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ARTICLE • Pap. Avulsos Zool. 60 • 2020 • https://doi.org/10.11606/1807-0205/2020.60.16   copy

Avifauna of the region of the Volta Grande Hydroelectric Power Plant in Southeast Brazil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The Volta Grande region in the Brazilian state of Minas Gerais is classified as of “High Biological Importance” for the conservation of birds in the state. Despite this, the avifauna of the region has yet to be adequately sampled, as evidenced by the few papers on the region in ornithological literature. The results of an avifaunal inventory conducted between March 2013 and January 2014 in five sites located throughout the region of the Volta Grande Hydroelectric Power Plant in Southeast Brazil are presented. Point-counts, ad libitum observations and mist-nets recorded 224 species for the region, with insectivorous and omnivorous being the predominant feeding habits. Species that are “independent” of forest habitats comprised 52% of the recorded species. Three species are endemics of the Cerrado, 85 are migratory and 33 are under some degree of threat of extinction. These findings demonstrate that the region of the Volta Grande Hydroelectric Power Plant is important for bird conservation. Additional inventories, adequate management plans and public policies aimed the preserving species are needed for more effective conservation of the biodiversity of the studied region.

Key-Words.
Birds; Cerrado; Grande River Basin; Inventory; Threatened Species; Trophic Guilds

INTRODUCTION

The states of Minas Gerais and São Paulo in the Southeast Region of Brazil have 785 (Drummond et al., 2005Drummond, G.M.; Martins, C.S. Machado, A.B.M; Sebaio, F.A. & Antonini, Y. 2005. Biodiversidade em Minas Gerais: um Atlas para sua conservação. 2.ed. Belo Horizonte, Fundação Biodiversitas. 220p.) and 789 (Silveira et al., 2009Silveira, L.F.; Benedicto, G.A.; Schunck, F. & Sugieda, A.M. 2009. Aves. In: Bressan, B.M.; Kierulff, M.C. & Sugieda, A.M. Fauna ameaçada de extinção no Estado de São Paulo: Vertebrados. São Paul,: Fundação Parque Zoológico de São Paulo: Secretaria do Meio Ambiente. p. 87-283.) recorded bird species, respectively. The greatest threat to these species in both states is the degradation of natural environments and the consequent fragmentation and loss of habitats (Drummond et al., 2005Drummond, G.M.; Martins, C.S. Machado, A.B.M; Sebaio, F.A. & Antonini, Y. 2005. Biodiversidade em Minas Gerais: um Atlas para sua conservação. 2.ed. Belo Horizonte, Fundação Biodiversitas. 220p.; Bressan et al., 2009Bressan, P.M.; Kierulff, M.C.M. & Sugieda, A.M. 2009. Fauna ameaçada de extinção no Estado de São Paulo: Vertebrados. São Paulo, Fundação Parque Zoológico de São Paulo. 645p.).

The Cerrado is the second largest biome of Brazil, encompassing approximately 200 million ha located mainly in the center of the country but with small areas in northeastern Paraguay and eastern Bolivia (Silva, 1995Silva, J.M.C. 1995a. Birds of the Cerrado region, South America. Steenstrupia, 21: 69-92.a; Ratter et al., 1997Ratter, J.A.; Ribeiro, J.F. & Bridgewater, S. 1997. The Brazilian Cerrado vegetation and threats to its biodiversity. Annals of Botany, 80: 223-230.; Pinheiro & Monteiro, 2010Pinheiro, M.H.O. & Monteiro, R. 2010. Contribution to the discussions on the origin of the Cerrado biome: Brazilian savanna. Brazilian Journal of Biology, 70(1): 95-102.). It is characterized by a mosaic of phytophysiognomies ranging from grasslands to forest formations (Silva, 1995aSilva, J.M.C. 1995a. Birds of the Cerrado region, South America. Steenstrupia, 21: 69-92.; MMA, 2007Ministério do Meio Ambiente (MMA). 2007. Biodiversidade do Cerrado e Pantanal: áreas e ações prioritárias para conservação. Brasília. Ministério do Meio Ambiente. 540p. (Biodiversidade, 17)).

The diversity of the vegetation mosaic of the Cerrado is further enhanced by the influence of adjacent biomes, such as the Atlantic Forest, Amazon rainforest, Caatinga and Chaco (Ratter et al., 1997Ratter, J.A.; Ribeiro, J.F. & Bridgewater, S. 1997. The Brazilian Cerrado vegetation and threats to its biodiversity. Annals of Botany, 80: 223-230.; Myers et al., 2000Myers, N.; Mittermeier, R.A.; Mittermeier, C.G.; Fonseca, G.A. & Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403(6772): 853-858.; Silva & Bates, 2002Silva, J.M.C. & Bates, J.M. 2002. Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience, 52(3): 225-230.). This great species diversity accompanied by drastic loss of original vegetation over a relatively short period of time due to anthropic actions has led to the Cerrado being classified as one of 34 global terrestrial hotspots (Ratter et al., 1997Ratter, J.A.; Ribeiro, J.F. & Bridgewater, S. 1997. The Brazilian Cerrado vegetation and threats to its biodiversity. Annals of Botany, 80: 223-230.; Myers et al., 2000Myers, N.; Mittermeier, R.A.; Mittermeier, C.G.; Fonseca, G.A. & Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403(6772): 853-858.; Myers, 2003Myers, N. 2003. Biodiversity hotspots revisited. BioScience, 53(10): 916-917.). The Cerrado is also considered the largest, richest and probably most endangered tropical savanna in the world (Silva & Bates, 2002Silva, J.M.C. & Bates, J.M. 2002. Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. BioScience, 52(3): 225-230.). The avifauna of the Cerrado comprises 837 species (Silva, 1995bSilva, J.M.C. 1995b. Avian inventory of the Cerrado region, South America: implications for biological conservation. Bird Conservation International, 5(2-3): 291-304.; Stotz et al., 1996Stotz, D.F.; Fitzpatrick, J.W.; Parker, T.A. & Moskivits, D.K. 1996. Neotropical birds: ecology and conservation. Chicago, University Chicago Press. 478p.), of which 30 are endemic and 34 endangered according to the Brazilian red list (Silva, 1995bSilva, J.M.C. 1995b. Avian inventory of the Cerrado region, South America: implications for biological conservation. Bird Conservation International, 5(2-3): 291-304.; Zimmer et al., 2001Zimmer, K.J.; Whittaker, A. & Oren, D.C. 2001. A cryptic new species of flycatcher (Tyrannidae: Suiriri) from the Cerrado region of central South America. Auk, 118(1): 56-78.; ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2018. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília, ICMBio. 4162p.).

