SEXUAL SEGREGATION IN UNGULATES:
NEW DIRECTIONS FOR RESEARCH
MARTIN B. MAIN, FLOYD
W
WECKERLY, AND VERNON
C.
BLEICH
Department of Fisheries and Wildlife, Oregon State University,
Corvallis, OR 97331 (MBM)
Department of Mathematics, Humboldt State University, Arcata, CA 95521 (FWW)
California Department of Fish and Game, 407 West Line Street,
Bishop, CA 93514 (VCB)
Present address of MBM: Southwest Florida Research and Education Center,
University of Florida, P.D. Drawer 5127, Immokalee, FL 33934-9716
We reviewed the literature on sexual segregation in polygynous ungulates in an effort to
clarify terms and concepts, summarize recent information that supports or discredits three
broadly defined hypotheses, and suggest directions for future research that should help
resolve when and why the sexes segregate in these large mammals. The hypotheses discussed include those based on intersexual differences in energetics and security (reproductive-strategy hypothesis), body size dimorphism and dietary requirements (sexual dimorphism-body size hypothesis), and social mechanisms (social-factors hypothesis). These hypotheses represent ecological, physiological, and social perspectives and are not mutually
exclusive. Most evidence reviewed supported the reproductive-strategy hypothesis. Less
support was available for either the sexual dimorphism-body size hypothesis or the socialfactors hypothesis. Nonetheless, most available evidence is provided by field studies that
contend with many confounding variables. We suggest several areas of future study that
may serve as critical tests and are likely to be productive in resolving why sexual segregation occurs in polygynous ungulates.
Key words:
lates
Bovidae, Cervidae, literature review, Ruminantia, sexual segregation, ungu-
ungulates (Table 1). These hypotheses are
not necessarily mutually exclusive and include explanations based on intersexual differences in reproductive strategy as they relate to energetics and security of offspring
(Bleich, 1993; Clutton-Brock et aI., 1987;
Main and Coblentz, 1990, in press; Miquelle
et aI., 1992), body size dimorphism and dietary requirements (Beier, 1987; Beier and
McCullough, 1990; Bowyer, 1984; McCullough et aI., 1989; Miquelle et aI., 1992;
Weckerly, 1993), and social mechanisms,
such as intersexual aggression (Ozoga et aI.,
1982) and the need for males to evaluate
potential rivals, develop fighting skills, and
establish dominance relationships (Beier and
McCullough, 1990; Geist, 1982; McCullough, 1979; Verme, 1988).
Much attention has been devoted to understanding sexual segregation in ungulates,
particularly among the Ruminantia (Bleich,
1993; Main and Coblentz, 1990; Miquelle
et aI., 1992; Weckerly, 1993). Sexual segregation occurs where males and females
live separately outside rut and is pronounced in wild, north-temperate cervids
(Beier, 1987; Clutton-Brock et aI., 1982)
and bovids (Festa-Bianchet, 1988; Shank,
1982), and also has been reported among
free-ranging feral livestock (Berteaux,
1993).
Based on a review of the literature, we
identified three broadly defined hypotheses
that have received the most support and
which we believe have the greatest potential
to explain sexual segregation in polygynous
Journal of Mammalogy. 77(2):449-461, 1996
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TABLE I.-The three most common hypotheses proposed to explain sexual segregation among
ungulates. Brief explanations and critical predictions are provided for each hypothesis. Potential
critical tests are discussed in the text.
I. Reproductive-strategy hypothesis
Explanation.-Ecological factors are largely responsible for sexual segregation. Because reproductive success
of males appears to be influenced by size, strength, and endurance, selective pressures favor behaviors that
maximize rates of growth and formation of energy reserves. Because reproductive success of females is determined by survival of offspring, selective pressures favor behaviors that reduce risk of predation and satisfy
requirements of offspring while providing those resources necessary for lactation and survival of females.
Predictions.-Males exploit areas where nutritious resources are abundant in all seasons, excluding rut. Males
avoid areas of high density of females when feeding pressure of females reduces the availability of preferred
forage below that found elsewhere. Females occupy areas that provide predictable sources of food and water
(for species that require free water) during parturition and lactation, and that increase security to offspring
during periods when offspring are highly vulnerable to predation. Sexual segregation is most pronounced during
periods when offspring are highly vulnerable and movement patterns of females are restricted to areas that
provide security and requisite resources for offspring.
2. Sexual dimorphism-body size hypothesis
Explanation.-Physiological factors related to nutrition are largely responsible for sexual segregation. Sexual
segregation is a reflection of each sex sequestering resources that satisfy their different physiological requirements. Larger males, with greater absolute metabolic requirements, feed on abundant, high-fiber forages and
retain digesta longer to improve efficiency of digestion. Smaller-bodied females selectively feed on low-fiber,
high-quality forages to satisfy nutritional demands of gestation and lactation.
