Mantled howler monkeys (Alouatta palliata) show no preferential hand use in two self-directed behaviors.

Hand preference is the preferential use of one hand for a single task. Its study provides insight into the neural mechanisms underlying motor skills, perception, and cognitive functions. From a comparative perspective, it also offers a window into evolutionary history, shedding light on whether manual preferences stem from genetics, environmental influences, or a combination of both. However, there is a paucity of information on preferential hand use for several primate taxa. Here we examine hand preference for the first time in mantled howler monkeys (Alouatta palliata) to determine if there is preferential hand use at the individual and population level as well as sex differences in hand use. We followed 17 wild adult individuals for 10 months and used focal animal sampling (506 focal samples) to record hand use in two types of self-directed behaviors, touching (1246 events) and scratching (1115 events). According to the binomial tests, four individuals were right-hand-preferent, two were left-hand-preferent, and 11 were ambilateral during touching, whereas for scratching seven individuals were right-hand-preferent, two were left-hand-preferent, and eight were ambilateral. At the population level, there was ambilaterality in both behaviors. At the individual level, according to the HI index, hand preference in touching and scratching were not associated and did not vary between sexes. These findings concur with previous studies with howler monkeys and other taxa suggesting that population-level hand preference is not a universal trait across primates.

Leadership and the finder's advantage in mantled howler monkeys.

Leading collective movements and arriving first at feeding sites may improve food acquisition. Specifically, the first individual to discover and exploit a feeding site may gain a feeding advantage known as the "finder's advantage." The aim of this research was to verify if the probability of leading group movements to feeding sites in mantled howler monkeys (Alouatta palliata) varied by sex and reproductive status, and whether finders had higher foraging success than followers. We studied 18 adult individuals from two groups in La Flor de Catemaco over a year (978 h), and sampled group movements (n = 211) and foraging behavior (n = 215 feeding episodes). Gestating females were leaders and finders of group movements to feeding sites more often than expected but were also replaced in the leading position more frequently than individuals of other sex/reproductive states. Feeding behavior was not influenced by the order of arrival at feeding sites per se, but gestating females had higher food intake rate, bite rate, and feeding time when arriving earlier (i.e., occupying front group positions) than later. Therefore, leadership and the finder's advantage occur in this species and are probably employed by gestating females to maintain their energetic condition.

Mantled howler monkey males assess their rivals through formant spacing of long-distance calls.

Formant frequency spacing of long-distance vocalizations is allometrically related to body size and could represent an honest signal of fighting potential. There is, however, only limited evidence that primates use formant spacing to assess the competitive potential of rivals during interactions with extragroup males, a risky context. We hypothesized that if formant spacing of long-distance calls is inversely related to the fighting potential of male mantled howler monkeys (Alouatta palliata), then males should: (1) be more likely and (2) faster to display vocal responses to calling rivals; (3) be more likely and (4) faster to approach calling rivals; and have higher fecal (5) glucocorticoid and (6) testosterone metabolite concentrations in response to rivals calling at intermediate and high formant spacing than to those with low formant spacing. We studied the behavioral responses of 11 adult males to playback experiments of long-distance calls from unknown individuals with low (i.e., emulating large individuals), intermediate, and high (i.e., small individuals) formant spacing (n = 36 experiments). We assayed fecal glucocorticoid and testosterone metabolite concentrations (n = 174). Playbacks always elicited vocal responses, but males responded quicker to intermediate than to low formant spacing playbacks. Low formant spacing calls were less likely to elicit approaches whereas high formant spacing calls resulted in quicker approaches. Males showed stronger hormonal responses to low than to both intermediate and high formant spacing calls. It is possible that males do not escalate conflicts with rivals with low formant spacing calls if these are perceived as large, and against whom winning probabilities should decrease and confrontation costs increase; but are willing to escalate conflicts with rivals of high formant spacing. Formant spacing may therefore be an important signal for rival assessment in this species.

Analytical and biological validation of a noninvasive measurement of glucocorticoid metabolites in feces of Geoffroy's spider monkeys (Ateles geoffroyi).

