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The genus Opisthacanthus Peters, 1861 (Scorpiones:
Hormuridae), a remarkable Gondwanian group of scorpions
Wilson Lourenço, Lucienne Wilmé, Patrick Waeber
To cite this version:
Wilson Lourenço, Lucienne Wilmé, Patrick Waeber. The genus Opisthacanthus Peters, 1861 (Scor-
piones: Hormuridae), a remarkable Gondwanian group of scorpions. Comptes Rendus Biologies,
Elsevier, 2018, 341 (2), pp.131-143. �10.1016/j.crvi.2017.12.003�. �hal-01741937�
The genus Opisthacanthus Peters, 1861 (Scorpiones:
Hormuridae), a remarkable Gondwanian group of scorpions
Le genre Opisthacanthus Peters (Scorpiones : Hormuridae), un remarquable groupe de scorpions gondwaniens
Wilson R. Lourenc ¸o
a,*, Lucienne Wilme´
b,c, Patrick O. Waeber
daMuse´umnationald’histoirenaturelle,Sorbonneuniversite´s,institutdesyste´matique,e´volution,biodiversite´ (ISYEB),UMR7205CNRS, MNHN,UPMC,EPHE,CP53,57,rueCuvier,75005Paris,France
bMissouriBotanicalGarden,MadagascarResearch&ConservationProgram,BP3391,Antananarivo101,Madagascar
cWorldResourcesInstitute,Washington,D.C.,UnitedStates
dForestManagementandDevelopment,DepartmentofEnvironmentalSciences,SwissFederalInstituteofTechnology,8092Zurich, Switzerland
Keywords:
Scorpion Opisthacanthus Madagascar Gondwanianmodel Centreoforigin Newspecies
ABSTRACT
NewcommentsareproposedonthegeographicdistributionofgenusOpisthacanthus,and theGondwanianmodelisfurthersupported.Thediversityofthegenusisextraordinaryin Madagascar,withthesamenumberofspeciesasincontinentalAfrica,butsub-Saharan AfricaishometosixoutoftheninegroupscurrentlyrecognizedofOpisthacanthus.Given theaffinitiesoftheOpisthacanthusgroupsandtheircurrentdistribution,acenteroforigin inAfricacouldbefavoredfortheseancientscorpions.TheproposedGondwanamodel suggeststhattheMadagascarOpisthacanthusareclosertothoseoftheNewWorld,which isconsistentwiththeaffinitiesobservedinmorphologicalcharacters.A newspecies, Opisthacanthustitanussp.n.,isdescribedfromtheTorotorofotsyForest,locatedinEastern Madagascar.ThenewspeciesshowsaffinitieswithbothOpisthacanthusmadagascariensis Kraepelin, 1894 known from dry regions in the western portion of the island and OpisthacanthuslavasoaLourenc¸o,Wilme´ &Waeber,2016onlyknownfromtheextreme southeastoftheisland.ThenewspeciesandO.madagascariensishavesimilarexternal morphologies but the morphometric values are markedly distinct. Moreover, O.madagascariensisisexclusively foundinspinyforestthicketsandopenwoodlands, whereasthenewspecieswasfoundinthehumidforestofTorotorofotsy.Thetotalnumber ofspeciesinMadagascaris nowraisedto twelve.Biogeographicalscenarios arealso proposedtoinfertheoriginoftheOpisthacanthusandbetterunderstanditsdistributionin theNewWorld,inAfricaandMadagascar.
* Correspondingauthor.
E-mailaddresses:wilson.lourenco@mnhn.fr(W.R.Lourenc¸o),lucienne.wilme@mobot-mg.org(L.Wilme´),patrick.waeber@usys.ethz.ch(P.O.Waeber).
1. Introduction
Asalreadydiscussedinseveralpreviouspublications, thetaxonomichistoryrelatedtothegenusOpisthacanthus Peters,1861israthercomplex[1,2].Thegenuswascreated byPeters[3],basedonthespeciesIschnuruselatusGervais, 1844[=Opisthacanthuselatus (Gervais, 1844)],a species distributedfromColombiatoPanama.Subsequently,the discovery in Africa of species with morphology closely relatedtoO.elatusledsomeauthorstoaccepttheexistence ofthisgenusonbothcontinents.Bytheendofthe19th century, the notion of Gondwanian groups was yet inexistentandconsequentlythismodelofdiscontinuous distributionappeareddifficulttoexplainbythattime.This complexsituationledPocock[4],inanewclassificationof scorpion,toproposea newgenusOpisthocentrusforthe Africanspecies,whereasOpisthacanthusremainedassoci- atedexclusivelywiththeNeotropicalspecies.Neverthe- less,inthefollowingyearsPocockhimselftookdifferent decisions and first placed both American and African speciesunderOpisthacanthus[5,6],butafewyearslaterhe splitthespeciesofthetwocontinentsagainintwogenera [7]. Other authors such as Kraepelin [8] considered OpisthocentrusasasynonymofOpisthacanthus,aposition followedbyseveralauthors[9,10].
