Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Eat the fruit earlier: Sakis (Pithecia chrysocephala) show enhanced temporal fruit resource access compared with squirrel monkeys (Saimiri sciureus) in an urban forest fragment in Brazil.

Fruit availability experienced by different primate species is likely to vary due to species-specific fruit use, even within the same habitat and timeframe. Pitheciines, primates of the subfamily Pitheciinae, particularly favor the seeds of unripe fruits. Researchers consider this dietary characteristic an adaptation to increase access to fruit resources. However, the relative advantages of pitheciines over sympatric non-pitheciine non-seed-eating primates regarding species-specific fruit availability is not well studied. In a 26-ha forest within the city of Manaus, Amazonian Brazil, we assessed the wild-food feeding behavior of free-ranging groups of golden-faced sakis (Pithecia chrysocephala) and sympatric common squirrel monkeys (Saimiri sciureus). We hypothesized that sakis would have greater and more consistent access to wild fruit due to (1) a wider variety of fruit species in their diet, and (2) longer consumption periods per fruit species. We recorded the plant species, part (pulp or seed), and developmental stage (ripe or unripe) of wild fruit consumed by both species. We also conducted monthly fruit censuses of 1000 trees and vines to estimate overall wild fruit abundance. As an indicator of fruit availability, we calculated the proportion of available fruiting trees and vines for each primate species separately based on their observed diet. Throughout the year, the proportion of available trees and vines was significantly higher and more temporally stable for sakis than for squirrel monkeys. This was because sakis used shared fruit species longer than squirrel monkeys by consuming both ripe and unripe fruit. Although sakis had a broader fruit repertoire than squirrel monkeys, it did not contribute to the higher fruit availability. Thus, the fruit feeding system of sakis identifies aspects of a niche that is less restricted in the timing of fruit consumption, which led to a relative advantage in fruit availability.

Searching for food in a concrete jungle: feeding ecology of a Psittacine assemblage (Aves, Psittacidae) in a major Amazonian city.

The efficient use of food resources is a precondition for wild species´ survival in urban environments. The feeding ecology of animals in tropical cities, however, remains poorly investigated. Here we study the feeding ecology of parrots in Manaus, a major Amazonian city, and compare the results with a parrot assemblage living in undisturbed habitats. We recorded 203 feeding bouts from eight parrot species, which consumed parts of 51 plant species. Parrot diets were dominated by native palm species (Arecaceae). Exotic plants, however, constituted an important portion of the diet of some parrots. Levin's indices, a measure of food niche width, varied from 0.40 to 0.83, indicating an overall tendency to generalist diets. Diet overlap between species was small, indicating broad resource partitioning between members of the assemblage. The diversity of plants consumed in the natural environment was greater than in the urban environment (71 species vs. 52). However, the diversity of plants consumed was similar for parrot species recorded both in natural and urban environments, indicating that occupation of the city does not imply an impoverishment in parrot diets. Creation of municipal protected areas and increasing the city afforestation would provide complementary strategies for Manaus parrot conservation.

Biotic Indicators for Ecological State Change in Amazonian Floodplains.

Riverine floodplains are biologically diverse and productive ecosystems. Although tropical floodplains remain relatively conserved and ecologically functional compared to those at higher latitudes, they face accelerated hydropower development, climate change, and deforestation. Alterations to the flood pulse could act synergistically with other drivers of change to promote profound ecological state change at a large spatial scale. State change occurs when an ecosystem reaches a critical threshold or tipping point, which leads to an alternative qualitative state for the ecosystem. Visualizing an alternative state for Amazonian floodplains is not straightforward. Yet, it is critical to recognize that changes to the flood pulse could push tropical floodplain ecosystems over a tipping point with cascading adverse effects on biodiversity and ecosystem services. We characterize the Amazonian flood pulse regime, summarize evidence of flood pulse change, assess potential ecological repercussions, and provide a monitoring framework for tracking flood pulse change and detecting biotic responses.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Foraging with finesse: A hard-fruit-eating primate selects the weakest areas as bite sites.

