Skip to main content
SpringerLink
Log in

Digestive strategies and food choice in mantled howler monkeys Alouatta palliata mexicana: bases of their dietary flexibility

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Mantled howler monkeys (Alouatta palliata) occupy a wide variety of tropical habitats and are the most folivorous of New World primates. However, their diet may include fruits, buds, petioles, and flowers, as well as leaves, suggesting they must cope with variations in the nutrient composition of their food. We studied the physiological basis of the dietary flexibility of these monkeys by comparing food choice, digestive performance and patterns of digesta flow in six adults, fed diets of either leaves or a mixture of fruit and leaves. Although monkeys ate similar amounts of the two diets, they ingested more digestible protein when offered the leaf diet, on which they lost body mass, but they ingested much more soluble sugars when offered fruit and leaves on which they gained mass. Digestibilities of dry matter, fat, energy and fibre did not differ between diets, but those of crude protein, soluble sugars and minerals were higher on the fruit–leaf diet. Mean retention times in the gut of solute (Co-EDTA) and particulate markers (Cr-mordanted cell walls) did not differ between diets, but on both diets the monkeys retained the particulate marker (mean retention time ca 55 h) for longer than they did the solute marker (MRT ca 50 h). A lack of selective retention of solutes and small particles in the gastro-intestinal tract of howler monkeys probably restricts them to mixed diets but their digestive strategy is sufficiently flexible to allow them to feed on a diet of leaves when fruit is unavailable.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

DM:

Dry matter

WM:

Wet matter

OM:

Organic matter

CT:

Condensed tannins

DEI:

Digestible energy intake

N:

Nitrogen

NDF:

Neutral detergent fibre

ADF:

Acid detergent fibre

SS:

Soluble sugars

MRT:

Mean retention time

TT:

Transit time

SRI:

Selective retention index

References

  • Balch CC (1950) Factors affecting the utilization of food by dairy cows. 1. The rate of passage of food through the digestive tract. Br J Nutr 4:361–388

    Article  CAS  PubMed  Google Scholar 

  • Baumgarten A, Williamson GB (2007) The distributions of howling monkeys (Alouatta pigra and A. palliata) in southeastern Mexico and Central America. Primates 48:310–315

    Article  PubMed  Google Scholar 

  • Bergero D, Tarantola M, Bassano B (2000) Feeding strategy for coprophagy events in a sport horses stable. Obiettivi e Documenti Veterinari 21:31–35

    Google Scholar 

  • Bozinovic F, Calosi P, Spicer JI (2011) Physiological correlates of geographic range in animals. Annu Rev Ecol Evol Syst 42:155–179

    Article  Google Scholar 

  • Campbell JL, Eisemann JH, Glander KE, Crissey SD (1999) Intake, digestibility, and passage of a commercially designed diet by two propithecus species. Am J Primatol 48:237–246

    Article  CAS  PubMed  Google Scholar 

  • Caton JM (1997) Digestive strategies of nonhuman primates. Ph.D. thesis, The Australian National University, Canberra

  • Caton JM (1999) Digestive strategy of the Asian colobine genus Trachypithecus. Primates 40:311–325

    Article  Google Scholar 

  • Cipollini ML (2000) Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Rev Chil Hist Nat 73:421–440

    Article  Google Scholar 

  • Clauss M, Polster C, Kienzle E, Wiesner H, Baumgartner K, von Houwald F, Ortmann S, Streich WJ, Dierenfeld ES (2005) Studies on digestive physiology and feed digestibilities in captive Indian rhinoceros (Rhinoceros unicornis). J Anim Physiol Anim Nutr 89:229–237

    Article  CAS  Google Scholar 

  • Clauss M, Lang-Deuerling S, Müller DWH, Kienzle E, Steuer P, Hummel J (2010) Retention of fluid and particles in captive tapirs (Tapirus spp.). Comp Biochem Physiol A Mol Integr Physiol 157:95–101

    Article  PubMed  Google Scholar 

  • Coltrane JA, Barboza PS (2010) Winter as a nutritional bottleneck for North American porcupines (Erethizon dorsatum). J Comp Physiol B 180:905–918

