Galaxea, Journal of Coral Reef Studies 22: 31-36（2020）

Note

Filling an empty role: first report of cleaning by pygmy angelfishes Centropyge( , Pomacanthidae)

Pauline NARVAEZ*1, 2, 3 and Renato A. MORAIS1, 3

1 ARC Centre of Excellence for Coral Reef Studies, 1 James Cook Drive, Townsville, Queensland 4810, Australia 2 Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, 1 James Cook Drive, Townsville, Queensland 4810, Australia 3 College of Science and Engineering, James Cook University, 1 James Cook Drive, Townsville, Queensland 4810, Aus­ tralia

* Corresponding author: Pauline Narvaez E-mail: [email protected]

Communicated by Frederic Sinniger (Associate Editor-in-Chief)

Abstract Cleaner fishes remove ectoparasites, mucus and search of ectoparasites, mucus, and dead or diseased dead tissues from other ‘client’ organisms. These mutu­ tissue (Côté 2000; Côté and Soares 2011). Cleaners have alistic interactions provide benefits for the ‘clients’ and, been classified as either dedicated or facultative, depend­ on a larger scale, maintain healthy reef ecosystems. Here, ing on their degree of reliance on cleaning interactions for we report two species of angelfishes, Centropyge bicolor accessing food (Vaughan et al. 2017). While dedicated and C. tibicen, acting as cleaners of the blue tang cleaners rely almost exclusively on cleaning, facultative Paracanthurus hepatus in an aquarium. This observation ones also exploit other food sources. In total, 208 fish and is the first time that pygmy angelfishes are recorded 51 shrimp species have been reported as either dedicated cleaning in any en­vironment. This novel cleaning ob­ or facultative cleaners (Vaughan et al. 2017). servation raises ques­tions on the ecosystem role of cleaner Previous studies have shown that cleaning interactions fishes and which biological traits facilitate cleaning. are widespread in the marine environment, although par­ ticularly prevalent on tropical reefs (Arnal et al. 2001; Keywords Cleaning behaviour, cleaning interaction, angel­ Vaughan et al. 2017). For example, the dedicated blue­ fishes, Centropyge bicolor, Centropyge tibicen streak cleaner wrasse, Labroides dimidiatus (Valenciennes, 1839), can inspect almost 2,300 ‘clients’ and consume up to 1,200 gnathiid ectoparasites per day (Grutter 1996). Introduction The activity of L. dimidiatus has positive effects at the reef scale, such as increased individual growth and re­ Cleaning symbiosis is one of the most widely used ex­ cruitment success (Waldie et al. 2011; Sun et al. 2015). amples of mutualistic associations (Cushman and Beattie Gobies and wrasses (families Gobiidae and Labridae 1991; Côté 2000). In marine ecosystems, cleaners are respectively) encompass all known dedicated cleaner usually small fish or shrimp species that inspect the body, fishes (Côté 2000; Vaughan et al. 2017). Whereas the most gills, and buccal cavity of other ‘client’ organisms in common facultative cleaners are wrasses (63 species 32 Narvaez and Morais: Cleaning behaviour pygmy angelfishes recorded, see Vaughan et al. 2017), many other families been shown to increase the chance that ‘clients’ are in­ include facultative species. For example, butterflyfishes spected by cleaners (Côté et al. 1998). The angelfishes (Chaetodontidae) and angelfishes (Pomacanthidae) have reacted to this signalling by inspecting the body surface of been reported multiple times exercising this role (e.g. P. hepatus and engaging in what are likely cleaning in­ Sazima et al. 1999; Sazima and Sazima 2001; Konow et teractions (a video of this cleaning behaviour can be viewed al. 2006; Morais et al. 2017). here: https://figshare.com/articles/Electronic_Supplementary Angelfishes of the genera Holacanthus Lacepède, 1802 _Material_Narvaez_and_Morais_mp4/12743861/1). Each and Pomacanthus Lacepède, 1802 are conspicuous coral interaction included up to seven repeated cleaning bouts, reef fishes that can also be active cleaners (see Table 1), sometimes followed by the ‘client’ jolting and subsequent especially as juveniles (Randall 2005). However, to the ceasing of the interaction. In addition to the angelfishes, best of our knowledge, the closely related pygmy angel­ we recorded a citron butterflyfish Chaetodon citrinellus fishes of the genus Centropyge Kaup, 1860 have never Cuvier, 1831 with 9 cm total length joining the cleaning been reported to clean, either in the wild or in captivity. interactions on one occasion. This C. citrinellus individual Here, we report, for the first time, cleaning by two Cen­ was observed engaging in cleaning behaviour by picking tropyge species. skin material from a posing blue tang. At the time of the observations, the aquarium hosted a variety of fishes with different morphological and behavioural traits, but no Material and Methods known dedicated or facultative cleaner organisms other than the citron butterflyfish (Grutter 2002). On three occasions in March 2017, we observed and An important feature of the interactions observed was video-recorded four bicolor angelfish Centropyge bicolor the occurrence of jolting behaviour from the clients in Bloch, 1787 individuals and one keyhole angelfish Cen­ response to some of the cleaners’ bites. Jolting behaviour tropyge tibicen Cuvier, 1831 inspecting and cleaning vari­ suggests the delivery of painful bites by the cleaners ous individuals of the blue tang Paracanthurus hepatus (Soares et al. 2008) and has been reported for both dedi­ (Linnaeus, 1766) in a large display aquarium (a 6 m height cated and facultative cleaners (e.g. Arnal and Morand cylindrical aquarium with closed re-circulation system 2001; Bshary and Grutter 2002; Soares et al. 2008; Oates manufactured by Advanced Aquarium Technologies© and et al. 2012; Narvaez et al. 2015). Clients may jolt in re­ containing 10,000 m3 of artificial sea water) at James sponse to deliberate cheating from the cleaner, such as Cook University, Townsville, Australia. The four C. bicolor when the dedicated cleaner wrasse Labroides dimidiatus ranged in size from 8 to 10 cm total length, whereas the or the cleaner goby Elacatinus prochilos remove mucus only individual C. tibicen was approximately 7 cm total instead of parasites (Grutter and Bshary 2004; Soares et length. Based on their size, all five were likely adults al. 2008); or to unintentionally painful bites. It is unlikely (Thresher and Brothers 1985). that rare cleaners such as Centropyge tibicen and C. bicolor would use behaviourally elaborate strategies such as occasional cheating to willingly remove mucus or other Results and Discussion healthy tissues from their ‘clients’. Moreover, the aqua­ rium where the observations took place was constantly Individuals from both species, Centropyge bicolor and provided with abundant and varied external food sources, C. tibicen, inspected Paracanthurus hepatus together (Fig. significantly decreasing the chances of potential cheating 1 A and B) or individually (Fig. 1 C and D). P. hepatus behaviour from cleaners being induced by food depri­ individuals repeatedly presented their body flanks and vation. Thus, we consider that Paracanthurus hepatus belly to the angelfishes, while spreading their pectoral fins probably jolted in response to unintentionally painful in an almost immobile pose. This type of visual displays bites from C. tibicen and C. bicolor. has been interpreted as willingness to be cleaned and has Pygmy angelfishes and the citron butterflyfish were the Narvaez and Morais: Cleaning behaviour pygmy angelfishes 33

