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Embryonic development of the lemon-yellow tree frog, $Hyla~ savignyi$ Audouin, 1827

Year 2023, , 192 - 207, 30.12.2023
https://doi.org/10.53447/communc.1350057

Abstract

Amphibians are widely used in temperature adaptation studies due to their compatibility in laboratory experiments. We investigated the embryonic development stages (from fertilization to $25^{th}$) of $Hyla ~savignyi$ following Gosner’s generalized table. Three pairs of $H.~ savignyi$ were collected during the breeding season (February 2015) from Northern Cyprus, Kalkanlı Region and maintained at 21±1 °C in the laboratory. The samples were set in 3 groups and examinations of embryos and photographs taken every 10 minutes were carried out during the 9-days embryonic period. Embryos hatched at stage 20 or 21 come up to 3rd – 4th days after fertilization. Embryonic development of $H.~ savignyi$ is about 157 hours (7 days). Cleavage is unequal holoblastic. The embryonic developmental stages of $H.~ savignyi$ were compared with the result of a similar study of two other $Hyla$ species ($H.~orientalis$ and $H.~ annectans$) at various temperatures, and the possible temporal effect of the temperature and ovum size on the growth rate of these species was discussed.

References

  • Callery, E. M., There's more than one frog in the pond: A survey of the Amphibia and their contributions to developmental biology, Seminars in cell & developmental biology, Academic Press, 17 (2006), 80–92. https://doi.org/10.1016/j.semcdb.2005.11.001
  • Gurdon, J.B., Hopwood, N., The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes, International Journal of Developmental Biology, 44 (1) (2000), 43–50.
  • Holtfreter, J., Amphibians. In: Willier, BH.; Weiss, PA.; Hamburger, V. Editors. Analysis of development. W. B. Saunders Company; Philadelphia: (1955), 230–296.
  • Ancel, P., Vintemberger, P., Recherches sur le déterminisme de la symétrie bilatérale dans l’oeuf des Amphibiens, Bulletin biologique de la France et de la Belgique. Suppléments, 31 (1948), 1–182.
  • Barth, L.G., Barth, L.J., Differentiation of Cells of the Rana pipiens Gastrula in Unconditioned Medium, Development, 7 (2) (1959), 210–222. https://doi.org/10.1242/dev.7.2.210
  • Briggs, R., King, T.J., Transplantation of living nuclei from blastula cells into enucleated frogs’ eggs, Proceedings of the National Academy of Sciences, 38 (5) (1952), 455–463. https://doi.org/10.1073/pnas.38.5.455
  • Pasteels, J., Les effets de la centrifugation sur la blastula et la jeune gastrula des Amphibiens: I. Mécanisme de la formation des organes secondaires aux dépens de l'ectoblaste, Development, 1 (2) (1953), 125–145. https://doi.org/10.1242/dev.1.1.5
  • Fankhauser, G., The effects of changes in chromosome number on amphibian development, The Quarterly Review of Biology, 20 (1) (1945), 20-78. https://doi.org/10.1086/394703
  • Harrison, R.G., Experiments in transplanting limbs and their bearing upon the problems of the development of nerves, Journal of experimental zoology, 4 (2) (1907), 239–281.
