Incubation parameters, offspring growth, and behavioral adaptations to heat stress of Black Skimmers (Rynchops niger) in a Neotropical inland colony (Aves, Charadriiformes, Laridae)

Authors

  • Karl-Ludwig Schuchmann Universidade Federal de Mato Grosso, Instituto Nacional de Ciência e Tecnologia em Áreas Umidas, Computational Bioacoustics Research Unit. Cuiabá, MT, Brasil https://orcid.org/0000-0002-3233-8917
  • Martin Schley Universidade Federal de Mato Grosso, Instituto Nacional de Ciência e Tecnologia em Áreas Umidas, Computational Bioacoustics Research Unit. Cuiabá, MT, Brasil https://orcid.org/0000-0003-1354-4173
  • Mona Hegmann Universidade Federal de Mato Grosso, Instituto Nacional de Ciência e Tecnologia em Áreas Umidas, Computational Bioacoustics Research Unit. Cuiabá, MT, Brasil https://orcid.org/0000-0002-5521-4052
  • Filipe Ferreira de Deus Universidade Federal de Mato Grosso, Instituto Nacional de Ciência e Tecnologia em Áreas Umidas, Computational Bioacoustics Research Unit. Cuiabá, MT, Brasil. https://orcid.org/0000-0002-2936-8074
  • Ana Silvia de Oliveira Tissiani Universidade Federal de Mato Grosso, Instituto Nacional de Ciência e Tecnologia em Áreas Umidas, Computational Bioacoustics Research Unit. Cuiabá, MT, Brasil. https://orcid.org/0000-0002-5128-2592
  • André-A. Weller Zoological Research Museum Alexander Koenig, Ornithology. Bonn, Germany. https://orcid.org/0000-0003-3479-311X
  • Marinêz Isaac Marques Universidade Federal de Mato Grosso, Instituto Nacional de Ciência e Tecnologia em Áreas Umidas, Computational Bioacoustics Research Unit. Cuiabá, MT, Brasil https://orcid.org/0000-0002-9890-8505

DOI:

https://doi.org/10.11606/1807-0205/2022.62.045

Keywords:

Behavior, Embryonal development, Growth rate, Incubation, Thermal imaging

Abstract

This study focuses on incubation parameters, egg morphometrics, and body mass development, hatching, and behavioral adaptations to heat stress within a colony of freshwater-breeding Black Skimmers (Rynchops niger) located in the private nature reserve of Serviço Social do Comércio (SESC) in the northern Pantanal, Mato Grosso, Brazil. Temperatures of nest, eggs, and surface substratum, as well as the development of embryos, were surveyed using thermal imaging, a method allowing digital recording from a distance and in a fraction of the time of traditional measuring techniques. The mean egg dimensions (n = 71) were 4.48 (± 0.13) × 3.27 (± 0.07) cm; the mean mass at hatching was 24.3 (± 1.9) g, with a significant decrease over incubation time. The mean surface temperature of eggs varied from 30.9℃ to 39.7℃, while the sand surface temperature was 20℃ at 06:00 h, rising to 47.7℃ at 11:00 h. There was a significant increase (7%) in egg surface temperature throughout incubation. Incubation-bout durations (n = 2108) were correlated with the microclimatic conditions of the substratum, becoming shorter with increasing sand-surface temperature around midday. Egg hatching lasted one day, and siblings hatched no more than 24 h apart. The mean body mass on Day 1 after hatching was 16.8 (± 1.6) g (n = 6). Three days after hatching, chicks moved to new sand depressions provided by parents near the original nest, where they remained motionless or tried to hide under riparian vegetation. The single chick that fledged had a growth rate of K = 0.117 and a t₁₀₋₉₀ value of 37.3 days. On Day 7, dorsal pintail feathers and primaries appeared, which were open on Day 15. After 14 days, the chick was able to regulate its body temperature, and no more feeding by parental birds during the daytime was observed. On Day 21, the immature plumage was fully developed. Fledging was completed on Day 27. Our study demonstrates that thermal imaging is a useful method of surveying egg and embryo development in the Black Skimmer, reducing nest disturbance and observation efforts.

Downloads

Download data is not yet available.

References

Alho, C.J.R. 2008. Biodiversity of the Pantanal: response to seasonal flooding regime and to environmental degradation. Brazilian Journal of Biology, 68(4): 957-966. https://doi.org/10.1590/S1519-69842008000500005.

