Elsevier

Aquaculture

Volume 318, Issues 1–2, 27 July 2011, Pages 138-144
Aquaculture

Developmental changes of digestive enzymes in Persian sturgeon (Acipenser persicus) during larval ontogeny

https://doi.org/10.1016/j.aquaculture.2011.04.032Get rights and content

Abstract

The development of digestive enzymes from the stomach (pepsin), pancreas (trypsin, chymotrypsin, α-amylase and lipase) and intestine (alkaline phosphatase) was studied in Persian sturgeon (Acipenser persicus) from hatching to the juvenile stage at 40 days post hatching (dph). Larvae were obtained from artificial propagation of one male and one female and transferred to larval culture tanks where, after yolk sac absorption (9 dph at 17–18 °C), they were fed with Artemia urmiana and Daphnia sp. The assessment of the activity of digestive enzymes showed that at the onset of exogenous feeding, gastric glands were already functional as indicated by the increase in pepsin specific activity. In contrast, alkaline proteases like trypsin and chymotrypsin decreased their specific activity after the onset of exogenous feeding, indicating the importance of these types of enzymes in the cleavage of yolk proteins during the endogenous feeding phase and the replacement of the larval alkaline-type digestion by a juvenile-type acid digestion. After the first feeding, amylase and lipase specific activities increased. Such increments in the activity of amylase might be genetically programmed to better digest carbohydrates in diets with the goal of sparing proteins during the larval stage, whereas the increase in lipase was related to changes in the lipid content of live prey and the progressive maturation of the pancreatic function during larval development. Changes in enzyme activities from the stomach and pancreas were coupled with that in the intestine (brush border membrane), where the specific activity of alkaline phosphatase progressively increased until 19–24 dph and remained constant thereafter, indicated the maturation of the intestine and the achievement of a juvenile-like mode of digestion. Considering these data on the digestive enzymes from the pancreas, stomach and intestine, Persian sturgeon larvae might be weaned around 19–24 dph, as larvae have achieved the complete maturation of their digestive functions by this date. This developmental process, and particularly for the digestive functions, can be considered as a reference to evaluate the effect of a formulated micro diets feeding on larvae.

Introduction

Persian sturgeon (Acipenser persicus) inhabits in the southern part of the Caspian Sea, being one of the most important components of the Caspian Sea ichthyofauna. In the mid-1980s, this sturgeon species constituted 85% of the standing stock of the world sturgeon population (Abhari and Tavakkoli, 1999), although the population collapsed in the 1970s (Moghim et al., 2006). Persian sturgeon is among the most vulnerable fish species because of overfishing for meat and caviar production, destruction of their spawning grounds and water pollution; this species is currently included in the IUCN Red Data List. For these reasons, most research in recent years has been focused on the culture of Persian sturgeon for restocking and commercial aquaculture programs. In this sense, there is a sturgeon stock replenishment program in Iran since 1972. The development of hatchery technology for sturgeon larvae rearing has become necessary in order to grow these fishes up to fingerling size for restocking and aquaculture purposes. Traditionally, hatchery-produced sturgeon larvae and fingerlings were raised on live food organisms, e.g., oligochaetes (Enchytraeus sp. and Tubifex sp.), daphnia (Daphnia sp. and Moina sp.) and Artemia sp. (see review in Gisbert and Williot, 2002). However, the production of live food is a labor-intensive and expensive process, since their production and enrichment require of considerable space, manpower and labor. Moreover, the nutritional supplies of live food are often inadequate to complete the growth-out phase. Although moist diets based on natural products (blood and bone meals, silk worms, mineral and vitamin supplements) were formulated in the former U.S.S.R. during the early development of sturgeon hatcheries, their use had limited success and did not replace cultured live feeds. During the last twenty years, several studies have demonstrated that artificial larval diets can be used successfully for intensive commercial culture of several sturgeon species (e.g., Acipenser baerii, A. transmontanus, A. oxyrinchus and A. medirostris) from the onset of exogenous feeding (Bardi et al., 1998, Buddington and Doroshov, 1984, Dabrowski et al., 1985, Gisbert and Doroshov, 2006). However, limited success has been observed when feeding Persian sturgeon larvae with compound diets.

The efficiency of food depends on physiological capacities in fish to digest and transform ingested nutrients (Furne et al., 2008). Digestion mechanisms in fish larvae have been particularly studied during the last 2 decades. Similar to most fish species, sturgeon larvae are not fully developed at hatch and must undergo further development and differentiation before external foods can be properly ingested and digested (Gisbert and Sarasquete, 2000). The ontogenetic development of digestive enzymes reflects the development of the digestive tract and digestive capability of the organism under study and can thus be used as an indicator of nutritional status at an early life stage (Yúfera and Darias, 2007a) and can provide information for determining the appropriate time for weaning in fish culture (Zambonino-Infante and Cahu, 2007). A comprehensive analysis of the ontogenic changes during the early life stages of fish is essential for the design of feeding strategies and formulation of dry diets (Verreth and Segner, 1995). The analysis of digestive enzyme activities is an easy and reliable biochemical method that can provide insight into the digestive physiology in fish larvae, their nutritional condition (Bolasina et al., 2006) and assist in defining the nutritional requirements for several nutrients like proteins, lipids or carbohydrates (Twining et al., 1983).