  • Holtfreter, J., Über die aufzucht isolierter teile des amphibienkeimes: II. Züchtung von keimen und keimteilen in salzlösung. Wilhelm Roux'Archiv für Entwicklungsmechanik der Organismen, 124 (1931), 404–466. https://doi.org/10.1007/BF00652482
  • Spemann, H., Entwickelungsphysiologische Studien am Triton-Ei. Archiv für Entwicklungsmechanik der Organismen, 12 (1901), 224-264 + 1 pI. (V).
  • Spemann, H., Über Transplantationen an Amphibienembryonen im Gastrulastadium. Sitz. Ber. Gesel!, Naturf. Freunde zu Berlin (1916), 306–320.
  • Spemann, H., Experimentelle forschungen zum determinations-und individualitätsproblem, Naturwissenschaften, 7 (1919), 581–591. https://doi.org/10.1007/BF01498212
  • Vogt, W., Morphologische und physiologische Fragen der Primitiventwicklung, Versuche zu ihrer Lösung mittels vitaler Farbmarkierung, Sitz. Ber. Ges. Morph. Physiol. Munchen., 35 (1924), 22–32.
  • Vogt, W., Gestaltungsanalyse am Amphibienkeim mit örtlicher Vitalfarbung. II. Gastrulation und Mesodermbildung bei Urodelen und Anuren, Arch. Entw.Mech., 120 (1) (1929), 384–706.
  • Beetschen, J.C., How did urodele embryos come into prominence as a model system?, The International journal of developmental biology, 40 (4) (1996), 629–636.
  • Malacinski, G.M., Rufus R. Humphrey (1892–1977), American Zoologist. 18 (1978), 191–193.
  • Smith, J.J., Putta, S., Zhu, W., Pao, G.M., Verma, I.M., Hunter, T., Bryant, S.V., Gardiner, D.M., Harkins, T.T., Voss, S.R., Genic regions of a large salamander genome contain long introns and novel genes, BMC Genomics, (2009), 10–19. https://doi.org/10.1186/1471-2164-10-19
  • Elinson, R.P., Fertilization in amphibians: the ancestry of the block to polyspermy, International review of cytology, 101 (1986), 59–100. https://doi.org/10.1016/S0074-7696(08)60246-6
  • Iwao, Y., Fertilization in amphibians. In: Tarin, JJ.; Cano, A. Editors. Fertilization in protozoa and metazoan animals, cellular and molecular aspects. Springer-Verlag; Berlin: (2000), 147-191. https://doi.org/10.1007/978-3-642-58301-8-4
  • Johnson, A.D., Richardson, E., Bachvarova, R.F., Crother, B.I., Evolution of the germ line-soma relationship in vertebrate embryos. Reproduction, 141 (3) (2011), 291–300. https://doi.org/10.1530/rep-10-0474
  • Nieuwkoop, P.D., Sutasurya, L.A., Primordial germ cells in the chordates. Cambridge University Press, Cambridge, 1979.
  • Stocum, D.L., The role of peripheral nerves in urodele limb regeneration. European Journal of Neuroscience, 34 (6) (2011), 908–916. https://doi.org/10.1111/j.1460-9568.2011.07827.x
  • Gosner, K.L., A Simplified table for staging Anuran embryos and larvae with notes on identification, Herpetologica, 16 (3) (1960), 183–190.
  • Duellman, W.E., Trueb, L. Biology of Amphibians. Baltimore and London, The Johns Hopkins University Press, 1994.
  • Iwasawa, H., Futagami, J., Normal stages of development of a Tree Frog, Hyla japonica Günther. Jpn. J. Herpetol., 14 (1992), 129–142. (in Japanese with English abstract)
  • Rugh, R., Experimental embryology; techniques and procedures. Burgess Publishing, Minneapolis, 1962.
  • Volpe, E.P., Embryonic temperature tolerance and rate of development in Bufo valliceps, Physiological Zoology, 30 (2) (1957), 164–176.
