Global patterns of species richness in coastal cephalopods

ma s-06-00469 Augus 1, 2019 Time: 18:37 # 1 ORIGINAL RESEARCH published: 02 Augus 2019 doi: 10.3389/ ma s.2019.00469 Edi ed by: Sophie on de Heyden, S ellenbosch Uni e si y, Sou h A ica Re iewed by: Xiubao Li, Hainan Uni e si y, China Luisa Fe nanda Dueñas, Uni e sidad Nacional de Colombia, Colombia B ian Bowen, Uni e si y o Hawai‘i, Uni ed S a es *Co espondence: Rui Rosa [email p o ec ed] Special y sec ion: This a icle was submi ed o Ma ine E olu iona y Biology, Biogeog aphy and Species Di e si y, a sec ion o he jou nal F on ie s in Ma ine Science Recei ed: 06 May 2019 Accep ed: 11 July 2019 Published: 02 Augus 2019 Ci a ion: Rosa R, Pissa a V, Bo ges FO, Xa ie J, Gleadall IG, Goliko A, Bello G, Mo ais L, Lishchenko F, Rou a Á, Judkins H, Ibáñez CM, Pia kowski U, Vecchione M and Villanue a R (2019) Global Pa e ns o Species Richness in Coas al Cephalopods. F on . Ma . Sci. 6:469. doi: 10.3389/ ma s.2019.00469 Global Pa e ns o Species Richness in Coas al Cephalopods Rui Rosa1*, Vasco Pissa a1, F ancisco O. Bo ges1, José Xa ie 2,3, Ian G. Gleadall4, Alexey Goliko 5, Giamba is a Bello6, Liliane Mo ais7, Fedo Lishchenko8, Ál a o Rou a9, Hea he Judkins10, Ch is ian M. Ibáñez11, Uwe Pia kowski12, Michael Vecchione13 and Roge Villanue a14 1MARE – Ma ine and En i onmen al Sciences Cen e, Labo a ó io Ma í imo da Guia, Faculdade de Ciências da Uni e sidade de Lisboa, Lisbon, Po ugal, 2MARE – Ma ine and En i onmen al Sciences Cen e, Depa men o Li e Sciences, Uni e si y o Coimb a, Coimb a, Po ugal, 3B i ish An a c ic Su ey, Na u al En i onmen Resea ch Council, Camb idge, Uni ed Kingdom, 4G adua e School o Ag icul u al Science, Tohoku Uni e si y Aobayama Campus, Sendai, Japan, 5Depa men o Zoology, Kazan Fede al Uni e si y, Kazan, Russia, 6A ion, Mola di Ba i, I aly, 7Ins i u e o En i onmen al Heal h, Facul y o Medicine, Uni e si y o Lisbon, Lisbon, Po ugal, 8A.N. Se e so Ins i u e o Ecology and E olu ion, Labo a o y o Ecology and Mo phology o Ma ine In e eb a es, Moscow, Russia, 9Ins i u o de In es igaciones Ma inas, Consejo Supe io de In es igaciones Cien í icas, Vigo, Spain, 10 Depa men o Biological Sciences, Uni e si y o Sou h Flo ida, S . Pe e sbu g, S . Pe e sbu g, FL, Uni ed S a es, 11 Depa amen o de Ecología y Biodi e sidad, Facul ad de Ciencias de la Vida, Uni e sidad And es Bello, San iago, Chile, 12 GEOMAR, Helmhol z Cen e o Ocean Resea ch Kiel, Kiel, Ge many, 13 Na ional Ma ine Fishe ies Se ice, Na ional Sys ema ics Labo a o y, Na ional Museum o Na u al His o y, Smi hsonian Ins i u ion, Washing on, DC, Uni ed S a es, 14 Ins i u de Ciencies del Ma , Consejo Supe io de In es igaciones Cien í icas, Ba celona, Spain Wi hin he con ex o global clima e change and o e ishing o ish s ocks, he e is some e idence ha cephalopod popula ions a e bene i ing om his changing se ing. These in e eb a es show enhanced pheno ypic lexibili y and a e ound om pola egions o he opics. Ye , he global pa e ns o species ichness in coas al cephalopods a e no known. He e, among he 370 iden i ied-species, 164 a e oc opuses, 96 a e cu le ishes, 54 a e bob ails and bo le ails, 48 a e insho e squids and 8 a e pygmy squids. The mos di e se ocean is he Paci ic (wi h 213 cephalopod species), ollowed by he Indian (146 species) and A lan ic (95 species). The leas di e se a e he Sou he n (15 species) and he A c ic (12 species) Oceans. Endemism is highe in he Sou he n Ocean (87%) and lowe in he A c ic (25%), which e lec s he younge age and he “A lan i ica ion” o he la e . The o me is associa ed wi h an old lineage o oc opuses ha di e ged a ound 33 Mya. Wi hin he 232 eco egions conside ed, he highes alues o oc opus and cu le ish ichness a e obse ed in he Cen al Ku oshio Cu en eco egion (wi h a o al o 64 species), ollowed by he Eas China Sea (59 species). This pa e n sugges s dispe sal in he Cen al Indo-Paci ic (CIP) associa ed wi h he highly p oduc i e Oyashio/Ku oshio cu en sys em. In con as , insho e squid ho spo s a e ound wi hin he CIP, namely in he Sunda Shel P o ince, which may be linked