Oecol Aust 16(2) 311-329 2012
Oecologia Australis16(2) 311-329 Junho 2012httpdxdoiorg104257oeco2012160209
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO FATORES REGULADORES E FLUXOS DE DIFERENTES AMBIENTES
Viviane Figueiredo Souzasup1 amp Alex Enrich-Prastsup1sup1Universidade Federal do Rio de Janeiro (UFRJ) Centro de Ciecircncias da Sauacutede (CCS) Instituto de Biologia Departamento de Ecologia Laboratoacuterio de Biogeoquiacutemica Av Carlos Chagas Filho 373 Inter-blocos A-F Caixa Postal 68016 Ilha do Fundatildeo - Cidade Universitaacuteria Rio de Janeiro RJ Brasil CEP 21941-971 E-mails vivibioufrjhotmailcom aenrichprastgmailcom
RESUMOO oacutexido nitroso (N2O) eacute um dos trecircs principais gases causadores do efeito estufa aleacutem de jaacute ser apontado
como o principal gaacutes destruidor da camada de ozocircnio neste seacuteculo Este gaacutes eacute produzido naturalmente atraveacutes dos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo em ambientes aquaacuteticos e terrestres Taxas de emissotildees de N2O tecircm sido amplamente estudadas em ecossistemas terrestres poreacutem comparativamente estas tecircm sido negligenciadas em ecossistemas aquaacuteticos continentais apesar do recente reconhecimento da importacircncia destes ambientes nos ciclos globais de carbono e nitrogecircnio O objetivo deste trabalho foi apresentar os principais fatores reguladores da produccedilatildeo de N2O atraveacutes dos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo em lagos reservatoacuterios rios mangues e estuaacuterios As taxas de emissatildeo N2O destes ambientes apresentam grande diferenccedila entre si variando em ateacute quatro ordens de magnitude Os maiores valores de fluxo de N2O foram observados em estuaacuterios manguezais e rios Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade de fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O uma vez que esse gaacutes eacute derivado de alteraccedilotildees ambientais Palavras-chave oacutexido nitroso nitrificaccedilatildeo desnitrificaccedilatildeo fatores reguladores sistemas aquaacuteticos continentais
ABSTRACTNITROUS OXIDE (N2O) IN AQUATIC SYSTEMS PRODUCTION REGULATING FACTORS
AND FLUXES FROM DIFERENT ENVIRONMENTS Nitrous oxide (N2O) is one of the three main greenhouse gases besides being identified as the main destroyer gas of the ozone layer in this century This gas is naturally produced through the processes of nitrification and denitrification in aquatic and terrestrial environments Rates of N2O emissions have been widely studied in terrestrial ecosystems but comparatively they have been neglected in freshwater ecosystems despite the recent recognition of the importance of these environments in the global cycles of carbon and nitrogen The objective of this study was to present the main regulating factors on the production of N2O through nitrification and denitrification processes in lakes reservoirs rivers mangroves and estuaries Rates of N2O emission in such environments exhibit great differences from each other ranging up to four orders of magnitude The highest N2O fluxes were observed in estuaries mangroves and rivers Lakes and reservoirs are more stable environments than mangroves estuaries and rivers and this feature makes the variability of factors such as pH and nutrient concentrations are lower favoring greater stability of processes and consequently a lower production and emission of N2O since this gas is derived from environmental changesKeywords nitrous oxide nitrification denitrification regulating factors continental aquatic systems
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RESUMENOacuteXIDO NITROSO (N2O) EN AMBIENTES ACUAacuteTICOS PRODUCCIOacuteN FACTORES
REGULADORES Y FLUJOS DE DIFERENTES AMBIENTES El oacutexido nitroso (N2O) es uno de los tres principales gases de efecto invernadero ademaacutes se manifiesta como el principal gas destructor de la capa de ozono en este siglo Este gas es producido naturalmente a traveacutes de los procesos de nitrificacioacuten y desnitrificacioacuten en ambientes acuaacuteticos y terrestres Las tasas de emisioacuten de N2O han sido ampliamente estudiadas en ecosistemas terrestres pero comparativamente han sido olvidadas en los ecosistemas de agua dulce a pesar del reciente reconocimiento de la importancia de estos ambientes en los ciclos globales de carbono y nitroacutegeno El objetivo de este estudio fue presentar los factores de regulacioacuten principales en la produccioacuten de N2O a traveacutes de los procesos de nitrificacioacuten y desnitrificacion en los lagos embalses riacuteos manglares y estuarios Las tasas de emisioacuten de N2O en tales ambientes exhiben grandes diferencias entre siacute variando en hasta cuatro oacuterdenes de magnitud Los mayores valores de flujo de N2O fueron observados en los estuarios manglares y riacuteos Los lagos y embalses son ambientes maacutes estables que los manglares estuarios y riacuteos y esta caracteriacutestica hace que la variabilidad de factores tales como el pH y las concentraciones de nutrientes sea inferior favoreciendo una mayor estabilidad de los procesos y en consecuencia una menor produccioacuten y emisioacuten de N2O dado que este gas deriva de las alteraciones ambientales Palabras clave oacutexido nitroso nitrificacioacuten desnitrificacioacuten factores reguladores ambientes acuaacuteticos continentales
INTRODUCcedilAtildeO
Eacute amplamente aceito que uma das principais causas das mudanccedilas climaacuteticas eacute o aumento da concentraccedilatildeo atmosfeacuterica de gases estufa como dioacutexido de carbono (CO2) metano (CH4) e oacutexido nitroso (N2O) (IPCC 2001) Apesar do CO2 estar em maior concentraccedilatildeo o N2O apresenta maior tempo de residecircncia na atmosfera aproximadamente 120 anos e eacute 310 vezes mais potente na retenccedilatildeo de radiaccedilatildeo infravermelha (IPCC 2001) que ocorre na troposfera onde o gaacutes fica acumulado Essa propriedade de absorver radiaccedilatildeo de ondas de comprimentos longos como a radiaccedilatildeo infravermelha confere ao N2O a capacidade de elevar a temperatura da atmosfera e consequentemente da Terra (Braker amp Conrad 2011) contribuindo com aproximadamente 6 do aquecimento adicional do planeta (Werner et al 2007)
Outra caracteriacutestica relevante do N2O eacute a similaridade deste gaacutes com os CloroFluorCarbonetos (CFCs) Quando presentes nas camadas atmosfeacutericas ambos os compostos satildeo estaacuteveis na troposfera mas instaacuteveis na estratosfera e assim portanto causando a liberaccedilatildeo de ativos quiacutemicos tal como o oacutexido niacutetrico (NO) que reagem com o ozocircnio da camada de ozocircnio causando sua destruiccedilatildeo cataliacutetica (Ravishankara et al 2009) Essa camada protege a Terra dos raios
UV e tem sido continuamente destruiacuteda o que agrava as chamadas mudanccedilas climaacuteticas (IPCC 2007) Atualmente o N2O tem sido considerado a principal substacircncia emitida destruidora do ozocircnio uma vez que os CFCs tecircm suas emissotildees fortemente controladas (Ravishankara et al 2009) De 1750 ateacute hoje as concentraccedilotildees atmosfeacutericas de N2O vecircm aumentando (Figura 1) com um acreacutescimo de aproximadamente 18 desde a era preacute-industrial quando sua concentraccedilatildeo era de cerca de 270ppb chegando a 319ppb em 2000 (Forster et al 2007)
Figura 1 Mudanccedilas nas concentraccedilotildees atmosfeacutericas de N2O de 1000 ateacute 2000 DC verificadas atraveacutes de testemunhos de gelo Eixo esquerdo concentraccedilotildees atmosfeacutericas de N2O (ppb) Eixo direito forccedila radiativa do
N2O atmosfeacuterico (adaptada de IPCC 2001)Figure 1 Changes in atmospheric concentrations of N2O form 1000 to 2000 AC verified by ice cores Left axis atmospheric concentrations of N2O (ppb) Right axis radioactive forcing of atmospheric N2O (adapted
from IPCC 2001)
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
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PROCESSOS FORMADORES DE N2O
A produccedilatildeo e consumo de N2O em ambientes aquaacuteticos continentais estatildeo diretamente associados aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Figura 2) Estes processos ocorrem em vaacuterios compartimentos dos ecossistemas aquaacuteticos como aacutegua solo sedimento perifiacuteton rizosfera de plantas aquaacuteticas ou algas Esses diferentes compartimentos apresentam distintas condiccedilotildees ambientais que afetam a composiccedilatildeo da comunidade microbiana e tambeacutem influenciam o seu potencial nitrificante e desnitrificante (Bastviken et al 2003)
Diante dessa variabilidade de fatores reguladores destaca-se a produccedilatildeo de N2O em virtude do acoplamento nitrificaccedilatildeo-desnitrificaccedilatildeo visto que o primeiro processo subsidia com seu produto final o segundo processo (Kremen et al 2005) Com isso as bacteacuterias desnitrificantes conseguem fazer uso do composto necessaacuterio advindo de uma via externa (desnitrificaccedilatildeo direta) ou interna (nitrificaccedilatildeo-desnitrificaccedilatildeo acoplada) o que pode aumenta o potencial desnitrificante do ambiente (Fennel et al 2009) Diversos estudos satildeo desenvolvidos visando identificar esse acoplamento dos processos atraveacutes do uso de isoacutetopos estaacuteveis que podem rastrear a origem dos compostos e verificar assim a contribuiccedilatildeo externa e interna na produccedilatildeo de gases nitrogenados (Nicolaisen et al 2004)
Figura 2 Ciclo do nitrogecircnio em ecossistemas aquaacuteticos continentais Em destaque os principais processos bacterianos envolvidos na emissatildeo
de N2O (adaptada de Santoro amp Enrich-Prast 2011)Figure 2 Nitrogen cycle in continental aquatic ecosystems Highlights the main bacterial processes involved in the emission of N2O (adapted
from Santoro amp Enrich-Prast 2011)
NITRIFICACcedilAtildeO
A nitrificaccedilatildeo autotroacutefica eacute um processo microbiano realizado por dois grupos de bacteacuterias quimiolitoautotroacuteficas (Nitrosospira e Nitrosomonas) bacteacuterias que obteacutem energia atraveacutes da oxidaccedilatildeo de compostos inorgacircnicos (Fiencke et al 2006) Esse processo do ciclo do N (Figura 2) se resume agrave oxidaccedilatildeo da amocircnia (NH3) a nitrito (NO2
-) e deste finalmente a nitrato (NO3
-) Esse processo eacute estritamente aeroacutebico ocorrendo obrigatoriamente na porccedilatildeo oacutexica de compartimentos como a aacutegua superfiacutecie do sedimento e solo ou no entorno de raiacutezes submersas (Reddy et al 1989) A formaccedilatildeo de N2O por esse tipo de nitrificaccedilatildeo pode ocorrer durante a oxidaccedilatildeo da NH3 a NO2
- (Frame amp Casciotti 2010) Entretanto sua produccedilatildeo eacute mais reduzida do que a quantidade do NO2
- produzido (Arp amp Stein 2003) e depende de caracteriacutesticas do ambiente (Schmidt et al 2001) Um fator crucial para a produccedilatildeo de N2O eacute a diminuiccedilatildeo das concentraccedilotildees de oxigecircnio disponiacuteveis durante o processo de nitrificaccedilatildeo uma vez que a reaccedilatildeo ocorre de maneira incompleta formando NO ou N2O ao inveacutes de formar NO2
- (Anderson et al 1993) O oacutexido de nitrogecircnio produzido tambeacutem seraacute regulado pela umidade do solo no momento das reaccedilotildees (Davidson et al 1993)
A nitrificaccedilatildeo heterotroacutefica eacute realizada por bacteacuterias fungos e algas que assim como na nitrificaccedilatildeo autotroacutefica oxidam a amocircnia a nitrato sob condiccedilotildees aeroacutebicas e tambeacutem produzem N2O (Hayatsu et al 2008) Entretanto por ser um processo heterotroacutefico natildeo haacute geraccedilatildeo de energia o que torna esses organismos dependentes de substratos orgacircnicos para obtenccedilatildeo de energia Aleacutem disso as taxas da desnitrificaccedilatildeo heterotroacutefica satildeo mais baixas que da nitrificaccedilatildeo autotroacutefica indicando uma reduzida contribuiccedilatildeo desse processo nitrogenado (Fiencke et al 2006)
Um terceiro tipo de nitrificaccedilatildeo eacute a desnitrificaccedilatildeo nitrificante uma das vias da nitrificaccedilatildeo realizada por um uacutenico grupo de bacteacuterias chamadas autotroacuteficas oxidadoras de NH3 (Wrage et al 2001) Nessa via ocorre a oxidaccedilatildeo de NH3 a NO2
- como na nitrificaccedilatildeo e posteriormente ocorre a reduccedilatildeo do NO2
- a N2ON2 como na desnitrificaccedilatildeo (Wrage et al 2001) Entretanto assim como a nitrificaccedilatildeo heterotroacutefica a
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desnitrificaccedilatildeo nitrificante eacute menos estudada e ateacute o momento sabe-se apenas que a contribuiccedilatildeo de ambos os processos na produccedilatildeo de N2O varia de acordo com fatores bioloacutegicos e fiacutesicos do solo (Kool et al 2011) A pequena quantidade de informaccedilotildees sobre estes processos indica que estes precisam ser melhor quantificados nas diversas regiotildees do nosso planeta
Indiscutivelmente o principal preacute-requisito para que a nitrificaccedilatildeo ocorra eacute a disponibilidade de NH3NH4
+ o substrato nitrogenado baacutesico para ocorrecircncia desse processo Uma das principais fontes desses compostos nos ecossistemas aquaacuteticos e terrestres eacute a degradaccedilatildeo de mateacuteria orgacircnica laacutebil que libera diferentes compostos como nitrogecircnio orgacircnico NH3 NO2
- NO3- e fosfato (Balota amp Auler 2011)
Derivado dessa mineralizaccedilatildeo a NH3 eacute uma fonte de nitrogecircnio extremamente laacutebil e de faacutecil assimilaccedilatildeo pelos vaacuterios tipos de macro e micro-organismos o que muitas vezes torna esse composto limitante no ambiente (Sasaki et al 2002 Schmidt et al 2011) Excretas nitrogenados advindos de organismos heterotroacuteficos tambeacutem satildeo uma importante fonte de NH3NH4
+As concentraccedilotildees relativas de NH3 e NH4
+ na aacutegua satildeo dependentes principalmente do pH da aacutegua Reconhecidamente na maioria dos ambientes a forma nitrogenada predominante eacute o NH4
+ jaacute que a forma NH3 gasosa eacute dominante apenas entre pH 8-10 (Johnson et al 2008) valores estes menos frequentes nos sistemas aquaacuteticos Entretanto eacute nessa faixa de pH alcalino que a NH3 estaacute na fase gasosa e eacute liberada em maior quantidade para a atmosfera atraveacutes da volatilizaccedilatildeo (Jayaweera amp Mikkelsen 1991 Bajwa et al 2006 Fiencke et al 2006 Haden et al 2011) Logo sua assimilaccedilatildeo bem como a volatilizaccedilatildeo indisponibilizam o nitrogecircnio para o processo nitrificante reduzindo as taxas de desnitrificaccedilatildeo e consequentemente a produccedilatildeo de N2O
Desnitrificaccedilatildeo
A desnitrificaccedilatildeo eacute um processo bacteriano anaeroacutebico facultativo de degradaccedilatildeo da mateacuteria orgacircnica que em ausecircncia de oxigecircnio utiliza o NO3
- como receptor de eleacutetrons reduzindo-o agrave N2 Esse processo ocorre no sedimento e na coluna drsquoaacutegua estratificada imediatamente abaixo da zona oacutexica devido agrave formaccedilatildeo de NO3
- via nitrificaccedilatildeo
ou utilizando o substrato que tenha sido formado em outro ambiente (Kuschk et al 2003) Produtos intermediaacuterios do processo de desnitrificaccedilatildeo o NO e o N2O podem ser emitidos para a atmosfera A principal forma de perda de nitrogecircnio disponiacutevel no ambiente eacute atraveacutes do processo de desnitrificaccedilatildeo (Fennel et al 2009) onde os produtos intermediaacuterio eou finais (NO N2O e N2) satildeo gasosos e podem ser difundidos para a atmosfera tornando o nitrogecircnio um elemento limitante para outros organismos no ambiente (Seitzinger 1988 Harrison et al 2005)
Em ambientes eutrofizados como rios lagos e solos agriacutecolas com excesso de nutrientes a desnitrificaccedilatildeo acaba por reduzir a quantidade de compostos nitrogenados diminuindo a eutrofizaccedilatildeo dos ecossistemas bem como a lixiviaccedilatildeo do nitrogecircnio para outros ecossistemas (Seitzinger 1988 Seitzinger et al 2006) Por outro lado esse eacute o principal processo microbiano produtor de N2O agravando problemas como o aquecimento global e a destruiccedilatildeo da camada de ozocircnio Alteraccedilotildees da quantidade de N2O emitido ocorrem com frequumlecircncia devido a modificaccedilotildees bruscas das condiccedilotildees oacutexica-anoacutexica de solos e sedimentos e das concentraccedilotildees de NH3 e de NO2
- (Kampschreur et al 2009) Com isso ecossistemas aquaacuteticos ou ambientes terrestres sujeitos a influecircncia de aporte de aacuteguas satildeo fontes potencias na emissatildeo de N2O (Scott et al 2008) Segundo Kool et al (2011) a desnitrificaccedilatildeo eacute o principal processo formador de N2O embora a nitrificaccedilatildeo tambeacutem seja representativa em alguns tipos de solo
O NO3- eacute o principal substrato limitante para
a desnitrificaccedilatildeo e sua disponibilidade no meio eacute variaacutevel e dependente de diversos aspectos sendo um deles o tipo de solo que pode reter esse acircnion (Barrett amp Burke 2002) Entretanto esse mecanismo abioacutetico ainda eacute pouco estudado (Berntson amp Aber 2000 Zhu amp Wang 2011) e resume-se a adsorccedilatildeo do NO3
- a partiacuteculas do solo imobilizando esse importante nutriente nitrogenado e podendo ateacute tornaacute-lo limitante aos organismos de acordo com o estado troacutefico do ambiente (Bernot amp Dodds 2005)
FATORES REGULADORES DA PRODUCcedilAtildeO DE N2O
Os processos de nitrificaccedilatildeo e de desnitrificaccedilatildeo demandam disponibilidade de amocircnia e nitrato (NH3
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
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e NO3-) no ambiente Entretanto essa disponibilidade
eacute alterada em funccedilatildeo de vaacuterios fatores reguladores como concentraccedilotildees de oxigecircnio e mateacuteria orgacircnica temperatura pH umidade (Darrouzet-Nardi amp Bowman 1988 Seitzinger 1988 Miller et al 2009 Ross amp Wemple 2011) topografia (John et al 2007) e tambeacutem competiccedilatildeo entre as bacteacuterias do ciclo do nitrogecircnio e destas com outros micro-organismos e plantas (Inselsbacher et al 2010) Tais fatores bioacuteticos e abioacuteticos satildeo relevantes pois afetam principalmente a atividade e o crescimento microbiano (Mamilov amp Dilly 2002) Fatores reguladores podem variar espaccedilo-temporalmente afetando a produccedilatildeo de oacutexido nitroso que por estar associada aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Perez et al 2006 Farquharson amp Baldock 2008 Ma et al 2008) pode variar nessa mesma escala (McClain et al 2003) A seguir apresentamos e descrevemos os principais fatores reguladores da nitrificaccedilatildeo e da desnitrificaccedilatildeo
OXIGEcircNIO
Sendo a nitrificaccedilatildeo um processo estritamente aeroacutebico a presenccedila de oxigecircnio eacute um dos seus principais fatores reguladores (Bollmann amp Conrad 1998) Na Figura 3 observa-se a taxa de nitrificaccedilatildeo aumentar concomitantemente com a pressatildeo parcial de oxigecircnio em um solo agriacutecola ressaltando a influecircncia da disponibilidade de oxigecircnio sobre esse processo (Bollmann amp Conrad 1998) A disponibilidade de O2 pode ser totalmente alterada em funccedilatildeo da presenccedila de aacutegua no solo que ocupa o espaccedilo do oxigecircnio e restringe a velocidade da sua difusatildeo (Tiedje 1988)
Sedimentos de ambientes lagunares muitas vezes tecircm uma miacutenima camada superficial oacutexica que pode variar com a profundidade do lago Desta maneira deve-se ressaltar a importacircncia da presenccedila de micro-organismos fotossintetizantes em sedimentos de ambientes aquaacuteticos aumentando a oxigenaccedilatildeo e penetraccedilatildeo de O2 nas camadas mais profundas e possibilitando a ocorrecircncia da oxidaccedilatildeo da amocircnia em outras faixas do sedimento (Lorenzen et al 1998) (Figura 4) De maneira semelhante aos fotossintetizantes as raiacutezes de plantas em sistemas aquaacuteticos proporcionam a difusatildeo de oxigecircnio das raiacutezes para zonas anoacutexicas do sedimento criando microambientes oxigenados e permitindo que a nitrificaccedilatildeo ocorra e subsidie a desnitrificaccedilatildeo atraveacutes
do acoplamento dos processos (Reddy et al 1989 Ottosen et al 1999)
Solos expostos satildeo ambientes com grande oxigenaccedilatildeo dependentes de eventos de alagamento e do tipo de agregaccedilatildeo das partiacuteculas que compotildeem o solo Logo satildeo ambientes com elevado potencial nitrificante e tambeacutem de produccedilatildeo N2O Isso porque uma vez que o solo eacute molhado a disponibilidade de oxigecircnio diminui progressivamente e a nitrificaccedilatildeo ocorre de maneira incompleta produzindo NO ou N2O (Davidson et al 1993)
Figura 3 Influecircncia da pressatildeo parcial de O2 sobre a mineralizaccedilatildeo de nitrogecircnio () e sobre a nitrificaccedilatildeo () em um solo agriacutecola de Timmerlah (Alemanha meacutedia plusmn DP n=3 adaptado de Bollmann and Conrad 1998)Figure 3 Influence of partial pressure of O2 on mineralization of nitrogen () and on nitrification () on an agricultural soil of Timmerlah (Germany mean plusmn DP n=3 adapted from Bollmann and Conrad 1998)
Realizada por bacteacuterias facultativas a desnitrificaccedilatildeo natildeo ocorre em locais com alta concentraccedilatildeo de oxigecircnio pois os micro-organismos datildeo prioridade para a respiraccedilatildeo aeroacutebica mais favoraacutevel energeticamente Isso torna a presenccedila de oxigecircnio um fator regulador de grande relevacircncia (Bollmann amp Conrad 1998 Morley amp Baggs 2010) Diante dessa importacircncia encontramos um maior nuacutemero de registros de desnitrificaccedilatildeo em ambientes com baixa concentraccedilatildeo ou completa ausecircncia de oxigenaccedilatildeo como eacute o caso do sedimento de lagos planiacutecies de inundaccedilatildeo ou quaisquer aacutereas cobertas por aacutegua de pouca turbulecircncia Solos tambeacutem tecircm alto potencial desnitrificante devido agrave ocorrecircncia de chuvas que os tornam temporariamente anoacutexicos ou com baixa oxigenaccedilatildeo Um bom exemplo da regulaccedilatildeo do oxigecircnio sobre a desnitrificaccedilatildeo (Figura 4) ocorre na zona onde o oxigecircnio estaacute ausente (Lorenzen et al 1998) Aleacutem do oxigecircnio observa-se a influecircncia direta do NO3
- sobre as taxas
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de desnitrificaccedilatildeo onde este composto eacute o principal substrato desse processo sendo entatildeo considerado seu principal fator regulador Dessa forma identificamos atraveacutes do perfil de concentraccedilatildeo de NO3
- na camada superficial do sedimento a zona de produccedilatildeo (nitrificaccedilatildeo) e a de consumo (desnitrificaccedilatildeo) do composto enfatizando sua importacircncia para o processo
TEMPERATURA
A temperatura eacute um fator abioacutetico que regula o metabolismo de organismos vivos em geral e consequentemente tambeacutem regula a intensidade e ocorrecircncia de processos microbianos Os microrganismos tecircm seu metabolismo afetado visto que existe um oacutetimo de temperatura para
Figura 4 Perfil de O2 () e NO3- () e faixas de atividades microbianas do ciclo do N sob condiccedilotildees de iluminaccedilatildeo em diferentes aacutereas do sedimento
lacustre assimilaccedilatildeo de NO3- (preto do topo) nitrificaccedilatildeo (cinza claro) e desnitrificaccedilatildeo (preto de baixo) Os valores de O2 e NO3
- satildeo meacutedia plusmn DP n=6 (adaptada de Lorenzen et al 1998)
Figure 4 Profile of O2 () and NO3- () and depths of microbial activities of N cycling under light condition in different areas of sediment from lakes
assimilation of NO3- (black top) nitrification (light gray) and denitrification (black low) The values of O2 and NO3
- are mean plusmn SD n=6 (adapted from Lorenzen et al 1998)
