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First report of cleaning activity of Lepadogaster candolii (Gobiesocidae) in the Mediterranean Sea

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Boris Weitzmann at Parc Natural Montgri, Medes, Baix Ter
Boris Weitzmann
  • Parc Natural Montgri, Medes, Baix Ter
Lluís Mercader
Lluís Mercader
Lluís Mercader
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First report of cleaning activity of Lepadogaster candolii
(Gobiesocidae) in the Mediterranean Sea
by
Boris WEITZMANN (1) & Lluís MERCADER* (2)
Cybium 2012, 36(3): 487-488.
(1) Centre d’Estudis Avançats de Blanes (CSIC), Carrer d’Accés a la Cala Sant Francesc 14, 17300 Blanes, Catalunya, Spain.
[boris@ceab.csic.es]
(2) Carrer Pedró 79 (2n), 17230 Palamós, Catalunya, Spain.
* Corresponding author [peixos@lluismercader.cat]
RÉSUMÉ. - Premier signalement de l’activité de nettoyage de
Lepadogaster candolii (Gobiesocidae) en Méditerranée.
L’activité de nettoyage de Lepadogaster candolii Risso, 1810
a été observée pour la première fois en août 2009, au cours d’une
plongée réalisée dans la Réserve Marine des Îles Medes (Médi-
terranée nord-occidentale). L’individu nettoyait la cavité buccale
d’un grand mérou Epinephelus marginatus (Lowe, 1834), qui res-
tait bouche ouverte et immobile à quelque distance du substrat. Ce
signalement apporte une information nouvelle quant au comporte-
ment alimentaire de cette espèce, considerée classiquement comme
cryptobenthique.
Key words. - Gobiesocidae - Lepadogaster candolii - MED - Medes
Islands - Cleaning behaviour - First record.
Cleaning behaviour is a specialized relationship between a
cleaner and host, in which the host benefits from ectoparasite
removal (Arnal et al., 2001), and the cleaner gets readily available
prey from a living substrate (Zander and Sötje, 2002). The host
benets from long-term repeated parasite removal (Trivers, 1971),
with the behaviour of the host determining the success of the clean-
er (Zander and Sötje, 2002).
The primary cleaner sh in the Mediterranean Sea is the labrid
Symphodus (Crenilabrus) melanocercus. Other species act as sup-
plementary cleaners including juveniles of several wrasses: Sym-
phodus (Crenilabrus) mediterraneus, Symphodus (Crenilabrus)
ocellatus, Symphodus (Crenilabrus) tinca, Thalassoma pavo, Coris
julis and Ctenolabrus rupestris (Zander and Sötje, 2002). Many of
these clean only occasionally (Van Tassell et al., 1994).
Clingsh (Gobiesocidae) are associated with the cryptobenthic
group (Patzner, 1999a). Due to their small size and cryptic life, lit-
tle is known about their behaviour and ecology (Gonçalves et al.,
1998; Patzner, 1999a). Usually, they live under rocks and crevices,
feeding on small invertebrates. There are seven species described
in the Mediterranean Sea (Hofrichter and Patzner, 2000), several of
which can only be identied from collected specimens.
Lepadogaster candolii differs markedly both in ecology and
behaviour from the remaining species of Lepadogaster. It is much
more mobile than others species of clingsh and is found in many
different habitats. L. candolii regularly inhabits boulder elds, but
also resides in small cavities, overhangs and caves (Hofrichter and
Patzner, 2000). In addition, the juveniles or subadults are found
co-habiting with sea urchins, generally when the echinoderm cov-
ers a small hole, crevice or near seagrass meadows, beneath flat
and overgrown stones in the rhizome zone of Posidonia oceanica
(Patzner, 1999a, 1999b; Hofrichter and Patzner, 2000). It swims
frequently in the water column and forages openly at consider-
able distance from shelter (Gonçalves et al., 1998; Hofrichter and
Patzner, 2000).
