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Universidade Estadual De Campinas Instituto De Biologia UNIVERSIDADE ESTADUAL DE CAMPINAS INSTITUTO DE BIOLOGIA THIAGO MARINHO ALVARENGA INFLUÊNCIA DAS PLANTAS HOSPEDEIRAS SOBRE AS ESTRATÉGIAS REPRODUTIVAS DE CASSIDINAE S. STR. (COLEOPTERA: CHRYSOMELIDAE), COM ÊNFASE NO CUIDADO MATERNO DE ESPÉCIES DA TRIBO MESOMPHALIINI CAMPINAS 2018 THIAGO MARINHO ALVARENGA INFLUÊNCIA DAS PLANTAS HOSPEDEIRAS SOBRE AS ESTRATÉGIAS REPRODUTIVAS DE CASSIDINAE S. STR. (COLEOPTERA: CHRYSOMELIDAE), COM ÊNFASE NO CUIDADO MATERNO DE ESPÉCIES DA TRIBO MESOMPHALIINI Tese apresentada ao Instituto de Biologia da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do Título de Doutor em Biologia Animal na Área de Biodiversidade Animal. ESTE ARQUIVO DIGITAL CORRESPONDE À VERSÃO FINAL DA TESE DEFENDIDA PELO ALUNO THIAGO MARINHO ALVARENGA E ORIENTADA PELO DR. JOÃO VASCONSELLOS NETO. Orientador: JOÃO VASCONSELLOS NETO Co-Orientador: VALMIR ANTONIO COSTA CAMPINAS 2018 Campinas, 09/02/2018. COMISSÃO EXAMINADORA Prof. Dr. João Vasconsellos Neto Prof. Dr. Adalton Raga Prof. Dr. Miguel Francisco de Souza Filho Prof. Dr. César Freire Carvalho Profa. Dra. Margarete Valverde de Macedo Os membros da Comissão Examinadora acima assinaram a Ata de Defesa, que se encontra no processo de vida acadêmica do aluno. Aos meus pais João e Márcia, que me apresentaram à importância da família e ao caminho da honestidade e persistência. DEDICO. AGRADECIMENTOS À CAPES e ao Programa de Pós Graduação em Biologia Animal da Unicamp pela bolsa e oportunidade de realizar esse estudo. Ao Prof. Dr. João Vasconcellos Neto, o meu respeito e admiração pela sua serenidade em momentos difíceis, capacidade de estimular e enxergar oportunidades de estudo e amizade ao longo desses anos. Ao Prof. Dr. Valmir A. Costa, pelas risadas infames da vida, apoio e estímulo à pesquisa de vespas parasitoides. À minha família, que sempre depositou sua confiança em mim. Poderia escrever um livro de agradecimentos e não bastaria para descrever todos os seus esforços. À Fernanda Fonseca, por ser meu porto seguro, pela paciência e amor ao longo de todos esses anos de indústria vital. À Camila Maioralli (in memoriam) e German A. Villanueva, pela amizade e cumplicidade nas descobertas acadêmicas. Ao meu cunhado Vinicius Fonseca, por estar sempre pronto a me ajudar. Ao Instituto Biólogico (CEIB) principalmente aos profissionais do laboratorio de Controle de Biológico que me fazem sentir a verdadeira força do trabalho entre amigos. A realização desse estudo só foi possível com o apoio de vários colaboradores. Aos professores do Dep. de Biologia Animal da UNICAMP, que sempre me escutaram e retornaram com conselhos valiosos. Em especial ao Prof. Martin Pareja, que sempre esteve presente nos meus conflitos intelectuais e me orientando de forma amiga. Ao Dr. Ernesto Prado pela amizade e valiosos conselhos. Ao Dr. Tales G. Vieira por criar possibilidades e compartilhar oportunidades. À Luciana Fernandes, do Departamento de Ecologia e Biologia Evolutiva da Universidade Federal de São Carlos, pelas fotomicrografias dos ovos de Mesomphaliini. À Antonio Fiorito e Yuri Messas pela disponibilidade das fotos de Cassidinae de Teresópolis, RJ. Ao Dr. Sebastian Felipe Sendoya, pela identificação das formigas. À Dra Flávia Fernandes, pela ajuda na identificação dos besouros. Ao Dr. Donald Windsor e Dr. Christer Hansson pela atenção e ensinamentos. Ao meu amigo Rodolfo Hebert, que mesmo com a distância, sempre pude contar com a sua visão prática e alegre da vida. Ao meu amigo Leonardo Davine Dantas “semeando a ferrugem que nunca dorme”. “Odessa, How strong am I? Odessa, How time goes by” Odessa – Bee Gees RESUMO A sobrevivência de inúmeras espécies de insetos fitófagos depende das plantas como fonte de alimento, sendo as interações entre plantas e herbívoros dominantes no ambiente terrestre. O objetivo principal deste estudo foi compilar informações sobre o uso de plantas hospedeiras por Cassidinae s. str., buscando padrões ecológicos nas associações e, por fim, entender como os atributos funcionais influenciam a evolução de estratégias de oviposição desses besouros. Observa-se que Cassidinae s. str. estão associados a lianas da família Convolvulaceae, plantas que apresentam atributos funcionais anti-herbivoria como nectários extraflorais (NEFs), látex e tricomas. Com relação às estratégias de oviposição, foram coletados e analisados ovos de 36 espécies identificadas de Mesomphaliini. Diversos visitantes dos nectários extraflorais de Convolvulaceae foram encontrados predando ovos de Mesomphaliini; no entanto, mesmo com o patrulhamento de formigas, as populações desses besouros conseguem se estabelecer utilizando diferentes estratégias defensivas. Avaliou-se tambem a influência da planta hospedeira na origem do comportamento de cuidado