o he occu ence o an ancien in e mi en biogeog aphic ba ie : a land b idge o med du ing he Pleis ocene which se e ely es ic ed wa e low be ween he Paci ic and Indian Oceans, he eby acili a ing squid auna di e en ia ion. Ano he ma ked pa e n is a longi udinal ichness cline om he Cen al (CIP) owa d he Eas e n Indo-Paci ic (EIP) ealm, wi h cen al Paci ic a chipelagos as e olu iona y dead ends. In he A lan ic Ocean, closu e o he A a o Seaway (a he Is hmus o Panama) and S ai s o Gib al a (Medi e anean Sea) F on ie s in Ma ine Science | www. on ie sin.o g 1Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 2 Rosa e al. Global Biogeog aphy o Coas al Cephalopods a e his o ical p ocesses ha may explain he con empo a y Ca ibbean oc opus ichness and Medi e anean sepiolid endemism, espec i ely. Las , we discuss how he li e cycles and s a egies o cephalopods may allow hem o adap quickly o u u e clima e change and ex end he bo ealiza ion o hei dis ibu ion. Keywo ds: biogeog aphy, mollusk, cephalopod, cu le ish, squid, oc opus, species ichness INTRODUCTION Gi en he impo ance ha biodi e si y plays in sus aining ecosys ems (Ca dinale e al., 2012;Hoope e al., 2012), iden i ica ion o he main h ea s o biodi e si y is impo an (Hobday and Pecl, 2014;Ma chese, 2015;Rami ez e al., 2017). Habi a deg ada ion, o e ishing, pollu ion, biological in asions and, in pa icula , clima e change a e he majo causes o biodi e si y loss, which has p obably al eady eached a c i ical ansi ion poin (Ba nosky e al., 2012). A global edis ibu ion o ma ine species, including cephalopods, due o bo h man- d i en biological in asions (e.g., di ec anspo o li ing beings, opening and widening o he Suez Canal) and, mos impo an ly, clima e change, is occu ing (Sunday e al., 2012), wi h ma ine o ganisms now expanding hei limi s o dis ibu ion by a mean o 72.0 ±13.5 km pe decade (Poloczanska e al., 2013). Among he ma ine bio a, and wi hin he no ion o winne s and lose s in he con ex o global change, he e is some e idence ha cephalopods (oc opuses, squids, and cu le ishes) a e bene i ing om he changing ocean en i onmen , due o he combina ion o global wa ming and o e ishing o hei p eda o s and compe i o s (Vecchione e al., 2009;Rodhouse, 2013;Doubleday e al., 2016). Pa o his success may be also ela ed o hei g ea pheno ypic lexibili y and, consequen ly, en i onmen al plas ici y, which may be linked o hei ex ensi e ecoding ac i i y, since in cephalopods gene ic changes “on he ly” by RNA edi ing a he ansla ion le el may be mo e impo an in he sho e m han ha dwi ed changes in DNA (Alon e al., 2015;Lisco i ch-B aue e al., 2017). Cephalopods a e ecologically and comme cially impo an in e eb a es ha a e semelpa ous wi h a gene ally sho li e cycle. The la e may be ca ego ized as: (i) holoben hic, when he en i e li e cycle is associa ed wi h he ben hos, as in mos cu le ishes; (ii) holopelagic, when he en i e cycle is associa ed wi h he pelagic en i onmen , in all oceanic squids; o (iii) me oben hic (o me oplank onic), when he ha chlings a e plank onic bu become ben hic a e se lemen a he ju enile s age, in some oc opuses (Villanue a e al., 2016). The sho li e span is also associa ed wi h high ood in ake and g ow h a es sus ained by o acious s a egies and oppo unis ic die s (Boyle and Bole zky, 1996;Boyle and Rodhouse, 2005). No su p isingly, and p obably as a esul o hei molecula and ecological ea u es, cephalopods a e ound in all ma ine habi a s (excluding he hadal zone and he Black Sea) om he pola egions o he opics (Boyle and Rodhouse, 2005). Al hough cephalopod di e si y and dis ibu ion ha e been s udied ex ensi ely in he pas , mos such esea ch and knowledge has been compiled as species accoun s (see examples in Je eb and Rope , 2005, 2010;Je eb e al., 2014). La ge-scale biogeog aphic s udies on cephalopod di e si y a e sca ce and mos ly concen a ed in he A lan ic Ocean (Rosa e al., 2008a,b;Judkins e al., 2010), pola zones (e.g., Xa ie e al., 1999;Allcock e al., 2011;Goliko e al., 2013;Xa ie e al., 2016b, 2018) and he Paci ic Ocean (Ibáñez e al., 2009, 2019) o speci ic