Ecologia trófica de anfíbios anuros:

Relações filogenéticas em diferentes escalas

Dissertação submetida para obtenção do título de Mestre em Ecologia

TALITA FERREIRA AMADO

Orientador: Adrian Antônio Garda

Co-orientador: Gabriel Corrêa Costa

Abril de 2014

UNIVERSIDADE FEDERAL DO RIO GRANDE DO NORTE

CENTRO DE BIOCIÊNCIAS

PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA

Catalogação da Publicação na Fonte. UFRN / Biblioteca Setorial do Centro de Biociências

Amado, Talita Ferreira.

Ecologia trófica de anfíbios anuros: relações filogenéticas em diferentes escalas / Talita Ferreira

Amado. – Natal, RN, 2014.

71 f.: il.

Orientador: Prof. Dr. Adrian Antônio Garda.

Coorientador: Prof. Dr. Gabriel Corrêa Costa.

Dissertação (Mestrado) – Universidade Federal do Rio Grande do Norte. Centro de Biociências.

Programa de Pós-Graduação em Ecologia.

1. Filogenia. – Dissertação. 2. Anfíbios. – Dissertação. 3. Métodos comparativos. – Dissertação. I.

Garda, Adrian Antônio. II. Costa, Gabriel Corrêa. III. Universidade Federal do Rio Grande do Norte. IV.

Título.

RN/UF/BSE-CB CDU 574

Dissertação realizada com o apoio da Coordenação de Aperfeiçoamento de

Pessoal de Nível Superior (CAPES) e aprovada junto ao Programa de Pós-Graduação

em Ecologia da Universidade do Rio Grande do Norte.

Comissão Examinadora:

Dra. Priscila Lemes de Azevedo Silva Universidade Federal de Goiás

Dr. Carlos Roberto Sorensen Dutra da Fonseca Universidade Federal do Rio Grande do Norte

Dr. Adrian Antônio Garda Universidade Federal do Rio Grande do Norte

Natal, 16 de abril de 2014

Prefácio Esta dissertação é resultado de dois anos de trabalho no Laboratório de Anfíbios

e Répteis- LAR, da Universidade Federal do Rio Grande do Norte. O projeto foi

supervisionado pelo Prof. Dr. Adrian Antônio Garda. Complementando minha

orientação, este trabalho contou com o auxílio do Prof. Dr. Gabriel Corrêa Costa no

debate teórico e analítico. Todos os custos da execução do projeto foram financiados

pela Coordenação de Aperfeiçoamento de Pessoal de Nível Superior- Capes.

A presente dissertação de mestrado consiste de duas partes: A primeira é uma

pequena introdução, em português, sobre os principais temas discutidos em ecologia de

comunidades. A segunda parte consiste em dois capítulos apresentados em forma de

manuscrito. Os manuscritos estão ainda em preparação para publicação e apresentam

uma edição básica em inglês.

Talita Ferreira Amado Natal, abril de 2014

Agradecimentos

Primeiro, eu gostaria de agradecer a Adrian Garda pela orientação nas ideias do

trabalho, por me acolher no laboratório, por criar no LAR um ambiente inspirador na

ciência e, principalmente, pela confiança no trabalho. Eu agradeço a Gabriel Costa pelas

ideias propostas no mestrado e pelo auxílio, quando necessário, prestado durante os dois

anos.

Agradeço, também, aos meus companheiros do LAR: Anne, Marcelo, Caicó

Pedro, Caicó Felipe, Will, Felipe Monitor, Felipe Caramujo, Thiago, Diego, Sarah,

David Lucas, Vinícius e Elianinha, pela excelente amizade, pelos momentos de risadas

no LAR e muita diversão ao longo desses dois anos. Também agradeço pela grande

ajuda inicial em campo e por me acolherem tão bem em Natal.

Um grande obrigado aos meus amigos da Ecologia, por fazerem das disciplinas e

das apresentações momentos inspiradores. Obrigado Tanquetão pela diversão sem fim,

pelos ensaios de apresentações e pela discussão acadêmica tão proveitosa.

Agradeço a minha família potiguar pelos momentos agradáveis sem os quais

seria impossível trabalhar, estudar e morar em Natal. Muito obrigada Marília, minha

parceira de surfe, pelas conversas e risadas com um toque de Alice e Lulu. Obrigada

Tida, por compartir comigo músicas, artes, pensamentos, falta de pensamentos, ciência

e alegria. Obrigada Clarinha por ser tão Pipoca! Obrigada Laurinha pelas aulas de

espanhol, aulas de disciplina e pela companhia nos momentos de crise criativa.

Gostaria de agradecer aos meus amigos de Brasília, por me acompanharem

durante a vida e me ajudarem a não ter medo de mudanças. Obrigada: Fernanda,

Thalitinha, Mariana, Maya Maia e Camila.

Agradeço muito a Pablo pelo suporte, amor e pela paciência constante.

Por último, agradeço a minha família: aos meus irmãos, Rafaella e Gabriel, pelo

companheirismo de sempre, a minha mãe Cleci pelo amor incondicional e ao meu pai

Alberto pelo amor e por me ensinar a questionar tudo.

SUMÁRIO

LISTA DE FIGURAS ...................................................................................................... i

LISTA DE TABELAS .................................................................................................... ii

RESUMO ........................................................................................................................ iii

ABSTRACT ................................................................................................................... iv

INTRODUÇÃO GERAL ............................................................................................... 2

1 Ecologia de Comunidades ......................................................................................... 3

1.1 Definindo Comunidades ...................................................................................... 4

1.2 Filogenia e Comunidades.................................................................................... 6

2 O Nicho Ecológico ..................................................................................................... 9

2.1 Nicho Grinnelliano .............................................................................................. 9

2.2 Nicho Eltoniano................................................................................................. 10

2.3 Nicho Fundamental e Realizado ....................................................................... 11

2.4 A Dieta como uma Dimensão do Nicho ............................................................ 12

3 A Distribuição Geográfica dos Anuros .................................................................... 13

Referências Bibliográficas .......................................................................................... 16

OBJETIVOS ................................................................................................................. 22

Objetivo Geral ............................................................................................................. 22

Objetivos Específicos ................................................................................................. 22

CAPÍTULO I

A hipótese Deep History e a dieta dos anuros ................................................................ 23

Abstract ....................................................................................................................... 24

Introduction ................................................................................................................. 25

Material and Methods ................................................................................................. 27

Results ......................................................................................................................... 29

Discussion ................................................................................................................... 30

References ................................................................................................................... 34

CAPÍTULO II

Largura de nicho, tamanho corporal e história evolutiva predizem a distribuição

geográfica dos anuros da Amazônia ............................................................................... 46

Abstract ....................................................................................................................... 47

Introduction ................................................................................................................. 48

Methods ...................................................................................................................... 51

Results ......................................................................................................................... 54

Discussion ................................................................................................................... 55

The relationship between niche breadth and geographical range ........................... 55

The relationship between body size and geographical range .................................. 57

The relationship between species age and geographical range ............................... 59

Conclusions ................................................................................................................. 60

References ................................................................................................................... 61

i

LISTA DE FIGURAS

Figura 1. As espécies em estudo pode ser dividas de acordo com 3 conjuntos: aquelas

definidas pela geografia, pela filogenia e pelos recursos que utilizam. As comunidades

são definidas pelas espécies encontradas em um determinado local. As interseções de

cada conjunto mostram como é definido cada

termo..................................................................................................................................4

CAPÍTULO I

Figura 1. Árvore filogenética com 148 espécies de sapos. Os números indicam o

ranqueamento dos oito clados que mais explicam a variância da dieta...........................41

Figura 2. Biplot de uma Análise de Correspondência Canônica (CCA) mostrando a

relação entre a filogenia (setas) e a dieta (losangos) dos sapos.......................................42

CAPÍTULO II

Figura 1. Árvore filogenética das 42 espécies de sapos amazônicos. A linha pontilhada

mostra o período de 30 milhões de anos..........................................................................64

Figura 2. Relação entre os contrastes do tamanho da distribuição geográfica e as

variáveis largura de nicho, tamanho corporal e tempo de divergência............................65

Figura 3. As duas árvores filogenéticas com a reconstrução do tamanho da área

geográfica e na largura de nicho......................................................................................66

ii

LISTA DE TABELAS

CAPÍTULO I

Tabela 1. Resultados da análise MANOVA não paramétrica da dieta de 148 espécies de

sapos representando os maiores clados...........................................................................40

CAPÍTULO II

Tabela 1. Resultados de uma análise de regressão filogenética das variáveis tamanho da

distribuição geográfica, largura de nicho e tamanho corporal. Os resultados estão

separados de acordo com o conjunto de dados utilizados...............................................63

iii

RESUMO

Entender a origem, manutenção e os mecanismos que operam na biodiversidade

atual são um dos principais objetivos da Ecologia. A ecologia das espécies pode ser

influenciada por diferentes fatores em diferentes escalas. Existem três abordagens a

cerca das diferenças ecológicas entre as espécies: a primeira traz essas diferenças

resultam de processos atuais atuando sobre as características do nicho (dieta, tempo,

espaço, etc); a segunda que divergências no nicho das espécies são explicadas por

padrões randômicos de especiação, dispersão e extinção; a terceira que eventos

históricos explicam a formação e a composição das espécies nas comunidades. Este

estudo tem como objetivo avaliar a influência das relações filogenéticas na

determinação de características ecológicas em anfíbios (globalmente) e testar, com isso,

se as diferenças ecológicas entre as espécies de anuros são resultado de diferenças

antigas pré-existentes ou como o resultado de interações ecológicas mais recentes.

Outro objetivo deste estudo é verificar que características ecológicas, históricas ou

atuais, determinam e influenciam o tamanho da distribuição geográfica das espécies. Os

dados de dieta para a análise da ecologia trófica dos anfíbios foram coletados a partir da

literatura já publicada. Realizamos uma MANOVA não paramétrica para testar a

existência de efeitos filogenéticos nas principais divergências na dieta dos anuros. Com

isso, espera-se conhecer os principais fatores que permitem a coexistência das espécies

de anfíbios anuros e quais os principais nós da filogenia de anfíbios responsáveis pelas

diferenças observadas atualmente no nicho trófico das espécies. Realizamos uma

regressão filogenética para analisar se as variáveis de largura de nicho, tamanho

corporal e tempo de divergência determinam o tamanho da distribuição geográfica dos

anfíbios anuros da Amazônia. Neste trabalho, novas contribuições ao conhecimento dos

padrões ecológicos apresentados pelos anuros são fornecidas e discutidas sob uma

perspectiva filogenética.