The Volta Grande Hydroelectric Power Plant (hereafter Volta Grande HPP) is located in the region of the lower Grande River at the boundary between the states of Minas Gerais and São Paulo in Southeast Brazil. This region is classified as of “High Biological Importance” for the conservation of birds in Minas Gerais (Drummond et al., 2005Drummond, G.M.; Martins, C.S. Machado, A.B.M; Sebaio, F.A. & Antonini, Y. 2005. Biodiversidade em Minas Gerais: um Atlas para sua conservação. 2.ed. Belo Horizonte, Fundação Biodiversitas. 220p.). Despite its importance, the avifauna of the region has yet to be adequately sampled (Silva, 1995Silva, J.M.C. 1995b. Avian inventory of the Cerrado region, South America: implications for biological conservation. Bird Conservation International, 5(2-3): 291-304.b), as evidenced by the low number of papers currently available in the ornithological literature (Silveira, 1998Silveira, L.F. 1998. The birds of Serra da Canastra National Park and adjacent areas, Minas Gerais, Brazil. Cotinga, 10: 55-63.; Andrade & Marini, 2002Andrade, R.D. & Marini, M.A. 2002. Bird species richness in natural forest patches in southeast Brazil. Lundiana, 3(2): 141-149.; MMA, 2005Ministério de Meio Ambiente (MMA). 2005. Plano de manejo do Parque Nacional da Serra da Canastra. Brasília, Ministério do Meio Ambiente/IBAMA. 104p.; Marçal-Júnior et al., 2009Marçal-Júnior, O.; Franchin, A.G.; Alteff, E.F.; Silva-Júnior, E.L. & Melo, C. 2009. Levantamento da avifauna na Reserva Ecológica Panga (Uberlândia, MG, Brasil). Bioscience Journal, 25(6): 149-164.; Bessa et al., 2011Bessa, R.; Parrini, R.; Abdala, A.; Kirwan, G.M.; Pimentel, L. & Bruno, S.F. 2011. Novos registros ornitológicos para a região da Serra da Canastra, Minas Gerais, Brasil. Cotinga, 33: 94-101.; IEF, 2011; Malacco et al., 2013Malacco, G.B.; Pioli, D., Silva-Junior, E.L.; Franchin, A.G.; Melo, C.; Silva, A.M. & Pedroni, F. 2013. Avifauna da Reserva do Clube Caça e Pesca Itororó de Uberlândia. Atualidades Ornitológicas, 173: 58-71.).

The objective of this study was to inventory the avifauna of the region of Volta Grande HPP, with the aim of increasing knowledge of its bird community. Specifically, the bird species of the community were characterized with regard to: (i) frequency of occurrence, (ii) trophic guild, (iii) dependence on forest habitat, (iv) endemism, (v) migratory condition and (vi) conservation status.

MATERIAL AND METHODS

Study area

Fieldwork was conducted in five sites distributed among four municipalities around the Volta Grande HPP reservoir (20°01′27″S, 48°12′45″W) (Table 1). The reservoir is located on the Grande River at the boundary between the states of Minas Gerais and São Paulo in Southeast Brazil. The reservoir is 46 years old, has an average elevation of 524 m and encompasses 19,800 ha (Fig. 1). The predominant morphoclimatic domain of the study region is Cerrado (Neotropical savanna). The region has a tropical climate with a dry winter (April to September) and a rainy summer (October to March) (Moreira et al., 2008Moreira, J.C.; Manduca, E.G.; Gonçalves, P.R.; Stumpp, R.; Pinto, C.G.C. & Lessa, G. 2008. Mammals, Volta Grande Environmental Unity, Triângulo Mineiro, states of Minas Gerais and São Paulo, Southeastern Brazil. Check List, 4: 349-357.). Mean annual rainfall ranges 1400-1600 mm, with the rainiest months being December and January, and the driest months June and July (Fujaco & Leite, 2016Fujaco, M.A.G. & Leite, M.G.P. 2016. Caracterização da paisagem do Reservatório de Volta Grande. In: Antonini, A. & Martins, J.P.V. (Eds.). Restauração e conservação de matas ciliares em reservatórios hidroelétricos. Ouro Preto, DEBIO-DEGEO/UFOP. p. 29-39.). The mean annual temperature ranges from 22°C to 24°C (Filardi et al., 2007Filardi, F.L.R.; Garcia, F.C.P. & Carvalho-Okano, R.M. 2007. Espécies lenhosas de Papilionoideae (Leguminosae) na Estação Ambiental de Volta Grande, Minas Gerais, Brasil. Rodriguésia, 58: 363-378.).

Figure 1
Grande River Basin located at the border between the states of Minas Gerais and São Paulo in Southeast Brazil. The five study sites are shown as: 1 and 2 located in Minas Gerais, and 3, 4 and 5 located in São Paulo.

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Table 1
Characteristics, coordinates and municipality of the five study sites.

The original vegetation of the region was mostly deforested or flooded during the construction of the Volta Grande HPP reservoir (from 1970 to 1974) (Pires et al., 2016Pires, M.R.S.; Magalhães, A.P.; Cruz, A.J.R.; Correa, M.R.J.; Mafia, P.O. & Martins, J.P.V. 2016. Conservação da fauna de vertebrados terrestres das matas ciliares do reservatório de Volta Grande. In: Antonini, A. & Martins, J.P.V. (Eds.). Restauração e conservação de matas ciliares em reservatórios hidroelétricos. Ouro Preto, MG, DEBIO-DEGEO/UFOP. p. 69-85.). Four out of the five study sites contain revegetated riparian forest patches that were the result of a reforestation program undertaken by the Minas Gerais state energy company (CEMIG). One of the sites has fragments of native vegetation. Together the five sites encompass a total of 423.8 ha.

Sampling

Field surveys were conducted during four months of each climatic season: April, May, June and July 2013 (dry season), and October, November, December 2013 and January 2014 (rainy season). The five study sites were sampled over the course of five consecutive days each month such that each site was sampled once per month. Quantitative data were collected using the point-count method (Vielliard et al., 2010Vielliard, J.M.E.; Almeida, M.E.C.; Anjos, I. & Silva, W.R. 2010. Levantamento quantitativo por pontos de escuta e o índice pontual de abundância (IPA). In: Matter, S.V.; Straube, F.C.; Accordi, I.; Piacentini, V. & Cândido-Jr., J.F. (Eds.). Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro, Technical Books. p. 47-60.), with six points in each site (three within riparian forest and three in surrounding areas) being sampled per campaign. Points were separated by 350 m to avoid overlapping of territory of some species (Ralph et al., 1995Ralph, C.J.; Sauer, J.R. & Droege, S. 1995. Monitoring bird populations by point counts. Albania,: U.S. Department of Agriculture. 191p. (General Technical Report PSW-GTR-149); Vielliard et al., 2010Vielliard, J.M.E.; Almeida, M.E.C.; Anjos, I. & Silva, W.R. 2010. Levantamento quantitativo por pontos de escuta e o índice pontual de abundância (IPA). In: Matter, S.V.; Straube, F.C.; Accordi, I.; Piacentini, V. & Cândido-Jr., J.F. (Eds.). Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro, Technical Books. p. 47-60.). Due to this distance it wasn’t necessary to establish a limiting radius for the detection of bird individuals. Point-counts of a given site were performed in the mornings (between 06:00 and 09:00 h), with points being sampled in a randomly determined order. The number of individuals of all bird species seen and/or heard during 20 min at each point was recorded (six points × 20 min × eight monthly visits = 960 min for each site).

Qualitative bird surveys were conducted through ad libitum observations during and after quantitative sampling between 06:00 to 11:00 and 13:00 to 18:00 h, for a sampling effort of 10 h of sampling/day (10 h sampling × eight monthly visits = 80 h sampling per site; 400 h total for all five sites).

Ten mist-nets (12 m × 2.5 m, 20 mm mesh) (License ICMBio № 36758-2) were opened within riparian forests from 06:00 to 17:00 h and checked every 30 min, for a total effort of 132,000 h.m² (computed according to Straube & Bianconi, 2003Straube, F.C. & Bianconi, G.V. 2003. Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes de-neblina. Chiroptera Neotropical, 8(1-2): 150-152.). Captured birds were marked with standard CEMAVE/ICMBio metallic bands (License № 367581), photographed, measured and released at the point of capture.

