Mutualistic interactions involve 2 species beneficially cooperating, but it is not clear how these interactions are maintained. In many mutualisms, one species interacts with multiple species, and since partners differ in terms of the commodities they trade, partner identity will directly influence the decisions and behaviors of interacting individuals. Here, we investigated the consequences of within and between-species diversity on a model cleaner–client interaction in a natural environment, by quantifying the behavior of both partners. We found that the predominant Caribbean cleaner fish, the sharknose goby ( Elacatinus evelynae ), shows personality variation as we documented repeatable individual differences in activity, boldness, and exploratory behaviors. Personality variation was associated with cleaner–client interactions: cleaner boldness and activity were significantly related to posing by clients and cleaning, respectively. Cleaner personality variation was also associated with the functional identity (sociality, mobility, body size, and trophic level) of clients posing and being cleaned. We thus demonstrate that partner identity can have consequences on mutualistic outcomes which will contribute to the context-dependency and highly heterogeneous patterns we observe at a population level. We also suggest that within- and between-species differences have consequences on partner choice, a feature that has been previously thought to be absent from these cleaner–client interactions.
Cleaning interactions, which involve a cleaner removing ectoparasites and other material from the body of a heterospecific (client), are iconic symbiotic interactions observed on coral reefs worldwide. These small cleaners play a disproportionately large role in the structuring and function of coral reefs, influencing species interaction networks, client health and biodiversity. Cleaning patterns, however, are likely to be context-dependent and highly heterogeneous, and although we have some understanding about their spatial variation, longer-term temporal changes in cleaning interactions have remained understudied. Given that coral reefs are globally threatened and are currently experiencing large shifts in their biodiversity, it is vital that we determine which clients are consistently most important for maintaining cleaning. Using a long-term, 8-yr data set (2010-17) on the cleaning behaviour of the predominant Caribbean cleaner, the sharknose goby (Elacatinus evelynae), we investigated whether cleaner fish from the same reef show consistent patterns in their interactions with client species over time. Here we conclusively show that cleaning behaviour is highly plastic, as no single species or family was cleaned consistently more than others, in terms of cleaning frequency and duration, across all years. Only 40% of the species were cleaned more than others, and we also observed ca. one-third of species experience inconsistent cleaning patterns across years. Our study thus quantifies how dynamic cleaner-client relationships are on the same reef across years and highlights the importance of long-term data.
Through the removal of parasites, dead skin and mucus from the bodies of visiting reef fish (clients), cleaner fish have a significant ecosystem function in the ecology of coral reefs. Cleaners gain nutrition from these interactions and through offering a 'service' are afforded protection from predators. Given these benefits, it is unclear why more fish do not engage in cleaning, and why part-time cleaning strategies exist. On coral reefs, dedicated species clean throughout their life, whereas some species are facultative, employing opportunistic and/or temporary cleaning strategies. Here, we investigate the cleaning behaviour of a facultative species to assess the relative importance of this interaction to the cleaner. Using a combination of focal and event sampling from a coral reef in Tobago, we show that cleaning is not an essential food source for facultative juvenile blue-headed wrasse (Thalassoma bifasciatum), as cleaning rate was unrelated to their foraging rate on the substrate. These wrasse displayed two cleaning strategies: stationary versus wandering cleaning, with cleaning frequency being highest for stationary cleaners. A specific cleaning location facilitated increased cleaning frequency, and wrasse cleaning rate decreased as cleaner or client abundance increased. We also compared juvenile blue-headed wrasse cleaning behaviour to a resident dedicated cleaner, the sharknose goby (Elacatinus evelynae), and showed that, in comparison, juvenile wrasse clean a narrower client range, predominately cleaning three species of gregarious free-ranging surgeonfish (Acanthurus spp.). The wrasse, however, frequently approached these clients without cleaning, which suggests that their selective cleaning strategy may be driven by the acquisition of a particular parasitic food source. Juvenile blue-headed wrasse are generalist foragers, and may thus be limited in their cleaning behaviour by their nutritional requirements, the availability of a suitable cleaning site, and fish density, which ultimately means that they do not adopt more dedicated cleaning roles within the reef community.
Mutualisms are driven by partners deciding to interact with one another to gain specific services or rewards. As predicted by biological market theory, partners should be selected based on the likelihood, quality, reward level, and or services each partner can offer. Third-party species that are not directly involved in the interaction, however, may indirectly affect the occurrence and or quality of the services provided, thereby affecting which partners are selected or avoided. We investigated how different clients of the sharknose goby (Elacatinus evelynae) cleaner fish were distributed across cleaning stations, and asked what characteristics, relating to biological market theory, affected this distribution. Through quantifying the visitation and cleaning patterns of client fish that can choose which cleaning station(s) to visit, we found that the relative species richness of visiting clients at stations was negatively associated with the presence of disruptive territorial damselfish at the station. Our study highlights, therefore, the need to consider the indirect effects of third-party species and their interactions (e.g., agonistic interactions) when attempting to understand mutualistic interactions between species. Moreover, we highlight how cooperative interactions may be indirectly governed by external partners.
The dynamics and prevalence of mutualistic interactions, which are responsible for the maintenance and structuring of all ecological communities, are vulnerable to changes in abiotic and biotic environmental conditions. Mutualistic outcomes can quickly shift from cooperation to conflict, but it unclear how resilient and stable mutualistic outcomes are to more variable conditions. Tidally controlled coral atoll lagoons that experience extreme diurnal environmental shifts thus provide a model from which to test plasticity in mutualistic behavior of dedicated (formerly obligate) cleaner fish, which acquire all their food resources through client interactions. Here, we investigated cleaning patterns of a model cleaner fish species, the bluestreak wrasse (Labroides dimidiatus), in an isolated tidal lagoon on the Great Barrier Reef. Under tidally restricted conditions, uniquely both adults and juveniles were part‐time facultative cleaners, pecking on Isopora palifera coral. The mutualism was not completely abandoned, with adults also wandering across the reef in search of clients, rather than waiting at fixed site cleaning stations, a behavior not yet observed at any other reef. Contrary to well‐established patterns for this cleaner, juveniles appeared to exploit the system, by biting (“cheating”) their clients more frequently than adults. We show for the first time, that within this variable tidal environment, where mutualistic cleaning might not represent a stable food source, the prevalence and dynamics of this mutualism may be breaking down (through increased cheating and partial abandonment). Environmental variability could thus reduce the pervasiveness of mutualisms within our ecosystems, ultimately reducing the stability of the system.
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