PROGRAMA DE PÓS-GRADUAÇÃO EM BIOLOGIA ANIMAL
FABRÍCIO BARRETO TERESA
Diversidade funcional de comunidades de peixes de riachos
Tese apresentada para obtenção do título de Doutor em Biologia Animal junto ao Programa de Pós-Graduação em Biologia Animal do Instituto de Biociências, Letras e Ciências Exatas da Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de São José do Rio Preto.
Orientador: Profª. Drª. Lilian Casatti
São José do Rio Preto - SP
Teresa, Fabrício Barreto.
Diversidade funcional de comunidades de peixes de riachos / Fabrício Barreto Teresa. - São José do Rio Preto : [s.n.], 2012.
101 f. : il. ; 30 cm.
Orientador: Lilian Casatti
Tese (doutorado) – Universidade Estadual Paulista, Instituto de
Biociências, Letras e Ciências Exatas
1. Ecologia animal. 2. Ictiofauna. 3. Peixe de riacho. 4. Peixe – Estrutura
de comunidades. 5. Diversidade biológica. I. Casatti, Lilian. II. Universidade Estadual Paulista, Instituto de Biociências, Letras e Ciências Exatas. III. Título.
CDU – 591.5
Este trabalho foi realizado no Laboratório de Ictiologia, do Departamento de
Zoologia e Botânica do Instituto de Biociências, Letras e Ciências Exatas, UNESP de
São José do Rio Preto, com auxílio financeiro da FAPESP na forma de bolsa de
doutorado
Diversidade funcional de comunidades de peixes de riachos
Tese apresentada para obtenção do título de Doutor em Biologia Animal junto ao Programa de Pós-Graduação em Biologia Animal do Instituto de Biociências, Letras e Ciências Exatas da Universidade
Estadual Paulista “Júlio de Mesquita Filho”, Campus de São
José do Rio Preto.
Banca Examinadora
Profª. Drª. Lilian Casatti
UNESP
–
São José do Rio Preto
Orientadora
Prof. Dr. Maurício Cetra
Universidade Federal de São Carlos (UFSCar)
Prof. Dr. Marcus Vinícius Cianciaruso
Universidade Federal de Goiás (UFG)
Profª. Drª. Katharina Eichbaum Esteves
Instituto de Pesca
Profª. Drª. Denise de Cerqueira e Rossa Feres
UNESP
–
São José do Rio Preto
A defesa de uma tese marca o término de um ciclo que começou muito tempo antes do ingresso na pós-graduação. Por isso, sou grato a todas as pessoas que contribuíram de alguma forma para a minha formação pessoal e profissional.
A minha orientadora, Profa. Dra. Lilian Casatti pela confiança, amizade e por tudo que me ensinou. Durante minha carreira espero um dia conseguir chegar ao menos próximo da sua dedicação, seriedade, dinamismo e competência.
A Profa. Dra. Eliane Gonçalves-de-Freitas, que além de acompanhar o
desenvolvimento do meu projeto de doutorado, orientou-me durante a graduação e o mestrado, ensinando-me a prática científica e despertando-me para o gosto pelo ensino.
A Profa Dra Maria Stela M.C. Noll e ao Dr. Mateus F. Ferrareze pelas críticas e sugestões proferidas durante a qualificação.
A todos os professores da graduação e pós-graduação, em especial a Profa Dra Denise de Cerqueira e Rossa Feres eao ProfDr. Francisco Langeani pela amizade, incentivo e ensinamentos ao longo de toda a minha vida acadêmica.
Ao Prof Dr. Marcus Vinícius Cianciaruso por gentilmente ter me recebido em seu
laboratório na UFG e pela solicitude no ensino de metodologias de análise de diversidade funcional.
Aos novos e antigos amigos do laboratório de Ictiologia André, Breno, Diego, Flávio,
Jaquelini, Mariela, Márcio, Paulo, Mateus, Lucas, em especial Ângelo, Camilo,
Cristiane, Gustavo, Fernanda, Fernando, Mônica, Renato e Roselene pela amizade, momentos agradáveis que compartilhamos e pela ajuda em diferentes etapas da tese.
A André L.S. Navarro, Angélica Amaya, Angelo R. Manzoti, Bruno Luiz R. Silva,
Galego pela ajuda nos trabalhos de campo.
Ao Bruno Luiz Rodrigues da Silva, amigo de longa data pela inestimável ajuda nas diferentes etapas deste trabalho, desde as viagens de reconhecimento até a última coleta, sempre disposto e bem-humorado. Também sou grato a sua família pela amizade e por acolher-me em sua casa no período final do doutorado
Ao Renato de Mei Romero, especialista em proporcionar apoio moral, pela amizade, companheirismo e pela ajuda em diversas etapas da tese, assim como em outros trabalhos.
Aos funcionários do IBILCE pela convivência e amizade nos últimos 12 anos, em especial Silvia E. Kazama, Vitor B. Thomazine e Rosemar R. C. Brena da seção de Pós-Graduação pela solicitude e paciência com os pedidos fora de prazo.
A Jane Dilvana Lima, pela amizade, incentivo, paciência e disponibilidade no
atendimento das minhas frequentes solicitações para revisão dos capítulos dessa tese; ao Dr. Robert Vadas-Jr e Dr. Fábio Cop Ferreira pela avaliação crítica do capítulo I; ao Diogo B. Provete e Thiago Gonçalves de Souza pela leitura crítica do capítulo III.
A todos os amigos futebolistas do IBILCE pelos agradáveis momentos compartilhados
nas “peladas” semanais que contribuíram para manter minha salubridade mental e
física.
A toda minha família em especial aos meus pais Maria Luiza Ribeiro Barreto e José
Teresa pelo amor, carinho e valores que alicerçam minha vida. Às minhas irmãs
Amanda e Débora, sobrinhas Anelise e Heloisa e cunhado Alexandre pelo carinho e companheirismo, tornando adoráveis os momentos que passamos juntos.
