Karlla V.C. Barbosa - Ecologia e Comportamento das Aves Migratórias e Urbanização da Mata Atlântica do Brasil. PROGRAMA DE PÓS-GRADUAÇÃO EM CIÊNCIAS BIOLÓGICAS (ZOOLOGIA) ECOLOGIA E COMPORTAMENTO DAS AVES MIGRATÓRIAS NEOTROPICAIS AUSTRAIS E A URBANIZAÇÃO DA MATA ATLÂNTICA DO BRASIL ECOLOGY AND BEHAVIOR OF NEOTROPICAL AUSTRAL MIGRANT BIRDS AND URBANIZATION IN THE ATLANTIC FOREST, BRAZIL Karlla Vanessa de Camargo Barbosa Tese apresentada ao Instituto de Biociências da Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de Rio Claro, para a obtenção do título de Doutora em Ciências Biológicas (Área de concentração: Zoologia) Rio Claro – SP 2020 Setembro 2020 2 ECOLOGIA E COMPORTAMENTO DAS AVES MIGRATÓRIAS NEOTROPICAIS AUSTRAIS E A URBANIZAÇÃO DA MATA ATLÂNTICA DO BRASIL ECOLOGY AND BEHAVIOR OF NEOTROPICAL AUSTRAL MIGRANT BIRDS AND URBANIZATION IN THE ATLANTIC FOREST, BRAZIL Karlla Vanessa de Camargo Barbosa Rio Claro - SP Setembro 2020 Tese apresentada ao Instituto de Biociências da Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de Rio Claro, para a obtenção do título de Doutora em Ciências Biológicas (Área de concentração: Zoologia) Orientador: Prof. Dr. Alejandro Edward Jahn Coorientador: Prof. Dr. Milton Cezar Ribeiro 3 Karlla V.C. Barbosa - Ecologia e Comportamento das Aves Migratórias e Urbanização da Mata Atlântica do Brasil. 7 AGRADECIMENTOS Esse trabalho só foi possível graças a ajuda de várias pessoas, desde voluntários (estagiários), a observadores de aves, professores e amigos. Por isso quero agradecer imensamente a todos que, de alguma forma, fizeram parte desse processo enriquecedor e de crescimento que foi para mim o doutorado. Cito alguns nomes abaixo, mas se eu esquecer de alguém com certeza vou reencontrar, lembrar e agradecer pessoalmente. Para que eu conseguisse realizar algumas atividades da pesquisa foi fundamental ter ajuda. Para as capturas-marcações das aves, principalmente do bem-te-vi-rajado, eu sempre precisei do apoio de pelo menos duas pessoas. Muito obrigada, amigos e voluntários que não mediram esforços para me ajudar: Albert Aguiar, Alcides Dutra, Alecsandra Tassoni, Alice Reisfeld, Amanda Viana, André Menini, Arthur M. Gomes, Beto Costa, Bianca Matinata, Carlos Henrique Ferreira (Ferreirinha), Carlos Gussoni, Clément Delaleu, Cristiane Gardim, Cristiane Santos, Denis Vinny, Evelyn Melo, Flavia Arantes, Gleyson George, Guilherme Brandão, Guilherme Canassa, Guilherme L. Ferreira, Gustavo A. Levy, Guto Carvalho, Ivan Provinciato, Juliana Vitorio, Kauan Martins, Kelly Pereira, Leticia Rodrigues, Luciano Bernardes, Lucas Gaspar, Marco Silva (Marcão), Maria Clara Tinti, Matheus Bernardo, Matheus M. Santos, Murilo Vicente, Nice Stramaro, Paulo Moura, Rafaela W. Carvalho, Rayane G. Tomaselli, Rodrigo Missano, Samuel Nunes, Vanesa Bejarano, Vanessa Valentim, Vinicius Secco, Voluntárias do PET (2019 – Andressa Garcia, Barbara Betini, Letícia Malta e Beatriz Valério de Jesus) e Yuri Napoleão. O meu muito obrigada também a todos observadores de aves e amigos que dedicaram seu tempo para me passar informações sobre ninhos e registros das aves migratórias. Cito aqui alguns nomes para representar todos os observadores que registraram no site Aves da Cidade ou em outras fontes: Adolf C. Kruger, Armando Stilhano Neto, Beatris Gianiselle, Bruna Gagetti, Bruna Lopes, Chico Martins, Christiane A. Ahlgrimm, Claudia Chang, Daniel Gracioso, Daniele C. Vanzo, Diomar A. Quadros, Douglas Negeini, Ednilson M. Pereira, Fabio Schunck, Fernando Lotto, Flavio T. Souza, Henrique (Carlos Pires), Igor Kusmitsch, Jairo E. Silva, Jane Rotta, Joana Tomazelli, Julia, Juliana Lima, Leandro, Luciano Breves, Marcos Granjeiro, Marina Cortes, Maristela Camolesi, Mauro Luiz Junior, Messias R. Neto, Natalia Allenspach, Renato M. Sobral, Rodolfo P. Graciotti, Rolf Gustaf Odelius, Luciana Souza, Rubens Galdino, Sergio Ambiel, Uêdson Rêgo e Valmir A. Costa. O Aves da Cidade é um site que criei para coletar informações para meu estudo sobre as aves migratórias, através de ciência cidadã, e também divulgar o trabalho com uma linguagem mais acessível ao público não acadêmico sobre as aves urbanas https://avesdacidade.wordpress.com/ Me sinto muito grata e privilegiada porque nos momentos de indecisão e dificuldade tive amigos muito queridos com o qual pude contar, tanto nas análises de dados como nas discussões de ideias. https://avesdacidade.wordpress.com/ 8 Muito obrigada: Augusto Batisteli (ajudou fornecendo dados dos bem-te-vi-rajados e sobre ninhos), Marcos Melo (me recebeu no zoo de Guarulhos e tivemos várias conversas sobre ecologia urbana), Natalia Stefanini (me ajudou com as análises de Kernel e em vários momentos de emergênica), Melina Leite (Meme - que me socorreu com os scripts do R...algumas vezes inclusive), Andrea L. Boesing (Lari - que me ajudou na classificação da paisagem), Carlos Candia-Gallardo (Kiwi - que me socorreu com os gráficos no R quando eu estava perdida), João Carlos Pena e Fabio Barros (que me ajudaram a decidir as paisagens do primeiro capítulo e participou da minha defesa de projeto), Karl Mokross (que participou do nascimento da ideia inicial dessa tese), Carlos Gussoni (além de ajudar no nascimento da ideia inicial também foi meu colega de casa e sempre me apoiou) e Rafael Souza (Urucum - como esquecer dele que sempre ajuda todos! Me ajudou com gravadores e apresentações). Do período que fiquei no Cornell Labo of Ornithology agradeço ao Gerardo Soto e Marcelo Awade que dedicaram horas para me ajudar nas análises do capítulo 1; e também àqueles que me deram apoio e contribuíram com ricas discussões sobre aves e conservação, Amanda Rodewald, Christopher Wood, Matthew Medler, Luciana Guimarães, e Wesley Hochachka, além de todos os amigos que me apresentaram as aves de Ithaca – NY (Karan Odom, Lilly Briggs, Ian Daves, Jay McGowan and Drew Meber). Nesse período tive também o apoio de instituições, o qual foi primordial para a realização do trabalho. Nessas instituições também fiz amigos que me apoiaram: Prefeitura de São Paulo – DEPAVE (Anelisa Magalhães, Leticia Zimback e Marcos Kawall), CRAS PET – Parque Ecológico do Tietê (Liliane Milanelo, Fabio Toledo, Lilian Sayuri, Valéria Pedro e Haroldo Furuya), Instituto Butantan (toda a equipe e em especial a Erika Hingst-Zaher), SAVE Brasil (toda equipe e em especial ao Pedro Develey por acreditar em mim), UNESP (turma dos laboratórios LEEC e LECAVE), Jardim Botânico de São Paulo (Domingos Rodrigues e Janaína Costa), Parque Estadual da Cantareira (todos os gestores e monitores dos núcleos Engordador e Pedra Grande) e Horto de São Paulo (todos os gestores e monitores). O presente trabalho foi realizado com apoio da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Código de Financiamento 001. Sou grata também a todos os financiamentos que recebi nesse período que permitiram que a pesquisa fosse realizada. Em especial agradeço a CAPES por fornecer minha bolsa de estudos e a ajuda de campo (através do PROAP), à AFO (Associantion of Field Ornithology), Idea Wild e The Cornell Lab of Ornithology. Aos amigos que me abriram seus lares e me receberam em suas casas, no Estados Unidos – Pedro Peloso/Silvia Pavan, Jennifer Bien-Aime, Luciana Guimarães/Matt Medler, Alex/Shazeeda – e em Rio Claro – Claudinha Kanda, Natalia Stefanini, Laurinha Honda, Cristina Gonçalves/Cesar Cestari e Ana Cristina Crestari/André Regolin – meu muito obrigada, vocês foram incríveis! 9 Minha gratidão aos professores, mentores e amigos que me apoiaram e me guiaram por todo esse período: Alex Jahn, Milton Ribeiro (Miltinho), Marco Aurélio Pizo e Amanda Rodewald. Agradeço os presentes que ganhei do bem-te-vi-rajado: quadro com a foto linda de filhotes de bem-te- vi-rajado da Diná Galdino (em memória) e seu filho Luciano; e a pintura da Cris Gardim. Obrigada a minha família que tanto amo, minhas irmãs (Kaccia e Karine), meu pai (Olaf - em memória) e principalmente a minha mãe Carmina. Mãe, sou muito grata pelo apoio e pela grande contribuição na minha formação como pessoa e profissional. Eu também não poderia esquecer de todos meus “Amigos para Sempre” pelo carinho, apoio e atenção quando precisei. E a família do Thiago, principalmente a minha sogra Claudete que sempre compartilhou das minhas alegrias e conquistas. E por último deixei para agradecer a pessoa mais especial nesse processo que passei nos últimos anos: o meu companheiro de lar, de artigos e de momentos bons e difíceis, Thiago VV Costa. Essa trajetória teria sido muito mais difícil sem você! Você esteve ao meu lado por todos esses anos me apoiando e ajudando em quase todos os campos, e revisando meus textos e artigos. Sem você eu não teria conseguido! Muito obrigada! “Nunca deixe que lhe digam que não vale a pena acreditar no sonho que se tem. ou que seus planos nunca vão dar certo ou que você nunca vai ser alguém... Se você quiser alguém em quem confiar confie em si mesmo. Quem acredita sempre alcança! ” Mais uma vez - Renato Russo 10 Sumário APRESENTAÇÃO _____________________________________________________________ 12 Resumo ______________________________________________________________________ 13 Abstract ______________________________________________________________________ 15 INTRODUÇÃO GERAL ____________________________________________________ 17 Referências bibliográficas _______________________________________________________ 22 CAPÍTULO 1 _____________________________________________________________ 28 Noise level and distance to water drive resident and migratory bird species richness within a Neotropical megacity ___________________________________________________________ 29 Abstract ______________________________________________________________________________ 29 1. Introduction _________________________________________________________________________ 30 2. Material and methods _________________________________________________________________ 32 3. Results _____________________________________________________________________________ 36 4. Discussion __________________________________________________________________________ 39 5. Conclusions _________________________________________________________________________ 42 6. References __________________________________________________________________________ 43 Supplementary material _________________________________________________________________ 49 Appendix A ___________________________________________________________________________ 52 Appendix B ___________________________________________________________________________ 53 CAPÍTULO 2 _____________________________________________________________ 57 Habitat use and home range of a migratory bird, Myiodynastes maculatus solitarius, in an urban park in the Atlantic Forest, Brazil _______________________________________ 58 Abstract ______________________________________________________________________________ 58 1. Introduction ______________________________________________________________________ 59 2. Methods ____________________________________________________________________________ 60 3. Results _____________________________________________________________________________ 62 4. Discussion __________________________________________________________________________ 65 5. References __________________________________________________________________________ 68 CAPÍTULO 3 _____________________________________________________________ 72 Body condition, sex and urbanization influences breeding-site fidelity of Neotropical austral migrant flycatchers (Tyrannidae) in Brazil _________________________________________ 73 Abstract ______________________________________________________________________________ 73 1. Introduction ______________________________________________________________________ 74 2. Methods _________________________________________________________________________ 75 3. Results __________________________________________________________________________ 