In Australia two clingfish species of the genus Cochleoceps
have been described to act as cleaners (Van Tassell et al., 1994). Up
to now, only one species (Diplecogaster bimaculata) has been doc-
umented, in the Mediterranean, as a cleaner and it was on a moray
eel (Muraena helena) (Patzner and Debelius, 1984) but, according
to Van Tassell et al. (1994), Lepadogaster candolii is not a cleaner
sh.
We document the feeding behaviour of L. candolii and show
that it is a cleaner in the Mediterranean Sea.
MATERIAL AND METHODS
While SCUBA-diving, August 2009 at Medes Islands Marine
Reserve (Fig. 1), a large dusky grouper Epinephelus marginatus
was observed in a cave (2 m x 2 m) at 16 meters depth. It was sta-
tionary, 50 cm off the ground and kept its mouth wide open. Upon
closer investigation, a small clingsh (Lepadogaster candolii) was
observed gliding in and out of the grouper’s mouth (Figs 2, 3).
Figure 1. - Map of the Medes Islands Marine Reserve (NW Mediterranean)
showing the area where the cleaning activity was observed.
Cleaning activity of Lepadogaster candolii (Mediterranean Sea) We i t z m a n n & mercader
488 Cybium 2012, 36(3)
RESULTS
Both, grouper and clingsh, exhibited a typical
cleaning behaviour, with the host holding its mouth
open, remaining motionless and allowing the cling-
fish to glide in and out of its mouth. The clingfish
was at an unusually far distance from the ground,
although this is the most active and free swimming of
all mediterranean clingsh species.
DISCUSSION
Epinephelus marginatus and Lepadogaster can-
dolii are both a very common species in western
Mediterranean and in eastern Atlantic from British
Isles to the Canary Islands.
According to Mazé (2007), there are differ-
ences in the diet of Lepadogaster lepadogaster and
L. candolii. Lepadogaster lepadogaster is strictly
benthophagous showing a specialization in amphi-
pods and gastropods while L. candolii has a more
diversified diet. Gut contents of this last species
reveals remains of tube feet and echinoderm pedicel-
laria. The frequency of Gnathiidae juveniles (ectopar-
asitic isopods on fishes) in their stomach contents,
embedded in mucus, and sh scales would indicate
that Lepadogaster candolii is propably a non-special-
ised cleaner (Mazé, 2007).
In conclusion, this paper documents L. candolii
as a cleaner in the Mediterranean Sea. Additional observations are
required to determine the extent of this activity within the Mediter-
ranean.
Acknowledgements. - We are grateful to Dr. Robert A. Patzner from the
Universität Salzburg, Dr. Antoni Garcia-Rubies from Centre d’Estudis
Avançats de Blanes and the referees for their valuable help and improve-
ment of the text.
REFERENCES
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cleaned? The importance of client ectoparasites and mucus in a
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GONÇALVES D.M., GONÇALVES E.J., ALMADA V.C. &
ALMEIDA S.P., 1998. - Comparative behaviour of two species
of Lepadogaster (Pisces: Gobiesocidae) living at different
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HOFRICHTER R. & PATZNER R.A., 2000. - Habitat and Micro-
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PATZNER R.A., 1999b. - Sea urchins as a hiding-place for juvenile
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Helgol. Mar. Res., 55: 232-241.
Reçu le 21 juillet 2011.
Accepté pour publication le 20 septembre 2011.
Figure 2. - Epinephelus marginatus observed in the Medes Islands holding its mouth wide
open while a Lepadogaster candolii swims out of it.