axonomic g oups (e.g., Ibáñez e al., 2016;Ulloa e al., 2017). Mo eo e , some o hose s udies we e designed o in es iga e b oad-scale la i udinal g adien s (e.g., ichness and body-size da a ac oss la i udinal bins) and desc ibe he espec i e en i onmen al de e minan s (e.g., Rosa e al., 2008a, 2012;Ibáñez e al., 2019). To he bes o ou knowledge, he e is no global quan i a i e in o ma ion on di e si y ho spo s o his cha isma ic g oup o in e eb a es on he con inen al shel egions o he wo ld. I is wo h no ing ha he concep o ho spo s has been used as a key s a egy o global conse a ion plans, bu hey emain la gely unexplo ed o ma ine habi a s (Wo m e al., 2003;Renema e al., 2008;Ti enso e al., 2010) due o da a de iciency (Mi e meie e al., 2011). Biodi e si y ho spo s ha e been de ined usually using species-based me ics (e.g., species ichness; endemic species ichness; numbe o a e/ h ea ened species) o , al e na i ely, ocusing on phylogene ic and unc ional di e si y me ics (Mye s, 1988, 2003;Reid, 1998;G ay, 2000; Hoeks a e al., 2005). Mo e ecen ly, ma ine ho spo s ha e been iden i ied based on ichness wi h me ics ha inco po a e bo h species abundances and unc ional ai s (S ua -Smi h e al., 2013) o , al e na i ely, based on egions ha a e wa ming mo e apidly (Hobday and Pecl, 2014). He e, he global biogeog aphy (pa e ns o species ichness and numbe o endemic species) o coas al cephalopods, which h i e on he wo ld’s con inen al shel egions, is desc ibed o he i s ime. The s udy was es ic ed o he ne i ic ealm (i.e., coas al species) because he e is a lack o knowledge abou he dis ibu ion/biogeog aphy o deep-sea/deme sal cephalopod auna in many pa s o he global ocean. A p esence/absence da abase was compiled and o ganized in i e majo coas al g oups (de ined in c . Hanlon e al., 2018, p. 72), namely: (i) cu le ishes (species belonging o he Family Sepiidae), (ii) bob ails and bo le ails (Families Sepiolidae and Sepiada iidae, espec i ely), (iii) pygmy “squids” (Family Idiosepiidae), (i ) insho e squids (Family Loliginidae), and ( ) ben hic inci a e oc opuses (Families Oc opodidae, Eledonidae, En e oc opodidae, Megaleledonidae, and Ba hypolypodidae). The occu ence o hese g oups was de e mined o Ma ine Eco egions o he Wo ld (MEOW; Spalding e al., 2007). The eco egions a e de ined as “A eas o ela i ely homogeneous species composi ion, clea ly dis inc om adjacen sys ems (. . .). The dominan biogeog aphic o cing agen s de ining he eco egions a y om loca ion o loca ion bu may include isola ion, upwelling, nu ien inpu s, eshwa e in lux, empe a u e egimes, ice egimes, exposu e, F on ie s in Ma ine Science | www. on ie sin.o g 2Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 3 Rosa e al. Global Biogeog aphy o Coas al Cephalopods sedimen s, cu en s, and ba hyme ic o coas al complexi y” (Spalding e al., 2007). The ollowing ques ions a e add essed. (1) Which oceans and o he la ge-scale ma ine egions (i.e., ealms – see Spalding e al., 2007) a e he mos di e se in e ms o coas al cephalopod auna? (2) Which coas al eco egions cons i u e he main ho spo s (and coldspo s)? (3) Wha a e he po en ial o igin and di e si ica ion pa e ns (based on he numbe o sha ed species)? and (4) Which ocean ealms p esen he g ea e le els o endemism? We discuss he impac o his o ical p ocesses and majo ma ine biogeog aphical ba ie s on he de ec ed pa e ns. MATERIALS AND METHODS Da abase The geog aphical anges o coas al cephalopod species we e in es iga ed, on a global scale, by means o an exhaus i e su ey o p ima y li e a u e (e.g., Rosa e al., 2008a;Judkins e al., 2010;Xa ie e al., 2018), wi h a special ocus on he mos ecen FAO guides on he cephalopods o he wo ld (Je eb and Rope , 2005, 2010;Je eb e al., 2014). The p esence/absence da abase was buil a ound 12 ealms [A c ic (ARC); Tempe a e No he n A lan ic (TNA); T opical A lan ic (TAT); Tempe a e Sou he n A ica (TSAF); Wes e n Indo-Paci ic (WIP); Tempe a e Aus alasia (TAUS); Indo-Paci ic (CIP); Tempe a e No he n Paci ic (TNP); Eas e n Indo-Paci ic (EIP); T opical Eas e n Paci ic (TEP); Tempe a e Sou h Ame ica (TSA); Sou he n Ocean (SO)] (Supplemen a y Tables S1–S3), and 232 eco egions, bo h de ined by Spalding e al. (2007). I includes a o al o 370 species associa ed wi h, bu no necessa ily es ic ed o, con inen al shel es (bo om dep hs <200 m) a la e on ogene ic s ages (because se e al species display on ogene ic ho izon al/slope- shel mig a ions). Oegopsid squids and pelagic oc opuses a e known o h i e in, o o pe iodically in ade he ne i ic p o ince bu we e no included in he p esen da abase o he sake o cla i y. Simila ly, deepe dwelling species a e no conside ed because his would hen include species such as nea -ben hic ci a e oc opuses, which show much b oade , oceanic dis ibu ion pa e ns. New (e.g., Lepidoc opus joaquini;Sales e al., 2019) and a e species (only known om hei ype locali y – no signi ican in o ma ion abou hei geog aphical dis ibu ion) we e excluded. Based on such c i e ia, he chambe ed nau iluses we e also excluded – he only species wi h a well-de ined geog aphical ange ou side i s ype locali y is Nau ilus pompilius. Simila ly, o he myopsid squid Aus ali eu his ald ichi ( he only membe o he Family Aus ali eu hidae). I is also wo h no ing ha some nominal species lis ed in he da abase a e known o comp ise species complexes. In con as o he Oc opus ulga is complex (a ocus o much ecen esea ch, e.g., Lei e e al., 2008;Amo e al., 2014, 2015, 2017;Gleadall, 2016; González-Gómez e al., 2018), he complexes o Sepia pha aonis (Ande son e al., 2011), Sepio eu his lessoniana (Cheng e al., 2014) and Lolliguncula b e is (Sales e al., 2014) a e no well- de ined in geog aphical e ms and he e o e a e lis ed as single species. The e o e, he species ichness pa e ns p esen ed he e a e conse a i e es ima es. Da a Analyses We used he so wa e A cGIS e sion 10.6.1 and he open- sou ce shape iles om Spalding e al. (2007) o he iden i ica ion o he ho spo s (eco egions) o cephalopod ichness. Addi ionally, eco egions we e clus e ed in 12 di e en ealms, acco ding o he c i e ia de ined by Spalding e al. (2007). The ela ionships among ealms we e e alua ed o he di e en cephalopod g oups based on he numbe o sha ed species (see simila app oach in Floe e e al., 2008). Fo each g oup we calcula ed a simila i y ma ix (using he B ay– Cu is index) o ob ain a dis ibu ion dend og am by means o hie a chical clus e analysis using he UPGMA algo i hm (PAST; Hamme e al., 2001). We hen esampled he o iginal bina y ma ix pe o ming 1000 s ochas ic eassignmen s o gene a e a boo s ap p ocedu e o ob ain he pe cen age o eplica es (1000 i e a ions) suppo ing each node o he dend og am (only alues >50% a e shown). Endemic species we e de ined as hose species es ic ed o a single ealm in he da abase. Bo le ails and pygmy squids we e excluded om he endemism analysis due o hei low eco egional ichness alues (up o a maximum o 2 species pe eco egion) and a es ic ed- ealm dis ibu ion. RESULTS Global Coas al Cephalopod Richness pe Ocean The p esen species ichness da abase e eals ha he mos di e se ocean is he Paci ic Ocean (wi h 213 cephalopod species), ollowed by he Indian (146 species) and A lan ic (95 species) Oceans. The leas di e se a e he A c ic (12 species) and Sou he n (15 species) Oceans. This end is mos ly obse ed in oc opuses (Families Oc opodidae, Eledonidae, En e oc opodidae, Megaleledonidae, and Ba hypolypodidae), insho e squids (Family Loliginidae) and pygmy “squids” (Idiosepiidae), since cu le ish (Family Sepiidae) ichness is highe in he Indian (62 species) ollowed by he Paci ic Ocean (49 species; Figu e 1). In con as , he ichness o bob ails and bo le ails (Families Sepiolidae and Sepiada iidae, espec i ely) is highes in he A lan ic (27 species). Among he 370 s udied-species wo ld-wide, 164 a e oc opuses, 96 a e cu le ishes, 54 a e bob ails and bo le ails, 48 a e insho e squids and 8 a e pygmy squids. I is impo an o no e he absence o : (i) cu le ishes, bob ails, bo le ails, pygmy “squids” and insho e squids in he Sou he n Ocean; (ii) cu le ishes, bo le ails, pygmy “squids” and insho e squids in he A c ic; and (iii) cu le ishes and bo le ails a ound he Ame