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First published online June 29, 2006
Journal of Experimental Biology 209, 2686-2695 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02299
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Performance-enhancing role of dietary fatty acids in a long-distance migrant shorebird: the semipalmated sandpiper
Biology Department, University of Ottawa, 30 Marie Curie, Ottawa, Ontario, K1N 6N5, Canada
* Author for correspondence (e-mail: jmweber{at}science.uottawa.ca)
Accepted 25 April 2006
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Summary |
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20 g
to 40 g) by feeding on a burrowing amphipod, Corophium volutator,
that contains unusually high levels of n-3 polyunsaturated fatty acids (PUFA).
In mammals, high n-3 PUFA content of membrane phospholipids (PL) is linked to
improved exercise performance due to increased membrane fluidity that
accelerates transmembrane lipid transport. We hypothesized that dietary n-3
PUFA could be used as a natural `performance-enhancing substance' by
semipalmated sandpipers to prepare their flight muscles for migration. Also,
PUFA stored as fuel in neutral lipids (NL) can be mobilized more quickly than
saturated fatty acids, but they contain less energy per unit mass. It is
therefore unclear whether dietary fatty acids are modified before storage.
Birds were collected at various stages of fat loading to examine changes in
the composition of tissue PL (membranes) and NL (fuel stores). Results show
that dietary n-3 PUFA are incorporated in tissue lipids in less than 2 weeks.
During the stopover, the double bond index of muscle PL increases by 25% and
the fatty acid profiles of both muscle PL and adipose NL converge with that of
the diet. However, >50% of dietary n-3 PUFA are converted to other fatty
acids before storage, mainly to oleate (18:1), possibly because
monounsaturates offer a compromise between high energy density and ease of
mobilization. This study shows that long-distance migrant birds can (1) use
natural diets rich in specific lipids to prime flight muscles for endurance
exercise, and (2) modify dietary fatty acids before storing them as fuel.
Key words: membrane phospholipids, fat stores, bird migration, nutrition, endurance exercise, fatty acid metabolism, sandpiper, Calidris pusilla, Corophium volutator
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). During the
2-week stopover, the birds double body mass by feeding on Corophium
volutator, a small amphipod responsible for 86% of their diet
(Napolitano and Ackman, 1990;
Napolitano et al., 1992). This
small mud shrimp is an extremely rich source of the n-3 polyunsaturated fatty
acids (PUFA) eicosapentaenoic acid (EPA; 20:5) and docosahexaenoic acid (DHA;
22:6) (Ackman et al., 1979).
Rapid fattening on this unique diet is rather intriguing because n-3 PUFA are
known to improve aerobic performance in other vertebrates and have many
beneficial health effects in humans
(Ruxton et al., 2004).
Multiple lines of evidence show that muscle performance can be affected by
the n-3 PUFA content of membrane phospholipids (PL) via changes in
fluidity and permeability (Daveloose et
al., 1993; Ernst,
1994; Stillwell and Wassal,
2003). For example, unusually high levels of n-3 PUFA have been
found in the membrane PL of highly aerobic muscles such as hummingbird flight
muscles (Infante et al.,
2001). Moreover, endurance training in rats and humans increases
the n-3 PUFA content of their muscle PL
(Andersson et al., 2000;
Helge et al., 2001;
Turner et al., 2004). A
particularly relevant laboratory study
(Pierce et al., 2005) shows
that the aerobic capacity of a migrant bird species, the red-eyed vireo
(Vireo olivaceous), is influenced by the fatty acid composition of
its diet.
Successful completion of a long migration does not only depend on intrinsic
characteristics of muscles, but also on the nature of the oxidative fuels
available. For example, saturated fatty acids provide an advantage because of
their higher energy content per unit mass compared to PUFA
(Blem, 1990). Selectivity has
been demonstrated for key steps of lipid metabolism including storage,
mobilization and oxidation. Diets high in monounsaturated fatty acids (MUFA)
are normally preferred (McWilliams et al.,
2002; Pierce et al.,
2004) and long-distance migrants commonly store large amounts of
oleate (18:1) (Blem, 1990;
Caldwell, 1973). However,
fasting studies reveal that PUFA (and EPA in particular) are more easily
mobilized than MUFA or saturated fatty acids
(Herzberg and Farrell, 2003;
Raclot and Groscolas, 1995).
