Ateline Primates Research Articles

Modelling 21st century refugia and impact of climate change on Amazonia's largest primates

Edaphic and vegetation conditions can render climatically suitable sites inadequate for a species to persist, constraining the amount of suitable habitat and the possibilities of tracking preferred climatic conditions as they shift in response to climate change. We combined climatic and remotely sensed data to model current and future distributions of nine extant taxa of ateline primates across the Amazon basin. We used the models to identify and quantify potential range changes and refugia of suitable habitat from the present to the latter half of the 21st century. We applied an ensemble forecasting approach for species distribution models using 596 spatially rarefied occurrences. We parameterised these models combining reflectance data from a basin‐wide Landsat TM/ETM+ image composite, and three sets of bioclimatic layers containing data for the current time period, and two different (moderate and worst‐case) climate change scenarios for 2041–2070. Eight out of nine taxa are likely to experience pronounced range losses, with seven of them predicted to lose over 50% of their currently suitable habitats irrespective of climate change scenarios. Modelled ateline richness exhibited a broad decrease in high‐richness areas, and a possible redistribution along the northernmost parts of western Amazonia. Refugia from 21st century climate change for the whole complex were mostly concentrated in western Amazonia, especially in its southern part. We identified hotspots of vulnerability to climate change and 21st century refugia for all Amazonian atelines while accounting for habitat characteristics that are important to guarantee the continued existence of suitable habitats for these strictly arboreal taxa. Increasing the understanding of climate change impacts on Amazonia's largest primates can help to inform spatial conservation planning decisions and management to sustain forest‐dwelling biodiversity over large areas such as Amazonia.

Reproductive seasonality in two sympatric primates (Ateles belzebuth and Lagothrix lagotricha poeppigii) from Amazonian Ecuador.

With their large body size and "slow" life histories, atelin primates are thought to follow a risk-averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species-white-bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)-in relation to habitat-wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35)and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high-levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year-round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk-averse breeding strategy.

Spider Monkeys Rule the Roost: Ateline Sleeping Sites Influence Rainforest Heterogeneity.

Simple SummarySpider monkeys are important dispersers of many hardwood trees that contribute greatly to the carbon sequestration of tropical forests. One way in which Spider monkeys influence tropical ecosystem structure and function is through the creation of visible terrestrial latrines beneath their “sleeping sites”—trees in which they frequently return to sleep. Spider monkey latrines are thought to create high quality resource patches for rainforest plants and other wildlife to exploit. We investigate this using camera traps placed in both the canopy and on the rainforest floor to determine which rainforest wildlife are attracted to the latrines beneath the sleeping sites of spider monkeys. We also assess the tree species and dung beetles found within the latrines compared with other areas of the forest. Our evidence suggests that spider monkey roosting sites are a hub of activity for other rainforest wildlife, and act as germinating beds for many rainforest trees. If rainforests were to lose spider monkeys, from intensive hunting for example, many other rainforest wildlife species would be affected, and forests would therefore be made up of different tree communities than landscapes where spider monkeys exist.The sleeping site behavior of Ateline primates has been of interest since the 1980s, yet limited focus has been given to their influence upon other rainforest species. Here, we use a combination of arboreal and terrestrial camera traps, and dung beetle pitfall traps, to characterize spider monkey sleeping site use and quantify the impact of their associated latrines on terrestrial vertebrate and dung beetle activity. We also characterize the physical characteristics of the sleeping sites and the floristic and soil composition of latrines beneath them. Spider monkey activity at sleeping sites peaked at dawn and dusk and group composition varied by sex of the adults detected. The habitat-use of terrestrial fauna (vertebrates and dung beetles) differed between latrine sites and non-latrine controls, underpinned by species-specific changes in the relative abundance of several seed-dispersing species (such as paca and great curassow). Seedling density was higher in latrines than in non-latrine controls. Although most soil properties were similar between latrines and controls, potassium and manganese concentrations were different. These results suggest that spider monkey sleeping site fidelity leads to a hotspot of ecological activity in latrines and downstream impacts on rainforest floristic composition and diversity.

