Density and spatial distribution of migratory shorebirds in different foraging habitats in the coastal region of Piauí State, Brazil
DOI:
https://doi.org/10.1590/Keywords:
Birds, Charadriiformes, Aquatic invertebrates, Feeding site, Coastal zonestAbstract
Coastal habitats are important feeding grounds for migratory shorebirds, which turns the coast of Piauí State into an
important region for birds’ migration cycle. This study aimed to identify migratory shorebirds, analyze their patterns of
habitat preference on coastal Piauí State, Brazil, and identify classes of invertebrates found in foraging sites. In total,
23,829 records of migratory shorebirds belonging to 15 species were found at feeding sites, presenting significant
segregation between different foraging substrates (F1,23 = 8.41; p = 0.001). Limnodromus griseus (56.5±98.42;
p > 0.001), Numenius hudsonicus (35.96±37.37; p > 0.001), and Calidris canutus (34.4±80.84; p < 0. 001) were the
species accounting for the highest densities in muddy substrate. Calidris pusilla (77.37±178.02; p > 0.001), Charadrius
semipalmatus (66±142.17: p > 0.001), and Calidris alba (56.5±181.24; p > 0.001) were the most significant species in
sandy-muddy substrate. Birds’ lowest density was observed in sandy habitat, but C. alba (22.41±40.9) recorded the
highest density in this substrate. Overall, most shorebirds (92.8 %) preferred foraging substrates presenting higher
concentration of fine particles (silt, clay, and fine sand). Invertebrates belonging to classes Polychaeta, Gastropoda,
Bivalvia, and Malacostraca prevailed in these sites. Therefore, substrate type and prey composition are factors influencing
the density of migratory shorebirds in foraging sites. In addition, this region witnesses the occurrence of endangered
species, and it reinforces the importance of these feeding sites for them during their migration to Brazil’s coastal region.
References
Anderson, M. J. 2005. Permutational multivariate analysis
of variance. Department of Statistics, University of
Auckland, Auckland, 26, 32–46. DOI: https://doi.
org/10.1002/9781118445112.stat07841
Angarita-Báez, J. A. & Carlos, C. J. 2024. Feeding
behavior and prey of three migratory shorebirds (Aves:
Charadriiformes) during the nonbreeding season in
southern Brazil. Acta Ethologica, 27(1), 27–38. DOI:
https://doi.org/10.1007/s10211-023-00427-3
Araújo, I. R. G. Gomes, É. R., Gonçalves, R. M. & Araújo
Queiroz, H. A. de. 2019. Estimativa do índice de
vulnerabilidade à erozão costeira (IVC) para o litoral do
Piauí, Brasil. Revista Brasileira de Geomorfologia, 20(1),
–118. DOI: https://doi.org/10.20502/rbg.v20i1.1260
Aveline, L. C. 1980. Fauna dos manguezais brasileiros.
Revista Brasileira de Geografia, 42(4), 786–821.
Backwell, P. R. Y., O’Hara, P. D. & Christy, J. H. 1998.
Prey availability and selective foraging in shorebirds.
Animal Behaviour, 55(6), 1659–1667. DOI: https://doi.
org/10.1006/anbe.1997.0713
Baptista, J. G. 1981. Geografia Física do Piauí (2. ed.),
Teresina, COMEPI.
Baroni, P. C. & Borges, R. P. 2015. Macrofauna bentônica
da faixa entremarés da praia de José Menino Intertidal
Benthic Macrofauna of Jose Menino Beach (SantosSP). Unisanta BioScience, 4(104), 98–104.
Beauchamp, G. 2009. Functional response of staging
semipalmated sandpipers feeding on burrowing
amphipods. Oecologia, 161(3), 651–655. DOI: https://
doi.org/10.1007/s00442-009-1398-6
Braga, S. de S., Guzzi, A., Perinotto, A. R. C. & Malta, G.
