Sex and grooming as exchange commodities in female bonobos’ daily biological market

The Biological Market Theory (BMT) posits that cooperation between non-human animals can be seen as a mutually beneficial exchange of commodities similarly to what observed in human economic markets. Positive social interactions are commodities in non-human animals, and mutual exchanges fulfilling the criteria of the BMT have been shown in several species. However, the study of biological markets suffers from methodological limitations that are mainly linked to the difficulty of clearly identifying the currencies and their exchanges in the short-term. Here, we test whether bonobo females are more attractive during their maximum swelling phase, whether they exchange grooming and Genito-Genital Rubbing (GGR) on a daily level of analysis, and whether these daily exchanges fulfil the BMT criteria. Females engaged more in GGR when their sexual swelling was in the maximum phase. Moreover, they exchanged grooming and sex according to the daily “market fluctuations” associated with swelling status. Females in the minimum phase (low-value) increased their probability to engage in GGR with females in the maximum phase (high-value) by grooming them preferentially. In line with the supply/demand law, the female grooming strategy varied depending on the daily number of swollen females present: the higher the number of swollen females, the lower the individual grooming preference. As a whole, our study confirms BMT as a valid model to explain daily commodity exchanges as a function of the temporary value of traders, and underlines the importance of a day-by-day approach to unveil the presence of a biological market when the value of traders frequently changes.

Beneficial interactions in communities: mutualism and facilitation

The consequences of beneficial interactions for the diversity and functioning of communities remain poorly understood, but this is changing. This chapter examines how mutualism may evolve in the face of cheating, using the concept of biological markets where members of each species exchange resources and services, with associated costs and benefits. Understanding the evolution and maintenance of positive interactions in communities requires that we consider the broader web of interactions and abiotic conditions in which mutualisms are embedded—their context dependency. Ant-plant mutualisms, plant-Rhizobium mutualisms, and plant-mycorrhizal fungi mutualisms are discussed as examples of shifting costs and benefits based on context dependency. Recent advances at incorporating positive interactions into community theory allow species to have both positive and negative effects on each other’s population growth rate. For example, the presence of a neighboring plant may enhance survival in a harsh environment, but may reduce plant growth due to competition for resources.

The dynamics of grooming interactions: maintenance of partner choice and the consequences of demographic variation for female mandrills

A large body of evidence suggests that female Old World monkeys maintain selective long-term grooming interactions with fitness benefits. The last two decades have produced evidence that the regulation of social interactions among primates can be, in part, explained by the Biological Markets theory, with grooming behaviour as the focus of these studies. Grooming facilitates bonding between individuals, constituting an essential part of the regulation of social relationships among female cercopithecids. In contrast to the well-studied baboons (Papio spp), knowledge about the nature of grooming interactions and their regulation is generally lacking for the large, terrestrial species of mandrills (Mandrillus sphinx). We used a combination of social network analysis tools and well-established methods for assessing partner diversity and reciprocity to characterise grooming networks, partner choice and patterns of trade (be groomed, give grooming) among females in a captive group of mandrills, both within and across two separate observation periods. Our results suggest that, even though the relatively stable conditions of captivity allowed the studied females to maintain selective grooming interactions across time, small scale demographic changes affected the grooming dynamics of the group in accordance with the expectations of the Biological Markets theory. In particular, the maturation and consequent integration of a high ranking female into the group’s grooming network from one period to the next resulted in a more pronounced effect of rank on the regulation of grooming interactions. In addition, the influence of the maturation of a dependent infant on the grooming interactions of his mother were evident between periods. Our results also demonstrate that grooming networks are dynamic and that high ranking individuals are not necessarily the most central in grooming networks. Finally, we discuss the potential of social network analysis to identify cases of social exclusion and its consequences for captive management.

