PLOS ONE Comparative Composition, Diversity and Trophic Ecology of Sediment Macrofauna at Vents, Seeps and Organic Falls

Published: April 04, 2012 DOI: 10.1371/journal.pone.0033515 ea!ured in P"O# $olle%!
ions
Comparative Composition, Diversity and Trophic Ecology of Sediment
Macrofauna at Vents, Seeps and Organic Falls
An&elo . 'ernardino , "isa A. "e(in, Andre) *. +hurber, $rai& *. #,i!h
Astract
#edi,en!s asso%ia!ed )i!h h-dro!her,al (en!in&, ,e!hane seepa&e and lar&e or&ani% .alls su%h as )hale, )ood and plan! de!ri!us %rea!e
so.!/sedi,en! habi!a!s .ueled, a! leas! in par!, b- !he o0ida!ion o. redu%ed %he,i%als. 'iolo&i%al s!udies a! deep/sea (en!s, seeps and or&
,a%ro.aunal !a0a, bu! !here has -e! !o be a s-s!e,a!i% %o,parison o. !he %o,,uni!-/le(el a!!ribu!es o. sedi,en! ,a%roben!hos in (arious
1ere )e re(ie) 2e- si,ilari!ies and di..eren%es in !he sedi,en!/d)ellin& asse,bla&es o. ea%h s-s!e, )i!h !he &oals o. 314 &enera!in& a p
e0plora!ion and s!ud- o. ne)l- iden!i.ied redu%in& habi!a!s, and 324 iden!i.-in& !a0a and %o,,uni!ies !ha! o(erlap a%ross e%os-s!e,s. 5e
(en! and or&ani%/.all sedi,en!s are hi&hl- he!ero&eneous. +he- sus!ain di..eren! &eo%he,i%al and ,i%robial pro%esses !ha! are re.le%!ed i
habi!a!s inhabi!ed b- a ,i0!ure o. spe%ialis! 3he!ero!rophi% and s-,bion!/asso%ia!ed4 and ba%2&round .auna. $o,,uni!-/le(el %o,parison
or&ani%/.all ,a%ro.auna are (er- dis!in%! in !er,s o. %o,posi!ion a! !he .a,ille(el, al!hou&h !he- share ,an- do,inan! !a0a a,on& !hese
#!ress &radien!s are &ood predi%!ors o. ,a%ro.aunal di(ersi!- a! so,e si!es, bu! habi!a! he!ero&enei!- and .a%ili!a!ion o.!en ,odi.- %o,,
bio&eo%he,i%al di..eren%es a%ross e%os-s!e,s and )i!hin habi!a!s resul! in )ide di..eren%es in or&ani% u!ili6a!ion 3i.e., .ood sour%es4 and
%he,os-n!hesis/deri(ed nu!ri!ion. In !he Pa%i.i%, (en!s, seeps and or&ani%/.alls e0hibi! dis!in%! ,a%ro.aunal asse,bla&es a! broad/s%ales
+his has i,por!an! i,pli%a!ions .or !he %onser(a!ion o. redu%in& e%os-s!e,s, )hi%h .a%e &ro)in& !hrea!s .ro, hu,an a%!i(i!ies.
Figures
Citation: 'ernardino A, "e(in "A, +hurber A*, #,i!h $* 320124 $o,para!i(e $o,posi!ion, Di(ersi!- and +rophi% 7%olo&- o. #edi,e
#eeps and Or&ani% alls. P"o# O87 7344: e33515. doi:10.1371/journal.pone.0033515
Editor: 9:ni%a 9edina, ;$ 9er%ed, #%hool o. 8a!ural #%ien%es, ;ni!ed #!a!es o. A,eri%a
Received: O%!ober 20, 2011< Accepted: ebruar- 10, 2012< Published: April 4, 2012
Copyright: = 2012 'ernardino e! al. +his is an open/a%%ess ar!i%le dis!ribu!ed under !he !er,s o. !he $rea!i(e $o,,ons A!!ribu!ion "
unres!ri%!ed use, dis!ribu!ion, and reprodu%!ion in an- ,ediu,, pro(ided !he ori&inal au!hor and sour%e are %redi!ed.
Funding: A por!ion o. !he (en! and seep s!udies re(ie)ed here )ere suppor!ed in par! b- &ran!s .ro, 8au!ilus 9inerals 8iu&ini 39anu
35217 and O$7 0> 2?254 !o "A". 5hale, )ood and 2elp/.all s!udies )ere .unded b- &ran!s .ro, !he 8a!ional ;ndersea *esear%h $e
O%eani% and A!,ospheri% Ad,inis!ra!ion 3no) !he 5es! $oas! and Polar *e&ions ;ndersea *esear%h $en!er4, and 8a!ional #%ien%e
O%ean #%ien%es &ran! 00@?422 !o $*#. +his s-n!hesis )as suppor!ed b- !he $ensus o. 9arine "i.e 3))).%o,l.or&
suppor!ed b- !ra(el &ran!s .ro, !he ;ni(ersi!- o. #Ao Paulo and $h7ss. +he .unders had no role in s!ud- desi&n, da!a %olle%!ion and a
publish, or prepara!ion o. !he ,anus%rip!.
Competing interests: +he au!hors ha(e de%lared !ha! no %o,pe!in& in!eres!s e0is!.
PLOS ONE: Comparative Composition, Diversity and Trophic Ecology ... http://.plosone.org/article/in!o:doi/"#."$%"/&o'rnal.pone.##$$("(
" o! )) #%/#*/)#"+ )#:"#
Introduction
*edu%ed 3or Bredu%in&C4 sedi,en!s o%%ur )here anaerobi% ,e!abolis, or &eo%he,i%al pro%esses pro(ide a .lu0 o. redu%ed inor&ani% %he,
,e!hane4 !ha! .uel %he,oau!o!rophi% produ%!ion. #u%h sedi,en!s are )idespread in )e!lands, es!uaries and or&ani%/ri%h shel(es, and on
re&ions o. hi&h pri,ar- produ%!i(i!-. +he- are also .ound a! si!es o. h-dro!her,al (en!in&, ,e!hane seepa&e and lar&e or&ani% .alls su%h a
de!ri!us. Al!hou&h a (arie!- o. %he,i%als %o/o%%ur in !hese so.! sedi,en! e%os-s!e,s, 1 # is !-pi%all- ele(a!ed and pla-s a 2e- role in s!ru
#ul.ide is !o0i% !o ,os! ,e!a6oan !a0a D1E, D2E, al!hou&h so,e sedi,en!/d)ellin& !a0a ha(e adap!ed !o %ondi!ions o. lo) o0-&en and a
presen%e o. sul.ide. Due !o hi&h lo%al produ%!ion, ,e!a6oans in redu%in& sedi,en!s in !he deep sea are o.!en released .ro, !he e0!re,e .
!he ba%2&round %o,,uni!- 3e.&. D3E4. Ins!ead, %he,i%al !o0i%i!- ,a- dri(e in.aunal %o,,uni!- s!ru%!ure. In !his ,e!a/an
!hese so.!/sedi,en! redu%in& e%os-s!e,s in !he deep sea, and in.er !he role o. o0-&en and sul.ide in s!ru%!urin& !hese .ood/ri%h FoasesG.
9e!hane seeps, sedi,en!ed h-dro!her,al (en!s and or&ani% .alls are pa!%hil- dis!ribu!ed< !he- o%%ur ,os! .reHuen!l- near o%ean ,ar&ins
dep!hs D4E, D5E, D?E, D7E, D>E. 5hale .alls are ,os! li2el- !o be %o,,on alon& )hale ,i&ra!ion rou!es, 2elp .alls adja%en! !o %oas!al 2elp bed
(er- )idespread, are li2el- !o be ,os! %o,,on alon& .ores!ed ,ar&ins and near !he ,ou!hs o. ri(ers drainin& .ores!ed e%os-s!e,s. 1-d
!e%!oni% pla!e boundaries in%ludin& bo!h spreadin& %en!ers and ba%2 ar% basins, bu! onl- subse!s o. !hese habi!a!s ha(e so.! sedi,en! o(e
basal!s or pre%ipi!a!ed sul.ides. 9e!hane seeps are %o,,on alon& %on!inen!al ,ar&ins in areas o. hi&h pri,ar- produ%!i(i!- and !e%!oni% a
de.or,a!ion and %o,pa%!ion dri(e e,issions o. ,e!hane ri%h .luid D@E. +o&e!her, !hese e%os-s!e,s %rea!e a ne!)or2, e0!endin& alon& ,ar
basins, o. so.!/sedi,en! habi!a!s .ueled, a! leas! in par!, b- !he o0ida!ion o. redu%ed %he,i%als.
'iolo&i%al s!udies a! (en!s, seeps and or&ani% .alls ini!iall- .o%used on hard subs!ra!es and ,e&a.aunal !a0a, espe%iall- !hose )i!h %he,oa
D11E, D12E. +he s!ud- o. sedi,en! bio!a a! (en!s and seeps in par!i%ular, and !o a lesser e0!en! 2elp, )ood and )hale .alls, de(eloped ,ore
D1?E, D17E, D1>E, D1@E, D20E. Al!hou&h s%ien!is!s )or2in& in ,ul!iple redu%in& s-s!e,s ha(e s!udied si,ilari!ies be!)een s-,bion!/bearin& an
3e.&. D21E, D22E, !here has -e! !o be a s-s!e,a!i% %o,parison o. !he %o,,uni!-/le(el a!!ribu!es o. sedi,en! ,a%roben!hos a%ross deep/se
1ere )e %o,pare !he %o,,uni!- s!ru%!ure, .un%!ion and d-na,i%s o. ,a%ro.aunal in(er!ebra!es 3I300 J,4 inhabi!in& sedi,en!s a! ,e!ha
(en!s, and surroundin& )hale, )ood and 2elp .alls a! )a!er dep!hs I200 ,. Ken! and seep bio!a belo) 200 , !-pi%all- e0hibi! ,u%h &rea!
and relian%e on %he,oau!o!roph- !han !hose .ro, shel. dep!hs D15E, D23E. 5hile !here is a &ro)in& li!era!ure on !he ,e!a6oan ,eio.auna a
)hale .alls, )e li,i! our s-n!hesis !o !he ,a%roben!hos .or )hi%h !here are a lar&e nu,ber o. sa,ples anal-6ed )i!h rela!i(el- s!andard a
%o,parisons are li,i!ed !o !he Pa%i.i% O%ean, )here parallel da!a se!s )ere a(ailable a%ross a ran&e o. redu%in& e%os-s!e,s. Our re(ie)
and di..eren%es in !he sedi,en!/d)ellin& asse,bla&es o. ea%h s-s!e, )i!h !he &oals o. 314 &enera!in& a predi%!i(e .ra,e)or2 .or !he e0p
iden!i.ied redu%in& habi!a!s, and 324 iden!i.-in& !a0a and %o,,uni!ies !ha! o(erlap a%ross e%os-s!e,s.
Lradien!s in redu%in& a%!i(i!- are &enera!ed !hrou&h dis!an%e .ro, or&ani% or (en!/seep sour%es, and .ro, !e,poral %han&es in seepa&e,
pro%esses. In ,os! s-s!e,s, !he bio!i% response !o .lo) or seepa&e !hrou&h sedi,en!s &enera!es re%o&ni6able bio&eni% habi!a!s su%h as
po&onophoran .ields, (esi%o,-id and %la, beds, or su%%essional s!a&es lin2ed !o sul.ide a(ailabili!- D24E. Pre(ious )i!hin/habi!a! s!udies h
sedi,en! .aunas )i!hin !hese ,i%rohabi!a!s %an be dis!in%! D25E al!hou&h so,e ,a- be a subse! o. o!hers D20E.
Li(en !ha! sedi,en! ,i%robiolo&i%al and &eo%he,i%al proper!ies are li2el- !o be dri(ers o. in.aunal asse,bla&e s!ru%!ure, )e .irs! as2: 5h
and di..eren%es in bio&eo%he,i%al %ondi!ions o. !he (arious (en!/seep/or&ani%/.all so.!/sedi,en! habi!a!s and su%%essional s!a&esM
in sulfide pore-water distributions, methane availability and temperature will promote comparable macrobenthic assemblages and nutri
asse,ble and s-n!hesi6e ,a%roben!hos da!a .ro, sedi,en! %ores !a2en in di..eren! redu%in& e%os-s!e,s. 5e as2 )he!her !here are asp
s!ru%!ure, in%ludin& pa!!erns o. abundan%e, !a0ono,i% %o,posi!ion, di(ersi!- or li.es!-les, shared a%ross ,a%roin.aunal asse,bla&es o. (e
.alls. We hypothesize that all systems at high sulfide concentrations will exhibit enhanced density, reduced diversity, and shared familie
bearing and heterotrophic taxa. or !hose s-s!e,s .or )hi%h s!able iso!ope da!a ha(e been %olle%!ed, )e assess !rop
%on!ribu!ions o. %he,oau!o!rophi% and pho!os-n!he!i% produ%!ion, !he %on!ribu!ions o. ,e!hane, and !he i,por!an%e o. sul.ide o0ida!ion in
e(alua!e !he i,pli%a!ions o. e%olo&i%al si,ilari!ies and di..eren%es .or le(els o. ende,i%i!- o. !he .auna asso%ia!ed )i!hin !hese e%os-s!e,
Methods
Da!a se!s
Seeps.
5i!h !he re%en! dis%o(er- o. a ,e!hane seep in !he #ou!hern O%ean D2?E, ,e!hane seeps are no) 2no)n in all o%eans
2
) o! )) #%/#*/)#"+ )#:"#
da!a are li,i!ed !o !he nor!heas!ern and sou!h)es!ern Pa%i.i% O%ean, !he Lul. o. 9e0i%o, and !he eas!ern A!lan!i% 3
, !o 44>0 , )a!er dep!hs, )i!h !he &rea!es! nu,ber .ro, alon& !he 7as!ern Pa%i.i% ,ar&in s!re!%hin& .ro, $os!a *i%a !o !he Aleu!ian Isl
able !. "lobal chemosynthetic ecosystems and study sites #here sediment macro$aunal data #ere available and analy%ed
doi:10.1371/journal.pone.0033515.!001
&ents.
5hile !he ,ajori!- o. h-dro!her,al (en! habi!a!s are pri,aril- hard subs!ra!e, a nu,ber o. 2no)n (en!s sus!ain h-dro!her,al .luids e..lu0 !
+he in.aunal ,a%roben!hos .ro, (en! s-s!e,s in !his s!ud- in%lude sedi,en!ed (en!s .ro, Lua-,as 'asin 31>00N2000 ,4, 7s%anaba +ro
Kalle- 32400 ,4, Lalapa&os 9ounds 32700 ,4, and 9anus 'asin 31430N1?30 ,< +able 14. +he ,os! de!ailed Huan!i!a!i(e anal-ses o. ,a
%ondu%!ed in 9iddle Kalle-, 87 Pa%i.i% D27E and a! !he #ol)ara and #ou!h #u ,inin& e0plora!ion si!es )i!hin 9anus 'asin, #5 Pa%i
'rganic $alls.