Duringthe1970sthequestionaroundtheissueofone ortwogeneraassociatedwithOpisthacanthuswasraised again by two authors: Newlands [11,12] and Francke [13].Newlands[11,12]suggestedtheexistenceofasingle genus,Opisthacanthusovertwocontinents(Americaand Africa),butrejectedanyhypothesisaboutaGondwanian distribution;basedonthetheoryof‘‘transoceanicrafting on driftwood’’, asdefinedby Darlington [14], Newlands [11,12]proposedthehypothesisofrecentdispersionfrom
AfricatoAmerica.Tothecontrary,Francke[13]rejected the idea of a single genus over two continents and revalidated the genus Opisthocentrus. However, since Opisthocentrus was already occupied by a fish genus, Opisthocentrus Kner, 1868 (Actinopterygii:Pholidae), he introduceda newreplacementnameNepabellusFrancke, 1974fortheAfricanspecies.
The arguments suggested both by Newlands [11,12]
andFrancke[13]wereentirelyrejectedbyLourenc¸o[1,2], andasinglegenusOpisthacanthuswasdefinedforallthe American and African species, based on a Gondwanian modelofdistribution(cf.Lourenc¸o[1,2]forfurtherdetails).
Itisimportanttonotethatintheirdifferentanalysisduring the1970s,authorssuchasNewlands[11,12]andFrancke [13] totally ignored the existence of the Malagasy species Opisthacanthus madagascariensis described by Kraepelin, 1894 and the fact that this last species presents more morphological traits in common with American than African species. At the time of their analysis, O. madagascariensis was the only species de- scribedinthegenus.Subsequently,in1995,Lourenc¸o[15]
confirmed the model of a single Gondwanian genus, Opisthacanthus,butwithtwosubgeneraOpisthacanthusfor the American species including also one species from Occidental Africa, Opisthacanthus lecomtei (Lucas, 1858) andNepabellusFrancke,1974fortheotherAfricanspecies.
The evergrowing knowledge on theMalagasy scorpion fauna[16]ledtothecreationofathirdsubgenusforthe MalagasyspeciesofOpisthacanthus:Monodopisthacanthus Lourenc¸o,2001[17].
One important question can however be addressed concerning the real phylogenetic affinities of the three different lineages defined at present. One group, Opis- thacanthus, is clearly defined for the American species, RE´ SUM E´
Une nouvelle re´flexion est propose´e sur la re´partition ge´ographique du genre Opisthacanthusaveclapropositiond’unmode`legondwanien.Ladiversite´ dugenreest extraordinairea` Madagascar,avecunnombred’espe`cesquie´galceluidel’Afrique,mais l’Afrique sub-saharienne abrite six des neuf groupes actuellement reconnus d’Opisthacanthus. Compte tenu des affinite´s des groupes d’Opisthacanthus et leur re´partition actuelle, un centre d’origine en Afrique pourrait eˆtre favorise´ pour ces scorpions anciens.Le mode`legondwanienpropose´ sugge`requelesOpisthacanthus de MadagascarsontplusprochesdeceuxduNouveauMonde,cequiestcohe´rentavecles affinite´s observe´es a` partir des caracte`res morphologiques. Unenouvelle espe`ce est de´crite, Opisthacanthus titanus sp. n.,connue de la foreˆt de Torotorofotsy,a` l’est de Madagascar.Lanouvelleespe`cemontredesaffinite´savecOpisthacanthusmadagascariensis Kraepelin,1894connudesre´gionsse`chesdel’Ouestdel’ıˆleetOpisthacanthuslavasoa Lourenc¸o,Wilme´ &Waeber,2016,quin’estconnuquedel’extreˆmeSud-Estdel’ıˆle.La nouvelleespe`ceetO.madagascariensisontdesmorphologiesexternessimilaires,mais leursvaleursmorphome´triquessontnettementdistinctes.Deplus,O.madagascariensisse trouveexclusivementdanslesfourre´se´pineuxetlesformationsarbore´esouvertes,tandis quelanouvelleespe`ceprovientdelaforeˆthumidedeTorotorofotsy.Lenombretotal d’espe`cesa` Madagascarestmaintenantporte´ a` douze.Dessce´nariosbioge´ographiques sontpropose´spourappre´henderl’originedesOpisthacanthusetmieuxcomprendreleur distributiondansleNouveauMonde,enAfriqueeta` Madagascar.
Motscle´s:
Scorpion Opisthacanthus Madagascar Mode`legondwanien Centred’origine Nouvelleespe`ce
withhoweveronespeciesinOccidentalAfrica.Therestof the African species, placed in the subgenus Nepabellus, constitute a rather homogeneous group. Finally, Mono- dopisthacanthus has some particularities isolating the group in Madagascar. Back to the original diagnosis proposedbyPocock[4]andFrancke[13]forOpisthocentrus and Nepabellus,it canbeobservedthatfor anumber of morphological characters, size of the excision on the anterior border of carapace, size and shape of genital operculum,inparticularthoseoffemales,morphologyof pectines,andsizeandmorphologyoftheanteriortubercle of pedipalp patella, two species couldnot beclassified amongtheotherAfricanspecies:Opisthacanthuslecomtei and Opisthacanthus madagascariensis. The discoveries of numerousnewspeciesbothinMadagascarbutalsointhe Neotropicalregionbroughtconfirmationtotheobserved morphological traits of both American and Malagasy species [18,19].Based on the characterslistedabove, it can be suggested that the species of the subgenus Opisthacanthusshowagreateraffinitywiththoseofthe subgenusMonodopisthacanthus.Themorphologicaltraits observedforthesetwogroupsappearaslessprimitivein relationtothoseofthesubgenusNepabellus,inparticularif comparedtothesingleknownfossilrecordwhichcanbe associatedwithelementsofOpisthacanthus:Protoischnurus axelrodorumCarvalho&Lourenc¸o,2001(familyProtoisch- nuridae)fromCretaceousSantanaFormationfromCrato areainBrazil[20](Fig.1).
