Behavioral Ecology Vol. 10 No. 3: 281-286
© 1999 International Society for Behavioral Ecology
Weight lifting and health status in the black wheatear
a Departamento Biología Animal y Ecología, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain b Laboratoire d'Ecologie, CNRS URA 258, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
Address correspondence to A. P. Møller. E-mail: amoller{at}hall.snv.jussieu.fr
Received 23 April 1998; revised 9 October 1998; accepted 25 October 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Male black wheatears Oenanthe leucura demonstrate an exaggerated sexual display by carrying many heavy stones (on average 3.1 kg per season for this 35-g passerine) to cavities inside caves before the start of each clutch. The energetic cost of this display is mainly determined by the size of stones, which gives rise to the largest power output of a muscle ever recorded for any species (400 W / kg), rather than the total number of stones carried, which only amounts to 1% of daily energy expenditure for a black wheatear male. We tested whether stone carrying reflected male health status by removing two primaries from a group of males, but not from controls. Experimental manipulation did not significantly affect stone carrying. Similarly, male health status measured as hematocrit, leukocyte concentration, and T-cell response to an injection with phytohemagglutinin (a lectin) was not affected by experimental manipulation. Male black wheatears that carried very heavy stones, each on average more than a quarter of their own body mass, had a stronger T-cell response to injection with a lectin than males that carried light stones. Furthermore, males that carried heavy stones had a reduced hematocrit level, which may have arisen from the effects of the extremely heavy work load. Rate of stone carrying and mass of stones was not significantly related to the abundance of two species of ectoparasites. Male black wheatears with high T-cell responses were significantly more likely to survive than males with low responses, but other measures of male performance did not differ significantly between survivors and nonsurvivors. The male stone-carrying display thus reflects male health status as demonstrated by a component of immunocompetence.
Key words: hematology, immune response, Oenanthe leucura, phytohemagglutinin, sexual selection, survival, T-cell response, wheatears.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Secondary sexual characters and sexual displays are often condition dependent in their expression, with excessively displaying individuals having superior condition both before as well as after the display (review in Andersson, 1994
). Receivers of
a sexual signal may use information on the condition of the signaler to obtain
direct fitness benefits in terms of fertility or costly parental care, or
indirect benefits in terms of genetically based viability. Differences in
condition may arise as a consequence of individual differences in parasitism,
hypothesized to be caused by genetically based resistance to parasites
(Hamilton and Zuk, 1982).
Sexual selection based on condition-dependent secondary sexual characters may
continuously reflect that ability of individuals to resist attacks from
currently detrimental parasite genotypes because frequency-dependent selection
maintains continuous variation in host resistance
(Hamilton and Zuk, 1982).
There is mounting evidence that parasites play an important role in host
sexual selection (Hamilton and Poulin,
1997; Møller et al.,
1999), particularly because host sexual displays reliably reflect
host immunity rather than the burden of innocuous parasites often studied by
behavioral ecologists (Møller et
al., 1998a).
Host immunity has been hypothesized to be directly revealed by secondary
sexual characters (Folstad and Karter,
1992), either because of the immunosuppressive effects of
biochemicals necessary for development of the sexual displays
(Folstad and Karter, 1992), or
because reproductive effort cannot be used simultaneously for sexual display
and immunity (Møller and Saino,
1994; Wedekind and Folstad,
1994). Comparative evidence suggests that bird species with
extravagant sexual coloration invest more heavily in immune function as
assessed from the size of their immune defense organs and the circulating
levels of leukocytes than bird species with sexually monomorphic displays
(Møller et al., 1998a).
Furthermore, there is a positive relationship between investment in immune
function in birds and extrapair paternity, which constitutes a measure of
intensity of an important component of sexual selection
(Møller, 1997a). Male
birds often have depressed immune function when adults, and the degree of
immunodepression is positively related to the intensity of sexual selection as
estimated from the frequency of extrapair paternity
(Møller et al., 1998b).
