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First published online June 15, 2007
Journal of Experimental Biology 210, 2361-2367 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.003517
Relationship between avian growth rate and immune response depends on food availability
k*
Department of Animal Ecology, University of Bia
ystok,
wierkowa 20B, 15-950 Biaystok, Poland
* Author for correspondence at present address: Department of Wildlife Ecology, University of Wisconsin, Madison, 213 Russell Labs, 1630 Linden Drive, Madison, WI 53706, USA (e-mail: pbrzek2{at}wisc.edu)
Accepted 26 March 2007
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Summary |
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Key words: body mass increments, food availability, immune response, life history, Riparia riparia, trade-off
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Such
trade-offs are considered to be fundamental factors shaping the evolution of
immune defence (Zuk and Stoehr,
2002). In recent years, one of the most intensively studied
trade-offs is that between immune function and growth, particularly in birds
(e.g. Hõrak et al.,
2000; Merino et al.,
2000; Soler et al.,
2003; Mauck et al.,
2005) (see also Pilorz et al.,
2005). Nestlings of altricial birds are characterized by a very
fast and resource-demanding growth (Starck
and Ricklefs, 1998). However, young birds frequently face
unfavourable environmental conditions, which reduce food availability,
suppress normal development, and subsequently compromise their fitness
(Gebhardt-Henrich and Richner,
1998; Lindström,
1999). Under such conditions limited resources are likely to be
preferentially allocated to the development of structures and functions
essential for survival and fledging (Schew
and Ricklefs, 1998; Metcalfe
and Monaghan, 2001).
The ability to mount a strong immune response is a significant determinant
of fitness in young altricial birds
(Christe et al., 1998;
Christe et al., 2001;
Merino et al., 2000;
Møller and Saino, 2004;
Cicho
and Dubiec, 2005;
Moreno et al., 2005). Since
immune function is costly (Lochmiller and
Deerenberg, 2000; Norris and
Evans, 2000; Klasing,
2004), one can expect it to drain essential resources away from
other important traits, in particular growth of nestlings. However, studies
aimed at demonstrating this relationship have yielded conflicting results.
Although many authors reported a negative correlation between body mass
increments and immune response (e.g.
Merino et al., 2000;
Soler et al., 2003;
Brommer, 2004), other studies
failed to demonstrate the expected trade-off (e.g.
Hõrak et al., 2000;
Whitaker and Fair, 2002).
Here, we propose that this ambiguity stems from the lack of experimental
control of the amount of resources traded between competing functions. The
significance of any trade-off can only be effectively tested under conditions
that preclude an increase of resource acquisition, which may cover the extra
costs evoked by immune challenge. This is because an increased resource
acquisition may weaken an otherwise inverse relationship between the traded
traits, or even reverse it to a positive one
(van Noordwijk and de Jong,
1986; Ksi
ek et
al., 2003; Sandland and
Minchella, 2003).
Aerial insectivores are frequently used as model organisms in studies on
immune function (e.g. Saino et al.,
1997; Saino et al.,
2001; Saino et al.,
2002; Christe et al.,
1998; Merino et al.,
1999; Merino et al.,
2000; Szép and
Møller, 1999;
Szép and Møller,
2000). They frequently face periods of food shortage incurred by
unfavourable weather conditions (Bryant,
1975; McCarty and Winkler,
1999; Lifjeld et al.,
2002), which adversely affect their immune function
(Christe et al., 2001;
Lifjeld et al., 2002). In the
present study, we investigated the effect of a gradient of food intake on the
relationship between body mass increments and the magnitude of response to a
novel antigen in nestlings of sand martin (Riparia riparia Linnaeus
1758) - a small aerial insectivorous passerine. Sand martin nestlings have a
considerable level of developmental plasticity, which enables them to tide
over inclement weather conditions. They are able to slow the pace of
development during food shortage, and resume it when feeding conditions
improve (Brzek and Konarzewski,
2001; Brzek and Konarzewski,
2004). Thus, they may be particularly likely to trade their growth
for enhanced immune response (Szép
and Møller, 1999). Sand martin nestlings are therefore a
suitable subject for testing the presumed trade-off between body mass
increments and immune function.
In our study we measured the thickness of swelling induced by sub-cutaneous injection of phytohaemagglutinin (PHA) as a surrogate for immune function of the sand martin nestlings. Our experiment was carried out under laboratory conditions. This enabled us to analyse the direction of correlation between body mass increments and PHA-induced swelling response after controlling for food intake. We attempted to simulate the range of food availability encountered by nestlings in the wild. We predicted that the direction of correlation between body mass increments and the magnitude of immune response should vary with different levels of food provisioning. In particular, we expected that the correlation was most likely to be negative in nestlings subjected to lowest food intake, which forces them to trade limited resources between competing demands of body mass increments and immune function.