Predictions.-Larger-bodied males are able to meet nutritional requirements by exploiting abundant, low-quality
forage and demonstrate preference for low-quality feed when higher-quality forage is available. Females require
high-quality feed to satisfy nutritional demands of gestation and lactation and exploit areas with greater biomass
of high-quality forages per capita than available in areas exploited by males. Sexual segregation is most
pronounced when differences in the spatial distribution of high- and low-quality forages are greatest.
3. Social-factors hypothesis
Explanation.-Social factors are largely responsible for sexual segregation and reflect the need for sexes to
segregate to learn important skills. This hypothesis is generally interpreted in terms of factors related to mating
success of males, such as the need for males to develop fighting skills, establish pre-rut dominance hierarchies,
and, in those areas where males and females demonstrate spatial overlap, learn the location of potential mates.
The hypothesis that sexual segregation is the product of aggressive behavior of females toward males also is
included in this category. Learned skills, such as where to find food, water, and suitable birthing areas are
presumed benefits of sexual segregation, but represent explanations that are functionally the same as provided
by the reproductive-strategy hypothesis.
Predictions.-Pre-rut dominance relationships between similar-sized males are reliable predictors of victory
during contests for mates. Where spatial overlap occurs between males and females, home ranges of males do
not change significantly during rut unless home ranges of females also change. If sexual segregation is the
product of aggression of females toward males, then females should be aggressive and dominant to mature
males throughout the period when sexual segregation occurs.
In addition to the debate as to what
drives sexual segregation, there has been
confusion as to what actually constitutes
sexual segregation. Must the sexes use spatially exclusive areas (Tierson et aI., 1985)
or does the formation of separate social
groups by each sex also constitute sexual
segregation when both sexes exhibit broad,
spatial-temporal overlap in their use of areas (Bowyer et aI., in press; McCullough et
aI., 1989)? Consequently, there exists a
need to define what constitutes sexual segregation as well as why and when the sexes
segregate. The objectives of this paper are
to clarify some terms and concepts concerning sexual segregation, review recent
information in terms of support for or
against three broadly defined hypotheses
proposed to explain sexual segregation in
polygynous ungulates, and suggest critical
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MAIN ET AL.-SEXUAL SEGREGATION IN UNGULATES
tests for future research that should help resolve why and when the sexes segregate in
polygynous ungulates.
DISCUSSION
Definition of sexual segregation.-In polygynous ungulates, sexual segregation
likely is influenced by social, spatial, and
temporal factors such as the periodicity of
mating opportunities, population densities,
resource distribution, and environmental
conditions. Species with prolonged mating
periods, such as African buffalo (Syncerus
caffer), exhibit mixing of adults of both
sexes more or less throughout the year
(Prins, 1989). Mixed-sex groups generally
occur less frequently outside rut in northtemperate species with relatively short, seasonal periods of mating (Bleich, 1993;
Bowyer, 1984; Clutton-Brock et aI., 1982;
Main, 1994), except when harsh winter
conditions or concentrated, localized abundance of forage causes animals to congregate (Marchinton and Hirth, 1984).
Sexual segregation has been reported in
both heterogeneous and homogeneous habitats and may result in either pronounced or
subtle differences in spatial distribution between sexes. In highly heterogeneous environments where requisite or favored resources are patchily distributed, differences
in spatial distribution tend to be pronounced
(Festa-Bianchet, 1988). In environments
where suitable habitat for both sexes is continuously or widely distributed, differences
in spatial distribution may be less obvious
(McCullough et aI., 1989; Weckerly, 1993),
particularly at high population densities
(Main, 1994).
Differences in spatial distribution typically have been demonstrated with indices
of overlap or by calculating the overlap of
observations of males and females in landscape cells of a particular size (Bowyer,
1984; Bowyer et aI., in press; CluttonBrock et aI., 1982; Main, 1994; Miquelle et
aI., 1992). Subtle differences in spatial distribution, however, may be difficult to detect depending upon the scale used in de-
451
fining sizes of cells or accuracy of researchers in identifying locations of animals and
delineating home ranges. Bowyer et aI. (in
press) reported that the size of the sampling
unit had considerable effects upon degree
of sexual segregation measured in blacktailed deer (Odocoileus hemionus) and concluded that failure to consider scale holds
the potential to misinterpret data.
Sexual segregation, therefore, is a behavioral pattern that may occur at different
scales under different ecological scenarios.
