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The Mating Communication of Stingless Bees (Hymenoptera: Apidae, Meliponini)

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The Mating Communication of Stingless Bees (Hymenoptera: Apidae, Meliponini) UNIVERSIDADE DE SÃO PAULO FFCLRP – DEPARTAMENTO DE BIOLOGIA PROGRAMA DE PÓS-GRADUAÇÃO EM ENTOMOLOGIA The mating communication of stingless bees (Hymenoptera: Apidae, Meliponini) A comunicação do processo reprodutivo em abelhas sem ferrão (Hymenoptera: Apidae, Meliponini) Lucas Garcia von Zuben Tese apresentada à Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto da USP, como parte das exigências para a obtenção do título de Doutor em Ciências. Área: ENTOMOLOGIA RIBEIRÃO PRETO-SP 2017 LUCAS GARCIA VON ZUBEN The mating communication of stingless bees (Hymenoptera: Apidae, Meliponini) A comunicação do processo reprodutivo em abelhas sem ferrão (Hymenoptera: Apidae, Meliponini) Tese apresentada à Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto da Universidade de São Paulo, como parte das exigências para a obtenção do título de Doutor em Ciências. Área: Entomologia Orientador: Prof. Dr. Fábio Santos do Nascimento RIBEIRÃO PRETO 2017 Autorizo a reprodução e divulgação total ou parcial deste trabalho, por qualquer meio convencional ou eletrônico, para fins de estudo e pesquisa, desde que citada a fonte. Von Zuben, Lucas Garcia The mating communication of stingless bees (Hymenoptera: Apidae, Meliponini) / A comunicação do processo reprodutivo em abelhas sem ferrão (Hymenoptera: Apidae, Meliponini). Ribeirão Preto, 2017. 106 p. : il. ; 30 cm Tese de doutorado, apresentada à Faculdade de Filosofia Ciências e Letras de Ribeirão Preto/USP. Área de concentração: Entomologia. Orientador: Nascimento, Fábio Santos do. 1. Scaptotrigona depilis. 2. Sex pheromones. 3. Mating behavior. 4. Social insects. 5. Drone aggregations. AGRADECIMENTOS À Universidade de São Paulo, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto e ao Programa de Pós-Graduação em Entomologia pela oportunidade concedida. Ao Conselho Nacional de Desenvolvimento Científico e Tecnológico e à Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) pelo financiamento da pesquisa. Ao Prof. Dr. Fábio Santos do Nascimento pela orientação, apoio, incentivo e confiança depositados, fundamentais para a realização deste estudo. Special thanks to Prof. Christoph Grueter for all the supervision given during the whole study. His contribution was fundamental for the development of this PhD. He was always very dedicated and patient to discuss, teach, and follow the project development. I am very grateful for all the discussions, ideas and valuable comments and suggestions in the preliminary versions of this thesis. He also kindly received me for internship in his laboratory at the University of Lausanne, greatly contributing to my academic formation. Special thanks to Francisca Serges for all the friendship and nice discussions, which directly and indirectly contributed to improve my work. I am also very grateful for the kind reception offered during my stay in Lausanne. To prof. Laurent Keller for receiving me in his group at the University of Lausanne and for the support given during the development of the internship. Aos indivíduos de Scaptotrigona depilis pelo sacrifício involuntário indispensável à realização desta pesquisa. Aos meus pais, Adriana e Marcos, e aos meus irmãos, Mari, Vitor, Carol e Dante, por serem parte de mim. Em especial à minha querida Carolinda, pela revisão e formatação final da tese. À Rafa, meu amor, pelo carinho, compreensão, parceria e apoio durante todo o doutorado, especialmente na reta final. Muito obrigado por ser essa mulher incrível e por compartilhar a vida comigo. À Decoy por permitir realizar os experimentos de olfatometria no seu laboratório e aos parceiros dessa empreitada, James e Túlio, pela compreensão e apoio durante todo o desenvolvimento deste trabalho. Aos meus amigos Ganso, Charales, Ingrid e Aline por revisarem o texto e pelos comentários e sugestões valiosíssimos. Às secretárias do Programa de pós-graduação em Entomologia, Renata e Vera, pela atenção, competência e presteza de sempre. A todos os colegas de laboratório por terem participado direta ou indiretamente na realização deste trabalho e, especialmente, ao Dr. Sidnei Mateus, que sempre ofereceu importante ajuda durante todo o doutorado; À Azia, minha primeira orientanda, pela amizade, compreensão e apoio oferecido. Aos amigos que de diferentes maneiras me ajudaram durante esses anos de convivência em Ribeirão Preto, especialmente àqueles da Kalakuta e os agregados. “Like a star rising from the dark and meeting other star that flashes up for a moment only to disappear again in the dark, so man and woman meet each other. They are gliding along together. They light up in love, a brief flame – and disappear again in different directions” Edvard Munch RESUMO Von Zuben, L. G. A comunicação do processo reprodutivo em abelhas sem ferrão (Hymenoptera: Apidae, Meliponini). 