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INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA - INPA PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA FILTROS AMBIENTAIS, SIMILARIDADE LIMITANTE E DIVERSIDADE FUNCIONAL DE PEIXES GYMNOTIFORMES EM DOIS RIOS AMAZÔNICOS NAYANA ESTRELA FERREIRA MARQUES Manaus, Amazonas Agosto, 2016

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Page 1: FILTROS AMBIENTAIS, SIMILARIDADE LIMITANTE E DIVERSIDADE ... · a diversidade funcional surge como uma ferramenta que vai além dos conceitos tradicionais, ao analisar as diferentes

INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA - INPA

PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA

FILTROS AMBIENTAIS, SIMILARIDADE LIMITANTE E DIVERSIDADE FUNCIONAL

DE PEIXES GYMNOTIFORMES EM DOIS RIOS AMAZÔNICOS

NAYANA ESTRELA FERREIRA MARQUES

Manaus, Amazonas

Agosto, 2016

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NAYANA ESTRELA FERREIRA MARQUES

FILTROS AMBIENTAIS, SIMILARIDADE LIMITANTE E DIVERSIDADE FUNCIONAL

DE PEIXES GYMNOTIFORMES EM DOIS RIOS AMAZÔNICOS

ORIENTADOR: DR. JANSEN ALFREDO SAMPAIO ZUANON

COORIENTADOR: DR. RAFAEL PEREIRA LEITÃO

Dissertação apresentada ao Instituto Nacional

de Pesquisas da Amazônia, como parte dos

requisitos para obtenção do título de Mestre em

Biologia, área de concentração em Ecologia.

Manaus, Amazonas

Agosto, 2016

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iii

BANCA EXAMINADORA DA DEFESA ORAL PÚBLICA

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FICHA CATALOGRÁFICA

M357 Marques, Nayana Estrela Ferreira

Filtros ambientais, similaridade limitante e diversidade funcional de

peixes Gymnotiformes em dois rios Amazônicos / Nayana Estrela

Ferreira Marques. --- Manaus: [s.n.], 2016.

42f.: il.

Dissertação (Mestrado) --- INPA, Manaus, 2016.

Orientador: Jansen Alfredo Sampaio Zuanon

Coorientador: Rafael Pereira Leitão

Área de concentração: Ecologia

1. Gymnotiformes. 2. Diversidade funcional. 3. Ecologia. I.

Título.

CDD 597.5

Sinopse

Foi avaliada a importância relativa de filtros ambientais e similaridade limitante

como mecanismos estruturadores de assembleias de peixes da ordem

Gymnotiformes no ambiente de fundo de canal em um rio de água branca e um

rio de água clara da bacia Amazônica, com base em atributos funcionais das

espécies.

Palavras-chave: Ecologia funcional, estrutura de comunidades, regras de

montagem.

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v

Dedico este trabalho à minha filha Halina,

pelas boas surpresas, horas de Skype e

beijinhos babados, e aos meus pais, pelo apoio

incondicional.

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Agradecimentos

Gostaria de agradecer ao Instituto Nacional de Pesquisas da Amazônia (INPA) e ao

Programa de Pós-Graduação em Ecologia (PPG-ECO), pela infraestrutura e auxílio

administrativo, especialmente a Val que está sempre pronta a resolver qualquer problema.

Agradeço ainda, à Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)

pela bolsa de mestrado.

Agradeço muitíssimo aos meus orientadores Jansen Zuanon e Rafael Leitão, por

tornarem o mestrado uma experiência incrível. Além de serem pesquisadores excepcionais, se

tornaram verdadeiros amigos, sempre me auxiliando e confortando nos momentos difíceis.

Obrigada pela paciência, conversas fantásticas e conhecimento transmitido. Vocês foram

fundamentais para a minha formação.

À Dra. Lúcia Rapp e todos da coleção de ictiologia do INPA: Isabel, Madoka, Douglas,

Alany, Batatinha, Rafa, Renildo, Shizuka, Bife e Lindalva, não só pela acolhida durante a fase

de medidas morfométricas, mas por toda a ajuda no processo.

Aos meus colegas da turma de 2014: Alê, Clari, Juliano, Rafa, Lu, Dilson, Fábio (de

Roraima), Juanito, Renata, Emerson, Deco, Gabi (+ Alan), Pedro, Naty, Giu, Carol, Dudu,

Andrezinho e Dieguito pelas boas experiências compartilhadas, companhia e apoio durante

esses últimos anos.

Aos sarapólogos anônimos (Elisa, Valesca, Isac, Dalton, Andrezinho, Thiago e

Douglas), o melhor grupo de ajuda para viciados em peixes elétricos e sarapólogos

desesperados que já se teve notícia! Nossas reuniões foram extremamente importantes para

ampliar meu conhecimento sobre nossos tão amados e eletrizantes peixes.

À família BADPI (Galuch, Rosse, Talles, Sérgio, Maeda, Tiago, Cris, Naty, Akemi,

Paulinha e a queridíssima Cláudia de Deus), que me adotou durante boa parte do mestrado e

me fez repensar sobre as quintas-feiras!

À Giu e ao Felipe, meus amigos de qualquer hora, pelo ombro amigo e pela ajuda e

apoio em inúmeras ocasiões. À Elisa, pela descontração e concentração na medida certa. À

Claudinha pelos bons tempos de salinha. Ao Gilberto pelos conselhos e reflexões profundas.

Aos meus antigos e atuais companheiros de república Damaris, Danilo, Scott, Cameron,

Kauê e Tai pelos almoços de domingo, cookies da amizade/inspiração e sorvetes a qualquer

hora.

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Ao Scott pelo abstract, ao Douglas pelos mapas e ao Pedro Pequeno pela ajuda no R.

Por fim, gostaria de agradecer imensamente aos meus pais que sempre me apoiaram e

incentivaram, mesmo achando uma loucura vir para a Amazônia e a minha estrelinha que nunca

esqueceu a mamãe mesmo com a distância e todo o período de separação.

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“ O rio precisa se arriscar e entrar no oceano. E

somente quando ele entra no oceano é que o medo

desaparece”

Osho

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Resumo

A utilização de uma abordagem que combina atributos funcionais das espécies com

modelos nulos auxilia no entendimento dos padrões de distribuição e dos mecanismos que

potencialmente afetam a coocorrência de espécies. Tendo em vista que os processos ecológicos

ou “regras de montagem" envolvidos na formação das assembleias devem ser dependentes da

escala espacial, espera-se que tais mecanismos tenham diferentes efeitos em escalas locais ou

regionais. Compreender essa relação entre os processos ecológicos e as escalas espaciais nas

quais eles atuam é um desafio para os ecólogos. Nesse contexto, esse estudo avaliou a

importância relativa de filtros ambientais e similaridade limitante como mecanismos

estruturadores de assembleias de Gymnotiformes no canal de dois rios amazônicos com

diferentes características limnológicas e em diferentes escalas espaciais. Através de coletas com

arrastos bentônicos nos rios Madeira e Trombetas, obtivemos informações sobre a diversidade

taxonômica dessas assembleias, além de mensurar variáveis ambientais em cada rio

(temperatura, condutividade, profundidade, transparência, oxigênio dissolvido, turbidez e pH).

Em seguida, todas as espécies foram caracterizadas funcionalmente por meio de análise

ecomorfológica. Diferenças significativas na identidade funcional (i.e. Community weighted

mean; CWM) entre as assembleias do rio Madeira e do Trombetas indicam que fatores

ambientais provavelmente limitam a ocorrência de determinados atributos funcionais em escala

regional. Por outro lado, ao contrastar padrões de diversidade funcional observada em escala

local (i.e. dentro de cada uma das drenagens) com modelos nulos, nota-se que nenhum dos dois

mecanismos de montagem é claramente predominante, embora tenha-se observado certa

influência da similaridade limitante para as assembleias do rio Trombetas. Esses resultados

sugerem que filtros ambientais devem ser mais importantes na distribuição de espécies de

Gymnotiformes no canal de rios amazônicos, sobretudo em escalas espaciais maiores como em

escala regional. Entretanto, também reforçam a importância da relação de dependência entre os

processos ecológicos e a escala espacial. O presente estudo contribui para ampliar o

conhecimento sobre os padrões de diversidade funcional e as regras de montagem de

assembleias de peixes em um ambiente altamente desconhecido até então.

