"symbiosis" between algal chloroplasts ano sacoglossan molluscs

28 Pages·2012·3.41 MB·English

HomagteoR amoMna rgao/reW,f,h 'y t herseu ciphs/ easiunsr uted yinnagt ure 271
(.JD . RosP r&a etdNs,.. 1)99.1. O ec%giaaq uiacta1,:02 7-1289
AOAPTIVE AOVANTAGES OF THE "SYMBIOSIS"
BETWEEN ALGAL CHLOROPLASTS ANO
SACOGLOSSANM OLLUSCS
JOANDOENMECR OS* & ARNALDOM ARÍN **
*D epartdEa'cmoelnFotag ciudal.eBt iaotl Uongiivaed.re Bs airtcaeAtlv Do.in aag.6o 4n05a8.l0 ,B2 a8r celona.
Spain
**D epartdaeBm eilnootgAoín ai myEa clo logíad.eB ilFooagcUíunali.tv aeddr esM iudracCdia am.p us de
Espridn3oa10.00 M urcSipaa.i n
ReceSievpetde:1m9 9b1e.r
SUMMARV
AHa vaiilonarfbmlaeit sri eovni oenwt ehcdeh aracatnetdrh iwesa tyi "ctysshm eb si"ob seitwaelegna l
chromoapnlsdaa sctosgm looHsuswsaocnrs uk ssi,tn hegex isbtiiibonlggr aanptdhh ayeu thoowrnss t'u dies.
Emphiapssl iasoc nte hdie m porotfa fntochoesed u bsriedcyeb iyv emtdoh lel usicos,n oewft h hvjeac rhi ous
benefitfsr otdmhae esr siovceaidna odtn ti hopeno ,s sbiebnleef itf rootbmht ciaosin nseobdry tt hiaeul mg al
speicniveosal nvde bdny o rtte htea ined wchhialcrohaer f,ota peHnlr,oa ns-tasu,ct eoolnrlog rrauncAe fltleers .
makivnagr itohueso rceotnisciadlae nrodan tt ihboean ssoi,fts h peo puldaytniaoomnfis cosrn e opfa irs
alga-sascpoegclioesss,aa nAnc e aesbtpuelacarciieaatH aybau nlEudlm y stiiam ipdoap ulatiosnt utdhioerdo ughly
byt haeu thtohfreHos o,w icnongc ludsriaownns: are
a)T hees tabloifass hymmebnriteo ltaitcbi eotnwssehaeicnpo glaoncsdhs raonmsoa pntldha desif tefsr ent
levoefml ust ual aandedafi pfctiareteniacocyanh r aeed d i,r feucntco tfti hdoein f f(isceualostrooy tn haelr wise)
experbiyte hnmeco eldIi uonsb ncti agfni ood.
b)D epenodnti hnmego meonftt h bei olocgyiciclnwae hl it chhae n irmeacle iittv,hee ens e srugbys idy
provbiytd hecedh lortootp hlheao smstotsH uascecti st ahsaed ri ectoamrpyl eadm ieensttua,pr pyl oeram ent
parstuibasJot fti htneuo tremo abltIayi nfeodo da.l gal
c)Th siusb siiisnd vye ssutcecde,as mi/soiarvl etleym aittnih evl elclmu'oygss,r o(wPtgh) t,hs eh iinfo tf ing
itrse prtoidpvuaect ftreoamlm e cithloatrdrveoavpleh liotcopa mednirte cotri inon ncer ee(xaPprsrale)tod,o ry
anfdo rianaggc ti(vLliRA)tHt.y h eesnet rreiperse bseennfetoft riham te o lliuans lcl,oi wttiob n emg o raec tive,
lviel onrgeeprr,mo odurecefie fc iaemi/noterlx yp lag orreea toefr tabhreeed a.s ea
d)W hetnh seu bsiindvyoa lnev neescr ogmyp lfeomtrehs neat c ogslpoescisiitaepsn sl ,a utshitabhtle e
moIlusci tgrsre adzruiacontengtes h e saplegciaint eh ssea, mp er opoartwt hiiiocrtnhe cetihsveue bss idy. In
thciass ea ltsghpaee aclibseeosn ewfhiiwtcoshu, al Hdot wh e relatiaolnag natbd he seta wceoegtnlo o tshsea n
bec lasassmi uftiueadIl aniH ts htoeit hce.r t hbceea nsieeesfsx i ctl ufsotirhvm eeo Hluys c.
KEY RWDOSS:a cogclholsosraao,dp alpatssatytsmi,bo iEnlo,yss tiiiasm i,Ad caea,bt ulaarcieat abulum.
"Thcel oesxea minaofta inoyen c osysrteevme ailnsm oscta sebse cuas eo ncken owint,i s d ififcutlot
ani fninoiftc yo mpar[atbrloepc hoilca treerlaalt]i eovnasl.u /anta en.yc asteh,e r esuilstt h attr aditional
Them osotb viroeussou fli tte sv oluitsti hoanit nt, h eb iolohgaysa lwagyisv emno rei mportatnoct eh e
enda,c ertsapienc fioremssa verys trrieclta twiiotnhs pecifofit chirete yl atthiaotnnot hter afneros rs aving
anothdefiern eds peciTehsep. r oceosfs s electoifeo nngye rthaitit mp lies("M.A RGALEF,
/974:5 43)
whichl ehtdaot s h ees tabliasnhdmm aeinntt enofa nce" Certain ocragnao nbitsamisn "hsaencdo"n d
sucrhe lathiaostn osb ee pxlainbeys do meen geyr algfaroem t heir. .pS.rt.er ya nsgteiirlst l h seu rvival,
ecnoomy;i np rcatcie, hoewver,t hsep ceificioftt yh e notof whloe celsl,b utof CodiaunmdB ryopsis
relationsd iebfrefetownretge ann iissmm osr neo tabpllea stiinEd sl yTsriiad,aa ncdPh liaac ainddt aha,t
or morea pparentth ana nyg enereanlge yr thespel astids ctoon htaivneau ef unctional
considersaotmieotnib,me ecsa iutis sue n knoawnnd, capa.c"i.(.t.M y AR GALEF,
/974:538).
