Behavioral Ecology Vol. 12 No. 1: 93-97
© 2001 International Society for Behavioral Ecology
Humoral immunocompetence correlates with date of egg-laying and reflects work load in female tree swallows
a Department of Neurobiology and Behavior, Seeley G. Mudd Hall, Cornell University, Ithaca, NY 14853-2702, USA b Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, NY 14853-2702, USA
Address correspondence to D. Hasselquist, who is now at the Department of Animal Ecology, Lund University, Ecology Building, 223 62 Lund, Sweden. E-mail: dennis.hasselquist{at}zooekol.lu.se .
Received 4 July 1999; revised 21 June 2000; accepted 5 July 2000.
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ABSTRACT |
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Because quality differences between individuals affect fitness, much research has attempted, with limited success, to relate physiological condition (e.g., body reserves), to differences in life history between individuals. Recently, it has been suggested that immunocompetence may reflect condition, and it thus may mediate variation in individual quality and reproductive performance and, ultimately, fitness. We measured humoral immunocompetence (HIC) by immunizing female tree swallows with a harmless antigen and measured the specific antibody responses in a novel enzyme-linked immunosorbent assay developed for passerine birds. HIC was strongly correlated with egg-laying date, an important determinant of reproductive success in female tree swallows. We also investigated the effect of increased workload on HIC by manipulating female flight costs by clipping flight feathers. Clipped females had lower HIC than nonclipped females. These data suggest that HIC is a measure that may reflect phenotypic quality and also appears to be sensitive to increased workload in female tree swallows.
Key words: ELISA, humoral immunocompetence, life history, phenotypic quality, reproductive effort, Tachycineta bicolor, timing of breeding.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSELISARESULTSDISCUSSIONREFERENCES |
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Considerable attention has been paid to the possibility of differences in physiological condition affecting life-history variation among individuals (Kirkpatrick et al., 1990
;
Price et al., 1988;
Rowe et al., 1994). For
example, female birds differ in the somatic stores of resources amassed before
reproduction, though evidence suggests that this factor does not predict any
life-history trait in passerines (Pahl et
al., 1997; Perrins,
1996; Winkler and Allen,
1996). Several avian studies have found that the prevalence of
blood parasites increases when clutch sizes are experimentally enlarged
(Allander, 1997;
Norris et al., 1994;
Richner et al., 1995) and that
the intensity of blood parasites can be correlated with measures of health and
individual quality (e.g., Atkinson and van
Riper III, 1991; Davidar and
Morton, 1993; Møller et
al., 1990). In barn swallows, Hirundo rustica,
unmanipulated males showed a significantly higher increase in total
gammaglobulin concentrations in the blood after an injection of sheep red
blood cells than did males with experimentally elongated tail streamers
(Saino and Møller,
1996). These results suggest that an individual's workload may
affect its immune function and that immune function may be related to other
aspects of phenotypic quality.
To investigate whether differences in immune function—that is,
immunocompetence (Lochmiller,
1995; Siva-Johty,
1995) —might be used as a measure of phenotypic quality, we
studied the relationship between humoral immunocompetence (HIC) and egg-laying
date of female tree swallows, Tachycineta bicolor. Laying date has
been identified as an important predictor of annual reproductive output in
this species (Stutchbury and Robertson,
1988; Winkler and Allen,
1996). To investigate whether HIC is affected by increased
workload, we manipulated flight costs by clipping feathers. Tree swallows are
exclusively aerial feeders, and during nestling provisioning they spend most
of their time on the wing capturing small insects, with each parent bringing
food to the nestlings on average 10-14 times per hour
(Winkler and Allen, 1995).
Feather clipping increases flight costs, and hence increases workload, which
may have a negative impact on HIC
(Deerenberg et al., 1997;
Hoffman-Goetz and Pedersen,
1994; Nordling et al.,
1998;
R
berg et
al., 1998).
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METHODS |
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General
We studied individually marked female tree swallows breeding in nest-boxes near Ithaca, New York, USA. We captured 36 females on the estimated penultimate day of incubation and aged them by plumage (Hussell, 1983
;
Robertson et al., 1992).
Twelve of these females were handicapped by clipping off every even-numbered
primary feather at its base (i.e., four primaries on each side). In a previous
study of Ithaca tree swallows where this manipulation was performed before egg
laying, it resulted in increased mass loss and lower nest visitation rate in
clipped females but had no significant effects on total (male and female) nest
visitation rate, chick mass, or fledging success
(Winkler and Allen, 1995).
