https://ebookmass.com/product/scallops-biology-ecologyaquaculture-and-fisheries-3rd-edition-sandra-e-shumway-and-
Instant digital products (PDF, ePub, MOBI) ready for you
Download now and discover formats that fit your needs...
The Diversity of Fishes: Biology, Evolution and Ecology, 3rd Edition Douglas E. Facey
https://ebookmass.com/product/the-diversity-of-fishes-biologyevolution-and-ecology-3rd-edition-douglas-e-facey/
ebookmass.com
Myxomycetes: biology, systematics, biogeography, and ecology Elsevier.
https://ebookmass.com/product/myxomycetes-biology-systematicsbiogeography-and-ecology-elsevier/
ebookmass.com
Neuropsychology: Science and Practice 3rd Edition Sandra Koffler (Editor)
https://ebookmass.com/product/neuropsychology-science-andpractice-3rd-edition-sandra-koffler-editor/
ebookmass.com
Binding 13 Chloe Walsh
https://ebookmass.com/product/binding-13-chloe-walsh/
ebookmass.com
Pirate's Ruin (Master and Command Her Book 3) Marie Hall
https://ebookmass.com/product/pirates-ruin-master-and-command-herbook-3-marie-hall-2/
ebookmass.com
A topical approach to life-span development 9th Edition
John W. Santrock
https://ebookmass.com/product/a-topical-approach-to-life-spandevelopment-9th-edition-john-w-santrock/
ebookmass.com
Fixing Broken Cities 2nd Edition John Kromer
https://ebookmass.com/product/fixing-broken-cities-2nd-edition-johnkromer/
ebookmass.com
Redemption (The Worthings Book 3) Noelle Adams
https://ebookmass.com/product/redemption-the-worthings-book-3-noelleadams/
ebookmass.com
500 AP Chemistry Questions to Know by Test Day (5 Steps to a 5), 4th Edition Mina Lebitz
https://ebookmass.com/product/500-ap-chemistry-questions-to-know-bytest-day-5-steps-to-a-5-4th-edition-mina-lebitz/
ebookmass.com
Philemon Iko-Ojo Omede
https://ebookmass.com/product/nigerian-consumer-credit-law-regulationand-market-insights-philemon-iko-ojo-omede/
ebookmass.com
SCALLOPS:BIOLOGY,ECOLOGY, AQUACULTURE,ANDFISHERIES THIRDEDITION DEVELOPMENTSINAQUACULTUREANDFISHERIESSCIENCE
Thefollowingvolumesarestillavailable:
22.FRONTIERSOFSHRIMPRESEARCH
EditedbyP.F.DeLoach,W.J.DoughertyandM.A.Davidson1991xv+412pages
24.MODERNMETHODSOFAQUACULTUREINJAPAN
EditedbyH.IkenoueandT.Kafuku1992xvi+274pages
26.PROTOZOANPARASITESOFFISHES
EditedbyJ.LomandI.Dykova´ 1992xii+316pages
28.FRESHWATERFISHCULTUREINCHINA:PRINCIPLESANDPRACTICE
EditedbyJ.MathiasandS.Li1994xvi+446pages
29.PRINCIPLESOFSALMONIDCULTURE
EditedbyW.PennellandB.A.Barton1996xxx+1040pages
30.STRIPEDBASSANDOTHERMORONECULTURE
EditedbyR.M.Harrell1997xx+366pages
31.BIOLOGYOFTHEHARDCLAM
EditedbyJ.N.KraeuterandM.Castagna2001xix+751pages
32.EDIBLESEAURCHINS:BIOLOGYANDECOLOGY
EditedbyJ.M.Lawrence2001xv+419pages
33.GLOBALSEAGRASSRESEARCHMETHODS
EditedbyF.T.ShortandR.G.Coles2001viii+482pages
34.BIOLOGYANDCULTUREOFCHANNELCATFISH
EditedbyC.S.TuckerandJ.A.Hargreaves2004x+676pages
36.THEKNOWLEDGEBASEFORFISHERIESMANAGEMENT
EditedbyL.MotosandD.Wilson2006xxi+476pages
38.SEAURCHINS
EditedbyJ.M.Lawrence2013xviii+532pages
39.THESEACUCUMBERAPOSTICHOPUSJAPONICUS
EditedbyH.Yang,J.F.Hamel,andA.Mercier2015xxiv+454pages
SCALLOPS Biology,Ecology,Aquaculture, andFisheries THIRDEDITION Editedby SANDRA E.SHUMWAY
DepartmentofMarineSciences,UniversityofConnecticut, Groton,Connecticut,USA
G.JAY PARSONS
FisheriesandOceansCanada,Aquaculture,Biotechnology andAquaticAnimalHealthScienceBranch,Ottawa,Ontario,Canada
Elsevier
Radarweg29,POBox211,1000AEAmsterdam,Netherlands TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UK
50HampshireStreet,5thFloor,Cambridge,MA02139,USA
Copyright r 2016,2006,1991ElsevierB.V.Allrightsreserved.
Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans,electronicormechanical, includingphotocopying,recording,oranyinformationstorageandretrievalsystem,withoutpermissioninwriting fromthepublisher.Detailsonhowtoseekpermission,furtherinformationaboutthePublisher’spermissionspolicies andourarrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyrightLicensing Agency,canbefoundatourwebsite: www.elsevier.com/permissions.
ThisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightbythePublisher (otherthanasmaybenotedherein).
Notices
Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchandexperiencebroadenour understanding,changesinresearchmethods,professionalpractices,ormedicaltreatmentmaybecomenecessary.
Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgeinevaluatingandusing anyinformation,methods,compounds,orexperimentsdescribedherein.Inusingsuchinformationormethods theyshouldbemindfuloftheirownsafetyandthesafetyofothers,includingpartiesforwhomtheyhavea professionalresponsibility.
Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors,assumeanyliability foranyinjuryand/ordamagetopersonsorpropertyasamatterofproductsliability,negligenceorotherwise,or fromanyuseoroperationofanymethods,products,instructions,orideascontainedinthematerialherein.
ISBN:978-0-444-62710-0
ISSN:0167-9309
BritishLibraryCataloguing-in-PublicationData AcataloguerecordforthisbookisavailablefromtheBritishLibrary.
LibraryofCongressCataloging-in-PublicationData AcatalogrecordforthisbookisavailablefromtheLibraryofCongress.
ForInformationonallElsevierPublishingpublications visitourwebsiteat https://www.elsevier.com/
ForAndyBrandandNeilBourne,scallopafficionados,mentors,andfriends.
ListofContributorsxi Prefacexiii
PrefacefromSecondEditionxv
PrfacefromFirstEditionxvii
1.ReconcilingMorphologicalandMolecular ApproachesinDevelopingaPhylogenyforthe Pectinidae(Mollusca:Bivalvia)
JEANNEM.SERB
Introduction1 WhatIsaScallop?2
ShellMorphologyandItsApplicationinTaxonomic ClassificationSystems5
TheInfluenceofMolecularPhylogeneticsonSystematics10 WhereDoWeGoFromHere?19 Summary24 Acknowledgements25 Glossary25 References25
2.BiologyandEcologyofScallopLarvae
SIMONM.CRAGG
Introduction31 EarlyLifeHistoryCharacteristicsofScallops31 LarvalDevelopment40 ComparativeAnatomy57 FunctionalMorphology58 PhysiologyandEffectsofEnvironmentalVariables60 BehaviourandLarvalDistribution62 RearingMethods70 FutureDirections72 Acknowledgements73 References73
3.ScallopStructureandFunction
PETERG.BENINGERANDMARCELLEPENNEC
Introduction85 AnOverviewoftheScallopBody85 TheMantleandItsDerivatives87 PallialOrgansandParticleProcessing91 DigestiveSystemandDigestion104 Cardio-vascularSystem111 ExcretorySystem119
ReproductiveSystem123 NervousandSensorySystems135 Foot ByssalComplex147 Acknowledgements150 References150
4.ScallopAdductorMuscles:StructureandFunction
PETERD.CHANTLER
Introduction161
StructureoftheStriatedAdductorMuscle162 StructureoftheSmoothAdductorMuscle171 Myosin177 FunctionoftheStriatedAdductor187 FunctionoftheSmoothAdductor200 AchievementsandCoda206 Acknowledgements207 References207
5.NeurobiologyandBehaviouroftheScallop
DANIELI.SPEISERANDLONA.WILKENS
Introduction219 TheMantleEyesofScallops219 VisuallyInfluencedBehavioursinScallops231 TheLocomotorySystem238 Acknowledgements248 References248
6.ReproductivePhysiology
BRUCEJ.BARBERANDNORMANJ.BLAKE
Introduction253 GametogenicCycles254 RegulationofGametogenicCycles268 EnergyMetabolism279 ApplicationstoAquaculture287 Summary290 Acknowledgements292 References292
7.Physiology:EnergyAcquisitionandUtilisation
BRUCEA.MACDONALD,V.MONICABRICELJ,AND SANDRAE.SHUMWAY
Introduction301 EnergyAcquisition301
8.NutritioninPectinids
SIMONESUHNELANDFRANCISCOJ.LAGREZE-SQUELLA
Introduction355
NutrientsandDietImprovementandSupplementation355 Summary366 References366
9.ScallopGeneticsandGenomics
MAUREENK.KRAUSEANDELISABETHVONBRAND
Introduction371 Cytogenetics371 PloidyManipulation373 MolecularMarkersofGeneticVariation376 Applications380 PopulationGenetics387 ScallopGenomics397
AdditionalAreasofGeneticResearch405 FutureDirectionsandConclusions412 References412
10.DiseasesandParasitesofScallops
RODMANG.GETCHELL,ROXANNAM.SMOLOWITZ, SHARONE.MCGLADDERY,ANDSUSANM.BOWER
Introduction425 MicrobialDiseases425 Mycota439 Protista441 Platyhelminthes448 Polychaetes452 Crustacea454 Gastropods456 Algae457 Foraminiferans458 Porifera458 Cnidaria459 Non-InfectiousDiseases459 Summary460 Acknowledgements460 References460
11.ScallopEcology:DistributionsandBehaviour ANDREWR.BRAND
FurtherStudy512 Acknowledgements513 References513
12.SwimminginScallops
HELGAE.GUDERLEYANDISABELLETREMBLAY
Introduction535