OBJECTIVES: Fruit husks are rarely uniformly hard, varying in penetrability via sulci and changes in thickness. We tested whether a hard-food specialist primate i) bites randomly on food fruit husk surfaces to access seeds, or ii) selects areas most easily penetrated by canines. We consider this would occur so as to minimize deployed mechanical force, energetic expenditure and risk of dental breakage when feeding. METHODS: A sulcus is the natural line of weakness where a dehiscent fruit breaks open. Using fruits dentally opened for seeds by golden-back uacaris (Cacajao ouakary) we: 1) analysed bite mark distribution on surface of four fruits types (hard-with-sulcus, soft-with-sulcus, hard-no-sulcus, soft-no-sulcus); 2) quantified the force needed to penetrate hard and soft fruits at sulci and elsewhere on fruit surface; 3) measured fruit wall thickness and correlated it with bite-mark distribution in all four categories of fruit. RESULTS: 1) Bite marks were distributed at random only on surfaces of soft fruits. For other fruits types, bite locations were concentrated at the thinnest areas of husk, either over the entire surface (non-sulcate fruits), or at sulci (sulcate fruits). 2) For hard-husked fruits, areas where uacaris concentrated their bites were significantly easier to penetrate than those where they did not. CONCLUSIONS: This hard-fruit feeding specialist primate is not biting at random on the surface of diet fruits. To access seeds they are focusing on those areas requiring less force to penetrate. This may be to save energy, to minimize the risk of breaking teeth used in food processing, or a combination of both. The study shows, for the first time, the subtlety by which these powerfully-jawed animals process their diet items.

Pitheciid research comes of age: Past puzzles, current progress, and future priorities.

For a long time, members of the Pitheciidae were among the least studied of all Neotropical primates. But times have changed. Here, we trace the trajectory of this change and show how the articles in this special edition illustrate new knowledge and developments in our understanding of pitheciid ecology, behavior, and conservation. We propose new directions and priorities for future research, especially to ensure the effective conservation of pitheciids, and demonstrate how studies of this family are now the focus of hypothesis-driven research that not only allows the details of this family's biology to be explored, but will allow its biology to be compared with other primate lineages.

Mixed-species associations in cuxiús (genus Chiropotes).

Polyspecific or mixed-species associations, where two or more species come together to forage and travel as a unit, have been reported in many primate species. These associations appear to offer a number of benefits to the species involved including increased foraging efficiency and decreased risk of predation. While several researchers have suggested that cuxiús (genus Chiropotes) form mixed-species associations, previous studies have not identified the circumstances under which cuxiús form associations or whether they form associations more often than would be expected by chance. Here we present data on the formation of mixed-species associations by four species of cuxiús at eight different sites in Brazil, Suriname, and Guyana. We analyzed data from two of the study sites, (Biological Dynamics of Forest Fragments Project (BDFFP), Brazil and the Upper Essequibo Conservation Concession (UECC), Guyana, to assess whether associations occurred more than would be expected by chance encounters and identify the factors influencing their formation. Cuxiús showed a high degree of inter-site variation in the frequency of time spent in association (ranging from 2 to 26% of observation time) and duration of associations (mean duration from 22 min to 2.5 hr). Sapajus apella was the most common association partner at most sites. At BDFFP, cuxiús formed associations more frequently but not for longer duration than expected by chance. For much of the year at UECC, associations were not more frequent or longer than chance. However, during the dry season, cuxiús formed associations with S. apella significantly more often and for longer duration than predicted by chance. Cuxiús at UECC formed associations significantly more often when in smaller subgroups and when foraging for insects, and alarm called significantly less frequently during associations. We suggest cuxiús form mixed-species associations at some sites as an adaptive strategy to decrease predation risk and/or increase foraging efficiency.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad-scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both.

