Client fish ectoparasite loads and cleaner shrimp Urocaridella sp c hunger levels affect cleaning behaviour

Cleaning is a classic example of mutualism and determining the factors that maintain the balance between the costs and benefits for mutualist partners can assist our understanding of how cleaning relationships are maintained. Optimal foraging theory suggests two factors that might help to maintain the relationship between cleaners and their clients: client ectoparasite load and cleaner hunger levels. The ecological relevance and importance of foraging by cleaner fish in marine systems has been demonstrated repeatedly, yet there is little information available on this behaviour in cleaner shrimp. To determine whether cleaner shrimp base their choice of client fish on food patch quality (i.e. client fish ectoparasite load) we offered the yellow-beaked cleaner shrimp Urocaridella sp. c a choice of parasitized and unparasitized rock cods, Cephalopholis cyanostigma. To determine whether cleaner shrimp hunger levels influence cleaning time, we manipulated hunger levels in Urocaridella sp. c and examined their behaviour towards parasitized client fish. Cleaner shrimp preferred parasitized to unparasitized client fish and food-deprived cleaner shrimp cleaned parasitized rock cods more frequently than satiated cleaner shrimp did. Therefore, variations in client fish ectoparasite load and cleaner shrimp hunger level are two factors that affect the balance in this mutualism. Finally, our results meet some of the assumptions of biological market theory, a framework used to understand cooperative interactions, and thus this framework is suggested for future studies on this cleaning system.

Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish

Cleaning behavior is a popular example of non-kin cooperation. However, quantitative support for this is generally sparse and the alternative, that cleaners are parasitic: has also been proposed. Although the behaviour involves some of the most complex and highly developed interspecific communication signals known, the proximate causal factors for why clients Seek cleaners are controversial. However, this information is essential to understanding the evolution of cleaning. I tested whether clients seek cleaners in response to parasite infection or whether clients seek cleaners for tactile stimulation regardless of parasite load. Parasite loads oil client fish were manipulated and clients exposed to cleaner fish and control fish hehind glass. I found that parasitized client fish spent more time than unparasitized fish next to a cleaner fish. In addition; parasitized clients spent more rime next to cleaners than next to control fish whereas unparasitized fish were not attracted to cleaners. This study shows, I believe for the first time, which is somewhat surprising, that parasite infection alone causes clients to seek cleaning by cleaners and provides insight into how this behaviour evolved.

Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions

Recent studies on cleaning behaviour suggest that there are conflicts between cleaners and their clients over what cleaners eat. The diet of cleaners usually contains ectoparasites and some client tissue. It is unclear, however, whether cleaners prefer client tissue over ectoparasites or whether they include client tissue in their diet only when searching for parasites alone is not profitable. To distinguish between these two hypotheses, we trained cleaner fish Labroides dimidiatus to feed from plates and offered them client mucus from the parrotfish Chlorurus sordidus, parasitic monogenean flat-worms, parasitic gnathiid isopods and boiled flour glue as a control. We found that cleaners ate more mucus and monogeneans than gnathiids, with gnathiids eaten slightly more often than the control substance. Because gnathiids are the most abundant ectoparasites, our results suggest a potential for conflict between cleaners and clients over what the cleaner should eat, and support studies emphasizing the importance of partner control in keeping cleaning interactions mutualistic.

Feeding ecology of the fish ectoparasite Gnathia sp. (Crustacea: Isopoda) from the Great Barrier Reef, and its implications for fish cleaning behaviour

The feeding rate of a parasitic gnathiid isopod on fish was examined. Individual fish, Hemigymnus melapterus, were exposed to gnathiid larvae and sampled after 5, 10, 30, 60, and 240 min. I recorded whether larvae had an engorged gut, an engorged gut containing red material, or had dropped off the fish after having completed engorgement; variation among sampling times and larval stages was analyzed using generalized linear mixed model analyses. The likelihood that larvae had an engorged gut increased with time and varied with larval stage. First stage (1.45 mm) larvae. After 30 min, however, most (>93%) larvae had an engorged gut regardless of their larval stage. The likelihood of red material in the gut of third stage larvae increased over time (46% after 30 min, 70% after 60 min, and 86% after 240 min) while that of first and second stage larvae remained relatively low (

Cleaner shrimp do clean

Apart from cleaner fish, there are many reports on cleaning by shrimps, yet whether shrimps actually 'clean', i.e. eat parasites in the wild, has not been demonstrated. For the first time, we show that, conclusively, cleaner shrimp in the wild do clean. We found crustacean ectoparasites from the Family Gnathiidae and the Class Copepoda in the gut contents of wild cleaner shrimp, Urocaridella sp. and Periclimenes holthuisi. In addition, they ate parasitic monogenean flatworms, Benedenia sp., offered to them in the laboratory. Finally, P. holthuisi, significantly reduced monogenean, Benedenia sp., loads by 74.5% on captive surgeonfish Ctenochaetus striatus within 48 h. Such large reductions in parasite loads are likely to benefit individual fish. These results emphasise the need for more information on the ecological role of cleaner shrimp on coral reefs.

