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First published online March 16, 2007
Journal of Experimental Biology 210, 1238-1244 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002741
Carotenoid availability does not limit the capability of nestling kestrels (Falco tinnunculus) to cope with oxidative stress
1 Dipartimento di Biologia Animale e dell'Uomo, Università La
Sapienza, Viale dell'Università 32, 00185 Roma, Italy
2 Dipartimento dell'Ambiente e Prevenzione Primaria, Unità di Chimica
Tossicologica, Istituto Superiore di Sanità, Viale Regina Elena 299,
00161 Roma, Italy
3 Ornis italica, Piazza Crati 15, 00199 Roma, Italy
* Author for correspondence (e-mail: david.costantini{at}uniroma1.it)
Accepted 1 February 2007
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Summary |
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Key words: antioxidants, free radicals, life history, metabolism, oxidative damage
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The anti-oxidant machinery is basically based
on endogenous (e.g. enzymes) and exogenous (e.g. dietary anti-oxidants)
chemicals (e.g. Yu, 1994).
When the anti-oxidant defence system is unable to cope with the anti-oxidant
capacity, or when pro-oxidants exceed it, oxidative stress can arise because
of an imbalance toward pro-oxidants. Oxidative stress is actually suggested to
be the main proximate mechanism underlying degenerative processes such as
aging (Harman, 1956;
Harman, 1972;
Beckman and Ames, 1998;
Finkel and Holbrook,
2000).
In birds, several factors have been shown to shift the redox balance toward
pro-oxidants, hence generating oxidative stress. In zebra finches
Taeniopygia guttata, increased rearing effort depletes the
anti-oxidant capacity of parents
(Alonso-Alvarez et al., 2004b;
Wiersma et al., 2004); zebra
finches injected with lipopolysaccharides have a weaker resistance of red
blood cells to a free radical attack than controls
(Bertrand et al., 2006a); in
nestling Eurasian kestrels Falco tinnunculus, T-cell-mediated immune
response causes increased and decreased levels of oxidative damage and
anti-oxidant capacity, respectively
(Costantini and Dell'Omo,
2006a); in barn swallows Hirundo rustica and garden
warblers Sylvia borin, oxidative stress is higher in individuals with
lower energy stores after a sustained flight across the sea, during spring
migration (Costantini et al.,
2007).
Carotenoids are fat-soluble pigments capable of scavenging pro-oxidants
(e.g. Møller et al.,
2000; Surai, 2002;
Krinsky and Yeum, 2003). Since
animals are unable to synthesise carotenoids de novo, they must rely
on dietary sources (Brush,
1990). Moreover, the complex absorption of carotenoids from the
intestinal tract also seems to put a physiological constraint on their
availability to wild birds (e.g.
Casagrande et al., 2007). In
this light, carotenoids are suggested to be in limited supply for
reproduction, health-related functions, or the expression of sexual
colouration (Blount, 2004).
Life-history theory states that an increase in the amount of limited energy
or chemicals devoted to one process might result in a decreased allocation to
other processes (Roff, 1992;
Stearns, 1992). This is
because life-history traits cannot evolve independently from one another. The
trade-off among competing demands of limited resources such as carotenoids is
therefore a pivotal issue, since organisms might trade the gains in increasing
allocation to one fitness component against losses in reducing allocation to
another one. Natural selection is actually predicted to favour individuals
able to deploy limited resources in a way that maximises their survival and
reproductive success.
Whilst it is well supported that maternally transferred carotenoids are
useful anti-oxidants in embryo and hatchling models
(Surai, 2002;
McGraw et al., 2005), recent
evidence suggests that the anti-oxidant role of xanthophylls (i.e. oxygenated
carotenoids) is less important than previously thought in nestling or adult
birds [Eurasian kestrel (Costantini et
al., 2006; Costantini and
Dell'Omo, 2006a); greenfinch Carduelis chloris
(Hõrak et al., 2006);
great tit Parus major (Tummeleht
et al., 2006)]. In addition, recent studies suggest that, at high
concentrations, carotenoids such as lutein and ß-carotene can lose their
anti-oxidant effectiveness and acquire pro-oxidant properties in
vitro or in vivo systems
(Young and Lowe, 2001;
El-Agamey et al., 2004;
Siems et al., 2005;
Costantini et al., in
press).