There is a growing number of intraspecific studies demonstrating associations
between the expression of secondary sexual characters and various measures of
immunity. For example, Saino and Møller
(1996) demonstrated that a
measure of B-cell-mediated immunity was depressed by experimentally increasing
the size of a secondary sexual character in the barn swallow Hirundo
rustica, and the measure of immunity was positively related to the
original expression of the sex trait. These results are consistent with the
secondary sexual character being a reliable signal of one component of
immunocompetence. Studies of 12 species have so far investigated the
relationship between immunity and morphological displays such as colors and
the size of secondary sexual characters, and these studies found positive
associations between immunocompetence and exaggeration of sexual displays
(review in Møller et al.,
1999). Currently, we are only aware of a single study
investigating the relationship between a behavioral display and immunity
(Saino et al., 1997e). Hence,
there is a need for additional studies of the role of immunity in behavioral
sexual displays.
The black wheatear is a small (about 35 g) passerine bird that is resident
in Spain and Morocco. Some weeks before egg laying, males start to collect
stones from the ground and place these in cavities in cliffs, caves, or
buildings while the female mate is present
(Moreno et al., 1994;
Soler et al., 1996).
Individual males carry stones that each weigh on average from 3.4 g to 8.2 g
for different males, in total 0.3-10.1 kg, on average 3.1 kg of stones per
season (Moreno et al., 1994).
The stone-carrying activity is performed before each breeding attempt during
the breeding season, although more stones are carried before the first
breeding attempt (Soler et al.,
1995). Male morphology is adapted to stone carrying: males have
large wing areas that give rise to a low wing loading compared to that of
females (Møller et al.,
1995). Male stone carrying is inversely related to wing loading
(Møller et al., 1995).
Females mated to males that carry more stones start laying earlier, lay more
eggs and clutches, and on average raise more offspring per season than females
mated to males that carry few stones
(Moreno et al., 1994;
Soler et al., 1996).
Experimental manipulation of the number of stones by addition or removal of
stones demonstrated that males are able to compensate for stone removal, and
they carry stones at a slower rate if stones are added
(Soler et al., 1996).
Handicapping of males by removal of primary feathers from each wing resulted
in a reduction in stone-carrying activity, which in turn reduced female
reproductive effort (Soler et al.,
1996).
The aim of the present study was to test the hypothesis that males signal
their current health status to their partner by carrying many heavy stones. We
predicted that males that carry many heavy stones would have lower hematocrit
levels, lower concentrations of leukocytes, lower erythrocyte sedimentation
rates, stronger immune responses, and have fewer parasites than males that
carry fewer stones. High levels of hematocrit are indicative of recent
exercise, whereas excessive exercise caused by extreme work load will depress
haematocrit (review in Birchard,
1997; Harrison,
1985). Hence, we predicted that the extremely heavy work load of
male black wheatears during bursts of stone carrying should result in a
reduction in hematocrit. Circulating levels of leukocytes reflect current
infection status for a number of parasites and diseases, with high levels
indicative of poor health (e. g., Dein,
1986). If male black wheatears that carry many heavy stones are
particularly healthy, we would predict that they had lower concentrations of
leukocytes than males that carry few light stones. The two main branches of
the vertebrate immune system are cell-mediated and humoral immunity
(Klein, 1990;
Roitt et al., 1996;
Wakelin, 1996). Here we
assessed one component of immune function in black wheatears, a measure of
T-cell-mediated immunity, based on the intensity of swelling of the skin of
the patagium in response to an injection with a lectin
(Cheng and Lamont, 1988). We
used this method because it does not require extensive recapture of
individuals. It is based on the observations that phytohemagglutinin has a
strong mitogenic effect on T-lymphocytes, stimulating macrophage infiltration
and dense perivascular accumulation of lymphocytes
(Goto et al., 1978;
McCorkle et al., 1980;
Stadecker et al., 1977). The
increase in thickness of the patagium of the wing has been shown to correlate
with a number of components of fitness in free-living birds (e. g.,
Saino et al., 1997b). If male
black wheatears carrying many heavy stones are healthy, we would expect them
to have stronger T-cell responses than males carrying few light stones.
