Female reproductive energetics in mantled howler monkeys (Alouatta palliata): A follow-up study.

OBJECTIVE: Reproduction entails several challenges to primate females, among which energetic costs are remarkable at certain stages of the reproductive cycle. Still, females may use behavioral and physiological strategies to cope with those challenges. We had previously reported covariation between female energetic condition through the reproductive cycle and time-budget adjustments in mantled howler monkeys (Alouatta palliata). Accordingly, we suggested that behavioral flexibility allowed coping with the energetic challenges of reproduction. Subsequent evidence from the same population, however, suggested otherwise, so we performed a follow-up study on the variation in female reproductive energetics based on a larger sample of females. METHODS: We studied 48 free-ranging adult females at Los Tuxtlas (Mexico). We assessed energy balance via urinary C-peptide concentrations (2717 urine samples), behavioral energy intake and expenditure (5728 sampling hours), and physiological energy expenditure via fecal triiodothyronine metabolites (fTH3; 3138 fecal samples). RESULTS: We found that energy balance varied among reproductive states: (a) cycling was a period of low C-peptide concentrations; (b) the highest C-peptide concentrations occurred during gestation; and (c) the beginning of lactation marked a notable decrease in C-peptide concentrations, which then improved at mid-lactation to again decline at lactation offset. These peaks and valleys in energy balance did not seem to be associated with variation in energy acquisition but were rather mirrored by activity levels and fTH3 during lactation. DISCUSSION: Energy balance was not preserved through the reproductive cycle, supporting previous contentions that the reproductive performance of female mantled howler monkeys may be energetically constrained. The contrast between these and results that we have previously reported, highlights the importance of conducting follow-up studies to continually improve our understanding of the reproductive energetics of primate females.

Vocal and movement responses of mantled howler monkeys (Alouatta palliata) to natural loud calls from neighbors.

Loud calls (i.e., long-range acoustic signals) regulate resource competition among neighboring groups of conspecifics in several nonhuman primate species. Ultimate explanations for primate loud calls include mate, offspring, and food defense. Additionally, loud calls may provide valuable information pertaining to the identity and health status of callers, their competitive abilities, and their spatial location. The loud calls of howler monkeys (Alouatta) have been thoroughly studied and seem to play an important function in the defense of valuable resources in a variety of socioecological contexts. Here, we examined whether the behavioral responses of mantled howler monkeys (Alouatta palliata) to natural loud calls from neighbors are linked to three factors: food availability, familiarity, and distance between groups. We studied three groups of mantled howler monkeys at La Flor de Catemaco (Los Tuxtlas, Mexico) for 15 months (1817 observation hours), during which we recorded 236 neighbor loud calls. Food availability per se did not influence the behavior of groups receiving loud calls, although males produced longer vocal responses toward unfamiliar neighbors when food availability decreased. Groups vocalized quicker and both vocalized and moved for longer after loud calls from unfamiliar neighbors. Additionally, groups vocalized and moved for longer at shorter distances from unfamiliar neighbors compared with familiar neighbors. Finally, groups usually moved away from calling neighbors that were closer. These results indicate that the behavioral responses of mantled howler monkeys to loud calls from neighbor groups are associated with the integration of information pertaining to caller identity as well as to their ecological and spatial context.

Isotopic niche partitioning in two sympatric howler monkey species.

OBJECTIVES: Ecological similarity between species can lead to interspecific trophic competition. However, when ecologically similar species coexist, they may differ in foraging strategies and habitat use, which can lead to niche partitioning. As the body tissues of consumers contain a stable isotope signature that reflects the isotopic composition of their diet, stable isotope analysis is a useful tool to study feeding behavior. We measured the isotopic niche width, which is a proxy for trophic niche width, of mantled (Alouatta palliata) and black (A. pigra) howler monkeys. Specifically, studied populations in allopatry and sympatry to assess whether these species showed niche partitioning. MATERIALS AND METHODS: Between 2008 and 2012, we collected hair samples from 200 subjects (113 black and 87 mantled howler monkeys) and used continuous flow isotope ratio mass spectrometry to estimate δ13 C and δ15 N. We described the isotopic niche width of each species in allopatry and sympatry with the Bayesian estimation of the standard ellipse areas. RESULTS: In allopatry, isotopic niche width and isotopic variation were similar in both species. In sympatry, black howler monkeys had a significantly broader isotopic niche, which was mainly determined by high δ15 N values, and included the majority of mantled howler monkeys' isotopic niche. The isotopic niche of mantled howler monkeys did not differ between sympatry and allopatry. CONCLUSIONS: The coexistence of these ecologically similar species may be linked to trophic niche adjustments by one species, although the particular features of such adjustments (e.g., dietary, spatial, or sensory partitioning) remain to be addressed.

