Does mutualism provide additional indirect benefits? Behavioral indicators of chemical communication in a temporally dynamic fish-mussel mutualism

Abstract

Mutualistic relationships confer selective advantages to interacting species through enhanced ecological benefits but may be functionally limited to certain life history stages. However, it is not yet known whether one party can indirectly benefit from risky cues released when the other party is threatened. Larval glochidia of the Chinese pond mussel (Anodonta woodiana) attach to fishes including the rosy bitterling (Rhodeus ocellatus) for dispersal, while reproductive-phase bitterling use the gills of adult mussels as spawning substrate, and their larvae remain inside the host mussel shells until they are capable of swimming. Here, we examined heterospecific responses to risky chemical cues by rosy bitterling as an indirect indicator of species affinity consistent with mutualism at different life history stages, to test for age-dependent response patterns indicating temporal patterning of shared predation risk. Bitterling demonstrated equivocal but similar responses to water controls and mussel odor and significant antipredator responses to bitterling chemical alarm cues (CAC) independent of life stage, while only reproductive adult bitterling demonstrated significant antipredator responses to mussel CAC. These findings suggest that the mutualistic affinity to mussels present in reproductive-phase adult rosy bitterling may result in shared predation risk and therefore provide them with additional indirect antipredator benefits. Our results revealed a life history stage-dependent mutualism in this bitterling-mussel system and describe a novel application of predation risk assays for studying temporal patterning in mutualistic relationships.

Significance statement

Interspecific interactions, including mutualisms, are a central component of community composition. Some freshwater fishes, including the rosy bitterling, and mussels share an interesting mutualism where each species provides early life habitat to the other. However, does mutualism provide additional indirect benefits? Here, we used responses to conspecific and Chinese pond mussel chemical cues in different life stages of bitterling to identify the occurrence of mutualistic behaviors. We demonstrated that the putative occurrence of mutualistic behaviors in rosy bitterling is not consistent over time and instead varies predictably with reproductive status of different life history stages. This study provides a novel perspective for a deeper understanding of labile interspecific relationships and provides a theoretical basis for indirectly examining mutualisms through chemical communication-based behavioral assays.