o funcionamento fisioloacutegico bacteriano (Saad amp Conrad 1993 Pilegaard et al 2006) Temperaturas mais elevadas estimulam o metabolismo o que faz com que as taxas de nitrificaccedilatildeo e tambeacutem de desnitrificaccedilatildeo aumentem ateacute seu oacutetimo metaboacutelico (Schimel amp Gulledge 1998) com maacutexima produccedilatildeo de NO3
- acompanhada pelos seus subprodutos incluindo o N2O (Godde amp Conrad 1999)
O controle desempenhado pela temperatura onde geralmente encontramos uma relaccedilatildeo positiva foi confirmado no experimento de Godde amp Conrad (1999) em solo com temperatura controlada (Figura 5) Estes autores demonstraram que tanto a nitrificaccedilatildeo quanto a desnitrificaccedilatildeo sofrem alteraccedilotildees em suas taxas quando a temperatura eacute alterada (Malhi et al 1990 Saad amp Conrad 1993)
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Figura 6 Taxas de produccedilatildeo potencial de N2O determinada pela atividade da enzima desnitrificante As temperaturas de incubaccedilatildeo foram 4 15 20 25 e 37degC durante 20 dias Os dados satildeo meacutedia plusmn EP n=2 (adaptada de Braker et al 2010)
Figure 6 Rates of potential production of N2O determined by denitrifying enzyme activity The incubation temperatures were 4 15 20 25 and 37degC during 20 days Data are mean plusmn SE n=2 (adapted from Braker et al 2010)
Braker et al (2010) verificaram diretamente a influecircncia da temperatura sobre a produccedilatildeo de N2O em solos agriacutecolas corroborando a hipoacutetese de que a temperatura influencia a fisiologia das bacteacuterias desnitrificantes com o aquecimento do ambiente as taxas metaboacutelicas se mostram elevadas produzindo mais N2O ateacute um oacutetimo de temperatura (Figura 6) Embora este resultado tenha sido obtido em solos natildeo eacute de nosso conhecimento um experimento semelhante em sedimento de ambientes aquaacuteticos poreacutem o resultado esperado seria semelhante uma vez que essa regulaccedilatildeo metaboacutelica independe do tipo de sistema
O valor de temperatura oacutetimo para as bacteacuterias nitrificantes e desnitrificantes varia de 25deg a 35degC sendo registradas nessa faixa de temperatura as maiores taxas de atividade (Saad amp Conrad 1993 Braker et al 2010) Entretanto em muitos ambientes onde a temperatura natildeo eacute ideal alcanccedilando valores consideravelmente abaixo ou acima do oacutetimo verificamos a ocorrecircncia de atividade microbiana o que estaacute relacionado agrave capacidade de adaptaccedilatildeo dos microrganismos da comunidade ecoloacutegica em questatildeo a ambientes diferentes do ideal (Saad amp Conrad 1993)
pH
O potencial hidrogeniocircnico (pH) eacute um paracircmetro ambiental crucial para os processos do ciclo do N
atuando por exemplo na proporccedilatildeo NH3NH4+ na
aacutegua Em pH aacutecido ocorre a predominacircncia de NH4+
em detrimento de NH3 ocorrendo o inverso em pH alcalino (De Boer amp Kowalchuk 2001 Bajwa et al 2006) O controle exercido pelo pH sobre a produccedilatildeo de N2O (Conrad 1996 Enwall et al 2005) reflete-se indiretamente atraveacutes do efeito do pH sobre a comunidade bacteriana que pode regular a abundacircncia e diversidade dos microorganismos (Enwall et al 2005)
Como as bacteacuterias nitrificantes tecircm preferecircncia por assimilar NH3 em detrimento do NH4
+ a nitrificaccedilatildeo apresenta taxas mais elevadas em ambientes alcalinos (Kowalchuk amp Stephen 2001 Nugroho et al 2007) Sua influecircncia sobre a produccedilatildeo de N2O pela oxidaccedilatildeo aeroacutebica da amocircnia ainda eacute discutida na literatura devido agrave variaccedilatildeo de dados encontrados (Moslashrkved et al 2007) O processo de nitrificaccedilatildeo heterotroacutefica apresenta alta produccedilatildeo de N2O em pH aacutecido mas natildeo haacute muitos estudos sobre esse processo e sua relaccedilatildeo com o pH (Moslashrkved et al 2007)
O pH tambeacutem atua diretamente sobre as enzimas desnitrificantes oacutexido nitroso redutases que reduz N2O a N2 (Tiedje 1988) cuja atividade aumenta com o aumento do pH do ambiente ateacute alcanccedilar o seu oacutetimo Quando o pH do ambiente eacute baixo a produccedilatildeo da enzima diminui podendo chegar a ficar inativa ocasionando uma elevada produccedilatildeo de N2O (Aumleuhel amp Aringimek 2011) Na medida em que o pH
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aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
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em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
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N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
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Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
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VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
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Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
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RESUMENOacuteXIDO NITROSO (N2O) EN AMBIENTES ACUAacuteTICOS PRODUCCIOacuteN FACTORES
REGULADORES Y FLUJOS DE DIFERENTES AMBIENTES El oacutexido nitroso (N2O) es uno de los tres principales gases de efecto invernadero ademaacutes se manifiesta como el principal gas destructor de la capa de ozono en este siglo Este gas es producido naturalmente a traveacutes de los procesos de nitrificacioacuten y desnitrificacioacuten en ambientes acuaacuteticos y terrestres Las tasas de emisioacuten de N2O han sido ampliamente estudiadas en ecosistemas terrestres pero comparativamente han sido olvidadas en los ecosistemas de agua dulce a pesar del reciente reconocimiento de la importancia de estos ambientes en los ciclos globales de carbono y nitroacutegeno El objetivo de este estudio fue presentar los factores de regulacioacuten principales en la produccioacuten de N2O a traveacutes de los procesos de nitrificacioacuten y desnitrificacion en los lagos embalses riacuteos manglares y estuarios Las tasas de emisioacuten de N2O en tales ambientes exhiben grandes diferencias entre siacute variando en hasta cuatro oacuterdenes de magnitud Los mayores valores de flujo de N2O fueron observados en los estuarios manglares y riacuteos Los lagos y embalses son ambientes maacutes estables que los manglares estuarios y riacuteos y esta caracteriacutestica hace que la variabilidad de factores tales como el pH y las concentraciones de nutrientes sea inferior favoreciendo una mayor estabilidad de los procesos y en consecuencia una menor produccioacuten y emisioacuten de N2O dado que este gas deriva de las alteraciones ambientales Palabras clave oacutexido nitroso nitrificacioacuten desnitrificacioacuten factores reguladores ambientes acuaacuteticos continentales
INTRODUCcedilAtildeO
Eacute amplamente aceito que uma das principais causas das mudanccedilas climaacuteticas eacute o aumento da concentraccedilatildeo atmosfeacuterica de gases estufa como dioacutexido de carbono (CO2) metano (CH4) e oacutexido nitroso (N2O) (IPCC 2001) Apesar do CO2 estar em maior concentraccedilatildeo o N2O apresenta maior tempo de residecircncia na atmosfera aproximadamente 120 anos e eacute 310 vezes mais potente na retenccedilatildeo de radiaccedilatildeo infravermelha (IPCC 2001) que ocorre na troposfera onde o gaacutes fica acumulado Essa propriedade de absorver radiaccedilatildeo de ondas de comprimentos longos como a radiaccedilatildeo infravermelha confere ao N2O a capacidade de elevar a temperatura da atmosfera e consequentemente da Terra (Braker amp Conrad 2011) contribuindo com aproximadamente 6 do aquecimento adicional do planeta (Werner et al 2007)
Outra caracteriacutestica relevante do N2O eacute a similaridade deste gaacutes com os CloroFluorCarbonetos (CFCs) Quando presentes nas camadas atmosfeacutericas ambos os compostos satildeo estaacuteveis na troposfera mas instaacuteveis na estratosfera e assim portanto causando a liberaccedilatildeo de ativos quiacutemicos tal como o oacutexido niacutetrico (NO) que reagem com o ozocircnio da camada de ozocircnio causando sua destruiccedilatildeo cataliacutetica (Ravishankara et al 2009) Essa camada protege a Terra dos raios
UV e tem sido continuamente destruiacuteda o que agrava as chamadas mudanccedilas climaacuteticas (IPCC 2007) Atualmente o N2O tem sido considerado a principal substacircncia emitida destruidora do ozocircnio uma vez que os CFCs tecircm suas emissotildees fortemente controladas (Ravishankara et al 2009) De 1750 ateacute hoje as concentraccedilotildees atmosfeacutericas de N2O vecircm aumentando (Figura 1) com um acreacutescimo de aproximadamente 18 desde a era preacute-industrial quando sua concentraccedilatildeo era de cerca de 270ppb chegando a 319ppb em 2000 (Forster et al 2007)
Figura 1 Mudanccedilas nas concentraccedilotildees atmosfeacutericas de N2O de 1000 ateacute 2000 DC verificadas atraveacutes de testemunhos de gelo Eixo esquerdo concentraccedilotildees atmosfeacutericas de N2O (ppb) Eixo direito forccedila radiativa do
N2O atmosfeacuterico (adaptada de IPCC 2001)Figure 1 Changes in atmospheric concentrations of N2O form 1000 to 2000 AC verified by ice cores Left axis atmospheric concentrations of N2O (ppb) Right axis radioactive forcing of atmospheric N2O (adapted
from IPCC 2001)
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PROCESSOS FORMADORES DE N2O
A produccedilatildeo e consumo de N2O em ambientes aquaacuteticos continentais estatildeo diretamente associados aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Figura 2) Estes processos ocorrem em vaacuterios compartimentos dos ecossistemas aquaacuteticos como aacutegua solo sedimento perifiacuteton rizosfera de plantas aquaacuteticas ou algas Esses diferentes compartimentos apresentam distintas condiccedilotildees ambientais que afetam a composiccedilatildeo da comunidade microbiana e tambeacutem influenciam o seu potencial nitrificante e desnitrificante (Bastviken et al 2003)
Diante dessa variabilidade de fatores reguladores destaca-se a produccedilatildeo de N2O em virtude do acoplamento nitrificaccedilatildeo-desnitrificaccedilatildeo visto que o primeiro processo subsidia com seu produto final o segundo processo (Kremen et al 2005) Com isso as bacteacuterias desnitrificantes conseguem fazer uso do composto necessaacuterio advindo de uma via externa (desnitrificaccedilatildeo direta) ou interna (nitrificaccedilatildeo-desnitrificaccedilatildeo acoplada) o que pode aumenta o potencial desnitrificante do ambiente (Fennel et al 2009) Diversos estudos satildeo desenvolvidos visando identificar esse acoplamento dos processos atraveacutes do uso de isoacutetopos estaacuteveis que podem rastrear a origem dos compostos e verificar assim a contribuiccedilatildeo externa e interna na produccedilatildeo de gases nitrogenados (Nicolaisen et al 2004)
Figura 2 Ciclo do nitrogecircnio em ecossistemas aquaacuteticos continentais Em destaque os principais processos bacterianos envolvidos na emissatildeo
de N2O (adaptada de Santoro amp Enrich-Prast 2011)Figure 2 Nitrogen cycle in continental aquatic ecosystems Highlights the main bacterial processes involved in the emission of N2O (adapted
from Santoro amp Enrich-Prast 2011)
NITRIFICACcedilAtildeO
A nitrificaccedilatildeo autotroacutefica eacute um processo microbiano realizado por dois grupos de bacteacuterias quimiolitoautotroacuteficas (Nitrosospira e Nitrosomonas) bacteacuterias que obteacutem energia atraveacutes da oxidaccedilatildeo de compostos inorgacircnicos (Fiencke et al 2006) Esse processo do ciclo do N (Figura 2) se resume agrave oxidaccedilatildeo da amocircnia (NH3) a nitrito (NO2
-) e deste finalmente a nitrato (NO3
-) Esse processo eacute estritamente aeroacutebico ocorrendo obrigatoriamente na porccedilatildeo oacutexica de compartimentos como a aacutegua superfiacutecie do sedimento e solo ou no entorno de raiacutezes submersas (Reddy et al 1989) A formaccedilatildeo de N2O por esse tipo de nitrificaccedilatildeo pode ocorrer durante a oxidaccedilatildeo da NH3 a NO2
- (Frame amp Casciotti 2010) Entretanto sua produccedilatildeo eacute mais reduzida do que a quantidade do NO2
- produzido (Arp amp Stein 2003) e depende de caracteriacutesticas do ambiente (Schmidt et al 2001) Um fator crucial para a produccedilatildeo de N2O eacute a diminuiccedilatildeo das concentraccedilotildees de oxigecircnio disponiacuteveis durante o processo de nitrificaccedilatildeo uma vez que a reaccedilatildeo ocorre de maneira incompleta formando NO ou N2O ao inveacutes de formar NO2
- (Anderson et al 1993) O oacutexido de nitrogecircnio produzido tambeacutem seraacute regulado pela umidade do solo no momento das reaccedilotildees (Davidson et al 1993)
A nitrificaccedilatildeo heterotroacutefica eacute realizada por bacteacuterias fungos e algas que assim como na nitrificaccedilatildeo autotroacutefica oxidam a amocircnia a nitrato sob condiccedilotildees aeroacutebicas e tambeacutem produzem N2O (Hayatsu et al 2008) Entretanto por ser um processo heterotroacutefico natildeo haacute geraccedilatildeo de energia o que torna esses organismos dependentes de substratos orgacircnicos para obtenccedilatildeo de energia Aleacutem disso as taxas da desnitrificaccedilatildeo heterotroacutefica satildeo mais baixas que da nitrificaccedilatildeo autotroacutefica indicando uma reduzida contribuiccedilatildeo desse processo nitrogenado (Fiencke et al 2006)
Um terceiro tipo de nitrificaccedilatildeo eacute a desnitrificaccedilatildeo nitrificante uma das vias da nitrificaccedilatildeo realizada por um uacutenico grupo de bacteacuterias chamadas autotroacuteficas oxidadoras de NH3 (Wrage et al 2001) Nessa via ocorre a oxidaccedilatildeo de NH3 a NO2
- como na nitrificaccedilatildeo e posteriormente ocorre a reduccedilatildeo do NO2
- a N2ON2 como na desnitrificaccedilatildeo (Wrage et al 2001) Entretanto assim como a nitrificaccedilatildeo heterotroacutefica a
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desnitrificaccedilatildeo nitrificante eacute menos estudada e ateacute o momento sabe-se apenas que a contribuiccedilatildeo de ambos os processos na produccedilatildeo de N2O varia de acordo com fatores bioloacutegicos e fiacutesicos do solo (Kool et al 2011) A pequena quantidade de informaccedilotildees sobre estes processos indica que estes precisam ser melhor quantificados nas diversas regiotildees do nosso planeta
Indiscutivelmente o principal preacute-requisito para que a nitrificaccedilatildeo ocorra eacute a disponibilidade de NH3NH4
+ o substrato nitrogenado baacutesico para ocorrecircncia desse processo Uma das principais fontes desses compostos nos ecossistemas aquaacuteticos e terrestres eacute a degradaccedilatildeo de mateacuteria orgacircnica laacutebil que libera diferentes compostos como nitrogecircnio orgacircnico NH3 NO2
- NO3- e fosfato (Balota amp Auler 2011)
Derivado dessa mineralizaccedilatildeo a NH3 eacute uma fonte de nitrogecircnio extremamente laacutebil e de faacutecil assimilaccedilatildeo pelos vaacuterios tipos de macro e micro-organismos o que muitas vezes torna esse composto limitante no ambiente (Sasaki et al 2002 Schmidt et al 2011) Excretas nitrogenados advindos de organismos heterotroacuteficos tambeacutem satildeo uma importante fonte de NH3NH4
+As concentraccedilotildees relativas de NH3 e NH4
+ na aacutegua satildeo dependentes principalmente do pH da aacutegua Reconhecidamente na maioria dos ambientes a forma nitrogenada predominante eacute o NH4
+ jaacute que a forma NH3 gasosa eacute dominante apenas entre pH 8-10 (Johnson et al 2008) valores estes menos frequentes nos sistemas aquaacuteticos Entretanto eacute nessa faixa de pH alcalino que a NH3 estaacute na fase gasosa e eacute liberada em maior quantidade para a atmosfera atraveacutes da volatilizaccedilatildeo (Jayaweera amp Mikkelsen 1991 Bajwa et al 2006 Fiencke et al 2006 Haden et al 2011) Logo sua assimilaccedilatildeo bem como a volatilizaccedilatildeo indisponibilizam o nitrogecircnio para o processo nitrificante reduzindo as taxas de desnitrificaccedilatildeo e consequentemente a produccedilatildeo de N2O
Desnitrificaccedilatildeo
A desnitrificaccedilatildeo eacute um processo bacteriano anaeroacutebico facultativo de degradaccedilatildeo da mateacuteria orgacircnica que em ausecircncia de oxigecircnio utiliza o NO3
- como receptor de eleacutetrons reduzindo-o agrave N2 Esse processo ocorre no sedimento e na coluna drsquoaacutegua estratificada imediatamente abaixo da zona oacutexica devido agrave formaccedilatildeo de NO3
- via nitrificaccedilatildeo
ou utilizando o substrato que tenha sido formado em outro ambiente (Kuschk et al 2003) Produtos intermediaacuterios do processo de desnitrificaccedilatildeo o NO e o N2O podem ser emitidos para a atmosfera A principal forma de perda de nitrogecircnio disponiacutevel no ambiente eacute atraveacutes do processo de desnitrificaccedilatildeo (Fennel et al 2009) onde os produtos intermediaacuterio eou finais (NO N2O e N2) satildeo gasosos e podem ser difundidos para a atmosfera tornando o nitrogecircnio um elemento limitante para outros organismos no ambiente (Seitzinger 1988 Harrison et al 2005)
Em ambientes eutrofizados como rios lagos e solos agriacutecolas com excesso de nutrientes a desnitrificaccedilatildeo acaba por reduzir a quantidade de compostos nitrogenados diminuindo a eutrofizaccedilatildeo dos ecossistemas bem como a lixiviaccedilatildeo do nitrogecircnio para outros ecossistemas (Seitzinger 1988 Seitzinger et al 2006) Por outro lado esse eacute o principal processo microbiano produtor de N2O agravando problemas como o aquecimento global e a destruiccedilatildeo da camada de ozocircnio Alteraccedilotildees da quantidade de N2O emitido ocorrem com frequumlecircncia devido a modificaccedilotildees bruscas das condiccedilotildees oacutexica-anoacutexica de solos e sedimentos e das concentraccedilotildees de NH3 e de NO2
- (Kampschreur et al 2009) Com isso ecossistemas aquaacuteticos ou ambientes terrestres sujeitos a influecircncia de aporte de aacuteguas satildeo fontes potencias na emissatildeo de N2O (Scott et al 2008) Segundo Kool et al (2011) a desnitrificaccedilatildeo eacute o principal processo formador de N2O embora a nitrificaccedilatildeo tambeacutem seja representativa em alguns tipos de solo
O NO3- eacute o principal substrato limitante para
a desnitrificaccedilatildeo e sua disponibilidade no meio eacute variaacutevel e dependente de diversos aspectos sendo um deles o tipo de solo que pode reter esse acircnion (Barrett amp Burke 2002) Entretanto esse mecanismo abioacutetico ainda eacute pouco estudado (Berntson amp Aber 2000 Zhu amp Wang 2011) e resume-se a adsorccedilatildeo do NO3
- a partiacuteculas do solo imobilizando esse importante nutriente nitrogenado e podendo ateacute tornaacute-lo limitante aos organismos de acordo com o estado troacutefico do ambiente (Bernot amp Dodds 2005)
FATORES REGULADORES DA PRODUCcedilAtildeO DE N2O
Os processos de nitrificaccedilatildeo e de desnitrificaccedilatildeo demandam disponibilidade de amocircnia e nitrato (NH3
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e NO3-) no ambiente Entretanto essa disponibilidade
eacute alterada em funccedilatildeo de vaacuterios fatores reguladores como concentraccedilotildees de oxigecircnio e mateacuteria orgacircnica temperatura pH umidade (Darrouzet-Nardi amp Bowman 1988 Seitzinger 1988 Miller et al 2009 Ross amp Wemple 2011) topografia (John et al 2007) e tambeacutem competiccedilatildeo entre as bacteacuterias do ciclo do nitrogecircnio e destas com outros micro-organismos e plantas (Inselsbacher et al 2010) Tais fatores bioacuteticos e abioacuteticos satildeo relevantes pois afetam principalmente a atividade e o crescimento microbiano (Mamilov amp Dilly 2002) Fatores reguladores podem variar espaccedilo-temporalmente afetando a produccedilatildeo de oacutexido nitroso que por estar associada aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Perez et al 2006 Farquharson amp Baldock 2008 Ma et al 2008) pode variar nessa mesma escala (McClain et al 2003) A seguir apresentamos e descrevemos os principais fatores reguladores da nitrificaccedilatildeo e da desnitrificaccedilatildeo
OXIGEcircNIO
Sendo a nitrificaccedilatildeo um processo estritamente aeroacutebico a presenccedila de oxigecircnio eacute um dos seus principais fatores reguladores (Bollmann amp Conrad 1998) Na Figura 3 observa-se a taxa de nitrificaccedilatildeo aumentar concomitantemente com a pressatildeo parcial de oxigecircnio em um solo agriacutecola ressaltando a influecircncia da disponibilidade de oxigecircnio sobre esse processo (Bollmann amp Conrad 1998) A disponibilidade de O2 pode ser totalmente alterada em funccedilatildeo da presenccedila de aacutegua no solo que ocupa o espaccedilo do oxigecircnio e restringe a velocidade da sua difusatildeo (Tiedje 1988)
Sedimentos de ambientes lagunares muitas vezes tecircm uma miacutenima camada superficial oacutexica que pode variar com a profundidade do lago Desta maneira deve-se ressaltar a importacircncia da presenccedila de micro-organismos fotossintetizantes em sedimentos de ambientes aquaacuteticos aumentando a oxigenaccedilatildeo e penetraccedilatildeo de O2 nas camadas mais profundas e possibilitando a ocorrecircncia da oxidaccedilatildeo da amocircnia em outras faixas do sedimento (Lorenzen et al 1998) (Figura 4) De maneira semelhante aos fotossintetizantes as raiacutezes de plantas em sistemas aquaacuteticos proporcionam a difusatildeo de oxigecircnio das raiacutezes para zonas anoacutexicas do sedimento criando microambientes oxigenados e permitindo que a nitrificaccedilatildeo ocorra e subsidie a desnitrificaccedilatildeo atraveacutes
do acoplamento dos processos (Reddy et al 1989 Ottosen et al 1999)
Solos expostos satildeo ambientes com grande oxigenaccedilatildeo dependentes de eventos de alagamento e do tipo de agregaccedilatildeo das partiacuteculas que compotildeem o solo Logo satildeo ambientes com elevado potencial nitrificante e tambeacutem de produccedilatildeo N2O Isso porque uma vez que o solo eacute molhado a disponibilidade de oxigecircnio diminui progressivamente e a nitrificaccedilatildeo ocorre de maneira incompleta produzindo NO ou N2O (Davidson et al 1993)
Figura 3 Influecircncia da pressatildeo parcial de O2 sobre a mineralizaccedilatildeo de nitrogecircnio () e sobre a nitrificaccedilatildeo () em um solo agriacutecola de Timmerlah (Alemanha meacutedia plusmn DP n=3 adaptado de Bollmann and Conrad 1998)Figure 3 Influence of partial pressure of O2 on mineralization of nitrogen () and on nitrification () on an agricultural soil of Timmerlah (Germany mean plusmn DP n=3 adapted from Bollmann and Conrad 1998)
Realizada por bacteacuterias facultativas a desnitrificaccedilatildeo natildeo ocorre em locais com alta concentraccedilatildeo de oxigecircnio pois os micro-organismos datildeo prioridade para a respiraccedilatildeo aeroacutebica mais favoraacutevel energeticamente Isso torna a presenccedila de oxigecircnio um fator regulador de grande relevacircncia (Bollmann amp Conrad 1998 Morley amp Baggs 2010) Diante dessa importacircncia encontramos um maior nuacutemero de registros de desnitrificaccedilatildeo em ambientes com baixa concentraccedilatildeo ou completa ausecircncia de oxigenaccedilatildeo como eacute o caso do sedimento de lagos planiacutecies de inundaccedilatildeo ou quaisquer aacutereas cobertas por aacutegua de pouca turbulecircncia Solos tambeacutem tecircm alto potencial desnitrificante devido agrave ocorrecircncia de chuvas que os tornam temporariamente anoacutexicos ou com baixa oxigenaccedilatildeo Um bom exemplo da regulaccedilatildeo do oxigecircnio sobre a desnitrificaccedilatildeo (Figura 4) ocorre na zona onde o oxigecircnio estaacute ausente (Lorenzen et al 1998) Aleacutem do oxigecircnio observa-se a influecircncia direta do NO3
- sobre as taxas
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de desnitrificaccedilatildeo onde este composto eacute o principal substrato desse processo sendo entatildeo considerado seu principal fator regulador Dessa forma identificamos atraveacutes do perfil de concentraccedilatildeo de NO3
