Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation

Microbial symbionts are nowadays considered of pivotal importance for animal life. Among the many processes where microorganisms are involved, an emerging research avenue focuses on their major role in driving the evolution of chemical communication in their hosts. Volatiles of bacterial origin may underlie chemical communication and the transfer of social information through signals, as well as inadvertent social information. We reviewed the role of microorganisms in animal communication between conspecifics, and, because the microbiome may cause beneficial as well as deleterious effects on their animal hosts, we also reviewed its role in determining the outcome of the interactions with parasites and predators. Finally, we paid special attention to the hypothetical role of predation and parasitism in driving the evolution of the animal microbiome. We highlighted the novelty of the theoretical framework derived from considering the microbiota of animals in scenarios of communication, parasitism, and predation. We aimed to encourage research in these areas, suggesting key predictions that need to be tested to better understand what is one of the main roles of bacteria in animal biology.

The hidden effect of inadvertent social information use on fluctuating predator–prey dynamics

Understanding biotic interactions and abiotic forces that govern population regulation is crucial for predicting stability from both theoretical and applied perspectives. In recent years, social information has been proposed to profoundly affect the dynamics of populations and facilitate the coexistence of interacting species. However, we have limited knowledge about how social information use influences cyclic and non-cyclic fluctuations of populations and if any population-level effects can be expected in species where individuals do not form social groups. In this study, I built individual-based models in a factorial design to investigate how predator avoidance behaviour and associated inadvertent social information (ISI) use alters the predictions of classical predator–prey population models in non-grouping (e.g., randomly moving) animals. Simulation results showed that ISI use in prey stabilized population dynamics by disrupting high-amplitude cyclic fluctuations in both predator and prey populations. Moreover, it also decreased the strength of the negative feedback of second-order dependence between predator and prey. I propose that if social cues are commonly used sources of information in animals regardless of the level of social organization, then similar social information-mediated effects on trophic interactions and population dynamics may be prevalent in natural communities.

Exploring the costs and benefits of social information use: an appraisal of current experimental evidence

Research on social learning has focused traditionally on whether animals possess the cognitive ability to learn novel motor patterns from tutors. More recently, social learning has included the use of others as sources of inadvertent social information. This type of social learning seems more taxonomically widespread and its use can more readily be approached as an economic decision. Social sampling information, however, can be tricky to use and calls for a more lucid appraisal of its costs. In this four-part review, we address these costs. Firstly, we address the possibility that only a fraction of group members are actually providing social information at any one time. Secondly, we review experimental research which shows that animals are circumspect about social information use. Thirdly, we consider the cases where social information can lead to incorrect decisions and finally, we review studies investigating the effect of social information quality. We address the possibility that using social information or not is not a binary decision and present results of a study showing that nutmeg mannikins combine both sources of information, a condition that can lead to the establishment of informational cascades. We discuss the importance of empirically investigating the economics of social information use.

Conspecifics as informers and competitors: an experimental study in foraging bumble-bees

Conspecifics are usually considered competitors negatively affecting food intake rates. However, their presence can also inform about resource quality by providing inadvertent social information. Few studies have investigated whether foragers perceive conspecifics as informers or competitors. Here, we experimentally tested whether variation in the density of demonstrators (‘none’, ‘low’ and ‘high’), whose location indicated flower profitability, affected decision-making of bumble-bees Bombus terrestris . Bumble-bees foraged on either ‘simple’ (two colours) or ‘complex’ (four colours) artificial floral communities. We found that conspecifics at low density may be used as sources of information in first flower choices, whereas they appeared as competitors over the whole foraging sequence. Low conspecific densities improved foragers' first-visit success rate in the simple environment, and decreased time to first landing, especially in the complex environment. High conspecific densities did not affect these behavioural parameters, but reduced flower constancy in both floral communities, which may alter the efficiency of pollinating visits. These results suggest that the balance of the costs and benefits of conspecific presence varies with foraging experience, floral community and density. Spatio-temporal scales could thus be an important determinant of social information use. This behavioural flexibility should allow bumble-bees to better exploit their environment.

Do female frogs exploit inadvertent social information to locate breeding aggregations?

The advertisement calls of male anurans (frogs and toads) are loud and conspicuous signals, and the sound generated by breeding aggregations of males propagates over long distances. As a by-product of communication within an aggregation, the sounds of a frog chorus constitute a form of inadvertent social information that provides potential long-distance cues about the location and timing of breeding. We investigated whether female American toads ( Bufo americanus Holbrook, 1836) and Cope’s gray treefrogs ( Hyla chrysoscelis Cope, 1880) use the sounds of a chorus to locate breeding aggregations in the absence of other sensory cues. Females of both species approached speakers broadcasting recordings of a chorus made from distances of 0, 20, and 40 m, but not from distances of 80 and 160 m. Female toads also exhibited phonotaxis to a completely artificial chorus sound, but female gray treefrogs did not. We found little evidence to suggest that female American toads and Cope’s gray treefrogs differed substantially in their responses to natural chorus sounds despite potential differences in the predictability and duration of breeding seasons in these two species. Our results suggest that the inadvertent social information of a chorus could be used over short distances to locate breeding aggregations.