"O verdadeiro mestre é aquele que
acredita que a sua palavra sempre fará
diferença"
Neste estudo avaliaram-se os efeitos do desmatamento das zonas ripárias sobre a composição e diversidade funcional de comunidades de peixes de riachos. Para isso, foram elaborados três capítulos a partir de amostragens da ictiofauna em 126 segmentos de cinco metros de extensão em seis riachos, sendo três florestados e três desmatados, localizados na bacia do rio São José dos Dourados, sistema do Alto rio Paraná, Noroeste do Estado de São Paulo, Brasil. No CAPÍTULO I duas características que descrevem a distribuição longitudinal das espécies, a preferência por fluxo e por profundidade, foram avaliadas. As espécies apresentaram diferentes padrões de preferência, mas as respostas ao fluxo foram mais consistentes entre riachos florestados e desmatados do que em relação à profundidade. No CAPÍTULO II os padrões de diversidade taxonômica e funcional foram comparados entre os riachos florestados e desmatados, considerando a heterogeneidade estrutural em uma escala de meso-hábitat e no CAPÍTULO III foi avaliado se as alterações provocadas pelo desmatamento representam filtros ambientais que modulam a composição funcional das comunidades. Os padrões de diversidade e composição funcional diferiram em função das alterações ambientais nos riachos associadas ao desmatamento. As características funcionais associadas com o uso de hábitat, ecologia trófica, tolerância à hipóxia e tamanho influenciaram a distribuição das espécies dentro e entre riachos. Os resultados sugerem que as mudanças na disponibilidade de hábitat e recursos alimentares, assim como nas condições físico-químicas representam filtros ambientais importantes na organização das comunidades. Ao relacionar o desmatamento com alterações em outros componentes da diversidade que não somente taxonômico, os resultados obtidos possibilitam uma avaliação mais completa sobre os impactos biológicos desse tipo de alteração.
The effects of riparian deforestation on the functional composition and diversity of stream fish communities were evaluated. This study was divided into three chapters whose data were obtained by sampling fish fauna in 126 five meters long mesohabitats in forested (n = 3) and deforested (n = 3) streams, located in the São José dos Dourados river Basin, upper Paraná river system, northwestern São Paulo State, Brazil. In CHAPTER I two traits that describe the longitudinal distribution of the species, the preference for velocity and depth were evaluated. The species showed different patterns of preference, but their responses were more consistent between forested and deforested streams for velocity than for depth. In CHAPTER II the patterns of taxonomic and functional diversity were compared between forested and deforested streams in a mesohabitat scale and in CHAPTER III it was evaluated if the environmental modifications caused by deforestation represent environmental filters that modulate the functional composition of communities. Patterns of functional diversity and composition differed according to the environmental changes in streams related to deforestation. The distribution of species within and between streams was influenced by traits such as habitat use, trophic ecology, tolerance to hypoxia and size. The results suggest that changes in the habitat and food availability and physicochemical conditions represent environmental filters acting in the organization of communities. By linking deforestation to changes in other components of diversity rather than only taxonomic, the results obtained here provide a more complete knowledge about the biological impacts of the loss of riparian forest.
INTRODUÇÃO GERAL... 14
CAPÍTULO ... 18
Abstract... 19
Introduction... 20
Methods... 22
Study area... 22
Fish sampling and environmental descriptors ... 22
Development of habitat suitability criteria and test for transferability….………… 23
Results... 24
Discussion... 27
References... 31
CAPÍTULO 2... 35
Abstract... 36
Introduction... 37
Material and Methods... 39
Study area and general sampling design……….. 39
Data sampling... 40
Trait and trait categories... 42
Functional diversity metrics... 44
Data analysis... 45
Results... 45
Discussion... 48
References... 52
Supporting information... 59
CAPÍTULO 3... 64
Resumo... 65
Introdução... 66
Material e Métodos... 68
Área de estudo... 68
Amostragem da ictiofauna... 69
Resultados... 75
Discussion... 81
Referências Bibliográficas... 85
Apêndice... 90
DISCUSSÃO GERAL... 93
CONCLUSÕES... 96
INTRODUÇÃO GERAL .
A conservação de ecossistemas aquáticos de água doce é um desafio limitado pela falta de conhecimento sobre a sua estrutura e funcionamento, bem como sobre as formas pelas quais esses sistemas são afetados pelas interferências antrópicas (BARLETTA et al., 2010). Dentre as atividades humanas que exercem impactos negativos sobre os rios e riachos destacam os represamentos, substituição de vegetação nativa por culturas agrícolas ou pecuária, introdução de espécies exóticas e poluição (ALLAN; FLECKER, 1993). A supressão da vegetação nativa dentro das bacias de drenagem e, especialmente nas margens dos rios (zonas ripárias), são uma das alterações cujos efeitos ainda não são completamente compreendidos, principalmente em ecossistemas tropicais (BOJSEN; BARRIGA, 2002; LORION; KENNEDY, 2009).
No Brasil, a importância do desmatamento como fonte de impactos aos rios e riachos varia regionalmente (BARLETTA et al., 2010). Em regiões populosas e industrializadas esse tipo de alteração é uma das principais ameaças. Um exemplo marcante é a região Noroeste do Estado de São Paulo, uma das mais desmatadas do país, apresentando apenas 4% de vegetação nativa remanescente (SMA/IF, 2005). A perda da vegetação nativa atinge 75% das zonas ripárias dos rios e riachos desta região (SILVA et al., 2007) que por sua vez apresentam baixa integridade física e biológica (CASATTI et al., 2006, 2009a).
nos barrancos (PUSEY; ARTHINGTON, 2003, GROWNS et al., 2003, ROCHA et al., 2009), que por sua vez constituem micro-hábitats favoráveis para a ocorrência de algumas espécies oportunistas (ROCHA et al., 2009).
Os efeitos do desmatamento das zonas ripárias sobre os organismos e populações traduzem-se também em nível de comunidade e são representadas por mudanças na composição de espécies e nos padrões de diversidade (e.g., Pusey & Arthington, 2003; CASATTI et al., 2009b). Bojsen; Barriga (2002) evidenciaram substituição de espécies e aumento da abundância de peixes em riachos submetidos a desmatamento das suas zonas ripárias na Amazônia equatoriana. Além desses efeitos, Lorion; Kennedy (2009) observaram também maior riqueza de espécies em riachos desprovidos de matas ripárias na Costa Rica, resultados corroborados por Teresa; Casatti (2010) no sudeste do Brasil.
