Birds from cerradão woodland, an overlooked forest of the Cerrado region, Brazil

The Cerrado region still receives relatively little ornithological attention, although it is regarded as the only tropical savanna in the world considered to be a biodiversity hotspot. Cerradão is one of the least known and most deforested Cerrado physiognomies and few recent bird surveys have been conducted in these forests. In order to rescue bird records and complement the few existing inventories of this under-studied forest type in the state of São Paulo, we looked for published papers on birds of cerradão. Additionally we surveyed birds at a 314-ha cerradão remnant located in central São Paulo, Brazil, from September 2005-December 2006 using unlimited distance transect counts. Out of 95 investigations involving cerradão bird studies, only 17 (18%) investigations teased apart bird species recorded inside cerradão from those recorded in other physiognomies of Cerrado. Except for one study, no research found more than 64 species in this type of forest, a result shared within many regions from Brazil and Bolivia. Differences in species richness do not seem be related with levels of disturbance of landscape or fragment size. Considering all species recorded in cerradão in Brazil and Bolivia, a compilation of data accumulated 250 species in 36 families and 15 orders. In recent surveys at central São Paulo, we recorded 48 species in 20 families, including the Pale-bellied Tyrant-Manakin Neopelma pallescens, threatened in São Paulo, and the Helmeted Manakin Antilophia galeata, near threatened in the state and endemic to the Cerrado region. Among the most abundant species inside this fragment, none was considered to be neither threatened nor endemic. Key-Words: Cerrado sensu lato; Endemic species; Peripheral Cerrado areas; Transect counts. Volume 51(17):259‐273, 2011 1. Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, no 101, CEP 05508-900, São Paulo, SP, Brasil. Corresponding author e-mail: cavarzere@usp.br 2. Departamento de Ciências Biológicas, Universidade Estadual Paulista. Rua Engenheiro Luiz Edmundo Carrijo Coube, 14-01, CEP 17033-360, Bauru, SP, Brasil. 3. Instituto de Biociências, Universidade Estadual Paulista. Rua José Barbosa de Barros, 1780, Caixa Postal 510, CEP 18618-000, Botucatu, SP, Brasil. 4. Current address: Seção de Aves, Museu de Zoologia da Universidade de São Paulo. Avenida Nazaré, 481, CEP 04218-970, São Paulo, SP, Brasil.


IntroductIon
Cerrado is the only tropical savanna among the 34 biodiversity hotspots of the world (Mittermeier et al., 2005), and represents one of the richest but most poorly known South American ecological regions (Silva, 1995).It is the second largest biome in the continent and includes most of central Brazil and parts of northeastern Paraguay and eastern Bolivia (Ab'Saber, 1977).Many physiognomies occur throughout Cerrado, such as gallery forests, marshlands and Cerrado sensu lato.The latter, strictly considered as the Cerrado Biome (Coutinho, 2006), includes four open physiognomies (Cerrado sensu stricto, campo Cerrado, campo sujo and campo limpo) and cerradão (Eiten, 1972).
Two Cerrado physiognomies have distinct aspects: cerradão, where arboreal and shrubby components predominate, as opposed to campo limpo, where herbaceous and sub-arboreal components are more evident (Coutinho, 1978).Cerradão is the tallest Cerrado phytogeographical sub-unit, and its trees usually average less than 15 m in height, accounting for a continuous and relatively closed canopy; it occurs in seasonal tropical climates (Eiten, 1972;Veloso et al., 1991;Andrade et al., 2002) and can be distinguished from dry forests by its physiognomy (there are no grasses, for example) and floristic structure (Rizzini, 1976).
Currently the Cerrado region has less than 20% of its original vegetation undisturbed (Myers et al., 2000).In 1962, all of the phytophysiognomical forms of Cerrado vegetation occupied 13.7% of its original area in the state of São Paulo (Borgonovi & Chiarini, 1965).In 1974, these values reduced to only 4.2% (Serra Filho et al., 1975) and at the end of the last decade, the original vegetation cover comprised 11.5% distributed in less than 7,505 fragments of Cerrado sensu stricto, cerradão and campo cerrado (Kronka et al., 2005).Formerly covering 14% of São Paulo, this domain has now less than 1% of original vegetation in this state (Durigan et al., 2004).
In this paper we review all published papers to date listing Cerrado birds and additionally we present recent data on the avifauna of a cerradão fragment from the central-western region of the state of São Paulo, Brazil.Our aims were to acknowledge on whether researchers have properly distinguished cerradão birds (species occurring inside cerradão and not those found temporally using different habitats around it) instead of simply mentioning the birds from "Cerrado habitats", as well as to provide a new account of cerradão birds for the state.

