An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects

Xiaoqiang Gao; Lei Hong; Zhifeng Liu; Zhenglong Guo; Yaohui Wang; Jilin Lei

doi:10.1007/s00343-016-5008-2

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An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects

OriginalPaper | Updated：2023-05-16

- An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects
- An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects
- 海洋湖沼学报（英文） 2016年34卷第1期页码：136-152
- Affiliations：
  
  1. College of Fisheries Ocean University of China
  2. Key Laboratory for Sustainable Development of Marine Fisheries Ministry of Agriculture Qingdao Key Laboratory for Marine Fish Breeding and Biotechnology Yellow Sea Fisheries Research Institute Chinese Academy of Fishery Sciences
  3. Jiangsu Zhongyang Group
- Author bio：
- Funds：
  
  Supported by the National Spark Program of China (No. 2012GA690001)
- DOI：10.1007/s00343-016-5008-2
  中图分类号：
- 网络首发：2015-09-09，
  
  纸质出版：2016
- Accepted：
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An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects[J]. 海洋湖沼学报（英文）, 2016,34(1):136-152.

Gao, X., Hong, L., Liu, Z. et al. An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects., Chin. J. Ocean. Limnol. 34, 136–152 (2016). https://doi.org/10.1007/s00343-016-5008-2
An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects[J]. 海洋湖沼学报（英文）, 2016,34(1):136-152. DOI： 10.1007/s00343-016-5008-2.

Gao, X., Hong, L., Liu, Z. et al. An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects., Chin. J. Ocean. Limnol. 34, 136–152 (2016). https://doi.org/10.1007/s00343-016-5008-2 DOI：

摘要

Abstract

We describe organogenesis at a histological level in American shad (Alosa sapidissima) larvae from 0 until 45 days after hatching (DAH). Larval development was divided into four stages based on the feeding mode

external morphological features

and structural changes in the organs: stage 1 (0–2 DAH)

stage 2 (3–5 DAH)

stage 3 (6–26 DAH) and stage 4 (27–45 DAH). At early stage 2 (3 DAH)

American shad larvae developed the initial digestive and absorptive tissues

including the mouth and anal opening

buccopharyngeal cavity

oesophagus

incipient stomach

anterior and posterior intestine

differentiated hepatocytes

and exocrine pancreas. The digestive and absorptive capacity developed further in stages 2 to 3

at which time the pharyngeal teeth

taste buds

gut mucosa folds

differentiated stomach

and gastric glands could be observed. Four defined compartments were discernible in the heart at 4 DAH. From 3 to 13 DAH

the excretory systems started to develop

accompanied by urinary bladder opening

the appearance and development of primordial pronephros

and the proliferation and convolution of renal tubules. Primordial gills were detected at 2 DAH

the pseudobranch was visible at 6 DAH

and the filaments and lamellae proliferated rapidly during stage 3. The primordial swim bladder was first observed at 2 DAH and started to inflate at 9 DAH; from then on

it expanded constantly. The spleen was first observed at 8 DAH and the thymus was evident at 12 DAH. From stage 4 onwards

most organs essentially manifested an increase in size

number

and complexity of tissue structure.

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Keywords

references

Arellano J M, Storch V, Sarasquete C. 2002. Ultrastructural study on the intestine of Senegal sole, Solea senegalensis. J. Appl. Ichthyol., 18 (3): 154–158.

Chantanachookhin C, Seikai T, Tanaka M. 1991. Comparative study of the ontogeny of the lymphoid organs in three species of marine fish. Aquaculture, 99 (1-2): 143–155.

Comabella Y, Franyutti A H, Hurtado A, Canabal J, García-Galano T. 2013. Ontogenetic development of the digestive tract in Cuban gar ( Atractosteus tristoechus ) larvae. Rev. Fish Biol. Fisheries, 23 (2): 245–260.

Conceição L E, Yúfera M, Makridis P, Morais S, Dinis M T. 2010. Live feeds for early stages of fish rearing. Aquaculture Research, 41 (5): 613–640.

Elbal M T, García-Hernández M P, Lozano M T, Agulleiro B. 2004. Development of the digestive tract of gilthead sea bream ( Sparus aurata L.). Light and electron microscopic studies. Aquaculture, 234 (1-4): 215–238.

Falk-Petersen I B. 2005. Comparative organ differentiation during early life stages of marine fish. Fish and Shellfish Immunol ogy, 19 (5): 397–412.

