Bird diversity and conservation in the southern coast of Santa Catarina state , Brazil

Coastal lagoons and their surrounding habitats often harbour high biodiversity and some of the most threatened ecosystems in the world. However, in the Neotropics the biodiversity is often poorly described, lacking even inventories of species which therefore limits the assessment of threats and the stablishment of efficient conservation measures. We present here lists of bird species recorded at ten sites along the under-studied coastal lagoons of southern Santa Catarina, Brazil, collected mainly from October 2012 to March 2018. We present quantitative data for endemic and threatened species, identify migratory status and highlight distributional novelties. In total, we recorded 229 species encompassing 63 families, including twelve species of conservation concern, 11 endemic to the Atlantic Forest or Pampas zoogeographical provinces and 38 migrants. We provide new records of seven rare species in Santa Catarina (Larus atlanticus, Calidris pusilla, Aramides ypecaha, Bubo virginianus, Limnornis curvirostris, Phacellodomus ferrugineigula and Pseudocolopteryx flaviventris) and report the first evidence of occurrence of Schoeniophylax phryganophilus for the State. Based on our findings, we discuss the regional diversity and conservation of the avifauna. Key-Words. Species list; Coastal lagoon; Inventory; Species richness; Threatened species.


INTRODUCTION
Coastal lagoons and their surrounding environments frequently form complex mosaics of aquatic and terrestrial ecossystems that harbor high biodiversity (Esteves et al., 2008).The high productivity of such wetlands provides essencial ecosystemic services to humankind such as water supply and fishing resources (Esteves et al., 2008).One of the largest complex of lagoons in the Neotropical region is found in the southern coast of Brazil, ranging from southern Santa Catarina state to southern Rio Grande do Sul state (Burger, 1999).This landscape was created by sea movements within the last 7,000 years and currently includes lagoons associated with a diverse range of habitats as estuaries, mangroves, grasslands, wetlands, restingas and lowland forests (Burger, 1999;Tomazelli & Villwock, 2005).These ecosystems have been intensively modified in southern Brazil due to human occupation, agriculture, pollution, and introduction of exotic species (Esteves et al., 2008).
Ornithological surveys on the coastal lagoons of southern Santa Catarina were pioneered by the French naturalist August de Saint-Hilaire in 1820, who made relevant contributions such as collecting the holotype of Sterna hirundinacea Lesson, 1831 in Laguna (Carlos & Voisin, 2013) and recording an enigmatic and unidentified blue macaw in Imbituba (Straube, 2010).After Saint-Hilaire, some few naturalists visited the region to collect specimens which are roughly listed in classical catalogues (e.g., Hellmayr, 1936, Pinto, 1938).Later surveys in such area include broad-scale inventories with overall descriptions of the species and their distribution, which are to date the most complete studies on the avifauna for the southern coast of Santa Catarina (Rosário-Bege & Marterer, 1991;Rosário, 1996).However, comprehensive studies are still missing for the last three decades, when the region experienced fast increasing habitat modification (Guadagnin & Laidner, 1999).The few recent studies include bird inventories in beaches and islands in Laguna (Silva, 2003) and in the microbasin of the Ibiraquera lagoon (Piacentini & Campbell-Thompson, 2006), and shorebirds censuses near the mouth of the Araranguá river (Branco et al., 2004).Additionally, several recent records of single or few species have been reported for the region (Azevedo & Ghizoni-Jr., 2005;Piacentini et al., 2006Piacentini et al., , 2009;;Amorim & Piacentini, 2006, 2007;Ghizoni-Jr. & Azevedo, 2010;Willrich et al., 2015).
Here we carried out bird inventories in ten sites in the southern coast of Santa Catarina.We provide a qualitative checklist of birds, highlighting endemic and Nearctic, Austral and Neotropical migrants and provide data on habitats, abundances and sites of occurrence for threatened, novel and poorly known species for Santa Catarina.Based on our findings we discuss the importance of the region for bird conservation.