A. P. 2022. Análise da atratividade turística do litoral
piauiense: atualização da avaliação dos atrativos
turísticos, entre 2010 e 2020. Revista Turismo Em
Análise, 33(1), 29–49. DOI: https://doi.org/10.11606/
issn.1984-4867.v33i1p29-49
Bray, J. R. & Curtis, J. T. 1957. An ordination of the upland
forest communities of southern Wisconsin. Ecological
Monographs, 27(4), 326–349.
Burger, J., Jeitner, C., Clark, K. & Niles, L. J. 2004. The effect
of human activities on migrant shorebirds: successful
Migratory shorebirds in different foraging habitats
Ocean and Coastal Research 2024, v72:e24065 12
Siqueira et al.
adaptive management. Environmental Conservation,
(4), 283–288.
Castro, G., Myers, J. P. & Place, A. R. 1989. Assimilation
Efficiency of Sanderlings (Calidris alba) Feeding
on Horseshoe Crab (Limulus polyphemus) Eggs.
Physiological Zoology, 62(3), 716–731. DOI: https://doi.
org/10.1086/physzool.62.3.30157923
Choi, C. Y., Battley, P. F., Potter, M. A., Ma, Z. & Liu, W.
Factors Affecting the Distribution Patterns of
Benthic Invertebrates at a Major Shorebird Staging Site
in the Yellow Sea, China. Wetlands, 34(6), 1085–1096.
DOI: https://doi.org/10.1007/s13157-014-0568-4
Churchwell, R. T., Kendall, S., Brown, S. C., Blanchard, A. L.,
Hollmen, T. E. & Powell, A. N. 2018. The First Hop: Use
of Beaufort Sea Deltas by Hatch-Year Semipalmated
Sandpipers. Estuaries and Coasts, 41(1), 280–292.
DOI: https://doi.org/10.1007/s12237-017-0272-8
Cohen, J. B., Karpanty, S. M., Fraser, J. D. & Truitt, B. R.
The effect of benthic prey abundance and size on
red knot (Calidris canutus) distribution at an alternative
migratory stopover site on the US Atlantic Coast.
Journal of Ornithology, 151(2), 355–364. DOI: https://
doi.org/10.1007/s10336-009-0462-7
Delchiaro, R. T. C., Barbieri, E. & Branco, J. O. 2013.
Distribuição do maçarico-branco (Calidris alba)
entre julho de 2008 e junho de 2009 na praia da Ilha
Comprida, São Paulo, Brasil. Estudos de Biologia,
(85), 177–184. DOI: https://doi.org/10.7213/estud.
biol.35.085.ao08
Dekinga, A. & Piersma, T. 1993. Reconstructing diet
composition on the basis of faeces in a mollusc-eating
wader, the Knot Calidris canutus. Bird Study, 40(2), 144–
DOI: https://doi.org/10.1080/00063659309477140
Ersoy, S., Beardsworth, C. E., Dekinga, A., van der Meer,
M. T. J., Piersma, T., Groothuis, T. G. G. & Bijleveld,
A. I. 2022. Exploration speed in captivity predicts
foraging tactics and diet in free-living red knots. Journal
of Animal Ecology, 91(2), 356–366. DOI: https://doi.
org/10.1111/1365-2656.13632
Esser, W., Vöge, S. & Exo, K. M. 2008. Day-night activity
of intertidal invertebrates and methods to estimate
prey accessibility for shorebirds. Senckenbergiana
Maritima, 38(2), 115–122. DOI: https://doi.org/10.1007/
BF03055286
Faria, F. A., Albertoni, E. F. & Bugoni, L. 2018. Trophic
niches and feeding relationships of shorebirds in
southern Brazil. Aquatic Ecology, 52(4), 281–296. DOI:
https://doi.org/10.1007/s10452-018-9663-6
Fedrizzi, C. E., Carlos, C. & Campos, A. 2016. Annual
patterns of abundance of Nearctic shorebirds and their
prey at two estuarine sites in Ceará, NE Brazil, 2008-
Wader Study, 123(2), 122–135. DOI: https://doi.
