Relationship between roving behaviour and the diet and client composition of the cleaner fish Labroides bicolor

Journal of Fish Biology (2012) 81, 210 219 doi:10.1111/j.1095-8649.2012.03330.x, available online at wileyonlinelibrary.com Relationship between roving behaviour and the diet and client composition of the cleaner fish Labroides bicolor J. Oates*, A. Manica*, R. Bshary and A. S. Grutter *Evolutionary Ecology Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, U.K., Institut de Biologie, Eco-Ethologie, Université de Neuchâtel, Neuchâtel CH-2009, Switzerland and School of Biological Sciences, The University of Queensland, Brisbane 4072, Australia (Received 7 November 2011, Accepted 26 March 2012) Diet analyses and observations of cleaning behaviour of two cleaner fishes revealed that Labroides bicolor fed more on client mucus, but Labroides dimidiatus fed more on ectoparasites, and that L. bicolor interacted with fewer species (36 species) compared with L. dimidiatus (44 species). The client species which contributed most to the dissimilarity between cleaner species were the dusky farmerfish Stegastes nigricans and bicolor chromis Chromis margaritifer damselfishes, which L. dimidiatus interacted with more often than L. bicolor, and the striated Ctenochaetus striatus and brown Acanthurus nigrofuscus surgeonfishes, which L. bicolor interacted with more; L. bicolor interacted with all parrotfishes (Scaridae) more. These results confirm the importance of repeated interactions and partner choice in determining the nature of interactions in mutualisms. Journal of Fish Biology 2012 The Fisheries Society of the British Isles Key words: behaviour; cheating; co-operation; coral reefs; mucus; mutualism. INTRODUCTION Co-operation between partners of different species (interspecific mutualism) may be maintained through repeated interactions (Trivers, 1971; Axelrod & Hamilton, 1981). Where repeated interactions do not occur, co-operative systems may break down because individuals lose the ability to control the behaviour of partners (Dugatkin & Wilson, 1991; Enquist & Leimar, 1993). Fish cleaning mutualisms, where cleaner fishes remove and eat parasites from a wide range of client fishes, but have the option to also remove client tissue, are an ideal model system to compare the effect of different levels of repeated interactions and partner control on feeding behaviour. The bluestreak cleaner wrasse Labroides dimidiatus (Valenciennes 1839) feed on parasites (Grutter, 1997) and they can greatly reduce the number of gnathiid isopods (Grutter, 1999a), which benefits clients because these parasites can be harmful (Hayes et al., 2011). Labroides dimidiatus also feeds on other items including client mucus, skin and scales (Grutter, 1997, 1999b). Fish mucus can have high calorific Author to whom correspondence should be addressed. Tel.: +61 7 3365 7386; email: a.grutter@uq.edu.au 210 Journal of Fish Biology 2012 The Fisheries Society of the British Isles

DIET AND CLIENTS OF TWO CLEANER FISHES 211 value (Gorlick, 1980; Arnal & Morand, 2001) and L. dimidiatus prefers bullethead parrotfish Chlorurus sordidus (Forsskål 1775) mucus to gnathiids (Grutter & Bshary, 2003), although the reason for this remains unclear. Since mucus serves an important immune function to clients (Ebran et al., 1999) and contains sun-screening compounds (Eckes et al., 2008), mucus feeding by cleaners has the potential to be costly to clients. Therefore, a conflict exists whereby clients prefer cleaners to co-operate by feeding on ectoparasites, while cleaners prefer to cheat by feeding on client mucus. Resident client species of L. dimidiatus typically punish cleaners by chasing them if they cheat, which encourages cleaners to provide a better service in the next interaction to avoid being punished again (Bshary & Grutter, 2002). Visitor client species typically respond to cheating by swimming off and visiting another cleaner for the next interaction (partner switching), which encourages cleaners to be more co-operative to ensure that clients return (Bshary & Schäffer, 2002). Evidence of the effectiveness of these control mechanisms is that gnathiid parasites are the most abundant food item in