functional traits among populations of copaifera ...pos.icb.ufmg.br/pgecologia/teses/t140 - matheus...
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UNIVERSIDADE FEDERAL DE MINAS GERAIS
INSTITUTO DE CIÊNCIAS BIOLÓGICAS
PROGRAMA DE PÓS-GRADUAÇ Ã O EM ECOLOGIA, CONSERVAÇ Ã O E
MANEJO DA VIDA SILVESTRE – PPGECMVS
Functional traits among populations of Copaifera
langsdorffii (Leguminosaea) in an environmental
gradient
MATHEUS LOPES SOUZA
Belo Horizonte/MG
Agosto de 2016
ii
MATHEUS LOPES SOUZA
Functional traits among populations of Copaifera
langsdorffii (Leguminosaea) in an environmental
gradient
Tese apresentada ao Programa de Pós-
Graduação em Ecologia, Conservação e
Manejo de Vida Silvestre do Instituto de
Ciências Biológicas da Universidade
Federal de Minas Gerais, como requisito
parcial à obtenção do título de Doutor em
Ecologia, Conservação e Manejo de Vida
Silvestre.
Orientador: Dr. José Pires de Lemos Filho
Co-orientador: Dr. Marcílio Fagundes
Co-orientador: Dr. Fernando Valladares
Belo Horizonte, MG
Agosto de 2016
iii
Dedico esta Tese à minha avó
Francisca Lopes Costa
iv
AGRADECIMENTOS
Durante quatro anos tive a oportunidade de conviver com todas essas pessoas
fantásticas e brilhantes que me ajudaram na construção desta tese. Neste período foram
percorridos mais de 30.000 km na coleta de dados. Infelizmente não é possível
descrever como em uma analise estatística a importância de cada uma destas pessoas
nesta trajetória, mas todas foram altamente significativas.
Gostaria de registrar os meus sinceros agradecimentos (...)
Ao Prof. José Pires de Lemos Filho pela oportunidade e confiança em mim depositada.
(...) Obrigado pela orientação, respeito, apoio, amizade.
Agradeço aos Prof. Marcel França, Queila Garcia e Luzia Modolo do
Laboratório de Fisiologia Vegetal/UFMG pelo respeito e aprendizado. A todos os
amigos deste laboratório, especialmente a Alexandre, Dávila, Laura, Silvana as meninas
da Queila e da Luzia pela amizade, pelas conversas, trocas de experiência e momentos
de descontração.
Ao Prof. Marcílio Fagundes, meu Co-orientador, que foi essencial na construção
desta tese, desde a ideia inicial do projeto até a coleta de dados em campo. Aos
companheiros do Laboratório Biologia da Conservação/UNIMONTES (Kenedy,
Leticia, Renata, Henrique e Rithiele) que foram meu braço direito nas coletas do norte,
Muito Obrigado!
Ao professor Fernando Valladares, também meu Co-orientador, com quem tive a
oportunidade de fazer o Doutorado Sanduiche. Suas contribuições foram relevantes para
a qualidade desta tese e durante minha estadia na Espanha eu aprendi muito, pois além
do Fernando ser um cientista brilhante é também uma excelente pessoa. A todos os
v
companheiros da “Planta 8” do Museo de Ciências Naturales/CSIC e a Nacho, Daniela e
família “Tengo mucho que agradecer a todos por una maravillosa estancia en España y
por las amistades preciosas que hice en Madrid. Gracias chicos!”
Tenho que agradecer ao apoio que tive em Lavras dos amigos Tulio, Ailton,
Guedes e Toin pelo abrigo e força no campo durante as coletas. Em Lavras as coletas
sempre foram recheadas de aventuras e perigos, mas felizmente saímos vivos e
parcialmente e ilesos de todas!
Agradeço também aos amigos (desde os tempos de UNIMONTES) Thaise,
Falcão, Etiene, Dudu, Rambo, Fred, Laura, Marina, Sarinha, Gramps, Cotonete e aos
“Sindicalistas”. À todos muito obrigado pela companhia, discussões e conselhos, me
sinto agraciado por ter conhecido e trabalhado com pessoas tão especiais como vocês.
À professora Maria Bernadete que participou ativamente no desenvolvimento
dos manuscritos desta tese. E ao Programa de Pós Graduação em Ecologia,
Conservação e Manejo de Vida Silvestre, aos professores que ministraram as
disciplinas, em especial aos secretários Fred e Cris, que prontamente sempre me
antederam.
Por fim não poderia de destacar a importância da minha família na construção
desta tese. A Ana e Gabriel (nascido durante o doutorado), pelo amor, encorajamento e
compreensão, que tanto me ajudaram nessa caminhada. Com chegada do Gabriel
tivemos um novo, e mais amplo, sentido às nossas vidas. Só vocês sabem o quanto foi
difícil passar toda a temporada do doutorado sanduiche longe de casa. No entanto, tenho
sorte de ter uma esposa que me apoia e me ajuda em minhas decisões.
À Tia Ebia e Tio Menon que investiram em minha educação, graças a vocês
conseguir chegar onde estou. À minha amada mãe Edina, a todos meus irmãos (que são
vi
muitos), mais principalmente a Bia e Rafa, Bruno, Thiago e João Victor ao meu pai JC,
Tios, Tias e primos. Obrigado a todos!
Este estudo foi realizado com o apoio financeiro do CNPq, FAPEMIG e
CAPES. Agradecemos a bolsa de estudos concedida pelo Programa Internacional de
Doutorado Sanduíche (PDSE) financiados pela CAPES. Agradecemos também ao
Museu Nacional de Ciências Naturais (MNCN-CSIC), Madrid-Espanha.
vii
PELO APOIO E FINACIAMENTO
viii
SUMÁRIO
INTRODUÇ Ã O GERAL ............................................................................................... 13
OBJETIVO ................................................................................................................. 19
ESPÉCIE ESTUDADA .............................................................................................. 20
Á REAS DE ESTUDO ................................................................................................ 20
REFERÊNCIAS BIBLIOGRÁ FICAS ....................................................................... 22
TABELAS .................................................................................................................. 34
FIGURAS ................................................................................................................... 35
CAPÍTULO I: Phenological variation within and among populations of Copaifera
langsdorffii in eastern tropical South America ............................................................... 39
ABSTRACT ................................................................................................................ 40
INTRODUCTION ...................................................................................................... 41
MATERIAL AND METHODS .................................................................................. 43
Study area ................................................................................................................ 43
Phenological monitoring ......................................................................................... 44
Data analysis ........................................................................................................... 44
RESULTS ................................................................................................................... 46
Vegetative phenophases .......................................................................................... 46
Reproductive phenophases ...................................................................................... 47
DISCUSSION ............................................................................................................. 49
ACKNOWLEDGEMENTS ........................................................................................ 51
LITERATURE CITED ............................................................................................... 52
TABLES ..................................................................................................................... 60
FIGURES .................................................................................................................... 64
ix
CAPÍTULO II: Soil fertility determines seed size/number trade-off of a widely
distributed Neotropical tree along a climatic gradient.................................................... 65
ABSTRACT ................................................................................................................ 66
INTRODUCTION ...................................................................................................... 67
MATERIAL AND METHODS .................................................................................. 69
Species and study area ............................................................................................ 69
Seed sampling .......................................................................................................... 70
Statistical analysis ................................................................................................... 71
RESULTS ................................................................................................................... 73
DISCUSSION ............................................................................................................. 74
ACKNOWLEDGEMENTS ........................................................................................ 77
LITERATURE CITED ............................................................................................... 78
TABLES ..................................................................................................................... 87
FIGURES .................................................................................................................... 94
CAPÍTULO III: Key factors affecting seed germination of Copaifera langsdorffii, a
Neotropical tree .............................................................................................................. 99
ABSTRACT .............................................................................................................. 100
INTRODUCTION .................................................................................................... 100
MATERIALS AND METHODS .............................................................................. 101
Study area .............................................................................................................. 101
Data collection ...................................................................................................... 101
Data Analysis ........................................................................................................ 102
RESULTS ................................................................................................................. 102
DISCUSSION ........................................................................................................... 103
ACKNOWLEDGMENTS ........................................................................................ 103
REFERENCES ......................................................................................................... 104
x
CAPÍTULO IV: Climatic heterogeneity as a generator of phenotypic plasticity in
functional leaf traits of a neotropical tree species widely distributed .......................... 106
ABSTRACT .............................................................................................................. 107
INTRODUCTION .................................................................................................... 108
MATERIALS AND METHODS .............................................................................. 110
Species and study area .......................................................................................... 110
Morphological traits ............................................................................................. 111
Physiological traits ............................................................................................... 111
Data analysis ......................................................................................................... 112
RESULTS ................................................................................................................. 113
Phenotypic variance partition ............................................................................... 113
Morphological and physiological traits along an aridity gradient ...................... 114
Plasticity vs. interannual variation in precipitation ............................................. 114
DISCUSSION ........................................................................................................... 115
ACKNOWLEDGEMENTS ...................................................................................... 118
LITERATURE CITED ............................................................................................. 119
TABLES ................................................................................................................... 127
FIGURES .................................................................................................................. 129
CONSIDERAÇ ÕES FINAIS ....................................................................................... 134
REFERÊNCIAS BIBLIOGRÁ FICAS ..................................................................... 139
xi
RESUMO
Avaliar como as plantas alteram as características funcionais em resposta a
diferentes condições ambientais é importante para entender a amplitude de nicho de
uma espécie e essencial para prever possíveis efeitos das mudanças climáticas. O
objetivo deste trabalho foi avaliar variações em caracteres funcionais dentro e entre
populações de Copaifera langsdorffii distribuídas ao longo de um gradiente ambiental.
Especificamente, testamos hipóteses relacionadas a variações em caracteres
morfológicos, fisiológicos, comportamentais e da plasticidade fenotípica destes traços
com fatores ambientais, focando a aridez e/ou a fertilidade do solo como drivers para
diferenciação populacional. Foram selecionadas seis populações de C. langsdorffii
cobrindo um gradiente de precipitação em solos com diferentes níveis fertilidade em
três biomas de ocorrência da espécie (Caatinga, Cerrado e Mata Atlântica). Nossos
resultados demostraram que caracteres morfológicos, fisiológicos e comportamentais
variaram entre e dentro das populações. Estas variações nos traços funcionais foram
associadas com a precipitação e/ou a fertilidade do solo de cada população,
demonstrando que estes fatores são chaves para direcionamento de adaptações
ecofisiológicas, gerando diferenciação nos traços funcionais entre populações naturais
de plantas. Encontramos ainda maiores níveis de plasticidade e variação fenotípica em
populações com maior heterogeneidade climática. Alta plasticidade combinada com
capacidade de alterar as características funcionais em resposta a diferentes condições
ambientais podem contribuir significativamente para a amplitude de nicho C.
langsdorffii, o que poderia explicar o sucesso desta espécie sobre uma gama de
diferentes tipos de habitats em toda a sua ampla distribuição geográfica. Além disso,
altos níveis de plasticidade e variação fenotípica podem contribuir para a persistência de
C. langsdorffii frente às mudanças climáticas.
Palavras chave: Copaifera langsdorffii; ecofisiologia; mudanças climáticas;
diferenciação de populações; gradiente ambiental; aridez; fertilidade do solo.
xii
ABSTRACT
Evaluate how plants change the functional traits under different environmental
conditions is important factor for niche breadth of the species, and essential to predict
possible effects of climate changes. The aim of this work was evaluate the variations in
functional traits within and among populations of Copaifera langsdorffii along an
environmental gradient. Specifically, we test hypotheses related to variations in
morphological, physiological, behavioral and phenotypic plasticity of these traits with
environmental factors, focusing on the aridity and/or soil fertility as drivers for
population differentiation. Six populations of C. langsdorffii were analysed covering a
rainfall gradient in soils with different fertility in the three biomes where the species
occurs (Caatinga, Cerrado, Atlantic Forest). Our results demonstrated that
morphological, physiological and behavioral traits vary within and among populations.
These variations in the functional traits were associated with rainfall and/or soil fertility
of each population, demonstrating that these environmental factors are drivers
ecophysiological adaptations, generating differentiation in functional traits among
natural populations of plants. We also found higher levels of plasticity and phenotypic
variation in populations with greater climatic heterogeneity. High plasticity and
phenotypic variation in environmentally heterogeneous sites combined with the ability
to alter the functional traits in response to different environmental conditions can
significantly contribute to the niche breadth C. langsdorffii, which could explain the
success of this species over a range of different types of habitats along its wide
geographic distribution. In addition, high levels of plasticity and phenotypic variation
can contribute for the persistence of C. langsdorffii to ongoing climatic changes.
Keywords: Copaifera langsdorffii; ecophysiology; climatic changes; population
differentiation; environmental gradient; aridity; soil fertility.
13
INTRODUÇ ÃO GERAL
Avaliar os efeitos das condições ambientais sobre as populações naturais tem
importância para o entendimento dos processos evolutivos que garantem a manutenção
dos ecossistemas e da biodiversidade frente a possíveis mudanças climáticas globais
(Hooper et al. 2012; Cardinale et al. 2012; Garcia et al. 2014). Diversos cenários futuros
apontam para mudanças climáticas globais, com aumento da temperatura e aridez e
maior variabilidade na precipitação (IPCC 2014). Mudanças no clima e na paisagem
alteram as condições e a disponibilidade de recursos, o que pode pôr em risco parcela
considerável da biodiversidade (Nicotra et al. 2010). Em função das rápidas mudanças
ambientais três respostas são esperadas: (i) migrar ajustando-se a um ambiente mais
favorável, (ii) ajustar às novas condições através da plasticidade fenotípica ou (iii)
evoluir através da seleção natural (Nicotra et al. 2010; Matesanz and Valladares 2014).
Essas respostas dependem da intensidade e direção das mudanças ambientais, de
características relacionadas com a história de vida das espécies, da variação genética
intraespecífica e das interações interespecíficas (Nicotra et al. 2010; Nunney 2016).
Deste modo, estudos que buscam avaliar variações em caracteres funcionais que
determinam a distribuição de espécies em condições naturais tem importância para
prever possíveis efeitos das mudanças climáticas (Valladares et al. 2014).
Espécies com ampla distribuição, geralmente tem suas populações submetidas a
diferentes pressões de seleção ao longo de sua área de ocorrência, sendo afetadas por
múltiplos e distintos fatores estressantes como: extremos de temperatura, luminosidade,
umidade e fertilidade dos solos (Valladares and Pearcy 1997; Lemos Filho 2000; Sultan
2003). Gradientes de aridez são comumente observados em espécies com ampla
distribuição, com populações ocorrendo em ambientes úmidos até zonas semiáridas (ex:
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Copaifera lagsdoffii). Em ecossistemas semiáridos as populações dessas espécies
muitas vezes são afetadas não apenas pela limitação sazonal de água dentro de um ano,
comum nestes ambientes, mas também por maior variabilidade climática, com
amplitudes extremas de temperatura e grande variabilidade interanual na precipitação, o
que torna estes ambientes de certa forma imprevisíveis (Gianoli and González-Teuber
2005; Lázaro-Nogal et al. 2015). A combinação de fatores estressantes e
imprevisibilidade ambiental podem afetar diretamente o desempenho das plantas. No
entanto, significativas modificações nas características ecofisiológicas são esperadas em
resposta às pressões seletivas impostas em cada população (Niinemets and Valladares
2004; Uribe-Salas et al. 2008; Lázaro-Nogal et al. 2015), permitindo o crescimento, a
sobrevivência e a reprodução dessas espécies em habitats com diferentes filtros
ambientais (Sultan 2003). De fato, espécies amplamente distribuídas são capazes de
modificar suas estratégias ecológicas através de diferenças significativas nas
características funcionais relacionadas ao estresse ambiental, a capacidade competitiva e
a tolerância a distúrbios (Uribe-Salas et al. 2008; Goulart et al. 2011; Lázaro-Nogal et
al. 2015), o que torna estas espécies excelentes modelos para avaliar possíveis
consequências das mudanças climáticas sobre populações naturais devido a suas
distintas respostas a fatores ambientais.
Estudos visando analisar as estratégias que permitem a ocorrência de populações
em ambientes contrastantes tem focado avaliar distintas características que respondam
ao estresse ambiental (Valladares et al. 2014; Lázaro-Nogal et al. 2015; Salgado-Negret
et al. 2015). Dentre as variáveis avaliadas, as características funcionais ligadas ao
metâmero foliar (entre nó, pecíolo e folha correspondente) têm sido amplamente
utilizadas devido a importantes trade-offs observados nestas estruturas e suas relações
com as variáveis ambientais (ver em: Ackerly et al. 2002; Bruschi et al. 2003; Reich et
15
al. 2003; González-Rodríguez e Oyama 2005; Lambrecht e Dawson 2007; Uribe-Salas
et al. 2008). A área foliar e área foliar específica (SLA - área foliar por unidade de
massa foliar) têm sido fortemente relacionadas à eficiência no uso dos recursos e à
tolerância a estresses ambientais, principalmente ao estresse hídrico (Ackerly et al.
2000; Poorter 2009). Diversos estudos tem demonstrado que plantas de ambientes com
baixa precipitação apresentam folhas com baixo SLA (Fonseca et al. 2000; Bruschi et
al. 2003; González-Rodríguez and Oyama 2005; Uribe-Salas et al. 2008). Esta estratégia
em grande parte tem sido associada à eficiência no uso da água e a capacidade
fotossintética, otimizando o desempenho da planta de acordo com as condições
ambientais (Lázaro-Nogal et al. 2015; Scoffoni et al. 2015). Além disso, outros
caracteres funcionais dos metâmeros foliares também influenciam nas taxas
fotossintéticas da planta (Ackerly et al. 2000; Poorter 2009), como as características do
entre-nó e do pecíolo, que são importantes para o suporte da folha no que diz respeito ao
posicionamento espacial, à biomecânica e à hidráulica (Santiago et al. 2004).
A capacidade de modificar a estratégia reprodutiva a diferentes condições
ambientais podem contribuir significativamente para a amplitude de nicho e a extensão
da distribuição geográfica de uma espécie vegetal (Primack 1979; Cabaço and Santos
2012; Colautti and Barrett 2013; Delerue et al. 2013). Características das sementes estão
relacionadas com o recrutamento e têm implicações na aptidão e persistência das plantas
no ambiente (Cochrane et al. 2015). A produção de poucas sementes grandes versus
maior número de sementes pequenas, representa um trade-off chave na alocação de
recursos para a reprodução (Leishman 2001). De modo geral, o número de sementes se
traduz diretamente em sucesso reprodutivo das plantas, e frequentemente a produção de
maior número de sementes ocorre em detrimento do tamanho (Leishman et al. 2000).