icas (Figu es 1,2). Ho spo s and Coldspo s o Cephalopod Richness pe Realm The mos di e se cephalopod ealm is he Cen al Indo-Paci ic (CIP, n= 129 species), ollowed by he Tempe a e No he n Paci ic (TNP, n= 98) and Wes e n Indo-Paci ic (WIP, n= 84). The leas di e se ealms we e he Sou he n (SO, n= 15) and F on ie s in Ma ine Science | www. on ie sin.o g 3Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 4 Rosa e al. Global Biogeog aphy o Coas al Cephalopods FIGURE 1 | Con inued F on ie s in Ma ine Science | www. on ie sin.o g 4Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 5 Rosa e al. Global Biogeog aphy o Coas al Cephalopods FIGURE 1 | To al numbe o species o cu le ishes (Family Sepiidae; A), bob ails (Family Sepiolidae; B), bo le ails (Family Sepiada iidae; C), pygmy squids (Family Idiosepiidae; D), insho e squids (Family Loliginidae; E), oc opuses (Families Oc opodidae, Eledonidae, En e oc opodidae, Megaleledonidae, and Ba hypolypodidae; F), and o e all ( o al cephalopods; G) h oughou he Wo ld Ocean. he A c ic (ARC, n= 12) oceans, and su p isingly he Eas e n Indo-Paci ic (EIP, n= 11; Figu e 2). The majo ho spo (CIP) is consis en in all cephalopod g oups, excep o bob ails and bo le ails which ha e hei ho spo in he Tempe a e No he n A lan ic (TNA), and Tempe a e Aus alasia (TAUS), espec i ely. Fo oc opuses, he leas di e se ealm is Tempe a e Sou he n A ica (TSAF, n= 4), and no EIP (n= 9) o he poles (ARC, n= 6; SO, n= 15). Simila i ies o Cephalopod Fauna Among Realms Figu e 3 summa izes he ela ionship o he numbe o sha ed species among ealms. Based on clus e analyses, cu le ishes show h ee majo clus e s: (i) CIP, TNP, and TAUS g oup, (ii) WIP and TSAF, and (iii) TNA and TAT (Figu e 3A). Bob ails show simila ends wi h CIP clus e ing wi h TNP and TAUS (Figu e 3B). In he bo le ails, CIP clus e s wi h TAUS and WIP wi h TNP (Figu e 3C). In pigmy “squids,” CIP also clus e ed wi h TNP and TAUS (bu below b oos ap h eshold; Figu e 3D). In con as , in bo h insho e squids (Figu e 3E) and oc opuses (Figu e 3F) CIP clus e s close o WIP and hen TNP, and EIP is sepa a e om he CIP, WIP, and TNP. Mo eo e , he oc opuses also clea ly show a second A c ic/A lan ic clus e and a hi d TNP and TAUS clus e . In he o e all analysis, cephalopod SO auna is clea ly sepa a e om he o he ealms (see sec ion “Endemism Ra es pe Realm”). As obse ed o he cu le ishes (and con a ily o oc opuses and squids), CIP cephalopod auna clus e s close o hose o he TNP and TAUS (Figu e 3G). Cephalopod Richness pe Eco egion Wi hin he 232 eco egions conside ed, he highes ichness alue is obse ed in he Cen al Ku oshio Cu en eco egion (CKC), wi h 64 species (Figu e 4), ollowed by he Eas China Sea (ECS) (59 species) and Eas e n Philippines (48 species) eco egions. As men ioned abo e, he Indian Ocean was he second mos di e se, and h ee ho spo s we e obse ed, namely he Ja a and Sulawesi Sea eco egions, each wi h 38 species, and he Malacca S ai eco egion wi h 33 species. Rega ding he A lan ic Ocean, a majo a ea o cephalopod ichness sp eads om he No h Sea down o no hwes e n A ica, wi h he Wes e n Medi e anean pa icula ly ich (wi h 29 species) and in he Ad ia ic, Aegean and Ionian seas eco egions (wi h 27 species). A any gi en la i ude, he eas e n A lan ic is always mo e di e se han he wes e n side, in pa because he amily Sepiidae and he sub amily Sepiolinae a e absen om he la e . As men ioned abo e, he amilies Sepiidae, Sepiada iidae, Idiosepiidae, and Loliginidae a e absen om he pola eco egions. Only he Family Sepiolidae and he oc opuses a e ound in he A c ic coas al a eas, a ying om 1 o 4 species among eco egions. Cu le ish, Bob ail, and Bo le ail Richness pe Eco egion The highes alues o species ichness in he Sepiidae a e in he CKC and he ECS eco egion, each wi h a o al numbe o 21 species (Figu e 5A). Two o he ho spo s a e he adjacen Sou he n China o Vie nam eco egion, and he Eas A ican Co al Coas , each wi h 13 species. A comple ely di e en global ichness pa e n was obse ed o bob ail species, membe s o he amily Sepiolidae. Thei maximum ichness alues we e ound