Hand preference in wild crab-eating capuchin monkeys (Sapajus libidinosus) in the coastal area of Northest Brazil.

Handedness is a fundamental human trait, although recent research, especially on nonhuman primates, has shown that it is displayed by other animals as well (e.g., chimpanzees, gorillas). In this study, we explore hand preference in wild crab-eating tufted capuchin monkeys (Sapajus libidinosus) inhabiting a mangrove forest located on the coastal area of Northeast Brazil (Maranhão State). Tufted capuchin monkeys at our site use facultatively wooden tools to crack open crabs. We observed hand preference in 12 subjects who spontaneously participated in experiment sessions, in which we provided crabs and tools on wooden platforms. We recorded (using events and bouts) two unimanual tasks, (tool or crab) grabbing and (tool or crab) pounding, and one bimanual task, crab pulling, where one hand kept the crab in place while the other pulled off parts of the crab. Hand preference increased with greater strength needed to perform the task and its complexity. While only 17%-25% of capuchins showed hand preference during grabbing, 44%-64% showed hand preference during pounding, and most subjects 64%-80% displayed a right-hand preference when performing the bimanual task, for which all lateralized individuals were right-handed. Hand preference did not vary between adults and juvenile individuals and was not consistent across tasks. Group-level hand preference was found only for the bimanual task, for which all lateralized individuals were right-handed. Our findings are in concordance with those of other primate studies showing the emergence of hemispheric specialization for bimanual actions, highlight the importance of conducting such studies on diverse type of tasks, and show the feasibility to conduct experimental manipulation under natural conditions.

Establishing the relationship between non-human primates and mangrove forests at the global, national, and local scales.

Global and spatially explicit information about the interaction between habitat and wildlife species is critical to enhancing conservation efforts. Despite the recognized importance of mangrove forests to non-human primates, the relationship between the two lacks understanding. To counter this, we created the MangPrim-21 database to map and measure the locations of interactions between all non-human primates and all mangrove forests globally. We report our findings across the global, national, and local scales for all inventoried non-human primates and all inventoried mangrove forests. Globally, we find that half of all non-primates potentially use mangrove forests, and more than half of the global mangrove forest falls within the delineated range of at least one non-human primate species. Nationally, we find that Indonesia, Madagascar, Brazil, Cameroon, and Malaysia likely have the most non-human primate and mangrove forest interactions. At the subnational level, we find that several discrete locations in Kalimantan are critical to both mangrove forests and non-human primates. The MangPrim-21 database provides a globally consistent and locally applicable database of non-human primate and mangrove forest interactions. The results presented have broader implications for non-human primate and mangrove conservation and global actions to protect both. Additionally, our results raise questions about the idea that non-human primates primarily use mangrove forests as a refuge from human encroachment and habitat degradation.

Stone tools improve diet quality in wild monkeys.

Tool use is a fundamental feature of human evolution. Stone tools are in the archaeological record from 3.4 Ma, even before Homo,1 and the use of stone tools probably predated the split between hominins and panins.2 Using tools (hereafter, tooling cf Fragaszy and Mangalam3) is hypothesized to have improved hominins' foraging efficiency or access to high-quality foods.4-7 This hypothesis is supported if feeding with tools positively contributes to diet quality in extant non-human primates or if foraging efficiency is increased by tooling. However, the contribution of tooling to non-human primates' foraging success has never been investigated through a direct analysis of nutritional ecology.8,9 We used multi-dimensional nutritional geometry to analyze energy and macronutrients (nonstructural carbohydrates, lipids, and protein) in the diets of wild capuchin monkeys (Sapajus libidinous) that routinely crack palm nuts with stone hammers.10,11 We show that eating nuts obtained through tooling helps monkeys to achieve more consistent dietary intakes. Tooling increased the net energy gain by 50% and decreased the proportion of fiber ingested by 7%. Tooling also increased the daily non-protein energy intake. By contrast, protein intake remained constant across foraging days, suggesting a pattern of macronutrient regulation called protein prioritization, which is also found in contemporary humans.8,9 In addition, tooling reduced dispersion in the ratio of protein to non-protein energy, suggesting a role in macronutrient balancing. Our findings suggest that tooling prior to tool making could have substantially increased the nutritional security of ancestral hominins, sowing the seeds for cultural development.5,7 VIDEO ABSTRACT.

