Avoidance of biological contaminants through sight, smell and touch in chimpanzees

Royal Society Open Science

Volumn 4, Issue 11, 2017, Pages

  Sarabian, Cecile ^a   Ngoubangoye, Barthelemy ^b   Macintosh, Andrewj J ^a  

^a KYOTO UNIVERSITY   (Japan)

^b CENTRE INTERNATIONAL DE RECHERCHES MÉDICALES DE FRANCEVILLE   (Gabon)

Author keywords

Bodily products; Disgust; Pan troglodytes; Parasite avoidance; Sensory modalities

Indexed keywords

EID: 85033551821     PISSN: None     EISSN: 20545703     Source Type: Journal    
DOI: 10.1098/rsos.170968     Document Type: Article

References (40)

1. Curtis V, Biran A. 2001 Dirt, disgust, and disease: is hygiene in our genes? Perspect. Biol. Med. 44, 17–31. (doi:10.1353/pbm.2001.0001)
2. Rivas FV, Chervonsky AV, Medzhitov R. 2014 ART and immunology. Trends Immunol. 35, 451. (doi:10.1016/j.it.2014.09.002)
3. Schaller M. 2006 Parasites, behavioral defenses, and the social psychological mechanisms through which cultures are evoked. Psychol. Inquiry 17, 96–137. (doi:10.1207/s15327965pli1702_2)
4. Curtis V, de Barra M, Aunger R. 2011 Disgust as an adaptive system for disease avoidance behaviour. Phil. Trans. R. Soc. B 366, 389–401. (doi:10.1098/rstb.2010.0117)
5. Curtis V, Aunger R, Rabie T. 2004 Evidence that disgust evolved to protect from risk of disease. Proc. R. Soc. Lond. B 271(Suppl. 4), S131–S133. (doi:10.1098/rsbl.2003.0144)
6. Darwin C. 1872 The expression of the emotions in man and animals, 3rd edn. NewYork, NY: Oxford University Press.
7. Curtis VA. 2014 Infection-avoidance behaviour in humans and other animals. Trends Immunol. 35, 457–464. (doi:10.1016/j.it.2014.08.006)
8. Oaten M, Stevenson RJ, Case TI. 2009 Disgust as a disease-avoidance mechanism. Psychol. Bull. 135, 303–321. (doi:10.1037/a0014823)
9. Behringer DC, Butler MJ, Shields JD. 2006 Ecology: avoidance of disease by social lobsters. Nature 441, 421. (doi:10.1038/441421a)
10. Poirotte C, Massol F, Herbert A, Willaume E, Bomo PM, Kappeler PM, Charpentier JE. 2017 Mandrills use olfaction to socially avoid parasitized conspecifics. Sci. Adv. 3, e1601721. (doi:10.1126/sciadv.1601721)
11. Meisel JD, Kim DH. 2014 Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans. Trends Immunol. 35, 465–470. (doi:10.1016/j.it.2014.08.008)
12. Sarabian C, MacIntosh AJ. 2015 Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biol. Lett. 11, 20150757. (doi:10.1098/rsbl.2015.0757)
13. Clayton DH, Koop JAH, Harbison CW, Moyer BR, Bush SE. 2010 How birds combat ectoparasites. Open Ornithol. J. 3, 41–71. (doi:10.2174/1874453201003010041)
14. Ezenwa V. 2004 Selective defecation and selective foraging: antiparasite behavior in wild ungulates? Ethology 110, 851–862. (doi:10.1111/j.1439-0310.2004.01013.x)
15. Cooper J, Gordon IJ, Pike AW. 2000 Strategies for the avoidance of faeces by grazing sheep. Appl. Anim. Behav. Sci. 69, 15–33. (doi:10.1016/S0168-1591(00)00116-7)
16. van derWal R, Irvine J, Stien A, Shepherd N. 2000 Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer. Oecologia 124, 19–25. (doi:10.1007/s004420050020)
17. Meisel JD, Panda O, Mahanti P, Schroeder FC, Kim DH. 2014 Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C. elegans. Cell 159, 267–280. (doi:10.1016/j.cell.2014.09.011)
18. Mansourian S, Corcoran J, Enjin A, Lofstedt C, Dacke M, Stensmyr MC. 2016 Fecal-derived phenol induces egg-laying aversion in Drosophila. Curr. Biol. 26, 2762–2769. (doi:10.1016/j.cub.2016.07.065)
19. Yanagawa A, Guigue AM, Marion-Poll F. 2014 Hygienic grooming is induced by contact chemicals in Drosophila melanogaster. Front. Behav. Neurosci. 8, 254. (doi:10.3389/fnbeh.2014.00254)