Documentation of this behavioral pattern
requires the measurement of both social and
spatial components within a temporal (seasonal) framework. A temporal framework is
necessary to place behavioral patterns in
context with reproductive and environmental variables. Only in this way can the patterns of sexual segregation observed among
different species and even different populations of the same species be compared
with predictions of hypotheses.
When should the sexes segregate?-If
sexual segregation confers advantages to reproductive success via improvements in
physical condition, then sexual segregation
should be most pronounced during those
periods when physical condition is most influenced by choice of habitat and when requirements influencing reproductive success differ most between sexes. For most
ungulates, this occurs during spring-summer when males are replenishing energy
stores in preparation for rut (Mautz, 1978),
and females are giving birth, lactating, and
raising offspring. Nonetheless, sexual segregation also may occur during winter as
males attempt to recover physical condition
lost during rut (Shank, 1982; Staines et aI.,
1982). For instance, Miquelle et aI. (1992)
reported that sexual segregation was most
pronounced during winter for moose (Alces
alces) residing in Alaska. Alternatively, if
social factors are responsible for producing
sexual segregation, then sexual segregation
should be most pronounced during periods
when intrasexual social interaction has the
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greatest potential influence on reproductive
success such as immediately prior to rut.
Species-specific or common impetus?-If
the underlying causes for sexual segregation are similar, variation reported by numerous studies regarding when and to what
extent sexual segregation occurs may reflect
the effects of different habitats, mating patterns, and other factors. We recognize the
risk that an all-encompassing explanation of
sexual segregation may be misleading at
this stage of understanding and may fail to
encompass potential benefits of this behavior to each gender. Conversely, the universal nature of sexual segregation among polygynous ungulates suggests this behavior
is the product of selective pressures from a
similar evolutionary background. Because
species- or area-specific explanations of intersexual requirements for habitat may falter when compared across taxa or in different environments, we contend that it may
be more profitable to attempt to understand
sexual segregation in terms of selective
pressures that influence reproductive success across taxa rather than to concentrate
solely on separate species- or site-specific
explanations.
Reproductive-strategy hypothesis.-Main
and Coblentz (1990) reviewed the literature
and argued that polygynous male ungulates
engage in foraging and behavioral patterns
that maximize body condition before rut,
even when these behaviors increase risks of
predation. Conversely, females opt for maximizing security of offspring as long as resource requirements are satisfied, even
when security decisions preclude optimalforaging behaviors (i.e., the satisficing concept described by Bunnell and Gillingham,
1985). This hypothesis is based on ecological criteria for lifetime reproductive success; males need to compete successfully
for mates, whereas females need to raise
offspring successfully. Hence, this hypothesis predicts that males will maximize energy reserves and growth rates by exploiting areas with abundant, high-quality forage or, at least, modify foraging behaviors
Vol. 77, No.2
to avoid those areas where foraging is less
productive. Conversely, females should act
to promote security and survival of offspring through use of habitats with characteristics such as increased protective cover, escape terrain, reduced activity of predators, and adequate availability of food and
water.
Support for this hypothesis has been provided by recent field studies that have identified greater quantities of high-quality forage in habitats used by males and greater
security from predation in habitats used by
females and offspring for African buffalo
(Prins and Iason, 1989), mountain sheep
(Ovis canadensis-Berger, 1991; Bleich,
1993; Festa-Bianchet, 1988), caribou (Rangifer tarandus-Bergerud et aI., 1984),
huemel (Hippocamelus bisulcus-Frid,
1994), mule deer (Odocoileus hemionusMain and Coblentz, in press), moose (Mique lIe et aI., 1992), and red deer (Cervus
elaphus-Clutton-Brock et aI., 1987). Additionally, Koga and Ono (1994) determined that male sika deer (Cervus nippon)
consumed higher-quality diets than did females during winter, and LaGory et aI.
(1991) reported that male white-tailed deer
(Odocoileus virginianus) frequented open
pastures more and obtained diets of higherquality than did females during May-November. Komers et aI. (1993) reported that
female wood bison (Bison bison) with
young formed nursery groups that were
segregated from solitary males, male
groups, and mixed-sex groups that contained females without young. Komers et
aI. (1993) suggested the increased ratio of
offspring to adults in nursery groups may
reduce risk of predation to individual offspring through dilution effects (Wrona and
Dixon, 1991). Thus, the formation of nursery groups of bison in a homogeneous prairie environment may represent females
seeking areas (nursery groups) that increase
security to offspring, roughly analogous to
the selection of habitats with characteristics
that increase security of offspring by females in heterogeneous environments.
