Do cleaner wrasses rub on reef manta rays to remove ...

aqua, International Journal of Ichthyology

Do cleaner wrasses rub on reef manta rays to remove their own parasites? João Paulo Krajewski1, Roberta M. Bonaldo1 and Ivan Sazima1, 2, 3

1) Grupo de História Natural de Vertebrados, Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13083-862 Campinas, SP, Brazil. 2) Museu de Zoologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13083-863 Campinas, SP, Brazil. 3) Corresponding author. E-mail: [email protected] Received: 06 February 2017 – Accepted: 03 April 2017

Keywords Chafing behaviour, cleaner fish, Labridae, Mobulidae, coral reefs, Micronesia

Abstract Cleaner wrasses of the genus Labroides are the epitome of a cleaner fish. Herein we describe two cleaner wrasse species, Labroides bicolor and Labroides dimidiatus, displaying a behaviour known as chafing or flashing. When chafing, a fish rubs itself against sandy bottoms, rocks, vessels, or other rough surfaces including sea turtles and sharks. We recorded the two cleaner wrasse species rubbing themselves against the rough skin of reef manta rays, Manta alfredi, on a coral reef cleaning station at Yap, Micronesia, western Pacific. As chafing is a way to relieve skin irritation and an alternative to reduce external parasites, we suggest that these specialised wrasse species use this behaviour to remove their own ectoparasites when other cleaning services are unavailable. The recorded ray-wrasse cleaning association is noteworthy, since the rays provide food and cleaning opportunity to the wrasses at the same time.

Zusammenfassung Die Putzer-Lippfische der Gattung Labroides sind der Inbegriff eines Putzerfisches. Hier beschreiben wir zwei Putzer-Lippfisch-Arten, Labroides bicolor und Labroides dimidiatus, die ein Verhalten zeigen, das als „Scheuern“ bezeichnet werden kann (engl. chafing oder flashing). Beim Scheuern reibt sich ein Fisch an sandigem Grund, Felsen, Gefäßen oder anderen rauhen Oberflächen, ja sogar an Meeresschildkröten und Haien. Wir beobachteten die beiden Putzer-Lippfisch-Arten beim Scheuern an der rauhen Haut eines Riffmanta-Rochens, Manta alfredi, in einer Korallenriff-Putzstation bei Yap, Mikronesien, Westpazifik. Weil das Scheuern eine Methode ist, sich bei Hautstörungen Erleichterung zu schaffen, und eine Alternative, um externe Parasiten zu reduzieren, haben wir die 47

Vorstellung entwickelt, dass diese spezialisierten LippfischArten das Verhalten einsetzen, um die eigenen Ektoparasiten zu entfernen, wenn andere Putzdienste nicht zur Verfügung stehen. Die beobachtete Rochen-Lippfisch-Putzgemeinschaft ist insofern bemerkenswert, als die Rochen sowohl Nahrung als auch Putzmöglichkeit zugleich bieten.

Resumo Os labros-limpadores do gênero Labroides são o exemplo típico de peixe limpador. Descrevemos aqui duas espécies de labros-limpadores, Labroides bicolor e Labroides dimidiatus, exibindo um comportamento conhecido como roçar ou lampejar. Ao roçar, um peixe se esfrega contra fundos arenosos, rochas, embarcações, ou outras superfícies ásperas, incluindo tartarugas marinhas e tubarões. Registramos as duas espécies de labros-limpadores se esfregando contra a pele áspera de jamantas-do-recife, Manta alfredi, em uma estação de limpeza em recife coralíneo em Yap, Micronésia, Oceano Pacífico ocidental. Como roçar é um modo de aliviar irritação da pele e uma alternativa para reduzir parasitas externos, sugerimos que estes dois labros especializados exibem esse comportamento para remover seus próprios ectoparasitos quando outros serviços de limpeza não estão disponíveis. Portanto, a associação de limpeza raia-labro aqui registrada é notável, já que as jamantas-do-recife oferecem, ao mesmo tempo, alimento e oportunidade de limpeza aos labros.

Résumé Les labres nettoyeurs du genre Labroides sont la quintessence du poisson nettoyeur. Ici nous décrivons deux espèces de labres nettoyeurs, Labroides bicolor et Labroides dimidiatus qui montrent un comportement connu sous le nom de frottement. Lors du frottement, un poisson se glisse contre un substrat de sable, des roches, des bateaux ou d’autres surfaces rugueuses, y compris des tortues de mer ou des requins. Nous avons observé les deux espèces aqua vol. 23 no. 2 - 28 April 2017

Do cleaner wrasses rub on reef manta rays to remove their own parasites?

de labres se frottant contre la peau rugueuse des raies mantas des récifs, Manta alfredi, sur un site de nettoyage à Yap, Micronésie, Pacifique occidental. En effet, le frottement est un moyen de soulager l’irritation de la peau et une solution alternative pour contrôler les parasites externes quand d’autres moyens font défaut. L’association de nettoyage raie-labre mentionnée est remarquable dans la mesure où les raies offrent simultanément de la nourriture et une occasion de nettoyage aux labres.

