universidade federal do rio grande do norte centro de

Transcription

UNIVERSIDADE FEDERAL DO RIO GRANDE DO NORTE
CENTRO DE BIOCIÊNCIAS
PÓS-GRADUAÇÃO EM ECOLOGIA
DEPARTAMENTO DE BOTÂNICA, ECOLOGIA E ZOOLOGIA
Gustavo Brant de Carvalho Paterno
O PAPEL DE INTERAÇÕES POSITIVAS ENTRE PLANTAS NA REGENERAÇÃO DE ÁREAS
DEGRADADAS NA CAATINGA
Natal 2013
GUSTAVO BRANT DE CARVALHO PATERNO
O PAPEL DE INTERAÇÕES POSITIVAS ENTRE PLANTAS NA REGENERAÇÃO DE ÁREAS
DEGRADADAS NA CAATINGA
Dissertação Apresentada à Coordenação do Curso
de Pós-Graduação em Ecologia, da Universidade
Federal do Rio Grande do Norte em cumprimento
às exigências para obtenção do Grau de Mestre
Orientadora: Profa. Dra. Gislene Ganade
Natal 2013
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Catalogação da Publicação na Fonte. UFRN / Biblioteca Setorial do Centro de Biociências Paterno, Gustavo Brant de Carvalho. O papel de interações positivas entre plantas na regeneração de áreas degradadas na Caatinga / Gustavo Brant de
Carvalho Paterno. – Natal, RN, 2013.
95 f.: il.
Orientadora: Profa. Dra. Gislene Ganade.
Dissertação (Mestrado) – Universidade Federal do Rio Grande do Norte. Centro de Biociências. Pós-Graduação em
Ecologia.
1. Restauração ecológica – Dissertação. 2. Desertificação – Dissertação 3. Germinação – Dissertação. I. Ganade,
Gislene. II. Universidade Federal do Rio Grande do Norte. III. Título.
RN/UF/BSE-‐CB CDU 574 3
4
Dedico ao simples fato das “coisas” existirem
Afinal, qual seria a outra possibilidade?
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Agradecimentos
Agradecimentos
Família
Antes de tudo agradeço à minha família, às minhas raízes e aos meus ancestrais. Em todos
os momentos eu tive o completo apoio de todos. Minha mãe Stella, meu pai Cesar e minhas três
irmãs, Lú, Má e Ciça. Todos eles são co-responsáveis por eu estar aqui.
Agradeço às minhas primas Paola e Fernanda e suas famílias lindas (Marcão, Artur, Felipe,
Guilherme e Letícia), que me receberam em Natal e desde então me deram apoio incondicional a
tudo que precisei. Gratidão.
Amigos
Agradeço em especial algumas pessoas que ajudaram diretamente no meu trabalho: Guedão,
Andrée, Biel, Vanessa, Márcio, Junia, Breno, Bia, Marcos (minha antiga república) e Laura, Lucão,
Luquinhas, Silvana, Nícholas, Ana e Nat (minhas república Atual); Jana obrigada por estar sempre
ali e ser você. Agredeço com muito o carinho todo o pessoal do Laboratório de Restauração da
UFRN e amigos de trabalho pelo apoio constante no campo experimental e nas ideias do meu
trabalho (Guiga, Dri, Leo, Felipe, Digo, Aninha, Marina, Tida e Fernanda). Mai, gratidão pelo
carinho imenso e pelo apoio em tantos momentos difíceis, sua ajuda foi muito importante para a
conclusão deste trabalho. Agredeço meus amigos do CRAD, José Alves, André, Jeferson, Sobrinho,
Renato, Marcos, Marcondes, Fabiana, Uêdja, Jarina, Felipe e todos os demais, obrigado por me
receberem tão bem e por terem me ajudado no campo em Petrolina. Agradeço minhas mães de
Natal, Telma e Edmar. Obrigado por terem sido minha família em terras estrangeiras.
Professores
Gostaria de agradecer a todos os professores que passaram pelo meu caminho e me
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orientaram com enorme dedicação. Agradeço em especial aos professores de Ecologia pelo grande
empenho com que se dedicaram na minha formação: Coca, Renata, Márcio, Lígia, Adriana
Monteiro, Adriana Carvalho, Gabriel, Alexandre, Carlos, Dadão, e Toti.
Com grande adimiração e carinho, gostaria de agradecer o apoio fundamental da minha
orientadora Gislene Ganade (Gis). De fato, não é possível descrever a contribuição que você
proporcionou na minha formação como pesquisador e ser humano. Realmente, muito obrigado por
mais de quatro anos trabalhando em conjunto.
Instituições
Agradeço à UFRN e e todas as pessoas brasileiras que financiaram meus estudos. Agradeço
ao CNPQ pela disponibilização de três bolsas de iniciação científica durante minha graduação. e
uma bolsa de mestrado. Agradeço ao CRAD – Centro de Referência para Recuperação de Áreas
Degradas (Caatinga), pela hospedagem e suporte em todas as necessidades dos meus dois
experimentos. Agradeço ainda ai IDEMA, pelo apoio em expedições de campo.
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Sumário
Páginas
Introdução Geral...............................................................................................................
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Objetivos............................................................................................................................
16
Manuscrito 1: Facilitation driven by nurse identity and target ontogeny in a degraded
Brazilian semiarid dry forest...............................................................................................
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Summary........................................................................................................................
24
Introduction....................................................................................................................
25
Methods..........................................................................................................................
28
Results............................................................................................................................
33
Discussion......................................................................................................................
36
References......................................................................................................................
43
Tables.............................................................................................................................
48
Figures legends..............................................................................................................
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Figures............................................................................................................................
Manuscrito 2: Nurse-nurse facilitation: water availability and nurse size shaping the
regeneration in Brazilian semiarid lands.............................................................................
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57
Summary........................................................................................................................
58
Introduction....................................................................................................................
69
Methods..........................................................................................................................
64
Results............................................................................................................................
70
Discussion......................................................................................................................
73
Reference.......................................................................................................................
79
Tables.............................................................................................................................
83
Figures............................................................................................................................
89
ANEXO 1: Fotografias manuscrito 1.................................................................................
94
ANEXO 2: Fotografias manuscrito 2.................................................................................
95
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Introdução Geral
Caatinga, um bioma ameaçado
O Bioma Caatinga ocupa a maior parte da região semiárida brasileira, representando
aproximadamente 10% do território nacional (mais de 800 000 km2), na qual vivem mais de 25
milhões de pessoas (MMA, 2009). A maior parte da população é de baixa renda e enfrenta grande
dificuldade de acesso à água potável, devido principalmente a falta de infraestrutura e às condições
climáticas da região. O domínio das Caatingas é composto por uma grande diversidade de
fitofisionomias, variando de florestas arbóreas ou arbustivas até áreas com vegetação esparsa,
contendo pequenos arbustos, cactos e bromélias (Prado, 2005). A maioria das espécies vegetais
lenhosas apresentam características de adaptação às condições climáticas de baixa precipitação,
como a presença de espinhos, deciduidade marcante e microfilia, enquanto que as espécies
herbáceas são efêmeras e crescem apenas durante a estão chuvosa (Queiroz, 2009). Quando
comparada com outras regiões semiáridas do mundo, a Caatinga se destaca por ter alta riqueza de
espécies (aproximadamente 2000) e elevado grau endemismo (Leal et al. 2005; Leal et al. 2005b).
Apesar de boa parte do bioma ser subestimado (MMA, 2003; Leal et al. 2005), 34% das plantas,
57% dos peixes, 15 espécies de aves e 10 de mamíferos são endêmicos da Caatinga (Leal et al.
2005b).
O clima da Caatinga é caracterizado por apresentar parâmetros meteorológicos extremos
entre os biomas brasileiros (Prado, 2005). Além da grande variação na precipitação de um ano para
o outro, as condições climáticas da Caatinga envolvem alta radiação solar, baixa precipitação
(300-1000 mm-ano), alta taxa de evapotranspiração potencial (1500-2000 mm –ano) e forte
sazonalidade nas chuvas, que geralmente se concentram em apenas 3 meses do ano (Prado, 2005;
Queiroz, 2009). De uma maneira geral, 50% da área do bioma recebe menos que 750 mm-ano
enquanto que 50-70% das chuvas estão concentradas em apenas três meses, sendo que algumas
localidades podem ficar até 11 meses sem registro de precipitação (Prado, 2005). Por fim, a
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ocorrência de eventos drásticos, sejam chuvas torrenciais concentradas em curtos períodos de tempo
ou ausência completa de precipitação em alguns anos, também são fenômenos climáticos
característico da região (INSA, 2011).
Apesar de sua alta relevância ecológica, o estado de conservação do bioma é alarmante, no
qual apenas 1% da área total está protegido por unidades de conservação de proteção integral
(Hauff, 2010). Até 2008, estima-se que 45% da vegetação original já havia sido desmatada e a
degradação do bioma continua crescendo a uma taxa de 0,33% ao ano (MMA, 2010), entretanto,
outros estudos relatam que a Caatinga já perdeu 62% de sua área original enquanto que 80% já
sofreu algum tipo de alteração humana (INSA, 2011). A Caatinga enfrenta também problemas como
a fragmentação de habitat e a invasão de espécies exóticas, estando estes processos relacionados
com a extinção global de espécies (Millennium Ecosystem Assessment, 2005). Leão et al. 2011, em
um levantamento recente sobre as espécies exóticas da Caatinga, listaram 69 espécies de animais e
51 espécies de plantas invasoras do bioma, enquanto que Castelletti et al., 2005, através de
simulações da paisagem, sugerem que a Caatinga é um bioma extremamente fragmentado, restando
poucas áreas com vegetação nativa maiores que 10.000 km2. Esse conjunto de fatores fazem da
Caatinga um dos biomas mais ameaçados do Brasil.
Atualmente as principais fontes de degradação da Caatinga são: a agricultura de corte, o
desmatamento para produção de lenha e a criação de animais com remoção da vegetação nativa
(gado e caprinos principalmente) (Leal et al. 2005b). Esses impactos associados com o aumento das
secas e a diminuição da precipitação média anual, decorrentes das mudanças climáticas, são
proponentes do processo de desertificação que afeta grandes áreas do bioma (MMA, 2007; INSA,
2011). Além disso, áreas de Caatinga que foram abandonadas após atividades de agricultura
intensiva apresentam baixa taxa de regeneração, podendo levar décadas para retornar a sua
vegetação (Pereira et al. 2003). Por fim, o avanço na degradação ambiental da Caatinga tem levado
à perda de espécies e de processos ecológicos importantes para manutenção dos serviços ambientais
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(Leal et al. 2005b), trazendo assim, sérias consequências para a população vivente no semiárido
brasileiro.
Este cenário impõe grandes desafios para a conservação da Caatinga, os quais são agravados
pela carência econômica da região e consequente falta de investimentos do governo voltados para
conservação da biodiversidade (Leal et al. 2005; Leal et al. 2005b). Tendo o menor índice de
conhecimento científico entre os biomas brasileiros (Santos et al. 2011), a Caatinga carece
urgentemente de um maior aporte de trabalhos científicos (MMA 2003; Leal et al. 2005; MMA,
2007). Devido a existência de áreas degradadas extensas, que estão em processo de regeneração
inicial (MMA, 2009), estudos que permitam um maior entendimento dos processos que catalisam a
regeneração natural da vegetação nativa apresentam grande potencial para melhorarem a capacidade
de manejo de áreas degradadas. Tais estudos podem gerar grandes contribuições na prevenção do
avanço da desertificação, contribuindo assim para a conservação do bioma (MMA, 2003; MMA,
2007; INSA 2011).
Interações positivas e a estrutura de comunidades vegetais semiáridas
Interações entre plantas são processos centrais na estruturação de comunidades biológicas
que ocorrem ao redor do mundo (Michalet, 2006; Morin, 2012), sendo que a competição é um dos
principais mecanismos neste processo (Grime, 1973). Uma vez que espécies vegetais geralmente
utilizam os mesmos recursos para se desenvolver (água, luz e nutrientes), plantas vizinhas tendem a
interagir negativamente
umas com as outras, resultando na exclusão competitiva de uma das
espécies11. Entretanto, nas últimas duas décadas, diversos estudos têm demonstrado que a
facilitação (interações positivas entre plantas), em conjunto com a competição, também é um
mecanismo chave na sucessão ecológica e na estruturação de comunidades vegetais (Callaway,
1995; Pugnaire et al. 1996; Brooker et al. 2008). Segundo Holmgren et al. (1997), a facilitação
ocorre quando uma planta aumenta a disponibilidade de recursos que são limitantes para o
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crescimento da planta beneficiada, melhorando assim, sua chance de sobrevivência no ambiente.