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Materials and methods |
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ystok, north-eastern Poland. To avoid
the possible effects of relatedness and hatching order, we did not use the
last-hatched young, collected no more than two nestlings from each nest, and
always assigned them to different feeding regimes. All laboratory rearing and
feeding protocols applied in the present study were validated in our previous
experiments, as described in details elsewhere
(Brzek and Konarzewski, 2001;
Brzek and Konarzewski, 2004).
Briefly, the nestlings were reared in artificial nests, made of transparent
plastic. The experiment was carried out in a climatic chamber at 32°C, 90%
relative humidity and 16 h:8 h light:dark regime. We created seven artificial broods, each of four nestlings, assigned randomly to the broods. We assigned the broods to three different feeding regimes. Eight nestlings (two whole artificial broods) were fed with a limited amount of food, resulting in low body mass increments. This group will be referred to as FR (food-restricted). The other twelve nestlings (three whole broods) were fed without restriction (hereafter referred to as the ad libitum, or AL group). The remaining eight nestlings (two whole broods) were fed with an amount of food intermediate between that fed to FR and AL individuals (referred to as the I group). The nestlings from group AL were fed until they stopped begging every 45 min between 06.00 h and 22.00 h CEST (22 times per day). The remaining groups (FR and I) were fed 17 times per day, between 08.00 h and 20.00 h CEST, with deliberately smaller quantities of food, representing around 40 and 70% of ad libitum intake, respectively. All nestlings were hand-fed alternately with equal amounts of crickets and a special formula designed for the nestlings of insectivore birds: fresh, soft cheese, glucose, rice flour and maize flour, mixed in the mass proportions 300:30:15:12 (J. Desselberger, personal communication). This mixture was subsequently added to hard-boiled hens' eggs in the proportion 3:1 and enriched with the vitamin mixture Vitaral (Jelfa, Jelenia Gora, Poland). Fresh portions of food were prepared twice a day. Since we were interested in testing not only between-, but also within-regime effects, we did not attempt to feed the artificial broods with strictly equal amounts of food. This resulted in within-regime variation in food consumption, which we quantified daily for each individual nestling. Energy content of food was determined in a Berthelot-type calorimeter. The energy intake during the whole experiment averaged 74±2.9 (mean ± s.e.m.), 121±2.9 and 186±2.6 kJ in FR, I and AL groups, respectively. The energy intake of individual nestlings was strongly correlated between subsequent days (Pearson correlation, r>0.95 for all comparisons).
The experiment stretched over three consecutive days (72 h; Fig. 1). The day when the experiment began is hereafter referred to as day 1, and the following days are referred accordingly. Two AL nestlings started to exhibit abnormally low food intake and low body mass increments (at the level of FR group) during day 3 and were subsequently excluded from the experiment and immediately returned to their natal nests. The remaining nestlings were returned to their natal nests upon termination of the experiment.
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; Smits et al.,
2001). The PHA trial started on day 2 of the experiment, when
nestlings were 8-days old (Fig.
1). The nestlings were injected into a marked site on the right
wing web with 0.2 mg of PHA (Sigma, Sp. zo.o., Poznan, Poland; L-8754),
diluted in 0.04 ml phosphate-buffered saline (PBS). We measured the thickness
of the wing web before injection and after 24 h with a spessimeter Teclock
SM-112 (Teclock, Nagano, Japan; accuracy 0.01 mm). Each measurement was
repeated three times, then the mean value was used for subsequent analyses.
Repeatability of our measurements calculated as an intraclass correlation
coefficient (Lessells and Boag,
1987) was 
=0.96. The magnitude of PHA-induced swelling
response was quantified as the difference between pre- and post-injection
measures of the wing web thickness.
Statistics
Differences between experimental groups were analysed by means of ANOVA or
ANCOVA, with feeding regime as the main effect, initial body mass and/or body
mass increment as covariates, and the respective interaction terms. In the
present experiment nestlings were reared in artificial broods. Therefore, in
all statistical models we also attempted to control for the possible effect of
a common artificial brood environment. However, the inclusion of this effect
produced spurious results in full ANCOVA models that contained feeding regime
and the brood (randomly nested within feeding regime) as main effects and the
respective interaction terms. Although the models were highly significant
(P<0.0001), none of their components were statistically
significant (in all cases P>0.7). We therefore recognized the full
ANCOVA models as over-parameterized. Further statistical analyses of reduced
models revealed that the nested effect reflected minor, but consistent
between-brood differences in food intake, being the primary determinant of
other studied traits. For these reasons in the final ANCOVAs testing the
effects of interactions we elected not to include the nested effect of
artificial broods, because it was collinear with the other analysed factors.