  • Ao, J.M., Development of Hyla annectans Jerdon, 1870 from Nagaland, India, Rüsıe: A Journal Of Contemporary Scıentıfıc, Academıc and Socıal Issues, 2 (2015), 6–11.
  • Sayim, F., Kaya, U., Embryonic development of the tree frog, Hyla arborea, Biologia, 63 (2008), 588–593. https://doi.org/10.2478/s11756-008-0086-z
  • McLaren, I.A., Cooley, J.M., Temperature adaptation of embryonic development rate among frogs, Physiological Zoology, 45 (3) (1972), 223–228.
  • Salthe, S.N., Duellman, W.E., Quantitative constraints associated with reproductive mode in anurans, In: Evolutionary Biology of the Anurans. Contemporary Research on Major Problems. Vial, JL (ed.). University of Missouri Press. Columbia, Missouri. (1973), 229–249.
  • Kuramoto, M., Embryonic temperature adaptation in development rate of frogs, Physiological Zoology, 48 (4) (1975), 360–366.
  • Kaplan, R.H., Maternal influences on offspring development in the California newt, Taricha torosa, Copeia, (1985), 1028–1035. https://doi.org/10.2307/1445258
  • Seymour, R.S., Bradford, D.F., Respiration of amphibian eggs. Physiological Zoology, 68 (1) (1995), 1–25.
  • Guinnee, M.A., Gardner, A., Howard, A.E., West, S.A., Little, T.J., The causes and consequences of variation in offspring size: a case study using Daphnia, Journal of Evolutionary Biology, 20 (2) (2007), 577–587. https://doi.org/10.1111/j.1420-9101.2006.01253.x
  • Kaplan, R.H., The implications of ovum size variability for offspring fitness and clutch size within several populations of salamanders (Ambystoma), Evolution, 34 (1) (1980), 51-64. https://doi.org/10.2307/2408314
  • Doughty, P., Roberts, J.D., Plasticity in age and size at metamorphosis of Crinia georgiana tadpoles: responses to variation in food levels and deteriorating conditions during development, Australian Journal of Zoology, 51 (3) (2003), 271–284. https://doi.org/10.1071/ZO02075
  • Bradford, D.F., Incubation time and rate of embryonic development in amphibians: the influence of ovum size, temperature, and reproductive mode, Physiological Zoology, 63 (6) (1990), 1157–1180.
  • Beattie, R.C., Tyler‐. Tones, R., Baxter, M.J., The effects of pH, aluminium concentration and temperature on the embryonic development of the European common frog, Rana temporaria, Journal of Zoology, 228 (4) (1992), 557-570. https://doi.org/10.1111/j.1469-7998.1992.tb04455.x
  • Steffen, W., Crutzen, P.J., McNeill, J.R., The Anthropocene: are humans now overwhelming the great forces of nature, Ambio-Journal of Human Environment Research and Management, 36 (8) (2007), 614-621. https://doi.org/10.18574/nyu/9781479844746.003.0006
  • Intergovernmental Panel on Climate Change. "Ipcc." Climate change, 2014
  • Hopkins, W.A., Amphibians as models for studying environmental change, ILAR journal, 48 (3) (2007), 270-277. https://doi.org/10.1093/ilar.48.3.270
  • Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J., Fromentin, J.M., Hoegh-Guldberg, O., Bairlein, F., Ecological responses to recent climate change, Nature, 416 (6879) (2002), 389–395. https://doi.org/10.1038/416389a
  • Bachmann, K., Temperature adaptations of amphibian embryos. The American Naturalist, 103 (930) (1969), 115–130.