in he Medi e anean eco egions, especially in he wes e n pa wi h a o al o 15 species (Figu e 5B). The adjacen eco egions, namely wes e n Eu ope and no h-wes e n A ica, also showed high alues (13 and 11, espec i ely). Qui e simila alues we e also obse ed in he ECS and CKC eco egions, each wi h eigh species. Bo le ails a e he leas speciose g oups, each wi h a maximum ichness alue o 2 pe eco egion, including he CKC, he Cen al and Sou he n G ea Ba ie Ree and he Eas Cen al Aus alian Shel (Figu e 5C). Pygmy “Squid,” Insho e Squid and Oc opus Richness pe Eco egion Conce ning he pygmy squids, he e a e ce ain simila i ies wi h he p e ious g oup ega ding he es ic ed numbe o species; ha is, a maximum o 2 species in he same eco egion. We iden i y wo main a eas: one in he Indo-Paci ic, om no h Aus alia o Indonesia, comp ising 9 eco egions; and a second in he a ea o Sou h A ica o sou he n Mozambique, comp ising 3 eco egions (Figu e 6A). Clea ho spo s o insho e squid species ichness occu in he Indo-Paci ic a ea, mo e p ecisely in he Ja a Sea eco egion (12 species), and Malacca S ai , Palawan and Sulawesi Seas (all h ee egions wi h 11 species each; Figu e 6B). In con as , he g ea es ho spo o oc opuses occu s in he CKC eco egion, yielding he maximum alue o 24 species (Figu e 6C). The nea by ECS and Eas e n Philippines eco egions also ha e high species ichness alues, each wi h 18 species. Some o he leas di e se eco egions o oc opuses we e ound wi hin he TSAF and EIP ealms. Endemism Ra es pe Realm Among he 12 ealms analyzed (Figu es 7A–E and Supplemen a y Table S2), he ealms wi h g ea e endemism a es o cu le ishes (Figu e 7A) a e TAUS (53%), WIP (46%), and TNP (38%). The e a e no cu le ish endemisms in TNA. Rega ding he bob ails (Figu e 7B), he op h ee a e he EIP (100%), TAUS (83%), and TNA (55%; mainly due o he highly- endemic Medi e anean auna). The lowes alue was ound in he A c ic (17%). Fo insho e squids (Figu e 7C), he op h ee o endemisms a e he TAT (36%), WIP (29%) and TNP (27%). No squid endemisms we e ound in he TSA o TEP. The oc opus auna (Figu e 7D) show mos endemisms in he SO (87%), TSA (67%), and TAUS (65%); and lowes alues in he F on ie s in Ma ine Science | www. on ie sin.o g 5Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 6 Rosa e al. Global Biogeog aphy o Coas al Cephalopods FIGURE 2 | Con inued F on ie s in Ma ine Science | www. on ie sin.o g 6Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 7 Rosa e al. Global Biogeog aphy o Coas al Cephalopods FIGURE 2 | To al numbe o species o cu le ishes (Family Sepiidae; A), bob ails (Family Sepiolidae; B), bo le ails (Family Sepiada iidae; C), pygmy squids (Family Idiosepiidae; D), insho e squids (Family Loliginidae; E), oc opuses (Families Oc opodidae, Eledonidae, En e oc opodidae, Megaleledonidae, and Ba hypolypodidae; F), and o e all ( o al cephalopods; G) pe ma ine ealm.: A c ic (ARC; ligh blue in lowe panel), Tempe a e No he n A lan ic (TNA; blue), T opical A lan ic (TAT; da k blue), Tempe a e Sou he n A ica (TSAF; ligh b own), Wes e n Indo-Paci ic (WIP; b own), Tempe a e Aus alasia (TAUS; pu ple), Cen al Indo-Paci ic (CIP; da k ed), Tempe a e No he n Paci ic (TNP; ed), Eas e n Indo-Paci ic (EIP; o ange), T opical Eas e n Paci ic (TEP, yellow), Tempe a e Sou h Ame ica (TSA; g een), Sou he n Ocean (SO; da k g ay). (H) Is a global map o easy e e ence o he di e en ealms. A c ic (17%) and TAT (31%). In con as o he o he cephalopod g oups, oc opus endemisms occu in all 12 ealms. As a g oup (Figu e 7E), cephalopods show highe endemism in he SO (87%) and TAUS (77%), and lowes in he A c ic (25%). DISCUSSION Da abase Limi a ions Species ichness pa e ns p esen ed he e should be conside ed conse a i e because: (i) some assump ions we e made (e.g., exclusion o oegopsids, new species and species-complexes; see sec ion “Ma e ials and Me hods”), and (ii) many coas al egions a e s ill unde -sampled (e.g., he A ican and wes e n Indian Ocean egion). Due o he lack o ha d mo phological s uc u es, cephalopod species iden i ica ion is challenging and di icul (Xa ie e al., 