To ensure that within-brood autocorrelation of values of studied traits did
not confound our results we checked the significance of this effect by means
of randomization tests (Manly,
1997) carried out on the residuals from the final ANCOVA models
described above. We randomly shuffled these residuals among artificial broods
(each time 1000 runs) and calculated the proportion of iterations for which
calculated within-brood sum of squares was larger than that in the original
data set. The tests revealed that the residuals were randomly distributed
among artificial broods (e.g. P=0.21 for the model testing the effect
of interaction between body mass increments and feeding regime on magnitude of
immune response), which indicated to us that pseudoreplication did not
significantly confound our statistical inference.
Individual a priori pair-wise means comparisons were tested by
t-statistics corresponding to the two-sided P values.
Variables were log-transformed to improve distribution of residuals. The
standard level of significance 
=0.05 was applied. In the case of
multi-group comparisons in Table
1, we adjusted the conventional level of significance by applying
a Bonferroni correction. To do this, we divided =0.05 by 6, i.e. the
number of inter-group tests performed. All tests were carried out using the
SAS 9.1.3 statistical package.
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Feeding regime significantly affected the magnitude of PHA-induced swelling response (Table 1; Fig. 2C). This response was stronger in the AL group than in the two other feeding regimes (AL vs I group: P=0.007; AL vs FR group: P<0.0001). Likewise, nestlings from group I had a stronger swelling response than those from group FR, though this difference did not reach statistical significance (P=0.059). However, another ANCOVA test of the magnitude of PHA-induced swelling response as a dependent variable, with feeding regime as the main factor, and the total body mass change during the course of the whole experiment as a covariate, revealed a strong interaction between body mass change and feeding regime (Fig. 3A; F2,20=6.63, P=0.006). This interaction was marginally non-significant, when the analysis was restricted to body mass change during the first 2 days of experiment, that is, before the immune challenge (F2,20=3.44, P=0.052). By contrast, the interaction was far from significance when ANCOVA was carried out for body mass increments during day 3, i.e. 24 h following the immune challenge (Fig. 3B; F2,20=0.83, P=0.45).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Saino et al.,
1997; Birkhead et al.,
1999). However, we were also able to demonstrate that, depending
on energy intake, the correlation between body mass increments and PHA-induced
swelling response may take all possible directions: it was positive in the
ad libitum-fed AL group, negative in the food-restricted FR
nestlings, and non-significant in the intermediate I group. Particularly
relevant here are the results reported by Snoeijs et al.
(Snoeijs et al., 2005), who
found a negative correlation between PHA-induced swelling response and tarsus
growth in great tit nestlings exclusively fed by a single mother, and a
positive correlation in the young reared by both parents. Our study strongly
suggests that similar changes in immune function reported in many other field
studies involving manipulation of the brood size or parental effort (e.g.
Fargallo et al., 2002;
Saino et al., 2002;
Gwinner and Berger, 2006) are
primarily underlined by food availability. This supports the general
prediction that the immune-related trade-offs should be mainly expressed when
resources are limited (Sandland and
Minchella, 2003;
Schmid-Hempel, 2003).
It is also important to note that the correlation between the magnitude of PHA-induced swelling response and body mass increments, calculated across all feeding regimes applied in our experiment, was strongly positive (Fig. 3). However, in the context of within-regime correlations, the cross-regime correlation must be interpreted as the epiphenomenon of the between-regime variation of food intake. This again highlights the necessity to take into account the resource availability in studies on immune-related trade-offs carried out under natural conditions.
The interaction between feeding regime and body mass increments, which
underlies the correlations between the magnitude of PHA-induced swelling
response and changes in body mass (Fig.
3A), was significant only for the whole period of our experiment
(i.e. days 1-3), and non-significant for body mass increments after antigen
injection (i.e. during day 3, Fig.
