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L. DONNARUMMA1,3, C. LOMBARDI2, S. COCITO2 and M.C. GAMBI1

1 Stazione Zoologica Anton Dohrn, Laboratorio di Ecologia Funzionale ed Evolutiva, Napoli, Italy

2 ENEA Centro Ricerche Ambiente Marino, La Spezia, Italy

3 present address Dipartimento di Scienze e Tecnologie, Università di Napoli “Parthenope”, Napoli, Italy Corresponding author: gambimc@szn.it

Handling Editor: Argyro Zenetos

Received: 29 October 2013; Accepted: 4 February 2014; Published on line: 28 February 2014

Abstract

(IIHFWVRIRFHDQDFLGL¿FDWLRQ 2$RQWKHFRORQL]DWLRQVHWWOHPHQWSDWWHUQRIWKHHSLELRQWFRPPXQLW\RIWKHOHDYHVDQGUKL]RPHV

of the Mediterranean seagrass, Posidonia oceanica, have been studied at volcanic CO2YHQWVRII,VFKLD ,WDO\ XVLQJ³PLPLFV´

DVDUWL¿FLDOVXEVWUDWHV7KHH[SHULPHQWVZHUHFRQGXFWHGLQVKDOORZPosidoniaVWDQGV PGHSWK LQWKUHHVWDWLRQVRQWKHQRUWK

DQGWKUHHRQWKHVRXWKVLGHVRIWKHVWXG\DUHDGLVWULEXWHGDORQJDS+JUDGLHQW$WHDFKVWDWLRQUKL]RPHPLPLFVDQGDUWL¿FLDO

OHDYHVZHUHFROOHFWHGHYHU\WKUHHPRQWKV 6HSW6HSW 7KHHSLELRQWVRQERWKOHDIDQGUKL]RPHPLPLFVVKRZHGFOHDU

FKDQJHVDORQJWKHS+JUDGLHQWFRUDOOLQHDOJDHDQGFDOFDUHRXVLQYHUWHEUDWHV EU\R]RDQVVHUSXOLGSRO\FKDHWHVDQGEDUQDFOHV ZHUH

GRPLQDQW DW FRQWURO VWDWLRQV EXW SURJUHVVLYHO\ GLVDSSHDUHG DW WKH PRVW DFLGL¿HG VWDWLRQV ,Q WKHVH H[WUHPHO\ ORZ S+ VLWHV WKH

DVVHPEODJHZDVGRPLQDWHGE\¿ODPHQWRXVDOJDHDQGQRQFDOFDUHRXVWD[DVXFKDVK\GURLGVDQGWXQLFDWHV6HWWOHPHQWSDWWHUQRQ

WKHDUWL¿FLDOOHDYHVDQGUKL]RPHPLPLFVRYHUWLPHVKRZHGDFRQVLVWHQWGLVWULEXWLRQSDWWHUQDORQJWKHS+JUDGLHQWDQGKLJKOLJKWHG

the peak of recruitment of the various organisms in different periods according to their life history. Posidonia mimics at the DFLGL¿HGVWDWLRQVKRZHGDSRRUDQGYHU\VLPSOL¿HGDVVHPEODJHZKHUHFDOFLI\LQJHSLELRQWVVHHPHGOHVVFRPSHWLWLYHIRUVSDFH7KLV

SURIRXQGGLIIHUHQFHLQHSLSK\WHFRPPXQLWLHVLQORZS+FRQGLWLRQVVXJJHVWVFDVFDGLQJHIIHFWVRQWKHIRRGZHERIWKHPHDGRZDQG

consequently, on the functioning of the system.

.e\words Seagrass, epiphytes, mimics, CO2 vents, colonization pattern, recruitment, biodiversity, Mediterranean Sea.

