Causas e consequências da onivoria de peixes em

Transcription

Universidade Federal do Rio Grande do Norte
Centro de Biociências
Programa de Pós-Graduação em Ecologia (PPgECO)
Causas e consequências da onivoria de peixes em ecossistemas
aquáticos.
Danyhelton Douglas Farias Dantas
Orientador: Prof. Dr. José Luiz Attayde, UFRN
Co-orientador: Prof. Dr. Ronaldo Angelini, UFRN
Natal - RN
2015
aquáticos.
Tese apresentada ao programa de Pósgraduação em ecologia da Universidade Federal
do Rio Grande do Norte, como parte dos
requisitos necessários para a obtenção do grau
de doutor Ecologia.
Orientador: Prof. Dr. José Luiz de Attayde
Co-orientador: Prof. Dr. Ronaldo Angelini
Natal - RN
2015
Catalogação da Publicação na Fonte. UFRN / Biblioteca Setorial do Centro de Biociências
Dantas, Danyhelton Douglas Farias.
Causas e consequências da onivoria de peixes em ecossistemas aquáticos / Danyhelton Douglas
Farias Dantas. – Natal, RN, 2015.
79 f.: il.
Orientador: Prof. Dr. José Luiz de Attayde.
Coorientador: Prof. Dr. Ronaldo Angelini.
Tese (Doutorado) – Universidade Federal do Rio Grande do Norte. Centro de Biociências. Programa
de Pós-Graduação em Ecologia.
1. Onivoria – Tese. 2. Metabolismo. – Tese. 3. Estrutura trófica. – Tese. I. Attayde, José Luiz de. II.
Angelini, Ronaldo. III. Universidade Federal do Rio Grande do Norte. IV. Título.
RN/UF/BSE-CB
CDU 591.131.1
aquáticos.
Tese apresentada ao programa de Pósgraduação em ecologia da Universidade
Federal do Rio Grande do Norte, como parte
dos requisitos necessários para a obtenção do
grau de doutor Ecologia.
Orientador: Prof. Dr. José Luiz de Attayde
Co-orientador: Prof. Dr. Ronaldo Angelini
Rosemberg Menezes, Dr.
Kermal Ali Ger, Dr.
Prof. Hugo Sarmento, Dr.
Prof. Rafael Guariento, Dr.
Prof. José Luiz de Attayde, Dr.
Natal - RN
2015
“Empty you mind.
Be formless, shapeless, like water.
Now, you put water into a cup, it
becomes the cup.
If you put water into a bottle, it
becomes the bottle.
If you put water into a tea pot, it
becomes the tea pot.
“Results were fond through direct
experimentation” = “We played
around with it until it worked”.
(PhD Comics)
Now, water can flow or it can
crash.
Be water my friend.”
(Bruce Lee).
“Tenho os sentidos já dormentes,
O corpo quer a alma entende.
Esta é terra de ninguém.
Sei que devo resistir
Eu quero a espada em minhas mãos.
Sou metal, raio relâmpago e trovão
Sou metal, eu sou o ouro em seu brasão
Sou metal, quem sabe o sobro do dragão.
Não me entrego sem lutar
Tenho ainda coração.
Não aprendi a me render
Que caia o inimigo então.
E nossa história não estará pelo avesso
Assim, sem final feliz
Teremos coisas bonitas.
E até lá, vamos viver
Temos muito ainda por fazer.
Não olhe pra trás.
Apenas começamos.
O mundo começa agora.
Apenas começamos.”
(Renato Russo).
Agradecimentos
Agradeço a meus pais pelo exemplo e as orientações que fizeram com que eu me
tornasse quem sou hoje. Durante muito tempo eles foram “as costas que vi” enquanto
trilhava o meu caminho.
Mais uma vez (e com certeza nunca a última) agradeço aos meus amigos e orientadores,
José Luiz de Attayde (tio Coca) e Ronaldo Angelini, pelas ajudas e conversas
profissionais, muitas vezes pessoais. Exemplos que vou sempre seguir. Obrigado por
sempre estarem por perto.
Aos professores Adriano Calliman, Luciana Carneiro, Sergio Maia, Vanessa Becker,
Adriana Carvalho, Michael Vanni :) e Maria González, por toda a ajuda e orientação
nesses últimos anos, contribuindo diretamente para meu crescimento intelectual e
profissional. Aos doutores Rosemberg Menezes (amigo de longas datas), Kermal Ali
Ger, Hugo Sarmento, e Rafael Guariento, por aceitarem fazer parte da minha banca
examinadora cedendo seu tempo e conhecimento para contribuir com o crescimento
destes trabalhos.
Aos muitos amigos de trabalho que compõem nossa base de pesquisa pela ajuda e
apoio, em especial aos alunos e profissionais do LEA (Laboratório de ecologia
aquática), LARHISA (Laboratório de Recursos Hídricos e Saneamento Ambiental) e do
Laboratório de Limnologia. A todos os amigos gringos (e os pseudogringos) que
fizeram do curto tempo em Oxford uma experiência fascinante e enriquecedora.
Um muito obrigado (!!!!!!) mais que especial à Mariana (Maricota), Pablo (Ped...fofim),
Leonardo (Carcará), Gabi (Gabeixon), Fabiana (Binha) e Maria (Marcolina). Sem
dúvida o melhor time de amigos que uma pessoa pode querer. Melhor até que a Liga da
Justiça/Vingadores. Espero que nos próximos anos possamos impulsionar, mais ainda, a
nossa produção acadêmica. Força galera!!!!.
A coordenação do curso de Pós-Graduação em Ecologia da UFRN pelo apoio.
A CAPES pela concessão das bolsas de doutorado e doutorado sanduíche.
Aos meus irmãos Diogo, Dagon e Lucas, por continuarem a me aturar nesses últimos
anos marcados por tantas dificuldades e alegrias; “Passamos por tudo, que venham
mais”. Mesmo um pouco distantes ainda estaremos perto. Sem vocês minha vida não
teria graça ou sentido, Obrigado por me deixarem estar perto de vocês.
Um mega agradecimento à pessoa que, a quase 10 anos (o/), consegue deixar todo esse
tumulto que é a minha vida ainda melhor. Que agora "upou" e subiu de nível
(masterizou a classe namorada e atingiu a classe esposa). Porque com você a mais
simples das atividades se torna "sensacional". Ainda continuo dizendo que com você ao
meu lado sou capaz de alcançar o mais impossível dos sonhos. Obrigado Nara.
Resumo
A onivoria é uma estratégia alimentar comum entre os peixes tropicais, mas pouco se
conhece sobre as possíveis causas e consequências deste padrão de comportamento
alimentar. Neste trabalho, levantamos a hipótese de que os peixes tropicais tendem a se
alimentar mais baixo nas redes alimentares para compensar a maior demanda
energética, a qual aumenta com a temperatura da água e o tamanho do corpo do animal.
A análise dos dados de 8172 espécies de peixes marinhos e de água doce do mundo, de
regiões tropicais e temperadas, demonstrou que a posição trófica dos peixes não
carnívoros diminui com o aumento do tamanho do corpo em regiões tropicais, mas não
em regiões temperadas. Este padrão sugere que a maior demanda energética dos peixes
tropicais maiores deve ter exercido uma pressão seletiva para a evolução da onivoria.
Como consequência, a dinâmica trófica dos ecossistemas aquáticos tropicais deve
apresentar padrões distintos aos observados em ambientes temperados, com implicações
importantes para o manejo da qualidade da água e a restauração de ecossistemas
aquáticos eutrofizados. Outra hipótese deste trabalho, é que os efeitos de peixes
planctívoros onívoros sobre comunidades planctônicas tropicais dependem da
composição estequiométrica dos produtores primários que, por sua vez depende da
disponibilidade relativa de luz e nutrientes. Um experimento em mesocosmos
manipulando a disponibilidade de luz e a presença de peixes planctívoros confirmou a
hipótese de trabalho, sugerindo que a composição estequiométrica e consequentemente
a qualidade dos recursos alimentares determinam a estrutura trófica das redes
alimentares pelágicas em lagos tropicais. Finalmente, outro experimento em
mesocosmos sugere que a remoção de peixes onívoros bentívoros deve ser mais eficaz
do que a remoção de peixes onívoros planctívoros para a melhoria da qualidade da água
de lagos e reservatórios tropicais. Este último experimento demonstrou que os peixes
planctívoros onívoros aumentam a biomassa fitoplanctônica através do mecanismo de
cascata trófica sem aumentar as concentrações de nutrientes na coluna d´água. Por outro
lado, os peixes bentívoros onívoros, se alimentando de detritos e outros recursos
bentônicos e excretando nutrientes na água, translocam nutrientes do sedimento para a
coluna d´água, aumentando o aporte interno de fósforo e a biomassa fitoplanctônica
através da sua interação com o sedimento. Portanto, o aporte interno de fósforo pode ser
reduzido e a qualidade da água de lagos tropicais eutrofizados pode ser melhorada
através da remoção de peixes bentívoros onívoros.
Palavras-chave: Onivoria, metabolismo, estrutura trófica,
biomanipulação, ciclagem de nutrientes, estequiometria ecológica.
cascata
trófica,
i
Abstract
Omnivory is a predominant feeding strategy among tropical fishes, but knowledge
about its causes and consequences of this pattern is scarce. In this study we
hypothesized that tropical fish feed lower in food web as a way to compensate a higher
energetic demand, which increases with increasing water temperature and body size.
Information about 8172 freshwater and marine fish species from whole world, from
tropical and temperate ecosystems, showed that the trophic position of non-carnivore
fish decreases with increasing body size in tropical but not in temperate ecosystems.
This result indicates that the higher energetic demand of large-bodied tropical fish
should exert a selective force in favor of omnivory. As a consequence, trophic dynamics
in tropical freshwater ecosystems should have different patterns comparing to temperate
ones, with major implications for water management and restoration of eutrophic
aquatic ecosystems. Another hypothesis of this work was that effects of tropical
omnivorous planktivorous fish on planktonic communities depend of primary producers
stoichiometric composition, which depends of light availability relative to nutrients
ratios. A mesocosm experiment, manipulating light availability and planktivorous fish
presence, confirmed our hypothesis indicating that resource stoichiometric composition
(consequently nutritional quality), determine trophic structure of pelagic food webs in
tropical lakes. Finally another mesocosm experiment indicated that the removal of
omnivorous benthivorous fish should be more efficient than removal of omnivorous
planktivorus fish, as a way to improve water quality in tropical lakes and reservoirs.
This last experiment showed that omnivorous planktivorous fish increase phytoplankton
biomass due to trophic cascade interactions, without increasing nutrient concentrations
in the water column. On the other hand, omnivorous benthivorous fish, feeding on
detritus and other benthonic food sources and excreting nutrients in the water column,
are responsible for translocate nutrient from sediments to the water column, increasing
phosphorus pool and phytoplankton biomass. Thereby, internal phosphorus supply
should be reduced and water quality of eutrophicated lakes could be improved by
removing omnivorous benthivorous fish.
Palavras-chave: Omnivory, metabolim, trophic structure, trophic cascades,
biomanipulation, nutrient cycling and ecological stoichiometry.
ii
Índice
Resumo
i
Abstract
ii
Introdução Geral
2
Capítulo I: "Temperature affects fish body size-trophic position relationship
in freshwater and marine ecosystems."
10
Capítulo II: "Ontogenetic development of omnivorous predator interacts
with resource stoichiometry to affect pelagic food webs."
22
Capítulo III: "Biomanipulation of lakes and reservoir should target the
removal of benthivorous instead of planktivorous fish."
39
Discussão Geral
54
Referências Bibliográficas
59
1
Introdução Geral
Entender a importância das relações alimentares como um elo de ligação das populações
dentro da comunidade foi um marco nos estudos ecológicos. A noção de cadeia e teia
alimentares desenvolvidas por Charles Elton (1927) mostrou uma maneira simples de
representar as conexões entre os indivíduos e espécies que compõem a comunidade.
Esse conhecimento foi posteriormente otimizado pela ecologia energética proposta por
Lindeman (1942) e ainda hoje intriga e desafia pesquisadores.
Desde meados dos anos 60 (Hairston et al., 1960) o interesse por compreender a
natureza dos fatores que estruturam e regulam o fluxo de energia e matéria nas teias
alimentares tem crescido (Power, 1992; Hairston & Hairston, 1993; Moore et al., 2004;
Gonzalez-Bergonzoni et al., 2014; Özen et al., 2014). Ideias como a regulação das teias
alimentares por vias ascendentes (por exemplo, nutrientes) e descendentes (ex.
predadores) (Leibold et al. 1997, Persson, 1999, Polis, 1999, Chase, 2000, Oksanen &
Oksanen, 2000; Borer et al., 2006; Gruner et al., 2008; Shurin et al., 2012; Majdi et al.,
2013) foram alvo de muitos estudos e são ainda bastante usuais.
