Arachidonic acid reduces the stress response of gilthead seabream Sparus aurata L.
1 Department of Animal Ecology and Ecophysiology, Faculty of Science,
University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The
Netherlands
2 Department of Larval Rearing, The National Center for Mariculture, PO Box
1212, Eilat 88112, Israel
* Author for correspondence (e-mail: rvanholt{at}sci.kun.nl)
Accepted 28 June 2004
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Summary |
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Key words: acetylsalicylic acid, arachidonic acid, cyclooxygenase, cortisol, eicosanoid, osmoregulation, prostaglandins, gilthead seabream, Sparus aurata
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Introduction |
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ArA is selectively incorporated into cellular phospholipids, especially
phosphatidylinositol, despite the general abundance of n-3 PUFA in
phospholipids of fish tissues (Linares and
Henderson, 1991). While the structural contribution of ArA to the
membrane appears to be limited, ArA can be rapidly converted into eicosanoids,
which can function as endocrine, paracrine and/or autocrine modulators of
secretory mechanisms in various organs
(Bihoreau et al., 1990
;
Lands, 1991
). The conversion
process begins when stress-related triggers induce the release of ArA within
5-60 s by activating phospholipases, mainly PLA2
(Axelrod et al., 1988
;
Smith, 1989
;
Buschbeck et al., 1999
). It is
often assumed that the effects of dietary ArA on fish are mainly due to its
function as a precursor to these eicosanoids, particularly the prostaglandins
of the 2-series (Beckman and Mustafa,
1992
; Bell et al.,
1995
; Harel et al.,
2001
; Bell and Sargent,
2003
). The prostaglandins are known to control a wide variety of
physiological processes in mammals as well as in fish, including respiratory
and cardiovascular output (McKenzie,
2001
), ovulation and spawning behavior, oocyte maturation, nervous
system function, osmoregulation (Mustafa
and Srivastava, 1989
) and immune functions
(Rowley et al., 1995
).
Furthermore, prostaglandins can modulate the sensitivity of the
hypothalamus-pituitary-adrenal (HPA) axis in mammals at various levels and
alter the release of cortisol and corticosterone in the stress response
(Zacharieva et al., 1992
;
Nye et al., 1997
;
Wang et al., 2000
). In teleost
fish the release of cortisol is controlled by the analogous
hypothalamic-pituitary-interrenal (HPI) axis
(Wendelaar Bonga, 1997
).
Several studies have found indications that ArA, and other PUFA, are involved
in the regulation of cortisol release in fish as well
(Gupta et al., 1985
;
Wales, 1988
;
Harel et al., 2001
;
Koven et al., 2003
). Moreover,
dietary supplementation with ArA clearly reduced the cortisol response of
seabream larvae to air exposure (Van
Anholt et al., 2004
).
The present study was designed to establish the influence of the dietary
level of ArA on the response of adult seabream to an acute stressor. This
could be relevant as attempts are being made to replace fish oil by vegetable
oils as a source of lipids in the production of fish feeds. These oils contain
no C20 and C22 PUFA, which might lead to deficiencies, particularly in marine
fish that depend on a dietary source of these long-chain fatty acids
(Bell, 1998;
Bell and Sargent, 2003
). More
specifically, several studies have indicated that effects of dietary ArA
during the stress response could be attributed to an increased production of
the 2-series prostaglandins (see, for instance,
Gupta et al., 1985
;
Harel et al., 2001
;
Van Anholt et al., 2003
).
Acetylsalicylic acid (ASA) is an irreversible blocker of the COX pathway,
which is responsible for the conversion of ArA into prostaglandins
(Smith, 1989
). The
administration of ASA was an effective and stress-free method for the in
vivo inhibition of the COX pathway in Mozambique tilapia Oreochromis
mossambicus (Van Anholt et al.,
2003
). Therefore, subgroups from each of the low- and high-ArA
treatments were fed ASA before being subjected to an acute stressor to
investigate the role ArA and prostaglandins in the stress response.