  • Guyetant, R., Influence du facteur temperature sur le développement embryonnaire de Rana temporaria et Rana dalmatina, Vie et Milieu, 20 (1969), 231–242.
  • Harkey, G.A., Semlitsch, R.D., Effects of temperature on growth, development, and color polymorphism in the Ornate Chorus Frog Pseudacris ornate, Copeia, 4 (1988), 1001–1007. https://doi.org/10.2307/1445724
  • Kuramoto, M., Embryonic temperature adaptation in development rate of frogs, Physiological Zoology, 48 (4) (1975), 360–366.
  • Mitchell, N.J., Seymour, R.S., Effects of temperature on energy cost and timing of embryonic and larval development of the terrestrially breeding Moss Frog, Bryobatrachus nimbus, Physiological and Biochemical Zoology, 73 (6) (2000), 829–840.
  • Smith, G.D., Hopkins, G. R., Mohammadi, S., Skinner, H.M., Hansen, T., Brodie, E.D., French, S.S., Effects of temperature on embryonic and early larval growth and development in the rough-skinned newt (Taricha granulosa), Journal of Thermal Biology, 51 (2015), 89–95. https://doi.org/10.1016/j.jtherbio.2015.03.010
  • Kaplan, R.H., Phillips, P.C., Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis, Evolution, 60 (1) (2006), 142–156. https://doi.org/10.1111/j.0014-3820.2006.tb01089.x
  • Niehaus, A.C., Angilletta Jr, M.J., Sears, M.W., Franklin, C.E., Wilson, R.S., Predicting the physiological performance of ectotherms in fluctuating thermal environments, Journal of Experimental Biology, 215 (4) (2012), 694–701. https://doi.org/10.1242/jeb.058032
  • Hagstrum, D.W., Milliken, G.A., Modeling differences in insect developmental times between constant and fluctuating temperatures, Annals of the Entomological Society of America, 84 (4) (1991), 369–379. https://doi.org/10.1093/aesa/84.4.369
  • Kingsolver, J.G., Feeding, growth, and the thermal environment of cabbage white caterpillars, Pieris rapae L, Physiological and Biochemical Zoology, 73 (5) (2000), 621–628.
  • Shine, R., Harlow, P.S. Maternal manipulation of offspring phenotypes via nest‐site selection in an oviparous lizard, Ecology, 77 (6) (1996), 1808–1817. https://doi.org/10.2307/2265785
  • Du, W.G., Feng, J.H., Phenotypic effects of thermal mean and fluctuations on embryonic development and hatchling traits in a lacertid lizard, Takydromus septentrionalis, Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 309 (3) (2008), 138–146. https://doi.org/10.1002/jez.442
  • Kingsolver, J.G., Ragland, G.J., Diamond, S.E., Evolution in a constant environment: thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta. Evolution, 63 (2) (2009), 537–541.
  • Georges, A., Beggs, K., Young, J.E. and Doody, J.S., Modelling development of reptile embryos under fluctuating temperature regimes, Physiological and Biochemical Zoology, 78 (1) (2005), 18–30. https://doi.org/10.1111/j.1558-5646.2008.00568.x
  • Yee, E. H., Murray, S. N., Effects of temperature on activity, food consumption rates, and gut passage times of seaweed‐eating Tegula species (Trochidae) from California, Marine Biology, 145 (2004), 895– 903. https://doi.org/10.1007/s00227-004-1379-6.
Year 2023, , 192 - 207, 30.12.2023
https://doi.org/10.53447/communc.1350057