ShellCharacteristicsandTheirInfluenceUpon SwimmingCapacities536 BiomechanicsofSwimminginScallops538 LigamentProperties539 EvaluationofScallopSwimmingPerformance inNature540 LaboratoryTestsofEscapeResponsePerformance541 VisualAssessmentofEscapeResponsePerformance intheLaboratory542 InterspecificDifferencesinLaboratoryEscape ResponsePerformance545 PhysiologyofScallopSwimming546 BioticandAbioticInfluencesonMuscleUse DuringEscapeResponses549 InterspecificDifferencesinPatternsofMuscleUse550 MetabolicSupportofSwimming552 DoChangesinMuscleMetabolicCapacitieswith ReproductiveInvestmentExplainShiftsinEscape ResponseBehaviour?556 InterspecificDifferencesinMuscleMetabolic Capacities557 DeterminantsofInterspecificDifferencesin EscapeResponseStrategies:AnIndepthStudy ofFiveScallopSpecies557 References562
13.ScallopsandMarineContaminants
ISLAYD.MARSDENANDPETERJ.CRANFORD
Introduction567 TraceMetals568 TraceOrganics571 NutrientLevels573 OffshoreOilandGasOperations574 HealthRisks576 ScallopsasSentinelOrganisms577 UseofBiomarkers578 FutureDirectionsandConclusions580 References580
14.QuantifyingandManagingtheEcosystem EffectsofScallopDredgeFisheries BRYCED.STEWARTANDLEIGHM.HOWARTH
Introduction585 TypesofScallopDredgeFishery586 EffectsonScallopPopulations586
EffectsonMarineEcosystems589 EffectsonDifferentSeabedTypes594 Management599 Conclusion603 Acknowledgements604 References604
15.Dynamics,Assessment,andManagement ofExploitedNaturalScallopPopulations
J.M.(LOBO)ORENSANZ,ANAM.PARMA,ANDSTEPHENJ.SMITH
Introduction611 PopulationStructureandDynamics613 AssessmentofAbundanceandItsSpatialDistribution632 TheFishingandDepletionProcesses640 OverfishingandEcologicalEffectsofFishing654 Management661 Acknowledgements676 Acronymsusedinthetext676 References677
16.ScallopsoftheWestCoastofNorthAmerica
G.JAYPARSONS,RAYMONDB.LAUZIER,ANDNEILF.BOURNE Foreword697 Introduction697 Fisheries698 Aquaculture709 Future713 Acknowledgements714 References714
17.FisheriesSeaScallop, Placopectenmagellanicus
KEVIND.E.STOKESBURY,CATHERINEE.O’KEEFE,AND BRADLEYP.HARRIS
Foreword719 Introduction719 LifeHistory721 Ecosystem723
TheFishingFleetsofCanadaandtheUnitedStates724 StockAssessments726 FisheriesManagement729 Summary731 Acknowledgements732 References732
18.ScallopAquacultureandFisheriesinEastern NorthAmerica
SHAWNM.C.ROBINSON,G.JAYPARSONS,LESLIE-ANNEDAVIDSON, SANDRAE.SHUMWAY,ANDNORMANJ.BLAKE
Introduction737
SeaScallop(Placopectenmagellanicus)737
BayScallop(Argopectenirradians)758 CalicoScallop, Argopectengibbus 761 AquacultureandEnhancement765 Future767 Acknowledgements767 References767
19.TheEuropeanScallopFisheriesfor Pecten maximus, Aequipectenopercularis,Chlamysislandica, and Mimachlamysvaria
PETERF.DUNCAN,ANDREWR.BRAND,ØIVINDSTRAND,AND ERICFOUCHER
Introduction781 BiologyandEcology782 Fisheries801 TheFuture838 Acknowledgements841 References841
20.EuropeanAquaculture ØIVINDSTRAND,ANGELESLOURO,ANDPETERF.DUNCAN
Introduction859 HistoricalOverviewofEuropeanScallopAquaculture859 SpatProduction862 Grow-OutCulture867 SeabedRanchingandStockEnhancement875 BiologicalConstraintstoScallopCulture879 MarketandEconomics881 StockProtectionSecurityandLegalIssues882 FutureProspects883 Acknowledgements884 References884
21.ScallopFisheriesandAquaculture inJapan
YOSHINOBUKOSAKA
Introduction891 Patinopecten(Mizuhopecten)yessoensis 891 Future926 Pectenalbicans 931 Chlamys(Mimachlamys)nobilis 932 Acknowledgements932 References933
22.ScallopsandScallopAquacultureinChina XIMINGGUOANDYOUSHENGLUO
Introduction937 TheChineseScallop938 OtherScallopSpecies943
Fishery945 Aquaculture945
Harvest,Processing,andMarketing951
Acknowledgements951 References951
23.ScallopsofNorthwesternPacificRussian Federation
VICTORV.IVIN,OLGAG.SHEVCHENKO,AND TATIANAYU.ORLOVA
Introduction953 BiologyandEcology953 FishingandAquaculture975
Acknowledgements991 References991
24.AquacultureoftheScallop Nodipectennodosus inBrazil
GUILHERMES.RUPPANDG.JAYPARSONS
Introduction999
Aquacultureof Nodipectennodosus inBrazil1001
Acknowledgements1015 References1015
25.ScallopsBiology,Fisheries,andManagement inArgentina
GASPARSORIA,J.M.(LOBO)ORENSANZ,ENRIQUEM.MORSAN, ANAM.PARMA,ANDRICARDOO.AMOROSO
Introduction1019
TheTehuelcheScallop, Aequipectentehuelchus
1019
ThePatagonianScallop, Zygochlamyspatagonica 1032 Acknowledgements1041 References1041
26.ScallopFisheryandAquacultureinChile: AHistoryofDevelopmentsandDeclines
ELISABETHVONBRAND,ALEJANDROABARCA, GERMANE.MERINO,ANDWOLFGANGSTOTZ
Introduction1047
SpeciesDescription1047 Fisheries1050
HowScallopAquacultureStartedinChile1053
AquacultureProduction1055
Acknowledgements1068 References1068
27.ScallopAquacultureandFisheriesinVenezuela CE ´ SARJ.LODEIROS,LUISFREITES,JOSE ´ J.ALIO ´ ,MAXIMIANONU ´ NEZ, ANDJOHNH.HIMMELMAN
Introduction1073
Distribution,Habitat,andReproduction1073 Fisheries1077 Aquaculture1078 PerspectivesforCulture1084 Acknowledgements1085 References1085
28.ScallopFisheryandCultureinPeru
JAIMEMENDO,MATTHIASWOLFF,TANIAMENDO,ANDLUISYSLA
Introduction1089
SpeciesDescription1089 ProductionChainandMarketing1094 FisheriesandAquacultureProduction1095 ChallengesandProjectionsofPeruvianScallopProduction1104 Acknowledgements1105 References1105
29.ScallopFisheriesandAquacultureinMexico
CESARA.RUIZ-VERDUGO,VOLKERKOCH,ESTEBANFELIX-PICO, ANAISABELBELTRAN-LUGO,CARLOSCA ´ CERES-MARTI ´ NEZ, JOSE MANUELMAZON-SUASTEGUI,MIGUELROBLES-MUNGARAY, ANDJORGECACERES-MARTI ´ NEZ
Introduction1111 DescriptionofMexicanScallops1112 Fisheries1114 Aquaculture1119 References1123
30.ScallopFisheries,Mariculture,andEnhancement inAustralasia
MICHAELC.L.DREDGE,ISLAYD.MARSDEN,ANDJAMESR.WILLIAMS
Introduction1127 Biology1129 FisheriesandFisheryManagement1140 Culture1161
FutureDirectionsandConclusions1164 Acknowledgements1166 References1166
GeneralIndex1171 SpeciesIndex1189
ListofContributors AlejandroAbarca DepartamentodeAcuicultura, UniversidadCato ´ licadelNorte,Coquimbo,Chile
Jose ´ J.Alio ´ InstitutoNacionaldeInvestigacionesAgrı´colas, Cumana ´ ,EstadoSucre,Venezuela
RicardoO.Amoroso SchoolofAquaticandFishery Sciences,UniversityofWashington,Seattle,WA,USA
BruceJ.Barber EckerdCollege,St.Petersburg,Florida, USA
AnaIsabelBeltran-Lugo DepartamentodeIngenierı ´ aen Pesquerı´as,UniversidadAuto ´ nomadeBajaCaliforniaSur Ap.,LaPaz,BajaCaliforniaSur,Me ´ xico
PeterG.Beninger LaboratoiredeBiologieMarine,Faculte ´ desSciences,Universite ´ deNantes,Nantes,France
NormanJ.Blake CollegeofMarineScience,Universityof SouthFlorida,St.Petersburg,Florida,USA
NeilF.Bourne FisheriesandOceansCanada,Pacific BiologicalStation,Nanaimo,BritishColumbia,Canada
SusanM.Bower FisheriesandOceansCanada,Pacific BiologicalStation,Nanaimo,BritishColumbia, Canada
AndrewR.Brand UniversityofLiverpool,PortErin,Isleof Man,UnitedKingdom
V.MonicaBricelj DepartmentofMarineandCoastal SciencesandHaskinShellfishResearchLaboratory,School ofEnvironmentalandBiologicalSciences,Rutgers University,PortNorris,NJ,USA
JorgeCaceres-Martı ´ nez CentrodeInvestigacio ´ nCientı´ficay Educacio ´ nSuperiordeEnsenada(CICESE),Ensenada, BajaCalifornia,Me ´ xico;InstitutodeSanidadAcuı´cola, Ensenada,BajaCalifornia,Me ´ xicoInstitutodeSanidad Acuı´cola,Ensenada,BajaCalifornia,Me ´ xico
CarlosCa ´ ceres-Martı ´ nez DepartamentodeIngenierı ´ aen Pesquerı´as,UniversidadAuto ´ nomadeBajaCaliforniaSur Ap.,LaPaz,BajaCaliforniaSur,Me ´ xico
PeterD.Chantler UnitofVeterinaryMolecularandCellular Biology,ComparativeBiomedicalSciences,RoyalVeterinary College,UniversityofLondon,London,UnitedKingdom
SimonM.Cragg InstituteofMarineSciences,Universityof Portsmouth,Portsmouth,UnitedKingdom
PeterJ.Cranford FisheriesandOceansCanada,Coastal EcosystemSciencesDivision,BedfordInstituteof Oceanography,Dartmouth,NovaScotia,Canada
Leslie-AnneDavidson FisheriesandOceansCanada, Moncton,NewBrunswick,Canada
MichaelC.L.Dredge Tasmania,Australia
PeterF.Duncan FacultyofScience,Health,Educationand Engineering,UniversityoftheSunshineCoast, Queensland,Australia
EstebanFe ´ lix-Pico CentroInterdisciplinariodeCiencias Marinas,LaPaz,BajaCaliforniaSur,Mexico
EricFoucher IFREMER LaboratoireHalieutiquedePort enBessin,PortenBessin,France
LuisFreites InstitutoOceanogra ´ ficodeVenezuela, UniversidaddeOriente,Cumana ´ ,EstadoSucre, Venezuela
