Biological Market examples:

Grooming in primates

vervet monkeys in the Loskop Dam Nature Reserve, South-Africa

photo: Ronald Noë

Primates trade grooming against other services, such as access to infants, tolerance at food sources and support in conflicts

Grooming is one of the few, if not the only, naturally occurring altruistic behaviour in primates that can easily be quantified. Louise Barrett and Peter Henzi were the first to systematically look at grooming from a biological market point of view. They realised that grooming can be traded, both for itself as well as for other commodities, such as tolerance near resources, access to young infants, support in conflicts and compliance during mating. Grooming thus has something in common with a currency that can be used to pay for different goods and services. The possibility of quantifying grooming opens the way to testing whether shifts in supply and demand lead to shifts in exchange rates of different commodities. The fact that grooming can be used to compensate for unbalanced trade in several other goods and services lends it a currency-like character.

More recently, important contributions have been published by Stefano Kaburu and Nick Newton-Fisher. They analysed the grooming patterns among adult male chimpanzees in two different communities and over different periods in great detail. I list a number of their papers below. One I can recommend in particular is Newton-Fisher (2017) in Animal Behaviour.

(see for 'A common fallacy: reciprocity and time frames' the Biological Markets main page)

Some general discussions of primate grooming markets

  • Balasubramaniam, K. N., Berman, C. M., Ogawa, H. & Li, J. 2011. Using biological markets principles to examine patterns of grooming exchange in Macaca thibetana. American Journal of Primatology, 73, 1269-1279.
  • Barrett, L. & Henzi, S. P. 2001. The utility of grooming in baboon troops. In: In: Noë, R.; van Hooff, J.A.R.A.M. & Hammerstein, P. (eds.) Economics in Nature. Social Dilemmas, Mate Choice and Biological Markets. Cambridge Univ. Press. pp. 119-145.
  • Barrett, L. & Henzi, S. P. 2001. Grooming and family life. Exchanging services among female monkeys. In: In: Macdonald, D. (ed.) The New Encyclopedia of Mammals. Oxford Univ. Press, Oxford, pp. 306-307.
  • Barrett, L. & Henzi, S. P. 2006. Monkeys, markets and minds: biological markets and primate sociality. In: Cooperation in Primates and Humans (Ed. by Kappeler, P. M. & van Schaik, C. P.), pp. 209-232. Berlin: Springer.
  • Gilby, I. C. 2012. Cooperation among non-kin: Reciprocity, markets, and mutualism. In: The Evolution of Primate Societies (Ed. by J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit & J. B. Silk), pp. 514-530. (This is a general review of cooperation among unrelated primates)
  • Gomes, C. and C. Boesch 2011. "Reciprocity and trades in wild West African chimpanzees." Behavioral Ecology and Sociobiology 65(11): 2183-2196.
  • Henzi, S. P. & Barrett, L. 2007. Coexistence in Female-Bonded Primate Groups. Advances in the Study of Behavior, 37, 43-81.
  • Kaburu, S. S. K. & Newton-Fisher, N. E. (2013). Social instability raises the stakes during social grooming among wild male chimpanzees. Animal Behaviour. (This paper reports a test of the 'raise-the-stakes' (RTS) model by looking at grooming among chimpanzees after relationships have been 'reset' (RTS predicts how relationships start from scratch), but concludes that the data are best understood in the context of a grooming market).
  • Kaburu, S. S. K., & Newton-Fisher, N. E. (2015). Egalitarian despots: hierarchy steepness, reciprocity and the grooming-trade model in wild chimpanzees, Pan troglodytes. Animal Behaviour, 99(0), 61-71 (An excellent analysis of grooming patterns in male chimps, contrasting BMT with Seyfarth's 1977 model. For a more extensive comment see my ScoopIt! page.)
  • Kaburu, S. S. K., & Newton-Fisher, N. E. (2015). Trading or coercion? Variation in male mating strategies between two communities of East African chimpanzees. Behavioral Ecology and Sociobiology, 69(6), 1039-1052 (Great paper that shows that markets (in this case exchanges of grooming for sex) don't work in a community with a steep male hierarchy, but do explain grooming patterns in a community with a shallow hierarchy. See my comment on the ScoopIt! page too.)
  • Kaburu, S. S. K., & Newton-Fisher, N. E. (2016). Bystanders, parcelling, and an absence of trust in the grooming interactions of wild male chimpanzees. Scientific Reports, 6, 20634 (Another great paper of this rather productive duo, this time they pay attention to Connor's parcelling strategy. Watch also what they have to say about 'bonds' and relationships based on trust.For a more extensive comment see my ScoopIt! page)
  • Newton-Fisher, N. E. 2014. Roving females and patient males: a new perspective on the mating strategies of chimpanzees. Biological Reviews 89(2), 356-374.
  • Newton-Fisher, N. E., & Kaburu, S. S. K. (2017). Grooming decisions under structural despotism: the impact of social rank and bystanders among wild male chimpanzees. Animal Behaviour, 128, 153-164
  • Russell, Y. I. & Phelps, S. 2013. How do you measure pleasure? A discussion about intrinsic costs and benefits in primate allogrooming. Biology & Philosophy 28(6), 1005-1020
  • Sánchez-Amaro, A., & Amici, F. (2015). Are primates out of the market? Animal Behaviour, 110, 51-60 (this is a paper with some good points, but also several errors and some dubious claims. For a more extensive comment, see my Biological Markets-page on ScoopIt! (entry of 25 October 2015). A rebuttal to this paper has been written by Stefano Kaburu & Nick Newton-Fisher Kaburu, S. S. K., & Newton-Fisher, N. E. (2016). Markets misinterpreted? A comment on Sánchez-Amaro, A. and Amici, F. (2015). Animal Behaviour 119, e1-e5; the answer to that: Sánchez-Amaro, A., & Amici, F. (2016). Markets carefully interpreted: a reply to Kaburu and Newton-Fisher (2016). Animal Behaviour, 119, e7-e13 and then a second rebuttal, this time published as a stand-alone paper: Dunayer, E. S., & Berman, C. M. (2016). Biological markets: theory, interpretation, and proximate perspectives. A response to Sánchez-Amaro and Amici (2015). Animal Behaviour, 121, 131-136). The whole discussion is quite interesting and worth reading; notably the paper by Dunayer and Berman shoudl not be missed!

