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Stanton Marianaalves M.Pdf ii iii Agradecimentos Gostaria de agradecer a todos que me ajudaram e incentivaram ao longo desse trabalho: Em primeiro lugar, aos meus pais, Virgilia e Michael, por me apoiarem em todos os momentos, pelos conselhos e consolos. Aos meus irmãos, Leonardo e Anthony, que mesmo de longe torceram sempre por mim. Ao Igor, minha força e minha calma, que chegou no meio dessa etapa da minha vida e sempre acreditou em mim. Ao meu orientador, Prof. Dr. José Roberto Trigo, pela oportunidade e pelos muitos ensinamentos. Aos membros da banca e pré-banca, Dr. Alberto Arab, Dra. Daniela Rodrigues, Prof. Dr. Eduardo L. Borba, Prof. Dr. Flavio A. M. dos Santos e Dra. Karina L. Silva- Brandão pelos comentários e sugestões importantes. À FAPESP, pela bolsa concedida. Aos companheiros de laboratório: Kamila, Alberto, Carlos, Marcela, Adriano, Tamara e Aline, pelas discussões, pela ajuda em laboratório, pela amizade e por tornarem o laboratório um ambiente de trabalho divertido. Aos amigos que me ajudaram em campo: Alberto, Ana, Henrique, Thiago e também ao funcionário Paulo Roberto Manzani. Ao funcionário José Carlos da Silva, o Zé, por me ajudar a carregar vasos pesados, quebrar muitos galhos e me ensinar quase tudo o que eu sei sobre cuidados com plantas. À Tamara pela ajuda indispensável com as extrações na etapa final. Às amigas da graduação (Ana, Alê, Bruna, Gaby, Karen, Marilini, Stef e Yara) por estarem comigo nos momentos bons e ruins. Aos muitos amigos do Rio, por entenderem iv minhas longas ausências e sempre me receberem de braços abertos quando eu volto. Aos amigos da pós da Ecologia pelas intensas discussões sobre ecologia ou sobre besteiras, pelos cafés e as cervejinhas. v Sumário RESUMO .........................................................................................................................................7 ABSTRACT.....................................................................................................................................9 INTRODUÇÃO GERAL..............................................................................................................11 REFERÊNCIAS BIBLIOGRÁFICAS ........................................................................................18 CAPÍTULO I: “SIMULATED HERBIVORY IN ASCLEPIAS CURASSAVICA (APOCYNACEAE: ASCLEPIADOIDEAE) AFFECTS GROWTH AND REPRODUCTION BUT NOT CARDENOLIDES”.......................................................................................................................22 INTRODUCTION.........................................................................................................................23 MATERIALS AND METHODS..................................................................................................26 RESULTS.......................................................................................................................................32 DISCUSSION ................................................................................................................................34 REFERENCES..............................................................................................................................38 CAPÍTULO II: “METHYL JASMONATE AFFECTS GROWTH, REPRODUCTION AND DEFENSES IN ASCLEPIAS CURASSAVICA (APOCYNACEAE: ASCLEPIADOIDEAE)”47 INTRODUCTION.........................................................................................................................48 MATERIALS AND METHODS..................................................................................................50 RESULTS.......................................................................................................................................55 DISCUSSION ................................................................................................................................56 REFERENCES..............................................................................................................................59 APPENDIX 1: CARDENOLIDE EXTRACTION AND LEAD ACETATE CLEANUP .......66 APPENDIX 2: LEAF AREA MEASUREMENTS ....................................................................68 CONCLUSÕES GERAIS .............................................................................................................69 vi Resumo. A produção de defesas contra a herbivoria é essencial para o sucesso reprodutivo das plantas, no entanto pode ser custosa. Esses custos resultam da redução de investimento em outras partes do metabolismo, como o crescimento e a reprodução. Nesse estudo, usamos Asclepias curassavica (Apocynaceae: Asclepiadoideae) como modelo para avaliar como uma planta divide seus recursos entre crescimento, reprodução e defesas. A. curassavica é uma planta anual que possui cardenolidas