Bird Conservation in Brazil MIGUEL ÂNGELO MARINI∗ AND FREDERICO INNECCO GARCIA Departamento de Zoologia, Instituto de Biologia, Universidade de Brası́lia, Brası́lia, D.F., 70.910-900, Brasil Abstract: Brazil has one of the richest avifaunas in the world, with recent estimates varying from 1696 to 1731 species. About 10% (193 taxa) of these are threatened. The Amazon has the highest number of species, followed by the Atlantic Forest and the Cerrado; most of Brazil’s endemic birds, however, are in the Atlantic Forest. Brazil’s threatened species occur mostly in the Atlantic Forest, especially in the southeast lowlands and the northeast. The Cerrado has the second highest number of threatened species. The two major threats to Brazilian birds are habitat loss, degradation, and fragmentation and hunting, most especially for illegal commerce. A number of conservation and research initiatives over the last 20 years have significantly improved our capacity to address and resolve major issues for bird conservation. Brazil requires a National Bird Conservation Plan to draw up priorities for research and conservation over the next decade. Conservación de Aves en Brasil Resumen: Brasil tiene una de las avifaunas más ricas del mundo, con estimaciones recientes que varı́an entre 1696 y 1731 especies. Cerca de 10% (193 taxa) de ellas están amenazadas. El Amazonas tiene el mayor número de especies, seguido por el Bosque Atlántico y el Cerrado; sin embargo, la mayorı́a de las aves endémicas de Brasil se encuentran en el Bosque Atlántico. Las especies amenazadas de Brasil ocurren principalmente en el Bosque Atlántico, especialmente en las tierras bajas del sureste y del noreste. El Cerrado tiene el segundo número mayor de especies amenazadas. Las dos principales amenazas a las aves brasileñas son la pérdida, degradación, y fragmentación del hábitat y la caceria—especialmente para el comercio ilegal. Numerosas iniciativas de conservación e investigación en los últimos 20 años han mejorado significativamente nuestra capacidad para abordar y resolver temas importantes para la conservación de aves. Brasil requiere un Plan Nacional de Conservación de Aves para definir prioridades de investigación y conservación para la siguiente década. Introduction Brazil harbors one of the most diversified bird faunas in the world, with species estimated at more than 1690 (CBRO 2003; IUCN 2004; NatureServe 2004). This amounts to about 57% of the bird species recorded for all of South America. More than 10% of these species are endemic to Brazil, making it one of the most important countries for conservation investments (Sick 1993). Human intervention has significantly affected the bird species that inhabit Brazilian natural ecosystems. Bird re- sponses to these alterations range from those that have benefited from the habitat alterations and increased their populations (e.g., Great Kiskadee [Pitangus sulphuratus]) to those that have become extinct in the wild (e.g., Razor-billed Curassow [Mitu mitu] and Glaucous Macaw [Anodorhynchus glaucus]). Within the Neotropics, Brazil contains the highest number of threatened bird species (Collar et al. 1997). We analyzed the distribution of Brazilian birds and the number and distribution of threatened species. We discuss the major present and future threats and provide an overview of the major conservation and research ∗ email [email protected] Paper submitted December 30, 2004; revised manuscript accepted February 3, 2005. 665 Conservation Biology, Pages 665–671 Volume 19, No. 3, June 2005 666 Bird Conservation in Brazil Marini & Garcia Table 1. Numbers of bird species, endemic species, and threatened taxa (species and subspecies) in Brazil and by biome. Threatened taxaa Biome Amazon Atlantic Forest Cerrado Caatinga Southern Grasslands Pantanal Coastal and marine Total Brazil Species Endemic species total endemic to biome endemic to Brazil 1,300b 1,020c 837d 510f 476c 463h >130i 1,696–1,731j 263b 188c 36e 15g 2c 0 0 504 20 112 48 25 20 13 23 193 6 54 14 7 3 0 0 84 10 90 14 15 0 1 0 119 a IBAMA 2003; IUCN 2004. et al. 2003. c MMA 2000. d Silva 1995. e Silva 1995; Cavalcanti 1999; Silva & Bates 2002; Lopes 2004. f Silva et al. 2003. g Universidade Federal de Pernambuco et al. 2002. h Tubelis & Tomas 2003. i Vooren & Brusque 1999. j CBRO 2003; IUCN 2004; NatureServe 2004. b Mittermeier initiatives. Finally, we outline the need for an integrated program of research and conservation for threatened bird species in Brazil. Composition and Distribution of Brazilian Birds The two areas with the highest number of bird species and the highest levels of endemism are the Amazon and the Atlantic Forest. Ninety-two percent of Brazilian bird species are resident species; only 8% are migrant species (Sick 1993). The distribution of resident bird species throughout Brazil is uneven, and