- na camada superficial do sedimento a zona de produccedilatildeo (nitrificaccedilatildeo) e a de consumo (desnitrificaccedilatildeo) do composto enfatizando sua importacircncia para o processo
TEMPERATURA
A temperatura eacute um fator abioacutetico que regula o metabolismo de organismos vivos em geral e consequentemente tambeacutem regula a intensidade e ocorrecircncia de processos microbianos Os microrganismos tecircm seu metabolismo afetado visto que existe um oacutetimo de temperatura para
Figura 4 Perfil de O2 () e NO3- () e faixas de atividades microbianas do ciclo do N sob condiccedilotildees de iluminaccedilatildeo em diferentes aacutereas do sedimento
lacustre assimilaccedilatildeo de NO3- (preto do topo) nitrificaccedilatildeo (cinza claro) e desnitrificaccedilatildeo (preto de baixo) Os valores de O2 e NO3
- satildeo meacutedia plusmn DP n=6 (adaptada de Lorenzen et al 1998)
Figure 4 Profile of O2 () and NO3- () and depths of microbial activities of N cycling under light condition in different areas of sediment from lakes
assimilation of NO3- (black top) nitrification (light gray) and denitrification (black low) The values of O2 and NO3
- are mean plusmn SD n=6 (adapted from Lorenzen et al 1998)
o funcionamento fisioloacutegico bacteriano (Saad amp Conrad 1993 Pilegaard et al 2006) Temperaturas mais elevadas estimulam o metabolismo o que faz com que as taxas de nitrificaccedilatildeo e tambeacutem de desnitrificaccedilatildeo aumentem ateacute seu oacutetimo metaboacutelico (Schimel amp Gulledge 1998) com maacutexima produccedilatildeo de NO3
- acompanhada pelos seus subprodutos incluindo o N2O (Godde amp Conrad 1999)
O controle desempenhado pela temperatura onde geralmente encontramos uma relaccedilatildeo positiva foi confirmado no experimento de Godde amp Conrad (1999) em solo com temperatura controlada (Figura 5) Estes autores demonstraram que tanto a nitrificaccedilatildeo quanto a desnitrificaccedilatildeo sofrem alteraccedilotildees em suas taxas quando a temperatura eacute alterada (Malhi et al 1990 Saad amp Conrad 1993)
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Figura 6 Taxas de produccedilatildeo potencial de N2O determinada pela atividade da enzima desnitrificante As temperaturas de incubaccedilatildeo foram 4 15 20 25 e 37degC durante 20 dias Os dados satildeo meacutedia plusmn EP n=2 (adaptada de Braker et al 2010)
Figure 6 Rates of potential production of N2O determined by denitrifying enzyme activity The incubation temperatures were 4 15 20 25 and 37degC during 20 days Data are mean plusmn SE n=2 (adapted from Braker et al 2010)
Braker et al (2010) verificaram diretamente a influecircncia da temperatura sobre a produccedilatildeo de N2O em solos agriacutecolas corroborando a hipoacutetese de que a temperatura influencia a fisiologia das bacteacuterias desnitrificantes com o aquecimento do ambiente as taxas metaboacutelicas se mostram elevadas produzindo mais N2O ateacute um oacutetimo de temperatura (Figura 6) Embora este resultado tenha sido obtido em solos natildeo eacute de nosso conhecimento um experimento semelhante em sedimento de ambientes aquaacuteticos poreacutem o resultado esperado seria semelhante uma vez que essa regulaccedilatildeo metaboacutelica independe do tipo de sistema
O valor de temperatura oacutetimo para as bacteacuterias nitrificantes e desnitrificantes varia de 25deg a 35degC sendo registradas nessa faixa de temperatura as maiores taxas de atividade (Saad amp Conrad 1993 Braker et al 2010) Entretanto em muitos ambientes onde a temperatura natildeo eacute ideal alcanccedilando valores consideravelmente abaixo ou acima do oacutetimo verificamos a ocorrecircncia de atividade microbiana o que estaacute relacionado agrave capacidade de adaptaccedilatildeo dos microrganismos da comunidade ecoloacutegica em questatildeo a ambientes diferentes do ideal (Saad amp Conrad 1993)
pH
O potencial hidrogeniocircnico (pH) eacute um paracircmetro ambiental crucial para os processos do ciclo do N
atuando por exemplo na proporccedilatildeo NH3NH4+ na
aacutegua Em pH aacutecido ocorre a predominacircncia de NH4+
em detrimento de NH3 ocorrendo o inverso em pH alcalino (De Boer amp Kowalchuk 2001 Bajwa et al 2006) O controle exercido pelo pH sobre a produccedilatildeo de N2O (Conrad 1996 Enwall et al 2005) reflete-se indiretamente atraveacutes do efeito do pH sobre a comunidade bacteriana que pode regular a abundacircncia e diversidade dos microorganismos (Enwall et al 2005)
Como as bacteacuterias nitrificantes tecircm preferecircncia por assimilar NH3 em detrimento do NH4
+ a nitrificaccedilatildeo apresenta taxas mais elevadas em ambientes alcalinos (Kowalchuk amp Stephen 2001 Nugroho et al 2007) Sua influecircncia sobre a produccedilatildeo de N2O pela oxidaccedilatildeo aeroacutebica da amocircnia ainda eacute discutida na literatura devido agrave variaccedilatildeo de dados encontrados (Moslashrkved et al 2007) O processo de nitrificaccedilatildeo heterotroacutefica apresenta alta produccedilatildeo de N2O em pH aacutecido mas natildeo haacute muitos estudos sobre esse processo e sua relaccedilatildeo com o pH (Moslashrkved et al 2007)
O pH tambeacutem atua diretamente sobre as enzimas desnitrificantes oacutexido nitroso redutases que reduz N2O a N2 (Tiedje 1988) cuja atividade aumenta com o aumento do pH do ambiente ateacute alcanccedilar o seu oacutetimo Quando o pH do ambiente eacute baixo a produccedilatildeo da enzima diminui podendo chegar a ficar inativa ocasionando uma elevada produccedilatildeo de N2O (Aumleuhel amp Aringimek 2011) Na medida em que o pH
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aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
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em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
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N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
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Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
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VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
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Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
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PROCESSOS FORMADORES DE N2O
A produccedilatildeo e consumo de N2O em ambientes aquaacuteticos continentais estatildeo diretamente associados aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Figura 2) Estes processos ocorrem em vaacuterios compartimentos dos ecossistemas aquaacuteticos como aacutegua solo sedimento perifiacuteton rizosfera de plantas aquaacuteticas ou algas Esses diferentes compartimentos apresentam distintas condiccedilotildees ambientais que afetam a composiccedilatildeo da comunidade microbiana e tambeacutem influenciam o seu potencial nitrificante e desnitrificante (Bastviken et al 2003)
Diante dessa variabilidade de fatores reguladores destaca-se a produccedilatildeo de N2O em virtude do acoplamento nitrificaccedilatildeo-desnitrificaccedilatildeo visto que o primeiro processo subsidia com seu produto final o segundo processo (Kremen et al 2005) Com isso as bacteacuterias desnitrificantes conseguem fazer uso do composto necessaacuterio advindo de uma via externa (desnitrificaccedilatildeo direta) ou interna (nitrificaccedilatildeo-desnitrificaccedilatildeo acoplada) o que pode aumenta o potencial desnitrificante do ambiente (Fennel et al 2009) Diversos estudos satildeo desenvolvidos visando identificar esse acoplamento dos processos atraveacutes do uso de isoacutetopos estaacuteveis que podem rastrear a origem dos compostos e verificar assim a contribuiccedilatildeo externa e interna na produccedilatildeo de gases nitrogenados (Nicolaisen et al 2004)
Figura 2 Ciclo do nitrogecircnio em ecossistemas aquaacuteticos continentais Em destaque os principais processos bacterianos envolvidos na emissatildeo
de N2O (adaptada de Santoro amp Enrich-Prast 2011)Figure 2 Nitrogen cycle in continental aquatic ecosystems Highlights the main bacterial processes involved in the emission of N2O (adapted
from Santoro amp Enrich-Prast 2011)
NITRIFICACcedilAtildeO
A nitrificaccedilatildeo autotroacutefica eacute um processo microbiano realizado por dois grupos de bacteacuterias quimiolitoautotroacuteficas (Nitrosospira e Nitrosomonas) bacteacuterias que obteacutem energia atraveacutes da oxidaccedilatildeo de compostos inorgacircnicos (Fiencke et al 2006) Esse processo do ciclo do N (Figura 2) se resume agrave oxidaccedilatildeo da amocircnia (NH3) a nitrito (NO2
-) e deste finalmente a nitrato (NO3
-) Esse processo eacute estritamente aeroacutebico ocorrendo obrigatoriamente na porccedilatildeo oacutexica de compartimentos como a aacutegua superfiacutecie do sedimento e solo ou no entorno de raiacutezes submersas (Reddy et al 1989) A formaccedilatildeo de N2O por esse tipo de nitrificaccedilatildeo pode ocorrer durante a oxidaccedilatildeo da NH3 a NO2
- (Frame amp Casciotti 2010) Entretanto sua produccedilatildeo eacute mais reduzida do que a quantidade do NO2
- produzido (Arp amp Stein 2003) e depende de caracteriacutesticas do ambiente (Schmidt et al 2001) Um fator crucial para a produccedilatildeo de N2O eacute a diminuiccedilatildeo das concentraccedilotildees de oxigecircnio disponiacuteveis durante o processo de nitrificaccedilatildeo uma vez que a reaccedilatildeo ocorre de maneira incompleta formando NO ou N2O ao inveacutes de formar NO2
- (Anderson et al 1993) O oacutexido de nitrogecircnio produzido tambeacutem seraacute regulado pela umidade do solo no momento das reaccedilotildees (Davidson et al 1993)
A nitrificaccedilatildeo heterotroacutefica eacute realizada por bacteacuterias fungos e algas que assim como na nitrificaccedilatildeo autotroacutefica oxidam a amocircnia a nitrato sob condiccedilotildees aeroacutebicas e tambeacutem produzem N2O (Hayatsu et al 2008) Entretanto por ser um processo heterotroacutefico natildeo haacute geraccedilatildeo de energia o que torna esses organismos dependentes de substratos orgacircnicos para obtenccedilatildeo de energia Aleacutem disso as taxas da desnitrificaccedilatildeo heterotroacutefica satildeo mais baixas que da nitrificaccedilatildeo autotroacutefica indicando uma reduzida contribuiccedilatildeo desse processo nitrogenado (Fiencke et al 2006)
Um terceiro tipo de nitrificaccedilatildeo eacute a desnitrificaccedilatildeo nitrificante uma das vias da nitrificaccedilatildeo realizada por um uacutenico grupo de bacteacuterias chamadas autotroacuteficas oxidadoras de NH3 (Wrage et al 2001) Nessa via ocorre a oxidaccedilatildeo de NH3 a NO2
- como na nitrificaccedilatildeo e posteriormente ocorre a reduccedilatildeo do NO2
- a N2ON2 como na desnitrificaccedilatildeo (Wrage et al 2001) Entretanto assim como a nitrificaccedilatildeo heterotroacutefica a
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desnitrificaccedilatildeo nitrificante eacute menos estudada e ateacute o momento sabe-se apenas que a contribuiccedilatildeo de ambos os processos na produccedilatildeo de N2O varia de acordo com fatores bioloacutegicos e fiacutesicos do solo (Kool et al 2011) A pequena quantidade de informaccedilotildees sobre estes processos indica que estes precisam ser melhor quantificados nas diversas regiotildees do nosso planeta
Indiscutivelmente o principal preacute-requisito para que a nitrificaccedilatildeo ocorra eacute a disponibilidade de NH3NH4
+ o substrato nitrogenado baacutesico para ocorrecircncia desse processo Uma das principais fontes desses compostos nos ecossistemas aquaacuteticos e terrestres eacute a degradaccedilatildeo de mateacuteria orgacircnica laacutebil que libera diferentes compostos como nitrogecircnio orgacircnico NH3 NO2
- NO3- e fosfato (Balota amp Auler 2011)
Derivado dessa mineralizaccedilatildeo a NH3 eacute uma fonte de nitrogecircnio extremamente laacutebil e de faacutecil assimilaccedilatildeo pelos vaacuterios tipos de macro e micro-organismos o que muitas vezes torna esse composto limitante no ambiente (Sasaki et al 2002 Schmidt et al 2011) Excretas nitrogenados advindos de organismos heterotroacuteficos tambeacutem satildeo uma importante fonte de NH3NH4
+As concentraccedilotildees relativas de NH3 e NH4
+ na aacutegua satildeo dependentes principalmente do pH da aacutegua Reconhecidamente na maioria dos ambientes a forma nitrogenada predominante eacute o NH4
+ jaacute que a forma NH3 gasosa eacute dominante apenas entre pH 8-10 (Johnson et al 2008) valores estes menos frequentes nos sistemas aquaacuteticos Entretanto eacute nessa faixa de pH alcalino que a NH3 estaacute na fase gasosa e eacute liberada em maior quantidade para a atmosfera atraveacutes da volatilizaccedilatildeo (Jayaweera amp Mikkelsen 1991 Bajwa et al 2006 Fiencke et al 2006 Haden et al 2011) Logo sua assimilaccedilatildeo bem como a volatilizaccedilatildeo indisponibilizam o nitrogecircnio para o processo nitrificante reduzindo as taxas de desnitrificaccedilatildeo e consequentemente a produccedilatildeo de N2O
Desnitrificaccedilatildeo
A desnitrificaccedilatildeo eacute um processo bacteriano anaeroacutebico facultativo de degradaccedilatildeo da mateacuteria orgacircnica que em ausecircncia de oxigecircnio utiliza o NO3
- como receptor de eleacutetrons reduzindo-o agrave N2 Esse processo ocorre no sedimento e na coluna drsquoaacutegua estratificada imediatamente abaixo da zona oacutexica devido agrave formaccedilatildeo de NO3
- via nitrificaccedilatildeo
ou utilizando o substrato que tenha sido formado em outro ambiente (Kuschk et al 2003) Produtos intermediaacuterios do processo de desnitrificaccedilatildeo o NO e o N2O podem ser emitidos para a atmosfera A principal forma de perda de nitrogecircnio disponiacutevel no ambiente eacute atraveacutes do processo de desnitrificaccedilatildeo (Fennel et al 2009) onde os produtos intermediaacuterio eou finais (NO N2O e N2) satildeo gasosos e podem ser difundidos para a atmosfera tornando o nitrogecircnio um elemento limitante para outros organismos no ambiente (Seitzinger 1988 Harrison et al 2005)
Em ambientes eutrofizados como rios lagos e solos agriacutecolas com excesso de nutrientes a desnitrificaccedilatildeo acaba por reduzir a quantidade de compostos nitrogenados diminuindo a eutrofizaccedilatildeo dos ecossistemas bem como a lixiviaccedilatildeo do nitrogecircnio para outros ecossistemas (Seitzinger 1988 Seitzinger et al 2006) Por outro lado esse eacute o principal processo microbiano produtor de N2O agravando problemas como o aquecimento global e a destruiccedilatildeo da camada de ozocircnio Alteraccedilotildees da quantidade de N2O emitido ocorrem com frequumlecircncia devido a modificaccedilotildees bruscas das condiccedilotildees oacutexica-anoacutexica de solos e sedimentos e das concentraccedilotildees de NH3 e de NO2
- (Kampschreur et al 2009) Com isso ecossistemas aquaacuteticos ou ambientes terrestres sujeitos a influecircncia de aporte de aacuteguas satildeo fontes potencias na emissatildeo de N2O (Scott et al 2008) Segundo Kool et al (2011) a desnitrificaccedilatildeo eacute o principal processo formador de N2O embora a nitrificaccedilatildeo tambeacutem seja representativa em alguns tipos de solo
O NO3- eacute o principal substrato limitante para
a desnitrificaccedilatildeo e sua disponibilidade no meio eacute variaacutevel e dependente de diversos aspectos sendo um deles o tipo de solo que pode reter esse acircnion (Barrett amp Burke 2002) Entretanto esse mecanismo abioacutetico ainda eacute pouco estudado (Berntson amp Aber 2000 Zhu amp Wang 2011) e resume-se a adsorccedilatildeo do NO3
- a partiacuteculas do solo imobilizando esse importante nutriente nitrogenado e podendo ateacute tornaacute-lo limitante aos organismos de acordo com o estado troacutefico do ambiente (Bernot amp Dodds 2005)
FATORES REGULADORES DA PRODUCcedilAtildeO DE N2O
Os processos de nitrificaccedilatildeo e de desnitrificaccedilatildeo demandam disponibilidade de amocircnia e nitrato (NH3
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e NO3-) no ambiente Entretanto essa disponibilidade
eacute alterada em funccedilatildeo de vaacuterios fatores reguladores como concentraccedilotildees de oxigecircnio e mateacuteria orgacircnica temperatura pH umidade (Darrouzet-Nardi amp Bowman 1988 Seitzinger 1988 Miller et al 2009 Ross amp Wemple 2011) topografia (John et al 2007) e tambeacutem competiccedilatildeo entre as bacteacuterias do ciclo do nitrogecircnio e destas com outros micro-organismos e plantas (Inselsbacher et al 2010) Tais fatores bioacuteticos e abioacuteticos satildeo relevantes pois afetam principalmente a atividade e o crescimento microbiano (Mamilov amp Dilly 2002) Fatores reguladores podem variar espaccedilo-temporalmente afetando a produccedilatildeo de oacutexido nitroso que por estar associada aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Perez et al 2006 Farquharson amp Baldock 2008 Ma et al 2008) pode variar nessa mesma escala (McClain et al 2003) A seguir apresentamos e descrevemos os principais fatores reguladores da nitrificaccedilatildeo e da desnitrificaccedilatildeo
OXIGEcircNIO
Sendo a nitrificaccedilatildeo um processo estritamente aeroacutebico a presenccedila de oxigecircnio eacute um dos seus principais fatores reguladores (Bollmann amp Conrad 1998) Na Figura 3 observa-se a taxa de nitrificaccedilatildeo aumentar concomitantemente com a pressatildeo parcial de oxigecircnio em um solo agriacutecola ressaltando a influecircncia da disponibilidade de oxigecircnio sobre esse processo (Bollmann amp Conrad 1998) A disponibilidade de O2 pode ser totalmente alterada em funccedilatildeo da presenccedila de aacutegua no solo que ocupa o espaccedilo do oxigecircnio e restringe a velocidade da sua difusatildeo (Tiedje 1988)
Sedimentos de ambientes lagunares muitas vezes tecircm uma miacutenima camada superficial oacutexica que pode variar com a profundidade do lago Desta maneira deve-se ressaltar a importacircncia da presenccedila de micro-organismos fotossintetizantes em sedimentos de ambientes aquaacuteticos aumentando a oxigenaccedilatildeo e penetraccedilatildeo de O2 nas camadas mais profundas e possibilitando a ocorrecircncia da oxidaccedilatildeo da amocircnia em outras faixas do sedimento (Lorenzen et al 1998) (Figura 4) De maneira semelhante aos fotossintetizantes as raiacutezes de plantas em sistemas aquaacuteticos proporcionam a difusatildeo de oxigecircnio das raiacutezes para zonas anoacutexicas do sedimento criando microambientes oxigenados e permitindo que a nitrificaccedilatildeo ocorra e subsidie a desnitrificaccedilatildeo atraveacutes
do acoplamento dos processos (Reddy et al 1989 Ottosen et al 1999)
Solos expostos satildeo ambientes com grande oxigenaccedilatildeo dependentes de eventos de alagamento e do tipo de agregaccedilatildeo das partiacuteculas que compotildeem o solo Logo satildeo ambientes com elevado potencial nitrificante e tambeacutem de produccedilatildeo N2O Isso porque uma vez que o solo eacute molhado a disponibilidade de oxigecircnio diminui progressivamente e a nitrificaccedilatildeo ocorre de maneira incompleta produzindo NO ou N2O (Davidson et al 1993)
Figura 3 Influecircncia da pressatildeo parcial de O2 sobre a mineralizaccedilatildeo de nitrogecircnio () e sobre a nitrificaccedilatildeo () em um solo agriacutecola de Timmerlah (Alemanha meacutedia plusmn DP n=3 adaptado de Bollmann and Conrad 1998)Figure 3 Influence of partial pressure of O2 on mineralization of nitrogen () and on nitrification () on an agricultural soil of Timmerlah (Germany mean plusmn DP n=3 adapted from Bollmann and Conrad 1998)
Realizada por bacteacuterias facultativas a desnitrificaccedilatildeo natildeo ocorre em locais com alta concentraccedilatildeo de oxigecircnio pois os micro-organismos datildeo prioridade para a respiraccedilatildeo aeroacutebica mais favoraacutevel energeticamente Isso torna a presenccedila de oxigecircnio um fator regulador de grande relevacircncia (Bollmann amp Conrad 1998 Morley amp Baggs 2010) Diante dessa importacircncia encontramos um maior nuacutemero de registros de desnitrificaccedilatildeo em ambientes com baixa concentraccedilatildeo ou completa ausecircncia de oxigenaccedilatildeo como eacute o caso do sedimento de lagos planiacutecies de inundaccedilatildeo ou quaisquer aacutereas cobertas por aacutegua de pouca turbulecircncia Solos tambeacutem tecircm alto potencial desnitrificante devido agrave ocorrecircncia de chuvas que os tornam temporariamente anoacutexicos ou com baixa oxigenaccedilatildeo Um bom exemplo da regulaccedilatildeo do oxigecircnio sobre a desnitrificaccedilatildeo (Figura 4) ocorre na zona onde o oxigecircnio estaacute ausente (Lorenzen et al 1998) Aleacutem do oxigecircnio observa-se a influecircncia direta do NO3
- sobre as taxas
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de desnitrificaccedilatildeo onde este composto eacute o principal substrato desse processo sendo entatildeo considerado seu principal fator regulador Dessa forma identificamos atraveacutes do perfil de concentraccedilatildeo de NO3
- na camada superficial do sedimento a zona de produccedilatildeo (nitrificaccedilatildeo) e a de consumo (desnitrificaccedilatildeo) do composto enfatizando sua importacircncia para o processo
TEMPERATURA
A temperatura eacute um fator abioacutetico que regula o metabolismo de organismos vivos em geral e consequentemente tambeacutem regula a intensidade e ocorrecircncia de processos microbianos Os microrganismos tecircm seu metabolismo afetado visto que existe um oacutetimo de temperatura para
Figura 4 Perfil de O2 () e NO3- () e faixas de atividades microbianas do ciclo do N sob condiccedilotildees de iluminaccedilatildeo em diferentes aacutereas do sedimento
lacustre assimilaccedilatildeo de NO3- (preto do topo) nitrificaccedilatildeo (cinza claro) e desnitrificaccedilatildeo (preto de baixo) Os valores de O2 e NO3
- satildeo meacutedia plusmn DP n=6 (adaptada de Lorenzen et al 1998)
Figure 4 Profile of O2 () and NO3- () and depths of microbial activities of N cycling under light condition in different areas of sediment from lakes
assimilation of NO3- (black top) nitrification (light gray) and denitrification (black low) The values of O2 and NO3
- are mean plusmn SD n=6 (adapted from Lorenzen et al 1998)
o funcionamento fisioloacutegico bacteriano (Saad amp Conrad 1993 Pilegaard et al 2006) Temperaturas mais elevadas estimulam o metabolismo o que faz com que as taxas de nitrificaccedilatildeo e tambeacutem de desnitrificaccedilatildeo aumentem ateacute seu oacutetimo metaboacutelico (Schimel amp Gulledge 1998) com maacutexima produccedilatildeo de NO3
- acompanhada pelos seus subprodutos incluindo o N2O (Godde amp Conrad 1999)
O controle desempenhado pela temperatura onde geralmente encontramos uma relaccedilatildeo positiva foi confirmado no experimento de Godde amp Conrad (1999) em solo com temperatura controlada (Figura 5) Estes autores demonstraram que tanto a nitrificaccedilatildeo quanto a desnitrificaccedilatildeo sofrem alteraccedilotildees em suas taxas quando a temperatura eacute alterada (Malhi et al 1990 Saad amp Conrad 1993)
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Figura 6 Taxas de produccedilatildeo potencial de N2O determinada pela atividade da enzima desnitrificante As temperaturas de incubaccedilatildeo foram 4 15 20 25 e 37degC durante 20 dias Os dados satildeo meacutedia plusmn EP n=2 (adaptada de Braker et al 2010)
Figure 6 Rates of potential production of N2O determined by denitrifying enzyme activity The incubation temperatures were 4 15 20 25 and 37degC during 20 days Data are mean plusmn SE n=2 (adapted from Braker et al 2010)
Braker et al (2010) verificaram diretamente a influecircncia da temperatura sobre a produccedilatildeo de N2O em solos agriacutecolas corroborando a hipoacutetese de que a temperatura influencia a fisiologia das bacteacuterias desnitrificantes com o aquecimento do ambiente as taxas metaboacutelicas se mostram elevadas produzindo mais N2O ateacute um oacutetimo de temperatura (Figura 6) Embora este resultado tenha sido obtido em solos natildeo eacute de nosso conhecimento um experimento semelhante em sedimento de ambientes aquaacuteticos poreacutem o resultado esperado seria semelhante uma vez que essa regulaccedilatildeo metaboacutelica independe do tipo de sistema
