Mantled Howler Monkeys (Alouatta palliata) in a Costa Rican Forest Fragment Do Not Modify Activity Budgets or Spatial Cohesion in Response to Anthropogenic Edges.

Forest fragmentation increases forest edge relative to forest interior, with lower vegetation quality common for primates in edge zones. Because most primates live in human-modified tropical forests within 1 km of their edges, it is critical to understand how primates cope with edge effects. Few studies have investigated how primates inhabiting a fragment alter their behaviour across forest edge and interior zones. Here we investigate how anthropogenic edges affect the activity and spatial cohesion of mantled howler monkeys (Alouatta palliata) at the La Suerte Biological Research Station (LSBRS), a Costa Rican forest fragment. We predicted the monkeys would spend greater proportions of their activity budget feeding and resting and a lower proportion travelling in edge compared to forest interior to compensate for lower resource availability in the edge. We also predicted that spatial cohesion would be lower in the edge to mitigate feeding competition. We collected data on activity and spatial cohesion (nearest neighbour distance; number of individuals within 5 m) in forest edge and interior zones via instantaneous sampling of focal animals. Contrary to predictions, the monkeys spent equal proportions of time feeding, resting and travelling in forest edge and interior. Similarly, there were no biologically meaningful differences in the number of individuals or the distance between nearest neighbours in the edge (1.0 individuals; 1.56 m) versus the interior (0.8 individuals; 1.73 m). Our results indicate that A. palliata at LSBRS do not adjust their activity or spatial cohesion patterns in response to anthropogenic edge effects, suggesting that the monkeys here exhibit less behavioural flexibility than A. palliata at some other sites. To develop effective primate conservation plans, it is therefore crucial to study primate species' responses to fragmentation across their geographic range.

Supplemented howler monkeys eat less wild fruits, but do not change their activity budgets.

Research on the influence of food supplementation on primate behavior has focused on terrestrial and semiterrestrial species. Its effects on highly arboreal species are poorly known. We assessed the influence of food supplementation on the feeding behavior and activity budget of four adult female and two adult male brown howler monkeys (Alouatta guariba clamitans) belonging to two groups (JA and RO) that inhabited periurban forest fragments in southern Brazil. We used the "focal-animal" method during 6-8 full days per month from March to August 2017 (916 h of observation) to record the behavior of the study subjects. The feeding events of the focal individual were recorded using the "all occurrences" method. The supplementation was unevenly distributed during the day and accounted for 5-6% of all feeding events of male and female howlers, respectively. JA always received fruit in a platform, whereas RO had access to fruits and processed foods on roofs and directly from humans. The mean biomass of wild foods ingested by each adult per day was >300% higher than the ingested biomass of supplemented foods (females: 395 vs. 109 g/day; males: 377 vs. 120 g/day), but the ingestion rate of supplemented foods was ca. 400% higher than that of wild foods (females: 17 vs. 4 g/min; males: 19 vs. 5 g/min). The activity budgets of females and males were dominated by resting (66-72%) followed by feeding (18-14%), moving (12-11%), and socializing (2%). We found that food supplementation reduced the ingestion of wild fruits, but it did not affect the howlers' need to ingest a given amount of leaves per day and the time spent resting, feeding, moving, and socializing.

Assessment of releases of translocated and rehabilitated Yucatán black howler monkeys (Alouatta pigra) in Belize to determine factors influencing survivorship.

