Howler Monkeys pp 229-258 | Cite as

The Howler Monkey as a Model for Exploring Host-Gut Microbiota Interactions in Primates

  • Katherine R. AmatoEmail author
  • Nicoletta Righini
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


The mammalian gut microbiota is essential to many aspects of host physiology, including nutrition, metabolic activity, and immune homeostasis. Despite the existence of numerous studies of the impact of the gut microbiota on human health and disease, much work remains to be done to improve our understanding of the host-microbe relationship in nonhuman primates. Howler monkeys (Alouatta spp.) are highly dependent on the gut microbiota for the breakdown of plant structural carbohydrates, and in this chapter we use new data describing the gut microbiome of captive and wild black howler monkeys (A. pigra) to develop and test two models of host-microbe interactions and bioenergetics. Improving our understanding of how spatial and temporal fluctuations in diet affect the nonhuman primate gut microbiota, and how this in turn influences host nutrition and physiology, has important implications for the study of the role that the gut microbiota plays in primate ecology, health, and conservation.


Gut microbiome Health Nutrition Growth Reproduction 


El papel de la microbiota intestinal es fundamental para muchos aspectos de la fisiología de los mamíferos, incluyendo la nutrición, la actividad metabólica y la homeostasis del sistema inmune. A pesar de la existencia de muchos estudios acerca de la microbiota intestinal humana debido a sus implicaciones para la salud, aún queda mucho por hacer para poder entender la relación huésped-microorganismos en primates no humanos. Los monos aulladores (Alouatta spp.) dependen de manera importante de los microbios intestinales para la digestión de los carbohidratos estructurales de las plantas. En este capítulo utilizamos nuevos datos sobre la composición de la microbiota de monos aulladores negros cautivos y silvestres (A. pigra) para desarrollar y poner a prueba dos modelos sobre las interacciones huésped-microbios desde un punto de vista ecológico y bioenergético. El análisis del efecto de las fluctuaciones espaciales y temporales de la dieta sobre la microbiota intestinal de los primates, y de cómo esto a su vez se refleja en la nutrición y fisiología del huésped, tiene implicaciones importantes para entender el papel de la microbiota en la ecología, salud y conservación de los primates.



We would like to thank A. Estrada and Universidad Nacional Autónoma de México for logistic support. Thanks are also due to R. Mackie for use of lab supplies and space at the University of Illinois. Research was carried out under permits from the Mexican environmental agencies, the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT), the Comisión Nacional de Áreas Naturales Protegidas (CONANP), and the Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP). The Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA) in Mexico and the Center for Disease Control in the U.S. provided permits for sample transport. We acknowledge the helpful comments of P. Garber and one anonymous reviewer on this manuscript. This project was funded by the NSF grant #0935347 (HOMINID). Fieldwork and preliminary lab work were funded by grants from the University of Illinois (Beckman, Tinker, and the Program in Ecology, Evolution and Conservation Biology) to KRA. KRA was supported by an NSF Graduate Research Fellowship. 16S sequence data are available from the authors upon request.