Free-Living Aquatic Turtles as Sentinels of Salmonella spp. for Water Bodies.

Reptile-associated human salmonellosis cases have increased recently in the United States. It is not uncommon to find healthy chelonians shedding Salmonella enterica. The rate and frequency of bacterial shedding are not fully understood, and most studies have focused on captive vs. free-living chelonians and often in relation to an outbreak. Their ecology and significance as sentinels are important to understanding Salmonella transmission. In 2012-2013, Salmonella prevalence was determined for free-living aquatic turtles in man-made ponds in Clarke and Oconee Counties, in northern Georgia (USA) and the correlation between species, basking ecology, demographics (age/sex), season, or landcover with prevalence was assessed. The genetic relatedness between turtle and archived, human isolates, as well as, other archived animal and water isolates reported from this study area was examined. Salmonella was isolated from 45 of 194 turtles (23.2%, range 14-100%) across six species. Prevalence was higher in juveniles (36%) than adults (20%), higher in females (33%) than males (18%), and higher in bottom-dwelling species (31%; common and loggerhead musk turtles, common snapping turtles) than basking species (15%; sliders, painted turtles). Salmonella prevalence decreased as forest cover, canopy cover, and distance from roads increased. Prevalence was also higher in low-density, residential areas that have 20-49% impervious surface. A total of 9 different serovars of two subspecies were isolated including 3 S. enterica subsp. arizonae and 44 S. enterica subsp. enterica (two turtles had two serotypes isolated from each). Among the S. enterica serovars, Montevideo (n = 13) and Rubislaw (n = 11) were predominant. Salmonella serovars Muenchen, Newport, Mississippi, Inverness, Brazil, and Paratyphi B. var L(+) tartrate positive (Java) were also isolated. Importantly, 85% of the turtle isolates matched pulsed-field gel electrophoresis patterns of human isolates, including those reported from Georgia. Collectively, these results suggest that turtles accumulate Salmonella present in water bodies, and they may be effective sentinels of environmental contamination. Ultimately, the Salmonella prevalence rates in wild aquatic turtles, especially those strains shared with humans, highlight a significant public health concern.

Using natural travel paths to infer and compare primate cognition in the wild.

Within comparative psychology, the evolution of animal cognition is typically studied either by comparing indirect measures of cognitive abilities (e.g., relative brain size) across many species or by conducting batteries of decision-making experiments among (typically) a few captive species. Here, we propose a third, complementary approach: inferring and comparing cognitive abilities through observational field records of natural information gradients and the associated variation in decision-making outcomes, using the ranging behavior of wild animals. To demonstrate the feasibility of our proposal, we present the results of a global survey assessing the availability of long-term ranging data sets from wild primates and the willingness of primatologists to share such data. We explore three ways in which such ranging data, with or without the associated behavioral and ecological data often collected by primatologists, might be used to infer and compare spatial cognition. Finally, we suggest how ecological complexity may be best incorporated into comparative analyses.

The role of hunting on Sapajus xanthosternos' landscape of fear in the Atlantic Forest, Brazil.

Habitats with spatial variation in food availability, predation risk, and hunting pressure allow us to study how animals resolve the trade-off between food searching and predator avoidance. We investigated the influence of food availability, predation risk, and the perceived predation risk on habitat use by a primate living under high hunting pressure, the yellow-breasted capuchin monkeys, Sapajus xanthosternos, at Una Biological Reserve (ReBio Una). We hypothesized that the hunting pressure occurring in the capuchins' home range would favor predator avoidance to the detriment of searching for food. We characterized a set of covariates related to resource availability (fruit and invertebrate biomasses, feeding on dispersed and clumped food items, sleeping sites), perceived predation risk (alarm calls given to terrestrial and aerial predators, silent group movement, and vigilance behavior), and actual predation risk (evidence of hunting) and estimated their effects on how one group of capuchin monkeys uses its habitat. The group divides its time among three major forest types within their home range: agroforest, mature, and secondary. Our results suggest that the actual and perceived risk of hunting by humans, as well as the perceived predation risk by both terrestrial and aerial predators, were significant determinants of capuchin monkeys' space use. Yellow-breasted capuchin monkeys' space use was negatively related to the risk of hunting by humans (actual evidence and silent behavior), the perceived risk of predation by both aerial and terrestrial predators, and the presence of sleeping sites. Capuchin monkeys' use of space was not related to the biomass of fruits in the habitat, and the biomass of invertebrates had a very low positive effect. We confirmed our prediction that in a habitat with high hunting pressure, the risk of predation, both perceived and actual, had a more significant impact on how yellow-breasted capuchins used space than did food availability.

