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. The ela i ely low le els o endemism
in he CIP (g een colo s in Figu e 7E) and he highe numbe
o sha ed species in bo h he TNP and TAUS (Figu e 3) a e
sugges i e ha he IAA was a cen e o o igin and a sou ce o
species o cephalopod communi ies in he No h Wes e n Paci ic
and Indian Oceans.
Richness Declines F om CIP o EIP
Figu e 4 e eals a s iking di e ence be ween he CIP and
EIP species ichness le els, and a d as ic shi om a ho spo
( o me ) o a coldspo (la e ) in adjacen ealms. Such a s eep
longi udinal cline is no seen in o he ma ine axa (S ua -Smi h
e al., 2013;Rami ez e al., 2017). Fo ins ance, Mo a e al. (2003)
F on ie s in Ma ine Science | www. on ie sin.o g 9Augus 2019 | Volume 6 | A icle 469
ma s-06-00469 Augus 1, 2019 Time: 18:37 # 16
Rosa e al. Global Biogeog aphy o Coas al Cephalopods
Randall, J. E. (1998). Zoogeog aphy o sho e ishes o he Indo-Paci ic egion. Zool.
S ud. 37, 227–268.
Reid, W. V. (1998). Biodi e si y ho spo s. T ends Ecol. E ol. 13, 275–280.
Reime , J. D., Biondi, P., Lau, Y. W., Masucci, G., Nguyen, X. H., San os, M. E. A.,
e al. (2019). Ma ine biodi e si y esea ch in he Ryukyu Islands, Japan: cu en
s a us and ends. Pee J 7:e6532. doi: 10.7717/pee j.6532
Renema, W., Bellwood, D. R., B aga, J. C., B om ield, K., Hall, R., Johnson, K. G.,
e al. (2008). Hopping ho spo s: global shi s in ma ine Biodi e si y. Science 321,
654–657. doi: 10.1126/science.1155674
Rodhouse, P. G. (2013). Role o squid in he Sou he n Ocean pelagic ecosys em
and he possible consequences o clima e change. Deep Sea Res. II 95, 129–138.
doi: 10.1016/j.ds 2.2012.07.001
Rosa, R., Die ssen, H. M., Gonzalez, L., and Seibel, B. A. (2008a). Ecological
biogeog aphy o cephalopod molluscs in he A lan ic Ocean: his o ical and
con empo a y causes o coas al di e si y pa e ns. Glob. Ecol. Biogeog . 17,
600–610. doi: 10.1111/j.1466-8238.2008.00397.x
Rosa, R., Die ssen, H. M., Gonzalez, L., and Seibel, B. A. (2008b). La ge-scale
di e si y pa e ns o cephalopods in he A lan ic open ocean and deep-sea.
Ecology 89, 3449–3461. doi: 10.1890/08-0638.1
Rosa, R., Gonzalez, L., Die ssen, H. M., and Seibel, B. A. (2012). En i onmen al
de e minan s o la i udinal size- ends in cephalopods. Ma . Ecol. P og. Se . 464,
153–165. doi: 10.3354/meps09822
Sales, J. B. L., Haimo ici, M., Ready, J. S., Souza, R. F., Fe ei a, Y., Pinon,
J. C. S., e al. (2019). Su eying cephalopod di e si y o he Amazon ee
sys em using samples om ed snappe s omachs and desc ip ion o a new
genus and species o oc opus. Sci. Rep. 9:5956. doi: 10.1038/s41598-019-
42464-8
Sales, J. B. L., Ma kaida, U., Shaw, P. W., Haimo ici, M., Ready, J. S., Figue edo-
Ready, W. M. B., e al. (2014). Molecula phylogeny o he genus Lolliguncula
S eens up, 1881 based on nuclea and mi ochond ial DNA sequences indica es
gene ic isola ion o popula ions om no h and sou h A lan ic, and he possible
p esence o u he c yp ic species. PLoS One 9:e88693. doi: 10.1371/jou nal.
pone.0088693
Sche , H. D., Whi ake , J. M., Williams, S. E., La ime , J. C., Ko desch, W. E.,
and Delaney, M. L. (2015). Onse o An a c ic Ci cumpola cu en 30 million
yea s ago as Tasmanian Ga eway aligned wi h wes e lies. Na u e 523:580. doi:
10.1038/na u e14598
Spalding, M. D., Fox, H. E., Halpe n, B. S., Mcmanus, M. A., Molna , J., Allen, G. R.,
e al. (2007). Ma ine eco egions o he wo ld: a bio egionaliza ion o coas al and
shel a eas. Bioscience 57, 573–583. doi: 10.1641/b570707
S ugnell, J. M., Roge s, A. D., P odohl, P. A., Collins, M. A., and Allock, A. L.
(2008). The he mohaline exp essway: he Sou he n Ocean as a cen e o o igin
o deep-sea oc opuses. Cladis ics 24, 853–860. doi: 10.1111/j.1096-0031.2008.
