E ec s o mac oalgae in asi e species and empe a u e on es ua ine
sedimen s mic obial communi ies and ni ogen biogeochemis y
MARISA ALEXANDRA MONTEIRO BATISTA DOS SANTOS
DISSERTAÇÃO DE MESTRADO EM CIÊNCIAS DO MAR – RECURSOS MARINHOS
2014
ii
MARISA ALEXANDRA MONTEIRO BATISTA DOS SANTOS
E ec s o mac oalgae in asi e species and empe a u e on es ua ine
sedimen s mic obial communi ies and ni ogen biogeochemis y.
Disse ação de Candida u a ao g au de Mes e em
Ciências do Ma – Recu sos Ma inhos subme ida ao
Ins i u o de Ciências Biomédicas de Abel Salaza da Uni e sidade do Po o
O ien ado : Dou o a Ca a ina Ma ia Pin o Mo a Pin o de Magalhães
Co- O ien ado : Dou o F ancisco Pa a A enas
iii
Dedicado às duas pessoas que me ize am chega a é aqui,
Aos meus A ós
i
Ag adecimen os
Deixo um desmedido ob igado:
À minha o ien ado a, a D .ª Ca a ina Magalhães po e sido incansá el e es a semp e
disponí el a qualque ho a. Pela sua paciência nos meus a asos e pela con ínua
ap endizagem que me p opo cionou. Pelo ac o de se uma e e ência de p o issionalismo que
e ei em men e ao longo da minha jo nada p o issional. Cla amen e, es e abalho não se ia
possí el sem ela. Mui o Ob igada.
Ao meu co- o ien ado , o D . F ancisco A enas pela ansmissão dos seus conhecimen os de
es a ís ica e o necimen o de e amen as de abalho.
Ao di e o do Mes ado em Ciências do Ma – Recu sos Ma inhos, P o . Edua do Rocha, que
mos ou-se semp e disponí el pa a me auxilia nas a e as mais bu oc á icas.
Aos meus colegas do ECOBIOTEC pelo acolhimen o, pelos conselhos sábios, pela ajuda em
qualque ques ão labo a o ial e não só. P incipalmen e pela boa disposição que p opo ciona a
um ó imo ambien e de abalho.
Aos meus colegas de mes ado. Es amos odos no mesmo ba co e o am uma g ande ajuda
em odo o p ocesso, an o em e mos de in e ajuda no p ocesso da disse ação, mas po odos
os abalhos que ealizamos jun os e que con ibuí am pa a amadu ece conhecimen os. Pelos
momen os de desespe o e pelos momen os de es ejo que pa ilhamos.
À minha amília que es e e semp e lá, pa a enco aja , pa a chama a a enção, pela cons an e
p eocupação pa a que eu chegasse ao im de mais uma e apa. À minha mãe, aos meus ios e
aos meus p imos: Família não se escolhe, mas com es a eu não que ia mais nenhuma.
Aos meus amigos/as, o a po que são eles a amília que eu ac escen ei à minha ida. Ob igada
a odos po aze em pa e do meu dia- a- dia, po con ibuí em a cons ui a pessoa que eu
sou. Pelas con e sas, pelos conselhos, pelos momen os de descon ação e di e são, pelas
nossas noi es sag adas de dança e po es a em semp e comigo que seja ísica ou
espi i ualmen e.
Especialmen e à minha i mã, ao meu se semelhan e, à pessoa que es á mais p óxima de mim
desde que enho noção de mim. Po me e es azido a é aqui, pelo que passamos jun as que
é incon á el e imensu á el, po ac edi a es em mim mais do que ninguém e po se es uma
i mã simplesmen e enomenal, de o- e odas as minhas conquis as e mais es a.
Finalmen e, es e abalho oi inanciado po Fundos Nacionais a a és da FCT – Fundação
pa a a Ciência e a Tecnologia no âmbi o do p oje o, P ojec PTDC/AAC-AMB/102866/2008, e
o P oje o PTDC/AAC-AMB/113973/2009 bem como o PEs -C/MAR/LA0015/2013.

i
Resumo
É ge almen e acei e que os e ei os das mudanças climá icas e espécies in aso as podem e
impac o siné gico nos ecossis emas cos ei os, no en an o exis em poucas e idências
quan i a i as ace ca de como é que es as al e ações i ão modi ica a es u u a e unção das
comunidades na u ais. Nes e es udo in es igamos o e ei o in e a i o da decomposição de
mac oalgas exó icas/in aso as e da empe a u a no ciclo biogeoquímico do azo o em
sedimen os es ua inos e na es u u a das comunidades mic obianas ben ónicas. Foi mon ado
um conjun o de mic ocosmos com sedimen o es ua ino a im de se manipula a empe a u a
(15ºC e 20ºC) e a decomposição de mac oalgas exó icas/in aso as (G acila ia e miculophylla
and Sa gassum mu icum) e na i as (Ul a lac uca, Fucus esiculosus, Ascophyllum nodosum) e
a e a ma inha na i a Zos e a ma ina. Nes es a amen os o am es imados os luxos líquidos
de amónia (NH4+), ni a os (NO3-) e ni i os (NO2-) en e o sedimen o e a coluna de água, e
a aliadas as al e ações na es u u a e di e sidade bac e iana do sedimen o, a a és da
u ilização da écnica de ARISA, Au oma ed RNA In e genic Space . Foi u ilizada a análise de
a iâncias e o pa icionamen o de a iâncias pa a analisa o e ei o da empe a u a e a
p esença de algas in aso as/os nos luxos de N. Apenas o luxo líquido de NO3- demons ou
se signi ica i amen e a e ado pela O igem, is o é, na i a e sus in aso a. Os nossos
esul ados demons a am que a decomposição das algas es imulou as axas de e luxo de
NH4+, p o a elmen e causada pelo aumen o das axas de amoni icação. Além disso, os
esul ados e ela am um impac o signi ica i o da empe a u a nos p ocessos en ol idos na
eciclagem do azo o, is o que empe a u as ele adas p omo e am um aumen o de libe ação
de NO3- e NO2-, e logo uma maio disponibilidade des es nu ien es na coluna de água. Apesa
de não se e e i icado al e ações na es u u a das comunidades bac e ianas nos a amen os
a di e en es empe a u as e com mac oalgas e e as ma inhas na i as e in aso as, oco eu
uma seleção na comunidade mic obiana nos sis emas com Fucus esiculosus e Ascophyllum
nodosum (R: 0.34, ní el de signi icância: 1%). Es as duas mac oalgas pe encem à mesma
amília Fucaceae, ap esen ando semelhanças químicas e isiológicas que podem jus i ica a
seleção de g upos bac e ianos especializados na sua deg adação. Os esul ados suge em que
ele adas empe a u as podem causa um dec éscimo na e iciência dos p ocessos do ciclo do
azo o que são esponsá eis pela eciclagem des es compos os no ecossis ema; p omo endo
um possí el c escimen o descon olado de mac oalgas, conduzindo a uma dis unção dos
ecossis emas es ua inos.