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Abstract

Environmental filtering, limiting similarity and functional diversity of Gymnotiformes

fishes in two Amazonian rivers

Using an approach that combines the species’ functional atributes with null models can help us

better understand the distribution patterns and mechanisms that potentially affect the co-

occurrence of species. If the ecological processes or "assembly rules" involved in the formation

of species assemblages are dependent on spatial scale, it is expected that such mechanisms have

different effects at local and regional scales. Understanding the relationship between ecological

processes and the spatial scale at which they act is a challenge for ecologists. In this context,

this study evaluated the relative importance of environmental filtering and limiting similarity

as structural mechanisms of assemblages of electric fishes (Gymnotiformes) in two Amazonian

river channels with different limnological characteristics and at different spatial scales. Through

benthic seine collections in the Madeira and Trombetas rivers, we obtained information on the

taxonomic diversity of these assemblages in addition to measuring environmental variables in

each river (temperature, conductivity, depth, transparency, dissolved oxygen, turbidity and pH).

All species were characterized functionally by ecomorphological analysis. Significant

differences in functional identity (i.e. Community weighted mean; CWM) between the

assemblages of the Madeira and Trombetas rivers indicate that environmental factors likely

limit the occurrence of certain functional attributes on a regional scale. Moreover, when

comparing observed patterns of functional diversity with null models at the local level (i.e.

within each drainage), we noted that none of the two mechanisms of assembly is clearly

predominant although there was some influence of similarity limiting on the assemblages of the

Trombetas River. These results suggest that environmental filters should be more important for

the distribution of Gymnotiformes species in Amazonian river channels at larger spatial scales,

especially at the regional scale. They also, however, stress the importance of the dependent

relationship between ecological processes and spatial scale. This study expands our knowledge

of functional diversity patterns and assembly rules for fish assemblages in a relatively unknown

system.

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Sumário

Lista de Figuras .................................................................................................................................... xii

Introdução geral .................................................................................................................................... 1

Objetivos ................................................................................................................................................ 5

Capítulo 1 - Environmental filtering, limiting similarity and functional diversity of

Gymnotiformes fishes in two Amazonian rivers ................................................................................ 6

Introduction ........................................................................................................................................... 8

Methods ................................................................................................................................................ 11

Study area.......................................................................................................................................... 11

Ichthyoogical material ...................................................................................................................... 12

Environmental data ........................................................................................................................... 12

Assemblage structure and diversity ................................................................................................... 12

Results .................................................................................................................................................. 15

General structure of Gymnotiforms assemblages in the Madeira and Trombetas Rivers ................ 15

Environmental characterization ........................................................................................................ 15

Functional structure of assemblages ................................................................................................. 15

Conclusions .......................................................................................................................................... 20

Acknowledgments ............................................................................................................................... 20

References ............................................................................................................................................ 21

Supporting information ...................................................................................................................... 33

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Lista de Figuras

Figure 1. Location of the study area and sampling sites (black triangles) in Madeira River. .............. 30

Figure 2. Location of the study area and sampling sites (black triangles) in Trombetas River. .......... 30

Figure 3. Non-Metric Multidimensional Scaling (NMDS) of Gymnotiformes assemblages of Madeira

(n = 15; triangules) and Trombetas (n = 12; circules) rivers based on species abundance (A) and

presence/absense (B) data. .................................................................................................................... 31

Figure 4. Tridimensional representation of the functional space occupied by the global species pool

(40 species) of Gymnotiformes in the Madeira and Trombetas rivers. Each plot represents two axes of

a Principal Coordinate Analysis (PC), where species are plotted according to their respective trait

values. Species ocurring in both regions are represented by “x” symbols. Species found exclusively in

Madeira or in Trombetas rivers are represented by empty or black circules respectively. Projections of

the convex hull volumes are illustrated by the polygons embedding the two sets of species. .............. 31

Figure 5. Community weighted means (CWM) of Gymnotiformes local assemblages of Madeira (n =

15) and Trombetas (n = 12) rivers, expressed by the average values of the first three axes of functional

space weighted by the abundance of species. Vertical lines represent 95% confidence intervals. ....... 32

Figure 6. Observed and expected relationships between species richness and functional richness

(FRic) of Gymnotiformes assemblies in the channel of Madeira (empty circles and dotted line) and

Trombetas (black dots and dashed line) rivers. Expected values of FRic were generated by null models

with 999 times resampling for each class of species richness (median and 95% confidence intervals

represented by the solid line and polygon). The null model assumed that local assemblies were formed

by subsets of the regional species pool, regardless of their functional attributes. ................................. 32

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Introdução geral

Uma das principais questões dentro da teoria ecológica é entender como a diversidade

de espécies está distribuída espacial e temporalmente, e que fatores afetam a coexistência de

organismos em determinado local. Além disso, há uma crescente consciência de que a

biodiversidade deve ser estudada em suas múltiplas facetas. Isso tem levado muitos autores a

sugerirem o uso de medidas que incorporem informações sobre a filogenia ou características

funcionais dos organismos, uma vez que as métricas tradicionais (taxonômicas) de diversidade

parecem ter poder de explicação limitado (Cianciaruso, Silva & Batalha, 2009). Nesse contexto,

a diversidade funcional surge como uma ferramenta que vai além dos conceitos tradicionais, ao

analisar as diferentes respostas dos organismos à variabilidade ambiental (Gerisch et al., 2012).

Tal faceta da biodiversidade pode ser entendida como uma medida da amplitude, dispersão ou

abundância relativa dos atributos funcionais das espécies ou indivíduos (Díaz & Cabido, 2001;

Tilman, 2001; Gerisch et al., 2012). Estes atributos funcionais, por sua vez, são quaisquer

características mensuráveis de caráter morfológico, fisiológico ou comportamental dos

organismos (McGill et al., 2006), e que estão associadas a um processo ou a uma propriedade

das comunidades bióticas e/ou do ecossistema em que estão inseridos (Naeem & Wright, 2003;

Violle et al., 2007; Podgaiski, Mendonça Jr. & Pillar, 2011). A utilização desta abordagem

oferece instigantes perspectivas, potencialmente permitindo a elaboração de modelos

ecológicos novos e mais generalizáveis, visto que são mais independentes da história evolutiva

de uma região e seus efeitos sobre as assembleias (Keddy, 1992; Dray & Legendre, 2008).

Análises baseadas somente na identidade das espécies tendem a revelar padrões gerais de

distribuição geográfica, enquanto que o uso de atributos funcionais pode distinguir assembleias

de acordo com características particulares do ambiente (Hoeinghaus, Winemiller & Birnbaum,

2007).

Várias questões ecológicas importantes podem ser investigadas através da abordagem

funcional, como, por exemplo, as relações entre heterogeneidade ambiental e diversidade, ou a

compreensão dos padrões de co-ocorrência de espécies e regras de montagem de assembleias

(Mason et al., 2007; Petchey et al., 2007; Gómez et al., 2010; Safi et al., 2011). A existência

de uma estrutura em assembleias ecológicas sugere que há conjuntos de restrições (regras) sobre

a formação e manutenção (montagem) desses conjuntos de espécies (Sobral & Cianciaruso,

2012). O termo “regras de montagem” (assembly rules) foi originalmente proposto por

Diamond (1975) em um estudo sobre a avifauna do arquipélago da Nova Guiné, buscando

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compreender como assembleias tão distintas são formadas a partir de um mesmo conjunto

regional (pool) de espécies. Posteriormente, essas regras foram definidas como os processos

ecológicos impostos a um pool regional de espécies que agem determinando a estrutura e a

composição de espécies da assembleia local (Keddy, 1992).

Nos últimos anos, ecólogos têm se dedicado a entender essas regras de montagem, e os

dois principais processos frequentemente investigados e considerados responsáveis pela

estruturação das assembleias ecológicas são os filtros ambientais e o princípio da similaridade

limitante (Sobral & Cianciaruso, 2012). Os filtros ambientais atuam como regras de montagem

ao selecionarem espécies que possuem características similares, as quais as permitem

sobreviver sob determinadas condições impostas pelo ambiente (Cornwell, Schwilk & Ackerly,

2006; Sobral & Cianciaruso, 2012). Em contrapartida, a similaridade limitante assume que

espécies sintópicas devem possuir características distintas entre si, uma vez que espécies com

características muito similares devem se excluir por causa da competição (Funk et al., 2008).

Estes processos envolvidos na formação das assembleias são dependentes da escala espacial, já

que escalas espaciais maiores comportam uma alta heterogeneidade de habitats, enquanto em

escalas espaciais menores os habitats tendem a ser mais homogêneos (Webb et al., 2002; Sobral

& Cianciaruso, 2012).

