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First published online January 18, 2008
Journal of Experimental Biology 211, 377-381 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012856
Long flights and age affect oxidative status of homing pigeons (Columba livia)
1 Division of Neuroanatomy and Behaviour, Institute of Anatomy, University of
Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
2 Dipartimento di Biologia Animale e dell'Uomo, University La Sapienza, Viale
dell'Università 32, I-00185 Roma, Italy
* Author for correspondence (e-mail: david.costantini{at}uniroma1.it)
Accepted 3 November 2007
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: aging, antioxidants, free radicals, migration, oxidative stress
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Pennycuick, 1990;
Tucker, 1968;
Schmidt-Nielsen, 1984;
Masman and Klaassen, 1987;
Ward et al., 2001;
Videler, 2006). Metabolic rate
during flight may actually increase by as much as 12 times the resting values
(Raveling and Lefebvre, 1967;
Rayner, 1982;
McWilliams et al., 2004;
Videler, 2006). It is also
known that metabolic demands may change from one species to another
(Hails, 1979).
Long-term fasting flights carried out during migration impose severe
physiological challenges (Wikelski et al.,
2003; McWilliams et al.,
2004; Costantini et al.,
2007a) (but see Hasselquist et
al., 2007), but also relatively short flights may demand
considerable energy (Nudds and Bryant,
2000). Several studies on homing pigeons have shown that none of
the investigated blood parameters (e.g. uric acid, haematocrit, osmolality,
Na+ and K+) show drastic changes during flights lasting
around 1 h (John et al., 1988;
Bordel and Haase, 1993;
George and John, 1993). During
flights of about 1–2 h, the metabolism of pigeons switches from using
carbohydrates to fats in order to produce energy
(John et al., 1988). Indeed,
circulating free fatty acids increase in pigeons after 1 h of flight. Similar
changes in nutrient consumption for energy production during flight have also
been found in several other species (Jenni
et al., 2000; McWilliams et
al., 2004). Given that, in general, lipids and, in particular,
unsaturated fatty acids are quite susceptible to free radical damage
(Bielski et al., 1983;
Porter et al., 1995) and that
birds mainly accumulate unsaturated (mostly 16:1, 18:1 and 18:2 fatty acids)
rather than saturated fatty acids (reviewed by
McWilliams et al., 2004), such
metabolic changes during long flights could expose birds to an oxidative
challenge (Costantini et al.,
2007a).
Metabolic activity produces reactive oxygen and nitrogen species
(Leffler, 1993;
Beckman and Ames, 1998). These
chemicals are responsible for a plethora of oxidative damages to lipids,
proteins and nucleic acids. To overcome pro-oxidants and to maintain redox
homeostasis (i.e. balance between pro-oxidants and antioxidants), organisms
have evolved numerous ways to protect themselves, such as enzymatic and low
molecular mass antioxidants, or specific cellular components that repair
oxidatively damaged molecules (Yu,
1994). The balance between pro-oxidants and antioxidants is
considered the degree of oxidative stress
(Finkel and Holbrook,
2000).
Studies on avian flight have so far considered several blood parameters,
such as biomacromolecules, electrolytes or hormones [e.g. circulating
proteins, uric acid and ions (George and
John, 1993); haematocrit, plasma free fatty acids and ions
(Bordel and Haase, 1993);
arginine vasotocin (Giladi et al.,
1997); corticosterone and uric acid
(Jenni et al., 2000); proteins
(Schwilch et al., 2002); and
haematocrit (Jenni et al.,
2006)]. However, only one recent study analysed pro-oxidants and
plasma antioxidants in flying birds
(Costantini et al., 2007a).
The study provided indirect evidence that long migratory flights may shift the
redox balance toward more oxidative conditions.
Sports medicine studies indicate that exercise may increase oxygen
consumption and pro-oxidant production
(Alessio, 1993;
Ji, 1999). Also, some recent
studies on birds have shown that the physical activity, such as breeding
effort (Alonso-Alvarez et al.,
2004; Wiersma et al.,
2004) or exercise in a hop/hover wheel
(Tsahar et al., 2006), may
affect the oxidative status.
