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Behavioral Ecology Vol. 12 No. 2: 171-176
© 2001 International Society for Behavioral Ecology
Experimentally reduced male attractiveness increases parental care in the pied flycatcher Ficedula hypoleuca
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), José Gutierrez Abascal 2, E-28006 Madrid, Spain
Address correspondence to J.J. Sanz. E-mail: sanz{at}mncn.csic.es .
Received 30 October 1999; revised 5 June 2000; accepted 15 July 2000.
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ABSTRACT |
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This study reports effects of experimental manipulations of reproductive effort and the size of the male's white forehead patch (a secondary sexual trait), on provisioning rates, reproductive success, and parental breeding dispersal distance in the pied flycatcher, Ficedula hypoleuca. Parents caring for enlarged broods resulting from manipulated clutches provisioned nests at higher rates than parents with reduced broods. Males with a reduced forehead patch fed their nestlings more in relation to males with an unmanipulated forehead patch, and their young fledging with a longer tarsi. This suggests that males with a reduced attractiveness may perceive their own attractiveness and they devote more time available for parental effort given their poorer prospects in male contest competition and/or female attraction for extra-pair copulations. However, their females did not alter their provisioning effort and this runs counter to both the differential allocation and the partner-compensation hypotheses. An artificial decrease in a male secondary sexual trait led to a wider breeding dispersal distance between successive years.
Key words: attractiveness, Ficedula hypoleuca, parental care, pied flycatcher, secondary sexual trait.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSREFERENCES |
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Secondary sexual traits may signal the direct fitness benefits that females can obtain or the indirect fitness of mate choice in terms of sexual attractiveness or genetic quality. Sexual selection occurs because the display traits may be used to assess the quality of potential mates and/or opponents (Andersson, 1994
). If the
expression of the secondary sexual trait reflects the males' ability to feed
their offspring, females would gain a direct fitness benefit from mating with
the most attractive males (Heywood,
1989; Searcy,
1982). The good genes hypothesis suggests that females would also
gain an indirect benefit because only males of high genetic quality will be
able to develop and maintain the largest degree of sexual ornamentation
(Iwasa et al., 1991;
Trivers, 1972;
Zahavi, 1975). The
differential allocation hypothesis suggests that females paired with
attractive mates may increase their parental investment in order to obtain
and/or maintain relatively attractive mates
(Burley, 1986), and
consequently, their partners can afford to reduce their parental investment
and thus gain a survival advantage. However, this could also be explained by
the partner-compensation hypothesis
(Witte, 1995;
Wright and Cuthill, 1992),
females are forced to invest more because their mate contribute less care.
In flycatcher species (Ficedula albicollis, F. hypoleuca), the
sexes differ in the expression of a dimorphic trait, a patch of white feathers
in the forehead (Cramp and Perrins,
1993). In a Spanish population of pied flycatchers Ficedula
hypoleuca a mating advantage was detected for those males with larger
white forehead patches, since chosen males had larger white forehead patches
than rejected ones (Potti and Montalvo,
1991). Evidence suggested that the size of the forehead patch is
highly heritable in both closely related species
(Potti, 1993;
Sheldon et al., 1997). The
white forehead patch is used in male contests, where male collared flycatchers
Ficedula albicollis with relatively large patches enjoy a competitive
advantage in disputes over nestboxes and acquire females more quickly
(Pärt and
Qvarnström, 1997). In male collared
flycatchers, the forehead patch size is positively related to a male's
lifetime reproductive success (Gustafsson
et al., 1995), to his likelihood of being polygynous
(Gustafsson et al., 1995), and
to have a smaller proportion of extra-pair young
(Sheldon et al., 1997). The
size of the forehead patch is sensitive to a male's environment and to past
reproductive effort (Gustafsson et al.,
1995). Finally, Qvarnström
(1997) has shown that male
collared flycatchers with experimentally enlarged forehead patches before
mating experience increased competition from other males, and that those males
have to tradeoff their effort spent in male contests against their parental
effort by reducing provisioning rates.
