Patterns of geographic distribution and conservation of the open-habitat avifauna of southeastern Brazilian mountaintops (campos rupestres and campos de altitude)

Patterns of geographic distribution and conservation of the open-habitat avifauna of southeastern Brazilian mountaintops (campos rupestres and campos de altitude)

Marcelo Ferreira de Vasconcelos^I,*; Marcos Rodrigues^I,II

^IDepartamento de Zoologia, ICB, Universidade Federal de Minas Gerais, Caixa Postal 486, 30123-970, Belo Horizonte, MG, Brasil

^IIE-mail: [e-mail]

ABSTRACT

Montane open-habitats of southeastern Brazil are represented by the campos rupestres (principally in the Espinhaço Range) and by the campos de altitude (in the Serra do Mar and Serra da Mantiqueira). In spite of the occurrence of endemic species in both vegetation types, an analysis and synthesis of their bird communities have never been conducted. In this paper, we present an avifaunal survey of these areas, describe patterns of geographic distribution, and comment on the conservation of those open-habitats and their avifauna. A total of 231 bird species was recorded in the open-habitats of southeastern Brazilian mountaintops. In the campos rupestres, 205 species were recorded, while in the campos de altitude, the total was 123 species. Five patterns of distribution are recognizable among birds occurring in these habitats: non-endemic (191 species), Atlantic Forest endemics (26 species), Cerrado endemics (6 species), Caatinga endemic (1 species), and montane open-habitat endemics (7 species). In spite of the presence of several protected areas in those regions, the existing reserves do not guarantee the conservation of their important vegetation types and their avifaunas under current low levels of implementation. Since several endemic and threatened bird species live in the campos rupestres and campos de altitude, more efforts must be directed for their conservation.

Keywords: Avifauna; Campos rupestres; Campos de altitude; Conservation; Distribution.

RESUMO

Os ambientes abertos das montanhas do sudeste do Brasil são representados pelos campos rupestres (principalmente na Cadeia do Espinhaço) e pelos campos de altitude (nas Serras do Mar e da Mantiqueira). Apesar da ocorrência de espécies endêmicas em ambos os tipos de vegetação, uma análise e síntese de suas comunidades de aves nunca foram realizadas. Nesse estudo, apresentamos uma revisão da avifauna dessas áreas, descrevemos padrões de distribuição geográfica e comentamos sobre a conservação destes ambientes e de sua avifauna. Um total de 231 espécies de aves foi registrado nos ambientes abertos dos topos de montanha do sudeste do Brasil. Nos campos rupestres, 205 espécies foram registradas, enquanto nos campos de altitude o total foi de 123 espécies. Cinco padrões de distribuição são reconhecidos dentre as aves que ocorrem nestes habitats: não-endêmicas (191 espécies), endêmicas da Mata Atlântica (26 espécies), endêmicas do Cerrado (6 espécies), endêmica da Caatinga (1 espécie) e endêmicas dos habitats abertos dos topos de montanha (7 espécies). Apesar da presença de várias unidades de conservação nessas regiões, estas reservas não garantem a conservação de seus importantes tipos vegetacionais e de suas avifaunas sob os atuais níveis de gestão. Uma vez que várias espécies de aves endêmicas e ameaçadas de extinção vivem nos campos rupestres e campos de altitude, maiores esforços devem ser direcionados à sua conservação.

Palavras-chave: Avifauna; Campos rupestres; Campos de altitude; Distribuição; Conservação.

INTRODUCTION

Montane open-habitats in southeastern Brazil are recognized as important centres of endemism for Neotropical flora and fauna (Eiten, 1992; Silva, 1995, 1997, 1998; Giulietti et al., 1997; Sick, 1997; Stattersfield et al., 1998; Safford, 1999a; Silva & Bates, 2002; Gonçalves et al., 2007). Those habitats -generally occur at higher elevations than the Cerrado and the Caatinga in their northern and western distribution and above the tree line in the Atlantic Forest region to the south and east.