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MAIN ET AL.-SEXUAL SEGREGATION IN UNGULATES
In contrast to predictions of the reproductive-strategy hypothesis, studies have
reported that females occupied superior
habitats based on physiographic characteristics (Shank, 1985; Watson and Staines,
1978) or obtained higher-quality diets than
did males, particularly during winter (Beier,
1987; Beier and McCullough, 1990). Nonetheless, conclusions of superior foraging
opportunities based on physiographic characteristics rather than actual measures of
nutritional parameters or available biomass
of forage may be misleading. Even when
females occupy potentially superior habitat,
males may still be foraging in an optimal
manner if feeding activity by females reduces the availability of preferred forage in
these areas or if greater mobility of males
results in higher rates of encounter with unexploited foods (Charnov, 1976). For example, females often use smaller home
ranges and demonstrate stronger site fidelity
(Beier and McCullough, 1990; Brown,
1992; Main, 1994; Weckerly, 1993), or occur in higher densities (Bowyer, 1984) than
do males. These patterns concentrate feeding efforts over smaller areas, particularly
during periods when offspring restrict
movements of females (Becker and Ginsberg, 1990; McCullough et aI., 1989) and
energy demands are dramatically elevated
by lactation (Sadlier, 1982). Consequently,
groups of females may reduce the availability of preferred forage such that males
do better by seeking forage elsewhere. Support for this argument was provided by
Clutton-Brock et ai. (1987), who concluded
that differences in gender in use of habitats
by red deer were related to grazing pressure
by groups of females and reduced tolerance
of low standing crops of grass by males.
Main and Coblentz (in press) reached similar conclusions for mule deer in eastern Oregon where the biomass of forbs, the dominant component (ca. 80%) in the diets of
both sexes, was significantly lower at feeding sites of females compared with males,
despite generally more mesic habitat where
females occurred. Additional support that
453
males may maximize foraging opportunities
by avoiding competition from groups of females was provided by observed improvement in physical condition of male African
buffalos after segregating from herds of females and their offspring (Prins, 1989).
Greater foraging mobility of males also was
implicated as a factor that improved survival of males during periods of food shortage
in populations of both African elephant
(Loxodonta aJricana-Corfield, 1973) and
feral cattle (Bos taurus-Berteaux, 1993)
because female-offspring groups, which
were restricted in their movement and feeding patterns to those areas near water, depleted local food supplies and suffered
higher rates of mortality from starvation.
The influence of water on the distribution
of females with young has been demonstrated for other species as well (Becker and
Ginsberg, 1990; Bowyer, 1984; Main,
1994).
Although scramble competition for forage may influence sexual segregation when
males avoid potentially superior habitat occupied by females, it is inappropriate to assume competition operates under all scenarios. For example, Miquelle et ai. (1992)
rejected scramble competition as an explanation for sexual segregation in a low-density population of moose in Alaska where
males consistently occupied habitats with
greater biomass of forage than did females.
Miquelle et ai. (1992) concluded that female moose occupied habitats with lower
biomass of forage because these areas increased security of offspring from predation. Although Miquelle et ai. (1992) acknowledged that competition may potentially influence sexual segregation under
certain conditions, it was not necessary to
explain sexual segregation in their study.
What constitutes resource limitation for
males is uncertain, but we do know that
mating opportunities are positively correlated with body size and condition in male
ungulates (Clutton-Brock, 1983; CluttonBrock et aI., 1982; Ralls, 1977). Hence, selection may favor males that maximize
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weight gain by ranging over large areas and
encountering unexploited food patches
(Charnov, 1976; Kacelnik and Todd, 1992),
while avoiding areas receiving heavy feeding pressure by females. Nonetheless, feeding groups of mixed sex also may occur
where preferred items in the diet are abundant. For instance, mule deer in eastern Oregon and white-tailed deer in southern Texas formed mixed-sex groups in areas where
forbs were abundant (Main, 1994). A detailed discussion of why or when females
should continue to remain in areas that receive heavy feeding pressure is beyond the
scope of this paper, but may be due to combinations of factors such as the availability
of palatable forage and water, security from
predators, the effects of philopatry, site fidelity, matrilineal cohesion, and the threat
of aggressive interactions with other groups
of females (Guinness et aI., 1979; Lazo,
1994).
Sexual dimorphism-body size hypothesis.-Intersexual differences in body size
that presumably affect digestive capabilities
and energetics have been invoked to explain sexual segregation, particularly when
males appear to use poorer-quality habitat
(Beier, 1987; Clutton-Brock et aI., 1982;
McCullough, 1979). The most common interpretations are that larger-bodied males
actively select habitats with abundant, lowquality forage because their larger ruminoreticular volume makes them more efficient
at converting fiber into energy (Demment,
1982), that males are less selective feeders
because of greater absolute metabolic requirements (Beier and McCullough, 1990;
Staines and Crisp, 1978), and that males are
less competitive feeders due to allometric
differences in size of bite (Illius and Gordon, 1987).