78 4. Discussion _______________________________________________________________________ 81 5. Conclusions ______________________________________________________________________ 85 6. References _______________________________________________________________________ 85 11 CAPÍTULO 4 _____________________________________________________________ 89 The potential for citizen science to contribute to research and conservation of birds in Brazil _____________________________________________________________________________ 90 Abstract ______________________________________________________________________________ 90 1. Introduction _________________________________________________________________________ 91 2. Methods ____________________________________________________________________________ 92 3. Results _____________________________________________________________________________ 95 4. Discussion _________________________________________________________________________ 100 5. Conclusions ________________________________________________________________________ 100 6. References _________________________________________________________________________ 104 CONSIDERAÇÕES FINAIS _______________________________________________ 111 12 APRESENTAÇÃO Este documento é o produto de quatro anos de pesquisa em ecologia de aves, ecologia urbana, migração das aves, história natural de aves migratórias e ciência cidadã. Esse período de pesquisa permitiu um grande conhecimento e crescimento profissional, gerando artigos em revistas científicas especializadas de grande impacto, matérias em jornais populares de ampla circulação, e encontros, estágios e discussões com especialistas no Brasil e Estados Unidos. Assim, como produto final, a presente tese de doutorado está dividida em quatro capítulos que estão estruturados em forma de artigos científicos. Apesar dos artigos serem independentes, seus resultados são complementares e apresentam resultados inéditos. O documento se inicia com uma introdução geral sobre os assuntos abordados nos capítulos, seguida dos artigos científicos produzidos com os resultados desta tese de doutorado, sendo parte já publicada em revistas revisada por pares: Capítulo 1: Barbosa KV, Rodewald AD, Ribeiro MC & Jahn AE (2020). Noise level and water distance drive resident and migratory bird species richness within a Neotropical megacity. Landscape and Urban Planning, 197, 103769. Capítulo 2: Vitorio JG*, Frenedozo RC & Barbosa KVC* (2019). Habitat use and home range of a migratory bird, Myiodynastes maculatus solitarius, in an urban park in the Atlantic Forest, Brazil. Brazilian Journal of Ornithology, 27(2): 115–121. * Both authors contributed equally to this work. Capítulo 3: Barbosa KV, Bejarano VA, Costa TVV, Ribeiro MC & Jahn, AE. Breeding- site fidelity of three Neotropical austral migrant flycatchers (Tyrannidae) in Brazil. In prep. Capítulo 4: Barbosa KV, Develey PF, Ribeiro MC & Jahn, AE. The potential of citizen science to contribute to research and conservation of birds in Brazil. Submitted to Ornithology Research. A última seção deste documento apresenta uma conclusão geral sobre os principais resultados obtidos e apresentados nos quatro capítulos e de acordo com o tema central da tese, que foi entender a ecologia e comportamento das aves migratórias neotropicais austrais na Mata Atlântica do Brasil. 13 Resumo geral Vivemos em uma era onde as paisagens naturais do planeta são alteradas rapidamente, formando mosaicos de estruturas antrópicas e manchas arborizadas inseridas em contextos urbanos. Essas manchas verdes servem como importantes locais para conservação da biodiversidade, bem como para reprodução e forrageamento de espécies de aves migratórias. No entanto, os efeitos das características da paisagem urbana sobre as aves ainda são pouco entendidos na região Neotropical. Este estudo buscou entender os efeitos da urbanização sobre as aves da Mata Atlântica e conhecer as demandas de habitat das aves migratórias em áreas urbanas. Nesse contexto, o estudo teve quatro objetivos: 1) Avaliar as respostas das aves a um conjunto de atributos de cobertura do solo na paisagem urbana da cidade de São Paulo; 2) Descrever o habitat e a área de vida do tiranídeo migratório Myiodynastes maculatus solitarius em um parque urbano da Mata Atlântica; 3) Verificar se os tiranídeos migratórios têm fidelidade de sítio reprodutivo, e se sexo, habitat ou condição corpórea afetam a fidelidade de sítio; e 4) Revisar o desenvolvimento da ciência cidadã e sua contribuição para a ornitologia no Brasil, bem como conhecer, através dessa fonte de dados, a agenda migratória e os requisitos mínimos de habitat de quatro espécies de aves migratórias Neotropicais austrais no Brasil. Como resultado encontramos que na paisagem urbana o uso de áreas verdes pelas aves migratórias e residentes são afetadas negativamente pelo alto índice de ruído e a distância dos corpos d´água, e que ambos grupos de espécies são afetados de maneira similar. Além disso, os efeitos da urbanização podem afetar comportamentos das espécies, como por exemplo mudar o uso do espaço. Para M. m. solitarius encontramos uma área de vida média de 5.4 hectares em parque urbano em São Paulo, sendo que quanto mais estruturas antrópicas maior é a área explorada pelo indivíduo. Assim como o M. m. solitarius, alguns indivíduos de Tyrannus savana e Empidonomus varius, segundo nossos resultados, retornam após migração ao sítio reprodutivo. No entanto, o sexo e o tipo de ambientes (rurais vs. urbano) são características que afetam para essa fidelidade. Segundo dados de ciência cidadã, essas espécies e P. rubinus, apresentaram diferentes requerimentos de habitat com relação a tamanho de áreas verdes, sendo para M. m. solitarius 10 hectares, P. rubinus 5 hectares, E. varius 1 hectare e T. savana no mínimo ruas urbanizadas. A ciência cidadã, que contribuiu de forma importante para obtenção de respostas nos estudos desta tese, tem crescido no Brasil e gerado conhecimento sobre as espécies brasileiras. Os dados provenientes da ciência cidadã 14 mostram-se eficientes no fornecimento de informações relevantes em áreas urbanizadas, onde se concentram os observadores de aves que contribuem para as bases de dados. Para a implementação de iniciativas de conservação de forma mais efetiva, é necessário um maior foco em diferentes mosaicos da paisagem, sendo as áreas verdes urbanas partes dessa composição como refúgio para diversas espécies de aves. O desafio que se apresenta está em conhecer e conciliar as necessidades da sociedade humana e da biodiversidade para manter condições ecologicamente sustentáveis para ambos. Palavras-chave: conservação das aves, ecologia urbana, ciência cidadã, Tyrannidae 15 General abstract We live in an era, when the planet's natural landscapes are rapidly changing, forming mosaics of both anthropogenic and green patches within urban areas. These green patches serve as important sites for biodiversity, for instance supporting reproduction and foraging for migratory bird species. However, the effects of urban landscape features on birds are still poorly understood in the Neotropical region. This study sought to understand the effects of urbanization on birds in the Atlantic Rainforest and to evaluate habitat requirements of migratory birds in urban areas. In this context, the study had four objectives: 1) To evaluate the responses of birds to a set of ground cover attributes in the urban landscape of the city of São Paulo; 2) To describe the habitat and home range of the migratory tyrannid flycatcher Myiodynastes maculatus solitarius in an urban park in the Atlantic Forest; 3) To evaluate the breeding site fidelity of migratory tyrannid flycatchers, and whether sex, habitat or body condition affect site fidelity; and 4) To review the development of citizen science and its contribution to ornithology in Brazil and to use citizen science to study migration timing and the minimum habitat requirements of four austral migratory bird species in Brazil. As a result, we found that the use of urban green areas by migratory and resident birds is negatively affected by high noise levels and distance from water and that both groups of species are similarly affected. In addition, the effects of urbanization can affect the behavior of species, such as changing the use of space. For M. m. solitarius, we found an average home range of 5.4 hectares in an urban park in São Paulo and a positive relationship between area explored by an individual and number of anthropic structures. Similar to M. m. solitarius, some individuals of Tyrannus savana and Empidonomus varius return to the breeding site; however, sex and environment (rural vs. urban) affect their breeding site fidelity. According to citizen science data, these species and P. rubinus have different habitat requirements with respect to the size of green areas, being 10 hectares for M. m. solitarius, 5 hectares for P. rubinus, 1 hectare for E. varius and, at the minimum, a few meters wide for T. savana. Citizen science, the origin of a significantly proportion of the data in this thesis, has grown in Brazil and generated substantial knowledge about Brazilian bird species. Citizen science is efficient in providing relevant information from urbanized areas, where bird observers who contribute to the databases are concentrated. In order to implement conservation initiatives more effectively, a greater focus is needed on various landscape mosaics besides forest remnants, 16 including urban green areas that are also important to many bird species. The challenge is to understand and reconcile the needs of human society and biodiversity to maintain ecologically sustainable conditions for both. Keywords: bird conservation, citizen science, Tyrannidae, urban ecology 17 INTRODUÇÃO GERAL Vivemos numa era onde as paisagens naturais por todo planeta são alteradas rapidamente, formando mosaicos de origem antrópica e natural (Metzger 2006). Nos grandes centros urbanos esse fenômeno é ainda mais complexo, restando muitas vezes apenas manchas verdes inseridas na matriz urbana (Alberti et al. 2001). Nesse contexto, essas manchas verdes representam áreas de extrema importância para as aves residentes e migratórias, particularmente para espécies que têm maior capacidade de tolerar distúrbios de origem antrópica. No entanto, aves que usam áreas dentro ou próximo a cidades são susceptíveis a diversos desafios, como o aumento das taxas de predação, parasitismo de ninhos e escassez de recursos (Bolger 2001; Tewksbury et al. 2006), podendo assim diminuir as chances de sobrevivência dos indivíduos. Além disso, outros fatores inerentes aos centros urbanos podem também prejudicar a ocorrência e sobrevivência de aves nas manchas verdes, tais como os altos índices de ruído (Brumm 2004; Pena et al. 2017; da Silva et al. 2020), alta porcentagem de áreas impermeáveis (McKinney 2002; Evans et al. 2018; Souza et al. 2019) e densidade da população humana (Fontana et al. 2011). Portanto, o desafio que se apresenta está em conhecer e conciliar as necessidades da sociedade humana e da biodiversidade para manter condições ecologicamente sustentáveis para ambos. Grande parte do conhecimento sobre os efeitos da urbanização nas aves provém de estudos realizados na região temperada, sendo esse padrão de distribuição do conhecimento ainda mais acentuado quando se trata especificamente das aves migratórias (e.g., Blake & Karr, 1987; Rodewald & Bakermans, 2006; Loss et al. 2009; Husté & Boulinier 2011; Evans et al. 2018). Alguns desses estudos demonstraram efeitos negativos sobre as aves migratórias, tais como sobre aspectos reprodutivos das aves (Rodewald & Bakermans 2006; Rodewald & Shustack 2008) e alteração das datas de chegada e partida (Norris et al. 2004). Em contrapartida, outros estudos mostraram que manchas florestais urbanas podem oferecer vantagens para