  1. Aiello LC, Wells JCK (2002) Energetics and the evolution of the genus Homo. Annu Rev Anthropol 31:323–338Google Scholar
  2. Altmann J, Alberts S (1987) Body mass and growth rates in a wild primate population. Oecologia 72:15–20Google Scholar
  3. Altmann J, Samuels A (1992) Costs of maternal care: infant-carrying in baboons. Behav Ecol Sociobiol 29:391–398Google Scholar
  4. Altmann SA (2009) Fallback foods, eclectic omnivores, and the packaging problem. Am J Phys Anthropol 140:615–629PubMedGoogle Scholar
  5. Amato KR (2013) Black howler monkey (Alouatta pigra) nutrition: integrating the study of behavior, feeding ecology, and the gut microbial community. Ph.D. dissertation, Program in Ecology, Evolution and Conservation Biology, University of Illinois, UrbanaGoogle Scholar
  6. Amato KR, Yeoman CJ, Kent A, Carbonero F, Righini N, Estrada AE, Gaskins HR, Stumpf RM, Yildirim S, Torralba M, Gillis M, Wilson BA, Nelson KE, White BA, Leigh SR (2013) Habitat degradation impacts primate gastrointestinal microbiomes. ISME J 7: 1344-1353PubMedCentralPubMedGoogle Scholar
  7. Amato KR, Yeoman CJ, Kent A, Righini N, Estrada AE, Stumpf RM, Yildirim S, Torralba M, Gillis M, Wilson BA, Nelson KE, White BA, Leigh SR (in review) Habitat degradation impacts primate gastrointestinal microbiomes.Google Scholar
  8. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D (2009) Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in aneroxic patients. PLoS One 4:e7125PubMedCentralPubMedGoogle Scholar
  9. Arroyo-Rodriguez V, Asensio N, Cristobal-Azkarate J (2008) Demography, life history and migrations in a Mexican mantled howler group in a rainforest fragment. Am J Primatol 70:114–118PubMedGoogle Scholar
  10. Arroyo-Rodriguez V, Dias PAD (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1–16PubMedGoogle Scholar
  11. Bailey M, Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35:146–155PubMedGoogle Scholar
  12. Barboza PS, Parker KL, Hume ID (2009) Integrative wildlife nutrition. Springer, BerlinGoogle Scholar
  13. Bauer E, Williams BA, Smidt H, Verstegen MW, Mosenthin R (2006) Influence of the gastrointestinal microbiota on development of the immune system in young animals. Curr Issues Intest Microbiol 7:35–51PubMedGoogle Scholar
  14. Behie AM, Pavelka MS (2005) The short-term effects of a hurricane on the diet and activity of black howlers (Alouatta pigra) in Monkey River, Belize. Folia Primatol 76:1–9PubMedGoogle Scholar
  15. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, Zhang M, Oh PL, Nehrenberg D, Hua K, Kachman SD, Moriyama EN, Walter J, Peterson DA, Pomp D (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A 107:18933–18938PubMedCentralPubMedGoogle Scholar
  16. Benveniste J, Lespinats G, Adam C, Salomon JC (1971a) Immunoglobulins in intact, immunized, and contaminated axenic mice: study of serum IgA. J Immunol 107:1647–1655PubMedGoogle Scholar
  17. Benveniste J, Lespinats G, Salomon JC (1971b) Serum and secretory IgA in axenic and holoxenic mice. J Immunol 108:1656–1662Google Scholar
  18. Bicca-Marques JC (2003) How do howler monkeys cope with habitat fragmentation? In: Marsh LK (ed) Primates in Fragments: Ecology and Conservation Kluwer Academic, New YorkGoogle Scholar
  19. Bjorkholm B, Bok CM, Lundin A, Rafter J, Hibberd ML, Pettersson S (2009) Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS One 4:e6958PubMedCentralPubMedGoogle Scholar
  20. Bo X, Zun-Xi H, Xiao-Yan W, Run-Chi G, Xiang-Hua T, Yue-Lin M, Yun-Juan Y, Hui S, Li-Da Z (2010) Phylogenetic analysis of the fecal flora of the wild pygmy loris. Am J Primatol 72:699–706PubMedGoogle Scholar
  21. Bonilla-Sanchez YM, Serio-Silva JC, Pozo-Montuy G, Chapman CA (2012) Howlers are able to survive in Eucalyptus plantations where remnant and regenerating vegetation is available. Int J Primatol 33:233–245Google Scholar
