Papers by Anthony Di Fiore
Molecular Phylogenetics and Evolution, 2015
Using complete mitochondrial genome sequences, we provide the first molecular analysis of the phy... more Using complete mitochondrial genome sequences, we provide the first molecular analysis of the phylogenetic position of the yellow-tailed woolly monkey, Lagothrix flavicauda (a.k.a. Oreonax flavicauda), a critically endangered neotropical primate endemic to northern Perú. The taxonomic status and phylogenetic position of yellow-tailed woolly monkeys have been debated for many years, but in this study both Bayesian and maximum likelihood phylogenetic reconstructions unequivocally support a monophyletic woolly monkey clade that includes L. flavicauda as the basal taxon within the radiation. Bayesian dating analyses using several alternative calibrations suggest that the divergence of yellow-tailed woolly monkeys from other Lagothrix occurred in the Pleistocene, $2.1 Ma, roughly 6.5 my after the divergence of woolly monkeys from their sister genus, Brachyteles. Additionally, comparative analysis of the cytochrome oxidase subunit 2 (COX2) gene shows that genetic distances between yellow-tailed woolly monkeys and other Lagothrix from across the genus' geographic distribution fall well within the range of between-species divergences seen in a large number of other platyrrhine primate genera at the same locus and outside the range of between-genus divergences. Our results thus confirm a position within Lagothrix for the yellow-tailed woolly monkey and strongly suggest that the name Oreonax be formally considered a synonym for this genus. This revision in taxonomic status does not change the dire conservation threats facing the yellow-tailed woolly monkey in Perú, where the remaining wild population is estimated at only $10,000 individuals living in a highly fragmented landscape.
Patterns of Aggression and Social Hierarchy in Wild Spider Monkeys (Ateles belzebuth)
American Journal of Physical Anthropology, 2013
Predation is proposed to be one of the most important factors influencing the evolution of mammal... more Predation is proposed to be one of the most important factors influencing the evolution of mammalian societies. Although predation risk is thought to influence both the behavior and grouping patterns of most diurnal primates, evidence supporting this hypothesis is still limited. The spatial and temporal patterns of mineral lick use by one group of white-bellied spider monkeys (Ateles belzebuth) were evaluated, based on the growing evidence that mineral licks are perceived as areas of relative high predation risk by Neotropical primates. The area immediately surrounding the mineral lick was the most intensively used area within the home range of the study group, particularly by large subgroups of monkeys, and there were differences in mean subgroup size on days of min-
Long-term thermal sensitivity of Earth’s tropical forests
Science
The sensitivity of tropical forest carbon to climate is a key uncertainty in predicting global cl... more The sensitivity of tropical forest carbon to climate is a key uncertainty in predicting global climate change. Although short-term drying and warming are known to affect forests, it is unknown if such effects translate into long-term responses. Here, we analyze 590 permanent plots measured across the tropics to derive the equilibrium climate controls on forest carbon. Maximum temperature is the most important predictor of aboveground biomass (−9.1 megagrams of carbon per hectare per degree Celsius), primarily by reducing woody productivity, and has a greater impact per °C in the hottest forests (>32.2°C). Our results nevertheless reveal greater thermal resilience than observations of short-term variation imply. To realize the long-term climate adaptation potential of tropical forests requires both protecting them and stabilizing Earth’s climate.
Ranging behavior and potential for territoriality in equatorial sakis (Pithecia aequatorialis ) in Amazonian Ecuador
American Journal of Physical Anthropology
Global Change Biology
This is an open access article under the terms of the Creative Commons Attribution License, which... more This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Animals : an open access journal from MDPI, Jan 13, 2018
Long-range vocal communication in socially monogamous titi monkeys is mediated by the production ... more Long-range vocal communication in socially monogamous titi monkeys is mediated by the production of loud, advertising calls in the form of solos, duets, and choruses. We conducted a power spectral analysis of duets and choruses (simply "duets" hereafter) followed by linear discriminant analysis using three acoustic parameters-dominant frequency of the combined signal, duet sequence duration, and pant call rate-comparing the coordinated vocalizations recorded from 36 family groups at 18 sites in Bolivia, Peru and Ecuador. Our analysis identified four distinct duetting patterns: (1) a donacophilus pattern, , characteristic of , , , and ; (2) a moloch pattern comprising , , , and ; (3) a torquatus pattern exemplified by the duet of ; and (4) the distinctive duet of , a putative member of the donacophilus group, which is characterized by a mix of broadband and narrowband syllables, many of which are unique to this species. We also document a sex-related difference in the bello...
