Client Fish Research Articles

Generalized rule application in bluestreak cleaner wrasse (Labroides dimidiatus): using predator species as social tools to reduce punishment.

Generalized rule application promotes flexible behavior by allowing individuals to adjust quickly to environmental changes through generalization of previous learning. Here, we show that bluestreak 'cleaner' wrasse (Labroides dimidiatus) uses generalized rule application in their use of predators as social tools against punishing reef fish clients. Punishment occurs as cleaners do not only remove ectoparasites from clients, but prefer to feed on client mucus (constituting cheating). We tested for generalized rule application in a series of experiments, starting by training cleaners to approach one of two fish models in order to evade punishment (by chasing) from a 'cheated' client model. Cleaners learned this task only if the safe haven was a predator model. During consecutive exposure to pairs of novel species, including exotic models, cleaners demonstrated generalization of the 'predators-are-safe-havens' rule by rapidly satisfying learning criteria. However, cleaners were not able to generalize to a 'one-of-two-stimuli-presents-a-safe-haven' rule, as they failed to solve the task when confronted with either two harmless fish models or two predator models. Our results emphasize the importance of ecologically relevant experiments to uncover complex cognitive processes in non-human animals, like generalized rule learning in the context of social tool use in a fish.

Dopamine disruption increases negotiation for cooperative interactions in a fish.

Humans and other animals use previous experiences to make behavioural decisions, balancing the probabilities of receiving rewards or punishments with alternative actions. The dopaminergic system plays a key role in this assessment: for instance, a decrease in dopamine transmission, which is signalled by the failure of an expected reward, may elicit a distinct behavioural response. Here, we tested the effect of exogenously administered dopaminergic compounds on a cooperative vertebrate’s decision-making process, in a natural setting. We show, in the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus, that blocking dopamine receptors in the wild induces cleaners to initiate more interactions with and to provide greater amounts of physical contact to their client fish partners. This costly form of tactile stimulation using their fins is typically used to prolong interactions and to reconcile with clients after cheating. Interestingly, client jolt rate, a correlate of cheating by cleaners, remained unaffected. Thus, in low effective dopaminergic transmission conditions cleaners may renegotiate the occurrence and duration of the interaction with a costly offer. Our results provide first evidence for a prominent role of the dopaminergic system in decision-making in the context of cooperation in fish.

Cleaning behaviour of the cichlid Mesonauta festivus in the Pantanal wetlands: evidence of a potential freshwater cleaning station

Cleaning interactions are known among several groups of fishes, with a higher number of records for marine fish species. These temporary associations occur between one species that acts as the cleaner and the other species as the client. The interaction usually takes place within the boundaries defined by the cleaner. This site, known as the cleaning station, allows the client fish to strike a typical pose allowing the cleaner to approach, such as wide-open fins and inclined, motionless body. Few studies have reported on the cleaning behaviour of freshwater fish species, and none has reported on behaviour that could be interpreted as establishing a cleaning station. Herein we present a new record of the cleaning interaction in the Neotropics, between the cichlid Mesonauta festivus as the cleaner and three species of anostomid (Leporinus macrocephalus, Leporinus friderici and Schizodon borellii) as clients on Pantanal wetlands, as well as the establishment of a defined cleaning station.

Nitrogen transfer in a Caribbean mutualistic network

Coral reef symbioses are well-established models for studying multi-level networks of species interactions that provide nutritional benefits to partners. While the contributions of endosymbionts to cnidarian hosts have been extensively documented, relatively little is known about how exosymbionts contribute to nutrient cycling in coral reef cnidarians. We investigated exosymbiotic sources of ammonia and their contributions to physiological processes in Caribbean corkscrew sea anemones Bartholomea annulata. In laboratory experiments, anemones absorbed ammonia from seawater, which significantly enhanced the mitotic index of their endosymbiotic microalgae Symbiodinium, while anemone shrimp presence alone had no effect. Anemone shrimps excreted ammonia at much slower rates than anemones were able to absorb it, indicating that shrimp alone were not able to meet host nitrogen demand. Client fishes excreted ammonia ~10× more rapidly than did associated shrimps. On Caribbean coral reefs, anemone shrimps attract diverse client fishes through their parasite-cleaning behavior; these fishes excrete substantial ammonia near anemones while being cleaned. Exosymbiotic anemone shrimps thus may provide nutritional benefits to host anemones and microalgae indirectly, through their attraction of nitrogen-excreting fishes. This multi-level mutualistic network facilitates tight nutrient cycling among diverse species belonging to several phyla on coral reefs. While we assessed the rates and benefits of nutrient transfer under laboratory conditions, further research is needed to quantify the contributions of ammonia and other nutrients from client fishes through cleaner shrimps to host sea anemones in the field.