Experimental manipulations of secondary sexual traits may fail to reveal
fitness costs related to the level of ornamentation, since they do not reflect
developmental costs (Partridge,
1994). However, this problem can be overcome when the main cost of
the trait is to maintain or possess it rather than to produce
(Møller, 1989). The
white forehead patch is presumably energetically cheap to produce
(Butcher and Rohwer, 1989). In
fact, the cost of producing an extra few square mm of white patch is likely to
be negligible
(Pärt and
Qvarnström, 1997). Manipulations of
this trait may be expected to reveal costs resulting from increased risk of
predation or social competition (Andersson,
1994;
Götmark,
1994; Møller,
1987; Rohwer,
1975).
In the present study, I experimentally address the question of whether the
expression of the white forehead patch and thus the attractiveness of male
pied flycatchers in relation to the level of brood demand affects parental
effort and reproductive success. Because of the large data sets needed to
demonstrate statistically small differences in survival probability
(Graves, 1991;
Moreno, 1993;
Roff, 1992), I concentrate my
effort on testing whether parental male breeding dispersal distance between
successive breeding seasons differ among experimental groups. The manipulation
of the attractiveness of males was carried out by reducing the size of the
forehead patch after their nestlings hatched, and was performed with pairs
feeding broods resulting from manipulated clutches. These manipulations were
performed simultaneously to test whether females adjusted their reproductive
activities to the attractiveness of their mate after they had chosen a mate,
in relation to the level of brood demand. I therefore expected that enlarged
clutches led to an increase in parental effort, and that males with an
experimentally reduced forehead patches should increase their parental effort
independently to the level of brood demand. Moreover, in accordance to the
differential allocation hypothesis, females with less attractive partners
should invest relatively less in reproduction independently to the level of
brood demand.
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METHODS |
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Study area and species
The study was conducted during the breeding season of 1997 in a deciduous forest of Quercus pyrenaica in central Spain (40°54' N, 04°01' W). The study area is described in detail by Sanz (1995
). Pied flycatchers are
small, migratory, sexually dichromatic and hole-nesting passerine of European
woodlands (Lundberg and Alatalo,
1992). Males are conspicuously black and white (females are dull
grey-brown and white), with a conspicuous, variably sized white forehead patch
(mean ± SD, 47.2 mm2 ± 14.5, range = 14.5-98.7,
n = 311 males), the size of which is determined during a partial
moult in the winter quarters. Males display their white forehead patch in
disputes over territories until one bird retreats or starts to flee
(Cramp and Perrins, 1993). Egg
laying in the population begins in late May, and clutch sizes range from two
to eight eggs with a mode of six eggs
(Sanz, 1997). Females incubate
alone and receive part of their food from their mate, and both sexes feed the
young that fledge within 15-18 days of hatching.
Breeding variables
Frequent checks of nestboxes provided data on laying date, clutch size and
hatching dates for all breeding pairs. Nestlings were measured and ringed on
day 13 after hatching (hatching date = day zero). Males were captured, aged
(yearlings versus older) according to Svensson
(1992), banded with numbered
aluminium rings and measured on day one or two after hatching of their young.
All birds were weighed to the nearest 0.1 g and their tarsus length was
measured to the nearest 0.1 mm (Svensson,
1992). The male white forehead patch is roughly rectangular in
shape, and patch area (mm2) was calculated by multiplying width and
height. Broods were visited daily from day 16 onwards to establish numbers of
fledged and dead young. Fledging success (proportion of hatchlings that
resulted in fledged young) was considered as a partial measure of reproductive
success. Breeding dispersal distance of survivors was determined as the
distance between the occupied nest-boxes in successive breeding seasons
(Greenwood and Harvey,
1982).
Manipulations of reproductive effort and white forehead patch
For the clutch size manipulation, I randomly assigned nests with the same
laying date and clutch size (six or seven eggs) to one of the experimental
treatments: reduced, control, and enlarged. On the day after clutch
completion, two randomly selected eggs were transferred quickly between nests
to create reduced and enlarged clutches, respectively. For each experimental
pair of nests, there was a control pair where clutch size was not altered but
the nest was subjected to the same disturbance as reduced and enlarged
clutches. Thus, I created three groups of pairs having a clutch size deviating
from their original one by -2, 0, and +2 eggs (original clutch size: 27 trios
of six-egg clutches and 12 trios of seven-egg clutches were used for the
experiment).