We recently showed that carotenoids may be considered a limited resource
for skin colour production in nestling kestrels
(Casagrande et al., 2007). In
addition, we proposed that the current idea that carotenoid availability might
limit the effectiveness of pro-oxidation retardation or inhibition should be
reconsidered (Costantini et al., in
press). In this light, our work aimed at investigating if
carotenoids are really useful anti-oxidants in wild birds, by a
supplementation experiment. We tested this hypothesis in nestling Eurasian
kestrels, a raptor species for which both the carotenoid and redox systems are
sufficiently known (see references herein). If carotenoids actually limit the
anti-oxidant capacity of the organism, we would expect to find supplemented
nestlings showing lower levels of oxidative damage and higher levels of
anti-oxidant capacity than controls.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The
solution was orally administered every other day for a total of five
administrations using a 1 ml syringe (Fig.
1). Control birds received 22.5 µl of oil only. To avoid
degradation and photo-oxidation of carotenoids, the safflower oil solution was
stored cold and in the dark. The dose was selected on the basis of the
available information about the xanthophyll content of the species preyed on
by kestrels (Czeczuga, 1978;
Czeczuga, 1979;
Goodwin, 1984;
Casagrande et al., 2006) and
of our previous supplementation studies to wild nestling
(Casagrande et al., 2007) or
captive adult (Costantini et al., in
press) kestrels.
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A blood sample (400 µl) was drawn from the brachial vein just before the beginning of the experiment (pre-treatment values), 10 days later (2 days since the end of the supplementation; day 10), and 1 week later (day 17). Blood samples were kept cool (0–5°C) until centrifugation, which occurred within a few hours, and the serum was stored at –20°C. At the time of bleeding, wing length (mm) and body mass (g) of each individual were also recorded.
In total, 61 nestlings (30 controls and 31 supplemented) from 12 nests were included in the experiment. Specifically, there were three nests with four chicks, five with five chicks, and four with six chicks. Within each brood (except the five-chick one), half of the nestlings were randomly assigned to the two treatment groups. In the five-chick broods, two nestlings were assigned to the controls and three to the supplemented or vice versa in order to get a balanced design.
Measurement of carotenoids
The serum (100 µl) was diluted with absolute methanol (1:8) and the
flocculent proteins were precipitated by centrifugation at 12 000
g for 5 min. Carotenoids were quantified with a Beckman DU
7400 spectrophotometer at 476 nm. The carotenoid concentration was estimated
as µg ml–1 of serum using the standard absorbance curve of
lutein (Sigma-Aldrich, Milano, Lombardia, Italy)
(Costantini et al., 2006).
Measurement of reactive oxygen metabolites
The serum concentration of reactive oxygen metabolites (ROMs; primarily
hydroperoxides, ROOH) was measured by the d-ROMs test (Diacron, Grosseto,
Italy). Hydroperoxides are primary products of the oxidative cascade derived
from the oxidation of organic compounds (mainly lipids) (e.g.
Porter et al., 1995;
Moore and Roberts, II, 1998).
The serum (20 µl) was first diluted with 200 µl of a solution containing
0.01 mol l–1 acetic acid/sodium acetate buffer (pH 4.8) and
N,N-diethyl-p-phenylenediamine as chromogen and then incubated for 75
min at 37°C. The acidic pH favours the release of iron and copper from
serum proteins. These metals catalyse the cleavage of ROOH, leading to the
generation of two highly reactive and histolesive pro-oxidants, namely the
alkoxyl (R-O–) and alkylperoxyl (R-OO–)
radicals. When these compounds react with an alkyl-substituted aromatic amine
(A-NH2) solubilized in the chromogen, they produce a complex whose
colour intensity (pink) is directly proportional to their concentration. After
incubation, the absorbance was read with a spectrophotometer (Microplate
Reader Model 550, Tokyo, Japan) at 490 nm and the concentration of ROMs was
calculated by comparison with a standard curve obtained by measuring the
absorbance of a standard solution. ROMs are expressed as mmol
l–1 of H2O2 equivalents (for details,
see Costantini et al., 2006;
Costantini and Dell'Omo,
2006a; Costantini and
Dell'Omo, 2006b).
|
;
Costantini and Dell'Omo,
2006a; Costantini and
Dell'Omo, 2006b).