algumas espécies por prover recursos durante a migração (Matthews & Rodewald 2010). Um outro aspecto que tem sido abordado nos estudos do hemisfério Norte é que, de uma forma geral em comparação às espécies residentes, as aves migratórias são mais propensas a serem impactadas pela urbanização. Essa diferença pode se dever ao fato das aves migratórias serem, geralmente, mais especialistas em habitat, enquanto que as aves residentes têm uma capacidade melhor de responder às 18 flutuações de disponibilidade de recursos (Martin & Fahrig 2018; Ortega-Álvarez & MacGregor- Fors 2009). Na região Neotropical, especialmente no Brasil, poucos estudos avaliaram os efeitos da urbanização sobre as aves e quais variáveis ambientais e antrópicas podem ter maior influência sobre a riqueza e abundância das espécies (Fontana et al. 2011; Pena et al. 2017; Souza et al. 2019; da Silva et al. 2020). Ademais, apesar das estimativas serem de quase 200 espécies de aves que realizam movimentos migratórios no Brasil (Somenzari et al. 2018), pouco se sabe sobre ecologia e biologia dessas espécies, principalmente em ambientes antropizados. Ou ainda, se aves migratórias e residentes são impactadas de maneiras diferentes pela urbanização, como é o padrão encontrado para o Hemisfério Norte. Aves migratórias no Brasil A migração é o movimento direcional, regular e sazonal de um grande contingente de indivíduos de uma espécie, de uma determinada localidade para outra (Begon et al. 1990). Esse movimento anual das aves geralmente envolve um sítio de reprodução e outro de invernada ou repouso reprodutivo (Schüz et al. 1971; Webster et al. 2002) e permite que elas busquem recursos em localidades distantes (Sick 1983; Joseph & Stockwell 2000). No entanto, movimentos migratórios e uso das áreas de invernada ou reprodução podem ser fortemente impactados por alterações ambientais de origem antrópica, tais como a urbanização (Wilson et al. 2018; Bonnet- Lebrun et al. 2020). No planeta existem diversos sistemas migratórios conhecidos para as aves (Newton 2008). Na região Neotropical são encontradas espécies migrantes neárticos (Hayes 1995), no qual os indivíduos reproduzem na América do Norte e migram para o sul para passar o período de invernada (e.g. Newton, 2008; Greenberg & Marra, 2004); migrantes altitudinais, no qual qualquer espécie de ave ou população da espécie migra regularmente de uma altitude para outra (Hayes 1995; Barçante et al. 2017); e os migrantes neotropicais-austrais, onde as espécies se reproduzem na região continental temperada da América do Sul e migram para o norte do continente durante o inverno austral (Cueto & Jahn 2008). O sistema neotropical-austral é o terceiro maior sistema migratório em número de espécies conhecido (Chesser 1994) e também um dos menos estudados. Estimativas indicam que cerca de 220 espécies realizam esse tipo de movimento migratório (Chesser 1994). 19 Considerando todas as aves migratórias neotropicais austrais, cerca de um terço são da família Tyrannidae, porém pouco ainda se conhece sobre os diversos aspectos da história natural dessas espécies. Estudos sobre aves migratórias no Brasil começaram na década de 80 dando início ao entendimento sobre a migração no país (Sick 1983; Antas 1986; Stotz et al. 1992), porém apenas alguns estudos focaram em espécies da família Tyrannidae (Erickson 1982; Marini & Cavalcanti 1990). Nos últimos 20 anos apesar de novos estudos sobre aves migratórias da família Tyrannidae terem surgido (e.g. Joseph & Stockwell 2000; Joseph et al. 2003; Alves 2007; Areta & Bodrati 2008; Jahn et al. 2013; Guaraldo el al 2016; Bejarano & Jahn 2018) muitas espécies relativamente comuns, ou mesmo abundantes, têm sua biologia e ecologia pouco ou nada conhecidas. História natural e ecologia das aves migratórias neotropicais austrais em ambientes urbanos As aves migratórias neotropicais austrais são conhecidas por se reproduzirem principalmente em ambientes abertos (Chesser 1994; Chesser & Levey 1998; Bejarano & Jahn 2018), o que não significa necessariamente que também não sejam afetadas por eventual falta de recursos, tal como baixa cobertura vegetal e arbórea (Cockle et al. 2010; Amaya-Espinel & Hostetler 2019) ou mesmo a urbanização (Wilson et al. 2018). Por serem abundantes, amplamente distribuídas e muitas dependerem de áreas florestais (Fitzpatrick 2004), as aves da família Tyrannidae podem ser bons indicadores para entendermos se os padrões do efeito da urbanização encontrados no hemisfério norte sobre as aves migratórias também se aplicam aos migrantes neotropicais austrais. Para se entender os efeitos da urbanização sobre as aves migratórias, é essencial conhecer seus requerimentos ecológicos, como elas utilizam o habitat e o tamanho de sua área de vida. Com relação a hábitat e área de vida, ou seja, o espaço usado pelo indivíduo durante suas atividades diárias (Burt 1943, Brown & Orians 1970, Powell 2000), é esperado que atenda às necessidades básicas da espécie (Hutto 1985). Portanto, quando a disponibilidade de recursos na área de vida é afetada, pode ocorrer maior competição por recursos, diminuindo, por exemplo, as chances de sucesso reprodutivo das espécies (Greenberg 1986). Outro aspecto de história natural pouco conhecido ou documentado sobre essas espécies é se elas apresentam fidelidade aos sítios reprodutivos. Atualmente, entre as cerca de 220 espécies 20 de migrantes neotropicais austrais, apenas para 10 espécies há documentação de que podem retornar para o mesmo local de reprodução de anos anteriores após a migração (McNeil 1982; Rumboll et al. 2005; Brown et al. 2007; Jahn et al. 2009). Esse fenômeno é, possivelmente, muito mais difundido entre as espécies do que tem sido documento. De fato, existem benefícios claros para as aves apresentarem fidelidade ao local de reprodução, geralmente relacionados ao fato do indivíduo ter conhecimento prévio do local. Em geral, se um território apresenta recursos de boa qualidade, é presumivelmente mais vantajoso que a ave retorne ao local ao qual está familiarizado do que procurar e defender um novo território (Bollinger & Gavin 1989; Greenwood 1980). O conhecimento prévio da área dá ainda vantagem nas interações competitivas com outros indivíduos, pois os tornam mais capazes de defender seus locais de alimentação e nidificação contra possíveis competidores. No entanto, essas interações só são vantajosas quando a qualidade do ambiente compensa o retorno (Black 1996). Portanto, é importante entender em que condições as manchas verdes urbanas podem fornecer habitat para as aves migratórias e a manutenção da biodiversidade em longo prazo. Ciência cidadã no Brasil Entender os diversos fatores que afetam as aves residentes e migratórias em ambientes urbanos em um país como o Brasil, que tem uma rica biodiversidade e dimensões continentais, é oneroso e difícil. Nesse contexto emerge a ciência cidadã moderna, que permite a todo cidadão acadêmico ou não acadêmico contribuir com o conhecimento de diversos aspectos ecológicos importantes das aves (Silvertown 2009; La Sorte et al. 2017; McKinley et al. 2017). Dados de observação de aves são frequentemente colectados com ajuda do aplicativos e depositados em banco de dados online, como eBird e WikiAves, que fornecem oportunidade de dados para pesquisas acadêmicas. No Brasil, alguns estudos nos últimos 5 anos têm utilizado dados de ciência cidadã para conhecer diferentes aspectos da migração das espécies (Lees & Martin 2015; Lees 2016; Schubert et al. 2019; Somenzari et al 2018). A coleta de dados por cidadãos cientistas pode, portanto, ser uma importante ferramenta para o conhecimento das aves migratórias (Hochachka et al. 1999; Lees 2016), principalmente em centros urbanos onde as observações das espécies costumam ser mais acessíveis. 21 No Brasil, os efeitos da urbanização sobre as aves (Fontana et al. 2011; Toledo et al. 2011; Pena et al. 2017; Souza et al. 2019) ou o comportamento migratório das espécies (Lees & Martin 2015; Lees 2016; Jahn et al. 2016; Lees 2016; Somenzari et al. 2018; Bejarano & Jahn 2018; Schubert et al. 2019) são assuntos ainda pouco explorados, sendo que nenhum estudo investigou o impacto da urbanização nas aves migratórias neotropicais austrais. Esse é, portanto, o primeiro estudo que investiga o comportamento de aves migratórias neotropicais austrais em ambientes urbanos e seus impactos, e que sugere novas direções para estudos com aves migratórias que utilizam áreas verdes urbanas. Os estudos existentes sugerem que o comportamento e ecologia das aves são influenciados pela composição da paisagem, sendo que em paisagem urbana os efeitos podem ser ainda mais complexos. Assim, a hipótese central dessa tese é que a riqueza, ecologia e comportamento das aves migratórias neotropicais austrais são afetadas em diferentes níveis pela urbanização. Para testar essa hipótese, o estudo dessa tese objetivou entender como a urbanização pode afetar as aves migratórias neotropicais austrais que usam manchas verdes urbanas da Mata Atlântica brasileira. Esse objetivo geral foi dividido em quatro objetivos específicos: 1) Avaliar as respostas das aves a um conjunto de atributos de cobertura do solo na paisagem urbana da cidade de São Paulo; 2) Descrever o habitat e a área de vida do tiranídeo migratório Myiodynastes maculatus solitarius em um parque urbano da Mata Atlântica; 3) Verificar se os tiranídeos migratórios têm fidelidade de sítio reprodutivo, e se sexo, habitat ou condição corpórea afetam uma possível fidelidade de sítio; e 4) Revisar o desenvolvimento da ciência cidadã e sua contribuição para a ornitologia no Brasil, bem como conhecer, através dessa fonte de dados, a agenda migratória e os requisitos mínimos de habitat de quatro espécies de aves migratórias Neotropicais austrais no Brasil 22 Referências bibliográficas Alberti, M., E. Botsford, & Cohen, A. (2001). Quantifying the urban gradient: Linking urban planning and ecology. In: J. M. Marzluuf, R. Bowman and R. Donnelly (eds), Avian Ecology and Conservation in an Urbanizing Word. Kluwer Academic Publishers, Boston. Alves (2007). Sistemas de migrações de aves em ambientes terrestres no Brasil: exemplos, lacunas e propostas para o avanço do conhecimento. Revista Brasileira de Ornitologia, 15 (2) 231-238. Amaya-Espinel, J.D., & Hostetler, M.E. (2019). The value of small forest fragments and urban tree canopy for Neotropical migrant birds during winter and migration seasons in Latin American countries: A systematic review. Landscape and Urban Planning, 190: 103592. doi.org/10.1016/j.landurbplan.2019.103592 Antas, P.T.Z. (1987). Migração de aves no Brasil. Anais do II Encontro Nacional de Anilhadores de Aves. Editora UFRJ, Rio de Janeiro, Brazil. Areta, J.I. & Bodrati, A. (2008). Movimientos estacionales y afinidad filogenética de la Viudita Coluda (Muscipipra vetula). Ornitología Neotropical, 19: 201-211. Begon, M., Harper, J.L., & Townsend, C.R. (1990). Ecology: Individuals, Populations and Communities. 2nd Ed. Blackwell Scientific Publications. Bejarano, V., & Jahn, A. E. (2018). Relationship between arrival timing and breeding success of intra‐tropical migratory Fork‐tailed Flycatchers (Tyrannus savana). Journal of Field Ornithology, 89(2): 109-116. Black, J.M. (ed.) (1996). Partnerships in birds. The study of monogamy. Oxford, University Press. Blake, J.G., & Karr, J.R. (1987). Breeding birds of isolated woodlots: Area and habitat relationships. Ecology, 68(6): 1724–1734. Bolger, D. (2001). Urban birds: population, community, and landscape approaches, p. 155-177. In: J. M. Marzluff, R. Bowman, and R. Donnelly [EDS.], Avian ecology. Bollinger E.K. & Gavin T.A. (1989). The effects of site quality on breeding-site fidelity in bobolinks. The Auk, 106: 584-594. Bonnet-lebrun, A.S., Manica, A., & Rodrigues, A.S.L. (2020). Effects of urbanization on bird. Biological Conservation, 244: 108423. doi.org/10.1016/j.biocon.2020.108423. 