Morphological features of the Black Sea turbot (Scophthalmus maeoticus) during the period of embryonic development

Main Article Content

A. N. Khanaychenko

http://orcid.org/0000-0002-4334-9996

https://elibrary.ru/author_items.asp?id=873164

V. E. Giragosov

http://orcid.org/0000-0002-1637-7449

https://elibrary.ru/author_items.asp?id=744994

Abstract

Black Sea turbot (hereinafter BST), Scophthalmus maeoticus (Pallas, 1814), is a valuable fish for commercial fishery and promising object of industrial mariculture. Potential fecundity of BST is very high, 3–13 million eggs; however, survival of its progenies during early development in the sea is unpredictable and low (mortality is up to 90 %). In nature fertilized pelagic BST eggs rise to the sea surface in 2–3 hours; BST develop in upper waters being part of neuston till hatching. BST on its early stages of development could be considered the most vulnerable as the embryo is exposed to diverse adverse effects. The survival and physiological state of the larvae at hatching till exogenous feeding depend on the norm of morphological characteristics of the embryos during their development. Our aim was to study the norm of the changes in BST morphological characteristics during embryogenesis. Morphological analysis of the BST embryogenesis stages from fertilization till hatching on the basis of detailed study of intact embryos (> 2000 eggs) sampled from different experimental batches incubated under experimental conditions is presented. Digital photos and videos of alive eggs were taken with Canon PowerShot A720 using binocular microscope MBS-10 at magnification 8×4 and under light inverted microscope Nikon Eclipse TS100, equipped with analog camera, at magnification ×4, ×10, and ×40. The morphological features of embryogenesis in BST before and after fertilization, cleavage, blastulation, gastrulation, epiboly, and neurulation and until hatching are presented by photos with detailed description of transforming embryological structures. Fertilized pelagic BST eggs covered by transparent shell vary from (1.26 ± 0.14) to (1.31 ± 0.15) mm in diameter, have homogenously distributed yolk and a single round transparent oil drop of 0.20–0.21 mm, positioned at the top of the yolk. Scale of timing of morphological changes is presented in relative time units (as a time interval from fertilization until the emergence of morphological structure in percentage of the total duration of embryogenesis, % RT). Cleavage starts at 2.5 % RT. Cell division desynchronizes between the 6th and 7th cleavage, at 128 blastomeres. Yolk syncytial layer controlling processes of epiboly, cells differentiation, and morphogenesis is formed during the 10th–11th mitotic cycle (12 % RT, about 512–1024 cells). From the germ ring registered at 21 % RT, the embryonic shield develops (at 25 % RT), and organize formation of embryonic axis from 20 to 50 % epiboly (31 % RT). During 70–75 % epiboly (40–45 % RT), the neural keel is formed; notochord and optical primordia become visible; Kupffer’s vesicle emerges at the start of segmentation. Optic cups develop, and more than 20 somites are observed at the end of epiboly (49 % RT). By 60 % RT the Kupffer’s vesicle disappears in tail bud formed; lens placodes are formed in optic cups. Notochord vacuolization, myotomes formation, and tail growth are observed by 65 % RT. The caudal part of the body separates from the yolk by 70–75 % RT. About 80 % RT neuromuscular activity starts; heart beating initiates; free tail covers more than 60 % of the yolk; differentiating xantophores give a pinkish hue to the embryo. By 90–95 % RT eye cups with lenses; three symmetric otic capsules with otoliths, melanophores, and xantophores present in the embryo with 33–38 body somites; it performs jerky movements. Prior hatching, the egg shell becomes elastic, stretches, and breaks in the head area. Hatching occurs 114–94 hours after fertilization at +14…+16 °С. By hatching, all organs are formed in bilateral symmetrical BST larva (standard length is (2.53 ± 0.13) to (2.91 ± 0.10) mm), three auditory chambers with otoliths exist, eyes are non-pigmented, intestinal tract is closed; within 3–5 days it develops at the expense of yolk. Description of morphological changes in the BST embryo at norm of development could be used for elaboration of criteria of developing BST eggs both in natural environment and under cultivation conditions.

Article Details

Khanaychenko A. N., Giragosov V. E. Morphological features of the Black Sea turbot (Scophthalmus maeoticus) during the period of embryonic development. Marine Biological Journal, 2019, vol. 4, no. 4, pp. 62-81. doi: 10.21072/mbj.2019.04.4.06
Keywords:
Black Sea turbot, embryogenesis, morphology, Scophthalmus maeoticus
Section
Scientific communications

References

Битюкова Ю. Е. Развитие зрительной рецепции у личинок черноморского калкана Psetta maeotica (Pallas) // Сенсорная физиология рыб / АН СССР, Отд-е физиологии ; [Кольский филиал АН СССР]. Апатиты, 1984. С. 110–112. [Bityukova Yu. E. Razvitie zritel’noi retseptsii u lichinok chernomorskogo kalkana Psetta maeotica (Pallas). Sensornaya fiziologiya ryb / AN SSSR, Otd-e fiziologii ; [Kol’skii filial AN SSSR]. Apatity, 1984, pp. 110–112. (in Russ.)]

