Birds of Estação Ecológica de Carijós , southern Brazil

Estacao Ecologica de Carijos , southern Brazil, was created to protect biodiversity found in mangrove areas, restingas , and swamps of Santa Catarina Island. This paper presents an updated bird list of this protected area based on different surveying methods between 2009 and 2012. Thirty new species were recorded to Estacao Ecologica de Carijos . Among 227 species known to occur in the area, 6 are threatened and 5 are highly dependent on mangrove areas or restingas . Study area has great importance, once it holds 64% of all bird species recorded in Santa Catarina Island, and 32% of those found in the state of Santa Catarina. High richness that was observed can be due to complex mosaic of natural habitats. Results show this protected area should be expanded to include not only nearby areas of restinga, but also the marine portion of Ratones Bay.


Introduction
Importance of coastal environments to regional biodiversity has been neglected despite these areas often exhibiting high levels of habitat heterogeneity and harboring habitat specialists (Rocha et al. 2007).In Brazil, these habitats began to be more valued for conservation purposes when endemic species, such as Stymphalornis acutirostris Bornschein, Reinert &Teixeira, 1995 andFormicivora littoralis Gonzaga &Pacheco, 1990 became globally threatened due to habitat loss (IUCN 2013).Fauna along Santa Catarina's coastline in southern Brazil remains understudied.Yet, it can potentially hold a significant and diverse bird assemblage due to its vast plains of unique vegetation.Region shelters the largest areas of restinga habitat in Brazil (Falkenberg 1999).Restinga is a coastal moist broadleaf forest formed on sandy, acidic, and nutrient-poor soils and characterized by medium sized trees and shrubs (Falkenberg 1999).Region also represents the southernmost mangroves along the Atlantic coast in South America (Chapman 1977;Spalding et al. 1997).Following a Brazilian trend, Santa Catarina coastal zone is under severe threat due to new settlements, invasions of exotic species, selective removal of species of economic importance, predatory fishing, and mining (MMA 2003;Rocha et al. 2007).
Estação Ecológica de Carijós is a protected area created to conserve the diversity found in mangrove areas, restingas, and swamps of Santa Catarina Island.Avifauna of this area has been sampled by Efe et al. (2007).However, many researchers have surveyed this area in recent years and gathered new unpublished data.Thus, this paper presents an updated bird list of Estação Ecológica de Carijós with new records to this protected area, including an update of birds conservation status.
Our sampling places (Figure 1) were ad libitum searched between September 2005 and September 2012 with around 100 fieldtrips.In addition, three point counts with a 300-m radius were performed during 1 h each at Pontal de Jurerê.Survey was carried out monthly from sunrise to sunset between August 2011 and October 2012.Mist-netting was used to sample avian assemblages at Fazenda Brinkas, the Station's headquarters, Antiga Estrada da Daniela, Restinga do Olandi, and Restinga de Ratones.Individuals were banded (permits SISBIO number 23678-1 and CEMAVE/IBAMA nunber 3272) in monthly samplings between November 2010 and March 2012.Mist-nets were opened before sunset for three consecutive days at each site, totaling 38,880 h•m² efforts (Straube and Bianconi 2002).
Birds were identified with the help of field guides and manuals, such as van Perlo (2009), Rosário (1996), and Sick (1997).Some photographs and voice recordings taken from the area were deposited in Wikiaves website (www.wikiaves.com)or Xeno-Canto website (www.xeno-canto.org).Scientific and common names, and systematic classification follow the Brazilian Committee of Ornithological Records (CBRO 2014), except for the treatment of their expanded Lanio; we instead follow Remsen et al. (2013) for those species.Conservation status of species was accessed at the state (CONSEMA 2011), national (MMA 2003), and global level (IUCN 2013).
Thirty species were added to the list from our own fieldwork (Table 1).We mist-netted and banded 185 individuals belonging to 33 species (Table 1).Coryphospingus cucullatus (Müller, 1776) was the only new species recorded exclusively by this method (Figure 2).We further recorded 115 species using point counts, with the highest number of species detected in aquatic habitats.Ad libitum searches detected 176 species.During point counts and ad libitum searches we recorded 168 species by visual contact and 104 by vocal signals (Table 1).Use of complementary surveying methods allowed improving site's check-list (Bibby et al. 2000).Previous surveys at this area resulted in 148 spp.(Efe et al. 2007).
Other bird studies along Brazilian coastline focused on inventorying the avifauna in restingas, mangrove  areas, beaches, swamps, and mudflats.Almeida and Barbieri (2008) found 46 species in mangrove areas in northeastern Brazil, while Mestre et al. (2007) listed 81 species in Paraná.Almeida et al. (2013) and Mota et al. (2012) listed respectively 136 and 96 bird species to restinga habitat in northeastern Brazil, and their species richness is similar to other protected (146 spp.;Simon et al. 2007) and not protected (87 spp.; Dario 2009) restingas in Espírito Santo.Southern Brazil has few studies on coastal bird assemblages, but Piacentini and Campbell-Thompson (2006) listed 117 species in different habitats (mostly affected by human presence) at the Lagoa de Ibiraquera basin, in Imbituba.
