Sexual dimorphism and growth in Alouatta palliata based on 20+ years of field data.

OBJECTIVES: Alouatta palliata patterns of growth and sexual dimorphism are evaluated using 20 plus years of field data. Comparisons are made to other species of Alouatta and other New World primates. MATERIALS AND METHODS: Records of 92 A. palliata from Guanacaste Province, Costa Rica, were used to generate growth curves for body mass and linear measurements. Timing of growth for the properties was compared, and males and females were contrasted. Slopes and elevations for periods of rapid growth were evaluated. Growth allometry and proportion ratios were also explored. RESULTS: Body mass growth is rapid during the first 2 years. Males and females begin to diverge around a year of age as male growth increases and female growth slows. Adult mass for both is reached about 4 years of age. Linear measurements show rapid growth the first 18 months for both sexes. Differences develop as males continue the same rate of linear growth while female growth slows. Adult size is reached for head and body length around 3 years, and for hind-foot and tail lengths around 2 years. DISCUSSION: A. palliata males grow in mass more rapidly than females, while both grow similarly in linear dimensions, so that dimorphism is more pronounced in mass. This pattern is seen in other dimorphic New World primates. Male A. palliata may grow more rapidly than A. seniculus, reflecting earlier emigration for A. palliata males. Linear dimensions reach adult proportions earlier than body mass. For hind-foot and tail, this is probably an adaptation for gripping.

Factors influencing infant sex ratio in howler monkeys (Alouatta spp.): A literature review and analysis.

OBJECTIVE: Frequency-dependent selection is expected to maintain infant sex ratios around parity over evolutionary time. However, over ecological time periods, infant sex ratios vary, and it has been proposed that this variation may reflect adaptive processes. In primates, there are consistent patterns of variation in infant sex ratios, although their adaptive significance remains contentious. In addition to design issues, contrasting results could have derived across primates from variation in the fitness benefits accrued through sons or daughters associated with the specific social, ecological, and demographic context of populations. Thus, different sex allocation tactics could occur within species over time and space. METHODS: We reviewed the literature to describe variation in infant sex ratio in howler monkeys (genus Alouatta) and to examine whether such a variation could be associated with adaptive sex allocation. We found 26 studies that provided data for this review. These studies yielded 96 infant sex reports, corresponding to 1,477 sexed infants. RESULTS: Infant sex ratio across howler monkey species tends to parity, but females produce more sons under high group densities and more daughters when rainfall increases. DISCUSSION: Based on these results, as well as on information on howler monkey dispersal patterns, demography, and within-group genetic relatedness, we speculate that, depending on population growth stage, sex allocation is explained by (a) local resource enhancement, that is, more cooperative philopatric daughters are produced when populations are growing; and (b) local resource competition, that is, more dispersing sons are produced when populations are saturated. Thus, there is evidence suggestive of adaptive variation in infant sex ratios in howler monkeys.

Evidence-based conservation education in Mexican communities: Connecting arts and science.

Several studies suggest that 63% of primate species are currently threatened due to deforestation, pet-trade, and bushmeat hunting. Successful primate conservation strategies require effective educational programs capable of enhancing critical system-thinking and responsible behavior towards these species. Arts-based conservation education can simultaneously foster cognitive and emotional processes. In this paper, we evaluate an arts-based educational program focused on the conservation of black howler monkeys (Alouatta pigra). Our goals were to determine (1) whether children's knowledge changed with our educational techniques, (2) if there was a particular educational technique that better improved the children's learning, and (3) the children's emotional feedback regarding the whole program. A total of 229 children from communities located in primate-habitat areas, both inside and outside protected areas, participated in the study. Different educational techniques were tested (storytelling, theater and shadow puppets), contrasted with a control group, and evaluated through an analysis of drawings. Our results showed that children's knowledge increase with each art-based technique, with storytelling being the most effective for children's learning. Specific drawings indicators also revealed the increase of children's knowledge and a decrease of misconceptions between pre and post evaluations. Finally, a satisfaction survey about the program showed a high positive feedback. The study highlights the value of designing multidisciplinary projects, where arts-based education program (grounded in scientific information) has shown to be a successful way to communicate animal knowledge and promote conservation.