ii
Abs ac
I is gene ally accep ed ha he e ec s o clima e change and in asi e species may
simul aneously impac coas al ecosys ems; howe e he e a e limi ed quan i a i e e idences
abou how i will modi y he s uc u e and unc ion o na u al communi ies. In his s udy we
in es iga ed he in e ac i e e ec o exo ic mac oalgae deg ada ion and empe a u e on
es ua ine sedimen s ni ogen biogeochemis y and on he s uc u e o ben hic mic obial
communi ies. One expe imen using mic ocosms wi h es ua ine sedimen s we e se up in o de
o examine he e ec s o empe a u e (15ºC and 20ºC) on he decomposi ion a es o in asi e
(G acila ia e miculophylla and Sa gassum mu icum) and na i e (Ul a lac uca, Fucus
esiculosus, Ascophyllum nodosum) and in he na i e seag ass Zos e a ma ina. In hose
ea men s changes in ino ganic ni ogen compounds we e e alua ed o e ime by measu ing
he ne luxes o NH4+, NO3- and NO2-, and he ARISA echnique was used o e alua e shi s on
sedimen mic obial composi ion. We used analysis o a iance and a iance pa i ioning
echniques o examine he e ec o empe a u e and he p esence o na i e s in asi e species
in N luxes. Only ne lux o NO3- was ound o be signi ican ly a ec ed by he o igin o he
mac oalgae/seag ass, i.e. na i e e sus in asi e. Ou esul s showed ha algae decomposi ion
inc eased a es o NH4+ e luxes p obably caused by a s imula ion o he amoni ica ion a es. In
addi ion, ou indings e ealed a signi ican impac o empe a u e on he p ocesses in ol ed on
ni ogen ecycling, since high empe a u es p omo ed an inc ease on he elease o NO3- and
NO2- o he wa e column. While, no changes in he mic obial communi ies we e obse ed
wi hin he di e en empe a u e and mac oalgae ype (na i e and in asi e) ea men s, a
mic obial communi y selec ion occu whe e Fucus esiculosus and Ascophyllum nodosum we e
p esen (Global R: 0.34, Signi icance le el: 1%). These wo mac oalgae belong o he amily
Fucaceae, p esen ing chemical and physiological simila i ies ha may explain hese
obse a ions. Ou esul s sugges ed ha high empe a u es may cause a dec ease on he
e iciency o he ni ogen cycle p ocesses ha a e esponsible o he abla ion o hese
compounds wi hin na u al impac sys ems, p omo ing a possible uncon olled g ow h o algae
and consequen ly a dys unc ion o he es ua ine ecosys ems.
.
iii
Table o Con en s
AGRADECIMENTOS .................................................................................................... IV
RESUMO ...................................................................................................................... VI
ABSTRACT ................................................................................................................. VII
LIST OF FIGURES......................................................................................................... X
LIST OF TABLES ........................................................................................................ XII
LIST OF PAPERS…………………………………………………………………….…......XIII
CHAPTER 1 ................................................................................................................... 1
1. In oduc ion ............................................................................................................................................... 1
1.1. Mac oalgae in asion .................................................................................................................... 1
1.1.1. Sa gassum mu icum .................................................................................................................... 2
1.1.2. G acila ia e miculophylla ............................................................................................................ 3
1.2. Aqua ic plan s decomposi ion ...................................................................................................... 3
1.3. Ma ine Ni ogen cycle .................................................................................................................. 5
1.4. Global wa ming consequences .................................................................................................... 7
1.5. Goals ............................................................................................................................................ 9
CHAPTER 2 ................................................................................................................... 9
2. Ma e ials and me hods ............................................................................................................................ 9
2.1. Si e desc ip ion and sample collec ion ......................................................................................... 9
2.2. Expe imen Se Up ..................................................................................................................... 10
2.3. Mac oalgae and Seag ass Ca bon and Ni ogen con en ......................................................... 12
2.4. Ino ganic Ni ogen De e mina ions ............................................................................................ 12
2.5. Ino ganic N in he in e s i ial wa e ............................................................................................. 14
2.6. Ne Ino ganic Ni ogen Fluxes ................................................................................................... 14
2.7. DNA ex ac ion and Au oma ed RNA In e genic Space Analysis (ARISA) ............................. 14
2.8. S a is ical analysis ...................................................................................................................... 15
CHAPTER 3 ................................................................................................................. 16
3. Resul s ..................................................................................................................................................... 16
ix
3.1. Mac oalgae and Seag ass Ca bon and Ni ogen Composi ion ................................................. 16
3.2. Biomass Deg ada ion ................................................................................................................. 18
3.3. NO3-, NO2- and NH4+ accumula ion in In e s i ial Wa e ............................................................. 19
3.4. Ne Fluxes o NO3-, NO2- and NH4+ ............................................................................................ 21
3.5. Bac e ial Di e si y ...................................................................................................................... 24
CHAPTER 4 ................................................................................................................. 25
4. DISCUSSION ........................................................................................................ 25
4.1. In luence on ino ganic N biogeochemis y ...................................................................................... 25
4.2. C: N Ra ios ................................................................................................................................. 28
4.3. Mac oalgae Decomposi ion ....................................................................................................... 28
4.4. E ec s on Bac e ial di e si y ...................................................................................................... 29
CHAPTER 5 ................................................................................................................. 30
5. Conclusion .............................................................................................................................................. 30
CHAPTER 6 ................................................................................................................. 31
6. Bibliog aphy ............................................................................................................................................ 31
2
accele a ion o he p ocesses in ol ed on seag ass decline in se e al na u al ecosys ems
(Ma ínez-Lüsche and Holme , 2010). The wo selec ed in asi e species o mac oalgae,
na i es om Asia ha ha e been in oduced in he No h o he Ibe ian Peninsula se e al
decades ago.
1.1.1. Sa gassum mu icum
Sa gassum mu icum is na i e o SE Asia (Yendo 1907), bu i s p esen dis ibu ion as an
in asi e species is widesp ead, including Eu ope, Medi e anean Sea and he wes coas o
No h Ame ica (B i on-Simmons 2004). In he Ibe ian Peninsula, i was i s eco ded in he 80s
bo h in he Basque P o ince and in he Galician coas (Pé ez-Ci e a 1989) eaching ecen ly
he sou he n coas o Spain (Be mejo e al. 2012). Some s udies suppo ha he success ul
coloniza ion o S. mu icum in No he n Spain is likely due o he la ge p oduc ion o emb yos
(A enas e al. 1995), i s as g ow h and la ge hallus size (>3 m). I also has a e y success ul
ep oduc i e s a egy by sel e iliza ion (Fle che 1975; No on 1976; No on 1977) and se e al
dispe sal mechanisms (including loa ing halli), which ha e u n his algae highly in asi e by
ou -compe e wi h na i e algal species and he o ganisms associa ed wi h hem (Buschbaum e
al. 2006). While s udies done on in e idal sho es ha e documen ed li le (Buschbaum e al.
