ORIGINAL ARTICLE
Looking o long- e m changes in hyd oid assemblages (Cnida ia,
Hyd ozoa) in Albo an Sea (Sou h-Wes e n Medi e anean):
a p oposal o a moni o ing poin o he global wa ming
Manuel Ma ı
´a Gonza
´lez-Dua e •Cesa Megina •
S e ano Pi aino
Recei ed: 21 Feb ua y 2014 / Re ised: 8 July 2014 / Accep ed: 15 July 2014 / Published online: 5 Augus 2014
ÓSp inge -Ve lag Be lin Heidelbe g and AWI 2014
Abs ac In he las 20–30 yea s, he empe a u e o he
Medi e anean Sea has inc eased and global wa ming is
allowing he es ablishmen o opical-a ini y species in o
mo e empe a e zones. Sessile communi ies a e pa icula ly
use ul as a baseline o ecological moni o ing; howe e , a
lack o his o ical da a se ies exis s o sessile ma ine
o ganisms wi hou comme cial in e es . Hyd oids a e
ubiqui ous componen s o he ben hic sessile auna on
ocky sho es and ha e been used as bio-indica o s o
en i onmen al condi ions. In his s udy on he ben hic
hyd oid assemblages o he Cha a inas Islands (Albo an
Sea, Sou h-Wes e n Medi e anean), we cha ac e ized he
hyd oid assemblages, iden i ied he ba hyme ic g adien s,
and compa ed hem wi h a p e ious s udy ca ied ou in
1991. Hyd oid assemblages showed a signi ican di e ence
bo h be ween yea and among dep hs. Fu he mo e, eigh
species no p esen in 1991 we e ound, including wo
possible new species and he opical and sub opical spe-
cies Se ula ia ma gina a. Due o i s s a egic posi ion a
he en ance o he Medi e anean and he exis ence o
p e ious da a on hyd oid assemblages, he Cha a inas
Islands a e p oposed as a possible moni o ing poin o
en ance o A lan ic opical species in o he Medi e anean
Sea.
Keywo ds Global wa ming Medi e anean Sea 
Hyd oid assemblages Cha a inas Islands Albo an Sea 
Moni o ing poin
In oduc ion
Reliable e idence demons a es ha he clima e is chang-
ing, and he a e age su ace empe a u e o he sea is
inc easing (B ie ley and Kings o d 2009). In he las dec-
ades, he mean su ace empe a u e has inc eased in he
Medi e anean (Nykjae 2009; Skli is e al. 2012) and, o
example, he Albo an Sea (Wes e n Medi e anean) has
shown a ise o he supe icial a e age empe a u e o
0.5 °C since he ea ly 1990s–2005 (Va gas Ya
´n
˜ez e al.
2007). The clime is an impo an de e minan in he ange
o dis ibu ion o species (Thomas 2010), and apid cli-
ma ic changes a e associa ed wi h changes in he dis i-
bu ional ange o he species (Hughes 2000; Ha ley e al.
2006). This oge he wi h o he an h opogenic impac s o
global e ec s, such as wo ldwide ansloca ion o species
and he associa ed biological in asions and ocean acidi i-
ca ion, is changing he composi ion o he communi ies
(Wal he e al. 2002; Occhipin i-Amb ogi 2007; B ie ley
and Kings o d 2009). Global wa ming, he inc ease o he
wa m season and human-media ed species ansloca ion
a e allowing he species o opical a ini y o mo e in o
mo e empe a e zones (Hughes 2000).
The clima e a ia ions modi y he dis ibu ion pa e ns
o he ma ine species in he Medi e anean Sea and nea by
wa e s esul ing in a p ocess known as ‘‘ opicaliza ion’’
(Bianchi 2007). This phenomenon is a ou ed by h ee
Communica ed by H. -D. F anke.
M. M. Gonza
´lez-Dua e (&)
Cen e o Ma ine Conse a ion, Depa amen o de Ecologı
´a,
Pon i icia Uni e sidad Ca o
´lica de Chile, Casilla 193, Co eo 22,
San iago, CP 6513677, Chile
e-mail: [email p o ec ed]; [email p o ec ed]
C. Megina
Dp o. de Zoologı
´a, Uni e sidad de Se illa, Se illa, Spain
S. Pi aino
DisTeBa, Uni e si a
`del Salen o, Lecce, I aly
123
Helgol Ma Res (2014) 68:511–521
DOI 10.1007/s10152-014-0406-3
main elemen s: (1) he con inuous en ance o A lan ic
species in o he Medi e anean since he opening o he
S ai o Gib al a in he basal Pliocene (Boe o e al. 2003);
(2) he opening o he Suez Canal in 1869 pe mi ed he
en ance o species om he Red Sea, gene ally con ined o
he Eas e n Medi e anean (Bianchi and Mo i 2000; Mo i
e al. 2009); and (3) he di ec in oduc ion o exo ic spe-
cies, mos o hem o wa m-wa e a ini y, by ac i i ies
such as ma i ime a ic o aquacul u e ha cons i u es an
addi ional sou ce o species o Medi e anean Fauna (Za-
i se and O
¨z u
¨ k 2001).