20. Soldano A et al. 2016 Gustatory-mediated avoidance of bacterial lipopolysaccharides via TRPA1 activation in Drosophila. eLife 5, e13133. (doi:10.7554/eLife.13133)
21. Boillat M, Challet L, Rossier D, Kan C, Carleton A, Rodriguez I. 2015 The vomeronasal system mediates sick conspecific avoidance. Curr. Biol. 25, 251–255. (doi:10.1016/j.cub.2014.11.061)
22. Ehman KD, Scott ME. 2002 Female mice mate preferentially with non-parasitized males. Parasitology 125, 461–466. (doi:10.1017/S003118200200224X)
23. Kavaliers M, Choleris E, Agmo A, Pfaff DW. 2004 Olfactory-mediated parasite recognition and avoidance: linking genes to behavior. Horm. Behav. 46, 272–283. (doi:10.1016/j.yhbeh.2004.03.005)
24. Dohi H, Yamada A, Entsu S. 1991 Cattle feeding deterrents emitted from cattle feces. J. Chem. Ecol. 17, 1197–1203. (doi:10.1007/BF01402943)
25. Aoyama M, Dohi H, Shioya S, Takeuchi Y, Mori Y, Okubo T. 1994 Feeding-deterrent substance in cattle feces: its effects on ingestive behavior in goats. Appl. Anim. Behav. Sci. 40, 253–262. (doi:10.1016/0168-1591(94)90066-3)
26. Goodall J. 1986 Social rejection, exclusion, and shunning among the Gombe chimpanzees. Ethol. Sociobiol. 7, 227–236. (doi:10.1016/0162-3095(86)90050-6)
27. O’Hara SJ, Lee PC. 2006 High frequency of postcoital penis cleaning in Budongo chimpanzees. Folia Primatol. 77, 353–358. (doi:10.1159/000093700)
28. Kawai M. 1965 Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima islet. Primates 6, 1–30. (doi:10.1007/BF01794457)
29. Nakamichi M, Kojima E, Itoigawa N. 1998 Carrying and washing of grass roots by free-ranging Japanese macaques at Katsuyama. Folia Primatol. 69, 35–40. (doi:10.1159/000021561)
30. Allritz M, Tennie C, Call J. 2013 Food washing and placer mining in captive great apes. Primates 54, 361–370. (doi:10.1007/s10329-013-0355-5)
31. Rozin P, Millman L, Nemeroff C. 1986 Operation of the laws of sympathetic magic in disgust and other domains. J. Pers. Soc. Psychol. 50, 703–712. (doi:10.1037/0022-3514.50.4.703)
32. Hoefling A, Likowski KU, Deutsch R, Hafner M, Seibt B, Muhlberger A, Weyers P, Strack F. 2009When hunger finds no fault with moldy corn: food deprivation reduces food-related disgust. Emotion 9, 50–58. (doi:10.1037/a0014449)
33. Go Y, Niimura Y. 2008 Similar numbers but different repertoires of olfactory receptor genes in humans and chimpanzees. Mol. Biol. Evol. 25, 1897–1907. (doi:10.1093/molbev/msn135)
34. Nevo O, Heymann EW. 2015 Led by the nose: olfaction in primate feeding ecology. Evol. Anthropol. 24, 137–148. (doi:10.1002/evan.21458)
35. Hornbuckle PA, Beall T. 1974 Escape reactions to the blood of selected mammals by rats. Behav. Biol. 12, 573–576. (doi:10.1016/S0091-6773(74)92531-0)
36. Jones RB, Black AJ. 1979 Behavioral responses of the domestic chick to blood. Behav. Neural Biol. 27, 319–329. (doi:10.1016/S0163-1047(79)92384-7)
37. Oum RE, Lieberman D, Aylward A. 2011 A feel for disgust: tactile cues to pathogen presence. Cogn. Emot. 25, 717–725. (doi:10.1080/02699931.2010.496997)
38. Winfield AJ, Richards ME. 2003 Pharmaceutical practice. London, UK: Churchill Livingstone.
39. Bertolani P, Pruetz JD. 2011 Seed reingestion in savannah chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. Int. J. Primatol. 32, 1123–1132. (doi:10.1007/s10764-011-9528-5)
40. Krief S, Jamart A, Hladik CM. 2004 On the possible adaptive value of coprophagy in free-ranging chimpanzees. Primates 45, 141–145. (doi:10.1007/s10329-003-0074-4)