Palavras-chave: Deep history, dieta, filogenia, anfíbios, MANOVA, regressão

filogenética, distribuição geográfica

iv

ABSTRACT

Understand the origin, maintenance and the mechanisms that operate in the current

biodiversity is the major goal of ecology. Species ecology can be influenced by different

factors at different scales. There are three approaches about the ecological differences

between species: the first brings that differences result from current processes on niche

characteristics (e.g. diet, time, space); the second that species differences are explained

by random patterns of speciation, extinction and dispersion, the third that historical

events explain the formation and composition of species in communities. This study

aims to evaluate the influence of phylogenetic relationships in determining ecological

characteristics in amphibians (globally) and test with that, if ecological differences

between species of frogs are the result of ancient pre-existing differences or as result of

current interactions. Another objective of this study is to verify if ecological, historical

or current characteristics determine the size of species geographical distribution. The

diet data for analysis of trophic ecology were collected from published literature. We

performed a non-parametric MANOVA to test the existence of phylogenetic effects in

diet shifts on frogs history. Thus, it is expected to know the main factors that allow the

coexistence of anuran species. We performed a phylogenetic regression to analyze if

niche breadth, body size and evolutionary age variables determine the size of the

geographical distribution of amphibians in the Amazon. In the present study, new

contributions to knowledge of major ecological patterns of anurans are discussed under

a phylogenetic perspective.

Keywords: Deep history, diet, phylogeny, amphibians, nonparametric MANOVA,

phylogenetic regression, geographic distribution.

1

INTRODUÇÃO GERAL

O Sapo, Pablo Picasso. Litografia, 1949.

2

Introdução Geral

Os anfíbios constituem o grupo mais antigo de vertebrados terrestres e um dos

mais diversos (Vitt and Caldwell 2009). Suas particularidades fisiológicas e ecológicas

têm fascinado biólogos e naturalistas e, mais recentemente, despertou o interesse de

pessoas não ligadas à área científica (Wells 2010). A atual onda de interesse tem

começo em 1989 no I Congresso Mundial de Herpetologia, onde muitos pesquisadores

expuseram sua preocupação sobre um aparente declínio global das populações de

anfíbios (Collins and Storfer 2003). Hoje, existe um consenso de que as espécies de

anfíbios estão se extinguindo sob uma grande velocidade (Alford 2011). Desta forma, se

tornou crucial entender a ecologia destes animais e desenvolver planos para proteger sua

diversidade (Biek et al. 2002).

Já foram descritas mais de 7.000 espécies de anfíbios no mundo (Frost 2014)

divididas em 3 ordens: Anura (sapos, rãs e pererecas), Caudata (salamandras e tritões),

Gymnophiona (cecílias). Ocupam a maioria dos habitats terrestres, excetuando as

regiões polares e possuem um papel importante na dinâmica entre ambientes aquáticos e

terrestres (Wells 2010). Entretanto, o impacto humano tem causado uma das maiores

extinções na história da Terra (Collins and Storfer 2003). Em alguns casos este impacto

tem levado com que espécies aumentem sua distribuição geográfica, especialmente

aquelas que são facilitadas por estruturas feitas pelo homem e ambientes alterados

(Vitousek et al. 1997). Desta forma a ecologia, a biogeografia e mais recentemente a

macroecologia são consideradas por muitos biólogos as áreas mais desafiadoras da

biologia.

3

Anfíbios são excelentes modelos no desenvolvimento e teste de teorias

ecológicas (Wells 2010). A ordem anura, a mais diversa dentre os anfíbios, tem servido

como organismos modelo importantes em toda a história da ciência (Vitt and Caldwell

2009). Atualmente, o rápido avanço em análises filogenéticas resultou em hipóteses

filogenéticas mais robustas e confiáveis, o que desenvolveu o campo da ecologia

histórica (Cavender-Bares et al. 2009). Desta forma, novas teorias ecológicas podem ser

geradas e testadas, podendo identificar novos padrões ecológicos em grandes escalas

temporais e espaciais (Levin 1992). Da mesma forma, a disponibilidade de grandes

bancos de dados, a facilidade em se acessar esses dados por meio da internet e o

desenvolvimento de novas ferramentas (como a tecnologia baseada em GIS

[Geographic Information Systems]), tem facilitado grandes generalizações ecológicas e

a análise dos fatores que podem afetar os organismos em diferentes níveis de

organização (Pausas and Verdú 2010).

1 Ecologia de Comunidades

O principal objetivo da ecologia de comunidades é entender a origem,

manutenção e as conseqüências evolutivas da diversidade biológica (Cavender-Bares et

al. 2009). Diferentes processos, em diferentes escalas espaciais e temporais, podem

influenciar a composição e as interações das espécies em um ambiente (Levin 1992).

Processos evolutivos geram comunidades diferentes, mudando e substituindo as

espécies que as compõem (Ricklefs 1987). Processos ecológicos levam a facilitações e

exclusões das espécies exercendo uma forte influência na dinâmica da comunidade

(Pausas and Verdú 2010). Contudo, o termo “comunidade” possui diferentes conotações

para diferentes ecólogos. Dentro do mundo científico existe um debate sutil sobre a

4

natureza de uma comunidade, mas que promove avanços importantes na pesquisa dos

processos que a moldam (Morin 2011). Desta forma, torna-se importante definir uma

comunidade ecológica a fim de melhor desenvolver leis e teorias mais gerais em

ecologia (Looijen and Van Andel 1999).

1.1 Definindo Comunidades

Uma comunidade ecológica pode ser definida como uma parte do pool global de

espécies a ser encontrada em um determinado local (Looijen and Van Andel 1999). Esta

é uma definição síntese paras os diferentes agrupamentos de espécies que coexistem e

termos chaves são utilizados como sinônimos na ecologia de comunidades:

“comunidade”, “guilda”, “assembleia” e “taxocenose”. Mas, cada termo representa

jeitos distintos que pesquisadores limitam os organismos que estudam. Fauth et al.

(1996) usa um digrama de Venn para distinguir e definir os termos ecológicos em

comunidades (Figura 1).

BA

C

Figura 1. As espécies em estudo pode ser dividas de acordo com 3 conjuntos: aquelas

definidas pela geografia, pela filogenia e pelos recursos que utilizam. As comunidades são

definidas pelas espécies encontradas em um determinado local. As interseções de cada

conjunto mostram como é definido cada termo. (Adaptado de Fauth et al. 1996)

5

No Conjunto A estão as comunidades ecológicas, estas são definidas por grupos

de espécies que coexistem ao mesmo tempo no mesmo lugar. Esta é a definição mais

comum, porém não é a única. As comunidades podem ser facilmente demarcadas de

acordo com o objetivo do pesquisador. O que diferencia uma comunidade da outras são

seus limites (Looijen and Van Andel 1999). Mas, em todo caso a fronteira de uma

comunidade foco é na maioria das vezes arbitrária e o objetivo é construir uma

comunidade de estudo que não esteja limitada pela filogenia ou pelo uso de recursos

(Fauth et al. 1996). Para outros casos, quando se necessita de um limite mais claro dos

organismos de estudo, é preciso utilizar termos mais precisos.

As guildas são definidas pelos recursos que consomem ou pela forma em que

consomem. Both et al. (2011) analisam se as guildas de girinos no sul do Brasil revelam

um padrão de segregação dos girinos. Os autores distinguem as espécies em 4 guildas

ecomorfológicas: bentônicos, nectônicos, raspadores de suspensão e filtradores de

suspensão. Esse tipo de separação das espécies ainda pode ser mais específico ao

inserirmos a variável espacial. Guildas locais surgem a partir do intercepto entre os

conjuntos A e B. Essa delimitação é ideal para pesquisas descritivas sobre hábitos

alimentares e, também, sobre interações interespecíficas, como competição.

O último conjunto constitui grupos filogeneticamente relacionados dentro das

comunidades. Este conjunto contém unidades taxonômicas que possuem uma

proximidade devido um ancestral comum. A própria definição de comunidades de

anfíbios contém um caráter filogenético. Mas, o uso da filogenia em estudos ecológicos

surgiu recentemente, como também os termos e definições relacionados a ela. Grupos

relacionados filogeneticamente e que coexistem em um mesmo local constituem

“assembleias”. Estudos com assembleias investigam mais diretamente a influencia de

fatores bióticos e abióticos que pressionam as espécies. Por exemplo, Vasconcelos et al.

6

(2011) avalia a distribuição de assembleias de girinos em Mata Atlântica do sudeste do

Brasil. Nessas assembleias a partição do espaço pareceu ser mais importante para

permitir que as espécies coexistam. Muitas espécies que possuem características

ecológicas e biológicas semelhantes segregam na utilização de recurso, espaço e habitat

a fim de evitar fortes pressões nas populações. Características essas que podem ser um

reflexo evolutivo inerentes destas espécies.

Esses diferentes recortes de uma comunidade ecológica proporcionam aos

ecólogos diferentes meios de se estudar uma comunidade. Seja em escala local ou

global, as causas que levam a coexistência de espécies são muitas. Entender os fatores

que permitem que diferentes organismos existam em um local possui um caráter

conservacionista da diversidade. Entender a estrutura de uma comunidade pode revelar

mais sobre a biodiversidade de um local e como essa diversidade interage com o meio.

Mas, principalmente, entender as diferenças ecológicas que levam à coexistência das

espécies presentes em uma comunidade é crítico para se manejar e restaurar a biota de

uma região. Para fins desse trabalho, uma comunidade ecológica será definida como

uma fração do total global de espécies. Desta forma, a ecologia dessa comunidade irá

incluir o estudo dos padrões e processos que envolvem mais de uma espécie em uma

escala regional e global.

1.2 Filogenia e Comunidades

Os processos evolutivos nas comunidades atuam de forma que estas não

permanecem estáveis ao longo do tempo. Os eventos de especiação e adaptação geram

espécies diferentes e a diversidade aumenta ou diminui dependendo do evento (Johnson

and Stinchcombe 2007). A relação histórica entre as espécies que fazem parte de uma

comunidade deixa traços que podemos utilizar para melhor entender a evolução de um

7

conjunto de organismos (Cavender-Bares et al. 2009). Essa abordagem tem sido

facilitada e melhorada pela rápida expansão de informações filogenéticas e ferramentas

computacionais (Cavender-Bares et al. 2009). O aumento do interesse sobre o papel da

história na ecologia e a relação filogenética entre os organismos traz uma nova

dimensão de informação para entender por que diferentes espécies ocupam ou não um

mesmo espaço (Pausas and Verdú 2010). A filogenia ajuda a entender e identificar o

papel de processos neutros e os relacionados com o nicho na dinâmica das comunidades

naturais, pois dados biológicos e ecológicos isolados não suportam hipóteses que

explicam os padrões observados (Ricklefs 1987).

