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.

Vertically stratified interactions of nectarivores and nectar-inhabiting bacteria in a liana flowering across forest strata.

PREMISE: Vertical stratification is a key feature of tropical forests and plant-frugivore interactions. However, it is unclear whether equally strong patterns of vertical stratification exist for plant-nectarivore interactions and, if so, which factors drive these patterns. Further, nectar-inhabiting bacteria, acting as "hidden players" in plant-nectarivore interactions, might be vertically stratified, either in response to differences among strata in microenvironmental conditions or to the nectarivore community serving as vectors. METHODS: We observed visitations by a diverse nectarivore community to the liana Marcgravia longifolia in a Peruvian rainforest and characterized diversity and community composition of nectar-inhabiting bacteria. Unlike most other plants, M. longifolia produces inflorescences across forest strata, enabling us to study effects of vertical stratification on plant-nectarivore interactions without confounding effects of plant species and stratum. RESULTS: A significantly higher number of visits were by nectarivorous bats and hummingbirds in the midstory than in the understory and canopy, and the visits were strongly correlated to flower availability and nectar quantity and quality. Trochiline hummingbirds foraged across all strata, whereas hermits remained in the lower strata. The Shannon diversity index for nectar-inhabiting bacterial communities was highest in the midstory. CONCLUSIONS: Our findings suggest that vertical niche differentiation in plant-nectarivore interactions seems to be partly driven by resource abundance, but other factors such as species-specific preferences of hummingbirds, likely caused by competition, play an important role. We conclude that vertical stratification is an important driver of a species' interaction niche highlighting its role for promoting biodiversity and ecosystem functioning.

A comparison of scan and focal sampling in estimating activity budgets, diet composition, and proximity patterns of a wild pair-living primate.

The choice of behavioral sampling method can impact the outcome of data collection, however, few direct comparisons between methods have been made. We compared the performance of instantaneous group scan sampling (scan sampling) and focal continuous sampling with variable session durations (focal sampling) in estimating activity patterns, diet composition, and spatial proximity in seven groups of wild coppery titi monkeys (Plecturocebus cupreus) in Peruvian Amazonia. We used a series of paired samples Wilcoxon tests to compare daily proportions of time allocated to each type of activity/food/proximity category in each sampling method. In addition, we compared our results with those of other studies conducted on the same population of titi monkeys at other times. Focal sampling provided significantly lower estimates for moving time and significantly higher estimates for resting time compared to scan sampling, likely because scan sampling tends to give higher estimates of more conspicuous behaviors and lower estimates of less conspicuous behaviors. For diet composition, scan sampling gave similar results to other studies, while focal sampling gave significantly lower estimates for feeding on fruits and higher estimates for feeding on arthropods. The most likely reason is that focal sampling with variable session durations tends to overestimate behaviors during which a focal animal is less likely to go out of view, such as feeding on arthropods in the lower strata of the forest. Our results suggest that a pilot study comparing different methods should be conducted prior to collecting data, as not all methods are interchangeable.

Corrigendum: A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

[This corrects the article DOI: 10.1093/biosci/biaa082.].

A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.

Effects of zoochory on the spatial genetic structure of plant populations.

Spatial genetic structure (SGS) of plants results from the nonrandom distribution of related individuals. SGS provides information on gene flow and spatial patterns of genetic diversity within populations. Seed dispersal creates the spatial template for plant distribution. Thus, in zoochorous plants, dispersal mode and disperser behaviour might have a strong impact on SGS. However, many studies only report the taxonomic group of seed dispersers, without further details. The recent increase in studies on SGS provides the opportunity to review findings and test for the influence of dispersal mode, taxonomic affiliation of dispersers and their behaviour. We compared the proportions of studies with SGS among groups and tested for differences in strength of SGS using Sp statistics. The presence of SGS differed among taxonomic groups, with reduced presence in plants dispersed by birds. Strength of SGS was instead significantly influenced by the behaviour of seed dispersal vectors, with higher SGS in plant species dispersed by animals with behavioural traits that result in short seed dispersal distances. We observed high variance in the strength of SGS in plants dispersed by animals that actively or passively accumulate seeds. Additionally, we found SGS was also affected by pollination and marker type used. Our study highlights the importance of vector behaviour on SGS even in the presence of variance created by other factors. Thus, more detailed information on the behaviour of seed dispersers would contribute to better understand which factors shape the spatial scale of gene flow in animal-dispersed plant species.

Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari (Cacajao calvus).

Colour vision is highly variable in New World monkeys (NWMs). Evidence for the adaptive basis of colour vision in this group has largely centred on environmental features such as foraging benefits for differently coloured foods or predator detection, whereas selection on colour vision for sociosexual communication is an alternative hypothesis that has received little attention. The colour vision of uakaris (Cacajao) is of particular interest because these monkeys have the most dramatic red facial skin of any primate, as well as a unique fission/fusion social system and a specialist diet of seeds. Here, we investigate colour vision in a wild population of the bald uakari,C. calvus, by genotyping the X-linked opsin locus. We document the presence of a polymorphic colour vision system with an unprecedented number of functional alleles (six), including a novel allele with a predicted maximum spectral sensitivity of 555 nm. This supports the presence of strong balancing selection on different alleles at this locus. We consider different hypotheses to explain this selection. One possibility is that trichromacy functions in sexual selection, enabling females to choose high-quality males on the basis of red facial coloration. In support of this, there is some evidence that health affects facial coloration in uakaris, as well as a high prevalence of blood-borne parasitism in wild uakari populations. Alternatively, the low proportion of heterozygous female trichromats in the population may indicate selection on different dichromatic phenotypes, which might be related to cryptic food coloration. We have uncovered unexpected diversity in the last major lineage of NWMs to be assayed for colour vision, which will provide an interesting system to dissect adaptation of polymorphic trichromacy.

Fruit Odor as A Ripeness Signal for Seed-Dispersing Primates? A Case Study on Four Neotropical Plant Species.

Fleshy fruits contain a myriad of secondary metabolites that may fulfill various non-mutually exclusive ecological functions. Among them are defense against pathogens and herbivores, manipulation of frugivores' gut retention time, or controlling the germination process. In addition, it has been suggested that aroma compounds may be used as fruit-selection cues by frugivores, and that plants may be under selection to provide a reliable signal for ripeness to seed-dispersal vectors through ripe fruit aroma. A previous project demonstrated that fruit odor of two Neotropical primate-dispersed plant species can be used by primates to identify ripe fruits. Here, we provide data supporting the hypothesis that olfactory conspicuousness of ripeness in these two species may be an evolved signal rather than a cue exploited by primates. We analyzed the odors of ripe and unripe fruits of the two species along with odors of two sympatric species whose main dispersal vector is passerine birds. We show that only primate-dispersed species significantly change their odor profiles upon ripening. Thus, odor of bird-dispersed species is not informative regarding their ripeness level and is likely to fulfill other functions. We discuss these data in light of the multiple hypotheses for the presence of fruit secondary metabolites, and we offer a roadmap for future studies to establish the hypothesis that fruit odor is an evolved signal for ripeness.

Led by the nose: Olfaction in primate feeding ecology.

Olfaction, the sense of smell, was a latecomer to the systematic investigation of primate sensory ecology after long years in which it was considered to be of minor importance. This view shifted with the growing understanding of its role in social behavior and the accumulation of physiological studies demonstrating that the olfactory abilities of some primates are on a par with those of olfactory-dependent mammals such as dogs and rodents. Recent years have seen a proliferation of physiological, behavioral, anatomical, and genetic investigations of primate olfaction. These investigations have begun to shed light on the importance of olfaction in the process of food acquisition. However, integration of these works has been limited. It is therefore still difficult to pinpoint large-scale evolutionary scenarios, namely the functions that the sense of smell fulfills in primates' feeding ecology and the ecological niches that favor heavier reliance on olfaction. Here, we review available behavioral and physiological studies of primates in the field or captivity and try to elucidate how and when the sense of smell can help them acquire food.

Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment.

Numerous animal species currently experience habitat loss and fragmentation. This might result in behavioral and dietary adjustments, especially because fruit availability is frequently reduced in fragments. Food scarcity can result in elevated physiological stress levels, and chronic stress often has detrimental effects on individuals. Some animal species exhibit a high degree of fission-fusion dynamics, and theory predicts that these species reduce intragroup feeding competition by modifying their subgroup size according to resource availability. Until now, however, there have been few studies on how species with such fission-fission dynamics adjust their grouping patterns and social behavior in small fragments or on how food availability influences their stress levels. We collected data on fruit availability, feeding behavior, stress hormone levels (measured through fecal glucocorticoid metabolites (FGCM)), subgroup size, and aggression for two groups of brown spider monkeys (Ateles hybridus) in a small forest fragment in Colombia and examined whether fruit availability influences these variables. Contrary to our predictions, spider monkeys ranged in smaller subgroups, had higher FGCM levels and higher aggression rates when fruit availability was high compared to when it was low. The atypical grouping pattern of the study groups seems to be less effective at mitigating contest competition over food resources than more typical fission-fusion patterns. Overall, our findings illustrate that the relationship between resource availability, grouping patterns, aggression rates, and stress levels can be more complex than assumed thus far. Additional studies are needed to investigate the long-term consequences on the health and persistence of spider monkeys in fragmented habitats.

