Behavioral Ecology Vol. 10 No. 5: 504-509
© 1999 International Society for Behavioral Ecology
Is clutch size individually optimized?
a Zoological Laboratory, Groningen University, PO Box 14, 9750 AA Haren, The Netherlands b Netherlands Institute of Ecology, Center for Terrestrial Ecology, PO Box 40, 6666 ZG Heteren, The Netherlands
Address correspondence to J. M. Tinbergen. E-mail: tinberge{at}biol.rug.nl .
Received 11 August 1998; revised 25 November 1998; accepted 2 February 1999.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Brood size manipulations were carried out to test whether clutch size variation in individual great tits (Parus major) controlled for laying date was tuned to their phenotypic quality and/or local food abundance (individual optimization hypothesis; IOH). Broods with different original clutch sizes, but equal hatching dates, were manipulated to a common brood size. A third brood was kept as a control. Under the IOH, we expected a positive association between reproductive success and original clutch size. Fledgling production varied in an inconclusive way after manipulation, with data from 1 out of 3 years favoring the IOH. The effect of manipulation on the probability of a second clutch was consistent with the IOH in another 1 out of the 3 years. When fitness accrued to second broods was also taken into consideration in terms of annual fledgling production, results from 2 out of 3 years tended to support the IOH. There was no effect of the manipulation on fitness (estimated as the number of recruits plus parents breeding in the next season). Both the clutch component (local recruitment) and the parental component (survival till next breeding season) varied inconclusively with respect to the IOH. On the basis of fitness measurements, the IOH could not be confirmed as an explanation for clutch size variation in this population. In 2 out of 3 years one of the three fitness components measured varied in accordance with the IOH. Overall the evidence for the IOH in this data set is therefore weak.
Key words: clutch size, brood size manipulation, fitness, great tits, individual optimization, Parus major, phenotypic quality.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Individual optimization of clutch size implies that phenotypic plasticity in clutch size is adaptive (Drent and Daan, 1980
;
Högstedt,
1980; Lessells,
1991; Perrins and Moss,
1975; Pettifor et al.,
1988). This means that individuals adjust clutch size to their
circumstances, and that any deviation from the chosen clutch size reduces
fitness (the individual optimization hypothesis; IOH). To prove the IOH
unambiguously, we face the enormous task of manipulating clutches of different
sizes and measuring subsequent fitness consequences for both the offspring and
the parents. Such an experiment supports the IOH if manipulation always lowers
the sum of offspring and parental fitness, independent of the original clutch
size. In this study we tested an aspect of the IOH using brood size
manipulations in the great tit. In this approach birds get "free"
chicks, and it thus assumes that fitness costs and benefits are primarily
derived during the nestling phase or later and are not associated with the
egg-laying or incubation process. Because Monaghan and Nager
(1997) showed that in a number
of species egg laying does incur a cost, experiments to validate this
assumption in the great tit are necessary.
From experimental studies where fitness consequences of variation in clutch
size were measured, evidence has accumulated that clutch sizes were optimized
at the individual level in a number of species.
Högstedt
(1980) showed that fledging
success in magpies Pica pica was maximized for the original clutch
size. In an English great tit study, Perrins and Moss
(1975) showed that
artificially large broods had lower recapture rates per brood than natural
large broods, while reduced broods did better when compared with the natural
small broods. These data point at a positive relation between the ability to
raise a brood and original clutch size. Pettifor et al.
(1988) followed up this work.
They did not find brood size manipulation effects on parental survival.
Recruitment rate (offspring returning to breed) per brood peaked around
non-manipulated clutch sizes, again pointing at individual optimization. In
the blue tit Parus caeruleus, Pettifor
(1993) showed similar results
for offspring recapture rates (after 3 months) per brood. In a Dutch great tit
study, Tinbergen and Daan
(1990) showed that there was
an effect of manipulation on both offspring and parental fitness. Brood size
reduction and enlargements reduced total fitness, but fitness was positively
related to natural variation in clutch size. The combination of these results
again suggests individual optimization of clutch size. In the collared
flycatcher Ficedula albicollis, Gustafsson and Sutherland
(1988) showed that the
nonmanipulated clutch size produced more recruits than an enlarged or reduced
clutch, and, in addition, that for natural clutch sizes there was a positive
relationship between clutch size and the number of recruits. In the kestrel
Falco tinnunculus, Daan et al.
