Behavioral Ecology Vol. 10 No. 5: 598-606
© 1999 International Society for Behavioral Ecology
Energy expenditure, nestling age, and brood size: an experimental study of parental behavior in the great tit Parus major
Zoological Laboratory, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands
Address correspondence to J.J. Sanz, Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutierrez Abascal 2, E-28006 Madrid, Spain. E-mail: sanz{at}mncn.csic.es .
Received 4 September 1998; revised 8 February 1999; accepted 6 March 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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A brood manipulation experiment on great tits Parus major was performed to study the effects of nestling age and brood size on parental care and offspring survival. Daily energy expenditure (DEE) of females feeding nestlings of 6 and 12 days of age was measured using the doubly-labeled water technique. Females adjusted their brooding behavior to the age of the young. The data are consistent with the idea that brooding behavior was determined primarily by the thermoregulatory requirements of the brood. Female DEE did not differ with nestling age; when differences in body mass were controlled for, it was lower during the brooding period than later. In enlarged broods, both parents showed significantly higher rates of food provisioning to the brood. Female DEE was affected by brood size manipulation, and it did not level off with brood size. There was no significant effect of nestling age on the relation between DEE and manipulation. Birds were able to raise a larger brood than the natural brood size, although larger broods suffered from increased nestling mortality rates during the peak demand period of the nestlings. Offspring condition at fledging was negatively affected by brood size manipulation, but recruitment rate per brood was positively related to brood size, suggesting that the optimal brood size exceeds the natural brood size in this population.
Key words: brood size manipulation, doubly-labeled water technique, energy expenditure, great tits, parental care, Parus major.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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One of the central questions in life-history evolution is how the timing and intensity of reproduction is allocated over the lifetime of an individual. Since Lack (1947
)
suggested that clutch size in birds was adjusted to the number of offspring
that the parents are able to raise, much work has been done to identify the
factors limiting the intensity of reproduction. As a model, clutch size
variation in birds has been studied intensively because it allows manipulation
of the parental choice and estimation of the consequences in terms of effort
or fitness (Stearns, 1992). To
identify selection pressures we have to (1) relate effort to brood size, (2)
relate brood size to brood fitness, (3) relate effort to parental fitness, and
(4) relate total fitness to brood size. In the present paper, we concentrate
on the first two questions.
Parental effort has been defined by Williams
(1966) as any behavior a
parent may perform to enhance the reproductive value of the offspring of its
current reproductive attempt at the cost of the parent's ability to invest in
future offspring. The best way to explore the relationship between parental
effort and brood size may be by experimental manipulations of reproductive
effort (Gustafsson and Sutherland,
1988; Tinbergen and Daan,
1990; van Noordwijk and de
Jong, 1986). As a manipulation of parental effort, experimental
modifications of brood size in birds have been studied
(Stearns, 1992), and parental
provisioning is often used as a measure of parental effort. Research has
concentrated on the provisioning behavior of the parents because it is
relatively easy to quantify and is related directly to nestling growth, and
thus probably related to brood fitness
(Lessells, 1993;
Nur, 1984). Most experimental
studies have shown an increase in feeding effort with manipulated brood size
(Lessells, 1993), but the
increase is less than proportional to the number of nestlings
(Nur, 1984). However,
provisioning behavior of the parents is only one aspect of parental care, and
an estimate of parental effort should also include resources allocated to
other forms of parental care such as brooding or nest defense. One approach to
this problem is to quantify parental effort in terms of parental energy
expenditure. Energy is a convenient measure because it allows the expression
of income, capital, and expenditure in the same units
(Drent and Daan, 1980). Work is
accumulating on how parental energy expenditure relates to brood size. The
doubly-labeled water technique (DLW;
Lifson and McClintock, 1966)
offers the possibility to measure energy expenditure under natural conditions.
Bryant and Westerterp (1983)
reported for house martins (Delichon urbica) that parental daily
energy expenditure (DEE) did not differ among treatments in a brood size
manipulation, but feeding rates by these birds were insufficient to match the
rates necessary to rear the enlarged broods. Williams
(1987) reported for Savannah
sparrows (Passerculus sandwichensis) a linear increase of parental
DEE, corrected for body mass, with experimental brood size. Deerenberg et al.