Além dos impactos sobre os padrões de composição e diversidade dentro de uma perspectiva taxonômica, existem evidências de que o declínio e/ou favorecimento das espécies em riachos submetidos ao desmatamento não é aleatório e dependem de algumas características dos organismos que influenciam o seu desempenho nesses ecossistemas (características funcionais). Por exemplo, Casatti et al. (2009b) compararam a fauna de peixes entre riachos mais afetados pela Interferências antrópica, com ausência de vegetação ripária arbórea e riachos submetidos a menor pressão antrópica, com zona ripária arborizada. Esses dois grupos de riachos abrigaram comunidades muito distintas, com as espécies tolerantes e generalistas dominando os riachos do primeiro grupo e as espécies reofílicas sendo mais associadas ao segundo grupo (CASATTI et al., 2009b). De forma congruente, Teresa; Casatti (2010) evidenciaram que o aumento da riqueza de espécies nos riachos desmatados é representado pelo aumento no número de espécies tolerantes à degradação física do hábitat.
(DIAZ; CABIDO, 2001). A importância de se considerar esse componente da biodiversidade é reforçada por estudos que têm revelado que a diversidade funcional tem maior poder preditivo sobre os processos ecossistêmicos do que a diversidade taxonômica (TILMAN et al., 1997; DIAZ; CABIDO, 2001; MOUILLOT et al., 2011). A explicação para isso reside no fato de que a abordagem taxonômica assume que as espécies são diferentes sem a ponderação sobre a equivalência ou complementaridade do papel que elas desempenham no ambiente (DIAZ; CABIDO, 2001). Nesse contexto, a avaliação dos padrões de diversidade funcional das comunidades em ambientes submetidos às interferências antrópicas pode contribuir também para a predição de mudanças em processos ecológicos. No caso dos riachos submetidos ao desmatamento, os padrões de diversidade funcional poderiam indicar o grau de modificação de processos (e.g., produtividade, sedimentação, dinâmica trófica) que são conhecidamente influenciados por esse tipo de alteração (MURPHY; HALL, 1981; SWEENEY et al., 2004).
Alguns estudos têm utilizados métricas de diversidade funcional dentro de uma perspectiva aplicada com o intuito de verificar os efeitos biológicos das interferências antrópicas (e.g., ERNST et al., 2006; EROS et al., 2009; FLYNN et al., 2009; VILLÉGER et al., 2010; BARRAGÁN et al., 2011). Por exemplo, Ernst et al. (2006) observaram redução da diversidade funcional de comunidades de anuros em fragmentos florestais degradados por desmatamento, embora não tenham diagnosticado mudanças na diversidade taxonômica. Nesse caso, a alteração ambiental resultou na substituição de espécies funcionalmente distintas por espécies redundantes. Dentro dessa abordagem aplicada, é evidente que a incorporação de métricas de diversidade funcional fornece subsídios para uma avaliação mais completa sobre os impactos das alterações humanas sobre a biodiversidade. Com relação aos riachos, embora os efeitos das alterações antrópicas sobre a estrutura e composição taxonômica das comunidades sejam relativamente bem compreendidos (BOJSEN; BARRIGA, 2002; PUSEY; ARTHINGTON, 2003; LORION; KENNEDY, 2009), o mesmo não acontece com relação à perspectiva funcional.
de que tais Efeitos são dependentes das características funcionais exibidas pelas espécies (CASATTI et al., 2009b; TERESA; CASATTI, 2010), hipotetizamos que as modificações ambientais causadas pelo desmatamento nos riachos refletem em mudanças na composição e diversidade funcional das comunidades. Para o cumprimento do objetivo geral, este estudo foi dividido em três capítulos que correspondem a manuscritos, cujos dados foram obtidos a partir das amostragens da ictiofauna em seis riachos, sendo três florestados e três desmatados, localizados na bacia do rio São José dos Dourados, sistema do Alto rio Paraná, Noroeste do Estado de São Paulo, Brasil.
Manuscrito submetido para Ecohydrology
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CAPÍTULO I
-Development of habitat suitability criteria for some Neotropical stream
fishes and an assessment of their transferability to streams with
ABSTRACT
We assessed the preference of 10 fish species for depth and velocity conditions in forested streams from southeastern Brazil using habitat suitability criteria (HSC curves). We also tested whether preference patterns observed in forested streams can be transferred to deforested streams. We used data from fish sampled in 62 five-meter quadrats in three forested streams to construct preference curves. Astyanax altiparanae,
A. fasciatus, Knodus moenkhausii, and Piabina argentea showed a preference for deep slow habitats, whereas Aspidoras fuscoguttatus, Characidium zebra, Cetopsorhamdia
iheringi, Pseudopimelodus pulcher, and Hypostomus nigromaculatus showed an
opposite pattern: preference for shallow fast habitats. Hypostomus ancistroides showed a multimodal pattern of preference for depth and velocity. To evaluate whether patterns observed in forested streams may be transferred to deforested streams, we sampled 64 five-meters quadrats in three deforested streams using the same methodology. The preference for velocity was more consistent than for depth, as success in the transferability criterion was 86% and 29% of species, respectively. This indicates that velocity is a good predictor of species abundance in streams, regardless of their condition.
INTRODUCTION
The recognition that species are distributed non-randomly in habitats, preferentially occupying suitable sites for feeding, reproduction, and survival (Grinnell, 1917; Hutchinson, 1957), constitutes the basis for developing predictive models of species distribution along environmental gradients (e.g., Ahmadi-Nedushan et al., 2006). This approach has a broad application for natural resources management, as since it allows prediction of changes in biological communities from changes in environmental conditions caused by human activities. However, the predictive power of these models depends on knowledge of the response of species in relation to the gradient of environmental conditions. This information can be obtained by developing habitat suitability criteria (HSC; Bovee, 1982, 1986), a component for conducting physical habitat simulation (PHABSIM), a tool used to assess the consequences of changes in river flows on habitat availability (Bovee, 1982).
The lack of knowledge about traits exhibited by species has limited the use of the functional approach in studies focusing in diversity patterns. In this way, the definition of HSC also may be useful, since the preference of the species for habitat features may be used as traits in functional diversity studies. The HSC can be assessed by curves defining the degree of preference by a given species in relation to habitat variables alone, such as depth, velocity, substrate and cover. Efforts to develop HSC for multiple species have increased, owing to the degradation of water resources and growing concern over biodiversity loss (e.g., Lamouroux et al., 1999; Vadas & Orth, 2001; Strakosh et al., 2003). However, this approach has not been applied in Neotropical environments, limiting the use of predictive models and the ability to quantitatively predict the biological impacts from changes in hydraulic variables of aquatic environments. This is especially alarming because changes in the natural flow regime are among the major anthropogenic threats for fish conservation in Neotropical lotic environments (Barletta et al., 2010).