For the forehead patch manipulation, nests of alternate previous trios were randomly assigned to either a group in which the male white forehead patch was going to be reduced (17 trios) or to a group in which the male white forehead patch was going to be unchanged (22 trios). In four control nests, males were accidentally assigned to the unmanipulated forehead patch group instead of reduced forehead patch group. Males were captured on day one or two after hatching of their young. There was no differences in male body mass among the different experimental groups (two-way ANOVA: clutch size manipulation, F = 0.00, df = 2, 99, p =.99; forehead patch manipulation, F = 0.69, df = 1, 99, p =.41; interaction, F = 0.33, df = 2, 99, p =.93). The first group of males (reduced forehead group) had their forehead patch reduced by cutting the white part of the feathers of their forehead patch. Their forehead patch was approximately reduced by two thirds. In the second group of males (unmanipulated forehead group), some black feathers were cut from their head without changing it's original forehead patch size. The effect of this manipulation was only temporary since feathers are replaced during the post-breeding moult.
There were no differences in original clutch size (two-way ANOVA, clutch size manipulation, F = 0.07, df = 2, 109, p =.93; forehead patch manipulation, F = 0.12, df = 1, 109, p =.73; interaction, F = 0.10, df = 2, 109, p =.99), laying date (clutch size manipulation, F = 0.01, df = 2, 109, p =.99; forehead patch manipulation, F = 0.88, df = 1, 109, p =.35; interaction, F = 0.88, df = 2, 109, p =.42) or original forehead patch size (clutch size manipulation, F = 2.21, df = 2, 99, p =.12; forehead patch manipulation, F = 0.13, df = 1, 99, p =.72; interaction, F = 0.60, df = 2, 99, p =.55) among the different experimental groups.
Provisioning rates
In experimental categories, feeding rates per h of both sexes were
recorded, between 830 and 1930 h, on day 13 after hatching of their broods
(n = 74 pairs). This day represents the plateau in provisioning rates
of almost fledged young by both parents
(Lundberg and Alatalo, 1992).
Nests were filmed during a period of 1 h with a video camera in order to count
the number of feeding trips performed by both mates. The video camera was
placed 10 m away from the nestbox. There were no significant differences among
experimental groups in the time of day that the nests were filmed (two-way
ANOVA, clutch size manipulation, F = 0.72, df = 2, 68, p
=.49; forehead patch manipulation, F = 0.66, df = 1, 68, p
=.42; interaction, F = 0.37, df = 2, 68, p =.69).
Data analyses
I tested for a relationship between the two treatments and their
interaction on the various measures of parental provisioning rates and
reproductive performance in two-way ANOVAs. Percentages (fledgling success,
proportion of male feeds) were analyzed after arcsine square root
transformation to attain homoscedasticity and normality. All analyses were
performed using SPSS (SPSS,
1986).
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RESULTS |
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Enlarged clutches resulted in more eggs hatched and more fledglings raised than control clutches, and those more than reduced clutches (Table 1, Bonferroni a posteriori test). Fledging success did not differ among clutch size manipulation groups (Table 1). Mean fledgling mass significantly differed among clutch size manipulation groups, with smaller values for the enlarged clutches (Table 1), Bonferroni a posteriori test). Differences between forehead patch manipulation groups in previous variables were not significant (Table 1). Chicks of males with unmanipulated forehead patches fledged with a smaller size than those of males with reduced forehead patches (Table 1, Bonferroni a posteriori test).
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The clutch size manipulation had a significant effect on male feeding rate, with smaller values for the reduced clutches, while there was no such difference between the control and enlarged clutches (Table 2 and Figure 1b, Bonferroni a posteriori test). Females in the reduced clutches feeding nestlings less often than those in the control and enlarged clutches (Table 2 and Figure 1b, Bonferroni a posteriori test). There was a significant effect of clutch size manipulation on the total feeding visits per h on day 13 after hatching, with pairs in the reduced clutches feeding nestlings less often than those in the control and enlarged clutches (Table 2, Bonferroni a posteriori test). The forehead patch manipulation had a significant effect on male feeding rates on day 13 after hatching (Table 2), with males with unmanipulated forehead patches feeding less than those with reduced forehead patches (Figure 1a, Bonferroni a posteriori test). However, female and total feeding rates on day 13 after hatching did not differ between forehead patch groups (Table 2 and Figure 1b). The forehead patch manipulation, but not the clutch size manipulation, had a significant effect on the relative male provisioning rates (Table 2), with lower values for males with unmanipulated forehead patches (Figure 2, Bonferroni a posteriori test).