O valor de temperatura oacutetimo para as bacteacuterias nitrificantes e desnitrificantes varia de 25deg a 35degC sendo registradas nessa faixa de temperatura as maiores taxas de atividade (Saad amp Conrad 1993 Braker et al 2010) Entretanto em muitos ambientes onde a temperatura natildeo eacute ideal alcanccedilando valores consideravelmente abaixo ou acima do oacutetimo verificamos a ocorrecircncia de atividade microbiana o que estaacute relacionado agrave capacidade de adaptaccedilatildeo dos microrganismos da comunidade ecoloacutegica em questatildeo a ambientes diferentes do ideal (Saad amp Conrad 1993)
pH
O potencial hidrogeniocircnico (pH) eacute um paracircmetro ambiental crucial para os processos do ciclo do N
atuando por exemplo na proporccedilatildeo NH3NH4+ na
aacutegua Em pH aacutecido ocorre a predominacircncia de NH4+
em detrimento de NH3 ocorrendo o inverso em pH alcalino (De Boer amp Kowalchuk 2001 Bajwa et al 2006) O controle exercido pelo pH sobre a produccedilatildeo de N2O (Conrad 1996 Enwall et al 2005) reflete-se indiretamente atraveacutes do efeito do pH sobre a comunidade bacteriana que pode regular a abundacircncia e diversidade dos microorganismos (Enwall et al 2005)
Como as bacteacuterias nitrificantes tecircm preferecircncia por assimilar NH3 em detrimento do NH4
+ a nitrificaccedilatildeo apresenta taxas mais elevadas em ambientes alcalinos (Kowalchuk amp Stephen 2001 Nugroho et al 2007) Sua influecircncia sobre a produccedilatildeo de N2O pela oxidaccedilatildeo aeroacutebica da amocircnia ainda eacute discutida na literatura devido agrave variaccedilatildeo de dados encontrados (Moslashrkved et al 2007) O processo de nitrificaccedilatildeo heterotroacutefica apresenta alta produccedilatildeo de N2O em pH aacutecido mas natildeo haacute muitos estudos sobre esse processo e sua relaccedilatildeo com o pH (Moslashrkved et al 2007)
O pH tambeacutem atua diretamente sobre as enzimas desnitrificantes oacutexido nitroso redutases que reduz N2O a N2 (Tiedje 1988) cuja atividade aumenta com o aumento do pH do ambiente ateacute alcanccedilar o seu oacutetimo Quando o pH do ambiente eacute baixo a produccedilatildeo da enzima diminui podendo chegar a ficar inativa ocasionando uma elevada produccedilatildeo de N2O (Aumleuhel amp Aringimek 2011) Na medida em que o pH
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aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
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em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
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N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
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Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
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VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
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Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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desnitrificaccedilatildeo nitrificante eacute menos estudada e ateacute o momento sabe-se apenas que a contribuiccedilatildeo de ambos os processos na produccedilatildeo de N2O varia de acordo com fatores bioloacutegicos e fiacutesicos do solo (Kool et al 2011) A pequena quantidade de informaccedilotildees sobre estes processos indica que estes precisam ser melhor quantificados nas diversas regiotildees do nosso planeta
Indiscutivelmente o principal preacute-requisito para que a nitrificaccedilatildeo ocorra eacute a disponibilidade de NH3NH4
+ o substrato nitrogenado baacutesico para ocorrecircncia desse processo Uma das principais fontes desses compostos nos ecossistemas aquaacuteticos e terrestres eacute a degradaccedilatildeo de mateacuteria orgacircnica laacutebil que libera diferentes compostos como nitrogecircnio orgacircnico NH3 NO2
- NO3- e fosfato (Balota amp Auler 2011)
Derivado dessa mineralizaccedilatildeo a NH3 eacute uma fonte de nitrogecircnio extremamente laacutebil e de faacutecil assimilaccedilatildeo pelos vaacuterios tipos de macro e micro-organismos o que muitas vezes torna esse composto limitante no ambiente (Sasaki et al 2002 Schmidt et al 2011) Excretas nitrogenados advindos de organismos heterotroacuteficos tambeacutem satildeo uma importante fonte de NH3NH4
+As concentraccedilotildees relativas de NH3 e NH4
+ na aacutegua satildeo dependentes principalmente do pH da aacutegua Reconhecidamente na maioria dos ambientes a forma nitrogenada predominante eacute o NH4
+ jaacute que a forma NH3 gasosa eacute dominante apenas entre pH 8-10 (Johnson et al 2008) valores estes menos frequentes nos sistemas aquaacuteticos Entretanto eacute nessa faixa de pH alcalino que a NH3 estaacute na fase gasosa e eacute liberada em maior quantidade para a atmosfera atraveacutes da volatilizaccedilatildeo (Jayaweera amp Mikkelsen 1991 Bajwa et al 2006 Fiencke et al 2006 Haden et al 2011) Logo sua assimilaccedilatildeo bem como a volatilizaccedilatildeo indisponibilizam o nitrogecircnio para o processo nitrificante reduzindo as taxas de desnitrificaccedilatildeo e consequentemente a produccedilatildeo de N2O
Desnitrificaccedilatildeo
A desnitrificaccedilatildeo eacute um processo bacteriano anaeroacutebico facultativo de degradaccedilatildeo da mateacuteria orgacircnica que em ausecircncia de oxigecircnio utiliza o NO3
- como receptor de eleacutetrons reduzindo-o agrave N2 Esse processo ocorre no sedimento e na coluna drsquoaacutegua estratificada imediatamente abaixo da zona oacutexica devido agrave formaccedilatildeo de NO3
- via nitrificaccedilatildeo
ou utilizando o substrato que tenha sido formado em outro ambiente (Kuschk et al 2003) Produtos intermediaacuterios do processo de desnitrificaccedilatildeo o NO e o N2O podem ser emitidos para a atmosfera A principal forma de perda de nitrogecircnio disponiacutevel no ambiente eacute atraveacutes do processo de desnitrificaccedilatildeo (Fennel et al 2009) onde os produtos intermediaacuterio eou finais (NO N2O e N2) satildeo gasosos e podem ser difundidos para a atmosfera tornando o nitrogecircnio um elemento limitante para outros organismos no ambiente (Seitzinger 1988 Harrison et al 2005)
Em ambientes eutrofizados como rios lagos e solos agriacutecolas com excesso de nutrientes a desnitrificaccedilatildeo acaba por reduzir a quantidade de compostos nitrogenados diminuindo a eutrofizaccedilatildeo dos ecossistemas bem como a lixiviaccedilatildeo do nitrogecircnio para outros ecossistemas (Seitzinger 1988 Seitzinger et al 2006) Por outro lado esse eacute o principal processo microbiano produtor de N2O agravando problemas como o aquecimento global e a destruiccedilatildeo da camada de ozocircnio Alteraccedilotildees da quantidade de N2O emitido ocorrem com frequumlecircncia devido a modificaccedilotildees bruscas das condiccedilotildees oacutexica-anoacutexica de solos e sedimentos e das concentraccedilotildees de NH3 e de NO2
- (Kampschreur et al 2009) Com isso ecossistemas aquaacuteticos ou ambientes terrestres sujeitos a influecircncia de aporte de aacuteguas satildeo fontes potencias na emissatildeo de N2O (Scott et al 2008) Segundo Kool et al (2011) a desnitrificaccedilatildeo eacute o principal processo formador de N2O embora a nitrificaccedilatildeo tambeacutem seja representativa em alguns tipos de solo
O NO3- eacute o principal substrato limitante para
a desnitrificaccedilatildeo e sua disponibilidade no meio eacute variaacutevel e dependente de diversos aspectos sendo um deles o tipo de solo que pode reter esse acircnion (Barrett amp Burke 2002) Entretanto esse mecanismo abioacutetico ainda eacute pouco estudado (Berntson amp Aber 2000 Zhu amp Wang 2011) e resume-se a adsorccedilatildeo do NO3
- a partiacuteculas do solo imobilizando esse importante nutriente nitrogenado e podendo ateacute tornaacute-lo limitante aos organismos de acordo com o estado troacutefico do ambiente (Bernot amp Dodds 2005)
FATORES REGULADORES DA PRODUCcedilAtildeO DE N2O
Os processos de nitrificaccedilatildeo e de desnitrificaccedilatildeo demandam disponibilidade de amocircnia e nitrato (NH3
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e NO3-) no ambiente Entretanto essa disponibilidade
eacute alterada em funccedilatildeo de vaacuterios fatores reguladores como concentraccedilotildees de oxigecircnio e mateacuteria orgacircnica temperatura pH umidade (Darrouzet-Nardi amp Bowman 1988 Seitzinger 1988 Miller et al 2009 Ross amp Wemple 2011) topografia (John et al 2007) e tambeacutem competiccedilatildeo entre as bacteacuterias do ciclo do nitrogecircnio e destas com outros micro-organismos e plantas (Inselsbacher et al 2010) Tais fatores bioacuteticos e abioacuteticos satildeo relevantes pois afetam principalmente a atividade e o crescimento microbiano (Mamilov amp Dilly 2002) Fatores reguladores podem variar espaccedilo-temporalmente afetando a produccedilatildeo de oacutexido nitroso que por estar associada aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Perez et al 2006 Farquharson amp Baldock 2008 Ma et al 2008) pode variar nessa mesma escala (McClain et al 2003) A seguir apresentamos e descrevemos os principais fatores reguladores da nitrificaccedilatildeo e da desnitrificaccedilatildeo
OXIGEcircNIO
Sendo a nitrificaccedilatildeo um processo estritamente aeroacutebico a presenccedila de oxigecircnio eacute um dos seus principais fatores reguladores (Bollmann amp Conrad 1998) Na Figura 3 observa-se a taxa de nitrificaccedilatildeo aumentar concomitantemente com a pressatildeo parcial de oxigecircnio em um solo agriacutecola ressaltando a influecircncia da disponibilidade de oxigecircnio sobre esse processo (Bollmann amp Conrad 1998) A disponibilidade de O2 pode ser totalmente alterada em funccedilatildeo da presenccedila de aacutegua no solo que ocupa o espaccedilo do oxigecircnio e restringe a velocidade da sua difusatildeo (Tiedje 1988)
Sedimentos de ambientes lagunares muitas vezes tecircm uma miacutenima camada superficial oacutexica que pode variar com a profundidade do lago Desta maneira deve-se ressaltar a importacircncia da presenccedila de micro-organismos fotossintetizantes em sedimentos de ambientes aquaacuteticos aumentando a oxigenaccedilatildeo e penetraccedilatildeo de O2 nas camadas mais profundas e possibilitando a ocorrecircncia da oxidaccedilatildeo da amocircnia em outras faixas do sedimento (Lorenzen et al 1998) (Figura 4) De maneira semelhante aos fotossintetizantes as raiacutezes de plantas em sistemas aquaacuteticos proporcionam a difusatildeo de oxigecircnio das raiacutezes para zonas anoacutexicas do sedimento criando microambientes oxigenados e permitindo que a nitrificaccedilatildeo ocorra e subsidie a desnitrificaccedilatildeo atraveacutes
do acoplamento dos processos (Reddy et al 1989 Ottosen et al 1999)
Solos expostos satildeo ambientes com grande oxigenaccedilatildeo dependentes de eventos de alagamento e do tipo de agregaccedilatildeo das partiacuteculas que compotildeem o solo Logo satildeo ambientes com elevado potencial nitrificante e tambeacutem de produccedilatildeo N2O Isso porque uma vez que o solo eacute molhado a disponibilidade de oxigecircnio diminui progressivamente e a nitrificaccedilatildeo ocorre de maneira incompleta produzindo NO ou N2O (Davidson et al 1993)
Figura 3 Influecircncia da pressatildeo parcial de O2 sobre a mineralizaccedilatildeo de nitrogecircnio () e sobre a nitrificaccedilatildeo () em um solo agriacutecola de Timmerlah (Alemanha meacutedia plusmn DP n=3 adaptado de Bollmann and Conrad 1998)Figure 3 Influence of partial pressure of O2 on mineralization of nitrogen () and on nitrification () on an agricultural soil of Timmerlah (Germany mean plusmn DP n=3 adapted from Bollmann and Conrad 1998)
Realizada por bacteacuterias facultativas a desnitrificaccedilatildeo natildeo ocorre em locais com alta concentraccedilatildeo de oxigecircnio pois os micro-organismos datildeo prioridade para a respiraccedilatildeo aeroacutebica mais favoraacutevel energeticamente Isso torna a presenccedila de oxigecircnio um fator regulador de grande relevacircncia (Bollmann amp Conrad 1998 Morley amp Baggs 2010) Diante dessa importacircncia encontramos um maior nuacutemero de registros de desnitrificaccedilatildeo em ambientes com baixa concentraccedilatildeo ou completa ausecircncia de oxigenaccedilatildeo como eacute o caso do sedimento de lagos planiacutecies de inundaccedilatildeo ou quaisquer aacutereas cobertas por aacutegua de pouca turbulecircncia Solos tambeacutem tecircm alto potencial desnitrificante devido agrave ocorrecircncia de chuvas que os tornam temporariamente anoacutexicos ou com baixa oxigenaccedilatildeo Um bom exemplo da regulaccedilatildeo do oxigecircnio sobre a desnitrificaccedilatildeo (Figura 4) ocorre na zona onde o oxigecircnio estaacute ausente (Lorenzen et al 1998) Aleacutem do oxigecircnio observa-se a influecircncia direta do NO3
- sobre as taxas
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de desnitrificaccedilatildeo onde este composto eacute o principal substrato desse processo sendo entatildeo considerado seu principal fator regulador Dessa forma identificamos atraveacutes do perfil de concentraccedilatildeo de NO3
- na camada superficial do sedimento a zona de produccedilatildeo (nitrificaccedilatildeo) e a de consumo (desnitrificaccedilatildeo) do composto enfatizando sua importacircncia para o processo
TEMPERATURA
A temperatura eacute um fator abioacutetico que regula o metabolismo de organismos vivos em geral e consequentemente tambeacutem regula a intensidade e ocorrecircncia de processos microbianos Os microrganismos tecircm seu metabolismo afetado visto que existe um oacutetimo de temperatura para
Figura 4 Perfil de O2 () e NO3- () e faixas de atividades microbianas do ciclo do N sob condiccedilotildees de iluminaccedilatildeo em diferentes aacutereas do sedimento
lacustre assimilaccedilatildeo de NO3- (preto do topo) nitrificaccedilatildeo (cinza claro) e desnitrificaccedilatildeo (preto de baixo) Os valores de O2 e NO3
- satildeo meacutedia plusmn DP n=6 (adaptada de Lorenzen et al 1998)
Figure 4 Profile of O2 () and NO3- () and depths of microbial activities of N cycling under light condition in different areas of sediment from lakes
assimilation of NO3- (black top) nitrification (light gray) and denitrification (black low) The values of O2 and NO3
- are mean plusmn SD n=6 (adapted from Lorenzen et al 1998)
o funcionamento fisioloacutegico bacteriano (Saad amp Conrad 1993 Pilegaard et al 2006) Temperaturas mais elevadas estimulam o metabolismo o que faz com que as taxas de nitrificaccedilatildeo e tambeacutem de desnitrificaccedilatildeo aumentem ateacute seu oacutetimo metaboacutelico (Schimel amp Gulledge 1998) com maacutexima produccedilatildeo de NO3
- acompanhada pelos seus subprodutos incluindo o N2O (Godde amp Conrad 1999)
O controle desempenhado pela temperatura onde geralmente encontramos uma relaccedilatildeo positiva foi confirmado no experimento de Godde amp Conrad (1999) em solo com temperatura controlada (Figura 5) Estes autores demonstraram que tanto a nitrificaccedilatildeo quanto a desnitrificaccedilatildeo sofrem alteraccedilotildees em suas taxas quando a temperatura eacute alterada (Malhi et al 1990 Saad amp Conrad 1993)
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Figura 6 Taxas de produccedilatildeo potencial de N2O determinada pela atividade da enzima desnitrificante As temperaturas de incubaccedilatildeo foram 4 15 20 25 e 37degC durante 20 dias Os dados satildeo meacutedia plusmn EP n=2 (adaptada de Braker et al 2010)
Figure 6 Rates of potential production of N2O determined by denitrifying enzyme activity The incubation temperatures were 4 15 20 25 and 37degC during 20 days Data are mean plusmn SE n=2 (adapted from Braker et al 2010)
Braker et al (2010) verificaram diretamente a influecircncia da temperatura sobre a produccedilatildeo de N2O em solos agriacutecolas corroborando a hipoacutetese de que a temperatura influencia a fisiologia das bacteacuterias desnitrificantes com o aquecimento do ambiente as taxas metaboacutelicas se mostram elevadas produzindo mais N2O ateacute um oacutetimo de temperatura (Figura 6) Embora este resultado tenha sido obtido em solos natildeo eacute de nosso conhecimento um experimento semelhante em sedimento de ambientes aquaacuteticos poreacutem o resultado esperado seria semelhante uma vez que essa regulaccedilatildeo metaboacutelica independe do tipo de sistema
O valor de temperatura oacutetimo para as bacteacuterias nitrificantes e desnitrificantes varia de 25deg a 35degC sendo registradas nessa faixa de temperatura as maiores taxas de atividade (Saad amp Conrad 1993 Braker et al 2010) Entretanto em muitos ambientes onde a temperatura natildeo eacute ideal alcanccedilando valores consideravelmente abaixo ou acima do oacutetimo verificamos a ocorrecircncia de atividade microbiana o que estaacute relacionado agrave capacidade de adaptaccedilatildeo dos microrganismos da comunidade ecoloacutegica em questatildeo a ambientes diferentes do ideal (Saad amp Conrad 1993)
pH
O potencial hidrogeniocircnico (pH) eacute um paracircmetro ambiental crucial para os processos do ciclo do N
atuando por exemplo na proporccedilatildeo NH3NH4+ na
aacutegua Em pH aacutecido ocorre a predominacircncia de NH4+
em detrimento de NH3 ocorrendo o inverso em pH alcalino (De Boer amp Kowalchuk 2001 Bajwa et al 2006) O controle exercido pelo pH sobre a produccedilatildeo de N2O (Conrad 1996 Enwall et al 2005) reflete-se indiretamente atraveacutes do efeito do pH sobre a comunidade bacteriana que pode regular a abundacircncia e diversidade dos microorganismos (Enwall et al 2005)
Como as bacteacuterias nitrificantes tecircm preferecircncia por assimilar NH3 em detrimento do NH4
+ a nitrificaccedilatildeo apresenta taxas mais elevadas em ambientes alcalinos (Kowalchuk amp Stephen 2001 Nugroho et al 2007) Sua influecircncia sobre a produccedilatildeo de N2O pela oxidaccedilatildeo aeroacutebica da amocircnia ainda eacute discutida na literatura devido agrave variaccedilatildeo de dados encontrados (Moslashrkved et al 2007) O processo de nitrificaccedilatildeo heterotroacutefica apresenta alta produccedilatildeo de N2O em pH aacutecido mas natildeo haacute muitos estudos sobre esse processo e sua relaccedilatildeo com o pH (Moslashrkved et al 2007)
O pH tambeacutem atua diretamente sobre as enzimas desnitrificantes oacutexido nitroso redutases que reduz N2O a N2 (Tiedje 1988) cuja atividade aumenta com o aumento do pH do ambiente ateacute alcanccedilar o seu oacutetimo Quando o pH do ambiente eacute baixo a produccedilatildeo da enzima diminui podendo chegar a ficar inativa ocasionando uma elevada produccedilatildeo de N2O (Aumleuhel amp Aringimek 2011) Na medida em que o pH
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aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
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em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
320
N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
321
Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
322
VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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Submetido em 13052012Aceito em 23062012
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
315
e NO3-) no ambiente Entretanto essa disponibilidade
eacute alterada em funccedilatildeo de vaacuterios fatores reguladores como concentraccedilotildees de oxigecircnio e mateacuteria orgacircnica temperatura pH umidade (Darrouzet-Nardi amp Bowman 1988 Seitzinger 1988 Miller et al 2009 Ross amp Wemple 2011) topografia (John et al 2007) e tambeacutem competiccedilatildeo entre as bacteacuterias do ciclo do nitrogecircnio e destas com outros micro-organismos e plantas (Inselsbacher et al 2010) Tais fatores bioacuteticos e abioacuteticos satildeo relevantes pois afetam principalmente a atividade e o crescimento microbiano (Mamilov amp Dilly 2002) Fatores reguladores podem variar espaccedilo-temporalmente afetando a produccedilatildeo de oacutexido nitroso que por estar associada aos processos de nitrificaccedilatildeo e desnitrificaccedilatildeo (Perez et al 2006 Farquharson amp Baldock 2008 Ma et al 2008) pode variar nessa mesma escala (McClain et al 2003) A seguir apresentamos e descrevemos os principais fatores reguladores da nitrificaccedilatildeo e da desnitrificaccedilatildeo
OXIGEcircNIO
Sendo a nitrificaccedilatildeo um processo estritamente aeroacutebico a presenccedila de oxigecircnio eacute um dos seus principais fatores reguladores (Bollmann amp Conrad 1998) Na Figura 3 observa-se a taxa de nitrificaccedilatildeo aumentar concomitantemente com a pressatildeo parcial de oxigecircnio em um solo agriacutecola ressaltando a influecircncia da disponibilidade de oxigecircnio sobre esse processo (Bollmann amp Conrad 1998) A disponibilidade de O2 pode ser totalmente alterada em funccedilatildeo da presenccedila de aacutegua no solo que ocupa o espaccedilo do oxigecircnio e restringe a velocidade da sua difusatildeo (Tiedje 1988)
Sedimentos de ambientes lagunares muitas vezes tecircm uma miacutenima camada superficial oacutexica que pode variar com a profundidade do lago Desta maneira deve-se ressaltar a importacircncia da presenccedila de micro-organismos fotossintetizantes em sedimentos de ambientes aquaacuteticos aumentando a oxigenaccedilatildeo e penetraccedilatildeo de O2 nas camadas mais profundas e possibilitando a ocorrecircncia da oxidaccedilatildeo da amocircnia em outras faixas do sedimento (Lorenzen et al 1998) (Figura 4) De maneira semelhante aos fotossintetizantes as raiacutezes de plantas em sistemas aquaacuteticos proporcionam a difusatildeo de oxigecircnio das raiacutezes para zonas anoacutexicas do sedimento criando microambientes oxigenados e permitindo que a nitrificaccedilatildeo ocorra e subsidie a desnitrificaccedilatildeo atraveacutes
do acoplamento dos processos (Reddy et al 1989 Ottosen et al 1999)
Solos expostos satildeo ambientes com grande oxigenaccedilatildeo dependentes de eventos de alagamento e do tipo de agregaccedilatildeo das partiacuteculas que compotildeem o solo Logo satildeo ambientes com elevado potencial nitrificante e tambeacutem de produccedilatildeo N2O Isso porque uma vez que o solo eacute molhado a disponibilidade de oxigecircnio diminui progressivamente e a nitrificaccedilatildeo ocorre de maneira incompleta produzindo NO ou N2O (Davidson et al 1993)
Figura 3 Influecircncia da pressatildeo parcial de O2 sobre a mineralizaccedilatildeo de nitrogecircnio () e sobre a nitrificaccedilatildeo () em um solo agriacutecola de Timmerlah (Alemanha meacutedia plusmn DP n=3 adaptado de Bollmann and Conrad 1998)Figure 3 Influence of partial pressure of O2 on mineralization of nitrogen () and on nitrification () on an agricultural soil of Timmerlah (Germany mean plusmn DP n=3 adapted from Bollmann and Conrad 1998)
Realizada por bacteacuterias facultativas a desnitrificaccedilatildeo natildeo ocorre em locais com alta concentraccedilatildeo de oxigecircnio pois os micro-organismos datildeo prioridade para a respiraccedilatildeo aeroacutebica mais favoraacutevel energeticamente Isso torna a presenccedila de oxigecircnio um fator regulador de grande relevacircncia (Bollmann amp Conrad 1998 Morley amp Baggs 2010) Diante dessa importacircncia encontramos um maior nuacutemero de registros de desnitrificaccedilatildeo em ambientes com baixa concentraccedilatildeo ou completa ausecircncia de oxigenaccedilatildeo como eacute o caso do sedimento de lagos planiacutecies de inundaccedilatildeo ou quaisquer aacutereas cobertas por aacutegua de pouca turbulecircncia Solos tambeacutem tecircm alto potencial desnitrificante devido agrave ocorrecircncia de chuvas que os tornam temporariamente anoacutexicos ou com baixa oxigenaccedilatildeo Um bom exemplo da regulaccedilatildeo do oxigecircnio sobre a desnitrificaccedilatildeo (Figura 4) ocorre na zona onde o oxigecircnio estaacute ausente (Lorenzen et al 1998) Aleacutem do oxigecircnio observa-se a influecircncia direta do NO3