At the ß-oxidation step, preference for MUFA
(Henderson and Sargent, 1985)
or PUFA (DeLany et al., 2000)
have both been reported.
Semipalmated sandpipers stopping in the Bay of Fundy provide ideal conditions to uncover potential effects of nutrition on lipid metabolism of long-distance migrants and, ultimately, on their capacity for endurance exercise. In this `natural experiment', large amounts of n-3 PUFA are consumed and it is unclear whether cell membranes are affected or if dietary fatty acids are modified before storage. Therefore, the goals of this study were to investigate semipalmated sandpipers during rapid fattening to determine: (1) the anatomical distribution of their lipid reserves, (2) the effect of a natural diet high in n-3 PUFA on the fatty acid composition of cell membranes, and (3) changes in the composition of storage lipids and whether the fatty acid profiles of the bird's fat reserves and of the diet converge during refueling. We anticipated that changes in lipid metabolism might not only provide sufficient energy for migration, but increased muscle capacity for endurance exercise.
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Materials and methods |
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4500 km migration from the Bay of Fundy
(Canada) to South America. A previous study on the same species had shown that
body mass is an accurate predictor of time spent refueling in the Bay of Fundy
(White, 1985). Therefore,
changes in body mass were used as an indirect measure of feeding time at the
last stopover before their long-distance flight to wintering grounds. Wild
sandpipers were caught with a pull trap
(Hicklin et al., 1989) at
Dorchester Cape, New Brunswick, Canada (65°10'N, 77°27 'W;
August 10 and 11, 2004; Canadian Wildlife Service permit SC2354). After
weighing, 45 adults were selected to obtain the widest possible range of body
masses (20-41 g) and percent body fat (12-43%) (see
Fig. 1). These animals were
euthanized by cervical dislocation, immediately frozen, and stored at
-20°C for up to 3 months before analyses. Mud shrimps (Corophium
volutator Pallas) were collected on the sandpipers' feeding grounds as
described previously (McCurdy et al.,
2000), and were immediately frozen at -20°C.
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). After
filtration, KCl (0.25%) was added and the mixture centrifuged to separate
aqueous and organic phases. The aqueous phase was discarded and the organic
phase containing the lipids was dried on a rotating evaporator (Büchi
Rotavapor, Flawil, Switzerland). Lipids from the diet samples of
(Corophium volutator) were extracted using the same procedure.
Separation of neutral lipids (energy stores) and phospholipids (membranes)
Following extraction and drying, total tissue lipids were resuspended in
chloroform. Neutral lipids (NL), nonesterified fatty acids (NEFA), and
phospholipids (PL) were separated by filtration on Supelclean solid-phase
extraction tubes (3 ml LC-NH2; Sigma, St Louis, MO, USA) as
described previously (Bernard et al.,
1999). Briefly, NL were eluted from the column with
chloroform:isopropanol (2:1 v/v), NEFA with isopropyl ether:acetic acid (98:2
v/v) and PL with methanol. The NL and PL fractions were then used for analysis
of their fatty acid composition. The detailed fatty acid composition of NEFA
is not reported here because they only accounted for less than 1% of total
tissue lipids.
Fatty acid composition
Heptadecanoic acid was added to each sample as an internal standard. The
fatty acid compositions of NL and PL were measured by gas chromatography
(McClelland et al., 1999)
after acid transesterification with acetyl chloride in methanol
(Abdul-Malak et al., 1989).
