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Breeding biology review of White-backed Stilt Himantopus melanurus in Brazil and a case study in the largest restinga protected area (Aves, Charadriiformes, Recurvirostridae)

Abstract

In Brazil, the White-backed Stilt Himantopus melanurus is distributed in the midwest, south and southeast but breeding information is scarce. In this study, species breeding information in the country was compiled from online platform (WikiAves, eBird) and literature. A case study describing nests and egg biometry were reported in Restinga of Jurubatiba National Park (RJNP), on the north cost of Rio de Janeiro state, as well potential threats to the species. Sampling was carried out in September and December 2018, monthly in 2019 and between January to March and September to December in 2020. Overall, 70 breeding records were compiled, between 1997 and November 2021, being 64 from WikiAves in all regions of Brazil, four records from eBird in São Paulo state (in 2021) and two records in literature (one from São Paulo state, in 2007 and one from Rio de Janeiro in 2012). In RJNP, 44 nests were identified being 34 active, with an average of 3.5 eggs per nest, and overall 118 eggs were measured. The main materials used to build the nests were the saltmarsh plant and mud. Around 60% of nests were degraded or predated. Predation was the main cause of egg loss. Successful nests (with chicks or hatching signs) represented 26% of the total nests monitored. This study reports the first information on the biometry of the species’ eggs and nests, confirming the northern coast of Rio de Janeiro state as a nesting area for the species.

Keywords.
Coastal lagoons; Recurvirostridae; Reproduction; Restinga de Jurubatiba; Shorebirds; Online platforms

INTRODUCTION

Charadriiformes includes 19 families, 95 genera with 383 species, being one of the largest orders in the Aves group (Billerman et al., 2020Billerman, S.M.; Keeney, B.K.; Rodewald, P.G. & Schulenberg, T.S. 2020. Birds of the World. Ithaca, Cornell Laboratory of Ornithology. Available: Available: https://birdsoftheworld.org/bow/home . Access: 03/06/2021.
https://birdsoftheworld.org/bow/home...
). Among the families, Recurvirostridae has three genera, with Himantopus and Recurvirostra considered cosmopolitan, and Cladorhynchus is monotypic and with distribution restricted to Australia (Pierce & Bonan, 2020Pierce, R.J. & Bonan, A. 2019. Avocets, Stilts (Recurvirostridae). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the World Alive. Barcelona, Lynx Edicions.; Winkler et al., 2020Winkler, D.W.; Billerman, S.M. & Lovette, I.J. 2020. Stilts and Avocets (Recurvirostridae), versão 1.0. In: Billerman, S.M.; Keeney, B.K.; Rodewald, P.G. & Schulenberg, T.S. (Eds.). Birds of the World. Ithaca, Cornell Lab of Ornithology.). Among the three genera, Himantopus has the most controversial taxonomy (Robinson et al., 2020Robinson, J.A.; Reed, J.M.; Skorupa, J.P. & Oring, L.W. 2020. Black-necked Stilt (Himantopus mexicanus), versão 1.0. In: Poole, A.F. & Gill, F.B. (Eds.). Birds of the World. Ithaca, Cornell Lab of Ornithology. https://doi.org/10.2173/bow.bknsti.01.
https://doi.org/10.2173/bow.bknsti.01...
). Some authors identify three to five subspecies (Iqbal et al., 2010Iqbal, M.; Abdillah, H. & Nurza, A. 2010. Black-winged Stilt Himantopus himantopus himantopus, a new shorebird for Indonesia. Wader Study Group Bulletin, 117: 1-3.; AOU, 1998American Ornithologists’ Union (AOU). 1998. Check-list da North American Birds. 7. ed. Washington, AOU.; Robinson et al., 2020Robinson, J.A.; Reed, J.M.; Skorupa, J.P. & Oring, L.W. 2020. Black-necked Stilt (Himantopus mexicanus), versão 1.0. In: Poole, A.F. & Gill, F.B. (Eds.). Birds of the World. Ithaca, Cornell Lab of Ornithology. https://doi.org/10.2173/bow.bknsti.01.
https://doi.org/10.2173/bow.bknsti.01...
), others consider only one (Johnsgard, 1981Johnsgard, P.A. 1981. The plovers, sandpipers, and snipes of the world. Lincoln, University of Nebraska Press.), two (Pierce, 1996Pierce, R.J. 1996. “Family Recurvirostridae (stilts and avocets).” In: del Hoyo, J.; Elliott, A. & Sargatal, J. (Eds.). Handbook of the Birds of the World . Vol. 3. Hoatzin to auks. Barcelona, Lynx Edicions. p. 332-347.; Pierce & Bonan, 2020Pierce, R.J. & Bonan, A. 2019. Avocets, Stilts (Recurvirostridae). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the World Alive. Barcelona, Lynx Edicions.) or five global species, and the Black-backed Stilt Himantopus mexicanus (Statius Muller, 1776) is distributed in North and Central America while the White-backed Stilt H. melanurus Vieillot, 1817 occurs in South America (Gochfeld et al., 1984Gochfeld, M.; Burger, J. & Jehl, J.R. 1984. The classification of coastal birds in the world. In: Burger, J. et al (Ed). Shorebirds: breeding behavior and populations. New York, Plenum Press. p. 1-15. (Behavior of Marine animals Current Perspectives in Research, 5); Robinson et al., 2020Robinson, J.A.; Reed, J.M.; Skorupa, J.P. & Oring, L.W. 2020. Black-necked Stilt (Himantopus mexicanus), versão 1.0. In: Poole, A.F. & Gill, F.B. (Eds.). Birds of the World. Ithaca, Cornell Lab of Ornithology. https://doi.org/10.2173/bow.bknsti.01.
https://doi.org/10.2173/bow.bknsti.01...
). In Brazil, the occurrence of both species is recognized (Pacheco et al., 2021Pacheco, J.F.; Silveira, L.F.; Aleixo, A.; Agne, C.E.; Bencke, G.A.; Bravo, G.A.; Brito, G.R.R.; Cohn-Haft, M.; Maurício, G.N.; Naka, L.N.; Olmos, F.; Posso, S.; Lees, A.C.; Figueiredo, L.F.A.; Carrano, E.; Guedes, R.C.; Cesari, E.; Franz, I.; Schunck, F. & Piacentini, V.Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee - second edition. Ornithology Research, 29: 94-105. https://doi.org/10.1007/s43388-021-00058-x.
https://doi.org/10.1007/s43388-021-00058...
). The White-backed Stilt is distributed in southern Peru, Bolivia, Argentina, Paraguay, Chile and Uruguay. In Brazil, the species occurs in the midwest, southeast and southern regions (Sick, 1997Sick, H. 1997. Ornitologia Brasileira. Rio de Janeiro, Nova Fronteira.; Robinson et al., 2020Robinson, J.A.; Reed, J.M.; Skorupa, J.P. & Oring, L.W. 2020. Black-necked Stilt (Himantopus mexicanus), versão 1.0. In: Poole, A.F. & Gill, F.B. (Eds.). Birds of the World. Ithaca, Cornell Lab of Ornithology. https://doi.org/10.2173/bow.bknsti.01.
https://doi.org/10.2173/bow.bknsti.01...
). It was considered short-distance migratory in southern Brazil, as it nests inland and lives on coastal beaches during the non-breeding period, generally seen in flocks of dozens of individuals (Belton, 1984Belton, W. 1984. Birds of Rio Grande do Sul, Brazil, Part 1. Rheidae trought Furnariidae. Bulletin of the American Museum of Natural History, 178: 369-636.; Vooren & Brusque, 1999Vooren, C.M. & Brusque, L.F. 1999. As aves do ambiente costeiro do Brasil: biodiversidade e conservação. Rio Grande, Editora Sagra.). However, the White-backed Stilt is not listed as migratory or partially migratory in a comprehensive review of migratory birds in Brazil (Somenzari et al., 2018Somenzari, M.; Amara, P.P.L; Cueto, V.R.; Guaraldo, A.C.; Jahn, A.E.; Lima, D.M.; Lima, P.C.; Lugarini, C.; Machado, C.G.; Martinez, J.; Nascimento, J.L.X.; Pacheco, J.F.; Paludo, D.; Prestes, N.P.; Serafini, P.P.; Silveira, L.F.; Sousa, A.E.B.A.; Sousa, N.A.; Souza, M.A.; Telino-Júnior, W.R. & Whitney, B.M. 2018. An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia, 58(3): 1-66. e20185803. https://doi.org/10.11606/1807-0205/2018.58.03.
https://doi.org/10.11606/1807-0205/2018....
; Jahn et al., 2020Jahn, A.E.; Cueto, V.R.; Fontana, C.S.; Guaraldo, A.C.; Levey, D.J.; Marra, P.P. & Ryder, T.B. 2020. Bird migration within the Neotropics. The Auk, 137: 1-23.).