3B). Thus, the correlations depicted in
Fig. 3A most likely reflect the
trade-off (or the lack thereof) involving the costs of development and
maintenance of immune function incurred prior to immune challenge
(constitutive costs) (sensu
Sandland and Minchella, 2003),
rather than the immediate investment in mounting a response to injected PHA
(i.e. inducible costs). When food is plentiful, as in the case of AL
nestlings, no limitations on nutrient or energy availability compromise immune
function (Klasing, 2004), and
the positive correlation between body mass increments and an immune response
presumably reflects the between-individual variation of genetic quality or
condition (Hõrak et al.,
2000; Hoi-Leitner et al.,
2001). In contrast to AL nestlings, under-fed FR nestlings traded
limited resources between competing demands of immune function and body mass
increments, which resulted in the observed inverse correlation between those
traits. However, immediate limitations resulting in this correlation are
difficult to identify, and deserve further study. Although widely used,
PHA-induced swelling response does not provide an unambiguous index of immune
function, because it involves both innate and adaptive components of the
immune response (Kennedy and Nager,
2006; Martin et al.,
2006). The costs of development, maintenance and use of these
components are different. Non-specific immune mechanisms are cheap to develop
and maintain, but the nutritional costs of their use are high, whereas the
opposite applies to the adaptive components of the immune response
(Klasing and Leschinsky, 1999;
Klasing, 2004). One can
therefore hypothesize that an inverse correlation between the magnitude of
PHA-induced swelling response and changes in body mass observed in FR
nestlings may stem from three processes: (i) a suppression of costly adaptive
components of the immune response, the development and maintenance of which
strongly impinge on the available nutrients, which are also required for the
competing demands of body mass increments; (ii) a suppression of costly acute
phase response; (iii) a suppression of both components.
The first hypothesis predicts the presence of a significant trade-off
between the magnitude of immune response and body mass increments before
antigen injection, whereas the second predicts the same after antigen
injection. In our experimental design the existence of such trade-offs would
be revealed by significant effects of the interaction between body mass
increments and feeding regime on the magnitude of PHA-immune swelling.
However, these interactions were not significant either before, or after
antigen injection, even though the interaction calculated over the whole
period of the experiment was highly significant
(Fig. 3A). This suggests that
neither hypotheses (i) nor (ii) may exclusively explain the observed pattern.
Nevertheless, our results lead us to reject the hypothesis that the
significant interaction resulted only from food shortage suppressing immediate
investment in mounting the acute phase response. It is also possible that the
growth retardation following PHA challenge may become apparent with some delay
longer than 24 h. However, the nestlings in our experiment were in the linear
phase of body mass growth (Turner and
Bryant, 1979), when its retardation due to conflicting resource
demands should be particularly evident. Moreover, several other studies
demonstrated that higher rate of development of immune function negatively
affects body mass growth or wing development
(Soler et al., 2003;
Brommer, 2004;
Mauck et al., 2005).
Our results suggest that the undernourished sand martin nestlings develop
higher immune function only at the expense of a part of their growth
potential. Body size is often a decisive factor, which determines the outcome
of sibling competition for food (Mock and
Parker, 1997). Therefore, if the development of immune function
drains some vital resources away from body mass increments, it may affect
nestlings' competitive abilities (Saino
and Møller, 2002). This effect is likely to be particularly
strong in asynchronously hatched broods, where younger and smaller nestlings
frequently face undernourishment (Mock and
Parker, 1997), and may be burdened with larger parasite load than
their bigger nest-mates (Christe et al.,
1998; Simon et al.,
2003). For example, Szép and Møller
(Szép and Møller,
2000) reported that parasitic infection increases the variation of
body mass in the sand martin broods. Thus, the trade-off between immune
function and body mass growth may significantly affect survival of small
nestlings in asynchronously hatched broods.
In conclusion, we demonstrated that the direction of correlation between magnitude of PHA-induced swelling response and body mass increments rate in young sand martins depends on food availability: they are inversely correlated when food is scarce, whereas both traits are positively correlated when the resources are plentiful. We therefore strongly advise that the design of the studies on immune function carried out under natural conditions should be based on a careful monitoring of the availability of resources essential for the immunity development and use.
|
Acknowledgments |
|---|
gorzata Lewoc, Bogusaw Lewoczuk,
Magorzata Olkowska and Joanna Przydacz. We would like to thank Mariusz
Cicho, William H. Karasov, Pawel Koteja, and Jan Taylor for their
valuable comments on earlier drafts of this paper. Nestlings were collected
under permission of the nature conservancy authorities (permit no.
DLOPiK.og-4201-03-95/2001/2002). All experimental procedures were accepted by
the ethics committee (permit no. LKE 68/OP/2001). This study was supported by
the State Committee for Scientific Research of the Republic of Poland grant 6
P04F 098 21 to P.B. |
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