Gross (1990) conducted controlled feeding trials and compared efficiency of digestion, fill of alimentary tract, and passage
rates between males and females in sexually
dimorphic Nubian ibex (Capra ibex nubiana; males: X = 60.2 kg, SD = 6.8 kg;
females: X = 23.0 kg, SD = 3.2 kg). Males
Vol. 77. No.2
and females were fed identical diets and
feeding trials were conducted with both
high-fiber grass hay (Pennisetum americanum) and low-fiber alfalfa hay (Medicago
sativa). Males had greater fill of alimentary
tract and retained forage in the digestive
tract longer than did females, which should
have resulted in more complete digestion
(Parra, 1978). Nevertheless, digestion of total dry matter, neutral detergent fiber, and
acid detergent fiber did not differ among
males, nonlactating females, or lactating females for either grass or alfalfa (Gross,
1990). Based on observations of increased
chewing by females during rumination,
Gross (1990) concluded that greater mastication by females increased the surface area
of food particles and the rate at which digestion of cell walls proceeded in the rumen. Although the energetic costs of increased rumination were not known, previous studies with moose, elk (Cervus elaphus), and domestic sheep (Ovis aries) have
estimated rumination increases metabolic
rate 1-2% over lying with the head up
(Fancy and White, 1985). The costs of increased rumination are small compared
with the costs of foraging, which has been
reported to increase metabolic rates 33% for
elk and 28% for moose (Fancy and White,
1985). Thus, larger-bodied males retained
forages longer, which increased the efficiency of digestion, but females compensated
for shorter passage times by increasing the
rate of digestion through increased rumination at low energetic expense. Questions
still remain, however, whether these results
are repeatable among other species, to what
extent rumination may be used to increase
the efficiency of digestion, and whether differences exist between males and females
regarding the extent to which the digestion
of high-fiber forage may be effectively influenced in this manner.
Gastrointestinal volume of digesta in
wild ungulates may change in either sex because of changing physical condition or energetic demands, and has been reported to
increase with nutritional stress from lacta-
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MAIN ET AL.-SEXUAL SEGREGATION IN UNGULATES
tion and as the result of poor quality of diet
(Baker and Hobbs, 1987; Gross, 1990;
Jenks et aI., 1994). Jenks et ai. (1994) reported that during summer, lactating whitetailed deer had greater gastrointestinal volumes than did males and suggested that females selected summer habitats with high
biomass of forage to maintain fill of the alimentary tract and males dispersed among
remaining available habitats. Measurements
of nitrogen in feces indicated that males and
females in this study consumed diets of
similar quality (J. A. Jenks, pers. comm.).
Consequently, sexual segregation did not
appear to result in the consumption of lower-quality diets by males as predicted by the
sexual dimorphism-body size hypothesis.
The energetic requirements of female ungulates increase ca. 40% during late gestation and 150% during lactation (Loudon,
1985). Consequently, females should eat
the highest-quality diet available to them
during these periods. If females follow a satisficing strategy (Bunnell and Gillingham,
1985), however, they may sacrifice foraging
opportunities for reasons related to welfare
of offspring (Becker and Ginsberg, 1990)
and obtain a diet of lower quality than that
obtained by males.
Dietary studies we reviewed generally
were not supportive of the sexual dimorphism-body size hypothesis. A widely cited
example of support for superior female diets is Beier (1987), who measured nitrogen
in feces of white-tailed deer. Nonetheless,
nitrogen in feces was similar for males and
females during May, June, and AugustSeptember (table 2 in Beier, 1987). Therefore, diets were similar during most of
spring-summer, which generally is considered the most important time for obtaining
high-quality forage and replenishing energy
reserves (Mautz, 1978). Dietary studies
generally were more supportive of the reproductive-strategy hypothesis, which predicts diets of males will be as good or better
than diets of females. For example, Bleich
(1993) measured higher concentrations of
crude protein in fecal samples of male com-
455
pared with female mountain sheep during
periods of sexual segregation in 2 of 3
years; no differences were measured during
a severe drought in the 3rd year. Main
(1994) measured higher concentrations of
diaminopimelic acid in fecal samples of
male mule deer during June and July and
reported no differences between males and
females during August and September
when quality of range declined. No measurable differences in protein, phosphorus,
or calcium content in the rumen occurred
between sexes in diets of white-tailed deer
in Texas (Kie et al., 1980). Although superior diets of females in winter have been
cited in support of the sexual dimorphismbody size hypothesis (Beier, 1987; Staines
and Crisp, 1978; Staines et al., 1982), other
studies report superior winter diets for
males (Koga and Ono, 1994; Shank, 1982),
higher concentrations of crude protein in diets of males and more carbohydrates in diets of females (Weckerly and Nelson,
1990), and no dietary differences between
sexes (LaGory et al., 1991). Hence, dietary
evidence that supports the prediction of the
sexual dimorphism-body size hypothesis
that males segregate to habitats where
greater quantities of low-quality forage may
be obtained is equivocal.
