Sex differences in leadership during group movement in mantled howler monkeys (Alouatta palliata).

Benefits of group life depend in large part on whether animals remain cohesive, which often requires collective decisions about where and when to move. During a group movement, the leader may be considered as the individual occupying the vanguard position of the group progression, when its movement evokes following by other group members. In nondespotic societies, individuals with greater incentives to move frequently are leaders. During 15 months of observations (1,712 contact hours), we investigated two mantled howler monkey (Alouatta palliata) groups at La Flor de Catemaco (Los Tuxtlas, Mexico) to examine whether sex and female reproductive state influenced leadership likelihood in two contexts: movements toward feeding trees; movements associated with loud calls, a group-defense behavior used by males of this genus. Females led and occupied forward positions during group movements toward feeding trees more often than adult males. Adult females led these movements more frequently when they were gestating than when they were lactating or cycling. There were no differences between sexes in the leadership of group movements associated with loud calls. Leadership by gestating females is perhaps the result of their higher nutritional/energetic needs when compared with cycling females, and of their greater mobility when compared with lactating females carrying dependent offspring. Female leadership during movements toward feeding trees may be a mechanism to optimize access to food resources in mantled howler monkeys.

Social play among black and gold howler monkey (Alouatta caraya) immatures during intergroup encounters.

We studied intergroup social play (IGSP) among immatures in wild black and gold howler monkeys (Alouatta caraya) in northeastern Argentina. IGSP events are one form of affiliative interaction that can occur during intergroup encounters. The main goal of this study was to analyze IGSP in A. caraya immatures and assess how intrinsic (e.g., age and sex) and extrinsic (e.g., seasonality) factors can influence the development of this type of social behavior. We followed 12 groups between 2008 and 2015 and recorded 182 encounters and 61 events of IGSP. Considering the composition of play partners, most IGSP events occurred among juveniles of both sexes (33%), followed by juveniles that were only-male (31%), and finally between mixed-sex juveniles and infants (20%) interactions. Additionally, most IGSP events occurred mainly in summer (56%), followed by spring (29%), with fewer events occurring in autumn (15%) and no IGSP events recorded in winter. Our results suggest that IGSP constitutes a beneficial activity in wild A. caraya that promotes behavioral flexibility, where immatures acquire social skills, such as tolerance, by interacting with unknown individuals. Moreover, the higher participation of young males in IGSP is consistent with the fact that adult black and gold howler males tend to be more actively involved in group encounters than females, supporting the hypothesis that social play provides benefits in the development of motor and social skills. Finally, seasonality in the frequencies of IGSP might be related to availability of foods with high and easily mobilized energy content in summer and spring.

Hormonal correlates of energetic condition in mantled howler monkeys.

Hormones have a key role in energy allocation, so their study allows understanding individual metabolic strategies. Because different hormones convey different information on the responses of individuals to energetic demands, a simultaneous analysis of variation in multiple hormones may offer a more reliable picture of metabolic strategies than single hormone assessments. In this study we focused on determining which factors were related to variation in fecal glucocorticoid and thyroid hormone metabolites in wild mantled howler monkeys (Alouatta palliata). Over 12months, we determined fecal glucocorticoid and thyroid hormone metabolite levels of 11 adults belonging to two groups, and examined the relationship between hormone metabolites and a variety of behavioral, physiological, and ecological factors (e.g., food intake, sex/reproductive state, activity, participation in agonistic interactions). We found that glucocorticoids were elevated in gestating and lactating females compared to males and cycling females, and were also higher when individuals were more active and participated in agonistic interactions. Thyroid hormone levels were also related to sex/reproductive state and activity, but were additionally positively related to fruit intake and negatively related to young leaf intake. Our study demonstrates that the non-invasive measurement of glucocorticoid and thyroid hormones of howler monkeys allows assessing different underlying physiological processes. By combining different biomarkers, which has seldom been done with wildlife, we could also parse the influence of psychological vs. metabolic challenges for individual energetic condition, which may be instrumental for deciding which factors should be accounted for when studying different hormone-behavior interactions.