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Materials and methods |
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Fish
Male and female gilthead seabream Sparus aurata L. were obtained
from a commercial hatchery (Vendée Aquaculture, La Faute sur Mer,
France) at an approximate mass of 5 g. They were raised in the laboratory of
the University of Nijmegen and fed commercial pellets for seabream and seabass
(crude protein 46%, total lipid 20%, ash 10%, water 5%; Filia LDX, Trouvit,
Fontaine Les Vervins, France) at 2% of their body mass. The fatty acid profile
of these pellets is listed in Table
1. Fish were kept in recirculated synthetic saltwater (Aqua Medic
Sea Salt, Bissendorf, Germany) of 34 and 20°C with a 12 h
photoperiod. The recirculation system was equipped with a protein skimmer,
biological filter and UV-sterilizing unit.
|
Experimental diets
Two types of 4 mm pelleted diets (The National Center for Mariculture,
Eilat, Israel) were used. These diets were identical in their protein, lipid
and micronutrient levels (crude protein 45%, total lipid 19%, ash 11% and
water 8%), but differed in their fatty acid composition. In the `low-ArA'
pellets, fish oil (predominantly capelin oil) was incorporated at 10% of the
pellet dry mass, which contained moderate levels of DHA, EPA and linoleic acid
(LA), while having low levels of ArA. In the other diet (high-ArA diet) 10% of
the fish oil fraction was replaced with ARASCO (Martek Biosciences, Columbia,
MD, USA) to give a final ArA level of 2.4±0.0% of total fatty acids,
compared to 0.9±0.0% of total fatty acids in the low-ArA diet. This
corresponded to 1.9 mg ArA g-1 dry mass and 0.6 mg ArA
g-1 dry mass in the high- and low-ArA pellets, respectively. ARASCO
is a highly purified ArA-rich oil extracted from the fungus Mortierella
alpina, containing 40% ArA of total fatty acids. The fatty acid
compositions of the pellets were determined according to Koven et al.
(2001
) and the results are
listed in Table 1.
Experimental design and stress challenge
In two consecutive trials, 160 seabream (80.7±1.2 g) from the same
cohort were used. Each trial included 80 seabream, which were equally divided
according to mass into eight groups of ten fish. Four groups of ten fish were
fed low-ArA containing pellets, while the other four groups were fed the
high-ArA containing pellets. All fish were fed daily rations of 2% of their
body mass for a period of 18 days. At the end of this period, two groups of
ten fish from each treatment group received three doses of ASA in 2 days (100
mg kg-1 body mass, based on mean mass of the group). ASA was
incorporated into gelatin capsules together with crushed pellets, which were
eaten voluntarily within 5 min, according to the method described by Van
Anholt et al. (2003). On the
second day, approximately 4 h after receiving their last meal or dose of ASA,
several fish were sampled for baseline values. Our previous observations in
tilapia indicated that plasma salicylate levels peaked around 5 h after
administration before declining to basal levels over a 15 h period
(Van Anholt et al., 2003
).
Confinement was therefore timed in such a way that the fish would experience
any stressor-induced peak in plasma cortisol whilst plasma salicylate levels
were still increasing. As plasma salicylate measurements are corrected for
blank readings (<0.14 mmol l-1), the salicylate in control fish
was probably of dietary origin such as vegetable material, a known source of
natural salicylates. The remaining fish were immediately subjected to the
stress challenge, which consisted of 5 min of confinement in a submerged
dip-net. After confinement they were released back into the aquarium and
sampled after 20 min, 60 min or 24 h. Fish were anaesthetized in a 2%
2-phenoxyethanol solution and blood samples were immediately collected from
the caudal vein using heparinized needles. Plasma samples were collected after
centrifugation (16 000 g, 5 min) and stored at -20°C until
analysis. Tissue samples of gills, muscle and kidney were removed immediately
and stored at -30°C until analysis. Gill arches were dissected and stored
frozen in SEI buffer (300 mmol l-1 sucrose, 20 mmol l-1
Na2EDTA, 100 mmol l-1 imidazole, adjusted to pH 7.4 with
Hepes-Tris) until analysis of Na+, K+-ATPase
activity.
Plasma measurements
Cortisol levels were determined using a competitive radioimmunoassay
(Campro Scientific, Veenendaal, The Netherlands) according to the procedure
described in Van Anholt et al.
(2003). Plasma glucose levels
were determined in duplicates with Sigma's INFINITY glucose reagent according
to the manufacturer's protocol (Sigma-Aldrich, Poole, Dorset, UK). Plasma
concentrations of lactate were assayed in duplicate by a standard colorimetric
assay (735-10; Sigma-Aldrich). Plasma concentrations of sodium, potassium and
chloride were determined by flame photometry (Radiometer FLM3, Copenhagen,
Denmark) and plasma osmolality was determined in 50 µl undiluted plasma
samples using an automatic cryoscopic osmometer (Osmomat 030, Gonotec, Berlin,
Germany).
