Switching between Food Patches Suggests a Need to Balance Nutrients while Foraging in Wild Black Howler Monkeys (Alouatta pigra)

Nicoletta Righini, Paul A. Garber, Jessica M. Rothman, Minerva S. Santillán-Rivera, Antonio López-Espinoza

Resumen


Studies of feeding patch choice in primates have traditionally analyzed individual foraging decisions in relation to patterns of social foraging,
dominance, and feeding competition. However, information on detailed ecological and nutritional characteristics of the patches also is needed
to understand the basis of feeding patch preferences. In particular, recent models of nutritional ecology have stressed the importance of nutrient
balancing as a primary driver of individual foraging decisions. Here we investigated the behavioral and nutritional factors affecting feeding patch
choice in black howler monkeys (Alouatta pigra) during a 15-month field study in Campeche, Mexico. We collected 1300 hours of behavioral data
on 14 focal animals, including full-day follows of one individual/day recording all feeding activities. We carried out nutritional analyses of foods
from feeding trees and calculated daily nutrient intake. A total of 690 trees (i.e., patches) were visited throughout the study period. The time spent
feeding and the amount of food consumed differed significantly according to patch type. Individuals consumed more food in mature and immature
fruit patches than in mature leaf, young leaf, and flower patches. Protein intake rates (kJoule/min) were similar in young and mature leaf patches,
and higher than in mature fruit, immature fruit, and flower patches, among which the rate was similar. In the majority of the cases (80.3%), the
focal animals left the feeding patch prior to satiation. On those occasions, resource mixing, or moving from one food type to another food type,
accounted for 49.4% of the patch leaving events. The fact that black howler monkeys alternated feeding bouts between fruit and leaf patches, as
well as alternating bouts of higher and lower protein intake, suggest that this pattern could be dictated by the need to balance nutrients.

Palabras clave


Feeding behavior; Food patch; Foraging; Neotropical primates; Nutritional ecology

Citas


Aristizabal, J. F., Negrete-Yankelevich, S., Macías-Ordóñez, R., Chapman, C. A., & Serio-Silva, J. C. (2019). Spatial aggregation of fruits explains food selection in a Neotropical primate (Alouatta pigra). Scientific Reports, 9, 19452. doi:10.1038/s41598-019-55932-y

Bicca-Marques, J. C., & Garber, P. A. (2005). Use of social and ecological information in tamarin foraging decisions. International Journal of Primatology, 26(6), 1321-1344. doi:10.1007/s10764-005-8855-9

Busia, L., Schaffner, C. M., Rothman, J. M., & Aureli, F. (2016). Do fruit nutrients affect subgrouping patterns in wild spider monkeys (Ateles geoffroyi)? International Journal of Primatology, 37, 738-751. doi:10.1007/s10764-016-9935-8

Chapman, C. (1988). Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behaviour, 105(1-2), 99-116. doi:10.1163/156853988X00467

Chapman, C. A., & Chapman, L. J. (2000a). Determinants of group size in primates: The importance of travel costs. In S. Boinski & P. A. Garber (Eds.), On The Move. How and Why Animals Travel in Groups. Chicago, IL: University of Chicago Press.

Chapman, C. A., & Chapman, L. J. (2000b). Constraints on group size in redtail monkeys and red colobus: Testing the generality of the ecological constraints model. International Journal of Primatology, 21, 565-585. doi:10.1023/A:1005557002854

Charnov, E. L. (1976). Optimal foraging: the marginal value theorem. Theoretical Population Biology, 9, 129-136. doi:10.1016/0040-5809(76)90040-X

Conklin-Brittain, N. L., Knott, C. D., & Wrangham, R. W. (2006). Energy intake by wild chimpanzees and oragutans: methodological considerations and a preliminary comparison. In G. Hohmann, M. Robbins & C. Boesch (Eds.), Feeding Ecology in Apes and Other Primates. Cambridge, UK: Cambridge University Press.

