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Endocrinology of Howler Monkeys: Review and Directions for Future Research

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Howler Monkeys

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR))

Abstract

Endocrine studies that investigate the interplay between hormones, behavior, and social and ecological environment are critical for our understanding of proximate, physiological mechanisms underlying the biology and sociality of a species. Nonetheless, only recently have endocrine studies been incorporated into research on howler monkeys (Alouatta spp.), and only few aspects of endocrinology in 6 out of 12 species have been addressed. These include androgen and estrogen profiles of juvenile A. palliata, and progestin and estrogen profiles of the ovarian cycle of A. arctoidea, A. caraya, and A. pigra. In addition, socioendocrine studies in A. pigra and A. palliata have investigated how male androgen levels and male and female glucocorticoid levels are influenced by intra- and extragroup male–male competition, whereas ecologically oriented endocrine studies have revealed that in A. pigra, A. palliata, A. belzebul, and A. seniculus male and female glucocorticoid levels are influenced by a scarcity of high-quality food resources, habitat fragmentation, human disturbance, and translocation. Endocrine studies have shed light on howler monkey biology and sociality that were not anticipated based on behavioral data alone. This includes a nonaggressive form of intragroup male–male competition over access to females, a more prominent reliance on high-quality food resources such as fruits for these primarily folivorous primates, and an apparent higher sensitivity to social and ecological stress in females than in males. Additional endocrine studies across howler monkey species are needed to further elucidate relationships among diet, mating competition, and social interactions.

Resumen

Estudios endocrinológicos que investigan la interacción entre las hormonas, el comportamiento, y el contexto social y ecológico son fundamentales para nuestra comprensión de los mecanismos fisiológicos subyacentes a la biología y al sistema social de una especie. Sin embargo, sólo recientemente estudios endocrinológicos han sido incorporado en la investigación de los monos aulladores (Alouatta), y sólo unos pocos aspectos de la endocrinología en seis de las 12 especies han sido abordado. Estos incluyen investigar los perfiles de andrógenos y estrógenos de juveniles de A. palliata, y los perfiles de progesterona y estrógeno de los ciclos ováricos en A. arctoidea, A. caraya, y A. pigra. Además, los estudios socio-endocrinológicos de A. pigra y A. palliata han investigado como los niveles de andrógenos en machos y los niveles de glucocorticoides en machos y hembras se ven influidos por la competencia entre machos adentro y entre grupos, mientras que los estudios endocrinológicos en A. pigra, A. palliata, A. belzebul, y A. seniculus con un enfoque en factores ecológicos han revelado que los niveles de glucocorticoides de machos y hembras son afectados por la disponibilidad de alimentos de alta calidad, la fragmentación del hábitat, perturbación humana y el estrés acumulado durante eventos de translocación. Estudios endocrinológicos en el mono aullador han revelado aspectos de su biología y su sistema social que no fueron anticipados en base a sólo datos de comportamiento. Esto incluye una forma de competición no agresivo entre machos por el acceso a hembras, una dependencia más prominente en los recursos alimenticios de alta calidad como las frutas para estos primates principalmente folívoros, y una sensibilidad superior al estrés social y ecológico en hembras en comparación con machos. Otros estudios endocrinológicos entre más especies de monos aulladores serán necesarios para elucidar aún más el vínculo entre la dieta, la competición reproductiva, y las interacciones sociales.

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Acknowledgments

I thank Martín M. Kowalewski, Paul A. Garber, Liliana Cortés-Ortiz, Bernardo Urbani, and Dionisios Youlatos for the invitation to contribute to this volume and to Martín M. Kowalewski, Paul A. Garber, and an anonymous reviewer for constructive suggestions that improved the quality of the chapter. I was supported by a postdoctoral fellowship from Universidad Nacional Autónoma de México (UNAM) during the writing of this manuscript.

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  1. Instituto de Biología, Universidad Nacional Autónoma de México, Circuito Exterior s/n, Ciudad Universitaria, Copilco, Coyoacan, Distrito Federal, 04510, Mexico

    Sarie Van Belle

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  1. Sarie Van Belle
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Correspondence to Sarie Van Belle .

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Editors and Affiliations

  1. Estación Biológica Corrientes, Museo Argentino de Ciencias Naturales, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Martín M. Kowalewski

  2. Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

    Paul A. Garber

  3. Museum of Zoology, Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA

    Liliana Cortés-Ortiz

  4. Centro de Antropología, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela

    Bernardo Urbani

  5. Department of Zoology, Aristotle University of Thessalonik, Thessaloniki, Greece

    Dionisios Youlatos

Appendix: The Effect of Male Migration and Reproductive Status on Black Howler Female Fecal Glucocorticoid Levels

Appendix: The Effect of Male Migration and Reproductive Status on Black Howler Female Fecal Glucocorticoid Levels

1.1 Methods

Two multimale–multifemale black howler (A. pigra) groups were studied in Palenque National Park, Mexico from June 2006 through July 2007. The Balam group had three adult females at the onset of the study, but one female (MI) disappeared on October 18, 2006. The Motiepa group had two adult females throughout the study period. Both groups underwent several changes in adult male group membership (Balam, n = 7; Motiepa, n = 2; for detailed description, see Van Belle et al. 2008). Fresh fecal samples were collected from each adult female, on average, every 4.1 ± 1.4 days, resulting in a total of 246 samples. Methods used for sample storage, hormone extraction, assay validation, and glucocorticoid EIA are described in detail in Van Belle et al. (2009b). Values of hormone concentrations were log10 transformed to normalize the distribution and equalize the variance (Kolmogorov–Smirnov tests and Levene’s tests, P > 0.05), allowing the use of parametric tests.

General linear mixed models (GLMM) were used to analyze whether glucocorticoid levels of females differed between the 2 weeks prior to and the 2 weeks after male migration events in their groups. Random factors in the GLMM included female identity to account for the repeated sampling of the same individual, which was nested within groups to account for the possibility that coresiding females had correlated hormone levels and migration events nested within groups to account for the possibility that coresiding females changed hormonal levels similarly to the same migration events. To examine whether female glucocorticoid levels changed according to their reproductive status, a GLMM was used with female identity nested within groups as random factors and reproductive status as predictor variable. Female reproductive status was classified as acyclic, cycling, pregnant, or lactating based on their fecal estrogen and progestin profiles and presence of young offspring (Van Belle et al. 2009a).

1.2 Results

Adult females did not differ in their fecal glucocorticoid levels between the 2 weeks before and after male migrations in their groups (MeanBefore = 0.99 ± SE 0.09, MeanAfter = 1.05 ± 0.07, F 2,39.6 = 0.650, P = 0.527). However, female fecal glucocorticoid levels across different reproductive states were significantly different with females having higher fecal glucocorticoid levels when lactating compared to other reproductive states (Fig. 8.3, F 3,240.7 = 10.48, P < 0.001)

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Van Belle, S. (2015). Endocrinology of Howler Monkeys: Review and Directions for Future Research. In: Kowalewski, M., Garber, P., Cortés-Ortiz, L., Urbani, B., Youlatos, D. (eds) Howler Monkeys. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1957-4_8

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