Study area
The entire coastal region of southern Santa Catarina state extends from the municipalities of Garopaba to Passo de Torres, in the border with Rio Grande do Sul state (Guadagnin & Laidner, 1999).In this study, we in- Table 1.Study sites in the southern coast of Santa Catarina state, Brazil, with details on coordinates, size, sample effort, periodicity and habitats sampled (be = beach, cf = cultivated field, ex = plantation of exotic trees -eucalyptus or pinus, fo = lowland forest, la = coastal lagoon, ma = marsh with stands of emergent macrophytes, ng = native grassland, om = open marsh, pa = pasture, sr = shrubby restinga, ua = urban area).

Data collection
We sampled ten sites located from the mouth of Urussanga River to the mouth of Mampituba River (Fig. 1).Sampled areas varied from 0.28 to 4.75 km² (summing up 21 km²) and up to 50 m above the sea level.Surveys were carried out between October 2012 and March 2018 and consisted of one-day samplings, lasting from 3 to 10 h per site, mainly from 07:00-12:00 h and 14:00-18:00 h.In total, each site was sampled between 8 h and 70 h, summing up 274 hours of fieldwork.Coordinates, dates of field expeditions and habitats sampled in each site are described in Table 1.In each field expedition, all birds heard or seen with aid of binoculars in pre-existing trails and roads were identified.Playbacks of voice-recordings of species potentially occurring in the area were used, especially to search for cryptic species.Photographs and voice-recordings obtained during fieldwork were archived in the website WikiAves (www.wikiaves.com.br) and can be accessed online using voucher codes provided in Table 2.In order to provide a more complete inventory, species undetected during field work but with previous records for these sites in the literature (i.e., Rosário, 1996;Branco et al., 2004;Rupp et al., 2007) or WikiAves (searched up to July 2017) were included as Appendix.Data from Rosário (1996) was obtained in the website Aves de Santa Catarina (http://avesdesantacatarina.com.br).Also, some records available at WikiAves or made by other reseachers in the study areas were cited in the species account and/or in the discussion.

Classification of endemic, migratory, threatened species and novel records
Classification of endemic species for Atlantic Forest and Pampas follows Bencke et al. (2006).Migrant species followed the list of migratory birds of Brazil (Somenzari et al., 2018) and were classified in three categories as follows: "Nearctic migrants" breed in the Northern Hemisphere and move southward to spend the austral winter (Chesser, 1994); "Austral migrants" breed in austral regions of South America and move northward to spend the austral winter (Chesser, 1994) and; "Neotropical migrants" breed in our study area and move northward to spend the austral winter in tropical humid regions (Belton, 1994).We considered species of conservation concern those listed in at least one redlist in global (GL) (IUCN, 2015), national (BR) (MMA, 2014) and/or local (SC) levels (CONSEMA, 2011).For threatened species and distributional novelties, we provide details on number of individuals, habitats and dates of records.We considered distributional novelties in Santa Catarina as those species whose nearest record lies over 100 km from our study sites or species previously unknown or known from less than five localities in this state (i.e., Rosário-Bege & Marterer, 1991;Rosário, 1996;Amorim & Piacentini, 2006;Piacentini et al., 2006;Ghizoni-Jr. & Azevedo, 2010).Both criteria follow Vizentin-Bugoni et al. (2015).Taxonomic nomenclature follows Piacentini et al. (2015).Specimens found dead were deposited at the ornithological collection of the Pontifícia Universidade Católica do Rio Grande do Sul.

Larus atlanticus Olrog, 1958 (GL -VU; BR -LC; SC -LC)
On June 29 th 2014, a juvenile was photographed (Fig. 3A; WA1372730) and five other adults were observed in a mixed flock with Larus dominicanus (Lichtenstein, 1823) on the beach in Praia do Rincão.On August 28 th 2016, again an adult individual was recorded in Praia do Rincão (WA2257972).

Gallinago undulata (Boddaert, 1783) (SC -VU)
On 13 th January 2018, we heard for five times calls of two individuals and once barely observed them in a natural grassland used for livestock raising near the mouth of Urussanga River (28°48'47.60"S,49°12'34.23"W).

