Direct links between resource availability and activity budget better reveal ecological patterns of endangered Coimbra-Filho's titi monkey.

Many primatological studies do not assess direct indexes of food availability to make inferences about behavioral strategies. We related the diet and behavior of a group of Callicebus coimbrai in northeastern Brazil to fruit availability indexes and compared this pattern between seasons (direct and indirect assessment of food availability) to assess whether direct and indirect approaches detect similar ecological patterns. We monitored the study group for 33 months (5 days/month) via scan sampling. The monthly availability of fruits and new leaves was recorded in phenological transects. Fruit availability varied across years based on fruit prevalence, and timing and duration of the abundant seasons. We did not find evidence of a time-minimizing strategy, since C. coimbrai did not change its activity levels according to food availability. However, the negative relationship between foraging and fruit availability indicates that C. coimbrai can compensate for the lower fruit availability by increasing the search for alternative food sources. Monthly fruit consumption was positively correlated to fruit availability and negatively related to the consumption of other food items. However, the behavioral and feeding profiles did not vary between seasons and were not related to rainfall levels. Primate studies should directly relate behavioral and feeding profiles to fruit availability indices, thus avoiding using seasons as proxies of food availability.

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.

Temperature and exudativory as drivers of the marmoset (Callithrix spp.) daily activity period.

Primates are affected by fluctuations in ambient temperatures, mostly through thermoregulatory costs and changes in the availability of food. In the present study, we investigate whether the ambient temperature and proxies of food availability affect the activity period of marmosets (Callithrix spp.). We predicted that: (i) at colder sites, marmosets would spend more time at sleeping sites; (ii) midday resting bouts would be longer at hotter sites; (iii) the onset/cessation of activity and resting behavior at midday would be more closely related to temperature than food availability, and (iv) highly exudativorous groups would have higher total levels of resting. We compiled data on the onset and cessation of activity and the time spent resting at midday from seven marmoset studies from sites with a wide range of temperatures. We used generalized linear mixed models to verify the relationship between the dependent variables (lag between dawn and the onset of activities, lag between cessation of activities and dusk, and proportion of resting during midday) and the minimum and maximum temperatures at the respective study sites, together with proxies of food availability (exudativory rates, the amount of habitat available per individual, and net primary productivity) using each sample month as a sampling unit and the identity of the study as a categorical random factor. At colder sites and during colder months, the marmosets left sleeping trees later in the morning and ceased their activities earlier, while at hotter sites and during hotter months, they spent more time resting during midday. More exudativorous groups become active later in the morning, but also ceased their activities later. The abundance of food did not affect the timing of activities. We provide evidence that both low and high temperatures affect marmosets' activities, and that their activity period appears to be more influenced by the thermal environment than food availability.

Taxonomic, functional and phylogenetic bat diversity decrease from more to less complex natural habitats in the Amazon.

The high levels of biodiversity in the Amazon are maintained mostly due to its composition as a natural mosaic of different habitats, including both unflooded and flooded forests, campinaranas, and savannahs. Here, we compared multiple dimensions of α- and ß- bat biodiversity between four natural Amazonian habitats (savannah, campinarana, forest patches, and continuous forest). In addition, we explored the extent to which bat communities in the different habitats are nested within one another, and compared the community-level functional uniqueness and community-weighted mean traits between habitats. Our results show that taxonomic, functional and phylogenetic α-diversity of bats is higher in continuous forest than in any of the other habitat types. The continuous forest also harbours more unique species, and indeed, the bat community assemblages in the less-complex habitats, including forest patches, campinarana and savannahs, are taxonomic, functional and phylogenetic sub-sets of the assemblage found in the continuous forest. By examining ß-diversity partitions and species composition, we are able to shed light on the mechanisms behind the variation in diversity between the four habitat types, which reflect a process of environmental sorting along a habitat gradient going from a more complex to a less complex habitat. We conclude that nesting patterns along the mosaic of habitats are determined by differences in complexity between habitats and that taxonomic and functional uniqueness contribute to overall regional bat diversity and functionality. Ongoing human-induced disturbances of these habitats could provoke an unprecedented loss of bat diversity and functionality with negative consequences for biodiversity and ecosystem services.

The occurrence of the red-handed howler monkey (Alouatta belzebul) in amazonian savannas is related to forest patch area and density of flooded area palms.

All Neotropical primates are arboreal and thus depend on forests for their survival. Arboreality puts many Neotropical primates at risk of extinction due to the high rates of deforestation in the tropics. We assessed the influence of vegetation structure and forest patch attributes on the occurrence of the threatened red-handed howler monkey (Alouatta belzebul) in an Amazonian savanna. Using a sample of 38 forest patches in a region of approximately 2000 km2 in the state of Amapá, northern Brazil, we used logistic regression to find the best predictors of the occurrence of A. belzebul. We assessed patch area, patch isolation, the proportion of seasonally flooded forest in the patch, the density of flooded area palms, forest height, canopy cover, and diameter at breast height of trees. Patch area and palm density were the best predictors of the occurrence of A. belzebul in forest patches, both having a positive effect on the probability of occurrence. Our results indicate that areas of flooded forest in forest patches may be keystone habitats for A. belzebul living in Amazonian savannas. The observed effect of palm density on A. belzebul suggests that this variable is useful for planning conservation actions, including the selection of areas for protection and management strategies for areas inhabited by this primate.