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.

SEROLOGIC SURVEY OF LEPTOSPIRA SPP. IN CAPTIVE ANIMALS FROM VERACRUZ, MEXICO.

Leptospirosis is the most common zoonotic disease worldwide and is considered endemic in countries with tropical climates. It is caused by 10 species of the Leptospira genus and by more than 275 serovars which can affect a wide range of vertebrates. In the Americas, 122 species of four classes of vertebrates have been reported to be infected or exposed to many Leptospira species. Many of these reports are from zoos and rehabilitation centers. Mexico has one single study that reported antibody titers against Leptospira in zoo animals. The purpose of this research was to identify the degree of exposure of some captive mammals and reptiles in Veracruz, a Mexican state with endemic leptospirosis, through microagglutination using 14 live strains of five Leptospira species. Sera samples were collected from 55 animals of 11 species from two classes (Mammalia and Reptilia), four orders (Primates, Artiodactyla, Carnivora, Crocodilia), and nine genera. The more prevalent serovars were Icterohaemorrhagiae and Tarassovi and the highest titers were reactive to the serovar Icterohaemorrhagiae with a value of 1: 51,200.

Maternal condition and maternal investment during lactation in mantled howler monkeys.

OBJECTIVES: Lactation is a costly reproductive state for females, as it may entail decreased body condition, increased morbidity, and increased mortality risk. To offset these costs, mothers should allocate investment in infant care as a function of their physical condition. Here, we assessed the relationship between maternal condition and maternal investment in wild mantled howler monkeys (Alouatta palliata) to determine: (1) whether maternal physical condition varied as a function of food availability, activity levels and feeding effort throughout lactation; (2) whether maternal investment was affected by maternal condition and offspring age. MATERIALS AND METHODS: We studied six adult females while rearing their immature offspring. We determined weekly food availability, C-peptide levels (as a measure of energy balance) in urine samples (306 samples), mothers' time budgets, feeding rates, time spent vigilant, and time spent carrying their offspring (for two years; 600 observation hours). RESULTS: C-peptide levels were positively related to food availability. Maternal care in terms of vigilance and offspring carrying peaked at early lactation and decreased progressively with offspring age. Carrying was positively related to C-peptide levels and was also influenced by variation in maternal condition throughout lactation. DISCUSSION: These results converge with previous theoretical and empirical studies on this topic and contribute to the growing evidence that nonhuman primate mothers allocate maternal care based on their current condition to maximize lifetime reproductive success.

Alouatta pigra males ignore A. palliata loud calls: A case of failed rival recognition?

OBJECTIVES: When closely related species overlap geographically, selection may favor species-specific mate recognition traits to avoid hybridization costs. Conversely, the need to recognize potential same-sex rivals may select for lower specificity, creating the possibility that selection in one domain constrains evolution in the other. Despite a wealth of data on mate recognition, studies addressing rival recognition between hybridizing species are limited to a few bird species. Using naïve populations, we examine the extent to which failed rival recognition might have affected hybridization patterns when two species of howler monkeys (Alouatta pigra and A. palliata) first met after diverging in allopatry. METHODS: We simulated first contact between naïve subjects using playback experiments in allopatric populations of the two purebred species. Using linear mixed models, we compared their look, move, and vocal responses to conspecific and heterospecific loud calls. RESULTS: Although not different in overall response strength to playbacks, the two species differed in reaction to heterospecific callers. Male A. pigra ignored calls from male A. palliata, but the reverse was not true. DISCUSSION: Despite striking differences in vocalizations, A. palliata respond equally to calls from both species whereas A. pigra respond only to conspecifics. This apparent failure of A. pigra males to recognize interspecific rivals might have biased hybridization (F1 hybrids = male A. palliata x female A. pigra), a pattern previously hypothesized based on genetic analysis of hybrids. Given that A. pigra males could be losing reproductive opportunities to heterospecific males, our findings add to growing evidence of potential costs for overly specific species recognition.