23 Brown, J.L. & Orians G.H. (1970). Spacing patterns in mobile animals. Annual Review of Ecology and Systematics, 1: 239–262. Brown, C.E., Anderson, C.B., Ippi, S., Sherriffs, M.F., Charlin, R., Mcgehee, S. & Rozzi, R. (2007). The autecology of the Fio-Fio (Elaenia albiceps Lafresnaye & D´Orbigny) in subantarctic forests of the Cape Horn Biosphere Reserve, Chile. Anales Instituto Patagonia (Chile), 35(2): 29-40. Brumm, H. (2004). The impact of environmental noise on song amplitude in a territorial bird. Journal of Animal Ecology, 73, 434–440 and conservation in an urbanizing world. Kluwer Academic, New York, NY. Burt, W.H. (1943). Territoriality and home range concepts as applied to mammals. Journal of Mammalogy, 24: 346–352. Chesser, R.T. (1994), Migration in South America: an overview of the austral system. Bird Conservation International, 4: 91-107. Chesser T. & Levey, D.J. (1998). Austral migrants and the evolution of migration in New World birds: diet, habitat, and migration revisited. American Naturalist, 152: 311-319. Cockle, K.L., Martin, K. & Drever, M. C. (2010). Supply of tree-holes limits nest density of cavity-nesting birds in primary and logged subtropical Atlantic forest. Biological Conservation, 143: 2851-2857 Cueto, V.R., & Jahn, A.E. (2008). Sobre la necesidad de tener un nombre estandarizado para las aves que migran dentro de América del Sur. Hornero, 23(1): 1-4. Erickson, H.T. (1982). Migration of the Fork-tailed Flycatcher through southeastern Brazil. America Birds, 36(2): 136-138. Evans, B.S., Reitsma, R., Hurlbert, A.H., & Marra, P.P. (2018). Environmental filtering of avian communities along a rural‐to‐urban gradient in Greater Washington, DC, USA. Ecosphere, 9(11): e02402. 10.1002/ecs2.2402 Fitzpatrick, J. W. (2004). Family Tyrannidae (Tyrant-flycatchers). In: Del Hoyo, J.; Elliot, A.; Christie, D. Handbook of the birds of the World: Cotingas to Pipits andWagtails. Vol. 9. Barcelona: Lynx Editions, 170-462. Fontana, C.S., Burger, M.I. & Magnusson, W.E. (2011). Bird diversity in a subtropical South- American City: effects of noise levels, arborisation and human population density. Urban Ecosystems, 14: 341-360. 24 Greenberg, R. (1986). Competition in migrant birds in the nonbreeding season. Current Ornithology 3: 281–307. Greenwood, P. J. (1980). Mating systems, philopatry and dispersal in birds and mammals. Animal behaviour, 28(4): 1140-1162. Guaraldo, A.C., Kelly J.F, Marini, M.A. (2016). Contrasting annual cycles of an intratropical migrant and a tropical resident bird. Journal of Ornithology, 157: 695–705. Hayes, F.E. (1995). Definitions for migrant birds: what is a Neotropical migrant? The Auk 112: 521-523. Hochachka, W.M., Wells, J.V., Rosenberg, K.V., Tessaglia-Hymes, D.L. & Dhondt, A.A. (1999). Irruptive migration of common redpolls. The Condor, 101: 195–204. Hutto, R.L. (1985). Habitat selection by nonbreeding, migratory land birds, p. 455–476. In: Cody M.L. (ed.). Habitat selection in birds. New York: Academic Press Husté, A. & Boulinier, T. (2011). Determinants of bird community composition on patches in the suburbs of Paris, France. Biological Conservation, 144(1): 243–252. Jahn, A.E., Cueto, V.R., Sagario, M.C., Mamani, A.M., Vidoz, J.Q., Casenave, J.L. & DI Giacomo, A.G. (2009). Breeding and winter site fidelity among eleven Neotropical austral migrant bird species. Ornitologia Neotropical, 20: 275–283. Jahn, A.E., Levey, D.J., Cueto V.R., Ledezma, J.P., Tuero, D.T., Fox, J.W. & Masson, D. (2013). Long-distance bird migration within South America revealed by light-level geolocators. The Auk, 130: 223-229 Jahn, A.E., Seavy, N.E, Bejarano, V., Guzmán, M.B., Provinciato, I.C., Pizo, M.A. & MACPHERSON, M. (2016). Intra-tropical migration and wintering areas of Fork-tailed Flycatchers (Tyrannus savana) breeding in São Paulo, Brazil. Revista Brasileira de Ornitologia, 24(2). Joseph, L., Wilke, T. & Alpers, D. (2003). Independent evolution of migration on the South American landscape in a long-distance temperate-tropical migratory bird, Swainson’s Flycatcher Myiarchus swainsoni. Journal of Biogeography, 30: 925-937. Joseph, L. & Stockwell, D. (2000). Temperature-based models of the migration of Swainson's Flycatcher (Myiarchus swainsoni) across South America: A new use for museum specimens of migratory birds. Proceedings of the Academy of Natural Sciences of Philadelphia, 150: 293-300. 25 La Sorte, F.A., Fink, D., Blancher, P.J., Rodewald, A.D., Ruiz-Gutierrez, V., Rosenberg, K.V., Hochachka, W.M., Verburg, P.H. & Kelling S. (2017). Global change and the distributional dynamics of migratory bird populations wintering in Central America. Glob Chang Biol. https://doi.org/10.1111/gcb.13794 Lees, A.C. (2016). Evidence for longitudinal migration by a “sedentary” Brazilian flycatcher, the Ash-throated Casiornis. Journal of Field Ornithology, 87(3): 251-259. Lees, A.C. & Martin, R.W. (2014). Exposing hidden endemism in a Neotropical forest raptor using citizen science. Ibis: 157, 103–114. doi.org/10.1111/ibi.12207 Loss, S.R., Ruiz, M.O. & Brawn, J.D. (2009). Relationships between avian diversity, neighborhood age, income, and environmental characteristics of an urban landscape. Biological Conservation, 142: 2578–2585. Marini, M.Â. & Cavalcanti, R.B. (1990). Migrações de Elaenia albiceps chilensis e Elaenia chiriquensis arbivertex (Aves: Tyrannidae). Boletim do Museu Paraense Emílio Goeldi 6: 59-66. Martin, A.E. & Fahrig, L. (2018). Habitat specialist birds disperse farther and are more migratory than habitat generalist birds. Ecology, 99 (9): 2058–2066. doi.org/10.1002/ecy.2428 Matthews, S. & Rodewald, P. (2010). Urban forest patches and stopover duration of migratory Swainson’s thrushes. Condor, 112: 96-104. Mckinley, D.C., Miller-Rushing, A.J., Ballard, H.L., Bonney, R., Brown, H., Cook-Patton, S.C., Evans, D.M., French, R.A., Parrish, J.K., Phillips, T.B., Ryan, S.F., Shanley, L.A., Shirk, J.L., Stepenuck, K.F., Weltzin, F.G., Wiggins, A., Boyle, O.D., Briggs, R.D., Chapin III, S.F.C., Hewitt, D.A., Preuss, W.P. & Soukup M. A. (2017). Citizen science can improve conservation science, natural resource management, and environmental protection. Biological Conservation 208: 15-28. Mcneil, R. (1982). Winter resident repeats and returns of austral and boreal migrant birds banded in Venezuela. Journal Field Ornithology, 53(2): 125-132. Metzger, J.P. (2006). Como lidar com regras pouco óbvias para conservação da biodiversidade em paisagens fragmentadas. Natureza & Conservação, 4:11-23. Newton, I. (2008). The migration ecology of birds. Academic Press, London. 26 Norris, R.D., Marra, P.P., Kyser, T.K., Sherry, T.W., & Ratcliffe, L.M. (2004). Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Biological Sciences, Vol. 271, 1534: 59-64 Pena, J.C.C., Martello, F., Ribeiro, M.C., Armitage, R.A., Young, R.J. & Rodrigues, M. (2017) Street trees reduce the negative effects of urbanization on birds. PLoS ONE 12(3). Powell, R.O. (2000). Animal home ranges and territories and home range estimators. In: Pearl M.C. (ed.). Research techniques in animal ecology: controversies and consequences. New York: Columbia University Press. Ortega-Álvarez, R. & Macgregor-Fors, I. (2009). Living in the big city: Effects of urban land-use on bird community structure, Landscape and Urban Planning, 90:189–195 Rodewald, A.D. & Bakermans, M.H. (2006). What is the appropriate paradigm for riparian forest conservation? Biological Conservation, 128: 193–200. Rodewald, A.D. & Shustack, D.P. (2008). Urban flight: understanding individual and population- level responses of Nearctic-Neotropical migratory birds to urbanization. Journal of Animal Ecology, 77: 83-91 Rumboll, M., P. Capllonch, Lobo R. & Punta G. (2005). Sobre el anillado en la Argentina: recuperaciones y recapturas. Nuestras Aves 50: 21–24. Sick, H (1983) Migrações de aves na América do Sul Continental. Publicação Técnica no. 2, CEMAVE – Instituto Brasileiro de Desenvolvimento Florestal, Brasília, DF. Schubert, S.C., Manica, L.T. & Guaraldo, A.C. (2019): Revealing the potential of a huge citizen- science platform to study bird migration, Emu - Austral Ornithology, DOI: 10.1080/01584197.2019.1609340 Silva, B.F., Pena, J.C, Viana-Junior, A.B, Vergne, M. & Pizo, M.A. (2020). Noise and tree species richness modulate the bird community inhabiting small public urban green spaces of a Neotropical city. Urban Ecosystems, DOI: 10.1007/s11252-020-01021-2. Silvertown, J. (2009). A new dawn for citizen science. Trends in Ecology & Evolution 24(9): 467-471. Somenzari, M., et al. (2018) A review of Brazilian migratory birds. Pap. Avulsos Zool. 58: 1– 66. Souza, F.L., Valente-Neto, F., Severo-Neto, F., Bueno, B., Ochoa-Quintero, J.M., Laps, R.R., Bolzan, F. & Roque, F.O. (2019). Impervious surface and heterogeneity are opposite drivers to maintain bird richness in a Cerrado city. Landscape and Urban Planning 192: 103643. 27 Stotz, D.F., Bierregaard, R.O., Cohn-Haft, M., Petermann, P., Smith, J., Wittaker, A. & Wilson, S.V. (1992). The Status of North American Migrants in Central Amazonian Brazil. The Condor, 94 (3): 608–621, DOI: 10.2307/1369246 Tewksbury, J.J., Garner, L., Garner, S., Lloyd, J.D., Saab, V. & Martin T.E. (2006). Tests of landscape influence: nest predation and brood parasitism in fragmented ecosystems. Ecology 87: 759-768 Toledo, M.C.B., Donatelli, R.J. & Batista, G.T. (2011). Relation between green spaces and bird community structure in an urban area in Southeast Brazil. Urban Ecosyst, 15:111-131. Webster, M.S., Marra, P.P., Haig, S.M., Bensch, S. & Holmes, R.T. (2002). Links between worlds: unraveling migratory connectivity. Trends in Ecology & Evolution, 17: 76-83. Wilson, S., Saracco, J.F., Krikun, R., Flockhart, D.T.T., Godwin, C., and Foster, K.R. (2018). Drivers of demographic decline across the annual cycle of a threatened migratory bird. Scientific Reports, 8:7316. Doi: 10.1038/s41598-018-25633-z http://dx.doi.org/10.1038/s41598-018-25633-z 28 CAPÍTULO 1 . 29 Noise level and distance to water drive resident and migratory bird species richness within a Neotropical megacity Abstract A large body of evidence indicates that urbanization profoundly affects ecological communities, but the extent to which patterns are generalizable across regions, such as in the Neotropics, remains unclear. We examined responses of migratory and resident birds to human disturbance and habitat attributes in São Paulo, Brazil, a tropical megacity in South America. In 2017-2018, we surveyed birds across 31 landscapes distributed across the urban landscape and evaluated competing models that included five non-correlated variables explaining variation in species richness: ambient noise level, distance to water, tree cover, human population size, and impervious surface. We recorded 142 bird species, 128 of which were resident and 14 migratory. Richness of both resident and migratory birds declined with increasing noise level and distance to water, which best explained variation in bird communities among the sampled landscapes. Although resident and migratory birds presented similar response patterns to local and landscape attributes, noise level was the best predictor of migratory species occurrence, whereas distance to water best explained the occurrence of resident species. Our results suggest that, although tree cover is important to biodiversity in urbanized landscapes, proper management of urban water bodies and reduction of noise levels are also essential to maintaining avian diversity within tropical urban areas and suggest novel avenues for future research in tropical urban ecology. Keywords: biodiversity, urbanization, urban parks, Atlantic Forest, South America 30 1. Introduction There is a growing urban footprint across the planet, with over half of the world’s human population now living in cities (United Nations, 2018). One of the effects of urban expansion is the transformation of landscapes into a mosaic