RodmanG.Getchell DepartmentofMicrobiologyand Immunology,CollegeofVeterinaryMedicine,Cornell University,Ithaca,NY,USA
HelgaE.Guderley De ´ partementdeBiologie,Universite ´ Laval,Que ´ becCity,Que ´ bec,Canada
XimingGuo HaskinShellfishResearchLaboratory, DepartmentofMarineandCoastalSciences,Rutgers University,PortNorris,NJ,USA
BradleyP.Harris Fisheries,AquaticScienceand TechnologyLaboratory,AlaskaPacificUniversity, Anchorage,AK,USA
JohnH.Himmelman De ´ partementdeBiologie,Universite ´ Laval,Que ´ becCity,Que ´ bec,Canada
LeighM.Howarth SchoolofOceanSciences,Bangor University,MenaiBridge,Anglesey,UnitedKingdom
VictorV.Ivin InstituteofMarineBiology,FarEastern BranchoftheRussianAcademyofSciences,Vladivostok, Russia
VolkerKoch DeutscheGesellschaftfu ¨ rInternationale Zusammenarbeit(GIZ),LaPaz,BajaCaliforniaSur,Me ´ xico YoshinobuKosaka AomoriPrefecturalIndustrial TechnologyResearchCenter,FoodResearchInstitute, Aomori,Japan
MaureenK.Krause DepartmentofBiology,Hofstra University,Hempstead,NY,USA
FranciscoJ.Lagreze-Squella FederalUniversityofParana ´ , PontaldoParana ´ ,Parana ´ ,Brasil
RaymondB.Lauzier FisheriesandOceansCanada,Pacific BiologicalStation,Nanaimo,BritishColumbia,Canada
MarcelLePennec InstitutUniversitaireEurope ´ endela Mer,Universite ´ deBretagneOccidentale,Plouzane ´ ,France
Ce ´ sarJ.Lodeiros InstitutoOceanogra ´ ficodeVenezuela, UniversidaddeOriente,Cumana ´ ,EstadoSucre,Venezuela
AngelesLouro InstitutoEspanoldeOceanografı´a,A Coruna,Spain
YoushengLuo MarineFisheriesResearchInstitute,Dalian, Liaoning,PRChina
BruceA.MacDonald BiologyDepartment,Universityof NewBrunswick,SaintJohn,NewBrunswick,Canada
IslayD.Marsden SchoolofBiologicalSciences,University ofCanterbury,Christchurch,NewZealand
Jose ´ ManuelMazon-Suastegui CentrodeInvestigaciones BiologicasdelNoroeste,LaPaz,BajaCaliforniaSur, Me ´ xico
SharonE.McGladdery FisheriesandOceansCanada,St. AndrewsBiologicalStation,St.Andrews,NewBrunswick, Canada
JaimeMendo Dpto.ManejoPesqueroyMedioAmbiente, FacultaddePesquerı´a,UniversidadNacionalAgrariaLa Molina,Lima,Peru
TaniaMendo InstituteforMarineandAntarcticStudies, UniversityofTasmania,Taroona,Tasmania,Australia
Germa ´ nE.Merino DepartamentodeAcuicultura, UniversidadCato ´ licadelNorte,Coquimbo,Chile
EnriqueM.Morsa ´ n InstitutodeBiologı´aMarinay Pesquera‘Alte.Storni’,UniversidadNacionaldel Comahue,SanAntonioOeste,Rı´oNegro,Argentina
MaximianoNu ´ n˜ez InstitutoOceanogra ´ ficodeVenezuela, UniversidaddeOriente,Cumana ´ ,EstadoSucre, Venezuela
CatherineE.O’Keefe SchoolforMarineScienceand Technology,UniversityofMassachusetts,Fairhaven,MA, USA
J.M.(Lobo)Orensanz CentroNacionalPatago ´ nicoCONICET,PuertoMadryn,Chubut,Argentina
TatianaYu.Orlova InstituteofMarineBiology,FarEastern BranchoftheRussianAcademyofSciences,Vladivostok, Russia
AnaM.Parma CentroNacionalPatago ´ nico-CONICET, PuertoMadryn,Chubut,Argentina
G.JayParsons FisheriesandOceansCanada,Aquaculture, BiotechnologyandAquaticAnimalHealthScienceBranch, Ottawa,Ontario,Canada
ShawnM.C.Robinson FisheriesandOceansCanada,St. Andrews,NewBrunswick,Canada
MiguelRobles-Mungaray AcuaculturaRobles,LaPaz, BajaCaliforniaSur,Me ´ xico
Ce ´ sarA.Ruiz-Verdugo DepartamentodeIngenierı ´ aen Pesquerı´as,UniversidadAuto ´ nomadeBajaCaliforniaSur Ap.,LaPaz,BajaCaliforniaSur,Me ´ xico
GuilhermeS.Rupp EPAGRI EmpresadePesquisa Agropecua ´ riaedeExtensaoRuraldeSantaCatarina, Floriano ´ polis,SantaCatarina,Brazil
JeanneM.Serb DepartmentofEvolution,Ecology andOrganismalBiology,IowaStateUniversity,Ames, IA,USA
OlgaG.Shevchenko InstituteofMarineBiology,Far EasternBranchoftheRussianAcademyofSciences, Vladivostok,Russia;ResearchandEducationalCenter PrimorskyAquarium,OstrovRusskii,Vladivostok, Russia
SandraE.Shumway DepartmentofMarineSciences, UniversityofConnecticut,Groton,Connecticut,USA
StephenJ.Smith FisheriesandOceansCanada,Bedford InstituteofOceanography,Dartmouth,NovaScotia, Canada
RoxannaM.Smolowitz AquaticDiagnosticLaboratory, FeinsteinCollegeofArtsandSciences,RogerWilliams University,Bristol,RI,USA
GasparSoria CentroNacionalPatago ´ nico(CONICET), PuertoMadryn,Chubut,Argentina
DanielI.Speiser DepartmentofBiologicalSciences, UniversityofSouthCarolina,Columbia,SC,USA
BryceD.Stewart EnvironmentDepartment,Universityof York,Heslington,NorthYorkshire,UnitedKingdom KevinD.E.Stokesbury SchoolforMarineScience andTechnology,UniversityofMassachusetts,Fairhaven, MA,USA
WolfgangStotz DepartamentodeBiologı´aMarina, UniversidadCato ´ licadelNorte,Coquimbo,Chile ØivindStrand InstituteofMarineResearch,Bergen, Norway
SimoneSu ¨ hnel FederalUniversityofSantaCatarina, Floriano ´ polis,SantaCatarina,Brasil.
IsabelleTremblay De ´ partementdeBiologie,Universite ´ Laval,PavillonAlexandre-Vachon,Que ´ becCity,Que ´ bec, Canada;RessourcesAquatiquesQue ´ bec,Institutdes sciencesdelamerdeRimouski,Universite ´ duQue ´ beca ` Rimouski,Rimouski,Que ´ bec,Canada
ElisabethvonBrand DepartamentodeBiologı´aMarina, FacultaddeCienciasdelMar,UniversidadCato ´ licadel Norte,Coquimbo,Chile
LonA.Wilkens CenterforNeurodynamicsand DepartmentofBiology,UniversityofMissouri-St.Louis, St.Louis,MI,USA
JamesR.Williams NationalInstituteofWaterand Atmosphere,ViaductHarbour,Auckland,NewZealand MatthiasWolff TheoreticalEcologyandModelling,Leibniz CenterforTropicalMarineEcology,Bremen,Germany
LuisYsla Dpto.ManejoPesqueroyMedioAmbiente, FacultaddePesquerı´a,UniversidadNacionalAgrariaLa Molina,Lima,Peru
Preface FromSandroBotticelli’sTheBirthofVenustothecorporatesymbolforShellOil,scallopsareoneofthemost widelyrecognisedshellfishworldwide.Theyareofglobaleconomicimportanceandsupportbothcommercial fisheriesandmaricultureefforts.Theyhavebeenthesubjectofnumerousresearcheffortsandtheirhigheconomicstatureencouragesaquacultureeffortsbyacademiciansandindustrialresearchers.Therapidgrowth,early maturityandhigheconomicvalueofmanyscallopspeciesofferspecialinducementtomariculturists.Scallops arealsokeyinthestructureandfunctionofthecommunitiesofwhichtheyarecharacteristiccomponents. Interestinallaspectsofscallopbiology,aquaculture,ecologyandfisheriescontinues;however,itisthefieldof geneticsthathasseenthegreatestsurgeinresearcheffortsoverthepastdecade.
TheFirstEdition,publishedin1991,representedthefirstcomprehensivetreatiseonscallops.Itwasprepared ascamera-readycopyusingtheveryearliestof‘desk-top’publishingprogrammesandonlythroughtheparticipationofScottSiddallwaspublicationmadepossible.Technologyhasthankfullyprogressedandword-processinghasmadeprojectssuchasthismoretenable butstillnotwithoutfrustrationsandroadblocks.
Theoriginalversionwasfollowed15yearslaterwiththeSecondEditionin2006.Sincethatprinting,five InternationalPectinidWorkshopshavebeenheld:Halifax,NovaScotia,Canada;SantiagodeCompostela,Spain; Quingdao,China;Florianopolis,Brazil;andmostrecently,Galway,Ireland.Thesemeetingsprovidedaunique andfocusedforumfordiscussionof‘allthingsscallop’andwebelievethatbothdirectlyandindirectlythecontributionspresentedherehavebenefittedgreatlyfromthoseopenandoftenlivelydiscussions.
ManyoftheauthorsfromtheFirstandSecondEditionshavesinceretiredortakenonotherresponsibilities andreaderswillnoteanumberofnewcontributors.Somehavejoinedforceswithpriorauthors,whileothercontributorshavepennednewsubmissions.
Thepresentvolumepresentsacomprehensiveoverviewofthebiology,ecology,aquaculture,andfisheries prospects,bothpresentandfuture,forscallopsworldwide.Theinclusionoffisheriesinthetitleisatestamentto increasedresearchandtheimportanceofthecommercialfleetsandhabitats.Somechaptershavebeencompletely rewritten,somehavebeenrevised,andnewchaptershavebeenadded.Whilethesubjectmatterisspecifically concernedwithscallopspecies,thebookshouldbeofinterestandrelevancetoanumberofreadersincluding advancedundergraduate/graduatestudents,mariculturists,researchersandfisheriesmanagers,andscallop enthusiasts.Chaptershavebeenpreparedbysomeoftheforemostauthoritiesintheirrespectivefieldsandrepresent24countries.ManuscriptssubmittedbyauthorswhosefirstlanguageisnotEnglishhavebeencorrectedfor grossgrammaticalerrorsandclarityofpresentationonly.Theireffortstowriteamanuscriptinaforeignlanguagearetobeapplaudedandshouldnotbecloudedbyeditoriallicense.Scallopsareofmoreeconomicimportanceinsomecountriesthaninothersandthisisreflectedinthespecificcoverageoftheindividualspecies.
