Diversity of birds in the Mata do Junco State Wildlife Refuge , a remnant of the Atlantic Forest of Northeastern Brazil

This study presents an inventory of the bird fauna of the Mata do Junco State Wildlife Refuge in Capela, in the northeastern Brazilian state of Sergipe. Monthly samples were collected between January 2011 and May 2012. Each 3-day sample was based on mistnetting (100 m) in two areas and the compilation of MacKinnon lists of 10 species. During the 17 months of the study period, the occurrence of 129 bird species belonging to 41 families was confirmed for the study area. In the mist-nets, a total of 469 individuals representing 58 species were captured in 3400 net-hours of sampling effort. A total of 100 MacKinnon lists were compiled, resulting in an inventory of 119 bird species. Eight of the species are endemic to Brazil, of which, five are restricted to the Brazilian Atlantic Forest. Three of the species are included in the IUCN Red List, at different levels of concern. Overall, the results of the study indicate that the Mata do Junco represents an important area for the protection of the region’s avian fauna and the habitats they rely on.


INTRODUCTION
The Brazilian Atlantic Forest is one of the world's 34 conservation hotspots (Conservation International 2012), which together account for more than 60% of the terrestrial species found on the planet (Lagos and Muller 2007).The northern extreme of the Atlantic Forest in the Brazilian Northeast originally covered an area of 255,245 km 2 , or almost 29% of its original extension, but in 2006 this had been reduced to only 19,427 km 2 (Tabarelli et al. 2006).The remnants of the original forest are distributed in relatively small fragments surrounded by agricultural matrix composed primarily of sugar cane plantations (Pereira and Alves 2006).
At least 400 fragments of Atlantic Forest can be found in the Brazilian state of Sergipe, covering a total area of approximately 36,000 ha, representing around 7% of the original forest cover of the state (Santos et al. 2013).The vast majority of these fragments are relatively small (20-450 ha), although there is one much larger fragment, of 1,000 ha, in the south of the state.
The creation of protected areas represents an important strategy for the conservation of natural resources, and in the state of Sergipe, a total of 19 reserves has been established by federal, state, and municipal governments.However, surveys of the avian fauna are available for only three of these areas (D'Horta et al. 2005;Ruiz-Esparza et al. 2011;Lyra-Neves et al. 2012).In 2007, the state government decreed the Mata do Junco Wildlife Refuge in the municipality of Capela, with the primary objective of protecting the local populations of endangered species endemic to the Atlantic Forest of northeastern Brazil, in particular the Coimbra Filho's Titi Monkey (Callicebus coimbrai) and the Fringe-backed Fire-eye (Pyriglena atra).
Almost seven hundred bird species are known to occur in the Atlantic Forest (Cordeiro 2003), of which 124 are endemic (Brooks et al. 1999), and 83 endangered (Olmos 2005).The care with possible future extinctions and maintaining the integrity and biological dynamics of ecosystems depends on scientific information about threatened species (Bencke et al. 2006) and species inventories (Farias et al. 2009).Here we present a bird inventory of Mata do Junco State Wildlife Refuge, Sergipe, within in the Atlantic Forest biome, and discuss the conservation importance of its avifauna.

LISTS OF SPECIES
characterized by a rainy season in the austral winter and a dry season in the summer (Köppen 1936).Mean temperatures are above 18°C, with maxima of between 21°C and 38°C and minima of 18-22.2°C(SEPLANTEC/ SRH 2009).The study area is based on rocks of the Cretaceous Riachuelo group of the Barreiras formation, with Holocene alluvial deposits at the surface (SEMARH 2011).