Montane open-habitats include the campos rupestres scattered along the Espinhaço Range and the campos de altitude dotting the ridges of the eastern mountains of the Serra do Mar, Serra da Mantiqueira, and associated ranges (Martinelli & Orleans e Bragança, 1996; Giulietti et al., 1997; Safford, 1999a; Menezes & Giulietti, 2000). Both habitats harbor a wide variety of physiognomies, ranging from open grasslands to habitats with a dense cover of scrub and small trees. Rock outcrops and marshy areas also occur in both formations, which have many typical and endemic plants, such as bromeliads (Bromeliaceae), "semprevivas" (Eriocaulaceae), "canelas-de-ema" (Velloziaceae), bamboos and grasses (Poaceae) (Andrade et al., 1986; Eiten, 1992; Meguro et al., 1994; Martinelli & Orleans e Bragança, 1996; Safford, 1999a; Menezes & Giulietti, 2000; Conceição & Giulietti, 2002; Benites et al., 2003; Caiafa & Silva, 2005; Conceição & Pirani, 2005; Ribeiro et al., 2007).

Although campos rupestres and campos de altitude can present similar landscapes and share some common plant genera and species, they show important differences in the biogeographic affinities of their floras (Menezes & Giulietti, 1986; Eiten, 1992; Harley, 1995; Martinelli & Orleans e Bragança, 1996; Giulietti et al., 1997; Rizzini, 1997; Safford, 1999a, 2007). The campos rupestres flora has affinities with those of central Brazilian Plateau, the Guianas Shield, and the restingas along the Atlantic Ocean coast of South America (Steyermark, 1986; Giulietti & Pirani, 1988; Giulietti & Hensold, 1990; Harley, 1995; Menezes & Giulietti, 2000; Alves, R.J.V. et al., 2007), but with a high number of endemic Bromeliaceae, Eriocaulaceae, Orchidaceae, and Velloziaceae (Eiten, 1992; Menezes & Giulietti, 2000; Versieux & Wendt, 2007).

On the other hand, campos de altitude show a remarkable affinity with the Andean region and also with southern Brazilian grasslands (Harley, 1995; Martinelli & Orleans e Bragança, 1996; Safford, 1999a, 2007). In fact, campos de altitude have been considered as 'Brazilian Páramos' because their floristic, physiognomic, climatic, and edaphic features are so similar to those of the Andes and the high Central American mountains (Harley, 1995; Safford, 1999a, b, 2007).

Furthermore, biogeographical affinities have been recognized between the flora and fauna of southeastern Brazilian mountains and the Andean-Patagonian region (Sick, 1970, 1985, 1997; Simpson-Vuilleumier, 1971; Simpson, 1979; Vielliard, 1990a, 1996; Safford, 1999a, 2007).

It is assumed that Brazilian mountains were colonized by Andean elements during Pleistocene glaciations, when climatic-vegetational connections between both regions were likely (Simpson-Vuilleumier, 1971; Simpson, 1979; Sick, 1970, 1985, 1997; Vielliard, 1990a). Those cooler periods would have led to the lowering of the tree line, increasing the latitudinal distribution of open-habitats in southeastern Brazil, similar to what is believed to have occurred in the Andean "páramos" (van der Hammen, 1974; Simpson-Vuilleumier, 1971; Simpson, 1979; Hooghiemstra & Cleef, 1995; Behling, 1998; Ledru et al., 1998; Safford, 1999a). Also, during Late Glacial times, subtropical grasslands expanded from latitudes of about 28º/27ºS to at least 20ºS (Behling, 2002). During interglacial periods, those montane habitats would have retreated to cooler upland areas, explaining the isolated occurrence of some Andean-Patagonian taxa on southeastern Brazilian mountaintops (Simpson, 1979; Safford, 1999a). This model supports the notion that the high-altitude avifauna of southeastern Brazil has a biogeographical influence of Andean-Patagonian elements, with the putative dispersion of those taxa from the Andes and Patagonia to southeastern Brazil during Quaternary glacial periods (Sick, 1970, 1985, 1997; Vielliard, 1990a, 1996; Willis, 1992).

Despite the occurrence of some endemic birds in the montane open-habitats of southeastern Brazil (Sick, 1970, 1985, 1997; Silva, 1995; Melo-Júnior et al., 1998; Stattersfield et al., 1998; Vasconcelos et al., 2003; Gonzaga et al., 2007; Vasconcelos, 2008b), their biogeography is poorly known, with only sparse surveys and checklists (e.g. Miranda-Ribeiro, 1906, 1923; Lüderwaldt, 1909; Peixoto-Velho, 1923a, b; Holt, 1928; Pinto, 1951, 1954; Willis & Oniki, 1991; Parrini et al., 1999; Simon et al., 1999; Vasconcelos, 1999a, 2003, 2008a; Melo-Júnior et al., 2001; Vasconcelos & Melo-Júnior, 2001). Bird communities from the campos rupestres and campos de altitude have never been subject to a thorough analysis and biogeographical synthesis. A good example of how poorly surveyed are these areas is the recent description of Formicivora grantsaui in the Chapada Diamantina (Gonzaga et al., 2007), a relatively well-known region (Funch, 1999; Parrini et al., 1999; Carvalhaes, 2001).