2006; Ha ies e al. 2007;) o no impac o S. mu icum (De W eede 1983; De W eede and
Vande meulen 1988; ; Viejo 1997; Wilson 2001; Sanchez and Fe nandez 2005), s udies in
sub idal habi a s ha e indica ed ela i ely s ong impac s (Amb ose and Nelson 1982; S aeh e
al. 2000; B i on-Simmons 2004). Indeed, compe i ion wi h S. mu icum educed he abundance
o na i e canopy algae by app oxima ely 75% and na i e unde s o y algae by abou 50% on
San Juan Island; changed he ela i e abundance o he wo mos common na i e kelp species,
Lamina ia bonga diana and Aga um imb ia um. L. bonga diana (B i on-Simmons 2004). The
in asion o Sa gassum mu icum in Lim jo den, a shallow Danish es ua y, was ound o a ec
he local algal communi y h ough compe i ion wi h membe s o he hick lea he y and coa sely
b anched algae (S aeh e al. 2000).
Al hough, Cacabelos e al. (2013) highligh ed ha he a ia ion in S. mu icum in asion was
ound o occu a small-scale sugges ing a majo ole o di e se local d i e s in he in asion
p ocess. En i onmen al ac o s ac ing a la ge and/o meso-scales, such as seawa e and ai
empe a u e, a iabili y in hyd odynamic condi ions o opog aphy, wa e exposu e and
sedimen ion a es (Ince a e al. 2009; Olaba ia e al. 2009) a e key ac o s d i ing i s
ep oduc i e pa e ns and dispe sal mechanisms (Ince a e al. 2011).
In he p ocess o a success ul in asion and se lemen ecen indings ha e poin ed ou ha he
na u al di e si y o unc ional g oups (enc us ing, u , sub canopy, and canopy species) in a

3
ce ain ecosys em is mo e decisi e han he species ichness in de e mining he esis ance o
ma ine mac oalgal assemblages agains in asion (A enas e al. 2006).
1.1.2. G acila ia e miculophylla
G acila ia e miculophylla is o pa icula in e es because is o igina ed om he no heas
Paci ic bu has been acciden ally in oduced o bo h he Eas and Wes A lan ic whe e i can
o m la ge mono-speci ic d i ma s in low-ene gy shallow es ua ies (Thomsen. e al 2006;
Thomsen and McGla he y, 2006b). Algal ma s o his specie can also o m physical ba ie s o
se ling la ae, dec ease ligh in ensi y, inc ease he likelihood o anoxia and change wa e
mo emen pa e ns, which in u n a ec s sedimen a ion a es and hus ood a ailabili y o
deposi eede s (Nybe g 2009).
The in asion by hese algae has been demons a ed o ha e nega i e e ec s on na i e
seag ass beds o Zos e a ma ina by dec easing ne lea pho osyn hesis and su i al a es
(Ma ínez-Lüsche and Holme 2010a). Nega i e e ec s on seag ass a e e en g ea e a highe
empe a u es, sugges ing ha impac s could inc ease wi h u u e ocean wa ming (Ma ínez-
Lüsche and Holme 2010a). In some a eas such as Hog Island Bay in Vi ginia, G.
e miculophylla domina e algal assemblages, in all seasons and ele a ion le els (Thomsen and
McGla he y, 2006a). G acila ia e miculophylla is s ill in an ea ly in asion phase bu is likely o
in ade p o ec ed es ua ies cha ac e ized by abundan seag ass beds as seen o G acila iopsis
ande sonii in Cali o nian seag ass beds (BE 2008).
Addi ionally, he wa e ad ec ion, accumula ion and decomposi ion o G. e miculophylla a e
likely o ha e impo an implica ions in nu ien cycling p ocesses and ophic dynamics in he
Sepa ina al e ni lo a domina ed low ma sh (Thomsen e al. 2009).
1.2. Aqua ic plan s decomposi ion
Deposi ion o o ganic ma e in hese en i onmen s can esul om episodic e en s such as he
apid sedimen a ion o phy oplank on o ben hic mac oalgal blooms, o , in sys ems whe e
oo ed mac ophy es a e dominan and deposi ion o dead plan ma e ial can occu h oughou
he yea .
The a i al o de i al in asi e seaweeds o new ecosys ems ha can appea mixed o na i e
species o in isola ion will ul ima ely al e he ca bon and ni ogen p o ision and consequen ly
modi y bo h ben hic communi y s uc u e and ca bon o ni ogen cycling (Rossi e al. 2011).
Unde s anding he decomposi ion o aqua ic plan s allows o he de e mina ion o hei ole in
p o iding o ganic ma e o de i al ood chains, o al e na i ely being a sou ce o egene a ed
ino ganic nu ien s o au o ophic assimila ion (Twilley e al. 1986). In in e idal sedimen s,
4
bu ial and decomposi ion o mac oalgae de i us can uel he sedimen o ca bon (C) and
ni ogen (N), which can be ei he p omp ly mine alized o assimila ed o en e in he ood web
(Rossi 2007). De ached seaweeds o en deposi as de i us on he subs a um o ma ine
in e idal zone whe e hey can be locally bu ied by sedimen ewo king and s a decomposing
(Fo d e al.1999; Kelahe and Le in on, 2003; Rossi 2007). When bu ied hey can ep esen a
ele an supply o o ganic ma e o he ben hos (Rossi 2006). The bac e ial espi a ion can
inc ease a highe le els o o ganic ma e (Fon aine e al. 2004). Howe e , he quan i y, quali y
and spa ial dis ibu ion o he deposi ed o ganic ma e in he sedimen egula e he a es o
ben hic nu ien egene a ion. Fo example, in mac oalgal domina ed sedimen , mine aliza ion
can be accele a ed in ela ion o sys ems domina ed by ascula plan s, because mac oalgae
ha e li le s uc u al ma e ial and decompose apidly (Enoksson 1993; Dua e 1995). Howe e ,
he high mac oalgal equi emen s o dissol ed ino ganic ni ogen in luences he lux o
dissol ed ino ganic ni ogen be ween sedimen and o e lying wa e , and hus he dissol ed
ino ganic ni ogen p oduced will supply he mac oalgal N equi emen s (T imme e al. 2000). In
ac , a la ge pe cen age o he NH4+ p oduced du ing mine aliza ion (40 o 60%) o o ganic
ni ogen in sedimen s can also be los om he ecosys ems as N2; essen ially he NH4+
p oduced in he sedimen s is ni i ied and subsequen ly deni i ied (Sei zinge 1990; Rossi
2007).
The accumula ion o excess nu ien s in o he sys em esul ed om massi e decomposi ion
caused by episodic e en s such as he apid sedimen a ion o mac oalgal blooms, will lead o
eu ophica ion wi h a consequen deple ion o dissol ed oxygen (hypoxia and anoxia),
esponsible o he loss o impo an habi a such as seag ass beds and co als, changes in
ma ine biodi e si y and dis ibu ion o species (wi h impac s on comme cial ishe ies), and
associa ed die-o s o ma ine li e (Howa h 2000).