The s udy o he di e si y and composi ion o ma ine
communi ies is he i s s ep in unde s anding he de el-
opmen o ma ine ecosys ems (Elahi e al. 2013). Fu -
he mo e, he changes in he abundance and composi ion o
species a e he main ac o s o ob ain in o ma ion abou he
dynamic o communi ies (Micheli e al. 1999). Howe e ,
he lack o his o ical da a is he main p oblem o ela ing
changes in ma ine communi ies wi h clima ic changes
(Sou hwa d 1995; Hawkins e al. 2003; Vandepi e e al.
2010). Sessile communi ies a e pa icula ly use ul as a
e e ence o ecological moni o ing (Ca ballo e al. 1996;
Na anjo e al. 1996; Gue a-Ga cı
´a e al. 2006; Gonza
´lez-
Dua e e al. 2013a). Al hough conspicuous g oups a e no
su icien o app ecia e ma ine biodi e si y and o unde -
s and i s unc ioning (Boe o e al. 2003), mos s udies abou
long- e m changes in ma ine communi ies a e ocused on
plank on (Degobbis e al. 1995; Beaug and and Ibanez
2004; Moline o e al. 2007) o comme cial species: ish-
e ies (Golani e al. 2002), c us acea (Galil e al. 2002)o
mollusks (Zene os e al. 2004). Indeed, Bu ows e al.
(2011) ci ed he s udy o Puce e al. (2009) on he hyd oid
assemblages in he Ligu ian Sea (Cen al Medi e anean)
as he only epo o he e ec s o global wa ming on
ma ine ben hic o ganisms.
Mos o he his o ical da a a e di icul o compa e
because hey we e no usually collec ed wi h he pu pose o
a s anda dized compa ison wi h u u e s udies. Howe e ,
due o he c i ical impo ance o asce aining changes in
ma ine communi ies associa ed wi h global wa ming, some
esea che s a e a p esen acing he challenge o analysis
o dispa a e da ase s coming om p e ious s udies (Elahi
e al. 2013). In he absence o adequa e eplica ed his o ical
da a, he a ailable da a a e o en he only possible chance
o s udy long- e m changes (B adshaw e al. 2002). Indeed,
one common p ac ice in he s udies abou global wa ming
is he compa ison o di e en wo ks, especially i he
sampling designs a e simila , bu no iden ical (Elahi e al.
2013) (e.g. Puce e al. 2009). We es ed ou esul s by
pe o ming a compa ison wi h simila s udies in he Med-
i e anean Sea.
Wi h ega d o hyd oids, hey a e among he mos
impo an componen s o ben hic communi ies on ocky
sho es (Boe o 1984; Gili and Hughes 1995; Bouillon e al.
2006), being usually p esen wi h a la ge numbe o colo-
nies and species (Boe o and F esi 1986; Gili and Hughes
1995; Pi aino e al. 2002). They a e among he i s o
colonize i gin subs a es, bu hey a e also p esen in la e
s ages o communi y de elopmen (Boe o 1984; Mo i and
Boe o 1986; Gili and Hughes 1995). They also se e as a
ophic sou ce and p o ide seconda y subs a es o many
in e eb a es (Di Camilo e al. 2013). Thei ben hic
assemblages ha e some p ope ies ha make hem a e y
in o ma i e model o en i onmen al and ecological s ud-
ies (Gili and Hughes 1995; Gonza
´lez-Dua e e al. 2013a;
Megina e al. 2013). Thus, he empe a u e is a c i ical
ac o o he ben hic hyd oid communi ies, a ec ing c u-
cial aspec s o hei li e cycle and biology: hei season-
ali y, he a e o oxygen consump ion, s olon egene a ion,
e c. (Boe o 1984; Boe o and F esi 1986; Gili and Hughes
1995; Ba es ello e al. 2006). Fu he mo e, hey a e
common componen s o ouling communi ies being e-
quen ly in ol ed in in oduc ion and in asion phenomena
since he globaliza ion o ma i ime ou es (Boe o 1984;
Boe o e al. 2003; G a ili e al. 2008); some o hem a e
conside ed as pe ec in ade s because hei li e cycles
include encys men phases o abili y o e e se de elop-
men (Boe o 2002; Megina e al. 2013).
The hyd oid assemblages o he Po o ino P omon o y
(Ligu ian Sea) we e ex ensi ely s udied be ween 1976 and
1983 (Boe o 1984; Boe o and F esi 1986; Boe o e al.
1986; Mo i and Boe o 1986). This pool o da a allowed
Puce e al. (2009) o in es iga e he changes in hyd oid
assemblages and o e alua e he in luence o global
wa ming on he ben hic ma ine ecosys em.
Simila ly, in 1991, Pen
˜a Can e o and Ga cı
´a Ca ascosa
(2002) conduc ed ex ensi e aunis ic esea ch abou
hyd oid assemblages o he Cha a inas Islands (Albo an
Sea, Wes e n Medi e anean). They iden i ied he species
p esen , hei subs a es and zona ion pa e n in dep h.
As a i s s ep, we s udied he ben hic hyd oid assem-
blages on ha d bo om o he Cha a inas Islands in he
summe o 2007. We used a s anda dized sampling design
o explo e he ho izon al a iabili y in hese assemblages,
iden i ying he ba hyme ic g adien s and he species
composi ion. La e , we compa ed hese da a wi h he p e-
ious census, 16 yea s p e iously, o e eal possible
changes in he hyd oid assemblages on ha d bo om.