Table 1 Fish species from the Pomacanthidae family reported as cleaners. † Distribution data from fishbase.org Type of Cleaning † Relevant Species Distribution environment of lifestyle References observations Western Atlantic: New England (USA) to Pomacanthus Brockmann and Facultative Rio de Janeiro, Brazil; Gulf of Mexico; Wild arcuatus Hailman (1976) Caribbean Indo-Pacific: Red Sea and East Africa to the Hawaiian, Line and Tuamoto islands, Pomacanthus Konow et al. Facultative north to southern Japan and the Ogasawara Wild imperator (2006) Islands, south to the Great Barrier Reef, New Caledonia, and the Austral Islands Western Atlantic: Florida (USA), Bahamas Pomacanthus Sazima et al. Facultative to Brazil, including Gulf of Mexico and Wild paru (1999) Caribbean Pomacanthus Eastern Pacific: Gulf of California; north McCourt and Facultative Wild zonipectus of Bahía Magdalena, Mexico to Peru Thomson (1984) Western Atlantic: Bermuda, Bahamas, Holacanthus Facultative southern Florida, (USA) to Gulf of Wild Thresher (1979) bermudensis Mexico, including Yucatan (Mexico) Western Atlantic: Florida (USA) and Holacanthus Facultative Gulf of Mexico to Brazil. Eastern Central Wild Thresher (1979) ciliaris Atlantic: St. Paul's Rocks Eastern Central Pacific: southern tip of Baja California, Mexico; also from Holacanthus Facultative Clarion, and the Revillagigedo Group off Wild Michael (1993) clarionensis the western coast of Mexico and from Clipperton Island Holacanthus Facultative Eastern Pacific: Clipperton Island Wild Feder (1966) limbaughi Holacanthus Eastern Pacific: Gulf of California to Peru; Facultative Wild Feder (1966) passer Galapagos Islands Western Atlantic: Georgia (USA), Thresher (1979); Holacanthus Facultative Bermuda, and northern Gulf of Mexico to Wild Gasparini and tricolor Santa Catarina, Brazil Floeter (2001) Indo-Pacific: East Africa to the Samoan Centropyge and Phoenix Islands, north to southern Facultative Aquarium Our study bicolor Japan, south to New Caledonia; throughout Micronesia Western Pacific: Christmas Island in the eastern Indian Ocean to Fiji, north to Centropyge Facultative southern Japan, south to Scott Reef (eastern Aquarium Our study tibicen Indian Ocean) and Lord Howe Island. Uncommon around oceanic islands