Several factors, such as environmental heterogeneity, food availability, predation, competition, and habitat availability influence the patterns of species occupancy in riverine patches (Power, 1984; Thomas & Bovee, 1993; Jackson et al., 2001; Leal et al., 2011). The differential effects of these factors may limit the applicability of HSC between different environments (Groshens & Orth, 1993; Freeman
for each type of stream are recommended (Bovee, 1986), which brings high costs and operational difficulties. However, other studies have found consistency in preference patterns across streams (Thomas & Bovee, 1993; Strakosh et al., 2003). This highlights the importance of testing HSC validity to the site of interest (transferability) before developing new criteria.
METHODS
Study area
All streams studied (second and third order) are located in the drainage of the São José dos Dourados, Upper Paraná River basin, northwestern region of the state of São Paulo, Brazil (Figure 1). The climate of the region is influenced by equatorial and tropical masses, resulting in a tropical climate with dry and rainy periods, with higher rainfall and higher temperatures from December to February and lower rainfall and milder temperatures between June and August (IPT, 1999). The forested streams are located in forest fragments, representing what is best preserved in the region, whereas the deforested streams are located away from forest fragments where the riparian zone is dominated by pasture.
Figure 1. Location of the study sites in the São José dos Dourados basin, São Paulo State, Brazil (A and B). Forested sites (dark circles) are located within the greatest forest fragments and deforested (gray circles) streams lack arboreal vegetation in their riparian zone and are located in areas dominated by pasture.
Fish sampling and environmental descriptors
reducing variation within each quadrat. The fish samplings were carried out during the dry season (September to November 2009 and April to July 2010) using electrofishing preceded by the up- and downstream isolation of each quadrat. The electrofishing sampling consisted of successive passes along the segment. The sample ended when no new individual was captured after one passage.
After the fish sampling, we characterized the segments in relation to depth and velocity. To accomplish this, we divided each quadrat into four equidistant, transverse transects, where were done measurements at five equidistant points from one margin to another. We used a mechanical flowmeter model 2030 (General Oceanics®) to measure water velocity at ~ 0.6 of total depth. Data from transects were lumped together to obtain the average values for the whole quadrat.
Development of habitat suitability criteria and test for transferability
Only species that occurred in at least 10 samples in forested streams were included in the habitat suitability criteria for depth and velocity. We adopted this procedure because infrequent species may have been under-sampled, resulting in higher estimated errors of preference. We classified the depth gradient into five classes (D1 = Ø to 0.2 m; D2 = 0.21 to 0.30 m; D3 = 0.31 to 0.40 m; D4 = 0.41 to 0.50 m; D5 > 0.51 m) and velocity into four classes (V1 = 0-0.20 m/s; V2 = 0.21 to 0.40 m/s; V3 = 0.41-0.60 m/s; V4 > 0.61 m/s). The limits for the classes were defined to represent discrete units of the hydrological gradient while ensuring a comparable number of samples in each class. We built HSC curves (type III, sensu Bovee, 1986) from preference values that were calculated the abundance ratio of species in each class of depth and velocity, divided by the proportionate number of habitat in the class in relation to all habitats sampled (Freeman et al., 1997). With this procedure, we considered both the relative abundance of species in the habitats and habitat availability. Posteriorly, we standardized the preference values to vary from 0 to 1, thereby obtaining the suitability index (SI). For the class with the highest preference value, we assigned an index of 1 and proportionally smaller values to other classes.
greater than 0.7, according to the criteria developed for forested streams. We choose 0.7 as a reference value because it included most of the raw values of habitat preference higher than 1, i.e., whose relative abundance is higher than the proportional availability of habitats.
To test the transferability of HSC from forested to deforested streams, we considered only species that occurred in at least 10 quadrats in the deforested streams. We classified the quadrats according to the optimum/non-optimum threshold defined from the HSC curves from forested streams. For the criterion to be considered
transferable, the abundance of a species should be higher in “optimal” samples of
deforested streams, as defined for forested streams. Thus, we conducted a comparison of the mean species abundance between optimum and non-optimum quadrats using a one-tailed t-test.
RESULTS
We recorded 31 species in forested streams, of which 10 occurred in at least 10 samples (Table I). The evaluation of the HSC curves for these species for depth and velocity demonstrated three main patterns (Figure 2). Astyanax altiparanae, A. fasciatus, Knodus moenkhausii, and Piabina argentea had high SI values in slow-flowing and deep segments. Another four species showed an opposite pattern, with higher SI values associated with shallow and fast-flowing habitats. This was the case of
Characidium zebra, Cetopsorhamdia iheringi, Pseudopimelodus pulcher, and
Hypostomus nigromaculatus. Aspidoras fuscoguttatus and Hypostomus ancistroides
Table I. Frequency of occurrence and number of individuals (in parentheses) of species occurring in at least 10 segments in forested streams (R1 to R3).
Family Species Code R1 R2 R3
Characidae Astyanax altiparanae Astalt 15 (97) 9 (26) 8 (30)
Astyanax fasciatus Astfas 6 (20) 14 (36) 17 (192)
Knodus moenkhausii Knomoe 8 (17) 10 (30) 8 (13)
Piabina argentea Piaarg 13 (35) 11 (34) 12 (42)
Crenuchidae Characidium zebra Chazeb 16 (31) 20 (66) 19 (89) Callichthydae Aspidoras fuscoguttatus Aspfus 0 (0) 6 (11) 10 (23) Heptapteridae Cetopsorhamdia iheringi Cetihe 5 (8) 4 (9) 6 (25)
Pseudopimelodus pulcher Psepul 11 (42) 9 (38) 0 (0)
Loricariidae Hypostomus ancistroides Hypanc 6 (10) 10 (23) 16 (38)
Figure 2. Habitat suitability criteria for depth and velocity of 10 species (codes in Table I) in five classes of depth (D1 = Ø to 0.2 m; D2 = 0.21 to 0.30 m; D3 = 0.31 to 0.40 m; D4 = 0.41 to 0.50 m; D5 > 0.51 m) and in four classes of velocity (V1 = > 0.0 to 0.2 m/s; V2 = 0.21 to 0.40 m/s; V3 = 0.41 to 0.60 m/s; V4 > 0.61 m/s) in forested streams. The dotted lines indicate SI = 0.7, above which conditions were considered optimal.
optimal and non-optimal habitats in deforested streams (t test, P > 0.15; Table II). In relation to water velocity, all species had higher abundances in optimal habitats of deforested streams, except for Hypostomus ancistroides, according to the criteria established for forested streams (t test, P < 0.02; Table II).
