Jurgi Cristóbal-Azkarate

Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa

The threat that forest fragmentation and habitat loss presents for several Alouatta taxa requires us to determine the key elements that may promote the persistence of howler monkeys in forest fragments and to evaluate how changes in the availability of these elements may affect their future conservation prospects. In this study we analyzed the relationship between the availability of both big trees of top food taxa (BTTFT) (diameter at breast height>60) and fruit of top food taxa (FrTFT) in the home ranges of two groups of Alouatta palliata mexicana occupying different forest fragments in Los Tuxtlas, Mexico, and their diet and activity pattern. Both study groups preferred big trees for feeding and the group with lower availability of BTTFT in their home range fed from more, smaller food sources. Furthermore, both study groups also increased the number of food sources when their consumption of fruit decreased, and the group with lower availability of FrTFT in their home range fed from more food sources. The increase in the number of food sources used under such conditions, in turn, set up a process of higher foraging effort and lower rest. In summary, our results support other studies that suggest that the availability of big trees and fruit may be two important elements influencing the persistence of howler monkeys in forest fragments. Am. J. Primatol. 71:654–662, 2009.

Foraging Habits of Alouatta palliata mexicana in Three Forest Fragments

The activity patterns and diet of howler monkeys (Alouatta palliata mexicana) were studied in 3 forest fragments in south-eastern Mexico: Playa Escondida (PLA), Agaltepec Island (AGA) and Arroyo Liza (LIZ). Intersite differences offered the opportunity to investigate the foraging adaptations of howler monkeys in response to population and habitat size. In the largest fragment (PLA), the howlers’ diet was based on high-quality items (fruit and young leaves). In AGA, where the density of howlers was the highest, their diet was mostly folivorous with a marked exploitation of uncommon food items such as vines, lianas, shrubs and herbs. The dietary differences in AGA were accompanied by more time spent travelling and less time spent resting. Although LIZ was the smallest fragment and had a high howler density, the small group size and the use of energy-minimizing strategies (less time spent travelling and more time spent resting) probably allowed howlers to maintain a frugivorous diet.

Testosterone levels of free-ranging resident mantled howler monkey males in relation to the number and density of solitary males: a test of the challenge hypothesis.

The challenge hypothesis asserts that testosterone levels and aggression in male adult animals are closely associated with one another in the context of intense reproductive competition, particularly when males challenge one another for the access to females. For mantled howler monkeys (Alouatta palliata), the presence of a solitary male in the vicinity of a social group can be considered a threat for the reproductive success of the resident males, as group takeovers by solitary males are followed by a reestablishment of the access to females among group males and sometimes by infanticide. Therefore, these episodes should be accompanied by an increase in testosterone secretion according to the challenge hypothesis. In order to test our prediction, we relate different group and subpopulation variables to the testosterone levels measured in feces collected from 10 groups living in 6 forest fragments, at Los Tuxtlas, Mexico. Our results suggest that resident A. palliata males regard solitary individuals as potential contesters for their reproductive success and that they respond to interactions with them with an increase in testosterone levels, that is increasing their aggressiveness. Our results also suggest that in the studied groups all males have at least certain access to mates and that the entrance of a new male would affect their reproductive success negatively. Finally, the negative effects of chronically high testosterone levels may be negatively affecting the fitness of our study groups living in high population densities and small fragments.

