Skip to main content
Log in

Morphological and histological changes in digestive tract development during starvation in the miiuy croaker

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

A histological method was used to describe the ontogenetic development of the digestive tract of laboratory-reared miiuy croaker (Miichthys miiuy) and to evaluate the effects of short-term food deprivation on the morphology and histology of the digestive tract. Larvae and juveniles were maintained at 24 °C in a thermostatically controlled system. Three starvation experiments were conducted during different developmental stages: 1–7 days after hatching (dah; prior to benthic swimming); 26–35 dah (during settling); and 42–53 dah (after benthic swimming). According to the structural changes in the ontogenetic development of the digestive tract, three stages were observed. The first stage was from hatching to 3 dah; the digestive tract was undifferentiated in newly hatched larvae and then showed remarkable morphological changes and differentiation. During this period, larvae depended on endogenous nutrition. The second stage (4–20 dah) was a critical period in which larvae transitioned from endogenous feeding to exogenous feeding and the digestive tract fully differentiated into the buccopharynx, oesophagus, stomach, anterior intestine and posterior intestine. Goblet cells and vacuoles appeared in the digestive tract, and pharyngeal teeth and taste buds developed. During the third stage (20–36 dah), the gastric glands developed and the stomach differentiated into the fundic, cardiac and pyloric regions. At 25 dah, pyloric caeca developed and mucosal folds and spiral valves were clearly distinguishable. After 30 dah, the digestive tract did not undergo any noticeable differentiation, indicating the complete development of the digestive system. The wet weight and SGR (specific growth rate) of miiuy croaker larvae and juveniles greatly decreased when they were deprived of food, and compensatory growth was observed in re-feeding juveniles. The livers of starved larvae and juveniles were atrophied and dark coloured, the intestines were transparent and thin, and the stomach cubages were reduced. The histological effects of starvation were mainly evident in the degeneration of cells in digestive organs, as seen in the shrinkage and separation of cells and the loss of intercellular substances in the liver, pancreas, intestine and stomach. These changes became more severe with increased duration of starvation. In addition, the histological structure of the digestive tracts of starved larvae and juveniles partly recovered after re-feeding, and the effects of starvation on miiuy croaker were age dependent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Baglole CJ, Murray HM, Goff GP, Wright GM (1997) Ontogeny of the digestive tract during larval development of yellowtail flounder: a light microscopic and mucous histochemical study. J Fish Biol 51:120–134

    Article  PubMed  Google Scholar 

  • Bisbal GA, Bengtson DA (1995) Development of digestive tract in larval summer flounder. J Fish Biol 47:277–291

    Article  Google Scholar 

  • Blaxter JHS (1992) The effect of temperature on larval fishes. Neth J Zool 42:336–357

    Article  Google Scholar 

  • Buddington RK, Diamond JM (1987) Pyloric caeca of fish: a “new” absorptive organ. Am J Physiol 252:65–76

    Google Scholar 

  • Canino MF, Bailey KM (1995) Gut evacuation of walleye pollock larvae in response to feeding conditions. J Fish Biol 46:389–403

    Article  Google Scholar 

  • Chen BN, Qin JG, Kumar MS (2006) Ontogenetic development of the digestive system in yellowtail kingfish Seriola lalandi larvae. Aquaculture 256:489–501

    Article  Google Scholar 

  • Chen BN, Qin JG, Carragher JF, Clarke SM, Kumar MS, Hutchinson WG (2007) Deleterious effects of food restrictions in yellowtail kingfish Seriola lalandi during early development. Aquaculture 271:326–335

    Article  Google Scholar 

  • Choi Y, Kim JH, Park JY (2002) Marine fishes of korea. Kyohaksa Publ. Co., Ltd, Seoul, p 352

    Google Scholar 

  • Clemmesen C (1993) Improvements in the fluorimetric determination of the RNA and DNA content of individual marine fish larvae. Mar Ecol Prog Ser 100:177–183

    Article  CAS  Google Scholar 

  • Dou SZ, Masuda R, Tanaka M, Tsukamoto K (2005) Effects of temperature and delayed initial feeding on the survival and growth of Japanese flounder larvae. J Fish Biol 66:362–377

    Article  Google Scholar 

  • Elbal MT, Garcia Hernandez MP, Lozano MT, Agulleiro B (2004) Development of the digestive tract of gilthead sea bream (Sparus aurata L.). Light and electron microscopic studies. Aquaculture 234:215–238

