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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
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
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:
©Koninklijke Brill NV, Leiden, 2018 DOI 10.1163/15685403-00003753
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.
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.
We greatly acknowledge J. Bayogan and G. Gumanao from Davao del Norte
State College, Panabo City, Philippines for logistic support during the fieldwork.
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
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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.
... The 'cleaning rock pool' shrimp, Urocaridella antonbruunii (Bruce, 1967) is an important marine ornamental decapod that is very popular in the global aquarium trade (Calado et al., 2007;Balaji et al., 2009). This species is having a cleaning symbiotic relationship with fishes that remove the ectoparasites, mucus, scales, or diseased tissue (Vaughan et al., 2018;Bos & Fransen, 2018). ...
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The ‘cleaning rock pool’ shrimp commonly inhabit the shallow waters of reef and crevices regions at 0.5-3.0 m depth. Recent exploration conducted off the Gulf of Mannar and Agatti Island yielded the species, Urocaridella antonbruunii (Bruce, 1967) from the bottom curve of the coral boulder at a depth of 0.5-1.0 m. This is the new record for the Gulf of Mannar and Lakshadweep waters. Major distinguishing morphological characters of the congener's were described and illustrated. The molecular analysis confirmed the species occurrence in Indian waters followed the intraspecific and interspecific genetic divergences (16S gene) were estimated between 0.3-2.1% for within species and 6.4-11.2% for between species respectively. Additionally, we updated and provided the illustrative key characters for all members of the genus Urocaridella.
... This includes breaking infection cycles by feeding on parasite eggs, cysts, and cocoons present in the environment (non-infective stage) in the laboratory (Vaughan 2018a, b;Barton et al. 2020), a function so far only known to be performed by cleaner shrimp. The degree of reliance on cleaning interactions is largely unknown for most shrimp species, mainly due to their secretive and often nocturnal habits (Bonaldo et al. 2015;Bos and Fransen 2018;Vaughan et al. 2018a). Besides removing parasites, at least one species of tropical cleaner shrimp, Lysmata amboinensis (de Man, 1888), is also capable of attending to injured clients by feeding on diseased tissue in laboratory conditions (Vaughan et al. 2018c). ...
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For the last seven decades, cleaning sym-biosis in the marine environment has been a research field of intrigue. There is substantial evidence that, by removing undesired items from their client fishes, cleaner organisms have positive ecosystem effects. These include increased fish recruitment, abundance and enhanced fish growth. However, the intimate association and high frequency of interactions between cleaners and clients potentially facilitates pathogen transmission and disease spread. In this review, we identify knowledge gaps and develop novel hypotheses on the interrelationship between parasites, hosts and the environment (disease triangle concept), with a particular emphasis on the potential role of cleaner organisms as hosts and/or transmitters of parasites. Despite evidence supporting the positive effects of cleaner organisms, we propose the cleaners as transmitters hypothesis; that some parasites may benefit from facilitated transmission to cleaners during cleaning interactions, or may use cleaner organisms as transmitters to infect a wider diversity and number of hosts. This cost of cleaning interactions has not been previously accounted for in cleaning theory. We also propose the parasite hotspot hypothesis; that parasite infection pressure may be higher around cleaning stations, thus presenting a conundrum for the infected client with respect to cleaning frequency and duration. The impact of a changing environment, particularly climate stressors on cleaners' performance and clients' cleaning demand are only beginning to be explored. It can be expected that cleaners, hosts/cli-ents, and parasites will be impacted in different ways by anthropogenic changes which may disrupt the long-term stability of cleaning symbiosis.
... Molecular Phylogenetics and Evolution 124 (2018) 71-81 phylogenetic analysis (Fig. 2, clades 1-3). Species of the IWP genus Urocaridella (Clade 1) have been frequently referred to as fish cleaners that are both diurnally or nocturnally active (e.g., Becker and Grutter, 2004;Bonaldo et al., 2015;Bos and Fransen, 2018;Chen and Huang, 2012), and U. antonbruunii has been regarded as a dedicated cleaner (Vaughan et al., 2017). They are somewhat similar in general appearance to shrimps of the genus Ancylomenes (Clade 4), both in their slender-build transparent body and their colour pattern, but are not associated with sea anemones (Fig. 3, Suppl. ...
Several species of palaemonid shrimps are known to act as fish-cleaning symbionts, with cleaning interactions ranging from dedicated (obligate) to facultative. We confirmed five evolutionarily independent origins of fish cleaning symbioses within the family Palaemonidae based on a phylogenetic analysis and the ancestral state reconstruction of 68 species, including 13 fish-cleaners from the genera Ancylomenes, Brachycarpus, Palaemon, Periclimenes, and Urocaridella. We focus in particular on two distantly related lineages of fish cleaning shrimps with allopatric distributions, the Indo-West Pacific Ancylomenes and the western Atlantic monophyletic Ancylomenes/Periclimenes group, which exhibit striking similarities in morphology, colouration and complex behaviour. Specifically, representatives of both lineages are similar in: (1) the general body shape and colour pattern; (2) the utilization of sea anemones as conspicuous cleaning stations; and (3) the use of sideways body swaying to visually promote their bright colour spots in order to attract fish clients. Such morphological, ecological and ethological convergences are apparently due to adaptations to fish cleaning linked to the establishment of similar modes of communication with fish clients in these species.