literature review
We found papers, thesis and books on Cerrado birds by searching Web of Knowledge (http:// sub3.isiknowledge.com) and Google Scholar (http:// scholar.google.com.br) using combination of key words or title words: aves, avifauna, birds, Cerrado and cerradão.
The matrix landscape around this fragment is greatly modified and composed of two small lakes, early stage regenerating secondary growth and anthropogenic habitats.The cerradão is also near an alluvial forest (1 ha) and surrounds a 5-ha seasonal semi-deciduous forest.

data collection
We surveyed the cerradão fragment every 15 days from September 2005-December 2006 using unlimited-distance transect counts.We started field work at sunrise, interrupted our surveys two hours before midday and continued from 15:00 until dusk.The same observers always visited ca.30% of the fragment (including both edges and its interior) due to locations of pre-existing transect lines.We observed birds using Nikon binoculars (8 × 42; 8 × 20) and some vocalizations were recorded with a Panasonic RQ-L31 (built-in microphone) cassette recorder We estimated species richness using nonparametric randomization estimators (Chao2 and Jack2) to evaluate potential variation in sampling effort using the software EstimateS 8.2 (Colwell, 2009).A species accumulation curve was calculated by randomizing sample accumulation order 50 times with Estimates 8.2.We used the goodness-of-fit G test to compare distribution of number of species during the months we surveyed cerradão and to analyze differences between (non)disturbed habitats.The Mann-Whitney test was used to compare medians of ranked sizes of cerradão remnants with species richness.We further compared bird species richness between different cerradão inventories using the Sørensen incidence-based similarity index (Chao et al., 2005).We estimated abundance by counting birds per 100 h of observations (see Willis & Oniki, 1981).Scientific nomenclature followed the Comitê Brasileiro de Registros Ornitológicos (CBRO, 2010).
results And dIscussIon literature We found 95 papers listing Cerrado birds.Among these studies, 37 (39%) did not survey cerradão (habitats included semi-deciduous forests or Cerrado sensu lato), while another 41 (43%) sampled cerradão but never teased apart birds occupying other habitats from birds occupying cerradão.Only 17 (18%) papers surveyed cerradão or studied cerradão birds and distinguished all birds recorded inside this forest.These latter investigations could be further divided into three categories: qualitative lists, surveys (or species accounts) and biology studies.Qualitative lists accounted for five studies (29%), surveys summed up six investigations (35%) and biology studies accounted for the remainder (36%).Lopes & Braz (2007) reported the Black Hawk-Eagle Spizaetus tyrannus from cerradão while discussing Cerrado noteworthy bird records.Although Olmos & Boulhosa (2000) recorded the Bicolored Conebill Conirostrum bicolor at cerradões from the municipality of Assis, São Paulo, we decided to exclude this undocumented species as it is typical of mangroves.We used those information to generate a list of bird species that have actually been recorded using cerradão as habitat.Studies that mentioned birds from cerradão were developed in 49 municipalities and two South American countries (Figure 1).This compilation accumulated 250 species in 36 families and 15 orders (Appendix).The complete set of references compiled for this review is available upon request.

