Cleaner Fish Drives Local Fish Diversity on Coral Reefs

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provided by Elsevier - Publisher Connector Current Biology, Vol. 13, 64–67, January 8, 2003, 2003 Elsevier Science Ltd. All rights reserved. PII S0960-9822(02)01393-3 Cleaner Fish Drives Local Fish Diversity on Coral Reefs

Alexandra S. Grutter,1,* Jan Maree Murphy,1,3 cies visit cleaner fish up to a mean 144 times a day [4]. and J. Howard Choat2 In the absence of such cleaning, which involves the 1Department of Zoology and Entomology removal of a mean 1218 parasites per day per cleaner University of Queensland [6], caged Hemigymnus melapterus fish that are placed Brisbane, Queensland 4072 on coral reefs experience a 4.5-fold increase in parasite Australia loads within 12 hr [10]. This level of interactions raises 2 Department of Marine Biology and Aquaculture the question of whether cleaner fish affect the local James Cook University abundance and distribution of coral reef fish. Higher Townsville, Queensland 4811 local-scale species diversity and increased abundance Australia of fish have been associated with the presence of cleaner fish, suggesting that clients are attracted to cleaners [11, 12]. Limbaugh [13] also suggested that Summary good fishing sites were located near cleaning stations. However, other sources of client attraction have not Coral reefs are one of the most diverse habitats in been taken into account [14, 15]. Limbaugh’s [13] uncon- the world [1], yet our understanding of the processes trolled qualitative study suggested that removing all affecting their biodiversity is limited [1–3]. At the local cleaner organisms resulted in a reduction of non-territo- scale, cleaner fish are thought to have a disproportion- rial fish. Recent quantitative studies, on the contrary, ate effect, in relation to their abundance and size, on have failed to find an effect of cleaner fish on the abun- the activity of many other fish species, but confirma- dance or diversity of client fish [16–21]. The lack of tion of this species’ effect on local fish diversity has experimental evidence that cleaners affect client fish proved elusive. The cleaner fish Labroides dimidiatus diversity has been interpreted to mean that cleaners has major effects on fish activity patterns [4] and may do not cause, but rather respond to, patterns of client indirectly affect fish demography through the removal distribution [14, 22]. Finally, controlled studies to date of large numbers of parasites [5, 6]. Here we show [17–21] have not separated the clients according to their that small reefs where L. dimidiatus had been experi- ability to move among reefs. However, in contrast to mentally excluded for 18 months had half the species resident client fish and cleaner fish [8], “visiting” client diversity of fish and one-fourth the abundance of indi- fish are highly mobile and can move among reefs. Visi- viduals. Only fish that move among reefs, however, tors include roving carnivores and piscivores that can were affected. These fish include large species that themselves influence local patterns of reef fish abun- themselves can affect other reef organisms [2, 7]. In dance and diversity. To resolve the controversial ques- contrast, the distribution of resident fish was not af- tion of whether cleaners affect client fish distribution, fected by cleaner fish. Thus, many fish appear to we tested whether cleaner fish affected the distribution choose reefs based on the presence of cleaner fish. of “visiting” and resident fish by using a long-term (18 Our findings indicate that a single small [8] and not month) and large-scale (18 reef) field experiment. very abundant [9] fish has a strong influence on the We found that the number of species of visiting client movement patterns, habitat choice, activity, and local fish as well as the number of visiting individuals, when diversity and abundance of a wide variety of reef fish sampled by remote video and by a snorkeler, were two- species. and four-fold higher, respectively, on reefs with cleaner fish than on reefs without (Figure 1) (for species and Results and Discussion individuals sampled by remote video, respectively: ex-

act F ϭ 8.661,12, P ϭ 0.012 and exact F ϭ 7.241,12, P ϭ

Fish communities are the most diverse vertebrate com- 0.020; and by snorkeler: exact F ϭ 14.451,12, P ϭ 0.003

munities in the world, with their highest diversity being and exact F ϭ 8.431,12, P ϭ 0.013). Similarly, when sam- found on coral reefs [2, 7]. At the local scale, coral reef pled by a scuba diver, reefs with cleaner fish also had fish diversity is explained by apparently stochastic (i.e., more species of visiting clients than reefs without recruitment, perturbation), ecological, and deterministic cleaner fish, but the difference was less (Figure 2) (F ϭ

