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Competição Por Mutualismos: Hierarquia De Dominância Interespecífica Mediada Pela Qualidade Do Recurso Regulando Interações Formiga-Planta

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Competição Por Mutualismos: Hierarquia De Dominância Interespecífica Mediada Pela Qualidade Do Recurso Regulando Interações Formiga-Planta UNIVERSIDADE FEDERAL DE UBERLÂNDIA INSTITUTO DE BIOLOGIA PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E CONSERVAÇÃO DE RECURSOS NATURAIS TESE DE DOUTORADO COMPETIÇÃO POR MUTUALISMOS: HIERARQUIA DE DOMINÂNCIA INTERESPECÍFICA MEDIADA PELA QUALIDADE DO RECURSO REGULANDO INTERAÇÕES FORMIGA-PLANTA ROBERTH FAGUNDES DE SOUZA 2015 i ii ROBERTH FAGUNDES DE SOUZA COMPETIÇÃO POR MUTUALISMOS: HIERARQUIA DE DOMINÂNCIA INTERESPECÍFICA MEDIADA PELA QUALIDADE DO RECURSO REGULANDO INTERAÇÕES FORMIGA-PLANTA Tese apresentada à Universidade Federal de Uberlândia, como parte das exigências para obtenção do título de Doutor em Ecologia e Conservação de Recursos Naturais Orientador: Prof. Kleber Del Claro Uberlândia, MG Fevereiro de 2015 iii COMPETIÇÃO POR MUTUALISMOS:HIERARQUIA DE DOMINÂNCIA INTERESPECÍFICA MEDIADA PELA QUALIDADE DO RECURSO REGULANDO INTERAÇÕES FORMIGA-PLANTA Doutorando: Roberth Fagundes de Souza Tese apresentada à Universidade Federal de Uberlândia, como parte das exigências para obtenção do título de Doutor em Ecologia e Conservação de Recursos Naturais Banca examinadora: Prof. Dr. Kleber Del Claro (Titular/Orientador) Prof. Dr. Gilberto Marcos de Mendonça Santos (Titular) Profa. Dra. Juliane Floriano Lopes (Titular) Prof. Dra. Solange Cristina Augusto (Titular) Prof. Dra. Helena Maura Torezan Silingardi (Titular) Prof. Dr. Everton Tizo Pedroso (Suplente) Prof. Dr. Denise Lange (Suplente) Uberlândia, MG Fevereiro de 2015 iv Agradecimentos Agradeço ao Prof. Kleber Del Claro, orientador e amigo, pelo aprendizado tão atenciosamente provido e pela dedicação paternal à minha orientação. Prof. Kleber é uma grande referência para mim de profissionalismo, humildade e humanidade. Agradeço ao Prof. Sérvio Pontes Ribeiro pelo constante aprendizado e pelo suporte intelectual e logístico durante o difícil, mas prazeroso, trabalho de se estudar Campos Rupestres. Agradeço aos amigos e colaboradores que contribuíram para o desenvolvimento desse estudo. Em especial, agradeço a Wesley Dáttilo e Denise Lange pelos conselhos, discussões e críticas fundamentais para a confecção desse estudo. Um agradecimento especial também ao Prof. Victor Rico Gray pelas orientações paralelas. Agradeço aos membros da banca examinadora, Prof. Gilberto M.M. Santos, Prof. Juliane F. Lopes, Profa. Solange C. Augusto, Prof. Helena M. T. Silingardi, Prof. Everton T. Pedroso e Profa. Denise Lange pela disposição em corrigir e avaliar minha tese. E por todos os avaliadores que o fizeram informalmente durante a escrita. Agradeço as agências CAPES pela bolsa de estudo, a FAPEMIG pelo apoio financeiro, a UFU e UFOP pelo apoio logístico e financeiro, ao IBAMA e IEF pelas licenças de coleta e apoio logístico. Agradeço a minha mãe Maria do Carmo Fagundes, pai Giovani Serrato e minha irmã Nayara Fagundes, assim como minha noiva Marcelle Braga pelo incentivo indispensável. Além disso, agradeço meus irmãos William Sabino e Caryne Braga pelas conversas e discussões que me levaram a prosseguir nessa carreira. Obrigado a todos que de alguma forma contribuíram para meu desenvolvimento profissional e me tornaram capazes de concorrer ao título de Doutor em Ecologia. “True glory consists in doing what deserves to be written, in writing what deserves to be read, and in so living as to make the word happier and better for our living in it”. Pliny the Elder v TESE DE DOUTORADO COMPETIÇÃO POR MUTUALISMOS: HIERARQUIA DE DOMINÂNCIA INTERESPECÍFICA MEDIADA PELA QUALIDADE DO RECURSO REGULANDO INTERAÇÕES FORMIGA-PLANTA ROBERTH FAGUNDES, KLEBER DEL-CLARO vi DOCTORAL THESIS COMPETITION FOR MUTUALISMS: INTERSPECIFIC DOMINANCE HIERARCHY MEDIATED BY RESOURCE QUALITY REGULATING ANT-PLANT INTERACTIONS ROBERTH FAGUNDES, KLEBER DEL-CLARO vii Resumo As formigas que recolhem o néctar das plantas com nectários extraflorais (EFN) podem defendê-las contra ataques de herbívoros. Muitos casos desse tipo de mutualismo foram descritos mas ainda é preciso entender os mecanismos que estruturam essas interações. Neste estudo, esse problema foi abordado através de observações de campo e experimentos sobre o comportamento das formigas compilados em cinco capítulos. Especificamente, foi avaliado o investimento da planta em atrair formigas (qualidade do néctar) e a relação competitiva entre formigas pelo néctar (hierarquias de dominância) como mecanismos estruturadores das interações formiga-planta (partição das interações). Todo o estudo ocorreu em áreas do ecossistema Campo Rupestre, localizadas em Ouro Preto (Brasil), de junho de 2011 a março de 2014. No Capítulo 1, observamos que redes de interação formiga-planta em Campo rupestre é aninhada