Cranial shape variation in adult howler monkeys (Alouatta seniculus).

Howler monkeys (genus Alouatta) display a distinctive cranial architecture characterized by airorhynchy (or retroflexion of the facial skeleton on the cranial base), a small braincase, and a posteriorly oriented foramen magnum. This configuration has been associated with distinct factors including a high folivory diet, locomotion, and the presence of a specialized vocal tract characterized by large hyoid bone. However, the morphological relationships between the facial and neurocranial blocks in Alouatta have been scarcely investigated. In this study we quantitatively analyzed the cranial shape variation in Alouatta seniculus, to evaluate possible influences and constraints in face and braincase associated with airorhynchy. We also considered the structural role of the pteric area within the cranial functional matrix. We applied landmark-based analysis and multivariate statistics to 31 adult crania, computing shape analyses based on 3D coordinates registration as well as the analysis of the Euclidean distance matrix to investigate patterns of intraspecific morphological variability. Our results suggest that allometry is the main source of variation involved in shaping cranial morphology in howlers, influencing the degree of facial proportions and braincase flattening, and generating the main sexual differences. Larger individuals are characterized by a higher degree of airorhynchy, neurocranial flattening, and expansion of the zygomatic arch. Allometric variations influence the skull as a whole, without distinct patterns for face and braincase, which behave as an integrated morphological unit. A preliminary survey on the pteric pattern suggests that the morphology of this area may be the result of variations in the vertical growth rates between face and braincase. Future studies should be dedicated to the ontogenetic series and focus on airorhynchy in terms of differential growth among distinct cranial districts.

Sex differences in the behavior of wild Alouatta caraya infants.

Several primates show sex-based differences in activity patterns and social interactions during infancy. These differences have been associated with adult social and reproductive functions of males and females and are related to male-male competition. Our goal was to describe behavioral patterns of wild Alouatta caraya male and female infants, a species with sexual dimorphism in body size and behavioral strategies during adulthood. We also examined the relationship between life history variables, infant sex and age, activity patterns, and social interactions in order to determine whether males and females follow different trajectories during early growth. Over a 27-month study, we observed 21 male infants and 14 female infants across two similar sites in northern Argentina. Data were analyzed using generalized linear mixed model (GLMM) tests. We found no differences in suckling time or weaning age between males and females (9.7 vs. 9.4 months), but male infants spent more time feeding on solid food and resting than female infants. Males also invested more time in contact with their mothers than did female infants, and mothers rejected and broke contact with males more frequently than with females. Other behavioral categories did not differ between the sexes. Our results suggest that higher nutritional demands of males compared with females may affect some behaviors. However, mothers of sons did not experience immediate trade-offs between current and future reproduction. Other behaviors, similarly expressed by the two sexes, suggest a similar developmental trajectory between male and female A. caraya infants, meaning that most differences emerge following the infant period.

When top-down becomes bottom up: behaviour of hyperdense howler monkeys (Alouatta seniculus) trapped on a 0.6 ha island.

Predators are a ubiquitous presence in most natural environments. Opportunities to contrast the behaviour of a species in the presence and absence of predators are thus rare. Here we report on the behaviour of howler monkey groups living under radically different conditions on two land-bridge islands in Lago Guri, Venezuela. One group of 6 adults inhabited a 190-ha island (Danto) where they were exposed to multiple potential predators. This group, the control, occupied a home range of 23 ha and contested access to food resources with neighbouring groups in typical fashion. The second group, containing 6 adults, was isolated on a remote, predator-free 0.6 ha islet (Iguana) offering limited food resources. Howlers living on the large island moved, fed and rested in a coherent group, frequently engaged in affiliative activities, rarely displayed agonistic behaviour and maintained intergroup spacing through howling. In contrast, the howlers on Iguana showed repulsion, as individuals spent most of their time spaced widely around the perimeter of the island. Iguana howlers rarely engaged in affiliative behaviour, often chased or fought with one another and were not observed to howl. These behaviors are interpreted as adjustments to the unrelenting deprivation associated with bottom-up limitation in a predator-free environment.