Table II. Transferability test of HSC from forested to deforested streams. The + sign indicates that the HSC developed for forested streams was able to predict the abundance of a given species in deforested streams, and the - sign indicates the opposite.
Species
Abundance Depth Velocity
Astyanax altiparanae + +
Astyanax fasciatus - +
Piabina argentea - +
Characidium zebra - +
Aspidoras fuscoguttatus + +
Hypostomus ancistroides - -
Hypostomus nigromaculatus - +
DISCUSSION
In this study we established the preference of ten species of stream fishes for depth and velocity conditions. In general, species showed well-defined preference patterns for depth and velocity, reinforcing the importance of hydraulic variables as predictors of fish distribution in lotic environments (Lamouroux et al., 1999; Vadas & Orth, 2001; Schwartz & Herricks 2008; Leal et al., 2011). One of the patterns was the association of Astyanax altiparanae, A. fasciatus, Knodus moenkhausii, and Piabina argentea in deep, slow-flowing habitats. Indeed, the morphology of these species is compatible with this habitat preference, as their compressed bodies, well-developed caudal and pectoral fins, and lateral eyes represent morphological adaptations to live in lentic habitats (Gatz, 1979; Oliveira et al., 2010). Behavioral patterns displayed by these species also favor the occupation of lentic and deep habitats, as they are mid water swimmers that feed on drift items in the water column (Casatti & Castro, 1998; Casatti
requires less energy expenditure for movement and feeding (Casatti & Castro, 1998; Bürhnheim, 2002).
An opposite pattern was observed for Characidium zebra, Cetopsorhamdia
iheringi, Pseudopimelodus pulcher, and Hypostomus nigromaculatus that showed
preference for shallow and fast-flowing habitats. These fish have morphological and behavioral adaptations congruent with life in these conditions. For example, these species share depressed bodies and expanded pectoral fins (Casatti et al. 2005; Casatti & Castro, 2006), which allow short movements in fast-flowing environments (Watson & Balon, 1984). In addition, the diet composed of periphyton (H. nigromaculatus) and aquatic insects (remaining species) is consistent with the high availability of these items in shallow, fast-flowing environments (Angermeier & Karr, 1983).
The conditions considered non-optimal in this study (SI < 0.7) are not necessarily uninhabitable. Within this range, one could still discriminate between a range of habitable or marginal conditions and another as uninhabitable (Thomas & Bovee, 1993), which would represent the conditions in which a given species could not live. Most species that preferred shallow, fast-flowing habitats were less plastic, with a wider range of conditions that may be considered uninhabitable (SI values close to zero in two classes of depth and velocity), compared with species that preferred deep, slow-flowing habitats. The only exception to this pattern was Characidium zebra, whose non-optimal, but occupied conditions could be considered habitable, as the SI values were higher than 0.37. Species that preferred deep, slow-flowing habitats showed SI values close to zero in a maximum of one class of depth and velocity. This indicates that species that preferred shallow, fast-flowing habitats are more specialized and probably more sensitive to changes in hydraulic conditions. In fact, the loss of rheophilic species in streams from our study region has been attributed to changes in hydraulic conditions and simplification of habitats (Casatti et al., 2006; Casatti et al., 2009a; Teresa and Casatti, 2010). For example, Cetopsorhamdia iheringi and Pseudopimelodus pulcher
did not occur in the degraded streams studied by Casatti et al. (2009a), a fact that they attributed to the loss of riffles from siltation and habitat simplification.
The habitat suitability criteria obtained for Hypostomus ancistroides and
Aspidoras fuscoguttatus were distinct from other species with respect to depth.
artifact of small sample sizes. Because this species occurred in only two out of three forested streams, we did not consider the samples from the stream in which it was absent to calculate the habitat availability. Consequently, only five samples fell into the deepest depth class. Because the calculation of SI involves the relative abundance ratio of the proportional availability of habitat, the occurrence of a few individuals (seven) in two samples resulted in high SI values. One of the procedures that can be adopted in this case is either group together two adjacent classes to increase sample size or not take into account the SI value obtained (see Freeman et al., 1997). With the adoption of these procedures, the preference pattern of A. fuscoguttatus would be similar to species with a preference for shallow habitats, and therefore consistent with the pattern of habitat use reported for this species (Araújo and Garutti, 2003). Although the criterium developed here is consistent in deforested streams, this was due to the preference of this fish for shallowest depth class, as no individual was recorded in the deepest depth class. This strengthens our suggestion that the second peak of the HSC curve for this species has no biological basis. The habitat use criterion for velocity indicated a preference for fast-flowing habitats, but similar to Characidium zebra, other velocity conditions were considered habitable (SI values > 0.32). This is consistent with the plasticity of this species, which occurs in streams with different hydrological characteristics (Casatti et al., 2009a,b).
The multimodal pattern of the depth preference curve of Hypostomus ancistroides suggests that this factor has little influence in determining its abundance patterns. On the other hand, velocity seems to be a good predictor of its abundance in forested streams, via a more uniform relationship, indicating a preference for lentic habitats, as also found by Uieda et al. (1997) and Casatti et al. (2005). Interestingly, this pattern is uncommon for species of Hypostomus, which are usually associated with fast-flowing habitats, like H. nigromaculatus in this study.
streams and (iii) failure of the criterion to describe optimal habitats. The first explanation may, at least partially, justify the failure in transferring the criteria for depth, especially for species whose optimum condition was assigned to the last depth class (> 0.51 m) like Astyanax fasciatus. In deforested streams, only four segments (~ 6%), three of which in the same stream, fell into the deepest depth class. According to Bovee (1986), the successful transfer of HSC is dependent on the availability of conditions in the site to which one wants to transfer the criterion.
The second explanation (interaction with other factors) may also apply if environmental factors influenced fish differently in forested as deforested streams. For example, the high abundance of marginal submerged vegetation in deforested streams, as a result of the proliferation of exotic grasses, provide favorable microhabitats for some species (Casatti et al., 2009) and may influence their response to other variables. Such grasses can attenuate water flow along stream banks, providing slow-flowing microhabitats even in stretches with high velocities. As a result, species with preferences for slow-flowing habitats would be favored, notably Hypostomus ancistroides in my study. In fact, individuals of this species were observed in the vegetation on the banks of deforested streams, even in stretches with high water flow. On the other hand, this species was restricted to the mid-channel in forested streams, where submerged grasses are lacking and supposedly the influence of velocity is higher. This could explain the failure to transfer the criterion for flow to H. ancistroides.
