Embryonic Growth and Yolk Depletion during Incubation in the Chinese Skink, Plestiodon chinensis
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摘要
We collected 24 gravid female Chinese skinks(Plestiodon chinensis) to study embryonic growth and yolk depletion during incubation. Females laid eggs between late May and mid-June. Eggs were incubated at 24(± 0.3) ℃. One egg from each clutch was dissected at 5-d intervals starting at laying. Embryonic stages at laying varied from Dufaure and Hubert's(1961) Stage 30-35, with a mean stage of 32.6. Incubation lengths at 24 ℃ varied from 35.1 to 48.3 d, with a mean of 41.5 d. Based on the derived functions describing instantaneous changes in embryo dry mass and yolk dry mass, we identified three phases of embryonic growth or yolk depletion in P. chinensis. Phase 1, from Day 0(at laying) to Day 15(～36% of the way through incubation), was one of minimal transfer of material from yolk to embryo. Phase 2, from Day 15 to Day 32-33(～77%-80% of the way through incubation), was characterized by increasingly rapid embryonic growth or yolk depletion. Phase 3, from Day 32-33 to hatching, was characterized by reduced embryonic growth or yolk depletion. The length of the last embryonic stage(Stage 40 = completely differentiated embryos) accounted for about 28% of incubation length, and the dry mass of the smallest embryos of Stage 40 accounted for only ～48% of the hatchling dry mass. Our study adds evidence to the idea that oviposition is not timed to coincide with the onset of rapid embryonic growth in oviparous reptiles, and is first to demonstrate that ～50% embryonic growth occurs in the last quarter of incubation in P. chinensis.
We collected 24 gravid female Chinese skinks(Plestiodon chinensis) to study embryonic growth and yolk depletion during incubation. Females laid eggs between late May and mid-June. Eggs were incubated at 24(± 0.3) ℃. One egg from each clutch was dissected at 5-d intervals starting at laying. Embryonic stages at laying varied from Dufaure and Hubert's(1961) Stage 30-35, with a mean stage of 32.6. Incubation lengths at 24 ℃ varied from 35.1 to 48.3 d, with a mean of 41.5 d. Based on the derived functions describing instantaneous changes in embryo dry mass and yolk dry mass, we identified three phases of embryonic growth or yolk depletion in P. chinensis. Phase 1, from Day 0(at laying) to Day 15(～36% of the way through incubation), was one of minimal transfer of material from yolk to embryo. Phase 2, from Day 15 to Day 32-33(～77%-80% of the way through incubation), was characterized by increasingly rapid embryonic growth or yolk depletion. Phase 3, from Day 32-33 to hatching, was characterized by reduced embryonic growth or yolk depletion. The length of the last embryonic stage(Stage 40 = completely differentiated embryos) accounted for about 28% of incubation length, and the dry mass of the smallest embryos of Stage 40 accounted for only ～48% of the hatchling dry mass. Our study adds evidence to the idea that oviposition is not timed to coincide with the onset of rapid embryonic growth in oviparous reptiles, and is first to demonstrate that ～50% embryonic growth occurs in the last quarter of incubation in P. chinensis.
We collected 24 gravid female Chinese skinks(Plestiodon chinensis) to study embryonic growth and yolk depletion during incubation. Females laid eggs between late May and mid-June. Eggs were incubated at 24(± 0.3) ℃. One egg from each clutch was dissected at 5-d intervals starting at laying. Embryonic stages at laying varied from Dufaure and Hubert's(1961) Stage 30-35, with a mean stage of 32.6. Incubation lengths at 24 ℃ varied from 35.1 to 48.3 d, with a mean of 41.5 d. Based on the derived functions describing instantaneous changes in embryo dry mass and yolk dry mass, we identified three phases of embryonic growth or yolk depletion in P. chinensis. Phase 1, from Day 0(at laying) to Day 15(～36% of the way through incubation), was one of minimal transfer of material from yolk to embryo. Phase 2, from Day 15 to Day 32-33(～77%-80% of the way through incubation), was characterized by increasingly rapid embryonic growth or yolk depletion. Phase 3, from Day 32-33 to hatching, was characterized by reduced embryonic growth or yolk depletion. The length of the last embryonic stage(Stage 40 = completely differentiated embryos) accounted for about 28% of incubation length, and the dry mass of the smallest embryos of Stage 40 accounted for only ～48% of the hatchling dry mass. Our study adds evidence to the idea that oviposition is not timed to coincide with the onset of rapid embryonic growth in oviparous reptiles, and is first to demonstrate that ～50% embryonic growth occurs in the last quarter of incubation in P. chinensis.