A pan-neotropical analysis of hunting preferences

Hunting in the neotropics is a widespread form of resource extraction. However, there is increasing concern that current activities are leading to the decline and extirpation of vulnerable species; particulary ateline primates, large ungulates (such as tapirs and white-lipped peccaries) and large birds such as curassows. Hunting patterns are expected to be a product of two principal influences: the value of return for a given amount of effort invested into hunting, and cultural factors that determine the prestige and usefulness of prey. Previous work has suggested that hunting profiles change in a predictable way over time, becoming more diverse and more dependent on smaller bodied species as preferred, large-bodied prey become scarcer. In this paper, we evaluate the hunting profiles of 78 neotropical communities in Central and South America. We investigate the uniformity of species preferences, whether communities that are geographically closer have similar hunting profiles, and whether the age and size of settlements can be used to predict the type and diversity of species targeted. We found that there was only a weak correlation between the structure of communities’ hunting profiles and their geographical proximity. Neither a community’s size nor age was a good predictor of the shape and structure of its hunting profile. Our data suggest that either the availability of prey or the cultural influences dictating the value of different species can change rapidly over small distances, and that older and larger settlements do not impact prey species distributions in a predictable way.

Effects of logging, hunting, and forest fragment size on physiological stress levels of two sympatric ateline primates in Colombia.

Habitat fragmentation and anthropogenic disturbances are of major concern to the conservation of endangered species because of their potentially negative impact on animal populations. Both processes can impose physiological stress (i.e. increased glucocorticoid output) on animals, and chronically elevated stress levels can have detrimental effects on the long-term viability of animal populations. Here, we investigated the effect of fragment size and human impact (logging and hunting pressure) on glucocorticoid levels of two sympatric Neotropical primates, the red howler monkey (Alouatta seniculus) and the critically endangered brown spider monkey (Ateles hybridus). These two species have been reported to contrast strongly in their ability to cope with anthropogenic disturbances. We collected faecal samples from eight spider monkey groups and 31 howler monkey groups, living in seven and 10 different forest fragments in Colombia, respectively. We measured faecal glucocorticoid metabolite (FGCM) levels in both species using previously validated methods. Surprisingly, fragment size did not influence FGCM levels in either species. Spider monkeys showed elevated FGCMs in fragments with the highest level of human impact, whereas we did not find this effect in howler monkeys. This suggests that the two species differ in their physiological responsiveness to anthropogenic changes, further emphasizing why brown spider monkeys are at higher extinction risk than red howler monkeys. If these anthropogenic disturbances persist in the long term, elevated FGCM levels can potentially lead to a state of chronic stress, which might limit the future viability of populations. We propose that FGCM measurements should be used as a tool to monitor populations living in disturbed areas and to assess the success of conservation strategies, such as corridors connecting forest fragments.

Genetic Structure and Kinship Patterns in a Population of Black Howler Monkeys,Alouatta pigra, atPalenqueNationalPark,Mexico

We investigated the genetic structure and kinship patterns of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. Fecal samples from 49 individuals residing in eight social groups were successfully genotyped for 19 polymorphic microsatellite markers known to be variable in other ateline primates. Overall, genetic diversity was low (H(o) = 0.588) with an average of 4.2 alleles per loci (range = 2-8). We found that intergroup genetic variation among adults was relatively high (mean between-group F(ST) = 0.119), largely due to the genetic divergence of one study group from the others. Intragroup kinship patterns showed that in most social groups, either adult males, adult females, or individuals of both sexes resided with same-sexed adult kin, suggesting that some black howler males and females may not disperse from their natal group or may disperse with related individuals. Of the six sampled immigrant males, two males joined established groups by themselves, and four males formed two pairs that each took over the social group they joined after evicting the resident males. Males in both these coalitions were genetically closely related, while the two solitary immigrants were not closely related to any of the resident males present in the group they joined.

Birth seasonality and offspring production in threatened neotropical primates related to climate

AbstractGiven the threatened status of many primate species, the impacts of global warming on primate reproduction and, consequently, population growth should be of concern. We examined relations between climatic variability and birth seasonality, offspring production, and infant sex ratios in two ateline primates, northern muriquis, and woolly monkeys. In both species, the annual birth season was delayed by dry conditions and El Niño years, and delayed birth seasons were linked to lower birth rates. Additionally, increased mean annual temperatures were associated with lower birth rates for northern muriquis. Offspring sex ratios varied with climatic conditions in both species, but in different ways: directly in woolly monkeys and indirectly in northern muriquis. Woolly monkeys displayed an increase in the proportion of males among offspring in association with El Niño events, whereas in northern muriquis, increases in the proportion of males among offspring were associated with delayed onset of the birth season, which itself was related, although weakly, to warm, dry conditions. These results illustrate that global warming, increased drought frequency, and changes in the frequency of El Niño events could limit primate reproductive output, threatening the persistence and recovery of ateline primate populations.