Thalasseus maximus (Boddaert, 1783) (GL -LC; BR -EN; SC -VU)
Several records during autumn, winter and spring were obtained on the beach in Praia do Rincão: in 2013, it was recorded on May 19 th (10 individuals), June 13 th (nine individuals) and June 15 th (four individuals; WA988660), July 13 th (nine individuals) and October 3 rd (eight individuals; Fig. 3B and WA1622675); in 2014, it was recorded on May 24 th (two individuals), June 29 th (two individuals) and June 26 th , 2014 (10 individuals).In addition, some scattered flocks of three up to four individuals were recorded near Araranguá river mouth on April 21 st 2013 (WA960303).

Bird diversity
We present here a comprehensive update of the bird diversity and composition in the region of the coast-al lagoons in southern Santa Catarina.In total, the 250 species recorded here represents 36% of the avifauna of Santa Catarina state (700 species; Aves de Santa Catarina, 2016).Proper comparisons of bird diversity between ours and previous studies from surrounding areas are limited due to major differences in sampling and habitats considered.In coastal wetlands of Rio Grande do Sul, for example, the presence of multiple habitats, e.g., forests, marshes, and grasslands, has been shown to increase considerably the bird species richness (Vizentin-Bugoni et al., 2015;Dias et al., 2016), which may be the case for coastal Santa Catarina as well, which encompass multiple habitats even in relatively short distances.Nevertheless, the total richness observed in our study can be considered intermediate in comparison to other coastal areas of southern Brazil: 120 species were recorded in Ibiraquera lagoon microbasin (Piacentini & Campbell-Thompson, 2006), 227 species in Carijós Ecological Station (Vieira et al., 2014) and 228 species in Pirajubaé Extractive Marine Reserve (Vieira, 2016), all of them in Santa Catarina.Other inventories in the coast of Santa Catarina (e.g., Branco et al., 2004;Grose et al., 2013;Grose & Cremer, 2015;Vieira et al., 2015) were restricted to few habitats (i.e., islands and beaches) and are too local for any comparison.For coastal wetland areas in Rio Grande do Sul, bird richness varies from 170 to 283 species (Vizentin-Bugoni et al., 2015).

Distributional novelties
A total of 68 species are novel records for the southern coast of the state in comparison to the previous broad-scale inventories (Rosário-Bege & Marterer, 1991;Rosário, 1996).However, most of the novel species to the region are currently common and locally widely distributed with numerous recent records on online databases (e.g., WikiAves).Some of these species represent recent range expansions in Santa Catarina as Eupetomena macroura (Gmelin, 1788), Myiopsitta monachus (Boddaert, 1783), Zenaida auriculata (Des Murs, 1847) and Turdus leucomelas Vieillot, 1818(e.g., Rosário, 1996;Straube et al., 2006) or are species difficult to detect due to inconspicuous behavior such as Botaurus pinnatus (Wagler, 1829), Ixobrychus involucris (Vieillot, 1823) and Bubo virginianus.We also recorded Schoeniophylax phryganophilus for the first time in Santa Catarina and presented the first records of Aramides ypecaha and Limnornis curvirostris in the field, which were to date known in the state only by single unpublished museum specimens.Larus atlanticus, Bubo virginianus and Phacellodomus ferrugineigula are known to the state by only one (Pacheco et al., 2009), four (Piacentini et al., 2006;Alves & Pozenato, 2013;Just et al., 2015Just et al., , 2016) ) and two (Minns et al., 2010;Just et al., 2015) previous records in literature, respectively.We also reported here the third and the first known populations of the globally threatened Xolmis dominicanus and Xanthopsar flavus, respectively, for the coast of Santa Catarina.As the nearest breeding populations of such species are known only for the coast of Rio Grande do Sul (Belton, 1994;Dias & Maurício, 2002) and upland grasslands in Santa Catarina and Rio Grande do Sul (Repenning et al., 2010), our records likely correspond to wintering individuals.

Conservation issues
The mosaic of habitats including the coastal lagoons of southern Santa Catarina has been recognized as "an area of extreme importance for the conservation, sustainable use and benefit sharing of the Brazilian biodiversity" (MMA, 2007).Likewise, Schott & Carbonell (1986) defined 'Lagoa do Sombrio' as an important area for the conservation of aquatic birds in the Neotropics.Despite these designations, there is currently only a few protected areas which cover small portions of natural habitats and are of sustanaible use, namely 'Área de Proteção Ambiental Baleia Franca' and 'Reserva Particular do Patrimônio Natural Capão Redondo' (14 ha).Additional protected areas have been created recently in the region of Praia do Rincão, namely 'Monumento Natural Morro dos Conventos' (280 ha), 'Área de Proteção Ambiental Costa de Araranguá' (3,213 ha) and 'Reserva Extrativista Rio Araranguá' extractive reserve (566 ha), but such reserves are not implemented yet and may be considered "paper parks" (Araranguá, 2016a, b, c).Importantly, the high diversity of Nearctic and Austral migrants and regionally threatened species found in the region of Praia do Rincão suggest that these protected areas may be especially important for the conservation of resident and migratory shorebirds.
Three threatened species, namely Larus atlanticus, Xolmis dominicanus and Xanthopsar flavus, were only scarsely recorded in the region and may be considered occasional visitors.Specifically, Larus atlanticus migrates northward after breeding in austral regions of South America, while the two other species are endemic to nat-ural grasslands of southeastern South America (Rosário, 1996).On the other hand, native habitats play an important role for the other nine threatened species in our study area.Lowland forests harbour high numbers of the vulnerable Phylloscartes kronei and other eight resident least concern species endemic to the Atlantic Forest.Mouths of Urussanga and Araranguá rivers and adjacent sandy beaches are important as wintering ground for a high number of long-distance migratory birds (Branco et al., 2004; this study), as breeding ground for some species as Sternula superciliaris (Vieillot, 1819) (Branco et al., 2004), Geositta cunicularia and Haematopus palliatus Temminck, 1820 (pers.obs.) and hold populations of regionally threatened birds, namely Thalasseus maximus, Calidris canutus, Sterna hirundinacea, and Geositta cunicularia.Marshy areas surrounding lagoons may be relevant in Santa Catarina to sustain high numbers of wetland-dependent species as the regionally threatened Tachuris rubrigastra and other least concern species as Pseudocolopteryx spp., Phleocryptes melanops (Vieillot, 1817), Limnornis curvirostris and Hymenops perspicillatus (Gmelin, 1789).
Notably, some bird species previously recorded in the region were not found in this study and the reasons may be diverse.Although some few species were likely undetected due to their cryptic habits, populations of other species may be decreasing or have gone locally extinct.This may be the case of species like: Rhea americana (Linnaeus, 1758), which is known for Santa Catarina only for a egg collected in 1934 in Sombrio (Rosário, 1996); Cygnus melancoryphus (Molina, 1782) and Netta peposaca (Vieillot, 1816) which were last recorded in the region almost 30 years ago (Sick et al., 1981;Rosário, 1996); Hydropsalis anomala (Gould, 1838) which was collected on 1991 in Sombrio (deposited in the Museu Nacional do Rio de Janeiro, MN-37515) (Rupp et al., 2007).There is also an intriguing undocumented report of the threatened Biatas nigropectus (Lafresnaye, 1850) for a lowland forest north of Lagoa do Caverá in 1988 (Rosário, 1996).Other records of this bamboo-dependent species in Santa Catarina are restricted to montane forests in the northeastern portion of the state (Rosário, 1996; distribution map available at WikiAves, www.wikiaves.com.br/mapaRegistros_papo-branco).
