Recent empirical research, mostly done on humans, recognizes that individuals" physiological state affects levels of cooperation. An individual"s internal state may affect the payoffs of behavioural alternatives, which in turn could influence the decision to either cooperate or to defect. However, little is known about the physiology underlying condition dependent cooperation. Here, we demonstrate that shifts in cortisol levels affect levels of cooperation in wild cleaner wrasse Labroides dimidiatus. These cleaners cooperate by removing ectoparasites from visiting "client" reef fishes but prefer to eat client mucus, which constitutes cheating. We exogenously administrated one of three different compounds to adults: a) cortisol, b) glucocorticoid receptor antagonist mifepristone RU486 or c) sham (saline); and observed their cleaning behaviour during the following 45 min. The effects of cortisol match an earlier observational study that first described the existence of "cheating" cleaners: such cleaners provide small clients with more tactile stimulation with their pectoral and pelvic fins, a behaviour that attracts larger clients that are then bitten to obtain mucus. Blocking glucocorticoid receptors led to more tactile stimulation to large clients. As energy demands and associated cortisol concentration level shifts affect cleaner wrasse behavioural patterns, cortisol potentially offers a general mechanism for condition dependent cooperation in vertebrates.
Cooperative interactions offer the inherent possibility of cheating by each of the interacting partners. A key challenge to behavioural observers is to recognize these conflicts, and find means to measure reliably cheating in natural interactions. Cleanerfish Labroides dimidiatus cheat by taking scales and mucus from their fish clients and such dishonest cleaning has been previously recognized in the form of whole‐body jolts by clients in response to cleaner mouth contact. In this study, we test whether jolts may be a general client response to cheating by cleaners. We experimentally varied the ectoparasite loads of yellowtail damselfish (Microspathodon chrysurus), a common client of the cleaning goby Elacantinus evelynae, and compared the rates of jolts on parasitized and deparasitized clients. As predicted if jolts represent cleaner cheating, deparasitized clients jolted more often than parasitized clients, and overall jolt rates increased over time as client parasite load was presumably reduced by cleaning activity. Yellowtail damselfish in the wild jolted significantly less frequently than those in captivity, which is consistent with a loss of ectoparasites during capture. Our results suggest that jolts by clients of cleaning gobies are not related to the removal of ectoparasites. Client jolts may therefore be a generally accurate measure of cheating by cleanerfish.
In the cleanerfish-client mutualism involving the Indo-Pacific cleaner wrasse Labroides dimidiatus and its reef fish clients, mechanisms such as 'tactile stimulation', partner switching and punishment are used by clients to control cheating by cleaners. We sought to establish whether these behaviours are general features of cleaning mutualisms by examining their presence in interactions between Caribbean cleaning gobies (Elacatinus spp.) and their clients. The cleaning goby-client mutualism bears several similarities to the cleaner wrasse system: clients visit cleaners frequently to have their ectoparasites removed while cleaners depend heavily on these visits for food, and cheating by cleaning gobies is also prevalent. However, our data revealed striking differences between the two cleanerfish systems: clients did not seem to attempt to control cheating by cleaning gobies and cleaning gobies did not perform tactile stimulation on their clients. We suggest three hypotheses that might explain these major differences between both systems, based on differences in mutual dependence between cleaners and clients or cognitive ability of cleaners, differences in costs of being cheated and differences in foraging preferences by cleaners. Interactions between L. dimidiatus and its clients should probably not be seen as the 'standard' marine fish cleaning mutualism.
Social stressors typically elicit two distinct behavioural responses in vertebrates: an active response (i.e., “fight or flight”) or behavioural inhibition (i.e., freezing). Here, we report an interesting exception to this dichotomy in a Caribbean cleaner fish, which interacts with a wide variety of reef fish clients, including predatory species. Cleaning gobies appraise predatory clients as potential threat and become stressed in their presence, as evidenced by their higher cortisol levels when exposed to predatory rather than to non-predatory clients. Nevertheless, cleaning gobies neither flee nor freeze in response to dangerous clients but instead approach predators faster (both in captivity and in the wild), and interact longer with these clients than with non-predatory clients (in the wild). We hypothesise that cleaners interrupt the potentially harmful physiological consequences elicited by predatory clients by becoming increasingly proactive and by reducing the time elapsed between client approach and the start of the interaction process. The activation of a stress response may therefore also be responsible for the longer cleaning service provided by these cleaners to predatory clients in the wild. Future experimental studies may reveal similar patterns in other social vertebrate species when, for instance, individuals approach an opponent for reconciliation after a conflict.
If cooperation often involves investment, then what specific conditions prevent selection from acting on cheaters that do not invest? The mutualism between the Indo‐Pacific cleaner wrasse Labroides dimidiatus and its reef fish clients has been a model system to study conflicts of interest and their resolution. These cleaners prefer client mucus over ectoparasites – that is, they prefer to cheat – but punishment and partner switching by clients enforce cooperative behaviour by cleaners. By contrast, clients of Caribbean cleaning gobies (Elacatinus spp.) do not to use punishment or partner switching. Here, we test the hypothesis that the behavioural differences between these two cleaner fish systems are caused by differences in cleaner foraging preferences. In foraging choice experiments, we offered broadstripe cleaning gobies Elacatinus prochilos client‐derived parasitic isopods, client mucus and a control food item. The cleaning gobies significantly preferred ectoparasites over mucus or the control item, which contrasts with cleaner wrasses. We propose that the low level of cleaner–client conflict arising from cleaning goby foraging preferences explains the observed lack of strategic partner control behaviour in the clients of cleaning gobies.
Herbivory is one of the most important biological processes influencing coral reefs. In the highly diverse Indo-Pacific reef fish communities, different herbivores can have strikingly different functions. We investigated the extent of functional diversity among herbivorous parrotfish of the more species-depauperate Caribbean Sea. We carried out observations of seven species of parrotfish (Scarus taeniopterus, Sc. vetula, Sc. iserti, Sparisoma viride, Sp. aurofrenatum, Sp. rubripinne and Sp. chrysopterum) on four Barbadian coral reefs to collect information on foraging techniques, rates, and targets, and found marked interspecific variation. Species of the genus Scarus had higher foraging rates than those of the genus Sparisoma. Different species took varying amounts of live coral, turf algae and macroalgae. A functional categorization based first on foraging technique (contact or no contact with the substratum) and secondarily on the more conventional criterion of foraging target (macroalgae, turf algae and live coral) allowed us to classify Sc. taeniopterus and Sc. iserti as 'scrapers', Sp. aurofrenatum, Sp. rubripinne and Sp. chrysopterum as 'grazers', Sp. viride as a 'bioeroder' and Sc. vetula as a 'bioeroder/scraper'. This functional group affiliation, together with species-specific foraging rates, allows us to predict the role of Caribbean parrotfish on major coral reef processes and their impact on coral reef benthic communities.
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