We report on an analytical and biological validation of a commercial cortisol enzyme immunoassay (EIA) to measure glucocorticoids (GC) in feces of Geoffroy's spider monkeys (Ateles geoffroyi). Validation of endocrinological methods for each sample matrix and study species is crucial to establish that the methods produce reliable results. For the analytical validation of the EIA, we assessed parallelism, accuracy, and precision. We carried out a biological validation based on three well-studied GC patterns with the following predictions: (1) increased fecal GC metabolite (fGCM) concentrations after veterinary intervention; (2) increased fGCM concentrations during early morning hours; and (3) higher fGCM concentrations during gestation than in other female reproductive states. For the first prediction, we sampled feces of two zoo-housed females 2 days before, the day of, and 2 days after a veterinary intervention. For the second prediction, we analyzed 284 fecal samples collected from 12 wild males using a linear mixed model (LMM). For the third prediction, we analyzed 269 fecal samples of eight wild females using an LMM. Analytical validation revealed that the EIA showed parallelism, was accurate, and precise within each assay. However, there was elevated variation in between-assay precision. The biological validation supported all predictions: (1) the two zoo-housed females showed a substantial increase in fGCM concentrations 2.5 and 11 h after veterinary intervention; (2) there was a negative effect of sample collection time on fGCM concentrations (i.e., higher concentrations during early morning); (3) gestating females had significantly higher fGCM concentrations than lactating females. Thus, we analytically validated the commercial EIA and, despite between-assay variation, we were able to find three biologically relevant GC signals in captive and wild settings, and in males and females. We are therefore confident that the method can be used to noninvasively address behavioral endocrinology questions in Geoffroy's spider monkeys.

Noise intensity modulates the responses of mantled howler monkeys to anthropophony.

Anthropogenic noise is a major global pollutant but its effects on primates are poorly understood, limiting our ability to develop mitigation actions that favor their welfare and conservation. In this study, we used an experimental approach to determine the impact of variation in noise intensity on mantled howler monkeys (Alouatta palliata). We conducted the study at Los Tuxtlas (México), where we studied the physiological stress (proxied via fecal glucocorticoid metabolites, fGCM) and behavioral responses of 16 males. We played back chainsaw noise at two intensities (40 and 80 dB) and used days in which groups were not exposed to noise as matched controls. With increased noise intensity fGCM increased, vigilance and vocalizations were longer, and vigilance, vocalizations, and flight occurred quicker. Physiological and behavioral responses occurred even after low-intensity noise playbacks (i.e., 40 dB). Therefore, noise intensity is a significant factor explaining the responses of mantled howler monkeys to anthropogenic noise. These results imply that management actions aimed at eradicating anthropogenic noise are required for the conservation and welfare of mantled howler monkeys at Los Tuxtlas.

Behavioral responses of mantled howler monkeys to neighbor long-distance vocalizations.

OBJECTIVES: Long-distance vocalizations are used by primates in a variety of contexts and may have different functions. The long-distance vocalizations of howler monkeys (Alouatta spp.) underlie the spatial regulation of neighboring groups and could be associated with the defense of food resources. Here, we test the hypothesis that the behavioral responses of mantled howler monkeys (A. palliata) to neighbor long-distance vocalizations are influenced by the potential for range defensibility while accounting for location within the home range and food availability. METHODS: We studied two groups for 13 months and a total of 888 h at La Flor de Catemaco (Mexico). Group 1 had a 92-ha home range and Group 2 had a 24-ha home range. We recorded vocalizations (N = 178 calls) and movements (N = 74 movements) of focal groups following long-distance vocalizations produced by their neighbors. RESULTS: Movement responses, but not vocal responses, were predicted by range defensibility, location, and food availability. As predicted, the group living in the smaller and more defendable range showed stronger movement responses than the group in the larger home range. These movement responses had a shorter latency and longer duration in more valuable spatial and temporal contexts (i.e., the core area and during periods of low food availability). CONCLUSIONS: These results suggest that the tradeoff between the costs and benefits of range defense varies according to the interactions between home range size and both the spatial (core areas) and temporal (food availability) abundance of resources. Thus, the responses of mantled howler monkeys to neighbor long-distance vocalizations could be related to home range defensibility.

Dog barks influence the physiological stress and behavior of a wild primate.