Adequacy of sampling effort was evaluated by constructing a species accumulation curve (Santos, 2003Santos, A.J. 2003. Estimativas de riqueza em espécies. In: Cullen-Júnior, L.; Rudran, R. & Valladares-Pádua, C. (Eds.). Métodos de estudos em biologia da conservação e manejo da vida silvestre. Curitiba, Editora da Universidade Federal do Paraná. p. 19-42.). Bird richness was estimated by the Chao 1 index using EstimateS 9.1 software (Colwell, 2009Colwell, R.K. 2009. EstimateS: Statistics of estimation of species richness and shared species form samples. Version 9.1.), which is based on the number of singletons and doubletons in each point count (Hortal et al., 2006Hortal, J.; Borges, P.A.V. & Gaspar, C. 2006. Evaluating the performance of species richness estimators: sensitivity to sample grain size. Journal of Animal Ecology, 75: 274-287.).

Birds were identified visually with binoculars, by photography (Canon PowerShot SX50 HS) or audibly. A Sony ICD-PX312 recorder was used to document vocalizations. Photographs and recordings that were archived on WikiAves (2019WikiAves (A Enciclopédia das Aves do Brasil). 2019. A Enciclopédia das Aves do Brasil. Available at: www.wikiaves.com.
www.wikiaves.com... ) are identified in Table 2.

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Table 2
Bird species recorded in the five study sites located in the region of the reservoir of the Volta Grande Hydroelectric Power Plant in Southeast Brazil, and their frequency of occurrence (FO), trophic guild (TG), forest habitat dependence (FHD), threat status, and migratory condition. Reference numbers for the online database www.wikiaves.com.br (WA) are also provided. Taxonomy and nomenclature follow Piacentini et al. (2015Piacentini, V.Q.; Aleixo, A.; Agne, C.E.; Maurício, G.N.; Pacheco, J.F.; Bravo, G.A.; Brito, G.R.R.; Naka, L.N.; Olmos, F.; Posso, S.; Silveira, L.F.; Betini, G.S.; Carrano, E.; Franz, I.; Lees, A.C.; Lima, L.M.; Pioli, D.; Schunck, F.; Amaral, F.R.; Bencke, G.A.; Cohn-Haft, M.; Figueiredo, L.F.A.; Straube F.C. & Cesari, E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee/Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Revista Brasileira de Ornitologia, 23(2): 91-298.).

Data analysis

Frequency of Occurrence (FO) was determined for each bird species based on the proportion of effort units (days) during which a given species was detected (adapted from Costa & Rodrigues (2012Costa, L.M. & Rodrigues, M. 2012. Bird community structure and dynamics in the campos rupestres of southern Espinhaço Range, Brazil: diversity, phenology and conservation. Revista Brasileira de Ornitologia, 20(2): 132-147.)) as: C (common) - species recorded between 75-100% of sampling days; RC (relatively common) - species recorded between 50-74% of sampling days; UC (uncommon) - species recorded between 25-49% of sampling days; R (rare) - species recorded between 6-24% of sampling days and O (occasional) - species recorded in less than 5% of the sampling days (effort was one day per sampling site and the presence of each species was only recorded once per sampling day).

Bird species were grouped into 25 trophic guilds considering not only food items, but also the environment and vertical strata most utilized during foraging (adapted from Willis (1979Willis, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia, 33(1): 1-25.) and Antunes (2005Antunes, A.Z. 2005. Alterações na composição da comunidade de aves ao longo do tempo em um fragmento florestal no sudeste do Brasil. Ararajuba, 13: 47-61.)): canopy frugivores (FRU-C), ground frugivores (FRU-G), canopy omnivores (OMNI-C), understory omnivores (OMNI-US), edge omnivores (OMNI-E), ground omnivores (OMNI-G), aquatic omnivores (OMNI-AQ), marsh omnivores (OMNI-M), nocturnal carnivores (CAR-N), diurnal carnivores (CAR-D), carrion eaters (CE), trunk and twig insectivores (INS-TT), predators of large ground arthropods (INS-LG), predators of small ground arthropods (INS-SG), predators of foliage arthropods (INS-F), bamboo or tangle insectivores (INS-BT), midlevel insectivores (INS-ML), canopy insectivores (INS-C), edge insectivores (INS-E), marsh insectivores (INS-M), aerial insectivores (INS-A), nocturnal insectivores (INS-N), nectarivores (NEC), granivores (GRA) and piscivores (PIS).

Bird species were classified into three categories of forest habitat dependence following Silva (1995Silva, J.M.C. 1995a. Birds of the Cerrado region, South America. Steenstrupia, 21: 69-92.a): (1) independent - species that forage and breed mainly in open vegetation; (2) semi-dependent - species that forage and breed in both forest habitats and open areas; and (3) dependent - species that forage and breed mainly in forest habitats. Endemism for the Cerrado was based on Silva (1995aSilva, J.M.C. 1995a. Birds of the Cerrado region, South America. Steenstrupia, 21: 69-92.) while endemism for riparian forest habitats followed Silva & Vielliard (2000Silva, W.R. & Vielliard, J. 2000. Avifauna de Mata Ciliar. In: Rodrigues, R.R. & Leitão-Filho, H.F. (Eds.). Matas Ciliares: conservação e recuperação. São Paulo, EDUSP. p. 169-185.).

The species were also classified according to their migratory condition according Chesser (1994Chesser, R.T. 1994. Migration in South America: an overview of the austral system. Bird Conservation International, 4: 91-107.), Sick (1997Sick, H. 1997. Ornitologia brasileira. Rio de Janeiro, Ed. Nova Fronteira. 912p.) and Somenzari et al. (2018Somenzari, M.; Amaral, P.P.; Cueto, V.R.; Guaraldo, A.C.; Jahn, A.E.; Lima, D.M.; Lima, P.C.; Lugarini, C.; Machado, C.G.; Martinez, J.; Nascimento, J.L.X.; Pacheco, J.F.; Paludo, D.; Prestes, N.P.; Serafini, P.P.; Silveira, L.F.; Sousa, A.E.B.A.; Sousa, N.A.; Souza, M.A.; Telino-Júnior, W.R. & Whitney, B.M. 2018. An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia, 58: 2-66, e20185803.) as: septentrional migrants (SM) - species from the northern hemisphere; and austral migrants (AM) - species that breed in temperate continental South America and migrate north, towards Amazonia, during the austral winter. Also included in this category are those resident species whose southernmost populations perform small-scale seasonal migrations.