No entanto, em diversas situações (ex. estresse hídrico, sombreamento, alta quantidade
16
de serrapilheira no solo ou a competição com a vegetação estabelecida) a estratégia de
produzir sementes grandes em detrimento da quantidade pode ser favorecida (Westoby
et al. 1996). Assim, diferentes pressões seletivas podem gerar variações no tamanho e
número das sementes produzidas pelas plantas entre e dentro das populações (Moles
and Westoby 2006; Souza et al. 2015b), afetando germinação e o estabelecimento
(Guariguata and Ostertag 2001). Variabilidade nas características das sementes entre e
dentro das populações pode aumentar a resiliência das espécies durante o período de
desenvolvimento inicial das plântulas, principalmente em ambientes sujeitos à
amplitudes extremas de temperatura e grande variabilidade na precipitação (Baker 1972;
Westoby 1998). No entanto, a relação da variação nas características das sementes com
o recrutamento em condições instáveis é pouco conhecida e muitas vezes é
desconsiderada nas avaliações do risco de extinção sob mudanças climáticas (Cochrane
et al. 2015).
Outra importante estratégia das plantas para tolerar estresses ambientais são os
ajustes no comportamento fenológico (Sultan 2003). Características relacionadas às
fenofases vegetativas em muitos casos podem ser atribuídas a tolerância ao estresse, por
exemplo, a marcante deciduidade em plantas observada em períodos mais severos de
estresse hídrico (Reich and Borchert 1984). Por outro lado, o período e a intensidade
reprodutiva podem refletir diretamente na capacidade competitiva da espécie, com
modificações que favoreçam, por exemplo, a formação e a dispersão dos diásporos
durante um período ideal para germinação das sementes (Singh and Kushwaha 2005;
Bustamante and Burquez 2008). Eventos fenológicos são regulados por características
endógenas associadas às variações do clima que regulam a época, a intensidade, a
duração e a periodicidade dos eventos (Ferraz et al. 1999). Espécies com ampla
distribuição apresentam diferenças fenológicas ao longo de gradientes geográficos e
17
ambientais (Blionis et al. 2001; Bustamante and Burquez 2008; Godoy et al. 2008).
Assim, mudanças ambientais podem alterar o comportamento fenológico das plantas e,
além disso, essas alterações podem afetar importantes interações com outros
organismos, como polinizadores, dispersores e predadores de sementes (Bustamante and
Burquez 2008).
A germinação das sementes representa uma das fases críticas do ciclo de vida
das plantas e determinam tanto a distribuição quanto à abundância das espécies nas
comunidades vegetais (Wulff 1986; Armstrong and Westoby 1993). Fatores bióticos e
abióticos afetam diferentemente na germinação (Baskin and Baskin 1998).
Especificamente em sementes zoocoricas dispersores podem desempenhar um
importante papel na dinâmica populacional das plantas, não apenas por carregar
sementes para longe da planta mãe, mas também por remover substância que inibem a
germinação das sementes (Robertson et al. 2006; Lessa et al. 2013). No entanto, este
efeito não é uniforme, nem é aplicável a todas as sementes zoocoricas (Figueroa and
Castro 2002). Por sua vez, o fogo é um importante fator abiótico que limita a
distribuição das espécies de planta (Pausas and Verdú 2005; Verdú and Pausas 2007),
sendo um agente evolutivo que pode interferir em diversos aspectos do
desenvolvimento das plantas, especialmente nas fases iniciais (Paula et al. 2009).
Sementes tendem a ser vulneráveis a altas temperaturas reduzindo a viabilidade
germinativa (Baskin and Baskin 1998). No entanto, para algumas espécies o fogo é
essencial na quebra de dormência provocado por altas temperaturas (Ribeiro et al. 2013)
e a fumaça ativa importantes genes relacionados germinação (Paula et al. 2009). O fogo
é um distúrbio comum no cerrado ha milhões de anos (Salgado-Labouriau et al. 1997) e
estudos recentes têm demonstrado adaptações fenotípicas e funcionais nas espécies
vegetais deste ambiente (Silva and Batalha 2010). No entanto, nas últimas décadas o
18
fogo tem se tornado mais frequente em ambientes de cerrado, principalmente devido a
ações antrópicas (Bond and Keeley 2005), e a maior frequência deste distúrbio pode
afetar a distribuição das espécies no cerrado.
Estudos sobre os níveis de variação intraespecífica em características
ecofisiológicas de espécies nativas dos biomas brasileiros são raros (mas veja Lemos
Filho et al. 2008), embora sejam fundamentais para a avaliação do potencial evolutivo
das espécies e populações frente as mudanças climáticas previstas para o século
presente. Variação intraespecífica, tanto entre como dentro de populações, tem sido
descrita para metâmeros foliares (Uribe-Salas et al. 2008), termotolerância do
fotossistema II (Barua et al. 2008), comportamento fenológico (Goulart et al. 2005) e a
morfologia das sementes (Souza et al. 2015b) para algumas espécies. Essa variação tem
sido associada às diferenças genéticas e/ou a plasticidade fenotípica (Lemos Filho et al.
2008). A plasticidade fenotípica representa a capacidade de um genótipo de produzir
diferentes respostas morfológicas e fisiológicas quando expostos a diferentes condições
ambientais (Sultan 1995; Lázaro-Nogal et al. 2015). Assim, a plasticidade pode
amortecer mudanças ambientais que ocorrem ao longo do ciclo de vida da planta,
aumentando a sua tolerância ao estresse, por exemplo, aclimatação de curto prazo para
luz e restrições hídricas. A plasticidade fenotípica pode também permitir a colonização
e o estabelecimento em diferentes habitats (Gimeno et al. 2008; Matesanz and
Valladares 2014). Por essa razão a plasticidade fenotípica tem sido considerada como
um importante mecanismo pelo qual os indivíduos podem enfrentar as variações
ambientais, sendo considerada essencial para evitar extinções locais frente a possíveis
mudanças climáticas (Matesanz et al. 2010; Hoffmann and Sgrò 2011). Estudos recentes
tem demonstrado que o grau de plasticidade varia entre as populações, sendo
frequentemente maior em ambientes mais heterogêneos (Gianoli 2004; Matesanz et al.
19
2010; Baythavong 2011; Lázaro-Nogal et al. 2015). No entanto, a plasticidade
fenotípica raramente tem sido considerada no contexto das respostas evolutivas das
plantas à mudança climática ao longo de intervalos de distribuição (Lázaro-Nogal et al.
2015).
OBJETIVO
O objetivo deste trabalho foi avaliar variações em caracteres funcionais dentro e
entre populações de Copaifera langsdorffii distribuídas ao longo de um gradiente
ambiental. Especificamente, testamos hipóteses relacionadas a variações em caracteres
morfológicos, fisiológicos, comportamentais e da plasticidade fenotípica destes traços
com fatores ambientais, focando a aridez e/ou a fertilidade do solo como drivers para
diferenciação populacional. De maneira inédita nós avaliamos caracteres funcionais de
uma espécie arbórea tropical ao longo de 600 km de sua distribuição cobrindo três
biomais e cinco fisionomias vegetais distintas. Ao longo desta tese discutimos a
importância das variações nos traços funcionais para distribuição de C. langsdorffii e
possíveis efeitos das mudanças climáticas em suas populações naturais nos seguintes
artigos: (Capítulo I) “Phenological variation within and among populations of
Copaifera langsdorffii in eastern tropical South America”; (Capítulo II) “Soil fertility
determines seed size/number trade-off of a widely distributed Neotropical tree along a
climatic gradient”; (Capítulo III) “Key factors affecting seed germination of Copaifera
langsdorffii, a Neotropical tree”; e (Capítulo IV) “Climatic heterogeneity as a
generator of phenotypic plasticity in functional leaf traits of a neotropical tree species
widely distributed”.
20
ESPÉCIE ESTUDADA
Copaifera langsdorffii Desf. (Figura 1) é uma espécie arbórea, com grande
variação em seu porte, dependendo do habitat de ocorrência (Carvalho 2003; Costa et
al. 2012). A espécie possui ampla distribuição, ocorrendo largamente na América do Sul
(Carvalho 2003). No Brasil, a espécie ocorre em fisionomias dos biomas Caatinga,
Cerrado, Mata Atlântica e Amazônia, desde a região norte ao sul do país (Almeida et al.
1998). C. langsdorffii possui folhas compostas, paripinadas, alternas, espiraladas com 4
a 12 folíolos alternos ou opostos (Almeida et al. 1998; Silva-Júnior 2005). A espécie
apresenta marcante queda foliar durante os meses mais secos, que é imediatamente
seguido pelo brotamento foliar (Pedroni et al. 2002; Fagundes 2014). A reprodução é
supra-anual com amadurecimento e dispersão dos frutos no período de seca entre os
meses de julho a setembro (Pedroni et al. 2002; Souza and Fagundes 2016). O fruto, ao
se abrir, expõe uma única semente elipsóide, negra e brilhante, parcialmente envolta por
um arilo amarelo-alaranjado (Carvalho 2003). C. langsdorffii apresenta diversos tipos
de dispersores generalistas, sendo os principais dispersores as aves (Rabello et al. 2010),
no entanto sementes caídas ao chão são carregadas e tem seu arilo retirado por formigas
(Leal and Oliveira 1998). As sementes possuem comportamento ortodoxo e o tamanho
das sementes e a remoção do arilo são fatores-chave na germinação de sementes de C.
langsdorffii (Souza and Fagundes 2014; Souza et al. 2015a).
ÁREAS DE ESTUDO
Foram selecionadas seis populações de Copaifera langsdorffii ao longo de 600
km combrindo três biomas no estado Minas Gerais-Brasil (Figura 2). Dados
meteorológicos dos últimos 54 anos (1961-2015) para cada população foram obtidos a
partir das estações meteorológicas mais próximas dos pontos de coleta junto ao Instituto
Nacional de Meteorologia Brasileiro (www.inmet.gov.br). Os dados meteorológicos
21
demonstram que a precipitação apresenta grande variação intra interanual entre as
populações. Nós calculamos a variação intra e interanual na precipitação das populações
estudadas usando o coeficiente de variação (CV = SD mean-1). A variabilidade intra e
interanual da precipitação foram altamente correlacionadas com a precipitação anual (r
= -0.88, P < 0.05 and r = -0.95, P < 0.05, respectively), mostrando que ambientes mais
xéricos também apresentam maior heterogeneidade na precipitação.
A partir dos dados meteorológicos foi calculado o índice de aridez (IA) para cada
população pela fórmula:
𝐼𝐴 = (𝑃
𝑃𝐸𝑇)
onde P é precipitação total do mês e PET a evapotranspiração potencial mensal em cada
local (Picotte et al. 2009). Assim como a precipitação, os dados de aridez mostram que
as populações ao norte estão localizadas em clima mais xérico e as ao sul em clima mais
úmido (Tabela 1), e também que as populações mais ao norte tendem a sofrer secas
mais prolongadas como pode ser observado na Figura 3. Deste modo, as populações
selecionadas neste estudo seguem um claro gradiente de aridez.
No geral, os ambientes estudados apresentam solos profundos, não
hidromórficos e ácidos (Embrapa 2013). Especificamente no ambiente de Campo
Rupestre Ferrugínoso o solo é superficial, pouco permeável e com alto teor de ferro
(Jacobi et al. 2007). Para caracterizar o solo em cada população foram coletadas três
amostras de solo (0-10 cm profundidade). Cada amostra era composta por 10 pontos,
coletados próximo aos indivíduos de C. langsdorffii selecionados neste estudo. As
amostras de solo foram secas ao ar livre e enviado para análise de fertilidade. A
caracterização do solo de cada população pode ser observada na Tabela 2. As
características dos solos foram comparadas entre as populações através Modelos
22
Lineares Generalizados (GLM) usando analise de contraste (Crawley 2000). No geral,
os resultados mostraram que as características do solo variaram entre as populações com
marcante diferença no ambiente de Campo Rupestre Ferrugínoso (Tabela 2), onde
foram encontrados os solos mais ácidos e com menor fertilidade.
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TABELAS
Tabela 1: Caracterização ambiental e climática de seis populações de Copaifera
langsdorffii. Valores de precipitação e temperatura média anual para as populações.
Média anual do Índice de Aridez. Os dados foram obtidos do Instituto Nacional de
Meteorologia (www.inmet.gov.br) para o período 1961-2015.
Descrição Lav Can Beh Par Moc Jap
Município Lavras Ibirité Belo Horizonte Paraopeba Montes Claros Japonvar
Coordenadas
21º15'S,
45º02'W
20°04’S,
43°59’W
19°53'S
43°58'W
19°20’S,
44°24’W
16o40’S,
43o48’W
15º58’S,
44º16’W
Altitude (m) 948 1423 842 763 645 804
Habitat Mata Atlântica Campo Rupestre
Ferrugínoso Mata Atlântica Cerrado Cerrado Caatinga
Precipitação
(mm) 1511.51 1490.12 1500.44 1295.27 1029.43 858.03
Variação
interanual (%) 18.06 21.35 21.94 22.22 26.24 30.68
Temperatura (°C) 20.02 20.74 21.54 21.29 22.97 24.23
Índice de aridez 1.25 1.12 1.21 1.03 0.72 0.59
35
Table 2. Fertilidade do solo de seis populações de Copaifera langsdorffii. H+Al = Potencial acidez; SB = Soma de bases; T= Capacidade de
troca catiônica; t= Capacidade efetiva de troca catiônica; M= Índice de saturação de alumínio; V = Saturação por bases. Os valores médios e o
desvio padrão (Sd) das características do solo são mostrados para cada população. Letras diferentes após a média e desvio padrão (Sd) indicam
diferenças significativas na análise de contraste em GLM (P < 0.05).
Populações Lav Can Beh Par Moc Jap
pH (in H2O) 5.10 (0.35)
a 4.50 (0.20)
b 5.27 (0.21)
a 5.33 (0.21)
a 5.30 (0.26)
a 5.57 (0.25)
a
H+Al (mmolc.dm-3
) 7.20 (2.11)b 20.31 (4.74)
a 5.24(0.49)
b 7.56 (1.94)
b 5.63 (1.10)
b 3.42 (0.67)
b
Al (mmolc.dm-3
) 0.84 (0.66)a 1.55 (0.67)
a 0.33(0.14)
a 1.17 (0.80)
a 1.43 (0.50)
a 0.39 (0.38)
a
Ca (mmolc.dm-3
) 2.05 (1.23)a 1.70 (0.29)
a 3.85(0.98)
a 2.46 (1.54)
a 1.29 (0.36)
a 1.72 (0.49)
a
Mg (mmolc.dm-3
) 0.63 (0.43)b 0.33 (0.03)
b 0.58(0.16)
b 1.22 (0.54)
a 0.68 (0.08)
b 0.91 (0.24)
b
P (mg.dm-3
) 3.33 (1.50)b 4.43 (0.55)
a 4.64(1.14)
a 2.60 (0.61)
b 1.33 (0.35)
b 1.97 (031)
b
K (mg.dm-3) 109.00 (41.61)
b 76.33 (14.29)
b 66.33(17.90)
b 182.67 (20.53)
a 166.00 (22.27)
a 86.33 (13.05)
b
SB (mmolc.dm-3
) 2.96 (1.75)a 2.22 (0.27)
a 4.60(0.89)
a 5.47 (1.33)
a 2.40 (0.37)
a 2.85 (0.54)
a
T 10.16 (1.05)b 22.50 (4.51)
a 9.84(0.54)
b 11.80 (0.18)
b 8.02 (0.84)
b 6.39 (1.15)
b
t 3.8 (1.19)a 3.77 (0.41)
a 4.93(0.78)
a 5.47 (1.33)
a 3.83 (0.23)
a 3.24 (0.57)
a
M 26.91 (23.57)a 40.13 (12.9)
a 6.92(3.63)
b 26.63 (21.50)
a 22.07 (15.84)
a 11.52 (11.07)
a
V 29.37 (18.73)a 10.28 (3.23)
b 46.56(6.99)
a 35.46 (17.35)
a 30.26 (6.52)
a 45.57 (3.36)
a
FIGURAS
Figura 1: Indivíduos adultos de Copaifera langsdorffii em diferentes ambientes: A) Mata
Atlântica; B) Cerrado; C) Campo Rupestre Ferrugínoso. Fases reprodutivas de Copaifera
langsdorffii: D) Flores abertas; E) Frutos imaturos; F) Frutos maduros. Fases vegetativas de
Copaifera langsdorffii: G) Brotação; H) Folhas novas; I) Folhas maduras.
37
Figura 2: Populações de Copaifera langsdorffii amostradas neste estudo (códigos das
populações Tabela 1).
38
Figura 3: Médias mensais históricas dos últimos 54 anos para o índice de aridez de cada
população de Copaifera langsdorffii analisada neste estudo. Os símbolos representam as
diferentes populações: triângulo fechado = Lav; circulo fechado = Can; quadrado fechado =
Beh; quadrado aberto = Par; triângulo aberto = Moc; circulo aberto = Jap; Cruz = índice de
aridez com valor < 0.5, indicando condições de hiperaridez (códigos das populações na
Tabela 1).
39
Capítulo I: Phenological variation within and among populations of
Copaifera langsdorffii in eastern tropical South America
Matheus Lopes Souza1; Walisson Kenedy Siqueira
2; Cristina Crespo Bastias
3; Marcílio
Fagundes2; Fernando Valladares
3;4; Jose Pires de Lemos Filho
1
1Departamento de Botânica, Universidade Federal de Minas Gerais, ICB-UFMG, Belo
Horizonte, 31270, Brazil; 2Departamento de Biologia Geral, Universidade Estadual de
Montes Claros, CCBS-UNIMONTES, Montes Claros, 39401, Brazil; 3LINCGlobal
Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias
Naturales, MNCN-CSIC, Madrid, 28006, Spain; 4Departamento de Biología y Geología
ESCET, Universidad Rey Juan Carlos, Móstoles, 28933, Spain.
* For correspondence: E-mail [email protected]. Av. Avenida Presidente
Antônio Carlos, 6627 - Pampulha, Belo Horizonte - MG, 31270-901. Phone: (031)
3409-2568; Fax: (031) 3409-2567.
