Bird diversity in the Serra do Aracá region , northwestern Brazilian Amazon : preliminary check-list with considerations on biogeography and conservation

We inventoried the birds from Serra do Aracá region, state of Amazonas. The region encompasses a high diversity of vegetation types, including white sand forests and campinas, terra firme and flooded forests, montane forests and tepuis. We recorded 416 bird taxa in 69 families through captures with mist nets, tape recording of bird voices, and collection of voucher specimens. A large proportion of them (61%) were recorded in a single vegetation type. Qualitative estimates suggest that approximately 580 bird species occur in the region. The avifauna of the Aracá region has a mixed biogeographic composition, with species typical of both margins of the Rio Negro occurring sympatrically. Additionally, species whose distributions are restricted to three areas of endemism for Amazonian birds (Imeri, Guiana and Pantepui) were recorded in the region. Rare landscapes in the Brazilian Amazon are found in the Serra do Aracá region. Additionally, we recorded endemic and rare birds, highlighting the value of the region for conservation. The Serra do Aracá State Park officially protects montane forests, terra firme forests and tepuis. We suggest that the large extension of white sand campinas and igapó forests at the southern portion of Serra do Aracá should be also preserved in order to improve the representation of the rich natural heritage of the region.

The biogeographic distribution of the Amazonian avifauna is complex, and includes geographic gradients of species diversity and the influence of rivers in the delimitation of areas of endemism (CRACRAFT 1985, HAFFER 1992, RAHBEK & GRAVES 2001, SILVA et al. 2005, COHN-HAFT et al. 2007a, b).Although the major geographic patterns of bird distribution in Amazonia have been identified since the late 1960's (HAFFER 1969(HAFFER , 1974)), recent studies have documented new areas of endemism, areas of biogeographic transition and large scale turnover of species composition in flooded forests (COHN-HAFT et al. 2007b, NAKA 2011, BORGES & SILVA 2012).These studies have demonstrated that larger scale inventories are useful for understanding the geographic patterns of bird distribution within the Amazon basin.
Although recent inventories have elucidadet the distribution of birds in the Amazon (see papers in SANTOS & ALEIXO 2011), several locations remain poorly investigated (OREN & ALBUQUER-QUE 1991, OREN 2001).The avifauna of the region located between the Branco and Negro rivers in the state of Amazonas, for example, remains poorly studied despite recent inventories (NAKA et al. 2006, NAKA et al. 2007).This region includes rare ecosystems of the Amazon such as white sand campinas, montane forests and tepuis (PRANCE & JOHNSON 1992, SANTOS et al. 1993).Moreover, this region is located between rivers that have a clear influence on the distribution of birds and other taxa (AYRES & CLUTTON-BROCK 1992, BORGES 2007, NAKA 2011).
We provide a preliminary check-list of the birds from the Serra do Aracá region, which is located in the Rio Negro/ Rio Branco interfluve, Northwestern Brazilian Amazon.Additionally, we perform qualitative analysis of the bird fauna, to understand how habitat heterogeneity and geographical context influence species distribution.And finally, we consider the effectivennes of the Serra do Aracá State Park to protect a representative sample of the regional diversity of bird species and environments.

