Content uploaded by Haitao Wang
Author content
All content in this area was uploaded by Haitao Wang on Oct 05, 2017
Content may be subject to copyright.
Chinese Birds 2010, 1(1):36–44
DOI 10.5122/cbirds.2009.0019
ORIGINAL ARTICLE
Offspring sex ratio in Eurasian Kestrel (Falco tinnunculus)
with reversed sexual size dimorphism
Hui WU 1,2, Haitao WANG 1,3,, Yunlei JIANG 4, Fumin LEI 3, Wei GAO 1
1 School of Life Sciences, Northeast Normal University, Changchun 130024, China
2 Current Address: Thirty-third High School of Baotou, Baotou 014060, China
3 Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
4 Animal’s Scientific and Technological Institute, Agricultural University of Jilin, Changchun 130118,
China
Abstract Fisher’s theory predicts equal sex ratios at the end of parental care if the cost associ-
ated with raising offspring of each sex is equal. However, sex ratios have important evolutionary
consequences and are often biased for many factors. Reported sex ratios are often biased in rap-
tors, which display various degrees of reversed sexual dimorphism, but there seems no consistent
pattern in their offspring sex ratios. In this study, we investigated the offspring sex ratio of the
Eurasian Kestrel (Falco tinnunculus) and tested whether the patterns of biased sex ratios were re-
lated to laying order, egg mass, hatching order, laying date or clutch size. The brood sex ratio of
the Eurasian Kestrel (male) in eggs was 47.0%, not statistically biased from 0.5, but in fledglings
it was 40.8%, significantly biased from 0.5 (p = 0.029). At population level, both primary and sec-
ondary sex ratios did not depart from parity. We found that clutch size and egg mass affected the
secondary brood sex ratio, i.e., the larger the clutch size, the larger the number of males and eggs
producing sons were heavier than eggs producing daughters. Laying date affected both the pri-
mary and secondary sex ratios, and laying earlier is associated with a greater proportion of males.
Keywords Eurasian Kestrel, primary sex ratio, secondary sex ratio, sex dimorphism.
Introduction
Over the past 40 years there have been intensive
theoretical and experimental investigations of how
natural selection moulds the sex ratio. Fisher’s (1930)
classic frequency-dependent model of sex allocation
predicts that the offspring sex ratio should not devi-
ate from parity as long as the costs of producing
males and females are equal. Modern empirical sex
ratio research began when Hamilton (1967) observed
that many insects and mites have highly fe-
male-biased sex ratios and that this trait is associated
with high levels of brother-sister mating. Hamilton
explained this result by his theory of local mate
competition, which has been extended to other cases
of interactions between siblings. Briefly, if one sex
suffers a greater reduction in fitness through compe-
tition with siblings of the same sex, the mother is
programmed in her selection of the sex ratio to favor
the sex that suffers less competition. Fisher’s fre-
quency-dependent argument is thus modified in
populations where relatives compete. A second ma-
jor development was by Trivers and Willard (1973)
who originally proposed that maternal quality should
Received 26 December 2009; accepted 26 February 2010
Author for correspondence (H.T. Wang)
E-mail: wanght402@nenu.edu.cn
H. Wu et al. Offspring sex ratio in Eurasian Kestrel 37
affect the direction of this investment for species,
exhibiting high variation in male reproductive suc-
cess. Modern classic sex allocation theory predicts
that selection should act on parents to
sex-specifically vary the level of investment in off-
spring when the fitness returns differ for the two
sexes (Charnov, 1982; Frank, 1990; Hardy, 2002).
Birds have long been considered incapable of fac-
ultatively shifting their primary sex ratio because
their sex determination is chromosomal (Clut-
ton-Brock, 1986). However, recent studies have
suggested that sex ratio adjustment in birds is not as
constrained as thought earlier (West and Sheldon,
2002). In birds, the sex-ratio adjustment can occur at
laying period (primary sex-ratio adjustment) and
during the period of provisioning for the young
(secondary sex-ratio adjustment) (Ellegren and Shel-
don, 1997; Kilner, 1998).
An increasing number of studies have provided
strong evidence that female birds can adjust the pri-
mary sex-ratio of their offspring by laying sex-biased
clutches (Dijkstra et al., 1990; Heinsohn et al., 1997;
Komdeur et al., 1997, 2002; Kilner, 1998; Nager et
al., 1999; Kalmbach et al., 2001; Rutstein et al.,
2004; Korsten et al., 2006). These studies have
shown that females adjust the sex ratio of their
clutches in relation to potential future fitness gains
(Komdeur et al., 1997; Kalmbach et al., 2001; Rut-
stein et al., 2004), to female body condition (Pike
and Petrie, 2005; Rutkowska and Cichoń, 2006),
attractiveness (Burley, 1981; Ellegren et al., 1996;
West and Sheldon, 2002; Griffith et al., 2003;
Cassey et al., 2006; Korsten et al., 2006; Ferree,
2007) or quality of their mates (Kölliker et al., 1999;
Oddie and Reim, 2002). Also, sex-biased mortality
between hatchings and fledgings has been shown to
further bias towards secondary sex ratios (Torres and
Drummond, 1997; Kilner, 1998; Legge et al., 2001;
Bize et al., 2005; Fargallo et al., 2006).
