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 E­mail: [email protected] Communicated by Frederic Sinniger (Associate Editor­in­Chief) 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 en vironment. This novel cleaning ob­ or facultative cleaners (Vaughan et al. 2017). servation raises ques tions 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 video­recorded 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 re­circulation 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 Indo­Pacific: 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) Indo­Pacific: East Africa to the Samoan Centropyge and Phoenix Islands, north to southern Facultative Aquarium Our study bicolor Japan, south to New Caledonia;