(i.e., competition, predation) processes [2, 7], most of 7.0611,1, P ϭ 0.021); this implies that visiting clients were whose relative effects are highly controversial, the latter disturbed by scuba divers but not by the remote video partly because of the complex multispecies interactions or snorkelers. Resident client species, in contrast, were involved. One of the most common interspecific interac- not affected by the presence of cleaner fish (Figure 2)

tions of coral reef fish involves those with cleaner fish. (F ϭ 2.4001,1, P ϭ 0.147). For example, on the Great Barrier Reef a mean 2297 In all analyses, the number of species of fish at the client fish interact with a single cleaner fish, Labroides Casuarina Beach site was significantly higher than at dimidiatus, each day [6]; individuals of some client spe- the Lagoon site (Figure 1A) (remote video: exact F ϭ 5.411,12, P ϭ 0.038. Snorkeler: exact F ϭ 9.111,12, P ϭ ϭ ϭ *Correspondence: [email protected] 0.011. Scuba: F 12.4241,1, P 0.004), and this did not 3 Present address: Animal Research Institute, 665 Fairfield Road, vary with cleaner-fish presence (all P Ͼ 0.37). These Yeerongpilly, Queensland 4105, Australia. results were not surprising because other studies have Brief Communication 65

the interaction between cleaner presence and the site (P ϭ 0.488) on fish abundance were not significant. When sampled by remote video and snorkeler, the abundance of fish did not vary among times, nor were any interactions with time significant (all P Ͼ 0.29), although the interaction between site and time was almost signifi-

