AMER. ZOOL.,
14:205-220
(1974).
On the Relationship of Social Evolution and Ecology in Ungulates
VALERIUS GEIST
Faculty of Environmental Design, The University of Calgary,
Calgary, Alberta, Canada
SYNOPSIS. Much of the social behavior and organization of ungulates can be related to
ecological parameters such as fiber content of forage, plant productivity, plant biomass,
plant species diversity, productivity gradients, temporal and spatial fluctuations in productivity, habitat stability, food dispersion, three-dimensional structure of habitat, colonization, and predator density and diversity. These ecological variables can be linked
via individual natural selection with the species' anti-predator strategies, emphasis on
different channels of communication, relative frequency of damaging and non-damaging
overt aggression, gregariousness and group structure, juvenile dispersal, home-range
traditions, monogamy and polygamy, sexual dimorphism, territoriality, hierarchical rank
structure, and plasticity of social structures. The ecological variables have primary manifestations which are behavior or which affect behavior, as well as secondary manifestations affecting behavior. There are logical links between the hypothesis linking ecology
and behavior discussed here with some principles from bioenergetics, zoogeography, and
paleontology. Although links do exist between ecology and behavior, they nevertheless
represent distinct realms of natural selection in which social behavior appears as the
more conservative element. The theoretical basis for this is discussed.
INTRODUCTION
The purpose of this paper is to present
the beginnings of a comprehensive theory
of social evolution as it relates to ecological variables. It deals primarily with
ungulates, that is, species of the orders
Artiodactyla, Perissodactyla, and Proboscida. There is urgency to this task since
behavioral and ecological studies of freeliving ungulates have only begun to blossom in the last decade, while the last
vestiges of wilderness are coming under
man's control; the day is in sight when
the last natural population of ungulates
will become a managed one. This applies
also to sanctuaries and national parks. We
need more and better theoretical guidance
in studying natural ungulate populations
to maximize our research efficiency and to
secure information we are unlikely to get
a few decades hence. Such guidance is most
important when studying relict and endangered species in order to minimize interference with the animals. We need better
theory in order to guide management of
ungulates in a rational manner.
In constructing a theory of social evolu-
tion, I have not followed tradition and
used behavioral and habitat correlates as
the basis of the theory. This approach has
been used with noteworthy success by Estes
(1974), Leuthold (1974), and Jarman (1968),
in relating ecology to social organization
and behavior in African bovids and by
Eisenberg and Lockhart (1972) for ungulates in Ceylon. A further attempt would
add nothing at this point. Rather, I have
used principles derived from several disciplines and deduced their ecological and/or
behavioral consequences, as well as some
a priori deductions, as will be shown below. The reasons for using this approach
are, first, that it is economical in reducing
diverse habitat types to a few ecological
variables and, second, that our knowledge
of the ecology and behavior of ungulates
is at present sketchy, biased in its sampling,
beset by some difficulties in concept, methodology, and terminology, and open to
some reasonable doubts. Despite some early
attention to ungulates by our pioneers in
animal behavior studies, i.e., Darling's
(1937) classic on red deer (Cervus elaphus)
and Scott's (1945) work on sheep, there had
been few studies made until well into the
205
206
VALERIUS GEIST
past decade. These studies were done on
the basis o£ quite diverse conceptions of
social behavior, terminology, and method.
There has been a bias toward studying the
most easily observable species, namely, the
large, gregarious forms living in open landscapes; we remain quite ill-informed on
small-bodied, and forest- or shrub-dwelling
species. There is a scarcity of data on species from large areas of the globe. For some
species we have fine studies of social behavior from captive groups (i.e., Walther
1958, 1964, 1968), but the ecology of many
of these species is as unknown as ever. The
converse is also found. Very few studies
have been conducted over the whole yearly
cycle of the study animals, and fewer still
have repeated annual cycles. Our studies
in the field have made me keenly aware
of differences in social organization and
behavior between years as a function of
different ecological circumstances and
changes in population composition, as well
as of real differences in behavior between
populations. Most studies have been done
on ungulates living in man-made environments found in Europe, North America,
and Africa, or on relict populations under
human control. Even where reasonably
natural conditions appear to exist, we may
still lack native predators or competitors
found but a century ago, as well as all of
the megafauna that vanished during and
after the last Ice Ages (Martin and Wright,
1967). We may, indeed, never solve puzzling aspects of behavior that were adaptive
a few millenia ago, or form pseudo explanations. In short, there is room for
doubt and suspended judgments when
treating our empirical data, and there is
much to be said for building theory independent of empirical data, but using empirical data to test theoretic predictions.
We need a sound theory to challenge facts
and arbitrate when there is doubt.
In the following theory, I linked ecological variables to social manifestations
using individual selection and reproductive fitness as criteria. Several times the
primary consequences of ecological parameters were taken to secondary consequences
(i.e., body size) and some concepts from
bioenergetics or psychology were used to
bridge gaps. In total, sixteen principles,
theories, or hypotheses were used, including twelve ecological parameters or variables. The theory is constructed in such a
fashion as to proceed stepwise from evolution in tropical to temperate or periglacial
regions. Since the structure of the theory
is complex, I cleaved to the bare bone and
cut descriptions, explanations, and discussions. The descriptions exclude mathematical formulations, but can be changed
into mathematical form. The hypotheses
or principles used are verified or can be
verified by their prediction. The theory is
tested by some linkages between principles
from different disciplines. Since this theory
is presented for discussion, I aimed only at
making it a logically sound structure,
which is not contradicted by our present
knowledge. Due to limitations of time, I
refrained from dealing with the relation
of ecological parameters on maternal or
juvenile behavior.
THE PROPOSED THEORY
To understand the relationship between
ecology and social behavior in ungulates
one may begin with the Jarman-Bell principle (Jarman, 1968; Bell, 1971).
1) The body size and population biomass of ungulate species is a function of
the fiber content (digestibility) and density
of the forage they exploit. (Ecological
parameters: fiber content of plant food
and relative availability of plant matter
of high and low fiber content.)
The Jarman-Bell principle is important
because body size affects many forms of
behavior in ungulates. It permits migration, determines the sound-frequency range
in vocalization, biases communication towards the visual or olfactory channels of
communication depending whether the
animal protrudes above the vegetation of
its habitat or not, and affects the antipredator strategy, as well as the social behavior, directly and indirectly. Thus, the
mass of an animal is in itself a constraint
on the kind of behavior pattern it may
perform. Thus, elephants or other large
207
SOCIAL EVOLUTION AND ECOLOGY IN UNGULATES
ungulates cannot use the violent, rapid
actions a mouse may perform without
smashing its body, while large-bodied ungulates may use head blows effectively in
fighting due to the mass and hence inertia
generated by heavy heads (see Geist, 1966a).
The Jarman-Bell principle can be explained as follows: The daily energy and
duikers (Cephalopinae) or tragulids may
supplement their herbivorous diet with
animal matter (Kurt, 1963; Walker, 1964;
Grim, 1970). The theory is well supported
by Schaller's (1967) and Hoogerwerf's
(1970) studies on Asian ungulates, as well
as by the diverse ecological literature on
European and North American ungulates.