Validation of an enzyme immunoassay for assessing adrenocortical activity and evaluation of factors that affect levels of fecal glucocorticoid metabolites in two New World primates.

Non-invasive methods to assess stress hormone output via fecal glucocorticoid metabolites (FGCMs) have become a powerful tool in behavioral studies and conservation biology because they allow exploring the link between behavior, an animal's socio-ecological environment and its adrenocortical activity. However, FGCM levels are influenced by numerous other factors which often confound their interpretation. Thus, before applying these methods, knowledge on the impact of these factors is important. In this study we investigated the effect of (1) time of day, (2) age, (3) sex and (4) female reproductive state on FGCM levels in brown spider monkeys (Ateles hybridus) and red howler monkeys (Alouatta seniculus). Initially, we validated a 11ß-hydroxyetiocholanolone enzyme immunoassay for monitoring the physiological stress response via fecal analysis in both species. We determined FGCM levels in fecal samples collected from two and six groups of wild spider monkeys (n=461 samples) and howler monkeys (n=166 samples), respectively. Our analyses revealed a strong effect of time of day on FGCM levels in spider monkeys, but no effect in howler monkeys. Adults of both species had significantly higher FGCM levels than subadults. In neither of the two species we found a sex-effect on FGCM output. Reproductive condition strongly affected FGCM levels in female spider monkeys which showed increasing concentrations with progressing gestation. This was not investigated in female howler monkeys due to an insufficient sample size. Our data indicate that the influence of the tested factors on fecal glucocorticoid metabolite output is species-specific, and that these variables need to be considered when interpreting FGCM levels in the species.

Distribution and abundance of white-fronted spider monkeys, Ateles belzebuth (Atelidae), and threats to their survival in Peruvian Amazonia.

The white-fronted spider monkey, Ateles belzebuth, is listed as 'Endangered' according to the IUCN classification. In Peru it is found in the departments of Loreto, San Martín, Amazonas and Cajamarca, but detailed data on its geographic distribution, population densities and conservation status are scarce. In order to obtain such information, we conducted transect censuses on the Río Aushiri and Río San Antonio (right bank of Río Napo), and between the Río Curaray and the Río Arabela and Río Nashiño, respectively, and made additional explorations on the northern and southern banks of the Río Marañón. We obtained 48 sightings along 761 km of census transect. Group size and population densities were lower in an area with high hunting pressure compared to areas with medium or low hunting pressure. Besides hunting, increasing deforestation is a major threat to the survival of A. belzebuth in Peruvian Amazonia.

Feeding ecology of monk sakis (Pithecia monachus) in a seasonally flooded forest in western Amazonia.

Sakis (genus Pithecia) are frugivorous primates with a preference for seeds that complete their diet with leaves and insects. Fruit pulp and seeds are known to have different nutritional characteristics that change during the process of ripening. The consumption of seeds can be an adaptation to changes in resource availability, as unripe seeds are a more steadily available resource than ripe pulp or young leaves. Here, we present the first study of the feeding ecology of monk sakis (Pithecia monachus). We investigated dietary composition and identified important feeding plants in a seasonally flooded forest within the Área de Conservación Regional Comunal Tamshiyacu-Tahuayo in Peruvian Amazonia. Throughout 20 months, we followed groups of monk sakis by foot and canoe and recorded 459 feeding events. Seeds were the most frequently consumed food item (49%), followed by pulp (mesocarp, pericarp or aril; 25%) and arthropods (22%). Leaves, bark, and flowers were ingested only sporadically. The importance of ripe seeds and arthropods in the diet of the monk sakis differed from other studies: we recorded the consumption of mostly ripe seeds and the share of arthropods was relatively high.

Brief communication: a preliminary study on the influence of physical fruit traits on fruit handling and seed fate by white-handed Titi monkeys (Callicebus lugens).