Supplementary resource (1)

cleaning activity of Lepadogaster candolii
Data
February 2013
Boris Weitzmann · Lluís Mercader
... Unfortunately, the blenny immediately got off the host as soon as one of the observers (one of the authors, MC) approached to take a photograph. During the analysis of photographs, we also recorded two new cases of the recently published association between Epinephelus marginatus (Lowe, 1834) and L. candolii from Medes (Spain) (Weitzmann and Mercader, 2012) and a first case of association (recorded twice) between Conger conger (Linnaeus, 1758) and P. rouxi from Capo Noli (Tyrrhenian Sea, Italy) (Fig. 2C). In other cases, P. rouxi was observed in proximity or inside the burrow shared by the two species, C. conger and M. helena (Fig. 1A and Supplementary Material). ...
... In our opinion, both species, L. candolii and P. rouxi, act as opportunistic cleaners on M. helena and we speculate that the association is therefore not casual, as similar cases are reported in the literature. In particular, Weitzmann and Mercader (2012) reported for the first time the cleaning activity of L. candolii on E. marginatus in the Mediterranean Sea. Patzner and Debelius (1984) reported of a Mediterranean clingfish (Diplecogaster bimaculata bimaculata) acting as a cleaner on M. helena. ...
... Patzner and Debelius (1984) reported of a Mediterranean clingfish (Diplecogaster bimaculata bimaculata) acting as a cleaner on M. helena. Furthermore, we have recorded the cleaning association between L. candolii and E. marginatus in the same location (Medes) as Weitzmann and Mercader (2012), at a depth of 18 m ( Fig. 1C and D). Finally, the cleaning activity of an Atlantic clingfish (Gobiesocidae), Diplecogaster tonstricula (Fricke et al., 2015), on the moray eel Gymnothorax afer Bloch, 1795 was recently reported for the first time in the Atlantic Ocean (Fricke et al., 2015). ...
From scuba diving to social networks: A curious association between two small fish species, Lepadogaster candolii Risso, 1810 and Parablennius rouxi (Cocco, 1833), and Muraena helena (Linnaeus, 1758) coming from citizen science
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In this work, we report for the first time the associationbetween two cryptobenthic fish, Lepadogaster candolii and Parablennius rouxi, and the Mediterranean moray, Muraena helena. The nature of these associations and the importance of citizen science and social network in marine biology are discussed. Other associations with two relatively large fishes (Conger conger and Epinephelus marginatus) emerged during the study.
View
... An increasing number of studies in temperate regions have led to the recognition of additional cleaner species (Zander & Sötje 2002, Weitzmann & Mercader 2012, such as the northeastern Atlantic Symphodus melops (Potts 1973) and Centrolabrus exoletus (Henriques & Almada 1997) and the Mediterranean Centrolabrus (Symphodus) melanocercus (Baliga & Law 2016) (see Almada et al. 2002, Hanel et al. 2002. To a lesser extent, Coris julis, Thalassoma pavo (Labridae) (Van Tassell et al. 1994) and Lepadogaster candolii (Gobiesocidae) (Weitzmann & Mercader 2012) have also been reported as cleaner species in the temperate northeastern Atlantic and Mediterranean. ...
... An increasing number of studies in temperate regions have led to the recognition of additional cleaner species (Zander & Sötje 2002, Weitzmann & Mercader 2012, such as the northeastern Atlantic Symphodus melops (Potts 1973) and Centrolabrus exoletus (Henriques & Almada 1997) and the Mediterranean Centrolabrus (Symphodus) melanocercus (Baliga & Law 2016) (see Almada et al. 2002, Hanel et al. 2002. To a lesser extent, Coris julis, Thalassoma pavo (Labridae) (Van Tassell et al. 1994) and Lepadogaster candolii (Gobiesocidae) (Weitzmann & Mercader 2012) have also been reported as cleaner species in the temperate northeastern Atlantic and Mediterranean. For this reason, many species are currently being used as cleaners in fish farms, which has been particularly evident in the salmon aquaculture industry (Robalo & Mirimin 2018). ...
