Historical knowledge, richness and relative representativeness of the avifauna of the largest native urban rainforest in the world

Vinicius R. Tonetti Marco A. Rego André C. De Luca Pedro F. Develey Fábio Schunck Luís F. Silveira About the authors

ABSTRACT

Stretching for more than 10,000 ha in the Metropolitan Area of São Paulo, southeastern Brazil, Serra da Cantareira comprises the largest native urban rainforest in the World, harboring a rich and diverse Atlantic Forest avifauna. Despite its closeness to major urban areas, few bird surveys have been conducted there. In this article we present an updated compilation of all bird species recorded for Serra da Cantareira, including personal records from the authors. A total of 326 species have been recorded for Serra da Cantareira since 1901; of these, nine have not been sighted there for the last two decades. The number of bird species endemic to the Atlantic Forest is high (80), and seven of its species are globally threatened. According to multivariate analyses the species diversity at Serra da Cantareira is similar to other regions of the Atlantic Forest, such as Carlos Botelho and Intervales state parks, where the vegetation is also ombrophilous dense forest. We discuss local changes in the avifaunal composition over the last decades and suggest the incorporation of large forest remnants to the Cantareira State Park to mitigate the impact of the northern section of Rodoanel Mário Covas, a highway (SP-21) that will soon be operational and will negatively impact the biodiversity of Serra da Cantareira.

KEY WORDS:
Atlantic Forest; bird conservation; hierarchical cluster analysis; principal coordinate analysis; Serra da Cantareira

INTRODUCTION

The Atlantic Forest (AF) is the second largest rainforest in South America and has a rich and diverse avifauna (900 species, 24% of which are endemic to the AF; Lima 2013Lima LM (2013) Birds of the Atlantic Forest: richness, compostion, status, endemism, and conservation. Master dissertation, Universidade de São Paulo, São Paulo. http://www.teses.usp.br/teses/disponiveis/41/41133/tde-17042014-091547/pt-br.php [Acessed: 19/03/2016]
http://www.teses.usp.br/teses/disponivei...
). New bird species are still being discovered in this forest, even near large urban areas (Buzzetti et al. 2013Buzzetti DRC, Belmonte-Lopes R, Reinert BL, Silveira LF, Bornschein MR (2013) A new species of Formicivora Swainson, 1824 (Thamnophilidae) from the state of São Paulo, Brazil. Revista Brasileira de Ornitologia 21: 269-291.), demonstrating that the local avifauna is not completely known, and reinforcing the importance of bird surveys there. Despite the high levels of species richness and endemism, only ~12% of the AF forest remains, and as a result, a large number of its component taxa are at imminent risk of extinction (Marini and Garcia 2005Marini MA, Garcia FI (2005) Bird conservation in Brazil. Conservation Biology 19: 665-671. https://doi.org/10.1111/j.1523-1739.2005.00706.x
https://doi.org/10.1111/j.1523-1739.2005...
, Ribeiro et al. 2009Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: 1141-1153. https://doi.org/10.1016/j.biocon.2009.02.021
https://doi.org/10.1016/j.biocon.2009.02...
). In addition to the importance of the AF for bird conservation, its forest remnants provide several ecosystem services for human populations, such as guaranteeing water supply near major urban areas (Dean 1995Dean W (1995) A ferro e fogo: a história de devastação da Mata Atlântica brasileira. Companhia das letras, São Paulo, 484 pp.).

After 1893, due to a water collapse in the city São Paulo, the government started to expropriate farms at Serra da Cantareira for reforestation, to ensure the recovery of the streams and river that supply the city with water (Vilar 2007Vilar DD (2007) Água aos Cântaros - Os reservatórios da Cantareira: um estudo de arqueologia industrial. PhD thesis, Universidade de São Paulo, São Paulo. Available online at: Available online at: http://www.teses.usp.br/teses/disponiveis/71/71131/tde-18032008-111130/pt-br.php [Acessed: 19/03/2016]
http://www.teses.usp.br/teses/disponivei...
). Considered the central piece in the São Paulo City Green Belt Biosphere Reserve by UNESCO and an Important Bird Area by BirdLife International (IBA SP03), Serra da Cantareira still provides water and other ecosystem services to the city, and houses a significant portion of the AF biodiversity, including several threatened and endemic species (Bencke et al. 2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp., Whately and Cunha 2007Whately M, Cunha P (2007) Cantareira 2006: um olhar sobre o maior manancial de água da Região Metropolitana de São Paulo. Instituto Socioambiental, São Paulo, 67 pp., Ayres 2008Ayres ACM (2008) O Ciclo da Caapora: A RMSP e o Parque da Cantareira. Annablume, São Paulo, 120 pp.). Serra da Cantareira stretches for more than 10,000 ha in the Metropolitan Area of the city of São Paulo, the most populated and urbanized region in South America, and currently comprises the largest native urban rainforest in the world (Ayres 2008Ayres ACM (2008) O Ciclo da Caapora: A RMSP e o Parque da Cantareira. Annablume, São Paulo, 120 pp.). The main impacts to the biodiversity of Serra da Cantareira are urban expansion and large infrastructure projects in nearby towns (Bencke et al. 2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp., Fig. 1).

Figure 1
Serra da Cantareira locations surveyed in this study. In the urban slope are Cantareira State Park admnistrative zones and their trails: AC = Águas Claras; PG = Pedra Grande; Eng = Engordador; Cab = Cabuçu; EL = Estrada do Lenhador; Alberto Löfgren State Park (ALSP) and A2. In the inner slope are A1, A3, A4, A5 and SC = Sítio Capuavinha private reserve.