Gao X Q, Hong L, Liu Z F, Guo Z L, Wang Y H, Lei J L. 2015a. The definition of point of no return of larvae and feeding characteristics of Alosa sapidissim a larvae and juvenile. Journal of Fisheries of China, 39 (3): 392–400. (in Chinese with English abstract)

Gao X Q, Hong L, Liu Z F, Guo Z L, Wang Y H, Lei J L. 2015b. The study of allometric growth pattern of American shad larvae and juvenile ( Alosa sapidissima ). Acta Hydrobiologica Sinica, 39 (3): 638–644. (in Chinese with English abstract)

Gisbert E, Piedrahita R H, Conklin D E. 2004. Ontogenetic development of the digestive system in California halibut ( Paralichthys californicus ) with notes on feeding practices. Aquaculture, 232 (1-4): 455–470.

Gisbert E, Sarasquete M C, Williot P, Castelló-Orvay F. 1999. Histochemistry of the development of the digestive system of Siberian sturgeon during early ontogeny. J. Fish Biol., 55 (3): 596–616.

Govoni J J, Boehlert G W, Watanabe Y. 1986. The physiology of digestion in fish larvae. Environ. Biol. Fishes, 16 (1-3): 59–77.

Hachero-Cruzado I, Ortiz-Delgado J B, Borrega B, Herrera M, Navas J I, Sarasquete C. 2009. Larval organogenesis of flatfish brill Scophthalmus rhombus L: histological and histochemical aspects. Aquaculture, 286 (1-2): 138–149.

Hall T E, Smith P, Johnston I A. 2004. Stages of embryonic development in the Atlantic cod Gadus morhua. Journal of Morphology, 259 (3): 255–270.

Hamre K, Yúfera M, Rønnestad I, Boglione C, Conceição L E C, Izquierdo M. 2013. Fish larval nutrition and feed formulation: knowledge gaps and bottlenecks for advances in larval rearing. Reviews in Aquaculture, 5 (S1): S26–S58.

He T, Xiao Z Z, Liu Q H, Ma D Y, Xu S H, Xiao Y S, Li J. 2012. Ontogeny of the digestive tract and enzymes in rock bream Oplegnathus fasciatus (Temminck et Schlegel 1844) larvae. Fish Physiol. Biochem., 38 (2): 297–308.

Hirji K N, Courtney W A M. 1983. Non-specific carboxylic esterase activity in the digestive tract of the perch, Perca fluviatilis L. J. Fish Biol., 22 (1): 1–7.

Hong X Y, Zhu X P, Chen K C, Pan D B, Li K B. 2013. Ontogenetic development of the digestive tract in larvae of American shad. North American Journal of Aquaculture, 75 (2): 220–227.

Hong X Y. 2011. Study on the morphogenesis and histology of the early American shad Alosa sapidissima. Shanghai Ocean University, Shanghai. p.1-60. (in Chinese)

Kato K, Ishimaru K, Sawada Y, Mutsuro J, Miyashita S, Murata O, Kumai H. 2004. Ontogeny of digestive and immune system organs of larval and juvenile kelp grouper Epinephelus bruneus reared in the laboratory. Fisheries Science, 70 (6): 1 061–1 069.

Klauda R J. 1994. Lethal and critical effects thresholds for American shad eggs and larvae exposed to acid and aluminum in the laboratory, with speculation on the potential role of habitat acidification on stock status in Maryland. In: Cooper J E, Eades R J, Klauda R J, Loesch J G eds. Anadromous Alosa Symposium. American Fisheries Society Tidewater Chapter, Bethesda, Maryland. p.7–39.

Kozarić Z, Kužir S, Petrinec Z, Gjurčević E, Božić M. 2008. The development of the digestive tract in larval European catfish ( Silurus glanis L.). Anatomia, histologia, embryologia, 37 (2): 141–146.

Leach S D, Houde E D. 1999. Effects of environmental factors on survival, growth, and production of American shad larvae. Journal of Fish Biology, 54 (4): 767–786.

Leonard J B K, McCormick S D. 1999. Effects of migration distance on whole-body and tissue-specific energy use in American shad ( Alosa sapidissima ). Can. J. Fish. Aquat. Sci., 56 (7): 1 159–1 171.

Leonard J B K, Norieka J F, Kynard B, McCormick S D. 1999. Metabolic rates in an anadromous clupeid, the American shad ( Alosa sapidissima ). J. Comp. Physiol. B, 169 (4-5): 287–295.

Limburg K E, Hattala K A, Kahnle A. 2003. American shad in its native range. In: Limburg K E, Waldman J R eds. Biodiversity, Status, and Conservation of the World’s Shads. American Fisheries Society Symposium 35, Bethesda, Maryland. p.125–140.

