Behavioral Ecology Vol. 13 No. 3: 401-407
© 2002 International Society for Behavioral Ecology
Differential effects of a parasite on ornamental structures based on melanins and carotenoids
Department of Zoology, University of Bern, CH-3032 Hinterkappelen, Switzerland
Address correspondence to P.S. Fitze, who is now at Laboratoire d'écologie, Université Pierre et Marie Curie, 7 Quai st Bernard, 75005 Paris, France. E-mail: patrick.fitze{at}esh.unibe.ch .
Received 24 January 2001; revised 10 July 2001; accepted 10 August 2001.
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ABSTRACT |
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Models of sexual selection predict that ornamental coloration should be affected by parasites in order to serve as honest signals. Animals are commonly infested by a range of parasite species and often simultaneously display several ornaments. Thus the specific effect of a given parasite on ornaments is important for the understanding of the signal. Here we investigate experimentally the effect of an ectoparasite on carotenoid- and melanin-based traits in breeding great tits Parus major. In the experiment, nests were either infested with hen fleas, Ceratophyllus gallinae, or kept free of parasites. The color of the two traits and the size of the melanin-based breast stripe were assessed both in the year of experimental parasite infestation and during the following breeding season, after the annual molt. The size of the breast stripe of infested males and females significantly decreased, but increased significantly in uninfested males and females. The blackness of the breast stripe and the carotenoid-based plumage coloration was unaffected. Our experiment demonstrates that the size of the melanin-based breast stripe of adults depends on parasite infestation, suggesting that the trait can serve as an honest signal of previous parasite exposure.
Key words: carotenoids, Ceratophyllus gallinae, great tits, hen fleas, honest signaling, melanins, ornaments, parasites, Parus major.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The evolution of conspicuous signals is a pathway for resolving conflicts of interest in an economical manner. Instead of solving a conflict by costly fighting, contestants may assess each other's quality by visual signals that indicate the bearer's quality honestly. Honesty is maintained by the cost of producing or carrying the signal and by the fact that signals are more costly to poorer phenotypes (e.g., Zahavi, 1975
,
1977;
Grafen, 1990). Parasites are
expected to influence signal expression by living off their host's resources
and by influencing the trade-offs for resource allocation among various
fitness components within hosts. Milinski and Bakker
(1990) have shown both that an
endoparasite Ichthyophthirius multifiliis reduces the intensity of a
carotenoid-based red signal in male sticklebacks Gasterosteus
aculeatus and that females select mates on the basis of this trait.
Similarly, male house finches, Carpodacus mexicanus, experimentally
infected with coccidiosis grow a less red plumage and are less often selected
by females (Hill, 1990;
Hill and Brawner, 1998). In
contrast to carotenoid-based signals, there is no experimental evidence yet
for parasites to affect melanin-based signals. Møller et al.
(1996) suggested that
ectoparasite load reduces the size of the melanin-based breast badge in house
sparrows, whereas in house finches Hill and Brawner
(1998) did not find a
correlation between experimental coccidial infection and melanin-based plumage
colors.
Great tits (Parus major) show both a carotenoid-based yellow
breast plumage and a melanin-based black breast stripe. Melanins are
synthesized by the birds before deposition in the melanophores of the feathers
(Brush, 1978). This process
depends on body condition during molt
(Veiga and Puerta, 1996).
Correlational evidence suggests that female great tits assess future mates by
the size of the breast stripe (Norris,
1990). In intrasexual interactions birds with experimentally
enlarged breast stripes are more dominant and gain more conflicts
(Järvi et al., 1987).
Carotenoids, in contrast to melanins, cannot be synthesized by birds and thus
have to be ingested with food. It has been suggested that restricted
availability of carotenoid-containing food
(Hill, 1992;
Hill and Montgomerie, 1994;
Slagsvold and Lifjeld, 1985),
low body condition of the individual bird
(Hill and Montgomerie, 1994),
and detrimental effects of the carotenoids on the organism
(Olson and Owens, 1998) may
limit the expression of the carotenoid-based plumage coloration. In great
tits, correlational evidence suggests that brighter males signal low parasite
level and thus better quality (Dufva and
Allander, 1995; Hõrak et al., 2000).