most of the species diversity is centered in the Amazon and the Atlantic Forest, two biomes that originally were covered mostly by humid forests. The highest number of resident bird species (1300) and highest rates of endemism (20%) occur in the Amazon (Mittermeier et al. 2003), followed by the Atlantic Forest, with 1020 species (18% endemics; Table 1) (MMA 2000). The Cerrado, dominated by a savanna-like vegetation, is the third richest biome, with 837 species (4.3% endemic) (Silva 1995; Cavalcanti 1999; Silva & Bates 2002; Lopes 2004). Caatinga, a dry forest vegetation in northeastern Brazil, has 510 bird species (2.9% endemics) (Silva et al. 2003), and the southern grasslands, an expansion of the Argentinean Pampas into Brazil, have 476 species and only 0.4% endemism (MMA 2000). The Pantanal, the largest South American wetland (Harris et al. 2005 [this issue]), has 463 species but no endemic species (Tubelis & Tomas 2003). Finally, about 130 species of typically marine fam- Conservation Biology Volume 19, No. 3, June 2005 ilies inhabit the coastal and marine habitats, but none are endemic to Brazil (Sick 1993; Vooren & Brusque 1999). Most migrant birds (61%) come from the northern hemisphere and are aquatic birds that migrate over long distances and congregate seasonally along the coast or major river drainages. Because of international collaboration and a well-designed banding system, these migrants have been well studied. In contrast, little is known about the migratory routes and ranges within Brazil of terrestrial northern migrants such as the Veery (Catharus fuscescens) and Swainson’s Thrush (Catharus ustulatus) (Remsen 2001). Southern migratory species represent 39% of the migrant species and include Hudson’s Black Tyrant (Knipolegus hudsoni). Their winter range is usually concentrated in southern Brazil, but their movements and natural history are comparatively less studied than those of the northern migrants (Sick 1993). Number and Distribution of Threatened Species We used two lists to define the number of threatened bird species in Brazil: the IUCN Red List of globally threatened species (124 species; IUCN 2004) and the Brazilian Red List of nationally threatened species (160 species; IBAMA 2003). Merging these two lists yielded a total of 193 threatened species and subspecies: 124 are globally threatened (IUCN 2004) and 69 are nationally threatened (IBAMA 2003). Among the nationally threatened birds, 25 are species, of which 10 are endemic to Brazil, and 44 are subspecies, all of which are endemic to Brazil. Of these Marini & Garcia Bird Conservation in Brazil Table 2. Number of Atlantic Forest bird taxa (species and subspecies) by Atlantic Forest region. Number of threatened taxa Atlantic Forest region total endemic to Atlantic Forest Lowlands southeast Northeast Mountains southeast Southern Planalto Total 52 51 29 11 112 34 13 9 2 54 endemic to Brazil 44 45 13 4 90 193 threatened birds, 119 (62%) are restricted to Brazil (Table 1). The Atlantic Forest contains 75.6% of Brazil’s endemic threatened species, making it the most critical biome in Brazil for bird conservation. Other areas where threatened endemic birds occur are the Cerrado (11.8%), the Caatinga (12.6%), the Amazon (8.4%), and the Pantanal (0.8%) (Table 1). The distribution of threatened bird species that are endemic to particular biomes shows a pattern similar to that of all threatened species, although their concentration is even greater in the Atlantic Forest (64.3%). Some are found in the Cerrado (16.7%) and the Caatinga (16.7%) and fewer are found in the other biomes (Table 1). Based on BirdLife International’s (2003) classification, Brazil has 63 threatened species with restricted ranges in 24 endemic bird areas (EBAs) and secondary areas. All Brazilian biomes except the Pantanal contain some EBAs. Most EBAs lie within the Atlantic Forest, which also contains a high concentration of endemic threatened species, making it a high priority for conservation (Collar et al. 1997). Four regions in the Atlantic Forest are priorities for threatened birds: the southeastern lowlands, the southeastern mountains, the northeastern lowlands and Atlantic slope, and the southern Planaltos. Between 29 and 52 threatened taxa occur in the first three regions, and 11 occur in the southern Planaltos (Table 2). Of these four regions, the most important area for conservation action is the southeastern lowlands. This area contains 46% (52 species) of the 112 threatened taxa of the biome, 34 of them endemic to the Atlantic Forest. The situation in northeastern Brazil is especially dire because it contains 51 threatened taxa, including 13 species endemic to the Atlantic Forest and 26 endemic threatened subspecies that remain in a few small forest fragments (Teixeira 1986; IBAMA 2003). The recently discovered Pigmy Owl (Glaucidium mooreorum) from the northeast is not included in either list and is apparently on the brink of extinction (Silva et al. 2002). The Cerrado ranks second in the numbers of threatened species and threatened endemics (Table 1). Nearly 80% 667 of its natural vegetation has been converted (Myers et al. 2000), largely to intensive pasture and widespread mechanized agriculture (Klink et al. 1993; Stotz et al. 1996; Klink & Moreira 2002). Recent estimates suggest that remaining natural habitat will be largely destroyed by 2030 if current rates of destruction continue (Machado et al. 2004). Major Present and Future Threats The major threat to Brazilian birds is habitat loss and fragmentation. Among the 124 Brazilian species on the IUCN Red List (IUCN 2004), 111 (89.5%) face habitat loss or degradation as one of the major threats, followed by overharvesting (35.5%). Other threats include invasive alien species and pollution (14%), human disturbance and accidental mortality (9.5%), changes in native species dynamics (6.5% each), natural disasters (5%), and persecution (1.5%). Studies of the effects of forest fragmentation on Brazilian birds were pioneered by Willis (1979), who looked at three forest patches in the Atlantic Forest in the state of São Paulo. The first long-term study, begun north of Manaus in 1979 by the Biological Dynamics of Forest Fragments Project (PDBFF), monitored avian communities before and after fragmentation (Bierregaard et al. 1992; Bierregaard & Stouffer 1997; Stouffer & Borges 2001). In the past decade, several studies on forest fragmentation in the Atlantic Forest have expanded on the Willis study, including Aleixo and Vielliard (1995), Machado (1995), Maldonado-Coelho and Marini (2003), Marsden et al. (2001), Galetti et al. (2003), and Ribon et al. (2003). In the Cerrado, Christiansen and Pitter (1997) and Marini (2001) confirmed species loss in smaller forest fragments, and Andrade and Marini (2001) demonstrated that movements among forest patches decreased in forest-dependent birds. No studies have evaluated habitat fragmentation on birds in the open habitats of the Caatinga, Cerrado, Pantanal, and Southern Grasslands. Illegal international trade of birds and wildlife is a major activity in Brazil (Lacava 2000; Renctas 2002). The Glaucous Macaw and Spix’s Macaw (Cyanopsitta spixii) became extinct largely because of illegal trade, and parakeets, parrots, and other macaws are also heavily traded (Guix et al. 1997; Wright et al. 2001). Around 12 million animals are traded every year in Brazil (Lacava 2000). They are caught at 229 sites and sold in 264 cities— mostly in northern Brazil—affecting mainly Amazonian but also Caatinga and Cerrado birds (Renctas 2002). Care and release of the enormous numbers of birds confiscated by the authorities is a problem because there are few appropriately planned translocation programs (Marini & Conservation Biology Volume 19, No. 3, June 2005 668 Bird Conservation in Brazil Marinho-Filho 2005). Most are released in inappropriate places (outside their natural geographic ranges) and without a proper health evaluation, and the effects of these releases is unknown. Solving the problem of wildlife trade requires law enforcement in the countries of origin and in the destination countries—mainly the United States, Saudi Arabia, Japan, and Europe. Conservation and Research Initiatives The Brazilian ornithological community has provided structure for and organization of research. The Brazilian Ornithological Society (SBO) has sponsored annual meetings since 1991, and has published a dedicated journal (Ararajuba, Revista Brasileira de Ornitologia) since 1990 (more than 300 articles). The SBO has also set up the Brazilian Committee of Ornithological Records (CBRO) to accumulate, review, and analyze reports of new species and new records and localities for Brazil. Brazil has a national banding center (National Center for the Study and Conservation of Birds [CEMAVE]), which regulates and provides permits and free metal bands to registered ornithologists and supports numerous research and conservation projects. One of the most successful endangered species programs in Brazil is the Blue Macaw Project in the Pantanal, created in 1991. IBAMA has established eight committees (and has plans for more) to develop and monitor conservation strategies for the following species: Alagoas Curassow (Mitu [Crax] mitu); the Red-billed Curassow (Crax blumenbachii); the Brazilian Merganser (Mergus octosetaceus); Lear’s Macaw (Anodorhynchus leari); the Hyacinth Macaw (Anodorhynchus hyacinthinus); Spix’s Macaw; and the Golden Conure (Guaruba guarouba). A separate committee also monitors albatrosses and petrels (23 species). BirdLife Brasil has established a program devoted to “important bird areas” (IBAs), focusing mostly on the Atlantic