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Nocturnal cleaning of sleeping rabbitfish Siganus canaliculatus by the cleaner shrimp Urocaridella antonbruunii (Decapoda, Palaemonidae)

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This article firstly reports nocturnal cleaning symbiosis in an Indo-Pacific coral reef performed by the cleaner shrimp Urocaridella antonbruunii . Furthermore, this observation stands out, because it is the first observation of sleeping fish being cleaned.
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Crustaceana 91 (2) 239-241
NOTES AND NEWS
NOCTURNAL CLEANING OF SLEEPING RABBITFISH,
SIGANUS CANALICULATUS, BY THE CLEANER SHRIMP,
UROCARIDELLA ANTONBRUUNII (DECAPODA, PALAEMONIDAE)
BY
ARTHUR R. BOS1,2)and CHARLES H. J. M. FRANSEN2,3)
1)Department of Biology, The American University in Cairo, P.O. Box 74,
New Cairo 11835, Egypt
2)Taxonomy and Systematics Group, Naturalis Biodiversity Center, P.O. Box 9517,
2300 RA Leiden, The Netherlands
Many coral reef fish regularly visit cleaning stations to have ectoparasites
removed by cleaner fish or shrimps (Cote, 2000; Bshary & Schäffer, 2002;
Chapuis & Bshary, 2009; Vaughan et al., 2016). Cleaners often attract potential
clients by using visual cues, such as dance behaviour (Becker et al., 2005),
signalling the location of the cleaning station while leading the client away from
competing cleaners. Visual signals however, only work during the day suggesting
that cleaning stations are closed at night. Militz and Hutson (2015) firstly observed
diminished nocturnal cleaning by the shrimp Lysmata amboinensis (De Man, 1888)
under laboratory conditions, and only one observation has been reported from a
coral reef (Bonaldo et al., 2015).
An individual of the cleaner shrimp Urocaridella antonbruunii (Bruce, 1967)
(cf. Anker & De Grave, 2016, fig. 108) was observed carefully approaching a
sleeping rabbitfish Siganus canaliculatus (Park, 1797) during a night dive in the
Davao Gulf, Philippines, on 2 October 2010 (fig. 1A). Once the shrimp ascended
upon the siganid, it started cleaning the siganid’s skin and continued doing so
for about 10 min (fig. 1B). The cleaner shrimp Urocaridella antonbruunii may
be specialized in nocturnal cleaning of fish avoiding competition with diurnal
cleaners.
Clients of cleaning stations are commonly predators or relatively large individ-
uals of non-predatory families (Cote, 2000). Juveniles or small-sized fish rarely
visit cleaning stations and, until today, only two siganids were observed at clean-
ing stations: Siganus rivulatus Forsskål & Niebuhr, 1775 (cf. Poulin, 1993) and
3)Corresponding author; e-mail: charles.fransen@naturalis.nl
©Koninklijke Brill NV, Leiden, 2018 DOI 10.1163/15685403-00003753
240 NOTES AND NEWS
Fig. 1. Urocaridella antonbruunii (Bruce, 1967) cleaning a sleeping rabbitfish, Siganus canaliculatus
(Park, 1797), in the Davao Gulf, Philippines, 2 October 2010. A, carefully approaching the siganid;
B, cleaning.
NOTES AND NEWS 241
S. corallinus (Valenciennes, 1835) (cf. Bonaldo et al., 2015). This report consti-
tutes the first record of a sleeping individual of S. canaliculatus being cleaned. If
the siganid intentionally chose its sleeping location for receiving cleaning service
is unknown and needs further investigation.
ACKNOWLEDGEMENTS
We greatly acknowledge J. Bayogan and G. Gumanao from Davao del Norte
State College, Panabo City, Philippines for logistic support during the fieldwork.
REFERENCES
ANKER,A.&S.DEGRAVE, 2016. An updated and annotated checklist of marine and brackish
caridean shrimps of Singapore (Crustacea, Decapoda). Raffles Bulletin of Zoology, (Suppl.)
34: 343-454.
BECKER,J.H.A.,L.M.CURTIS &A.S.GRUTTER, 2005. Cleaner shrimp use a rocking dance to
advertise cleaning service to clients. Current Biology, 15: 760-764.
BONALDO,R.M.,A.S.GRUTTER,I.SAZIMA &J.P.KRAJEWSKI, 2015. 24/7 service: nocturnal
cleaning in a tropical Indo-Pacific reef. Marine Biodiversity, 45: 611-612.
BSHARY,R.&D.SCHÄFFER, 2002. Choosy reef fish select cleaner fish that provide high-quality
service. Animal Behaviour, 63: 557-564.
CHAPUIS,L.&R.BSHARY, 2009. Strategic adjustment of service quality to client identity in the
cleaner shrimp Periclimenes longicarpus. Animal Behaviour, 78: 455-459.
COTE, I. M., 2000. Evolution and ecology of cleaning symbioses in the sea. Oceanography and
Marine Biology, 38: 311-355.
MILITZ,T.A.&K.S.HUTSON, 2015. Beyond symbiosis: cleaner shrimp clean up in culture. PLoS
ONE, 10: e0117723.
POULIN, R., 1993. A cleaner perspective on cleaning symbiosis. Reviews in Fish Biology and
Fisheries, 3: 75-79.
VAUGHAN,D.B.,A.S.GRUTTER,M.J.COSTELLO &K.S.HUTSON, 2016. Cleaner fishes and
shrimp diversity and a re-evaluation of cleaning symbioses. Fish Fish., DOI:10.1111/faf.12198
First received 29 August 2017.
Final version accepted 23 October 2017.
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