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Cleaning symbiosis has been documented extensively in the marine environment over the past 50 years. We estimate global cleaner diversity comprises 208 fish species from 106 genera representing 36 families and 51 shrimp species from 11 genera representing 6 families. Cleaning symbiosis as originally defined, is amended to highlight communication between client and cleaner as the catalyst for cooperation, and to separate cleaning symbiosis from incidental cleaning, which is a separate mutualism preceded by no communication. Moreover, we propose the term “dedicated” to replace “obligate” to describe a committed cleaning lifestyle. Marine cleaner fishes have dominated the cleaning symbiosis literature, with comparatively little focus given to shrimp. The engagement of shrimp in cleaning activities has been considered contentious because there is little empirical evidence. Plasticity exists in the use of “cleaner shrimp” in the current literature, with the potential to cause significant confusion. Indeed, this term has been used incorrectly for the shrimp Infraorder Stenopodidea, involving three families, Stenopodidae, Palaemonidae, and Hippolytidae, and to represent all members of Lysmata and Stenopus. Caution is expressed in the use of grey literature and anecdotal observations to generate data on cleaning interactions, due to the presence of species complexes. Interest in cleaning organisms as biological controls in aquaculture is increasing due to their value as an alternative to various chemical ectoparasite controls. Reports of the importance of cleaner organisms in maintaining a healthy reef ecosystem has also been increasing and we review the current biological knowledge on cleaner-organisms, highlighting areas that are understudied.
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The present checklist represents a synthesis of the current state of knowledge of the caridean shrimp fauna of Singapore, based mainly on the abundant material collected in the Straits of Johor and Strait of Singapore during the Comprehensive Marine Biodiversity Survey of Singapore (CMBS) in 2010–2014. Some additional caridean material from Singapore, for instance, material collected and identified by D.S. Johnson in the 1950–1960s, were also included. All reported taxa are listed with selected synonymy, as well as taxonomic, ecological and biogeographical notes; most species are also illustrated in colour, some for the first time. Many taxa, especially in the family Alpheidae, represent taxonomically challenging species complexes that may each take several years to be completely resolved. The material collected during CMBS contains a total of 128 taxa (including well-defined species, tentatively identified species (cf., aff.), and species complexes = species sensu lato) in 53 genera and 12 families. Species previously reported from Singapore but not re-collected by CMBS are included in a table summarising all caridean records from the country, totalling 219 taxa in 63 genera and 14 families; however, some of these records appear to be questionable and require confirmation. A total of 47 caridean species are recorded from Singapore for the first time, the most notable new records being, for the Alpheidae: Alpheus ehlersii De Man, 1909; Automate anacanthopus De Man, 1910; Prionalpheus sulu Banner & Banner, 1971; Salmoneus seticheles Anker, 2003 (previously known only from northern Australia); S. alpheophilus Anker & Marin, 2006; Synalpheus thai Banner & Banner, 1966; Thuylamea camelus Nguyên, 2001 (genus and species previously known only from Vietnam); for the Palaemonidae: Periclimenaeus arabicus (Calman, 1939); P. orontes Bruce, 1986 (previously known only from northern Australia); Pontonides loloata Bruce, 2005; and for the remaining families: Latreutes anoplonyx Kemp, 1914; Leptochela crosnieri Hayashi, 1995 (previously known only from New Caledonia); Lysmata lipkei Okuno & Fiedler, 2010 (previously known only from Japan); Ogyrides orientalis (Stimpson, 1860); Philocheras pilosus (Kemp, 1916) and Thor marguitae Bruce, 1978 (previously known only from eastern Australia). Taxonomic changes are made for Alpheus dispar Randall, 1840 (previously considered a synonym of A. brevirostris (Olivier, 1811)), A. imitatrix De Man, 1909b (previously considered a subspecies of A. pareuchirus Coutière, 1905) and A. monoceros Heller, 1862 which is herein formally considered to be a nomen dubium.
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Cleaner organisms exhibit a remarkable natural behaviour where they consume ectoparasites attached to "client" organisms. While this behaviour can be utilized as a natural method of parasitic disease control (or biocontrol), it is not known whether cleaner organisms can also limit reinfection from parasite eggs and larvae within the environment. Here we show that cleaner shrimp, Lysmata amboinensis, consume eggs and larvae of a harmful monogenean parasite, Neobenedenia sp., in aquaculture. Shrimp consumed parasite eggs under diurnal (63%) and nocturnal (14%) conditions as well as infectious larvae (oncomiracidia) diurnally (26%). Furthermore, we trialled the inclusion of cleaner shrimp for preventative parasite management of ornamental fish, Pseudanthias squamipinnis, and found shrimp reduced oncomiracidia infection success of host fish by half compared to controls (held without shrimp). Fish held without cleaner shrimp exhibited pigmentation changes as a result of infection, possibly indicative of a stress response. These results provide the first empirical evidence that cleaner organisms reduce parasite loads in the environment through non-symbiotic cleaning activities. Our research findings have relevance to aquaculture and the marine ornamental trade, where cleaner shrimp could be applied for prophylaxis and control of ectoparasite infections.