Fish mucus versus parasitic gnathiid isopods as sources of energy and sunscreens for a cleaner fish

The cleaning behaviour of the bluestreak cleaner wrasse Labroides dimidiatus is extensively used as a model system for understanding cooperation. It feeds mainly on blood-sucking gnathiid isopods and also on the epidermal mucus of client fish; the nutritional quality of these foods, however, is unknown. The epidermal mucus of reef fish contains ultraviolet (UV)-absorbing compounds (mycosporine-like amino acids, MAAs), which are only obtained via the diet; nevertheless, while La. dimidiatus has high amounts of MAAs in its mucus, their source is unknown. Therefore, the energetic value (calories and protein estimated using carbon and nitrogen) and MAA level in gnathiids and mucus from several clients [parrotfishes, wrasses (Labridae), and a snapper (Lutjanidae)] were determined. The energetic value of mucus and gnathiids varied among fishes. Overall, carbon, nitrogen, calories, and protein per dry weight were higher in the mucus of most client species compared to gnathiids. Thus, depending on the client species, mucus may be energetically more advantageous for cleaner wrasse to feed on than gnathiids. UV absorbance, a confirmed proxy for MAA levels, indicated high MAA levels in mucus, whereas gnathiids had no detectable MAAs. This suggests that La. dimidiatus obtain MAAs from mucus but not from gnathiids. Hence, in addition to energy, the mucus of some clients also provides La. dimidiatus with the added bonus of UV-absorbing compounds. This may explain why cleaner fish prefer to feed on mucus over gnathiid isopods. The likely costs and benefits to clients of the removal of UV protecting mucus and parasitic gnathiids, respectively, and the variation in benefits gained by cleaner fish from feeding on these foods may explain some variation in cooperation levels in cleaning interactions.

The welfare of ornamental fish in the home aquarium

The welfare of ornamental fish kept in aquariums or ponds has historically been taken for granted by fish keepers, the ornamental fish industry and animal welfare organisations. This is attributed to the low cost of many ornamental fish, lack of reliable information about their health care, or a perceived lack of veterinarians with skills in aquatic animal health. Moreover, it is not uncommon for our veterinary colleagues to refer potential fish clients to fish stores or pet stores, as had been done in the past with less commonly seen species like birds and ‘pocket pets’. Slowly, veterinary surgeons and veterinary organisations are increasingly becoming involved in aquatic veterinary medicine to help improve the welfare of pet fish. This article presents the current status of ornamental fish welfare, the issues and their causes, and provides further sources of information.

Forebrain neuropeptide regulation of pair association and behavior in cooperating cleaner fish

Animals establish privileged relationships with specific partners, which are treated differently from other conspecifics, and contribute to behavioral variation. However, there is limited information on the underlying physiological mechanisms involved in the establishment of these privileged ties and their relationship to individual cooperation levels. The Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus often forages in mixed-sex pairs when cleaning fish clients. Intra-couple conflicts often arise during a joint client inspection, which may alter the overall quality of cleaning service provided. Here we tested two hypotheses: a) whether intra-pair association (i.e. association index), measured with joint interspecific cleaning and intraspecific behavior, is correlated with neuroendocrine mechanisms involving forebrain neuropeptides arginine vasotocin (AVT) and isotocin (IT) and b) whether these neuropeptide level shifts relate to an individual's interspecific service quality. We found that partner support (number of cleaning interactions and tactile stimulation) received by male cleaners increased with association index. When cleaners inspected clients alone, cleaners' cheating decreased with association index for females but not males. AVT levels did not differ according to sex or association level. Forebrain IT levels increased with association index for males, whereas no relationship was found for females. Finally, cleaner cheating varied between sex and forebrain IT levels. Findings indicate that variation in pairs' relationships influences male and female cleaner fish differently and contributes to the variation of brain neuropeptide levels, which is linked to distinct cooperative outcomes.

