Download Dynamics of Arachidonic Acid Transfer from Diet to Eggs in Red Drum

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).
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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
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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.
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