Para se ter uma ideia clara desse cenário, por volta de 1980, três linhas de pensamento
influenciavam de maneira significativa os trabalhos em ambientes aquáticos. A primeira
delas era que os nutrientes (principalmente o fósforo) desempenhavam um papel
fundamental sobre a biomassa e a produção fitoplanctônica (Schindler, 1977). De fato,
se percebeu que o aporte de nutrientes respondia por mudanças nessas variáveis, mas
ainda existia uma parcela significativa de variância inexplicada (Carpenter et al., 1991).
A segunda ideia era o uso de biomanipulação da cadeia trófica com a finalidade de
aumentar as taxas de herbivoria, e desse modo promover o controle da biomassa algal
nos lagos (Shapiro et al., 1975). Apesar de ser uma ótima ideia, o mecanismo por trás da
melhoria nas condições da água se mostrou muito mais complexo que simplesmente a
manipulação da herbivoria. A terceira linha de pensamento era a união do conceito de
teia alimentar com a ideia de fluxo de carbono e nutrientes através da teia, essa ideia
sugeria que mudanças na estrutura das comunidades poderiam refletir em alterações nos
processos ecossistêmicos assim como nos fluxos biogeoquímicos (Schindler et al.,
1997; Paine 1980).
2
Essas três ideias serviram de alicerce para a construção da teoria de cascata trófica, a
qual sugere que mudanças em um determinado nível trófico afetam negativamente a
abundância e/ou comportamento de organismos em níveis tróficos adjacentes,
geralmente resultando, indiretamente, em respostas inversas na abundância ou biomassa
de níveis tróficos inferiores não adjacentes (Carpenter et al., 1985; Pace et al., 1999;
Polis et al., 2000). Um dos primeiros autores a utilizar o termo "cascata trófica" foi
Paine (1980), muito embora, o pensamento por trás dessa ideia já houvesse sido
trabalhado por Hairston e colaboradores (1960) quando eles usaram a abstração de que
o mundo é verde porque os carnívoros mantém os herbívoros em baixas densidades, o
que permite que as plantas cresçam livres da pressão dos herbívoros. Um exemplo claro
desse efeito de cascata trófica pode ser visto ao se observar que a presença de peixes
piscívoros pode influenciar a abundância de peixes planctívoros, que por sua vez podem
afetar a abundância, estrutura de tamanho e a produtividade da comunidade planctônica
(Brooks & Dodson, 1965; Carpenter & Kitchell, 1993). Carpenter e colaboradores
(1985 e 1987) em uma série de estudos clássicos comprovaram, através da manipulação
da estrutura trófica de lagos com características semelhantes, que, ambientes cujo aporte
externo de nutrientes é similar, podem apresentar diferenças significativas em sua
biomassa e produtividade primária (fitoplanctônica) devido a variações nas estruturas de
suas teias alimentares. Essa teoria tem estimulado pesquisas em diferentes áreas da
ecologia, principalmente como ferramenta de manejo com o objetivo de restaurar
ambientes eutrofizados (Carpenter et al., 1985; Carpenter et al., 1987; Hansson et al.,
1998; Mehner et al., 2002; Albright et al., 2004; Moss et al., 2004).
Durante algum tempo se pensou que a ideia de cascata trófica fosse restrita a ambientes
aquáticos, isso porque nesses ambientes a manipulação trófica resultava em fortes
interações (Strong, 1992; Polis, 1999; Halaj & Wise, 2001; Shurin et al., 2006).
Entretanto, hoje já se sabe da ocorrência de cascatas tróficas em diversos ecossistemas
(Pace et al., 1999; Schmitz et al., 2000; Shurin et al., 2002; Shurin et al., 2005; Shurin et
al., 2006) e mesmo através de ecossistemas (Knight et al., 2005; Romero & Srivastava,
2010; Wesner, 2010). Para abordar essa questão das cascatas tróficas através de
ecossistemas é necessário esclarecer que esse processo envolve espécies que apresentam
histórico de vida complexo, as quais frequentemente mudam de habitat durante seus
ciclos de vida (Werner & Gilliam, 1984), e podem desencadear o processo de
acoplamento de habitats. Nesse sentido interações locais que afetem a abundância de
3
um predador em um determinado ecossistema podem gerar efeitos indiretos em outro
ecossistema. Um exemplo claro disso pode ser descrito ao pensarmos em um simples
lago (Knight et al., 2005, ver figura 1 do artigo), onde os peixes se alimentam de larvas
de insetos aquáticos, insetos esses que na sua fase adulta se alimentam de espécies
polinizadoras. Desse modo os peixes podem ser responsáveis por, indiretamente,
facilitarem a reprodução de plantas terrestres, uma vez que eles, por meio de um efeito
de cascata trófica, reduzem a pressão de competição sobre os polinizadores. Dessa
maneira efeitos diretos dos indivíduos com histórico de vida complexo podem ser
responsáveis por efeitos em cascata que vão alem dos limites do ecossistema.
Embora existam muitas evidências empíricas que dão suporte a essa teoria (Brett &
Goldman, 1996; Brett & Goldman, 1997), e trabalhos demonstrando a prevalência e
ocorrência de cascatas tróficas em ambientes naturais (Vanni et al., 1990; Kauffman et
al., 2010; Dobson, 2014), a ideia de manipulação dos níveis superiores a fim de
controlar as cadeias tróficas sofreu com algumas criticas, principalmente por assumir
que as interações têm uma natureza estática do ponto de vista espacial e temporal
(Chase, 2003) ou mesmo com relação à maneira como é utilizado o termo "cascata
trófica" (Polis et al., 2000). A teoria de cascata trófica chegou a ser contestada devido
ao número de estudos que não apresentavam impactos estatisticamente significativos de
peixes piscívoros ou zooplanctívoros sobre a estrutura das cadeias alimentares em
ambientes de água doce (DeMelo et al., 1992). Isso se deve em parte ao fato de que a
estrutura e a dinâmica trófica dos ambientes naturais são mais complexas do que se
presumiu inicialmente na teoria de cadeias alimentares (Polis & Strong, 1996; Finke &
Denno, 2004; Hillebrand & Cardinale, 2004; Finke & Denno, 2005; Edwards et al.,
2010) o que torna a magnitude dos efeitos de cascata trófica muito mais variáveis (Borer
et al., 2005).
Com base nos elementos apresentados ate aqui fica clara a existência e a onipresença da
cascata trófica. Entretanto, a indicação de ocorrência de cascata trófica não deve ser
baseada apenas em mudanças relativas da biomassa de espécies que ocupam os níveis
mais baixos da cadeia. Tessier e Woodruff (2002) sugerem que os estudos sobre os
efeitos das interações tróficas passem a quantificar a consequência funcional associada a
mudanças na composição das comunidades. Por exemplo, um peixe onívoro como a
tilápia que possui uma atividade filtradora capaz de promover a seleção e captura do
fitoplancton de grande porte, pode exercer uma grande influência sobre a estrutura de
4
tamanho e composição da comunidade fitoplanctônica, sem, entretanto, afetar a
biomassa total do fitoplâncton (Okun et al., 2008). A esse tipo de interação eles
atribuíram o termo cascata trófica "críptica" (Tessier & Woodruff, 2002).
Interações de cascata trófica são comumente identificadas em estudos utilizando peixes
piscívoros e zooplanctívoros (e.g. Brooks & Dodson, 1965; Carpenter et al., 1987;
Carpenter & Kitchell, 1993; Brett & Goldman, 1996), isso se deve ao fato que hoje já se
possui bastante conhecimento acerca dos efeitos desses peixes sobre a comunidade
planctônica (Brooks & Dodson, 1965). Entretanto, a ideia da onivoria altera a força da
cascata trófica. Isso ocorre porque peixes onívoros podem, por diferentes modos, afetar,
direta e indiretamente, diferentes níveis dentro da cadeia trófica, uma vez que é
característica desta guilda utilizar recursos provenientes de mais de um nível trófico
(Pimm & Lawton, 1978). Assim, diferente das espécies piscívoras e zooplanctívoras, os
impactos causados pela presença de peixes onívoros em ecossistemas aquáticos são
mais complexos e isso têm desperto o interesse científico nos últimos anos (Carneiro,
2008). Aliado a isso existe o fato de que nos ambientes aquáticos a onivoria é uma
estratégia alimentar bem difundida entre os peixes, principalmente nos ecossistemas
tropicais de água doce (Fernando, 1994; Gonzalez-Bergonzoni et al., 2012). A simples
presença da onivoria pode ser responsável por mudar alguns conceitos bem
estabelecidos na ecologia. Por exemplo, é consenso que, em peixes, o tamanho corporal
do indivíduo está diretamente relacionado com sua posição trófica (os maiores
indivíduos estão no topo da cadeia) (Pauly, 1998; Romanuk et al., 2011), sendo este
padrão principalmente determinado por uma limitação morfológica associada ao
tamanho da abertura da boca dos predadores para ingerir suas presas.
No primeiro capítulo desta tese é abordada a questão de como o clima afeta a relação
entre tamanho do corpo e posição trófica dos peixes, o resultado encontrado mostra
como a onivoria pode alterar essa relação. A ideia subjacente ao delineamento deste
capítulo foi que, uma vez que as áreas de baixas latitudes (regiões trópicos) apresentam
elevadas temperaturas é esperado que os organismos tenham um aumento da sua
demanda energética (Gillooly et al., 2001, Brown et al., 2004), e que esse aumento seja
proporcional ao tamanho corporal (Peters, 1983; McNab, 2002). Se uma espécie passa a
ser energeticamente limitada por esses fatores é viável pensar que os indivíduos nos
trópicos tenderiam a ser menores (Atkinson, 1994; Atkinson & Sibly, 1997; Blackburn
et al., 1999) e/ou usariam de estratégias diversas para contornar essa limitação (Arim et
5
al., 2007). Uma dessas estratégias seria o forrageio nos níveis mais baixos da cadeia
alimentar, tais como a maior expressão da detritivoria, herbivoria e/ou onivoria.
Portanto, a onivoria surgiria como uma possibilidade de contornar essa possível
limitação energética a qual os indivíduos de grande porte sofrem nos ambientes
aquáticos tropicais.
Grande parte dos impactos causados pelos peixes onívoros sobre a estrutura da teia
alimentar passa diretamente pela seleção do recurso a ser explorado. Essa seletividade
depende de uma gama de fatores como, a qualidade nutricional do recurso, estágio de
vida do consumidor, abundância e disponibilidade do recurso. Por exemplo, embora
peixes onívoros filtradores, como a Tilápia do Nilo (Oreochromis niloticus), possam se
alimentar tanto do fito quanto do zooplâncton, um aumento na densidade ou na
qualidade nutricional do fitoplâncton pode ser responsável por aumentar o grau de
herbivoria do peixe. Uma vez que a as razões estequiométricas do fitoplâncton variam
bem mais que as razões do zooplâncton (Darchambeau et al., 2005) esse tipo de
mudança pode acontecer nos ambientes e, neste caso, a herbivoria seria uma estratégia
alimentar mais eficiente. A qualidade nutricional do fitoplâncton, por sua vez, está
intimamente relacionada com a concentração de nutrientes presentes na composição dos
mesmos, ex. concentrações e razões celulares de C, N, e P. As razões desses elementos
podem variar em resposta a disponibilidade de nutrientes e da radiação no ambiente
(Sternet & Elser 2002). A hipótese da luz e nutrientes (HLN) embasa essa mudança na
estequiometria dos produtores, e prediz que um aumento na razão luz:nutriente aumenta
a razão C:nutriente da alga (reduzindo a qualidade nutricional da mesma) (Sterner et al.
1997).
Além da qualidade nutricional do recurso, outro fator relevante no entendimento do
impacto do onívoro é o papel funcional desempenhado pela espécie, o qual não é
imutável dentro da comunidade (Petchey & Gaston, 2006; Hillebrand & Matthiessen,
2009). A mesma espécie é capaz de apresentar características ecológicas (como dieta e
uso do habitat) completamente distintas em diferentes estágios de vida (Munoz &
Ojeda, 1998; Woodward & Hildrewref, 2002; Rudolf & Rasmussen, 2013).