Activity Patterns of Brachyteles arachnoides in the Largest Remaining Fragment of Brazilian Atlantic Forest

Time is an important currency for primate energetics, reproduction, and survival. Here, we describe the activity budgets of a group of southern muriquis (Brachyteles arachnoides) inhabiting the largest continuous fragment of Brazilian Atlantic Forest (210,000 ha) in Parque Estadual Carlos Botelho (24°44´–15´S, 47´46–10 W), in the southern region of Sao Paulo State. We collected instantaneous scan sampling data to assess monthly, seasonal, and between-year differences in time allocation for the different activities for 2 complete, nonconsecutive years—1995 and 2002—and compare these with measures of food availability. Over the 2 yr, the group rested on average for 48%, fed for 28%, traveled for 22.5%, and socialized for 1.5% of daylight hours. On a monthly basis, resting correlated negatively with traveling in 1995, and strongly negatively correlated with feeding for both years. Feeding correlated negatively with traveling in 2002, with significantly more time spent traveling during periods of higher young leaf availability. Season was a major influence on activity: the group rested more during the hotter, rainy austral summer season, whereas feeding occurred more frequently in the cooler, drier winter season. We found no consistent associations between food availability and the time that southern muriquis spent in most activities. We suggest that these southern muriquis, like many other large-bodied and atelin primates, minimize energy expenditure while maximizing energy intake, which may be associated with their ability to be folivorous when their preferred fruit foods are less available. They thus adopt a flexible energetic strategy for coping with variable climatic conditions rather than being constrained by food availability.

Tropical warming and the dynamics of endangered primates

Many primate species are severely threatened, but little is known about the effects of global warming and the associated intensification of El Niño events on primate populations. Here, we document the influences of the El Niño southern oscillation (ENSO) and hemispheric climatic variability on the population dynamics of four genera of ateline (neotropical, large-bodied) primates. All ateline genera experienced either an immediate or a lagged negative effect of El Niño events. ENSO events were also found to influence primate resource levels through neotropical arboreal phenology. Furthermore, frugivorous primates showed a high degree of interspecific population synchrony over large scales across Central and South America attributable to the recent trends in large-scale climate. These results highlight the role of large-scale climatic variation and trends in ateline primate population dynamics, and emphasize that global warming could pose additional threats to the persistence of multiple species of endangered primates.

The evolution of brachiation in ateline primates, ancestral character states and history

This study examines how brachiation locomotion evolved in ateline primates using recently-developed molecular phylogenies and character reconstruction algorithms, and a newly-collected dataset including the fossils Protopithecus, Caipora, and Cebupithecia. Fossils are added to two platyrrhine molecular phylogenies to create several phylogenetic scenarios. A generalized least squares algorithm reconstructs ateline and atelin ancestral character states for 17 characters that differentiate between ateline brachiators and nonbrachiators. Histories of these characters are mapped out on these phylogenies, producing two scenarios of ateline brachiation evolution that have four commonalities: First, many characters change towards the Ateles condition on the ateline stem lineage before Alouatta splits off from the atelins, suggesting that an ateline energy-maximizing strategy began before the atelines diversified. Second, the ateline last common ancestor is always reconstructed as an agile quadruped, usually with suspensory abilities. It is never exactly like Alouatta and many characters reverse and change towards the Alouatta condition after Alouatta separates from the atelins. Third, most characters undergo homoplastic change in all ateline lineages, especially on the Ateles and Brachyteles terminal branches. Fourth, ateline character evolution probably went through a hindlimb suspension with tail-bracing phase. The atelines most likely diversified via a quick adaptive radiation, with bursts of punctuated change occurring in their postcranial skeletons, due to changing climatic conditions, which may have caused competition among the atelines and between atelines and pitheciines.

Glenohumeral joint surface characters and its relation to forelimb suspensory behavior in three ateline primates, Ateles, Lagothrix, and Alouatta

Intergeneric morphological variation of the glenohumeral joint surface was investigated among three ateline genera (Ateles, Lagothrix, Alouatta) and compared with Cebus (an ancestral morphotype of atelines) and Hylobates (a specialized brachiator) to reveal characters associated with forelimb suspensory behavior. Seventy-six skeletal specimens were examined, and articular surface curvature was measured by a three-dimensional digitizer. It was found that Ateles exhibits joint features distinct from the other atelines, but resembles Hylobates in its large breadth–length ratio of the glenoid surface and the humeral head, a relatively spherical humeral head, and a dorsoventrally extensive humeral head relative to the glenoid surface. These morphologies are likely to be related to brachiation, rather than to climbing behavior. A dorsoventrally extensive glenohumeral joint is interpreted to facilitate an increased stride length during brachiation. Lagothrix was found to show many primitive features that are shared with Alouatta in spite of its forelimb suspensory behavior. This may be related to the less specialized mode of forelimb suspensory behavior in Lagothrix compared with Ateles. Those characters that apparently correspond to dependency on suspensory behavior can be useful in interpreting the positional behavior of extinct primate taxa.