The present study of new samples of hormurid scorpions of the genusOpisthacanthus, subgenus Mono-
dopisthacanthus from Madagascar, has resulted in the discoveryofonenewspecies.Thesewerecollectedfrom theEastoftheIsland,intheTorotorofotsyForest(dense humidforest), andare inpartrelated toOpisthacanthus madagascariensisKraepelin,1894whichisknownfromthe westernportionoftheislandandOpisthacanthuslavasoa Lourenc¸o, Wilme´ & Waeber, 2016 only known from the extreme southeast of the island. Nevertheless, O. madagascariensis is exclusively foundin spiny forest thickets and grassland formations. Comments are pro- posedonthegeographicdistributionandecologyofthe Malagasy species of Opisthacanthus. Given the global distributionofthisancientgroupofscorpions,thispaper explorespotentialscenariosoforiginanddistribution.
2. Methods
Illustrationsand measurements weremadewiththe aid of a Wild M5 stereo-microscope equipped with a drawingtube(cameralucida)andanocularmicrometer.
MeasurementsfollowStahnke[21]andaregiveninmm.
TrichobothrialnotationsfollowVachon[22]andmorpho- logicalterminologymostlyfollowsHjelle[23].
3. Thepresentcompositionofthe genusOpisthacanthus
Theclassificationgiven belowtakesintoaccountthe most recent taxonomic modifications proposed for the genus[18,19,24,25].Sincemosthistoricalaspectsconcern- ingMalagasyspeciesofOpisthacanthushavealreadybeen presentedinpreviouspublications[19,24–27],thesewill notbefurtherdiscussedhere.
SubgenusOpisthacanthusPeters,1861.
1.cayaporumgroup
OpisthacanthuscayaporumVellard,1932.
OpisthacanthusheurtaultaeLourenc¸o,1980.
OpisthacanthussurinamensisLourenc¸o,2017.
OpisthacanthusweyrauchiMello-Leita˜o,1948.
2.lepturusgroup
OpisthacanthusautanensisGonza´lez-Sponga,2006.
OpisthacanthusborboremaiLourenc¸o&Fe´,2003.
Opisthacanthus brevicauda Rojas-Runjaic, Borges &
Armas,2008.
Opisthacanthuselatus(Gervais,1844).
Opisthacanthuslepturus(Beauvois,1805).
OpisthacanthusvalerioiLourenc¸o,1980.
3.lecomteigroup
Opisthacanthuslecomtei(Lucas,1858).
SubgenusNepabellusFrancke,1974.
4.africanusgroup
OpisthacanthusafricanusafricanusSimon,1876.
OpisthacanthusafricanuspallidusLourenc¸o,2003.
OpisthacanthuscapensisThorell,1876.
Opisthacanthusdiremptus(Karsch,1879).
5.aspergroup
Opisthacanthusasper(Peters,1861).
OpisthacanthusbasutusLawrence,1955.
OpisthacanthusrugicepsPocock,1897.
6.laevipesgroup
Opisthacanthuslaevipes(Pocock,1893).
Fig. 1.Current knowndistributionofthegroupsofOpisthacanthusin Central and South-America, sub-Saharan Africa andMadagascar. (the groups are numberedfrom 1 to 9 as following: 1: O. cayaporum+ O. heurtaultae+O. surinamensis+O. weyrauchi; 2: O. autanensis + O. borboremai+O. brevicauda+O. elatus+O. lepturus+ O. valerioi; 3:
O.lecomtei;4:O.africanus+O.capensis+O.diremptus;5:O.asper+O.
basutus+O. rugiceps; 6: O. laevipes; 7: O. lamorali+O. rugulosus; 8:
O.validus+O.piscatorius;9:O.ambanja+O.andohahela+O.antsiranana+ O. darainensis+ O. lavasoa+O. lucienneae+ O. maculatus+ O.madagascariensis+O.milloti+O.pauliani+O.piceus+O.titanussp.;the crossmarksthetypelocalityoftheCretaceousProtoischnurusaxelrodorum).
7.rugulosusgroup
OpisthacanthuslamoraliLourenc¸o,1981.
OpisthacanthusrugulosusPocock,1896.
8.validusgroup
OpisthacanthuspiscatoriusLawrence,1955.
OpisthacanthusvalidusThorell,1876.
SubgenusMonodopisthacanthusLourenc¸o,2001.
9.madagascariensisgroup
OpisthacanthusambanjaLourenc¸o,2014.
OpisthacanthusandohahelaLourenc¸o,2014.
OpisthacanthusantsirananaLourenc¸o,2014.
OpisthacanthusdarainensisLourenc¸o&Goodman,2006.
Opisthacanthus lavasoa Lourenc¸o, Wilme´ & Waeber, 2016.
OpisthacanthuslucienneaeLourenc¸o&Goodman,2006.
OpisthacanthusmaculatusLourenc¸o&Goodman,2006.