- sobre as taxas
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
316
de desnitrificaccedilatildeo onde este composto eacute o principal substrato desse processo sendo entatildeo considerado seu principal fator regulador Dessa forma identificamos atraveacutes do perfil de concentraccedilatildeo de NO3
- na camada superficial do sedimento a zona de produccedilatildeo (nitrificaccedilatildeo) e a de consumo (desnitrificaccedilatildeo) do composto enfatizando sua importacircncia para o processo
TEMPERATURA
A temperatura eacute um fator abioacutetico que regula o metabolismo de organismos vivos em geral e consequentemente tambeacutem regula a intensidade e ocorrecircncia de processos microbianos Os microrganismos tecircm seu metabolismo afetado visto que existe um oacutetimo de temperatura para
Figura 4 Perfil de O2 () e NO3- () e faixas de atividades microbianas do ciclo do N sob condiccedilotildees de iluminaccedilatildeo em diferentes aacutereas do sedimento
lacustre assimilaccedilatildeo de NO3- (preto do topo) nitrificaccedilatildeo (cinza claro) e desnitrificaccedilatildeo (preto de baixo) Os valores de O2 e NO3
- satildeo meacutedia plusmn DP n=6 (adaptada de Lorenzen et al 1998)
Figure 4 Profile of O2 () and NO3- () and depths of microbial activities of N cycling under light condition in different areas of sediment from lakes
assimilation of NO3- (black top) nitrification (light gray) and denitrification (black low) The values of O2 and NO3
- are mean plusmn SD n=6 (adapted from Lorenzen et al 1998)
o funcionamento fisioloacutegico bacteriano (Saad amp Conrad 1993 Pilegaard et al 2006) Temperaturas mais elevadas estimulam o metabolismo o que faz com que as taxas de nitrificaccedilatildeo e tambeacutem de desnitrificaccedilatildeo aumentem ateacute seu oacutetimo metaboacutelico (Schimel amp Gulledge 1998) com maacutexima produccedilatildeo de NO3
- acompanhada pelos seus subprodutos incluindo o N2O (Godde amp Conrad 1999)
O controle desempenhado pela temperatura onde geralmente encontramos uma relaccedilatildeo positiva foi confirmado no experimento de Godde amp Conrad (1999) em solo com temperatura controlada (Figura 5) Estes autores demonstraram que tanto a nitrificaccedilatildeo quanto a desnitrificaccedilatildeo sofrem alteraccedilotildees em suas taxas quando a temperatura eacute alterada (Malhi et al 1990 Saad amp Conrad 1993)
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
317
Figura 6 Taxas de produccedilatildeo potencial de N2O determinada pela atividade da enzima desnitrificante As temperaturas de incubaccedilatildeo foram 4 15 20 25 e 37degC durante 20 dias Os dados satildeo meacutedia plusmn EP n=2 (adaptada de Braker et al 2010)
Figure 6 Rates of potential production of N2O determined by denitrifying enzyme activity The incubation temperatures were 4 15 20 25 and 37degC during 20 days Data are mean plusmn SE n=2 (adapted from Braker et al 2010)
Braker et al (2010) verificaram diretamente a influecircncia da temperatura sobre a produccedilatildeo de N2O em solos agriacutecolas corroborando a hipoacutetese de que a temperatura influencia a fisiologia das bacteacuterias desnitrificantes com o aquecimento do ambiente as taxas metaboacutelicas se mostram elevadas produzindo mais N2O ateacute um oacutetimo de temperatura (Figura 6) Embora este resultado tenha sido obtido em solos natildeo eacute de nosso conhecimento um experimento semelhante em sedimento de ambientes aquaacuteticos poreacutem o resultado esperado seria semelhante uma vez que essa regulaccedilatildeo metaboacutelica independe do tipo de sistema
O valor de temperatura oacutetimo para as bacteacuterias nitrificantes e desnitrificantes varia de 25deg a 35degC sendo registradas nessa faixa de temperatura as maiores taxas de atividade (Saad amp Conrad 1993 Braker et al 2010) Entretanto em muitos ambientes onde a temperatura natildeo eacute ideal alcanccedilando valores consideravelmente abaixo ou acima do oacutetimo verificamos a ocorrecircncia de atividade microbiana o que estaacute relacionado agrave capacidade de adaptaccedilatildeo dos microrganismos da comunidade ecoloacutegica em questatildeo a ambientes diferentes do ideal (Saad amp Conrad 1993)
pH
O potencial hidrogeniocircnico (pH) eacute um paracircmetro ambiental crucial para os processos do ciclo do N
atuando por exemplo na proporccedilatildeo NH3NH4+ na
aacutegua Em pH aacutecido ocorre a predominacircncia de NH4+
em detrimento de NH3 ocorrendo o inverso em pH alcalino (De Boer amp Kowalchuk 2001 Bajwa et al 2006) O controle exercido pelo pH sobre a produccedilatildeo de N2O (Conrad 1996 Enwall et al 2005) reflete-se indiretamente atraveacutes do efeito do pH sobre a comunidade bacteriana que pode regular a abundacircncia e diversidade dos microorganismos (Enwall et al 2005)
Como as bacteacuterias nitrificantes tecircm preferecircncia por assimilar NH3 em detrimento do NH4
+ a nitrificaccedilatildeo apresenta taxas mais elevadas em ambientes alcalinos (Kowalchuk amp Stephen 2001 Nugroho et al 2007) Sua influecircncia sobre a produccedilatildeo de N2O pela oxidaccedilatildeo aeroacutebica da amocircnia ainda eacute discutida na literatura devido agrave variaccedilatildeo de dados encontrados (Moslashrkved et al 2007) O processo de nitrificaccedilatildeo heterotroacutefica apresenta alta produccedilatildeo de N2O em pH aacutecido mas natildeo haacute muitos estudos sobre esse processo e sua relaccedilatildeo com o pH (Moslashrkved et al 2007)
O pH tambeacutem atua diretamente sobre as enzimas desnitrificantes oacutexido nitroso redutases que reduz N2O a N2 (Tiedje 1988) cuja atividade aumenta com o aumento do pH do ambiente ateacute alcanccedilar o seu oacutetimo Quando o pH do ambiente eacute baixo a produccedilatildeo da enzima diminui podendo chegar a ficar inativa ocasionando uma elevada produccedilatildeo de N2O (Aumleuhel amp Aringimek 2011) Na medida em que o pH
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aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
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em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
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N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
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Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
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VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
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Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
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de desnitrificaccedilatildeo onde este composto eacute o principal substrato desse processo sendo entatildeo considerado seu principal fator regulador Dessa forma identificamos atraveacutes do perfil de concentraccedilatildeo de NO3
- na camada superficial do sedimento a zona de produccedilatildeo (nitrificaccedilatildeo) e a de consumo (desnitrificaccedilatildeo) do composto enfatizando sua importacircncia para o processo
TEMPERATURA
A temperatura eacute um fator abioacutetico que regula o metabolismo de organismos vivos em geral e consequentemente tambeacutem regula a intensidade e ocorrecircncia de processos microbianos Os microrganismos tecircm seu metabolismo afetado visto que existe um oacutetimo de temperatura para
Figura 4 Perfil de O2 () e NO3- () e faixas de atividades microbianas do ciclo do N sob condiccedilotildees de iluminaccedilatildeo em diferentes aacutereas do sedimento
lacustre assimilaccedilatildeo de NO3- (preto do topo) nitrificaccedilatildeo (cinza claro) e desnitrificaccedilatildeo (preto de baixo) Os valores de O2 e NO3
- satildeo meacutedia plusmn DP n=6 (adaptada de Lorenzen et al 1998)
Figure 4 Profile of O2 () and NO3- () and depths of microbial activities of N cycling under light condition in different areas of sediment from lakes
assimilation of NO3- (black top) nitrification (light gray) and denitrification (black low) The values of O2 and NO3
- are mean plusmn SD n=6 (adapted from Lorenzen et al 1998)
o funcionamento fisioloacutegico bacteriano (Saad amp Conrad 1993 Pilegaard et al 2006) Temperaturas mais elevadas estimulam o metabolismo o que faz com que as taxas de nitrificaccedilatildeo e tambeacutem de desnitrificaccedilatildeo aumentem ateacute seu oacutetimo metaboacutelico (Schimel amp Gulledge 1998) com maacutexima produccedilatildeo de NO3
- acompanhada pelos seus subprodutos incluindo o N2O (Godde amp Conrad 1999)
O controle desempenhado pela temperatura onde geralmente encontramos uma relaccedilatildeo positiva foi confirmado no experimento de Godde amp Conrad (1999) em solo com temperatura controlada (Figura 5) Estes autores demonstraram que tanto a nitrificaccedilatildeo quanto a desnitrificaccedilatildeo sofrem alteraccedilotildees em suas taxas quando a temperatura eacute alterada (Malhi et al 1990 Saad amp Conrad 1993)
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Figura 6 Taxas de produccedilatildeo potencial de N2O determinada pela atividade da enzima desnitrificante As temperaturas de incubaccedilatildeo foram 4 15 20 25 e 37degC durante 20 dias Os dados satildeo meacutedia plusmn EP n=2 (adaptada de Braker et al 2010)
Figure 6 Rates of potential production of N2O determined by denitrifying enzyme activity The incubation temperatures were 4 15 20 25 and 37degC during 20 days Data are mean plusmn SE n=2 (adapted from Braker et al 2010)
Braker et al (2010) verificaram diretamente a influecircncia da temperatura sobre a produccedilatildeo de N2O em solos agriacutecolas corroborando a hipoacutetese de que a temperatura influencia a fisiologia das bacteacuterias desnitrificantes com o aquecimento do ambiente as taxas metaboacutelicas se mostram elevadas produzindo mais N2O ateacute um oacutetimo de temperatura (Figura 6) Embora este resultado tenha sido obtido em solos natildeo eacute de nosso conhecimento um experimento semelhante em sedimento de ambientes aquaacuteticos poreacutem o resultado esperado seria semelhante uma vez que essa regulaccedilatildeo metaboacutelica independe do tipo de sistema
O valor de temperatura oacutetimo para as bacteacuterias nitrificantes e desnitrificantes varia de 25deg a 35degC sendo registradas nessa faixa de temperatura as maiores taxas de atividade (Saad amp Conrad 1993 Braker et al 2010) Entretanto em muitos ambientes onde a temperatura natildeo eacute ideal alcanccedilando valores consideravelmente abaixo ou acima do oacutetimo verificamos a ocorrecircncia de atividade microbiana o que estaacute relacionado agrave capacidade de adaptaccedilatildeo dos microrganismos da comunidade ecoloacutegica em questatildeo a ambientes diferentes do ideal (Saad amp Conrad 1993)
pH
O potencial hidrogeniocircnico (pH) eacute um paracircmetro ambiental crucial para os processos do ciclo do N
atuando por exemplo na proporccedilatildeo NH3NH4+ na
aacutegua Em pH aacutecido ocorre a predominacircncia de NH4+
em detrimento de NH3 ocorrendo o inverso em pH alcalino (De Boer amp Kowalchuk 2001 Bajwa et al 2006) O controle exercido pelo pH sobre a produccedilatildeo de N2O (Conrad 1996 Enwall et al 2005) reflete-se indiretamente atraveacutes do efeito do pH sobre a comunidade bacteriana que pode regular a abundacircncia e diversidade dos microorganismos (Enwall et al 2005)
Como as bacteacuterias nitrificantes tecircm preferecircncia por assimilar NH3 em detrimento do NH4
+ a nitrificaccedilatildeo apresenta taxas mais elevadas em ambientes alcalinos (Kowalchuk amp Stephen 2001 Nugroho et al 2007) Sua influecircncia sobre a produccedilatildeo de N2O pela oxidaccedilatildeo aeroacutebica da amocircnia ainda eacute discutida na literatura devido agrave variaccedilatildeo de dados encontrados (Moslashrkved et al 2007) O processo de nitrificaccedilatildeo heterotroacutefica apresenta alta produccedilatildeo de N2O em pH aacutecido mas natildeo haacute muitos estudos sobre esse processo e sua relaccedilatildeo com o pH (Moslashrkved et al 2007)
O pH tambeacutem atua diretamente sobre as enzimas desnitrificantes oacutexido nitroso redutases que reduz N2O a N2 (Tiedje 1988) cuja atividade aumenta com o aumento do pH do ambiente ateacute alcanccedilar o seu oacutetimo Quando o pH do ambiente eacute baixo a produccedilatildeo da enzima diminui podendo chegar a ficar inativa ocasionando uma elevada produccedilatildeo de N2O (Aumleuhel amp Aringimek 2011) Na medida em que o pH
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aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
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em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
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N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
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Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
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VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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0761(2006)016[2153NONADN]20CO2
PILEGAARD K SKIBA U AMBUS P BEIER C
BRUGGEMANN N BUTTERBACH-BAHL K DICK
J DORSEY J DUYZER J GALLAGHER M GASCHE
R HORVATH L KITZLER B LEIP A PIHLATIE MK
ROSENKRANZ P SEUFERT G VESALA T WESTRATE
H amp ZECHMEISTER-BOLTENSTERN S 2006 Factors
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org105194bg-3-651-2006
PINtildeA-OCHOA E amp ALVAREZ-COBELAS M 2006
Denitrification in aquatic environments A cross-system analysis
Biogeochemistry 81 111-130 httpdxdoiorg101007s10533-
006-9033-7
POULIN P PELLETIER E amp SAINT-LOUIS R 2007
Seasonal variability of denitrification efficiency in northern
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org101016jmarenvres200612003
RAVISHANKARA AR DANIEL JS amp PORTMANN
RW 2009 Nitrous oxide (N2O) The dominant ozone-depleting
substance emitted in the 21st century Science 326 123-125
httpdxdoiorg101126science1176985
REDDY KR PATRICK WH amp LINDAU CW 1989
Nitrification-Denitrification at the Plant Root-Sediment Interface
in Wetlands Limnology and Oceanography 34 1004-1013
httpdxdoiorg104319lo19893461004
ROBINSON AD NEDWELL DB HARRISON RM amp
OGILVIE BG 1998 Hypernutrified estuaries as sources of
N2O emission to the atmosphere the estuary of the River Colne
Essex UK Marine Ecology Progress Series 164 59-71 http
dxdoiorg103354meps164059
ROSS DS amp WEMPLE BC 2011 Soil nitrification in a large
forested watershed Ranch Brook (Vermont) mirrors patterns
in smaller northeastern USA catchments Forest Ecology and
Management 262 1084-1093 httpdxdoiorg101016j
foreco201106002
RYSGAARD S RISGAARD-PETERSEN N NIELSEN LP
amp REVSBECH NP 1993 Nitrification and Denitrification in
Lake and Estuarine Sediments Measured by the N-15 Dilution
Technique and Isotope Pairing Applied and Environmental
Microbiology 59 2093-2098
SAAD O amp CONRAD R 1993 Temperature-Dependence of
Nitrification Denitrification and Turnover of Nitric-Oxide in
Different Soils Biology and Fertility of Soils 15 21-27 http
dxdoiorg101007BF00336283
SANTORO AL amp ENRICH-PRAST A 2011 Regulaccedilatildeo
microbioloacutegica da disponibilidade de nitrogecircnio em ecossistemas
aquaacuteticos continentais Oecologia Australis 15 213-235 http
dxdoiorg104257oeco2011150203
SASAKI H MARUYAMA G SUZUKI H NONAKA
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Characterization of ammonia-assimilating bacteria in a
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3941200200004x
SCHIMEL JP amp GULLEDGE J 1998 Microbial community
structure and global trace gases Global Change Biology 4 745-
758 httpdxdoiorg101046j1365-2486199800195x
SCHMIDT BHM KALBITZ K BRAUN S FUAtildeY
R MCDOWELL WH amp MATZNER E 2011 Microbial
immobilization and mineralization of dissolved organic nitrogen
from forest floors Soil Biology and Biochemistry 43 1742-1745
httpdxdoiorg101016jsoilbio201104021
SCOTT JT MCCARTHY MJ GARDNER WS amp DOYLE
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99-111 httpdxdoiorg101007s10533-007-9171-6
SEITZINGER SP 1988 Denitrification in Fresh-Water and
Coastal Marine Ecosystems - Ecological and Geochemical
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dxdoiorg104319lo1988334_part_20702
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
329
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SEITZINGER S HARRISON JA BOHLKE JK
BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
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208
STOW CA WALKER JT CARDOCH L SPENCE P amp
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TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
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Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
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httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
317
Figura 6 Taxas de produccedilatildeo potencial de N2O determinada pela atividade da enzima desnitrificante As temperaturas de incubaccedilatildeo foram 4 15 20 25 e 37degC durante 20 dias Os dados satildeo meacutedia plusmn EP n=2 (adaptada de Braker et al 2010)
Figure 6 Rates of potential production of N2O determined by denitrifying enzyme activity The incubation temperatures were 4 15 20 25 and 37degC during 20 days Data are mean plusmn SE n=2 (adapted from Braker et al 2010)
Braker et al (2010) verificaram diretamente a influecircncia da temperatura sobre a produccedilatildeo de N2O em solos agriacutecolas corroborando a hipoacutetese de que a temperatura influencia a fisiologia das bacteacuterias desnitrificantes com o aquecimento do ambiente as taxas metaboacutelicas se mostram elevadas produzindo mais N2O ateacute um oacutetimo de temperatura (Figura 6) Embora este resultado tenha sido obtido em solos natildeo eacute de nosso conhecimento um experimento semelhante em sedimento de ambientes aquaacuteticos poreacutem o resultado esperado seria semelhante uma vez que essa regulaccedilatildeo metaboacutelica independe do tipo de sistema
O valor de temperatura oacutetimo para as bacteacuterias nitrificantes e desnitrificantes varia de 25deg a 35degC sendo registradas nessa faixa de temperatura as maiores taxas de atividade (Saad amp Conrad 1993 Braker et al 2010) Entretanto em muitos ambientes onde a temperatura natildeo eacute ideal alcanccedilando valores consideravelmente abaixo ou acima do oacutetimo verificamos a ocorrecircncia de atividade microbiana o que estaacute relacionado agrave capacidade de adaptaccedilatildeo dos microrganismos da comunidade ecoloacutegica em questatildeo a ambientes diferentes do ideal (Saad amp Conrad 1993)
pH
O potencial hidrogeniocircnico (pH) eacute um paracircmetro ambiental crucial para os processos do ciclo do N
atuando por exemplo na proporccedilatildeo NH3NH4+ na
aacutegua Em pH aacutecido ocorre a predominacircncia de NH4+
em detrimento de NH3 ocorrendo o inverso em pH alcalino (De Boer amp Kowalchuk 2001 Bajwa et al 2006) O controle exercido pelo pH sobre a produccedilatildeo de N2O (Conrad 1996 Enwall et al 2005) reflete-se indiretamente atraveacutes do efeito do pH sobre a comunidade bacteriana que pode regular a abundacircncia e diversidade dos microorganismos (Enwall et al 2005)
Como as bacteacuterias nitrificantes tecircm preferecircncia por assimilar NH3 em detrimento do NH4
+ a nitrificaccedilatildeo apresenta taxas mais elevadas em ambientes alcalinos (Kowalchuk amp Stephen 2001 Nugroho et al 2007) Sua influecircncia sobre a produccedilatildeo de N2O pela oxidaccedilatildeo aeroacutebica da amocircnia ainda eacute discutida na literatura devido agrave variaccedilatildeo de dados encontrados (Moslashrkved et al 2007) O processo de nitrificaccedilatildeo heterotroacutefica apresenta alta produccedilatildeo de N2O em pH aacutecido mas natildeo haacute muitos estudos sobre esse processo e sua relaccedilatildeo com o pH (Moslashrkved et al 2007)
O pH tambeacutem atua diretamente sobre as enzimas desnitrificantes oacutexido nitroso redutases que reduz N2O a N2 (Tiedje 1988) cuja atividade aumenta com o aumento do pH do ambiente ateacute alcanccedilar o seu oacutetimo Quando o pH do ambiente eacute baixo a produccedilatildeo da enzima diminui podendo chegar a ficar inativa ocasionando uma elevada produccedilatildeo de N2O (Aumleuhel amp Aringimek 2011) Na medida em que o pH
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
318
aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
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319
em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
320
N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
321
Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
322
VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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Submetido em 13052012Aceito em 23062012
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
318
aumenta a proporccedilatildeo de N2O produzido em relaccedilatildeo ao N2 diminui (Aumleuhel amp Aringimek 2011)
MATEacuteRIA ORGAcircNICA
A relevacircncia da mateacuteria orgacircnica para processos microbianos estaacute relacionada a disponibilidade de compostos orgacircnicos que satildeo fonte de carbono e energia para microrganismos heterotroacuteficos como bacteacuterias desnitrificantes e nitrificantes heterotroacuteficas e como fonte de substrato para os autotroacuteficos como as nitrificantes autotroacuteficas
Para processos microbianos heterotroacuteficos como a desnitrificaccedilatildeo e a nitrificaccedilatildeo heterotroacutefica a presenccedila de mateacuteria orgacircnica no meio eacute um fator regulador limitante Sua disponibilidade no ambiente eacute dependente de carbono orgacircnico para obtenccedilatildeo de energia A labilidade dessa mateacuteria orgacircnica tambeacutem eacute um fator importante para a eficiecircncia desses processos Esse eacute o caso da nitrificaccedilatildeo heterotroacutefica e da desnitrificaccedilatildeo que necessitam da energia oriunda de mateacuteria orgacircnica dissolvida como fonte de energia (Farquharson amp Baldock 2008)
Figura 7 Box-whisker plot das taxas de desnitrificaccedilatildeo em diferentes ecossistemas aquaacuteticos em baixa e alta concentraccedilatildeo de carbono orgacircnico (lt 10mgg-1) Teste de Mann-Whitney comparando os dados de baixo e
alto carbono (adaptada de Pintildea-Ochoa amp Alvares-Cobelas 2006)Figure 7 Box-whisker plot of denitrification rates in different aquatic ecosystems in low and high concentration of organic carbon (lt 10mgg-1) Mann-Whitney test comparing the data of low and high carbon (adapted
from Pintildea-Ochoa amp Alvares-Cobelas 2006)
Na revisatildeo feita por Pintildea-Ochoa amp Alavarez-Cobelas (2006) as taxas de desnitrificaccedilatildeo foram avaliadas de acordo com a disponibilidade de carbono orgacircnico em diferentes ecossistemas aquaacuteticos incluindo oceanos lagos rios e estuaacuterios Em baixas
concentraccedilotildees as taxas foram significativamente inferiores agraves encontradas em ambientes com grande quantidade de carbono (Figura 7) Esse padratildeo encontrado estaacute diretamente relacionado com o fornecimento de substrato para o crescimento bacteriano que aleacutem de estimular o consumo de oxigecircnio permite que o ambiente torne-se anoacutexico e propiacutecio para a desnitrificaccedilatildeo (Seitzinger 1988 Pina-Ochoa amp Alvarez-Cobelas 2006) Todavia a disponibilidade de carbono orgacircnico regula de diferentes maneiras a produccedilatildeo de N2O pois em presenccedila de especiacuteficos substratos de carbono a enzima oacutexido nitroso redutase recebe estiacutemulo diferenciado o que gera uma discrepacircncia entre as taxas de desnitrificaccedilatildeo e a produccedilatildeo efetiva de N2O (Morley amp Baggs 2010)
EMISSAtildeO DE N2O POR AMBIENTES AQUAacuteTICOS
LAGOS E RESERVAacuteTORIOS