Thebookiscomprisedof30chapters:thefirst15spanningtopicsfromphylogeny,biologyoflarvae,structure andfunction,genetics,physiology,nutrition,swimming,ecology,populationsdynamics,etc.Andthesecond halfofthebookisacomprehensivecountryorregionaloverviewofthefisheryandaquacultureofscallopsfrom allthekeyareasofproduction.
Wehavededicatedthiseditiontoourfriendsandcolleagues,Andrew(Andy)BrandandNeilBourne.From hishomebaseontheIsleofMan,Andydevotedhiscareertomentoringstudents,andbringingtop-tierscience tofishermen,governmentmanagers,aquaculturists,andmostrecentlytothesustainabilitycertificationeffortsof theMarineStewardshipCouncil.Andyhasalwaysbeengenerouswiththisknowledgeandtime,andunofficially recognisedastheseniorstatesmanoftheInternationalPectinidWorkshops.Thankyou,Andy,forallyouhave contributed.AndfromhisscenicbaseinNanaimo,BritishColumbia,CanadaNeil,too,hasspentanillustrious careerasashellfishresearcherworkingwithmanagers,scientists,students,andfishingandaquacultureindustry memberstodiscoverandcommunicateavastarrayofknowledgeofscallopsandotherbivalvespecies.Inadditiontobeingamentor,teacherandresearcherparexcellence,Neilwasinstrumentalinlayingthefoundationfor
thescallopaquacultureindustryinBritishColumbia.Neil,thankyouforyourfriendship,insightsand contributions.
ThecurrenteditionhasbenefittedgreatlyfromtheeffortsofNoreenBlaschikwhohastirelesslyhelpedwith proofreading,referencecross-checkingandotherthanklesstasks.ThetalentsofEricHeupelwerekeyinredraftingmanyofthefiguresandaregratefullyacknowledged.Gettingauthorstoagreetoparticipateinventuressuch asthisismucheasierthanextractingthefinaltextsandweextendourdeepestgratitudetotheauthorsfortheir skill,patienceandperseverance.ThankstoSharon,MichaelandChristopherfortheirsupport,cajolingand patience.GusandZeusspentmanyeveningspawingovertexts,andtheirassistancemadethetasksathand moretolerable.
AspecialthankstoPatriciaOsborne,ElsevierSciencePublisherswhoinitiatedandencouragedtheeffortfora ThirdEditionandtoJaclynTruesdell,DebbieClarkandKarenMillerfortheirpatienceandguidanceduringthe production.
Forsuccessfulcultureandmanagement,agoodknowledgeofthebiology,ecology,physiologyandfisheriesof thespeciesisnecessaryandwehopethatthisThirdEditionofScallops:Biology,Ecology,Aquaculture,and Fisherieswillserveasasolidreferencebaseforyearstocome.
SandraE.Shumway1 andG.JayParsons2
1DepartmentofMarineSciences,UniversityofConnecticut,Groton,CT,USA 2FisheriesandOceansCanada,Aquaculture,BiotechnologyandAquaticAnimalHealthScienceBranch, Ottawa,ON,Canada
PrefacefromSecondEdition Fromtheircontinuedappearanceinartandculturetotheirsavouredplaceatthedinnertable,scallopshave notlosttheirgeneralappealandcontinuetogarnertheattentionofscientists,aquaculturists,chefs,shellcollectorsandothers.DiscussionduringtheSixthInternationalPectinidWorkshopin1987providedtheimpetusfor theFirstEditionof Scallops:Biology,EcologyandAquaculture whichwaspublishedin1991andhasbeenoutof printfornearlyadecade.TalkofaSecondEditionbeganalmostimmediately,butwasgentlyignoredforsome yearsbecauseofthetimeandeffortrequiredofallcontributorsandasenseonthepartoftheoriginaleditorthat therewasnotenoughnewinformationtowarrantasecondvolume.
Interestinallaspectsofscallopbiologyandecologyhascontinuedtoincrease,cultureeffortshaveexpanded globallyandscallopscontinuetobringhighpricesfromboththecommercialfisheriesandaquacultureventures.
PotentialauthorsbegantoenquireenthusiasticallyaboutthepotentialforaSecondEdition,ElsevierScience Publisherswereeagertoaddthevolumetotheirseriesandtherewasarenewedsenseofneedcoupledwith availabilityofnewinformationtoproceedwithpublishingaSecondEdition.
ThepresentvolumerepresentsanupdatedandrevisedversionoftheFirstEdition.Itisacomprehensiveoverviewofthebiology,ecologyandaquacultureforscallopspeciesworldwide.Somechaptershavebeencompletely rewrittenbypreviousornewauthorsandtwochaptershavebeenreprintedasintheoriginalvolume (seeChapter5 NeurobiologyandBehaviouroftheScallopbyWilkensandChapter8 Physiological IntegrationsandEnergyPartitioningbyThompsonandMacDonald)astheyareaspertinentnowastheywerein 1991.Otherchaptershavebeenrevisedandnewonesadded(Nutritionandaccountsbycountryofaquaculture andfisheries Brazil,VenezuelaandtheRussianFederationnowthattheformerSovietUnionhastransformed sincetheFirstEdition!).Thisworkwouldnothavebeenpossiblewithouttheassistanceofseveralindividuals. WethankLindaKallansrude,ManonChouinardandDinahHelpertwhoprovidedsecretarialandadministrative support,MailleLyonswhotookonthearduoustaskofdevelopingtheindices,MaraVos-Sarraiento(Elsevier) forassistance,guidanceandsupport,andaspecialthankstoSharon,Christopher,MichaelandMaxfortheir supportandpatience.
Finally,theauthorsaretobecongratulatedfortheireffortsandthankedprofuselyfortheirpatienceduring thepublicationprocess.
WehavededicatedthisvolumetoSamNaidu,friendandcolleague,whodevotedhiscareertoworkingwith fishermen,aquaculturistsandgovernmentmanagerstoensureasustainablefisheryforfuturegenerations.Sam wasagentleman,generouswithhisknowledgeandexpertise,acceptednosocialbarriersandwasapillarofthe PectinidWorkshops.Moreover,hehadperfectedtheartoflivingwellandappreciatinglife.Sincepublicationof theFirstEdition,therehavebeen7subsequentInternationalPectinidWorkshops,the15thheldinMooloolaba, Australiaandthe16thheldinHalifax,NovaScotia,Canadain2007.
Wehopethisvolumewillcontinuetofosterinterestinscallops,especiallyaquacultureforasustainablefuture, foryearstocome.
SandraE.ShumwayandG.JayParsons Groton,CT,USA Ottawa,ON,Canada
PrefacefromFirstEdition Scallopsareamongthebetterknownshellfishesandarewidelydistributedthroughouttheworld.Theyareof worldwideeconomicimportanceandsupportbothcommercialfisheriesandmaricultureefforts.Theyhavebeen thesubjectofnumerousresearcheffortsandtheirhigheconomicstatureencouragesaquacultureeffortsbyboth academiciansandindustrialresearchers.Therapidgrowth,earlymaturityandhigheconomicvalueofmany scallopspeciesofferspecialinducementtomariculturists.Scallopsarealreadyculturedsuccessfullyinanumber ofgeographiclocationsandemphasisisincreasingglobally.Further,scallopsplayanimportantroleinthestructureandfunctionofthecommunitiesofwhichtheyareacharacteristicandimportantcomponent.
NotsincethepublicationofMarineMussels(Bayne,1975:IBPHandbook)hasthecurrentknowledgeofaparticulargroupofmolluscsreceivedacomprehensivecoverage.Hiseffortwasawelcomeadditiontothescientific literatureandprovidedanopportunitytosynthesiseawealthofinformation.Forsuccessfulcultureandmanagement,agoodknowledgeofthebiologyofthespeciesisnecessary.Whilescallopshavebeenthesubjectofaconsiderableamountofresearch,todatenointegratedaccountexistsofthebiology.
Discussionsregardingtheneedforacomprehensivetreatiseonscallopsfirsttookplacein1987duringthe SixthInternationalPectinidWorkshopinMenaiBridge,Wales.Thelevelofenthusiasmwashighandconvincing theindividualauthorstoundertakewritingthechapterswasaneasytask.Thesubsequenttaskofcollectingand integratingthosemanuscriptsprovedtobeconsiderablymorearduous.Therewerefurtherdiscussionsregarding thefinalversionsofmanuscriptsduringtheSeventhInternationalPectinidWorkshopheldinPortland,Maine,in 1989.Thesemeetingsprovidedauniqueopportunityforspecialistsinthefieldofscallopbiologyrepresenting over20countriestomeetanddiscusstheirindividualviewsandIbelievethatthefinalproducthasbenefited greatlyfromthoseopenandoftenlivelydiscussions.
Thepresentvolumepresentsacomprehensiveoverviewofthebiology,ecology,andaquacultureprospects, bothpresentandfuture,forscallopsworldwide.Althoughthesubjectmatterisspecificallyconcernedwiththe biology,ecologyandaquacultureofscallopspecies,thebookshouldbeofinterestandrelevancetoanumberof readersincludingadvancedundergraduate/graduatestudents,mariculturistsandresearchworkers.Contributed chaptershavebeenpreparedbysomeoftheforemostauthoritiesintheirrespectivefieldsandrepresentsome18 countries.ManuscriptssubmittedbyauthorswhosefirstlanguageisnotEnglishhavebeencorrectedforgross grammaticalerrorsandclarityofpresentationonly.Theireffortstowriteamanuscriptinaforeignlanguageare tobeapplaudedandshouldnotbecloudedbyeditoriallicence.
Thebookisdividedintotwomainsections:thefirstdealingwithgeneralbiology,ecology,andphysiology andtheseconddealingwithfisheriesandcultureeffortsinspecificcountries.Obviously,scallopsareofmore economicimportanceinsomecountriesthaninothersandthisisreflectedinthespecificcoverageofspecificspeciesinChapter12.
