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Universidade Federal Do Paraná UNIVERSIDADE FEDERAL DO PARANÁ THAIS BASTOS ZANATA BEIJA-FLORES E SUAS FONTES DE NÉCTAR: INTERAÇÕES RARAS, ESPÉCIES-CHAVE E VULNERABILIDADE À EXTINÇÃO CURITIBA 2018 THAIS BASTOS ZANATA BEIJA-FLORES E SUAS FONTES DE NÉCTAR: INTERAÇÕES RARAS, ESPÉCIES-CHAVE E VULNERABILIDADE À EXTINÇÃO Tese apresentada como requisito parcial à obtenção do título de Doutora em Ecologia e Conservação, no Curso de Pós-Graduação em Ecologia e Conservação do Setor de Ciências Biológicas da Universidade Federal do Paraná. Orientadora: Prof.ª Dr.ª Isabela Galarda Varassin Co-orientador: Prof. Dr. Bo Dalsgaard CURITIBA 2018 Universidade Federal do Paraná. Sistema de Bibliotecas. Biblioteca de Ciências Biológicas. (Telma Terezinha Stresser de Assis –CRB/9-944) Zanata, Thais Bastos Beija-flores e suas fontes de néctar: interações raras, espécies chave e vulnerabilidade à extinção. – Curitiba, 2018. 190 p.: il. ; 30cm. Orientadora: Isabela Galarda Varassin Co-orientador: Bo Dalsgaard Tese (Doutorado) - Universidade Federal do Paraná, Setor de Ciências Biológicas. Programa de Pós-Graduação em Ecologia e Conservação. 1. Beija-flor. 2. Polinização. 3. Conservação. I. Título. II. Varassin, Isabela Galarda. III. Dalsgaard, Bo. IV. Universidade Federal do Paraná. Setor de Ciências Biológicas. Programa de Pós-Graduação em Ecologia e Conservação. CDD (20. ed.) 581.16 Dedico este trabalho ao meu pai, Angelo A. Zanata, cujo apoio e amor me permitiram realizar este sonho. AGRADECIMENTOS O doutorado foi um intenso caminho percorrido ao longo de quatro anos e foram as pessoas que encontrei nesta caminhada que tornaram esta experiência mais especial. E são a elas que eu agradeço: Isabela G. Varassin, obrigada pela generosidade em me ensinar a ser uma pesquisadora. Seu carinho, calma e compreensão tornaram leves até os momentos mais tensos desta caminhada. Bo Dalsgaard, obrigada por me ensinar a fazer ciência desde o primeiro contato durante o mestrado. Obrigada também por me receber no Center for Macroecology, Evolution and Climate, onde pude aprender mais sobre Ecologia com você e com outros grandes pesquisadores. Laboratório de Ecologia Vegetal, obrigada pela alegria que vocês trouxeram aos meus dias, com as discussões científicas, bolos, risadas e festas. Obrigada também pela paciência com as minhas perguntas sem fim. Levo comigo o meu “temido caderninho”, cheio de anotações das nossas reuniões, que servirão de estímulo para projetos futuros. Vocês sempre serão minha inspiração! Mas preciso agradecer especialmente àqueles que tiraram muitas das minhas dúvidas e que compartilharam e escutaram as minhas angústias científicas: Tiago S. Machado, Vinicius M. da Silva, Ricardo A. C. Oliveira, Israel Schneiberg, Luciana C. Franci e Victor P. Zwiener. Muito obrigada! Sem vocês o processo teria sido muito mais difícil. E é claro, muito obrigada, Tiago S. Malucelli, por toda a ajuda no R e por todos os “vai dar tudo certo” nas etapas finais do doutorado. Márcia C. Marques, obrigada por me ensinar a fazer ciência através das reuniões do laboratório, mas acima disso, obrigada por me ensinar a ser uma cientista mulher. Você sempre será uma das minhas inspirações na luta pelo espaço feminino na academia. James J. Roper, André C. Guaraldo, Guilherme D. S. Seger, Marcos B. Carlucci, Luiz H. Varzinczak, Jeferson V. Bugoni, Pietro K. M. Mendonça, Maurício O. Moura, André A. Padial e Fernanda T. Brum, obrigada por toda ajuda e discussões científicas ao longo do doutorado. Jeferson V. Bugoni, Luísa G. Carvalheiro, Marco A. Mello, Marcos B. Carlucci, Marina Wolowski Torres e Maurício O. Moura, obrigada por terem aceito compor a banca de avaliação, pelas correções e sugestões para melhoria da tese. Luisa F. L. Latorre e Paula V. Stica, muito obrigada pela paciência e pela oportunidade de aprender a ensinar. Embora o meu papel tenha sido ensinar um pouco do que sei a vocês, sinto que durante este período eu aprendi muito mais do ensinei. Obrigada ao CNPq, ao Danish Council for Independent Research Natural Sciences e ao Center for Macroecology Evolution and Climate pelo financiamento das visitas aos museus para coleta dos dados morfológicos. Alexandre Aleixo (Museu Paraense Emílio Goeldi, Belém, Brasil), Gary Graves (Smithsonian National Museum of Natural History, Washington, USA), Gerald Mayr (Senckenberg Naturmuseum Frankfurt, Frankfurt, Germany), John Bates (Field Museum of Natural History, Chicago, USA), Jon Fjeldså (Zoologisk Museum, Statens Naturhistoriske Museum, Copenhagen, Denmark), Juliana Paulo da Silva (Museu de Biologia Mello Leitão, Santa Teresa, Brasil), Karl-Ludwig Schuchmann (Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany), Marcos Raposo (Museu Nacional, Rio de Janeiro, Brasil), Mark Adams (Natural History Museum of Tring, Tring, UK), Paul