Statistical analyses
ANOVA for repeated measures (RM) was performed to evaluate the effects of
the treatment on serum carotenoids, ROMs, OXY, OS (index of oxidative stress
evaluated as ROMs/OXYx1000) (see
Costantini et al., 2006), body
mass and body condition (residuals of a linear regression of body mass on the
wing length, calculated for each sampling separately). Treatment (Tr) was
included as fixed factor and nest as random factor to avoid pseudoreplication.
Two- and three-way interactions were included in all the models.
Post-hoc comparisons were performed by the Tukey test (results are
shown in the figures). Log- or square-root transformations were applied where
appropriate. All the statistical analyses were performed with STATISTICA 6.0
(StatSoft 2001, Tulsa, OK, USA).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Circulating ROMs were unaffected by the treatment with surplus carotenoids (Tr: F1,11=0.21, P=0.65; TrxRM: F2,22=0.15, P=0.86; Fig. 2B), and no significant nestxTr (F11,37=0.64, P=0.78) or nestxTrxRM interaction (F22,74=1.24, P=0.24) emerged. The nest of rearing accounted for most of the ROMs variance (F11,37=2.06, P=0.05) and for the negative relationship between ROMs and age of chicks (RM: F2,22=4.99, P=0.016; nestxRM: F22,74=5.85, P<0.001).
Supplemental carotenoids did not increase OXY (Tr: F1,11=0.28, P=0.61; TrxRM: F2,22=0.11, P=0.89; Fig. 2C), although a significant interaction nestxTrxRM emerged (F22,74=2.05, P=0.012). The nest of rearing significantly accounted for OXY variance (nest: F11,37=2.79, P=0.009) and for the negative relationship between OXY and age of chicks (RM: F2,22=6.53, P=0.006; nestxRM: F22,74=1.86, P=0.026). The interaction between nest and Tr was not significant (F11,37=0.87, P=0.58).
The variance in OS was explained only by the nest
(F11,37=2.22, P=0.035) and by the interaction
between nest and RM (F22,74=3.60, P<0.001),
all P-values of the other terms being 
0.12.
Body mass and body condition were unaffected by the supplementation (all
P-values 0.18). Body mass showed a significant increase over time
(RM: F2,22=1369.42, P<0.001).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Casagrande et al.,
2007; Costantini et al.,
2006), hence we can exclude any pharmacological effect of the
administered dose.
Baseline levels of serum carotenoids measured in the present study are
lower than those in wild adult kestrels measured during the courtship phase
(Casagrande et al., 2006) and
are twofold higher than those measured in captive nestling American kestrels
Falco sparverius (Negro et al.,
1998). If compared to a larger dataset (25 families, eight orders)
(Tella et al., 2004), baseline
levels of nestling kestrels are within the physiological range of plasma
carotenoids measured in 80 species, which varies from a mean concentration of
0.47 µg ml–1 to 53.17 µg ml–1.
It has recently been shown that carotenoids may be a limited resource for
colour expression in nestling kestrels
(Casagrande et al., 2007).
Nestlings supplemented with different doses of carotenoids show a quick
increase in circulating xanthophylls and a slow intensification of the skin
colour of tarsi. The present study, using a lower dosage and a different
timing of supplementation, corroborates the observation that carotenoid
availability limits the circulating levels of carotenoids in nestling
kestrels. Yet the significance and the effects of such limitation seem to vary
largely between nests. Indeed, a large inter-nest variance in serum carotenoid
concentration can be observed in kestrels
(Casagrande et al., 2006;
Casagrande et al., in press).
Circulating carotenoids harbour a high level of environmental variance, which
is mainly diet-dependent (Bortolotti et
al., 2000; Casagrande et al.,
in press). In our study region, kestrels show consistent
differences in feeding habits, even when sharing the same hunting habitat
(Costantini et al., 2005).
Such feeding styles, together with habitat differences in prey availability,
might affect the carotenoid intake in free-living kestrels, since the
carotenoid content may vary greatly amongst prey groups (e.g.