Evolutionary Trade-Off between Vocal Tract and Testes Dimensions in Howler Monkeys

Summary Males often face a trade-off between investments in precopulatory and postcopulatory traits [1], particularly when male-male contest competition determines access to mates [2]. To date, studies of precopulatory strategies have largely focused on visual ornaments (e.g., coloration) or weapon morphology (e.g., antlers, horns, and canines). However, vocalizations can also play an important role in both male competition and female choice [3, 4, 5]. We investigated variation in vocal tract dimensions among male howler monkeys (Alouatta spp.), which produce loud roars using a highly specialized and greatly enlarged hyoid bone and larynx [6]. We examined the relative male investment in hyoids and testes among howler monkey species in relation to the level of male-male competition and analyzed the acoustic consequences of variation in hyoid morphology. Species characterized by single-male groups have large hyoids and small testes, suggesting high levels of vocally mediated competition. Larger hyoids lower formant frequencies, probably increasing the acoustic impression of male body size and playing a role analogous to investment in large body size or weaponry. Across species, as the number of males per group increases, testes volume also increases, indicating higher levels of postcopulatory sperm competition, while hyoid volume decreases. These results provide the first evidence of an evolutionary trade-off between investment in precopulatory vocal characteristics and postcopulatory sperm production.

Seasonal Variations in the Diet and Feeding Effort of Two Groups of Howlers in Different Sized Forest Fragments

Little is known about how resource limitation affects the feeding ecology of primates in forest fragments. Here, we describe seasonal variation in the diet and feeding effort of 2 groups (RH and RC3) of howlers (Alouatta palliata mexicana) living in different sized forest fragments in Los Tuxtlas, Mexico. The RH group, which lived in a larger and more preserved forest fragment, with a higher availability of fruit and Ficus trees, had a higher and more constant consumption of fruit throughout the study year. Moreover, this group fed from larger food sources, i.e., trees, lianas, and shrubs, and spent more time feeding from each food source. The feeding effort, defined as the time spent feeding and traveling divided by time spent resting, of the RH group was also significantly lower and more stable than that of the RC3 group throughout the study year. As feeding effort has been positively related to stress in primates, such increases in feeding effort could have negative consequences for howlers in small or degraded forest fragments. Our study suggests that habitat characteristics interact with plant seasonality to determine the diet and feeding effort of howlers in forest fragments and that groups living in small and degraded forest fragments may be particularly vulnerable to years of low fruit production.

Travel Time Predicts Fecal Glucocorticoid Levels in Free-Ranging Howlers (Alouatta palliata)

Environmental stressors impact physiology in many animal species. Accordingly, the monitoring of fecal glucocorticoid metabolites (fGCM) has been increasingly used to evaluate the physiological costs of habitat disturbance on wild animal populations, providing a powerful tool for conservation and management. Several studies have suggested that primates in forest fragments have higher fGCM levels than those in continuous forests, yet the proximate causes of fGCM variation remain to be identified. In previous studies of Mexican howlers (Alouatta palliata mexicana) in Los Tuxtlas, Mexico, we found that individuals living in a smaller and more disturbed forest fragment consumed significantly less fruit and had a significantly higher feeding effort than those living in a bigger, more conserved forest fragment. Here, we aimed to examine the effects of fruit consumption and travel time on fGCM levels in the same two groups of howlers, during three sampling sessions that differed markedly in fruit availability. We found that fGCM levels (N = 202 fecal samples) were higher in the howler group living in the smaller forest fragment and varied seasonally in both focal groups, being lowest when fruit consumption was highest. However, our results suggest that travel time is the main factor predicting fGCM levels in howlers, and that although fruit consumption may be negatively related to fGCM levels, this relationship is probably mediated by the strong effect that fruit consumption has on travel time. Our results provide important insight into the proximate causes of fGCM variation in primates in fragments and highlight the potential conservation significance of studies showing that habitat loss and transformation can lead to increases in travel time in wild primates.

