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On the Origin of Misophrioid Copepods from Anchialine

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On the Origin of Misophrioid Copepods from Anchialine JanH. Stock Memorial Issue ONTHEORIGIN OF MISOPHRIOID COPEPODS FROM ANCHIALINE CAVES BY GEOFF A.BOXSHALL 1) and DAMIAÁ JAUME2 ) 1)TheNatural History Museum, Cromwell Road, London SW7 5BD,U.K. 2 )InstitutoMediterr aneo de Estudios A vanzados(CSIC-UIB), Ctra. V alldemossa,km 7 0 5, E-07071Palma de Mallorca, Spain ABSTRACT Phylogeneticrelationships between the known genera of the order Misophrioida permit the identi®cation of two lineages: one consisting of the family Misophriidae Brady, 1878 which comprisesseven genera, and a new,monotypicfamily, the Palpophriidae Boxshall & Jaume,1999; theother consisting of anothernew family, the Speleophriidae Boxshall & Jaume,1999, comprising eightgenera. Habitat exploitation by these families is discussed: members of the Misophriidae are primarilyhyperbenthic, those of thePalpophriidae and Speleophriidae are primarily cavernicolous inanchialinehabitats. The occurrence of misophriids in littoraland submarine caves is interpreted asevidence of a relativelyrecent landward extension of the habitat range in this family, from ashallow-waterhyperbenthic ancestor. The distribution of speleophriids in anchialine caves is interpretedas resulting from a colonizationepisode prior to the closure of the Tethys Sea. The analysisalso indicates that deep-water forms may represent a secondarycolonization rather than anindication of deep-water ancestry for the entire order. RESUMEN El estudiode las relaciones ® logeneticas entre los distintos g eneros pertenecientes al orden Misophrioidaha permitido la identi®caci on dedos linajes principales: uno compuesto por la familia MisophriidaeBrady, 1878, integrada por siete g eneros, y unafamilia nueva, Palpophriidae Boxshall &Jaume,1999; el otro, integrado por otra nueva familia, Speleophriidae Boxshall & Jaume,1999, compuestapor ocho g eneros. Se discutela explotaci on que del habitat hacen estas familias: los Misophriidaeson primariamente hiperb enticos, mientras que Palpophriidae y Speleophriidaeson cavernõÂcolasen medio anquialino. La presenciade misofr õÂidosen cuevas litorales y submarinas esinterpretado como evidencia de una relativamente reciente extensi on tierra adentro del h abitat ordinariode esta familia, a partirde un ancestro hiperb entico propio de aguas someras. La distribucion de los espeleofr õÂidosen cuevas anquialinas es interpretada como resultado de un episodiode colonizaci on anterior a laoclusi on del mar de Tetis. El an alisis indica tambi en que lasformas de aguasprofundas representan una colonizaci on secundaria mas que indicaci on de un ancestrode aguas profundas para el orden entero. Ó KoninklijkeBrill NV ,Leiden,1999 Crustaceana 72(8) 958 GEOFFA. BOXSHALL &DAMI AÁ JAUME INTRODUCTION Boxshall(1989) identi® ed two main lineages within the Misophrioida; the Misophria-lineagecomprising Misophria, Benthomisophria , Misophriella , and Misophriopsis , and the Archimisophria -lineagecomprising Palpophria, Dimi- sophria, Speleophria , Expansophria , Boxshallia, and Archimisophria . Both of theselineages had a deep-seahyperbenthic taxon as theirearliest offshoot, Misophriopsis and Archimisophria ,respectively.Boxshall (1989) interpreted theresults of this analysis of the taxa known at that time as evidencethat the misophrioidsinhabiting anchialine caves onoceanic islands belong to lineages thatoriginated in the deep-sea. This con¯ icted with the view of Stock (1986) thata deep-seaorigin of certainanchialine cave taxa on Atlanticislands was un- likelybecause of an anoxic stage in the Middle Tertiary that would have wiped outmuch of the bathyal-abyssal fauna. Thecontinuing discovery of newmisophrioids from anchialine caves, and from hyperbenthichabitats in both shallow, and in deepor highlatitude waters has pro- videda newand broader perspective on themorphological diversity of thisinter- estingorder (see Boxshall& Jaume,1999, and references therein).These recent discoverieshave provided the new data required for a thoroughre-examination of thecontroversial question of whetherthe anchialine cave misophrioids descended fromancestors found in deep water or in shallow water hyperbenthic habitats. Theobjective of this paper is tosummarize the new evidence relevant to this questionby usinga phylogeneticanalysis of thegenera currently comprising the Misophrioida. RESULTS Thetopology presented in ® g.1, extracted from Boxshall & Jaume (1999), was usedas thebasis fora proposeddivision of the Misophrioida into three families.The Misophriidae Brady, 1878 comprises the core Misophria-group of sevengenera and is arelativelyhomogeneous group of mostlyhyperbenthic taxa. Themonotypic Palpophriidae Boxshall & Jaume,1999 is thesister groupof the Misophriidae.The