Lagos e reservatoacuterios satildeo corpos aquaacuteticos que recebem aporte de aacutegua com mateacuteria orgacircnica e nutrientes advindos de rios e tributaacuterios o que os torna suscetiacuteveis ao processo de eutrofizaccedilatildeo de origem antroacutepica (Huttunen et al 2003 Liikanen amp Martikainen 2003) Segundo Mengis et al (1997) zonas pelaacutegicas aparentemente natildeo contribuem significativamente para a emissatildeo de N2O (Tabela 1) fato que pode ser explicado pela baixa oxigenaccedilatildeo das camadas mais profundas da aacutegua mantendo o sedimento anoacutexico Dessa forma a nitrificaccedilatildeo eacute inibida natildeo produzindo NO3
- e diminuindo a produccedilatildeo de N2O e N2 via desnitrificaccedilatildeo No entanto o aporte terrestre de carbono e nutrientes pode alterar esta condiccedilatildeo (Huttunen et al 2003) A cascata de reservatoacuterios do Rio Tietecirc apresenta uma mudanccedila do estado troacutefico passando de eutroacutefico para oligotroacutefico da nascente para a foz Os reservatoacuterios mais eutroacuteficos apresentam taxas de desnitrificaccedilatildeo significativamente mais elevadas (Abe et al 2003) Como consequecircncia as concentraccedilotildees de N2O na aacutegua destes ambientes tambeacutem satildeo mais elevadas Aleacutem disso observou-se uma variaccedilatildeo temporal nas concentraccedilotildees de N2O nestes reservatoacuterios demonstrando que eles satildeo uma fonte de N2O para atmosfera (Abe et al 2003) A maioria dos poucos estudos existentes em reservatoacuterios e lagos ocorrem
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
319
em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
320
N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
321
Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
322
VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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Soil Biology and Biochemistry 42 1864-1871 httpdxdoi
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Nitrification-denitrification dynamics and community structure
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Applied and Environmental Microbiology 45 444-450
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
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89-97 httpdxdoiorg101007s00248-006-9142-9
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ame019081
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Denitrification in aquatic environments A cross-system analysis
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006-9033-7
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Seasonal variability of denitrification efficiency in northern
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RW 2009 Nitrous oxide (N2O) The dominant ozone-depleting
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Nitrification-Denitrification at the Plant Root-Sediment Interface
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dxdoiorg103354meps164059
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foreco201106002
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httpdxdoiorg101016jsoilbio201104021
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OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
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329
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YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
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ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
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httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
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org105194bg-7-3505-2010
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variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
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Submetido em 13052012Aceito em 23062012
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
319
em ambientes temperados que apresentam baixas taxas de emissatildeo de N2O fazendo com que pouca atenccedilatildeo seja direcionada para esses sistemas se comparado com ecossistemas terrestres (Liu et al 2011)
RIOS
Rios satildeo sistemas loacuteticos onde a aacutegua estaacute em constante movimento devido agrave correnteza que representam uma ligaccedilatildeo entre sistemas terrestres e aquaacuteticos como lagos manguezais estuaacuterios e oceanos (Yang et al 2011) onde nutrientes orgacircnicos e inorgacircnicos bem como gases satildeo transportados das zonas terrestres Muitas vezes zonas agriacutecolas adjacentes aos rios satildeo responsaacuteveis pela eutrofizaccedilatildeo desses ecossistemas atraveacutes da lixiviaccedilatildeo de compostos laacutebeis aplicados ao solo (Kroeze amp Seitzinger 1998)
Essa frequente lixiviaccedilatildeo de diferentes compostos a partir de sistemas terrestres naturais ou artificiais influenciam os processos biogeoquiacutemicos que ocorrem no sedimento e na aacutegua refletindo na taxa de emissatildeo de gases logo no fluxo de N2O (Guimaratildees amp de Mello 2008) Poreacutem poucos estudos tecircm mensurado diretamente o fluxo de N2O em rios (Cole amp Caraco 2001 Clough et al 2011) principalmente em ambientes tropicais (Guimaratildees amp de Mello 2008)
Analisando assim os dados de fluxo de N2O de rios (Tabela 1) verificamos valores de fluxo de N2O bastante variados indo de negativos indicando consumo de N2O atmosfeacuterico e baixos (-96 056 e 24 microg N2O-N m-2 h-1 por exemplo) a valores bastante elevados chegando a 2000 microg N2O-N m-2 h-1 Essa variabilidade aleacutem dos diferentes fatores fiacutesicos e biogeoquiacutemicos de cada rio pode estar atrelada a velocidade da aacutegua grau de turbulecircncia e ao aporte de nitrogecircnio de diferentes origens que podem influenciar a taxa de troca gasosa na interface aacutegua-atmosfera
PLANIacuteCIE DE INUNDACcedilAtildeO
As planiacutecies de inundaccedilatildeo tecircm sido reconhecidas pela sua relevante importacircncia no que diz respeito agrave manutenccedilatildeo da diversidade da fauna e flora bem como a prevenccedilatildeo de alagamentos por reter o excesso de
aacuteguas (Whitaker amp Matvienko 1992) Essas satildeo aacutereas naturais governadas por um regime de inundaccedilatildeo perioacutedico com alternacircncia de niacutevel drsquoaacutegua de cheiaseca A zona litoracircnea desses sistemas satildeo aacutereas-chave (hot spots) para a produccedilatildeo e emissatildeo de N2O pois o solo exposto eacute oxigenado na eacutepoca da seca quando ocorre o processo de nitrificaccedilatildeo ocasionando muitas vezes o acuacutemulo de NO3
- no solo Quando este solo eacute inundado acaba por ficar anoacutexico o que proporciona as condiccedilotildees ideais para o processo de desnitrificaccedilatildeo consumir o NO3
- acumulado Como consequumlecircncia deste processo tambeacutem ocorre a produccedilatildeo de N2O (Figueiredo 2012) Aleacutem disso as chuvas no periacuteodo da seca tambeacutem permitem que haja produccedilatildeo de N2O tanto pela nitrificaccedilatildeo incompleta quanto pela desnitrificaccedilatildeo Isso mostra a regulaccedilatildeo exercida pelo ciclo perioacutedico das aacuteguas sobre os processos microbianos (Akatsuka amp Mitamura 2010) em um tipo de ecossistema que apresenta grande disponibilidade de mateacuteria orgacircnica aloacutectone e autoacutectone (Alho et al 1988) A presenccedila dessa mateacuteria orgacircnica estimula a desnitrificaccedilatildeo e com isso a emissatildeo de N2O (Metay et al 2011)
MANGUEZAL E ESTUAacuteRIO
Tambeacutem sob influecircncia constante de aacuteguas ambientes costeiros como os manguezais estuaacuterios e marismas tecircm recebido maior atenccedilatildeo no que diz respeito ao papel dos microorganismos no ciclo do N diante do aumento da eutrofizaccedilatildeo de ambientes marinhos (Rysgaard et al 1993 Fernandes et al 2010) Em aacutereas de manguezal os nutrientes nitrogenados (NH4
+ e NO3-) disponibilizados pelas
aacuteguas costeiras regulam a atividade de bacteacuterias nitrificantes e desnitrificantes pois a variaccedilatildeo do niacutevel drsquoaacutegua eacute constante e diaacuteria Aleacutem disso a temperatura se mostra um fator abioacutetico determinante nos processos do ciclo do N nesses sistemas (Poulin et al 2007) que estatildeo localizados em sua maioria nas aacutereas tropicais Outra questatildeo que deve ser destacada eacute o fato dos sedimentos de manguezais serem anaeroacutebicos uma vez que satildeo encharcados a maior parte do tempo e como seu sedimento apresenta elevadas concentraccedilotildees de mateacuteria orgacircnica o processo de desnitrificaccedilatildeo eacute favorecido Fernandes et al (2010) demonstraram que a desnitrificaccedilatildeo era o principal processo responsaacutevel pela produccedilatildeo de
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
320
N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
321
Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
322
VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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immobilization and mineralization of dissolved organic nitrogen
from forest floors Soil Biology and Biochemistry 43 1742-1745
httpdxdoiorg101016jsoilbio201104021
SCOTT JT MCCARTHY MJ GARDNER WS amp DOYLE
RD 2008 Denitrification dissimilatory nitrate reduction to
ammonium and nitrogen fixation along a nitrate concentration
gradient in a created freshwater wetland Biogeochemistry 87
99-111 httpdxdoiorg101007s10533-007-9171-6
SEITZINGER SP 1988 Denitrification in Fresh-Water and
Coastal Marine Ecosystems - Ecological and Geochemical
Significance Limnology and Oceanography 33 702-724 http
dxdoiorg104319lo1988334_part_20702
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
329
SEITZINGER SP amp KROEZE C 1998 Global distribution of
nitrous oxide production and N inputs in freshwater and coastal
marine ecosystems Global Biogeochemical Cycles 12 93-113
httpdxdoiorg10102997GB03657
SEITZINGER S HARRISON JA BOHLKE JK
BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
320
N2O no manguezal de Goa Iacutendia Estima-se que o fluxo de N2O oriundo de manguezais corresponda a
13 do fluxo total global da aacuterea coberta por estuaacuterios (Corredor et al 1999)
Tabela 1 Fluxos de N2O em ecossistemas aquaacuteticos ou influenciados por aacutegua (microg N2O-N m-2 h-1) C (carbono ) N (nitrogecircnio ) (adaptada de Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Table 1 N2O fluxes in aquatic ecosystems influenced by water (microg N2O-N m-2 h-1)C (carbon ) N (nitrogen ) (adapted from Huttunen et al 2003 Mengis et al 1997 Allen et al 2011 Zhang et al 2010 e Liu et al 2011)
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
Rio Brisbane Rio Logan Baiacutea Moreton oeste e leste QueeslandAustraacutelia
Manguezal - - -
sup1283plusmn 22 a 2019plusmn298
Allen et al 2011sup265plusmn15 a 265plusmn15
QueeslandAustraacutelia Manguezal - - --2 a 14
Kreuzwieser et al 2003-3 a 13
MuthupetIacutendia Manguezal 73 - - 262 Krithika et al 2008
Rio Brisbane QueeslandAustraacutelia Rio - - - 5 a 68 Allen et al 2007
Bird IslandPorto Rico Manguezal - - - 3423 Corredor et al 1999
STPPorto RicoManguezal com
despejo de esgoto tratado
- - - 53 Corredor et al 1999
Recife EnriquePorto Rico Recife de coral - - - 11 Corredor et al 1999
Tuven GoaIacutendia Manguezal - 358 - 1320 Fernandes et al 2010
Divar GoaIacutendia Manguezal - 316 - 4400 Fernandes et al 2010
Costa sudoestePorto Rico Manguezal - - - 208 Munoz-Hincapie et al 2002
Ilha de MagueyesPorto Rico Manguezal - - - 225 Bauza et al 2002
Peninsula de MorningtonAustraacutelia Manguezal - - - lt3 Livesley amp Andrusiak 2012
MarshlandChina Aacuterea Pantanosa 74 - - 218 Yao et al 2010
Estuaacuterio TamarIngralerra Estuaacuterio - - - 1364 a 484 Law et al 1992
ChangjangChina Estuaacuterio - - -396
Zhang et al 201077
ColneInglaterra Estuaacuterio - - - 3998 Robinson et al 1998
Rio SenaParis RioEstuaacuterio - - - 221 a 571 Garnier et al 2006
YangtzeChina Estuaacuterio - - - 4480 Wang et al 2009
Rio HudsonEUA Rio - - - 32 Cole amp Caraco 2001
Rio ColneInglaterra Rio - - - 056 a 24 Dong et al 2002
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
321
Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
322
VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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Submetido em 13052012Aceito em 23062012
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
321
Rio SwaleouseInglaterra Rio - - - 196 a 1400 Garciacutea-Ruiz et al 1999
Rio South PlateEUA Rio - - - 38 a 1358 McMahon amp Dennehy 1999
Rio NeuseEUA Rio - - - -84 a 644 Stow et al 2005
Rio NafeiChina Rio - - - 2368 Yang et al 2011
Rio FengleChina Rio - - - 287 Yang et al 2011
Rio HangbuChina Rio - - - 116 Yang et al 2011
Rio HangouChina Rio - - - 2212 Wang et al 2009
Rio TemmesjokiFinlacircndia Rio - - - -96 a 604 Silvennoinen et al 2008
Sitka streamRepuacuteblica Tcheca Riacho - - - 354 Hlavacova et al 2006
Rio AshburtonNova Zelacircndia Rio - - - 23 Clought et al 2011
JiaozhouChina Baiacutea - - -54
Zhang et al 2006111
TokyoJapatildeo Baiacutea - - - 088 a 8925 Hashimoto et al 1999
Baiacutea de GuanabaraBrasil Baiacutea 85 - - 165 Guimaratildees amp de Mello 2008
HongjaduChina Reservatoacuterio - - - 63 Liu et al 2011
WujiangduChina Reservatoacuterio - - - 89 Liu et al 2011
IbitingaBrasil Reservatoacuterio - - - 28287 Abe et al 2003
PromissatildeoBrasil Reservatoacuterio - - - 799 Abe et al 2003
Barra BonitaBrasil Reservatoacuterio - - - 255 Abe et al 2003
LokkaFinlacircndia Reservatoacuterio - - -05
Huttunen et al 2003385
PorttipahtaFinlacircndia Reservatoacuterio - - - 476 Huttunen et al 2003
Jaumlnkaumllaumlisenlampi PondFinlacircndia Reservatoacuterio - - - 063 Huttunen et al 2003
Kotsamolampi PondFinlacircndia Reservatoacuterio - - - 026 Huttunen et al 2003
Three GorgesChina Reservatoacuterio - - - 155 Chen et al 2003
LokkaFinlacircndia Reservatoacuterio - - - -37 a 1125 Huttunen et al 2003
Lago BiwaJapatildeo Lago - - - lt 0001 Akatsuka et al 2010
Lago NakawiJapatildeo Lago 62 - - -6 a 13 Hirota et al 2007
OkaroNova Zelacircndia Lago - - - 035 Downes 1991
KevatonFinlacircndia Lago - - - 126 a 7 Huttunen et al 2003
PostilampiFinlacircndia Lago - - --02
Huttunen - dados natildeo publicados088
PostilampiFinlacircndia Lago - - - 128 Huttunen et al 2003
HeinaumllampiFinlacircndia Lago - - - 33 Huttunen - dados natildeo publicados
KevaumltonFinlacircndia Lago - - --102
Huttunen - dados natildeo publicados-029
Continuaccedilatildeo Tabela 1
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
322
VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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microbioloacutegica da disponibilidade de nitrogecircnio em ecossistemas
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J SATO M SASAKI T OHTA M amp NAKAI Y 2002
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OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
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Submetido em 13052012Aceito em 23062012
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
322
VehmasjaumlrviFinlacircndia Lago - - --0238
Huttunen - dados natildeo publicados108
MaumlkijaumlrviFinlacircndia Lago - - --044
Huttunen - dados natildeo publicados385
MochouAntartica Lago 55 064 011 31plusmn67 Liu et al 2011
TuanjieAntartica Lago 55 6 102 25plusmn28 Liu et al 2011
DamingAntartica Lago 63 264 008 72plusmn68 Liu et al 2011
Baiacutea NarragansettEUA Costa - - - 044 a 4048 Seitzinger amp Kroeze 1998
Baiacutea TampaEUA Costa - - - 418 Nishio et al 1983
Baiacutea de TokyoJapatildeo Costa - - - 264 a 308 Koike amp Terauchi 1996
ErnestEUA Lago - - - 154 Seitzinger amp Kroeze 1998
LacawacEUA Lago - - - 176 Seitzinger amp Kroeze 1998
Alpnacher SeeSuiacuteccedila Lago - - - 396 Mengis et al 1997
Brienzer SeeSuiacuteccedila Lago - - - 3696 Mengis et al 1997
Lac de NeuchacirctelAlemanha Lago - - - 044 Mengis et al 1997
Walen SeeSuiacuteccedila Lago - - - 1364 Mengis et al 1997
Baldegger SeeSuiacuteccedila Lago eutroacutefico - - - 132 a 308 Mengis et al 1996
Local Ecossistema pH H2O C N Fluxo de N2O Referecircncia
sup1Coletas realizadas no veratildeo sup2Coletas realizadas no inverno Dados referentes a coletas de ano diferentes quando realizadas pelo mesmo autor e sistema aquaacutetico
Continuaccedilatildeo Tabela 1
Comparaccedilatildeo entre ecossistemas
A Tabela 1 mostra os valores de emissatildeo de N2O que apresentam grande diferenccedila entre si sendo esta de ateacute quatro ordens de magnitude Esta variabilidade tatildeo acentuada pode estar relacionada agrave quantidade de mateacuteria orgacircnica e nutrientes que esses sistemas recebem de origem natural ou antroacutepica uma vez que esses ambientes tecircm variados estados troacuteficos que alteram a produccedilatildeo de N2O (Mengis et al 1997) Aleacutem disso provavelmente encontramos diferenccedilas metodoloacutegicas entre os artigos analisados o que pode afetar os valores observados Entretanto essa imensa variabilidade enfatiza a importacircncia dos fatores reguladores controlando o fluxo individualmente em cada sistema uma vez que caracteriacutesticas fiacutesico-quiacutemicas satildeo particulares a cada ambiente principalmente em ecossistemas
fechados como eacute o caso de lagos e reservatoacuterios (Allen et al 2011)
As taxas de emissatildeo de N2O em diferentes sistemas aquaacuteticos continentais foram comparadas entre si (Tabela 1) Atraveacutes de um teste de normalidade (Kolmogorov-Smirnov) verificamos que os dados satildeo natildeo parameacutetricos e para comparaacute-los estatisticamente utilizamos o Teste natildeo parameacutetrico de Kruskall-Wallis (plt005) com Poacutes-Teste de Dunn (Figura 8) Dessa maneira verificamos que os valores de emissatildeo de N2O de lagos satildeo significativamente diferentes (n=26 ANOVA plt005) de manguezais estuaacuterios e rios (n=14 7 e 12 respectivamente) que natildeo diferiram significativamente entre si (ANOVA pgt005) O mesmo ocorreu para reservatoacuterios (n=12) que apresentam a maioria dos valores absolutos na mesma faixa dos valores de lagos Com isso lagos e reservatoacuterios emitem menos que os demais sistemas aquaacuteticos
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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Submetido em 13052012Aceito em 23062012
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
323
Diante da influecircncia dos fatores reguladores sobre o fluxo de N2O que vimos acima podemos entender porque em lagos grande parte dos dados de fluxo de N2O eacute reduzido com valores variando entre -1 e 39microg N2O-Nm-2h-1 Aleacutem disso encontramos valores de fluxo elevados para lagos com ordem de grandeza semelhante agrave dos manguezais Poreacutem satildeo poucos os dados com elevado valor de emissatildeo (3696microg N2O-N m-2h-1) em lagos enquanto que em manguezais notamos que grande parte dos valores eacute mais elevada (apesar de um menor nuacutemero de dados compilados) Isto indica uma influecircncia positiva da variaccedilatildeo do niacutevel drsquoaacutegua do mar sobre a produccedilatildeo e emissatildeo de N2O Os fluxos de reservatoacuterios seguiram um padratildeo de emissatildeo semelhante ao encontrado para lagos uma vez que satildeo sistemas semelhantes
Lago
Reserv
atoacuterio
Manguez
al
Estuaacuteri
o Rio-505
101520253035404550
1200240036004800
plt005
a
ab
b b
b
200
Flux
o de
N2O
(microg
N 2O
-N m
-2 h
-1)
Figura 8 Fluxos de N2O (microg N2O-N m-2 h-1) de sistemas sob influecircncia permanente ou temporaacuteria de aacutegua de diversas localidades do mundo calculados com dados apresentados na Tabela 1 Siacutembolos representam a mediana de cada grupo e barras representam a faixa de interquartis (25-75) lago (ciacuterculo n=26 32 026-1153) reservatoacuterio (quadrado n=12 4305 111-8673) manguezal (triacircngulo n=14 2215 521-1719) estuaacuterio (triacircngulo invertido n=7 396 77-2212) rio
(losango n=12 3205 1445-570) Figure 8 N2O fluxes (microg N2O-N m-2 h-1) of systems under permanent or temporary water influence from various localities around the world calculated using data presented in the Table 1 Symbols represent the median of each group and bars represent interquartile range (25-75) lake (circle n=26 32 026-1153 ) reservoir (square n=12 4305 111-8673) mangrove (triangle n=14 2215 521-1719) estuary (inverted triangle n=7 396 77-2212) river (lozenge n=12 3205
1445-570)
Os maiores valores de fluxo de N2O foram observados em estuaacuterios e manguezais seguido dos valores de rios Em manguezais e estuaacuterios o grau de oxigenaccedilatildeo do sedimento eacute bastante variaacutevel ao longo
do dia devido agrave alternacircncia do niacutevel de mareacute aleacutem de outros paracircmetros que tambeacutem variam como pH e concentraccedilatildeo de nutrientes Nestes ecossistemas a produccedilatildeo interna de NO3
- principal fator regulador da desnitrificaccedilatildeo estaacute relacionada agrave presenccedila de oxigecircnio que apresenta uma maior variabilidade No caso dos lagos e reservatoacuterios estes muitas vezes apresentam condiccedilotildees anoacutexicas proacuteximas ao sedimento fato que inibe a produccedilatildeo de NO3
- via nitrificaccedilatildeo (processo aeroacutebico) Este resultado sugere que a variaccedilatildeo da coluna drsquoaacutegua aparentemente favorece a ocorrecircncia de condiccedilotildees para produccedilatildeo e emissatildeo de N2O
Tambeacutem deve ser considerado o fato de que manguezais e estuaacuterios recebem grande aporte de nitrogecircnio de origem externa (despejo de esgoto e entrada de aacutegua do mar e rio) e de origem interna (floresta de mangue) que podem favorecer e fornecer substrato para os processos formadores de N2O (Fernandes et al 2010) Lagos e reservatoacuterios satildeo ambientes mais estaacuteveis do que manguezais estuaacuterios e rios e esta caracteriacutestica faz com que a variabilidade em fatores como pH e concentraccedilotildees de nutrientes seja menor favorecendo uma maior estabilidade de processos e consequentemente uma menor produccedilatildeo e emissatildeo de N2O
AGRADECIMENTOS Esse estudo contou com o apoio financeiro do CNPq CAPES e PETROBRAS aleacutem da colaboraccedilatildeo do ProfDr Ralf Conrad do Instituto Max Planck (MarburgAlemanha)
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formation in the Colne Estuary England the central role of
nitrite Applied and Environmental Microbiology 68 1240-1249
httpdxdoiorg101128AEM6831240-12492002
DOWNES MT 1991 The production and consumption of
nitrate in an eutrophic lake during early stratification Archiv Fur
Hydrobiologie 122 257-274
ENWALL K PHILIPPOT L amp HALLIN S 2005 Activity
and composition of the denitrifying bacterial community respond
differently to long-term fertilization Applied and Environmental
Microbiology 71 8335-8343 httpdxdoiorg101128
AEM71128335-83432005
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modelling N2O emissions from land use Plant and Soil 309147-
167 httpdxdoiorg101007s11104-007-9485-0
FENNEL K BRADY D DITORO D FULWEILER RW
GARDNER WS GIBLIN A MCCARTHY MJ RAO
A SEITZINGER S THOUVENOT-KORPPOO M amp
TOBIAS C 2009 Modeling denitrification in aquatic sediments
Biogeochemistry 93 159-178 httpdxdoiorg101007s10533-
008-9270-z
FERNANDES SO BHARATHI PAL BONIN PC amp
MICHOTEY VD 2010 Denitrification An Important Pathway
for Nitrous Oxide Production in Tropical Mangrove Sediments
(Goa India) Journal of Environmental Quality 39 1507-1516
httpdxdoiorg102134jeq20090477
FIENCKE C SPIECK E amp BOCK E 2006 Nitrifying
Bacteria Pp 255-276 In D Werner amp WE Newton (eds)
Nitrogen Fixation in Agriculture Forestry Ecology and the
Environment Springer Netherlands Amsterdam 371p
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emissotildees de oacutexido nitroso (N2O) em aacutereas tropicais Dissertaccedilatildeo
de Mestrado Universidade Federal do Rio de Janeiro Rio de
Janeiro RJ Brasil 90p
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T BETTS R FAHEY DW HAYWOOD J LEAN J
LOWE DC MYHRE G NGANGA J PRINN R RAGA
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atmospheric constituents and in radiative forcing Pp 129-234
In S Solomon D Qin M Manning Z Chen M Marquis