We highlighted those species considered threatened in the state of Minas Gerais (COPAM, 2010Conselho Estadual de Política Ambiental (COPAM). 2010. Deliberação Normativa COPAM № 147, de 30 de abril de 2010. Aprova a Lista de Espécies Ameaçadas de Extinção da Fauna do Estado de Minas Gerais. Diário Executivo, Minas Gerais. Available at: www.siam.mg.gov.br/sla/download.pdf?idNorma=13192.
www.siam.mg.gov.br/sla/download.pdf?idNo... ; Drummond et al., 2008Drummond, G.M.; Machado, A.B.M.; Martins, C.S.; Mendonça, M.P. & Stehmann, J.R. 2008. Listas vermelhas das espécies da fauna e da flora ameaçadas de extinção em Minas Gerais. Belo Horizonte, Fundação Biodiversitas. for near threatened and data-deficient species), the state of São Paulo (Bressan et al., 2009Bressan, P.M.; Kierulff, M.C.M. & Sugieda, A.M. 2009. Fauna ameaçada de extinção no Estado de São Paulo: Vertebrados. São Paulo, Fundação Parque Zoológico de São Paulo. 645p.), nationally (ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2018. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília, ICMBio. 4162p.) and globally (IUCN, 2020International Union for Conservation of Nature and Natural Resources (IUCN). 2020. The IUCN Red List of Threatened Species. Version 2020-1. Available at: Available at: https://www.iucnredlist.org . Access in: 14/04/2020.
https://www.iucnredlist.org... ). Scientific names followed Piacentini et al. (2015Piacentini, V.Q.; Aleixo, A.; Agne, C.E.; Maurício, G.N.; Pacheco, J.F.; Bravo, G.A.; Brito, G.R.R.; Naka, L.N.; Olmos, F.; Posso, S.; Silveira, L.F.; Betini, G.S.; Carrano, E.; Franz, I.; Lees, A.C.; Lima, L.M.; Pioli, D.; Schunck, F.; Amaral, F.R.; Bencke, G.A.; Cohn-Haft, M.; Figueiredo, L.F.A.; Straube F.C. & Cesari, E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee/Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Revista Brasileira de Ornitologia, 23(2): 91-298.).

RESULTS

A total of 224 bird species distributed among 24 orders and 58 families was recorded (Table 2). Passeriformes was the most representative order with 113 species, corresponding to 50% of the total recorded. The most representative family was Tyrannidae, with 35 species (16%), followed by Thraupidae (23 species; 10%). Among non-Passeriformes, the most representative families were Ardeidae, Psittacidae and Trochilidae, each one with nine species (4%).

The species richness curve produced by the Chao 1 index estimated (mean ± SD) 232 ± 8.7 species for the study area (Fig. 2). Thus, the observed richness represented 97% of the estimated richness.

Figure 2
Bird species accumulation curve and estimated richness curve obtained from the Chao 1 index for the study area located throughout the reservoir of the Volta Grande Hydroelectric Power Plant in Southeast Brazil. Vertical bars represent the standard deviation of the estimate.

According to the FO estimates, only 16% (n = 36) of the recorded species were considered common in the study area (Table 2). Among the common species, only five (2%) had an FO of 100% by being present in all samples (Table 2). The majority of the species (50%, n = 113) were classified as occasional or rare. Thirty-two species (14%) were recorded only once in the study area (single records) (Table 2).

Fifty-two percent of the bird species recorded (n = 117) were forest independent, while 19% (n = 42) were strictly dependent on forest habitats for breeding or foraging. Three recorded species were endemic to the Cerrado: Herpsilochmus longirostris, Clibanornis rectirostris, and Antilophia galeata. These three species were also considered endemic of the Central Brazil riparian forests (Silva & Vielliard, 2000Silva, W.R. & Vielliard, J. 2000. Avifauna de Mata Ciliar. In: Rodrigues, R.R. & Leitão-Filho, H.F. (Eds.). Matas Ciliares: conservação e recuperação. São Paulo, EDUSP. p. 169-185.).

Eighty-five migratory species were recorded, corresponding to 38% of the total sampled. Only four species came from the Northern Hemisphere (Table 2), while the remaining migratory species came from the southernmost regions of South America. Thirty-three of the recorded species appeared in at least one of the lists of endangered, near threatened and data-deficient species considered in this study (Table 2). In study sites located in the state of Minas Gerais three species were considered threatened in the state: Crax fasciolata, Mycteria americana, and Ara ararauna (COPAM, 2010Conselho Estadual de Política Ambiental (COPAM). 2010. Deliberação Normativa COPAM № 147, de 30 de abril de 2010. Aprova a Lista de Espécies Ameaçadas de Extinção da Fauna do Estado de Minas Gerais. Diário Executivo, Minas Gerais. Available at: www.siam.mg.gov.br/sla/download.pdf?idNorma=13192.
www.siam.mg.gov.br/sla/download.pdf?idNo... ). C. fasciolata also appears on the IUCN red list, in the “vulnerable” category (IUCN, 2020International Union for Conservation of Nature and Natural Resources (IUCN). 2020. The IUCN Red List of Threatened Species. Version 2020-1. Available at: Available at: https://www.iucnredlist.org . Access in: 14/04/2020.
https://www.iucnredlist.org... ). Two other species present in the Minas Gerais red list were registered only in areas located in the state of São Paulo: Platalea ajaja and Sporophila angolensis.

According to the red list of threatened species of the state of São Paulo, 24 species recorded in study sites located in this state were under some degree of threat of extinction (Table 2). Amazona aestiva was classified as Near Threatened in the Brazilian national list (ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2018. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília, ICMBio. 4162p.) (Table 2).

The trophic guilds with the greatest number of species were edge insetivores (n = 25), edge omnivores (n = 21), canopy frugivores (n = 15), piscivores (n = 13) and granivores (n = 13) (Table 3). Bamboo or tangle insectivores, understory omnivores and nocturnal carnivores were the least representative trophic guilds with only one species each.

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Table 3
Number of species per each trophic guild recorded on the region of reservoir of Volta Grande Hydroelectric Power Plant in Southeast Brazil.

DISCUSSION

The region of the lower Grande River was found to possess high bird species richness, with various threatened (almost exclusively locally, present only in State lists; with the exception of C. fasciolata, present in the global list) and some endemic species. The area was also found to be a feeding and resting area for migratory birds, confirming its status as an area of “High Biological Importance” for the conservation of birds in the states of Minas Gerais (Drummond et al., 2005Drummond, G.M.; Martins, C.S. Machado, A.B.M; Sebaio, F.A. & Antonini, Y. 2005. Biodiversidade em Minas Gerais: um Atlas para sua conservação. 2.ed. Belo Horizonte, Fundação Biodiversitas. 220p.). The species accumulation curve indicated that the sampling effort satisfactorily detected a significant portion of the region’s avifauna. In fact, at 50% of the total sampling effort, 89% (n = 200) of the species had already been recorded. It is important to emphasize that most of the sampling sites were reforested areas, reaffirming their importance to bird communities.

Studies addressing the bird community of non-urban areas of the region of the lower Grande River and Paranaíba River (Triângulo Mineiro region) are extremely scarce in the scientific literature. The few that do exist have found 403 bird species for Serra da Canastra National Park (2,000,000 ha, and 90 km from the study area) (Silveira, 1998Silveira, L.F. 1998. The birds of Serra da Canastra National Park and adjacent areas, Minas Gerais, Brazil. Cotinga, 10: 55-63.; Andrade & Marini, 2002Andrade, R.D. & Marini, M.A. 2002. Bird species richness in natural forest patches in southeast Brazil. Lundiana, 3(2): 141-149.; MMA, 2005Ministério de Meio Ambiente (MMA). 2005. Plano de manejo do Parque Nacional da Serra da Canastra. Brasília, Ministério do Meio Ambiente/IBAMA. 104p.; Bessa et al., 2011Bessa, R.; Parrini, R.; Abdala, A.; Kirwan, G.M.; Pimentel, L. & Bruno, S.F. 2011. Novos registros ornitológicos para a região da Serra da Canastra, Minas Gerais, Brasil. Cotinga, 33: 94-101.); 231 species for RPPN Panga Ecological Reserve (410 ha, and 130 km from the study area) (Marçal-Júnior et al., 2009Marçal-Júnior, O.; Franchin, A.G.; Alteff, E.F.; Silva-Júnior, E.L. & Melo, C. 2009. Levantamento da avifauna na Reserva Ecológica Panga (Uberlândia, MG, Brasil). Bioscience Journal, 25(6): 149-164.); 202 species for a private reserve located in the municipality of Uberlândia (640 ha, and about 130 km from the study area) (Malacco et al., 2013Malacco, G.B.; Pioli, D., Silva-Junior, E.L.; Franchin, A.G.; Melo, C.; Silva, A.M. & Pedroni, F. 2013. Avifauna da Reserva do Clube Caça e Pesca Itororó de Uberlândia. Atualidades Ornitológicas, 173: 58-71.), 221 species for Pau Furado State Park (2,000 ha, and 140 km from the study area) (IEF, 2011Instituto Estadual de Florestas (IEF). 2011. Plano de manejo do Parque Estadual do Pau Furado. Uberlândia, MG, Instituto Estadual de Florestas. 650p.), and 328 species for the 17 forest remnants in northwestern São Paulo state (Bispo et al., 2011Bispo, A.A.; Hasui, E. & Pedro, W.A. 2011. Aves da região noroeste do estado de São Paulo. In: Necchi Junior, O. (Org.). Fauna e flora de fragmentos florestais remanescentes da região noroeste do estado de São Paulo. Ribeirão Preto, Holos Editora. p. 242-268.).