引文
Andrews R.M.2004.Patterns of embryonic development.In:Deeming,D.C.(Ed.),Reptilian Incubation:Environment,Evolution,and Behaviour.Nottingham:Nottingham University Press,229-251
Booth D.T.,Yu C.Y.2009.Influence of the hydric environment on water exchange and hatchlings of rigid-shelled turtle eggs.Physiol Biochem Zool,82:382-387
Cai Y.,Zhou T.,Ji X.2007.Embryonic growth and mobilization of energy and material in oviposited eggs of the red-necked keelback,Rhabdophis tigrinus lateralis.Comp Biochem Physiol A,147:57-63
Du W.G.,Ji X.,Xu W.Q.2001.Dynamics of material and energy during incubation in the soft-shelled turtle(Pelodiscus sinensis).Acta Zool Sin,47:371-375
Dufaure J.P.,Hubert J.1961.Table de développement du lézard vivipare:Lacerta(Zootoca)vivipara Jacquin.Arch Anat Microsc Morphol Exp,50:309-328
Fischer R.U.,Mazzotti F.J.,Congdon J.D.,Gatten R.E.1991.Post-hatching yolk reserves:parental investment in American alligators from Louisiana.J Herpetol,25:253-256
Ji X.,Bra?a F.1999.The influence of thermal and hydric environments on incubating eggs and embryonic use of energy and nutrients in the wall lizard Podarcis muralis.Comp Biochem Physiol A,124:205-213
Ji X.,Sun P.Y.,Fu S.Y.,Zhang H.S.1997.Utilization of energy and nutrients in incubating eggs and post-hatching yolk in a colubrid snake,Elaphe carinata.Herpetol J,7:7-12
Ji X.,Sun P.Y.,Fu S.Y.,Zhang H.S.1999.Utilization of energy and material in eggs and post-hatching yolk in an oviparous snake,Elaphe taeniura.Asiat Herpetol Res 8:53-59
Ji X.,Zhang C.H.2001.Effects of thermal and hydric environments on incubating eggs,hatching success and hatchling traits in the Chinese skink(Eumeces chinensis).Acta Zool Sin,47:250-259
Kolá?kováM.,Prok?pkováL.,Albrecht T.,Ho?ák D.2015.Incubation temperature influences trade-off between structural size and energy reserves in mallard hatchlings.Physiol Biochem Zool,88:1-10
Lin Z.H.,Ji X.2000.Food habits,sexual dimorphism and female reproduction of the skink(Eumeces chinensis)from a Lishui population in Zhejiang.Acta Ecol Sin,20:304-310
Lu H.L.,Hu R.B.,Ji X.2009.Embryonic growth and mobilization of energy and material during incubation in the checkered keelback snake,Xenochrophis piscator.Comp Biochem Physiol A,152:214-218
Lu H.L.,Lin Z.H.,Li H.,Ji X.2014.Geographic variation in hatchling size in an oviparous skink:effects of maternal investment and incubation thermal environment.Biol J Linn Soc,113:283-296
Ma L.,Lin Z.H.,Gao J.F.,Li H.,Ji X.,Lu H.L.2018.Maternal thermal effects on female reproduction and hatchling phenotype in the Chinese skink(Plestiodon chinensis).Asian Herpetol Res,9:250-257
Packard M.J.,Packard G.C.,Miller J.D.,Jones M.E.,Gutzke W.H.N.1985.Calcium mobilization,water balance,and growth in embryos of the agamid lizard Amphibolurus barbata.J Exp Zool,235:349-357
Qu Y.F.,Lu H.L.,Li H.,Ji X.2014.Incubation temperature fluctuation does not affect incubation length and hatchling phenotype in the Chinese skink Plestiodon chinensis.J Therm Biol,46:10-15
Qu Y.F.,Zhao S.Z.,Jiang X.F.,Lin L.H.,Ji X.2019.Can snakes use yolk reserves to maximize body size at hatching?Curr Zool,doi:10.1093/cz/zoy098
Shadrix C.A.,Crotzer D.R.,McKinney S.L.,Stewart J.R.1994 Embryonic growth and calcium mobilization in oviposited eggs of the scincid lizard,Eumeces fasciatus.Copeia,1994:493-498
Shen W.,Pei J.C.,Lin L.H.,Ji X.2017.Effects of constant versus fluctuating incubation temperatures on hatching success,incubation length and hatchling morphology in the Chinese skink(Plestiodon chinensis).Asian Herpetol Res,8:262-268
Shine R.1983.Reptilian reproductive modes:the oviparityviviparity continuum.Herpetologica,39:1-8
Thompson M.B.,Stewart J.R.1997.Embryonic metabolism and growth of the genus Eumeces.Comp Biochem Physiol A,118:647-654
Wu Y.Q.,Qu Y.F.,Wang X.J.,Gao J.F.,Ji X.2017.Does the oviparity-viviparity transition alter the partitioning of yolk in embryonic reptiles?BMC Evol Biol,17:235
Xu X.F.,Wu Y.L.2003.Changes of material and energy in eggs of lacertid lizards,Eremias brenchleyi during incubation at Mount Qianshan,Anhui.Zool Res,24:106-110