Mechanisms for both primary and secondary
sex-ratio adjustment in birds remain largely unknown
(Emlen, 1997; Sheldon, 1998; Krackow, 1999; Mar-
tins, 2004), but preovulatory mechanisms have been
suggested as the most efficient means of primary
sex-ratio adjustment for some species (Komdeur et
al., 2002). Pike and Petrie (2003) presented an ex-
cellent review of the potential mechanisms of avian
sex manipulation, such as steroid hormones, paternal
attractiveness, maternal condition, photoperiod and
phenotypic sex and others. In addition, much new
experimental and relevant evidence have appeared
since then, providing new and interesting perspectives
(Pike and Petrie, 2006; Rutkowska and Badyaev,
2008).
Sex allocation patterns among raptor populations
have attracted considerable research attention be-
cause most raptorial birds exhibit reversed sexual
size dimorphism (females are the larger sex) (New-
ton and Marquiss, 1979; Olsen and Cockburn, 1991;
Appleby et al., 1997; Brommer et al., 2003; McDon-
ald et al., 2005). One consequence of this size dif-
ference is a disparity in food requirements: daughters
require more food than sons do during the nestling
period (Anderson et al., 1993a; Krijgsveld et al.,
1998; Riedstra et al., 1998; Laaksonen et al., 2004).
Rearing larger daughters is more costly since they
require more parental investment in the form of food
requirements as opposed to sons. Theoretically, the
offspring sex ratio in raptors should be male-biased.
However, there seems no consistent pattern in the
offspring sex ratios of raptors; the proportion of
males is either increasing (Newton and Marquiss,
1979; Olsent and Cockburn, 1991; Korpimäki et al.,
2000) or decreasing (Tella et al., 1996) and no clear
adaptive explanations for these trends have been
found so far.
The Eurasian Kestrel (Falco tinnunculus), a sexu-
ally size-dimorphic raptor (females ca. 20% heavier
than males; Village, 1990), widespread in open
country throughout the Palearctic, Afrotropical and
Oriental regions (Cramp and Simmons, 1980). A
total of 12 subspecies have been identified (Dickin-
son, 2003). The subspecies in our study is F. tin-
nunculus interstinctus. The female Eurasian Kestrel
might be able to adjust her reproductive effort by
promoting sex differences in the mass of first-laid
eggs (Blanco et al., 2003), where sexual differences
in the size of first-laid eggs defines the pattern of
within-brood mass hierarchies of fledglings. In addi-
tion, some researchers have documented that females
have the potential ability to adjust resources allo-
cated to different-sex eggs laid in varying order
(Anderson et al., 1997; Blanco et al., 2003;
Martínez-Padilla and Fargallo, 2007).
We investigated the primary and secondary off-
spring sex ratio of the Eurasian Kestrel at the Zuojia
Nature Reserve in northeastern China. Our objec-
tives were: 1) to test whether its offspring sex ratio
demonstrates a general deviation from a balanced
sex ratio and 2) whether a pattern of biased sex ratio
exists in relation to laying order, egg mass, hatching
order, laying date and clutch size.
38 Chinese Birds 2010, 1(1):36–44
Study area and methods
Study area
We conducted the study in the Zuojia Nature Re-
serve in Jilin Province, northeastern China during
the breeding seasons (from late March to late July)
in 2007 and 2008. The Zuojia Nature Reserve
stretches from the eastern Changbai mountains to the
western plains (126°1′–127°2′N, 44°6′–45°5′E), where
the elevation ranges from 200 m to 530 m. The re-
gion is subject to an eastern monsoon climate, char-
acterized by hot, dry summers and cold, snowy win-
ters; the area is covered by approximately 35% open
habitat and 65% forests. Vegetation in the area is
diverse and the existing forests are secondary.
Data collection
The Eurasian Kestrels do not build their own nests,
but rely mainly on the stick nests of the Magpie
(Pica pica) in our study area (Xiang et al., 1991;
Deng et al., 2006; Zhou et al., 2009). Most magpie
nests used by the kestrels were inaccessible. We
therefore installed nest boxes to develop the study and
most kestrels then shifted to breed in these boxes.