Additionally, the rate of records of some aquatic and wetland dependent species seems to have considerably decreased in the last three decades.For example, hundreds of individual of waterfowl species (Anatidae) were historically reported for the coastal lagoons of southern Santa Catarina (Rosário-Bege & Marterer, 1991;Rosário, 1996), however, we recorded less than half of the Anatidae species mentioned for these studies and always in small flocks up to ten individuals.Other aquatic species of the families Podicipedidae (i.e., Podicephorus major (Boddaert, 1783), Podilymbus podiceps (Linnaeus, 1758) and Rollandia Rolland (Quoy & Gaimard, 1824)) and Rallidae (Fulica armillata Vieillot, 1817) were also detected in low numbers and some other species were not even found (i.e., Fulica rufifrons Philippi & Landbeck, 1861 and Porphyriops melanops (Vieillot, 1819)).Capture for pet trade and habitat loss may have extirpated the once frequent Sporophila collaris (Boddaert, 1783) from most suitable marshy areas in the region (Rosário, 1996), as it has few recent records (WikiAves, www.wikiaves.com.br/ mapaRegistros_coleiro-do-brejo).
In regard to migratory birds, the lack of previous comprehensive studies on these groups has apparently hampered the inclusion of the southern coast of Santa Catarina in conservation initiatives (Bencke et al., 2006;Valente et al., 2011;CEMAVE/ICMBio, 2016).For instance, an attempt to identify important areas for Nearctic migratory birds in Brazil included adjacent Rio Grande do Sul and Santa Catarina states, but excluded the southern coast of the latter (Valente et al., 2011).Our records of 18 shorebirds species plus six other species from literature and WikiAves sum up 24 species of Nearctic migrants for southern Santa Catarina; additional species are Numenius hudsonicus Latham, 1790 (Silva, 2010), Calidris himantopus (Bonaparte, 1826) (Willrich et al., 2015), Calidris minutilla (Vieillot, 1819) (Leal, 2015), Calidris subruficollis (Vieillot, 1819) (Machado, 2012), Arenaria interpres (Linnaeus, 1758) (Bianco, 2009) and Phalaropus tricolor (Vieillot, 1819) (Santos, 2012).This high richness compared to other important stopover areas (Valente et al., 2011;CEMAVE/ICMBio, 2016) demonstrates the importance of southern Santa Catarina for several migratory species.Thus, we strongly recommend that future initiatives on migratory birds carefully consider the southern coast of Santa Catarina, especially sandy beaches from Laguna to Passo de Torres.
In summary, we demonstrated that the region of the coastal lagoons of southern Santa Catarina harbours high bird richness, including several threatened, endemic and long-distance migratory species.We believe this inventory presents crucial basic information useful to support further conservation strategies concerning this important coastal area in southern Brazil.The regional avifauna would be benefited by the implementation and proper management of the existing protected areas.Moreover, areas of high diversity of threatened and migratory birds such as Praia do Rincão and Lagoa do Sombrio, may be priority regions for the establishment of new protected areas and conservation efforts.We also encourage further surveys in such areas specially focused on assessing the abundances of endemic, threatened and migratory species.Further research aiming to investigate the consequences of anthropic activities on the avifauna is also necessary in order to understand the extent of such impacts, especially fragmentation of wetlands and grasslands, plantation of large stands of exotic trees, traffic on beaches and drainage of wetlands.

Figure 2 .
Figure 2. Habitats surveyed in the southern coast of Santa Catarina state, Brazil.(A) A general view of Morro dos Conventos beach, Araranguá; (B) Dunes and shrubby restingas near the mouth of Araranguá river, Araranguá; (C) Lagoon in the locality of Ilhas, near the mouth of Araranguá river, Araranguá; (D) A general view of the northeastern portion of Lagoa da Urussanga Velha, Balneário Rincão; (E) Understory of a lowland forest in Morro dos Macacos ecological park, Passo de Torres; (F) Wetlands of Typha domingensis in the border of Lagoa do Sombrio, Passo de Torres; (G) Mouth of Urussanga river, Balneário Rincão; (H) Wetlands with Scirpus giganteus in Lagoa do Rincão, Balneário Rincão.