Pairs of cleaner fish prolong interaction duration with client reef fish by increasing service quality

Few biological examples of cooperation seem to precisely fit the assumptions of an iterated prisoner’s dilemma. In an attempt to increase biological validity, one model altered the assumption that cooperating is an all-or-nothing decision to a situation where benefits are a function of interaction duration, which in turn is a function of the levels of cooperation. A potential application involves pairs of cleaner fish coinspecting a client fish. In this mutualism, clients visit cleaners to have ectoparasites removed but a conflict of interest exists, as cleaners prefer to eat client mucus, which constitutes cheating. As large clients often flee in response to a cleaner cheating, pair inspections lead to a dilemma: the cheater obtains the benefit while both cleaners share the cost of the client leaving. The model predicts that pairs of cleaners behave more cooperatively toward reef fish clients than when inspecting alone, to entice clients to profit from the increased parasite removal rate and keep interaction duration almost constant. Here, we present field experiments that first replicate results that pairs behave indeed more cooperatively than when inspecting alone and second show that levels of cooperation quantitatively predict the duration of cleaning interactions. We also found that several additional variables may affect the duration of cleaning interactions, such as a client’s willingness to interact with a cleaner, identity of interaction terminator, and the presence of bystanders. In conclusion, introducing benefits as a function of interaction duration into the prisoner’s dilemma framework provides a biologically relevant framework to study cooperation.

Variation in Cleaner Wrasse Cooperation and Cognition: Influence of the Developmental Environment?

AbstractDeviations from model‐based predictions of strategies leading to stable cooperation between unrelated individuals have raised considerable debate in regards to decision‐making processes in humans. Here, we present data on cleaner wrasse (Labroides dimidiatus) that emphasize the importance of generalizing this discussion to other species, with the aim to develop a coherent theoretical framework. Cleaners eat ectoparasites and mucus off client fishes and vary their service quality based on a clients’ strategic behaviour. Hitherto, cognitive tasks designed to replicate such behaviour have revealed a strong link between cooperative behaviour and game theoretic predictions. However, we show that individuals from a specific location within our study site repeatedly failed to conform to the published evidence. We started exploring potential functional and mechanistic causes for this unexpected result, focusing on client composition, cleaner standard personality measures and ontogeny. We found that failing individuals lived in a socially simple environment. Decision rules of these cleaners ignored existing information in their environment (‘bounded rationality’), in contrast to cleaners living in a socially complex area. With respect to potential mechanisms, we found no correlations between differences in performance and differences in aggressiveness or boldness, in contrast to results on other cooperative species. Furthermore, juveniles from the two habitat types performed similarly, and better than the adults from the socially simple environment. We propose that variation in the costs and benefits of knowledge may affect a cleaners’ information acquisition and storage, which may explain our observed variation in cooperation and cognition.

Cleaning up the biogeography of Labroides dimidiatus using phylogenetics and morphometrics

Cleaner fishes are some of the most conspicuous organisms on coral reefs due to their behaviour and prominent body pattern, consisting of a lateral stripe and blue/yellow colouration. All obligate cleaner fishes share this body stripe pattern, which is an important signal for attracting client fishes. However, variability in the cleaning signal of the cleaner fish Labroides dimidiatus has been documented across its range. Here, we investigate the geographic distribution of cleaner signal polymorphisms in L. dimidiatus and contrast this to phylogeographic variation in mitochondrial (mt) DNA. We used samples from 12 sites for genetic analyses, encompassing much of L. dimidiatus’ range from the Red Sea to Fiji. We obtained morphometric measures of the cleaner signal body stripe width from individuals among six of the sites and qualitatively grouped tail stripe shape. mtDNA control region sequences were used for phylogenetic and population genetic analyses. We found that body stripe width was significantly correlated with tail stripe shape and geographical location, with Indian Ocean populations differing in morphology from western Pacific populations. L. dimidiatus haplotypes formed two reciprocally monophyletic clades, although in contrast to morphology, Japanese cleaner fish fell within the same clade as Indian Ocean cleaner fish and both clade types were sympatric in Papua New Guinea. An additional novel finding of our research was that the inclusion of two closely related cleaner fish species, Labroides pectoralis and Labroides bicolor, in the phylogenetic analysis rendered L. dimidiatus polyphyletic. Overall, the findings suggest the diversity within L. dimidiatus is underestimated.

Power and temptation cause shifts between exploitation and cooperation in a cleaner wrasse mutualism

In many instances of cooperation, only one individual has both the potential and the incentive to 'cheat' and exploit its partner. Under these asymmetric conditions, a simple model predicts that variation in the temptation to cheat and in the potential victim's capacity for partner control leads to shifts between exploitation and cooperation. Here, we show that the threat of early termination of an interaction was sufficient to induce cleaner wrasse Labroides dimidiatus to feed selectively against their preference (which corresponds to cooperatively eating client fish ectoparasites), provided that their preference for alternative food was weak. Under opposite conditions, cleaners fed selectively according to their own preference (which corresponds to cheating by eating client mucus). By contrast, a non-cleaning fish species, Halichoeres melanurus, failed to adjust its foraging behaviour under these same conditions. Thus, cleaners appear to have evolved the power to strategically adjust their levels of cooperation according to the circumstances.