  22. Bovee-Oudenhoven IM, Wissink ML, Wouters JT, Van der Meer R (1999) Dietary calcium phosphate stimulates intestinal Lactobacilli and decreases the severity of a Salmonella infection in rats. J Nutr 129:607–612PubMedGoogle Scholar
  23. Bradley BJ, Stiller M, Doran-Sheehy DM, Harris T, Chapman CA, Vigilant L, Poinar H (2007) Plant DNA sequences from feces: potential means for assessing diets of wild primates. Am J Primatol 69:699–705PubMedGoogle Scholar
  24. Brourton MR, Perrin MR (1991) Comparative gut morphometrics of Vervet (Cercopithecus aethiops) and Samango (C. mitis erytharchus) monkeys. Z Saugetierkunde 56:65–71Google Scholar
  25. Buhnik-Rosenblau K, Danin-Poleg Y, Kashi Y (2011) Host genetics and gut microbiota. In: Rosenberg E, Gophna U (eds) Beneficial Microorganisms in Multicellular Life Forms. Springer, BerlinGoogle Scholar
  26. Carbonero F, Benefiel AC, Gaskins HR (2012) Contributions of the microbial hydrogen economy on colonic homeostasis. Nat Rev Gasteroenterol Hepatol 9:504–518Google Scholar
  27. Cavedon K, Leschine SB, Canale-Parola E (1990) Cellulase system of a free-living mesophilic Clostridium (strain C7). J Bacteriol 172:4222–4230PubMedCentralPubMedGoogle Scholar
  28. Chaney AL, Marbach EP (1962) Modified reagents for the determination of urea and ammonia. Clin Chem 8:130–132PubMedGoogle Scholar
  29. Chilvers BL, Wilkinson IS (2009) Diverse foraging strategies in lactating New Zealand sea lions. Marine Ecol 378:299–308Google Scholar
  30. Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 166:337–386PubMedGoogle Scholar
  31. Chivers DJ, Langer P (1994) Gut form and function: variations and terminology. In: Chivers DJ, Langer P (eds) The Digestive System in Mammals: Food, Form and Function. Cambridge University, CambridgeGoogle Scholar
  32. Clark KR, Gorley RN. (2006). PRIMER v6: User Manual/Tutorial. PRIMER-E, PlymouthGoogle Scholar
  33. Clayton JB, Kim HB, Glander K, Isaacson RE, Johnson TJ (2012) Fecal bacterial diversity of wild mantled howling monkeys (Alouatta palliata). Am J Phys Anthropol 147:116Google Scholar
  34. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA (2012) An application of ecological theory toward an understanding of the human microbiome. Science 336:1255–1262PubMedCentralPubMedGoogle Scholar
  35. Cristobal-Azkarate J, Arroyo-Rodriguez V (2007) Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. Am J Primatol 69:1013–1029PubMedGoogle Scholar
  36. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nat 505:559–566Google Scholar
  37. Deschner T, Kratzsch J, Hohmann G (2008) Urinary c-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). Horm Behav 54:620–626PubMedGoogle Scholar
  38. Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811–818PubMedGoogle Scholar
  39. Di Fiore A, Link A, Campbell C (2011) The atelines: behavioral and socioecological diversity in a New World radiation. In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in Perspective, vol 2. Oxford University, OxfordGoogle Scholar
  40. Dias PAD, Rangel-Negrin A, Canales-Espinosa D (2011) Effects of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra). Am J Phys Anthropol 145:137–146PubMedGoogle Scholar
  41. Donnet-Hughes A, Perez PF, Dore J, Leclerc M, Levenez F, Benyacoub J, Serrant P, Segura-Roggero I, Schiffrin EJ (2010) Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nutr Soc 69:407–415PubMedGoogle Scholar
  42. Dunn JC, Cristobal-Azkarate J, Vea JJ (2009) Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. Am J Primatol 71:654–662PubMedGoogle Scholar
  43. Eckert KA, Hahn NE, Genz AK, Kitchen DM, Stuart MD, Averbeck GA, Stromberg BE, Markowitz H (2006) Coprological surveys of Alouatta pigra at two sites in Belize. Int J Primatol 27:227–238Google Scholar
  44. Edwards MS, Ullrey DE (1999) Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut- and foregut-fermenting folivores. Zoo Biol 18:537–549Google Scholar