Although Serra da Cantareira is continuous with one of the largest cities in the world and near several research institutions and universities, few ornithological studies have been performed there. Museum collectors were the first to survey these mountains in the end of the XIX century (see Pinto 1938Pinto OMO (1938) Catálogo das Aves do Brasil e lista dos exemplares que as representam no Museu Paulista. Museu Paulista, São Paulo, 566 pp. https://doi.org/10.5962/bhl.title.99663
https://doi.org/10.5962/bhl.title.99663...
, 1944Pinto OMO (1944) Catalogo das Aves do Brasil e Lista dos Exemplares Existentes na Coleção do Departamento de Zoologia, Vol. 2. Departamento de Zoologia, São Paulo, 700 pp., Paynter and Traylor 1991Paynter RA, Traylor MA (1991) Ornithological Gazzeteer of Brazil. Cambridge, Harvard University, 788 pp.). Graham (1992Graham DJ (1992) The Avifauna of the Serra da Cantareira, São Paulo, Brazil: A preliminary survey. IF, Série Registros 10: 1-56.) published the only comprehensive bird inventory of the region, more than 20 years ago. Other than museum specimens and Graham’s article, there have been few ornithological studies and bird surveys. They range from comparison of communities in different vegetation types (Graham 1991Graham DJ (1991) The avifauna and the vegetation structure of a mature araucaria plantation in São Paulo, Brazil. IF, Série Registros 6: 1-79., Antunes et al. 2009Antunes AZ, Wyrgun B, Eston MR (2009) Composição das comunidades de aves em duas florestas secundárias contíguas no sudesde do Brasil. Revista do Instituto Florestal 21: 93-106.; frugivory (Fonseca and Antunes 2007Fonseca FY, Antunes AZ (2007) Frugivoria e predação de sementes por aves no Parque Estadual Alberto Löfgren, São Paulo, SP. Revista do Instituto Florestal 19: 81-91., Ikuta and Martins 2013Ikuta KG, Martins FC (2013) Interação entre aves frugívoras e plantas no Parque Estadual da Cantareira, estado de São Paulo. Atualidades Ornitológicas 172: 33-36.); new species records (Antunes et al. 2008aAntunes AZ, dos Santos AMR, Eston MR (2008a) Registros relevantes de aves para a grande São Paulo obtidos no Parque Estadual da Cantareira (Nota Científica). Revista do Instituto Florestal 20: 221-224.), plumage anomaly (Cavarzere and Tonetti 2015Cavarzere V, Tonetti VR (2015) Complete leucism in the Fawn-breasted Tanager Pipraeidea melanonota (Aves: Thraupidae). Boletim do Museu de Biologia Prof. Mello Leitão 37: 233-240.); nest description (V.R. Tonetti et al. unpublished data), studies on species ecology (Tonetti and Pizo 2016Tonetti VR, Pizo MA (2016) Density and microhabitat preference of the Southern Bristle-tyrant (Phylloscartes eximius): Conservation policy implications. The Condor: Ornithological Applications 118: 791-803. https://doi.org/10.1650/CONDOR-16-89.1
https://doi.org/10.1650/CONDOR-16-89.1...
), technical reports (Antunes and Eston 2009Antunes AZ, Eston MR (2009) Anexo 10: espécies de aves registradas no PEC. In: Leonel C, Déscio F, Mazzei K, Leite MO, Barros MIA (Eds). Parque Estadual da Cantareira: plano de manejo. São Paulo, Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, 1-10., 2012Antunes AZ, Eston MR (2012) Anexo 8: espécies de aves registradas no PEAL. In: Arromba AL, Leonel C, Santiago CM, Mazzei K, Bucci LA, Nalon MA, Barros MIA (Eds) Parque Estadual Alberto Löfgren: plano de manejo. Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, São Paulo, 1-10., DERSA 2010DERSA (2010) Programa Rodoanel Mario Covas, Trecho Norte: Estudo de Impacto Ambiental. Volume IV. Desenvolvimento Rodoviário S/A, Consórcio JPGP-PRIME, São Paulo, 451 pp.) and records provided by birdwatchers (WikiAves 2016WikiAves (2016) A enciclopédia das aves do Brasil. http://ww.wikiaves.com.br [Acessed: 19/03/2016]
http://ww.wikiaves.com.br...
, Xeno-Canto 2016Xeno-Canto (2016) Xeno-Canto, compartilhando sons de aves do mundo todo. http://www.xeno-canto.org [Acessed: 19/03/2016]
http://www.xeno-canto.org...
).

In this article, we present an updated compilation of all bird species recorded for Serra da Cantareira, including our personal records. We compare the avifauna between Serra da Cantareira and other regions of AF using multivariate analysis, discuss changes in avifaunal composition during the last decades, and provide additional information on some threatened and/or uncommon species. Lastly, we focus on specific localities and measures for bird conservation in our study area.

MATERIAL AND METHODS

Serra da Cantareira ranges from 750 to 1,250 m asl. The vegetation there is predominantly montane ombrophilous dense forest. The climate is mesothermal and humid, with rainy summers and dry winters (CWA Köppen), and annual temperature and rainfall averaging 20 °C and 1,500 mm, respectively (Bencke et al. 2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp.). The slope facing the urban area comprises the most preserved area, with continuous forests, which is mostly protected by Cantareira (7,900 ha; hereafter CSP) and Alberto Löfgren state parks (187 ha; ALSP). CSP is divided into four administrative zones: Águas Claras, Cabuçu, Engordador and Pedra Grande (Fig. 1). Patches in the inner slope have variable sizes (~1 to 100 ha) and are at different stages of regeneration. In this study we considered bird records from CSP, ALSP, neighboring patches in the inner slope, including the 20-ha private reserve Sítio Capuavinha (Lemos 2014Lemos RF (2014) Avifauna da Reserva Particular do Patrimônio Natural (RPPN) Sítio Capuavinha, município de Mairiporã, São Paulo. Atualidades Ornitológicas 179: 38-45.) and records that indicated only “Serra da Cantareira” as a location, without any further detail.

We obtained species records over the last decade during systematic and unsystematic bird surveys. In unsystematic surveys, samplings consisted of recording all aurally or visually detected birds at unlimited distance, while walking on trails (Ribon 2010Ribon R (2010) Amostragem de aves pelo método de listas de Mackinnon. In: Von Matter S, Straube FC, Accordi IA, Piacentini VQ, Cândido Jr JF (Eds) Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Technical Books, Rio de Janeiro, 33-44.). Surveys were performed during the morning in different seasons and were mostly concentrated on the available trails of the four CSP administrative zones and a dirt road named “estrada do lenhador”, at the park’s boundaries (Fig. 1). Birds were recorded with the aid of binoculars and song recordings and photographs were occasionally taken during surveys.

VRT performed a systematic survey using point-counts. In this study, 100 fixed-points were established in the four CSP administrative zones and visits lasted 10 minutes during the morning. Each point was visited six times on different days between May and December 2014, resulting in a total of 600 samples, which include only birds detected within a 50-m radius (Vielliard et al. 2010Vielliard JME, Almeida MEC, Anjos L, Silva WR (2010) Levantamento quantitativo por pontos de escuta e o Índice Pontual de Abundância (IPA). In: Von Matter S, Straube FC, Accordi IA, Piacentini VQ, Cândido Jr JF (Eds) Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Technical Books, Rio de Janeiro , 47-06., Tonetti and Pizo 2016Tonetti VR, Pizo MA (2016) Density and microhabitat preference of the Southern Bristle-tyrant (Phylloscartes eximius): Conservation policy implications. The Condor: Ornithological Applications 118: 791-803. https://doi.org/10.1650/CONDOR-16-89.1
https://doi.org/10.1650/CONDOR-16-89.1...
). MAR, along with other researchers (see names in acknowledgements), performed another systematic study using line transects (80 h of sampling effort) and mist-nets (2,600 net-hours) in five different areas (A1 to A5; Fig. 1). These surveys were conducted during the morning and late afternoon from August 12th 2009 to April 29th 2010. Some netted specimens were collected and deposited in the MZUSP collection (details in DERSA 2010DERSA (2010) Programa Rodoanel Mario Covas, Trecho Norte: Estudo de Impacto Ambiental. Volume IV. Desenvolvimento Rodoviário S/A, Consórcio JPGP-PRIME, São Paulo, 451 pp.).