MATERIAL AND METHODS
Birds were sampled in the major habitats of the Serra do Aracá and the valleys of the Aracá and Demini rivers, at the Negro/Branco interfluve in 2004 (December), 2006 to 2008 (July/August) and 2010 (July/August) years.During the expeditions we held nearly 55 field days, which were distributed among 25 sites throughout the region (Fig. 1), though not evenly.We spent only 10 days in the montane forest and summit of Serra do Aracá due to difficulties accessing the site and remaining in it, and a limited time in the terra firme and Bird diversity in the Serra do Aracá region, northwestern Brazilian Amazon: preliminary check-list with considerations on biogeography and conservation Sérgio Henrique Borges1 , Andrew Whittaker2 & Ricardo Afonso Machado de Almeida 1  ZOOLOGIA 31 (4): 343-360, August, 2014 flooded forests.Therefore, sampling was more intense in white sand campinas and campinaranas (ANDERSON 1981), which are easy to access from rivers and are relatively low in species diversity.
The Aracá river valley and its tributaries are extensively covered with white sand campinas, sand dunes, low canopy forests (campinaranas) and black water flooded forests (igapó forests).In the Aracá valley, we also visited granite rock outcrops (inselbergs), with altitudes varying from 80-120 m and sparse vegetation cover.Hillside montane forests and the open vegetation of Serra do Aracá were found between 400 and 1,200 m a.s.l.Serra do Aracá has a flat table shape, which is typical of the Venezuelan tepuis (HUBER 1988, HUBER 2005) and its summit is occupied by partially flooded grasslands and scrublands and patches of low-canopy forests.The montane forests have a more heterogeneous vegetation structure and normally are covered by clouds in cold mornings.Detailed descriptions of the floristic and vegetation physiognomy of the Serra do Aracá can be found in PRANCE & JOHNSON (1992).Inventories of terra firme forests and igapó flooded forests were concentrated in Serra do Aracá foothills and along the lower courses of Aracá and Demini rivers (Fig. 1).
Our field methods included capture of birds with mist nets (36 mm mesh, 12 x 2.5 m), tape recording of bird vocalizations using professional tape recorders (Sony TCM 5000, Marantz PMD 660) and collection of specimens.We captured 635 individuals in 2,204 nets/hours of mist net operation.Biogeographic and/or taxonomic relevant specimens were collected (SISBIO #32122-1) and deposited in the bird collection of Instituto Nacional de Pesquisas da Amazônia (INPA).Voice records will be deposited in public archives of the British Library's Sound Archive and the bird collection of the Instituto Nacional de Pesquisas da Amazônia (INPA).Meanwhile photographs or recordings can be requested from the authors (see Appendices S1-S6*).
Each species was recorded in the habitat categories defined in Appendix 1. Harrison indices were calculated between pairs of habitats using this categorization to determine the turnover of species between major habitats in the study region.This index is a measure of beta diversity, and is insensitive to differences in the total number of species of the sampling units compared (MAGURRAN 2004), which is useful for comparing habitats with very different numbers of species, as reported here.This index varies from 0 (total overlap in species composition) to 100 (completely different species composition) (MAGURRAN 2004).Only species in the following habitats were included in the analysis: terra firme forests, tepuis (including montane forests plus grassland and scrub on the Serra do Aracá summit), igapó forests and white sand campinas and campinaranas.
We described the geographic distributions of individual bird species in the following categories: 1) monotypic or polytic species with widespread distribution in the Amazon, especially in the northern portion of the basin; 2) taxa (species or subspecies) whose distribution includes the left margin of the Rio Negro, including the Guianas and both margins of the Rio Branco.Some species in this category are also found in the southern part of the Amazon river, while others are not recorded in the Central Amazon; 3) taxa whose distribution falls primarily on the right margin of the Rio Negro, but which extends to the left margin (Negro/Branco interfluve).Some of these species can also be found in the south-western parts of the Amazon; 4) taxa apparently restricted to the north-western Amazon in the upper Rio Negro, South Venezuela, and Eastern Colombia; 5) taxa endemic to the Guyana Highlands (tepuis).Since no extensive collection of bird specimens has been conducted in the region, subspecies identification was tentative and made after extensive literature review (DEL HOYO et al. 1992-2004, RESTALL et al. 2006), including regional catalogues (FRIEDMANN 1948, PINTO 1966).
*Available as Online Supplementary Material accessed with the online version of the manuscript at http://www.scielo.br/zoolGenerally, the diversity of birds in most habitats studied seems to be undersampled, considering the expected diversity found for similar habitats in more thoroughly studied regions (Table I).The exception was white sand campinas and campinaranas, where bird diversity was high compared with other better sampled regions (Table I).This result is likely related to the wide extension occupied by this habitat in Aracá (Fig. 1).Sampling efforts were less intense in terra firme forest and therefore it is likely that species diversity there is underestimated by at least 28% (Table I).Considering the deficit in the number of species found in the major habitats (Table I), we expect that 160 to 167 species will be added to the current check-list in future surveys, increasing the known bird diversity of region to approximately 580 species.
A large proportion of birds (61%, 231/379 species) were recorded in a single habitat.Most species were restricted to terra firme forest (27%), followed by igapó forests (14%), white sand campinas and campinaranas (16%) and tepuis (4%).Igapó flooded forests and white sand campinas and campinaranas have the most similar avifaunas (Table II).The avifauna of each vegetation type, however, is quite distinct in bird species composition, since Harrison index values were greater than 80 in most paired comparisons (Table II).Most avian taxa in the Aracá region are widely distributed throughout the Amazon basin (Table III).A smaller pro-ZOOLOGIA 31 (4): 343-360, August, 2014 portion of representative taxa have their geographical distribution centered in the right or left banks of the Rio Negro, while only a few species have more restricted distributions (Table III).

DISCUSSION
Future inventories will significantly increase the bird diversity documented for the Aracá region.We recommend that additional inventories target the less known avifauna of the terra firme forests and tepuis.Also, increasing specimen collections is fundamental for understanding bird species diversity and biogeographical patterns in the region.Although incomplete, the results reported here suggests that large rivers (Branco and Negro), the Guyana mountain system and habitat diversity are the major determinants of the regional bird species distribution.
It is well-known that large rivers in the Amazon basin such as the Madeira, Negro and Solimões-Amazonas strongly influence the distribution of bird species (HELLMAYR 1910, HAFFER 1992, BORGES 2007).In the study region, the Negro influences the geographic distribution of several bird species, especially in its lower course (BORGES 2007, NAKA 2011).Bird species such as Selenidera nattereri (Gould, 1836) and Tyranneutes stolzmanni (Hellmayr, 1906), recorded on the right margin of the Negro (BORGES et al. 2001) and Aracá region, are substituted by related species (S. piperivora (Linnaeus, 1766), and T. virescens (Pelzeln, 1868)) on the left margin of Rio Branco near Manaus (COHN-HAFT et al. 1997).Additionally, some species typical of the left margin of Rio Branco (COHN-HAFT et al. 1997), such as Monasa atra (Boddaert, 1783) and Gymnopithys rufigula, (Boddaert, 1783) were also recorded in the Aracá region and sites in southern Venezuela.These species are substituted by related species on the right margin of Rio Negro (COHN-HAFT et al. 1997, ZIMMER & HILTY 1997, BORGES et al. 2001).
The avifauna of the Aracá region has a mixed composition, with species from both margins of the Rio Negro occurring sympatrically.Reinforcing the mixed nature of its avifauna, Aracá is located in a region of confluence of three areas of endemism for Amazonian birds: Imeri, Guianas and Pantepui (CRACRAFT 1985).The bird species C. heilprini and A. pelzelni are representatives of the Imeri area, while the Guiana is exempli-fied by the occurrence of Crax alector Linnaeus, 1766, M. atra and G. rufigula.The Pantepui area of endemism is characterized by birds of the Guyana highlands (MAYR & PHELPS 1967), and is represented in the study region by species that occur in Serra do Aracá, such as Ceratopipra cornuta (Spix, 1825) and Hylophilus sclateri Salvin & Godman, 1883.
The patterns of species diversity and turnover of bird communities are clearly influenced by the various vegetation types found in the Aracá region, as shown by the high Harrison index values (Table II).The large difference in bird composition between habitats is partially explained by incomplete sampling, and it is likely that additional inventories will increase the similarity of bird species composition between them.However, natural history knowledge of several bird species suggests that the regional avifauna is well compartmentalized among the major regional landscapes.
These qualitative and preliminaries results suggests that the avifauna of the Aracá region is a product of interactive effects of geomorphological (development of rivers and mountains) and ecological (habitats diversity) processes.Further quantitative biogeographic analyses are needed to investigate the relative contribution of those processes in determining patterns of species distribution.
The extensive white sand campinas of the Aracá region, although relatively poor in species, contain large populations of birds that are specialized in this habitat type (ALONSO & WHITNEY 2003, BORGES 2004, ALEIXO & POLLETO 2007, GUILHERME & BORGES 2011).These specialized birds are represented by subpopulations that are more or less isolated from each other through the Amazon basin, and hence this island-like habitat (PRANCE 1996) represents an ideal situation to evaluate the level of genetic and morphological divergence of birds and other organisms (see CAPURUCHO et al. 2013 for an illustrative example).
Serra Aracá is part of a mountain system with different levels of isolation that composes the biogeographical region of Pantepui (MAYR & PHELPS 1967).In Brazil, this biogeographical unit is represented by transnational (Brazil-Venezuela) mountains such as Pico da Neblina and Monte Roraima.Serra do Aracá is relatively isolated from a more continuous block of mountains and is entirely found in the Brazilian territory.Intensification of bird inventories in the Serra do Aracá will result in a better knowledge of the geographic distribution of Taxa apparently restricted to Northwestern Amazonia 12 (4%) Brotogeris chrysoptera tenuifrons Friedmann, 1945, Cyanocorax heilprini Gentry, 1885 Taxa endemic to Guyana mountain system (tepuis) 13 (4%) Trogon personatus Gould, 1842, Ceratopipra cornuta (Spix, 1825) the birds that are already known, and may result in the discovery of new taxa.A non-avian example of the potential of the Aracá region for taxonomic studies is the recent discovery of a new primate species of the genus Cacajao (BOUBLI et al. 2008).
The unique features of the Aracá region require conservation strategies that consider its biological and environmental diversity.Serra do Aracá State Park, with 1,818.700ha, is one of the largest protected areas of the Brazilian Amazon.Unfortunately, the boundaries of this State Park do not include the large white sand campinas, the sand dunes and igapó flooded forests, which are found surrounding the Aracá river and its tributaries (Fig. 1).These habitats make an important contribution to the regional diversity of bird species.Moreover the occurrence of related taxa in the summits of the Serra do Aracá (e.g., Turdus ignobilis cf.murinus) and white sand campinas (e.g., Turdus ignobilis cf.arthuri) suggests that these birds share an evolutionary history (D.C.Oren unpubl.data).Also, the sand dunes of the Aracá region are relicts of unique geological events that occurred in the Holocene and Pleistocene (CARNEIRO et al. 2002).Extending the boundaries of Serra do Aracá State Park or creating an adjacent newly protected area to incorporate the large extension of white sand campinas in the southern part of the Serra do Aracá would substantially improve the representation of the rich biological, historical and environmental heritage of the region.

ACKNOWLEDGMENTS
The field research in the Aracá region received financial support from the Gordon and Betty Moore Foundation through the Geopolitics of Conservation in the Rio Negro project.We would like to acknowledge the enthusiastic support of Enrique Ortiz and Jason Cole.Our fieldwork would not be possible without the collaboration of Zélio (Soldado), Raimundo, Roberto and Antenor.Carlos Durigan, Zig Kok and Marcelo Moreira who all shared important ornithological records.The State Center for Conservation Units (CEUC) and the Chico Mendes Institute for Biodiversity Conservation (ICMBIO) provided the formal licences for fieldwork and skin collections in the Serra do Aracá State Park.Thanks to our colleagues Carlos Durigan, Simone Iwanaga, Marcelo Moreira, Márcio Oliveira, Jansen Zuanon, Alberto Akama, Alexandre Loy (in memorian), Cintia Cornelius, Claudeir Vargas, Tiago, Célio, Daniel, Dalva and Cledson for the sense of humor during the hard work in the hills, sand fields, and rivers of the Aracá region.Cintia Cornelius kindly allowed us to include some of her species records in the check-list.In 2010, a field expediction to Aracá was supported by resources provided by Fundação de Amparo a Pesquisa do Amazonas (FAPEAM) and Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) through the FAPESP/FAPEAM joint funding program (09/53365-0).Marcelo Moreira kindly prepared the map.Nigel Smith, Yiyuan Jasmine and Karl Didier helped with the use of English language.Two anonymous reviewers helped to clarify important points in the text.Bird diversity in the Serra do Aracá region, northwestern Brazilian Amazon ZOOLOGIA 31 (4): 343-360, August, 2014 Appendix 1. List of bird species recorded in the Aracá region, Amazonas State, Brazilian Amazon.Taxonomic nomenclature follows the Brazilian Committee of Ornithological Records (CBRO 2014).Species between parentheses do not have adequate documentation for a safe identification.4,15,16,17,18,20,21,22,25

Figure 1 .
Figure 1.Northwestern region of the state of Amazonas showing the study sites, mainly rivers and municipalities.Note the large areas occupied by white sand campinas in the study region.

Table I .
Number of bird species recorded in the terrestrial habitats in the Aracá region compared with the same habitats in better sampled places in the Amazon.

Table II .
Harrison indices calculate in paired comparisons between major vegetation types in the Aracá region.

Table III .
Taxa (species or subspecies) recorded in Aracá region distributed in major biogeographic categories.For more details in categories definition see Methods section.