the diet of L. dimidiatus on Lizard and Heron Island in Australia (Grutter, 1997). A decrease in repeated interactions is predicted to destabilize co-operative behaviour (Dugatkin & Wilson, 1991) because it undermines the effectiveness of punishment (Bshary & Grutter, 2002) and partner switching (Bshary & Schäffer, 2002). Repeated interactions between cleaners and clients are predicted to decrease with increasing home range (Mills & Côté, 2010). Labroides dimidiatus has relatively small home ranges and some of its clients repeatedly visit the same cleaner (Randall, 1958). In contrast, adult bicolor cleaner wrasse Labroides bicolor Fowler & Bean 1928 rove over larger home ranges (Randall, 1958; Mills & Côté, 2010; Oates et al., 2010a). Indeed, L. bicolor inspects half as many individual clients per unit of time as L. dimidiatus, which means repeat encounters with the same client may be generally lower for L. bicolor (Mills & Côté, 2010). Roving also enables L. bicolor to seek out clients and actively choose and initiate interactions with them; indeed, L. bicolor cleans half the number of species compared with L. dimidiatus (Mills & Côté, 2010). Theory predicts this would diminish co-operative behaviour even further (Johnstone & Bshary, 2002). Accordingly, jolt rate (used as a measure of cheating) is higher in clients of L. bicolor than of L. dimidiatus (Oates et al., 2010a), and jolt rate increases as the encounters between L. bicolor and clients decrease (Oates et al., 2010b). Jolt frequency is correlated with mucus feeding in L. dimidiatus (Bshary & Grutter, 2002) and the cleaning goby Elacatinus evelynae (Böhlke & Robins 1968) (Soares et al., 2008). Jolts are an indirect measure of cheating since clients may vary in their tendency to jolt, and different cleaner species might vary in their propensity to cause jolts. Direct analyses of gut contents would allow verification of whether observed differences in client jolt rate correlate with cheating behaviour. Oates et al. (2010a) observed differences in client jolt rate between L. dimidiatus and L. bicolor in the same location. Gut analyses of L. dimidiatus collected in various locations in the Pacific Ocean (Randall, 1958) found parasites in all specimens, but in L. bicolor, only 25% contained parasites and 50% contained only a mucus-like substance. Although this suggests that the diet does differ between L. dimidiatus and L. bicolor, direct comparisons at the same site have not been carried out. In this study, gut contents of sympatric L. bicolor and L. dimidiatus were analysed.

212 J. OATES ET AL. In addition, it is likely that the differences in home range size of L. bicolor and L. dimidiatus may lead to differences in the client species that are served. Due to their large home ranges and roving behaviour, L. bicolor can actively seek out clients to initiate interactions with them, unlike L. dimidiatus which generally remains in a small area and must wait for clients to approach for cleaning interactions (Oates et al., 2010a). In this study, the client composition of L. bicolor and L. dimidiatus was compared in order to relate differences in client species composition to differences in behaviour of the two cleaner species. MATERIALS AND METHODS Observational data and samples for diet analysis of L. dimidiatus and L. bicolor were collected on Moorea Island in French Polynesia (17 29 S; 149 49 W) between March and April 2000. Observations were carried out on fringing reefs in Opunohu Bay, where both species are found at the same depths. GUT ANALYSES Eight L. dimidiatus and nine L. bicolor were collected by scuba divers using a hand net and barrier net between 0915 and 1720 hours. The fishes were killed immediately with a blow to the head and guts fixed underwater by injecting 50% formalin in filtered sea water into the gut cavity. Fishes were fixed 1 h later by placing them in 10% formalin in sea water and guts were dissected 2 3 days later and stored in 10% formalin in sea water. All L. dimidiatus showed adult colouration (5 6 6 9 cm standard length, L S ); five of the L. bicolor had grey colouration with a black lateral stripe (5 5 6 0 cml S ) and four had blue and black anterior regions with yellow