+he ,os! %o,ple!e su%%essional s!ud- o. in.aunal ,a%roben!hos a! a )hale .all )as %ondu%!ed in !he 87 Pa%i.i% on an i,plan!ed 30/!on &
robustus4 s!udied o(er 7 -ears a! 1?70 , dep!h in #an!a $ru6 'asin D1?E, D2>E, D2@E 3+able 14. #edi,en! sa,ples )ere %olle%!ed a! 0 !o 1
)hale %ar%ass, allo)in& %o,parisons o. %o,,uni!- s!ru%!ure a! di..eren! le(els o. or&ani% enri%h,en! and sul.ide %on%en!ra!ion
o. ,os! o!her )hale %ar%asses ha(e used i,a&in& or bone %olle%!ions !o .o%us on ,e&a.auna and bone epi.auna so !hese )ere no! in%lud
D35E. +he e..e%!s o. or&ani% enri%h,en! .ro, )ood and 2elp .alls on !he sedi,en! ,a%ro.auna )ere Huan!i!a!i(el- s!udied in !he 87 Pa%i.i%
.alls 3100 and 200 2& ea%h, respe%!i(el-4 )ere deplo-ed a! 1?70 , dep!h and re(isi!ed a.!er 0.25 !o 5.5 - D17E. #edi,en! sa,ples )ere !
O100 , dis!an%es, pro(idin& !he .irs! robus! unders!andin& o. in.aunal d-na,i%s a! !hese or&ani%/.all !-pes in !he deep 87 Pa%i.i% 3
Da!a anal-sis
9a%roin.aunal abundan%e and %o,posi!ion )ere s!a!is!i%all- %o,pared be!)een si,ilar habi!a!s a%ross (en!s, seeps and or&ani%/.alls 3
$o,,uni!- anal-ses )ere ,ainl- per.or,ed on da!ase!s !ha! had spe%ies %oun!s and repli%a!ed sa,ples .ro, sin&le habi!a!s, )hi%h li,i!
e0a,ined da!a se!s. Al!hou&h ,os! si!es )here spe%ies abundan%e ,a!ri%es )ere a(ailable )ere in%luded in !he da!a anal-sis 3
!he li!era!ure a(ailable .ro, ,an- o!her si!es and re&ions 3+able #14. Abundan%e da!a )ere nor,ali6ed !o 1 , , and ea%h %ore sa,ple !re
sin&le habi!a! 3see belo)4. Due !o di..eren! sa,plin& e..or!s, !he nu,ber o. repli%a!es )i!hin ea%h habi!a! per si!e (aried 38 P 2 !o 204, and
e%olo&i%all- %o,parable dep!h ran&es and su%%ession s!a&es 3a! or&ani% .alls4 )i!hin ea%h habi!a! )ere %o,bined in order !o .a%ili!a!e s!a
or&ani%/.all habi!a!s, )e in%luded onl- sa,ples adja%en! !o e0peri,en!s 30 ,4, )here redu%in& %ondi!ions are li2el- !o be ,os! in!ense a!
3e.&., D31E4. Al!hou&h sedi,en!s a! &rea!er dis!an%es 3up !o 10 ,e!ers4 e0hibi! dis!in%! ,a%ro.aunal %o,,uni!ies %o,pared !o ba%2&round
li2el- represen! di..eren! redu%in& %ondi!ions and habi!a! !-pes. or !he )hale .all, da!a are in%luded .ro, !i,e poin!s o. 4.5, 5.> and ?.> -
5.5 -r, and .or 2elp/.alls .ro, 0.25 -r a.!er e,pla%e,en! D17E, D32E. #!a!is!i%al anal-ses o. ,a%ro.aunal densi!- )ere %ondu%!ed )i!h A8O
ho,o&enei!- o. (arian%es. or si&ni.i%an! A8OKA resul!s, post-hoc !es!s )ere used !o e0a,ine di..eren%e in ,eans usin& !he s!a!is!i%al p
9a%ro.aunal %o,posi!ion )as &enerall- %o,pared a! !he .a,il- or hi&her le(els, -ieldin& up !o 73 dis!in%! !a0a )i!hin a! leas! one sa,ple.
e(alua!ed .or pooled repli%a!e %ores a! ea%h habi!a! and si!e sa,pled 3n P 1N44 due !o !he lo) densi!- o. ,e!a6oans. 1ulber!Qs 31@714
rare.a%!ion 37# 4 )as used !o %o,pare spe%ies di(ersi!- be!)een !rea!,en!s.
2
n
$ o! )) #%/#*/)#"+ )#:"#
Figure !. "lobal distribution o$ (no#n chemosynthetic ecosystems.
$olored do!s represen! Huan!i!a!i(e .aunal s!udies a! h-dro!her,al (en!s 3red4, %old seeps 3blue4, and or&ani% .alls 3&reen4. 'la%2 do!s
%he,os-n!he!i% si!es used .or %o,parisons onl-.
doi:10.1371/journal.pone.0033515.&001
8on/,e!ri% ,ul!i di,ensional s%alin& 39D#4 and $lus!er !e%hniHues )ere used !o %o,pare %o,,uni!- s!ru%!ure a%ross habi!a!s 39i%robia
1-dro!her,al ,uds, renula!e .ields, Or&ani%/ri%h sedi,en!s4 and %he,os-n!he!i% s-s!e,s 3Ken!s, #eeps and Or&ani% .alls<
based on 'ra-/$ur!is si,ilari!ies %al%ula!ed .ro, .our!h/roo! !rans.or,ed, .a,il- abundan%e da!a .ro, s!andardi6ed Huan!i!a!i(e sa,ples
si,ilari!- !es!s 3A8O#I9 rou!ine4 )as used !o de!er,ine si&ni.i%an! di..eren%es a,on& &roups iden!i.ied b- %lus!er and 9D# !e%hniHues. D
.our!h/roo! !rans.or,ed, s!andardi6ed Huan!i!a!i(e da!a )ere ob!ained .ro, #I9P7* anal-sis D37E. 'ased on ,ul!i(aria!e dispersions .ro,
all si!es, )e !es!ed !he null h-po!hesis o. no di..eren%es in )i!hin/&roup dispersion a,on& &roups usin& !he P7*9DI#P rou!ine
.or di..eren%es in be!a di(ersi!- a,on& si!es 3Ken!s, #eeps and Or&ani%/.alls4 and habi!a!s, based on 'ra-/$ur!is rese,blan%e on presen
dissi,ilari!- inde04 .ro, all si!es 3P*I97*< D3@E4.
Results
'io&eo%he,i%al pro%esses
&ents.
1-dro!her,al (en!in& !hrou&h sedi,en!s is asso%ia!ed )i!h ele(a!ed sedi,en! !e,pera!ures and sul.ide %on%en!ra!ions, and !he o%%asiona
,a!s or (esi%o,-id %la,s. 7n(iron,en!al and bio&eo%he,i%al pro%esses in deep/sea h-dro!her,al (en! s-s!e,s di..er si&ni.i%an!l- .ro,
D41E. +he pronoun%ed !e,pera!ure di..eren%es a,on& (en! si!es !-pi%all- o%%ur due !o di..eren! si6es o. (en!in& areas and (ariable di..usi(
su%h as a%!i(e si!es near (en!in& %hi,ne-s, ina%!i(e (en! sedi,en!s or ,i%robial ,a!s D23E, D27E, D42E, D43E. Deep/)a!er h-dro!her,al .luid
o. 400R$ D23E. Al!hou&h !he (en! ben!hi% bio!a is usuall- .ound in !e,pera!ures be!)een 10 and 25R$ D44E, !e,pera!ures up !o @4R$ %an o
sedi,en! %olu,n in (en! habi!a!s D27E. $on%en!ra!ion o. inor&ani% %he,i%als in deep/)a!er (en! .luids (ar- si&ni.i%an!l- )
a! a%!i(e (en! sedi,en!s !here are usuall- hi&h %on%en!ra!ions o. $1 , 1 #, 1 and ,e!als D23E. 7nd ,e,ber (en! .luids are enri%hed in su
.or,ed b- !her,al sul.a!e redu%!ion and basal! lea%hin& abo(e 250R$ D45E, )hile ,e!hane %on%en!ra!ions are !-pi%all- sub/,illi,olar in %o
#edi,en!ed h-dro!her,al areas %an be re&arded as &eo%he,i%all- si,ilar !o ,e!hane seeps bu! )i!h ele(a!ed !e,pera!ures in pore .luid
$o,pared !o basal!/hos!ed h-dro!her,al (en!s, !he- are ,ore enri%hed in ,e!hane 3up !o 2 orders o. ,a&ni!ude4
ri%h in redu%ed ,e!als. #edi,en!/%o(ered (en! .ields are si&ni.i%an!l- lo)er in !e,pera!ure !han bare/ro%2 (en!s. #edi,en!s appear !o .a%
and reeHuilibra!ion o. hi&h/!e,pera!ure .luids be.ore (en!in& o%%urs a! !he sedi,en!/)a!er in!er.a%e. In %on!ras! !o basal!/hos!ed h-dro!he
sedi,en!ed areas are enri%hed in ,e!hane and h-dro&en due !o !her,o&eni% de%o,posi!ion o. sedi,en!ar- or&ani% ,a!!er
enhan%es ,i%robial sul.a!e/redu%!ion ra!es, leadin& !o enhan%ed sul.ide %on%en!ra!ions in sedi,en!s D4@E, D50E, D51E
h-dro!her,al/(en! sedi,en!s and are %onsidered an i,por!an! .ood sour%e .or ,a%ro.aunal or&anis,s a! so,e (en! si!es
ba%!eria do,ina!e a! ,an- (en! si!es, bu! !he o%%urren%e o. ,e!hano!rophi% ba%!eria is also %o,,on in sedi,en!ed A!lan!i% and Pa%i.i% (e
Seeps.
9e!hane seep habi!a!s %onsis! o. a %on!inuu, .ro, ba%2&round !o hi&hl- sulphidi% sedi,en!s asso%ia!ed )i!h ,e!hane e,ission. As ,e!h
deep/subsur.a%e reser(oirs alon& subsur.a%e de.or,a!ions and .aul!s, i! %an be ini!iall- o0idi6ed anaerobi%all- b- a s-n!rophi% %onsor!iu,
+his pro%ess, !he anaerobi% o0ida!ion o. ,e!hane 3AO94, %o,,onl- uses sul.a!e as !he ele%!ron a%%ep!or 3bu! see
bo!h respired and i!s %arbon used !o build !he ,i%robial %onsor!iu, bio,ass D53E, D54E, D55E. +hese %onsor!ia are %o,posed o. ,e!hano!ro
4 2 2
+ o! )) #%/#*/)#"+ )#:"#
sul.a!e redu%in& ba%!eria. As bo!h ,e!hane and sul.ide, !he la!!er .or,ed .ro, AO9, rea%h o0-&ena!ed sedi,en!s or !he o(erl-in& )a!er
o0ida!ion and ,e!hano!roph- 3,e!hane o0ida!ion4 pro(ide !)o addi!ional pa!h)a-s o. %arbon .i0a!ion, bo!h o. )hi%h are %arried ou! b- ba%
S/ pro!eoba%!eria< D5?E, D57E4. As in all o. !he o!her redu%in& habi!a!s, !he sul.ide/o0idi6in& ba%!eria %an be lar&e enou&h !o be (isible !o !he
%rea!in& ,i%robial ,a!s. 9a! %ons!i!uen!s e0hibi! ,i0o!roph-, %o,binin& %he,oau!o!rophi% produ%!ion )i!h he!ero!roph-
In addi!ion !o ,i%robial ,a!s, a (arie!- o. o!her habi!a!s o%%ur a! ,e!hane seeps, )hi%h are iden!i.ied b- !heir do,inan! ,e&a.auna and re
underl-in& bio&eo%he,is!r-. 9i%robial ,a!s %o,,onl- sus!ain hi&h ,e!hane e,ission ra!es and !he &rea!es! %on%en!ra!ions o. sul.ide 3rea
%on%en!ra!ion )i!hin !he sur.a%e sedi,en!s4. $la, beds 3inhabi!ed b- %he,os-n!he!i%, s-,bion!/bearin& (esi%o,-id and sole,-id %la,s4
3sibo&linid pol-%hae!es pre(iousl- re.erred !o as po&onophora4 are %hara%!eri6ed b- lo)er sul.ide %on%en!ra!ions near !he sedi,en! sur.a
beds also ha(e lo)er and/or os%illa!in& .luid .lo) %o,pared !o ba%!erial ,a!s D?0E, D?1E. +he %la,s !he,sel(es bio/irri&a!e !he sedi,en!, e
pene!ra!ion !o 3 !o ? %, belo) !he sedi,en! sur.a%e D?2E< in ,i%robial ,a!s o0-&en pene!ra!ion is T1 %,. In %er!ain habi!a!s, a,phare!id p
densi!ies 3I35,000 indi(iduals , < D?3E4. +he a,phare!id !ubes ,a- .a%ili!a!e up)ard !ranspor! o. ,e!hane as !his habi!a! e0
2no)n .ro, non/bubblin& si!es 3I200 ,,ol ,e!hane , da-< D?4E, D?5E. +hese .our seep habi!a!s re.le%! &eo%he,i%al and !rophi% he!ero
able ). Sediment organic content and ma*imum sul$ide $or (elp+, #ood+ and #hale+$alls.
doi:10.1371/journal.pone.0033515.!002
+he di..eren! bio&eo%he,is!r- !ha! underlies ea%h o. !he seep habi!a!s leads !o dis!in%! !rophi% si&na!ures in !he .auna. 9e!hane %an be .o
&eolo&i% pro%esses or !hrou&h AO9< !his la!!er pro%esses ,a- be !he do,inan! sour%e o. ,e!hane .or seep s-s!e,s
!he role o. ,e!hane/.ueled produ%!ion. 'io&eni% ,e!hano&enesis, or ,e!hane .or,ed b- AO9, i,par!s a hi&hl- s2e)ed ra!io o. $
iso!ope. +his uniHue iso!opi% ra!io 3$ /$ 4 pro(ides a ,e%hanis, !o iden!i.- ani,als !ha! %onsu,e !his !-pe o. produ%!ion, as a
is deri(ed .ro, !heir die!. 5hile AO9 ,edia!ed ,e!hano&enesis resul!s in !he ,os! ne&a!i(e iso!opi% si&na!ure 3re.erred !o as U
%o,pared !o a s!andard4, !he o!her sour%es o. .i0ed %arbon, in%ludin& sul.ide o0ida!ion, sul.a!e redu%!ion, aerobi% ,e!hane o0ida!ion, as )
produ%!ion .ro, !he o(erl-in& )a!ers, all i,par! a %hara%!eris!i%, al!hou&h o.!en o(erlappin&, U $ si&na!ure D??E. $arbon is .i0ed a! seeps
pa!h)a-s in%ludin& !he r+$A %-%le and !he $al(in/'enson/'essha, %-%le D?7E. +hus, s!able iso!ope s!udies ha(e pro(ided insi&h!s in!o !h
,e!hane/based %he,oau!rophi% produ%!ion pa!h)a-s 3e.&. D?3E, D?>E, D?@E and uniHue bio,ar2ers presen! in aerobi% ,e!hano!rophi% ba%!
use o. ,e!hano!rophi% produ%!ion b- seep ,eio.auna and ,a%ro.auna D70E, D71E. +he role o. anaerobi% ,e!hano!roph- re,ains eni&,a!i%
does su&&es! !ha! ar%haeal bio,ass asso%ia!ed )i!h AO9 is %onsu,ed b- in.auna li(in& in ,i%robial/,a! and %arbona!e habi!a!s
'rganic $alls.