ThephylogeneticrelationshipofscallopspeciesofcommercialinterestisexaminedbyWallerinChapter1. Theavailableinformationonlarvalrequirementsandrangesoftoleranceofenvironmentalvariables,bothprime importancetoaquacultureefforts,arediscussedbyCraggandCrispinChapter2.BeningerandLePennecprovideanelegantaccountoftheinternalanatomyofscallopsinChapter3.Theimportanceofscallopadductor musclestothefieldofmusclephysiologyisclearlydefinedbyChantlerinChapter4.EnergyacquisitionandutilisationarediscussedbyBriceljandShumwayinChapter5andthephysiologicalintegrationsandpartitioningof thisenergyarediscussedinChapter6byThompsonandMacDonald.Reproductivebiology,anotherareaof primeimportancetoculturists,isreviewedbyBarberandBlakeinChapter7.Twoofthemoststrikingfeatures ofscallops,eyesandtheirabilitytoswim,arediscussedbyWilkensinChapter8.Diseasesandparasites,major threatstoaquacultureventures,arediscussedbyGetchellinChapter9,andGouldandFowlerreviewtheeffects ofpollutantsonthecommercialspeciesofscallopsinChapter10.Generalecology,distributionandbehaviour aregiveninChapter11byBrand.BeaumontandZourosreviewtheapplicationofgenetictoolstoscallopsand
theimportanceofgeneticstofisheriesandaquacultureofscallopsinChapter12.InChapter13,Orensanz,Parma andIribanediscusspopulationdynamicsandthemanagementofnaturalstocks.ThecommercialspeciesofscallopsarecoveredinChapter14accordingtogeographiclocation.MuchofthedatapresentedinChapter14is beingreportedforthefirsttime,includingsuchelementarymeasuresasgrowth,meatweightandlandings. ThisworkwouldnothavebeenpossiblewithouttheeffortsofDr.ScottSiddall.Hisexpertiseinthefieldof desktoppublishingcoupledwithhisknowledgeofshellfishbiologymademytaskpossible.Hiscontinuedinterest,supportandinterjectionsofhumourwhenmostneededmadethetaskenjoyable.JanBarter,Martha Hernandez-Davis,JohnHedleyandJimRollinshelpedinvariouswaysandtheirwillingnesstoundertakesuch arduoustasksasproofreading,crosscheckingreferences,retypingofmanuscriptsandredrawingandrepairof submitteddiagramsaregratefullyacknowledged.AspecialthanksmustgotoBobGoodman,ElsevierScience PublishingCompany,forhisconsiderablepatiencein‘meeting’deadlinesandhisinsightandsupport.Finally, Iwouldliketothanktheauthorsfortheirskill,patience,andperseverance.
1 ReconcilingMorphologicalandMolecular ApproachesinDevelopingaPhylogenyforthe Pectinidae(Mollusca:Bivalvia) JeanneM.Serb
INTRODUCTION Scallops(PectinidaeRafinesque,1815)areoneofthemostmorphologically,behaviourally,andbiologically diversefamilyofbivalves.AsamajormolluscancladeofMesozoicandCenozoiceras,thePectinidaehashada tumultuous245-million-yearhistory,survivingtwomassextinctioneventsattheTriassic-Jurassicand Cretaceous-Paleogeneboundaries(Hautmann,2010;NewellandBoyd,1995;Waller,2006a).Overtheintervening quarterofabillionyears,itislikelythatscallopsunderwentseveraladaptiveradiationsthatplayedamajorrole ingeneratingthebiologicaldiversityseentoday.Currently,about270extantspeciesofscallopsarerecognised (Dijkstra,2014)andaredistributedacrosspolar,temperate,andtropicalseas,withthegreatestbiologicaldiversityinthetropicalCaribbeanandIndo-Pacificoceans(RainesandPoppe,2006).Mostscallopspeciesarefound intheshallowsofsublittoralreefs,sandybays,andseagrassbedsofthecontinentalshelves,withasmallernumberofspeciesrestrictedtodeeperwaterincludingtheabyssaldepthsat7000m.Whilethetypicalscallopshell shapeisthefamiliarroundeddiskandstraighthingelineformedbytwoear-likeauricles,scallopsexhibitawide rangeofmodificationsonthisgeneralisedphenotype,withstrikingshape,texture,andcolourvariantsofthe shell.Thisvarietyhasmadescallopsafavouriteofamateurshellcollectorsandscientistsalikeand,asaresult, theirshellsarewellrepresentedinthecollectionsofnaturalhistorymuseums(e.g. Dijkstra,1999; Dijkstraand Koehler,2008).Theon-goingchallengeforscallopbiologistsistoorganisetheimpressivebiologicaldiversityof thePectinidaeinaphylogeneticcontext.
Underaphylogeneticclassificationsystem,taxaareorganisedhierarchicallyintogroupsthatreflectahypothesisofevolutionaryrelationshipderivedfromaphylogenetictree.Aphylogenetictree(alsocalleda‘phylogeny’ or‘topology’)isabifurcatingdiagramthatdepictstherelationshipsbetweentaxabasedonsharedhistory throughcommondescent(Gregory,2008).Notonlycanthephylogenyhelpidentifygroupsoftaxa(clades),but phylogenetictreesindicaterelationshipsbetweenthesegroups,forexample,howtribesarerelatedtooneanother inasubfamily.Phylogenetictreesalsoprovideahistoricalcontextandarelativeorderforwhenlineagesarose anddiversified.Moreover,thephylogenycanbeusedtostudytheevolutionoftraits,suchaswhetheracharacterstateisancestral(plesiomorphic)orderived(i.e.traitpolarity),ortotesthypothesesregardingtherateor modeoftraitevolution.
Basingaclassificationsystemonphylogenyincorporatestheevolutionaryhistoryofthosetaxaandallthe associatedinformationintotheclassification.Speciesorlineagesthataredescendantsofasingleancestorrepresent‘naturalgroups’,andtherecognitionofnaturalgroupsgivespredictivepowertoaclassificationsystem becausethesharedcharactersmayalsoindicatesimilaritiesinlifehistorytraits,habitatrequirements,orecologicalfunctionduetosharedhistoryoftheorganisms.Thus,modernclassificationsystemsareinformationretrieval resources,whereanindividualspeciescanbeusedtorepresentabroadersetofspeciesinsomecontexts,suchas
2 1.RECONCILINGMORPHOLOGICALANDMOLECULARAPPROACHESINDEVELOPINGAPHYLOGENYFORTHEPECTINIDAE(MOLLUSCA:BIVALVIA)
the‘surrogateapproach’forconservationmanagement(Wiensetal.,2008)orasanorganismalmodelfora researchprogramme(JennerandWills,2007).ForthePectinidae,abetterunderstandingofthephylogenyofscallopscouldguideaquaculturalistswhentargetingwhichspecieswouldbebestsuitedforculturingunderparticularconditions.Inaddition,acommonnomenclatureforscallopswillfacilitatecommunicationamongworkers fromdifferentscientificdisciplinesorcountries.
Furthermore,thePectinidaehasgreatpotentialtobeamodelsysteminevolutionarybiology.Scallopsrepresentalargeanddiversegroupofanimalswithasuperbfossilrecord,andsocantellusmuchaboutevolutionary processeslikespeciation,adaptation,andextinction.AlreadythePectinidaehasdemonstratedutilityinthestudy ofmorphology(Serbetal.,2011;Sherrattetal.,n.d.),behaviour(Alejandrinoetal.,2011),sensorybiology(Pairett andSerb,2013;Serbetal.,2013),genomeevolution(WangandGuo,2004),andextinctionrisk(SmithandRoy, 2006;Harnik,2011).Butinordertounderstandtheprocessesunderlyingthesetrends,weneedanaccuratephylogenyand,preferably,worktowardsaninclusivephylogenythataccountsforbothlivingandextinctspecies. Withthisphylogenyinhand,researcherscannotonlyorganisebiologicaldiversityintoaclassificationscheme thatreflectsrelatednessbutalsostudytheprocessesthatgeneratedthisbiologicaldiversity.
Thisreviewexaminestheconflictsbetweenmorphological-basedandmolecularphylogenetichypothesesof thePectinidae.Thefirstsectiondescribesthecharacteristicsofscallopsbydefiningthetraitsuniquetothefamily andprovidesbackgroundontheecologicalandphenotypicdiversityofthegroup.Throughareviewofprevious work,thesecondsectionexplainshowthismorphologicaldiversitywasusedtodevelopaclassificationsystem forthePectinidaeandshowshowthesesystemsareaffectedbyconvergentevolutionoftheshell.Thethirdsectiondescribeshowmolecularphylogeneticscanaddtoourunderstandingofscalloprelationshipsandevolution, reviewsthelastdecadeofphylogeneticstudyonthePectinidae,andprovidesacasestudy.Thechapterends withsomethoughtsaboutwhatstillneedstobedonetoaddresslong-standingissuesinscallopphylogenetics includingdeterminingtheevolutionaryoriginofthePectinidae,howtobetterestimatebiologicaldiversityinthe family,andmethodstoincorporateextantandextincttaxainacomprehensivephylogenetichypothesisforthe scallops.
WHATISASCALLOP? DefiningthePectinidae ScallopsbelongtothePectinoideaRafinesque,1815,asuperfamilythatincludesthePectinidae;Entoliidae Teppner,1922;Propeamussiidae Abbott,1954;SpondylidaeGray,1826;andtheextinctEntolioidesidaeKasumZade,2003;NeitheidaeSobetski,1960;PernopectinidaeNewell,1938;Tosapectinidae(Bieleretal.,2010).All membersofPectinoideaareunitedbyhavingatriangularresiliumwithanon-mineralisedmedialcorethatfunctionsbelowthehingeline(Waller,1978,2006b).Inearlyontogeny,allspeciesexhibitapectiniformgrowthstage completewithabyssalnotch,andpresumablythesespeciescanattachtosubstratesusingabyssus(Waller, 2006b).AfterthePectinidae,thesecondlargestextantfamilyofthePectinoideaisthePropeamussidaeor‘glass scallops’(B200species).Shellsofthesesmall,deep-waterbivalvesarethin,colourless,andresemblesomepectinidspecies.ThefamilySpondylidaeor‘thornyoysters’(B70species)isdistributedthroughoutthetropicaland subtropicaloceansandallmemberscementtosubstrates.Thefamilywiththefewestextantspeciesisthe Entoliidae,or‘smoothpectens’(twospecies).Asamendedby Waller(2006b),thisfamilycontainstwoextantspecies.Othermorphologicaldifferencesamongthepectinoideanfamiliesincludethehingedentitionandthemineralcompositionofthevalves(see Waller,2006b).
