Journal of Avian Biology 46: 40–45, 2015
doi: 10.1111/jav.00358
© 2014 The Author. Journal of Avian Biology © 2014 Nordic Society Oikos
Subject Editor: Ruedi Nager. Accepted 22 May 2014
Body-mass-dependent trade-off between immune response and
uropygial gland size in house sparrows Passer domesticus
Gregorio Moreno-Rueda
G. Moreno-Rueda ([email protected]), Depto de Zoología, Univ. de Granada, ES-18071 Granada, Spain.
Parasites greatly impact host fitness. The immune system is fundamental to combat endoparasites, and survival increases
with greater investment in immunity. Some ectoparasites, by contrast, are reportedly combated by the use of the uropygial
gland, an organ exclusive to birds, which secretes an oily substance (preen oil) that is spread on plumage. However, both
mounting an immune response against a parasite and producing uropygial gland secretion depend on the same resources, a
situation which may induce trade-offs between the two antiparasitic functions. In this study, I experimentally test whether
immune response is traded off against uropygial gland size in the house sparrow Passer domesticus. In the experiment, a
group of sparrows were injected with an antigen (lipopolysaccharide, LPS), which stimulates the immune system, while
the other group received a sham injection. The uropygial gland of LPS-treated birds decreased significantly more than that
of the control birds after treatment. Nevertheless, the effect of the treatment was limited to house sparrows with low body
mass, suggesting that heavy house sparrows were able to produce an immune response while maintaining a relatively large
uropygial gland. Given that uropygial gland size is strongly related to production of preen oil, these results suggest that
preen oil production declines in birds in poor body condition when resources are preferentially diverted to other demanding functions, such as the immune system. Considering that the uropygial gland is involved in several fitness-related
processes in birds, the trade-off between immune response and uropygial gland size may have important consequences for
bird life histories.
Pathogens and parasites exert a major impact on the fitness
of organisms (reviewed by Schmid-Hempel 2011). Consequently, host organisms have evolved a set of strategies in
order to combat parasites, one of the most important being
the immune system (Davison et al. 2008), so that survival
increases with immune capacity (Møller and Saino 2004).
Nevertheless, birds may host different types of parasites
(Clayton and Moore 1997), requiring different antiparasitic
strategies. Endoparasites such as Apicomplexa protozoans
usually trigger the immune system (Bonneaud et al. 2006).
However, ectoparasites, which live on the host surface, are
usually not affected by the host’s immune system (but see
Møller and Rózsa 2005, Owen et al. 2010) and would be
combated with other anti-parasite mechanisms (Clayton
et al. 2010).
Ectoparasites such as feather-degrading bacteria, egg-shell
bacteria, or chewing lice (order Phthiraptera), negatively
impact the host’s fitness (Brown et al. 1995, Clayton et al.
1999, Saag et al. 2011, Soler et al. 2012). It has been proposed that birds combat these ectoparasites with uropygial
gland secretions (preen oil), which birds spread onto their
plumage when preening. In vitro studies have shown that
preen oil has antibacterial and antifungal properties
(Bandyopadhyay and Bhattacharyya 1999, Shawkey et al.
2003, Reneerkens et al. 2008). Correlational (Møller et al.
2009) and comparative studies (Soler et al. 2012) relating
40
uropygial gland size which is directly proportional to preen
oil volume (Pap et al. 2010) with bacteria load, support the
contention that preen oil affects parasitic bacteria. Nevertheless, in vivo experimental studies have failed to find any
effect of preen oil on feather-degrading bacteria (Czirják
et al. 2013, Giraudeau et al. 2013). Similarly, Moyer et al.
(2003) showed that preen oil has an insecticidal effect against
chewing lice in vitro, but not in vivo.
Although the anti-parasitic function of preen oil is still
under debate, its positive effect on plumage is well established. Plumage condition is positively correlated with
uropygial gland size (Moreno-Rueda 2010b, 2011a), while
plumage condition deteriorated in birds that had access to
their uropygial gland experimentally blocked (Jacob and
Ziswiler 1982, Moyer et al. 2003, Giraudeau et al. 2010a).
Moreover, the uropygial gland intervenes in other important
functions for bird’s fitness, such as sexual communication,
by producing pheromones (Hagelin 2007, Hirao et al. 2009,
Zhang et al. 2010, Whittaker et al. 2011, Amo et al. 2012)
and affecting bird coloration (Delhey et al. 2007, 2008,
Surmacki and Nowakowski 2007, López-Rull et al. 2010,
Pérez-Rodríguez et al. 2011, Amat et al. 2011).