In summary, experimental evidence that parasites affect melanin- and
carotenoid-based signals is scant. Here we investigate, by experimental
infestation, the influence of a hematophageous ectoparasite (Ceratophyllus
gallinae) that affects reproductive success and reproductive effort
(e.g., Christe et al., 1996;
Richner et al., 1993) on the expression of a melanin- and a carotenoid-based
plumage trait in great tits (P. major). We assessed the effect of
flea infestation during reproduction on the plumage coloration of the
subsequent year and predicted a change in signal size or intensity as a
function of the applied ectoparasite load. Whether ectoparasites change their
hosts' plumage coloration directly or cause a change indirectly by imposing
higher reproductive effort requires further work beyond the present study.
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MATERIALS AND METHODS |
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Experimental setup
The experiment was performed on a great tit population breeding in nest-boxes in the Forst, a forest near Bern, Switzerland (46°54' N, 7°17' E to 46°57' N, 7°21' E). On a first set of birds, the parasite load was manipulated in 1997, and the change in plumage color from 1997 to 1998 was assessed (i.e., after the annual molt). On a second set the same procedure was used from 1998 to 1999. We eliminated nest-based ectoparasites by subjecting all nests to a heat treatment inside a microwave oven on the day the birds laid their second egg, following Heeb et al. (1996
). Nests were then
alternately assigned to a group left free of parasites or to a group infested
with 40 adult hen fleas Ceratophyllus gallinae obtained from
naturally infested nests of the same forest. There was no significant
difference in laying date between nests allocated to the two experimental
treatments (Student's t test: t = 0.048, p =.962
N = 74). In 1997, 14 nests were experimentally infested while 15
nests were kept free of parasites, and in 1998, 22 nests were infested and 23
were kept parasite-free. Thirteen days after hatching, parents were caught in
the nest-box, and a digital photograph of the breast plumage was taken. The
year following parasite manipulation, all breeding adults were captured again
and photographed. For each adult we measured body mass to the nearest 0.01 g
using an electronic scale (Sartorius) and measured the length of the
metatarsus to the nearest 0.1 mm using slide calipers
(Svensson, 1992). Age was
determined by the presence or absence of molt limits
(Jenni and Winkler, 1994).
Breeding birds were classified as either first-year birds (molt limits
present) or birds older than one year (molt limits absent). Fifteen days after
hatching each nestling was weighed and the length of the metatarsus measured
(Svensson, 1992).
Quantifying the carotenoid-based yellow plumage coloration
Great tits were placed in a box covered with a photographic filter lens
(Hoya UV-filter, 59 x 74 mm), including a thin cardboard at one end to
protect the bird's eyes from the flash. This box was placed in a standard
position inside a larger opaque camera box. Two flashes (Nikon SB26) were
mounted at an angle of 13° to the optical axis, 10 cm below and 20 cm
beside the front lens of the camera (Nikon E2 with a 105 mm f/2.8 Nikkor
objective) measuring the red, green, and blue values (RGB) of the color. The
distance between the feathers and the front lens was fixed to 50 cm. The
settings of the camera and flashes were always identical, and thus all
photographs received a standard light exposure. Standard white chips (Kodak
Color Control Patches with R = 255, G = 255, B = 255) were fixed to each side
of the filter for calibration of the equipment during color analysis.
The photographs were imported into the Adobe Photoshop program, and a
virtual second layer, holding 10 square measurement areas of 400 pixels each,
was placed over the photograph. Then the program calculated the mean RGB
values of each square. The squares falling on the black breast stripe were not
used for the quantification of the yellow coloration. There was no correlation
between the color values and the number of squares analyzed in the 52
recaptured birds (R: r = -0.14, p =.27; G: r =
-0.16, p =.21; B: r =.121, p =.34), demonstrating
that the exclusion of squares did not bias the results. Both the photographing
and the analyses were done blindly with respect to origin and condition of the
birds. Mean RGB values per bird were converted to hue-saturation-brightness
(HSB) values by the algorithm described in Foley and Van Dam
(1984). The variation in light
exposure, as assessed from the measurements of the white reference chips, was
small (R: 254 ± 1, G: 254 ± 1, B: 243 ± 3; mean ±
SD; N = 131), and therefore no correction of the color values
measured on the plumage was required.