Individual fatty acid methyl esters were separated and quantified on a
Hewlett-Packard gas chromatograph (5890 series II with 7673 autosampler)
equipped with flame-ionization detector and a 30 m fused silica column
(Supelco 2330; Sigma, St Louis, MO, USA). Helium was the carrier gas. The
injector port was at 220°C and the detector at 240°C. Column
temperature was kept at 185°C for 35 min, raised to 210°C at a rate of
5°C min-1, and maintained at 210°C for 10 min. Exact
retention times of individual fatty acids were determined with pure standards
(Sigma-Aldrich, St Louis, MO, USA).
Calculations and statistical analyses
The relationships between body mass and % body fat
(Fig. 1), and between lean
pectoral muscle mass and body fat mass
(Fig. 2B) were assessed by
simple linear regression, whereas the relationships between fat mass of
different tissues (carcass, pectoral muscle, liver and fat depots) and body
fat mass were assessed by multiple regression
(Fig. 2A). For all analyses of
lipid composition (Figs 3,
4 and
5), the birds were divided into
three groups of equal size. Because % body fat is an accurate index of time
spent refueling in the Bay of Fundy
(White, 1985);
Fig. 1), we ranked the birds
according to % body fat and divided them in three equal groups containing
`lean', `medium' and `fat' birds (N=15 for each group). Lean birds
had <25% fat and were assumed to have recently arrived in the Bay of Fundy.
Medium birds had 25-35% fat, whereas fat birds had stored >35% lipids and
were ready to start their long migratory flight.
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One-way ANOVA and post-hoc Tukey tests were used to compare group
means (lean, medium and fat) for double bond index (DBI) and % contribution of
individual fatty acids to total fatty acids within each lipid class (NL or
PL). Fatty acids accounting for less than 1% of total fatty acids within each
lipid class were not included in our analysis. The double bond index was used
to quantify the level of fatty acid unsaturation in each lipid class and was
calculated as follows (expressing percentages as ratios):
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The average number of double bonds (also called degree of unsaturation) was
calculated as:
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A 
predator-prey index (PPI) was used to measure the difference
between the fatty acid composition of pectoral muscle or lipid reserve
(combining contributions from fat depots and carcass) and that of
Corophium volutator. It was calculated as follows:
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Statistical analyses were performed using SYSTAT version 8.0. All variables were tested for normality and homogeneity of variances. Percentages were transformed to the arcsine of their square root before analysis, and all values given are means ± standard error of the mean (s.e.m.). P<0.05 was considered significant.
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Results |
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Double bond index
To analyze changes in tissue lipid composition during refueling, the
sandpipers were divided into three groups: lean, medium and fat (see Materials
and methods). Fig. 3 summarizes
changes in double bond index (DBI) in storage lipids (NL) and in membrane
lipids (PL) of the three tissues that show significant fat accumulation:
pectoral muscle (Fig. 3A),
carcass (Fig. 3B) and fat
depots (Fig. 3C). Phospholipids
have a higher DBI than NL in the pectoral muscle of all birds
(P<0.001). However, only medium birds show a higher DBI in PL than
NL for carcass (P<0.001) and fat depots (P<0.05).
During refueling, increases in DBI were observed in the membranes of pectoral
muscle and in the storage lipids of the carcass. Pectoral muscle PL and
carcass NL have a higher DBI in medium and fat birds than in lean birds
(P<0.05; Fig. 3).
For fat depots, no differences in DBI were observed between lean, medium and
fat birds (P>0.05).
Tissue fatty acid composition
Changes in the fatty acid composition of tissues during refueling are
presented in Table 1. To start
analyzing the mechanisms responsible for the observed changes in DBI, Figs
4 and
5 only focus on the fatty acids
showing significant differences between lean, medium and fat birds. Changes in
the fatty acid composition of tissue PL are presented in
Fig. 4. In pectoral muscle PL,
the increase in DBI observed during the stopover is explained by increases in
%20:5 and %22:6 that overcompensate a small decrease in %20:4
(P<0.001; Fig. 4A).