In his classic review of the physical environment and flora of the campos de altitude, Safford (1999a) recommended flora and fauna inventories as a first priority for research and conservation of this habitat. Following his lead, the goals of this paper are: 1) to review and present an ornithological synthesis of the campos rupestres and campos de altitude; 2) to describe patterns of geographic distribution of the montane open-habitat avifauna of southeastern Brazil; 3) to discuss the conservation of those habitats and their avifauna.

MATERIAL AND METHODS

We included in our survey those species that live in open natural habitats in the mountain areas of southeastern Brazil from Bahia south to São Paulo (Fig. 1). Those include marshes, grasslands, bamboo stands (Chusquea spp.), rocky outcrops covered with rupicolous herbs and shrubs, or with clumped shrubs and sparse low trees. Both campos rupestres and campos de altitude occur over a wide variety of rock substrates, such as granite, gneiss, quartzite, sandstone, and even iron ore. For physical and floristic characterizations of these habitats, see Andrade et al. (1986), Menezes & Giulietti (1986, 2000), Eiten (1992), Alves & Kolbek (1994), Meguro et al. (1994), Harley (1995), Martinelli & Orleans e Bragança (1996), Rizzini (1997), Safford (1999a), Conceição & Giulietti (2002), Dias et al. (2002), Benites et al. (2003, 2007), Vincent (2004), Caiafa & Silva (2005, 2007), Conceição & Pirani (2005), Conceição et al. (2007), Jacobi et al. (2007), and Ribeiro et al. (2007).

In this survey, we did not include species living strictly in forested habitats associated with the campos rupestres or the campos de altitude, such as gallery, cloud, and montane forests. Nevertheless, some typical forest birds do use dense clumps of shrubs or bamboos in those montane open-habitats (e.g. Mackenziaena leachii, Drymophila genei, Hemitriccus obsoletus, Phylloscartes difficilis, and Haplospiza unicolor), and they were included in this revision. We also excluded bird species that live only in the different physiognomies of the Cerrado, such as cerradão, cerrado "sensu stricto", parque de cerrado, and campo sujo (see Ribeiro & Walter, 1998 for a detailed description of these habitat types).

We selected different areas of campos rupestres and campos de altitude for our analysis (Fig. 1); the Chapada Diamantina region (Dias Coelho) was considered our northernmost site and Serra da Mantiqueira (Atibaia) the southern limit of the study area (Fig. 1). Localities surveyed in this study are summarized in Table 1. They were separated by mountain range (Espinhaço Range, Serra da Mantiqueira, and Serra do Mar) and type of habitat (campo rupestre or campo de altitude). All localities in the Espinhaço Range are covered by campos rupestres, and all localities in the Serra do Mar are represented by campos de altitude. The majority of the localities in the Serra da Mantiqueira are covered by campos de altitude, except Serra de São José and Serra do Lenheiro, which are covered by campos rupestres (see Alves & Kolbelk, 1994, 2009).

Due to the scarcity of data on birds of Brazilian montane open-habitats, we used all information gathered during fieldwork between 1993 and 2008. Voucher specimens were collected with mist-nets and shotguns, and deposited in the Coleção Ornitológica do Departamento de Zoologia da Universidade Federal de Minas Gerais, Belo Horizonte (DZUFMG). We also checked published bird records and data from specimens deposited in the following museums and collections: American Museum of Natural History, New York (AMNH); Museu de Biologia Mello Leitão, Santa Teresa (MBML); Museu de Ciências Naturais da Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte (MCN); Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre (MCP); Museu de História Natural de Taubaté, Taubaté (MHNT); Museu Paraense Emílio Goeldi, Belém (MPEG); Museu de Zoologia da Universidade de São Paulo, São Paulo (MZUSP); and Coleção Rolf Grantsau, São Bernardo do Campo (SG). In addition, we considered specimens deposited in the Museu Nacional, Rio de Janeiro (MNRJ), mentioned in the literature. We did not use published records by Ihering (1900) and Ruschi (1978, 1982b), since those authors did not mention the elevation and habitats where they recorded the species (see Remsen, 1994). Based on our field experience, we also did not include species only recorded in some published checklists not supported by physical evidence (specimens, photos or tape-recordings) since these records are possibly based on misidentifications. A list of all sources used in this revision is presented in Appendix 1.