Considering the importance of both the uropygial gland
and the immune system for bird fitness, individuals may be
expected to invest as much as possible in both traits. However, mounting an immune response is energetically costly
(Martin et al. 2003, Demas 2004, Schmid-Hempel 2011).
Moreover, preen oil is composed mainly of oily substances
(Sweeney et al. 2004), which require considerable energy in
their anabolism. Thus, it is presumable that the synthesis of
preen oil is also energetically costly. Moreover, lipids diverted
for preen oil production cannot be used for immune functions and vice versa. Furthermore, preening behaviour that
is essential for the use of preen oil is an energetically costly
activity (Goldstein 1988), taking up a substantial portion of
a bird’s time budget (Walther and Clayton 2005). Hence,
birds in better condition may have more time and energy
available to invest in preen oil production and preening. In
support of this contention, the size of the uropygial gland
has been positively correlated with body condition in house
sparrows Passer domesticus (Moreno-Rueda 2010b). Therefore, it is probable that both mounting an immune response
and producing preen oil compete for energy. When two
fitness-related traits compete for the same resources, investment in one trait implies a decrease in the resources available for the other life-history traits, leading to a trade-off
between the two traits (de Jong and van Noordwijk 1992,
Stearns 1992, Zera and Harshman 2001, Roff 2002,
Garland 2014). In fact, the immune response to an antigen is
frequently traded-off against other life-history components,
such as reproduction or self-maintenance (review by Ardia
and Schat 2008).
Following this reasoning, I hypothesise that there is a
trade-off between uropygial gland size and immune response
in birds. One prediction of this hypothesis is that birds
mounting an immune response against an antigen should
reduce preen oil production, given that they divert energy
from the uropygial gland to the immune system. Supporting
this prediction, the uropygial gland grew less in tawny owl
Strix aluco nestlings challenged with an antigen (lipopolysaccharide from the cell wall of Escherichia coli, LPS) than in
control owlets (Piault et al. 2008). A smaller uropygial gland
indicates lower preen oil production, as uropygial gland size
is positively correlated with preen oil volume (Pap et al.
2010). Despite of the current interest in the uropygial gland
function in birds, no study has tested the trade-off between
immune system in other species, nor in adult individuals (in
which the function of uropygial gland is more evident). In
the present paper, I examine the trade-off between immune
system and uropygial gland size in adult birds, by stimulating the immune system in a group of moulting house sparrows, which were inoculated with LPS, while another group
served as control. Then, I examined the change in uropygial
gland size between the two groups, which is indicative of
change in preen oil production.
Material and methods
The study was conducted during September 2011 with 88
adult house sparrows (19 females and 69 males). Sparrows
were captured at 5 September 2011 with mist-nets on a farm
in Padul (SE Spain, 37°01′28″N, 3°37′36″W), and quickly
transferred to an outdoor aviary located in Moraleda de
Zafayona (37°11′N, 3°57′W; SE Spain; 60 km away). No
bird suffered any damage during capture, transport, maintenance in the aviary or as a consequence of the experiment.
The aviary structure followed the recommendations of the
European directive as well as national legislation. Measuring
about 60 m3, the aviary was built with bricks at the base (1-m
height) and a complete wall, the remaining being covered
with a mesh (1 cm2 openings) supported by a metal framework. The structure was designed to avoid injuring the birds.
A roof was provided to protect birds from rainfall and direct
sunlight. All birds were individually marked with colour
rings, and were supplied with water and food (seed mixture,
fruit, and different vitamins and minerals) with ad libitum
access, as well as diverse perches, and trays with water and
powder for bathing and dust bathing (Moreno-Rueda and
Soler 2002). The aviary, and especially the water and food
containers, were carefully cleaned and disinfected before the
capture of birds. Confinement lasted for five days, and when
the study ended, sparrows were released in the same place
where they had been captured. The study was performed
with the permissions of the Andalusian government.
On 5 September 2011, 35 males and 9 females were
subcutaneously injected in the patagium with 0.1 mg of a
lipopolysaccharide (LPS) from the cell wall of Escherichia
coli (serotype 055:B5, L-2880, Sigma Aldrich), diluted in
0.01 ml of isotonic phosphate buffer. This substance acts
as an antigen, provoking a humoral immune reaction that
mimics an infection, and diverts energy from other functions to the immune system. Consequently, inoculating LPS
lowers body mass in the house sparrow (Bonneaud et al.
