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Fish Physiology and Biochemistry

, Volume 43, Issue 6, pp 1613–1628 | Cite as

Histological study of the gastrointestinal tract in longfin yellowtail (Seriola rivoliana) larvae

  • Andressa Teles
  • Joan Salas-Leiva
  • Carlos Alfonso Alvarez-González
  • Enric Gisbert
  • Leonardo Ibarra-Castro
  • Juan Carlos Pérez Urbiola
  • Dariel Tovar-Ramírez
Article

Abstract

This work contributes basic knowledge on larval development of Seriola rivoliana. A histological study describes the development of the digestive tract and accessory glands in S. rivoliana larvae reared under laboratory conditions at 24 °C from hatching to 30 days post-hatching (DPH). At hatching (2.6 ± 0.12 mm), larvae had an undifferentiated digestive tract with a closed straight tube and a large yolk sac with an oil globule. The liver and pancreas were observed at 1 and 2 days, and the mouth and anus opened at day 2. Enriched rotifers were visible in their digestive tract. At the beginning of the pre-flexion stage, a mixed nutritional period was observed. At day 3, exogenous feeding began; the digestive tract became differentiated into the buccopharynx, esophagus, an undifferentiated stomach, and the intestines. Zymogen granules were visible in the exocrine pancreas. At day 4, supranuclear vacuoles were present in the posterior intestine, indicating the beginning of intracellular digestion. At day 5, goblet cells were present in the esophagus and became functional at day 7 in the esophagus and intestine. The buccopharynx goblet cells developed at day 15. The presence of gastric glands and differentiation of the stomach in the fundic, cardiac, and pyloric regions during the post-flexion stage occurred at day 20. This was the onset of the juvenile period and the beginning of weaning; however, a long co-feeding phase is recommended. Pyloric caeca were observed at day 30 (13.6 ± 1.6 mm). These results provide valuable information on S. rivoliana larvae biology and digestive physiology, which should be useful to improve cultivation techniques and identify ecological features involved in ontogeny.

Keywords

Seriola Ontogeny Marine fish Histology Digestive system 

Notes

Acknowledgements

The authors thank Kampachi Farms for providing fertilized eggs; Maria Del Carmen Rodriguez Jaramillo and Maria Eulalia Meza Chavez for technical assistance in preparing histological slides. Funding was provided by Consejo Nacional de Ciencia y Tecnología (CONACYT grant 157763). A.T. is a recipient of CONACYT fellowship (grant 335728) and J.S.L. is a recipient of AMEXCID fellowship (grant 811-06-9616).