bauru cerradão
Over a total of 190 h and approximately 90 km of transects, we recorded 48 species of 20 families only at cerradão (Appendix), which represented 5% of all bird species recorded for the Cerrado region (Silva, 1995;Silva & Santos, 2005).The randomized cerradão species accumulation curve rose quickly at first but tended to level off towards an asymptote five months before the end of the survey (Figure 2).Nonparametric species richness estimators Chao2 and Jack2 predicted 48.19 and 48.36 species, respectively.As no new species were detected prior to the end of the survey, and the predicted species richness were exactly the same as the empirical value, we concluded that the majority of bird species was recorded at our fragment.
Other studies that have discriminated birds recorded in the matrix habitat from cerradão birds obtained similar values of species richness.Therefore, bird species richness observed here ( 48) is considered to be low only if compared with gallery forests or Cerrado sensu stricto (Bagno & Marinho Filho, 2001).Furthermore, our species richness did not represent a sample artifact.We always recorded few species in cerradão (21 ± 4.56; mean ± SE) throughout the months we conducted this survey, and species richness was not greater during any particular month of the year than expected by chance (G = 10.62,df = 31, P = 0.224).Values of species richness of different bird inventories conducted in cerradão, as well as their sampling methods, can be seen in Table 1.They are only slightly different in spite of differences in sampling effort and field method.Only biology studies, basically fauna-flora interactions, accounted for fewer species.Mist-netting results accounted for the lowest richness values (mean = 38.3species), while qualitative lists and transects seemed to record more species (61.2 and 52, respectively).It was an expected result due to the limitations of mist net sampling (Karr, 1981), which do not represent the entire community.Almeida (1979) was one of the earliest researchers looking for differences on bird diversity between natural and man-made habitats, such as Eucalyptus plantations, in Brazil.His results yielded 31 species from cerradões in São Paulo, but also may have suffered from mist-netting limitations.Silva & Oniki (1988) surveyed for a short period of time a greatly modified cerradão fragment at Mato Grosso State, Brazil, but they could still record as many species as the present survey.Fry (1970) and Parker & Remsen Jr. (1993) also found roughly the same species richness at Mato Grosso and Bolivia, respectively, as other investigators have found in different cerradões.Fry (1970), however, based his cerradão list mainly on mist-netting data.As a result, many species that failed to be netted were not represented in his study, probably artificially decreasing his species richness.Using mist nets at Mato Grosso do Sul State, Brazil, Piratelli & Blake (2006) were able to record 39 species.These authors only mentioned those species with more than five captures.Willis (2006) recorded 56 species in São Paulo when border and flying over species are excluded.Manica et al. (2010) found 29 species in a cerradão remnant in São Paulo, but this cerradão was the least visited habitat by the authors.
Antunes (2010) and Santos et al. (2010) found 64 and 110 species occurring in cerradão.Some of this species may not use the forest itself, but be present in nearby habitats, such as the White-tailed Kite Elanus leucurus and Red-legged Seriema Cariama cristata.Furthermore, the latter authors surveyed three different cerradão fragments without discriminating the records of each locality.This may have inflated the overall number of species by the addition of many species present uniquely in one fragment.
Considering habitat level of disturbance given by these authors (Table 1), species richness did not seem to be related with landscape modifications where one would expect to find more species in undisturbed environments and matrix habitats (G = 2.36, df = 1, P = 0.125).Excluding biology studies, which would compromise this following analysis, size of remnant did not show an expected pattern either.Fragments larger than 500 ha (Table 1) did not harbor more species than smaller remnants (U = 4.5, P = 0.592).
Species richness composition greatly differed between our study and those obtained from other cerradões from Brazil and Bolivia.Cerradões from São Paulo obtained the highest similarity values, while São Paulo and Mato Grosso shared few species (Table 2).This is partly explained because many typical Amazonian elements of central Brazil's gallery forests are absent in São Paulo (Silva, 1996).Another reason is due to the transversal distribution pattern of the avifauna of central regions of the country.In peripheral areas, these species reach only the westernmost Cerrado of São Paulo (Sick, 1965).Furthermore, Atlantic Forest species, such as Hylophilus poicilotis (song recorded), absent in studies from Mato Grosso, Mato Grosso do Sul and Bolivia, also influenced and contributed for the low similarity values.
It would be expected to find more similarities between cerradões from São Paulo, whereas species richness should be less similar between central and peripheral areas of the Cerrado region.Although the sampling efforts differed considerably in these studies and comparing them seems inappropriate, these patterns were nonetheless corroborated (Table 2).Similarity indexes were highest between the municipalities of Bauru and Corumbataí, São Paulo (Willis, 2006), and lowest between Amazonia-influenced Serra do Roncador, Mato Grosso (Fry, 1970) and Agudos, São Paulo (Almeida, 1979).There were no species shared among all of the analyzed inventories, but some tended to be present in most locations, such as the Flavescent Warbler Basileuterus flaveolus, a very common species of both cerradões and semi-deciduous forests from the Cerrado domain (Sick, 1997).