cant (exact F ϭ 4.6501,12, P ϭ 0.052). Of the 78 visiting species, 38% (belonging to the Acanthuridae, Balistidae, Carangidae, Dasyatidae, Hae- mulidae, Holocentridae, Labridae, Lethrinidae, Lutjani- dae, Priacanthidae, Scaridae, Siganidae, and Sphyrae- nidae) were found only on reefs with cleaner fish, 52% (Acanthuridae, Ephippidae, Hemigaleidae, Haemulidae, Holocentridae, Labridae, Lethrinidae, Lutjanidae, Mulli- dae, Nemipteridae, Pomacanthidae, Scaridae, Sigani- dae) were found both on reefs with and on reefs without cleaner fish, and 9% (Acanthuridae, Carangidae, Carch- arhinidae, Holocentridae, Labridae) were only found on reefs without cleaner fish. The cleaner fish L. dimidiatus has a major influence on the local demography, species assemblage, movement patterns, and habitat choice of coral reef fishes, and this influence is disproportionate to its abundance and Figure 1. Mean (s.e.) Visiting Client Fish Numbers per Reef at Two size. Our findings add to the body of work suggesting Sites Counted by Remote Video and by a Snorkeler that cleaner fish have major effects on individual fish (A) The number of visiting species on reefs with (closed symbols) activity patterns [4, 6] and, indirectly, on demography and without (open symbols) cleaner fish at Casuarina Beach (circles) because of the potential health benefits they may pro- and Lagoon (squares) sites. vide by removing large numbers of parasites [6, 10]. (B) The log10 (x ϩ 1) abundance of visiting client fish per reef. Symbols are as in (A). Counts in (A) and (B) were pooled across different These results argue for a functionally significant role of times of the day. cleaner fish on the composition of reef fish species. The presence of cleaners in an area or type of habitat may in part explain the distribution of many fishes. Further- shown that coral reef fish diversity varies spatially [9, 23]. more, we detected an effect of cleaners at two different When sampled by remote video and snorkel, species sites. Thus, although the study was done on only one number did not vary between sampling times, nor were island, our study suggests that estimates of abundance ϫ any interactions with time (time cleaner presence, for reef fishes for larger spatial-scale comparisons, such ϫ ϫ ϫ time site, time cleaner presence site) significant as regional comparisons, should err on the cautious side Ͼ (all P 0.15). The number of resident species did not and account for the strong influence of the presence differ between sites (Figure 2), nor was the interaction and activities of a single taxon, L. dimidiatus, on local between the cleaner-fish presence and site significant fish diversity estimates. Furthermore, this effect appears Ͼ (all P 0.77). to be restricted to a particular group of fishes, those When sampled by remote video, the effect of the site that move among reefs. Such fish appear to base their (Figure 1B) and the interaction between the site and choice of a suitable habitat at least partly on the pres- cleaner presence on fish abundance were not significant ence of cleaner fish. That these fish mainly consist of Ͼ (all P 0.57). When sampled by snorkeler, the effect of large roving carnivores and herbivores, which them- ϭ ϭ the site (exact F 4.121,12, P 0.065) (Figure 1B) and selves can affect other reef organisms [2, 7], is an addi- tional effect with potentially significant ecological implications. For residents, which were not affected by cleaner-fish presence, the costs of seeking cleaners, (e.g., increased predation risk when moving between reefs, loss of territory, and energy output) may outweigh the costs of not being cleaned [20, 24]. Or, if the costs of not being cleaned increase with time, it is possible that a longer period without cleaners may be needed to detect an effect on resident fish distributions. Finally, resident fish are generally small and so may have few parasites. Although this may imply that the benefits of cleaning are therefore less for residents than for visitors, the opposite may be true; smaller fish may be more Figure 2. Mean (s.e.) Visiting and Resident Client Fish Species per vulnerable to parasites because of their small size. Reef at Two Sites as Counted by a Scuba Diver Although a previous study using 16 of the same reefs Symbols are as for Figure 1. Counts were pooled across different found no effect of cleaner fish either on fish species times of the day. number or on total abundance counted by a scuba diver Current Biology 66