An Improved Technique Using Dental Prostheses for Field Quantification of the Force Required by Primates for the Dental Penetration of Fruit.

Tooth morphology is an important determinant of primate diet, setting potential limits on processable item size and material properties. Plunger-based commercial fruit firmness testers (penetrometers) have been used to estimate primate diet item hardness and, by proxy, bite force required for penetration. However, geometric forms and surface areas of penetrometer plungers and primate teeth differ considerably. Accurate bite force estimation is especially important with pitheciine primates as these penetrate fruit pericarps with their canines. To achieve more realistic bite force measures, we replaced a fruit penetrometer's standard plunger with a Cacajao calvus canine prosthesis. We compared indentation and penetration values for Hevea spruceana (Euphorbiaceae; hard-pericarp) and Mauritia flexuosa (Arecaceae; soft-pericarp) fruits (both natural Cacajao foods), and standard penetrometer head and canine prosthesis values for penetrating H. spruceana sulci. Compared to the canine prosthesis, a standard head overestimated the force needed to indent and penetrate H. spruceana fruit by more than twofold and, due to greater width, could not effectively penetrate a sulcus: sulcal penetrability data were easily retrieved with the canine prosthesis. We believe this new approach using dental prostheses has potential in the analysis of primate foraging mechanisms, especially for pitheciines for which canines are of paramount importance in accessing food.

Crying tapir: the functionality of errors and accuracy in predator recognition in two neotropical high-canopy primates.

Predation is often considered to be a prime driver in primate evolution, but, as predation is rarely observed in nature, little is known of primate antipredator responses. Time-limited primates should be highly discerning when responding to predators, since time spent in vigilance and avoidance behaviour may supplant other activities. We present data from two independent studies describing and quantifying the frequency, nature and duration of predator-linked behaviours in 2 high-canopy primates, Ateles belzebuth and Cacajao ouakary. We introduce the concept of 'pseudopredators' (harmless species whose appearance is sufficiently similar to that of predators to elicit antipredator responses) and predict that changes in behaviour should increase with risk posed by a perceived predator. We studied primate group encounters with non-primate vertebrates across 14 (Ateles) and 19 (Cacajao) months in 2 undisturbed Amazonian forests. Although preliminary, data on both primates revealed that they distinguished the potential predation capacities of other species, as predicted. They appeared to differentiate predators from non-predators and distinguished when potential predators were not an immediate threat, although they reacted erroneously to pseudopredators, on average in about 20% of the responses given toward other vertebrates. Reacting to pseudopredators would be interesting since, in predation, one error can be fatal to the prey.

Terrestrial activity in pitheciins (Cacajao, Chiropotes, and Pithecia).

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a "local pattern" of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types.

Terrestrial foraging by Cacajao melanocephalus ouakary (primates) in Amazonian Brazil: is choice of seed patch size and position related to predation risk?

We analyse the behaviour of Cacajao melanocephalus ouakary feeding at patches of germinating seedlings in dried-out flooded forest. Seedlings of Eschweilera tenuifolia (Lecythidaceae) were the most commonly eaten (88.9%). Some seed patches were revisited over several days, while others were consistently ignored. We tested 3 predictions relating uacari terrestrial foraging behaviour to: (1) arboreal escape route proximity, (2) seed patch size choice and (3) temporal patterns of repeat exploitation. Comparison of fed-at and ignored patches revealed significant preferences for larger patches, and for those close to arboreal refuges but distant from dense ground-based vegetation. Support for these predictions is interpreted as evidence for predation risk-sensitive foraging.

For emergency only: terrestrial feeding in Coimbra-Filho's titis reflects seasonal arboreal resource availability.