The measures of color used here do not correspond exactly to the colors
perceived by birds. Also, birds possess biologically functional receptors for
UV light (e.g., Cuthill et al.,
2000), to which our equipment was insensitive. However, as also
remarked by Bennett et al.
(1994: 855), "for
heuristic purposes, it may be useful to express color patterns in subjective
terms that humans can readily understand."
Quantifying the melanin-based black breast stripe
The black area of the breast stripe was measured with the NIH Image program
(developed at the U.S. National Institutes of Health and available on the
Internet at
http://rsb.info.nih.gov/nih-image/
) after calibration of the digital photograph using a standard distance.
Pixels with gray values between 150 and 254 (i.e., the ones appearing as black
on the digital photograph) were included for measuring the area of the black
breast stripe. In males the breast stripe joins the base of the legs
(Gosler, 1993), and therefore
the area between the base of the neck and the base of the legs was measured.
Compared to males, in females the breast stripe is much reduced and usually
does not reach the base of the legs
(Gosler, 1993). To avoid
measuring plumage parts not belonging to the breast stripe, the area between
the base of the neck and the end of the breast stripe was measured. The five
females in the sample with a breast stripe reaching the base of the legs were
analyzed like the males. Skeletal size and body condition, defined as the
residuals of the regression of body mass on tarsus, of adult great tits
remained constant from one year to the other (paired t test: male
tarsus length t = -0.038, n = 22, p =.97; male body
condition t < -0.001, n = 22; p = 1; female
tarsus length t = -1.32, n = 30, p = 2; female body
condition t < -0.001, n = 30, p = 1). Therefore,
differences in male breast stripe area is not due to different skeletal size
or different chest-diameters between years and thus must be the result of
differences in mean width. In females, area differences might be due to
changes in mean width and length of the breast stripe. The blackness of the
breast stripe was calculated by averaging the gray values of the pixels
belonging to the breast stripe. Repeatability
(Lessells and Boag, 1987)
among 14 adult birds (seven females and seven males) measured twice during the
same capture occasion in winter 1997 was highly significant (breast stripe
area: r [repeatability] = 0.923, F1,12 = 68.84,
p <.001; breast stripe blackness: r =.9925,
F1,12 = 242.74, p <.001). Similarly,
repeatabilities of the carotenoid-based measurements were highly significant
(H: r =.80, F1,12 = 9.11, p =.01; S:
r =.842, F1,12 = 11.618, p <.01; B:
r =.824, F1,12 = 10.374, p <.01),
indicating that the measuring of coloration and area by our photographic
system is well standardized.
Mortality and recaptures
Seven broods in 1997 (four infested, three uninfested) and nine broods in
1998 (four infested, five uninfested) failed before the nestlings fledged.
Brood failures were not influenced by the treatment (chi-square test:
2 = 0.026, N = 74, p >.5). Of the 22
successful nests in 1997, 13 males (eight infested, five uninfested) and 17
females (nine infested, eight uninfested) were recaptured during the
subsequent breeding season. Of the 36 successful nests in 1998, 15 males (five
infested, 10 uninfested) and 18 females (seven infested, 11 uninfested) were
recaptured. Neither the treatment (
D = 0.02, N = 116,
p =.88) nor the set of birds manipulated for parasite exposure in
both 1997 or 1998 (hereafter referred to "year of experimental
infestation") influenced the recapture rate significantly
(D = 2.33, N = 116, p =.13). Therefore
differences between treatment groups are not due to a treatment-dependent
recapture bias. Females were recaptured more often (57.6%) than males (38.6%;
D = 4.42, N = 116, p =.04). The proportion
of recaptured adults was analyzed using logistic regression analysis with
binomial errors and a logit link, taking recapture as the dependent binomial
variable. The statistical significance of a recapture bias in relation to the
independent variables was assessed from the change in deviance (denoted as
D) when a variable was excluded first from (or included last
into) the model (Crawley,
1993). The change in deviance is asymptotically distributed as
2 with corresponding degrees of freedom
(Crawley, 1993). The scale was
estimated at a value of 1.38. Statistical analysis of the recapture rate was
carried out using the statistical package GLM Stat
(Beath, 1997).