Energetic constraints on the reproduction of female mantled howlers.

The reproductive process of female primates is energetically constrained. However, while there is extensive evidence about factors that influence the maintenance of gestation and lactation, less is known about energetic correlates of cycling and the occurrence of conception in wild primates. We examined how female physical condition affected the occurrence of conception and interbirth intervals (IBI) in female mantled howler monkeys, a species in which females experience long non-conceptive periods. For 6 years we followed 7 females at La Flor de Catemaco (Los Tuxtlas, Mexico). In addition to noting the presence of dependent immatures, we collected fecal samples that were analyzed for thyroid hormone and glucocorticoid metabolite concentrations (N = 1,460). Conception was more likely following months when females were not lactating and had higher thyroid hormone and lower glucocorticoid levels. IBIs were shorter when females had higher thyroid hormone and lower glucocorticoid levels, and when the infant at the beginning of the interval died. Due to their obvious impact on female fecundity and fertility, gestation and lactation are the stages of the reproductive process that have traditionally received more attention in studies of female reproductive performance. Still, the cycling stage accounts for a large proportion of IBIs in many primate species. Here we demonstrate that the reproductive rates of female mantled howler monkeys are energetically constrained: both the occurrence of conception and IBI are positively affected by female energetic condition.

Diel and infradian (7-day) activity rhythms in Mexican spider monkeys (Ateles geoffroyi) kept with and without visitor contact.

Diel activity rhythms in mammals are regulated by an endogenous (circadian) timing system which is synchronized by environmental 24-hr periodicities called zeitgebers. Additional direct responses to stochastic environmental factors ensure the fine-tuning to the actual situation and may mask the circadian time course. Following an observational study on behavioral effects of visitor activities in a group of spider monkeys (Ateles geoffroyi) kept free-ranging on a small island of Lake Catemaco, Veracruz, Mexico, we analyzed the effect of weekly varying numbers of visiting tourist boats on the monkeys' diel activity rhythm. With small accelerometer-data logger devices we recorded the monkeys' locomotor activity continuously for several months each. Then we compared the data with those from spider monkeys living without tourist contact. Neither the duration of the monkeys' activity time (α) nor its phase relationship to the 24-hr solar day did change on different weekdays in either site. However, their activity level showed a clear 7-day rhythm. The monkeys of the tourist site showed highest activity on Saturday and Sunday, when the frequency of visiting tourist boats was highest, whereas those of the non-tourist site were least active on Sunday and Monday, when human activities were lowest there. While the monkeys of the non-tourist site usually displayed a distinct bimodal activity pattern peaking in the morning and late afternoon, the pattern in those of the tourist site mostly lacked a morning peak and varied more over time. Based on our results, we suggest that circadian entrainment is not involved in the differences between the diel activity rhythms of the spider monkeys from the two keeping sites and the differing 7-day variation in their activity level. Rather, these differences seemingly reflect direct responses to the differing human activities and thus may correspond to circadian masking effects.

The Influence of Leaf Consumption on Time Allocation in Black Howler Monkeys (Alouatta pigra).

The analysis of factors that determine variation in time budgets is important to understand the interactions between environment, behaviour and fitness. We tested the hypothesis that changes in the dietary patterns of black howler monkeys (Alouatta pigra) caused by a decrease in the availability of preferred foods are a main determinant of variation in time budgets. We predicted that individuals would trade off travel time for resting time (i.e., minimize energy expenditure) as the diet included more leaves. We conducted our study in the Mexican state of Campeche between 2005 and 2008, where we studied the behaviour of 28 adult males and 32 adult females belonging to 14 different groups for a total of 3,747.2 focal sampling hours. Study groups lived in forest fragments with variation in habitat quality. Individuals showed different rest:travel trade-offs in response to leaf consumption according to the quality of the forest fragments they lived in. Individuals that lived in high-quality fragments increased resting time under more folivorous regimes, whereas those living in low-quality fragments increased travel time. Our results suggest that howler monkeys living in low-quality fragments spend more time foraging to compensate for the low quality of the available resources.

