Received:10June2016 | Accepted:15November2016 DOI: 10.1111/faf.12198 ORIGINAL ARTICLE Cleaner fishes and shrimp diversity and a re- evaluation of cleaning symbioses David Brendan Vaughan1 | Alexandra Sara Grutter2 | Mark John Costello3 | Kate Suzanne Hutson1 1CentreforSustainableTropicalFisheries andAquaculture,CollegeofScienceand Abstract EngineeringSciences,JamesCookUniversity, Cleaningsymbiosishasbeendocumentedextensivelyinthemarineenvironmentover Townsville,Queensland,Australia the past 50years. We estimate global cleaner diversity comprises 208 fish species 2SchoolofBiologicalSciences,theUniversity ofQueensland,StLucia,Queensland,Australia from106generarepresenting36familiesand51shrimpspeciesfrom11generarep- 3InstituteofMarineScience,Universityof resentingsixfamilies.Cleaningsymbiosisasoriginallydefinedisamendedtohighlight Auckland,Auckland,NewZealand communication between client and cleaner as the catalyst for cooperation and to Correspondence separatecleaningsymbiosisfromincidentalcleaning,whichisaseparatemutualism DavidBrendanVaughan,Centrefor precededbynocommunication.Moreover,weproposetheterm‘dedicated’tore- SustainableTropicalFisheriesand Aquaculture,CollegeofScienceand place‘obligate’todescribeacommittedcleaninglifestyle.Marinecleanerfisheshave Engineering,JamesCookUniversity, dominatedthecleaningsymbiosisliterature,withcomparativelylittlefocusgivento Townsville,Queensland,Australia. Email:[email protected] shrimp.Theengagementofshrimpincleaningactivitieshasbeenconsideredconten- tiousbecausethereislittleempiricalevidence.Plasticityexistsintheuseof‘cleaner shrimp’ in the current literature, with the potential to cause significant confusion. Indeed,thistermhasbeenusedincorrectlyfortheshrimpInfraorderStenopodidea, involvingthreefamilies,Stenopodidae,PalaemonidaeandHippolytidae,andtorepre- sentallmembersofLysmata and Stenopus.Cautionisexpressedintheuseofgreylit- eratureandanecdotalobservationstogeneratedataoncleaninginteractions,dueto thepresenceofspeciescomplexes.Interestincleaningorganismsasbiologicalcon- trolsinaquacultureisincreasingduetotheirvalueasanalternativetovariouschemi- calectoparasitecontrols.Reportsoftheimportanceofcleanerorganismsinmaintaining ahealthyreefecosystemhasalsobeenincreasingandwereviewthecurrentbiological knowledgeoncleanerorganisms,highlightingareasthatareunderstudied. KEYWORDS cleanerfishes,cleanershrimp,cleaningsymbiosis,Lysmata,Stenopus 1 | INTRODUCTION thoseinteractionsinwhichbothsymbiontslivetogetherinprolonged intimatecontact,orwherethesesymbiontsarephysiologicallyinte- Symbiosis is the living together of two or more different taxa and grated(Bauer,2004;Bronstein,2015).Assuch,thetemporarymutu- includesmutualism,parasitismandcommensalism(Martin&Schwab, alismrepresentingcleaningsymbiosisisconsideredbytheseauthors 2013; Figure1). However, many symbiotic relationships are sub- asnon-symbiotic.However,DeBary(1879)discussedlesspermanent tle, and the variables that influence them can often be overlooked symbiotic interactions(Peacock 2011; reviewby Martin&Schwab, (Egerton, 2015; Feder, 1966), or have been incorrectly interpreted. 2013).Peacock(2011)labelledthenotionof‘intimatecontact’asim- The term symbiosis is considered by some authors to include only preciseandtoorestrictivebecauseitishighlyscaledependent.He Fish and Fisheries 2016; 1–19 wileyonlinelibrary.com/journal/faf © 2016 John Wiley & Sons Ltd | 1 2 | VAUGHAN ET AL . FIGURE 1 Symbiosisisthecollective termforcommensal,mutualandparasitic associationsbetweenorganisms.Cleaning symbiosisandincidentalcleaningare consideredmutualisticassociationsunder symbiosis addedthattherearecasualinteractionsbetweensymbionts.Theterm with the hummingbird genus Throchilus, Trochilidae) and a Nile ‘cleaningsymbiosis’hasthusbecomewidelyusedintheliteraturewith crocodile(Crocodylus niloticus,Crocodylidae)whichallowedthebird over1,000hitsinGoogleScholar.Weagreethatcleaningsymbiosis accesstoitsmouthtoremoveleeches(Herodotos).Althoughclean- reflectsalegitimatesymbiosisandfollowtheviewofPeacock(2011). ing symbioses are reported from terrestrial ecosystems (e.g., Hart, Cleaning symbiosiswas defined by Feder (1966) as the removal Hart, &Mooring,1990;Mooring &Mundy, 1996;Sazima, Jordano, ofectoparasites,bacteria,diseasedandinjuredtissue,andunwanted Guimarães,DosReis,&Sazima,2012),theyappeartobemorecom- foodparticlesbycleanerorganismsfromcooperativehostorganisms. monanddiverseinaquaticenvironments,particularlyintropicalma- Feder(1966)addedthatthemutuallybeneficialbehaviouralsopro- rineenvironments(Grutter,2002;Limbaugh,1961;Poulin&Grutter, videsasourceoffoodforthecleaner.Losey(1972)added‘andsubse- 1996).Thegreaternumberofobservationsintropicalaquaticvs.tem- quentingestion’toemphasizethisnutritionalbenefitforthecleaner. perateaquaticenvironmentsmayreflectgreatervisibilityunderwater, However,theoriginaldefinitionisinneedofamendmentbecauseit