The nest boxes we used in the study were con-
structed from rough-cut boards and put together with
exterior nails or deck screws. The internal dimen-
sions of the boxes were all the same: 50 cm deep, a
35 cm × 35 cm bottom area and with a 12.5 cm or 15
cm diameter entrance hole near the top. These nest
boxes were placed randomly about 8–13 m above
ground in various tree species with distances ranging
from 50 m to 150 m between the nearest two boxes.
The number of boxes monitored was 68 in 2007 and
77 in 2008.
We monitored nest boxes used by the Eurasian
Kestrels every day to record the laying date and
marked the laying sequence of each egg accurately
during the egg laying period. We used an electronic
balance to weigh eggs to the nearest 0.01 g on the day
of being laid. In order to assign all marked eggs to
their corresponding nestlings, and record the hatching
order, we checked nests hourly (between 08:00 and
19:00 hours) on the days of expected hatching. We
distinguished nestlings by drawing some simple
symbols on their head with indelible ink. We removed
unhatched eggs from the nest after several days when
the rest of the clutch had hatched. We discarded eggs
containing no visible embryos, and stored dead em-
bryos in 100% ethanol. After hatching, we visited
nests at an interval of two days to collect body tis-
sues of the dead nestlings as a source of DNA and to
monitor fledging success. We collected a blood
sample of each nestling (20–50 μL) from brachial
veins with a sterilized hypodermic needle, 9 to 11
days after hatching. We stored blood samples in
EDTA for determination of sex in the laboratory.
Sex determination
We sexed the nestlings using a polymerase chain
reaction (PCR) amplification based on the technique
used by Fridolfsson and Ellegren (1999). We iso-
lated DNA from the red blood cells using proteinase
K digestion and phenol-chloroform extraction. We
ran PCR amplification using a particular set of
primers (2550F and 2718R), as suggested by Fri-
dolfsson and Ellegren (1999). The temperature pro-
file in PCR was as follows: hotstart at 94°C, initial
denaturation at 94°C for 5 min, followed by a
“touch-down” scheme (Don et al., 1991) where the
annealing temperature was lowered 1°C per cycle,
starting from 58°C, until a temperature of 48°C was
reached. Then 25–35 additional cycles were run at a
constant annealing temperature of 48°C. Denatura-
tion was at 94°C for 30 s, annealing for 45 s and
extension at 72°C for 1 min. A final extension step
of 5 min was added after the last cycle. PCR prod-
ucts, separated by electrophoresis on 2% agarose
gels containing ethidium bromide, were visualized
under UV light. We assigned the sex of individuals
from five adult pairs correctly using this technique,
so we could be confident the method worked suc-
cessfully in this species.
Statistics analysis
We used two data sets to analyze the offspring sex
ratio. The data set for analyzing the primary sex ratio
included broods that all laid eggs had hatched suc-
cessfully, including dead embryos. We sampled all
nestlings (both blood and tissue samples) for a total
of 81 nestlings in 15 broods. The data set for ana-
lyzing the secondary sex ratio included 105 nestlings
in 23 successfully fledged broods. We examined the
brood sex ratio (hereafter referred to as the pro-
portion of males) using the binomial test (Zar,
1984). We used the Wilcoxon signed rank test in
S-PLUS 6.0 to test the primary and secondary sex
ratios at population level. In order to study the rela-
H. Wu et al. Offspring sex ratio in Eurasian Kestrel 39
tionship between primary sex ratio, laying order,
clutch size and egg mass, we performed linear mixed
model (LMM) in SPSS 14.0 (SPSS Inc., Chicago,
Illinois, USA). In this model, we entered the sex
ratio as the response variable, clutch size and laying
order as fixed factors. The kestrel hatches asynchro-
nously with a hatching spread of 3–5 days and
therefore we divided the laying order into three
categories: initial, middle and last. The initial cate-
gory corresponded to the first eggs and the last
category to the last eggs. The other eggs were de-
fined as the middle category (Hardy, 2002). Thus,
the sex ratio used in the model stood for the sex ratio
of each category. Moreover, egg mass in the model
also represented the egg mass of each category. We
encoded the laying dates into five stages: March,
early April (April I), middle April (April II), late
April (April III) and May and introduced it as a ran-
dom factor, with egg mass as covariate. By intro-
ducing the laying date as a higher level random ef-
fect in addition to the residual error term, our LMM
permitted an estimation of the fixed effects and in-
teraction parameters while accounting for random
variation in the sex ratio between broods. We ana-
lyzed the relationship between secondary sex ratio,
laying order, clutch size, hatching order and egg
mass using the same model. For all statistical tests,
we used a significance level of 0.05. We presented
values as means ± SD.
Results
Sex ratio at brood and population level
The brood sex ratio of the Eurasian Kestrel in eggs
was 47.0±4.3%, not statistically biased from 0.5
(Wilcoxon signed rank test, Z15 = –0.402, p = 0.342).