Cleaner shrimp use a to advertise cleaning rocking dance service to clients

Signals transmit information to receivers about sender attributes, increase the fitness of both parties, and are selected for in cooperative interactions between species to reduce conflict [1, 2]. Marine cleaning interactions are known for stereotyped behaviors [3-6] that likely serve as signals. For example, dancing and tactile dancing in cleaner fish may serve to advertise cleaning services to client fish [7] and manipulate client behavior [8], respectively. Cleaner shrimp clean fish [9], yet are cryptic in comparison to cleaner fish. Signals, therefore, are likely essential for cleaner shrimp to attract clients. Here, we show that the yellow-beaked cleaner shrimp [110] Urocaridella sp. c [11] uses a stereotypical side-to-side movement, or rocking dance, while approaching potential client fish in the water column. This dance was followed by a cleaning interaction with the client 100% of the time. Hungry cleaner shrimp, which are more willing to clean than satiated ones [12], spent more time rocking and in closer proximity to clients Cephaiopholis cyanostigma than satiated ones, and when given a choice, clients preferred hungry, rocking shrimp. The rocking dance therefore influenced client behavior and, thus, appears to function as a signal to advertise the presence of cleaner shrimp to potential clients.

Cleaning symbioses from the parasites' perspective

Cleaning behaviour has generally been viewed from the cleaner or client's point of view. Few studies, however, have examined cleaning behaviour from the parasites' perspective, yet they are the equally-important third players in such associations. All three players are likely to have had their evolution affected by the association. As cleaner organisms are important predators of parasites, cleaners are likely to have an important effect on their prey. Little, however, is known of how parasites are affected by cleaning associations and the strategies that parasites use in response to cleaners. I examine here what parasites are involved in cleaning interactions, the effect cleaners have on parasites, the potential counter-adaptations that parasites have evolved against the predatory activities of cleaner organisms, the potential influence of cleaners on the life history traits of parasites, and other factors affected by cleaners. I have found that a wide range of ectoparasites from diverse habitats have been reported to interact with a wide range of cleaner organisms. Some of the life history traits of parasites are consistent with the idea that they are in response to cleaner predation. It is clear, however, that although many cleaning systems exist their ecological role is largely unexplored. This has likely been hindered by our lack of information on the parasites involved in cleaning interactions.

Optimising cleaning behaviour: minimising the costs and maximising ectoparasite removal

Little is known of how client fish minimise the costs of cleaning behaviour while maximising ectoparasite removal by cleaner fish. Previous studies have found that abundance on fish and infestation behaviour of gnathiid isopods, the main parasite eaten by cleaner fish, varies diurnally. We examined whether reduced foraging is a cost of cleaning behaviour in clients and whether the behaviour of the client fish, the thick-lipped wrasse Hemigymnus melapterus, towards the cleaner fish Labroides dimidiatus varied diurnally to maximise ectoparasite removal, possibly in response to the diurnal changes in the abundance and infestation patterns of gnathiids. We found that during the midday and afternoon, client foraging rates were negatively related to the duration and frequency of inspections, suggesting that cleaning may, at some times of the day, be energetically costly to the client in terms of reduced foraging opportunities. Surprisingly, we found that the duration and frequency of inspections of clients by cleaners did not vary among diel time periods. A model of gnathiid dynamics on individual fish is proposed. It shows that the observed diurnal pattern in gnathiid abundance on fish can be generated with the constant duration and frequency of inspections that was observed in this study. Thus clients would not have more gnathiids removed by modifying their cleaning behaviour.

9-28 d of exposure to elevated pCO2 reduces avoidance of predator odour but had no effect on behavioural lateralization or swimming activity in a temperate wrasse(Ctenolabrus rupestris)

Most studies on the impact of near-future levels of carbon dioxide on fish behaviour report behavioural alterations, wherefore abnormal behaviour has been suggested to be a potential consequence of future ocean acidification and therefore a threat to ocean ecosystems. However, an increasing number of studies show tolerance of fish to increased levels of carbon dioxide. This variation among studies in susceptibility highlights the importance of continued investigation of the possible effects of elevated pCO2. Here, we investigated the impacts of increased levels of carbon dioxide on behaviour using the goldsinny wrasse (Ctenolabrus rupestris), which is a common species in European coastal waters and widely used as cleaner fish to control sea lice infestation in commercial fish farming in Europe. The wrasses were exposed to control water conditions (370 µatm) or elevated pCO2 (995 µatm) for 1 month, during which time behavioural trials were performed. We investigated the possible effects of CO2 on behavioural lateralization, swimming activity, and prey and predator olfactory preferences, all behaviours where disturbances have previously been reported in other fish species after exposure to elevated CO2. Interestingly, we failed to detect effects of carbon dioxide for most behaviours investigated, excluding predator olfactory cue avoidance, where control fish initially avoided predator cue while the high CO2 group was indifferent. The present study therefore shows behavioural tolerance to increased levels of carbon dioxide in the goldsinny wrasse. We also highlight that individual fish can show disturbance in specific behaviours while being apparently unaffected by elevated pCO2 in other behavioural tests. However, using experiments with exposure times measured in weeks to predict possible effects of long-term drivers, such as ocean acidification, has limitations, and the behavioural effects from elevated pCO2 in this experiment cannot be viewed as proof that these fish would show the same reaction after decades of evolution.

