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.

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.

Flower consumption, ambient temperature and rainfall modulate drinking behavior in a folivorous-frugivorous arboreal mammal.

Water is vital for the survival of any species because of its key role in most physiological processes. However, little is known about the non-food-related water sources exploited by arboreal mammals, the seasonality of their drinking behavior and its potential drivers, including diet composition, temperature, and rainfall. We investigated this subject in 14 wild groups of brown howler monkeys (Alouatta guariba clamitans) inhabiting small, medium, and large Atlantic Forest fragments in southern Brazil. We found a wide variation in the mean rate of drinking among groups (range = 0-16 records/day). Streams (44% of 1,258 records) and treeholes (26%) were the major types of water sources, followed by bromeliads in the canopy (16%), pools (11%), and rivers (3%). The type of source influenced whether howlers used a hand to access the water or not. Drinking tended to be evenly distributed throughout the year, except for a slightly lower number of records in the spring than in the other seasons, but it was unevenly distributed during the day. It increased in the afternoon in all groups, particularly during temperature peaks around 15:00 and 17:00. We found via generalized linear mixed modelling that the daily frequency of drinking was mainly influenced negatively by flower consumption and positively by weekly rainfall and ambient temperature, whereas fragment size and the consumption of fruit and leaves played negligible roles. Overall, we confirm the importance of preformed water in flowers to satisfy the howler's water needs, whereas the influence of the climatic variables is compatible with the 'thermoregulation/dehydration-avoiding hypothesis'. In sum, we found that irrespective of habitat characteristics, brown howlers seem to seek a positive water balance by complementing the water present in the diet with drinking water, even when it is associated with a high predation risk in terrestrial sources.

Salivary tannin-binding proteins are a pervasive strategy used by the folivorous/frugivorous black howler monkey.

Dietary tannins can affect protein digestion and absorption, be toxic, and influence food selection by being astringent and bitter tasting. Animals that usually ingest tannins may regularly secrete tannin-binding salivary proteins (TBSPs) to counteract the negative effects of tannins or TBSPs production can be induced by a tannin-rich diet. In the wild, many primates regularly eat a diet that contains tannin-rich leaves and unripe fruit and it has been speculated that they have the physiological ability to cope with dietary tannins; however, details of their strategy remains unclear. Our research details the salivary protein composition of wild and zoo-living black howler monkeys (Alouatta pigra) feeding on natural versus manufactured low-tannin diets, and examines differences in TBSPs, mainly proline-rich proteins (PRPs), to determine whether production of these proteins is dependent on the tannin content of their food. We measured the pH, flow rate, and concentration of total protein and trichloroacetic acid soluble proteins (an index of PRPs) in saliva. Howler monkeys produced slightly alkaline saliva that may aid in the binding interaction between tannin and salivary proteins. We used gel electrophoresis to describe the salivary protein profile and this analysis along with a tannin-binding assay allowed us to detect several TBSPs in all individuals. We found no differences in the characteristics of saliva between wild and zoo-living monkeys. Our results suggest that black howler monkeys always secrete TBSPs even when fed on foods low in tannins. This strategy of constantly using this salivary anti-tannin defense enables them to obtain nutrients from plants that sometimes contain high levels of tannins and may help immediately to overcome the astringent sensation of their food allowing howler monkeys to eat tanniferous plants.

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.

Oxygen isotope values in bone carbonate and collagen are consistently offset for New World monkeys.

Stable oxygen isotopes are increasingly used in ecological research. Here, I present oxygen isotope (δ(18)O) values for bone carbonate and collagen from howler monkeys (Alouatta palliata), spider monkeys (Ateles geoffroyi) and capuchins (Cebus capucinus) from three localities in Costa Rica. There are apparent differences in δ(18)Ocarbonate and δ(18)Ocollagen among species. Monkeys from moist forest have significantly lower isotope values than those from drier localities. Because patterns are similar for both substrates, discrimination (Δ) between δ(18)Ocarbonate and δ(18)Ocollagen is relatively consistent among species and localities (17.6 ± 0.9‰). Although this value is larger than that previously obtained for laboratory rats, consistency among species and localities suggests it can be used to compare δ(18)Ocarbonate and δ(18)Ocollagen for monkeys, and potentially other medium-bodied mammals. Establishing discrimination for oxygen between these substrates for wild monkeys provides a foundation for future environmental and ecological research on modern and ancient organisms.

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

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

Traditional nutritional analyses of figs overestimates intake of most nutrient fractions: a study of ficus perforata consumed by howler monkeys (Alouatta palliata mexicana).

