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

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.

Keywords

• Fertilization
• cleavage
• gastrula
• tadpole
• growth rate
• ovum size
• gosner stages
• hylidae

References

1. 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
2. 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.
3. Holtfreter, J., Amphibians. In: Willier, BH.; Weiss, PA.; Hamburger, V. Editors. Analysis of development. W. B. Saunders Company; Philadelphia: (1955), 230–296.
4. 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.
5. 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
6. 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
7. 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
8. 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

9. 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.
10. 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
11. Spemann, H., Entwickelungsphysiologische Studien am Triton-Ei. Archiv für Entwicklungsmechanik der Organismen, 12 (1901), 224-264 + 1 pI. (V).
12. Spemann, H., Über Transplantationen an Amphibienembryonen im Gastrulastadium. Sitz. Ber. Gesel!, Naturf. Freunde zu Berlin (1916), 306–320.
13. Spemann, H., Experimentelle forschungen zum determinations-und individualitätsproblem, Naturwissenschaften, 7 (1919), 581–591. https://doi.org/10.1007/BF01498212
14. 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.
15. Vogt, W., Gestaltungsanalyse am Amphibienkeim mit örtlicher Vitalfarbung. II. Gastrulation und Mesodermbildung bei Urodelen und Anuren, Arch. Entw.Mech., 120 (1) (1929), 384–706.
16. 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.
17. Malacinski, G.M., Rufus R. Humphrey (1892–1977), American Zoologist. 18 (1978), 191–193.
18. 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
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
20. 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
21. 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
22. Nieuwkoop, P.D., Sutasurya, L.A., Primordial germ cells in the chordates. Cambridge University Press, Cambridge, 1979.
23. 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
24. Gosner, K.L., A Simplified table for staging Anuran embryos and larvae with notes on identification, Herpetologica, 16 (3) (1960), 183–190.
25. Duellman, W.E., Trueb, L. Biology of Amphibians. Baltimore and London, The Johns Hopkins University Press, 1994.
26. 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)
27. Rugh, R., Experimental embryology; techniques and procedures. Burgess Publishing, Minneapolis, 1962.
28. Volpe, E.P., Embryonic temperature tolerance and rate of development in Bufo valliceps, Physiological Zoology, 30 (2) (1957), 164–176.
29. 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.
30. 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
31. McLaren, I.A., Cooley, J.M., Temperature adaptation of embryonic development rate among frogs, Physiological Zoology, 45 (3) (1972), 223–228.
32. 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.
33. Kuramoto, M., Embryonic temperature adaptation in development rate of frogs, Physiological Zoology, 48 (4) (1975), 360–366.
34. Kaplan, R.H., Maternal influences on offspring development in the California newt, Taricha torosa, Copeia, (1985), 1028–1035. https://doi.org/10.2307/1445258
35. Seymour, R.S., Bradford, D.F., Respiration of amphibian eggs. Physiological Zoology, 68 (1) (1995), 1–25.
36. 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
37. 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
38. 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
39. 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.
40. 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
41. 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
42. Intergovernmental Panel on Climate Change. "Ipcc." Climate change, 2014
43. 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
44. 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
45. Bachmann, K., Temperature adaptations of amphibian embryos. The American Naturalist, 103 (930) (1969), 115–130.
46. Guyetant, R., Influence du facteur temperature sur le développement embryonnaire de Rana temporaria et Rana dalmatina, Vie et Milieu, 20 (1969), 231–242.
47. 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
48. Kuramoto, M., Embryonic temperature adaptation in development rate of frogs, Physiological Zoology, 48 (4) (1975), 360–366.
49. 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.
50. 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
51. 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
52. 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
53. 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
54. 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.
55. 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
56. 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
57. 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.
58. 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
59. 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.