Abstract
Differences in bird eggshell thicknesses occur due to numerous factors, including thinning due to persistent organic pollutants. Not only does thinning weaken the shell; weaker shells combined with elevated ambient temperature and changes in humidities may result in changes in water loss rates from the egg contents. Therefore, thinner eggshells raise concern of water being lost faster than normal at lower relative humidities, which may affect hatching. To investigate the combined effects, we developed and tested an effective method that measures water loss through different thickness eggshells at controlled temperatures and relative humidities to assist in ascertaining the combined effects of climate change (temperature and humidity) and changes in eggshell thickness on bird reproduction. The fastest rate of loss was at 40% RH at 40 °C (0.1 mL/cm2/day), and the slowest was at 22 °C at 80% RH (0.02 mL/cm2/day). Eggshell thickness had a significant effect on water loss at all humidity treatments, except at the highest temperature and humidity treatment (80% RH and 40 °C). Temperature explained 40% of the variance, RH explained 20%, and interactions between temperature and humidity explained 15% of the variance (repeated-measures, two-way ANOVA). Generalized linear analyses revealed that both factors temperature and humidity contributed significantly in any two-way combinations. We have laid the ground for a system to test the combined effects of temperature and humidity changes associated with climate change and eggshell thinning associated with pollutants, on water loss across eggshells.
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Alasahan, S., Akpinar, G. C., Canogullari, S., & Baylan, M. (2016). The impact of eggshell colour and spot area in Japanese quails: I. eggshell temperature during incubation and hatching results. Revista Brasileira de Zootecnia,45, 219–229.
Amat, J. A., Gómez, J., Liñán-Cembrano, G., Rendón, M. A., & Ramo, C. (2017). Incubating terns modify risk-taking according to diurnal variations in egg camouflage and ambient temperature. Behavioral Ecology and Sociobiology,71, 72.
Amat, J. A., & Masero, J. A. (2007). The functions of belly-soaking in Kentish Plovers Charadrius alexandrinus. Ibis,149, 91–97.
Ar, A., & Rahn, H. (1980). Water in the avian egg: overall budget of incubation. American Zoologist,20, 373–384.
Basso, A., & Richner, H. (2015). Predator-specific effects on incubation behaviour and offspring growth in Great Tits. PLoS ONE,10, e0121088.
Bignert, A., Litzén, K., Odsjö, T., Olsson, M., Persson, W., & Reutergårdh, L. (1995). Time-related factors influence the concentrations of ΣDDT, PCBs and shell parameters in eggs of Baltic Guillemot (Uria aalge). Environmental Pollution,89, 27–36.
Bomm, E. R., Figueiredo, E. A., Saatkamp, M. G., & Scmidt, G. S. (2009). Effect of storage period and egg weight on embryo development and incubation results. Brazilian Journal of Poultry Science,11, 1–5.
Booth, D. T., & Seymour, R. S. (1987). Effect of eggshell thinning on water vapour conductance of Malleefowl eggs. The Condor,89, b453–b459.
Bouwman, H., Govender, D., Underhill, L., & Polder, A. (2015). Chlorinated, brominated, and fluorinated organic pollutants in African Penguin eggs. 30 years since the previous assessment. Chemosphere,126, 1–10.
Bouwman, H., Polder, A., Venter, B., & Skaare, J. U. (2008). Organochlorine contaminants in cormorant, darter, egret, and ibis eggs from South Africa. Chemosphere,71, 227–241.
Bouwman, H., Viljoen, I. M., Quinn, L. P., & Polder, A. (2013). Halogenated pollutants in terrestrial and aquatic birds: Converging pollutant profiles, and impacts and risks from high levels. Environmental Research,126, 240–253.
Capp, E., Liebl, A. L., Cones, A. G., & Russel, A. F. (2017). Advancing breeding phenology does not affect incubation schedules in Chestnut-crowned Babblers: Opposing effects of temperature and wind. Ecology and Evolution,ece3, 3524.
