Ilaria Agostini

Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya.

According to the principle of competitive exclusion, niche differentiation allows the stable coexistence of closely related species. We analyzed dietary profile and diversity, and dietary overlap between syntopic brown howlers (BR; Alouatta guariba clamitans) and black and gold howlers (BLG; A. caraya) in the Atlantic Forest of NE Argentina, with the objective of evaluating the degree of trophic niche overlap and potential interspecific competition for food. During 12 months, we collected data on feeding behavior of two groups of each howler species using the scan sampling method, together with data on food availability. Both at the group‐ and species‐level, we analyzed feeding behavior in terms of monthly percentages of time spent feeding on each food type and specific food item, dietary diversity (Shannon index H′), and we estimated dietary overlap using the percentage index and the Morisita–Horn index (CH). Across months, both howlers showed species‐specific preferences for certain food items, and BLG had a more diverse diet (mean±SE, H′=2.77±0.08) than BR (H′=2.39±0.09). However, diets of both species overlapped extensively (percentage index=45.64±2.97%; CH=0.6±0.05) and diets of conspecific groups did not overlap more than diets of groups of different species. Given their high degree of trophic overlap, syntopic BR and BLG meet one of the conditions necessary for interspecific food competition to occur. Although at present we lack direct evidence for interspecific competition in these howler species, we conclude that high levels of niche overlap may have an important role in maintaining the essentially parapatric distribution of howler species throughout the Neotropics. Am. J. Primatol. 72:173–186, 2010.

Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitans and A. caraya) in Misiones, Argentina

Two yellow fever outbreaks (YFOs) ocurred in northeastern Argentina between November 2007 and October 2008, seriously affecting populations of two howler monkey species: the brown howler Alouatta guariba clamitans and the black howler Alouatta caraya. Both howlers live syntopically in El Piñalito Provincial Park, Misiones, where four groups (36 individuals) were studied since January 2005. The first dead howlers were found on January 20, 2008, in El Piñalito. Systematic searches found 14 dead howlers within the area (12 from the study groups and two from neighboring groups), with only two young seen on January 25, 2008, and none found since up to December 2008. In October 2008, another YFO hit howler monkey populations from El Soberbio, Misiones. Overall, 59 howlers were found dead in Misiones from November 2007 to December 2008. Thanks to the alert of the howlers death in El Piñalito, a prompt human vaccination campaign started in the area. Wild howler monkey populations from both species are in a delicate situation in Misiones, especially the brown howler, an already endangered species in Argentina and endemic to the Atlantic Forest. If we add the recurrence of YFOs to the reduction of suitable habitat to small fragments, it could be only a matter of time until howler populations disappear from the Upper Paraná Atlantic Forest in Misiones. Am. J. Primatol. 72:475–480, 2010.

Hybridization in Howler Monkeys: Current Understanding and Future Directions

Hybridization, or the process by which individuals from genetically distinct populations (e.g., species, subspecies) mate and produce at least some offspring, is of great relevance to understanding the basis of reproductive isolation and, in some cases, the origins of biodiversity. Natural hybridization among primates has been well documented for a few taxa, but just recently the genetic confirmation of hybridization for a number of taxa has produced new awareness of the prevalence of this phenomenon within the order and its importance in primate evolution. The study of hybridization of Alouatta pigra and A. palliata in Mexico was among the first to genetically confirm the current occurrence of hybridization in primates. Following this study, other reports of hybridization have shown that this phenomenon is more widespread among primates than previously anticipated. Within the genus Alouatta, there have been reports on the presence of hybridization between A. caraya and A. guariba in a number of contact zones in Brazil and Argentina, and various studies are currently ongoing in some of these sites to understand the extent and patterns of hybridization between these species. In this chapter, we evaluate the extent of hybridization in the genus Alouatta, revise the current knowledge of the genetic and morphological aspects of these hybrid systems, and identify future directions in the study of hybridization within this genus, to understand the possible implications of the hybridization process in the evolutionary history of howler monkeys.