Apesar de ser um fenômeno distribuído nos mais variados ecossistemas do mundo (Callway et al.
2002; Brooker et al. 2008), a facilitação têm sido registrada com mais frequência em ambientes
áridos e semiáridos (Flores & Jurado, 2003).
Nestes ambientes, nos quais o stress abiótico (pouca disponibilidade de água, elevada
temperatura do solo e alta evapotranspiração potencial) impõe grandes dificuldades para a
regeneração da comunidade vegetal, o estabelecimento da maioria das espécies em áreas sem
vegetação é bastante limitado (Franco & Nobel, 1988; Valiente-Banuet et al. 1991). Uma vez que a
sombra de indivíduos pré-estabelecidos diminui a amplitude térmica do solo e aumenta umidade, a
colonização de novas áreas por plântulas tende a ser favorecida pelo microclima menos estressante
gerado sob a copa de espécies facilitadoras (nurse plants) (Franco & Nobel, 1988; Valiente-Banuet
et al. 1991; Valiente-Banuet & Ezcurra, 1991). Muitos trabalhos têm demonstrado que além de
melhorar as condições microclimáticas do solo, estas espécies podem também aumentar a
disponibilidade de nutrientes para as plântulas, fornecendo microambientes mais adequados (“ilhas
de fertilidade”) para a germinação, estabelecimento e crescimento de espécies menos tolerantes a
stress (Pugnaire et al. 1996; Walker et al. 2001; para uma revisão dos principais mecanismos de
facilitação veja Callaway, 1995). Mesmo que as interações positivas entre plantas vizinhas ocorram
em escalas locais, seus efeitos podem repercutir em escalas mais amplas, sendo mecanismos
importantes na manutenção da biodiversidade mundial (Hacker & Gaines, 1997; Pugnaire et al.
1996; Callaway et al. 2002; Valiente-Bunet et al. 2006; Holmgren & Schefer, 2010). Estudos
recentes apontam que a facilitação contribui para o aumento da diversidade no nível da comunidade
(Pugnaire, 2010) e pode inclusive operar em escalas temporais geológicas (Valiente-Banuet et al.
2006). Estes autores, demonstraram que muitas espécies do período terciário (com clima mais
úmido), registradas em ecossistemas mediterrâneos, persistiram no ambiente provavelmente devido
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a facilitação por espécies que evoluíram no período quaternário (com clima mais seco), evitando
assim, a extinção em escala global de táxons menos tolerantes a seca (Valiente-Banuet et al. 2006).
O balanço entre facilitação e competição
De uma maneira geral, interações positivas e negativas atuam de forma conjunta, sendo o
resultado final de interações entre plantas vizinhas determinado pelo balanço líquido dessas duas
forças antagônicas (Holmgren et al. 1997; Pugnaire & Luque, 2001). A partir do recente aumento da
popularidade de interações positivas no meio científico, diversos mecanismos foram propostos para
tentar prever em quais condições a facilitação ou a competição devem prevalecer como processos
dominantes nas comunidades biológicas (Brooker et al. 2008). Na metade dos anos noventa,
Bertness & Callaway (1994) e Callaway & Walker (1997) propuseram que o balanço entre
competição e facilitação depende do grau de stress do ambiente (Hipótese do Gradiente de Stress –
SGH). Estes autores sugeriram que a frequência de interações positivas deve ser maior em
ambientes mais estressantes ou pouco produtivos enquanto que a competição deve dominar em
ambientes mais amenos ou muito produtivos (Bertness & Callaway, 1994; Callway & Walker,
1997). De acordo com estas previsões, Callaway et al. (2002), através experimentos realizados em
diversas comunidades vegetais alpinas do mundo, encontrou que a facilitação foi a interação
predominante em ambientes mais estressantes (localidades com altitude elevada), enquanto que a
competição se destacou em ambientes menos estressantes (localidades de menor altitude). Apesar
de muitos estudos corroborarem a SGH (Callaway et al. 2002; Brooker, 2008), existem vários
contraexemplos que desafiam suas previsões (Ganade & Brown, 2002; Maestre & Cortina, 2004;
Maestre et al. 2006, demonstrando que outros fatores também influenciam o balanço entre
facilitação e competição (Reginos et al. 2005). Este cenário, têm proporcionado espaço para um
intenso debate científico e o avanço teórico da ecologia vegetal, que por sua vez, possibilitou um
ganho significativo em nossa compreensão dos processos que estruturam comunidades biológicas
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(Bruno et al. 2003; Michallet, 2006; Brooker et al 2008; Maestre et al. 2009; Homgreen & Scheffer,
2010).
Adicionalmente, a ontogenia das espécies envolvidas também pode ocasionar mudanças de
facilitação para competição (Valient-Banuet et al. 1991; Pugnaire et al. 1996; Rousset & Lepart,
2000; Miriti, 2006; Reisman-Berman, 2007). Valiente-Banuet et al. (1991), demonstraram em um
vale semiárido no México, que o cactos Neubuxbaumia tetetzo, após ser facilitado pelo arbusto
Mimosa luisana enquanto jovem, suprimia a planta facilitadora quando adulto, provavelmente
devido a competição por água. Miriti, (2006) também encontrou mudanças de facilitação para
competição ao longo do desenvolvimento ontogenético da espécie beneficiada, evidenciando que
indivíduos jovens cresciam melhor perto da planta facilitadora enquanto que os adultos eram
desfavorecidos. No entanto, a maioria destes estudos utilizaram métodos estatísticos baseados em
dados de associação espacial para sugerir interações positivas ou negativas entre as espécies,
existindo poucos trabalhos com experimentos de campo ou que consideraram o estágio de vida da
planta facilitadora (Pugnaire et al. 1996; Reisman-Berman, 2007). Neste sentido, existe uma grande
carência de trabalhos que testem experimentalmente como a idade ou o tamanho de plantas
facilitadoras afetam a direção e a intensidade de interações entre plantas.
Aspectos relacionados com a estratégia de vida das espécies, como a tolerância à stress,
também são considerados fatores importantes no balanço de interações entre plantas (Maestre et al.
2009). Liancourt et al. (2005), através de experimentos envolvendo espécies com diferentes
habilidades competitivas e tolerância a stress, mostraram que as espécies menos tolerantes e mais
competitivas são mais beneficiadas que espécies tolerantes a stress. Isso ocorre, justamente por que
espécies menos tolerantes são mais dependentes das condições amenas geradas na presença de
plantas vizinhas (Liancourt et a. 2005; Maestre et al. 2009). Entretanto, a maioria dos trabalhos
experimentais desenvolvidos até o momento analisaram apenas interações entre pares de espécies,
não existindo um entendimento claro de como a facilitação pode afetar a dinâmica de comunidades
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contendo muitas espécies e estratégias de vida contrastantes (Pugnaire, 2010; Xu et al. 2010). Por
exemplo, Landero & Valient-Banuet (2010) demonstraram que diferentes espécies facilitadoras
afetaram de forma distinta a dinâmica de populações de uma mesma espécie beneficiada
(Neubuxbaumia mezcalaensis), evidenciando assim, a importância de interações espécie-específicas
no balanço entre facilitação e competição (Callaway, 1998). A partir destes resultados, fica evidente
que experimentos envolvendo múltiplas espécies de plantas facilitadoras e beneficiadas podem
proporcionar um entendimento mais detalhado sobre a importância da facilitação no nível da
comunidade (Pugnaire, 2010; Xu et al. 2010). Em resumo, o balanço de interações entre plantas é
um processo complexo e dependente de muitos fatores que atuam conjuntamente, sendo muitas
vezes contexto-dependente (Reginos et al. 2005).
Neste contexto, a Caatinga se apresenta como um sistema ideal para o desenvolvimento de
experimentos e estudos envolvendo interações positivas. Uma vez que possui um clima marcado
por variações intensas na disponibilidade hídrica, a Caatinga proporciona condições experimentais
para o teste de diversas hipóteses relacionadas com o balanço entre competição e facilitação. Além
disso, existe uma grande lacuna de informação sobre o bioma, não existindo um entendimento de
quais são os principais mecanismos que estruturam suas comunidades vegetais. Até o presente
momento, o único trabalho experimental, de conhecimento do autor, que testa a importância de
interações positivas na Caatinga foi desenvolvido por Meiado, 2008, em sua dissertação de
mestrado, realizada no Parque Nacional do Catimbau. Neste estudo, o autor demonstrou que a
espécie Trischidium molle é um arbusto facilitador na Caatinga, melhorando as condições para a
germinação da comunidade regenerante sob sua copa (Meiado, 2008). Neste sentido, esta
dissertação em conjunto com trabalho de Meiado (2008), representam a abertura de uma nova área
de pesquisa para a Caatinga, evidenciando que interações positivas podem ser um processo chave
nesse bioma tão pouco estudado. Por fim, o entendimento detalhado dos mecanismos que afetam as
interações entre plantas facilitadoras e espécies beneficiadas da Caatinga, podem oferecer uma
15
excelente base de referencia para projetos que visem a restauração ecológica de áreas degradadas e
a prevenção da desertificação (Gomez-Aparício et al. 2004; Gomez-Aparício, 2009; Matías et al.
2012).
Objetivo Geral
Investigar quais são os principais mecanismos e fatores que modulam as interações entre
plantas na Caatinga e como a facilitação afeta a regeneração natural de áreas degradadas e a
estruturação de comunidades vegetais nesse bioma
Objetivos Específicos
1. Manuscrito 1
a. Investigar se interações positivas são um mecanismo importante na estruturação de
comunidades vegetais da Caatinga
b. Investigar se as interações entre plantas facilitadoras e espécies beneficiadas são
espécie-específicas e como essas interações variam em função da estágio de vida das
plantas beneficiadas
2. Manuscrito 2
a. Investigar como a espécie pioneira Mimosa tenuiflora afeta as condições abióticas do
solo
b. Investigar como a facilitação entre duas espécies pioneiras varia em intensidade e
importância ao longo de um gradiente de tamanho da planta facilitadora,
disponibilidade de água (nível de stress) e estágio de vida da espécie beneficiada
16
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21
Manuscrito a ser submetido ao Periódico Journal of Ecology
22
Facilitation driven by nurse identity and target ontogeny in a
degraded Brazilian semiarid dry forest
Gustavo Brant de Carvalho Paterno1
Gislene Ganade1 *
Fabiana de Arantes Basso2
José Alves de Siqueira Filho2
1Universidade
Federal do Rio Grande do Norte (UFRN), Natal, Brasil.
2Universidade
Federal do Vale do São Francisco (UNIVASF), Petrolina, Brasil.
*gganade@gmail.com
23
Summary
1. Facilitation by nurse plants is now widely recognized as a key process structuring plant
communities in dry lands but the mechanisms determining the net balance between
facilitation and competition remain uncertain. Most studies have focused on pair-wise
experiments that are neither able to detect species-specific interactions nor their impacts on
plant community regeneration.
2. We conducted a factorial multi-species experiment in a degraded Brazilian semi-arid forest
to test how species-specific interactions and target ontogeny modulate intensity and
direction of nurse facilitation. Seeds and seedlings of five target species were sown in the
presence and absence of three pioneer tree species and target performance was monitored
for distinct ontogenetic stages. We also measured the diversity and composition of
regenerating plant communities established under the same nurse treatments.
3. Facilitation by nurse plants was a widespread process in degraded semi-arid Caatinga since
species with completely different ecological strategies improved their germination and
establishment underneath nurse plants. Nurse plants also increased abundance and richness
of regenerating plant communities when compared with open sites. However, as targets
ontogeny developed, facilitation shifted to competition for particular target/nurse
combinations revealing that some nurses could became competitors over time.