(1990) showed that the seasonal
decline in clutch size could be explained by individual optimization. In
contrast to these data supporting the IOH, Nur
(1986; but see
Pettifor, 1993) did not find
evidence in blue tits for individual optimization, and in an island population
of great tits, Verhulst (1995)
showed that brood reduction increased fitness, leading to the conclusion that
clutches were larger than optimal. Also, Lessells
(1986) did not find evidence
for individual optimization of clutch size in the Canada geese Branta
canadensis.
As mentioned, there is evidence that individual optimization occurred in
our study population (Tinbergen and Daan,
1990). We based our argument on a rather complex analysis of the
different fitness components involved and calculated the overall effect of
clutch size on the sum of offspring and parental fitness. Theoretically this
approach is correct, but the drawback is that direct statistical tests cannot
be applied. We felt that a more direct test to show the existence of IOH was
appropriate.
In this study, in contrast to earlier studies, we manipulated different clutch sizes to a common brood size and controlled for hatching date by analyzing the manipulation effects within the manipulation set. Each set contained the two nests between which we exchanged young, in most cases supplemented with the control nest. We concentrated on the aspect of the IOH that original clutch size is adjusted to phenotypic quality and/or food abundance, and clutch size therefore should correlate with the chick-raising ability of that parent. Because we do not test whether fitness is reduced after either reduction or enlargement of brood size, the tests cannot be regarded as a test of the IOH in general. Furthermore, we specifically tested for clutch size variation independently of date. On one hand, this approach reduced the variation in clutch size used; on the other hand, the outcome is not affected by date-dependent processes such as juvenile dispersal. If clutch size is not adjusted to phenotypic quality (including environment), fitness after manipulation of two different clutch sizes to one common brood size should not depend on the original clutch size. However, if clutch size was adjusted to phenotypic quality, we expected the fitness after manipulation to be positively related to the original clutch size. Thus, under the IOH we have the expectation that birds that laid large clutches would do better than birds that laid smaller clutches when facing an identical task: raising an equal number of offspring.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Study area
The experiments were carried out in the Hoge Veluwe in the central Netherlands. The study area covers 171 ha of mixed wood, with oak and pine as the dominant tree species, in which about 400 nest-boxes were provided. The nest-boxes were checked at least weekly during the breeding season from the beginning of April until mid-July. For a more detailed description of the study area and the nest-box inspections, see Van Balen (1973
).
The great tit is an 18-g, hole-nesting passerine, common in woodlands in
Europe and large parts of temperate Asia. In our area great tits sometimes
start a second breeding attempt after successfully raising a first brood; low
breeding densities and breeding early in the season enhance the probability of
a second clutch (Kluyver,
1951). After failure of the first brood, most great tits start a
repeat clutch.