Using Species Distribution Modeling to Assess Factors that Determine the Distribution of Two Parapatric Howlers (Alouatta spp.) in South America

Through presence-only data, ecological niche modeling can use environmental variables to generate maps of areas that are potentially suitable for the presence of a species, improving our knowledge of its niche requirements and extending our understanding of its geographic distribution. We used the ecological niche model MaxEnt to predict the potential distribution of black-and-gold howlers (Alouatta caraya) and brown howlers (Alouatta guariba clamitans) in South America, as well as the potential sympatry area between both species. We modeled distributions of Alouatta caraya (196 presence localities, 8 bioclimatic variables) and A. guariba clamitans (74 presence localities, 13 bioclimatic variables) using bioclimatic variables from WorldClim with habitat suitability categorized as low, moderate, or high. Alouatta caraya showed a broader potential distribution, occupying a wide variety of habitats in a broad range of temperatures. Temperature annual range (Bio 7) was the bioclimatic variable with most influence in modeling the potential distribution of this species. Alouatta guariba clamitans was more restricted to rainy areas of mature forests at higher altitudes with low minimum temperatures. Mean temperature of coldest quarter (Bio 11) was the bioclimatic variable with the highest influence in this model. The predicted area of potential sympatry of both species was a relatively small area in the interior Atlantic Forest ecoregion, and a new syntopy locality occurred within the predicted area of sympatry. This narrow zone of overlap could be maintained, among other causes, by the role of the Paraná River as a natural barrier for dispersion, differences in niche requirements, potential interspecific competition, and hybridization.

Influence of seasonality, group size, and presence of a congener on activity patterns of howler monkeys

Abstract Ecologically similar and closely related species in sympatry may differ in their activity patterns to avoid interspecific contest competition. We here present the 1st study aimed at evaluating the effects of seasonality, group size, and presence of a congener on the activity patterns of 2 syntopic species of howler monkeys, the brown howler (Alouatta guariba clamitans) and the black-and-gold howler (A. caraya), in northeastern Argentina. During 12 months, we collected activity data on 2 groups of each species characterized by different sizes and degrees of home-range overlap, together with data on food availability. We analyzed seasonal variation in activity budgets and daily activity patterns, as well as the relationships between monthly activity budget and food availability, diet, and climate, both within and between species. Black-and-gold howlers, more clearly than brown howlers, adopted an energy-minimization strategy, reducing costly activities such as moving and traveling, during the lean season. Within each howler species, individuals in the largest group showed a greater proportion of time spent moving or traveling, or both, compared to individuals in the smallest group, suggesting the existence of within-group food competition. Juveniles of both species rested less and moved and socialized more than adults. Overall, black-and-gold howlers spent proportionately more time moving and traveling, and less time resting, probably due to their larger mean group size, than brown howlers. Daily feeding peak times diverged only slightly among groups in the lean season, but differences between groups of different species with overlapping home ranges were not larger than those among scarcely or nonoverlapping groups (of same or different species). In conclusion, even though the 2 howler species showed differences in activity patterns, mainly related to differences in their response to food seasonality, and in group size, we found no evidence of time partitioning.

Yellow fever impact on brown howler monkeys (Alouatta guariba clamitans) in Argentina: a metamodelling approach based on population viability analysis and epidemiological dynamics.

In South America, yellow fever (YF) is an established infectious disease that has been identified outside of its traditional endemic areas, affecting human and nonhuman primate (NHP) populations. In the epidemics that occurred in Argentina between 2007-2009, several outbreaks affecting humans and howler monkeys (Alouatta spp) were reported, highlighting the importance of this disease in the context of conservation medicine and public health policies. Considering the lack of information about YF dynamics in New World NHP, our main goal was to apply modelling tools to better understand YF transmission dynamics among endangered brown howler monkey (Alouatta guariba clamitans) populations in northeastern Argentina. Two complementary modelling tools were used to evaluate brown howler population dynamics in the presence of the disease: Vortex, a stochastic demographic simulation model, and Outbreak, a stochastic disease epidemiology simulation. The baseline model of YF disease epidemiology predicted a very high probability of population decline over the next 100 years. We believe the modelling approach discussed here is a reasonable description of the disease and its effects on the howler monkey population and can be useful to support evidence-based decision-making to guide actions at a regional level.