Geographical distribution patterns for bird species were discussed based on: 1) our own fieldwork conducted in the following regions: Brazil (Pará, Maranhão, Ceará, Pernambuco, Tocantins, Bahia, Goiás, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina, Rio Grande do Sul), Peru (Ancash), Bolivia (Santa Cruz), and Argentina (Misiones); 2) specimens housed in the above mentioned institutions; and 3) literature review (see Appendix 1).

Taxonomy follows the Brazilian Committee of Ornithological Records (CBRO, 2007). Bird species were classified following their endemism after several authors (Ridgely & Tudor, 1989, 1994; Silva, 1995, 1997; Stotz et al., 1996; Sick, 1997; Stattersfield et al., 1998; Brooks et al., 1999; Silva & Bates, 2002; Silva & Santos, 2005). The exceptions are those typical species of the campos rupestres considered restricted to the Cerrado region (Silva, 1995; 1997; Silva & Bates, 2002; Silva & Santos, 2005). Here, they were considered endemics to the open-habitats of southeastern Brazilian mountaintops (following arguments presented by Vasconcelos et al., 2003; Lopes, 2008; Vasconcelos, 2008b). These species are Augastes scutatus, Asthenes luizae, Polystictus superciliaris, and Embernagra longicauda.

RESULTS AND DISCUSSION

Species richness and composition

A total of 231 bird species was recorded in the open-habitats of southeastern Brazilian mountaintops (Appendix 2). The list for the campos rupestres has a total of 205 species, while the campos de altitude has 123 species (Appendix 2). Ninety-seven species occur both in the campos rupestres and in the campos de altitude. One hundred and eight species were exclusive to the campos rupestres, while 26 species were recorded only in the campos de altitude (Appendix 2).

The higher species richness recorded in the campos rupestres can be attributed to the Espinhaço Range being in the contact zones among Atlantic Forest, Cerrado, and Caatinga (Giulietti & Pirani, 1988; Ab'Sáber, 1990; Harley, 1995; Giulietti et al., 1997). Such a variety of biomes within the Espinhaço Range leads to an increase in its species richness, especially because birds typical of the open-habitats of the Cerrado and semi-open-habitats of the Caatinga can also live in the campos rupestres (see Parrini et al., 1999; Vasconcelos & D'Angelo-Neto, 2007). By contrast, the campos de altitude can be considered as isolated islands of open-habitat among forested areas in the Atlantic Forest region. Since many forest bird species cannot live in open areas, colonization of the campos de altitude by species from nearby habitats is more difficult than in the campos rupestres. Low temperature, episodic frosts and even snow (Sick, 1970; Martinelli & Orleans e Bragança, 1996; Safford, 1999b) may also preclude permanent colonization by open-habitat birds found in lower altitudes that could use current man-made pastures to get there. Furthermore, campos rupestres areas are more naturally interconnected compared with the campos de altitude. This island feature of the campos de altitude could explain their lower species richness (MacArthur & Wilson, 1967). Meanwhile, more systematic surveys and area estimation based on satellite images are still necessary in order to test such hypothesis, as has been done for the northern Andes (Vuilleumier, 1970), Tepuis (Cook, 1974), and Sierras Pampeanas (Nores, 1995).

The differences in bird species composition between the campos rupestres and the campos de altitude, despite some species being common to both, demonstrate a pattern similar to that recognized for the flora (Safford, 1999a, 2007).

Geographic distribution patterns of the avifauna

Five patterns of distribution among the bird species occurring in the campos rupestres and campos de altitude can be recognized (Table 2):

- Non-endemic (191 species): Widespread species non-endemic to any biome.

- Atlantic Forest endemics (26 species): Species endemic to the Atlantic Forest region in southeastern Brazil and adjacent areas (eastern Paraguay, northeastern Argentina, and Uruguay).

- Cerrado endemics (6 species): Species restricted to the Cerrado region, except those typical of the campos rupestres, included here in another category (see materials and methods).

- Caatinga endemic (1 species): Species endemic to the Caatinga region in northeastern Brazil.