4. Synthesis: Our results agree with previous predictions that facilitation by nurse plants can be
critical in promoting recruitment and maintaining diversity on harsh environments.
However, we provide novel experimental evidence that the balance between facilitation and
competition could be simultaneously influenced by nurse identity and target ontogeny which
strongly affect succession and restoration methods.
Key-words: Benefactor, competition, germination, establishment, restoration, Caatinga, diversity,
species-specific patterns
24
Introduction
Interactions among plant species are important forces influencing the structure and
composition of plant communities. Although in the past many studies focused on competition
(Grime 1977) recent research showed that positive interactions (facilitation) could play an
important role structuring plant communities (Broker et al. 2008). As facilitation and competition
act simultaneously, the net balance between these contrasting forces will determine the final
outcome of plant interactions (Holmgren et al. 1997). Interactions can shift from facilitation to
competition depending on: environmental severity (Bertness & Callaway, 1994; Lortie & Callaway,
2006), ontogeny (Valiente-Banuet et al. 1991; Rousset & Lepart, 2000; Miriti, 2006), life-form
(Gómez-Aparicio, 2009); plant density (Walker & Chapin, 1987); grazing intensity (Graff et al.
2007) and stress-tolerance ability (Liancourt et al. 2005).
Positive plant interactions have been reported for a broad range of ecosystems (Brooker et
al. 2008), from tropical and subtropical rainforests (Ganade & Brown, 2002; Zanine et al. 2006) to
arid environments where facilitation tends to be more frequent (Callaway, 1995; Flores & Jurado,
2003). While plants compete for similar resources, especially light, water and nutrients, there are
many ways one plant can improve conditions for others (Callaway, 1995 and Callaway & Walker,
1997). Facilitation occurs through amelioration of microclimatic conditions (Franco & Nobel,
1989), reduction of herbivory (Graff et al. 2007); soil nutrients improvement (Callaway, 1995) or
seed dispersal enhancement (Zanini & Ganade, 2005; Dias et al. 2005).
There is now strong evidence that nurse plants can influence plant community diversity and
function (Cavieres & Badano, 2009; Cavieres & Badano 2010). Mesquita et al. (2001) showed that
during Amazonian secondary succession pioneer species could differ in the way they influence
community regeneration by promoting alternative successional pathways with contrasting species
diversity. In a degraded Araucaria forest in Brazil, Ganade et al. (2011) found that the pioneer
species Vernonia discolor maintained greater native plant diversity beneath its canopy and
25
hampered pine invasion, while Baccharis uncinella facilitated pine invasion and diminished plant
diversity under its crown. Facilitation effects could also improve ecosystem function by allowing
the coexistence of species with distinct ecological strategies and evolutionary histories (Cavieres &
Badano, 2010). Meanwhile, the inclusion of positive interactions on the fundamental ecological
theory is still only rising (Bruno et al. 2003; Brooker et al. 2008).
In arid and semi-arid environments plant community regeneration strongly depend on
facilitation, although ontogenetic shifts from facilitation to competition might occur as seedlings
grow (Rousset & Lepart, 2000; Ganade & Brown 2002, Miriti, 2006). Nurse shade can diminish
temperature amplitudes and decrease water evaporation providing better conditions for young
individuals to establish under water stress (Franco & Nobel, 1989; Valiente-Banuet et al. 1991).
However, studies on plant spatial distribution have shown that as target plants grow, disputes over
water and other resources may emerge.
Miriti (2006) found strong ontogenetic shifts from
facilitation to competition where neighbors of Ambrosia dumosa improved juveniles performance
but suffer competition from adults. Until now, there is few experimental evidence of how plant
ontogeny can influence the intensity and direction of species-specific interactions in dry lands.
Another critical factor is that semi-arid environments tend to suffer desertification, meaning
irreversible catastrophic shifts from a vegetated to a non-vegetated state (Rietkerk et al. 2004). In
this scenario, facilitation through nurse plants might be a key process for managing ecosystems to a
recovered state. Recent studies have shown that nurse plants can be critical tools for restoration
programs (Gómez-Aparicio et al. 2004; Padilla & Cavieres, 2006), especially in semi-arid
environments (Gómez-Aparcicio, 2009).
Caatinga is a mosaic of tropical dry forest and shrubby vegetation located at northeast
Brazil. Most of its woody species loose their leaves during long periods of drought while its
herbaceous species are ephemeral and grow only during rain events. Caatinga’s climate is marked
by high inter annual variation of rainfall with frequent occurrences of severe droughts (Prado,
26
2003). With high plant diversity and endemism, Caatinga covers nearly 10% of the Brazilian
territory. Unfortunately, this poorly protected ecosystem has been suffering intense human impact
(large areas under desertification process) and sustains the lowest score of scientific knowledge
when compared to other Brazilian ecosystems (Leal et al 2005; Santos et al. 2011, INSA, 2011).
Thus, there is a complete lack of information on the main processes governing community structure
and plant succession in degraded Caatinga lands.
We seek to answer the following questions: (i) Is facilitation by pioneer woody species an
important process structuring diversity and composition of Caatinga plant communities?; (ii) How
pioneer woody species affect seed loss, germination and establishment of a range of target
species?; (iii) Are nurse-target interactions species-specific and how this relationship changes
through target species ontogeny?
27
Methods
STUDY SITE
The study was conducted on a 0.5 ha site at the Centre for Restoration of Degraded Areas
(CRAD) (9º19’45,10”S 40º32’52,44”W), located near Petrolina, north-eastern Brazil. The mean
annual rainfall is 500 mm, with rainy seasons from November to April. The climate is classified as
semi-arid, characterized by periodic severe droughts and high variability of inter-annual rainfall
(Coelho, 2009).
The study site consists of a shrubby Caatinga forest that has been degraded by grazing and
logging activities during the last decades. The site has been fenced since 2005 to avoid goat
browsing. There are only 30 plant species registered in which 20 are annual herbs and 10 are woody
species. It is likely that many species became locally extinct as a result of past disturbances, severe
bare ground conditions and absence of seed sources. The following woody plants are dominant in
the area: Mimosa tenuilfora (Willd.) Poir. (Fabaceae), Poincianella microphylla (Mart. Ex G.Don)
L.P.Queiroz (Fabaceae), Jatropha mutabilis (Pohl) Baill. (Euphorbiaceae) and Cnidoscolus
quercifolius Pohl (Euphorbiaceae) (Coelho, 2009).
STUDY SPECIES
Species selected were classified into two groups: potential nurse plants (from now on nurse
plants) and target species. To select nurse plants, the following criteria were required: (I) woody
species; (ii) short period of leaf deciduousness (provides greater shade); and (iii) species common in
degraded and pristine Caatinga. Target species were selected from CRAD seed collection based on
their contrasting ecological strategies. The target species selected have rapid germination, are
woody plants, but exhibit distinct conservation status (Table 1). Three nurse plants (Cnidoscolus
quercifolius Pohl, Mimosa tenuiflora (Willd.) Poir. and Poincianella microphylla (Mart. Ex G.Don)
L.P.Queiroz) and six target species (Amburana cearenses (Allemão) A.C.Sm., Aspidosperma
28
pyrifolium Mart, Erythrina velutina Willd., Myracrodruon urundeuva Allemão, Poincianella
pyramidalis (Tul.) L.P. Queiroz and Pseudobombax simplicifolium A. Robyns) were selected for the
seed sowing and seedling transplantation experiments (Table 1).
For the seedling transplantation
experiment, A. cearensis was replaced by P. simplicifolium due to lack of available seedlings.
GREEN HOUSE GERMINATION TESTS
Seed viability and seedling establishment tests were conducted for all target species in a
greenhouse located at CRAD. For each target species (with exception of P. simplicifolium) four
replicates of thirty seeds were sown in soil plus pine bark and osmocote fertilizer. Seeds were
irrigated three times a day, light conditions were reduced by 20% under greenhouse structure. Each
seed group was placed at random on the greenhouse bench. Mechanical scarification was performed
to break E. velutina seeds dormancy (Matheus et al. 2010). The number of seeds germinated and
seedlings established was registered at two days intervals during 20 days.
SURVEY UNDER POTENTIAL NURSE PLANTS
To test if nurse plants enhance natural recruitment and affect plant community structure and
composition, an inventory of woody and Cactaceae plants was conducted in areas with and without
nurse plants. At the study site, eight adult individuals of each nurse plants (twenty four individuals
in total) were selected randomly from a pool of all eligible individuals at the site. Nurses selected
were surrounded by bare soil with no crown overlay with neighbours. A 3 x 3 m plot was delimited
with one nurse plant at the centre, comprising an area of 9 m² under the selected plant (nurse
treatment). For the “no nurse” treatment, 3 x 3m plots were implemented in adjacent open areas
randomly selected within a 7 m range from the nurse plant. In these areas, adult woody plants were
absent and bare ground frequently occurred. Pairs of plots, with and without nurse plants were
considered blocks. All species registered inside study plots were identified with the help of CRAD
29
specialists.
To test if potential nurse plants enhance species richness and abundance beneath their
canopies we ran a generalized mixed model (GMM) with Poisson error distribution, “nurse effect”
as split factor and “block” as random effect (Crawley, 2007). To account for the effect of abundance
on richness, the latter was used as a response variable and the former as a covariant. The “nurse
effect” (nurse and no nurse treatments) and the “nurse species” (C. quercifolus, M. tenuiflora and P.
microphylla) were used as fixed factors. To access statistical significance of fixed factors the
deviance from the models were compared through log likelihood ratio tests.
To test if nurse plants affected plant community composition we used PERMANOVA nonparametric test, with species abundances as response variables, “nurse effect” and “nurse species”
as explanatory variables. To solve the problem of empty samples associated with open sites, the
distances matrix was calculated with the Zero-adjusted Bray-Curtis coefficient, which considers
denude assemblages (Clarke et al. 2006). To visualize possible differences in plant community
composition between open sites and nurse plots, we plotted the two main axis of a Principal
Coordinates Analysis (PcoA) based on species abundances using Bray-Curtis distance.
FIELD EXPERIMENT
Seeds and seedlings of the five target species (A. pyrifolium, M. urundeuva, A. cearensis, E.
velutina, P. pyramidalis) were placed in the field and subjected to the presence and absence of nurse
plants. In the seedling experiment A. cearensis was replaced by P. simplicifolium. Both experiments
were implemented at the same “nurse” and “no nurse” replicates described in the previous section.
Experiments were structured in a split-plot design with target species subplots randomly assigned
within “nurse” and “no nurse” treatments (split-factor). Groups of 25 seeds of each target species
were randomly assign in each treatment. Seeds were sown 10 cm apart and marked with wooden
sticks. A total of 6000 seeds were used, 1200 per target species. Distances between blocks varied
30
from 2 to 40 m. In the seedling experiment, five subplots (40 x 50cm) were delimited at the
opposite side of the seeds subplots. Four seedlings of each target species were transplanted per
subplot 25 cm apart. A total of 960 seedlings (192 per target species) were used.
Experiments started in January 2010, at the beginning of the raining season to improve
germination and survival. Seeds were collected in local Caatinga sites and stored in a low
temperature chamber (5-7 °C) for approximately six months, with exception of P. pyramidalis
seeds, which were stored for two years. All seedlings were produced in identical conditions inside
CRAD green house and were three to four months old. Before transplantation all seedlings were
subjected to acclimation in full sun and limited water for one month to simulate field conditions. All
seedlings that died at the first week after transplantation were replaced.
For the seed experiment, the number of seeds lost (predation, wind or runoff), germinated
(root emission) and the number of seedlings established (leaf emergence) were registered weekly
during five months. To test if the presence of nurse plants affected target species seed loss,
germination and seedling establishment we ran a split-plot GMM with binomial errors for each
nurse species separately. Nurse effect and target species were used as fixed factors. The significance
of each factor was tested with a log-likelihood ratio test. For the seedling experiment, the number of
survived seedlings and their height were record monthly during five months.