Na Amazônia, os sistemas hídricos apresentam características ambientais bastante

distintas, onde o tipo de água tem importância fundamental na determinação dos conjuntos de

espécies presentes. As águas são consideradas bastante heterogêneas do ponto de vista físico-

químico, podendo ser classificadas de acordo com Sioli (1950) em três tipos principais: brancas,

pretas e claras. As águas brancas são túrbidas e ricas em nutrientes, onde os intensos processos

de erosão e deposição de sedimentos resultam no transporte de grandes cargas de argila e silte

em suspensão, conferindo uma cor barrenta à água. Nesse tipo de água, o pH é

aproximadamente neutro e a alta concentração de íons dissolvidos proporciona uma elevada

condutividade elétrica, além de alta capacidade de troca catiônica dos solos associados às

várzeas (Santos & Ribeiro, 1988; Aucour et al., 2003). As águas pretas são pobres em nutrientes

e apresentam pH ácido, devido às altas concentrações de substâncias orgânicas dissolvidas,

principalmente sob a forma de ácidos húmicos e fúlvicos provenientes da decomposição

incompleta da matéria orgânica da floresta (Sioli, 1967; Goulding, Carvalho & Ferreira, 1988).

As águas claras, por sua vez, possuem elevada transparência, com uma visibilidade variando

entre 1 e 5 m ao longo da coluna d’água (Smerman, 2007). São águas ácidas, com baixa

condutividade elétrica e pobres em sais dissolvidos, caracterizadas pelo diminuto transporte de

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sedimentos argilosos (Santos & Ribeiro, 1988; Konhauser, Fyfe & Kronberg, 1994; Furch &

Junk, 1997).

Nos ambientes aquáticos amazônicos, a riqueza e biomassa da ictiofauna têm sido

positivamente relacionadas com a concentração de oxigênio dissolvido (Henderson & Walker,

1990), com a condutividade elétrica e com a concentração de nutrientes na água (Ibarra &

Stewart, 1989; Galacatos, Stewart & Ibarra, 1996; Saint-Paul et al., 2000; Arbeláez,

Duivenvoorden & Maldonado-Ocampo, 2008). Entretanto, o conhecimento sobre como essas

diferenças afetam a estrutura das assembleias de peixes ainda é escasso em sistemas de água

doce (Hoeinghaus et al., 2007).

Apesar da existência de uma grande diversidade de ambientes aquáticos na Amazônia,

a maioria dos estudos realizados até o presente está concentrada nos grandes rios, onde o foco

principal são as espécies nectônicas de interesse comercial (Ferreira, Zuanon & Santos, 1998;

Cardoso & Freitas, 2008). Embora haja estudos publicados sobre peixes bentônicos associados

ao fundo do canal dos grandes rios (Lopez-Rojas, Lundberg & Marsh, 1984; Stewart, Barriga-

Salazar & Ibarra, 1987; Marrero & Winemiller, 1993; Garcia, 1995; Campos-da-paz, 2000),

apenas a partir das últimas duas décadas foram feitas amostragens sistemáticas neste tipo de

ambiente (e.g. Cox Fernandes, Podos & Lundberg, 2004; Thomé-Souza & Chao, 2004; Cela-

Ribeiro, 2010; Duarte, 2015). Esses estudos evidenciaram a presença de uma ictiofauna

composta por conjuntos de espécies bastante peculiares em termos de adaptações evolutivas e

características funcionais, predominantemente pertencentes às ordens Siluriformes e

Gymnotiformes (Cox Fernandes, 1999; Albert, 2001; Cella Ribeiro, 2010; Duarte, 2016).

Gymnotiformes são peixes conhecidos pela capacidade de gerar (eletrogênese) e

detectar (eletrorrecepção) campos elétricos no meio em que vivem, sendo tais características

utilizadas na comunicação, detecção de presas, defesa, reprodução e movimentação na ausência

de luminosidade (Albert & Crampton, 2005). Estes peixes são facilmente diferenciados dos

demais grupos de peixes neotropicais devido à combinação de algumas características

morfológicas únicas, que incluem corpo alongado e comprimido lateralmente, nadadeira anal

extremamente longa e ausência de nadadeiras dorsal e pélvicas (Frota, Souza & Silva, 2014).

Além de representarem um componente muito importante da biomassa bentônica dos canais

dos rios das bacias Amazônica e do Orinoco (Marrero & Taphorn, 1991; Gracia, 1995), onde

se concentra sua maior diversidade (Albert & Crampton, 2005), o clado representa uma fração

pequena e endêmica da ictiofauna Neotropical (cerca de 3% das espécies; de Santana, 2007).

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Apesar da aparente baixa diversidade específica, em relação às outras ordens reconhecidas para

região Neotropical (Reis, Kullander & Ferraris, 2003), a diversidade e variedade de formas em

Gymnotiformes proporcionam uma importante contribuição para o entendimento da evolução

da biota Neotropical (Hopkins & Heiligenberg, 1978; Albert & Crampton, 2005).

Algumas características físicas do fundo do canal de grandes rios propiciaram a

evolução de uma série de adaptações morfológicas e fisiológicas exclusivas para

Gymnotiformes, contribuindo para uma diversa e especializada assembleia dessa ordem, com

espécies que raramente são encontradas em outros habitats (Albert, 2001; Albert & Crampton,

2005). Estes ambientes possuem profundidade elevada, podendo chegar até 110 m em alguns

rios (Strasser, 2002) e são caracterizados pela ausência de luz e produtividade primária

autóctone, além de forte e constante correnteza (Lundberg et al., 1987; Lundberg & Rapp Py-

daniel, 1994; Albert & Crampton, 2005). Tal conjunto particular de condições provavelmente

gera fortes restrições para o estabelecimento da ictiofauna, o que indica um importante papel

de filtros ambientais selecionando espécies capazes de ocupar esses ambientes. Em

contrapartida, o elevado número de espécies de Gymnotiformes no fundo do canal dos grandes

rios sugere que processos de exclusão competitiva, como previstos pela hipótese de

similaridade limitante, também podem ser importantes na montagem das assembleias locais.

A contribuição relativa desses dois processos para o estabelecimento das assembleias

de Gymnotiformes no canal profundo dos grandes rios amazônicos pode variar em função das

características ambientais predominantes em um determinado rio ou bacia hidrográfica. Estudos

intensivos sobre as assembleias de Gymnotiformes do fundo de canal de rios de águas brancas

e pretas na região de Tefé mostraram que, apesar da maioria das espécies serem encontradas

nos dois ambientes, algumas espécies ocorreram apenas em um dos dois sistemas (Crampton

1996, 1998a b, 1999; Crampton & Albert, 2005). Outro estudo sobre os Gymnotiformes de

canal de grandes rios realizado por Cox Fernandes (1999) no rio Amazonas e em dez de seus

principais tributários mostrou a existência de correlações entre fatores limnológicos e a

ocorrência de espécies. Assim, é razoável supor que as características ambientais dos sistemas

aquáticos afetam a estrutura funcional de assembleias de peixes Gymnotiformes, e que esses

efeitos sejam diferenciados de acordo com o tipo de água predominante nesses sistemas.

Considerando que os organismos em uma assembleia apresentam características que os

permitem sobreviver em um ambiente restritivo e competitivo (Cornwell et al., 2006), o

presente estudo visa investigar se espécies de Gymnotiformes que vivem na calha principal de

rios amazônicos com diferentes tipos de águas apresentam características funcionais

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semelhantes (determinadas por filtros ambientais), ou predominantemente diferentes (segundo

a hipótese de similaridade limitante). Além disso, este estudo avalia se os processos acima

citados atuam de forma diferente em função da escala espacial de observação: regional (entre

rios) e local (entre as assembleias de cada rio).

Objetivos

O objetivo geral deste trabalho foi avaliar a importância relativa de filtros ambientais e

similaridade limitante como mecanismos estruturadores de assembleias de Gymnotiformes em

dois grandes rios amazônicos com diferentes tipos de água. De forma mais específica,

pretendeu-se:

Descrever as assembleias de Gymnotiformes em dois rios amazônicos com

diferentes tipos de água (branca e clara);

Comparar a estrutura funcional de assembleias de Gymnotiformes em dois rios

amazônicos com diferentes tipos de água (branca e clara);

Testar como filtros ambientais e similaridade limitante atuam na montagem de

assembleias de Gymnotiformes em um rio de água branca e um de água clara,

com base em atributos funcionais das espécies.