Alho, C.J.R. 2011. A conservation agenda for the Pantanal´s biodiversity. Brazilian Journal of Biology, 71(1): 327-335. https://doi.org/10.1590/S1519-69842011000200012.

Alho, C.J.R. & Silva, J.S.V. 2012. Effects of severe floods and droughts on wildlife of the Pantanal wetland (Brazil) – a review. Animals, 2(4): 591-610. https://doi.org/10.3390/ani2040591.

Alho, C.J.R.; Lacher Jr., T.E. & Gonçalves, H.C. 1988. Environmental degradation in the Pantanal environmental degradation in the Pantanal ecosystem: in Brazil, the world's largest wetland is being threatened by human activities. BioScience, 38(3): 164-171. https://doi.org/10.2307/1310449.

Amat, J.A. & Masero, J.A. 2006. The function of belly-soaking in Kentish Plovers Charadrius alexandrinus. Ibis, 149: 91-97. https://doi.org/10.1111/j.1474-919X.2006.00615.x.

Amat, J.A.; Monsa, R. & Masero, J.A. 2012. Dual function of egg-covering in the Kentish Plover Charadrius alexandrinus. Behaviour, 149(8): 881-895. https://doi.org/10.2307/41720591.

Antas, P.T.Z.; Carrara, L.; Kulaif-Ubaid, F.; Borges-Junior, S. & Pinheiro-Ferreira, L. (Eds.). 2016. Conhecendo o Pantanal, no. 10: Aves coloniais da Reserva Particular do Patrimônio Natural SESC Pantanal. Rio de Janeiro, SESC – Departamento Nacional.

Cade, T.J. & Mclean, G.L. 1967. Transport of water by adult sandgrouse to their young. Condor, 69(4): 323-343. https://doi.org/10.2307/1366197.

Cordoba-Cordoba, S.; Ouyang, J.Q. & Hauck, S.J. 2010. Nesting preferences and population estimates of a new Black Noddy Anous minutus breeding colony on One Tree Island, Great Barrier Reef, Australia. Marine Ornithology, 38: 79-84.

Crabb, L.; Laing, A.; Whitney, B. & Saito, C. 2017. Hydroelectric dams threaten Brazil's mysterious Pantanal – one of the world's great wetlands. Available: https://theconversation.com/hydroelectric-dams-threaten-brazils-mysterious-pantanal-one-of-the-worlds-great-wetlands-86588. Access: 10/10/2021.

Da Silva, C.J.; Wantzen, K.M.; Nunes da Cunha, C. & Machado, F.D.A. 2001. Biodiversity in the Pantanal Wetland, Brazil. In: Gopal, B.; Junk W.J. & Davis, J.A. (Eds.). Biodiversity in wetlands: assessment, function and conservation. Leiden, Backhuys Publishers. v. 2, p. 187-215.

Deeming, D.C. 2002. Avian incubation. Behaviour, environment, and evolution. New York, Oxford University Press.

Deeming, D.C. & Ferguson, M.W.J. 1991. Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press. 464p.

Drent, R. 1975. Incubation. In: Farner, D.S.; King, J.R. & Parkes, K.C. (Eds.). Avian biology. New York, Academic Press. p. 333-420.

Drent, R.H. 1970. Functional aspects of incubation in the Herring Gull. Behaviour Supplement, 17: 1-132. https://www.jstor.org/stable/30039168.

Efe, M.A.; Bugoni, L.; Mohr, L.V.; Scherer, A. & Scherer, S.B. 2001. First-known record of breeding for the Black Skimmer (Rynchops niger) in a mixed colony in Iticuí river, Rio Grande do Sul state, southern Brazil. International Journal of Ornithology, 2001: 103-107.

Erwin, R.M. 1977. Black Skimmer breeding ecology and behaviour. The Auk, 94(4): 709-717. https://doi.org/10.2307/4085267.

Gordon, C.A.; Christol, D.A. & Beck, R.A. 2000. Low reproductive success of Black Skimmers associated with low food availability. The International Journal of Waterbird Biology, 23(3): 168-171. https://scholarworks.wm.edu/aspubs/61.

