Download Birth-sex ratios and local resource competition

Behavioral Ecology Vol. 7 No. 4: 461-464
Birth-sex ratios and local resource competition
in roe deer, Capreolus capreolus
A. J. Mark Hewison* and J. M. Gaillardb
department of Biology, University of Southampton, Southampton, SO9 3TU, UK, and HJniversite
Claude Bernard, Lyon 1, URA CNRS 2055, 43 boulevard du 11 novembre 1918, 69622 Villeurbanne,
France
We investigated variation in the primary sex ratio within and between 14 populations of roe deer (Capreolus capreolus) in
relation to maternal body condition. The sex ratio was increasingly male biased as average maternal body weight decreased.
This relationship did not vary according to the population considered and was not affected by the litter size produced. This
relationship was also apparent within populations. These results indicate that, where environmental conditions are limiting, roe
does tend to produce male-biased litters. Dispersal is more common and occurs at an earlier age among male juveniles in this
species, particularly as density increases and resources become increasingly scarce. Thus, we suggest that where females experience environmental stress, they tend to produce male kids to avoid potential future local resource competition posed by
female offspring. Key words: local resource competition, maternal condition, roe deer, sex ratio. [Behav Ecol 7:461-464 (1996)]
I
f the production of sons and daughters is equally cosdy,
selection should favor a one-to-one ratio of males to females among the offspring of a population (Fisher, 1930).
However, if costs and/or benefits to an individual differ for
production of either sex, this may favor adaptive manipulation
of the birth-sex ratio (invertebrates: Charnov, 1982; mammals:
Clutton-Brock and Iason, 1986). Trivers and Willard (1973)
proposed that in species in which variance in male reproductive success exceeds that of females, additional parental investment would benefit sons more than it would daughters,
provided that offspring reproductive success is determined by
phenotypic quality and that phenotypic quality is in turn determined by the level of maternal care during the juvenile
stage. When these conditions are met, mothers in better-thanaverage condition should invest more heavily in production
of the sex with greatest variation in expected reproductive
success, generally the male. Thus, in the polygynous red deer
(Census elaphus), the birth-sex ratio (male : female) increases
with die dominance rank of the mother (Clutton-Brock et al.,
1984), as relatively larger dominant hinds are able to invest
heavily in male calves, which are dierefore more likely themselves to become dominant and thus gain a disproportionate
number of matings. Further data supporting the Trivers and
Willard hypothesis have been presented for several ungulate
species (e.g., reindeer, Rangifer larandus. Kojola and Eloranta,
1989; mule deer, Odocoileus hemionus. Kucera, 1991; bison,
Bison bison: Rutberg, 1986).
Clark (1978) described a second independent selective
force, resulting from potential for future competition for resources posed by nondispersing progeny. This idea was developed by Silk (1983), describing a situation where females in
poorer-than-average condition should invest in diat sex of offspring more likely to disperse from the natal area, and only
mothers in good condition could afford the postweaning costs
associated with the nondispersing sex. Local resource competition (LRC) has been implicated in sex-ratio variation in
several studies of mammals (Clark, 1978; Cockburn et al.,
A. J. M. Hewison ij now at Institui de Recherche sur les Grands
Mammiferes, INRA, BP 27, Castanet-Tolosan Cedex, F 31326, France.
Received 10 October 1994; revised 23 December 1995; accepted 28
December 1995.
1045-2249/96/$5.00 O 1996 International Society for Behavioral Ecology
1985; Silk, 1983), including some cervids (white-tailed deer,
Odocoileus virginianus. Caley and Nudds, 1987; Verme, 1983;
reindeer: Skogland, 1986).
A further factor that may influence sex-ratio variation is the
relative direct metabolic costs incurred by the mother due to
the demands of gestation and lactation. In sexually dimorphic
species such as red deer, the costs of rearing males are significandy greater than those of rearing females (Clutton-Brock
et al., 1981), and mothers may only do so when in superior
condition, to avoid subsequent impairment of their own reproductive performance (Gomendio et al., 1990). Indeed, for
species that generally produce twins, Williams (1979) suggested a sequence of increasing reproductive cost of one female,
one male, two females, one male plus one female, and two
males due to the higher metabolic expenditure associated
with rearing male offspring.
