Anthony Di Fiore

Drought sensitivity of the Amazon rainforest

Amazon forests are a key but poorly understood component of the global carbon cycle. If, as anticipated, they dry this century, they might accelerate climate change through carbon losses and changed surface energy balances. We used records from multiple long-term monitoring plots across Amazonia to assess forest responses to the intense 2005 drought, a possible analog of future events. Affected forest lost biomass, reversing a large long-term carbon sink, with the greatest impacts observed where the dry season was unusually intense. Relative to pre-2005 conditions, forest subjected to a 100-millimeter increase in water deficit lost 5.3 megagrams of aboveground biomass of carbon per hectare. The drought had a total biomass carbon impact of 1.2 to 1.6 petagrams (1.2 × 1015 to 1.6 × 1015 grams). Amazon forests therefore appear vulnerable to increasing moisture stress, with the potential for large carbon losses to exert feedback on climate change.

Fission-Fusion Dynamics: New Research Frameworks

Renewed interest in fission‐fusion dynamics is due to the recognition that such dynamics may create unique challenges for social interaction and distinctive selective pressures acting on underlying communicative and cognitive abilities. New frameworks for integrating current knowledge on fission‐fusion dynamics emerge from a fundamental rethinking of the term “fission‐fusion” away from its current general use as a label for a particular modal type of social system (i.e., “fission‐fusion societies”). Specifically, because the degree of spatial and temporal cohesion of group members varies both within and across taxa, any social system can be described in terms of the extent to which it expresses fission‐fusion dynamics. This perspective has implications for socioecology, communication, cognitive demands, and human social evolution.

Global Conservation Significance of Ecuador's Yasuní National Park

Background The threats facing Ecuadors Yasuní National Park are emblematic of those confronting the greater western Amazon, one of the worlds last high-biodiversity wilderness areas. Notably, the countrys second largest untapped oil reserves—called “ITT”—lie beneath an intact, remote section of the park. The conservation significance of Yasuní may weigh heavily in upcoming state-level and international decisions, including whether to develop the oil or invest in alternatives. Methodology/Principal Findings We conducted the first comprehensive synthesis of biodiversity data for Yasuní. Mapping amphibian, bird, mammal, and plant distributions, we found eastern Ecuador and northern Peru to be the only regions in South America where species richness centers for all four taxonomic groups overlap. This quadruple richness center has only one viable strict protected area (IUCN levels I–IV): Yasuní. The park covers just 14% of the quadruple richness centers area, whereas active or proposed oil concessions cover 79%. Using field inventory data, we compared Yasunís local (alpha) and landscape (gamma) diversity to other sites, in the western Amazon and globally. These analyses further suggest that Yasuní is among the most biodiverse places on Earth, with apparent world richness records for amphibians, reptiles, bats, and trees. Yasuní also protects a considerable number of threatened species and regional endemics. Conclusions/Significance Yasuní has outstanding global conservation significance due to its extraordinary biodiversity and potential to sustain this biodiversity in the long term because of its 1) large size and wilderness character, 2) intact large-vertebrate assemblage, 3) IUCN level-II protection status in a region lacking other strict protected areas, and 4) likelihood of maintaining wet, rainforest conditions while anticipated climate change-induced drought intensifies in the eastern Amazon. However, further oil development in Yasuní jeopardizes its conservation values. These findings form the scientific basis for policy recommendations, including stopping any new oil activities and road construction in Yasuní and creating areas off-limits to large-scale development in adjacent northern Peru.

Markedly divergent estimates of Amazon forest carbon density from ground plots and satellites