Sweet (American Museum of Natural History, New York, USA), Robert Prys-Jones (Natural History Museum of Tring, Tring, UK) e Till Töpfer (Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany), obrigada por permitirem a minha visita aos museus para coleta dos dados morfológicos. Alan D. C. Moura, Allan Timmermann, Aline G. Coelho, Ana Maria M. Gonzalez, Ana M. Rui, Andrea C. Araújo, Andrea Barquero, Bo Dalsgaard, Boris Tinoco, Caio G. Machado, Carlos Lara, Erich Fischer, Flor Maria G. Las-Casas, Genilda M. Oliveira, Glauco Kohler, Jeferson V. Bugoni, Juan F. Ornelas, Licléia C. Rodrigues, Liliana R. Lasprilla, Márcia Rocca, Marlies Sazima, Maria A. Maglianesi, Monica B. Ramirez, Oscar H. M. Gómez, Paulo E. Oliveira, Pete Cotton, Pietro K. Maruyama, Raul O. Pulido, Ruben Alarcon, Stefan Abrahamczyk, Stella Watts, Tanja T. Ingversen e Tiago S. Malucelli, obrigada por compartilharem os dados não publicados das interações entre beija-flores e plantas. Obrigada à CAPES e ao PPG em Ecologia e Conservação da UFPR pela bolsa de doutorado e doutorado sanduíche. Mas acima disso, obrigada aos brasileiros que pagam seus impostos e que financiam a ciência feita no país. E finalmente, obrigada à minha família e amigos, que são a minha maior fonte de alegria e amor. “The important thing is not to stop questioning. Curiosity has its own reason for existence”. (Albert Einstein) RESUMO Beija-flores são aves nectarívoras que polinizam mais de 1.300 espécies de plantas nas Américas, desempenhando um importante papel na manutenção da biodiversidade. As questões exploradas nesta tese foram norteadas pela seguinte ameaça à biodiversidade: a extinção das interações mutualísticas, como a polinização realizada pelos beija-flores. Considerando este problema e a importância dos beija-flores como polinizadores, no primeiro capítulo investigamos a vulnerabilidade das interações raras entre beija-flores e plantas, uma vez que interações raras tendem a ser mais vulneráveis à extinção do que interações redundantes. Para isso, utilizamos 74 redes de interação entre beija-flores e plantas distribuídas ao longo de um amplo gradiente latitudinal (38°N– 31°S). Encontramos que beija-flores pertencentes a linhagens raras e que possuem morfologias distintas tendem a realizar interações raras, além de evitarem co-extinções, uma vez que realizam interações não redundantes. No segundo capítulo, descrevemos as características das espécies-chave de beija-flores nas redes de interação, já que espécies- chave contribuem para a manutenção das interações no sistema. Detectamos que beija- flores com bico curto e reto, tamanho alar grande, que possuem maior frequência de interação com as plantas e pertencentes aos clados dos Bees, Emeralds e Mangoes tendem a ser espécies-chave nas redes de interação. E finalmente, no terceiro capítulo, testamos quais características estão associadas à vulnerabilidade à extinção de 341 espécies de beija-flores. Encontramos que beija-flores com bico curto e reto e pertencentes a linhagens evolutivas comuns possuem maior vulnerabilidade à extinção. Dessa forma, considerando os resultados obtidos, detectamos as seguintes vulnerabilidades no sistema de polinização de beija-flores: as interações raras e a estabilidade do sistema são garantidas por espécies não redundantes evolutiva e morfologicamente e que atributos morfológios das espécies-chave estão associados a vulnerabilidade à extinção dos beija-flores. Palavras-chave: Centralidade. Conservação. Espécies ameaçadas. Extinção. Polinização. Interação animal-planta. Raridade. ABSTRACT Hummingbirds are nectar-feeding birds that pollinate more than 1,300 plant species in the Americas, performing an essential role for the maintenance of biodiversity. The questions explored in this thesis were guided by the following biodiversity threat: the extinction of mutualistic interactions, like the pollination by hummingbirds. Considering this threat and the importance of hummingbirds as pollinators, in the first chapter we explored the vulnerability of rare interactions between plants and hummingbirds, since rare interactions tend to be more vulnerable to extirpation than redundant interactions. To answer this question, we used 74 plant-hummingbird interaction networks widely distributed across the Americas (38°N–31°S). We found that hummingbirds belonging to rare evolutionary lineages and having distinct morphologies tend to perform rare interaction, and are also those preventing secondary extinctions, since they perform non- redundant interactions. In the second chapter, we described the characteristics of keystone hummingbird species in the networks, since keystone species tend to prevent the extinction of mutualistic interactions. We detected that hummingbirds with short and straight bills,
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