272 ROS& MARíN
INTRODCUTION Int hsei txis,et hee lenc tmrioc roscope
enableeads yi dentifiocfa tthieosne
TheO psithobraanrceah gsr oup orogfea llnesi nP lakaonbcrhuosc ellatus,
marignaes trowphoidcshv ipdnreuo m eroEulyss iaat rovisi arnidod thsearc loogsnssa
examploefms o lclsum saknig useo f (KAWAGUTI,1 491; KAWAGUT&I
moroplhoglei elcmaenbtesl ontgoit nhge iYrA MASU1,69 5; KAWAGUTeIt a l.,
presyp eecsis,u cahs p lnata nda nima1l69 5;e ct)P.h ysiolaongdbi icoeacmlhi cal
pigemnt(sme lnaicna,r eontoipdtse,ra inndes tudoifve rasoi ussep ci(ewsh iicnhuc d1ed
punreig rnauleesct,. )s,p ongiec uslptehsme,e asureomfoe xnytg perno duacnepd
cnairdinaenm atoceyt.sc( tEsD,M UDNS,o ft hec arbfoxine db yp hotosynthesis)
1696,1 794;·T HOMPSON1,690 ,1 796;b egsahno ratfltyed rswT:a YrAL OR( 9167),
HAEFELFINGE1R69,9R ;O S1,79 61,79 7; GREENE( 9170a1,79 0b)T,R ENCH&
TODD, 1891;G REENWOOD & SMITH(9 170G)R,E ENE& MUSACTINE
MARISCA1L89,4 ;C ATTANE1O99,0 ;( 1792e)t;.c
ect.) Thesset udlietedos three vfiiaernwsdst
TheS acoglo(s=sAas cogMloonsos­satt,ih eorestnyhitecsaelws h,i cdhi sceudt shse
chogloasrasen ao )r doefro pisthobrroalneco hfs t he chrlooplast-sacoglossan
of benthhiabci tTsh.e ya rem ainlrye latio(nTsAhYiLp,O R1793,1 891;
hebrivooursa,n d ssoprneec rieetsat ihneG REENE,1 794; TRENCH, 1795;
chloroopftl haaesl tgsta heat th ecyo nsuTmAeY LOR1 7931,89 1H;I NDE18,93 ;e ct.).
(KAWAGUTI & YAMASU,1 695; A rletaiveelxyh auslttii osvfte h em ain
TAYLOR1,69 71,7 93;G REENE1,79 0a;r ecewnotrk osnt hceh lolrsaotpc-osgaslaons
TRENHC,1 795;H INDE1,8 93M;A RÍN & relationbsehf iopu nicdnta hnea r ct1ies
ROS,1 898;M ARÍN,1 991e;ct .)T.he mentioanbeody aen di nW ILLIAMS
chloroaprlneao sitt mmse deiladyti gest(e91d8,6M )A,R ÍN (1898), ÍNM &A RROS
butrme aianc tive wdeuerkoisrne gv en( 9189i,n p reas,s Tbh)e.s ynstihbsey
montihnts h cele losft he diggelsantHdiIv.Ne D (E91 83i)ps a ircturlltyah orough.
Them olcl usoftheosnue ss o many Thep reseonfpc ales tiindt sh etiirs sues
chrlooplatshtasit t s copleeorcuftrl hya sl edt hesaenm ialsto be cald le
matcheso ftt hhaeft o oadl g(ag reecnr,y ptogmaomulislcc asn d" elavetsh at
ocsciaonraeldal)lyh,t o ugsho mettihmeessce rw al"( TRECNH,1 795)M.an yo ft he
colroscu oemf rmo thiegn esatnaad r e saeneant ornaincda lb ehacvhiaoreuairrtcsaitlc s
byt ranesnpcaryre,gd alreosfws h etthheeryo fc hlorospt-rlteaaingsi anocglonsscs aannot
corresoprno onttdof unctciholnpoaalrlso .t sbee xpinleadi fn oats adapttoa ittsih ons
They amlasbyoe d uteo t haen mial'sow n peculr iaassotocini:"a Spielaceidst issues
pigemn.t s sucahs t hel arfigated orsmaaln tolfe
It hask nboewfenon or verc ean tuErlyys ia[ vriidiwsh} iccho ntanienast
thats orne sagclosoasns posseasgsr icurlotwuosrf a lco hplslotarssa,l vaged
chlohryoclpp 1giimenDtEsN .E GRI& DE froCmo iduma,er .a. c.o nsequoeftn hcee
NEGR(I1 87o6b)s ertvheedpi rre seinnc iem portoafnt chees ymbiaostsiocic oina"t
Elysviiar iadnidsB ,RA NDT( 818)5l taer( DYE1R89,9 ).
descrcihbleodr oipntl hasesa tmsse p ceies.T hef unctioofnt ahpleil ntatoy r ngaelles
Zooxhaelnleta werel taero bservede nabletde rstmyh meb itoobs eiu ss e(dsa
m
nudibran(cNhVAsI L LE, 1296, in mentiaobnoeydbe y) tfhierr sets eartcoh ers
Aeolidieall ldraei, ) a nd YON&G El ooki tno itsh alga-anilm arletaion
NICHOLA(S1 490)d escritbheedm (KWAAGUTI& YAMASU,1 695;
m
the sacosgalno Tsricdhaiac rispaGtREaE NE1,79 0a1,79 0bT;R ENCH1,7 95),
(althtohuegwyhe re lryde eaialgnl wiht which hams esbs eoemqneu taiileidaf s
cholrop)la.s ts chrlooplsaysmtb i(oHIsNiDsE& SMTIH,
SYMSIOSSIETSW EENA LGACLH OLROPALSTSA NO SACOGLOSSANS 273
1794T;R ENHC,1 795)S.uc ha symobsii(swi tqhu otamtairokHns IN:D E& SMTIH,
haasl wabyesei ntn erpraesmt uetdu satlii1c79 4M;A RÍN & ROS,1 899e;ct .).