Some s udies ha e demons a ed ha mac oalgae deg ade as e han seag asses and highe
plan s (likely due o hei highe N-con en ), eleasing bo h ino ganic nu ien s and o ganic N
(Williams 1984; Buchsbaum e al. 1991; Bou guès e al. 1996). Fas -g owing plan s end o
ha e high nu ien concen a ions (Chapin e al. 1987), and also decompose as because o
he adequacy o hei li e as subs a e o mic obial g ow h (En iquez e al. 1993). Di ec
compa isons o lea decomposi ion, on ee lea es and mac ophy es in lakes, s eams, and
we lands showed ha in cases o nu ien -poo e sus nu ien - ich sys ems ha e indica ed
as e b eakdown in nu ien - ich sys ems and highe empe a u es (B ock e al. 1985; Webs e
and Ben ield 1986;). Ne e heless, each algal species has di e en cha ac e is ics ha will
a ec he a e o i s decomposi ion depending on he biochemical and mo phological
composi ion. The e o e, decomposi ion o algae p o ides a po en ially impo an supply o
5
o ganic and ino ganic compounds o he wa e column whe e hey can be ecycled apidly
(Gab ielson e al. 1983; Twilley e al. 1986; Paalme e al. 2002)
Tempe a u e is ega ded as one o he key ac o s esponsible o con olling decomposi ion
pa hways (Paalme e al. 2002). Thus, i is expec ed ha lowe empe a u es (e.g. 15°C)
s ongly decele a e decomposi ion o all mac ophy e species (Paalme e al. 2002). Howe e , as
he empe a u e inc eases owa ds 30°C a endency o apid deg ada ion o algal popula ions
is documen ed, wi h ega ds o biomass loss (Hanisak 1993; Paalme e al. 2002;). The
decomposi ion p ocess is ini ia ed wi h an enzyma ic b eakdown o cellula cons i uen s, such
as cell walls, which ul ima ely inc eases i s suscep ibili y o bac e ial ac i i y (Gab ielson e al.
1983). As a esul , in mac oalgae deg ada ion expe imen s, i is impo an o use li ing algal
ma e ial, wi h in ac cell walls, as his ensu es g ea e accu acy when de e mining he ‘ac ual’
ex en o ino ganic nu ien elease (Gab ielson e al. 1983; Paalme e al. 2002;).
1.3. Ma ine Ni ogen cycle
Nu ien a ailabili y is one o he key ac o s egula ing he main physiological esponses o
seaweeds, wi h ni ogen (N) being he mos likely o limi hei g ow h in empe a e wa e s
(DeBoe e al. 1978; Lobban and Ha ison, 1994;). Ni ogen is he mos abundan chemical on
Ea h’s a mosphe e bu i can only be used by N2- ixing specialized mic oo ganisms, which
ha e he abili y o educe i o ammonium and in eg a e i in o biomass. The o he p oka yo es
and all euka yo es can only use ixed ni ogen in he o m o ni a e, ammonium o o ganic
ni ogen, which ep esen s less han 0.1% o he o al N in ea h (Thamd up 2012). The gene al
una ailabili y o N2 o ma ine o ganisms makes he con e sion o N2 o o ganic ni ogen (N-
ixa ion), and he con e sion o ixed ni ogen (NO3-) o N2 (deni i ica ion), pa icula impo an
p ocesses in con olling he N a ailabili y in na u al ecosys ems (Capone e al. 2008).
Biogeochemical cycling o ino ganic ni ogen in ma ine en i onmen s has ecei ed much
a en ion o e he las se e al decades, mos ly because o p oblems associa ed wi h excess
ni ogen loadings, being a main conce n eu ophica ion o aqua ic sys ems (G ube and
Galloway 2008). Indeed a i icial N inpu s due o indus ial e ilize p oduc ion (140 TgNyea −1)
exceed na u al N sou ces (110 TgNyea −1) (Can ield e al. 2010). In his way, human ac i i ies
ha e shi ed he balance be ween N2 ixa ion and i s complex ecycling p ocesses o he
ex eme (Thamd up 2012). Because ni ogen is equi ed by all plan s, animals, and
mic oo ganisms, changes in he luxes o his elemen can al e he a es o basic p ocesses. To
unde s and he consequences o his ins abili y a de ailed unde s anding on how ni ogen in
cycling o e he di e en ecosys ems is equi ed. Howe e , while he e is a wo ldwide ma ine
li e a u e a ailable o mos ni ogen biogeochemical ans o ma ions and on he
6
mic oo ganisms in ol ed (Zum 1997; Valiela 1997; Jickells 1998; Sei zinge and Ha ison
2006; P osse and Nicol 2008; ) ou unde s anding o how N is cycled on Ea h has changed
g ea ly in he las ew yea s. Fi s by he disco e y o anae obic ammonium oxida ion in na u al
ecosys ems (Thamd up 2012) and secondly by he demons a ion o ae obic ammonia
oxida ion wi hin he domain A chaea (T eusch e al. 2005; Könneke e al. 2005;).
The complexi y o he ni ogen cycle is demons a ed in Figu e 1, which shows ha ni ogenous
compounds unde go a se ies o oxida ion/ educ ion eac ions media ed by a me abolically
di e se ange o au o ophic and he e o ophic o ganisms. These biogeochemical con e sions
a e ei he ene gy-yielding (e.g. ni i ica ion and deni i ica ion) o ene gy-demanding (e.g.
ni ogen ixa ion) and a e undamen al p ocesses in mic obial biosyn hesis and bioene ge ics
(Madigan e al. 2004).
The e a e wo dissimila o y mic obial p ocesses ha con ey he ecycling o ammonium, as
gene a ed by he decomposi ion o o ganic N (ammoni ica ion): (1) ni i ica ion, he ae obic
oxida ion o ammonium (NH4+) o ni i e (NO2-) and ni a e (NO3-), wi h each s ep pe o med by a
specialized g oup o p oka yo es, and (2) deni i ica ion, he espi a o y educ ion o ni a e
Figu e 1- Schema ic ep esen a ion o he ni ogen cycle. Me abolic ans o ma ions a e
shown as hick a ows. I shows he classical p ocesses o assimila ion (g een) and
dissimila ion (g ay) as well as ecen ly disco e ed pa hways (colo ed). Ae obic and
anae obic p ocesses a e sepa a ed, and dashed e ical a ows indica e exchange o
anspo be ween oxic and anoxic en i onmen s, wi h he ela i e size o a owheads
indica ing he dominan di ec ion o anspo . Abb e ia ion: DNRA, dissimila o y ni a e
educ ion o ammonium (Thamd up 2012).
7
(NO3) and ni i e (NO2-) educ ions o ni ic oxide (NO), ni ous oxide (N2O) and N2 (Thamd up
2012). One o he eac ions ha link he ni ogen and he ca bon cycle is pe o med by he
au o ophic ni i ying bac e ia, which use some o he elec ons om oxida ion o ammonium
and ni i e o educe CO2 and c ea e biomass. The second mechanism o educing ni a e
in ol es ni a e- educing bac e ia ha media e a p ocess e med dissimila o y ni a e educ ion
o ammonium (DNRA). In con as o deni i ica ion whe e ni ogen is los om he ecosys em,
DNRA esul s in he conse a ion o ixed ni ogen wi hin he sys em (Magalhães 2005).