With respect to initial plumage characteristics, recaptured males and females were not significantly different from birds not recaptured (Student's t tests: male hue: t1,65 = 0.31, p =.76; male saturation: t1,65 = -1.34, p =.19; male brightness: t1,65 = -0.41, p =.68; breast stripe area: t1,65 = 0.43, p =.67; male breast stripe blackness: t1,65 = -0.50, p =.62; female hue: t1,63 = -2.45, p =.02; female saturation: t1,63 = -1.62, p =.11; female brightness: t1,63 = -0.25, p =.81; female breast stripe area: t1,63 = 0.48, p =.64; female breast stripe blackness: t1,63 = -1.56; p =.13). Because there were no differences in nest failures and recapture rates between treatment groups and recaptured birds did originally not differ significantly in the measured plumage traits from birds not recaptured the subsequent year, birds used in our analysis appear to represent a random sample of the original sample.
Statistical analysis
The overall plumage coloration was evaluated using the first principle
component (PC1) from a Principal Components Analysis including hue,
saturation, and brightness. PC1 explained 55.9% of the total variance in male
and 50.7% in female plumage coloration, respectively. A repeated-measures
ANOVA with breast coloration in the first and in the subsequent year as
repeated measures, parasites, year of experimental infestation, and age as
factors and body condition as a covariate (see
Table 2), was conducted using
the JMP statistical package (Sall and
Lehman, 1996). In addition to these univariate analyses, we used
multivariate analyses to test the pure variation of a single color parameter
without the influence of the intercorrelated color parameters. Therefore each
color parameter was corrected for both intercorrelated color parameters (e.g.,
hue for saturation and brightness) by taking the residuals of a model with one
color parameter as the dependent variable and the two others as covariates,
before analyzing the data with a repeated-measures ANOVA (see Appendix Table
B). Because all between-subject factors and the within-subject interactions of
age and body condition were not significant (p >.1) in both
analyses, only the within-subject analyses with the factors parasites and year
of experimental infestation are presented in
Table 2 and Appendix Table B,
with the exception of the significant effect of year of experimental
infestation in hue, as mentioned in the results section.
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Blackness of the breast stripe was positively correlated with the breast
stripe area in both males (F1,64 = 6.62, p =.012) and
females (F1,58 = 7.93, p =.007). Therefore, in
addition to the univariate repeated-measures ANOVAs presented in
Table 1, a multivariate
analysis was conducted. Each parameter was first corrected for the
intercorrelated parameter (e.g., breast stripe area for blackness) by taking
the residuals of a correlation with one parameter as the dependent variable
and the other one as the independent variable. Residuals were then used for
the repeated-measures ANOVA (see Appendix Table A). Experimental treatment,
year of experimental infestation, and age were included as factors and body
condition as a covariate into the model. Because the factors age and year and
the covariate body condition and their interactions were not significant
(p >.1), they are not shown in
Table 1 and Appendix Table A.
Parasite load of six males and five females was manipulated in both years 1997
and 1998, and these birds were captured in each of the three breeding seasons.
To avoid pseudoreplication we included the 11 individuals only in the data set
of the first year of experimental infestation. For the analyses we used the
JMP statistical package (Sall and Lehman,
1996). Normality was evaluated by a Lilliefors test
(Wilkinson, 1989).
Significance levels are two-tailed with a.05 significance level. Bonferroni
corrections were applied to adjust the p values for the increased
probability of obtaining statistical significance from multiple testing
(Rice, 1989). Means ± 1
SE are given.
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RESULTS |
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Melanin-based plumage coloration
Male breast stripes covered an average area of 682 ± 21.5 mm2 in the first year and 676 ± 25.6 mm2 in the subsequent year. In females the breast stripes covered an average area of 351 ± 15.2 mm2 in the first year and 346 ± 14.4 mm2 in the subsequent year. The sexual size difference of the breast stripe was highly significant (t = -13.18, n = 52, p <.0001).
Parasite exposure during breeding significantly affected the area of the breast stripe the subsequent year in both males and females (Figure 1, Table 1; area change x parasites). Breast stripes of parasitized males decreased by 49 ± 28.0 mm2 (7.2%), and of parasitized females by 57 ± 19.2 mm2 (16.2%), while parasite-free males increased their breast stripes by 55 ± 27.9 mm2 (8.1%), and parasite-free females by 42 ± 18.8 mm2 (12.0%). Neither the year of experimental infestation nor the age of the birds explained a significant part of the variation of the area change in males and females. Similarly, breast stripe area was not correlated with body condition. Parasite exposure had no significant effect on the blackness of the breast stripe in both males and females (Table 1; blackness change x parasites). The multivariate approach (Appendix Table A) led to the same results, suggesting the lack of an underlying trade-off between breast stripe area and blackness.