Mantled howler monkey spatial foraging decisions reflect spatial and temporal knowledge of resource distributions.

An animal's ability to find and relocate food items is directly related to its survival and reproductive success. This study evaluates how mantled howler monkeys make spatial foraging decisions in the wild. Specifically, discrete choice models and agent-based simulations are used to test whether mantled howler monkeys on Barro Colorado Island, Panama, integrate spatial information in order to maximize new leaf flush and fruit gain while minimizing distance traveled. Several heuristic models of decision making are also tested as possible alternative strategies (movement to core home range areas instead of individual trees, travel along a sensory gradient, movement along arboreal pathway networks without a predetermined destination, straight-line travel in a randomly chosen direction, and random walks). Results indicate that although leaves are the single most abundant item in the mantled howler monkey diet, long-distance travel bouts target the areas with the highest concentrations of mature fruits. Observed travel patterns yielded larger estimated quantities of fruit in shorter distances traveled than all alternative foraging strategies. Thus, this study both provides novel information regarding how primates select travel paths and suggests that a highly folivorous primate integrates knowledge of spatiotemporal resource distributions in highly efficient foraging strategies.

Variation in dietary breadth among groups of black howler monkeys is not associated with the vegetation attributes of forest fragments.

Habitat disturbance alters vegetation structure and composition. For example, in forest fragments, the rate of secondary plant species recruitment and mortality in species typical of old-growth forests are higher. For many arboreal primates, movement between fragments is infrequent and difficult, thus the dietary breadth of herbivorous primates that live in fragments is expected to change. It is likely that the ability of howler monkeys (Alouatta spp.) to live in a large array of habitat types is related to their ability to exploit a broad set of both difficult to digest and high energy resources. However, if small fragments have fewer trees and plant species, food selection by howler monkeys could be limited, which would undermine their persistence. To address this question, we compared the dietary breadth of 14 groups of Yucatán black howler monkeys (Alouatta pigra) living in different fragments, and hypothesized that dietary breadth should be associated to the vegetation attributes of the habitat. We characterized the vegetation structure and composition in each fragment and collected a total of 3,747 focal hr on the feeding behavior of 60 adult individuals. Dietary diversity, both in terms of the rate of plant species used as food sources (plant species used per unit of time) and percentage of ingested food from the top five plant species with overall highest ingestion rate, was not related to vegetation attributes but rather associated with the degree of folivory, such that higher folivory led to more diverse diets. Groups living in fragments with higher tree density used a larger number of trees as food sources. Therefore, black howler monkeys living in small fragments with disturbed vegetation continued to preserve diet diversity, confirming that dietary diversification is an important goal in the foraging strategy of howler monkeys.

When top-down becomes bottom up: behaviour of hyperdense howler monkeys (Alouatta seniculus) trapped on a 0.6 ha island.

Predators are a ubiquitous presence in most natural environments. Opportunities to contrast the behaviour of a species in the presence and absence of predators are thus rare. Here we report on the behaviour of howler monkey groups living under radically different conditions on two land-bridge islands in Lago Guri, Venezuela. One group of 6 adults inhabited a 190-ha island (Danto) where they were exposed to multiple potential predators. This group, the control, occupied a home range of 23 ha and contested access to food resources with neighbouring groups in typical fashion. The second group, containing 6 adults, was isolated on a remote, predator-free 0.6 ha islet (Iguana) offering limited food resources. Howlers living on the large island moved, fed and rested in a coherent group, frequently engaged in affiliative activities, rarely displayed agonistic behaviour and maintained intergroup spacing through howling. In contrast, the howlers on Iguana showed repulsion, as individuals spent most of their time spaced widely around the perimeter of the island. Iguana howlers rarely engaged in affiliative behaviour, often chased or fought with one another and were not observed to howl. These behaviors are interpreted as adjustments to the unrelenting deprivation associated with bottom-up limitation in a predator-free environment.

Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids.