    Article  Google Scholar 

  • Galaviz MA, García-Gasca A, Drawbridge M, Álvarez-González CA, López LM (2011) Ontogeny of the digestive tract and enzymatic activity in white seabass, Atractoscion nobilis, larvae. Aquaculture 318:162–168

    Article  CAS  Google Scholar 

  • Gao LJ, Chen LQ, Zhao XQ, Zhuang P (2004) Starvation and compensatory growth of Acipenser schrenckii juveniles-Effects on digestive organs structure and digestive enzymes activity. J Fish Sci China 11(5):413–419

    CAS  Google Scholar 

  • Gawlicka A, Teh SJ, Hung SSO, Hinton DE, de la Noüe J (1995) Histological and histochemical changes in the digestive tract of white sturgeon larvae during ontogeny. Fish Physiol Biochem 14:357–371

    Article  CAS  PubMed  Google Scholar 

  • Gawlicka A, Leggiadro CT, Gallart JW, Douglas SE (2001) Cellular expression of the pepsinogen and gastric proton pump genes in the stomach of winter flounder as determined by in situ hybridization. J Fish Biol 58:529–536

    CAS  Google Scholar 

  • Gisbert E, Doroshov SI (2003) Histology of the developing digestive system and the effect of food deprivation in larval green sturgeon (Acipenser medirostris). Aquat Living Recourses 16:77–89

    Article  Google Scholar 

  • Gisbert E, Rodriguez A, Castelló-Orvay F, Williot P (1998) A histological study of the development of the digestive tract of Siberian sturgeon (Acipenser baeri) during early ontogeny. Aquaculture 167:195–209

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gisbert E, Piedrahita RH, Conklin DE (2004) Ontogenetic development of the digestive system in California halibut (Paralichthys californicus) with notes on feeding practices. Aquaculture 232:455–470

    Article  Google Scholar 

  • Gisbert E, Ortiz-Delgado JB, Sarasquete C (2008) Nutritional cellular biomarkers in early life stages of fish. Histol Histopathol 23:1525–1539

    CAS  PubMed  Google Scholar 

  • Govoni JJ, Boehlert GW, Watanabe Y (1986) The physiology of digestion in fish larvae. Environ Biol Fish 16:59–77

    Article  Google Scholar 

  • Green BS, McCormick MI (1999) Influence of larval feeding history on the body condition of Amphiprion melanopus. J Fish Biol 55:1273–1289

    Article  Google Scholar 

  • Hamlin H, Hurt I, Kling LJ (2000) Histological and morphological evaluations of the digestive tract and associated organs of haddock throughout post-hatching ontogeny. J Fish Biol 57:716–732

    Article  Google Scholar 

  • He T, Xiao ZZ, Liu QH, MaO DY, Xu SH, Xiao YS, Li J (2012) Ontogeny of the digestive tract and enzymes in rock bream Oplegnathus fasciatus (Temminck et Schlegel 1844) larvae. Fish Physiol Biochem 38:297–308

    Article  CAS  PubMed  Google Scholar 

  • Herrera M, Hachero-Cruzado I, Naranjo A, Mancera JM (2010) Organogenesis and histological development of the wedge sole Dicologoglossa cuneata M. Larva with special reference to the digestive system. Rev Fish Biol Fish 20:489–497

    Article  Google Scholar 

  • Hong WS, Zhang QY (2002) Artificial propagation and breeding of marine fish in China. Chin J Oceanol Limnol 20(1):41–51

    Article  Google Scholar 

  • Hong XY, Zhu XP, Chen KC, Pan DB, Li KB (2013) Ontogenetic development of the digestive tract in larvae of American Shad. N Am J Aquac 75(2):220–227

    Article  Google Scholar 

  • Iguchi K, Mizuno N (1999) Early starvation limits survival in amphidromous fishes. J Fish Biol 54:705–712

    Article  Google Scholar 

  • Kaji T, Tanaka M, Takahashi Y, Oka M, Ishibashi N (1996) Preliminary observations on development of Pacific bluefin tuna Thunnus thynnus (Scombridas) larvae reared in the laboratory, with special reference to the digestive system. Mar Freshw Res 47:261–269

    Article  Google Scholar 

  • Kamler E (1992) Early life history of fish: an energetics approach. Fish and Fisheries Series 4, Chapman & Hall, London, p 267

  • Kjorsvik E, Pittman K, Pavlov D (2004) From fertilization to the end of metamorphosisfunctional development. In: Moksness E, Kjorsvik E, Olsen Y (eds) Culture of cold-water marine fish. Blackwell Publishing, Carlton, pp 204–278