In order to compile our data, we searched for museum specimens collected from “Cantareira State Park”, “Parque Estadual da Cantareira”, “Cantareira Mountains”, “Serra da Cantareira”, “Cantareira”, “Alberto Löfgren State Park”, “Parque Estadual Alberto Löfgren”, “Horto Florestal”, “Cuca, Horto Florestal” and “Parque Florestal”. We surveyed the collections of the following museums: Museum of Zoology of the University of São Paulo (MZUSP, Brazil), Museum of Zoology of the Campinas University (MUNICAMP, Brazil), and the Field Museum of Natural History (FMNH, USA). The localities cited above correspond to CSP, ALSP or not specified sites at Serra da Cantareira (Paynter and Traylor 1991Paynter RA, Traylor MA (1991) Ornithological Gazzeteer of Brazil. Cambridge, Harvard University, 788 pp.). Using the same terms as outlined above, we searched for indexed articles potentially containing bird records in the citation databases Web of Science, Google Scholar and SciELO. Additionally, we used Google to search for non-indexed articles and “gray” literature, such as technical reports and theses. We also compiled records from the WikiAves (www.wikiaves.com; WA) and Xeno-canto (www.xeno-canto.org; XC) databases. All searches were performed until June 1st 2016. We discarded erroneous or doubtful records - i.e. misidentified pictures and song records, as well as species pending confirmation of their occurrence in our study area according to the literature. We followed the nomenclature of the CBRO (Brazilian Ornithological Records Committee) (Piacentini et al. 2015Piacentini VQ, Aleixo A, Agne CE, Maurício GN, Pacheco JF, Bravo GA, Brito GRR, Naka LN, Olmos F, Posso S, Silveira LF, Betini GS, Carrano E, Franz I, Lees AC, Lima LM, Pioli D, Schunck F, Amaral FR, Bencke GA, Cohn-Haft M, Figueiredo LFA, Straube FC, Cesari E (2015) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Revista Brasileira de Ornitologia 23: 91-298.).

We used Mountford’s dissimilarity index (Wolda 1981Wolda H (1981) Similarity Indices, Sample Size and Diversity. Oecologia 50: 296-302.) to perform a hierarchical cluster analysis (HCA) and a Principal Coordinate Analysis (PCoA) to compare the bird communities from Serra da Cantareira with other AF regions. After calculating the Mountdord’s index using presence/absence data with the vegdist function in the R package vegan (Oksanen et al. 2016Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: Community Ecology Package. https://CRAN.R-project.org/package=vegan [Acessed: 18/03/2016]
https://CRAN.R-project.org/package=vegan...
), we performed the HCA using the Ward’s minimum variance criterion as the objective function, the results of which define which clusters merge at each step (Ward Jr 1963Ward Jr JH (1963) Hierarchical Grouping to Optimize an Objective Function. Journal of the American Statistical Association 58: 236-244. https://doi.org/10.1080/01621459.1963.10500845
https://doi.org/10.1080/01621459.1963.10...
). The HCA and the PCoA were performed using the hclust and ordiplot functions (Oksanen et al. 2016Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: Community Ecology Package. https://CRAN.R-project.org/package=vegan [Acessed: 18/03/2016]
https://CRAN.R-project.org/package=vegan...
, R Core Team 2016R Core Team (2016) R: A language and environment for statistical computing, R Foundation for Statistical Computing. Available online at: Available online at: https://www.R-project.org/ [Accessed: 18/03/2016]
https://www.R-project.org/...
). We also calculated the Jaccard dissimilarity index using the function vegdist (Oksanen et al. 2016Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: Community Ecology Package. https://CRAN.R-project.org/package=vegan [Acessed: 18/03/2016]
https://CRAN.R-project.org/package=vegan...
). The Jaccard coefficient ranges from 0 (identical pairwise) to 1 (totally different pairwise) and it is a robust index to ascertain similarity among groups (Krebs 1999Krebs CJ (1999) Ecological Methodology. Addison-Welsey Educational Publisher, Menlo Park, 642 pp.).

We compared bird communities between Serra da Cantareira and the following AF regions that also have dense ombrophilous forest: Boraceia Biological Station (Cavarzere et al. 2010Cavarzere V, Moraes GP, Silveira LF (2010) Boracéia Biological Station: an ornithological review. Papéis Avulsos de Zoologia 50: 189-201. https://doi.org/10.1590/S0031-10492010001300001
https://doi.org/10.1590/S0031-1049201000...
), Carlos Botelho State Park (Antunes 2013Antunes AZ (2013) Aves do Parque Estadual Carlos Botelho. Biota Neotropica 13: 124-140. https://doi.org/10.1590/S1676-06032013000200012
https://doi.org/10.1590/S1676-0603201300...
), Intervales State Park (Antunes et al. 2008bAntunes AZ, Menezes GV, Eston MR (2008b) Avifauna. In: Furlan SA, Leite SA (Eds) Parque Estadual de Intervales: plano de manejo. São Paulo, Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, 122-138.), Morro Grande Reserve (Develey and Martensen 2006Develey PF, Martensen AC (2006) As aves da Reserva do Morro Grande (Cotia, SP). Biota Neotropica 6: 1-16. https://doi.org/10.1590/S1676-06032006000200008
https://doi.org/10.1590/S1676-0603200600...
), Municipality of Ilha Comprida (Gussoni 2010Gussoni COA (2010) Novas informações sobre a história natural da maria-da-restinga (Phylloscartes kronei) (Aves, Tyrannidae). Master dissertation, Universidade Estadual Paulista Júlio de Mesquita Filho, Rio Claro. Available online at: Available online at: https://repositorio.unesp.br/bitstream/handle/11449/99487/gussoni_coa_me_rcla.pdf?sequence=1&isAllowed=y [Acessed: 19/03/2016]
https://repositorio.unesp.br/bitstream/h...
), Municipality of Ubatuba (Simpson et al. 2012Simpson R, Cavarzere V, Simpson E (2012) List of documented bird species from the municipality of Ubatuba, State of São Paulo, Brazil. Papéis Avulsos de Zoologia 52: 233-254.), and in Serra da Mantiqueira, where the vegetation is predominantly mixed ombrophilous forest: Campos do Jordão (composed by the Mananciais de Campos do Jordão and Campos do Jordão State Parks; Willis and Oniki 1981Willis EO, Oniki Y (1981) Levantamento preliminar de aves em treze áreas do estado de São Paulo. Revista Brasileira de Biologia 41: 121-135. https://doi.org/10.1007/BF00344966
https://doi.org/10.1007/BF00344966...
) and Itatiaia National Park (Barreto et al. 2013Barreto CG, Campos JB, Roberto DM, Schwarzstein NT, Alves GSG, Coelho WC (2013) Plano de manejo: Parque Nacional do Itatiaia. Instituto Chico Mendes de Conservação da Biodiversidade, Ministério do Meio Ambiente, Brasília, 215 pp.), as well as regions of semi-deciduous forest: Barreiro Rico Ecological Station (Antunes 2005Antunes AZ (2005) Alterações na composição da comunidade de aves ao longo do tempo em um fragmento florestal no sudeste do Brasil. Ararajuba 13: 47-61.), Caetetus Ecological Station (Tabanez et al. 2005Tabanez MF, Durigan G, Keurogkian A, Barbosa AF, Freitas CA, Silva CEF, Silva DA, Eaton EP, Brisolla G, Faria HH, Mattos IFA, Lobo MT, Barbosa MR, Rossi M, Souza MG, Machado RB, Pfeifer RM, Ramos VS, Andrade WJ, Contiere WA (2005) Plano de Manejo da Estação Ecológica dos Caetetus. IF, Série Registros 29: 1-104., Cavarzere et al. 2009Cavarzere V, Moraes GP, Donatelli RJ (2009) Avifauna da Estação Ecológica dos Caetetus. Papéis Avulsos de Zoologia 49: 477-485.), Mata dos Godoy State Park (Anjos 2001Anjos L (2001) Bird communities in five Atlantic forest fragments in southern Brazil. Ornitología Neotropical 12: 11-27.), Morro do Diabo State Park (Uezu and Metzger 2016Uezu A, Metzger JP (2016) Time-Lag in Responses of Birds to Atlantic Forest Fragmentation: Restoration Opportunity and Urgency. PLoS ONE 11: e0147909. https://doi.org/10.1371/journal.pone.0147909
https://doi.org/10.1371/journal.pone.014...
), Porto Ferreira (composed by Porto Ferreira and Vassununga State Parks, Uezu and Gaban-Lima 2003Uezu A, Gaban-Lima R (2003) Anexo 3: espécie de aves registradas na região do Parque Estadual de Porto Ferreira (incluindo a estação experimental e estação ecológica de Jataí e o Parque Estadual de Vassununga). In: Tabanez MF, Zanchetta D (Eds) Plano de Manejo do Parque Estadual de Porto Ferreira. Secretaria do Meio Ambiente do Estado de São Paulo, Instituto Florestal, São Paulo, 16-23.) and Rio Claro Farm (Donatelli et al. 2004Donatelli RJ, da Costa TVV, Ferreira CD (2004) Dinâmica da avifauna em um fragmento de mata na Fazenda Rio Claro, Lençóis Paulista, São Paulo, Brasil. Revista Brasileira de Zoologia 21: 97-114. https://doi.org/10.1590/S0101-81752004000100017
https://doi.org/10.1590/S0101-8175200400...
). In addition to the references cited above, to complement lists of birds from those regions, we also used records from WikiAves and Xeno-Canto databases (WikiAves 2016WikiAves (2016) A enciclopédia das aves do Brasil. http://ww.wikiaves.com.br [Acessed: 19/03/2016]
http://ww.wikiaves.com.br...
, Xeno-Canto 2016Xeno-Canto (2016) Xeno-Canto, compartilhando sons de aves do mundo todo. http://www.xeno-canto.org [Acessed: 19/03/2016]
http://www.xeno-canto.org...
). Most of those regions are or incorporate large conservation areas (reserves) where bird richness is high. Additionally, whenever possible, we also compiled records from patches surrounding the parks and reserves, to better characterize the avifauna, in the same manner that we did for Serra da Cantareira. These regions are ~230 km distant from our study area (50 km the nearest and 600 km the farthest; Fig. 2). For comparisons, we ignored seabirds records for Boracéia Biological Station and municipalities of Ilha Comprida and Ubatuba (e.g. the Magnificent Frigatebird Fregata magnificens [Mathews, 1914]) as well as exotic species, such as the House Sparrow Passer domesticus (Linnaeus, 1758), and birds from other regions in Brazil that escaped or were intentionally released from captivity (e.g. the Yellow-rumped Cacique Cacicus cela [Linnaeus, 1758]).