Two-percent of the species encountered in the present study had 100% FO. Studying rural forest fragments in the state of São Paulo, Almeida et al. (1999Almeida, M.E.C.; Vielliard, J.M.E. & Dias, M.M. 1999. Composição da avifauna em duas matas ciliares na bacia do rio Jacaré-Pepira, São Paulo, Brasil. Revista Brasileira de Zoologia, 16(4): 1087-1098.) and Donatelli et al. (2004Donatelli, R.J.; Costa, T.V.V. & Ferreira, C.D. 2004. Dinâmica da avifauna em fragmentos de mata na Fazenda Rio Claro, Lençóis Paulista, São Paulo, Brasil. Revista Brasileira de Zoologia, 21: 97-114.) also found a very low number of species with 100% FO, with 1% and 3%, respectively. The majority of bird species recorded (50%) in our study were classified as occasional and rare, with FOs of less than 25%. A similar result was obtained by Almeida et al. (1999Almeida, M.E.C.; Vielliard, J.M.E. & Dias, M.M. 1999. Composição da avifauna em duas matas ciliares na bacia do rio Jacaré-Pepira, São Paulo, Brasil. Revista Brasileira de Zoologia, 16(4): 1087-1098.) in two areas located in the Jacaré-Pepira River Basin (rural state of São Paulo), and by Lyra-Neves et al. (2004Lyra-Neves, R.M.; Dias, M.M.; Azevedo-Júnior, S.M.; Telino-Júnior, W.R. & Larrazábal, M.E.L. 2004. Comunidade de aves da Reserva Estadual de Gurjaú, Pernambuco, Brasil. Revista Brasileira de Zoologia, 21(3): 581-592.) in a study in the Gurjau State Reserve, state of Pernambuco. The low percentage of species with 100% FO, and the high percentage with FOs of less than 25%, can be explained by the presence of wandering species that remain in areas for a few days, species with inconspicuous vocalizations and/or behaviors, accidental species from neighboring habitats and migratory species. It can also be explained by the possibility that the studied sites do not possess the resources and conditions necessary to maintain larger bird populations (Aleixo & Vielliard, 1995Aleixo, A.J. & Vielliard, M.E. 1995. Composição e dinâmica da avifauna da mata de Santa Genebra, Campinas, São Paulo, Brasil. Revista Brasileira de Zoologia, 12(3): 493-511.; Donatelli et al., 2007Donatelli, R.J.; Ferreira, C.D.; Dalberto, A.C. & Posso, S.R. 2007. Análise comparativa da assembleia de aves em dois remanescentes florestais no interior do Estado de São Paulo, Brasil. Revista Brasileira de Zoologia, 24: 362-375.).

The guild of edge insectivores is commonly favored by small patches because birds of this guild possesses foraging plasticity, being able to search for food among different strata such as in tangled vegetation and in the middle and canopy levels (Willis, 1979Willis, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia, 33(1): 1-25.; Borges & Stouffer, 1999Borges, S.H. & Stouffer, P.C. 1999. Bird communities in two types of anthropogenic successional vegetation in central Amazonia. The Condor, 101: 529-536.; Stouffer et al., 2009Stouffer, P.C.; Strong, C. & Naka, L.N. 2009. Twenty years of understorey bird extinctions from Amazonian rain forest fragments: consistent trends and landscape-mediated dynamics. Diversity and Distribution, 15: 88-97.). The data obtained in the present study support this assertion because the guild edge insectivores was the trophic guild with the greatest number of species. This result is also likely due to the sampling performed in surrounding open areas, which included edges of the forest fragments. In contrast, insectivorous species foraging in the lower strata, such as predators of small ground arthropods, predators of foliage arthropods and understory omnivores, tend to be more susceptible to habitat degradation due to the consequent structural simplification of the environment, and, thus, are less common in small patches (Willis, 1979Willis, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia, 33(1): 1-25.; Castaño-Villa et al., 2014Castaño-Villa, G.J.; Ramos-Valencia, S.A. & Fontúrbel, F.E. 2014. Fine-scale habitat structure complexity determines insectivorous bird diversity in a tropical Forest. Acta Oecologica, 61: 19-23.; Cid & Caviedes-Vidal, 2014Cid, F.D. & Caviedes-Vidal, E. 2014. Differences in bird assemblages between native natural habitats and small-scale tree plantations in the semiarid midwest of Argentina. The Wilson Journal of Ornithology, 126(4): 673-685.). Structural simplification of the environment and the inability to adapt to the surrounding open habitat has a greater influence on species of these guilds than the availability of arthropods as a food resource (Sekercioglu et al., 2002Sekercioglu, C.H.; Ehrlich, P.R.; Daily, G.C.; Aygen, D.; Goehring, D. & Sandy, R.F. 2002. Disappearance of insectivorous birds from tropical forest fragments. Proceedings of the National Academy of Sciences, 99: 263-267.). Predators of foliage arthropods and understory omnivores were among the guilds with the lowest number of species in the present study. In contrast, the guild of edge omnivores has been shown to be favored by small patches due to the larger proportion of edge environments in these habitats (Willis, 1979Willis, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia, 33(1): 1-25.; Austen et al., 2001Austen, M.J.W.; Francis, C.M.; Burke, D.M. & Bradstreet, M.S.W. 2001. Landscape context and fragmentation effects on forest birds in southern Ontario. The Condor, 103(4): 701-714.; Anjos et al., 2007Anjos, L.; Volpato, G.H.; Lopes, E.V.; Serafini, P.P.; Poletto, F. & Aleixo, A. 2007. The importance of riparian forest for the maintenance of bird species richness in an Atlantic Forest remnant, southern Brazil. Revista Brasileira de Zoologia, 24(4): 1078-1086.), which likely explains why this guild was well represented (second greatest number of species) in the present study.

