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Conclusions
CONCLUSIONS
The principal results obtained in this thesis are as follows:
The barn swallow obtained the carotenoids that are present in plasma, eggs, red facial feathers
and gape of nestlings through the diet. However, carotenoids seems limited for adult barn
swallows since adults bring prey with a lower carotenoid content to the nest than randomly
collected insects in the feeding area.
Carotenoids seemed to play a role in assuring that arrival date is a condition-dependent
character. Males that arrived early had lower carotenoid concentration than late arriving birds
and depleted their carotenoids to a lesser extent than late arriving males.
Carotenoid content in blood differed during the breeding season between the sexes. In
particular females depleted to a greater extent their circulating carotenoids than males during
the laying period.
Male barn swallows developed facial feathers with a colour with a higher absorbance in the
lutein band, a hue more shifted to the red part of the spectrum and that was more saturated
than females.
Males developed smaller facial feathers than females and allocated coloured pigments to a
proportionally larger surface of feathers than females. Moreover, individuals that had a larger
proportion of the feathers pigmented also had a more saturated colour and a hue more shifted
towards the red. I found evidence that the degree of pigmentation is condition-dependent
since males that arrived in better condition had a higher proportion of the feather pigmented
than males in poor condition.
In this thesis, I report empirical studies on the barn swallow, planned to investigate the
role of carotenoids in determining variability of coloured signals and other activities that are
carotenoid-dependent.
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Conclusions
Carotenoids, are unique pigments, because animal have to ingest them and because they
have several physiological functions that can ultimately affect fitness (review in Chapter 3). I
reviewed recent information about their presence in coloured tissues (Chapters 2 and 4) and
their role in immune function, as free radical scavengers and as fundamental resources to
embryos and chicks (Chapter 3).
All hypotheses concerning the evolution and the maintenance of carotenoid-based
characters are based on the assumption that these pigments are limiting in the environment. I
reported evidence that barn swallows might be limited by the amount of carotenoids in the
diet even if carotenoids are widely present in the foraging range of the species. My results
uniformly support the hypothesis that obtaining carotenoids seems difficult for barn swallows.
If carotenoids are limiting in the environment, this could have implications for the
evolution of reproductive strategies and life history traits. I showed that parent barn swallows
bring insects to the nest with a lower content in carotenoids than insects in the field. A tradeoff mediated by carotenoids between the number of nestlings raised and their quality can be
expected, and optimal clutch size should be influenced by environmental availability of these
pigments.
In the third chapter of this thesis, I considered the role of carotenoids in assuring that
arrival date in the barn swallow is a condition-dependent character. To my knowledge there
are no studies that investigated the mediating role of carotenoids in assuring honesty of a
behavioural trait that is involved in reproduction. Although experimental studies are needed to
identify which mechanisms are underlying these observations, my results suggest that
carotenoids are involved in determining and maintaining variability in arrival date. Migratory
species could be affected by the trade-off between early arrival at the breeding grounds
(which has been repeatedly associated with several kinds of fitness benefits) and the cost of
increased production of free radicals
Song and territory defence could also be affected by carotenoids. Song is a costly
activity that raises the metabolic level which in turn might increase the risk of lipid
peroxidation. Moreover, the increase in testosterone at the beginning of the breeding season
and during mating display suppresses immunity (von Schantz et al. 1999). If carotenoids
modulate the antioxidant systems during production of songs or other sexual behaviour,
individuals with higher levels of carotenoids should display at a higher rate.
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Conclusions
When we talk about ‘high level of carotenoids’ we do not know which tissue best
indicates the total amount of carotenoids of a given individual. Circulating carotenoids might
reflect short-term availability, while reserves that can be mobilised (e.g. the liver) probably
gives a better indication of carotenoids of a given individual. Carotenoids stored in adipose
tissues are not easily and rapidly mobilised as shown in laying hens (Surai and Speake 1998)
and wild geese (Negro et al. 2001b), and they are hardly available for metabolic needs.
There are a few studies performed on recently hatched chicks that reported carotenoid
concentration in plasma and/or other tissues (Surai and Speake 1998; Surai et al. 1999a).