We found that the 10 most abundant species during our survey at Bauru were Turdus leucomelas, Basileuterus flaveolus, Patagioenas picazuro, Brotogeris chiriri, Vireo olivaceus, Myiodynastes maculatus, Leptotila verreauxi, Thamnophilus pelzelni, Picumnus albosquamatus and Herpsilochmus atricapillus (Appendix).None of them is considered neither threatened nor endemic and only one (T.pelzelni) was exclusively recorded inside cerradão.These forests do not harbor a significant amount of typical Cerrado birds, a result constantly shared with other surveys analyzed herein (Appendix).
We recorded one species endemic to the Cerrado region (Silva, 1995;Appendix) that is also near threatened with extinction in the state of São Paulo (Helmeted Manakin Antilophia galeata).This species is typically found at Cerrado gallery forests (Sick, 1997) and in our study site it was rarely recorded in cerradão.Many individuals, however, could be detected in the nearby semi-deciduous forest.We recorded one vulnerable species in the state (Silveira et al., 2009;Appendix), the Pale-bellied Tyrant-Manakin Neopelma pallescens.It was never commonly recorded, but it may have gone unnoticed several times as it was inconspicuous at the fragment.Mato Grosso, Brazil (Fry, 1970) São Paulo, Brazil (Manica et al., 2010) Mato Grosso, Brazil (Silva & Oniki, 1988) Santa Cruz, Bolivia (Parker & Remsen Jr., 1993) Mato Grosso do Sul, Brazil (Piratelli & Blake, 2006) Maranhão, Brazil (Santos et al., 2010) São Paulo, Brazil (Willis, 2006) São Paulo, Brazil (Almeida, 1979)  Three species (Baryphthengus ruficapillus, Automolus leucophthalmus and Hylophilus poicilotis) are considered to be Atlantic Forest endemics (Parker et al., 1996).In spite of suitable habitat in the 5-ha semi-deciduous forest, these birds were seen several times foraging far from it and inside the cerradão itself.These species are also recorded in other Cerrado localities from São Paulo (Willis & Oniki, 2003) and in the case of B. ruficapillus, even in forests of the Cerrado region (Straube & Bornschein, 1991).The same is valid for the Violet-capped Woodnymph Thalurania glaucopis and Rufous-capped Spinetail Synallaxis ruficapilla, both recorded by Willis (2006), Surucua Trogon Trogon surrucura, recorded by Antunes (2010), and Black Jacobin Florisuga fusca, recorded from São Paulo Cerrado landscapes (Motta-Junior et al., 2008;Ubaid et al., in prep.).Despite present in semi-deciduous forests, which share many Atlantic Forest elements (Silva, 1996), these seven species have been reported from peripheral areas of the Cerrado domain and we hereby suggest they should have their Atlantic Forest endemic status reevaluated.
Cerradão harbors fewer bird species compared to Cerrado sensu stricto or gallery forests as every available survey indicates that rarely more than 64 species use cerradão as permanent habitat.Furthermore, few Cerrado endemics were recorded from cerradões surveyed at Cerrado localities in Brazil and abutting countries.It is extremely important to preserve cerradão as much of its extent has been reduced in the state of São Paulo without proper bird surveys having been conducted.Besides conservation of threatened species, such as N. palescens, there should be more emphasis on the importance and urgency to conduct surveys in these scientifically under-explored and threatened forests, especially in Cerrado peripheral areas (Motta-Junior et al., 2008).Cerradões must be considered as part of the diversity and environmental heterogeneity of Cerrado as birds use its different physiognomies on a seasonal basis.Therefore, all such physiognomies must readily be conserved.
Many problems can arise from the confusing terminologies of cerradão.Among the papers analyzed, this type of forest has been called dry forest, deciduous forest, Cerrado, dense cerrado, stunted forest and wooded cerrado.Some of them may not be suitable for properly identifying cerradão.Here we suggest that cerradão may be named hereafter as "cerradão woodland".We hope to motivate the continuity of bird monitoring in cerradão woodland, a very rare type of bird survey, in order to assess the diversity of these threatened habitats over time.

FIgure 1 :
FIgure 1: Locations (n = 49) where cerradão bird surveys have been conducted.An arrow indicates the region of Bauru, São Paulo State, southern Brazil.Cerrado is represented by light gray, while Pantanal is represented by dark gray.

FIgure 2 :
FIgure 2: Accumulation curve for number of bird species in relation to sample effort from a cerradão fragment in the municipality of Bauru, São Paulo State, Brazil.Sample accumulation order was randomized 50 times.

tAble 1 :
Location, number of species exclusively detected and field method used in several bird inventories conducted in cerradão woodland, Cerrado region, Brazil.When available by the study, habitat degradation (+ for very modified; -for less modified) and size of remnant (+ for larger than 500 ha; -for smaller than 500 ha) is given.

tAble 2 :
Sørensen incidence-based similarity indexes calculated for bird species richness in different cerradão woodlands from the Cerrado region of Brazil.