Carey, C. (1986). Tolerance of variation in eggshell conductance, water loss, and water content by Red-winged Blackbird embryos. Physiological Zoology,59, 109–122.
Carey, C. (2009). The impacts of climate change on the annual cycles of birds. Philosophical Transactions of the Royal Society B,364, 3321–3330.
Castilla, A. M., Herrel, A., Robles, H., Malone, J., & Negro, J. J. (2010). The effect of developmental stage on eggshell thickness variation in endangered falcons. Zoology,113, 184–188.
Cortinovis, S., Galasi, S., Melone, G., Saino, N., Porte, C., & Bettinetti, R. (2008). Organochlorine contamination in the Great Crested Grebe (Podiceps cristatus): Effects on eggshell thickness and egg steroid levels. Chemosphere,73, 320–325.
Crick, H. Q. (2004). The impact of climate change on birds. Ibis,146, 48–56.
Dauwe, T., Eens, M., Janssens, E., & Kempenaers, B. (2004). The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in Blue Tit Parus caeruleus eggs. Environmental Pollution,129, 125–129.
Davis, T. A., & Ackerman, R. A. (1987). Effect of increased water loss on growth and water content of the chick embryo. The Journal of Experimental Zoology,1, 357–364.
de Araújo, I. C., Leandro, N. S. M., Mesquita, M. A., Café, M. B., Mello, H. H. C., & Gonzales, E. (2017). Water vapor conductance: a technique using eggshell fragments and relations with other parameters of eggshell. Brazilian Journal of Animal Science,46, 896–902.
Deeming, D. C. (2011). A review of the relationship between eggshell colour and water vapour conductance. Avian Biology Research,4, 224–230.
Dong, Y. H., Wang, H., An, Q., Ruiz, X., Fasola, M., & Zhang, Y. M. (2004). Residues of organochlorinated pesticides in eggs of water birds from Tai Lake in China. Environmental Geochemistry and Health,26, 259–268.
Dunne, J. P., Stauffer, R. J., & John, J. G. (2013). Reductions in labour capacity from heat stress under climate warming. Nature Climate Change,3, 563–566.
DuRant, S. E., Hopkins, W. A., Hepp, G. R., & Walters, J. R. (2013). Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds. Biological Reviews,88, 499–509.
Finnlund, M., Hissa, R., Koivusaari, J., Merilä, E., & Nuuja, I. (1985). Eggshells of Arctic Terns from Finland: Effects of incubation and geography. The Condor,87, 79–86.
Fisher, E. M., & Knutti, R. (2012). Robust projections of combined humidity and temperature extremes. Nature Climate Change,3, 126–130.
Gómez, J., Pereira, A. I., Pérez-Hurtado, A., Castro, M., Ramo, C., & Amat, J. A. (2016). A trade-off between overheating and camouflage on shorebird eggshell colouration. Journal of Avian Biology,47, 346–353.
Gómez, J., Ramo, C., Stevens, M., Liñán-Cembrano, G., Rendón, M. A., Troscianko, J. T., et al. (2018a). Latitudinal variation in biophysical characteristics of avian eggshells to cope with differential effects of solar radiation. Ecology and Evolution. https://doi.org/10.1002/ece3.4335.
Gómez, J., Ramo, C., Troscianko, J., Stevens, M., Castro, M., Pérez-Hurtado, A., et al. (2018b). Individual egg camouflage is influenced by microhabitat selection and use of nest materials in ground-nesting birds. Behavioral Ecology and Sociobiology,72, 142.
Grant, G. S., Paganelli, C. V., & Rahn, H. (1984). Microclimate of Gull-billed Tern and Black Skimmer nests. The Condor,86, 337–338.
Griffith, S. C., Mainwaring, M. C., Sorato, E., & Beckman, C. (2016). High atmospheric temperatures and ‘ambient incubation’ drive embryonic development and lead to earlier hatching in a passerine bird. Royal Society Open Science,3, 150371.