Битюкова Ю. Е., Ткаченко Н. К. Влияние солёности на эмбриональное развитие черноморской камбалы калкана Psetta maeotica (Pallas) // Экология моря. 1998. Вып. 47. С. 25–28. [Bityukova Yu. E., Tkachenko N. K. Effect of salinity on the embryonic development of Black Sea turbot Psetta maeotica (Pallas). Ekologiya morya, 1998, iss. 47, pp. 25–28. (in Russ.)]

Битюкова Ю. Е., Ткаченко Н. К., Чепурнов А. В. Термочувствительность калкана Psetta maeotica (Pallas) (Scophthalmidae) в период эмбрионального развития при искусственном выращивании // Вопросы ихтиологии. 1984. Т. 24, вып. 3. С. 459–463. [Bityukova Yu. E., Tkachenko N. K., Chepurnov A. V. Termochuvstvitel’nost’ kalkana Psetta maeotica (Pallas) (Scophthalmidae) v period embrional’nogo razvitiya pri iskusstvennom vyrashchivanii. Voprosy ikhtiologii, 1984, vol. 24, iss. 3, pp. 459–463. (in Russ.)]

Дехник Т. В. Ихтиопланктон Чёрного моря. Киев : Наукова думка, 1973. 235 с. [Dekhnik T. V. Ikhtioplankton Chernogo morya. Kiev : Naukova dumka, 1973, 235 p. (in Russ.)]

Игнатьев С. М., Мельников В. В., Климова Т. Н., Мельник Л. А., Губанов В. В., Бирюкова М. А. Макро- и ихтиопланктон прибрежных районов Крыма летом 2016 г. // Системы контроля окружающей среды. 2017. Вып. 28. С. 93–100. [Ignatiev S. M., Melnikov V. V., Klimova T. N., Melnik L. A., Gubanov V. V., Biryukova M. A. Summer macro- and ichthyoplankton of Crimea coastal areas in 2016. Sistemy kontrolya okruzhayushchei sredy, 2017, iss. 28, pp. 93–100. (in Russ.)]

Макеева А. П. Эмбриология рыб. Москва : Изд-во МГУ, 1992. 246 с. [Makeeva A. P. Embriologiya ryb. Moscow : Izd-vo MGU, 1992, 246 p. (in Russ.)]

Махотин В. В. Эмбриональное и раннее личиночное развитие беломорской трески Gadus morhua marisalbi (Gadidae) // Вопросы ихтиологии. 2016. Т. 56, вып. 2. С. 177–199. [Makhotin V. V. Embryonic and early larval development of White Sea cod Gadus morhua marisalbi (Gadidae). Voprosy ikhtiologii, 2016, vol. 56, iss. 2, pp. 177–199. (in Russ.)]. https://doi.org/10.1134/S0032945216020119

Попова В. П. Особенности биологии размножения черноморской камбалы-калкана Scophthalmus maeoticus maeoticus (Pallas) (наблюдения в море) // Вопросы ихтиологии. 1972. Т. 12, вып. 6. С. 1057–1063. [Popova V. P. Biological characteristics of reproductions Scophthalmus maeoticus (Pallas) (observation in the sea). Voprosy ikhtiologii, 1972, vol. 12, iss. 6, pp. 1057–1063. (in Russ.)]

Терещенко В. А., Битюкова Ю. Е., Ткаченко Н. К. Движения зародышей камбалы калкана Psetta maeotica и изменения механических свойств оболочки икры в период эмбриогенеза // Вопросы ихтиологии. 1992. Т. 32, вып. 6. С. 175–178. [Tereshchenko V. A., Bityukova Yu. E., Tkachenko N. K. Movements of the Black Sea turbot’s, Psetta maeotica, embryos, and changes of the mechanical characteristics of the egg-membrane during embryogenesis. Voprosy ikhtiologii, 1992, vol. 32, iss. 6, pp. 175–178. (in Russ.)]

Ханайченко А. Н., Битюкова Ю. Е. Искусственное разведение камбаловых: история вопроса и перспективы их выращивания на Чёрном море // Рыбное хозяйство Украины. 1999. Т. 4, вып. 7. С. 15–17. [Khanaichenko A. N., Bityukova Yu. E. Iskusstvennoe razvedenie kambalovykh: istoriya voprosa i perspektivy ikh vyrashchivaniya na Chernom more. Rybnoe khozyaistvo Ukrainy, 1999, vol. 4, iss. 7, pp. 15–17. (in Russ.)]