Hence, feather-clipping is an appropriate manipulation of workload in this
species. The proportions of females clipped were balanced among groups of
early (17-21 May), average (22-24 May), and late (25-29 May) clutch initiation
dates. Because female age normally predicts some of the laying-date variation
in tree swallows (Stutchbury and
Robertson, 1988; Winkler and
Allen, 1996), we also balanced the proportions of clipped females
between first-year and older breeders. The number of chicks in the nest-box at
day 9 after hatching was our measure of brood size during parental
provisioning. When investigating the effect of clipping on HIC, we excluded
two broods containing only one young each. These broods had suffered from
severe brood reduction (see Winkler,
1991), indicating that the provisioning by either the female or
the male in these pairs had not been normal.
Antigen injections
To measure humoral immunocompetence (HIC), we elicited an antibody response
in the birds by immunizing them with a harmless, immunogenic protein antigen,
keyhole limpet hemocyanin (KLH), to which tree swallows had never been exposed
(see also Klein and Nelson,
1997). We emulsified 1 mg KLH/ml sterile H2O with 1 ml
of incomplete Freund's adjuvant (Sigma Chemical Co., St. Louis, Missouri,
USA). A total volume of 50 µl of this emulsion, containing 25 µg KLH,
was injected into the breast muscle of each immunized bird when it was first
captured (i.e., on the penultimate day of incubation). Blood samples (20-70
µl) were taken just before immunization and 10 days thereafter, when
females were feeding 8-day-old nestlings. We used the preimmunization sample
for measuring the background value for nonspecific binding of antibodies
against the antigen and used the postimmunization sample taken 10 days after
injection for measuring the level of antibody production against the specific
antigen (i.e., our measure of HIC). Serum was separated by centrifugation and
stored at -50°C until it was analyzed. In red-winged blackbirds,
Agelaius phoeniceus, a first immunization with KLH resulted in a
primary immune response that peaked around 12 days after injection
(Hasselquist et al., 1999).
Our aim when injecting the birds with a harmless antigen was to induce
measurable levels of humoral immune responses without causing other
significant physiological effects. In a field study on red-winged blackbirds,
males injected with KLH behaved normally, and there were no negative effects
on territory maintenance or mating and reproductive success (Hasselquist D,
unpublished data). Moreover, in the blue tit, Parus caeruleus, a
small passerine bird, immunizations with harmless antigens (diptheria and
tetanus vaccine) did not result in any significant increase in resting
metabolic rate during either primary or secondary antibody responses
(Svensson et al., 1998).
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ELISA |
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As a measure of HIC, we analyzed the level of anti-KLH antibodies in the birds' sera using an enzyme-linked immunosorbent assay (ELISA; Exon and Talcott, 1995
). We
adopted the same ELISA setup previously developed for red-winged blackbirds
(see Hasselquist et al., 1999),
and this assay proved to work with high accuracy for tree swallows. This ELISA
method provides sensitive measures of the amount of passerine antibodies that
specifically bind to a certain antigen (in this case KLH).
Here we briefly describe the ELISA we used for tree swallows (for more
details, see Hasselquist et al.,
1999). ELISA plates (96-well) were first coated with KLH. To these
plates we then added diluted pre- and postimmunization serum samples from tree
swallows (see below), after which plates were incubated over night at 4°C.
Plates were then washed (in phosphate-buffered saline and Tween 20), and as a
result only tree swallow antibodies that specifically had bound to the KLH
fixed to the sides of the wells remained on the ELISA plate. To each well, we
then added a secondary rabbit anti—redwinged-blackbird-immunoglobulin
antiserum which we had produced by immunizing rabbits with purified red-winged
blackbird IgM and IgG (this rabbit antiserum binds to immunoglobulins of
several species of passerine birds but not to chicken; Hasselquist D,
unpublished data). After a second incubation and wash, a commercial
peroxidase-labeled goat anti-rabbit antiserum (Kirkegard and Perry,
Gaithersburg, Maryland, USA) was added to the plates. Following incubation and
wash, peroxidase substrate
(2,2-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid) and peroxide
were added, and the plates were immediately transferred to a BioTek 312 EL
(Winooski, Vermont, USA) kinetics ELISA reader. Plates were read at 30-s
intervals for 16 min using a 405-nm wavelength filter. All antibody
concentrations are given as the slope of the substrate conversion (in
10-3 x optical densities; mOD) over time (mOD/min), analyzed
using KineticCalc software (Winooski), with a higher slope indicating a higher
concentration of anti-KLH antibodies in a sample.