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Females moved between two successive breeding years significantly further than males did (Student t test, t = 3.45, df = 62, p =.001). Female and male breeding dispersal distances did not differ among clutch size manipulation groups (Table 2). However, male, but not female, breeding dispersal distance significantly differed among forehead patch manipulation groups (Table 2), with smaller values for males with unmanipulated forehead patches (Figure 3). There was no differences in male white forehead patch in the subsequent breeding season among the different experimental groups (two-way ANOVA, clutch size manipulation, F = 0.50, df = 2,24, p =.62; forehead patch manipulation, F = 0.01, df = 1,24, p =.90; interaction, F = 0.81, df = 2,24, p =.46).
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Discussion
Parents caring for enlarged clutches fed their broods at a higher rate than
parents rearing reduced clutches on day 13 of nestling life. Therefore, the
experimental manipulation changed the work load of parents. However, fledgling
body mass was negatively related to the experimental change in clutch size.
These results suggest that the increased feeding response by parents did not
compensate for the increased food demand in the enlarged clutches. There was
no effect of the clutch size manipulation on parental breeding dispersal
distance between two successive breeding years. The present result is parallel
to that of Siikamäki et al.
(1997) with a similar
experimental manipulation with pied flycatchers in northern Europe.
The main aim was to manipulate male attractiveness and parental effort
(clutch size manipulation) after mate acquisition to examine whether females
adjusted their reproductive effort to the attractiveness of their mates after
they had chosen them. The design allows one to test in a field study
predictions of the differential allocation hypothesis
(Burley, 1986). The findings
partially support the differential allocation hypothesis, as males with a
reduced attractiveness increased their parental effort and had a wider
breeding dispersal distance between two successive breeding years. However,
the hypothesis is not borne out in other way, as the females of attractive
males did not have higher feeding rates, although the trend is actually in the
predicted direction (Figure
1b). Moreover, offspring reared by males with reduced forehead
patches were larger. Thus, this study does not support the differential
allocation hypothesis, but the power of the test is weak due to small sample
sizes (Figure 1). Rather, the
increased feeding rate by males with reduced white forehead patch size appears
to be totally male-driven. Males provided a relatively larger fraction of
feeding visits to their brood if their forehead patch had been experimentally
reduced. The result was independent of the manipulation of parental effort
that was created by the clutch size manipulation.
Witte (1995) suggested that
it is difficult to distinguish between the partner-compensation effect and the
attractiveness-effect predicted by the differential allocation hypothesis
because the feeding rate of one partner depends on that of the other partner
(Sanz et al., 2000, and
references therein). Further evidence for differential investment in barn
swallows (Hirundo rustica) was that females paired to attractive
males often lay a second clutch (de Lope
and Møller, 1993). However, the partner-compensation effect
predicts that an increase in feeding effort by one partner may result in a
decrease in effort by the other (Winkler,
1987), but the present study does not support this prediction.
Females worked at the same level independently of what their males were doing.
It has been repeatedly shown that the provisioning rates of both members of
the same pair are not correlated in the Pied Flycatcher (Moreno et al.,
1995,
1997). In the present study,
the feeding contribution of parents was measured in terms of the number of
feeding visits to the nest and not in terms of number of prey brought per
visit or food quality. Thus, an increase of parental effort could occur if
birds fed their broods with larger or better quality prey. This possibility
could be tested with more data, but in a brood size manipulation in the same
population there were no effects of brood size on the mean number of prey
brought per feeding visit and on nestling diet
(Moreno et al., 1995).
Why do males with a reduced forehead patch increase their parental effort?
One possible explanation of this fact is that males may perceive that they are
now less attractive. Males perceiving a reduction in their own attractiveness
may have a reduced expectation of future reproductive success and this could
account for their increased investment. Another possible explanation of this
fact is that males trade-off their effort spent in other activities against
their parental effort
(Qvarnström,
1997). Less attractive males may not be able to obtain extra-pair
copulations due to their lower attractiveness, or they may not be able to
intimidate other competitors over territory disputes. Therefore, they may have
more time available for parental effort. Extra-pair copulation attempts occur
when the intruding male's female is incubating or feeding nestlings and the
territory on which he intrudes has a female which is in the nest-building or
egg-laying period (Lundberg and Alatalo,
1992). Male pied flycatchers guard females during this time
suggesting that there is a risk of extra-pair copulations
(Lundberg and Alatalo, 1992).