Recurvirostrids nest in colonies (Nicholson, 1929Nicholson, D.J. 1929. The breeding range of the Black-necked Stilt. The Wilson Bulletin, 41(4): 248-249.; Hamilton, 1975Hamilton, R.B. 1975. Comparative behavior of the American Avocet and the Black-Necked Stilt (Recurvirostridae). Ornithological Monographs, 1: 1-98.) and build their nests on the ground. The White-backed Stilt breeds on the muddy shores of lakes, lagoons, swamps, mangroves, rice paddies, estuaries, and river and sea beaches (Sick, 1997Sick, H. 1997. Ornitologia Brasileira. Rio de Janeiro, Nova Fronteira.; Vooren & Brusque, 1999Vooren, C.M. & Brusque, L.F. 1999. As aves do ambiente costeiro do Brasil: biodiversidade e conservação. Rio Grande, Editora Sagra.; Sigrist, 2009Sigrist, T. 2009. Guia de campo, avifauna brasileira: The avis brasilis field guide to the birds of Brazil. São Paulo, Editora Avis Brasilis. 2v.). The species breeding areas are little known in Brazil, as well as their breeding period, characterization and biometry of eggs and nests have not been described. In the literature, the nests of the species were previously recorded in Guarapiranga, SP, in 2007 (Schunck et al., 2016Schunck, F.; Melo, M.A.; Sanches, L.A.; Godoy, F.I.; Martins, G.G.; Mix, P. 2016. Avifauna do Parque Ecológico do Guarapiranga e sua importância para a conservação das aves da Região Metropolitana de São Paulo. Ornithologia, 9: 35-57.) and in Quissamã, on the northern coast of the Rio de Janeiro state (Tavares & Siciliano, 2013Tavares, D.C. & Siciliano, S. 2013. An inventory of wetland non-passerine birds along a southeastern Brazilian coastal area. Journal of Threatened Taxa, 5(11): 4586-4597.). Breeding records of its cogeneric species (H. mexicanus) were reported in Rio Grande do Norte (Lunardi et al., 2015Lunardi, V.O.; Mendonça, M.L.A.; Elias, A.P.R. & Lunardi, D.G. 2015. First record of a breeding colony of Black-necked Stilt Himantopus mexicanus (Aves: Recurvirostridae) in northeastern Brazil. Brazilian Journal of Biology, 75(4): 259-261.; Mendonça et al., 2019Mendonça, M.L.A.; Elias, A.P.R.; Lunardi, D.G. & Lunardi, V.O. 2019. Four-years of monitoring a breeding colony of Black-necked Stilt (Himantopus mexicanus) on the Rio Grande do Norte State coast. Brazilian Journal of Biology, 79: 158-161.) and on the northern coast of Bahia (Santos & Lima, 2004Santos, S.S. & Lima, P.C. 2004. Ensaio fotográfico sobre o comportamento reprodutivo do pernalonga Himantopus himantopus mexicanus (Muller, 1776). Atualidades Ornitológicas (Impresso), 120: 1-28.).

Literature and online plataforms (WikiAves, E-bird) review has been widely used to update information of birds species occurrence (Martínez-Curci et al., 2014Martínez-Curci, N.S.; Azpiroz, A.B.; Gianuca, A.T.; Gianuca, D.; Simpson, R.E. & Dias, R.A. 2014. Willet (Tringa semipalmata) status update in southeastern South America. Ornitologia Neotropical, 25: 135-144.; Frias et al., 2020aFrias, R.T.; Porto, L.R.M.; Fischer, L.G. & Mancini, P.L. 2020a. New record and occurrence review of Jabiru mycteria (Ciconiidae) in Rio de Janeiro state, Brazil. Pan-American Journal of Aquatic Sciences, 15(1): 49-53.; Barbosa et al., 2021Barbosa, R.A.P.; Teixeira, D.C.; Albino, A.M.; Nascimento, W.S.P.; Dutra, R.S.S.; Sousa, A.A.; Oliveira, M.A. & Prestes, A.L.C. 2021. First record of Fulvous Whistling-duck, Dendrocygna bicolor (Vieillot, 1816) (Anseriformes, Anatidae), in the Rondônia state, Brazil. Check List, 17(5): 1261-1264. https://doi.org/10.15560/17.5.126.
https://doi.org/10.15560/17.5.126...
; Pinheiro et al., 2021Pinheiro, L.V.S.; Cerqueira, P.V.; Leite, G.A.M.; Fialho, S. & Gonsioroski, G. 2021. Primeiro registro documentado de Leucopternis melanops (Latham, 1790) (Aves: Accipitridae) no estado do Maranhão e atualização da distribuição geográfica da espécie no Brasil. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais, 16(1): 131-143. https://doi.org/10.46357/bcnaturais.v16i1.450.
https://doi.org/10.46357/bcnaturais.v16i...
; Kaiser et al., 2022Kaiser, S.M.; Goncalves, J.M.A. & Perelló, L.F.C. 2022. Turismo de observação de aves no PN Lagoa do Peixe: oportunidades ou ameaças? Revista Brasileira de Ecoturismo (RBEcotur), 15(1): 9-24. https://doi.org/10.34024/rbecotur.2022.v15.11994.
https://doi.org/10.34024/rbecotur.2022.v...
), breeding (Scherer et al., 2013Scherer, A.L; Scherer, J.F.M. & Petry, M.V. 2013. North wintering distribution, habitat use and reproduction of the Two-banded Plover (Charadrius falklandicus) in Brazil. Oecologia Australis, 17(4): 522-526.; Guilherme & Lima, 2020Guilherme, E. & Lima, J. 2020. Breeding biology and morphometrics of Common Pauraque Nyctidromus a. albicollis in south-west Amazonia, and the species’ breeding season and clutch size in Brazil. Bulletin of the British Ornithologists Club, 140(3): 344-350. https://doi.org/10.25226/bboc.v140i3.2020.a7.
https://doi.org/10.25226/bboc.v140i3.202...
; Tubelis, 2020Tubelis, D.P. 2020. Breeding biology of the Horned Screamer (Anhima cornuta) in non-protected areas in the Brazilian Cerrado, Ornithology Research, 28: 115-124.; Tubelis & Sazima, 2020Tubelis, D.P. & Sazima, I. 2020. Biologia reprodutiva do carão, Aramus guarauna (Gruiformes: Aramidae), no Pantanal brasileiro, com uso de dados da ciência-cidadã. Atualidades Ornitológicas, 215.; Frias et al., 2020bFrias, R.T.; Porto, L.R.M.; Fischer, L.G. & Mancini, P.L. 2020b. Breeding review of Gray-hooded Gull Chroicocephalus cirrocephalus in Brazil with contributions on nests and egg biometry. Papéis Avulsos de Zoologia, 60(60): 1-6, e20206060.; Alexandrino et al., 2022Alexandrino, E.R.; Silva, G.A.; Corbo, M.C.; Demuner, B.A. & Szabo, J.K. 2022. Urban southern house wren (Troglodytes aedon musculus) nesting in apparently unsuitable human-made structures: Is it worth it? Ornitología Neotropical, 33: 44-52.), and migration (Schubert et al., 2019Schubert, C.; Manica, L.T. & Guaraldo, A.C. 2019. Revealing the potential of a huge citizen-science platform to study bird migration Stephanie. Emu - Ornitologia Austral, 1-10. https://doi.org/10.1080/01584197.2019.1609340.
https://doi.org/10.1080/01584197.2019.16...
; Degroote et al., 2020DeGroote, L.W.; Hingst-Zaher, E.; Moreira-Lima, L.; Whitacre, J.V.; Slyder, J.B. & Wenzel, J.W. 2020. Dados da ciência cidadã revelam a migração enigmática do Poto Comum Nyctibius griseus no Brasil. Ibis, 163(2): 380-389. https://doi.org/10.1111/ibi.12904.
https://doi.org/10.1111/ibi.12904...
).