KB Averty M Tignor amp HL Miller (eds) Climate Change
2007 The physical science basis Cambridge University Press
Cambridge Reino Unido e Nova York 1008p
FRAME CH amp CASCIOTTI KL 2010 Biogeochemical
controls and isotopic signatures of nirous oxide production by a
marine ammonia-oxidizing bacterium Biogeosciences 7 2695-
2709
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1999 Nitrous oxide production in the river swale-ouse North-
East England Water Research 33 1231-1237
GARNIER J CEacuteBRON A TALLEC G BILLEN G
SEBILO M amp MARTINEZ A 2006 Nitrogen behavior and
nitrous oxide emission in the tidal Seine River estuary (France)
as influenced by human activities in the upstream watershed
Biogeochemistry 77 305-326 httpdxdoiorg101007s10533-
005-0544-4
GODDE M amp CONRAD R 1999 Immediate and adaptational
temperature effects on nitric oxide production and nitrous oxide
release from nitrification and denitrification in two soils Biology
and Fertility of Soils 30 33-40 httpdxdoiorg101007
s003740050584
GUIMARAtildeES M amp DE MELLO WZ 2008 Nitrous oxide
fluxes ate the air-sea interface in Guanabara bay Quiacutemica Nova
31 1613-1620
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in aerobic rice use of soil properties to predict ammonia
volatilization following urea application and the adverse effects
on germination European Journal of Soil Science 62 551-559
httpdxdoiorg101111j1365-2389201001346x
HARRISON JA MATSON PA amp FENDORF SE 2005
Effects of a diel oxygen cycle on nitrogen trsnformations and
greenhouse gas emissions in a eutrophied subtropical stream
Aquatic Sciences 67 308-315 httpdxdoiorg101007s00027-
005-0776-3
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
326
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two contrastive fringing zones of coastal lagoon Lake Nakaumi
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DE BOER W amp KOWALCHUK GA 2001 Nitrification in
acid soils micro-organisms and mechanisms Soil Biology and
Biochemistry 33 853-866 httpdxdoiorg101016S0038-
0717(00)00247-9
DONG LF NEDWELL DB UNDERWOOD GJC
THORNTON DCO amp RUSMANA I 2002 Nitrous oxide
formation in the Colne Estuary England the central role of
nitrite Applied and Environmental Microbiology 68 1240-1249
httpdxdoiorg101128AEM6831240-12492002
DOWNES MT 1991 The production and consumption of
nitrate in an eutrophic lake during early stratification Archiv Fur
Hydrobiologie 122 257-274
ENWALL K PHILIPPOT L amp HALLIN S 2005 Activity
and composition of the denitrifying bacterial community respond
differently to long-term fertilization Applied and Environmental
Microbiology 71 8335-8343 httpdxdoiorg101128
AEM71128335-83432005
FARQUHARSON R amp BALDOCK J 2008 Concepts in
modelling N2O emissions from land use Plant and Soil 309147-
167 httpdxdoiorg101007s11104-007-9485-0
FENNEL K BRADY D DITORO D FULWEILER RW
GARDNER WS GIBLIN A MCCARTHY MJ RAO
A SEITZINGER S THOUVENOT-KORPPOO M amp
TOBIAS C 2009 Modeling denitrification in aquatic sediments
Biogeochemistry 93 159-178 httpdxdoiorg101007s10533-
008-9270-z
FERNANDES SO BHARATHI PAL BONIN PC amp
MICHOTEY VD 2010 Denitrification An Important Pathway
for Nitrous Oxide Production in Tropical Mangrove Sediments
(Goa India) Journal of Environmental Quality 39 1507-1516
httpdxdoiorg102134jeq20090477
FIENCKE C SPIECK E amp BOCK E 2006 Nitrifying
Bacteria Pp 255-276 In D Werner amp WE Newton (eds)
Nitrogen Fixation in Agriculture Forestry Ecology and the
Environment Springer Netherlands Amsterdam 371p
FIGUEIREDO VF 2012 Influecircncia da inundaccedilatildeo sobre
emissotildees de oacutexido nitroso (N2O) em aacutereas tropicais Dissertaccedilatildeo
de Mestrado Universidade Federal do Rio de Janeiro Rio de
Janeiro RJ Brasil 90p
FORSTER P RAMASWAMY V ARTAXO P BERNTSEN
T BETTS R FAHEY DW HAYWOOD J LEAN J
LOWE DC MYHRE G NGANGA J PRINN R RAGA
G SCHULZ M amp VAN DORLAND R 2007 Changes in
atmospheric constituents and in radiative forcing Pp 129-234
In S Solomon D Qin M Manning Z Chen M Marquis
KB Averty M Tignor amp HL Miller (eds) Climate Change
2007 The physical science basis Cambridge University Press
Cambridge Reino Unido e Nova York 1008p
FRAME CH amp CASCIOTTI KL 2010 Biogeochemical
controls and isotopic signatures of nirous oxide production by a
marine ammonia-oxidizing bacterium Biogeosciences 7 2695-
2709
GARCIacuteA-RUIZ R PATTINSON SN amp WHITTON BA
1999 Nitrous oxide production in the river swale-ouse North-
East England Water Research 33 1231-1237
GARNIER J CEacuteBRON A TALLEC G BILLEN G
SEBILO M amp MARTINEZ A 2006 Nitrogen behavior and
nitrous oxide emission in the tidal Seine River estuary (France)
as influenced by human activities in the upstream watershed
Biogeochemistry 77 305-326 httpdxdoiorg101007s10533-
005-0544-4
GODDE M amp CONRAD R 1999 Immediate and adaptational
temperature effects on nitric oxide production and nitrous oxide
release from nitrification and denitrification in two soils Biology
and Fertility of Soils 30 33-40 httpdxdoiorg101007
s003740050584
GUIMARAtildeES M amp DE MELLO WZ 2008 Nitrous oxide
fluxes ate the air-sea interface in Guanabara bay Quiacutemica Nova
31 1613-1620
HADEN VR XIANG J PENG S KETTERINGS QM
HOBBS P amp DUXBURY JM 2011 Ammonia toxicity
in aerobic rice use of soil properties to predict ammonia
volatilization following urea application and the adverse effects
on germination European Journal of Soil Science 62 551-559
httpdxdoiorg101111j1365-2389201001346x
HARRISON JA MATSON PA amp FENDORF SE 2005
Effects of a diel oxygen cycle on nitrogen trsnformations and
greenhouse gas emissions in a eutrophied subtropical stream
Aquatic Sciences 67 308-315 httpdxdoiorg101007s00027-
005-0776-3
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
326
HASHIMOTO S GOJO K SENDAI N amp OTSUKI A
1999 Nitrous oxide emission from coastal Waters in Tokyo Bay
Marine Environmental Research 47 213-223
HAYATSU M TAGO K amp SAITO M 2008 Various players in
the nitrogen cycle Diversity and functions of the microorganisms
involved in nitrification and denitrification Soil Science and
Plant Nutrition 54 33-45 httpdxdoiorg101111j1747-
0765200700195x
HIROTA M SENGA Y SEIKE Y NOHARA S amp KUNII
H 2007 Fluxes of carbon dioxide methane and nitours oxide in
two contrastive fringing zones of coastal lagoon Lake Nakaumi
Japan Chemosphere 68 597-603 httpdxdoiorg101016j
chemosphere200701002
HLAVAacuteCOVAacute E RULIacuteK M CAacuteP L amp MACH V 2006
Greenhouse gas (CO2 CH4 N2O) emissions to the atmosphere
from a small lowland stream in Czech Republic Archiv fur
Hydrobiologie 165 339-353 httpdxdoiorg1011270003-
913620060165-0339
HUTTUNEN JT ALM J LIIKANEN A JUUTINEN S
LARMOLA T HAMMAR T SILVOLA J amp MARTIKAINEN
PJ 2003 Fluxes of methane carbon dioxide and nitrous oxide
in boreal lakes and potential anthropogenic effects on the
aquatic greenhouse gas emissions Chemosphere 52 609-621
httpdxdoiorg101016S0045-6535(03)00243-1
INSELSBACHER E UMANA NHN STANGE FC
GORFER M SCHUumlLLER E RIPKA K ZECHMEISTER-
BOLTENSTERN S HOOD-NOVOTNY R STRAUSS J
amp WANEK W 2010 Short-term competition between crop
plants and soil microbes for inorganic N fertilizer Soil Biology
and Biochemistry 42 360-372 httpdxdoiorg101016j
soilbio200911019
IPCC (Intergovernmental Panel on Climate Change) 2001
Climate Change 2001 Impacts Adaptation and Vulnerability
Cambridge University Press Reino Unido e Nova York 1042p
IPCC (Intergovernmental Panel on Climate Change) 2007
Climate Change 2007 The Physical Science Basis Cambridge
University Press Reino Unido e Nova York 1008p
JAYAWEERA GR amp MIKKELSEN DS 1991 Assessment Of
Ammonia Volatilization From Flooded Soil Systems Advances
in Agronomy 45 303-356 httpdxdoiorg101016S0065-
2113(08)60044-9
JOHN R DALLING JW HARMS KE YAVITT JB
STALLARD RF MIRABELLO M HUBBELL SP
VALENCIA R NAVARRETE H VALLEJO M amp FOSTER
RB 2007 Soil nutrients influence spatial distributions of tropical
tree species Proceedings of the National Academy of Sciences
of the United States of America 104 864-869 httpdxdoi
org101073pnas0604666104
JOHNSON MT LISS PS BELL TG LESWORTH TJ
BAKER AR HIND AJ JICKELLS TD BISWAS KF
WOODWRAD EMS amp GIBB SW 2008 Field observations
of the ocean-atmosphere exchange of ammonia Fundamental
importance of temperature as revealed by a comparison of high
and low latitudes Global Biogeochemical Cycles 22 GB1019
httpdxdoiorg1010292007GB003039
KAMPSCHEREUR MJ TEMMINK H KLEEREBEZEM
R JETTEN MSM amp VAN LOOSDRECHT MCM
2009 Nitrous oxide emission during wastewater treatment
Water Research 43 4093-4103 httpdxdoiorg101016j
watres200903001
KOIKE I amp TERAUCHI K 1996 Fine scale distribution
of nitrous oxide in marine sediments Marine Chemistry 52
185-193
KOOL DM DOLFING J WRAGE N amp VAN GROENIGEN
JW 2011 Nitrifier denitrification as a distinct and significant
source of nitrous oxide from soil Soil Biology Biochemistry 43
174-178 httpdxdoiorg101016jsoilbio201009030
KOWALCHUK GA amp STEPHEN JR 2001 Ammonia-
oxidizing bacteria A model for molecular microbial ecology
Annual Review of Microbiology 55 485-529 httpdxdoi
org101146annurevmicro551485
KREMEN A BEAR J SHAVIT U amp SHAVIV A 2005
Model demonstrating the potencial for coupled nitrification
denitrification in soil aggregates Environmental Science
Technology 39 4180-4188 httpdxdoiorg101021es048304z
KREUZWIESER J BUCHOLZ J amp RENNENBERG H
2003 Emission of methane and nitrous oxide by Australian
mangrove ecosystems Plant Biology 5 423-431
KRITHIKA K PURVAJA R amp RAMESH R 2008 Fluxes
of methane and nitrous oxide from an Indian mangrove Current
Science 94 218-224
KROEZE C amp SEITZINGER SP 1998 Nitrogen inputs
to rivers estuaries and continental shelves and related
nitrous oxide emissions in 1990 and 2050 a global model
Nutrient Cycling Agroecosystems 52 195-212 httpdxdoi
org101023A1009780608708
KUSCHK P WIESSNER A KAPPELMEYER U
WEISSBRODT E KASTNER M amp STOTTMEISTER
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
327
U 2003 Annual cycle of nitrogen removal by a pilot-scale
subsurface horizontal flow in a constructed wetland under
moderate climate Water Research 37 4236-4242 httpdxdoi
org101016S0043-1354(03)00163-5
LAW CS REES AP amp OWENS NJP 1992 Nitrous oxide
Estuarine sources and atmospheric flux Estuarine Coastal and
Shelf Science 35 301-314 httpdxdoiorg101016S0272-
7714(05)80050-2
LIIKANEN A amp MARTIKAINEN PJ 2003 Effect of
ammonium and oxygen on methane and nitrous oxide
fluxes across sediment-water interface in a eutrophic lake
Chemosphere 52 1287-1293 httpdxdoiorg101016S0045-
6535(03)00224-8
LIU Y ZHU R MA D XU H LUO Y HUANG T amp
SUN L 2011 Temporal and spatial variations of nitrous oxide
fluxes from the littoral zones of three alga-rich lakes in coastal
Antarctica Atmospheric Environment 45 1464-1475 http
dxdoiorg101016jatmosenv201012017
LIVESLEY S amp ANDRUSIAK SM 2012 Temperate mangrove
and salt marsh sediments are a small methane and nitrous oxide
source but important carbon store Estuarine Coastal and Shelf
Science 97 19-27 httpdxdoiorg101016jecss201111002
LORENZEN J LARSEN LH KJAER T amp REVSBECH
NP 1998 Biosensor determination of the microscale distribution
of nitrate nitrate assimilation nitrification and denitrification
in a diatom-inhabited freshwater sediment Applied and
Environmental Microbiology 64 3264-3269
MA WK BEDARD-HAUGHN A SICILIANO SD amp
FARRELL RE 2008 Relationship between nitrifier and
denitrifier community composition and abundance in predicting
nitrous oxide emissions from ephemeral wetland soils Soil
Biology Biochemistry 40 1114-1123 httpdxdoiorg101016j
soilbio200712004
MALHI SS MCGILL WB amp NYBORG M 1990 Nitrate
losses in soils Effect of temperature moisture and substrate
concentration Soil Biology and Biochemistry 22 733-737
httpdxdoiorg1010160038-0717(90)90150-X
MAMILOV AS amp DILLY OM 2002 Soil microbial eco-
physiology as affected by short-term variations in environmental
conditions Soil Biology and Biochemistry 34 1283-1290 http
dxdoiorg101016S0038-0717(02)00071-8
MCCLAIN ME BOYER EW DENT CL GERGEL SE
GRIMM NB GROFFMAN PM HART SC HARVEY
JW JOHNSTON CA MAYORGA E MCDOWELL WH
amp PINAY G 2003 Biogeochemical hot spots and hot moments
at the interface of terrestrial and aquatic ecosystems Ecosystems
6 301-312 httpdxdoiorg101007s10021-003-0161-9
MCMAHON PB amp DENNEHY KF 1999 N2O emissions from
a nitrogen-enriched river Environmental Science Technology 33
21-25 httpdxdoiorg101021es980645n
MENGIS M GACHTER R amp WEHRLI B 1996 Nitrous
oxide emissions to the atmosphere from an artificially oxygenated
lake Limnology and Oceanography 41 548-553
MENGIS M GACHTER R amp WEHRLI B 1997 Sources and
sinks of nitrous oxide (N2O) in deep lakes Biogeochemistry 38
281-301 httpdxdoiorg101023A1005814020322
METAY A CHAPUIS-LARDY L FINDELING A OLIVER
R MOREIRA JAA amp FELLER C 2011 Simulating N2O
fluxes from a Brazilian cropped soil with contrasted tillage
practices Agriculture Ecosystems amp Environment 140 255-263
httpdxdoiorg101016jagee201012012
MILLER AE SCHIMEL JP SICKMAN JO SKEEN
K MEIXNER T amp MELACK JM 2009 Seasonal variation
in nitrogen uptake and turnover in two high-elevation soils
mineralization responses are site-dependent Biogeochemistry
93 253-270 httpdxdoiorg101007s10533-009-9301-4
MOslashRKVED PT DOumlRSCH P amp BAKKEN LR 2007 The
N2O product ratio of nitrification and its dependence on long-term
changes in soil pH Soil Biology and Biochemistry 39 2048-
2057 httpdxdoiorg101016jsoilbio200703006
MORLEY N amp BAGGS EM 2010 Carbon and oxygen
controls on N2O and N2 production during nitrate reduction
Soil Biology and Biochemistry 42 1864-1871 httpdxdoi
org101016jsoilbio201007008
MUNtildeOZ-HINCAPIEacute M MORELL JM amp CORREDOR
JE 2002 Increase of nitrous oxide flux to the atmosphere upon
nitrogen addition to red mangroves sediments Marine Pollution
Bulletin 44 992-996
NICOLAISEN MH RISGAARD-PETERSEN N
REVSBECH NP REICHARDT W amp RAMSING NB 2004
Nitrification-denitrification dynamics and community structure
of ammonia oxidizing bacteria in a high yield irrigated Philippine
rice filed FEMS Microbiology Ecology 49 359-369 http
dxdoiorg101016jfemsec200404015
NISHIO T KOIKE I amp HATTORI A 1983 Estimates of
denitrification and nitrification in coastal and estuarine sediments
Applied and Environmental Microbiology 45 444-450
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
328
NUGROHO RA ROLING WFM LAVERMAN AM amp
VERHOEF HA 2007 Low nitrification rates in acid scots pine
forest soils are due to pH-related factors Microbial Ecology 53
89-97 httpdxdoiorg101007s00248-006-9142-9
OTTOSEN LDM RISGAARD-PETERSEN N amp NIELSEN
LP 1999 Direct and indirect measurements of nitrification
and denitrification in the rhizosphere of aquatic macrophytes
Aquatic Microbial Ecology 19 81-91 httpdxdoiorg103354
ame019081
PEREZ T GARCIA-MONTIEL D TRUMBORE S
TYLER S DE CAMARGO P MOREIRA M PICCOLO M
amp CERRI C 2006 Nitrous oxide nitrification and denitrification
N-15 enrichment factors from Amazon forest soils Ecological
Applications 16 2153-2167 httpdxdoiorg1018901051-
0761(2006)016[2153NONADN]20CO2
PILEGAARD K SKIBA U AMBUS P BEIER C
BRUGGEMANN N BUTTERBACH-BAHL K DICK
J DORSEY J DUYZER J GALLAGHER M GASCHE
R HORVATH L KITZLER B LEIP A PIHLATIE MK
ROSENKRANZ P SEUFERT G VESALA T WESTRATE
H amp ZECHMEISTER-BOLTENSTERN S 2006 Factors
controlling regional differences in forest soil emission of nitrogen
oxides (NO and N2O) Biogeosciences 3 651-661 httpdxdoi
org105194bg-3-651-2006
PINtildeA-OCHOA E amp ALVAREZ-COBELAS M 2006
Denitrification in aquatic environments A cross-system analysis
Biogeochemistry 81 111-130 httpdxdoiorg101007s10533-
006-9033-7
POULIN P PELLETIER E amp SAINT-LOUIS R 2007
Seasonal variability of denitrification efficiency in northern
salt marshes An example from the St Lawrence Estuary
Marine Environmental Research 63 490-505 httpdxdoi
org101016jmarenvres200612003
RAVISHANKARA AR DANIEL JS amp PORTMANN
RW 2009 Nitrous oxide (N2O) The dominant ozone-depleting
substance emitted in the 21st century Science 326 123-125
httpdxdoiorg101126science1176985
REDDY KR PATRICK WH amp LINDAU CW 1989
Nitrification-Denitrification at the Plant Root-Sediment Interface
in Wetlands Limnology and Oceanography 34 1004-1013
httpdxdoiorg104319lo19893461004
ROBINSON AD NEDWELL DB HARRISON RM amp
OGILVIE BG 1998 Hypernutrified estuaries as sources of
N2O emission to the atmosphere the estuary of the River Colne
Essex UK Marine Ecology Progress Series 164 59-71 http
dxdoiorg103354meps164059
ROSS DS amp WEMPLE BC 2011 Soil nitrification in a large
forested watershed Ranch Brook (Vermont) mirrors patterns
in smaller northeastern USA catchments Forest Ecology and
Management 262 1084-1093 httpdxdoiorg101016j
foreco201106002
RYSGAARD S RISGAARD-PETERSEN N NIELSEN LP
amp REVSBECH NP 1993 Nitrification and Denitrification in
Lake and Estuarine Sediments Measured by the N-15 Dilution
Technique and Isotope Pairing Applied and Environmental
Microbiology 59 2093-2098
SAAD O amp CONRAD R 1993 Temperature-Dependence of
Nitrification Denitrification and Turnover of Nitric-Oxide in
Different Soils Biology and Fertility of Soils 15 21-27 http
dxdoiorg101007BF00336283
SANTORO AL amp ENRICH-PRAST A 2011 Regulaccedilatildeo
microbioloacutegica da disponibilidade de nitrogecircnio em ecossistemas
aquaacuteticos continentais Oecologia Australis 15 213-235 http
dxdoiorg104257oeco2011150203
SASAKI H MARUYAMA G SUZUKI H NONAKA
J SATO M SASAKI T OHTA M amp NAKAI Y 2002
Characterization of ammonia-assimilating bacteria in a
lagoon for wastewater from a paddock of dairy cattle Animal
Science Journal 73 73-76 httpdxdoiorg101046j1344-
3941200200004x
SCHIMEL JP amp GULLEDGE J 1998 Microbial community
structure and global trace gases Global Change Biology 4 745-
758 httpdxdoiorg101046j1365-2486199800195x
SCHMIDT BHM KALBITZ K BRAUN S FUAtildeY
R MCDOWELL WH amp MATZNER E 2011 Microbial
immobilization and mineralization of dissolved organic nitrogen
from forest floors Soil Biology and Biochemistry 43 1742-1745
httpdxdoiorg101016jsoilbio201104021
SCOTT JT MCCARTHY MJ GARDNER WS amp DOYLE
RD 2008 Denitrification dissimilatory nitrate reduction to
ammonium and nitrogen fixation along a nitrate concentration
gradient in a created freshwater wetland Biogeochemistry 87
99-111 httpdxdoiorg101007s10533-007-9171-6
SEITZINGER SP 1988 Denitrification in Fresh-Water and
Coastal Marine Ecosystems - Ecological and Geochemical
Significance Limnology and Oceanography 33 702-724 http
dxdoiorg104319lo1988334_part_20702
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
329
SEITZINGER SP amp KROEZE C 1998 Global distribution of
nitrous oxide production and N inputs in freshwater and coastal
marine ecosystems Global Biogeochemical Cycles 12 93-113
httpdxdoiorg10102997GB03657
SEITZINGER S HARRISON JA BOHLKE JK
BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
326
HASHIMOTO S GOJO K SENDAI N amp OTSUKI A
1999 Nitrous oxide emission from coastal Waters in Tokyo Bay
Marine Environmental Research 47 213-223
HAYATSU M TAGO K amp SAITO M 2008 Various players in
the nitrogen cycle Diversity and functions of the microorganisms
involved in nitrification and denitrification Soil Science and
Plant Nutrition 54 33-45 httpdxdoiorg101111j1747-
0765200700195x
HIROTA M SENGA Y SEIKE Y NOHARA S amp KUNII
H 2007 Fluxes of carbon dioxide methane and nitours oxide in
two contrastive fringing zones of coastal lagoon Lake Nakaumi
Japan Chemosphere 68 597-603 httpdxdoiorg101016j
chemosphere200701002
HLAVAacuteCOVAacute E RULIacuteK M CAacuteP L amp MACH V 2006
Greenhouse gas (CO2 CH4 N2O) emissions to the atmosphere
from a small lowland stream in Czech Republic Archiv fur
Hydrobiologie 165 339-353 httpdxdoiorg1011270003-
913620060165-0339
HUTTUNEN JT ALM J LIIKANEN A JUUTINEN S
LARMOLA T HAMMAR T SILVOLA J amp MARTIKAINEN
PJ 2003 Fluxes of methane carbon dioxide and nitrous oxide
in boreal lakes and potential anthropogenic effects on the
aquatic greenhouse gas emissions Chemosphere 52 609-621
httpdxdoiorg101016S0045-6535(03)00243-1
INSELSBACHER E UMANA NHN STANGE FC
GORFER M SCHUumlLLER E RIPKA K ZECHMEISTER-
BOLTENSTERN S HOOD-NOVOTNY R STRAUSS J
amp WANEK W 2010 Short-term competition between crop
plants and soil microbes for inorganic N fertilizer Soil Biology
and Biochemistry 42 360-372 httpdxdoiorg101016j
soilbio200911019
IPCC (Intergovernmental Panel on Climate Change) 2001
Climate Change 2001 Impacts Adaptation and Vulnerability
Cambridge University Press Reino Unido e Nova York 1042p
IPCC (Intergovernmental Panel on Climate Change) 2007
Climate Change 2007 The Physical Science Basis Cambridge
University Press Reino Unido e Nova York 1008p
JAYAWEERA GR amp MIKKELSEN DS 1991 Assessment Of
Ammonia Volatilization From Flooded Soil Systems Advances
in Agronomy 45 303-356 httpdxdoiorg101016S0065-
2113(08)60044-9
JOHN R DALLING JW HARMS KE YAVITT JB
STALLARD RF MIRABELLO M HUBBELL SP
VALENCIA R NAVARRETE H VALLEJO M amp FOSTER
RB 2007 Soil nutrients influence spatial distributions of tropical
tree species Proceedings of the National Academy of Sciences
of the United States of America 104 864-869 httpdxdoi
org101073pnas0604666104
JOHNSON MT LISS PS BELL TG LESWORTH TJ
BAKER AR HIND AJ JICKELLS TD BISWAS KF
WOODWRAD EMS amp GIBB SW 2008 Field observations
of the ocean-atmosphere exchange of ammonia Fundamental
importance of temperature as revealed by a comparison of high
and low latitudes Global Biogeochemical Cycles 22 GB1019
httpdxdoiorg1010292007GB003039
KAMPSCHEREUR MJ TEMMINK H KLEEREBEZEM
R JETTEN MSM amp VAN LOOSDRECHT MCM
2009 Nitrous oxide emission during wastewater treatment
Water Research 43 4093-4103 httpdxdoiorg101016j
watres200903001
KOIKE I amp TERAUCHI K 1996 Fine scale distribution
of nitrous oxide in marine sediments Marine Chemistry 52
185-193
KOOL DM DOLFING J WRAGE N amp VAN GROENIGEN
JW 2011 Nitrifier denitrification as a distinct and significant
source of nitrous oxide from soil Soil Biology Biochemistry 43
174-178 httpdxdoiorg101016jsoilbio201009030
KOWALCHUK GA amp STEPHEN JR 2001 Ammonia-
oxidizing bacteria A model for molecular microbial ecology
Annual Review of Microbiology 55 485-529 httpdxdoi
org101146annurevmicro551485
KREMEN A BEAR J SHAVIT U amp SHAVIV A 2005
Model demonstrating the potencial for coupled nitrification
denitrification in soil aggregates Environmental Science
Technology 39 4180-4188 httpdxdoiorg101021es048304z
KREUZWIESER J BUCHOLZ J amp RENNENBERG H
2003 Emission of methane and nitrous oxide by Australian
mangrove ecosystems Plant Biology 5 423-431
KRITHIKA K PURVAJA R amp RAMESH R 2008 Fluxes
of methane and nitrous oxide from an Indian mangrove Current
Science 94 218-224
KROEZE C amp SEITZINGER SP 1998 Nitrogen inputs
to rivers estuaries and continental shelves and related
nitrous oxide emissions in 1990 and 2050 a global model
Nutrient Cycling Agroecosystems 52 195-212 httpdxdoi
org101023A1009780608708
KUSCHK P WIESSNER A KAPPELMEYER U
WEISSBRODT E KASTNER M amp STOTTMEISTER
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
327
U 2003 Annual cycle of nitrogen removal by a pilot-scale
subsurface horizontal flow in a constructed wetland under
moderate climate Water Research 37 4236-4242 httpdxdoi
org101016S0043-1354(03)00163-5
LAW CS REES AP amp OWENS NJP 1992 Nitrous oxide
Estuarine sources and atmospheric flux Estuarine Coastal and
Shelf Science 35 301-314 httpdxdoiorg101016S0272-
7714(05)80050-2
LIIKANEN A amp MARTIKAINEN PJ 2003 Effect of
ammonium and oxygen on methane and nitrous oxide
fluxes across sediment-water interface in a eutrophic lake
Chemosphere 52 1287-1293 httpdxdoiorg101016S0045-
6535(03)00224-8
LIU Y ZHU R MA D XU H LUO Y HUANG T amp
SUN L 2011 Temporal and spatial variations of nitrous oxide
fluxes from the littoral zones of three alga-rich lakes in coastal
Antarctica Atmospheric Environment 45 1464-1475 http
dxdoiorg101016jatmosenv201012017
LIVESLEY S amp ANDRUSIAK SM 2012 Temperate mangrove
and salt marsh sediments are a small methane and nitrous oxide
source but important carbon store Estuarine Coastal and Shelf
Science 97 19-27 httpdxdoiorg101016jecss201111002
LORENZEN J LARSEN LH KJAER T amp REVSBECH
NP 1998 Biosensor determination of the microscale distribution
of nitrate nitrate assimilation nitrification and denitrification
in a diatom-inhabited freshwater sediment Applied and