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Cleaning symbiosis encompasses a large diversity of organisms in reef systems, but has been mostly recorded at daytime. We report two instances of nocturnal cleaning by the shrimp Urocaridella sp. in a shipwreck at Tulamben, Bali, Indonesia. These cleaning episodes involved the pufferfish Arothron nigropunctatus and the rabbitfish Siganus studeri as clients. The fishes were resting near the shipwreck while the shrimp inspected them. Different from records of diurnal cleaning, in which clients pose and change colours to attract the cleaner´s attention, it seems unlike that fishes would have intentionally attracted the attention of the cleaner in the present study, as both fishes were resting. Therefore, both events seem to have occurred due to the simple presence of fishes resting next to cleaner shrimps. Therefore, the scarcity of nocturnal cleaning records may be explained by the strict diurnal activity of cleaner fishes, especially wrasses (Labridae) and gobies (Gobiidae). Additionally, visual communication has been shown to be an important component of interactions between cleaner fishes and clients, what seems to restrict these interactions at night. However, as cleaner shrimps are distributed worldwide, and since some species are active at night and not predominately visually oriented, we suggest that this type of nocturnal cleaning occurs globally in the reef habitat.
Reef fish that actively visit cleaner fish to have parasites and dead or infected tissue removed face two potential problems: they might have to wait while cleaners inspect other clients, and cleaners might feed on healthy body tissue, a behaviour that is referred to as cheating. Individuals of some ‘client’ species have large home ranges, which cover several cleaning stations, while others have small territories or home ranges with access to only one cleaning station. The former can thus choose between cleaners, while the latter cannot. We investigated whether clients with large home ranges change cleaning partners to outplay cleaners against each other to achieve (1) priority of access over clients with no choice at cleaning stations and (2) control over cheating by cleaners. We followed individuals of longnosed parrotfish, Hipposcarus harid, for up to 120 min in their natural environment and noted their interactions with cleaner wrasses, Labroides dimidiatus. Individuals were likely to return to the same cleaning station if the previous interaction had ended without conflict but changed cleaners for the next inspection if they had been either cheated or ignored, at least if the time between two consecutive visits was short. The overall attractiveness of a cleaning station seemed to be largely independent of service quality, which appeared to be similar at all stations. This is the first empirical evidence that the option to change partners is used as a control mechanism to stabilize cooperative behaviour.
Cleaning mutualism, in which cleaning organisms remove ectoparasites from cooperating ‘clients’, is widespread among marine animals. Until now, research has focused on fishes as cleaners, whereas cleaner shrimps have received little attention. The aim of this study was to investigate the cleaning behaviour of the cleaner shrimp, Periclimenes longicarpus, and to compare the results directly to data on the sympatric and well-studied cleaner wrasse, Labroides dimidiatus. We first compared the time spent cleaning and client diversity as indicators of the potential importance of the cleaner shrimp to client health and found strong similarities between shrimp and wrasse. We further looked at three correlates of service quality: duration of interactions, tactile stimulation of clients, and jolt rates as correlates of mucus feeding (=cheating). We specifically predicted that shrimps would cheat clients less frequently than the wrasses because they should be more vulnerable to aggressive responses by clients. Although the results partly support our hypothesis, they also suggest that both species strategically adjust cheating rates according to risk, as predatory clients jolted less frequently than nonpredatory clients. In conclusion, the results suggest that the shrimps play an important role in client health but that nonpredatory clients have to control the shrimps' behaviour to receive a good service.
Signals transmit information to receivers about sender attributes, increase the fitness of both parties, and are selected for in cooperative interactions between species to reduce conflict [1, 2]. Marine cleaning interactions are known for stereotyped behaviors [3-6] that likely serve as signals. For example, "dancing" and "tactile dancing" in cleaner fish may serve to advertise cleaning services to client fish [7] and manipulate client behavior [8], respectively. Cleaner shrimp clean fish [9], yet are cryptic in comparison to cleaner fish. Signals, therefore, are likely essential for cleaner shrimp to attract clients. Here, we show that the yellow-beaked cleaner shrimp [10] Urocaridella sp. c [11] uses a stereotypical side-to-side movement, or "rocking dance," while approaching potential client fish in the water column. This dance was followed by a cleaning interaction with the client 100% of the time. Hungry cleaner shrimp, which are more willing to clean than satiated ones [12], spent more time rocking and in closer proximity to clients Cephalopholis cyanostigma than satiated ones, and when given a choice, clients preferred hungry, rocking shrimp. The rocking dance therefore influenced client behavior and, thus, appears to function as a signal to advertise the presence of cleaner shrimp to potential clients.