+he na!ure and ,ass o. indi(idual or&ani% .alls a! !he deep/sea .loor ,a- ha(e ,ajor e..e%!s on de%o,posi!ion ra!es, and ul!i,a!el- in.lue
ben!hi% ,i%robes and in(er!ebra!es a! !he .all si!e D30E. $ar%asses o. dead )hales %an deli(er o(er 30 !ons 3per )hale4 o. .resh or&ani% ,
.loor D73E. As a resul! o. rapid dispersal o. .lesh .ro, !he %ar%ass b- s%a(en&ers, and !he in!rusion o. bones and so.! !issue in!o sedi,en!s
sedi,en!s around )hale %ar%asses be%o,e ,assi(el- enri%hed in or&ani% ,a!erial 3+able 2, D1?E, D31E4. Anaerobi% de&rada!ion o. or&ani%
produ%!ion o. sul.ides and ,e!hane )i!hin !he sedi,en!s around !he )hale .all, suppor! rapid 3T1> ,on!hs4 de(elop,en! o. %he,oau!o!rop
)hale/.all sedi,en!s D1?E, D31E, D32E. In or&ani%/ri%h sedi,en!s near a )hale .all, sul.a!e/redu%!ion ra!es %an in%rease b
ba%2&round sedi,en!s, rea%hin& 300 !o 700 ,,ol , d D31E and -ieldin& sul.ide %on%en!ra!ions up !o 20 ,9 D1?E
dra,a!i%all- near )hale .alls, indi%a!in& !ha! ,e!hano&enesis is an i,por!an! de&rada!ion pa!h)a- )i!hin !he )hale/.all in.luen%ed sedi,en
5ood is %o,posed o. hi&h %on%en!ra!ions o. rela!i(el- re.ra%!or- or&ani% ,a!erials, in%ludin& %ellulose and li&nin D75E
,a!erial is ,edia!ed b- )ood/borin& Xylophaga bi(al(es and de%o,posi!ion is ,edia!ed b- .un&ae and ba%!eria D7?E
)ood de%o,posi!ion )i!hin )ood par%els ,a- be en(iron,en!all- lin2ed !o i,,ersion period, o0-&en %on%en!ra!ions and )ood !-pe
and bio%he,i%al proper!ies o. !he subs!ra!e. +he release o. par!i%ula!e or&ani% ,a!!er and Xylophaga .e%al ,a!erial !o sedi,en!s nearb-
or&ani% enri%h,en!, anaerobi% ,i%robial ,e!abolis,, and ,odes! enhan%e,en! o. pore/)a!er sul.ide %on%en!ra!ions in nearb- sedi,en!s
D4@E.
Velp par%els %on!ain ,u%h ,ore labile or&ani% ,a!erial !han )ood, and !hus are s%a(en&ed b- in(er!ebra!es and de%o,posed b- ,i%robe
W2
W2
12 13
13
W2 W1
( o! )) #%/#*/)#"+ )#:"#
)ood .alls o. si,ilar ,ass D17E, D7@E. As a resul!, par!i%ula!e or&ani% ,a!erial is rapidl- released !o underl-in& sedi,en
in%reases pore/)a!er sul.ides %on%en!ra!ions )i!hin 3 ,on!hs 3up !o 1.5 ,9 1#< D30E4, allo)in& !he de(elop,en! o. ,i%robial ,a!s
,a!!er release and ,i%robial sul.ide produ%!ion, and !heir in.luen%e on ,a%ro.aunal su%%ession in sedi,en!s, )ill be dis%ussed belo).
In(er!ebra!e %o,,uni!- s!ru%!ure: 9a%ro.aunal abundan%e and %o,posi!ion
&ents.
'ased on a li,i!ed nu,ber o. s!ud- si!es, !here is no %onsis!en! enhan%e,en! o. ,a%ro.aunal densi!- or bio,ass a! h-dro!her,all- a%!i(e
ina%!i(e si!es 3+able #14. aunal densi!- responses appear !o be a .un%!ion o. s!ress le(el. or e0a,ple, a! 9iddle Kalle- 32410 ,4, e0!re
@4R$ a! 5 %, in!o !he sedi,en! %olu,n4 suppor! (er- .e) ,a%ro.auna, )hereas ,odera!el- )ar, sedi,en!s inhabi!ed b- (esi%o,-id %la,
,a%ro.aunal densi!ies 31?,500 ind , 4 rela!i(e !o !hose in ,i%robial ,a!s 3?,>40 ind , 4, ho! sedi,en! 31,?@0 ind ,
2@.@, PT0,001< i&ure 24. 'io,ass di..eren%es a,on& ,a%ro.auna in 9iddle Kalle- habi!a!s are less dra,a!i% 3and no! s!a!is!i%all- di..ere
ran2in& !o densi!- D27E. In 9anus 'asin, ,a%ro.aunal densi!ies )ere lo) a! !)o ina%!i(e si!es and one a%!i(e si!e 3T1,000 ind ,
ano!her a%!i(e si!e 3#ou!h #u / 3,4@4 ind , 4, due !o !he presen%e o. rela!i(el- lar&e spionid pol-%hae!es and nu%ulanoid bi(al(e
100/.old rela!i(e !o a nearb- ina%!i(e si!e.
Figure ). Macro$aunal density per habitat across &ents -upper panel., Seeps -middle panel., and 'rganic+Fall -lo#er panel. e
A(era&e (alues 3X1 #74.
doi:10.1371/journal.pone.0033515.&002
1-dro!her,al sedi,en!s )i!h ele(a!ed densi!ies are %hara%!eri6ed b- hi&h do,inan%e and an absen%e o. lar&e nu,bers o. rare spe%ies 3
so,e ins!an%es, spionid pol-%hae!es 3&enus Prionospio 3Minuspio44 do,ina!e 320N?0Y o. abundan%e a! #ou!h #u in 9anus 'asin and 9
34. #-llid pol-%hae!es 3Sphaerosyllis sp.4 are also abundan! in 9iddle Kalle- ho!/,ud sedi,en!s, as )ell as in %la, beds a
3uculana spp.4 are a )idespread &roup %o,,on in 9anus 'asin a%!i(e and ina%!i(e sedi,en!s, !o&e!her )i!h !anaid and isopod %rus!a%
dor(illeid and hesionid pol-%hae!es are also )ell represen!ed in h-dro!her,al sedi,en!s o. !he 7. Pa%i.i% 3+able #1
W2 W2
W2
* o! )) #%/#*/)#"+ )#:"#
Figure /. Macro$aunal composition #ithin habitats in &ent, Seep and 'rganic+Fall ecosystems.
Kalues are rela!i(e abundan%e 3Y4 o. all sa,ples )i!hin ea%h habi!a!/si!e. $olor/%ode: Pol-%hae!es 3pa!!erns in bla%24< 9ollus2s 3in blu
and O!her !a0a 3purple4. A,phare!id beds represen!ed onl- in 8e) Zealand.
doi:10.1371/journal.pone.0033515.&003
Seeps.
#eep habi!a!s %o,,onl- ha(e in%reased ,a%ro.aunal densi!- %o,pared !o ba%2&round sedi,en!s 3e.&., D>0E4, -e! !here are e0%ep!ions !o
upper ba!h-al dep!hs 3i&ure 24. In.aunal densi!ies .or seep ,a%ro.auna ran&e .ro, 2,400 3#an $le,en!e ,e!hane seep
Zealand4 )i!h a ,ean o. 20,200X>?0 ind , . +he ,a%ro.auna o. !hese habi!a!s are .ar ,ore dense !han ba%2&round si!es, )hi%h ra
9e0i%o, 3300 ,4 !o 1@,7?0 ind , 37el *i(er, 500 ,4, )i!h a ,ean o. >,1>0X>70 ind , . In !he .our &eo&raphi% lo%a!ions )i!h ,i%robial
had ,i%robial/,a! ,a%ro.aunal densi!ies T0.> !i,es !ha! o. %la, beds, )hile one 3$os!a *i%a4 ha(in& o(er 2.0 !i,es !he densi!- in ,i%rob
beds. renula!e .ields in all %ases had in%reased ,a%ro.aunal densi!- %o,pared !o re.eren%e si!es. A,phare!id beds had !he hi&hes! den
,ean densi!- on !he 8e) Zealand ,ar&in !ha! )as o(er 13 !i,es &rea!er !han an o../seep re.eren%e s!a!ion.
#eep in.auna in%ludes a subse! o. ba%2&round !a0a apparen!l- !oleran! o. hi&h sul.ide or )i!h beha(iors !o a(oid i!s !o0i%i!-. 5i!hin !he Pol-
are an abundan! %o,ponen! o. seep habi!a!s, a!!ainin& !he hi&hes! do,inan%e a! ,i%robial ,a! habi!a!s a! 7el *i(er seeps, and in .renula
9e0i%o and on !he 8or)e&ian ,ar&in 3+able #1, i&ure 34. +heir radia!ion and !oleran%e !o sul.ide is re.le%!ed in !he presen%e o. 30 spe%i
seeps o.. $A and O* 3D15E< unpubl4. A,phare!id and hesionid pol-%hae!es also appear !o be )ell sui!ed !o a )ide (arie!- o. seep habi!a!
sedi,en!/)a!er in!er.a%e, li2el- as a )a- !o ,ini,i6e sul.ide s!ress. +he a,phare!ids, )hile presen! in ,os! seep habi!a!s, )ere do,inan
and $os!a *i%a ,ar&in seeps, %o,prisin& 24X4Y, 4?X?Y and 14X3Y, o. !he .auna a! !hese lo%a!ions, respe%!i(el- 3
!he Lul. o. Luinea and a! !he 1[2on 9osb- (ol%ano D25E. 1o)e(er !he- )ere no! as abundan! in areas )i!h lo)er sul.ide %on%en!ra!ions,
!he- )ere absen! .ro, hal. !he sa,ples %olle%!ed.
5hile bo!h !he dor(illeids and !he a,phare!ids )ere )idespread a,on& !he seep habi!a!s, %er!ain &roups )ere do,inan! in jus! one or a
,a!s a! seeps on !he Ore&on, lorida, and $os!a *i%a ,ar&ins had uniHuel- hi&h rela!i(e densi!ies o. &as!ropods 3?3Y4, hesionids 37@Y4
respe%!i(el-. +here )as an in%rease in di(ersi!- in less sulphidi% habi!a!s, su%h as %la, beds and so,e .renula!e .ields, )i!h %irra!ulid, spio
pol-%hae!es as )ell as &as!ropods, a,phipods, and %u,a%eans, presen! a! ,an- o. !hese lo%a!ions 3i&ure 3, +able #1
o. .a,ilies in%ludin& !hose adap!ed !o hi&hl- sulphidi% seep habi!a!s 3e.&., dor(illieds4, &roups do,inan! in onl- spe%i.i% %ondi!ions and a! p
hesionids4, or !a0a !ha! sus!ain enhan%ed abundan%e asso%ia!ed )i!h hi&her produ%!i(i!- around seeps 3e.&, a,phare!ids4.
'io,ass is .reHuen!l- hi&her in seep sedi,en!s !han non/redu%in& habi!a!s. In !he 8ile del!a, ,i%robial ,a! in.aunal bio,ass )as 3750 !i,
D?@E. +he hi&hes! bio,ass o. he!ero!rophi% .auna )as .ound in 8e) Zealand a,phare!id beds )i!h a ,a0i,u, o. 27> & ,
,a0i,u, bio,ass, in%ludin& s-,bion! bearin& .auna, )as presen! in (esi%o,-id %la, beds, 1?1X50 & , , bio,ass in beds o. !he sole,
hi&h 3143X?7 & , 4. A! 1-dra!e *id&e, bio,ass )as ,odera!e in ,i%robial ,a!s 34?X23 & , 4, and lo)es! a! re.eren%e si!es 310X5 & ,
*id&e, si!es )i!h !he hi&hes! sul.ide %on%en!ra!ions had ,odes! bio,ass b- seep s!andard, -e! enhan%ed ,a%ro.aunal abundan%e.
'rganic $alls.
+he ,a%ro.aunal abundan%e in or&ani%/ri%h sedi,en!s around )hale, )ood and 2elp .alls )as %onsis!en!l- hi&her !han in ba%2&round sedi
%ar%ass in #an!a $ru6 'asin, $ali.ornia, ,a%ro.aunal densi!ies adja%en! !o !he )hale 30 ,4 rea%hed 41,5@? ind ,
4.5 !o ?.> - !i,e .ra,e 3+able #1, i&ure 24. 9e!er/s%ale pa!%hes o. or&ani%/ri%h sedi,en!s produ%ed hi&h he!ero&enei!- in in.au
sul.ide %on%en!ra!ions around !he )hale %ar%ass< )i!h !he hi&hes! ,a%ro.aunal densi!ies up !o 53/.old &rea!er !han ba%2&round le(els 37>0
,a%ro.aunal abundan%es 321,000N45,000 ind , 4 )ere obser(ed in sedi,en!s nearb- )hale .alls in #an Die&o +rou&h and 9on!ere- 'a
#14. A! 2elp .alls, ,a%ro.aunal densi!ies are enhan%ed 35,2>?X@@7 ind , 4 o(er spa!ial s%ales o. \1 , .or a! leas! 0.5 -. i(e/.old in%reas
sedi,en!s )ere obser(ed 3up !o >,320 ind/, 4, espe%iall- )i!hin or&ani%/ri%h, bu! rela!i(el- sul.ide/poor, sedi,en!s. 9a%ro.auna
par%els rea%h (er- hi&h nu,bers 31@,500 ind , 4.