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tUa r i i m l n i n t A<
function of their body weight raised to the gestive system as compared to that of horses
power of 0.75. For this reason, small-bodied has additional benefits. It allows us to exspecies require more energy and protein plain why perissodactyls achieved much
per day per unit of body weight than do larger body sizes in their evolutionary hislarge-bodied forms (assuming identical tory than did artiodactyls. The ruminant's
work regime and exposure to temperature digestive system is passive in the sense that
and wind). The high metabolism of small- the animal cannot change the rate of gut
bodied species can be sustained only on clearance, but must wait for the rumen
highly digestible forage. Since digestibility, content to decrease via anearobic fermenand hence daily intake of forage, is a func- tation. In the perissodactyl, however, the
tion of the fiber and protein content of the animal can vary the rate of gut clearance,
forage (Blaxter et al., 1961; Elliot and and compensate for poor forage of low diTopps, 1963), small-bodied ungulates re- gestibility by eating more and passing out
quire a forage of relatively lowfibercon-the undigested portions relatively quickly.
tent and high protein content; large- It can thus maintain a steady stream of
bodied ungulates can feed on forage with energy and nutrients across the gutwall,
higher fiber and lower protein content but does so by digesting the forage less
since their requirement for energy and efficiently than do ruminants and by connutrients per unit of body weight are suming more forage. This mechanism perlower. A ruminant can eat only as much mits the exploitation of very coarse forage
as it digests; hence, the more it digests the or, conversely, it permits the perissodactyl
more it can eat; hence, the more energy to reach larger body size than a ruminant
it requires, the more digestible the forage on identical forage. This may be the reamust be. However, highly digestible forage son for perissodactyls reaching the largest
(fruits, seeds, flowers, sprouting shoots) is body sizes known from terrestrial mammals
available mainly in small bits, makes up in the paraceratheres from the Oligocene
only a tiny fraction of the total plant bio- and Miocene of Central Asia (Thenius and
mass, and is dispersed and relatively rare. Hofer, 1960), and being an order in which
Thus, the absolute amount of such forage giants such as the brontotheres, elasmoan animal can gather per day is very small. theres, chalicotheres, and most rhinos were
Only a small-bodied animal could get the rule rather than the exception.
enough of such forage to live on. ThereBell's (1971) analysis also suggests that
fore, species adopting a feeding strategy for any given forage type, perissodactyls
based on highly digestible forage will be reach a lower biomass than do artiodactyls
small-bodied. Second, since the relative and should thus have relatively lower denbiomass of their forage is very small, the sities in any given habitat, and larger
biomass of such small-bodied ungulates will home ranges and territories than do bovids
be very small (see Bourliere, 1965). We can or cervids. Klingel's (19741 observations
argue the converse for species exploiting tend to bear this out for equids.
plentiful forage of high fiber content,
2) The anti-predator strategy of an unhence low digestibility.
gulate species is a function of its body size.
The Jarman-Bell theory makes it underThis is a well-recognized relationship, an
standable why small-bodied ungulates like excellent discussion of which is found in
208
VALERIUS GEIST
Eisenberg and Lockhart (1972). The largerbodied a species of ungulate, the more
likely it stands and fights predators or attacks them, rather than runs away. In addition to Eisenberg and Lockhart's (1972)
examples, we are familiar with the defensive rings of musk-oxen against wolves
(Pederson, 1958; Tener, 1965), the attacks
of African buffalo on hunters and predators (Schaller, 1972; Sinclair, 1974), and
the recognition that large ungulates, like
rhinos and elephants, have little to fear
from common predators and, in fact, attack them (Schenkel and Schenkel, 1969;
Sikes, 1971; Hindrichs, 1971). Good discussions of anti-predator behavior of various African bovids may also be found in
Kruuk (1972) and Schaller (1972).
There are some subtle influences of
predators on the social behavior of a species. Thus, Geist (1963) pointed to the
unusual nature of "scare threat" in moose
{Alces alces). This threat, plus the ability
of moose to kick with their hind legs
against opponents, appears to be an adaptation of moose against wolves. In late
winter, when the snow lies deep, moose
may be mired in snow and at this time
have little choice but to stand and fight
wolves. They may also stand off wolves in
other seasons (Mech, 1966; Geist, 1971a).
3) The anti-predator behavior of an ungulate species is a function of the cover of
its habitat. (Ecological parameter: threedimensional structure of habitat.)
Since in thick cover an animal may be
heard before it is seen, while in the open
it can be detected visually before it is
heard, an ungulate inhabiting dense cover
may minimize detection by minimizing
auditory clues to its whereabouts. If it is
too small to successfully confront predators, it assumes a hiding strategy (see Eisenberg and Lockhart, 1971). This means it
may reduce or abandon auditory signals
in social communication, avoid company
to reduce noise levels, step daintily and
carefully on the ground, become nocturnal, seek to hide in thick cover, adopt
a cryptic coloration, and remain motionless on detecting danger. Conversely, since
ungulates inhabiting open plains are de-
tected by predators on the basis of sight
rather than sound, they may—but need
not—elaborate on vocal communication.
Hence, social, open-country ungulates may
be expected to vocalize freely when undisturbed. This hypothesis appears to be valid
since small, forest-dwelling ungulates are
largely silent and seen singly, while species
inhabiting the ecotone between forest and
plains tend to be noisy. A corollary of this
is that open-country forms are likely to
use special visual predator warning signals
in addition to vocal ones. Indeed, we do
find conspicuous spotting, flashing of rumppatches, excitation jumps, and pronking in
small and medium-sized plains and ecotone dwellers (i.e., Gazella thomsoni,
Aepyceros melampus, Antilocapra americana, Antilope cervicapra, Odocoileus hemionus, Antidorcas marsupialis, Rangifer
tarandus), but an emphasis on vocal antipredator signals and thumping with hooves
in forest and brush dwellers (i.e., Old
World deer in general, Odocoileus virginianus, Madoqua, Muntiacus, Redunca).
The foregoing permits the following prediction: For any given body size, species
exploiting the ecotone between forest and
steppe or meadows—that is, between high
and low structured habitats—will have the
greatest diversity of anti-predator strategies.
Such species will use strategies relevant to
high and low structured habitats.
Whereas shrub and forest dwellers
evolved cryptic coloration or dull body
colors probably to reduce detection by
predators, no such constraint is evident in
the color patterns and conspicuous hair
pattern of plains dwellers. On the contrary, the color and hair patterns appear
to be "designed" to catch the attention of
onlookers and to distinguish clearly the
animal from its surroundings. Walther
(1966) pointed out how oryx antelopes
(Oryx gazella) are framed by their markings; Geist (1966a) pointed out that one
can recognize in the markings and hair
patterns of ungulates, the very attentionfixing and attention-guiding mechanisms
employed by artists painting pictures. In
short, plains dwelling has permitted an
elaboration of vocal and visual signals so
SOCIAL EVOLUTION AND ECOLOGY IN UNGULATES
well illustrated in gnus (Estes, 1969), while
forest dwellers appear to elaborate olfactory
signals (see also Estes, 1974).
It can be predicted from the foregoing
that for species of equal body size, those
from the ecotones of high and low structured habitats will have the richest repertoire of social signals since they will use
seiisoiy modalities applicable, for instance,
to forest and open landscapes.
4) Populations of large-bodied ungulates
have a lower turnover rate than do populations of small-bodied ungulates; in consequence, there will be greater selection for
non-damaging intraspecific fighting in
large-bodied species than in small-bodied
ones.
Granted Brody's (1945) findings that
each unit of protoplasm has roughly the
same number of calories to burn before
senescence and death, and granted that
small-bodied mammals have a higher metabolic rate than large-bodied ones per
unit of body weight, it follows that smallbodied ungulates have the higher turnover
rates. Evidence to this effect is shown by
Bourliere and Hadley (1970) in African
ungulates. It is evident that, as the number of seasons in which a male breeds becomes reduced, a greater risk of death from
intraspecific combat becomes acceptable.