Goodwin, 1984). Yet, it is
suggested that such variance may also be related to a physiological constraint
during the absorption in the gut
(Casagrande et al., 2007).
Finally, in ovo carotenoid exposure in chickens Gallus
gallus is important later in life for subsequent absorption, metabolism
and/or tissue deposition of diet-derived carotenoids
(Koutsos et al., 2003).
Further study is needed to disentangle the importance of all these components
potentially underlying carotenoid variance in free-living birds.
The absence of a nest-related effect of treatment and of a treatment
per se on both markers of oxidative stress rule out the possibility
that such inter-nest variation in diet affects the levels of oxidative stress
by shifting the carotenoid supplies or demands of chicks. Indeed, our study
shows that carotenoids are minor anti-oxidants in nestling kestrels more than
1-week-old. Whilst carotenoids represent a limited resource for colour
expression, they seem not to be a limiting factor for the maintenance of redox
homeostasis. In fact, nestlings did not benefit from the increased intake of
carotenoids in terms of reduction in oxidative damage and increase in serum
anti-oxidant capacity. Therefore, the recent proposal that carotenoid
availability might not limit the effectiveness of coping with oxidative stress
in kestrels (Costantini et al., in
press) is additionally supported by the present work.
It is known that maternally transferred carotenoids are useful
anti-oxidants in developing embryos. It is also suggested that carotenoids are
likely to be especially important during the immediate post-hatching period
(Surai, 2002;
Karadas et al., 2005;
McGraw et al., 2005). Indeed,
the hatching and early neonatal stages represent a critical period for birds
in terms of oxidative stress, due to the exposure of the chick to atmospheric
oxygen, the shift to pulmonary respiration, and the increase in metabolic rate
(Freeman and Vince, 1974;
Vleck and Bucher, 1998). For
example, circulating ROMs are negatively related to age in nestling kestrels
(Costantini et al., 2006).
This observation is supported by the present work. In addition, the serum
anti-oxidant capacity is negatively correlated with age. In both cases,
however, this pattern seems to differ amongst nests. Finally, the level of
oxidative stress as defined by the balance between ROMs and OXY decreased with
age, as found in a previous study
(Costantini et al., 2006), but
in the present study this trend was not significant. Taken together, these
results suggest that younger nestlings have to cope with higher free radical
production than older ones. This in turn might mediate the overexpression of
the anti-oxidant response in order to balance pro-oxidants (for reviews, see
Dröge, 2002;
Scandalios, 2005). In
contrast, nestlings about to fledge suffer from lower oxidative damage and do
not need to maintain a high anti-oxidant defence.
The inter-nest differences in the relationship between age and ROMs or
serum anti-oxidant capacity might reflect, to some extent, the expression of
different genetic polymorphisms and differences in dietary uptake of
anti-oxidants, respectively, as we recently suggested in this species
(Costantini et al., 2006b; Martin et al.,
1996).
Carotenoid-supplemented females of free-living lesser black-backed gulls
Larus fuscus had eggs with lower susceptibility to lipid
peroxidation, as measured by malondialdehyde
(Blount et al., 2002a), and
higher plasma anti-oxidant activity (Blount
et al., 2002b). Lutein supplementation to captive zebra finches
had no direct effect on resistance to oxidative stress, as measured by the
time needed to haemolyse 50% of the red blood cells exposed to a controlled
free radical attack (Alonso-Alvarez et al.,
2004a). In the same experiment, however, the birds with the
highest increase in plasma carotenoids (as a result of the supplementation)
showed the highest resistance to the free radical attack. In a subsequent
paper, the same authors suggested that carotenoid availability might modulate
the trade-off between reproduction and resistance to oxidative stress in zebra
finches (Bertrand et al.,
2006b).
Supplementation of carotenoids to free-living hihi Notiomystis
cincta females had no effect on retinol or tocopherol concentrations in
egg yolk, but caused decreased and increased levels of 
-tocopherol and
retinol in nestling plasma, respectively
(Ewen et al., 2006). The
decrease in plasma vitamin E was related to the reduction in the requirement
of this vitamin in self-maintenance because of the concomitant increased
carotenoid concentration in plasma.
