Identifying structural connectivity priorities in eastern Paraguay's fragmented Atlantic Forest.

The Atlantic Forest of eastern Paraguay has experienced extensive recent deforestation. Less than one-third of the region is forested, and the remaining forest largely consists of isolated remnants with potentially disrupted connectivity for forest fauna. We used a graph theory approach to identify those forest remnants that are important in maintaining landscape structural connectivity for mammals in this fragmented forest. We quantified structural connectivity for forest remnants over the period 2000-2019 at three levels: the entire network of Atlantic Forest remnants in eastern Paraguay; at 10 smaller, nested spatial scales (40-10,000 m) encompassing a range of potential mammalian dispersal abilities; and at the level of individual remnants. We used 10 graph theory metrics to assess aspects of network complexity, dispersal-route efficiency, and individual remnant importance in supporting structural connectivity. We identified forest remnants that serve as important structural connectivity roles as stepping stones, hubs, or articulation points and that should be prioritized for connectivity conservation. Structural connectivity was constrained for organisms incapable of travelling at least 9-12 km (farthest distances between nearest-neighboring forest remnants depending on whether smaller remnants were included or not) and was particularly limited for area-sensitive forest-specialist mammals. With the increased forest loss and fragmentation that is occurring, the connectivity of this system will likely be further compromised, but most of the remnants that we identified as playing important roles for structural connectivity were outside of the country's proposed "green corridor," indicating additional areas where conservation action can be directed.

Food availability, plant diversity, and vegetation structure drive behavioral and ecological variation in Endangered Coimbra-Filho's titi monkeys.

There is wide variability in primate behavior and ecology. Understanding how frugivorous primates behave under different habitat fragmentation levels is key for effective conservation and management of species and their habitats. We evaluated the seasonality in activity budget, diet, and ranging behavior of two groups of Endangered Coimbra-Filho's titi monkeys (Callicebus coimbrai). One group inhabited a 14-ha forest fragment, whereas the other lived in a 522-ha fragment. We measured the monthly density of trees and lianas available as food sources over 8 months. We also collected behavioral and group location data every 5 min, from dawn to dusk, using the scan sampling method. The two forest fragments differed seasonally in the number of fruiting food-resource available. In the 14-ha fragment, we found that the time spent by titi monkeys feeding, foraging, resting, and traveling differed seasonally. In the 522-ha fragment, titi monkeys exhibited seasonal differences in time spent sleeping, socializing, foraging, and revisiting food sources. In both titi monkey groups, diets varied seasonally. Our findings indicate that Coimbra-Filho's titi monkeys can exhibit behavioral flexibility in their activity budgets, diets, and movement patterns. Such flexibility is important for this species to survive in fragmented habitats and may be linked to three key factors: species-specific resource availability, plant species diversity, and the vegetation structure of each forest fragment.

Small mammal glucocorticoid concentrations vary with forest fragment size, trap type, and mammal taxa in the Interior Atlantic Forest.

Species that live in degraded habitats often show signs of physiological stress. Glucocorticoid hormones (e.g., corticosterone and cortisol) are often assessed as a proxy of the extent of physiological stress an animal has experienced. Our goal was to quantify glucocorticoids in free-ranging small mammals in fragments of Interior Atlantic Forest. We extracted glucocorticoids from fur samples of 106 small mammals (rodent genera Akodon and Oligoryzomys, and marsupial genera Gracilinanus and Marmosa) from six forest fragments (2-1200 ha) in the Reserva Natural Tapytá, Caazapá Department, Paraguay. To our knowledge, this is the first publication of corticosterone and cortisol levels for three of the four sampled genera (Akodon, Oligoryzomys, and Marmosa) in this forest system. We discovered three notable results. First, as predicted, glucocorticoid levels were higher in individuals living withing small forest fragments. Second, animals captured live using restraint trapping methods (Sherman traps) had higher glucocorticoid levels than those animals captured using kill traps (Victor traps), suggesting that hair glucocorticoid measures can reflect acute stress levels in addition to long-term glucocorticoid incorporation. These acute levels are likely due to urinary steroids diffusing into the hair shaft. This finding raises a concern about the use of certain trapping techniques in association with fur hormone analysis. Finally, as expected, we also detected genus-specific differences in glucocorticoid levels, as well as cortisol/corticosterone ratios.

Predictive sampling effort and species-area relationship models for estimating richness in fragmented landscapes.

