Boracéia Biological Station : an ornithological review

Boracéia Biological Station, near the city of Salesópolis, SP, is located in one of the most welldefined centers of endemism in eastern Brazil – the Serra do Mar Center. While the station was established only in 1954 under the auspices of the Museu de Zoologia da Universidade de São Paulo, the avifauna of this locality had already attracted the attention of ornithologists by the 1940s, when the first specimens were collected. Here we describe the ornithological history of the Boracéia Biological Station with a review of all the bird species recorded during more than 68 years, including recent transect and mist-netting records. Boracéia’s records were found in museums, literature and unpublished reports that totaled 323 bird species when recent data is also considered. Of these, 117 are endemic to the Atlantic forest and 28 are threatened in the state. Although there are a few doubtful records that need to be checked, some species are the only sightings in the state. Boracéia includes a recently discovered species near the station site and is extremely important for the conservation of Atlantic forest birds.


IntroductIon
The region of Brazil that is considered Atlantic forest originally comprised an almost continuous zone of several forest types along the Brazilian coast from the state of Rio Grande do Norte in the north to the state of Rio Grande do Sul in the south (Silva et al., 2004).The coastal mountains of the states of Rio de Janeiro, São Paulo, Paraná and Santa Catarina are known as the Serra do Mar (Almeida & Carneiro, 1998), in which is found an important biogeographical region that is also a well-defined center of endemism for many taxa, including birds (Müller, 1973;Haffer, 1974Haffer, , 1985;;Cracraft, 1985).At least 660 species of birds breed in the nonmarine Atlantic Forest Region, 200 (30%) of which are considered endemic (Goerck, 1997).
The greatest levels of endemism in the Atlantic forest are found in the Serra do Mar (Haffer, 1985) where the complex of mountains has influenced bird species composition (Silva et al., 2004).About 140 endemic species are passerine forest birds (Haffer, 1985) of which 88 species are in monotypic genera with no close relatives (Willis, 1992).Endemism is probably even greater because several putative subspecies may prove to be biological (BSC) and/or phylogenetic (PSC) species once detailed taxonomic studies have been carried out (Silveira et al., 2003).
Bird inventories are fundamental and valuable sources of information for conservation and often such knowledge can influence the creation of reserves and other conservation units as well as justify their existence.Therefore these areas may be the last hope for preservation of the rich and diverse Atlantic forest avifauna (Develey, 2004).
While over 60 years have passed since the earliest formal ornithological studies in the area of the Boracéia Biological Station, no concise summary of the avian fauna of the region yet exists, which makes such a summary long past due.Here, we describe the local community of birds and summarize the history of bird studies at the station.

MAterIAl And Methods study Area
Boracéia Biological Station (23°38'S, 45°52'W), established in 1954 (Travassos Filho & Camargo, 1958), is now administered by the Museu de Zoologia da Universidade de São Paulo (MZUSP).It is located near the city of Salesópolis, in the state of São Paulo, southeastern Brazil (Camargo, 1946).The station includes 96 ha of montane Atlantic forest (750-900 m) and is within the Casa Grande Reserve, which belongs to Departamento de Águas e Esgotos (DAEE) do Estado de São Paulo, part of the Serra do Mar State Park.Climate is wet tropical (Cfa; Köppen's classification), with uniform rainfall (average 2010 mm y -1 ) throughout the year and a hot summer (average temperature 17.9°C; Custódio Filho, 1989).

data collection reviews
We searched for all specimens that were collected in "Boracéia" and "Casa Grande" in the MZUSP collection as well as those of the Museu de Zoologia da Universidade Estadual de Campinas and the Coleção Ornitológica da Universidade Federal de Minas Gerais.Unpublished reports were also included and the visitor's registry book at the station.Unpublished data from collaborators and visits conducted by colleagues of the Departamento de Zoologia (USP), among others, were included and cited in the acknowledgements.