Existem três abordagens a cerca da dinâmica e manutenção de

comunidades. A primeira traz que uma comunidade é estruturada através de processos

relacionados ao nicho, que seguem regras determinadas pelo ambiente e a competição

por recursos (Connor and Simberloff 2007). A segunda, uma resposta a este

pensamento, é a Teoria Neutra (Hubbell 2001), que afirma que a abundância e a riqueza

de espécies são explicadas por padrões randômicos de dispersão, extinção e especiação

na comunidade, e que as espécies que compõem uma determinada comunidade são

equivalentes. Uma terceira perspectiva destaca a importância de fatores históricos na

formação das comunidades. Nesta, as condições iniciais e eventos de especiação e

dispersão importam mais do que processos locais (Ricklefs 1987).

A ideia de que a história evolutiva tem um papel na ecologia das comunidades

atuais possui um longo histórico dentro do debate científico (Morin 2011). A maioria

dos estudos ecológicos ignora os dados genéticos que diferenciam as unidades

biológicas dentro de cada escala ecológica estudada (Connor and Simberloff 2007). Em

contrapartida, a biologia evolutiva considera como a variação genética leva a mudanças

genéticas e fenotípicas dentro de populações (Gotelli 2007). Assim, existe uma forte

8

tendência em trabalhos evolutivos em investigar como os fatores ecológicos afetam a

evolução (Hairston et al. 2005). Ao unir essas duas vertentes biológicas em um único

estudo é possível ter novas visões sobre questões tipicamente feitas por ecologistas

(Hairston et al. 2005). Ao analisarmos uma comunidade, dado o ancestral comum entre

as espécies que a compõem e se existe uma tendência a conservatismo de nicho

filogenético, é possível observar relações entre a proximidade filogenética e

características ecológicas (Wiens 2011). Desta forma, se as espécies se encontram

próximas ou distantes filogeneticamente, podemos inferir quais pressões, atuais ou

passadas, levaram a tal padrão (Wiens and Graham 2005). Entretanto, uma perspectiva

mais clássica assume que as comunidades ecológicas são governadas por processos

relacionados ao nicho (Gotelli et al. 2007).

As diferentes dimensões do nicho de uma espécie podem ser estudadas a fim de

se compreender as interações, ocupação do espaço e atividade de um organismo

(Leibold and Jul 2007). Uma dessas dimensões, o habitat, é conhecido por determinar a

distribuição e o comportamento de indivíduos (Begon et al. 2006). A forma como um

ser-vivo utiliza o seu habitat e os locais que ele ocupa tem efeito na composição das

espécies de uma área e na relação dessas espécies entre si (Garda et al. 2012). Em uma

grande escala, uma espécie ocupa um habitat se este possui as condições e os recursos

que permitem a ocupação do espaço físico (Ricklefs 1987). Isto influencia diretamente

no tamanho e na localização da área que uma ou mais espécies ocuparão (Brown et al.

1996). Portanto, analisar a relação do nicho com a história evolutiva de uma

comunidade ilumina o entendimento da biodiversidade global (Soberon and Peterson

2005). Entretanto, antes é preciso entender a natureza do nicho ecológico das espécies.

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2 O Nicho Ecológico

Nicho ecológico é um termo geralmente utilizado como a posição de uma

espécie dentro de um ecossistema (Ricklefs 2003). O nicho descreve o leque de

condições e recursos necessários para persistência dos indivíduos desta espécie, bem

como seu papel dentro do ecossistema (Begon et al. 2006). Portanto, uma separação

distinta do organismo com o seu ambiente torna-se um desafio (Dray and Legendre

2008). Consequentemente, a primeira formulação do conceito de nicho tem ênfase no

ambiente habitado pela espécie (Leibold and Jul 2007). Uma segunda tentativa em

conceituar nicho dá ênfase no papel funcional da espécie, onde esta altera e não apenas

ocupa o ambiente (Polechová and Storch 1989). Contudo, o conceito de nicho possui

dois lados: um em relação aos efeitos que o ambiente tem sobre as espécies, o outro em

relação aos efeitos que as espécies têm sobre o ambiente (Severtsov 2013). Como na

maioria dos objetos de estudo da ecologia, ambos os pensamentos estão de alguma

forma misturados.

2.1 Nicho Grinnelliano

O conceito inicial de nicho vem da arquitetura, o que significa um pequeno

espaço na parede para abrigar uma estátua (Frankl 2000). Esta definição não se desvia

muito da definição cunhada por Joseph Grinnell em 1917. Em seu artigo “The niche

relationships of the California Thrasher”, Grinnell caracteriza o nicho como o habitat

no qual uma espécie vive. Ele se interessava principalmente em quais fatores

determinam onde encontramos uma espécie e em como o nicho é preenchido pelos

indivíduos desta espécie. Este espaço ecológico é ocupado de acordo com os

requerimentos abióticos, preferências alimentares, características do habitat e prevenção

da predação (Polechová and Storch 1989).

10

Esta perspectiva permite a existência de nichos „vagos‟, ou seja, espaços

ecológicos equivalentes e que não foram ocupados por nenhuma espécie (Lekevičius

2009). A questão sobre o que significa um nicho vago ou se este realmente existe no

ecossistema ainda é controversa (Polechová and Storch 1989). O debate ainda é mais

complexo quando se questiona se ecossistemas podem atingir um equilíbrio, onde estes

podem ficar saturados de espécies (Walker and Valentine 1984). Este princípio tem

forte conseqüência quando pensamos na distribuição geográfica das espécies. A idéia de

que o nicho é determinado pela soma dos requerimentos do habitat é essencial para

entender e prever a área ocupada por uma espécie e ainda se esta se expande (Brown et

al. 1996).

2.2 Nicho Eltoniano

Neste conceito, cada espécie possui um papel no funcionamento e na dinâmica

do ecossistema (Elton 1927). Da mesma forma que o nicho Grinnelliano, o nicho

proposto por Charles Elton (1927) pode ser preenchido por espécies equivalentes

quando o nicho encontra-se vago (Severtsov 2013). Esta idéia surge da observação de

espécies distantes filogeneticamente, mas que possuem papéis ecologicamente

equivalentes (Begon et al. 2006). Desta forma, existe um nicho para detritívoros, os

limpadores de parasitas, polinizadores, predadores e demais funções correspondentes à

posição trófica de um organismo. Esta abordagem é a forma mais direta de descrever as

necessidades de recursos de uma espécie, ao focar nos hábitos alimentares (Levin 1992).

Desta forma, é uma definição importante quando se quer estudar ecologia espacial e sua

dinâmica.

11

2.3 Nicho Fundamental e Realizado

Hutchinson reconhece o nicho ecológico como multidimensional, onde cada

dimensão representa as condições e os recursos que cada indivíduo de uma espécie

necessita para sobreviver (Hutchinson 1957). Contudo, Hutchinson reconhece que os

indivíduos não são unidades isoladas de outros indivíduos. A presença de interações

inter e intraespecíficas (e.g. competição, predação, facilitação) interferirá na forma

como a espécie consome os recursos e ocupa espaços (Connor and Simberloff 2007).

Um organismo livre de interferência de outras espécies poderá usufruir das

diferentes dimensões de seu nicho em sua totalidade. Essa é a definição básica de nicho

fundamental, onde descreve a potencialidade das espécies de ocuparem todo o nicho.

O nicho de uma espécie é formado desde que essa mesma espécie surge (Peterson

1999). Assim, os limites do nicho são determinados pelo grau de tolerância e resistência

dos indivíduos (Severtsov 2013). Entretanto, pressões e interações com outros

organismos força com que uma espécie ocupe um nicho menor do que o seu (Greene

and Jaksić 1983). Desta forma, a espécie está restrita a porções do seu nicho onde ela é

mais adaptada, ocupando um nicho realizado (Wiens 2011).

De acordo com Hutchinson, diferentes espécies não podem ocupar o mesmo

nicho, o que é diferente da idéia concebida por Grinnell. Isso se deve, pois o nicho é

uma fração do espaço ecológico específica de uma única espécie, com um conjunto de

dimensões parecidas, mas diferentes espécies se diferenciarão em pelo menos uma

dimensão (Wiens 2011).

Devido à complexidade da natureza do nicho, se torna difícil descrever

apropriadamente o nicho de uma espécie (Nakazawa 2013). O número de dimensões do

nicho é potencialmente infinito e os eixos significantes são difíceis de achar (Jackson et

12

al. 2009). Contudo, algumas variáveis são suficientes para separar o nicho de diferentes

espécies e a dieta, ou o comportamento alimentar, é uma delas.

2.4 A Dieta como uma Dimensão do Nicho

Todos os organismos requerem energia para manterem sua organização corporal

complexa ou simples (Begon et al. 2006). Esta energia possui uma natureza química,

liberada através da transformação de compostos complexos em outros mais simples

(Ricklefs 2003). Os vertebrados dependem dos compostos orgânicos originários de

outros seres vivos e isto possui um grande impacto na sua ecologia (Begon et al. 2006).

O alimento consumido por uma espécie reflete suas preferências de habitat, suas

relações com outras espécies, sua zona geográfica habitada, seu estágio na história de

vida e também sua história evolutiva (Vitt and Caldwell 2009). Portanto, os hábitos

alimentares de um organismo descrevem uma dimensão do seu nicho e com eles

podemos estabelecer relações com outras variáveis biológicas de interesse (Wells 2010).

Espécies simpátricas, próximas filogeneticamente, tendem a se diferenciar

ecologicamente a fim de minimizar competição pelo recurso limitado, ou pelo acesso a

esse recurso (Greene and Jaksić 1983). Com isso, diferentes estratégias adaptativas ou o

uso diferenciado de alguma dimensão do nicho (e.g. espacial, temporal, alimentar) são

observados (Connor and Simberloff 2007). Por outro lado, a diferenciação das

dimensões do nicho pode ser devido às competições passadas (Vitt and Pianka 2005).

Assim, essas espécies apresentam comportamento de acordo com a maior separação de

seus nichos, e não devido à presença de competição atual (Colston et al. 2010).

Portanto, ao lidar com mecanismos de coexistência e diferenciações ecológicas, um

pesquisador deve também olhar a história da espécie de interesse.

13

A dieta dos sapos é composta principalmente por pequenos invertebrados,

pequenos vertebrados e também partes de plantas (Vitt and Caldwell 2009). Devido à

alta diversidade e abundância dos indivíduos deste grupo, o impacto destes sobre outras

espécies animais e vegetais é grande e o consumo destas pelos anuros dependerá de

diferentes fatores (Wells 2010). Na natureza, os sapos possuem um amplo espectro de

itens alimentares para consumirem, contudo, eles não consomem todos (Abbey-Lee

2012). Uma espécie consome uma parte do pool geral de itens alimentares disponíveis e

a dieta dos indivíduos reflete a dieta geral da espécie (Colwell and Futuyma 1971).