Rehabilitation and reintroduction have become important to the management and welfare of primates worldwide. However, the suitability and success of these practices must be evaluated to determine their effectiveness as well as to improve programs and methods, as little is known about the factors influencing survival of released individuals. Between 2011 and 2014, 28 howler monkeys, Alouatta pigra, were released at Fireburn Reserve, northern Belize by the Primate Rehabilitation Centre of Belize: Wildtracks. From March to August 2015, field trips were made to determine the number and identity of surviving individuals to assess whether differences in individual outcomes (survived or disappeared) could be associated with specific characteristics or backgrounds of the monkeys. Fourteen of the twenty rehabilitated monkeys and seven of the eight translocated monkeys were found alive. The proportion of surviving individuals was not significantly different between rehabilitants and translocated animals, males and females, former pets and wild animals, short- and long-term rehabilitants, or different ages at release or intake. As mortality was low and none of the general factors analyzed influenced survivorship, it is suggested that chance or individual traits may be important in the outcomes of releases. This study provides an example of successful population reintroduction from both rehabilitation and translocation programs, and the first analyses of characteristics impacting the success of releases of howler monkeys.

An assessment of skin temperature gradients in a tropical primate using infrared thermography and subcutaneous implants.

Infrared thermography has become a useful tool to assess surface temperatures of animals for thermoregulatory research. However, surface temperatures are an endpoint along the body's core-shell temperature gradient. Skin and fur are the peripheral tissues most exposed to ambient thermal conditions and are known to serve as thermosensors that initiate thermoregulatory responses. Yet relatively little is known about how surface temperatures of wild mammals measured by infrared thermography relate to subcutaneous temperatures. Moreover, this relationship may differ with the degree that fur covers the body. To assess the relationship between temperatures and temperature gradients in peripheral tissues between furred and bare areas, we collected data from wild mantled howling monkeys (Alouatta palliata) in Costa Rica. We used infrared thermography to measure surface temperatures of the furred dorsum and bare facial areas of the body, recorded concurrent subcutaneous temperatures in the dorsum, and measured ambient thermal conditions via a weather station. Temperature gradients through cutaneous tissues (subcutaneous-surface temperature) and surface temperature gradients (surface-ambient temperature) were calculated. Our results indicate that there are differences in temperatures and temperature gradients in furred versus bare areas of mantled howlers. Under natural thermal conditions experienced by wild animals, the bare facial areas were warmer than temperatures in the furred dorsum, and cutaneous temperature gradients in the face were more variable than the dorsum, consistent with these bare areas acting as thermal windows. Cutaneous temperature gradients in the dorsum were more closely linked to subcutaneous temperatures, while facial temperature gradients were more heavily influenced by ambient conditions. These findings indicate that despite the insulative properties of fur, for mantled howling monkeys surface temperatures of furred areas still demonstrate a relationship with subcutaneous temperatures. Given that most mammals possess dense fur, this provides insight for using infrared imaging in thermoregulatory studies of wild animals lacking bare skin.

Determinants of daily path length in black and gold howler monkeys (Alouatta caraya) in northeastern Argentina.

Models used to explain the social organization of primates suggest that variation in daily path length (DPL) is a response to variation in resource distribution and the intensity of intragroup feeding competition. However, daily path length may be affected by a number of other factors including the availability and distribution of nutritionally complementary food items, temperature which can influence activity budget, patterns of subgrouping, and the frequency and function of intergroup encounters. In this 6-month study (total 495 hr of quantitative data), we examined daily path lengths in two neighboring groups of black and gold howler monkeys (Alouatta caraya) inhabiting a semi-deciduous gallery forest in San Cayetano (27° 30'S, 58° 41'W), in the northwest province of Corrientes, Argentina. Both study groups were of similar size and composition. We identified relationships across groups between time spent feeding on fruits, leaves, and flowers, the number of trees visited, group spread, frequency of intergroup encounters, mean daily temperature, and DPL. Our results suggest that variation in food availability had a significant impact on howler ranging behavior by increasing DPL under conditions of high immature and mature fruit availability, and by decreasing DPL with increased availability and increased time invested in feeding on mature leaves. These results do not support the contention that a reduction in food availability or an increase in within-group feeding competition increased DPL in black and gold howler monkeys. DPL in black and gold howlers is influenced by several interrelated factors. In this regard we suggest that models of socio-ecology and ecological constraints need to reconsider how factors such as individual nutritional requirements, social tolerance and group cohesion, and the spatial and temporal availability of preferred and nearby food resources influence primate ranging behavior. Am. J. Primatol. 78:825-837, 2016. © 2016 Wiley Periodicals, Inc.