Ханайченко А. Н., Светличный Л. С., Гирагосов В. Е., Губарева Е. С. Дыхание икры черноморского калкана (Scophthalmus maeoticus) как показатель её развития // Журнал Сибирского федерального университета. Серия «Биология». 2017. Т. 10, № 1. С. 9–19. [Khanaychenko A. N., Svetlichny L. S., Giragosov V. E., Hubareva E. S. Respiration of the Black Sea turbot (Scophthalmus maeoticus) eggs as an indicator of its development. Journal of Siberian Federal University. Biology, 2017, vol. 10, no. 1, pp. 9–19. (in Russ.)]. https://doi.org/10.17516/1997-1389-0004

Ханайченко А. Н., Гирагосов В. Е., Баяндина Ю. С., Ельников Д. В. Выживаемость и вариабельность аномалий икры черноморского калкана Psetta maxima maeotica из нерестового стада юго-западного шельфа Крыма // Тези II Міжнар. іхтіол. наук.-практ. конф., Севастополь, 16–19 вересня 2009 р. Севастополь, 2009. С. 156–159. [Khanaichenko A. N., Giragosov V. E., Bayandina Yu. S., El’nikov D. V. Vyzhivaemost’ i variabel’nost’ anomalii ikry chernomorskogo kalkana Psetta maxima maeotica iz nerestovogo stada yugo-zapadnogo shel’fa Kryma. In: Modern problems of theoretical and practical ichthyology : proceedings of the 2nd International ichthyological conference, Sevastopol, Sept. 16–19, 2009. Sevastopol, 2009, pp. 156–159. (in Russ.)]

APROMAR 2018 : La Acuicultura en España / Asociación Empresarial de Acuicultura de España. Chiclana (Cádiz), 2018, 94 p.

Ballard W. W. Morphogenetic movements and fate map of the cypriniform teleost, Catostomus commersoni (Lacepede). Journal of Experimental Zoology, 1982, vol. 219, iss. 3, pp. 301–321. https://doi.org/10.1002/jez.1402190306

Bian X., Zhang X., Gao T., Wan R., Chen S., Sakurai Y. Morphology of unfertilized mature and fertilized developing marine pelagic eggs in four types of multiple spawning flounders. Ichthyological Research, 2010, vol. 57, iss. 4, pp. 343–357. https://doi.org/10.1007/s10228-010-0167-1

Carvalho L., Heisenberg C.-P. The yolk syncytial layer in early zebrafish development. Trends in Cell Biology, 2010, vol. 20, iss. 10, pp. 586–592. https://doi.org/10.1016/j.tcb.2010.06.009

Devauchelle N., Alexandre J. C., Le Corre N., Letty Y. Spawning of turbot (Scophthalmus maximus) in captivity. Aquaculture, 1988, vol. 69, iss. 1–2, pp. 159–184. https://doi.org/10.1016/0044-8486(88)90194-9

Doldán M. J., Cid P., Mantilla L., de Miguel Villegas E. Development of the olfactory system in turbot (Psetta maxima L.). Journal of Chemical Neuroanatomy, 2011, vol. 41, iss. 3, pp. 148–157. https://doi.org/10.1016/j.jchemneu.2011.01.003

Essner J. J., Amack J. D., Nyholm M. K., Harris E. B., Yost H. J. Kupffer’s vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development, 2005, vol. 132, no. 6, pp. 1247–1260. https://doi.org/10.1242/dev.01663

Gibson S., Johnston I. A. Temperature and development in larvae of the turbot Scophthalmus maximus. Marine Biology, 1995, vol. 124, no. 1, pp. 17–25. https://doi.org/10.1007/BF00349142

Kjørsvik E., Pittman K., Pavlov D. From fertilisation to the end of metamorphosis – functional development. In: Culture of cold-water marine fish / E. Moksness, E. Kjørsvik, Y. Olsen (Eds). Oxford : Blackwell Publ. Ltd, 2004, pp. 204–278. http://doi.org/10.1002/9780470995617.ch6

Kondakova E. A., Efremov V. I. Morphofunctional transformations of the yolk syncytial layer during zebrafish development. Journal of Morphology, 2014, vol. 275, iss. 2, pp. 206–216. https://doi.org/10.1002/jmor.20209

Polat H., Özen M. R., Keskin S. Y. The embryonic development of Black Sea turbot (Psetta maxima Linnaeus, 1758) eggs in different incubation temperatures and salinities. Turkish Journal of Fisheries and Aquatic Sciences, 2018, vol. 18, no. 3, pp. 475–482. https://doi.org/10.4194/1303-2712-v18_3_13

Tong S., Xu H., Liu Q. H., Li J., Xiao Z. Z., Ma D. Y. Stages of embryonic development and changes in enzyme activities in embryogenesis of turbot (Scophthalmus maximus L.). Aquaculture International, 2013, vol. 21, iss. 1, pp. 129–142. https://doi.org/10.1007/s10499-012-9540-6