after 3 and 6 months, it did not separate fish into resi- Fish in the field of view of two video cameras (Sony digital Handi- dents and visitors [21]. A subsequent analysis of that cam DCR-VX1000E) in underwater housings (Amphibico VX1000 ϫ data, however, tested for an effect of cleaner presence housings) with a .55 port were recorded for 65 min. Cameras were placed on the edge of the reef so that they maximized the area of and site by using only the visiting species and found no reef recorded (the maximum angle of view was 64Њ). Each day (March effect of cleaners on species number and fish abun- 21–30 and April 17, 2002) one reef with and one without cleaners dance after 6 months (both P Ͼ 0.50, A.S.G., unpub- from the same site were selected at random, with the order of lished data). The reason that an effect was detected at sites also being random. Recordings were made in the morning and 18 months rather than earlier may be that some fish afternoon (beginning between 0851 and 0957 or 1528 and 1611 hr). need time to adjust to new conditions at other cleaning We selected times that would maximize available light. Cameras were turned on by a snorkeler at least 15 min after scuba divers stations (e.g., establish a position in a hierarchy, avoid securing cameras had exited the water. predators, or find food); alternatively, they might wait Counts by a snorkeler involved slowly approaching each of the until the costs of increased parasite loads outweigh the reefs at one site and swimming around it for about three min. Counts costs of finding a new reef. were made in the morning (0956–1127 hr), noon (1119–1243 hr), and That cleaner fish affect the local distribution of many afternoon (1435–1637 hr) on April 3, 4, and 12, 2002, respectively. coral reef fishes at Lizard Island has broad implications Each time period was sampled on a separate day, and hence time periods are confounded with day. for understanding fish community structure and coral A scuba diver counted the number of species of visiting and reef management. In addition to predation, competition, resident fish per reef for approximately 30 min and sampled two to and ecological and stochastic processes [2, 7], cleaner four reefs per day (April 13, 14, and 16–19, 2002) between 0800 and fish also appear to affect the local distribution of fish. 1030 hr except for two reefs (1 and 11) that were sampled between Many of the visiting fish species are of commercial value 1334 and 1610 hr. The order of reefs sampled by the snorkeler and [25]. Some fish travel long distances to be cleaned [26], scuba diver involved alternating between sites and between reefs with and without cleaners. Pairs of reefs were selected at random. and thus the effects of cleaners may extend much farther than the vicinity of reef. Introductions of cleaner fish Removal of Cleaner Fish may be useful for increasing fish diversity on artificial Cleaner fish Labroides dimidiatus were removed with a barrier net or damaged reefs. The aquarium fish industry, which and handnet (two to six adults and zero to three juveniles per reef) includes cleaner fish, is rapidly growing [27]. Our results from nine patch reefs and counted (one to five adults and zero to suggest that caution should be exercised in allowing one juvenile per reef) on nine control patch reefs from two sites (Casuarina Beach and Lagoon) on Lizard Island, Australia [20] on the removal of cleaners from reefs on a commercial Sept. 9–18, 2000. Control reefs were similarly disturbed to the “re- scale. Furthermore, reports of marine diseases, includ- moval” reefs by the process of counting cleaners. The same reefs ing those in fish, are increasing, and the current trend (29–245 m2 ) as in Grutter [20], but with different treatments (cleaner of a warming climate will only augment this rate [28]. In fish presence), were used plus two reefs (17 and 18, 137 and 42 m2 such situations, the ecological role of cleaner fish, with located northeast and east to reef 