(MAGRALEF1,7 94;A HMADJIAN& Thipsa pebra,s oends tudciaerrsio eudt
PARACER1,89 6D;O UGLA&S S MITHb,y t haeu th0o11 ras s coorfes acloosgsan
1899)t,h aitsw ,ih t mutubaeln etfoit hte s peciest hfeSr paonmi Msehd tierranean
twsop ieecisn volved. coascto,n tridbauttaaen sd a gruments
Ith asb eeenfe fcvteilsyh own tthhewa hti cdhe monstthratatht seey mobsii(st he
photosyntphraotdeusc ebdy them utuaals sociafrtoimow nh ihc both
chloroaprlueaes sdat,tsl a est pbayrt thlepy a,r tbneenresif snio tbt)e twtehemeno lulsc
mollu(sGcRsE EN1E79,0 bT;R ENCeHt antdh peal notr ngealbluert,a thbeetrw een
al.1,79 0;G REENE& MUSCATINEt,h meo ulslacn tdh feo oadl ga.
1792H;IN DE& SMTIH,1 795C;L AReKt Atl eaisnst o rnseiu attsi,to hnbee nefit
al,. 1891M;A RÍN & ROS,1 899e;ct .)f.o r the allgiaielns rstephdeeuc ciotefis o n
Indivifdruoamld sif freenstp ieecso f istp redabtyit ohnme o lluisnc ,t he same
chloroplasts-arcelostogsaainnlsii nvgpe r oportiino n which the retained
longweirt hoeuatt itnhga enq uailvencth,l oropprloavsitdsme o lltuhsweci tahn
none-tnraigin spceieosr,g rowf astiefre nersguyb ys ibdaseodn p hotosynthates
exposteodl ihgtt hainf t helyvi e i n whicha dadriet tioot hnfeao lo cdo unmsed
danrkestsh;ae n imcaoln sotrhtubsse nefbiytt h lea tter tthhnero orumhgaehlr bivory
frotmh uinsu sla usasioaicton. procedAu vreerp.yer limriydn raaofftt h e
The same bces aaniondfot th e ntp lpraeseanrtg umewnatss advanced
m
consortthsec, h rlooplaTshtesy.a reM ARÍN & ROS( 9189).
orngeallesse rpaatferdo tmh ea 1gcaell ls
and are,t herefoirnec,a paobfl e
reopdructaionndo f increatshieniSgrA COGLOSSANS AND THEIR
Darwinfiiatnn( ewschshi i so neo ft heA SSOCIATION WITH ALGAL
premitsheasht a st ob ef ulfilledi na CHLOROPLASTS
mutusatliiscy mbsi)o.sT ihen,s trictly
speakitnhger, e latiocnasnhniobpte TheS acogloscsaanbn esd i viitdnoe d
quaileiadfss ymbi(oHItNiDcE1 ,89 3). threem ani morphologtiycspa el
Thes amed oenso to ccurw iht the( MOTRON,1 799;T HOMPSON1,79 6;
relationesshtiapb lisbheetdw eSeCnH MEEKL & PORTAMNN,1 892,
cnidariann-uedaitbirnaagnn cdht sh eiGrA SCOIGN1E89,5;s eJeE NSE1N99,1 .)
symbci oztoioxanthwehlilcahea ,r eT he mporsmiti tiavreet het estaceous,
icnorporianottt ehdte i ssoufte hspe r edasteholrd l eforomfts h es uborJdu elcriesaa ,
(NAIVLLE1,29 6;K EMPF1,89 4,1 991;V ovlatellaancdeO ax ynoacwehai,c h
MARNÍ & ROS1,99 1.) / appardeonn tolrtey t aacitnci hvrleoo plasts.
TRENCH(9 180) pro�epdot he terTmh eraer e tmwanoi typeosfm ore
"ofriegno rganerleeltnieto n"f ort he advanmcoerhdpo gliolcf aormnsa,k eadn d
sacloosgs�acnhloroplaaIss ts ociatsiehol-nll eosfst ,h seu borEdleyrcsse iaaan d
(BALCKBOURNe t al,. 1793)a,n dP latyhedwyhliaccchea anb, e s lug-like,
CLAKR & DeFREE(S1E9 8s7u)g geswtihet dp arapoadnidaw ihtoutd orsal
"ke1ptop"l,ba osttthye rmisnw hicthh ea ppendage(sfm aielsi Elyisdiae,
mutubaeln eoffit th ea ssociiasnt oitoP nl akobranchBiosdelailied,a e and
implic"iChotlr.o plsaybsmito shiassa" l sLoi mapontoiriw diatech)e ,r a(tdao rsal
beenu sebdy sornaeu th(oHrsI N&D Ep api;l lfamaeielsi Poyblarnchiei,d a
SMITH,17 94; CLARK& BUSACCA,H ermaeidSatieig,le ridAaled,e riidae,
1798C;L ARKe ta l,. 1891W;I LLIAMS,P latyhedMyanlyio dfa ets)hp.ee cfireosm
1896e,ct .,w) hiolteh eursse" y smiboiss"t heslseat t wog rouhposu sfeu nctional
274 ROS M&A RNí
TA BEL Systeamraarntgiecom fet nhoter dSearc ogtlhoes ssutabw;oor sr, td hefei svuep aemrifalnitdeh se
1.
fourgteeneenar caclelfpymat lieid(e GsA SCOI1G89N5TE;H, O MPS1O79N6,M; A RCUS1,89 2J;E NSEN,
1893L;ON G,18 93a)r e showwni,tt hhm eaa liwonon rgl d Tghoeesng eernaae.rri ean diicnaw theidc h
chlorroeptleansbttei reoennp oh(raftsue Idl tdhooitswnseh ) i rcaehnt ded notneioseot xn (i ospte nf rdotomht es ,
speciesT hssetp uedcliiieesidstns) e t.da ntdyapred awrhei sctthhu,obd syide ei df faeurtehnhovtare bs e,e n
shotworn e tcahilno rTohpselp aeslctiisse.its nie tdah laivbcees es nt uodria erbdee isntgu bdyit ehadeu thors
(RO&S R ODRÍGU18E95ZM,;A RÍ1N89,8 1,99 1M;A RÍ&N R OS1,89 81,89 9i,np reas,bs )a ntdh e
precseydmibniogn ldsit chtaahttree ey t fauinnc cthiloonarlo) ptlhtaahstdet oyns o rte ttahienmo rt hiaitts
(e , n
noktn owwhne tthhererey t tahieonmrn o(t+ a;l sseoe TaNboltteeh m aatn gye nhearvane oy te bte en
11).