As Buddington and Doroshov (1986) stated in their review, the composition of digestive enzymes in sturgeons depends on the fish age, diet composition, genetic and other factors. The early development of sturgeons includes three phases: the yolk sac stage, the actively feeding larval period and metamorphosis, during which enzymatic activity reaches a level typical for juveniles and adults (Buddington, 1985, Zółtowska et al., 1999). The ontogenetic development of the digestive enzymes has been described in many marine and freshwater fish species (see review in Zambonino-Infante et al., 2009); however, there is very limited information on acipenserid species with partial information on A. transmontanus (Buddington and Doroshov, 1986), A. baerii (Gisbert et al., 1999, Zółtowska et al., 1999), Huso huso and Acipencer ruthenus (Timeiko and Bondarenko, 1988). No data are available on the ontogenetic development of digestive enzymes in Persian sturgeon.

The aim of this study was to describe the onset and development of the main digestive enzymes (stomach, pancreas and intestine) in Persian sturgeon fed live prey to provide data on the digestive features of larvae and juveniles (from hatching to 40 days after hatching), which will be useful for the development of a formulated compound diet specific for this sturgeon species.

Section snippets

Rearing procedures

Persian sturgeon larval culture was performed at Shahid Rajaee Sturgeon Hatchery Center, (Sari, Mazandaran, Iran; Lat 36°37′ N, Long 53°05′ E). Broodstock was selected from wild breeders originating from the Caspian Sea and stocked in a 75.4 m3 tank with a freshwater supply. Persian sturgeon larvae were obtained from artificial propagation of one male (19 kg) and one female (26 kg) in April–May 2009. The type and dose of hormone administration for artificial propagation were LH-RH-A2 and 5 μg kg 1,

Results

The mean wet body weight and total length (TL) evolution of Persian sturgeon from hatching to the juvenile stage (40 dph) are given in Fig. 1. Newly hatched larvae weighed 16.7 mg and measured 11.2 mm in TL; at the end of the study they measured 921.3 mg and 56.1 mm, respectively. Larval growth in weight showed rapid exponential growth from hatching to 40 dph.

Discussion

Physiological studies during the early stages of development of fish, as well as the evolution of the digestive enzyme activities, are valuable tools for better understanding the nutritional capabilities of young larvae and establishing adequate feeding protocols for optimizing larval mass rearing production (Diaz et al., 1997). In this sense, it is very important to synchronize the physiological digestive status of the larva, measured by its digestive capabilities, with the feeding protocol

Conclusion

This study showed that the live prey feeding schedule commonly used in hatcheries for many freshwater species also allowed the proper development and growth in Persian sturgeon larvae. During larval development, trypsin and chymotrypsin showed decreasing trends in specific activity that were coupled with increasing levels of pepsin activity. These results indicated a progressive transformation of the digestion mode from an alkaline larval digestion, mainly characterized by pancreatic proteases

Acknowledgments

The authors wish to thank to the Tarbiat Modares University (Noor, Iran) for their financial support. Thanks are also extended to the technical staff of Shahid Rajaee Sturgeon Hatchery Center (Sari, Iran) for their valuable practical assistance.

References (53)

  • M.J. Darias et al.

    Ontogeny of pepsinogen and gastric proton pump expression in red porgy (Pagrus pagrus): determination of stomach functionality

    Aquaculture

    (2007)
  • B. Erlanger et al.

    The preparation and properties of two new chromogenic substrates of trypsin

    Arch. Biochem. Biophys.

    (1961)
  • M. Furne et al.

    Effect of starvation and refeeding on digestive enzyme activities in sturgeon (Acipenser naccarii) and trout (Oncorhynchus mykiss)

    Comp. Biochem. Physiol.

    (2008)
  • E. Gisbert et al.

    Development of digestive enzymes in common dentex Dentex dentex during early ontogeny

    Aquaculture

    (2009)
  • S. Kolkovski

    Digestive enzymes in fish larvae and juveniles—implications and applications to formulated diets

    Aquaculture

    (2001)
  • J.P. Lazo et al.

    Characterization of digestive enzymes during larval development of red drum (Sciaenops ocellatus)

    Aquaculture

    (2007)
  • H. Ma et al.

    Activities of selected digestive enzymes during larval development of large yellow croaker (Pseudosciaena crocea)

    Aquaculture

    (2005)
  • R.J. Shields et al.

    Natural copepods are superior to enriched Artemia nauplii as feed for halibut larvae (Hippoglossus hippoglossus) in terms of survival, pigmentation and retinal morphology: relation to dietary essential fatty acids

    J. Nutr.

    (1999)
  • S.S. Twining et al.

    A pepsinogen from rainbow trout

    Comp. Biochem. Physiol.

    (1983)
  • J. Walford et al.

    Development of digestive tract and proteolytic enzyme activity in seabass (Lates calcarifer) larvae and juveniles

    Aquaculture

    (1993)
  • M. Yúfera et al.

    The onset of exogenous feeding in marine fish larvae

    Aquaculture

    (2007)
  • M. Yúfera et al.

    Changes in the gastrointestinal pH from larvae to adult in Senegal sole (Solea senegalensis)

    Aquaculture

    (2007)
  • J.L. Zambonino-Infante et al.

    High dietary lipid levels enhance digestive tract maturation and improve Dicentrarchus labrax larval development

    J. Nutr.

    (1999)
  • J.L. Zambonino-Infante et al.

    Ontogeny of the gastrointestinal tract of marine fish larvae

    Comp. Biochem. Physiol.

    (2001)
  • J.L. Zambonino-Infante et al.

    Dietary modulation of some digestive enzymes and metabolic processes in developing marine fish: applications to diet formulation

    Aquaculture

    (2007)
  • S. Abhari et al.

    Study of Diets in Sturgeon in Kheirud Kenar Fishery Catch Station

    (1999)
  • Cited by (0)

    View full text