Environmental Microbiology 64 3264-3269
MA WK BEDARD-HAUGHN A SICILIANO SD amp
FARRELL RE 2008 Relationship between nitrifier and
denitrifier community composition and abundance in predicting
nitrous oxide emissions from ephemeral wetland soils Soil
Biology Biochemistry 40 1114-1123 httpdxdoiorg101016j
soilbio200712004
MALHI SS MCGILL WB amp NYBORG M 1990 Nitrate
losses in soils Effect of temperature moisture and substrate
concentration Soil Biology and Biochemistry 22 733-737
httpdxdoiorg1010160038-0717(90)90150-X
MAMILOV AS amp DILLY OM 2002 Soil microbial eco-
physiology as affected by short-term variations in environmental
conditions Soil Biology and Biochemistry 34 1283-1290 http
dxdoiorg101016S0038-0717(02)00071-8
MCCLAIN ME BOYER EW DENT CL GERGEL SE
GRIMM NB GROFFMAN PM HART SC HARVEY
JW JOHNSTON CA MAYORGA E MCDOWELL WH
amp PINAY G 2003 Biogeochemical hot spots and hot moments
at the interface of terrestrial and aquatic ecosystems Ecosystems
6 301-312 httpdxdoiorg101007s10021-003-0161-9
MCMAHON PB amp DENNEHY KF 1999 N2O emissions from
a nitrogen-enriched river Environmental Science Technology 33
21-25 httpdxdoiorg101021es980645n
MENGIS M GACHTER R amp WEHRLI B 1996 Nitrous
oxide emissions to the atmosphere from an artificially oxygenated
lake Limnology and Oceanography 41 548-553
MENGIS M GACHTER R amp WEHRLI B 1997 Sources and
sinks of nitrous oxide (N2O) in deep lakes Biogeochemistry 38
281-301 httpdxdoiorg101023A1005814020322
METAY A CHAPUIS-LARDY L FINDELING A OLIVER
R MOREIRA JAA amp FELLER C 2011 Simulating N2O
fluxes from a Brazilian cropped soil with contrasted tillage
practices Agriculture Ecosystems amp Environment 140 255-263
httpdxdoiorg101016jagee201012012
MILLER AE SCHIMEL JP SICKMAN JO SKEEN
K MEIXNER T amp MELACK JM 2009 Seasonal variation
in nitrogen uptake and turnover in two high-elevation soils
mineralization responses are site-dependent Biogeochemistry
93 253-270 httpdxdoiorg101007s10533-009-9301-4
MOslashRKVED PT DOumlRSCH P amp BAKKEN LR 2007 The
N2O product ratio of nitrification and its dependence on long-term
changes in soil pH Soil Biology and Biochemistry 39 2048-
2057 httpdxdoiorg101016jsoilbio200703006
MORLEY N amp BAGGS EM 2010 Carbon and oxygen
controls on N2O and N2 production during nitrate reduction
Soil Biology and Biochemistry 42 1864-1871 httpdxdoi
org101016jsoilbio201007008
MUNtildeOZ-HINCAPIEacute M MORELL JM amp CORREDOR
JE 2002 Increase of nitrous oxide flux to the atmosphere upon
nitrogen addition to red mangroves sediments Marine Pollution
Bulletin 44 992-996
NICOLAISEN MH RISGAARD-PETERSEN N
REVSBECH NP REICHARDT W amp RAMSING NB 2004
Nitrification-denitrification dynamics and community structure
of ammonia oxidizing bacteria in a high yield irrigated Philippine
rice filed FEMS Microbiology Ecology 49 359-369 http
dxdoiorg101016jfemsec200404015
NISHIO T KOIKE I amp HATTORI A 1983 Estimates of
denitrification and nitrification in coastal and estuarine sediments
Applied and Environmental Microbiology 45 444-450
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
328
NUGROHO RA ROLING WFM LAVERMAN AM amp
VERHOEF HA 2007 Low nitrification rates in acid scots pine
forest soils are due to pH-related factors Microbial Ecology 53
89-97 httpdxdoiorg101007s00248-006-9142-9
OTTOSEN LDM RISGAARD-PETERSEN N amp NIELSEN
LP 1999 Direct and indirect measurements of nitrification
and denitrification in the rhizosphere of aquatic macrophytes
Aquatic Microbial Ecology 19 81-91 httpdxdoiorg103354
ame019081
PEREZ T GARCIA-MONTIEL D TRUMBORE S
TYLER S DE CAMARGO P MOREIRA M PICCOLO M
amp CERRI C 2006 Nitrous oxide nitrification and denitrification
N-15 enrichment factors from Amazon forest soils Ecological
Applications 16 2153-2167 httpdxdoiorg1018901051-
0761(2006)016[2153NONADN]20CO2
PILEGAARD K SKIBA U AMBUS P BEIER C
BRUGGEMANN N BUTTERBACH-BAHL K DICK
J DORSEY J DUYZER J GALLAGHER M GASCHE
R HORVATH L KITZLER B LEIP A PIHLATIE MK
ROSENKRANZ P SEUFERT G VESALA T WESTRATE
H amp ZECHMEISTER-BOLTENSTERN S 2006 Factors
controlling regional differences in forest soil emission of nitrogen
oxides (NO and N2O) Biogeosciences 3 651-661 httpdxdoi
org105194bg-3-651-2006
PINtildeA-OCHOA E amp ALVAREZ-COBELAS M 2006
Denitrification in aquatic environments A cross-system analysis
Biogeochemistry 81 111-130 httpdxdoiorg101007s10533-
006-9033-7
POULIN P PELLETIER E amp SAINT-LOUIS R 2007
Seasonal variability of denitrification efficiency in northern
salt marshes An example from the St Lawrence Estuary
Marine Environmental Research 63 490-505 httpdxdoi
org101016jmarenvres200612003
RAVISHANKARA AR DANIEL JS amp PORTMANN
RW 2009 Nitrous oxide (N2O) The dominant ozone-depleting
substance emitted in the 21st century Science 326 123-125
httpdxdoiorg101126science1176985
REDDY KR PATRICK WH amp LINDAU CW 1989
Nitrification-Denitrification at the Plant Root-Sediment Interface
in Wetlands Limnology and Oceanography 34 1004-1013
httpdxdoiorg104319lo19893461004
ROBINSON AD NEDWELL DB HARRISON RM amp
OGILVIE BG 1998 Hypernutrified estuaries as sources of
N2O emission to the atmosphere the estuary of the River Colne
Essex UK Marine Ecology Progress Series 164 59-71 http
dxdoiorg103354meps164059
ROSS DS amp WEMPLE BC 2011 Soil nitrification in a large
forested watershed Ranch Brook (Vermont) mirrors patterns
in smaller northeastern USA catchments Forest Ecology and
Management 262 1084-1093 httpdxdoiorg101016j
foreco201106002
RYSGAARD S RISGAARD-PETERSEN N NIELSEN LP
amp REVSBECH NP 1993 Nitrification and Denitrification in
Lake and Estuarine Sediments Measured by the N-15 Dilution
Technique and Isotope Pairing Applied and Environmental
Microbiology 59 2093-2098
SAAD O amp CONRAD R 1993 Temperature-Dependence of
Nitrification Denitrification and Turnover of Nitric-Oxide in
Different Soils Biology and Fertility of Soils 15 21-27 http
dxdoiorg101007BF00336283
SANTORO AL amp ENRICH-PRAST A 2011 Regulaccedilatildeo
microbioloacutegica da disponibilidade de nitrogecircnio em ecossistemas
aquaacuteticos continentais Oecologia Australis 15 213-235 http
dxdoiorg104257oeco2011150203
SASAKI H MARUYAMA G SUZUKI H NONAKA
J SATO M SASAKI T OHTA M amp NAKAI Y 2002
Characterization of ammonia-assimilating bacteria in a
lagoon for wastewater from a paddock of dairy cattle Animal
Science Journal 73 73-76 httpdxdoiorg101046j1344-
3941200200004x
SCHIMEL JP amp GULLEDGE J 1998 Microbial community
structure and global trace gases Global Change Biology 4 745-
758 httpdxdoiorg101046j1365-2486199800195x
SCHMIDT BHM KALBITZ K BRAUN S FUAtildeY
R MCDOWELL WH amp MATZNER E 2011 Microbial
immobilization and mineralization of dissolved organic nitrogen
from forest floors Soil Biology and Biochemistry 43 1742-1745
httpdxdoiorg101016jsoilbio201104021
SCOTT JT MCCARTHY MJ GARDNER WS amp DOYLE
RD 2008 Denitrification dissimilatory nitrate reduction to
ammonium and nitrogen fixation along a nitrate concentration
gradient in a created freshwater wetland Biogeochemistry 87
99-111 httpdxdoiorg101007s10533-007-9171-6
SEITZINGER SP 1988 Denitrification in Fresh-Water and
Coastal Marine Ecosystems - Ecological and Geochemical
Significance Limnology and Oceanography 33 702-724 http
dxdoiorg104319lo1988334_part_20702
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
329
SEITZINGER SP amp KROEZE C 1998 Global distribution of
nitrous oxide production and N inputs in freshwater and coastal
marine ecosystems Global Biogeochemical Cycles 12 93-113
httpdxdoiorg10102997GB03657
SEITZINGER S HARRISON JA BOHLKE JK
BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
327
U 2003 Annual cycle of nitrogen removal by a pilot-scale
subsurface horizontal flow in a constructed wetland under
moderate climate Water Research 37 4236-4242 httpdxdoi
org101016S0043-1354(03)00163-5
LAW CS REES AP amp OWENS NJP 1992 Nitrous oxide
Estuarine sources and atmospheric flux Estuarine Coastal and
Shelf Science 35 301-314 httpdxdoiorg101016S0272-
7714(05)80050-2
LIIKANEN A amp MARTIKAINEN PJ 2003 Effect of
ammonium and oxygen on methane and nitrous oxide
fluxes across sediment-water interface in a eutrophic lake
Chemosphere 52 1287-1293 httpdxdoiorg101016S0045-
6535(03)00224-8
LIU Y ZHU R MA D XU H LUO Y HUANG T amp
SUN L 2011 Temporal and spatial variations of nitrous oxide
fluxes from the littoral zones of three alga-rich lakes in coastal
Antarctica Atmospheric Environment 45 1464-1475 http
dxdoiorg101016jatmosenv201012017
LIVESLEY S amp ANDRUSIAK SM 2012 Temperate mangrove
and salt marsh sediments are a small methane and nitrous oxide
source but important carbon store Estuarine Coastal and Shelf
Science 97 19-27 httpdxdoiorg101016jecss201111002
LORENZEN J LARSEN LH KJAER T amp REVSBECH
NP 1998 Biosensor determination of the microscale distribution
of nitrate nitrate assimilation nitrification and denitrification
in a diatom-inhabited freshwater sediment Applied and
Environmental Microbiology 64 3264-3269
MA WK BEDARD-HAUGHN A SICILIANO SD amp
FARRELL RE 2008 Relationship between nitrifier and
denitrifier community composition and abundance in predicting
nitrous oxide emissions from ephemeral wetland soils Soil
Biology Biochemistry 40 1114-1123 httpdxdoiorg101016j
soilbio200712004
MALHI SS MCGILL WB amp NYBORG M 1990 Nitrate
losses in soils Effect of temperature moisture and substrate
concentration Soil Biology and Biochemistry 22 733-737
httpdxdoiorg1010160038-0717(90)90150-X
MAMILOV AS amp DILLY OM 2002 Soil microbial eco-
physiology as affected by short-term variations in environmental
conditions Soil Biology and Biochemistry 34 1283-1290 http
dxdoiorg101016S0038-0717(02)00071-8
MCCLAIN ME BOYER EW DENT CL GERGEL SE
GRIMM NB GROFFMAN PM HART SC HARVEY
JW JOHNSTON CA MAYORGA E MCDOWELL WH
amp PINAY G 2003 Biogeochemical hot spots and hot moments
at the interface of terrestrial and aquatic ecosystems Ecosystems
6 301-312 httpdxdoiorg101007s10021-003-0161-9
MCMAHON PB amp DENNEHY KF 1999 N2O emissions from
a nitrogen-enriched river Environmental Science Technology 33
21-25 httpdxdoiorg101021es980645n
MENGIS M GACHTER R amp WEHRLI B 1996 Nitrous
oxide emissions to the atmosphere from an artificially oxygenated
lake Limnology and Oceanography 41 548-553
MENGIS M GACHTER R amp WEHRLI B 1997 Sources and
sinks of nitrous oxide (N2O) in deep lakes Biogeochemistry 38
281-301 httpdxdoiorg101023A1005814020322
METAY A CHAPUIS-LARDY L FINDELING A OLIVER
R MOREIRA JAA amp FELLER C 2011 Simulating N2O
fluxes from a Brazilian cropped soil with contrasted tillage
practices Agriculture Ecosystems amp Environment 140 255-263
httpdxdoiorg101016jagee201012012
MILLER AE SCHIMEL JP SICKMAN JO SKEEN
K MEIXNER T amp MELACK JM 2009 Seasonal variation
in nitrogen uptake and turnover in two high-elevation soils
mineralization responses are site-dependent Biogeochemistry
93 253-270 httpdxdoiorg101007s10533-009-9301-4
MOslashRKVED PT DOumlRSCH P amp BAKKEN LR 2007 The
N2O product ratio of nitrification and its dependence on long-term
changes in soil pH Soil Biology and Biochemistry 39 2048-
2057 httpdxdoiorg101016jsoilbio200703006
MORLEY N amp BAGGS EM 2010 Carbon and oxygen
controls on N2O and N2 production during nitrate reduction
Soil Biology and Biochemistry 42 1864-1871 httpdxdoi
org101016jsoilbio201007008
MUNtildeOZ-HINCAPIEacute M MORELL JM amp CORREDOR
JE 2002 Increase of nitrous oxide flux to the atmosphere upon
nitrogen addition to red mangroves sediments Marine Pollution
Bulletin 44 992-996
NICOLAISEN MH RISGAARD-PETERSEN N
REVSBECH NP REICHARDT W amp RAMSING NB 2004
Nitrification-denitrification dynamics and community structure
of ammonia oxidizing bacteria in a high yield irrigated Philippine
rice filed FEMS Microbiology Ecology 49 359-369 http
dxdoiorg101016jfemsec200404015
NISHIO T KOIKE I amp HATTORI A 1983 Estimates of
denitrification and nitrification in coastal and estuarine sediments
Applied and Environmental Microbiology 45 444-450
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
328
NUGROHO RA ROLING WFM LAVERMAN AM amp
VERHOEF HA 2007 Low nitrification rates in acid scots pine
forest soils are due to pH-related factors Microbial Ecology 53
89-97 httpdxdoiorg101007s00248-006-9142-9
OTTOSEN LDM RISGAARD-PETERSEN N amp NIELSEN
LP 1999 Direct and indirect measurements of nitrification
and denitrification in the rhizosphere of aquatic macrophytes
Aquatic Microbial Ecology 19 81-91 httpdxdoiorg103354
ame019081
PEREZ T GARCIA-MONTIEL D TRUMBORE S
TYLER S DE CAMARGO P MOREIRA M PICCOLO M
amp CERRI C 2006 Nitrous oxide nitrification and denitrification
N-15 enrichment factors from Amazon forest soils Ecological
Applications 16 2153-2167 httpdxdoiorg1018901051-
0761(2006)016[2153NONADN]20CO2
PILEGAARD K SKIBA U AMBUS P BEIER C
BRUGGEMANN N BUTTERBACH-BAHL K DICK
J DORSEY J DUYZER J GALLAGHER M GASCHE
R HORVATH L KITZLER B LEIP A PIHLATIE MK
ROSENKRANZ P SEUFERT G VESALA T WESTRATE
H amp ZECHMEISTER-BOLTENSTERN S 2006 Factors
controlling regional differences in forest soil emission of nitrogen
oxides (NO and N2O) Biogeosciences 3 651-661 httpdxdoi
org105194bg-3-651-2006
PINtildeA-OCHOA E amp ALVAREZ-COBELAS M 2006
Denitrification in aquatic environments A cross-system analysis
Biogeochemistry 81 111-130 httpdxdoiorg101007s10533-
006-9033-7
POULIN P PELLETIER E amp SAINT-LOUIS R 2007
Seasonal variability of denitrification efficiency in northern
salt marshes An example from the St Lawrence Estuary
Marine Environmental Research 63 490-505 httpdxdoi
org101016jmarenvres200612003
RAVISHANKARA AR DANIEL JS amp PORTMANN
RW 2009 Nitrous oxide (N2O) The dominant ozone-depleting
substance emitted in the 21st century Science 326 123-125
httpdxdoiorg101126science1176985
REDDY KR PATRICK WH amp LINDAU CW 1989
Nitrification-Denitrification at the Plant Root-Sediment Interface
in Wetlands Limnology and Oceanography 34 1004-1013
httpdxdoiorg104319lo19893461004
ROBINSON AD NEDWELL DB HARRISON RM amp
OGILVIE BG 1998 Hypernutrified estuaries as sources of
N2O emission to the atmosphere the estuary of the River Colne
Essex UK Marine Ecology Progress Series 164 59-71 http
dxdoiorg103354meps164059
ROSS DS amp WEMPLE BC 2011 Soil nitrification in a large
forested watershed Ranch Brook (Vermont) mirrors patterns
in smaller northeastern USA catchments Forest Ecology and
Management 262 1084-1093 httpdxdoiorg101016j
foreco201106002
RYSGAARD S RISGAARD-PETERSEN N NIELSEN LP
amp REVSBECH NP 1993 Nitrification and Denitrification in
Lake and Estuarine Sediments Measured by the N-15 Dilution
Technique and Isotope Pairing Applied and Environmental
Microbiology 59 2093-2098
SAAD O amp CONRAD R 1993 Temperature-Dependence of
Nitrification Denitrification and Turnover of Nitric-Oxide in
Different Soils Biology and Fertility of Soils 15 21-27 http
dxdoiorg101007BF00336283
SANTORO AL amp ENRICH-PRAST A 2011 Regulaccedilatildeo
microbioloacutegica da disponibilidade de nitrogecircnio em ecossistemas
aquaacuteticos continentais Oecologia Australis 15 213-235 http
dxdoiorg104257oeco2011150203
SASAKI H MARUYAMA G SUZUKI H NONAKA
J SATO M SASAKI T OHTA M amp NAKAI Y 2002
Characterization of ammonia-assimilating bacteria in a
lagoon for wastewater from a paddock of dairy cattle Animal
Science Journal 73 73-76 httpdxdoiorg101046j1344-
3941200200004x
SCHIMEL JP amp GULLEDGE J 1998 Microbial community
structure and global trace gases Global Change Biology 4 745-
758 httpdxdoiorg101046j1365-2486199800195x
SCHMIDT BHM KALBITZ K BRAUN S FUAtildeY
R MCDOWELL WH amp MATZNER E 2011 Microbial
immobilization and mineralization of dissolved organic nitrogen
from forest floors Soil Biology and Biochemistry 43 1742-1745
httpdxdoiorg101016jsoilbio201104021
SCOTT JT MCCARTHY MJ GARDNER WS amp DOYLE
RD 2008 Denitrification dissimilatory nitrate reduction to
ammonium and nitrogen fixation along a nitrate concentration
gradient in a created freshwater wetland Biogeochemistry 87
99-111 httpdxdoiorg101007s10533-007-9171-6
SEITZINGER SP 1988 Denitrification in Fresh-Water and
Coastal Marine Ecosystems - Ecological and Geochemical
Significance Limnology and Oceanography 33 702-724 http
dxdoiorg104319lo1988334_part_20702
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
329
SEITZINGER SP amp KROEZE C 1998 Global distribution of
nitrous oxide production and N inputs in freshwater and coastal
marine ecosystems Global Biogeochemical Cycles 12 93-113
httpdxdoiorg10102997GB03657
SEITZINGER S HARRISON JA BOHLKE JK
BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
FIGUEIREDO VF amp ENRICH-PRAST A
Oecol Aust 16(2) 311-329 2012
328
NUGROHO RA ROLING WFM LAVERMAN AM amp
VERHOEF HA 2007 Low nitrification rates in acid scots pine
forest soils are due to pH-related factors Microbial Ecology 53
89-97 httpdxdoiorg101007s00248-006-9142-9
OTTOSEN LDM RISGAARD-PETERSEN N amp NIELSEN
LP 1999 Direct and indirect measurements of nitrification
and denitrification in the rhizosphere of aquatic macrophytes
Aquatic Microbial Ecology 19 81-91 httpdxdoiorg103354
ame019081
PEREZ T GARCIA-MONTIEL D TRUMBORE S
TYLER S DE CAMARGO P MOREIRA M PICCOLO M
amp CERRI C 2006 Nitrous oxide nitrification and denitrification
N-15 enrichment factors from Amazon forest soils Ecological
Applications 16 2153-2167 httpdxdoiorg1018901051-
0761(2006)016[2153NONADN]20CO2
PILEGAARD K SKIBA U AMBUS P BEIER C
BRUGGEMANN N BUTTERBACH-BAHL K DICK
J DORSEY J DUYZER J GALLAGHER M GASCHE
R HORVATH L KITZLER B LEIP A PIHLATIE MK
ROSENKRANZ P SEUFERT G VESALA T WESTRATE
H amp ZECHMEISTER-BOLTENSTERN S 2006 Factors
controlling regional differences in forest soil emission of nitrogen
oxides (NO and N2O) Biogeosciences 3 651-661 httpdxdoi
org105194bg-3-651-2006
PINtildeA-OCHOA E amp ALVAREZ-COBELAS M 2006
Denitrification in aquatic environments A cross-system analysis
Biogeochemistry 81 111-130 httpdxdoiorg101007s10533-
006-9033-7
POULIN P PELLETIER E amp SAINT-LOUIS R 2007
Seasonal variability of denitrification efficiency in northern
salt marshes An example from the St Lawrence Estuary
Marine Environmental Research 63 490-505 httpdxdoi
org101016jmarenvres200612003
RAVISHANKARA AR DANIEL JS amp PORTMANN
RW 2009 Nitrous oxide (N2O) The dominant ozone-depleting
substance emitted in the 21st century Science 326 123-125
httpdxdoiorg101126science1176985
REDDY KR PATRICK WH amp LINDAU CW 1989
Nitrification-Denitrification at the Plant Root-Sediment Interface
in Wetlands Limnology and Oceanography 34 1004-1013
httpdxdoiorg104319lo19893461004
ROBINSON AD NEDWELL DB HARRISON RM amp
OGILVIE BG 1998 Hypernutrified estuaries as sources of
N2O emission to the atmosphere the estuary of the River Colne
Essex UK Marine Ecology Progress Series 164 59-71 http
dxdoiorg103354meps164059
ROSS DS amp WEMPLE BC 2011 Soil nitrification in a large
forested watershed Ranch Brook (Vermont) mirrors patterns
in smaller northeastern USA catchments Forest Ecology and
Management 262 1084-1093 httpdxdoiorg101016j
foreco201106002
RYSGAARD S RISGAARD-PETERSEN N NIELSEN LP
amp REVSBECH NP 1993 Nitrification and Denitrification in
Lake and Estuarine Sediments Measured by the N-15 Dilution
Technique and Isotope Pairing Applied and Environmental
Microbiology 59 2093-2098
SAAD O amp CONRAD R 1993 Temperature-Dependence of
Nitrification Denitrification and Turnover of Nitric-Oxide in
Different Soils Biology and Fertility of Soils 15 21-27 http
dxdoiorg101007BF00336283
SANTORO AL amp ENRICH-PRAST A 2011 Regulaccedilatildeo
microbioloacutegica da disponibilidade de nitrogecircnio em ecossistemas
aquaacuteticos continentais Oecologia Australis 15 213-235 http
dxdoiorg104257oeco2011150203
SASAKI H MARUYAMA G SUZUKI H NONAKA
J SATO M SASAKI T OHTA M amp NAKAI Y 2002
Characterization of ammonia-assimilating bacteria in a
lagoon for wastewater from a paddock of dairy cattle Animal
Science Journal 73 73-76 httpdxdoiorg101046j1344-
3941200200004x
SCHIMEL JP amp GULLEDGE J 1998 Microbial community
structure and global trace gases Global Change Biology 4 745-
758 httpdxdoiorg101046j1365-2486199800195x
SCHMIDT BHM KALBITZ K BRAUN S FUAtildeY
R MCDOWELL WH amp MATZNER E 2011 Microbial
immobilization and mineralization of dissolved organic nitrogen
from forest floors Soil Biology and Biochemistry 43 1742-1745
httpdxdoiorg101016jsoilbio201104021
SCOTT JT MCCARTHY MJ GARDNER WS amp DOYLE
RD 2008 Denitrification dissimilatory nitrate reduction to
ammonium and nitrogen fixation along a nitrate concentration
gradient in a created freshwater wetland Biogeochemistry 87
99-111 httpdxdoiorg101007s10533-007-9171-6
SEITZINGER SP 1988 Denitrification in Fresh-Water and
Coastal Marine Ecosystems - Ecological and Geochemical
Significance Limnology and Oceanography 33 702-724 http
dxdoiorg104319lo1988334_part_20702
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
329
SEITZINGER SP amp KROEZE C 1998 Global distribution of
nitrous oxide production and N inputs in freshwater and coastal
marine ecosystems Global Biogeochemical Cycles 12 93-113
httpdxdoiorg10102997GB03657
SEITZINGER S HARRISON JA BOHLKE JK
BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012
OacuteXIDO NITROSO (N2O) EM AMBIENTES AQUAacuteTICOS CONTINENTAIS PRODUCcedilAtildeO REGULACcedilAtildeO E FLUXOS
Oecol Aust 16(2) 311-329 2012
329
SEITZINGER SP amp KROEZE C 1998 Global distribution of
nitrous oxide production and N inputs in freshwater and coastal
marine ecosystems Global Biogeochemical Cycles 12 93-113
httpdxdoiorg10102997GB03657
SEITZINGER S HARRISON JA BOHLKE JK
BOUWMAN AF LOWRANCE R PETERSON B TOBIAS
C amp VAN DRECHT G 2006 Denitrification across landscapes
and waterscapes A synthesis Ecological Applications 16 2064-
2090 httpdxdoiorg1018901051-0761(2006)016[2064DAL
AWA]20CO2
SILVENNOINEN H LIIKANEN A RINTALA J amp
MARTIKAINEN PJ 2008 Global distribution Greenhouse gas
fluxes from the eutrophic Temmsjoki River and its Estuary in the
Liminganlahti Bay (the Baltic Sea) Biogeochemistry 90 193-
208
STOW CA WALKER JT CARDOCH L SPENCE P amp
GERON C 2005 N2O emissions from streams in the Neuse river
watershed North Carolina Environmental Science Technology
39 6999-7004 httpdxdoiorg101021es0500355
TIEDJE JM 1988 Ecology of Denitrification and Dissimilatory
Nitrate Reduction to Ammonium Pp 179-244 In AJB Zehnder
(ed) Biology of Anaerobic Microorganisms John Wiley amp Sons
New York 872p
WANG D CHEN Z SUN W HU B amp XU S 2009 Methane
and nitrous oxide concentration and emission flux of Yangtze
Delta plain river net Science in China series B Chemistry 52
652-661 httpdxdoiorg101007s11426-009-0024-0
WERNER C BUTTERBACH-BAHL K HAHS E
HICKLER T amp KIESE R 2007 A global inventory of
N2O emissions from tropical rainforest soils using a detailed
biogeochemical model Global Biogeochemical Cycles 21 1-18
httpdxdoiorg1010292006GB002909
WHITAKER V amp MATVIEKO B 1992 A Method for the
Study of N2O Evolution in Tropical Wetlands Hydrobiologia
230 213-218 httpdxdoiorg101007BF00036567
WRAGE N VELTHOF GL VAN BEUSICHEM ML
amp OENEMA O 2001 Role of nitrifier denitrification in the
production of nitrous oxide Soil Biology and Biochemistry 33
1723-1732 httpdxdoiorg101016S0038-0717(01)00096-7
YANG LB YAN WJ MA P amp WANG JN 2011 Seasonal
and diurnal variations in N(2)O concentrations and fluxes
from three eutrophic rivers in Southeast China Journal of
Geographical Sciences 21 820-832 httpdxdoiorg101007
s11442-011-0882-1
YAO Z WOLF B CHEN W BUTTERBACH-BAHL K
BRUumlGGEMANN N WIESMEIER M DANNENMANN
M BLAN B amp ZHENG X 2010 Spatial variability of N2O
CH4 and CO2 fluxes within the Xilin River catchment of Inner
Mongolia China a soil core study Plant Soil 331 341-359
httpdxdoiorg101007s11104-009-0257-x
ZHANG G ZHANG J XU J amp ZHANG F 2006
Distributions sources and atmospheric fluxes of nitrous oxide in
Jiaozhou Bay Estuarine coastal and shelf science 68 557-566
httpdxdoiorg101016jecss200603007
ZHANG GL ZHANG J LIU SM REN JL amp ZHAO YC
2010 Nitrous oxide in the Changjiang (Yangtze River) Estuary
and its adjacent marine area Riverine input sediment release and
atmospheric fluxes Biogeosciences 7 3505-3516 httpdxdoi
org105194bg-7-3505-2010
ZHU W-X amp WANG W 2011 Does soil organic matter
variation affect the retention of 15NH4+ and 15NO3
- in forest
ecosystems Forest Ecology and Management 261 675-682
httpdxdoiorg101016jforeco201011024
Submetido em 13052012Aceito em 23062012