Grant, G.S. 1981. Belly-soaking by incubating Common, Sandwich, and Royal Terns. Journal of Field Ornithology, 52(3): 244.

Grant, G.S. 1982. Avian incubation. Egg temperature, nest humidity, and behavioural thermoregulation in a hot environment. Ornithological Monographs, 30: 1-75. https://doi.org/10.2307/40166669.

Grant, G.S.; Paganelli, C.V. & Rahn, H. 1984. Microclimate of Gull-billed Tern and Black Skimmer nests. Condor, 86(3): 337-338. https://doi.org/10.2307/1367005.

Gwynne, J.A. & Ridgely, R.S. 2010. The birds of Brazil. The Pantanal and Cerrado of central Brazil. Ithaca, Cornell University Press.

Hart, L.A.; Downs, C.T. & Brown, M. 2016. Sitting in the sun: nest microhabitat affects incubation temperatures in seabirds. Journal of Thermal Biology, 60: 149-154. https://doi.org/10.1016/j.jtherbio.2016.07.001.

Howell, T.R. & Bartholomew, G.A. 1962. Temperature regulation in the Sooty Tern Sterna fuscata. Ibis, 104: 98-105. https://doi.org/10.1111/j.1474-919X.1962.tb08632.x.

Junk, W.J.; Bayley, P.B. & Sparkt, R.E. 1989. The flood pulse concept in river-floodplain-systems. Canadian Special Publication of Fisheries and Aquatic Sciences, 106: 110-127.

Junk, W.J.; Nunes da Cunha, C.; Wantzen, K.M.; Petermann P.; Strüssmann, C.; Marques, M.I. & Adis, J. 2006. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Journal of Aquatic Sciences, 68: 278-309. https://doi.org/10.1007/s00027-006-0851-4.

Krannitz, P.G. 1989. Nesting biology of Black Skimmers, Large-billed Terns, and Yellow-billed Terns in Amazonian Brazil. Journal of Field Ornithology, 60: 216-223. https://www.jstor.org/stable/4513423.

Matthysen, E.; Adriaensen, F. & Dhondt, A.A. 2011. Multiple responses to increasing spring temperatures in the breeding cycle of Blue and Great Tits (Cyanistes caeruleus, Parus major). Global Change Biology, 17: 1-16. https://doi.org/10.1111/j.1365-2486.2010.02213.x.

McCafferty, D.J. 2013. Applications of thermal imaging in avian science. Ibis, 155: 4-15. https://doi.org/10.1111/ibi.12010.

Mclean, G.L. 1974. Belly-soaking in the Charadriiformes. Journal of the Bombay Natural History Society, 72: 74-82.

Morales, M. & R Development Core Team. 2012. sciplot: Scientific graphing functions for factorial designs, Version 1.1-0. Available: http://cran.r-project.org/web/packages/sciplot/index.html. Access: 15/05/2013.

Nakage, E.S.; Cardozo, J.P.; Pereira, G.T.; Queiroz, S.A. & Boleli, I.C. 2003. Effect of temperature on incubation period, embryonic mortality, hatch rate, egg water loss and partridge chick weight (Rhynchotus rufescens). Revista Brasileira de Ciência Avícola, 5: 131-135. https://doi.org/10.1590/S1516-635X2003000200007.

Nisbet, I.C.T. 1983. Belly-soaking by incubating and brooding Common Terns. Journal of Field Ornithology, 54(2): 190-192. https://www.jstor.org/stable/4512811.

Paganelli, C.V.; Reeves, R.B.; Greene, D.G. & Rahn, H. 1974. The avian egg: water vapor conductance, shell thickness, and functional pore area. Condor, 76: 153-158. https://doi.org/10.2307/1366725.

Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D.; EISPACK; Heisterkamp, S.; Van Willigen, B.; Ranke, J. & R Development Core Team. 2012. nlme: Linear and nonlinear mixed effect models, version 3.1-110. Available: http://cran.r-project.org/web/packages/nlme/index.html. Access: 29707/2013.

R Development Core Team. 2013. R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. The R Foundation for Statistical Computing.

Raeder, F.L. & Bernhard, R. 2003. A method for quantifying bird colonies in sand bars via GPS. Brazilian Journal of Biology, 63(3): 545-549. https://doi.org/10.1590/S1519-69842003000300021.

