Birds of the Arvoredo Marine Biological Reserve , southern Brazil

The Arvoredo Marine Biological Reserve (RBMA) is a protected area in southern Brazil created in 1990 to safeguard the marine biodiversity of the Arvoredo Archipelago. There are only few studies about bird assemblage in most of the Brazilian coastal islands, including this protected area. Therefore, this paper presents the first complete list of birds for RBMA based on data from literature and surveys between 1986 and 2012 on islands and surrounding waters. Birds were recorded during captures using mist-nets and opportunistic observations on land in January 2012, as well as in monthly strip-transects and sectors on sea between 2010 and 2012. The present list includes 84 species (15 captured) from primary data and 22 species from other sources, totaling 106 species from 37 families. Bird assemblage in the RBMA is composed by 44 aquatic birds and 62 landbirds, whereas 13 are endemic to the Atlantic Forest and 12 are threatened. As expected due to the diversity of habitats, Arvoredo and Galé Islands supported the richest assemblages in the RBMA. The number of species in the whole RBMA is smaller than bigger islands elsewhere in the Atlantic Forest domain, but similar to same-sized and same-habitat ones. Our results highlight the importance of this reserve as a suitable and isolated habitat to forest species. Deserta Island is an important site for nesting, resting, and foraging seabirds.


INTRODUCTION
The Arvoredo Marine Biological Reserve (RBMA) is a protected area in southern Brazil created in 1990 to safeguard the marine biodiversity of the Arvoredo Archipelago.This reserve plays an important role as a resting and breeding site for seabirds (Branco 2003a(Branco , 2004;;Vooren and Brusque 1999;Efe et al. 2000;Branco 2004).Also, it has suitable habitats for terrestrial species since two of the islands are covered by a well-preserved Atlantic Forest (Salvador et al. 2009).
In recent decades, the number of studies on seabirds at the RBMA and adjacent coastline has increased substantially (Bege and Pauli 1988;Schiefler and Soares 1994;Soares and Schiefler 1995;Efe et al. 2000;Branco 2000;Branco and Ebert 2002;Branco 2003aBranco , 2003bBranco , 2004;;Branco et al. 2004;Branco and Fracasso 2005;Branco et al. 2005;Neves et al. 2006;Branco et al. 2007;Ebert and Branco 2009;Prellvitz et al. 2009;Branco et al. 2010a;Cremer and Grose 2010;Hogan et al. 2010).Nevertheless, there still are few studies on landbird assemblage in islands at this region (Bege and Pauli 1988;Graipel et al. 1997;Ghizoni et al. 2013).The available data is insufficient to support management decisions in the RBMA.Therefore, we present a complete list of marine and terrestrial birds of Arvoredo Marine Biological Reserve, discussing aspects of richness, composition, and threatened or endemic species.

Study area
The RBMA is located in the state of Santa Catarina, southern Brazil, about 10 km from mainland.It comprises 17,600 ha and includes São Pedro Rock, Arvoredo, Galé, and Deserta islands, and the surrounding sea (Figure 1).Arvoredo Island (27°17′ S, 048°21′ W) has 270 ha of Atlantic Forest in different sucessional stages surrounded by cliffs 1-20 m high.Deserta Island (27°16′ S, 048°19′ W) has almost 20 ha of herbaceous and shrubs also bordered by high rocky cliffs.Galé Island (27°10′ S, 048°24′ W) has 160 ha of herbaceous, shrubs, and trees.Galés Island also has two rocky islets northeastern to it.Lastly, São Pedro Rock has 2 ha (27°15′ S, 048°25′ W) with only a few herbaceous cover on the top.

Data Collection
Records were obtained from literature review, birds deposited at Coleção Científica de Aves da Universidade Federal de Santa Catarina, ad libitum searches, strip-transects with boats, and captures with mist-nets.Literature review considered studies performed within the RBMA geographical limits (27°09′ S, 048°25′ W and 27°17′ S, 048°22′ W, see details in Brazilian Federal Decree 99,142/1990), except for seabirds, which included records made over a wider area (27° S, 048° W and 28° S, 049° W, see Rosário 1996).Sectors with continuous census (following Branco et al. 2010b) were performed monthly between May 2010 and March 2012 with a boat cruising at 10 knots around each island.Strip-transects were performed following Camphuysen et al. (2004) at the same day as the census by sectors, but recorded in Bege and Pauli (1988) within the geographical limits established to seabirds in this study, but it was not included due to its vagrancy.The number of species found only in one literature, without subsequent records, may indicate that around 14% of the species are represented by accidentals.Nevertheless, we cannot rule out this may be a bias of the different methods and efforts used by us.Long-term systematic samplings are recommended to confidentially stablish the occurrence status of these species in the RBMA.
Sixty-two species are landbirds occurring in open areas, shrubs or forest (Table 1).Almost half of them were found in at least two different environments.Fortytwo species were record in forests and 50% of them were exclusive to this habitat.From the 44 aquatic birds, three were migratory shorebirds and 32 were seabirds.The coastline was also used by terrestrial species (Table 1), such as Pitangus sulphuratus (Linnaeus, 1766) and Athene cunicularia (Molina, 1782).
Arvoredo and Galé were the most species-rich islands, with 70 and 44 species respectively (Table 1).Both islands have more habitat heterogeneity, from rock cliffs to Atlantic Forest.Data from the Arvoredo Island included 34 species not found in the Galé Island (Table 1).We suppose that real richness of both islands can be higher, since Galé was surveyed only by boat along the shoreline and Arvoredo still needs further efforts in higher forested areas.Deserta Island and São Pedro Rock had 23 and 11 species respectively, probably due to their rocky characteristics, small size, and herbaceous vegetation.Deserta Island has low habitat diversity and its exposure to winds and waves prevents the establishment of terrestrial birds.Nevertheless, Deserta Island plays an important role as a breeding site to Sternidae, Laridae, and Sulidae (Efe et al. 2000;Branco 2003aBranco , 2003b;;Prellvitz et al. 2009;Hogan et al. 2010).
Total of species in the whole RBMA is smaller than in larger islands elsewhere in the Atlantic Forest domain, cruising at 20 knots along each of the four routes between islands.Atlantic Forest endemic status follows Bencke et al. (2006).
Among the endemics, Tangara peruviana is globally and nationally Vulnerable and Endangered at regional level due to habitat loss (CONSEMA 2011;ICMBio 2014;IUCN 2014) 2,3,8,11,12,UFSC (244,245,) 5,8,11,12,UFSC (269,278)  they are respectively Vulnerable and Endangered at global and regional levels.Most of these and other pelagic species have irregular occurrence along most of the Brazilian inshore.All of them seem to use the RBMA to rest and feed while migrating.