W2
W2 W2
W2
W2 W2
W2
W2
W2
2
W2
% o! )) #%/#*/)#"+ )#:"#
A.!er !he onse! o. !he sul.ophili% s!a&e 3sensu D1?E4, ,i%robial ,a!s and pa!%hes o. bla%2 sedi,en!s de(eloped adja%en! !o !he )hale %ar%
are hea(il- %oloni6ed b- sul.ide/!oleran! or&anis,s su%h as dor(illeid pol-%hae!es and b- (esi%o,-id %la,s 3i&ure 3
.reHuen!l- be%o,es do,ina!ed b- dor(illeid 3I3?Y a! all si!es4 and a,phare!id pol-%hae!es, !he .or,er &roup bein& %o,posed o. a ,ul!i/
dor(illeid spp. D32E4. 9a%ro.aunal %o,posi!ion around or&ani% .alls e0hibi!s s!ron& si,ilari!- o. hi&h/le(el !a0a 3i&ure 3
2elp/ and )hale/.alls 3I15N30Y4. +his su&&es!s si,ilar %o,,uni!- responses !o or&ani% and sul.ide enri%h,en!. +he sul.ophili% s!a&e is b
%an las! .or a! leas! 5 !o ?.> -ears a! )ood/ and )hale/.all sedi,en!s, )i!h an apparen! &radual re/%oloni6a!ion b- ba%2&round spe%ies.
$ross/si!e ,ul!i(aria!e %o,parisons
$ross/si!e %o,parisons o. asse,bled da!a se! re(ealed si&ni.i%an! di..eren%es in ,a%ro.aunal densi!- be!)een %he,os-n!he!i% si!es and
(en!s, (esi%o,-id %la, beds a! 9iddle Kalle- (en!s e0hibi!ed !he hi&hes! ,a%ro.aunal densi!- 3pT0.001< i&ure 24. +he ele(a!ed ,a%ro.au
bed habi!a!s in 8e) Zealand seeps 35?,5@5 ind , 4, )ere si&ni.i%an!l- 3or ,ar&inall- si&ni.i%an!4 hi&her !han all o!her si!es %o,pare
densi!ies in !he li!era!ure also rea%h !hese le(els De.&., D2>E, +able #14. $la, bed and ,i%robial ,a! habi!a!s a! !he shallo)er $ali.ornian s
hi&her ,a%ro.aunal densi!ies !han ,i%robial ,a! habi!a!s a! (en!s, .renula!e .ields a! seeps, and or&ani% .all habi!a!s 3 P 7,7@, pT0.01<
a! 1-dra!e *id&e, O* and a! 7el *i(er, $A also had si&ni.i%an!l- hi&her densi!ies !han si,ilar habi!a!s a! $os!a *i%a and !he deepes! Vod
3pT0,014. renula!e .ields a! #an $le,en!e, ;ni,a2 and Vodia2 seeps had si,ilar ,a%ro.aunal densi!ies, bu! !hese )ere &enerall- lo)er
3i&ure 24.
A! !he .a,ille(el, !here is si,ilari!- be!)een 2elp/, )ood/, and )hale/.all in.auna, )hi%h also rese,ble seep and lo)er ba!h-al (en! si!es
si&ni.i%an! dissi,ilari!- in %o,,uni!- s!ru%!ure 3.a,ille(el4 )i!hin ea%h si!e, dep!h and habi!a!s 3i&ure 4 / AN$4. Ken! si!es .ro, !he 5es
di..eren! .ro, all o!her seep and or&ani% .all si!es, ,os! o. )hi%h o%%ur in !he 7 Pa%i.i% and are !hus hi&hl- separa!ed bio&eo&raphi%all- 3A
i&ure 4 / $4. A,on& (en! sedi,en!s 3i&ure 4 / A4, %o,,uni!ies in !he rela!i(el- shallo) 9anus 'asin 314>0 ,4 are si&ni.i%an!l- d
9iddle Kalle- si!e 32410 ,< A8O#I9 * P 0,??2, PT0.0014. Pol-%hae!es 3s-llids, dor(illeids and orbiinids4 and bi(al(es %on!ribu!ed ,os! !o
3#I9P7*, i&ure 34. A! 9iddle Kalle-, ,i%robial ,a!s )ere dis!in%! .ro, all o!her (en! habi!a!s 3pT0.0014, bu! %la, beds and ho! ,uds )e
ea%h o!her 3p P 0.0?< i&ure 44. +he dissi,ilari!- be!)een ho! ,ud and o!her (en! habi!a!s )as hi&her 3I7>Y4 !han b
#I9P7*4. #eep si!es e0hibi!ed s!ron& di..eren%es in ,a%ro.aunal %o,,uni!- s!ru%!ure be!)een upper ba!h-al 3200N1500 ,4 and !he o!he
0.?03, PT0.0014, bu! no! be!)een !he !)o deeper 6ones 3lo)er ba!h-al and ab-ssal4. Di..eren%es be!)een seep asse,bla&es a%ross de
lo)er ba!h-al4 )ere espe%iall- e(iden! be!)een ,i%robial ,a!s and %la, bed or a,phare!id bed %o,,uni!ies 3A8O#I9 * P 0,34, PT0.00
%o,,uni!ies a! .renula!e .ields )ere ,os! si,ilar !o !hose in %la, bed sedi,en!s, bu! )ere dissi,ilar !o !hose in o!her seep habi!a!s 3pT0
%o,,uni!ies a! or&ani% .alls )ere no! s!ri2in&l- di..eren! .ro, ea%h o!her a! !he .a,ille(el 3i&ures 3 and 44.
Figure 0. M1S plots o$ $amily+level abundance based on the 2ray Curtis similarity inde*.
Panels AN$: #Huares N ;pper ba!h-al 3;b 200N1500 ,4< $ir%les N "o)er ba!h-al 3"b 1501N3000 ,4< +rian&les / Ab-ssal 3AbI3000 ,
indi%a!e habi!a!s )i!hin si!es: "i&h! &reen / ,i%robial ,a!s 39a!4, Dar2 blue / %la, beds 3$b4, *ed / ho! ,uds 31,4, Oran&e / a%!i(e (e
ina%!i(e (en!in& 3I%4, 'ro)n / .renula!e beds 3P&4, ]ello) / a,phare!id beds 3A,ph4< 'la%2 / 'a%2&round sedi,en!s. Panel D: #-,bol
sa,ples 3in bla%24 in di..eren! basins 3si!es4.
doi:10.1371/journal.pone.0033515.&004
9ul!i(aria!e dispersion anal-sis based on â%%ardQs dissi,ilari!- inde0 indi%a!es s!ron& di..eren%es in ,a%ro.aunal be!a/di(ersi!- a,on& (e
.alls 3P7*9DI#P P 30,>, p P 0,0014. Pair/)ise %o,parisons indi%a!e s!ron& di..eren%es in be!a/di(ersi!- be!)ee
be!)een (en!s and seeps 3pT0.0014. +he (en! .auna e0hibi!ed !he )ides! he!ero&enei!- a,on& all si!es 355Y â%%ardQs dis!an%e4, )here
ho,o&eneous be!)een si!es 332Y on a(era&e4. +his ho,o&enei!- is li2el- a %onseHuen%e o. !he li,i!ed bio&eo&raphi% ran&e represen!ed
sa,ples.
W2
per,
, o! )) #%/#*/)#"+ )#:"#
#pe%ies di(ersi!-
*are.a%!ion anal-sis indi%a!ed a &eneral !rend o. ele(a!ed di(ersi!- a! a .e) seep and or&ani%/.all habi!a!s, )hereas (en! sedi,en!s in &e
3i&ure 54. A! a%!i(e and ina%!i(e (en! si!es in 9anus 'asin di(ersi!- )as lo) and si,ilar !o ho! ,ud sedi,en!s in 9iddle Kalle- 3
(en! sedi,en!s )ere .ound in %la, bed and ,i%robial ,a! habi!a!s 37s P 114. #eep habi!a!s e0hibi!ed a broad di(ersi!- ran&e 37s
o!her si!es, re.le%!in& hi&her (ariabili!- o. &eo%he,i%al %ondi!ions 3i&ure 54. renula!e .ields a! !he deeper ;ni,a2 and #an $le,en!e see
beds a! 7el *i(er seeps e0hibi!ed !he hi&hes! di(ersi!- o. all seep habi!a!s 37s P 27 .or bo!h habi!a!s< i&ure 54. +hese areas also !end
3^_ P 0.>7 and ^_ P 0.71N0.@5 .or %la, beds a! 7el *i(er and .renula!e .ields a! #an $le,en!e and ;ni,ar2, respe%!i(el-4. A se%ond %lus!e
Fin!er,edia!eG di(ersi!- (alues in%luded ,i%robial ,a! habi!a!s, or&ani%/.alls and o!her %la, bed and .renula!e .ields a! (arious si!es 3
)i!h lo)es! di(ersi!- )ere ,i%robial ,a!s a! !he lorida es%arp,en! and 7el *i(er, $A 37s P 7, and 7s15 P 4, respe%!i(el-4 and .renula
es%arp,en! 37s P 44. 1o)e(er, %o,,uni!- e(enness in lorida 7s%arp,en! .renula!e .ields )as ele(a!ed 3^_ P 0.@04, in %on!ras! !o !he h
pol-%hae!es in ,i%robial ,a!s a! !he sa,e si!e 3i&ure 34.
Figure 3. Rare$action diversity at species level $or vent -upper., seep -middle. and organic+$all -lo#er. habitats -cores pooled
$olors indi%a!e si!es< "ine pa!!erns di..eren!ia!e habi!a!s )i!hin si!es. "e&end: Mat N ,i%robial ,a!s, !b N %la, beds,
beds, "c N a%!i(e (en! sedi,en!s, #c N ina%!i(e (en! sedi,en!s, $m N (en! ho! ,uds, O. N or&ani%/.alls. #i!es: 9K N 9iddle Kalle-, 9'
7el *i(er, 1* N 1-dra!e *id&e, " N lorida 7s%arp,en!, VD N Vodia2 Alas2a, ;9 N ;ni,ar2 Aleu!ians, #$ N #an $le,en!e 'asin, 8
Velp/.all, 5d N 5ood/.all, 5h N 5hale/.all.
100
100
100
15
- o! )) #%/#*/)#"+ )#:"#
doi:10.1371/journal.pone.0033515.&005
8u!ri!ional sour%es
&ents.
#-,bion!/bearin& (en! !a0a, )hile (er- %o,,on on hard subs!ra!es, are !-pi%all- li,i!ed !o (esi%o,-id bi(al(es in h-dro!her,al sedi,en!s
e0%ep!ion< Siboglinum spp. is presen! in )ar, sedi,en!s o. 9iddle Kalle- D>2E and a! !he $hile +riple ûn%!ion 3+hurber e! al. unpublished
presen! in lo) .lo) (en!s a! 'rans.ield #!rai!, An!ar%!i%a D>3E. 5here s!udied, !he (en! in.auna e0hibi!s a ran&e o. nu!ri!ional sour%es depe
habi!a! 3+able 34. A! 9anus 'asin a%!i(e si!es, hea(- U $ si&na!ures o. ,os! in.auna 3W13 !o W1?`4 ,a- re.le%! relian%e on ,i%robes )i
+$A %-%le D27E. A,on& !he redu%in& en(iron,en!s %onsidered here, !his !rophi% pa!h)a- appears !o be uniHue !o h-dro!her,al (en!s. A!
si&na!ures 3W20 !o W2?`4 re.le%! a ,i0 o. pho!os-n!he!i%all- deri(ed or&ani% ,a!!er and sul.ide/o0idi6in& ,i%robes. In %on!ras!, in.auna in
appear !o rel- lar&el- on sul.ide/o0idi6in& ba%!eria, based on li&h!er U 8 (alues !han ba%2&round .auna and a(era&e U
%on!ribu!ions !o !he $ pool see, rare, bu! ha(e been obser(ed in !he ,aldanid icomache sp. and !apitella spp. .ro, 9iddle Kalle- and
+riple ûn%!ion 3+hurber a! al., unpublished4. e) in.aunal spe%ies )i!hin 9iddle Kalle- h-dro!her,al sedi,en!s appear !o rel- on pho!os-
sour%es. A! !he Lorda *id&e, orbiniids in !he %la, bed 3W40`4 and an apla%ophoran 3W37`4 in ba%!erial ,a!s in ho! sedi,en!s 3W41.?`
si&na!ures, bu! !his ,a- no! indi%a!e ,e!hane in%orpora!ion D>4E.
able /. Stable isotope signatures o$ sediment macro$auna $rom chemosynthetic sites and habitats.
doi:10.1371/journal.pone.0033515.!003
Seeps.
Al!hou&h ,e!hane seeps are .ueled b- ,e!hane, !he do,inan! .or, o. au!o!rophi% produ%!ion is based on !he resul!an! sul.ide apparen!l-
all !he si!es s!udied, onl- a subse! o. !he .auna ob!ains %arbon .ro, ,e!hane, -e! !he di(ersi!- o. !his &roup is surprisin&: a,phare!ids, %a
%u,a%eans, dor(illeids, &a,arids, lu,brinerids, nereidids, ,aldanids, !urbellarians, and ph-llodo%ids all ha(e iso!opi% si&na!ures !ha! indi%
,e!hane/deri(ed %arbon 3D?3E, D?>E, D>0E. +he e0!en! o. ,e!hane/deri(ed %arbon has been in(es!i&a!ed a! a ran&e o. seep si!es
Zealand seeps, !he ,a%ro.auna deri(ed ?N100Y o. !heir %arbon .ro, ,e!hane D?3E. 9a%ro.aunal !issues had up !o 55Y ,e!hane/deri(ed
es%arp,en! ,a!s, 20N44Y in Ore&on ,i%robial ,a!s, lorida, O*, $A and Vodia2, AV %la, beds, and Vodia2 po&onophoran .ields, and
beds and po&onophoran .ields and 7el *i(er, $A ,i%robial ,a! habi!a!s D?>E, D>0E. 9a%ro.auna .ro, seep si!es e0hibi! ,ore (ariable ran&
!han in !he o!her s-s!e,s 3+able 34 and !here is no s!ron& !rend in !he iso!opi% si&na!ures )i!h dep!h or bio&eo&raphi%
,ar&in, !he a(era&e iso!opi% si&na!ure o. seep ,a%ro.auna su&&es!s s!ron&er relian%e on ,e!hane/deri(ed %arbon as dep!h in%reases
seeps and in ,os! habi!a!s s!udied !here are a subs!an!ial nu,ber o. he!ero!rophi% or&anis,s u!ili6in& o!her non/%he,os-n!he!i% .ood sou
3i.e. be!)een habi!a!s )i!hin a si!e4, !he iso!opi% %o,posi!ion o. ,e!hane and !he ,e!hane .lu0 ra!es in.luen%e !he U
13
15
"# o! )) #%/#*/)#"+ )#:"#
he!ero!rophs.