Figure 2
Dendogram with Atlantic Forest regions based on their bird community using Hierarchical Cluster Analysis (Mountford’s distance coefficient; a) and the Principal Coordinate Analysis of these areas (b). 1 = Morro do Diabo State Park; 2 = Mata dos Godoy State Park; 3 = Caetetus Ecological Station; 4 = Rio Claro Farm; 5 = Intervales State Park; 6 = Barreiro Rico Ecological Station; 7 = Carlos Botelho State Park; 8 = Ilha Comprida; 9 = Morro Grande Reserve; 10 = Porto Ferreira (Porto Ferreira and Vassununga State Parks); 11 = Serra da Cantareira; 12 = Boracéia Biological Station; 13 = Campos do Jordão (composed by Mananciais de Campos do Jordão and Campos do Jordão State Parks); 14 = Ubatuba; 15 = Itatiaia National Park.

RESULTS

Overall, 326 species were found at Serra da Cantareira, including seven exotic species, e.g. the Rock Pigeon Columba livia (Gmelin, 1789), or species that may have escaped from captivity, such as the Red-cowled Cardinal Paroaria dominicana (Linnaeus, 1758). For nine species with previous records for Serra da Cantareira there have been no further records for the last two decades, and 55 species records are not adequately documented (through either museum specimen, photograph or song record; Appendix 1). Additionally, nine questionable literature records of bird species, for instance the Vinaceous Parrot Amazona vinacea (Kuhl, 1820), were not included in this report (Appendix 2). Non-passerines accounted for 138 species in 32 families and passerines are represented by 188 species in 34 families (Piacentini et al. 2015Piacentini VQ, Aleixo A, Agne CE, Maurício GN, Pacheco JF, Bravo GA, Brito GRR, Naka LN, Olmos F, Posso S, Silveira LF, Betini GS, Carrano E, Franz I, Lees AC, Lima LM, Pioli D, Schunck F, Amaral FR, Bencke GA, Cohn-Haft M, Figueiredo LFA, Straube FC, Cesari E (2015) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Revista Brasileira de Ornitologia 23: 91-298.). Tyrannidae was the most representative family (35 species), followed by Thraupidae (33) and Furnariidae (18). AF endemics accounted for 24.5% of the records according to Lima’s (2013Lima LM (2013) Birds of the Atlantic Forest: richness, compostion, status, endemism, and conservation. Master dissertation, Universidade de São Paulo, São Paulo. http://www.teses.usp.br/teses/disponiveis/41/41133/tde-17042014-091547/pt-br.php [Acessed: 19/03/2016]
http://www.teses.usp.br/teses/disponivei...
) classification and 227 are forest birds (Parker et al. 1996Parker TAI, Stotz DF, Fitzpatrick JW (1996) Ecological and Distributional Databases. In: Stotz DF, Fitzpatrick JW, Parker TAI, Moskovits DA (Eds) Neotropical Birds: Ecology and Conservation. The University of Chicago Press, Chicago, 133-293.). Seven species recorded in our study area are globally threatened (BirdLife 2016BirdLife International (2016) IUCN Red List for Birds. http://www.birdlife.org [Accessed: 19/03/2016]
http://www.birdlife.org...
); five are threatened in Brazil (MMA 2014MMA (2014) Lista de espécies ameaçadas. Ministério do Meio Ambiente. http://www.icmbio.gov.br [Accessed: 18/03/2016]
http://www.icmbio.gov.br...
) and 17 in the state of São Paulo (São Paulo 2014São Paulo (2014) Decreto n° 60.133, de 7 de Fevereiro de 2014. Declara as espécies da fauna silvestre ameaçadas de extinção, as quase ameaçadas e as deficientes de dados para avaliação no Estado de S. Paulo e dá providências correlatas. http://www.al.sp.gov.br/repositorio/legislacao/decreto/2014/decreto-60133-07.02.2014.html [Accessed: 18/03/2016]
http://www.al.sp.gov.br/repositorio/legi...
). The ornithological knowledge of Serra da Cantareira has increased significantly since Graham’s study. Only 71 birds were reported before 1992Graham DJ (1992) The Avifauna of the Serra da Cantareira, São Paulo, Brazil: A preliminary survey. IF, Série Registros 10: 1-56., all represented by museums specimens (Fig. 3). Records exclusively from the authors of this study contributed to add four species (Appendix 1). Species in the urban slope accounted for most records (Table 1).