See also Dario Maestripieri's book 'Games primates play' (2012) Chpt 8 'Shopping for partners in the biological market'. This chapter gives an easy to read account of the BM paradigm with examples from primates as well as non-primates, several of which you'll find elsewhere on this site too. Oddly missing, however, is an acknowledgement of the role play by Louise Barrett and Peter Henzi in developing market ideas in primatology.

Baby markets

A striking example is the so-called 'baby market': the fewer infants in a group the higher the price that has to be paid in the form of grooming to gain the mother's permission to inspect and handle it. This was first described for chacma baboons, but similar results have been found in other primate species, such as sooty mangabeys and vervet monkeys (Fruteau et al. 2011), longtailed macaques (Gumert 2007), spider monkeys (Schaffner & Aureli 2005; Slater et al. 2007) and golden-snub nosed monkeys (Wei et al 2013). The latter is a highly interesting example of baby markets in a harem-species.

  • Fruteau, C., van de Waal, E., van Damme, E. & Noë, R. 2011. Infant access and handling in sooty mangabeys and vervet monkeys. Animal Behaviour, 81, 153-161
  • Henzi, S. P. & Barrett, L. 2002. Infants as a commodity in a baboon market. Animal Behaviour, 63, 915-921.
  • Schaffner, C. & Aureli, F. 2005. Embraces and grooming in captive spider monkeys. International Journal of Primatology, 26, 1093-1106.
  • Slater, K. Y., Schaffner, C. M. & Aureli, F. 2007. Embraces for infant handling in spider monkeys: evidence for a biological market? Animal Behaviour, 74, 455-461.
  • Gumert, M. 2007. Grooming and infant handling interchange in Macaca fascicularis : the relationship between infant supply and grooming payment. International Journal of Primatology, 28, 1059-1074
  • Tiddi, B., F. Aureli, et al. (2010). "Grooming for infant handling in tufted capuchin monkeys: a reappraisal of the primate infant market." Animal Behaviour 79: 1115-1123
  • Wei, W., Qi, X., Garber, P. A., Guo, S., Zhang, P. & Li, B. 2013. Supply and demand determine the market value of access to infants in the Golden Snub-Nosed monkey (Rhinopithecus roxellana). PLoS ONE, 8, e65962.

Trading tolerance for grooming

Peter Henzi and Louise Barrett also pointed out that 'tolerance' is another important commodity that can be traded. This explains why the asymmetry in grooming between a dominant and a subordinate is strongest when resources are scarce and can be monopolized by a single animal. Rebecca Chancellor and Lynne Isbell (2008) point out that market effects also influence grooming patterns under scramble competition. Markus Port and colleagues (2009) show how important tolerance is for our understanding of grooming in primates. Their analysis reveals the effect of market forces in grooming patterns that superficially seem to adhere to the reciprocal altruism model. Barbara Tiddi and colleagues (2011) provide an important contribution to the discussion by testing the relative predictive power of dyadic reciprocity driven exchanges (as predicted by the reciprocal altruism paradigm) against partner choice driven exchanges (as predicted by the biological markets paradigm) in capuchins foraging on baited platforms. Their results confirm a number of  convictions I have had for years: partner choice is much more important than partner control; tolerance is an important commodity traded on monkey markets and primate cooperation among unrelated individuals is driven by "attitudinal partner choice" (Fruteau et al 2009; the partner choice based form of de Waal's (2000) "attitudinal reciprocity"). Sick and colleagues (2014) found that grooming for tolerance in chacma baboons occurs mainly in the morning and ebbs off later in the day when bellies fill up.