12, respectively) (see map in their ability to reduce fish parasite loads [10], should Grutter [20]). Reefs 2–4, 6, 8, 11, 14, 17, and 18 were removal reefs; reefs 1, 5, 7, 9, 10, 12, 13, 15, and 16 were controls [20]. Reefs were therefore not be ignored. Indeed, increased cleaning surveyed again at several-month intervals (November 6–17, 2000; rates correlated with increased water temperatures have January 4–16, April 15, August 14–24, and November 29–30, 2001; been observed [29]. Cleaner organisms are widespread and January 28–February 1 and March 21–26, 2002) and new cleaner in marine and freshwater environments [30]; this study fish were removed from “removal” reefs (one to three juveniles per shows that on coral reefs the cleaner fish L. dimidiatus reef on one to two reefs per time, except in November 2001 and plays a key ecological role. January 2002, which had two to five and one to three juveniles on five and four reefs, respectively, excluding reefs 14 and 17; see statistical-analyses section below). Two removal reefs remained free Experimental Procedures of cleaners at all times. At the end of the experiment, control reefs had two to three adults and zero to four juveniles. Fish Counts Using three different methods, we examined whether the abundance Statistical Analyses and number of species of visiting clients varied between reefs with To test for an effect of cleaner-fish presence and site on the total cleaner fish and reefs with all cleaner fish excluded for 18 months. abundance of visiting fish and the number of species per reef, we To avoid disturbing visiting clients, we counted fish by using remote used four separate multivariate two-factor repeated-measures anal- underwater video and by snorkeling on the water surface. Counts yses of variance (ANOVA) for counts made by remote video and by were replicated at two sites (Casuarina Beach and Lagoon) [21] on a snorkeler. Time of day was used as the repeated measure. We Lizard Island, Great Barrier Reef and were made at different times used separate two-factor ANOVAs to test for an effect of cleaner of the day to account for any diurnal variation in abundance. For presence and site on the number of visiting and resident species comparison with resident fishes (fish that cannot move among reefs) per reef sampled by a scuba diver. The effect of reef area [20] as that are not easily disturbed by observers and can only be reliably a covariate was initially included in all analyses but was omitted counted by a scuba diver, resident fish species in addition to visiting from the analyses when it was consistently found to be nonsignifi- ϩ species were also counted by a scuba diver. Visiting fish less than cant. The total abundance of fish was log10(x 1) transformed to 2 m from reefs were counted. Visiting fish were defined as adult satisfy the assumptions of homogeneity of variance. Two “removal” fish that could have moved among reefs during the course of the reefs (14 and 17) that had been recolonized by a juvenile cleaner fish study. The species list was drawn from knowledge obtained from at the time of the counts were omitted from the analyses because the hundreds of hours of scuba diving by A.S.G. on the same patch cleaners were observed interacting with many fish throughout the reefs in previous studies [10, 20, 21, 31] and was based on observa- fish counts. tions of species seen moving between reefs or of species that had not always been present on the reefs. The 18 month duration of the Acknowledgments study was chosen because it was longer than most other removal studies [13, 17, 18, 20, 21] (but see Gorlick [19]), covered all seasons We thank S. Box, K. Coufal, C. Fury, K. Jennings, M. Johnson, S. within a year, and the beginning and end dates coincided with peri- Ivermee, A. O’Toole, and the Lizard Island Research Station staff ods of low recruitment of cleaner-fish juveniles [20]. for assistance in the field; J. Ackerman and W. Robbins for technical Brief Communication 67

