Cleaner Fishes and Shrimp Diversity and a Re‐Evaluation of Cleaning Symbioses

Cleaner Fishes and Shrimp Diversity and a Re‐Evaluation of Cleaning Symbioses

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-

View Full Text

Details

  • File Type
    pdf
  • Upload Time
    -
  • Content Languages
    English
  • Upload User
    Anonymous/Not logged-in
  • File Pages
    19 Page
  • File Size
    -

Download

Channel Download Status
Express Download Enable

Copyright

We respect the copyrights and intellectual property rights of all users. All uploaded documents are either original works of the uploader or authorized works of the rightful owners.

  • Not to be reproduced or distributed without explicit permission.
  • Not used for commercial purposes outside of approved use cases.
  • Not used to infringe on the rights of the original creators.
  • If you believe any content infringes your copyright, please contact us immediately.

Support

For help with questions, suggestions, or problems, please contact us