However, the brood sex ratio in fledglings was
40.8±4.5%, significantly different from 0.5 (Wil-
coxon signed rank test, Z23 = –1.882, p = 0.029).
The primary sex ratio at population level was
48.2%, which did not depart from parity (binomial
test, n = 81, p = 0.824). The sex ratio in eggs for the
two study years showed a similar pattern (binomial
test, 48.9%, n = 45, p = 1.000 in 2007; 47.2%, n = 36,
p = 0.868 in 2008). The secondary sex ratio at popu-
lation level was 42.9%, which did not depart sig-
nificantly from parity (binomial test, n = 105, p =
0.172). Moreover, we detected the same tendency in
nestlings (binomial test, 41.9%, n = 62, p = 0.253 in
2007; 44.2%, n = 43, p = 0.542 in 2008).
Effect of laying order, egg mass, clutch size on
primary brood sex ratio
The sex ratio of eggs for different categories of lay-
ing order did not differ from parity (binomial tests:
initial, 40.0%, n = 15, p = 0.607; middle, 43.1%, n =
51, p = 0.401; last, 73.3%, n = 15, p = 0.118). Re-
sults of LMM showed that the sex ratio in eggs was
not associated with laying order, clutch size and their
interaction (Table 1). Our results indicate that the
laying date had a significant impact on primary off-
spring sex (Table 1), but there was no significant
correlation (r = –0.025, p = 0.929) (Fig. 1a). Egg
mass did not have a significant effect on primary sex
ratio, but the egg mass of males (23.15±1.36, n = 42)
was slightly heavier than that of females (22.89±1.28,
n = 38), although the difference was not statistically
significant (Mann-Whitney test U = 712, p = 0.407).
In addition, egg mass was not associated linearly
with laying order; the eggs in the middle position in
the laying order were the heaviest (Fig. 2).
Effects of laying order, egg mass, clutch size and
hatching order on secondary brood sex ratio
The secondary brood sex ratio was significantly re-
lated to clutch size (F = 5.297, p = 0.017) and egg
mass (F = 8.099, p = 0.016). With increasing clutch
size and egg mass, the proportion of males became
gradually higher, but there were no significantly
positive correlations (Figs. 3 and 4). Laying order
Table 1 LMM analyses of the effects of clutch size and
laying order on the sex of the eggs in Eurasian Kestrels
Source NDF DDF FNDF, DDF p
Clutch size 3 8 1.570 0.271
Laying order 1 8 0.004 0.951
Egg mass 1 8 1.796 0.217
Clutch size × Laying
order
1 8 0.000 0.983
Covariance parameter
estimates:
Estimate SE Z p
Laying date 0.262 0.130 2.000 0.046
The model accounts for random variation between laying
date. NDF represents the degrees of freedom of the numerator
and DDF that of the denominator. FNDF, DDF stands for Fisher’s
test statistics, p represents the significance level, “estimate”
represents the estimated covariance parameters, SE stands for
standard error, Z represents Z statistic value of the Wald test.
40 Chinese Birds 2010, 1(1):36–44
and hatching order did not have a significant effect
on the proportion of males in fledglings; however,
when they interacted with clutch size, both factors
had a significant effect on the secondary brood sex
ratio (Table 2). In addition, the LMM showed that
laying date had a significant effect on secondary
offspring sex (Table 1), but there was no significant
correlation (r = –0.267, p = 0.218) (Fig. 1b).
Discussion
In this study, the sex ratio at population level and the
primary brood sex ratio did not depart from parity,
which was similar to the result obtained by Ankney
(1982). We found that the secondary brood sex ratio
of Eurasian Kestrels was consistently female-biased
across the two-year study. A number of studies have
shown that females can adjust sex ratio of their off-
spring by adjusting the laying and hatching orders
(Ankney, 1982; Kilner, 1998; Cichoń et al., 2003;
Ležalová et al., 2005). However, our results, as an-
other study (Martínez-Padilla and Fargallo, 2007) on
the species, indicated that the laying order did not
affect the sex ratio of Eurasian Kestrels. Interest-
ingly, our results showed that clutch size and egg
mass only affected secondary brood sex ratio, while
the laying date affected both primary and secondary
sex ratios.
For many bird species, there is no a consistent re-
Fig. 1 Primary sex ratio (a) and secondary sex ratio (b)
of Eurasian Kestrel in relation to laying date
Fig. 2 Relationship between eggs mass and laying order
in Eurasian Kestrel in northeastern China
Fig. 3 Relationship between secondary brood sex ratio
and clutch size in Eurasian Kestrel in northeastern China
Fig. 4 Correlations between secondary brood sex ratio
and egg mass in Eurasian Kestrel in northeastern China
H. Wu et al. Offspring sex ratio in Eurasian Kestrel 41
lationship between egg mass and sex ratio, because
females might adjust egg mass either positively or
negatively to correlate with the laying order in as-
signing resources to different sexual offspring (Fiala,
1981; Ankney, 1982; Bancroft, 1984). Anderson et
al. (1997) suggested that the sex ratio of offspring
was significantly associated with the laying order
and that male eggs were significant larger than fe-
male eggs in the American Kestrel (F. sparverius).
