An inventory of wetland non-passerine birds along a southeastern Brazilian coastal area

1 Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF). Av. Alberto Lamego, 2000, Parque Califórnia. 28013-602. Campos dos Goytacazes, RJ, Brasil. Campos dos Goytacazes, RJ, Brasil. 2,3 Escola Nacional de Saúde Pública FIOCRUZ. Rua Leopoldo Bulhões, 1480, 6o. andar, sala 611, Manguinhos. 21041210. Rio de Janeiro, RJ, Brasil. 1 wetlandbirdsbrazil@gmail.com (corresponding author), 2 gemmlagos@gmail.com

From the biological standpoint, mangroves, estuaries and coastal lagoons rank among the most productive environments, with undisputable importance in the life cycle of water birds (Knoppers 1994;Weller 2003; Alfaro & Clara 2007).However, compared to other environments, these ecosystems have been more intensely affected by anthropogenic activities (World Resources Institute 2005).In a conjoint effort by several nations to identify wetlands of transnational importance, the Ramsar Convention establishes goals and raises funds for recovery and conservation initiatives (Ramsar Convention 2009).
In Brazil, the Atlantic Forest is a priority area in biodiversity conservation strategies (Myers et al. 2000).Several wetland environments are observed in the biome, like rivers, marshes, floodable plains, mangroves, estuaries and coastal lagoons (Veloso et al. 1991).More specifically, anthropogenic practices as varied as the digging of canals, land filling for reclaiming, urbanization, industrial developments as well as unrestrained commercial fishing and hunting have reshaped coastal wetlands in southeastern Brazil, leading to an overall decline in the region's natural wetlands (Antas et al. 1986;Czech & Parsons 2002;Esteves 2011).These practices pose a real risk not only to bird populations, but also to the whole existing diversity in these coastal environments (Ma et al. 2010;Tavares et al. 2012).
The composition and distribution of bird species in coastal wetlands of Rio de Janeiro State, southeastern Brazil have been poorly investigated.Most inventories published till date have addressed bird assemblages in the state's central coastal area, especially the city of Rio de Janeiro (e.g., Sick & Pabst 1968;Mallet-Rodrigues et al. 2008;Maciel 2009).Although the state's northern coast is the most representative area in terms of coastal lagoons and other wet environments, systematic, longterm studies on the water bird assemblages in the area have not been published.In this sense, Pacheco et al. (1996), who made new bird records for the region, underscore the wide ornithological information gap in northern Rio de Janeiro State.
This study presents an inventory of non-passeriform birds sighted in wetlands along an area in the northern expanse of the coast of Rio de Janeiro, southeastern Brazil.

Study area
The study area covered 44km of the shoreline in the municipality of Quissamã (22 0 12'22"S & 41 0 24'29"W), northern Rio de Janeiro, southeastern Brazil, between João Francisco and Barra do Furado beaches (Fig. 1).This area has a chain of 17 shallow coastal lagoons whose size, vegetation and salinity, among other physicochemical parameters, are strongly influenced by rainfall precipitation (Hollanda-Carvalho et al. 2003;Bove & Paz 2009).The dry season spans from May to August, while the rainy season lasts from September to April (Quissamã-RJ 2006).Of the 44km of the transect assessed, 21km are part of the 'Restinga de Jurubatiba National Park', whose conservation area includes marshes, lagoons, floodable plains, beaches as such and 'restinga' vegetation.Restingas are characterized by mosaics of coastal plant communities under high fluviomarine influence, which are included in the Atlantic Forest biome (See Assumpção & Nascimento 2000).Also, Feia lagoon, the second Brazilian freshwater lagoon in size, stands out as a remarkable natural feature.This lagoon communicates with the Atlantic Ocean through a channel locally known as 'Canal das Flechas', in Barra do Furado.