The predictions were tested by experimentally manipulating the working
ability of male black wheatears by either removing primaries number four and
five or by handling the wings without feather removal, and subsequently
assessing the three health parameters of the males. Previous experiments have
demonstrated that feather removal has a strong negative effect on
stone-carrying ability of males because it increases wing loading and hence
reduces the stone-lifting ability of males
(Møller et al.,
1995).
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MATERIALS AND METHODS |
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Study area
We studied black wheatears in Hoya de Guadix, Granada Province, Spain, during March-July 1996. Breeding sites of this species are restricted to areas with nest holes in cliffs or deserted buildings. Based on our experience from a previous study, we located all potential breeding territories and captured the territory owners. We found 38 territories with black wheatears. Not all birds were captured due to practical difficulties, and the final sample size was thus reduced to 29.
We searched territories regularly for nests and recorded the breeding
activities of pairs, including information on date of start of laying, clutch
size, brood size at fledging, number of broods, and seasonal reproductive
success. We obtained information on precipitation for the spring months
January-March for the weather station at Guadix, which is in the center of our
study site
(Consejería
de Medio Ambiente, 1997).
Capture, measurement, and blood sampling of adults
Adult black wheatears were captured in snap traps with a mealworm. After
capture adults were measured (length of wing, outermost tail feathers, length
of white part of seventh rectrix, all measured to the nearest 1 mm, length of
tarsus to the nearest 0.1 mm) and weighed (with a Pesola spring balance to the
nearest 0.1 g). When nestlings were approximately 13 days old, they were
measured as described for adults.
We removed a sample of blood from the brachial vein of each adult black
wheatear and placed the sample in two standard 100-µl capillary tubes. The
capillary tubes were stored horizontally in a cooling box with frozen cooling
blocks. Tubes were subsequently centrifuged for 10 min at 11,500 rpm, and the
hematocrit and the buffy coat (which mainly consists of leukocytes and was
used as an estimate of leukocyte concentration; e.g.,
Dein, 1986) were expressed as
the percentage of the capillary (measured to the nearest 0.1 mm) occupied by
erythrocytes and the buffy coat, respectively. The plasma and the erythrocytes
were then separated and frozen.
We assessed T-lymphocyte immune responsiveness by injecting the patagium
with phytohemagglutinin (PHA). The thickness of the left- and right-wing webs
(patagia) of adult males at premarked sites was measured three times with a
caliper to the nearest 0.01 mm. The right-wing web was injected with 0.2 mg of
PHA (Sigma, L-8754) in 0.04 ml of phosphate-buffered saline (PBS). The
left-wing web was injected with 0.04 ml PBS only. Males were kept in a cage
for 12 h and provided with mealworms and water ad libitum. After 12 h we
remeasured the thickness of wing webs at the inoculation sites. The measure of
immune response is the difference in wing web thickness after 12 h and
immediately after injection for the PHA-inoculated wing minus the difference
in wing web thickness after 12 h and immediately after injection for the
PBS-inoculated wing (see Saino et al.,
1997b, for details). The measurements of PHA response of the same
individuals were significantly repeatable (F = 8.83, df = 23,24,
p =.0068). The assessment of immunity was performed during the
prebreeding period in early spring during the time of stone carrying.
We assessed the abundance of two species of ectoparasites in adult males.
The abundance of Mallophaga of the suborder Ischnocera was assessed from the
number of holes in the primaries, secondaries, and rectrices because these
feather lice chew large, clearly visible holes in feathers (e.g.,
Møller, 1991). This
estimate of lice abundance is strongly positively correlated with the
abundance estimated directly from counts of lice in another passerine
(Møller, 1991). Black
wheatears are parasitized by an unidentified species of hematophagous mite
that sucks blood from the skin around the eyes and the bill. The abundance of
this species of mite was estimated by carefully counting the number of mites
around the eyes and the bill.