2003, Moreno-Rueda 2011b). Another 34 males and 10
females were injected with 0.01 ml of isotonic phosphate
buffer saline (PBS) as a control. I assigned the treatment to
each bird following a sequential criterion (taking sex into
account): first LPS, then PBS, guaranteeing randomization,
as the birds were captured. To determine whether the antigen effectively stimulated the immune system, I measured
the thickness of the patagium where the substances were
inoculated with a pressure-sensitive micrometer (Mitutoyo;
accuracy 0.01 mm), in a subset of 24 sparrows (12 inoculated with LPS and 12 with PBS). Measurements were taken
before injecting the substance and four hours afterwards,
when the immune response to LPS is maximal (Parmentier
et al. 1998), and calculated the difference between the two
measures as swelling due to LPS. Then, I tested whether
the patagium significantly swelled in LPS-inoculated birds,
which would indicate an immune response to the antigen.
I measured the uropygial gland size and body mass the
day that the experiment started, and five days afterwards (10
September 2011). I measured the length, width, and height
(from the base of the gland to the base of the papilla) of
the uropygial gland (three times each) with a digital calliper
(accuracy 0.01 mm), and estimated its size by multiplying
the three measurements, which is a good estimator of gland
volume and preen oil production (Pap et al. 2010). I repeated
this process, resulting in two estimates of uropygial gland size
for 21 sparrows and then calculated the repeatability (after
Lessells and Boag 1987) of the two estimates of uropygial
gland size yielding r ⫽ 0.76 (F1,19 ⫽ 72.70, p ⬍ 0.001).
I measured body mass, with a digital balance (accuracy
0.1 g). In the study population, body mass is a good indicator of body condition (Moreno-Rueda 2010b) explaining 86.3% of variation in body condition (F1,93 ⫽ 597.3,
p ⬍ 0.001). Body condition was estimated as the residuals
41
of body mass regressed on tarsus length (measured with a
digital calliper, accuracy 0.01 mm) with both variables logtransformed. Thus, I used body mass as a proxy for body
condition.
The change in uropygial gland size during the experiment
was statistically tested with a paired t-test. The effect of the
treatment and sex on the magnitude of change in both uropygial gland size (final gland size minus initial gland size) and
body mass was tested with linear models of type-III sums
of squares, implying no a priori hypotheses of how variance
should be decomposed (Quinn and Keough 2002). Both
initial uropygial gland size and body mass were included
in the model as covariates, given that both were related to
change in gland size and initial uropygial gland size, respectively (see Results). In all models, collinearity among continuous variables was checked by examining tolerance (Quinn
and Keough 2002), which in all cases was higher than 0.85.
Normality and homoscedasticity of residuals of the models
were checked according to Shapiro–Wilks and Levene’s tests,
respectively (Quinn and Keough 2002). Means are given
with the standard error.
Results
There were no significant differences in initial body mass
(F1,86 ⫽ 0.14, p ⫽ 0.71) or uropygial gland size (F1,86 ⫽ 0.28,
p ⫽ 0.60) between LPS- and PBS-injected sparrows before
the treatment (Table 1). Females weighed less than males
(F1,86 ⫽ 4.63, p ⫽ 0.034), but there was no sexual differences in uropygial gland size (F1,86 ⬍ 0.01, p ⫽ 0.94; Table 1).
The inoculation of LPS stimulated an immune response,
in contrast to the inoculation of PBS (swelling of the patagium according to treatment, LPS: 0.37 ⫾ 0.06 mm; PBS:
0.03 ⫾ 0.02; t-test, t22 ⫽ 6.44, p ⬍ 0.001). The uropygial
gland size shrank during the experiment (paired t-test,
t87 ⫽ 11.73, p ⬍ 0.001; Table 1). Heavier sparrows tended
to have larger uropygial glands, although not significantly
(r ⫽ 0.19, p ⫽ 0.08). Moreover, reduction in uropygial
gland size was correlated with initial uropygial gland size
(r ⫽ ⫺0.49, p ⬍ 0.001); that is, birds with larger uropygial
glands underwent greater reductions in gland size. For these
Table 1. Mean ⫾ SE of both initial uropygial gland size and body
mass for male and female house sparrows in each treatment, as
well as changes in uropygial gland size and body mass.