Terrestriality in Platyrrhine primates is primarily associated with low arboreal resource availability, low predation risk when on the ground and increased contact time with human observers. To test the relationship between these variables and ground use frequency, we studied a group of endangered Coimbra-Filho's titi monkeys (Callicebus coimbrai) in a 14-ha forest fragment in north-eastern Brazil. Terrestriality data were collected on a monthly basis (33 months) using scan sampling procedures from July 2008 to July 2012. Overall, Coimbra-Filho's titi monkeys were recorded during 0.6% of observation time (113 out of 18,164 scans) on the ground. Most of the time on the ground was spent feeding on young leaves (71 records) and the least amount of time on fruits (14 records). Availability of arboreal foods, rainfall, and time of contact with human observers did not influence overall terrestrial behaviour (ground use). However, the timing and nature of the monkeys' terrestrial feeding was strongly related to the absence of arboreal fruit (ß-estimate = -3.078) and young leaf (ß-estimate = -3.515) food resources. We suggest that terrestrial feeding by Coimbra-Filho's titi monkeys could be an adaptation to low arboreal fruit availability and the exploitation of alternative food resources.

New records and modelling the impacts of climate change on the black-tailed marmosets.

Climate change represents an unprecedented threat to global biodiversity and, for many species, gaps in our knowledge of their biology remain acute. Gaps in baseline knowledge, such as confirmed identifications (Linnean shortfalls) and adequate collections (Wallacean shortfalls), need to be minimized with new studies, since this is often critical for effective conservation. Despite the increase in scientific research on primates in the southwest of the Brazilian Amazon, little is known about the species Mico nigriceps (Ferrari & Lopes, 1992) Primates, Platirryni. In the current study, we sought to reduce the extent of the Wallacean shortfall for M. nigriceps, understand whether climate change represents a threat to the distribution of the species, and identify priority areas for its conservation. Accordingly, we provide 121 new records in 14 locations, obtained directly from the field, and five from the literature. Using this, we carried out ecological niche modeling, to better understand how environmental suitability might limit the area occupied by the species. We then projected a distribution for 2070 with the SSP2-4.5 (more optimistic) and SSP5-8.5 (more pessimistic) scenarios. Our data confirmed the geographic distribution of the species as being restricted to headwaters of the Ji-Paraná/Machado river, but with a 400 km extension to the south. Under the modeled climate change scenarios, the area suitable for the species declines by 21% under the most optimistic, and by 27% in the pessimistic, scenario across the projected 50-year period. Although we have expanded the area of known occurrence for this species, we point out that climate change threatens the stability of this newly-discovered population strongly, and that this danger is intensified by deforestation, fire and hunting. We recommend that further studies be carried out to confirm the presence of the species in adjacent areas, those indicated by generated models as being potential environmentally suitable. In addition, we recommend intensifying forest restoration in currently pastured areas, and protection of the areas forming the current and future habitat of this species through such measures as protected area creation.

Differential resilience of Amazonian otters along the Rio Negro in the aftermath of the 20th century international fur trade.

Commercial hunting for the international trade in animal hides in the 20th century decimated many populations of aquatic wildlife in Amazonia. However, impacts varied significantly between different species and regions, depending upon hunting intensity, accessibility of habitat, and the inherent resilience of various species and their habitats. We investigated the differential responses of two Amazonian Mustelid species, the neotropical otter and giant otter, to commercial hunting pressure along the upper Rio Negro in Brazil, and examined historical factors that influenced spatial and temporal variation in commercial exploitation. We analyzed previously unanalyzed data from historical records of hide shipments to track changes in hide sales and prices for the two species in the late 20th century. We also gathered oral histories from older Baniwa people who had witnessed or participated in commercial otter hunting. These complimentary data sources reveal how intrinsic biological and social characteristics of the two otter species interacted with market forces and regional history. Whereas giant otter populations were driven to local or regional extinction during the late 20th century by commercial hunting, neotropical otters persisted. In recent decades, giant otter populations have returned to some parts of the upper Rio Negro, a development which local people welcome as part of a generalized recovery of the ecosystems in their territory as a result of the banning of animal pelt exports and indigenous land demarcation. This paper expands the scope of the field historical ecology and reflects on the role of local knowledge in biodiversity conservation.