prospectedh,a vteahmn eod sp trn iemisitptheie(cvrJiie uea lscp eaar,tt h Oeox fy nooartc ehmaeo) sa,td vanced
onesso,rno eft heemg g-e(aAtledreOsrl ieiiaddnapaderate o, f Sttlihigee r.i dae)
SACOGLOBSeSrAg1 7h86,( =ASCOGLvO.S SEAl iyosbraPnrcuhvuo1st39 -0F ol,
Iher17i86nMg;O, N OSTICHOPGaLgOeSnSsAt eEclhyersB,ie erl1g7l8h2a,
1785) EliyosptMearcru,u1s s59 7
CONCHOIGDaEsAc o1i89g5n e, ThurBiedri1gl78hl2,a T. hopei
JuilacBeoae t1t69g3e r, e TridDaecshhia1a5y8 7e s,Te .cr ispata
JuildiEa.Ae . S mi1t8.8h5 , e TriideaaMlc ahlcFa'r1l9aT2n.d4d i ,o medea
JuGloiua1l 68d2., eP attyMcalrac1yu89as2 ,
BeertlhiCnrioas17 s85e , PlakobrRaann1cg28h,9i dae
o
Edeenltltin1a69 0 PlakobVraaHnna cshs1ue28sl4P t i., ah notbasp,s u
TamanBoKuvama,w lavgau ti1 59&9 Baba, e Po.cellatus
VolvatMealrlc1a8u9c2se a BoeslaleiM,ia drc1u89s2,
VolvatPeillls1i9b8d5ra ye, BoslaeiT Irinc19h8-0e19s e,B .m imetica
Volvate1l68l0a Pease, Peo lybraHn.&c A h.Ai diadm1a5s8ee 4,
CydlrionbuTlhlii1ed39la1ee , CalipAh.Co yslt,1la 68a5 (69)
CylindPr.o bFu1i5l8s7lh ae r, MourgMoanrac1 u79s0,
AscoMbaurlcl1u7a9s 2, +A .fr gailis LoberiPafe a1s8e17 ,
Oxynoacea16 93B oettger, PolycbhrPiaeana 1s68e0,
OxynoFiidsac1eh88 e3r , CyeBrecre1g 78h1,
OxynRoaef in1e8s1qu9e ,a ntOi.I laHreurmm,a He.&iA d.Aad ea m15s8,4
o.a zuropuncte aHtear, mLaoeva1é 4n84, e H.b ífida,
O.o livacea, + H.p aucrircai
O.p anamensCioss iteaPlsrluav o1t59-1F oC.lIl ,ii anae
Lobigerida15e94 P ruvot-Fol,Ae plysDieosphsa1i3y8s9e -s5,3
LobiKgreor1h4 n87, serraaldcifi HermaTeriinnac1 7h84e se,
o oL .
LophopZlieIu1cr59he6,l la SteirliiIdgraee&d O aD'loen og1h29u3e ,
RobumMealrlc1au89 s2, CailolpDa'Oebrai gn13y87, bellula
ACONCHOGIaDsEcAo 1i89g5n e, StiigElehrr en1b8e3r1g , oC .
EEllyiysdsBiHaiea.&ercA 1ge7.A8ha2 d, a m15s84, e PlaTcriidesnaec 1,h78 6 +P .c remoniana,
P.d endrítica,
Elysia1 8R1i8s so,E .at irrovidis, e
e P.v iridis,
E.a usitsr,a l
+ P.v erticillata
E.c auze, ErcoTlrainnic1a7h8 2e se,+ E .c aerulea,
E.c hlorotica,
funerea
e E.
E.f lava, OlAegae rs1b29o3r g,
Ee .f urvacaLuoid maa poGnryta,1i4 i82d ae
Ee E..h g eodrgdapaene,t hei L,i mapJoonhtni1sa38t 6o nLo, Ld. .ce appirteastsa,a
E. maoriaA,l derBiaabo,1p6 9s8i s
E.s ubomatAal,d eriidae
timida, AldAelriln,am1 a486
e E. o
translucenAsl,d erelril Fnar aO1nd69ch8,n e
E.