The ISME journal, Jan 11, 2018
Over the past decade several studies have reported that the gut microbiomes of mammals with simil... more Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or...
Proceedings. Biological sciences, Jan 30, 2018
Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggr... more Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (), chimpanzees () and geladas (). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Ou...
Molecular phylogenetics and evolution, Jul 12, 2018
Phylogenetic relationships amongst the robust capuchin monkeys (genus Sapajus) are poorly underst... more Phylogenetic relationships amongst the robust capuchin monkeys (genus Sapajus) are poorly understood. Morphology-based taxonomies have recognized anywhere from one to twelve different species. The current IUCN (2017) classification lists eight robust capuchins: S. xanthosternos, S. nigritus, S. robustus, S. flavius, S. libidinosus, S. cay, S. apella and S. macrocephalus. Here, we assembled the first phylogenomic data set for Sapajus using ultra-conserved elements (UCEs) to reconstruct a capuchin phylogeny. All phylogenomic analyses strongly supported a deep divergence of Sapajus and Cebus clades within the capuchin monkeys, and provide support for Sapajus nigritus, S. robustus and S. xanthosternos as distinct species. However, the UCE phylogeny lumped the putative species S. cay, S. libidinosus, S. apella, S. macrocephalus, and S. flavius together as a single widespread lineage. A SNP phylogeny constructed from the UCE data was better resolved and recovered S. flavius and S. libidin...
Scientific reports, Jan 17, 2018
Species distribution models (SDMs) are widely used in ecology and conservation. Presence-only SDM... more Species distribution models (SDMs) are widely used in ecology and conservation. Presence-only SDMs such as MaxEnt frequently use natural history collections (NHCs) as occurrence data, given their huge numbers and accessibility. NHCs are often spatially biased which may generate inaccuracies in SDMs. Here, we test how the distribution of NHCs and MaxEnt predictions relates to a spatial abundance model, based on a large plot dataset for Amazonian tree species, using inverse distance weighting (IDW). We also propose a new pipeline to deal with inconsistencies in NHCs and to limit the area of occupancy of the species. We found a significant but weak positive relationship between the distribution of NHCs and IDW for 66% of the species. The relationship between SDMs and IDW was also significant but weakly positive for 95% of the species, and sensitivity for both analyses was high. Furthermore, the pipeline removed half of the NHCs records. Presence-only SDM applications should consider th...
Proceedings. Biological sciences, Jan 6, 2017
In wild primates, social behaviour influences exposure to environmentally acquired and directly t... more In wild primates, social behaviour influences exposure to environmentally acquired and directly transmitted microorganisms. Prior studies indicate that gut microbiota reflect pairwise social interactions among chimpanzee and baboon hosts. Here, we demonstrate that higher-order social network structure-beyond just pairwise interactions-drives gut bacterial composition in wild lemurs, which live in smaller and more cohesive groups than previously studied anthropoid species. Using 16S rRNA gene sequencing and social network analysis of grooming contacts, we estimate the relative impacts of hierarchical (i.e. multilevel) social structure, individual demographic traits, diet, scent-marking, and habitat overlap on bacteria acquisition in a wild population of Verreaux's sifaka (Propithecus verreauxi) consisting of seven social groups. We show that social group membership is clearly reflected in the microbiomes of individual sifaka, and that social groups with denser grooming networks h...