Patterns of resource-use and competition for mutualistic partners between two species of obligate cleaner fish

Cleaner mutualisms on coral reefs, where specialized fish remove parasites from many species of client fishes, have greatly increased our understanding of mutualism, yet we know little about important interspecific interactions between cleaners. Here, we explore the potential for competition between the cleaners Labroides dimidiatus and Labroides bicolor during two distinct life stages. Previous work has demonstrated that in contrast to L. dimidiatus, which establish cleaning stations, adult L. bicolor rove over large areas, searching for clients. We show that site-attached juvenile L. bicolor associate with different microhabitat than juvenile L. dimidiatus and that L. bicolor specialize on a narrower range of species than L. dimidiatus as both juveniles and adults. Further, we present evidence suggesting that differences in resource-use are influenced by competitive interactions between the two species. Finally, we discuss the implications of these results for understanding the ecology and evolution of the mutualism.

Face your fears: cleaning gobies inspect predators despite being stressed by them.

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.

Reef fishes use sea anemones as visual cues for cleaning interactions with shrimp

Marine cleaners benefit diverse fish clients via removal of ectoparasites, yet little is known about how fishes locate small, inconspicuous cleaner shrimps on coral reefs. Pederson shrimp Ancylomenes pedersoni are effective cleaners in the Caribbean Sea, and additionally form obligate associations with corkscrew sea anemones Bartholomea annulata, which also serve as hosts to a variety of other crustacean symbionts. We examined the visual role of B. annulata to reef fishes during cleaning interactions with A. pedersoni by comparing anemone characteristics with fish visitation rates, and by manipulating the visibility of anemones and cleaner shrimp in field experiments using mesh covers. Rates of visitation by fishes to cleaning stations increased primarily with anemone body size and the total number of crustacean symbionts, but did not change consistently in response to covers. Fishes posed for cleaning at stations only where anemones remained visible, regardless of whether shrimp were visible. Shrimp at stations where anemones were covered performed fewer cleaning interactions with fishes, as fishes did not continue to pose when anemones were not visible. We conclude that anemones serve as visual cues to client fishes prior to cleaning by shrimp. These visual cues facilitate fish cleaning interactions with shrimp, and provide a previously unknown symbiotic benefit to cleaner shrimp from association with sea anemones.

Host selection by the cleaner shrimp Ancylomenes pedersoni: Do anemone host species, prior experience or the presence of conspecific shrimp matter?

In the symbiotic association that exists between cleaner shrimp Ancylomenes pedersoni (=Periclimenes pedersoni) and host sea anemones, specificity varies among populations, and shrimp are believed to search among different individual hosts for favourable positions from which to attract client fish. Four laboratory-based experiments were conducted to test host selection of A. pedersoni between the following: i) Bartholomea annulata (corkscrew anemone) and Condylactis gigantea (condy anemone), ii) B. annulata, with or without a conspecific resident, iii) a previously known or unknown B. annulata, and iv) a previously known or unknown C. gigantea. Preference (active selection) was distinguished from mere passive association by comparing shrimp acclimation to anemones offered in choice and no-choice (control) situations. The results were analysed using asymmetrical χ2 contingency tables (in each experiment, n=60) where expected frequencies were obtained with maximum likelihood estimators. Shrimp acclimated more frequently to B. annulata than to C. gigantea, but they acclimated similarly to anemones with or without another resident and to those B. annulata and C. gigantea anemones that were familiar rather than unfamiliar. However, none of the χ2 values were statistically significant (χ2df=1=0.48, 0.19, 0.42, 0.42; overall p>0.45), suggesting that preference may not be responsible for the association between adult A. pedersoni and its host anemones observed in the field. Differences in the frequency of association may be due to factors other than the active decisions made by shrimp when presented with more than one alternative host.

Patterns of cleaning behaviour on coral reef fish by the anemoneshrimpAncylomenes pedersoni

Little is known about the cleaning behaviour of shrimps in comparison to that of cleaner fish, and only recently have cleaner shrimps been shown to remove parasites effectively from coral reef fish. Here we describe patterns of cleaning interactions between Pederson shrimpAncylomenes pedersoniand fish clients in St Thomas, US Virgin Islands. Clients observed here were members of at least 16 fish families, including three previously unreported client families. Most cleans lasted <20 seconds; surgeonfish were cleaned most frequently, but lizardfish and groupers received the longest cleans. The shrimp formed social groups of varying sizes on individuals of the host sea anemoneBartholomea annulata, which served as the centres of their cleaning stations. The number and duration of cleans per station increased with the number of resident shrimp, however most anemones hosted small groups of fewer than four individuals, while larger groups of up to nine individuals were relatively rare. Some client fish chased away other fish and competitively excluded them from anemone stations. We conclude that these shrimp clean a wide diversity of clients, vary their clean duration with fish identity, and clean more when in large groups. In addition, clients in part control these patterns of interaction by interfering with access to these stations by other clients.