40
ABSTRACT 1
Phenological studies are very helpful to understand population dynamics and 2
niche width of plant species. The plant phenology is closely related climatic variables, 3
this way, dramatic changes in the climate are challenge for natural plant population. We 4
tested the effect of intra-annual variation of rainfall in the phenology within and among 5
populations of Copaifera langsdorffii along the rainfall gradient. We hypothesized that 6
plants in populations from environments with greater heterogeneity in rainfall are more 7
likely to adjust their phenology according the environmental conditions change. Six 8
populations of C. langsdorffii were selected along a climatic gradient from semi-arid to 9
more rainy regions covering three different biomes (Caatinga, Cerrado, and Atlantic 10
Forest). Our results have showed that the populations of C. langsdorffi adjust the 11
phenological pattern according to environmental conditions of the region they are 12
located. In general, the reduction in rainfall affected directly the vegetative phenology. 13
C. langsdorffii individuals in all populations began drop the leaves earlier in drought 14
years. Changes in phenology influenced by environmental conditions can significantly 15
contribute to the niche width of a species, which could explain the success of C. 16
langsdorffii over a range of different types of habitats. The plasticity that had been 17
observed in all populations studied for vegetative phenology, mainly for leaf fall, 18
modulated by water availability is an important factor for persistence of species forward 19
future climate change. 20
Key works: Copaifera langsdorffii; aridity gradient; climate changes; plasticity; 21
differentiation of populations; Leaf fall. 22
23
41
INTRODUCTION 1
Phenology is an important factor that drives population dynamics of plants 2
(Walther et al. 2002; Chambers et al. 2013) and niche width of plant species (Goulart et 3
al. 2005; Godoy et al. 2008; Wolkovich and Cleland 2014). Adaptive changes in the 4
time and duration of vegetative and reproductive phases can increase the capacity of 5
established itself in a given habitat, and this could determine the distribution of the 6
species (Pau et al. 2011). In seasonal environments the vegetative phenology (i.e cycles 7
of leaf flushing and leaf fall) is attributed to maintenance of the water status with 8
deciduousness as a strategy to avoid water loss during periods of drought (Reich and 9
Borchert 1984; Toledo et al. 2012). On the other hand, the time and intensity of 10
flowering and fruiting play an important role on reproductive success. The time of 11
fruiting can directly reflect in the competitive ability like the dispersion of the seeds 12
only happen in an ideal conditions for the germination (Blionis et al. 2001; Singh and 13
Kushwaha 2005; Bustamante and Burquez 2008). 14
The phenological events of plants are regulated by endogenous factors 15
associated with climate variations that govern the timing, intensity and duration of 16
events (Silveira et al. 2013; Azevedo et al. 2014; Pezzini et al. 2014). In seasonal 17
environments, plant growth and reproduction are limited by water availability, since 18
rainfall are concentrated in few months with large intra- and inter-annual variation 19
(Walker et al. 1995; Chesson et al. 2004; Liu et al. 2016). Multiple phenological 20
strategies to assure the persistence and reproductive success in seasonal environments 21
are observed (Venable 2007; Silveira et al. 2013; Azevedo et al. 2014; Pezzini et al. 22
2014). Besides, an increase in climate unpredictability and extreme events are expected 23
due to the climatic changes (IPCC, 2014), thus phenological shifts would be able to 24
ensure populations persistence. Changes in environmental conditions and in resource 25
42
availability affect the plant phenology and other associated trophic levels, endangering 1
large portion of biodiversity (Bustamante and Burquez 2008; Bewick et al. 2016). Thus, 2
the phenotypic plasticity is crucial to the persistence of these organisms to new 3
environments (Nicotra et al. 2010; Matesanz and Valladares 2014). However, 4
phenotypic plasticity varies widely among and within species. It depends on the 5
intensity and direction of environmental change, life history characteristics and 6
intraspecific genetic variation (Nicotra et al. 2010; Lázaro-Nogal et al. 2015; Nunney 7
2016). 8
Copaifera langsdorffii Desf (Fabaceae) is a tropical tree with wide distribution 9
in South America, occurring in different biomes as Caatinga, Cerrado, Atlantic Forest 10
and Amazon (Almeida et al. 1998). This species has populations under different 11
environmental conditions, such as variation in rainfall, temperature, solar radiation and 12
soil fertility (Almeida et al. 1998; Carvalho 2003; Costa et al. 2012). For this reason, 13
significant differences in phenological response of geographic and environmental 14
gradients are expected among and within populations (Rathcke and Lacey 1985). 15
Moreover the different levels of plasticity and/or genetic variability can contribute much 16
more for those differences (Goulart et al. 2005; Wilczek et al. 2010). As C. langsdorffii 17
is widely spread along the America under different environmental pressure and stress, it 18
makes C. langsdorffii an excellent model to evaluate consequences of climate change on 19
natural populations, since significant changes are observed in the functional traits in a 20
favorable way to the environmental pressures imposed on different populations (Gianoli 21
and González-Teuber 2005; Lázaro-Nogal et al. 2015). Although there are relatively 22
few studies of phenological patterns of several species in the eastern tropical south 23
America (Pedroni et al. 2002; Goulart et al. 2005; Morellato et al. 2013; Silveira et al. 24
2013; Pezzini et al. 2014) and fewer about changes of the phenological patterns among 25
43
populations (Goulart et al. 2005; Toledo et al. 2012). Plants are closely linked to the 1
climate conditions of their environment, and shifts in these conditions affect 2
phenological responses of natural plant populations (Cleland et al. 2007). So it is 3
important to examine the capacity of phenological adjust of different populations along 4
a climatic gradient to cope with the new environmental conditions. We hypothesized 5
that plants from more arid populations and with more inter-annual heterogeneity in 6
rainfall would present higher capacity of adjust in their phenology according the 7
environmental conditions change. For this propose we evaluated the effect of intra-8
annual variation of rainfall in the phenological responses within and among populations 9
of C. langsdorffii distributed along a rainfall gradient. 10
11
MATERIAL AND METHODS 12
Study area 13
Six populations of C. langsdorffii were selected along a rainfall gradient in the 14
Minas Gerais state, southeastern Brazil. We obtained climatic data for the last 54 years 15
(1961-2014) for each are of study from the Brazilian National Institute of Meteorology 16
(INMET, 2015). A clear aridity gradient was assured for this sampling procedure which 17
north populations located in more xeric climate (Table 1). We calculate the intra inter-18
annual variation in annual rainfall of populations studied as coefficients of variation 19
(CV = SD mean-1). The variability of intra and inter-annual rainfall was highly 20
correlated whit annual rainfall (r = -0.88, P < 0.05 and r = -0.95, P < 0.05, 21
respectively), showing that more xeric environments also show higher temporal 22
heterogeneity in precipitation. During the study a large difference in rainfall between 23
44
the years (2013 and 2014) was found with considerable reduction in rainfall in 2014 1
(Table 1 and Fig 1). 2
3
Phenological monitoring 4
Twenty-seven adult trees of C. langsdorffii were randomly selected in each 5
population. The trees were monitored monthly for 24 months, from January 2013 to 6
December 2014. In each individual, three vegetative phenophases were observed: leaf 7
fall, leaf flushing and mature leaf; and three reproductive phenophases: open flowers, 8
unripe fruit, and ripe fruit. Leaf fall was marked by visible canopy defoliation, presence 9
of senescent leaves, and ease of falling leaves by wind action. Leaf flushing was 10
identified by the presence of small red leaves, after the period of total leaf fall. Mature 11
leaves were identified by fully leaf size and dark green. The open flower phenophase 12
was characterized as the period in which the tree exhibited flowers in anthesis. The 13
unripe fruits phase was characterized by presence of developing fruits. The ripe fruit 14
phase was observed diaspores were brown and ready to be dispersed, when the fruit 15
open exposes a black seed, partially wrapped in a yellow-orange aril. We evaluated 16
monthly the activity of each phenophase for all individuals studied. Phenological 17
activity was evaluated by observing the presence or absence of each phenophase. 18
19
Data analysis 20
The rainfall was correlated with the vegetative and reproductive phenophases 21
using a Spearman correlation test. The phenological events were correlated to total 22
rainfall of the previous month to the event. 23
45
To test for seasonality in vegetative and reproductive phenophases, circular 1
statistics were made with the frequency distribution of phenophases for the 27 2
individuals of each population in the years of 2013 and 2014. The frequency of 3
occurrence was considered to be the proportion of individuals in each phenophase. The 4
months were converted into angles, with intervals of 30°, and then the average angle or 5
average date (μ), the circular concentration (r), and the circular standard deviation 6
(CSD) were calculated. The average angle (μ) is the period around which a determined 7
phenophase was recorded in most individuals. A Rayleigh test (Z) was used to 8
determine the significance of the angle. When the average angle is significant, there is 9
seasonality of the phenophase. The intensity of circular concentration around the 10
average angle (r) varies from 0 (phenological activity uniformly distributed throughout 11
the year) to 1 (phenological activity concentrated in a period of the year). Phenological 12
differences among and within populations were performed with pairwise Watson–13
William F-tests in circular statistic. These analyses were performed with the ORIANA 14
package (Kovach 2007). 15
We performed generalized linear models (GLM) to test if the duration of leaf fall 16
and reproductive periods varied within and among populations. The duration of leaf fall 17
period was determined for each individual by the interval between the start of leaf fall 18
until the start of leaf flushing. In turn, the duration of the reproductive period was 19
determined by the interval between the start of open flowers until the start of ripe fruits. 20
In this analysis we used the duration of leaf fall and reproductive periods as responses 21
variables and the populations and years of study as explanatory variable. The 22
differences in the duration of leaf fall and reproductive periods within and among 23
populations were evaluated by contrast analysis (Crawley 2000). 24
46
All GLMs were performed using the R software (R Core Team 2013), with 1
appropriate error distribution considering the nature of each response variable, 2
following by model criticism via residual analysis (Crawley 2000). All created models 3
were compared with the null model and the appropriateness of the models was tested by 4
residue analysis (Crawley 2000). 5
6
RESULTS 7
Vegetative phenophases 8
Individuals of Copaifera langsdorffii of the populations studied showed marked 9
seasonality in vegetative phenophases with total deciduousness in dry season (Table 2). 10
Our results showed that the vegetative phenophases were correlated with rainfall (Table 11
3). In all populations the phenophases ‘leaf fall’ and ‘leaf flushing’ were negatively 12
correlated with rainfall, except in Can population which was not observed correlation 13
between ‘leaf flushing’ and rainfall (Table 3). Instead, ‘mature leaves’ was positively 14
correlated with rainfall (Table 3). 15
Vegetative phenophases showed temporal differences within and among 16
populations (Table 4). Within populations significant differences were observed in leaf 17
fall and leaf flushing between the years of study in all populations except in Can 18
population (Table 4). For mature leaves differences were observed between the years of 19
study only in Lav, Beh and Jap populations, the other populations did not varied (Table 20
4). Among populations, to year of 2013 (the rainiest year), our results showed that 21
individuals of Can, Moc and Jap populations began the leaf fall in the end of the wet 22
season (March-May; Fig 2) with a peak in the beginning of the dry season (June-July; 23
Fig 2). The Lav, Beh and Par populations keeps the leaves for longer time, with the start 24
47
of leaf fall in the beginning of the dry season (May-June; Fig 2) and peak deciduousness 1
in the middle of the dry season (July-August; and Fig 2). Leaf fall was followed by leaf 2
flushing in the end of dry season and mature leafs were maintained during the all wet 3
season (Fig 2). In the year of 2014 (the driest year) although, our results demonstrate 4
that the vegetative phenophases were anticipated in all populations studied (Fig 2). 5
Thus, a smaller difference in vegetative phenology among populations was observed in 6
the year rain lower compared to the wet year. 7
The duration of the leaf fall period varied among populations, in the two 8
monitored years of study (Fig. 3A). In general, individuals in Can, Moc and Jap 9
populations remain more time losing leaves, with some individuals in these populations 10
presenting between seven e eight months of deciduousness. On the other hand, in Lav, 11
Beh and Par populations the period of losing leaves does not exceed 6 months. Our 12
results also showed the reduction in the duration of the leaf fall period to the driest year 13
in Can and Jap populations when compared with the rainiest year, indicating that the 14
leaf fall in these populations was more abruptly in the driest year. 15
16
Reproductive phenophases 17
We observed a considerable reduction in the number of reproductive individuals 18
in the drier year. In 2013 85.2% of individuals analyzed produced flowers and 80.3% 19
completed the reproductive phase dispersing seeds, while in 2014 43.8% of individuals 20
produced flowers and only 22.8% dispersed the seeds. Due to the low proportion of 21
reproductive individuals in 2014 the analysis for reproductive phenophases were 22
conducted only for the year 2013. 23
48
The reproductive phenophases of this species were also correlated with rainfall. 1
In all populations the phenophase open flower was positively correlated with rainfall 2
and ripe fruit was negatively correlated with rainfall, these results were observed for 3
activity and intensity phenological (Table 3). The activity of phenophase unripe fruit 4
was negatively correlated with rainfall in Par population and intensity this phenophase 5
was positively correlated with rainfall in Lav population (Table 3). For other 6
populations there was no correlation between phenophase unripe fruit and rainfall 7
(Table 3). 8
All reproductive phenophases were seasonal (Table 2) and varied among 9
populations (Table 4). The flowers were produced during the wet season. Individuals of 10
C. langsdorffii in Lav, Can and Beh populations presented peak flowers early in the 11
year, between the months of January and February (Fig 4), while in Par, Moc and Jap 12
presented peak flowers a little later, between the months of February and March (Fig 4). 13
The fruits development occurred during the wet and dry seasons. In Lav, Can, Beh and 14
Par populations the phenophases fruit unripe was long, occurring among the months of 15
February to August (Fig 4). In Moc and Jap populations this phenophase was shorter, 16
only among the months of March to June (Fig 4). Dispersal of seeds occurred in dry 17
season. In Moc and Jap populations the phenophase ripe fruit between the months of 18
May and July, with peak dispersion in July. Already Lav, Can, Beh and Par populations 19
presented phenophase ripe fruit from July to September, with peak dispersion in August 20
(Fig 4). 21
The duration of the reproductive period varied among populations (Fig. 3B). 22
Individuals of C. langsdorffi in Moc and Jap populations showed shorter duration of the 23
reproductive period (open flowers to ripe fruits) when compared with the others 24
populations. In Moc and Jap populations the reproductive period lasted at most 5 25
49
months, while that in Lav population some individuals presenting 9 months 1
reproductive period. 2
DISCUSSION 3
In this study, we demonstrate that inter-annual differences in rainfall modulate 4
the phenology of individuals of Copaifera langsdorffii of the populations studied. The 5
year 2014 was marked by a severe drought in all populations, with reduction of 6
approximately 40% of rainfall compared with the historical average. This reduction in 7
rainfall affected directly the response of vegetative phenological of individuals of C. 8
langsdorffii in all studied populations. In general, the individuals of C. langsdorffii 9
started leaf fall early in drought year. Our results also show less differentiation in 10
vegetative phenology among populations in the year of low annual rainfall. These 11
differences between years point out that the plasticity in the vegetative phenology is 12
modulated by water availability. The phenotypic plasticity in phenologycal events has 13
been pointed as essential to prevent local extinctions of species under a possible 14
climate change scenario (Matesanz et al. 2010; Hoffmann and Sgrò 2011). 15
Individuals from more arid sites (Moc and Jap) presented leaf fall early even in 16
the wetter year. They also presented a longer time of deciduousness when compared 17
with populations from wetter sites. Similar results to leaf fall in arid sites were also 18
found in Can population, although this population is located in an environment with 19
high rainfall. This apparently contradictory result could be related with the specificity of 20
the ferruginous rock grassland environmental conditions, characterized by low fertility 21
soils, and spite of high rainfall has low capacity of soil water storage (Jacobi et al. 22
2007). The main differences among populations were related to leaf fall, whit starts leaf 23
fall earlier in the populations of more arid sites, as described by Goulart et al. (2005) for 24
populations of another legume tree. The intensity and duration of leaf fall is directly 25
50
related to the availability of water in the environment (Walker et al. 1995; Silveira et al. 1
2013; Liu et al. 2016), varying among populations as demonstrated here. During the dry 2
period there is higher incidence of solar radiation with an increase on 3
evapotranspiration which and combined with the hydric deficit affects promote 4
limitation on stomatal openness reducing transpiration, damaging the photosynthetic 5
apparatus and reducing efficiency in water use (Franco 1998; Meinzer et al. 1999; 6
Lemos Filho 2000). Thus the deciduousness during periods of limited water is an 7
important strategy developed to reduce this stress by means of leaf loss, which prevents 8
transpiration and dehydration even more pronounced during this period (Borchert 1980; 9
Reich and Borchert 1984). Moreover, the reduction in transpiration is important 10
mechanism return of internal water levels in plant (Borchert 1980; Reich and Borchert 11
1984). This strategy enables leaf sprouting even in the dry season, pattern observed here 12
in C. langsdorffii. This sprouting during the dry season also has been described as 13
important anti herbivory escape strategy (Forister 2005; Fagundes 2014). 14
In all C. langsdorffii populations significant differences were observed in the 15
reproductive activity between the years of study. The reproductive pattern for C. 16
langsdorffii is described as supra-annual, with years of massive production of flowers 17
and seeds followed by years where reproduction can be drastically reduced (Pedroni et 18
al. 2002; Souza et al. 2015). A key element for the success of supra-annual reproduction 19
is the synchronism reproductive (Kelly and Sork 2002; Koenig and Knops 2005). Our 20
results demonstrate strong spatial reproductive synchrony in populations distributed 21
across 600 km. The main evolutionary advantages of supar-annual reproduction in 22
plants are increasing pollination efficiency, and the predator satiation (Silvertown 1980; 23
Sork 1993; Kelly and Sork 2002). Despite the spatial synchrony, our results also 24
showed temporal differences in the production of flowers and fruit development time 25
51
among populations. Individual in wetter environments produce flowers early and fruits 1
have higher development time when compared to individual in xeric environments. 2
Precipitation has been suggested as the primary cause of variations in the start and 3
duration of reproduction seasonal environments (Petit 2001; Borchert et al. 2004). The 4
lowest levels of stress that plants of wetter sites are subjected allow a speedy recovery 5
after dry period (Toledo et al. 2012) allocating resource for flower production. In 6
addition, more time for development of the seed generate larger and more vigorous 7
seeds (unpublished data), important features for the development of seedlings in 8
competitive environments (Leishman 2001; Yanlong et al. 2007; Souza and Fagundes 9
2014). 10
Our study showed the populations of C. langsdorffi adjust the phenological 11
behavior according to environmental conditions of each population, this feature can 12
significantly contribute to the niche breadth of a species, which could explain the 13
success of C. langsdorffii over a range of different types of habitats across its wide 14
geographic distribution. Furthermore, the phenotypic plasticity observed in all 15
populations studied for vegetative phenology, mainly for leaf fall, in terms of 16
adjustments to the start and duration modulated by water availability is an important 17
factor for persistence of species forward future climate change. 18
19
ACKNOWLEDGEMENTS 20
We thank all the collaborators of the Plant Physiology Laboratory - UFMG, 21
Conservation Biology Laboratory – UNIMONTES and directors of Paraopeba National 22
Forest (FLONA-PARAOPEBA) for logistical support in the fieldwork. This study was 23
carried out with financial support from CNPq and FAPEMIG. This work was conducted 24
52
with a scholarship supported by the International Doctoral Sandwich Program (PDSE). 1
Financed by CAPES – Brazilian Federal Agency for Support and Evaluation of 2
Graduate Education within the Ministry of Education of Brazil. We also thank all the 3
collaborators Ecology and Global Change Group of National Museum of Natural 4
Sciences (MNCN-CSIC), Madrid-Spain. 5
6
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60
TABLES
Table 1: Environment and climatic characterization of Copaifera langsdorffii populations. Population values of annual rainfall and annual
temperature are means. Data were obtained from the Brazilian National Meteorology Institute (www.inmet.gov.br) for the period 1961-2014.