In our study, egg mass had a significant effect on the
secondary brood sex ratio and showed the same pat-
tern as the American Kestrel in spite of a lack of
significant difference between female and male eggs.
Therefore, we speculate that the sexually size-dimorphic
Eurasian Kestrel was able to adjust the sex ratio of
its offspring by adopting different strategies of egg
mass provisioning according to egg sex and laying
order.
Some studies showed that the fledgling sex ratios
of several raptor species are skewed toward males
early in the season while late broods had an excess
of females (Dijkstra et al., 1990; Daan et al., 1996;
Tella et al., 1996; Griggio et al., 2002). In our study,
the laying date had a significant effect on the pri-
mary and secondary brood sex ratios. Moreover,
both sex ratios showed a slightly decreasing trend as
the season progressed in spite of a lack of significant
shift. Eurasian Kestrel nestlings are sexually dimor-
phic, with daughters larger than sons. The larger
daughters may need more foods and have an advan-
tage during sibling competition for food (Anderson
et al., 1993a, 1993b). Sex-specific characteristics of
nestlings may affect the reproductive biology of the
species, while nestling mortality should fall more
heavily on sons than on daughters. We suggest that
the seasonal variation in the sex ratio of the Eurasian
Kestrel might be associated with favouritism for the
male function on the part of the parents, both to
counter the risk of excess mortality of sons and be-
cause sons require less parental care per capita dur-
ing earlier breeding seasons.
A large number of studies show that clutch size
does not affect the sex ratio of birds, except for the
study by Wegge (1980), who indicated that in a de-
clining population of Capercaillie (Tetrao urogallus),
the sex ratio of fledglings declined with clutch size,
but that this was probably a consequence of differen-
tial mortality between hatchings and fledgings. In
our study, clutch size had a significant effect on the
secondary sex ratio in spite of a lack of significant
correlation. The highest male proportion occurred
with a clutch size of seven, with the highest prob-
ability of mortality of hatchings from the seventh
egg. Two potential reasons may explain this conclu-
sion. First, we found that the Eurasian Kestrel, bred
in an artificial nest box, had a larger clutch size than
kestrels bred in natural nests (5.77±0.15 vs 4.86±
0.26), where clutch size of the species was not more
than 6 in natural nests (W. Gao unpublished data).
As a result, it was difficult for the parents to rear all
the nestlings in this condition. We therefore consid-
ered that the kestrel may adopt a “brood reduction
strategy” in order to adjust the secondary brood sex
ratio (Slagsvold et al., 1984). Secondly, food avail-
ability might also constrain the survival rate of nes-
tlings. Kestrels feed mainly on small mammals, es-
pecially voles, but birds, frogs and insects also form
part of their diet during the nestling period, which
might reflect a reduced availability of rodents due to
their being preyed upon continuously by the kestrels
and several other raptor species in the study area
(Geng et al., 2009).
Our results revealed relatively complex patterns of
sex allocation in the Eurasian Kestrel that appears to
be associated with both maternal ability to modify
the sex of the progeny by adapting to its environ-
ment. Future work on the kestrel should include ex-
Table 2 LMM analyses of the effects of clutch size, laying
order and hatching order on the sex of the fledgings in Eura-
sian Kestrel
Source NDF DDF FNDF, DDF p
Clutch size 3 11 5.297 0.017
Laying order 1 11 0.851 0.376
Hatching order 1 11 0.128 0.728
Egg mass 1 11 8.099 0.016
Clutch size × Laying
order
1 11 6.447 0.028
Clutch size × Hatching
order
1 11 5.508 0.039
Covariance parameter
estimates:
Estimate SE Z p
Laying date 0.194 0.008 2.345 0.019
The model accounts for random variation between laying
date. NDF is the degree of freedom of the numerator and DDF
of the denominator, FNDF, DDF is Fisher’s test statistic, p repre-
sents significance level, “estimate” represents the estimated
covariance parameters, SE stands for standard error, and Z
represents the Z statistic value of the Wald test.
42 Chinese Birds 2010, 1(1):36–44
periments that evaluate the ultimate mechanism of
sex ratio allocation and parental provisioning pat-
terns to different sex eggs with egg mass, adjusting
for reproductive efforts.
Acknowledgements This work was supported by the Na-
tional Natural Science Foundation of China (Grant No.
30400047), the Training Fund of Northeast Normal University
Scientific Innovation Project (Grant No. 07013) and the Jilin
Provincial Science and Technology Department (Grant No.