materno em Mesomphaliini. Verificou-se que os predadores e parasitoides que visitam NEFs de Convolvulaceae são agentes importantes na mortalidade dos besouros associados. Experimentalmente avaliou-se a importância do comportamento materno em plantas que apresentam NEFs (nectários extraflorais). Os parasitoides de ovos encontrados frequentemente sobre o élitro das diversas espécies de besouros pertenciam ao gênero Emersonella Girault, 1916 (Hymenoptera: Eulophidae). O parasitoide Emersonella pubipennis Hansson, 2002 foi encontrado em todas as espécies de Mesomphaliini com cuidado materno avaliadas nesse estudo. Palavras chave: Adaptations; América Latina; Atributos Funcionais; Formigas; Relação inseto-planta; Oviposição ABSTRACT The survival of numerous species of phytophagous insects depends on plants as a source of food, and the interactions between plants and herbivores are dominant in the terrestrial environment. The main objective of this study was to compile information on the use of host plants by Cassidinae s. str., searching for ecological patterns in the associations and, finally, to understand how the functional attributes influence the evolution of oviposition strategies of these beetles. It is observed that Cassidinae s. str. are associated with Convolvulaceae lianas, plants that exhibit functional anti-herbivory attributes such as extrafloral nectariess (EFNs), latex and trichomes. Regarding oviposition strategies, eggs from 36 species identified Mesomphaliini species were collected and analyzed. Several visitors to the extrafloral nectar of Convolvulaceae were found preying on Mesomphaliini eggs; however, even with ant patrolling, the populations of these beetles can be established using different defensive strategies. The influence of the host plant on the origin of the maternal care behavior in Mesomphaliini was also evaluated. It has been found that predators and parasitoids that visit Convolvulaceae EFNs are important agents in the mortality of associated beetles. The importance of maternal behavior in plants with EFNs has been evaluated. The parasitoids of eggs frequently found on the elytron of various species of beetles belonged to the genus Emersonella Girault, 1916 (Hymenoptera: Eulophidae). The parasitoid Emersonella pubipennis Hansson, 2002 was found in all species of Mesomphaliini with maternal care evaluated in this study. Key words: Adaptation; Ants; Functional traits; Insect-plant relationships; Latin America; Oviposition. Sumário 1 INTRODUÇÃO GERAL ........................................................................................................ 12 2 REVISÃO DE LITERATURA ................................................................................................. 14 2.1 Termos e conceitos utilizados nesse estudo ........................................................................... 14 2.2 Interações inseto-planta em Cassidinae s. str. .......................................................................... 16 2.3 Ecologia evolutiva e a influência da planta hospedeira na evolução dos herbívoros ............... 17 2.4 Plantas hospedeiras de Mesomphaliini (Coleoptera: Cassidinae s. str.) e atributos funcionais de defesas que atuam contra a herbivoria .................................................................................... 19 2.5 Nectários extraflorais em Convolvulaceae com ênfase no gênero Ipomoea ............................ 20 2.6 Aspectos da História Natural relacionadas a sobrevivência de Cassidinae s. str. com ênfase em Mesomphaliini ........................................................................................................................... 26 2.7 O cuidado materno em Cassidinae s. str. com ênfase na tribo Mesomphaliini ........................ 28 2.8 Evolução fenotipica paralela e o cuidado materno em Insecta ................................................ 31 2.9 Inimigos naturais de Cassidinae s. str. como agentes de seleção ............................................. 33 3 REFERÊNCIAS BIBLIOGRÁFICAS ...................................................................................... 37 4 ASSOCIAÇÕES ENTRE CASSIDINAE S. STR. E PLANTAS HOSPEDEIRAS ................. 49 4.1 Resumo ...................................................................................................................................... 49 4.2 Abstract ..................................................................................................................................... 49 4.3 Introdução ................................................................................................................................. 50 4.4 Material e Métodos ..................................................................................................................
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