Population Coordinates Habitat
Annual rainfall (mm)
Historic
Annual rainfall (mm)
2013
Annual rainfall (mm)
2014
Annual temperature (°C)
Historic
Jap 15º58’S, 44º16’W Caatinga 858.03 1108.4 605.1 24.23
Moc 16o40’S, 43o48’W Cerrado 1029.43 1255.1 478.7 22.97
Par 19°20’S, 44°24’W Cerrado 1295.27 1155.4 551.2 21.29
Beh 19°53'S 43°58'W Atlantic forest 1500.44 1573 944.1 21.54
Can 20°04’S, 43°59’W Ferruginous rock grassland 1490.12 1755.7 918.7 20.74
Lav 21º15'S, 45º02'W Atlantic forest 1511.51 1380.6 1087.6 20.02
61
Table 2: Seasonality in vegetative and reproductive phenophases among and within of populations of Copaifera langsdorffii.
Jap Moc Par Beh Can Lav
R Z R Z r Z R Z r Z R Z
Leaf fall -2013 0.55 49.44*** 0.70 57.35*** 0.79 52.92*** 0.89 51.75*** 0.70 50.82*** 0.75 48.34***
Leaf fall -2014 0.72 43.48*** 0.71 49.18*** 0.87 50.33*** 0.91 41.17*** 0.76 50.39*** 0.84 54.03***
Leaf flushing -2013 0.91 42.59*** 0.78 41.02*** 0.97 28.85*** 0.92 40.96*** 0.78 37.11*** 0.98 30.70***
Leaf flushing -2014 0.92 39.38*** 0.85 34.48*** 0.89 24.49*** 0.90 26.60*** 0.76 21.71*** 0.97 33.53***
Mature leaf -2013 0.50 11.37*** 0.39 8.68*** 0.41 11.00*** 0.39 10.34*** 0.38 11.92*** 0.41 11.29***
Mature leaf -2014 0.21 14.77*** 0.18 10.05*** 0.20 10.91*** 0.20 9.95*** 0.22 9.20*** 0.21 10.80***
Flower -2013 0.89 28.78*** 0.82 32.15*** 0.94 46.72*** 0.97 30.82*** 0.94 24.76*** 0.96 49.22***
Unripe fruit -2013 0.81 50.52*** 0.60 38.22*** 0.50 43.94*** 0.77 56.48*** 0.51 37.15*** 0.49 45.12***
Ripe fruit -2013 0.85 40.97*** 0.79 41.55*** 0.85 61.01*** 0.93 28.36*** 0.90 33.19*** 0.92 40.49***
r= Intensity of circular concentration around the average angle varies from 0 (phenological activity uniformly distributed throughout the year) to
1 (phenological activity concentrated in a period of the year); Z= Rayleigh test. (***P < 0.001; **P < 0.01; *P < 0.05; NS P>0.05 in Z)
62
Table 3. Spearman correlations between the rainfall and the phenophases in different
populations of Copaifera langsdorffii from January 2013 to December 2014 for
vegetative phenophases and from January 2013 to December 2013 for reproductive
phenophases.
Phenophases Jap Moc Par Beh Can Lav
Activity index Leaf fall -0.39 -0.36 -0.33 -0.33 -0.27 -0.39
Leaf flushing -0.26 -0.25 -0.15 -0.19 NS -0.20
Mature leaf 0.33 0.29 0.24 0.30 0.16 0.30
Open flower 0.47 0.41 0.49 0.68 0.10 0.70
Unripe fruit NS NS -0.13 NS NS NS
Ripe fruit -0.32 -0.27 -0.69 -0.26 -0.29 -0.34
Values shown for Spearman correlations (p<0.05). NS= Non-significant results (p
>0.05).
63
Table 4. Mean values in vegetative and reproductive phenophases among and within of populations of Copaifera langsdorffii.
Jap Moc Par Beh Can Lav
µ CSD µ CSD µ CSD µ CSD µ CSD µ CSD
Leaf fall -2013 200.47°aB 62.26° 187.016°aC 48.67° 218.53°aA 39.44° 222.11°aA 28.26° 179.80°aC 48.81° 213.25°aA 43.05°
Leaf fall -2014 180.00°bC 46.91° 158.492°bD 47.577° 205.47°bA 30.64° 197.74°bA 25.26° 192.40°aB 42.78° 192.70°bB 33.47°
Leaf flushing -2013 270.79°aA 24.33° 247.64°aB 40.13°a 278.68°aA 15.38° 276.98°aA 22.81° 257.14°aB 40.40° 273.22°aA 11.69°
Leaf flushing -2014 226.92°bC 24.11° 221.59°bC 32.96°b 259.93°bA 27.82° 246.27°bB 26.60° 263.52°aA 42.87° 248.05°bB 15.28°
Mature leaf -2013 69.85°aB 96.57° 53.03°aB 103.88° 81.09°aA 102.57° 75.04°aA 104.16° 54.89°aB 104.92° 79.81°aA 102.80°
Mature leaf -2014 35.67°bB 101.67° 34.36°aB 106.23° 62.50°aA 102.33° 46.34°bA 103.44° 59.96°aB 100.40° 51.22°bB 101.91°
Flower -2013 54.60°A 27.12° 38.28°B 36.27° 31.74°B 20.34° 24.83°C 14.98° 23.17°C 20.09° 20.20°C 54.60°
Unripe fruit -2013 113.59°B 37.20° 94.47°C 58.40° 130.93°A 67.22° 113.03°B 41.73° 123.06°B 66.86° 124.87°B 68.19°
Ripe fruit -2013 186.72°C 32.93° 175.11°D 38.98° 219.43°A 32.40° 194.61°B 22.30° 221.51°A 26.34° 222.74°A 186.72°
µ= Mean Vector; CSD= Circular Standard Deviation. Lowercase letters comparison vegetative phenophases within populations between years of
collecting 2013 and 2014. Capital letters comparison vegetative phenophases among populations. Different letters P<0.05.
64
FIGURES
Fig. 1: Rainfall monthly for populations studied of Copaifera langsdorffii. A) Lav; B)
Can; C) Beh; D) Par; E) Moc; and F) Jap. Historical monthly average of 54 years for
rainfall of locations of Copaifera langsdorffii populations.
65
Fig. 2: Activity index for the vegetative phenophases and monthly rainfall during the
study in Copaifera langsdorffii for populations A) Lav; B) Can; C) Beh; D) Par; E)
Moc; and F) Jap. The symbols represent the following phenophases: Closed triangles=
Mature leaf; Closed circles= Leaf flushing; Closed squares= Leaf fall.
66
Fig 3: Variation in the duration of leaf fall (A) and reproductive (B) periods in
Copaifera langsdorffii populations for years of 2013 (black bar) e 2014 (gray bar).
Population means and SE are shown. Arrow indicating gradient mesic (M) to xeric (X)
sites.
67
Fig. 4: Activity index for the reproductive phenophases and monthly rainfall during the
study in Copaifera langsdorffii for populations A) Lav; B) Can; C) Beh; D) Par; E)
Moc; and F) Jap. The symbols represent the following phenophases: Closed triangles=
Ripe fruit; Closed circles= Unripe fruit; Closed squares= Flower.
65
Capítulo II: Soil fertility determines seed size/number trade-off of a widely
distributed Neotropical tree along a climatic gradient
Matheus Lopes Souza1,*
, Marcilio Fagundes2, Maria Bernadete Lovato
3, Fernando
Valladares4,5
and José Pires de Lemos Filho1
1Departamento de Botânica, Universidade Federal de Minas Gerais, ICB-UFMG, Belo
Horizonte, 31270, Brazil. 2Departamento de Biologia Geral, Universidade Federal de Minas
Gerais, ICB-UFMG, Belo Horizonte 31270, Brazil; 3Departamento de Biologia Geral,
Universidade Estadual de Montes Claros, CCBS-UNIMONTES, Montes Claros, 39401,
Brazil; 4LINCGlobal Departamento de Biogeografía y Cambio Global, Museo Nacional de
Ciencias Naturales, MNCN-CSIC, Madrid, 28006, Spain; 4,5
Departamento de Biología y
Geología ESCET, Universidad Rey Juan Carlos, Móstoles, 28933, Spain.
* For correspondence: E-mail [email protected]. Av. Avenida Presidente Antônio
Carlos, 6627 - Pampulha, Belo Horizonte - MG, 31270-901. Phone: (031) 3409-2568; Fax:
(031) 3409-2567.
66
ABSTRACT 1
Aims We evaluated variation in seed traits and seed allocation of the widespread Neotropical 2
tree Copaifera langsdorffi. We hypothesized a seed size/number trade-off in populations of 3
environments with limited resource availability (low soil fertility and rainfall), determining 4
the production of larger seeds and in lower number. 5
Methods Five populations of C. langsdorffii were analysed covering a rainfall gradient in soils 6
with different fertility in the three biomes where the species occurs (Caatinga, Cerrado, 7
Atlantic Forest). 8
Results An independent effect of soil fertility and rainfall on seed mass was found, but the 9
number of seeds was only affected by rainfall. The seed size/number trade-off was determined 10
only by soil fertility. The results showed that low fertility soil is a key factor for size/number 11
trade-off in C. langsdorffii determining the production of large seeds in the poorest soil. 12
However, populations from sites with lower resource limitation exhibited lack of seed size/ 13
number trade-off, with populations in more mesic environments producing not only larger 14
seeds but also in higher number. A wide phenotypic variation in both seed mass and number 15
was observed especially in sites with high sazonality and inter-annual variability in 16
precipitation. 17
Conclusion The high capacity of C. langsdorffi to adjust the reproductive strategy according 18
to environmental conditions can significantly contribute to the niche breadth of the species, 19
and represents an important attribute for its persistence under future climate changes. 20
21
Keywords: Reproductive strategy; Soil fertility; Masting fruiting; Niche breadth; Climate 22
changes; Copaifera langsdorffii. 23
24
67
INTRODUCTION 1
The capacity to modulate the reproductive allocation to different environmental 2
conditions can substantially contribute to the niche breadth and the extension of the 3
geographical distribution of a plant species (Primack 1979; Cabaço and Santos 2012; Colautti 4
and Barrett 2013; Delerue et al. 2013). The resource allocated to reproduction expresses the 5
success of the plants to produce propagules and is an important measure of plant fitness 6
(Harper and Ogden 1970). However, reproduction is widely recognized as costly and due to 7
limited resources in natural conditions a trade-off among the allocation recourse for 8
reproduction and other drains of plants (Chapin, 1991; Obeso 2002; Colautti and Barrett 9
2013). Resource allocation to reproduction varies according to life history of plant and the 10
needs of plants throughout their life cycle in different environmental conditions (Harper and 11
Ogden 1970; Koenig and Knops 2005; Wong and Ackerly 2005; Delerue et al. 2013; Wang et 12
al. 2015). In general, plants tend to allocate higher proportion of their energy to reproduction 13
in environments with limited resources (Primack 1979; Cabaço and Santos 2012; Wang et al. 14
2016). However, some studies have shown the contrary (Harper and Ogden 1970; Matlaga 15
and Horvitz 2015; Yuan et al. 2016). 16
One of the key processes that optimize reproductive allocation of plants in different 17
environments is the seed size/number trade-off (Venable 1992; Paul-Victor and Turnbull 18
2009). In general, the seed number translates directly into plant reproductive success and 19
often the production of more seeds occurs in detriment of their size (Westoby et al. 1992; 20
Leishman et al. 2000). However, in many situations (water stress, soil conditions, shading or 21
competition with established vegetation), the production of large seeds can be favored over 22
seed number (Westoby et al. 1996). Strategies with respect to variations in the size and 23
number of seeds produced by plants affect important ecological processes especially those 24
related to germination and establishment in different habitats (Guariguata and Ostertag 2001; 25
68
Souza and Fagundes 2014). These variations in seed production can increase resilience of 1
species during the initial growth period of seedlings, particularly in environments subject to 2
extreme temperature ranges and a great variability in the precipitation throughout the year 3
(Baker 1972; Westoby 1998). Seedling initial size is crucial for survival in stressful 4
environments and this is determined by seed size (Baker 1972; Hanley et al. 2007). However, 5
the variation of seed traits in unstable conditions is still little known and its importance under 6
climate change is often ignored (Cochrane et al. 2015). 7
Species with wide distribution generally encompass great spatial variation in soil and 8
climate conditions, making them excellent models to evaluate consequences of environmental 9
change on natural populations, since variations in functional traits are found in a way to favor 10
the persistence of populations (Gianoli and González-Teuber 2005; Lázaro-Nogal et al. 2015, 11
Ribeiro et al. 2016). The fertility of the soil and climatic conditions are key factors that 12
determine the functional traits in plant species (Ramírez-Valiente et al. 2009; Yuan et al. 13
2016; Pontara et al. 2016). Changes in climate and landscape alter the environmental 14
conditions and the availability of resources, which can endanger large portion of biodiversity 15
(Nicotra et al. 2010). 16
Studies which encompass variation of seed traits in populations from different 17
environments are scarce for Neotropical plants (Lovato et al. 1994; Lacerda et al. 2004; 18
Goulart et al. 2006; Sales et al. 2013). In this study, we evaluated variations in seed 19
size/number trade-off along rainfall and soil fertility gradients in populations of Copaifera 20
langsdorffii, a widely distributed tree species. We hypothesized that the environment affects 21
the seed size, so that populations in environments with more limited resource (arid 22
environments and low soil fertility) have larger seeds and a lower number of seeds per 23
individual. We also evaluated the effects of soil fertility and rainfall in total investment in 24
biomass of seeds per branch to test whether allocation to reproduction increases under harsh 25
69
conditions as has been hypothesized in previous studies (Cabaço and Santos 2012; Miranda et 1
al. 2014). Finally, we tested the effects of soil fertility and rainfall in phenotypic variation in 2
seed production within individuals of the different populations of C. langsdorffii. 3
4
MATERIAL AND METHODS 5
Species and study area 6
Copaifera langsdorffii Desf (Fabaceae) is a tropical tree species, with wide 7
distribution in South America (Carvalho 2003). In Brazil, this species occurs in vegetation 8
biomes (Caatinga, Cerrado, Atlantic Forest and Amazon), from north to south (Fagundes 9
2014). Individuals adult of C. langsdorffii vary from 2-35m, depending on the habitat where 10
occurs (Carvalho 2003; Costa et al. 2012). This species has reproduction supra-annual with 11
maturity and dispersion of fruit in the dry season between July and September (Pedroni et al. 12
2002; Costa et al. 2016). The fruit, when open exposes a single ellipsoid seed, black, partially 13
wrapped in a yellow-orange aril (Carvalho 2003). The main seed dispersers of C. langsdorffii 14
are birds (Rabello et al. 2010), however seeds on the ground can be also charged and removed 15
its arils by ants (Leal and Oliveira 1998; Fagundes et al. 2013). The seeds of C. langsdorffii 16
are orthodox and size and aryl removal of the seeds are key factors in the germination (Souza 17
and Fagundes 2014; Souza et al. 2015a). 18
This study was conducted in five populations of C. langsdorffii along 600 km in three 19
biomes in the state Minas Gerais, southeastern Brazil (Table 1). In each population were 20
obtained climatic data for the last 54 years (1961-2014) from the Brazilian National Institute 21
of Meteorology (INMET, 2015). Populations selected follow a gradient of dryness, with 22
populations further north located in a more xeric climate (average annual rainfall of 858.03-23
1029.43mm) with rainfall concentrated in a few months (Fig. 1), whereas populations further 24
70
south are under a higher average annual precipitation (1490.12-1511.51mm) and better 1
distributed during the year (Fig. 1). We calculate the intra-annual variation in annual rainfall 2
of populations as coefficients of variation (CV = SD mean-1). The variability of intra-annual 3
rainfall was highly correlated whit annual precipitation (r = -0.88, P < 0.05), showing that 4
more xeric environments also show higher temporal heterogeneity in precipitation. 5
In general, the environments studied exhibit deep soils, not hydromorphic and acids 6
(Embrapa 2013). Specifically in the environments of population Can the shallow soil with low 7
permeability and high iron content (Jacobi et al. 2007). To characterize soil fertility in each 8
population were collected three soil samples (0-10 cm depth). Each soil sample was 9
composed of 10 points, collected near the individuals of C. langsdorffii selected for this study. 10
The soil samples were air dried and sent to soil fertility analysis. The soil characteristics of 11
each population are presented in Table 2. Generalized Linear Models (GLM) were conducted 12
for each soil characteristic and compared among populations through contrast analysis 13
(Crawley 2000). In general, the results show that the soil characteristics vary among 14
populations with marked differences in the population Can (Table 2), which is characterized 15
by more acid soils with lower fertility. Finally we conducted an analysis of principal 16
component (PCA) using all the soil fertility characteristics in order to obtain a single synthetic 17
variable soil. The complete results of the PCA can be seen in Table S1. Here, we used only 18
PC1 (axis of greater explanation of the PCA), here called "soil fertility". To facilitate 19
interpretation of the results we multiply the variable soil fertility by -1. 20
21
Seed sampling 22
Between July and September 2013, ten individuals of C. langsdorffii in reproductive 23
activity were selected in each study area. All trees were with a fully developed crown and in a 24
71
good phytosanitary state (e.g. without lianas, parasitic plants or evidence of pathogens attack). 1
The data were collected in a year that C. langsdorffii had mass reproduction, which in all 2
populations approximately 75% of individuals presented reproductive activity at high 3
intensity (unpublished data). To estimate the number of seeds produced by individual of C. 4
langsdorffii, ten terminal branches (30 cm long) were collected from each tree in different 5
points of the canopies (Souza et al. 2015b). This collection aimed to evaluate the number of 6
seeds produced in the fixed branch length. To estimate average seed size produced by each 7
individual, fruits at dispersion stage were randomly collected over the crown. All fruits were 8
manually processed, eliminating malformed seeds and that exhibiting symptoms of attacks by 9
predators or pathogens. After processing, 20 seeds were randomly sampled per individual. As 10
size measurements, was evaluated the mass of each seed. 11
Total investment in biomass of seeds per branch in a plant (BSB) was calculated as 12
follows: BSB = Ns * Ms(g), where Ns is the average number of seeds per branch and Ms(g) is 13
the average mass of seeds of the plant. 14
15
Statistical analysis 16
Mixed generalized linear models (GLMM) were performed using the size and number 17
of seeds per plant as response variables. The partition of the variance of size and number of 18
seeds was considered for the following hierarchical levels: among populations, trees within 19
populations, seeds within individuals, this last level used as the error term (Uribe-Salas et al. 20
2008). F-tests were conducted using the appropriate error terms, considering the variation 21
among populations as a fixed factor and other explanatory variables as random effects. The 22
differences in the size and number of seeds among populations were evaluated by contrast 23
analysis (Crawley 2000). 24
72