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Carotenoid-based plumage coloration
Carotenoid-based plumage color was not affected by parasites in either
males or females (Table 2;
color change x parasites, p >.05). The year of experimental
infestation explained a significant proportion of the variation in hue (color
change-independent variation [between subjects, not shown in
table 2]: males:
F1,15 = 11.085, p =.005; females:
F1,22 = 13.146, p =.002) but not in overall
plumage coloration, saturation, and brightness (p >.1). In males,
the color change (Table 2;
color change x year of experimental infestation) was not significantly
different between the two data sets in any of the four color variables,
whereas in females the change in overall plumage coloration and brightness was
significantly affected by the year of experimental infestation
(Table 2; color change x
year of experimental infestation). The multivariate approach (Appendix Table
B) led to similar results, except in male brightness being significantly
different between males of different ages (color change-independent between
subjects factor [not presented in Appendix Table B]) and in the color change
of female hue, being significantly different between years (Appendix Table
B).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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This study shows experimentally that ectoparasites can induce a change in the size of a melanin-based plumage trait that had been suggested to function as an honest signal during processes of inter-and intrasexual selection in male great tits. It demonstrates that melanin-based traits of adults are dependent on the parasite load during reproduction. The blackness of the breast stripe was not significantly modified. The multivariate approach led to the same results, suggesting that there is no underlying trade-off between signal size and signal intensity. It is interesting that the effect of parasites on signal size was also found in females. This result is not surprising considering the study of Wilson (1992
), which suggested a
correlation between the size of the female breast stripe and social dominance.
Thus, in both male and female great tits, the size of the breast stripe is a
potential signal to conspecifics for individual parasite load and/or
resistance against this ectoparasite, as had been suggested in barn owls for
another melanin-based trait (Roulin et
al., 2001).
The mechanism leading to reduced breast stripe size cannot be revealed by
our experiment and needs further investigation. Both a direct mechanism
through blood sucking and/or disease transmission by the fleas and an indirect
effect due to flea-induced higher reproductive investment
(Christe et al., 1996;
Richner and Tripet, 1999) are
conceivable.
In the house sparrow (Passer domesticus), nutritional constraints
affect body condition and influence the expression of badge size
(Veiga and Puerta, 1996),
whereas in our study body condition alone, as measured 13 days after hatching,
did not explain a significant proportion of the total variance in breast
stripe area. Although in house sparrows the body condition was directly
manipulated via access to food, we did not manipulate body condition directly.
It might be for this reason that body condition affected breast stripe area in
house sparrows, but not in our study where body condition was merely a
correlational variable. Moreover, it is conceivable that body condition later
in the year, when melanins are deposited during molt, is only poorly
correlated with the body condition measured during parasite exposure.
Therefore only body condition measured and manipulated during molt could
reveal the relationship with breast stripe area. In contrast to our study, a
melanin-based trait in another species, the black tail coloration of house
finches (Carpodacus mexicanus), was unaffected by coccidial infection
(Hill and Brawner, 1998). It
has been suggested that the honesty of melanin-based signals is maintained by
the costs arising from social dominance interaction
(Møller, 1987;
Veiga, 1993) and not by the
costs of the melanin synthesis per se
(Gray, 1996). It has further
been suggested that the black tail of house finches is not used in conspecific
signaling (Hill and Brawner,
1998), implying that tail color has not been selected to indicate
parasite exposure.
In contrast to previous studies (Hill
and Brawner, 1998; Milinski
and Bakker, 1990), we did not find an effect of the parasites on
carotenoid-based coloration of the plumage. There are at least four not
mutually exclusive explanations. First, parasites may have affected the
coloration exclusively in the UV range of the visual spectra not measured
here. Second, both of the above-mentioned studies used endoparasites. Coccidia
infections, as used in the study on house finches
(Hill and Brawner, 1998),
inhibit the uptake of nutrients in the gut, including carotenoids
(Augustine and Ruff, 1983;
Ruff et al., 1974).