Possibly the white forehead patch is used by females in deciding whether or
not to solicit or permit an extra-pair copulation
(Sheldon et al., 1997). In the
present breeding population, males were seen visiting nestboxes of other pairs
during the nestling period (Sanz JJ, unpublished observations), perhaps
looking for information about future territories or extra-pair copulations.
Males with a reduced forehead patch may decide to invest more in their current
brood, instead of spending more time in other activities. However, such a
re-allocation should not result in a wider breeding dispersal distance. On the
other hand, at this time (day 13 after hatching) male-male competitions for
territories are very rare, and it is very unlikely to find a fertile female
for an extra-copulation. Thus, this argument does not hold to explain why
unacttractive males fed young more often. To get a better idea about why males
with a reduced forehead patch feed their young more often, we need more data
about on male-male interactions and extrapair copulations during the
experimental period to be able to get a better explanation of this fact.
A different possible explanation is that females may force their mates to
work harder via behavioral clues. Males with a reduced forehead patch that
decided to invest more in their current brood obtained a clear benefit, their
young fledging with longer tarsi. In the Pied Flycatcher it is known that
prospects of future survival for fledglings are weight and size dependent
(Lundberg and Alatalo, 1992).
However, the results obtained from the present study can not be fully
understood in the context of both the differential allocation and the
partner-compensation hypotheses.
The present study shows that an artificial increase in male parental effort
via a decrease in their attractiveness led to a wider breeding dispersal.
Moreover, females without an observed increase in parental effort and mated
with less attractive males did not change their breeding dispersal distance.
Breeding-site fidelity of pied flycatcher males has been found to be quite
high (Lundberg and Alatalo,
1992). Movements have often been interpreted as a means of
acquiring better territories (Newton and
Marquiss, 1982) and can be explained in terms of individual choice
strategies
(Pärt and
Gustafsson, 1989). Pärt and
Gustafsson (1989) have been
shown that breeding dispersal distances are related to prior local experience
in the Collared flycatcher because they benefit from exploring more sites
before settling than do those with good local experience. A possible
explanation of the present results is that males paired with females that did
not response to their increase in parental effort tended to move to a new
breeding site looking for different mates or territories. They had a bad local
experience and decided to find a new territory, because in this species male
choice of breeding site is based mainly on territory quality
(Lundberg and Alatalo, 1992).
Breeding dispersal may indeed be correlated with mate fidelity
(Harvey et al. 1979;
Newton and Marquiss, 1982). It
has been found that individuals with a low breeding success in the previous
year tended to move to a new breeding site
(Greenwood and Harvey,
1982).
In conclusion, this study shows that clutch size manipulations provoke changes in work rate in both sexes. On the other hand, the present study provides more evidence that the attractiveness of parents influences provisioning effort. Males with a reduced white forehead patch may perceived their own attractiveness and they devote more time available for parental effort given their poorer prospects in male contest competition or female attraction for extra-pair copulations. However, in disagreement with both the differential allocation and the partner-compensation hypotheses, females paired with less attractive males that reduced their feeding effort do not decrease their effort, but the power of the test is weak due to small sample sizes and the trend is actually in the predicted direction. Finally, this study reveals that an artifical decrease in a secondary sexual trait increased male breeding dispersal distance between two successive breeding years.
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ACKNOWLEDGEMENTS |
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I thank Juan Moreno for assistance to collect data in 1998. J. Moreno and anonymous referees provided constructive criticism on the manuscript This is a contribution from the field station "El Ventorrillo," Museo Nacional de Ciencias Naturales (CSIC). I was supported by a "reincorporation contract" from the projects PB94-0070-C02-01 (DGICYT) and PB97-1233-C02-01 (DGES) of the Spanish Ministry of Education and Culture. The Dirección General para la Conservación de la Naturaleza donated the nestboxes, while J. Donés (Montes de Valsain) gave permission to work in the forest. The Dirección General del Medio Natural of the Junta de Castilla y León gave license (EP-51/97) for capturing, ringing and handling birds.
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