Cranial ontogeny and sexual dimorphism in two new world monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae).

Pattern of skull development and sexual dimorphism was studied in Cebus apella and Alouatta caraya using univariate, bivariate, and multivariate statistics. In both species, sexual dimorphism develops because the common growth trajectory in males extends and because of differences in growth rates between sexes. The expectation that the ontogenetic bases of adult dimorphism vary interspecifically is well substantiated by this study. A. caraya exhibits transitional dimorphism in its subadult stage, although the condylobasal length, zygomatic breadth, and rostrum length are strongly dimorphic in the final adult stage, being greater in males. Most cranial measurements in C. apella exhibit significant dimorphism in the adult stage, being strongly influenced by a faster rate of growth in males. Sexual dimorphism is also evidenced through sex differences in growth rates in several cranial measurements. These results also indicate that different ontogenetic mechanisms are acting in C. apella and A. caraya and reveal differences in the way through which neotropical primates attain adult sexual dimorphism.

Anotaciones de la ecología alimentaria de monos aulladores negros en un fragmento con condiciones de hacinamiento (Balancán, Tabasco, México) / Anotações sobre a ecologia alimentar de bugios num fragmento superlotado (Balancán, Tabasco, México) / Annotations on the feeding ecology of black howler monkeys in an overcrowded fragment in Balancán, Tabasco, México

Se describió el comportamiento de alimentación del mono aullador negro centroamericano (Alouatta pigra) en un fragmento de menos de una hectárea de selva húmeda perennifolia rodeada de pastizales de uso ganadero, árboles dispersos y huertos de mango en la región de Balancán (Tabasco, México). Objetivo: reportar la dieta y actividad del mono aullador negro en condiciones de hacinamiento durante el mes más lluvioso en Balancán, Tabasco, México. Materiales y métodos: las observaciones conductuales (81 h) se hicieron mediante la metodología animal focal de una tropa de A. pigra constituida por tres individuos (un macho adulto, un hembra adulta y un infante). Resultados: del tiempo total de observación, la alimentación representó el 15,97%, el descanso el 78% y la locomoción el 4,57%. En el área de estudio se registraron 14 especies de plantas, de las cuales 10 fueron consumidas por los monos aulladores. El 55% del tiempo de alimentación fue invertido al consumo de frutos, 27% a las hojas, 17% al tallo y 1% a los retoños. La especie de árbol más consumida fue Spondias mombin, con el 61% del tiempo invertido. Conclusión: al igual que otros estudios, se confirmó la tendencia alimentaria folívoro-frugívora del género Alouatta. Se provee información sobre la flexibilidad que tienen los monos aulladores negros para vivir y mantenerse en condiciones de extrema perturbación donde su hábitat es de 0,1 hectáreas con pocas especies de árboles para utilizar, lo que además obliga a los individuos a hacer uso del suelo para trasladarse. Palabras clave: Alouatta pigra, Dieta, Patrón de actividad, Frugivoría, Hábitat fragmentado...

Annotations on the feeding ecology of black howler monkeys in an overcrowded fragment in Balancán, Tabasco, México. We described the feeding behavior of Central-American black howler monkey (Alouatta pigra) in a fragment of less than one hectare of humid evergreen forest surrounded by grassland for livestock use, isolated trees and mango orchards, in the region of Balancán (Tabasco, México). Objective: To record the diet and activity of black howler monkeys in crowded conditions during the wettest month in Balancán (Tabasco, México). Methods and methods: The behavioral observations (81 h) were made using the focal animal methodology with an A. pigra troop made up of three individuals (1 adult male, 1 adult female and 1 infant). Results: Feeding time represented 15.97%, rest 78% and locomotion 4.57% of total time. In the study area we recorded 14 plant species, with 10 being consumed by howler monkeys. 55% of feeding time was devoted to the consumption of fruits, 27% to leaves, 17% to stems, and 1% to sprouts. Spondias mombin was the tree species most consumed, with 61% of the time invested on it. Conclusion: Like other studies, we confirmed the frugivore-folivore feeding tendency of the genus Alouatta. We provide information on the black howler monkey flexibility to live and maintain themselves in extreme perturbation conditions, where their habitat is 0.1 ha with few tree species to use, forcing individuals to move around the ground...

