Eckhard W. Heymann

The behavioural ecology of mixed-species troops of callitrichine primates

This review summarizes information on the behavioural ecology of mixed‐species troops (interspecific associations) formed by different species of callitrichines, small New World monkeys, in western and central Amazonia. The formation of mixed‐species troops is an integral part of the biology of several species of this subfamily. Niche separation between associated species is obtained through vertical segregation which results in differences in the prey spectrum. The degree of niche separation is a predictor for the stability of mixedspecies troops. Individuals may benefit from the formation of mixed‐species troops through increased safety from predators, increased foraging effciency, and or increased resource defence. Costs of mixed‐species troop formation are probably very low and mainly relate to patterns of interspecific behavioural interactions. We point to gaps in our knowledge and suggest pathways for future research into mixed‐species troops.

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

A Field observation of predation on a Moustached Tamarin(Saguinus mystax) by an Anaconda

Snakes are supposed to be predators of callitrichids (Hershkovitz, 1977) but hitherto no factual information has been available. The following report o f an anaconda (Eunectes murinus) preying on a moustached tamarin (Saguinus mystax) is the first observation of snake predation on a New World callitrichid monkey. The observation took place on January 20, 1986, on Padre Isla, an 8-km 2 island in the Amazon River in northeastern Peru, where wild-trapped moustached tamarins were released in 1977, 1978, and 1980 (Soini, 1985). At 1112 hr four of the nine animals in the study group crossed a narrow lake on fallen tree trunks; they returned on the same trunks at 1221 hr. At 1325 hr the group gathered near the tree trunks, and at 1329 hr one animal climbed down and crossed the lake on these tree trunks again. One minute later, the groups adult female started to walk along the same tree trunks. During her walk she stopped four times and looked forward. About 20 sec after the female had started to walk along the tree trunks she was seized during a jump by an anaconda. At the moment of being seized, the adult female gave a harsh cry. The anaconda threw three coils o f its body around the female. Two other tamarins that arrived at the site where the adult female had been caught looked at the anaconda and emitted excitation calls, in which the rest of the group joined. One of these two tamarins then ran away quickly, while the other jumped to a tree t runk above the anaconda and stared at it twice. Then it, too, ran away. No other group member crossed the lake. At 1339 hr the group left the scene of the incident. At 1350 hr the head of the anaconda was seen, and at 1353 hr the snake started to loosen the coils

Field Observation of Snake-Mobbing in a Group of Saddle-Back Tamarins, Saguinus fuscicollis nigrifrons

At the Rio Blanco in Northeastern Peru a group of 6 saddle-back tamarins was observed to mob two Corallus enydris snakes which were hanging from a liana. These and other observations of snake-mobbing demonstrate that callitricids exhibit a special behaviour against potential predators, which is very similar to the mobbing displays of birds and other mammals. It is suggested that the adaptive significance of snake-mobbing in tamarins lies in the cultural transmission of information about potential predators.

Malaria infection and host behavior : a comparative study of Neotropical primates

Parasites are ubiquitous in populations of free-ranging animals and impact host fitness, but virtually nothing is known about the factors that influence patterns of disease risk across species and the effectiveness of behavioral defenses to reduce this risk. We investigated the correlates of malaria infection (prevalence) in Neotropical primates using data from the literature, focusing on host traits involving group size, body mass, and sleeping behavior. Malaria is spread to these monkeys through anopheline mosquitoes that search for hosts at night using olfactory cues. In comparative tests that used two different phylogenetic trees, we confirmed that malaria prevalence increases with group size in Neotropical primates, as suggested by a previous non-phylogenetic analysis. These results are consistent with the hypothesis that larger groups experience increased risk of attack by mosquitoes, and counter to the hypothesis that primates benefit from the encounter-dilution effect of avoiding actively-seeking insects by living in larger groups. In contrast to non-phylogenetic tests, body mass was significant in fewer phylogeny-based analyses, and primarily when group size was included as a covariate. We also found statistical support for the hypothesis that sleeping in closed microhabitats, such as tree holes or tangles of vegetation, reduces the risk of malaria infection by containing the host cues used by mosquitoes to locate hosts. Due to the small number of evolutionary transitions in sleeping behavior in this group of primates, however, this result is considered preliminary until repeated with a larger sample size. In summary, risk of infection with malaria and other vector-borne diseases are likely to act as a cost of living in groups, rather than a benefit, and sleeping site selection may provide benefits by reducing rates of attack by malaria vectors.

Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: diversity and characteristics of plant species.