Normalmente essa mudança no nicho ecológico das espécies pode ser atribuída a
alterações na composição corporal e nas necessidades elementares, associadas às
mudanças ontogenéticas (Werner & Giliam, 1984). Um bom exemplo disso é o
comportamento alimentar de O. niloticus nessa espécie os indivíduos pequenos
6
(<≈60mm) são predadores visuais, e provavelmente selecionam o zooplâncton de
grande porte como presa (com exceção das larvas muito pequenas, as quais são
limitadas pelo tamanho da boca), similar a diversos outros peixes. Estes indivíduos
podem indiretamente favorecer o crescimento fitoplanctônico via efeito de cascata
trófica. Entretanto, indivíduos grandes podem optar por serem filtradores, alimentandose tanto de fitoplâncton como também do zooplâncton, e muito provavelmente de
detritos bentônicos. Dessa maneira eles podem afetar a biomassa fitoplanctônica
diretamente via herbivoria e indiretamente através da redução da densidade do
zooplâncton, pelo mecanismo de cascata trófica. Além disso, ambos os estágios de vida
podem diretamente favorecer o crescimento fitoplanctônico via excreção de nutrientes.
Dessa maneira onívoros filtradores podem afetar as comunidades fitoplanctônicas e
zooplanctônicas, através de mecanismos diretos e indiretos e o seu real efeito será
dependente do estágio de vida do organismo.
Desta maneira o segundo capítulo desta tese avaliou a influência da estequiometria do
recurso sobre o efeito de peixes planctívoros sobre as teias tróficas pelágicas. A ideia
que estimulou esse trabalho foi que o balanço entre luz e nutrientes controla a
composição estequiométrica dos produtores (Sterner et al., 1997), os quais por sua vez,
influenciam a produção secundária, a ciclagem de nutrientes e a eficiência na
transferência de energia dentro das teias tróficas aquáticas (Sterner & Elser, 2002;
Dickman et al., 2008). Dessa maneira é esperado que em ambientes com alta
disponibilidade de luz relativa a fósforo, efeitos de cascata trófica sejam enfraquecidos
no nível do herbívoro, uma vez que, a qualidade nutricional do alimento é baixa o
desenvolvimento do herbívoro seja limitado, reduzindo sua capacidade de responder a
uma redução na pressão de predação pelo peixe planctívoro.
Outro pensamento, posto em cheque pela onivoria é a ideia simplista de reduzir a
estrutura dos ecossistemas a apenas uma cadeia trófica, comprometendo o entendimento
das relações que ali ocorrem (Polis & Strong, 1996). Em um ambiente natural os
integrantes (predadores, presas e recursos) podem ultrapassar os limites de
compartimentos, habitats e ecossistemas (Polis, 1991), o que gera um acoplamento entre
esses compartimentos (Schindler & Scheuerell, 2002), permitindo troca de matéria e
energia entre eles (Vanni et al., 2002). Um claro exemplo desse efeito de acoplamento
mediado por peixes onívoros foi apresentado por Schaus e Vanni (2000). Nesse trabalho
7
os autores observaram a capacidade de um peixe onívoro (Dorosoma cepedianum)
translocar nutrientes do habitat bentônico para o habitat pelágico.
Essa translocação ocorre durante a interação do peixe com o sedimento do lago, e pode
causar um processo conhecido como bioturbação, que seria a mistura e a ressuspensão
de parte do sedimento causando um aumento da turbidez (Breukelaar et al.,1994; Croel
& Kneitel, 2011) e da concentração de nutrientes (Schaus & Vanni, 2000; Adamek &
Marsalek, 2013) na coluna de água. Ou seja, além da parcela de nutrientes oriundos da
reciclagem de nutrientes pelos peixes (excreção), que tem um papel fundamental na
estruturação dos ambientes aquáticos (Vanni & Layne, 1997; Attayde & Hansson, 2001,
Torres & Vanni, 2007), surge uma “nova” fonte de nutrientes, pois é diferente daquela
originada pelo padrão convencional de reciclagem (Caraco et al., 1992), que é
dependente do acoplamento de habitats mediado pelo acesso do peixe ao sedimento.
Esse aporte alternativo de nutrientes pode resultar em um aumento na disponibilidade
de nutrientes para os produtores primários, levando a mudanças na biomassa e na
estrutura da composição da comunidade planctônica (Schaus & Vanni, 2000). Esse
impacto de peixes que apresentam um hábito bentônico mediado pelo seu acesso ao
sedimento, sobre a dinâmica de nutrientes no ecossistema aquático é tema do terceiro
capítulo dessa tese.
Dessa maneira o terceiro capítulo desta tese avaliou e quantificou, através de dois
experimentos em escala de mesocosmo (o primeiro realizado com o peixe bentívoro
Prochilodus brevis e o segundo com o onívoro filtrador Oreochromis niloticus), o efeito
do acesso ao sedimento por peixes onívoros sobre a comunidade planctônica e o fluxo
de nutrientes na coluna de água. A ideia que levou ao desenvolvimento deste capítulo
foi que peixes com hábitos bentônicos podem ter um forte efeito sobre a comunidade
planctônica em lagos rasos tropicais, mas que esse efeito é determinado pelo acesso do
peixe ao sedimento. O que colocaria em cheque a ideia de que o impacto dos peixes
sobre as comunidades planctônicas são fracos em lagos quentes quando comparados
com lagos mais frios (Lazzaro, 1997; Moss et al., 2004; Stephen et al., 2004; Jeppesen
et al., 2007), uma vez que, mesmo que de maneira indireta, os peixes seriam
responsáveis por alterar a disponibilidade de nutrientes para os produtores.
8
Desse modo, o efeito de espécies onívoras em ambientes aquáticos é extremamente
variável, o que dificulta fazer qualquer tipo de previsão sobre o efeito dessas espécies na
teia trófica e propor estratégias clássicas de manejo em ambientes com alto grau de
onivoria. A proposta desta tese é detectar padrões de posição trófica em relação ao
tamanho de corpo dos peixes tropicais e temperados e avaliar, as consequências da
onivoria dos peixes para a estrutura e dinâmica trófica nos ecossistemas aquáticos
continentais.
9
Capítulo I
Temperature affects fish body size-trophic position relationship in
freshwater but not in marine ecosystems.
Danyhelton D. F. Dantas1, Ronaldo Angelini2, Adriano Caliman1, Luciana S. Carneiro1, Sergio M. Q.
Lima3, Pablo A. Martinez4 & José L. Attayde1.
1
Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal 59078-900, Brasil.
2
Departamento de Engenharia Civil, Universidade Federal do Rio Grande do Norte, Natal 59078-900,
Brasil.
3
Departamento de Botânica, Ecologia e Zoologia, Universidade Federal do Rio Grande do Norte, Natal
59078-900, Brasil.
4
Departamento de Biologia e Geologia, Física e Química inorgânica, Universidade Rey Juan Carlos,
Mostoles, Madrid, Espanha.
10
Abstract
The trophic position of fish species in aquatic food webs is constrained by their
energetic demand, which scales positively with fish body size and water temperature.
We hypothesized that larger fish species with higher energetic demand would tend to
become more energy limited and forage lower in the food web with increasing water
temperature. We tested the hypothesis that the trophic position of larger fish species
would be lower in tropical than in temperate waters. Using the FishBase dataset, we
analyzed the relationship between the maximum length (body size) and trophic position
of 7,587 ray-finned fish species, categorized according to ecosystem type (freshwater or
marine) and climatic region (tropical or temperate). Linear mixed-effects models
(LMMs), with controlled nested effect for phylogeny (i.e., order, family, and genus),
confirmed the prediction for the entire dataset and for freshwater but not for marine fish
species. The results suggest that fish species compensate for the energetic constraints of
a larger body size by increasing omnivory in tropical freshwaters. On the other hand, the
larger size of marine ecosystems may compensate for energy limitation and fulfill the
greater energetic demand of larger fish in tropical marine waters. Our results suggest
that global warming may affect the fish trophic position and food-chain length in
freshwater but not in marine ecosystems.
Keywords: trophic structure, omnivory; energy limitation; global warming.
11
Introduction
Energy flows in ecosystems supports life and are guided by the laws of
thermodynamics. As energy moves up through a food web, much of it is lost as heat of
respiration, with a consequent decrease in energy availability to top predators (Elton
1927). The absolute rate of respiration depends on the energetic demand of the species
and individuals, which increases with increasing body size (Peters 1983, McNab 2002)
and temperature (Gillooly et al. 2001, Brown et al. 2004). If no other ecological
mechanism compensate for energy limitation, the expected increase in absolute
individual’s energetic demand with increasing body size and temperature, requires an
increase in individual’s energy consumption to compensate for its higher absolute
energetic demand (Arim et al. 2007). Corollary, as individuals become more energy
limited with increasing body size and temperature, they would tend to be smaller
(Atkinson 1994, Atkinson & Sibly 1997, Blackburn et al. 1999) and/or forage lower in
food webs in warmer temperatures (Arim et al. 2007).
Furthermore, fish body size and trophic position are expected to be positively correlated
(Romanuk et al. 2011). Fish gape-size is a function of fish body size and puts an upper
limit to the size of the prey a predator can consume creating a hierarchy of trophic
connections in which large animals consume small ones (Arim et al. 2007). Larger
individuals have the morphological ability to occupy higher trophic positions in the
food web but also have higher absolute energetic demands and should be limited by the
amount of energy available to them. Therefore, energetic constraints limit the trophic
position of larger animal individuals if no other ecological processes (i.e. reduction in
abundance) compensate for energy limitation (Arim et al. 2007).
This paper addresses the question of how temperature affects fish trophic position and,
therefore, food-chain length in freshwater and marine food webs. We tested the
hypothesis that the trophic position of larger fish is lower in tropical than in temperate
waters (Figure 1). In terms of climate change, this question can represent important
theoretical and applied ramifications as aquatic food web structure and dynamics might
be impacted by an increase in water temperature.
12
Figure 1: Hypothesized relationships between fish trophic position and body size in tropical (solid line)
and temperate (dashed line) ecosystems. Warmer temperature is expected to decrease trophic position for
larger more than for smaller ray-finned fish.
Methods
We obtained data on maximum total length (body size) and trophic position for 7.587
ray-finned fish (Actinopterygii) species, the dominant of freshwater and marine
vertebrate fauna (Near et al., 2012), from FishBase (www.fishbase.org; see S1). In
FishBase, freshwater and marine species are categorized according to climatic zones
and depth ranges (Froese & Pauly 2011). To avoid confounding effects by including
species which distributions do not correspond to a particular climate, we only included
in our analysis species that have the preferred depth range above 200 m and are
categorized as tropical or temperate. Since species have a shared evolutionary history,
species level studies require control of the phylogenetic dependence, being the
phylogenetic generalized least squares regression most widely used method (Felsenstein
1985; Garamszegi 2014). Unfortunately, the actinopterygii, which comprises about half
of vertebrate species richness (Thomson & Shaffer, 2010; Eschmeyer & Fricke, 2012),
are the most unknown group of vertebrates from a phylogenetic point of view, being
represented less than 5% of their species according with recent phylogenies researches
(Thomson & Shaffer, 2010; Near et al., 2012). Given the lack of phylogenies, a valid
alternative would be a linear mixed-effect models (LMMs), using the taxonomic
categories as random effects (Bunnefeld and Phillimore, 2012; Luiz et al, 2012; Luiz et
al. 2013). Therefore, we chose to perform a mixed-effect linear model to control for the
effect of non-independence of species traits, using as nested random factors the order,
13
family and genera of the species. Trophic position was the response variable, ecosystem
type (freshwater or marine), climatic zones (tropical or temperate) and maximum body
length were included as fixed variables and phylogenetic resolution such as order,
family and genus were included as nested random variables.
Defined as the longest individual recorded for a given species, maximum total body
length was used as a metric of body size (Froese & Pauly, 2013). Although mass, not
length per se, is the most relevant size metric for exploring energetic constraints,
maximum total body length was used as a proxy of maximum body mass because these
two variables are highly positively correlated (r2= 0.94, p< 0.001 see Romanuk et al.,
2011) and data on maximum body mass was not available for many species. Trophic
position is calculated in FishBase by adding 1 to the mean trophic position, weighted by
relative abundance, of all food items consumed by a species (Froese & Pauly, 2013).
For a given consumer j, trophic position is defined as:
S
Trophj =1+ å DCij *Trophi
i=1
where Trophyi is the fractional trophic level of preyi, DCij is the proportion of prey i in
the diet of a consumer (j) and S is the total number of prey species. Trophic position
values are based on diet information for each species supported by more than 800
references and the verification of over 16,000 records (Froese and Pauly 2013). Prey
items include organisms that have been found in stomach content analysis or are
otherwise known to be ingested by a given species. In cases when diet composition data
is lacking the approach chosen to estimate trophic position relies on the demonstrated
similarity of trophic positions in taxonomically related species, and on the equally well
established relationship between body size and trophic level, anchored in a value of
trophic position equal to 3.0 for larvae of about 1 cm (Froese and Pauly, 2013). In
FishBase, primary producers and detritus (including associated bacteria) are assigned a
trophic level of 1, while primary consumers, which consume mainly plant or detritus are
assigned trophic positions between 2 and 2.19. We excluded these from the analysis
because their trophic position did not vary with body size and thus cannot usefully
inform an analysis of the relationship between body size and trophic position in fishes.