(1995) reported for European
kestrels (Falco tinnunculus) that male DEE did not differ among
experimental treatments, but female DEE increased with experimental brood
size. Moreno et al. (1995)
reported for pied flycatchers (Ficedula hypoleuca) a positive effect
of experimental brood size on male DEE but not on female DEE. Verhulst and
Tinbergen (1997) reported for
great tits (Parus major) in a clutch size reduction experiment that
female and male DEE did not decrease with experimentally reduced clutches. An
association between parental effort, measured as energy expenditure, and
future prospects of the parents has been reported for two species: Deerenberg
et al. (1995) and Daan et al.
(1996) reported for European
kestrels a negative relation between parental DEE and survival rate of the
parents, and Verhulst and Tinbergen
(1997) reported for great tits
a negative relation between parental DEE on the size of second clutches.
Therefore, parental effort may increase linearly with manipulated brood
size (reduced < control < enlarged). However, Drent and Daan
(1980) have suggested that
sustained parental DEE approaches an "energetic ceiling" with
increasing brood size. This hypothesis predicts that parental effort may
asymptotically increase with manipulated brood size (reduced < control =
enlarged). Alternatively, parental effort increases in an accelerating manner
with manipulated brood size (reduced = control < enlarged). This pattern
could come about if the parents have already budgeted the amount of energy to
expend on the chicks for the brood size they produce, and so reducing the
brood could mean that the parent will still be able to invest what it has
already budgeted for, meaning that a reduced brood will receive the same
amount of care as a control brood.
Measurements of parental energy expenditure in brood size manipulations are
made around the time that provisioning is maximal, which occurs in the late
nestling period (Deerenberg et al.,
1995; Moreno et al.,
1995; Verhulst and Tinbergen,
1997). We have little knowledge about how energy expenditure
changes over the nestling period. Hails and Bryant
(1979) found that male, but
not female, house martins increase their DEE in direct relation to the biomass
of the brood. Ricklefs and Williams
(1984) found that female
European starlings (Sturnus vulgaris) increase their DEE from the
early part to the middle part of the nestling period. Deerenberg et al.
(1995) reported for European
kestrels that females, but not males, increase their DEE in direct relation to
the age of the brood. However, in Savannah sparrows
(Williams, 1987), northern
wheatears (Oenanthe oenanthe;
Moreno, 1989), and pied
flycatchers (Moreno et al.,
1995), females show a similar DEE early and late in the nestling
period. Among species with altricial young, more information is needed to
understand how parental energy expenditure changes over the nestling period in
relation to brood size. When sexes share all parental duties, but females do
all or most of the brooding, a principal effect on female DEE is likely to be
the transition from brooding to provisioning.
In the present study, we measured DEE of female great tits tending size-manipulated broods at nestling ages of 6 and 12 days to test (1) whether DEE was dependent on nestling age and (2) whether the effect of manipulation on DEE would depend on nestling age. We further studied the consequences of brood manipulation for nestling growth and survival as well as intraseasonal costs for the parents to interpret how effort relates to costs and benefits of reproduction.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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General
The study was conducted in a mixed deciduous forest in the Lauwersmeer area, The Netherlands (53°20' N, 06°12' E). The Lauwersmeer area comprises land reclaimed from the sea with newly planted patches of trees (age around 25 years) surrounding a lake. The most common tree species are willow, Salix spp.; poplar, Populus spp.; birch, Betula spp.; alder, Alnus spp.; elm, Ulmus spp.; oak, Quercus spp.; and maple, Acer spp. In 1995, 199 nest-boxes were checked for occupation by great tits, and laying date and clutch size were recorded. We checked nests daily around the expected day of hatching to establish the hatching date. Adults were captured with spring traps when the young were 7-10 days old (day of hatching = 0) and ringed, weighed, and measured. We measured and weighed nestlings when they were 6 and 15 days old. All birds were weighed to the nearest 0.1 g with a spring balance, and their tarsus length was measured to the nearest 0.1 mm with a dial caliper (Svensson, 1992
).