Methods
Surveys were carried out once a month, from June 2011 to May 2012, covering a whole year's season cycle and totaling a sighting effort of about 68hr.Bird sightings were made along a 44-km linear continuous transect of beaches, preferably between 06:00 and 10:00 hr in a motor vehicle at a mean speed of 20km/hr (Bibby et al. 2000).More specifically, sighting covered 300m on either side of the transect.This afforded the ability to record birds in three different environments: coastal lagoons adjacent to the shoreline, the marine environment, and the beach as such (Veloso et al. 1991;Caris et al. 2009).Records were made using binoculars (Nikon Monarch 8x42) and a telescope (Celestron Ultima 80x20-60).Additionally, ad libitum observations were carried out during 72 beach patrols (totaling 204hr of field effort) for seabirds and marine mammal carcasses, between February 2008 and July 2012.
The species list included only non-passerine wetland birds, since this study is part of a larger waterbird monitoring project in the wetlands in northern Rio de Janeiro State.The taxonomic sequence and scientific nomenclature follow the most recent checklist of Brazilian birds (CBRO 2011).The final checklist was based on field work data as well as on current literature, in order to include species previously mentioned in the study area, as recommended by Carlos et al. (2002).
The species accumulation curve was plotted using the Jackknife 1 estimator of species richness, considering 1000 randomizations with replacements, using the software EstimateS (Colwell 2005), for data obtained during the monthly excursions between June 2011 and May 2012.Jackknife 1 is appropriate for the design of the present study, since it requires occurrence data only, instead of abundance information (Heltshe & Forrestor 1979).Variation of monthly species richness was tested by the chi-square test (Brandolin et al. 2007) using the software R 3.0.0.

Results and Discussion
In total, 76 bird species of 15 families were recorded (Appendix 1).Of these, the Comb Duck Sarkidiornis sylvicola, Pectoral Sandpiper Calidris melanotos, Wilson's Phalarope Phalaropus tricolor, South American Painted-Snipe Nycticryphes semicollaris and Franklin's Gull Leucophaeus pipixcan were recorded during ad libitum beach patrols.The inclusion of Wood Stork Mycteria americana and Clapper Rail Rallus longirostris was based on the Agroecological Zoning Reports of Restinga of Quissamã (Quissamã-RJ 1994).Therefore, 69 species were detected in the field excursions carried out between June 2011 and May 2012.It should be stressed that Blue-winged Teal Anas discors, previously observed by Antas et al. (1986) as a pseudo-vagrant species in wetlands of the Feia lagoon, was not recorded in the present survey.The majority of species recorded belonged to families Scolopacidae (15), Ardeidae (10), Rallidae (10) and Anatidae (9).
Of the total 76 species recorded, 24 (31.6%) were migrants, of which 22 breed in the northern hemisphere, and only two originate from southern South America, namely Magellanic Penguin Spheniscus magellanicus, recorded in August and September 2011, and Great Grebe Podicephorus major, observed in June 2011, February and December 2012.Remarkably, 17 (22.4%)Nearctic shorebird species were observed.
Nine species (11.8%) recorded are listed as threatened in Rio de Janeiro (Alves et al. 2000).The Maguari Stork Ciconia maguari and the Muscovy Duck Cairina moschata are Vulnerable, while the Black-bellied Whistling-Duck Dendrocygna autumnalis, Roseate Spoonbill Platalea ajaja, White-backed Stilt Himantopus melanurus, Grey-  Concerning environment use, 50 species were observed to take only one environment, 48 of which used lagoons and two (Brown Booby Sula leucogaster and Magnificent Frigatebird Fregata magnificens) the marine environment.No species used the beach in an exclusive fashion (Appendix 1).These findings reflect the important role of coastal lagoons and surrounding environments in the maintenance of regional biodiversity, possibly due to the wide variety and considerable abundance of food resources that result from the high biological production of these environments (Esteves 1998b;Hollanda-Carvalho et al. 2003;Enrich-Prast et al. 2004;Macedo-Soares et al. 2010).Also, nearctic shorebirds were more abundantly recorded in marshes and lagoons less than 20cm in depth.The Sanderling Calidris alba, White-rumped Sandpiper Calidris fuscicollis and Ruddy Turnstone Arenaria interpres were often sighted feeding on small gastropods associated with aquatic plants of the genus Utricularia (Lentibulariaceae) and puddles in the Casa Velha and Ubatuba lagoons (Fig. 1).