We performed generalized linear models (GLM) to test seed mass, seed number and 1
seed size/number within and among populations. The differences in the size and number of 2
seeds and seed size/number among populations were evaluated by contrast analysis. We also 3
performed GLM analyses to evaluate the effect of soil fertility and annual rainfall in seed 4
mass, seed number and seed size/number. In this case we use ratio between seed mass (g)/ 5
number of seeds per branch as response variable and the soil fertility and annual rainfall as 6
explanatory variable. To test if the resource allocation (total investment in biomass of seeds 7
per branch) is affected by environmental conditions, GLMs were constructed by using the 8
resource allocation as the response variable and the soil fertility and annual rainfall as 9
explanatory variables. 10
We tested the effect of soil fertility and annual rainfall in phenotypic variation (PV) of 11
size and number of seeds through regression performed by GLM, using the phenotypic 12
variation as response variables and soil fertility and annual rainfall as explanatory variable. 13
The phenotypic variation in the size and number of seeds was estimated as the percentage of 14
variation for the data set of each individual using the following formula: PV = (Sd / x) * 100, 15
where Sd is the standard deviation of a particular trait in an individual and x is the mean value 16
of this trait in the individual. 17
All data were analyzed using the R software (R Core Team 2013). All models were 18
built using the appropriate error distribution considering the nature of each response variable, 19
following by model criticism via residual analysis (Crawley 2000). All created models were 20
compared with the null model and the appropriateness of the models was tested by residual 21
analysis (Crawley 2000). 22
73
RESULTS 1
GLMM revealed that the size and number of seeds produced per plant varied 2
significantly among and within populations (Table 3). Seed mass showed greater variation 3
among populations (44.15% of the total variance). The number of seeds varied more strongly 4
within individuals (error term, 86.63% of the variance explained at this level), with low 5
variation among populations (3.05%). Heavier seeds were found in Can population, with 6
approximately 75% heavier seeds as compared to seeds produced in Moc and Jap populations 7
that yielded the smallest seeds (Table 4). The number of seeds produced per branch was 8
significantly higher in Lav population, which produced approximately twice seeds per branch 9
than the individuals in Can and Jap populations, which have produced fewer seeds per branch 10
(Table 4). The highest seed size/number ratio was observed for the Can population, which 11
was at least twice that observed for the other populations (Table 4). 12
The seed mass of each population was affected by soil fertility and annual rainfall 13
(Table 5). Individuals of C. langsdorffii in populations in low fertility soils presented heavier 14
seeds (Fig. 2A), but the number of seeds per branch did not vary significantly with the soil 15
fertility (Table 5, Fig. 2B). However, if a population from a very oligotrophic soil (Can) is 16
excluded of the analysis, a negative liner correlation between seed number per branch and soil 17
fertility is found (F1,38= 4.18 P < 0.05 R2= 0,86), i.e, an increase of number of seeds with the 18
decrease of soil fertility. The seed mass and number of seeds produced were affected by 19
annual rainfall (Table 5), with heavier seeds and higher number of seeds produced in 20
populations from environments with higher annual rainfall (Fig. 2D and E, respectively). The 21
seed size/number was affected by soil fertility but not by rainfall (Table 5, Fig 2), with Can 22
population showing the highest values. 23
The seed size/number trade-off was observed only Can population (F1,8= 7.68 P < 0.05 24
R2= 0,49). Our results showed a negative relationship between the size and number of seeds in 25
74
the Can population (Fig 3B), but in other populations this relationship was not observed (Fig 1
3). The ratio seed mass/ number per branch did not vary among populations, except Can that 2
showed values twice to three times higher than others did (Table 4). In Can population larger 3
seeds were found, however in a smaller number per branch (Fig. 2). 4
The reproductive allocation (total investment in biomass of seeds per branch) was 5
affected by annual rainfall but not by soil fertility (Table 6; Fig4). Populations in higher 6
rainfall environments invested more in reproduction when compared to populations in lower 7
rainfall environments (Fig. 4B) producing more and larger seeds (Fig. 2D and E). 8
The phenotypic variance in seed mass per individual and number of seeds per branch 9
were affected by environmental conditions of the populations. Lower phenotypic variation for 10
mass seeds (F1,48 = 8.00 P < 0.01; Fig 5A) and number of the seeds per branch (F1,48 = 5.67 P 11
< 0.05; Fig 5B) was found in poorer soils. Annual rainfall affected negatively phenotypic 12
variation of seed mass (F1,48 = 12.87 P < 0.001; Fig 5C) and number of the seeds per branch 13
(F1,48 = 6.63 P < 0.05; Fig 5D). 14
15
DISCUSSION 16
Our study showed that highly distrophic soil determined a seed size/number trade-off 17
in Copaifera langsdorffii. In populations from less distrophic soils, the seed size was not 18
associated with the number of seeds. Different of soil fertility, no relationship was found 19
between rainfall and seed size/number. On the other hand, the reproductive allocation (total 20
seed biomass per branch) was influenced by rainfall, so that plants of populations in 21
environments more mesic produced larger seeds and in higher amounts. 22
The trade-off between the number and size of the seeds has a solid theoretical base 23
(Smith and Fretwell 1974; Lloyd 1987) and several studies have shown this trade-off in plant 24
75
reproductive processes (Shipley and Dion 1992; Turnbull et al. 1999; Jakobsson and Eriksson 1
2000; Leishman 2001; Sadras 2007). Limited resource availability generates a stronger trade-2
off in the allocation of energy for the production of larger seed or more seeds in function of 3
environment of plant, usually shifted to production of large seeds (Baker 1972; Stromberg and 4
Patten 1990; Murray et al. 2004; Ramírez-Valiente et al. 2009). The size of the seeds is 5
directly related to the amount of nutritional reserves that will be allocated for the initial 6
seedling growth (Primack 1987) and large seeds produce more vigorous seedlings when 7
compared to small seeds (Gross and Werner 1983; Gross 1984; Souza and Fagundes 2014). 8
Greater amount of stored reserves allows a higher probability of seedling establishment at 9
sites with lower resource availability (Baker 1972; Moles and Westoby 2004). Individuals of 10
C. langsdorffii in the more distrophic soil (Can population) produced larger seeds and in 11
smaller amounts. Thus, the low fertility of the soil is a key factor for the seed size/number 12
trade-off in C. langsdorffii. Although the relatively high total annual rainfall in the poorest 13
soil site of Can population, it is important to note that Ferruginous Rock Grassland soils also 14
have low water storage capacity (Jacobi et al. 2007), strengthening their low resource 15
availability. 16
The lack of the seed size/number trade-off in populations from less distrophic soils in 17
C. langsdorffii can be due to the reproductive pattern of the species (Koenig et al. 2009). C. 18
langsdorffii shows mass fruiting (Pedroni et al. 2002; Souza et al. 2015b) and this 19
reproductive pattern is marked by years of high seed production followed by years in which 20
production is drastically reduced (Silvertown 1980; Ramirez and Arroyo 1987; Tsvuura et al. 21
2011; Souza et al. 2015b). This study was conducted in a year of mass reproduction and 22
during events of mass reproduction trees shunt an disproportionate amount of resources into 23
flower and seed production, causing direct negative impact on growth and subsequent 24
reproductive events of individual plants (Koenig and Knops 1998; Koenig and Knops 2005; 25
76
Hacket-Pain et al. 2015). Thus, the large allocation of resources to reproduction observed in 1
masting episodes could offset the size/number of seeds trade-off in species with mass 2
reproduction, since that resource limitation is not extreme, as was the case of Can population. 3
It has been proposed that resource availability is a key factor for supra-annual species 4
to display their reproductive activity and intensity of seeds production (Sork 1993; Koenig 5
and Knops 2005). Populations in places with higher water availability usually have higher 6
photosynthetic rates (Llorens et al. 2004; Lázaro-Nogal et al. 2015), may allocate more 7
resources for reproduction, producing larger seeds and in larger amount (Yuan et al. 2016). In 8
contrast, performance of individuals from dry sites can be impaired resulting in negative 9
impacts on reproductive allocation. Our results showed that the size and number of seeds 10
were positively correlated with rainfall. Therefore the variation among populations in total 11
seed biomass per branch observed in this study may represent an allocation to reproduction 12
contingent on resource availability. This idea is reinforced by the fact that environments with 13
high rainfall but in extremely poor soils (Can population) rendered reduced seed biomass per 14
branch, with production of large seeds, but in small quantities amounts. 15
Populations in low rainfall environments and more fertile soils presented higher intra-16
individual phenotypic variability in seed size and number. This high intra-individual variation 17
phenotypic variability can be attributed to the low environmental predictability, since these 18
sampled sites are also more heterogeneous climatically, with high seasonality and interannual 19
variation in precipitation. In unpredictable environments plants can develop certain 20
morphological and physiological adaptations in their seeds that increase survival under these 21
uncertain conditions (Harper and Ogden 1970; Wang et al. 2008). Small seeds germinate 22
faster so the seedlings can quickly occupy the environment (Baskin and Baskin 1998; Souza 23
and Fagundes 2014) making better use of the window of time when water is available. On the 24
other hand, large seeds produce more vigorous seedlings with a higher probability of survival, 25
77
particularly under stressful conditions (Baker 1972; Hanley et al. 2007). Therefore, the 1
variation in seed size allows species to cope well with a relatively wide range of 2
environmental conditions, buffering, for instance, the negative influence of unpredictable 3
rainfall. 4
Our study highlights the capacity of C. langsdorffi to adjust the reproductive strategy 5
according to environmental conditions. This capacity can significantly contribute to the niche 6
breadth of the species. The most likely scenario of the climatic changes for the Neotropics is 7
an increase in heterogeneity and unpredictability of rainfall (Marengo et al. 2012). Thus, the 8
wide phenotypic variation in seed production presented by C. langsdorffii, especially in 9
environments with high variability in precipitation could be an important factor for the 10
persistence of C. langsdorffii under future climatic changes. 11
12
ACKNOWLEDGEMENTS 13
We thank all the collaborators of the Plant Physiology Laboratory - UFMG, Conservation 14
Biology Laboratory – UNIMONTES and directors of Paraopeba National Forest (FLONA-15
PARAOPEBA) for logistical support in the fieldwork. This study was carried out with 16
financial support from CNPq and FAPEMIG. This work was conducted with a scholarship 17
supported by the International Doctoral Sandwich Program (PDSE). Financed by CAPES – 18
Brazilian Federal Agency for Support and Evaluation of Graduate Education within the 19
Ministry of Education of Brazil. We also thank all the collaborators Ecology and Global 20
Change Group of National Museum of Natural Sciences (MNCN-CSIC), Madrid-Spain. 21
78
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87
TABLES
Table 1: Environment and climatic characterization of Copaifera langsdorffii populations. Population values of annual rainfall and annual
temperature means. Values of intra annual variation in annual rainfall are coefficients of variation (CV = SD mean-1
) expressed as percentage.
Data were obtained from the Brazilian National Meteorology Institute (www.inmet.gov.br) for the period 1961-2014. Population Coordinates Habitat Altitude (m) Rainfall (mm) Intra annual variation rainfal (%) Temperature (°C)
Jap 15º58’S, 44º16’W Caatinga 804 858.03 100.68 24.23
Moc 16o40’S, 43o48’W Cerrado 645 1029.27 101.99 22.97
Par 19°20’S, 44°24’W Cerrado 763 1295.27 94.69 21.29
Can 20°04’S, 43°59’W Ferruginous rock grassland 1423 1490.12 91.15 20.74
Lav 21º15'S, 45º02'W Atlantic forest 948 1511.51 83.69 20.02
88
Table 2. Soil fertility properties in five populations Copaifera langsdorffii. H+Al = Potential acidity; SB = Sum of bases; T= Cation exchange
capacity; t= Effective capacity of cation exchange; M= Aluminum saturation index; V = base saturation. Mean values and standard deviation
(Sd) of soil characteristics in each population are shown.
Populations Jap Moc Par Can Lav
pH (in H2O) 5.57 (0.25)
a 5.30 (0.26)
a 5.33 (0.21)
a 4.50 (0.20)
b 5.10 (0.35)
a
H+Al (mmolc.dm-3
) 3.42 (0.67)b 5.63 (1.10)
b 7.56 (1.94)
b 20.31 (4.74)
a 7.20 (2.11)
a
Al (mmolc.dm-3
) 0.39 (0.38)a 1.43 (0.50)
a 1.17 (0.80)
a 1.55 (0.67)
a 0.84 (0.66)
a
Ca (mmolc.dm-3
) 1.72 (0.49)a 1.29 (0.36)
a 2.46 (1.54)
a 1.70 (0.29)
a 2.05 (1.23)
a
Mg (mmolc.dm-3
) 0.91 (0.24)b 0.68 (0.08)
b 1.22 (0.54)
b 0.33 (0.03)
a 0.63 (0.43)
a
P (mg.dm-3
) 1.97 (031)b 1.33 (0.35)
b 2.60 (0.61)
b 4.43 (0.55)
a 3.33 (1.50)
a
K (mg.dm-3) 86.33 (13.05)
b 166.00 (22.27)
a 182.67 (20.53)
a 76.33 (14.29)
b 109.00 (41.61)
b
SB (mmolc.dm-3
) 2.85 (0.54)a 2.40 (0.37)
a 5.47 (1.33)
a 2.22 (0.27)
a 2.96 (1.75)
a
T 6.39 (1.15)b 8.02 (0.84)
b 11.80 (0.18)
b 22.50 (4.51)
a 10.16 (1.05)
b
t 3.24 (0.57)a 3.83 (0.23)
a 5.47 (1.33)
a 3.77 (0.41)
a 3.8 (1.19)
a
M 11.52 (11.07)a 22.07 (15.84)
a 26.63 (21.50)
a 40.13 (12.9)
a 26.91 (23.57)
a
V 45.57 (3.36)a 30.26 (6.52)
a 35.46 (17.35)
a 10.28 (3.23)
b 29.37 (18.73)
a
Different letters after mean and standard deviation (Sd) indicate significant differences in Contrast analysis in GLM (P < 0.05).
89
Table 3: Partitioning of variance (in percentage) for seed mass and seed number in
Copaifera langsdorffii. Variance components and significance levels were determined
with a GLMM.
Level
Population
Plant
[Population]
Individual
[Error]
Seed mass 44.15*** 23.91*** 31.92
Seed number 3.05** 10.31*** 86.63
(***, P < 0.001; **, P < 0.01; in GLMM).
90
Table 4: Analysis of deviance of complete models to evaluate the seed mas, seed
number per branch and seed size/number trade-off among populations of Copaifera
langsdorffii. Mean values and standard deviation (in brackets) are shown.
Variables Jap Moc Par Can Lav
Seeds mass (g) 0.44 (0.11)c 0.42 (0.09)
c 0.54 (0.08)
b 0.75 (0.11)ª 0.56 (0.10)
b
Seed number 4.16 (3.06)c 5.65 (4.05)
b 6.87 (3.50)
b 3.00 (1.90)
c 8.29 (6.57)ª
Seed size/number
trade-off †
0.18 (0.15)b 0.14 (0.16)
b 0.10 (0.05)
b 0.36 (0.24)
a 0.17 (0.19)
b
Different letters after mean and standard deviation indicate significant differences in
Contrast analysis in GLM (P < 0.05). †, ratio between seed mass (g)/seed number per
branch.
91
Table 5 – Analysis of deviance of complete models to evaluate the effect of soil fertility
and the annual rainfall in the size and number of seeds and to evaluate seed size/number
trade-off in Copaifera langsdorffii in different populations.
Response
Variable
Explanatory
variable
Deviance
Residual
Df
Residual
deviance
F P
Seed mass (g)
Soil fertility 0.32 48 0.68 30.43 ***
Rainfall (mm) 0.20 47 0.49 18.52 *
Soil fertility X
Rainfall (mm)
0.01 46 0.49 0.33 NS
Seed number
Soil fertility 34.77 48 938.16 2.02 NS
Rainfall (mm) 144.27 47 793.89 8.40 **
Soil fertility X
Rainfall (mm)
3.91 46 789.97 0.22 NS
Seed
size/number
trade-off †
Soil fertility 0.40 48 1.41 13.64 ***
Rainfall (mm) 0.06 47 1.35 2.15 NS
Soil fertility X
Rainfall (mm)
0.01 46 1.34 0.28 NS
***, P < 0.001; **, P < 0.01; * P < 0.05; NS, P > 0.05 in GLM. †, ratio between seed
mass to seed number.
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Table 6: Analysis of deviance of complete models to evaluate the effect of soil fertility
and the annual rainfall in the resource allocation to reproduction of Copaifera
langsdorffii in different populations.
Response
Variable
Explanatory
variable
Deviance
Residual
Df.
Residual
deviance
F P
Reproductive
allocation†
Soil fertility 5.03 48 376.32 0.74 NS
Rainfall (mm) 64.20 47 312.12 9.48 **
Soil fertility X
Rainfall (mm)
0.49 46 311.64 0.07 NS
**, P < 0.01; NS, P > 0.05 in GLM; †, total seed mass per branch.
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Table S1: Principal component analysis (PCA) for soil fertility characteristic in populations of Copaifera langsdorffii. . H+Al = Potential acidity;
SB = Sum of bases; T = Cation exchange capacity; t = Effective capacity of cation exchange; m = Aluminum saturation index; V = base
saturation.
PCA PC1 PC2 PC3 PC4
Eigenvalues 6.69 3.08 1.35 0.34
Percent (%) 55.75 25.66 11.27 2.85
Cumulative Percent (%) 55.75 81.41 92.69 95.53
Soil characteristic Eigenvectors
pH (in H2O) -0.88 0.40 -0.04 0.15
H+Al (mmolc.dm-3
) 0.82 -0.52 0.07 -0.01
Al (mmolc.dm-3
) 0.77 -0.07 -0.58 -0.16
Ca (mmolc.dm-3
) -0.66 -0.67 0.28 0.00
Mg (mmolc.dm-3
) -0.85 -0.34 -0.22 0.17
P (mg.dm-3
) 0.46 -0.75 0.32 0.06
K (mg.dm-3) -0.58 -0.23 -0.73 -0.09
SB (mmolc.dm-3
) -0.79 -0.60 0.04 0.05
T 0.70 -0.67 0.09 0.00
T -0.49 -0.80 -0.33 -0.05
M 0.80 -0.02 -0.32 0.50
V -0.96 0.07 0.16 0.06
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FIGURES
Figure 1: Historical monthly average of 54 years for rainfall of locations of Copaifera
langsdorffii populations. The symbols represent the following populations: Closed
triangles = Lavras (Lav); Closed circles = Canga (Can); Closed squares = Paraopeba
(Par); Open triangles = Montes Claros (Moc); Open circles = Japonvar (Jap).