This study reviewed breeding records of the White-backed Stilt in Brazil compiled from literature review (scientific articles) and online platforms (WikiAves and eBird), from 1997 to April 2022. Furthermore, a local case study of breeding aspects and the identification of main threats to the species were carried out in Restinga of Jurubatiba National Park (RJNP), in the north coast of Rio de Janeiro state. These are essential information that may contribute to habitat management for species conservation, especially in protected areas as RJNP.

MATERIAL AND METHODS

Study area

The study area comprises the RJNP and its surroundings (Table 1), about 20 meters from the park’s edge, called “Adjacent area”. RJNP has 18 coastal lagoons, and is 44 km long, 2 to 4 km wide, totaling around 15,000 hectares, encompassing the municipalities of Macaé, Carapebus and Quissamã in the north coast of Rio de Janeiro state (Fig. 1). Restingas are characteristic habitats of the Atlantic Forest, located in coastal lowlands. They are composed of dunes and sandy ridges of recent formation, existing along thousands of kilometers of the Brazilian coast and with characteristic herbaceous plants (Rocha et al., 2004Rocha, C.F.D.; Bergallo, H.G.; Alves, M.A.S. & Sluys, M.V. 2004. A Restinga de Jurubatiba e a Conservação dos ambientes de restinga do Estado do Rio de Janeiro. In: Rocha, C.F.D.; Esteves, F.A. & Scarano, F.R. (Eds.). Pesquisas ecológicas de longa duração na restinga de Jurubatiba. Ecologia, História Natural e Conservação. São Carlos, RiMA. p. 341-352.). In the Rio de Janeiro state, few restinga areas are in protected areas and, among them, the RJNP is considered the largest restinga of the state and one of the largest in Brazil (Rocha et al., 2004Rocha, C.F.D.; Bergallo, H.G.; Alves, M.A.S. & Sluys, M.V. 2004. A Restinga de Jurubatiba e a Conservação dos ambientes de restinga do Estado do Rio de Janeiro. In: Rocha, C.F.D.; Esteves, F.A. & Scarano, F.R. (Eds.). Pesquisas ecológicas de longa duração na restinga de Jurubatiba. Ecologia, História Natural e Conservação. São Carlos, RiMA. p. 341-352.). However, all restingas are Permanent Preserved Areas according to Brazilian Forest Code (Law 12651/2012). The climate in the region is warm (annual average of 24℃) and rainy (35 and 180 mm), with the dry season in autumn and winter (Fischer et al., 2007Fischer, C.F.; Nunes, M.F.S.Q.C. & Campos, D.P. 2007. Contextualização da Unidade de Conservação: Plano de Manejo do Parque Nacional Restinga de Jurubatiba. Rio de Janeiro, Encarte. 670p.).

Figure 1
Breeding records of White-backed Stilt Himantopus melanurus in Brazil (WikiAves - blue, eBird - orange and literature - yellow, Table 2) and this study area (red) with colonies identified in the Restinga de Jurubatiba National Park and adjacent area, in 2018, 2019 and 2020, in the northern coast of Rio de Janeiro state. *Colonies: 1 = Visgueiro/2018; 2 = Maria Menina/2018; 3 = Robalo/2018; 4 = Ubatuba/2019; 5 = Visgueiro/2020; 6 = Adjacent Area/2020.

Table 1
Characterization of areas (lagoons) with colonies of the species White-backed Stilt Himantopus melanurus in Restinga of Jurubatiba National Park and adjacent area.

RJNP preserves sandbank and restinga habitats (Rocha et al., 2004Rocha, C.F.D.; Bergallo, H.G.; Alves, M.A.S. & Sluys, M.V. 2004. A Restinga de Jurubatiba e a Conservação dos ambientes de restinga do Estado do Rio de Janeiro. In: Rocha, C.F.D.; Esteves, F.A. & Scarano, F.R. (Eds.). Pesquisas ecológicas de longa duração na restinga de Jurubatiba. Ecologia, História Natural e Conservação. São Carlos, RiMA. p. 341-352.). However, it has some environmental conflicts, such as subsistence fishing, domestic effluents dumping in some lagoons, lack of sewage treatment plant in the Park area in Quissamã, agricultural and livestock activities (ICMBio, 2007Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2007. Plano de Manejo do Parque Nacional da Restinga de Jurubatiba: Contextualização da Unidade de Conservação. Rio de Janeiro, Ministério do Meio Ambiente.).

Secondary data compilation

Search in scientific literature (scientific articles) and online platforms were carried out. For literature review it was used the following keywords in Google Academic: “Breeding”, “reproduction”, “biometry”, “life history”, “Himantopus melanurus”, “Himantopus himantopus mexicanus” and “Himantopus mexicanus”. On WikiAves (https://www.wikiaves.com/buscaavancada.php), an advanced search was carried out based on the species name (Himantopus melanurus) + photo content (egg; nest); or age (chicks) or observed action (mating; hatching; feeding the chicks; building the nest). We carefully check to avoid duplicate record of species breeding. On eBird, photos of the species were searched with the filter “reproducing” and all actions present, “age” - juvenile. The last search on online platforms was on April 18, 2022.

Field sampling

Two expeditions per month were carried out in eight RJNP lagoons: Garças, Maria Menina, Robalo, Visgueiro, Catingosa, Pires, Barrinha, Casa Velha, Ubatuba and adjacent area (temporary wetlands, see details in “study area” section, Table 1). Observations were carried out between 07:00 and 15:00, totaling 25 h in the field in 13 days of observations (Table S1).