Of all the species recorded in the present study, only Nycticryphes semicollaris, Pomarine Jaeger Stercorarius pomarinus and Parasitic Jaeger Stercorarius parasiticus were not recorded inside Restinga de Jurubatiba National Park.However, remarkably high abundances of some species were recorded outside the limits of this protected area.Flocks of c. 600 Cabot's Terns Thalasseus acuflavidus were often sighted in Barra do Furado.Also, fledglings of H. melanurus and the largest flocks of C. maguari were inside that area and nearby (Image 1D).It should be emphasized that F. magnificens, S. leucogaster and T. acuflavidus were recorded feeding on fish waste disposed by artisanal fishing boats in areas nearing the terrestrial limits of the National Park.So far, no study has been published addressing the interaction between birds inhabiting the region and fishing activities.
Monthly richness values differed significantly from June 2011 to May 2012 (χ² = 19.98;df= 11; P<0.05).The highest richness value was recorded in May 2012, with 47 species, while the lower ones were observed in September and November 2011, with 22 species sighted in each month (Fig. 2).The contribution represented by the arrival of nearctic migrants between December 2011 and May 2012 for the increased richness values observed is evident (Fig. 2).However, contrary to expectations, relatively high species richness values were observed in June, due to the simultaneous sighting of bird species not customarily seen in the region, like C. moschata, Rufescent Tiger-Heron Tigrisoma lineatum, South American Tern Sterna hirundinaceae and P. major.High species richness is expected in the summer, when shorebirds, the main representatives of these bird assemblages, arrive at the study area.
Since at least one species was sighted in each of the last three months during field excursions, it is not possible to state that species numbers stabilized, as the species accumulation curve shows (Fig. 3).When the 69 species sighted between June 2011 and May 2012 are considered, the Jackknife 1 estimator of species richness foresaw the occurrence of 71 (±3) species in the area surveyed, similar to the richness observed (76 species), after 72 ad libitum excursions to the surveyed area for additional sightings.These results indicate that the estimator was effective in predicting species richness in the present survey.
The sightings reported herein enlarge the list of nearctic shorebirds species in the coastal area of Quissamã, from 5 to 17 (Santos & Alves 2011) (Appendix 1).However, it should be emphasized that Santos & Alves (2011) surveyed a 2-km transect of Restinga de Jurubatiba National Park, considerably shorter than the transect covered in the present study.The numerous shallow water bodies and low anthropogenic influence in the region surveyed, compared to other areas of Rio de Janeiro, make it a suitable site for Nearctic shorebirds (Isola et al. 2000;Holm & Clausen 2006;D.C. Tavares pers. obs. 2008D.C. Tavares pers. obs. -2012)).
The staging sites along the Atlantic Flyway are important in terms of molting and renovation of energy supplies required during migration (Leu & Thompson 2002).Twenty eight shorebird species (CBRO 2011) use staging areas along the Brazilian coast, mainly in the north and the south regions of the country, where high bird abundance and richness are observed (Sick 1997;Mestre et al. 2010).As for richness, the most representative areas have been shown to be in the states of Maranhão, with 15 species (Rodrigues 2000), Sergipe, with 16 species (Barbieri 2007), and Rio Grande do Sul, with 16 species (Dias et al. 2011;Petry et al. 2012).The high nearctic shorebird species richness observed in coastal lagoons in Quissamã (17 species) gives evidence of the important role of the region as a staging area for migratory birds at national level.Nevertheless, abundance data should be included in sampling efforts, comparing data collected in these areas with other sites in Brazil, and assessing their potential to be recognized as an Important Bird Area (IBA).The total richness observed was higher than the value reported by Alves & Pereira (1998) in Rodrigo de Freitas Lagoon, located on the central coast of Rio de Janeiro, more specifically, in the city of Rio de Janeiro, the state's capital.Alves & Pereira (1998) reported only nine waterbirds in that environment, a number that reflects the high degree of environmental degradation and historic anthropogenic influence in its natural hydrological conditions.This difference in richness values highlights the negative impact changes in hydrological regimens and water quality have on waterbird populations (Ma et al. 2010  Based on a literature review and weekly field excursions, Mallet- Rodrigues et al. (2008) listed 77 aquatic birds for Baixada de Jacarepaguá, Rio de Janeiro, of which 41 (53.2%) were not recent records.Among these 41 species, at least 30 (73.2%) were also sighted in the Quissamã coastline, underlining the important role the region plays in the species conservation scenario in Rio de Janeiro.
