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Howler Monkeys (Alouatta palliata mexicana) Produce Tannin-Binding Salivary Proteins

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Abstract

Dietary tannins are ubiquitous in woody plants and may have serious negative effects on herbivores by inducing a loss of dietary protein and producing toxins if they are hydrolyzed in the gut. Many herbivorous mammals counter the negative effects of tannins through tannin-binding salivary proteins (TBSPs) that inactivate tannins by forming insoluble complexes and prevent them from interacting with other more valuable proteins. Howlers are the most folivorous New World primates and ingest foods with varying tannin content. We studied the presence of TBSPs in six wild mantled howlers (Alouatta palliata mexicana) immediately after capture and in captivity when fed on two diets composed of natural ingredients: a mixture of fruit and leaves or only leaves. Protein concentration was determined in whole saliva samples, followed by gel electrophoresis. We identified two protein bands of 17 and 25 kDa that have tannin-binding capacity. Although the monkeys ate almost twice as much condensed tannins in the leaf diet than in the fruits and leaves diet (7 vs. 4 g/d dry matter) the salivary protein concentration did not differ between the two diets (leaf diet: 3.29 ± SE 0.82 vs. fruit and leaves diet: 3.42 ± SE 0.62 mg/ml) and we found no additional protein bands in response to either diet. We suggest that the continuous expression of TBSPs is part of a dietary strategy that enables howlers to consume diets with variable tannin contents, thus partly explaining their dietary flexibility. Although the importance of salivary proteins to arboreal primates is broadly accepted, to our knowledge this is the first report of TBSPs in any Neotropical primate.

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Acknowledgments

This research was funded by CONACYT-FOMIX 109499 and by CONACYT I010/458/2013 C-703/2013. F. E. Gómez was supported by CONACYT Scholarship 171093. We especially appreciate the work and dedication of several field assistants: Gildardo Castañeda, Antonio Jauregui, Rubén Mateo, and biologist Denedi García. F. E. Gómez thanks Dr. Fausto Rojas for help with laboratory techniques and Dr. Javier Hermida for his support during the capture of animals. We are very grateful to Dr. Ken Glander, Dr. Ellen Dierenfeld, and Dr. Jessica Rothman for the very helpful comments that improved the article.

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Authors and Affiliations

  1. Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, C.P. 91190, México

    F. Espinosa Gómez, Jorge Morales Mávil, Domingo Canales Espinosa & Laura Hernández Salazar

  2. Instituto de Investigaciones Biológicas, Universidad Veracruzana, Xalapa, Veracruz, C.P. 91190, México

    Juan Santiago García

  3. Centro Nacional de Investigación Disciplinaria en Fisiología y Mejoramiento Animal, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Ajuchitlán, C.P. 76280, Querétaro, México

    Sergio Gómez Rosales

  4. Evolution, Ecology and Genetics, Research School of Biology, Australian National University, Canberra, 0200, Australia

    Ian R. Wallis

  5. McGill School of Environment and Dept. of Anthropology, McGill University, Montreal, Quebec, H3A 2T7, Canada

    F. Espinosa Gómez & Colin A. Chapman

  6. Wildlife Conservation Society, Bronx, NY, 10460, USA

    Colin A. Chapman

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Espinosa Gómez, F., Santiago García, J., Gómez Rosales, S. et al. Howler Monkeys (Alouatta palliata mexicana) Produce Tannin-Binding Salivary Proteins. Int J Primatol 36, 1086–1100 (2015). https://doi.org/10.1007/s10764-015-9879-4

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