Manipulation experiments
Manipulation experiments were carried out in 1988, 1991, and 1992 with the
goal of equalizing the brood size of pairs that had laid clutches that
differed in clutch size. In addition, one control nest with intermediate
clutch size was chosen. We inspected nests daily at the time the eggs were
expected to hatch in order to obtain hatching date. Chicks were exchanged
between sets of two or three nests with different clutch sizes that hatched on
the same date. We did not compensate for hatching failure by adding chicks
from other nests because most individuals do experience hatching failure of
one egg or more (two-thirds of the population). The proportion of eggs not
hatched was independent of clutch size (logistic regression, p
>.5); the number of nonhatched eggs was dependent on clutch size (Poisson
regression, p <.02). A bird "choosing" a particular
number of eggs is expected to anticipate the hatching failure. Before
manipulation the chicks were marked so that they could be recognized at
ringing (nestling age 7 days, hatching date = day 0). Experimental sets of
three nests were composed of clutches with the same difference between
smallest and the control and between the control and largest clutches. One to
four days after the first egg hatched (mean = 2.11, SD = 0.83), we manipulated
all broods within an experimental set to the same brood size. To control for
possible genetic and maternal effects, chicks were transferred between broods
so that no brood contained more than half of its original chicks. The
manipulation resulted in experimental sets having a reduced brood (the
original largest clutch), an enlarged brood (the original smallest clutch),
and usually having a control brood (the intermediate clutch size). Within
broods there was no difference between the initial (paired t test, t
= -0.41, df = 103, p =.68) or final (t = -0.41, df = 99,
p =.68) mass of the additional chicks compared to the host chicks,
nor in the final tarsus length (paired t test, t = -0.88, df
= 102, p =.38). No differences in survival between own and
manipulated young were found, nor was there a correlation between the clutch
size of the real parents and offspring survival.
In 1988, 1991, and 1992 the number of broods used was 51 (17 sets), 46 (16 sets), and 59 (25 sets), respectively. Clutch size, the absolute difference between clutch size and brood size after manipulation, nestling survival, nestling growth, recruitment rate, and the occurrence of second broods all varied significantly between years (clutch size, F2, 153 = 37.12, p <.001; manipulation F2, 153 = 7.27, p =.001; see Results for statistics on other variables). We believe that this variation between years is important in the interpretation of clutch size optimization, and therefore most analyses have been carried out for each year separately. An overview of the most important parameters measured per manipulation category is given in Table 1 as a summary over all years.
|
Fitness measurements
As the fitness measure of a brood, we used the sum of offspring and parents
produced in the year of study that were recovered in the next year's breeding
population. The offspring of second and repeat clutches were included when
produced by the female. Longer lasting effects of manipulation have not been
shown in this population (Tinbergen and
Daan, 1990). Because offspring and adults differ in the rate of
dispersal, we analyzed, in addition to total fitness, each of the components
separately.
Breeding adults were identified on the basis of their rings, allowing us to
estimate the probability of the parents having a second brood in the same
year, or survival to the following year, and of the offspring surviving and
breeding in the study population (hereafter called "local
recruitment"). To analyze effects of manipulation in more detail, a
number of additional measurements were used: survival rates of offspring in
the nest and mean fledgling mass per nest (at brood age of 14 or 15 days),
together predictors for recruitment
(Tinbergen and Boerlijst,
1990).
|
ANALYSES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
All analyses were performed on mean values per nest. To control for differences in hatching date and initial condition of the chicks, comparisons were made after controlling statistically for the experimental sets. Binomial variables, such as survival rates or probability of having a second brood, were analyzed using logistic regression. Where appropriate, Williams correction or an F test was used to correct for overdispersion (Crawley, 1993
). We used
log-linear models with a Poisson error (Poisson regression) to analyze fitness
variation. All significance tests are two-tailed, unless otherwise stated. In
analyses where data of the different years were tested simultaneously, we
tested the interaction term between year and experimental treatment.
Nonsignificant interaction terms are not mentioned in the text. |
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Nestling mass
Fledgling mass differed between years (ANOVA, F2, 131 = 6.87, p =.0016). Within years, only in 1988 was there a set effect (Table 2), with later fledglings being lighter. After controlling for set, there was no effect of manipulation in any of the years (Table 2). Tarsus lengths differed between years (ANOVA, F2, 130 = 20.37, p <.001), but not between sets or manipulation (Table 3).
|
|
Nestling survival
Nest failure rates (no chicks fledged) did not differ between years, nor
between sets (logistic ANOVA, 
22 = 2.5, p
>.5, 572 = 55.6, p >.5). Taking all
years together, nest-failure rates differed significantly between manipulation
categories after controlling for set (logistic regression,
22 = 13.69, p =.0016). Nest failure rates
for enlarged, control, and reduced clutches were 10%, 5%, and 21%,
respectively.