Hence, in species with long-lived males,
the male maximizes his chances of reproduction by reducing damaging intraspecific
fights and increasing alternative mechanisms for establishing dominance. Second,
granted the acceptability in small- and
large-bodied forms of some absolute number of wounds per lifetime, such wounds
would have to be inflicted at lower rates
in large-bodied forms than in small-bodied
forms. The above hypothesis may explain
the frequent, intense, damaging fights of
saiga antelope (Saiga tatarica) (Bannikov
et al., 1961), while intense fighting in such
species as rhinos, elephants, or even African buffalo is rather rare fSchenkel and
Schenkel, 1969; Sikes, 1971; Sinclair, 1974).
In the small-bodied roe deer (Capreolus),
Kurt (1970) reports that fighting is common, while Bramley (1970) and Cumming
(1966) report the opposite. However, Bram-
209
ley saw roe bucks chase each other frequently. We would expect damaging combat in this small-bodied, short-lived deer
(Lettow-Vorbeck and Rieck, 1956). As will
be shown later, there are other parameters
selecting for or against damaging combat,
besides those in the present hypothesis.
5) In habitats with little or no cover, ungulates use each other as orientation points
and for cover. (Ecological parameters:
three-dimensional structure of habitat.)
This hypothesis is of considerable antiquity, has been proposed independently
by several authors (see Estes, 1974), and is
best explained in Walther (1966). This
hypothesis explains why species usually
considered solitary, such as roe deer (Lettow-Vorbeck and Rieck, 1956; Kurt, 1970),
red buck (Jungius, 1971), white-tailed deer
(Sparrow and Springer, 1972), or even
moose on rare occasions, congregate into
herds if they feed in the open, coverless
plains.
This hypothesis accounts for clumping
of ungulates, but not for the social structure of open-country species. This is in
part accounted for by the following hypothesis.
6) The exploitation of stable, self-regenerating, climax-plant communities selects
in ungulates for juvenile-retention (which
manifests itself in cohesion between individuals, leadership, gradual disassociation
of mother and young, and home range
traditions); exploitation of serai plant communities which appear due to catastrophic
events (fires, floods, avalanches) and which
cannot be predicted in space and time, selects for juvenile dispersal. (Ecological
parameter: climax versus serai plant community, habitat stable or subject to sudden
contraction and slow expansion versus
habitat subject to rapid expansion but slow
contraction.)
This hypothesis proved useful in explaining the differences in the behavioral
biology between mountain sheep (Ovis
canadensis) and moose (Geist, 1967, 1971a).
It is likely to be valid for other species also.
It explains why plains dwellers exploiting
dispersed patches of habitat should evolve
traditions, why colonizing juveniles can-
210
VALERIUS GEIST
not be expected, and why refined, complex all ungulates will strive to reduce the high
mechanisms of social submission should caloric costs of excitement and physical
work1 since this detracts from the resources
exist in such species.
7) Territoriality is permitted to evolve available for reproduction.
Studies of domestic ruminants have
in forms living in habitats where the diversity and productivity of plant matter is shown that on good to medium hay, the
relatively great and continuous such as to animals can ingest daily only about 160
fulfill the living requirements of the species Kal kg W0-75 (W = body weight) of metabon a small area; breeding territories may be olizable energy (Blaxter et al., 1961; Blaxter and Willson, 1962). However, normal
permitted in species where the mobility of
females is low during rutting seasons. (Eco- daily grazing requires an expenditure of
logical parameters: amount of primary pro- metabolizable energy ranging from 114-167
ductivity, fluctuation in primary produc- Kal kg W0-75 depending on pasture quality
(Graham, 1964; Young and Corbett, 1968;
tivity, species diversity in plants.)
The proposed ecological conditions are Young, 1971) and as high as 140-189 Kal
0 75
essential for an area to contain defensible kg W - in lactating cows. Since one hour
food resources following Brown's (1964) hy- of running a day at 10 times basal would
pothesis. The hypothesis does not state increase the normal daily cost of living by
0 75
why territoriality evolves, but states where about 30 Kal kg W - , a sheep so exercised,
it will not occur, namely in ungulate spe- while grazing on poor pasture, would ex0 75
cies which must be continuously prepared pend about 190 Kal kg W - of metaboto move, be it that snow falls, frost and lizable energy or about 19% more energy
wind close some forage areas and expose than it could possibly ingest when feeding
others, or the forage is unpredictable in the on good to medium hay. Since excitation
time of an annual cycle for whatever rea- elevates metabolism by 20% or more (Websons (Geist, 1974). This hypothesis explains ster and Blaxter, 1966), harassment and
why we cannot expect northern ungulates running are costly. We can safely assume
to be territorial if they rut in fall and early that a reduction in harassment and runwinter, as almost all do, and it explains the ning entails real benefits to the female.
two known exceptions as well. Thus, the
The second hypothesis related to the
long gestation period of Antilocapra and above was suggested by Crook (1970) and
the delayed implantation in Capreolus per- Eisenberg and Lockhart (1972): If the male
mit these two ruminants to rut in summer forages over the same area as the females
or early fall when forage production is which bear and nurse his young, it bestill high and no snowfalls or frosts give comes adaptive for the male to remove
cause to move to different habitats. Both other males from the foraging area and
species are territorial (Bromley, 1969; Kurt, thereby reduce competition in favor of the
1968, 1970; Bramley, 1970). Kramer's (1969) mothers of his young. Geist (1974) sughypothesis that chamois (Rupicapra rupi- gested, with some support of evidence, that
capra) are territorial may be based on it becomes adaptive for males to assume
an artifact of high population density.
diffei-ent food habits from the females and
8) The behavior of females compared to thus reduce competition. The third manimales will be such as to maximize energy festation will be discussed under sexual
and nutrients available towards fetal dimorphism below. This hypothesis was
successful in explaining the social structure
growth and lactation.
There are several manifestations of this of some ungulate societies, in particular
hypothesis. In the strongly sexual di- the segregation of males from gestating and
morphic mountain sheep, females reduce lactating females, sex-related differences in
to a minimum the cost of harassment by habitat preference, and reduction in
males, the cost of work, and communica1
tion as well as competition for forage with
For effects of harassment, see Geist's (1971c)
males (Geist, 1971a). We can expect that summary.
SOCIAL EVOLUTION AND ECOLOGY IN UNGULATES
amount and redundancy of communication
by females as compared to males.
9) Dispersed and diffused food of low
density per unit area will lead to a selection against food competition by overt
aggression, as will highly localized food
resources found at high density; overt aggression will be selected for as a means of
intraspecific competition lohere it. will result in a significant return in food in short
supply, compared to the cost of defending
it. (Ecological parameters: food density and
concentration.)
The above hypothesis is essentially
Brown's (1964) concept of defendability
of resources as applied to ungulates. It is
self-evident that where forage is diffuse and
widespread, a female attacking another one
only causes the latter to jump aside and
continue feeding on a site a few paces
away. The aggressor has incurred the cost
of aggression without gaining any resources
in return, since its life depends on exploiting a wide area in which forage is thinly
scattered and thus cannot be defended.
Here the best strategy is to compete by
feeding more intensely and reducing aggression to save energy for reproduction
and growth. This is the situation we find
apparently in most ruminants and explains
the relatively tolerant behavior of females
grazing together in groups and the formation of maternally related groups of females into clans (Kurt, 1968) or home
range groups as Hunter (1962) has called
them.
Conversely, when food is localized and
superabundant so that it attracts many females, there will also be selection against
aggression but for different reasons. A female attempting to defend the resource
must take on many females simultaneously.
The cost of defence now becomes prohibitively high and it becomes more adaptive
to feed as much as possible and thus compete by feeding (increasing rate of food
intake) rather than wasting time and resources fighting as Kruuk (1972) has suggested.
From the foregoing, we can assume that
selection for overt aggression in food competition will be greatest where forage is
211
neither superabundant nor scarce.
