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ABOVE, FIGURE 1. Eggs of red drum Sciaenops ocellatus are about 1 mm in diameter. At about 17 hours after fertilization, these well-developed embryos have very large yolk sacs and a single oil globule that are their source of essential fatty acids. Photo by C. Faulk. Dynamics of Arachidonic Acid Transfer from Diet to Eggs in Red Drum Lee A. Fuiman and Cynthia K. Faulk R A common bottleneck in the successful ed drum (Sciaenops species is a steady supply of production of any species is a steady supply of highocellatus) is a popular sportfish high-quality eggs for grow-out. quality eggs for grow-out. Producing high-quality along the western Atlantic and Producing high-quality eggs eggs often requires the inclusion of wild-caught Gulf of Mexico coastlines from often requires the inclusion marine organisms in the broodstock diet. Virginia, USA to northern of wild-caught marine However, practicing responsible aquaculture Mexico. In the 1970s and organisms in the broodstock means reducing the use of such feed ingredients 1980s, sharp declines in red diet. However, practicing and replacing them, at least partially, with more drum populations led to nearly responsible aquaculture means sustainable ingredients, such as agricultural crops. complete bans on commercial reducing the use of such feed fishing and stricter regulations ingredients and replacing on recreational harvests. As a result, interest in the culture of them, at least partially, with more sustainable ingredients, such this species for the seafood industry and for stock enhancement as agricultural crops. This presents a considerable challenge developed rapidly, and reliable techniques for spawning and rearing to broodstock managers, inasmuch as more sustainable feeds red drum in captivity were soon developed (Chamberlain et al. typically lack nutrients that are vital for the production of high 1990). Since then, worldwide production of red drum has increased quality eggs and larvae, including highly unsaturated fatty acids steadily, particularly over the past decade, from 2,115 t in 2000 to (HUFAs), particularly docosahexaenoic acid (DHA, 22:6 ω-3), 67,339 t in 2011 (FAO 2013). eicosapentaenoic acid (EPA, 20:5ω-3) and arachidonic acid (ARA, (CONTINUED ON PAGE 60) A common bottleneck in the successful production of any 20:4ω-6). W W W.WA S .O R G • W O R L D AQ UACU LT U R E • J U N E 2 014 59 Embryos and pre-feeding larvae (Fig. 1) receive these fatty acids from their yolk. Because marine fishes are unable to manufacture essential HUFAs in sufficient quantities to meet physiological requirements (Tocher 2003), HUFAs contained in yolk ultimately originate from the maternal diet. It is well known that the fatty acid composition of fish eggs reflects that of the broodstock diet (Izquierdo et al. 2001). The period of influence of the maternal diet on egg composition differs among species because the duration of gonadal maturation and feeding patterns prior to and during spawning vary widely (Izquierdo et al. 2001, Johnson 2009). Few studies have attempted to identify the exact timeframe over which this occurs or, more especially, the rate at which egg composition changes in response to a change in maternal diet. Understanding how and when the maternal diet influences egg fatty acid composition would allow hatchery managers to adjust diets and feeding protocols to achieve high-quality eggs while making most efficient use of marine products in the boodstock diet. Recent experiments on red drum Sciaenops ocellatus demonstrate that ARA, one of the important HUFAs, is transferred from the diet to eggs very quickly, depending on the diet history (Fuiman and Faulk 2013a). This suggests that more environmentally sustainable egg production can be achieved. a time course for the incorporation of ARA into eggs. All time courses were approximately linear, so a simple linear regression was used to estimate the incorporation rate of ARA in eggs (IARA, in mg ARA g-1 DW d-1) following the diet change. Simple linear regression was also used to explore how the magnitude of dietary change in ARA (ΔARA = ARApre - ARApost) influenced the dynamics of ARA incorporation into eggs (IARA). Additional details of the experiments, methods and data can be found in Fuiman and Faulk (2013a, b). Results and Discussions In the 15 experiments, ΔARA ranged from -418 to +598 mg wk-1 fish-1. Observable changes in the ARA content of eggs occurred rapidly after the diet shift and followed a linear trend in all experiments (Fig. 2). Incorporation rate (IARA) was directly