Nestling survival differed significantly between years (means: 1988, 65%; 1991, 44%; 1992, 68%; F2, 153 = 6.15, p =.003). Nestling survival was affected by manipulation in 1988, but not in the other years (Table 4). This effect was in the direction predicted under the IOH: the survival rates for enlarged, control, and reduced clutches were 53%, 70%, and 74%, respectively. Excluding the failed nests from the analysis of nestling survival did not qualitatively alter the results of the treatment effect.
|
Occurrence of second broods
The occurrence of second broods after parents had successfully fledged a
first brood differed significantly between years (logistic ANOVA,
22 = 42.22, p <.001, percentages for
1988, 1991, and 1992 were 0%, 17%, and 47%, respectively). Only in 1992 was
there both a set effect (242 = 37.9, p
=.035) and a manipulation effect (22 = 11.46,
p =.0033): the percentage of second broods for enlarged, control, and
reduced broods were 33%, 57%, and 60%, respectively. The results for 1992 are
in accordance with the IOH.
Total number of fledglings in the whole breeding season
The total number of fledglings (including first, second, and repeat
clutches) produced during the breeding season differed between years (ANOVA,
F2, 153 = 35.8, p <.001). Within years it only
differed in 1988 between the sets (ANOVA, 1988: F16, 32 =
3.45, p =.0014; 1991: F15, 39 = 0.60, p
=.85; 1992: F25, 32 = 1.01, p =.48), and
controlled for years and sets, there was no treatment effect in any of the
years (ANOVA, 1988: F2, 32 = 2.79, p =.076; 1991:
F2, 30 = 0.18, p =.83, 1992: F2,
32 = 1.89, p =.18). In 2 out of 3 years there was a trend in
the direction expected under the IOH
(Figure 1).
|
Taking all years together, the total number of fledglings produced over the breeding season differed between experimental sets (F57, 96 = 2.38, p <.001). There was an almost significant effect of manipulation (F2, 96 = 2.92, p =.057) in the direction predicted by the IOH. Birds with a larger original clutch size tended to produce more fledglings during the whole breeding season. Although in 1988 we found an effect on the first brood, in 1992 on the second brood, and in 1991 no effect of the manipulation at all, the interaction between year and experimental treatment was nonsignificant.
Local survival of parents and juveniles and brood fitness
Parental local survival (recovered as breeding bird in the next year's
population) did not differ between years for either males or females (males:
22 = 3.84, p =.14; females:
22 = 2.53, p =.28). Taking all years
together, for males there was no between-experimental sets effect
(572 = 70.48, p =.11), but within sets
there was a manipulation effect (22 = 6.16,
p =.046; enlarged 38%, control 41%, reduced 23%). The lower survival
of the males in the reduced category originates from 1992 alone. This effect
could not be explained by the higher incidence of second clutches in that year
(12 = 0.92, p >.3), and remains
unexplained. For females there was a between-set effect
(22 = 83.4, p =.012) but no effect of
manipulation on local survival (22 = 0.90,
p =.64, enlarged 43%, control 49%, and reduced 46%).
The number of recruits from first broods in the local population differed
between years (22 = 36.36, p <.001),
and between sets (572 = 92.77, p =.01),
but within sets there was no manipulation effect on local recruitment
(22 = 2.68, p =.26, log linear model with
Poisson error).
To judge the overall effect of manipulation on fitness, we estimated
fitness as the sum of the recruits and the survived parents. Fitness did not
differ between years (22 = 2.29, p >.3)
or among manipulation categories (22 = 2.36,
p >.3, log linear model with Poisson error) when controlled for
set (Figure 2). The survival
data for parents and offspring combined as a fitness measure provided no
support for the IOH.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
This paper tested the prediction of the IOH that birds that lay a large clutch do better in raising a brood manipulated to intermediate size than birds that lay a small clutch. When years were analyzed separately, we found an association in 1 year (1988) between nestling survival and original clutch size and in another (1992) between the probability of a second clutch and original clutch size. In the third year (1991) a spring frost damaged the major food plant of the bird's prey, resulting in exceptionally low food abundance. Overall annual fledgling production tended to be associated with original clutch size.