Abstract

References

  • Callery, E. M., There's more than one frog in the pond: A survey of the Amphibia and their contributions to developmental biology, Seminars in cell & developmental biology, Academic Press, 17 (2006), 80–92. https://doi.org/10.1016/j.semcdb.2005.11.001
  • Gurdon, J.B., Hopwood, N., The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes, International Journal of Developmental Biology, 44 (1) (2000), 43–50.
  • Holtfreter, J., Amphibians. In: Willier, BH.; Weiss, PA.; Hamburger, V. Editors. Analysis of development. W. B. Saunders Company; Philadelphia: (1955), 230–296.
  • Ancel, P., Vintemberger, P., Recherches sur le déterminisme de la symétrie bilatérale dans l’oeuf des Amphibiens, Bulletin biologique de la France et de la Belgique. Suppléments, 31 (1948), 1–182.
  • Barth, L.G., Barth, L.J., Differentiation of Cells of the Rana pipiens Gastrula in Unconditioned Medium, Development, 7 (2) (1959), 210–222. https://doi.org/10.1242/dev.7.2.210
  • Briggs, R., King, T.J., Transplantation of living nuclei from blastula cells into enucleated frogs’ eggs, Proceedings of the National Academy of Sciences, 38 (5) (1952), 455–463. https://doi.org/10.1073/pnas.38.5.455
  • Pasteels, J., Les effets de la centrifugation sur la blastula et la jeune gastrula des Amphibiens: I. Mécanisme de la formation des organes secondaires aux dépens de l'ectoblaste, Development, 1 (2) (1953), 125–145. https://doi.org/10.1242/dev.1.1.5
  • Fankhauser, G., The effects of changes in chromosome number on amphibian development, The Quarterly Review of Biology, 20 (1) (1945), 20-78. https://doi.org/10.1086/394703
  • Harrison, R.G., Experiments in transplanting limbs and their bearing upon the problems of the development of nerves, Journal of experimental zoology, 4 (2) (1907), 239–281.
  • Holtfreter, J., Über die aufzucht isolierter teile des amphibienkeimes: II. Züchtung von keimen und keimteilen in salzlösung. Wilhelm Roux'Archiv für Entwicklungsmechanik der Organismen, 124 (1931), 404–466. https://doi.org/10.1007/BF00652482
  • Spemann, H., Entwickelungsphysiologische Studien am Triton-Ei. Archiv für Entwicklungsmechanik der Organismen, 12 (1901), 224-264 + 1 pI. (V).
  • Spemann, H., Über Transplantationen an Amphibienembryonen im Gastrulastadium. Sitz. Ber. Gesel!, Naturf. Freunde zu Berlin (1916), 306–320.
  • Spemann, H., Experimentelle forschungen zum determinations-und individualitätsproblem, Naturwissenschaften, 7 (1919), 581–591. https://doi.org/10.1007/BF01498212
  • Vogt, W., Morphologische und physiologische Fragen der Primitiventwicklung, Versuche zu ihrer Lösung mittels vitaler Farbmarkierung, Sitz. Ber. Ges. Morph. Physiol. Munchen., 35 (1924), 22–32.
  • Vogt, W., Gestaltungsanalyse am Amphibienkeim mit örtlicher Vitalfarbung. II. Gastrulation und Mesodermbildung bei Urodelen und Anuren, Arch. Entw.Mech., 120 (1) (1929), 384–706.
  • Beetschen, J.C., How did urodele embryos come into prominence as a model system?, The International journal of developmental biology, 40 (4) (1996), 629–636.
  • Malacinski, G.M., Rufus R. Humphrey (1892–1977), American Zoologist. 18 (1978), 191–193.
  • Smith, J.J., Putta, S., Zhu, W., Pao, G.M., Verma, I.M., Hunter, T., Bryant, S.V., Gardiner, D.M., Harkins, T.T., Voss, S.R., Genic regions of a large salamander genome contain long introns and novel genes, BMC Genomics, (2009), 10–19. https://doi.org/10.1186/1471-2164-10-19
  • Elinson, R.P., Fertilization in amphibians: the ancestry of the block to polyspermy, International review of cytology, 101 (1986), 59–100. https://doi.org/10.1016/S0074-7696(08)60246-6
  • Iwao, Y., Fertilization in amphibians. In: Tarin, JJ.; Cano, A. Editors. Fertilization in protozoa and metazoan animals, cellular and molecular aspects. Springer-Verlag; Berlin: (2000), 147-191. https://doi.org/10.1007/978-3-642-58301-8-4
  • Johnson, A.D., Richardson, E., Bachvarova, R.F., Crother, B.I., Evolution of the germ line-soma relationship in vertebrate embryos. Reproduction, 141 (3) (2011), 291–300. https://doi.org/10.1530/rep-10-0474