    Chapter  Google Scholar 

  • KozarićZ Kuzir S, Petrinec Z, Gjurcvic E, Bozic M (2008) The development of the digestive tract in larval European catfish (Silurus glanis L.). Anat Histol Embryol 37:141–146

    Article  Google Scholar 

  • Kumari U, Yashpal M, Mittal S, Mittal AK (2005) Morphology of the pharyngeal cavity, especially the surface ultrastructure of gill arches and gill rakers in relation to the feeding ecology of the catfish Rita rita (Siluriformes, Bagridae). J Morphol 265:197–208

    Article  PubMed  Google Scholar 

  • Li X, Jiang ZQ, Tan XZ, Jia ZM (2002) Effects of starvation and refeeding on histology of digestive system in Sciaenops ocellatus. J Fish Sci China 9(3):211–214

    Google Scholar 

  • Liu CX, Luo Z, Tan XY, Gong SY (2013) Ontogenetic development of the digestive system in agastric Chinese sucker, Myxocyprinus asiaticus, larvae. J World Aquac Soc 44(3):350–362

    Article  Google Scholar 

  • Lundstedt LM, Bibiano J, Moraes G (2004) Digestive enzymes and metabolic profile of Pseudoplatystoma corruscans (Teleostei: Siluriformes) in response to diet composition. Comp Biochem Physiol 137B:331–339

    Article  CAS  Google Scholar 

  • Mai KS, Yu HR, Ma HM, Duan QY, Gisbert E, Zamboniono Infante JL, Cahu C (2005) A histological study on the development of the digestive system of Pseudosciaena crocea larvae and juveniles. J Fish Biol 67(4):1094–1106

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Önal U, Celik I, Cirik S (2010) Histological development of digestive tract in discus, Symphysodon spp. larvae. Aquac Int 18:589–601

    Article  Google Scholar 

  • Osse JWM, van den Boogaart JGM, van Snik GMJ (1997) Priorities during growth of fish larvae. Aquaculture 155:249–258

    Article  Google Scholar 

  • Peña R, Dumas S, Villalejo-Fuerte M, Ortiz-Galindo JL (2003) Ontogenetic development of the digestive tract in reared spotted sand bass Paralabrax maculatofasciatus larvae. Aquaculture 219:633–644

    Article  Google Scholar 

  • Pradhan PK, Jena JK, Mitra G, Sood N, Gisbert E (2012) Ontogeny of the digestive tract in butter catfish Ompok bimaculatus (Bloch) larvae. Fish Physiol Biochem 38:1601–1617

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro L, Sarasquete C, Dinis MT (1999) Histological and histochemical development of the digestive system of Solea senegalensis (Kaup, 1958) larvae. Aquaculture 171:293–308

    Article  CAS  Google Scholar 

  • Saelee T, Kiriratnikon S, Suwanjarat J, Thongboon L, Pongsuwan K (2011) The development of the digestive system in Clarias nieuhofii larvae: histology and histochemical studies. J Microsc Soc Thail 4:16–19

    Google Scholar 

  • Sánchez-Amaya MI, Ortiz-Delgado JB, García-López Á, Cárdenas S, Sarasquete C (2007) Larval ontogeny of red banded seabream Pagrus auriga (Valenciennes, 1843) with special reference to the digestive system. A histological and histochemical approach. Aquaculture 263:259–279

    Article  Google Scholar 

  • Santamaría CA, Marin de Mateo M, Traveset R, Sala R, Grau A, Pastor E, Sarasquete C, Crespo S (2004) Larval organogenesis in common dentex Dentex dentex L. (Sparidae): histological and histochemical aspects. Aquaculture 237:207–228

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Shan XJ, Dou SZ (2011) Effects of short-term deprivation on the growth and activities of digestive enzymes of miiuy croaker Miichthys miiuy larvae and juveniles. Oceanologia Et Limnologia Sinica 42(2):213–220

    CAS  Google Scholar 

  • Shan XJ, Cao L, Huang W, Dou SZ (2009a) Feeding, morphological changes and allometric growth during starvation in miiuy croaker larvae. Environ Biol Fish 86:121–130

    Article  Google Scholar 

  • Shan XJ, Huang W, Cao L, Xiao ZZ, Dou SZ (2009b) Ontogenetic development of digestive enzymes and effects of starvation in miiuy croaker Miichthys miiuy larvae. Fish Physiol Biochem 35:385–398