Figure 3
Number of species reported by different sources during different periods in Serra da Cantareira. Museums: specimens deposited in ornithological collections between 1901 and 1992; Graham: Graham 1992Graham DJ (1992) The Avifauna of the Serra da Cantareira, São Paulo, Brazil: A preliminary survey. IF, Série Registros 10: 1-56.; Authors: species recorded by the authors during unsystematic surveys; WA: WikiAves 2016WikiAves (2016) A enciclopédia das aves do Brasil. http://ww.wikiaves.com.br [Acessed: 19/03/2016]
http://ww.wikiaves.com.br...
; XC: Xeno-Canto 2016Xeno-Canto (2016) Xeno-Canto, compartilhando sons de aves do mundo todo. http://www.xeno-canto.org [Acessed: 19/03/2016]
http://www.xeno-canto.org...
; Recent literature: Figueiredo and Loo 2000Figueiredo LFA, Loo VK (2000) Lista das aves do município de São Paulo. Boletim do CEO 14: 15-35., Develey and Endrigo 2004Develey PF, Endrigo E (2004) Guia de Campo - Aves da Grande São Paulo. Editora Aves e Fotos, São Paulo, 295 pp., Fonseca and Antunes 2007Fonseca FY, Antunes AZ (2007) Frugivoria e predação de sementes por aves no Parque Estadual Alberto Löfgren, São Paulo, SP. Revista do Instituto Florestal 19: 81-91., Antunes et al. 2008aAntunes AZ, dos Santos AMR, Eston MR (2008a) Registros relevantes de aves para a grande São Paulo obtidos no Parque Estadual da Cantareira (Nota Científica). Revista do Instituto Florestal 20: 221-224., 2008bAntunes AZ, Menezes GV, Eston MR (2008b) Avifauna. In: Furlan SA, Leite SA (Eds) Parque Estadual de Intervales: plano de manejo. São Paulo, Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, 122-138., 2009Antunes AZ, Wyrgun B, Eston MR (2009) Composição das comunidades de aves em duas florestas secundárias contíguas no sudesde do Brasil. Revista do Instituto Florestal 21: 93-106., Antunes and Eston 2009Antunes AZ, Eston MR (2009) Anexo 10: espécies de aves registradas no PEC. In: Leonel C, Déscio F, Mazzei K, Leite MO, Barros MIA (Eds). Parque Estadual da Cantareira: plano de manejo. São Paulo, Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, 1-10., 2012Antunes AZ, Eston MR (2012) Anexo 8: espécies de aves registradas no PEAL. In: Arromba AL, Leonel C, Santiago CM, Mazzei K, Bucci LA, Nalon MA, Barros MIA (Eds) Parque Estadual Alberto Löfgren: plano de manejo. Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, São Paulo, 1-10., Minns et al. 2009Minns JC, Buzzetti DRC, Albano CG, Whittaker A, Grosset AE, Parrini R (2009) Birds of Brazil/Aves do Brasil. Aves Brasilis Editora, Vinhedo, DVD-ROOM., Dersa 2010DERSA (2010) Programa Rodoanel Mario Covas, Trecho Norte: Estudo de Impacto Ambiental. Volume IV. Desenvolvimento Rodoviário S/A, Consórcio JPGP-PRIME, São Paulo, 451 pp., Ikuta and Martins 2013Ikuta KG, Martins FC (2013) Interação entre aves frugívoras e plantas no Parque Estadual da Cantareira, estado de São Paulo. Atualidades Ornitológicas 172: 33-36., Lemos 2014Lemos RF (2014) Avifauna da Reserva Particular do Patrimônio Natural (RPPN) Sítio Capuavinha, município de Mairiporã, São Paulo. Atualidades Ornitológicas 179: 38-45., Cavarzere and Tonetti 2015Cavarzere V, Tonetti VR (2015) Complete leucism in the Fawn-breasted Tanager Pipraeidea melanonota (Aves: Thraupidae). Boletim do Museu de Biologia Prof. Mello Leitão 37: 233-240.. All recent encompasses records obtained in recent literature cited above as well as specimens deposited in museuns after the work performed by Graham (1992Graham DJ (1992) The Avifauna of the Serra da Cantareira, São Paulo, Brazil: A preliminary survey. IF, Série Registros 10: 1-56.) and species recorded by the authors.

Table 1
Number of species recorded in the different slopes of Serra da Cantareira. Urban slope corresponds to species recorded in Cantareira and Alberto Löfgren State Parks. Inner slope corresponds to species recorded in the slope faced to inner Atlantic forest in A1, A3, A4, A5 and the private reserve Sítio Capuavinha. In this table we did not take into account species which the location pointed only to Serra da Cantareira.

HCA showed two major groups of areas, separated according to their bird communities. One is in a macro-region where the vegetation is predominantly ombrophilous dense or ombrophilous mixed forest near the coast, and comprises the following areas: Boracéia Biological Station, Campos do Jordão, Serra da Cantareira, Carlos Botelho and Intervales State Parks, Ilha Comprida, Itatiaia National Park, Morro Grande Reserve and Ubatuba. The other group, encompassing more inland areas, has lower rainfall rates with seasonal semi-deciduous forests and includes: Barreiro Rico Biological Station, Caetetus Ecological Station, Mata dos Godoy State Park, Morro do Diabo State Park, Porto Ferreira and Rio Claro Farm (Fig. 2). The bird community of Serra da Cantareira is more similar to a clade composed of Boracéia Biological Station, Carlos Botelho and Intervales state parks and Morro Grande Reserve (Fig. 1a) according to HCA. According to the Jaccard index the bird community of Serra da Cantareira is more similar to Carlos Botelho State Park, while Pontal do Parapanapanema has a more distinct avifauna (Table 2). Although the ombrophilous mixed forests, represented here by Campos do Jordão and Itatiaia National Park, are more related to ombrophilous dense forests according to HCA, they form a separated clade within this major group (composed by areas 13 and 15, Fig. 2a). The PCoA also showed two regions of ombrophilous mixed forests that are more related to ombrophilous dense forests in the first dimension, while in the coordinate 2 they were more distant from other omborphilous dense forest areas (Fig. 2b).

Table 2
Areas compared with Serra da Cantareira in multivariate analysis using presence/absence bird species data. spp. = number of species reported; Distance (km) = distance in kilometers from our study area; Jaccard = Jaccard dissimilarity index, the lower the number, the greater the similarity in avifauna composition with Serra da Cantareira. Areas with avifauna most (Carlos Botelho State Park) and least (Morro do Diabo State Park) similar to Serra da Cantareira are indicated in bold.

DISCUSSION

Our results are consistent with other ornithological compilations conducted at Boracéia Biological Station, which is an AF reserve located at Serra do Mar, 75 km distant from Serra da Cantareira, and where the vegetation is also dense mountain rain forest (Fig. 2). Cavarzere et al. (2010Cavarzere V, Moraes GP, Silveira LF (2010) Boracéia Biological Station: an ornithological review. Papéis Avulsos de Zoologia 50: 189-201. https://doi.org/10.1590/S0031-10492010001300001
https://doi.org/10.1590/S0031-1049201000...
) performed transect counts, mist netting and unsystematic surveys at the station, where they recorded 242 bird species. After accounting for museums specimens, literature records, and records provided by birdwatchers, 323 species were reported for that reserve, 30% of which are endemic to the AF (Cavarzere et al. 2010Cavarzere V, Moraes GP, Silveira LF (2010) Boracéia Biological Station: an ornithological review. Papéis Avulsos de Zoologia 50: 189-201. https://doi.org/10.1590/S0031-10492010001300001
https://doi.org/10.1590/S0031-1049201000...
, Lima 2013Lima LM (2013) Birds of the Atlantic Forest: richness, compostion, status, endemism, and conservation. Master dissertation, Universidade de São Paulo, São Paulo. http://www.teses.usp.br/teses/disponiveis/41/41133/tde-17042014-091547/pt-br.php [Acessed: 19/03/2016]
http://www.teses.usp.br/teses/disponivei...
). This suggests that ornithological reviews provide a more comprehensive knowledge on the actual bird diversity of a given region than localized surveys, even when using different methodologies and intensive sampling effort.