recent records
All birds we found during systematic field surveys were also included.As part of a larger on-going study, here we only included information from transect counts and mist-netting that were carried out from August 2008 -February 2010.Transects with unlimited distance were walked slowly beginning at dawn along dirt roads running through the station.Mist-nets (10; 12 m x 2.5 m x 30 mm) were placed on five different 1.5-4 m wide trails at least 1 km apart.Nets were open around 6:30 AM and closed only after 5:00 PM, though earlier during inclement weather.Collected specimens were deposited at the MZUSP and tape recordings with Panasonic RQ-L31, at the Arquivo Sonoro do Laboratório de Ornitologia da Universidade de São Paulo.

And dIscussIon
During 68 years, 323 bird species were found at Boracéia Biological Station.Non-passerines accounted for 117 species in 32 families while Passerines comprised the remaining 206 species in 26 families.Forest species were > 60% of all bird species, 116 (36%) of which are endemic to the Atlantic forest (Parker et al., 1996;Appendix).Boracéia has about 18% of all bird species recorded in Brazil (CBRO, 2008), 41% in the state of São Paulo (Silveira et al., 2009) and 48% in the Atlantic forest (Goerck, 1997).This diversity and endemism is similar to that found elsewhere in the Serra do Mar of São Paulo (Höfling & Lencioni, 1992;Goerck, 1999;Develey, 2004) and in other nearby mountain ranges, such as Serra de Paranapiacaba (Vielliard & Silva, 1994).The difference in the counts at Boracéia is the smaller elevational gradient (200 m).

registry for Visitors
Investigators and birdwatchers who wrote their observations in the station comment book included 34 species.

specimens collected
The first specimens collected in the station (housed at MZUSP) were from 1942 by J.L. Lima and E. Dente on 13 April and 17 September.Following this early start, several researchers have worked at the station and a fine collection has been amassed over the years.The first extensive collections were by H.F.A. Camargo and E. Dente in the mid 1940s.Important contributors were D. Seraglia, L. D'Amico, L. Travassos Filho, M. Ventell, W. Bokermann, E.X.Rabelo, F. Novaes, J.L. Silva, P. Schwartz, D.F. Stotz, and others who collected from 1945 through 1992.No collections date from the 1980s.After the contributions of D.F. Stotz in 1992, F.S.R. Amaral and V. Cavarzere both added to the collections.Today, the MZUSP collection includes 784 specimens of a total of 147 species.Adding specimens collected in Casa Grande from the other museums, the total Boracéia collection includes 906 specimens in 159 species.
A.M. Olalla collected four individuals at "Boracéia, Estado de São Paulo" on 30 January and 7 September 1963 and on 23 May 1964 which might have come from Boracéia Beach, in the city of Bertioga, and were thus excluded from our analyses.

Publications
Birds from Boracéia first entered the scientific literature with a study by Camargo (1946), with collections dating from 1-12 November 1945.This first bird list included 84 species, of which 62 were sent to MZUSP.During a short, preliminary visit between 31 August and 7 September 1977, Willis & Oniki (1981) found 132 bird species.A few years later, the same Willis & Oniki (2003) included another 11 species here, some of which may also have included species found elsewhere, and were not included in the species list herein.

other sources and recent records
Many ornithologists contributed with bird lists produced over 20 years at Boracéia.These included sporadic visits and birdwatching trips.During our recent field trips, we recorded 242 bird species during approximately 270 transect hours and 920 mistnetting hours; 19 species were not recorded before, of which three are Atlantic forest endemics: two forest species (Sporophila frontalis and S. falcirostris) and another of campos de altitude (Knipolegus nigerrimus).
Numbers of species recorded during such expeditions and years they were conducted are presented in Table 1.