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Capítulo 1

Marques, N. E. F.; Leitão, R. P.; Cella-Ribeiro, A.; Zuanon, J. A. S. Environmental filters,

limiting similarity, and functional diversity of Gymnotiform fishes in two Amazonian

rivers. Manuscrito em revisão - Freshwater Biology.

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Environmental filters, limiting similarity, and functional diversity of

Gymnotiform fishes in two Amazonian rivers

NAYANA E. F. MARQUES, RAFAEL P. LEITÃO†, ARIANA CELLA-RIBEIRO‡ E

JANSEN A. S. ZUANON

*Instituto Nacional de Pesquisas da Amazônia, Manaus, Brasil †Universidade Federal de Minas Gerais, Belo Horizonte, Brasil ‡Universidade Federal de Rondônia, Porto Velho, Brasil

SUMMARY

1. Using an approach that combines species functional traits with null models helps

explain species distribution and co-occurrence patterns and community assembly

processes. Such assembly rules are expected to have different effects at diferente

spatial scales as community assembly processes appear to vary with scale.

2. In this study, we assessed the relative importance of environmental filters and

limiting similarity as structuring mechanisms of Gymnotiformes assemblages in two

Amazonian river channels with differing limnological characteristics and at different

spatial scales.

3. Using functional indices and null models, we have demonstrated that local

environmental factors are most likely to limit the presence of particular functional

traits in both rivers, thereby leading to a functionally unique ichthyofauna in each

water system. A limiting similarity effect on Trombetas River assemblages was

observed at a smaller spatial scale, thus reinforcing the importance of the relationship

of dependence between ecological processes and spatial scale.

4. The results reported here suggest that environmental filters are more important for

Gymnotiformes species distribution in Amazonian river channels, at both large and

small spatial scales, and that they are mediated by species’ functional traits.

Keywords: assembly rules, null models, ecomorphological traits, functional diversity indices,

benthic ichthyofauna

Correspondence: Nayana Marques, Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Avenida André Araújo, 2936, CEP 69080-971, Manaus, Brazil. Email: [email protected]

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Introduction

Understanding how species diversity is spatially and temporally distributed, as well as

the factors that affect the coexistence of organisms at a particular site, are key to

understanding theoretical ecology. Recently, there has been a growing sentiment that

biodiversity should be studied in its multiple facets and many researchers now recommend

using measures that include information on the phylogeny or functional traits of organisms

because traditional (taxonomic) diversity metrics have limited explanatory power

(Cianciaruso et al., 2009). In this context, functional diversity emerges as a tool that extends

beyond traditional concepts by analysing organisms’ responses to environmental variability

based on their ecological/functional traits (Gerisch et al., 2012). Such traits include any

measurable morphological, physiological or behavioural characteristics of those organisms

(McGill et al., 2006), and are often associated with processes or properties of biotic

communities and/or the ecosystem in which they occur (Naeem & Wright, 2003; Violle et al.,

2007; Podgaiski et al., 2011). These aspects of biodiversity may therefore be considered a

measure of the amplitude, dispersion or relative abundance of species functional traits in na

assemblage (Díaz & Cabido, 2001; Tilman, 2001; Gerisch et al., 2012). The use of this

approach offers exciting new prospects to researchers in this field, potentially enabling them

to construct new and more generalizable ecological models because they are less dependent

on the regional evolutionary history and its effects on assemblages (Keddy, 1992; Dray &

Legendre, 2008). Analyses based exclusively on species taxonomic identity tend to generate

general geographical distribution patterns, whereas using functional traits differentiates

assemblages according to specific environmental characteristics (Hoeinghaus et al., 2007).

Several key ecological issues may be examined using the functional approach,

including, for example, environmental heterogeneity and diversity relationships or the

understanding species co-occurrence patterns and community assembly rules (Mason et al.,

2007; Petchey et al., 2007; Gómez et al., 2010; Safi et al., 2011). The existence of an

ecological structure of assemblages suggests there is a set of constraints (rules) on the

formation and maintenance (assemblage) of those species groups (Sobral & Cianciaruso,

2012). The term ‘assembly rules’ (cf. Diamond, 1975) refers to processes involved in the

formation of different assemblages from the same regional species pool. Those rules were

later defined as ecological processes imposed on a regional species pool, which control the

species structure and composition of local assemblages (Keddy, 1992).

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In more recent years, ecologists have focused on understanding those assembly rules,

with environmental filters and limiting similarity being the two mechanisms most often

examined and considered responsible for structuring ecological assemblages (Sobral &

Cianciaruso, 2012). Environmental filters hypothetically select species with similar

characteristics, which allow them to survive under specific environmental conditions

(Cornwell et al., 2006; Sobral & Cianciaruso, 2012). Conversely, the principle of limiting

similarity assumes that syntopic species should have different traits because competitive

exclusion should prevent the co-occurrence of species with similar traits (Funk et al., 2008).

Many studies indicate that different mechanisms affect species co-occurrence patterns and

assemblage maintenance at different spatial scales (Buckley et al., 2010; Gotelli, Graves &

Rahbek, 2010; McGill, 2010). At large spatial scales, high environmental heterogeneity is

likely to increase the importance of environmental filters, selecting species with similar

environmental requirements in specific habitats. In contrast, at small spatial scales,

environmental homogeneity implies that limiting similarity plays a key role in assemblage

structure, restricting the occurrence of species with similar traits (Webb et al., 2002; Sobral &

Cianciaruso, 2012).

Testing such processes is challenging because the Amazon is an extremely diverse and

heterogeneous environment. Such heterogeneity is also observed in Amazonian water

systems, which can be differentiated according to their physico-chemical properties. Sioli

(1950) classified Amazonian rivers into the following three main types: white-, black-, and

clear-water rivers. These classifications were based on differences that were mainly related to

the quantity of nutrients, suspended solids, pH, and electrical conductivity. Despite the fact

that most studies focus on nektonic areas of rivers and lakes, particularly on species of

commercial interest (Ferreira, Zuanon & Santos, 1998; Cardoso & Freitas, 2008), there is a

large diversity of aquatic habitats in the Amazon, in addition to the physico-chemical

heterogeneity observed in those rivers. Although reports on benthic fish associated with large

riverbeds are not recent (for example, Lopez-Rojas, Lundberg & Marsh, 1984; Stewart,

Barriga-Salazar & Ibarra, 1987; Marrero & Winemiller, 1993; M. Garcia, unpublished data;

Campos-da-Paz, 2000), systematic samplings were only conducted in this environment during

the last two decades (Cox-Fernandes, Podos & Lundberg, 2004; Thomé-Souza & Chao, 2004;

A. Cella-Ribeiro, unpublished data; Duarte 2016). Those studies revealed that ichthyofauna

consisted of unusual species in terms of evolutionary adaptation and functional traits,

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especially species belonging to the Siluriforms and Gymnotiforms orders (Cox-Fernandes,

1999; Albert, 2001; Duarte 2016).

Gymnotiforms is an order of fishes known for their capacity to generate

(electrogenesis) and detect (electroreception) electric fields in the environment they inhabit.

Such traits are used for communication, prey detection, defense, reproduction, and movement

in the absence of light, including in large riverbeds (Albert & Crampton, 2005; Alves-Gomes,

2014). Other traits (morphological, physiological and behavioural) exclusive to

Gymnotiforms must also have been favoured in such environmental conditions, thereby

contributing to the high ecological specialisation of these fishes, which rarely occur in other

habitats (Albert, 2001; Albert & Crampton, 2005). Gymnotiformes are an important

component of the benthic biomass of Amazon basin river channels (Marrero & Taphorn,

1991; M. Garcia, unpublished data) and an endemic component of neotropical ichthyofauna

(de Santana 2007). This clade is therefore of great interest to those studying biogeography.

The channels of large Amazonian rivers are deep, often descending down to 110 m

(Strasser 2002). Their riverbeds typically receive no light, exhibit no autochthonous primary

productivity, and have strong, constant currents (Lundberg et al., 1987; Lundberg & Py-

Daniel, 1994; Albert & Crampton, 2005). Such a particular set of conditions appears to

impose strong constraints to ichthyofauna establishment, which highlights the role of

environmental filters in selecting the species capable of occupying those environments.

Conversely, the high number of Gymnotiforms species co-occurring in large riverbeds

suggests that competitive exclusion processes may also be important for local community

assembly, as predicted by the limiting similarity theory.