Assim, mesmo que duas espécies ocorram em um mesmo habitat, estas podem

apresentar dietas muito diferentes (Cáceres and Machado 2013). Mesmo entre os

indivíduos de uma mesma espécie os tipos de itens alimentares não são os mesmos

(Araújo and Bolnick 2009). Muitos cientistas agregam este fenômeno à competição

histórica ou recente, o que leva à diferenciação entre espécies (Connor and Simberloff

2007). Contudo, esta variação também pode ser conseqüência da especialização de

algumas espécies a determinados itens (Araújo et al. 2011). Isto ilustra os obstáculos em

se trabalhar com o nicho ecológico. Apesar de complexo e de difícil mensuração, as

dimensões do nicho devem ser acessadas, analisadas e utilizadas em trabalhos

ecológicos e a dieta é uma delas (Bolnick et al. 2011).

3 A Distribuição Geográfica dos Anuros

Anfíbios anuros são dependentes de condições ambientais úmidas, temperaturas

relativamente altas e disponibilidade de água para a reprodução e desenvolvimento de

girinos (Vitt and Caldwell 2009). Muitas das espécies que coexistem em um mesmo

local ainda enfrentam outros fatores que poderiam limitar sua distribuição (Wiens

14

2007). Em uma escala global e regional, a distribuição dos anfíbios tem pouca relação

com interações com outras espécies, mas possui uma forte relação com eventos

históricos e com a estrutura da paisagem e do clima (Wells 2010).

Em geral, os anuros apresentam uma tendência latitudinal do padrão de riqueza e

a maior parte das espécies se encontra na região tropical, essa riqueza diminui ao nos

aproximarmos dos pólos (Olalla-Tárraga et al. 2011). Isso é verdadeiro para boa parte

dos vertebrados ectotérmicos e anfíbios apresentam uma mistura entre fatores regionais,

ecológicos e históricos que influenciam a abundância e riqueza de suas espécies (Wiens

2007). Muitos trabalhos encontraram fortes correlações desses padrões de distribuição

com fatores ambientais e, com isso, consideram os fatores climáticos como a principal

explicação (Morin 2011). Mas, ainda é difícil um consenso na comunidade científica

diante das inúmeras hipóteses sobre o gradiente latitudinal.

Com exceção de alguns táxons (e.g. gramíneas), a diversidade declina do

equador aos pólos (Rohde 2007). Uma das hipóteses propostas para explicar esse

padrão é a de energia (cita). Esta hipótese considera que a produtividade primária limita

a quantidade de espécies encontradas na região (Begon et al. 2006). Portanto, a

densidade de indivíduos deve ser maior em lugares quentes e úmidos, onde existe uma

maior produtividade (Rohde 2007). Entretanto, outra ideia assume que a riqueza

encontrada em uma região é derivada da capacidade das espécies de persistirem no

ambiente (Mittelbach et al. 2007). Em regiões tropicais a variação de variáveis

ambientais (e.g temperatura), é menor do que em regiões temperadas (Morin 2011).

Com isso, apenas espécies tolerantes a grandes variações ambientais estariam presentes

em tais regiões (Begon et al. 2006). Uma última hipótese (diversificação evolucionária)

sugere que a taxa de evolução é maior em locais com maior temperatura, o que remete

às outras duas teorias (Mittelbach et al. 2007). Essa taxa de evolução é devido a

15

gerações mais curtas, mutações mais frequentes, processos fisiológicos mais rápidos

(Wiens 2007). Desta forma, uma maior taxa de especiação deve ser encontrada também

em ambientes mais quentes (Mittelbach et al. 2007). Contudo, por volta dos anos 90,

muitos ecologistas convergiram para uma mesma idéia: a hipótese do conservatismo

tropical.

A hipótese do conservatismo tropical assume que espécies de clados muito

diversos se originaram nos trópicos e apenas algumas dessas espécies conseguiram

dispersar até as zonas temperadas (Wiens and Donoghue 2004). Mais ainda, a dispersão

entre as regiões tropicais e temperadas estaria limitada pela diferenciação de algumas

linhagens a determinados regimes de clima, conhecido como conservatismo de nicho

(Wiens and Graham 2005). O conservatismo de nicho é a tendência geral das espécies

de manterem características de nicho de um ancestral comum (Peterson 1999). Outra

idéia dessa hipótese é de que simplesmente a região tropical aporta mais espécies, pois

foi uma região mais extensa por mais tempo (Behrensmeyer 1992). Esta última

afirmação é sustentada pela biogeografia de ilhas, onde a riqueza de espécies aumenta

com o aumento da área geográfica (MacArthur and Wilson 1967).

Para anfíbios o padrão de distribuição de riqueza e abundância parece estar mais

relacionado com as altas taxas de extinção das áreas temperadas, apesar de que também

possa ser causado por maiores taxas de especiação nos trópicos (Wiens 2007). Esta

afirmação não é muito surpreendente, já que as temperaturas relativamente constantes e

o clima úmido dos habitats tropicais são adequados para os anfíbios (Vitt and Caldwell

2009). Em ambas as regiões, temperada e tropical, a diversidade de anfíbios é

fortemente influenciada pelo regime de chuvas e outros fatores abióticos (Wells 2010).

16

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OBJETIVOS

Objetivo Geral Avaliar a influência das relações filogenéticas na determinação de

características ecológicas em anuros (globalmente) e em anuros amazônicos

(regionalmente) e testar, com isso, se as diferenças ecológicas entre as espécies são

decorrentes de diferenças antigas pré-existentes ou como o resultado de interações

ecológicas mais recentes e quais variáveis afetam a distribuição geográfica das espécies.

Objetivos Específicos

Compilar, a partir de dados da literatura, uma base de dados global da dieta de

anfíbios anuros e testar a correlação entre duas matrizes, uma de relações

filogenéticas e outra de outra de dieta, para avaliar se as diferenças observadas

se devem a fatores recentes (interações ecológicas) ou mais antigos (hipótese do

"Deep History");

Observar se a hipótese Deep History é sustentada para os dados alimentares dos

anfíbios.

Analisar a partir de dados de dieta de espécies amazônicas se a largura do nicho

trófico afeta o tamanho da área de distribuição das espécies de anuros.

Testar se espécies com ampla distribuição possuem maior tamanho corporal e

maior tempo de divergência.

23

CAPÍTULO I

A hipótese Deep History e a dieta dos

anuros

Manuscrito sob preparação

1. Sapo mumificado, Maurits Cornelis Escher. Mezzo tinta sobre

papel, 1985.

24

DIET OF AMPHIBIANS AND THE DEEP HISTORY HYPOTHESIS

Talita Ferreira Amado

Laboratório de Anfíbios e Répteis, DBEZ- Centro de Biociências, Universidade Federal do Rio

Grande do Norte

Pablo Ariel Martinez

Laboratório de Macroecologia, DECOL- Centro de Biociências, Universidade Federal do Rio

Grande do Norte

Gabriel Corrêa Costa

Laboratório de Macroecologia, DECOL- Centro de Biociências, Universidade Federal do Rio

Grande do Norte

Adrian Antonio Garda

Laboratório de Anfíbios e Répteis, DBEZ- Centro de Biociências, Universidade Federal do Rio

Grande do Norte

*Corresponding author: amadotalita@gmail.com

ABSTRACT

Similar species in ecological communities compete for limited resources and

coexistence is achieved through the divergence of ecological niches. For more than half

century, species interactions were believed to be the sole cause of shifts in resource use

and conditions for occupancy. In the past two decades, the availability of well-resolved

phylogenies has made it possible to incorporate and test the effect of evolutionary

history in several biological phenomena. As a result, the deep history hypothesis as

formulated as an alternative to current species interactions. According to this

hypothesis, ecological differences between species in present-day communities emerged

in older clades in the evolutionary history of these species. In the present study we test

the deep history hypothesis along one niche axis, diet, using frogs as a model clade. We

used a diet dataset compiled from early-published works with frogs around the world

(149 species) and a new large-scale phylogeny of amphibians. In the evolutionary

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history of frogs, the dietary divergence is dispersed over the phylogeny, with major

shifts not restricted to deep branches. The most divergent node (giving rise to Hylidae)

accounted for almost 6% of the divergence explained by our data. The arboreal habit of

this family is correlated with diet, with many species consuming available and

camouflaged arthropods in the foliage. Nevertheless, major dietary shifts are

distributed along frogs' evolutionary history, showing an alternative scenario to deep

history hypothesis. However, it is not clear how competition, predation, and other

ecological interactions have shaped the shifts identified by our analysis.

Keywords: phylogeny, amphibians, diet, community ecology, nonparametric

MANOVA

INTRODUCTION

Ecological divergence contributes to the origin and maintenance of biodiversity

(Schluter 2009). The evolution of key ecological traits gives new lineages access to

adaptive zones, which influences diversification, long-term persistence, and coexistence

by allowing the use of different resources and minimizing interactions between

sympatric and closely-related species (Kozak et al. 2005, Toft 1985). Similar species

competing for a limited resource will affect the stability of an ecological community

(Morin 2011). Thus, persistence and coexistence are obtained through the divergence of

ecological niches (Bastolla and Lässig 2005), and ecological niche differentiation was

for a long time considered the fundamental factor explaining the maintenance of

biological diversity (Chesson 2000).

For more than a half century, species interactions were considered the key to

explain how communities function and how they are structured (Morin 2011).

Competition, predation, and other interactions were believed to cause shifts in resource

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use and conditions for occupancy (Stokstad 2009). According to this species interaction

hypothesis, differences between species in recent communities are driven by current

ecological interactions (Hutchinson 1957, Wiens 2011). This idea was supported by

experiments with introduction of similar species into communities that resulted in a

shift in some ecological trait (e.g. diets, microhabitat use, daily activity patterns, (Toft

1985). However, these changes were usually small because they occur in a small

temporal scale (Levin 1992, Vitt and Pianka 2005). Conversely, significant differences

in species niches can be derived from past events (e.g. past pressures of competition)

instead of current interactions, in which case ecological differences are expected to be

more profound (Connell 1980). Testing alternative hypothesis to the species interaction

hypothesis has recently become possible with the advent of phylogenetic comparative

analyses and large-scale, well supported phylogenetic hypotheses (Johnson and

Stinchcombe 2007, Cavender-Bares et al. 2009).