A physical mechanism to explain why
males might seek out habitats with abundant, low-quality forage was proposed by
the model of Illius and Gordon (1987). This
model, developed for red deer, was based
on the interspecific allometric relationship
between the width of the incisor arcade and
body size. The model suggested that males,
as a result of their narrower breadths of incisors in relation to body size, were less effective competitors for forage in short
swards than were smaller-bodied females.
Consequently, Illius and Gordon (1987) hypothesized that heavy grazing pressure by
females reduced standing crops to levels
where males were prevented from foraging
effectively. Although this hypothesis provides a potential explanation for why males
would choose to forage in poorer-quality
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JOURNAL OF MAMMALOGY
habitats, it is also consistent with the arguments that males forage optimally by
avoiding those areas that have reduced biomass of forage. Regardless, evidence from
other species does not support the mechanism of Illius and Gordon (1987). For instance, intersexual size of bites of moose
were variable (Miquelle et aI., 1992) and
measurements of breadth of incisors of
male and female black-tailed deer did not
covary with body size as predicted (Weckerly, 1993). Consequently, the incisorbreadth hypothesis does not appear to be a
mechanism that can explain sexual segregation in general.
In light of the information provided, perhaps the most perplexing aspect regarding
arguments that males willingly segregate to
poorer-quality habitats is the lack of a reason for them to do so. The ability for males
to simply satisfy nutritional requirements
cannot, by itself, explain why males segregate to obtain poorer-quality forage.
Males that maximize nutritional condition
and replenish energy reserves may have
greater body mass, greater endurance during rut, and higher reproductive success
than males in poorer condition (Bergerud,
1974; Clutton-Brock et aI., 1982). Even if
differences in behavior or physiological
mechanisms make males inherently better
than females at exploiting resources in
poorer-qUality habitat, this does not explain
why males do not also exploit habitats occupied by females. Some incentive must exist, such as a preference by males for highfiber forage or a net energetic savings from
avoiding habitats used by females either because these habitats have naturally low biomass of forage (e.g., lambing cliffs) or because they sustain high levels of herbivory
from females (e.g., scramble competition).
This latter explanation incorporates aspects
of both the sexual dimorphism-body size
hypothesis (i.e., the ability for males to digest high-fiber forage efficiently) and the
reproductive-strategy hypothesis (i.e., a foraging strategy of males that maximizes energetic gain).
Vol. 77, No.2
Social factors hypothesis.-Hypotheses
that invoke social factors as determinants of
sexual segregation generally have focused
on behaviors of males such as the need to
develop fighting skills, evaluate potential rivals and establish dominance relationships,
and to scout potential breeding partners before rut (Beier and McCullough, 1990;
Geist, 1982; McCullough, 1979; Verme,
1988). Aggressiveness of females during
parturition also has been invoked based on
observations of a captive population of
white-tailed deer (Ozoga et aI., 1982), but
has received little support in natural systems or in other species. Mature males are
larger and have been widely reported as
dominant to adult females during aggressive interactions (Clutton-Brock et aI.,
1982; Hirth, 1977; Main, 1994; McCullough, 1979; Ozoga, 1972), and aggression of females during parturition cannot
explain why males segregate during other
times of the year.
Although sexual segregation may enable
males to learn fighting skills and establish
dominance relationships with other males,
it seems unlikely that this is the primary
reason for sexual segregation because males
could conceivably associate and establish
dominance relationships in the presence of
females, assuming females do not avoid
males. An alternative argument is that the
skills needed by each sex are associated
with where they are learned, such as where
to locate food, water, and suitable birthing
sites. This explanation seems particularly
appropriate for explaining philopatric behavior by females. Under this scenario, the
impetus for sexual segregation would not
necessarily be a choice strictly initiated by
one sex, but the consequence of each sex
seeking behavioral interactions that influence reproductive success (Clutton-Brock
et al., 1982; McCullough, 1979; Weckerly,
1993). This latter argument, however, is
functionally the same as the reproductivestrategy hypothesis; males segregate and associate with other males to learn foraging
patterns that maximize seasonal intake of
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MAIN ET AL.-SEXUAL SEGREGATION IN UNGULATES
food, whereas females are philopatric and
learn behavioral patterns that improve survival of offspring.