Non-lethal impacts of dogs on primates have seldom been assessed. We used an experimental approach to determine if mantled howler monkeys (Alouatta palliata) perceive dog barks as an aversive stimulus and thus display physiological and behavioral responses toward simulated barks. For one year (1754 h of observations) we studied 16 adult males belonging to five groups in Los Tuxtlas (Mexico), and recorded the occurrence of naturally occurring dog barks, their sound pressure level (SPL), and the behavioral responses of howler monkeys to barks. We then exposed males to bark playbacks at two SPL treatments, 40 and 80 dB in a total of 50 experiments. We assayed glucocorticoid metabolite concentrations in fecal samples (fGCM) as a marker of the physiological stress response of males. We also recorded the duration of vigilance, vocalizations, and flight in relation to playbacks. Naturally occurring barks were frequent and usually elicited behavioral responses by males. fGCM concentrations increased after bark playbacks and with stimuli intensity. Time spent vigilant increased following playbacks independently of stimuli intensity but both vocalizations and flight were linked to stimuli intensity: vocalizations were the longest after barks played-back at 80 dB, but males spent more time fleeing in response to 40 dB bark playbacks. These results provide evidence that dog barks are pervasive in the habitat of mantled howler monkeys living at Los Tuxtlas and disturb males, both physiologically and behaviorally. Although the potential costs of physiological and behavioral responses could not be determined, there is sufficient evidence to assume that they do have negative impacts on individuals. Therefore, our study provides avenues for future research on dog-wildlife interactions and valuable information for the design of conservation actions aimed at mitigating the impact of dogs on mantled howler monkeys.

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.

One step forward, two steps backward: The frailty of howler monkey conservation in Los Tuxtlas, Mexico.

Most primate taxa are threatened by extinction and their populations are decreasing. The persistence of primates is thus conditional on conservation actions aimed at protecting them and their habitat. Here, we focus on the conservation of mantled howler monkeys (Alouatta palliata) in the Los Tuxtlas Biosphere Reserve, Mexico. Following the creation of the reserve in 1998, habitat availability and howler monkey abundance increased, suggesting that progress was being made in terms of the conservation of this species. Recent events, however, suggest otherwise, as mantled howler monkey habitat within the biosphere reserve is being disturbed by mining operations endorsed by the Mexican government. We report this case to raise awareness about the challenges for primate and habitat conservation in protected areas.

The influence of anthropogenic noise on the behavior of male mantled howler monkeys.

Anthropogenic noise is increasingly disturbing natural soundscapes and affecting the physiology, behavior, and fitness of wildlife. However, our knowledge about the impact of anthropogenic noise on wild primates is scant. Here, we assess the effects of anthropogenic noise on the behavior of male mantled howler monkeys (Alouatta palliata). Specifically, we describe the types, rates, and sound pressure level (SPL) of anthropogenic noise that occurs in areas inhabited by mantled howler monkeys and determine if the behavioral responses of males to anthropogenic noise are influenced by noise attributes. For 1 year (1753 h), we characterized anthropogenic noise in the Los Tuxtlas Biosphere Reserve (Veracruz, Mexico) and studied the behavior of males belonging to five groups. Anthropogenic noise was common, diverse, and varied among areas in terms of rate, type, and SPL. Males did not display behavioral responses toward most (60%) anthropogenic noises, but were more likely to respond to certain noise types (e.g., aerial traffic) and toward noise with high SPL. Group identity influenced the likelihood of displaying behavioral responses to noise. The most common behavioral responses were vocalizations and vigilance. Males vocalized in response to noise with high SPL, although this relationship depended on group identity. The effect of the number of noises on vocalizations also varied among groups. Males were more likely to display vigilance toward high SPL and infrequent noise, but, again, these relationships varied among groups. In sum, anthropogenic noise is pervasive in areas inhabited by mantled howler monkeys and influences male behavior. Experience and frequency of exposure may modulate the behavioral responses of male mantled howler monkeys to noise and explain the group differences.

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.

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.

Maternal care according to offspring sex and maternal physical condition in mantled howler monkeys (Alouatta palliata).