only fishes in the aquarium observed cleaning Para­ behaviour from the ‘clients’, on the other hand, raises the canthurus hepatus, suggesting that they had the most possibility that these traits were not specialised enough appropriate morphological and/or behavioural traits to for harmless cleaning. For instance, it has been shown that clean among the available species pool. The jolting bite force differs between facultative cleaner and non- 34 Narvaez and Morais: Cleaning behaviour pygmy angelfishes

Fig. 1 Paracanthurus hepatus exhibiting its flanks (A), belly and spreading its pectoral fins (B) to be cleaned simul­taneously by C. bicolor and C. tibicen. (C) Centropyge bicolor and (D) Centropyge tibicen individually cleaning Paracanthurus hepatus.

cleaner species of the wrasse genus Thalassoma. Cleaner cleaning interactions in the past decades (Côté 2000; species in this genus deliver a lower bite force when Vaughan et al. 2017), indicates that pygmy angels rarely compared to non-cleaner species (Baliga and Metha clean. This fact offers support to the hypothesis that 2014). These weaker bites decrease the chance of collateral Centropyge species lack other specialised morphological damage to clients’ tissues and, hence, increase the like­ or behavioural traits that would facilitate the removal of lihood of subsequent interactions. Angelfishes have tiny organisms or dead tissues from ‘clients’ without relatively strong bite forces (grab-and-tearing feeding causing damage (Baliga and Law 2016). Our results sug­ pattern; Konow and Bellwood 2011), which they use to gest that, from a P. hepatus perspective, the benefit of tear apart pieces of their feeding substrate, often sponges, being cleaned out-weighed potential accidental risks of ascidians and, in the case of Centropyge, mainly fila­ tissue damage (i.e. due to a lack of specialised cleaning mentous algae (Randall et al. 1997; Allen et al. 1998). The traits by the pygmy angelfishes). fact that Centropyge species were never previously Other instances of marine fishes acting as cleaners in observed cleaning, despite a large body of research on captivity only have been reported previously (e.g. Heniochus Narvaez and Morais: Cleaning behaviour pygmy angelfishes 35 monoceros and H. acuminatus, Shigeta et al. 2001), and could represent incidental or opportunistic cleaning be­ Compliances haviour. The lumpfish Cyclopterus lumpus Linnaeus, 1758, for example, has never been observed engaging in clean­ Observational work. Ethical permission was not nec­ ing symbioses in the wild. This species shows no obvious essary. traits for cleaning (e.g. body shape and colouration), yet it is often used as a biological control to remove sea lice (Lepeophtheirus salmonis Krøyer, 1837) from farmed References Atlantic salmon (Salmo salar Linnaeus, 1758) in Norway (Imsland et al. 2014). This apparent decoupling between Allen GR, Steene R, Allen M (1998) A guide to angelfishes and the species’ likelihood of engaging in cleaning interactions butterflyfishes. Odyssey Publishing and Tropical Reef in the wild and captivity, could suggest that our obser­ Research, Perth, pp 250 vations only represent incidental cleaning and, just as the Arnal C, Côté IM, Morand S (2001) Why clean and be cleaned? lumpfish case, have essentially been set by the captivity The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behav Ecol Sociobiol 51: 1-7 context. However, communication between cleaners and Arnal C, Morand S (2001) Importance of ectoparasites and clients has been proposed to be the main feature separating mucus in cleaning interactions in the Mediterranean cleaner opportunistic mutualisms from cleaning symbioses, re­ wrasse Symphodus melanocercus. Mar Biol 138: 777-784 gardless of the context (wild or captivity; Vaughan et al. Baliga VB, Mehta RS (2014) Scaling patterns inform ontogenetic 2017). While there is no evidence of any communication transitions away from cleaning in Thalassoma wrasses. J between Atlantic salmon and lumpfish during cleaning Exp Biol 217: 3597-3606 interactions, we observed clear signs of communication Baliga VB, Law CJ (2016) Cleaners among wrasses: phylo­ between pygmy angelfishes and blue tangs (Fig. 1). This genetics and evolutionary patterns of cleaning behavior point clearly positions our observations as a rare- within Labridae. Mol Phylogenet Evol 94: 424-35 occurrence cleaning mutualism and raises the question Brockmann HJ, Hailman JP (1976) Fish cleaning symbiosis: of whether spontaneous willingness to clean (i.e. as de­ notes on juvenile angelfishes (Pomacanthus, Chaeto­ rived from previous records of cleaning) is the only factor dontidae) and comparisons with other species. Zeitschrift - determining propensity to act as a cleaner. In our case, für Tierpsychologie 42: 129 138 pygmy angelfish cleaning may have only occurred be­ Bshary R, Grutter AS (2002) Asymmetric cheating opportunities and partner control in a cleaner fish mutualism. Anim cause these were the only species in that context with Behav 63: 547-555 generalised traits to clean, even if they would usually not. Côté IM, Arnal C, Reynolds JD (1998) Variation in posing On ultra-diverse Indo-Pacific coral reefs, where hundreds behaviour among fish species visiting cleaning stations. J of fish species are concentrated within small areas, such a Fish Biol 53: 256-266 complete lack of more common cleaners may never occur. Côté IM (2000) Evolution and ecology of cleaning symbioses in Thus, this previously unreported behaviour highlights the the sea. Oceanogr Mar Biol 38: 311-355 need to understand what triggers the transition between Côté IM, Soares MC (2011) Gobies as cleaners. In: Patzner RA, potential and realised species interactions. Van Tassell JL, Kovacíc M, Kapoor BG (eds) The Biology of Gobies, Science Publishers, pp 525-555 Cushman JH, Beattie AJ (1991) Mutualisms: assessing the bene­ Acknowledgements fits to hosts and visitors. Trends Ecol Evol 6: 193-195 Feder HM (1966) Cleaning symbiosis in the marine environment. We thank David Vaughan for insightful comments on In: Henry SM (ed) Symbiosis, vol: 1. Academic Press, - the draft of this manuscript. We thank Sally Keith and one New York, pp 327 380 Froese R, Pauly D (2019) FishBase www.fishbase.org. Accessed other anonymous reviewer for their helpful feedback. Feb 2019 36 Narvaez and Morais: Cleaning behaviour pygmy angelfishes