All mic obial media ed N ans o ma ions a e s ongly egula ed by he p e ailing en i onmen al
physico-chemical condi ions. Thus, en i onmen al speci ici ies o each ma ine ecosys em can
a ec he complex in e ac ions o he se e al ecycling ni ogen pa hways, and he signi icance
o he N p ocesses can a y acco ding o he speci ic cha ac e is ics and an h opogenic
p essu es o each habi a (Lobban and Ha ison, 1994). In nu ien en iched aqua ic sys ems,
blooms o mac oalgae a e ollowed by dys ophic e en s du ing which he bloom c ashes
eleasing la ge amoun s o pa icula e and dissol ed o ganic ma e , dissol ed ino ganic
ni ogen (DIN) and dissol ed o ganic ni ogen (DON) (Tyle e al. 2001; Sundbäck e al. 2003).
Respi a ion o he o ganic ma e , eleased du ing mic o- and mac oalgal senescence, o en
esul s in se e e oxygen deple ion (hypoxia) in bo h sedimen s and he wa e column. The shi
o hypoxia o anae obic condi ions acili a es ixed ni ogen emo al om he en i onmen ia
deni i ica ion (Figu e 1; Sei zinge 1988; Ogil ie e al. 1997; Sei zinge 2000).
1.4. Global wa ming consequences
Global wa ming has been inc eased along he decades, especially because o human ac i i ies
ha inc eased he emissions o ca bon dioxide, me hane and ni ous oxide and oxic
compounds. This emissions gene a ed an inc ease o 0.6ºC (0.4ºC-0.8ºC) global mean su ace
empe a u e o e he las 100 yea s (Gi ay 2002) and om 1901 o 2013, empe a u es ose a
an a e age a e o 0.13°F pe decade (Sp ing 2001) (Figu e 2).

8
This issue ook g ea ele ance because o he social economical and en i onmen al p oblems
al eady caused and p edic ed in he nea u u e, including loss o seag ass beds, mac oalgal
beds, and changes in co al ee s (Howa h e al. 2000). Al hough mos eac i e ni ogen is
e en ually deni i ied o N2 wi hin he coas al ecosys ems and associa ed shel , eac i e
ni ogen pollu ion has signi ican and widesp ead impac s on a ious ecosys ems and in human
heal h (Galloway e al. 2003).
A ele an ac is he in e ac ion o ni ogen wi h o he biogeochemical cycles, like he ca bon
cycle ha has pa icula ele ance, because o he cen al ole o a mosphe ic CO2 in
con olling clima e (Sa mien o and G ube , 2002) and wi h ni ogen ha ing a c ucial ole in
con olling key aspec s o his cycle (G ube and Galloway, 2008). As a esul o he bu ning o
ossil uels and ca bon emissions om land-use change, a mosphe ic CO2 has inc eased o
le els ha a e mo e han 30% abo e hose o p e-indus ial imes (G ube and Galloway,
2008).
These biogeochemical cycles a e linked o each o he and he p ocess consis s on he
e iciency o he a mosphe e in sp eading he ni ogen oxides and ammonia emi ed as a esul
o ene gy and ood p oduc ion and he deposi ion o ni ogen in he g ound ha is al eady
a ailable o plan s, allowing he p oduc ion and imp o ing he up ake o CO2 om he
Figu e 2 - High empe a u es a e accompanied by high concen a ions o CO2, and
his inc eased became clea ly e iden since he 80s and con inues o he p esen
days (EPA 2014)
9
a mosphe e. The global oceans, eshly p oduced algae in he ocean su ace ypically ha e a
ca bon o ni ogen a io o abou 4 o 10 (Meye s 1994).
1.5. Goals
In his s udy we in es iga ed he in e ac i e e ec o exo ic mac oalgae deg ada ion and
empe a u e on ben hic ino ganic ni ogen luxes (ammonia, ni a e and ni i e) and on he
di e si y o ben hic mic obial communi ies.
In his s udy we hypo hesized ha empe a u e is a key ac o in con olling a es o mac oalgae
and seag ass decomposi ion wi h a di ec impac on N ino ganic lux dynamics and ha
di e ences be ween indigenous (Ascoplyllum nodosum, Fucus esiculosus, Ul a lac uca,
Zos e a ma ina) and non indigenous species (G acila ia e miculophylla and Sa gassum
mu icum) will a ec a es o N ecycling.
CHAPTER 2
2. Ma e ials and me hods
2.1. Si e desc ip ion and sample collec ion
Sampling p og am was conduc ed in he Ria de Vigo si ua ed in he no heas Ibe ian
Peninsula, in he p o ince o Pon e ed a (Galiza). Ria de Vigo has 35 km leng h and i s la ge
ba hyme y is eached in A cade. Ex ends i sel om sou hwes o no heas p o ec ed in he
en y by Islas Cíes, d aining in he A lan ic Ocean (Figu e 3). The a e aged alues o su ace
empe a u e anged be ween 13ºC, om Janua y o ea ly May, and 18ºC, du ing July and
Augus (Noguei a e al. 1997). The No h Eas A lan ic Cen al Wa e (NEACW) is
cha ac e ized by an almos linea ela ionship be ween salini y and empe a u e, wi h salini ies
anging om 36.0 o 35.6 and empe a u es om 15 o 11 º C, a 50-75m and 400 m dep h,
espec i ely (González-Ga cés San iso e al. 2011). Salini y su ace wa e s ange om 35.5 o
35.7, showing an homogeneous wa e column (De Cas o e al. 2006). The sampling was
conduc ed a low ide and he sedimen was collec ed om an in e idal muddy sedimen s bank.
10
The non-indigenous species G acila ia e miculophylla and Sa gassum mu icum, and he
na i e species Ascophyllum nodosum, Fucus esiculosus, Ul a lac uca and he na i e
seag ass Zos e a ma ina, we e collec ed a di e en in e idal banks o Ria de Vigo.
Algae, seag ass and sedimen we e collec ed by hand and wi h sho els, placed in bags and
plas ic boxes and anspo ed o he lab in ice ches s.
2.2. Expe imen Se Up
A se o mic ocosm expe imen s wi h sedimen s oge he wi h in asi e (G acila ia
e miculophylla and Sa gassum mu icum) o na i e mac oalgae (Ul a lac uca, Fucus
esiculosus, Ascophyllum nodosum) and na i e seag ass (Zos e a ma ina) we e se up unde
wo empe a u e condi ions (15ºC and 20ºC).
Figu e 3- Map o he s udy si e a ea. Ria de Vigo is loca ed on he no heas Ibe ian Peninsula.
Samples we e collec ed on he in e idal banks a he en y o he es ua y.
11
As shown in Figu e 4, he expe imen se up consis ed in o six eplica es o sedimen
mic ocosms wi h he s udied mac oalgae species, seag ass, and only sedimen (con ol).
T iplica e mic ocosms o each ea men we e incuba ed a 15ºC and he o he se o iplica e
mic ocosms a 20ºC. The whole expe imen was composed by wo la ge anks (15ºC and
20ºC) including a o al o 42 mic ocosms. In each mic ocosm was in oduced 1kg o
homogenized sedimen , ollowed by 12g o he espec i e mac oalgae o seag ass, ollowed by
ano he 1 kg o sedimen o bu y mac oalgae in o he sedimen . 1L o o e lying wa e was hen
added o each mic ocosm.