Contemporary Issues in Ecology, Behavior and Evolution of the Atelin Primates

In the early 1990s, when we were graduate students beginning our respective dissertation projects on atelin primates, the number of studies available to us for background information was limited. Long-term field research on the genera discussed in this issue was restricted to a few sites scattered around Central and South America and it was being carried out by an equally limited number of scientists. If one were interested in spider monkeys (Ateles spp.), Cant, Chapman, Klein, Symington, and van Roosmalen were among the few researchers who had each authored multiple publications on the ecology and behavior of the genus. Even fewer had contributed to the literature on woolly monkeys (Lagothrix spp.)— most notably Defler, Nishimura, Peres, and Soini—while Milton and Strier were the only scientists associated with multiple publications on muriquis (Brachyteles spp.). We are very pleased that in the intervening decade, the number of long-term studies conducted on atelin primates has grown dramatically as a diverse international group of new researchers and established veterans have made substantial contributions to our understanding of

Frugivory and Seed Fate in Bursera inversa (Burseraceae) at Tinigua Park, Colombia: Implications for Primate Conservation1

ABSTRACTThe large ateline primates are efficient seed dispersers in Neotropical forests and hunting is driving their populations to extinction, but we do not know whether other frugivores could substitute primates in their ecological role as seed dispersers. In this study we test this possibility using a potential keystone species (Bursera inversa) at Tinigua Park, Colombia. This plant species allows us to compare seed removal rates between emergent, isolated trees, without primate visitors and trees with connected crowns. We used traps to estimate fruit production and seed removal rates in six different trees, and fruiting trees were observed during 2 yr to quantify the number of seeds manipulated by different animal species. We carried out seed predation experiments to test if seed removal by predators was affected by distance or density effects. We found that the most productive trees attracted more visiting species and seed removal rates differed among trees, the lowest corresponding to trees without primate access. Seed removal rates from the ground by predators were not higher below parental trees than away from them, but the distribution of saplings in the forest suggests that seed dispersal is advantageous. Although it is likely that the effect of primate extinctions will vary depending on tree species traits, conserving the populations of primate seed dispersers is critical to maintain the ecological processes in this forest.

Eat or be eaten: predator sensitive foraging among primates

Preface 1. An introduction to predator sensitive foraging Lynne E. Miller Part I. Biological Variables: 2. Dangers in the dark: are some nocturnal primates afraid of the dark? Simon K. Bearder, K. A. I. Nekaris and Courtney A. Buzzell 3. Predation sensitive foraging in captive tamarins Mark J. Prescott and Hannah M. Buchanan-Smith 4. Seeing red: consequence of individual differences in color vision in callitrichid primates Nancy G. Caine 5. Predator sensitive foraging in Thomas langurs Elisabeth H. M. Sterck Part II. Social Variables: 6. The role of group size in predator sensitive foraging decisions for wedge-capped capuchin monkeys (Cebus olivaceous) Lynne E. Miller 7. Group size effects on predation sensitive foraging in wild ring-tailed lemurs (Lemur catta) Michelle L. Sauther 8. Species differences in feeding in Milne Edward's sifakas (Propithecus diadema edwardsi), rufus lemurs (Eulemur fulvus rufus) and red-bellied lemurs (Eulemur rubriventer) in southeastern Madagascar: implications for predator avoidance Deborah J. Overdorff, Suzanne G. Strait and Ryan G. Seltzer 9. Evidence of predator sensitive foraging and traveling in single- and mixed-species tamarin troops Paul A. Garber and Julio Cesar Bicca-Marques 10. Predator (in)sensitive foraging in sympatric female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas): a test of ecological models of group dispersion Lynne A. Isbell and Karen L. Enstam 11. Predation risk and anti-predator adaptions in white-faced sakis (Pithecia pithecia) Terrence M. Gleason and Marilyn A. Norconk Part III. Environmental Variables: 12. Foraging female baboons exhibit similar patterns of antipredator vigilance across two populations Russell A. Hill and Guy Cowishaw 13. Foraging and safety in adult female blue monkeys in the Kakamega Forest, Kenya Marina Cords 14. Predicting predation risk for foraging arboreal monkeys Adrian Treves 15. Predator sensitive foraging in ateline primates Anthony Di Fiore 16. Anti-predatory behaviour in gibbons (Hylobates lar, Yai/Thailand) Nicola L. Uhde and Volker Sommer.