Adult and nestling conditions on day 15 after hatching were calculated as the
residuals from the regression of body mass on tarsus length. We visited broods
daily from day 16 onward to establish fledging dates and number of fledged
young.
Brood size manipulation
We randomly assigned nests (only first broods were used) with a similar
hatching date (maximum difference of 1 day) and the same numbers of hatchlings
to one of the treatments: reduced, control, or enlarged. There were no
differences in laying date (ANOVA, F =.13, df = 2, 48, p
=.87) or clutch size (F =.93, df = 2, 48, p =.40) among the
experimental treatments. Manipulation of brood size was carried out on day 2
after the nestlings hatched. Three nestlings were transferred quickly between
nests to create reduced and enlarged broods with the same age. For each
experimental pair of nests, there was a control brood where brood size was not
altered but the nest was subjected to the same disturbance as reduced and
enlarged broods. The experimental broods produced in this way were within the
size range found naturally and, hence, near the expected heritable variation
(Gustafsson and Sutherland,
1988).
Measurements of female daily energy expenditure
We measured DEE of female great tits using the DLW technique
(Lifson and McClintock, 1966).
We measured DEE simultaneously in three birds, one per experimental category,
that hatched their young on the same day, on days 6 (n = 12) and 12
(n = 12) of nestling life. Female great tits stay in the nest-box at
night until around day 14 of nestling life
(Tinbergen and Dietz, 1994).
Females were caught in the nest-boxes between 2100 and 2400 h. After weighing
and measuring their tarsi, we injected them with 0.10 ml of a mixture
containing 2.69 g of 90.1 AP (atom %) [18O]H2O and 1.22
g of 99.9 AP [16O]D2O and kept them in their own closed
nest-box for 1 h (Williams,
1985) to obtain equilibration of isotopes in the body fluids.
Therefore, females were kept from eating and drinking during equilibration
time. After equilibration time, we took blood samples from a brachial vein on
the wing and kept the samples in flame-sealed, heparinized capillary tubes.
After bleeding was arrested, the birds were returned to the brood. The next
night, we caught the females again and took the final blood samples from the
brachial vein in the opposite wing. The females were reweighed and returned to
the brood.
Some females (11 out of 24) did not sleep in the nest-box during the night
that the second blood sample would otherwise be taken. In these cases the
female was captured the next morning to collect the second sample. The energy
expenditure during the inactive phase may have been different from that of the
birds that had roosted in the nest-box. However, due to lack of data, we had
to assume that the night costs for these birds were not different from the
birds that had roosted in the nest-box
(Tinbergen and Dietz, 1994;
Verhulst and Tinbergen, 1997).
As some studies have shown (Tinbergen and
Dietz, 1994; Verhulst and
Tinbergen, 1997), a possible bias is sufficiently small to be
ignored. Statistical analysis showed that the energy expenditure per 24 h was
independent of the duration of the measurement-period (r2
=.03, F = 0.78, df = 1, 22, p =.39), and the duration of
this period did not significantly differ among experimental treatments
(F = 0.64, df = 2, 21, p =.54). Blood samples were also
obtained from five uninjected birds to determine background isotope
concentrations. Background values expressed in 
relative to standard
mean ocean water (SMOW) (Ehleringer and
Rundel, 1988) for both 18O and deuterium were, on
average, 
-18: -1.941% SMOW (SD = 2.11), and -2:
18.428 SMOW (SD = 25.36), respectively.
Blood samples were analyzed for 18O and deuterium concentrations
at the Centre for Isotope Physics of the University of Groningen (The
Netherlands) by mass spectrometry (Masman
and Klaassen, 1987). Estimation of body water via isotope dilution
was not feasible because of lack of precision of injection, and we assumed the
water content to be 66% of body mass
(Mertens, 1987). Daily
CO2 production was determined from fractional turnovers of the two
isotopes using the equations of Lifson and McClintock
(1966). CO2
production was converted to DEE (kJ/day) assuming a respiratory quotient of
0.75 and an energetic equivalent of 19.9 kJ/l of oxygen consumed.