The failure in transferring HSCs also may be related to the fact that they do not always describe a habitat preferred by species. For example, in this study, depth and velocity co-varied in both forested and deforested streams (Pearson’s product-moment
preference for fast-flowing habitats, like Hypostomus nigromaculatus and Characidium zebra.
The results indicated a high consistency in the response of species for velocity, suggesting that this variable is a good predictor of species abundance and that its HSC has great potential to be transferred to streams of different conservation status. The scale of this study is relevant, because the transferability of criteria is usually tested between streams (Thomas and Bovee, 1993) or between regional models built for individual streams (Lamouroux et al., 1999). The data presented in this study should represent part of an effort to develop criteria for Neotropic species, encompassing a broader spectrum of conditions, as well as other variables known to be important for fish, like substrate and cover (Vadas and Orth, 2001; Wright and Flecker, 2004; Leal et al., 2011).
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Casatti L, Castro RMC. 1998. A fish community of the São Francisco river headwater riffles, southeastern Brazil. Ichthyological Exploration of Freshwaters9: 229-242. Casatti L, Castro RMC. 2006. Testing the ecomorphological hypothesis in a headwater
riffles fish assemblage of the rio São Francisco, southeastern Brazil. Neotropical Ichthyology4: 203–214.
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(Pisces, Loricariidae) in southeastern brazilian streams. Biota Neotropica 5: 157–
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Manuscrito aceito para publicação na Ecology of Freshwater Fish
- CAPÍTULO II -
Influence of forest cover and mesohabitats types on functional and
taxonomic diversity of fish communities in Neotropical lowland
ABSTRACT
In this study, we investigated how taxonomic and functional diversity of fish communities is influenced by forest cover and mesohabitat types in Neotropical lowland streams. We sampled fish fauna of 126 five meter-long mesohabitats using an electrofishing unit in forested (n = 3) and deforested (n = 3) streams in the upper Paraná River basin of southeastern Brazil. According to velocity depth, three mesohabitat types have been considered: riffles (shallow and fast-flowing habitat), pools (deep and slow-flowing habitat) and run (intermediate depth and velocity). Seven functional traits and 27 trait categories related to ecological, behavioral and life history aspects of fish were considered. Our results indicate that forest cover and mesohabitat type influence differently functional patterns of communities. While deforestation affects communities primarily through changes in diversity (functional and taxonomic), mesohabitat types determine changes in the functional composition. The increased diversity in deforested mesohabitats is driven by a decrease of species turnover among habitat patches within streams. This can be attributed to new feeding opportunities and microhabitat availabilities in deforested streams and favors the occurrence species with a particular set of traits, indicating a strong habitat-trait relationship.
INTRODUCTION
Deforestation of the riparian zone is one of the most important threats to the conservation of freshwater fish species (Naiman & Décamps 1997; Sweeney et al. 2004). Deforestation primarily affects streams, whose physical and biological integrity depends on native forests in riparian zones (Pinto et al. 2006). Changes resulting from deforestation include modifications to aquatic communities and ecosystem services (Sweeney et al. 2004). The consequences of deforestation on fish communities have been primarily examined under a taxonomic perspective (Bojsen & Barriga 2002; Casatti et al. 2010). These studies have shown changes in species composition and indicators of species diversity such as the richness, diversity, and dominance of species (Bojsen & Barriga 2002; Wright & Flecker 2004; Teresa & Casatti 2010). However, these metrics represent a limited set of traits of biological communities because they do not take accont the relative functional differences between species and often fail to detect changes caused by anthropogenic interference (Rabeni & Smale 1995; Ernst et al. 2006).
Recently, there has been remarkable growth in the number of studies incorporating aspects of the functional diversity of communities (Petchey & Gaston 2002; Hoeinghaus et al. 2007; Poff et al. 2010). This approach takes into account both the functional traits of species and the ecological roles they play in the ecosystem, and it provides additional information otherwise not obtainable through a taxonomic approach (Eros et al. 2009). In addition, the functional structure of communities is considered a better predictor of ecosystem functioning than species diversity itself (Tilman et al. 1997; Mokany et al. 2008; Moulliot et al. 2011). The study of the anthropogenic impacts on the functional structure of communities is fundamental because it may predict not only communities patterns but also processes operating in ecosystems (Mayfield et al. 2010).
suggesting that deforestation limits or favors certain species according to their traits. For example, Rabeni & Smale (1995) demonstrated that species that rely on hard substrates for reproduction tend to disappear from environments subject to siltation.
In addition to functional composition, functional diversity is another way in which community structure can be described. Indices that have been developed recently deal with functional traits within a multivariate framework (e.g., Petchey & Gaston 2006; Villéger et al. 2008). This approach has also been useful in identifying functional changes along gradients of deforestation (Ernst et al. 2006; Barragán et al. 2011), and its use in streams is promising because little is known about how different components of biodiversity in these environments respond to human impacts.
Streams are heterogeneous systems composed of a mosaic of patches recognized at different scales (Frissel et al. 1986). At the mesohabitat scale, three physiognomies are easily recognized according to their geomorphological and hydrological features: riffles represent shallow, fast waters; pools are deep, slow waters that usually have fine substrate; runs are intermediate between riffles and pools. These mesohabitats influence the composition and structure of fish fauna (Bührnheim 2002; Langeani et al. 2005; Schwartz & Herricks 2008; Rezende et al. 2010), as well as some characteristics of fish species (e.g., diet, reproductive strategies and preference for substrate) (Berkman & Rabeni 1987; Casatti & Castro 1998; Goldstein & Meador 2004). For example, fish with less diversified diets predominate in riffles, while the increased variety of food items available in pools would support communities composed of more generalist species (Angermeier & Karr 1983; Berkman & Rabeni 1987). Thus, it is expected that different mesohabitats and their associated communities respond differently to environmental disturbances.
MATERIAL AND METHODS
Study area and general sampling design
Fig. 1. Map of the study area, showing São Paulo state (A), São José dos Dourados basin (B) and location of the forested (dark circles) and deforested (open circles) streams. Large forest fragments (>100ha) present in the basin are shown.
We sampled 126 five meters-long mesohabitats (with between 16 to 24 sites in each stream), 62 of which were in deforested streams and 64 in forested streams. The mesohabitat were chosen in order to represent the structural variation present in each stream. We sampled fish fauna and environmental descriptors in each mesohabitat from September to November 2009 and from April to July 2010.