The support for the IOH was thus weak as compared to the results of
Högstedt
(1980). Other studies that
specifically addressed the question of individual optimization of clutch size
and measured short-term consequences did not support the IOH
(Barber and Evans, 1995;
Harper et al., 1994;
Maigret and Murphy, 1997).
Decisive for accepting the IOH are the long-term consequences: fitness effects
of manipulation in relation to the original clutch size. In this study overall
fitness estimates (offspring plus parents surviving till the next year) were
not related to original clutch size and therefore did not support the IOH.
Two aspects of phenotypic quality can play a role in individual
optimization: environmental variation and variation in parental quality.
Offspring chances depend strongly on food abundance and subsequent growth
(Henrich-Gebhardt, 1990;
Tinbergen and Boerlijst, 1990;
Van Balen, 1973;
Van Noordwijk and
Müller, 1994;
Verboven, 1998), and parents
are expected to enhance their fitness by adjusting clutch size to the food
availability if cues are available. In addition, quality differences between
parents independent of their current environment may also affect the
individual optimal clutch size. The fact that we did not find an association
between original clutch size and the ability to raise a brood shows that in
our experiment both food availability and parental quality did not covary
detectably with original clutch size. This may be because the parents were
constrained by low predictability of the food supply or energetically during
the egg laying or the incubation phase, for instance. It is also feasible that
the costs associated with clutch size are not paid during the chick-rearing
phase but in an earlier phase (egg laying or incubation). These effects cannot
be detected with brood size manipulations as used in this experiment
(Monaghan and Nager, 1997) and
need further study.
The results of this paper contrast with our interpretation of earlier
results obtained in the same study population
(Tinbergen and Daan, 1990). As
mentioned in the Introduction, we found that experimental variation in clutch
size lowered fitness, while fitness was positively associated with natural
variation in clutch size. Combination of these two findings led us, in
agreement with Gustafsson and Sutherland's
(1988) findings for the
collared flycatcher, to the conclusion that great tits were individually
optimizing their clutch size.
There are a number of reasons the interpretation of the earlier results
(Tinbergen and Daan, 1990)
might differ from the results of the current study. First, fitness surface
around the optimal clutch size is expected to be flat, and therefore small
deviations in clutch size may not have measurable effects in fitness. Compared
to the other experiments, our current manipulation was small in 2 years (1991,
1992), whereas in the first year (1988) the manipulation was larger and some
effect was found. This indicates that the power of the current test may simply
be too small to detect differences due to a smaller manipulation at comparable
sample size. For mean nestling mass we calculated the power on the basis of
the data set used in Tinbergen and Daan
(1990). When controlled for
year, nestling mass differed 0.089 g per egg (SE 0.062,
F1,219 = 2.056, p >.15) for the natural
variation, while for manipulation this effect was.293 g per manipulated young
(SE = 0.026, F1,219 = 117.16, p <.0001). The
expected difference in nestling mass between the enlarged and the reduced
broods in the current experiment was therefore 0.602 g [(3.08 x 0.293) -
(3.38 x 0.089)]. From the same material, the standard deviation of mean
nestling body mass was estimated for control broods as 1.43 g. The power to
detect such a difference over the whole material (n = 58) was
>0.95, which can be regarded as high. Because we expected, on the basis of
earlier experiments, that if anything was affected by the experiment, it would
be mean nestling mass, we see this as an argument against the idea that our
results are solely due to small sample sizes.