Experimental evidence for delayed contingent cooperation among wild dwarf mongooses

Many animals participate in biological markets, with strong evidence existing for immediate cooperative trades. In particular, grooming is often exchanged for itself or other commodities, such as coalitionary support or access to food and mates. More contentious is the possibility that nonhuman animals can rely on memories of recent events, providing contingent cooperation even when there is a temporal delay between two cooperative acts. Here we provide experimental evidence of delayed cross-commodity grooming exchange in wild dwarf mongooses (Helogale parvula). First, we use natural observations and social-network analyses to demonstrate a positive link between grooming and sentinel behavior (acting as a raised guard). Group members who contributed more to sentinel behavior received more grooming and had a better social-network position. We then used a field-based playback experiment to test a causal link between contributions to sentinel behavior and grooming received later in the day. During 3-h trial sessions, the perceived sentinel contributions of a focal individual were either up-regulated (playback of its surveillance calls, which are given naturally during sentinel bouts) or unmanipulated (playback of its foraging close calls as a control). On returning to the sleeping refuge at the end of the day, focal individuals received more grooming following surveillance-call playback than control-call playback and more grooming than a matched individual whose sentinel contributions were not up-regulated. We believe our study therefore provides experimental evidence of delayed contingent cooperation in a wild nonprimate species.

Biological markets in cooperative breeders: quantifying outside options

A major aim in evolutionary biology is to understand altruistic help and reproductive partitioning in cooperative societies, where subordinate helpers forego reproduction to rear dominant breeders' offspring. Traditional models of cooperation in these societies typically make a key assumption: that the only alternative to staying and helping is solitary breeding, an often unfeasible task. Using large-scale field experiments on paper wasps ( Polistes dominula ), we show that individuals have high-quality alternative nesting options available that offer fitness payoffs just as high as their actual chosen options, far exceeding payoffs from solitary breeding. Furthermore, joiners could not easily be replaced if they were removed experimentally, suggesting that it may be costly for dominants to reject them. Our results have implications for expected payoff distributions for cooperating individuals, and suggest that biological market theory, which incorporates partner choice and competition for partners, is necessary to understand helping behaviour in societies like that of P. dominula . Traditional models are likely to overestimate the incentive to stay and help, and therefore the amount of help provided, and may underestimate the size of reproductive concession required to retain subordinates. These findings are relevant for a wide range of cooperative breeders where there is dispersal between social groups.

Attractiveness biases are the tip of the iceberg in biological markets

Physical attractiveness affects how one gets treated, but it is just a single component of one's overall “market value.” One's treatment depends on other markers of market value, including social status, competence, warmth, and any other cues of one's ability or willingness to confer benefits on partners. To completely understand biased treatment, we must also incorporate these other factors.

Grooming interchange for resource tolerance: biological markets principles within a group of free-ranging rhesus macaques

In group-living animals, allogrooming is a common, heterogeneously distributed affiliative behaviour. Among non-human primates, Barrett et al. (1999) predicted ways in which Biological Markets principles interact with competitive regimes to influence grooming reciprocity and interchange. Most tests of these predictions, done at a group level, have produced inconsistent results. Here we take a novel approach by testing these predictions across individuals within a group. This is based on the premise that in groups facing moderate-to-high within-group-competition, individuals vary in their abilities to access resources based on their competitive abilities, causing them to pursue different grooming exchange strategies. We examine evidence for grooming reciprocity and interchange for tolerance at drinking sources among adult females within a group of rhesus macaques (Macaca mulatta) on Cayo Santiago. We test the above premise by assessing hierarchical steepness, and the relationship between individuals’ David’s scores (DS) and access to drinking sources. Finally, we examine the relationship of DS with grooming reciprocity and interchange to see whether they are consistent with the operation of market forces among individuals. Social network comparisons revealed that giving grooming was strongly predicted by both receiving drinking tolerance (interchange) and receiving grooming (reciprocity), despite strong associations with proximity and maternal kinship. The group showed a moderately steep hierarchy, and negative correlations between individuals’ David’s scores and difficulties in accessing drinking stations. Finally, we found partial support for a market-based explanation. Individuals with relatively low David’s scores were more likely to interchange grooming with drinking tolerance. However, grooming reciprocity wasn’t greater among individuals with higher David’s scores. Our findings suggest that multiple explanatory frameworks — reciprocity, market-based interchange, and/or proximity-mediated interchange/social bond investment — may all shape rhesus grooming exchange patterns. Future directions include examining evidence for additional forms of grooming interchange, and the influence of between-group-competition and stress-indicators on grooming reciprocity.