of patches with different land uses embedded within an urban-dominated matrix. This landscape-level conversion alters the functioning of ecosystem and ecological processes (Grimm, Grove, Pickett, & Redman, 2000), contributing to biodiversity loss and environmental homogenization (Chace & Walsh, 2006). Therefore, the challenge of the 21st Century is to reconcile the needs of human society and those of biodiversity to maintain conditions that are ecologically sustainable for both. To be effective, such efforts require information about which landscape characteristics drive the maintenance of biodiversity within urban green spaces (Aronson et al., 2017; Lepczyk et al., 2017). Perhaps no other taxonomic group within cities has been well studied as birds (Palacio, Ibañez, Maragliano, & Montalti, 2018). Birds are relatively easy to detect and survey, are often sensitive to disturbance, and are generally effective sentinels of environmental change (MacGregor-Fors, 2008; McKinney, 2002; Barbosa, Knogge, Develey, Jenkins, & Uezu, 2017). Among the documented proximate drivers that shape urban bird communities are: changes in vegetation cover, floristics, and microclimate (Chace & Walsh, 2006; Rodewald & Shustack, 2008; Rodewald, Shustack, & Hitchcock, 2010; Lowry, Lill, & Wong, 2012), abundance of predators and brood parasites (Rodewald, Kearns, & Shustack, 2011), urbanization and the spatial distribution of green patches (Husté & Boulinier, 2011), and food resource availability (Rodewald et al., 2011; Lowry et al., 2012). Thus, urbanization can profoundly impact bird community composition and structure. In particular, urbanization has been linked both to declines of sensitive species and to positive effects on synanthropic or non-native species (Ortega-Alvarez & MacGregor-Fors, 2009). Although species richness of birds within cities tends to increase with tree cover (Emlen, 1974; Chace & Walsh, 2006; MacGregor-Fors, 2008), richness typically declines with impervious surface area (McKinney, 2002; Evans, Reitsma, Hurlbert, & Marra, 2018; Souza et al., 2019), density of buildings (Palacio et al., 2018), proximity to urban parks (Loss, Ruiz, & Brawn, 2009), ambient noise level (Brumm, 2004; Pena, Martello, Ribeiro, Armitage, Young & Rodrigues, 2017), and human population density (Fontana, Burger, & Magnusson, 2011). 31 One of the most consistent patterns reported in urban bird studies from temperate regions is the negative relationship between urbanization and migratory bird abundance (Loss et al., 2009; Husté & Boulinier, 2011; Evans et al., 2018). Migratory birds that breed in temperate latitudes are thought to be more sensitive than resident birds (i.e., which do not migrate) to landscape composition and configuration, such as patch size, forest cover, edge effects and connectivity (e.g., Blake & Karr, 1987; Rodewald & Bakermans, 2006). Compared to residents, migratory birds are also more likely to be habitat specialists, since residents presumably have a better capacity to respond to fluctuations in resource availability and habitat quality (Martin & Fahrig, 2018). Additionally, migratory birds generally have lower reproductive potential (i.e., are usually single-brooded) and tend to be more vulnerable to nest predation (Robinson, Thompson III, Donovan, Whitehead, & Faaborg, 1995; Rodewald et al., 2011), whereas resident birds tend to be better at exploiting anthropogenic resources, are more tolerant of human disturbance, and are more resistant or resilient to nest predation (Blair, 2001; Ortega-Álvarez & MacGregor-Fors, 2009). Thus, understanding how the quality and configuration of urban green spaces can limit the richness of migratory bird species during breeding season is key to informing conservation planning for those species (Lepczyk et al., 2017). However, due to the scarcity of research on the urban ecology of birds at tropical latitudes, we still know little about the urban ecology of tropical birds and whether they respond in similar ways as species that breed at temperate latitudes. Given that the tropics harbor the highest levels of bird species on the planet, a sound understanding of the mechanisms that shape tropical urban avian communities is essential to effectively conserve their populations on an increasingly urbanized planet. In particular, research is needed on the urban ecology of migratory birds at tropical latitudes, to understand which landscape characteristics determine their use of urban habitats during migration and winter (Amaya-Espinel & Hostetler, 2019). To contribute to filling this gap in our knowledge, we assessed the responses of birds to a suite of land cover attributes across the urban landscape of São Paulo, a tropical Brazilian megacity. Based on what has been previously reported about the effects of urbanization on bird assemblages, we hypothesized that: a) tree cover, ambient noise level, distance to water, human population density and urban structures act as filters on avian communities in São Paulo’s urban green spaces, and b) these factors affect migratory and resident birds differently. We expected that avian species richness would be positively related to tree cover and negatively related to 32 ambient noise level, distance to water, human population density, and area of urban structures. We also expected that the response of migratory birds to these variables would be stronger than that of residents. 2. Material and methods 2.1 Study area The study was conducted in the city of São Paulo, in southeastern Brazil (S 23º32′51″; W 46°38′10). The city is embedded within the Atlantic Forest biome, which has less than 16% of its original cover remaining and is today primarily composed of relatively small patches, most of 50 ha or less in size (Ribeiro, Metzger, Martensen, Ponzoni, & Hirota, 2009). São Paulo is one of the most populous cities in the world, where more than 12 million people occupy an area of 1,521 km² (IBGE, 2018). Even though urban structures dominate São Paulo’s land cover, the city contains numerous small parks and is bordered by two large blocks of forest, the Serra da Cantareira to the northwest and the Serra do Mar to the southwest. Land cover in São Paulo city is comprised of approximately 32% tree cover, 51% urban structures (e.g., buildings and impervious surface), 10% lawn and 7% water (Laboratório de Silvicultura Urbana, 2010). 2.2 Site selection and attributes Landscape composition metrics were calculated using land cover maps made available by Laboratório de Silvicultura Urbana (2010), which were generated from satellite imagery (infrared orthophotos with 5-m resolution) of the year 2010 data collection (UTM-WGS84 zone 23S). The land cover maps include the following cover classes: trees, lawn, water, impervious surfaces (streets, avenues, and concrete), and buildings. We then selected 31 sampling sites located in green spaces, at least 2 km apart, distributed across the city and which represent the range of green space sizes present in the city: 11 to 73% tree cover within a 1 km buffer at the center of the green space. Three sampling sites were located in large public protected areas of continuous forest (numbers 11, 12 and 13 in Fig. 1) and 28 were located urban parks and smaller green spaces (locally known as praças – Fig. 2). 33 Figure 2: Location of 31 point count sites in the city of São Paulo, Brazil. Circle size represents noise level and color hue of each circle represents distance to water. The number next to each circle represents the green space referred to in Appendix A1. Tree cover, lawn, water and urban structures (impervious surface and building cover) is also shown. Map classification is from Laboratório de Silvicultura Urbana (2010). Figure 1: Contextual photos representing the essential nature of the landscape of São Paulo city. Yellow squares represent the locality where the picture was taken; A1, B1 and C1 are Google Earth images and A2, B2 and C2 are pictures by KVCB. A - Ecológico do Tietê Park, a typical Brazilian green space embedded among urban structures and with a lake and trails; B – Ibirapuera Park, an urban green space with more trees in the landscape and smaller population around; and C – Praça Comendador Vargas – a typical small green space called praça (see Fig.2, map location numbers 1, 6 and 32). 34 At each sampling site, we quantified the percent of land cover in landscape (tree, lawn, and impervious surface; Fig. 1) and human population density (extracted from GeoSampa; www.geosampa.prefeitura.sp.gov.br). These variables were selected because they have been shown to affect urban bird communities in previous studies (Emlen, 1974; Chace & Walsh, 2006; MacGregor-Fors, 2008; McKinney, 2002; Fontana et al., 2011; Evans et al., 2018; Amaya- Espinela & Hostetler, 2019; Souza et al., 2019). We also measured distance (meters) to the nearest water body, up to any distance (log10 transformed), and ambient noise level. The latter was measured at the center point of the sample site and it refers to the mean noise level recorded during three visits in the center of the green area where we did the survey. Ambient noise was recorded for 2-min during each visit (for a total of 6 min at each sample point), using the ‘Sound Meter’ application on a smartphone (Asus Zenfone 3 Max 5.2). This app measures the noise level in decibels and displays a graphic the last 30 seconds, with the minimum, average and maximum ambient noise from 0 to 95 db. We used the average value generated by the app for each of the three visits and made a weighted average of that value, which is a proxy for ambient noise. To ensure consistency, we used the same protocol and cell phone equipment across all point count (Zamora, Calafate, Cano, & Manzoni, 2017) and calibrated our ambient noise measurements to avoid errors (Maisonneuve, Stevens, Niessen, & Steels, 2009). 2.3 Bird surveys The bird community in this city is composed of both residents and migrants from three migratory systems: a) breeding Neotropical austral migrants, which breed at south-temperate latitudes and spend the non-breeding season closer to the Equator (Cueto & Jahn, 2008); b) breeding altitudinal migrants, which migrate up and down mountain slopes (Barçante, Vale, & Alves, 2017); and c) non-breeding Nearctic-Neotropical migrants, which breed at north- temperate latitudes and spend the non-breeding season in the Neotropics (Joseph, 1996). The most recent report from the municipality of São Paulo shows that 464 bird species have been recorded in the city (SVMA, 2018). Birds were surveyed between October 2017 and January 2018 (spring/summer), which represents the breeding season of most birds in southeastern Brazil, when birds are most active and singing, and when most migratory species are in the region. We conducted a point count in each landscape, which consisted of one 20-minute fixed-radius count (Bibby, Burgess, & Hill, http://www.geosampa.prefeitura.sp.gov.br/ 35 1992). The location of each count was recorded in UTM (Datum WGS84) using a GPS receiver. Each point count was conducted three times at each sample location and all point counts were conducted in the early morning (7:00 to 10:00) within a 20 to 30-day interval, to increase the chances of species detection. We alternated the order in which each point count was conducted, to avoid bias in detection of species during the counts. Counts were always conducted on weekdays (excluding holidays) to minimize the effect of visitors, since parks usually have more visitors on weekends. All surveys were conducted by KVCB, who has extensive experience identifying birds in the region by sight and sound. Any records that were suspicious, such as unconfirmed species or individuals that were likely captive/pets, were not included in the analysis. 