Data sampling
São José do Rio Preto, Brazil (see Table A1, Supporting Information, for a species list of each stream).
We collected data on the physical structure of habitat after fish sampling. To do this, we sub-divided each mesohabitat into four transversal, equidistant transects where we recorded the following data: width, measured at the surface and at the middle of the water column; depth, measured at five equidistant points from one margin to another; velocity (with a mechanical flowmeter), measured at the middle of the water column; streambed substrate composition (i.e., the relative proportion of each substrate component) visually estimated according to Cummins (1962) and the volume occupied by the submerged vegetation (roots, leaves and stems from the submerged terrestrial vegetation) on the banks of each margin, based on the measures of the height and the width of vegetation on stream banks of each transect. We classified the streambed substrate as either stable, which allows colonization by benthic fauna (in the consolidated clay, gravel, pebble and rock) or unstable, with sand and unconsolidated clay. The values of each mesohabitat unit were calculated by the mean of the values obtained in the transects.
The mesohabitat units were classified according to their depth and velocity characteristics. These two variables were chosen because they represent important predictors of fish community structure in streams (Lamouroux et al. 1999; Bürhnheim 2002). Moreover, both forested and deforested streams had similar mesohabitats considering these two variables. After performing a hierarchical agglomerative cluster analysis with Euclidean distance by using UPGMA method, mesohabitats were classified in three types: (i) shallow, fast-flowing habitat; (ii) deep, slow-flowing habitat; (iii) intermediate conditions in relation to these two descriptors. These three groups of mesohabitats were named riffles, pools, and runs, respectively. We then pooled and averaged the structural descriptors data to represent the mesohabitats in each stream.
Traits and trait categories
We adopted a multidimensional approach to characterize fish species traits. We considered seven traits and 27 trait categories, including behavioral and ecological aspects (Table 1). We defined traits and their categories based on the species information recorded in literature and in this study. The species characterization followed a binary approach, with each species being associated to one trait category for each trait. We adopted this practice because there is little information on the variability of traits for many species. This approach was conservative, but it was sufficient for an analysis of the communities’ general patterns (Poff et al. 2006). The most common trait
categories expressed by each species were obtained from the literature, from data collected in this study and based on the author’s experience (Table A2 – Supporting
Table 1. Description of seven functional traits and 27 trait categories used to characterize fish species with their respective codes, including aspects of ecology and feeding behavior, habitat use, life history and tolerance.
Traits Trait categories
Ecology and feeding behavior
Diet1 Omnivore, periphytivore, insectivore, carnivore or detritivore
Feeding tactic,3 Water column feeding, substrate speculation, stealth predation, grazing, nocturnal predation or digging
Habitat use2,4
Velocity preference Slow, intermediate or fast Stable substrate preference High, moderate or low
Habitat use Surface, nektonic, nectobenthic, margins or benthic
Life history5
Size Small (< 50 mm), intermediate (50-150 mm) or large (> 150 mm)
Tolerance6
Tolerance to hypoxia Tolerant or intolerant 1 Diet analysis made by us
2 Underwater observations made by us
3 Keenleyside (1979), Sazima (1986), Sabino & Zuanon (1998)
4 Casatti & Castro (1998), Casatti et al. (2001), Casatti (2002) and personal observation 5 Biometry made by us
6 Kramer & Mehegan (1981), Araujo & Garutti (2003), Bozzetti & Schulz (2004) and Casatti et al. (2006)
assigning a trophic group to a species, we considered the most important items in their diet. Species with less than five individuals had their diet characterized based on data available in literature.
We evaluated the independence or redundancy of traits prior to the calculation of functional diversity metrics. This allowed the identification of non-informative and autocorrelated traits that should be removed from the analysis to avoid under or overestimation of functional diversity (Petchey & Gaston 2006). We performed a matrix correlation analysis (2Stage analysis) using the software PRIMER 6.0 (Clarke & Gorley 2006) from binary matrices for each trait (species as samples and trait categories as variables). The results of this analysis indicated that the seven traits had low autocorrelation (< 0.53), meaning that the previously selected traits represent different aspects of species. Thus, we considered all seven traits in additional analyses.
Functional diversity metrics
proposed by Villéger et al. (2008) more flexible, making possible the use of exclusively qualitative traits (Laliberté & Legendre 2010), as is the case in our study.
Data analysis
We used two-way ANOVA to investigate how the number of species within each trait category varied depending on forest cover and mesohabitats types in the R software (R Development Core Team 2011). Because part of the data did not fit assumptions of normality and/or homogeneity of variance, we used a more conservative significance
level (p ≤ 0.01) to minimize type I error. We evaluated the effects of forest cover and
mesohabitats on functional diversity metrics and species richness with the same analytical strategy. In order to evaluate the contribution of species exclusive to forested or deforested streams to the general patterns of diversity, we also conducted an analysis considering only the species shared between these groups of streams.In these cases, data had normal distribution and homogeneous variances; therefore, we used p ≤ 0.05 to
attribute significance. We considered different mesohabitats types and streams as independent samples. Prior to hypothesis testing, we pooled data by mesohabitat type within streams, producing a matrix with 18 samples corresponding to the three types of mesohabitats sampled in the six streams.
RESULTS
mesohabitats and forest cover was corroborated by MANOVA that revealed a significant main effect of both factors (p < 0.01).
Fig. 2. Ordination (PCA) of the three types of mesohabitats (triangles = riffles; circles = runs; squares = pools) in forested streams (dark symbols) and deforested (open symbols) according to the descriptors of physical habitat.
hand, some trait categories became more representative along the pool-riffle gradient, such as an insectivorous diet, benthic habitat, substrate speculation, high preference for stable substrates, and a preference for fast velocity (effect of mesohabitat: p < 0.01). A carnivorous diet was exclusive of fish from deforested streams and found with great
frequency in pools (interaction “forest cover” vs. “mesohabitats”; p < 0.01). Forest
cover or mesohabitats did not influence (p > 0.04) the following trait categories: periphytivorous diet, nektonic habitat, grazing, stealth predation, nocturnal predation, moderate preference for stable substrate, and preference for intermediate velocity.
