Jacob C. Dunn

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.

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.

Primates in Fragments 10 Years Later: Once and Future Goals

In 2010, the Food and Agriculture Organization of the United Nations (FAO) estimated that 16 million hectares of forest per year were lost globally in the 1990s (FAO 2010), and approximately 12.5 million hectares/year were lost in countries with primate populations, an area just smaller than Greece or the US State of Mississippi (Chapman and Peres 2001; Chapman and Gogarten 2012). In contrast, in the last decade (2000–2010), the rate of deforestation has decreased globally by approximately 5.2 million hectares/year, and reforestation and natural expansion of forests in some countries significantly reduced the net loss of forest (FAO 2010). This may be in part due to the lack of resonance in satellite imagery between secondary and primary forest regions, particularly in the tropics. Unfortunately, the increase in forested lands has principally affected temperate regions of Europe and eastern Asia (e.g., China, Japan), but deforestation of most tropical forests has continued steadily (e.g., annual loss: 0.5 % in Africa, 1.2 % in Mesoamerica, 0.5 % in South America, 0.4 % in southeastern Asia; FAO 2011).

Body size and vocalization in primates and carnivores

A fundamental assumption in bioacoustics is that large animals tend to produce vocalizations with lower frequencies than small animals. This inverse relationship between body size and vocalization frequencies is widely considered to be foundational in animal communication, with prominent theories arguing that it played a critical role in the evolution of vocal communication, in both production and perception. A major shortcoming of these theories is that they lack a solid empirical foundation: rigorous comparisons between body size and vocalization frequencies remain scarce, particularly among mammals. We address this issue here in a study of body size and vocalization frequencies conducted across 91 mammalian species, covering most of the size range in the orders Primates (n = 50; ~0.11–120 Kg) and Carnivora (n = 41; ~0.14–250 Kg). We employed a novel procedure designed to capture spectral variability and standardize frequency measurement of vocalization data across species. The results unequivocally demonstrate strong inverse relationships between body size and vocalization frequencies in primates and carnivores, filling a long-standing gap in mammalian bioacoustics and providing an empirical foundation for theories on the adaptive function of call frequency in animal communication.

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.

Role of Emitter and Severity of Aggression Influence the Agonistic Vocalizations of Geoffroy's Spider Monkeys (Ateles geoffroyi)

Natural selection has resulted in the acoustic convergence of many animal vocalizations. During agonistic interactions vocalizations may vary depending on the role an individual plays in the interaction and on the severity of the attack. Motivation-structural rules describe how aggressors are thought to have evolved to use low-frequency vocalizations, whereas victims often use high-frequency vocalizations. This is because call frequency (Hz) is negatively related to body size across species. Motivational theory predicts that during more severe attacks, vocal structure will also change in response to increased arousal, leading to the production of noisy (high-entropy) vocalizations. Little is known about the acoustic characteristics of vocalizations produced during agonistic encounters in primates, and the limited available data are highly biased toward Old World species. Here, we evaluated the effect of the role of the emitter (aggressor or victim) and the severity of the behavior (with or without contact) on the acoustic parameters of 185 agonistic vocalizations emitted by 15 spider monkeys (Ateles geoffroyi) in two captive groups. Our results supported the predictions of both the motivation-structural rules and motivational theory: Call frequency (Hz) was lower in aggressors than in victims and lower during high-severity encounters than low-severity encounters. Further, average entropy was higher during high-severity encounters. These findings suggest that the agonistic vocalizations of spider monkeys convey information about both the role of the emitter and the severity of the interaction.

Angiosperms, Los Tuxtlas Biosphere Reserve, Veracruz, Mexico

The Los Tuxtlas Reserve has been heavily deforested and fragmented since the 1970’s. Although the flora of Los Tuxtlas has been described previously, most floristic lists come from the large forest reserve of the Los Tuxtlas field station. Here we present a check list of Angiosperms recorded in 45 rainforest fragments (< 1 to 266 ha) located in three landscapes with different levels of deforestation. We sampled all trees, shrubs, lianas, palms and herbs with diameter at breast height (dbh) Ā 2.5 cm within ten 50 m x 2 m plots per fragment. We recorded 9,435 plants belonging to 73 families and 372 species. Fabaceae, Rubiaceae, and Moraceae were best represented. Eight species are classified as Endangered by the Mexican government, and five are human-introduced species. We conclude that the conservation and restoration of all the remaining rainforest fragments are necessary to effectively preserve the plant diversity of this region.

Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production

A fundamental issue in the evolution of communication is the degree to which signals convey accurate (“honest”) information about the signaler. In bioacoustics, the assumption that fundamental frequency (fo) should correlate with the body size of the caller is widespread, but this belief has been challenged by various studies, possibly because larynx size and body size can vary independently. In the present comparative study, we conducted excised larynx experiments to investigate this hypothesis rigorously and explore the determinants of fo. Using specimens from eleven primate species, we carried out an inter-specific investigation, examining correlations between the minimum fo produced by the sound source, body size and vocal fold length (VFL). We found that, across species, VFL predicted minimum fo much better than body size, clearly demonstrating the potential for decoupling between larynx size and body size in primates. These findings shed new light on the diversity of primate vocalizations and vocal morphology, highlighting the importance of vocal physiology in understanding the evolution of mammal vocal communication.