  45. Erwin ES, Marco GJ, Emery EM (1961) Volatile fatty acid analysis of blood and rumen fluid by gas chromatography. J Dairy Sci 44:1768–1771Google Scholar
  46. Fedigan LM, Rose LM (1995) Interbirth interval variation in three sympatric species of neotropical monkey. Am J Primatol 37:9–24Google Scholar
  47. Fischer SG, Lerman LS (1979) Length-independent separation of DNA restriction fragments in two-dimensional gel electrophoresis. Cell 16:191–200PubMedGoogle Scholar
  48. Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636PubMedCentralPubMedGoogle Scholar
  49. Flint HJ, Bayer EA (2008) Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract. Ann N Y Acad Sci 1125:280–288PubMedGoogle Scholar
  50. Flint HJ, Duncan SH, Louis P (2011) Impact of intestinal microbial communities upon health. In: Rosenberg E, Gophna U (eds) Beneficial Microorganims in Multicellular Life Forms. Springer, BerlinGoogle Scholar
  51. Fons M, Gomez A, Karjalainen T (2000) Mechanisms of colonisation resistance of the digestive tract. Part 2: bacteria/bacteria interactions. Microb Ecol Health Dis 12:240–246Google Scholar
  52. Foster JA, McVey Neufeld KA (2013) Gut-brain axis: How the microbiome influences anxiety and depression. Cell 36:305–312Google Scholar
  53. Forsythe P, Sudo N, Dinan T, Taylor VH, Bienenstock J (2010) Mood and gut feelings. Brain Behav Immun 24:9–16PubMedGoogle Scholar
  54. Frey JC, Rothman JM, Pell AN, Nizeyi JB, Cranfield MR, Angert ER (2006) Fecal bacterial diversity in a wild gorilla. Appl Environ Microbiol 72:3788–3792PubMedCentralPubMedGoogle Scholar
  55. Friswell MK, Gika H, Stratford IJ, Theodoridis G, Telfer B, Wilson ID, McBain AJ (2010) Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS One 5:e8584PubMedCentralPubMedGoogle Scholar
  56. Fujita S, Kageyama T (2007) Polymerase chain reaction detection of Clostridium perfringens in feces from captive and wild chimpanzees, Pan troglodytes. J Med Primatol 36:25–32PubMedGoogle Scholar
  57. Girard-Buttoz C, Higham JP, Heistermann M, Wedegartner S, Maestripieri D, Engelhardt A (2011) Urinary c-peptide measurement as a marker of nutritional status in macaques. PLoS One 6:e18042PubMedCentralPubMedGoogle Scholar
  58. Grueter CC, Li DY, Ren BP, Wei FW, Xiang ZF, Van Schaik CP (2009) Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. Am J Phys Anthropol 140:700–715PubMedGoogle Scholar
  59. Hammond KA, Kristan DM (2000) Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol Biochem Zool 73:547–556PubMedGoogle Scholar
  60. Harris TR, Chapman CA, Monfort SL (2009) Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. Behav Ecol 21:46–56Google Scholar
  61. Havel PJ (1998) Leptin production and action: relevance to energy balance in humans. Am J Clin Nutr 67:355–356PubMedGoogle Scholar
  62. Hill MJ (1997) Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6:S43–S45PubMedGoogle Scholar
  63. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336:1268–1273PubMedGoogle Scholar
  64. Jaroszewska M, Wilczynska B (2006) Dimensions of surface area of alimentary canal of pregnant and lactating female common shrews. J Mammal 87:589–597Google Scholar
  65. Kau AL, Abern PP, Griffin NW, Goodman AL, Gordon JI (2011) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336PubMedCentralPubMedGoogle Scholar
  66. Kay RNB, Davies AG (1994) Digestive physiology. In: Davies AG, Oates JF (eds) Digestive physiology. Cambridge University, CambridgeGoogle Scholar
  67. Kelaita M, Dias PAD, Aguilar Cucurachi MS, Canales-Espinosa D, Cortés-Ortiz L (2011) Impact of intrasexual selection on sexual dimorphism and testes size in the Mexican howler monkeys Alouatta palliata and A. pigra. Am J Phys Anthropol 146:179–187Google Scholar
  68. Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AGP, Pettersson S, Conway S (2003) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-g and RelA. Nat Immun 5:104–112Google Scholar