Navigating in a challenging semiarid environment: the use of a route-based mental map by a small-bodied neotropical primate.

To increase efficiency in the search for resources, many animals rely on their spatial abilities. Specifically, primates have been reported to use mostly topological and rarely Euclidean maps when navigating in large-scale space. Here, we aimed to investigate if the navigation of wild common marmosets inhabiting a semiarid environment is consistent with a topological representation and how environmental factors affect navigation. We collected 497 h of direct behavioral and GPS information on a group of marmosets using a 2-min instantaneous focal animal sampling technique. We found that our study group reused not only long-route segments (mean of 1007 m) but entire daily routes, a pattern that is not commonly seen in primates. The most frequently reused route segments were the ones closer to feeding sites, distant to resting sites, and in areas sparse in tree vegetation. We also identified a total of 56 clustered direction change points indicating that the group modified their direction of travel. These changes in direction were influenced by their close proximity to resting and feeding sites. Despite our small sample size, the obtained results are important and consistent with the contention that common marmosets navigate using a topological map that seems to benefit these animals in response to the exploitation of clustered exudate trees. Based on our findings, we hypothesize that the Caatinga landscape imposes physical restrictions in our group's navigation such as gaps in vegetation, small trees and xerophytic plants. This study, based on preliminary evidence, raises the question of whether navigation patterns are an intrinsic characteristic of a species or are ecologically dependent and change according to the environment.

Spatial cognition in western gorillas (Gorilla gorilla): an analysis of distance, linearity, and speed of travel routes.

Spatial memory allows animals to retain information regarding the location, distribution, and quality of feeding sites to optimize foraging decisions. Western gorillas inhabit a complex environment with spatiotemporal fluctuations of resource availability, prefer fruits when available, and travel long distances to reach them. Here, we examined movement patterns-such as linearity, distance, and speed of traveling-to assess whether gorillas optimize travel when reaching out-of-sight valued resources. Our results show that gorillas travel patterns are affected by the activity they perform next, the type of food they feed on, and their preference level to specific fruits, suggesting they are able to optimize foraging based on spatial knowledge of their resources. Additionally, gorillas left in the direction of the next resource as soon as they started traveling and decelerated before approaching food resources, as evidence that they have a representation of their exact locations. Moreover, home range familiarity did not influence gorillas' movement patterns, as travel linearity in the core and periphery did not differ, suggesting that they may not depend wholly on a network of paths to navigate their habitat. These results show some overlap with chimpanzees' spatial abilities. Differences between the two ape species exist, however, potentially reflecting more their differences in diet (degree of frugivory) rather than their cognitive abilities. Further studies should focus on determining whether gorillas are able to use shortcuts and/or approach the same goal from multiple directions to better identify the spatial abilities used by this species.

Spatial mapping shows that some African elephants use cognitive maps to navigate the core but not the periphery of their home ranges.

Strategies of navigation have been shown to play a critical role when animals revisit resource sites across large home ranges. The habitual route system appears to be a sufficient strategy for animals to navigate while avoiding the cognitive cost of traveling using the Euclidean map. We hypothesize that wild elephants travel more frequently using habitual routes to revisit resource sites as opposed to using the Euclidean map. To identify the elephants' habitual routes, we created a python script, which accounted for frequently used route segments that constituted the habitual routes. Results showed elephant navigation flexibility traveling at Kruger National Park landscape. Elephants shift strategies of navigation depend on the familiarity of their surroundings. In the core area of their home range, elephants traveled using the Euclidean map, but intraindividual differences showed that elephants were then converted to habitual routes when navigating within the less familiar periphery of their home range. These findings are analogous to the recent experimental results found in smaller mammals that showed that rats encode locations according to their familiarity with their surroundings. In addition, as recently observed in monkeys, intersections of habitual routes are important locations used by elephants when making navigation decisions. We found a strong association between intersections and new segment usage by elephants when they revisit resource sites, suggesting that intersection choice may contribute to the spatial representations elephants use when repeatedly revisiting resource sites.