Good part of the regional biodiversity can be found in ESEC Carijós.Sixty-four percent of bird species historically recorded in the Santa Catarina Island (ca. 355;Ghizoni-Jr. et al. 2013) have been found in our study area.In addition, bird assemblage represents about 32% of the species known to occur in the Santa Catarina state (ca.700; VQP unp.data).Despite many new species added to ESEC Carijós, sampling effort was spatially unequal, with Manguezal do Saco Grande still in need of more intensive and longer-term surveys.There is a need also of studies focusing on nocturnal species, as well as swamp specialists (e.g., Rallidae and some Passeriformes).

Unconfirmed and questioned species
Three species have been reported to ESEC Carijós but were not validated in our review.Additionally, one species could not be identified to species level: Flamingo (Phoenicopteridae): at an unspecified date, L.O.F.Rocha (pers. comm.)saw flamingos near the Station's headquarters, but the birds could not be identified.Ghizoni-Jr.and Piacentini (2010) suggested that Phoenicoparrus andinus (Philippi, 1854) might use the Pontal de Jurerê.But in fact, Coroa do Bicudo is a very likely place to be visited by flamingos given its habitat.
Buteo nitidus (Latham, 1790): Though cited in Efe et al. (2007) to ESEC Carijós and in Naka et al. (2000) to Santa Catarina Island, this hawk has no confident records in southern Brazil.Closest known population of this species is in northern São Paulo state, around 700 km of Santa Catarina (Sick 1997;Ferguson-Less and Christie 2001).We therefore believe that this record should be left as hypothetical until physical evidence becomes available.Given the presence of some gray-backed and/or lightplumaged individuals of Rupornis magnirostris (Gmelin, 1788) in Santa Catarina (e.g., records WA412005 -Niehues 2011; WA431470 -Florencio 2011; and WA880322 -Andrade 2013), confusion with the latter species is likely (VQP pers.obs.).
Sporophila frontalis (Verreaux, 1869): cited by Efe et al. (2007) to ESEC Carijós based on a pair of buff Sporophila seedeaters with facial markings seen in a restinga area by a roadside (M.A.G.Azevedo in litt.).The habitat where the record was made differs strikingly from the bamboo patches within forested areas where S. frontalis is found (see Areta et al. 2013).Indeed, there seems to be no suitable habitat to this species at ESEC Carijós, so we have chosen to exclude it from the list until physical evidence for its presence in the area becomes eventually available.
Spheniscus magellanicus (Forster, 1781): one adult and two juveniles were observed swimming and foraging in the Ratones Bay on 17 June 2012 (Figure 3C).Carcasses have been sporadically observed along the beach of the Pontal de Jurerê.The species appears in the reserve during the period of winter migration (Rosário 1996;Sick 1997), when it is commonly seen near beach areas.
Elanus leucurus (Vieillot, 1818): One individual was observed flying above Ratones River on 27 January 2012.Naka and Rodrigues (2000) noted that this species is common in the continent, but rare in the Santa Catarina Island, so it is worth mentioning recent records by BPV and DD in Via Expressa Sul on 20 November 2009 and in Beira-Mar Norte Avenue on 25 September 2012.
Pluvialis dominica: This migratory species, which was only recently found in Santa Catarina Island (Rosario 2004), was observed at the Pontal de Jurerê on 3 January 2011 (Figure 4A).The bird foraged along the beach and close to two Tringa melanoleuca (Gmelin, 1789).This species occasionally appears in the region between October and January (BPV pers.obs.).
Pluvialis squatarola: First species record in ESEC Carijós was at the Pontal de Jurerê on 13 November 2010.
On 3 January 2011, another one rested in the intertidal zone together with Calidris alba.In that same year, four individuals were found foraging with Numenius phaeopus (Linnaeus, 1758) on 18 November (Figure 4B).Calidris alba: Rosário (2004) obtained the first record for the Santa Catarina Island.It was initially observed in ESEC Carijós on 10 October 2010 (Figure 3D), using beaches and mudflats between September and January (BPV pers.obs.).In 2012, a few individuals were seen sporadically in April, May, and August (BPV pers.obs.).
Calidris pusilla (Linnaeus, 1766): We recorded the species at Pontal de Jurerê on 29 August 2012 (Figure 3D), representing the first record to Santa Catarina Island (see Ghizoni-Jr. et al. 2013).The species was seen again foraging again at Pontal de Jurerê with two Calidris alba and few C. fuscicollis on 9 and 23 September 2012.