Anotações sobre a ecologia alimentar de bugios num fragmento superlotado (Balancán, Tabasco, México). Descreve-se o comportamento alimentar do bugio centro-americano (Alouatta pigra) num fragmento menor que 1 ha de floresta úmida perenifólia rodeada por pastos para uso do gado, árvores dispersas e pomares de manga na região de Balacán (Tabasco, México). Objetivo: Registrar a dieta e atividade do bugio em condições de superlotação durante o mês mais chuvoso em Balacán, Tabasco, México. Materiais e métodos: As observações de comportamento (81 h) se fizeram por abordagem animal focal de um grupo de A. pigra constituído por três indivíduos (um macho adulto, uma fêmea adulta e um infante). Resultados: Do tempo total de observação, a alimentação representou 15,97%, o descanso 78% e a locomoção 4,57%. Na área de estudo se registraram 14 espécies de plantas das quais 10 foram consumidas pelos bugios. O 55% do tempo de alimentação foi gasto para o consumo de frutas, 27% às folhas, 17% ao caule e 1% aos brotos. A espécie de árvores mais consumida foi Spondias mombin, com 61% do tempo investido. Conclusão: Assim como outros estudos confirma-se a tendência alimentaria folívora-frugívora do gênero Alouatta. Fornece-se informação sobre a flexibilidade que têm os bugios para viver e ficar em condições de extrema perturbação, onde seu habitat é de 0,1 ha com poucas espécies de árvores para seu uso. Forçando, além disso, aos indivíduos a usar o terreno para se deslocar...

Survey of the black howler monkey, alouatta pigra, population at the Mayan site of Palenque, Chiapas, Mexico.

A survey of the population of the black howler monkey (Alouatta pigra) present at the Mayan site of Palenque was conducted during 2000. A total of 911 man/hours, spread over 112 days were spent surveying the 600 ha area of pristine forest at the site for howler troops. We detected the presence of 136 individuals of which 131 were members of 20 troops, the rest were 3 solitary adult males and 2 adult males travelling as a pair. Ecological density was estimated at 23 individuals/km(2). Mean troop size was 7.0 individuals and it ranged from 2 - 12 individuals; 60% of the troops were multimale. All sighting of howler monkeys were in evergreen rain forest and 75% were in trees > or = 20 m in height. The reported densities and mean troop size are higher than those reported for the species in Guatemala and in central Quintana Roo, Mexico. The vegetation of the forest contains tree species reported to be used by species of Alouatta in the Moraceae, Sapotaceae, Leguminosae, and Lauraceae plant families. Protection of a large perimeter area (ca 1700 ha) around the archeological site by the Mexican government ensures the conservation of the forest and of the black howler monkey population present at the site.

Ontogenetic correlates of diet in anthropoid primates.

This study assesses ontogenetic correlates of diet in anthropoid primates. Associations between body weight growth, adult size, and diet are evaluated for a sample of 42 primate species, of which 8 are classifiable as "folivores." The hypothesis that folivores show a pattern of growth that differs from "nonfolivores" is tested. Ontogenetic variation is summarized through use of parametric and nonparametric regression analysis. Several analytical techniques, including broad interspecific and detailed comparisons among species of similar adult size, are applied. This investigation indicates a clear association between body weight ontogeny and diet: folivorous species grow more rapidly over a shorter duration than comprably sized nonfolivorus species. A positive correlation between adult size and diet is not unambiguously established in this sample. A threshold (at around 1 kg) below which insectivory is very common may adequately characterize the association between adult size and diet in anthropoid primates. Above this threshold, adult size does not appear to covary predictably with diet. Evolutionary correlates of the ontogenetic pattern seen in folivores may include a variety of factors. The distinctive pattern of development in folivores may relate to the profile of ecological and social risks that these species face. Morphophysiological advantages to rapid growth may relate to a need for accelerated alimentary (dental and gut) development. The implications of ontogenetic variation in folivores are discussed.