Di Bitetti, M., & Janson, C. (2001). Social foraging and the finder's share in capuchin monkeys, Cebus apella. Animal Behavior, 62, 47-56. doi:10.1006/anbe.2000.1730

Erlenbach, J. A., Rode, K. D., Raubenheimer, D., & Robbins, C. T. (2014). Macronutrient optimization and energy maximization determine diets of brown bears. Journal of Mammalogy, 95, 160-068. doi:10.1644/13-MAMM-A-161

Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W.J. (2009a). Nutritional goals of wild primates. Functional Ecology, 23, 70-78. doi:10.1111/j.1365-2435.2008.01526.x

Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., Wallis, I., & Lindenmayer, D. B. (2009b). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology, 20, 685-690. doi:10.1093/beheco/arp021

Felton, A. M., Felton, A., Wood, J. T., Foley, W. J., Raubenheimer, D., Wallis, I. R., & Lindenmayer, D. B. (2009c). Nutritional ecology of Ateles chamek in lowland Bolivia: How macronutrient balancing influences food choices. International Journal of Primatology, 30, 675-696. doi:10.1007/s10764-009-9367-9

Garber, P. A. (2000). The Ecology of group movement: Evidence for the use of spatial, temporal, and social information in some primate foragers. In S. Boinski, & P. A. Garber (Eds.), On the Move: How and Why Animals Travel in Group. Chicago, IL: University of Chicago Press.

Garber, P. A., & Kowalewski, M. M. (2011). Collective action and male affiliation in howler monkeys (Alouatta caraya). In R.W. Sussman & C.R. Cloninger (Eds.), Origins of Altruism and Cooperation. New York, NY: Springer.

Garber, P. A., Bicca-Marques, J. C., & Azevedo Lopes, M. A. O. (2009). Primate Cognition: Integrating social and ecological information in decision-making. In P.A. Garber, A. Estrada, J. C. Bicca-Marques, E. Heymann & K. B. Strier, (Eds.), South American Primates: Comparative Perspectives in the Study of Behavior, Ecology, and Conservation. New York, NY: Springer.

Grether, G. F., Palombit, R. A., & Rodman, P. S. (1992). Gibbon foraging decisions and the marginal value model. International Journal of Primatology, 13, 1-17. doi:10.1007/BF02547724

Hailey, A., Chidavaenzi, R., & Loveridge, J. (1998). Diet mixing in the omnivorous tortoise Kinixys spekii. Functional Ecology, 12, 373-385. doi:10.1046/j.1365-2435.1998.00203.x

Harrison, M. J. S. (1984). Optimal foraging strategies in the diet of the green monkey, Cercopithecus sabaeus, at Mount Assirik, Senegal. International Journal of Primatology, 5, 435-471. doi:10.1007/BF02692269

Houston, A.I., Higginson, A.D., & McNamara, J.M. (2011). Optimal foraging for multiple nutrients in an unpredictable environment. Ecology Letters, 14, 1101-1107. doi:10.1111/j.1461-0248.2011.01678.x

Isbell, L. A. (1991). Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behavioral Ecology, 2, 143-155. doi:10.1093/beheco/2.2.143

Isbell, L. A. (2012). Re-evaluating the Ecological Constraints model with red colobus monkeys (Procolobus rufomitratus tephrosceles). Behaviour, 149, 493-529. doi:10.1163/156853912X641748

Janson, C. H., & van Schaik, C. P. (1988). Recognizing the many faces of primate food competition - methods. Behaviour, 105, 165-186. doi:10.1163/156853988X00502

Jiménez, I. (2004). Understanding vertebrate frugivores through foraging theory: patch use, diet composition and the abundance of curassow (Aves: Cracidae). PhD dissertation. St. Louis, MO: University of Missouri.