Individual participation in intergroup contests is mediated by numerical assessment strategies in black howler and tufted capuchin monkeys.

Asymmetries in resource-holding potential between opposing groups frequently determine outcomes of intergroup contests. Since both numerical superiority and high intergroup dominance rank may confer competitive advantages, group members should benefit from assessing the relative strength of rivals prior to engaging in defensive displays. However, differences in individual assessment may emerge when cost-benefit trade-offs differ among group members. We examine the influence of numerical superiority and intergroup dominance relationships on individual participation in intergroup encounters in black howler monkeys (Alouatta pigra) and tufted capuchin monkeys (Sapajus nigritus). Black howlers responded with longer vocal displays during encounters with neighbours with an equal number of resident males, while tufted capuchins increased their participation with increasing relative male group size. Within each species, males and females responded similarly to varying numerical odds, suggesting that despite pay-off asymmetries between males and females, both sexes were similarly influenced by numerical asymmetries in deciding to participate in collective group defence. Whereas the outcome of contests among tufted capuchins was determined by relative male group size, reflected in a pronounced intergroup dominance hierarchy, the absence of dominance relationships among black howler groups may have provoked prolonged vocal displays in order to assess rival groups with matching competitive abilities.

A comparative assessment of hand preference in captive red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos.

There are two major theories that attempt to explain hand preference in non-human primates-the 'task complexity' theory and the 'postural origins' theory. In the present study, we proposed a third hypothesis to explain the evolutionary origin of hand preference in non-human primates, stating that it could have evolved owing to structural and functional adaptations to feeding, which we refer to as the 'niche structure' hypothesis. We attempted to explore this hypothesis by comparing hand preference across species that differ in the feeding ecology and niche structure: red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. The red howler monkeys used the mouth to obtain food more frequently than the yellow-breasted capuchin monkeys. The red howler monkeys almost never reached for food presented on the opposite side of a wire mesh or inside a portable container, whereas the yellow-breasted capuchin monkeys reached for food presented in all four spatial arrangements (scattered, on the opposite side of a wire mesh, inside a suspended container, and inside a portable container). In contrast to the red howler monkeys that almost never acquired bipedal and clinging posture, the yellow-breasted capuchin monkeys acquired all five body postures (sitting, bipedal, tripedal, clinging, and hanging). Although there was no difference between the proportion of the red howler monkeys and the yellow-breasted capuchin monkeys that preferentially used one hand, the yellow-breasted capuchin monkeys exhibited an overall weaker hand preference than the red howler monkeys. Differences in hand preference diminished with the increasing complexity of the reaching-for-food tasks, i.e., the relatively more complex tasks were perceived as equally complex by both the red howler monkeys and the yellow-breasted capuchin monkeys. These findings suggest that species-specific differences in feeding ecology and niche structure can influence the perception of the complexity of the task and, consequently, hand preference.

Effects of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra).

Lactation is an energy demanding phase in the reproductive cycle of female mammals. For this reason, several studies have assessed the effects of lactation on female behavior. In this study we examine the influence of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra) in Campeche, Mexico. We observed 32 adult females and 35 infants belonging to 14 groups of black howlers for a total of 2,224 focal hours. We found that lactating females spent more time being inactive and feeding from fruits than nonlactating females. In addition, during the first two-thirds of lactation females were more active (i.e., rested less, fed more, devoted more time to social activities, and moved more) and foraged more intensively (i.e., ranged over larger distances, used more feeding trees and feeding species, and consumed more leaves) than females in the last third of lactation. Lactation seems to force black howler females to reduce activity and to maximize the intake of high-quality foods, with inactivity being the highest during late lactation, when females probably face the cumulative effects of nursing older infants and of a new pregnancy. Early lactation is probably the most energetically demanding stage of lactation for black howler females. This study demonstrates that despite being energetically constrained by a highly folivorous diet, reproductive state affects several dimensions of the behavior of black howler females. Therefore, variation in time-budgets and foraging strategies of howlers has been probably underestimated by previous research that has not considered physiological differences among individuals.

Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in Northern Argentina.

A population of black and gold howler monkeys (Alouatta caraya) living near the southern limit of its distribution in a semideciduous forest located in northern Argentina was studied in 2003 to evaluate the possible effects of habitat fragmentation - owing to logging - on its density and social organization within it. Aerial photographs taken in 1982, 1992, and 2001 were used to compare maps of vegetation. These maps were used to evaluate changes in the area covered by forest fragments. From March to June 2003, 10-day monthly surveys of howlers were made in each fragment. A total of 232 individual howlers were counted, belonging to 34 groups plus a solitary adult female. Groups ranged from 2 to 19 individuals (mean = 6.82, SD = 4.23), and 21% of the groups contained more than one adult male. Adults accounted for 55% of the individuals, immatures for 45%, and infants represented 13% of the total. Data obtained were compared with information available for the same population for 1982 and 1995. Results revealed no significant changes in the area of fragments, the crude and ecological density of howlers, and group composition. Group sizes and group composition of howlers suggest that the population remained stable over the past 22 years. The density, number of groups, and individuals appears not to be affected by fragmentation and logging, but crude density was low compared with other less-disturbed habitats. The status of the population remains uncertain owing to isolation, and because there are no protected areas to ensure its stability for the future.

Group size in folivorous primates: ecological constraints and the possible influence of social factors.

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobus's home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobus's home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.

Primates as pets in Mexico City: an assessment of the species involved, source of origin, and general aspects of treatment.

The large human populations in cities are an important source of demand for wildlife pets, including primates, and not much is known about the primate species involved in terms of their general origin, the length of time they are kept as pets, and some of the maintenance problems encountered with their use as pets. We report the results of a survey conducted in Mexico City among primate pet owners, which was aimed at providing some of the above information. We used an ethnographic approach, and pet owners were treated as informants to gain their trust so that we could enter their homes and learn about the life of their primate pets. We surveyed 179 owners of primate pets, which included 12 primate species. Of these, three were native species (Ateles geoffroyi, Alouatta pigra, and A. palliata). The rest were other neotropical primate species not native to Mexico, and some paleotropical species. Spider monkeys and two species of howler monkeys native to Mexico accounted for 67% and 15%, respectively, of the primate cases investigated. The most expensive primate pets were those imported from abroad, while the least expensive were the Mexican species. About 45% of the native primate pets were obtained by their owners in a large market in Mexico City, and the rest were obtained in southern Mexico. Although they can provide companionship for children and adults, primate pets are subject to a number of hazards, some of which put their lives at risk. The demand by city dwellers for primate pets, along with habitat destruction and fragmentation, exerts a significant pressure on wild populations in southern Mexico.

Social organization and food resources availability in primates: a socio-bioenergetic analysis of diet and disease hypotheses.

Data obtained during a field study of two species of nonhuman primates (Alouatta villosa and Ateles geoffroyi) living in the Tikal National Park in Guatemala are used to suggest an answer to the question: To what extent is the existence of a particular form of social organization (group size, structure, and composition) an indication of the amount of energy in the form of food resources available to animals in a particular habitat? Seven researchers working in teams spent 2,318 hours in the field, 1,145 hours of which were in contact with the monkeys. Comparisons of dietary data, estimated energy expenditures, and habitat productivity provide indications of the degree to which a habitat is capable of supporting the energy and other nutritional requirements of howler and spider monkeys living within the study area. These data suggest that much larger populations and different forms of social organizations can be supported by resources available within the habitat.