  • Nieuwkoop, P.D., Sutasurya, L.A., Primordial germ cells in the chordates. Cambridge University Press, Cambridge, 1979.
  • Stocum, D.L., The role of peripheral nerves in urodele limb regeneration. European Journal of Neuroscience, 34 (6) (2011), 908–916. https://doi.org/10.1111/j.1460-9568.2011.07827.x
  • Gosner, K.L., A Simplified table for staging Anuran embryos and larvae with notes on identification, Herpetologica, 16 (3) (1960), 183–190.
  • Duellman, W.E., Trueb, L. Biology of Amphibians. Baltimore and London, The Johns Hopkins University Press, 1994.
  • Iwasawa, H., Futagami, J., Normal stages of development of a Tree Frog, Hyla japonica Günther. Jpn. J. Herpetol., 14 (1992), 129–142. (in Japanese with English abstract)
  • Rugh, R., Experimental embryology; techniques and procedures. Burgess Publishing, Minneapolis, 1962.
  • Volpe, E.P., Embryonic temperature tolerance and rate of development in Bufo valliceps, Physiological Zoology, 30 (2) (1957), 164–176.
  • Ao, J.M., Development of Hyla annectans Jerdon, 1870 from Nagaland, India, Rüsıe: A Journal Of Contemporary Scıentıfıc, Academıc and Socıal Issues, 2 (2015), 6–11.
  • Sayim, F., Kaya, U., Embryonic development of the tree frog, Hyla arborea, Biologia, 63 (2008), 588–593. https://doi.org/10.2478/s11756-008-0086-z
  • McLaren, I.A., Cooley, J.M., Temperature adaptation of embryonic development rate among frogs, Physiological Zoology, 45 (3) (1972), 223–228.
  • Salthe, S.N., Duellman, W.E., Quantitative constraints associated with reproductive mode in anurans, In: Evolutionary Biology of the Anurans. Contemporary Research on Major Problems. Vial, JL (ed.). University of Missouri Press. Columbia, Missouri. (1973), 229–249.
  • Kuramoto, M., Embryonic temperature adaptation in development rate of frogs, Physiological Zoology, 48 (4) (1975), 360–366.
  • Kaplan, R.H., Maternal influences on offspring development in the California newt, Taricha torosa, Copeia, (1985), 1028–1035. https://doi.org/10.2307/1445258
  • Seymour, R.S., Bradford, D.F., Respiration of amphibian eggs. Physiological Zoology, 68 (1) (1995), 1–25.
  • Guinnee, M.A., Gardner, A., Howard, A.E., West, S.A., Little, T.J., The causes and consequences of variation in offspring size: a case study using Daphnia, Journal of Evolutionary Biology, 20 (2) (2007), 577–587. https://doi.org/10.1111/j.1420-9101.2006.01253.x
  • Kaplan, R.H., The implications of ovum size variability for offspring fitness and clutch size within several populations of salamanders (Ambystoma), Evolution, 34 (1) (1980), 51-64. https://doi.org/10.2307/2408314
  • Doughty, P., Roberts, J.D., Plasticity in age and size at metamorphosis of Crinia georgiana tadpoles: responses to variation in food levels and deteriorating conditions during development, Australian Journal of Zoology, 51 (3) (2003), 271–284. https://doi.org/10.1071/ZO02075
  • Bradford, D.F., Incubation time and rate of embryonic development in amphibians: the influence of ovum size, temperature, and reproductive mode, Physiological Zoology, 63 (6) (1990), 1157–1180.
  • Beattie, R.C., Tyler‐. Tones, R., Baxter, M.J., The effects of pH, aluminium concentration and temperature on the embryonic development of the European common frog, Rana temporaria, Journal of Zoology, 228 (4) (1992), 557-570. https://doi.org/10.1111/j.1469-7998.1992.tb04455.x
  • Steffen, W., Crutzen, P.J., McNeill, J.R., The Anthropocene: are humans now overwhelming the great forces of nature, Ambio-Journal of Human Environment Research and Management, 36 (8) (2007), 614-621. https://doi.org/10.18574/nyu/9781479844746.003.0006
  • Intergovernmental Panel on Climate Change. "Ipcc." Climate change, 2014
  • Hopkins, W.A., Amphibians as models for studying environmental change, ILAR journal, 48 (3) (2007), 270-277. https://doi.org/10.1093/ilar.48.3.270
  • Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J., Fromentin, J.M., Hoegh-Guldberg, O., Bairlein, F., Ecological responses to recent climate change, Nature, 416 (6879) (2002), 389–395. https://doi.org/10.1038/416389a
  • Bachmann, K., Temperature adaptations of amphibian embryos. The American Naturalist, 103 (930) (1969), 115–130.
  • Guyetant, R., Influence du facteur temperature sur le développement embryonnaire de Rana temporaria et Rana dalmatina, Vie et Milieu, 20 (1969), 231–242.
  • Harkey, G.A., Semlitsch, R.D., Effects of temperature on growth, development, and color polymorphism in the Ornate Chorus Frog Pseudacris ornate, Copeia, 4 (1988), 1001–1007. https://doi.org/10.2307/1445724
  • Kuramoto, M., Embryonic temperature adaptation in development rate of frogs, Physiological Zoology, 48 (4) (1975), 360–366.
  • Mitchell, N.J., Seymour, R.S., Effects of temperature on energy cost and timing of embryonic and larval development of the terrestrially breeding Moss Frog, Bryobatrachus nimbus, Physiological and Biochemical Zoology, 73 (6) (2000), 829–840.
  • Smith, G.D., Hopkins, G. R., Mohammadi, S., Skinner, H.M., Hansen, T., Brodie, E.D., French, S.S., Effects of temperature on embryonic and early larval growth and development in the rough-skinned newt (Taricha granulosa), Journal of Thermal Biology, 51 (2015), 89–95. https://doi.org/10.1016/j.jtherbio.2015.03.010
  • Kaplan, R.H., Phillips, P.C., Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis, Evolution, 60 (1) (2006), 142–156. https://doi.org/10.1111/j.0014-3820.2006.tb01089.x
  • Niehaus, A.C., Angilletta Jr, M.J., Sears, M.W., Franklin, C.E., Wilson, R.S., Predicting the physiological performance of ectotherms in fluctuating thermal environments, Journal of Experimental Biology, 215 (4) (2012), 694–701. https://doi.org/10.1242/jeb.058032
  • Hagstrum, D.W., Milliken, G.A., Modeling differences in insect developmental times between constant and fluctuating temperatures, Annals of the Entomological Society of America, 84 (4) (1991), 369–379. https://doi.org/10.1093/aesa/84.4.369
  • Kingsolver, J.G., Feeding, growth, and the thermal environment of cabbage white caterpillars, Pieris rapae L, Physiological and Biochemical Zoology, 73 (5) (2000), 621–628.
  • Shine, R., Harlow, P.S. Maternal manipulation of offspring phenotypes via nest‐site selection in an oviparous lizard, Ecology, 77 (6) (1996), 1808–1817. https://doi.org/10.2307/2265785
  • Du, W.G., Feng, J.H., Phenotypic effects of thermal mean and fluctuations on embryonic development and hatchling traits in a lacertid lizard, Takydromus septentrionalis, Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 309 (3) (2008), 138–146. https://doi.org/10.1002/jez.442
  • Kingsolver, J.G., Ragland, G.J., Diamond, S.E., Evolution in a constant environment: thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta. Evolution, 63 (2) (2009), 537–541.
  • Georges, A., Beggs, K., Young, J.E. and Doody, J.S., Modelling development of reptile embryos under fluctuating temperature regimes, Physiological and Biochemical Zoology, 78 (1) (2005), 18–30. https://doi.org/10.1111/j.1558-5646.2008.00568.x
  • Yee, E. H., Murray, S. N., Effects of temperature on activity, food consumption rates, and gut passage times of seaweed‐eating Tegula species (Trochidae) from California, Marine Biology, 145 (2004), 895– 903. https://doi.org/10.1007/s00227-004-1379-6.
There are 59 citations in total.

Details

Primary Language English
Subjects Computational Ecology and Phylogenetics
Journal Section Research Articles
Authors

Şefik Karanlık 0009-0008-1995-963X

Elnaz Najafı-majd 0000-0001-7710-1625

Elif Yıldırım 0000-0001-9614-5754

Uğur Kaya 0000-0002-6718-5842

Early Pub Date November 21, 2023
Publication Date December 30, 2023
Acceptance Date October 3, 2023
Published in Issue Year 2023

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Communications Faculty of Sciences University of Ankara Series C-Biology.

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