Additional measurements
Mean ambient temperatures on the day of energy expenditure measurements
were obtained from the KNMI monthly reports of Eelde airport, about 50 km
inland from the study area.
We monitored nest-boxes for 3 h using a video camera. The data were averaged to periods of 1 h. Ambient temperature was recorded during video monitoring. Each visit of the nest-box was recorded for both sexes. Feeding visits usually take only a few seconds, but females sometimes remained in the nest-box for a longer period brooding the young. Brooding bout was defined for each observation period as the mean length of the female visits lasting longer than 1 min. In unmanipulated nests, feeding rates per hour of both sexes and time spent brooding by the female were recorded on days 1 (n = 8 pairs), 3 (n = 12 pairs), 6 (n = 14 pairs), and 12 (n = 9 pairs) after hatching. When more than one observation per pair was available for different brood ages, we included one randomly chosen observation in the analyses to avoid pseudoreplication. We calculated female feeding rates per foraging time during the first week after hatching per time not spent brooding. In the experimental categories, these observations were done on days 6 (n = 28 pairs) and 12 (n = 27 pairs) after hatching, including those where DLW measurements were taken.
Statistical procedures
We used stepwise multiple regression analyses and the backward elimination
method of variable selection. Proportions and frequencies were subjected to
arcsine and square-root transformations before parametric statistical analysis
to attain homoscedasticity and normality. Due to the lack of normality and
homoscedasticity in the interval between broods (= laying date of the first
egg of the second brood—hatching date of the first brood) and the laying
date of the second clutch, the differences between experimental treatments in
these variables were analyzed by means of the nonparametric Kruskal-Wallis
one-way test. The effects of experimental treatments were analyzed with
one-way ANOVAs. Using planned a priori specific contrasts for the manipulation
factor, we tested whether aspects of parental effort increased linearly
(reduced < control < enlarged), asymptotically (reduced < control =
enlarged), or in an accelerating manner with experimental treatment (reduced =
control < enlarged). The number of recruits did not differ from a Poisson
distribution (Kolmogorov-Smirnov test, p =.31), and therefore
regression models with Poisson error distributions were used. The statistical
package used for Poisson error analysis was GLIM
(Numerical Algorithms Group,
1987). See Crawley
(1993) for details of GLIM.
Significance was tested with the F test when the scale parameter
(deviance/df) was larger than 1 (p values are conservative).
Statistics are presented as means ± 1 SD.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Parental care: brooding behavior
Only females brooded the young. The proportion of time spent brooding per hour in unmanipulated nests decreased with brood age throughout the nestling period (Figure 1 a; r = -.80, df = 22, p <.001). When combined in a multiple regression, females had shorter average brooding bouts per hour in unmanipulated nests as brood size increased (ß = -.36, p =.02), ambient temperature increased (ß = -.51, p =.01), and as female feeding rate per time not brooding increased (ß = -.39, p =.04) throughout the first week after hatching. These variables contributed significantly to variation in the duration of brooding bouts (R2 =.70, df = 3, 15, p <.001). Ambient temperature (ß = -.46, p =.04) contributed significantly only to variation in the number of brooding bouts throughout the first week after hatching (R2 =.21, df = 1, 18, p =.04). Female feeding rates per foraging time in unmanipulated nests increased with brood age (ß =.69, p <.001) throughout the first week after hatching (R2 =.47, df = 1, 18, p <.001), and the inclusion of brood size and ambient temperature (all p >.24) did not improve this analysis significantly.
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There was no effect of experimental treatment on the proportion of female brooding time on day 6 after hatching (Table 1). When the effects of experimental brood size and ambient temperature were entered as covariates, the proportion of time spent brooding per hour on day 6 after hatching did not differ among experimental treatments, although the effect was close to significance (ANCOVA; F = 3.17, df = 2, 21, p =.06) and showed a negative relationship with the covariates (brood size, ß = -.02, p =.001; ambient temperature, ß = -.10, p =.002).