Omnivores, which consume plants or detritus as well as animals, have trophic positions
between 2.20 and 2.79, while carnivores are assigned trophic positions ≥ 2.8.
14
Species that have their preferred upper depth range below 200 m were excluded from
our analysis because they are classified as cold-water regardless of their climatic zone.
Species classified as subtropical were also excluded from our analysis because many
cosmopolitan fishes that occur in both tropical and temperate zones are included into
this category. For ecosystem type classification, since some freshwater fishes enter
brackish and marine water and vice versa, FishBase assign the three yes-no categories
Saltwater, Brackish, Freshwater on the basis of occurrence and tolerance reported in the
literature. For this paper we only considered species with one classification. Fishbase
considers as a primary freshwater (or a primary marine) species a fish that has evolved
in freshwater (or saltwater) and spends all their life time there. Data on maximum total
body length and trophic position were log10 transformed prior to the analysis to meet the
assumptions of the statistical analysis.
The LMM fitted using the function “lmer” from the package “lme4” (Bates et al., 2014) in
R. For model selection we used the Akaike’s Information.
Results
We observed a significant effect of the interaction between climate and ecosystem type
on fish trophic position and this interaction was dependent on maximum body length
(Table 1). We found that the expected temperature effect on the trophic position of
larger fish was significant for the whole dataset and for freshwater fish species but not
for marine ones (Figure 2). Across all fishes and for freshwater fish species the positive
relationship between maximum body length and trophic position was weaker for
tropical than for temperate species (comparison of the slopes in Fig. 2 and 3a). On the
other hand, across all marine fish species similar relationships were found for tropical
and temperate species (comparison of slopes in Fig. 3b). Non-independence species
traits (phylogeny) did not affect the results, since phylogenetic dependence were
controlled by LMM, which using taxonomic categories as random effect.
15
Table 1: Results of the Linear Mixed-Models for all 7587 species of Actinopterygii used in this study. In
this analysis, phylogeny did not affect the results, once taxonomic categories (order, family, and genus)
were used as nested random factors to control for the effect of nonindependence of species traits. The
nested random factors explain 82% of variance. The slope of the relation with 95% confidence intervals
(CI), t-value, and p-value are shown. Bold values are significant (p < 0.05).
Source of variation
Slope
CI (95%)
t-value
p
Climate (C)
0.019
0.005; 0.465
2.79
0.005
Ecosystem (E)
-0.013
-0.010; 0.035
1.11
0.268
Body size
0.041
0.032; 0.050
8.56
<0.001
C×E
-0.025
-0.478; -0.002
2.16
0.031
C × Body size
-0.015
-0.025; -0.005
2.90
0.004
E × Body size
0.006
-0.009; -0.022
0.81
0.419
C × E × Body size
0.020
0.003; 0.036
2.34
0.019
16
Figure 2: Trophic position as a linear function of the maximum total body length for all actinopterygian
fish, grouped according to tropical (dashed line; grey circles; n = 6,549) and temperate (solid line; dark
grey squares; n = 1,038) climates. Confidence intervals of 95% showed that the slopes of the trophic
position-body length relationships were significantly different between tropical and temperate climates.
17
Figure 3: Trophic position as a linear function of the maximum total body length for Actinopterygii
species across (A) freshwater (n = 5,972 species) and (B) marine (n = 1,615 species) ecosystems. In each
panel, species were grouped according to tropical (dashed line; grey circles) and temperate (solid line;
dark grey squares) climates. Confidence intervals of 95% showed that the slopes of the trophic positionmaximum total body length relationships were significantly different between tropical and temperate fish
species in freshwater but not in marine ecosystems.
18
Discussion
Our results show that larger freshwater fish forage lower in the food web in warmer
tropical climate compared to cooler temperate climate, indicating that the support of our
hypothesis is dependent on ecosystem type. Food availability increases as we go down
the food web, implying that the energetic demands of larger animals are more easily met
for herbivores, detritivores and omnivores than for carnivores. Therefore, feeding on
primary producers and detritus may compensate for energy limitation and fulfill the
greater energetic demand of larger fish in warmer freshwaters. Recent studies have
demonstrated shorter food chain length (Doi et al. 2012) and greater catabolic demand
(Amado et al. 2013) for freshwater communities in warmer climates. Furthermore, a
recent meta-analysis shows a consistent increasing trend in the relative richness of
omnivorous fish with decreasing latitudes for both freshwaters and marine ecosystems,
but omnivore richness was higher in freshwaters than in marine ecosystems (GonzálezBergonzoni et al. 2012) a pattern also observed in our study (S1). Combined with the
fact that our results were unaffected by phylogeny, these aforementioned body of
evidences may indicate that the structure and topology of freshwater food webs were
more affected by climate-dependent mechanisms that constraints energy flow than
marine food webs.
The larger size of marine ecosystems may compensate the energy limitation and fulfill
the greater energetic demand of larger fish in warmer marine waters. Ecosystem size is
positively correlated to food chain length (Post et al. 2000; Post 2002, Takimoto & Post
2013). Larger ecosystems may have greater total resources available at the base of food
webs (Schoener 1989) and higher functional trophic diversity (Cohen & Newman 1991;
Post et al. 2000) to maintain longer food chains. Moreover, spatial processes in larger
ecosystems may enhance the persistence and stabilize predator-prey interactions,
promoting long food chains (Wilson et al. 1998; Holt 2002; Takimoto et al. 2012).
Alternatively, the larger range of water temperature found in freshwater than in marine
ecosystems from temperate to tropical climatic zones may partially explain the observed
pattern. Therefore, fish body size-trophic position relationship would not be affected by
climate in marine ecosystems because water temperature in larger marine systems is not
so strongly influenced by climate as it is in smaller freshwater ecosystems. Whatever
the mechanistic explanation may be, our results indicate that global warming may affect
19
food-web structure in freshwater but not in marine ecosystems, decreasing the trophic
position of larger fish and the length of food chains. Such alterations in the topology of
freshwater food webs in response to increasing temperature may affect the connectivity
and the interaction strength among species and consequently, the ecosystem attributes
that are governed by these food web properties.
20
Supplementary material.
S 1: Table showing relative frequency of omnivorous and carnivorous for all classifications applied in
this work.
% omnivorous % carnivorous
Tropical
12.61
87.39
Temperate
6.55
93.45
Freshwater Tropical
13.89
86.11
Freshwater Temperate
8.66
91.34
Marine Tropical
7.52
92.48
Marine Temperate
1.34
98.66
S 2: Results of linear mixed-effect model of climate (tropical and temperate), ecosystem (freshwater and
marine), body size (cm), and their interactions on trophic position. Akaike’s Information Criterion (AIC),
the log-Likelihood (logLik), Chi-Square test (Chisq), Chi-Square probabilities (p(>Chisq)), and degree of
freedom (DF) are listed for each model.
Model
DF Chisq p(>Chisq) logLik AIC ∆AIC
Trofic~Climate
6
6.53
0.01
8596.4 -17181 354
Trofic~Ecosistem
6
0
1
8593.7 -17175 360
Trofic~Climate*Ecosistem
8
6,41
0.04
8596.9 -17178 357
Trofic~Climate*Ecosistem*Bodysize 12 365.03 <0.0001 8779.4 -17535
0
21
Capítulo II
Ontogenetic development of omnivorous predator interacts with
resource stoichiometry to affect pelagic food webs.
Danyhelton D. F. Dantas1, Jennifer M. Newell2, Jandeson B. Dias3, Renata F. Panosso1, Maria J.
González2, Michael J. Vanni2, Jose L. Attayde1.
1
Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal 59078-900, Brasil.
2
Department of Zoology, Miami University, Oxford, Ohio.
3
Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21230770, Brasil.
22
Abstract
The balance between light and nutrients controls the stoichiometric composition of
phytoplankton, which is known to influence secondary production and nutrient cycling by
aquatic consumers. Therefore, we hypothesize that the stoichiometric composition of
phytoplankton may influence the predation and excretion effects of planktivorous fish on
pelagic food webs. To test this hypothesis we performed a mesocosm experiment with a 2 x 3
factorial design, where two levels of light (low and high) were combined with three levels of
planktivorous fish (no fish, with zooplanktivorous fish, with omnivorous filter-feeding fish).
The zooplanktivorous larvae and omnivorous juvenile stages of the planktivorous fish species
Oreochromis niloticus was used in our experiment to manipulate the planktivore type while
standardizing the fish species. The six treatments were replicated four times and randomly
allocated in 24 mesocosms (250L). The experiment lasted 21 days and each mesocosm was
monitored, at the beginning and at the end of the experiment, for the stoichiometric composition
of organic particulate matter (seston) and the abundance and composition of phytoplankton and
zooplankton communities. Nutrient excretion by fish was also measured at the end of the
experiment. Results of a two-way ANOVA show that fish increased seston C:P and N:P ratios
and that this effect was stronger when light was high relative to nutrient availability. Total
phytoplankton biovolume increased with increasing light availability in the absence of fish,
while in treatments with fish no change in total phytoplankton biovolume was observed in
response to light availability. Fish increased the proportion of cyanobacteria at high light levels.
Results of the contrasts among the three levels of fish show that juvenile fish account for most
of the significant fish effect on seston C:P and N:P ratios and on phytoplankton biovolume and
composition. A significant interaction was observed between light and fish effects on total
zooplankton density, as fish larvae increased total zooplankton density but only at high light
levels. On the other hand, both fish stages increased the proportion of small grazers,
independent of light levels. The above results suggest that when phytoplankton is carbon rich
and phosphorus poor, planktivorous fish release less phosphorus back to phytoplankton,
increasing phosphorus limitation and favoring cyanobacteria species with high affinity for
phosphorus. This effect is stronger in juvenile stages for which P demand for fish growth is
higher. We conclude that resource stoichiometry interacts with the ontogenetic development of
planktivorous fish to influence their effects on pelagic food webs.
Key words: Stoichiometry theory, planktivorous fish, trophic cascade, omnivory.
23
Introduction
Ecological stoichiometry theory predicts that the balance between light and nutrients
influences the stoichiometric composition of primary producers (Sterner et al., 1997),
which is known to influence secondary production, nutrient recycling and the efficiency
of energy transfer in aquatic food webs (Sterner & Elser, 2002; Dickman et al., 2008).
According to this theory, as light relative to phosphorus availability increases, lake
ecosystems become more carbon rich and phosphorus poor, causing direct P limitation
of the growth of multiple trophic levels, weakening the strength of trophic cascades and
diminishing P recycling by consumers (Sterner et al., 1997). In lakes with high light to
phosphorus ratios, trophic cascades would be dampened at the herbivore level because
nutritional constraints on herbivore growth would decrease their ability to respond to
reduced predation pressure by planktivorous fish (Frost et al., 2006). In such lakes, Plimited consumers would have low rates of mass-specific P release as they would
increase the efficiency of P uptake and retention. On the other hand, in lakes with low
light to phosphorus ratios opposite patterns would be expected.
The effects of planktivorous fish on the structure and dynamics of planktonic
communities have been well documented in the last five decades (Carpenter & Kitchell,
1993). It has been recognized that planktivorous fish not only affects plankton through
size-selective predation on zooplankton, but they can also affects plankton through
nutrient recycling (Vanni et al., 1997; Attayde & Hansson, 2001; Vanni, 2002). In
tropical lakes some planktivorous fish are filter-feeding omnivores and can also affects
plankton through grazing on phytoplankton (Lazzaro 1987; Menezes et al., 2010).
Although these effects of planktivorous fish on plankton communities have been
extensively investigated, the influence of resource stoichiometry on such effects have
been largely neglected (but see Higgins et al., 2006; Dickman et al., 2008).
We hypothesized that trophic cascades by visual-feeding zooplanktivorous fish would
be stronger at low light to phosphorus ratios as predicted by ecological stoichiometric
theory. However, we hypothesized that grazing on phytoplankton by filter-feeding
omnivorous fish would be higher at low light to phosphorus ratio, compensating the
effects of stronger trophic cascades and resulting in weak response of total
phytoplankton biomass to filter-feeding planktivorous fish (Figure 1).
24
Here, we investigate whether the effects of planktivorous fish on plankton communities
depend on the light to phosphorous ratio, which is known to determine the seston C:P
ratio in lakes (Sterner et al., 1997). We used the species Oreochromis niloticus (Nile
tilapia) as a model system because it is widespread in tropical freshwater ecosystems
and has an ontogenetic niche shift from a visual-feeding zooplanktivory to filter-feeding
omnivory (Beveridge & Baird, 2000). Thus, using zooplanktivorous larvae and
omnivorous juveniles of O. niloticus allowed us to manipulate planktivore type while
standardizing the fish species. However, manipulating planktivore type in this way
would introduce a confounding effect of different fish sizes and metabolic rates. To
counteract this problem, the stocking densities of the larvae and juvenile fishes were
adjusted to guarantee similar metabolic rates.