Forest. Several institutions have projects and programs that contribute to bird conservation and research, including the Ministry of the Environment; the National Institute for Amazon Research (INPA); PDBFF of INPA and the Smithsonian Institution (Bierregaard et al. 2001); and the Brazilian Long-Term Ecological Research (LTER) project (Pesquisas Ecológicas de Longa Duração [PELD]). The PELD is funded by the Brazilian Science Council (CNPq) and the Ministry of Science and Technology (MCT) through FINEP and the Ministry of the Environment, with nine sites in almost all Brazilian biomes. Also, the Ministry of the Environment’s Project for the Conservation and Sustainable Use of Brazilian Biological Diversity (PROBIO) finances projects on specific conservation themes each year (e.g., MMA 2003). Over the last decade, Conservation Biology Volume 19, No. 3, June 2005 Marini & Garcia the Ministry of the Environment (2002) and some state governments have organized priority-setting workshops, and the participation of ornithologists has been consistently influential in the selection of conservation areas. Renctas is a Brazilian nongovernmental organization that monitors and helps in taking rapid action against the illegal trade of wildlife. Some Brazilian states have compiled their own red lists of threatened species, which are of enormous value in promoting awareness of the plight of the state’s fauna and flora and in influencing and guiding conservation measures. States with lists include Minas Gerais (Machado et al. 1998), São Paulo (São Paulo 1998), Rio de Janeiro (Bergallo et al. 2000), Rio Grande do Sul (Fontana et al. 2003), and the recently updated from Paraná (Mikich & Bérnils 2004). The greatest challenge facing Brazilian ornithologists is the lack of information on the basic biology of the rare species and the increasing number of threatened species. Also, 19 new bird species, primarily passerines, have been described in Brazil since 1990, mostly from the Atlantic Forest (Table 3), at a rate of more than 1 species per year. Our knowledge of the biology and ecology of Brazilian birds was summarized by Sick (1985; English version 1993; revised and extended Portuguese edition 1997), but basic information on many species is meager or nonexistent. Of the 36 birds endemic to the Cerrado (Silva 1995), for example, only 6 have been studied in the field for at least 1 year. Inventories and taxonomic studies are still required for almost all the regions. Conclusions In the last 20 years, many institutions and professionals have adopted research approaches that directly tackle conservation issues, and the ornithological and conservation communities have provided the means to study, plan, and take a hands-on approach to conserving Brazil’s rich and increasingly threatened avifauna. We know which species are threatened, what their key threats are, and where they should be preserved. Information on new species and the biology of old and new species, however, is lacking. Research and conservation measures are still unevenly distributed among regions and species, and threats are not diminishing. Brazil requires a major National Bird Conservation Plan that would organize and set priorities for the activities of different institutions and professionals, define needs for future research and capacity building, establish national priorities for conserving and managing threatened species and important conservation areas, and promote public policies to improve the protection of birds. Marini & Garcia Bird Conservation in Brazil 669 Table 3. Bird species described from Brazil between 1990 and 2004. Species Biome Cercomacra manu Formicivora littoralis Asthenes luizae Clytoctantes atrogularis Phylloscartes kronei Chordeiles vielliardi Stymphalornis acutirostris Phylloscartes beckeri Synallaxis whitneyi Hylexetastes brigidae Acrobatornis fonsecai Arremon franciscanus Antilophia bokermani Scytalopus iraiensis Herpsilochmus sellowi Suiriri islerorum Glaucidium moororum Micrastur mintoni Thamnophilus divisorius ∗ Threat Amazon Atlantic Forest Cerrado Amazon Atlantic Forest Caatinga Atlantic Forest Atlantic Forest Atlantic Forest Amazon Atlantic Forest Caatinga Cerrado Atlantic Forest Caatinga Cerrado Atlantic Forest Amazon and Atlantic Forest Amazon Threat status∗ Reference — CR VU CR VU — EN EN VU — VU — CR EN — — CR — — Fitzpatrick & Willard 1990 Gonzaga & Pacheco 1990 Vielliard 1990 Lanyon et al. 1990 Willis & Oniki 1992 Lencioni-Neto 1994 Bornschein et al. 1995 Gonzaga & Pacheco 1995 Pacheco & Gonzaga 1995 Silva et al. 1995 Pacheco et al. 1996 Raposo 1997 Coelho & Silva 1998 Bornschein et al. 1998 Whitney et al. 2000 Zimmer et al. 2001 Silva et al. 2002 Whittaker 2002 Whitney et al. 2004 status: CR, critically endangered; VU, vulnerable; EN, endangered. 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