ThePectinidaeisthelargestpectinoideanfamilyanditsmemberscanbeidentifiedbytwokeystructures:(i)a particularhinge-ligamentsystemthatconnectsthetwovalvesoftheshelland(ii)thepresenceofactenolium (Waller,1984;Hautmann,2010).Thehinge-ligamentsystemofthescallopisthealivincular-alateligamentcondition (asdescribedin Hautmann,2004),whereatriangular-shaped,fibrousligament(theresilium)issecretedinadepression(theresilifer)oninternalsurfaceofalong,straighthingemarginofthedorsalportionofthevalve.Asecond ligamentextendslaterallyalongtheouterlengthofthestraighthingemargin,inawing-likeor‘alate’manner. Thelateralligamentalignsandconnectstheleftandrightvalvesoftheshelltogether,whilecompressionof theuncalcifiedcentreoftheresiliumperformslikeaspring,actinginoppositiontotheactionoftheadductormusclesthatdrawbothvalvestogether.Thus,ithasbeenhypothesisedthattheelastichingewaskeytodevelopmentof shellclappingandswimmingbehavioursexhibitedbyscallops(Trueman,1953;MarshandOlson,1994;Dickinson etal.,2000).Allscallops,andafewextinctfamilies(e.g.PernopectinidaeandEntiolioididae; Korobkov,1960),
possessthealivincular-alateligament.Incontrast,thectenoliumisuniquetothePectinidaeandispresentatleastin theearlypost-larval(dissoconch)growthstages.Thectenoliumisarowofhook-shapeddenticlesalongtheventral edgeofbyssalnotch(Waller,1978,1984)(Figure1.1).Asaproteinbyssusissecretedbythebyssalglandwithinthe muscularfoot,itpassesoverthedenticlesofthectenoliumwhichkeepsthearrayofthreadsflatalongtheedgeof theshell(Waller,1984:Figure4b,c).Thecombinationofabyssalthreadsheetandthetwo-pointcontactofshelltoa surface(see Stanley,1972)stabilisestheanimal’sconnectiontothesubstrateandgreatlyreduceshowmuchtheshell canrotatearoundthebyssus.Asaresult,muchmoretorquemustbeappliedtobreakthebyssalattachment(Waller, 1984)andthismayprovideanadditionallevelofprotectionfrompredatorsthatmustdislodgeandmanipulateprey itemsbeforeconsumption(Caroetal.,2008).
TheRelationshipBetweenLifeHabitandShellShape Scallopsmetamorphosefromaswimmingpediveligertoacrawling,benthicpost-larva.Atthistime,themantlebeginssecretionofthedissoconchshell(HodgsonandBurke,1988),whosemicrosculpturepatternshavebeen usedascharactersinsomeclassificationsystems(Waller,1991).Allnewlymetamorphosedscallopspossessactenoliumandcanproduceabyssustoattachtoasubstrate.Thisattachmentistemporaryastheanimalcanrelease thebyssusandthensecreteanewbyssustoattachtoanothersubstrate.Astheanimalgrowsandmatures,the ctenoliummaybeovergrownbytheadvancingfrontoftheanteriorauricle(Waller,1984:Figures2a c,3b).This resultsintheprogressivelossoftheabilitytoattachusingabyssusasbodysizeincreases(Caddy,1972).Thus, somescallopspeciesonlyemployabyssusasjuvenilesandlosetheabilitytoproduceabyssusasadults,becoming‘free-living’.
Basedontheabilitytoattachandmodeoflocomotion,adultscallopscanbeplacedintosixfunctionalgroups orlifehabits(sensu Stanley,1970).Theselifehabitsareassociatedwithspecificshellformsofscallops(Stanley, 1970).Themajorityofscallopspecieshavethebyssalattachinglifehabit,whereabilitytoattachtemporarilytoa substrateviabyssusismaintainedaftermaturity.Byssalattachershaveachlamydoidform,wheretheshellhasa strongasymmetryalongtheanterior posterioraxissuchthattheauriclesareofdifferentsizesandtheshell outlineisoblique(Figure1.2A).Additionally,therightvalvehasadeepbyssalnotchwithawell-developed ctenolium(Figure1.1).Ithasbeenhypothesisedthatthechlamydoidformistheplesiomorphicconditionforthe Pectinidae(Waller,1993).Afewbyssalattachingspecies,like Pedumspondyloidium (Gmelin,1791),exhibitthe nestlinglifehabit.Thesespeciesareobligateassociateswithlivingscleractiniancorals,wherethepost-larvapreferentiallysettleson,andbyssallyattachesto,coralpolypswhichgrowaroundthescallopencasingit(Yonge, 1967;Waller,1972a).
Otherspecies,suchas Crassadomagigantea (Gray,1825),permanentlyattachtohard,oftenabiotic,substrates bysecretingnewshellmaterial.Thiscementinglifehabitisassociatedwithashellthattransitionsfromthe
FIGURE1.1 Somemorphologicalfeaturesofthepectinidshell.Rightvalveof Volachlamystranquebaria orientedwithanterior(ant.)towards rightandposterior(post.)towardsleft.
Ctenolium
Ant. auricle Post. auricle Byssal notch Umbo
Right valve
4 1.RECONCILINGMORPHOLOGICALANDMOLECULARAPPROACHESINDEVELOPINGAPHYLOGENYFORTHEPECTINIDAE(MOLLUSCA:BIVALVIA)
FIGURE1.2 Fourcommonformsofscallopshells.Three-dimensionalsurfacescansoftheleftvalveofrepresentativescallopspeciesfor thechlamydoid(A);aequipectinoid(B);pectinoid(C),andamusioid(D)forms.Thecementingformisnotshown.Anterior(ant.)towards rightandposterior(post)towardsleft.
chlamydoidformtohighlyvariableshellshapeasgrowthoftherightvalveconformstothesubstrate. Morphologicalchangesincludeventralmigrationoftheligamentsystemandanincreaseddistancebetweenthe palliallineandshellmargin(Yonge,1951;Waller,1972a;Harper,1991),creatingathickenedanddistortedshell thatsuperficiallyresemblestheshellofoyster.Whilenotaspecificshellshape,thisshellformisoftenassociated withthename Hinnites (asin Hinnitespusio (Linnaeus,1758)).
Somepectinidspeciesdonotattachtoasubstrateofanykindasadults.These‘free-living’specieseitherpassivelyoccupyapositionon,orarepartiallycoveredin,asoftsubstrate(‘recliners’ sensu Stanley,1970).Shellsthat reflectthereclininglifehabitarelike Aequipectenopercularis (Linnaeus,1758)(aequipectinoidform),wherethe valvesaremoreequilateralandflaringthanthechlamydoidformandtherightvalvehasashallowbyssalnotch thatpersistslateinontogeny(Figure1.2B).Likeaequipectinoidform,eachvalveinthepectinoidform(asin Pecten Mu ¨ ller,1776, sensustricto)isstronglysymmetricalongtheanterior posterioraxisandishighlyflared alongthedorsal ventralaxis(Figure1.2C).Incontrast,thereisadramaticshapeasymmetrybetweentheleft andrightvalvesnotpresentintheaequipectinoidform,wheretheleftvalveisflatorslightlyconcaveandthe rightvalveisstronglyconvex.Thepectinoidformisassociatedwiththerecessinglifehabit,wherescallopsconstructasaucer-shapeddepressioninsoftsubstratesbydirectingwaterjetsfromitsmantlecavity(Baird,1958; SakuraiandSeto,2000).Speciesofthisformoftenlackabyssalnotchasadults.
Perhapsthemostintriguingscalloplifehabitisgliding(‘swimming’ sensu Stanley,1970).Whileallnon-permanentlyattachedscallopspecieshavetheabilitytoswimtoescapepredators(Himmelmanetal.,2009)orseek favourablehabitat(BuddenbrockandMoller-Racke,1953;HamiltonandKoch,1996),theseactivitiesarenot stronglydependentonshellshape.Glidingisatypeofswimmingbehaviourthatincludes:(i)agreatdistance travelledperswimmingeffort(5 30mpereffort; Brand,2006);(ii)themaintenanceofanear-horizontaltrajectoryabovethesubstrate(Morton,1980;Joll,1989;Anselletal.,1998);and(iii)aglidingcomponent,wherethe animalcontinuestomoveforwardwhilethevalvesareheldclosed(ManuelandDadswell,1993;Chengetal., 1996;Anselletal.,1998).Neitherhorizontaltrajectorynoraglidingcomponentisobservedinscallopsthatswim forshortdistances(Marshetal.,1992;Anselletal.,1998;Donovanetal.,2002).Theglidinglifehabitisassociated withtheamusioidform(asin Amusium Roding,1798, sensustricto).Animalswiththisformhavethin,lightweightshellswithasmoothexteriorandcircularoutlineconducivetoreducingdragandincreasinglift (Figure1.2D).Fromtheside,theshellsareslightlyconvexandcreateagapalongthemarginsventraltotheauriclessothatwatercanbeexpelledduringtheglidingphase(Hayami,1991:Figure1).Bothauriclesaresymmetricalandaregreatlyreducedinsizecomparedtoothershellforms.Specieswithanamusioidformrarelyattach, andassuchtherightvalvehasasmallbyssalnotchorlacksonealltogether.
SinceallfiveshellshapeshaveevolvedinarepetitivefashioninthehistoryofthePectinidae,theydonot denotehigher-leveltaxa.Rather,ithasbeendemonstratedthatshellformsreflectlifehabitratherthanhomologoustraits(Stanley,1970;Alejandrinoetal.,2011;Serbetal.,2011).Thus,theutilityofshellformasthesole basisofanyscallopclassificationsystemisquestionable(Waller,1991,2006a).Indeed,80%oftherecentandfossilspeciesandsubspecieswereoriginallyplacedintoonlyfivegenera, Chlamys, Aequipecten, PectenAmusium,and Hinnites,basedsolelyonshellform.Asaresult,thesefivegenerawererecognisedaspolyphyletic,and
subsequentlyover100genericnameshavebeenintroduced,compoundingthetaxonomicconfusionandinstabilitywithinthefamily(Waller,1991).Thenextsectionprovidesabriefreviewofthetransitionfromusinghighly convergentadultshellformtousingshellmicrosculptureandhingefeaturesinthedevelopmentofaclassificationsystemforthePectinidae.
SHELLMORPHOLOGYANDITSAPPLICATIONINTAXONOMIC CLASSIFICATIONSYSTEMS Theearliestandmostcomprehensivetaxonomictreatmentsofthefamilyarebasedonthemacroscopiccharactersoftheadultshellsorshellform(Thiele,1935;Korobkov,1960;Hertlein,1969;Habe,1977),butoften,these classificationsystemslackcleardiagnosticcharacters(e.g. Thiele,1935; Habe,1977).Forexample, Thiele(1935) hadafoursubfamilyclassificationforthePectinidaedividingitintothePectininae,Amussiinae[=Amusiinae], SpondylinaeandPlicatulinae(thelattertwosubfamiliesarenolongerconsideredscallops(Bieleretal.,2010)). SpecieswereplacedintothePectininaeorAmussiinaebasedonthethickness,coloration,anddegreeofexterior sculptureofthevalves.Forinstance,speciesin Propeamussium, Adamusium,and Amusium,whichpossesssmooth valves,internalribs,and/ortranslucentshells(i.e.theamusioidform)wereplacedintheAmusiinae.Theclassificationof Korobkov(1960) issimilartoThiele’s,butsubdividedThiele’ssubfamiliesintoPectininaeand ChlamydinaeorAmusiinaeandPalliolinae.