The identification of White-backed Stilt colonies was done through active search in areas with many individuals or when they were seen incubating. The sighting was carried out by two observers with the aid of binoculars (Nikon Prostaff 10 × 42) and spottingscope (Celestron 22-66 × 100). Nests were approached when the adult birds were not close. Each nest was marked with a numbered label, photographed (Nikon P600) and geo-referenced (ViewRanger App). Searches and sampling occurred in September and December 2018, monthly in 2019, and between January to March and September to December in 2020. After identifying the colonies, weekly expeditions were carried out during September and October, which comprised the breeding period at the sites between 2018 and 2020. For each nest in the colonies were recorded: (i) type of nesting microhabitat; (ii) distance between the nest and the edge of the water body; (iii) distance from the next closest nest; (iv) types of materials used to build the nest; (v) outer and inner diameter of the nest; (vi) number, height and width of eggs (according Pinho & Marini, 2014Pinho, J.B. & Marini, M.A. 2014. Birds nesting parameters in four forest types in the Pantanal wetland. Brazilian Journal of Biology, 74(4): 890-898. https://doi.org/10.1590/1519-6984.08713.
https://doi.org/10.1590/1519-6984.08713...
; Mendonça et al., 2019Mendonça, M.L.A.; Elias, A.P.R.; Lunardi, D.G. & Lunardi, V.O. 2019. Four-years of monitoring a breeding colony of Black-necked Stilt (Himantopus mexicanus) on the Rio Grande do Norte State coast. Brazilian Journal of Biology, 79: 158-161.). Egg measurements were performed with a caliper rule (accuracy of 0.01 mm) and nest measurements were made with a tape measure and ruler (accuracy of 1 mm). Each registered nest was identified with a numbered blue tag. The nests were classified as: (i) active nest (with an egg and without hatching or predation traces), (ii) predated nest (when at least one egg was damaged or had disappeared, and/or when predator footprints were close to the nest), and (iii) successful nest (presence of at least one chick inside or close to the nest) (Fonseca, 2013Fonseca, D.M.L.A. 2013. Seleção de habitat e conservação de aves nidificantes nas salinas do Samouco. Dissertação (Mestrado em Biologia) - Universidade de Coimbra, Coimbra.).

Data analysis

The biometric parameters of nests and eggs were compared between colonies through analysis of variance to identify potential differences. Only colonies with more than three nests (colonies 1, 2, 3 and 4) were tested. Data normality and homoscedasticity were evaluated by the Shapiro-Wilk and Levene tests, respectively. For the parametric data (outer diameter of the nests), One-Way ANOVA was used, followed by the Tukey test. For the non-parametric data (nest height and internal diameter; distance from water; distance from the closest nest; height and width of eggs), the Kruskal-Wallis and Dunn tests were performed, adjusted with the Holm method. Tests were considered significant when p < 0.05. One-Way ANOVA and Mann-Whitney were used to evaluated if the distance from water and distance from the closest nest differed between “successful” and “not successful” nests. R software and the FSA package were used in all analysis (Ogle & Wheeler, 2020Ogle, D.H.P. & Wheeler, A.D. 2020. FSA: Fisheries Stock Analysis . R package version 0.8.31. https://github.com/droglenc/FSA.
https://github.com/droglenc/FSA...
). The relative frequency of occurrence of the materials used to build the nests was calculated summing the total number of nests with a certain material used, divided by the total number of nests, and multiplied by 100.

RESULTS

Literature review and online searches

In the literature, only two studies recorded nests and/or nestlings of H. melanurus in Guarapiranga, SP in 2007 (Schunck et al., 2016Schunck, F.; Melo, M.A.; Sanches, L.A.; Godoy, F.I.; Martins, G.G.; Mix, P. 2016. Avifauna do Parque Ecológico do Guarapiranga e sua importância para a conservação das aves da Região Metropolitana de São Paulo. Ornithologia, 9: 35-57.) and in Rio de Janeiro in 2012 (Tavares & Siciliano, 2013Tavares, D.C. & Siciliano, S. 2013. An inventory of wetland non-passerine birds along a southeastern Brazilian coastal area. Journal of Threatened Taxa, 5(11): 4586-4597.), but none described breeding details of the species in Brazil (Table 2). The record of Schunck et al., (2016Schunck, F.; Melo, M.A.; Sanches, L.A.; Godoy, F.I.; Martins, G.G.; Mix, P. 2016. Avifauna do Parque Ecológico do Guarapiranga e sua importância para a conservação das aves da Região Metropolitana de São Paulo. Ornithologia, 9: 35-57.) was also in the WikiAves platform, so we considered it only one time as literature review.

Table 2
Breeding records of the White-backed Stilt (Himantopus melanurus) on WikiAves, eBird and literature. Local (municipallity and state): RS = Rio Grande do Sul; SP = São Paulo; MG = Minas Gerais; SC = Santa Catarina; PR = Paraná; RJ = Rio de Janeiro; GO = Goiás; RO = Rondônia Records listed chronologically from 1997 to 2021. NA = Not applicable. * = Same record on literature and WikiAves.

On WikiAves and eBird 68 breeding records of the species were found in Brazil, between 1997 and November 2021 (Table 2, Fig. 1). These records were concentrated mainly in the south (n = 29) and southeast (n = 28), in addition to six in the midwest (Goiás), one in the northeast (Bahia), and one in the north (Rondônia). The breeding period in almost all regions was similar to this study, except in Rio de Janeiro state (Cabo Frio in March, and Campos dos Goytacazes and São Pedro da Aldeia in May). Nearly 90% of breeding records occurred between August and November (Table 2).

Field sampling

In RJNP and adjacent area, six colonies were identified between 2018 and 2020 in Visgueiro, Maria Menina, Robalo, Ubatuba lagoons, and adjacent area (Fig. 1, Table 3). Only in Visgueiro two colonies were registered in different years (2018 and 2020). Overall, 44 nests of the species were identified, being 34 active.

Table 3
Biometry of the nests of the White-backed Stilt Himantopus melanurus registered in the Restinga of Jurubatiba National Park and adjacent area. *Colony 1: Visgueiro/2018; Colony 2: Maria Menina/2018; Colony 3: Robalo/2018; Colony 4: Ubatuba/2019; Colony 5: Visgueiro/2020; Colony 6: Adjacent Area/2020. N = Number of nests. DCN = Distance from closest nest; DW = Distance from water; ODN = Outer diameter of the nest; ID = Internal diameter; HN = Height of the nest. Mean ± standard deviation; (min-max. value).

The breeding season of the species in the colonies occurred mainly in September and October 2018, 2019, and 2020. In 2018, during these months, 32 nests were registered. In 2019, seven nests and in 2020 five nests in September were observed (Table 3). In July 2019, one single nest was identified on an islet in the middle of a flooded, in an inaccessible area.

Most of the nests (95%) were built on the ground, close to water. Nests biometry and measurements parameter in each colony are shown in Table 3. The outer diameter of the nest did not differ significantly between colonies (ANOVA, F = 0.099; p = 0.755), neither did the internal diameter (Kruskal-Wallis X² = 2.891, p = 0.408). Nest height differed among colonies (Kruskal-Wallis X² = 20.805, p = 0.001), with higher nests in colony 4 (Dunn Test, p < 0.05) (Table 4), which the highest average height of 20.5 cm.

Table 4
Dunn test results, pairwise comparisons in relation to nest height, distance from water and distance to the closest nest in colonies recorded in the Restinga of Jurubatiba National Park and adjacent area. Z = Z test statistic values for each comparison; P.unadj = unadjusted p-values for each comparison; P.adj = Adjusted p values for each comparison. * = Significant difference.

The nest distance from water also differed between colonies (Kruskal-Wallis X² = 27,138, p = 5.5*10-6) and all comparisons showed significant differences (Dunn Test, p < 0.005) (Tables 3 and 4). Colonies 1 and 2, for example, had different distances from the water, 26 cm and 3.1 cm, respectively. The distances of the closest nests were different (Kruskal-Wallis X² = 8.1176, p = 0.043), and only colony 3 differed from colony 4 (Dunn Test, p = 0.035) (Table 4).