Causes of Intraspecific Aggression in Alouatta palliata mexicana: Evidence From Injuries, Demography, and Habitat

Although howlers have been traditionally considered to be pacific, showing one of the lowest rates of aggression among primates, new evidence is emerging to question this image. We present data on injuries in Mexican mantled howlers (Alouatta palliata mexicana) in relation to different sociecological parameters. We censused howler populations in 19 forest fragments over a 17-mo period in the Los Tuxtlas Region, southern Veracruz, Mexico. We conducted detailed observations of scars, torn lips, broken fingers, mutilated tails and other visible injuries. We also collected data on the demography, biogeography and vegetation of each fragment in order to relate injury data to them. We censused 333 howlers, of which we exhaustively observed 254 for injuries. Four resident adult females (n = 108) and 29 adult resident males (n = 76) had injuries, while none of the solitary males (n=16), solitary females (n=1), juveniles (n=23) and infants (n=30) had them. We discuss possible interpretative scenarios for the distribution of injuries. Although some results suggest that food resource concentration may determine intergroup agonistic encounters, we propose that physical injury is primarily associated with male-male agonistic encounters during takeovers, and consequently it could indicate migration among troops.

Resistance to Antibiotics of Clinical Relevance in the Fecal Microbiota of Mexican Wildlife

There are a growing number of reports of antibiotic resistance (ATBR) in bacteria living in wildlife. This is a cause for concern as ATBR in wildlife represents a potential public health threat. However, little is known about the factors that might determine the presence, abundance and dispersion of ATBR bacteria in wildlife. Here, we used culture and molecular methods to assess ATBR in bacteria in fecal samples from howler monkeys (Alouatta palliata), spider monkeys (Ateles geoffroyi), tapirs (Tapirus bairdii) and felids (jaguars, Panthera onca; pumas, Puma concolor; jaguarundis, Puma yagouaroundi; and ocelots, Leopardus pardalis) living freely in two regions of the Mexican state of Veracruz under different degrees of human influence. Overall, our study shows that ATBR is commonplace in bacteria isolated from wildlife in southeast Mexico. Most of the resistances were towards old and naturally occurring antibiotics, but we also observed resistances of potential clinical significance. We found that proximity to humans positively affected the presence of ATBR and that ATBR was higher in terrestrial than arboreal species. We also found evidence suggesting different terrestrial and aerial routes for the transmission of ATBR between humans and wildlife. The prevalence and potential ATBR transfer mechanisms between humans and wildlife observed in this study highlight the need for further studies to identify the factors that might determine ATBR presence, abundance and distribution.

Metabolic strategies in wild male Barbary macaques: evidence from faecal measurement of thyroid hormone

Selection is expected to favour the evolution of flexible metabolic strategies, in response to environmental conditions. Here, we use a non-invasive index of basal metabolic rate (BMR), faecal thyroid hormone (T3) levels, to explore metabolic flexibility in a wild mammal inhabiting a highly seasonal, challenging environment. T3 levels of adult male Barbary macaques in the Atlas Mountains, Morocco, varied markedly over the year; temporal patterns of variation differed between a wild-feeding and a provisioned group. Overall, T3 levels were related to temperature, foraging time (linked to food availability) and intensity of mating activity, and were higher in the provisioned than in the wild-feeding group. In both groups, T3 levels began to increase markedly one month before the start of the mating season, peaking four to six weeks into this period, and at a higher level in the wild-feeding group. Our results suggest that while both groups demonstrate marked metabolic flexibility, responding similarly to ecological and social challenges, such flexibility is affected by food availability. This study provides new insights into the way Barbary macaques respond to the multiple demands of their environment.

Feeding encounters between a group of howler monkeys and white-nosed coatis in a small forest fragment in Los Tuxtlas, Mexico

Interactions between sympatric species are of particular interest for understanding the mechanisms that allow animal coexistence in the ecological community. The mantled howler monkey ( Alouatta palliata Gray) and the white-nosed coati ( Nasua narica Linnaeus) are similar-sized mammals with a sympatric distribution in the Neotropics (Nowak 1999). Since these two species are partly frugivorous (howler, Crockett & Eisenberg 1987; coati, Gompper 1997), and fruit is often limited (Laurance et al . 2003), howlers and coatis might be observed foraging from the same fruiting tree, but there is no information regarding this possibility. We studied the feeding encounters between these two species in a small forest fragment, and discuss the conditions under which these episodes occur.