Ichthyopthirius multifilis, as used in the stickleback experiments,
feeds on cells and blood below the epidermis
(Schäperclaus, 1990) and
reduces the condition of the fish
(Milinski and Bakker, 1990),
whereas hen fleas do not directly inhibit the uptake of nutrients, nor do they
feed on body cells. This might explain the absence of negative effects of hen
fleas on the carotenoid-based plumage coloration. Third, the chemical pathways
of the carotenoid deposition in house finches and sticklebacks are different
from those in great tits. The red coloration of house finches and sticklebacks
originates from carotenoids being modified before deposition
(Brush, 1990;
Wedekind et al., 1998),
whereas the yellow carotenoid-based coloration of the great tits originates
from carotenoids being deposited unmodified in the feathers
(Partalli et al., 1987). If
carotenoid modification is costly, it is conceivable that the altered energy
balance due to parasites reduces the quantity of energy available for the
chemical processes before carotenoid deposition. Therefore, differences in red
but not yellow coloration are predicted. Finally, in contrast to house
finches, this carotenoid-based trait may not be used in conspecific signaling
in great tits, implying that it has not been selected to indicate parasite
exposure.
Slagsvold and Lifjeld
(1985) found an effect of
habitat type on yellow plumage coloration. The significant color change of
individuals (Table 2; color
change, p <.01) suggests that this effect may also arise due to
varying carotenoid availability between years.
The present study demonstrates that ectoparasite exposure reduces the
expression of a melanin-based signal, suggesting that the size of the breast
stripe can be a signal of previous parasite exposure. Further work should
focus on whether the carotenoid-based breast coloration of great tits is
signaling the presence of another parasite species than hen fleas, as
suggested by two recent studies (Dufva and
Allander, 1995; Hõrak et al., 2000). Additionally it would
be important to investigate whether a signal (melanin- or carotenoid-based)
reflects the presence of a single parasite species only, or whether different
parasite species affect the same signal similarly, revealing the specificity
of such signals.
,
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ACKNOWLEDGEMENTS |
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We thank K. Büchler, B. Holzer, A. Jacot, V. Saladin, F. Tripet, and B. Tschirren for their help in catching adult birds, and F. Balloux, A. Roulin, and two anonymous referees for comments on the manuscript. The work was financially supported by the Swiss National Science Foundation (grants 31-43570.95 and 31-53956.98 to H. Richner). The experiment was conducted under a license provided by the Office of Agriculture of the Canton Berne.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Augustine PC, Ruff MD, 1983. Changes in carotenoid and vitamin A levels in young turkeys infected with Eimeria meleagrimitis or E. adenoiedes. Avian Dis 27: 963-971.[Web of Science][Medline]
Beath K, 1997. GLM Stat, version 5.2.1. Sydney.
http://www.ozemail.com.au/
kjbeath/glmstat.html
.
Bennett ATD, Cuthill IC, Norris KJ, 1994. Sexual selection and the mismeasure of color. Am Nat 144: 848-860.[Web of Science]
Brush AH, 1978. Avian pigmentation. In: Chemical zoology (Brush AH, ed). New York: Academic Press; 141-164.
Brush AH, 1990. Metabolism of carotenoid pigments in birds. FASEB J 4: 2969-2977.[Abstract]
Christe P, Richner H, Oppliger A, 1996. Begging, food
provisioning, and nestling competition in great tit broods infested with
ectoparasites. Behav Ecol 7:
127-131.
Crawley M, 1993. GLIM for ecologists. Oxford: Blackwell Scientific.
Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S, 2000. Ultraviolet vision in birds. Adv Study Behav 29: 159-214.
Dufva R, Allander K, 1995. Intraspecific variation in plumage coloration reflects immune response in great tits (Parus major) males. Funct Ecol 9: 785-789.
Foley JD, Van Dam A, 1984. Intensity and color. In: Fundamentals of interactive computer graphics. Philippines: Addison-Wesley; 593-622.
Gosler S, 1993. The great tit. London: Hamlyn Limited.
Grafen A, 1990. Sexual selection unhandicapped by the Fisher process. J Theor Biol 144: 473-516.[Web of Science][Medline]
Gray DA, 1996. Carotenoids and sexual dichromatism in North American passerine birds. Am Nat 148: 453-480.[Web of Science]
Heeb P, Werner I, Richner H, Kölliker M, 1996. Horizontal transmission and reproductive rates of hen fleas in great tit nests. J Anim Ecol 65: 474-484.