2015), and some o he p esen di e si y pa e ns may be d i en by an unde es ima ed c yp ic di e si y (T on elj and Fiše , 2009). Mo eo e , cephalopods a e known o be “mas e s o disguise” (Hanlon and Messenge , 2018), which may pose addi ional obse a ional di icul ies, pa icula ly in he complex and he e ogeneous opical ee habi a s (such as hose ound in he Eas e n Indo-Paci ic coldspo ). Cen al Indo-Paci ic Realm and he Co al T iangle The p esen s udy e ealed ha he g ea es alues in species ichness o coas al cephalopod auna we e ound in he CIP ealm (Figu e 2), a la ge a ea encompassing he Co al T iangle [known as he Indo-Aus alian A chipelago (IAA)], which is a well- known ma ine cen e o specia ion and he la ges global ma ine biodi e si y ho spo o many axa, anging om co als o ee ishes (Bowen e al., 2013;B iggs and Bowen, 2013;Cowman and Bellwood, 2013). The IAA is a pa icula ly b oad shallow-wa e a ea wi h p onounced geological complexi y and connec s wi h wo majo biogeog aphic egions, key aspec s ha may p omo e specia ion p ocesses and/o p o ide species e uges (Bowen e al., 2013;B iggs and Bowen, 2013;Cowman and Bellwood, 2013). Gi en ha such a di e si y ho spo is ecu en o so many axonomic g oups, including cephalopods (Figu e 4), Renema e al. (2008) a gued ha he e mus be a uni ying explana ion. Th ee main hypo heses a e based on specia ion p ocesses and dispe sal, desc ibing his egion as: (i) a “cen e o o igin,” implying ha he IAA is a majo si e o specia ion om which species dispe se; (ii) a “cen e o o e lap,” o which he IAA ho spo is a consequence o o e lap om su ounding aunas, each o which is dispe sing in all di ec ions om i s own sepa a e biogeog aphic a ea; o (iii) a “cen e o accumula ion” whe e specia ion occu s in pe iphe al a eas and species ex end hei anges in o his a ea h ough unidi ec ional dispe sal as a esul o p e ailing cu en s (Woodland, 1983;Bellwood and Wainw igh , 2002;Mo a e al., 2003;Bowen e al., 2013;Gai he and Rocha, 2013;Bellwood e al., 2015). I is possible ha , a he han jus one mechanism, each o hese p ocesses migh be con ibu ing (see Mi ono , 2006). A geological ime scales, he e is some e idence o h ee po en ial e ol ing s ages. The IAA may ha e (i) begun as a cen e o accumula ion (and/o e uge) o species ha we e pa o he Te hys Sea auna (du ing he loss o habi a as he Te hys Sea closed du ing he la e Eocene and Oligocene); hen (ii) become a cen e o o igin o di e si ica ion, s a ing du ing he Miocene; and (iii) s a ed a pe iod o dispe sal ollowing he Pliocene (Bellwood and Wainw igh , 2002;Renema e al., 2008;B iggs and Bowen, 2013; Cowman and Bellwood, 2013). Such a biogeog aphic pa e n may esul om highe a es o su i al wi hin he IAA, wi hou he need o any excep ional specia ion e en s (Cowman and Bellwood, 2013). The appa en enhanced a es o specia ion in he IAA may also be a compa a i e phenomenon linked o he lowe empe a u es and high endemism a highe la i udes (c . Rabosky e al., 2018). Cen al Ku oshio Cu en and Eas China Sea Eco egions (Including he Ryukyu A chipelago) The geological and e olu iona y backg ound men ioned abo e may explain why he CIP is he iches cephalopod- ela ed ealm. Ye , inc easing he spa ial esolu ion o analyses e eals ha he wo main ho spo s (a he eco egion le el) a e ou side he CIP, lying wi hin he TNP ealm. Among he 232 eco egions conside ed, he highes cephalopod ichness alues a e obse ed in he CKC and ECS eco egions (Figu e 4). Such a pa e n may cons i u e e idence o he p e iously men ioned IAA dispe sal s age: hese wo TNP eco egions a e loca ed in a sub opical gy e wi h p edominan cu en s unning om he IAA, which is hus p o ided wi h a s ong dispe sal mechanism. Mo eo e , he CKC is also in luenced by he Oyashio/Ku oshio ansi ion zone. Such a complex oceanog aphic con ex , oge he wi h he nu ien en ichmen dynamics o eddies and upwelling sys ems in he a ea, a e known o g ea ly in luence such ma ine ecosys ems and ela ed ishe ies (Ya su e al., 2013). Ano he , and p obably mo e ele an , ea u e is he ac ha bo h CKC and EAS eco egions comp ise he sub opical Ryukyu (Okinawan) A