A primate at risk in Northeast Brazil: local extinctions of Coimbra Filho's titi (Callicebus coimbrai).

Identifying the factors that determine local extinction of populations is crucial to ensure species conservation. Forest-dwelling primates are especially vulnerable to habitat fragmentation, although few studies have provided systematic evidence of local extinctions. Over an 11-year period, approximately 100 remnant populations of the endangered Coimbra Filho's titi monkey (Callicebus coimbrai) have been found within the geographic range of the species in Bahia and Sergipe, Northeast Brazil. During the present study, extinction of 13 of these populations was recorded through intensive surveys. These extinctions were detected from evidence of intensive logging and clear-cutting, interviews with local residents and systematic searches of the sites where occurrence of the species had been confirmed in previous surveys. These local extinctions represent approximately 10 % of the known populations of C. coimbrai and up to 28.3 % of the area occupied by the species. Comparison of the vegetation structure in fragments where extinction was recorded and where the species still occurs indicated that sparser understorey may be a correlate of extinction, combined with the fact that extinctions occurred within fragments characterised by relatively high levels of anthropogenic disturbance. These findings reinforce the Endangered status of the species and the urgent need for intensification of conservation measures within the most impacted areas of the geographic distribution of C. coimbrai.

Dense understory and absence of capuchin monkeys (Sapajus xanthosternos) predict higher density of common marmosets (Callithrix jacchus) in the Brazilian Northeast.

Understanding the effects of habitat structure and other environmental variables on the density of a species can help define its habitat preferences and key ecological determinants of population parameters. The present study evaluated the effects of fragment size, the presence of a key predator/competitor, the yellow-breasted capuchin (Sapajus xanthosternos), primary productivity, the abundance of bromeliads, and habitat structure on the population density of the common marmoset (Callithrix jacchus). A total of 21 fragments were surveyed within a 350-km long zone of coastal Atlantic Forest representing the southern extreme of the distribution of the species in the Brazilian Northeast. An index of marmoset density was generated for each site based on playback surveys. The relationship between the density of marmosets and a set of parameters was evaluated by multiple regression. A Principal Components Analysis (PCA) condensed the five variables of habitat structure into two principal components, which contained 85% of their combined variation. The model that best explained the density of marmosets (R(2) = 59.1) contained the second PCA component and the presence/absence of capuchins. The analysis indicated that the marmosets prefer forests with denser understory, whether or not they are secondary habitats. The negative effect of the presence of capuchins may be related to predation pressure. The results of this study indicate that multiple-site studies may provide important insights into the habitat preferences of primate species and the factors that affect their population density.

Seasonal variation in the length of the daily activity period in buffy-headed marmosets (Callithrix flaviceps): an important consideration for the analysis of foraging strategies in observational field studies of primates.

Activity budgets are widely used in primate behavioral studies for the analysis of ecological strategies. In some cases, there is considerable seasonal variation in the length of the daily activity period. Here, activity budgets from two field studies of Callithrix flaviceps were compiled first by the traditional approach (proportion of scan sample records) and then by considering the proportion of time dedicated to each activity over the 24-hr cycle (adjusted budget). Both groups were almost invariably active for at least 1-2 hr less than the daylight period, with significantly shorter activity periods during the austral winter, when the daylight period was up to 2:35 hr shorter than in the summer. The adjustment of activity budgets provided a completely different perspective on foraging strategies. Whereas the basic budgets indicated a significant increase in foraging and moving during the resource-poor dry season (winter) months, the time-adjusted data revealed that the primary strategy was a time-minimizing one, with the animals simply spending more time at rest during the longer activity periods of summer days. While both groups followed the same pattern of relatively short activity periods, there were considerable differences between sites in the mean duration of the period in a given month, and in behavior patterns, although the analysis of the determining factors was beyond the scope of the present study. Overall, the results of the study indicate that the manipulation of the duration of the daily activity period may be an integral component of primate behavioral strategies, and that this parameter should be taken into account systematically when evaluating activity patterns, especially at sites at relatively high latitudes where day length may vary considerably over the course of the year.

Can roads be used as transects for primate population surveys?.