Ricklefs, R.E. 1967. A graphical method of fitting equations to growth curves. Ecology, 48(6): 978-983. https://doi.org/10.2307/1934545.

Ricklefs, R.E. 1968. Patterns of growth in birds. Ibis, 110(4): 419-451. https://doi.org/10.1111/j.1474-919X.1968.tb00058.x.

Ricklefs, R.E. 1973. Patterns of growth in birds. II. Growth rate and mode of development. Ibis, 115(2): 177-201. https://doi.org/10.1111/j.1474-919X.1973.tb02636.x.

Ricklefs, R.E. 1976. Growth rates of birds in the humid New World tropics. Ibis, 118(2): 179-207. https://doi.org/10.1111/j.1474-919x.1976.tb03065.x.

Riechert, J.; Chastel, O. & Becker, P.H. 2012. Why do experienced birds reproduce better? Possible endocrine mechanisms in a long-lived seabird, the Common Tern. General and Comparative Endocrinology, 178(2): 391-399. https://doi.org/10.1016/j.ygcen.2012.06.022.

Roberts, G.R. 1976. Belly-soaking and chick transport in the African Skimmer. Ostrich, 47: 126. https://doi.org/10.2173/bow.blkski.01.

Scherer, A.L.; Scherer, J.F.M.; Petry, M.V. & Valiati, V.H. 2013. Sexual dimorphism, habitat use and molt in wintering Black Skimmers (Rynchops niger) in the Lagoa do Peixe, southern Brazil. The International Journal of Waterbird Biology, 36(4): 438-447. https://doi.org/10.1675/063.036.0401.

Schuchmann, K.-L. 1985. Natal care and growth in a nestling Reddish Hermit Phaethornis ruber in Suriname. Ardea, 74: 101-104.

Schuchmann, K.-L.; Hegmann, M.; Schley, M.; Marques, M.I.; de Deus, F.F. & Weller, A.-A. 2018. Reproduction and agonistic behavior of Black Skimmers (Rynchops niger) in a mixed-species colony in the Brazilian Pantanal. Studies on Neotropical Fauna and Environment, 53(3): 219-232. https://doi.org/10.1080/01650521.2018.1479951.

Seidl, A.F. & Moraes, A.S. 2000. Global valuation of ecosystem services: application to the Pantanal da Nhecolandia, Brazil. Ecological Economics, 33: 1-6. https://doi.org/10.1016/S0921-8009(99)00146-9.

Vieira, B.P. 2017. Influence of environmental changes on the resource use and abundance of Black Skimmers. (Doctoral Thesis). University of Glasgow, Glasgow.

Ward, D. 1990. Incubation temperatures and behavior of Crowned, Black-winged, and Lesser Black-winged Plovers. The Auk, 107: 10-17. https://www.jstor.org/stable/4087797.

Webb, D.R. 1987. Thermal tolerance of avian embryos: a review. Condor, 89(4): 874-898. https://doi.org/10.2307/1368537.

Zarza, R.; Cintra, R. & Anciaes, M. 2013. Distribution, abundance and habitat selection by breeding Yellow-billed Terns (Sternula superciliaris), Large-billed Terns (Phaetusa simplex) and Black Skimmers (Rynchops niger) in the Brazilian Amazon. The International Journal of Waterbird Biology, 36(4): 470-481. https://doi.org/10.1675/063.036.0404.

Zusi, R.L. 1996. Family Rynchopidae (Skimmers). 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. 668-667.

Zusi, R.L. & Garcia, E.F.J. 2017. Black Skimmer (Rynchops niger). In: del Hoyo, J.; Elliott, A.; Sargatal, J.; Christie, D.A. & Juana, E. (Eds.). Handbook of the Birds of the World Alive. Barcelona, Lynx Edicions.

Downloads

Published

2022-08-02

Issue

Section

Original Article

How to Cite

Schuchmann, K.-L., Schley, M., Hegmann, M., Deus, F. F. de, Tissiani, A. S. de O., Weller, A.-A., & Marques, M. I. (2022). Incubation parameters, offspring growth, and behavioral adaptations to heat stress of Black Skimmers (Rynchops niger) in a Neotropical inland colony (Aves, Charadriiformes, Laridae). Papéis Avulsos De Zoologia, 62, e202262045. https://doi.org/10.11606/1807-0205/2022.62.045