Research Article Mediterranean Marine Science

,QGH[HGLQ:R6 :HERI6FLHQFH,6,7KRPVRQ DQG6&2386 7KHMRXUQDOLVDYDLODEOHRQOLQHDWKWWSZZZPHGLWPDUVFQHW 'RLKWWSG[GRLRUJPPV

Introduction

The amount of CO2 in the atmosphere has steadily increased since the industrial period. According to es

timates, if greenhouse gas emissions continue to rise at current rates, the atmospheric CO2 concentration levels ZLOOEHSSPE\DQGSSPE\ ,3&&

 7KHVXUIDFHRFHDQS+OHYHOPD\WKHUHIRUHIDOOWR

RUZLWKDQLQFUHDVHLQDFLGLW\RIFRPSDUHG

WRSUHLQGXVWULDOYDOXHV +DUGW 6D¿QD 7KLVGH

crease in the ocean pH level, as a result of atmospheric CO2 GLVVROXWLRQ LQ WKH VXUIDFH ZDWHUV RI WKH RFHDQV LV

WHUPHG³RFHDQDFLGL¿FDWLRQ´ 2$  &DOGHLUD :LFNHWW

 RU³WKHRWKHU&22 SUREOHP´ 'RQH\et al., 

In particular, OA is the result of carbonic acid formation +2CO3 ZKLFKGLVVRFLDWHVWRELFDUERQDWH +&23 FDU

ERQDWHLRQV &23 DQGSURWRQV ++ 

$FLGL¿FDWLRQ DIIHFWV PDLQO\ WKH SURFHVV RI FDOFL¿

cation of organisms such as corals, molluscs, and many RWKHURUJDQLVPVZLWKVNHOHWRQVDQGVKHOOVFRPSRVHGRI

FDOFLXP FDUERQDWH 5R\DO 6RFLHW\  'RQH\ et al., 2009; Lombardi et al.,DE ,QDGGLWLRQZKHQWKH

VHDZDWHULVFRPELQHGZLWKRWKHUNLQGVRIQDWXUDODQGRU

DQWKURSRJHQLFVWUHVVIDFWRUV HJZDUPLQJSROOXWLRQDQG

RYHU¿VKLQJ LWPD\FDXVHVHQVLEOHFKDQJHVLQWKHEHQ

WKLFFRPPXQLW\VWUXFWXUH .URHNHUet al.,5RGROIR

Metalpa et al., LPSDFWLQJPRVWIXQGDPHQWDOELR

ORJLFDODQGJHRFKHPLFDOSURFHVVHV .OH\SDVet al., 2006;

Fabry et al., 0DQ\ODERUDWRU\VWXGLHVKDYHVKRZQ

that the early life stages of several organisms are also QHJDWLYHO\LQÀXHQFHGE\DFLGL¿HGVHDZDWHU .URHNHUet al., DQGWKLVKDVEHHQREVHUYHGDOVRLQin situH[

periments at CO2YHQWV &LJOLDQRet al., 2010; Ricevuto et al., +RZHYHUWKHUHVSRQVHRIPXOWLVSHFLHVDVVHP

EODJHVWR2$DWQDWXUDOO\DFLGL¿HGZDWHULVVWLOOSRRUO\

GRFXPHQWHG HVSHFLDOO\ UHJDUGLQJ KLJKO\ FRPSOH[ V\V

WHPVEXLOWE\VWUXFWXULQJKDELWDWIRUPLQJVSHFLHVVXFK

DVVHDJUDVVPHDGRZV 0DUWLQet al., 

Posidonia oceanica /  'HOLOH LV WKH HQGHPLF DQG

GRPLQDQWVHDJUDVVLQWKH0HGLWHUUDQHDQ6HD,WIRUPVH[

WHQVLYHPHDGRZVIURPWKHVXUIDFHGRZQWRDPD[LPXP

RIDERXWPGHSWK 3URFDFFLQLet al., 6WXGLHVRQ

the fauna associated to P. oceanica revealed high diver

VLW\RIVSHFLHVVHWWOHGERWKRQOHDYHVDQGUKL]RPHV 0D]

Medit. Mar. Sci., 15/3, 2014, 498-509 499 zella et al., 1992; Cocito et al., DQGEHORQJLQJWR

GLIIHUHQWWD[RQRPLFJURXSVZKLFKLQFOXGHVPDQ\FDOFL

I\LQJWD[DVXFKDVFRUDOOLQHDOJDHFUXVWDFHDQVPROOXVFV

VHUSXOLGSRO\FKDHWHVEU\R]RDQV 0D]]HOODet al., 1992;