org/10.18194/ws.00036
Ferreira, L. G. C. & Kemenes, A. 2023. A influência dos
eventos climáticos extremos na climatologia da planície
litorânea piauiense. Revista Brasileira de Climatologia,
, 634–657. DOI: https://doi.org/10.55761/abclima.
v32i19.16349
Fonseca, J. & Navedo, J. G. 2020. Shorebird predation
on benthic invertebrates after shrimp-pond harvesting:
Implications for semi-intensive aquaculture
management. Journal of Environmental Management,
, 110290. DOI: https://doi.org/10.1016/j.
jenvman.2020.110290
González, A., Jiménez, A., García-Lau, I., Mugica, L. &
Acosta, M. 2022. Trophic ecology of Calidris minutilla,
Calidris pusilla, and Calidris mauri (Aves: Scolopacidae)
in two natural wetlands of Cuba. Caldasia, 44(1),
–164. DOI: https://doi.org/10.15446/caldasia.
v44n1.85223
Grond, K., Ntiamoa-Baidu, Y., Piersma, T. & Reneerkens,
J. 2015. Prey type and foraging ecology of Sanderlings
Calidris alba in different climate zones: Are tropical
areas more favourable than temperate sites? PeerJ, (8),
–17. DOI: https://doi.org/10.7717/peerj.1125
Hayman, P., Marchant, J. & Prater, T. 2010. Shorebirds:
An identification guide to the waders of world, London,
Bloomsbury.
Heller, E. L., Karpanty, S. M., Cohen, J. B., Catlin, D. H.,
Ritter, S. J., Truitt, B. R. & Fraser, J. D. 2022. Factors
that affect migratory Western Atlantic red knots (Calidris
canutus rufa) and their prey during spring staging on
Virginia’s barrier islands. PLoS ONE, 17, 1–31. DOI:
https://doi.org/10.1371/journal.pone.0270224
Hernández, M. de los Á., Bala, L. O. & Musmeci, L. R. 2008.
Dieta de tres especies de aves playeras migratorias en
Península Valdés, Patagonia Argentina. Ornitologia
Neotropical, 19(Suppl.), 605–611.
ICMBio (Instituto Chico Mendes de Conservação da
Biodiversidade). 2018. Livro Vermelho da Fauna
Brasileira Ameaçada de Extinção: Aves. (1. ed., vol. 7).
Brasília, DF.
Iglecia, M. & Winn, B. 2021. A shorebird management
manual, Massachusetts, Manomet.
Kober, K. & Bairlein, F. 2009. Habitat choice and niche
characteristics under poor food conditions. A study
on migratory nearctic shorebirds in the intertidal
flats of Brazil. Ardea, 97(1), 31–42. DOI: https://doi.
org/10.5253/078.097.0105
Linhart, R. C., Hamilton, D. J., Paquet, J., Bellefontaine, S.
C., Davis, S., Doiron, P. B. & Gratto-Trevor, C. L. 2022.
Variation in resource use between adult and juvenile
Semipalmated Sandpipers (Calidris pusilla) and use
of physiological indicators for movement decisions
highlights the importance of small staging sites during
southbound migration in Atlantic Canada. Frontiers
in Ecology and Evolution, 10, 1–18. DOI: https://doi.
org/10.3389/fevo.2022.1059005
Lyra-Neves, R. M. de, Azevedo Júnior, S. M. de & TelinoJúnior, W. R. 2004. Monitoramento do maçarico-branco,
Calidris alba (Pallas) (Aves, Scolopacidae), através de
recuperações de anilhas coloridas, na Coroa do Avião,
Igarassu, Pernambuco, Brasil. Revista Brasileira de
Zoologia, 21(2), 319–324. DOI: https://doi.org/10.1590/
s0101-81752004000200027
Lunardi, V. O., Bard, B., Darl, K., Dark, L. & Fardi, G.