Na+, K+-ATPase activity
Branchial filaments were collected and homogenized in 250 µl SEI buffer
containing aprotinin (5 µl ml-1), and after centrifugation (10
min at 500 g) supernatants were used for analysis. ATPase
activity was determined as the specific release of inorganic phosphate
Pi from ATP, using either 12.5 mmol l-1 KCl or 1 mmol
l-1 ouabain in the medium, according to the method described in Van
Anholt et al. (2003). The
difference between the total ATPase activity and the ouabain-insensitive
ATPase activity was designated as the ouabain-sensitive,
K+-dependent Na+, K+-ATPase activity and
expressed in µmol Pi h-1 mg-1 protein.
The in vitro effect of free ArA on Na+, K+-ATPase activity
Gill and kidney homogenates of eight control fish were pooled and the COX
inhibitor indomethacin (10 µg ml-1 homogenate) was added to
prevent prostaglandin synthesis. The Na+, K+-ATPase
activity was assayed using free ArA in both incubation media, containing KCl
or ouabain, respectively. Stock solutions of free ArA (Sigma, St Louis, MI,
USA) were prepared in 100% methanol and 100x diluted with the reaction
media to their final concentrations, 1-100 µmol l-1 at 1% (v/v)
methanol. Enzyme activity in the presence of added ArA was expressed as a
percentage of the value in the 1% methanol controls.
Statistics
Initial analysis revealed no differences between the two trials and the
results were therefore combined and treated as one experiment. All data are
expressed as means ± S.E.M. Levene's Tests for homogeneity of variances
indicated that log-transformation was required for cortisol data and arcsine
transformations were performed on the percentage data of fatty acids to
achieve homogeneity of variance. Three-way analyses of variance (ANOVAs) were
performed to determine the effects of the factors ArA feeding,
ASA-administration and time of sampling. Post hoc multiple comparison
tests (Tukey's HSD) were used to determine which time points differed
significantly (SPSS software, version 11.5). Effects of free ArA in the in
vitro Na+, K+-ATPase test were compared with
repeated-measures ANOVA against the activity at 1% methanol. 5% level of
probability was accepted as statistically significant.
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Results |
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ArA feeding had no effect on plasma salicylate levels. Salicylate levels were significantly elevated in seabream that received ASA (P<0.001; Table 2). In all four treatments salicylate levels had dropped below those of all other time points after 24 h (P<0.001). Furthermore, a significant interaction existed between ASA administration and time of sampling (P=0.013).
|
Fatty acid profiles of gill, kidney and muscle tissues prior to net confinement (t=0) and 24 h after the stressor (t=24 h) are listed in Table 3, and significant effects are presented in Table 4. Feeding the ArA-supplemented diet for 18 days to seabream significantly increased (P=0.028) the levels of ArA in kidneys and reduced the level of linoleic acid (P=0.046), as well as increased the saturated fatty acid levels (P=0.049). ArA feeding decreased the DHA/ArA and EPA/ArA ratios in kidneys (P<0.001), while reducing the DHA/ArA ratio in gill tissues (P=0.035). In the gills, all major fatty acids were significantly different 24 h after confinement, exhibiting either increasing or declining percentages, except for the DHA/EPA ratio (for details, see Table 4). At the same time the levels of saturated fatty acids in the kidneys were significantly (P=0.029) enhanced by confinement, where muscle tissues exhibited a significant increase (P=0.042) in the DHA/EPA ratio after 24 h. There were no significant interactions between factors in any of tissues tested.
|
|
Within 20 min after confinement plasma cortisol levels increased substantially in all treatments, resulting in significantly higher plasma levels compared to all other time-points (P<0.001; Fig. 1). After 60 min, cortisol levels were no longer significantly elevated compared to the pre-confinement levels. The ArA-supplemented seabream exhibited a significantly lower cortisol response (P=0.012) compared to the fish fed the `low-ArA' diet. In addition, ASA significantly affected the cortisol response (P=0.045). In the low-ArA fed seabream cortisol levels were reduced by ASA, whereas in the high-ArA fed fish cortisol levels were enhanced by ASA. There were no significant interactions between ArA, ASA, and/or the time of sampling.