Some records of species for Serra da Cantareira are based on only one source of information (records from the authors, those provided by birdwatchers, reported in the literature or represented by museums specimens; Fig. 3), e.g. the Gray-bellied Hawk Accipiter poliogaster (Temminck, 1824). This bird was only recently spotted by the authors and had not been previously recorded there. Despite its broad-range distribution (north Colombia to south Brazil, and more recently found in Costa Rica and Panama), this species is considered uncommon and is sparsely found throughout its range (Bierregard et al. 2016Bierregard RO, Christie DA, Kirwan G (2016) Grey-bellied Goshawk (Accipiter poliogaster). In: del Hoyo J, Elliot A, Sargatal J, Christie DA, de Juana E (Eds) Handbook of the birds of the world alive. Available online at: Available online at: http://www.hbw.com/node/53041 [Acessed: 27/05/2016]
http://www.hbw.com/node/53041...
). VRT first recorded a juvenile at Cabuçu (a CSP administrative zone; Fig. 1) on May 5, 2014. On that day, the birds’ vocalization was recorded.

The high number of species recorded by birdwatchers (76% of all species compiled in this study, ten of which reported only by them; Appendix 1) highlights the importance of public websites where digital vouchers can be deposited, such as WikiAves (http://www.wikiaves.com) and Xeno-Canto (http://www.xeno-canto.org). Among the records provided only by these databases is the Shrike-like Cotinga Laniisoma elegans (Thunberg, 1823) (WA1076770). This frugivorous bird, found mostly in old-growth forests, was photographed in a forest edge at the Engordador administrative CSP zone. Birds recorded only in the literature accounted for 13 species, such as the Rufous-tailed Attila Attila phoenicurus Pelzeln, 1868, song-recorded at Cabuçu (Minns et al. 2009Minns JC, Buzzetti DRC, Albano CG, Whittaker A, Grosset AE, Parrini R (2009) Birds of Brazil/Aves do Brasil. Aves Brasilis Editora, Vinhedo, DVD-ROOM.). The Rufous-tailed Attila breeds in southeast Brazil during the austral winter, and is found in greater numbers in Serra do Mar (Walther 2016Walther B (2016). Rufous-tailed Attila (Attila phoenicurus). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (Eds) Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. http://www.hbw.com/node/57521 [Acessed: 27/05/2016]
http://www.hbw.com/node/57521...
), being uncommon in our study area (pers. obs.).

Although museum records until 1992 did not account for 80% of the species in Serra da Cantareira, some relevant birds were reported only until that year. The most noticeable is the Purple-winged Ground-Dove Claravis geoffroyi (Temminck, 1811) collected in 1937 at a CSP site named “Cuca” (MZUSP 17040; Fig. 1). It was once a fairly common and widely distributed species (occurring from Bahia [Brazil] south through eastern Brazil to northern Argentina and eastern Paraguay). During the last three decades, however, there have beeen only a few non-documented records of this globally “Critically Endangered” AF endemic species (MMA 2014MMA (2014) Lista de espécies ameaçadas. Ministério do Meio Ambiente. http://www.icmbio.gov.br [Accessed: 18/03/2016]
http://www.icmbio.gov.br...
, BirdLife 2016BirdLife International (2016) IUCN Red List for Birds. http://www.birdlife.org [Accessed: 19/03/2016]
http://www.birdlife.org...
). Claravis geoffroyi feeds on bamboo seeds (Guadua sp.), and most likely travels far in search for flowering events (Sick 1997Sick H (1997) Ornitologia brasileira. Editora Nova Fronteira, Rio de Janeiro, 912 pp., Areta et al. 2009Areta JI, Bodrati A, Cockle K (2009) Specialization on guadua bamboo seeds by three bird species in the Atlantic forest of Argentina. Biotropica 41: 66-73. https://doi.org/10.1111/j.1744-7429.2008.00458.x
https://doi.org/10.1111/j.1744-7429.2008...
). Guadua spp. have synchronous masting events in cycles of ~30 y, attracting birds that eat their seeds, such as the Buffy-fronted Seedeater Sporophila frontalis (Verreaux, 1869) and the Temminck’s Seedeater S. falcirostris (Temminck, 1820), both registered at Serra da Cantareira and globally threatened (Areta et al. 2009Areta JI, Bodrati A, Cockle K (2009) Specialization on guadua bamboo seeds by three bird species in the Atlantic forest of Argentina. Biotropica 41: 66-73. https://doi.org/10.1111/j.1744-7429.2008.00458.x
https://doi.org/10.1111/j.1744-7429.2008...
, BirdLife 2016BirdLife International (2016) IUCN Red List for Birds. http://www.birdlife.org [Accessed: 19/03/2016]
http://www.birdlife.org...
). As Guadua sp. bamboo tickets are common in several parts of Serra da Cantareira (Bencke et al. 2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp.; pers. obs.), we suggest that those searching for the Purple-winged Ground-Dove should try to locate flowering events of that bamboo.

Due to severe forest loss and human intervention at Serra da Cantareira, it is possible that local extinctions have occurred, but they are difficult to document. For example, Cavarzere et al. (submitted) recorded the Squamate Antbird Myrmoderus squamosus (Pelzeln, 1868) after a 190-y time span from the last confirmed record at the Ipanema National Forest, an AF reserve 100 km from our study area. This is a good example of imperfect detection and insufficient sampling effort (Mackenzie et al. 2003Mackenzie DI, Nichols JD, Hines JE, Knutson MG, Franklin AB (2003) Estimating site occupancy, colonization, and local exticntion when a specie is detected imperfectly. Ecology 84: 2200-2207. https://doi.org/10.1890/02-3090
https://doi.org/10.1890/02-3090...
). The Spot-billed Toucanet Selenidera maculirostris (Lichtenstein, 1823) is an example of a species recently recorded at Serra da Cantareira after 45 y without records. Six specimens were collected in 1965 (MZUSP 60592 to 60597), and after it, the only confirmed record was provided by MAR and his team in A5 (Fig. 1).

More important than accounting for local bird extinctions per se is identifying functional extinctions and their impact on the ecosystem. Habitat disturbance is one of the main drivers of functional extinctions of sensitive guilds, such as understory insectivorous and large-bodied frugivorous (Martensen et al. 2012Martensen AC, Ribeiro, MC, Banks-Leite C, Prado PI, Metzger JP (2012) Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance. Conservation Biology 26: 1100-1111. https://doi.org/10.1111/j.1523-1739.2012.01940.x
https://doi.org/10.1111/j.1523-1739.2012...
, Galetti et al. 2013Galetti M, Guevara R, Côrtes MC, Fadini R, Von Matter S, Leite AB, Labecca F, Ribeiro T, Carvalho CS, Collevatti RG, Pires MM, Guimarães PR, Brancalion PH, Ribeiro MC, Jordano P (2013) Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size. Science 340: 1086-1090. https://doi.org/10.1126/science.1233774
https://doi.org/10.1126/science.1233774...
, Morante-Filho et al. 2015Morante-Filho JC, Faria D, Mariano-Neto E, Rhodes JR (2015) Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic forest. PLoS ONE 10: e0128923. https://doi.org/10.1371/journal.pone.0128923
https://doi.org/10.1371/journal.pone.012...
). It is very possible that, of the currently rarest species in our study area - e.g. the Saffron Toucanet Pteroglossus bailloni (Vieillot, 1819), a large-bodied frugivorous, and the Speckle-breasted Antpitta Hylopezus nattereri (Pinto, 1937), an understory insectivorous - were more abundant in the past, given their presence in museums collections. Declines in the populations of these birds have been recorded in other AF regions due to habitat disturbances (Guix et al. 2000Guix JC, Martín M, Hernandéz A, Souza FL (2000) Conservation status of the Saffron Toucanet (Baillonius bailloni, Ramphastidae): a new case of population isolation and depletion in South America. Grupo de Estudos Ecológicos, Série Documentos 6: 10-25., Anjos 2006Anjos L (2006) Bird species sensitivity in a fragmented landscape of the Atlantic forest in southern Brazil. Biotropica 38: 229-234. https://doi.org/10.1111/j.1744-7429.2006.00122.x
https://doi.org/10.1111/j.1744-7429.2006...
), and since they participate in key-ecological processes (e.g. seed dispersal), the consequences of their functional extinctions should be better investigated.