- Montane open-habitat endemics (7 species): Species endemic to the open-habitats of southeastern Brazilian mountaintops (campos rupestres and campos de altitude), including those restricted to campos rupestres (see above).

The highest proportion of the species living in southeastern Brazilian montane open-habitats is represented by widespread and non-endemic species (82.7%), with only 3.0% endemic to these habitats (Table 2). This is the opposite pattern of that found in the Andean puna and páramo, where 29% of the species are endemics and only 13.5% are widespread species (Vuilleumier, 1986). The high percentage of widespread bird species living in Brazilian montane open-habitats also contrasts to the local flora, which contains many endemic species (Eiten, 1992; Martinelli & Orleans e Bragança, 1996; Giulietti et al., 1997; Safford, 1999a; Menezes & Giulietti, 2000).

The distribution patterns of the birds from campos rupestres and campos de altitude show remarkable differences between both vegetation types. Although both formations show a dominance of wide-ranging species, their percentage is a little higher in the campos rupestres (85.9%) than in the campos de altitude (79.7%) (Table 2).

Atlantic Forest birds from southeastern Brazil and adjacent areas account for more species in the campos de altitude (17.1%) than in the campos rupestres (7.3%) (Table 2). The campos de altitude have 21 of the 26 Atlantic Forest endemics (80.8%) that have been recorded in the montane open-habitats of southeastern Brazil, while in the campos rupestres, there are only 15 (57.7%) (Table 2). The ranges of many Atlantic Forest species found in the campos de altitude do not reach northwest to the campos rupestres region. Some examples are: Stephanoxis lalandi, Drymophila genei, Scytalopus notorius, Hemitriccus obsoletus, Phylloscartes difficilis, Poospiza thoracica, and Saltator maxillosus. Nevertheless, some Atlantic Forest endemics do reach the campos rupestres, especially at localities in the southern Espinhaço Range (Vasconcelos et al., 1999b; Vasconcelos & Melo-Júnior, 2001) and their presence can be explained by the geographical proximity of this region to the coastal ranges. Such taxa include: Leucochloris albicollis, Muscipipra vetula, Tangara desmaresti, and Haplospiza unicolor.

Among the bird species restricted to the Atlantic Forest region, four show a distribution pattern associated with the highlands in southeastern Brazil, despite the fact that they also occur either in lowlands or highlands in subtropical regions of southern Brazil and adjacent areas (south of 23º30'S). Those species are: Stephanoxis lalandi, Scytalopus iraiensis, Stephanophorus diadematus, and Emberizoides ypiranganus.

This pattern was also recognized in some plant genera (Simpson, 1979; Safford, 1999a), bees (Silveira & Cure, 1993), and a rodent (Gonçalves et al., 2007), suggesting that these taxa probably had larger ranges during the Pleistocene (Simpson, 1979; Silveira & Cure, 1993; Safford, 1999a, 2007; Gonçalves et al., 2007). During interglacial periods, with the predominance of warmer climates, the ranges of these taxa would have retreated southward and upward, with the probable trapping of several taxa in the "glacial refugia" provided by the southeastern Brazilian mountaintops. In the case of S. diadematus, populations do not appear to be isolated, with possible connections throughout coastal São Paulo. Nevertheless, S. lalandi, S. iraiensis, and E. ypiranganus appear to have two main isolated population centers, one in the southeastern Brazilian mountains and another in forests and wetlands south of 23º30'S. We could not find any geographic variation in specimens of S. iraiensis and E. ypiranganus we collected in southeastern Brazilian highlands compared to southern specimens (see Vasconcelos et al., 2006, 2008a). Forest expansion over grasslands in southeastern Brazil appears to be recent (Behling, 2002) and this could explain the absence of morphological differentiation in those species.

Nevertheless, S. lalandi is represented by two very different subspecies: S. l. lalandi (southeastern Brazilian mountains) and S. l. loddigesii (lowlands and/or highlands south of 23º30'S). Since these geographical forms are morphologically distinctive, do not have any known intermediate specimen, and do not present any known range overlap, it is suggested that each one can be considered a valid species.

This same pattern of distribution is shown by Poospiza lateralis / P. cabanisi (Assis et al., 2007). The pattern found for S. lalandi and P. lateralis groups suggests that the original ranges of the ancestral taxa have retreated to two areas with cooler and moister climatic features, with subsequent isolation and differentiation: 1) the high mountains of coastal southeastern Brazil; and 2) southern Brazil and adjacent areas (eastern Paraguay, northeastern Argentina, and Uruguay). This pattern should also be associated to Plio-Pleistocene tectonic movements (Petri & Fúlfaro, 1986) that also appear to have influenciated the differentiation of some forest bird species (Pinto, 1978; Silva & Stotz, 1992; Silva & Straube, 1996).