Species of the guild bamboo or tangle insectivores can be considered specialized microhabitat foragers (Goerck, 1997Goerck, J.M. 1997. Patterns of rarity in the birds of the Atlantic Forest of Brazil. Conservation Biology, 11: 112-118.; Areta & Cockle, 2012Areta, J.I. & Cockle, K.L. 2012. A theoretical framework for understanding the ecology and conservation of bamboo-specialist birds. Journal of Ornithology, 153(Suppl. 1): S163-S170.; Lebbin, 2013Lebbin, D.J. 2013. Nestedness and patch size of bamboo-specialist bird communities in southeastern Peru. The Condor, 115(2): 230-236.), and thus tend to be rare in small patches since they are competitively excluded by edge insectivores (Willis, 1979Willis, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia, 33(1): 1-25.; Cockle & Areta, 2013Cockle, K.L. & Areta, J.I. 2013. Specialization on Bamboo by Neotropical Birds. The Condor, 115(2): 217-220.). The only species of the bamboo or tangle insectivores guild recorded in the present study was Poecilotriccus latirostris. This species is the most widely distributed species of its genus in western Brazil, and is characteristic of middle and lower strata of tangled vegetation in riparian forests of Central Brazil (Sick, 1997Sick, H. 1997. Ornitologia brasileira. Rio de Janeiro, Ed. Nova Fronteira. 912p.; Sigrist, 2013Sigrist, T. 2013. Avifauna Brasileira guia de campo. São Paulo, Avis Brasilis. 592p.).

It is important to highlight the occurrence of only one species of more specialized insectivorous as regards the foraging site: Dendrocolaptes platyrostris. The woodcreepers are trunk and twig insectivores that forage preferentially on senile trees. They are also sensitive to environmental disturbances, and thus are the first to disappear locally when environmental degradation occurs (Laurance et al., 2002Laurance, W.F.; Lovejoy, T.E.; Vasconcelos, H.L.; Bruna, E.M.; Didham, R.K.; Stouffer, P.C.; Gascon, C.; Bierregaard, R.O.; Laurance, S.G. & Sampaio, E. 2002. Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conservation Biology, 16(3): 605-618.; Cleary et al., 2007Cleary, D.F.R.; Boyle, T.J.B.; Setyawati, T.; Anggraeni, C.D.; Van-Loon, E.E. & Menken, S.B.J. 2007. Bird species and traits associated with logged and unlogged forest in Borneo. Ecological Applications, 17(4): 1184-1197.; Dahal et al., 2015Dahal, B.R.; McAlpine, C.A. & Maron, M. 2015. Impacts of extractive forest uses on bird assemblages vary with landscape context in lowland Nepal. Biological Conservation, 186: 167-175.).

Large frugivores (e.g., Crypturellus spp., Crax spp. and Penelope spp.) which feed mostly on the ground were poorly represented in the present study. Overall, frugivores are more susceptible to local extinction because their populations are possibly limited by the availability of fruit during periods of scarcity (Antunes, 2005Antunes, A.Z. 2005. Alterações na composição da comunidade de aves ao longo do tempo em um fragmento florestal no sudeste do Brasil. Ararajuba, 13: 47-61.; Cleary et al., 2007Cleary, D.F.R.; Boyle, T.J.B.; Setyawati, T.; Anggraeni, C.D.; Van-Loon, E.E. & Menken, S.B.J. 2007. Bird species and traits associated with logged and unlogged forest in Borneo. Ecological Applications, 17(4): 1184-1197.; Kennedy et al., 2010Kennedy, C.M.; Marra, P.P.; Fagan, W.F. & Neel, M.C. 2010. Landscape matrix and species traits mediate responses of Neotropical resident birds to forest fragmentation in Jamaica. Ecological Monographs, 80(4): 651-669.) and by hunting (Peres, 2001Peres, C.A. 2001. Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conservation Biology, 15(6): 1490-1505.). Thus, species belonging to this guild tend to disappear from small patches, since they require areas with a wide variety of tree species that produces fruit at different seasons of the year (Willis, 1979Willis, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia, 33(1): 1-25.; Piratelli et al., 2005Piratelli, A.; Andrade, V.A. & Lima-Filho, M. 2005. Aves de fragmentos florestais em área de cultivo de cana-de-açúcar no sudeste do Brasil. Iheringia Série Zoologia, 95: 217-222.; Ferger et al., 2014Ferger, S.W.; Schleuning, M.; Hemp, A.; Howell, K.M. & Böhning-Gaese, K. 2014. Food resources and vegetation structure mediate climatic effects on species richness of birds. Global Ecology and Biogeography, 23(5): 541-549.). Also, large frugivores are cinegetic species, i.e, species that suffer from hunting pressure by humans (Pereira & Schiavetti, 2010Pereira, J. & Schiavetti, A. 2010. Conhecimentos e usos da fauna cinegética pelos caçadores indígenas ‘Tupinambá de Olivença’ (Bahia). Biota Neotropica, 10: 175-183.), and this impact associated with habitat loss can drive these species to extinction (Simberloff, 1995Simberloff, D. 1995. Habitat fragmentation and population extinction of birds. Ibis, 137(Suppl. 1): S105-S111.; Symes et al., 2018Symes, W.S.; Edwards, D.P.; Miettinen, J.; Rheindt, F.E. & Carrasco, L.R. 2018. Combined impacts of deforestation and wildlife trade on tropical biodiversity are severely underestimated. Nature Communications, 9: 4052.). In the study region occurs the Speckled chachalaca (Ortalis remota) in São Paulo state. Deforestation caused mainly by the construction of the Lower Grande reservoir may be responsible for the extinction of this species in Minas Gerais state (Silveira et al., 2017Silveira, L.F.; Tomotani, B.M.; Cestari, C.; Straube, F.C. & Piacintini, V.Q. 2017. Ortalis remota: a forgotten and critically endangered species of chachalaca (Galliformes: Cracidae) from Eastern Brazil. Zootaxa, 4306: 524-536.).

Like large frugivores, nectarivores birds are also dependent on plant species that contribute with food resources throughout the year (Bennett et al., 2014Bennett, J.M.; Clarke, R.H.; Thomson, J.R. & Nally, R.M. 2014. Variation in abundance of nectarivorous birds: does a competitive despot interfere with flower tracking? Journal of Animal Ecology, 83(6): 1531-1541.; Rodrigues & Rodrigues, 2015Rodrigues, L.C. & Rodrigues, M. 2015. Floral resources and habitat affect the composition of hummingbirds at the local scale in tropical mountaintops. Brazilian Journal of Biology, 75(1): 39-48.). According to Willis (1979Willis, E.O. 1979. The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos de Zoologia, 33(1): 1-25.) and Bowen et al. (2009Bowen, M.E.; McAlpine, C.A.; Seabrook, L.M.; House, A.P.N. & Smith, G.C. 2009. The age and amount of regrowth forest in fragmented brigalow landscapes are both important for woodland dependent birds. Biological Conservation, 142: 3051-3059.), the few plant diversity and the structural simplification in small patches probably explains the tendency to the nectarivores to disappear from these habitats. On the other hand, there is evidence that in the Neotropical region nectarivores birds are not very sensitive to the habitat fragmentation effects, and may even be benefited by the high abundance of light-dependent plants and the increase of flower production in clearings and forest edges (Vetter et al., 2011Vetter, D.; Hansbauer, M.M.; Vegvari, Z. & Storch, T. 2011. Predictors of forest fragmentation sensitivity in Neotropical vertebrates: a quantitative review. Ecography, 34: 1-8.). Still according to Vetter et al. (2011Vetter, D.; Hansbauer, M.M.; Vegvari, Z. & Storch, T. 2011. Predictors of forest fragmentation sensitivity in Neotropical vertebrates: a quantitative review. Ecography, 34: 1-8.), nectarivores often travel long distances to find their food resources and are able to cross open areas. Thus, to better understand this relationship, future studies are needed to evaluate how these trophic guild responds to the consequences of the fragmentation processes and habitat loss.