This study sought to evaluate how the redox system responds to different
flight efforts in homing pigeons (Columba livia), a bird species in
which flight physiology is well known (e.g.
Pennycuick, 1968;
Rothe et al., 1987;
John et al., 1988;
Bordel and Haase, 1993;
Bordel and Haase, 2000;
George and John, 1993;
Schwilch et al., 1996). To
quantify the oxidative status of this species, we determined, (1) the
oxidative damage as serum reactive oxygen metabolites (ROMs; primarily
hydroperoxides) and (2) the total serum antioxidant capacity (OXY). In
addition, we used the ratio between ROMs and OXY as a measure of the oxidative
status with higher values, meaning higher oxidative stress (OS)
(Costantini et al., 2006;
Costantini et al., 2007a;
Costantini et al., 2007b).
Given that high activity levels may increase free radical production, we
expected to find a positive association between flight time and oxidative
stress.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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For the experiments, birds of both sexes were used. They were 1–5 years old, and all individuals had undergone numerous training flights before being used for the study. Body mass (to the nearest 5 g) was recorded for both control and flying birds on the morning of the release.
Pigeons (19, 10 and 17) were released, respectively, from Lake Vico (linear
distance between the release site and the loft: 45 km; short distance, SD),
and from Ardea (linear distance between the release site and the loft: 39 km;
short distance, SD), and Arezzo (linear distance between the release site and
the loft: 172 km; long distance, LD). We chose these distances because given a
flight speed of around 60–70 km h–1, we expected
pigeons released from Arezzo to fly for more than 2 h. This is important
because within about 1–2 h of flight, the metabolism of pigeons switches
from carbohydrates to fats (John et al.,
1988).
All birds included in a same release were released together. Two more
pigeons were released along with the other for the releases from Ardea and
Arezzo with a miniaturised global position system (GPS) data logger attached
on their backs to track the pigeons' flight paths
(Steiner et al., 2000). These
birds were not included in the oxidative stress analyses.
On all release days, there were sunny conditions and wind was absent or weak. On the day of release, pigeons had been put in transport cages at sunrise and transported to the site of release. Meanwhile, one of the investigators manipulated the control birds in a similar manner. Control birds were also kept in transport cages, were released in the loft at the same time of release of flying pigeons, and were not allowed to access food or water until bleeding. Control birds for the release from Vico were not included in the analyses because they were manipulated in a different and slightly more stressful way as were those released from Ardea and Arezzo. This itself caused changes in the redox status that will be reported elsewhere. Both control and flying pigeons were bled 2 days before the release in order to avoid pre-release stress. These values were considered baseline values. Post-treatment blood samples were taken within 15 min of the birds' return to the loft. We bled only specimens that returned on experimental days (5, 3 and 7 from Vico, Ardea, and Arezzo, respectively). Control pigeons (N=7) were bled concomitantly with birds that flew. Both pre- and post-treatment blood samples (300 µl) were drawn from the tarsal vein and kept on ice until centrifugation. The serum was stored at –20°C.