E.tu ca, PlatyhReadnykl17ia99nc ,e a
e E.v iridis PlatyhSeadlyvliindi1a7-9e3P lawen,
AchiGlalsecao1 i89g5n e, PlatyShaeldvyilnei1 7-93P lawen,
chlorofprlotamhs feto soa dl g(aTea b1l)e. p hytophsaugcotuofseer diearlts h,ai gtne st
Alomsatl tlh Sea cloosgsasn pecaireess uctortihacely ltyo polfac samu plaelrean
SYMBIOSBIETWSE ENA LGACLH OLROPALSTS ASNACOO GLOSSANS 275
algaaneod f o thseirp honcahlleoarno pahdyatpat atdieosnisg fnoerdt hee fifcient
andr hodopFhoyrtti has.r eastohnte e rme xpiltoatoifot nh er etaicnheldo roplasts
chromo(pcloarlseotpdu l satiidsp) r efer(rFeid1g .).T hesaed aptartainofgnreso t mh e
toc hloro(pglraepseltnta is,da )ss ornoef strucotftu hrreea lduaa ndt hseu bstitution
thoer ganreeltlaeiasnr feer dmo readl gameec hnaisomft he roonwol fyr adutleaert h,
(rhodiodplsa;Ys LtTOAR1 ,79 1M;A RÍN & tot hrea mificoaftt hideoi ng esgtlniadiv en
ROS,1 898)T.h et erkml epto(ptsloalsettnh mea nt(lweh olsieg ht-caantdgc ahsi­ng
plashtaisad l)s boe euns e(dWA UGH& and nutr-ieexnctih gan ngsufracei s
CLARK1,89 6M;A RÍN & ROS,1 899). increbayst ehdpe r eseonfflc aep osr b y
Beseistd hemo rpholooftg hybe u cacle ratad-olrisakapelp endaTgAeYsL;O R,
apptauraasd,a pftoetrdh pee orrfatoifto hne 1 891;a) ndfr mo thper efnecrfeeo cre rtain
algcaelllsa ndt huel tesruicotroi fto hne iirne tntsiiesl iogtfhot t h,se y nchronoifs ation
conte(nTtHMsOP SON,17 96C;L ARK& thleei fcycw1ieht thaotft hfeo oadl ga
BUSACCA,1 798J;E NSE1N8,90 ,18 91,( MAÍRN & ROS,i np reas,)sa ndt ot he
1991;C LAKR & DeFERESE,18 97;a nmialb ehaviiocnu1ru,d isnygn copated
MARIN1,89 8)t,h esmeo lslcusp ossevsesnl ttaiiomno vemeonftt hsme a ntclaev ity
anatompihcyaslgi,io lcla aondb ehaviotuhraeatnul sr e rtahperi edn eowfat lh wea ter
p
r
�
chrlpoolats
�
� rteetinno
\: Jr-------J......,
"
nutorni li
trsapnort
r::r�",C HO
cehmical
�'lCHO
denfcee
X
FIGURDEi agrarnrmeaptriecs oeftn htweao trikooinfan s gasc ogAlboosvspaearn,ot. fs s tahceo ng'loss sa
L
digetsutbBieev.le ao f wu,n ctainsodyn mablro elspiercne toaftt hideoi ng etsutbWiehv.eei n et a tthsa,en imal
holtdhfseo opdl awnitt hl i(ipmtsa)s n pde rfotrhpaelt acenestl w listt hhre a d(urlw)ah, it lhpeeh arynx
(f)
woraksass ucptuimofpnot rh e s(tsoatml)as;co h sthhosewa nlg ilavaraneld sw h(ossl)ye.s wtToerhmlke is k e
as yr(ibnegleTo hwpe)l .ac nytt opilnagseimsds ti esdt rtihbruottuhdegeidh v erttihcel edsi goefs tive gland (dg)
(trancsnapalob erlotw .) Int eh clesl oft eh foarementniedo digesgtliavntedh p,el aonrtg anaenldlJetoshr e
moleciunlveoislnt v hedede feonftc haeel gaarreee tainetdob eu isneltdaa tbceyttr h,m e o ll(ussccrt oe en
captsuorlreaa rd iaantodir ognam noilce bceulloTewh )pe.l asnatip n geisslt iekde uwsieasdsfe o od. The
materialn outws heidrc ehti ustir ostn hesedt omfarcowhmh, e iritesm ovteodt h aen us (at)h et hrough
inte(siTt)hi.din isea gsrhaomaws sa cog(laoEnsl syainsf ioird aeexa,m lpaltpeea)rr aalwp( ioptd)hi, a which in
thPeo lybraannScdth eiirliiiddgaaee ared osrauspbapslet ni(dtcauegtreeasdt af)o.r
276 ROS& MARíN
TA BELI IS.ac ogslpoesfcsriaotenmhs s e o uetaohsfS t p asitnu bdyit ehadeu thsopresoc,fai legsua seae fsdo od
anfdu nccthiloonraolp lians tmt ohrleel Ttuhessency tsmi.boi onnl lsta chsoetl uirnndni tchaatte ex tihsoetf e nce
functciholnoarhloa psl acbsoetnesfn i( r+t)mh,ea dt m otlhldeuo secsr enttoahtie (nm- o )rt, h iahtta s yentot
beepno sstiotb eflsoettr h p er eseanbcseeo nfsoc urec h orgNaon ealthltaebessem empnat d teod istinguish
O).
dfiefrednetg roefke lse pt(oiptlnhsa ees ntosyfCe L AReKta l,.1 990T)h.re e feraerinedc eensit ntif hiee d
biblioOgt,rh paiapsph eyr;.