Buia et al., 2000; Borg et al., 2006; Balata et al.,

Nesti et al., 

:LWKLQWKHPosidoniaFRPSOH[V\VWHPWKHHSLSK\WHV

settled on the leaves and the rhizomes play an important UROH LQ WKH IRRG ZHE DQG IXQFWLRQLQJ RI WKH PHDGRZV

0D]]HOODet al., 7KHHSLSK\WLFDOJDOFRPSRQHQW

UHSUHVHQWV WKH PDLQ LWHP IRU HQHUJ\ WUDQVIHU ZLWKLQ WKH

³JUD]LQJFKDLQ´RIWKHVHDJUDVVIRRGZHEIURPSULPDU\

producers to higher trophic levels through the consump

tion due to small mesoherbivores, a guild of grazers that not only fed on the system but also found shelter and SHUPDQHQWKDELWDWLQWKHPHDGRZ %UDZOH\ 7KH

animal component of the epiphytes is also consumed by RWKHU VSHFLDOL]HG LQYHUWHEUDWHV *DPEL  0RUUL   DQG VKRZV LQWHUHVWLQJ H[DPSOHV RI DGDSWDWLRQ WR WKH

VSHFLDOORFDOFRQGLWLRQVRIWKHOHDIFDQRS\ZLWKVHYHUDO

FKDUDFWHULVWLFDQGRUH[FOXVLYHVSHFLHV HJWKHEU\R]RDQ

Electra posidoniae 

In addition, the epiphytes represent sensitive indica

WRUVRIQDWXUDORUDQWKURSRJHQLFLPSDFWV HJHXWURSKL

FDWLRQ  0RUUL   DQG DUH DEOH WR UHFRUG WKH HQYL

URQPHQWDODOWHUDWLRQVUHVXOWLQJIURPFOLPDWHFKDQJH HJ

VHDZDWHUDFLGL¿FDWLRQ  0DUWLQet al., ,QIDFWWKH

epiphytic community of P. oceanica, and especially that IRXQGRQWKHOHDYHVPDLQO\FRQVLVWVRIVKRUWOLYHGVSH

FLHVZKLFKVKRZDKLJKO\VHDVRQDOGHYHORSPHQWIROORZ

LQJWKHF\FOHRIOHDIJURZWK 0D]]HOODet al., DV

ZHOO DV D KLJK GHJUHH RI VPDOO VFDOH VSDWLDO YDULDELOLW\

1HVWLet al.,DQGOLWHUDWXUHKHUHLQ 

8SWRGDWHWKHRQO\VWXG\GHDOLQJZLWKVHDJUDVVHSL

phytes in relation to OA is that carried out by Martin et al.  DORQJDQ2$JUDGLHQWDWQDWXUDO&22 vents off Ischia. These authors highlighted big differences in the composition and structure of the calcareous epiphytic community of P. oceanicaOHDYHVLQDFLGL¿HGVHDZDWHUV

ZKHUHFRUDOOLQHDOJDHDQGRWKHUFDOFL¿HUVZHUHVWURQJO\

UHGXFHG RU DEVHQW +RZHYHU 0DUWLQ et al.   OLP

LWHGWKHLUVWXG\WRDVLQJOHVSDWLDOWUDQVHFW RQWKHVRXWK

VLGHRIWKHVWXG\DUHD DQGRQDVLQJOHREVHUYDWLRQSHULRG

$SULO DQGGLGQRWFRQVLGHUWKHFRPPXQLW\VHWWOHGRQ

the rhizomes.

6LPLODUUHVXOWVVKRZLQJDUHGXFHGFRORQL]DWLRQRIFDO

careous macroalgae and calcifying benthic invertebrates colonizing the hard rocky reefs, adjacent to the Posidonia VWDQGVLQWKHVDPHVWXG\DUHDZHUHVKRZQE\RWKHUDXWKRUV

+DOO6SHQFHU et al.,  .URHNHU et al., 2011; Porzio et al., 6RPHRIWKHSDWWHUQVREVHUYHGLQWKHDGXOW

SRSXODWLRQVRIYDULRXVVSHFLHVRIWKHURFN\VXEVWUDWHZHUH

due to selective pressure on the larval and juvenile stages &LJOLDQRet al., 2010; Ricevuto et al., 