Xu X.F.,Wu Y.L.,Zhang J.L.2004.Dynamics of material and energy during incubation in the grass lizards Takydromus septentrionalis.Acta Zool Sin,50:37-42
Booth D.T.,Yu C.Y.2009.Influence of the hydric environment on water exchange and hatchlings of rigid-shelled turtle eggs.Physiol Biochem Zool,82:382-387
Cai Y.,Zhou T.,Ji X.2007.Embryonic growth and mobilization of energy and material in oviposited eggs of the red-necked keelback,Rhabdophis tigrinus lateralis.Comp Biochem Physiol A,147:57-63
Du W.G.,Ji X.,Xu W.Q.2001.Dynamics of material and energy during incubation in the soft-shelled turtle(Pelodiscus sinensis).Acta Zool Sin,47:371-375
Dufaure J.P.,Hubert J.1961.Table de développement du lézard vivipare:Lacerta(Zootoca)vivipara Jacquin.Arch Anat Microsc Morphol Exp,50:309-328
Fischer R.U.,Mazzotti F.J.,Congdon J.D.,Gatten R.E.1991.Post-hatching yolk reserves:parental investment in American alligators from Louisiana.J Herpetol,25:253-256
Ji X.,Bra?a F.1999.The influence of thermal and hydric environments on incubating eggs and embryonic use of energy and nutrients in the wall lizard Podarcis muralis.Comp Biochem Physiol A,124:205-213
Ji X.,Sun P.Y.,Fu S.Y.,Zhang H.S.1997.Utilization of energy and nutrients in incubating eggs and post-hatching yolk in a colubrid snake,Elaphe carinata.Herpetol J,7:7-12
Ji X.,Sun P.Y.,Fu S.Y.,Zhang H.S.1999.Utilization of energy and material in eggs and post-hatching yolk in an oviparous snake,Elaphe taeniura.Asiat Herpetol Res 8:53-59
Ji X.,Zhang C.H.2001.Effects of thermal and hydric environments on incubating eggs,hatching success and hatchling traits in the Chinese skink(Eumeces chinensis).Acta Zool Sin,47:250-259
Kolá?kováM.,Prok?pkováL.,Albrecht T.,Ho?ák D.2015.Incubation temperature influences trade-off between structural size and energy reserves in mallard hatchlings.Physiol Biochem Zool,88:1-10
Lin Z.H.,Ji X.2000.Food habits,sexual dimorphism and female reproduction of the skink(Eumeces chinensis)from a Lishui population in Zhejiang.Acta Ecol Sin,20:304-310
Lu H.L.,Hu R.B.,Ji X.2009.Embryonic growth and mobilization of energy and material during incubation in the checkered keelback snake,Xenochrophis piscator.Comp Biochem Physiol A,152:214-218
Lu H.L.,Lin Z.H.,Li H.,Ji X.2014.Geographic variation in hatchling size in an oviparous skink:effects of maternal investment and incubation thermal environment.Biol J Linn Soc,113:283-296
Ma L.,Lin Z.H.,Gao J.F.,Li H.,Ji X.,Lu H.L.2018.Maternal thermal effects on female reproduction and hatchling phenotype in the Chinese skink(Plestiodon chinensis).Asian Herpetol Res,9:250-257
Packard M.J.,Packard G.C.,Miller J.D.,Jones M.E.,Gutzke W.H.N.1985.Calcium mobilization,water balance,and growth in embryos of the agamid lizard Amphibolurus barbata.J Exp Zool,235:349-357
Qu Y.F.,Lu H.L.,Li H.,Ji X.2014.Incubation temperature fluctuation does not affect incubation length and hatchling phenotype in the Chinese skink Plestiodon chinensis.J Therm Biol,46:10-15
Qu Y.F.,Zhao S.Z.,Jiang X.F.,Lin L.H.,Ji X.2019.Can snakes use yolk reserves to maximize body size at hatching?Curr Zool,doi:10.1093/cz/zoy098
Shadrix C.A.,Crotzer D.R.,McKinney S.L.,Stewart J.R.1994 Embryonic growth and calcium mobilization in oviposited eggs of the scincid lizard,Eumeces fasciatus.Copeia,1994:493-498
Shen W.,Pei J.C.,Lin L.H.,Ji X.2017.Effects of constant versus fluctuating incubation temperatures on hatching success,incubation length and hatchling morphology in the Chinese skink(Plestiodon chinensis).Asian Herpetol Res,8:262-268
Shine R.1983.Reptilian reproductive modes:the oviparityviviparity continuum.Herpetologica,39:1-8
Thompson M.B.,Stewart J.R.1997.Embryonic metabolism and growth of the genus Eumeces.Comp Biochem Physiol A,118:647-654
Wu Y.Q.,Qu Y.F.,Wang X.J.,Gao J.F.,Ji X.2017.Does the oviparity-viviparity transition alter the partitioning of yolk in embryonic reptiles?BMC Evol Biol,17:235
Xu X.F.,Wu Y.L.2003.Changes of material and energy in eggs of lacertid lizards,Eremias brenchleyi during incubation at Mount Qianshan,Anhui.Zool Res,24:106-110
Xu X.F.,Wu Y.L.,Zhang J.L.2004.Dynamics of material and energy during incubation in the grass lizards Takydromus septentrionalis.Acta Zool Sin,50:37-42