Spatial Patterns of Primate Electrocutions in Diani, Kenya.

Electrocution from power infrastructure threatens many primate species, yet knowledge of effective evidence-based mitigation strategies is limited. Mitigation planning requires an understanding of the spatial distribution of electrocutions to prioritize high-risk areas. In Diani, a coastal Kenyan town, electrocution is an important cause of death for five primate species. In this study we aim to describe the spatial patterns of electrocutions and electric shock incidents (collectively referred to as electrocutions hereafter) and identify electrocution hotspots to guide an effective primate conservation approach in Diani. Colobus Conservation, a not-for-profit organization, has recorded electrocutions and annual primate census data since 1998. We georeferenced 329 electrocution data points and analyzed them using QGIS. We identified and compared hotspots across species, seasons, and time using kernel density estimation and Getis-Ord-Gi*. We employed spatial regression models to test whether primate population density and power line density predicted the location of electrocution hotspots. Electrocutions occurred in hotspots that showed little variation in location between species and seasons. The limited variation in hotspot location over time likely occurred as a result of new building development in Diani and variability in primate detection rates by community members. Primate density and power line density were significant predictors of electrocution density for Angolan black-and-white colobus (Colobus angolensis palliatus) and Sykes monkeys (Cercopithecus mitis albogularis), but the relationship was weak, suggesting the presence of additional risk factors. This study provides a framework for systematic spatial prioritization of power lines that can be used to reduce primate electrocutions in Diani, and can be adopted in other areas of the world where primates are at risk from electrocution.

Urbanized White Ibises (Eudocimus albus) as Carriers of Salmonella enterica of Significance to Public Health and Wildlife.

Worldwide, Salmonella spp. is a significant cause of disease for both humans and wildlife, with wild birds adapted to urban environments having different opportunities for pathogen exposure, infection, and transmission compared to their natural conspecifics. Food provisioning by people may influence these factors, especially when high-density mixed species flocks aggregate. White Ibises (Eudocimus albus), an iconic Everglades species in decline in Florida, are becoming increasingly common in urbanized areas of south Florida where most are hand-fed. We examined the prevalence of Salmonella shedding by ibises to determine the role of landscape characteristics where ibis forage and their behavior, on shedding rates. We also compared Salmonella isolated from ibises to human isolates to better understand non-foodborne human salmonellosis. From 2010-2013, 13% (n = 261) adult/subadult ibises and 35% (n = 72) nestlings sampled were shedding Salmonella. The prevalence of Salmonella shedding by ibises significantly decreased as the percent of Palustrine emergent wetlands and herbaceous grasslands increased, and increased as the proportion of open-developed land types (e.g. parks, lawns, golf courses) increased, suggesting that natural ecosystem land cover types supported birds with a lower prevalence of infection. A high diversity of Salmonella serotypes (n = 24) and strain types (43 PFGE types) were shed by ibises, of which 33% of the serotypes ranked in the top 20 of high significance for people in the years of the study. Importantly, 44% of the Salmonella Pulsed-Field Gel Electrophoresis patterns for ibis isolates (n = 43) matched profiles in the CDC PulseNet USA database. Of these, 20% came from Florida in the same three years we sampled ibis. Importantly, there was a negative relationship between the amount of Palustrine emergent wetland and the number of Salmonella isolates from ibises that matched human cases in the PulseNet database (p = 0.056). Together, our results indicate that ibises are good indicators of salmonellae strains circulating in their environment and they have both the potential and opportunity to transmit salmonellae to people. Finally, they may act as salmonellae carriers to natural environments where other more highly-susceptible groups (nestlings) may be detrimentally affected.

Diversity and Persistence of Salmonella enterica Strains in Rural Landscapes in the Southeastern United States.