The deep history hypothesis posits that ecological differences between species in

present day communities emerged in older clades in the evolutionary history of these

species (Connell 1980, Vitt et al. 1999, Vitt and Pianka 2005). In species that compete

for specific food resources, for example, chances for niche differentiation are limited

(Chesson 2000). If one of these species is a superior competitor, the stability of

communities is affected (Gause 1934). However, if different lineages are superior

competitors in different resources, then competing species will the able to coexist

(Connell 1980). Hence, current species coexist by maintaining differences from

ancestors (Bastolla et al. 2008). This hypothesis is consistent with the niche

conservatism hypothesis, which states the species tendency to retain aspects of ancestral

niche over a long evolutionary timescale (Ackerly 2003, Wiens and Graham 2005).

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Thus, past events may influence the ecology of current species and these modifications

are maintained (Vitt and Pianka 2005, Colston et al. 2010).

Most anuran amphibians are sit-and-wait foragers and, as adults, feed almost

exclusively on invertebrates (Vitt and Caldwell 2009). Frogs use visual ability to detect

moving prey and they feed on a wide diversity of available food (Stebbins and Cohen

1997). However, frogs do not consume available food items randomly, instead they

select specific prey and the diet usually reflects morphological and behavior adaptations

(Wells 2010). Morphological constrains limit frogs' diets, and frogs prey selection has

been anecdotally defined by the phrase "they will eat mostly what fits in their mouth"

(Toft 1980). Furthermore, dietary variation in frogs is also correlated with taxonomic

groups (Toft 1981). This phylogenetic signal may support the deep history hypothesis

because deep dietary divergences are unlikely to have evolved recently (Hairston et al.

2005).

In this article, we test the deep history hypothesis in Anura. We evaluate where

major shifts in diet have occurred, evaluating if trophic niche partition in most anuran

communities is due to ecological interactions or past selective forces. Here we used a

diet dataset compiled from early-published works with frogs around the world (149

species). To test the deep history hypothesis we use a new large-scale phylogeny of

amphibian species and we test two predictions of this hypothesis: (i) the first is that the

diets must be correlated with frogs‟ phylogeny, (ii) the second is that major clades that

are consistent with the phylogenetic history of frogs should be identified.

MATERIAL AND METHODS

FROGS DIET – We collected diet data of 149 frogs from available literature (Appendix

S1). To better access published works we conducted searches in distinct sources: Web

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of Knowledge, Zoological Records, Google Scholar, and also contacted authors and

specialists. Nevertheless, for some clades we found no published information on diet

(e.g. Centrolenidae species). We collected the diet description from studies of different

parts of the world and used prey categories to access the dietary shifts in frogs‟ diets.

Some studies identify prey to species, but others only report major categories (e.g. ants,

beetles, spiders). Thus, we chose to classify prey into biological order or broader

categories. Not all the published papers supply quantitative measures of prey

proportions, but only inform the prey types consumed. We chose to use the presence or

absence of prey categories in species diets to construct a diet matrix because of the great

variation in diet data. By doing this, we have a data with less resolution, but we were

able to incorporate more different species in our analyses.

STATISTICAL ANALYSIS− To test the association between phylogenetic history and

anuran diets, we performed a nonparametric multivariate analysis of covariance

(MANCOVA) (Anderson 2001). The nonparametric MANCOVA is a statistical method

for comparing multivariate values (prey items) for several groups (clades). This method

is robust and lacks formal assumptions concerning distribution of variables. The

significance of the dietary niches differences is given by F-tests based on sequential

sums of square from permutations of the raw data.

We constructed a diet matrix and a phylogenetic matrix with presence/absence

data. To construct these matrices we used a large-scale phylogeny of Amphibia (Pyron

and Wiens 2011), pruning the original phylogeny to include only the species present in

our data using the R package “ape” (Paradis et al. 2014). In the matrices „1‟ indicates

presence and „0‟ indicates absence of prey items (diet matrix) or presence and absence

of species in phylogenetic clades in the phylogenetic matrix. Because prey type and size

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are often influenced by frog's body size, we used maximum snout-vent length reported

for each species as a covariate. Permutation tests were performed on phylogenic clade

representations using 9999 permutations. We tested each clade manually to obtain F and

P values. To verify whether main dietary divergences occurred in ancient clades we

rank the chosen nodes by the determination coefficient, with the first node having the

higher coefficient. We performed the analysis in vegan package for R version 3.0.2

(Oksanen et al. 2013).

CCA BIPLOT- To best represent the correlation between diet and phylogenetic

variables we construct an exploratory graph of canonical correspondence analysis

(CCA). A biplot allows the display of both diet and phylogenetic information, showing

associations between nodes and prey items. To construct this type of graphic we used

the same matrices used in nonparametric MANCOVA. We perform the CCA biplot in

vegan package for R environment (Oksanen et al. 2013).

RESULTS

Frog species used in our analysis ate a great variety of prey. We identified 35

discrete prey categories: acarina, annelida, arachnida, blattaria, coleoptera, crustacea,

dermaptera, diptera, ephemeroptera, formicidae, gastropoda, hemiptera, hymenoptera,

isoptera, lepidoptera, mantodea, mollusca, myriapoda, nematoda, neuroptera, odonata,

oligochaeta, opiliones, orthoptera, other invertebrate, vertebrates, plecoptera,

pseudoscorpionida, psocoptera, thysanoptera, tricoptera, invertebrate eggs, invertebrate

larvae, other invertebrates, and plant parts. All clades consume invertebrates, and some

also consume small vertebrates such as other frogs, small birds, bats, and snakes. The

most specialist clade was Aromobatidae, which eat mostly ants (Fig. 2).

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In the evolutionary history of frogs, the dietary divergence is dispersed over the

phylogeny, with major shifts not restricted to deep branches (Fig. 1). The most

divergent node (giving rise to Hylidae) accounted for almost 6% of the divergence

explained by our data (Table 1). Hylidae has a diet rich in spiders, dragonflies, and

crickets (Fig. 2). The second most significant node is the one giving rise to

Aromobatidae (arrow number 3 in Fig. 2), occupying the opposite extreme of CCA axes

with, a diet consisting mainly of ants. The next five nodes that contribute for significant

divergences in diets consist of a complex of frog families whose diet is similar to

Hylidae (Fig. 2, Table 1).

Despite the low coefficient of determination (the highest R2 was 0.058),

differences in frogs‟ diets species are significantly associated with phylogeny (Table 1).

However, our results show that dietary divergence is distributed throughout the

evolutionary history of Anura. The group that comprises Ranidae and Mantellidae

families has the most diverse diets, the only group on our dataset that ate vertebrates.

However, the species that occur in this group separate in other niche axes (they have

different habits, behavior and adaptations). Maybe, the node that mainly explains major

divergences in diets of frogs give rise to Aromobatidae and Dendrobatidae. Those two

families differ from each other by the ability to produce poison (dendrobatids produce

toxic skin alkaloids derived from arthropod prey items). However, both families are ant

specialists, which differ from the other clades present in the phylogeny.

DISCUSSION

Significant shifts in frog‟s diets occurred along all the evolutionary history of this

group. This contrasts with what is described for squamates (Vitt and Pianka 2005) and

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snakes (Colston et al. 2010), in which the major part of dietary divergence occurred

early in the evolutionary history. Within Anura, changes in diet are shallow in a

phylogenetic sense. Hylid frogs have diverged during the Cretaceous (~74 Ma), which

is relatively recent compared to anuran evolutionary history (Anura rise as a

monophyletic group in the late Triassic, ~225.5 million years ago, Pyron 2011).

While most frogs are generalists, some specialize on particular types of prey. About

all frogs are insectivorous or carnivorous as adult, although there are some cases of

frugivory in hylid frog species (Silva et al. 1989). This may explain the presence of

plants part in frogs diets of our dataset, on which the Hylidae family is associate.

However, an evidence of adaptations for herbivory is unknown and much of the

taxonomic composition in preys depending mainly on body size and microhabitat use

(Stebbins and Cohen 1997). For several authors, (Hutchinson 1957, Schoener 1974,

Costa et al. 2008) differences in many biological traits (body size, skull size, and visual

accuracy) have been interpreted as evolutionary response that allows species to

minimize interactions. While the body and skull sizes may be the main cause behind the

dietary divergence in frogs, part of those differences are echoes of major divergences

that occurred in frogs evolutionary history. This last statement is corroborated by our

results because the main divergence in frog diet is consistent with one phylogenetic

group of tree frogs.

The more important dietary divergence occurred in the family Hylidae. The arboreal

habit of this family is correlated with diet, with many species consuming available and

camouflaged arthropods in the foliage (Parmelee 1999). Indeed, our data show that the

items more associated with arboreal habits like mantises, crickets, and spiders. In the

Green Treefrog (Hyla cinerea), for example, the response to presence of a prey is faster

if the prey is close to frog (Freed 1982). Freed (1982), found that prey size, shape, and

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distance at the time of detection is positively correlated with the feeding response by

Green Treefrog. One other study suggests that prey selection is related to prey activity

in hylid frogs, with the most active prey being the most frequently eaten by sit and wait

foragers (Menin et al. 2005). Therefore, due to the arboreal habit of treefrogs the preys

that this type of anuran will consume are more likely to be arboreal prey.

Diet differentiation in anurans seems therefore to be more heavily influenced by

microhabitat selection then by evolutionary history. Competition for food usually occurs

between closely related species and differentiated use of microhabitats leads to a

reduction of negative interactions. Members of different species are less likely to

compete for resources when they often live in different environments, feed at different

time, and for those reasons eat different food. Those partitioning of food than arise by

current competition and microhabitat separation reflects on a small specialization on

prey types, as seen in hylid frogs.

In the evolution of Anura the types of prey consumed do not correspond mainly to

ecological differences between frog species. Many small anurans, like some dendrobatid

frogs, microhylids and small bufonids eat tiny prey items as termites, collembolans,

mites, and ants (Ernst et al. 2006). In contrast, large-bodied anurans also feed on small

invertebrates, and most of these appear to eat any prey than specialize in a particular set

of food (Costa et al. 2008). In a lack of conspicuous shifts in diet, and its correlation

with the phylogeny, ecological differences may result from shifts in different niche

dimensions. However, in some cases closely-related species not differentiate their

trophic niches if there is sufficient geographic and ecological space for organisms to

expand for (Sahney et al. 2010). Thus, the coexistence is achieved by spatial or

behavioral segregation between two or more species (Menin et al. 2005). What is

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important to keep in mind is that the ecological differentiation and interspecific

competition, even when in a past ancestor, cannot always be considered linked.

The most embracing evolutionary effect of competition is ecological diversification,

or niche partitioning. For extant anuran, diet changes may only appear recently.