Second, we controlled more rigidly for date effects in the current experiment. By using the set approach, we compared birds that hatched their eggs on the same day instead of controlling statistically for date as we did before. Potentially the IOH effect could arise by differences between early and late broods in both their clutch size and their fitness. We therefore analyzed the fitness effects regardless of set or date using Poisson regression. The effect of original clutch size on the number of recruits did not explain a significant amount of variation (p >.3), even when controlled for year and/or brood size after manipulation, leaving no scope for this explanation of the discrepancy.
Third, the fitness measure used differed between the studies. In our
earlier paper (Tinbergen and Daan,
1990) we used the expected lifetime production of eggs as a
fitness estimate. Consequently we weighed eggs of second clutches equal to
eggs of first clutches. Local recruitment rates of second-brood young are,
however, much lower than those of first-brood young
(Verboven and Visser, 1998),
leading to differences between the fitness estimates used. Which fitness
estimate is better depends on the dispersal of the offspring. Dhondt
(1970) showed in a number of
small woods around Ghent in Belgium that survival of second-brood young did
not differ with that of first-brood young when adjusted for dispersal. Because
we only found effects of manipulation on the occurrence of the second clutches
in 1 out of 3 years, we do not think that the difference in fitness measure
used causes the discrepancy.
Finally, individual optimization occurs in some years or areas and not in
others. Birds that optimize their clutch size individually in a variable
environment need cues to predict environmental variation. Cues may not always
be available, resulting in variation in the degree to which individual
optimization occurs. We believe that this last point offers the most likely
explanation for the discrepancy between our current and earlier results
(Tinbergen and Daan, 1990).
There is need for more research that addresses differences in optimal clutch
size between years within a data set to clarify this point further.
Summing up, seven studies provide experimental data to specifically test
the IOH on the basis of fitness measures in relation to manipulation and
original clutch size. Three support the IOH
[Daan et al., 1990 [clutch size
and laying date, kestrel]; Perrins and
Moss, 1975; Pettifor et al.,
1988 [clutch size, great tit];
Pettifor, 1993 [clutch size,
blue tit]); four did not find evidence supporting the IOH
(Lessells, 1986 [clutch size,
canada geese]; Nur, 1986
[clutch size, blue tit]; Verhulst,
1995 [clutch size, great tit]; this study [clutch size, great
tit]). Two further studies deduced the occurrence of individual optimization
from the fact that artificial variation in brood size led to fitness
reduction, whereas fitness was positively associated with natural variation in
clutch size (Gustafsson and Sutherland,
1988 [clutch size, collared flycatcher];
Tinbergen and Daan, 1990
[clutch size, great tit]). Individual optimization of clutch size is thus by
no means a general rule. The picture emerges that the role of individual
optimization differs between populations and species, or perhaps within
populations individual optimization occurs in some years but not in others.
But why? One suggestion is that some populations deal with more predictable
variation in the relevant parameters; another is that quality differences
between birds are more pronounced in some populations than in others. Verhulst
(1995) suggested that optimal
decision rules for clutch size might differ between populations but that gene
flow prevents local adaptation. In this light it is interesting that the tit
populations where individual optimization was detected tend to occur in richer
forests, potentially the source populations.
|
ACKNOWLEDGEMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
We particularly wish to thank Jan Visser for all the advice, assistance during fieldwork, and management of the database. Martin Olthoff and Dirk Westra made most of the weekly nest-box checks. Maarten Boerlijst did a lot of fieldwork as part of his undergraduate project. Serge Daan, Rudi Drent, Kate Lessells, Arie van Noordwijk, and Marcel Visser made many valuable comments on earlier drafts of this paper.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSANALYSESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Barber CA, Evans RM, 1995. Clutch-size manipulations in the yellow-headed blackbird: a test of the individual optimization hypothesis. Condor 97 (2):352-360.
Crawley MJ, 1993. GLIM for ecologists. Oxford: Blackwell Scientific.
Daan S, Dijkstra C, Tinbergen JM, 1990. Family planning in the kestrel (Falco tinnunculus): the ultimate control of covariation of laying date and clutch size. Behaviour 114:83-116.