2017. 106f. Tese (Doutorado em Ciências). Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, 2017. O processo reprodutivo é de extrema importância para os organismos vivos, é através dele que os indivíduos transmitem as informações contidas em seus genes para as próximas gerações. Para que qualquer indivíduo seja bem-sucedido nesse processo, o primeiro desafio a ser superado é encontrar um parceiro sexual. Para cumprir essa tarefa, machos e fêmeas comunicam sua presença utilizando uma variedade de canais sensoriais. Nas abelhas sociais, o encontro entre machos e fêmeas é um processo complexo e resultado de um refinado sistema de comunicação, mediado principalmente por sinais químicos. Embora Meliponini seja o maior e mais diverso grupo de abelhas sociais, existem poucas informações sobre a comunicação sexual desses insetos. Um fenômeno comum nesse grupo de abelhas é a formação de grandes agregados de machos nas proximidades de colônias que possuem uma rainha virgem. No entanto, os sinais envolvidos na atração dos machos e na formação desses agregados são pouco conhecidos. Desse modo, este trabalho objetivou investigar os fatores envolvidos na comunicação sexual de Meliponini. Para explorar esse problema, nós realizamos uma revisão sobre a biologia reprodutiva dessas abelhas (cap. 1), testamos o papel das forrageiras na atração de machos (cap.2), identificamos os compostos presentes nas marcas depositadas por machos nas agregações (cap.3) e investigamos os fatores relacionados à escolha dos machos por uma determinada colônia (cap. 4). Os resultados obtidos apontam que as forrageiras têm um papel central na atração dos machos e que os machos depositam ativamente seus hidrocarbonetos cuticulares nos locais de agregação. Além disso, foi possível identificar que a atratividade de uma colônia está relacionada com a sua biomassa. Assim, esses resultados contribuem para ampliar nosso conhecimento sobre o processo reprodutivo em abelhas sem ferrão e mostram que a comunicação sexual desse grupo de insetos é um processo tão complexo quanto fascinante que envolve machos, rainhas e operárias. Palavras-chave: Scaptotrigona depilis; feromônios sexuais; comportamento de cópula; insetos sociais; agregações de machos. ABSTRACT Von Zuben, L. G. The mating communication of stingless bees (Hymenoptera: Apidae, Meliponini). 2017. PhD thesis. Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, 2017. Reproduction is the utmost important process for living organisms since it is through this process that individuals can transmit their genetic information to the next generation. To be successful in this process, the first challenge individuals need to overcome is finding a sexual partner. To accomplish this task, males and females communicate their presence using several sensorial modalities. In highly eusocial bees, this complex process is the outcome of a precise chemical communication system. Stingless bees (Meliponini) represents the most species-rich group of eusocial bees and although a lot of information related to the group can be found in the literature, very little is known about their mating communication. A common phenomenon in this group of social bees is the formation of large male aggregations in front of nests during reproductive events. However, the factors involved in the formation of such male aggregation are poorly understood. Therefore, the aim of this study was to investigate the mating communication of stingless bees. To explore this problem, we reviewed the mating biology of the bees (chapter 1), tested the role of foragers in the attraction of males (chapter 2), identified the compounds that drones deposit at the aggregation site (chapter 3) and investigated the factors related to the differential attraction of males to colonies (chapter 4). Our results suggest that foragers have a central role in the long-range attraction of males and that males actively deposit their cuticular hydrocarbons at the aggregation site. Furthermore, we observed that the number of attracted males increased with the weight of colonies, showing that the attractiveness of colonies is related to their biomass. Thus, these results contribute to improve our knowledge about the reproductive process of stingless bees and show that the sexual communication of these bees is as complex as fascinating and involves males, queens and workers. Key words: Scaptotrigona depilis; sex pheromones; mating behavior; social insects; drone aggregations. SUMÁRIO General Introduction ................................................................................................................ 9 CHAPTER 1 – Stingless bees
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