    Article  PubMed  Google Scholar 

  • Cork SJ, Foley WJ (1991) Digestive and metabolic strategies of arboreal mammalian folivores in relation of chemical defenses in temperate and tropical forest. In: Palo TR, Robbins CT (eds) Plant defenses against mammalian herbivory. CRC Press, Boca Raton, pp 133–166

    Google Scholar 

  • Crockett CM (1998) Conservation biology of the genus Alouatta. Int J Primatol 19:549–578

    Article  Google Scholar 

  • Crockett CM, Eisenberg JF (1987) Howlers: variations in group size and demography. In: Primate Societies. University of Chicago Press, Chicago, pp 54–68

  • Dellow DW, Hume ID (1982) Studies on the nutrition of macropodine marsupials. I. Intake and digestion of lucerne hay and fresh grass. Aust J Zool 30:391–398

    Article  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem (Wash) 28:350–356

    Article  CAS  Google Scholar 

  • Edwards MS, Ullrey DE (1999) Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. I. Ruffed lemurs (Varecia variegata vauiegata and V-v. rubra). Zoo Biol 18:529–536

    Article  Google Scholar 

  • Eisenberg JF (1979) Habitat, economy and society: some correlations and hypotheses for the Neotropical primates. In: Bernstein IS, Smith EO (eds) Primate ecology and human origins. Garland STPM, New York, pp 215–262

    Google Scholar 

  • Eisenberg JF, Rudran R, Muckenhirn NA (1972) Relation between ecology and social structure in primates. Science 176:863–874

    Article  CAS  PubMed  Google Scholar 

  • Espinosa-Gómez FC (2008) Estrategias digestivas del mono aullador negro (Alouatta pigra) en dos fragmentos con diferente grado de perturbación. M.Sc. thesis, University of Veracruz, Veracruz

  • Fekete S, Bokori J (1985) Effect of zootrichobezoar on the digestibility coefficients and fattening indexes of rabbits. Magy Allatorv Lapja 40:735–736

    Google Scholar 

  • Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, Wood JT, Wallis IR, Lindenmayer DB (2009) Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 20:685–690

    Article  Google Scholar 

  • Gibson LA, Hume ID (2000) Digestive performance and digesta passage in the omnivorous greater bilby, Macrotis lagotis (Marsupialia: Peramelidae). J Comp Physiol B 170:457–467

    Article  CAS  PubMed  Google Scholar 

  • Groves CP (2001) Primate Taxonomy. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Hagerman AE, Butler LG (1994) Assay of condensed tannins or flavonoid oligomers and related flavonoids in plants. Oxyg Radic Biol Syst Pt D 234:429–437

    Article  CAS  Google Scholar 

  • Helrich K (1990) Official methods of analysis of the association of official analytical chemist, 15th edn. Association of Official Analytical Chemist, Arlington

    Google Scholar 

  • Hladik CM (1967) Surface relative du tractus digestif de quelques primates. Morphologie des velosités intestinales et corrélations avec la régime alimentaire. Mammalia 31:120–147

    Article  Google Scholar 

  • Holleman DF, White RG (1989) Determination of digesta fill and passage rate from nonabsorbed particulate phase markers using the single dosing method. Can J Zool/Rev Can Zool 67:488–494

    Article  Google Scholar 

  • Hume ID (1989) Optimal digestive strategies in mammalian herbivores. Physiol Zool 62:1145–1163

    Google Scholar 

  • Hume ID (2002) Digestive strategies of mammals. Acta Zool Sin/Dongwu Xuebao 48:1–19

    CAS  Google Scholar 

  • Hume ID (2004) Concepts of digestive efficiency. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield

    Google Scholar 

  • IUCN (1998) IUCN position statement on the translocation of living organisms. In: 22nd meeting of the IUCN Council in Gland, Switzerland on 4th September, 1987

  • Karasov WH (1996) Digestive plasticity in avian energetics and feeding ecology. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 61–84

    Chapter  Google Scholar 

  • Karasov WH, Martínez del Río C (2007) Physiological ecology, How animals process energy, nutrients and toxins. Princeton University Press, Princeton

    Google Scholar 

  • Karasov WH, McWilliams SR (2005) Digestive constraints in mammalian and avian ecology. In: Starck JM, Wang T (eds) Physiological adaptations to feeding in vertebrates. Science Publishers, Enfield, pp 87–112