|
The fish responded to confinement with a significant increase (P<0.001) in plasma glucose at t=20 min, but glucose was no longer significantly different from pre-confinement levels after 60 min (Fig. 2). Glucose levels were significantly influenced by the administration of ASA (P=0.015). Glucose levels were markedly reduced after ASA administration in the seabream fed the low-ArA diet, while glucose levels were not influenced by ArA-supplementation, nor were there any significant interactions between ArA, ASA, and/or time of sampling.
|
Plasma lactate levels increased in all treatments 20 min after confinement (P<0.001; Fig. 3). 1 h later, lactate levels were still significantly higher than prior to confinement (P=0.029), as well as at 20 min and 24 h afterwards (P=0.001 and 0.032, respectively). The dietary level of ArA had no effect on plasma lactate levels, whereas the administration of ASA significantly (P=0.024) altered the lactate response, mainly in the high-ArA fed seabream. This was also indicated by the significant interaction between all three factors, ArA, ASA and time of sampling (P=0.032).
|
Plasma osmolality increased considerably within 20 min in all treatments (P<0.001), until at least 60 min (P=0.008), but after 24 h these levels were no longer significantly different from levels prior to confinement (Fig. 4). Plasma osmolality was not affected by ArA-supplementation, but the effect of ASA was significant (P=0.020). In the low-ArA group plasma osmolality was reduced, while in the high-ArA group plasma osmolality was elevated by ASA. Furthermore, there was a strong interaction between ArA and time of sampling (P<0.001), as well as between ArA and ASA (P=0.023). The interaction of ASA administration with time was also significant (P=0.001).
|
Plasma sodium levels were markedly altered by confinement (P<0.001), with a clear increase after 20 min (P=0.012), followed by a decrease below pre-confinement levels after 24 h in all treatments (P<0.001; Fig. 5A). Neither ArA nor ASA had a significant effect on the sodium response when analyzed as separate factors, yet the interaction between ArA and ASA was significant (P=0.043).
|
In all treatments plasma chloride levels increased within 20 min after confinement (P<0.001) and remained significantly elevated for at least 24 h compared to the levels prior to confinement (P=0.007; Fig. 5B). ArA-supplemented seabream exhibited significantly higher (P<0.001) plasma chloride levels compared to the fish fed the low-ArA diet. In addition, plasma osmolality was significantly elevated (P=0.017) in both dietary treatments after ASA treatment. No significant interactions were found between any of the factors.
Confinement had a significant effect on plasma potassium (P<0.001) with a significant decrease after 20 min (P=0.010) in all treatments. Potassium levels remained lower than pre-confinement levels for at least 24 h (P<0.001; Fig. 5C). ArA-supplementation had no effect on plasma potassium levels, whilst ASA administration resulted in significantly elevated levels of potassium (P=0.041), mainly in the ArA-supplemented seabream.
The branchial Na+, K+-ATPase activity was significantly higher (P<0.001) in the ArA-supplemented fish than in the low-ArA group. The ATPase activity was also markedly higher 24 h after confinement than prior to confinement (P=0.039; Fig. 6). In addition, the interaction between ArA and time of sampling was significant (P=0.041), while ASA had no significant effect on the ATPase activity.
|
Free ArA in the incubation medium reduced the Na+, K+-ATPase activity of gill homogenates in a dose-dependent way (P=0.003), except at 10 and 30 µmol l-1 ArA (Fig. 7).
|
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Discussion |
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On subjecting the seabream to confinement to induce a stress response, the
fatty acid composition of the gills was affected, but levels in muscle or
kidney tissues hardly at all. After confinement the levels of polyunsaturated
fatty acids had decreased in gill tissues, while the monounsaturated as well
as the saturated fatty acids exhibited an increase. These changes were not
only relative (in percentages of total fatty acids), but were also accompanied
by decreasing amounts of EPA, DHA and ArA, when expressed in mg g-1
dry mass (data not shown). When synthesizing new membranes, incorporation of
readily synthesized saturated and monounsaturated fatty acids is faster than
that of PUFA originating from the diet. Hence it is possible that the changes
in the gills reflect a higher rate of turnover than in kidneys and muscle. The
observed changes might also arise from ß-oxidation of the long-chain
fatty acids. However, this does not correspond to the general preference in
fish tissues for oxidation of monounsaturated fatty acids over saturated fatty
acids, which in turn are preferred over polyunsaturated fatty acids
(McKenzie et al., 2000).