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Parental care: feeding rate
Feeding rates in unmanipulated nests significantly increased with brood age
(Figure 1 b; females:
r =.86, df = 22, p <.001; males: r =.68, df =
22, p <.001). Feeding rates between the sexes differed
significantly on days 3 and 6 after hatching
(Figure 1 b; paired t
test, day 3: t = 4.72, df = 11, p <.001; day 6:
t = 5.13, df = 13, p <.001), but not on days 1 and 12
after hatching (Figure 1 b; day
1: t = 0.44, df = 7, p =.67; day 12: t = 0.44, df =
8, p =.67).
There was a significant effect of experimental treatment on the number of feeding visits per brood on days 6 and 12 after hatching, which persisted when the sexes were analyzed separately (Table 1). Total feeding rate per hour on day 12 after hatching was positively related to experimental brood size (r =.60, df = 26, p <.001). To look at variation in feeding rates per brood, two-way ANOVAs were performed on the two sexes separately, with experimental treatment and period (day 6/ day 12 after hatching) as factors. Female feeding rate per brood significantly differed among experimental treatments and periods (experimental treatment: F = 10.36, df = 2, 51, p < 001; period: F = 39.42, df = 1, 51, p <.001). For males, there was a significant effect of experimental treatment but not of period on feeding rate per brood (experimental treatment: F = 8.83, df = 2, 51, p =.001; period: F =.99, df = 1, 51, p =.32). Total, female, and male feeding visits per young did not differ among experimental treatments on days 6 and 12 after hatching (Table 1).
When examining differences in female feeding rate per brood on day 6 and male feeding rate per brood on days 6 and 12 among experimental treatments, the prediction that parental effort shows a linear relationship with manipulation explained more variation than the other two predictions (Table 2). However, when examining differences in female feeding rate per brood on day 12 after hatching among experimental treatments, the prediction that parental effort shows an increase in an accelerating way explained more variation than the other two predictions (Table 2).
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Parental care: energy expenditure
The average female DEE measured on day 6 was 85.20 kJ/day (SD = 13.76,
n = 12) and on day 12 was 92.77 kJ/day (SD = 13.16, n = 12).
To look at variation in female DEE, a two-way ANOVA was performed with
experimental treatment and period as factors. In the analysis, experimental
treatment had a significant effect on female DEE (F = 3.93, df = 2,
20, p =.036; Table 3),
but female DEE did not vary significantly with period (F = 2.96, df =
1, 20, p =.10). The interaction between period and experimental
treatment did not improve the analysis significantly (F =.24, df = 2,
18, p =.79). This result was surprising because the female role was
clearly different between these periods, as females brooded the young on day 6
and not on day 12 (Figure 1a),
and consequently feeding rate per foraging time on day 6 was only half of that
on day 12 (Table 1). The lack
of differences in female DEE between periods cannot be due to lower ambient
temperatures because there was no significant difference between periods in
ambient temperature (t = 0.08, df = 22, p =.94). However,
female body mass did differ significantly between periods (t = 3.63,
df = 22, p =.001). Female DEE significantly differed between periods
when controlling for the effect of female body mass (ANCOVA, female body mass,
F = 5.43, df = 1, 21, p =.03, period: F = 6.89, df
= 1,21, p =.016).
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Combining energy measurements for days 6 and 12 after hatching, female DEE was positively related to experimental brood size (Figure 2). Female DEE was not related to the proportion of time spent brooding the young (r = -.27, df = 23, p =.21), although it was positively related to female feeding visits to the nest (r =.57, df = 23, p =.004). When examining differences in female DEE on day 6 after hatching among experimental treatments, the prediction that parental effort shows a linear relationship with manipulation was supported because it explained more variation than the other two predictions (Table 2). However, female DEE on day 12 after hatching did not support any of the predictions (Table 2).
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Nestling growth and survivorship
Nestling body mass on day 6 after hatching did not differ among
experimental treatments (ANOVA, F = 1.20, df = 2, 46, p
=.31). Moreover, nestling body mass and tarsus length on day 15 after hatching
did not differ among experimental treatments (nestling mass: F =
2.28, df = 2, 46, p =.11; tarsus length: F = 1.55; df = 2,
46, p =.22). However, nestling condition on day 15 after hatching
significantly differed among experimental treatments, with higher values in
the reduced treatment (linear contrast, F = 9.33, df = 1, 46,
p =.004; Table 4).