The overall aim of this study is to highlight the ef

IHFWVRIRFHDQDFLGL¿FDWLRQRQWKHFRORQL]DWLRQDQGVHW

tlement pattern of the Posidonia epibiont community of the leaves and rhizomes along a gradient of pH reduction, and increased pCO2XVLQJDQHZH[SHULPHQWDODSSURDFK

ZLWK³PLPLFV´ VHH0HWKRGV  *DPELet al., 2011; Cocito et al., 7KHSODQWPLPLFVZHUHXVHGWRUHGXFHWKH

LPSDFWRIH[SHULPHQWDOVWXGLHVRQWKHQDWXUDOPosidonia PHDGRZZLWKLQWKHVWXG\DUHD0RUHRYHUPLPLFVDUHHV

VHQWLDOIRUKDYLQJDQXQFRORQL]HGVXEVWUDWHWRH[DPLQH

WKHVHDVRQDOF\FOHVRIHSLSK\WHUHFRORQL]DWLRQDWDJLYHQ

time interval and to compare possible quantitative and TXDOLWDWLYH GLIIHUHQFHV LQ VSHFLHV EHWZHHQ DUWL¿FLDO DQG

QDWXUDOVXEVWUDWHV LHP. oceanicaWLVVXH ,QGHWDLORXU

JRDOV DUH L  WR FKDUDFWHUL]H WKH Posidonia VWDQGV ZKHUH

PosidoniaPLPLFVZHUHSODFHGLL WRUHSRUWFRORQL]DWLRQ

SDWWHUQ RQ WKH ¿UVW WKUHH PRQWKV RI H[SRVXUH DORQJ WKH

JUDGLHQWV IRU ERWK WKH OHDYHV DQG UKL]RPH PLPLFV LLL  to study the settlement pattern through time of the main HSLELRQWV OLPLWHGWRWKHVRXWKVLGHRQO\ 

Materials and Methods Study site

The study area is adjacent to Castello Aragonese, D YROFDQLF GRPH DQG LVOHW ORFDWHG DW WKH QRUWKHDVWHUQ

VLGHRI,VFKLDLVODQG *XOIRI1DSOHV,WDO\  Ħ1

Ħ(  5LWWPDQQ  *RWWLQL   3UHYLRXV DQG

UHFHQWJDVDQDO\VHV 7HGHVFR+DOO6SHQFHUet al.,

S+ YDULHV IURP WKH QRUPDO YDOXH RI  WR DV ORZ DV

 DORQJ D FRQWLQXRXV JUDGLHQW RFFXUULQJ ERWK DW WKH

QRUWK DQG VRXWKZHVWHUQ VLGHV RI WKH &DVWHOOR .URHNHU

et al., 2011; Lombardi et al., E  2Q ERWK VLGHV RI

WKH&DVWHOORLVOHWDVKDOORZPosidonia oceanicaPHDGRZ

subjected to CO2HPLVVLRQLVSUHVHQW %XLDet al., 2003;

+DOO6SHQFHUet al., 2QWKHVRXWKVLGHWKHPRVW

intense venting activity include also PosidoniaPHDGRZ

here in some restricted areas Posidonia can reach very VKDOORZGHSWK P DQGIRUPVDVRUWRIUHHI7KLV

VLGHRIWKH&DVWHOORLVDOVRPRUHVKHOWHUHGWRZDWHUPRYH

PHQW UHVSHFW WR WKH QRUWK VLGH ZKLFK LV H[SRVHG WR WKH

GRPLQDQWQRUWKZHVWHUQZLQGV$WWKHQRUWKVLGHPosido-niaPHDGRZLVYHU\FORVHWRWKHDFWLYHYHQWLQJDUHDEXW

direct gas bubbling is very limited or absent inside the PHDGRZ,QDGGLWLRQLQWKLVDUHDDQHFGRWDOREVHUYDWLRQV

RIRQHRIXV 0&* DVZHOODVRWKHUUHVHDUFKHUVWHVWLI\

WKDWYHQWLQJZDVDEVHQWLQWKHHDUO\¶ 5XVVR*)%RX

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FRPPXQLFDWLRQ VRWKDWZDWHUDFLGL¿FDWLRQLVDUHODWLYHO\

recent phenomenon on the north side of the Castello. The H[SHULPHQWVDUHFRQGXFWHGLQVKDOORZPosidonia stands