References

  1. Blacio E, Darquea J, Rodríguez S (2003) Avances en cultivo de huayaipe, Seriola rivoliana, en las instalaciones del Cenaim. El mundo acuícola 9:21–24Google Scholar
  2. Boglino A, Gisbert E, Darias MJ, Estévez A, Andree KB, Sarasquete C, Ortiz-Delgado JB (2012) Isolipidic diets differing in their essential fatty acid profiles affect the deposition of unsaturated neutral lipids in the intestine, liver and vascular system of Senegalese sole larvae and early juveniles. Comp Biochem Physiol A 162:59–70CrossRefGoogle Scholar
  3. 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 271:326–335CrossRefGoogle Scholar
  4. Chen BN, Qin JG, Kumar MS, Hutchinson W, Clarke S (2006) Ontogenetic development of the digestive system in yellowtail kingfish Seriola lalandi larvae. Aquaculture 256:489–501CrossRefGoogle Scholar
  5. Comabella Y, Hernández Franyutti A, Hurtado A et al (2013) Ontogenetic development of the digestive tract in Cuban gar (Atractosteus tristoechus) larvae. Rev Fish Biol Fish 23:245–260CrossRefGoogle Scholar
  6. Conceição L, Aragão C, Rønnestad I (2011) Proteins. In: Holt GJ (ed) Larval fish nutrition. Wiley-Blackwell, Oxford, pp 83–116CrossRefGoogle Scholar
  7. Darias MJ, Ortiz-Delgado JB, Sarasquete C, Martínez Rodríguez G, Yúfera M (2007) Larval organogenesis of Pagrus pagrus L., 1758 with special attention to the digestive system development. Histol Histopathol 22:753–768PubMedGoogle Scholar
  8. Faccioli CK, Chedid RA, Mori RH, do Amaral AC, RAF B, IBF V, Vicentini CA (2016) Organogenesis of the digestive system in Neotropical carnivorous freshwater catfish Hemisorubim platyrhynchos (Siluriformes: Pimelodidae). Aquaculture 451:205–212CrossRefGoogle Scholar
  9. Galaviz MA, García-Gasca A, Drawbridge M et al (2011) Ontogeny of the digestive tract and enzymatic activity in white seabass, Atractoscion nobilis, larvae. Aquaculture 318:162–168CrossRefGoogle Scholar
  10. Galaviz MA, López LM, García-Gasca A, Álvarez-González CA, True CD, Gisbert E (2015) Digestive system development and study of acid and alkaline protease digestive capacities using biochemical and molecular approaches in totoaba (Totoaba macdonaldi) larvae. Fish Physiol Biochem 41:1117–1130CrossRefPubMedGoogle Scholar
  11. Gisbert E, Giménez G, Fernández I, Kotzamanis Y, Estévez A (2009) Development of digestive enzymes in common dentex Dentex dentex during early ontogeny. Aquaculture 287:381–387CrossRefGoogle Scholar
  12. Gisbert E, Ortiz-Delgado JB, Sarasquete C (2008) Nutritional cellular biomarkers in early life stages of fish. Histol Histopathol 23:1525–1539PubMedGoogle Scholar
  13. Gisbert E, Piedrahita RH, Conklin DE (2004) Ontogenetic development of the digestive system in California halibut (Paralichthys californicus) with notes on feeding practices. Aquaculture 232:455–470CrossRefGoogle Scholar
  14. Gisbert E, Villeneuve L, Zambonino-Infante JL, Quazuguel P, Cahu CL (2005) Dietary phospholipids are more efficient than neutral lipids for long chain polyunsaturated fatty acid supply in European sea bass Dicentrarchus labrax larval development. Lipids 40:609–618CrossRefPubMedGoogle Scholar
  15. Harder W (1976) Anatomy of fishes. E.Schweizerbart’sche Verlagshuchhandlung, StuttgartGoogle Scholar
  16. Hekimoğlu MA, Suzer C, Saka Ş, Fırat K (2014) Enzymatic characteristics and growth parameters of ornamental koi carp (Cyprinus carpio var. koi) larvae fed by Artemia nauplii and cysts. Turk J Fish Aquat Sci 114:125–133Google Scholar
  17. Hopkins KD (1992) Reporting fish growth: a review of the basics. J World Aquacult Soc 23:173–179CrossRefGoogle Scholar
  18. Kaji T, Tanaka M, Takahashi Y, Oka M, Ishibashi N (1996) Preliminary observations on development of Pacific bluefin tuna Tunnus thynnus (Scombridae) larvae reared in the laboratory, with special reference to the digestive system. Mar Freshw Res 47:261–269CrossRefGoogle Scholar