posterior regions (5 9 7 6 cml S ) (Randall et al., 1997). Dark brown amorphous matter, most likely digested food (Grutter, 1997), was not included in the diet analyses because it was assumed that it would consist of the same relative proportions of the other food types. Only one gut from a blue and yellow L. bicolor (7 5 cml S ) had this matter and was excluded from the analyses. Although absolute values of cover per food category have previously been used in comparisons of cleaner fish stomach contents (Grutter, 1997), they were converted into proportions out of the total cover because it was difficult to compare absolute values between species due to the greater overall volume of L. bicolor guts and the fact that diet quantification methods were optimized for L. dimidiatus (Grutter, 1997). CLIENT COMPOSITION Focal observations (30 min) of 14 L. dimidiatus and 13 L. bicolor were carried out by snorkelling over the reef. All L. dimidiatus showed adult colouration; six of the L. bicolor had grey colouration with a black lateral stripe and seven had blue and black anterior regions with yellow posterior regions (Randall et al., 1997). Observations were carried out in different areas of the site to maximize the probability that each focal observation was on a different individual. There was substantial overlap in the location of focal L. bicolor and L. dimidiatus, so the same client species would have been available to all cleaners. For each cleaning interaction observed, the species of client and duration of each interaction was recorded. The total number of cleaning interactions with each client species is defined as the sum of the interactions per 30 min observation and these were used as individual samples for analysis. STATISTICAL ANALYSES All analysis was carried out using Community Analysis Package v3 (Pisces Conservation Ltd; www.piscesconservation.com). Non-metric multidimensional scaling (MDS) was used to group samples (individual cleaner fish) according to similarity in terms of (1) food cover

DIET AND CLIENTS OF TWO CLEANER FISHES 213 proportions and (2) client composition. As both food cover and client composition are quantitative measures, MDS was carried out using the Bray Curtis index. To avoid the species sample matrix being dominated by zeros, the MDS was carried out on a sub-set of the client composition data containing only species that were present in at least two samples. This involved removing 22 species from the client composition data; the client species were relatively equally spread between the two cleaners (Supporting information, Table SI). In order to prevent the results being driven by high numbers of cleaning interactions by both cleaner species with dusky farmerfish Stegastes nigricans (Lacépède 1802), the number and duration of client interactions were square root transformed to reduce the range and make it more likely that underlying patterns would not be masked. To test for significant differences between the two cleaner species in food cover proportions and client composition, an analysis of similarities (ANOSIM) was carried out. To quantify the contribution of each food type and client species to the total dissimilarity between cleaner species, similarity percentages analyses (SIMPER) were used. ANOSIM and SIMPER are widely used in the analysis of ecological species samples, including comparing stomach content samples (Batistic et al., 2005). For the overall comparison of total number of client species cleaned for each cleaner species, one randomly selected L. dimidiatus sample was excluded so that the sample number per cleaner species was balanced, otherwise a greater number of species may have been recorded for L. dimidiatus due to more sampling. GUT ANALYSES RESULTS The MDS plot (Fig. 1) showed that L. dimidiatus and L. bicolor gut content sample groups were generally overlapping so most of the food types were found 1 5 1 0 0 5 Axis 2 0 0 0 5 1 0 2 0 1 5 1 0 0 5 0 0 0 5 1 0 1 5 2 0 Axis 1 Fig. 1. Multidimensional scaling plot (2D) on the proportions of different food types grouped by cleaner type (, Labroides bicolor;, Labroides dimidiatus). Stress = 0 051. Overlapping points have been jiggered so they are visible.