Studies of sex-ratio variation of particular ungulate species
have often presented data that are not in agreement and that
have contrasting interpretations (white-tailed deer: Caley and
Nudds, 1987; McGinley, 1984; Woolf and Harder, 1979; reindeer: Kojola and Eloranta, 1989; Skogland, 1986; bison: Green
and Rothstein, 1991; Rutberg, 1986). These inconsistencies
may arise because the selection pressures outlined above may
act simultaneously, and the favored strategy will depend on
the relative importance of each within a particular species or
population. This in turn will depend on the level of intrasex
differences in expected reproductive success and philopatry,
as well as the relative metabolic costs to die mother of rearing
either sex. Roe deer present an interesting model in which to
examine the influence of these selection pressures on sexratio variation because substantial polygamy is unlikely (Kurt,
1968; Strandgaard, 1972) and sexual dimorphism is minimal
(Niethammer and Krapp, 1986), but sex-dependent differences in dispersal ofjuveniles have been observed, particularly
at high density (Bideau et al., 1993; Strandgaard, 1972). Here
we report on sex-ratio variation within and between 14 populations of roe deer (Capreolus capreolus) in relation to maternal condition and show that, for this polytocous species,
males and females are interchanged in the sequence of increasing metabolic cost proposed by Williams (1979), indicating females are die cosdier sex to rear when intraspecific competition is high. The LRC hypothesis is die most likely theory
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Behavioral Ecology Vol. 7 No. 4
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Figure 1
Embryo sex ratio (number of
males: females) plotted against
maternal body weight (kg) for
1181 roe deer embryos from
14 populations. Body weight
was divided into units of 2.5
percentiles. The size of each
square is directly proportional
to the sample size for a given
unit. The regression line corresponds to the logistic regression [logit (sex-ratio) = 1.045
(SE = 0.406) - 0.0579 (SE =
0.0250) (body weight)]. This
model fits the data significantly
(X1 = 5.40, df = \,p = .02)
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to explain the significance of sex-ratio manipulation in this
species.
METHODS
Data collection
Data were collected between 1983 and 1990 and consisted of
1181 embryos from culled adult female roe deer (>2 years)
belonging to 14 populations that cover the full geographical
range of this species in Britain. These are free-ranging populations in largely coniferous forests where controlled culling
is the only form of predation. Culling decisions basically conform to a shoot-on-sight policy. Although culling may not be
random, it is unlikely that this introduced any sampling bias
with respect to embryo sex. From each roe doe shot by professional stalkers and deer managers during routine culling
operations, the number and sex of embryos carried was recorded at postmortem. Due to embryonic diapause (Aitken,
1974), roe deer fetuses are not implanted until the end of
December or the beginning ofJanuary and, even at this stage,
are not easily sexed. Therefore, data collection was limited to
the latter hah0 of January and the entire month of February,
after which open season ends. Even with these constraints, it
was not possible to sex a total of 479 fetuses due to their size;
these were not considered in the analysis. Maternal condition
was taken as the eviscerated "clean" body weight, but with
head and feet on. Fecundity (number of embryos per doe)
varied little among animals >2 years old (Hewison, 1993), so
data were pooled for all adults. We examined the tendency to
produce litters biased toward one or other sex in relation to
maternal body weight, both between and within populations.
Data analysis
To test whether the embryo sex ratio (measured as the proportion of males) decreased as maternal condition increased
(i.e., to test for the LRC hypothesis), we first performed a
logistic regression of embryo sex ratio on maternal body
weight We accounted for the possible effects of population
of origin, litter size, and interaction between these factors on
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10
12
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Female Body Mass (Kg)
this relationship by incorporating these parameters as covariables in an ANCOVA-like procedure. To guard against the possibility that heterogeneity among populations might be
masked due to small sample sizes for some populations, we
also fitted a logistic regression on the embryo sex ratio-maternal body weight relationship for each of the 14 populations. We distinguished singleton litters and twin litters and
used sign tests to assess whether within-population sex-ratio
patterns were consistent with the LRC hypothesis.
RESULTS
The embryo sex ratio decreased as maternal condition increased [logit (sex ratio) = 1.045 - 0.0579 (body weight), x2
= 5.40, df = 1, p = .02; Figure 1]. This negative relationship
was not affected by any interaction between litter size and
population (x2 = 17.10, df = 13, p = .20), by litter size (x2
= 1.60, df = 1, p = .20), or by population (x2 = 20.4, df =
13, p = .10). This indicates that the relationship is consistent
across a wide range of environmental conditions (low- and
high-performance populations, small and large litters).
This result was supported by the analysis of within-population sex-ratio variability in relation to maternal body weighL
For litters of one, despite low sample sizes in some populations, in 10 out of 13 populations (data not available for singletons in one population), logistic regression showed that
increasing sex ratio was linked to decreasing maternal body
weight (p = .0349). Similarly, for females that produced twins,
the same pattern was observed in 11 of 14 populations (p =
.0222).
However, maternal condition, as measured by body weight,
varied widely among populations and between litter sizes (twoway ANOVA). Not surprisingly, females with twins were heavier than females with singletons (F = 3.65, df = 14, 1153, p <
.01), but this was particularly pronounced in low body weight
populations, revealed by the significant interaction between
litter size and population in their effects on female body
weight {F = 2.16, df = 13, 1153, p < .05). This combination
of the marked positive effect of litter size on female body
weight when body weight was low, together with the inverse
463
Hewison and Gaillard • Roe deer birth-sex ratios
relationship between embryo sex ratio and maternal body
weight, independent of any effects of litter size or population,
indicates a sequence of one male, one female, two males, two
females with increasing maternal condition. This contrasts
with the sequence proposed by Williams (1979) for dimorphic
species where males are die cosdier sex to rear, but would be
expected under the LRC hypothesis. Thus, it appears that roe
does in populations where resources are limiting (low fecundity rates and low body weights) tend to produce an excess of
male offspring.