Johnson, C. A., Raubenheimer, D., Chapman, C. A., Tombak, K. J., Reid, A. J., & Rothman, J. M. (2017). Macronutrient balancing affects patch departure by guerezas (Colobus guereza). American Journal of Primatology, 79, 1-9. doi:10.1002/ajp.22495

Karasov, W. H. (2011). Digestive physiology: a view from molecules to ecosystem. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology, 301, R276-R284. doi:10.1152/ajpregu.00600.2010

Kazahari, N., & Agetsuma, N. (2008). Social factors enhancing foraging success of a wild group of Japanese macaques (Macaca fuscata) in a patchy food environment. Behaviour, 145, 843-860. doi:10.1163/156853908783929188

Kazahari, N., Tsuji, Y., & Agetsuma, N. (2013). The relationships between feeding-group size and feeding rate vary from positive to negative with characteristics of food items in wild Japanese macaques (Macaca fuscata). Behaviour, 150, 175-197. doi:10.1163/1568539X-00003044

Kelaita, M., Dias, P. A. D., Aguilar-Cucurachi, M. S., Canales-Espinosa, D., & Cortes-Ortiz, L. (2011). Impact of intrasexual selection on sexual dimorphism and testes size in the mexican howler monkeys Alouatta palliata and A. pigra. American Journal of Physical Anthropology, 146, 179-187. doi:10.1002/ajpa.21559

King, A. J., Isaac, N. J. B., & Cowlishaw, G. (2009). Ecological, social, and reproductive factors shape producer-scrounger dynamics in baboons. Behavioral Ecology, 20, 1039-1049. doi:10.1093/beheco/arp095

Koenig, A. (2000). Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behavioral Ecology Sociobiology, 48, 93-109. doi:10.1007/s002650000198

Kowalewski, M. M. (2007). Patterns of affiliation and co-operation in howler monkeys: an alternative model to explain social organization in non-human primates. PhD dissertation. Urbana, IL: University of Illinois.

Leighton, M. (1993). Modeling dietary selectivity by Bornean orangutans - evidence for integration of multiple criteria in fruit selection. International Journal of Primatology, 14, 257-313. doi:10.1007/BF02192635

Leighton, M., & Leighton, D. R. (1982). The relationship of size of feeding aggregate to size of food patch: howler monkeys (Alouatta palliata) feeding in Trichilia cipo fruit trees on Barro Colorado Island. Biotropica, 14, 81-90. doi:10.2307/2387735

Levey, D. J., & Martinez del Rio, C. (2001). It takes guts (and more) to eat fruit: Lessons from avian nutritional ecology. Auk, 118, 819-831. doi:10.2307/4089834

Marshall, H. H., Carter, A. J., Coulson, T., Rowcliffe, J. M., Cowlishaw, G. (2012). Exploring foraging decisions in a social primate using discrete-choice models. American Naturalist, 180, 481-495. doi:10.1086/667587

Martin, P., & Bateson, P. (2007). Measuring Behaviour. an Introductory Guide. Cambridge, UK: Cambridge University Press.

Milton, K. (1980). The Foraging Strategy of Howler Monkeys: A Study in Primate Economics. New York: Columbia University Press.

Peres, C. A. (1996). Food patch structure and plant resource partitioning in interspecific associations of Amazonian tamarins. International Journal of Primatology, 17, 695-723. doi:10.1007/BF02735261

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team (2019). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-143, https://CRAN.R-project.org/package=nlme.