Loss of habitat, specifically deforestation, is a major driver of biodiversity loss. Species-area relationship (SAR) models traditionally have been used for estimating species richness, species loss as a function of habitat loss, and extrapolation of richness for given areas. Sampling-species relationships (SSRs) are interrelated yet separate drivers for species richness estimates. Traditionally, however, SAR and SSR models have been used independently and not incorporated into a single approach. We developed and compared predictive models that incorporate sampling effort species-area relationships (SESARS) along the entire Atlantic Forest of South America, and then applied the best-fit model to estimate richness in forest remnants of Interior Atlantic Forest of eastern Paraguay. This framework was applied to non-volant small mammal assemblages that reflect different tolerances to forest loss and fragmentation. In order to account for differences in functionality we estimated small mammal richness of 1) the entire non-volant small mammal assemblage, including introduced species; 2) the native species forest assemblage; and 3) the forest-specialist assemblage, with the latter two assemblages being subsets of the entire assemblage. Finally, we geospatially modeled species richness for each of the three assemblages throughout eastern Paraguay to identify remnants with high species richness. We found that multiple regression power-law interaction-term models that only included area and the interactions of area and sampling as predictors, worked best for predicting species richness for the entire assemblage and the native species forest assemblage, while several traditional SAR models (logistic, power, exponential, and ratio) best described forest-specialist richness. Species richness was significantly different between assemblages. We identified obvious remnants with high species richness in eastern Paraguay, and these remnants often were geographically isolated. We also found relatively high predicted species richness (in relation to the entire range of predicted richness values) in several geographically-isolated, medium-size forest remnants that likely have not been considered as possible priority areas for conservation. These findings highlight the importance of using an empirical dataset, created using sources representing diverse sampling efforts, to develop robust predictive models. This approach is particularly important in geographic locations where field sampling is limited yet the geographic area is experiencing rapid and dramatic land cover changes. When combined, area and sampling are powerful modeling predictors for questions of biogeography, ecology, and conservation, especially when addressing habitat loss and fragmentation.

Impending extinction crisis of the world's primates: Why primates matter.

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.

Run, hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia.

Although primate predation is rarely observed, a series of primate anti-predation strategies have been described. Energetic costs of such strategies can vary from high-cost mobbing, via less costly alarm calling, to low-cost furtive concealment. Here we report the anti-predation strategies of red-nosed cuxiú, Chiropotes albinasus, based on direct observations from four study sites in southeastern Brazilian Amazonia. Over a collective period of 1255 fieldwork hours, we observed nine direct interactions between raptors (all potential predators) and red-nosed cuxiús. Of these, one (11%) resulted in predation. Raptors involved were: Harpia harpyja (four events), Leucopternis sp. (two events), Spizaëtus tyrannus (one event), and unidentified large raptors (two events). Predation attempts occurred in flooded-forest and terra firme rainforest, were directed at both adult and non-adult cuxiús, and involved both adult and juvenile raptors. Anti-predation strategies adopted by the cuxiús included: (1) group defence and mobbing behaviour (two occasions), (2) dropping into dense sub-canopy (seven occasions), (3) alarm calling (eight occasions), and (4) fleeing to, and hiding in, dense vegetation (eight occasions). During each encounter at least two of these behaviours were recorded. These are the first published records of predation, predation attempts, and anti-predator behaviour involving red-nosed cuxiú.

Pitheciid research comes of age: Past puzzles, current progress, and future priorities.

For a long time, members of the Pitheciidae were among the least studied of all Neotropical primates. But times have changed. Here, we trace the trajectory of this change and show how the articles in this special edition illustrate new knowledge and developments in our understanding of pitheciid ecology, behavior, and conservation. We propose new directions and priorities for future research, especially to ensure the effective conservation of pitheciids, and demonstrate how studies of this family are now the focus of hypothesis-driven research that not only allows the details of this family's biology to be explored, but will allow its biology to be compared with other primate lineages.

Pitheciids in fragmented habitats: Land cover change and its implications for conservation.