However, even when dietary differences between our anuran species is not marked,

these differences exist and could be a result of profound changes in its biology. Many

morphological adaptations in frogs were shown to drive species ecology and behavior,

as the shape of skull is correlated with the size and types of preys consumed (Emerson

1985). However, much of the ecological separation that allows species persistence is on

exploring different habitats or microhabitats. For example, burrowing frogs eats a lot of

ants and termites, whereas other anuran seems to avoid this type of food (Toft 1980).

But, as shown in our results (Hylidae as the most divergent clade), the anurans can be

divided into two distinct groups: arboreal and litter frogs.

Arboreal frogs find their food in vegetation or yet in the forest canopy. The period

of activity generally encompasses most of the night, and they spend the day in protected

sites (Parmelee 1999). They often eat relatively large preys, such mantodeans,

orthopeteras and beetles (Menin et al. 2005). The species of this group usually have

wide mouths, a trait that is more typical of generalists predators (Emerson 1985). The

second group, the litter frogs, is composed by species that spend most of their lives in

the leaf litter of the forest floor. One of the most divergent clade in our results, the

Aromobatidae family, constitutes an interesting group of litter frogs. Poison frogs

forage in the litter of tropical forests and present range of strategies, from sit-and-wait

predation to active foraging searching for food in the early morning (Darst and

Menéndez-Guerrero 2005). Their diet is dominated by ants and its foraging strategy is

correlated with differences in activity metabolism (Vences et al. 2003).

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Major dietary shifts are distributed along frogs' evolutionary history, showing an

alternative scenario to deep history hypothesis. However, the role of competition,

predation and other ecological interactions in a past moment still has a little exploratory

power in ecological differentiation of anurans. Likewise, the relatedness of species may

act jointly with interactions to determine which species will compose a community

(Scheffer and Van Nes 2006). Our analysis suggests that diet partitioning were a

secondary step from evolutionary change. Change to one prey to another requires first

changes in morphology, body size, behavior and microhabits. Anurans have a diet that

diverges from differences in more biological traits, like those cited above (Wells 2010).

Contrasting with recent studies on lizards and snakes, our analysis reveals that major

divergences in frogs' diets occurred in different periods during its phylogenetic history.

In contrast to recent studies on lizards, where relative proportions of prey categories for

many species were available (Vitt and Pianka 2005), the present study was conducted

with presence-absence data to construct our prey matrix for analysis, reducing the

resolution of our dataset. For example, a specialist species might occasionally eat some

preys that are not the main important item in its diet (e.g. bufonid diets have a high

proportion of ants, but they also eat other preys like beetles, spiders, hemipterans).

Thereby, our analysis misses many important dietary shifts that would be detected with

appropriate quantitative data. Yet, we are confident with the major dietary shifts

identified by our study.

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global change. - N. Z. J. Ecol. 21: 1–16.

Vitt, L. J. and Pianka, E. R. 2005. Deep history impacts present-day ecology and

biodiversity. - Proc. Natl. Acad. Sci. U. S. A. 102: 7877–81.

Vitt, L. J. and Caldwell, J. P. 2009. Herpetology. - Elsevier.

Vitt, L. J. et al. 1999. Historical Ecology of Amazonian Lizards : Implications for

Community Ecology. - Oikos 87: 286–294.

Walker, T. and Valentine, J. 1984. Equilibrium models of evolutionary species diversity

and the number of empty niches. - Am. Nat. 124: 887–899.

Wells, K. 2010. The ecology and behavior of amphibians. - The University of Chicago

Press.

Wiens, J. J. 2007. Global Patterns of Diversification and Species Richness in

Amphibians. - Am. Nat. 170: S86–S106.

Wiens, J. J. 2011. The niche, biogeography and species interactions. - Philos. Trans. R.

Soc. Lond. B. Biol. Sci. 366: 2336–50.

Wiens, J. J. and Donoghue, M. J. 2004. Historical biogeography, ecology and species

richness. - Trends Ecol. Evol. 19: 639–44.

40

Wiens, J. J. and Graham, C. H. 2005. Niche conservatism: Integrating Evolution,

Ecology, and Conservation Biology. - Annu. Rev. Ecol. Evol. Syst. 36: 519–539.

Willis, J. 1922. Age and area. - Cambrigde University Press.

41

42

Node Clades R2 F P

1 Hylidae 0.058 9.28 <0.001

2 Hylinae 0.044 6.82 <0.001

3 Aromobatidae 0.044 6.85 <0.001

4 Hylidae, Bufonidae, Aromobatidae, Leptodactylidae 0.039 6.02 <0.001

5 Osteocephalus, Phyllodytes, Trachycephallus, Nyctimantis, Itapotihyla

0.038 6.00 <0.001

6 Myobatrachidae, Bachycephalidae, Craugastoridae, Eleutherodactylidae

0.032 4.89 <0.001

7 Bufonidae, Leptodactylidae, Aromobatidae, Hylidae, Cycloramphidae, Odontophrynidae

0.031 4.86 <0.001

8 Rhacophoridae, Mantellidae, Ranidae, Dicroglossidae, Ptychadenidae

0.030 4.60 <0.001

9 Node 7 + Craugastoridae, Eleutherodactylidae 0.030 4.57 <0.001

10 Scinax, Hyla, Osteocephalus, Phyllodytes, Trachycephalus, Nyctimantis, Itapotihyla

0.030 4.62 <0.001

11 Node 25 + Scaphiopodidae, Pelobatidae, Megophrynidae 0.030 4.65 0.002

12 Hyla, Osteocephalus, Dendropsophus, Pseudis 0.028 4.38 0.003

13 Bufonidae, Aromobatidae 0.027 4.22 0.002

14 Dendropsophus, Pseudis 0.024 3.73 0.002

15 Tachynemis till Polipedates * 0.023 3.56 0.004

16 Alytidae, Bombinatoridae 0.021 3.20 0.009

17 Bufonidae, Aromobatidae, Leptodactylidae 0.020 3.14 0.005

18 Lithoria, Phyllomedusa, Hylomantis 0.016 2.47 0.029

19 Bufonidae 0.015 2.32 0.025

20 Scaphiopodidae, Pelobatidae, Megophyidae 0.010 1.60 0.131

21 Cycloramphidae, Hylodidae, Odontophrynidae 0.009 1.40 0.181

22 Craugastoridae, Eleutherodactylidae, Brachycephalidae 0.006 1.01 0.398

23 Myobatrachidae 0.005 0.82 0.544

24 Leptodactylidae 0.003 0.58 0.763

25 Node 15 + Myobatrachidae, Brachycephalidae, Eleutherodactylidae

0.003 5.13 0.002

All the nodes were ranked by the proportion of total variation of outcomes explained by the model, which is

given by the coefficient of determination. The clades that are included in the nodes are represented in the

second column.

Table 1. Results of a nonparametric MANOVA analysis on diets of 148 frog species representing all

major clades

43

Figure 1. A phylogenetic three for the 148 frog species. Numbers indicates the ranking of eight nodes

that explain most of the variance of diet.

44

Figure 2. Biplot from a Canonical Correspondence Analysis (CCA) showing the

relation between frog phylogeny (arrows) and frog diets (diamonds). The length of

arrows represents the strength of correlation of the phylogeny with the axes. Prey

items (diamonds) close to the graph center indicates that a low association with

frogs clades or a positive association with a group of clades. Prey items close to

graph periphery indicate a high association with a specific clade or an occasional

association. The numbers represents the phylogeny nodes on which are included

several clades: 1 (Hylidae); 2 (Hylinae); 3 (Aromobatidae); 4 (Hylidae, Bufonidae,

Aromobatidae, Leptodactylidae); 5 (Osteocephalus, Phyllodytes, Trachycephallus,

Nyctimantis, Itapotihyla); 6 (Myobatrachidae, Bachycephalidae, Craugastoridae,

Eleutherodactylidae); 7 (Bufonidae, Leptodactylidae, Aromobatidae, Hylidae,

Cycloramphidae, Odontophrynidae); 8 (Rhacophoridae, Mantellidae, Ranidae,

Dicroglossidae, Ptychadenidae).

45

46

CAPÍTULO II

Largura de nicho, tamanho corporal e

história evolutiva predizem a

distribuição geográfica dos anuros da

Amazônia

Manuscrito sob preparação.

Sapo voador, Alfred Russel Wallace. Nanquim sobre papel, 1869.

47

NICHE BREADTH, BODY SIZE AND EVOLUTIVE HISTORY JOINTLY

PREDICT GEOGRAPHICAL RANGE SIZES IN AMAZON RAINFOREST

ANURANS

Talita Ferreira Amado

Laboratório de Anfíbios e Répteis, DBEZ- Centro de Biociências, Universidade Federal do Rio

Grande do Norte

Gabriel Corrêa Costa

Laboratório de Macroecologia, DECOL- Centro de Biociências, Universidade Federal do Rio

Grande do Norte

Janalee Paige Caldwell

Sam Noble Oklahoma Museum of Natural History, Departament of Zoology, University of

Oklahoma. USA

Adrian Antônio Garda

Laboratório de Anfíbios e Répteis, DBEZ- Centro de Biociências, Universidade Federal do Rio

Grande do Norte

ABSTRACT

The niche breadth of a species the array of conditions and resources that a species can

use or occupy, might determine the distribution of species. But, also the species

evolutionary history and body size new areas are known to be related to the species

geographical range size. We analyzed 42 anuran species of Amazonia and we used a

phylogenetic regression to test for a relationship between geographical range size

(GRS) and the variables: niche breadth, body size, and species’ divergence age. We

repeat our analyses with 24 species that have its divergence age superior than 30

million years. We also analyzed the phylogenetic signal for the species to further test if

the variables are phylogenetically structured and shows conservatism over the species

evolutionary history. With the older 22 species we found a significant positive

relationship between GRS and niche breadth, and species divergence age, and body

48

size. Only body size had a positive correlation with GRS when we test all the 42 species.

We find that the niche breadth is the most conserved trait. This result suggests that the

array of resources that those species consume is relicts from the ancestor and do not

shown relationship with the GRS. Our results provide support for Brown’s hypothesis,

or the argument that species with broad niches have a wider distribution. Our analysis

also demonstrates that the frog size contributes to its geographical distribution, which

is an intuitively and common pattern in vertebrates, and that the older species are more

widespread.

Keywords: niche breadth, frogs, phylogeny, niche conservatism, phylogenetic

regression

INTRODUCTION

A species niche breadth represents the diversity of conditions and resources that

it can use or occupy (Putnam and Wratten 1984, Gaston and Spicer 2001). Species can

be either specialists, when they use a relative narrow spectrum of resources or

generalists, when they use a broad spectrum of resources. (Devictor and Clavel 2010).