Sommario I labridi del genere Labroides rappresentano il modello di pesce pulitore. Qui descriviamo il comportamento di due specie di labridi pulitori, Labroides bicolor e Labroides dimidiatus, noto come sfregamento o lampeggio. Quando esegue sfregamenti, un pesce si strofina contro fondali sabbiosi, rocce, vasi o altre superfici ruvide, tra cui anche tartarughe marine e squali. Abbiamo registrato le due specie sfregarsi contro la pelle ruvida della manta Manta alfredi in una stazione di pulizia lungo la barriera corallina a Yap, Micronesia, Pacifico occidentale. Poiché lo sfregamento è un modo per alleviare l'irritazione della pelle e un sistema per ridurre i parassiti esterni, suggeriamo che queste specie utilizzino questo comportamento per rimuovere i propri ectoparassiti quando altri servizi di pulizia non sono disponibili. L'associazione di pulitura registrata tra una razza e un labride è notevole, poiché le razze forniscono cibo e allo stesso tempo un’opportunità di ripulirsi dei parassiti.

INTRODUCTION The cleaner wrasses of the genus Labroides Bleeker, 1851, are the most specialised and the best studied fishes involved in cleaning symbiosis. Cleaning comprises a fish, the cleaner, which removes external parasites – and sometimes diseased tissue and mucus – from another fish, the client. Various definitions and descriptions of cleaning symbiosis may be found in Potts (1973), Losey (1987), Losey et al. (1999), Côté (2000), Grutter (2005) and Vaughan et al. (2016) to mention only a few. From the cleaning perspective, the bluestreak wrasse Labroides dimidiatus (Valenciennes 1839) is the best studied among the five species of Labroides, and much of what is currently known about cleaning symbiosis derives from studies on this species (e.g., the extensive literature by Alexandra S. Grutter and co-authors). However, cleaning of a Labroides cleaner wrasse by other cleaner fish is infrequently mentioned in the copious literature about the species within this genus (Randall 1958; Cheney & Eckes 2008; Grutter 2010; Clague et al. 2011). However, in his unpublished PhD thesis, Robertson (1974) mention that L. dimidiatus and L. bicolor Fowler & Bean, 1928 of all ages pose and clean conspecifics and congeners. Among other aqua vol. 23 no. 2 - 28 April 2017

parasite infection sources, cleaner wrasses are infected when feeding on parasitic worms encysted in the skin of their clients (Grutter 2010). Herein we touch briefly on cleaning of reef manta rays Manta alfredi (Kreft, 1868) by the bluestreak cleaner wrasse Labroides dimidiatus and the bicolor cleaner wrasse Labroides bicolor, and describe for both wrasses a behaviour known as chafing or flashing (Gooding & Magnuson 1967; Robertson 1974; DeLoach 1999). Besides the description and illustration of this behaviour, we speculate on the significance of chafing against the reef manta rays by these two specialized cleaners. MATERIALS AND METHODS We observed and recorded the two cleaner wrasse species and the mantas at a prominent coral formation, formed mostly by Porites cyllindrica Dana, 1846 about 20 m long and 12 m wide, which served as cleaning station at Yap, Micronesia (9°35’57.30”N; 138°08’26.41”). The depth at the reef was 2-6 m, and the water visibility was about 8 m. All our dives were with scuba in the morning (between 08:00 and 11:00 h). We photographed and video-recorded the slow passes of the mantas over the reef, the wrasses cleaning the mantas and, on occasions, chafing against the mantas’ skin. Throughout the observation sessions we used “ad libitum”, “all occurrences”, and “sequence” samplings (Altmann 1974). Ten observation sessions lasted 100 and one lasted 120 min, in a total of about 18 h of observations. The identification of the cleaner wrasses followed Randall (1958) and Robertson (1974), and that of the manta ray followed Marshall et al. (2009) and Kashiwagi et al. (2011). We estimated the sizes of the wrasses and the mantas against objects of known size: total length (TL) for the wrasses, and disc width (DW) for the mantas. RESULTS During the dives, we observed up to about 15 reef manta rays Manta alfredi passing slowly over the reef (Fig. 1) or hovering briefly there. In both situations, the mantas were jointly cleaned by the bicolor cleaner wrasse Labroides bicolor and the bluestreak cleaner wrasse L. dimidiatus. The size (TL) of the cleaner wrasses was about 5-10 cm and the reef mantas had about 3-4 m DW. The cleaners inspected almost the whole body of the mantas, and entered the gill slits and the mouth in search of external parasites (Fig. 1). The cleaner wrasses dis48