proportional TOP, FIGURE 2. Selected time courses (4 of 15 to ΔARA (Fig. 3) and 64% of the experiments) illustrating the incorporation of ARA into total variance in IARA was explained red drum eggs following a diet shift. Each data point by ΔARA: IARA = 0.004 + 0.00022 x represents an individual spawn. Numbers within panels ΔARA. denote the magnitude of the diet shift (ΔARA). Data from The immediate source of HUFAs Fuiman and Faulk (2013 a, b). BOTTOM, FIGURE incorporated into eggs by fishes could 3. Relationship between the rate of incorporation of ARA be body stores, such as adipose tissue into red drum eggs (IARA) and the magnitude of the diet and liver, the current diet, or both shift (ΔARA). IARA (± S.E.) was estimated as the slope of (Pavlov et al. 2004). Changes in dietary a linear regression fitted to each time course relating ARA intake of ARA by reproductively active content of the eggs to ΔARA (Fig. 1). Data from Fuiman red drum result in rapid changes (4and Faulk (2013a, b). Study Methods 16 days) in the ARA content of eggs. We conducted 15 diet-shift experiments in which the ARA Changes in fatty acid composition of gilthead seabream Sparus content of the broodstock diet was changed from one level aurata eggs following a dietary shift in ω-3 HUFAs were also (ARApre, in mg ARA wk-1 fish-1) to another (ARApost) and then rapid, within 15 days (Harel et al. 1994). These results indicate measured ARA content of eggs from spawns produced over one a direct pathway for HUFAs from diet to eggs, or at least a very month after the diet shift. Each broodstock tank contained 2-5 short residence time in maternal body stores. Red drum and fish with 1-3 females per tank, which were fed three times per gilthead seabream actively feed during gonadal maturation and week (Monday, Wednesday, Friday). Broodstock diets containing spawning and this may explain the rapid transfer from diet to eggs. the desired levels of ARA were constructed by varying the In contrast, accumulated body stores are likely to play a greater proportions of several diet components, including whole marine role in egg composition for species such as Atlantic cod that cease organisms (shrimp, squid, fish), beef liver, dry commercial feed or substantially decrease feed intake during the spawning season. and an ARA supplement. ARApre and ARApost were calculated The rate of change in the fatty acid profile, particularly in as the mean weekly intake of ARA averaged over 28 days before muscle tissue, is of considerable interest in aquaculture when a plant-based fatty acid profile is “washed out” before harvest by and after the diet shift, respectively. shifting from a more sustainable, less costly plant-based diet to a The ARA content of eggs and diet components was “finishing” diet that includes more marine ingredients. Robin et al. measured by gas chromatography. The series of measurements (2003) proposed a dilution model to describe the rate of change in of ARA concentration of eggs from each experiment represented 60 J U N E 2 014 • W O R L D AQ UACU LT U R E • W W W.WA S .O R G fatty acid composition of somatic tissues after a diet switch. The dilution model predicts that the rate of change in tissue fatty acid content is proportional to the difference between the current and final tissue levels of fatty acids. If the dilution model applies to eggs, the rate of incorporation of ARA in eggs (IARA) would be directly proportional to ΔARA. The results presented here are consistent with this prediction. The dilution model also predicts that the rate of change is greatest immediately after the diet change, diminishing over time as the fatty acid content of the body approaches the final, equilibrated level. However, our data indicated no decrease in IARA through one month of spawning after a diet shift. Equilibration in eggs may be prevented by frequent spawning, which eliminates large amounts of fatty acids from the body and maintains an elevated fatty acid differential between diet and eggs (Fuiman and Faulk 2013a). New approaches for managing egg and larval quality become possible with this understanding of the dynamics of fatty acid transfer from broodstock diet to eggs. Specifically, the strategy used in wash-out studies could be applied to broodstock to achieve levels of fatty acids in eggs that maximize egg and larval quality while minimizing the use of fish-oil-based diet components and reducing feed costs. A sensible approach would include three diets: 1) a non-spawning diet used outside of the spawning season, 2) a maturation diet to fortify eggs and 3) a spawning