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.

Visitor effect on the behavior of a group of spider monkeys (Ateles geoffroyi) maintained at an island in Lake Catemaco, Veracruz/Mexico.

We analyzed the effect of human visitors on the behavior of a group of spider monkeys (Ateles geoffroyi) kept on a small tourist island. Although the spider monkey is a common species in zoos, there are very few specific studies on visitor effects on these monkeys. We conducted behavioral observations on the group of spider monkeys to evaluate the effect of visitors. We also used actimetry devices to measure the variations in the spider monkeys' locomotor activity associated with human presence. With regard to the effect on behavior, we found an increase in self-directed behaviors and a decrease in vocalization, both associated with human presence. Moreover, our results suggest that when people feed monkeys, there is an increase in agonistic behaviors. On the other hand, we found that changes in activity levels in response to human presence vary among individuals. We conclude that changes in spider monkeys' behavior could provide evidence of the negative effect of visitors in our study conditions. Although we discuss the differences in activity levels due to differences in social position, further research is required this topic. Our results can be used to inform management plans for this species in captivity. Improving this relationship between humans and non-human primates through tourism education programs would benefit ecotourism and therefore species conservation programs.

Striking differences in the loud calls of howler monkey sister species (Alouatta pigra and A. palliata).

Comparing vocalizations across species is useful for understanding acoustic variation at mechanistic and evolutionary levels. Here, we take advantage of the divergent vocalizations of two closely related howler monkey species (Alouatta pigra and A. palliata) to better understand vocal evolution. In addition to comparing multiple acoustic and temporal features of roars and the calling bouts in which they are produced, we tested several predictions. First, A. pigra should have roars with lower fundamental frequency and lower formant dispersion because they are larger than A. palliata and have a larger hyoid apparatus. Second, A. pigra should have faster calling rates, longer roars, longer bouts, and exaggerated call features linked to vocal effort (e.g., nonlinear phenomena and emphasized frequencies) because they are the more aggressive species during intergroup encounters. We found significant interspecific differences supporting our predictions in every tested parameter of roars and bouts, except for roar duration and barking rate. Stepwise discriminant function analyses identified the best features for differentiating roars (acoustic features: formant dispersion followed by highest frequency; temporal features: longest syllable duration followed by number of syllables). Although resembling each other more than they resemble South American howler monkeys, our comparison revealed striking differences in the vocalizations of the two Mesoamerican species. While we cannot completely rule out the influence of body size or the environmental conditions in which the two species evolved, vocal differences were likely influenced by sexual selection. The exaggerated roars and intense calling patterns in A. pigra seem more suitable for intergroup competition, whereas A. palliata calls may be better suited for mate attraction and competition within groups. With interspecific acoustic differences quantified, we will now be able to examine how vocalizations contribute to the evolutionary dynamics of the A. palliata × A. pigra hybrid zone in southern Mexico. Am. J. Primatol. 78:755-766, 2016. © 2016 Wiley Periodicals, Inc.

Behavioural and Glucocorticoid Responses of a Captive Group of Spider Monkeys to Short-Term Variation in Food Presentation.

The presentation of food may affect feeding competition and the well-being of captive social species. We hypothesized that feeding competition in a captive group of 5 black-handed spider monkeys (Ateles geoffroyi) should increase in response to certain food presentations in terms of size, distribution and quality of food, and that higher feeding competition should lead to an increase in agonism and physiological stress (measured by faecal glucocorticoid metabolites, FGCM) as well as to a decrease in affiliation, proximity among individuals and feeding activity. We used 5 experimental treatments representing different combinations of size, distribution and quality of food. We observed social interactions for 100 h, collected 6,500 proximity and feeding activity records, and gathered 226 faecal samples. When food was clumped, individuals spent less time feeding, and there was also significant individual variation in feeding activity within treatments. FGCM levels were higher when food was clumped. These results are probably linked to an increase in feeding competition when food is concentrated. At least in small groups of spider monkeys, dispersing food in two feeding stations may be sufficient to decrease differences among individuals in priority of access to food resources, hence reducing physiological stress and interindividual differences in feeding activity.