The Trivers-Willard hypothesis (TWH) posits that maternal care will be biased in favor of the sex that provides the greatest fitness returns per unit of investment, depending on maternal physical condition. Our aim was to examine the TWH in mantled howler monkeys living at Los Tuxtlas (Veracruz, Mexico). The biological attributes of mantled howler monkeys (Alouatta palliata) meet the assumptions of TWH better than those of other explanations, so we expected that females in better physical condition should bias maternal care toward sons, whereas mothers in worse physical condition should bias care toward daughters. Between December 2017 and March 2019, we studied mother-infant interactions in 20 dyads with focal-animal sampling and continuous recording (N = 204 h). We performed genetic analysis to determine offspring sex (N = 7 daughters and 13 sons) and measured C-peptide in urine samples of mothers to assess their physical condition (N = 46 samples). Mothers in better physical condition spent less time in contact with their sons but more time in contact with their daughters. For proximity behavior, mothers in better physical condition spent more time near their sons and less time near their daughters. These results suggest a bias in maternal care towards daughters, contrary to our predictions. In light of current models of maternal investment, our results support that mothers obtain higher fitness returns through daughters.

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.

Factors influencing infant sex ratio in howler monkeys (Alouatta spp.): A literature review and analysis.

OBJECTIVE: Frequency-dependent selection is expected to maintain infant sex ratios around parity over evolutionary time. However, over ecological time periods, infant sex ratios vary, and it has been proposed that this variation may reflect adaptive processes. In primates, there are consistent patterns of variation in infant sex ratios, although their adaptive significance remains contentious. In addition to design issues, contrasting results could have derived across primates from variation in the fitness benefits accrued through sons or daughters associated with the specific social, ecological, and demographic context of populations. Thus, different sex allocation tactics could occur within species over time and space. METHODS: We reviewed the literature to describe variation in infant sex ratio in howler monkeys (genus Alouatta) and to examine whether such a variation could be associated with adaptive sex allocation. We found 26 studies that provided data for this review. These studies yielded 96 infant sex reports, corresponding to 1,477 sexed infants. RESULTS: Infant sex ratio across howler monkey species tends to parity, but females produce more sons under high group densities and more daughters when rainfall increases. DISCUSSION: Based on these results, as well as on information on howler monkey dispersal patterns, demography, and within-group genetic relatedness, we speculate that, depending on population growth stage, sex allocation is explained by (a) local resource enhancement, that is, more cooperative philopatric daughters are produced when populations are growing; and (b) local resource competition, that is, more dispersing sons are produced when populations are saturated. Thus, there is evidence suggestive of adaptive variation in infant sex ratios in howler monkeys.

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.

Reduced Introgression of Sex Chromosome Markers in the Mexican Howler Monkey (Alouatta palliata × A. pigra) Hybrid Zone.

Interspecific hybridization allows the introgression or movement of alleles from one genome to another. While some genomic regions freely exchange alleles during hybridization, loci associated with reproductive isolation do not intermix. In many model organisms, the X chromosome displays limited introgression compared to autosomes owing to the presence of multiple loci associated with hybrid sterility or inviability (the "large X-effect"). Similarly, if hybrids are produced, the heterogametic sex is usually inviable or sterile, a pattern known as Haldane's rule. We analyzed the patterns of introgression of genetic markers located in the mitochondrial (control region) and nuclear (autosomal microsatellites and sex chromosome genes) genomes of two howler monkey species (Alouatta palliata and A. pigra) that form a natural hybrid zone in southern Mexico, to evaluate whether the large X-effect and Haldane's rule affect the outcomes of hybridization between these sister species. To identify the level of admixture of each individual in the hybrid zone (N = 254) we analyzed individuals sampled outside the hybrid zone (109 A. pigra and 39 A. palliata) to determine allele frequencies of parental species and estimated a hybrid index based on nuclear markers. We then performed a cline analysis using individuals in the hybrid zone to determine patterns of introgression for each locus. Our analyses show that although the hybrid zone is bimodal (with no known F1 s and few recent generation hybrids) and quite narrow, there has been extensive introgression in both directions, and there is a large array of admixed individuals in the hybrid zone. Mitochondrial and most autosomal markers showed bidirectional introgression, but some had biased introgression toward one species or the other. All markers on the sex chromosomes and a few autosomal markers showed highly restricted introgression. This pattern is consistent with the hypothesis that the sex chromosomes make a disproportionate contribution to reproductive isolation, and our results broaden the taxonomic representation of these patterns across animal taxa.

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.

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.