diet to maintain egg quality during the spawning season. Because the dilution model and our results both indicate that ARA is incorporated into tissues and eggs faster when the dietary change in ARA is large, the maturation diet should contain much more ARA than the non-spawning diet or the spawning diet. The regression equation can be applied to determine the optimal fatty acid content of the non-spawning and maturation diets that minimizes the time and, therefore, the total amount and cost of the higher quality feed required to reach a targeted level of ARA before or shortly after spawning begins. When eggs reach the targeted level on the maturation diet, broodstock would be switched to a spawning diet with a lower ARA level sufficient to maintain egg quality through the spawning period. Our results suggest that the release of eggs may contribute to the IARA level, so the timing of the diet shift may be critical to the effectiveness of this approach. Of course, egg quality is not determined by ARA alone and a variety of nutrients must be present in appropriate quantities. It is not yet known whether other HUFAs or nutrients that are critical determinants of egg quality in red drum follow the same dynamics as ARA. It is also important to determine whether dietary manipulations of some nutrients interfere with incorporation of other nutrients and if diets that enhance transfer of fatty acids to eggs would adversely affect reproductive physiology. Nevertheless, because fish oils are the source of much of the lipid used in broodstock diets, a feeding regime that greatly reduces the use of these oils is a step toward more sustainable aquaculture practices. Acknowledgments Experiments conducted for this study spanned several years and two locations. We are grateful to G. Joan Holt (retired) of the University of Texas Marine Science Institute and Robert Vega of the Texas Parks and Wildlife Department for providing facilities for our experiments. We also thank the staff of both institutions, especially Jeffery Kaiser and Scott Walker, for their important contributions to this project. This research was supported by the National Science Foundation (OCE-0425241), Texas Sea Grant College Program (NA10OAR4170099), and the Guy Harvey Ocean Foundation. All animal procedures used in this study were reviewed and approved by the Institutional Animal Care and Use Committee at the University of Texas at Austin. Contribution number 1676 of the University of Texas Marine Science Institute. Notes Lee A. Fuiman and Cynthia K. Faulk, Fisheries and Mariculture Laboratory, University of Texas Marine Science Institute, 750 Channel View Drive, Port Aransas, Texas 78373, USA. References Chamberlain, G.W., R.J. Miget, and M.G. Haby, editors. 1990. Red Drum Aquaculture. Texas A&M University Sea Grant College Program, TAMU-SG-90-603. FAO (Food and Agriculture Organization of the United Nations). 2013. Global aquaculture production 1950-2011. Accessed Sept. 10, 2013. www.fao.org/fishery/statistics/globalaquaculture-production/query/en Fuiman, L.A. and C.K. Faulk. 2013a. Batch spawning facilitates transfer of an essential nutrient from diet to eggs in a marine fish. Biological Letters 9: 20130593. dx.doi.org/10.1098/ rsbl.2013.0593 Fuiman, L.A. and C.K. Faulk. 2013b. Data from: Batch spawning facilitates transfer of an essential nutrient from diet to eggs in a marine fish. Dryad Digital Repository. doi:10.5061/ dryad.056r5 Harel, M., A. Tandler, G.W. Kissil and S.W. Applebaum. 1994. The kinetics of nutrient incorporation into body tissues of gilthead seabream (Sparus aurata) females and the subsequent effects on egg composition and egg quality. British Journal of Nutrition 72:45-58. Izquierdo, M.S., H. Fernández-Palacios and A.G.J. Tacon. 2001. Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197:25-42. Johnson, R.B. 2009. Lipid deposition in oocytes of teleost fish during secondary oocyte growth. Reviews in Fisheries Science 17:79-99. Pavlov, D., E. Kjorsvik, T. Refsti and O. Andersen. 2004. Broodstock and egg production. pp. 129-203 In: E. Moksness, E. Kjorsvik and Y. Olsen, editors. Culture of Cold-water Marine Fish. Blackwell Publishing Ltd., Oxford, UK. Robin, J.H., C. Regost, J. Arzel and S.J. Kaushik. 2003. Fatty acid profile of fish following a change in dietary fatty acid source: Model of fatty acid composition with a dilution hypothesis. Aquaculture 225: 283-293. Tocher, D.R. Metabolism and functions of lipids and fatty acids in teleost fish. Reviews in Fisheries Science 11:107-184. W W W.WA S .O R G • W O R L D AQ UACU LT U R E • J U N E 2 014 61