Different materials were used in to build the nests, such as saltmarsh plant Sesuvium portulacastrum L., grass, mud, shells; and cattle feces (Figs. 2 and 3).

Figure 2
Nests of White-backed Stilt Himantopus melanurus monitored in Restinga de Jurubatiba National Park and adjacent area. A = Nest built with saltmarsh plant Sesuvium portulacastrum L. and suspended over cattle feces; B = Nest with dry saltmarsh plant and mud fragments; C = Nest with shells, saltmarsh plant and mud; D = Nest with mud and dry saltmarsh plant fragments. Photos: Lucas R.M. Porto.

Figure 3
Frequency of occurrence of the materials used to build the nests of the White-backed Stilt Himantopus melanurus in the Restinga de Jurubatiba National Park and adjacent area.

Thirty-five nests (79%) had the saltmarsh plant as one of the main items, in addition to mud in a smaller proportion (34%). Within the shell group, gastropods represented 5% (Fig. 3).

In total 118 eggs were registered in the 34 active nests of the six colonies. Twenty-six nests contained four eggs, three nests had three eggs, two nests had two eggs, and three nests had only one egg. Eggs biometry are in Table 5. Egg height did not differ between colonies (Kruskal-Wallis X² = 8.482, p = 0.131), however there was a difference in egg width (Kruskal-Wallis X² = 16.848, p = 0.004), between colony 4 and colonies 1 and 6 (4 and 1, Dunn Test, p = 0.014) (4 and 6, Dunn Test, p = 0.006) (Table 6).

Table 5
Biometry of eggs of the White-backed Stilt (Himantopus melanurus) recorded in the Restinga de Jurubatiba National Park and adjacent area. Mean ± standard deviation; (min-max. value). *N = number of eggs; EH = eggs height; EW = eggs width.

Table 6
Result of the Dunn Test, pairwise comparisons, in relation to egg width, of colonies in the Restinga of Jurubatiba National Park and adjacent area. Z = Values the Z-test statistic for each comparison; P.unadj = unadjusted p-values for each comparison; P.adj = Adjusted p values for each comparison. * = Significant difference.

Egg predation was identified in 21 active nests (61.7%, Fig. 4). During monitoring, footprints of wild animals such as the crab-eating foxes Cerdocyon thous Linnaeus, 1766, crab-eating raccoon Procyon cancrivorus (Cuvier, 1798) and domestic animals (cattle and domestic dog) were recorded close to the nests (Fig. 5). Besides predation, two nests (5.8%) were trampled by cattle and two other nests were flooded.

Figure 4
Predated/degraded eggs of White-backed Stilt Himantopus melanurus in Restinga de Jurubatiba National Park in October 2018. A, B and C: Colony 1 (Visgueiro), D: Colony 2 (Maria Menina). Photos: Lucas R.M. Porto.

Of the 34 active nests monitored, nine (26.4%) were successful, as there was a record of egg hatching or chicks close to the nest (Fig. 6), two in colonies 1 and 2, and three in colony 4. Successful and unsuccessful nests had no significant differences for the parameters analyzed: outer diameter of the nest (ANOVA, F = 1.477; p = 0.231), internal diameter (Man-Whitney U = 115; p = 0.308), nest height (ManWhitney U = 127; p = 0.517), and the distance from the water (Man-Whitney U = .101; p = 0.618). However, in the distance to the closest nest, there was a significant difference (Man-Whitney U = 9.5; p < 0.005).

Figure 5
Footprints records of possible predators and cattle trampling near nests of White-backed Stilt Himantopus melanurus in Restinga de Jurubatiba National Park. (A) Footprints of domestic dogs and trampling of cattle in the Visgueiro lagoon (2018). (B) crab-eating fox (Cerdocyon thous) footprints, and (C) crab-eating raccoon (Procyon cancrivorus) footprints in adjacent area (2020). Photos: Lucas R.M. Porto.

Figure 6
Successful nesting records of the White-backed Stilt Himantopus melanurus in Restinga de Jurubatiba National Park and adjacent area. (A) White-backed Stilt chicks found in Visgueiro lagoon (September 2018); (B) Hatchling and eggs in the Maria Menina Lagoon (October 2018); (C and D) Chicks in the nests in Ubatuba lagoon (September 2019). Photos: Lucas R.M. Porto.

DISCUSSION

On Wikiaves, 90% of breeding records of the White-backed Stilt were from August to November. Based in the WikiAves records, the main breeding areas of the species are concentrated in the southeast and south, which corroborates with literature (Belton, 1984Belton, W. 1984. Birds of Rio Grande do Sul, Brazil, Part 1. Rheidae trought Furnariidae. Bulletin of the American Museum of Natural History, 178: 369-636.; Lima et al., 2009Lima, L.M.; Pacheco, J.F.; Alves, V.S.; Soares, A.B.A.; Couto, G.S.; Siciliano, S.; Tavares, D.C.; Serpa, G.A. & Rennó, B.M.E. 2009. O pernilongo-de-costas-brancas, revisão dos registros e novas observações Himantopus melanurus no Estado do Rio de Janeiro: (Charadriiformes: Recurvirostridae). Atualidades Ornitológicas, on-line, 147: 58-65.; Tavares & Siciliano, 2013Tavares, D.C. & Siciliano, S. 2013. An inventory of wetland non-passerine birds along a southeastern Brazilian coastal area. Journal of Threatened Taxa, 5(11): 4586-4597.). However, these data could be bias because southeast is the most populated region in the country, with great number of birdwatchers (n = 21935, 37%) and together with south region sums 53% of the observers registered in this platform (WikiAves, 2022A Enciclopédia das Aves do Brasil (WikiAves). 2022. [online] Available: Available: https://www.wikiaves.com.br/index.php . Access: 20/03/2022.
https://www.wikiaves.com.br/index.php...
). Species breeding records in other regions are reported for the first time, including the northeast (Bahia), midwest (Goiânia) and north (Rondônia). On eBird, the records in São Paulo state were in September and October, similar to the data recorded in the RJNP colony. The breeding period differences in some states may be linked to distinct rainfall regimes and consequently the availability of food resources.

The White-backed Stilt breeding in RJNP and adjacent area were recorded mainly between September and October. This period includes the dry season (June, July, August, September and October) in the northern region of Rio de Janeiro state. The dry season may also explain the nest recorded in July 2019 in this study, similar to the breeding record of the species in RJNP in June 2012 (Tavares & Siciliano, 2013Tavares, D.C. & Siciliano, S. 2013. An inventory of wetland non-passerine birds along a southeastern Brazilian coastal area. Journal of Threatened Taxa, 5(11): 4586-4597.). Water levels in wetlands are determined by a variety of factors including the effect of tides, river overflows and the level of local precipitation (Burger et al., 1977Burger, J.M.; Howe, D.H. & Chase, J. 1977. Effects of tide cycles on habitat selection and habitat partitioning by migrating shorebirds. The Auk, 94(4): 743-758.; Collazo et al., 2002Collazo, J.A.; O’harra, D.A. & Kelly, C.A. 2002. Accessible habitat for shorebirds: Factors influencing its availability and conservation implications. Waterbirds, 25: 13-24.). These factors determine the water depth in shorebird foraging areas, which affects both bird access to these areas and invertebrate abundance (Marín et al., 2006Marín, G.L.; Blanco, A.; Prieto, J.M. & Alzola, R. 2006. Dependencia de pequeñas lagunetas y charcas costeras para la avifauna residente y migratoria: Dos casos en Venezuela. Boletín del Instituto Oceanográfico de Venezuela, 45: 149-163.; Giner & Pérez-Emán, 2016Giner, S.B. & Pérez-Emán, J.L. 2016. Spatio-temporal dynamics of shorebird assemblages in coastal Falcon State, Venezuela. Acta Biologica Venezuelica, 36: 77-97.), influencing the availability of food resources and adequate breeding sites. These environmental conditions, together with the availability of exposed areas, influence the establishment of nesting areas for the species.