10) Habitats stable in space and time
(fluctuations less than maximum population growth of species) select for territoriality and reduced sexual dimorphism;
habitats which fluctuate in space and time
(in excess of maximum population growth
rate) select for hierarchical system of dominance in males and increased sexual dimorphism; stable habitats in which food
is unpredictably dispersed in time and
space but locally abundant select in territorial or hierarchical species for reduced
sexual dimorphism. (Ecological parameters:
habitat stability and instability of food
resources.)
a) The seventh, eighth, and ninth hypotheses are central to this hypothesis. In
an exceedingly stable, qualitatively uniform habitat such as climax tropical rain
forest, in which the prerequisites for territoriality—high density, diversity, and defendability of resources (Brown, 1964)—
are found, there will be constant, severe
competition for the available living space
and the resources it contains. Here an individual's only chance to reproduce or even
to live is to capture and defend successfully
a piece of real estate and its resources.
Otherwise, the individual must take up
residence in an unsuitable locality; it becomes part of the population surplus.
Hence, there is selection for intolerance of
other individuals within a circumscribed
space the animal can successfully defend.
Under the stated conditions there will
be selection against sexual dimorphism via
male mimicry by the female: a female holding a territory here would be under constant pressure by non-territory holders and
would be forced during gestation and lactation to divert energy and nutrients towards territorial defence. Hence each territorial female benefits by a defender of the
territory which is relatively cheap to maintain. This can only be a male, not another
female. By mimicking the external appearance of the male and assuming the male's
scent, the female reduces the chances of
being attacked, since a female intruder
would be at a loss to identify quickly what
is male or female. A male-mimicking fe-
212
VALERIUS GEIST
male introduces ambiguity for the intruder, while doubling the redundancy of
the message that the territory is occupied.
A female intruder maximizes its chances
of taking over a territory if it can concentrate its attacks on the territory owner of
its own sex. This the male-like female
denies.
In this system, a male maximizes its reproductive fitness by protecting the resources for the development and growth
of his children, by aiding his mate in territorial defence, hence reducing the chances
of interrupted gestation, suckling, or development of his offspring. The male
should be large enough to be a good defender, and small enough to be inexpensive
to maintain in food resources. In this system, an adult sex ratio of 1 male: 1 female
is mandatory, as is a strong pair bond, for
the following reasons: In a territory in
which a female's success depends on the
male's defence of resources for reproduction, a male may not permit another female to enter, since her presence increases
competition to his pregnant or lactating
mate and thus reduces the male's chances
of leaving behind viable offspring. Hence,
a male must learn to distinguish sharply
between his female and a stranger. Second,
the male must choose a reproductive partner very carefully, since he will breed probably only one female in his lifetime and so
must reduce the chances of mating with a
poor mother. If the male's mate dies, a
quick choice of females and remating with
any female would, on the average, lead to
more poor mothers being bred than if the
choice were made deliberately and slowly.
Therefore, we can expect that males losing
their mates will not remate quickly. This
was found for Madoqua by Hindrichs and
Hindrichs (1971). In a polygamous system,
in which a male maximizes reproduction
by breeding many females, he need not be
choosy. This raises the question: on what
basis does a territorial male select his mate,
and what attributes of the female predict
a good mother?
We expect the territorial system described in ungulates from tropical climax
rain forests, or limited habitats such as
cliff outcroppings, or permanent clumps
of shrubs in savannahs. The biology of
Madoqua appears to fit this system (Hindrichs and Hindrichs, 1971). For the genus
Cephalophus, there are only circumstantial data (see Rails, 1971; Estes, 1974).
b) If the habitat increases and decreases
between years so that the resources for
the species vary by a multiple from year to
year, then, in years of plenty, females will
experience little or no competition for resources and all females can raise offspring
successfully. This includes females of low
aggressiveness. Granted this situation, there
is reduced selection for aggressive females;
females squandering resources on aggression and excitation may be expected to be
less successful during the expanding phase
of the populations than calm, unaggressive
females. Since during "good" years the population raises a large number of unaggressive females, it is probable that these
females are largely left to breed during
the "poor" years.
The male becomes superfluous for territorial defence. He can maximize reproductive fitness by maximizing the number
of females he inseminates. If the habitat
fluctuations are very large, so that the females inseminated by one male do not
benefit materially from that male's actions
to expel other males from their foraging
sites to reduce harassment and competition
for food, then there will be no selection
for territoriality and a hierarchical male
society will evolve. If the female benefits
from the male's protection, a system of male
territories will overlap the home ranges of
females. In both systems there will be selection for large, aggressive males. There
will be no selection for male mimicry on
the part of the female, and the female can
divert a maximum of nutrients towards
reproduction. The male increases his
chances of breeding by extending body
growth long into adulthood. Intense male
competition for females is likely to result
in intense agonistic interactions among
males, and a short life-expectancy for adult
males. Since subordinate males are also
relegated to inferior habitat where they
suffer increased mortality, we can expect
SOCIAL EVOLUTION AND ECOLOGY IN UNGULATES
an adult sex ratio favoring females.
It may be that we will find in ungulate
species with great sexual dimorphism a
greater "vocabulary" of social behavior patterns than in pair-forming or gregarious
species with low sexual dimorphism as was
found by Brereton (1970) for Australian
parrots.
Since both systems (a) and (b) could
evolve in tropical climates, and tropical
plant associations are believed to be of
great antiquity (see Baker, 1970), it follows
that the territorial and hierarchical social
systems are equally ancient. We have, therefore, little reason to believe that the hierarchical social system evolved from the territorial one, or vice versa.
c) In an open landscape with a high
carrying capacity of ungulates, or with
spotty, periodic food production, selection
for sexual dimorphism must collapse. In
large congregations of ungulates, males
would be hard put to protect a large number of females from the continuous courtship (and hence cost of harassment and
running) of smaller males. In essence, the
harem is an undefendable resource (Brown,
1969). Since harassment and running are
exceedingly costly in energy, it would be
adaptive for females to reduce the courtships of small males. This females can do
by becoming less "attractive," that is, more
male-like in appearance and body size. Male
mimicry is again adaptive for females. One
can hence expect the females in highly
gregarious ungulates to look much like the
males, even to the extent of having penis
tufts as in the gnu (Gonnochaetes) (Estes,
1973). This explains the reduction in sexual
dimorphism in many gregarious ungulates
such as bison, buffalo, reindeer, spring bok,
many gazelles, oryx, and eland antelope.
The females become capable of defending
themselves, which has the added advantage
of the females successfully competing with
males over resources. Hence, sexual dimorphism is least in the highly social and
pair-forming species, and greatest in the
moderately gregarious ungulates.
If the resource is highly localized and
available for a short duration only, there
will be not only male-mimicry among fe-
213
males, but females may become dominant
over males. (This would appear to hold
true also for a predator of ungulates, the
spotted hyena, reported on by Kruuk,
1972). As indicated earlier, if the resource
is fed on simultaneously by a large number
of individuals, competition may take the
form of exceedingly hasty eating rather
than fighting (Kruuk, 1972), for aggression
would lead to a loss of resource through
competition to both combatants. This suggests that, in highly gregarious forms exploiting sporadic occurrences of food
sources, we need not expect a high level
of aggression, although we can expect little
sexual dimorphism. For parrots, but not
yet in ungulates, this concept fits the data
(Brereton, 1970).
d) In Eurasian and American mountain
bovids, sexual dimorphism or the lack
thereof has no obvious ecological relationship. Thus, the dimorphic sheep may live
side by side with the non-dimorphic mountain goat in many areas of the Canadian
Rockies. The reduced sexual dimorphism
of mountain goats appears to be a function
of their weapons combined with narrow
habitat preference and wide, catholic food
habits. It can be explained as follows: The
horns of mountain goats are very sharp
and are used in intraspecific combat only
as weapons (Geist, 1965, 19666). Since subadult goats strike at each other and at kids
with the risk of wounding or killing each
other or the kid, it is adaptive for females
to be aggressive towards all goats which
approach their kids. Hence, there is a selection for aggressive, dangerous females.