We used a diluent of 1% powdered milk in 0.01 phosphate-buffered saline (pH 7.2) to produce 1:200, 1:800, and 1:1600 dilutions of each postimmunization serum sample. To avoid between-plate variation, we ran postimmunization serum samples from all studied females and each dilution on the same 96-well plate, and the three ELISA-plates were all analyzed on the same day. For the analyses, we used the results obtained for the 1:200 and 1:800 dilutions because these dilutions showed the largest range of antibody titers between individuals. In general, the results of the analyses using the 1:200 or 1:800 dilutions were similar. We did not use the results from the 1:1600 dilution because test samples were overdiluted and antibody titers therefore close to nil for many of the females. We ran one preimmunization serum sample from each female, diluted 1:200, to investigate each individual's back-ground level of anti-KLH antibodies. For each individual, postimmunization serum samples were added to the plate in duplicate, and the average of these was our measure of the antibody titer for each dilution. On each plate we ran at least two wells with blank samples (these wells were treated in the same way as test sample wells except for not adding any tree swallow serum). As our measure of pre- and postimmunization antibody titers of individual females, we subtracted the mean value of these blanks from the measured antibody concentration. Antibody production against KLH in postimmunization samples diluted 1:200 was in all cases at least two times as high as in preimmunization samples. Hence, all female tree swallows reacted to the KLH injection by producing specific antibodies. The postimmunization antibody titer values were then log10 transformed to obtain a more normally distributed data set. To use all the information we gathered from the ELISA and combine it into one measure of HIC for each bird, we standardized (mean = 0; SD = 1) the antibody titers for each of the dilutions 1:200 and 1:800 separately and used the average of these standardized titers as our measure of HIC.
The repeatability (Lessells and Boag,
1987) of the antibody titers between duplicate samples of the same
individuals was high (R =.84, F = 12.5, p <.001,
n = 36). By investigating the plots of substrate conversion over
time, we confirmed that the antibody titers of all individuals were within the
linear range of the ELISA reader. In three females where blood samples were
taken on both day 10 and day 11 after the primary injection, our measures of
antibody production were similar.
Statistics
We used SYSTAT 8.0 (SYSTAT, Chicago) for all statistical analyses.
Residuals were tested for normality using Lilliefors test. We standardized the
antibody titers (see above) and used the average of the standardized titers
for the two dilutions as the measure of each individual's HIC in the
statistical analyses. To obtain a measure of overall female body size, we used
the average of the two measures of female body mass taken at the two times of
capture. These mass measurements were adjusted for the sizes of the birds' fat
deposits by using the residuals from the regressions between fat score and
body mass at first (r =.20, p =.26) and second (r
=.46, p =.006) capture.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSELISARESULTSDISCUSSIONREFERENCES |
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HIC was strongly correlated with the date of egg laying in female tree swallows (r = -.49, p =.002, n = 36; Figure 1). In a multiple regression controlling for female age, size, and feather clipping, there was still a strong negative relationship between laying date and HIC (p =.003), whereas there was no relationship between laying date and age (p =.27), body size (p =.46) or clipping (p =.73; Table 1).
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We also investigated whether increased workload, caused by feather clipping, was a significant predictor of HIC at the time of nestling provisioning. Our feather-clipping treatment had a significant negative effect on HIC when we excluded the two cases with small (one nestling) and considerably reduced brood sizes (t test on the combined means of the standardized log10 antibody titers for the two dilutions; t = 2.47, df = 32.0, p =.019; Table 2). When we accounted for other possible factors affecting HIC during nestling provisioning in a multiple regression analysis, HIC was predicted by clipping (p =.05), but not by brood size (p =.10) or female age (p =.30; Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSELISARESULTSDISCUSSIONREFERENCES |
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In this study we found a strong negative correlation between HIC and date of egg laying in female tree swallows. Surprisingly, this effect is stronger than the effects of age detected in a much larger sample by Winkler and Allen (1996
). Like Winkler and Allen
(1996), we found no effect of
female mass (= body size) on laying date, and the lack of a clipping effect on
laying date (contra Winkler and Allen,
1995) presumably arises because the clipping in our study was
conducted after egg laying and thus could not have had a causal effect on
laying date.
A general problem with correlational studies is how to interpret the
direction of causality between the investigated factors. Our data could either
be interpreted as the result of earlier-breeding females being in better
physical condition and/or of higher quality and therefore able to lay earlier,
or as a result of females breeding earlier in the season gaining higher HIC.