To access the intensity and direction of interactions between nurse plants and target species,
the relative intensity index (RII, see Armas et al. 2004) was calculated for each of the following
ontogenetic phase: germination, establishment, seedling survival and seedling growth. The RII is
calculated by the formula:
where (Bo) is the performance of target species in the absence of nurse plants and (Bw) is the
performance of target species at the presence of nurse plants. This index represents the relative
31
effect of nurse plant on target species, varying from -1 (maximum competition) to +1 (maximum
facilitation) (Armas et al. 2004). To test if the relationship between nurse plants and target species
were species-specific and changed with ontogeny, RII indexes (response variable)were compared
for each ontogenetic stage separately, through a linear mixed model (LMM) using “nurse species”
and “target species” treatments as factors. All statistical analysis was performed using R 2.15.0 (R
Development Core Team, 2012). GLMM models used the “lme4” package (Bates et al. 2011) and
PERMANOVA used “vegan” package (Oksanen et al. 2012).
32
Results
GREEN HOUSE EXPERIMENT
In controlled conditions target species differed in their germination (F4,15 = 98; p < 0,001)
and establishment performance (F4,15 = 48; p < 0,001). A. pyrifolium (17% and 11% );
P.
pyramidalis (91% and 84%); A. cearensis (85% and 85%); E. velutina (86% and 67% ); and M.
urundeuva (56% and 53%) for germination and establishment respectively. Despite differences
between targets, most seeds that germinated were able to establish.
SURVEY UNDER NURSE PLANTS
Richness and abundance of woody seedlings found under nurse plants were much higher
than in areas without nurses. Under nurses abundance ranged from 2-12 times higher and richness
from 2-16 times higher (Fig. 1a and1b). Despite positive effects of abundance on species richness,
when the first was included as covariant in the model, “nurse effect” still explained richness
significantly (Table 2). All nurse plants showed similar effects on species richness and abundance
and there were no interactions among factors (Table 2).
Composition of the regenerating plant community differed between open areas and nurse
canopy (Fig. 1c, F45,1 = 8.79; p < 0.001; Table s1 in supplementary material), however, there was no
difference between nurse species (F45,2 = 1.18; p = 0.297). Ninety-two individuals of eight species
were found under the canopy of nurse plants, encompassing four families (Burseraceae, Cactaceae,
Euphorbiaceae, Fabaceae), 37 under C. quercifolius, 31 under M. tenuiflora and 24 under P.
microphylla ( Table s2, supplementary material). Four species were only found under the canopy of
nurse plants (Commiphora leptophloeos, Melocactus zehntneri (endemic & endangered), Tacinga
inamoena (endemic) and Mimosa tenuiflora. In open areas only 13 individuals of four species were
found all occurring under nurse canopy. The presence of nurses increased species, genus and
families by 50%, endemic species by 66% and sheltered all endangered species found in our
33
surveys.
TRANSPLANTATION EXPERIMENTS
In general, nurse plants had no effect on seed loss, with the exception of P. microphylla that
showed a significant interaction between “nurse effect” and “target species” indicating speciesspecific interactions (Fig. 2b; Table 3). Target species had different probabilities of seed loss, M.
urundeuva and E. velutina had the highest rates while the other targets showed probabilities equal
or lower than 20% (Fig. 2abc).
The presence of nurse plants had a strong positive effect on seed germination probability for
all target species, increasing it from 2 to 9 fold, depending on the target species identity (Table 3;
Fig. 2def). For the nurse C. quercifolius there was a significant interaction between “nurse effect”
and “target species”, demonstrating that target species differed in the way their germination
performance was positively affected by this nurse (Table 3). For instance, A. cearencis showed
higher seed germination improvements when compared with other targets (Fig. 2d).
When considering seedling establishment, the presence of nurse plants also had positive
effects on target species (although marginal for P. mycrophylla ) (Table 3, Fig. 2ghi). Because few
seedlings of A. pyrifolium, E. velutina and A. cearensis were able to establish, the nurse effect on
these target species could not be fully detected. However, nurse plants improved seedling
establishment for P. pyramidalis and M. urundeuva.
Although nurses improved targets early performance, all experimental plants (6000 seeds
and 960 seedlings) died within six months due to atypical drought. Precipitation during this time
was 64-75% lower than what is historically expected for the first three months of the growing
season.
FACILITATION VERSUS COMPETITION
The RII index revealed clear shifts from facilitation to competition as target ontogeny
34
developed (Fig. 3, Table 4). Facilitation prevailed during germination and survival phases with no
significant differences between nurse and target species (Fig. 3a and 3c). Nonetheless, seedling
establishment performance showed a significant “nurse” “target” interaction, with some
combinations being neutral or minor while others showed extreme values of facilitation (Fig. 3b).
For example, M. urundeuva was extremely facilitated by C. quercifolius and P. microphylla and not
affected by M. tenuiflora, while A. cearensis was only facilitated by M. tenuiflora and not affected
by other nurses. Additionally, nurse plants affected target latter development in different ways, P.
microphylla facilitates, C. quercifolius was neutral and M. tenuiflora showed negative effects on
target growth (Fig. 3d). As a whole, P. microphylla was the nurse that showed the most consistent
patterns of facilitation throughout target ontogeny.
35
Discussion
Facilitation by nurse plants was widespread in degraded areas of the semi-arid Caatinga as
predicted by the stress gradient hypothesis (Bertness & Callaway, 1994; Callaway & Walker, 1997).
This is so because species with completely different ecological strategies improved their
germination and establishment underneath nurse plants that are common in Caatinga dry forest
degraded areas . Positive effects of nurse plants on seed germination and seedling establishment
have been registered for a wide range of ecosystems (Callaway, 1995; Zanini et al. 2006; Brooker et
al. 2008). However, most facilitation experiments have been restricted to pairwise interactions,
while only few studies have accessed the impact of facilitation in multiple-species experiments or at
the entire community level (Cavieres & Bandano, 2009; Landero & Valiente-Banuet, 2010). This
facilitation processes unveiled by our experiment is most likely to be driven by the unsuitable
abiotic conditions found in Caatinga open sites, such as drought, high soil temperatures and direct
radiation. Thus, as demonstrated for others dry ecosystems, microclimatic amelioration by nurse
plants seems to be the major mechanism promoting better establishment and survival at this plant
community (Gómez-Aparicio et al. 2004).
This work also provides novel experimental results highlighting that the balance between
facilitation and competition could be simultaneously influenced by nurse species identity and target
species ontogeny. For seed germination, facilitation was a widespread phenomenon regardless nurse
identity. However, as target ontogenetic development progressed, differences between nurse plants
became clear. P. microphylla remained a good benefactor improving target species growth, while C.
quercifolius and M. tenuiflora, depending on the target species in question, showed neutral and/or
negative effects. These results indicate that plant community regeneration may strongly depend on a
broad range of nurse species that can facilitate distinct arrays of plant functional groups at different
ontogenetic stages (Callaway, 1998; Landero & Valient-Banuet, 2010). Thus, species-specific
interactions between nurse pioneer trees and regenerating species might affect plant community
36
future composition (Mesquita et al. 2001; Rousset & Lepart, 2000; Ganade et al. 2011).
Nurse characteristics that control their distinct influence on target species performance are
yet to be unveiled.
Differences in root structure and soil use strategies may lead to micro scale
differences in soil properties beneath distinct nurse species. Nurse canopy size and architecture are
also important factors affecting nurse performance and can influence the net balance between
facilitation and competition (Tewksbury & Lloyde, 2001). Interactions between nurse size and
water stress are still poorly tested, but Reisman-Berman (2007) found age-related interactions in a
semiarid shrub ecosystem, where nurse effect changed from positive for young nurses to negative
for old nurses. In the semi-arid Caatinga, nurses that are able to increase environmental water
availability are most likely to facilitate target species. In our study, best and worse facilitators
exhibited very similar ecological and morphological characteristics, differing only in their
conservation status. However, P. microphylla and C. quercifolius are species with denser leaves
which provide greater shade. The best facilitator (P. microphylla) was an endemic species while the
worse facilitator expressed wide geographical occurrence. It is plausible that endemic species would
be less aggressive in the way they explore water while wide occurrence species would be more
efficient in competing for this key resource. Future works should look at how morphological traits
and geographical distribution of nurse species would reflect their facilitation skills.
It is well recognized that ontogenetic changes influence the net balance of competition and
facilitation in arid environments (Miriti, 2006). However, we do not have knowledge of multiplespecies experiments that tested how ontogeny affects intensity and direction of plant interactions
(but see Rouseet et al. 2000). Our results show that depending on the ontogenetic stage of target
species, nurse influence may change from facilitation to competition. During early ontogenetic
phases (germination) all target species were benefited by the presence of all nurse plants studied.
Water stress may be an important force controlling this pattern because all species showed much
lower germination rates in the field compared with the green house experiments. However, nurse
37
plants could compensate part of this stress improving germination by more than 3 times in some
cases. For latter ontogenetic stages (seedlings), nurse species started to compete with target species
decreasing their ability to grow beneath nurse shelter. In semiarid environments rainfall is
extremely unpredictable, with long drought intervals (Prado, 2003). For successful performance,
seedlings need to grow to a certain size to withstand the next drought period otherwise they may die
due to tissue fragility (Fenner & Thompson 2005). Our results indicate that when more sensitive
target species interact with a resource demanding nurse, improvements of the key resource (water)
provided by this nurse may not be sufficient to overcome negative effects of nurse competition by
other resources (Holmgren et al. 1997). Future studies should go beyond the early stages of
development to fully access the role of ontogeny on plant interactions and succession.
Previous works have shown that positive interactions can enhance community richness by
enlarging realized niche or releasing intolerant species from stress (Bruno et al. 2003; Michalet et
al. 2006). If so, one would expect to find higher species richness and different species composition
beneath nurse canopies when compared with open areas. In agreement with these predictions our
results corroborate the hypothesis that facilitation by nurse plants increase community richness
(Cavieres & Badano, 2009). Additionally, many species found under nurses were not found in open
areas showing that a range of plants, including endemic and endangered species, could be locally
extinct in the absence of nurses. These data suggest that less-tolerant species depend on specific
sheltered conditions provided by nurses to establish and survive (Zonneveld et al. 2012), therefore,
nurse plants appear to play a key role in maintaining local diversity at all taxonomic levels
(Cavieres & Badano, 2010).
Increased plant regeneration under nurse trees could also be attributed to an increased rate of
seed arrival bellow nurses, because seed dispersers tend to use nurse structure as perches (Zanini &
Ganade 2005; Dias et al. 2005). We attribute minor importance to this type of indirect facilitation
since all nurse species studied are anemochoric and therefore do not offer any attractive reward.
38
Moreover, this possible lack of nurse ability to attract dispersers would restrict colonization of a
range of sensitive target plants that have to perform long distance travelling. Indeed, we did not find
any of our experimentally studied target species present in our community regeneration survey.
These findings would explain why we did not encounter detectable differences in community
regeneration among nurse species. Future works should look at the relative importance of dispersal
and facilitation as drivers of secondary succession where nurse plants seem to catalyze the
regeneration of various species and functional groups (Fuentes-Castillo et al 2012).
IMPLICATIONS FOR ECOLOGICAL RESTORATION IN SEMIARID LANDS
The potential for using nurse plants as tools for restorations programs are now widely
recognized for different ecosystems (Padilla & Pugnaire, 2006; Gómes-Aparicio 2009). Our results
points out that pioneer shrubs and trees are good candidates to be used in restoration programs of
semiarid degraded lands (Gómes-Aparicio 2009). Our survey has shown that nurse plants are
critical for maintaining endemic and endangered species in degraded areas. However, we found
strong evidence that nurse plant positive effects are not enough to restrain mortality in drier years,
in agreement with the refined stress-gradient hypothesis (Maestre et al. 2009). Therefore, during
drought events the use of nurse-assisted technics by itself may be inefficient. New studies should
test if nurse plants combined with artificial irrigation could be an option to achieve successful target
species establishment during restoration. A second major challenge for the use of nurse-assisted
technics is to fully understand how species-specific interactions affect natural regeneration. This
fine-scale comprehension could provide direct insights into which species should be used as nurse
plants forbetter results on local plant community regeneration (Gómes-Aparicio 2009). Complex
interaction may arise among different nurse plants and target species because facilitation effects can
be highly depended on nurse identity and target ontogeny. Therefore, restoration programs that aim
to use nurse-based technics need to investigate how different dominant nurse species might
39
influence diversity and regeneration of plant communities (Mesquita et al. 2001; Ganade & Brown,
2002). We found evidences that P. microphylla and C. quercifolius are better nurse plants in
degraded Caatinga .These nurses enhanced performance of different targets on a variety of
ontogenetic phases (although this positive effect was more evident for P. microphylla). Even if our
findings are restricted to early establishment, survival during this particular phase is usually crucial
for launching plant populations, because Caatinga species have evolved a range of adaptations to
tolerate extreme drought events during latter developmental stages (Prado, et al. 2003).