  19. Kaji T, Tanaka M, Oka M, Takeuchi H, Ohsumi S, Teruya K, Hirokawa J (1999) Growth and morphological development of laboratory-reared yellowfin tuna Thunnus albacares larvae and early juveniles, with special emphasis on the digestive system. Fish Sci 65:700–707CrossRefGoogle Scholar
  20. Kissinger KR, García-Ortega A, Trushenski JT (2016) Partial fish meal replacement by soy protein concentrate, squid and algal meals in low fish-oil diets containing Schizochytrium limacinum for longfin yellowtail Seriola rivoliana. Aquaculture 452:37–44CrossRefGoogle Scholar
  21. Kozarić Z, Kužir S, Petrinec Z et al (2008) The development of the digestive tract in larval European catfish (Silurus glanis L.) Anat Histol Embryol 37:141–146CrossRefPubMedGoogle Scholar
  22. Lazo JP, Darias MJ, Gisbert E (2011) Ontogeny of the digestive tract. In: Holt GJ (ed) Larval fish nutrition. Wiley-Blackwell, Oxford, pp 5–46Google Scholar
  23. Ma Z, Guo H, Zheng P (2014) Ontogenetic development of digestive functionality in golden pompano Trachinotus ovatus (Linnaeus 1758). Fish Physiol Biochem 40:1157–1167PubMedGoogle Scholar
  24. Mai K, Yu H, Ma H, Duan Q, Gisbert E, Zambonino Infante J, Cahu C (2005) A histological study on the development of the digestive system of Pseudosciaena crocea larvae and juveniles. J Fish Biol 67:1094–1106CrossRefGoogle Scholar
  25. McGuckin MA, Lindén SK, Sutton TP, Florin H (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265–278CrossRefPubMedGoogle Scholar
  26. Mesa-Rodríguez A, Hernández-Cruz CM, Socorro JA, Fernández-Palacios H, Izquierdo MS, Roo J (2014) Skeletal development and mineralization pattern of the vertebral column, dorsal, anal and caudal fin complex in Seriola Rivoliana (Valenciennes, 1833) larvae. J Aquac Res Dev. doi: 10.4172/2155-9546.1000266
  27. Mesa-Rodríguez A, Hernández-Cruz CM, Betancor MB, Fernández-Palacios H, Izquierdo MS, Roo J (2016) Bone development of the skull, pectoral and pelvic fins in Seriola rivoliana (Valenciennes, 1833) larvae. Fish Physiol Biochem doi. doi: 10.1007/s10695-016-0257-8
  28. Papadakis IE, Kentouri M, Divanach P, Mylonas CC (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 388:76–88CrossRefGoogle Scholar
  29. Papadakis IE, Zaiss MM, Kyriakou Y et al (2009) Histological evaluation of the elimination of Artemia nauplii from larval rearing protocols on the digestive system ontogeny of shi drum (Umbrina cirrosa L.) Aquaculture 286:45–52CrossRefGoogle Scholar
  30. Peña R, Dumas S, Contreras-Olguín M (2016) Organogenesis of the digestive system in Pacific red snapper (Lutjanus peru) larvae. Aquac Res. doi: 10.1111/are.12991
  31. Quiñones-Arreola MF, Arcos-Ortega GF, Gracia-López V, Casillas-Hernández R, Weirich C, Morris T, Ibarra-Gámez C (2015) Desempeño reproductivo y calidad de huevos en reproductores de origen silvestre y domesticado-F1 de jurel Seriola rivoliana bajo las mismas condiciones de cultivo. Lat Am J Aquat Res 43:953–962Google Scholar
  32. Roo J, Fernández-Palacios H, Hernández-Cruz CM, Mesa-Rodriguez A, Schuchardt D, Izquierdo M (2014) First results of spawning and larval rearing of longfin yellowtail Seriola rivoliana as a fast-growing candidate for European marine finfish aquaculture diversification. Aquac Res 45:689–700CrossRefGoogle Scholar
  33. Rønnestad I, Yúfera M, Ueberschär B, Ribeiro L, Sæle Ø, Boglione C (2013) Feeding behaviour and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Rev Aquacult 5:S59–S98CrossRefGoogle Scholar
  34. Sánchez-Amaya MI, Ortiz-delgado JB, García-lópez Á (2007) Larval ontogeny of red banded seabream Pagrus auriga Valenciennes, 1843 with special reference to the digestive system. Histol Histochem Approach 263:259–279Google Scholar
  35. Sanderson SL, Kupferberg SJ (1999) Development and evolution of aquatic larval feeding mechanisms. In: Hall BK, Wake MH (eds) The origin and evolution of larval forms. Academic Press, San Diego, pp 301–377CrossRefGoogle Scholar
  36. Santamaria CA, Marín De Mateo M, Traveset R et al (2004) Larval organogenesis in common dentex Dentex dentex L. (Sparidae): histological and histochemical aspects. Aquaculture 237:207–228CrossRefGoogle Scholar