    Article  CAS  PubMed  Google Scholar 

  • Shoji J, Aoyam M, Fujimoto H (2002) Susceptibility to starvation by piscivorous Japanese Spanish mackerel Scomberomorus niphonius (Scombridae) larvae at first feeding. Fish Sci 68:59–64

    Article  CAS  Google Scholar 

  • Song ZB, He XF (2000) Effects of starvation on morphology and histology of digestive system in larval and juveniles Silurus meridionalis Chen. Acta Hydrobiol Sin 24(2):155–161

    Google Scholar 

  • Suneetha KB, Folkvord A, Johannessen A (1999) Responsiveness of selected condition measures of herring, Clupea harengus, larvae to starvation in relation to ontogeny and temperature. Environ Biol Fish 54:191–204

    Article  Google Scholar 

  • Theilacker GH, Porter SM (1995) Condition of larval walleye pollock Theragra chalcogramma, in the Western Gulf of Alaska, assessed with histological and shrinkage indices. Fish Bull 93:333–344

    Google Scholar 

  • Theilacker GH, Bailey KM, Canino MF, Porter SM (1996) Variations in larval walleye pollock feeding and condition: a synthesis. Fish Oceanogr 5:112–123

    Article  Google Scholar 

  • Trevinõ L, Alvarez-Gonza´alez CA, Perales-Garcíıa N, Arevalo-Galan L, Uscanga-Martínez A, Marquez-Couturier G, Fernáandez I, Gisbert E (2011) A histological study of the organogenesis of the digestive system in bay snook Petenia splendida Gunther, 1862 from hatching to the juvenile stage. J Appl Ichthyol 27:73–82

    Article  Google Scholar 

  • Verreth JA, Torrelle E, Spazier E, Sluiszen HW (1992) The development of a functional digestive system in the African catfish, Clarias garipinus. J World Aquac Soc 23:286–298

    Article  Google Scholar 

  • Watanabe Y (1984) Morphological and functional changes in rectal epithelium cells of pond smelt during postembryonic development. Bull Jpn Soc Sci Fish 50:805–814

    Article  Google Scholar 

  • Wegner A, Ostaszewska T, Rozek W (2009) The ontogenetic development of the digestive tract and accessory glands of sterlet (Acipenser ruthenus L.) larvae during endogenous feeding. Rev Fish Biol Fish 19:431–444

    Article  Google Scholar 

  • Yang RB, Xie CX, Fan QX, Gao C, Fang LB (2010) Ontogeny of the digestive tract in yellow catfish Pelteobagrus fulvidraco larvae. Aquaculture 302:112–123

    Article  Google Scholar 

  • Yin MC (1991) Studies and its progress in early life history of fish. J Fish Chn 4:348–358

    Google Scholar 

  • Yin MC (1996) Natural mortality of early life stages of fish. Acta Hydrobiol Sin 4:363–372

    Google Scholar 

  • Yu HR (2006) A study on digestive physiology, protein and methionine requirements for larvae of large yellow croaker Pseudosciaena crocea. Doctor thesis of Ocean University of China

  • Yúfera M, Darias MJ (2007) The onset of exogenous feeding in marine fish larvae. Aquaculture 268:53–63

    Article  Google Scholar 

  • Yúfera M, Pascual E, Polo A, Sarasquete MC (1993) Effect of starvation on the feeding ability of gilthead seabream (Sparus aurata L.) larvae at first feeding. J Exp Mar Biol Ecol 169:259–272

    Article  Google Scholar 

  • Zhong JS, Lou B, Yuan J (2005) Study on the early development in larvae and juveniles of Miichthys miiuy. J Shanghai Fish Univ 14(3):231–237

    Google Scholar 

Download references

Acknowledgments

This study was funded by the National Basic Research Program of China (2015CB453300), the International Science & Technology Cooperation Program of China (2013DFA31410) and the Special Fund of the “Taishan Scholar” Project. Special thanks are given to two anonymous reviewers for their valuable and constructive comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiujuan Shan.

Ethics declarations

Conflict of interest

Xiujuan Shan, Hanfeng Quan and Shuozeng Dou declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shan, X., Quan, H. & Dou, S. Morphological and histological changes in digestive tract development during starvation in the miiuy croaker. Fish Physiol Biochem 42, 529–546 (2016). https://doi.org/10.1007/s10695-015-0157-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-015-0157-3

Keywords

Navigation