Pitheciids (Cacajao, Callicebus, Chiropotes, and Pithecia) have experienced habitat loss and fragmentation across their geographic range in South America. Some populations living in habitat fragments live in smaller groups, travel shorter distances, and consume items that are not regularly found in the diets of populations living in continuous habitat; however, these patterns are not consistent across species. I used the IUCN Red List of Threatened Species to delineate the geographic range and conservation status of 43 pitheciid species. I calculated the amount of modified land cover within the range of each species, as well as the extent to which the remaining habitat exists in small fragments and the amount of forest lost from 2000 to 2012. Mean forest fragment size ranged from 12 to 12,027 ha, and mean forest loss from 2000 to 2012 ranged from 10.7% for Chiropotes to 0.9% for Pithecia. Critically Endangered and Endangered species represented 20.9% of the pitheciid species, and 46.5% of these species had population trends documented as decreasing. Total modified land cover was greatest for Callicebus species (18.0% of geographic range), followed by Chiropotes (13.8%), Pithecia (4.4%), and Cacajao (1.1%). Species of greater conservation concern had smaller geographic ranges, and a greater percentage of their range consisting of modified land cover than species of lower conservation concern. Species of greater conservation concern also had a greater percentage of forest lost from 2000 to 2012 and a smaller percentage of the remaining forest being protected. Most studies of pitheciids in fragments have concentrated on census data; the behavior of pitheciids in fragments has been examined for only 9 of the 43 species. Increased data on the responses of pitheciid species to forest loss and fragmentation are necessary in order to address pitheciid conservation, especially in areas undergoing severe habitat loss.

Mixed-species associations in cuxiús (genus Chiropotes).

Polyspecific or mixed-species associations, where two or more species come together to forage and travel as a unit, have been reported in many primate species. These associations appear to offer a number of benefits to the species involved including increased foraging efficiency and decreased risk of predation. While several researchers have suggested that cuxiús (genus Chiropotes) form mixed-species associations, previous studies have not identified the circumstances under which cuxiús form associations or whether they form associations more often than would be expected by chance. Here we present data on the formation of mixed-species associations by four species of cuxiús at eight different sites in Brazil, Suriname, and Guyana. We analyzed data from two of the study sites, (Biological Dynamics of Forest Fragments Project (BDFFP), Brazil and the Upper Essequibo Conservation Concession (UECC), Guyana, to assess whether associations occurred more than would be expected by chance encounters and identify the factors influencing their formation. Cuxiús showed a high degree of inter-site variation in the frequency of time spent in association (ranging from 2 to 26% of observation time) and duration of associations (mean duration from 22 min to 2.5 hr). Sapajus apella was the most common association partner at most sites. At BDFFP, cuxiús formed associations more frequently but not for longer duration than expected by chance. For much of the year at UECC, associations were not more frequent or longer than chance. However, during the dry season, cuxiús formed associations with S. apella significantly more often and for longer duration than predicted by chance. Cuxiús at UECC formed associations significantly more often when in smaller subgroups and when foraging for insects, and alarm called significantly less frequently during associations. We suggest cuxiús form mixed-species associations at some sites as an adaptive strategy to decrease predation risk and/or increase foraging efficiency.

Terrestrial activity in pitheciins (Cacajao, Chiropotes, and Pithecia).

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a "local pattern" of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types.

Behavioral modifications in northern bearded saki monkeys (Chiropotes satanas chiropotes) in forest fragments of central Amazonia.

We investigated behavioral differences among seven groups of northern bearded saki monkeys (Chiropotes satanas chiropotes) living in five forest fragments and two areas of continuous forest at the Biological Dynamics of Forest Fragments Project study area, located approximately 80 km north of Manaus, Brazil. We collected data in six research cycles from July-August 2003 to January 2005-April 2006. When bearded saki monkeys were present in a study area, we followed the group from dawn until dusk for three consecutive days. Every 5 min, we conducted behavioral scans of all visible individuals. There was a positive relationship between forest size and group size, but animals in the small forest fragments lived at greater densities. Bearded saki monkeys in the smaller fragments spent more time resting, less time traveling, and less time vocalizing, but there was no relationship between forest size and the amount of time spent feeding. Our results indicate that the main behavioral differences among the groups are related to the amount of forest resources (e.g., fruit trees, space) available to the monkeys in the smaller fragments, as well as the resulting smaller group sizes. We stress the need to preserve large tracts of forest and provide connectivity between forest patches.

Home range estimates vary with sample size and methods.

Accurate estimates of a primate's home range are important, yet methods vary greatly. This paper examines the accuracy of minimum convex polygon (MCP), adaptive kernel (AK) and fixed kernel (FK) estimators by comparing home range estimates of northern bearded saki monkeys (Chiropotes satanas chiropotes) living in forest fragments and continuous forest in the Brazilian Amazon area. MCP was more accurate than AK and FK in calculating home and day range when sample size was small, and AK overestimated range most frequently. It is important to consider the various home range methods, as the appropriate method may depend on sample size and the species' behavioral ecology.