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Figure 2: Effect of environmental conditions in seed production of the populations of
Copaifera langsdorffii and seed size/number trade-off. Figures A, B and C) Effect of
soil fertility in seed mass (g), number per branch and seed size/number trade-off,
respectively; Figures C, D and E) Effect of annual rainfall in seed mass (g), number per
branch and seed size/number trade-off, respectively. The seed size/number trade-off was
by ratio between seed mass (g) to seed number number per branch. Population means
and SE are shown (N= 50). ***, P < 0.001; **, P < 0.01; * P < 0.05; NS, P > 0.05 in
GLM. For populations symbols see Figure 1.
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Figure 3: Seed size/number trade-off in different populations of Copaifera langsdorffii.
A) Lavras (Lav); B) Canga (Can); C) Paraopeba (Par); D) Montes Claros (Moc); D)
Japonvar (Jap). Individual means of each population are shown (N= 10). *, P < 0.05;
NS, P > 0.05 in GLM. For populations symbols see Figure 1.
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Figure 4: Effect of soil fertility (A) and rainfall (B) in the reproductive allocation (total
seed mass per branch) in Copaifera langsdorffii populations. Population means and SE
are shown (N= 50). *, P < 0.05; NS, P > 0.05 in GLM. For populations symbols see
Figure 1.
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Figure 5: Effect of environmental conditions in phenotypic variation (measured as
percentage of change) of the populations of Copaifera langsdorffii for: Figures A and
B) Effect of soil fertility in seed mass (g) and number per branch; Figures C and D)
Effect of annual rainfall in seed mass (g) and number per branch. Population means and
SE are shown (N= 50). M, mesic; X, xeric. ***, P < 0.001; **, P < 0.01; * P < 0.05 in
GLM. For populations symbols see Figure 1.
99
Capítulo III: Key factors affecting seed germination of Copaifera
langsdorffii, a Neotropical tree
Artigo publicado na revista Acta Botanica Brasilica 29(4): 473-478. 2015.
Matheus Lopes Souza1, Dávila Regina Pacheco Silva
1, Laura Bubantz Fantecelle
1, José Pires
de Lemos Filho1
Corresponding author: Matheus Lopes Souza
1. Programa de Pós-Graduação em ecologia conservação e manejo da vida silvestre,
Laboratório de Fisiologia Vegetal, Universidade Federal de Minas Gerais - UFMG, Belo
Horizonte, Minas Gerais, Brazil.
Address: Av. Avenida Presidente Antônio Carlos, 6627 - Pampulha, Belo Horizonte - MG,
31270-901.
E-mail: [email protected]
Received: April 11, 2015 Accepted: June 11, 2015
ABSTRACTIn natural conditions biotic and abiotic factors interact, synergistically affecting seed germination. In this study, we ex-perimentally simulated natural conditions that occur during seed dispersal that can affect the germination of Copaifera langsdorffii. Specifically we evaluated the effect of aril removal by different dispersal agents (birds and ants) and fire on germination. The seeds were submitted to the following treatments: Control (seeds placed to germinate with aril intact); Acid (simulation of passage through the digestive tract of a bird); Aril removal (simulation of aril removed by ants); Fire (seeds exposed to fire). Germination percentage and time varied among treatments (X²=89.735, P<0.001; X²=16.225, P<0.001, respectively). None of the control seeds (intact aril) germinated. Treatments that simulated dispersal (Acid, Aril removal) did not differ in germination percentage, with about 50% of the seeds germinating, however, the acid treatment accelerated seed germination. Fire also had a positive effect on seed germination with about 80% of the seeds germinating. Our results demonstrate the importance of dispersal agents to the population dynamics of C. langsdorffii. Furthermore, the capacity of seeds of C. langsdorffii to tolerate high temperatures is an important attribute for the occurrence of this species in the Cerrado.
Keywords: Cerrado, Copaifera langsdorffii, fire, plant-disperser interaction, seed germination
Acta Botanica Brasilica 29(4): 473-478. 2015.doi: 10.1590/0102-33062015abb0084
Key factors affecting seed germination of Copaifera langsdorffii, a Neotropical tree
Matheus Lopes Souza1*, Dávila Regina Pacheco Silva1, Laura Bubantz Fantecelle1 and José Pires de Lemos Filho1
1 Programa de Pós-Graduação em ecologia conservação e manejo da vida silvestre, Laboratório de Fisiologia Vegetal, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazil* Corresponding author: [email protected]
IntroductionSeed germination is a critical phase of the plant life cy-
cle, influencing the distribution and abundance of species in plant communities (Wulff 1986; Armstrong & Westoby 1993). Biotic factors, intrinsic to the seed and/or interac-tions with other organisms and abiotic factors, such as light, temperature, humidity and fire, affect germination differently (Baskin & Baskin 1998). Zoochorous seeds have fleshy structures that attract and reward their dispersers (Christianini et al. 2007) and often have substances that inhibit germination (Cipollini & Levey 1997; Yagihashi & Miyamoto 1998; Robertson et al. 2006). Thus, in addition to transporting seeds away from the mother plant, seed dispersers can be important to the successful germination of some species by removing compounds that inhibit germina-tion (Robertson et al. 2006; Silveira et al. 2012; Lessa et al. 2013). Birds and ants are important groups that mutually interact as seed dispersers and can remove inhibitors, thus promoting germination (Meyer & Witmer 1998; Chris-tianini & Oliveira 2010; Guerta et al. 2011; Lima et al. 2013), however, this influence is not uniform among zoochorous species (Barnea et al. 1991; Figueroa & Castro 2002).
Fire can interfere in many aspects of plant development, especially in the biology of seeds (Paula et al. 2009). The effects of fire on the seeds include loss of viability (Schmidt et al. 2005), dormancy break (Ribeiro et al. 2013), and the activation of genes important to germination by the pres-ence of smoke (Moreira et al. 2010). These effects depend mainly on the degree of tolerance a seed and the species life history has to high temperatures (Luna et al. 2007). The Cer-rado is an environment in which fire has been a recurrent factor for thousands of years (Salgado-Laboriau et al. 1997). In fact, recent studies have shown that seeds of plants of the Cerrado tend to be more tolerant to high temperatures than seeds of forest plants (Ribeiro et al. 2013; Ribeiro & Borghetti 2014). Despite these recent efforts, studies assess-ing the effects of fire on the germination of native Cerrado plant species remain scarce, especially investigations involv-ing species that are not endemic to this biome.
Copaifera langsdorffii (Fabaceae) is a species of tropical tree of 7-30 m in height (Carvalho 2003). The species is widely distributed in South America (Carvalho 2003). In Brazil the species occurs in the physiognomies of Cerrado, Atlantic Forest and gallery forest, from the north to the south (Almeida et al. 1998). Copaifera langsdorffii presents
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Acta bot. bras. 29(4): 473-478. 2015.
supra-annual fruiting, with alternating years of high and low or no fruit production (Pedroni et al. 2002; Fagundes et al. 2013). Flowering occurs from November to January and fruits mature in July to September, coinciding with the period of greatest deciduousness (Pedroni et al. 2002; Fagundes et al. 2013). There are many types of dispersers of the seed of Copaifera langsdorffii, but the primary seed dis-persers are birds (see Rabello et al. 2010), and the secondary dispersers are ants (see Leal & Oliveira 1998; Silva & Souza 2014). The seeds of C. langsdorffii have orthodox behavior (Bezerra et al. 2002) and pre-germination treatments of scarification can accelerate the germination process (Perez & Prado 1993). In addition, Souza & Fagundes (2014) showed that seed size as key factor in germination of C. langsdorffii.
In natural conditions, biotic and abiotic factors interact synergistically directly affecting time to germination and the percentage of successful seed germinations. Thus, the objective of this study was to evaluate seed dispersal of C. langsdorffii, in laboratory situations simulating field conditions, in order to determine the effects of biotic and abiotic factors on the process of seed germination. Specifi-cally we seek to answer the following questions: (i) What influence does aril removal have on seed germination of C. langsdorffii? (ii) Knowing that birds and ants can disperse the seeds of C. langsdorffii and that they remove the aril differently, do they have differing affects on germination? (iii) Does fire affect seed germination of C. langsdorffii?
Materials and methodsStudy area
Fieldwork was conducted in a Cerrado (Brazilian sa-vanna) area located in the Floresta Nacional de Paraopeba (FLONA-PARAOPEBA, 19°20’S, 44°24’W), in the munici-pality of Paraopeba, in southeastern Brazil. The climate is type AW according to the Köppen classification, with a rainy summer and a dry season from April to September, corresponding to the fall and winter. The average annual temperature is 20ºC and the annual accumulated rainfall is about 1300 mm (INMET 2015). Annual climatic variation is shown in Fig. 1.
Data collection
In August 2013, 10 reproductive individuals of Copaifera langsdorffii Desf. were selected at the study area. The trees were five to seven meters high, had well-formed crowns and were in a good phytosanitary state (e.g. without lianas or parasitic plants). Fruits were haphazardly collected from throughout the canopy of each selected tree (Costa et al. 2010). All collected fruits were manually treated and using similarly sized seeds, with malformed seeds and those with visual signals of attack by predators or pathogens being eliminated. After processing, the seeds of all individuals
were mixed and divided randomly among four treatments, with 100 seeds per treatment. The probability of germina-tion was calculated assuming each seed to be a statistically independent experimental unit (see Warton & Hui 2011).
The treatments used here simulate situations observed in the field that are suspected to influence the germination process. To evaluate the affect of aril removal by different seed dispersers and of fire on seed germination of C. langsdorffii, the seeds were submitted to the following treatments: control treatment, seeds placed to germinate with aril intact; acid treat-ment, simulation of the passage through the digestive tract of birds by exposing seeds to sulfuric acid (H2SO4) for 5 minutes; aril removed, simulation of aril removal by ants; fire treatment, seeds lacking arils into were partially buried in a layer of 5 cm of Cerrado soil in a 20 x 40 cm tray and covered by a litterfall layer from the study area, which was subsequently burned for about 30 minutes. After all treatments the seeds were rinsed with distilled water and tested for germination.
The seeds were placed in a gerbox, properly identified with their treatment, and covered with filter paper. The germination experiment was conducted in a germination chamber with controlled photoperiod and temperature (12 h/light at 30°C e 12 h/dark at 25°C). The seeds were monitored daily for 30 days to determine the percentage of germination and time to germination. A seed was consid-ered germinated when primary root protrusion occurred (Ferreira & Borghetti 2004).
A soaking test was conducted under the same germi-nation conditions using 30 different seeds. Seed mass was determined and then all seeds were immersed in distilled water and reweighed after 6, 18, 30, 48, 72, 96, 120, 144, 168, 192, 216 and 240 hours of water absorption. Relative increase in fresh weight (Wr) of seeds was calculated as Wr = [(Wf −Wi)/ Wi] ×100 where Wi is the initial seed weight and Wf the weight after each time interval of water absorp-tion (Baskin & Baskin 2004). Thus, imbibition curves were based on the increase in seed mass at different time intervals of seed immersion in distilled water.
Figure 1. Average monthly precipitation and temperature in Paraopeba-MG.
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Acta bot. bras. 29(4): 473-478. 2015.
Data Analysis
Data were analyzed using R software (R Core Team 2014). Germinability was evaluated by constructing a generalized linear model (GLM) using an appropriate er-ror distribution for each response variable. The model was assessed via residual analysis (Crawley 2007). The germi-nability of a seed, based on a binary response (germinated or non germinated), is commonly expressed as a percentage (Ranal & Santana 2006). We used the binomial distribution error, indicated for binary data as the germination. Recently, Warton & Hui (2011) showed that this statistical approach provides a significant gain in power. The effect of treatments on germination was tested using the germination percentage of each treatment as response variables and treatments as explanatory variables.
To evaluate the probability of germination over a period of time, survival analysis was performed in order to test the effect of treatments on time of seed germination (Souza & Fagundes 2014). Thus, germination percentage within each treatment was used as response variables, while germina-tion time was the explanatory variable. Survival analysis evaluates the likelihood of germination at a certain point in time, thus avoiding the temporal pseudo-replication inherent to the data.
Seed water absorption was tested by constructing Generalized Linear Mixed Models (GLMM), since these data also showed temporal pseudo-replication (Souza & Fagundes 2014). Thus, increased seed mass (Wr) was used as the response variable and time of water absorption (6, 18, 30, 48, 72, 96, 120, 144, 168, 192, 216 and 240 hours) as the explanatory variable.
ResultsGerminability varied among treatments (X² = 89.735,
P< 0.001). Our results demonstrated that aril removal positively influenced germination (Fig. 2). No significant
differences were observed in the proportion of germinated seeds between acid treatment and without aril. No seed with aril intact (control treatment) germinated (Fig. 2). Fire also positively affected seed germination (Fig. 2), having the highest germination percentage among treatments with about 80% of the seeds germinating. At the end of the ger-mination test, all non-germinated seeds were examined and found to be damaged and marked by the presence of fungi.
Overall, seeds germinated from the 4th to 25th day. The time to seed germination varied among treatments (X² = 16.225, P< 0.001). In this case, the removal of the aril af-fected germination time. Seeds submitted to acid treatment germinated more quickly than those without aril and those exposed to fire, which did not differ significantly (Fig. 3). The soaking test showed that water absorption varied with time (F = 243.609, P <0.001), and that the seeds of C. langs-dorffii exhibited great variation in water imbibition (Fig. 4).
Figure 2. Percentage of seeds of Copaifera langsdorffii succesfully germinatiing in different treatments. Control: seeds placed to germinate with aril intact. Acid: simulation of the seed passage through the digestive tract of birds through exposing seeds to sulfuric acid for 5 minutes. Aril removal: simulation of aril removal by ants. Fire: aril removal followed by partial burial.
Figure 3. Time to seed germination for Copaifera langsdorffii in different treatments. Vertical lines indicate the time required for germination of 50% of the seeds. Acid: simulation of the seed passage through the digestive tract of birds by exposing seeds to sulfuric acid for 5 minutes. Aril removal: simulation of aril removal by ants. Fire: aril removal followed by partial burial.
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DiscussionIn this study we examined some of the factors that af-
fect seed germination of Copaifera langsdorffii. Our results demonstrate that removing the aril is essential for seed germination in this species, since the maintenance of the aril completely inhibited seed germination. Studies show that zoochorous seeds have secondary compounds that inhibit germination (Cipollini & Levey. 1997; Yagihashi & Miyamoto 1998; Robertson et al. 2006). The presence of secondary compounds (e.g. coumarins) in arils may inhibit seed germination by one of two ways: by direct chemical inhibition or by influencing micro-environmental factors such as light and oxygen (Cipollini & Levey 1997). The characteristics of the seeds of C. langsdorffii indicate that germination inhibition is chemical, since the seeds are not photoblastic and the aril only partially covers the seed. Furthermore, the presence of the aril favors the growth of fungi, which may prevent seed germination (Ohkawara & Akino 2005). Our results also show that the seeds of C. langsdorffii do not exhibit physical dormancy, despite their slow water uptake (Baskin & Baskin 2004).
Aril removal positively affected germination. The treat-ments that simulated the effects of a disperser increased ger-mination by about 50%. These results are in accordance with other studies (Leal & Oliveira 1998; Robertson et al. 2006; Christianini et al. 2007; Lessa et al. 2013; Lima et al. 2013), and demonstrate the potential benefits of the seed dispersal process on seed germination (Lima et al. 2013). These results suggest that dispersers, in addition to transporting seeds away from the mother plant and thus avoiding intraspecific competition and decreasing the likelihood of an attack by predators (Janzen 1970; Swamy et al. 2011), are essential in the germination success of C. langsdorffii. Furthermore, during passage through the digestive tract of a frugivore, the seeds become scarified such that structures that can reduce or even prevent germination may be removed. Such scarification can accelerate the speed of germination and increase the proportion of successful germinating seeds (Robertson et al. 2006).
In many cases, zoochorous seeds, being produced in large numbers, are not all consumed by a primary disperser and usually fall to the soil near the mother plant, becoming available to other groups of animals, among which are other important dispersers (Christianini & Oliveira 2010; Lima et al. 2013). Specifically, C. langsdorffii has supra annual mass reproduction with high fruit production (Fagundes et al. 2013; Souza et al. 2015) and many seeds may go uneaten in this manner. Studies have shown that in such cases, ants are important secondary seed dispersers, carrying the seeds far from the mother plant (see Christianini & Oliveira 2010). Also, by removing the arils, ants reduce the chances of fungal attack on the seeds fallen on the fungi-prone tropical forest floor (Lima et al. 2013).
Our results indicate that fire was not detrimental to the survival of seeds of C. langsdorffii. Historically, fires appeared concomitantly with the origin of land plants and have played an important role throughout the history of life (Pausas & Keeley 2009). Traits adaptive to fire, such as toler-ance to high temperatures, increased plant fitness in these environments (Keeley et al. 2011). Studies in savannas have shown that some species adapted to these environments are able to tolerate high temperatures from the passage of fire (Delgado et al. 2008; Fichino et al. 2012; Ribeiro et al. 2013; Ribeiro & Borghetti 2014). Copaifera langsdorffii is a com-mon tree species in tropical forest environments (Carvalho 2003), and fire tolerance may be an attribute important for the occurrence of this species in the Cerrado (Rizzini 1976). Seeds of C. langsdorffii tolerate high temperatures, and the germination percentage increases after the passage of fire, which can be attributed to the control of microorganisms, such as fungi (Alencar et al. 2009). In fact, in our study, the seeds treated with fire had a low level of infestation by fungi.
Finally, our results show that biotic and abiotic factors can interact synergistically, affecting time to germination and the percentage of successful germinations of a zoo-chorous Neotropical tree. Evaluating the effects of dispersal on germination is important for understanding the quali-tative effectiveness of seed dispersal, as well as elucidating the role that dispersers play in the population dynamics of plants (Schupp et al 2010). The lack of germination among seeds with their arils intact demonstrates the importance of dispersal to the germination of C. langdorffii. Thus, con-servation of viable habitat for the maintenance of dispersers is essential for the reproductive success of C. langsdoffii. Considering the approaches, results and analyses of the present study, additional investigations into germination in field conditions are needed to elucidate the factors that determine the spatial distribution and abundance of species in natural plant communities.
AcknowledgmentsWe thank all the collaborators of the Plant Physiology
Laboratory - UFMG, for logistical support in the fieldwork.
Figure 4. Imbibition curve for seeds of Copaifera langsdorffii.
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Acta bot. bras. 29(4): 473-478. 2015.