Another southern montane species recently found in the southeastern Brazilian mountaintops is Cinclodes pabsti (Freitas et al., 2008). Nevertheless, it is necessary to analyze more specimens and voice recordings of this northern population to assess if it can be treated as a new taxon.

No species endemic to the Caatinga was recorded in the campos de altitude and only one Cerrado endemic (0.8%) was found in this habitat type. Small percentages of Cerrado (2.9%) and Caatinga endemics (0.5%) were found among the campos rupestres avifauna (Table 2).

All Cerrado endemics recorded in the campos rupestres have original distributions that do not reach the coastal ranges, except Cyanocorax cristatellus. This species have been expanding its range eastward and southward due to the deforestation of the Atlantic Forest (Alvarenga, 1990; Vasconcelos, 1999a; Mallet-Rodrigues et al., 2007; Lopes, 2008), but it is possible that it is a native species in the only area of campos de altitude it was recorded (Serra do Ibitipoca), since the region is in a transitional zone between Atlantic Forest and Cerrado, with several bird species typical of each biome (Pacheco et al., 2008).

The Caatinga reaches the borders of the central and northern Espinhaço Range, what explains the occurrence of one of its endemics (Sakesphorus cristatus) in the campos rupestres. Despite the fact that Marini & Lopes (2005) found S. cristatus in the Rio Doce basin at Conceição do Mato Dentro, we still consider it as a Caatinga endemic since it is probably expanding its range due to deforestation, as observed for other typical Caatinga birds in this river valley, such as Columbina picui, Compsothraupis loricata, and Icterus jamacaii (M.F.V., pers. obs.).

Bird species that have ranges restricted to mountaintop open-habitats of southeastern Brazil are represented by low percentages in both formations: 3.4% in the campos rupestres and 2.4% in the campos de altitude (Table 2). Montane open-habitat endemics with ranges restricted to the campos rupestres of the Espinhaço Range are: Augastes lumachella, Augastes scutatus, Formicivora grantsaui, and Asthenes luizae. A. lumachella and F. grantsaui are endemic to the northern Espinhaço Range, while A. scutatus and A. luizae are restricted to the central and southern regions (Vasconcelos, 2008b). Oreophylax moreirae was considered restricted to the campos de altitude in coastal mountains (Serra da Mantiqueira, Serra dos Órgãos, and Serra do Caparaó), but was recently discovered in the highest peaks of the southern Espinhaço Range, at Serra do Caraça (Melo-Júnior et al., 1998; Vasconcelos, 2000; Vasconcelos & Melo-Júnior, 2001). Polystictus superciliaris and Embernagra longicauda were considered endemic to the campos rupestres of the Espinhaço Range, and also as Cerrado endemics (Silva, 1995, 1997; Silva & Bates, 2002; Silva & Santos, 2005). Nevertheless, these species were recorded outside the Espinhaço Range, in the Serra da Canastra and in the coastal mountains of the Atlantic Forest region, such as Serra do Mar, Serra da Mantiqueira, and Serra do Caparaó (Sick, 1997; Silveira, 1998; Vasconcelos, 1999a, b, 2003, 2008a, b; Vasconcelos et al., 2003). The occurrence of E. longicauda, a typical species of the serras in the Espinhaço Range, in the Caparaó highlands suggests past connections between the campos de altitude of this area and the intermost open areas of Central Brazil, a pattern also corroborated by a recent study on Akodon rodents (Gonçalves et al., 2007). Therefore, among the seven endemic bird species of the open-habitats of southeastern Brazilian mountaintops, four are restricted to the campos rupestres of the Espinhaço Range, but none of them is restricted to the campos de altitude of the eastern mountains.

In addition to those endemic species, there are four subspecies that appear to be restricted to the campos rupestres area of the Espinhaço Range: Phaethornis pretrei schwarti, Campylopterus largipennis diamantinensis, Colibri delphinae greenewalti, and Knipolegus nigerrimus hoflingi. Nevertheless, validity of some of those taxa are questionable (Vielliard, 1994; Stiles, 1999; Brammer, 2002) and further taxonomic studies are still necessary.