The taxonomic richness and functional richness was higher in deforested than in forested mesohabitats (effect of forest cover: p = 0.01), but did not differ among mesohabitats (effect of mesohabitat: p = 0.34, Figure 3). Neither forest cover nor mesohabitat had an effect on functional evenness (p > 0.42, Figure 3). The functional dispersion was higher in deforested streams, but this effect was mesohabitat-dependent
(interaction “forest cover” vs. mesohabitats: p = 0.01), being significant only in riffles
Fig. 3. Taxonomic richness, functional richness, evenness and dispersion in forested (white bars) and deforested (gray bars) streams in relation to mesohabitats types. Data presented as mean ± standard deviation. * Indicates statistically significant difference between forested and deforested riffles and also among the remaining forested
mesohabitats (Tukey test, p ≤ 0.01).
DISCUSSION
diversity in amphibian communities from different deforestation regimes, but no effect on taxonomic richness along the gradient of degradation. By contrast, taxonomic richness increased as functional diversity decreased in estuarine fish communities of a degraded lake associated with the Gulf of Mexico (Villéger et al. 2010). These patterns are consistent with habitat loss and simplification in degraded ecosystems, which in turn result in the loss of species and functional traits (Flynn et al. 2009) or in the replacement of species with unique traits by functionally redundant species (Ernst et al. 2006; Villéger et al. 2010).
The increased diversity in deforested mesohabitats would be due to the addition of functionally distinct species in these streams. However, while species were added to the deforested streams, an equivalent number of species occurred exclusively in the forested streams, corroborating other studies and evidencing a pattern of species substitution along the gradient of deforestation (Bojsen & Barriga 2002; Casatti et al. 2009). When considering all of the species and excluding species absent in either deforested or forested streams, the congruence of the patterns of functional diversity suggest that the exclusive species influenced the functional diversity of both group of streams in a similar way. For example, while a carnivorous diet (Hoplias malabaricus
The functional evenness in both groups of streams was relatively high (> 0.6) regardless of mesohabitat, indicating that the functional space was evenly occupied. These results also suggest that the species added in deforested mesohabitats filled unoccupied niches, leading to a more even use of resources. In fact, when the number of species in a community increases, local assemblages can accommodate new species by increasing the volume of niche space (Barragán et al. 2011). The increase of the niche space in deforested streams may be represented by rare or formerly absent opportunities that become available, favoring the occurrence of opportunistic and/or invasive species (Lorion & Kennedy 2009). Some of the new opportunities in deforested streams can be represented by the greater availability of microhabitats (Casatti et al. 2009; Teresa & Casatti 2010) and food items, such as detritus (Rocha et al. 2009), algae and periphyton (Rounick et al. 1982; Bojsen & Barriga 2002; Lorion & Kennedy 2009), and this would favor, for example, the occurrence of omnivorous species. One the most prominent habitat alterations recorded was the greater abundance of marginal herbaceous vegetation in deforested streams (see Figure 2). This vegetation is composed mainly of exotic grasses (Brachiaria spp.) that tend to invade stream banks of deforested areas (Casatti et al. 2009) and may provide substrate for shelter and reproduction (Growns et al. 2003; Teresa & Romero, 2010). This would favor the occurrence of species usually associated with submerged vegetation, like Crenicichla britskii, Gymnotus carapo,
Hoplias malabaricus, and Hysonotus francirochai. The high abundance of marginal
submerged vegetation may have contributed to the higher richness of species with a preference for slow or intermediate velocities, as they can attenuate water velocity along stream banks and provide slow-flowing microhabitats even in areas with fast velocities. The vegetation can also trap detritus in their leaves and roots (Rocha et al. 2009), which are favored by detritivores (Casatti et al. 2009) like Corydoras aeneus,
Geophagus brasiliensis, Hypostomus ancistroides and Poecilia reticulata, all of which became more frequent in the deforested streams.
Some of the species favored by submerged marginal vegetation (e.g., G. carapo,
are more likely to autocorrelate with other trait categories. Hoplias malabaricus and
Synbranchus marmoratus can be cited as examples of carnivores that have been
associated with degraded environments (Casatti et al. 2006; Casatti et al. 2009, this study), but other traits (e.g., hypoxia tolerance or margin habitat) rather than the diet may be important in determining their association with deforested streams. Furthermore, the higher richness of carnivorous fish in pools can also be associated with the use of these sites as refuge during periods of inactivity (Power 1984).
Traits like tolerance to hypoxia, small body size and the use of surface may favor the colonization of shallow, warm, vegetated microhabitats and are shared by opportunistic species like Phalloceros harpagos, Serrapinnus notomelas and the exotic
Poecilia reticulata, which are dominant in the grass-dominated banks of degraded
streams (Casatti et al. 2009). The increased richness of fish tolerant to hypoxia in deforested streams is probably related to rising temperatures and reduced oxygen levels, conditions commonly found in silted deforested streams (Heartsill-Scalley & Aide 2003; Casatti et al. 2006). The higher number of species with a low preference for stable substrates reflects the physical alterations commonly reported for structurally degraded streams (Gregory et al. 1991; Walser & Bart 1999; Casatti et al. 2006) that experienced higher fine-sediment deposition, as shown in the PCA plot (see Figure 2).
streams, as forested riffles had a lower functional dispersion than deforested riffles and other mesohabitats. This result indicates that, on average, species are functionally more similar to each other on these sites. In fact, two groups of species predominated in forested riffles: benthic, grazers and periphytivorous fish (e.g., Hypostomus nigromaculatus) and benthic, speculators and insectivorous fish (e.g., Pseudopimelodus pulcher and Cetopsorhamdia iheringi). The fast water velocity and limited availability of food items in the riffles (Angermeier & Schlosser 1989) might represent more restrictive environmental filters, limiting the occurrence of a great diversity of traits and resulting in highly similar assemblages. The increased functional dispersion in deforested streams might indicate a relaxation of these filters. For example, the constraint imposed by the fast velocity of water would be minimized in these streams by an abundance of submerged marginal vegetation (Pusey & Arthington 2003).
In summary, our results indicate that forest cover and mesohabitat types influence different aspects related to the functional patterns of communities. While deforestation affects communities primarily through changes in diversity (both functional and taxonomic), mesohabitat types mainly determine changes in the functional composition. The increased diversity in deforested mesohabitats is driven by a decrease in species turnover among habitat patches within streams. The new opportunities available in deforested streams favor species with a particular set of traits (e.g., detritivores, species inhabiting stream margins, tolerant to hypoxia), indicating a strong habitat-trait relationship. Knowledge of how functional patterns and processes operate on aquatic communities over a wider range of degradation contexts, and whether the patterns observed herein are consistent with other scales, are promising topics for future research.
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