In 2018, 32 nests were recorded while in 2020 only five were found in the same area. Several factors may have influenced the species’ breeding in the area. In 2018, the annual average of rainfall (115 mm) was lower than in 2019 (128 mm) and 2020 (136 mm) (INMET, 2020Instituto Nacional de Meteorologia (INMET). 2020. [online] Available: Available: https://portal.inmet.gov.br . Access: 15/01/2020.
https://portal.inmet.gov.br...
). Open areas with a smaller flooded surface are essential for the establishment of breeding colonies, thus the higher rainfall may explain the differences in the number of nests between the sampling years (Hamilton, 1975Hamilton, R.B. 1975. Comparative behavior of the American Avocet and the Black-Necked Stilt (Recurvirostridae). Ornithological Monographs, 1: 1-98.). Only the Visgueiro lagoon was used in more than one breeding season (2018 and 2020). This lagoon has a larger and exposed lateral area, with muddy substrate and close to water, which is a favorable environment for the establishment of the species. Another possibility is that in 2019 and 2020 White-backed Stilt couples may have nested in different areas than those monitored. In 2020, the expedition occurred from January to March and September to December, thus only for seven months compare to 2019. The distances between the closest nests differed between colonies, mainly between colony 3 and 4. These differences can be explained because colony 4 is mixed with nests of the Gray-hooded Gull (Chroicocephalus cirrocephalus Swainson, 1837), where the nests were further apart. The spacing between Recurvirostridae nests varies between 5 and 30 m (Nicholson, 1929Nicholson, D.J. 1929. The breeding range of the Black-necked Stilt. The Wilson Bulletin, 41(4): 248-249.; Hamilton, 1975Hamilton, R.B. 1975. Comparative behavior of the American Avocet and the Black-Necked Stilt (Recurvirostridae). Ornithological Monographs, 1: 1-98.). No pattern was identified regarding the nest distribution in the colonies. They can be located close or far apart, according to habitat conditions (Gibson, 1920Gibson, E. 1920. Further ornithological notes from the neighborhood of Cape San Antonio, Province of Buenos Ayres. Ibis, 11: 1-97.), such as size of available area, availability of resources and number of breeding couples.

The distance between the nests and water differed significantly between colonies. Most of the nests were built on the ground around the lagoon, while in colony 4 there were nests built on the water. Proximity to water is often an important predictor of nest viability because, although water can make the presence of terrestrial predators more difficult, the further away from the water, the lower the risk of flooding (Cuervo, 1993Cuervo, J.J. 1993. Biología reproductiva de la avoceta (Recurvirostra avosetta) y la cigüeñuela (Himantopus himantopus) (Recurvirostridae, Aves) en el sur de España. Doctoral Thesis. Universidad Complutense de Madrid, Madrid.; Polak & Kasprzykowski, 2013Polak, M. & Kasprzykowski, Z. 2013. The effect of weather conditions on the breeding biology of the Eurasian Bittern Botaurus stellaris in eastern Poland. Ethology Ecology and Evolution, 25(3): 243-252.; Harmon et al., 2021Harmon, K.C.; Wehr, N.H. & Price, M.R. 2021. Seasonal patterns in nest survival of a subtropical wading bird, the Hawaiian Stilt (Himantopus mexicanus knudseni). PeerJ, 9: e10399.). Only two flooded nests were recorded in the study area. Regarding the height of the nests, the highest one was in colony 4 (Ubatuba, height = 27.5 cm) and was suspended over the water in a large tangle of vegetation. During this period (September and October 2019), the volume of water in the lagoon was increasing. Considering all colonies, the average nest height was 7.4 cm. The external and internal diameters of the nests were smaller than H. mexicanus nests (Lunardi et al., 2015Lunardi, V.O.; Mendonça, M.L.A.; Elias, A.P.R. & Lunardi, D.G. 2015. First record of a breeding colony of Black-necked Stilt Himantopus mexicanus (Aves: Recurvirostridae) in northeastern Brazil. Brazilian Journal of Biology, 75(4): 259-261.; Mendonça et al., 2019Mendonça, M.L.A.; Elias, A.P.R.; Lunardi, D.G. & Lunardi, V.O. 2019. Four-years of monitoring a breeding colony of Black-necked Stilt (Himantopus mexicanus) on the Rio Grande do Norte State coast. Brazilian Journal of Biology, 79: 158-161.). As in North America (Saito, 1975Saito, R.S. 1975. Field investigation of native Hawaiian waterbirds on the island of Oahu (S). Honolulu, Division for Wildlife.; Dinsmore, 1977Dinsmore, J.J. 1977. Notes on avocets and stilts in Tampa Bay, Florida. Florida Field Naturalist, 5: 25-30.; Coleman, 1981Coleman, R.A. 1981. The reproductive biology of the Hawaiian subspecies of the Black-necked Stilt, Himantopus mexicanus knudseni. Doctoral Thesis, Pennsylvania State University, University Park.; Grant, 1982Grant, G.S. 1982. Avian incubation: Egg temperature, nest humidity, and behavioral thermoregulation in a hot environment. Ornithological Monographs, 30.), such differences can be determined by the type of habitat and materials used in the construction of nests in each area.

White-backed Stilt nests on muddy soil or in very shallow waters, in open areas (Ridgely & Tudor, 2016Ridgely, R.S. & Tudor, G. 2016. “Plovers & Lapwings”. In: Wildlife Conservation Society Birds of Brazil. Ithaca, Cornell University Press, p. 114-118. https://doi.org/10.7591/9781501704307-031.
https://doi.org/10.7591/9781501704307-03...
), corroborating with this study. Several types of materials were used as nest structure, with the saltmarsh plant and mud being the most frequent. These materials were also abundant in the colonies areas and the saltmarsh plant is a native vegetation found in other wetlands, which the cogeneric species H. mexicanus breeds (Robinson et al., 2020Robinson, J.A.; Reed, J.M.; Skorupa, J.P. & Oring, L.W. 2020. Black-necked Stilt (Himantopus mexicanus), versão 1.0. In: Poole, A.F. & Gill, F.B. (Eds.). Birds of the World. Ithaca, Cornell Lab of Ornithology. https://doi.org/10.2173/bow.bknsti.01.
https://doi.org/10.2173/bow.bknsti.01...
). Nest composition for Recurvirostidae ranges from small, simple tangles with almost no material, to clumps of stems and branches (up to 40 cm high) (Wetmore, 1925Wetmore, A. 1925. Food of American phalaropes, avocets, and stilts. Bulletin of the US Department of Agriculture, 1359: 1-19.; Wheeler 1955Wheeler, R. 1955. Charadriiformes at the Laverton Saltworks, Victoria, 1950-1953. Emu, 55(4): 279-295.; von Frisch, 1961von Frisch, O. 1961. Zur Jugendentwicklung und Ethologie des Stelzenlaufers (Himantopus himantopus) und der Brachschwalbe (Glareola pratincola). Zeitschrift für Tierpsychologie, 18: 67-70.; Palmer, 1967Palmer, R.S. 1967. Plumage descriptions. In: Stout, G.D. (Ed.). The shorebirds of North America. New York, Viking Press. p. 139-267.). Sometimes, nests are built over a mound of vegetation, in water and on floating vegetation (Hamilton, 1975Hamilton, R.B. 1975. Comparative behavior of the American Avocet and the Black-Necked Stilt (Recurvirostridae). Ornithological Monographs, 1: 1-98.).