The authors are indebted to Thais Ferreira Costa for her valuable revision of the English version. We also thank the directors of FLORESTA NACIONAL DE PARAOPEBA for logistical support. This study was carried out with financial support from CNPq and FAPEMIG. The authors also ac-knowledge CAPES, CNPq and FAPEMIG for research grants.
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Capítulo IV: Climatic heterogeneity as a generator of phenotypic plasticity
in functional leaf traits of a neotropical tree species widely distributed
Matheus Lopes Souza1,*
, Alexandre Aparecido Duarte1, Maria Bernadete Lovato
2, Marcilio
Fagundes3, Fernando Valladares
4,5, Jose Pires de Lemos Filho
1
1Departamento de Botânica, Universidade Federal de Minas Gerais, ICB-UFMG, Belo
Horizonte, 31270, Brazil; 2Departamento de Biologia Geral, Universidade Federal de Minas
Gerais, ICB-UFMG, Belo Horizonte 31270, Brazil; 3Departamento de Biologia Geral,
Universidade Estadual de Montes Claros, CCBS-UNIMONTES, Montes Claros, 39401,
Brazil; 4LINCGlobal Departamento de Biogeografía y Cambio Global, Museo Nacional de
Ciencias Naturales, MNCN-CSIC, Madrid, 28006, Spain; 5Departamento de Biología y
Geología ESCET, Universidad Rey Juan Carlos, Móstoles, 28933, Spain.
* For correspondence: E-mail [email protected]. Av. Avenida Presidente Antônio
Carlos, 6627 - Pampulha, Belo Horizonte - MG, 31270-901. Phone: (031) 3409-2568; Fax:
(031) 3409-2567.
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ABSTRACT 1
Climatic changes are challenging for sessile organisms and phenotypic plasticity has been 2
regarded as an important way to cope with these changes, preventing local extinctions. We 3
evaluate variation in metamer traits (internode, petiole and corresponding leaf) and 4
chlorophyll fluorescence parameters within and between populations of Copaifera 5
langsdorffii along a climatic gradient. We hypothesized that environmental variability 6
increases both phenotypic variability and plasticity. We selected six populations of C. 7
langsdorffii along a climatic gradient from semi-arid to more humid regions covering three 8
different biomes (Caatinga, Cerrado, and Atlantic Forest) in Brazil. Local climatic conditions 9
significantly affected the morphological and physiological traits of each population. 10
Individuals from xeric regions had lower specific leaf area (SLA), lower investment in leaf 11
area per total dry mass of metamer and higher specific petiole length. Greater plasticity in 12
response to light was found in environments with greater interannual variation of rainfall and 13
higher aridity. High plasticity in environmentally heterogeneous sites and large differences 14
among populations can explain, at least in part, the wide geographic distribution of C. 15
langsdorffii over a range of different types of habitats. Higher plasticity in unpredictable 16
environments can contribute for C. langsdorffii cope with ongoing climatic changes. 17
18
Key works: Copaifera langsdorffii; heterogeneous precipitation; aridity gradient; climate 19
changes; differentiation of populations. 20
21
108
INTRODUCTION 1
Evaluating the effects of environmental conditions on natural populations is important to 2
understand the evolutionary processes maintaining biodiversity and the possible impacts that 3
global climate change can cause in ecosystems (Hooper et al. 2012; Cardinale et al. 2012; 4
Garcia et al. 2014). Climate change is expected to increase average global temperature, 5
precipitation variability and frequency of extreme events, leading to drier environments in 6
many already arid regions (IPCC 2014). Changes in climate and landscape alter the 7
environmental conditions and the availability of resources, which can endanger large portion 8
of biodiversity (Nicotra et al. 2010). Due to the rapid environmental changes, species can 9
show three different responses: (i) migration to a more favorable environment, (ii) adjusting 10
their functional trait values to new conditions by phenotypic plasticity or (iii) adaptation 11
through natural selection (Nicotra et al. 2010; Matesanz and Valladares 2014). However, 12
these responses depend on the intensity and direction of environmental change, life history 13
characteristics, intraspecific genetic variation and interspecific interactions (Nicotra et al. 14
2010; Nunney 2016). 15
Phenotypic plasticity is the ability of a genotype to produce different morphological 16
and physiological responses when is exposed to different environmental conditions (Sultan 17
1995; Lázaro-Nogal et al. 2015). Thus, plasticity can attenuate effects of environmental 18
changes that occur throughout the plant life cycle, increasing their tolerance to stress 19
(Gimeno et al. 2008; Matesanz and Valladares 2014). In this sense, phenotypic plasticity is a 20
major mode of adaptation in plants, and therefore essential to prevent local extinctions of 21
species under a possible climate change scenario (Matesanz et al. 2010; Hoffmann and Sgrò 22
2011). The degree of phenotypic plasticity varies among populations and is often higher in 23
environments with greater variation in rainfall (Gianoli 2004; Matesanz et al. 2010; 24
Baythavong 2011; Lázaro-Nogal et al. 2015). The high plasticity found in some populations 25
109
in unpredictable environments suggests that these populations are better prepared for possible 1
climate changes. However, phenotypic plasticity has rarely been considered in the context of 2
the evolutionary responses of plants to climate change along their geographic distribution 3
(Lázaro-Nogal et al. 2015). 4
Species that are widely distributed generally present populations under different 5
environmental pressures, being affected by multiple and unpredictable stressful factors such 6
as variation in rainfall, temperature, light and soil fertility (Valladares and Pearcy 1997; 7
Lemos Filho 2000; Sultan 2003; Lázaro-Nogal et al. 2015). For this reason, significant 8
differences in ecophysiological characteristics are expected among and within populations 9
(Bruschi et al. 2003; González-Rodríguez and Oyama 2005; Uribe-Salas et al. 2008), in 10
response to environment due to different levels of plasticity and genetic variability (Heschel 11
et al. 2004; Goulart et al. 2005; Lemos Filho et al. 2008; Ramírez-Valiente et al. 2014a). The 12
combination of stressful factors and environmental unpredictability that widely distributed 13
species are subject make them excellent models to evaluate consequences of climate change 14
on natural populations, since significant changes are observed in the functional traits of these 15
species in a favorable way to the environmental pressures imposed on each population 16
(Gianoli and González-Teuber 2005; Lázaro-Nogal et al. 2015). 17
Here we evaluated the variation in morphological and physiological traits of metamers 18
among and within populations of Copaifera langsdorffii, a neotropical tree widely 19
distributed, along a climatic gradient. In addition, we determined the effects of climate 20
heterogeneity in the phenotypic plasticity of morpho-physiological traits of metamers. For 21
that, we hypothesized that environmental conditions will determine distinct morphological 22
and physiological traits in different populations since populations exposed to long periods of 23
drought may have evolved adaptations to low availability of water. Furthermore, we expect 24
that a greater heterogeneity in rainfall may have led to greater plasticity in functional traits. 25
110
MATERIALS AND METHODS 1
Species and study area 2
Copaifera langsdorffii Desf (Fabaceae) is a tropical tree species, with a wide variation in size 3
with reproductive adults varying from 2 to35m, depending on the habitat where it occurs 4
(Carvalho 2003; Costa et al. 2012). This species has a wide distribution in South America 5
(Carvalho 2003). Particularly in Brazil, it occurs in the biomes Caatinga, Cerrado, Atlantic 6
Forest and Amazon (Almeida et al. 1998). C. langsdorffii has composite leaves with 4 to 12 7
leaflets alternate or opposite (Almeida et al. 1998; Silva-Júnior 2005). This species has a 8
striking leaf fall during the driest months, which is immediately followed by leaf flush 9
(Pedroni et al. 2002). Reproduction is supra-annual with seed dispersion in the dry season 10
(Pedroni et al. 2002). C. langsdorffii seed dispersion is realized mainly by animals, 11
particularly birds (Rabello et al. 2010), however seeds on the floor can be also charged and its 12
arils removed by ants (Leal and Oliveira 1998). The size of the seeds and the aryl removal are 13
key factors in the germination of seeds of C. langsdorffii (Souza and Fagundes 2014; Souza 14
et al. 2015). 15
Six populations of C. langsdorffii were selected in the Minas Gerais state, 16
southeastern Brazil (Fig. 1). Climatic data for the last 54 years (1961-2014) for each location 17
were obtained from the Brazilian National Institute of Meteorology (INMET, 2015). 18
Distribution of studied populations follows a gradient of dryness, which north populations 19
located in more xeric climate (Table 1). Populations located further north are under lower 20
mean annual rainfall (858.0-1029.4 mm) and higher interannual rainfall variability (30.7-21
26.2%), On the other hand, population further south have a higher mean annual precipitation 22
(1490.1-1511.5mm) and less variability (21.4-18.1%). From the climatic data, we calculated 23
the aridity index (AI) for each population by the formula: AI = P/PET, where P is total 24
precipitation of the month and PET monthly potential evapotranspiration at each location 25
111
obtained from climatic stations (Picotte et al. 2009). The aridity data showed that 1
northernmost populations suffer a longer drought period during the year (Figure 2). 2
3
Morphological traits 4
Between April and May 2013, 20 individuals of C. langsdorffii were selected in each 5
population, except population Beh with 12 individuals by difficulty of access to trees. From 6
each individual, we collected a total of 22 metamer (i.e. internode, petiole and corresponding 7
leaf), 11 metamers exposed to the sun and 11 metamers in the shade (Hulshof and Swenson 8
2010). Metamers in the last nodes with mature and fully expanded leaves were sampled. 9
Once collected, metamers were immediately photographed with a millimeter scale for a later 10
determination of leaf area (LA in cm²), the length of the petiole and between nodes (PL and 11
IL, respectively, in cm) using software Image J. Metamers were put in paper bags and dried 12
in an oven (at 70 ° C for 72h). Each part of metamer was weighted separately to obtain the 13
dry mass. We calculated specific leaf area (SLA; area of the leaf blade by dry mass unit, in 14
cm²g-1
), the metamer leaf area ratio (LARm; area of the leaf blade per unit mass of metamer; 15
in cm²g-1
), the specific length of the petiole (SPL; length of the petiole per unit mass of the 16
petiole; in cm g-1
), and specific length of internode (SIL; internode length per unit mass of 17
internode, in cm g-1
) (Poorter 2009). 18
19
Physiological traits 20
Photosynthesis fluorescence measurements were conducted in three individuals of C. 21
langsdorffii from each population. In each individual, chlorophyll fluorescence was measured 22
in 6 leaves, 3 exposed to sun and 3 shaded. The chlorophyll fluorescence measurements were 23
performed at midday, using portable fluorometer (PAM-2500, Walz Germany). The potential 24
112
quantum yield of photosystem II was calculated by Fv/Fm = (Fm-F0)/Fm, where Fm and F0 1
are the fluorescence maximum and minimum, respectively. Fm and F0 were measured after 2
30 minutes of dark adaptation. Light saturation curves were obtained using the light curve 3
program of the fluorometer, and used to determinate maximum apparent photosynthetic 4
electron transport rate (ETRmax) and saturating photosynthetically active photon flux density 5
(PPFDsat) following Rascher et al. (2000). 6
7
Data analysis 8
Mixed generalized linear models (GLMM) were performed using all morphological and 9
physiological traits as response variables. The partition of the variance of traits was 10
considered for the following hierarchical levels: among populations, among individuals 11
within populations, among leaves within individuals in different light conditions and leaves 12
within individuals in the same light conditions, this last level was used as the error term 13
(González-Rodríguez and Oyama 2005; Uribe-Salas et al. 2008). F-tests for each metamer 14
trait were conducted using the appropriate error terms, considering the variation among 15
populations as a fixed factor and other explanatory variables as random effects (Crawley 16
2000). 17
We performed generalized linear models (GLM) to test the hypothesis that 18
populations exposed to long periods of drought have evolved adaptations to low availability 19
of water. In this case, we used average values of each individual of the morphological and 20
physiological traits as response variables and the aridity index of each population as an 21
explanatory variable. A model for each response variable was performed. 22
Phenotypic plasticity (P) was estimated as the percentage of change in the mean trait 23
value from individual for different light conditions, thus P = [(Xi - Xs) / Xi] * 100, where Xi 24
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is the highest average value of a particular trait in an individual and Xs is the lowest average 1
value of a particular trait in an individual (Valladares et al. 2006). We tested the effect of 2
environmental heterogeneity in phenotypic plasticity using GLM. We used average values of 3
each individual of the morphological and physiological traits, the average plasticity of all 4
morphological traits and the average plasticity of all physiological traits as response variables 5
and the interannual variation in precipitation and the aridity index of each population as 6
explanatory variables. 7
All data were analyzed using the R software (R Core Team 2013). All models were 8
built using the appropriate error distribution considering the nature of each response variable, 9
following by model criticism via residual analysis (Crawley 2000). All created models were 10
compared with the null model and the appropriateness of the models was tested by residue 11
analysis (Crawley 2000). 12
13
RESULTS 14
Phenotypic variance partition 15
GLMM revealed that all morphological traits significantly varied in all hierarchical levels 16
considered (Table 2). For all leaf morphological traits, the higher proportion of variance 17
(41.47-68.43%) was found among leaves within individuals in the same light condition (error 18
term) (Table 2). For all traits, a significant variation among light conditions within of 19
individual and population was found, with SLA, LARm, ETRmax and Fv/Fm, showing 20
considerable proportion of variance in this hierarchical level (17.90-67.14%). The differences 21
among individuals within of the populations for morphological traits varied from 3.93 to 22
29.34%. No variation among individuals within populations was observed for any 23
physiological trait. The traits that were the most strongly differentiated among individuals 24
114
within populations were PL and IL (29.34 and 24.52%, respectively). Significant variation 1
among populations was found for all traits, with exception of Fv/Fm, ranging from 8.85 to 2
38.85%. Higher divergence among populations was found for LA (25.46%), SPL (37.71%), 3
ETRmax (26.08%) and PPDFsat (38.85%) (Table 2). 4
5
Morphological and physiological traits along an aridity gradient 6
Most of the morphological and physiological traits of metamers were significantly associated 7
with aridity (P < 0.05), except the petiole length, internode length and ETRmax. The effect of 8
aridity on morphological traits was more evident in characteristics related to water 9
conservation. Populations in more xeric environments tend to have metamers with larger 10
leaves (R² = 0.54, P = 0.001, Fig. 3a). However, these same populations have metamers with 11
lower SLA (R² = 0.91, P=0.001, Fig. 3b), lower leaf area per metamer mass (LARm; R² = 12
0.83, P = 0.001, Fig. 3c) and lower specific length of the petiole (SPL; R² = 0.97, P = 0.001, 13
Fig. 3d), and specific length of internode (SIL, R² = 0.50, P = 0.001, Fig. 3e). The level of 14
light for photosynthesis saturation (PPDFsat) was affected by aridity. Individuals of C. 15
langsdorffii in drier habitats showed higher PPDFsat compared to habitats more humid (R² = 16
0.54, P = 0.01, Fig. 3f). The potential quantum yield of photosystem II (Fv/Fm) was 17
significantly reduced along the aridity gradient, indicating a higher photoinhibition in more 18
xeric habitats (R² = 0.93, P = 0.001, Fig. 3g). 19
20
Plasticity vs. interannual variation in precipitation 21
The variability of interannual precipitation and aridity index were highly correlated (r = -22
0.96, P < 0.001), showing that more xeric environments also show higher temporal 23
heterogeneity in precipitation. So here we presented only results of the effects of interannual 24
115
variation of precipitation in plasticity (Fig. 4), however the effects of aridity in plasticity can 1
be observed in Supplementary Data Fig. S1. The plasticity of petiole length, internode length, 2
ETRmax, Fv/Fm and general mean plasticity of morphological and physiological traits were 3
positively correlated with the interannual variation in precipitation (Fig. 4). LA, SLA, LARm, 4
SPL, SIL and PPDFsat showed no relation with interannual variation in precipitation (data no 5
showed). 6
7
DISCUSSION 8
In this study, we investigated climatic drivers of variation in morpho-physiological traits and 9
phenotypic plasticity in metamers of Copaifera langsdorffii populations. Our results showed 10
that aridity was associated with the variation in morphological and physiological traits in 11
different populations. Moreover, aridity index and the interannual precipitation variation 12
influenced the phenotypic plasticity of each population in response to light. Populations in 13
more arid habitats and with higher precipitation heterogeneity had higher phenotypic 14
plasticity. However, the largest fraction of total morpho-physiological variation was found 15
within individuals. The total variance within individuals, including the variance among leaves 16
both in different and in the same light conditions, was on average 64.4% and 75.1% for the 17
morphological and physiological traits, respectively. These results are in accordance with 18
other studies also showing a greater variation within individuals (Bruschi et al. 2003; 19
González-Rodríguez and Oyama 2005; Uribe-Salas et al. 2008). The traits that showed higher 20
variation within individuals were: SLA, SIL, LARm, ETRmax and Fv/Fm. These traits, 21
directly related to water economy, differential allocation of resources and the photosynthetic 22
efficiency, tended to present high phenotypic plasticity, optimizing performance in response 23
to changing environmental conditions (Lázaro-Nogal et al. 2015; Scoffoni et al. 2015). 24
116
High variation was found among populations of C. langsdorffii for morphological and 1
physiological traits (ranging from 8.8 to 38.9%) in comparison with other tree species 2
(Bruschi et al. 2003; González-Rodríguez and Oyama 2005). Selection can lead to the 3
development of morphological and physiological adaptations to the local environment 4
generating ecotypic differentiation in functional traits (Lemos Filho et al. 2008; Goulart et al. 5
2011). Thus, a certain degree of genetic differentiation among populations can explain the 6
phenotypic divergence among them, with genotypes adapted to local environmental 7
conditions. Individuals from more xeric habitats showed ecophysiological traits to reduce loss 8
of water by transpiration, such as minor values of SLA, SPL, SIL and LARm. Several studies 9
analyzing the relationship between climate and leaf morphological traits in other ecosystems 10
around the world have found patters similar to our results (Fonseca et al. 2000; Reich et al. 11
2003; Calagari et al. 2006; Uribe-Salas et al. 2008; Poorter 2009; Niinemets 2015; El Zerey-12
Belaskri and Benhassaini 2016; Ribeiro et al. 2016). Plants in arid environments tend to have 13
lower investment in leaf area, tougher leaves with petioles proportionally shorter, so it has 14
been suggested that these traits are representative of a functional strategy associated with low 15
water availability (Poorter 2009; Ramírez-Valiente et al. 2014b). Populations from more 16
xeric environments also had higher values of PPFDsat and lower values of Fv/Fm, indicating 17
that these populations are more adapted to high light radiation but they suffer from certain 18
degree of photoinhibition. A high incidence of light combined with water stress can 19
compromise the photosynthetic apparatus of plants leading to photoinhibition even in 20
drought-adapted species with xeromorphic traits (Lemos Filho 2000). The variability found in 21
functional traits of C. langsdorffii among populations suggests adaptations to local conditions 22
regarding water availability 23
Several studies have shown that plants exposed to water stress tend to reduce their leaf 24
area as a strategy to minimize water loss through transpiration (Gutschick 1999; Fonseca et 25
117
al. 2000; Uribe-Salas et al. 2008). However our results showed the opposite, plants in xeric 1
habitats showing higher leaf area. This result suggests that other strategies can be acting to 2
reduce the effect of water stress, for example, plants can discard the leaves in severe periods 3
of stress to prevent loss of water (Reich and Borchert 1984). In our study populations located 4
further north suffer more strongly with the seasonality and variability in rainfall, with four to 5
five months of drought. Phenological studies in these same populations of Copaifera 6
langsdorffii indicate leaf fall over the driest periods (unpublished data). Thus, we hypothesize 7
that northern populations exhibit a very dynamic foliage strategy, maximizing leaf area to 8
maximize carbon gain during the high water availability period and abruptly decrease their 9
transpiring surface area by shedding the leaves during the dry periods. 10
Overall we found greater phenotypic variability and plasticity in populations from 11
drier habitats and with greater interannual variation in precipitation. These results support the 12
theoretical predictions of greater plasticity in more heterogeneous environments (Gianoli 13
2004; Matesanz et al. 2010; Baythavong 2011). Our results are in accordance with studies 14
reporting a positive association between phenotypic plasticity and annual variability of 15
rainfall (Gianoli and González-Teuber 2005; Lázaro-Nogal et al. 2015). C. langsdorffii 16
populations from drier habitats had greater plasticity in petiole length, internode length, 17
ETRmax, Fv/Fm and also considering the mean of all traits for both, morphological and 18
physiological data. In our study, we evaluated the phenotypic plasticity in adults in their 19
natural conditions, which would be especially challenger under experimental conditions. Sun-20
exposed leaves when compared to shade leaves are subjected to conditions of greater water 21
stress due to high irradiance, higher temperature and wind action on the outermost portion of 22
the canopy (Niinemets and Kull 2001; Sanches et al. 2010). Evaluating leaves of sun and 23
shade is plausible to expect greater plasticity in populations of more mesic environments 24
where there is a greater light gradient (Houter and Pons 2012). However, we found greater 25
118
plasticity in populations from more xeric habitats and with greater variability of rainfall, 1
which had open canopies and thus less variation of light within the crown (Abrahamson 2
2007). This result suggests that the variability of precipitation influences phenotypic 3
plasticity in response to other environmental factors such as light. Although it has not been 4
evaluated in this study, some authors have demonstrated that this plasticity can be adaptive in 5
some cases (Ghalambor et al. 2007; Lázaro-Nogal et al. 2015), since high levels of 6
phenotypic plasticity were positively associated with plant fitness under drought. So, it seems 7
plausible that the greater plasticity in C. langsdorffii may favor the performance at individual 8
level in populations from xeric habitats. Nevertheless, explicit attention should be given to 9
the interaction of these two factors, light and water, and how it influences the phenotypic 10
plasticity of natural plant populations in response to each factor. 11
Finally, our results demonstrate that a great part of the phenotypic variation of 12
metamers in C. langsdorffii is due to phenotypic plasticity. The ability to modify functional 13
traits in response to changing environmental conditions can significantly contribute to the 14
niche breadth of a species, which could explain the success of C. langsdorffii over a range of 15
different types of habitats across its wide geographic distribution. Populations from drier 16
environments could be better suited to cope with the climatic changes expected due not only 17
to their xerophytic features but also to their higher levels of phenotypic plasticity. 18
19
ACKNOWLEDGEMENTS 20
We thank all the collaborators of the Plant Physiology Laboratory - UFMG, Conservation 21
Biology Laboratory – UNIMONTES and directors of Paraopeba National Forest (FLONA-22
PARAOPEBA) for logistical support in the fieldwork. This study was carried out with 23
financial support from CNPq and FAPEMIG. This work was conducted with a scholarship 24
119
supported by the International Doctoral Sandwich Program (PDSE) financed by CAPES – 1
Brazilian Federal Agency for Support and Evaluation of Graduate Education within the 2
Ministry of Education of Brazil. We also thank all the collaborators of Ecology and Global 3
Change Group of National Museum of Natural Sciences (MNCN-CSIC), Madrid-Spain. 4
5
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TABLES
Table 1: Environment and climatic characterization of Copaifera langsdorffii populations.