The higher species richness reported in the Quissamã coastline is probably due to the vast chain of coastal lagoons, marshes and flooded patches in sites nearby, closely located in a rather large area, compared to what is seen in other regions of Rio de Janeiro (Paracuellos & Tellería 2004).The diversity of hydrochemical patterns, water depth and vegetation features increases the available resource variability as well as waterbird species diversity (Esteves 1998a;Esteves 1998b;Taft et al. 2002;Hollanda-Carvalho et al. 2003;Enrich-Prast et al. 2004;Bove & Paz 2009).This is because the high richness of waterbirds is linked with the variety of habitat conditions (Ma. et al 2010).In this sense, it has been shown that lagoons deeper than 1m attract diving birds, while lagoons as shallow as 15cm are suitable feeding sites for small, medium and large shorebirds (Ntiamoa-Baidu et al. 1998).
In the area surveyed in the present study, the digging of canals caused most sites to dry out completely during the dry season.Large flocks of C. cirrocephalus and T. acuflavidus were observed feeding in at least eight coastal lagoons along the transect, except in the dry season, when these species concentrated mainly in Robalo and Visgueiro Lagoons (Fig. 1).Among the lagoons with favorable feeding conditions for these species, like abundant food resources and appropriate depth, Robalo and Visgueiro were the only water bodies that did not dry out due to canal digging.In spite of that, small flocks were sighted in the Canema and Piripiri Lagoons (Fig. 1) which, though richer in potential prey for C. cirrocephalus during the dry season (Macedo-Soares et al. 2010), is located in an urbanized area, a less advantageous aspect for this species, when compared to Robalo and Visgueiro Lagoons.
Despite the importance of the present inventoried coastal lagoons for waterbirds' stopover, these environments have experienced intense pressure from development, especially due to the digging of canals to claim land for agriculture, land filling practices and sewage discharges (Esteves 2011;Tavares et al. 2012).The construction of new ports and shipyards on the northern coast of the state of Rio de Janeiro brought a great new conservation concern regarding these lagoons, which are under risk of salinization due to the dredging of sea sand and its use for grounding practices.The salinization of water bodies may result in negative impacts on the habitat quality for shorebirds and other waterbirds (Rubega & Robinson 1996;Weller 2003;Ma et al. 2010).
Bird abundance data for the wetlands in the studied region is essential in the comparison with other areas in South America and in the assessment of its importance for the conservation of migratory and globally threatened bird species.More studies should be carried out on bird populations in these environments to define important and priority areas concerning use by waterand migratory birds in Rio de Janeiro State.It should be mentioned that other regions in Rio de Janeiro seem to provide suitable habitats for many water bird species, among which the area around Araruama Lagoon, where several existing salt ponds are used as staging areas (Santos & Alves 2011), and swamp areas to the north, like the water bodies in São João da Barra and São Francisco de Itabapoana.

Noteworthy records
Podicephorus major (Boddaert, 1783): Occurrence restricted to South America (Sick 1997).In Brazil, it occurs between the states of Rio Grande do Sul and Espírito Santo (Sick 1997;Simon et al. 2005).Here recorded in sea waters from 22 to 28 December 2011; 3, 9, 16 and 19 January 2012; 8 and 18 February 2012.Recorded also in June 2011 in Pires Lagoon (Fig. 1).Number of records and permanence figures lend strength to the species' geographic expansion hypothesis proposed by Simon et al. (2005) and its character of regular visitor in the region surveyed.Not previously recorded in northern Rio de Janeiro.
Ciconia maguari (Gmelin, 1789): Flocks of up to 26 individuals along large coastal lagoons under 30cm in depth, suitable for the species' feeding habits (Sick 1997).Carrilho Lagoon (Fig. 1 and Image 1D), outside Restinga de Jurubatiba National Park, seems to be the main area used by the species in the region.