Line transect distance sampling (LTDS) can be applied to either trails or roads. However, it is likely that sampling along roads might result in biased density estimates. In this paper, we compared the results obtained with LTDS applied on trails and roads for two primate species (Callithrix penicillata and Callicebus nigrifrons) to clarify whether roads are appropriate transects to estimate densities. We performed standard LTDS surveys in two nature reserves in south-eastern Brazil. Effective strip width and population density were different between trails and roads for C. penicillata, but not for C. nigrifrons. The results suggest that roads are not appropriate for use as transects in primate surveys, at least for some species. Further work is required to fully understand this issue, but in the meantime we recommend that researchers avoid using roads as transects or treat roads and trails as covariates when sampling on roads is unavoidable.

Use of water sources by buffy-headed marmosets (Callithrix flaviceps) at two sites in the Brazilian Atlantic Forest.

Many primates are able to satisfy most of their water requirements from the liquid content of their food, but almost all need to visit external water sources during critical periods. The present study analyses the use of water sources in two free-ranging groups of buffy-headed marmosets (Caratinga and RBAR groups) over an annual cycle. At both sites, a large proportion of the days had no visits, and the visitation rate fell by approximately half in the wet season. Differences between sites appear to reflect both contrasts in habitat structure and the composition of the diet. Despite inhabiting a more humid environment, for example, the RBAR group visited water sources on a significantly larger proportion of days than the Caratinga group. While 94.2% of the records for the RBAR group involved bromeliads, this type of source was not recorded at Caratinga, where terrestrial sources were used relatively frequently. Seasonal variation indicates that arboreal sources are preferred over terrestrial ones at both sites, and that rivers are used as a last resort, when other sources are scarce. The use of terrestrial sources involves cautious and coordinated group behaviour, which presumably reflects the perceived predation risk. Overall, the relatively frequent use of watering sites in the RBAR group might be related to its highly fungivorous diet, in comparison with the more typical gummivorous diet of the Caratinga group, although the exact implications of this difference are not clear from the available data.

Why feed on fungi? The nutritional content of sporocarps consumed by buffy-headed marmosets, Callithrix flaviceps (Primates: Callitrichidae), in southeastern Brazil.

The typical diet of Callithrix marmosets is based on gums, although fungi are the dietary staple of a single group of Callithrix flaviceps studied in the Augusto Ruschi Biological Reserve, in southeastern Brazil. Here, we present the nutritional composition of two species of Mycocitrus fungi consumed by C. flaviceps, and discuss possible determinants of the preference of the marmosets for fungi over gums. The fungi were high in sugar/fiber and poor in proteins, and were similar in composition to the gums exploited by other marmosets and to the fungi consumed by Callimico goeldii. The reduced protein content of the fungi may be offset by the arthropod component of the diet of the Callithrix flaviceps study group. The low relative metabolic rate and enlarged cecum of Callithrix enable these marmosets to exploit foods with a high fiber content. In addition, the greater digestibility of chitin in comparison with plant fiber may make fungi a nutritionally more valuable resource to marmosets than gums. Marmosets, thus, may prefer to feed on fungi when an adequate supply of this resource is available in the environment.

Four breeding females in a free-ranging group of buffy-headed marmosets (Callithrix flaviceps).

The reproductive patterns recorded in a free-ranging group of Callithrix flaviceps were unique in a number of ways, including 4 females breeding simultaneously, a non-breeding dominant female, and a well-defined birth season. In addition, all observed copulations involved extragroup individuals. The more socially dominant breeding female had more births and more surviving offspring, on average, than subordinate females, and was implicated in at least 1 infanticide. All 4 females carried their own infants for relatively long periods following the births, apparently as a defence mechanism related to the risk of infanticide. It remains unclear whether the unusual number of breeding females in the group represents a species-specific pattern, or the result of specific local circumstances.

Feeding ecology of a group of buffy-headed marmosets (Callithrix flaviceps): fungi as a preferred resource.

Mycophagy is a relatively rare behavior in primates and has only been recorded in five callitrichid species. Here, we present data on the feeding ecology of a free-ranging group of Callithrix flaviceps, which was studied in the Augusto Ruschi Biological Reserve, Southeastern Brazil, in 2008. In contrast with other marmosets, which are typically gummivorous, the study group was predominantly mycophagous-insectivorous, with fungi corresponding to 64.8% of total feeding records, and gum (6.1%) and fruit (3.3%) together providing only a minor part of the diet. Prey corresponded to 25.8% of the group's diet. The fungi (Mycocitrus spp.) consumed by the marmosets were found attached to the stems of Merostachys bamboo. As the animal component of the group's diet was similar to that recorded in studies of other marmosets, we propose that fungi were exploited primarily as a substitute for plant material, in particular exudates. This highly mycophagous diet may be determined by two principal factors: (1) the abundance of fungi within the study area, and (2) the avoidance of bark gouging, for which C. flaviceps may be less specialized than most other marmosets. These conclusions are supported by comparisons with other marmoset groups, which indicate an ecological specialization for mycophagy in C. flaviceps, and that the species will resort to gummivory in habitats where fungi are scarce.