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Brood size at fledging significantly increased with experimental manipulation, with higher values in the enlarged treatment (linear contrast, F = 127.36, df = 1, 46, p <.001; Table 4). This was not due to initial differences among experimental treatments, because original brood size did not differ among experimental treatments (Table 4). The mean age at which broods fledged (18.4 ± 1.1 days, n = 47) did not differ among experimental treatments (ANOVA, F = 2.23, df = 2, 44, p =.12). Nestling survivorship between days 2 and 6 did not differ among experimental treatments, but survivorship between days 6 and fledging differed significantly among experimental treatments, with lower values in the enlarged treatment (linear contrast, F = 13.01, df = 1, 46, p <.001; Table 4). There was a significant effect of experimental treatment on fledging success, with lower values in the enlarged broods (linear contrast, F = 7.93, df = 1, 46, p =.007; Table 4).
The number of recruits increased with both experimental treatment (Figure 3 and Table 5) and brood size after manipulation (Table 5). The number of recruits did not vary with female DEE during the nestling period (Poisson error analysis, F =.07, df = 1, 21, p =.79), with total feeding rate on day 12 after hatching (F = 1.04, df = 1, 25, p =.32), or with female feeding rates on day 12 after hatching (F =.58, df = 1, 25, p =.45), but the number of recruits increased with male feeding rates on day 12 after hatching (F = 5.56, df = 1, 25, p =.026). When brood size after manipulation was included in the analyses, the number of recruits increased with male feeding rates on day 12 after hatching, but did not vary with female feeding rates on day 12 after hatching (Table 5), suggesting that male effort affects recruitment rate per fledgling.
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Parental condition and second clutches
Female and male condition during the nestling period did not differ among
experimental treatments (Table
4). Female condition did not vary significantly with female
feeding rate on day 12 after hatching (r = -.22, df = 23, p
=.30) or DEE during the nestling period (r =.20, df = 20, p
=.38). Male condition did not vary significantly with male feeding rate on day
12 after hatching (r =.04, df = 26, p =.84).
In a logistic model the probability of a second clutch did not differ among experimental treatments (.50,.47, and.50 for reduced, control, and enlarged broods, respectively; F = 1.44, df = 1, 47, p =.24). There was no evidence that the probability of a second clutch and feeding rate on day 12 after hatching were related (female: t = 0.34, df = 25, p =.74; male: t = 1.38, df = 25, p =.18). Moreover, there was no relation between female DEE and the probability of a second clutch (t = 0.01, df = 22, p =.99). However, the length of the interval between the first and the second brood and the laying date of second clutch differed significantly among experimental treatments (Table 6), whereas the clutch size of second clutches did not differ among experimental treatments (Table 6). Laying date of the second clutch was positively correlated with female DEE (Figure 4). The length of the interval between the first and the second brood was positively correlated with female DEE (r =.60, df = 10, p =.05), whereas clutch size of the second clutch was not correlated with female DEE (r = -.25, df = 10, p =.45).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Parental effort and nestling age
Females reduced the proportion of time spent brooding as the young grew older until an age of about 7 days. Females adjusted their brooding behavior to the age of the young, as was experimentally demonstrated by Sanz and Moreno (1995
). As reported in other
studies (Dunn, 1976;
Moreno, 1987;
O'Connor, 1975), the time
spent brooding decreases with increasing brood size. Royama
(1966) suggested that thermal
insulation is dependent on brood size because heat loss per nestling decreases
with increasing brood size (see also
Mertens, 1969). The occurrence
of brooding behavior may balance the brood's decreasing need for brooding with
the increasing energy demands with age
(Clark, 1984;
Moreno, 1987). In
unmanipulated broods, females reduced the duration of brooding bouts with
brood size, but did not increase the feeding visits per foraging time during
the first week after hatching. These results suggest that female brooding
behavior was guided by the brood's need for brooding. In line with this, the
duration and number of brooding bouts decreased as ambient temperature
increased. An alternative explanation for this observation is that foraging
profitability increased with increasing ambient temperature
(Avery and Krebs, 1984).
