Ingrid Holzmann

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.

Production of Loud and Quiet Calls in Howler Monkeys

One of the most striking features of howler monkeys’ natural history is their loud call, which gives the genus Alouatta its common name in English. However, the disproportionate focus on functional aspects of those calls has driven attention away from other relevant issues related to their vocal behavior. In this chapter, we review the studies of acoustic structure conducted so far on these peculiar calls, highlighting the variation among and within the species of this genus. The variation we uncover runs against the notion of uniformity among howler monkeys, but we do find that the relationship between loud call structure and phylogeny compliments genetic work in this genus. We also show how the anatomy of howler monkey’s vocal organs can explain the unusual features of their loud calls and possibly the variation found between species, while also pointing to the various gaps that exist in our knowledge regarding the role of the several components of their highly specialized vocal apparatus. Additionally, we review some basic concepts about sound propagation and geographic variation in long-distance communication. Unlike loud calls, we know relatively little about the low-amplitude calls of howler monkeys. Such calls have received a great deal of attention in the literature, particularly in Old World monkeys, because they can offer insights into the social lives of these animals. Because few comparable studies have been conducted on howler monkeys, we propose some lines of future research that we deemed potentially interesting. We conclude with some methodological approaches to recording howler monkey calls in the field and for sharing vocalizations with other researchers.

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.

Function of Loud Calls in Howler Monkeys

Beyond the unique sound of howler monkey vocalizations, their vigorous loud calling displays are perplexing given the otherwise sedentary lifestyle of these primates. Here we provide potential explanations for this energetic investment by reviewing all available functional studies conducted to date. We highlight the variation among and even within species when we explore whether male loud calls are used in group cohesion, predator avoidance, attraction of females, or competition with other males or other groups over resources. In the competition scenario, we examine strategies of avoidance versus direct competition and whether contests are focused on defense of space, food, mates, or infants. We suggest that much of the debate surrounding the function of loud calls stems from methodological differences among researchers and from the varied levels of analyses used, although we also demonstrate that studies of form and function can be intertwined. We emphasize the need to examine different call types separately and discuss the role of howling in intragroup male relationships. Finally, we address the understudied role of female loud calling and the potential use of hybrid populations to examine the evolution of species-typical loud calls. We conclude with some practical hints for designing field tests to uncover functional significance.

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.

Natural History, Distribution, and Conservation of Two Nomadic Sporophila Seedeaters Specializing on Bamboo in The Atlantic Forest

Abstract. Semelparous woody bamboos flower fairly synchronously and in clocklike fashion after many years, providing abundant and nutritious seeds. However, this resource is ephemeral, localized, and unpredictable from the perspective of birds that feed on those seeds. Birds specializing on bamboo seeds track this food source and are nomadic. We recorded Temmincks Seedeater (Sporophila falcirostris) at 29 localities and the Buffy-fronted Seedeater (S. frontalis) at 23 localities in Argentina, Paraguay, and southeastern Brazil. In these species, nomadism is unassociated with any seasonal factor: birds may persist year round over several consecutive years if the seed supply is constant enough. Most occurrences and all breeding records were related to masting of bamboo; records of isolated birds away from seeding bamboo must represent individuals searching for bamboo patches. We report winter breeding of these species for the first time and demonstrate that the supply of bamboo seeds is the main limitation to their breeding. On a broad spatiotemporal scale, large-seeded bamboos (e.g., Guadua spp.) may function as strong population pumps, small-seeded bamboos (e.g., Chusquea spp.) as maintenance stations. Both species fed mostly on bamboo seeds, occasionally on bamboo flowers, and rarely on alternative food sources. They consumed insects frequently and occurred in mixed-species flocks, especially during autumn and winter. Creation of a network of protected areas is essential to preserve bamboo patches that flower at different times and localities in sufficiently large quantities to guarantee the long-term survival of the peculiarly dynamic populations of bamboo seedeaters.

Mate recognition systems and species limits in a warbling-finch complex (Poospiza nigrorufa/whitii)

ABSTRACT Species limits in the Poospiza nigrorufa/whitii complex are not well understood. Three taxa formally described as species are now considered as subspecies (nigrorufa, whitii and wagneri) of a widespread species. The heavier nigrorufa has longer bill, tarsus and wings, is slightly dimorphic with males showing tawny rufous throat, breast and flanks, and brownish grey upper parts with a slate tinge, while females differ in the orange tinge of ventral parts and in the more olivaceous upper parts; inhabits shrubby open areas and wetlands with reeds and bulrushes in eastern southern South America, and gives a simple three-note pattern that repeats to form the song and diagnostic calls. The lighter whitii (including wagneri as a synonym) has a shorter bill, tarsus and wings, is highly dimorphic with males having dark chestnut throat, breast and flanks, and slate upper parts, while females exhibit tawny pale-orange ventral parts, and olivaceous light-brown upper parts; inhabits closed to semi-closed xerophytic to semi-humid scrub and woodlands in the western highlands, and has a complex multi-noted song and diagnostic calls. Reciprocal playback experiments indicate that both taxa are able to discriminate each other’s songs. Locality data and ecological niche modelling show that nigrorufa and whitii are narrowly allopatric or parapatric in central Córdoba province (Argentina).This integrative evidence and the ~2.5% divergence in mtDNA show that nigrorufa and whitii possess different Specific Mate Recognition Systems and should be afforded full species status under any species concept.