We repeatedly searched the study area during intensive field work during 1997-1998 for the presence of survivors from 1996. Male black wheatears are resident passerines that often stay in their territories throughout the year. Breeding dispersal is very restricted, usually being limited to movements to a neighboring territory (M. Soler et al., unpublished data). Hence it is unlikely that males that were not resighted in 1997-1998 were breeding elsewhere.
Experimental manipulation of stone-carrying ability
We manipulated the ability of males to carry stones by randomly allocating
a sample of males captured before the start of stone carrying to either of two
treatments: (1) removal of primaries number four and five by cutting the
feathers at the base (manipulation) or (2) capturing the male and handling the
wings as in the first treatment without cutting them (control). We did not use
a sham manipulation by, for example, removing the tips of two feathers in some
birds, as done previously (Møller
et al., 1995) because a previous experiment demonstrated that
there were no differences between males that were handled and males that were
sham manipulated (Møller et al.,
1995). Males were manipulated on average 14.9 days (SE = 4.3,
n = 29) before they were tested for immune responsiveness, and there
was no difference between experimental and control males [mean (SE),
experimental: 15.1 (6.2), n = 14; control: 14.7 (6.0), n =
15). The two groups of males did not differ significantly (p >.05)
with respect to any of the morphological measurements recorded.
Statistical analyses
Hematocrit and leukocyte concentration were expressed as the proportion of
erythrocytes and leukocytes, respectively, that constituted the entire
capillary tube. We assessed the reliability of the estimates of hematocrit and
leukocyte concentration in different capillary tubes with repeatability
analyses that quantify the amount of within-individual as opposed to
among-individual variation (Falconer and
Mackay, 1996).
Differences between experimental treatments were assessed by means of
one-way analyses of variance. When several analyses were made for a single
data set, the level of significance of 5% was adjusted for the number of tests
made using the sequential Bonferroni adjustment
(Holm, 1979). Not all
variables were estimated for all males, and sample sizes thus differed
slightly among the statistical tests. Values are reported as means ±
SE.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Stone carrying and health status
Before the first clutch, male black wheatears carried, on average, 163±2 stones (n = 29 males) weighing 6.54±0.35 g, in total 1173±184 g. The height of the nest, where most stones were located, was 148±10 cm (n = 29). The experimental treatment did not significantly affect the number of stones carried (F = 0.84, df = 1,27, p =.37; experimental: 183±35, n = 14; control: 137±15, n = 15), average mass of stones (F = 1.45, df = 1,27, p =.24; experimental: 7.02±0.360 g, control: 6.16±0.56 g), total mass of stones (F = 1.00, df = 1,27, p =.33; experimental: 1,378± 283 g; control: 1.062±238 g), or nest height (F = 1.05, df = 1,27, p =.31; experimental: 137±15 cm; control: 155±12 cm).
The total number of stones carried by males was positively correlated with the mean mass of stones (r =.45, n = 29, p =.019), but it was unrelated to the height of the cavity (r =.08, p =.78). Similarly, mean stone mass for individual males was unrelated to the height that the stones were carried (r = -.08, p =.71).
The experimental treatment did not significantly affect the phytohemagglutinin response (F = 1.26, df = 1,19, p =.29; experimental: 0.303± 0.035, n = 11; control: 0.354±0.029, n = 10). The power of this test is low, so the null hypothesis of no significant difference cannot readily be accepted. Average mass of stones was positively correlated with the response to injection with phytohemagglutinin [Figure 1; F = 9.27, df = 1,19, r2 =.33, p =.0067; mean stone mass (g) = (4.00±1.10) + [(9.98±3.28) x T-cell response] (mm)]. The total number of stones carried was not significantly related to immune responsiveness to phytohemagglutinin (F = 0.002, df = 1,19, p =.96).