214 J. OATES ET AL. Table I. Results of similarity percentages analysis on the proportion of food types in the gut samples of Labroides bicolor (n = 8) and Labroides dimidiatus (n = 8), showing all food types except parasitic gnathiid isopods (the contribution to the total dissimilarity for this food type was negligible and so is not included in the table). Values are given for food types showing average proportion across samples, average dissimilarity of samples and per cent contribution to the total dissimilarity Food type L. bicolor average proportion L. dimidiatus average proportion Average dissimilarity Per cent contribution Caligid copepods (parasitic) 0 09 0 55 25 9 30 8 Mucus 0 41 0 10 21 0 25 0 Non-parasitic copepods 0 07 0 25 11 4 13 6 Skin 0 21 0 10 5 12 5 Scales 0 09 0 11 8 10 3 in both species; L. dimidiatus samples formed a sub-group within the L. bicolor samples, suggesting that the diet of L. dimidiatus predominantly consists of a sub-set of the food types in the diet of L. bicolor. The difference between the proportions of different food types found in the guts of L. bicolor and L. dimidiatus was significant (ANOSIM, global sample statistic = 0 308, P<0 01, n = 8, 8). The SIMPER analysis (Table I) showed that parasitic caligid copepods and mucus contributed most to the differences in proportions of food types between cleaner species: the guts of L. dimidiatus had a greater proportion of caligid copepods, whereas L. bicolor had more mucus. There were also greater proportions of nonparasitic copepods and scales found in the guts of L. dimidiatus, and a greater proportion of skin found in the guts of L. bicolor (Table I). Gnathiid isopods were only found in the guts of one L. bicolor and one L. dimidiatus, so the contribution of this food type to the difference between cleaner species was very small. CLIENT COMPOSITION Labroides bicolor cleaned 36 species and L. dimidiatus cleaned 44 species, with 19 species cleaned by both types of cleaner. The MDS plot showed clear separation between L. dimidiatus and L. bicolor sample groups on the basis of the total number of cleaning interactions with different client species per sample (Fig. 2); this difference was significant (ANOSIM, global sample statistic = 0 239, P<0 01, n = 13, 14). The difference between cleaner species was also significant when considering the presence or absence of client species per sample (ANOSIM, global sample statistic = 0 304, P<0 01, n = 13, 14) and the total duration of interactions per species per sample (ANOSIM, global sample statistic = 0 276, P<0 01, n = 13, 14). The SIMPER analysis showed that the client species which contributed most to the dissimilarity between cleaner species were the dusky farmerfish S. nigricans (Pomacentridae or damselfish), which had more interactions per observation with L. dimidiatus than L. bicolor, and striated surgeonfish Ctenochaetus striatus (Quoy & Gaimard 1825) (Acanthuridae), which had more interactions with L. bicolor

DIET AND CLIENTS OF TWO CLEANER FISHES 215 2 0 1 5 1 0 0 5 Axis 2 0 0 0 5 1 0 1 5 2 0 2 0 1 5 1 0 0 5 0 0 0 5 1 0 1 5 Axis 1 Fig. 2. Multidimensional scaling plot (2D) on square root transformed client composition counts grouped by cleaner type (, Labroides bicolor;, Labroides dimidiatus). Stress = 0 147. (Table II). Other client species which accounted for high proportions of the dissimilarity between cleaner species were bicolor chromis Chromis margaritifer Fowler 1946 (Pomacentridae), which interacted more often with L. dimidiatus, and brown surgeonfish Acanthurus nigrofuscus (Forsskål 1775), which interacted more often with L. bicolor. All parrotfish (Scaridae) interacted more often with L. bicolor. DISCUSSION The diet of L. dimidiatus and L. bicolor in Moorea contained mainly the same food types, indicating their capacity to behave co-operatively by feeding on parasites and behave non-co-operatively by feeding on fish mucus, which clients probably need for protection against infection (Ebran et al., 1999) and ultraviolet radiation (Eckes et al., 2008). Labroides dimidiatus guts, however, contained a greater proportion of parasitic caligid copepods, whereas L. bicolor had more mucus. This shows that L. bicolor cheats more by feeding on client mucus more often than L. dimidiatus in Moorea, which corroborates observational evidence of higher client jolt rates involving L. bicolor at the same site (Oates et al., 2010a) and in Rangiroa Atoll (Mills & Côté, 2010). The results of this study are consistent with the concept that the client control mechanisms punishment (Bshary & Grutter, 2002) and partner switching (Bshary & Schäffer, 2002) are effective at ensuring that L. dimidiatus feeds on ectoparasites which are less preferred. As roving is likely to reduce the frequency of repeated interactions, it seems that clients may be less effective in using control mechanisms to prevent L. bicolor cleaners feeding on preferred mucus. In addition, the roving behaviour of L. bicolor is likely to give them a greater ability to initiate