20070558 and 20090575). The authors thank Shi Jiao, Bo Qin
and Yufang Qin for assistance in the field and anonymous
reviewers for providing comments to improve the manuscript.
References
Anderson DJ, Budde C, Apanius V, Gomez JEM, Bird DM,
Weathers WW. 1993a. Prey size influences female com-
petitive dominance in nestling American kestrels. Ecology,
74:367–376
Anderson DJ, Reeve J, Bird DM. 1997. Sexually dimorphic
eggs, nestling growth and sibling competition in American
Kestrels (Falco sparverius). Funct Ecol, 11:331–335
Anderson DJ, Reeve J, Gomez JEM, Weathers WW, Hutson S,
Cunningham HV, Bird DM. 1993b. Sexual size dimor-
phism and food requirements of nestling birds. Can J Zool,
71: 2541–2545
Ankney CD. 1982. Sex ratio varies with egg sequence in
Lesser Snow Geese. Auk, 99:662–666
Appleby BM, Petty SJ, Blakey JK, Raieny P, Macdonald DW.
1997. Does variation of sex ratio enhance reproductive
success of offspring in Tawny Owls (Strix aluco). Proc R
Soc B, 264:1111–1116
Bancroft GT. 1984. Patterns of variation in size of Boat-tailed
Grackle (Quiscalus major) eggs. Ibis, 126:496–509
Bize P, Roulin A, Telia JL, Richner H. 2005. Female-biased
mortality in experimentally parasitized Alpine Swift (Apus
melba) nestlings. Funct Ecol, 19:405–413
Blanco G, Martínez-Padilla J, Serrano D, Dávila JA, Viñuela
J. 2003. Mass provisioning to different-sex eggs within the
laying sequence: Consequences for adjustment of reproduc-
tive effort in a sexually dimorphic bird. J Anim Ecol, 72:
831–838
Brommer JE, Karell P, Pihlaja T, Painter JN, Primmer CR,
Pietiäinen H. 2003. Ural Owl sex allocation and parental
investment under poor food conditions. Oecologia, 137:
140–147
Burley N. 1981. Sex ratio manipulation and selection for
attractiveness. Science, 211:721–722
Cassey P, Ewen JG, Møller AP. 2006. Revised evidence for
facultative sex ratio adjustment in birds: a correction. Proc
R Soc B, 273:3129–3130
Charnov EL. 1982. The theory of sex allocation. Monogr
Popul Biol, 18:1–355
Cichoń M, Dubiec A, Stoczke M. 2003. Laying order and
offspring sex in blue tits Parus caeruleus. J Avian Biol, 34:
355–359
Clutton-Brock TH. 1986. Sex ratio variation in birds. Ibis, 128:
317–329
Cramp S, Simmons KEL. 1980. Handbook of the Birds of
Europe, the Middle East and North Africa. Oxford Univer-
sity Press, Oxford
Daan S, Dijkstra C, Weissing FJ. 1996. An evolutionary ex-
planation for seasonal trends in avian sex ratios. Behav
Ecol, 7:426–430
Deng QX, Gao W, Yang YL, Zhou T. 2006. The role of mag-
pie in formed bird community organism in secondary forest.
J Northeast Normal Univ, 38:101–104 (in Chinese)
Dickinson EC. 2003. The Howard and Moor Complete
Checklist of the Birds of the World. 3rd ed. Princeton Uni-
versity Press, Princeton
Dijkstra C, Daan S, Buker JB. 1990. Adaptive seasonal varia-
tion in the sex ratio of kestrel broods. Funct Ecol, 4:143–
147
Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS. 1991.
‘Touchdown’ PCR to circumvent spurious priming during
gene amplification. Nucl Acids Res, 19:4008
Ellegren H, Gustafsson L, Sheldon BC. 1996. Sex ratio ad-
justment in relation to paternal attractiveness in a wild bird
population. Proc Natl Acad Sci USA, 15:11723–11728
Ellegren H, Sheldon BC. 1997. New tools for sex identifica-
tion and the study of sex allocation in birds. Trends Ecol
Evol, 12:255–259
Emlen ST. 1997. When mothers prefer daughters over sons.
Trends Ecol Evol, 12:291–292
Fargallo JA, Polo V, De Neve L, Martin J, Davila JA, Soler M.
2006. Hatching order and size-dependent mortality in rela-
tion to brood sex ratio composition in chinstrap penguins.
Behav Ecol, 17:772–778
Ferree ED. 2007. White tail plumage and brood sex ratio in
Dark-eyed Juncos (Junco hyemalis thurberi). Behav Ecol
Sociobiol, 62:109–117
Fiala KL. 1981. Sex ratio constancy in the red-winged black-
bird. Evolution, 35:898–910
Fisher R. 1930. The Genetical Theory of Natural Selection.