DISCUSSION
Roe deer bucks are strongly territorial during the rut (Bramley, 1970; Kurt, 1968; Strandgaard, 1972). Sexual weaponry is
less well-developed and testes are smaller relative to red deer
and other cervids (Clutton-Brock et al., 1982), indicating substantial polygamy probably does not occur (Kurt, 1968). Thus,
an a priori differential between the sexes in expected reproductive success, as observed, for example, in red deer (Clutton-Brock et al., 1984), is unlikely. Furthermore, sexual dimorphism during adulthood is minimal (Niethammer and
Krapp, 1986), timing and synchrony of births are identical
between the sexes (Gaillard et al., 1993c), early growth rates
(during die first mondi of life) do not differ according to sex
(Gaillard et al., 1993b), and both first summer (Gaillard JM,
et al., unpublished data) and first winter survival (Gaillard et
al., 1993a) are similar in males and females. This suggests that
the direct metabolic costs to the mother of rearing either sex
are similar. However, several authors note dispersal is far more
prevalent and occurs earlier among roe bucks than does, particularly at high densities where resources may be limiting (Bideau et al., 1993; Gaillard, 1988; Strandgaard, 1972; Vincent
et al., 1995; Wahlstrom, 1995). Some variation in the primary
sex ratio has previously been reported in roe (Ellenberg,
1978). The data presented here suggest sex-ratio variation in
diis species occurs in response to resource limitation. Where
philopatric offspring pose a direat to subsequent survival and
reproductive performance, does tend to produce male kids to
avoid future LRC. Furthermore, the bias in favor of producing
male offspring increases as habitat quality decreases (see
Chapman et al., 1989). Thus, the relative influence of the
selection pressures acting on sex-ratio variation in roe deer
appears to be different to diat predominating in red deer
(Clutton-Brock et al., 1984; Gomendio et al., 1990), and these
differences can be satisfactorily explained in terms of the particular ecological characteristics of diese species.
Roe deer may be considered the European equivalent of
the North American Odocoileus in terms of die ecology of
these species. In a review of sex-ratio variation from 29 studies
of white-tailed deer and mule deer in North America, Verme
(1983) noted that the proportion of male fawns produced
widiin a population was inversely correlated with average female fecundity, and suggested that this relationship was driven
by differences in diet quality (Verme, 1969). However, in direct contrast, Kucera (1991) found that mule deer mothers
in better-dian-average condition tended to produce male-biased litters, and Woolf and Harder (1979) summarized some
data on white-tailed deer that did not conform to expectations
under Verme's hypothesis. Aldiough in Odocoileus, female juveniles are generally philopatric for a longer period dian are
males (Verme, 1983), die direct metabolic costs of rearing
males are probably higher. Males on average weigh more dian
females as fetuses (mule deer Kucera, 1991) and at birth
(white-tailed deer: McCullough, 1979; mule deen Robinette
et al., 1973), and preweaning nutritional requirements of
male juveniles are higher than diose of females (white-tailed
deen Robbins and Moen, 1975; mule deen Nordan et al.,
1970). Furthermore, aldiough often territorial, white-tailed
deer may become polygynous in open habitats (Hirth, 1977),
introducing sex bias in potential reproductive success. Thus,
die predominant selective forces operating on sex-ratio variation in populations of Odocoileus will depend on die relative
costs and benefits of producing eidier sex imposed by each
of diese factors (see Degayner and Jordan, 1987), and so it
seems diat die effects of LRC are more clearly expressed in
roe deer.
The marked pattern of sex-ratio variation in relation to maternal condition reported here, which was consistent over a
wide range of environmental conditions, may indicate sex-ratio variation is an adaptive trait in roe deer. Aldiough diis
requires confirmation dirough experimental studies, we propose a possible mechanism diat could facilitate die process in
diis species. Implantation of die fertilized blastocyst is delayed
about 5 mondis in roe deer (Aidten, 1974) and may only occur if conditions remain suitable during mid-winter (Hewison,
1993). This delay may also facilitate sex-selective implantation
according to maternal condition at diat time, prior to substantial parental investment. The level of implantation failure
of fertilized blastocysts was estimated as generally approximately 30% but was as high as 60% in one population (Hewison AJM, unpublished data), certainly high enough to produce the observed fetal sex ratios dirough sex-selective implantation. Maynard Smith (1980) showed diat recognition of
offspring sex must occur very early in the investment process
for such a strategy to be selectively favored. The metabolic
costs of ovulation are minimal, particularly when compared
to total maternal investment in an individual progeny, dius
die existence of delayed implantation may explain why LRC
has a strong potential influence on sex-ratio manipulation in
diis species.
Thanks are due to Rory Putman for his assistance and comments and
Jochen Langbein and Nigel Gilles Yoccoz for stimulating discussions,
as well as Phil Ratclifie and all those at the Forestry Commission and
the Ministry of Defence who contributed to the project. The work
was funded by the Science and Engineering Research Council and
the Forestry Commission.
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