Finally, processes of facilitation could influence vegetation resilience and resistance in
semiarid degraded lands by expanding vegetation patches that would otherwise be prone to
desertification (Rietkerk et al. 2004; Scheffer et al. 2005). Our experimental evidences also call
attention to the difficulty to restore degraded areas on bare ground. Miles et al. (2006) in a global
survey of tropical dry forests found that practically all remaining areas are now highly fragmented
and threated by human activities. The Caatinga dry forest represents well such cases with the
aggravation of having large areas affect by desertification and climatic models foreseeing an even
drier future (INSA, 2011). In this scenario, it is imperative to stop land degradation and increase
efforts to create and restore new protected areas (Leal et al. 2005). Gathering of future information
on the way facilitation processes contribute to ecosystem water retention might generate practical
directions to prevent desertification expansion and improve restoration practices for managers and
policy makers.
CONCLUSIONS
Facilitation is an important force structuring the regeneration of degraded Caatinga dry
forests. Native pioneer tree species proved to be effective nurse plants by improving plant
community diversity, enhancing the establishment of endemic and endangered species, and
increasing performance of woody colonizers. However, the nurse target relationship changed from
40
facilitation to competition depending on nurse identity and target ontogeny. These results have
strong consequences on the way restoration should occur in degraded semi-arid lands.
41
Acknowledgments
We are grateful to Andrée Kimber, José Guedes, André, Uêdja, Felipe and Jarina for their help in
the field work. We thank CRAD-Univasf for logistic support.. This study was funded by Conselho
Nacional de Pesquisa e Tecnologia (CNPQ), which provided grants to G.B.C. Paterno and G.
Ganade (PQ/Produtividade). We thank Fonseca, C. R., Attayde, J.L., Costa, G., Fadigas, A.
Mazzochine G. and Rohr L. for important comments on early versions of this manuscript.
42
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47
Table 1. Morphological, physiological and ecological aspects of nurse, target and regenerating
plants. The deciduous category represents species that during the dry season lose all leaves (deci);
lose part of their leaves (semi); , or are not applicable due to lack of leaves (na). * Species that
replaced A. cearensis in the seedling experiment. ww Endangered species. Wide distribution (species
with occurrence not restricted to Caatinga); endemic (species with occurrence restricted to
Caatinga); regional (species that occurr in specific regions of Caatinga).
Famíly / Species
Max height Deciduos N² fixing Life form Succ. Estage
(m)
Occurrence / Conservation
Nurse Species
Euphorbiaceae
Cnidoscolus quercifolius Pohl
Fabaceae
Mimosa tenuiflora (Willd.) Poir.
Poincianella microphylla (Mart.
ex G.Don) L.P.Queiroz
Malvaceae
Pseudobombax simplicifolium A.
Robyns *
Burseraceae
Commiphora leptophloeos
(Mart.) J.B.Gillett
Tacinga inamoena (K.Schum.)
N.P.Taylor & Stuppy
Cactaceae
Melocactus zehntneri (Britton &
Rose) Luetzelb.
Euphorbiaceae
Jatropha mutabilis (Pohl) Baill.
12
8
7
deci
deci
0.5
0.4
3
shrub/tree
no
yes
no
tree
tree
tree
Regenerating Species
na
na
semi
yes
no
no
no
no
no
yes
cactus
shrub
tree
wide distribution ww
secundary
climax
regional occurrence
endemic
pioneer
pioneer
pioneer
wide distribution
pioneer
regional distribution ww
endemic
climax
shrub
climax
wide distribution
cactus
pioneer
tree
secundary
climax
shrub/tree
endemic
tree
wide distribution
pioneer
wide distribution
yes
semi
no
deci
3
deci
9
no
pioneer
shrub/tree
deci
Jatropha ribifolia (Pohl) Baill.
Fabaceae
Bauhinia cheilantha (Bong.)
Steud.
12
pioneer
Target Species
semi
shrub/tree
yes
deci
tree
30
yes
semi
no
8
semi
5
Anacardiaceae
Myracrodruon urundeuva
Allemão
semi
Poincianella pyramidalis (Tul.)
L.P.Queiroz
5
Apocynaceae
Aspidosperma pyrifolium Mart.
Fabaceae
Amburana cearensis (Allemão)
A.C.Sm.
Erythrina velutina Willd.
4
secundary
endemic
endemic ww
endemic
regional distribution
wide distribution
48
Table 2. Results of generalized mixed model (GMM) with Poisson distribution for richness and
abundance. For analysis of species richness, Abundance (ABU), nurse species (NSP) and nurse
effect (NEF) were included as fixed factors and NEF nested in NSP as a random factor. P-values
were obtained through Log-likelihood ratio test.
Richness Source
Complete Model
Abundance
df
-21.42
Nurse species (NS)
4
Nurse effect (NE)
3
NS x NE
2
df
Loglik
Complete Model
Nurse species (NSP)
-16.34
1
Abundance
Source
P
-18.33
10.160
3.990
< 0.001
0.407
-21.89
10.100
0.011
-18.21
3.740
0.153
-46.4
X2
Loglik
X2
P
4
-43.54
5.724
0.220
Nurse effect (NEF)
3
-54.175
21.266
< 0.001
NS x NE
2
-44.548
2.01
0.365
49
Table 3. Split-plot GMM with binomial family distribution for seed loss, seed germination and
seedling establishment of each nurse species. Nurse effect (NE) and target species (T) were used as
fixed factors in the model while T nested in NE was used as random factor. The significance of each
factor was tested with the Loglikelihood ratio test.
Seed loss
Germination
Establishment
C. quercifolius
Source
df
LogLik
5
-82.79
-86.43
Target species (T)
8
-404.83
NE x T
4
-85.63
Complete Model
Nurse effect (NE)
x²
P
LogLik
0.200
-70.97
-90.205
7.2
644.0
5.6
< 0,001
0.224
x²
295.8
11.3
-76.65
LogLik
< 0,001
-26.17
-43.93
38.4
-218.92
P
< 0,001
0.022
x²
-164.98
-26.89
P
35.5
< 0,001
277.6
1.4
< 0,001
0.836
M. Tenuiflora
Complete Model
Nurse effect (NE)
5
-85.08
-90.05
Target species (T)
8
-435.52
NE x T
4
-86.58
9.9
0.076
700.8
3.0
< 0,001
0.556
-65.33
-79.53
-167.96
-67.72
28.3
< 0,001
205.2
4.7
< 0,001
0.312
-27.73
-38.44
-142.63
-31.76
21.42
0.001
229.8
8.0
< 0,001
0.089
P. microphylla
Complete Model
Nurse effect (NE)
5
-52.55
-60.12
Target species (T)
8
-457.57
NE x T
4
-57.5
15.1
0.009
810.0
9.900
< 0,001
0.042
-71.6
-85.71
-211.97
-74.52
28.2
< 0,001
280
5.8
< 0,001
0.211
-42.69
-47.86
-193.94
-43.47
10.3
0.066
302.5
1.5
< 0,001
0.816
50
Table 4. Results of a Linear mixed model for RII index tested for each ontogenetic stage. Nurse
species (NS) and target species (T) were used as fixed factors in the model and T nested in NS as a
random factor. The significance of factor was tested with Loglikelihood ratio test.
Seed Germination
Source
Complete Model
df
LogLik
-55.39
x²
P
Nurse species (NS)
8
-61.81
12.6
0.248
Target speciess (T)
6
-64.58
10
-55.39
18.4
10.1
0.105
0.257
NS x T
Seedling Establishment
Complete Model
Nurse species (NS)
Target species (T)
NS x T
8
-47.21
-61.73
6
-66.85
10
-58.31
29.03
0.001
39.27
22.18
< 0,001
0.004
Juveniles survival
Complete Model
Nurse species (NS)
Target species (T)
NS x T
8
-26.13
-28.23
6
-30.32
10
-27.19
4.21
0.937
8.39
2.12
0.754
0.976
Juveniles Growth
Complete Model
Nurse species (NS)
Target species (T)
NS x T
8
-105.95
-115.06
6
-112.41
10
-111.51
18.22
0.051
12.9
11.1
0.375
0.195
51
Figure 1. Richness (a) and abundance (b) of regenerating woody species beneath nurse plants and
in open areas. Regenerating species composition (c), represented by the first two PCoA axes,
accounting for 56% of variation. Ellipses represent two statistically different groups by
PERMANOVA (F = 4.702, p = 0.002). In the legend micr, quer and tenu represent P. microphylla,
C. quercifolius and M. tenuiflora respectively. Error bars represent +/- 1 SE.
Figure 2. Maximum likelihood probability of seed loss (a,b,c), seed germination (e,f,g) and
seedling establishment (h,I,j) for each nurse and target species. In the figures axes, pyri, pyra, urun,
velu and cear represent A. pyrifolium, P. pyramidalis, M. urundeuva, E. velutina and A. cearensis
respectively. Error bars represent maximum loglikelihood 95% confidance interval.
Figure 3. Relative intensity index (RII) for each nurse-target combination along the following
ontogenetic stages: germination (a), establishment (b), survival (c) and growth (d). In the figure,
pyra, velu, pyri, urun, cear and simp represent P. pyramidalis, E. velutina, A. pyrifolium, M.
urundeuva, A. cearensis and P. simplicifolium. Errors bars represent +/- 1 SE. * This species was
used only in the seedling experiment in substitution of A. cearensis.
52
Figure 1.
53
Figure 2.
54
Figure 3.
55
Manuscrito a ser submetido ao periódico Journal of Vegetation Science
56
Nurse-nurse facilitation: water availability and nurse size shaping
the regeneration in Brazilian semiarid lands
Gustavo Brant de Carvalho Paterno1
Gislene Ganade1 (Author for correspondence - gganade@gmail.com)
1Universidade
Federal do Rio Grande do Norte (UFRN), Natal, Brasil.
57
Summary (350 words)
1. Question: Positive plant-plant interactions are known to be central process shaping
community diversity and structure in arid and semiarid environments. However, the net
balance between nurse and beneficiary species can vary depending on rainfall availability,
nurse size and beneficiary ontogeny. Indeed only few experimental studies have tested the
interactions among these factors. In this paper we seek to investigate how facilitation
between two pioneer nurse species change in intensity and importance along a gradient of
nurse size, water availability and beneficiary life stage.
2. Location: Reserva de Desenvolvimento Sustentável da Ponta do Tubarão, Macau town (5°
7.309'S; 36° 28.450'W), in degraded semiarid dry forest (Caatinga), northeast Brazil
3. Methods: In a 10 ha degraded area the two dominant wood species (M. tenuiflora and P.
pyramidalis), which are both pioneers nurse species, were select for the experiment. A
randomized split-plot experiment was established, with 45 replicates, where seeds of P.
pyramidalis (beneficiary) were sown in the presence and absence of M. tenuiflora (nurse)
with two levels of water along a gradient of nurse species size. Microclimatic conditions and
beneficiary performance were measured in all factorial combinations.
4. Main Results: We found that microclimatic alleviation increased linearly with nurse size,
but small nurses also provide better conditions then open sites. Nurse plant and water
enhanced beneficiary germination, establishment and survival in the field. Although we did
not found evidence of competition, facilitation intensity and importance varied depending of
complex interactions among water availability, size and beneficiary life stage.
5. Conclusions: Our results suggest that nurse-nurse facilitation might be a novel important
mechanism of plant community regeneration in semiarid areas. Additionally, inter-annual
variations in rainfall together with nurse plant availability are key processes governing
natural regeneration of degraded dry forests.