    Google Scholar 

  • Kotb R, Luckey TD (1972) Markers in nutrition. Nutr Abstr Rev 42:813–845

    CAS  PubMed  Google Scholar 

  • Krockenberger AK, Hume ID (2007) A flexible digestive strategy accommodates the nutritional demands of reproduction in a free-living folivore, the koala (Phascolarctos cinereus). Funct Ecol 21:748–756

    Article  Google Scholar 

  • Kuijper DPJ, van Wieren SE, Bakker JP (2004) Digestive strategies in two sympatrically occurring lagomorphs. J Zool 264:171–178

    Article  Google Scholar 

  • Lechner I, Barboza P, Collins W, Fritz J, Günther D, Hattendorf B, Hummel J, Südekum K-H, Clauss M (2010) Differential passage of fluids and different-sized particles in fistulated oxen (Bos primigenius f. taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces): rumen particle size discrimination is independent from contents stratification. Comp Biochem Physiol A Mol Integr Physiol 155:211–222

    Article  PubMed  Google Scholar 

  • Marsh KJ, Wallis IR, Foley WJ (2005) Detoxification rates constrain feeding in common brushtail possums (Trichosurus vulpecula). Ecology 86:2946–2954

    Article  Google Scholar 

  • Miller RO (1998) Nitric-perchloric acid wet digestion in an open vessel. In: Kalra YP (ed) Handbook of reference methods for plant analysis. CRC Press, Boca Raton, pp 57–61

    Google Scholar 

  • Milton K (1978) Behavioral adaptations to leaf-eating by the mantled howler monkey. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Press, Washington, DC

    Google Scholar 

  • Milton K (1979) Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat 114:362–378

    Article  CAS  Google Scholar 

  • Milton K (1980) The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York

    Google Scholar 

  • Milton K (1981) Food choice and digestive strategies of two sympatric primate species. Am Nat 117:496–505

    Article  Google Scholar 

  • Milton K (1998) Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. Int J Primatol 19:513–548

    Article  Google Scholar 

  • Milton K, McBee RH (1983) Rates of fermentative digestion in the howler monkey, Alouatta palliata (primates, Ceboidea). Comp Biochem Physiol A Physiol 74:29–31

    Article  CAS  Google Scholar 

  • Milton K, Casey T, Casey K (1979) The basal metabolism of the mantled howler monkey (Alouatta palliata). J Mammal 60:373–376

    Article  Google Scholar 

  • Milton K, Van Soest PJ, Robertson JB (1980) Digestive efficiencies of wild howler monkeys. Physiol Zool 53:402–409

    Google Scholar 

  • Mueller DWH, Caton JM, Codron D, Schwarm A, Lentle R, Streich WJ, Hummel J, Clauss M (2011) Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores. Comp Biochem Physiol A: Mol Integr Physiol 160:207–220

    Article  CAS  Google Scholar 

  • Nagy KA, Milton K (1979) Energy-metabolism and food-consumption by wild howler monkeys (Alouatta-palliata). Ecology 60:475–480

    Article  Google Scholar 

  • Pei YX, Wang DH, Hume ID (2001) Selective digesta retention and coprophagy in Brandt’s vole (Microtus brandti). J Comp Physiol B 171:457–464

    Article  CAS  PubMed  Google Scholar 

  • Quan-Sheng L, De-Hua W (2007) Effects of diet quality on phenotypic flexibility of organ size and digestive function in Mongolian gerbils (Meriones unguiculatus). J Comp Physiol B 177:509–518

    Article  Google Scholar 

  • Reynolds V, Plumptre AJ, Greenham J, Harborne J (1998) Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Oecologia 115:331–336

    Google Scholar 

  • Rogers ME, Maisels F, Williamson EA, Fernandez M, Tutin CEG (1990) Gorilla diet in the Lope Reserve, Gabon: a nutritional analysis. Oecologia 84:326–339

    Google Scholar 

  • Rothman JM, Raubenheimer D, Chapman CA (2011) Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biol Lett 7:847–849

    Article  CAS  PubMed  Google Scholar 

  • Sakaguchi E, Kaizu K, Nakamichi M (1992) Fiber digestion and digesta retention from different physical forms of the feed in the rabbit. Comp Biochem Physiol A Physiol 102:559–563