'rganic $alls.
+he ,os! abundan! in(er!ebra!es %oloni6in& )hale/, 2elp/ and )ood/.all sedi,en!s do no! .eed e0%lusi(el- on or&ani% %arbon .ro, !he or&
)ood bio,ass4. Al!hou&h a hi&h propor!ion 3I50Y4 o. !he die! %an %o,e .ro, !he or&ani% islands D17E, D>5E, sedi,en! or&ani% %arbon and
!o !he die! o. !he oppor!unis! spe%ies. A! bo!h 2elp and )ood par%els !here is an inpu! o. %he,os-n!he!i% %arbon (ia %onsu,p!ion o. .ree/l
on sedi,en!s and possibl- o(er !he sur.a%e o. )ood and 2elp par%els. Dead bio,ass .ro, )hale .alls ,a- suppor! %he,os-n!hesis a! ea
3i.e. T1> ,on!hs4. +here.ore, he!ero!rophi% %onsu,p!ion o. %he,os-n!he!i% and o!her .ood sour%es produ%e a broad ran&e o. ,a%ro.auna
around or&ani% .alls 3+able 34. "o) U $ si&na!ures .ro, or&ani%/.all sedi,en! ,a%ro.auna are .ound in %u,a%eans and dor(ill
&eneral !hese si&na!ures are )i!hin !he broad spe%!ru, o. (alues .ound a! (en! and seep habi!a!s. In sulphidi% sedi,en!s a! )hale .alls, in
appears !o be do,ina!ed b- (esi%o,-id %la,s D32E, )hi%h rel- on sul.ide/based %he,oau!o!rophi% produ%!ion.
7nde,i%i!- and lin2s !o !he surroundin& deep sea
1-dro!her,al (en! sedi,en!s appear !o suppor! a ,i0 o. &enera or spe%ies a%2no)led&ed !o be (en!/seep/)hale/.all spe%ialis!s 3e.&.,
%epressigyra, $yalogyrina, Paralvinella, ereis sandersi&, bu! also !a0a broadl- presen! on %on!inen!al ,ar&ins around !he )orld 3
'phryotrocha4. Di..eren! sub habi!a!s ,a- suppor! &rea!er or lesser nu,bers o. (en!/ende,i% spe%ies D27E. 'e!)een Lua-,as and 9idd
he!ero!rophi% spe%ies are shared< an a,phare!id, hesionid and pol-noid pol-%hae!e D14E. A,on& s-,bion!/bearers li(in& in sedi,en!s, !he
barhami, (scarpia spicata, and !he %la, "rchivesica gigas, !alyptogena pac)ardana, and !* Pacifica .reHuen!l- o%%ur a! (en!s, seeps 3
D1?E, D32E, D>7E, D>>E
'ased on sa,plin& o. %old seep si!es in !he #ea o. O2ho!s2 be!)een 1?0 and 1?00 ,, #ahlin& e! al. 320034 D>@E %on%luded !ha! seep end
!o dep!hs belo) 370 ,. 5hile ,os! o. !he s-,bion!/bearin& in(er!ebra!es a! deep/)a!er seeps are seep/ 3or in so,e %ases (en!/4 ende,
seep/(en! ende,is, is si&ni.i%an!l- less a,on& !he he!ero!rophi% in.auna. +he ,os! sulphidi% sedi,en!s 3,i%robial ,a!s do,ina!ed b-
.reHuen!l- suppor! !he lar&es! nu,ber o. seep/ende,i% spe%ies. A! !he spe%ies le(el, "e(in e! al. .ound onl- abou! 50Y o. seep ,a%roin.a
and 7el *i(er, $A )ere seep ende,i%s, )i!h !he re,ainder presen! in nearb- ba!h-al slope sedi,en!s. 'ernardino a #,i!h 320104
spe%ies presen! near !ube)or, !hi%2e!s )ere also .ound a! nearb- )hale, )ood, and 2elp .alls. Al!hou&h in.aunal ,eio.auna are no! a .o%
al,os! no ,e!a6oan ,eio.aunal &enera or .ora,ini.eral &enera presen! a! seeps are %onsidered ende,i% !o %he,os-n!he!i% e%os-s!e,s
Or&ani%/.all sedi,en!s, in par!i%ular !hose around )hale .alls, appear !o hos! a nu,ber o. ende,i% dor(illeid spe%ies, al!hou&h ,an- o. !h
%olle%!ed a! )hale .alls are s!ill in !he pro%ess o. des%rip!ion. #o,e o. !he dor(illeid spe%ies a! )hale .alls 3in%ludin& spe%ies in !he &enera
and Schistomeringos4, %an o%%ur in abundan%e a! )ood .alls and seeps D17E, D32E, D@3E. 9os! do,inan! !a0a presen! a! !hese islands are
preda%ious pol-%hae!es as )ell as oppor!unis!i% %u,a%eans D17E.
1iscussion
$on%ep!ual .ra,e)or2 o. redu%in& sedi,en! ,a%ro.aunal di(ersi!-
Deep/sea %he,os-n!he!i% e%os-s!e,s hos! a (arie!- o. &eo%he,i%al and ,i%robial pro%esses !ha! ,edia!e or&ani% %arbon .i0a!ion, i,pos
o. s!resses reHuirin& ph-siolo&i%al adap!a!ions, and in.luen%e asso%ia!ions o. (arious ende,i% endos-,bion!/bearin& spe%ies, enri%h,en!
ba%2&round .auna. #edi,en!s in !hese %he,os-n!he!i% e%os-s!e,s usuall- share !he presen%e o. redu%ed inor&ani% %o,pounds, spe%i.i%
sul.ide, h-dro&en, or a %o,bina!ion o. !hese. 1i&h .lu0 ra!es o. redu%ed %he,i%als 3e.&. 1 #, $1 4 appear !o be a %o,,on .a%!or in.luen%
,a%ro.auna a! seeps, (en!s and a! so,e or&ani% .alls 3i&ure ?4. 5hile !hese redu%ed %he,i%als in pore)a!ers pro(ide a %ross/e%os-s!e
i,por!an! e..e%!s on !he bio!a, !he e%os-s!e,s %onsidered here di..er in addi!ional en(iron,en!al .a%!ors !ha! ,odi.- !he lo%al 3i.e. ,e!er s
,a%roben!hi% %o,,uni!ies. +here.ore, seep, (en! and or&ani%/.all sedi,en!s are hi&hl- he!ero&eneous )i!h respe%! !o !heir &eolo&i%al or
&eo%he,i%al and ,i%robial pro%esses, and 3!o so,e e0!en!4 !heir e(olu!ionar- his!ories< !he- .reHuen!l- e0hibi! a %o,ple0 ,osai% o. habi!a
spe%ialis! and ba%2&round .auna, )hi%h are in !urn in.luen%ed b- !her,al s!ress 3a! (en!s4, pa!%h d-na,i%s 3seeps and or&ani% .alls4 and b
D15E, D1?E.
13
2 4
"" o! )) #%/#*/)#"+ )#:"#
Figure 4. A conceptual $rame#or( o$ $actors shaping the biodiversity, density, and biomass o$ macro$auna in reducing ecos
+he !op !hree panels hi&hli&h! dri(ers !ha! are uniHue !o %er!ain s-s!e,s. +he bo!!o, !)o panels pro(ide a0es .or .ea!ures !ha! are si,
3no!e !ha! )hile (alues are &i(en .or !hese !)o a0es !he (alues are no! %onsis!en! a%ross !he di..eren! e%os-s!e,s represen!ed al!hou&
+he ,iddle panel illus!ra!es ho) !hese .a%!ors !ransla!e in!o %o,,uni!- a!!ribu!es o. ea%h o. !he e%os-s!e,s. +he bi.ur%a!ion in !he ab
.a%!ors indi%a!e !ha!, dependin& on !he s-s!e,, s!ress o(errides hi&h produ%!i(i!- in !hese habi!a!s and bo!h bio,ass and spe%ies ri%hn
in!er,edia!e le(el 3e.&. h-dro!her,al sedi,en!s )here !he !e,pera!ure s!ress o(errides !he i,por!an%e o. a hi&h produ%!i(i!- s-s!e,4
doi:10.1371/journal.pone.0033515.&00?
Our %o,parison o. seep, (en! and or&ani%/.all sedi,en!s su&&es!s !ha! .ood a(ailabili!- asso%ia!ed )i!h in%reased .lu0 o. redu%ed %he,i%
,a%ro.aunal densi!ies and bio,ass %o,pared !o deep/sea sedi,en!s a! si,ilar dep!hs. +his obser(a!ion &enerall- suppor!s our h-po!hes
ele(a!ed sul.ide %on%en!ra!ions )ill e0hibi! enhan%ed densi!-. +he abundan%e and %o,posi!ion o. !he sedi,en! ,a%ro.auna a! (en!s, seeps
rela!ed !o !he ra!es o. sul.ide or ,e!hane produ%!ion 3i.e. .luid .lo) and &eo%he,is!r-4, habi!a! 3i.e. based on do,inan! .ounda!ion spe%ies
3a! .ood/.alls4, and leads !o predi%!able !rends in ,a%ro.aunal %o,,uni!ies rela!i(e !o ba%2&round asse,bla&es 3i&ure ?
sele%!i(el- e0%lude non/!oleran! ba%2&round ,a%ro.auna .ro, ,os! %he,os-n!he!i% habi!a!s a! seeps, (en!s and or&ani% .alls. As !he le(e
or&ani% enri%h,en! in%rease )i!hin !he sedi,en!s, ,a%roin.aunal abundan%es !-pi%all- in%rease. In sedi,en!s nearb- or&ani% .alls, ,a%ro
%onsis!en!l- hi&her in sedi,en!s )i!h hi&h or&ani% enri%h,en! D1?E, D17E, )hi%h is in a%%ordan%e )i!h !he Pearson and *osenber& #A' ,o
densi!ies a! seep habi!a!s 3e.&. %la, beds, ,i%robial ,a!s and a,phare!ids beds4 are asso%ia!ed )i!h in%reased do,inan%e o. pol-%hae!
pa!!ern in (arious seep habi!a!s a! !he Lul. o. Luinea, 8ile Del!a, Lul. o. 9e0i%o and !he 9edi!erranean D25E, D@5E. 1o)e(er, ,a%ro.aunal
sedi,en!s a! seeps and (en!s ,a- be lo)er !han ba%2&round sedi,en!s as a resul! o. in%reased sul.ide .lu0 ra!es, de%reased sedi,en! s
!e,pera!ures D?3E.
9a%ro.aunal %o,posi!ion and di(ersi!- a! seeps, (en!s and or&ani% .alls are !i&h!l- asso%ia!ed )i!h !he sedi,en! &eo%he,is!r- 3e.&. le(els
%on!en!< i&ure ?4. 9an- o. !he %o,,on .a,ilies and &enera o. s-,bion!/bearin& and he!ero!rophi% !a0a %hara%!eris!i% o. !hese s-s!e,s
sulphidi% sedi,en!s. +he seep in.auna is a ,i0!ure o. ba%2&round, sul.ide/!oleran! and ende,i% spe%ies, and ,os! sulphidi% habi!a!s are d
3Dor(illeidae, 1esionidae, A,phare!idae4, &as!ropods and pera%arid %rus!a%eans. $api!ellid pol-%hae!es also appear !o !olera!e !hese inh
!he di(ersi!- )i!hin !he seep $api!ellidae is poorl- %ons!rained and reHuires .ur!her ,ole%ular anal-sis. #ur(i(al s!ra!e&ies .or so,e spe%ie
sedi,en!s re,ain eni&,a!i%, in%ludin& .or a ne)l- dis%o(ered spionid pol-%hae!e li(in& I10 %, do)n in !he sedi,en!s in ano0i% and hi&hl-
8e) Zealand D17E. Dor(illeid pol-%hae!es are e0!re,el- abundan! and di(erse a! or&ani% .alls in !he 87 Pa%i.i% D?1E
spe%ies o. dor(illeids in seep and )hale/.all sedi,en!s, respe%!i(el- D?2E, D@7E. 5hereas a di(ersi!- o. dor(illeid and %api!ellid pol-%hae!es
ph-siolo&i%al abili!- !o )i!hs!and hi&h sul.ide se!!in&s, o!her spe%ies ei!her o0-&ena!e !he sedi,en! !o redu%e %he,i%al s!ress or are res!ri
por!ion o. !he sedi,en! %olu,n. $la,s and sibo&linid pol-%hae!es bioirri&a!e !he sedi,en!, in%reasin& !he (er!i%al pene!ra!ion o. o0-&en
appear !o use an al!erna!e approa%h holdin& !heir bra%hia ou! o. !he seep sedi,en! )hile inhabi!in& (er!i%al !ubes, a,eliora!in& sul.ide s!re
,a- also o%%ur a! or&ani%/ri%h )hale .all sedi,en!s inhabi!ed b- !he a,phare!id +lyphanostomum sp. no(. D43E. A di(ersi!- o. .auna o%%u
") o! )) #%/#*/)#"+ )#:"#
redu%in& habi!a!s, in%ludin& ,an- &as!ropods and h-droids, )hi%h %an be nu,eri%all- do,inan! 3+able #1< i&ure 3
h-dro!her,al sedi,en!s4 and hesionids also are .reHuen!l- abundan! !a0a in !he ,os! sulphidi% sedi,en!s< and %u,a%eans, a,phipods, a
abundan! in %er!ain lo%a!ions. Ken! sedi,en!s )i!h hi&h !e,pera!ures harbor a (er- dis!in%! ,a%ro.auna rela!i(e !o seeps and or&ani% .alls
ins!an%es b- spionid pol-%hae!es 3&enus Prionospio 3Minuspio44, s-llids and orbiinid pol-%ha!es. 8u%ulanid bi(al(es 3
%o,,on in 9anus 'asin a%!i(e and ina%!i(e sedi,en!s, and in Lua-,as 'asin D27E.