25
Figure 1: Conceptual model showing expected interactions in (A) high light condition (HL) and (B) low
light conditions (LL). Arrows thickness indicates intensity of the interaction.
26
Methods
Study site and Experimental design
We conducted a mesocosm experiment in a fish hatchery station located at the UFRN
campus in Macaíba, Rio Grande do Norte, Brazil (5°53'7"S; 35°21'38"W). We used a
2x3 factorial design with two light levels (low and high) crossed with three fish level
(no fish, with larvae or juvenile of tilapia). These six treatments were replicated four
times and randomly allocated to 24 mesocosm (250 L). Mesocosms were filled with a
mixture of water and plankton from a mesotrophic reservoir and a eutrophic fish pond
of the hatchery station. This was done to provide an inoculum of plankton species from
both mesotrophic and eutrophic systems.
On 27th March mesocosms were filled and water and plankton samples were taken from
six randomly chosen mesocosms to check for similar initial conditions. On the same
date, half of the mesocosms was covered with a fine screen while the other half was
covered with a gross screen to manipulate the two light levels. The two screens,
respectively, reduced 10% and 90% the radiation on the water surface of the
mesocosms. Fish used in the experiment were collected from the fish ponds and added
to the mesocosms on 8th April when the experiment started. In the treatments with
juvenile fish, three individual were added per tank (77-95 mm SL), while in the
treatments with fish larvae, we added 12 individuals per tank (20-45mm SL) in order to
achieve similar metabolic rates in all fish treatments (assuming metabolic rate scales
with the ¾ power of fish mass). Samples were taken on 8th and 29th April at the start and
end of the experiment, respectively.
Sampling and analysis
Water samples were collected from each mesocosm with a PVC tube (1m) from which
subsamples were taken for analysis of seston stoichiometry, phytoplankton and
zooplankton abundance and community composition. Seston samples were filtered
through a pre-ashed Pall A/E glass-fiber filters. Seston C and N concentrations were
measured using a Perkin Elmer Series 2400 carbon–hydrogen–nitrogen analyzer (Perkin
Elmer), while seston P concentration was analyzed following HCl digestion using the
molybdenum blue method with a Lachat QC 8000 FIA autoanalyzer (Lachat
27
Instruments; Stainton et al., 1977). Seston C, N, and P concentrations were used to
calculate C : N, C : P, and N : P ratios, which are expressed here in molar units.
Subsamples for phytoplankton analysis were fixed with lugol’s solution. Phytoplankton
was quantified according to Utermöhl’s method (Wetzel & Likens, 2000) under an
inverted microscope. Before counting, subsamples were allowed to sediment for 3h for
each centimeter height of the chamber. The individuals (cells, colonies and filaments)
were enumerated in random fields as proposed by Uhelinger (1964), with an error
smaller than 20% and a confidence interval of 95% (Lund et al., 1958). To estimate the
phytoplankton biovolume at least 25 individuals from each species were measured by
applying approximations to similar geometric solids.
For zooplankton analysis a subsample of 30L were filtered through a plankton net with
68µm mesh size and preserved with 4% formaldehyde. Zooplankton organisms were
counted under a microscope in a 1mL Sedwick-Rafter chamber. Zooplankton was
divided in two size classes: large (cladoceran and adults copepods) and small (nauplii
copepod and rotifer) zooplankton.
We also quantified nutrient excretion rates of fish at the end of the experiment. We
randomly removed one single individual from each mesocosm of the juvenile fish
treatments and four individuals from each mesocosms of the fish larvae treatments and
put them separately in plastic bags filled with distilled water to release nutrients for one
hour. Water samples were then collected from each plastic bag and used to quantify
phosphorus and nitrogen concentration excreted by fish.
Prior to all statistical analyses, when necessary, data was transformed to homogenize
variances. To analyze the effects of light availability, planktivorous fish and their
interactions we conducted a two-way ANOVA.
Results
Increasing light availability increased seston C:P and C:N ratios, while fish increased
seston C:P and N:P ratios (Figure 2). We found a significant interaction between the
light and fish effects on seston C:P and N:P, the effects of fish being stronger at high
light availability (Figure 2). A significant interaction was also found between the light
and fish effects on total phytoplankton biovolume and the proportion of cyanobacteria
and chlorophytes (Figure 3). Total phytoplankton biovolume increased with increasing
28
light availability in the absence of fish, while in the presence of fish no change in total
phytoplankton biovolume was observed in response to light availability (Figure 3a).
Fish increased the proportion of cyanobacteria at high light levels, while increased the
proportion of chlorophytes at low light levels (Figure 3b, c). Both light and fish
decreased the proportion of diatoms, but no significant interaction between their effects
on diatoms was found (Figure 3d). Results of the contrasts between the three levels of
fish show that juvenile fish accounted for most of the fish effects on seston C:P and N:P
ratios and on phytoplankton biovolume and composition (data not shown).
A significant interaction was observed between light and fish effects on total
zooplankton density, as fish larvae increased total zooplankton density but only at high
light levels (Figure 4a). On the other hand, both fish stages increased the proportion of
small grazer, independent of light level (Figure 4b). Mass-specific P excretion rates by
fish larvae were higher than by juvenile fish, but were apparently not affected by light
availability (Figure 5a). The mass-specific N excretion rates were marginally affected
by fish and light but no significant interaction was observed between these two factors
(Figure 5b). The N:P ratio released by juvenile fish increased with increasing light
availability, but no significant interaction was observed between the effects of fish and
light on this ratio (Figure 5c). Because, the two fish treatments had different stocking
biomass to allow similar metabolic rates, the rates of nutrient excretion by the total
amount of fish was similar between the fish treatments.
29
Figure 2: Effects of light and fish levels and their interactions on seston C:N (A), C:P (B) and N:P (C)
molar ratios. HL - high light condition; LL – low light condition. Different letters represent significant
difference between treatments. Bars represent standard deviation.
30
Figure 3: Effects of light and fish levels and their interactions on total phytoplankton biovolume (A), the
proportion of total biovolume composed by cyanobacteria (B), chlorophytes (C) and diatoms (D). HL high light condition; LL – low light condition. Different letters represent significant difference between
treatments; same letters shows no difference between treatments. Bars represent standard deviation.
31
Figure 4: Effects of light and fish levels and their interactions on total zooplankton density (A) and the
proportion of such total density composed by small grazers (B). HL - high light condition; LL – low light
condition. Different letters represent significant difference between treatments, same letters or absence
shows no difference between treatments. Bars represent standard deviation.
32
Figure 5: Mass-specific nutrient excretion rates for (a) phosphorus, (b) nitrogen and (c) N:P excretion
rates. HL - high light condition; LL – low light condition. Bars represent standard deviation. Significant
values (p<0.05) are in bold.
33
Discussion
In this work we showed that the effects of planktivorous fish on plankton communities
depend on the relative availability of light and nutrients. Our results confirmed the
assumption of increasing seston carbon relative to nutrient ratios with increasing light
availability (Sterner et al., 1997), but also show that the effects of light on seston
stoichiometry depends on planktivorous fish. At high light to phosphorus availability,
planktivorous fish shoud be limited by phosphorus and should release nutrients at high
C:P and N:P ratios. However, only juvenile fish released nutrients at higher N:P ratios
with increasing light availability and this was caused by an increase in N instead of a
decrease in P release rates with increasing light availability. Therefore, the effects of
fish on seston stoichiometry can only partially be explained by fish-mediated nutrient
recycling and our hypothesis that mass-specific P release rates would decrease with
increasing light availability was not confirmed.
We predicted that variation in primary producers’ nutritional quality would be
responsible for changes in the effects of planktivorous fish on plankton communities. In
particular we expected that trophic cascades by visual-feeding zooplanktivorous fish
would be stronger at low light to phosphorus ratios. On the other hand, we hypothesized
that grazing on phytoplankton by filter-feeding omnivorous fish would be higher at low
light to phosphorus ratio, compensating the effects of stronger trophic cascades and
resulting in weak response of total phytoplankton biomass to filter-feeding
planktivorous fish.
We expected that the strength of trophic cascade effects of both planktivores types
would decrease with increasing light availability, but we found only weak evidence
supporting our hypothesis. We also expected that omnivorous filter-feeding juveniles
would have weaker trophic cascade effects on phytoplankton than zooplanktivorous
larvae at low light to nutrient ratios. This is because tilapia grazing would be stronger
under this condition, when seston quality is higher.
34
At high light condition omnivore’s food choice apparently was more influenced by
quantity than quality of food. We used results of fish nutrient excretion experiment to
evaluate fish food choice. Since fish nutrient excretion rates are expected to reflect
stoichiometry of food source we expected that if large tilapia feed heavily on
phytoplankton under low light conditions, P excretion rates should be relatively high
(because algal C:P will be low), and we predict that they will excrete at low N:P. If
these individuals feed (partly or wholly) on phytoplankton under high light, they should
excrete less P (and at higher N:P) than at low light. N:P excretion ratio across light
treatments may be especially pronounced if P assimilation efficiency is lower on Pdeficient phytoplankton, as has been show for others organisms (Higgins et al., 2006;
Frost et al., 2004).
Excretion results showed evidence that food quantity was more determinant than quality
in choosing of a most suitable feeding strategy by omnivorous filter-feeding fish. Even
in presence of low nutritional quality food (high light conditions) juvenile fish grazing
on phytoplankton. Thus, P excretion rate for large fish in high light condition was
smaller than other treatments and N:P ratio was higher. Similar to our results Higgins et
al. (2006) also found that even in presence of a better quality food (large bodied
zooplankton) omnivorous gizzard shad feed on detritus (a bad quality food). In our
study high light juvenile treatment was dominated by Nostocales, a cyanobacteria taxa
characterized as a filamentous and nitrogen fixing. Cyanobacteria are well known as a
“bad” food, some mechanisms proposed to account for this scenario include physical
interference (Gliwicz & Siedlar, 1980), nutritional inadequacy (Martin-Creuzburg et al.,
2008), protease inhibition (Agrawal et al., 2001; Kuster & Von Elert, 2013) and toxicity
(DeMott & Moxter, 1991; da Costa et al., 2013). A significant positive correlation
between percentage of cyanobacteria in total biovolume and seston C:P ratios (p<0,001;
r2=0,715) was found, reinforcing the argument of a bad quality food in this treatment.
For low light-juvenile treatment, excretion and phytoplankton community composition
results indicated that fish grazing on palatable phytoplankton groups. Excretion
experiment done with juvenile fishes in low light condition showed a high P excretion
and low N:P excretion. About plankton community composition chlorophytes
dominated in this treatment. Generally chlorophytes are considered a intermediate
quality food (Klausmeier et al., 2004). This group showed a absence of relationship
with seston C:P ratios (p<0,815; r2=0,003).
35
Moreover, the mass-specific nutrient excretion ratios of phosphorus and nitrogen
showed a higher excretion rate for larvae fish, probably this difference could be related
to differences in individual body N:P ratios. Because the elemental content of an
individual’s body and diet often change during development, the ecological
stoichiometry of an individual should also vary ontogenetically. For example, larger and
more developed individuals, as our juvenile fish, often have higher calcium and
phosphorus contents, likely due to bone formation (Davis & Boyd, 1978; Hendrixson et
al., 2007; Pilati & Vanni, 2007). In addition, larger individuals often having greater fat
stores and higher carbon contents than smaller individuals. The relationship between
ontogenetic diet shifts and a consumer’s body composition (and needs) may be quite
complex, depending on the nature of the diet shifts. However, we are confident that
variations in fish nutrients excretion rates among treatments are due to food nutritional
quality, since the positive association between nutritional quality of ingested food and
nutrient excretion rates are consistent with the prediction that nutrients releases rates
increase with food nutrient content.
In both light conditions, high- and low light, we expected that larvae fish, due to
zooplanktivory feeding strategy, reduce zooplankton density, and through a classic
trophic cascade increased phytoplankton biomass. Trophic cascade effect did not
involve only shifts in biomass, its occurrence could be characterized by change in
communities composition or functional groups, resulting in a cryptic trophic cascade
(Tessier & Woodruff, 2002). Many studies that aim to find trophic cascade effect in
aquatic ecosystem focus on phytoplankton biomass shifts and don’t give attention to
alterations in functional groups. Although tropical zooplankton are characterized for a
absence of large zooplankton taxa that could be able to control phytoplankton biomass
(Lazzaro, 1987; Fernando, 1994; Jeppesen et al., 2007) there are studies showing that
some groups of copepods can efficiently graze on large phytoplankton groups, even
filamentous and colonials cyanobacteria (Panosso et al., 2003). As commented above,
fish presence had a positive effect on phytoplankton biomass, although juvenile and
larvae fish has similar impact on plankton biomass, mechanisms behind these effects are
distinct. Larvae fish excretion experiments showed high values of N excretion rates and
the highest values of P excretion rates, characteristic of zooplanktivory diet, as predicted
by stoichiometry theory (Sterner & Elser, 2002). So, juvenile and larvae fish showed
different feeding strategy during our experiment.