  69. Kisidayova S, Varadyova Z, Pristas P, Piknova M, Nigutova K, Petrzelkova KJ, Profousova I, Schovancova K, Kamler J, Modry D (2009) Effects of high- and low-fiber diets on fecal fermentation and fecal microbial populations of captive chimpanzees. Am J Primatol 71:548–557PubMedGoogle Scholar
  70. Kleiber M (1975) The fire of life: an introduction to animal energetics. Krieger, HuntingtonGoogle Scholar
  71. Kruszynskia YT, Home PD, Hanning I, Alberti K (1987) Basal and 24-h c-peptide and insulin secretion rate in normal man. Diabetology 30:16–21Google Scholar
  72. Lambert JE (1998) Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20Google Scholar
  73. Lambert JE (2011) Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in Perspective, 2nd edn. Oxford University, New YorkGoogle Scholar
  74. Lambert JE, Fellner V (2012) In vitro fermentation of dietary carbohydrate consumed by african apes and monkeys: preliminary results for interpreting microbial and digestive strategy. Int J Primatol 33:263–281Google Scholar
  75. Lantz EL, Santymire RM, Murray CM, Heintz M, Lipende I, Travis DA, Lonsdorf EV (2011) Characterization of immunocompetence via immunoglobulin A in wild chimpanzees (Pan troglodytes schweinfurthii) at Gombe Stream National Park, Tanzania. Am J Primatol 73:52.Google Scholar
  76. Larimer SC, Fritzsche P, Song Z, Johnston J, Neumann K, Gattermann R, McPhee ME, Johnston RE (2011) Foraging behavior of golden hamsters (Mesocricetus auratus) in the wild. J Ethology 29:275–283Google Scholar
  77. Ley RE, Backhed F, Turnbaugh PJ, Lozupone C, Knight R, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102:11070–11075PubMedCentralPubMedGoogle Scholar
  78. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008a) Evolution of mammals and their gut microbes. Science 320:1647–1651PubMedCentralPubMedGoogle Scholar
  79. Ley RE, Lozupone C, Hamady M, Knight R, Gordon HA (2008b) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature 6:776–788Google Scholar
  80. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Human gut microbes associated with obesity. Nature 444:1022–1023PubMedGoogle Scholar
  81. Louis P, Scott KP, Duncan P, Flint HJ (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102:1197–1208PubMedGoogle Scholar
  82. Mackie RI (2002) Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integr Comp Biol 42:319–326PubMedGoogle Scholar
  83. Mackie RI, Gilchrist FMC, Robberts AM, Hannah PE, Schwartz HM (1978) Microbiological and chemical changes in the rumen during the stepwise adaptation of sheep to high concentrate diets. J Agric Sci 90:241–254Google Scholar
  84. Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69:1035S–1045SPubMedGoogle Scholar
  85. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P (2008) The immune geography of IgA induction and function. Nat Rev 1:11–22Google Scholar
  86. Marques S, Ramos JL (1993) Transcriptional control of the Pseudomonas putida TOL plasmid catabolic pathways. Mol Microbiol 9:923–929PubMedGoogle Scholar
  87. Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M (2009) Defining fallback foods and assessing their importance in primate ecology and evolution. Am J Phys Anthropol 140:603–614PubMedGoogle Scholar
  88. Martinez-Mota R, Valdespino C, Sanchez-Ramos MA, Serio-Silva JC (2007) Effects of forest fragmention on the physiological stress of black howler monkeys. Anim Cons 10:374–379Google Scholar
  89. McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University, IthacaGoogle Scholar
  90. McCord AI, Chapman CA, Weny G, Tumukunde A, Hyeroba D, Klotz K, Koblings AS, Mbora DNM, Cregger M, White BA, Leigh SR, Goldberg TL (2013) Fecal microbiomes of non-human primates in western Uganda reveal species-specific communities largely resistant to habitat perturbation. Am J Primatol Google Scholar
  91. Medani M, Collins D, Docherty NG, Baird AW, O’Connell PR, Winter DC (2011) Emerging role of hydrogen sulfide in colonic physiology and pathophysiology. Inflamm Bowel Dis 17:1620–1625PubMedGoogle Scholar