Dhondt A, 1970. De regulatie der aantallen in Ghentse Koolmeespopulaties (PhD dissertation). Ghent, Belgium: RU Ghent.
Drent RH, Daan S, 1980. The prudent parent: energetic adjustments in avian breeding. Ardea 68:225-252.[Web of Science]
Gustafsson L, Sutherland WJ, 1988. The cost of reproduction in the collared flycatcher Ficedula albicollis.Nature 335:813-815.[Web of Science]
Harper RG, Juliano SA, Thompson CF, 1994. Intra population variation in hatching synchrony in house wrens: test of the individual-optimization hypothesis. Auk 111 (3):516-524.
Henrich-Gebhardt SG, 1990. Temporal and spatial variation in food availability and its effects on fledgling size in the great tit. In: Population biology of passerine birds, 1st ed (Blondel J, et al. eds). Berlin: Springer;175 -185.
Högstedt G, 1980.
Evolution of clutch size in birds: adaptive variation in relation to territory
quality. Science
210:1148-1150.
Kluyver HN, 1951. The population ecology of the great tit, Parus m. major L. Ardea 39:1-135.
Lessells CM, 1986. Brood size in Canada Geese: a manipulation experiment. J Anim Ecol 55:669-689.
Lessells CM, 1991. The evolution of life histories. In: Behavioural ecology: an evolutionary approach, 3rd ed (Krebs JR, Davies NB, eds). Oxford: Blackwell Scientific;32 -68.
Maigret JL, Murphy MT, 1997. Costs and benefits of
parental care in eastern kingbirds. Behav Ecol
8(3):250-259.
Monaghan P, Nager R, 1997. Why don't birds lay more eggs? Trends Ecol Evol 12:270-274.
Nur N, 1986. Is clutch size variation in the blue tit (Parus caeruleus) adaptive? An experimental study. J Anim Ecol 55:983-999.
Perrins CM, Moss D, 1975. Reproductive rates in the great tit. J Anim Ecol 44:695-706.
Pettifor RA, 1993. Brood-manipulation experiments. 1. The number of offspring surviving per nest in blue tits (Parus caeruleus). J Anim Ecol 62:131-144.
Pettifor RA, Perrins CM, McCleery RH, 1988. Individual optimization of clutch size in great tits. Nature 336:160-162.
Tinbergen JM, Boerlijst MC, 1990. Nestling weight and survival in individual great tits (Parus major). J Anim Ecol 59:1113-1127.
Tinbergen JM, Daan S, 1990. Family planning in the great tit (Parus major): optimal clutch size as integration of parent and offspring fitness. Behaviour 114:161-190.
Van Balen JH, 1973. A comparative study of the breeding ecology of the great tit Parus major in different habitats.Ardea 61:1-93.
van Noordwijk AJ, Müller CB,1994 . On adaptive plasticity in reproductive traits, illustrated with laydate in the great tit and colony inception in a bumble bee. In:Animal societies; individuals, interactions and organisation (Jarman PJ, Rossiter A, eds). Kyoto: Kyoto University Press;180 -194.
Verboven N, 1998. Multiple breeding in a seasonal environment (PhD dissertation). Utrecht: RU Utrecht.
Verboven N, Visser ME, 1998. Seasonal variation in local recruitment of great tits: the importance of being early.Oikos 81:511-524.[Web of Science]
Verhulst S, 1995. Reproductive decisions in great tits: an optimality approach (PhD dissertation). Groningen, the Netherlands: RU Groningen.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Husby, L. E.B. Kruuk, and M. E. Visser Decline in the frequency and benefits of multiple brooding in great tits as a consequence of a changing environment Proc R Soc B, May 22, 2009; 276(1663): 1845 - 1854. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. M. Tinbergen and J. J. Sanz Strong evidence for selection for larger brood size in a great tit population Behav. Ecol., July 1, 2004; 15(4): 525 - 533. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||