assistance; and J. Becker, M. Blows, D. Green, E. Krebs, E. McGraw, 22. Coˆ te´ , I. (2000). Evolution and ecology of cleaning symbioses in V. Olson, M. Srinivasan, and R. Warner for commenting on the manu- the sea. Oceanography and Marine Biology: An Annual Review script. This research was supported by grants to A.S.G. from the 38, 311–355. Australian Research Council and the University of Queensland. 23. Choat, J.H., and Bellwood, D.R. (1985). Interactions amongst herbivorous fishes on a coral reef: influence of spatial variation. Received: September 16, 2002 Mar. Biol. 89, 221–234. Revised: October 23, 2002 24. Cheney, K.L., and Coˆ te´ , I. (2001). Are Caribbean cleaning symbi- Accepted: October 23, 2002 osis mutalistic? Costs and benefits of visiting cleaning stations Published: January 8, 2003 to longfin damselfish. Anim. Behav. 62, 927–933. 25. Dalzell, P., Adams, T.J.H., and Polunin, N.V.C. (1996). Coastal References fisheries in the pacific islands. Oceanography and Marine Biol- ogy: An Annual Review 34, 395–531. 1. Reaka-Kudla, M.L. (1997). The global biodiversity of coral reefs: 26. Randall, J.E. (1958). A review of the labrid fish genus Labroides, a comparison with rain forests. In: Biodiversity II: Understanding with description of two new species and notes on ecology. and Protecting Our Biological Resources, M.L. Reaka-Kudla, Pacific Science 12, 327–347. D.E. Wilson, and E.O. Wilson, Eds. (Washington, D.C.: Joseph 27. Edwards, A.J., and Shepherd, A.L. (1992). Environmental impli- Henry Press), pp. 83-108. cations of aquarium-fish collection in the Maldives, with propos- 2. Sale, P.F. (2002). Coral Reef Fishes: Dynamics and Diversity in als for regulation. Environ. Conserv. 19, 61–72. a Complex Ecosystem. (Boston, MA: Academic Press). 28. Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, 3. Bellwood, D.R., and Hughes, T.P. (2001). Regional-scale assem- P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D., bly rules and biodiversity of coral reefs. Science 292, 1532–1534. Overstreet, R.M., et al. (1999). Emerging marine diseases - cli- 4. Grutter, A.S. (1995). The relationship between cleaning rates mate links and anthropogenic factors. Science 285, 1505–1509. and ectoparasite loads in coral reef fishes. Mar. Ecol. Prog. Ser. 29. Parker, R.O., Jr., and Dixon, R.L. (1998). Changes in a North 118, 51–58. Carolina reef fish community after 15 years of intense fishing— 5. Grutter, A.S. (1997). Spatio-temporal variation and feeding se- global warming implications. Trans. Amer. Fish. Soc. 127, lectivity in the diet of the cleaner fish Labroides dimidiatus. 908–920. Copeia, 1997, 346–355. 30. Grutter, A.S. (2002). Cleaning behaviour: from the parasite’s 6. Grutter, A.S. (1996). Parasite removal rates by the cleaner perspective. Parasitology S65–S81. wrasse Labroides dimidiatus. Mar. Ecol. Prog. Ser. 130, 61–70. 31. Grutter, A.S., and Poulin, R. (1998). Cleaning of coral reef fishes 7. Sale, P.F. (1991). The Ecology of Fishes on Coral Reefs. (San by the wrasse Labroides dimidiatus: influence of client body Diego, CA: Academic Press). size and phylogeny. Copeia 1998, 120–127. 8. Robertson, D.R., and Choat, J.H. (1974). Protogynous hermaph- roditism and social systems in labrid fish. Proceedings of the Second International Coral Reef Symposium, 217–225. 9. Green, A.L. (1996). Spatial, temporal and ontogenetic patterns of habitat use by coral reef fishes (Family Labridae). Mar. Ecol. Prog. Ser. 133, 1–11. 10. Grutter, A.S. (1999). Cleaner fish really do clean. Nature 398, 672–673. 11. Potts, G.W. (1973). The ethology of Labroides dimidiatus (Cuv. & Val.) (Labridae, Pisces) on Aldabra. Anim. Behav. 21, 250–291. 12. Slobodkin, L.B., and Fishelson, L. (1974). The effect of the cleaner-fish Labroides dimidiatus on the point diversity of fishes on the reef front at Eilat. Am. Nat. 108, 369–376. 13. Limbaugh, C. (1961). Cleaning symbiosis. Scientific American 205, 42–49. 14. Johnson, W.S., and Ruben, P. (1988). Cleaning behavior of Bodi- anus rufus, Thalassoma bifasciatum, Gobiosoma evelynae, and Periclimenes pedersoni along a depth gradient at Salt River Submarine Canyon, St. Croix. Environmental Biology of Fishes 23, 225–232. 15. Gorlick, D.L., Atkins, P.D., and Losey, G.S., Jr. (1978). Cleaning stations as water holes, garbage dumps, and sites for the evolution of reciprocal altruism? Am. Nat. 112, 341–353. 16. Whiteman, E.A., Coˆ te´ , I.M., and Reynolds, J.D. (2002). Do cleaning stations affect the distribution of territorial reef fishes? Coral Reefs 21, 245–251. 17. Youngbluth, M.J. (1968). Aspects of the ecology and ethology of the cleaning fish, Labroides phthirophagus Randall. Z. Tier- psychol. 25, 915–932. 18. Losey, G.S. (1972). The ecological importance of cleaning symbiosis. Copeia 1972, 820-833. 19. Gorlick, D.L., Atkins, P.D., and Losey, G.S. (1987). Effect of cleaning by Labroides dimidiatus (Labridae) on an ectoparasite population infecting Pomacentrus vaiuli (Pomacentridae) at En- ewetak Atoll. Copeia 1987, 41–45. 20. Grutter, A.S. (1996). Experimental demonstration of no effect by the cleaner wrasse Labroides dimidiatus (Cuvier and Valen- ciennes) on the host fish Pomacentrus moluccensis (Bleeker). J. Exp. Mar. Biol. Ecol. 196, 285–298. 21. Grutter, A.S. (1997). Effect of the removal of cleaner fish on the abundance and species composition of reef fish. Oecologia 111, 137–143.