58
Key-words: secondary succession, positive interactions, precipitation, desertification, pioneer
species, germination, emergence, establishment, seedlings growth, competition
59
Introduction
In arid and semiarid ecosystems, suitable microsites beneath nurse plants crowns provide
unique opportunities for seedlings to successful colonize new sites (Franco & Nobel, 1989; ValientBanuet et al. 1991). Nurse plants can help beneficiary species to withstand the stressful conditions
found in open areas, such as high soil temperatures, intense solar radiation, poor soil fertility and
low water availability, which are strong barriers to plant regeneration (Callaway, 1995). Shade by
nurse plants canopy can buffer temperatures amplitudes and decrease beneficiary species water
demand through alleviation of evapotranspiration rates (Valiente-Banuet & Ezcurra, 1991).
Additionally nurse plants can also affect soil fertility and texture, by improving soil nutrients and
water content (Pugnaire et al. 1996; Walker et al. 2001; Barchuck, 2005). In this sense, nurse
facilitation is a central process that shapes plant community regeneration and increases community
diversity and ecosystem stability in dry environments (Pugnaire et al. 1996, but see Cavieres &
Badano, 2010 for a recent review).
Nurse species, however, can have distinct effects on soil water availability and can even
show negative effects on neighbours through root competition or intense shading (Walker et al.
2001, Reisman-Berman, 2007). The net balance between nurse-beneficiary interactions can depend
upon which resources the nurse plant affect, directly or indirectly, and what are the key resources
that limit beneficiary survival and growth (Holmgren et al. 1997). If nurse plants improves limiting
resources to beneficiary species, then its positive effects on neighbours will overcome negative
ones, whereas, if nurse plants decreases the availability of key resources to beneficiary species,
negative effects might overcome positive ones changing the net interactive balance to competition
(Holmgren et al. 1997).
Environmental stress is also an important factor influencing the net balance of plant
interactions. Early studies predicted that facilitation should increase in stressful or unproductive
ecosystems while competition would decrease (Stress Gradient Hypothesis - SGH) (Bertness &
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Callaway, 1994; Callaway & Walker, 1997). Although many studies corroborate this hypothesis
worldwide (Callway et al. 2002; Lortie & Callaway, 2006; Brooker et al. 2008), other studies
rejected these predictions and challenge SGH generality (Reginos et al. 2005; Maestre et al. 2006).
Recently, Maestre et al. 2009 proposed that different combinations of benefactor-beneficiary
species life stories and type of stress need to be considered in order to refine SGH predictions along
stress gradients. Holmgren & Scheffer (2010) also revisited the SGH and proposed that facilitation
would prevail in moderate not in high stress conditions, since competition can outcome positive
effects of nurse plants under extreme abiotic stress. Thus, studies undertaken in arid and semiarid
ecosystems (where water stress is usually the most limiting factor for plant colonization) can bring
important contributions to refine these predictions (Luzuriaga et al. 2012).
In dry ecosystems it is reasonable to expect that effects of nurse plants on beneficiary
species will vary with precipitation, since dry years impose greater water stress to seedlings
colonization when compared to humid years. For example, Kitzberger (2000) showed in northern
Patagonia that Austrocedrus seedlings depended on nurse facilitation only in years with average
precipitation, while in humid years seedlings could establish in the absence of nurse shelter.
However, during dry years, even though nurse plants partially ameliorated harsh conditions for
beneficiary species, high soil temperatures and limited water availability strongly inhibited plant
recruitment (Kitzberger, 2000). Similarly, in a Brazilian dry forest, a multiple-species experiment
showed that although nurse plants improved beneficiary species germination and establishment, all
recruits were dead by the end of the growing season due to scarce precipitation (Paterno et al. 2013
unpublished data). Pugnaire & Lazaro (2000) found that increases in richness beneath nurse plants
also depended on precipitation. Additionally, Barchuck et al. 2005 found that precipitation
distribution along the year (rainfall evenness) is also an important factor affecting the intensity of
facilitation by nurse plants in arid environments. Thus, a clear understanding on how water
availability and nurse plants facilitation interact to shape natural regeneration of semiarid plant
61
communities is still needed. Experimental approaches that involve water manipulation in the
presence and absence of nurse plants can provide clear insights on how precipitation variability
among years and positive interactions could modulate plant regeneration.
There is now good evidence that ontogenetic changes also affect the intensity and direction
of nurse-beneficiary interactions in semiarid environments (Miriti, 2006). Shifts from facilitation to
competition have been reported through changes in the spatial association between nurse and
beneficiaries along beneficiary species ontogeny (Valient-Banuetet al. 1991; Callaway & Walker,
1997). Miriti (2006) proposed that, in semiarid environments, the benefits from nurse proximity
should depend on beneficiary life stage. The author found that juveniles growing near adult nurses
are facilitated while adult individuals tend to compete with adult nurses. Callaway & Walker (1997)
proposed that facilitation strength also depends on benefactor size, where facilitation should
increase with nurse plant size or density. In agreement with this hypothesis, Pugnaire et al. (1996)
found that nurse plant facilitation increased with shrub age, with older nurses sheltering higher
species richness and different plant communities along its ontogenetic development. The authors
argue that resource accumulation is probably the main mechanism explaining this pattern.
Nevertheless, Reisman-Berman (2007) found a unimodal relationship between nurse size and
facilitation, where nurse positive effect was higher at median plant size. The author showed that
largest nurses could block 93% of radiation diminishing beneficiary densities, while median nurses
could favour higher recruitment (Reisman-Berman, 2007). However, most studies that tested the
effects of nurse plant ontogeny (age- or size-related) on nurse-beneficiary interactions used only
spatial association data, while field experimental evidence is still poorly represented in the literature
(Callaway & Walker, 1997, Reisman-Berman, 2007). Thus, there is a clear need to better
understand how nurse size (ontogeny) and water stress would affect beneficiary performance in
environments with high precipitation variability. Finally, the understanding of the key mechanisms
that govern nurse-beneficiary interaction can provide well-defined reference to ecological
62
restoration of semiarid degraded lands (Gomez-Aparício, 2009).
In this paper we seek to investigate the following questions: (i) How water availability and nurse
facilitation affect pioneer species regeneration in degraded semiarid lands? (ii) How nurse plant size
affects microclimatic conditions? and (iii) How nurse facilitation change in intensity and
importance along a gradient of nurse size, water availability and beneficiary life stage?
63
Methods
STUDY SITE
The study was carried out on a 10 ha site at the Reserva Estadual de Desenvolvimento Sustentável
da Ponta do Tubarão (protected area that allows resource use by local community), located near
Macau town (5° 7.309'S; 36° 28.450'W), northeast Brazil (Fig. 1). The study area is located at the
Piranhas river basin, has a mean annual rainfall of 470 mm with a rainy season from January to July
(INMET, 2012; Brazilian meteorological data base available at www.inmet.gov.br). The inter
annual variation in rainfall is extremely unpredictable through the rainy season, however, the dry
season is well defined and has six months of none or very low precipitation (Fig. 2, but see Fig. s1
in supplementary material for a detailed graph). The study site is an early successional degraded
Caatinga forest consisting of patches of pioneer trees, shrubs and bare soil. Herbaceous plants grow
only after rain events and rapidly produce seeds, which remain as a seed bank in the soil until the
next rainy season. Native vegetation of the study site was removed to plant Anacardium occidentale
crops (Caju nutz), however, this crop production did not succeed and the land was abandoned more
than a decade ago. The vegetation now is dominated by two nurse species (Mimosa tenuiflora
(Willd.) Poir. and Poincianella pyramidalis (Tul.) L.P.Queiroz) that established naturally in the area
forming vegetation patches surrounded by bare soil. The area is under great herbivory pressure by
goat and cows which are constantly feeding on herbaceous and woody species (personal
observation).
STUDY SPECIES
As study species we selected the two dominant tree species occurring in the area (M. Tenuiflora and
P. pyramidalis). For the experiment, we considered M. tenuiflora as nurse plant and P. Pyramidalis
as beneficiary. M. tenuiflora is a Fabacae pioneer species which has a wide geographic distribution,
ranging from northeast Brazil to dry valleys in Mexico (Queiroz, 2009). This species is adapted to
64
periodic drought and has great ability to establish in disturbed lands. Early experiments have shown
that M. Tenuiflora is an important nurse plant in Brazilian semiarid Caatinga, once it improved
germination, establishment and species richness of different regenerating species (Paterno et al.
2013, unpublished data). P. Pyramidalis is also a pioneer legume that, in Brazil, occurs in sympatry
with M. tenuiflora, but it is endemic from Caatinga dry forests (Queiroz, 2009). Likewise, there is
evidence that P. pyramidalis acts as a nurse plant, once it can improve species richness beneath its
canopy (unpublished data). Since this two pioneer species commonly occur along the large
extension of Caatinga dry forest, understanding the mechanisms that control their interaction would
certainly have important implication for management practices in Brazilian semiarid degraded
lands.
EXPERIMENTAL DESIGN
At the study site, all isolated M. tenuiflora trees (from now on nurse) found in the area were marked
and numbered. Only individuals taller than 1.5 m were used. We considered isolated individuals
those which did not overlap their canopy with others adult plants. From these individuals we
randomly selected 45 trees (replicates) within a gradient of shoot height, ranging from 1.5- 4.5
meters. To ensure a well-distributed size gradient, we randomly selected 15 individuals between
1.5-2.5 m (small), 15 individuals between 2.5-3.5 m (median) and 15 individuals larger than 3.5 m
(large). For each M. tenuiflora individual selected, the following morphological traits were
registered: maximum hight (m); maximum canopy diameter (m); minimum canopy diameter (m)
and trunk circumference at soil level (cm). Under each nurse individual, two 80 x 80 cm plots were
implemented, in the north-south direction, 20 cm far from the trunk center (“nurse treatment”) (Fig.
1). To establish the “no nurse treatments”, two paired plots of 80 x 80 cm were also implemented in
open sites at 2.5 m from the nurse canopy boundary. Open site plots were arranged randomly in one
of the four cardinal directions from nurse individual (north, east, south or west). Plots were
65
established using the same design used for “nurse treatments” (Fig. 1). Within each nurse effect
level (“nurse” and “no nurse”) one plot was randomly selected to receive artificial irrigation (“water
treatment”) while the other only received natural precipitation (“no water treatment”) (see Fig. 1 &
Fig. 2 for details). The experiment was structured in a randomized split-plot design with nurse as
split factor.
The irrigation treatments consisted of monthly manual irrigation. Two water tanks were installed in
the study site with 8000 L capacity. In each month, the water tanks were filed with drinkable water
that was transported with donkey wagons to the experimental blocks. With 10 L watering cans,
plots were manually irrigated once a day during five-seven days at each irrigation expedition.
Manually irrigation started in March and stopped at August. Plots without water received only
natural precipitation (summing 202 mm during the rainy season) while watered plots received
natural precipitation plus manual irrigation (summing 577 mm during the rainy season). In
summary, watered treatments received 2.8 times the amount of water compared with control plots
(Fig. 2). During the year of the experiment, rainfall reached only 42% of average precipitation, an
amount which stands bellow the 50% percentile of historical rainfall (260-650 mm). Therefore, it
was assumed that plots without irrigation represent dry years while irrigated plots represent years
with average precipitation (=~ 500 mm).
MICROCLIMATIC MEASURES
Under each nurse individuals, soil temperature was registered between 11:00 am and 13:00 pm
during five days, at the start of the dry season (August). In each plot, five measures were taken and
the mean value was used for analysis. Air temperature and humidity were also registered at the
same period, but only 31 and 33 blocks were sampled respectively. Air temperatures and air
humidity were registered at the height of 10 cm from the soil, close to the nurse central trunk in the
“nurse treatments” and at the centre of the experimental plots in the “no nurse treatments”. All
66
measurements of soil temperature, air temperature and air humidity were performed in sunny days
with less than 30% of cloud cover. Additionally, one spherical photograph was taken in each
experimental plot in order to access canopy openness. Photographs were taken at 45 cm above
ground at the center of each plot and facing north (Frazer et al. 1999). Canopy openness was
calculated with Gap Light Analyzer program (Frazer et al. 1999; freely available at http://
www.caryinstitute.org). To test if nurse plants affect microclimatic conditions beneath their canopy,
we run paired t-tests for each abiotic variable described above between “nurse” no “no nurse”
treatments. To understand how canopy size affected microclimatic conditions, we ran linear
regressions with each abiotic variable as response variable and canopy mean diameter as
explanatory variables.