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The diversity and abundance of cleaner species have been frequently associated with ectoparasite load and ecological wealth of tropical fish communities. Cleaning behaviour in temperate regions has received less attention, with few labrid species being described as cleaners. The context and frequency of cleaning behaviour by juvenile white seabream Diplodus sargus are described. Surface observations from pontoons in yachting marinas were carried out based on a method used in a recent first report of cleaning behaviour by this northeastern Atlantic and Mediterranean sparid. A total of 51 h of observations revealed that these juveniles (<10 cm total length [TL]) display similar or higher cleaning rates (13.1 cleaning events per hour) compared to other temperate cleaners. The high cleaning rates, high abundance of young D. sargus on rocky shores along their distribution area and preferential targeting of adults by coastal fisheries highlight the ecological importance of D. sargus. The most common client species include grey mullets (Mugilidae), which represent 93.5% of total cleaning events registered. Regarding TL, clients were 4.6 to 6.6 times larger than cleaners. Environmental factors such as water temperature (14.0-24.0°C), wave exposure (6.0-17.0 s) and wind speed (2.0-8.0 m s-1) influence white seabream cleaning rates. Thus, a combination of factors may affect the health of temperate client fish communities. On a different perspective, these results also highlight the potential of juvenile D. sargus in integrated multitrophic aquaculture. In conclusion, white seabream cleaning behaviour plays an important role in temperate fish communities and its relevance in different habitats should be further assessed.
View
... lepadogaster and L. purpurea) were obtained in a moderately supported sister-group relationship with Gouania and not as close relatives of L. candolii. Due to the nonmonophyly of Lepadogaster, Almada et al. (2008) recommended reclassifying L. candolii to the genus Mirbelia, but this nomenclatural act has not been widely adopted (e.g., Weitzmann and Mercader, 2012;Wagner et al., 2017;Fricke et al., 2020). Almada et al. (2008) recovered Opeatogenys as the sister taxon to the clade containing Gouania, L. lepadogaster, and L. purpurea, Diplecogaster as the sister taxon to a clade containing the aforementioned taxa plus L. candolii and Aspasma ubauo, and Apletodon as the sister taxon to all aforementioned taxa (Fig. 2C). ...
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Gobiesocidae are a moderate-sized family (currently 182 species, 51 genera) of predominantly coastal marine fishes, commonly referred to as clingfishes. Depending on the classification adopted, the species and genera of clingfishes are organized either across ten subfamilies, based on a classification scheme introduced in the 1950s (“traditional” classification, comprising Aspasminae, Cheilobranchinae, Chorisochisminae, Diademichthyinae, Diplocrepinae, Gobiesocinae, Haplocylicinae, Lepadogastrinae, Protogobiesocinae, and Trachelochisminae), or just two subfamilies, in a classification scheme adopted only recently (“reduced” classification, comprising Cheilobranchinae and Gobiesocinae). We investigated the phylogenetic relationships among members of the family Gobiesocidae using both mitochondrial and nuclear DNA sequence data to assess whether the alternative classification schemes (traditional and reduced) are compatible with inferred evolutionary relationships. Phylogenetic hypotheses are derived from maximum-likelihood and Bayesian analyses of a seven-gene concatenated dataset (2 mitochondrial and 5 nuclear markers; 4,857 bp) compiled from individuals representing 82 (of 182) species, 42 (of 51) genera, and 10 (of 10) subfamilies of the Gobiesocidae. Although our investigation provides strong support for the monophyly of the Gobiesocidae, multiple subfamilies of