Hałupka, L., & Orłowsk, G. (2015). Embryonic eggshell thickness erosion: A literature survey re-assessing embryo-induced eggshell thinning in birds. Environmental Pollution,205, 218–224.
Hargitai, R., Boross, N., Nyiri, Z., & Eke, Z. (2016). Biliverdin- and protoporphyrin-based eggshell pigmentation in relation to antioxidant supplementation, female characteristics and egg traits in the canary (Serinus canaria). Behavioral Ecology and Sociobiology,70, 2093–2110.
Helander, B., Bignert, A., & Asplund, L. (2008). Using raptors as environmental sentinels: Monitoring the White-tailed Sea Eagle Haliaeetus albicilla in Sweden. Ambio,37, 425–431.
Hu, Y., Qi, S., Yuan, L., Liu, H., & Xing, X. (2018). Assessment of organochlorine pesticide contamination in waterbirds from an agricultural region, Central China. Environmental Geochemistry and Health,40, 175–187.
Hullet, R. M., Christensen, W. L., & Bagley, L. G. (1987). Controlled egg weight loss during incubation of turkey eggs. Poultry Science,66, 428–432.
IPCC. (2013). Summary for policymakers. In T. F. Stocker, D. Qin, G. K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, & P. M. Midgley (Eds.), Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press.
Järvinen, A. (1994). Global warming and egg size of birds. Ecography,17, 108–110.
Joyner, C. J., Peddie, M. J., & Taylor, T. G. (1987). The effect of age on egg production in the domestic hen. US National Library of Medicine National Institutes of Health,65, 331–336.
Kilner, R. M. (2006). The evolution of egg colour and patterning in birds. Biological Reviews,81, 383–406.
Kylin, H., Bouwman, H., & Louette, M. (2011). Distributions of the subspecies of Lesser Black-backed Gulls Larus fuscus in sub-Saharan Africa. Bird Study,58, 186–192.
Lahti, D. C., & Ardia, D. R. (2016). Shedding light on bird egg color: Pigment as parasol and the dark car effect. The American Naturalist,187, 547–563.
Laporte, P. (1982). Organochlorine residues and eggshell measurements of Great Blue Heron eggs from Quebec. Colonial Waterbirds,5, 95–103.
Lei, B. R. L., Green, J. A., & Pichegru, L. (2014). Extreme microclimate conditions in artificial nests for endangered African Penguins. Bird Conservation International,24, 201–213.
Lundholm, C. E. (1997). DDE-induced eggshell thinning in birds: Effects of p, p’-DDE on the calcium and prostaglandin metabolism of the eggshell gland. Comparative Biochemistry and Physiology, Part C,118, 113–128.
Martin, P. A., & Arnold, T. W. (1991). Relationships among fresh mass, incubation time, and water loss in Japanese Quail eggs. The Cooper Ornithological Society,93, 28–37.
Massaro, M., & Davis, L. S. (2005). Differences in egg size, shell thickness, pore density, pore diameter and water vapour conductance between first and second eggs of Snares Penguins (Eudyptes robustus) and their influence on hatching asynchrony. Ibis,147, 251–258.
Maurer, G., Portugal, S. J., & Cassey, P. (2012). A comparison of indices and measured values of eggshell thickness of different shell regions using museum eggs of 230 European bird species. Ibis,154, 714–724.
Meir, M., & Ar, A. (1990). Gas pressures in the air cell of the ostrich egg prior to pipping as related to oxygen consumption, eggshell gas conductance, and egg temperature. The Condor,92, 556–563.
Miljeteig, C., Gabrielsen, G. W., Strøm, H., Gavrilo, M. V., Lie, E., & Jenssen, B. M. (2012). Eggshell thinning and decreased concentrations of vitamin E are associated with contaminants in eggs of Ivory Gulls. Science of the Total Environment,431, 92–99.
Morgan, K. R., Paganelli, C. V., & Rahn, H. (1978). Egg weight loss and nest humidity during incubation in two Alaskan gulls. The Condor,80, 272–275.