In carcass PL, DBI remains unchanged because the increase in %20:5 is offset
by a decrease in %20:4 (P<0.01;
Fig. 4B). In the PL of fat
depots, %18:2 and %20:4 both decrease during the stopover (P<0.01;
Fig. 4C).
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Significant changes in the fatty acid composition of tissue NL are presented in Fig. 5. In pectoral muscle NL, %20:5 increases while %18:0 decreases as lipid stores are being deposited (P<0.05; Fig. 5A). In carcass NL, %20:5 and %22:6 show increases while %20:4 decreases (P<0.005; Fig. 5B). In the NL of fat depots, DBI remains unchanged because increases in %20:5 and %22:6 are compensated by decreases in %20:4 and %18:2 as the birds accumulate fat reserves (P<0.05; Fig. 5C).
Fatty acid composition of food and differences between prey and predator
The fatty acid composition of Corophium volutator, the
invertebrate prey item accounting for 86% of the birds' diet
(Napolitano et al., 1992), is
presented in Table 2.
Corophium is particularly rich in the n-3 polyunsaturated fatty acids
20:5 and 22:6 that, together, account for 45% of all fatty acids consumed by
the sandpipers. The difference in fatty acid composition between
Corophium and tissue lipids of the sandpipers were calculated as an
index: the delta predator-prey index or PPI (a single value representing
the sum of differences for all fatty acids; see Materials and methods).
Changes in PPI are summarized in Fig.
6. During refueling, convergence between the fatty acid
compositions of predator and prey was observed for pectoral muscle PL
(Fig. 6A) and lipid reserves NL
(Fig. 6B) that showed a
significant decrease in PPI (P<0.005).
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;
Jump, 2002a;
Jump, 2002b;
Totland et al., 2000;
Yamazaki et al., 1987), and to
increase the activities of key Krebs Cycle and ß-oxidation enzymes
(Froyland et al., 1997;
Guo et al., 2005;
Jump and Clarke, 1999;
Sanz et al., 2000;
Yamazaki et al., 1987). This
study shows that massive consumption of n-3 PUFA causes a rapid increase in
the unsaturation levels of muscle PL and adipose tissue NL. However, a
significant fraction of the dietary n-3 PUFA consumed is modified before
storage to maintain high MUFA levels in the fuel reserves used for
migration.
Flight muscle membranes are modified
Phospholipids are the main structural lipids of cell membranes. In
semipalmated sandpipers, the rapid consumption of n-3 PUFA over a short
stopover period is sufficient to cause a 25% increase in the double bond index
of flight muscle phospholipids (Fig.
3), a change achieved by incorporating dietary EPA and DHA
(Table 1;
Fig. 4). Recent experiments on
rats (Turner et al., 2004) and
humans (Andersson et al., 2002)
reveal that mammals respond similarly after feeding on a high n-3-PUFA diet
for periods of 2-3 months. Our study is the first to show: (1) that nutrition
can also modify avian muscle membranes, (2) that natural diets can have this
effect in wild birds, and (3) that muscle membranes of some long-distance
migrants respond very rapidly (1 week).
Information presently available on various animal models is not sufficient
to identify a clear mechanism linking a specific fatty acid composition of
membranes with increased muscle performance. However, several lines of
evidence show that muscle PL composition and capacity for endurance exercise
are related. Membranes of high-performance muscles like hummingbird flight
muscle, rattlesnake shaker muscle and hare locomotory muscle, all contain
unusually high amounts of n-3 PUFA
(Infante et al., 2001;
Valencak et al., 2003). In
addition, endurance training increases the n-3 PUFA content of muscle PL in
rats and humans (Andersson et al.,
2000; Helge et al.,
2001; Turner et al.,
2004). Paradoxically, feeding rats a diet rich in n-3 PUFA affects
their membrane PL composition (Turner et
al., 2004), but decreases endurance in vivo
(Ayre and Hulbert, 1997),
though isolated muscle function seems to remain normal
(Ayre and Hulbert, 1996).