the traditional classification (Aspasminae, Diademichthyinae, Diplocrepinae, Gobiesocinae, and Trachelochisminae), one subfamily of the reduced classification (Gobiesocinae), and multiple genera (Aspasmichthys, Cochleoceps, Lepadogaster, and Lepadichthys) are resolved as non-monophyletic groups. Based on our results and the results of previous studies, we recommend a systematic reassignment of genera between subfamilies, of which we recognize nine: Cheilobranchinae, Chorisochisminae, Diademichthyinae, Diplocrepinae, Haplocylicinae, Gobiesocinae, Lepadogastrinae, Protogobiesocinae, and Trachelochisminae. Membership of the Lepadogastrinae is unchanged from previous usage; the Cheilobranchinae are expanded to contain additional genera from southern Australia, including those placed previously in the Aspasminae (Nettorhamphos and Posidonichthys) and the Diplocrepinae (Barryichthys, Cochleoceps, and Parvicrepis); the Aspasminae are placed in the synonymy of the Diademichthyinae and all genera placed in the former (excluding Modicus and Posidonichthys) are transferred to the latter; the Diplocrepinae are restricted to Diplocrepis; Eckloniaichthys scylliorhiniceps is transferred from the Gobiesocinae to the Chorisochisminae; Gobiesocinae are restricted to the New World members of this group (Acyrtops, Acyrtus, Arcos, Derilissus, Gobiesox, Rimicola, Sicyases, and Tomicodon); the Haplocylicinae are expanded to include additional genera from New Zealand (Gastrocyathus, Gastrocymba, and Gastroscyphus); the Protogobiesocinae are expanded to accommodate three genera of deep water taxa (Gymnoscyphus, Kopua, and Protogobiesox); and the Trachelochisminae are restricted to Dellichthys and Trachelochismus. Four genera (Aspasmogaster, Conidens, Creocele, and Modicus) of uncertain placement are not assigned to any subfamily herein and are considered incertae sedis within the Gobiesocidae.
View
... Likewise, a few CRFs provide behaviours such as cleaning services (e.g. the goby genus Elacatinus, the clingfish Lepadogaster candollei, some pipefish species). While cleaning behaviour may have primarily evolved to serve as a foraging strategy, there is evidence to support its role in reducing predation pressure (Côté & Soares, 2011;Weitzmann, 2012): potential predators benefit from parasite removal by the goby, and consequently, relatively low predation rates are reported (Benkwitt, 2015;Tuttle, 2017). Taking this strategy one step further, some species of blenny (e.g. ...
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... Other studies on parasites of dusky grouper have called attention to symbiotic relationships with other fishes. For instance, dusky groupers may have a symbiotic relationship with a clingfish (Lepadogaster candolii), which removes parasites from the grouper's mouth (Weitzmann and Mercader 2012). In aquaculture settings, the symbiotic barber goby Elacatinus figaro, remove the parasite Neobenedenia melleni from dusky grouper individuals (Souza et al. 2014). ...
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... Hutchins (1991) described Cochleoceps bicolor from southern and south-western Australia, and C. orientalis from south-eastern Australia, as setting up cleaning stations to remove parasites of other teleosts. Weitzmann and Mercader (2012) reported an observation of Lepadogaster candolii in the north-western Mediterranean Sea which was cleaning a grouper, Epinephelus marginatus. ...
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... Other studies on parasites of dusky grouper have called attention to symbiotic relationships with other fishes. For instance, dusky groupers may have a symbiotic relationship with a clingfish (Lepadogaster candolii), which removes parasites from the grouper's mouth (Weitzmann and Mercader 2012). In aquaculture settings, the symbiotic barber goby Elacatinus figaro, remove the parasite Neobenedenia melleni from dusky grouper individuals (Souza et al. 2014). ...