The relative contribution of both processes to establishing Gymnotiforms assemblages

in the large Amazonian riverbeds may vary with the environmental conditions prevailing in

any particular river or river basin. Intensive studies on the Gymnotiforms assemblages of deep

white- and black-water river channels in the Tefé region showed that, although most species

are found in both environments, some species only occurred in one of the two systems

(Crampton, 1996, 1998a b, 1999; Crampton & Albert, 2005). Another study on large river

channel Gymnotiforms, conducted by Cox-Fernandes (1999) in the Amazon River and ten of

its main tributaries, showed there was a correlation between limnological factors and species

occurrence. Thus, the environmental characteristics of water systems presumably affect the

functional structure of Gymnotiforms assemblages, and such effects differ according to the

predominant water type in those systems.

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This study aims to assess the functional traits of Gymnotiforms species that inhabit the

main channels of Amazonian rivers with different water types. Considering that organisms in

a given assembly represent the characteristics that allow them to survive in a restrictive and

competitive environment (Cornwell et al., 2006), do these fishes exhibit similar

(environmental filters) or predominantly different (limiting similarity) functional traits?

Additionally, this study evaluates whether the aforementioned processes act differently

depending on whether they are observed at local (between the assemblages of each river) or

regional (between rivers) spatial scales.

Methods

Study area

In this study, we used data previously collected from two large Amazonian riverbed

environments with different limnological characteristics: the Madeira and Trombetas rivers.

The Madeira River is part of the largest sub-basin of the Amazon basin, covering 1,380,000

km2 in Brazil, Bolivia, and Peru (Goulding, Barthem & Ferreira, 2003; Py-Daniel, 2007). The

river runs approximately 3,400 km from its headwaters in the Bolivian Andes to the mouth of

the Amazon River and is the longest tributary of the Amazon River (Py-Daniel, 2007;

Bernardi et al., 2009). The Madeira River is a typically rectilinear river, with meandering

passages that account for 15% of Amazon River discharge into the Atlantic Ocean. Based

upon a classification by Sioli (1967), it is considered a white-water river (Goulding et al.,

2003; Py-Daniel, 2007). Its waters are highly turbid, yellowish to ochre, and carry large

quantities of nutrient-rich suspended solids (originating in the Andean and pre-Andean

regions; Goulding, Barthem & Ferreira, 2003). Although vertical transparency is less than 10

cm for most of the year, that value may increase to 40 cm during short periods of local

drought (Goulding 1979). Samples collected from 15 points, stretching approximately 370

km, and from six collection sites during December 2008 to January 2011 (Figure 1), were

used to characterise the electric fish assemblages of this river.

The Trombetas River, in contrast, was classified as a clear-water river (Sioli & Klinge,

1962), with low quantities of suspended solids and vertical transparency ranging from 0.6 m

to 4.0 m. The river was formed by the union of the Poana and Anamú Rivers, the headwaters

of which are within the borders of both Guyana and Suriname. It is approximately 760 km

long from its headwaters to the mouth of the Amazon River (Ferreira, 1993). Its basin covers

an area of approximately 134,000 km 2 and is located in the state of Pará, Brazil (Ferreira,

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1993; Goulding, Barthem & Ferreira, 2003). Data were collected six times at 12 sampling

points (Figure 2) from a stretch of river approximately 70 km long during the period from

March 2005 to February 2006.

Ichthyoogical material

Samples of Gymnotiforms assemblages were performed using a standardised collection

procedure and a benthic trawl net (Figure S1, Supporting information). This funnel-shaped net

is 6 m long and approximately 6 m high, with a 3 m wide mouth opening, and is composed of

6 mm mesh (opposite knots). A pair of wooden doors, with an iron frame on the net mouth,

allowed for the maintenance of the vertical opening of the trawl net when it was towed

downriver by a motorized canoe. Bottom trawling was carried out for approximately 10

minutes (covering a length of about 400 m) per period at each sampling point. Voucher

specimens of collected species were deposited at the National Institute of Amazonian

Research (INPA) and the Federal University of Rondônia (UNIR).

Environmental data

Environmental variables were recorded during the collections in order to characterize the

sampling sites. Limnological variables were analysed using portable digital devices of water

samples in a vertical Van Dorn bottle. Those samples were taken just prior to collecting the

fishes. The following limnological parameters were measured: pH, electrical conductivity

(µS.cm-1), water temperature (°C), dissolved oxygen (mg.l-1), and turbidity (UNT). Water

transparency (cm) was determined using a Secchi disk. The mean water column depth at each

collection site was measured using a digital echo sounder that took readings during every

minute of fish collection.

Assemblage structure and diversity

Non-Metric Multidimensional Scaling (NMDS) analysis was performed in both rivers

to evaluate the Gymnotiforms’ taxonomic composition (species). The structure and functional

diversity of Gymnotiforms assemblages were subsequently evaluated using an

ecomorphological analysis, where morphological and anatomical measurements were taken

from up to 12 adult specimens of each species (Figure S2, Supporting information). Those

measurements were combined into 13 ecomorphological traits related to trophic ecology,

habitat use, and locomotion type for each species. Specimens from other sites and other

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periods of time, were measured for those rare species that were represented by less than three

adult specimens. In addition to the external measurements, tooth number and gill raker shape

were analysed in at least three specimens per species, totalling 15 functional traits (Table S1,

Supporting information). Such traits are commonly used in functional and ecomorphological

studies (Gatz, 1979; Fulton, Bellwood & Wainwright, 2001; Sibbing & Nagelkerke, 2001;

Karpouzi & Stergiou, 2003; Dumay et al., 2004; Villéger et al., 2010; Leitão et al., 2016).

The specimens were photographed and then weighed on an electronic scale (0.01 g).

Body width, mouth width, mouth height, and snout length were measured using a digital

calliper (0.01 mm). All other morphological measurements were taken using digital images

analysed using Image J software, version 1.49. Tooth count and gill raker characteristics were

determined using a stereomicroscope.

A Gower distance matrix between each pair of species was calculated for the regional

species pool based on ecomorphological data (Madeira and Trombetas Rivers). This method

permits the use of different functional traits, but assigns equal weight to each trait, as some

measured functional traits are not represented by continuous variables (Villéger, Mason &

212 Mouillot, 2008). Subsequently, a principal coordinates analysis (PCoA) of the distance

matrix was performed, with the first three axes being used to construct the multidimensional

functional space of the assemblages. The selection of the number of PCoA axes was

determined based on a trade-off between functional space quality (according to Maire et al.,

2015; Figure S3, Supporting information) and the number of samples that should be excluded

because of restrictions on the computation of functional diversity indices. That is, the number

of species of a local assemblage should be higher than the number of axes selected (Villéger

et al., 2008).

Based on that functional space, where each species was placed according to the coordinates of

their functional traits (each PCoA axis, in this study), two indices were calculated to

quantitatively describe the functional structure of assemblages: Functional Richness (FRic)

and functional identity (community-weighted mean of a trait – CWM). Functional Richness is

the volume of the functional space occupied by all species within the assemblage, indicating

the range of trait combinations or niche occupation (Villéger et al., 2008). The CWM is the

mean value of each trait for a local assemblage, weighted by species abundance (Lavorel et

al., 2008). This index may be considered the functional identity of an assemblage and has

proven effective in explaining community dynamics and ecosystem properties (Garnier et al.,

2004; Louault et al., 2005; Lavorel et al., 2008; Leitão et al., 2016). Functional indices were

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calculated using cluster, ape and geometry analyses in R software, version 3.0.3 (R Core

Team, 2014).

Testing assembly rules

Two analytical approaches were used to test how environmental filters and/or limiting

similarity processes operated in structuring Gymnotiforms assemblages. First, the functional

identity (CWM) values of assemblages were compared between the Madeira and Trombetas

Rivers using Student’s t-tests for regional-scale analyses. For such analyses, the CWM values

of each PCoA axis were initially evaluated for normality and homoscedasticity using the

Shapiro-Wilk and Levene tests, respectively. A significance level of ɑ = 0.05 was used. The

greater differences between both systems, rather than within each system, suggested that

environmental filters would be key assemblage structuring mechanisms at a regional scale.

The relationships between species richness and functional richness (FRic) of the

assemblages of each system were evaluated separately and at a local scale. Null models were

used to test the significance of the observed relationships, assuming that local assemblages

would be random subsets of the regional species pool, which were assembled regardless of

species functional traits (Mouillot, Dumay & Tomasini, 2007). Thus, species were randomly

removed from the regional pool without changing the number of species in each local

assemblage, and the FRic values were calculated 999 times for each condition of taxonomic

richness. The median, lower, and upper quartile FRic null values were then calculated.

