Martín M. Kowalewski

Possible fruit protein effects on primate communities in madagascar and the neotropics.

Background The ecological factors contributing to the evolution of tropical vertebrate communities are still poorly understood. Primate communities of the tropical Americas have fewer folivorous but more frugivorous genera than tropical regions of the Old World and especially many more frugivorous genera than Madagascar. Reasons for this phenomenon are largely unexplored. We developed the hypothesis that Neotropical fruits have higher protein concentrations than fruits from Madagascar and that the higher representation of frugivorous genera in the Neotropics is linked to high protein concentrations in fruits. Low fruit protein concentrations in Madagascar would restrict the evolution of frugivores in Malagasy communities. Methodology/Principal Findings We reviewed the literature for nitrogen concentrations in fruits from the Neotropics and from Madagascar, and analyzed fruits from an additional six sites in the Neotropics and six sites in Madagascar. Fruits from the Neotropical sites contain significantly more nitrogen than fruits from the Madagascar sites. Nitrogen concentrations in New World fruits are above the concentrations to satisfy nitrogen requirements of primates, while they are at the lower end or below the concentrations to cover primate protein needs in Madagascar. Conclusions/Significance Fruits at most sites in the Neotropics contain enough protein to satisfy the protein needs of primates. Thus, selection pressure to develop new adaptations for foods that are difficult to digest (such as leaves) may have been lower in the Neotropics than in Madagascar. The low nitrogen concentrations in fruits from Madagascar may contribute to the almost complete absence of frugivorous primate species on this island.

Birth Seasonality in Alouatta caraya in Northern Argentina

Given appropriate ecological and social conditions, natural selection should favor individuals that can concentrate their reproductive events to a particular time of the year that offers high opportunities for infant survivorship. Previous studies on births in Alouatta caraya in Northern Argentina revealed the existence of a peak during the dry season—a period with scarcity of food resources—in mainland gallery forest (G. E. Zunino, Extra 133: 1–10, 1996). The time of conception and the period of independence of the offspring are positively correlated with precipitation, temperature and availability of food. Offspring became independent from their mothers when the availability of resources was high, and conception coincided with the peak of fruit production. Our goal was to examine patterns of birth seasonality in Alouatta caraya in flooded forest on an island in Northern Argentina for comparison with the mainland population. Both sites are at similar latitudes, but differ in forest type. The results indicate that the availability of new and mature leaves is more consistent throughout the year in the flooded forest (p<0.05); however, there was no difference in the availability of fleshy fruits between sites (p>0.05). The pattern of births differed between the gallery forest and the flooded forest (2-way Anova, p<0.001). In the flooded forest births occurred throughout the year, which supports the contentions that howlers do not have a fixed birth season and that the observed variation in the timing of births appears to represent a facultative behavioral response to changes in food availability.

Mating promiscuity and reproductive tactics in female black and gold howler monkeys (Alouatta caraya) inhabiting an island on the Parana river, Argentina

In several primate species, females mate promiscuously and several adult males peacefully co‐reside in the same social group. We investigated female mating behavior in two neighboring multimale–multifemale groups of Alouatta caraya in northern Argentina (27°20′S–58°40′W). All adult individuals in each group were marked with identification anklets and ear tags, and followed for five consecutive full days per month during 20 consecutive months. We recorded 219 copulations for eight resident females in these two groups. Thirty‐two percent of matings involved extra‐group copulations and 68% were with resident males. During periods when females were likely to conceive and during periods when females were nonfertile (pregnancy and lactation), there were no significant differences in the average number of resident and nonresident males with which they copulated (G‐test: Gadj=0.1, df=3, P>0.05). In both of our study groups, adult males were tolerant of the mating activities between resident males and resident females, but acted aggressively and collectively (howling, border vigilance, and fighting) when extragroup males attempted to enter the group and mate with resident females. Given the frequency of extragroup matings, we examined the distance females traveled to engage in these copulations, time engaged in pre‐ and postcopulatory behavior, and the risk of injury during extragroup copulations. These costs were found to be relatively small. We suggest that female promiscuity is the prime driver or constraint on male reproductive opportunities in this species. Female promiscuity in A. caraya appears to represent a mixed mating strategy that may serve to increase opportunities for genetic diversity between a females successive offspring as well as minimize the risk of infanticide by spreading paternity estimates across a larger number of adult males. Am. J. Primatol. 72:734–748, 2010.