216 J. OATES ET AL. Table II. Results of similarity percentages analysis on client composition for Labroides bicolor and Labroides dimidiatus, showing client species which contribute up to 90% of the total dissimilarity. Values are given for client species showing average number of individuals cleaned across samples, average dissimilarity of samples and per cent contribution to the total dissimilarity Client species L. bicolor average number of individuals cleaned L. dimidiatus average number of individuals cleaned Average dissimilarity Per cent contribution Mucus quality index of other species of same genera from Arnal et al. (2001) Dusky farmerfish Stegastes nigricans 4 4 6 0 15 8 23 5 2 5, 6 5 Striated surgeonfish Ctenochaetus striatus 2 7 1 8 5 4 8 0 Bicolor chromis Chromis margaritifer 0 2 1 7 4 3 6 4 5 5 Twotone tang Zebrasoma scopas 1 6 2 4 4 0 6 1 Brown surgeonfish Acanthurus nigrofuscus 1 6 0 8 3 9 5 8 11 5, 13 0 Floral wrasse Cheilinus chlorourus 1 3 0 3 3 3 4 9 Orange-lined triggerfish Balistapus undulatus 0 1 1 2 3 2 4 7 Manybar goatfish Parupeneus multifasciatus 0 2 1 2 3 2 4 7 Common parrotfish Scarus psittacus 1 1 0 3 0 4 4 14 5 Bluestreak cleaner wrasse Labroides dimidiatus 0 0 5 1 4 2 1 Bluespotted cornetfish Fistularia commersonii 0 1 0 4 1 3 2 0 Bullethead parrotfish Chlorurus sordidus 0 3 0 3 1 3 1 9 Soldierfish Myripristis sp. 0 5 0 1 2 1 7 Starspotted grouper Epinephelus hexagonatus 0 3 0 1 0 1 5 Yellowband parrotfish Scarus schlegeli 0 4 0 1 0 1 4 14 5 Raccoon butterflyfish Chaetodon lunula 0 0 3 0 9 1 4 Mailed butterflyfish Chaetodon reticulatusi 0 2 0 2 0 9 1 4 Red shoulder wrasse Stethojulis bandanensis 0 0 3 0 8 1 2 Sling-jaw wrasse Epibulis insidiator 0 2 0 1 0 8 1 2 Speckled butterflyfish Chaetodon citrinellus 0 2 0 1 0 8 1 2 Moorish idol Zanclus cornutus 0 2 0 2 0 7 1 1 Peacock hind Cephalopholis argus 0 0 3 0 7 1 1 Parrotfish Scarus sp. 0 2 0 2 0 7 1 1 14 5 Whitebar gregory Stegastes albifasciatus 0 1 0 2 0 7 1 1 2 5, 6 5 Half-and-half chromis Chromis iomelas 0 0 2 0 7 1 1 5 5

DIET AND CLIENTS OF TWO CLEANER FISHES 217 interactions, which may provide further leverage to increase cheating (Oates et al., 2010a). This provides support for a game theoretical model, which predicts that increasing control over the occurrence and duration of an interaction would lead to more cheating (Johnstone & Bshary, 2002). Although skin has been found in the diet of L. dimiditus elsewhere (Grutter, 1997), it was not in the diet of this species in this study. Most likely this is because skin is rarely eaten by cleaners, as Grutter (1997) only found it in one of 65 L. dimidiatus guts. The composition of clients and the cleaning interactions per client species also differed between the two cleaners. Labroides bicolor in this study cleaned fewer species than L. dimidiatus, as found by Mills & Côté (2010), indicating L. bicolor is more selective. More importantly, the cleaning interactions with particular species differed in terms of total number of cleaning interactions per observation, the presence or absence of species and the total duration of interactions per species. Among the client species which contributed most to the dissimilarity in the total number of interactions between cleaner species were S. nigricans and C. margaritifer (damselfishes), which L. dimidiatus interacted with more often than L. bicolor, and the striated C. striatus and brown A. nigrofuscus (surgeonfishes), which L. bicolor interacted with more; also, L. bicolor interacted with all parrotfishes (Scaridae) more. Mills & Côté (2010) also found a significant difference in client composition between L. bicolor and L. dimidiatus, but it is difficult to make specific comparisons with this study because it was carried out at a different location with higher species diversity (Rangiroa Atoll), and the authors did not quantify the contribution of each client species to the total dissimilarity between cleaner species. The study carried out by Mills & Côté (2010) did, however, also find that L. dimidiatus interacted more with S. nigricans and C. margaritifer compared with L. bicolor, but in contrast to this study, L. dimidiatus cleaned C. striatus more than L. bicolor. Labroides dimidiatus cleaners tend to remain in a small area waiting for clients to approach and are not able to seek out