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.
9
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: [email protected]
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
29
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).
30
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
31
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
32
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
33
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).
34
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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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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