36
Plankton community composition was affected by treatments. Although we did not
found interactive effect between treatments on zooplankton density or community
structure, fish presence was responsible for the major impact on zooplankton
community structure. Filter-feeder omnivores (juvenile fish) and zooplanktivores
(larvae fish) had similar effects on zooplankton community. Apparently both fish size
predate on large zooplankton (cladoceran and copepod) and create a scenario in favor of
small size zooplankton (rotifer, copepodite and nauplii). As commented before this kind
of impact could generate implications for whole ecosystem, since in tropical shallow
lakes are often dominated by inedible phytoplankton, which are supposed to not be
grazed by small body zooplankton, as rotifer (Fernando, 1994; Lazzaro, 1987; Jeppesen
et al., 2007).
Treatments interactively affect phytoplankton community composition. Particular
response of phytoplankton communities to light and fish suggest that even abroad
taxonomic groups, phytoplankton taxa are differently adapted to environmental
conditions (Reynolds et al., 1993). Phytoplankton ability to adapted to differential
resource and grazers regimes are diverse and include morphological, chemical and
behavior attributes, these attributes could be responsible for some community-level
responses (Lichman & Klausmeier, 2008). Half of our treatments present singular
phytoplankton community composition. In high light-juvenile fish phytoplankton
community was dominated by cyanobacteria, low light-juvenile fish treatment showed
chlorophytes dominance, and in high light-larvae fish phytoplankton community
composition showed a codominance scenario between chlorophytes and diatoms. Other
treatments showed a diatoms dominance. Probably fish nutrient excretion rates were
determinant for phytoplankton community structure, since our mesocosms did not have
any input of nutrient, fish nutrient excretion assume the main role as nutrient source.
We also found evidences that seston stoichiometric is strongly related with
phytoplankton composition (Dickman et al., 2006; Hall et al., 2007; Striebel et al.,
2008). Seston C:P was significantly correlated with proportional biovolume of two of
trhee major taxonomic groups. We found a positive relation between % cyanobacteria
and seston C:P and a negative correlation for % diatoms. No relation was seen between
% chlorophytes and seston C:P. These regression are a good indicative of phytoplankton
nutritional quality and functional role on the food webs (Klausmeier, et al., 2004; Mette
et al., 2011).
37
Our study shows that alterations in resource stoichiometry can create a different
scenario in aquatic ecosystem, which is dependent of predominant planktivory type.
Since light and nutrients supply are affected by different global environmental
perturbations, i.e. eutrophication increases nutrient and reduce light availability in
aquatic ecosystems (Schindler, 2006), our result assume a relevant importance for
studies of restoration and management of aquatic ecosystems. Moreover our results
highlight the importance of both, top-down and bottom-up controls in regulation of
tropical aquatic ecosystems.
38
Capítulo III
Biomanipulation of lakes and reservoir should target the removal of
benthivorous instead of planktivorous fish
1
1
1
Danyhelton D. F. Dantas , Caroline G. B. Moura, Pablo L. Rubim , Leonardo Teixeira , Mariana C.
1
1
1
Amaral , Fabiana Araújo , José L. Attayde .
1
Departamento de Ecologia, Universidade Federal do Rio Grande do Norte.
39
Abstract
The removal of benthivorous and planktivorous fish have been extensively used as a
management tool to improve the water quality of temperate lakes and reservoirs.
However, the extent to which such biomanipulation can be equally successful in tropical
systems remains a controversial issue. This study aimed to evaluate the effects of a
benthivorous (Prochilodus brevis) and a planktivorous (Oreochromis niloticus) fish on
the water quality of a tropical eutrophic man-made lake. Because both fish species can
bioturbate lake sediment, we also investigated whether their effects on water quality are
mediated by their interactions with the sediment. Two consecutive experiments with a
2x2 factorial design were carried out in 20 mesocosms (6 m3), where fish
presence/absence were manipulated in combination with the presence/absence of a fish
cage (4 m3) preventing fish access to the sediment. Nutrients (N and P) and chlorophyll
a concentrations as well as water transparency were measured in all treatments at the
beginning. middle and end of the experiments. The benthivorous fish increased total
phosphorus and chlorophyll a concentration and decreased water transparency only
when they had access to the sediment. However, no differences were found in the
excretion rates of benthivorous fish with and without access to the sediment, suggesting
that their effects were caused by bioturbation of the sediment and not by nutrient
translocation through bottom feeding and excretion in the water column. On the other
hand, the planktivorous fish increased phytoplankton biomass without changing the
concentrations of nutrients and the water transparency. Moreover, their positive effect
on phytoplankton biomass was independent of their access to the sediment, suggesting
that they increased phytoplankton biomass through a trophic cascading effect. We
conclude that biomanipulation of eutrophic lakes in the tropics should target the
removal of benthivorous fish, because they increase the internal load of phosphorus to
the water column stimulating phytoplankton growth in tropical as in temperate lakes.
Removing planktivorous fish may also reduce phytoplankton biomass and improve
water quality, but this would depend on the strength of the trophic cascading effects,
which should be lower in tropical than in temperate lakes.
Keywords: Habitat coupling, bioturbation, nutrient transport, lake management, lake
restoration.
40
Introduction
Fish play a key role in the resilience of the turbid state of eutrophic shallow lakes
because they can control the abundance of zooplankton herbivores, thus increasing
phytoplankton biomass (Scheffer, 1998). Moreover, they can resuspend sediments in
search for benthic food, increasing turbidity (Zambrano et al., 2001; Scheffer et al.,
2003), and also translocate nutrients from benthic to pelagic habitats, enhancing
phytoplankton growth (Vanni, 2002). Therefore, a strong reduction of planktivorous
and/or benthivorous fish biomass is often needed to bring the lake back to a clear water
state after reduction of external nutrient loading (Scheffer, 1998). The effects of such
biomanipulation have been extensively investigated in temperate lakes and have been
reviewed by many authors in the last two decades (e.g. Hansson et al., 1998; Mehner et
al., 2002; Cooke et al., 2005; Søndergaard et al., 2008; Jeppesen et al., 2012).
On the other hand, very few studies have investigated the applicability of
biomanipulation as a tool for water quality management of tropical and subtropical
lakes (Jeppesen et al., 2012). It has been suggested that (sub) tropical lakes may not
respond to planktivorous fish manipulation as trophic cascade theory predicts because
zooplankton grazing pressure on phytoplankton should be weak in these systems
(Jeppesen et al., 2007). In such warm lakes, zooplankton is often dominated by smallsized grazers (Lacerot, 2010; Iglesias et al., 2011) while phytoplankton is often
dominated by large colonial or filamentous cyanobacteria (Kosten et al., 2012), which
cannot be efficiently grazed by such small-sized herbivores (Carpenter & Kitchell,
1993).
However, aggregation and colony formation may decrease cyanobacteria vulnerability
to zooplankton grazing, but simultaneously increases their vulnerability to other grazers,
like filter-feeding planktivorous fish (Northcott et al., 1991, Turker et al., 2003 a,b).
Thus, attempts have been made to use filter-feeding fish such as silver carp and Nile
tilapia to reduce phytoplankton biomass and thus improve water quality in some (sub)
tropical lakes (Lazzaro & Starlin, 2005; Zhang et al., 2008). However, reports on their
effects on phytoplankton biomass and water transparency have been contradictory and a
mathematical model of planktivory by filter-feeding fish predicts a unimodal response
of phytoplankton biomass to increasing filter-feeding fish biomass (Attayde et al.,
41
2010). Based on such prediction, any reduction in planktivorous fish biomass may
either increase or decrease phytoplankton biomass, depending on the initial fish biomass
and the relative strength of the direct and indirect effects of filter-feeding fish on
phytoplankton (Attayde et al., 2010).
On the other hand, the effects of benthivorous fish on the water quality of tropical
shallow lakes should be similar to those observed in temperate lakes. Benthivorous fish
enhance phytoplankton via nutrient cycling resulting from two functionally distinct
processes: i) nutrient release by excretion and egestion and ii) bioturbation of the
sediment during their foraging activities. Benthivorous fish feeds on benthic resources,
and release nutrients into the water column, translocating nutrients from benthic to
pelagic habitats and transforming them from particulate to dissolved forms (Vanni,
2002). Nutrient translocation by benthivorous fish is different from nutrient recycling
by planktivorous fish, which release nutrients within the same pelagic habitat in which
food is ingested. Thus, nutrient translocation by benthivorous fish brings “new”
nutrients to the euphotic zone, increasing the total mass of nutrients and stimulating
“new primary production” in the pelagic habitat (Vanni, 2002). In contrast, nutrient
recycling by planktivorous fish cannot increase the mass of nutrients in the pelagic
habitat, but rather it sustains “recycled production” (Vanni, 2002).
Some fish also have the ability to influence nutrient cycling and primary production
through bioturbation of the sediment, defined as all transport processes carried out by
animals that directly or indirectly affect sediment matrices (Kristensen et al., 2012).
This process could happen due to feeding, resuspension and burrowing activities (e.g.
nest building). Through bioturbation these organisms can increase turbidity (Croel and
Kneitel, 2011) and nutrient concentration (Schaus and Vanni, 2000; Adamek and
Marsalek, 2013) in the water column.
42
In this study we examined the effects of a benthivorous (Prochilodus brevis) and a
planktivorous (Oreochromis niloticus) fish on the water quality of a tropical eutrophic
man-made lake. Because both fish species can bioturbate lake sediment, we also
investigated whether their effects on water quality are mediated by their interactions
with the sediment. P. brevis is a continuous bioturber, feeding on the sediment surface,
while O. niloticus is an occasional bioturber, digging site-specific holes during nest
building activities. Both species are common and economically important in the inland
water fisheries of the semi-arid region of Brazil.
We conducted two experiments in mesocosm scale with a 2x2 factorial design,
manipulating presence of omnivorous fish (Fish/No Fish) and its access to sediment
(Access/No Access), to test the hypothesis that benthivorous fish has stronger negative
effects on the water quality of tropical lakes and reservoirs due to their nutrient
translocation from the sediment to the water column.
Methods
Experimental design
Two consecutive enclosure experiments were carried out in a eutrophic man-made
shallow lake located inside the Ecological Station of Seridó, a conservation unit of the
Caatinga Biome in the state of Rio Grande do Norte, Brazil (6º34’49,3” S; 37º15´20”
W). The first experiment was conducted with the native benthivorous fish Prochilodus
brevis between
20th June 2013 and 26th July 2013. The second experiment was
conducted with the exotic planktivorous fish
Oreochromis niloticus between 10th
February 2014 and 11th March 2014. The experiments had a 2 x 2 factorial design,
where
fish
presence/absence
were
manipulated
in
combination
with
the
presence/absence of a fish cage (4 m3) preventing fish access to the sediment. The four
treatments were randomly allocated into 20 mesocosms of 6 m³ (4 m² area x 1.5m
depth) placed side by side in the littoral zone of the lake. All mesocosms were fixed at
the lake bottom and were isolated from the surrounding lake water by a transparent
plastic film, but were open to the atmosphere and to the sediment inside the mesocosms.
43
To prevent fish access to the sediment inside the mesocosms, fish were placed inside a 4
m3 cage (4 m2 area x 1 m depth) with 2 cm mesh size. Although the cage limited fish
interaction with the sediment, it allowed all other chemical and biological interactions
inside the mesocosms. In both experiments fish were caught in the lake and added just
after the initial water samples were taken. In the benthivorous fish experiment, four
individuals (335,9 ± 35,9 g mean weight) were added while in the planktivorous fish
experiment, three individuals (482,5 ± 66,7g mean weight) were added to each
mesocosm of the fish treatments.
Sampling and analyses
Water samples were taken from each mesocosm just before fish additions and after 15
and 30 days from the beginning of the experiments. Oxygen concentration and water
temperature were measured in situ with a Instrutherm MO - 900 probe. Water
transparency was measured with a Secchi disc. Water samples were collected at
different points of each mesocosm with a PVC tube (1.5 m) and integrated into a single
representative sample of each mesocosm, from which subsamples were taken to
quantify chlorophyll a [Chl a], total phosphorous [TP] and total dissolved nitrogen
[TDN]. The same procedure was done at two different points of the lake, to monitor any
variation in the lake that could be misinterpreted as a treatment effect.