2.4 Statistical analysis We first identified multi-collinearity between explanatory variables (i.e., building cover, impervious surface area, lawn area, tree cover, human population density, distance to water, and ambient noise level) using Pearson’s correlation coefficient (r), and excluded those that were highly correlated (r > 0.7; see Supplementary Material S1 and S2). After this step, we constructed candidate models with the five remaining and uncorrelated variables. We developed a multi-scale approach to relate bird responses to our environmental and landscape attributes (impervious surface area, tree cover, and human population density). The evaluated spatial extents were 50, 250, 500, 750 and 1,000 m around the sample locations within each of our 31 point count sites. Because the spatial scale at which landscape modification most strongly influences species distributions and richness remains unclear for many species and taxa worldwide (Jackson & Fahrig, 2015), we used model selection to identify the scale at which each of our explanatory variables best explained migratory and resident species richness (Burnham & Anderson, 2002 - Supplementary Material S3). After this step, we selected 1,000 m radius around the sample point, as the difference between scales were not strong and this spatial extent best explained the effect of most explanatory variables. Furthermore, 1,000 m is a radius size that is often used to understand the impact of urbanization on bird community dynamics (e.g., Stratford & Robinson, 2005; Loss et al, 2009; Evans et al, 2018; see Supplementary Material S3). We evaluated a list of competing models (i.e., different Generalized Linear Models; GLMs) explaining variation in species richness using Akaike Information Criterion corrected for 36 small sample sizes (AICc). A total of 17 models, which were composed by a single-model, adding model with combination of two variables (impervious surface area, tree cover, human population density, distance to water, and ambient noise level), one model with the anthropogenic variable (impervious surface area, human population density, and ambient noise level), and a null model were used to explain patterns of resident and migratory bird richness. The difference between the AICc of each model and the best model (i.e., with the lowest AICc; ΔAICc) was calculated for each competing model. Models having a ΔAICc < 2.0 were considered equally plausible (Burnham and Anderson, 2002). We also calculated the weight of evidence (wAICc) for each competing model, which is the sum of the weights of the models in which the variable appears (Burnham & Anderson, 2002; Barbosa et al., 2017). All analyses were conducted using program R version 3.4.1 (R Core Team, 2017). 3. Results Approximately one-third (142 species from 48 families) of all bird species already recorded in São Paulo (464 species – SVMA, 2018) were detected at our 31 sample sites. Of the 128 resident species recorded, 29 are endemic to the Atlantic Forest. Most species were insectivores (63), followed by frugivores (24), omnivores (23), carnivores (16), granivores (10) and nectarivores (6). Most species foraged in the canopy (45) and/or mid-story (40), with fewer foraging in the understory (26), on the ground (26) or in water (19). Fourteen species were Neotropical austral or altitudinal migrants that breed in the study area (for more details, see Appendix B1), with most migratory species belonging to the Tyrannidae (43% of species) and Turdidae (18%). Resident bird species richness across point count sites varied from 7 to 49 (mean = 22.1; SD = 9.9) and migratory bird species richness varied from 0 to 10 (mean 4.2; SD=2.1 species/point). The average ambient noise level at each sample site varied from 19.8 to 48.8 db, and the distance from each point count to a body of water varied from 1 to 1,500 meters. 37 The model that combined distance to water and noise level best explained variation in resident (wAIC = 0.70) and migrant (wAIC = 0.43) species richness (Fig. 3). Species richness was negatively related to both noise level and distance to water (Table 1). Although tree cover was not among the selected models, both resident and migratory species richness were positively related to it (Fig. 4). In terms of the contribution of explanatory variables (weight of evidence), distance to water had a sum of Akaike weight of 0.96 and noise level had a weight of 0.73 for resident bird species. For migratory birds, noise level had a sum of Akaike weight of 0.79 and distance to water had a weight of 0.54. The sum of the weights of other explanatory variables for resident species were: 0.05 - tree cover, 0.23 - impervious surface, and 0.01- human population density, and for migratory species they were: 0.06 - tree cover, 0.26 - impervious surface, and 0.07 - human population density (Fig. 5). Figure 4: Influence of noise level index and distance to water (meters, log10 transformed) on resident and migratory bird species richness for 31 green areas within the city of São Paulo, Brazil. Tree cover (%) was calculated within a 1 km radius around each point count site. Gray areas represent 95 % confidence intervals. Figure 0-3: Patterns obtained in the multivariate models assessing the effects of exposure to ambient noise and distance to water on the richness of resident and migratory bird species in the city of São Paulo, Brazil. The bright colors represent higher response values. 38 .Table 1: Model performance using Akaike´s Information Criterion on multiple regression to explain resident and migratory bird species richness as a function of different environmental variables within green areas in the megacity of São Paulo, Brazil. For the best models (ΔAICc < 2.0), we present AICc - Akaike Information Criterion corrected for small sample sizes, ΔAIC and weight of evidence (wAIC). Explanatory variables measured within a 1,000 m buffer are: Tree cover – percent tree cover; population – human population density; impervious – percent impervious surface (asphalt and concrete); water - distance from the point count site to the closest lake or river; noise – ambient noise level recorded during the point count; null – uncertainty of the relationship between selected variables and species presence. Response variable Model AICc ΔAIC df wAIC R es id en t b ir d s p ec ie s ri ch n es s ~ water + noise 211.34 0 4 0.6966 ~ impervious + water 213.68 2.3 4 0.2171 ~ tree cover + water 216.82 5.5 4 0.0450 ~ impervious + noise 219.34 8.0 4 0.0128 ~ noise 220.16 8.8 3 0.0085 ~ impervious + noise + population 221.14 9.8 5 0.0052 ~ tree cover + noise 221.42 10.1 4 0.0045 ~ population + water 221.79 10.4 4 0.0038 ~ population + noise 222.16 10.8 4 0.0031 ~ impervious 223.86 12.5 3 0.0013 ~ tree cover + impervious 224.98 13.6 4 0.0010 ~ population + impervious 225.86 14.5 4 0.0010 ~ tree cover 226.55 15.2 3 0.0010 ~ tree cover + population 227.26 15.9 4 0.0010 ~ water 227.28 15.9 3 0.0010 ~ null 232.64 21.3 2 0.0010 ~ population 233.43 22.1 3 0.0010 Figure 0-5: Explanatory power of environmental variables in explaining bird species richness in green spaces in the city of São Paulo, Brazil. The weight of evidence (wAIC) is the sum of the weights of the models in which the variable appears 39 M ig ra to ry b ir d s p ec ie s ri ch n es s ~ water + noise 117.66 0 4 0.4305 ~ noise 120.09 2.4 3 0.1281 ~ impervious + noise 120.16 2.5 4 0.1234 ~ impervious + water 120.53 2.9 4 0.1028 ~ impervious + noise + population 121.44 3.8 5 0.0652 ~ population + noise 121.85 4.2 4 0.0531 ~ tree cover + noise 121.97 4.3 4 0.0500 ~ impervious 123.82 6.2 3 0.0198 ~ population + impervious 125.66 8.0 4 0.0079 ~ tree cover + population 125.78 8.1 4 0.0074 ~ tree cover + water 126.57 8.9 4 0.0050 ~ population + water 128.29 10.6 4 0.0021 ~ water 129.02 11.4 3 0.0015 ~ tree cover 129.10 11.4 3 0.0014 ~ tree cover + population 130.49 12.8 4 0.0010 ~ null 130.52 12.9 2 0.0010 ~ population 132.05 14.4 3 0.0010 4. Discussion Our findings provide mixed support for our original expectations. Contrary to other studies from north-temperate (e.g., Emlen, 1974; Chace & Walsh, 2006; Loss et al., 2009) and South American cities (e.g., Fontana et al., 2011 Leveau, 2013; Pena et al., 2017), avian species richness was only weakly related with tree cover in São Paulo’s green spaces. Instead, patterns of species richness in urban parks in the city of São Paulo were best explained by, and negatively related to, distance to water and ambient noise, as shown in prior research in South American cities (Fontana et al., 2011; Pena et al., 2017). To the best of our knowledge, ours is the first study to show that urban Neotropical bird species richness is related to distance to water, but see Faggi and Perepelizin (2006), who found that urban water bodies may contribute to bird species richness in Argentina. Overall, we found little evidence that migratory birds were more sensitive to these variables than residents. 4.1 Urban green spaces as biodiversity refuges Urbanization can exclude more sensitive bird species (Jokimäki, Jukkab, & Marja-Liisaa, 2018), but small green spaces may serve as refuges for birds within the urban matrix, especially those that are less sensitive to human disturbance (Aronson et al., 2017; Lepczyk et al., 2017; Barbosa et al., 2017). Green spaces within Neotropical urban areas likely play an important role 40 as a refuge for birds in megacities as São Paulo. For instance, in isolated parks we recorded >20% (>30 species) of the total number of bird species that occur in São Paulo (Fig. 1, numbers 26, 5, 7), including 35% (five species) of the number of migratory species that occur in the city. Species differ in regards to sensitivity to urbanization (Stotz, Fitzpatrick, & Parker III, 1996), and their use of green spaces is related to their traits (Pena et al., 2017). For example, foraging behavior or diet can be decisive to successfully living in the most highly urban areas (Husté & Boulinier, 2011; Pena et al., 2017). Notably, 44% of the bird species we recorded in urban green spaces were insectivorous, which may be related to the greater resilience that certain insectivores display to increasing levels of urbanization (Trollope, White, & Cooke, 2009). Urbanization may also alter the temporal dynamics of resource availability, influencing bird community composition and dynamics across space and time (McKinney, 2002). Future studies on both the spatial and temporal foraging patterns of birds relative to food resource availability across São Paulo’s urban gradient may help explain the patterns we detected. 