However, female provisioning rate did not increase as ambient temperature
increased, suggesting that brooding time spent by females is determined
primarily by the thermoregulatory requirements of the brood.
To judge which part of the reproductive period can be regarded as the most
difficult for altricial birds, more information is needed about how parental
energy expenditure changes in the course of reproduction. In the present
study, female DEE did not differ between the early and the late nestling
period. In the European starling, brooding females showed lower metabolic
rates than females feeding ectothermic nestlings
(Ricklefs and Williams, 1984),
and there is evidence that female DEE increased with brood age in house
martins (Hails and Bryant,
1979) and in European kestrels
(Deerenberg et al., 1995),
while male DEE was not affected. However, in Savannah sparrows
(Williams, 1987), northern
wheatears (Moreno, 1989), and
pied flycatchers (Moreno et al.,
1995), brooding females show a similar DEE as females feeding
endothermic nestlings. Williams
(1997) compared energy
expenditure during incubation with energy expenditure during the late nestling
phase. He did not find convincing evidence of differences. Thus, although some
researchers do find evidence that the late nestling period is energetically
expensive for the parents, this is by no means a general rule. Moreover,
feeding rate to the nestlings increases with nestling age, yet no obvious
effect on energy expenditure is apparent. Daily energy expenditure can
therefore not be a unbiased estimate of feeding rate, and vice versa. Because
in a seasonal environment we would expect ecological circumstances to improve
during reproduction, energetic bottlenecks may be expected earlier in the
reproductive cycle. The fact that DEE did not increase with brood age while
feeding rate did needs more attention. Perhaps this was due to differences in
female body mass between the sample periods or to an increase in the food
availability.
Parental effort and brood size
Feeding rates differed between sexes, with males tending to feed more than
females before the peak of nestling demand. As a result of the brood size
manipulation, feeding rates of both sexes were increased in the enlarged
broods. In other brood size manipulations with great tits, Richner et al.
(1995) and Smith et al.
(1988) found that females in
the enlarged broods did not increase their feeding rate with respect to
control broods, but Richner et al.
(1995) found an increase for
males. In the present study, both males and females in enlarged broods fed
significantly more than in control or reduced broods. This leads to the
question of whether there are benefits for each parent of the present breeding
population when they increase their parental effort (see below). On the other
hand, the results suggest that different populations of the same species
responded in a different way to a similar brood size manipulation. The
variation in the conclusions across studies suggest that the ecological
situation may have differed. Feeding rates differed between sexes on day 6
after hatching in the reduced and control broods, but did not in the enlarged
broods. Females fed less to the brood on day 6 in the reduced and control
broods, but they did not brood more at this nestling age. This result does not
support the suggestion that females face a trade-off between collecting food
for the young and brooding them (Moreno,
1987).
Female DEE increased from the reduced to the enlarged treatments,
suggesting that birds adjusted their DEE to manipulated brood size. However,
when we analyzed female DEE separately on days 6 and 12 after hatching, we
observed that on day 6 after hatching female DEE increased linearly with
experimental treatment, but on day 12 DEE was higher but tended to flatten off
with brood enlargement. This is consistent with the idea of a ceiling to
energy expenditure (Drent and Daan,
1980) that limited DEE in the enlarged group during day 12
(Table 3). As a result, until
day 6 after hatching, nestling growth and survival did not differ among
experimental treatments. When birds were raising endothermic nestlings,
nestling mortality appeared and nestling growth differed significantly among
experimental treatments. Nestling body mass and tarsus length on day 15 after
hatching did not differ among experimental treatments, but nestling condition
differed among experimental treatments. Birds increased their parental effort
during the late nestling period, but, perhaps due to an energetic ceiling, not
enough to fully compensate for the manipulation.