Mortola, J. P. (2009). Gas exchange in avian embryos and hatchlings. Comparative Biochemistry and Physiology, Part A,153, 359–377.
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 rufescencs). Brazilian Journal of Poultry Science,5, 131–135.
Noiva, R. M., Menezes, A. C., & Peleteiro, M. C. (2014). Influence of temperature and humidity manipulation on chicken embryonic development. BMC Veterinary Research,10, 234.
Nybø, S., Staurnes, M., & Jerstad, K. (1995). Thinner eggshells of dipper (Cinclus cinclus) eggs from an acidified area compared to a non-acidified area in Norway. Water, Air, and Soil pollution,93, 255–266.
Pacifici, M., Visconti, P., Butchard, S. H. M., Watson, J. E. M., Cassola, F. M., & Rondini, C. (2017). Species’ traits influenced their response to recent climate change. Nature Climate Change. https://doi.org/10.1038/nclimate3223.
Paganelli, C. V. (1980). The physics of gas exchange across the avian eggshell. American Zoologist,20, 329–338.
Portugal, S. J., Maurer, G., & Cassey, P. (2010). Eggshell permeability: A standard technique for determining interspecific rates of water vapour conductance. Physiological and Biochemical Zoology,83, 1023–1031.
Portugal, S. J., Maurer, G., Thomas, G. H., Hauber, M. E., Grim, T., & Cassey, P. (2014). Nesting behaviour influences species-specific gas exchange across avian eggshell. The Journal of Experimental Biology,217, 3326–3332.
Potti, J. (2008). Temperature during egg formation and the effect of climate warming on egg size in a small songbird. Acta Oecologica,33, 387–393.
Rahn, H., Carey, C., Balmas, K., Bhatia, B., & Paganelli, C. (1977). Reduction of pore area of the avian eggshell as an adaptation to altitude. Physiological Sciences,74, 3095–3098.
Rahn, H., Krog, J., & Mehlum, F. (2016). Microclimate of the nest and egg water loss of the eider Somateria mollissima and other waterfowl in Spitsbergen. Polar Research,1, 171–183.
Rahn, H., Paganelli, C. V., Nisbet, C. T., & Whittow, G. C. (1976). Regulation of incubation water loss in eggs of seven species of terns. Physiological Zoology,49, 245–259.
Roudybush, T., Hoffman, L., & Rahn, H. (1980). Conductance, pore geometry, and water loss of eggs of Cassin’s Auklets. Condor,82, 105–106.
Ruzal, M., Shinder, D., Malka, L., & Yahav, S. (2011). Ventilation plays an important role in hens’ egg production at high ambient temperature. Poultry Science,90, 856–862.
Ton, R., & Martin, T. E. (2017). Proximate effects of temperature versus evolved intrinsic constraints for embryonic development times among temperate and tropical songbirds. Nature Scientific Reports,7, 895.
Vleck, C. M., Vleck, D., Rahn, H., & Paganelli, C. V. (1983). Nest microclimate, water-vapour conductance, and water loss in heron and tern eggs. Auk,100, 76–83.
Yom-Tov, Y., Wilson, R., & Ar, A. (1986). Water loss from Jackass Penguin Spheniscus demersus eggs during natural incubation. Ibis,128, 1–8.
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Funding was provided by North-West University (Grant No. General funds).
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L-mV conducted the study, collected the data, and drafted the manuscript. HK assisted with planning, interpretation, and editing. PB helped design and adapt the incubator. IE assisted with the design of the study, conducted some of the statistical analyses, and assisted with editing. HB conceived the idea, planned the outlay, conducted some of the statistical analyses, and assisted with drafting and editing.
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Veldsman, Lm., Kylin, H., Bronkhorst, P. et al. A method to determine the combined effects of climate change (temperature and humidity) and eggshell thickness on water loss from bird eggs. Environ Geochem Health 42, 781–793 (2020). https://doi.org/10.1007/s10653-019-00274-x
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DOI: https://doi.org/10.1007/s10653-019-00274-x