According to Silva (1995Silva, J.M.C. 1995a. Birds of the Cerrado region, South America. Steenstrupia, 21: 69-92.a), 52% of the 759 bird species that reproduce in the Cerrado are dependent on forest habitat. However, species dependent on forest habitat corresponded to only 19% of all the species recorded in the present study (see Table 2). According to Laurance et al. (2002Laurance, W.F.; Lovejoy, T.E.; Vasconcelos, H.L.; Bruna, E.M.; Didham, R.K.; Stouffer, P.C.; Gascon, C.; Bierregaard, R.O.; Laurance, S.G. & Sampaio, E. 2002. Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conservation Biology, 16(3): 605-618.), a reduced number of forest bird species in small, isolated and impacted patches can be due to morphological and behavioral constraints.

Another possible explanation for the reduced number of forest species in isolated fragments is the reluctance of these species to cross open areas, possibly due to the increased predation risk (Watson et al., 2004Watson, J.E.M.; Whittaker, R.J. & Dawson, T.P. 2004. Habitat structure and proximity to forest edge affect the abundance and distribution of forest-dependent birds in tropical coastal forests of southeastern Madagascar. Biological Conservation, 120(3): 311-327.; Piratelli et al., 2005Piratelli, A.; Andrade, V.A. & Lima-Filho, M. 2005. Aves de fragmentos florestais em área de cultivo de cana-de-açúcar no sudeste do Brasil. Iheringia Série Zoologia, 95: 217-222.). These studies reported that the probability that an individual will cross an open field between two forest fragments decreases rapidly as the distance between fragments increases.

The most important action for the conservation of species dependent on forest habitats is to prevent future forest losses, and to conduct habitat restoration. These two activities should be the most effective conservation strategies for ensuring the persistence of forest birds in fragmented landscapes (Mortelliti et al., 2010Mortelliti, A.; Fagiani, S.; Battisti, C.; Capizzi, D. & Boitani, L. 2010. Independent effects of habitat loss, habitat fragmentation and structural connectivity on forest-dependent birds. Diversity and Distributions, 16(6): 941-951.; Mendoza et al., 2014Mendoza, S.V.; Harvey, C.A.; Saenz, J.C.; Casanoves, F.; Carvajal, J.P.; Villalobos, J.G.; Hernandez, B.; Medina, A.; Montero, J.; Merlo, D.S. & Sinclair, F.L. 2014. Consistency in bird use of tree cover across tropical agricultural landscapes. Ecological Applications, 24(1): 158-168.). In the long-term, conservation of the species dependent on forest habitats in the area of the present study, like C. fasciolata, M. nigrifrons, and C. rectirostris, is unfavorable because the few forest remnants remaining are small, isolated from each other, and among a habitat matrix that is predominantly impermeable to forest species displacements (mostly sugar cane plantations). Furthermore, most of the remnants do not receive effective conservation measures.

On the other hand, most of the birds recorded in the present study were classified as forest independent (52%) or semi-dependent (29%) species (see Table 2). For these species, the matrix may be more permeable, allowing movements among different isolated forest patches (Yabes et al., 2010Yabes, R.S.; Marques, E.J. & Marini, M.A. 2010. Movements of birds among natural vegetation patches in the Pantanal, Brazil. Bird Conservation International, 20(4): 400-409.). Characteristics of the matrix will then favor or not bird movements. In our study area, most of the matrix was composed by sugar cane crops and pasture lands (≈ 90%). This structure will limit movements or modify movements of the birds. In pasture lands, for example, forest-dependent and semi-dependent birds will probably perform fast and straight flights direct to the nearest forest patch, while in sugar cane crops, flights would be slowly because birds could use sugar cane as cover to protection against predators (Biz et al., 2017Biz, M.; Cornelius, C. & Metzger, J.P.W. 2017. Matrix type affects movement behavior of a Neotropical understory forest bird. Perspectives in Ecology and Conservation, 15: 10-17.). Thus, in our study area, due to the structure of the matrix and the isolation of the forest patches, movements across the matrix would be performed mostly by independent bird species, decreasing the genetic flow and persistence of the forest dependent species (Braunisch et al., 2010Braunisch, V.; Segelbacher, G. & Hirzel, A.H. 2010. Modelling functional landscape connectivity from genetic population structure: a new spatially explicit approach. Molecular Ecology, 19(17): 3664-3678.; Prevedello & Vieira, 2010Prevedello, J.A. & Vieira, M.V. 2010. Does the type of matrix matter? A quantitative review of the evidence. Biodiversity Conservation, 19(5): 1205-1223.). The disappearance of forest-dependent birds in the region, like Arremon semitorquatus and Chordeiles pussillus, have been already recorded (Willis & Oniki, 2002Willis, E.O. & Oniki, Y. 2002. Birds of a central São Paulo woodlot: 1: censuses1982-2000. Brazilian Journal of Biology, 62(2): 197-210.; Silveira & Uezu, 2011Silveira, L.F. & Uezu, A. 2011. Checklist das aves do Estado de São Paulo, Brasil. Biota Neotropica, 11: 83-110.).

Some authors have indicated that the adverse effects of vegetation degradation and the isolation of the resultant fragments affect more negatively endemic species than species with broad geographic distributions (Aleixo & Vielliard, 1995Aleixo, A.J. & Vielliard, M.E. 1995. Composição e dinâmica da avifauna da mata de Santa Genebra, Campinas, São Paulo, Brasil. Revista Brasileira de Zoologia, 12(3): 493-511.; Ribon et al., 2003Ribon, R.; Simon, J.E. & Mattos, G.T. 2003. Bird extinctions in Atlantic Forest fragments of the Viçosa region, Southeastern Brazil. Conservation Biology, 17(6): 1827-1839.). These authors refer to geographic endemism and not ecological endemism, because data from the literature show that ecologically endemic species of riparian forests often maintain linear territories along riverbanks and, for this reason, do not suffer significant changes due to variation in riparian forest size (Shirley & Smith, 2005Shirley, S.M. & Smith, J.N.M. 2005. Bird community structure across riparian buffer strips of varying width in a coastal temperate forest. Biological Conservation, 125(4): 475-489.; Lees & Peres, 2008Lees, A.C. & Peres, C.A. 2008. Conservation value of remnant riparian forest corridors of varying quality for Amazonian birds and mammals. Conservation Biology, 22(2): 439-449.).

Of the three Cerrado endemic species recorded in this study, only A. galeata was not recorded in all sampled areas. It is a predominantly frugivores species and forages mainly in the canopy of riparian forests (Marini, 1992Marini, M.A. 1992. Foraging behavior and diet of the Helmeted Manakin. The Condor, 94: 151-158.). In addition to being considered a rare species in the state of São Paulo (Donatelli et al., 2004Donatelli, R.J.; Costa, T.V.V. & Ferreira, C.D. 2004. Dinâmica da avifauna em fragmentos de mata na Fazenda Rio Claro, Lençóis Paulista, São Paulo, Brasil. Revista Brasileira de Zoologia, 21: 97-114.) and included in the Near Threatened category in the state (Bressan et al., 2009Bressan, P.M.; Kierulff, M.C.M. & Sugieda, A.M. 2009. Fauna ameaçada de extinção no Estado de São Paulo: Vertebrados. São Paulo, Fundação Parque Zoológico de São Paulo. 645p.), it was also classified as a rare for the study region of the present study according to its FO (14%).