Since goats stick closely to cliffs, but have
wide food habits (see Hibbs, 1966, for review) males and females are competitors
on the same limited areas of habitat. It is
hence adaptive for the female to remove
the males from her winter range (where
she stays during gestation). Attacks by females on males were observed by Geist
(1965); DeBock (1970) found males relegated to poor habitat after the rutting season. Clearly, if the female removes the
males from her winter quarters, it is adaptive for the female to mimic males in external appearance. This increases the con-
214
VALERIUS GEIST
tent (rather than redundancy) of her
message during attacks. Chamois females
may also mimic males; Kramer (1969)
found that females may perform ejaculatory
motions during threats directed at small
males.
11) Where ungulates are faced with a
high density and diversity of predators,
predators will select against damaging, intraspecific combat in their prey. (Ecological parameters: predator density and
diversity.)
It can be argued that individuals which
are quick to jab painfully or cut a nearequal conspecific are likely to trigger a
desperate cdunter-attack (Geist, 1966b,
1971a). This argument is supported by
experimentally induced aggression in various mammals (Ulrich and Azrin, 1962;
Azrin et al., 1965; Galef, 1970). Clearly, an
individual who is quick to attack is quick
to be wounded in a counter-attack, and thus
increases his chances of being weakened,
sickened, and spotted by predators as such
(Estes, 1969). The individual less likely to
become prey is the one using "ritualized"
combat and dominance displays. In regions
where the predator density and diversity is
low, such as in north-temperate environments, we can expect a relatively greater
frequency of deaths and wounding through
intraspecific combat. This appears to be
so. By contrast, in African bovids faced
with high predation pressures, relatively
non-damaging combat is typical (see discussion in Geist, 1971a; also Bergerud, 1974;
Hindrichs and Hindrichs, 1971). An additional parameter affecting intensity and
frequency of intraspecific combat is discussed under hypotheses 13 and 15.
12) / / there is a great range of productivity (long quality gradient) in a stable
habitat there will be reduced selection for
female aggression; males maximize reproductive fitness by capturing territories in
high-quality habitat and advertising to females; females maximize fitness by selecting best-quality habitat, in non-territorial
species selecting the most dominant male.
(Ecological parameter: habitat quality
gradient.)
This is essentially an hypothesis of Ver-
ner and Willson (1966) as discussed in
Orians (1969) which explains the evolution
of polygamy. The converse of this hypothesis is: a stable habitat with a short productivity gradient will select for monogamy as
I argued under hypothesis 10(a) following
Brown's (1964) concept of defensibility of
resources. There will be reduced selection
for aggression since females of low aggressiveness will be able to survive and reproduce on sites of lower productivity. Second,
on sites of very high productivity, highly
aggressive females will be constantly confronted by intruders and will expend too
much time and energy fighting or chasing
off others, as explained under hypothesis 9.
The male would gain little defending the
aggressive female (no gain in resources in
short supply since resources are superabundant), but would maximize his reproduction by maximizing the number of females he can inseminate. These selection
pressures would result in reasonably tolerant females which would cluster on high
quality sites of the habitat and aggressive,
large, strongly dimorphic males which
would place their territories over the best
sites, expel subordinate males to poorer
sites, and advertise themselves to the females. If the female has no need of the male
to protct her from harassment or to reduce
food competition on her home range, females will select males only on the basis
of dominance. Hence, males compete on
the basis of displays signalling high dominance rank. This could lead in hierarchical
species to extreme male dimorphism and
in territorial species of ungulates to leks,
where males advertise by number rather
than by greater difference (R. D. Guthrie,
personal communication). In short, lek
males increase redundancy of the message,
hierarchical dimorphic males the content
of the message.
Verner and Willson (1966) pointed out
that habitats with great productivity gradients are marshes, while terrestrial habitats tend to fluctuate less in productivity.
Orians (1969) following Verner and Willson (1966) predicted that marsh species
would be relatively more sexually dimorphic than species inhabiting terrestrial
SOCIAL EVOLUTION AND ECOLOGY IN UNGULATES
habitats. This prediction is adequately supported by comparing such marsh dwellers
among ungulates as marsh deer (Odocoileus
dichotomus), barasingha (Cervus duvavceli),
milu (Elaphurus davidanus), sitatunga
(Tragelaphus spekei), and water buffalo
(Bubalus arnee) with their closest relatives
for terrestrial habitats. The greatest sexual
dimorphism is reached by 11011-i.eiritorial
ungulates in the Temperate Zones as well
as by the Tragelaphinae in Africa. The
above hypothesis may explain the strong
dimorphism of the latter, but the strong
dimorphism of northern and periglacial
ungulates is explained by hypotheses 13
and 15.
13) Dispersal theory. (Ecological parameter: unoccupied habitat available for
colonization.)
Since this theory has been explained in
several publications (Geist, 19666, \%l\a,b,
1974) and applied to various lineages of
large mammals, primarily ungulates, I shall
give a short summary here only and list
some of its predictions.
During colonization of vacant habitat,
ungulates experience a superabundance of
forage prior to reaching the carrying capacity of the new habitat. During the
population's expanding phase, selection
favors large, vigorous males skilled in intense combat and females producing genotypically large offspring. One mechanism
permitting individuals to attain large body
size is physiological "juvenileness." Its extension into adult life produces neotenous
and/or paedomorphic individuals which
are distinguished from their parent population by an increase in "juvenile" features
in appearance and behavior. Since, even in
the stable populations, at carrying capacity
dominance depends on skill in combat and
efficiency of weapons and defences, and
dominants breed, the evolutionary trend
towards specialization in combat and display organs becomes fixed. This is true even
though phenotypically the animals become
smaller in size. In warm or tropical environments, where a dispersing species may
meet a closely related, but ecologically different population, there will be selection
for isolating mechanisms (Mayr, 1966) pri-
215
marily in the dispersing species (the species
in lower abundance), which in ungulates
takes the form of visual, vocal, and olfactory
isolating mechanisms. This is, in essence,
the skeleton of the dispersal theory.
It predicts: (i) In tropical, but not northtemperate and periglacial environments,
social specialization follows ecological specialization and parallels it. Thus, the
greatest ecological specialists are also the
most "bizarre" in external appearance, featuring usually contrasting color and hair
patterns, large rump patches, and often
large and bizarre horn-like organs, (ii) Frequent expansions of habitats on a geologic
time-scale increase the rate of evolution and
produce in a short time-span a diversity of
large-bodied, bizarre species. This explains
the great number of gigantic, bizarre-like
mammals during the Pleistocene, (iii) Ancient immigrants of a species to a continent
tend to be larger in body size than their
descendants, (iv) In the north-temperate
regions, clinal variations in ungulate races
may reflect the dispersal history of the species, not an ecological gradient, (v) Evolutionary trends set during dispersal are
irreversible, explaining thereby Dollo's
law. (vi) In tropical environments, the dispersal and evolution of large mammals follows Darlington's (1957) conceptions; in
periglacial environments, Mathew's (1915).
Thus, the theory unites two previously contradictory views, (vii) If lack of ritual, overt
aggression, and sexuality are typical of
juveniles, advanced species are more overtly
aggressive and unritualized compared to
primitive ones. This latter prediction could
be verified for mountain sheep (Geist,
1971a).