Positive and negative relationships between niche breadth and geographical range size

(GRS) have been proposed (Brown 1984, Williams et al. 2006). Brown (1984) states

that species with broad niches must be geographically widespread, because by utilizing

more resources and by maintaining viable populations in a greater array of conditions

species become more widespread and locally abundant (Brown et al. 1996, Kirkpatrick

and Barton 1997, Slatyer et al. 2013). Therefore, generalists can potentially occupy

wider geographic ranges by taking advantage of a broad set of resources, leading to a

49

positive relationship between niche breadth and GRS (Lawton et al. 2012, Nakazawa

2013).

Two hypotheses other than Brown's hypothesis may explain a positive

correlation between GRS and niche breadth (Williams et al. 2006). First, range-

restricted species are more likely to evolve ecological specializations due to natural

selection (Futuyma and Moreno 1988) because in widespread species local adaptation is

attenuated by gene flow among different locations with different selective pressures

(Kirkpatrick and Barton 1997). Second, a positive relationship may result from a

sampling effect, because widespread species have access to a more diverse pool of

resources (Gaston et al. 1997, Williams et al. 2006). The use of different geographic

scales and sampling bias may lead to a positive statistical relationship between niche

breadth and range size (Slatyer et al. 2013). This false positive correlation may arise

when in widespread species the niche breadth is calculated from more individuals or

more populations (Brown 1984, Gaston et al. 1997), generating a sampling bias.

Alternatively, a negative correlation may arise from niche breadth and GRS

(Williams et al. 2006). If the pattern pointed out by Brown (1984) is plausible then

specialist species rely on a limited range of resources and have a narrow distribution.

But, due to environmental stochasticity, restricted and specialist species are more

sensitive to extinction and we should find a few example of them (Pyron 1999, Devictor

et al. 2008, Devictor and Clavel 2010, Clavel et al. 2010). At last, because widespread

species are less likely to go extinct, they have more opportunities to evolve

specializations. In this way, a specialist must present a wider distribution to compensate

its limited exploration of the niche (Williams et al. 2006). Thus, a negative relationship

between niche breadth and GRS is occurs by selective extinction.

50

All these relationships between niche breadth and GRS are intuitive explanations

for the commonness and rarity of species, and the first one tells us that a specialist

species has to be more rare and restricted (Slatyer et al. 2013). Thus, the niche

breadth/geographical range size can be a key in ecology being relevant to predict the

species vulnerability to extinction (Devictor et al. 2008, Devictor and Clavel 2010,

Clavel et al. 2010). Traditionally, niche breadth is inferred indirectly from spatial and

environmental data (e.g. microhabitats variables, species performances in different

environments), and more directly from dietary data (Soberón 2007, Calenge and Basille

2008). The emerging of detailed measures of specialism allowed us to better understand

the relationship between trophic ecology and the distribution and abundance of a species

(Elton 1927, Van Valen 1965). But, together with niche breadth, the evolutionary

history of organisms leads to greatly understanding of the history of animal

distributions.

The actual distribution of a species is a complex mosaic of spatial and temporal

areas (Brown et al. 1996). The first to consider that the species geographic distribution

may reflect its evolutionary history was Willis (1922). In his book “Age and Area”,

Willis states that the older species are more widespread. In speciation events most part

of new species rises with a small GRS but, during its evolutionary history a species may

expand its range and become more widespread (Taylor and Gotelli 1994, Webb and

Gaston 2000). If the environment provides all the resources and conditions to the

species establishment, then its GRS increases. This expansion is supported by adaptive

differentiation which is commonly observed in invasion processes that allow species to

extend their ranges (Phillips et al. 2006). This mechanisms leads to a positive

correlation between species age and GRS, supporting the age-area hypothesis of Willis

51

(Willis 1922). Therefore, this approach is a key to better understand the historical

factors that determines the geographical range of species.

Here we aim to understand the factors that leads to a widespread or a narrow

geographic distribution. In this study we use a dataset on amphibians that includes the

dietary data of 61 anuran species. We chose amphibians for several reasons. First, for

many species geographic distribution maps and molecular phylogeny was recently made

and is available online (Stuart et al. 2004, IUCN 2008, Pyron and Wiens 2011). Second,

anurans are easy to collect and examine diet breadth. Our database includes diet

information from field surveys conducted along seven years in three different countries

of Amazon forest. In the present study, we measured the niche breadth, body size,

species age and geographical range of tropical rainforest frogs. By doing this we aimed

to (i) further test the hypothesis that widespread species should present wider niches,

and (ii) that an older and bigger species are more widespread.

METHODS

DATA COLLECTION - From 1993 to 1999 one of us (JPC) collected dietary data on 61

anuran species in different field expeditions to Nicaragua, Ecuador, and Brazil

(Appendix 1). The field work was conducted in Amazonian tropical forests and

amphibians were collected by hand during searches in the forest. Frogs were humanely

killed by rubbing anesthetic cream in their abdomen, an approved form of euthanasia for

small vertebrates (American Society of Ichthyologists and Herpetologists et al. 2006).

We measured the snout-vent length (to 0.1 mm), a standard measurement of body

length, from the tip of the snout to the cloacal aperture. Detailed methods for collection

52

of frogs, identification and measurements of preys appear elsewhere (Caldwell 1996,

Caldwell and Vitt 1999, Garda et al. 2012).

NICHE BREADTH MEASUREMENTS - Most measurements of species niche breadths

compare frequency distributions of resource use to and resource availability (Levins

1962, Feinsinger et al. 1981). Levin (1968) suggested the inverse of the Simpson index

of diversity. That is given as:

∑

where is the proportion of all resources used by the individual i. We used the Levin‟s

index of niche breadth to further test our hypotheses.

GEOGRAPHICAL RANGE - We downloaded anuran species distribution maps from the

Global Amphibian Assessment database (Stuart et al. 2004, IUCN 2008). Species

distribution maps were loaded in DIVA-GIS 7.5 (Hijmans et al. 2004), where we

calculated average geographical range area (km2) for all species, but considering only

the original distribution. Areas where some species were introduced were not included

in the calculation. We also excluded all the ranges smaller than 5 km2. In all analyses

we use log10-tranformed range size for a distribution approximately log-normal of

amphibian GRS.

STATISTICAL ANALYSES - We used phylogenetic signal to measure conservatism among

species traits (body size, niche breadth, and GRS). Phylogenetic signal is a tendency of

close and related species to resemble each other more than other species in the tree

(Blomberg and Garland 2002). Thus, an ecological trait is highly conserved over the

evolutionary history of species if the signal is high. We verified whether or not our data

53

were phylogenetically structured from a random test that uses the descriptive statistic k

proposed by Blomberg ( 2003).

We performed a phylogenetic regression analysis to examine the relationship

between geographical range size and niche breadth, body size, and species‟ divergence

age. We test the relationships with phylogenetically independent contrasts of all

variables to control for effects of phylogeny. Independent contrasts use the phylogenetic

information to transform observed data into values that are independent and identically

distributed (Felsenstein 1985).

We believe that young species have not yet achieve their potential geographical

distribution and may deviate from any relationship between GRS and our variables

because allopatric speciation events may lead to a presence of different sizes of

geographic ranges between young species (Webb and Gaston 2000). During the

Eocene/Oligocene boundary (about 40 – 30 million years ago) the Earth experienced

major climatic changes that leaded to a massive extinction and split of the distribution

of plants and animals (Prothero 1994). These geoclimatic events shaped the Neotropical

region and may have promoted variance (Wesselingh and Salo 2006, Heinicke et al.

2007, Santos et al. 2009, Rull 2011, Fouquet et al. 2012). If the range of a widespread

species is fragmented over time, resulting diverging populations may inherit the dietary

niche breadth from the ancestor and therefore show no relationship between a

geographic distribution and dietary breadth (Webb and Gaston 2000, Graham et al.

2004, McCormack et al. 2010). Due the reasons above, we repeated our analyses after

excluding species younger than 30 Myr.

To further test the hypotheses and to calculate the species‟ divergence age we

use a phylogenetic tree calibrated in million years (Myr) from Pyron and Wiens (2013).

54

All the analyses were performed with R software version 3.0.1 (R Team, 2013). We

calculated the phylogenetic signal with Picante package (Kembel et al. 2010) and the

phylogenetic regression with both CAPER and APE package (Orme 2012, Paradis

2012).

RESULTS

The niche breadth and body size showed phylogenetic signal, which indicates

that those observations are structured phylogenetically. The variable that presents the

highest signal is niche breadth (k=0.97, p<0.001) follow by body size (k=0.70, p<0.01).

The only variable that showed no phylogentic signal was GRS (k=0.39, p=0.14). Those

results suggest that niche breadth presents a high degree of conservatism over the

evolutionary history of Amazon anurans.

Forty-two species had their range distribution, dietary niche, body size and age

measured (Figure 1). The smaller species was Epipedobates boulengeri, a species that

has a lower locomotion due its small size, and the Andes Mountains had an important

role in its limitation to dispersion (Vences et al. 2003). When examining the

relationship between geographical range and body size we found a positive correlation

(Figure 2c; r2=0.23 and P<0.01). This relationship is maintained even when we exclude

younger species (Figure 2d; r2= 0.17 and P=0.01). The larger species in our dataset was

Lithobates palmipes, a species that occurs widely in the Amazon basin (Oliveira et al.

2010).

We found no relationship between dietary niche breadth and geographical range

(Figure 2a; r2=0.05 and P=0.13) with all forty two species in the analysis. However,

55

when we consider only the species that did not have an origin under major climatic

changes of Amazonia (e.g. 30 Mya), the niche breadth-geographical range correlation

becomes significant (Figure 2b; r2=0.42 and P<0.001). Leptodactylus fuscus was the

species with broadest geographical range, and Allobates caeruleodactylus had the

narrowest distribution (Appendix 1).

We also found a relationship between geographical range size and species

divergence in the phylogeny (Figure 2f; r2=0.31 and P<0.001), which indicates that

older species have widespread ranges. This result is achieved only in older species

which did not have its geographical range splitted. With also the younger species found

no relationship between geographical range size and species divergence in the

phylogeny (Figure 2e; r2=0.03 and P=0.26).

DISCUSSION

Our findings suggest that generalists, large-bodied and older species are more

widespread with strong dietary niche conservatism. The same relationships have been

reported across a great array of taxa, with a positive relationship between niche breadth

and geographical range (Slatyer et al. 2013), a positive relationship between body size

and geographical range for Australian frogs (Murray et al. 1998) and also between

species age and geographic range in birds (Webb and Gaston 2000).