Controlled-diet studies in fish (Wagner et
al., 2004) and birds (Pierce
et al., 2005) also show that changing the fatty acid composition
of food can affect their performance. Unfortunately, very few studies have
attempted to characterize a direct link between the consumption of specific
fatty acids with improved endurance, and they provide conflicting results. In
rats, dietary n-6 PUFA have been reported to cause the greatest increase in
endurance (Ayre and Hulbert,
1997). For salmon, Wagner et al. suggest that n-3 PUFA increase
swimming performance (Wagner et al.,
2004), whereas McKenzie et al. come to the opposite conclusion
(McKenzie et al., 1998). It is
therefore premature to determine whether n-3 or n-6 PUFA are most beneficial,
or to generalize to all animals. However, it is well established that membrane
fluidity and permeability are significantly increased by all high PUFA diets
(Ernst, 1994) and decreased by
diets poor in PUFA (Daveloose et al.,
1993). In this study, we show that semipalmated sandpipers modify
their muscle membranes by feeding on Corophium as they prepare for
long-distance flight. This functional change is consistent with changes in
membrane fluidity and permeability that would increase capacity for fatty acid
transport. Therefore, this response may contribute to support the high lipid
fluxes that these impressive athletes need for migration.
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),
but decreases the rates of mobilization and oxidation
(DeLany et al., 2000;
Raclot, 2003;
Raclot and Groscolas, 1995).
Therefore, migrant birds may modify dietary fatty acids before storage to
achieve a compromise between high energy density and ease of
mobilization/oxidation. To address this possibility, we calculated the
composition of a theoretical fat bird from the measured composition of lean
birds (Table 1) and of their
food (Table 2), assuming that
dietary fatty acids are stored without modification. Then, we compared this
theoretical fatty acid composition with that actually observed in fat birds.
This analysis is presented in Fig.
7 where stored fatty acids with a higher observed abundance than
expected have a positive value whereas those with a lower abundance have a
negative value. We can estimate that over 50% of total dietary EPA and DHA are
modified before storage, and show that they are mainly converted to oleate and
palmitate (Fig. 7). One
possible reason for this conversion is to decrease the overall vulnerability
of lipid reserves to degradation, PUFA being particularly sensitive to
peroxidation (Gutierrez et al.,
2006). Like semipalmated sandpipers, other migrant birds
(Blem, 1990), some mammals
(Florant et al., 1990) and
fish (Lund and Sidell, 1992)
also store most of their lipids as oleate, and to a lesser extent as
palmitate. This remarkably ubiquitous preference for storing monounsaturates
has never been explained (Weber et al.,
2003). The above analysis suggests that MUFA may offer optimal
characteristics by providing higher energy density than PUFA, together with
higher mobilization and oxidation rates than saturated fatty acids.
Changes in lipid reserves and pectoral muscle lean mass
By capturing and re-capturing the same individual semipalmated sandpipers,
White determined that body mass is an accurate predictor of feeding time in
the Bay of Fundy (White,
1985). Here, we show that % body fat is closely correlated with
body mass (Fig. 1), and have
therefore used % fat as an indirect measure of refueling time (i.e. birds were
allocated to `lean', `medium' and `fat' groups according to % body fat).
Previous studies have reported the anatomical distribution of lipid reserves
in migratory birds to assess seasonal differences at different stages of
complete migrations (Marsh,
1983; Piersma et al.,
1999; Scott et al.,
1994). Our study is the first to examine rapid changes in fat
reserves during a single refueling stopover, as migrants prepare for a long
flight. In semipalmated sandpipers, almost all the fat is deposited in
discrete adipose tissue depots placed around flight muscles (42%) and as
subcutaneous reserves in the carcass (54%)
(Fig. 2). In contrast, minimal
amounts of fat are directly stored in pectoral muscles (4%), and the liver is
not used for this purpose. Interestingly, lean birds have completely depleted
their fat depots, but they maintain significant amounts of subcutaneous fat in
the carcass (Fig. 2). Favoring
the use of internal adipose tissue over subcutaneous fat may be linked to the
thermoregulatory requirements of these animals as they travel from the
Arctic.
