Primates

, Volume 58, Issue 3, pp 449–459

Observations of termitarium geophagy by Rylands’ bald-faced saki monkeys (Pithecia rylandsi) in Madre de Dios, Peru

  • Dara B. Adams
  • Jennifer A. Rehg
  • Mrinalini Watsa
Original Article

Abstract

Geophagy, or soil consumption, has been documented in diverse animal taxa, including many primates. Physiological functions such as mineral supplementation, detoxification of secondary compounds, and antacid properties are possible causes for this behavior. We report on observations of geophagy at arboreal termitaria by free-ranging Pithecia rylandsi at La Estación Biológica Los Amigos (EBLA) in Perú between 2008 and 2015. Characteristics of geophagy events, including saki monkey behavior at the termitaria, were recorded and geochemical analyses were conducted on consumed termitaria, nearby topsoils, and unvisited termitaria. We observed 76 feeding bouts at 26 different termitaria by two groups of P. rylandsi during 1125 observational hours (0.07 bouts/obs. h). Geophagy occurred throughout the year, but rates peaked in January during the rainy season. All age and sex classes visited both active and inactive mounds. Feeding bouts were brief (171 ± SD 154 s), and no differences were observed in time spent feeding at active or inactive termitaria. Analyses showed that consumed soils contained higher concentrations of phosphorous, potassium, calcium, and magnesium than did topsoil. Consumed soils also contained a higher total cation exchange capacity than topsoil. Our analysis of consumed versus control termitaria revealed no differences in their chemical composition. We discuss these results in the context of the two primary hypotheses proposed for geophagy in pitheciins: mineral supplementation and toxin adsorption. Our data are consistent with the interpretation that P. rylandsi consume soils from arboreal termitaria to aid in adsorption of toxins found in immature seeds, which are a year-round component of their diet.

Keywords

Pithecia Geophagy Soil composition Feeding ecology Nutritional supplementation Tannin adsorption 

Supplementary material

Supplementary material 1 (M4 V 17148 kb) Supporting Information: Saki monkeys feeding on an arboreal termitarium