In contrast with the decreasing populations of some species in response to habitat disturbances, species that benefit from altered environments are expected to expand their ranges and increase their abundance. Graham (1992Graham DJ (1992) The Avifauna of the Serra da Cantareira, São Paulo, Brazil: A preliminary survey. IF, Série Registros 10: 1-56.), using point-counts (37 hours of sampling effort) between December 11th 1985 and March 29th 1986, did not record any individual of the White-eyed Parakeet Psittacara leucophthalmus (Statius Muller, 1776) within the CSP, although this species has been frequently recorded in our study area over the last decade. The White-eyed Parakeet benefits from deforestation and occupies forest edges and areas of open vegetation, and its presence in AF is an indication of environmental degradation (Sick 1997Sick H (1997) Ornitologia brasileira. Editora Nova Fronteira, Rio de Janeiro, 912 pp.). Increases in the numbers of generalist bird species, together with decreases in the numbers of sensitive species, have also been reported for other large and protected AF remnants after a 30-y time span - at the Caetetus Ecological Station (Cavarzere et al. 2012Cavarzere V, Marcondes RS, Moraes GP, Donatelli RJ (2012) Comparação quantitativa da comunidade de aves de um fragmento de floresta semidecidual do interior do Estado de São Paulo em intervalo de 30 anos. Iheringia 102: 384-393. https://doi.org/10.1590/S0073-47212012000400004
https://doi.org/10.1590/S0073-4721201200...
; 2,800 ha, Fig. 2).

Biogeographic affinities

Similarly to a study on the plants of Serra da Cantareira, our results indicate that the local avifauna is associated more strongly with dense ombrophilous forest areas, to a lesser extent to mixed ombrophilous forest and to an even lesser extent to seasonal semi-deciduous forests (Salis et al. 1995Salis SM, Shepherd GJ, Joly CA (1995) Floristic comparison of mesophytic semideciduous forests of the interior of the state of São Paulo, Southeast Brazil. Vegetatio 119: 155-164. https://doi.org/10.1007/BF00045595
https://doi.org/10.1007/BF00045595...
; Fig. 2a, Table 2). The Black-backed Tanager Tangara peruviana (Desmarest, 1806) and the Olive-green Tanager Orthogonys chloricterus (Vieillot, 1819) are typical of the dense omborphilous forest species of Serra da Cantareira that occur predominantly near the coast. However, birds commonly found in seasonal semi-deciduous forests, such as the Southern Antpipit Corythopis delalandi (Lesson, 1830), were also recorded. This understory insectivorous species has been song-recorded only once by the MAR team at the administrative zone of Pedra Grande at CSP. In order to maintain the genetic flow and evolutionary processes between these three types of vegetation, the stablishment of forest corridors uniting them is crucial. Forest patches are important in facilitating bird dispersal over landscapes and can help to connect larger AF remnants (Ribeiro et al. 2009Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: 1141-1153. https://doi.org/10.1016/j.biocon.2009.02.021
https://doi.org/10.1016/j.biocon.2009.02...
).

Conservation

In addition providing information on the bird community of Serra da Cantareira, our results reinforce the relevance of the area for birds. Bencke et al. (2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp.) estimated an avifauna richness of 250 species for the region and reported 65 AF endemics and four globally threatened species, less than the numbers provided by us (326, 80 and seven respectively). Although located at an urban matrix and composed mostly of secondary forest, Serra da Cantareira accounted for 17% of all species recorded in Brazil (Piacentini et al. 2015Piacentini VQ, Aleixo A, Agne CE, Maurício GN, Pacheco JF, Bravo GA, Brito GRR, Naka LN, Olmos F, Posso S, Silveira LF, Betini GS, Carrano E, Franz I, Lees AC, Lima LM, Pioli D, Schunck F, Amaral FR, Bencke GA, Cohn-Haft M, Figueiredo LFA, Straube FC, Cesari E (2015) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Revista Brasileira de Ornitologia 23: 91-298.) and 36.7% in AF (Lima 2013Lima LM (2013) Birds of the Atlantic Forest: richness, compostion, status, endemism, and conservation. Master dissertation, Universidade de São Paulo, São Paulo. http://www.teses.usp.br/teses/disponiveis/41/41133/tde-17042014-091547/pt-br.php [Acessed: 19/03/2016]
http://www.teses.usp.br/teses/disponivei...
). Moreover, it is a stronghold for populations of some species that are suffering a sharp decline in several other AF regions, for instance the Solitary Tinamou Tinamus solitarius (Vieillot, 1819), currently found mostly in large forest remnants such as those in Serra do Mar (BirdLife 2016BirdLife International (2016) IUCN Red List for Birds. http://www.birdlife.org [Accessed: 19/03/2016]
http://www.birdlife.org...
) and also an abundant bird in our study area (Bencke et al. 2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp., pers. obs.), as well as the Southern Bristle-tyrant Phylloscartes eximius (Temminck, 1822), a passerine that was once broadly distributed but now is found only in a few places (Silveira 2009Silveira LF (2009) Phylloscates eximius (Temminck, 1822). In: Bressan PM, Kierulff MCM, Sugieda AM (Eds) Fauna ameaçada de extinção no estado de São Paulo: vertebrados. Fundação Parque Zoológico de São Paulo, Secretaria do Meio Ambiente, São Paulo, 223., Tonetti and Pizo 2016Tonetti VR, Pizo MA (2016) Density and microhabitat preference of the Southern Bristle-tyrant (Phylloscartes eximius): Conservation policy implications. The Condor: Ornithological Applications 118: 791-803. https://doi.org/10.1650/CONDOR-16-89.1
https://doi.org/10.1650/CONDOR-16-89.1...
).