Social differences between primate species may result from both flexible responses to current conditions or fixed differences across taxa, yet we know little about the relative importance of these factors. Here, we take advantage of a naturally occurring hybrid zone in Tabasco, Mexico to characterize the variation in social structure among two endangered howler monkey species, Alouatta pigra and A. palliata, and their hybrids. Work in pure populations has suggested that A. pigra females maintain closer proximity, exhibit higher rates of affiliation, and lower rates of agonism than A. palliata females, but we do not know what accounts for this difference. Using identical data collection and analysis methods across three populations, we first seek to confirm previously reported interspecific differences in social structure across all sexes. We next examine: (1) how female social relationships changed with ancestry (by comparing pure and hybrid individuals); (2) how female social relationships changed with group size (A. pigra have smaller groups than A. palliata); and (3) whether female social relationships differed between two taxonomic groups within a single forest fragment (thus controlling for ecological variation). We confirmed previously described species differences, including closer proximity among females than among males in all populations. We also found that smaller groups maintained closer proximity. However, even after accounting for variation in group size, A. pigra females had closer proximity and more affiliation than A. palliata females. Furthermore, differences between pigra-like and palliata-like hybrids paralleled differences between pure populations and persisted even after controlling for ecological variation. Together, our results suggest that flexibility cannot account for all of the social differences between A. pigra and A. palliata and indicate an important genetic component in primate social behavior.

The effect of energetic and psychosocial stressors on glucocorticoids in mantled howler monkeys (Alouatta palliata).

The proximate causes of variation in glucocorticoids (GCs) of many free-ranging primates are still unclear, and in some cases, the available evidence is contradictory. Such is the case of mantled howler monkeys. In the present study, we tested whether variation in GC levels in this species could be predicted by energetic challenges or by psychosocial stressors. We focused on two groups living in Los Tuxtlas (Veracruz, Mexico) that differed in a number of parameters including: group size, habitat size, number of groups, and solitary males within the same habitat. Furthermore, one of the groups experienced changes in composition during our observations. From March to December 2009 we determined food availability in each group's habitat, studied the behavior of all adult individuals (N = 17), including, feeding, time budgets, ranging, and social interactions (N = 426.6 h), and measured weekly GCs in fecal samples (N = 160 individual/weeks) of both females and males. We found that participation in agonistic interactions, which were more frequent in the group that lived in the smaller habitat, was associated with increased weekly GCs, particularly in pregnant and lactating females. During the dry season weekly GCs were also higher in the group that lived in the smaller habitat. Although in this group individuals significantly increased travel time during the dry season, weekly GC levels were unrelated to time-budgets or ranging distances, contrasting with previous findings on mantled howler monkeys' GC response. We found no evidence that weekly variation in GC levels between groups resulted from differences in food availability. Our results indicate that mantled howler monkey GC levels respond to the effects of agonism, reproductive state, and the influence of a seasonal stressor, which may be attributable to anthropogenic disturbance. We conclude that psychosocial stressors affect the GC response of mantled howler monkeys, and that this response is modulated by reproductive state.

Behavioral and physiological responses to subgroup size and number of people in howler monkeys inhabiting a forest fragment used for nature-based tourism.

Animals' responses to potentially threatening factors can provide important information for their conservation. Group size and human presence are potentially threatening factors to primates inhabiting small reserves used for recreation. We tested these hypotheses by evaluating behavioral and physiological responses in two groups of mantled howler monkeys (Alouatta palliata mexicana) at the "Centro Ecológico y Recreativo El Zapotal", a recreational forest reserve and zoo located in the Mexican state of Chiapas. Both groups presented fission-fusion dynamics, splitting into foraging subgroups which varied in size among, but not within days. Neither subgroup size nor number of people had an effect on fecal cortisol. Out of 16 behavioral response variables tested, the studied factors had effects on six: four were affected by subgroup size and two were affected by number of people. With increasing subgroup size, monkeys increased daily path lengths, rested less, increased foraging effort, and used more plant individuals for feeding. As the number of people increased, monkeys spent more time in lower-quality habitat, and less time engaged in social interactions. Although fecal cortisol levels were not affected by the factors studied, one of the monkey groups had almost twice the level of cortisol compared to the other group. The group with higher cortisol levels also spent significantly more time in the lower-quality habitat, compared to the other group. Our results suggest that particular behavioral adjustments might allow howler monkeys at El Zapotal to avoid physiological stress due to subgroup size and number of people. However, the fact that one of the monkey groups is showing increased cortisol levels may be interpreted as a warning sign, indicating that an adjustment threshold is being reached, at least for part of the howler monkey population in this forest fragment.