Data collection
Data were collected using two complementary approaches -mist-netting and MacKinnon lists.Ten 10 m × 2.5 m mist-nets were set in line along trails in two in the state of Sergipe, Brazil (Figure 1).The refuge has a total area of approximately 900 ha, and is located within the basin of the Japaratuba River, which flows into the Atlantic.The vegetation is typical plateau Atlantic rainforest, with some areas of laterized soil, on which a more open type of vegetation is found, dominated by sclerophyllous shrubs.Natural clearings are characterized by the presence of pioneer trees, such as Cecropia spp., Tapirira guianensis, and Sclerolobium paniculata, which are typical of different stages of regeneration (SEMARH 2011).
The inventory of species was complemented with MacKinnon lists (MacKinnon and Phillips 1993), which are based on standardized surveys of the principal trails within the refuge, using 8 × 40 binoculars and a field identification guide (Sigrist 2007).During each survey, the observer recorded the first ten species encountered, which constitute one MacKinnon list (Ribon 2010).Five MacKinnon lists (10 species) were collected each month, with an overall total of 100 lists being recorded during the study period.Nomenclature follows the Brazilian Committee of Ornithological Records (CBRO, 2014).
Sampling effort for mist-netting totaled 3400 nethours (12 m of net = 1 net-hour) over the 17 months of fieldwork, which resulted in the capture of 469 specimens (49 of which were recaptured) belonging to 58 species.The Jackknife 1 analysis estimated a total of 82 bird species for the study area, 24 more than the actual number captured in the mist-nets (Figure 3).
Five MacKinnon lists were collected each month, with an overall total of 100 lists being recorded during the study period.A total of 119 species were recorded in these lists, although the Jackknife 1 analysis estimated a total of 149 species for the study area (Figure 4).The most common species recorded in the MacKinnon lists were Chiroxiphia pareola, Manacus manacus, Vireo chivi, Columbina talpacoti, Arremon taciturnus and Stelgidopteryx ruficollis, which together contributed just over one-quarter (26.3%) of the individual records (n = 1632).
Eight of the species recorded in the present study are endemic to Brazil (Appendix 1), of which five-Pyriglena atra, Hemitriccus nidipendulus, Ramphocelus bresilius, Hylophilus poicilotis and Thalurania glaucopis-are endemic to the Brazilian Atlantic Forest (Brooks et al. 1999).Three of the species are red-listed by the IUCN (2013).Thalurania watertonii is listed as Near-Threatened, Herpsilochmus pectoralis as Vulnerable and Pyriglena atra  (Figure 5) as Endangered.
Based on the classification of Stotz et al. (1999), 48 of the species recorded in the present study can be characterized as specialists or indicators of specific types of habitat.Three of the species (Herpsilochmus pectoralis (Figure 6A, B), Picumnus pygmaeus (Figure 6C) and Formicivora melanogaster) can be considered to be specialized for the occupation of deciduous tropical forests, and are endemic to central South America.
Two Nearctic migrants-Egretta thula and Falco sparverius-breed in the Neotropics.Buteo albonotatus is a partial Nearctic migrant.

DISCUSSION
Over the course of the present study, a total of 129 bird species were recorded in the RVS Mata do Junco, representing the first systematic survey of birds of the Atlantic Forest for Sergipe.Eight of the species are endemic to Brazil, of which, five are restricted to the Brazilian Atlantic Forest.Three of the species are included in the IUCN Red List, at different levels of concern and 22 of the species recorded are classified as full or partial migrants by Stotz et al. (1996).
Five endemic species were recorded occasionally during the study.Anopetia gounellei was captured in October, 2011, for example, whereas Ramphocelus bresilius was observed between March and May, and Thalurania watertonii was seen on two occasions, in March 2011 and January 2012.Picumnus pygmaeus was observed in March 2011, and a specimen was captured in June 2011, while Hemitriccus nidipendulus was captured in February 2011, and observed in June 2011 and April 2012.
Other species were recorded more frequently.For example, while only two specimens of Herpsilochmus pectoralis were captured, in June 2011, the species was observed and heard throughout the year.Thamnophilus pelzelni was also present throughout the year, and 16 specimens were captured.Pyriglena atra was observed and heard during the 10 months between April and January, and six males and two females were captured, with brood patches being found in both sexes in November, February, April, and May.While Lima and Neto (2007) reported that the breeding season of this species began at the end of October, it lasted only until March, two months earlier than the evidence found in the present study.
While the Brazilian Atlantic Forest has a unique biota, with many endemic genera and species (Myers et al. 2000), the present study recorded species endemic to the Caatinga and other open formations, such as Picumnus pygmaeus, Anopetia gounellei, and Herpsilochmus pectoralis.This may be related to the geographic position of the Mata do Junco State Wildlife Refuge, which, while representative of the Atlantic Forest, is located marginally within the Atlantic Forest-Caatinga ecotone.
The results of the present study indicate that the MacKinnon lists are a relatively effective approach for the inventory of birds in comparison with mist-netting, although each method has its specific advantages.In particular, the MacKinnon lists provide data on canopydwelling species that are rarely or never captured in mist-nets.Thus, 71 of the species recorded in the MacKinnon lists were not captured in the mist-nets, while 11 of the species collected in the nets were not observed during the observation-based surveys (Appendix 1).
Together with the species recorded in the present study, this would bring the total number of bird species known to occur in this protected area to 127.The management plan published for this conservation unit (SEMARH 2011) refers to a further 37 bird species not recorded in either study that may potentially occur in the area (unpublished data), although it is unclear which of these taxa may actually occur in the refuge.
Overall, then, the available evidence indicates that at The presence of a diverse avian fauna at Mata do Junco, which includes three rare or threatened species, represents an important resource for the conservation of the region's biota, given the decimation of local ecosystems in recent decades.More information on the status of these populations and their ecological relationships will be required, however, to develop adequate management strategies over the long term.