Di(ersi!- is hi&hl- (ariable in ,an- seep habi!a!s and &enerall- lo)es! a! hi&h/!e,pera!ure sedi,en!s o. h-dro!her,al (en!s, )hi%h is %ons
!ha! s-s!e,s )i!h hi&h sulphidi% %on%en!ra!ions and/or hi&h !e,pera!ures )ill ha(e redu%ed di(ersi!-. 1-dro!her,al (en! sedi,en!s %o,,u
all o!her %he,os-n!he!i% e%os-s!e,s 3i&ure 54, su&&es!in& !ha! !e,pera!ure s!ress ,a- li,i! ,a%ro.aunal %oloni6a!ion. +his is sup
,i%robial ,a! and %la, bed sedi,en!s o. (en!s rela!i(e !o a%!i(e 3ho!4 and ina%!i(e sedi,en!s 3i&ure 5< D25E, D@7E,
habi!a!s )i!h lo)er ,a%ro.aunal do,inan%e !ha! are apparen!l- less sulphidi%< bu! !his pa!!ern )as no! uni(ersal. or e0a,ple, sibo&linid b
)ere hi&hl- di(erse bu! no! o.. lorida. +he sa,e pa!!ern is .ound in ,i%robial ,a!s alon& !he $ali.ornia ,ar&in 37* and O*4. +he he!ero&
%ondi!ions a! seep habi!a!s a! s%ales o. ,e!ers ,a- %ause subs!an!ial he!ero&enei!- in lo%al di(ersi!- in habi!a!s !ha! appear si,ilar (isual
+a0ono,i% and !rophi% si,ilari!ies
9ul!idi,ensional anal-ses re(eal !ha! (en!, seep and or&ani% .all ,a%ro.auna are dis!in%! 3i&ure 74. +he hi&hes! %o,,uni!- si,ilari!- )as
)ood and )hale .alls, )hi%h share ,an- do,inan! ,a%ro.aunal !a0a 3e.&., dor(illeid and a,phare!ids pol-%hae!es, %u,a%ean spe%ies4 )
are hi&h D27E, D100E< bu! !his si,ilari!- ,a- be e0plained in par! b- !he s,all bio&eo&raphi% ran&e represen!ed in our da!a se! 387 Pa%i.i%4
di..eren! ,a%ro.aunal %o,,uni!ies !han seeps and or&ani% .alls. +he (en! ,a%ro.auna responds !o lo%al/s%ale 3i.e. ,e!er4 pro%esses lin2e
also re.le%!s re&ional/s%ale isola!ion be!)een !he 5es!ern Pa%i.i% and 87 Pa%i.i% pro(in%es D1?E, D100E. +his spe%ies/le(el se&re&a!ion o.
,ar2ed %on!ras! !o !he hi&h &eneri% o(erlap o. do,inan! %he,os-,bio!i% ,e&a.auna !ha! is .ound in seeps, (en!s and )hale .alls
,a%ro.auna do no! sho) a s-s!e,a!i% response in !er,s o. spe%ies %o,posi!ion !o habi!a! he!ero&enei!- a! lo%al and re&ional s%ales, and
+here is a %lear separa!ion o. %la, bed and ,i%robial ,a!/asso%ia!ed ,a%ro.auna be!)een lo)er and upper ba!h-al si!es 3
.renula!e .ield ,a%ro.auna. +he 8e) Zealand a,phare!id beds appear !o hos! a dis!in%! upper ba!h-al .auna and ,a- %hara%!eri6e a ne)
se!!in&s D100E.
Figure 5. 1iagram sho#ing degree o$ community similarity or dissimilarity bet#een chemosynthetic ecosystems and habitat
Kalues ou!side bars deno!e a(era&e dissi,ilari!- be!)een si!es )i!h all habi!a!s %o,bined and !a0a responsible .or !hose di..eren%es.
indi%a!e !he lo)es! dissi,ilari!- be!)een !)o habi!a!s a,on& !he !)o si!es %o,pared. ,egend- Lreen %olor N indi%a!es dissi,ilari!- pe
#I9P7* anal-sis.
doi:10.1371/journal.pone.0033515.&007
Our s!ud- suppor!s dis!in%!ions o. (en!, seep and or&ani%/.all ,a%ro.aunal asse,bla&es a! broad s%ales 3b di(ersi!-4. +he (en! .auna e0h
he!ero&enei!- a,on& all si!es suppor!in& dis!in%! e(olu!ionar- ori&ins D15E, D1?E, D103E. 5hile sharin& so,e spe%ies, or&ani% .alls and seep
dis!in%! .aunas a! ba!h-al and ab-ssal dep!hs 3e.&., D>?E4. +here.ore, al!hou&h hi&h sulphidi% sedi,en!s usuall- lead !o ,a%ro.aunal %o,,
he!ero!rophi% and s-,bion!/bearin& spe%ies a! seeps, (en!s and or&ani% .alls, !here appears !o be li,i!ed o(erlap be!)een !hese e%os-s!
3i&ure 74. 9e&a.auna in %on!ras!, share 20Y o. spe%ies a! (en!s and seeps in %lose pro0i,i!- o.. âpan D104E.
9os! ,a%ro.aunal spe%ies 3and hen%e ,os! o. !he spe%ies ri%hness4 in (en!, seep and or&ani%/.all sedi,en!s are he!ero!rophi%, )i!h a li,
%he,oau!o!rophi% s-,bion!s 3e.&. sibo&linid pol-%hae!es, and (esi%o,-id and solenid bi(al(es4. +he %he,os-n!he!i% produ%!ion a(ailable
is ,os!l- deri(ed .ro, .ree/li(in& %he,oau!o!rophi% ,i%robes ra!her !han sin2in& de!ri!al or&ani% ,a!!er 3D?3E, D?>E,
"$ o! )) #%/#*/)#"+ )#:"#
be!)een (en!, seep and or&ani%/.all sedi,en!s resul! in )ide di..eren%es in or&ani% u!ili6a!ion 3i.e., .ood sour%es4 and in !he de&ree o. %he
9a%ro.auna .ro, seeps probabl- e0hibi! !he )ides! ran&e in iso!ope si&na!ures due !o !he inpu! o. iso!opi%all- li&h! ,e!hane, )hi%h pro(id
,i%robial produ%!ion a(ailable !o he!ero!rophi% .auna D15E, D27E, D?0E, D?3E. +he ,os! deple!ed U $ si&na!ures a! seeps %o,e .ro, ,i%rob
8e) Zealand a,phare!id beds, )hi%h are li2el- a resul! o. hi&h ra!es o. ar%haeal ,e!hane o0ida!ion and/or sul.ide .lu0
no! )ell do%u,en!ed a! )hale .alls, e(en !hou&h ,e!hane %on%en!ra!ions %an rea%h 2.@ ,9 a! )hale .alls D105E. Ken!s %an also sus!ain ,
deri(ed %arbon has been de!e%!ed in so,e (en! ,a%ro.auna 3,en!ioned abo(e4, bu! h-dro!her,al ,e!hane does no! ha(e a uniHue iso!op
di..i%ul! !o iden!i.- ,e!hano!roph- in (en! habi!a!s. In all o. !he redu%in& e%os-s!e,s, a broad ran&e o. ,a%ro.aunal iso!ope si&na!ures indi
%he,os-n!he!i% %arbon is in%ons!an! in !i,e or lo%all- and !ha! !here is addi!ional inpu! o. pho!os-n!he!i% .ood sour%es. +here is e(iden%e .
pho!os-n!he!i% %arbon !o shallo)er seep si!es a! !he $ali.ornia ,ar&in D@@E, D10?E. 8o! surprisin&l-, ,a%ro.auna .ro, or&ani% .alls e0hibi! a
si&na!ures %onsis!en! )i!h a (arie!- o. .ood resour%es a! !hese islands, )i!h !he do,inan! dor(illeid pol-%hae!es and %u,a%eans e0hibi!in&
%he,oau!o!rophi%all- based nu!ri!ion.
Dep!h !rends and 6ona!ion
I! is s!ill un%lear i. !he ,a%ro.auna e0hibi! dep!h 6ona!ion a%ross %he,os-n!he!i% sedi,en!s in !he deep sea. #!ron& dep!h 6ona!ion o. seep
do%u,en!ed in !he Lul. o. 9e0i%o D>@E, and in !he #ea o. O2ho!s2 D107E, bu! %o,parable s!udies ha(e no! been done .or ,os! in.auna. A
.a,il- Kesi%o,-idae, )hi%h o%%urs a! dep!hs .ro, 100 !o @,000 , bu! )i!h s!ron& dep!h 6ona!ion .or ,os! &enera
ba!h-,e!ri% 6one, se(en had ba!h-al dis!ribu!ions and !)o )ere ab-ssal D>?E. #e(eral .a,ilies o. o!her !a0a !ha! ha(e radia!ed in %he,os-
3A,phare!idae, Dor(illeidae, 1esionidae, Pol-noidae4 are no) subje%! !o ,ole%ular e(olu!ionar- s!udies. #o,e spe%ies .ound a! bo!h (en
pro0i,i!- ha(e been sho)n !o share haplo!-pes a%ross !hese e%os-s!e,s. In so,e %ases, !here are a..ini!ies 3a! spe%ies le(el4 )i!h shall
3e.&., Dor(illeidae D10>E4. A 2e- Hues!ion re,ainin& !o be addressed in(ol(es !he rela!i(e i,por!an%e o. %onne%!i(i!- 3e.&., &eo&raphi% isola
&eo%he,is!r- in de!er,inin& !he .aunal si,ilari!ies a%ross !he di..eren! redu%in& en(iron,en!s %onsidered here.
$on%ludin& re,ar2s
Deep/sea %he,os-n!he!i% sedi,en!s pro(ide a ,osai% o. habi!a!s !ha! o..er an e(olu!ionar- oppor!uni!- !o adap! !o e0!re,e, ener&-/ri%h
!ha! ha(e e0%luded ,u%h o. !he ba%2&round deep/sea .auna. Al!hou&h !he ,a%ro.aunal s!ru%!ure 3.a,ille(el4 o. (en!, seep and or&ani% .
%o,,onali!ies su%h as lo) di(ersi!- and hi&h do,inan%e o. a .e) pol-%hae!e !a0a, %o,,uni!-/le(el anal-ses re(eal s!ron& di..eren%es in
be!)een !hese e%os-s!e,s. +hese di..eren%es are li2el- !o resul! .ro, di..eren! re&i,es o. ph-siolo&i%al s!ress 3e.&., hi&h !e,pera!ures,
.ro, popula!ion and %o,,uni!-/le(el pro%esses in%ludin& preda!ion and .a%ili!a!ion, and .ro, poorl- 2no)n dep!h !rends, bio&eo&raphi% is
di(er&en%e. 'road/s%ale anal-sis su&&es! !ha! ,a%ro.aunal asse,bla&es in %he,os-n!he!i% sedi,en!s e0hibi! a lo) de&ree o. si,ilari!- a
s-s!e,s, ,a2in& !he, ,ore sus%ep!ible !o in%reasin& hu,an e0!ra%!i(e and disposal a%!i(i!ies 3re(ie)ed in D27E4.
Supporting In$ormation
13
+ablec#1.do%0
"+ o! )) #%/#*/)#"+ )#:"#
!.
Kie) Ar!i%le Pub9ed/8$'I Loo&le #%holar
).
/.
0.
3.
4.
able S!.
Summary o$ comparable #or( on macrobenthos community structure in bathyal hydrothermal vent sediments, cold seeps, #ha
+his !able in%ludes addi!ional si!es no! %i!ed in !he !e0!
doi:10.1371/journal.pone.0033515.s001
3DO$d4
Ac(no#ledgments
5e o..er spe%ial !han2s !o 9aria 'a2er, 7(a *a,ire6/"lodra, ]oshihiro uji)ara and Â9#+7$ .or or&ani6a!ion and suppor! o. !he 4!h $
O2ina)a. i&ure 1 )as ,ade b- Dr. 9aria 'a2er 38O$/;V4. +his is #O7#+ %on!ribu!ion nu,ber >5??.
Author Contributions
$on%ei(ed and desi&ned !he e0peri,en!s: "A" $*#. Per.or,ed !he e0peri,en!s: "A" A*+ $*#. Anal-6ed !he da!a: A' "A" A*+. $on!
/anal-sis !ools: A' "A" A*+ $*#. 5ro!e !he paper: A' "A" A*+ $*#.
Re$erences
#o,ero L8, $hildress ^^, Anderson A7 31@>@4 +ranspor!, ,e!abolis,, and de!o0i.i%a!ion o. h-dro&en sul.ide in ani,las .ro, sul.i
en(iron,en!s. $*$ $ri! *e( AHua! #%i 1: 5@1N?14.
'a&arinao + 31@@24 #ul.ide as an en(iron,en!al .a%!or and !o0i%an!: !olrran%e and adap!a!ion in aHua!i% or&anis,s. AHua!i% +o0i%o
#,i!h $*, De "eo $, 'ernardino A, #)ee!,an AV, Arbi6u P9 3200>4 Ab-ssal .ood li,i!a!ion, e%os-s!e, s!ru%!ure and %li,a!e
and e(olu!ion 23: 51>N52>.
Ler,an $*, *a,ire6/"lodra 7, 'a2er 9$, +-ler PA, $o,,i!!ee $## 320114 Deep/5a!er $he,os-n!he!i% 7%os-s!e, *esear%h
9arine "i.e De%ade and 'e-ond: A Proposed Deep/O%ean *oad 9ap. P"O# One ?: e2325@.
"e(in "A, #ibue! 9 320124 ;nders!andin& $on!inen!al 9ar&in 'iodi(ersi!-: A 8e) I,pera!i(e. Annual *e(ie) o. 9arine #%ien%e 4:
êssen L", Pan!oja #, Lu!ierre6 9A, euinones *A, Lon6ales **, e! al. 9e!hane in shallo) %old seeps a! 9o%ha Island o.. %en!r
*esear%h. 3in press4.
do#nload
"( o! )) #%/#*/)#"+ )#:"#
5.
6.
7.
!8.
!!.
!).
!/.
!0.
!3.
!4.
!5.
!6.
!7.
)8.
)!.
"i ", Luen6enne% ^, 8i%hols P, 1enr- P, ]ana&iba-ashi 9, e! al. 31@@@4 9i%robial di(ersi!- in 8an2ai +rou&h sedi,en!s a! a dep!h
O%eano&raph- 55: ?35N?42.
Ler,an $*, 'o)en A, $ole,an 9", 1oni& D", 1uber Â, e! al. 320104 Di(erse s!-les o. sub,arine (en!in& on !he ul!raslo) spre
P8A# 107: 14020N14025.
V(en(olden VA 31@@34 Las h-dra!es / &eolo&i%al perspe%!i(e and &lobal %han&e. *e( Leoph-s 31: 173N1>7.
#ibue! 9, Olu V 31@@>4 'io&eo&raph-, biodi(ersi!- and .luid dependen%e o. deep/sea %old/seep %o,,uni!ies a! a%!i(e and passi(
*esear%h II 45: 517N5?7.
+unni%li..e K, 9%Ar!hur AL, 9%1u&h D 31@@>4 A bio&eo&raphi%al perspe%!i(e o. !he deep/sea h-dro!her,al (en! .auna. Ad(an%es
353N442.
+unni%li..e K, ûniper #V, #ibue! 9 320034 *edu%in& en(iron,en!s o. !he deep/sea .loor. In: +-ler PA, edi!or. 7%os-s!e,s o. !he D
7lse(ier. pp. >1N110.