Use of space, activity patterns, and foraging behavior of red howler monkeys (Alouatta seniculus) in an Andean forest fragment in Colombia.

Howler monkeys are among the most studied primates in the Neotropics, however, behavioral studies including estimation of food availability in Andean forests are scarce. During 12 months we studied habitat use, behavior, and feeding ecology of two groups of red howler monkeys (Alouatta seniculus) in an isolated fragment in the Colombian Andes. We used a combination of focal animal and instantaneous sampling. We estimated fruit production (FP) using phenology transects, and calculated young leaf abundance by observing marked trees. The home range area used by each group was 10.5 and 16.7 ha and daily distances traveled were 431 ± 228 and 458 ± 259 m, respectively. We found that both groups spent most of their time resting (62-64%). Resting time did not increase with leaf consumption as expected using a strategy of energy minimization. We did not find a relationship between daily distances traveled and leaf consumption. However, howlers consumed fruits according to their availability, and the production of young leaves did not predict feeding time on this resource. Overall, our results are similar to those found on other forest types. We found that despite limited FP in Andean forests, this did not lead to a higher intake of leaves, longer resting periods, or shorter traveling distances for red howlers.

Mating promiscuity and reproductive tactics in female black and gold howler monkeys (Alouatta caraya) inhabiting an island on the Parana river, Argentina.

In several primate species, females mate promiscuously and several adult males peacefully co-reside in the same social group. We investigated female mating behavior in two neighboring multimale-multifemale groups of Alouatta caraya in northern Argentina (27 degrees 20'S-58 degrees 40'W). All adult individuals in each group were marked with identification anklets and ear tags, and followed for five consecutive full days per month during 20 consecutive months. We recorded 219 copulations for eight resident females in these two groups. Thirty-two percent of matings involved extra-group copulations and 68% were with resident males. During periods when females were likely to conceive and during periods when females were nonfertile (pregnancy and lactation), there were no significant differences in the average number of resident and nonresident males with which they copulated (G-test: G(adj)=0.1, df=3, P>0.05). In both of our study groups, adult males were tolerant of the mating activities between resident males and resident females, but acted aggressively and collectively (howling, border vigilance, and fighting) when extragroup males attempted to enter the group and mate with resident females. Given the frequency of extragroup matings, we examined the distance females traveled to engage in these copulations, time engaged in pre- and postcopulatory behavior, and the risk of injury during extragroup copulations. These costs were found to be relatively small. We suggest that female promiscuity is the prime driver or constraint on male reproductive opportunities in this species. Female promiscuity in A. caraya appears to represent a mixed mating strategy that may serve to increase opportunities for genetic diversity between a female's successive offspring as well as minimize the risk of infanticide by spreading paternity estimates across a larger number of adult males.

Sources of variation in fecal cortisol levels in howler monkeys in Belize.

High cortisol levels are known to cause low fecundity and increased mortality; thus, the prospect of using cortisol as a measure of population health is an exciting one. However, because so many factors can interact to influence cortisol release, it can be difficult to interpret what exactly is creating changes to cortisol levels. This study investigates variation in fecal cortisol levels in a population of black howlers (Alouatta pigra) from 350 fecal samples collected from 33 individuals in more than 4 years. A general linear mixed model revealed that cortisol varied significantly with fruit availability and contact with tourists. When fruit availability was low, cortisol increased, likely because when fruit availability is low monkeys eat less fruit, thus obtaining less sugar. This result may simply reflect cortisol's metabolic function of mobilizing glucose. It also indicates that these monkeys may be experiencing periods of food stress throughout the year, which was earlier thought to be minimal for a primarily folivorous species. Presence of tourists was the only other factor found to lead to high cortisol; with exposure to tourists increasing stress levels. These results highlight the importance of understanding how physiological factors can influence cortisol, making it easier to interpret results and determine the external social or ecological stressors that may increase cortisol.