Oxford University Press, London
Frank SA. 1990. Sex allocation theory for birds and mammals.
Annu Rev Ecol Syst, 21:13–56
Fridolfsson AK, Ellegren H. 1999. A simple and universal
method for molecular sexing of non-ratite birds. J Avian
Biol, 30:116–121
Geng R, Zhang XJ, Ou W, Sun HM, Lei FM, Gao W, Wang
H. Wu et al. Offspring sex ratio in Eurasian Kestrel 43
HT. 2009. Diet and prey consumption of breeding Common
Kestrel (Falco tinnunculus) in Northeast China. Prog Nat
Sci, 19:1501–1507
Griffith SC, Örnborg J, Russell AF, Andersson S, Sheldon BC.
2003. Correlations between ultraviolet coloration, overwin-
ter survival and offspring sex ratio in the Blue Tit. J Evol
Biol, 16:1045–1054
Griggio M, Hamerstrom F, Rosenfield R N, Tavecchia G.
2002. Seasonal variation in sex ratio of fledgling American
Kestrels: A long term study. Wilson Bull, 114:474–478
Hamilton WD. 1967. Extraordinary sex ratios. Science, 156:
477–488
Hardy ICW. 2002. Sex Ratios: Concepts and Methods. Cam-
bridge University Press, Cambridge
Heinsohn R, Legge S, Barry S. 1997. Extreme bias in sex
allocation in Eclectus parrots. Proc R Soc Lond B, 264:
1325–1329
Howe HF. 1977. Sex ratio adjustment in the Common Grackle.
Science, 198: 744–745
Kalmbach E, Nager RG, Griffiths R, Furenss RW. 2001. In-
creased reproductive effort results in male-biased offspring
sex ratio: an experimental study in a species with reversed
sexual size dimorphism. Proc R Soc B, 268:2175–2179
Kilner R. 1998. Primary and secondary sex ratio manipulation
by Zebra Finches. Anim Behav, 56:155–164
Kölliker M, Heeb P, Werner I, Mateman AC, Lessells CM,
Richner H. 1999. Offspring sex ratio is related to male body
size in the great tit (Parus major). Behav Ecol, 10:68–72
Komdeur J, Daan S, Tinbergen JM, Mateman AC. 1997. Ex-
treme adaptive modification in sex ratio of the Seychelles
warbler’s eggs. Nature, 385:522–526
Komdeur J, Magrath MJL, Krackow S. 2002. Pre-ovulation
control of hatchling sex ratio in the Seychelles Warbler.
Proc R Soc B, 269:1067–1072
Korpimäki E, May CA, Parkin DT, Wetton JH, Wiehn J. 2000.
Environmental- and parental condition-related variation in
sex ratio of kestrel broods. J Avian Biol, 31:128–134
Korsten P, Lessells CM, Mateman AC, van der Velde M,
Komdeur J. 2006. Primary sex ratio adjustment to experi-
mentally reduced male UV attractiveness in blue tits. Behav
Ecol, 17:539–546
Krackow S. 1999. Avian sex ratio distortions: the myth of
maternal control. Proc Int Ornithol Congr, 22:425–433
Krijgsveld KL, Daan S, Dijkstra C, Visser GH. 1998. Energy
requirements for growth in relation to sexual size dimor-
phism in Marsh Harrier (Circus aeruginosus) nestlings.
Physiol Biochem Zool, 71:693–702
Laaksonen T, Fargallo JA, Korpimäki E, Lyytinen S,
Valkama J, Pöyri V. 2004. Year- and sex-dependent effects
of experimental brood sex ratio manipulation on fledging
condition of Eurasian kestrels. J Anim Ecol, 73:342–352
Ležalová R, Tkadlec E, Obornák M, Šimek J, Honza M. 2005.
Should males come first? The relationship between off-
spring hatching order and sex in the Black-headed Gull
(Larus ridibundus). J Avian Biol, 36:478–483
Legge S, Heinsohn R, Double MC, Griffiths R, Cockburn A.
2001. Complex sex allocation in the Laughing Kookaburra.
Behav Ecol, 12:524–533
Martínez-Padilla J, Fargallo JA. 2007. Food supply during
prelaying period modifies the sex-dependent investment in
eggs of Eurasian Kestrels. Behav Ecol Sociobiol, 61:1735–
1742
Martins TLF. 2004. Sex-specific growth rates in zebra finch
nestlings: a possible mechanism for sex ratio adjustment.
Behav Ecol, 15:174–180
McDonald PG, Olsen PD, Cockburn A. 2005. Sex allocation
and nestling survival in a dimorphic raptor: does size matter?
Behav Ecol, 16:922–930
Nager RG, Monagham P, Griffiths R, Houston DC, Dawson R.