The majority of birds living in the open-habitats of southeastern Brazilian mountaintops are represented by widespread and non-endemic species. Thus, the Andean-Patagonian influence in the avifauna in those habitats is small. Nevertheless, four endemic species appear to have close relationships with other Andean (Augastes lumachella, A. scutatus, and Oreophylax moreirae) and Andean-Chacoan-Patagonian (Asthenes luizae) species (Sick, 1970, 1985; Silva, 1995; Vielliard, 1996; Vasconcelos et al., 2008b), but in the absence of any phylogenetic analysis, it is impossible to determine the precise evolutionary relationships and biogeographical origins of these species.

Conservation

This review shows that bird species endemic to the Atlantic Forest, Cerrado, and Caatinga may be found together at the montane open-habitats of southeastern Brazil. Besides this contact zone character, those habitats have their own few endemic birds. Among the birds of the montane open-habitats of southeastern Brazil, 16 are considered threatened or near-threatened either globally or in Brazil (Table 3). There are some discrepancies between both checklists. For instance, in Brazil, there are four threatened and two near-threatened species (Machado et al., 2005), while globally there are six threatened and 10 near-threatened species (BirdLife International, 2007) (Table 3). Two examples are Asthenes luizae and Poospiza cinerea, both not considered as threatened species in Brazil, but classified as globally vulnerable (Table 3).

Despite 32 protected areas established in campos rupestres and campos de altitude, especially national and state parks (Table 4), those reserves cannot guarantee the conservation of all of their vegetation types and endemic and threatened birds found atop those mountain ranges. The first reason is, following a rule in Brazil and other developing countries, many of the reserves exist only "on paper", and there is neither financial support nor control of illegal activities inside their areas. Examples of paper parks with little enforcement are Serra Nova State Park, Grão Mogol State Park, Serra do Cabral State Park, and Sempre Vivas National Park (all in Minas Gerais state), the last one not included in this revision, but in the main massif of Espinhaço Range with large areas of campos rupestres. Most of these reserves were decreed without local landowners receiving compensation for their lands. Besides lack of funds, the main reasons for that are the lack of legal titles by the de facto owners and the generalized mess of land tenure in Brazil. As a result, there were reports of landowners setting fire to the campos rupestres of Serra do Cabral and Grão Mogol State Parks as a way of demanding the money they never received (see below).

Secondly, the staff working in most Brazilian protected areas consists of too few people unable to control and protect large areas against the pillaging of the natural heritage. Also, most reserves are threatened by uncontrolled tourism in southeastern Brazil. The recently created "Estrada Real" touristic route linking the southeastern Brazilian coast (Parati and Rio de Janeiro) to the highlands of Minas Gerais state, is an important threat to the conservation of the campos rupestres and campos de altitude as the number of tourists visiting these mountainous areas has shown a rapid increase in the last three years without proper control on their activities. A portion of this "ecological road" partially destroyed the campos rupestres in the type-locality of Asthenes luizae, a globally vulnerable species (BirdLife International, 2007). This kind of development is a serious threat to this endemic bird species, as well as to a restricted-range plant species (Viana et al., 2005). In the campos de altitude of Caparaó, Itatiaia, and Serra dos Órgãos National Parks, as well as in the Ibitipoca State Park, large numbers of tourists camp in the mountaintops, trampling the fragile native vegetation and causing fire hazards. It is common to find hundreds of people in those areas during weekends, holidays, or vacations. In Caparaó National Park, mules take the tourists to the highlands of this important area (Vasconcelos, 2003). These animals crush and graze the flora of the campos de altitude of Serra do Caparaó, composed of endemic and rare plant species (Leoni, 1997). So, management of these reserves is poor and obviously not conservation-focused. Additionally, some tourists also collect endemic plants like orchids and bromeliads (Conceição, 2000; Vasconcelos, 2000). In Reserva Particular do Patrimônio Natural do Caraça, a private reserve, tourists used to collect endemic "canelas-deema" (Velloziaceae) in the campos rupestres as firewood (Vasconcelos, 2000).

Fire is another significant problem closely related to uncontrolled touristic activities, and large areas of Chapada Diamantina burn every year (Conceição, 2000). In the Serra do Caraça region, criminal fires affected one of the marshes where Scytalopus iraiensis, a globally endangered species at global and national levels, was recorded. After the fire, the species was not recorded again in this marsh (M.F.V., pers. obs.).