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.

Time Allocation Patterns of Lowland Woolly Monkeys (Lagothrix lagotricha poeppigii) in a Neotropical Terra Firma Forest

We investigated the time allocation decisions of lowland woolly monkeys (Lagothrix lagotricha poeppigii )i n aterra firma forest in eastern Ecuador where they occur sympatrically with 9 other primate species. Woolly monkeys spent considerable amounts of time searching for and attempting to procure animal prey—roughly as much time as they spent consuming plant material: ripe fruits, leaves, and flowers. The amount of time spent foraging for animal prey is positively related to the habitat-wide availability of ripe fruits (the predominant component of the woolly monkey diet), and negatively related to both ambient temperature and the abundance of potential prey items in the habitat. Time spent resting showed exactly the opposite pattern with respect to these ecological variables. These results suggest that woolly monkeys follow an energy-maximizing strategy of food acquisition during times of fruit abundance—focusing on animal foods and perhaps laying down fat reserves to utilize when ecological conditions worsen—and follow an energy-minimizing strategy when fruit resources are scarce. Such a strong and seasonal commitment to animal prey foraging is unique among the ateline primates and is not ubiquitous even among lowland woolly monkeys. We suggest that this foraging strategy, and the greater intragroup cohesion that characterizes some populations of Lagothrix, are both opportunistic responses to regional differences in habitat quality. Identifying and accounting

Brotherhoods Among Atelins: Kinship, Affiliation, and Competition

AbstractThis paper examines differences in male affiliative associations and dominance relationships in atelin primates. Despite the occurrence of male philopatry in all three genera, male social relations varied considerably. The strength of male affiliations was attributed to differences in between group competition for access to groups of females, while the type of male dominance relationships was attributed to differences in within group competition for access to individual females. Female grouping patterns and the socionomic sex ratio appeared to be more important than group size in predicting the strength of between group competition and male affiliations. Male dominance over females appeared to be more important than estrus synchrony in predicting the type of within group competition and the presence of hierarchical or egalitarian relationships among males.

Adaptive radiation of the ateline primates

We propose a synthesis of anatomical, behavioral and ecological data in reconstructing the phylogeny and evolution of the ateline primates. The atelines are a monophyletic group divisible into an alouattin lineage, including Alouatta and the Miocene fossil Stirtonia, and an atelin lineage, including Lagothrix and its sister-group, the Ateles-Brachyteles clade. Body size increase was important in the origins of atelines and in their subsequent diversification. Larger body size perimitted an increased reliance on leaves (probably immature) by comparison with other platyrrhines, even in predominantly frugivorous forms. A novel locomotor pattern involving climbing, some forelimb climbing/hauling and hanging by the prehensile tail, which involved the evolution of many features derived for platyrrhines, was present in the first atelines, perhaps also connected with relatively large body size. The last common ancestor (LCA) of atelines, which morphologically resembled Lagothrix more than any other living form, probably lived in fluid multi-male polygynous groups characterized by female dispersal and had a moderate degree of sexual dimorphism. Alouattins became strongly committed to an energy minimizing adaptive strategy based upon a bulky, nutritionally poor diet composed mainly of leaves. Alouatta thus travels relatively little daily, uses a non-acrobatic style of deliberate quadrupedalism, defends resources inexpensively by long distance calling, lives in cohesive polygynous groups that influenced the development of high sexual dimorphism, and has a proportionately small brain size. These are derived characteristics which facilitate their exploitation of a wide variety of habitats, frequently in sympatry with atelins. Ancestral atelins were probably larger than the LCA. They engaged in more forelimb-dominated climbing and probably ranged widely in fluid, polygynous social groups. The least known modern form, Lagothrix, may occupy a hard-fruit feeding niche, in contrast to the soft-fruit specialist Ateles. A lithe, brachiating body plan that resembles hylobatids typifies Ateles and Brachyteles, suggesting a common ancestral foraging strategy involving rapid bursts of energy expenditure. The subsequent evolution of shearing postcanines in Brachyteles, which converges on Alouatta superficially, is interpretated as a derived adaptive compromise possibly related to the greater seasonality of the Atlantic Coastal Forest of southeastern Brazil, where the genus probably arose, in comparison to inland tropical forests. Energy saving features of Brachyteles include contracted home ranges and low intra-group aggression.