Feeding the ArA-supplemented diet to gilthead seabream for 18 days was
sufficient to substantially diminish the cortisol response after net
confinement, compared to the fish fed a diet containing a low level of this
fatty acid. This blunted response to stress was very similar to what was found
in seabream larvae exposed to another type of acute stress. Both 28- and 50
days post-hatch larvae showed considerable lower peak cortisol levels when
they were fed ArA-enriched Artemia nauplii prior to a brief exposure
to air (Van Anholt et al.,
2004). These observations in seabream are in complete contrast to
the augmented cortisol response observed in tilapia Oreochromis
mossambicus, when fed the same diet enriched with ArA (R.D.V.A.,
F.A.T.S., W.M.K. and S.E.W.B., submitted). Tilapia, like most freshwater
species, can convert linoleic acid into ArA, while gilthead seabream has a low
ability to form ArA from its precursor. Gilthead seabream apparently became
more sensitive to an acute stressor when the dietary intake of ArA was low,
emphasizing the importance of ArA in this respect.
To determine whether the observed effects of ArA could be contributed to an
enhanced production of prostaglandins, the COX-inhibiting ability of ASA was
utilized. A previous study on tilapia verified that the effect of ASA in fish
was similar to that in humans, as ASA inhibited the COX activity of kidney
homogenates and reduced plasma levels of prostaglandin E2
(PGE2; Van Anholt et al.,
2003). Feeding the ASA-containing capsules resulted in an almost
threefold increase of the plasma salicylate levels in our seabream and the low
basal levels of cortisol at the start of the tests confirmed that this was a
stress-free method to administer ASA. This ASA treatment also attenuated the
confinement-induced cortisol response in the seabream fed the low-ArA diet,
which would indicate that prostaglandins stimulated the release of cortisol at
a low dietary intake of ArA. However, this would not correspond to the
observed blunted cortisol response observed in seabream with a high dietary
intake of ArA, which would have resulted in an elevated release of
prostaglandins during stress. In fact, administration of ASA caused a slight
elevation of the cortisol levels in those seabream that were supplemented with
ArA in advance. This argues against the assumption that ArA-mediated effects
can be attributed to the formation of COX-derived metabolites.
It is possible that in this study the inhibition of the COX pathway by ASA
increased the availability of free ArA immediately after confinement for the
alternative pathways in certain tissues. Eicosanoids resulting from conversion
of ArA by lipoxygenase and epoxygenase have been shown to stimulate the
release of ACTH and ß-endorphin from the pituitary, as well as to modify
the induced release of cortisol from the adrenals
(Hirai et al., 1985). The
available information on the functions of other eicosanoids besides
prostaglandins in the control of the HPI axis of fish is very limited and it
remains to be determined how ArA is exactly involved in this process.
Acute stress is normally associated with the release of catecholamines that
promote glycogenolysis in the liver cells of fish, causing a rapid increase of
plasma glucose levels (Wendelaar Bonga,
1997). The accumulation of lactate during stress either points to
reduced uptake by liver cells for gluconeogenesis or to the incomplete
oxidation of glucose, resulting from insufficient oxygen supply
(Vijayan and Moon, 1992
;
Vijayan et al., 1997
;
Wendelaar Bonga, 1997
;
Fabbri et al., 1998
). In the
present study the dietary level of ArA had no effect on the basal levels of
plasma glucose or lactate, nor did it affect the confinement-induced
hyperglycemia and lactacidemia, suggesting that the catecholamine release was
not affected. Nevertheless, the treatment with ASA reduced the basal glucose
levels in the `low-ArA'-fed fish, whereas ASA had no effect on the fish fed
the ArA-supplemented diet. The lactate levels were affected in a different way
by ASA. ASA delayed the recovery to basal levels in the low-ArA group, and
augmented the lactate response in the ArA-supplemented seabream. Though it is
unclear which processes were altered by the change in the dietary ArA intake,
some suggestions can be made. For instance, the low ratio of n-3/n-6 PUFA
might have enhanced the metabolic rate and oxygen demand, as suggested by
McKenzie et al. (2000
) and
McKenzie (2001
). On the other
hand, free ArA has been shown to change the binding of catecholamines or
corticosteroids to their receptors in liver cells
(Vallette et al., 1991
;
Lee and Struve, 1992
;
Skalski et al., 2001
), which
could have reduced hepatic gluconeogenesis causing elevated lactate levels in
the seabream in the present study.