Finally, the observed FRic values were compared with those generated by applying the null

model (cf. Mason et al., 2012). Higher values than those expected indicated there was a

predominance in the limiting similarity process (that is, co-existing species are functionally

more different from each other than expected by chance). In contrast, the reverse (lower FRic

values than randomly expected) indicated there was a predominance of environmental filters

(that is, co-existing species are functionally more similar to each other than randomly

expected). Observed values similar to those generated by the null model indicated that

assemblages should have been randomly structured (Villéger et al., 2008). All analyses were

performed using R software, version 3.0.3 (R Core Team, 2014).

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Results

General structure of Gymnotiforms assemblages in the Madeira and Trombetas Rivers

A total of 40 Gymnotiforms species, belonging to the Apteronotidae, Hypopomidae,

Rhamphichthyidae, and Sternopygidae families, were collected from both study areas,

including 25 species from the Trombetas River and 31 from the Madeira River (Table B1,

Supporting information). These assemblages were dominated by species within the

Apteronotidae (26 species) and Sternopygidae (nine species) families. Specimens from both

families were also collected in trawl samples. The Apteronotidae family accounted for 83% of

the 1367 specimens collected in the Madeira River. Of the 1909 specimens collected from the

Trombetas River, the Sternopygidae family accounted for 85% of them. On average, the

assemblages of the Madeira and Trombetas Rivers included nine (four to 21) and eight (four

to11) species, respectively. Although 16 species were identified in trawl samples taken from

both rivers, the taxonomic composition of those samples were different (Figure 3).

Environmental characterization

Table 1 outlines the values of limnological parameters encountered at the sampling points in

the Madeira and Trombetas Rivers. Mean depth, temperature, pH, and dissolved oxygen were

similar in both the Madeira and Trombetas Rivers (Table 1). Differences were, however,

observed in the other variables analysed. Despite the variation in electrical conductivity along

the Madeira River (22 -76 µS.cm-1) (Table 1), electrical conductivity was generally higher

here than in the Trombetas River. Water transparency in the Trombetas River (150 ± 40.35

cm) was considerably higher than in the Madeira River (24.76 ± 16 cm). Similarly, turbidity

was low in the Trombetas River (4.57 ± 1.7 UNT) with a narrow variation (2 – 7 UNT) but

high in the Madeira River (226.92 ± 146.25 UNT) (Table 1).

Functional structure of assemblages

Functional traits were measured in 444 specimens from 40 Gymnotiforms species. Those

species exhibited a wide variation in the values of some functional traits, especially those

associated with body size and trophic traits (Figure S3, Supporting information). The

functional structure of assemblages revealed a high level of overlap in both rivers, with the

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Madeira species group encompassing almost all the functional richness of the species found in

the Trombetas River (Figure 4).

Environmental filters or limiting similarity

The functional identity (CWM) of Gymnotiforms assemblages was significantly

different between the Madeira and Trombetas Rivers, particularly in axes 1 and 2 of the

functional space (Figure 5). In axis 1, mouth position and eye size were the most important

traits, as suggested by their positive values. Pectoral fin position, mouth shape, and relative

snout length produced negative values. In axis 2, body mass, mouth-opening area, and eye

position resulted in a positive correlation with this axis, whereas body area produced the

highest negative correlation (Table B2, Supporting information).

In the Madeira River, the FRic values of local Gymnotiforms assemblages were

predominantly lower than expected, whereas in the Trombetas River, the FRic values of local

assemblages were mostly higher than the values randomly generated by the null model

(Figure 6).

Discussion

This study showed that the functional diversity of Gymnotiforms assemblages in two

Amazonian riverbeds with different water types is primarily affected by mechanisms of

environmental filters. These results corroborate those from other studies of fish assemblages,

which showed that interspecific competition plays no role in the structure and co-occurrence

patterns of such assemblages (de Azevedo et al., 2006, Mouillot et al., 2007). Some

researchers have reported a weak interaction between fish species in freshwater environments,

where species co-occurrence patterns are driven by common species-habitat relationships,

indicating that environmental filters may promote the functional patterns of such assemblages

(Poff & Allan, 1995; Peres-Neto, 2004). Some small spatial scales studies have showed,

however, that the occurrence of competition (and the limiting similarity principle) between

fish species (Rodrigues, 1995; Resetarits, 1997) occurs because community assembly

processes are spatial scale-dependent, as observed in our results at a local scale along the

Trombetas River. Thus, the critical question is what mechanism has the strongest effect on

assemblage structure at the scale of observation used (Mouillot et al., 2007, Mouchet et al.,

2010, Arrieira, 2015).

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Species within the Apteronotidae and Sternopygidae families exhibited the greatest

species richness and abundance in this study. The predominance of certain species from both

families in the channels of large rivers may be related to their specific morphological and

physiological adaptations, which developed to occupy just such a habitat. These

specializations are typical of a Gymnotiforms assemblage that rarely occurs in other

environments (Albert & Crampton, 2005). A body adapted to foraging, locomotion in

environments with a constant and relatively strong current, small eyes, and an efficient

electrogenic-electrosensory system are among such adaptations (Stewart, Ibarra & Barriga-

Salazar, 2002; Albert & Crampton, 2005). Although all Gymnotiforms have such sensory

systems, species with wave-type electric organ discharges (EODs), including those in the

Apteronotidae and Sternopygidae families, tend to dominate large riverbed environments,

with few species that generate pulse-type discharges (Albert & Crampton, 2005). The low

incidence of pulse species in such extremely restrictive environments may be related to the

low and irregular frequencies of EODs of those fish species. This is in contrast to the high and

constant frequencies of wave fishes, which enable the latter species to gather information

about their environment faster.

Although some correlations between water quality and species occurrence have been

reported in the literature (Cox-Fernandes, 1999), riverbed assemblages of white-water rivers

tend to be similar to those of nutrient-poor rivers, including black- and clear-water rivers (M.

Garcia, unpublished data; Crampton, 1998b), as was observed between the Madeira and

Trombetas Rivers. However, the difference observed here between the functional identity of

Gymnotiforms assemblages in two riverbeds implies the existence of different environmental

pressures selecting species according to the functional traits in the trawl samples of each river.

This difference was probably accentuated by the unequal abundances of species between the

two rivers; functional identity calculations take into account the abundance of species in each

local assemblage.

Some environmental factors may limit the presence of specific functional traits and,

therefore, particular functional groups of species in specific locations, thus acting as

environmental filters (Mouillot et al., 2007). Although parameters, including temperature, pH,

and dissolved oxygen, which are considered key abiotic factors affecting electric fish

assemblages (Crampton, 1998a, Silva et al., 2002), showed no significant difference between

the two rivers, electrical conductivity varied significantly. These key physico-chemical

parameters may affect the electrosensory system sensitivity of those fishes and even the

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18

distribution and relative abundance of some species (Bullock et al., 1972; Knudsen, 1975;

Bell et al., 1976; Silva et al., 2003). Marked differences in turbidity and water transparency

may have also generated key environmental constraints in both rivers. This may have been

due to the dynamics of some ecosystem processes, e.g., primary productivity, in other areas of

those water systems, such as riverbanks and floodplain forests, resulting in repercussions to

the main channel.

In this context, the predominance of members of the Apteronotidae family in the

Madeira River, and those of the Sternopygidae family in the Trombetas River, may be related

to some of their functional traits, adapting the species of both families to each environment.

The functional structure of assemblages of each river suggests differences primarily related to

body size and trophic morphology, as expected for Gymnotiforms, since the presence of an

electrogenic-electrosensory system imposes strong restrictions on the morphological diversity

of the group (Albert, 2001; Albert & Crampton, 2005).

In rivers with high quantities of suspended solids, including the Madeira River, the

proportionally smaller size of fish eyes may function as mechanical protection against such

particles (Ryder & Pesendorfer, 1989). This is usually offset by the improvement of another

sensory organ, which most likely replaces sight in the search for food (Stewart et al., 2002).

Such increased dependency on the electrosensory system in the Madeira River may favor the

increased occurrence of the Apteronotidae in that river because those species possess a

neurogenic electric organ. The synapses involved in the EODs of those fish species are faster

than the chemical synapses of electric fishes with a myogenic electric organ (Alves-Gomes,

2014). Furthermore, rivers with high electrical conductivity tend to cause interference and

more quickly dissipate electric fields, reinforcing the need for a more refined sensory system.