Although most species that occur in the Cerrado depend on forest habitats for reproduction, the majority of migratory species are considered to be independent of these environments. Indeed, according to Silva (1995Silva, J.M.C. 1995a. Birds of the Cerrado region, South America. Steenstrupia, 21: 69-92.a), 88% of the septentrional migrants and 67% of the austral migrants already recorded in the Cerrado do not depend on forest habitats. The data obtained in the present study corroborate this assertion, since 66% of the migratory species recorded were classified as independent of forest habitat. Other authors have affirmed that migratory species, independent of trophic guild, preferentially exploit open areas for breeding and foraging (Alves, 2007Alves, M.A.S. 2007. Sistemas de migrações de aves em ambientes terrestres no Brasil: exemplos, lacunas e propostas para o avanço do conhecimento. Revista Brasileira de Ornitologia, 15(2): 231-238.; Robertson et al., 2013Robertson, B.A.; Landis, D.A.; Sillett, T.S.; Loomis, E.R. & Rice, R.A. 2013. Perennial agroenergy feedstocks as en route habitat for spring migratory birds. BioEnergy research, 6(1): 311-320.).

The Blue-tufted Starthroat (Heliomaster furcifer), recorded only once in the present study (a male with post-nuptial plumage), in the municipality of Igarapava, state of São Paulo, appears to be a low-density species, with few records in the literature (Macarrão et al., 2011Macarrão, A.; Nunes-de-Almeida, C.H.L. & Corbo, M.C. 2011. Primeiros registros de Heliomaster furcifer (Trochilidae) no estado de São Paulo e ampliação de sua distribuição. Revista Brasileira de Ornitologia, 19(3): 422-423.). The first documented record of these species in São Paulo occurred only in 2010, in a rural environment of the municipality of Brotas (Macarrão et al., 2011Macarrão, A.; Nunes-de-Almeida, C.H.L. & Corbo, M.C. 2011. Primeiros registros de Heliomaster furcifer (Trochilidae) no estado de São Paulo e ampliação de sua distribuição. Revista Brasileira de Ornitologia, 19(3): 422-423.). According to these author, H. furcifer appears in São Paulo during his migratory movements, which probably occur during the dry season, suggesting that these species may occur as a winter migrant in the southeastern region of Brazil (Mazzoni & Perillo, 2014Mazzoni, L.G. & Perillo, A. 2014. The wintering distribution of the Blue-tufted Starthroat Heliomaster furcifer (Apodiformes: Trochilidae) in Minas Gerais, and its association with Pyrostegia venusta (Bignoniaceae). Atualidades Ornitológicas, 180: 7-9.). Thus, the record made in the present study, on July 28, 2013, coincides with this period of occurrence described in the literature.

Three of the septentrional migrant species (Tringa solitaria, Hirundo rustica, and Petrochelidon pyrrhonota) were observed only in the rainy season, which corresponds to winter in the Northern Hemisphere. This pattern of occurrence is consistent with that described in the literature (Sick, 1997Sick, H. 1997. Ornitologia brasileira. Rio de Janeiro, Ed. Nova Fronteira. 912p.). The Cliff Swallow (P. pyrrhonota) was observed forming extremely large flocks of more than 150 individuals when foraging through the aerial stratum. The Barn Swallow (H. rustica) was also observed in very numerous groups, but less numerous than the Cliff Swallow. The Solitary Sandpiper (T. solitaria) was recorded only once in November 2013 when two individuals foraged in the midst of swamp vegetation within the sampled area.

The only septentrional migrant recorded during all months of the study, and thus in both in the dry and rainy seasons, was the Osprey (P. haliaetus). This rapinant species, which feeds almost exclusively on fish (Mestre & Bierregaard-Jr., 2009Mestre, L.A.M. & Bierregaard-Jr., R.O. 2009. The role of Amazonian rivers for wintering ospreys (Pandion haliaetus): clues from North American band recoveries in Brazil between 1937 and 2006. Studies on Neotropical Fauna and Environment, 44(3): 141-147.), is most frequently recorded at the end and the beginning of each year in its wintering places, but can be seen during any season in Brazil, with records existing for every month of the year (Sick, 1997Sick, H. 1997. Ornitologia brasileira. Rio de Janeiro, Ed. Nova Fronteira. 912p.).

It is also important to highlight the record of the Greater Rhea (Rhea americana), observed on three occasions only in the municipality of Igarapava, São Paulo: on November 13, 2013, an adult was observed when foraging in the middle of sugarcane monoculture accompanied by eight immature individuals. In January 2014, this family group was recorded again, being possible to notice the development of the immatures. Habitat destruction and fragmentation, hunting, pesticide contamination and few localities with recent records of the species in the state justify their inclusion in the threatened species list of São Paulo as a critically endangered species (Bressan et al., 2009Bressan, P.M.; Kierulff, M.C.M. & Sugieda, A.M. 2009. Fauna ameaçada de extinção no Estado de São Paulo: Vertebrados. São Paulo, Fundação Parque Zoológico de São Paulo. 645p.). Thus, the records made in the present study are important because they provide data about its occurrence (with evidence of reproduction) in a new locality in the state of São Paulo.

CONCLUSION

According to Drummond et al. (2005Drummond, G.M.; Martins, C.S. Machado, A.B.M; Sebaio, F.A. & Antonini, Y. 2005. Biodiversidade em Minas Gerais: um Atlas para sua conservação. 2.ed. Belo Horizonte, Fundação Biodiversitas. 220p.), the region of the lower Grande River is currently considered as of “High Biological Importance” for bird conservation in the state of Minas Gerais because it has a high number of threatened species. The results of the present study corroborate this statement since a great number of endangered species were recorded in the sampled areas, at least locally (in the State level). The main cause of decline for all threatened species is habitat destruction, mining, dam’s constructions and agricultural activities (Drummond et al., 2005Drummond, G.M.; Martins, C.S. Machado, A.B.M; Sebaio, F.A. & Antonini, Y. 2005. Biodiversidade em Minas Gerais: um Atlas para sua conservação. 2.ed. Belo Horizonte, Fundação Biodiversitas. 220p.; Faria et al., 2008Faria, L.C.P.; Carrara, L.A. & Rodrigues, M. 2008. Biologia reprodutiva do fura-barreira Hylocryptus rectirostris (Aves: Furnariidae). Revista Brasileira de Zoologia, 25(2): 172-181.; Bressan et al., 2009Bressan, P.M.; Kierulff, M.C.M. & Sugieda, A.M. 2009. Fauna ameaçada de extinção no Estado de São Paulo: Vertebrados. São Paulo, Fundação Parque Zoológico de São Paulo. 645p.). Additional research, with bird inventories, adequate management plans and public policies aimed at conserving habitats, with the creation of conservation units, are needed for more effective conservation of local biodiversity (Drummond et al., 2005Drummond, G.M.; Martins, C.S. Machado, A.B.M; Sebaio, F.A. & Antonini, Y. 2005. Biodiversidade em Minas Gerais: um Atlas para sua conservação. 2.ed. Belo Horizonte, Fundação Biodiversitas. 220p.).

ACKNOWLEDGMENTS

The authors would like to thank Companhia Energética de Minas Gerais (CEMIG) and Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG) for financial (grants CRAAPQ03055-2011), logistic and technical support. Thanks also go to the staff of Volta Grande Reservoir for logistical support.

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Edited by

Edited by: Luís Fábio Silveira

Publication Dates

  • Publication in this collection
    12 Aug 2020
  • Date of issue
    2020

History

  • Received
    22 Feb 2019
  • Accepted
    20 Apr 2020
  • Published
    08 June 2020
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