OpisthacanthusmadagascariensisKraepelin,1894.
OpisthacanthusmillotiLourenc¸o&Goodman,2008.
OpisthacanthuspaulianiLourenc¸o&Goodman,2008.
OpisthacanthuspiceusLourenc¸o&Goodman,2006.
Opisthacanthustitanussp.n.
The genus Opisthacanthusis currently distributed in Madagascar, sub-Saharan Africa, and the Caribbean, CentralandSouthAmerica(Fig.1).Therangeofthegenus inAfricaisalmost7.5millionkm2,itisca.3.5millionkm2 in the New World, and less than 0.45 million km2 in Madagascar.Despiteitssmallsize,Madagascarishometo 12species,asmuchasAfrica,butAfricashowsthehighest diversityofgroups,withasmanyas6groupsVS.onegroup in Madagascar, andonly two groupsin theNew World (Fig.2).Thefossilmaterialforthesegroupsislimitedtoa single specimen collected in the Cretaceous of Brazil (Fig.1)[20].
4. Taxonomictreatment
FamilyHormuridaeLaurie,1896.
GenusOpisthacanthusPeters,1861.
Fig.2. Distributionofthe34knownspeciesofOpisthacanthusinninegroups(colorpatternasinFig.1).
SubgenusMonodopisthacanthusLourenc¸o,2001.
Opisthacanthus (Monodopisthacanthus) titanus sp. n.
(Figs.3–7).
Madagascar, ex-Province of Toamasina, Region of Alaotra-Mangoro, District of Moramanga, Torotorofotsy
Forest (dense humid forest), 1020m, XI/1974 (J.- M.Betsch–RCP-225):1maleholotype,1femaleparatype (MNHN)(Fig.8).
Etymology: The specific name derives from the mythological Titans and conveys the idea of giant, powerful.
Diagnosis: Scorpions of large size: male and female with respectively 96.6 and 88.0mm in total length.
Colorationreddishtoreddish-brown,withblackishzones overcarinaeandsomedarkvariegatedzonesonchelicerae.
Pectines with 8–8 teeth in male and 8–7 in female.
Fig.3. Opisthacanthus(Monodopisthacanthus)titanussp.n.A–B.Maleholotype.C–D.Femaleparatype,dorsalandventralaspects.Hemispermatophoreis highlightednearbythemaleholotype.
Fig.4. Opisthacanthus(Monodopisthacanthus)titanussp.n.Maleholotype.
A.Hemispermatophore,lateralaspect.B-C.Chelicera,dorsalaspectwith teethindetail.D.Cuttingedgeofmovablefinger,showingthetwoseries ofgranulations.
Fig.5.Opisthacanthus(Monodopisthacanthus)titanussp.n.Metasomal segment V and telson, lateral aspect. A. Male holotype. B. Female paratype.
Hemispermatophoremoderatelyslenderwithanelongat- eddistallamina,moderatelyenlarged.Genitaloperculum inmaleformedbytwosemi-ovaltoroundplates,witha minuteincisioninthebase;infemalewithamoreorless hexagonal shape. Trichobothrial pattern of type C, orthobothriotaxy.
Descriptionbasedonholotypeandparatype.
Coloration. Basically reddish to reddish-brown with blackish zones over carinae and some dark variegated zonesonchelicerae.Carapacereddish-brown;medianand lateral eyes surrounded with black pigment. Tergites reddish-brown. Metasomal segments reddish-brown to
darkbrown;vesiclereddishwithareddish-brownlateral strip;aculeusdarkreddishtoblackish.Cheliceraereddish- brown; base of fingers darker; the whole surface with diffuse variegated spots; fingers yellowish-brown with darkredteeth.Pedipalpsreddishtoreddish-brown;most carinaeblackish;chelafingersreddish-browntoblackish.
Venterandsternitesreddish-yellow;pectinesandgenital operculumyellow,muchpalerthansternites,sternumand coxapophysisreddish;legsreddishtoreddish-yellow.
Morphology.Carapacewithsomegranulations,better marked on female; male withpunctuation and smooth zones;furrowsmoderatelyshallow.Anteriormarginwith Fig.6. Opisthacanthus(Monodopisthacanthus)titanussp.n.Maleholotype.Trichobothrialpattern.A–C.Chela,dorso-external,ventralandexternalaspects.
astrongconcavityreachingasfarasthelevelofthe2nd lateraleye.Medianoculartubercleflattenedandalmostin thecenterofthecarapace;medianeyesmoderatetosmall, separated by one ocular diameter; three pairs of large lateraleyes.Sternumpentagonal,widerthanlong.Genital operculum formedbytwo semi-oval toround plates in male,withaminuteincisioninthebase;withamoreor
lesshexagonalshapeinfemale.Tergiteswithamoderate toweak median carina,smooth and withpunctuations.
Pectinaltoothcount8–8inmaleholotype(8–7infemale paratype).Sternitessmoothandshiny;VIIacarinatewith veryfewpunctuations.MetasomalsegmentsItoVlonger than wide, with some thin but intense granulations in female and mainly punctuations in male. All carinae Fig.7.Opisthacanthus(Monodopisthacanthus)titanussp.n.Maleholotypeandfemaleparatype.Trichobothrialpattern.A–B.Femur,dorsalaspect(maleand female).C–E.Patella,dorsal,externalandventralaspects(male).
moderatelymarkedinsegmentsI-IV;segmentVrounded withsomeweakspinoidgranulesontheventralsurface.