João Paulo Krajewski, Roberta M. Bonaldo and Ivan Sazima

played the typical behavioural repertoire while cleaned the mantas, including the pelvic-ride (cf. Losey Jr. 1978), in which the pelvic fins of the cleaner touched the client. Besides cleaning behaviour, in each of our 11 dives we recorded L. bicolor and L. dimidiatus chafing against the skin of the mantas. We were unable to count the number of chafing displayed by one given individual, but recorded about 10 chafing episodes in each 100 min dive. When chafing, a wrasse rubbed parts of its body against several body parts of the mantas. For instance, a L. bicolor individual chafed with undulatory movements, rubbing the head and ventral surface of its anterior body part against the lateral side of the manta’s tail base (Figs 2a-b). The same individual engaged in a second chafing bout afterwards, again rubbing its head against the manta (Fig. 2c). On the other hand, a L. dimidiatus individual also chafed with undulatory movements, but initiated the bout rubbing the belly, flank and posterior body part against the manta’s head, and ended the bout touching the manta with its tail (Figs 3a-c). Thus, various body parts of a given wrasse were rubbed against the mantas’ skin, presumably the ones that itched or were otherwise irritating. The chafing was alternated with cleaning: the wrasse cleaned a

manta for a while, chafed once or twice, and then resumed cleaning to chafe again later. Each chafing lasted about 1 sec. DISCUSSION Although we spent several hours underwater observing the activity of Labroides bicolor and L. dimidiatus on the reef, we recorded the wrasses cleaning the manta rays and other reef fishes (but not conspecifics or congeners), and chafing only against the mantas. Individuals of the two wrasse species often cleaned the same manta but did not interact with conspecifics or each other. When they are near one another, these two species rarely interact or display territoriality at Society Islands, Tuamotus, and Marquesas in Polynesia (Randall 1958), although L. dimidiatus is territorial, forms harems and interacts aggressively both with conspecifics and with L. bicolor at Heron Island, Australia (Robertson 1974). On three occasions at Tuamotus, Labroides dimidiatus was recorded pecking briefly at L. bicolor (Randall 1958), which may be an instance of fleeting cleaning service on a congener. An instance of intraspecific and interspecific cleaning is exemplified by a L. dimidiatus individual that cleaned several individuals of its mimic Aspidontus taeniatus and also cleaned conspecifics in

Fig. 1. A reef manta ray, Manta alfredi, passes slowly above a cleaning station held by two cleaner wrasse species, Labroides bicolor and L. dimidiatus. Note a L. bicolor individual (foreground) partly hidden by the first right gill slit of the ray. Photo by J. P. Krajewski. 49

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Fig. 2a-c. Chafing by the cleaner wrasse Labroides bicolor a. the wrasse approaches its head towards the manta skin between the tail and the fin; b. the fish undulates and rubs its head and anterior portion of the body against the manta skin; c. the wrasse ends a rubbing bout, and initiates another, its head touching the manta. Video screen shots by J. P. Krajewski. aqua vol. 23 no. 2 - 28 April 2017

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Sulawesi, Indonesia (Cheney & Eckes 2008; see also Robertson 1974 on this cleaner servicing its mimic). One adult L. dimidiatus individual was recorded cleaning other adult at Lizard Island, Australia (Clague et al. 2011), which seems to be an

infrequent behaviour. However, juveniles of both L. bicolor and L. dimidiatus are known to clean conspecific and congener adults at Heron Island, Australia (Robertson 1974). In the case of L. dimidiatus, intraspecific cleaning is limited to

Fig. 3a-c. Chafing bout by the cleaner wrasse Labroides dimidiatus a. the wrasse begins to rub, touching its belly against the manta skin near the head; b. the fish rubs its flank; c. the wrasse ends the rubbing bout, its tail touching the manta. Video screen shots by J. P. Krajewski. 51