Liu Y, Zhang S C, Jiang G L, Yang D, Lian J H, Yang Y W. 2004. The development of the lymphoid organs of lounder, Paralichthys olivaceus, from hatching to 13 months. Fish Shellfish. Immu nol., 16 (5): 621–632.

Mai K, Yu H, Ma H, Duan Q, Gisbert E, Zambonino Infante J L, Cahu C L. 2005. A histological study on the development of the digestive system of Pseudosciaena crocea larvae and juveniles. J. Fish Biol., 67 (4): 1 094–1 106.

Micale V, Garaffo M, Genovese L, Spedicato M T, Muglia U. 2006. The ontogeny of the alimentary tract during larval development in common pandora Pagellus erythrinus L. Aquaculture, 251 (2-4): 354–365.

Morrison C M. 1993. Histology of the Atlantic Cod, Gadus morhua: An Atlas. Part Four: Eleutheroembryo and Larva/ Atlas d’histologie de la morue franche, Gadus morhua. Quatrième partie. Éleuthéro-embryon et larve. Accents Pubns Service. 496p.

Moyano F J, Barros A M, Prieto A, Cañ avate J P, Cá rdenas S. 2005. Evaluación de la ontogenia de enzimas digestivas en larvas de hurta, Pagrus auriga (Pisces: Sparidae). Revista Aquatic, 22 (5): 39–47.

Murray H M, Wright G M, Golf G P. 1994. A study of the posterior esophagus in the winter flounder, Pteuronectes americanus, and the yellowtail flounder, Pleuronectes ferruginea: morphological evidence for pregastric digestion? Can. J. Zool., 72 (7): 1 191–1 198.

Padrós F, Crespo S. 1996. Ontogeny of the lymphoid organs in the turbot Scophthalmus maximus: a light and electron microscope study. Aquaculture, 144 (1-3): 1–16.

Padrós F, Villalta M, Gisbert E, Estévez A. 2011. Morphological and histological study of larval development of the Senegal sole Solea senegalensis: an integrative study. Journal of Fish Biology, 79 (1): 3–32.

Papadakis I E, Kentouri M, Divanach P, Mylonas C C. 2013. Ontogeny of the digestive system of meagre Argyrosomus regius reared in a mesocosm, and quantitative changes of lipids in the liver from hatching to juvenile. Aquaculture, 388-391: 76–88.

Pradhan P K, Jena J K, Mitra G, Sood N, Gisbert E. 2012. Ontogeny of the digestive tract in butter catfish Ompok bimaculatus (Bloch) larvae. Fish Physiol. Biochem., 38 (6): 1 601–1 617.

Ribeiro L, Sarasquete C, Dinis M T. 1999. Histological and histochemical development the digestive system of Solea senegalensis (Kaup, 1858) larvae. Aquaculture, 171 (3-4): 293–308.

Rombough P J. 2004. Gas exchange, ionoregulation, and the functional development of the teleost gill. Am. Fish. Soc. Symp., 40: 47–83.

Sánchez-Amaya M I, Ortiz-Delgado J B, García-López Á, Cardenas S, Sarasquete C. 2007. Larval ontogeny of redbanded seabream Pagrus auriga Valenciennes, 1843 with special reference to the digestive system. A histological and histochemical approach. Aquaculture, 263(1-4): 259–279.

Santamaría C A, De Mateo M M, Traveset R, Sala R, Grau A, Pastorc E, Sarasqueted C, Crespo S. 2004. Larval organogenesis in common dentex Dentex dentex L. (Sparidae): histological and histochemical aspects. Aquaculture, 237(1-4): 207–228.

Schrøder M B, Villena A J, Jørgensen T Ø. 1998. Ontogeny of lymphoid organs and immunoglobulin producing cells in Atlantic cod ( Gadus morhua L.). Developmental & Comparative Immunology, 22(5-6): 507–517.

Scott W B, Crossman W J. 1973. Freshwater Fishes of Canada. Gordon Soules Book Pub. 966p.

Segner H, Rösch R, Schmidt H, Von Poeppinghausen K J. 1989. Digestive enzymes in larval Coregonus lavaretus L. J. Fish Biol., 35(2) 249–263.

Segner H, Rösch R, Verreth J, Witt U. 1993. Larval nutritional physiology: studies with Clarias gariepinus, Coregonus lavaretus and Scophthalmus maximus. J. World Aquacult. Soc., 24(2) 121–134.

Shardo J D. 1995. Comparative embryology of teleostean fishes. I. Development and staging of the American shad, Alosa sapidissima (Wilson, 1811). J. Morphol., 225(2) 125–167.

Stroband H W J, Kroon A G. 1981. The development of the stomach in Clarias lazera and the intestinal absorption of protein macromolecules. Cell Tissue Res., 215(2) 397–415.