In the Trombetas River, the presence of species with larger eyes, combined with high water

transparency, suggests that sight may play a more important role in complementing the

electrogenic-electrosensory system than was previously thought. Regarding trophic

morphology, species from the Madeira River had longer snouts and a greater mouth opening,

exhibiting trophic specialisations typical of species that forage among substrate particles and

use suction to catch their prey. Conversely, most species in the Trombetas River had a short

snout and terminal mouth, indicating that those species feed primarily in the water column.

This suggests that there are different food preferences between the two rivers. The increased

transparency observed in the Trombetas River, for example, appeared to favour the

occurrence of Rhabdolichops species, which are mostly planktivorous (Lundberg et al., 1987)

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19

and may benefit from the higher planktonic productivity of clear-water rivers and, therefore,

the greater availability of such prey carried in the channel.

At a small spatial scale, the functional diversity observed in assemblages along the

channel of each river was mostly lower than expected for the Madeira River. This suggests

that the processes of environmental filters must have played a key role in structuring those

assemblages and that co-existing species tend to be more similar than expected. This indicates

that environmental filters may strongly affect the functional diversity of electric fish

assemblages at both large and small spatial scales. Although it is expected that the habitat

homogeneity increases the importance of limiting similarity and restricts the co-occurrence of

species with similar functional characteristics in smaller spatial scales (Webb et al., 2002;

Sobral & Cianciaruso, 2012), the importance of intrinsic properties of environment should not

be underestimated. Recent studies of assemblages inhabiting large Amazonian river channels

(e.g., M. Freitas, unpublished data; Duarte, 2016) have reported high diversity and constant

food availability in those environments, wherein species showed generalist and opportunistic

feeding strategies. Such high trophic plasticity may reduce the competition for resources

between species, thereby leading to a decreased importance of the limiting similarity process,

as observed in the Madeira River assemblages. Furthermore, sampling points in that river

were separated by far greater distances than in the Trombetas River, potentially encompassing

a more heterogeneous environment. However, limiting similarity may not be completely

discarded because this mechanism was also observed in the results from the Trombetas River

samples, albeit less strongly. Thus, the two mechanisms may affect local community

assemblages, albeit with different effects on the functional diversity of electric fish

assemblages, depending on the scale and local environmental characteristics.

The difficulty of sampling in the channels of the great Amazonian rivers imposed

some limitations to this study, since the benthic trawling could not accurately demarcate the

habitat breadth occupied by each local assemblage. This fact makes it difficult to assess local

environmental conditions and thus hinders the understanding of the relationships between the

patterns that structure assemblages and the environment. Furthermore, due to the low number

of captures per month, samples were grouped by collection site, which could have led to a

loss of fine-scale data in the analyses. Finally, the lack of biological and ecological

information for most of the species that inhabit this environment restricts the feasibility of

using functional attributes directly related to the electrogenic-electrosensory system. This

natural history information would certainly contribute to a more accurate assessment of the

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20

processes and important environmental characteristics that structure Gymnotiforms

assemblages in the large Amazonian river channels.

Conclusions

Using an approach combining species functional traits with null models helps to

understand species distribution and co-occurrence patterns and community assembly

processes. The results reported in this study suggest that environmental filters are more

important for Gymnotiforms species distribution in Amazonian river channels, at both large

and small spatial scales, and that they are mediated by species’ functional traits. Local

environmental factors most likely limits the presence of particular functional traits in both

rivers, thereby leading to a functionally unique ichthyofauna in each of the water systems.

Acknowledgments

We thank Douglas Bastos for the preparation of the maps; the partnership between

Santo Antônio Energia (SAE), the Universidade Federal de Rondônia (UNIR), and the

Instituto Nacional de Pesquisas da Amazônia (INPA) for the data generated during

ichthyological studies along the Madeira River. We also thank ICMBio and the Mineração

Rio do Norte for the opportunity to carry out fish sampling in the Trombetas River. Nayana

Marques received a study grant from CAPES. Jansen Zuanon received a CNPq productivity

grant (process # 313183/2014-7).

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Table 1. Average ± S.E. and minimum and maximum values of limnology parameters measured in December /

2008, Jul / 2009, Oct / 2009, Jan / 2010, Aug / 2010 and jan / 2011 on the Madeira River and during every month

of the 2005 year in Trombetas.

Madeira

Trombetas

Average ± S.E. Min.-Max. Average ± S.E. Min.-Max.

Conductivity

(µS.cm-1)

49.35 ± 17.23

22 – 76

12 ± 2.12

8.5 – 19.6

Dissolved

oxygen

(mg.l-1)

6.40 ± 2.27

4.45 – 11.2

5.43 ± 0.37

4.68 – 6.2

Ph

6.714 ± 0.55

5.28 – 7.56

6.18 ± 0.37

5.1 – 7.25

Mean depth

(m)

8.55 ± 3.69

2.36 – 21.36

8.33 ± 3.1

2 – 16.9

Temperature

(°C)

29.22 ± 1.22

27.49 – 32.13

30 ± 2.54

23.9 – 33.3

Transparency

24.76 ± 16

8 – 70

150 ± 40.35

100 – 310

(cm)

Turbidity

(UNT)

226.92 ± 146.25

17.17 – 634

4.57 ± 1.7

2 – 7

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Figure 1. Location of the study area and sampling sites (black triangles) in Madeira River.

Figure 2. Location of the study area and sampling sites (black triangles) in Trombetas River.

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Figure 3. Non-Metric Multidimensional Scaling (NMDS) of Gymnotiformes assemblages of Madeira (n = 15;

triangules) and Trombetas (n = 12; circules) rivers based on species abundance (A) and presence/absense (B)

data.

Figure 4. Tridimensional representation of the functional space occupied by the global species pool (40 species)

of Gymnotiformes in the Madeira and Trombetas rivers. Each plot represents two axes of a Principal Coordinate

Analysis (PC), where species are plotted according to their respective trait values. Species ocurring in both

regions are represented by “x” symbols. Species found exclusively in Madeira or in Trombetas rivers are

represented by empty or black circules respectively. Projections of the convex hull volumes are illustrated by the

polygons embedding the two sets of species.

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Figure 5. Community weighted means (CWM) of Gymnotiformes local assemblages of Madeira (n = 15) and

Trombetas (n = 12) rivers, expressed by the average values of the first three axes of functional space weighted by

the abundance of species. Vertical lines represent 95% confidence intervals.

Figure 6. Observed and expected relationships between species richness and functional richness (FRic) of

Gymnotiformes assemblies in the channel of Madeira (empty circles and dotted line) and Trombetas (black dots

and dashed line) rivers. Expected values of FRic were generated by null models with 999 times resampling for

each class of species richness (median and 95% confidence intervals represented by the solid line and polygon).

The null model assumed that local assemblies were formed by subsets of the regional species pool, regardless of

their functional attributes.

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Supporting information

Figure S1. Schematic illustration of the use of bottom trawl net sampling. (Source: A. Cella-Ribeiro,

unpublished MSc Thesis).

Figure S2. Morphological traits measured for Gymnotiforms fishes from digital pictures (A): Amc body depth,

Cfna length to the end of anal fin, Cc head depth along the vertical axis of the eye, Inp distance between the

insertion of pectoral fin to the bottom of the body, Ainp body depth at the level of the pectoral-fin insertion, Cnp

pectoral-fin length, Arnp pectoral-fin surface, Cna anal-fin length, Arna anal fin surface, Ac head depth along the

vertical axis of the eye, Do eye diameter, Doc distance between the center of the eye to the bottom of the head,

Dbc distance from the top of the mouth to the bottom of the head along the head depth axis; and with digital

caliper; Cf snout length (B,C): Lc body width, Lb mouth width, Ab mouth depth.

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Figure S3. Relation between the quality of functional space (calculated conjointly to Madeira and Trombetas

rivers) and the number of axes of the e o número de eixos da Principal Coordinates Analysis (PCoA).

Body Mass

Figure S4. Representation of the functional space of the regional pool of Gymnotiforms (N= 40 species). Each

plot represents two axes of a Principal Coordinates Analysis, where each species was plotted according to its

atribute values. Species with high (superior quartile) and low (inferior quartile) values for each continuous

ecomorphological trait are represented by red and blue dots respectively. Pleas check specific legends to ordinal

and nominal traits below the respective plots.