Unfortunately, many fires in the montane open-habitats are accidentally caused by tourists who camp in those areas, by ranchers renewing their pastures, or by disgruntled landowners who have not been paid for the land expropriated by parks and other reserves. Environmental modifications caused by fire in the campos rupestres and campos de altitude include floristic impoverishment and later occurrence of invasive plant species, which compete for space and light with native and endemic ones (Martinelli & Orleans e Bragança, 1996; Safford, 1999a; Vasconcelos, 2000; Vasconcelos et al., 2002b).

Other human impacts are widespread in the mountains, such as mining, hunting, and overgrazing by cattle and horses (Safford, 1999a; Vasconcelos, 2000, 2003; Vasconcelos et al., 2002b). In the Quadrilátero Ferrífero, extensive areas of campos rupestres growing on rock outcrops rich in iron ore ("canga") have been quickly destroyed for mining (Jacobi et al., 2007; Versieux & Wendt, 2007). The demise of this special type of campos rupestres probably led Augastes scutatus, a near-threatened species, to local extinction in one locality of Quadrilátero Ferrífero (Vasconcelos, 1999b). In the Cipó Range and Chapada Diamantina region, many families live based on the collection and sale of "sempre-vivas", endemic plants of the family Eriocaulaceae, which are valuable for ornamental purposes.

An important set of endemic and threatened bird species live in the campos rupestres and campos de altitude, and better efforts must be directed toward the better conservation of those important vegetation types. Safford (1999a) presented a series of actions that should be taken as a base for the conservation of the campos de altitude flora. Those can also be applied to avifauna conservation in the highlands of southeastern Brazil.

ACKNOWLEDGEMENTS

We thank Brehm Foundation, World Wildlife Fund (WWF), and United States Agency for International Development (USAID) for financial support during this study. M.F.V. thanks Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for the permission to collect bird specimens in Brazil, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a master and a doctoral fellowship, and AMNH for a Collection Study Grant to work on eastern Brazilian birds. M.R. is supported by a grant from CNPq (1998-2001, 2007-2009 and 473428/2004-9), Fundação O Boticário de Proteção à Natureza, and Fapemig (APQ-0434-5.03/07). D. Hoffmann kindly prepared the map. C.R.M. Abreu, C.E.A. Carvalho, E.P.M. Carvalho-Filho, S. D'Angelo-Neto, H.B. Gomes, E. Gouvêa (in memoriam), D. Hoffmann, J. Julio-Filho, M. Maldonado-Coelho, G.N. Maurício, T.A. Melo-Júnior, R. Nassau e Braga, and L.F. Silveira, helped in the field. M. Votaw, F.A. Silveira, K.-L. Schuchmann, and L.E. Lopes kindly commented on draft versions of the manuscript. F.F. Vasconcelos, F. Mallet-Rodrigues, F.S. Leite, G.B. Malacco, J.F. Pacheco, and R. Parrini shared their records based on personal observations from some localities. We also thank the staffs of the museums visited during this study, especially: J. Cracraft, P. Sweet, and P. Hart (AMNH), M. Hoffmann (MBML), L. Guimarães (MCN), C.S. Fontana (MCP), H.M.F. Alvarenga (MHNT), A. Aleixo (MPEG), L.F. Silveira (MZUSP), and R. Grantsau (SG).

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Recebido em: 11.07.2008

Aceito em: 18.11.2009

Impresso em: 31.03.2010

APPENDIX 1

List of sources used in the revision of the open-habitat avifauna of southeastern Brazilian mountaintops.

Apenndix 1 - click to extended

Apenndix 1 - click to extended

APPENDIX 2

Checklist of the avifauna recorded in the campos rupestres and campos de altitude of southeastern Brazilian mountaintops and patterns of endemism. Numerical codes for localities and sources are presented in Table 1 and ^{Appendix 1}, respectively. Endemism: AF = endemic to the Atlantic Forest region; CA = endemic to the Caatinga region; CE = endemic to the Cerrado region; MT = endemic to the open-habitats of southeastern Brazilian mountaintops (campos rupestres and campos de altitude).

Apenndix 2 - click to extended

Apenndix 2 - click to extended

Apenndix 1 - click to extended

Apenndix 2 - click to extended

Publication Dates

• Publication in this collection
  05 Apr 2010
• Date of issue
  2010

History

• Received
  11 July 2008
• Accepted
  18 Nov 2009