Tanaka M, Tanangonan J B, Tagawa M, De Jesus E G, Nishida H, Isaka M, Kimura R, Hirano T. 1995. Development of the pituitary, thyroid and interrenal glands and applications of endocrinology to the improved rearing of marine fish larvae. Aquaculture, 135(1-3): 111–126.

Verreth J A J, Torreele E, Spazier E, Van Der Sluiszen A, Rombout J H W M, Booms R, Segner H. 1992. The development of a functional digestive system in the African catfish, Clarias garipinus (Burchell). J. World Aquacult. Soc., 23(4) 286–298.

Walburg C H, Nichols P R. 1967. Biology and management of the American shad and status of the fisheries, Atlantic coast of the United States, 1960. United States Department of the Interior, Washington, D C. p.1–105.

Wan Z Z, Gao T X, Zhang X M, Chen C, Yu C H. 2006. Histological study on the digestive system development of Takifugu rubripes larvae and juvenile. Journal of Ocean University of China, 5(1) 39–44.

Watts M, Kato K, Munday B L, Burke C M. 2003. Ontogeny of immune system organs in northern bluefin tuna (Thunnus orientalis, Temminck and Schlegel 1844). Aquac. Res., 34(1) 13–21.

Wu H W, Wang B, Shi W et al. 2004. Study on culture technology of American shad (Alosa sapidissima ) on a large scale I. juveniles culturing. Chinese Journal of Fisheries, 17(2) 61–64. (in Chinese with English abstract)

Xiao Z Z, Yu D D, Sun Z Z, Xu S H, Ma D Y, Li J. 2008. Ontogeny of immune organs during early development stage of barfin flounder. Marine Sciences, 32(7) 88–92. (in Chinese with English abstract)

Xiao Z H, He T, Li J, Gao T X. 2013. Ontogeny of the immune system in rock bream Oplegnathus fasciatus. Chinese Journal of Oceanology and Limnology, 31(5): 1028–1 035.

Xu G C, Zhang C X, Zheng J L, Gu R B. 2012. Artificial propagation and embryonic development of American shad, Alosa sapidissima. Marine Sciences, 36(7) 89–96. (in Chinese with English abstract)

Yang R B, Xie C X, Fan Q X, Gao C, Fang L B. 2010. Ontogeny of the digestive tract in yellow catfish Pelteobagrus fulvidraco larvae. Aquaculture, 302(1-2): 112–123.

Yúfera M, Fernández-Díaz C, Pascual E, Sarasquete M C, Moyano F J, Díaz M, Alarcón F J, García-Gallego M, Parra G. 2000. Towards an inert diet for first-feeding gilthead seabream (Sparus aurata L.) larvae. Aquac. Nutr., 6(3) 143–152.

Yúfera M, Ortiz-Delgado J B, Hoffman T, Siguero I, Urup B, Sarasquete C. 2014. Organogenesis of digestive system, visual system and other structures in Atlantic bluefin tuna (Thunnus t hynnus ) larvae reared with copepods in mesocosm system. Aquaculture, 426-427: 126–137.

Zaiss M M, Papadakis I E, Maingot E, Divanach P, Mylonas C C. 2006. Ontogeny of the digestive tract in shi drum (Umbrina cirrosa L.) reared using the mesocosm larval rearing system. Aquaculture, 260(1-4): 357–368.

Zambonino-Infante J L, Cahu C L. 2001. Ontogeny of the gastrointestinal tract of marine fish larvae. Comparative Biochemistry and Physiology Part C, 103(4) 477–487.

Zambonino-Infante J L, Gisbert E, Sarasquete C, Navarro I, Gutiérrez J, Cahu C L. 2008. Ontogeny and physiology of the digestive system of marine fish larvae. In: Cyrino J E O, Bureau D, Kapoor B G eds. Feeding and Digestive Functions of Fishes. Science Publishers Inc., Enfield, USA. p.277–344.

Zapata A, Diez B, Cejalvo T, De Frías C G, Cortés A. 2006. Ontogeny of the immune system of fish. Fish Shellfish. Immu nol., 20(2) 126–136.

Zhang C X, Xu G C, Xu P, Zheng J L, Gu R B. 2010. Morphological development and growth of American shad (Alosa sapidissima ) at larvae, fry and juvenile stages. Journal of Fishery Sciences of China, 17(16): 1227–1 235. (in Chinese with English abstract)

Zydlewski J, McCormick S D. 1997. The ontogeny of salinity tolerance in the American shad, Alosa sapidissima. Canadian Journal of Fisheries and Aquatic Sciences, 54(1) 182–189.

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