#,i!h $*, 9a-bau, 1", 'a%o/+a-lor A, Pope *1, $arpen!er #D, e! al. 31@@>4 #edi,en! %o,,uni!- s!ru%!ure around a )hale s2
8or!heas! Pa%i.i%: ,a%ro.aunal, ,i%robial and bio!urba!ion e..e%!s. Deep/#ea *esear%h II 45: 335N3?4.
ûniper #V, +unni%li..e K, #ou!h)ard 7$ 31@@24 1-dro!her,al (en!s in !urbidi!e sedi,en!s on a nor!heas! Pa%i.i% spreadin& %en!re
a! an O%ean Drillin& #i!e. $an ^ Zool 70: 17@2N1>0@.
"e(in "A 320054 7%olo&- o. %old seep sedi,en!s: in!era%!ions o. .auna )i!h .lo), %he,is!r- and ,i%robes. O%eano&raph- and 9a
*e(ie) 43: 1N4?.
#,i!h $*, 'a%o A* 320034 7%olo&- o. )hale .alls a! !he deep/sea .loor. O%eano&raph- and 9arine 'iolo&-: an Annual *e(ie) 41
'ernardino A, #,i!h $*, 'a%o A*, Al!a,ira I, #u,ida P]L 320104 9a%ro.aunal su%%ession in sedi,en!s around 2elp and )ood
and %o,,uni!- o(erlap )i!h o!her redu%in& habi!a!s. Deep/#ea *esear%h I 57: 70>N723.
Lrassle ^, 'ro)n/"e&er #, 9orse/Por!eous "#, Pe!re%%a *, 5illia,s I 31@>54 Deep/sea .auna o. sedi,en!s in !he (i%ini!- o. h-
#o% 5ash ?: 443N452.
#ahlin& 1, *i%2er! D, "ee *5, "in2e P, #uess 7 320024 9a%ro.aunal %o,,ui!- s!ru%!ure and sul.ide .lu0 a! &as h-dra!e deposi!s .
%on(er&en! ,ar&in, 87 Pa%i.i%. 9arine 7%olo&- Pro&ress #eries 231: 121N13>.
"e(in "A, 9endo6a L, Lon6ale6 ^P, +hurber A*, $ordes 77 320104 Di(ersi!- o. ba!h-al ,a%ro.auna on !he nor!heas!ern Pa%i.i%
,e!hane seeps and o0-&en ,ini,u, 6ones. 9arine 7%olo&- 31: @4N110.
Paull $V, 1e%2er ', $o,,eau *, ree,an/"-nde *P, 8eu,ann $, e! al. 31@>44 'iolo&i%al %o,,uni!ies a! !he lorida 7s%arp,en
(en! !a0a. #%ien%e 22?: @?5N@?7.
"* o! )) #%/#*/)#"+ )#:"#
)).
)/.
)0.
)3.
)4.
)5.
)6.
)7.
/8.
/!.
/).
//.
/0.
/3.
/4.
/5.
/6.
Krijenhoe2 *$ 320104 Lene!i%s and e(olu!ion o. deep/sea %he,os-n!he!i% ba%!eria and !heir in(er!ebra!e hos!s. In: Viel #, edi!or.
#prin&er #%ien%e. pp. 15N4@.
+araso( KL, Lebru2 AK, 9irono( A8, 9os2ale( "I 320054 Deep/sea and shallo)/)a!er h-dro!her,al (en! %o,,uni!i!es: !)o di..e
Leolo&- 224: 5N3@.
$ordes 77, $unha 9*, Lalfron ^, 9ora $, Olu/"e *o- V, e! al. 320104 +he in.luen%e o. &eolo&i%al, &eo%he,i%al, and bio&eni% ha
seep biodi(ersi!-. 9arine 7%olo&- 31: 51N?5.
9eno! ", Lalfron ^, Olu V, $aprais ^, $rassous P, e! al. 320104 #pa!ial he!ero&enei!- o. ,a%ro.aunal %o,,uni!ies in and near a &
deep Lul. o. Luinea. 9arine 7%olo&- 31: 7>N@3.
Do,a%2 7, Ish,an #, "e(en!er A, #-l(a #, 5ill,o!! K, e! al. 320054 A %he,o!rophi% e%os-s!e, .ound benea!h An!ar%!i% I%e #hel.
A,eri%an Leoph-si%al ;nion >?: 2?@N27?.
"e(in "A, 9endo6a L, Vono!%hi%2 +, "ee *5 3200@4 9a%roben!hos %o,,uni!- s!ru%!ure and !rophi% rela!ionships )i!hin a%!i(e a
h-dro!her,al sedi,en!s. Deep/#ea *esear%h II 5?: 1?32N1?4>.
#,i!h $*, 'a%o/+a-lor A*, Llo(er AL 320024 aunal su%%ession on repli%a!e deep/sea )hale .alls: !i,e s%ales and (en!/seep a.
9arine 43: 2@3N2@7.
#,i!h $*, 'ernardino A, 1annides AV, 'a%o A*, Al!a,ira ILeo%he,i%al and ,a%ro.aunal %o,,uni!- su%%ession in sedi,en!s a
)hale: a se(en/-ear s!ud-. 3in prep4.
1annides AV 3200>4 Or&ani% ,a!!er %-%lin& and nu!rien! d-na,i%s in ,arine sedi,en!s. 1onolulu: ;ni(ersi!- o. 1a)aii. 43@ p.
+reude +, #,i!h $*, 5en6ho.er , $arne- 7, 'ernardino A, e! al. 3200@4 'io&eo%he,i%al pro%esses a! a deep/sea )hale .all: ra
sul.ide e..lu0 and ,e!hano&enesis. 9arine 7%olo&- Pro&ress #eries 3>2: 1N21.
#,i!h $*, 'ernardino A, 1annides AV, 'a%o A*, Al!a,ira I 3in prep4 Leo%he,i%al and ,a%ro.aunal %o,,uni!- su%%ession in se
deep/sea )hale: a se(en/-ear s!ud-.
8a&anu,a +, 5ada 1, ujio2a V 31@@?4 'iolo&i%al %o,,uni!- and sedi,en! .a!!- a%ids asso%ia!ed )i!h !he deep/sea )hale s2ele
sea,oun!. ôurnal o. O%eano&raph- 52: 1N15.
Lo..redi #V, Paull $V, ul!on/'enne!! V, 1ur!ado "A, Krijenhoe2 *$ 320044 ;nusual ben!hi% .auna asso%ia!ed )i!h a )hale .all in
$ali.ornia. Deep/#ea *esear%h I 51: 12@5N130?.
uji)ara ], Va)a!o 9, ]a,a,o!o +, ]a,ana2a +, #a!o/O2oshi 5, e! al. 320074 +hree/-ear in(es!i&a!ions in!o sper, )hale/.all e
9arine 7%olo&- 2>: 21@N232.
1ulber! #9 31@714 +he non/%on%ep! o. spe%ies di(ersi!-: a %ri!iHue and al!erna!i(e para,e!ers. 7%olo&- 52: 577N5>?.
$lar2e V*, Lorle- *8 3200?4 P*I97* (?: ;ser 9anual/+u!orial. ? ed. Pl-,ou!h.
Anderso, 9^ 3200?4 Dis!an%e/based !es!s .or ho,o&enei!- o. ,ul!i(aria!e dispersions. 'io,e!ri%s ?2: 245N253.
"% o! )) #%/#*/)#"+ )#:"#
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Anderso, 9^, Lorle- *8, $lar2e V* 3200>4 P7*9A8OKAg .or P*I97*: Lu
s!a!is!i%al ,e!hods. Pl-,ou!h: P*I97*/7. 214 p.
Kan Do(er $" 320004 +he e%olo&- o. deep/sea h-dro!er,al (en!s. 8e) êrse-: Prin%e!on ;ni(ersi!- Press.
isher $* 31@@54 +o)ard an appre%ia!ion o. h-dro!her,al (en! ani,als: !heir en(iron,en!, ph-siolo&i%al e%olo&- and !issue s!able
1u,phris #7, Zierenber& *A, 9ullineau0 "#, +ho,son *7, edi!ors. #ea.loor h-dro!her,al s-s!e,s: A,eri%an Leoph-si%al ;nion
Lrassle ^, Pe!re%%a * 31@@44 #o.!/sedi,en! h-dro!her,al (en! %o,,uni!ies o. 7s%anaba +rou&h. In: Zierenber& *A, *eiss $A
h-dro!her,al, and biolo&i%al s!udies a! 7s%anaba +rou&h, Lorda *id&e, o..shore 8or!hern $ali.ornia: ;.#. Leolo&i%al #ur(e-. pp.
Pe!re%%a *, Lrassle ^ 31@@04 8o!es on .auna .ro, se(eral deep/sea h-dro!her,al (en! and %old seep so.!/sedi,en! %o,,uni!
edi!or. Lorda *id&e: a sea.loor spreadin& %en!er in !he ;ni!ed #!a!es 70%lusi(e 7%ono,i% Zone. 8e) ]or2: #prin&er Kerla&. pp. 2
$hildress ^^, isher $* 31@@24 +he biolo&- o. h-dro!er,al (en! ani,als: ph-siolo&-, bio%he,is!r- and au!o!rophi% s-,bioses. O%
'iolo&- an Annual *e(ie) 30: 337N441.
1er6i& P9, 1annin&!on 9D 320004 Inpu! .ro, !he deep: 1o! (en!s and %old seeps. In: #%hul6 1D, Zabel 9, edi!ors. 9arine Leo%h
Kerla&. pp. 3@>N41?.
$harlou ^", Don(al ^P, Dou(ille 7, êan/'ap!is!e P, *ad.ord/Vnoer- ^, e! al. 320004 $o,pared &eo%he,i%al si&na!ures and !he e(
337o50_84 and "u%2- #!ri2e 337o17_84 h-dro!her,al .luids, sou!h o. !he A6ores +riple ûn%!ion on !he 9id/A!lan!i% *id&e. $he,i%a
5elhan Â 31@>>4 Ori&ins o. ,e!hane in h-dro!her,al s-s!e,s. $he,i%al Leolo&- 71: 1>3N1@>.
#e-.ried 57, ous!ou2os DI, Allen D7 320044 ;l!ra,a.i%/hos!ed h-dro!her,al s-s!e,s a! ,id/o%ean rid&es: %he,i%al and ph-si%
and %arbon redu%!ion rea%!ions. In: Ler,an $*, "in ^, Parson "9, edi!ors. Leoph-s 9ono&r #er. pp. 2?7N2>4.
ôr&ensen '' 31@>24 9inerali6a!ion o. or&ani% ,a!!er in !he sea bed / !he role o. sulpha!e redu%!ion. 8a! *e( 9i%robiol 5: 770N7>
ôr&ensen '', 'an& 9, 'la%2burn +1 31@@04 Anaerobi% ,inerali6a!ion in ,arine sedi,en!s .ro, !he 'al!i% #ea/8or!h #ea !ransi!i
Pro&ress #eries 5@: 3@N54.
5eber A, ôr&ensen '' 320024 'a%!erial sul.a!e redu%!ion in h-dro!her,al sedi,en!s o. !he Lua-,as 'asin, Lul. o. $ali.ornia, 9
I 4@: >27N>41.
'eal 7^, 1ouse $1, Orphan K 3200@4 9an&anese/ and Iron/dependen! ,arine ,e!hane o0ida!ion. #%ien%e 325: 1>4N1>7.
Orphan K, 1ouse $1, 1inri%hs V, 9%Vee&an VD, Delon& 7 320024 9ul!iple ar%haeal &roups ,edia!e ,e!hane o0ida!ion in ano0i%
P8A# @@: 7??3N7??>.
'oe!ius A, *a(ens%hla& V, #%huber! $^, *i%2er! D, 5iddel , e! al. 320004 A ,arine ,i%robial %onsor!iu, apparen!l- ,edia!in& an
,e!hane. 8a!ure 407: ?23N?2?.
Orphan K, 1inri%hs V, ;ssler 5 , Paull $V, +a-lor "+, e! al. 320014 $o,para!i(e anal-sis o. ,e!hane/o0idi6in& ar%haea and sul.a!e
,arine sedi,en!s. Applied and 7n(iron,en!al 9i%robiolo&- ?7: 1@22N1@34.
", o! )) #%/#*/)#"+ )#:"#
34.
35.
36.
37.
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43.
44.
45.
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9urase ^, ren6el P 320074 A ,e!hane/dri(en ,i%robial .ood )eb in a )e!land ri%e soil. 7n(iron,en!al 9i%robiolo&- @: 3025N3034
Din& 1, Kalen!ine D" 3200>4 9e!hano!rophi% ba%!eria o%%up- ben!hi% ,i%robial ,a!s in shallo) ,arine h-dro%arbon seeps, $oal O
o. Leoph-si%al *esear%h 113: L01015.
Pearson A, #ee)ald ^#, 7&lin!on +I 320054 'a%!erial in%orpora!ion o. reli%! %arbon in !he h-dro!her,al en(iron,nen! o. Lua-,as
$os,o%hi,i%a A%!a ?@: 5477N54>?.
'oe!ius A, #uess 7 320044 1-dra!e *id&e: a na!ural labora!or- .or !he s!ud- o. ,i%robial li.e .ueled b- ,e!hane .ro, near/sur.a%e
Leolo&- 205: 2@1N310.
+r-on 9D, 'ro)n V9 320014 $o,ple0 .lo) pa!!erns !hrou&h 1-dra!e *id&e and !heir i,pa%! on seep bio!a. Leoph-si%al *esear%
"e(in "A, Ziebis 5, 9endo6a L, Lro)ne-/$annon K, +r-on 9D, e! al. 320034 #pa!ial he!ero&enei!- o. ,a%ro.auna a! nor!hern $
in.luen%e o. sul.ide %on%en!ra!ion and .luid .lo). 9arine 7%olo&- Pro&ress #eries 2?5: 123N13@.
Ziebis 5, 1aese ** 320054 In!era%!ions be!)een .luid .lo), &eo%he,is!r- and bio&eo%he,i%al pro%esses a! ,e!hane seeps. In: V
1aese **, edi!ors. 9a%ro and ,i%roor&anis,s in ,arine sedi,en!s: AL; 2?7N2@>:
+hurber A*, Vro&er V, 8eira $, 5i2lund 1, "e(in "A 320104 #!able iso!ope si&na!ures and ,e!hane use b- 8e) Zealand %old see
272: 2?0N2?@.