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.

Emergence rates from the benthos of the parasitic juveniles of gnathiid isopods

Variation in the rate at which parasitic gnathiid isopod juveniles emerged from the benthos at Lizard Island, Great Barrier Reef, Australia, was examined (I) every 4 or 8 h throughout the day and night over a 24 h period, (2) over a 12 h period during the day or night, and (3) during different lunar phases (weeks). The number of gnathiids sampled per 4 or 8 h was low, with only 30% of the traps containing gnathiids and the abundance ranging from 0 to 3 gnathiids m(-2). The number of gnathiids that emerged over 12 h, in contrast, ranged from 0 to 36 m(-2). During the third and fifth weeks sampled, more gnathiids emerged during the day than at night. This coincided with the full moon and new moon. Most gnathiids that emerged from the reef during the day (98 %) had not fed, in contrast to those sampled at night (71%). Of the gnathiids with no engorged gut, most (97 %) of those collected during the day were small (II. mm) compared to those collected at night (19%), the latter being mostly >1 mm. Of the gnathiids with an engorged gut, most were sampled at night (83 %) and 97 % were >1 mm in size. These percentages suggest differences in the emergence behaviour among Life stages or species of gnathiids. This study, which shows that gnathiids do emerge during the day and supports other studies showing that gnathiids also attack fishes during the day, has important implications for understanding the role of cleaner fish and their main food source, gnathiids, as it shows there is a constant source of gnathiids emerging from the reef during the day and night in search of hosts.

Labroidaes dimidiatus (Valenciennes, 1839)

Labroides dimidiatus, is one of several species of cleaner wrasses found on coral reefs from Eastern Africa and the Red Sea to French Polynesia, for the first time from Iran (Persian Gulf, Kish Island). Like other cleaner wrasses, it eats parasites and dead tissue off larger fishes’ skin in a mutualistic relationship that provides food and protection for the wrasse, and considerable health benefits for the other fishes. Some fish mimic cleaner wrasses. For example, a species of blenny called Aspidontus taeniatus has evolved the same behavior to tear small pieces of flesh from bigger fish. Cleaner wrasses are usually found at cleaning stations. Cleaning stations are occupied by different units of cleaner wrasses, such as a group of youths, a pair of adults, or a group of females accompanied by a dominant male. When visitors come near the cleaning stations, the cleaner wrasses greet the visitors by performing a dance-like motion in which they move their rear up and down. The visitors are referred to as "clients". Blue streak cleaner wrasses clean to consume ectoparasites on client fish for food. The bigger fish recognise them as cleaner fish because they have a lateral stripe along the length of their bodies and by their movement patterns.

Signalling by the cleaner shrimp Periclimenes longicarpus

Signals increase the fitness of a sender by altering the behaviour of receivers. For cooperative interactions biological market theory proposes that signalling strength may be linked to supply and demand. In this context, a recent laboratory experiment demonstrated that cleaner shrimps may advertise their service to client reef fish and that the advertisement is linked to hunger levels. We investigated signalling by the cleaner shrimp Periclimenes longicarpus in the field to test more detailed predictions of biological market theory. Shrimps often clapped with their pair of claws in response to approaching clients. In line with both theory and the previous study, the probability of clapping increased when the shrimps had been food deprived and clapping shrimps were more likely to clean than nonclapping individuals. However, we found no evidence for the market theory prediction that signalling was targeted specifically to visiting client species with the option to choose other cleaning stations. Instead, shrimps signalled more frequently towards predatory clients than towards nonpredatory clients. We conclude that the signal does not serve primarily to attract the choosy clients but to convey information about identity as preconflict management to avoid predation.

CLEANER SHRIMP (CARIDEA: PALAEMONIDAE) ASSOCIATED WITH SCYPHOZOAN JELLYFISH

Shrimp are found in association with many hosts (sponges, anthozoans, mollusks, echinoids, ascidians and fish). Shrimp are rarely observed in association with jellyfish. The interaction between the cleaner shrimp Periclimenes paivai and jellyfish is poorly known, with only one published report for Brazilian waters. We add new information about this association, based on field and laboratory observations. Shrimp were collected from three locations on the coast Of Sao Paulo State (Cananeia, Santos and Sao Sebastiao) and from two species of scyphozoan rnedusae: Chrysaora lactea and Lychnorhiza lucerna. We classify the association as facultative commensalism, since the shrimp gain protection and probably feed on mucus produced by the jelly fish. The maximum carapace length of the shrimp collected was 9.2 min. Medusa bel I diameter ranged between about 10 and 19 cm for C. lactea and between 4.5 and 25 cm for L. lucerna. We also provide a list of records of Periclimenes in association with different scyphornedUsae, and additional information on the size and coloration of P. paivai.