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.

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.

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.

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.

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.

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.

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.

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.

Myrmecovory in Neotropical primates.

Ants are the dominant group of animals in many habitats, particularly in tropical rainforests. High abundance and formation of large colonies convert them into a potential food source for a broad spectrum of animals. In this paper we review myrmecovory (consumption of ants) in Neotropical primates. Myrmecovory has been reported from 57 taxa (species + subspecies) out of 217 species of Neotropical primates, representing 18 out of 22 genera. The proportion of ants in the animal portion of the diet is highest amongst members of the genera Cebus, Sapajus, Cheracebus and Plecturocebus, but generally low in callitrichids, large pitheciids (Cacajao, Chiropotes) and atelids. Ants from seven subfamilies of Formicidae (out of 13 subfamilies found in the Neotropics) are consumed, including taxa with and without functional sting and with varying other defences. Foraging technics employed in myrmecovory range from picking ants from open substrates to extractive foraging involving the destruction of ant nests or shelters, but tool use has not been reported. We conclude that myrmecovory is widespread amongst Neotropical primates but on average contributes only a minor proportion of the diet. The diversity of foraging technics employed and lack of tool use in Neotropical primate myrmecovory, even for ants with functional stings and aggressive biting, suggests that tool use for myrmecovory in hominids has not evolved in response to ant defences but is a consequence of enhanced cognitive skills that evolved under other selection pressures.

Estación Biológica Quebrada Blanco: un sitio poco conocido para investigación en biodiversidad y ecología en la Amazonía peruana

La Estación Biológica Quebrada Blanco (EBQB), en el nororiente de la Amazonía peruana, es un lugar donde se ha venido realizando investigación científica desde 1984. En sus inicios la investigación se enfocaba en la ecología y el comportamiento de primates; sin embargo, también se suman trabajos sobre inventarios de algunos grupos de árboles (>10 cm DAP), helechos y aves. El área de la EBQB es muy poco perturbada y está ubicada en una zona de alta biodiversidad. En este trabajo resumimos su historia, la información sobre biodiversidad de que se dispone y mostramos a la EBQB como un lugar con alto potencial para futuros estudios en biodiversidad y ecología en un amplio espectro de organismos.

The Estación Biológica Quebrada Blanco (EBQB) in north-eastern Peruvian Amazonia is a place where research has been conducted since 1984; mainly, on the ecology and behavior of primates, but, later inventories were realized for trees (>10 cm dbh), ferns and birds. The EBQB area is very little disturbed and located in a region of high biodiversity. Here we describe the history of EBQB, summarize the available information on its biodiversity and point out the potential of EBQB for future studies on the biodiversity and ecology of a broad spectrum of organisms.

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

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

Vertical stratification of seed-dispersing vertebrate communities and their interactions with plants in tropical forests.

Vertical stratification (VS) is a widespread phenomenon in plant and animal communities in forests and a key factor for structuring their species richness and biodiversity, particularly in tropical forests. The organisms composing forest communities adjust and shape the complex three-dimensional structure of their environment and inhabit a large variety of niches along the vertical gradient of the forest. Even though the degree of VS varies among different vertebrate groups, patterns of compositional stratification can be observed across taxa. Communities of birds, bats, primates, and non-flying small mammals are vertically stratified in terms of abundance, species richness, diversity, and community composition. Frugivorous members of these taxa play important roles as seed dispersers and forage on fruit resources that, in turn, vary in quantity and nutritional value along the vertical gradient. As a consequence, plant-seed disperser interaction networks differ among strata, which is manifested in differences in interaction frequencies and the degree of mutual specialization. In general, the canopy stratum is composed of strong links and generalized associations, while the lower strata comprise weaker links and more specialized interactions. Investigating the VS of communities can provide us with a better understanding of species habitat restrictions, resource use, spatial movement, and species interactions. Especially in the face of global change, this knowledge will be important as these characteristics can imply different responses of species and taxa at a fine spatial scale.

Genetic monogamy and mate choice in a pair-living primate.

In pair-living mammals, genetic monogamy is extremely rare. One possible reason is that in socially monogamous animals, mate choice can be severely constrained, increasing the risk of inbreeding or pairing with an incompatible or low-quality partner. To escape these constraints, individuals might engage in extra-pair copulations. Alternatively, inbreeding can be avoided by dispersal. However, little is known about the interactions between mating system, mate choice, and dispersal in pair-living mammals. Here we genotyped 41 wild individuals from 14 groups of coppery titi monkeys (Plecturocebus cupreus) in Peruvian Amazon using 18 microsatellite loci. Parentage analyses of 18 young revealed no cases of extra-pair paternity, indicating that the study population is mostly genetically monogamous. We did not find evidence for relatedness- or heterozygosity-based mate choice. Despite the lack of evidence for active inbreeding avoidance via mate choice, mating partners were on average not related. We further found that dispersal was not sex-biased, with both sexes dispersing opportunistically over varying distances. Our findings suggest that even opportunistic dispersal, as long as it is not constrained, can generate sufficient genetic diversity to prevent inbreeding. This, in turn, can render active inbreeding avoidance via mate choice and extra-pair copulations less necessary, helping to maintain genetic monogamy.