The se up p o ided an ai ci cula ion sys em, and con olled hea ing sys em o main ain he
equi ed empe a u es in each ank.
Figu e 4- a) Mic ocosm se up schema ics. Each mic ocosm was composed by 1kg
sedimen in he base, ollowed by 12g o mac oalgae/seag ass, ano he 1kg o sedimen
and 1L o saline wa e (35) b) Scheme o he expe imen se up. F om he o al o 42
mic oscosms, 21 we e incuba ed a 15ªC and o he 21 a 20ºC.
18
3.2. Biomass Deg ada ion
The mac oalgae/seag ass biomass deg ada ion was de e mined a he end o he expe imen
by deduc ing he inal esh weigh o ini ial esh weigh (12g).
Acco ding o he ANOVA analysis, he biomass deg ada ion was no signi ican ly di e en
be ween he di e en empe a u e ea men s o all he mac oalgae and seag ass analyzed
alues (p>0.05). Howe e , a clea endency o highe biomass loss was obse ed in he highe
empe a u e ea men (20ºC).
Di e ences among species we e signi ican (p<0.05). The specie ha p esen ed he minimum
biomass loss was he seag ass Zos e a ma ina wi h wo eplica es eaching almos no
deg ada ion a 15ºC. The mac oalgae U. lac uca was he one ha had highe biomass
deg ada ion loosing on a e age 11.11g o biomass a 15ºC and 11.54g a 20ºC. Simila ly, F.
esiculosus and A. nodusum p esen ed simila deg ada ion alues a bo h empe a u es. Fucus
esiculosus los 9.16g and 10.01g and A. nodusum 8.02g and 9.61g, espec i ely a 15ºC and
20ºC. G acila ia e miculophylla and S. mu icum we e he wo species o mac oalgae ha
showed highe di e ences be ween empe a u es. G acila ia’s biomass loss was o 5.20g a
15ºC (lowe compa a i ely wi h he o he s) and 8.28g a 20ºC. Sa gassum’s biomass
deg ada ion was 6.33g a 15ºC and 8.79g a 20ºC. Al hough no s a is ically signi ican ,
di e ences be ween empe a u es in hese las wo in asi e species we e g aphically ob ious.
Figu e 9- Biomass deg ada ion o mac oalgae/seag ass species du ing he pe iod
o incuba ion exp essed in g ams (mean ± s anda d de ia ion).

19
3.3. NO3-, NO2- and NH4+ accumula ion in In e s i ial Wa e
As s a ed in he me hods sec ion, a he end o he expe imen he concen a ions o ino ganic
ni ogen compounds p esen in he in e s i ial wa e we e e alua ed in each mic ocosm (Figu e
10).
The concen a ions o NO3- seemed o be di e en be ween species and also be ween
empe a u es (Figu e 10a) howe e , ANOVA analysis e ealed only signi ican e ec s o
empe a u e on he NH4+ concen a ion ( able 1)
The highes NO3- concen a ion in he in e s i ial wa e we e egis e ed in he G. e miculophylla
(41; 02 ± 11; 06µM/m2 a 15ºC), F. esiculosus (37; 37 ± 2; 79µM/m2 a 20ºC) and A.nodusum
(36; 67 ± 7; 49µM/m2 a 15ºC). The lowes concen a ions occu ed in he con ol (14; 19 ± 4;
63µM/m2 a 20ºC) and in he sys ems wi h A.nodusum (22; 18 ± 3; 70µM/m2 a 20ºC).
Like he NO3- esul s, he NO2- concen a ions in in e s i ial wa e didn’ p esen signi ican
di e ences be ween ea men s. Howe e , in he case o Fucus, Sa gassum and Zos e a
ma ina, highe NO2- accumula ions in he po e wa e we e egis e ed in he lowe empe a u e
ea men s (15ºC). In gene al he quan i y o ni i es was low, wi h he excep ion o S.mu icum
(1; 81 ± 0; 87µM/m2 a 15ºC) and Z.ma ina (1; 65 ± 0; 11µM/m2 a 15ºC) (Figu e 10b). In wha
NH4+ concen a ions a e conce ned alues in he in e s i ial wa e we e ound o be much highe
han ni a es and ni i es. G acila ia e miculophylla (1482, 60 ± 318, 34µM/m2 a 15ºC), A.
nodosum (1410; 62 ± 408; 70µM/m2 a 15ºC) and F. esiculosus (1278; 39 ± 287; 72µM/m2 a
15ºC) egis e ed he highe NH4+ concen a ions in he po e wa e a he end o he expe imen
(Figu e 10c). The lowe concen a ions we e obse ed in con ol (91; 95 ± 159; 26µM/m2) and
A.nodusum (235; 40 ± 72; 53µM/m2) a 20ºC.
20
-
Figu e 10 - NO3- (a),NO2- (b) and NH4+ (c) in e s i ial wa e concen a ions,
measu ed in iplica e ea men s wi h he six species o mac oalgae and
he seag ass a e 3 weeks o incuba ion (µM) mean and s anda d
de ia ion).
21
3.4. Ne Fluxes o NO3-, NO2- and NH4+
Acco ding o igu e 11, a 15ºC, an a e age nega i e NO3- ne lux we e obse ed meaning a
clea abso p ion o NO3- by he wa e column. Ne NO3- luxes p esen ed signi ican di e ences
ela i ely o he empe a u e ea men s acco ding o he ANOVA analysis (Table 1). An
opposi e pa e n was obse ed o he 20ºC ea men , whe e he ne luxes o NO3- we e
posi i e in mos cases. Mo e impo an ly he signi ican in e ac ion be ween empe a u e and
o igin (TempxO igin, p<0.05) sugges ha empe a u e e ec s we e di e en depending on he
o igin o he species.
Ne NO2- luxes we e ela i ely lowe when compa ed wi h NO3- ne luxes and he lowes alues
we e egis e ed in he con ols. Tempe a u e seemed o ha e e ec s, con ibu ing o highe
elease o NO2- o he wa e column a 20ºC. A 15ºC he luxes we e null o nega i e in mos o
he cases, wi h he excep ion o Zos e a ma ina and Fucus esiculosus, whe e e luxes o NO2-
we e also egis e ed a 15ºC. Howe e none o he ea men s we e signi ican .
Figu e 11 - NO3- ne lux o all he ea men s pe o med a 15ºC and 20ºC (µmol
NO3-m-2, mean, s anda d de ia ion). Posi i e alues ep esen elease o he nu ien
o he wa e column and nega i e alues ep esen up ake o he nu ien by he
sedimen s. Blue ba s ep esen alues a 15ºC; Red ba s ep esen he alues a
20ºC.
