Domingo Canales-Espinosa

Hybridization in Large-Bodied New World Primates

Well-documented cases of natural hybridization among primates are not common. In New World primates, natural hybridization has been reported only for small-bodied species, but no genotypic data have ever been gathered that confirm these reports. Here we present genetic evidence of hybridization of two large-bodied species of neotropical primates that diverged ∼3 MYA. We used species-diagnostic mitochondrial and microsatellite loci and the Y chromosome Sry gene to determine the hybrid status of 36 individuals collected from an area of sympatry in Tabasco, Mexico. Thirteen individuals were hybrids. We show that hybridization and subsequent backcrosses are directionally biased and that the only likely cross between parental species produces fertile hybrid females, but fails to produce viable or fertile males. This system can be used as a model to study gene interchange between primate species that have not achieved complete reproductive isolation.

Non-invasive measurement of thyroid hormone in feces of a diverse array of avian and mammalian species

We developed and validated a non-invasive thyroid hormone measure in feces of a diverse array of birds and mammals. An I(131) radiolabel ingestion study in domestic dogs coupled with High Pressure Liquid Chromatography (HPLC) analysis, showed that peak excretion in feces occurred at 24-48h post-ingestion, with I(131)-labelled thyroid hormone metabolites excreted primarily as triiodothyronine (T3) and relatively little thyroxine (T4), at all excretion times examined. The immunoreactive T3 profile across these same HPLC fractions closely corresponded with the I(131) radioactive profile. By contrast, the T4 immunoreactive profile was disproportionately high, suggesting that T4 excretion included a high percentage of T4 stores. We optimized and validated T3 and T4 extraction and assay methods in feces of wild northern spotted owls, African elephants, howler monkeys, caribou, moose, wolf, maned wolf, killer whales and Steller sea lions. We explained 99% of the variance in high and low T3 concentrations derived from species-specific sample pools, after controlling for species and the various extraction methods tested. Fecal T3 reflected nutritional deficits in two male and three female howler monkeys held in captivity for translocation from a highly degraded habitat. Results suggest that thyroid hormone can be accurately and reliably measured in feces, providing important indices for environmental physiology across a diverse array of birds and mammals.

Astronomical and meteorological parameters and rest-activity rhythm in the Spider monkey Ateles geoffroyi

UNLABELLED All animals including primates show regular variations in their behavioural activities and physiological functions. In numerous species diel, ultradian, infradian, annual and/or lunar rhythms have been established; however, the use of the focal sampling method does not provide information on hour-to-hour nor day-to-day variations. In behavioural field studies dealing with primate activity rhythms and their modulation by environmental variables the possible dual, synchronizing and/or masking effect of these variables is often ignored. In the present study, we analyze the relation between astronomical and meteorological parameters and various parameters of the rest-activity rhythm in Ateles geoffroyi, a species scarcely investigated with respect to biological rhythms. These Ateles were kept under semi-natural conditions, exposed to natural light, temperature and humidity cycles, and sky state. Motor activity was recorded with actiwatch accelerometers during 180 days (5-min intervals), starting from the autumn equinox. RESULTS Ateles is active throughout the day, rests during the night and presents bimodal activity. Activity time, onset and end of activity as well as the times of their two activity peaks were significantly correlated with duration of the solar day and sunrise or sunset time. The behavioural parameters also correlated with ambient temperature. Climate factors and sky-state significantly influenced the duration and times of onset and end of activity. Our findings identified a clear modulation of the rest-activity pattern by astronomical variables serving as Zeitgebers, such as the natural light-dark cycle, and by masking effects of meteorological factors (temperature, weather and cloudiness), as well as of artificial variables introduced by the interaction with man.

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.

Impact of Intrasexual Selection on Sexual Dimorphism and Testes Size in the Mexican Howler Monkeys Alouatta palliata and A. pigra

One of the goals of physical anthropology and primatology is to understand how primate social systems influence the evolution of sexually selected traits. Howler monkeys provide a good model for studying sexual selection due to differences in social systems between related species. Here, we examine data from the sister howler monkey species Alouatta palliata and A. pigra inhabiting southeastern Mexico and northern Guatemala. We use a resampling approach to analyze differences in sexual dimorphism of body and canine size. In addition, we compare testes size as a way of gauging the intensity of sperm competition in both species. Morphometric data were collected from wild-caught individuals, including body mass and length, and dental data were obtained from casts from wild individuals and from museum specimens. Although A. pigra individuals are larger than their A. palliata counterparts, we find that both species exhibit similar levels of sexual dimorphism for all of the variables considered. Testicular volume results indicate that A. palliata male testes are on average twice as large as those of A. pigra males, suggesting more intense sperm competition in the former species. Our study shows that A. pigra is not highly sexually dimorphic as was once thought, and testes size differences suggest the need for a clearer understanding of howler monkey social systems.

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.

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. Am. J. Primatol. 76:855–867, 2014.