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Hematocrit estimates were significantly repeatable among blood samples collected from the same male (F = 58.22, df = 22,23, p <.0001). Hematocrit values were not affected significantly by the experimental treatment (F = 0.12, df = 1,20, p =.73). Male black wheatears that carried heavy stones had a low hematocrit value compared to males that carried light stones [Figure 2; F = 5.13, df = 1,20, r2 =.16, p =.035; mean stone mass (g) = (24.12±7.60)—(31.73± 14.00) x hematocrit]. The fit was not significantly improved by a polynomial regression. The total number of stones was not significantly related to hematocrit (F = 1.44, df = 1,20, p =.24).
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Leukocyte estimates were significantly repeatable among blood samples collected from the same male (F = 4.73, df = 22,23, p =.040). Leukocytes were not significantly affected by the experimental treatment (F = 0.27, df = 1, 19, p =.69). The concentration of leukocytes in the blood was not significantly related to the two measures of stone carrying (F <.29, df = 1,19, p >.60).
The prevalence of the single species of Mallophaga was 0.86 in adult males (n = 101), and its abundance was 5.62±0.41. The prevalence of the mite was 0.36 (n = 101), and its abundance was 3.03±0.58. The abundance of the two species of parasites was not significantly related to the two measures of stone carrying (F < 1.40, df = 1,27, p >.25).
Health status and reproductive success
The experimental treatment did not significantly affect laying date, clutch
size, or seasonal production of fledglings (laying date: F = 3.04, df
= 1,35, p =.09; clutch size: F = 0.06, df = 1,35, p
=.81; no. of fledglings: F = 0.30, df = 1,35, p =.59). The
three measures of health status were not significantly related to the
life-history variables. Laying date, clutch size, and seasonal production of
fledglings were not significantly related to phytohemagglutinin response
(F < 1.08, df = 1,19, p >.31). Similarly, hematocrit
was not significantly related to the three life-history variables (F
< 0.22, df = 1,19, p >.38). Males with a high leukocyte
concentration started breeding later than other males (F = 5.53, df =
1,19, r2 =.19, p =.03; laying date =
(10.18±9.03) + [(1600.54±680.73) x leukocyte
concentration]). There was no significant relationship between leukocyte
concentration and clutch size or number of fledglings (F < 0.69,
df = 1,19, p >.42). The single statistical significance
disappeared after Bonferroni-adjustment for multiple tests of the
hypothesis.
Health status and survival of adult males
Males that survived from 1996 to 1997 or 1998 had a stronger immune
response than males that were not recorded in the study area in 1997 or 1998.
The T-cell response of survivors was 0.366±0.036 mm (n = 8),
but males that were not subsequently resighted had a response that was more
than 25% lower (0.269±0.017 mm (n = 17; t = 2.81, df
= 23, p =.01; Figure
3). The only variable that approached statistical significance was
leukocyte concentration, which tended to be elevated among nonsurvivors
(survivors: 0.011±0.002, n = 8; nonsurvivors:
0.015±0.001, n = 17; t = 1.75, df = 23, p
=.09). None of the other measures of male performance differed significantly
between survivors and nonsurvivors.
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Weather conditions in 1996
The spring of 1996 was characterized by extreme precipitation in our study
area, with 453.1 l/m2 of rainfall in this otherwise extremely dry
area
(Consejería
de Medio Ambiente, 1997). The average for 1990-1995 was only
approximately half of that recorded in 1996 (233.7±25.0
l/m2, minimum 174.6 l/m2, maximum 342 l/m2,
n = 6). The average for the 1990s was slightly lower than that for
the period 1970-1996 (292.0 l/m2, n = 26), and only one
other year had precipitation as high as 1996 (1989, 468 l/m2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Health status and sexual display
Sexual displays have been hypothesized to reveal the health status of males because male phenotypic or genotypic quality in terms of parasite resistance affects the display ability of an individual (Hamilton and Zuk, 1982
;
review in Møller et al.,
1999). Most intraspecific studies have considered morphological
displays such as color or exaggerated traits like elongated feathers or
antlers, but relatively little attention has been paid to behavioral displays
(Møller et al., 1999).