Sou ce F P F e sus F P F e sus F P F e sus
Tempe a u e 0.37 0.5692 eXid 0.22 0.6585 eXid 65.41 0.0005 eXid
Iden i y 1.24 0.3201 RES 0.23 0.9477 RES 0.95 0.4669 RES
Tempe a u e X Iden i y 0.72 0.6122 RES 0.69 0.635 RES 0.08 0.9952 RES
Ni a es
Ni i es
Ammonia
Slu ies Concen a ions
Table 1 - ANOVA analysis be ween empe a u e ( ixed e ec ) and iden i y ( andom e ec ) on N in in e s i ial
wa e Concen a ions. None o he esul s was signi ican in ela ion o he di e en empe a u es (p>0.05)
22
In he highe empe a u e ea men s (20ºC), a es o NO2- elease we e highe in he
mic ocosm wi h he di e en mac oalgae, compa ing wi h he con ols (only sedimen ), whe e
almos null ne luxes o NO2- we e egis e ed. Lowe NO2- ne luxes we e also e i ied in he
Sa gassum mu icum ea men . The highe elease a es we e obse ed a in Ascophyllum
nodosum and Fucus esiculosus a he 20ºC ea men (Figu e 12).
In gene al, he lowe empe a u e (15ºC) seemed o s imula e he ne NH4+ elease o he wa e
column, wi h he excep ion o G acila ia e miculophylla and Sa gassum mu icum. This
empe a u e e ec was no signi ican bu p alues we e ela i ely low (p<0.1). Wi h espec o
NH4+ ne luxes di e en esul s seemed o occu acco ding o he mac oalgae/seag ass
species iden i y, howe e hese di e ences we e no signi ican (Table 2) (Figu e 13).
Figu e 12 - NO2- ne lux o all he ea men s pe o med a 15ºC and 20ºC (µmol NO2-
m-2, mean, s anda d de ia ion). Posi i e alues ep esen elease o he nu ien o he
wa e column and nega i e alues ep esen up ake o he nu ien by he sedimen s.
Blue ba s ep esen alues a 15ºC; Red ba s ep esen he alues a 20ºC.
Figu e 13 - NH4+ ne lux o all he ea men s pe o med a 15ºC and 20ºC (µmol NH4+
m-2, mean, s anda d de ia ion). Posi i e alues ep esen elease o he nu ien o
he wa e column and nega i e alues ep esen up ake o he nu ien by he
sedimen s. Blue ba s ep esen alues a 15ºC; Red ba s ep esen he alues a
20ºC
23
Table 2 - ANOVA analysis be ween empe a u e ( ixed e ec ) and iden i y ( andom e ec ) on N Ne
Fluxes. Signi ican alues (p <0,05) a e p esen ed on NO3 Ne Fluxes ( ed bold). Iden i y has an
in luence on he ne luxes (p = 0, 03) be ween na i e species (p = 0, 13) allowing o ob ain he and p
alues o empe a u e X o igin (p = 0, 0095).
Sou ce F P F e sus F P F e sus F P F e sus
Tempe a u e 8.15 0.029 eXid 0.69 0.4372 eXid 3.92 0.0951 eXid
Iden i y 0.36 0.8971 RES 0.56 0.7608 RES 0.77 0.6007 RES
Tempe a u e X Iden i y 3.14 0.029 RES 1.29 0.2949 RES 0.79 0.5845 RES
Tempe a u e X IdNa i e 1.94 0.130 RES
Tempe a u e X IdIn asi e 3.36 0.077 RES
Tempe a u e X O igin 7.74 0.00096 RES
N Ne Fluxes
Ni a es
Ni i es
Ammonia

24
4. Bac e ial Di e si y
DNA p o iling o he bac e ial communi ies in he sedimen s o all ea men s was pe o med by
Au oma ed RNA In e genic Space analysis agmen leng hs (ARISA-AFLs). The dis ibu ion
o he di e en phylo ypes among he di e en samples co esponds o di e ences in hei
gene ic s uc u es. We pe o med a mul idimensional scaling analysis based on he bac e ia
ARISA-AFLs p o iles ob ained o all ea men s (Figu e 14). Resul s showed no signi ican
di e ences in he s uc u e o bac e ia communi ies wi hin he di e en empe a u e ea men s
(15ºC and 20ºC), con i med by he ANOSIM es (R = -0,009; Signi icance le el = 53, 8%) and
be ween mac oalgae ypes (in asi e and na i e) acco ding o he ANOSIM es (R= -0,007;
Signi icance le el = 45, 6%). Al hough acco ding o ou analysis is clea he occu ence o a
bac e ial communi y selec ion in Fucus esiculosus and Ascophyllum nodosum (R= 0.34;
Signi icance le el= 0.1%), since MDS analysis showed a clea di e en ia ion in he mic obial
communi y s uc u e in samples collec ed in he F. esiculosus and A.nodusum ea men s,
bo h a 20ºC and 15ºC.
Figu e 14 -Mul idimensional scaling (MDS) o dina ion based on B ay–
Cu is simila i ies on he p esence/absence ma ix ob ained om ARISA
inge p in s o bac e ial communi ies. The numbe s (1 and 2) ha
appea ed nex o he species names a e e e ed o 15ºC and 20ºC,
espec i ely.
25
CHAPTER 4
4. Discussion
S esso s a e expec ed o exe complex e ec s ha canno be easily in e ed using single-
s esso s udies because syne gis ic o an agonis ic in e ac ions may occu (Fol and Chen
1999). Fo ins ance, some e idence sugges s ha in e ac ions be ween clima e change and
biological in asions a e likely o ha e widesp ead and unexpec ed e ec s on coas al
ecosys em dynamics (Ha ley and Hughes 2006). None heless, despi e he high esea ch e o
dedica ed o clima e change and non-indigenous species in he ma ine ealm, empi ical s udies
linking hese s esso s a e limi ed and mos ly a e obse a ional s udies p e en ing any
p edic ion o u u e scena ios. Rossi (2007) in es iga ed he ans e o algal-de i ed C and N o
he sedimen and o he in auna eeding and disco e ed ha he ans e o C and N o he
sedimen and o he su ace deposi - eede s can be a ele an mechanism o emo e he
excess o de i us. The ela ionship be ween species di e si y and ecosys em unc ioning in
na u al communi ies a e se e e en i onmen al s ess we e s udied by Rossi e al. (2009), who
demons a ed ha he ca bon ha low wi hin he sys em is highly dependen on he dominan
species ha a en’ eplaced du ing succession, becoming a keys one o he s abili y o
ecosys em unc ioning unde en i onmen al dis u bances.
4.1. In luence on ino ganic N biogeochemis y
S udies in Sa gassum mu icum in asion showed di e en conclusions (Wilson, 2001; B i on-
Simmons, 2004; A enas e al. 2006; Olaba ia e al. 2009; Cacabelos e al. 2013). While some
demons a ed no impac o S. mu icum on he na i e species abundance, o he s showed e ec
a small-scales and wi h in luence in educing he abundance o na i e canopy algae. Rela i ely
o G acila ia e micullopylla, hese p e ious indings demons a ed ha he in asion o his
algae ha e nega i e e ec s on na i e seag ass beds o Zos e a ma ina by dec easing ne lea
pho osyn hesis and su i al a es (Ma ínez-Lüsche and Holme 2010b) and a ec ing he
ecosys em nu ien s cycling (Thomsen e al. 2009). In ag eemen , ou esul s clea ly showed an
impac o he mac oalgae deg ada ion bu ied in he sedimen s, in o he ne luxes o NO2-, NO3-
and NH4+ o he wa e column, howe e he e was no di e en ia ed e ec o S. mu icum and G.
e micullophylla when compa ed wi h all he o he na i e mac oalgae/seag ass na i e species.