 Medit. Mar. Sci., 15/3, 2014, 498-509 DWPGHSWKLQWKUHHVWDWLRQVORFDWHGRQWKHQRUWK

VLGH 111 DQGWKUHHRQWKHVRXWKVLGH 6&6

6 GLVWULEXWHGDORQJDJUDGLHQWRIS+7KHVWDWLRQVKDYH

been selected based on previous studies in relation to SUR[LPLW\WR&22 emissions and mean pH values record

HG VHH&LJOLDQRet al., 2010 for a map of the area, Lom

bardi et al., E  7KH 6 DQG 1 VWDWLRQV DFLGL¿HG

VLWHVZLWKYHU\ORZS+DUHORFDWHGLQDQDUHDZLWKKLJK

EXEEOLQJ DQG GHQVH HPLVVLRQV  EXEEOHV HPLVVLRQV

to m2  0HDQ S+ YDOXHV DUH DSSUR[LPDWHO\  DW WKH

northern and 6.6 at the southern sites, near the rocky reef .URHNHUet al., ,QWKHVHVWDWLRQVWKHP. oceanica PHDGRZLVYHU\GHQVH RYHUVKRRWVP2  %XLDet al.,

 ZLWKWKHVKRUWOHDYHVGXHWRWKHIUHTXHQWJUD]LQJE\ DURXQG +DOO6SHQFHUet al., 2008; Lombardi et al.,E EXWLWKDVDOVRDFRQVLGHUDEOHYDULDELOLW\LQ

WLPH DOVR DW GDLO\ VFDOH .HUULVRQ et al.,  .URHN

er et al.,   DQG WKH EXEEOHV HPLVVLRQV DUH UHGXFHG

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m2 7KH6&DQG1DUHFRQWUROVWDWLRQVORFDWHGDSSUR[L

PDWHO\PIURPWKH61ZKHUHWKH&22 emissions are almost absent and the pH values are those of normal VHD ZDWHUV   7KH VRXWK VLGH VWDWLRQ 6&  KDV EHHQ

XVHGDVDFRQWUROVLWHIRUSUHYLRXVWUDQVSODQWH[SHULPHQWV

/RPEDUGLet al.,DE5RGROIR0HWDOSDet al.,

 DQGLWGRHVQRWFRLQFLGHZLWKWKHVRXWKFRQWUROVWD

WLRQRIRWKHUVWXGLHV HJ.URHNHUet al.,D 

Sampling methods and data analysis

$UWL¿FLDO VWUXFWXUHV PLPLFNLQJ WKH SODQW PRUSKRO

ogy, both rhizome and leaves have been developed ad hoc for this study. This methodology, implying the use RI DUWL¿FLDO VXEVWUDWHV LV DQDORJRXV WR WKH XVH RI SDQ

els and volcanic tiles to study the fouling, community UHFRORQL]DWLRQ DQG VXFFHVVLRQ SDWWHUQ LQ KDUG ERWWRP

HQYLURQPHQWV 5HOLQL  )DLPDOL  .URHNHU et al.,

D  0RUHRYHU DUWL¿FLDO VWUXFWXUHV PLPLFNLQJ WKH

physical structure and morphology of a seagrass have DOUHDG\EHHQXVHGE\RWKHUDXWKRUV 3LQNQH\ 0LFKHOL

 HVSHFLDOO\WRVWXG\WKHUHFRORQL]DWLRQRIDVVRFL

DWHGÀRUDDQGIDXQD %RORJQD +HFN/HHet al., 2001; Cocito et al.,   DQG WR GHWHFW WKH VSHFL¿FLW\

RIWKHHSLSK\WHVIRUWKHVHDJUDVVVXEVWUDWH 0D]]HOODet al., $OWKRXJKVHDJUDVVPLPLFVDUHQRWH[DFWVXU

URJDWHV RI WKH SODQW 3LQNQH\  0LFKHOL   LI DS

propriately designed, they can simulate plant architecture and structure. So they have the merit to reduce variability RISODQWIHDWXUHVUHVSHFWWRWKHQDWXUDOFRQWH[W0LPLFV

DOVRDOORZWRWHVWWKHVLPSOHLQÀXHQFHRISODQWDUFKLWHF

ture and physical structure on the epibiont community

colonization vs the biological and chemical effect. In ad

GLWLRQ LQ WKH VSHFL¿F FRQWH[W RI WKH QDWXUDO &22 vents, the use of mimics reduces the impact on the Posidonia system caused by shoot collection in the relatively lim