The relationship between niche breadth and geographical range

The limit of a species geographic range is the clear limit of its niche (Sexton et

al. 2009). It is clear, therefore, that a broad niche must enable a species to become

widespread (Slatyer et al. 2013). A species that is able to consume different resources in

different conditions can persist more in the environment. This species has also a large

56

range of suitable areas to explore its resources (Brown 1984). With more areas to

explore, survive, and perhaps reproduce it is logical that generalists will have the larger

distribution area. Our results agree with a recent meta-analysis (Slatyer et al. 2013) that

showed that the niche breadth-geographical range relationship is a general ecological

pattern.

Our findings suggest that among Amazonian anurans the dietary niche is

conserved. The niche conservatism is the species tendency to maintain aspects of their

niches over evolutionary time scales (Graham et al. 2004). Consequently, a conserved

trait must have played an important role by structuring and limiting the species

distribution (Angulo et al. 2011). The low frequency in ecological trait change may

allow restricted species higher chance of persistence in the environment. In this way, a

negative correlation between niche breadth and range size may have arisen. Williams et

al. (2006) argue that this negative correlation is a compensation for the rarity of species.

Thus, rare species with restricted distributions must be more generalist in order to

persist.

We found no significant correlation between niche breadth and range size of all

forty-two species analyzed together. In this full dataset we have species that diversified

in periods of great environmental changes, which may lead to speciation events by

isolating some species populations. The geographical range of these species is a

consequence of how the ancestral geographic range was divided (Webb and Gaston

2000). Thus, this lack of correlation is observed when we exclude younger species that

arose from vicariance. Those younger species inherited a conserved dietary niche

breadth, but also inherited a geographical range that does not reflect an ecological

relationship with an biological trait. Still, this species range size will be reflecting its

evolutionary history.

57

The relationship between body size and geographical range

In many different animal taxa a positive relationship between body size and

geographic range has been observed (Gaston and Blackburn 1996). This is a consistent

and intuitive pattern within vertebrates, where bigger species tend to have larger

distribution areas. For Amazonian frogs, our results with the full dataset, as well with

the older lineages only, confirm this tendency (Figure 2 c and d). Some mechanisms

may explain the pattern found in our study: (1) large-bodied species require wider

ranges to maintain viable populations, (2) large-bodied species can maintain

homeostasis over a wide array of conditions, and (3) dispersal ability increases with

body size (Brown and Maurer 1987).

Locally abundant species tend to be more widely distributed than locally rare

species for a number of different taxa (Brown and Maurer 1987). It is also intuitive that

larger animals require more space to supply their needs. Like Murray et al. (1998), we

cannot evoke a mechanism like the minimum viable population size to explain that a

bigger body size leads to a wider range, due that amphibians are not highly

territorialists. However, frogs are strongly associated to the environment due to their

dependence on moisture and in general show large aggregations of individuals along

watercourses for reproduction and feeding (Wells 2007). Even when territorialism is

absent, the competition for food, mates, and nesting areas promotes the species to

spread its individuals. Thus, larger species require larger areas to supply their needs and

sustain a minimum viable population size (Brown 1984).

Species with broad dietary niche have the potential to explore and occupy a

great diversity of environments (Slatyer et al. 2013). With sufficient resources, an

organism can maintain its physiological requirements balanced. Allied with a broad

58

niche breadth, a larger body size allows a species to tolerate changes in habitat, and as

body size increases the ability to maintain the homeostasis in a greater array of

conditions also increases (Kearney and Porter 2009). However, even when an area has

all the requirements, conditions, resources and is totally appropriate to the maintenance

of viable populations if the individuals are unable to reach this, the species will not

occur. Thus, the possibility to disperse is a variable that influences the species

geographical range.

The most obvious ecological implication of body size is the dispersal capability.

Like many other biological activities, locomotion requires energy and the cost of

walking, flying or swimming is markedly increased in larger animals (Petters 1983).

Despite the higher cost, larger size may enable long periods of locomotion by increasing

the starvation resistance and providing larger energy storage (Juliano 1983). The larger

species in our dataset was Lithobates palmipes, when compared with the smallest one

Epipedobates boulengeri clearly seems to have a dispersal advantage, which supports

our findings. Still, some ecological aspects of species may retain the expansion of

species range, like environmental barriers (Sexton et al. 2009). However, Rhinella

marina is a species that reaches larger body sizes, although, in our observations R.

marina is smaller than L .palmipes, and it reaches broader distributions due to greater

dispersal capacity (Phillips et al. 2006). R. marina is also an environmental generalist,

occurring both in open (savannahs, grasslands, marshy areas, degraded forests and

urban habitats) and dry equatorial forests, while L. palmipes is more related to forest

formations (IUCN 2008). Therefore, larger species are more able to disperse

successfully and likely had more time since speciation to disperse and establish a larger

range than small-bodies species.

59

The relationship between species age and geographical range

Among closely related species, evolutionary mechanisms may also determine

differences in niche and geographical range sizes (Webb and Gaston 2000).

Transformations in the area occupied by organisms occur in early stages of species

evolution, and an evolutionary inertia is expected to keep its geographic range size

somewhat constant throughout time. This is a stasis model proposed by Jablonski

(1987) who states that the major modification in range size will occur during the

processes of speciation and extinction, and in regions with high environmental

instability. In general, the ideas of Jablonski (1987) were supported by the analyses in

the present study. By excluding species that originated within Amazonia and just after a

period of major climate changes (the Eocene/Oligocene boundary), we note that older

species may be reaching this stasis. This reinforces that major modifications in ranges

occur in the early ages of species.

The age-area hypothesis argues that geographic range size may increase over

time (Willis 1922). The evidence of a positive correlation between the age of our

species and their geographic range size is presented here. This period of increase may

culminate in a decline of range size for some species. This last statement is also

supported by our findings, when along our phylogenetic tree closely related species

show geographic distributions both small and large. For example, Chiasmocleis bassleri

is older than Elachistocleis ovalis, but C. bassleri has a distribution area smaller than E.

ovalis (Figure 3). Nevertheless, despite some deviations, it is clear that the geographical

range size increases with the species evolutionary age. Some mechanisms of adaptive

differentiation may explain this pattern (Webb and Gaston 2000).

60

Species that derived in “island” habitats are expected to deviate from any

relationship between species age and geographic distribution. In a fragment of habitat

that provides all species requirements, surrounded by an impermeable matrix,

individuals tend to move towards the center of this island and become more specialized

with time (Angert et al. 2011). This will limit the range expansion unless the species

dispersal ability or adaptive differentiation allows the range growth (Phillips et al.

2006). Again, dispersal capability is a key variable in range expansion and is improved

over time. The absence of individuals of a species from suitable habitats may arise from

dispersal limitations, but during the course of its evolution a species may become

capable to reach and occupy a new area (Webb and Gaston 2000).

CONCLUSIONS

The main hypothesis of Brown (1984), of a positive relationship between niche

breadth and geographic range size, has been studied during the past twenty years but a

consensus about this generality was slow to emerge. Our work shows evidences for a

relationship between niche breadth and range size considering other factors that may

mediate the expected relationship. Evolutionary mechanisms and events also determine

the niche and distribution size, and were evidenced by our study: the older the species,

the more widespread it is. This finding reflects all the process range expansion, which is

achieved over the evolutionary time. Still, even when the area supplies all requirements,

if the species cannot access it the expansion will not occur. Nevertheless, our results

show that the larger-bodies species, which have higher dispersal abilities and can resist

in a greater array of environmental conditions and have larger distributions. We also

61

found that the dietary niche of Amazonian frogs is conserved and may be what enable

species with restricted ranges to maintain viable populations.

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All species included Cut at 30 Myr

Variable Factor df r2 p df r2 p

Geographical Range Size

Niche Breadth 40 0.05 0.13 23 0.42 <0.001

Divergence Age 40 0.03 0.26 23 0.31 <0.001

Body Size 40 0.12 0.019 23 0.22 <0.01

Table 1 Phylogenetic regression analyses of geographical range size, niche breadth, divergence and adult body size. The results are separated accordantly to which dataset we used. The first are the result with all 42 species included and the second are the results with only the species that are older than 30 million years

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Figure 1 The phylogenetic tree of forty two species of Amazonian anurans. The dashed line shows

the period of 30 million of years. Prothero (1994) argue that, during the late Eocene-Oligonece

period, about 40 to 30 Myr, the Earth experienced major climatic changes. These changes caused

mass extinctions and area splits that produce significant differences in species geographical range

size. The species in blue are those that we exclude to repeat the analyses and show the effect of

evolutionary history of species distribution size.

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Figure 2 Relationship between the contrasts of geographical range size and the variables

niche breadth, body size, and divergence age. The results the two phylogenetic

regressions: one realized with all forty two species, and a second with the twenty two

species older than 30 million years.

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Figure 3 The two phylogenetic trees with all forty four species used in the analyses. Here we have the

reconstruction of geographical range across the phylogeny with smaller ranges shown as blue (left). As

the range become bigger the color passes to red. We did the same for the species niche breadth (right),

with specialist lineages shown colored as a blue gradient. A lack of correlation between niche breadth and

geographical range is evident, but when we look to deeper lineages a relationship arose.

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CONCLUSÕES

Na presente dissertação foram testadas diferentes hipóteses sobre os fatores que

levam à coexistência das espécies e sobre os fatores que determinam a distribuição dos

anuros. Em ambos os capítulos, os resultados foram gratificantes e adequados para que

possamos fazer novas generalizações a cerca da ecologia dos anuros. No primeiro

capítulo, ao testarmos a hipótese deep history, concluímos que as diferenças que levam

as espécies de sapos a coexistirem surgiram em diferentes momentos na evolução desses

organismos. Contrastando com estudos recentes com serpentes e lagartos, nossas

análises revelam que as maiores divergências na dieta dos sapos ocorreram durante toda

a história filogenética desses organismos. O estudo foi conduzido com dados de

presença e ausência para a construção de uma matriz de dieta e matriz filogenética,

reduzindo a resolução nos nossos dados. Entretanto, acreditamos que as principais

divergências na dieta foram identificadas.

No segundo capítulo, observamos que tanto a dieta como as características

biológicas, como tamanho corporal, são elementos importantes para se definir a área

ocupada pelas populações das espécies de sapos. Nosso trabalho mostra uma relação

positiva entre largura de nicho e distribuição geográfica. Mecanismos evolutivos e

eventos também determinam a área ocupada pelas espécies: quanto mais antigas, mais

dispersas são as espécies. Esses resultados refletem os processos de expansão de área, o

qual é alcançado ao longo do tempo. Ainda, mesmo se a área supri tidas as necessidades

e requerimentos do organismo, se este não consegue acessá-la a expansão não ocorrerá.

Portanto, nossos resultados mostram que espécies com grande tamanho corporal, as

quais possuem elevado potencial de dispersão, possuem áreas de distribuição maiores.

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