Building a Species Conservation Strategy for the Brown Howler Monkey (Alouatta Guariba Clamitans) in Argentina in the Context of Yellow Fever Outbreaks

The brown howler monkey (Alouatta guariba clamitans) is endemic to South Americas Atlantic Forest, with a small population extending into the northern portion of Misiones province in northeastern Argentina. In 2012, the species was classified as Critically Endangered in Argentina due to its highly restricted distribution, low population density and dramatic declines from recent Yellow Fever outbreaks. In March 2013, we organized an international workshop in Misiones to evaluate population status in Argentina and conduct a threat analysis. We developed population viability models using Vortex and Outbreak software packages. These tools allowed us to explore how several biological and demographic parameters of brown howlers, as well as factors related to Yellow Fever epidemiology, affect the probability of species extinction. The discussion among diverse specialists and analysis of model results identified Yellow Fever as the main threat to brown howler population persistence in Argentina. Our threat analysis, focused on the dynamics of Yellow Fever outbreaks and their impact on howler populations, led to the identification of gaps in knowledge that helped prioritize objectives and actions for the development of a Species Conservation Strategy in Argentina.

Experimental testing of reciprocal effects of nutrition and parasitism in wild black capuchin monkeys

Nutritional stress may predispose individuals to infection, which in turn can have further detrimental effects on physical condition, thus creating an opportunity for reciprocal effects between nutrition and parasitism. Little experimental investigation has been conducted on this “vicious circle” hypothesis in wild animals, especially under natural conditions. We evaluated the reciprocal effects of nutritional status and parasitism using an experimental approach in two groups of wild black capuchin monkeys (Sapajus nigritus). Across two consecutive winters, we collected faecal samples from identified capuchins to determine presence and load of gastrointestinal helminthes, and measured individual body mass as a proxy of physical condition. Food availability was manipulated by provisioning monkeys with bananas, and parasite burdens by applying antiparasitic drugs to selected individuals. We found no effect of antiparasitic drugs on physical condition, but parasite loads decreased in response to high levels of food availability. Our results represent the first experimental evidence that the nutritional status may drive parasite dynamics in a primate.

ATLANTIC MAMMAL TRAITS: a data set of morphological traits of mammals in the Atlantic Forest of South America

Measures of traits are the basis of functional biological diversity. Numerous works consider mean species-level measures of traits while ignoring individual variance within species. However, there is a large amount of variation within species and it is increasingly apparent that it is important to consider trait variation not only between species, but also within species. Mammals are an interesting group for investigating trait-based approaches because they play diverse and important ecological functions (e.g., pollination, seed dispersal, predation, grazing) that are correlated with functional traits. Here we compile a data set comprising morphological and life history information of 279 mammal species from 39,850 individuals of 388 populations ranging from -5.83 to -29.75 decimal degrees of latitude and -34.82 to -56.73 decimal degrees of longitude in the Atlantic forest of South America. We present trait information from 16,840 individuals of 181 species of non-volant mammals (Rodentia, Didelphimorphia, Carnivora, Primates, Cingulata, Artiodactyla, Pilosa, Lagomorpha, Perissodactyla) and from 23,010 individuals of 98 species of volant mammals (Chiroptera). The traits reported include body mass, age, sex, reproductive stage, as well as the geographic coordinates of sampling for all taxa. Moreover, we gathered information on forearm length for bats and body length and tail length for rodents and marsupials. No copyright restrictions are associated with the use of this data set. Please cite this data paper when the data are used in publications. We also request that researchers and teachers inform us of how they are using the data.