Hertlein(1969) wasthefirsttoaddresstheissueofconvergentevolutioninpectinidshellshapewhendevelopinghisclassificationsystem.Aftercomparingextinctandrecenttaxa,hefoundthedatasupported Philippi’s (1853) theoryofiterationandconcludedthatsimilaritiesinshellformusedtodefinesupra-specificgroupsof pectinidsaremostlikelyduetoconvergenceratherthansharedhistory.Assuch, Hertlein(1969) adoptedaconservativeapproachandplacedspeciesinto11supragenericgroupswithoutusingtheformaltaxonomictermof ‘subfamily’,whichwouldimplyrelationship.Sevenofthe11supragenericunits,the Amusium, Chlamys, Decatopecten, Eburneopecten, Hinnites, Lentipecten,and Pecten groupscontainextantspecies,withmostmoderngenerabelongingtothe Chlamys Group(Table1.1). Hertlein(1969) recognisedthatconvergentshellshapewasparticularlyproblematicwhendeterminingtheplacementofamusiidscallopsandotheramusioidformtaxa. Historically,theamusiidshavebeenplacedinthePectinidaewhileothertimesconsideredaseparatefamily(e.g. Ridewood,1903).Takingintoaccountfossiltaxasuchas Amussiopecten,Hertleinfavouredplacingamusiidsback intothePectinidae,althoughhefeltthatthisissuewasnotsatisfactorilyresolved.Bothsmooth-shelledamusiid andpropeamussidtaxaareinthe Amusium Group;however,Hertleinnotesthatthesetaxamayhavebeen derivedfromdifferentancestrallineagesandmaynotrepresentanaturalgroup.
Habe(1977) producedaclassificationsystemof10pectinidsubfamiliesprimarilybasedonrecentJapanese taxa.Animportantcontributionofthisworkwastoelevatethe Camptonectes Grouptothesubfamilylevel. Habe’sCamptonectinaeincludedfourextantgenera(Cyclopecten, Palliolium, Hyalopecten,and Delectopecten),but sincepublication,allbut Delectopecten havebeenmovedtoothersubfamilies(WallerandMarincovich,1992).
Ingeneral,theseearlyclassificationsystemsdidnotincludesoftanatomycharacters(butsee Thiele,1935),as oldermuseumcollectionsprimarilywerecomprisedofdrymaterials.Yet,thedemonstratedmorphologicalplasticity(e.g. Laudienetal.,2003; Culveretal.,2006; Lam,2006)andconvergentevolution(e.g. Stanley,1970,1972, 1975; Serbetal.,2011)ofthebivalveshellcastssomedoubtonthevalidityofclassificationschemesbasedsolely onshapeandsculptureoftheadultshell.
Inanefforttoavoidtheuseofhomoplasiouscharacters, Waller(1986,1991,1993) developedaclassificationof bothextantandextincttaxathatprimarilyfocusedonmicrosculptureofthejuvenileshell,shellmicrostructure (e.g.crystallinecomposition),andhingedentition(Waller,1991:pp.3 9).Unlikepreviousclassificationsofthe Pectinidae,Wallerappliedhispaleontologicalbackgroundtoinferevolutionaryrelationshipsamongpectinid taxabasedonsharedderivedmorphologicalstates(synapomorphies)ofthesetraits.
Waller’searliestphylogenetichypothesiswashis1969paperontheevolutionofthe Argopectengibbus stock,a monophyleticgroupofspeciesfromtheCaribbeanandPanamicprovinces(Waller,1969).Thegoalofthestudy wastoreconstructtheCenozoichistoryof17fossilandlivingtaxa.Todoso,hecollecteddataonmorphology andecologyoflivingspeciesandthenusedpatternsidentifiedinextantspeciestointerpretdatafromthefossil species.Hisdatasetincluded70morphometricmeasurementsofoutline,ligamenture,andmusculatureforover 4100valvesofbothfossilandlivingtaxafrommorethan95localities.Bycombiningbothpaleontologicaland neontologicalinformation,Wallerwasabletodevelopaphylogenetichypothesisthattookintoaccountboth
TABLE1.1 FourModernClassificationSchemesofExtantScallopSpecies
Hertlein,1969,withsomerepresentativegenera Waller(1986,1991,1993,2006) Dijkstra(2004,2014)RainesandPoppe(2006)
CamptonectesGroup (allextinct)
ChlamysGroup
Chlamys
HinnitesGroup
Pedum
Hinnites
LentipectenGroup
Adamussium
EburneopectenGroup
Hemipecten
Palliolum
Delectopecten
Pseudamussium
SubfamilyCamptonectinaeSubfamilyCamptonectinaeSubfamilyCamptonectinae
SubfamilyChlamydinae
TribeChlamydini
TribeCrassadomini
TribeMimachlamydini
SubfamilyPalliolinae
TribeAdamussiini
TribeMesopeplini
TribePalliolini
DecatopectenGroupSubfamilyPectininae
AmusiumGroup Amusium
Propeamussium
PectenGroup
TribeAequipectinini
TribeAmusiini
TribeDecatopectinini
TribePectinini
SubfamilyChlamydinae
TribeChlamydini
TribeCrassadomini
TribeFortipectinini
TribeMimachlamydini
SubfamilyPalliolinae
TribeAdamussiini
TribeMesopeplini
TribePalliolini
SubfamilyHemipectinae
SubfamilyChlamydinae
TribeAdamussiini
TribeAequipectinini
TribeAustrochlamydini
TribeChlamydini
TribeCrassadomini
TribeFortipectinini
TribeMimachlamydini
SubfamilyPalliolinae
TribePalliolini
SubfamilyPectininae
TribeAequipectinini
TribeAmusiini
TribeAustrochlamydini
TribeDecatopectinini
TribePectinini
SubfamilyPedinae
TribePedini
SubfamilyPectininae
TribeDecatopectinini
TribePectinini
morphologicalchangealongalineageandchangethatresultedintheformationofnewlineages(i.e.speciation). Then,byplacingthephylogeneticrelationshipsinthecontextofecological(baysvsopen-marineenvironments) andbiogeographicbarriers,hedevelopedahypothesistoexplainthedifferenceinratesofmorphologicalevolutionandspeciationbetweenthetwobiogeographicprovinces.Basedontheresultingphylogeny,heupdatedthe taxonomicdescriptionsoffossilandextantspeciesexamined.
Subsequently,Wallerbeganexploringtheuseofshellmicrostructureandmicrosculptureascharacterstodefine taxonomicgroupsandtheirrelationships.Hefirstfoundanassociationbetweenmicrostructureandsurfacesculptureoftheshell,wheresurfacesculptureisinhibitedwhentheoutershelllayeriscomposedofprismaticcalcite (Waller,1972b).Thus,thechangeduringshellgrowthfromprismaticcalcitetofoliatecalcitecorrespondswitha changefromasmoothsurfacetothebeginningofradialsculpture.Wallerdeterminedthatthetimingofthis microstructuralshiftmaybeusefulindefiningtaxonomicgroups(Chlamys vs Pecten speciesgroups).Similarly, Wallerdeterminedthatshellmicrosculptureonthesurfaceoffoliatecalcitecouldbeappliedtotaxonomic andphylogeneticstudiesofpectinids.Heusedshellmicrosculpturetodefineanewtribe,theDecatopectinini (Waller,1986)andlaterappliedthesecharacterstatestodevelopphylogenetichypotheses(Waller,1991,1993).
In1991,WallerexaminedthePectinidaeinamoreinclusivemanner.Hedevelopedaphylogenetichypothesis (Figure1.3)basedprimarilyonpre-radialstageshellmicrosculpture.Theresultwasaphylogenetic-basedclassificationsystemthatdividedthePectinidaeintothreesubfamilies(Camptonectinae,Chlamydinae,andPectininae) andtheirrespectivespeciesgroups,manyofthesetaxacorrespondtopreviouslyrecognisedtribes(Waller,1986). ThisstudywasmonumentalasWallerdevelopedaphylogenetichypothesisofthePectinidaethatwastime-calibratedwiththeinclusionoffossiltaxa.Furthermore,hegeneratedspecifichypothesesfortheoriginofthefamily andidentifiedthebasalgroup,theCamptonectinae,asrepresentedbytheextant Delectopecten (‘basal Camptonectinae’hypothesis,see‘Delectopecten astheBasalLineageofthePectinidae’section).Last,foreachspeciesgroupheidentified,Wallerdevelopedspecificevolutionaryhypothesesbasedongeologicalevidence.
While Waller’s1991 paperfocusedoncommercialspecies,hissubsequentpublications(Waller,1993,2006a) providedamorecompleteclassificationschemethathasbeenpartiallyadoptedoramendedbyotherauthors
group
FIGURE1.3 Waller’s1991 phylogenetichypothesisforscallopgroupscontainingcommercialspecies.Phylogenyisplottedagainsttimein millionsofyears(basedon Harlandetal.,1982).Numbersonbranchesrefertomorphologicalcharacterswhichdefineclades:(1)resilium withnon-calicifedcore;(2)ctenolium;(3)earlypre-radialstageofleftdissoconchwithantimarginalgroovesandridgeletsinmicrosculpture, resilial,anddorsalhingeteetharenearlyequallydeveloped;(4)earlypre-radialstageofmicrosculpturemaybesimilarto(1)inbeingpredominatelyantimarginalorpatternmaybeobscuredbyclosed-spacedcommarginallirae;tendencyforreductionofresilialhingeteethwhile dentalpatternbecomesdominatedbydorsal,infradorsal,orsupradorsalteeth;(5)earlypre-radialstageofmicrosculptureofleftvalveis eitherveryfinelypittedorcompletelysmooth,hingedominatedbydorsaland/orintermediateteeth,internalribcarinaebecomesnearlyuniversalinthe Decatopecten and Pecten groups;(6)prismaticstageofrightvalveissecondarilyextendedtoaheightofseveralmillimetres(in contrasttomoreancestralpectinids,whereitislimitedto ,2mm),leftpre-radialstageisgenerallysmooth,rarelyfinelypitted;(7)earlypreradialstageofmicrosculptureofleftvalveisverycoarselypittedandthesepitsarenearlyequidimensionalremnantsofoncecontinuousantimarginalgrooves,hingeteethsimilarto Chlamys group;and(8)earlypre-radialstageofmicrosculptureofleftvalveisverycoarselypitted, hingedentitionbecomesdominatedbyresilialteeth,atleastinearlygrowthstages.
Source:Imagereprintedfrom Waller(1991) withpermission.