In migrating birds, seasonal changes in body mass were traditionally
attributed to fluctuations in fat reserves. However, recent studies have shown
that the lean mass of various organs like pectoral and leg muscle, heart,
kidney, liver and gut is also modified
(Driedzic et al., 1993;
Jehl, 1997;
Marsh, 1983;
Piersma and Gill, 1998;
Piersma et al., 1999). During
refueling, we observed that the pectoral muscle lean mass of semipalmated
sandpipers increases by 40% (or 2 g). Flight muscle hypertrophy has also
been observed in red knots (Calidris canutus islandica)
(Piersma et al., 1999),
bartailed godwits (Limosa lapponica)
(Piersma and Gill, 1998) and
eared grebes (Podiceps nigricollis)
(Jehl, 1997) in preparation
for migration. In these other studies, it is not clear whether the change is
necessary to meet the new power requirements of heavy birds, or if additional
proteins are stored for another purpose [e.g. to restore muscle mass after
particularly strenuous flights (Baucheinger
and Biebach, 2005) or to provide an immediate protein source for
reproduction upon landing (Evans et al.,
1992)]. Semipalmated sandpipers only use multiple short-distance
flights to reach the Bay of Fundy
(Hicklin, 1987) and do not
reproduce in South America. Therefore, the observed increase in pectoral lean
mass of this species is probably needed to transport their large fuel
load.
Limitations of study
The experimental design of this study only provides indirect support for
the idea that dietary PUFA are being used to improve capacity for endurance
exercise. However, our results are an important step towards a more rigorous
test of this hypothesis under the controlled laboratory conditions that a
`natural experiment' does not permit. Significant questions remain unanswered.
For example, it could be argued that semipalmated sandpipers do not `prefer'
Corophium as a diet, but simply eat large quantities of this
invertebrate because it happens to be abundant at the stopover site. A diet
preference experiment would settle this issue (e.g.
McWilliams et al., 2002), but
field observations suggest that Corophium would be preferred by
semipalmated sandpipers. Other food items are readily available in the Bay of
Fundy (Hicklin and Smith,
1979), and even though Corophium is abundant, it contains
rather low levels of lipids and energy
(Ackman et al., 1979).
Interestingly, the least sandpiper (Calidris minutilla) is another
species that refuels on a diet consisting of 89% Corophium to prepare
for a non-stop transoceanic flight
(Cooper, 1994), whereas
semipalmated plovers (Charadrius semipalmatus) only eat 48%
Corophium, but migrate over much shorter distances
(Hicklin and Smith, 1979;
Nol and Blanken, 1999). Future
laboratory experiments should also test whether the exercise performance of
birds is actually improved by consuming large amounts of n-3 PUFA. The `flying
wheel' protocol developed by Chappell et al. may be ideal for this purpose
(Chappell et al., 1999).
Conclusions
Before long-distance migration, semipalmated sandpipers modify their muscle
membranes and load large fat reserves by feeding on marine invertebrates. In
addition to building adequate fuel stores, migrant birds can therefore use
natural diets rich in specific lipids to prepare flight muscles for endurance
exercise. Rapid consumption of dietary PUFA allows them to prime membranes for
high fatty acid fluxes. However, a large fraction of dietary EPA channeled
towards storage is initially converted to oleate. This common preference for
storing monounsaturates over other fatty acids may provide the required
compromise between high energy density and ease of metabolism. No marine
invertebrate other than Corophium volutator contains such large
amounts of PUFA, and, in North America, this species is only found in the Bay
of Fundy and in the Gulf of Maine. If human activities were to compromise
Corophium populations, the migration cycle of semipalmated sandpipers
and their survival could be greatly affected. Corophium appears to be
a non-replaceable component of this shorebirds' diet and its habitat should
therefore be protected.
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Acknowledgments |
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References |
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