On average, the number of eggs per nest was four eggs, similar to H. mexicanus (Lunardi et al., 2015Lunardi, V.O.; Mendonça, M.L.A.; Elias, A.P.R. & Lunardi, D.G. 2015. First record of a breeding colony of Black-necked Stilt Himantopus mexicanus (Aves: Recurvirostridae) in northeastern Brazil. Brazilian Journal of Biology, 75(4): 259-261.). However Mendonça et al. (2019Mendonça, M.L.A.; Elias, A.P.R.; Lunardi, D.G. & Lunardi, V.O. 2019. Four-years of monitoring a breeding colony of Black-necked Stilt (Himantopus mexicanus) on the Rio Grande do Norte State coast. Brazilian Journal of Biology, 79: 158-161.), reported an average of three eggs in the Apodi-Mossoró River estuary, Rio Grande do Norte. Overall, nests are composed of 3-4 eggs for the genus Himantopus (Gibson, 1920Gibson, E. 1920. Further ornithological notes from the neighborhood of Cape San Antonio, Province of Buenos Ayres. Ibis, 11: 1-97.; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. Rio de Janeiro, Nova Fronteira.). The eggs of Recurvirostrids, on average measure 4.5 × 3.3 cm, in height and width, respectively (Gibson, 1920Gibson, E. 1920. Further ornithological notes from the neighborhood of Cape San Antonio, Province of Buenos Ayres. Ibis, 11: 1-97.), values similar to those recorded in this study. The diameter of the eggs, considering all colonies, had an average similar to H. mexicanus, (3.1 cm) (Lunardi et al., 2015Lunardi, V.O.; Mendonça, M.L.A.; Elias, A.P.R. & Lunardi, D.G. 2015. First record of a breeding colony of Black-necked Stilt Himantopus mexicanus (Aves: Recurvirostridae) in northeastern Brazil. Brazilian Journal of Biology, 75(4): 259-261.), and different considering the other study (2.8 cm) (Mendonça et al., 2019Mendonça, M.L.A.; Elias, A.P.R.; Lunardi, D.G. & Lunardi, V.O. 2019. Four-years of monitoring a breeding colony of Black-necked Stilt (Himantopus mexicanus) on the Rio Grande do Norte State coast. Brazilian Journal of Biology, 79: 158-161.).

Predation and trampling by cattle seem to be the main threats to the species’ nesting in RJNP and in the adjacent area. The Maria Menina and Visgueiro lagoons are close to urbanized areas, where there are domestic animals, such as dogs (Canis familiaris). Furthermore, tracks of natural predators such as crab-eating fox and raccoon were recorded close to the nests. The main predators of Recurvirostrid eggs are terrestrial vertebrates, which can either ingest the eggs (dogs, snakes) or trample them (cattle and horses) (Cuervo, 1993Cuervo, J.J. 1993. Biología reproductiva de la avoceta (Recurvirostra avosetta) y la cigüeñuela (Himantopus himantopus) (Recurvirostridae, Aves) en el sur de España. Doctoral Thesis. Universidad Complutense de Madrid, Madrid.; Arroyo, 2000Arroyo, G.M. 2000. Influencia de las transformaciones humanas de hábitats costeiros supralitorales sobre la ecología de la reproducción de la cigüeñuela Himantopus himantopus y la avoceta Recurvirostra avosetta (Aves: Recurvirostridae) en la Bahía de Cádiz: aplicación a la gestión de espacios naturales protegidos. PhD Thesis, Puerto Real, Spain, University of Cádiz.). In addition to mammals and reptiles, some birds also prey on eggs and chicks, such as herons, vultures and falcons that are abundant in the area (Teunissen et al., 2008Teunissen, W.; Schekkerman, H.; Willems, F. & Majoor, F. 2008. Identifying predators of eggs and chicks of Lapwing Vanellus vanellus and Black-tailed Godwit Limosa limosa in the Netherlands and the importance of predation on wader reproductive output. Ibis, 150(Suppl. 1): 74-85.; Andrade et al., 2020Andrade, L.P.; Lyra-Neves, R.M.; Andrade, H.M.L.S.; Albuquerque, U.P.; Siqueira, A.J.S.; Guzzic, A. & Telino-Júnior, W.R. 2020. Records of breeding in Wilson’s Plover Charadrius wilsonia with new localities for Brazil. Brazilian Journal of Biology, 80(1): 81-86.; Canabarro & Fedrizzi, 2010Canabarro, P.L. & Fedrizzi, C.E. 2010. Aspectos da reprodução do piru-piru Haematopus palliatus (Charadriiformes: Haematopodidae) na Praia do Hermenegildo, Rio Grande do Sul, Brasil. Revista Brasileira de Ornitologia, 18(3): 249-255.; Frias et al., 2020bFrias, R.T.; Porto, L.R.M.; Fischer, L.G. & Mancini, P.L. 2020b. Breeding review of Gray-hooded Gull Chroicocephalus cirrocephalus in Brazil with contributions on nests and egg biometry. Papéis Avulsos de Zoologia, 60(60): 1-6, e20206060.). Despite the high number of preyed nests, about a quarter of them (26%) were successful, considering hatched eggs. The characteristics of successful and unsuccessful nests did not differ, only the distance between the closest nests. The average distance between the nests was greater for the successful ones (22 m) with a maximum distance of 34 m. Breeding neighbors are known to reduce predator pressure on waterbird species, both because of their occupation of nearby space (dilution effect), and in the case of nest-defending species, because of their defensive behavior against predators (Brzeziński et al., 2018Brzeziński, M.; Chibowski, P.; Gornia, J.; Górecki, G. & Zalewski, A. 2018. Spatio-temporal variation in nesting success of colonial waterbirds under the impact of a non-native invasive predator. Oecologia, 188(4): 1037-1047. https://doi.org/10.1007/s00442-018-4270-8.
https://doi.org/10.1007/s00442-018-4270-...
). In this study, colonies were relatively small and nests were rarely very close (smallest distance was 1.7 m). However, it is not clear whether colonial breeding always reduces predation, there may be a negative relationship between nest predation risk and colony aggregation or size (Varela et al., 2007Varela, S.A.M.; Danchin, E. & Wagner, R.H. 2007. Does predation select for or against avian coloniality? A comparative analysis. Journal of Evolutionary Biology, 20(4): 1490-503.), but some studies have found differences (Rolland et al., 1998Rolland, C.; Danchin, E. & Fraipont, D.E.M. 1998. The evolution of coloniality in birds in relation to food, habitat, predation, and life-history traits: a comparative analysis. The American Naturalist, 151: 514-529., Picman et al., 2002Picman, J.; Pribil, S. & Isabelle, A. 2002. Antipredation value of colonial nesting in Yellow-headed Blackbirds. The Auk, 119(2): 461-472.).