Gasparini JL, Floeter SR (2001) The shore fishes of Trindade Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Island, western south Atlantic. J Nat Hist 35(11): 1639- Barrier Reef and Coral Sea 2nd ed. University of Hawai’i 1656 Press, Honolulu, pp 584 Grutter AS (1996) Parasite removal rates by the cleaner wrasse Randall JE (2005) A review of mimicry in marine fishes. Zool Labroides dimidiatus. Mar Ecol Prog Ser 130: 61-70 Stud 44: 299-328 Grutter AS (2002) Cleaning symbioses from the parasites’ per­ Sazima I, Moura RL, Sazima C (1999) Cleaning activity of spective. Parasitology 124: 65-81 juvenile angelfish, Pomacanthus paru, on the reefs of the Grutter AS, Bshary R (2004) Cleaner fish, Labroides dimidiatus, Abrolhos Archipelago, western South Atlantic. Environ diet preferences for different types of mucus and parasitic Biol Fishes 56: 399-407 gnathiid isopods. Anim Behav 68: 583-588 Sazima C, Sazima I (2001) Plankton-feeding aggregation and Imsland AK, Reynolds P, Eliassen G, Hangstad TA, Foss A, occasional cleaning by adult butterflyfish, Chaetodon striatus Vikingstad E, Elvegård TA (2014) The use of lumpfish (Chaetodontidae), in southwestern Atlantic. Cybium 25: (Cyclopterus lumpus L.) to control sea lice (Lepeophtheirus 145-151 salmonis Krøyer) infestations in intensively farmed At­ Shigeta T, Usuki H, Gushima K (2001) Interaction between lantic salmon (Salmo salar L.). Aquaculture 424: 18-23 cleaner and host: The black porgy cleaning behavior of Konow N, Fitzpatrick R, Barnett A (2006) Adult Emperor angel­ juvenile sharpnose tigerfish, Rhyncopelates oxyrhynchus fish (Pomacanthus imperator) clean Giant sunfishes (Mola in the Seto Inland Sea, Western Japan. Proceedings of the mola) at Nusa Lembongan, Indonesia. Coral Reefs 25: 208 30th U.S. – Japan Meeting on Aquaculture 30: 3-4 Konow N, Bellwood DR (2011) Evolution of high trophic di­ Soares MC, Bshary R, Cardoso SC, Côté IM (2008) The meaning versity based on limited functional disparity in the feeding of jolts by fish clients of cleaning gobies. Ethol 114: 209- apparatus of marine angelfishes (f. Pomacanthidae). PloS 214 ONE 6: e24113 Sun D, Cheney KL, Werminghausen J, Meekan MG, McCormick McCourt RM, Thomson DA (1984) Cleaning behaviour of the MI, Cribb TH, Grutter AS (2015) Presence of cleaner juvenile Panamic sergeant major, Abudefduf troschelii wrasse increases the recruitment of damselfishes to coral (Gill), with a résumé of cleaning associations in the Gulf of reefs. Biol Lett 11: 20150456 California and adjacent waters. Calif Fish Game 70: 234- Thresher RE (1979) Possible mucophagy by juvenile Holacanthus 239 tricolor (Pisces: Pomacanthidae). Copeia 1979: 160-162 Michael SW (1993) Reef sharks and rays of the world. A guide Thresher RE, Brothers EB (1985) Reproductive ecology and to their identification, behaviour, and ecology. Sea Chal­ biogeography of Indo-west Pacific angelfishes (Pisces: lengers, Monterey, pp 107 Pomacanthidae). Evolution 39: 878-887 Morais RA, Brown J, Bedard S, Ferreira CEL, Floeter SR, Vaughan DB, Grutter AS, Costello MJ, Hutson KS (2017) Cleaner Quimbayo JP, Rocha LA, Sazima I (2017) Mob rulers and fishes and shrimp diversity and a re-evaluation of cleaning part-time cleaners: two reef fish associations at the isolated symbioses. Fish Fish 18: 698-716 Ascension Island. J Mar Biol Assoc UK 97: 799-811 Waldie PA, Blomberg SP, Cheney KL, Goldizen AW, Grutter AS Narvaez P, Furtado M, Neto AI, Moniz I, Azevedo JM, Soares (2011) Long-term effects of the cleaner fish Labroides MC (2015) Temperate facultative cleaner wrasses selec­ dimidiatus on coral reef fish communities. PLoS ONE 6: tively remove ectoparasites from their client-fish in the e21201 Azores. Mar Ecol Prog Ser 540: 217-226 Oates J, Manica A, Bshary R, Grutter AS (2012) Relationship Received: 22 June 2020 between roving behaviour and the diet and client com­ Accepted: 24 August 2020 position of the cleaner fish Labroides bicolor. J Fish Biol 81: 210-219 Ⓒ Japanese Coral Reef Society