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. Am. J. Primatol. 73:75–83, 2011.

Impact of Deforestation on a Population of Alouatta caraya in Northern Argentina

Some kinds of disturbance, such as selective logging and clear-felling, may alter population parameters [1] and assume special importance when they alter the density or distribution of tree species used by the primates, thus altering their diet [2]. The goal in this study was to determine if a reduction in the area of suitable forest had an effect on the associated population of Alouatta caraya. We evaluated the effects of forest disturbance using several population parameters, such as ecological density, absolute density, number of animals, relative biomass and total biomass.

Howler monkeys : behavior, ecology, and conservation

PART 1. INTRODUCTION.- Chapter 1. Why is it Important to Continue Studying the Behavioral Ecology and Conservation Management of Howler Monkeys?.- PART 2: BEHAVIORAL ECOLOGY.- Chapter 2. Diets of Howler Monkeys.- Chapter 3. Insights into Reproductive Strategies and Sexual Selection in Howler Monkeys.- Chapter 4. Evidence of Alternative Dietary Syndromes and Nutritional Goals in the Genus Alouatta.- Chapter 5. Seed Dispersal by Howler Monkeys: Current Knowledge, Conservation Implications, and Future Directions.- Chapter 6. Interactions of Howler Monkeys with Other Vertebrates: A Review.- Chapter 7. Solving the Collective Action Problem During Intergroup Encounters: The Case of Black and Gold Howler Monkeys.- Chapter 8. Howler Monkey Positional Behavior.- Chapter 9. Ranging Behavior and Spatial Cognition of Howler Monkeys.- PART 3: CONSERVATION AND MANAGEMENT.- Chapter 10. The Ethnoprimatology of Howler Monkeys (Alouatta spp.): From Past to Present.- Chapter 11. Anthropogenic Habitat Modification, Tourist Interactions and Crop-Raiding in Howler Monkeys.- Chapter 12. Health and Welfare of Howler Monkeys in Captivity.- Chapter 13. Fruit as a Key Factor in Howler Monkey Population Density: Conservation Implications. Chapter 14. Conservation of Alouatta: Social and Economic Drivers of Habitat Loss, Information Vacuum and Mitigating Population Declines.- PART 4: CONCLUSION.- Chapter 15. New Challenges in the Study of Howler Monkey Behavioral Ecology and Conservation: Where we are and where we need to go?.

Howler Monkeys: Adaptive radiation, systematics, and morphology

Part 1. Introduction.- Chapter 1. Why is it Important to Continue Studying the Anatomy, Physiology, Sensory Ecology, and Evolution of Howler Monkeys?.- Part 2. Taxonomy, Genetics, Morphology and Evolution.- Chapter 2. Fossil Alouattines and the Origins of Alouatta: Craniodental Diversity and Interrelationships.- Chapter 3. The Taxonomy of Howler Monkeys: Integrating Old and New Knowledge from Morphological and Genetic Studies.- Chapter 4. Cytogenetics of Howler Monkeys.- Chapter 5. Hybridization in Howler Monkeys: Current Understanding and Future Directions.- Chapter 6. Morphology of Howler Monkeys: A Review and Quantitative Analyses.- Part 3. Physiology.- Chapter 7. Hematology and Serum Biochemistry in Wild Howler Monkeys.- Chapter 8. Endocrinology of Howler Monkeys: Review and Directions for Future Research.- Chapter 9. The Howler Monkey as a Model for Exploring Host-Gut Microbiota Interactions in Primates.- Chapter 10. Ecological Determinants of Parasitism in Howler Monkeys.- Part 4. Ontogeny and Sensory Ecology.- Chapter 11. An Ontogenetic Framework for Alouatta: Infant Development and Evaluating.- Chapter 12.The Sensory Systems of Alouatta: Evolution with an Eye to Ecology.- Chapter 13. Production of Loud and Quiet Calls in Howler Monkeys.- Chapter 14. Function of Loud Calls in Howler Monkeys.- Part 5. Conclusions.- Chapter 15. New Challenges in the Study of Howler Monkey Anatomy, Physiology, Sensory Ecology, and Evolution: Where we are and where we need to go?.