Behavioral displays differ from morphological ones in that the costs of
display are only paid when the individual is displaying, whereas morphological
traits generally are subject to natural selection pressures both during and
outside periods of display. Hence, we might expect behavioral displays to be
less costly than morphological ones.
The present study of stone carrying in the black wheatear concerns an
extreme behavioral display—males carrying heavy stones to cavities
inside caves—and the functional significance of this display is that it
affects the parental investment of their mates
(Moreno et al., 1994;
Soler et al., 1996). This
display is not very costly in terms of metabolism because males carry only an
average of 21 stones per day, each stone weighing an average of 5.8 g. This
equals an increase in energy expenditure of only 1% of daily energy
expenditure (Møller et al.,
1995). Because individual stones (which weigh 3.4-8.2 g for
different males) are heavy relative to the bird (which weighs about 35 g),
males may display their maximum working ability during stone-carrying
displays. Consistent with this expectation, Møller et al.
(1995) calculated that males
experience an increase in power output due to stone carrying of 55kJ/h, or 28
times their basal metabolic rate. This estimate equals an energy output of 400
W/kg, which is close to the upper limit of sustainable power of any muscle
(Goldspink, 1977).
In the present study we found that a measure of immunocompetence was
significantly positively related to the average mass of stones carried by each
male, implying that males carrying very heavy stones were better able to raise
a strong immune response to a novel antigen than males carrying light stones
(Figure 1). The T-cell response
to injection with phytohemagglutinin provides an important measure of a
component of immune function that is directly related to condition of chickens
(Glick et al., 1981,
1983), a measure of
immunocompetence that has a genetic basis in chickens and barn swallows
(Cheng and Lamont, 1988;
Saino et al., 1997b), and this
measure of immune function provides reliable information about long-term
viability of male barn swallows (Saino et
al., 1997a) and black wheatears
(Figure 3). Hence, an aspect of
the stone-carrying display reliably reflected the immunocompetence of male
black wheatears. This finding is consistent with the hypothesis that stone
carrying reveals the maximum working ability of a male, thereby reflecting
male health status. We did not find any correlation between immunocompetence
and total number of stones carried, which is as expected, as total
stone-carrying activity mainly reflects the working effort during the extended
stone-carrying period rather than the maximum stone-carrying ability of an
individual.
Two species of ectoparasites were commonly found in adult black wheatears.
Their abundance was not significantly related to the expression of the
stone-carrying display. This observation adds to an increasing number of
studies showing that sexual displays are much more weakly correlated with the
abundance of parasites than with measures of immune defense
(Møller et al., 1999).
The abundance of different kinds of parasites is generally not positively
correlated for hosts of a given population
(Møller et al., 1999).
Thus, it is unlikely that the abundance of different kinds of parasites of a
host species should, in general, be negatively correlated with the expression
of sexual displays (Møller et al.,
1999). Measures of general antiparasite defenses such as measures
of immunocompetence are likely to provide reliable information about the
ability of males to cope with the currently most detrimental species of
parasites, and their abundance is thus more likely to be related to the
expression of secondary sexual characters
(Møller et al., 1999).
In accordance with this suggestion, the correlation between the expression of
secondary sexual characters and parasite load was on average only -.06 for 52
samples, whereas the correlation between the expression of secondary sexual
characters and measures of immune function was on average.43 in 17 samples
(Møller et al., 1999).
The strong, positive relationship between T-cell response in male black
wheatears and stone carrying and the weak relationship between parasite load
and stone carrying is in agreement with this general trend.