Population values of annual rainfall and annual temperature are means. Values of interannual
variation in annual rainfall are coefficients of variation (CV = SD mean-1
) expressed as
percentage. Annual average aridity index. Data were obtained from the Brazilian National
Meteorology Institute (www.inmet.gov.br) for the period 1961-2014.
Description Pop. Jap Pop. Moc Pop. Par Pop. Beh Pop. Can Pop Lav
Population Japonvar Montes Claros Paraopeba Belo Horizonte Canga Lavras
Coordinates
15º58’S,
44º16’W
16o40’S,
43o48’W
19°20’S,
44°24’W
19°53'S
43°58'W
20°04’S,
43°59’W
21º15'S,
45º02'W
Altitude (m) 804 645 763 842 1423 948
Habitat Caatinga Cerrado Cerrado Atlantic forest
Ferruginous
rock grassland
Atlantic forest
Annual rainfall
(mm)
858.03 1029.43 1295.27 1500.44 1490.12 1511.51
Interannual
rainfall variation
(CV %)
30.68 26.24 22.22 21.94 21.35 18.06
Average of mean
annual
temperature (°C)
24.23 22.97 21.29 21.54 20.74 20.02
Aridity index 0.59 0.72 1.03 1.21 1.12 1.25
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Table 2: Hierarchical partitioning of variance (in percentage) for morphological and
physiological traits in the Copaifera langsdorffii. Variance components and significance
levels were determined with a GLMM.
Level
Traits
morphological
Population
Plant
[Population]
Leaf different light
[Plant, Population]
Leaf same light
[Error]
Leaf area 25.46*** 20.13*** 12.93*** 41.47
Petiole length 15.85*** 29.34*** 9.37*** 45.44
Internode length 12.51*** 24.52*** 8.02*** 54.94
SLA 11.91*** 5.07*** 17.90*** 65.12
LARm 8.85*** 3.93*** 20.86*** 66.36
SPL 33.71*** 13.65*** 5.80*** 46.84
SIL 10.56*** 10.64*** 10.38*** 68.43
Average 16.98 17.23 10.74 53.71
Traits
physiological
ETRmax 26.08** 5.13-7
NS 48.41*** 25.51
PPDFsat 38.85*** 5.94-5
NS 16.01* 45.14
Fv/Fm 7.75-8
NS 1.96-11
NS 67.14*** 32.86
Average 17.99 6.87 22.83 52.31
(***P < 0.001; **P < 0.01; *P < 0.05; NS P>0.05 in GLMM).
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FIGURES
Fig 1 Location of the six populations of Copaifera langsdorffii selected for this study (codes
in Table 1).
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Fig 2 Historical monthly average of 54 years (1961-2014) for aridity index for populations of
Copaifera langsdorffii. Study sites codes in Table 1. An aridity value < 0.5 indicates hyper
arid conditions.
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Fig 3 Relationship between different functional traits and aridity index for populations of
Copaifera langsdorffii for: a) leaf area (cm²); b) SLA (cm² g-1
); c) LARm (cm² g-1
); d) SPL
(cm g-¹); e) SIL (cm g-¹); f) PPDF sat (mmolm-2
s-1
); g) Fv/Fm;. Average values and SE of
each population are shown (for morphological traits N = 112 and physiological traits N = 18).
SLA, specific leaf area; LARm, leaf area ratio of the metamer; SPL, specific petiole length;
SIL, specific internode length; PPDF sat, saturating photosynthetically active photon flux
density; Fv/Fm, potential quantum yield of photosystem II; M, mesic; X, xeric.
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Fig 4 Relationship between trait plasticity (measured as percentage of change) and
interannual precipitation variability in populations of Copaifera langsdorffii for: a) petiole
length; b) internode length; c) overall morphological plasticity (measured as the arithmetic
mean of the percentage of change for all morphological traits); d) ETRmax; e) Fv/Fm; f)
overall physiological plasticity (measured as the arithmetic mean of the percentage of change
for all physiological traits). Average values and SE of each population are shown (for
morphological traits N = 112 and physiological traits N = 18). ETR, electron transport rate;
Fv/Fm, potential quantum yield of photosystem II.
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Supplementary Data Fig S1 Relationship between trait plasticity (measured as percentage
of change) and aridity index in populations of Copaifera langsdorffii for; a) Petiole length; b)
SPL; c) overall morphological plasticity (measured as the arithmetic mean of the percentage
of change for the all morphological traits); d) ETRmax; e) Fv/Fm; f) overall physiological
plasticity (measured as the arithmetic mean of the percentage of change for the all
physiological traits). Average values and SE of individual in each population are shown (for
morphological traits N = 112 and morphological traits N = 18). SPL, Specific petiole length;
ETR, electron transport rate; Fv/Fm, potential quantum yield of photosystem II; M, mesic; X,
xeric.
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CONSIDERAÇ ÕES FINAIS
Neste estudo, avaliamos os efeitos das condições ambientais em traços
funcionais de diferentes populações de Copaifera langsdorffii ao longo de um gradiente
de aridez em distintas condições de solo. Nossos resultados demostraram que caracteres
morfológicos, fisiológicos e comportamentais variaram entre e dentro das populações
em função das condições ambientais locais. Variações nas características dos
metâmeros foram associadas com a aridez das diferentes populações. Indivíduos de C.
langsdorffii em habitats xéricos apresentaram estratégias adaptativas associadas à baixa
disponibilidade hídrica (Poorter 2009; Ramírez-Valiente et al. 2014), com menor área
foliar especifica, pecíolos e entre-nó proporcionalmente mais curtos e aparato
fotossintético menos sensível à fotoinibição. Além disso, indivíduos de C. langsdorffii
em ambientes áridos e com maior heterogeneidade de precipitação tiveram maior
plasticidade fenotípica nas características morfológicas e fisiológicas dos metâmeros.
Uma maior plasticidade nas características morfológicas e fisiológicas implica em um
maior arcabouço de respostas e alguns autores demonstraram que essa plasticidade pode
ser adaptativa, uma vez que altos níveis de plasticidade fenotípica foram positivamente
associados com o desempenho da planta em condições de estresse hídrico (Ghalambor
et al. 2007; Lázaro-Nogal et al. 2015). Assim parece plausível que em C. langsdorffii, a
maior plasticidade pode favorecer o desempenho dos indivíduos em populações de
ambientes mais secos.
A fenologia vegetativa também demonstrou forte correlação com
disponibilidade hídrica. Indivíduos de populações em ambientes xéricos apresentaram
mais precoce senescência e abscisão foliar, com maior intensidade e duração quando
comparado com indivíduos em ambientes mésicos. A redução na precipitação observada
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no ano de 2014 afetou diretamente a fenologia dos indivíduos de C. langsdorffii em
todas as populações. De maneira geral, os indivíduos de C. langsdorffii iniciaram a
abscisão foliar mais precocemente no ano de 2014. A deciduidade foliar durante
períodos de limitação hídrica reduz a perda de água por transpiração, além de
representar um importante mecanismo de recuperação do status hídrico da planta
(Borchert 1980; Reich and Borchert 1984). Estes ajustes observados para o início,
intensidade e duração das fenofases vegetativas em resposta a variações interanuais na
precipitação sugerem plasticidade fenotípica no comportamento fenológico de C.
langsdorffii em resposta a variação interanual da precipitação, sendo um importante
atributo para persistência da espécie frente às mudanças climáticas. No entanto, apesar
da plasticidade fenotípica observada no comportamento fenológico de C. lansdorffii
nossos resultados também demonstram que a redução na precipitação diminui as
diferenças fenológicas entre populações.
A fertilidade do solo foi o fator determinante para o trade-off tamanho/número
de sementes em C. langsdorffii. Nós observamos este trade-off apenas em indivíduos de
C. langsdorffii na população do ambiente de Canga Ferrugínea, onde foram produzidas
as maiores sementes, no entanto, em menor quantidade. O ambiente de Canga
Ferrugínea é caracterizado por solos de baixa fertilidade e apesar da elevada
pluviosidade tem baixa capacidade de armazenamento de água (Jacobi et al. 2007). A
disponibilidade limitada de recursos gera um forte trade-off na alocação de recurso para
a produção de sementes grandes vs. maior número de sementes, geralmente deslocado
para produção de sementes grandes (Baker 1972; Stromberg and Patten 1990; Murray et
al. 2004; Ramírez-Valiente et al. 2009). Isso porque, o tamanho das sementes está
diretamente relacionado com a quantidade de reservas que será destinada para o
crescimento inicial das plântulas (Primack 1987) permitindo uma maior probabilidade
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de estabelecimento e sobrevivência de plântulas em locais com baixa disponibilidade de
recurso (Baker 1972; Moles and Westoby 2004). Assim a limitação de recursos em
ambientes com solos de baixa fertilidade determinou o trade-off semente
tamanho/número, direcionando a produção de sementes grandes.
A alocação reprodutiva (biomassa total de sementes) foi maior em populações
em sítios com menor fertilidade do solo e alta precipitação, exceto na população em
ambiente de Canga Ferrugínea, onde os indivíduos apresentaram baixa biomassa total
de sementes. Populações em locais com menor estresse hídrico geralmente têm maiores
taxas fotossintéticas (Llorens et al. 2004; Lázaro-Nogal et al. 2015), podendo alocar
mais recursos para a reprodução, produzindo sementes maiores e em maior quantidade
(Yuan et al. 2016). Nossos resultados corroboram essa afirmação, com indivíduos em
populações de sítios mésicos produzindo sementes grandes e em maior quantidade.
Assim, a variação entre populações na biomassa total de sementes por ramo observada
neste estudo pode representar uma alocação para reprodução dependente da
disponibilidade de recursos no ambiente. Apesar da maior alocação reprodutiva
observada em indivíduos de populações de sítios mésicos, a variação fenotípica na
produção de sementes aumentou com a aridez e a fertilidade do solo. Em nosso estudo,
as populações em ambientes com baixa precipitação e solos mais férteis também são
climaticamente mais heterogêneas, com forte sazonalidade e variabilidade na
precipitação. A maior variação fenotípica na produção de sementes em habitats
imprevisíveis sugere uma importância ecológica desta variação, com produção de
sementes com diferentes tamanhos. Por exemplo, sementes pequenas germinam mais
rapidamente formando plântulas ocupando o ambiente (Baskin and Baskin 1998; Souza
and Fagundes 2014). Por outro lado, as sementes grandes produzem mudas mais
vigorosas com uma maior probabilidade de sobrevivência, especialmente sob condições
137
estressantes (Baker 1972; Hanley et al. 2007). Dessa forma, a ampla variação no
tamanho da semente permite a espécie lidar relativamente melhor com uma ampla gama
de condições ambientais, reduzindo a influência negativa da imprevisibilidade na
precipitação.
Em todas as populações foram observadas uma grande variação na proporção de
indivíduos reprodutivos entre os anos de estudo fenológico. Em 2013 encontramos um
forte sincronismo espacial reprodutivo entre indivíduos de C. langsdorffii distribuídos
ao longo de 600 km, com mais 80% dos indivíduos analisados reproduzindo. No entanto
em 2014 apenas cerca de 20% reproduziram. Estes resultados reforçam o caráter
reprodutivo supra-anual descrito para C. langsdorffii com anos de intensa reprodução
seguidos de 2 ou 3 anos no qual a reprodução é drasticamente reduzida (Pedroni et al.
2002; Souza et al. 2015). Durante eventos de reprodução em massa uma quantidade
desproporcional de recursos é deslocada para a produção de flores e sementes, causando
impactos negativos sobre o crescimento e subsequentes eventos reprodutivos das
plantas (Koenig and Knops 1998; Koenig and Knops 2005; Hacket-Pain et al. 2015).
Assim, a grande alocação de recursos para a reprodução observada em episódios de
reprodução em massa poderia cancelar o trade-off tamanho/número de sementes em
espécies com reprodução supra anual, mas a falha no trade-off tamanho/número de
sementes ocorre apenas em populações onde a limitação de recursos não é extrema.
Neste estudo, também abordamos alguns fatores que afetam a germinação das
sementes de C. langsdorffii. Experimentalmente em laboratório demonstramos que a
remoção do arilo das sementes é fundamental para a germinação, uma vez que nenhuma
semente mantida com arilo germinou. Em condições naturais as sementes C.
langsdorffii são dispersas por aves e formigas (Leal and Oliveira 1998; Rabello et al.
2010), que removem o arilo que contém compostos secundários inibidores da
138
geminação (Cipollini and Levey 1997; Robertson et al. 2006). Assim, os dispersores
além de depositar sementes longe da planta mãe reduzindo competição intraespecífica e
ataque de predadores (Janzen 1970; Swamy et al. 2011), também são fundamentais no
sucesso germinativo de C. langsdorffii. Nossos resultados ainda demonstraram que as
sementes de C. langsdorffii são tolerantes ao fogo. Encontramos um efeito positivo do
fogo na germinação de sementes, com cerca de 80% das sementes germinadas. Apesar
de C. langsdorffii ser uma espécie arbórea comum em ambientes florestais, a capacidade
das sementes tolerar altas temperaturas pode ser um atributo importante para a
ocorrência desta espécie em fitofisionomias do Cerrado, cujo fogo é um distúrbio
comum ha milhões de anos (Salgado-Labouriau et al. 1997).
A variabilidade observada nos metâmeros, na fenologia e sementes entre
populações em resposta da precipitação e da fertilidade do solo demonstram que estes
fatores são chaves para direcionamento de adaptações ecofisiológicas, gerando
diferenciação nos traços funcionais entre populações naturais de plantas. A capacidade
de modificar as características funcionais em resposta às mudanças nas condições
ambientais contribui significativamente para a amplitude de nicho de uma espécie, o
que poderia explicar o sucesso de C. langsdorffii sobre uma gama de diferentes tipos de
habitats em toda a sua ampla distribuição geográfica. No entanto, em um cenário futuro
no qual se espera aumento na aridez e maior heterogeneidade na precipitação por todo
Neotrópico (Marengo et al. 2012) a capacidade de se adaptar a essas novas condições é
fundamental para o sucesso da espécie e a plasticidade fenotípica tem sido considerada
como um importante mecanismo pelo qual os indivíduos podem enfrentar as variações
ambientais futuras evitando extinções locais (Matesanz et al. 2010; Hoffmann and Sgrò
2011). Assim, populações de ambientes mais secos podem ser mais adaptadas para lidar
com as previstas mudanças climáticas, devido não só às suas estratégias funcionais
139
associadas à baixa disponibilidade hídrica, mas também aos seus níveis mais elevados
de variação e plasticidade fenotípica em caracteres funcionais.
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