Callicebus and the pitheciins are closely related; however, differences in their diets and dental morphology suggest that they differ in the use of mechanically protected food. We describe physical traits of fruits consumed by white-handed titi monkeys (Callicebus lugens) and determine their influence on fruit part selection and immediate seed fate after fruit handling. We tested two hypotheses about the effects of mechanical fruit traits on fruit part selection and seed fate: (1) fruits selected for seed consumption are harder than fruits selected for their fleshy parts and (2) consumed seeds are softer than seeds with other fates. In addition, we analyzed the influence of other physical fruit traits on fruit part selection and seed fate. C. lugens included 69 species in its diet, from which it mainly consumed their fleshy parts. It also consumed seeds, alone or with fleshy fruit parts, but most of them ended up close to parent trees after being dropped or spat out. The first hypothesis was supported while the second was rejected, indicating that C. lugens tends to rely on hard fruits for obtaining seeds, while seed hardness had no influence on fruit part selection and seed fate, contrasting with the pattern reported for Pithecia and Chiropotes in other studies. Ripeness was the most influential factor for fruit part and seed fate discrimination. Results suggest a tendency to sclerocarpic foraging in C. lugens when feeding on seeds.

On the identity of the tamarin AMNH 98303 ("Saguinus fuscicollis tripartitus"; Primates: Haplorrhini: Simiiformes: Platyrrhini: Callitrichidae).

The American Museum of Natural History houses the skin of a tamarin (AMNH 98303) labelled as Saguinus fuscicollis tripartitus. However, the specimen does not match the phenotype of this taxon, now named Leontocebus tripartitus, nor that of any other known species or subspecies of Leontocebus. In this note, we review past taxonomic revisions of the genus Saguinus - revisions that were largely driven by the contentious species or subspecies status of the golden-mantled saddleback tamarin S. fuscicollis tripartitus - and compare the phenotype of AMNH 98303 with those of other tamarins in the same genus to discuss the possible status of this specimen.

Fur rubbing in Plecturocebus cupreus - an incidence of self-medication?

Fur rubbing, i.e. rubbing a substance or an object into the pelage, has been described in numerous Neotropical primate species, including species of titi monkeys, but it seems to be a rare behaviour. Here we describe a fur rubbing event in a wild coppery titi monkey (Plecturocebus cupreus) with Psychotria sp. (Rubiaceae) leaves observed and videotaped during a field study on vigilance behaviour between September-December 2019 in the Peruvian Amazon. Plants of the genus Psychotria contain a great diversity of secondary metabolites and are often used in traditional medicine. We suggest that the fur rubbing was an act of self-medication. This is the first record of fur rubbing in coppery titi monkeys in almost 4400 h of observation accumulated over more than 20 years.

Southern range extension of Spix's saddle-back tamarin, Leontocebus fuscicollis fuscicollis, in Peru.

Peru has the highest diversity of members of the tamarin genus Leontocebus (Callitrichidae). However, for a number of taxa from this genus the distributional ranges are still not well known. In this paper we provide evidence for the extension of the southern range of Leontocebus fuscicollis fuscicollis to the right bank of the Río Abujao, south of which it is replaced by Leontocebus weddelli weddelli.

Non-random host tree infestation by the Neotropical liana Marcgravia longifolia.

The question whether or not tropical lianas infest host trees randomly or they exert host selection has implications for the structure and dynamics of tropical rainforests, particularly if colonization by lianas impacts host fitness. In this study, we present evidence that the Neotropical liana Marcgravia longifolia (Marcgraviaceae) infests host trees non-randomly. We identified host trees to species or genus level for 87 of the 100 M. longifolia individuals found in the study area of the Estación Biológica Quebrada Blanco (EBQB) in north-eastern Peruvian Amazonia. Data on host availability were taken from two 1-ha plots sampled at EBQB as part of a large-scale tree inventory in western Amazonia. Of the total of 88 tree genera with two or more individuals present in the inventory, 18 were represented amongst hosts. Host genera with a probability of colonization higher than expected by chance were Eschweilera (Lecythidaceae), Pouteria (Sapotaceae), Brosimum (Moraceae), and Hymenaea (Fabaceae). These findings suggest that M. longifolia exerts some level of host selectivity, but the mechanisms for this are completely unknown. Given the large number of animal species (41 bird species, three primate species) that are dispersing the seeds of M. longifolia and that have diverse ecological strategies, directed seed dispersal is unlikely to account for the observed patterns of host infestation.

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.