FIELD EXPERIMENT
Seeds of P. pyramidalis (from now on beneficiary) were sown in the field in 45 experimental
blocks, each block containing a full factorial design, with all water and nurse treatment
combinations: (i) with nurse and with water; (ii) with nurse without water; (iii) without nurse and
with water and (iv) neither nurse nor water. In each experimental plot, 25 seeds were sown, 20 cm
apart from each other and marked with wooden sticks. A total of 4500 seeds were sown in February,
at the beginning of the rainy season, 1225 in each combination of water and nurse factors. Seeds
were donated by the Centro de Referência em Recuperação de Áreas Degradas (CRAD) and were
collected in Caatinga sites located in Pernanbuco state, northeast Brazil. During six months the
following measurements were registered monthly in all treatments: number of seeds germinated
(root emission), number of seedlings established (leaf emergence), number of seedlings that
survived through the first growing season, seedling shoot size, number of leafs and number of
leaflets of established seedlings.
To test if the presence of nurse plant and irrigation affected probabilities of seed germination,
67
seedling establishment and seedling survival we ran generalized linear mixed models (GLMM) with
binomial errors in a factorial split-plot design. Block and nurse nested within block were used as
random factors. The significance of each factor and interaction was tested with the log-likelihood
ratio test (LRT), through deviance contrast the between simpler and complete model (Crawley,
2007). To test if nurse plant and water affected beneficiary growth, we run linear mixed models
(LME) for each growth trait (shoot size, number of leafs and number of leaflets). In the model,
nurse and water were used as fixed factor while block and nurse nested within block were used as
random factors. The significance of each factor was also tested with the LRT between models. In all
models, residuals were verified for normality using graphical analysis (Crawley, 2007).
To access how water, nurse and target life stage affected the intensity, importance and
direction of nurse-beneficiary interaction, the relative intensity index (RII, see Armas et al. 2004)
and the relative neighbour importance (RNI, but see Kikvidize & Armas, 2010 for a recent review)
were calculated for each combination of factors. It was not possible to calculate the RII or RNI
indices for growth traits due to small sample size of seedlings that could survive to the end of the
experiment. RII was calculate through this formula:
where Bo is the performance of beneficiary species in the absence of nurse plants and Bw is the
performance of beneficiary species in the presence of nurse plants. RNI index was calculated with
the following formula:
where Bmax is the maximum beneficiary performance in the presence or absence of nurse. While the
RII represents the relative effect of the nurse plant in the beneficiary species without considering
the environment impact on plant performance, RNI index accesses the effect of biotic interaction
relative to the weighted effect of environment on beneficiary performance (Kikvidize & Armas,
68
2010). Both indices have strong statistical power and are symmetrical around zero, varying from -1
(maximum competition) to +1 (maximum facilitation) (Armas et al. 2004; Kikvidiz & Armas,
2010).
To test if nurse size, water and target life stage affected the intensity and importance of
nurse-target interaction we ran LME. Nurse size was grouped into the same three categories of
shoot size used for the stratified sampling of nurse individuals: (a) 1.5-2.5 m (small); (b) 2.5-3.5 m
(median) and (c) > 3.5 m (large). In the model, nurse size, water and life stage were used as fixed
factors while stage nested in water, nested in size, nested in block were used as a random factor. We
used model selection to define the best model through AIC comparisons for each interaction index
(RII and RNI). All statistical analysis was performed with R 2.15.0 (R Development Core Team,
2012), GLMM models were fitted with the “lme4” package (Bates et al. 2011) and LME were fitted
using “nlme” package (Pinheiro et al. 2012).
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Results
EARLY ESTABLISHMENT
Nurse plant and water irrigation improved seed germination probability of P. pyramidalis.
Highest germination rates were found in treatments with water and nurse while the lowest
germination rates occurred in treatments without water and without nurse (Fig. 3a). There was no
interaction between factors, but nurse plant greatly improved germination probabilities when
compared with the water treatment (Fig. 3a; Table 1). For seedling establishment, however, there
was an interaction between water and nurse, where seedlings beneath nurse plants did not depend
on water to improve their establishment probabilities while seedlings in open sites strongly
depended on water to establish (Fig. 3b). At the end of the experiment few seedlings were able to
survive and only seedlings beneath nurse plants or in treatments with water successful established
in the field (Fig. 3c). For survival probability, water was the only significant factor, although
survival probability beneath nurse also showed a positive tendency (Fig. 3c; Table 1). However,
nurse effect may be not clearly expressed by the data due to the low number of seedlings that
survived at the end of the experiment.
SEEDLINGS GROWTH
In general, water and nurse tended to improve seedlings growth. Seedling height results
were similar to germination results once nurse and water treatments improved seedlings size (Fig.
3d). However, in this case, both factors improved height in a very similar way with no significant
interaction among factors (Table 1). Similar to germination, seedling growth was maximum in
treatments with nurse and water. When considering the number of leafs, only water improved
seedling performance, although there was a marginal interaction between water and nurse (p =
0.064), where seedlings with water and beneath nurse tended to produce more leafs (Fig. 3e). For
number of leaflets there was a significant interaction between water and nurse, where water effect
70
was stronger beneath nurse plant and did not improve number of leaflets in open sites (Table 1, Fig.
3f). Although there was a tendency to seedlings in plots without water and nurse to produce more
leaflets this effect was not significant.
MICROCLIMATIC AMELIORATION AND CANOPY SIZE
In general, M. tenuiflora nurse greatly improved microclimatic conditions beneath its
canopy, with milder temperatures, lower solar radiation (canopy openness) and higher air humidity
(for statistical detail see Table s1 in supplementary material). Soil temperature was significantly
lower under nurse shelter with a mean difference of - 6.5 ºC (t89 = -17.63; p < 0.001; Fig. 4a).
Canopy openness was 20% lower beneath nurses when compared with open sites (t89 = -18.32; p <
0.001; Fig. 4b). In the same way, air temperature was in average 2 ºC lower beneath nurse (t65 =
-5.12; p < 0.001; Fig. 4c). Finally, air humidity was in average 2.5% higher beneath nurse plant (t65
= 3.92; p < 0.001; Fig. 4d).
Nurse plants positive effects on microclimatic conditions generally increased with size.
When considering soil temperature buffer (temperature beneath nurse minus temperature in open
sites) we found a linear decreased on temperature with increasing canopy size (F1,43 = 68.70; p <
0.001; R2 = 0.61; Fig. 4d). Temperature difference between nurse and no nurse treatments ranged
from 2 ºC under small nurse plants to 13 ºC underneath larger nurse plants. Canopy openness
followed a similar trend, with a strong decline in canopy openness difference, between nurse and no
nurse treatments, with increasing canopy size (F1,43 = 46.291; p < 0.001; R2 = 0.50; Fig. 4e).
Canopy openness difference between nurse and no nurse treatments varied from 1-40 % in small
and larger nurse plants respectively. Though, for air temperature and air humidity, plant size was not
an important factor explaining microclimatic variation. We found that mean effect of nurse plant on
air humidity and temperature remained constant along nurse plant size. (Fig. 4fg; Table 2).
71
FACILITATION INTENSITY AND IMPORTANCE
In general, the presence of the nurse plant improved all beneficiary plant performance at all
life stages considered. We did not find any evidence of an interaction shift to competition in this
experiment. Indeed interaction intensity and importance indices remained above zero for all
combination of nurse size, water availability and beneficiary life stage (Fig. 5). However, the
intensity of nurse plant facilitation varied depending on the interaction between life stage and water
(Table 3). In general, facilitation intensity for seedling establishment was higher than for
germination and survival, while water only improved facilitation intensity at the survival phase
(Fig. 5abc). The importance of facilitation was also positive for all life stages, but in a slightly
different way (Fig. 5cde). For the importance index there was a marginal interaction between size
and stage and a significant interaction between water and stage (Table 3). In the first case, smaller
plants showed lower facilitation importance, indicating that small nurse plants may not be able to
greatly improve germination and survival of beneficiary (Fig. 5ce). For seedlings establishment,
however, nurse plant size did not affected importance of facilitation, where all plant sizes showed
similar importance index (Fig. 5d). In the second case, facilitation importance was greater for
germination and establishment phase, but minor for survival phase. This was probably due to a
sample size effect, since only few seedlings could survive until the end of the experiment. Similar
to facilitation intensity results, water improved the importance of facilitation only for the survival
phase. Although intensity and importance of facilitation are not necessarily correlated, we found
strong association between these two indices, reinforcing similar patterns found for both indices
(see Fig s2 in supplementary material).
72
Discussion
EARLY ESTABLISHMENT MECHANISMS AND NATURAL REGENERATION
Our results show clear evidence that plant regeneration in Brazilian semiarid Caatinga are
highly dependent on the presence of nurse plants even in years with median precipitation. In dry
years, however, plant community regeneration might be very slow, especially in areas where nurse
plants occur at low densities. These findings corroborate the hypothesis that drought is a strong
barrier for the recovery of degraded semiarid systems specially when considering a dryer global
change scenarios (Holmgren & Scheffer, 2001; Matías et al. 2012). In this sense, facilitation by
nurse plants can play a central role in preventing desertification expansion or catalysing natural
vegetation recovering during milder years (Matías et al. 2012).
We found that nurse plants and water had additive effects on beneficiary germination
probability. However, nurse effects were greater than water effects, suggesting that microclimatic
amelioration by nurses are), at least partially compensating beneficiary water stress (Holmgren et
al. 1997). This probably occurred due to alleviation of beneficiary water demand as nurse plants
lowered soil temperatures and solar radiation, diminishing seedlings evapotranspiration rates
(Valient-Banuet et al. 1991). Additionally, M. tenuiflora could also have positive effects on soil
water content (Pugnaire et al. 1996; Walker et al. 2001). Nonetheless, it is clear that beneficiary
seeds were still limited by water, even beneath nurse shelter, once water irrigation improved
germination probabilities in treatments with and without nurses. Seedling establishment was also
more depended on nurse facilitation then on water. This pattern suggests that pioneer establishment
in dry years may strongly depend on other nurse plants to succeed. As both species studied (M.
tenuiflora and P. pyramidalis) are pioneer trees and nurse species in Caatinga dry forests, our
findings highlight that nurse-nurse facilitation can be a novel important mechanism of plant
community regeneration, where even pioneer nurse species can be limited by water stress in the
absence of other nurse shrubs.
73
Considering these results, differential precipitation among years will certainly have strong
implications on Caatinga regeneration dynamics. Many studies have shown that variation in
precipitation among years can alter nurse plant effects on beneficiary species and shape plant
interactions dynamics (Tilborger & Kadmon, 2000; Barchuck et al. 2005; Reginos et al. 2005).
Tielborger & Kadmon (2000) showed that facilitation effect by nurse plants varied with
precipitation depending on which species was considered. Barchuck et al. (2005) found that
survival of beneficiary species increased with precipitation and that seasonal variability on
precipitation might be an overlooked process shaping plant interactions. We forecast that
unpredictable variation of rain among years and irregular availability of nurse plants at the
landscape can promote complex spatial-temporal dynamics in the regeneration of degraded semiarid
vegetation. Therefore, nurse plants density may play a central role favouring secondary succession.
SEEDLING EARLY GROWTH
When considering seedling growth we found that both water and nurse plants also increased
shoot height, number of leaves and number leaflets, although with very small sizes effects. This
result contrasts with our previous experimental evidence, where M. tenuiflora trees diminished
juveniles growth of two beneficiary species (Paterno et al. 2013, unpublished data). Nevertheless,
these experiments were performed with juveniles up to six-months old, which have greater water
needs and thus, may compete with nurse plants for shared resources. The positive effect of nurse
plants on early seedling growth can probably be related to the stress release experienced by
beneficiaries, which allows seedlings to invest more biomass on shoots and leaves. Although small
effects on leaf production can have positive impacts on later seedling growth, shifts from
facilitation to competition along ontogeny may occur as beneficiary species become adults (ValientBanuat et al. 1991; Miriti, 2006). From our results it is not reasonable to extrapolate early growth of
very young seedling to juveniles or adult growth. But we can expect that facilitation may only hold
74
into adult age if environmental alleviation surplus negative competition for water and light
(Holmgren et al. 1997). In order to address this issue long-term experimental studies, involving
nurse-beneficiary interactions, need to be developed between years with contrasting precipitation
and ontogenetic phases (Brooker et al. 2008).