Limosa haemastica (Linnaeus, 1758): Recorded on 13 May 2011 feeding in Pires Lagoon (Fig. 1 and Image 1C).Listed as locally rare along the Atlantic coastline by O'Brien et al. (2006) and in Rio de Janeiro state (Gagliardi 2011).However, it may occur as regular or abundant along Rio Grande do Sul state coastline during migration (Scherer & Petry 2012).Few scattered records in Central Amazônia (Sick 1997).
Calidris canutus rufa (Linnaeus, 1758): Recorded in flocks of 3 to 18 individuals feeding at lagoons inside Jurubatiba National Park in March, April and May 2012 (Image 1F).In Brazil, only the Canadian-breeding population, subspecies rufa occurs, most abundantly in Rio Grande do Sul and northern coasts (Harrington et al. 1986;Rodrigues & Lopes 2000).Heavy decline, commenced in the late 1990's (Niles et al. 2008).However, not listed as globally threatened because the IUCN does not consider subspecies (IUCN 2012b).Depleted food resources considered relevant threat to populations (Morrinson et al. 2004).
Himantopus melanurus (Vieillot, 1817): Eight adult individuals near a nest with two fledglings recorded on the 20 of June 2012 in a floodable plain in the mangrove São Miguel, cut by the road connecting downtown Quissamã to Barra do Furado (Image 1B).This record confirms the species' breeding on the coast of Rio de Janeiro, as previously suggested by Novelli (1997).
Nycticryphes semicollaris (Vieillot, 1816): Recorded on 19 July 2010 in a flooded area outside Restinga de Jurubatiba National Park, near Barra do Furado.Also recorded in June and July 2011 in Carrilho Lagoon (Fig. 1), in whose vegetation Cyperaceae prevail.Considered near threatened in Rio de Janeiro State (Alves et al. 2000).Mistakenly reported as winter visitor in banks of Feia Lagoon (Antas et al. 1986), probably due to usual concentrations of flocks of c.100 individuals in northern Rio de Janeiro State after post-breeding movements (Sick 1997;Maciel 2009).
Phalaropus tricolor (Vieillot, 1819): One individual sighted on 17 December 2010 in Ubatuba Lagoon (Fig. 1) next to a mixed flock of C. fuscicollis, Calidris alba and Pluvialis squatarola.Though not photographed, sighting by telescope was possible.Listed as relatively common in southern Brazil, floodable plains of Amazônia, and Campos dos Goytacazes lowlands, Rio de Janeiro State (Sick 1997).Not cited in the list of birds occurring in the state, until present record (Gagliardi 2011), possibly due to the lack of published records in the past 10 years.
Chroicocephalus cirrocephalus (Lichtenstein 1823): Flocks of 300-1000 individuals have been recorded during the dry season, when using the coastal lagoons as feeding and resting sites, mainly Robalo, Visgueiro and Barra do Furado Lagoons (Fig. 1 and Image 1A).Considered threatened in Rio de Janeiro (Alves et al. 2000).Possible breeds in the region.
Stercorarius pomarinus (Temminck, 1815): One individual resting on a beach on 27 January 2012 was the first record in Rio de Janeiro (Image 1E).Though difficult to identify in its winter resting areas (Olmos 2000), the species differs from S. parasiticus and S. longicaudus by a more robust and bi-colored bill (Lima et al. 2004;Perlo 2009).Previously considered rare in western Atlantic  (Olsen & Larsson 1997).More recent data by Olmos (2000) suggests that this species is a regular visitor in the coast of Brazil and that the status of rare species in the country is due to the lack of regular observation efforts.

Figure 3 .
Figure 3. Accumulation curve of waterbird species recorded on the coastal area of the Quissamã Municipality, northern coast of Rio de Janeiro State, Brazil.Continuous line: Jackknife 1 estimator values, considering 1000 randomizations with replacement.

Monthly richness of waterbird assemblages on the coastal area of Quissamã municipality, northern coast of Rio de Janeiro State, Brazil, between June 2011 and May 2012.
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