Unexpected response of a captive blackeye thicklip, Hemigymnus melapterus (Bloch), from Lizard Island, Australia, exposed to juvenile isopods Gnathia aureamaculosa Ferreira & Smit

Gnathiid isopods (Crustacea: Isopoda: Gnathiidae) have complex, biphasic life cycles demonstrating protelian parasitism; the reproductive adults are freeliving, and the juveniles are haematophagous ectoparasites feeding on either teleost or elasmobranch fish (Raibaut & Trilles 1993; Smit & Davies 2004). Pathological effects resulting from gnathiid blood feeding are reported in aquaria, fish farming and in the wild (Marino, Giannetto, Paradiso, Bottari, De Vico & Macri´ 2004; Smit & Davies 2004; Jones & Grutter 2005; Hayes, Smit & Davies 2007). The action of cleaner fish in removing juvenile gnathiids from client fish on coral reefs has been well recognized in recent years, especially on the Great Barrier Reef (GBR), Australia (Grutter 2008; Grutter, Pickering, McCallum & McCormick 2008; Penfold, Grutter, Kuris, McCormick & Jones 2008). However, relatively little is known of the rapid, direct effects of juvenile gnathiids feeding on their hosts in this ecological system. Here, we report briefly on the death and associated histopathology observed when a specimen of captive H. melapterus (Teleostei: Labridae) was experimentally exposed to juveniles of Gnathia aureamaculosa Ferreira & Smit (in Ferreira, Smit, Grutter & Davies 2009) at Lizard Island Research Station, GBR, Australia (14°40′S; 145°28′E), in 2004.

High-quality habitat and facilitation ameliorate competitive effects of prior residents on new settlers

Many species disperse during their lifetime. Two factors that can affect the performance of individuals following dispersal are the presence of conspecifics and intrinsic habitat quality at the settlement site. Detecting the influence of these factors can be difficult for at least two reasons: (1) the outcomes of interactions with conspecifics are often variable including both competition and facilitation, and (2) selection of high quality habitats often leads to positive covariance between habitat quality and density. In this study, I investigate positive and negative effects of resident blue streak cleaner wrasse (Labroides dimidiatus) on the growth and survival of recently settled conspecifics while accounting for habitat quality. Juvenile L. dimidiatus settle near adult conspecifics, but likely have to compete with resident adults for access to food. However, field experiments indicate that settlers have access to more resources at occupied sites, and as a result, grow faster despite evidence for competition with residents. This result is a direct consequence of two factors: (1) resident conspecifics facilitate settlers by attracting client fish, and (2) resident conspecifics are strongly associated with high quality habitat. These results highlight the need to simultaneously consider habitat quality and competitive and facilitative interactions between conspecifics when making inferences about ecological processes from spatial patterns of individual performance.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-010-1826-7) contains supplementary material, which is available to authorized users.

Caribbean Cleaning Gobies Prefer Client Ectoparasites Over Mucus

AbstractIf 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.

Crime and punishment in a roaming cleanerfish

Cheating is common in cooperative interactions, but its occurrence can be controlled by various means ranging from rewarding cooperators to active punishment of cheaters. Punishment occurs in the mutualism involving the cleanerfish Labroides dimidiatus and its reef fish clients. When L. dimidiatus cheats, by taking scales and mucus rather than ectoparasites, wronged clients either chase or withhold further visits to the dishonest cleaner, which leads to more cooperative future interactions. Punishment of cheating L. dimidiatus may be effective largely because these cleaners are strictly site-attached, increasing the potential for repeated interactions between individual cleaners and clients. Here, we contrast the patterns of cheating and punishment in L. dimidiatus with its close relative, the less site-attached Labroides bicolor. Overall, L. bicolor had larger home ranges, cheated more often and, contrary to our prediction, were punished by cheated clients as frequently as, and not less often than, L. dimidiatus. However, adult L. bicolor, which had the largest home ranges, did not cheat more than younger conspecifics, suggesting that roaming, and hence the frequency of repeated interactions, has little influence on cheating and retaliation in cleaner-client relationships. We suggest that roaming cleaners offer the only option available to many site-attached reef fish seeking a cleaning service. This asymmetry in scope for partner choice encourages dishonesty by the partner with more options (i.e. L. bicolor), but to be cleaned by a cleaner that sometimes cheats may be a better option than not to be cleaned at all.