third family, the Speleophriidae Boxshall & Jaume,1999, comprisesthe other lineage identi® ed in the analysis and contains at least seven genera(® g.1). The position of Dimisophria is equivocalbut it was tentatively placedin the Speleophriidae. Substitutinghabitat types for names ofgenera in ® g.1 providesa simple indicationof the main trends in habitat use inthe Misophrioida. The family Misophriidaeis ahyperbenthicgroup, with most of its 12 species occurringin thehyperbenthos over a widerange of depths. The genus Misophriopsis , for MISOPHRIOIDHABITA TUTILIZATION 959 Fig.1. Cladogram depicting inferred phylogenetic relationships between genera of Misophrioida, basedon analysis using P AUP 3.11(Boxshall & Jaume,1999). The major shifts in habitat utilizationare also indicated. example,contains species knownfrom deep oceanic (3000 m) andshallow (8-9m) coastalwaters. A newspecies of Misophriopsis has nowbeen discovered fromCova de na Mitjana on Mallorca and is currentlybeing described by one ofus (D.J.).The discovery of the new species suggestsa directroute by which coastalcave habitats can be colonizedfrom the shallow hyperbenthic. Cova de na Mitjanais nota trueanchialine cave. The cave lake is extremelyclosely linked withthe nearby coastal water as indicatedby the detectable wave action within thecave. The wave action ensures mixingin the cave lake so thewater column is 960 GEOFFA. BOXSHALL &DAMI AÁ JAUME notstrati® ed (with a freshwaterlens overlying deeper, poorly-oxygen atedlay- ers), as intypical anchialine caves. Cova de na Mitjana ® ts thede® nition of a littoralcave: acoastalmarine cave opening below sea level,containing air plus sea waterbut lacking terrestrial in¯ uence. This classi® cationis supportedby the presencein the cave lake of a typicallybenthic marine fauna. The presence of Misophriopsis insuch a caveis unremarkablesince it can be viewedas amere landwardextension from its normal hyperbenthic habitat. Asimilarroute can be hypothesized to explain the presence of Stygomisoph- riakororiensis (Boxshall& Iliffe,1987), the sister taxonof the shallow water hyperbenthicgenus Misophria (® g.1), in South Point Cave, on the island of Koror,Palau. South Point is asubmarinecave (a voidcompletely ® lledwith seawater)in close contact with the coastal waters, as evidencedby thedetectable tidalcurrent, the full or near full salinity, and the range of associated fauna. Theoccurrences of S.kororiensis and the new Misophriopsis species incoastal marinecaves ofthe littoral and submarine types are theresult of independent colonizationevents (® g.1). These two types of marine caves canbe viewedas ecotones,transitional zones between the open sea andtrue anchialine systems, whichhave a markedterrestrial in¯ uence particularly in theform of fresh water input.Misophriids have colonized these ecotones but have not successfully penetratedanchialine systems. Thepresence of members ofthe Misophriidae in such coastal marine caves is anindication of one possible origin of anchialine copepod faunas: bydirect rangeextension from the shallow water hyperbenthos. A similar,but vertical ratherthan landward, range extension has occurredwithin the family in thecase of Benthomisophria .Thetwo species ofthis genus are widelydistributed in oceanicwaters from depths of 2000 to 4000 m butthe greatest concentrations werefound in the hyperbenthic zone just above the sea bed(Boxshall & Roe, 1980).These species are associatedwith the hyperbenthos but exploit a greater partof thebathypelagic water column above it. Thesingle species ofthe Palpophriidae occurs in Jameos delAgua, the clas- sic anchialinesystem onLanzarote. Its startlingsuite of autapomorphies sug- gests thatit represents an ancient and distinct lineage. The sister groupof the Misophriidae-Palpophriidaeclade is theSpeleophriidae (® g.1),which comprises primarilyspecialized anchialine taxa. These relationships could be interpreted as evidencethat the presence of Palpophria inthe anchialine Jameos delAgua representsthe retention of an ancestral habitat association and that the diver- genceof the Misophriidae was linkedto its colonization and to exploitation of thehyperbenthic. W edonot favour that interpretation. MISOPHRIOIDHABITA TUTILIZATION 961 Themembers ofthefamily Speleophriidae are almostexclusively known from anchialinehabitats. The only exception is Archimisophria ,thetwo species of whichinhabit the hyperbenthic community in the deep Atlantic Ocean. The nearestrelatives of Archimisophria thereforeoccur in anchialinehabitats, as also indicatedby the earlier analysis (Boxshall, 1989), however, the topology of thenew cladogram (® g.1) suggests that the deep-water genus Archimisophria descendedfrom ancestors inhabiting anchialine systems inshallowwater, rather thanvice versa. This would appear to support the contention (Stock, 1986) that adeep-waterorigin
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