Hill GE, 1990. Female house finches prefer colourful males: sexual selection for a condition-dependent trait. Anim Behav 40: 563-572.
Hill GE, 1992. Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109: 1-12.
Hill GE, Brawner WR III, 1998. Melanin-based plumage
coloration in the house finch is unaffected by coccidial infection.
Proc R Soc Lond B 265:
1105-1109.
Hill GE, Montgomerie R, 1994. Plumage colour signals
nutritional condition in the house finch. Proc R Soc Lond B
258: 47-52.
Hõrak P, Ots I, Vellau H, Spottiswoode C, Møller AP, 2001. Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126: 166-173.[Web of Science]
Järvi T, Walsø Ø, Bakken M, 1987. Status signalling by Parus major: an experiment in deception. Ethology 76: 334-342.[Web of Science]
Jenni L, Winkler R, 1994. Moult and ageing of European passerines. London: Academic Press.
Lessells CM, Boag PT, 1987. Unrepeatable repeatabilites: a common mistake. Auk 104: 116-121.[Web of Science]
Milinski M, Bakker TCM, 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344: 330-333.
Møller AP, 1987. Social control of deception among status signalling house sparrows Passer domesticus. Behav Ecol Sociobiol 20: 307-311.[Web of Science]
Møller AP, Kimball RT, Erritzoe J, 1996. Sexual ornamentation, condition, and immune defence in the house sparrow Passer domesticus. Behav Ecol Sociobiol 39: 317-322.[Web of Science]
Norris KJ, 1990. Female choice and the evolution of conspicuous plumage coloration of monogamous male great tits. Behav Ecol Sociobiol 26: 129-138.
Olson VA, Owens IPF, 1998. Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13: 510-514.
Partalli V, Liaaen-Jensen S, Slagsvold T, Lifjeld JT, 1987. Carotenoids in food chain studies—II. The food chain of Parus spp. monitored by carotenoid analysis. Comp Biochem Physiol B 82: 767-772.
Rice WR, 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.[Web of Science]
Richner H, Tripet F, 1999. Ectoparasitism and the trade-off between current and future reproduction. Oikos 86: 535-538.[Web of Science]
Roulin A, Riols C, Dijkstra C, Ducrest A, 2001. Female
plumage spottiness and parasite resistance in the barn owl (Tyto
alba). Behav Ecol 12:
103-110.
Ruff MD, Reid WM, Johnson J, 1974. Lowered blood carotenoid levels in chickens infected with coccidia. Poult Sci 53: 1801-1809.[Web of Science][Medline]
Sall J, Lehman A, 1996. JMP start statistics. New York: Duxbury Press.
Schäperclaus W, 1990. Fischkrankheiten. Berlin: Akademie-Verlag.
Slagsvold T, Lifjeld JT, 1985. Variation in plumage colour of the great tit Parus major in relation to habitat, season and food. J Zool 206: 321-328.[Web of Science]
Svensson L, 1992. Identification guide to European passerines. Stockholm, Sweden: Heraclio Fournier SA.
Veiga JP, 1993. Badge size, phenotypic quality, and reproductive success in the house sparrow—a study on honest advertisement. Evolution 47: 1161-1170.[Web of Science]
Veiga JP, Puerta M, 1996. Nutritional constraints
determine the expression of a sexual trait in the house sparrow, Passer
domesticus. Proc R Soc Lond B 263:
229-234.
Wedekind C, Meyer P, Frischknecht M, Niggli UA, Pfander H, 1998. Different carotenoids and potential information content of red coloration of male three-spined stickleback. J Chem Ecol 24: 787-800.[Web of Science]
Wilkinson DP, 1989. SYSTAT: the system for statistics. Evanston, Illinois: Systat, Inc.
Wilson JD, 1992. A re-assessment of the significance of status signalling in populations of wild great tits, Parus major. Anim Behav 43: 999-1009.
Zahavi A, 1975. Mate selection—a selection for a handicap. J Theor Biol 53: 205-214.[Web of Science][Medline]
Zahavi A, 1977. The cost of honesty (further remarks on the handicap principle). J Theor Biol 67: 603-605.[Web of Science][Medline]
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