Lemley e al. (2014) s udied he e ec o di e en empe a u e egimes on he a e o
decomposi ion o h ee mac ophy e species and e alua ed he ex en o ino ganic nu ien s
eleased. Thei esul s showed ha he elease o ino ganic nu ien s was g ea es a highe
26
empe a u es (i.e. 25°C and 30°C), due o he educed bac e ial ac i i y a lowe empe a u es
(i.e. 15°C). Ou esul s o ne luxes o NO2- and NO3- a e in ag eemen wi h his p e ious s udy,
since we ound ha he highe empe a u e es ed gene ally shi he ne luxes o hese
compounds om an up ake by he sedimen s a 15ºC o a elease o he o e lying wa e a
20ºC. Howe e , a di e en pic u e eme ges in he case o NH4+ ne luxes, since highe elease
was almos always egis e ed in he lowe empe a u e ea men . While he p ocesses
esponsible o he ni ogen ans o ma ions we e no e alua ed in ou s udy, p e ious indings
could be explained by he ac ha mic obial communi ies ha use NH4+ (Ni i ie s) whe e
s imula ed a highe empe a u es educing he amoun o he NH4+ a ailable and consequen ly
lowe elease o he wa e column. In ac , esul s on he concen a ions o NH4+ in he
in e s i ial wa e a e in ag eemen , since highe NH4+ concen a ions in he po e wa e we e in
almos o he cases ob ained o he lowe empe a u e ea men (15ºC). The decomposi ion o
algae he e o e p o ides a po en ially impo an supply o o ganic and ino ganic compounds o
he wa e column whe e hey can be ecycled apidly (Gab ielson e al. 1983; Twilley e al.
1986; Paalme e al. 2002).
Acco ding o ou s a is ical analysis, NO3- ne luxes, we e he only lux signi ican ly a ec ed by
empe a u e, howe e no signi ican di e ences we e obse ed among na i es (p=0.13,
p>0.05) o in asi e (p=0.07. p>0.05) species. Ne e heless, when using he me hod o
combining he sum o squa es alues om sepa a e analyses o a iance we eached a
signi ican alue be ween empe a u e and o igin (p =0.0095, p<0.05) meaning ha being
na i e o in asi e make di e ence on he assimila ion o elease o ni a es a he di e en
empe a u e ea men s. Al hough no s a is ically signi ican , in asi e species p esen an
app oxima ed p alue o 0.05 (p = 0. 07), hus is mo e likely o ha e a g ea e e ec in on he
ni ogen cycle be ween he wo in asi e species han na i e ones. Ne NO3- luxes we e
always nega i e o he 15ºC ea men , wi h he excep ion o Sa gassum mu icum and
Zoos e a ma ina, whe e a elease o NO3- o he wa e column was obse ed. These esul s
sugges ed ha he lowe empe a u e s imula es he ben hic p ocesses in ol ed in NO3-
consump ion, i.e. deni i ica ion, anammox, and dissimila o y ni a e educ ion o ammonia
(DNRA) (Jensen e al. 1990; Kemp e al. 1990; Sei zinge 1990). An explana ion o he
excep ions ha occu ed on NO3- luxes a e he ac ha Sa gassum mu icum is an in asi e
species wi h di e en beha io a low empe a u es han he o he species (Allison 2004; Ha ley
and Hughes 2006), con ibu ing o he adso p ion o consump ion o ni a es by he sedimen s.
Howe e , Zos e a ma ina, which is a seag ass, has di e en me abolic pa e ns ela i ely o
mac oalgae (Hemminga and Dua e 2000).
On he o he hand ea men s a 20ºC, showed posi i e ne NO3- luxes wi h he excep ion o
Sa gassum mu icum, whe e an adso p ion o NO3- by he sedimen s we e egis e ed. Taking in
27
o accoun he p ocesses in ol ed in he N cycle, we can hypo hesized ha he NO3- educ ion
p ocesses, like deni i ica ion and annamox a e a o able by low empe a u es. I could be also
he case ha hose p ocesses a e no a ec ed, bu empe a u e could s imula e ni i ica ion
(oxida ion o NH4+ o NO3- and o NO2-), esul ing in a highe elease o NO3- and NO2- o he
o e lying wa e a he 20ºC ea men s (Lemley e al. 2014). The ni i e luxes a 15ºC we e
close o ze o, and only Zos e a ma ina p esen ed a clea abso p ion o ni i es. In deed NO2-
and PO43– ne e luxes a e no mally expec ed o be lowe han hose o NO3– and NH4+ (Ga cía-
Robledo e al. 2008). A 20ºC, was obse ed a gene al elease o ni i e o he wa e column.
Ne luxes o NH4+ we e always posi i e, so he e is a gene al elease o ammonia o he wa e
column, p obably because mac oalgae/seag ass deg ada ion s imula ed bac e ial deg ada ion /
ammoni ica ion by he la ge inpu o o ganic ma e in o he sedimen s. The highe a es o NH4+
e luxes egis e ed a he 15ºC ea men s could no jus be explain by a s imula ion o
ammoni ica ion bu also on he mic obial communi ies in ol ed on he DNRA.
Rossi e al. (2011) emphasized he impo ance o de i al di e si y and non-na i e seaweeds in
ben hic ni ogen cycling showing ha he de i al mixing o S. mu icum, F. esiculosus and
U.lac uca p o ided mo e 15N-ni ogen o sedimen s and o he mac o auna due o he high
composi ion o polyphenols in S. mu icum and F. esiculosus, and he la ge amoun s o
ni ogen con en in U. lac uca. In e es ing, in ou expe imen s he sys ems wi h F. esiculosus
p esen ed he highes accumula ion o NO2- in he in e s i ial wa e , when compa ed wi h he
o he mac oalgae/seag ass ea men s. Acco ding o he ANOVA analysis, he ino ganic N
concen a ions in he in e s i ial wa e we e no a ec ed by he di e en empe a u es (Table 2).
Al hough a signi ican inc ease o NO2-, NO3- and NH4+ in po e wa e occu ed in all ea men s
wi h mac oalgae/seag ass compa ed wi h he con ols (only sedimen ), sugges ing ha he
deg ada ion o hese species s imula ed N accumula ion/a ailabili y in he in e s i ial wa e s. In
ag eemen o ou esul s, a s udy pe o med in he egion o Puck Bay also showed ha he
inc eased concen a ions o o ganic ma e we e ollowed by highe NH4+ concen a ions in
in e s i ial wa e s (Bolałek and G aca 1996). In ac hese esul s a e expec ed since he
concen a ion o ino ganic ni ogen compounds in in e s i ial wa e s end o be p opo ional
ela ed o he o ganic ma e con en in he sedimen s which in u n s imula ed ammoni ica ion,
wi h he o ma ion o ammonium (Bolałek and G aca 1996).
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