Finally, we compa ed ou esul s wi h simila wo ks ca ied
ou in he Medi e anean Sea (i.e. Puce e al. 2009), which
es ablished a ela ionship be ween global wa ming and
changes in hyd oid assemblages. We p o ide in o ma ion
abou hyd oid assemblages o he Cha a inas as a baseline
s udy, and we p opose his a chipelago as a poin o
moni o ing he long- e m changes in he ben hic commu-
ni ies o he Albo an Sea and Wes e n Medi e anean.
512 Helgol Ma Res (2014) 68:511–521
123
Ma e ials and me hods
Sampling and so ing
Hyd oid sampling was ca ied ou in he a chipelago o
Cha a inas in summe (Augus 2007), as well as p e ious
s udy (Pen
˜a Can e o and Ga cı
´a Ca ascosa 2002). Cha a-
inas islands a e a p o ec ed a ea wi h es ic ed access due
o mili a y su eillance, whe e only scien i ic ac i i ies a e
allowed in bo h he e es ial and ma ine en i onmen , so
ha di ec an h opogenic in luence is minimal. I is si ua ed
in he Albo an Sea (Wes e n Medi e anean), nea he
No h A ican coas (35°10045.3300N; 2°25049.4900W).
Th ee olcanic islands o m he Cha a inas a chipelago
(‘‘Cong eso’’, ‘‘Isabel II’’ and ‘‘Rey F ancisco’’) close o
he mou h o he Ouad-Moulouya Ri e . Two sampling
poin s we e selec ed a he eas e nmos and wes e nmos
ends o he a chipelago o conside he in e nal geog aph-
ical a iabili y, and wo eplica e andom ansec s a each
poin , om some me es o ens o me es apa (Fig. 1).
Each ansec was subdi ided in o ou dep h bands
(0/-5m,-5/-10 m, -10/-15 m and -15/-20 m) ol-
lowing he me hodology o Boe o and F esi (1986).
Samplings we e ca ied ou by SCUBA di ing using
isual collec ion echniques, which has been shown o
e icien ly ep esen he hyd oid di e si y in shallow
coas al ben hic habi a s (Boe o and F esi 1986; Puce e al.
2009; Gonza
´lez-Dua e e al. 2013a; Megina e al. 2013).
Samples we e p ese ed ei he in e hanol 90 % o in o -
malin 4 %. Specimens we e so ed and iden i ied o he
maximum le el o axonomic esolu ion possible, in mos
cases o speci ic le el. The abundance o e e y axon was
es ima ed by coun ing he numbe o polyp-bea ing hy-
d ocauli (s ems) in he sample (see Gonza
´lez-Dua e e al.
2013a; Megina e al. 2013).
In he p esen s udy, we compa ed ou esul s wi h he
p e ious wo k ca ied ou by Pen
˜a Can e o and Ga cı
´a
Ca ascosa (2002) in he Cha a inas Islands. They did
epo in o ma ion abou ansec s, s a ions on e e y an-
sec and species lis , oge he wi h dep h and subs a e o
each species. Hyd oids a e a he non-speci ic (wi h a ew
excep ions) and can be p esen in a high numbe o di -
e en subs a es in a gi en a ea (Co nelius 1982; Calde
1991; Gili and Balles e os 1991; Genzano and Rod iguez
1998). Thus, we coun ed he imes ha each species was
p esen on a di e en subs a e as an indica ion o hei
ela i e abundance. I allowed a mo e sensi i e compa ison
o ou da a wi h hose om he s udy o Pen
˜a Can e o and
Ga cı
´a Ca ascosa (2002). The aunis ic s udy ca ied ou
by Pen
˜a Can e o and Ga cı
´a Ca ascosa (2002) was also
based on se e al ansec s in dep h, bu wi h a di e en
quan i y and dis ibu ion o hem. Fo a mo e sensible
compa ison accoun ing o spa ial a iabili y wi hin he
a chipelago and wi h dep h g adien , we g ouped he
samples o each island and each dep h band in he wo
sampling pe iods. The wo sampling pe iods unde com-
pa ison (1991 and 2007) we e conduc ed in summe ;
he e o e, he seasonal a ia ions a e no aken in o
accoun . Fu he mo e, o a oid a i icial di e ences bu
ying o p ese e he maximum in o ma ion o simila i ies
o di e ences be ween samples, all he specimens which
could no be eliably sepa a ed as belonging o di e en
species, due o he lack some diagnos ic in o ma ion ( e -
ile ma e ial, a jelly ish s age o any o he cha ac e s), we e
g ouped oge he (some imes by genus, some imes by a
g oup o species wi hin a genus): Scandia spp.; La oeina
enuis/Egmundella ami an ensis;Filellum disagg ega um
and Filellum sp.1 sensu Pen
˜a Can e o and Ga cia Ca as-
cosa (2002)asFilellum sp.1 and Filellum se pens and
Filellum sp.2 sensu Pen
˜a Can e o and Ga cia Ca ascosa
(2002)asFilellum sp.2.