It also solves another puzzle: granted the
Bell-Jarman principle, it would be impossible for small-bodied tropical ungulates to
evolve into large-bodied forms. Yet this is
a well-recognized "rule" in evolutionary
radiation (Scott, 1937; Simpson, 1949; Thenius and Hofer, 1960). A small-bodied species is locked into its body size range by its
inability to increase its energy uptake (and
grow bigger) by eating forage of high fiber
content (and consequently low digestibility). However, if for some fortuitous reason
216
VALERIUS GEIST
a population of that species reaches relatively large body size, it is preadapted to
exploit forage of lower quality. Such a fortuitous reason would be a superabundance
of forage during colonization of vacant
habitats.
One can use the same argument towards
the prediction that, in sexually dimorphic
species, the larger male becomes preadapted
to feeding on coarser forage. Such selection
would be reinforced since males, in their
period as subordinates, are forced into poor
habitats by dominants. Moreover, once
dominant, the male reduces his competition with the females on his territory.
An important part of the dispersal theory
is the statement that the social behavior of
individuals is determined in its frequency
of expression by the nutritional state of
individuals. In mountain sheep it was
found that frequency of play, combat, display, and sexual behavior was apparently
related to the quality of the population,
and it, in turn, to the population's resource
base (Geist, 1966a, 1971a). The better the
nutritional state of the animal the more
vigorous it acted. In other vertebrates, there
is a host of relationships between nutrition
and their social behavior, as recently reviewed by Watson and Moss (1970) and
Cowley (1970) or discussed by Dubos (1968)
for man. We can distinguish the effect of
nutrition alone on the expression of behavior versus the secondary effects of nutrition on behavior via population density.
T h e subject is complex and I refer to above
references for discussions and further literature.
14) Edinger's principle.
This principle states that during evolution body size and legs are first to change,
teeth are next, and brain size and morphology last (Edinger, 1948); it was derived
from paleontological studies of equids, but
appears to have application in primates
(Hofer, 1972). Its behavioral implications
are well discussed by Hofer (1972) and state
that the signal structure is likely to be
conservative during evolution, so that
within a genus or family highly diverse
species will still show very similar social
behavior patterns. Walther's (1964) studies
of tragelaphinae and Geist's (19710^ review
of caprid behavior are compatible with this
view.
15) Predictable, periodic productivity sets
birth seasons and shortens birth and rutting
seasons. This leads to idleness of males outside the rutting season, as well as intensifying the rutting activities, in particular,
combat. (Ecological parameter: seasonal
superabundance of forage.)
I discussed this concept in detail elsewhere as it applies to ruminants (Geist,
1974). Since the period of idleness in males
coincides with the time of greatest productivity in the temperate north, the males
are free to draw from the seasonal superabundance in order to grow large stores of
fat and huge horn-like organs. This process
is accelerated by the greater caloric density
of plant matter available as forage from
temperate and arctic regions, compared to
tropical ones (Jordan, 1971). The fat, in
turn, permits the males to spend their time
rutting rather than feeding. Thus, we can
expect differences in intensity of courtship
and combat activities between tropical and
temperate forms of the same family. This
hypothesis does not say what selects for
huge, excessive, horn-like organs (Portmann, 1959) so common to northern ungulates, but it does identify the ecological
conditions when such horn-like organs may
evolve.
16) Daily, seasonal, and annual variation
in availability of forage may result in a
population assuming different social organizations. (Ecological parameter: shortterm fluctuations of resource availability.)
Many authors have commented on the
ability of ungulate populations to alter
their grouping characteristics—apparently
in response to differences in the availability
of food and cover. Some of the most striking changes are seen in usually solitary
species once they are on open plains away
from cover, as indicated earlier for roe deer,
white-tailed deer, and reed buck. Moose
may also congregate in open areas, such as
old burns. The largest group I saw exceeded 36 moose, essentially in "one bunch"
on an open snow-covered hillside. Group
sizes in African ungulates tend to increase
SOCIAL EVOLUTION AND ECOLOGY IN UNGULATES
as the forage resources decrease (see Bourliere and Hadley, 1970; Estes, 1974), which
is also accepted knowledge for northern ungulates. Thus, moose are more likely to be
in groups in early winter or during the
spring migration than during summer
(Geist, 1963; Houston, 1968). High snowfall may concentrate ungulates and produce
a social system quite different to mat during low snow levels as I found studying
mountain goats (Geist, 1965). Migration
imposed on a species may change its patterns of territoriality as described for gnu
by Estes (1969). A comparison of Alpine
ibex (Capra ibex) and Walia ibex (C. walie)
showed differences in grouping tendencies
that could be ascribed to climatic parameters controlling the duration of the rutting
seasons (Nievergelt, 1974). However, a great
difference in density between a population
of Ovis dalli stonei and Ovis canadensis
canadensis did not produce any marked
differences in the social structure (Geist,
1971a). For further examples, I refer to
Estes (1974).
DISCUSSION
The foregoing 16 hypotheses contained
12 ecological variables or perhaps 13, if
sudden habitat availability leading to colonization is taken as a special case (ecological parameters: fiber content of forage,
primary annual productivity, relative biomass of plants, plant species diversity, productivity gradient within habitat, productivity fluctuation in time, habitat stability,
food availability, three-dimensional structure of habitat, climax versus serai plant
communities, predator density, predator
diversity). These hypotheses were able to
explain much of the behavior and social
organization of ungulates from habitats as
diverse as tropical rainforest or periglacial
tundra. However, it is expected that further
hypotheses will need to be formulated to
explain, for instance, why most Old World
deer (Plesiometecarpalia) are harem-herders, while New World deer (Telemetecarpalia) defend only females in heat, as my
recent unpublished studies and the dispersed literature on cervids indicates. In
217
addition, I largely excluded consideration
of special cases, such as the evolution of
delayed implantation in roe deer, which is
apparently an adaptation to avoid rutting
in winter by a small-bodied deer and has
various secondary consequences on the behavior and biology of this species. Nor did
I discuss the combat adaptations of ungulates as they relate to social behavior and
social structure, since there is no apparent
relationship between the ecology of ungulates and their mode of intraspecific combat, and since I discussed this in detail
elsewhere (Geist, 1966a, 1971a). It is sufficient to say that combat adaptations are an
important non-ecological variable in the
social behavior and social organization of
ungulates.
It may be noteworthy that the 16 hypotheses discussed are linked easily to one
another and explain rules from seemingly
unrelated biological disciplines. If hypothesis 8 were false, so would be 9, 10, 12, and
13. The Jarman-Bell principle can be extended into paleontology to explain why
perissodactyls and proboscidians have been
orders of giants. This principle also permits us to speculate that the American
ground sloths which reached gigantic size
were probably relatively rare animals that
used huge amounts of food, reproduced
little, and had little to fear from common
predators, all of which made them most
susceptible to over-hunting by early man
in America (see Martin and Wright, 1967).
The dispersal theory explains some old
paleontological laws, such as Dollo's law
of the irreversibility of evolution; Cope's
law that primitive forms give rise to many
specialized forms; the trend in the evolution of mammals towards larger body size;
and, in combination with hypothesis 15, it
explains the evolution of huge horn-like
organs in ungulates from the Pleistocene.
This theory also reconciles Darlington's
and Mathew's view of biogeography and
evolution in mammals as indicated earlier.
The dispersal theory itself unites principles
from diverse biological disciplines.
An important set of rules that explains
why ecological and social adaptations may
be at times unrelated or only indirectly
218
VALERIUS GEIST
related is Edinger's principle (hypothesis
14) and Krumbiegel's rule (Krumbiegel,
1954). Krumbiegel elevated to a rule the
observation that behavior patterns may
continue to exist long after the appropriate
organs or habitat conditions have vanished. These rules indicate that behavioral
adaptations may be slow to change and are
hence rather conservative, while ecological
adaptations may proceed at a faster rate.
Clearly, this predicts that ecologically diverse but closely related species found allopatrically will have very similar social behavior. (Where species are sympatric we
may expect also a divergence in social behavior patterns to reduce ambiguity and
hybridization.) This does not contradict
the predictions of the dispersal theory that
ecological and social specializations may
evolve in parallel, in the sense of advancing
in parallel. Hence, ecological and social
selection appear to exist as largely separate
spheres of natural selection, as I had to conclude on the basis of empirical studies on
mountain bovids (Geist, 1971a).
REFERENCES
Azrin, N. H., R. R. Hutchinson, and R. McLaughlin. 1965. The opportunity for aggression as an
operant reinforcer during aversive stimulation.
J. Exp. Anal. Behav. 8:171-80.
Baker, H. G. 1970. Evolution in the tropics. Biotropica 2:101-11.
Bannikov, A. G., L. V. Zhirnov, L. S. Levedeva, and
A. A. Fandeev. 1961. Biology of. the saiga. English
translation. U.S. Dept. of Commerce. Springfield,
Va.
Bell, R. H. V. 1971. A grazing ecosystem in the
Serengeti. Sci. Amer. 225(l):86-93.
Bergerud, A. T. 1974. Rutting behaviour of Newfoundland caribou. In V. Geist and F. Walther
[ed.]. The behaviour of ungulates and its relation
to management. Vol. I. I.U.C.N., Morges. (In
press)
Blaxter, K. L., and R. S. Willson. 1962. The voluntary intake of roughages by steers. Anim. Prod.
4:315-58.
Blaxter, K. L., F. W. Wainman, and R. S. Willson.
1961. The regulation of food intake by sheep.
Anim. Prod. 3:51-56.
Bourliere, F. 1965. Densities and biomasses of some
ungulate populations in eastern Congo and
Rwanda, with notes on population structure and
lion/ungulate ratios. Zool. Afr. 16:199-207.
Bourliere, F., and M. Hadley. 1970. The ecology of
tropical savannas. Annu. Rev. Ecol. Syst. 1:125-52.
Bramley, P. S. 1970. Territoriality and reproductive
behaviour of roe deer. J. Reprod. Fert. Suppl. 11:
43-70.
Brereton, J. L. 1971. A self-regulation to densityindependent continuum in Australian parrots,
and its implication for ecological management,
p. 207-221. In E. Duffey and A. S. Watt [ed.],
The scientific management of animal and plant
communities for conservation. Blackwell, London.
Brody, S. 1945. Bioenergetics and growth. Reinhold
Publ. Co., New York.
Bromley, P. T. 1969. Territoriality in pronghorn
bucks on the National Bison Range, Moise, Montana. J. Mammal. 50:81-89.
Brown, J. L. 1964. The evolution of diversity in
avian territorial systems. Wilson Bull. T6:160-69.
Crook, J. H. 1970. The socio-ecology of primates,
p. 103-168. In J. H. Crook [ed.], Social behaviour
in birds and mammals. Academic Press, London.
Cowley, J. J. 1970. Food intake and the modification
of behaviour, p. 167-220. In A. Watson [ed.], Animal populations in relation to their food resources. Blackwell, Oxford.
Cumming, G. H. 1966. Cited in Bramley, 1970.
Darling, F. F. 1937. A herd of red deer: a study in
animal behaviour. Oxford Univ. Press, London.
Darlington, P. J. 1957. Zoogeography: The geographic distribution of animals. John Wiley, New
York.
de Bock, E. A. 1970. On the behavior of the mountain goat (Oreamnos americanus) in Kootenay National Park. Master's Thesis. The University of
Alberta, Edmonton.
Dubos, R. 1968. So human an animal. C. Scribner's
Sons, New York.
Eisenberg, J. F., and M. Lockhart. 1972. An ecological reconnaissance of Wilpattu National Park,
Ceylon. Smithsonian Contrib. Zool. No. 101. 118 p.
Edinger, T. 1948. Evolution of the horse brain. Geol.
Soc. Amcr. Mem. 25.
Elliot, R. C, and J. H. Topps. 1963. Voluntary intake of low protein diets by sheep. Anim. Prod.
5:269-76.
Estes, R. D. 1969. Territorial behaviour of the wildebeest (Connochaetes taurinus Burchell, 1823). Z.
Tierpsychol. 26:284-370.
Estes, R. D. 1974. Social organization of the African
bovids. In V. Geist and F. Walther [ed.], The
behaviour of ungulates and its relation to management. Vol. I. I.U.C.N., Morges. (In press)
Galef, B. G. 1970. Target novelty elicits and directs
shock-associated aggression in wild rats. J. Comp.
Physiol. Psychol. 71:87-91.
Geist, V. 1963. On the behaviour of the North
American moose {Alces alces andersoni Peterson,
1950) in British Columbia. Behaviour 20:377-416.
Geist, V. 1965. On the rutting behavior of the
mountain goat. J. Mammal. 45:551-68.
Geist, V. 1966a. On the behaviour and evolution of
American mountain sheep. Ph.D. Diss. The University of British Columbia, Vancouver.
Geist, V. 1966b. The evolution of horn-like organs.
Behaviour 27:175-214.
SOCIAL EVOLUTION AND ECOLOGY IN UNGULATES
Geist, V. 1967. A consequence of togetherness. Natur.
Hist. 76:24-30.
Geist, V. 1971a. Mountain sheep: a study in behavior and evolution. Univ. Chicago Press, Chicago.
Geist, V. 19716. On the relation of the social evolution and dispersal in ungulates during the Pleistocene, with emphasis on the Old World Deer and
the genus Bison. Quat. Res. 1:283-315.
Geist, V. 1971c. A behavioural approach to the management of wild ungulates, p. 413-424. In E. Duffey and A. S. Watt [ed.], The scientific management of animal and plant communities for conservation. Blackwell, London.
Geist, V. 1974. On the relationship of ecology and
behaviour in the evolution of ungulates: theoretical considerations. In V. Geist and F. Walther
[ed.], The behaviour of ungulates and its relation
to management. Vol. I. I.U.C.N., Morges. (In
press)
Graham, N. McC. 1964. Maintenance requirements
of sheep indoors and at pasture. Proc. Aust. Soc.
Anim. Prod. 5:272-74.
Grim, R. 1970. Blaubockchen (Cephalophus monticola Thurnberg, 1798; Cephalopinae, Bovidae) als
Insectenfresser. Z. Saugetierk. 35:357-59.
Harris, L. D. 1972. An ecological description of a
semi-arid East African ecosystem. Colorado State
University Range Science Dept. Series, No. 11. 80
?•
Hibbs, L. D. 1966. A literature review of mountain
goat ecology. Colorado Dept. of Game, Fish and
Parks Special Report, No. 8. 23 p.
Hindrichs, H. 1971. Freiland Beobachtungen zum
Sozialsystem des Afrikanischen Elephanten, Loxodonta africana (Blumback, 1797), p. 11-74. In
H. Hindrichs and U. Hindrichs [ed.], Dikdik und
Elephanten. Pieper, Munchen.
Hindrichs, H., and U. Hindrichs. 1971. Freiland
Untersuchungen zur Okologie und Ethologie der
Zwerg-Antilope Madoqua (Rhynchotragus) kirki
(GUnther, 1880), p. 77-173. In H. Hindrichs and
U. Hindrichs [ed.], Dikdik und Elephanten. Pieper, Munchen.
Hofer, H. 1972. Prolegomena primatologiae, p. 3146. In H. Hofer and G. Altner [ed.], Die Sonderstellung des Menschen. G. Fischer Verlag, Stuttgart.