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.

Do saki monkeys possess a grooming claw?

The presence of a grooming claw on the second toe is a characteristic of Strepsirrhini and tarsiers. There is also some evidence for the presence of a grooming claw in Platyrrhini. Here we report qualitative findings from different species of saki monkeys, genus Pithecia, on the presence of modified nails on the second toe. These observations suggest that a grooming claw or a grooming claw-like nail occurs in different Pithecia species, but that it does not consistently occur in all individuals.

What makes a pair bond in a Neotropical primate: female and male contributions.

Pair living and pair bonding are rare in mammals, and the mechanisms of their maintenance remain a puzzle. Titi monkeys, a 'textbook example' for 'monogamous' primates, have strong pair bonds and extensive male care. To investigate mechanisms of pair-bond maintenance, we studied seven wild groups of red titis (Plecturocebus cupreus) in Peruvian Amazonia over a period of 14 months. We analysed pair bonds by measuring proximity, grooming and approaches/leaves within pairs, and collected data on intergroup encounters. Females contributed to grooming more than males, especially during infant dependency, when most of the grooming within pairs was done by females. Females were also more active in controlling proximity between pair mates, making most of the approaches and leaves. Males, on the other hand, invested more in territorial defences. They participated in more intergroup encounters than females and were more active during these encounters. Our data is most consistent with the 'male-services' hypothesis for pair-bond maintenance, where a female contributes more to the proximity and affiliation maintenance while a male provides beneficial services.

Mixed company: a framework for understanding the composition and organization of mixed-species animal groups.

Mixed-species animal groups (MSGs) are widely acknowledged to increase predator avoidance and foraging efficiency, among other benefits, and thereby increase participants' fitness. Diversity in MSG composition ranges from two to 70 species of very similar or completely different phenotypes. Yet consistency in organization is also observable in that one or a few species usually have disproportionate importance for MSG formation and/or maintenance. We propose a two-dimensional framework for understanding this diversity and consistency, concentrating on the types of interactions possible between two individuals, usually of different species. One axis represents the similarity of benefit types traded between the individuals, while the second axis expresses asymmetry in the relative amount of benefits/costs accrued. Considering benefit types, one extreme represents the case of single-species groups wherein all individuals obtain the same supplementary, group-size-related benefits, and the other extreme comprises associations of very different, but complementary species (e.g. one partner creates access to food while the other provides vigilance). The relevance of social information and the matching of activities (e.g. speed of movement) are highest for relationships on the supplementary side of this axis, but so is competition; relationships between species will occur at points along this gradient where the benefits outweigh the costs. Considering benefit amounts given or received, extreme asymmetry occurs when one species is exclusively a benefit provider and the other a benefit user. Within this parameter space, some MSG systems are constrained to one kind of interaction, such as shoals of fish of similar species or leader-follower interactions in fish and other taxa. Other MSGs, such as terrestrial bird flocks, can simultaneously include a variety of supplementary and complementary interactions. We review the benefits that species obtain across the diversity of MSG types, and argue that the degree and nature of asymmetry between benefit providers and users should be measured and not just assumed. We then discuss evolutionary shifts in MSG types, focusing on drivers towards similarity in group composition, and selection on benefit providers to enhance the benefits they can receive from other species. Finally, we conclude by considering how individual and collective behaviour in MSGs may influence both the structure and processes of communities.

Author Correction: Small Neotropical primates promote the natural regeneration of anthropogenically disturbed areas.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Estimating seed dispersal distance: A comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species.

Seed dispersal distance (SDD) critically influences the survival of seedlings, spatial patterns of genetic diversity within plant populations, and gene flow among plant populations. In animal-dispersed species, foraging behavior and movement patterns determine SDD. Direct observations of seed dispersal events by animals in natural plant populations are mostly constrained by the high mobility and low visibility of seed dispersers. Therefore, diverse alternative methods are used to estimate seed dispersal distance, but direct comparisons of these approaches within the same seed dispersal system are mostly missing.We investigated two plant species with different life history traits, Leonia cymosa and Parkia panurensis, exclusively dispersed by two tamarin species, Saguinus mystax and Leontocebus nigrifrons. We compared SDD estimates obtained from direct observations, genetic identification of mother plants from seed coats, parentage analysis of seedlings/saplings, and phenomenological and mechanistic modeling approaches.SDD derived from the different methods ranged between 158 and 201 m for P. panurensis and between 178 and 318 m for L. cymosa. In P. panurensis, the modeling approaches resulted in moderately higher estimates than observations and genotyping of seed coats. In L. cymosa, parentage analysis resulted in a lower estimate than all other methods. Overall, SDD estimates for P. panurensis (179 ± 16 m; mean ± SD) were significantly lower than for L. cymosa (266 ± 59 m; mean ± SD).Differences among methods were related to processes of the seed dispersal loop integrated by the respective methods (e.g., seed deposition or seedling distribution). We discuss the merits and limitations of each method and highlight the aspects to be considered when comparing SDD derived from different methodologies. Differences among plant species were related to differences in reproductive traits influencing gut passage time and feeding behavior, highlighting the importance of plant traits on animal-mediated seed dispersal distance.