Behavioral effects of introducing pied tamarin (Saguinus bicolor) to black howler monkey (Alouatta caraya) and white-faced saki (Pithecia pithecia) in a zoological park.

Mixed-species primate exhibits are becoming more common in zoological parks as a means to display a diverse array of animals both more naturalistically and with more economy of space. Here, we describe behavioral changes during the introduction process of a pair of pied tamarins (Saguinus bicolor) to an established group of black howler monkeys (Allouatta caraya) and white-faced saki monkeys (Pithecia pithecia). Data were collected during six phases, representing introductions among the various species and to exhibit space and off-exhibit holding. The pied tamarins were consistently the most active of the three species. Although activity levels of the howler and saki monkeys remained constant throughout, that of the tamarins declined as the introduction progressed. Several episodes of aggression between the tamarins and the sakis were observed, but did not coincide with patterns predicted by previous intra-specific introductions. The three-species mix remained stable for several months; however, escalating aggression ultimately led to the removal of the sakis from the mixed-species exhibit. Despite our mixed results, we contend that only through continued trials, coupled with careful and systematic monitoring, can we ultimately identify stable mixes of species.

Glucocorticoid levels in free ranging resident mantled howlers: a study of coping strategies.

A growing amount of data shows that a preference for passive-nonaggressive over active-aggressive problem solving is associated with higher levels of glucocorticoids (GC). For mantled howlers, the arrival of an adult male in a new group is a potential source of psychological stress for both resident males and females. Resident mantled howler males take an active stand and aggressively repel the entrance of solitary males, while females take a passive-nonaggressive stand. In order to study whether the relationship between coping strategies and the activation of the hypothalamic-pituitary-adrenal (HPA) axis observed in other species applies to the response of resident mantled howlers to the presence of solitary males, we examine the relationship between different group and subpopulation variables and the GC levels measured in feces collected from 10 groups living in six forest fragments, in Los Tuxtlas, Mexico. The results of our study suggest that the resident mantled howler females' passive response to the presence of solitary males is accompanied by the activation of the HPA axis, whereas resident males' aggressive response is not accompanied by any changes in the HPA axis. In contrast, a previous study suggests that resident male howlers respond by increasing their testosterone levels to the presence of solitary males (Cristobal-Azkarate et al., Hormones and Behavior 2006;49 261-267). These different behavioral and hormonal responses coincide with the active and passive coping styles described for other species. The conditions in which howlers live in our study area may be favoring the interaction between solitary and resident howlers, and inducing chronically high GC levels, which in turn could negatively affect the fitness of these subpopulations.

Exploring immature-to-mother social distances in Mexican mantled howler monkeys at Los Tuxtlas, Mexico.

We analyzed immature-to-mother social distance (juveniles and non-nursing infants) in two Mexican mantled howler monkey (Alouatta palliata) troops inhabiting a tropical rainforest fragment (40 ha) at Los Tuxtlas, Veracruz, Mexico. During July and August of 2000 and 2001 we applied an instantaneous sampling method (317 hr) to record the behaviors of the immatures and their mothers, as well as distances (ordinal scale) between immatures and their mothers (IMD), and between immatures and nonmother individuals (INMD). Immatures were generally less than 5 m away from any individual of the troop. Social distance was influenced by the different behaviors of both mothers and immatures, with the shortest distances occurring during rest (IMD <5 m in 94% of all instantaneous samples) and the longest during exploration (21% > or =10 m) and play (26% > or =10 m). When IMD increased, we found a higher percentage of records <5 m to other individuals, particularly with the probable father. When the variation in distance to the mother and to other individuals in the troop was considered, the immature animals' distance to other troop members depended on the immatures' age and type of behavior. Overall, these results suggest that in this low-activity species the development of the immature is associated with a complex set of relationships with other troop members.