  92. Mellado M, Rodriguez A, Villareal JA, Olvera A (2005) The effect of pregnancy and lactation on diet composition and dietary preference of goats in a desert rangeland. Small Ruminant Res 58:79–85Google Scholar
  93. Meserve PL et al (2003) Thirteen years of shifting top-down and bottom-up control. Bioscience 53:633–646Google Scholar
  94. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson JF, Tougeot C, Pichelin M, Cazaubiel M, Cazaubiel JM (2010) Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 105:755–764PubMedGoogle Scholar
  95. Milton K (1980) The foraging strategy of howler monkeys. Columbia University, New YorkGoogle Scholar
  96. Milton K (1984) The role of food-processing factors in primate food choice. In: Rodman PS, Cant JGH (eds) Adaptations for foraging in nonhuman primates: Contribution to an organismal biology of prosimians, monkeys, and apes. Columbia University, New YorkGoogle Scholar
  97. Milton K, McBee RH (1983) Rates of fermentative digestion in the howler monkey, Alouatta Palliata (Primates: Ceboidea). Comp Biochem Physiol 74A:29–31Google Scholar
  98. Milton K, Van Soest P, Robertson J (1980) Digestive efficiencies of wild howler monkeys. Physiol Zool 53:402–409Google Scholar
  99. Moeller AH, Peeters M, Ndjango JB, Li Y, Hahn BH, Ochman H (2013) Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res 23: 1715–1720PubMedCentralPubMedGoogle Scholar
  100. Moreau MC, Ducluzeau R, Guy-Grand D, Muller MC (1978) Increase in the population of duodenal immunoglobulin a plasmocytes in axenic mice associated with different living or dead bacterial strain of intestinal origin. Infect Immun 21:532–539PubMedCentralPubMedGoogle Scholar
  101. Nagy KA, Milton K (1979) Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata). Ecology 60:475–480Google Scholar
  102. Nakamura N, Amato KR, Garber PA, Estrada AE, Mackie RI, Gaskins HR (2011) Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in Palenque National Park, Mexico. Am J Primatol 73:909–919PubMedGoogle Scholar
  103. Nakamura N, Leigh SR, Mackie RI, Gaskins HR (2009) Microbial community analysis of rectal methanogens and sulfate reducing bacteria in two non-human primate species. J Med Primatol 38:360–370PubMedGoogle Scholar
  104. Nakata PA, McConn MM (2007) Calcium oxalate content affects the nutritional availability of calcium from Medicago truncatula. Plant Sci 172:958–961Google Scholar
  105. Neish AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136:65–80PubMedCentralPubMedGoogle Scholar
  106. Norconk MA, Wright BW, Conklin-Brittain NL, Vinyard CJ (2009) Mechanical and nutritional properties of food as factors in platyrrhine dietary adaptations. In: Garber PA, Bicca-Marques JC, Estrada AE, Heymann EW, Strier KB (eds) South American Primates, Developments in Primatology: Progress and Prospects. Springer, New YorkGoogle Scholar
  107. O’Brien TG, Kinnaird M, Dierenfeld ES, Conklin-Brittain NL, Wrangham RW, Silver SC (1998) What’s so special about figs? Nature 392:668Google Scholar
  108. Ochman H, Worobey M, Kuo CH, Ndjango JBN, Peeters M, Hahn BH, Hugenholtz P (2010) Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8:e1000546PubMedCentralPubMedGoogle Scholar
  109. Oftedal OT, Whiten A, Southgate DAT, Van Soest P (1991) The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philos Trans R Soc Lond B Biol Sci 334:161–170PubMedGoogle Scholar
  110. Ohara H, Karita S, Kimura T, Sakka K, Ohmiya K (2000) Characterization of the cellulolytic complex (cellulosome) from Ruminococcus albus. Biosci Biotechnol Biochem 64:254–260PubMedGoogle Scholar
  111. Osborn AM, Morre RB, Timmis KN (2000) An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2:39–50PubMedGoogle Scholar
  112. Ostfeld RS, Keesing F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15:232–237PubMedGoogle Scholar