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Oral-gape surface

Oral-gape shape

Oral-gape position

Figure S4 (Cont.). Representation of the functional space of the regional pool of Gymnotiforms (N= 40

species). Each plot represents two axes of a Principal Coordinates Analysis, where each species was plotted

according to its atribute values. Species with high (superior quartile) and low (inferior quartile) values for each

continuous ecomorphological trait are represented by red and blue dots respectively. Pleas check specific legends

to ordinal and nominal traits below the respective plots.

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Eye size

Eye position

Body transversal shape

Figure S4 (Cont.). Representation of the functional space of the regional pool of Gymnotiforms (N= 40

species). Each plot represents two axes of a Principal Coordinates Analysis, where each species was plotted

according to its atribute values. Species with high (superior quartile) and low (inferior quartile) values for each

continuous ecomorphological trait are represented by red and blue dots respectively. Pleas check specific legends

to ordinal and nominal traits below the respective plots.

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Body transversal surface

Pectoral-fin position

Aspect ratio of the pectoral-fin

Figure S4 (Cont.). Representation of the functional space of the regional pool of Gymnotiforms (N= 40

species). Each plot represents two axes of a Principal Coordinates Analysis, where each species was plotted

according to its atribute values. Species with high (superior quartile) and low (inferior quartile) values for each

continuous ecomorphological trait are represented by red and blue dots respectively. Pleas check specific legends

to ordinal and nominal traits below the respective plots.

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Pectoral-fins surface to body size ratio

Anal-fin surface to body size ratio

Snout length

Figure S4 (Cont.). Representation of the functional space of the regional pool of Gymnotiforms (N= 40

species). Each plot represents two axes of a Principal Coordinates Analysis, where each species was plotted

according to its atribute values. Species with high (superior quartile) and low (inferior quartile) values for each

continuous ecomorphological trait are represented by red and blue dots respectively. Pleas check specific legends

to ordinal and nominal traits below the respective plots.

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Gill-raker shape

Number of teeth

Figure S4 (Cont.). Representation of the functional space of the regional pool of Gymnotiforms (N= 40

species). Each plot represents two axes of a Principal Coordinates Analysis, where each species was plotted

according to its atribute values. Species with high (superior quartile) and low (inferior quartile) values for each

continuous ecomorphological trait are represented by red and blue dots respectively. Pleas check specific legends

to ordinal and nominal traits below the respective plots.

Gill-raker shape categories

+ Short/sparse

▲ Intermediate

■ Long/numerous

Teeth shape categories

● Absent

♦ Sparse

x Intermediate

Numerous

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Figure S5. Observed (points) and expected (dashed line) relationships between species richness and functional

richness (FRic) of Gymnotiformes assemblages from the channels of Madeira (A) and Trombetas (B) rivers.

Expected values of FRic were generated by null models with 999 times resampling for each class of species

richness (median and 95% confidence intervals represented by the solid line and polygon). The null model

assumed that local assemblies were formed by subsets of the species pool of each river separately, regardless of

their functional attributes.

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Table S1. List of the functional traits measured and their respective ecological meanings. Codes for

morphological measures are shown in Fig. S2.

Functional trait Calculation/ Class Ecological meaning References

Number of teeth Absent

Sparse

Intermediate

Numerous

Nature of food items captured

and feeding method

adapted from Gatz

(1979)

Gill-raker shape

Short/ sparse

Intermediate

Long/ numerous

Filtering ability and gill

protection

adapted from Sibbing &

Nagelkerke (2001)

Oral-gape surface

Mw Md/Bw Bd Nature of food items captured

and feeding method

adapted from Karpouzi

& Stergiou (2003)

Oral-gape shape Md/Mw Method to capture food items Karpouzi & Stergiou

(2003)

Oral-gape position Mo/Hd Feeding method in the water

column

adapted from Sibbing &

Nagelkerke (2001)

Eye size Ed/Hd Prey detection adapted from Boyle &

Horn (2006)

Eye position Eh/Hd Vertical position in the water

column

Gatz (1979)

Body transversal

shape

Bd/Bw Verrtical position in the water

column and hydrodynamism

Sibbing & Nagelkerke

(2001)

Body transversal

surface Ln[(π/4 Bw Bd) + 1]/

ln (Mass + 1)

Mass distribution along the

body for hydrodynamism

Villéger et al. (2010)

Pectoral-fin position PFi/PFb Pectoral fin use for

maneuverability

Dumay et al. (2004)

Aspect ratio of the

pectoral fin

PFi2/PFs Pectoral fin use for propulsion adapted from Fulton et

al. (2001)

Pectoral-fins surface

to body size ratio 2 PFs/(π/4 Bw Bd) Acceleration and/or

maneuverability efficiency

adapted from Villéger et

al. (2010)

Anal-fin surface to

body size ratio

AFs/Bd x Bw Maneuverability and

moviment stabilization

Present study

Snout length Sn/Hd Method to capture food items Present study

Mass Log (Mass + 1) Metabolism, endurance and

swimming ability

Villéger et al. (2010)

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Table S2. Taxonomic composition and abundance of Gymnotiformes assemblages from Madeira and Trombetas

rivers.

Family Species Cod. sp Madeira Trombetas

Apteronotidae Adontosternarchus balaenops ado.bala 36 6

Adontosternarchus clarkae ado.clar 211 1

Adontosternarchus nebulosus ado.nebu 2 -

Adontosternarchus sachsi ado.sach 1 30

Apteronotus bonapartii apt.bona 18 7

Compsaraia cf. compsus com.comp 183 14

Magosternarchus duccis mag.ducc - 1

Magosternarchus raptor mag.rapt 11 -

Orthosternarchus tamanduá ort.tama 1 -

Parapteronotus hasemani par.hase 1 -

Pariosternarchus amazonenses par.amaz 10 -

Platyurosternarchus macrostomus pla.macr 1 -

Porotergus gimbeli por.gimb 47 -

Sternarchella calhamazon ste.calh 312 -

Sternarchella schotti ste.scho 2 2

Sternarchella terminalis ste.term 59 -

Sternarchogiton cf. preto ste.natt 1 -

Sternarchogiton nattereri ste.pret 182 5

Sternarchorhamphus muelleri ste.muel 52 50

Sternarchorhynchus chaoi ste.chao 2 -

Sternarchorhynchus cramptoni ste.cram 1 -

Sternarchorhynchus curvirostris ste.curv 1 7

Sternarchorhynchus goeldii ste.goel 4 -

Sternarchorhynchus mormyrus ste.morm - 2

Sternarchorhynchus oxyrhynchus ste.oxyr - 16

Sternarchorhynchus retzeri ste.retz 1 -

Hypopomidae Steatogenys elegans ste.eleg 128 74

Rhamphichthyidae Gymnorhamphichthys hypostomus gym.hypo 4 28

Rhamphichthys cf. lineatus rha.line 1 -

Rhamphichthys marmoratus rha.marm - 9

Rhamphichthys rostratus rha.rost - 1

Sternopygidae Distocyclus conirostris dis.coni 15 32

Eigenmannia limbata eig.limb 1 -

Eigenmannia macrops eig.macr 8 1337

Eigenmannia trilineata eig.tril - 5

Eigenmannia virescens eig.vire - 1

Rhabdolichops caviceps rha.cavi - 3

Rhabdolichops eastward rha.east 63 160

Rhabdolichops electrogrammus rha.elec 8 15

Rhabdolichops troscheli rha.tros - 71

Total specimens 1367 1909

Total species 31 24

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Table S3. Contribution of each functional trait to the first three axes of the Principal Coordinates Analysis.

Functional traits PC 1 PC 2 PC 3

Mass - 0.351 0.801 - 0.072

Oral-gape surface 0.452 0.688 - 0.320

Oral-gape shape - 0.838 - 0.193 0.277

Oral-gape position 0.872 0.282 - 0.060

Eye size 0.641 - 0.334 - 0.045

Eye position - 0.485 0.621 0.323

Body transversal

shape

- 0.493 - 0.114 0.122

Body transversal

surface

0.413 - 0.768 - 0.079

Pectoral-fin

position

- 0.804 - 0.005 - 0.319

Aspect ratio of the

pectoral-fin

0.203 - 0.487 0.579

Pectoral-fins

surface to body size

ratio

- 0.507 - 0.058 - 0.178

Anal-fin surface to

body size ratio

- 0.154 0.497 - 0.300

Snout length - 0.867 - 0.078 0.346