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A better understanding of population dynamics including the identification of reproductive areas and their contribution to the maintenance of fish stocks is essential for population conservation. Dusky grouper, Epinephelus marginatus, is a broadly distributed fish species, usually found in marine rocky bottoms. It is currently listed as “endangered” by the IUCN Red List. The available information on its population in southern Brazil suggests that the neritic habitat of Carpinteiro Bank - CB is the main growth and spawning ground in the region. We investigated if the dusky groupers caught in the rocky-jetties of Rio Grande city (a littoral artificial habitat with no spawning activity) originated from the CB. We sampled 28 individuals from the littoral rocky-jetties aged between 2 and 12 years, and 44 individuals from the neritic CB aged between 2 and 40 years. Individuals from both areas had their otolith sections analyzed with LA-ICPMS (core-to-edge profiles) for 86Sr:43Ca, 138Ba:43Ca ratios. The otolith core (natal origin) and edge (time shortly before capture) from individuals of the same age class showed no difference between the two sites. Individual profiles of 138Ba:43Ca ratios of fish from the littoral zone indicated, for the first time, that some juveniles of dusky grouper enter the Patos lagoon and remain within the estuarine environment between the first and second years of life. This interpretation of otolith chemical data is supported by the marked differences in salinity between the littoral and estuarine sites in these studies areas, and by the marked differences in otolith 138Ba:43Ca of other fish species analyzed along the salinity gradient in the Patos Lagoon estuary. The identification of differential juvenile habitat use patterns is crucial for the establishment and implementation of management and conservation strategies to safeguard this endangered species.
View
... Other studies on parasites of dusky grouper have called attention to symbiotic relationships with other fishes. For instance, dusky groupers may have a symbiotic relationship with a clingfish (Lepadogaster candolii), which removes parasites from the grouper's mouth (Weitzmann and Mercader 2012). In aquaculture settings, the symbiotic barber goby Elacatinus figaro, remove the parasite Neobenedenia melleni from dusky grouper individuals (Souza et al. 2014). ...
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  • Nov 2015
The dusky grouper Epinephelus marginatus has a broad global distribution and is currently listed as an endangered species at the IUCN Red List. This species has large commercial and ecological importance, but only at the last decade the first studies were carried out on its bioecology at its southernmost distribution limit in Southwestern Atlantic. This region is largely formed by sand bottoms, where the occurrence of reefs and rocks are scarce. Rocky bottoms occur in the neritic region (along 20 to 30 m isobaths) and in the jetties in the littoral region, and in both areas the dusky grouper occur frequently. Our studies showed that immature individuals (mean: 4 yrs) of dusky groupers inhabiting rocky jetties in the littoral region represents an important economical incoming for artisanal fishermen, whereas adults (mean: 8 yrs) are mostly caught at offshore banks 15-25 m deep by coastal fisheries. Microscopic analyses of gonads of littoral and neritic individuals suggest that the littoral region is a growing nursery area and the neritic is a reproductive site. Feeding ecology studies based on stomach content and stable isotopes showed that the species has an important role as top predators in both regions. Future studies on the residence time of immature individuals in the littoral using telemetry are fundamental to further understand the ecology of this endangered species in the Southwestern Atlantic and to help its fishing management and conservation.
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... In the Mediterranean Sea, the fist record of L. candolii was a 50.4 mm male specimen captured off Bari, Italy, during an Adriatic deepsea expedition in 1894 (Ahnelt and Elvira, 1991). Although L. candolii is occasionally captured throughout the littoral zone along the Mediterranean, actual documentation from Bari, Italy (Ahnelt and Elvira, 1991); Lampedusa Island, Italy (Mazzoldi and De Girolamo, 1997); Ibiza Island, Spain (Patzner, 1999); Cyprus, Banyuls, Genova, Messina and the upper parts of Adriatic (Hofrichter and Patzner, 2000); Velebit Channel, Croatia (Novosel et al., 2002); Koper Bay, Gulf of Trieste, Slovenia (Turk et al., 2002); Central Black Sea, Turkey (Bat et al., 2005); Syrian coast (Saad, 2005); Gulf of Gabes, Tunisia (Bradai et al., 2007); Livorno, Italy (Piazzi et al., 2009); Ischia Island, Italy (Zupo and St€ ubing, 2010); Medes Island, Spain (Weitzmann and Mercader, 2012) and off Kastamonu, western Black Sea, Turkey (Dalgıc ß and Ceylan, 2012), indicates that L. candolii is more common in the central and western parts of the Mediterranean. ...