SACOGLOSSAN ALGAFLOOD CHLOROPLAST
RETENTION
Ascofbrguail(llJiaes f 1f58r6e)y s, Caulperroeprl(aai4 1 f,1) 5
Oxynoolceie vRaaai fnes1q8u1e9, Caulperroeprl(aai 1, f1 4)5 -(41,1 5)
Lobisgeerrr a(dCiafla1c4l8a0cr)ia , Caulperroeprl(aai4 1 f,1) 5 -(1,1 4)5
ElyfsliaVave iarl r1l9,0 1 Cldaophsop?r(. a 1, 1 4)5, +( 1,1 4)5
Halismiemdua(l 5a)n s
Elygsoirad Tahnoamep& sJ oank1 189i8n , Cldaophsop(r4.1a,1 5) +( 1,1 4)5
Elytmsiii da(a R i1s8s)o1 ,8 Acetaabcueltaar(bi41,ua1 l ,52u1,m ) +( 1,14 ,5202,1 )
A.ca ly(c1,u1 4l)5u s
Elytsrsialanu Pcreunvso 1t59-7F ol, Udopteetai (o1,l14 a)5t a +( 1,1 4)5
Elysisa( Mvoinrt1i0a84dg)iu , Codifaurgmi( l1)e,2 b uCr.s a, +( 1,1 2,52 6)
C.t omen(t2o)s um
Thurhiodpielil a1( 58V3é)r any, Cldaophvoargaa b(4u1n,1)d 5,a +( 1,1 4)5
Pseuodrooscdmhefilucsre llata,
Derbteesniuai( sOs)i ma
BosemlilmieTatr iicnac1 9h80es e, Halitmue(nd1a,a1 4 ,51 )9, +( 41,1 5)
H.s imu(l5a)n s
Hermbaief(aiM doan t1a8)g1 u5, Griffith(si2a7 )f,l osc+u( l1,1o 4,5s2 a7 )
Lophossip(p.h1, 1o 4)5n ia
Hermpaaeuac (iPcriurvr1oa59t 4-)F olC,o difurimal ge C(.t2 o2m)e,n - +( 1,1 4)5
tos(u2mL) o,p hossipp(.h1, 1o 4)5n ia
Placcriedmao (nTirainn1ac9 8h2e)s e,U nknown
Placida( Adle&dnH edarrn ict1oi48cc3ka), C odituomm enCt.ofs riau1(gme9, ) , +( 1,1 0,41 ,52 6)
BryopsiCs. vp elrruma(mi 1o,l1s 4a)5a ,
Plavceicrditatli Oalr at1e89a2, Codituomm enCt.o suamd(,h7a 1)e,r ens
Bryospp(s.1,i1 4 s)5
Plavciird(iaTd riisn1 c78h3e)s e, Bryospp(s.1,i 14 s52 ,3) + (1,1 4)5
CailolpbaeelaDl O'urlbai 1g78n3y , Chaetolmionr(up1)mh 6 a -(1,14)5
ErcoclaaenriTuarl ienac1 9h8e2s e, Valountirai (c2u8l)ar is
Ercofluanne(irAaCe. oa s 1t68a7,) ChaetoameorrCep.lahu i,amn( 1,1 4)5, +( 1,1 4)5
Cladop(ho5r)o psis
Limapcoanpti(itMaaü tl1al77 e4r), CldaophrourpaeE snttreirso,sm po.r- (p9h1,,a21 ,41 )5
(31)C,.s er(i7cE)e.i;a n testinalis,
(8C).a,r cCt.va a,g ab(u1,n1 4)d5 a
thacto meisnc ontwaitchti t( RAHAT & 1898M;A RÍN & ROS,1 898J,EN SEN,
MONSEILSE1,79 9C;L ARKet a l,1. 891;1 991M;A RÍN eta l.1,99 1,a) lthotuhgeh
ROS& RODÍRGUEZ1,8 95;M ARÍN & moshti ghelvyo lfvoerdma sre eg g-eaters.
ROS1,89 9), Thedierv elopimsae lnsctoh aractbeyr ised
TheS acogslsoaanrsae l os charascetdea r hiigh piornoo pflo erctitholtarrovpahli c
by hai gthr opshpiiecac slait(iToanb IlIe)d ,ev eolpmenatn de npcsautleadm eta­
whicthu rtnhse imtn op erhatphsem ostm orpho(sCiLsA R&K GOETZRFIED,
stenophaogfo umsa rinhee rbiv1o7r98eCs;L ARK& JENSE1N8,9 1R;O S,
(CLAR&K DeFEREES,1 897M;A RÍN, 1891M;A RÍN,1 898M;A RÍN & ROS,i n
SYMBIOBSEIWTSE ENA LGACLH OLROPALSTAS NOS ACOLGOSSANS 277
FIGUR2E.Ch loorpla�hl I¡rc\ ew/m/l(Ilrcie{//o (/6xm0/00)Ie".l" c hlrooplasPt.p:y reinJoS: .sl carh.
FIGUR3E.D iegstitvuebo er E /ys/iiad/ als /hiowinga Jiegslicveel lw ilhi ntaccth olrolp�at�( x6 UU)U. eL.
chloro1pv,le assitac;lI oelnsmug i nabolr dLe,rl;i piicndI usiNo,nnu sc;l ;eP u,ps yrenoVi,mdi sc;vr iolli.
278 ROS&MARíN
preas)s. The aolrggaaln ealnlde sct yhteo plasm
Ins pitoef appear(iilnkgem ostw hicthh ecya rrsyt uck thteoma re
nudibrsapniecechs i)n r elatilvoewls yu rroubnyad h eodsm te mbra(nHWeA E S,
densiitnti heesni art uhraabli taastt hse,y1 799)i nw hosien tetrhieco hrl oroplasts
explpolniatts pecwiheisc hc haermei craelmlayui nnd aagmed( HWAE S & COBB,
relatiwveellldy e fend(ePdA UL& 1890)T.h ec hromoptluhasss tist uated
FENICAL1,89 6)o,rc a1ci(fCiLeAdR& K (Fig3s a.n d4 )r emafinunc tioannadl
DeFERESE1,89 7;M ARNÍ & ROS,i nc ontitnoup eh otosynwtihtehsiins e the
preas)st, h Seac oglospsearnfsoar kme ya nimcaellli, n s ornsep ieecfso artl eaasst
roilent hceo asetcaols ysitnwe hmisc h tlhoengyt harsme oen t(hHIsN DE& SMTIH,
live (CL&A.RD Ke FREES1E89,7 ;1 794M;A RÍN & ROS,1 899C;L ARKe t
MARÍN,1 898a)s,t hey amf arktaeic oonf al,1. 990).
thper imaprryo ducotfti homena rianned Thed uratoifot nh ep hotosynthetic
lagomoanc roph(ywtheisic sho theirswec apacoiftt hyer etaicnherdo mopilsa sts
hartdoo btaaivnla)ai btlote h feol lwoingd ireccotrlrayte eldt ot hed ifficiunlt y
troplheivsce. l obtaifnoionodgr,i no thweorr dtso, the
Thed iegsticveel olfst hem olludsecg roefec a1icciaftoifot nh ef ooadl ga
phagoctyhtece h romopilnta shtes a(lTgaablIl IeCI L;A RK& DeFREESE1,89 7;
cyotplas(mF ig2.; T RENHC, 1795;M ARÍN & ROS1,89 9T)h.ep hotosynthetic
HINDE1,7 93)wh,i eciht rheemra firnei en c apacoiftt yh e klep(tgoepnlearsatlsl y
thcey toploafts hmae nilmc aellso ra rem easuarsea dm ouonftr adioaccatribvoen
founidnd seia vcauo(lMeA ÍRN,1 898)f.i xpeedr ounfci htl orlolpi)hsu y slulay
FIGU4RE.D i gedsitvievroetfE li ycstuiilam aisd hao wsiinndggi lgeec setcliolvnset aiinntciahnclgto r(oxp lasts
6000)e.L c,h lorEo,rp oluaegsnhtd ;o prleactsuimlHiu,cmm i;t ochMo,sn mdormoituahs;f c ilbeSr ,set ;a Vr,c h;
miocvrilli.