Aim The accurate mapping of forest carbon stocks is essential for understanding the global carbon cycle, for assessing emissions from deforestation, and for rational land-use planning. Remote sensing (RS) is currently the key tool for this purpose, but RS does not estimate vegetation biomass directly, and thus may miss significant spatial variations in forest structure. We test the stated accuracy of pantropical carbon maps using a large independent field dataset. Location Tropical forests of the Amazon basin. The permanent archive of the field plot data can be accessed at: http://dx.doi.org/10.5521/FORESTPLOTS.NET/2014_1 Methods Two recent pantropical RS maps of vegetation carbon are compared to a unique ground-plot dataset, involving tree measurements in 413 large inventory plots located in nine countries. The RS maps were compared directly to field plots, and kriging of the field data was used to allow area-based comparisons. Results The two RS carbon maps fail to capture the main gradient in Amazon forest carbon detected using 413 ground plots, from the densely wooded tall forests of the north-east, to the light-wooded, shorter forests of the south-west. The differences between plots and RS maps far exceed the uncertainties given in these studies, with whole regions over- or under-estimated by > 25%, whereas regional uncertainties for the maps were reported to be < 5%. Main conclusions Pantropical biomass maps are widely used by governments and by projects aiming to reduce deforestation using carbon offsets, but may have significant regional biases. Carbon-mapping techniques must be revised to account for the known ecological variation in tree wood density and allometry to create maps suitable for carbon accounting. The use of single relationships between tree canopy height and above-ground biomass inevitably yields large, spatially correlated errors. This presents a significant challenge to both the forest conservation and remote sensing communities, because neither wood density nor species assemblages can be reliably mapped from space.

Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity

Seed dispersal by frugivores is thought to play an important role in the maintenance of tropical forest diversity. Spider monkeys ( Ateles spp.) are amongst the most frugivorous primates known, and they incorporate a diverse array of fruit species in their diets. In a 1-y study in lowland Ecuador, 670 h of focal observations and data on 916 faecal depositions were collected, and these data are used to describe the seed dispersal patterns of one group of wild spider monkeys ( Ateles belzebuth ) in terms of both the quantity of seeds dispersed and the primary seed shadows generated. Spider monkeys fed on the fruits of at least 152 plant species and swallowed seeds from more than 98% of these. Collected faecal samples contained seeds from at least 133 different plant species, with an average of 1.9 species (range: 0–7) per defecation. Individual spider monkeys dispersed a minimum of ∼195 000 seeds >1 mm in diameter per year, ∼35 000 of which were >3 mm in diameter. Mean retention time for seeds was 4.5 h. Seed dispersal distances averaged 443 m, but some seeds were moved >1250 m away from parental sources. These results suggest that declines in populations of spider monkeys might have a direct effect on forest dynamics, especially if other disperser species cannot compensate for their lost ecological services.

Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications.

Many wild primates occupy large home ranges and travel long distances each day. Navigating these ranges to find sufficient food presents a substantial cognitive challenge, but we are still far from understanding either how primates represent spatial information mentally or how they use this information to navigate under natural conditions. In the course of a long-term socioecological study, we investigated and compared the travel paths of sympatric spider monkeys (Ateles belzebuth) and woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. During several field seasons spanning an 8-year period, we followed focal individuals or groups of both species continuously for periods of multiple days and mapped their travel paths in detail. We found that both primates typically traveled through their home ranges following repeatedly used paths, or “routes”. Many of these routes were common to both species and were stable across study years. Several important routes appeared to be associated with distinct topographic features (e.g., ridgetops), which may constitute easily recognized landmarks useful for spatial navigation. The majority of all location records for both species fell along or near identified routes, as did most of the trees used for fruit feeding. Our results provide strong support for the idea that both woolly and spider monkey use route-based mental maps similar to those proposed by Poucet (Psychol Rev 100:163–182, 1993). We suggest that rather than remembering the specific locations of thousands of individual feeding trees and their phenological schedules, spider and woolly monkeys could nonetheless forage efficiently by committing to memory a series of route segments that, when followed, bring them into contact with many potential feeding sources for monitoring or visitation. Furthermore, because swallowed and defecated seeds are deposited in greater frequency along routes, the repeated use of particular travel paths over generations could profoundly influence the structure and composition of tropical forests, raising the intriguing possibility that these and other primate frugivores are active participants in constructing their own ecological niches. Building upon the insights of Byrne (Q J Exp Psychol 31:147–154, 1979, Normality and pathology in cognitive functions. Academic, London, pp 239–264, 1982) and Milton (The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York, 1980, On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 375–417, 2000), our results highlight the likely general importance of route-based travel in the memory and foraging strategies of nonhuman primates.