  37. Sarasquete C, Gisbert E, Ribeiro L, Vieira L, Dinis MT (2001) Glyconjugates in epidermal, branchial and digestive mucous cells and gastric glands of gilthead sea bream, Sparus aurata, Senegal sole, Solea senegalensis and Siberian sturgeon, Acipenser baeri development. Eur J Histochem 45:267–278CrossRefPubMedGoogle Scholar
  38. Shahriari MM, Abtahi B, Rezaei S, Rahdari A (2014) Early ontogenetic development of digestive system in Schizothorax zarudnyi Nikolskii, 1897 (Actinopterygii: Cyprinidae) larvae. Italian J Zool 81:194–203CrossRefGoogle Scholar
  39. Shan X, Quan H, Dou S (2016) Morphological and histological changes in digestive tract development during starvation in the miiuy croaker. Fish Physiol Biochem 42:529–546CrossRefPubMedGoogle Scholar
  40. Sheridan MA (1988) Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp Biochem Physiol B 90:679–690CrossRefPubMedGoogle Scholar
  41. Srichanun M, Tantikitti C, Vatanakul V, Musikarune P (2012) Digestive enzyme activity during ontogenetic development and effect of live feed in green catfish larvae (Mystus nemurus Cuv. & Val.) Songklanakarin J Sci Technol 34:247–254Google Scholar
  42. Solovyev MM, Campoverde C, Öztürk S et al (2016) Morphological and functional description of the development of the digestive system in meagre (Argyrosomus regius): an integrative approach. Aquaculture 464:381–391CrossRefGoogle Scholar
  43. Treviño L, Alvarez-González CA, Perales-García N, Arevalo-Galan L, Uscanga-Martínez A, Marquez-Couturier G, Fernández 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 27:73–82CrossRefGoogle Scholar
  44. Umeda S, Ochiai A (1973) On the development of the structure and function of the alimentary tract of the yellowtail from the larval to the juvenile stage. Bull Jap Soc Sci Fish 39:923–930CrossRefGoogle Scholar
  45. Umeda S, Ochiai A (1975) On the histological structure and function of digestive organs of the fed and starved larvae of the yellowtail, Seriola quinqueradiata. Jpn J Ichthyol 21:213–219Google Scholar
  46. Umeda S, Yamasaki K, Sugimoto M, Ochiai A (1987) On the differentiation and development of the digestive system of the amberjack, Seriola lalandi, from the larval to juvenile stage. Rep USA Mar Biol Stn 9:223–231Google Scholar
  47. Yúfera M, Darias MJ (2007) The onset of exogenous feeding in marine fish larvae. Aquaculture 268:53–63CrossRefGoogle Scholar
  48. Zaiss MM, Papadakis IE, Maingot E et al (2006) Ontogeny of the digestive tract in shi drum (Umbrina cirrosa L.) reared using the mesocosm larval rearing system. Aquaculture 260:357–368CrossRefGoogle Scholar
  49. Zambonino Infante JL, Cahu CL (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol C 130:477–487Google Scholar
  50. Zambonino-Infante J, Gisbert E, Sarasquete C, Navarro I, Gutiérrez J, Cahu CL (2009) Ontogeny and physiology of the digestive system of marine fish larvae. In: Cyrino JEO, Bureau D, Kapoor BG (eds) Feeding and digestive functions of fish. Science Publishers, Enfield, NH, pp 277–344Google Scholar
  51. Zhang J, Yang R, Yang X et al (2016) Ontogeny of the digestive tract in mud loach Misgurnus anguillicaudatus larvae. Aquac Res 47:1180–1190CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Andressa Teles
    • 1
  • Joan Salas-Leiva
    • 1
  • Carlos Alfonso Alvarez-González
    • 2
  • Enric Gisbert
    • 3
  • Leonardo Ibarra-Castro
    • 4
  • Juan Carlos Pérez Urbiola
    • 1
  • Dariel Tovar-Ramírez
    • 1
  1. 1.Laboratorio de Fisiología Comparada y Genómica FuncionalCentro de Investigaciones Biológicas del NoroesteLa PazMexico
  2. 2.Laboratorio de Acuicultura TropicalDACBIOL-UJATVillahermosaMexico
  3. 3.Unitat de Cultius Aqüìcoles, IRTA (Institut de Recerca i Tecnologia Agroalimentàries), IRTA-SRCTarragonaSpain
  4. 4.Centro de Investigación en Alimentación y DesarrolloMazatlánMexico

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