    Article  CAS  Google Scholar 

  • Sassi PL, Caviedes-Vidal E, Anton R, Bozinovic F (2010) Plasticity in food assimilation, retention time and coprophagy allow herbivorous cavies (Microcavia australis) to cope with low food quality in the Monte desert. Comp Biochem Physiol A: Mol Integr Physiol 155:378–382

    Article  Google Scholar 

  • Sawada A, Sakaguchi E, Hanya G (2011) Digesta passage time, digestibility, and total gut fill in captive Japanese Macaques (Macaca fuscata): effects food type and food intake level. Int J Primatol 32:390–405

    Article  Google Scholar 

  • Schurg WA, Frei DL, Cheeke PR, Holtan DW (1977) Utilization of whole corn plant pellets by horses and rabbits. J Anim Sci 45:1317–1321

    Google Scholar 

  • Sibly RM (1981) Strategies of digestion and defecation. In: Townsend CR, Calow P (eds) Physiological ecology: an evolutionary approach to resource use. Blackwell Scientific Publications, Oxford, pp 109–139

    Google Scholar 

  • Simpson SJ, Raubenheimer D (1999) Assuaging nutritional complexity: a geometrical approach. Proc Nutr Soc 58:779–789

    Article  CAS  PubMed  Google Scholar 

  • Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system, 2nd edn. Cambridge University Press, New York

    Google Scholar 

  • Uden P, Colucci PE, Vansoest PJ (1980) Investigation of chromium, cerium and cobalt as markers in digesta—rate of passage studies. J Sci Food Agric 31:625–632

    Article  CAS  PubMed  Google Scholar 

  • Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597

    Article  PubMed  Google Scholar 

  • Warner ACI (1981) Rate of passage of digesta through the gut of mammals and birds. Nutr Abstr Rev 51:789–820

    Google Scholar 

  • Weiner J (1992) Physiological limits to sustainable energy budgets in birds and mammals—ecological implications. Trends Ecol Evol 7:384–388

    Article  CAS  PubMed  Google Scholar 

  • Willard JG, Willard JC, Wolfram SA, Baker JP (1977) Effect of diet on cecal pH and feeding behavior of horses. J Anim Sci 45:87–93

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by CONACYT-FOMIX 109499 “Capacidad de detoxificación y estrategias digestivas en Ateles geoffroyi y Alouatta palliata”. FEG was supported by CONACYT Scholarship 171093. We especially appreciate the work and dedication of the field assistants: Gildardo Castañeda, Antonio Jauregui, Rubén Mateo y Denedi García. We thank the Instituto de Neuroetología of Universidad Veracuzana and Centro Nacional de Investigación Disciplinaria en Fisiología y Mejoramiento Animal of INIFAP for all facilities granted. This article benefited from insightful comments and suggestions by Professor Ian Hume who read and commented on earlier versions of this article.

Ethical standards

This work complies with the current laws of Mexico. The monkeys were captured under the guidelines of the IUCN (1998) and the Mexican authority for the “Translocation of Mexican howler monkey program” by the Universidad Veracruzana (General Management of Wildlife SGPA/DGVS/02315/07) and held under the legal and ethical requirements of the Mexican Government (Official Journal of the Federation, 1999).

Author information

Authors and Affiliations

  1. Instituto de Neuroetología, Universidad Veracruzana, Av. Dr. Luis Castelazo s/n Col. Industrial Animas, Xalapa, Veracruz, C.P. 91160, Mexico

    Fabiola Espinosa-Gómez, Domingo Canales-Espinosa & Laura Hernández-Salazar

  2. Centro Nacional de Investigación Disciplinaria en Fisiología y Mejoramiento Animal, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Ajuchitlán, Querétaro, Mexico

    Sergio Gómez-Rosales

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

    Ian R. Wallis

Authors
  1. Fabiola Espinosa-Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergio Gómez-Rosales
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ian R. Wallis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Domingo Canales-Espinosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laura Hernández-Salazar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Hernández-Salazar.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Espinosa-Gómez, F., Gómez-Rosales, S., Wallis, I.R. et al. Digestive strategies and food choice in mantled howler monkeys Alouatta palliata mexicana: bases of their dietary flexibility. J Comp Physiol B 183, 1089–1100 (2013). https://doi.org/10.1007/s00360-013-0769-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-013-0769-9

Keywords

Search

Navigation