(e.g. RainesandPoppe,2006; Dijkstra,2013a).Inhis1993work, Waller(1993) focusedonrelationshipswithinthe Chlamydinae,whichhefurthersubdividedintofourtribes(Chlamydini,Crassadomini,Mimachlamydini,and Aequipectinini).Thispaperalsoincludedtheintroductionoftwonewextanttribes(Crassadomini, Mimachlamydini),threenewextantgenera(Caribachlamys Waller,1993, Laevichlamys Waller,1993 and Spathochlamys Waller,1993),andclearhypothesesfortaxonomicrelationshipsamonglineages,whichhereferred toas‘paraclades’,that‘cannotyetbecharacterizedonthebasisofuniqueapomorphies(=synapomorphies)’ (Waller,1993:p.199).Onemajorcontributionofhis1993workwastodividespeciespossessingthecommon chlamydoidformintodifferenttribes(Chlamydini,Crassadomini,Mimachlamydini),asWallerrecognisedthis shellshapeasplesiomorphic.Later, Waller(2006a) revisedhistaxonomicclassificationmovingthePalliolini fromthePectininae(Waller,1993:Figure1)andelevatedthetribetothesubfamily,Palliolinae(Figure1.4).The Palliolinaewasdividedintofivetribes,threeofwhich(Adamussiini,Mesopeplini,Palliolini)includeextanttaxa
8 1.RECONCILINGMORPHOLOGICALANDMOLECULARAPPROACHESINDEVELOPINGAPHYLOGENYFORTHEPECTINIDAE(MOLLUSCA:BIVALVIA)
FIGURE1.4 Waller’s2006phylogenetichypothesisforthesubfamilyPalliolinae.Dashedlinesindicatemissingfossilrecords.Branches endinginarrowsrepresentextantlineages,thoseendingincross-barsareextincttaxa.Letter-numberlabelsonnodesrefertocharacters describedin(Waller,2006a).Timeinmillionsofyearsfrom Berggrenetal.(1995). Source:Imagereprintedfrom Waller(2006a) withpermission.
fromthegenera Adamussium Thiele,1934, Palliolum Monterosato,1884, Placopecten Verrill,1897,and Pseudamussium Morch,1853.Basedonevidencefrommolecularphylogeneticstudies, Waller(2006a) createdthe tribeAmusiiniandmoved Annachlamys Iredale,1939and Flexopecten Sacco,1897fromtheDecatopectininitothe PectininiandAequipectinini,respectively(Table1.1)(Figure1.5).
Waller’sworkpresentsmanyfirsts.Hewasthefirstworkerinscallopstoroutinelyincorporatefossilandlivingtaxaintophylogenetichypotheses(Waller,1969,1991,2006a).Hewasthefirsttodevelopafamilialclassificationsystembasedonaphylogeny,notsimplybinningmorphologicallysimilarspeciesintogroups(Waller,1991, 2006a).Hewasthefirstresearchertoovercomeadependenceofusinghomoplasiouscharactersinscallopmorphologyandsetouttodevelopasetofcharacterstoavoidissueswithconvergenceintheadultshellshape
FIGURE1.5 Waller’s2006phylogenetic hypothesisforthesubfamilyPectininae. Branchesendinginarrowsrepresentextant lineages,thoseendingincross-barsareextinct taxa.Timeinmillionsofyearsfrom Berggren etal.(1995) Source:Imagereprintedfrom Waller (2006a) withpermission.
(Waller,1972a,b,1986,1991,1993,2006a).AsaresultofWaller’stotalbodyofwork,thePectinidaehasachieved ameasureoftaxonomicstability.
TheclassificationsfromWallerprovidedanoverviewofhowdifferenthighertaxonomicgroupswererelated tooneanotherandlinkedextinctandextanttaxaunderageologictimescale;however,fewspecieswerespecificallyplacedinthissystem. Dijkstra(2004) developedacomprehensivetaxonomicsynopsisofscallopsthat includesallrecognisedpectinidspecies.ThisclassificationisbasedonthescaffoldingofWaller’sclassification system,theworkof Coanetal.(2000) andoverthreedecadesofpublishedworkbyDijkstrahimself(seewebsite forcompletelist, www.scallop.nl).ThemajortaxonomicdifferenceintheDijkstra’sclassificationsystemisthe resurrectionofthreetribes:FortipectininiMasuda1963,AustrochlamydiniJonkers,2003,PediniBronn,1862 (Table1.1).Topublicisehisclassificationsystem,Dijkstradevelopedawebpagesummarisinghispeer-reviewed work.Thefirstiterationwasavailableintheearly2000sasthe‘ScallopCabinet’(Dijkstra,2004)andlater renamedasthe‘World-widelivingscallops’website(Dijkstra,2014).Dijkstra’sbodyofworkhasprimarily focusedonalphataxonomy(e.g. Dijkstra,1986,1988,1989,2008; DijkstraandRoussy,1994; DijkstraandKilburn, 2001)andistheresultofacoordinatedeffortwithlargeresearchexpeditionsorganisedbytheMuse ´ umNational d’HistoireNaturelledeParis(DrPhilippeBouchet)andtheFrenchresearchorganisation,theInstitutde recherche ´ pourlede ´ veloppement(IRD),andcollectionholdingsofDijkstra’shomeinstitution,theNaturalis BiodiversityCenter,Leiden(previouslytheZoologicalMuseum,UniversityofAmsterdam).Thus,muchof Dijkstra’sworkhasfocusedontaxaofthetropicalIndo-PacificOcean.PerhapsofDijkstra’smostimportantcontributiontothestudyofPectinidaeisthathenotonlydescribesnewtaxa,buthepresentsimportantecological information.Hispapersprovidedetaileddescriptionsoflifehabit,associatedsubstrates,andbathymetricalrange togiveahabitatprofileforpectinidspecies(e.g. Dijkstra,2013b).
Mostrecently, RainesandPoppe(2006) compiledabeautifullyphotographediconographyof250speciesin thePectinidae.Theclassificationsystemtheyemployedprimarilyfollowstheoneby Hertlein(1969),butmodifiedbytheworksofDijkstra,Habe,Kafanov,Wagner,andWaller.TheclassificationofRainesandPoppeisthe onlysystemtorecognisethesubfamilyHemipectinae.Inaddition,theirsubfamilyChlamydinaeincludesmore tribesthanothermoderntaxonomictreatments(Table1.1).
Thefourmostcomprehensiveclassificationsystemsof Hertlein(1969), Waller(1986,1991,1993,2006a), Raines andPoppe(2006),and Dijkstra(2014) arecomparedin Table1.1.Differencesamongtheclassificationsystems includewhetherextincttaxaareintegrated(Hertlein,Waller),ifallcurrentlyrecognisedspeciesareincluded (RainesandPoppe,Dijkstra),andiftheauthorgivesahypothesisofhowhighertaxaarerelatedtooneanother (Waller).Thesemodernclassificationsystemshaveinfluencedandsubsequentlyhavebeeninfluencedby(e.g. Waller,2006a)themolecular-basedphylogeneticstudiesdescribedbelow.
THEINFLUENCEOFMOLECULARPHYLOGENETICSONSYSTEMATICS Inmolecularphylogenetics,speciesarerepresentedbynucleotidesequencesthatencodegenes,oraminoacid sequencesthatencodeproteins.Thesedataarealignedascharacterstatesinamatrixandanalysedunderamathematicalmodeldescribingevolutionarychange.Themethodsoftreeestimationincludeavarietyofapproaches andthereisalargebodyofliteratureonthesubject(Hillisetal.,1996;Swoffordetal.,1996;Felsenstein,2004). Currentlyacceptedphylogeneticmethodsutilisesometypeofoptimalitycriterion,whichisameasureoffitof thedata(charactermatrix)toagivenhypothesis(phylogenetictree).Thesemethodsinclude:Maximum Parsimony(MP: Fitch,1971);MaximumLikelihood(ML: Felsenstein,1981);andBayesianInference(BI: Yangand Rannala,1997).MP,ML,andBIarecharacter-basedmethods,wheretheoptimalitycriterionisappliedtoeach position(nucleotideoraminoacid)alongthealignment.Amongthese,MLandBIuseexplicitmodelsof sequenceevolutiontosearchforthebesttree(ML)ortrees(BI)thatareconsistentwithboththemodelanddata. Incontrast,distance-basedmethods,suchasneighbour-joining(SaitouandNei,1987),summarisethemolecular charactermatrixintoadistancematrix,wheresequencesinthealignmentarecomparedinapairwisefashionto calculatethefractionofsimilarity,thenaseriesofalgorithmsareappliedtoconstructasingletree.Theusefulnessofanyofthesemethodsdependsonitsphylogeneticaccuracy,theabilityofamethodtorecoveratopology thatbestfitsthedataathand.Computersimulation(Hall,2005;OgdenandRosenberg,2006),observationalbased(Yang,1996),andexperimentalevolution(Hillisetal.,1994)studieshaveagreedthattheapproachesthat areexplicitlymodel-based(BIandML)aremorephylogeneticallyaccuratethanMPestimates.Distance-based approaches,suchasneighbour-joiningorUPGMA,aretheleastaccurate.Adescriptionofthesimilaritiesand differencesamongtheoptimalitycriteriaandotherapproachescanbefoundin Hall(2008).Itisworthnoting thatphylogeneticinferencemethodsareundercontinualevaluationandre-developmenttoimprovetheaccuracy andspeedofcomputation.
Molecularphylogeneticsisapowerfultoolindevelopingaclassificationsystembecause:(i)molecularmarkers (e.g.genes)canbeselectedthatareindependentofshellmorphologyand,presumably,thesemarkerswillbeless influencedbyconvergentevolutionsothattheresultingtreeisamoreaccuraterepresentationofthedata; (ii)molecularmatriceshavealargenumberofcharactersformorerobustandaccuratephylogenetichypotheses; (iii)molecularcharactershavediscretestates(4nucleotidesor23aminoacids)whicharelesssubjectiveand reduceerrorinstatecalling;and(iv)selectionofappropriateoutgrouptaxacanbeusedtoidentifytheoldest lineageofthestudygroup(i.e.‘ingroup’),totestthemonophylyoftheingroupandtopolarisethehistorical sequenceofallsubsequentevolutionaryevents.Thus,themajorlimitationsinamolecularphylogeneticstudy aretheavailabilityofDNAorRNAsamplesforthetaxaofinterestandthenumberofmolecularmarkersdevelopedforthatparticulargroupoforganisms.
MolecularPhylogeneticStudiesofScallops Earlymolecularphylogeneticstudiesthatincludedpectinidtaxawereinvestigatingrelationshipswithin Bivalvia.ManyofthesestudiesusedDNAsequencefromasinglenuclearlocus,18SrRNA(Riceetal.,1993; KenchingtonandRoddick,1994;SteinerandMuller,1996;Frischeretal.,1998;GiribetandCarranza,1999; SteinerandHammer,2000).Areviewofthesepapersisgivenin Waller(2006a).Primarily,thesestudiesexaminedthephylogeneticplacementofthePectinidaewithintheBivalvia.Becauseofthisbroadtaxonomicfocus,