Noteworthy records
Some interesting records during surveys are highlighted for the Arvoredo Marine Biological Reserve: Crypturellus obsoletus: One individual briefly vocalized at Saco do Capim on the evening of 16 January 2012.This species is endemic to the Atlantic Forest.Future studies on this species in the RBMA may clarify about the existence of an isolated population, vagrancy or recent colonization patterns.
Puffinus puffinus (Brünnich, 1764): Five individuals swimming between Deserta and Galé Islands on 21 November 2010 and one near the Arvoredo Island on 14 December 2011.This last one was oil-stained on the chest, but with no sign of illness (Figure 3D).The species had been recorded dead in beaches along the Santa Catarina Island (Naka and Rodrigues 2000) and near the mainland (Rosário 1996).
Calidris canutus: A migratory flock with 78 shorebirds resting at the São Pedro Rock was recorded on 30 March 2012 (Figure 3A).Seven individuals had green flags banded in the USA in 2004.They were reported to CEMAVE and the USA Banding and Resightings Project.This species is Critically Endangered in national level (ICMBio 2014).

CONCLUSION
Reviewing published and grey literature as complementary data is an important step to produce checklists (Vieira et al. 2014).Findings from literature contributed with many important records of threatened species in the RBMA.Even if these species are rare and went unrecorded during our field work, their presence could suggest the need of new adaptive management to attend their priorities in the RBMA.However, records from literature must not stand alone and long-term monitoring is important to evaluate the presence of those species and habitat use, as well as the efficiency of the management.
Deserta Island is an important breeding site to Larus dominicanus, Sula leucogaster, Sterna hirundinacea, and Thalasseus acuflavidus (Efe et al. 2000;Branco 2003aBranco , 2003b;;Prellvitz et al. 2009;Hogan et al. 2010).In this context, Myers et al. (1987) point out that breeding efficiency depends on conditions such as abundant food and safety, which is also related to isolation from human disturbances.Only a few places in the state of Santa Catarina support the breeding of migratory species as does the Deserta Island.
Further systematic efforts on terrestrial species are still needed, mainly in Galé and Arvoredo islands.RBMA holds a significant percentage of the marine bird richness of Santa Catarina coastline.The Arvoredo Archipelago is a natural biogeography experiment isolating terrestrial populations from the mainland since the sea-level rose in the quaternary period (Angulo et al. 2006).Further studies on terrestrial endemics can provide insights on speciation processes and long-term population viability of isolated areas.
occurred from 16-18 January 2012 at Saco do Capim (27°17′30″ S, 048°21′56″ W, 70 m elevation), Arvoredo Island, totaling 7,290 h•m² effort.Ad libitum observations occurred from boats during the intervals of strip-transects or by walking through southern and western sides of the Arvoredo Island (up to 100 m above sea level) during the intervals of mist-netting.Systematic classification and names follow the Brazilian Ornithological Records Committee (CBRO 2014).Species were classified according to habitat and location where they were recorded in the RBMA.Conservation status follows CONSEMA (2011), ICMBio (2014), and IUCN (2014).
Graipel etGhizoni et al. 2013)to same-size and same-habitat ones.Arvoredo Archipelago is richer than other archipelagos throughout the Santa Catarina coastline, such as Itacolomis (17 species; Branco 2004), Tamboretes (15 species;Branco 2004)or Moleques do Sul (31 species;Bege and Pauli 1988).These islands only have herbaceous or shrubs while Arvoredo Archipelago has two islands with developed Atlantic Forest.Relation between richness and forest development is reinforced when comparing Arvoredo Island (67 spp.) to Ratones Grande Island (51 spp.;Graipel et al. 1997).On the other hand, the bird richness in RBMA is lower than in larger islands with more habitats, such as Santa Catarina Island(352 spp.;Ghizoni et al. 2013), Ilha Grande in the state of Rio de Janeiro (222 spp.; Alves and Vecchi 2009) or São Sebastião Island in the state of São Paulo (207 spp.; . The shorebird Calidris canutus(Linnaeus, 1758)is Critically Endangered at national level.Ten seabirds listed in this study are also threatened (Table1).Diomedea epomophora and Procellaria aequinoctialis are Vulnerable and Thalassarche chlororhynchos (Gmelin, 1789) and Pterodroma incerta are Endangered at all levels.Diomedea dabbenena is Critically Endangered at all levels while Diomedea exulans is Critically Endangered at national level but Vulnerable at global and regional levels.Thalasseus maximus (Boddaert, 1783) is Endangered at national level and Vulnerable at global and regional levels Thalassarche chrysostoma and Thalassarche melanophris(Temminck, 1828)are not listed in Brazilian Red List but