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Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses
Article
Full-text available
  • Dec 2016
  • FISH FISH
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 Evolution of Reciprocal Altruism
Article
Full-text available
  • Mar 1971
  • Q REV BIOL
A model is presented to account for the natural selection of what is termed reciprocally altruistic behavior. The model shows how selection can operate against the cheater (non-reciprocator) in the system. Three instances of altruistic behavior are discussed, the evolution of which the model can explain: (1) behavior involved in cleaning symbioses; (2) warning cries in birds; and (3) human reciprocal altruism. Regarding human reciprocal altruism, it is shown that the details of the psychological system that regulates this altruism can be explained by the model. Specifically, friendship, dislike, moralistic aggression, gratitude, sympathy, trust, suspicion, trustworthiness, aspects of guilt, and some forms of dishonesty and hypocrisy can be explained as important adaptations to regulate the altruistic system. Each individual human is seen as possessing altruistic and cheating tendencies, the expression of which is sensitive to developmental variables that were selected to set the tendencies at a balance ap...
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Why clean and be cleaned? The importance of ectoparasites and mucus in a marine cleaning symbiosis
Article
Full-text available
  • Dec 2001
The preferences exhibited by cleaner fishes for particular client species and the high variability in rates at which various clients visit cleaning stations have remained largely unexplained. In this study, we assessed the relative importance of client ectoparasite load and mucus characteristics for the behaviour of cleaning gobies, Elacatinus spp, and their fish clients on a Barbadian fringing reef. Client species with high ectoparasite loads visited cleaning stations more often than less parasitised species. This effect was independent of body size. Frequency of visits to cleaning stations was not related to client mucus characteristics. These results suggest that the main motivation for clients to interact with cleaners is ectoparasite removal. Cleaners did not preferentially clean clients with higher ectoparasite load or better mucus, nor did they spend more time inspecting such clients. The interests of cleaners and clients therefore appear to be inconsistent. This may be due to the generally low rate of ectoparasitism on Barbadian fish compared to fish of other regions. Cleaning gobies fed at a lower rate on client species with higher loads of gnathiid isopod larvae, which may be explained if cleaners switch from eating ectoparasites to other items, such as mucus, on clients with few ectoparasites. Our estimates of caloric and protein content of fish mucus suggest that it may be as valuable a food source per unit weight as ectoparasites. However, no data are available to compare the value of each item per unit feeding time. The fact that clients with few ectoparasites still visit cleaners, albeit at a low rate, suggests that the cost of mucus removal may be low, compared to the benefit of incidental parasite removal. Thus, the outcome of cleaning interactions may remain positive, even in areas characterised by naturally low parasitism on clients.
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Habitat Utilization and Depth Distribution of Small Cryptobenthic Fishes (Blenniidae, Gobiesocidae, Gobiidae, Tripterygiidae) in Ibiza (Western Mediterranean Sea)
Article
Full-text available
  • Jul 1999
The paper describes the habitat utilization of small cryptobenthic fishes of the families Blenniidae (Lipophrys nigriceps, and Parablennius zvonimiri), Gobiesocidae (Apletodon incognitus, Gouania wildenowi, Lepadogaster candollei, and L. lepadogaster), Gobiidae (Chromogobius zebratus, Corcyrogobius liechtensteini, Didogobius splechtnai, Gammogobius steinitzi, Millerigobius macrocephalus, Thorogobius ephippiatus, T. macrolepis, and Zebrus zebrus), and Tripterygiidae (Tripterygion melanurus). Nine different habitats from the waterline to a depth of about 40m were examined. The depth distributions of the single species and co-occurrences with other cryptobenthic fish species are given.
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Sea urchins as a hiding-place for juvenile benthic teleosts (Gobiidae and Gobiesocidae) in the Mediterranean Sea
Article
  • Mar 1999
  • CYBIUM
Associations between juveniles of two species of clingfish (Apletodon incognitus and Lepadogaster candollei) and gobies (Gobius bucchichi, Millerigobius macrocephalus and Zebrus zebrus) and two species of sea urchins (Arbacia lixula and Paracentrotus lividus) are described in the western Mediterranean Sea. The fish hide below the sea urchins between the spines.