  • Barrett, L., Henzi, S. P., Weingrill, T. & Hill, R. A. 1999. Market forces predict grooming reciprocity in female baboons. Proceedings of the Royal Society B-Biological Sciences, 266, 665-670.
  • Barrett, L., Gaynor, D. & Henzi, S. P. 2002. A dynamic interaction between aggression and grooming reciprocity among female chacma baboons. Animal Behaviour, 63, 1047-1053.
  • Chancellor, R. L. & Isbell, L. A. 2009. Female grooming markets in a population of gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology, 20, 79-86.
  • Fruteau, C., Voelkl, B., van Damme, E. & Noë, R. 2009. Supply and demand determine the market value of food providers in wild vervet monkeys. Proceedings of the National Academy of Sciences, 106, 12007-12012.
  • Henzi, S. P. & Barrett, L. 1999. The value of grooming to female primates. Primates, 40, 47-59.
  • Leinfelder, I., de Vries, H., Deleu, R. & Nelissen, M. 2001. Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons. American Journal of Primatology, 55, 25-42.
  • Newton-Fisher, N. E. & Lee, P. C. 2011. Grooming reciprocity in wild male chimpanzees. Animal Behaviour 81, 439-446.
  • Payne, H. F. P., Lawes, M. J. & Henzi , S. P. 2003. Competition and the exchange of grooming among female samango monkeys (Cercopithecus mitis erythrarchus). Behaviour, 140, 453-471.
  • Port, M., Clough, D. & Kappeler, P. M. (2009). Market effects offset the reciprocation of grooming in free-ranging redfronted lemurs, Eulemur fulvus rufus. Animal Behaviour 77, 29-36.
  • Sick, C., Carter, A. J., Marshall, H. H., Knapp, L. A., Dabelsteen, T., & Cowlishaw, G. (2014). Evidence for varying social strategies across the day in chacma baboons. Biology Letters, 10(7)
  • Tiddi, B., Aureli, F., Polizzi di Sorrentino, E., Janson, C. H. & Schino, G. 2011. Grooming for tolerance? Two mechanisms of exchange in wild tufted capuchin monkeys. Behavioral Ecology, 22, 663-669.
  • de Waal, F. B. M. 2000. Attitudinal reciprocity in food sharing among brown capuchin monkeys. Animal Behaviour, 60, 253-261.
  • Wei, W., Qi, X.-G., Guo, S.-T., Zhao, D.-P., Zhang, P., Huang, K. & Li, B.-G. 2012. Market powers predict reciprocal grooming in golden snub-nosed monkeys (Rhinopithecus roxellana). PLoS ONE, 7, e36802.
  • Xia, D., Li, J., Garber, P. A., Sun, L., Zhu, Y. & Sun, B. 2012. Grooming reciprocity in female Tibetan macaques Macaca thibetana. American Journal of Primatology, 74, 569-579
  • Xia, D.-P., Li, J.-H., Garber, P. A., Matheson, M. D., Sun, B.-H. & Zhu, Y. 2013. Grooming reciprocity in male Tibetan macaques. American Journal of Primatology.

Trading  grooming for sex

The idea that sex can be traded for other commodities is much older than the biological market paradigm (see also 'Mating markets'). The idea that reproduction takes place in the context of a mating market also exists at least since Darwin set the theory of sexual selection in motion. We seem nevertheless to have inspired a few people to take a closer look at exchange rates between grooming and access to sexual partners
  • Barelli, C., Reichard, U. H. & Mundry, R. 2011. Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar? Animal Behaviour,82, 801-809
  • Clarke, P. M. R., Halliday, J. E. B., Barrett, L. & Henzi, S. P. 2010. Chacma baboon mating markets: competitor suppression mediates the potential for intersexual exchange. Behavioral Ecology, 21, 1211-1220
  • Gomes, C. & Boesch, C. 2011. Reciprocity and trades in wild West African chimpanzees. Behavioral Ecology and Sociobiology, 65, 2183-2196
  • Gumert, M. D. 2007. Payment for sex in a macaque mating market. Animal Behaviour, 74, 1655-1667
  • Koyama, N. F., Caws, C. & Aureli, F. 2012. Supply and demand predict male grooming of swollen females in captive chimpanzees, Pan troglodytes. Animal Behaviour 84, 1419-1425
  • Lewis, R. J. 2010. Grooming patterns in Verreaux's sifaka. American Journal of Primatology, 72, 254-261
  • Norscia, I., Antonacci, D. & Palagi, E. 2009. Mating first, mating more: biological market fluctuation in a wild prosimian. PLoS ONE, 4, e4679
  • Tiddi, B., F. Aureli, et al. (2011). "Social relationships between adult females and the alpha male in wild tufted capuchin monkeys." American Journal of Primatology 73, 812-820

 Grooming for support in conflicts

The popularity of this idea seems inversely correlated to the quantity of data supporting it, but here are some interesting exceptions:

  • Carne, C., Wiper, S. & Semple, S. 2011. Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi-free-ranging Barbary macaques. American Journal of Primatology, 73, 1127-1133
  • Ventura, R., Majolo, B., Koyama, N. F., Hardie, S. & Schino, G. 2006. Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support. American Journal of Primatology, 68, 1138-1149
  • Watts, D. P. 2000. Grooming between male chimpanzees at Ngogo, Kibale National Park. II. Influence of male rank and possible competition for partners. International Journal of Primatology, 21, 211-238.