Salmonellosis cases in the in the United States show distinct geographical trends, with the southeast reporting among the highest rates of illness. In the state of Georgia, USA, non-outbreak associated salmonellosis is especially high in the southern low-lying coastal plain. Here we examined the distribution of Salmonella enterica in environmental waters and associated wildlife in two distinct watersheds, one in the Atlantic Coastal Plain (a high case rate rural area) physiographic province and one in the Piedmont (a lower case rate rural area). Salmonella were isolated from the two regions and compared for serovar and strain diversity, as well as distribution, between the two study areas, using both a retrospective and prospective design. Thirty-seven unique serovars and 204 unique strain types were identified by pulsed-field gel electrophoresis (PFGE). Salmonella serovars Braenderup, Give, Hartford, and Muenchen were dominant in both watersheds. Two serovars, specifically S. Muenchen and S. Rubislaw, were consistently isolated from both systems, including water and small mammals. Conversely, 24 serovars tended to be site-specific (64.8%, n = 37). Compared to the other Salmonella serovars isolated from these sites, S. Muenchen and S. Rubislaw exhibited significant genetic diversity. Among a subset of PFGE patterns, approximately half of the environmental strain types matched entries in the USA PulseNet database of human cases. Ninety percent of S. Muenchen strains from the Little River basin (the high case rate area) matched PFGE entries in PulseNet compared to 33.33% of S. Muenchen strains from the North Oconee River region (the lower case rate area). Underlying the diversity and turnover of Salmonella strains observed for these two watersheds is the persistence of specific Salmonella serovars and strain types that may be adapted to these watersheds and landscapes.

Epidemiology of a Salmonella enterica subsp. enterica serovar Typhimurium strain associated with a songbird outbreak.

Salmonella enterica subsp. enterica serovar Typhimurium is responsible for the majority of salmonellosis cases worldwide. This Salmonella serovar is also responsible for die-offs in songbird populations. In 2009, there was an S. Typhimurium epizootic reported in pine siskins in the eastern United States. At the time, there was also a human outbreak with this serovar that was associated with contaminated peanuts. As peanuts are also used in wild-bird food, it was hypothesized that the pine siskin epizootic was related to this human outbreak. A comparison of songbird and human S. Typhimurium pulsed-field gel electrophoresis (PFGE) patterns revealed that the epizootic was attributed not to the peanut-associated strain but, rather, to a songbird strain first characterized from an American goldfinch in 1998. This same S. Typhimurium strain (PFGE type A3) was also identified in the PulseNet USA database, accounting for 137 of 77,941 total S. Typhimurium PFGE entries. A second molecular typing method, multiple-locus variable-number tandem-repeat analysis (MLVA), confirmed that the same strain was responsible for the pine siskin epizootic in the eastern United States but was distinct from a genetically related strain isolated from pine siskins in Minnesota. The pine siskin A3 strain was first encountered in May 2008 in an American goldfinch and later in a northern cardinal at the start of the pine siskin epizootic. MLVA also confirmed the clonal nature of S. Typhimurium in songbirds and established that the pine siskin epizootic strain was unique to the finch family. For 2009, the distribution of PFGE type A3 in passerines and humans mirrored the highest population density of pine siskins for the East Coast.

Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus.

Socioecological models assume that primates adapt their social behavior to ecological conditions, and predict that food availability and distribution, predation risk and risk of infanticide by males affect patterns of social organization, social structure and mating system of primates. However, adaptability and variation of social behavior may be constrained by conservative adaptations and by phylogenetic inertia. The comparative study of closely related species can help to identify the relative contribution of ecological and of genetic determinants to primate social systems. We compared ecological features and social behavior of two species of the genus Sapajus, S. nigritus in Carlos Botelho State Park, an area of Atlantic Forest in São Paulo state, and S. libidinosus in Fazenda Boa Vista, a semi-arid habitat in Piauí state, Brazil. S. libidinosus perceived higher predation risk and fed on clumped, high quality, and usurpable resources (fruits) all year round, whereas S. nigritus perceived lower predation risk and relied on evenly distributed, low-quality food sources (leaves) during periods of fruit shortage. As predicted by socioecology models, S. libidinosus females were philopatric and established linear and stable dominance hierarchies, coalitions, and grooming relationships. S. nigritus females competed less often, and could transfer between groups, which might explain the lack of coalitions and grooming bonds among them. Both populations presented similar group size and composition and the same polygynous mating system. The species differed from each other in accordance with differences in the characteristics of their main food sources, as predicted by socioecological models, suggesting that phylogenetic inertia does not constrain social relationships established among female Sapajus. The similarity in mating systems indicates that this element of the social system is not affected by ecological variables and thus, is a more conservative behavioral feature of the genus Sapajus.