Lab analyses
ROMs and OXY were measured by the d-ROMs test and the OXY-adsorbent test,
respectively, as previously described
(Costantini and Dell'Omo,
2006a; Costantini and Dell'Omo,
2006b; Costantini et al.,
2006; Costantini et al.,
2007a; Costantini et al.,
2007b). Briefly, reactive oxygen metabolites (primarily
hydroperoxides, ROOH) are early peroxidation products of the exposure of
biological macromolecules (mainly lipids, but also proteins and nucleic acids)
to reactive oxygen species. ROMs were determined by diluting the serum (20
µl) with 200 µl of a solution containing 0.01 mol l–1
acetic acid and sodium acetate buffer (pH 4.8), and
N,N-diethyl-p-phenylenediamine as chromogen, followed by
incubation for 75 min at 37°C. The acidic pH favours the release of iron
and copper from serum proteins that catalyse the cleavage of hydroperoxides in
two different free radicals. When these compounds react with an
alkyl-substituted aromatic amine solubilized in the chromogen, they produce a
complex of a colour intensity that is directly proportional to its
concentration. ROMs are expressed as mmol l–1
H2O2 equivalents. The total serum antioxidant capacity
was quantified as the ability of the serum antioxidant barrier to cope with
the oxidant action of hypochlorous acid (HOCl; oxidant of pathologic relevance
in biological systems). The serum (10 µl) was diluted 1:100 with distilled
water. A 200 µl aliquot of a titred HOCl solution was incubated with 5
µl of the diluted serum for 10 min at 37°C. Then, 5 µl of the same
chromogen solution used for the ROMs determination was added. An
alkyl-substituted aromatic amine dissolved in the chromogen is oxidized by the
residual HOCl and transformed into a pink derivative. The intensity of the
coloured complex is inversely related to OXY. Measurements are expressed as
mmol l–1 HOCl neutralised. The repeatability tested on 35
duplicates was significantly high for both markers of oxidative stress
(intraclass correlation coefficient: ROMs, r=0.94,
P<0.001; OXY, r=0.99, P=0.001) (see
Lessells and Boag, 1987).
Statistical analyses
Statistical analyses were performed using the STATISTICA package (version
7.0, StatSoft, Inc. 2004, Tulsa, OK, USA). Generalized linear/non linear
models (GLZ) (McCullagh and Nelder,
1989; Dobson,
2001) with normal error function and an identity-link function
(all dependent variables are normally distributed) were used to evaluate
whether flight duration affected ROMs and OXY values. A backward removal with
a critical P<0.05 was used to build the minimum model,
significantly explaining the observed variance. In both models, we included,
as dependent variables, post-flight values of ROMs and of OXY, respectively,
with their pre-flight values included as covariates. Two more models were
tested to evaluate effects of flight on the relative balance between ROMs and
OXY (i.e. degree of oxidative stress), including in one model as dependent
variable the ROMs/OXY (x1000) ratio and in the other one the post-flight
values of ROMs as dependent variable and the post-flight values of OXY as
covariate, according to previous studies
(Costantini et al., 2007a).
Age and body mass were always included as covariates (Pearson correlation
between age and body mass: r=–0.21, P=0.36). Two-way
interactions between distance and age or body mass were also included in all
models. Values are shown as mean ± s.e.m.
|
RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The three experimental groups (Table 1) did not differ in age (F2,19=0.75, P=0.49) or in body mass (F2,19=1.18, P=0.33).
|
Reactive oxygen metabolites showed a significant (54%) increase in LD
pigeons (Wald=10.54, d.f.=2, P=0.005) All other terms were removed at
P values 
0.83. By contrast, all three experimental groups showed
decreased levels of OXY. However, this was mainly evident in LD pigeons that
had a 19% drop in antioxidant capacity (Wald=15.86, d.f.=2, P=0.0004;
Fig. 1) that was as much as
five to six times that of control or SD pigeons. The lose in serum antioxidant
capacity was higher in older individuals (Wald=27.03, d.f.=1,
P<0.001; Fig. 2).
Finally, the covariation between body mass and change in OXY was different
across groups (experimental groupxbody mass: Wald=14.03, d.f.=2,
P=0.0009). Specifically, the sign of the covariation was positive for
LD pigeons and negative for control and SD pigeons. All other terms were
removed at P values 0.73.
|
|
0.49. Similar results were obtained for the second
model of oxidative stress (experimental group: P=0.005). |
DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Finally, among LD pigeons, heavier individuals depleted
less serum antioxidants.
Studies from sports medicine show that strenuous exercise may increase
reactive oxygen species production in skeletal muscle and, to a lesser extent,
in the heart, jeopardizing body redox homeostasis (e.g.