In respect to dominance relationships, the
large overlapping home ranges and ephemeral social structure of mature males outside
rut may promote the establishment of dominance relationships among many different
individuals (Clutton-Brock et aI., 1982;
Main, 1994; McCullough, 1979). Knowledge of the status of rivals would be useful
if it reduced potentially serious conflicts
over breeding partners because the costs of
conflict can be severe (Berger, 1986; Clutton-Brock et aI., 1982). Clutton-Brock et aI.
(1988), however, reported no consistent relationship between dominance status of
male red deer while in bachelor groups and
their fighting ability and mating success
during rut. Also, larger home ranges typically used by males (Beier and McCullough, 1990; Main, 1994; Weckerly,
1993) or aggregating behavior by females
(Bleich, 1993; Clutton-Brock et aI., 1982)
during rut increases the likelihood of contact between unfamiliar males. Hence, although pre-established dominance relationships may reduce conflict between familiar
males in some instances, the likelihood of
encounters between unfamiliar males and
the detailed posturing behaviors that have
evolved to assess rivals and establish dominance between males during rut (Geist,
1981, 1982) suggest that this is not likely
the primary impetus for sexual segregation.
Even if relationships of pre-rut dominance
were important among males, these relationships conceivably could be established
under a mixed-sex social structure if males
traveled freely among different social
groups. Males searching for potential mates
outside of rut also has been suggested as a
possible benefit for white-tailed deer when
home ranges of males overlap those of females (Beier and McCullough, 1990;
McCullough, 1979). Nonetheless, this also
seems unlikely as an explanation for sexual
segregation because many examples exist
where males segregate to areas where fe-
457
males seldom occur (Bleich, 1993; Gross,
1990; Main, 1994). Consequently, although
social advantages or skills may accrue from
the formation of single-sex aggregations,
formation of these might also be explained
by attraction to mutually desired resources
or for security reasons (Hamilton, 1971).
Hypothesis predictions and potential
critical tests.-Information cited to support
or discredit the three hypotheses discussed
in this paper comes almost entirely from
field studies that must deal with multiple
confounding variables and, often, multiple
interpretations. We recognize the logistical
difficulty in designing field experiments
with free-ranging ungulates, particularly
with respect to replication (Hurlbert, 1984).
Moreover, substitution of small mammals
into experimental designs may have little
relevance to ungulates due to their dissimilar characteristics of life history. Although
we do not provide the necessary experimental designs to test these hypotheses and
conclusively resolve this debate, we have
identified several aspects of these hypotheses that could potentially serve for conducting critical tests (Table 1).
Effects of foraging pressure of females
and competitive exclusion of males.-Clutton-Brock et aI. (1987), Illius and Gordon
(1987), and Main and Coblentz (in press)
suggested that localized pressure of grazing
by groups of females may reduce the availability of preferred forage and render areas
unattractive to males. Although this aspect
of the reproductive-strategy hypothesis may
be unimportant when groups of females occupy areas that naturally support lower biomass of forage than areas used by males
(e.g., lambing cliffs-Bleich, 1993; FestaBianchet, 1988), it is a critical assumption
when groups of females appear to occupy
superior habitat. Inherent in this prediction
is that use of habitat by males is in response
to the availability of preferred forage and
that males avoid areas where activity of females is high due to the effects of herbivory
of females on the availability of these forages.
458
JOURNAL OF MAMMALOGY
Critical tests of these predictions may
take several forms. Herbivory exclosures
may be useful for estimating the effects of
grazing pressure of males and females on
diversity and biomass of forage and should
be linked to analyses of range and diet such
that data may be interpreted as to what is
being eaten and when, what is available,
and what might be available in the absence
of herbivory. Measurements of range, however, may not be sensitive to the effects of
selective herbivory. Also, design of exclosures should consider the potential effects
of smaller herbivores and the use of moveable exclosures should be considered to address the response of plants to herbivory
and recycling of nutrients (Danell et aI.,
1994; Ruess and McNaughton, 1984).
Field studies that demonstrate positive
correlations between density of females and
the degree of sexual segregation, combined
with negative correlations between density
of females and standing biomass of preferred forage, may be easier to obtain and
would support the hypothesis that foraging
pressure by females influences sexual segregation by males. Clutton-Brock et aI.
(1987) reported these effects during an 11year study of red deer where densities of
females increased due to cessation of culling. As feeding activity of females increased in areas traditionally used by males,
standing biomass of grass and use of these
areas by males declined. Additional work is
needed to determine if these types of responses are repeatable among other species
and under what circumstances feeding pressure by females may be expected to influence sexual segregation. Direct manipulations of availability of forage through supplementation and removal, reduction of
densities of females through culling, and
modification of habitat with fire or other
means to influence patterns of use of habitat
by females may represent productive approaches for testing response of males to
changes in feeding patterns of females.