Due to the human occupation of the coastal zone, natural breeding areas for the White-backed Stilt and several other shorebird species have been constantly destroyed (Weber et al., 1999Weber, T.P.; Houston, A.I. & Ens, B. 1999. Consequences of habitat loss migratory stopover sites: a theoretical investigation. Journal of Avian Biology, 30(4): 416-426.; Rais et al., 2010Rais, M.; Kabeer, B.; Anwar, M & Mehmood, T. 2010. Efect of habitat degradation on breeding water birds at kallar kahar lake district chakwalj. The Journal of Animal & Plant Sciences, 20(4): 318-320.). Livestock is one of the main activities responsible for the destruction of breeding areas for many shorebird species (Powers & Glimp, 1996Powers, L.C. & Glimp, H.A. 1996. Impacts of livestock on shorebirds: A review and application to shorebirds of the western Great Basin. International Wader Studies, 9: 55-63.). As a result, shorebird species have sought alternative breeding habitats such as rice fields, pastures and artificial salt pans in some locations (Masero, 2003Masero, J.A. 2003. Avaliação de habitats antropogênicos alternativos para a conservação de aves aquáticas: salinas como áreas tampão contra o impacto da perda de habitat natural para aves limícolas. Conservação da Biodiversidade, 12: 1157-1173.; Dias, 2009Dias, M.P. 2009. Use of Salt Ponds by Wintering Shorebirds throughout the Tidal Cycle. Waterbirds, 32(4): 531-537.; Rocha et al., 2016Rocha, A.D.; Fonseca, D.; Masero, J.A. & Ramos, J.A. 2016. Coastal saltpans are a good alternative breeding habitat for Kentish plover Charadrius alexandrinus when umbrella species are present. Journal of Avian Biology, 47: 1-10.; Barnagaud et al., 2019Barnagaud, J.Y.; Papaïxb, J.; Audevardc, A.; Lascèved, M.; Wrozaa, S. & Geoffroye, D. 2019. Interspecific variations in shorebird responses to management practices on protected Mediterranean saltpans. Biological Conservation, 237: 470-479.). Nest trampling by cattle was recorded as another impact for the species, affecting two nests in the Visgueiro lagoon (colony 1, 2018) and has already been observed previously in other species, in Long-billed Curlew Numenius americanus (Gregory et al., 2011Gregory, C.J.; Dinsmore, S.J.; Powell, L.A. & Jorgensen, J.G. 2011. Nest survival of Long-billed Curlew in Nebraska. Wader Study Group Bulletin, 118: 109-113.), Calidris alpina schinzii (Pakanen et al., 2011Pakanen, V.M.; Luukkonen, A. & Koivula, K. 2011. Nest predation and trampling as management risks in grazed coastal meadows. Biodiversity and Conservation, 20(9): 2057-2073.), Tringa totanusa (Sharps et al., 2017Sharps, E.; Smart, J.; Mason, L.R.; Jones, K.; Martin, W.; Skov, A. Garbutt. & Hiddink, J.G. 2017. Nest trampling and ground nesting birds: Quantifying temporal and spatial overlap between cattle activity and breeding redshank. Ecology and Evolution, 7(16): 6622-6633.), Bartramia longicauda (Bowen & Kruse, 1993Bowen, B.S. & Kruse, A.D. 1993. Effects of grazing on nesting by upland sandpipers in southcentral North Dakota. The Journal of Wildlife Management, 57(2): 291-30.). In addition, two nests built on feces and inside cattle tracks were observed at the same site. Some advantages of building the nests on the feces are: (1) increase in the nest temperature when unprotected by the parents; (2) increase of the height of the nest reducing potential flooding; and (3) “disguising” nests from predators, due to feces color and odor (Grau, 1975Grau, W.D. 1975. Breeding Biology of the Mountain Plover. The Wilson Bulletin, 87(1): 6-3.). Cattle grazing may also favor shorebird species in other aspects during breeding, decreasing vegetation height and facilitating foraging, and may allow birds to better see predators (Colwell & Dodd, 1995Colwell, M.A. & Dodd, S.L. 1995. Waterbird communities and habitat relationships in coastal pastures of northern California. Conservation Biology, 9(4): 827-834.; Rottenborn, 1996Rottenborn, S.C. 1996. The use of coastal agricultural fields in Virginia as foraging habitat by shorebirds. Wilson Bulletin, 108(4): 783-796.). Although there are possible positive and negative factors between livestock and shorebirds, to avoid other types of impacts, some strategies, such as installation of signs with bird’s biology information, monitoring populations size, access restriction in breeding areas frequently use by birds and installation of bird watching platforms are indicate to conservation management of the species (Burger et al., 2004Burger, J.; Jeitner, C.; Clark, K. & Niles J.L. 2004. The effect of human activities on migrant shorebirds: successful adaptive management. Environmental Conservation, 31(4): 283-288.).

RJNP and its adjacent areas are considered annual breeding sites for the White-backed Stilt, on the northern coast of the state of Rio de Janeiro, in southeastern Brazil. The area is also home to a large population (nearly 112.4 birds/km) of the White-backed Stilt during most of the year (authors obs.). More aspects of the breeding biology and ecology of the species, that were not the focus of this study, should be evaluated, such as incubation period, details of parental care and breeding success rate along the years in the colonies in Brazil.

CONCLUSION

White-backed Stilt in Brazil breeds mainly from August to November, and most of the breeding records were in southeast and south regions. Domestic animals and livestock may represent some threats and potential predators during species breeding period in RJNP. Management and mitigation actions, as restrict the access of domestic animals and livestock near the breeding areas should be implement, targeting specie conservation. Furthermore, this study brings the first data on the nest and egg biometry of this species in Brazil, highlighting the northern coastal region of Rio de Janeiro state as a breeding area in the largest protected restinga area in Brazil.

ACKNOWLEDGMENTS

The authors thank M. Pessanha (head of the Restinga Jurubatiba National Park), M.C. Santos, A.N. Miranda and A. Maynhone for all the logistical support at RJNP; T.P. Xavier for kindly drawing up the map. M.P. de Araújo for grass identification. P.R. Gonçalves for animal footprints identification. To citizen-scientists who made the photos of birds available on WikiAves/E-bird and to Yasmina Shah Esmaeili for the English revision of the manuscript.

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  • FUNDING INFORMATION: R.F. Teixeira received a scholarship from Fundação de Amparo à Pesquisa no Rio de Janeiro (FAPERJ - DSC - Proc. № 200.856/2018) and currently receives at scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) Proc. 88887.505354/2020-00, Chamada CNPq/Capes/FAPs/BC - Fundo Newton - Pesquisa Ecológica de Longa Duração - PELD № 15/2016. L.R.M. Porto received a graduate scholarship from “Projeto Costões Rochosos. P.L. Mancini received a postdoctoral scholarship from “Projeto Costões Rochosos”, and currently receives a PNPD postdoctoral scholarship from CAPES, Finance Code 001. The Projeto Costões Rochosos: Ecologia, Impactos e conservação nas Regiões dos Lagos e Norte Fluminense”, is an environmental offset measure established through a Consent Decree/Conduct Adjustment Agreement between Petrorio and the Brazilian Ministry for the Environment, with the Brazilian Biodiversity Fund - FUNBIO as an implementer.
  • Published with the financial support of the "Programa de Apoio às Publicações Científicas Periódicas da USP".

SUPPLEMENTARY MATERIAL

Table S1
Data from sampling fields from monitoring the nests of Himantopus melanurus in the Restinga de Jurubatiba National Park and adjacent areas between 2018 and 2020.

Edited by

Edited by: Luís Fábio Silveira.

Publication Dates

  • Publication in this collection
    03 Oct 2022
  • Date of issue
    2022

History

  • Received
    11 Jan 2022
  • Accepted
    04 May 2022
  • Published
    02 Aug 2022
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