NURSE PLANT SIZE AND MICROCLIMATIC ALLEVIATION
Early studies have shown that nurse plants can increase water availability, improve soil
nutrient contents, block radiation and diminish temperature amplitudes (Valiente-Banuet et al. 1991;
Domingo et al. 1999), however, different nurse species can also have antagonistic effects (Walker et
al 2001). We found that the M. tenuiflora greatly improved all microclimatic conditions considered,
diminishing soil and air temperature, blocking solar radiation and enhancing relative air humidity.
Although positive effects of nurse plants on microclimatic conditions are very well documented in
literature (Callway et al. 1995), the relationship between nurse size and these positive effects on
abiotic conditions remains poorly understood (Pugnaire et al. 1996; Reisman-Berman, 2007; Haugo
et al. 2010; Yu et al. 2010). We found clear evidence of size-related alleviation of microclimatic
conditions by nurse plants, where larger nurses provided better conditions for beneficiary species
when compared with young and smaller nurses. However, air temperatures and humidity did not
change with nurse size, suggesting that even small nurse plants can provide suitable microhabitats
for juvenile recruitment. Pugnaire et al. (1996) found that effects of nurse plants on soil fertility and
water soil content greatly increased with nurse age (which was related with size). The authors also
showed that species richness recruiting underneath nurse shelter followed the same pattern,
suggesting that nurse facilitation could be an important mechanism maintaining regional
biodiversity and ecosystem stability. However, Resiman-Berman (2007) found that as leaf number
increased with nurse plant age, positive effects of nurse plants should be higher at intermediate
ages. The author argue that strong shade imposed by older nurses can have negative effects on
75
beneficiary species once light become a limiting resource for seedlings. Nonetheless, in our survey
even the largest M. tenuiflora nurse could block only a smal part of the solar radiation so we would
not expect this species to have negative effects on beneficiary through shade effects. However, in
order to fully understand the relative importance of nurse size on microclimatic alleviation and light
availability it would be necessary to considerer how species traits change along ontogeny.
INTENSITY AND IMPORTANCE OF FACILITATION
To understand how plant-plant interactions are shaped, ecologists have developed many
indices that allow to integrated measures of neighbour net effects on plant performance (Kikvidize
& Armas, 2010). Although RII and RNI indices were positively correlated we shall highlight
important difference in their meaning. As RNI values were always lower than RII, we found
evidence that environmental stress is still a strong factor affecting plant performance, even beneath
nurse shelter. The RNI index is a measure that considers the relative effect of nurse weighed by
other environmental factors (Kikvidize & Armas, 2010). Thus, even through the overall effect of
nurse plant on interaction intensity was positive, it did not fully compensate for the beneficiary
species water stress, suggesting that average precipitation years still impose great difficulties for
plant community regeneration. This result agrees with our previous findings related to the low early
establishment probabilities of beneficiaries species.
Our results challenge traditional SGH predictions where facilitation should increase with
abiotic stress (Bertness & Callaway, 1994; Callaway & Walker, 1997). We found clear evidence that
water irrigation (less stressful condition) enhanced facilitation intensity and importance. However,
our results agree with a recent review of the SGH, in which Holmgren & Scheffer (2010) argue that
facilitation should be more relevant in intermediary levels of stress when compared with the
extreme end of the stress gradient. Under extreme stressful conditions nurse and beneficiary species
can compete for key resources overcoming nurse positive effects or be inefficient in fully
76
alleviating abiotic conditions for beneficiary species to succeed (Holmgren & Scheffer, 2010). In
our experiment, we did not find any evidence of competition and both nurse and beneficiary species
are pioneer trees and therefore tolerate stress. This suggests that the second mechanism may be the
main reason why in intermediate levels of stress (water treatments) facilitation was more evident.
This data also highlight that our experimental design encompasses higher and intermediary levels of
stress since no water plots represented atypical dry years in the system (highly stressful condition)
while watered plots represented years with median precipitation (intermediary stress). Our findings
also agree with Maestre et al. 2009 predictions of SGH, where facilitation should prevail on
intermediated stress, when stress is promoted by a resource (like water) and both nurse and
beneficiary species are stress-tolerant. Nonetheless, facilitation importance and intensity also
depended on beneficiary life stage. For germination and establishment water and size were not so
relevant when compared with survival. These results show that facilitation importance can be
modulated by complex interactions between nurse plant size, water stress and beneficiary species
life stage.
Other prediction from SGH is that facilitation should increase with nurse size or density
(Callaway & Walker, 1997). Our results corroborate this hypothesis since facilitation importance
was greater for larger nurses, although this pattern was not consistent for facilitation intensity.
Pugnaire et al. (1996) also found an increasing positive effect of nurse plants with increasing size
and age. However, Reisman-Berman (2007) found that larger nurses could negatively affect
beneficiary performance through shading, the species considered by the author forms extremely
dense foliage while M. tenuiflora have sparse small leaves.
Experiments that tests how species with different root and canopy systems influence nursebeneficiary interaction along nurse and beneficiary age gradients will greatly improve our
understanding of how ontogeny influence the balance between facilitation and competition in dry
systems.
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Conclusion
Understanding which are the main mechanisms that govern natural regeneration in degraded
semiarid lands can provide critical insights for better management practices (Gomez-Aparício,
2009). Our results highlight that inter-annual variation in rainfall, together with nurse plant
availability can be the main mechanisms governing natural regeneration of Caatinga dry forests. We
found strong evidence that degraded semiarid lands may be resistant to regeneration in atypical dry
years. However, nurse-nurse facilitation might be an important mechanism improving ecosystem
resilience and its ability to recover from a degraded state. To fully address the relationship between
stress and plant-plant interactions in dry lands it is essential that new studies focus on how nursebeneficiary ontogeny and rainfall variability affect the net balance between nurse and beneficiary
species.
Acknowledgments
We are especially grateful to Guilherme, Adriana, Rosa, Natalia, Felipe, Rodrigo, Vandir, João,
Lucas and Laura for their help in the field and the exchange of ideas. We thank Centro de
Referência de Recuperação de Áreas Degradadas (CRAD-Univasf) for technical support for
theexperiment. We also thank G. Mazzochine for statistical support and M. Fagundes for help in
data analysis. This study was funded by Conselho Nacional de Pesquisa e Tecnologia (CNPQ),
which also provided G.B.C. Paterno with a master scholarship and G. Ganade with a Pq Grant. We
thank A. F. de Souza e G. C. Costa for important comments on early version of this manuscript.
78
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82
Table 1. Results of generalized linear mixed model (GLMM) with binomial distribution for
germination, establishment and survival. Nurse effect and water were used as fixed factors in the
model while block and nurse nested in block were used as random factors. On lower table, results of
linear mixed model (LME) for seedling height, number of leafs and number of leaflets. In the
model, nurse and water were used as fixed factor while block and nurse nested in block were used
as random factors. P-values were obtained through Loglikelihood ratio test.
Early establishment
Germination
Source
df
LogLik
x²
P
Complete Model
6
-209.65 Nurse (N)
4
-176.91
65.481
< 0.001
Water (W)
4
-198.78
43.748
< 0.001
NxW
1
-178.45
3.087
0.078
Establishment LogLik
x²
-131.14 P
-160.07
57.85
< 0.001
-133.66
5.04
0.080
-133.44
4.59
0.032
LogLik
-51.24 -51.96
-58.25
-51.94
Survival
x²
P
1.44
0.488
14.02
< 0.001
1.39
0.239
Early Growth
LogLik
0.017
-36.54
3.73
0.155
121.73
10.30
0.006
15.17
< 0.001
-42.33
15.32
0.001
126.48
19.80
< 0.001
0.01
0.931
-36.39
3.43
0.064
121.50
9.85
0.002
high
df
LogLik
Complete Model
7
-94.80
Nurse (N)
5
-98.85
8.11
Water (W)
5
-102.38
NxW
6
-94.80
L.Ratio
P
nº leafs
-34.67
L.Ratio
P
nº leaflet LogLik
L.Ratio
116.58 P
83
Table 2. Results of linear regressions for soil temperature, canopy openness, air temperature and air
humidity. In the model abiotic variable were used as response variable and canopy size as
explanatory variable.
soil temperature
Source
df
SSQ
MSQ
F
P
canopy size
1
284.36
284.362
68.706
< 0.001
43
177.97
4.139
residuals
canopy openness
Source
df
SSQ
MSQ
F
P
canopy size
1
1874.7
1874.7
46.291
< 0.001
29
1741.4
40.5
residuals
air temperature
Source
df
SSQ
MSQ
F
P
canopy size
1
0.341
0.341
0.156
0.6957
29
63.388
2.1858
residuals
air humidity
Source
df
SSQ
MSQ
F
P
canopy size
1
11.54
11.535
0.4006
0.5314
31
892.65
28.795
residuals
84
Table 3. Results of LME model selection fir RII and RNI interaction index. In the model, nurse
size, water and ontogenetic stage were used as fixed factors while stage nested in water nested in
block were used as random factors. Complete model was selected through best AIC values. Pvalues were obtained through log-likelihood ratio test.
Source
complete model
water (w)
size (s)
stage (sta)
RII df
AIC
LogLik
12
297.85
-136.93
L. ratio
P
9
302.40
-142.20
10.55
0.014
10
298.16
-139.08
4.31
0.116
8
373.86
-178.93
84.00
< 0.001
w x sta
10
304.35
-142.18
10.50
0.005
Source
complete model
df
AIC
LogLik
16
-14.27
23.13
water (w)
13
-13.15
19.58
7.12
0.068
size (s)
10
-14.52
17.26
11.75
0.068
8
57.52
-20.76
87.79
< 0.001
14
12
-11.33
-13.02
19.67
18.51
6.94
9.25
0.031
0.055
RNI
stage (sta)
w x sta
s x sta
L. ratio
P
85
Table s1. Results of paired t-test between nurse and no nurse treatments for soil temperature, air
temperature and air humidity
soil temperature
mean diff.
df
t
P
-6.49
89
-17.64
< 0.001
air temperature
mean diff.
df
t
-1.86
mean diff.
2.55
65
-5.12
air h midity
df
t
65
3.92
P
< 0.001
P
< 0.001
86
Figure 1. Experimental design and study area. Different circles represent M. tenuiflora nurse
individuals with different sizes ranging from 1.5 to 4.5 m in height. Blocks represent paired plots
within each nurse plant and contains all treatments levels.
87
Figure 2. Historical precipitation since 1961 and amount of water applied to irrigated and control
plots during the experiment. The “no water” treatment received only natural precipitation (light gray
bars) while watered treatments received natural precipitation plus manually applied water (dark
gray bars). Error bars represent +/- 1 standart deviation.
88
Figure 3. Maximum likelihood probability estimate of seed germination (a), seedling establishment
(b), seedling survival (c) and shoot height (d), number of leafs (e) and number of leaflets (f) for
each combination of water and nurse factors. Errors bars for a,b and c represent 95% of likelihood
confidence limits. For d,e and f erros bars represent +/- 1 standar errors.
89
Figure 4. Paired t-test between nurse and no nurse treatments for: (a) soil temperature; (b) canopy
openness; (c) air temperature; (d) and air humidity. Error bars represent +/- 1 standard error. Linear
regression between canopy size and: (d) soil temperature; (e) canopy openness; air temperature (f)
and (g) air humidity. Buffer values represent difference between nurse and no nurse treatments.
90
Figure 5. Relative intensity index (RII) and importance index (Imp) for each combination of the
following factors: water, size and ontogenetic stage. Germination stage (a, d), establishment (b,e)
and survival (c,e). Error bars represent +/- 1 standard error.
91
Figure s1. Rainfall precipitation between 1961 and 2012. Each cell represents the sum of
precipitation in one month. Darker colours represent wet months while light colours represent dry
months. Data from INMET (2012) online database.
92
Figure s2. Linear regression between RII and Imp interaction index.
93
ANEXO 1
94
ANEXO 2
95

universidade federal do rio grande do norte centro de

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