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.

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.

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.

Demography and life-history parameters of mantled howler monkeys at La Flor de Catemaco: 20 years post-translocation.

Translocations usually aim at maintaining and enhancing wild populations. Thus, the long-term monitoring of translocated individuals is critical for assessing translocation success. In this study, we report the demographic and life-history parameters of mantled howler monkeys that were translocated to La Flor de Catemaco (Los Tuxtlas, Mexico) to determine the success of the translocation process. Nine individuals belonging to two social groups living in areas that were going to be destroyed were released into La Flor de Catemaco between 2002 and 2004. Before 2022 there were no resident monkeys at the site. From January 2012 to December 2021, we recorded births, deaths, migrations, and group formation (1535 sampling days). The population grew until reaching 35 mantled howler monkeys. Two new groups including both individuals born at the site and migrants were founded. Mean ± SD group size was 8.1 ± 1.1 individuals. We recorded 42 births and 14 deaths, mostly of young infants (< 6 months of age). We recorded emigrations and immigrations of adult and immature individuals as well as several instances of individuals that remained and reproduced in their natal groups. Mean female age at first birth was 57.8 ± 18.5 months, interbirth intervals were 23.3 ± 11.3 months, and birth rates were 0.5 ± 0.2 births per female per year. The growth and persistence of the groups at the site, as well as similarity in demographic and life-history parameters between this and unmanaged populations, suggest that mantled howler monkeys living at La Flor de Catemaco represent a stable population and thus that this was a successful translocation.

Correlates of hormonal modulation in mantled howler monkey males, Alouatta palliata.

OBJECTIVES: The study of hormone modulation may offer important insight into the responses of individuals to environmental challenges. Here we studied C-peptide, thyroid hormone (T3), glucocorticoid (GC), and testosterone (T) metabolites of mantled howler males to assess: 1) correlations among hormones; 2) individual and temporal variation in hormone concentrations; and 3) the influence of ecological, climatic, behavioral, social, and reproductive factors on hormone variation. METHODS: We studied 10 adult males at La Flor de Catemaco (Mexico) from January 2012 to December 2016. We collected information on food availability; ambient temperature; time budgets; male involvement in mating, agonistic interactions, and interactions with extragroup males. We analyzed C-peptide concentrations in urine samples and T3, GC, and T in fecal samples. RESULTS: C-peptide was negatively correlated with other hormones, whereas T3, GC, and T were positively related. Hormonal variation was unrelated to individual or yearly differences. Food availability was positively related to C-peptide and T3, and negatively related to GC. Involvement in mating was positively related to T3 and T, whereas the rate agonistic interactions was positively related to GC and T. The rate of interactions with extragroup males was positively related to T. When males mated, the increase in C-peptide and the decrease in GC with increasing food availability were less notable. CONCLUSIONS: Hormonal variation in mantled howler monkey males is generally stable, but it is influenced by several factors. Our results offer a broad picture of the hormonal modulation of mantled howler monkey males in response to diverse challenges.

Social modulation of testosterone levels in male black howlers (Alouatta pigra).

The influence of social factors on the modulation of male testosterone levels has been demonstrated among several vertebrate species. In addition to sexual activity, parental care and reproductive competition affect testosterone secretion. We examined variations in testosterone levels among male black howlers (Alouatta pigra) in various social contexts. Fecal samples were collected from nine males living in five different groups in the Mexican state of Campeche. The potential for intragroup and extragroup competition varied among the groups. The number of resident males living in the groups was the only variable that significantly explained variations in testosterone levels. Males living in unimale groups had higher testosterone levels; the highest testosterone levels were recorded for males that had experienced a shift from multimale to unimale group compositions. In this species, the probability of being challenged by extragroup males and evicted from the group during immigration events increases when males live in unimale groups. Therefore, our results suggest that male black howlers respond to competition for group membership by increasing their testosterone levels. In this context, testosterone secretion represents an anticipatory response to reproductive conflicts. Therefore, although males living in unimale groups have exclusive access to females, they face higher physiological costs associated with sustaining high testosterone levels for extended time periods.