Ecology and evolution, Jun 1, 2017
With many sophisticated methods available for estimating migration, ecologists face the difficult... more With many sophisticated methods available for estimating migration, ecologists face the difficult decision of choosing for their specific line of work. Here we test and compare several methods, performing sanity and robustness tests, applying to large-scale data and discussing the results and interpretation. Five methods were selected to compare for their ability to estimate migration from spatially implicit and semi-explicit simulations based on three large-scale field datasets from South America (Guyana, Suriname, French Guiana and Ecuador). Space was incorporated semi-explicitly by a discrete probability mass function for local recruitment, migration from adjacent plots or from a metacommunity. Most methods were able to accurately estimate migration from spatially implicit simulations. For spatially semi-explicit simulations, estimation was shown to be the additive effect of migration from adjacent plots and the metacommunity. It was only accurate when migration from the metacomm...
Influences of sunrise and morning light on visual behavior of four sympatric New World primates ( Ateles, Callicebus, Lagothrix, and Pithecia)
Journal of Vision
Integrative and Comparative Biology
studies increasingly note the effect of captivity or the built environment on the microbiome of h... more studies increasingly note the effect of captivity or the built environment on the microbiome of humans and other animals. As symbiotic microbes are essential to many aspects of biology (e.g., digestive and immune functions), it is important to understand how lifestyle differences can impact the microbiome, and, consequently, the health of hosts. Animals living in captivity experience a range of changes that may influence the gut bacteria, such as diet changes, treatments, and reduced contact with other individuals, species and variable environmental substrates that act as sources of bacterial diversity. Thus far, initial results from previous studies point to a pattern of decreased bacterial diversity in captive animals. However, these studies are relatively limited in the scope of species that have been examined. Here we present a dataset that includes paired wild and captive samples from mammalian taxa across six Orders to investigate generalizable patterns of the effects captivity on mammalian gut bacteria. In comparing the wild to the captive condition, our results indicate that alpha diversity of the gut bacteria remains consistent in some mammalian hosts (bovids, giraffes, anteaters, and aardvarks), declines in the captive condition in some hosts (canids, primates, and equids), and increases in the captive condition in one host taxon (rhinoceros). Differences in gut bacterial beta diversity between the captive and wild state were observed for most of the taxa surveyed, except the even-toed ungulates (bovids and giraffes). Additionally, beta diversity variation was also strongly influenced by host taxonomic group, diet type, and gut fermentation physiology. Bacterial taxa that demonstrated larger shifts in relative abundance between the captive and wild states included members of the Firmicutes and Bacteroidetes. Overall, the patterns that we observe will inform a range of disciplines from veterinary practice to captive breeding efforts for biological conservation. Furthermore, bacterial taxa that persist in the captive state provide unique insight into symbiotic relationships with the host.
Patterns in Gut Microbiota Similarity Associated with Degree of Sociality among Sex Classes of a Neotropical Primate
Microbial ecology, Jul 26, 2017
Studies of human and domestic animal models indicate that related individuals and those that spen... more Studies of human and domestic animal models indicate that related individuals and those that spend the most time in physical contact typically have more similar gut microbial communities. However, few studies have examined these factors in wild mammals where complex social dynamics and a variety of interacting environmental factors may impact the patterns observed in controlled systems. Here, we explore the effect of host kinship and time spent in social contact on the gut microbiota of wild, black howler monkeys (Alouatta pigra). Our results indicate that closely related individuals had less similar gut microbial communities than non-related individuals. However, the effect was small. In contrast, as previously reported in baboons and chimpanzees, individuals that spent more time in contact (0 m) and close proximity (0-1 m) had more similar gut microbial communities. This pattern was driven by adult female-adult female dyads, which generally spend more time in social contact than a...
Science advances, 2017
Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cul... more Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats-mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers ...