como defesas. Para verificar como esta responde a herbivoria, simulamos a mesma através de dano artificial (DA) e medimos crescimento (biomassa de folhas e raízes) e reprodução (número de flores, frutos e sementes e biomassa de sementes) em um experimento em longo prazo. Em um experimento em curto prazo, medimos a produção de defesas (concentração de cardenolidas), para avaliar se estas podem estar interferindo no crescimento e reprodução desta espécie. Correlacionamos também, em uma população natural, a concentração de cardenolidas com a percentagem de herbivoria foliar. O hormônio jasmonato de metila (JM) é usado para induzir compostos do metabolismo secundário em plantas, sem o custo adicional da remoção de tecido fotossinteticamente ativo causada por dano artificial ou natural. Usamos esse composto em ambos os desenhos experimentais acima ao invés de remoção da área foliar para avaliar se havia indução de cardenolidas e seu efeito sobre o crescimento e reprodução de A. curassavica . Nossos resultados demonstraram uma redução significativa do número total de frutos, sementes e da massa final de raízes em plantas com tratamento de DA em longo prazo. O crescimento do tratamento DA não diferiu do controle, sugerindo crescimento compensatório das folhas à custa do investimento em raízes e em reprodução. Os custos reprodutivos e de crescimento de raízes detectados no experimento de longo prazo podem 7 resultar da diminuição da capacidade fotossintética em plantas danificadas e investimento simultâneo em crescimento compensatório das folhas. No experimento de curto prazo, não houve alteração da razão de indução de cardenolidas sugerindo que o dano artificial não induz defesas nessa espécie. A ausência de correlação entre cardenolidas e porcentagem de dano natural em plantas coletadas em campo pode sugerir dois cenários excludentes: 1. a indução de cardenolidas não seria importante para a defesa de A. curassavica , ou 2. a ausência de correlação, associada a baixa percentagem de herbivoria implicaria em uma defesa constitutiva eficaz contra herbívoros. O tratamento com JM a longo prazo também mostrou uma tendência à redução do crescimento de raízes e redução significativa da biomassa e porcentagem de germinação de sementes. Nas plantas tratadas com JM a curto prazo, houve um aumento significativo de cardenolidas tardio (384 h após tratamento) sugerindo que estas podem contribuir para a redução de aptidão observada no experimento de longo prazo e que existem custos da produção das mesmas. Dano artificial leva à diminuição da aptidão, através de desvio de investimento em raízes para o crescimento compensatório das folhas. No caso do jasmonato, não houve perda de massa fotossinteticamente ativa (folhas) e a redução do crescimento de raízes pode ser resultado de um efeito direto do tratamento de JM ou indireto causado pela indução de outras partes do metabolismo (p.ex. metabolismo secundário) causada por esse fitohormônio. Experimentos futuros devem comparar os presentes resultados com dano real por um dos herbívoros especialistas para avaliar a eficácia do dano artificial em induzir cardenolidas e o papel dessa indução sobre outras partes do metabolismo da mesma. 8 Palavras-chave: Alocação, Asclepias curassavica , cardenolidas, crescimento compensatório, jasmonato de metila, herbivoria, respostas induzidas. Abstract. Although the investment in defensive traits against herbivory is essential to the reproductive success of plants, it may be costly. These costs result from reduced investment in other metabolic functions such as growth and reproduction. In the present study, we used the milkweed Asclepias curassavica (Apocynaceae: Asclepiadoideae) as a model to study how a plant divides its resources between growth, reproduction and defense. A. curassavica is an annual weed that uses cardenolides as defenses against herbivory. To evaluate how Asclepias curassavica responds to herbivores, we simulated herbivory by artificial damage (AD) and measured growth (leaf and root biomass) and reproduction (number of flowers, fruit and seeds and seed biomass) in a long term experiment. We also measured defensive traits (cardenolide concentration) in a short term experiment to verify whether there is an investment in defense that may interfere with growth and reproduction. We also correlated cardenolide concentration in a natural population with percent leaf damage. As the plant hormone, methyl jasmonate (MJ) is commonly used to induce secondary metabolism in plants without the additional costs of tissue removal, we used this compound in the same experimental designs instead of AD. Our results from the long term AD treatment showed a significant decrease in final root biomass and in total fruit set and seed number. Plants from the AD treatment
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