Measurements of response necessitate information on patterns of use of habitat prior
Vol. 77, No.2
to treatments, and traditional patterns of behavior may influence results, particularly if
the effects of treatments are not discovered
by males. Also, in areas where broad spatial
overlap occurs between males and females
(McCullough et aI., 1989), treatment response may be subtle, such as modifications
of core areas of activity.
Use of habitat and security of offspring.-If use of habitat by females is influenced by security concerns for offspring
(Festa-Bianchet, 1988; Main and Coblentz,
in press; Whitten et aI., 1992), then shifts
in use of habitat might be predicted if the
presence of offspring were manipulated.
Comparisons between females with and
without young also may be productive, but
consideration should be given to the influence that social groups may have on individual patterns of behavior in those species
where matrilineal bonds are strong. Also,
due to the strong site fidelity often demonstrated by groups of female ungulates
(Brown, 1992; Weckerly, 1993), changes in
behavioral patterns may be subtle, such as
increased distance from escape terrain during foraging bouts.
Dietary differences related to sexual dimorphism.-The hypothesis that males are
better able to digest poor-quality forage due
to larger body-size was not supported by
available information (Gross, 1990), but requires additional investigation. Perhaps a
more important question is whether and
when males preferentially consume high-fiber forage. The studies of diet reviewed indicated males generally consumed diets of
equal or better quality than females, particularly during summer, but differences may
exist between sexes in their willingness to
consume poor-quality forage, depending on
the amount of effort required to find highquality forage. Choice experiments may
provide answers to if and when preferences
for forage differ between males and females, and whether specific dietary components such as protein or digestible energy
influence these preferences. Feeding studies, under more natural conditions, are
May 1996
MAIN ET AL.-SEXUAL SEGREGATION IN UNGULATES
needed to elucidate the relationships between digestive capabilities, metabolic requirements, and body size so that intersexual differences in search effort, consumption of forage, and energy expenditure may
be assessed.
Segregation for social factors.-The establishment of dominance hierarchies
(Geist, 1982; McCullough, 1979; Verme,
1988) is probably the most widely cited hypothesis regarding sexual segregation for
social reasons, but Clutton-Brock et ai.
(1988) determined dominance relationships
during pre-rut did not hold during rut for
red deer, presumably because the incentives
for conflict were vastly different. If males
segregate to establish dominance relationships that serve to reduce aggressive encounters (among similar-sized individuals),
then isolated males should experience higher rates of aggression. This prediction might
be experimentally tested in a captive population of males of similar size by allowing
some individuals to associate in bachelor
groups during nonbreeding periods, while
isolating others until rut. Due to the influence of body size, weaponry, and physical
condition on dominance relationships (Clutton-Brock et aI., 1982), these factors should
be controlled to the greatest extent possible.
The accumulated evidence seems to support the reproductive-strategy hypothesis
(Main and Coblentz, 1990): behaviors of females promote security of offspring and
males segregate to prepare for the energetic
demands of competing for mates (Bleich,
1993; Main, 1994) or to recover from the
energetic drain of rut (Koga and Qno, 1994;
Miquelle et aI., 1992). This hypothesis was
founded in the logic of McCullough (1979)
and Clutton-Brock et ai. (1982), who argued that females compete for resources to
provision offspring, whereas males compete
for access to females. The reproductivestrategy hypothesis argues that groups of
females and young will be restricted to habitats that provide adequate forage and water
resources for raising offspring and, in environments where predation is important, to
459
habitats with suitable protective or escape
cover or lower densities of predators
(Bleich, 1993; Main, 1994). Because males
are in an energetic race against time and
against all other males, they should segregate to maximize foraging opportunities,
which may require avoiding areas where
activity of females is high (Clutton-Brock
et aI., 1987; Main and Coblentz, in press).
ACKNOWLEDGMENTS
The authors extend thanks to B. E. Coblentz,
J. G. Kie, and D. R. McCullough who participated in a workshop that helped develop many
of the ideas in this manuscript. The authors also
thank J. Gross and J. Jenks for their contributions to this manuscript. This research was made
possible, in part, by a Welder Wildlife Foundation Fellowship to M. B. Main. This is Oregon
Agricultural Station technical paper no. 10,844,
and a contribution from Humboldt State University and the California Department of Fish
and Game, Mountain Sheep Management Program.
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Submitted 5 June 1995. Accepted 15 June 1995.
Associate Editor was R. Terry Bowyer.