Hoogerwerf, A. 1970. Udjung Kulon: land of the
last Javan rhinoceros. E. J. Brill, Leiden.
Houston, D. B. 1968. The Shiras moose in Jackson
Hole, Wyoming. Grand Teton Natural History
Association. Technical Bulletin No. 1.
Hunter, R. F. 1962. Hill sheep and their pasture:
A study of sheep grazing in southeast Scotland.
J. Ecol. 50:651-80.
Jarman, P. 1968. The effect of the creation of Lake
Kariba upon the terrestrial ecology of the middle
Zambezi Valley, with particular references to the
large mammals. Ph.D. Diss. Manchester Univ.
Library.
Jordan, C. F. 1971. A world pattern in plant energetics. Amer. Sri. 59:425-33.
Jungius, H. 1971. The biology and behaviour of the
219
reed buck in the Kruger National Park: Mammalia depicta. P. Parey Verlag, Hamburg. 106 p.
Klingel, H. 1974. A comparison of the social behaviour of equids. In V. Geist and F. Walther [ed.],
The behaviour of ungulates and its relation to
management. Vol. 1. I.U.C.N., Morges. (In press)
Kramer, A. 1969. Soziale Organization und Sozialverhalten einer Gemspopulation (Rupicapra rupicapra L.) der Alpen. Z. Tierpsychol. 26:889-964.
Krumbiegel, T. 1954. Biologie der Saueetiere. Vol.
II. AGIS Verlag, Krefeld. "
Kruuk, H. 1972. The spotted hyena: a study in predation and social behavior. Univ. Chicago Press,
Chicago.
Kurt, F. 1963. Zur Carnivorie bei Cephalophus dorsalis. Z. Saugetierk. 28:309-13.
Kurt, F. 1968. Das Sozialverhalten des Rehes. Mammalia depicta. P. Parey, Berlin. 102 p.
Kurt, F. 1970. Rehwild. Bayerischer Landwirtschafts
Verlag, Munchen.
Lettow-Vorbeck, G. V., and W. Rieck. 1956. In F. V.
Raesfeld. Das Rehwild. 4th ed. P. Parey Verlag,
Berlin.
Leuthold, W. 1974. Observations on home range and
social organization of lesser kudu, Tragelaphus
imberbis (Blyth, 1869). In V. Geist and F. Walther
[ed.], The behaviour of ungulates and its relation
to management. Vol. I. I.U.C.N., Morges. (In
press)
Martin, P. S., and H. E. Wright, Jr. [Ed.] 1967.
Pleistocene extinctions. Yale Univ. Press, New
Haven.
Mathew, W. D. 1915. Climate and evolution. Ann.
N.Y. Acad. Sci. 24:171-318.
Mayr, E. 196. Animal species and evolution. Belknap, Harvard Univ. Press, Cambridge, Mass.
Mech, L. D. 1966. The wolves of Isle Royale. U.S.
Nat. Park Serv. Fauna Series, No. 7.
Nievergelt, B. 1974. The reproductive cycle and
grouping behaviour in the Ethiopian ibex, with
comparisons to the Alpine ibex. In V. Geist and
F. Walther [ed.], The behaviour of ungulates and
its relation to management. Vol. I. I.U.C.N.,
Morges. (In press)
Orians, G. H. 1969. On the evolution of mating systems in birds and mammals. Amer. Natur. 103:
589-603.
Pedersen, A. 1958. Der Moschusochs (Ovibos moschatus Zimmermann). Neue Brehm Bucherei. A.
Ziemsen Verlag, Wittenberg-Lutherstadt. 54 p.
Portmann, A. 1959. Einfiihrung in die Vergleichende
Morphologie der Wirbeltiere. Schwabe and Co.,
Basel.
Rails, Kathrine. 1971. Mammalian scent marking.
Science 171:443-49.
Schaller, G. B. 1967. The deer and the tiger. Univ.
Chicago Press, Chicago.
Schaller, G. B. 1972. The Serengeti lion: a study in
predator-prey relations. Univ. Chicago Press, Chicago.
Schenkel, R. 1966. On sociology and behaviour in
impala (Aepyceros melampus suara Matchie). Z.
Saugetierk. 31:177-205.
220
VALERIUS GEIST
Schenkel, R., and Schenkel-Hulliger, L. 1969. Ecology and behaviour of the black rhinoceros (Diceros Bicornis L.): Mammalia depicta. P. Parey Verlag, Hamburg. 100 p.
Scott, J. P. 1945. Social behavior, organization and
leadership in a small flock of domestic sheep.
Comp. Psychol. Monogr. 18:1-29.
Scott, W. B. 1937. A history of land mammals in the
western hemisphere. Rev. ed. Reprinted 1962.
Hafner Pub. Co., New York.
Sikes, S. K. 1971. The natural history of the African
elephant: the world naturalist. Weidenfeld and
Nicolson, London.
Simpson, G. G. 1949. The meaning of evolution.
Yale Univ. Press, New Haven, Conn. Reprinted.
Mentor Books, New York.
Sinclair, A. R. E. 1974. The social organization of
the East African buffalo (Syncerus caffer, Sparrman). In V. Geist and F. Walther [ed.], The behaviour of ungulates and its relation to management. Vol. I. I.U.C.N., Morges. (In press)
Sparrow, R. D., and P. F. Springer. 1970. Seasonal
activity patterns of white-tailed deer in eastern
South Dakota. J. Wildlife Manage. 34:420-31.
Tener, J. S. 1965. Muskoxen in Canada. Queen's
Printer, Ottawa.
Thenius, E., and H. Hofer. 1960. Stammesgeschichte
der Saugetiere. Springer Verlag, Berlin.
Ulrich, R. E., and N. H. Azrin. 1962. Reflexive fighting in response to aversive stimulation. J. Exp.
Anal. Behav. 5:511-20.
Verner, J., and M. F. Willson. 1966. The influence
of habitats on mating systems of North American
passerine birds. Ecology 47:143-47.
Walker, E. P. 1964. Mammals of the world. Vol. II.
Johns Hopkins Press, Baltimore, p. 642-1500.
Walther, F. 1958. Zum Kampf- und paarungsverhalten einiger Antilopen. Z. Tierpsychol. 15:34080.
Walther, F. 1964. Verhaltensstudien an der Gattung
Tragelaphus de Blainville (1816) in Gefangenschaft, unter besonderer Beriicksichtigung des Sozialverhaltens. Z. Tierpsychol. 21:393-467.
Walther, F. 1966. Mit Horn und Huf. P. Parey Verlag, Berlin.
Walther, F. 1968. Verhalten der Gazellen. Die Neue
Brehm Bucherei, no. 373. A. Ziemsen Verlag, Wittenberg-Lutherstadt. 144 p.
Watson, A., and R. Moss. 1970. Dominance, spacing
behavior and aggression in relation to population
limitation in vertebrates, p. 167-220. In A. Watson
[ed.], Animal populations in relation to their food
resources. Blackwell, Oxford.
Webster, A. J. F., and K. L. Blaxter. 1966. The
thermal regulation of two breeds of sheep exposed to air temperatures below freezing point.
Res. Vet. Sci. 7:466-79.
Young, B. A. 1971. Application of the carbon dioxide entry rate technique to measurement of
energy expenditure by grazing cattle, p. 237-241.
In 5th Symp. Energy Metabolism of Farm Animals. Joris Druck and Verlag, Zurich.
Young, B. A., and Corbett, J. L. 1968. Energy requirement for maintenance of grazing sheep measured by calorimetric techniques. Proc. Aust. Soc.
Anim. Prod. 1:327-34.