Allsegmentswithmoderatechetotaxy.Telsonwithapear- likeshape; smooth and covered with strong chetotaxy.
Pedipalps: femur with dorsal internal, dorsal external, ventral internal and ventral external carinae strong, tuberculate; dorsal face with thin granulation; ventral face withminute granulation; internal face moderately granulose better marked on female. Patella with internalandexternalfacesmoderatelygranulated;dorsal and ventral faces weak to moderately granulated;
dorsal internal, ventral internal, ventral external and externalcarinaestrong;othercarinaeless wellmarked.
Chelamoderatelytostronglygranularexceptedonventral face;dorsalmarginal,externalsecondary,ventrointernal and ventral median carina strong; other carinae less well marked. Chelicerae typical of Scorpionoidea [28];
teethstronglysharp.TrichobothriotaxytypeC;orthobo- thriotaxic[22].Legs:tarsiwithtwolateralrowsofspines, surrounded byafew longsetae.Spursmoderate.Hemi- spermatophoremoderatelyslenderwithanelongatedand bi-lobateddistallamina,weaklyenlarged.
Relationships:Thenewspeciesseemstobeassociated withOpisthacanthusmadagascariensisandwithO.lavasoa but can be distinguished from these two species by a numberofcharacters:
biggerglobalsize;
quitedistinctmorphometricvalues,and;
hemispermatophore with a distinct morphology–
slender compared to that of O. madagascariensis [26]
andwithabi-lobatedistallamina.
Itshouldbenotedthatthetypesofforestsin which O. madagascariensis and O. lavasoa are encountered include subhumid forests according to Moat & Smith [29]inthesubhumidbioclimateaccordingtoCornet[30], andthetypelocalityofthenewspeciesisattheedgeofthe humidbioclimateontheeasternhumidbeltoftheisland (Fig.8).
Morphometric values (inmm) of male holotype and femaleparatype.Totallength(includingtelson)96.6/88.0.
Carapace: length 15.5/13.4; anterior width 10.7/8.7;
posterior width 15.7/13.2. Mesosoma length 31.8/35.6.
Metasomal segment I: length 5.8/4.5, width 3.6/3.8; II:
length6.8/5.3,width2.9/3.3;III:length7.2/5.7,width2.6/
2.9;IV:length8.0/6.3,width2.3/2.6;V:length10.2/8.4, width 2.3/2.5, depth 3.2/2.9. Telson length 11.3/8.8.
Vesicle: width 3.3/2.5, depth 4.2/3.2. Pedipalp: femur length24.7/11.4,width6.4/5.4;patellalength21.6/12.2, width6.1/5.9;chelalength42.6/24.4,width7.8/8.8,depth 8.4/10.2;movablefingerlength16.4/12.9.
Reports: Male totallength96.6/Pedipalp span177.8.
Femaletotallength88.0/Pedipalpspan96.0.
5. BiogeographicconsiderationsforthenewMadagascar species
TheMadagascarOpisthacanthusbelongtoasinglegroup andareextremelydiversifiedatthespecieslevel.Thisis not unusual in the global Malagasy faunal and floral context,i.e.highspeciesdiversityandendemism,andalso inthescorpioncontext.
Lourenc¸oandcolleagues[19]detailedthebiogeography of thesubgenus Monodopisthacanthusatthetimeofthe description of Opisthacanthus (Monodopisthacanthus) lavasoa. The 12th Madagascar species O. titanus sp. n.
described hasseveral characteristicsoutlined earlierfor severalspeciesofMadagascarscorpions:
thespeciesbelongstoanoldbradytelicgroupwithslow evolution,sensuLourenc¸oetal.[19]);
the species is known from a mountain located in the rainshadow on the leeward side of the humid Betsimisaraka mountains, therefore experiencing a localclimatewithlowerrainfallascompared tomost humidforestsfoundalongtheEasternbeltoftheisland [31–34];
Fig.8.Distributionofthe12species ofOpisthacanthusinMadagascar accordingtothesimplifiedbioclimatesproposedbyCornetin1974[30].
(yellowtodarkorangeforhumid,subhumid,drytosubarid;thedarkspot forTorotorofotsy,thetypelocalityofOpisthacanthustitanussp.n.Other speciesofOpisthacanthusasfollow:a:O.ambanja;b=O.andohahela;c:
O. antsiranana; d: O. darainensis; e: O. lavasoa; f: O. lucienneae; g:
O.maculatus;h:O.madagascariensis;i:O.milloti;j:O.pauliani;k:O.piceus).
thespeciesisknownfromalocalitysharingbioclimate aspectswithlocalitieswhereO.ambanja,O.andohahela, O.lavasoa,andO.piceushavebeencollected,i.e.inthe subhumidbioclimateasdefinedbyCornet[30](Fig.8).
Opisthacanthus madagascariensis as it is currently circumscribed, is distributed in the subarid and dry bioclimates,and inpockets ofsubhumidclimate.Inthe drybioclimate,thespecieshasbeencollectedinthetsingy ofNamoroka,andthetsingyofBemarahawheresubhumid forestsoccurinthecanyons[29].