In a comparative study of Saguinus mystax and Saguinus fuscicollis, we examined the spectrum of plant species whose seeds are dispersed by these two tamarin species. We characterize these plants in terms of life form, fruit colour, pulp consistency and seed dimensions. The tamarins disperse a much broader spectrum of plant species than previously reported (88 of the total of 155 species exploited for fruit). While the distribution over plant life form, fruit colour and pulp consistency is identical between dispersed plant species and the overall spectrum of consumed plant species, clear differences exist in all seed parameters (length, width, height, volume, mass) except specific weight between dispersed and non-dispersed plant species for both tamarin species. Plant and fruit characteristics and seed parameters of dispersed plant species do not differ between S. mystax and S. fuscicollis, suggesting that their ecological and evolutionary interaction with plants is very similar or identical.

Boa constrictor attack and successful group defence in moustached tamarins, Saguinus mystax.

Co-operative defence against predators is probably one of the advantages of primate sociality [Schaik, 1983]. It usually takes the form of vigilance and mobbing of predators, but in larger primates may also involve attacking predators [Cheney and Wrangham, 1987]. The small-bodied callitrichines are often considered as relying on crypticity rather than on active defence [Isbell, 1994], but they mob all major types of predators [Bartecki and Heymann, 1987; Ferrari and Lopes Ferrari, 1990]. Here we report on the rescue of a Saguinus mystax, captured by a Boa constrictor, through the action of other group members.

Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group.

Tamarins of the genus Saguinus, subfamily Callitrichinae, represent one of the most diverse primate radiations. So far, about 35 taxa have been described, but detailed information about their taxonomy and phylogeny is still lacking. To further elucidate the phylogenetic relationships and the biogeographic history within the genus, and to contribute to a more reliable classification of its taxa, we sequenced the complete mitochondrial cytochrome b gene and the hypervariable region I of the D-loop. Therefore, we mainly used fecal samples from wild tamarins collected during two expeditions to the Peruvian Amazon, an area of high tamarin diversity. Our data suggest that the numerous taxa of the S. nigricollis species group are derived from a common ancestor that separated from the other representatives of the genus ~10 mya. Most taxa of the S. nigricollis group form monophyletic clusters, which mainly originated in a single rapid radiation ~2.9 mya. S. fuscicollis and S. nigricollis appear as polyphyletic taxa, but we could identify various clusters, which are mainly consistent with differences in coat coloration. We could confirm most of the existing taxa as distinct entities and suggest species status for fuscicollis, illigeri, lagonotus, leucogenys, nigricollis, nigrifrons, tripartitus, and weddelli. Our genetic data do not support a separate status for melanoleucus and graellsi, but due to differences in fur coloration, we give them subspecies status. The species group most likely originated in western Amazonia and diversified during the decline of the Acre wetland and the formation of the Amazonian river system.

Geophagy in moustached tamarins,Saguinus mystax (platyrrhini: Callitrichidae), at the Río Blanco, Peruvian Amazonia

During a field study at the Río Blanco in northeastern Peru between June and September 1990, moustached tamarins (Saguinus mystax) were observed to feed on soil material on three different occasions. Soil was taken directly from bare spots of surface soil (two observations) and from the broken mound of leaf-cutting ants (Atta sp.; one observation). Exposed surface soil is rare throughout the study area. Geochemical analyses of the soils that were consumed showed elevated concentrations of several elements in the ant mound sample compared to the other two soil samples. The most likely hypothesis for the function of soil feeding in moustached tamarins is that it serves in mineral supplementation.

Characterization and Social Correlates of Fecal Testosterone and Cortisol Excretion in Wild Male Saguinus mystax

Reproductive success in male primates can be influenced by testosterone (T) and cortisol (C). We examined them in wild Saguinus mystax via fecal hormone analysis. Firstly, we wanted to characterize male hormonal status over the course of the year. Further we tested the influence of the reproductive status of the breeding female, social instability, and intergroup encounter rates on T levels, comparing the results with predictions of the challenge hypothesis (Wingfield et al., 1990). We also tested for interindividual differences in hormonal levels, possibly related to social or breeding status. We collected data during a 12-mo study on 2 groups of moustached tamarins at the Estación Biológica Quebrada Blanco in northeastern Peru. We found fairly similar T and C levels over the course of the year for all males. Yet an elevation of T shortly after the birth of infants, during the phase of ovarian inactivity of the group’s breeding female, was evident. Hormonal levels were not significantly elevated during a phase of social instability, did not correlate with intergroup encounter rates, and did not differ between breeding and nonbreeding males. Our results confirm the challenge hypothesis (Wingfield et al., 1990). The data suggest that reproductive competition in moustached tamarins is not based on endocrinological, but instead on behavioral mechanisms, possibly combined with sperm competition.