  113. Overdorff DJ, Strait SG, Telo A (1997) Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. Am J Primatol 43:211–223PubMedGoogle Scholar
  114. Pavelka MSM, Knopff KH (2004) Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: does degree of frugivory influence activity level? Primates 45:105–111PubMedGoogle Scholar
  115. Park AJ, Collins J, Blennerhassett P, Ghia JE, Verdu EF, Bercik P, Collins SM (2013) Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterology and Motility 25: 733–e575PubMedCentralPubMedGoogle Scholar
  116. Peles JD, Barrett GW (2008) The golden mouse: a model of energetic efficiency. In: Barrett GW, Feldhamer GA (eds) The Golden Mouse: Ecology and Conservation. Springer, New YorkGoogle Scholar
  117. Phillips KA, Abercrombie CL (2003) Distribution and conservation status of the primates of Trinidad. Primate Conserv 19:19–22Google Scholar
  118. Pozo-Montuy G, Serio-Silva JC, Bonilla-Sanchez YM (2011) Influence of the landscape matrix on the abundance of arboreal primates in fragmented landscapes. Primates 52:139–147PubMedGoogle Scholar
  119. Raguet-Schofield ML (2009) The ontogeny of feeding behavior of Nicaraguan mantled howler monkeys (Alouatta palliata). Ph.D. dissertation, Department of Anthropology University of Illinois, UrbanaGoogle Scholar
  120. Redford KH, Segre JA, Salafsky N, Martinez del Rio C, McAloose D (2012) Conservation and the microbiome. Conserv Biol 26:195–197PubMedCentralPubMedGoogle Scholar
  121. Righini N (2014) Primate nutritional ecology: the role of food selection, energy intake, and nutrient balancing in Mexican black howler monkey (Alouatta pigra) foraging strategies. Ph.D. dissertation, Department of Anthropology, University of Illinois at Urbana-Champaign, UrbanaGoogle Scholar
  122. Ronaghi M, Uhlen M, Nyren P (1998) A sequencing method based on real-time pyrophosphate. Science 281:363PubMedGoogle Scholar
  123. Rothman JM, Dierenfeld ES, Molina DO, Shaw AV, Hintz HF, Pell AN (2006) Nutritional chemistry of foods eaten by gorillas in Bwindi Impenetrable National Park, Uganda. Am J Primatol 68:675–691PubMedGoogle Scholar
  124. Rothman JM, Plumptre AJ, Dierenfeld ES, Pell AN (2007) Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats. J Trop Ecol 23:673–682Google Scholar
  125. Santacruz A, Collado MC, Garcia-Valdes L, Segura MT, Martin-Lagos JA, Anjos T, Marti-Romero M, Lopez RM, Florido J, Campoy C, Sanz Y (2010) Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 104:83–92PubMedGoogle Scholar
  126. Schoeninger MJ, Iwaniec UT, Glander K (1997) Stable isotope ratios indicate diet and habitat use in New World monkeys. Am J Phys Anthropol 103:69–83PubMedGoogle Scholar
  127. Sekirov I, Russel SI, Antunes CM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904PubMedGoogle Scholar
  128. Serio-Silva JC, Hernandez-Salazar LT, Rico-Gray V (1999) Nutritional composition of the diet of Alouatta palliata mexicana females in different reproductive states. Zoo Biol 18:507–513Google Scholar
  129. Servin AL (2004) Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28:405–440PubMedGoogle Scholar
  130. Sherry DS, Ellison PT (2007) Potential applications of urinary c-peptide of insulin for comparative energetics research. Am J Phys Anthropol 133:771–778PubMedGoogle Scholar
  131. Spor A, Koren O, Ley RE (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev 9:279–290Google Scholar
  132. Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. Cambridge University, New YorkGoogle Scholar
  133. Stoner KE, Gonzalez Di Pierro A (2006) Intestinal parasitic infections in Alouatta pigra in tropical rainforest in Lacandona, Chiapas, Mexico: implications for behavioral ecology and conservation. In: Estrada AE, Garber PA, Pavelka MS, Luecke L (eds) New perspectives in the study of Mesoamerican primates. Springer, New YorkGoogle Scholar
  134. Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299:1259–1260PubMedCentralPubMedGoogle Scholar