Ecological and Anthropogenic Influences on Patterns of Parasitism in Free-Ranging Primates: A Meta-analysis of the Genus Alouatta

Parasites play a central role in tropical ecosystems, affecting the ecology and evolution of species interactions, host population growth and regulation, and community biodiversity (Esch and Fernandez 1993; Hudson, Dobson and Newborn 1998; Hochachka and Dhondt 2000; Hudson et al. 2002). Our understanding of how natural and anthropogenic factors affect host-parasite dynamics in free-ranging primate populations (Gillespie, Chapman and Greiner 2005a; Gillespie, Greiner and Chapman 2005b; Gillespie and Chapman 2006) and the relationship between wild primates and human health in rural or remote areas (McGrew et al. 1989; Stuart et al. 1990; Muller-Graf, Collins and Woolhouse 1997; Gillespie et al. 2005b; Pedersen et al. 2005) remain largely unexplored. The majority of emerging infectious diseases are zoonotic – easily transferred among humans, wildlife, and domesticated animals – (Nunn and Altizer 2006). For example, Taylor, Latham and Woolhouse (2001) found that 61% of human pathogens are shared with animal hosts. Identifying general principles governing parasite occurrence and prevalence is critical for planning animal conservation and protecting human health (Nunn et al. 2003). In this review, we examine how various ecological and anthropogenic factors affect patterns of parasitism in free-ranging howler monkeys (Genus Alouatta).

The Effects of Captivity on the Mammalian Gut Microbiome.

Synopsis Recent studies increasingly note the effect of captivity or the built environment on the microbiome of humans and other animals. As symbiotic microbes are essential to many aspects of biology (e.g., digestive and immune functions), it is important to understand how lifestyle differences can impact the microbiome, and, consequently, the health of hosts. Animals living in captivity experience a range of changes that may influence the gut bacteria, such as diet changes, treatments, and reduced contact with other individuals, species and variable environmental substrates that act as sources of bacterial diversity. Thus far, initial results from previous studies point to a pattern of decreased bacterial diversity in captive animals. However, these studies are relatively limited in the scope of species that have been examined. Here we present a dataset that includes paired wild and captive samples from mammalian taxa across six Orders to investigate generalizable patterns of the effects captivity on mammalian gut bacteria. In comparing the wild to the captive condition, our results indicate that alpha diversity of the gut bacteria remains consistent in some mammalian hosts (bovids, giraffes, anteaters, and aardvarks), declines in the captive condition in some hosts (canids, primates, and equids), and increases in the captive condition in one host taxon (rhinoceros). Differences in gut bacterial beta diversity between the captive and wild state were observed for most of the taxa surveyed, except the even-toed ungulates (bovids and giraffes). Additionally, beta diversity variation was also strongly influenced by host taxonomic group, diet type, and gut fermentation physiology. Bacterial taxa that demonstrated larger shifts in relative abundance between the captive and wild states included members of the Firmicutes and Bacteroidetes. Overall, the patterns that we observe will inform a range of disciplines from veterinary practice to captive breeding efforts for biological conservation. Furthermore, bacterial taxa that persist in the captive state provide unique insight into symbiotic relationships with the host.

Evidence of Alternative Dietary Syndromes and Nutritional Goals in the Genus Alouatta

Howler monkeys exploit difficult-to-digest and potentially toxic food items such as mature leaves and unripe fruits; persist across an extreme range of habitat types, including highly disturbed forests; and have the most widespread geographical distribution of any genus of New World primate. Given evidence of dietary variability in the amount of monthly fruit, leaf, and flower consumption, howler monkeys provide an instructive model for examining relationships among foraging strategies, activity budgets, and patterns of habitat utilization. In this chapter we examined evidence for interspecific differences in dietary patterns and nutritional ecology within the genus Alouatta and identified three dietary “syndromes” that are generally consistent with howler monkey phylogeny and biogeography. Specifically, we show that Mesoamerican howler monkeys and A. seniculus are characterized by a balanced leaf and fruit diet, Amazonian species by a fruit enriched diet, and Atlantic Forest and southern howler monkeys by a leaf-enriched diet. Finally, to be able to identify species-specific dietary strategies and syndromes across the primate Order, we recommend an approach that includes collecting data on feeding rates and the nutritional composition of the diet.