Ariadna Rangel-Negrín

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.

Diets of Howler Monkeys

Based on a bibliographical review, we examined the diets of howler monkeys to compile a comprehensive overview of their food resources and document dietary diversity. Additionally, we analyzed the effects of rainfall, group size, and forest size on dietary variation. Howlers eat nearly all available plant parts in their habitats. Time dedicated to the consumption of different food types varies among species and populations, such that feeding behavior can range from high folivory to high frugivory. Overall, howlers were found to use at least 1,165 plant species, belonging to 479 genera and 111 families as food sources. Similarity in the use of plant taxa as food sources (assessed with the Jaccard index) is higher within than between howler species, although variation in similarity is higher within species. Rainfall patterns, group size, and forest size affect several dimensions of the dietary habits of howlers, such that, for instance, the degree of frugivory increases with increased rainfall and habitat size, but decreases with increasing group size in groups that live in more productive habitats. Moreover, the range of variation in dietary habits correlates positively with variation in rainfall, suggesting that some howler species are habitat generalists and have more variable diets, whereas others are habitat specialists and tend to concentrate their diets on certain plant parts. Our results highlight the high degree of dietary flexibility demonstrated by the genus Alouatta and provide new insights for future research on howler foraging strategies.

Preliminary evidence of accumulation of stress during translocation in mantled howlers

Translocation—an extensively used conservation tool—is a potentially stressful event, as animals are exposed to multiple stressors and cannot predict or control the changes in their environment. Therefore, it may be expected that during a translocation program stress accumulates and social behavior changes. Here, we present data from a translocation of four adult mantled howlers (Alouatta palliata), which was conducted in southern Veracruz (Mexico). We found that stress (measured in fecal corticosterone) increased during translocation, but that the rate of both affiliative and agonistic interactions remained unchanged. Females showed higher levels of corticosterone than males throughout translocation, although no sex differences were observed in social interactions. Our findings provide a preliminary evidence for accumulation of physiological stress during translocation in primates, and may have implications for decisions concerning releasing practices. Am. J. Primatol. 72:805–810, 2010.© 2010 Wiley‐Liss, Inc.

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.

Primates living outside protected habitats are more stressed: the case of black howler monkeys in the Yucatán Peninsula.

The non-invasive monitoring of glucocorticoid hormones allows for the assessment of the physiological effects of anthropogenic disturbances on wildlife. Variation in glucocorticoid levels of the same species between protected and unprotect areas seldom has been measured, and the available evidence suggests that this relationship may depend on species-specific habitat requirements and biology. In the present study we focused on black howler monkeys (Alouatta pigra), a canopy-dwelling primate species, as a case study to evaluate the physiological consequences of living in unprotected areas, and relate them with intragroup competition and competition with extragroup individuals. From February 2006 to September 2007 we collected 371 fecal samples from 21 adults belonging to five groups (two from protected and three from unprotected areas) in Campeche, Mexico. We recorded agonistic interactions within groups and encounters with other groups (1,200 h of behavioral observations), and determined fecal glucocorticoid metabolite (FGM) concentrations with radioimmunoassays. We used linear mixed models and Akaikes information criterion to choose the best model explaining variation in FGM concentrations between protected and unprotected areas calculated from five categorical variables: habitat type (protected vs. unprotected), participation in agonistic interactions, intergroup encounters, sex and female reproductive state, and season. The best model included habitat type, the interaction between habitat type and agonism, and the interaction between habitat type and season. FGM concentrations were higher in unprotected habitats, particularly when individuals were involved in agonistic interactions; seasonal variation in FGM concentrations was only detected in protected habitats. High FGM concentrations in black howler monkeys living in unprotected habitats are associated with increased within-group food competition and probably associated with exposure to anthropogenic stressors and overall food scarcity. Because persistent high GC levels can be detrimental to health and fitness, populations living in disturbed unprotected areas may not be viable in the long-term.

Transmission Patterns of Pinworms in Two Sympatric Congeneric Primate Species

Understanding pathogen transmission is essential to addressing the dynamics of infectious diseases in animal populations. Directly transmitted parasites spread in host populations via 1) contact with infected individuals and 2) contact with contaminated substrates. Although studies exist that support social or ranging effects on transmission, it is less clear how these factors interact. We test the hypothesis that a combination of social, ranging, diet, and intrinsic factors account for Trypanoxyuris minutus (pinworm) infections in sympatric howler species Alouatta palliata and A. pigra. We collected 211 howler fecal samples from 34 adults living in four groups, two of each species, in Tabasco (Mexico), and calculated pinworm prevalence and eggs per gram of feces (EPG). We followed each group for 80 h to determine ranging, diet, frequency of contact, and conspecific proximity. Prevalence of Trypanoxyurisminutus was high, with 82% of all individuals infected. Logistic modeling indicated that pinworm prevalence was positively associated with proximity and the proportion of group members contacted by focal individuals. Although EPG results should be interpreted cautiously owing to variable egg excretion, this index was also positively associated with proximity and the proportion of group members that were contacted, as well as with dietary diversity and use of non-tree foods. Neither intrinsic factors such as species and sex, nor group and population level variables, such as group and home range size, home range overlap, and intensity of range use, were significant predictors of pinworm infection. We conclude that both sociality and feeding behavior are key factors in infection dynamics of Trypanoxyuris minutus in sympatric Alouatta palliata and A. pigra, confirming that contact with infected conspecifics and contaminated substrates are important mechanisms for directly transmitted parasites.

Behaviour accumulation curves: a method to study the completeness of behavioural repertoires

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Group Structure and Dynamics in Black Howlers (Alouatta pigra): A 7-year Perspective

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

The long-term monitoring of group structure and dynamics is critical to the study of primate ecology and evolutionary processes, as well as to understand the responses of individuals to changes in their environments. We monitored individually recognized black howlers (Alouatta pigra) belonging to 11 groups for 7 yr in different habitats and landscapes in Campeche (Mexico). Our aims were 1) to describe group structure and dynamics; 2) to determine whether group structure and dynamics changed significantly over time; and 3) to evaluate which habitat and landscape-scale attributes best predicted variation among groups in structure and dynamics. Each year we surveyed the groups twice in each climatic season (wet and dry season), resulting in a total of 10,083 sampling days. Although group size increased over time, mostly as a result of moderate to high infant survival rates and increases in the number of juveniles in groups, other demographic parameters, such as the number of adults and infants per group, were stable. We observed no group takeovers involving two or more males and infrequent takeovers by solitary males; frequent disappearances of individuals of both sexes from their natal groups around the age of sexual maturation, suggesting a bisexual dispersal pattern; concentration of births in the wet season; male-biased sex ratios at birth but female-biased immature survival. Group structure and dynamics were affected by both habitat and landscape-scale attributes, but factors acting at the habitat scale had an overall higher impact on demographics. Besides reporting new life history and demographic data for this species, the results from this study suggest that black howlers may be more sensitive to habitat disturbance than previously reported.

Landscape Attributes Affecting the Natural Hybridization of Mexican Howler Monkeys

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. Am. J. Primatol. 76:1151–1162, 2014.