Acute stress and the associated release of catecholamines can lead to an
increased permeability of the branchial epithelium, leading to an influx of
ions in fish in a hyperosmotic environment. This in turn stimulates the ionic
extrusion by the chloride cells, located mainly in the opercula and gills
(Wendelaar Bonga, 1997;
McCormick, 2001
). In seabream
from both dietary treatments, plasma sodium and chloride levels increased
within 20 min after confinement in a similar way, indicating an increased
permeability. The immediate decrease in plasma potassium in all treatments was
more likely caused by the enhanced uptake of K+ into red blood
cells, in reaction to the low plasma oxygen levels associated with acute
stress (Gibson et al., 2000
).
ArA supplementation attenuated the stressor-induced increase in plasma
osmolality. The plasma levels of sodium and chloride did not exhibit a
corresponding increase, suggesting the presence of other factors that
influence the osmolality. Interestingly, ASA treatment appeared to counteract
the effect of ArA and resulted in an increase in plasma osmolality after 1 h.
Furthermore, both plasma chloride and potassium levels were enhanced by ASA in
the ArA-supplemented seabream. This suggested a possible increase in the
permeability of the membranes due to the combination of ASA and ArA. However,
the confinement-induced increase in sodium was attenuated by ASA in that same
group, arguing against an enhanced influx of ions.
Cortisol has been shown to stimulate the proliferation of branchial
chloride cells and to increase the activity of ion-transporting enzymes,
particularly Na+, K+-ATPase, the major driving force for
branchial transepithelial ion transport located in the chloride cells
(Wendelaar Bonga, 1997).
Indeed, the branchial Na+, K+-ATPase activity had
increased in both dietary treatments 24 h after confinement. In addition, the
ArA-supplemented seabream showed a distinctly higher branchial Na+,
K+-ATPase activity already prior to confinement. Although the
effect of ASA treatment was not significant, the ArA-supplemented fish
exhibited no increase in the ATPase activity when treated with ASA. From these
results it is not clear whether ArA-derived prostaglandins were involved in
the regulation of the branchial Na+, K+-ATPase. However,
it also appears unlikely that the stimulating effect of ArA supplementation on
the ATPase activity could be contributed to ArA itself, as the tests showed
that free ArA was an inhibitor of the branchial ATPase activity in
vitro. Inhibitory effects of unsaturated fatty acids on Na+,
K+-ATPases have been demonstrated in vitro before, and
were attributed to a decreased enzyme affinity for extracellular K+
due to direct interactions of the fatty acids with sodium-pump protein
subunits (Swann, 1984
;
Swarts et al., 1990
;
Haag et al., 2001
).
Alternatively, ArA might have stimulated the Na+,
K+-ATPase activity in gills by enhancing the release of
osmoregulatory hormones such as prolactin and thyroxin (Kolesnick et al.,
1984a
,b
;
Mustafa and Srivastava,
1989
).
In this study we have demonstrated marked changes in the stress response
due to feeding different dietary levels of ArA for 18 days, which emphasizes
the physiological impact that a relatively small change in a single dietary
fatty acid can have. Providing optimal ArA levels in commercial diets for
marine species could be effective in moderating the stress response and
improving survival following exposure to handling and transport, as routinely
occurs during the grow-out of fish in aquaculture. Furthermore, replacing fish
oils in commercial diets with vegetable oils that contain no C20 and C22 PUFA,
combined with the low fatty acid elongation and desaturation activities of
carnivorous/marine species, will result in reduced tissue levels of ArA, EPA
and DHA (Bell, 1998;
Bell and Sargent, 2003
;
Montero et al., 2003
). It is
advisable to determine the effects of such a low dietary intake of ArA and
other PUFA on a longer term, focussing not only on growth performance and feed
efficiency, but also on possible health effects.
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List of abbreviations |
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The seabream fingerlings were a generous gift of Fendée Aquaculture (La Faute sur Mere, France). The authors thank Dr G. Kissil (IOLR-NCM, Eilat, Israel) for providing the specially prepared pellets. R. Van Anholt received a travel grant from the Netherlands Organization for Scientific Research (NWO; R88-242) to visit the National Center for Mariculture. The authors also thank the department of Epidemiology and Biostatistics (Nijmegen University Hospital St Radboud) for their advice on the statistical analyses.
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References |
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