  135. Strier KB (1992) Atelinae adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88:515–524PubMedGoogle Scholar
  136. Stuart CS, Duncan SH, Cave DR (2004) Oxalobacter formigenes and its role in oxalate metabolism in the human gut. FEMS Microbiol Lett 230:1–7Google Scholar
  137. Sudo N (2006) Stress and gut microbiota: does postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response? Int Cong Ser 1287:350–354Google Scholar
  138. Suzuki K, Harasawa R, Yoshitake Y, Mitsuoka T (1983) Effect of crowding and heat stress on intestinal flora, body weight gain, and feed efficiency of growing rats and chicks. Nippon Juigaku Zasshi 45:331–338PubMedGoogle Scholar
  139. Szekely BA, Singh J, Marsh TL, Hagedorn C, Werre SR, Kaur T (2010) Fecal bacterial diversity of human-habituated wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale Mountains National Park, western Tanzania. Am J Primatol 72:566–574PubMedGoogle Scholar
  140. Talham GL, Jiang HQ, Bos NA, Cebra JJ (1999) Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun 67:1992–2000PubMedCentralPubMedGoogle Scholar
  141. Thompson ME, Knott CD (2008) Urinary c-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. Horm Behav 53:526–535Google Scholar
  142. Thompson ME, Muller MN, Wrangham RW, Lwanga JS, Potts KB (2008) Urinary c-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav 55:299–305Google Scholar
  143. Trejo-Macias G, Estrada AE, Mosqueda Cabrera MA (2007) Survey of helminth parasites in populations of Alouatta palliata mexicana and A. pigra in continuous and in fragmented habitat in Southern Mexico. Int J Primatol 28:931–945Google Scholar
  144. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031PubMedGoogle Scholar
  145. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon HA (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1:6ra14. doi:  10.1126/scitranslmed.3000322.
  146. Uenishi G, Fujita S, Ohashi G, Kato A, Yamauchi S, Matsuzawa T, Ushida K (2007) Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity. Am J Primatol 69:367–376PubMedGoogle Scholar
  147. Vitazkova SK, Wade SE (2007) Effects of ecology on the gastrointestinal parasites of Alouatta pigra. Int J Primatol 28:1327–1343Google Scholar
  148. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105–108PubMedCentralPubMedGoogle Scholar
  149. Xu B, Xu W, Yang F, Li J, Yang Y, Tang X, Mu Y, Zhou J, Huang Z (2013) Metagenomic analysis of the pygmy loris fecal microbiome reveals unique functional capacity related to metabolism of aromatic compounds. PLoS One 8:e56565PubMedCentralPubMedGoogle Scholar
  150. Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239Google Scholar
  151. Yeoman CJ, Chia N, Yildirim S, Berg Miller ME, Kent A, Stumpf RM, Leigh SR, Nelson KE, White BA, Wilson BA (2011) Towards an evolutionary model of animal-associated microbiomes. Entropy 13:570–594Google Scholar
  152. Yildirim S, Yeoman CJ, Sipos M, Torralba M, Wilson BA, Goldberg TL, Stumpf RM, Leigh SR, White BA, Nelson KE (2010) Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS One 5:e13963PubMedCentralPubMedGoogle Scholar
  153. Zoetendal EG, Akkermans ADL, Akkermans-va Vliet WM, de Visser JAGM, De Vos WM (2001) The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis 13:129–134Google Scholar
  154. Zunino GE, Kowalewski MM, Oklander LI, Gonzalez V (2007) Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in Northern Argentina. Am J Primatol 69:966–975PubMedGoogle Scholar

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Program in Ecology, Evolution, and Conservation BiologyUniversity of Illinois at Urbana-ChampaignChampaignUSA
  2. 2.Department of AnthropologyUniversity of Colorado BoulderBoulderUSA
  3. 3.Department of AnthropologyUniversity of Illinois at Urbana-ChampaignChampaignUSA
  4. 4.Instituto de Ecologia, A.C.XalapaMexico

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