LPS-treatment
(n ⫽ 35 males and
9 females)
Initial uropygial gland size (in mm3)
Males
147.60 ⫾ 5.65
Females
142.31 ⫾ 11.15
Initial body mass (in g)
Males
27.12 ⫾ 0.38
Females
25.70 ⫾ 0.75
Change in uropygial gland size (in mm3)
Males
⫺26.13 ⫾ 3.01
Females
⫺26.25 ⫾ 6.08
Change in body mass (in g)
Males
⫺1.04 ⫾ 0.19
Females
⫺1.11 ⫾ 0.38
42
PBS-treatment
(n ⫽ 34 males and
10 females)
148.91 ⫾ 5.73
154.77 ⫾ 10.56
27.26 ⫾ 0.39
26.17 ⫾ 0.71
⫺25.57 ⫾ 3.09
⫺22.92 ⫾ 5.74
⫺0.49 ⫾ 0.19
⫺1.33 ⫾ 0.36
reasons, in order to determine the effect of the treatment
on change in uropygial gland size, I introduced treatment as
factor, as well as initial body mass and initial uropygial gland
size as covariates. Only significant interactions were retained
in the final model.
The model revealed that reduction in uropygial gland
size was significantly higher in LPS- (least squares mean:
⫺26.15 ⫾ 2.65 mm3) than in PBS-inoculated birds
(⫺24.96 ⫾ 2.65 mm3; Table 2), but depended on body
mass. Larger uropygial glands lost more volume (β ⫽ ⫺0.47)
and the uropygial glands shrank less in heavier sparrows
(β ⫽ 0.21, Table 2). Moreover, I found a significant interaction between initial body mass and treatment (Table 2). This
interaction occurred because in LPS-inoculated sparrows,
the reduction in uropygial gland size was lower the heavier
the birds (r ⫽ 0.43, p ⬍ 0.01), while in PBS-inoculated birds
there was no relationship between initial body mass and
reduction in uropygial gland size (r ⫽ ⫺0.11, p ⫽ 0.46; Fig.
1). That is, there was no difference in change of uropygial
gland size between LPS- and PBS-inoculated sparrows when
the birds were relatively heavy, while in the lightest birds the
uropygial gland size was more reduced in LPS-challenges
sparrows than in PBS-inoculated birds.
Although body mass decreased during the experiment
(paired t-test, t87 ⫽ 6.95, p ⬍ 0.001; Table 1), the effect of the
LPS antigen on uropygial gland size cannot be ascribed to a
correlated effect on body mass, given that, in this study, LPS
inoculation did not affect body mass. The change in body
mass during the study period was not influenced by treatment (F1,85 ⫽ 2.37, p ⫽ 0.13), while it was negatively related
to initial body mass (β ⫽ ⫺0.34, F1,83 ⫽ 11.48, p ⫽ 0.001).
Moreover, change in uropygial gland size was not correlated
with change in body mass (r ⫽ ⫺0.04, p ⫽ 0.71), nor there
was any interaction with treatment (F1,83 ⫽ 0.31, p ⫽ 0.58;
controlling for initial uropygial gland size).
Discussion
This study provides evidence of a mass-dependent trade-off
between immune response and uropygial gland size in the
house sparrow. Uropygial gland size was more reduced in
birds challenged with an antigen than in control birds. However, this trade-off was mass dependent, as lighter-weight
sparrows paid a cost, greater reduction in uropygial gland
size, while this trade-off was not detected in heavy sparrows.
The reduction in uropygial gland size in sparrows was probably due to a reduction in preen oil production, given that
Table 2. Results of the final lineal model examining the effect of
treatment on change in uropygial gland size, controlling by initial
uropygial gland size and initial body mass. Only significant interactions have been retained. A model including sex gave qualitatively
the same results, sex having no significant effect (data not shown).
F- and p-values are shown, as well as degree of freedom (DF).
Effect
DF
F
p
Treatment
Initial body mass
Initial uropygial gland size
Treatment ⫻ Body mass
Error
1
1
1
1
83
6.02
4.78
25.78
5.94
0.016
0.032
⬍ 0.001
0.017
Figure 1. Change in uropygial gland size according to body mass in
house sparrows injected with LPS antigen (black points, continuous line) and PBS control (empty squares, dashed line).
preen oil volume is positively correlated with uropygial gland
size in the house sparrow (Pap et al. 2010).
The results in the present study coincide with those
reported in Piault et al. (2008). Similarly, Pap et al. (2013)
found that house sparrows infected with coccidians have
smaller uropygial glands. As a whole, all these studies support the idea that birds fighting an infection may pay a cost
in the form of reduced preen oil production. Birds mounting an immune response decreased their uropygial gland size
presumably because the two systems compete for similar
resources, mainly energy (see Introduction). The fact that
the trade-off between immune response and uropygial gland
size was apparent only in light-weight sparrows supports this
idea. In the house sparrow, the uropygial gland size is larger
and immune response stronger in birds in better condition
(Møller et al. 1998, González et al. 1999, Navarro et al.