Chlorophyll a was determined in spectrophotometer after water filtration onto a 1.2 µm
glass fiber filter (VWR 696) and pigment extraction with ethanol (Jespersen &
Christoffersen, 1988). Total phosphorus (TP) concentration was measured by the acid
ascorbic method after persulfate digestion (Valderrama, 1981). Filtered water (1.2 µm
glass fiber filter - VWR 696) were used to determinate soluble reactive phosphorous
(SRP) according to Murphy & Riley (1962), while total dissolved nitrogen (TDN) was
analyzed using a carbon analyzer TOC-V Shimadzu.
A one-way ANOVA was used to test for any differences in the initial conditions
between the treatments. A two-way ANOVA was used to test for the effects of fish and
their access to the sediment as well as the interaction between these two factors on the
measured variables after 15 and 30 days from the beginning of the experiment. When
necessary, data were log transformed to homogenize variance. A paired t-test analysis
was used to test for differences between initial and final fish weight at the beggining
44
and end of the experiments. For all analyses p values were considered significant if <
0.05.
Results
In both experiments omnivorous fish presence increased phytoplankton biomass, but the
mechanisms responsible for this increment were different for benthivorous and
planktivorous fish. Although both fish species are potentially bioturbers, only the effect
of the benthivorous P. brevis was dependent on its access to sediment.
In agreement with our hypothesis, the benthivorous fish increased total phosphorus and
chlorophyll a concentrations and decreased Secchi depth , but only when they had
access to the sediment (Figure 1). On the other hand, the planktivorous fish had no
effects on nutrient concentrations in the water column, but still increased chlorophyll a
concentrations with no effects on Secchi depth. However, the significant effect of
planktivorous fish on chlorophyll a concentration was not dependent of their interaction
with the sediment as no significant interaction between planktivorous fish and access
effects was observed.
45
Figure 1: Results of the two-way ANOVA for total phosphorous (I, II), total nitrogen (III, IV), Chl a (V,
VI) and Secchi disk deep (VII, VIII). Graphs on left side of figure (odd numbers) are for P. brevis
experiment, while graphs on right side of the figure (even numbers) are for O. niloticus. Significant
values (p<0.05) are in bold. Bars represent standard deviation.
46
P. brevis weight significantly decreased in both fish treatments (Figure. 2). In both
cases, the difference between initial and final weights were near 15%. On the other
hand, tilapia did not lose or gain weight during the experiment in both treatments
(Figure 2).
Figure 2: Wet weight of P. brevis (left) and O. niloticus (right) at the beginning and end of the
experiments in the fish treatments with and without access to the sediment. Results of the t-tests are given
on the top of the bars being compared. Significant p values (< 0.05) are in bold. Bars represent standard
deviation.
Discussion
The most important result of this paper was to show that omnivorous fish can affect
plankton community via different ways and that interaction with sediment can influence
this effect. In both experiments fish presence increased phytoplankton biomass, but
mechanisms responsible for this increase were apparently different for each fish species,
and access to sediment was determinant only for benthic-feeding omnivorous.
It is common to associate positive effects of fish on phytoplankton biomass to a topdown cascading effects and nutrient excretion (Terborgh & Estes, 2010). However, fish
bioturbation processes can also represent a meaningful force in this process. Although
initially this idea may sound a bit counterintuitive, as bioturbation process decrease
water transparency and reduce the availability of light for photosynthesis (Hellstrom,
1991). This and many other studies shows results that support this positive effect of
bioturbers on phytoplankton biomass (Meijer et al., 1990; Breukelaar et al., 1994;
Nalewajko & Murphy, 1998; Zambrano & Hinojosa, 1999; Roozen et al., 2007;
Adamek & Marsalek, 2013).
47
In recent years some studies have associated bioturbers role as ecosystem engineers,
highlighting their abilities to modify ecosystem features (Meysman et al., 2006).
However, impacts of a potential bioturber fish in aquatic ecosystems could be variable,
and one of the features that determine this impact is the way that a species interacts with
the sediment (Adamek & Marsalek, 2013). Although our results have shown a similar
pattern, an increase in phytoplankton biomass, in both experiments, it happens in
different conditions for each one: for P. brevis, (benthic-feeding) phytoplankton
increase in a condition in which fish had access to sediment. So, fish was able to feed on
sediment promoting sediment resuspension and nutrient translocation from benthic to
pelagic habitat. This increase in nutrient availability for phytoplankton in the water
column (Fig.1 I and III) was probably the cause of high values of Chl a (Fig. 1 V).
Others studies support the idea that bioturbers fish can significantly contribute to a
increase in nutrient concentration and turbidity at the water column (Schaus & Vanni,
2000; Adamek & Marsalek, 2013). Sometimes this source of nutrients was about double
that of external loading (Braband et al., 1990). Shostell and Bukaveckas (2004)
conducted a study in which they quantified the proportion of phytoplankton nutrient
demand sustained by gizzard shad, (the same bioturber omnivorous fish used for Schaus
& Vanni (2000), they found that nutrient excretion by gizzard shad supplied 14-20% of
P uptake and 31-58% of N uptake by plankton. This example highlight the importance
the nutrient cycling by a bioturber in a aquatic ecosystem.
Besides nutrient translocation, bioturbers organisms can affect biomass and community
structure of phytoplankton due to mechanical resuspension of settled algal cells (Misson
at al., 2011). This could represent other positive impact of bioturbers on phytoplankton
biomass, since sedimentation of viable phytoplankton cells appears as one of the most
significant process whereby biomass reduces (Reynolds & Wiseman, 1982; Reynolds et
al., 1982). In a recent work Roozen et al. (2007) used a combination of field and
laboratory approaches to show that benthivorous fish, through bioturbation activity, are
able to resuspend settled algal cells and enhance phytoplankton biomass and community
composition.
Different from the latter case in which fish access to sediment was determinant for
positive effects on phytoplankton biomass, the experiment with the filter-feeding, O.
niloticus, showed an increase in phytoplankton biomass that was associated with fish
presence, but independent of fish access condition. Although, there are some studies
48
showing variable effects for omnivorous filter-feeding fish on phytoplankton biomass
(Diana et al., 1991; Elhigzi et al., 1995; Starling et al., 1998; Figueredo & Giani, 2005;
Attayde & Menezes, 2008; Okun et al., 2008; Rondel et al., 2008; Menezes et al., 2010),
our results shows evidence of a classic trophic cascade mediated by this omnivorous
fish, which by filtering activity probably reduced zooplankton density and released
phytoplankton from grazing pressure.
This positive effect of O. niloticos on phytoplankton biomass is reported in other studies
(Starling et al., 2002; Menezes et al., 2010). Unlike P. brevis experiment, O. niloticus
was not responsible for increase nutrient concentration or decrease water transparency
in the water column, even in the control treatment, both effects indicators of
bioturbation process (Croel and Kneitel, 2011; Adamek & Marsalek, 2013). This lack in
bioturbation evidence could be explained by the fact that omnivorous filter-feeders as
O. niloticus just feed on benthic habitat in specific conditions and the main interaction
with sediment occurs for nest build activity (Joyni et al., 2011). Possibly, the ways that
fish species interact with the sediment was a determinant to explain mechanisms
responsible for an increase in phytoplankton biomass. Data of zooplankton and
phytoplankton community composition are still in analysis phase and will be important
to clarify mechanisms behind this positive effect of omnivorous filter-feeding on
plankton community.
We compared fish weight at the beginning and at the end of the experiment and expect
that both fish species' enhanced weight in the control treatment due to the presence of
more food options in this treatment. However P. brevis, that showed strong evidences of
interaction with sediment, lose weight (≈15% of initial weight) in both control and no
access treatment. We could attribute this reduction as a mesocosm effect, since in
control treatment fish was able to feed on sediment. O. niloticus showed a stability of
weight in both control and no access treatments, probably due to their filter-feeding
strategy that permits fish good conditions for feeding in both treatments, regardless of
access condition.
Contrary to the idea that top-down interactions are weaker in tropical than temperate
lakes (Moss et al., 2004; Stephen et al., 2004; Jeppesen et al., 2007), our results
highlight the importance of top-down interaction in tropical aquatic ecosystems. The
idea behind this hypothesis is that zooplankton in tropical lakes are often dominated by
49
small-bodied species with low grazing pressure (Fernando, 1994; Lazzaro, 1987;
Jeppesen et al., 2007), thereby removal of planktivorous fish was not expected to result
in a decrease in phytoplankton biomass as in temperate lakes. Furthermore tropical
aquatic ecosystems shows a high numbers of herbivorous/omnivorous species
(Gonzáles-Bergonzoni et al., 2012). However, as showing by our results the indirect
effect of omnivorous fish in these ecosystems cannot be neglected and trophic
manipulation can be a useful tool in tropical shallow lakes management and restoration
process and this process should focus on benthivorous species as P. brevis not
omnivorous filter-feeding as O. niloticus. Another relevant point that reinforce the
removal of benthivorous species, as a biomanipulation strategy in tropical shallow lakes
is the fact that these individuals act as a sink for benthic habitat nutrients but as a source
for pelagic habitat. Strategies that focus on removal of these fish takes nutrients from
the ecosystem and may reduce nutrient flux from the benthos to water by reducing fishmediated bioturbation and/or excretion of benthic-derived nutrients. This kind of
strategy was done in Florida lakes (Catalano et al., 2010; Schaus et al., 2010).
Reduction in bioturbers fish activity in warme lakes can represent a significant decrease
in nutrient flux from benthic to pelagic habitat. Benthic habitat often have a lower
oxygen concentration, but activity of bioturbers agents can increase oxygen penetration
into the sediment (Brönmark & Hansson, 2005), promoting a increase in mineralisation
process by which nutrients are released to the pelagic habitat (Fukuhara
& Sakamoto, 1987; Hansen et al., 1998). In a model proposed by Vanni et al. (2013)
suggest that the sink strength of fish depends greatly on the fate of carcass P, both
percentage of P mineralized and the fractions of this P taken up by benthic vs. pelagic
producers. According with them low mineralization rates and a high proportion of
benthic uptake both increase the chance that fish will be sinks for pelagic P. Possibly
removal of strong biotubers as P. brevis in tropical shallow lakes can create a scenario
in favor of fish become a nutrient sink at pelagic habitat. Unfortunately, there is little
quantitative information available on effects of bioturbers fish on mineralization rates of
fish carcasses. Because bones and scales contain a high amount of P (Hendrixson et al.,
2007) understand the fate of this P is important.
50
Since bioturbers fish potentially can act as ecosystem engineers changing quality,
quantity and distribution of resources used by others species (Kristensen et al., 2012),
studies that try to identify impacts of these fishes in ecosystem scale are important.
Experimental designs (i.e. mesocosms) are useful for this kind of study since they
permit a better approximation to real conditions in a lake and are "simpler" than whole
lake experiments. Although our results showed similar impacts on phytoplankton
biomass for both filter-feeding and benthic-feeding fishes, mechanisms that were
responsible for it are different. This kind of information is important for management
strategy in aquatic ecosystems. Understanding the mechanisms used by a species (i.e.
bioturbation and trophic cascades) will aid our development of more efficient strategies
to control and regulate algae proliferation in aquatic ecosystems.
51
Supplementary information
S 1 - Mean values of phosphorous total (PT, µg/L) and nitrogen total concentration (NT, mg/L), phytoplankton biomass (Chl a, µg/L) and secchi
deep (m) and number replicate of each treatment (N). SD=standard deviation.
Curimatã
Tilapia
Access
Response variable
PT
NT
CHL a
Secchi
No Access
Access
No Access
Mean
SD
N
Mean
SD
N
Mean
SD
N
Mean
SD
N
Fish
133,70
23,55
5
57,70
9,82
5
163,80
13,05
5
128,80
15,68
5
No Fish
48,30
6,64
5
45,20
8,02
5
178,00
28,86
5
145,80
17,95
5
Fish
3,71
0,38
5
3,22
0,07
5
2,12
0,10
5
2,03
0,43
5
No Fish
3,18
0,22
5
3,36
0,49
5
1,93
0,15
5
1,95
0,08
5
Fish
43,68
12,42
5
10,13
5,19
5
25,81
8,23
5
25,98
11,41
5
No Fish
19,13
12,91
5
17,63
10,64
5
12,66
3,36
5
13,10
2,76
5
Fish
0,51
0,10
5
0,98
0,02
5
0,19
0,04
5
0,49
0,20
5
No Fish
1,36
0,08
5
0,97
0,23
5
0,19
0,02
5
0,35
0,11
5
52
S 2 - Results of the two-way ANOVA. Significant values (p<0,05) are bold; "*" mark log transformed variables, Secchi was transformed in both
experiments while NT only in tilapia.