There continue to remain uncertainty concerning the nutritional importance of figs (Ficus spp.) in the primate diet. Although studies have been performed on the nutritional analysis of fig pulp and seed fractions separately, there has not been an attempt to quantify the contribution of animal matter within figs. Here we report nutritional values of figs (Ficus perforata) (Urostigma) consumed by a troop of howler monkeys (Alouatta palliata mexicana). Separate nutritional assays were performed on the pulp, seed, and animal fraction. Whole-fig analyses significantly exaggerate the concentrations of all nutrients (lipids especially) as seeds, which represent a large proportion of the fig (45%), cannot be digested. Animal matter only represents 1% of the fig, and augments fig protein and lipid content by 0.44 and 0.30%, respectively. This represents the 11 and 9% of the fraction available for digestion. Differences in fig consumption were observed between age and sex classes (P=0.04) and periods of the day (P=0.001); females consumed more figs than males and the highest consumption of figs was observed in the afternoon. F. perforata figs may be an important component of the howler monkeys diet owing to their high content of water and calcium.

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.

Behavior and endocrine concentrations do not distinguish sex in monomorphic juvenile howlers (Alouatta palliata).

Behavioral observations on juvenile mantled howlers are limited by visually undifferentiated genitalia; however, animals can be sexed when they are very young or if they are captured. Behavioral data and fecal samples from juveniles during month-long field studies from 1993 to 1995 were analyzed to determine whether there are developmental differences in behavior or hormone concentrations that can be used to differentiate males from females. The subjects were juveniles of known sex and age from five different social groups on Hacienda La Pacifica, Costa Rica. Based on 749.8 hr of focal-animal sampling, there were no sex differences in daily activity patterns. There were no sex differences in proximity to mothers and other group members, and age differences reflected howler life-history patterns. There were no differences in estradiol or testosterone concentration by age or sex. Juvenile monomorphy thus extends beyond morphology to behavioral and hormonal similarity as well. Most juveniles are forced out of their natal groups and remain solitary until they join new groups by supplanting all same-sex adult group members. Monomorphy may allow them to spend more time in natal groups, and thus both reduce the solitary period and allow the juveniles to improve social skills needed for later immigration. While this strategy may benefit juvenile howlers, it remains a problem for those who wish to study juvenile sex differences from a distance.

Phenotypic diversity of the cellular 1,25-dihydroxyvitamin D3-receptor interaction among different genera of New World primates.

High serum of 1,25-dihydroxyvitamin D3 [1,25-(OH)2D3] concentrations and target organ resistance to the hormone are characteristic findings in some New World primates (platyrrhines). We examined the abilities of cultural dermal fibroblasts from individual platyrrhines of four different genera, Aotus, Alouatta, Pithecia, and Saguinus, to internalize and respond to 1,25-(OH)2D3 in an attempt to identify possible phenotypic heterogeneity in the 1,25-(OH)2D3-receptor interaction among them. Results were compared to those from two Old World primates (catarrhines), Pan troglodytes and Pongo pygmaeus. Compared to catarrhine cells, cells from Alouatta, Pithecia, and Saguinus demonstrated 1) a 10-fold decrease in [3H] 1,25-(OH)2D3 internalization capacity; 2) a 2- to 5-fold increase in the apparent internalization constant [3H]1,25-(OH)2D3; and 3) a 3- to 15-fold increase in the 1,25-(OH)2D3 concentration required to elicit half-maximal induction of [3H]25-hydroxyvitamin D3-24-hydroxylating activity (ED50; rank order Sanguinus much greater than Pithecia greater than Alouatta). Although the internalization capacity of cells from two different primates in the genus Aotus was 3- to 4-fold lower than that in catarrhine cells, the internalization constant for hormone and ED50 for 24-hydroxylating activity were similar. These data suggest that the functional 1,25-(OH)2D3-receptor phenotype of the owl monkey, Aotus trivirgatus, is more closely aligned to the catarrhine phenotype than are those of other platyrrhines in the families Cebidae and Callitricidae.

Rates of fermentative digestion in the howler monkey, Alouatta palliata (primates: ceboidea).

1. Caecal material of wild howler monkeys was analyzed by gas chromatography for evidence of fermentation activity and rates of production and absorption of volatile fatty acids. 2. Results showed a high rate of production of acetic acid and lesser production of propionic, butyric and isobutyric acids. The VFA content of the blood was increase in passage through the caecal vascular system. 3. We estimate that howler monkeys may obtain as much as 31% of their required daily energy from fermentation end products. 4. Energy rich fatty acids may be of particular importance to howlers when they are living on diets high in leaves, which have high cell wall contents and low contents of nonstructural carbohydrates.