Da a analysis
In he s udy o hyd oid assemblages in 2007 conside ed
wo ac o s, ‘‘Dep h’’ and ‘‘Island’’. In compa ison be ween
Fig. 1 Cha a inas a chipelago
and i s posi ion in he Wes e n
Medi e anean showing he wo
ansec s sampled on each
sampling poin : ‘‘Cong eso
Island’’ (C) and ‘‘Rey Island’’
(R)
Helgol Ma Res (2014) 68:511–521 513
123
1991 and 2007, we conside ed wo ac o s, ‘‘Dep h’’ and
‘‘Yea ’’, conside ing he islands as eplica es. The da a
we e o ganized in species/sample abundance ma ix.
A B ay-Cu is simila i y ma ix was calcula ed as a dis-
ance measu e among samples (B ay and Cu is 1957)on
squa e oo - ans o med da a in he analysis o he hyd oid
assemblages in 2007 and on s anda dized da a o minimize
he po en ial e ec o di e en sampling e o s, in com-
pa ison wi h Pen
˜a Can e o and Ga cı
´a Ca ascosa (2002)
da a. We used a dis ance-based pe mu a ional mul i a ia e
analysis o a iance (PERMANOVA) (Ande son 2001;
McA dle and Ande son 2001) o pa i ion a iance in
assemblage composi ion acco ding o he abo e designs.
When app op ia e, signi ican e ms in he ull model we e
analysed indi idually using pai -wise compa ison wi h he
PERMANOVA es . The homogenei y o mul i a ia e
dispe sion among he g oups o each ac o o in e es was
es ed by PERMDISP (Ande son 2006).
The dissimila i ies among samples we e ep esen ed by
non-me ic mul idimensional scaling o dina ions (nMDS,
(Cla ke 1993)). SIMPER (Cla ke 1993) was used o iden-
i y he pe cen age con ibu ion ha each axon made o he
measu es o simila i y wi hin (o dissimila i y among) he
di e en le els o he ixed ac o s o which signi ican
di e ences we e ound. The a io a e age simila i y/s an-
da d de ia ion (SIM/SD) and a e age dissimila i y/s an-
da d de ia ion (DISS/SD) a e use ul measu es o how
consis en ly a componen o he assemblage ypi ies a
g oup o disc imina es be ween g oups (Cla ke and Wa -
wick 2001). We abula ed he axa wi h hese a ios la ge
han o equal o 1.4 (Gonza
´lez-Dua e e al. 2013a; Megina
e al. 2013). Mul i a ia e analyses we e pe o med using
he so wa e PRIMER 6.1.11 and PERMANOVA ?
1.0.1 s a is ical package (Cla ke and Go ley 2006).
Addi ionally, we examined he numbe o species in he
explo ed assemblages in a wo-way ANOVA, wi h a sim-
ila design o ha explained abo e. This analysis was done
using S a is ica 6.0 package (S a so Inc 2001).
Resul s
Hyd oid assemblages in 2007
The nMDS plo s in Fig. 2show he di e en dis ibu ion o
he samples om he wo islands based on hyd oid
assemblages, al hough his esul was only ma ginally
signi ican (Table 1). The samples also showed a e ical
zona ion in dep h, wi h he samples be ween 0 and 10 m
and samples be ween 15 and 20 m in dep h as wo di e en
g oups. These wo g oups we e mo e e iden in Rey Island
han Cong eso Island. The PERMANOVA showed signi -
ican di e ences in he mul i a ia e s uc u e o hyd oid
assemblages among dep hs. Pai -wise compa ison showed
a clea g adien in dep h (Table 2). This es did no show
signi ican di e ences be ween con iguous dep h bands and
showed signi ican di e ences be ween mo e sepa a ed
ones. The in e ac ions be ween hese wo ac o s (‘‘dep h’’
and ‘‘islands’’) we e no signi ican ; hus, he di e ences
wi h dep h did no change signi ican ly be ween sampling
poin s.
0
5
10 15
05
10
15
0
5
10
15
0
5
10
15
Fig. 2 Non-me ic mul i-dimensional scaling o dina ion o he sam-
pled hyd oid assemblages on he basis o he B ay–Cu is dissimi-
la i y. In e ed iangle Rey Is.; squa e Cong eso Is.; 0 =0/-5m;
5=-5/-10 m; 10 =-10/-15 m and 15 =-15/-20 m
(s ess =0.15)
Table 1 Resul s o PERMANOVA pa i ioning spa ial a ia ion in
hyd oid assemblage composi ion in 2007
d SS MS Pseudo-F P(pe m)
Dep h 3 5,541.3 1847.1 2.3988 0.003*
Island 1 1,602.7 1,602.7 2.0813 0.053
Dep h 9Island 3 2,820.8 940.26 1.2211 0.225
Residual 8 6,160.1 770.01
To al 15 16,125
* Signi ican di e ences a P 0.05
Table 2 Resul s o pai -wise compa ison o he ixed ac o ‘‘dep h’’
o he hyd oid assemblages in 2007
G oups P(pe m)
0–5 0.969 0.555
0–10 1.732 0.026*
0–15 2.034 0.028*
5–10 1.380 0.099
5–15 1.749 0.044*
10–15 1.227 0.214
(0 =0/–5 m; 5 =–5/–10 m; 10 =–10/–15 m; 15 =–15/–20 m).