clients in the same way as roving L. bicolor (Oates et al., 2010a), which may explain the differences in the types of client species which are cleaned more often by L. dimidiatus. Considering that the diet of L. bicolor consists largely of mucus and that their large home ranges allow them to seek out clients (Oates et al., 2010a), it seems likely that L. bicolor may preferentially initiate interactions with certain species. This may partly be influenced by differences in client mucus quality, which can vary among client species (Gorlick, 1980; Arnal & Morand, 2001; Arnal et al., 2001). Indeed, client preference for the Hawaiian cleaner wrasse Labroides phthirophagus Randall 1958 is approximately positively correlated with mucus load and caloric value of client species (though this result may have been confounded by client size; Gorlick, 1980). Mediterranean cleaner wrasse Symphodus melanocercus (Risso 1810) tends to interact with clients with high-quality mucus more (Arnal & Morand, 2001), and it has been shown experimentally that L. dimidiatus prefers parrotfish C. sordidus (Forsskål 1775) mucus to snapper Lutjanus fulviflamma (Forsskål 1775) mucus (Grutter & Bshary, 2004). Due to the lack of data on client mucus at this study site, however, only general associations with published data on a genus level are possible. For example, in Barbados, Acanthurus and Scarus genera ranked highest on a mucus quality index (Arnal et al., 2001) and in this study, it was found that L. bicolor interacted with these genera more than L. dimidiatus (Table II). Labroides dimidiatus in this study also interacted more often than L. bicolor with species that

218 J. OATES ET AL. belong to genera that are associated with low mucus quality (Arnal et al., 2001), such as the damselfishes S. nigricans and C. margaritifer (Table II). When examining the client inspection rates in the study by Mills & Côté (2010), however, there is no clear relationship between mucus quality index and inspection rates for L. bicolor and L. dimidiatus. Clearly, more information is needed to determine the role of mucus quality in client choice. In conclusion, by showing that the diet of L. bicolor contains more mucus and fewer ectoparasites than L. dimidiatus, this study confirms that at this site roving behaviour in L. bicolor is associated with less co-operative feeding behaviour compared to L. dimidiatus. This difference in feeding behaviour is in agreement with the presumption that repeated interactions are likely to be infrequent in the large home ranges of L. bicolor, so partner control mechanisms cannot effectively reduce cheating. In addition, roving L. bicolor cleaners can actively seek out clients to initiate interactions with them (Oates et al., 2010a), which may be associated with the differences in client composition between L. dimidiatus and L. bicolor, found in this study. These findings also suggest that in this L. bicolor system, there may be a reversal of the partner choice system used by clients of L. dimidiatus (Bshary & Schäffer, 2002), because L. bicolor may be able to seek out preferred clients. These results confirm the importance of both repeated interactions and partner choice in determining the nature of interactions in mutualisms. Thanks to M. A. Johnson for his help in the field, C. Lo for facilitating the research, S. Marshall for entering the behavioural data into the computer and J. H. Choat for helpful discussions. Logistical support and approval for procedures and collections were provided by Le Centre de Recherches Insulaires et Observatoire de l Environnement de Polynésie Française (CRIOBE). The Australian Research Council (A.S.G.) funded this work. SUPPORTING INFORMATION Supporting Information may be found in the online version of this paper: Table SI. List of 22 client species cleaned by the cleaner species not present in at least two samples and hence omitted from the non-metric multidimensional scaling statistical analysis. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article. References Arnal, C. & Morand, S. (2001). Importance of ectoparasites and mucus in cleaning interactions in the Mediterranean cleaner wrasse Symphodus melanocercus. Marine Biology 138, 777 784. Arnal, C., Côté, I. M. & Morand, S. (2001). Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behavioural Ecology and sociobiology 51, 1 7. Axelrod, R. & Hamilton, W. D. (1981). The evolution of cooperation. Science 211, 1390 1396. Batistic, M., Tutman, P., Bojanic, D., Skaramuca, B., Kozul, V., Glavic, N. & Bartulovic, V. (2005). Diet and diel feeding activity of juvenile pompano (Trachinotus ovatus)

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