References

  1. Atrium: Biodiversity Information System for the Andes to Amazon Biodiversity Program (2008) Botanical Research Institute of Texas. http://atrium.andesamazon.org/. Accessed 10 Apr 2015
  2. Barnett AA, Boyle SA, Norconk MA, Palminteri S, Santos RR, Veiga LM, Alvim THG, Bowler M, Chism J, Di Fiore A, Fernandez-Duque E, Guimarãres ACP, Harrison- Levine A, Haugaasen T, Lehman S, MacKinnon KC, de Melo FR, Moreira LS, Moura VS, Phillips CR, Pinto LP, Port-Carvalho M, Setz EZF, Shaffer C, da Silva LR, da Silva SSB, Soares RF, Thompson CL, Vieira TM, Vreedzaam A, Walker- Pacheco SE, Spironello WR, MacLarnon A, Ferrari SF (2012) Terrestrial activity in pitheciins (Cacajao, Chiropotes, and Pithecia). Am J Primatol 74:1106–1127CrossRefPubMedGoogle Scholar
  3. Bolton KA, Campbell VM, Burton FD (1998) Chemical analysis of soils of Kowloon (Hong Kong) eaten by hybrid macaques. J Chem Ecol 24:195–205CrossRefGoogle Scholar
  4. Boyle SA, Lourenco WC, da Silva LR, Smith AT (2009) Travel and spatial patterns change when Chiropotes satanas chiropotes inhabit forest fragments. Int J Primatol 30:515–531CrossRefGoogle Scholar
  5. Brightsmith DJ, Muñoz-Najar RA (2004) Avian geophagy and soil characteristics in Southeastern Peru. Biotropica 36:534–543Google Scholar
  6. Brightsmith DJ, Taylor J, Phillips TD (2008) The roles of soil characteristics and toxin adsorption in avian geophagy. Biotropica 40:766–774CrossRefGoogle Scholar
  7. Burger J, Gochfeld M (2003) Parrot behavior at a Rio Manu (Peru) clay lick: temporal patterns, associations, and antipredator responses. Acta Ethol 6:23–34Google Scholar
  8. Costa-Pereira R, Severo-Neto F, Inforzato I, Lap RR, Piza MA (2015) Nutrients drive termite geophagy in Yellow-chevroned parakeets (Brotogeris chiriri). Wilson J Ornithol 127:506–510CrossRefGoogle Scholar
  9. Davies AG, Baillie IC (1988) Soil-eating by red leaf monkeys (Presbytis rubicunda) in Sabah, Northern Borneo. Biotropica 20:252–258CrossRefGoogle Scholar
  10. De Souza LL, Ferrari SF, Da Costa ML, Kern DC (2002) Geophagy as a correlate of folivory in red-handed howler monkeys (Alouatta belzebul) from eastern Brazilian Amazonia. J Chem Ecol 28:1613–1621CrossRefPubMedGoogle Scholar
  11. Ferrari SF, Veiga LM, Urbani B (2008) Geophagy in New World monkeys (Platyrrhini): ecological and geographic patterns. Folia Primatol 79:402–415CrossRefPubMedGoogle Scholar
  12. Gilardi JD, Toft CA (2012) Parrots eat nutritious foods despite toxins. PLoS One 7:e38293CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gilardi JD, Duffey SS, Munn CA, Tell LA (1999) Biochemical functions of geophagy in parrots: detoxification of dietary toxins and cytoprotective effects. J Chem Ecol 25:897–922CrossRefGoogle Scholar
  14. Happel RE (1982) Ecology of Pithecia hirsuta in Peru. J Hum Evol 11:581–590CrossRefGoogle Scholar
  15. Holt AJ, Lepage M (2000) Termites and soil properties. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Springer, The Netherlands, pp 389–407CrossRefGoogle Scholar
  16. Hunter JM, De Kleine R (1984) Geophagy in Central America. Geogr Rev 74:157–169CrossRefPubMedGoogle Scholar
  17. Izawa K (1975) Foods and feeding behavior of monkeys in the Upper Amazon Basin. Primates 16:295–316CrossRefGoogle Scholar
  18. Izawa K (1993) Soil-eating by Alouatta and Ateles. Int J Primatol 14:229–242CrossRefGoogle Scholar
  19. Janzen DH (1974) Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6:69–103CrossRefGoogle Scholar
  20. Janzen DH, Juster HB, Bell EA (1977) Toxicity of secondary compounds to the seed-eating larvae of the bruchid beetle Callosobruchus maculatus. Phytochemistry 16:223–227CrossRefGoogle Scholar
  21. Kinzey W, Norconk MA (1993) Physical and chemical properties of fruits and seeds eaten by Pithecia and Chiropotes in Surinam and Venezuela. Int J Primatol 14:207–227CrossRefGoogle Scholar
  22. Klaus G, Klaus-Hugi C, Schmid B (1998) Geophagy by large mammals at natural licks in the rain forest of the Dzanga National Park, Central African Republic. J Trop Ecol 14:829–839CrossRefGoogle Scholar
  23. Knezevich M (1998) Geophagy as a therapeutic mediator of endoparasitism in a free- ranging group of rhesus macaques (Macaca mulatta). Am J Primatol 44:71–82CrossRefPubMedGoogle Scholar
  24. Krishnamani R, Mahaney WC (2000) Geophagy among primates: adaptive significance and ecological consequences. Anim Behav 59:899–915CrossRefPubMedGoogle Scholar
  25. Marsh L (2014) A taxonomic revision of the saki monkeys, Pithecia Desmarest, 1804. Neotrop Primates 21:1–163CrossRefGoogle Scholar
  26. Müller K, Ahl C, Hartmann G (1997) Geophagy in masked titi monkeys (Callicebus personatus melanochir) in Brazil. Primates 38:69–77CrossRefGoogle Scholar