Costs of reproduction
In theory, reproductive costs may be survival costs, but also intra- or
interseasonal fecundity costs (Stearns,
1992). We did not try to analyze the effect of the manipulation on
adult survival because of the large data sets needed to demonstrate
statistically small differences in survival probability
(Graves, 1991;
Moreno, 1993;
Nur, 1988;
Roff, 1992). Interseasonal
fecundity costs have been revealed for some species
(Gustafsson and
Pärt, 1990;
Gustafsson and Sutherland,
1988; Røstkaft,
1985), while they have not been found in others
(Korpimäki,
1988; Lessells,
1986; Orell et al.,
1996; Pettifor,
1993; Pettifor et al.,
1988). In the great tit, a double-brooded species, an
intraseasonal cost has been revealed
(Smith et al., 1987;
Tinbergen, 1987;
Verhulst and Tinbergen, 1997).
In double-brooded species, parents can be strongly time- and/or
energy-constrained, facing conflicts between breeding, molting, and the
establishment of winter territories
(Lindén
and Møller, 1989). In the present study, great tits were
able to raise a larger brood than the natural brood size, although larger
broods suffered from increased nestling mortality rates that were detected
during the peak demand period of the nestlings
(van Balen, 1973). Also,
offspring condition at fledging was negatively affected by brood size. Similar
trade-offs have been demonstrated in different studies of birds (review in
Stearns, 1992). In contrast to
previous great tit studies (Smith et al.,
1987; Verhulst and Tinbergen,
1997), young did not fledge at different ages among experimental
treatments. Because parental care in great tits continues after fledging,
Smith et al. (1987) and
Tinbergen (1987) hypothesized
that brood size manipulations could affect this period after fledging.
However, Verhulst and Hut
(1996) showed that the
duration of postfledgling care was not affected in a clutch size manipulation
with great tits.
As has been previously reported in other brood size manipulations
(Smith et al., 1987;
Tinbergen, 1987;
Verhulst and Tinbergen, 1997),
the interval between clutches was affected by the experimental manipulation.
Thus, manipulated female parental effort negatively affected future
reproduction by delaying the second clutch. We observed a correlation between
female DEE and the laying date of the second clutch, although this is not
necessarily causal. To test for causality, other experiments are needed where
energy expenditure is manipulated independently of parental care to avoid the
influence of the first brood on future reproductive decisions of the parents.
A direct association between parental DEE and costs of reproduction has been
shown previously in survival rates of European kestrels
(Daan et al., 1996;
Deerenberg et al., 1995) and in
the size of second clutches of great tits
(Verhulst and Tinbergen,
1997). Costs of reproduction for the parent may be of temporary
nature, and thus recoverable, or they may be persistent. In the present study,
there was no evidence for a permanently decreased reproductive performance
because there was no effect on the size of the subsequent clutch.
Benefits of an increase in parental effort
In altricial birds, clutch size is generally thought to be limited by (1)
the ability of parents to raise young
(Lack, 1947) under prevailing
conditions of their physiology (Drent and
Daan, 1980) in combination with territory quality
(Högstedt,
1980), or (2) the cost incurred by the parents (subsequent
fecundity and/or survival) when raising too many young
(Charnov and Krebs, 1974;
Daan et al., 1996). The higher
offspring recruitment rate that we found in enlarged broods compared to
control or reduced broods suggests that the number of eggs laid by parents may
not be optimal with respect to their ability to raise young in this population
and that parents would be more successful if they laid more eggs. We need more
data on this point to be able to estimate the full consequences in terms of
both costs and benefits of brood manipulations.
The present study suggests that, at least for males, an increase in
parental effort independent of brood size is reflected in a per capita
increase in offspring recruitment rate. This interesting result suggests that
in the great tit there may be a different optimal feeding effort for females
and males. However, this is a complicated problem because the young receive
food from both the male and female. Females could make their males work harder
by working less, and therefore the optimal brood size is a frequency-dependent
problem which cannot be analyzed without knowing the cost. Male great tits
might work at a suboptimal level in a normal situation, and this may explain
why there are differential responses by males and females to brood
manipulations in the great tit (Richner et
al., 1995).
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Blood samples were efficiently taken care of by H. Visser (University of Groningen). J. Moreno and two anonymous referees commented on the manuscript. The study was supported by the H. Kluyver-fonds and the BION grant 436.911-P to J.M.T.J.J.S. was supported by a post-doctoral grant from the Ministerio Español de Educación y Cultura and a contract from projects PB94-0070-C02-01 and PB97-1233-C02-01.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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