#o,,er #, "in2e P, P.ann2u%he O, +reude +, 8ie,ann 1 320104 $arbon .lo) !hrou&h a no(el seep habi!a! do,ina!ed b- dense b
pol-%hae!es. 9arine Leolo&- 272:
8aud!s ", Lreiner! ^, Poor! ^, 'el6a ^, Kan&a,pelaere 7, e! al. 320104 A%!i(e (en!in& si!es on !he &as/h-dra!e/bearin& 1i2uran&i 9
Di..usi(e/ (ersus bubble/released ,e!hane. 9arine Leolo&- 272:
$on)a- 89, Venni%ul! 9$ II, Kan Do(er $" 31@@44 #!able iso!opes in !he s!ud- o. ,arine %he,os-n!he!i%/based e%os-s!e,s. In
edi!ors. #!able Iso!opes in 7%olo&- and 7n(iron,en!al #%ien%e. O0.ord: 'la%2)ell. pp. 15>N1>?.
1u&ler 9, #ie(er! #9 320114 'e-ond !he %al(in $-%le: au!o!rophi% %arbon .i0a!ion in !he o%ean. Annual *e(ie) o. 9arine #%ien%e
"e(in "A, 9i%hener *1 320024 Iso!opi% e(iden%e .or %he,os-n!hesis/based nu!ri!ion o. ,a%roben!hos: !he li&h!ness o. bein& a! Pa
"i,nolo&- and O%eano&raph- 47: 133?N1345.
*i!! ', Pierre $, Lau!hier O, 5en6ho.er , 'oe!ius A, e! al. 320114 Di(ersi!- and dis!ribu!ion o. %old/seep .auna asso%ia!ed )i!h di
en(iron,en!al se!!in&s a! ,ud (ol%anoes and po%2,ar2s o. !he 8ile Deep/#ea an. 9arine 'iolo&- 15>: 11>7N1210.
Kanreusel A, De Lroo!e A, Lollner #, 'ri&h! 9 320104 7%olo&- and bio&eo&raph- o. .ree/li(in& ne,a!odes asso%ia!ed )i!h %he,o
!he deep sea: a re(ie). P"O# One 5: e1244@.
+hurber A* 320104 9i%robe/,e!a6oan in!era%!ions a! Pa%i.i% O%ean ,e!hane seeps. #an DIe&o: ;ni(ersi!- o. $ali.ornia.
"- o! )) #%/#*/)#"+ )#:"#
5).
5/.
50.
53.
54.
55.
56.
57.
68.
6!.
6).
6/.
60.
63.
64.
65.
66.
+hurber A*, "e(in "A, Orphan K^, 9arlo) Âr%haea in ,e!ha6oan die!s: I,pli%a!ions .or .ood )ebs and bio&eo%he,i%al %-%lin&.
#,i!h $* 3200?4 'i&&er is be!!er: +he roles o. )hales as de!ri!us in ,arine e%os-s!e,s. In: 7s!es ^, edi!or. 5hales, 5halin& and
$ali.ornia: ;ni(ersi!- o. $ali.ornia.
Lo..redi #V, 5ilpis6es2i *, "ee *5, Orphan K 3200>4 +e,poral e(olu!ion o. ,e!hane %-%lin& and ph-lo&ene!i% di(ersi!- o. ar%hae
deep/sea )hale/.all in 9on!ere- $an-on, $ali.ornia. I#97 2: 204N220.
8ishi,o!o A, 9i!o #, #hira-a,a ] 3200@4 Or&ani% %arbon and ni!ro&en sour%e o. sun2en )ood %o,,uni!ies on %on!inen!al shel(e
.ro, s!able iso!ope ra!ios. Deep/#ea *esear%h II 5?: 1?>3N1?>>.
Pala%ios $, Zbinden 9, Paillere! 9, Laill , "ebaron P 3200@4 1i&hl- si,ilar pro2ar-o!i% %o,,uni!ies o. sun2en )ood a! shallo) a
!he o%eans. 9i%robial 7%olo&- 5>: 737N752.
+urner *D 31@774 5ood, ,ollus2s, and deep/sea .ood %hains. 'ulle!in o. !he A,eri%an 9ala%olo&i%al ;nion. 1@7?. : 13N1@.
Dupon! ^, 9a&nin #, *ousseau , Zbinden 9, rebour& L, e! al. 3200@4 9ole%ular and ul!ras!ru%!ural %hara%!eri6a!ion o. !)o as%o
)ood o.. Kanua!u Islands in !he deep Pa%i.i% O%ean. 9-%olo&i%al *esear%h 113: 1351N13?4.
#,i!h $*, 1a,il!on #$ 31@>34 7piben!hi% ,e&a.auna o. a ba!h-al basin o.. sou!hern $ali.ornia: pa!!erns o. abundan%e, bio,ass a
*esear%h 30: @07N@2>.
"e(in "A, 9endo6a L 320074 $o,,uni!- s!ru%!ure and nu!ri!ion o. deep ,e!hane/seep ,a%roben!hos .ro, !he 8or!h Pa%i.i% 3Ale
o. 9e0i%o 3lorida 7s%arp,en!4. 9arine 7%olo&- 2>: 1N21.
#,i!h $*, 'ernardino A, 'a%o/+a-lor A*, +reude +, Al!a,ira I 3200@4 $he,os-n!he!i% %o,,uni!- de(elop,en! in sedi,en!s aro
bio&eo%he,is!r-, biodi(ersi!-, and persis!en%e !i,es. In: uji)ara ], edi!or. O2ina)a, âpan: 4@ p.
ûniper #V, ônasson I*, +unni%li..e K, #ou!h)ard A^ 31@@24 In.luen%e o. !ube buildin& pol-%hae!e on h-dro!her,al %hi,ne- ,iner
>@5N>@>.
#ahlin& 1, 5all,ann V, Dahl,ann A, #%h,aljohann *, Pe!ersen # 320054 +he ph-si%o%he,i%al habi!a! o. #%lerolinu, sp. a! 1oo2
'rans.ield #!rai!, An!ar%!i%a. "i,nolo&- and O%eano&raph- 50: 5@>N?0?.
Kan Do(er $", r- ' 31@@44 9i%roor&anis,s as .ood resour%es a! deep/sea h-dro!her,al (en!s. "i,nolo&- and O%eano&raph- 3
'ernardino A 3200@4 5hales, )ood and 2elp islands in !he deep/sea: e%olo&i%al su%%ession and spe%ies o(erlap )i!h o!her %he,
$ali.ornian %on!inen!al slope 387 Pa%i.i%4. #ao Paulo: ;ni(ersi!- o. #ao Paulo. 155 p.
5a!anabe 1, uji2ura V, Voji,a #, 9i-a6a2i ^, uji)ara ] 320104 âpan: Ken!s and seeps in %lose pro0i,i!-. In: Viel #, edi!or. +h
Aspe%!s .ro, 9i%robes !o 7%os-s!e,s: #prin&er. pp. 37@N401.
#,i!h $*, Vu2er! 1, 5hea!%ro.! *A, û,ars PA, De,in& ^5 31@>@4 Ken! .auna on )hale re,ains. 8a!ure 34: 127N12>.
'a%o A*, #,i!h $*, Pee2 A, *oderi%2 L, Krijenhoe2 *$ 31@@@4 +he ph-lo&ene!i% rela!ionships o. )hale/.all (esi%o,-id %la,s ba
D8A seHuen%es. 9arine 7%olo&- Pro&ress #eries 1>2: 137N147.
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67.
78.
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7).
7/.
70.
73.
74.
75.
76.
77.
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!8).
!8/.
#ahlin& 1, Lal2in #K, #al-u2 A, Lreiner! ^, oers!el 1, e! al. 320034 Dep!h/rela
e%olo&i%al si&ni.i%an%e o. %old/seep %o,,uni!ies / a %ase s!ud- .ro, !he #ea o. O2ho!s2. Deep/#ea *esear%h I 50: 13@1N140@.
'ernardino A, #,i!h $* 320104 $o,,uni!- s!ru%!ure o. in.aunal ,a%roben!hos around (es!i,en!i.eran !hi%2e!s a! !he #an $le,e
9arine 7%olo&- 31: ?0>N?21.
'ernhard ^9, 'u%2 V*, 'arr- ^P 320014 9on!ere- 'a- %old seep bio!a: Asse,bla&es, abundan%e and ul!ras!ru%!ure o. li(in& .ora
*esear%h I 4>: 2233N224@.
*a!hburn A7, Pere6 97, 9ar!in ^', Da- #A, 9ahn $, e! al. 320034 *ela!ionships be!)een !he dis!ribu!ion and s!able iso!opi% %o,
.ora,ni.era and %old seep bio&eo%he,is!r- in 9on!ere- 'a-, $ali.ornia. Leo%he,is!r-, Leoph-si%s, Leos-s!e,s 4:
5i2lund 1, Llo(er AL, ôhannessen P^, Dahl&ren +L 3200@4 $r-p!i% spe%ia!ion a! or&ani%/ri%h ,arine habi!a!s: a ne) ba%!eri(ore
and .ish .ar,s in !he 8or!h/7as! A!lan!i%. Zoolo&i%al ôurnal o. !he "innean #o%ie!- 155: 774N7>5.
Pearson +1, *osenber& * 31@7>4 9a%roben!hi% su%%ession in rela!ion !o or&ani% enri%h,en! and pollu!ion in !he ,arine en(iron,e
9arine 'iolo&- an Annual *e(ie) 1?: 22@N311.
*i!! ', #arra6in ^, $aprais ^, 8oel P, Lau!hier O, e! al. 320104 irs! insi&h!s in!o !he s!ru%!ure and en(iron,en!al se!!in& o. %old/se
9ar,ara #ea. Deep/#ea *esear%h I 57: 1120N113?.
5i2lund 1, Llo(er AL, Dahl&ren +L 3200@4 +hree ne) spe%ies o. 'phryotrocha 3Annelida: Dor(illeidae4 .ro,a )hale/.all in !he 8
222>: 43N5?.
Dando P*, #ou!h)ard A^, #ou!h)ard 7$, "a,on! P, 1ar(e- * 3200>4 In!era%!ions be!)een sedi,en! %he,is!r- and .renula!e po
!he nor!h/eas! A!lan!i%. Deep/#ea *esear%h I 55: @??N@@?.
"e(in "A, Da-!on PV 3200@4 7%olo&i%al !heor- and %on!inen!al ,ar&ins: )here shallo) ,ee!s deep. +rends in e%olo&- and e(olu!io
$ordes 77, 'e%2er 7", 1ourde6 #, isher $* 320104 In.luen%e o. .ounda!ion spe%ies, dep!h and lo%a!ion on di(ersi!- and %o,,u
9e0i%o lo)er/slope %old seeps. Deep/#ea *esear%h II 57: 1>70N1>>1.
Kan Do(er $", Ler,an $*, #peer VL, Parson "9, Krijenhoe2 *$ 320024 7(olu!ion and bio&eo&raph- o. deep/sea (en! and seep
2@5: 1253N1257.
$ordes 77, $arne- #", 1ourde6 #, $arne- *#, 'roo2s ^9, e! al. 320074 $old seeps o. !he deep Lul. o. 9e0i%o: %o,,uni!- s!ru
%o,parisons !o A!lan!i% eHua!orial bel! seep %o,,uni!ies. Deep/#ea *esear%h I 54: ?37N?53.
+hurber A*, "e(in "A, *o)den AA, #o,,er #,, "in2e P, e! al. 33in re(ision44 9i%robes, ,a%ro.auna and ,e!hane: a no(el, hi&h bi
.ueled b- aerobi% ,e!hano!roph-. P"O# One.
Llo(er AL, Loe!6e 7, Dahl&ren +L, #,i!h $* 320054 9orpholo&-, reprodu%!i(e biolo&- and &ene!i% s!ru%!ure o. !he )hale/.all an
spe%ialis! .athy)urila guaymasensis Pe!!ibone, 1@>@ 3Annelida: Pol-noidae4. 9arine 7%olo&- 2?: 223N234.
)" o! )) #%/#*/)#"+ )#:"#
!80.
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!84.
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r- ', #herr 7' 31@>44 d13$ ,easure,en!s as indi%a!ors o. %arbon .lo) in ,a
e%os-s!e,s. $on!ribu!ions !o 9arine #%ien%e 27: 15N47.
*eebur& 5# 320074 O%eani% 9e!hane 'io&eo%he,is!r-. $he,i%al *e(ie)s 107: 4>?N513.
"essard/Pilon #, Por!er 9D, $ordes 77, 9a%Donald I, isher $* 320104 $o,,uni!- %o,posi!ion and !e,poral %han&e a! deep L
Deep/#ea *esear%h II 57: 1>@1N1@03.
Vr-lo(a 79, #ahlin& 1 320104 Kesi%o,-idae 3'i(al(ia4: $urren! !a0ono,- and dis!ribu!ion. P"O# One 5:
+hornhill D^, #!ru%2 +1, 7bbe ', 9endo6a L, "e(in "A, e! al. 7(olu!ionar- his!or- o. %old ,e!hane seep dor(illeids 3Annelida4. 3in
"e(in "A, Ziebis 5, 9endo6a L, Lro)ne-/$annon K, 5al!her # 3200?4 *e%rui!,en! response o. ,e!hane/seep ,a%ro.auna !o s
in si!u e0peri,en!. ôurnal o. 70peri,en!al 9arine 'iolo&- and 7%olo&- 330: 132N150.
Kan Do(er $", Aharon P, 'ernhard ^9, $a-lor 7, Doerries 9, e! al. 320034 'la2e *id&e ,e!hane seeps: %hara%!eri6a!ion o. a so.
%he,os-n!he!i%all- based e%os-s!e,. Deep/#ea *esear%h 50: 2>1N300.
*obinson $A, 'ernhard ^9, "e(in "A, 9endo6a L, 'lan2s ^V 320044 #ur.i%ial h-dro%arbon seep in.auna .ro, !he 'la2e *id&e 3A
and !he Lul. o. 9e0i%o 3?@0N2240 ,4. 9arine 7%olo&- 25: 313N33?.
'er&Huis! D$, le%2ens!ein $, Vnisel ^, 'e&le- ', 9a%Donald I*, e! al. 320054 Karia!ions in seep ,ussel bed %o,,uni!ies alon& p
en(iron,en!al &radien!s. 9arine 7%olo&- Pro&ress #eries 2@3: @@N10>.
De%2er $, 9orineau0 9, Kan Lae(er #, $aprais ^, "i%h!s%hia& A, e! al. 1abi!a! he!ero&enei!- in.luen%es %old/seep ,a%ro.aunal %
a,on& seeps alon& !he 8or)e&ian ,ar&in. Par! 1: ,a%ro.aunal %o,,uni!- s!ru%!ure. 9arine 7%olo&-. 3in press4.
)) o! )) #%/#*/)#"+ )#:"#

PLOS ONE Comparative Composition, Diversity and Trophic Ecology of Sediment Macrofauna at Vents, Seeps and Organic Falls

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PLOS ONE Comparative Composition, Diversity and Trophic Ecology of Sediment Macrofauna at Vents, Seeps and Organic Falls

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Published: April 04, 2012 DOI: 10.1371/journal.pone.0033515 ea!ured in P"O# $olle%!

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