Excessive exercise is known to depress the relative amount of erythrocytes
measured as the hematocrit (reviews in
Saino et al., 1997c,
d). For example, several
studies of animals and humans performing excessive exercise show a reduction
in hematocrit (Birchard, 1997;
Harrison, 1985;
Escribano et al., 1995;
Riera et al., 1983;
Saino et al., 1997c,
d). An experimental study of
the barn swallow demonstrated that tail elongation decreased hematocrit
(Saino et al., 1997c). Male
black wheatears that carried heavy stones had a reduced hematocrit value
compared to males that carried few stones
(Figure 2). Because the work
load of stone-carrying males is the largest ever reported for any muscle, we
can be confident that the stone-carrying display is close to the maximum
amount of work possible. The reduction in hematocrit among males carrying very
heavy stones is consistent with the prediction that increased workload
depresses hematocrit. A negative relationship between stone carrying and
hematocrit was not repeated for the total number of stones carried, which
supports the suggestion that males are displaying maximum working ability
during a short burst rather than working ability during extended periods.
Previous experimental work on the black wheatear revealed that experimental
manipulation of the stone-carrying ability of males by removal of primary
feathers from experimental males caused a significant reduction in the number
and the mass of stones carried
(Møller et al., 1995).
The present study found no evidence for such an effect. This difference in the
effect of wing feather removal on the stone-carrying display in different
years may be explained by extreme among-year variation in environmental
conditions. Hoya de Guadix is a particularly warm and dry area with summer
temperatures exceeding 45°C and sparse precipitation falling in winter.
The warm and dry climate results in a low abundance of invertebrates in most
years. The present study was performed in 1996, which was a year with
considerable rainfall
(Consejería
de Medio Ambiente, 1997). The relationship between invertebrate
abundance and precipitation has not been investigated specifically in the
Guadix area, although the relationship between precipitation and primary
productivity and between primary and secondary productivity are well known
from many terrestrial ecological studies
(Polis et al., 1997, and
references therein). Hence, the vegetation and the abundance of insects may
have been considerably elevated in 1996 compared to 1991 and 1992, when the
first two experiments were made. Hence, we hypothesize that any effects of the
experimental treatment on stone carrying, health status, and reproductive
success may have been compensated by readily available food during this
favorable year.
Immune response and survival of adult males
Parasites are often presumed to play a significant role in determining
fitness of their hosts by competing for resources from maintenance and
reproduction (Price, 1980).
This assumption is founded on observational and experimental studies
demonstrating reduced fitness of heavily infested hosts (reviews in
Lehmann, 1993;
Møller, 1997a). If
parasites impose severe selection pressures on their hosts, this should result
in the evolution of efficient host defenses. The immune system is supposedly
one such efficient host defense (Klein,
1990; Roitt et al., 1995;
Wakelin, 1996). However, there
is little empirical evidence for the efficiency of the immune system. For
example, a recent study of male barn swallows provided one of the first field
demonstrations of a strongly positive correlation among B-cell—mediated
immune response, tail length, and survival prospects to the subsequent year in
this long distance transequatorial migratory bird
(Saino et al., 1997a). T-cell
response to injections with phytohemagglutinin is also positively correlated
with tail length in male barn swallows (S. Merino, personal
communication).
In the present study of the black wheatear, we found that adult males
recorded in the study area in a subsequent year had a significantly greater
T-cell response than males that were not resighted in subsequent years
(Figure 3). The increased
concentration of leukocytes in nonsurvivors is also consistent with the
interpretation that survivorship was related to health status
(Dein, 1986). None of the other
measures of performance by adult male black wheatears differed significantly
between survivors and nonsurvivors. Hence, it seems likely that a strong
immune response by male black wheatears provides an advantage in terms of
survival prospects. Females may benefit from mating with immunocompetent males
because such males may provide more resources for their offspring
(Moreno et al., 1994) and
because immunocompetent males may provide genetic benefits in terms of
parasite resistance to their offspring
(Hamilton and Zuk, 1982).
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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J. Fernandez provided invaluable help in the field. M.S., M.M.V., and J.M.M. were supported by a grant from the Spanish DGICYT (project PB91-0084-CO3-02). A.P.M. was supported by a grant from the Danish Natural Science Research Council and an ATIPE BLANCHE from the CNRS.
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REFERENCES |
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