  27. Noirot C (1970) The nests of termites. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic, New York, pp 73–125Google Scholar
  28. Norconk MA, Conklin-Brittain NL (2004) Variation on frugivory: the diet of Venezuelan white-faced sakis. Int J Primatol 25(1):1–26CrossRefGoogle Scholar
  29. Norconk MA, Grafton BW, Conklin-Brittain NL (1998) Seed dispersal by Neotropical seed predators. Am J Primatol 45:103–126CrossRefPubMedGoogle Scholar
  30. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Issue 939, USDA, Washington DCGoogle Scholar
  31. Palminteri S (2010) Determinants of primate distribution and abundance in south-western Amazonia, with a focus on bald-faced saki monkey (Pithecia irrorata). Ph.D. dissertation. University of East Anglia, UKGoogle Scholar
  32. Palminteri S, Peres CA (2012) Habitat selection and use of space by bald-faced sakis (Pithecia irrorata) in Southwestern Amazonia: lessons from a multiyear, multigroup study. Int J Primatol 33:401–417CrossRefGoogle Scholar
  33. Palminteri S, Powell GV, Peres CA (2012) Advantages of granivory in seasonal environments: feeding ecology of an arboreal seed predator in Amazonian forests. Oikos 121:1896–1904CrossRefGoogle Scholar
  34. Palminteri S, Powell G, Adamek K, Tupayachi R (2013) Competition between pitheciines and large Ara macaws, two specialist seed-eaters. In: Veiga LM, Barnett AA, Ferrari SF, Norconk MA (eds) Evolutionary biology and conservation of titis, sakis and uacaris. Cambridge University Press, Cambridge, pp 114–126CrossRefGoogle Scholar
  35. Peres CA (1993) Notes on the ecology of buffy saki monkeys (Pithecia albicans, Gray 1860): a canopy seed-predator. Am J Primatol 31:129–140CrossRefGoogle Scholar
  36. Pitman NCA (2010) An overview of the Los Amigos watershed, Madre de Dios, southeastern Peru. February 2010 version of an unpublished report available from the author at ncp@duke.eduGoogle Scholar
  37. R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria Google Scholar
  38. Setz EZF, Enzweiler J, Solferini VN, Amêndola MP, Berton RS (1999) Geophagy in the golden-faced saki monkey (Pithecia pithecia chrysocephala) in the Central Amazon. J Zool (London) 247:91–103CrossRefGoogle Scholar
  39. Tan KH (1996) Soil sampling, preparation, and analysis. Marcel Dekker, New YorkGoogle Scholar
  40. Thompson CL (2011) Sex, aggression, and affiliation: the social system of the white-faced saki monkeys (Pithecia pithecia). Ph.D. dissertation. Kent State University, KentGoogle Scholar
  41. Urbani B, Norconk MA, Flaschka MJ (2005) Mineral content of foods eaten by wild Guianan white-faced sakis (Pithecia pithecia) in southeastern Venezuela: A preliminary assessment. Programa y libro de résumenes del II Congreso Mexicano de Primatología, p 50Google Scholar
  42. Veiga LM, Ferarri SF (2007) Geophagy at termitaria by bearded sakis (Chiropotes satanas) in southeastern Brazilian Amazonia. Am J Primatol 69:816–820CrossRefPubMedGoogle Scholar
  43. Vermeer DE, Ferrell RE (1985) Nigerian geophagical clay: a traditional antidiarrheal pharmaceutical. Science 227:634–636CrossRefPubMedGoogle Scholar
  44. Vié JC, Richard-Hansen C, Fournier-Chambrillon C (2001) Abundance, use of space, and activity patterns of white-faced sakis (Pithecia pithecia) in French Guiana. Am J Primatol 55:203–221CrossRefPubMedGoogle Scholar
  45. Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Ann Rev Ecol Evol Syst 17:137–167CrossRefGoogle Scholar
  46. Voight CC, Capps KA, Dechmann DKN, Michener RH, Kinz H (2008) Nutrition or detoxification: why bats visit mineral licks of the Amazonian rainforest. PLoS One 3:e2011CrossRefGoogle Scholar
  47. Voros J, Mahaney WC, Milner MW, Krishnamani R, Aufreiter S, Hancock RGV (2001) Geophagy by the bonnet macaques (Macaca radiata) of Southern India: a preliminary analysis. Primates 42:327–344CrossRefGoogle Scholar
  48. Wakibara JV, Huffman MA, Wink M, Reich S, Aufreiter S, Hancock RGV (2001) The adaptive significance of geophagy for Japanese macaques (Macaca fuscata) at Arashiyama, Japan. Int J Primatol 22:495–520CrossRefGoogle Scholar
  49. Watsa M (2013) Growing up tamarin: morphology, reproduction, and population demography of sympatric free-ranging Saguinus fuscicollis and S. imperator. Ph.D. dissertation. Washington University in St. Louis, St. LouisGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2017

Authors and Affiliations

  1. 1.Department of AnthropologyThe Ohio State UniversityColumbusUSA
  2. 2.Department of AnthropologySouthern Illinois University EdwardsvilleEdwardsvilleUSA
  3. 3.Department of AnthropologyWashington University in St. LouisSt. LouisUSA
  4. 4.Field Projects InternationalSt. LouisUSA

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