Alessio, 1993;
Ji, 1999). In birds, endurance
flight is known to increase protein catabolism of muscle fibres
(Bordel and Haase, 2000;
Jenni et al., 2000;
Schwilch et al., 2002). This
is in turn translated into increased levels of uric acid, a waste product of
nitrogen metabolism. We did not measure uric acid, but it is known that flight
increases its concentration in the blood of homing pigeons
(Bordel and Haase, 1993;
Schwilch et al., 1996). Uric
acid is well known as an important antioxidant
(Ames et al., 1981;
Iqbal et al., 1999;
Klandorf et al., 1999;
Tsahar et al., 2006), but
serum antioxidant capacity decreased in LD pigeons. This result may suggest
that the uric acid levels did not increase enough to buffer the high depletion
of other serum antioxidants, such as vitamins.
Studies on pigeons flying in a wind tunnel
(Rothe et al., 1987) or in the
wild (Schwilch et al., 1996)
showed a shift to a high and stable lipid-based metabolism within 1–2 h
of flight. Prolonged flights caused increased hydrolysis of triglycerides from
adipose tissues to free fatty acids and glycerol and oxidation of free fatty
acids by muscle activity (Schwilch et al.,
1996). To some extent, such metabolic changes may be determined by
the time since feeding, which is an important determinant of the fuels pigeons
use in flight (Gannes et al.,
2001). Overall, a lipid-based metabolism may have further
contributed to increasing oxidative stress in LD pigeons. Unsaturated fatty
acids are the main form of lipids stored in avian tissues
(McWilliams et al., 2004), and
are quite susceptible to free radical damage. These findings may suggest that
pigeons and, in general, birds might need to balance energy gain and oxidative
cost, both derived from metabolising lipids.
Unexpectedly, we found that older pigeons depleted more serum antioxidants
in order to maintain redox homeostasis. This pattern held for controls and
both experimental treatments. Mechanisms that regulate and maintain body
homeostasis are known to lose functionality as a consequence of aging
(Martin and Grotewiel, 2006;
Kregel and Zhang, 2007). Also,
studies on birds show a loss in physiological function with time (reviewed by
Vleck et al., 2007).
In the present study, the higher depletion of serum antioxidant capacity of older pigeons has two possible explanations: a declining capability of the organism to respond to stress or an increasing susceptibility to stress. Actually, our data suggest that, by depleting more serum antioxidants, older pigeons were able to maintain levels of oxidative damage, as measured by ROMs, similar to those in younger pigeons.
A pigeon's lifespan is from 3–5 years in the wild to a maximum of 35
years in a managed loft (Johnston and
Janiga, 1995). The average lifespan of pigeons included in the
present study (3.1 years) is therefore about 9% of the maximum life-span that
pigeons should attain when kept in a loft. It is known that pigeons may show
signs of declining body function with age. For example, declines with age in
choroidal blood flow and choroidal vascularity have been actually observed at
3–5 years (Fitzgerald et al.,
2001). This fact, along with the findings of the present study,
suggests that a loss in body function might already be evident when pigeons
are 4–5 years old. Yet, our data do not allow us to choose between these
two explanations.
It is not clear why heavier LD pigeons depleted less serum antioxidants.
Given that age and body mass were not correlated, age does not seem to explain
this result. A study on red knots (Calidris canutus) showed that
flight muscle efficiency increases with body mass because of a higher fuel
load (Kvist et al., 2001).
This could suggest that somehow heavier birds might have higher metabolic
efficiency, produce fewer pro-oxidants, and have less oxidative damage.
However, further research is warranted to test this hypothesis.
Conclusions
Our study showed for the first time that long flights may cause oxidative
stress, and that older pigeons deplete more serum antioxidants. Possibly,
heavier pigeons may deplete less serum antioxidants during a long-distance
flight. Given that our study was not specifically designed for evaluating
whether age or body mass affects redox status of flying pigeons, future
research should analyse in detail how these two factors modulate the oxidative
cost of long flights. Finally, future studies of our group will be aimed also
at evaluating to what extent increase in distance remains correlated with
changes in redox status.
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