higherspeciesrichness,aswellasbiogeographicandhabitatdistribu- excludescommunicationasthecatalystforcooperationinthesein- tionsofclientandcleanerspecies.Themajorityofpublishedreports teractions and does not clearly highlight the shared reason for this on cleaning symbioses from aquatic environments deal with fishes cooperation;itpresentsapositiveeffectonthesurvivalofbothclient ascleaners(seesupplementaryinformation).Marinecrustaceansas and cleaner. cleaningorganismshavereceivedfarlessattentionhistorically,partly Theuseofimpreciseterminologyinthebiologicalsciencesiscom- due to their often cryptic crevice-living nature. There are currently mon(Wilkins,2005).Thefrequentmisuseormisinterpretationofterms noreportsofcleaninginteractionsinvolvingfreshwatercrustaceans. suchas‘cleaningsymbiosis’or‘cleanershrimp’overthelast20years However,cleanershrimpmayhaveequallyimportantecologicalroles has created significant ambiguity in the literature.The construction tocleanerfishes(Becker&Grutter,2004). oftermsofintimacytoattempttofurtherqualifythedegreeofthe Cleaner organisms are considered in the majority of the litera- cleaningrelationshiphascreatedfurtherambiguity.Forexample,the tureaseitherobligateorfacultative.Youngbluth(1968)distinguished term‘obligate’denotesastrictnecessityinitsmode,outsideofwhich between obligate cleaners, those which rely almost exclusively on survivaliscompromised.Inthecleaningsymbiosisliterature,theterm cleaning, and facultative cleaners which do not.This was based on ‘obligate’isusedforalackofatermtodescribeasemipermanentor Limbaugh’s(1961)useof‘full-time’cleanersandreflectedtheirdiet full-timecleanerorganism.Yet,cleanerscanliveindependently,and and habits. Nevertheless, there is no empirical evidence that any thus,nocleanersareobligate. cleaneristrulyobligateinthestrictsense,asthiswouldimplythat Thisreviewprovidesthefirsttaxonomicallyupdatedglobalesti- these cleaning organisms would be compelled to derive all of their mateofcleanerfishesandshrimpdiversity.Furthermore,weaddress nutritionfromtheirclientsduringsuchsymbioticinteractions,with- inconsistenciesandambiguityintherelevantliterature,torefinethe outwhichtheywouldperish.Thedefinitionof‘obligate’inacleaning definitionofacleaningsymbiosisandtoexploretheattributesthat symbiosisisequivocalandthistermshouldonlybereservedforcer- definecleanerorganisms.Thisisthefirstreviewtoseparateincidental tain modes of parasitic or other symbioseswhere it holds true.We cleaningfromcleaningsymbiosis.WeexpandonthereviewofCôté proposeheretheuseoftheterm‘dedicated’toreplace‘obligate’when (2000) to include freshwater species and those fishes and shrimp describingthosecleanersthatexhibitacommittedmodeofcleaning newlyidentifiedascleaners. lifestylethroughouttheirnon-larvalontogeny,anddifferentiatethese fromtheothervaryinglevelsoffacultativecleaners,thosewhichare opportunistic,temporarycleanersorinteractascleanersonlyinpart 2 | CLEANING SYMBIOSIS of their ontogeny.The consideration of Limbaugh (1961), that ded- icated cleaners are more highly evolved than those that exhibit an The first possible recorded observation of a cleaning symbiosis opportunisticmodeofcleaning,isdifficulttoevaluate,andmaynot between two different species was made by the Greek historian necessarily be correct. Limbaugh (1961) considered that dedicated HerodotosinthefifthcenturyBC.Herodotosobservedthecleaning cleaners evolved from forms that were more free-living and exhib- interactionbetweenabirdhecalled‘thetrochilus’(nottobeconfused ited opportunistic cleaning, while Gorlick, Atkins, and Losey (1978) VAUGHAN ET AL . | 3 consideredthatatleastmembersofonegenusofdedicatedcleaner & Gushima, 2001; Sazima & Moura, 2000; Sazima & Sazima, 2000; fishes, Labroides (Labridae), may have evolved from an ectoparasitic Becker,Curtis,&Grutter,2005;Shepherd,Teale,&Muirhead,2005; form.However,Baeza(2009)concludedthat,atleastforsomeshrimp, Craig, 2007; Bertoncini et al., 2009; Horton, 2011; Abe, Sekiguchi, the ancestral lifestyle was likely to have been equally symbiotic or Onishi, Muramatsu, & Kamito, 2012; Huebner & Chadwick, 2012a; free-living.Asimplerexplanationmaybethatanimalsthatevolvedto Karplus,2014).Dedicatedcleanersandfacultativecleanersactively browseonepifaunawouldalsobrowseontheskinoflargeranimals, asserttheirintentionstocleanoftenbyusingconspicuousdances,or be they mammals, turtles or large fishes. Cleaner fishes and shrimp throughtactilestimulation.Clientsoftenposesubmissivelytosignala obtaintheirfoodfromcleaningandfromthewiderenvironment.The desiretobecleaned.Communicationtocooperateisclearlythecata- relativeimportanceofeachsourceislikelytovaryinspaceandtime, lystforcleaninginteractionsthatnotonlytranscendsspeciesbound-