Figure 1 .
Figure 1.Location of the Mata do Junco State Wildlife Refuge in Capela, Sergipe (Brazil).

Figure 2 .
Figure 2. Location of the mist-nets in the open forest habitat at the RVS Mata do Junco.

Figure 3 .
Figure 3. Sample rarefaction (Mao tau) of the observed species richness and expected richness estimated by Jackknife 1 for the bird species captured in mist-nets (January 2011-May 2012) at the Mata do Junco State Wildlife Refuge in Sergipe, Brazil.

Figure 4 .
Figure 4. Sample rarefaction (Mao tau) and expected species richness estimated by Jackknife 1 for the bird species recorded in the MacKinnon lists at the Mata do Junco State Wildlife Refuge in Sergipe, Brazil.Each sample corresponds to five lists.

Figure 6 .
Figure 6.Specialist species captured in the mist-nets at the Mata do Junco State Wildlife Refuge, Sergipe, Brazil: a) and b) pair of Pectoral Antwren (Herpsilochmus pectoralis) and c) Spotted Piculet (Picumnus pygmaeus).

Figure 5 .
Figure 5. Pair of Fringe-backed Fire-eye (Pyriglena atra) captured in the mist-nets at the Mata do Junco State Wildlife Refuge in Sergipe, Brazil.
Ruiz-Esparza et al. | Bird inventory at Mata do Junco State Wildlife Refuge northeastern Brazil least 127 bird species, and possibly as many as 164, occur in the Mata the do Junco State Wildlife Refuge.This total is comparable with that recorded (123) at the Serra de Itabaiana National Park in central Sergipe by D'Horta et al. (2005), located within an Atlantic Forest transition zone, but slightly lower than the 140 species recorded in the Grota do Angico Natural Monument in the Caatinga scrub of northern Sergipe by Ruiz-Esparza et al. (2011).
Ruiz-Esparza et al. | Bird inventory at Mata do Junco State Wildlife Refuge northeastern Brazil APPENDIX 1. Bird species recorded at RVS Mata do Junco, Sergipe, during the present study.The classification and nomenclature follows the Brazilian Committee for Ornithological Records (CBRO 2014).Type of record: O = observation; C = specimen collected in mist-nets.Continued versity of Chicago Press.502 pp.Tabarelli, M., J.A. Siqueira Filho and A.M.M. Santos.2006.A floresta Atlântica ao norte do Rio São Francisco.pp.21-35, in: K.C. Pôrto, J.A. Cortez and M. Tabarelli (eds.).Diversidade biológica e conservação da floresta Atlântica ao norte do Rio São Francisco.Brasília: Ministério do Meio Ambiente, Coleção Biodiversidade.JR, CS and MA collected the data, JR, PR and SF wrote the text, and DR, PA and RB made the analysis.Darius Tubellis, Thiago V. V. da Costa Ruiz-Esparza et al. | Bird inventory at Mata do Junco State Wildlife Refuge northeastern Brazil