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. 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 are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

Dispersal patterns in sympatric woolly and spider monkeys: integrating molecular and observational data

Dispersal is a behavioral process that shuffles genes across the physical and social landscapes. Analysis of how genetic variation is structured hierarchically and among males versus females can provide insights into underlying dispersal processes, even when direct observations of dispersal events are lacking, but application of these techniques in primate studies has been limited. We investigated dispersal patterns in two South American primates — woolly and spider monkeys — using a combination of multilocus genotype data from > 150 animals sampled at two sites in Amazonian Ecuador and opportunistic field observations that shed light on likely dispersal events. Molecular analyses revealed considerable gene flow by females, but substantial male-mediated gene flow was also detected, particularly for woolly monkeys. In both taxa, the extent of population differentiation between the two study sites was greater for males than for females, indicating that gene flow by males has been more restricted historically. Additionally, in one group of spider monkeys, the average relatedness among adult males was significantly greater than that among females, consistent with strong male philopatry, and assignment tests for that group likewise suggest female-biased dispersal. However, for another group of spider monkeys — and for all groups of woolly monkey surveyed — these patterns were not observed. Our molecular results are concordant with field observations of immigrations by female spider monkeys, disappearances (likely emigrations) involving females of both species, and multiple sightings of solitary males and small bachelor groups in woolly monkeys, as well as with the specific dispersal histories of a few woolly monkey individuals discernable through longitudinal molecular sampling. Overall, the results demonstrate the utility of molecular approaches to studying dispersal in primates as a complement to observational studies, but also suggest that further evaluation of dispersal patterns among these primates is needed.

Social Behavior, Reproductive Strategies, and Population Genetic Structure of Lagothrix poeppigii

For species of primates in which females emigrate, we would expect males within groups to be related to one another. Kin selection theory suggests that these males should associate preferentially with one another, be more affiliative and cooperative with one another than females are, and compete less overtly with one another over reproductive opportunities than males in female philopatric taxa do. Precisely these patterns of social behavior characterize well-studied populations of 2 of the 3 atelin primate genera: spider monkeys (Ateles) and muriquis (Brachyteles). For the third atelin genus, Lagothrix, patterns of intragroup social behavior have been less well-documented. We studied the social and reproductive behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Ecuador during a one-year observational study and subsequently used molecular techniques to investigate population genetic structure and dispersal patterns for this taxon.Among adult male woolly monkeys, both affiliative and agonistic interactions were rare, and males were seldom in close proximity to one another. Relationships among male woolly monkeys are best characterized as tolerant, especially in the context of mating wherein direct competition among males was minimal despite the fact that females mated with multiple males. Relationships among females were likewise generally tolerant but nonaffiliative, though females often directed harassment towards copulating pairs. Affiliative interactions that did occur among woolly monkeys tended to be directed either between the sexes—primarily from female to male—or from younger towards older males, and the proximity partners of females tended to be members of the opposite sex. These results suggest that bonds between the sexes may be more important than same-sex social relationships and that direct female-female competition is an important feature of woolly monkey reproductive biology. Our genetic results indicate that, as in other atelins, dispersal by females is common, but some male dispersal likely occurs as well. In some but not all groups we studied, nonjuvenile males within social groups were more closely related to one another on average than females were, which is consistent with greater male than female philopatry. However, differences in these patterns among our study groups may reflect local variation in dispersal behavior.

Spider Monkeys: Diets of wild spider monkeys

Introduction The first comprehensive field study of wild spider monkeys was undertaken in Panama in the early 1930s by C. R. Carpenter. In discussing the diet of Ateles geoffroyi , Carpenter (1935) wrote, “Red spider monkeys have been classed correctly as frugivorous. It is estimated that about 90 percent of their food consists of fruit or nuts” (p. 174). Since that time, field studies of wild Ateles have consistently confirmed Carpenters early assessment of the highly frugivorous diet of spider monkeys, to the point where they are now treated as a classic example of a frugivorous primate and are often considered to be “ripe fruit specialists” (Cant, 1977; Klein and Klein, 1977; van Roosmalen, 1985; van Roosmalen and Klein, 1988; Cant, 1990; Dew, 2005; Wallace, 2005; Di Fiore and Campbell, 2007). In this chapter, we first review what is known of the diet of wild Ateles , paying particular attention to data from long-term ecological studies. In doing so, we address the physiological and morphological adaptations for frugivory that spider monkeys have evolved, as well as the connections among diet, food resource distribution and foraging behavior that are relevant to understanding the characteristic “fission–fusion” social organization of Ateles . From there, we move on to discussing the interesting variation seen in the diets of spider monkeys across tropical forest sites, and we address in more detail the diets of two populations of white-bellied spider monkeys ( Ateles belzebuth belzebuth ) which we and our colleagues and collaborators have studied over multiple years in Colombia and Ecuador.