* Signi ican di e ences a P 0.05
514 Helgol Ma Res (2014) 68:511–521
123
Table 3shows he 21 mos signi ican species (SIM/
SD C1.4) o cha ac e ize he di e en dep h bands
acco ding o SIMPER analysis. Aglaophenia ki chenpau-
e i,An ennella ansini, Campanula ia hincksii,Cly ia
linea is,Filellum sp.1 and Halecium lankes e i cha ac e -
ized he assemblages a he ou dep h bands. An hohebella
pa asi ica,Cly ia g acilis,Cly ia hemisphae ica and
Dynamena dis icha cha ac e ized he supe icial dep hs
(0–10 m). On he o he hand, Halecium enellum,Salacia
desmoides,Scandia spp., Se ula ella ellisii,Se ula ella
polyzonias and Se ula ia dis ans cha ac e ized he deepe
samples (10–20 m). Figu e 3 isually ep esen s he
abundances ac oss he di e en sampling dep hs o he
mos ep esen a i e species iden i ied by he SIMPER
analysis.
The uni a ia e analysis did no show signi ican di e -
ences be ween islands o among dep hs o he numbe
o species (Dep h: F
3
=0.154, p=0.920; Island:
F
1
=2.727, p=0.197).
Two species belonging o he genus Halecium could no
be assigned o any o he known species, and hey a e
possible new species. Al hough beyond he scope o his
pape , he desc ip ion and discussion he iden i y o his
ma e ial will be p esen ed in u u e publica ions.
Long- e m changes in he hyd oid assemblages 1991
e sus 2007
The nMDS showed a clea sepa a ion in he mul i a ia e
s uc u e o hyd oid assemblage be ween 1991 and 2007
(Fig. 4). Resul s o he mul i a ia e analyses using PER-
MANOVA a e epo ed in Table 4and e ealed signi ican
di e ences in he s uc u e o he hyd oid assemblages
be ween 1991 and 2007 and among dep hs. The in e ac-
ions be ween hese wo ac o s we e no signi ican ly
di e en ; hus, he e we e no signi ican changes in he
a ia ion o hyd oid assemblages wi h dep h g adien du -
ing hese pe iods. Pai -wise compa ison among dep hs also
showed a e ical g adien o he hyd oid assemblages
(Table 5).
The SIMPER analysis iden i ied 16 species as con ib-
u ing mos o he cha ac e iza ion o he assemblages in one
o he o he sampling pe iod o o di e en ia e hem
(Table 6). Fou species cha ac e ized he hyd oid assem-
blage in he wo pe iods: An ennella ansini,Campanula ia
hincksii,Cly ia linea is and Halecium lankes e i. Only
Scandia spp. cha ac e ized exclusi ely he hyd oid
assemblage in 1991 (SIM =45.71 %). Eigh axa cha ac-
e ized he hyd oid assemblage in 2007 (SIM =57.35 %)
and we e no cha ac e is ics in 1991: Aglaophenia ki -
chenpaue i,Aglaophenia ubi o mis,Cly ia g acilis,
Filellum sp.1, Ki chenpaue ia pinna a,Obelia dicho oma,
Se ula ella ellisii and Se ula ia dis ans. Ele en species
con ibu ed signi ican ly o he dissimila i ies be ween
pe iods (DISS =57.88 %): A.ki chenpaue i,An hohe-
bella pa asi ica,C.g acilis,C. linea is,Filellum sp.1,
Halecium delica ulum,H. lankes e i,O.dicho oma,
Plumula ia se acea,S.ellisii and S. dis ans. Figu e 5
isually ep esen s he abundances o mos ep esen a i e
species ha con ibu ed o he dissimila i y be ween yea s
iden i ied by he SIMPER analysis.
Table 3 SIMPER analysis
A e age o simila i y
0–5 m
(54.75 %)
5–10 m
(56.56 %)
10–15 m
(62.07 %)
15–20 m
(60.98 %)
Aglaophenia
ki chenpaue i
4.22 3.7 3.42 4.7
Aglaophenia
ubi o mis
1.91 4.88 3.55 –
An ennella
ansini
4.44 4.54 5.39 4.41
An hohebella
pa asi ica
3.87 2.02 – –
Campanula ia
hincksii
4.1 3.14 4.23 4.79
Cly ia g acilis 3.93 5.31 – –
Cly ia
hemisphae ica
2.01 – – –
Cly ia linea is 5.28 2.67 4.03 4.5
Dynamena
dis icha
4.76 5.03 – –
Filellum sp.1 2.94 3.14 5.54 4.67
Halecium beani 3.51 – 2.14 –
Halecium
delica ulum
– 3.17 2.13 –
Halecium
lankes e i
3.38 2 6.31 5.83
Halecium
enellum
– – – 4.39
Ki chenpaue ia
pinna a
– 3.02 2.13 –
Obelia
dicho oma
– 2.7 – 2.87
Salacia
desmoides
–– 4 –
Scandia spp. – – – 7.09
Se ula ella
ellisii
– – 4.17 2.72
Se ula ella
polyzonias
– – – 2.41
Se ula ia
dis ans
– – 2.14 –
Species signi ican ly con ibu ing o he simila i y among dep hs in
2007 (a e age o simila i y/SD C1.4). Da a we e ans o med on
squa e oo
Helgol Ma Res (2014) 68:511–521 515
123

The uni a ia e analysis o he numbe o species by he
gene al linea model did no show signi ican di e ences
be ween yea s (F
1
=1.809; p=0.203) o among dep hs
(F
3
=0.183; p=0.905), wi h 60 being he o al numbe
o species collec ed in 2007 and 66 in 1991.
F om a quali a i e poin o iew, 15 species sampled in
1991 we e no ound in 2007, and eigh species had no
p e iously been eco ded o he Cha a inas Islands
(Table 7).
Discussion
Ve ical zona ion is he mos ob ious dis ibu ion pa e n o
ha d-bo om communi ies, o en explained in ela ion o
en i onmen al ac o s such as ligh , empe a u e and wa e
mo emen (Te lizzi and Schiel 2009). A e ical zona ion
in dep h seems o be he ule o hyd oids (Boe o and F esi
1986). Indeed, a g adual a iabili y o he mul i a ia e
s uc u e o he hyd oid assemblages wi h dep h was gen-
e ally ound in he s udy zone, despi e he dep h ange
su eyed was be ween 0 and 20 m in dep h. Some species
(Fig. 3) we e pa icula ly illus a i e in his sense, showing
a con inuous dec ease o inc ease wi h dep h. Fo example,
Cly ia g acilis showed maximum abundances in he mo e
supe icial dep h, and Halecium lankes e i showed an
in e se end.
O e his gene al end, he e exis s sligh e idence o a
mo e ab up discon inui y be ween he mos supe icial
samples (0–10 m) and he deepes samples (10–20 m).
Indeed, some species we e almos exclusi ely p esen in
hese shallowes o deepes a eas. An hohebella pa asi ica
o Dynamena dis icha (0–10 m) and Scandia spp. o Se -
ula ella polyzonias (10–20 m) indica ed he sepa a ion
8
32
56
80
0
5
10 15
05
10
15
0
5
10
15
0
5
10
15
An hohebella
pa asi ica
20
80
140
200
0
5
10 15
05
10
15
0
5
10
15
0
5
10
15
Cly ia g acilis
20
80
140
200
0
5
10 15
05
10
15
0
5
10
15
0
5
10
15
Dynamena
dis icha
30
120
210
300
0
5
10 15
05
10
15
0
5
10
15
0
5
10
15
Halecium
lankes e i
30
120
210
300
0
5
10 15
05
10
15
0
5
10
15
0
5
10
15
Scandia spp.
3
12
21
30
0
5
10 15
05
10
15
0
5
10
15
0
5
10
15
Se ula ella
polyzonias
Fig. 3 Bubble plo o e ical zona ion o some species sampled in 2007 iden i ied by SIMPER analysis. Size o he bubbles is p opo ional o
he abundance o he ep esen ed species. (0 =0/–5 m; 5 =–5/–10 m; 10 =–10/–15 m; 15 =–15/–20 m) (s ess =0.15)
516 Helgol Ma Res (2014) 68:511–521
123
be ween supe icial and deepe samples. The dis ibu ion in
dep h o hese species is in ag eemen wi h o he s udies
ca ied ou in he Medi e anean Sea (Gili and Cas ello
`
1985; Boe o and F esi 1986; De Vi o 2006; Puce e al.
2009). The excep ion was Scandia spp., because hese
au ho s desc ibed he species belonging o his genus as
cha ac e is ics o a wide dep h ange o 0–30 m. This
discon inui y was mo e e iden in he samples om Rey
Island, whe e ansec s we e loca ed in he eas e nmos pa
o he a chipelago. In he deepes zones o hese sampling
poin s, he subs a e and ben hic o ganisms we e mo e
isibly co e ed wi h some muddy sedimen han in
Cong eso Island, pe haps om he Ri e Moulouya dis-
cha ge (Gualla and A an 2013), which could c ea e some
pa icula en i onmen al condi ions ending o inc ease he
sepa a ion be ween deepe and supe icial samples.
Ou compa ison o p e ious and p esen s udies in
Cha a inas sugges ed ha he hyd oid assemblage has
changed. Al hough he compa ison be ween s udies wi h
di e en me hodologies and sampling e o s mus be
conside ed wi h cau ion, some addi ional e idence and he
compa ison wi h simila s udies make ou esul s mo e
eliable. In ag eemen wi h Puce e al. (2009), he amily
Aglaopheniidae and Co ynidae showed a educ ion in hei
abundance and in he numbe o species; Cly ia g acilis
and Se ula ella polyzonias we e also epo ed as being
mo e abundan . In pa icula , eigh species o he genus
Aglaophenia we e collec ed in 1991, and his was educed
o ou in 2007. Ki chenpaue ia halecioides o Cly ia sp.
we e e y abundan species in 1991 ( hey we e p esen in a
high numbe o di e en subs a es), and hey we e no
ound in 2007.
The a ia ion o he hyd oid assemblages wi h he dep h
g adien , howe e , seems o ha e emained unchanged in
Cha a inas since 1991. Also, he o al numbe o species
did no show signi ican changes be ween he compa ed
0
5
10
15
0
5
10
15
0
5
1015
0
5
10
15
05
10
15
Fig. 4 Non-me ic mul i-dimensional scaling o dina ion o he sam-
pled hyd oid assemblages a Cha a inas Islands in 1991 ( iangle) and
2007 (squa e). 0 =0/-5m;5=-5/-10 m; 10 =-10/-15 m and
15 =-15/-20 m (s ess =0.11)
Table 4 Resul s o PERMANOVA pa i ioning spa ial a ia ion in
hyd oid assemblage composi ion in compa ison be ween yea s
d SS MS Pseudo-F P(pe m)
Yea 1 5,914.3 5,914.3 5.262 0.001*
Dep h 3 5,765.9 1,922 1.71 0.016*
Yea 9dep h 3 3,670.4 1,223.5 1.0,885 0.332
Residual 12 13,488 1,124
To al 19 29,600
* Signi ican di e ences a P 0.05
Table 5 Resul s o pai -wise compa ison o he ixed ac o ‘‘dep h’’
in compa ison be ween yea s
G oups P(pe m)
0–5 1.067 0.372
0–10 1.611 0.023*
0–15 1.793 0.015*
5–10 0.964 0.531
5–15 1.213 0.162
10–15 0.945 0.575
(0 =0/–5 m; 5 =–5/–10 m; 10 =–10/–15 m; 15 =–15/–20 m).
* Signi ican di e ences a P 0.05
Table 6 Species signi ican ly con ibu ing o cha ac e izing each
yea and he dissimila i y be ween 1991 and 2007 (a e age o simi-
la i y/SD C1.4)
SIM DISS
1991 2007 1991 e sus 2007
Aglaophenia ki chenpaue i – 5.53 3.15
Aglaophenia ubi o mis – 2.46 –
An ennella ansini 5.22 4.8 –
An hohebella pa asi ica – – 0.57
Campanula ia hincksii 3.27 3.64 –
Cly ia g acilis – 2.7 2.22
Cly ia linea is 4.41 6.88 2.76
Filellum sp.1 – 3.34 1.84
Halecium delica ulum – – 1.81
Halecium lankes e i 4.97 2.53 2.01
Ki chenpaue ia pinna a – 2.55 –
Obelia dicho oma – 2.01 1.77
Plumula ia se acea – – 0.55
Scandia spp. 12.89 – –
Se ula ella ellisii – 2.73 1.69
Se ula ia dis ans – 2.04 1.47
Da a we e s anda dized and squa e oo - ans o med da a.
SIM =A e age o Simila i y; DISS =A e age o Dissimila i y
Helgol Ma Res (2014) 68:511–521 517
123
pe iods. This is in ag eemen wi h o he s udies dealing
wi h long- e m changes in hyd oid assemblages wi h global
wa ming ha sugges ha he numbe o species ends o
emain s able, bu he s uc u e and composi ion o he
assemblages change (Puce e al. 2009; G a ili e al. 2013).
Al hough Pen
˜a Can e o and Ga cı
´a Ca ascosa (2002)
ca ied ou a aunis ic s udy wi h a highe sampling e o
( ime, dep h ange and numbe o samples) han ou s udy
in 2007, he samples in 2007 p o ided a good ep esen a-
ion o he global di e si y o hyd oid assemblages. How-
e e , i is a guable ha some a e species de ec ed in 1991
could ha e passed unno iced in 2007. The e o e, he spe-
cies only sampled in 2007 and no ound p e iously by
Pen
˜a Can e o and Ga cı
´a Ca ascosa (2002) a e pa icula ly
meaning ul (Table 7). Fo example, Se ula ia ma gina a
is a ci cum opical and sub opical species in oduced in o
he Medi e anean Sea (Bouillon e al. 2004; Mo i e al.
2009). The specimens o S.ma gina a collec ed in
Cha a inas cons i u ed he i s eco d o he wes e n
Medi e anean whe e his species may ha e ecen ly
expanded and na u alized in he Medi e anean (Gonza
´lez-
Dua e e al. 2013b).
The ben hic species can eac by a ying i s dis ibu ion
and abundance o changes in he empe a u e in he o de o
0.5 °C (Hiscock e al. 2004), such as he one obse ed in
he supe icial empe a u e in he Albo an Sea (Va gas
Ya
´n
˜ez e al. 2007). Hyd oids a e ex emely sensi i e in
hei biology and communi y s uc u e o clima ic changes
(Puce e al. 2009). Fu he mo e, global wa ming could
acili a e he in oduc ion and pos e io sp ead o non-
An hohebella
pa asi ica
0.3
1.2
2.1
3
1991
1991
1991
1991
1991
1991
1991
1991
1991
1991
19911991
2007
2007
2007
2007
2007
2007
2007
2007
Halecium
delica ulum
3
12
21
30
1991
1991
1991
1991
1991
1991
1991
1991
1991
1991
19911991
2007
2007
2007
2007
2007
2007
2007
2007
Obelia
dicho oma
2
8
14
20
1991
1991
1991
1991
1991
1991
1991
1991
1991
1991
19911991
2007
2007
2007
2007
2007
2007
2007
2007
Plumula ia
se acea
0.2
0.8
1.4
2
1991
1991
1991
1991
1991
1991
1991
1991
1991
1991
19911991
2007
2007
2007
2007
2007
2007
2007
2007
Scandia spp.
4
16
28
40
1991
1991
1991
1991
1991
1991
1991
1991
1991
1991
19911991
2007
2007
2007
2007
2007
2007
2007
2007
Cly ia g acilis
2
8
14
20
1991
1991
1991
1991
1991
1991
1991
1991
1991
1991
19911991
2007
2007
2007
2007
2007
2007
2007
2007
Fig. 5 Bubble plo o some species iden i ied by he SIMPER analysis con ibu ed o he dissimila i y be ween 1991 and 2007. Size o he
bubbles is p opo ional o he abundance o he ep esen ed species (s ess =0.11)
518 Helgol Ma Res (2014) 68:511–521
123
indigenous species in he Medi e anean Sea (Occhipin i-
Amb ogi and Sa ini 2003), pa icula ly hose o wa m-
wa e o igins. In gene al, wa m-wa e species a e expand-
ing hei dis ibu ional a eas, while cold-wa e species a e
showing a educ ion (CIESM 2002; Guide i e al. 2002).
Speci ically, in ou s udied a ea, opical A lan ic species
a e a i ing a he S ai o Gib al a and sp eading in o he
Medi e anean Sea, whe e he sou he n pa p esen s a
highe abundance o sub opical species (Lejeusne e al.
2010). Howe e , he No h A ican coas is usually no
well known (Pen
˜a Can e o and Ga cı
´a Ca ascosa 2002;
Zene os e al. 2005).
The Cha a inas a chipelago is a ma ine-p o ec ed a ea
isola ed om human ac i i ies, loca ed a he sou he n
coas o he Albo an Sea, in he en ance o he Medi e -
anean. I is highly in luenced by he asymme ic incoming
su ace A lan ic wa e s, di ec ly d i ing owa ds i s coas
(Candela 1991; Skli is and Becke s 2009; Gonza
´lez-Dua e
e al. 2013a). I is he e o e a e y app op ia e zone o
ea ly de ec ion o new en ances o opical A lan ic spe-
cies ha can po en ially sp ead in o he Medi e anean.
Gonza
´lez-Dua e e al. (2013a) desc ibed his asymme ical
in luence o he A lan ic wa e s as ex ending o ben hic
communi ies. These au ho s de ined an A lan ic In luence
Zone (A lan ic coas o he S ai o Gib al a and Sou he n
Albo an Sea), whe e he ben hic hyd oid assemblages ha e
a mo e A lan ic cha ac e . Iazza e al. (2013) also poin ed
ou he s ong ela ionship be ween he hyd oid auna in he
en ance o he Medi e anean and he Sou h A lan ic
Mo occan auna. Species a i ing om he A ican
A lan ic coas and coming in o he Medi e anean could
each mainly he sou he n coas o he Albo an Sea. The
highe A lan ic a ini y o he Albo an Sea Fauna (Bianchi
and Mo i 2000), he A lan ic In luence Zone desc ibed o
he A ican coas o he Albo an Sea (Gonza
´lez-Dua e
e al. 2013a), he ecen new eco ds (Gonza
´lez-Dua e
e al. 2013b; Iazza e al. 2013 and p esen da a) and he
collec ion o new undesc ibed species in hese coas s
ein o ce his idea.
These ac s, oge he wi h he exis ence o p e ious da a
abou he hyd oid auna, in 1991 (Pen
˜a Can e o and Ga cı
´a
Ca ascosa 2002) and 2007 (p esen s udy), allow us o
p opose Cha a inas as a moni o ing poin o long- e m
changes in he wes e n Medi e anean ben hic communi ies
and o he de ec ion o no el opical A lan ic species in
he Medi e anean. Long- e m moni o ing may con i m
whe he he changes in he hyd oid assemblages desc ibed
he e a e consis en and s able wi h ime. This will allow
co ela ing he clima ic changes and he changes in he
ben hic assemblages, excluding he in luence o o he
ac o s such as he na u al luc ua ion o he ma ine ben hic
popula ions.
Acknowledgmen s This s udy has been suppo ed by p ojec s P05-
RNM-369 (Jun a de Andalucı
´a), PCI2005-A7-0347 (Spanish Minis y
o Educa ion and Science), A/5481/06 and A/8688/07 (Spanish
Minis y o Fo eign A ai s and Coope a ion). We wish o hank he
Scien i ic Di ing Uni o he Uni e si y o Ca
´diz who assis ed us
in sampling expedi ion, as well ‘‘O ganismo Au o
´nomo de Pa ques
Nacionales’’ (Spanish Minis y o Ag icul u e, Food and
En i onmen ).
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Table 7 Species only ound in 1991 o in 2007
Species only ound in 1991 and no
sampled in 2007
New eco ds o Cha a inas
Is. (2007)
Agalophenia acacia Cly ia i idicans
Aglaophenia pica di Eudend ium a ma um
Aglaophenia pluma Gono hy aea lo eni
Cly ia sp. Halecium sp.1
Co yne muscoides Halecium sp.2
Ec opleu a w igh i Halecium ex um
Eudend ium simplex Neme esia an ennina
Eudend ium sp. Se ula ia ma gina a
Hyd ac inia ine mis
Hyd an hea ma ga ica
Hyd odend on mi abile
Ki chenpaue ia halecioides
Laomedea pseudodicho oma
Neme esia amosa
Se ula ia pe pusilla
Helgol Ma Res (2014) 68:511–521 519
123