LWHGH[WHQVLRQRIWKHPosidoniaPHDGRZVKHUHDYDLODEOH

0LPLFV )LJ   RI Posidonia rhizomes consist of hol

ORZF\OLQGHUVPDGHRIHDUWKHQZDUHZLWKURXJKDQG¿QHO\

grooved surface to reproduce the roughness of the natural rhizomes as best as possible. The length of the cylinders, set according to the rhizome mean height from literature GDWDLVFPZLWKDGLDPHWHURIDSSUR[LPDWHO\FP

*DPELet al., 2011; Cocito et al., 0LPLFVRIPosi-doniaOHDYHVDUHPDGHZLWKQRQWR[LFGDUNJUHHQÀH[

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LQ VWULSV  FP ZLGH DQG  FP ORQJ )RXU 39& VWULSV

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WRDKRRNHGLURQVWDNH )LJ 7KHVWDNHVZLWKDUWL¿FLDO

OHDYHVDUHWKHQLQVHUWHGLQWKHKROORZRIWKHF\OLQGHUDQG

hammered on the bottom among the Posidonia natural UKL]RPHVSURGXFLQJDPLQLPDOLPSDFWRQWKHPHDGRZ

At each of the 6 stations, PosidoniaPLPLFVZHUHLQVHUWHG

LQWRWKHPHDGRZLQDQDUHDRIDSSUR[LPDWHO\[P

ZKHUHWKHFRQGLWLRQRI&22 emissions and the pH value variability could be considered relatively homogeneous in time according to previous measurements on the same VSRWV &LJOLDQRet al., 2010; Lombardi et al.,E $W

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tographed. In order to study the pattern of settlement of Fig. 1:$UWL¿FLDOVWUXFWXUHVPLPLFNLQJWKHP. oceanica rhizome and leaves used to study colonization and settlement patterns RI WKH HSLELRQW SRSXODWLRQV$  UKL]RPH PLPLF %  WKH PHWDO

KRRNHGVWLFNZLWKDUWL¿FLDOOHDYHVWLHG& DZKROHYLHZRID

mimic Posidonia shoot.

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reinserted at three month time intervals from September

 'HFHPEHU0DUFK-XQHDQG6HSWHPEHU 

7KHVRXWKVLGHZDVVHOHFWHGWRUHGXFHWKHVDPSOLQJHIIRUW

since here the pH gradient is stronger than to the north side .URHNHU HW DO  $W HDFK VWDWLRQ Posidonia shoot GHQVLW\ZDVPHDVXUHGLQ6HSWHPEHUDQGVDPSOLQJV

of Posidonia QDWXUDO VKRRWV  VKRRWV  IRU WKH PRU

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year in order to characterize the features of the Posidonia VKRRWVLQWKHSORWXVHGIRUPLPLF¶VGHSOR\PHQW %XLDet al.,

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of epibiont coverage and the abundance of the main epibi

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analyzing program Vidana 1.1. Data related to cover, as ZHOODVWKRVHRQVKRRWPRUSKRPHWULFPHDVXUHPHQWVZHUH

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Results

Shoot density and morphometric analysis of Posidonia along the pH gradient

Posidonia oceanica VKRRWGHQVLW\VKRZHGERWKDWWKH

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due to various grazers, is the main source of leaf damaging.

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Fig. 2: Trends of Posidonia oceanicaPRUSKRORJLFDOIHDWXUHVPHDVXUHGLQWKHPLPLF¶VSORWVDORQJWKHS+JUDGLHQW HDFKVWDWLRQ

LVWKHPHDQRIVDPSOLQJSHULRGVEHWZHHQ6HSW6HSW %DUVUHSUHVHQWVWDQGDUGGHYLDWLRQV$ PHDQOHDIOHQJWK%  PHDQVXUIDFHRIWKHVKRRW FP2 & SHUFHQWDJHRIW\SHVRIOHDIDSH[HURVLRQ' SHUFHQWDJHRIW\SHVRIELRORJLFDODSH[HURVLRQ

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Among the type of biological damaging, Sarpa salpa graz

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