Run, hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia.

Although primate predation is rarely observed, a series of primate anti-predation strategies have been described. Energetic costs of such strategies can vary from high-cost mobbing, via less costly alarm calling, to low-cost furtive concealment. Here we report the anti-predation strategies of red-nosed cuxiú, Chiropotes albinasus, based on direct observations from four study sites in southeastern Brazilian Amazonia. Over a collective period of 1255 fieldwork hours, we observed nine direct interactions between raptors (all potential predators) and red-nosed cuxiús. Of these, one (11%) resulted in predation. Raptors involved were: Harpia harpyja (four events), Leucopternis sp. (two events), Spizaëtus tyrannus (one event), and unidentified large raptors (two events). Predation attempts occurred in flooded-forest and terra firme rainforest, were directed at both adult and non-adult cuxiús, and involved both adult and juvenile raptors. Anti-predation strategies adopted by the cuxiús included: (1) group defence and mobbing behaviour (two occasions), (2) dropping into dense sub-canopy (seven occasions), (3) alarm calling (eight occasions), and (4) fleeing to, and hiding in, dense vegetation (eight occasions). During each encounter at least two of these behaviours were recorded. These are the first published records of predation, predation attempts, and anti-predator behaviour involving red-nosed cuxiú.

Reconsidering the taxonomy of the Black-Faced Uacaris, Cacajao melanocephalus group (Mammalia: Pitheciidae), from the northern Amazon Basin.

The black-faced uacaris are a poorly known group of platyrrhine monkeys from the Rio Negro basin in northwestern Amazonia. Originally described as two distinct species-Cacajao melanocephalus (Humboldt 1812) and Cacajao ouakary (Spix 1823)-from opposite banks of the Negro, they were treated as a single species until the end of the twentieth century, when molecular studies reconfirmed their status as true species. One of these studies not only nominated a third (northern) species, Cacajao ayresi Boubli et al. 2008, but also identified C. ouakary as a junior synonym of C. melanocephalus, resulting in the introduction of a new nomen, Cacajao hosomi Boubli et al. 2008. In the present study, additional evidence on morphological and zoogeographic variables is analyzed, which indicates that C. ouakary should be reinstated, and supports the nomination of a neotype of C. melanocephalus. The molecular and zoogeographic data on the species status of the ayresi form are also re-assessed, leading to the conclusion that, on the basis of the evidence available at the present time, this form should be considered a subspecies of C. melanocephalus. A new taxonomic arrangement is proposed, which recognizes two species, C. ouakary and C. melanocephalus, the latter with two subspecies, C. m. melanocephalus and C. m. ayresi.

A randomised, double-blind, placebo-controlled trial of photodynamic therapy using 5-aminolaevulinic acid for the treatment of cervical intraepithelial neoplasia.

Photodynamic therapy (PDT) using topical 5-aminolaevulinic acid (ALA) has been used to treat histologically confirmed cervical intraepithelial neoplasia (CIN-I and -I/II) in a randomised, double-blind, placebo-controlled protocol. Fluorescence microscopy revealed that topical application of 3% ALA in Intrasite Gel to the cervix for 3 hr resulted in the accumulation of protoporphyrin IX in the cervical epithelium. Treatment of CIN with ALA-PDT was well tolerated, with only 3/12 patients in the PDT arm (0/13 in the placebo arm) reporting any discomfort during illumination. Histologic examination of the treated tissue following loop excision 3 months post-PDT indicated that 33% of patients had no evidence of CIN, 42% had no change in the grade of their disease, whilst 25% exhibited an apparent progression of disease. In the control group, the respective figures were 31%, 38% and 31%. There was no significant difference in response between the groups receiving ALA-PDT and those receiving placebo treatment.