Migratory flows and foraging habitat selection
by shorebirds along the northeastern cost of Brasil: the
case of Baía de Todos os Santos. Estuarine, Coastal
and Shef Science, (96), 179–187.
McNeil, R. & Rodriguez, S. R. 1996. Nocturnal foraging in
shorebirds. International Wader Studies, 8, 114–121.
Migratory shorebirds in different foraging habitats
Ocean and Coastal Research 2024, v72:e24065 13
Siqueira et al.
Meireles, A. J. A. & Campos, A. A. 2011. Componentes
geomorfológicos, funções e serviços ambientais de
complexos estuarinos no Nordeste do Brasil. Revista
da Anpege, 6(6), 89–107. DOI: https://doi.org/10.5418/
ra2010.0606.0007
Morales-Torres, D. F., Valdivia, N., Rodríguez, S. M. &
Navedo, J. G. 2024. The importance of feeding fast
when thieves are around: A case study on Whimbrels
foraging on a wave-exposed sandy beach in southern
Chile. Austral Ecology, 49(1), 1–10. DOI: https://doi.
org/10.1111/aec.13298
Neves, F. M. & Bemvenuti, C. E. 2009. Daily zonation
variation of sandy beach benthic macrofauna in north
coast of the Rio Grande do Sul, Brazil. Iheringia – Serie
Zoologia, 99(1), 71–81. DOI: https://doi.org/10.1590/
s0073-47212009000100011
Nuka, T., Norman, C. P. & Miyazaki, T. 2005. Feeding
behavior and effect of prey availability on Sanderling
Calidris alba distribution on Kujukuri Beach.
Ornithological Science, 4(2), 139–146.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R.,
Legendre, P., McGlinn, D., Minchin, P. R., o’Hara, R. B.,
Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs,
E., & Wagner, H. 2020. Vegan: community ecology
package version 2.5-7.
Paludo, D., Marcelino, A. M. T., Telino Júnior, W. R., Perello,
L. F., Petry, M. V., Mobley, J. A. & Arantes, M. S. 2022.
Áreas Estratégicas para a Conservação de Aves
Limícolas na Costa Brasileira. Revista Costas, 4(2), 21–
DOI: https://doi.org/10.25267/costas.2023.v4.i2.0204
Robert, M. & McNeil, R. 1989. Comparative day and night
feeding strategies of shorebird species in a tropical
environment. Ibis, 131(1), 69–79. DOI: https://doi.
org/10.1111/j.1474-919X.1989.tb02745.x
Saint-Béat, B., Dupuy, C., Bocher, P., Chalumeau, J.,
Crignis, M. de, Fontaine, C., Guizien, K., Lavaud, J.,
Lefebvre, S., Montanié, H., Mouget, J. L., Orvain, F.,
Pascal, P. Y., Quaintenne, G., Radenac, G., Richard, P.,
Robin, F., Vézina, A. F. & Niquil, N. 2013. Key Features
of Intertidal Food Webs That Support Migratory
Shorebirds. PLoS ONE, 8(10), 1–17. DOI: https://doi.
org/10.1371/journal.pone.0076739
Santos, C. D., Rocha, T. M. S., Nascimento, A. W. B., Oliveira,
V. & Martínez, C. 2019. Prey Choice by Declining Atlantic
Flyway Semipalmated Sandpipers (Calidris pusilla) at a
Major Wintering Area in Brazil. Waterbirds, 42(2), 198–
DOI: https://doi.org/10.1675/063.042.0206
Schlacher, T. A., Carracher, L. K., Porch, N., Connolly, R.