chipelago o Japan. This sou he n egion o Japan bo de s he no he n limi o he IAA and is well-known o i s co al ee s and e y high le els o ma ine biodi e si y, bo h in e ms o species ichness and endemism (Hughes e al., 2002;Cowman e al., 2017; Reime e al., 2019). F on ie s in Ma ine Science | www. on ie sin.o g 7Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 8 Rosa e al. Global Biogeog aphy o Coas al Cephalopods FIGURE 3 | Con inued F on ie s in Ma ine Science | www. on ie sin.o g 8Augus 2019 | Volume 6 | A icle 469 ma s-06-00469 Augus 1, 2019 Time: 18:37 # 9 Rosa e al. Global Biogeog aphy o Coas al Cephalopods FIGURE 3 | Dissimila i y index o cu le ishes (Family Sepiidae; A), bob ails (Family Sepiolidae; B), bo le ails (Family Sepiada iidae; C), pygmy squids (Family Idiosepiidae; D), insho e squids (Family Loliginidae; E), oc opuses (Families Oc opodidae, Eledonidae, En e oc opodidae, Megaleledonidae, and Ba hypolypodidae; F), and o e all ( o al cephalopods; G). A c ic (ARC; ligh blue in lowe panel), Tempe a e No he n A lan ic (TNA; blue), T opical A lan ic (TAT; da k blue), Tempe a e Sou he n A ica (TSAF; ligh b own), Wes e n Indo-Paci ic (WIP; b own), Tempe a e Aus alasia (TAUS; pu ple), Cen al Indo-Paci ic (CIP; da k ed), Tempe a e No he n Paci ic (TNP; ed), Eas e n Indo-Paci ic (EIP; o ange), T opical Eas e n Paci ic (TEP, yellow), Tempe a e Sou h Ame ica (TSA; g een), Sou he n Ocean (SO; da k g ay). (H) Is o easy e e ence o he di e en ealms. FIGURE 4 | Wo ldwide ichness (numbe o species pe eco egion) pa e ns o coas al cephalopods. Taxonomic Di e ences Be ween CIP and TNP Ho spo s Conside ing he o e all pa e ns o majo axonomic (and consequen ly also ecological unc ional) g oups, di e si y is d i en mainly by he oc opus and cu le ish auna. The o me eaches maximum ichness alues in he TNP, namely in CKC (24 species) and ECS (18 species; Figu e 6). The (nek oben hic) amily Sepiidae shows a simila occu ence o ho spo s (CKC and ECS: each wi h 21 species; Figu e 5A). In con as , he (pelagic) insho e squid g oup shows highes ichness in he CIP, wi hin wo di e en p o inces: (i) he Sunda Shel P o ince (al eady ou side he IAA), composed o he Ja a Sea (12 species) and Malacca S ai eco egions (11 species); and (ii) he Wes e n IAA P o ince, which encompasses he Palawan and Sulawesi Seas eco egions (each wi h 11 species; Figu e 6). Unde s anding such specia ion p ocesses is qui e challenging, i s , because he e a e ew geog aphic ba ie s (B iggs, 1994;B iggs and Bowen, 2013) and, second, because some coas al cephalopods ha e high dispe sal po en ial wi h plank onic pa ala al s ages (Villanue a e al., 2016). Ye , he p esence o ‘weak’ o in e mi en ba ie s may ha e acili a ed cephalopod di e en ia ion in hese Indo-Paci ic a eas. Fo ins ance, du ing Pleis ocene sea-le el luc ua ions pa icula ly du ing glacial pe iods wi h consequen low sea le els, a land b idge was o med on he Sunda shel ( he loca ion o he p esen squid ho spo s), which se e ely es ic ed (bu did no s op) wa e low be ween he Paci ic and Indian Oceans (McManus, 1985). A simila occu ence has been used o explain he e olu iona y pa i ions ( ica ian specia ion) o o he ee - associa ed g oups, namely s oma opods (Ba be e al., 2000) and ishes (Randall, 1998). In addi ion, he g ea e species ichness o he ben hic (oc opuses) and nek oben hic (cu le ishes and sepiolids) o ms compa ed o he pelagic (squid) ones (see Figu e 1) may indica e he impo ance o seabed (i.e., co al ee habi a ) complexi y and he e ogenei y as a d i ing o ce in sympa ic and/o pa apa ic specia ion p ocesses in he ben hic and nec oben hic g oups. 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The use, dis ibu ion o ep oduc ion in o he o ums is pe mi ed, p o ided he o iginal au ho (s) and he copy igh owne (s) a e c edi ed and ha he o iginal publica ion in his jou nal is ci ed, in acco dance wi h accep ed academic p ac ice. No use, dis ibu ion o ep oduc ion is pe mi ed which does no comply wi h hese e ms. F on ie s in Ma ine Science | www. on ie sin.o g 16 Augus 2019 | Volume 6 | A icle 469