SYMBIOSBIETSW EENA LGACLH OLROPALSTAS NDS ACOLGOSSANS 279
TA BLIEI AIs.ch o natneodnrt g amnaitccto enrot feTn A tB EL ICVa.r bfoinx artaitoens s evienr al
thael gsaple ceiaetbsey tn h Ieb erSia,gaclnoo sssaanc oglossrane latstocpi ehoclnio ercsoo,pn htyielnnl t
speciebsy t shateuu tdh(ioRerO&dsS R ODRIGUaEnZid,l lumTihnreae tfniecoraeners.ie d enitnithf ei ed
189;5M ARÍ1N89,8 M;A RÍ&N R O,S1 8981,89 9)b.i bglria(opFhryMo AmR Í&N R OS1,89 9).
sornfei ghuarbveees ee nst ibmyat thaeeud t ohfto hre
refnecr(ee* o)rb yu s( *.*W )hetnh earrete w o Carbfoinx aItlilounm,iR neaft.i on,
figutrheecsyo, r responadn odtl opd l aynoutnsg, IglCm ghC1rh -1¡.LE m-s-2l
recstpeiNvoetlteyh .ia tng,e netrhhaeil g,th heaers h
cont(eonrt l otwhteeh rOe M c ontoeftn htfe)o odA )M etdeirrsapneecaine s
algtahl,eo nagreferu nctcihornoamlor peltaasitnse d
byt hsea coglsopsescTaihnee rs e.fn ecreaesr e
Elystiiam ida 144 200 15
identiifnti hebedi i bolgra(pMhoiyde.ifd fr om
Elysviiar idis 95 126 11
MARÍ&NR O,S1 899).
Elystiraa nslucen6s8 100 15
Thuridhiolpleai 40 100 15
Algsaple cies As%h ,O M%, RefB.o selmliimae tica 45 100 15
(eabtyse anc ogslpoescsiaens ) Calliobpealelau la O 14
Limapocnatpiiat ataO 25
Cauplaep rroieflr(aA scobu1l.l4a9 8 .51 5
B)N on-tMeerdrisapneecaine s
frgailOixsoy,n oel ivacea,
Lobisgeerrr aaldciif)
Griffithfslioas culosa 30*7 0* Costasliiellila2an0 a-03e0 0 500 6
Elystiuac a 60 24
(Hermbaífeiad a)
Chaetomoareprheaa 30**7 0**
(Ercolaniafunerea)
Chaetomolripnhuam 30** 70** hig(hT abIlVe)s ,o metiamshe isga hst hat
(CalliboeplaleEua.fl uan,e rea) oft hfeo oadl giat s(eBAlLfL ESRTOES,
Clapdhoorvaa gabunda 371*.6 83*. 1894;M ARÍN,1 898M;A RÍN & ROS,
(Limapcoanptiitaa ta,
1899T;E RRAD&O SR OSi,np rse)s.
Thuridhiolpleai )
Clapdhoorsae ricea 32* 68* Theo xygeann dt hep hotosynthates
(Lc.a pitEaltyasf,il aa va) produbcyet dhc eh loro(pglclaoussatens d
Bryopspilsu mosa 32.46*7 .6*
other carbohywdirtlahit peaisnd,d s along
(Placdiednad riPt.vi icrai,d is)
Psuedolcrohodeisfsmur cleltaa 32.46*7 .6* proteairnesr )e leaisnetdto h ea nimal
(hTuridihlolpae O tissues R (eTtaR lE1.N7,9C 3bR;I ND&E
Derbetseinau is(sT.hi ompae i3)2. 4*6* .76** SMIT,R1 795;R IDNE,1 7981,8 93;R OS
Enteromionrtpehas tina3l9i*s 61* & RODÍRGUEZ1,89 5;M ARÍN & ROS,
(Limapcoanptiitaa ta)
Cladhoopraar c(tLac. a pita4t0a)* 6 0* 1899)I.nt hwiasy t,h meo ulslccna satisfy
Clapdhoorrau pestris 40*6 0* sornoef i tmse tabolic rweiqtuhi rements
(Lc.a pitEaltyasg,io ar danae) thiosr gamnaitct er osfua bustiodtyr ophic
Codifurmga il(eE lyvsiirai d4i2s.,0 5 8.01 8
oirgi(nSooe rns pechiaevasel so sbheoewnn
Placdiednad ritica,
Hermapeaau criac)i r toa bsorb aacmiiddnisoos l sdv ienw ater;
Acetabualcaertiaab ulum1 .29/ 26.94/ DeFREE&S CEL ARK1,9 9.I1 n) short, the
(Elytsiimai da) /371. /80.8 mucus prionda ubcuendd abnyct eh ese
Codivuemr mi(lEav.ri ar idi4s71,. 14 .77/
astrocpoondntssaa ism ucahs 3 6%o ft he
H.P .vp earutciiccPii.dlr elrana,dt rai)t /i25c.3a ,/ 25.9 r,4C fixbeydt hceh loro(pTlRaEsNtCesRt
Udotpeeat iolata 50.50.00 al1.7,90 1,79 2R;IN DE1,8 93;M ARÍN &
(Elytsriaan slucens) ROS, 1899),i n the foorfm
Codibuums ra( E.v iridis)5 4.4753 . mucopsoalcychaorris diemsp glulec ides
Codiaudmh al!rens 55*4 *5
(Placviedrat icillata) scuha sg aloascetT.h et rsaolncatoifo n
Valonia utricula6r.4i7s 35.3 glucipdreosnt,se a indl ipifdrmso the
(Ercolcaoneirau lea) chloroptlota hsmeto llaunstdch ,fe a ctth at
Halimteudnaa 551./1 .98/
ins ornsep ecuipte osa t hiorftd h cea rbon
(BDsemLiLn'liecata) i
Halimeda simulan/8s8. 800 ./1224. 40. 95 fxiedp hotosyntihsme ettiacbaolbllyiy s ed
(Bm.i metEilcsyaif,al ava) the acnielmlsrna ela ntsh apth otosynthesis
isa ni mporstoaunrtoc foe r gannuitcr ients