Aphantochroa cirrochloris: On 9 November 2011, one individual was foraging in a feeder at a residence near the mangrove swamp of Pontal de Jurerê.Piacentini et al. (2006) made the first record for the Santa Catarina Island.
Certhiaxis cinnamomeus: This bird is common in restingas, swamps, and mangrove areas around the island (Figure 4E).It was recorded in swamps at Restinga do Olandi and along the Antiga Estrada da Daniela, as well as in the mangroves of Pontal de Jurerê and of the Station's headquarters since 2011.Rosário (2004) first recorded the species in January 2003.
Mimus triurus: Two individuals were observed foraging in shrub-dominated restinga at Antiga Estrada da Daniela on 9 September 2012 (Figure 4F).This migratory species was first documented in the Santa Catarina Island by Ghizoni-Jr. et al. (2013).
Coryphospingus cucullatus: One adult individual was mist-netted, banded (CEMAVE F24918), and released on 12 November 2010 at the Station's headquarters (Figure 2; see Ghizoni-Jr. et al. 2013).It is a recent colonizer in eastern Santa Catarina state, likely through releases and escape as pet birds (VQP pers.obs.).Soares (2004) recorded one individual in the locality of Ribeirão da Ilha,
Threatened species have general reduced population sizes or populations in decline due to habitat loss and resource scarcity (CONSEMA 2011;IUCN 2013).Despite not being a nesting site for birds as S. tyrannus and T. maximus, the study area plays an important role as foraging grounds.According to Ghizoni-Jr. et al. (2013), there have been at least five pairs of S. tyrannus observed using areas in the Santa Catarina Island.At the ESEC Carijós, they are often observed searching for food in tree-dominated restingas (Azevedo et al. 2003;Ghizoni-Jr. et al. 2013).
Thalasseus maximus is present throughout the year, with greater numbers between July and November (BPV pers.obs.), corresponding to breeding period in Uruguay coastline (Lenzi et al. 2010).ESEC Carijós is close enough of Uruguay considering birds' flight capacity.They could fly from one place to another in a few days, once they can move up to 40 km per day to search for food (Del-Hoyo 1996).It is possible that species uses ESEC Carijós region to forage and rest during its breeding season (BPV pers.obs.).
Among forest birds, Ramphocelus bresilius is a species under pressure from illegal capture and trade (IUCN 2013).In 2012, for example, a man was observed with cages and traps at the Antiga Estrada da Daniela.This is the same place where Sporophila caerulescens (Vieillot, 1823) occurs.
Egretta caerulea (Linnaeus, 1758), Nyctanassa violacea (Linnaeus, 1758), R. longirostris, and Conirostrum bicolor are especial due to their strong dependence on mangrove areas.Tangara peruviana also represents an endemic species threatened due to the destruction of the restingas (CONSEMA 2011).Rallus longirostris, as well as C. bicolor and T. peruviana are at regional risk due to the isolation of subpopulations in fragmented and/or polluted habitats (CONSEMA 2011;IUCN 2013).
Population fluctuations, even if they are not significant, have also been globally observed for Spheniscus magellanicus and Puffinus griseus (Gmelin, 1789) likely due to the fishing industry and marine pollution (IUCN 2013).North Bay region, including Ratones Bay, could be a valuable foraging and resting area for these species, due to the low fishing pressure in the area, although it has been suffering from irregular dumping of waste into the sea (Severino et al. 2006;Vieira et al. 2011Vieira et al. , 2012)).Therefore, we recommend to intensify the water quality monitoring in ESEC Carijós and to establish its relationship with avian health.Efe et al. (2007) have recommended special attention to human pressures such as settlements in the restinga habitat at ESEC Carijós and surrounding areas.Expansion of ESEC Carijós throughout buffer zone, in order to include marine area in Ratones Bay and the restingas of Olandi, Brinkas, and Ratones, could restrict human activities and reduce pressure upon this protected area.Our results reinforce the strategic importance of this protected area in the conservation of Atlantic Forest biodiversity.3B)   03, 05, 07, 08, 11; E101567, 568, 570-572, 581-583, 588-591, 593, 594, 607, 610-613, 615-618, 626, 627, 630, 634, 637, 638, 656, 657, 658) Basileuterus
Arenaria interpres: One individual (Figure 4C) in adultintermediate plumage was observed foraging with one C. canutus (Linnaeus, 1758), four C. fuscicollis, and six Charadrius semipalmatus at the Pontal de Jurerê, on 14 November 2012.Five days later, Ghizoni-Jr.et al. (2013) recorded two individuals at the same place.The first documented record for Santa Catarina Island was in 2005 (Ghizoni-Jr.et al. 2013) Numenius phaeopus: One individual recorded at the Pontal de Jurerê on 18 November 2011 (Figure 4D) foraging on polychaetes and Uca spp.close to four Pluvialis squatarola.This is the first record of the species on Santa Catarina Island (see Ghizoni et al. 2013).