Lourenc¸oet al.[19]looked attheclimaticcontextof Madagascar since theCretaceous–Paleogene (K–Pg) and proposedthatfollowingtheK–Pgmassextinctionatthe endoftheCretaceoussome66Ma,andduringtheearly Paleogene, the ancestral Monodopisthacanthus was as- sumed present in Madagascar and survived the K–Pg.
Madagascar waslocated at some7 to8 degrees tothe southofitscurrentposition(itssoutherntipat32.98Svs.
current25.68S;itsnortherntipat20.18Svs.current12.08S [35]. During the Paleocene (66.0–56.0Ma), Madagascar wasisolatedfromAfricaandIndia;theSouth-Indiandrift was affecting the eastern coast of Madagascar which increasedtherainfall,andNorthernMadagascarentered themonsoonbelt.AttheendofthePaleocene(56.0Ma),a major global increase in temperature occurred, the Paleocene–Eocene thermal maximum (PETM), which lastedsome200,000years[36].OnlybythemidOligocene,
29Ma,hasMadagascarcompleteditsdriftoutofthearid belt and entered completely the trade wind regime [35,37,38]andreferencestherein(Fig.9).
Atthetimeof thePETM, theancestralpopulationof O.madagascariensisandO.titanussp.n.wouldhavebeen able tocope withdry conditionsbut would have been extirpatedfromthedriestregionsoftheisland,orcould havesurvivedinsomerefugiaoftheseregions[39].Atthe timeofthePETM,SouthernMadagascarwasstillinthearid beltandthustheconditionstofindhumidrefugiawere reduced.
Adaptation to dry conditions of the Madagascar Monodopisthacanthus lineage can be inferred from a combinationof thefollowing:itscurrentdistributionin thedrybiomeofwesternandsouthernMadagascar(Fig.8), the wide range of O. madagascariensis in western and southernMadagascar,andtheancientageofthegroupin Madagascarwhentheclimatewasalotwarmeranddrier duringthePaleogene.Atthetime,acommonancestorof O.madagascariensisandO.titanussp.n.isassumedtohave beendistributedovertheeasternbeltoftheislandwhich was likely covered with sometypes of dry forests and thickets [35].At thesame time, somepopulations may havebeenabletocopewithincreaseddrought,atleastin somerefugiaofwesternandsouthernMadagascar.
Lourenc¸o et al. [19] proposed that the ancestral Monodopisthacanthus populations adapted to the dry conditions during the Paleocene in eastern Madagascar
Fig.9.BreakupofGondwanaandchangingpalaeoclimateduringtheCenozoicaftertheK–Pgmassextinction.(modifiedfrom[19,46]);Af:Africa;Am:
SouthAmerica;M:Madagascar.
(Fig.9),butcouldhavedisappearedfromtheeasternbeltof the island when Madagascar entered the trade wind regimewithincreasedhumidityalongthisportionofthe island.Somepopulationscouldhavesurvivedatthelimit ofthenewrainforest beltwhere humiditywaslimited.
Several species in the genus Opisthacanthus seem to reflect this scenario, as O. andohahela and O. piceus occurringinthehumidsubtropicalforestofAndohahela, O.madagascariensisinthesubhumidforestsoccurringin thewestern tsingyformationsasencounteredinNamo- roka,orBemaraha,O.paulianiinthesubhumidforestsof Ankarana, and finally O. titanus sp. n. in the forest of Torotorofotsy in the rainshadow of the Betsimisaraka mountains(Fig.8).
ThecurrentdistributionofthegroupsofOpisthacanthus and the affinities of the genus with the Cretaceous ProtoischnurusaxelrodoruminBrazildatebacktodistant times in a Gondwana model. The origins are thus considered during the Jurassic (201 Ma–145 Ma) and LowerCretaceous(145Ma–100Ma)whenthesouthern continentallandmasseswerestillconnected.
6. FurthersupportfortheGondwanianmodel
Afterevolutionoftherespectivepopulationsofances- tral Opisthacanthus on the isolated landmasses, the resultinglineageswiththemostaffinitieswouldbethose thatwouldhavebeenincontactinthemostrecenttimes.
At the end of the Cretaceous, Antarctica, Africa and Madagascarwereisolatedfromeachother;SouthAmerica was still connected with Antarctica, Madagascar was within the 30-degree subtropical arid belt [35] and peninsularIndiawasdetachedfromMadagascar.Penin- sularIndiadidonlycollidewithAsiaduringtheEocene, betweenca.54and40Ma[40,41].Weinferthatancestral Opisthacanthus survived the K–Pg at least in Africa, MadagascarandSouthAmerica.Vicariancewilltakeplace during the following Cenozoic characterized by the breakup and changing palaeo-climate of Gondwana, at leastduringtheOligocenebetween30Maand28Mawhen thesouthernlandmasseswhereisolated(Fig.9).Tobetter understandtheextantdistributionofOpisthacanthus,we useascenarioapproachtohighlightpossiblebranchingof sisterclades.
6.1. TheGondwanabreakup
DuringtheJurassicMadagascarhasdriftedawayAfrica and Africa has drifted away Antarctica, while South AmericawasstillconnectedtobothAfricaandAntarctica.
Indo-Madagascar started rifting away Africa during the lower Jurassic 182 million years ago (Ma), as early as 206Ma[42]toaslateas160Ma[43].Atthesametime, AfricastartedriftingawayAntarcticacontiguouslybutata lowerstartingvelocityontheothersideoftheGondwana.