280 ROS&MARíN
fort hes caoglnoss swaithr etaiwnietdh tohueetn zymperse siennt th e algal
orglanlees. cyptlosam.A sacogloisscs oannns ttlay
Thep hotosypnrtohdeutcioctft i hoens ree newiitnsg soufpc phlryo mopblya sts
molclsui ssof t hsea moer daestr h aotft hef eeding neowna lgabeu,tt hefee ding
aglaet heeya t( TRENCeHla l.1,79 3b;fer quensceye mtso abbeo yteh at which
MARÍN1,89 8M;A RÍN & ROS, 1899)w.o ulbden ecersyis fai tosn loyjb cetive
Thes caogslsoanhso,w evearr,en otw erteh seu tbistuotfi otnnho en -functional
compleatuetloyti rcao,spi hnn onoef t hec hlolrao.sp tTshe scaogslaonsst,h en,
casesst udiiesdt hea lgahle rbi dveopreyon npd h otosyfnotrh eaosp nialsroy tf
comepetlly substitubtye dt het hemiert abroelqieucmei nr.t s
photosynotfht ehseki lse ppltsaot;s the Otheard ditiqouniaatlla tmievtbeao lic
degroefde e pencdeve anr ies accboerndeifhniagtv bsete oe n sugagpeasfrtrteo dm ,
thsep ecTiherso.u cgohn ventfeeidoinnatglh es impqluea ntitative ofc ontribution
them olclsua slscoo nsyt amnatnlagteo nutriTehnuttssh,.me o llusccosu sludb ssti
replacec hltohreo ptlhaadtse tcsa y oanna dnu nbalaonric necdo lmepte (tdhiaett
becoimneca tiTvheec. h romopclaansntoostft hael gsaalop r c yptloaswmh,i clha cks
diivdiesn iedt hmeo llucsb ecatuhseeay r et hcea rbdorthaeyso f atlhlgec aelwl allasn d
incapaobfl sey netsshiign chlohryolptluh s ctointssu at feood iwniptauh lt wo
5�A COGLO
FIGUR5E.D iagramrmeaptriecs oenftt haet ion
benebfriotuasgb hotu t absys otcbhieeat twieoenn
algcahlr omoapnldSa asctosg l(oasbsoaavnneds)
betwzeoeonx anatnhNdeu ldliaber( abneclThohswe ) .
organoertl hplele ascn etld lesp,e nodnti hncega se,
arien pcoorraitnte hdme o lltuhsrcot uhfgeeh e ding
2
proctehsaesn ;im muaslet ac to ntintuoeo nussulrye
therierp lacaelmtehinonttu ,hgb ehe tetsetra blished 4
constohret iraoe fpt lenatsaitnoidcn/del osmlsr a lya st
weeaknsed vemno ntThhsee. g gdson octa rry
chromooprzl oaosxtasna tntedhl el aelo artr hvea e
youancgq utihreem whfeinfr estetThd hea.eyr rows
goifnrgot mhp el apnste udostyotm hbmeiol olucn st
(aboovre )f trhosemy mbailognatt hmteoo l lusc
(belionwd)id cifaeftrete ynptoe fbs e nefitthesN fBorU RDAyI
sacoglaonsdts hanenu dibrraenstcpihev,ce1 l)y :
Deefns(itvahene i imscar ly potni fcio tossdp ecies
anodn o ccastihloeaen trsstd' efenssyisvtaeer mes
usetdo t hsea meen dbsy t hme ollu2s)c );
Transloofcp ahtoitoons y(ntthpheaa stseoasfg e
glucpirdoetasen,ild nii sdph sa bse edne monstrated);
Othbeern emfoirtsesp ,e cualnadt ipnrvooetv en
3)
(whiicnuhcd let hpea ssoafog lei goealnedm ents 3
vitafmiixnaostfn,i i otnrb oytg heaenl gal acnodn sort
6
fcaiitlatoifo nct haeli ccaitfpiroonc eisns etsh e
mollusIcnt) h.e molclounssdcoi-rratelt cghtaeilro en
arneo b ene(f4if)to tsrh oer ngeallest,h ew hile
zooxanatswh eleallso l batea,aic neirnptgra oitne ction
agaeixntsetr naalr dedi asnpg(ee6rar)sns,ewd, di th
thciascn o mptlheebtiiero locgyic(clseaMe lAe R ÍN
&R O,S1 9.9T 1hb)ee nfeoftrihf teo sodp ecointe hse,
otheri msho aranepd p,a reanltgu;ap eowt nhh itech he
sacogplroeesxys paenrsri eednuccee dp rgersaszuirneg
int hsea mper opoirnwt hiioicnth cs h romopdliaasgttrhcsaeo m n clcuabsnei odntr haoawntntl wyoo f
provtihmdeoe l lwuisptchho tos(y5nI)tht.ha n asot tet sh efsoeuc ro nsaorrtetr iumaeu tuaslyimsbtiiocs es
beesnh otwhnta htse a m(e7h )a ppweinttshha e n im(aall ga-saanczdooo gxlaonstshaenl lateh-en udibranch),
pr(ecyn iwdhairhciahavs )ey mbziooonxta notnh aeslsloacebi,ea ttwciehoernno moapnsldaa csotgsl ossan and
whidcehn dronaonetdoa lccieedafaanena e ndod ba tint,ho en bee twceindeanra innadu dibnrofatuni llclgifh n
at stahmete i mseec,o ndsayrmyb iFornottmhs i.ts h ree quoifms utuiatblee nefits.