4.2 The influence of noise level and water proximity on urban birds We found that occurrence of both resident and migratory birds was well explained by a combination of ambient noise level and distance to water. However, the sum of weights of those models differed between the two groups, with resident species occurrence having a stronger association with distance to water and occurrence of migratory species being more strongly associated with noise level. Our findings corroborate those of other studies in South America, in which noise was shown to negatively impact bird species richness in urban green spaces (Fontana et al., 2011; Pena et al., 2017). Moreover, a growing body of evidence has shown that acoustic environments or soundscapes can affect the distribution, abundance, and activity of birds (Brumm, 2004; Pena et al., 2017; Narango & Rodewald, 2015). Anthropogenic noise is primarily composed of low frequencies in the 0 to 3 kHz range (Wood & Yerezinac, 2006; Goodwin & Shriver, 2011), such that species that vocalize within this frequency range may be affected by acoustic masking (Narango & Rodewald, 2015; Roca et al., 2016). Over the long-term, anthropogenic noise can act as a novel selective pressure, potentially favoring habitat generalists over specialists (McKinney, 2002), thereby contributing to low species richness in urban areas. In our study region, more than 12 million people live and work, 41 and roughly 8 million motorized vehicles are on the streets (IBGE, 2018), such that even inside of the parks in the central region of the city, or in praças surrounded by avenues, the noise level can reach higher level. The consistently lower bird species richness detected in the city center further suggests that noise level may negatively influence the use of parks by birds. Similar to noise level, distance to water explained much of resident and migratory bird richness in São Paulo’s urban green spaces. The apparent preference of species to be closer to water is not necessarily due to their use of water as a resource; rather, it may be because water supports or ameliorates other physiological demands related to heat and water balance (Karr & Freemark, 1983) or food resource availability (Faggi & Perepelizin, 2006; Leveau, 2018). The heat island effect created by the city of São Paulo (Tarifa & Armani, 2000; Ferreira et al., 2012) is typical of large cities (Trusilova, Jung & Churkina, 2009). Such urban heat may have an indirect effect on birds, impacting the resources they depend upon, such as arthropods abundance and plant growth (Leveau, 2018). Urban water bodies and green spaces also help regulate a region’s microclimate (Bolund & Hunhammar, 1999), which may attract birds seeking a favorable thermal gradient. This may potentially explain species occurrence at Cidade Toronto Park (Fig 2 – number 15), which is surrounded by a high area of concrete, but which has a lake and holds six of the 14 migratory species we detected, and 36 of 49 resident species were detected. The positive relationship between distance to water and species richness may also be a product of higher food resource abundance for insectivores closer to water (Leveau, 2018). Water is essential for the reproduction of many arthropods, such that water may increase availability of arthropods. Even birds that are not primarily insectivorous often consume arthropods during specific life stages or feed on arthropods as a dietary supplement (Jordano, 2000). In particular, the strong relationship between migratory species richness and distance to water may be related to the dietary ecology of these species, since nine of 14 austral migratory species in our study were insectivores. Indeed, seven of these species are in the family Tyrannidae, a highly insectivorous family (Stotz et al., 1996). 42 4.3 Responses to urbanization: resident versus migratory birds As opposed to most studies on north-temperate urban bird communities (e.g. Stratford & Robinson, 2005; Rodewald & Bakermans, 2006; Husté & Boulinier, 2011), migratory birds in São Paulo were no more sensitive to urbanization than residents, potentially due to the relatively low habitat specificity that characterizes Neotropical austral migrants (Stotz et al., 1996). In contrast to many migratory birds that breed at north-temperate latitudes, which largely occupy forests, most Neotropical austral migrant bird species more frequently use open and edge- dominated habitats (Chesser, 1994) and may thus be more pre-adapted to urban environments than most migratory birds at north-temperate latitudes. Nevertheless, given that temporal availability of food resources is often dampened in urban versus rural environments (Leveau, 2018) and that birds often depend on such surpluses, the temporal homogenization of food resource availability has the potential to negatively impact birds in urban areas (Leveau, 2018). Results of our study suggest several promising avenues for research on specific ecological, behavioral and physiological mechanisms driving spatio-temporal patterns of avian biodiversity in urban environments. For example: Which mechanisms drive the relationship between avian species richness, noise level and distance to water that we detected? Given that nearly half of São Paulo’s rivers are polluted (SOS, 2017), future studies could evaluate the combined impact of distance to water and water quality on the presence of birds in the city across space and time. Why do resident and migratory birds respond similarly to São Paulo’s urban landscape? Are there specific life history and ecological characteristics of some groups of birds that make them more or less vulnerable to urbanization in the Atlantic Forest? 5. Conclusions Variation in avian diversity within São Paulo green spaces was best explained by noise level and distance to water. As such, our findings suggest that managing anthropogenic noise and water resources are two pathways to support bird communities within Neotropical cities. Additionally, given that tree cover had a weak but positive influence on both resident and migratory species richness in our study, maintaining healthy urban forests is important for providing adequate habitat for many urban birds. The maintenance of water bodies and their related vegetation is also essential for creating a bird-friendly city and improving human welfare 43 (Faggi & Caula, 2017). Indeed, natural areas within the urban matrix have been shown to provide multiple social and psychological benefits for humans, and environmental services such as air purification, regulation of microclimate, and noise level reduction (Bolund & Hunhammar, 1999; Chiesura, 2004). We encourage landscape and city planners to carefully consider the composition and configuration of green spaces within tropical cities to optimize ecological and social benefits. Further research on the relationship between birds and urbanization in the tropics is imperative, given that our results and those of other studies show that tropical birds may be responding to urbanization in unique ways than do birds at north-temperate latitudes. 6. References Amaya-Espinel, J.D., & Hostetler, M.E. (2019). The value of small forest fragments and urban tree canopy for Neotropical migrant birds during winter and migration seasons in Latin American countries: A systematic review. Landscape and Urban Planning 190: 103592. doi.org/10.1016/j.landurbplan.2019.103592 Aronson, M.F.J., Lepczyk, C.A., Evans, K.L., Goddard, M.A., Lerman, S.B., Maclvor, J.S., Nilon, C.H., & Vargo, T. (2017). Biodiversity in the city: key challenge for urban green space management. Frontiers in Ecology and the Environment doi:10.1002/fee.1480 Barbosa, K.V.C., Knogge, C., Develey, P.F., Jenkins, C.N., & Uezu, A. (2017). Use of small Atlantic Forest fragments by birds in Southeast Brazil. Perspectives in Ecology and Conservation, 15, 42–46. Barçante, L., Vale, M., & Alves, M.A.S. (2017). Altitudinal migration by birds: a review of the literature and a comprehensive list of species. Journal of Field Ornithology, 88, 321–335. Blair, R.B. (2001). Creating a homogenous avifauna. In J. M. Marzluff, R. Bowman, and R. Donelly (Eds.). Avian ecology and conservation in an urbanizing world (pp. 459–486). Boston: Kluwer Academic Publishers. Blake, J.G., & Karr, J.R. (1987). Breeding birds of isolated woodlots: area and habitat relationships. Ecology, 68(6): 1724-1734. Bibby, C.J., Burgess, N.D., & Hill, D.A. (1992). Bird census techniques. British Trust for Ornithology and the Royal Society for the Protection of Birds. 44 Bolund, P., & Hunhammar, S. (1999). Ecosystem service in urban areas. Ecological Economics, 29, 293–301. Burnham, K.P., & Anderson, D.R. (2002). Model Selection and Multimodel Inference, 2nd edn. Springer–Verlag, New York, NY, USA. Brumm, H. (2004). The impact of environmental noise on song amplitude in a territorial bird. Journal of Animal Ecology, 73, 434–440. Chace, J.F., & Walsh, J.J. (2006). Urban effects on native avifauna: a review, Landscape and Urban Planning, 74, 46–69. Chesser, R. T. (1994). Migration in South America: an overview of the austral system. Bird Conservation International, 4, 91-107. Chiesura, A. (2004). The role of urban parks for the sustainable city. Landscape and Urban Planning, 68, 129-138. doi:10.1016/j.landurbplan.2003.08.003 Cueto, V.R., & Jahn, A.E. (2008). Sobre la necesidad de tener un nombre estandarizado para las aves que migran dentro de América del Sur. Hornero, 23(1), 1-4. Emlen, J.T. (1974). An urban bird community in Tucson, Arizona: derivation, structure, regulation. Condor, 76, 184–197. Evans, B.S., Reitsma, R., Hurlbert, A.H., & Marra, P.P. (2018). Environmental filtering of avian communities along a rural‐to‐urban gradient in Greater Washington, DC, USA. Ecosphere, 9(11): e02402. 10.1002/ecs2.2402 Ferreira, M.J., de Oliveira, A.P., Soares, J., Codato, G., Bárbaro, E.W., & Escobedo, J.F. (2012). Radiation balance at the surface in the city of São Paulo, Brazil: diurnal and seasonal variations. Theoretical and applied climatology, 107(1-2), 229-246. Faggi, A., & Perepelizin, P. (2006). Riqueza de aves a lo largo de un gradiente de urbanización en la ciudad de Buenos Aires. Revista del Museo Argentino de Ciencias Naturales nueva serie, 8(2), 289-297. Faggi, A., & Caula, S. (2017). ‘Green’ or ‘Gray’? Infrastructure and Bird Ecology in Urban Latin America. In MacGregor-Fors, I., & Escobar-Ibáñez, J.F.(Eds.), Avian Ecology in Latin American Cityscapes. (pp.79-98). Springer Nature, DOI 10.1007/978-3-319-63475-3_5 Fontana, C.S., Burger, M.I., & Magnusson, W.E. (2011). Bird diversity in a subtropical South- American City: effects of noise levels, arborisation and human population density. Urban Ecosystems, 14, 341-360. 45 Goodwin, S.E., & Shriver, W.G. (2011). Effects of traffic noise on occupancy patterns of forest birds. Conservation Biology, 25, 406–411. Grimm, N.B., Grove, J.M., Pickett, S.T.A., & Redman, C.I. (2000). Integrated Approaches to Long-Term Studies of Urban Ecological Systems. BioScience, 50 (7), 571-584. Husté, A., & Boulinier, T. (2011). Determinants of bird community composition on patches in the suburbs of Paris, France. Biological Conservation, 144(1), 243-252. IBGE - Instituto Brasileiro de Geografia e Estatística (2018). Brazilian government geographic and statistics – data from 2018. Retrieved from https://cidades.ibge.gov.br/brasil/sp/sao-paulo/ Joseph, L. (1996). Preliminary climatic overview of migration patterns in South America Austral Migrant passerines, Ecotropica 2: 185-193. Jackson, H.B., & Fahrig, L. (2015) Are ecologists conducting research at the optimal scale? Global Ecology and Biogeography, 24, 52-63. Jokimäki, J., Suhonen J., & Kaisanlahti-Jokimäki, M. (2018). Urban core areas are important for species conservation: A European-level analysis of breeding bird species. Landscape and Urban Planning, 178, 73-81. Jordano, P. (2000). Fruits and frugivory. In: Fenner, M. (ed.). Seeds: the ecology of regeneration in plant communities, 2nd edition. CABI Publ. Wallingford, UK. Pages 125-166. Karr, J.R., & Freemark, K.E. (1983). Habitat Selection and Environmental Gradients: Dynamics in the "Stable". Tropics Ecology, 64 (6), 1481-1494. Laboratório de Silvicultura Urbana (2010). Centro de Métodos Quantitativos. Retrieved 1 August 2017 from http://cmq.esalq.usp.br/wiki/lib/exe/fetch.php?media=publico:mapeamento_tematico_sp_2010.p df. Lepczyk, C.A., Aronson, M.F.J., Evans, K.L., Goddard, M.A., Lerman, S.B., & Macivor, J.S. (2017). Biodiversity in the city: fundamental questions for understanding the ecology of urban green spaces for biodiversity conservation. BioScience 67: 799–807 Leveau, L. M. (2013). Relaciones aves–habitat en el sector suburbano de Mar del Plata, Argentina. Ornitologia Neotropical, 24, 201-212 Leveau, L.M. (2018). Urbanization, environmental stabilization and temporal persistence of bird species: a view from Latin America. PeerJ 6:e6056 https://doi.org/10.7717/peerj.6056 http://cmq.esalq.usp.br/wiki/lib/exe/fetch.php?media=publico:mapeamento_tematico_sp_2010.pdf http://cmq.esalq.usp.br/wiki/lib/exe/fetch.php?media=publico:mapeamento_tematico_sp_2010.pdf 46 Loss, S.R., Ruiz, M.O., & Brawn, J.D. (2009). Relationships between avian diversity, neighborhood age, income, and environmental characteristics of an urban landscape. Biological Conservation, 142, 2578–2585. Lowry H., Lill, A., & Wong, B.B.M. (2012). Behavioural responses of wildlife to urban Environments. Biological Reviews 000–000. doi: 10.1111/brv.12012 MacGregor-Fors, I. (2008). Relation between habitat attributes and bird richness in a western Mexico suburb. Landscape and Urban Planning, 84, 92–9b8. Maisonneuve, N., Stevens, M., Niessen, M.E., & Steels, L. (2009). NoiseTube: Measuring and mapping noise pollution with mobile phones. DOI 10.1007/978-3-540-88351-7_16 Martin, A.E., & Fahrig, L. (2018). Habitat specialist birds disperse farther and are more migratory than habitat generalist birds. Ecology, 99(9), 2058–2066. doi.org/10.1002/ecy.2428 McKinney, M.L. (2002). Urbanization, Biodiversity, and Conservation the impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems. BioScience, 52 (10), 883-890. Narango, D.L. & Rodewal, A.D. (2015). Urban-associated drives of song variation along a rural-urban gradient. Behavior Ecology, 27(2), 608-616. Ortega-Álvarez, R., & MacGregor-Fors, I. (2009). Living in the big city: Effects of urban land-use on bird community structure, Landscape and Urban Planning, 90,189–195 Palacio, F.X, Ibañez, L., Maragliano, R., & Montalti, D. (2018). Urbanization as a driver of taxonomic, functional and phylogenetic diversity loss in bird communities. Canadian Journal of Zoology. https://doi.org/10.1139/cjz-2018-0008 Pena, J.C.C., Martello, F., Ribeiro, M.C., Armitage, R.A., Young, R.J., & Rodrigues, M. (2017) Street trees reduce the negative effects of urbanization on birds. PLoS ONE 12(3). doi.org/10.1371/journal.pone.0174484 R Core Team (2017). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., & Hirota, M.M. (2009). The Brazilian Atlantic Forest: How much is left and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142 (6), 1141–1153. https://doi.org/10.1371/journal.pone.0174484 47 Robinson, S.K., Thompson III, F.R., Donovan, T.M., Whitehead, D.R., & Faaborg, J. (1995). Regional forest fragmentation and the nesting success of migratory birds. Science, 267, 1987- 1990. Rodewald, A. D., & Bakermans, M.H. (2006). What is the appropriate paradigm for riparian forest conservation? Biological Conservation, 128, 193-200. Rodewald, A.D., & Shustack D.P. (2008). Consumer resource-matching in urbanizing landscapes: are synanthropic species over-matching? Ecology, 89, 515-521. Rodewald, A.D., Shustack, D.P., & Hitchcock, L.E. (2010). Exotic shrubs as ephemeral ecological traps for nesting birds. Biological Invasions, 12, 33-39. Rodewald, A.D., Kearns, L.J., & Shustack, D.P. (2011). Anthropogenic resources decouple predator-prey relationships. Ecological Applications, 21, 936-943. Roca, I.T., Desrochers, L., Giacomazzo, M., Bartolo, A., Bolduc P., Deschesnes, R., Martin, C.A., Rainville, V., Rheault, G., & Proulx, R. (2016). Shifting song frequencies in response to anthropogenic noise: a meta-analysis on birds and anurans. Behavioral Ecology. 27:1269–1274. Souza, F.L., Valente-Neto, F., Severo-Neto, F., Bueno, B., Ochoa-Quintero, J.M., Laps, R.R., Bolzan, F., & Roque, F.O. (2019). Impervious surface and heterogeneity are opposite drivers to maintain bird richness in a Cerrado city. Landscape and Urban Planning 192: 103643. doi.org/10.1016/j.landurbplan.2019.103643 SOS - Mata Atlântica (2017). Observando-os-Rio. O retrato da qualidade da água nas bacias da Mata Atlântica (SOS Mata Atlântica Techinical Report) Retrieved from https://www.sosma.org.br/wp-content/uploads/2017/03/SOSMA_Observando-os-Rios- 2017_online.pdf. Stratford, J.A., & Robinson, W.D. (2005). Distribution of neotropical migratory bird species across an urbanizing landscape. Urban Ecosystems 8:59–77. Stotz, D.F., Fitzpatrick, J.W. & Parker III, T. (1996). Neotropical Birds: Ecology and Conservation. University of Chicago Press, Chicago. SVMA - Secretaria Municipal do Verde e do Meio Ambiente (2018). Inventário da Biodiversidade do Município de São Paulo (Technical Report). Diário Oficial da Cidade de São Paulo, 61Number 241, 24 December. Retrieved from https://www.prefeitura.sp.gov.br/cidade/secretarias/upload/PUB_FAUNA_DIGITAL_2018%20d ownload2.pdf https://www.sosma.org.br/wp-content/uploads/2017/03/SOSMA_Observando-os-Rios-2017_online.pdf https://www.sosma.org.br/wp-content/uploads/2017/03/SOSMA_Observando-os-Rios-2017_online.pdf 48 Tarifa, J.R., & Armani, G. (2000). Unidades Climáticas Urbanas da Cidade de São Paulo (primeira aproximação). In: Atlas Ambiental do Município de São Paulo – FASE I. SVMA, Prefeitura Municipal de São Paulo. Toledo, M.C.B., Donatelli, R.J., & Batista, G.T. (2011). Relation between green spaces and bird community structure in an urban area in Southeast Brazil. Urban Ecosyst 15:111-131. Trollope, ST., White, J.G., & Cooke, R. (2009). The response of ground and bark foraging insectivorous birds across an urban–forest gradient. Landscape and Urban Planning 93: 142–150 Trusilova, K., Jung, M., & Churkina, G. (2009). On climate impacts of a potential expansion of urban land in Europe. J Appl Meteor Climatol 48:1972–1980. doi:10.1175/2009JAMC2108.1 United Nations (2018). Word Urbanization Prospects: The 2018 Revision – Key facts. United Nations. Available in https://esa.un.org/unpd/wup/Publications/Files/WUP2018-KeyFacts.pdf Wood, W.E., & Yerezinac, S.M. (2006). Song sparrow (Melospiza melodia) song varies with urban noise. Auk, 123, 650–659. Zamora, W., Calafate, C.T., Cano, J.C., & Manzoni, P. (2017). Accurate ambient noise assessment using smartphones. Sensors, 17, 917; doi:10.3390/s17040917 49 Supplementary material S1: Variables vs richness of migratory and resident birds - Graphics of variables tendency versus resident and migratory species. Proximity to water Noise level 50 S2: Correlation matrix of variables: Lawn – Percentage of lawn, Tree_cover (veg) – percentage of cover tree; Water - measurement of the distance from the point count until the closest lake or river (selected just primary or secondary river); Human_pop (pop) – index of population living inside the buffer (Prefeitura da Cidade de São Paulo – GeoSampa); Noise – index of noise in the point count - the average value generated by the cellphone app for each of the three visits and made a weighted average of that value; Buildings: percentage of buildings in the landscape; Impervious_surface – Percentage of impervious surface (asphalt and concrete areas). We consider the landscape for measure the variables a buffer or 1km from the bird species point count. We collected the noise in the point count using the cellphone app ‘Sound Meter’ for 1 min, 3 times, during each visit. For collecting these data, we used the same cell phone, by the same person and protocol. We create an index of noise using the average of collected data from each landscape, and the index vary between 19.8 to 48.8. 51 S3: Selection procedure to choose the best scales of response for each dependent variable: imp – percentage of impervious surface (asphalt and concrete areas) in the landscape; veg – percentage of tree cover in the landscape; pop – index of population living in the landscape. We define scale as the spatial extent of a measured landscape (buffer size), from the point count: 50m, 250m, 500m, 1000m and 2000m. Residents Migratory Scales and variables ΔAIC df wAIC Scales and variables ΔAIC df wAIC res.imp_500 0 3 0.7677 migra.imp_1000 0 3 0.4074 res.imp_1000 3.3 3 0.1453 migra.imp_500 0.7 3 0.2836 res.imp_250 4.7 3 0.0741 migra.imp_2000 1.8 3 0.1638 res.imp_2000 8.5 3 0.011 migra.imp_250 2.2 3 0.1377 res.imp_50 12 3 0.0019 migra.imp_50 8 3 0.0075 res.veg_1000 0 3 0.67 migra. veg_1000 0 3 0.293 res. veg_500 2.7 3 0.177 migra. veg_50 0.6 3 0.221 res. veg_l2000 3.5 3 0.114 migra. veg_2000 0.6 3 0.218 res. veg_250 6.5 3 0.026 migra. veg_500 0.6 3 0.213 res. veg_50 7.8 3 0.013 migra. veg_50 3.3 3 0.055 res.pop50 0 3 0.27 migra.pop1000 0 3 0.4074 res.pop250 0.2 3 0.24 migra.pop500 0.7 3 0.2836 res.pop500 0.4 3 0.22 migra.pop2000 1.8 3 0.1638 res.pop1000 1.1 3 0.16 migra.pop250 2.2 3 0.1377 res.pop2000 1.8 3 0.11 migra.pop50 8 3 0.0075 52 Appendix A Sites and characteristics Table A1: Green areas visited in São Paulo, Brazil; Pq = Park, Pr = “Praça” and St = Street; ‘Tree cover’ = percent tree cover, ‘Water’ = distance from the point count to the nearest water body (in meters); ‘Noise’ = noise index, number of migratory (M) and resident (R) bird species observed, foraging strata (CN – canopy, MI – mid-story, UN – understory, GR – ground and WA – water) and diet (CA – carnivore, FR – frugivore, IN- insectivore, NE – nectarivore and OM – omnivore). Id number refers to the location of 31 point counts in the city of São Paulo, Brazil (Fig. 1). Id Site Tree cover Water Noise M R CN MI UN GR WA CA FR IN NE OM 1 Pq Ecológico Tietê 1 0.41 146 36.7 3 19 9 7 2 4 0 2 4 6 2 7 2 Pq Ecológico Tietê 2 0.39 128 33.2 6 36 17 12 7 6 0 3 6 20 3 8 3 Pr AntonioCastroLopes 0.17 10 42.2 6 24 11 7 8 4 0 1 3 15 2 6 4 Pq Tiquatira 0.15 3 43.0 3 18 10 5 4 2 0 0 4 7 2 6 5 Pq Jardim Botânico 0.52 67 24.6 4 30 13 12 4 3 2 3 5 16 2 7 6 Pq Ibirapuera 0.47 356 33.8 3 22 10 5 6 2 2 2 7 9 0 6 7 Pq Aclimação 0.20 3 32.4 5 28 16 7 4 2 4 5 7 13 1 5 8 Pq Independência 0.19 662 35.2 3 23 12 5 6 2 1 2 4 10 0 7 9 Pq Instituto Butantan 0.45 458 27.2 3 19 11 8 1 2 0 2 5 9 1 4 10 Pq Horto Florestal 0.61 50 26.0 5 32 15 7 3 6 6 8 8 13 2 6 11 Pq Cantareira - Engordador 0.57 64 19.8 10 48 26 22 7 2 1 1 14 29 3 10 12 Pq Anhanguera 0.72 264 22.7 4 17 9 8 2 2 0 0 3 12 1 4 13 Pq Cantareira - PedraGrande 0.63 182 19.8 6 44 17 20 8 5 0 2 9 24 2 9 14 Pq Trianon 0.17 1500 38.5 3 10 8 4 0 1 0 1 3 4 1 4 15 Pq Cidade Toronto 0.35 1 38.8 4 37 13 6 7 7 10 8 4 16 2 9 16 Pq Vila Lobos 0.39 50 32.8 4 24 13 6 6 2 1 2 8 9 2 5 17 St Aquário 0.43 2 34.2 4 22 11 4 7 4 0 1 3 11 1 7 18 Pr Amaguas 0.2 1255 48.8 0 8 4 2 1 1 0 0 2 1 1 3 19 Pr Memórias Jaçanã 0.22 488 46.5 2 14 8 4 1 3 0 1 3 3 1 6 20 Pq Luz 0.11 279 38.6 4 17 11 4 4 2 0 0 6 8 0 6 21 Pr Pedro José Nunes 0.19 15 36.0 2 21 8 4 8 3 0 1 3 8 2 5 22 Pq Piqueri 0.15 50 37.8 5 18 12 5 3 3 1 3 5 8 1 6 23 Pq BulerMarx 0.41 160 36.8 4 23 11 10 3 3 0 1 4 12 2 6 24 Pq Nove de Julho 0.23 5 23.8 7 40 15 6 9 7 12 8 4 20 0 11 25 Pq Guarapiranga 0.18 196 27.8 5 16 12 6 2 1 0 1 4 10 1 4 26 Pq Carmo 0.72 300 31.4 5 27 13 8 7 4 2 0 6 13 2 11 27 Pq Água Branca 0.18 834 36.2 5 13 9 6 2 1 0 0 4 9 1 4 28 Pq Juventude 0.15 121 31.8 2 21 10 5 5 3 0 2 5 7 1 7 29 St Vila Constância 0.12 91 35.3 3 16 8 4 5 2 0 0 3 7 2 5 30 Pq USP 0.37 314 27.8 2 15 6 7 3 1 0 0 3 7 1 5 31 Pr Comendador Vargas 0.28 1280 38.5 2 15 8 4 3 2 0 1 3 5 2 3 53 Appendix B Bird species registered in the study and their traits Table B1 – Number of parks where a given species was registered; strata – foraging strata: GR – Ground, UN – Understory, MI – Mid-story, CA – Canopy, and WA – Water (adapted from Stotz et al 1996*); diet – CA – Carnivorous, FR – mostly frugivorous, IN – mostly insectivorous/consumes arthropods, NE – Nectarivorous and OM – Omnivorous (i.e., frequently use more than two food resources – from del Hoyo et al 2018**); dist – Distribution: N – Native, E – Exotic and I – Introduced (species native to other parts of the country that currently are occurring in the city of São Paulo); R/M – Resident or Migratory species in this region, according to Somenzari et al (2017)*** and from observations in the city of São Paulo by ornithologists, and AM – altitudinal migrant (Barçante et al., 2017); AF – Atlantic Forest endemic (1) and non-endemic (0); Sensitivity: L – Low, M – Medium, and H – High (Stotz et al 1996). Family Species Total strata diet dist R/M AF Sensitivity Tinamidae Tinamus solitarius 1 GR SE N R 1 M Crypturellus obsoletus 1 GR SE N R 0 L Anatidae Dendrocygna viduata 4 WA OM N R 0 L Amazonetta brasiliensis 2 WA OM N R 0 L Anas versicolor 1 WA IN N R 1 L Cracidae Penelope obscura 1 MI FR N R 0 M Podicipedidae Podilymbus podiceps 1 WA IN N R 0 M Phalacrocoracidae Nannopterum brasil