2003, Moreno-Rueda 2010b), suggesting that both preen oil
production and the immune response are costly, so that only
individuals in good condition may afford them.
When house sparrows are challenged with an antigen during breeding or wintering, they lose body mass (Bonneaud
et al. 2003, Moreno-Rueda 2011b), given that mounting an
immune response is energetically costly (Martin et al. 2003).
However, during moult (the phase in which this study was
made), immune-challenged sparrows maintain their body
mass by suppressing another energy-consuming function, the
moult (Martin 2005, Moreno-Rueda 2010a). There is also
a trade-off between moult speed and body mass (MorenoRueda 2010a). Therefore, heavy sparrows, with substantial
reserves, probably mount an immune response while maintaining body mass and uropygial gland size, by suppressing
moult. However, in light-weight sparrows that are mounting an immune response, it is probable that the energy
re-allocated from the moult (suppressed) to immune system was
not sufficient to mount a suitable immune response. Therefore,
they had to divert resources otherwise allocated to preen oil
production, resulting in the observed reduction in uropygial
gland size. However, this is an ad hoc hypothesis that should
be properly evaluated. In any case, the accumulated evidence
points to complex trade-offs among the immune response,
preen oil production, fat accumulation, and moult.
House sparrows in poor condition that, moreover, are
mounting an immune response would pay a number of
costs related to a small uropygial gland. As mentioned in the
Introduction, if preen oil is a defensive method against
ectoparasites, results in this study suggest that combating
ectoparasites with preen oil and combating endoparasites
with a humoral immune response should be traded-off.
Thus, poor-condition birds should not be highly resistant
to endoparasites and ectoparasites at the same time. Hence,
hosts facing immune stimulation could be less resistant or
tolerant to ectoparasites such as feather-degrading bacteria. Consequently, they become more susceptible of plumage deterioration (Moreno-Rueda 2010b, 2011a), which
in turn is related to diminished thermoregulation capacity (Booth et al. 1993), poorer flight ability (Barbosa et al.
2002), delayed arrival from migration (Møller et al. 2004),
delayed breeding (Pap et al. 2005), and reduced survival
expectancy (Clayton et al. 1999, Pap et al. 2005). In fact,
mallards Anas platyrhynchos deprived of uropygial gland
secretion show reduced body condition and lay smaller eggs
than mallards with a normal uropygial gland (Giraudeau
et al. 2010b). Moreover, birds with smaller uropygial glands
are more depredated, probably as a consequence of having
plumage in worse conditions (Møller et al. 2010). Therefore,
future survival and breeding success might be diminished in
poor-condition immunochallenged birds as a consequence
of reduced uropygial gland. Nonetheless, long-term studies
in free-living birds would be necessary in order to evaluate
the impact of uropygial gland shrinkage during an immune
challenge.
Moreover, the uropygial gland affects the size and coloration of different visual sexual signals in birds (Delhey
et al. 2007), as well as pheromone emission (Hagelin 2007).
Therefore, a reduction in uropygial gland size associated with
an immune response might explain why individual attractiveness is reduced in some species when investing more
in the immune response. For example, immune challenge
by diphtheria and tetanus antigens provokes a reduction in
the extent of white plumage in common eider Somateria
mollissima (Hanssen et al. 2008). Various feather-degrading
bacterial strains deteriorate white feathers quicker than
feathers of other colours (Burtt and Ichida 2004, Goldstein
et al. 2004, Gunderson et al. 2009; but see Grande et al.
2004), affecting the size of sexually selected patches
(Ruiz-de-Castañeda et al. 2012). Individuals with smaller
uropygial glands are more affected by feather-degrading
bacteria (Møller et al. 2009). Therefore, white plumage of
birds heavily investing in immune system could be more
deteriorated (leading to smaller patches) as a consequence
of having a smaller uropygial gland. In this way, the results
in this study could explain the findings in Hanssen et al.
(2008).
In conclusion, the results in the present study show that,
in birds with low body condition, the investment in immune
response is traded against investment in uropygial secretion.
Given that the uropygial gland is involved in several aspects
of bird survival and reproduction, this trade-off might be
relevant for bird fitness.
43
Acknowledgements – GM-R was supported by a postdoctoral fellowship and a research contract (Juan de la Cierva programme) by the
Spanish government (Ministerio de Ciencia e Innovación). José M.
Rivas and Álvaro Rivas helped me during the capture of the birds.
Carlos Marfil Daza helped me during the experimental study.
David Nesbitt and Jean Mattos-Reaño revised the English. All work
was performed with the permission of the Andalusian government.
Comments by Csongor Vágási greatly improved the manuscript.
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