00234.x
S ua -Smi h, R. D., Ba es, A. E., Le check, J. S., Du y, J. E., Bake , S. C., Thomson,
R. J., e al. (2013). In eg a ing abundance and unc ional ai s e eals new
global ho spo s o ish di e si y. Na u e 501, 539–542. doi: 10.1038/na u e
12529
Sunday, J. M., Ba es, A. E., and Dul y, N. K. (2012). The mal ole ance and he
global edis ibu ion o animals. Na . Clim. Change 2, 686–690. doi: 10.1038/
nclima e1539
Ti enso , D. P., Mo a, C., Je z, W., Lo ze, H. K., Rica d, D., Vanden Be ghe, E.,
e al. (2010). Global pa e ns and p edic o s o ma ine biodi e si y ac oss axa.
Na u e 466, 1098–U1107. doi: 10.1038/na u e09329
T on elj, P., and Fiše , C. (2009). Pe spec i es: c yp ic species di e si y should
no be i ialised. Sys . Biodi e s. 7, 1–3. doi: 10.1017/s147720000800
2909
Ulloa, P. M., He nández, C. E., Ri e a, R. J., and Ibáñez, C. M. (2017). Biogeog a iía
his oó ica de los calama es de la amilia Loliginidae (Teu hoidea: Myopsida).
La . Am. J. Aqua . Res. 45, 113–129.
Vecchione, M., Allcock, L., Pia kowski, U., Jo genson, E., and Ba a , I. (2009).
“Pe sis en ele a ed abundance o oc opods in an o e ished An a c ic a ea,”
in Smi hsonian a he Poles. Con ibu ions o In e na ional Pola Yea Science,
eds I. K upnik, M. A. Lang, and S. E. Mille (Washing on, DC: Smi hsonian
Ins i u ion Schola ly P ess), 197–203.
Ve meij, G. J. (1993). The biological his o y o a seaway. Science 260, 1603–1604.
doi: 10.1126/science.260.5114.1603
Villanue a, R., Vidal, E. A. G., Fe nández-Ál a ez, F. Á, and Nabhi abha a, J.
(2016). Ea ly mode o li e and ha chling size in cephalopod molluscs: in luence
on he species dis ibu ional anges. PLoS One 11:e0165334. doi: 10.1371/
jou nal.pone.0165334
Voigh , J. R. (1988). T ans-Panamanian gemina e oc opods (Mollusca: Oc opoda).
Malacologia 29, 289–294.
Woodland, D. J. (1983). Zoogeog aphy o he Siganidae (Pisces): an in e p e a ion
o dis ibu ion and ichness pa e ns. Bull. Ma . Sci. 33, 713–717.
Wo m, B., Lo ze, H. K., and Mye s, R. A. (2003). P eda o di e si y ho spo s in
he blue ocean. P oc. Na l. Acad. Sci. U.S.A. 100, 9884–9888. doi: 10.1073/pnas.
1333941100
Xa ie , J. C., Allcock, A. L., Che el, Y., Lipinski, M. R., Pie ce, G. J., Rodhouse,
P. G. K., e al. (2015). Fu u e challenges in cephalopod esea ch. J. Ma . Biol.
Assoc. U. K. 95, 999–1015. doi: 10.1017/s0025315414000782
Xa ie , J. C., Che el, Y., Allcock, L., Rosa, R., Sabi o , R. M., Bliche , M. E.,
e al. (2018). A e iew on he biodi e si y, dis ibu ion and ophic ole o
cephalopods in he A c ic and An a c ic ma ine ecosys ems unde a changing
ocean. Ma ine Biology 165, 93.
Xa ie , J. C., Peck, L. S., F e well, P., and Tu ne , J. (2016a). Clima e change and
pola ange expansions: could cu le ish ac oss he A c ic? Ma . Biol. 163:78.
Xa ie , J. C., Raymond, B., Jones, D. C., and G i i hs, H. (2016b). Biogeog aphy
o cephalopods in he Sou he n Ocean using habi a sui abili y p edic ion
modelsEcosys ems 19, 220–247. doi: 10.1007/s10021-015-9926-1
Xa ie , J. C., Rodhouse, P. G., T a han, P. N., and Wood, A. G. (1999). A
geog aphical in o ma ion sys em (GIS) a las o cephalopod dis ibu ion in he
Sou he n Ocean. An a c . Sci. 11, 61–62. doi: 10.1017/s0954102099000097
Ya su, A., Chiba, S., Yamanaka, Y., I o, S.-I., Shimizu, Y., Kae iyama, M., e al.
(2013). Clima e o cing and he Ku oshio / Oyashio ecosys em. ICES J. Ma .
Sci. 70, 922–933. doi: 10.1093/icesjms/ s 084
Zeidbe g, L. D., and Robison, B. H. (2007). In asi e ange expansion by he
Humbold squid, Dosidicus gigas, in he eas e n No h Paci ic. P oc. Na l. Acad.
Sci. U.S.A. 104, 12948–12950. doi: 10.1073/pnas.0702043104
Con lic o In e es S a emen : GB was employed by he company A ion.
The emaining au ho s decla e ha he esea ch was conduc ed in he absence o
any comme cial o inancial ela ionships ha could be cons ued as a po en ial
con lic o in e es .
Copy igh © 2019 Rosa, Pissa a, Bo ges, Xa ie , Gleadall, Goliko , Bello, Mo ais,
Lishchenko, Rou a, Judkins, Ibáñez, Pia kowski, Vecchione and Villanue a. This
is an open-access a icle dis ibu ed unde he e ms o he C ea i e Commons
A ibu ion License (CC BY). 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