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Habitat and Microhabitat of Mediterranean Clingfishes (Teleostei: Gobiesociformes: Gobiesocidae)
Article
  • Dec 2001
  • MAR ECOL-EVOL PERSP
This study addresses the habitat and microhabitat of the seven species of gobiesocid fish in the Mediterranean Sea. It is shown that Lepadogaster lepadogaster is closely adapted to large pebbles and boulder fields of rounded stones with a smooth surface. L. candollei is more euryecious and, in addition to inhabiting boulder fields also, occurs close to seagrass meadows, in small cavities and in association with sea urchins. Diplecogaster bimaculata is also euryecious and extends to greater depths. It lives on sand and muddy bottoms as well as on coralline grounds. At some locations this species is found in high abundance during the spawning season under empty bivalve shells or flat stones. Apletodon dentatus is the rarest species of Gobiesocidae in the Mediterranean Sea. It has a close association with seagrass or large brown algae (Cystoseira). Juveniles of A. incognitus are either associated with sea urchins or inhabit Posidonia meadows. Adults prefer the vicinity of seagrass meadows under empty bivalve shells and stones overgrown with red algae. Gouania wildenowi is stenoecious and is restricted to the interstices of roundish coarse gravel near the waterline. Opeatogenys gracilis is also stenoecious and lives only on the leaves of Posidonia and Cymodocea seagrass. The colourations of the different species and their variations are described and discussed.
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Comparative behaviour of two species of Lepadogaster (Pisces: Gobiesocidae) living at different depths
Article
The two clingfish species studied occupied similar habitats but occurred at different depths. When compared with the subtidal species Lepadogaster candollei, the intertidal species Lepadogaster l. purpurea was less active, spent more time in shelters, visited fewer shelters, showed more site fidelity, and spent less time swimming. Feeding, swimming, and agonistic behaviours were performed mainly in close contact with the substrate in this species. It is hypothesized that these contrasts in behaviour may have evolved under different levels of turbulence.
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Seasonal and geographical differences in cleaner fish activity in the Mediterranean Sea
Article
  • Feb 2002
Investigations into symbioses may be important in order to analyse the grade of stability in ecosystems. Host–cleaner relationships were investigated in two localities of the Mediterranean Sea: Giglio (Tuscany, Italy) and Banyuls-sur-Mer (France). The cleaner wrasse, Symphodus melanocercus, was the main cleaner. Supplementary cleaners, such as the young of several wrasses, Symphodus mediterraneus, Symphodus ocellatus, Symphodus tinca, Coris julis and Ctenolabrus rupestris, are able to help out in times when there is a shortage of cleaners. Differences between the localities were obvious by a greater fish (host) density in Banyuls, which is probably due to eutrophication and might improve and increase cleaner activities. Regarding two seasons, spring and late summer, the fishes presented a lower degree of activity in Giglio, but a higher one in Banyuls – in late summer compared with spring. The main hosts were Chromis chromis, Symphodus tinca and Coris julis; additionally Diplodus sargus in Banyuls and Apogon imberbis in Giglio. Chromis chromis may be a key host species because of its distribution in large groups in the whole Mediterranean; Coris julis is of similar abundance. Symphodus melanocercus additionally came into contact with Symphodus tinca in order to partake of the food of the peacock wrasse. During cleaning activities, Diplodus sargus and other sparids present hesitant behaviour, where the cleaner probably picks more than parasites (skin, scales?) from the body surface. Apogon imberbis (which prefers dark habitats such as caves) totally rejects the main cleaner but was cleaned exclusively by Coris julis which, unlike Symphodus melanocercus, is regularly present near cave entrances. The investigations may present models of the evolutionary processes on specialised partnerships in ecosystems.
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