Plante, S., Colchero, F., & Calmé, S. (2014). Foraging strategy of a Neotropical primate: how intrinsic and extrinsic factors influence destination and residence time. Journal of Animal Ecology, 83, 116-125. doi: 10.1111/1365-2656.12119

R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

Righini, N., Garber, P. A., & Rothman, J. M. (2017). The effects of plant nutritional chemistry on food selection of Mexican black howler monkeys (Alouatta pigra): the role of lipids. American Journal of Primatology, 79, e22524. doi:10.1002/ajp.22524

Roberts, M. T., Bermingham, E. N., Cave, N. J., Young, W., McKenzie, C. M., & Thomas, D. G. (2018). Macronutrient intake of dogs, self‐selecting diets varying in composition offered ad libitum. Journal of Animal Physiology and Animal Nutrition,102, 568-575. doi:10.1111/jpn.12794

Rothman, J. M., Chapman, C. A., & Pell, A. N. (2008). Fiber-bound nitrogen in gorilla diets: Implications for estimating dietary protein intake of primates. American Journal of Primatology, 70, 690-694. doi:10.1002/ajp.20540

Rothman, J. M., Chapman, C. A., & Van Soest, P. J. (2012). Methods in Primate Nutritional Ecology: A User's Guide. International Journal of Primatology, 33, 542-566. doi:10.1007/s10764-011-9568-x

Simpson, S. J., & Raubenheimer, D. (2012). The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity. Princeton: Princeton University Press.

Snaith, T. V., & Chapman, C. A. (2005). Towards an ecological solution to the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles). Behavioral Ecology and Sociobiology, 59, 185-190. doi:10.1007/s00265-005-0023-x

Snaith, T. V., & Chapman, C. A. (2007). Primate group size and interpreting sociolecological models: Do folivores really play by different rules? Evolutionary Anthropology, 16, 94-106. doi:10.1002/evan.20132

Snaith, T. V., & Chapman, C. A. (2008). Red colobus monkeys display alternative behavioral responses to the costs of scramble competition. Behavioral Ecology, 19, 1289-1296. doi:10.1093/beheco/arn076

StatSoft, Inc. (2011). STATISTICA. Data Analysis Software System.

Stephens, D. W, & Krebs, J. R. (1986). Foraging Theory. Princeton, NJ: Princeton University Press.

Stephens, D. W., Brown, J. S., & Ydenberg, R. C. (2007). Foraging: Behavior and Ecology. Chicago: University of Chicago Press.

Tombak, K. J., Reid, A. J., Chapman, C. A., Rothman, J. M., Johnson, C. A., & Reyna-Hurtado, R. 2012. Patch depletion behavior differs between sympatric folivorous primates. Primates, 53, 57-64. doi:10.1007/s10329-011-0274-2

Tujague, M. P., & Lahitte, H. B. (2013). Secuencias de forrajeo en monos capuchinos en cautiverio: Aprendizaje y memoria en contexto de grupo. Revista Mexicana de Análisis de la Conducta, 39, 39-55. doi:10.5514/rmac.v39.i3.63926

Tujague, M. P., Bacigalupe, M. Á., Lahitte, H. B., & Janson, C. (2016). Memoria espacial en monos capuchinos de Argentina: un estudio observacional en vida silvestre. Revista Argentina de Antropología Biológica, 18, 1-13. doi:10.17139/raab.2016.0018.01.01

van Hooff, J., & van Schaik, C. (1992). Cooperation in competition: the ecology of primate bonds. In A. H. Harcourt & F. B. M. de Waal (Eds.), Coalitions and Alliances in Humans and Other Animals. Oxford: Oxford Science Publications.

Wang, E., & Milton, K. (2003). Intragroup social relationships of male Alouatta palliata on Barro Colorado Island, Republic of Panama. International Journal of Primatology, 24, 1227-1243. doi:10.1023/B:IJOP.0000005989.29238.ce

Ydenberg, R. C., Brown, J. S., & Stephens, D. W. (2007). Foraging: an overview. In D. W. Stephens, J. S. Brown & R. C. Ydenberg (Eds.), Foraging: Behavior and Ecology. Chicago: University of Chicago Press.

Zuur, A., Ieno, E., & Meester,s E. (2009). A Beginner's Guide to R. New York: Springer. 218 p.




DOI: http://dx.doi.org/10.22201/fesi.20070780e.2020.12.2.76795