Response variable
PT
NT*
CHL a
Secchi*
Curimatã
Tilápia
Df
Sum-of-squares
Meansquare
F
p-value
Df
Sum-of-squares
Meansquare
F
p-value
Interaction
1
6643
6643
35
< 0,0001
1
9,8
9,80
0,02
0,8765
Access
1
7821
7821
41,21
< 0,0001
1
5645
5645
14,37
Fish
1
11981
11981
63,12
< 0,0001
3,10
0,0016
0,0975
Residual
16
3037
189,80
Interaction
1
0,55
0,55
5,12
Access
1
0,13
0,13
1,18
0,0379
0,2942
Fish
1
0,20
0,20
1,82
0,1961
Residual
16
1,72
0,11
Interaction
1
1284
1284
11,14
Access
1
1535
1535
13,32
Fish
1
363,4
363,40
3,154
Residual
16
1844
115,20
Interaction
1
0,25
0,25
50,45
Access
1
0,02
0,02
4,27
< 0,0001
0,0554
Fish
1
0,21
0,21
42,44
< 0,0001
Residual
16
0,08
0,00
1
1217
1217
16
6284
392,80
1
0,001
0,001
0,538
0,4739
1
0,001
0,001
0,251
0,6236
1,313
0,2687
1
0,003
0,003
16
0,040
0,002
0,0042
1
0,09
0,09
0,00
0,9673
0,0022
0,0948
1
0,46
0,46
0,01
0,9275
15,63
0,0011
1
847,30
847,30
16
867,30
54,21
1
0,02
0,02
1,13
0,3038
1
0,48
0,48
24,66
1
0,02
0,02
0,92
0,0001
0,3530
16
0,31
0,02
53
Discussão Geral
Estudos focados no entendimento dos ecossistemas são fascinantes, e em parte, isso se
deve ao alto grau de complexidade desses sistemas. De forma geral, um ecossistema é
composto de várias espécies que interagem através das mais variadas formas possíveis
entre si e com o ambiente. Além do que, estes sistemas muitas vezes se apresentam
conectados entre si, o que aumenta ainda mais o grau de complexidade. Surge então a
questão sobre qual seria a melhor forma de se estudar um ecossistema. Nos últimos anos
duas abordagens distintas cresceram dentro da ecologia e hoje originaram duas frentes
de pesquisas distintas, a ecologia de comunidade e a ecologia de ecossistemas. Ambas
com potencial para responderem perguntas relevantes para o melhor entendimento do
ecossistema.
Vista de forma simplista a ecologia de comunidades tem como ponto central a
importância dos organismos, suas interações intra e interespecíficas, e a influência da
estrutura da comunidade sobre o ecossistema. Geralmente responde a questões tais
quais: como as interações entre as espécies limitam o número de espécies que podem
coexistir em uma área? Quais padrões surgem a partir dessas interações? Já a ecologia
de ecossistemas tem como foco uma abordagem mais abrangente, como entender os
processos ecossistêmicos, incluindo produção primaria, sequestro de carbono e ciclos de
nutrientes, ou mesmo entender a estequiometria ecológica dentro do ecossistema. E
responde a questões do tipo: como é o fluxo de energia em diferentes ecossistemas?
Como os nutrientes limitantes são reciclados, garantindo a manutenção dos elementos
necessários para o crescimento dos produtores? Quais fatores e processos estão
envolvidos no fluxo energético e de matéria, tanto em escala local como global?
Entretanto, ambas as abordagens estão intimamente relacionadas, mas nosso
entendimento sobre essa conectividade ainda hoje é limitado. Nos últimos anos essa
relação tem se tornado cada vez mais evidente. São várias as formas de abordagem que
buscam essa interação como, por exemplo, a ligação entre ciclagem de nutrientes e teias
tróficas, a conexão entre espécies e ecossistemas, ecologia estequiométrica através de
diferentes níveis de organização ecológica ou mesmo a teoria metabólica na ecologia.
Esses e outros pensamentos forma postos em prática durante a concepção desta tese.
54
Na concepção atual da ciência é de suma importância que os estudos passem a ter um
caráter mais de síntese e não apenas o papel de “gerar informação”. Nos últimos anos
muito tem sido produzido a cerca das mais variadas hipótese e teorias propostas. O que
falta são estudos que sintetizem esses resultados e os organizem em um conjunto
coerente de hipóteses alternativas ou complementares que produzam predições que
possam ser testadas e levem o conhecimento atual para um nível acima. Foi com esse
pensamento que essa tese foi concebida. Embora a um primeiro momento os trabalhos
que a compõem não parecem estar relacionados, todos eles têm esse foco e através das
estratégias propostas cada um deles respondeu a questões relevantes para o
entendimento dos ecossistemas aquáticos.
Para isso, dois dos três capítulos aqui presentes utilizaram uma abordagem
experimental, a qual tem se mostrado como uma das melhores opções para se elucidar
os mecanismos responsáveis pelos padrões e processos observados na natureza.
Experimentos, como os aqui realizados, podem ser conduzidos em diversas escalas,
desde microcosmo até experimentos que envolvam ecossistemas inteiros (Carpenter et
al., 1995; Carpenter, 1996; Pace, 2001). Neste sentido, a escala escolhida para o
desenvolvimento de um experimento terá relação com o grau de realismo e o poder de
explicação. Apesar dos experimentos realizados em escala de ecossistemas inteiros (i.e
um lago) terem a vantagem de serem bastante realistas (Carpenter et al., 1995; Pace et
al., 2004), eles têm uma série de limitações como um reduzido controle experimental e
baixa replicação (Hurlbert, 1984; Drenner & Mazumder, 1999). Assim, devido a essas
limitações e a dificuldades logísticas, muitos pesquisadores usam mesocosmos,
estruturas desenhadas para, em menor escala, reproduzir os sistemas naturais (Odum,
1984; Drenner & Mazumder, 1999).
Os experimentos em escala de mesocosmo tiveram e têm tido um papel importante na
construção do nosso entendimento sobre a ecologia de comunidade e o funcionamento
dos ecossistemas (Fraser & Keddy, 1997; Jessup et al., 2004; Spivak et al., 2009), além
de contribuírem para diversas abordagens teóricas (Pfisterer & Schmid, 2002; Cardinale
et al., 2006), e inclusive na obtenção de conhecimento sobre processos globais (Benton
et al., 2007; Duffy, 2009). Entretanto, como mencionado anteriormente, é necessário
uma abordagem que vá além, e que assuma uma caráter de síntese sobre esses
resultados.
55
Por exemplo, é fato que as comunidades biológicas são reguladas por meio de
interações ascendentes (bottom-up; i.e. disponibilidade nutrientes ou luz) e interações
descendentes (top-down; i.e. predação). Foi hipotetizado que, nos habitats pelágicos dos
lagos, a importância relativa dessas interações sobre o plâncton pode variar com a
latitude, apontando uma diminuição na importância das interações descendentes em
latitudes mais baixas (Moss et al., 2004; Stephen et al., 2004; Jeppesen et al., 2007). Um
dos argumentos que embasa esse pensamento é que em ambientes mais quentes (e.g.
trópicos) o crescimento do fitoplâncton seria beneficiado pelo maior período favorável
ao crescimento deste, e uma vez que, o fitoplâncton tem um crescimento mais acelerado
que o zooplâncton, o fitoplâncton tenderia a ser mais controlado por nutrientes (controle
ascendente) do que pela pressão de herbivoria do zooplâncton (controle descendente)
(Moss et al., 2004). Além disso, a ideia que, em lagos tropicais, a comunidade de
zooplancton é dominada por espécies de pequeno porte, as quais apresentam um baixo
potencial de predar e controlar o fitoplâncton (Fernando, 1994; Jeppesen et al., 2007)
reforça o pensamento exposto.
Entretanto, este pensamento deve ser repensado. Trabalhos recentes mostram que ao
contrário da ideia difundida, em ecossistemas aquáticos tropicais, a influência dos
peixes sobre a comunidade planctônica, e a dinâmica de nutrientes é significativamente
mais forte que aquela associada aos controles ascendentes (Attayde & Menezes, 2008;
Menezes et al., 2010). Estes trabalhos, assim como alguns dos resultados obtidos nesta
tese, sugerem que estratégias como a biomanipulação de peixes onívoros (como P.
brevis e O. niloticus) nesses ambientes pode sim ter uma papel crucial no processo de
recuperação e manejo de ambientes aquáticos tropicais.
Essa mudança na linha de pensamento se deve, em parte, aos efeitos indiretos dos
peixes sobre a regulação e a estruturação da cadeia trófica nesses ambientes. Por
exemplo, nos ecossistemas aquáticos, os animais podem desempenhar um papel
fundamental na ciclagem de nutrientes (Vanni et al., 2002). Especificamente, o papel
dos peixes parece ser particularmente variável entre os ecossistemas (Vanni 2002,
Mehner et al., 2005, Sarnelle and Knapp, 2005). Uma vez que nos ambientes tropicais é
forte a presença de peixes herbívoros/onívoros (Gonzalés-Bergonzoni et al., 2012),
muitos dos quais adotam estratégias alimentares como a detritivoria ou a planctivoria
(principalmente filtradores), capazes de se reproduzir ao longo de todo o ano e que não
são controlados pela disponibilidade de zooplâncton ou mesmo pela predação de
56
espécies piscívoras (Fernando 1994; Jeppesen et al., 2007). Fica a questão de qual seria
o impacto desses indivíduos nos ecossistemas aquáticos tropicais, e se haveria uma
diferença no papel que esses grupos no processo de estruturação e regulagem do
ecossistema. Algumas evidências sugerem que os peixes detritívoros teriam um papel
mais relevante do que os planctívoros no processo de ciclagem de nutrientes (Brabrand
et al., 1990; Schaus et al., 1997; Zimmer et al., 2006; Vanni et al., 2006). Alguns dos
resultados dessa tese, além de mostrar a relevância da força dos controles ascendentes
nos lagos tropicais rasos, corroboram com essa ideia da importância dos peixes
bentívoros nesses ambientes.
Tanto na descrição de padrões no primeiro capítulo como nos experimentos em escala
de mesocosmo (segundo e terceiro capítulo) os resultados obtidos reforçam a ideia de
que as interações ascendentes desempenham um papel fundamental nos ecossistemas
aquáticos tropicais, influenciando na estruturação das comunidades planctônicas. Os
resultados obtidos através da modelagem do banco de dados com informação de mais de
7.000 espécies deixa claro a importância dos peixes onívoros sobre padrões ecológicos
em escala global nos diversos ecossistemas aquáticos. Nesse trabalho os peixes com
nível trófico inferior a 2.8 foram responsáveis pelo enfraquecimento na relação entre
tamanho do corpo e posição trófica em ambientes tropicais de água doce, mostrando que
nesses ambientes a maior presença de espécies onívoras pode ser devido a uma
limitação energética causada pelas altas temperaturas. Esse resultado é importante frente
ao quadro de aquecimento global previsto para os tempos futuros, pois mostra uma
maior "fragilidade" na estrutura das teias alimentares nos ambientes aquáticos de água
doce quando comparados com os ecossistemas marinhos.
Nos dois capítulos com abordagem experimental encontramos evidências que reforçam
que o controle e a manipulação da comunidade de peixes nos lagos e reservatórios
tropicais pode ser fundamental no processo de manejo e restauração desses ambientes.
No terceiro capítulo fica claro que peixes bioturbadores têm o potencial de agir como
engenheiros ecossistêmicos alterando a quantidade, qualidade e distribuição dos
recursos utilizados por outras espécies (Kristensen et al., 2012). O controle da biomassa
de peixes como P. brevis em lagos rasos tropicais pode e deve ser usado em conjunto
com outras estratégias, como a redução das fontes difusas de nutrientes, como medida
de melhoria da qualidade da água nesses ambientes.
57
Já no segundo capítulo a qualidade do recurso se mostra importante sobre o efeito dos
dois tipos de planctivoria presente nos ecossistemas aquáticos tropicais. Uma vez que
mudanças na composição estequiométrica do recurso podem alterar a estrutura e a
composição desses ecossistemas. Estes resultados são de importante relevância para a
restauração e o manejo desses ambientes, pois sintetizam ideias e conceitos já bem
definidos dentro da ecologia e permitem um olhar mais refinado sobre as relações
tróficas nesses sistemas.
Por fim reforço que, contrariamente ao exposto na literatura, interações descendentes
podem ser responsáveis por regular, de maneira significativa, ecossistemas aquáticos
tropicais. Entretanto esse ainda é um campo carente de estudos que pode e deve ser
explorado nos próximos anos.
58
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