Ranging pattern and use of space in a group of red howler monkeys (Alouatta seniculus) in a southeastern Colombian rainforest.

We studied a group of red howler monkeys (Alouatta seniculus) bordering a lake in an eastern Colombian Amazon rainforest for 10 months. The group used an area of 182 ha located mainly on Pleistocene terrace forest and had no overlap with other howler home ranges. Home range use varied through the year as a consequence of fruit and leaf abundance. For example, during the fruit scarcity season the group used an area of flooded forest nearly exclusively, indicating that at least for a portion of the year they are habitat specialists. Two areas intensively used by the group were identified, representing 17.6 % of the home range, and within which 56.9 % of the feeding trees were located. Overall density of feeding trees within the group's home range was very low (1.12 trees/ha). Home range size, as well as mean length of daily ranges (1,150 m), is the largest reported for this species to date, and it is likely a consequence of the diminished productivity of the plant communities on poor soil. Our results give an interesting example of the ranging behavior of this primate, which clearly differs from previous descriptions of red howlers.

Behavioral thermoregulation in a sexually and developmentally dichromatic neotropical primate, the black-and-gold howling monkey (Alouatta caraya).

Behavioral thermoregulation in primates may provide a means for the conservation of heat during periods of low ambient temperature and/or food shortage as well as a way to dissipate heat under hot conditions. This article focuses on behavioral thermoregulation in a sexually dichromatic primate, the black-and-gold howling monkey (Alouatta caraya). Two models have been proposed to explain the evolution of sexual dichromatism in this species: thermoregulation and sexual selection. Five hypotheses associated with thermoregulatory behaviors are tested. These are as follows: (1) energy-conserving postures are used mainly under low ambient temperatures; (2) sunny resting places are selected during periods of low temperature; (3) exposure of the less-insulated ventral region to sunlight decreases with increasing temperature; (4) black-colored adult males use energy-conserving postures, sunny places, and exposure of the ventral region to sunlight less frequently than do blonde-colored adult females; and (5) smaller individuals use energy-conserving postures, sunny places, and exposure of the ventral region to sunlight in significantly greater frequency than do larger individuals. Over a 12-month period, behavioral data were collected on a free-ranging habituated group of 15-17 howlers of all age-sex classes. Ambient temperature was measured each hour. The results indicate that during resting, howlers showed a consistent use of heat-conserving postures, showed a preference for sunny places, and exposed their ventral region to sunlight under low ambient temperatures. A preference for shady places, heat-dissipating postures, and exposure of the back were observed under high ambient temperatures. Despite sex differences in adult color patterns and differences in size between age classes, no significant age or sex differences in thermoregulatory behaviors were detected. Failure to confirm a thermoregulation model implies that sexual selection may be responsible for sexual dichromatism in this species.

Feeding ecology of the black howler monkey (Alouatta pigra) in northern Belize.

We studied the feeding ecology of the black howler monkey (Alouatta pigra) from March 1994 to April 1995 in the Community Baboon Sanctuary in northern Belize, Central America. Activity and diet composition were recorded using continuous focal animal sampling. Diet composition was compared with the relative abundance of plant parts eaten by the howlers within the study site. The study animals spent an average of 24.4% of their time feeding, 61.9% resting, and approximately 9.8% traveling. In contrast to previously published reports on A. pigra, we found the diet composition to be similar to that of other Alouatta species (conforming to the folivore/frugivore profile), with 41% of feeding time spent eating fruit, 45% foliage, and 11% flowers. This contrast may indicate a wide degree of dietary flexibility that allows A. pigra to inhabit a variety of habitat types. We suggest that a high level of resource abundance throughout the year makes the Community Baboon Sanctuary excellent habitat for Alouatta pigra.