Despite differences in sampling effort, we found that the avifauna composition of CSP and that of the inner slope patches are similar (Appendix 1), corroborating the hypothesis that even fragmented landscapes with high levels of forest cover can maintain similar species richness to areas of continuous forest (Martensen et al. 2012Martensen AC, Ribeiro, MC, Banks-Leite C, Prado PI, Metzger JP (2012) Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance. Conservation Biology 26: 1100-1111. https://doi.org/10.1111/j.1523-1739.2012.01940.x
https://doi.org/10.1111/j.1523-1739.2012...
, Morante-Filho et al. 2015Morante-Filho JC, Faria D, Mariano-Neto E, Rhodes JR (2015) Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic forest. PLoS ONE 10: e0128923. https://doi.org/10.1371/journal.pone.0128923
https://doi.org/10.1371/journal.pone.012...
). This supports the idea that forest patches surrounding Serra da Cantareira should be protected, since they can act as corridors between our study area and other large AF remnants, such as those in Serra da Mantiqueira and Serra do Mar (Fig. 2). Since seasonal semi-deciduous forests have been more extensively devastated than ombrophilous and mixed forests, there are only a few seasonal semi-deciduous forest remnants that are larger than 500 ha with weakly connected patches (Ribeiro et al. 2009Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: 1141-1153. https://doi.org/10.1016/j.biocon.2009.02.021
https://doi.org/10.1016/j.biocon.2009.02...
), which means that genetic flow between Cantareira birds and those that inhabit the inner AF can be seriously compromised.

Similarly to Serra da Cantareira, other large (15,700 ha) urban forests, in the city Rio de Janeiro City, the Tjuca National Forest and the Pedra Branca State Park, have high bird richness (325 species; Lepage 2016Lepage D (2016) Parque Nacional da Tijuca, Rio de Janeiro. Avibase - Bird Checklists of the World. http://avibase.bsc-eoc.org/checklist.jsp?region=BRrj01 [Accessed: 19/03/2016]
http://avibase.bsc-eoc.org/checklist.jsp...
), and are also considered Important Bird Areas (IBA RJ07, Bencke et al. 2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp.), with seven globally threatened species. This highlights the importance of such reserves, which despite the high levels of anthropic pressure, harbor a significant portion of our biodiversity. As in our study area, the main threats to the Tijuca National Forest are urban sprawl, and the impacts of large infrastructure projects in the surrounding cities (Bencke et al. 2006Bencke GA, Maurício GN, Develey PF, Goerck JM (2006) Áreas importantes para a conservação das aves no Brasil: parte 1 - estados do domínio da Mata Atlântica. SAVE Brasil, São Paulo, 494 pp.).

When it comes to infrastructure, roads cause one of the largest disturbances in urban forests. Their intense noise can cause changes in the foraging behavior of birds, hinder intra and inter-specific communication, and cause chronic stress. The animals, in turn, become more prone to diseases and their reproductive success is reduced (Ortega 2012Ortega CP (2012) Effects of noise pollution on birds: a brief review of our knowledge. Ornithological Monographs 74: 6-22. https://doi.org/10.1525/om.2012.74.1.6
https://doi.org/10.1525/om.2012.74.1.6...
). There is one highway (Fernão Dias, BR-116) and tree paved roads with intense traffic crossing CSP (da Silva et al. 2009da Silva DA, Pavão M, Fernandes A, Zuquim ML, Miaciro K, Gaspareto TC, Veiga MF (2009) Avaliação do meio antrópico. In: Leonel C, Déscio F, Mazzei K, Leite MO, Barros MIA (Eds) Parque Estadual da Cantareira: plano de manejo . Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, São Paulo, 145-222.). In addition to this, the northern section of Rodoanel Mário Covas (SP-21) will be operating soon (DERSA 2010DERSA (2010) Programa Rodoanel Mario Covas, Trecho Norte: Estudo de Impacto Ambiental. Volume IV. Desenvolvimento Rodoviário S/A, Consórcio JPGP-PRIME, São Paulo, 451 pp.; Fig. 1). This new highway is being built close to the boundaries of CSP and ALSP, crossing the first in some sections via tunnels, and will represent a new threat to the biodiversity of Serra da Cantareira (Ayres 2008Ayres ACM (2008) O Ciclo da Caapora: A RMSP e o Parque da Cantareira. Annablume, São Paulo, 120 pp., da Silva et al. 2009da Silva DA, Pavão M, Fernandes A, Zuquim ML, Miaciro K, Gaspareto TC, Veiga MF (2009) Avaliação do meio antrópico. In: Leonel C, Déscio F, Mazzei K, Leite MO, Barros MIA (Eds) Parque Estadual da Cantareira: plano de manejo . Secretaria de Estado de Meio Ambiente, Instituto Florestal, Fundação Florestal, São Paulo, 145-222., DERSA 2010DERSA (2010) Programa Rodoanel Mario Covas, Trecho Norte: Estudo de Impacto Ambiental. Volume IV. Desenvolvimento Rodoviário S/A, Consórcio JPGP-PRIME, São Paulo, 451 pp.; Fig. 1). As a strategy to mitigate the damage caused by those roads, we suggest the incorporation of forest remnants to the CSP, especially those large patches in the west portion of the Park, and near Cuca (Fig. 1).

ACKNOWLEDGEMENTS

We thank the staff of Cantareira State Park for logistic assistance; the scientific technical committee (COTEC) which authorized VRT to work on the Park (proc. 260108-007.094/2013); Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for collecting permits; the Brazilian National Council for Scientific and Technological Development (CNPq) which provided a scholarship to VRT (proc. 130279/2013-7) and for grants and financial support to LFS; people who contribute in the maintenance as well as providing their personal records to WikiAves and Xeno-Canto databases; MAR team: Aline Correa, Fernanda Alves, Fernanda Bocalini, Giuliana Althman, Glaucia Del Rio, Leo Signorini, Rafael Marcondes, Thiago Vernaschi and Vagner Cavarzere. We are also indebted with Tatiana Pongiluppi. Fernanda Alves helped with the English. Maria de Fátima Rodrigues funded part of this research.

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  • Editorial responsibility:

    Walter A.P. Boeger

  • Zoobank:

    http://zoobank.org/D811F345-6865-4000-B2F7-0E025BDADA2C

APPENDIX 1

Appendix 1
Species recorded in Serra da Cantareira. Bird families are in capital letters and in bold with the number of species in parenthesis. Nomenclature followed the Brazilian Ornithological Records Committee classification (Piacentini et al. 2015); ªtl = Atlantic Forest endemics (Lima 2013); F° = forest species (Parker et al. 1996); SP = species threatened in São Paulo state (São Paulo 2014); BR = species threatened in Brazil (MMA 2014); GL = globally threatened species (BirdLife 2016); * = birds lacking documented records (museum specimen, picture or song record); = species without recent records (i.e. after Graham 1992); Locality = specific location where each species were recorded; ALSP = Alberto Löfgren State Park; CSP = Cantareira State Park, including the locality “estrada do lenhador”; Patch = species recorded in the inner slope patches (A1, A3, A4, A5 and the private reserve Sítio Capuavinha); Serra Cantareira = species recorded in Serra da Cantareira and where the specific location was not pointed; Source = record source; 1 = authors’ records during unsystematic surveys; 2 = systematic surveys (fixed-points[100 h sample effort]) performed by Vinicius R. Tonetti in CSP; 3 = systematic study (line transect [80 h] and mist-nest [2,600 nest-hours]) performed by Marco A. Rego along with other researches (names in Acknowledgements) in A1-A5; 4 = records from literature; 5 = museum specimens; 6 = species in WikiAves and/or Xeno-Canto databases.

APPENDIX 2

Appendix 2
Species reported for Serra da Cantareira and pending confirmation. * = Birds pending confirmation according to Graham (1992); ‡ = Species only reported in Figueiredo and Loo (2000) and without any further mention, possibly escaped or intentionally released from captivity; CSP = Cantareira State Park; ALSP = Alberto Löfgren State Park.

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    28 June 2016
  • Reviewed
    12 Jan 2017
  • Accepted
    21 Jan 2017
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