Scientific Reports, 2016
In some primate lineages, polymorphisms in the X-linked M/LWS opsin gene have produced intraspeci... more In some primate lineages, polymorphisms in the X-linked M/LWS opsin gene have produced intraspecific variation in color vision. In these species, heterozygous females exhibit trichromacy, while males and homozygous females exhibit dichromacy. The evolutionary persistence of these polymorphisms suggests that balancing selection maintains color vision variation, possibly through a 'trichromat advantage' in detecting yellow/orange/red foods against foliage. We identified genetic evidence of polymorphic trichromacy in a population of Verreaux's sifaka (Propithecus verreauxi) at Kirindy Mitea National Park in Madagascar, and explored effects of color vision on reproductive success and feeding behavior using nine years of morphological, demographic, and feeding data. We found that trichromats and dichromats residing in social groups with trichromats exhibit higher body mass indices than individuals in dichromat-only groups. Additionally, individuals in a trichromat social group devoted significantly more time to fruit feeding and had longer fruit feeding bouts than individuals in dichromat-only groups. We hypothesize that, due to small, cohesive sifaka social groups, a trichromat advantage in detecting productive fruit patches during the energetically stressful dry season also benefits dichromats in a trichromat's group. Our results offer the first support for the 'mutual benefit of association' hypothesis regarding the maintenance of polymorphic trichromacy in primates. Researchers have long noted that primates are unique among placental mammals in exhibiting trichromatic color vision 1,2. Whereas most other mammals are dichromats and can distinguish color along a single dimension (shorter wavelengths vs. longer wavelengths, or blues/violets vs. yellows/greens/reds), trichromats can distinguish not only between these shorter and longer wavelengths but also between middle and long wavelengths (i.e., greens vs. reds: Fig. 1). Anatomically, trichromacy in primates is achieved through the presence of three types of retinal cone photoreceptors that are maximally responsive to either short wavelengths (S cones), middle wavelengths (M cones), or long wavelengths (L cones); however, the genetic mechanisms underlying trichromacy differ between major primate clades 2. All catarrhine primates (Old World monkeys, apes, humans) exhibit routine trichromacy due to a fixed duplication of the M/LWS opsin gene that allows normal individuals to produce both M and L retinal cones 3,4. In contrast, most platyrrhines (New World monkeys) and some lemurs exhibit polymorphic trichromacy, wherein different alleles encoding M or L cones are found at the X-linked M/LWS opsin locus 5-8. In these species, females that are heterozygous at the M/LWS locus develop separate M and L retinal cones, which-in conjunction with the autosomally-encoded S cone-produce trichromacy. Meanwhile homozygous females and all males develop a single type of M/L cone and thus have dichromatic color vision 2. Since sex-linked polymorphic trichromacy was first identified, researchers have sought to understand the ecological factors influencing its evolution and maintenance 7,9-13. The long-term persistence of polymorphic trichromacy suggests that balancing selection acts to maintain color vision diversity in some primate species 7,9,14. However, substantial debate exists 7,9,12-15 regarding which form of balancing selection is acting on the M/LWS locus to maintain polymorphic trichromacy (i.e., 'heterozygote advantage' , 'niche divergence' , or 'mutual benefit of association').
Assay for determining the sex of primates
Amer J Primatol, 2003
In a year-long study, I investigated the ranging behavior of lowland woolly monkeys (Lagothrix la... more In a year-long study, I investigated the ranging behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a terra firma rainforest in Yasuní National Park, Ecuador, and examined the relationship between ranging, diet, food availability, and food patch use for this population. In Yasuní the total home range sizes for two social groups were 124 and 108 ha, which are much smaller than has been reported previously for Lagothrix elsewhere in its geographic distribution. The mean yearly day range estimates for these same groups were 1,792 m and 1,878 m, which are well within the range of variation previously reported. Ranging behavior was not correlated with the current habitat-wide abundance of ripe fruit, which comprises 76.3% of the yearly diet for this population, but was associated with one measure of likely insect prey abundance and with the availability of immature fruits, a minimal part of the diet. Specifically, one study group moved significantly greater distances during months of high likely insect prey abundance and when immature fruits were abundant. The second study group also traveled farther when likely insect prey abundance was high and when immature fruits were abundant, although the latter relationship only approached significance. This group also devoted significantly more of its daily activity budget to travel during these times. These results indicate that variation in ripe fruit abundance makes no meaningful contribution to explaining variation in ranging behavior for this population of woolly monkeys. Instead, the results raise the possibility that some aspects of the ranging behavior of frugivorous primates may be related to the availability of alternative food sources, such as animal prey, or to monitoring the phenological status of important fruit trees, rather than simply reflecting the degree of intragroup feeding competition. Am. J.
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Papers by Anthony Di Fiore