high and easily mobilized energy content in summer and spring.

Aged Black-and-Gold Howler Monkey Female (Alouatta caraya): A Sign of Reproductive Senescence?

Reproductive senescence patterns have been scarcely studied in Neotropical primates. The few studies available on the hormonal profiles of aging female monkeys indicate that the decline of ovarian function in nonhuman primates may resemble the hormonal events associated with the perimenopause in women. In this study, we explore a reproductive hormone profile of an aged black-and-gold howler monkey female (Alouatta caraya) from a wild population in northeastern Argentina and compare this profile with that of a cycling female in the same population. As part of a larger study, we recorded sociosexual behaviors in adult and subadult females belonging to two groups, and we collected urine (n = 877) to determine the sex hormone profile of each female. These samples were analyzed using enzyme immunoassays for estrone conjugates and pregnanediol-3-glucuronide (PdG). We found differences in mean values of PdG between the younger (cycling) and the older female. These hormone values were lower in the older female, and she did not show any signs of cyclicity for either reproductive hormone. Our results show that the aging female in this wild population shows signs of ovarian senescence, indicated by low, acyclic levels of progesterone metabolites.

Determinants of daily path length in black and gold howler monkeys (Alouatta caraya) in northeastern Argentina.

Models used to explain the social organization of primates suggest that variation in daily path length (DPL) is a response to variation in resource distribution and the intensity of intragroup feeding competition. However, daily path length may be affected by a number of other factors including the availability and distribution of nutritionally complementary food items, temperature which can influence activity budget, patterns of subgrouping, and the frequency and function of intergroup encounters. In this 6-month study (total 495 hr of quantitative data), we examined daily path lengths in two neighboring groups of black and gold howler monkeys (Alouatta caraya) inhabiting a semi-deciduous gallery forest in San Cayetano (27° 30'S, 58° 41'W), in the northwest province of Corrientes, Argentina. Both study groups were of similar size and composition. We identified relationships across groups between time spent feeding on fruits, leaves, and flowers, the number of trees visited, group spread, frequency of intergroup encounters, mean daily temperature, and DPL. Our results suggest that variation in food availability had a significant impact on howler ranging behavior by increasing DPL under conditions of high immature and mature fruit availability, and by decreasing DPL with increased availability and increased time invested in feeding on mature leaves. These results do not support the contention that a reduction in food availability or an increase in within-group feeding competition increased DPL in black and gold howler monkeys. DPL in black and gold howlers is influenced by several interrelated factors. In this regard we suggest that models of socio-ecology and ecological constraints need to reconsider how factors such as individual nutritional requirements, social tolerance and group cohesion, and the spatial and temporal availability of preferred and nearby food resources influence primate ranging behavior. Am. J. Primatol. 78:825-837, 2016. © 2016 Wiley Periodicals, Inc.

Black and gold howler monkeys (Alouatta caraya) as sentinels of ecosystem health: patterns of zoonotic protozoa infection relative to degree of human-primate contact.

Exponential expansion of human populations and human activities within primate habitats has resulted in high potential for pathogen exchange creating challenges for biodiversity conservation and global health. Under such conditions, resilient habitat generalists such as black and gold howler monkeys (Alouatta caraya) may act as effective sentinels to overall ecosystem health and alert us to impending epidemics in the human population. To better understand this potential, we examined noninvasively collected fecal samples from black and gold howler monkeys from remote, rural, and village populations in Northern Argentina. We examined all samples (n=90) for the zoonotic protozoa Cryptosporidium sp. and Giardia sp. via immunofluorescent antibody (IFA) detection. All samples were negative for Cryptosporidium sp. The prevalence of Giardia sp. was significantly higher at the rural site (67%) compared with the remote forest (57%) and village (40%) sites. A lack of Cryptosporidium sp. in all samples examined suggests that this pathogen is not a natural component of the howler parasite communities at these sites and that current land-use patterns and livestock contact are not exposing Argentine howler monkeys to this pathogen. High prevalence of Giardia sp. at all sites suggests that howler monkeys may serve as a viable reservoir for Giardia. Significantly higher prevalence of Giardia sp. at the rural site, where primate-livestock contact is highest, suggests the presence of multiple Giardia clades or increased exposure to Giardia through repeated zoonotic transmission among nonhuman primates, livestock, and/or people. These results highlight the need for future research into the epidemiology, cross-species transmission ecology, and clinical consequences of Giardia and other infectious agents not only in humans and livestock, but also in the wild animals that share their environments.