We consider the latter explanation less likely. Breeding earlier appears to be
stressful for Ithaca tree swallows because both temperature and insect
availability increase throughout the period of clutch initiations (e.g.,
Winkler and Allen, 1996;
Winkler DW, unpublished data). Thus, we expect that, like the blue tits
studied by Svensson (1998), the challenge of breeding in colder temperatures
should, if anything, have compromised immune function. Instead, we found a
strong relationship between HIC, an independent, directly measurable
physiological trait, and laying date (an important determinant of reproductive
output in female tree swallows: Stutchbury
and Robertson, 1988; Winkler
and Allen, 1996; Winkler DW, unpublished data). This is an
intriguing indication that variation in HIC among individuals may be an
important component of phenotypic quality in this species. Moreover, in an
indoor study of red-winged blackbirds, there was a relatively high
repeatability (50%) of HIC measured as responses to KLH injected at different
times of the season (Hasselquist et al.,
1999), which supports the interpretation that HIC reflects some
intrinsic quality of individual birds.
HIC is the first known independent physiological measure of phenotypic
quality that shows a relationship with the timing of breeding in female tree
swallows (cf. Winkler and Allen,
1996). As such, it is an important complement to the study by
Saino et al. (1997) on barn
swallows, in which an indirect measure of immunocompetence (change in total
gammaglobulin level in the blood after a challenge with sheep erythrocytes)
was positively correlated with male survival
(Saino et al., 1997). These
studies are important first steps in understanding the biological basis of
quality differences among breeding individuals under natural conditions.
Because HIC can be measured in a large number of animals, including passerine
birds (see also Nordling et al.,
1998; Hasselquist et al.,
1999), it should provide a new and important tool for researchers
investigating the ecologies and life histories of vertebrates.
We also found that the feather-clipping experiment had a negative impact on
female humoral immunocompetence during nestling provisioning, suggesting that
the higher work load reduced HIC. There are a few other studies in wild birds
that have found a negative relationship between workload and immunocompetence.
Svensson et al. (1998) found
that HIC, estimated as antibody responses to diphtheria and tetanus toxoid as
measured in an ELISA, was suppressed in blue tits kept under cold conditions,
as compared with control birds under normal thermal conditions. In an indoor
brood-manipulation experiment on zebra finches Poephila guttata,
Deerenberg et al. (1997) found
that experimentally increased brood size lowered the probability of detecting
any immune response against sheep red blood cells in a hemagglutination test.
An ELISA-based approach to measure HIC was used in a brood-manipulation
experiment (Nordling et al.,
1998) in collared flycatchers, Ficedula albicollis,
showing that increased brood size resulted in lowered antibody production
against an injected antigen (Newcastle disease virus). Moreno et al.
(1999) conducted a brood-size
manipulation experiment and found that T-cell—mediated immune response
(measured as hypersenstivity response; i.e., the relative swelling caused by
an injection with phytohemagglutinin) in females was negatively related to
brood size when controlling for female body mass.
The results of this and other studies indicate that measures of HIC may
serve an important dual role in the analysis of passerine reproduction: HIC
may reflect individual quality (Saino et
al., 1997; this study), and HIC may serve as a sensitive measure
of workload
(Rberg et
al., 1998; Svensson et al.,
1998; this study) and the cost of reproductive effort
(Deerenberg et al., 1997;
Moreno et al., 1999;
Nordling et al., 1998). The
precise nature of the linkage between immunocompetence, phenotypic quality,
and performance of costly behaviors (e.g., reproductive effort) remains
obscure. Careful experimental research under natural conditions will be
required to interpret the causality of these relationships.
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ACKNOWLEDGEMENTS |
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We thank C. Brown, R. Carter, A. Clark, K. Fitch, D. Lapoint, J. Marsh, M. Medler, H. Reeve, and G. Shuster for technical assistance, and E. Adkins-Regan, A. Clark, A. Dhondt, S. Edwards, S. Emlen, T. Natoli, P. Sherman, D. Westneat, and P. Wrege for discussions and encouragement. L. R
berg, J.-
.
Nilsson, R. Ydenberg and two anonymous referees gave constructive comments on
an earlier version of the manuscript. D.H. was supported by grants from the
Swedish Forestry and Agricultural Research Council (SJFR), the Fulbright
Commission, the Swedish Institute, the Crafoord Foundation, the National
Science Foundation (NSF), Cornell University, and Lund University, M.F.W. was
supported by grants from the Benning fund of the Cornell Laboratory of
Onithology, and D.W.W. was supported by NSF IBN 92-07-231, USDA Hatch Project
no. 183428, and Cornell University. The antigen injections, blood sampling,
and feather clipping were conducted under Master Banding Permit 20576,
USF&WS PRT-757670, NYS LCP 96-190, and an approved Cornell Animal Welfare
Protocol. |
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