members of the same social group (Robertson 1974), and the same may apply to L. bicolor. These two characteristics (age and social group) may explain the lack of intraspecific and interspecific cleaning interactions during our observations of both wrasse species cleaning the reef manta rays at Yap, as the cleaner wrasse individuals were all adults (Randall 1958; Robertson 1974). Both L. bicolor and L. dimidiatus cheat on their clients, in the form of taking mucus and skin from their clients (Poulin & Vickery 1995; Mills & Côté 2010; Vaughan et al. 2016), and this trait may also be related to the two Labroides species we observed not cleaning conspecifics and congeners, as they could cheat one on another. Additionally, cheating by L. dimidiatus may vary between areas (Poulin & Vickery 1995). If our speculations above hold true, cleaner wrasses of the genus Labroides may resort to chafing to remove their own external parasites when cleaning services by conspecifics, congeners or other fishes and shrimps are unavailable, as recorded here for Labroides bicolor and L. dimidiatus. Chafing or flashing is a way to relieve skin irritation and an alternative to cleaning used by most fish, including L. dimidiatus, to get rid of ectoparasites (Gooding & Magnuson 1967; Wicklund 1969; Losey Jr. 1987; Robertson 1974; De Loach 1999; Papamastiou et al. 2007; Grossman et al. 2009). Rubbing against the rough skin of sharks and rays is recorded for several fish species (e.g., EiblEibesfeldt 1955; Robertson 1974; Wicklund 1979; Papamastiou et al. 2007; present paper), and we view this behaviour as equivalent to rubbing against other substrate types (Grossman et al. 2009). However, this behaviour can hardly be compared to cleaning symbiosis as proposed by Papamastiou et al. (2007), who ascribe a cleaner role to two shark species against which two carangid species rubbed themselves. In this latter example, there are no evidences of any of the elaborate behaviours displayed by a cleaner fish and its clients (Potts 1963; Côté 2000; Grutter 2005; Vaughan et al. 2016). Merely, when chafing, the fish that rubs itself against a moving shark, ray, or sea turtle should adjust its swimming speed and rubbing according to the moving animal it uses for rubbing (Eibl-Eibesfeldt 1955; Wicklund 1979; Grossman et al. 2009). An alternative (or complementary) explanation for chafing would be delivering tactile stimulus for the client (Losey & Margules 1971; Losey 1978). However, given the relative size of the cleaner aqua vol. 23 no. 2 - 28 April 2017

wrasse and the manta client, this explanation seems less plausible than that of alleviating skin irritation and removing parasites. In conclusion, we suggest herein that the chafing on the reef manta rays we recorded for Labroides bicolor and L. phthirophagus may be viewed as an alternative mode to remove external parasites from the body of these highly specialised and obligate cleaners when other cleaning services are unavailable. If our suggestion holds true, the recorded manta-wrasse cleaning association is noteworthy since the rays provide, at the same time, both food and cleaning opportunity to the wrasses servicing them. ACKNOWLEDGEMENTS We are grateful to Patricia and Bill Acker, from Manta Ray Bay Resort, and José Truda Palazzo Jr. for the logistical support in Yap. We thank two anonymous reviewers, whose criticism improved the paper considerably. We also thank the CNPq and FAPESP for past grants that allowed us to study cleaning symbiosis in the southwestern Atlantic. REFERENCES ALTMANN, J. 1974. Observational study of behaviour: sampling methods. Behaviour 49 (3): 227-267. CHENEY, K. L. & ECKES, M. J. 2008. Cleaners clean cleaner mimics. Coral Reefs 27 (3): 527. CLAGUE, G. E., NEWPORT, C. & GRUTTER, A. S. 2011. Intraspecific cleaning behaviour of adult cleaner wrasse, Labroides dimidiatus (Perciformes: Labridae). Marine Biodiversity Records 4e56: 1-3. CÔTÉ, I. M. 2000. Evolution and ecology of cleaning symbioses in the sea. In: Oceanography and marine biology: An Annual review. (Eds. R. N. Gibson & M. Barnes) 38: 311-356. Taylor and Francis, New York. EIBL-EIBESFELDT, I. 1955. Über Symbiosen, Parasitismus un andere besondere zwischenartliche Beziehungen tropischer Meeresfische. Zeitschrift für Tierpsychologie 12 (2): 203-219. DELOACH, N. 1999. Reef fish behavior: Florida, Caribbean, Bahamas. New World Publications, Jacksonville, 359 pp. GOODING, R. M. & MAGNUSON, J. J. 1967. Ecological significance of a drifting object to pelagic fishes. Pacific Science 21 (4): 486-497. GROSSMAN, A., SAZIMA, C. & SAZIMA, I. 2009. Rub and move: barracudas (Sphyraena barracuda) use swimming turtles as scraping surfaces in the south-western Atlantic. Marine Biodiversity Records 2(e106): 1-3. GRUTTER, A. S. 2005. Cleaning mutualism in the sea. In: Marine parasitology. (Ed. K. Rohde): 264-278. CABI Publishing, Wellington. GRUTTER, A. S. 2010. Cleaner fish. Current Biology 20 (13): R547-R549 52


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