An inventory of wetland
non-passerine birds along a southeastern Brazilian coastal area
Davi Castro Tavares 1,2 & Salvatore Siciliano 3
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.
21041-210. Rio de Janeiro, RJ, Brasil.
1 wetlandbirdsbrazil@gmail.com (corresponding author), 2 gemmlagos@gmail.com
doi: http://dx.doi.org/10.11609/JoTT.o3424.4586-97 | ZooBank: urn:lsid:zoobank.org:pub:1791462D-647E-4DA0-BB05-D5F6AF0741C1
Editor: Anonymity requested. Date
of publication: 26 July 2013 (online & print)
Manuscript details: Ms #
o3424 | Received 03 December 2012 | Final received 28 May 2013 | Finally
accepted 02 July 2013
Citation: Tavares, D.C. & S. Siciliano(2013). An inventory of wetland non-passerine birds along a
southeastern Brazilian coastal area. Journal of Threatened Taxa5(11): 4586–4597; http://dx.doi.org/10.11609/JoTT.o3424.4586-97
Copyright: © Tavares & Siciliano 2013. Creative Commons
Attribution 3.0 Unported License. JoTT allows unrestricted use of this
article in any medium, reproduction and distribution by providing adequate
credit to the authors and the source of publication.
Funding: State University of Northern
of Rio de Janeiro (UENF); Oswaldo Cruz Foundation (FIOCRUZ); Prefeitura de
Quissamã.
Competing Interest: None.
Acknowledgements:Theauthors are grateful to the municipal authorities of Quissamã and Carapebus,
the Ecology and Natural Resources Post-graduation Program, Universidade
Estadual do Norte Fluminense, to C. J. Carlos and F. Olmos for the confirmation
of the record of Stercorarius pomarinus and J. F. Pacheco for kindly
providing historically relevant literature. To M. Almeida, D. Awabdi, E. Zart,
L. Valadares, M. Gonçalves and M. Sucunza for their enduring help in
fieldworks. S.S. is supported by Conselho Nacional de
Desenvolvimento Científico e Tecnológico-CNPq. D.C.T. is supported by
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES.
Abstract: This paper presents the list of non-passerine birds of coastal
environments of the Quissamã municipality, northern Rio de Janeiro State,
southeastern Brazil. The surveys
were conducted monthly between June 2011 and May 2012. Additional ad libitumobservations were made between February 2008 and July 2012. We recorded 76 waterbird species of 15
families, of which Scolopacidae was the most representative, with 15 species. The high Nearctic shorebird species
richness observed in coastal lagoons in Quissamã (17 species) is an evidence of
the important role of the region as staging site for migratory birds at
national level. Also, nine of the
species recorded are threatened at regional and one is threatened at national
level. It should be emphasized that
three species considered locally extinct in the municipality of Rio de Janeiro,
the most extensively surveyed area in the State, were recorded in the present
study. Additionally, we present a high number of previously unrecorded species
in northern Rio de Janeiro, and report the first documented record of Stercorarius
pomarinus in Rio de Janeiro State. The region has a notorious Waterbird richness including endangered and
migratory species, when compared to other coastal areas of the state.
Keywords: Habitat diversity, northern Rio de Janeiro,
Restinga de Jurubatiba, shorebirds, threatened environment, tropical coastal
lagoons.
For figures, images, tables -- click here
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, long-term 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 (22012’22”S &
41024’29”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 fluvio-marine 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 longirostriswas 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 maguariand 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-hooded Gull Chroicocephalus cirrocephalus, Black
Skimmer Rynchops niger and N. semicollaris are Near Threatened
(Alves et al. 2000). Additionally, the Royal Tern Thalasseus maximus is
nationally threatened (Silveira & Straube 2005) and S. magellanicusis a Near Threatened species at global level (IUCN 2012a). Interestingly, the list included three
species currently considered locally extinct in the municipality of Rio de Janeiro,
a region that has been comprehensively surveyed: C. maguari, M. americana and Cairina moschata (Maciel
2009). Besides, D. autumnalis,H. melanurus and C. cirrocephalus, considered rare in this
municipality, were often observed in flocks of up to 100, 400 and 800
individuals, respectively, along the coastal lagoons in Quissamã. Also, of the 76
waterbird species recorded, 31 (40.8%) have special importance due to
the lack of data necessary for a precise assessment of threatened status at
regional level (Alves et al. 2000). Of these, 19 (61.3%) are nearctic migratory
species.
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 ofH. melanurus and the largest flocks of C. maguari were
inside that area and nearby (Image 1D). It should be emphasized that F. magnificens, S. leucogasterand 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. 2008–2012).
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 eightshorebird 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 water- and 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.
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