1999. Experimental demonstration that offspring sex ratio
varies with maternal condition. Proc Natl Acad Sci USA,
96:570–573
Newton I, Marquiss M. 1979. Sex ratio among nestlings of the
European sparrowhawk. Am Nat, 113:309–315
Oddie KR, Reim C. 2002. Egg sex ratio and paternal traits:
using within-individual comparisons. Behav Ecol, 13:503–
510
Olsent PD, Cockburn A. 1991. Female-biased sex allocation
in Peregrine Falcons and other raptors. Behav Ecol Socio-
biol, 28:417–428
Pike TW, Petrie M. 2003. Potential mechanisms of avian sex
manipulation. Biol Rev, 78:553–574
Pike TW, Petrie M. 2005. Maternal body condition and
plasma hormones affect offspring sex ratio in peafowl.
Anim Behav, 70:745–751
Pike TW, Petrie M. 2006. Experimental evidence that corti-
costerone affects offspring sex ratios in quail. Proc R Soc B,
273:1093–1098
Riedstra B, Dijkstra C, Daan S. 1998. Daily energy expendi-
ture of male and female marsh harrier nestlings. Auk, 115:
635–641
Rutkowska J, Badyaev AV. 2008. Meiotic drive and sex de-
termination: molecular and cytological mechanisms of sex
ratio adjustment in birds. Philos T R Soc B, 363:1675–1686
Rutkowska J, Cichoń M. 2006. Maternal testosterone affects
the primary sex ratio and offspring survival in Zebra
Finches. Anim Behav, 71:1283–1288
Rutstein AN, Slater PJB, Graves JA. 2004. Diet quality and
resource allocation in the zebra finch. Proc R Soc Lond B,
271(Suppl.):286–289
Sheldon BC. 1998. Recent studies of avian sex ratios. Hered-
ity, 80:397–402
44 Chinese Birds 2010, 1(1):36–44
Slagsvold T, Sandvik J, Rofstad G, Husby M. 1984. On the
adaptive value of intraclutch egg-size variation in birds.
Auk, 101:685–697
Tella JL, Donazar JA, Negro JJ, Hiraldo F. 1996. Seasonal
and interannual variations in the sex-ratio of Lesser Kestrel
(Falco naumanni) broods. Ibis, 138:342–345
Torres R, Drummond H. 1997. Female-biased mortality in
nestlings of a bird with size dimorphism. J Anim Ecol, 66:
859–865
Trivers RL, Willard DE. 1973. Natural selection of parental
ability to vary the sex ratio of offspring. Science, 179:90–
92
Village A. 1990. The Kestrel. Poyser, London
Wegge P. 1980. Distorted sex ratio among small broods in a
declining Capercaillie population. Ornis Scand, 11:106–109
West SA, Sheldon BC. 2002. Constraints in the evolution of
sex ratio adjustment. Science, 295:1685–1688
Xiang GQ, Gao W, Feng HL. 1991. The study on breeding
ecology of European Magpie (Pica pica). In: Gao W (ed)
Chinese Bird Study. Chinese Science Press, Beijing, pp
102–106 (in Chinese)
Zar JH. 1984. Biostatistical Analysis. Prentice Hall, Engle-
wood
Zhou T, Wang HT, Liu Y, Lei FM, Gao W. 2009. Patterns of
magpie nest utilization by a nesting raptor community in a
secondary forest. Prog Nat Sci, 19:1253–1259
两性异型红隼的子代性比研究
吴慧 1,2,王海涛 1,3,姜云垒 4,雷富民 3,高玮 1
(1东北师范大学生命科学学院,长春,130024; 2 包头市第三十三中学,包头,014060;
3 中国科学院动物研究所,北京,100101; 4 吉林农业大学动物科学学院,长春,130118)
摘要:Fisher经典的性比分配理论预测:如果双亲繁殖雄性和雌性子代的代价相同,那么子代的性比
应趋于平衡。然而,性比组成是长期进化的结果,常因不同因素的影响而出现偏离。文献报道猛禽由
于存在不同形式的两性异型现象而导致子代性比常出现偏离,但子代性比偏离方向因种而异。本研究
中我们对红隼(Falco tinnunculus)子代的性比组成进行了调查,目的是检验红隼子代性比是否受产卵
日期、产卵顺序、卵重、出雏顺序或窝卵数影响。在窝水平上,红隼(雄性)的初级性比为47.0%,
没有偏离0.5,但次级性比为40.8%,显著偏离0.5(p = 0.029)。在种群水平上,初级性比和次级性比
都没有出现偏离。窝卵数和卵重影响红隼的次级性比组成,窝卵数越大,雄性后代数量越多,且发育
为雄性后代的卵重较发育为雌性后代的重。初级性比和次级性比都受到产卵日期的影响,产卵越早,
雄性后代比例越高。
关键词:红隼,初级性比,次级性比,两性异型