e generalizada como esperado para mutualismos, mas difere da rede formiga- hemíptero, seu equivalente ecológico, apesar de compartilharem as mesmas espécies de formigas interagentes. No Capítulo 2, nós aprofundamos no efeito dos recursos estruturando interações, e mostramos que a qualidade mais do que a quantidade de néctar determina o padrão de interação entre formigas (32 espécies) e plantas (10 espécies), bem como os benefícios desta interação (benefícios condicionais). No Capítulo 3, nós demonstramos através de encontros interespecíficos pareados que as formigas são organizadas em hierarquias de dominância comportamental baseadas em agressividade. Essa hierarquia afeta a dominância numérica por territorialidade e, mais importante, o domínio das interações e do néctar. Mantendo esta linha de pensamento, demonstramos no Capítulo 4 que nem todas as formigas que coletam néctar realmente protegem a planta contra herbívoros mas somente as espécies dominantes e altamente interagidas. Finalmente, fechamos a tese demonstrando no Capítulo 5 que as espécies de formiga que interagem com as plantas durante o dia não são o mesmo à noite, mas esta rotatividade diurno-noturno não afeta a estrutura das interações devido a troca específica da formiga dominante. Este estudo traz evidências comportamentais e empíricas sobre a importância da identidade de espécies de formiga e sua dominância ecológica, assim como da qualidade do recurso, para a estrutura de rede da formiga-planta e eficácia do mutualismo. Palavras chave: mutualismo, rede mutualista, rede formiga-planta, herbivoria, dominância ecológica, partição de recurso, competição interespecífica, ciclos diurnos, Cerrado. viii Abstract Ants that collect nectar from plants bearing extrafloral nectaries (EFN) can defend them against the attacks of herbivores. Many cases of this food-for-protection mutualism have been described and the next step is to understand the mechanisms that structure these interactions. In this study, this issue was addressed through field observations and experiments on ant behaviour in studies compiled into five chapters. Specifically, we evaluated the plant's investment in attracting ants (nectar quality) and the competitive relationship between ants (resource dominance hierarchies) as structuring mechanisms of ant-plant interactions. The entire study took place in areas of the ecosystem known as Rupestrian Fields, located in Ouro Preto (Brazil), between June 2011 and March 2014. In Chapter 1, we observe that ant-plant interaction network in Rupestrian Fields is nested and generalized as expected for mutualisms, but differs from ant- hemipteran network, its ecological equivalent, despite both share ant species interactions. In Chapter 2, we delve into the study of the effect of resources in interaction frequency, and we showed that the quality more than quantity of nectar determines the pattern of interaction between plants (10 species) and ants (32 species), as well as the benefits of this interaction (conditional outcomes). In the Chapter 3, we focus on the ants to demonstrate, using paired encounters, that ants species are organized in dominance hierarchies based on aggressiveness. This hierarchies affects the numerical dominance based on territoriality and, more importantly, in the dominance of interactions and nectar. Keeping this line of thought, we demonstrated in Chapter 4 that not all ants that collect nectar really protect the plant against herbivores but only the ecological dominant and highly interacted species. Finally, we close the thesis demonstrating in Chapter 5 that the ant species interacted with plants during the day are not the same at night, but this diurnal-nocturnal turnover does not affect the structure of the interactions by only changing the dominant species. This study brings behavioural and empirical evidences on the importance of the identity of the ant species and its ecological dominance, as well the effect of the nectar quality, for the structure of ant-plant interactions and effectiveness of mutualisms. Key words: mutualism, mutualistic network, ant-plant network, herbivory, resource partitioning, ecological dominance, interspecific competition, co-occurrence, daily turnover, Cerrado. ix Lista de Figuras / List of Figures Introdução Geral Figura 1. Mapa do Parque Estadual do Itacolomi (PEIT), localizado entre Ouro Preto e Mariana (MG, Brasil). Mapas na lateral esquerda localizam o PEIT em diferentes escalas geográficas. Pontos 1, 2, 3 e 10 representam as áreas de estudo contempladas nessa tese de doutorado. (Fonte: IBGE)............................................................................................................................14 Figura 2. Panorâmica da Floresta Estacional Semidecidual (Inferior) e dos Campos Rupestres (Superior). Imagem capturada na região da Fazenda do Manso, interior do Parque Estadual do Itacolomi, entre Ouro Preto e Mariana (MG, Brasil). (Foto: Fagundes
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