AlandrouteofdispersalstillexistedbetweenAntarctica and Indo-Madagascar (via the Kerguelen plateau), Antarctica and South America, Southern Africa and southernSouthAmerica,andWesternandCentralAfrica andnorthernSouthAmerica(Fig.10). Micro-continental blocks bridged Southern South America and Antarctica
untiltheLowerCretaceous[145–100Ma],includingTierra delFuego,SouthGeorgia,andSouthOrkney[44].Through theJurassicandduringtheLowerCretaceous170–120Ma, Southern Africa was disconnectedfrom southern South America,whileIndo-Madagascar’s positiondifferedwith relationtoAntarctica(Fig.10).Thecessationoftherifting between Madagascar and Africa occurred at 120 Ma [43].AtthetimeoftheMiddleAptianatca.120Ma,the connections between Indo-Madagascar and Antarctica werelimitedtoasmallfractionoftheKerguelenplateau thatemerged[45,46].Continuouslandbetweenterminal southernSouth-AmericaandtheAntarcticpeninsulawas maintained from the Upper Cretaceous [100–66 Ma]
through Eocene [56–34 Ma] [47], and possibly until 30Ma[48].
6.2. Scenariosoforigin
WeproposevicarianteventsduringtheMesozoicwith severalscenariosoforiginsoftheancestralpopulationsin theGondwana,whicharebasedontheslowevolutionof scorpionsingeneral,theancestralityofthemembersofthe familyHormuridaeinparticular,andthecurrentdistribu- tionofthegenusOpisthacanthus.Weinferthephylogenyof theresultingpopulationsintheisolatedlandmassesafter the breakup of the Gondwana. Cenozoic over-water dispersalisnotconsideredinthescenariosproposed.
Scenario1:Madagascarorigin
Antarctica is bridging Africa, South America and Madagascar;aslongasSouthernAfricawasstillconnected tosouthernSouthAmerica,anancestralIndo-Madagascar orMadagascarOpisthacanthus(I-M0)couldhavedispersed clockwise from Indo-Madagascar towards Antarctica, SouthAmerica,andfromSouthAmericatowardsSouthern Africa, or Western or Central Africa (Fig. 10). In this scenario,theAmericangroupsaremorecloselyrelatedto theAfricangroups,andtheMadagascargrouphasmore affinitieswiththeAmericangroupsthanwiththeAfrican groups.However,thesplitwouldhaveoccurredduringthe Cretaceous(Fig.10).ThescenariowithaMadagascarorigin would imply that the youngest Opisthacanthus would occurinAfrica,andthelatestsplitbetweenthelineages would have occurred between theSouth American and Africanlineages.TheMadagascarlineagewouldshowthe leastaffinitieswiththetwootherlineages.Thepresenceof a single group of Opisthacanthus in Madagascar can be explainedbythesmallsizeoftheislandascomparedto Africa,but thelowgroupdiversityintheNewWorldas compared to thehigh groupdiversity observed in sub- SaharanAfricaseemsincompatiblewithalatearrivalofan ancestralOpisthacanthusinAfrica.
Scenario2:Antarcticorigin
ThescenariowithanancestralAntarcticOpisthacanthus (Ac0)resultswiththesameaffinitiesbetweenthecurrent lineagesasdescribedforaMadagascarorigin(e.g.,closer affinitiesbetween MadagascarandNewWorldlineages) (Fig.10). Theabsenceof Opisthacanthusin Antarcticais explainedbytheglaciationofthesoutherncontinent,and itsabsencefromIndiacouldbeexplainedbytheglobal mass extinction at the K–Pg, or the local extinction occurringduringthefastdriftingoftheIndianpeninsula
towards the North during the Upper Cretaceous. The absenceofOpisthacanthusinAustraliaismoredifficultto explain,especiallybecauseAntarcticahasbeenproposed asamajordispersalpathwaybetweenSouthAmericaand AustraliaduringtheCenozoic[48].Thegroupcouldhave beenexterminatedatthetimeoftheK–Pg,orcouldhave beenoutcompetedbyamoderngroupofscorpions.
Scenario3:Americanorigin
An ancestral American Opisthacanthus (Am0) would implytheclosestaffinitiesbetweentheAmericanlineages andtheAfricanlineages,withpossibleroutesofdispersal to Central and Southern Africa (Fig. 10). By the Lower Cretaceous, South America drifted away from Southern Africa,thelatterwasisolatedfromotherlandmassesin Southern Gondwana, but Antarctica was still bridging SouthAmericaandMadagascar,thusallowingdispersalof ancestralOpisthacanthus(Am0)toIndo-Madagascarviathe Antarctic(Fig.10).SuchascenarioimpliesaMadagascar lineageclosertotheSouthAmericanlineagethantoany other,aswellaslongbranches,i.e.earlysplitbetweenthe African and the New World lineages, which would therefore share some characteristics, e.g., a similar diversityinspeciesandgroups.