Taken together, these studies suggest an important role of carotenoids as
anti-oxidants in birds. However, recent studies, together with the present
work, challenge this view. All these studies were carried out on nestlings
older than 1 week or adult birds of several species with different life
histories, and no relationships between carotenoids and several markers of
oxidative stress were found. For example, circulating carotenoids were not
correlated with either oxidative damage or anti-oxidant capacity in nestling
kestrels (Costantini et al.,
2006; Costantini and Dell'Omo,
2006a), nor to the anti-oxidant capacity in male greenfinches
(Hõrak et al., 2006) or
in breeding female great tits (Tummeleht
et al., 2006). In our case, the absence of a relationship between
circulating carotenoids and serum anti-oxidant capacity is not dependent on
the method used since it is widely demonstrated that HOCl reacts with
carotenoids (Handelman et al.,
1991; Siems et al.,
2000).
These results suggest that the systemic anti-oxidant capacity of
carotenoids in birds (except for well-established protective effects on
embryos and hatchlings) may not appear as important as previously thought.
However, it could be argued that the activity of carotenoids in a specific
tissue is not reflected at the systemic level, so that the anti-oxidant
capacity in the blood is not affected. It is known that tissues may show
differences in anti-oxidant distribution or susceptibility to oxidative stress
(Surai et al., 1996;
Surai, 1999;
Karadas et al., 2005). It is
also known that the relevance of a specific anti-oxidant can vary from one
tissue to another. For example, zeaxanthin supplementation reduced lipid
peroxidation in the liver but not in plasma, heart or pectoral skeletal muscle
in male 1-day-old Leghorn chicks Gallus gallus
(Woodall et al., 1996).
Instead, canthaxanthin supplementation did not influence susceptibility to
oxidative stress in any tissue examined. In addition, some anti-oxidants show
a high variation across the avian orders (e.g. carotenoids)
(Olson and Owens, 2005),
whilst others can be synthesised or obtained by diet in a species-specific way
(e.g. ascorbic acid) (Del Rio,
1997).
In the studies on oxidative stress, the recommendation is to use more than
a single oxidative biochemical marker in order to get a better insight into
such a complex system. Indeed, we used two different markers (ROMs and OXY),
which are known to appropriately reflect oxidative stress in birds (e.g.
Costantini and Dell'Omo,
2006a) and mammals (e.g.
Brambilla et al., 2001).
Therefore, we are confident that carotenoid availability does not limit the
capability to regulate redox homeostasis in our model species.
It could be that the importance of carotenoids as anti-oxidants varies
according to the species or to the specific life cycle phase investigated. For
example, carotenoids may be limiting in other model systems with lower natural
blood carotenoid levels than kestrels. It should also be noted that the
methods used sometimes vary from one study to another, which may make
comparison of the results difficult. This is because the specificity of the
method to be used or its underlying biochemical rationale can be very
different. For example, shortcomings can emerge in the quantification of
malondialdehyde to assess lipid peroxidation in complex biological fluids or
tissues because of its non-specificity
(Chirico, 1994).
Finally, supplemental carotenoids did not affect body mass or body
condition (i.e. energy stores). Previous studies with carotenoid
supplementation to avian species (i) could not find any effect on body mass
[e.g. Leghorn chicks supplemented with 100 mg kg–1 diet
(Woodall et al., 1996); zebra
finches supplemented with 12.5–200 µg ml–1 of
drinking water (Alonso-Alvarez et al.,
2004a); kestrel nestlings supplemented with different doses
(Casagrande et al., 2007)],
(ii) found a gain of mass in zebra finches supplemented with 100 µg
ml–1 of drinking water
(Bertrand et al., 2006b), or
(iii) found an immediate loss of mass in captive kestrels following a
supplementation of 8 mg of carotenoids/day in a 4-week study
(Costantini et al., in press).
This latter result was perhaps related to the high intake of carotenoids that
caused the dysfunction of liver or kidney caused by pervasive oxidative
damage, and secondarily to peroxidation of fat reserves.
In conclusion, our results show that the capability of wild nestling kestrels to cope with oxidative stress is not limited by carotenoid availability in the diet. This finding supports previous studies suggesting that the anti-oxidant activity of carotenoids in nestling and adult birds has been exaggerated.
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Acknowledgments |
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