doubtful records
Four species were each reported only once and need to be checked.While climbing down the slopes of the Serra do Mar, E. Dente was said to have heard the fading whistle of the Black-and-gold Cotinga (Tijuca atra; Camargo, 1946).This species, known from higher altitudes and found only in northern São Paulo, has never been seen or heard since.Instead, perhaps it was a Sharpbill (Oxyrunchus cristatus) which is a common species on those lower slopes (V.Cavarzere, pers. obs.).Camargo (1946) collected a putative female Rusty-backed Antwren (Formicivora rufa) which was destroyed by the shot and thus not prepared and deposited in MZUSP.This species is usually found in open, dry habitats (Sick, 1997) and clearly does not belong to the avifauna of Boracéia.Certainly it was instead a recently discovered species related to the Marsh Antwren (Stymphalornis acutirostris; Buzzetti et al., in prep.) and collected near the station.Females of the new species and of Rusty-backed Antwren have similar plumage and may indeed be in the same genus, thus explaining the confusion by H.F.A. Camargo.Another example is the Canebrake Groundcreeper (Clibanornis dendrocolaptoides) reported by D.F. Stotz.The only documented record of this species from São Paulo was questioned by Willis & Oniki (2003), who suggested it was from the state of Paraná.Simon et al., 2008), of swampy areas which are very common around the station.We have only noted this latter species at Boracéia.A.M. Olalla probably collected the following species at Boracéia Beach: Charadrius collaris, Chiroxiphia caudata and Parula pitiayumi.We did not include these here because C. collaris was never seen at Boracéia, yet is quite common on the beach in the city of Bertioga (V.Cavarzere, pers.obs.).We followed the same rules with respect to Willis & Oniki (2003) who noted Calidris pusilla, Amazilia fimbriata, Drymophila squamata and Cantorchilus longirostris.Although the hummingbird was seen at the station by D.F. Stotz, these species are typically found in aquatic environments or lower elevation Atlantic forest sites and may have come from the homonymous beach instead of the reserve.D.F. Stotz reported a few interesting low elevation sightings: Leucopternis lacernulatus, Ramphodon naevius, Amazilia fimbriata, Trogon viridis, Myrmotherula unicolor, Formicarius colma, Hemitriccus orbitatus, Phylloscartes paulista and Tachyphonus cristatus.We have documented only R. naevius, T. viridis and M. unicolor.
Two Boracéia species include the only sightings in the state of São Paulo: Swainson's Thrush Catharus ustulatus (specimen collected by E. Dente) and the Cerulean Warbler Dendroica cerulea.We did not see these boreal migrants and they deserve more attention to document their status.

threatened species
Boracéia has 28 species that are considered threatened in the state (Silveira et al., 2009), seven species threatened in Brazil (MMA, 2003), and nine globally threatened species (IUCN, 2007;Appendix).At least 88 species, 77% of all threatened bird species in Brazil, are from the Atlantic forest (BirdLife International, 2003).It is shocking that this incredible bird diversity includes so many threatened species and unlike the Amazon forest, where large blocks of primary vegetation can be set aside as preserves, the long-term survival of Atlantic forest birds will depend on conservation of the remaining fragments (Goerck, 1997) that will become ecological refuges for many of these species.
We found that 323 bird species were reported during 68 years at Boracéia.Many of these are threatened or endemic to the Atlantic forest and several others should be considered for future study so that their status may be confirmed.This incredible diversity must be monitored in long-term studies to understand theoretical issues, such as ecological interactions and evolution of the bird communities of the Atlantic forest, as well as conservation issues and to insure that threatened species are adequately monitored and to confirm doubtful records.

tAble 1 :
Number of species recorded by and years in which investigators conducted bird surveys on Boracéia Biological Station, state of São Paulo, Brazil.
J. Minns' sighting of Red-eyed Thornbird (Phacellodomus erythrophthalmus) may have been a recently split taxon, Orange-eyed Thornbird (P.ferrugineigula; BoracéiaBiological Station is an extremely important site for Atlantic forest bird study and conservation in the state of São Paulo.