Scenario4:Africanorigin
Antarctica is bridging Africa, South America and Madagascar. An ancestral African Opisthacanthus (Af0) couldhavedispersedoverSouthernandCentralAfrica,and fromtheretowardsnorthernSouthAmerica,aswellasto Antarctica, before dispersing to Indo-Madagascar. From Central or Western Africa, Af0 could have dispersed towardsnorthernSouthAmerica,latertoAntarctica,and Indo-Madagascar. After the drifting of South America during the Lower Cretaceous, the land dispersal routes wouldbelimitedtoaroutestartinginCentralorWestern Africa towards Madagascar in anti-clockwise direction.
Thisscenarioisbasedontheassumptionthattheancestral populationscolonizingMadagascarshouldhavedoneso duringtheCretaceous,i.e.beforeMadagascardriftedaway Antarctica.This alsoimplies early dispersal fromAfrica towardsSouthAmerica.
Theglobalaffinitiesobservedbetweenthegroups,as well as the high diversity of the genus in Africa with sixgroupswidelydistributedonthecontinent,including theafricanusgroupoccurringboth inCentral Africaand SouthernAfrica,wouldpointtowardsanAfricanoriginof Opisthacanthus.TheSouthAmericanfossil(Protoischnurus Fig.10.ScenariosoforiginandpotentialdispersalofOpisthacanthususingtheconnectedlandmassesafterthebreakupoftheGondwanasome200Ma.The initialbreakupoftheGondwanaoccurredsimultaneouslybetweenIndo-Madagascar,AntarcticaandAustraliaononeside,andbetweenSouth-Americaand Africaontheotherside.Indo-MadagascarstartedriftingawayAfricaduringthelowerJurassic182millionyearsago(Ma),whenAfricastartedriftingaway Antarctica(2ndcolumnfromleft).Between140and120Ma,arapidincreaseofspreadingvelocityoccurredbetweenAfricaandAntarctica,andWestern GondwanastartedbreakingupwithSouthAmericariftingawayfromAfrica(column3).Micro-continentalblocksbridgedSouthernSouthAmericaand AntarcticauntiltheLowerCretaceous[145–100Ma].ThefinalbreakupofGondwanalandoccurredinsouthernSouthAmericaandtheAntarcticpeninsula.
OrigininIndo-MadagascarorMadagascar=I-M0;inAntarctica=Ac0,inSouthernAmerica=Am0,inAfrica=Af0.TheresultinggroupsinAfricacouldhave evolvedinWesternorCentralAfrica(AfC)orSouthernAfrica(AfS).AsfromtheOligocene,Africa(Af),SouthAmerica(Am),andMadagascar(M)wereall isolatedfromeachother.
axelrodorum (family Protoischnuridae) from Cretaceous SantanaFormation fromCratoarea inBrazil[20]would therefore supportan early dispersal to theNew World duringtheUpperJurassic,LowerCretaceous,withfurther vicarianceaftertheseparationofthecontinents.Finally, theaffinitiesshownbetweenthegroupsoftheNewWorld andMadagascarwouldalsobebestsupportedbyalater dispersal from the New World to Madagascar when Antarctica was still bridging these land masses during theJurassic–Cretaceous170–120Ma(Fig.10).
7. TheGondwanianmodelinothergroups
TherearemanymorecasesofGondwaniandistribution in the Madagascar context, and they mostly relate to archaicorextinctgroups.Forinstance,theprimitivefamily WinteraceaeR.Br.exLindl.oftreesandshrubsisabsent fromAfrica,representedinMalesia,Oceania,theNeotrop- icsandinMadagascarwiththemonotypicnarrowendemic monotypicgenus Takhtajania M. Baranova & J.-F. Leroy [49].
TheextinctCretaceousfrogBeelzebufoampingaEvans, Jones, & Krause, 2008 from Madagascar has its closest living relatives, the members of the Subfamily Cerato- phryinaeTschudi, 1838occuring inSouth America[50–
52].Basedonanexplicitphylogeneticanalysis,Ruaneand colleagues[51]proposedaSouthAmericanoriginofthe group.
The most relevant example to illustrate an ancient Gondwana lineage comes from an endemic beetle of Madagascarrepresentinganancientlineagewithorigins fromUpperTriassictoLower Jurassic(226Ma–187Ma).
After theK–Pg, Madagascarserved asa refugia for this beetle,HeterogyrusmillotiLegros,1953whichiscurrently the new case recognized for vicariance given that it divergedfromitsclosest continentalrelative before the breakupoftheGondwana[53].
8. Conclusion
Theimplicationsofthebiogeographicscenariosoutli- nedabovecanbesurprisinggiventhattheyshowvicariant events between the most distant land masses. The Gondwanianmodeltoexplaintheoriginoftheancestral OpisthacanthusisjustifiedbytheCretaceoussisterclade,or stemgroup,fromBrazil.Tofullyunderstandthetreeofthe Opisthacanthus groups in the New World, Africa and Madagascar,onewouldneedalargersampleoftheentire clade,DNAsequencedata,andmorefossilmaterialfrom various places to calibrate the phylogeny of the Opisthacanthus. Withtheinformation currentlyat hand, toexplainthedistributionandpatternoftheOpisthacan- thusgroups,ratherthantheCenozoicoverwaterdispersal, we privilege the Mesozoicvicariance withan origin in Africa, and Madagascar serving as a dead-end within SouthernGondwana.
Disclosureofinterest
The authors declare that they have no competing interest.
Acknowledgements
We aremostgratefultoE´lise-AnneLeguin(Muse´um, Paris)forhercontributiontothepreparationofthephotos andplates.
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