However we do not know how carotenoid concentration in blood changes when carotenoids
are mobilised from other tissues. This represents a problem while interpreting, for example,
variation in circulating carotenoids in laying females as reported in the second part of Chapter
3. The amount of carotenoids that barn swallows allocate to eggs, as reported by Saino et al.
(2002a), is several times larger than the reduction in circulating carotenoids that I recorded
during laying. Females might actively transfer carotenoids from blood to liver during egg
production, or transport between these two compartment could be passive. Further studies are
certainly needed.
I reported a difference in circulating carotenoids between sexes in the barn swallow.
Females had a lower concentration of carotenoids during laying than males. This supports the
hypothesis that variability in carotenoid concentration in blood is independent of foraging
efficiency. I showed that females during the first, second and third clutch decreased the
amount of carotenoids circulating in blood. Both males and females decreased their
concentration during reproduction, but females showed a larger reduction. Moreover I could
not show the same pattern at arrival of circulating carotenoids in females as I did in males.
This result contrasts with the hypothesis that feeding ability determines intraspecific
variability in carotenoid concentration in barn swallows. The sexes seem to differ in the
functions to which they allocate carotenoids during reproduction, and sex-specific trade-offs
are therefore expected.
The evolution of coloration is linked to the fact that such traits are costly to produce and
hence reliable signals, because these pigments are limiting. The results that I presented in
Chapter 4 are in agreement with this hypothesis.
To my knowledge there are no studies that considered the relative degree of
pigmentation of coloured feathers in birds. I showed that males had smaller feathers than
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Conclusions
females, but allocated coloured pigments to a relatively greater surface of a given feather than
females.
I reported evidence suggesting that the proportion of the feather being pigmented could
be condition-dependent: a positive correlation was found between the relative part of the
feather being pigmented and coloration in terms of saturation and hue shifted towards the red.
Individuals that had feathers with a larger degree of pigmentation developed a more
conspicuous colour than those that pigmented a smaller surface. Moreover I found a positive
correlation between the pigmented part and body condition at arrival. Based on these results I
proposed a new mechanism for models of honest signalling. The trade-off between the size of
the surface being pigmented and coloration could assure honesty of pigment-based coloration.
Badyaev et al. (2001) recognised four distinct components of carotenoid-based
coloration: 1) pigment elaboration or patch colour, a function of the type and quantity of
carotenoids deposited in the growing feathers; 2) patch area (number of feathers pigmented),
3) pigment symmetry or bilateral consistency of feather pigmentation; and 4) patch symmetry
or the bilateral symmetry in the area of carotenoid pigmentation. As reported by Badyaev et
al. (2001) each of these multiple components might be proximately produced by different and
partially independent mechanisms. Distinct selection can act on each component and distinct
fitness consequences might arise from variability in relationships that link each of these
components to fitness (Pryke et al. 2002). We suggest that the degree of pigmentation as
estimated in Paper 3 and feather size could be another important component of pigment-based
patch coloration.
An important point should be considered when discussing the cost of coloration of red
facial feathers in the barn swallow. As reported in Paper 3 the colour is not entirely
determined by carotenoids. It is possible that melanins contribute to the colour of facial
feathers of the barn swallow, since carotenoid pigments extracted from the feathers are yellow
and orange. However, biochemical analyses that identify all determinants of coloration are
still lacking.
An interesting point raised by this study is heterogeneity in the relationship between
facial feather coloration and length of the outermost tail feathers among populations of barn
swallows. As suggested in Paper 3, ecological differences related to the wintering grounds
and distance of migration could be responsible for this result. However, as discussed by
Shykoff (1997), characters with a continuous cost of maintenance after development might
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Conclusions
trade resources in different ways than those that have been developed once and that are fixed
with apparently no cost of maintenance. The elongated forked tail in the barn swallow
represents a handicap to males during the reproductive season. However, to date there are no
indications for any cost imposed after development of facial feather coloration in the barn
swallow, and further studies are needed.
In conclusion, my empirical observations support the hypothesis that carotenoid-based
characters have evolved because they reliably signal quality, and that reliability of signals is
maintained mainly because of the trade-off between the mediating action of carotenoids in
display and condition.
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