M., Olds, A. D., Gilby, B. L., Ekanayake, K. B., Maslo,
B. & Weston, M. A. 2016. The early shorebird will catch
fewer invertebrates on trampled sandy beaches. PLoS
ONE, 11(8), 1–13. DOI: https://doi.org/10.1371/journal.
pone.0161905
Schlacher, T. A., Nielsen, T. & Weston, M. A. 2013. Human
recreation alters behaviour profiles of non-breeding
birds on open-coast sandy shores. Estuarine, Coastal
and Shelf Science, 118, 31–42. DOI: https://doi.
org/10.1016/j.ecss.2012.12.016
Sigrist, T. 2009. Avifauna Brasileira: The avis brasilis field
guide to the birds of Brazil. São Paulo, Avis Brasilis.
Sigrist, T. 2014. Guia de Campo: Avifauna Brasileira
(4. ed.). São Paulo: Avis Brasilis.
Silva, L. de M. R. & Rodrigues, A. A. F. 2015. Densidade e
distribuição espacial de aves limícolas em habitats de
forrageio na costa amazônica brasileira. Ornithologia,
(1), 17–21. Available from: http://cemave.net/
publicacoes/index.php/ornithologia/article/view/206.
Acess date: 2023 Feb. 20
Smith, R. V., Stafford, J. D., Yetter, A. P., Horath, M. M.,
Hine, C. S. & Hoover, J. P. 2012. Foraging Ecology of
Fall-Migrating Shorebirds in the Illinois River Valley.
PLoS ONE, 7(9), 18–22. DOI: https://doi.org/10.1371/
journal.pone.0045121
Souza, M. T. de, Silva, D. R. da, Fortunato, W. C. P.,
Santos, A. C. M. dos & Pereira, S. F. 2020. Composição
e variabilidade espaço-temporal da meiofauna da praia
do Goiabal, Calçoene – AP. Brazilian Journal of Animal
and Environmental Research, 3(3), 1755–1765. DOI:
https://doi.org/10.34188/bjaerv3n3-091
Ter Braak, C. J. 1995. Ordination. In: Jongman, R. H. g.,
Ter Braak, C. J. F. & Van Tongeren, O. F. R. (Ed.). Data
analysis in community and landscape ecology (pp. 91-
). Cambridge: Cambridge University Press.
Vanden Eede, S., Van Tomme, J., De Busschere, C.,
Vandegehuchte, M. L., Sabbe, K., Stienen, E. W. M.,
Degraer, S., Vincx, M. & Bonte, D. 2014. Assessing the
impact of beach nourishment on the intertidal food web
through the development of a mechanistic-envelope
model. Journal of Applied Ecology, 51(5), 1304–1313.
DOI: https://doi.org/10.1111/1365-2664.12314
Van Gils, J. A. & Piersma, T. 2004. Digestively constrained
predators evade the cost of interference competition.
Journal of Animal Ecology, 73(2), 386–398. DOI: https://
doi.org/10.1111/j.0021-8790.2004.00812.x
Van Gils, J. A., Piersma, T., Dekinga, A. & Dietz, M. W. 2003.
Cost-benefit analysis of mollusc-eating in a shorebird:
II. Optimizing gizzard size in the face of seasonal
demands. Journal of Experimental Biology, 206(19),
–3380. DOI: https://doi.org/10.1242/jeb.00546
Vielliard, J. M. E., Almeida, M. E. C., Anjos, L. & Silva,
W. R. 2010. Levantamento quantitativo por pontos de
escuta e Índice Pontual de Abundância. In: Von Matter,
S., Straube, F. C., Queiroz Piacentini, V., Accordi, I. A.,
& Cândido Jr, J. F. (Ed.). Ornitologia e conservação:
ciência aplicada, técnicas de pesquisa e levantamento
(pp. 45-60). Rio de Janeiro: Technical Books Editora.
Zuur, A. F., Ieno, E. N. & Elphick, C. S. 2010. A protocol for
data exploration to avoid common statistical problems.
Methods in Ecology and Evolution, 1(1), 3–14. DOI:
