Download MATING SYSTEMS, PHILOPATRY AND DISPERSAL IN BIRDS

Anita. Behav., 1980, 28, 1140-1i62
MATING SYSTEMS, PHILOPATRY AND DISPERSAL IN BIRDS AND
MAMMALS
BY PAUL J. GREENWOOD
School of Biological Sciences, University of Sussex, Brighton, BN1 9 QG*
Abstract. Many species of birds and mammals are faithful to their natal and breeding site or group.
In most of them one sex is more philopatric than the other. In birds it is usually females which disperse
more than males; in mammals it is usually males which disperse more than females. Reproductive
enhancement through increased access to mates or resources and the avoidance of inbreeding are
important in promoting sex differences in dispersal. It is argued that the direction of the sex bias is a
consequence of the type of mating system. Philopatry will favour the evolution of cooperative traits
between members of the sedentary sex. Disruptive acts will be a feature of dispersers.
Faithfulness to a site or group is a well documented trait of many species of birds and mammals. It is particularly striking among adults
which return to breed in the same area in successive years. Migratory birds provide perhaps the
most striking illustrations. In the colonially nesting common tern Sterna hirundo over half the
returning adults reoccupy their previous mating
territory (Austin 1949, 1951). Site fidelity also
occurs in more sedentary species of birds (Werth
1948). Among mammals, primates are often
faithful to territories or home ranges, and boundaries between adjacent individuals or groups
can be stable for long periods (Jolly 1972).
Migratory species (e.g moose Alces alces), like
birds, often return annually to the same summer
range (Houston 1974).
Although many species are philopatric, only a
proportion of individuals of any species is faithful
to one locality. The dispersal of the remainder
may be voluntary or enforced, environmentally
determined or innate (Howard 1960). The importance of dispersal is widely appreciated. It is
increasingly identified as having a major role in
both population regulation (Lidicker 1975) and
spatial distribution (Taylor & Taylor 1977). It
can have substantial effects on the genetic structure of populations. Since dispersal is a prerequisite for gene flow, widespread movement may
disrupt local adaptations; any restriction may
promote inbreeding and the genetic differentiation ofneighbouring groups (Wright 1943, 1946).
Recently the consequences of dispersal (or lack
of it) to the evolution of social and disruptive
behaviour have been discussed (Hamilton 1964,
1972).
*Present Address: Departmentof Adult and Continuing
Education and Department of Zoology, University of
Durham, Durham.
1140
This review examines dispersal in birds and
mammals. In most species juveniles are more
prone to dispersal than adults. A detailed discussion of age differences in dispersal can be
found in Baker (1978). In addition, there are
often sex differences in dispersal in both of these
age classes. Reference has been made to the predominance of male dispersal in many species of
mammals (Lidicker 1975; Clutton-Brock &
Harvey 1976; Packer 1979), but it seems less well
known that a sex bias in the opposite direction
is more commonly recorded in birds (Greenwood
& Harvey 1976a; Greenwood 1978; Baker 1978).
A number of evolutionary hypotheses have
been proposed to explain the occurrence of sex
differences in dispersal, particularly for the male
bias in mammals. These hypotheses will be considered in the light of the converse pattern of
female biased dispersal in most birds. Certain
modifications to these hypotheses will be suggested which stress the importance of mating
systems as a prime determinant of any sex bias
in dispersal and the direction of the bias. The
extent to which any general theory can satisfactorily account for the exceptions to the prevalent
pattern of dispersal within the two groups is
discussed. The final section deals briefly with the
different effects that male and female biased
dispersal have on species' social structures.
Terminology
Any discussion of dispersal is beset with problems of terminology. Authors vary in their use
of terms as a result either of the topic or the
organism of their research, The most widely used
definition of dispersal is that by Howard (1960):
'Dispersal of an individual vertebrate is the
movement the animal makes from its point of
origin to the place where it reproduces or
GREENWOOD: MATING SYSTEMS AND DISPERSAL
would have reproduced if it had survived and
found a mate.'
This refers only to juveniles undergoing a permanent movement from birth site to first breeding or potential breeding site and can perhaps
more correctly be termed natal dispersal This
can be distinguished from breeding dispersal
which is the movement of individuals, which
have reproduced, between successive breeding
sites. The definitions do not specify that the
dispersal is reproductively successful. Gross dispersal refers to the permanent movement of individuals to a new location irrespective of whether
or not they reproduce after dispersing. When an
individual has reproduced following dispersal
the movement can be described as effective
(Greenwood 1978; Shields 1979; see also below).
(For a radically different view of terminologies
see Baker (1978).)
Methods
Details of dispersal in birds and mammals are
shown in Tables I-IV. Species mentioned in the
tables will only be referred to by their common
names in the text. The lists are probably not
exhaustive, but examples have been extracted
from the literature irrespective of the presence
or absence of any sex bias in dispersal. Where
one sex is labelled as the predominant disperser
it does not imply that dispersal is an exclusive
characteristic of that sex. In several instances sex
differences in dispersal have been extrapolated
from the information available, e.g. song thrush
(Davies & Snow 1965), orang-utah (Rodman
1973; Horr 1975). In most cases (see below)
examples have only been used when studies have
been sufficiently detailed for the presence or absence of a sex bias to be detected.
For some species data are available on both
natal and breeding dispersal; in the remainder
the details are either for adults or juveniles. When
studies of the same species have produced different results these have been included in the tables.
Almost invariably natal dispersal is more extensive and over longer distances than breeding dispersal. Consequently sex differences in dispersal
are derived from comparisons within each of
these categories and they may not be comparable
between categories. For example, the breeding
dispersal of adult female pied flycatchers is further than that of adult males. Similarly, the natal
dispersal of females may be further than that of
males (Haartmann 1949). However, the natal
dispersal of males is considerably further than
the breeding dispersal of adult females.
1141
There are three major problems in classifying
patterns of dispersal. First, natal dispersal refers
to individuals which have not yet reproduced,
breeding dispersal to those which have reproduced. Such an unambiguous separation cannot
always be made from the data available. This is
particularly true for small mammals where the
age, size or reproductive condition of a disperser
does not necessarily indicate whether it is undergoing natal or breeding dispersal (Myers &
Krebs I971). However, when members of a
population have been designated as juvenile and
adult I have assumed that the former should be
classified as natal dispersers and the latter as
breeding dispersers. Second, sex differences in
natal or breeding dispersal may not be expressed
in effective dispersal if the predominant dispersing sex suffers a higher rate of mortality.
Similarly, there could be a sex bias in effective
dispersal in species for which no sex difference
in gross dispersal has been found. Unfortunately,
very few studies (Greenwood & Harvey 1976a, b;
Leuze 1976, and in press) have shown that the
costs of dispersal may act differentially on the
sexes. As a result the majority of examples in the
tables indicate differences in gross dispersal.
The importance of differential costs and benefits
of dispersal between the sexes will be considered
later. Third, age and sex differences in dispersal
may vary with population changes in species
subject to wide fluctuations in density (Myers &
Krebs 1971). In these instances I have attempted
to derive an overall average of dispersal for the
different categories.
Dispersal in Birds
The data for natal and breeding dispersal of birds
are shown in Table I, and the results are summarized in Table II. Female biased natal dispersal occurs in the majority of species; only three
are male biased. Breeding dispersal also occurs
predominantly in females. Two studies of one
species have produced different results.
Haartmann (1949) noted female biased natal dispersal in the pied flycatcher whereas similar dispersal of both sexes was recorded for a different
population by Berndt & Sternberg (1969); their
results for breeding dispersal were similar.
The most detailed studies of dispersal in birds
have been those on the pied flycatcher and great
tit (see references in Table I). In a Scandinavian
population of the flycatcher, 7% of males as
compared with 2 7o of females breed for the first
time within their territory of birth. Among
adults, 93 % of males but only 37 % of females
1142
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return each year to their first nesting locality:
61% of females nest in a different place each
year. Among females, those which nest unsuccessfully due, for example, to predation, undergo
greater breeding dispersal than those which do
raise a brood (Haartmann 1949). Predation of
eggs or fledglings has been implicated as a factor
promoting the greater breeding dispersal of females in a number of other species (e.g. yelloweyed penguin, Richdale 1957; reed warbler,
Catchpole 1972). In the great tit, 25 % of males
and 10 % of females have their first territory on,
or adjacent to, their natal one. The modal number of territories moved from birth to first
breeding site is from one to two in males and
from two to three in females (Greenwood et al.
1979a). Among adults, both sexes are as faithful
to their former territory after a successful breeding attempt the year before when re-pairing
either with the same mate or a new bird after the
death of a previous mate. However, following a
divorce, 80 % of males but only 40 % of females
breed within one territory's width of their previous year's nest site. Divorce occurs between at
least 29 % of birds which have the possibility of
re-pairing with the same individual (Harvey et al.
1979).
The pied flycatcher and great tit are both
woodland passerines which defend feeding territories. Sex differences in dispersal are not, however, restricted to species of a particular ecology
or habitat. In the herring gull 77% of males
which return to the colony of their birth breed
within their natal sub-colony whereas the comparable figure for females is 54 %. A larger proportion of females than males are also recruited
into a colony other than that of their birth
(Chabrzyk & Coulson 1976). Likewise in the
colonially breeding red-billed gull, kittiwake, and
Manx shearwater, there is a greater tendency for
females rather than males to disperse from tlleir
natal colony (Mills 1973; Wooller & Coulson
1977; Brooke 1978, respectively).
Table II. The Numbers of Species and Families of Birds
with Female Biased, Male Biased and No Sex Difference
in Natal and Breeding Dispersal
Predominant Dispersing Sex
Breeding
Natal
Male Female Both Male Female Both
Species
Families
3
1
21
11
6
5
3
1
25
14
1
1
28,
4
Striking examples of sex differences in natal
dispersal occur in several species of communally
breeding birds. In several species of babblers
most females leave their natal group prior to
breeding. The majority of males remain as members of their group of birth (Zahavi 1974;
Gaston 1976, 1978). A similar sex bias occurs in
the Florida scrub jay, which lives in stable groups
consisting of a breeding pair and their young of
previous years. The non-breeding offspring assist
in the feeding of related nestlings. Accession is
patrilineal and a male which inherits its natal
territory, or one adjacent to it, pairs with an immigrant female (Woolfenden 1975; Woolfenden
& Fitzpatrick 1978). The absence or infrequency
of breeding dispersal is a feature of this type of
communal breeding system. Greater female n a t a l
dispersal is not however an invariable rule among
such species. The Mexican jay lives in social,
stable and sedentary units of 8-22 birds. Each
unit defends a territory within which one to four
pairs may nest simultaneously in separate nests
(J. L. Brown 1974). The majority of offspring
remain within their natal unit to breed and both
sexes are equally represented among the few
which do disperse to nearby groups (J. L. Brown,
personal communication).
Exceptions to the prevalent pattern of female
biased dispersal in birds have been reported in
only one family, the Anatidae. The lesser snow
goose is the best documented example of male
biased natal and breeding dispersal (Cooke et al.
1975). As with many other species of geese and
ducks, pair formation occurs during spring migration or on the wintering grounds. At such
times, individuals from different colonies may
intermingle and pair; males return to the females'
natal colony to breed. This is the pattern of dispersal in males nesting for the first time and
adults re-pairing after the loss of a former mate.
There are a number of other species of Anatidae
in which the faithfulness of females to previous
nest sites is well known (e.g. Sowls 1955; Gates
1962; Doty & Lee 1974). In most of these, however, the relative patterns of dispersal of males
and females are unknown. Baker (1978) in fact
has overestimated the amount of evidence for
male biased dispersal in ducks. However, o n e
species, the pintail, does have male biased dispersal and there is suggestive evidence for similar
patterns in two others, the common shelduck and
long-tailed duck (Young 1970; Alison 1975,
1977).
Over 90 % of bird species are monogamous or
at most only facultatively polygamous (Lack
GREENWOOD: MATING SYSTEMS AND DISPERSAL
1968). Because of this, the information on dispersal is predominantly for those species with
this type of pair bond. An exception is the whitebearded manakin, a lek species. Male manakins
aggregate in groups of up to 60 birds at traditional arenas during the breeding season. There
is intense competition to achieve lek status, but
once an individual has established a display territory, it is usually resident for a prolonged period.
There is very little male movement between leks.
Breeding females, on the other hand, are much
more mobile, frequently mating at different leks
in different seasons (Lill 1974).
Dispersal in Mammals
The data for natal and breeding dispersal in
mammals are shown in Table III, and the results
are summarized in Table IV. Male biased natal
dispersal occurs in the majority of mammals;
only five are female biased. Breeding dispersal
also occurs predominantly in males.
The breeding systems of mammals vary from
the comparatively open asocial dispersions of
numerous species of small rodents to the semiclosed, highly structured social units typical of
many primates (Eisenberg 1966); a number of
both types are monogamous (see Kleiman 1977).
Sex differences in dispersal are not confined to
species with a particular social structure, although social structure may influence the degree
of difference in dispersal between the sexes (see
below).
In some rodents, similar and substantial proportions of juveniles of both sexes m a y leave
their natal area, particularly in those species
which undergo marked fluctuations in density.
These species often have dispersal biased in
favour of males in older age classes (Krebs et al.
1976). Male biased natal dispersal is a characteristie feature of sciurid social systems (Lidicker
1975). In a number of species, females remain
close to their birth site and occupy home ranges
adjacent to their mothers and siblings (Yeaton
1972; Sherman 1977; Dunford 1977). This arrangement was probably the incipient evolutionary stage in the progression to the more complex
matrilineal units of marmots, where females may
remain within their maternal group (e.g. yellowbellied marmot, Armitage 1973, 1974). In those
species in which males do not apparently maintain exclusive access to one or a number of
females during the reproductive period, breeding
dispersal is male biased. Conversely, male-female
relations are stable and long-lasting in marmots
and prairie dogs, and adults of both sexes may
1145
disperse together (King 1955; Armitage 1974).
For example, new coteries are almost invariably
established by adult black-tailed prairie dogs,
leaving offspring to retain the natal burrow (King
1955).
Studies of primates have yielded perhaps the
most detailed information on natal and breeding
dispersal in mammals. Several species exemplify
the semi-closed polygynous societies in which
movement between groups is often a characteristic of the male. Examples range from the multimale troops of the olive baboon (Packer 1979)
and Japanese monkey (Itani 1972; Sugiyama
1976) to the single male troops of the Hanuman
langur (Hrdy 1977). Of 50 olive baboons which
transferred between troops in a nine-year period
only two were females. In addition, all males left
their natal troop prior to breeding (Packer 1979).
Similarly, in the Japanese monkey the majority,
if not all, of males undergo natal dispersal (Itani
1972).
Although the majority of highly social polygynous mammals have male biased dispersal, it is
not an invariable rule. The plains zebra is one
species in which natal dispersal occurs in both
sexes. It has a harem breeding system consisting
of one stallion and one to several mares with
foals. Young males leave voluntarily and join
bachelor groups; young mares are abducted by
stallions during oestrus (Klingel 1969). A similar
pattern of dispersal occurs in the hamadryas baboon (Kummer 1968).
In monogamous species (e.g. dik-dik, lar gibbon) offspring of both sexes leave their natal
territories. For example, a male gibbon which
reaches sexual maturity is driven out by its
father, a female by its mother (Carpenter 1940).
The conventional interpretation is that both
sexes have dispersed or transferred (Itani 1972;
Packer 1979). In the absence of more detailed
information, I have acceded to that classification.
However, by analogy with the situation in monogamous birds, it could well be that one sex is
more likely than the other to breed closer to the
natal territory.
Only recently has female biased dispersal been
documented in mammals. Currently, five species
have been reported with this pattern for natal
dispersal and two for breeding dispersal, but
with long-term studies in progress more can be
expected. Most individuals undergoing natal dispersal are female in one species of lagomorph,
the pika (A. T.~Smith 1974, 1978). In the field
vole, natal dispersal is male biased but adult females change breeding sites more readily than
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GREENWOOD: MATING SYSTEMS AND DISPERSAL
do males (Myllym~iki 1977). More marked sex
differences in dispersal occur in the chimpanzee
and the wild hunting dog. Male chimpanzees live
in patrilineal communities in which several adult
males share a common home range that may
encompass the overlapping and smaller ranges
of females. At various times females may associate with males from two adjacent communities,
and nulliparous females transfer permanently to
a new community from their natal one (Pusey,
in press; Nishida, in press). African wild dogs
have a social organization consisting of one reproductive pair and their pups plus a cooperative
group of non-breeding adults (usually male)
which assist in the rearing of the young. Female
biased natal dispersal is divisible into two components. First, all female offspring leave their
natal pack and males usually remain. Second,
although females (often sisters) frequently transfer together, only one female eventually breeds
in each pack; the remaining individuals may subsequently undergo further natal dispersal (Frame
& Frame 1976). The sex difference in dispersal in
the gorilla is likewise associated with patrilineal
inheritance, although some males do leave the
unit of their birth. The gorilla social system is,
in terms of reproduction, effectively a single male
group. An old silverback male is eventually replaced by a younger one born into the unit and
which is probably its son. Those males which disperse attempt to attract females and thus form a
new group. On the other hand, nearly all females
leave their natal group at maturity and about
half join an established unit, the remainder a
lone male (Harcourt et al. 1976). The final example is the white-lined bat. Single males defend
foraging territories and harems o f females are
distributed among them. Tannenbaum (1975)
has shown that male offspring often establish
territories close to their parental one whereas
only a small fraction of females breed in the vicinity of their birth site.
Table IV. The Numbers of Species and Families of Mammals with Female Biased, Male Biased and No Sex
Difference in Natal and Breeding Dispersal
Predominant Dispersing Sex
Natal
Breeding
Male Female Both Male Female Both
Species
Families
45
23
5
4
15
7
21
6
2
2
2
2
1149
Factors Promoting S e x Differences in Dispersal
What are the salient ecological or behavioural
factors that account for the apparent differences
in sex biased dispersal between birds and mammals ? The problem is not one of producing alternative hypotheses for birds and mammals per se;
rather it is to identify underlying similarities that
may account for female biased as opposed to
male biased dispersal, irrespective of the vertebrate class. To help to clarify the problem this
section has three purposes: (i) to discuss a number of recent evolutionary explanations for sex
differences in dispersal; (ii) to highlight a number
of factors that are known to influence dispersal
and the reasons why they may or may not promote a sex bias; and (iii) to evaluate whether
these factors can satisfactorily account for the
direction of the sex bias.
Sex Chromosomes
Females are the heterogametic sex in birds;
males are the heterogametic sex in mammals.
Whitney (1976), extrapolating from Hamilton
(1972), proposed that sex chromosome asymmetries would result in the evolution of greater
female sociality in mammals and male sociality
in birds. Criticisms by Kurland (in press), on the
basis of the probable outcome of intra-genome
conflict, make the hypothesis largely untenable
as an explanation for the matrilineal social structure common in mammals or the patrilineal
organizations of communal birds. Likewise it
cannot be considered as a basis for differential dispersal of the sexes, Nor is it likely that the presence of sex-linked deleterious genes would result
in the preferential avoidance o f inbreeding by
the heterogametic sex. In addition, there is no
clear cut division between the two taxonomic
groups of female biased as opposed to male
biased dispersal. Finally, there are simpler
explanations for the observed sex bias in sociality
between some birds and mammals that take into
account sex differences in dispersal (see below).
Dominance
A second general theory for sex biased dispersal is that by Gauthreaux (1978). He has produced a behavioural dominance theory to account for age and sex differences in dispersal.
Notwithstanding that subordinate and young individuals are frequent dispersers, his view that
male dominance over females provides a causal
explanation for greater female dispersal is erroneous. Males are dominant to females in some
contexts in many species of higher vertebrates (see
1150
ANIMAL
BEHAVIOUR,
Wilson 1975; Rails 1976), but that fact could
hardly account for dispersal being female biased
in most birds and male biased in most mammals.
Among the exceptions to this male-female relation are the spotted hyena, where females are
dominant to males yet males disperse (Kruuk
1972), and in birds of prey, where the larger females are dominant to males yet female biased
natal dispersal occurs, in the sparrowhawk
(Newton, personal communication) and the
hobby (Fiuczynski 1978).
Environmental Change
A sex bias in dispersal is unlikely to be associated with major changes in the distribution of
resources (e.g. food, breeding sites) if both sexes
would benefit from moving (see Baker 1978). An
interpretation of the high level of dispersal in the
greenfinch is based on the relatively unpredictable nature of its food supply (Greenwood &
Harvey 1977). Likewise, a marked skew in the
sex ratio of dispersers compared to the population as a whole should not be apparent when
species, such as small rodents, are at or above
the carrying capacity of their habitat, unless
male and female thresholds to change are different or the life history of a species in a fluctuating
habitat facilitates the transport of progeny by
only one of the sexes (see Lidicker 1975).
Species of birds and mammals have a wide
diversity of life histories. Despite the marked
differences in the modes of reproduction between
the two taxa, it is unlikely that environmental
change affects them in sufficiently different ways
to account for the general patterns of sex biased
dispersal. In fact, it appears that sex differences
in dispersal occur most markedly in species inhabiting stable and predictable habitats, which
is not to say that all species in such habitats will
have a sex bias.
Population Density
Dispersal may have a major role in the population control of many species of birds and mammals. Individuals forced to disperse are frequently the socially subordinate, younger and
weaker members of the population (for reviews
see Archer 1970; Watson & Moss 1970;
Lidicker 1975). High or increasing population
densities may be associated with high levels of
dispersal (Myers & Krebs 1971). The question
that concerns us here, however, is whether fluctuations in density alter the relative patterns of
male and female dispersal. In other words, is
there a consistent sex bias within a species irre-
28, 4
spective of population size ? Some small rodents
may experience substantial changes in density
within and between breeding seasons. Such
species also provide examples where the sex ratio
of dispersers may vary over time (e.g meadow
mouse, Myers & Krebs 1971; Townsend's
meadow mouse, Krebs et al. 1976), although
changes in the sex ratio do not appear to be
closely aligned to changes in population density.
In species less subject to wide variations in
population size, an underlying sex bias in either
natal or breeding dispersal is not markedly
altered by density changes (e.g. greater male than
female dispersal in the yellow-bellied marmot
(Armitage 1973) and the round-tailed ground
squirrel (Dunford 1977)). Nevertheless, it would
be wrong to assume that changes in density produce equivalent effects on different components
within a population. In the great tit, increased
breeding density is related to increased effective
natal dispersal of males, measured in terms of the
number of territories moved. Females, on the
other hand, have a similar pattern of effective
natal dispersal each year with no comparable
density effect. Even so, within the upper and
lower limits of observed breeding densities,
greater male than female dispersal has been noted
in only one of 12 years (Greenwood et al. 1979a).
To summarize, although population density
can affect the degree of sex bias in dispersal, there
does not appear to be a consistent pattern whereby changes in species' densities accentuate or
diminish underlying sex differences in dispersal.
Avoidance of Inbreeding
Since Lincoln (1934) many authors have felt
that the dispersal of offspring from their natal
group or area functions, in part, as an inbreeding
avoidance mechanism (e.g. Howard 1960;
Lidicker 1962; Itani 1972; Bischof 1975;
Greenwood & Harvey 1976a). Nevertheless,
there is only a limited amount of field evidence
from vertebrates to substantiate laboratory work
(Sittman et al. 1966; Hill 1974) that close inbreeding is harmful. Great tits which mate with
close relatives have a lower than expected nesting
success (Greenwood et al. 1978). The viability of
offspring sired by a male olive baboon which
mated with probable female relatives was substantially less than that of outbred young (Packer
1979). To what extent then are sex differences in
dispersal a result of avoiding such matings 9.
Unfortunately there are very few species for
which good data are available, The study by
Packer (t979) of the olive baboon is the best so
GREENWOOD: MATING SYSTEMS AND DISPERSAL
far. The reproductive activity of males prior to
natal dispersal is low in the troop of their birth
and they do not compete for access to females.
These males are attracted to oestrous females in
neighbouring groups and females may solicit the
attention of potential dispersers. Despite the fact
that there may be difficulties in joining a new
troop due to the aggression of resident males,
the costs of male natal dispersal are less than the
probable costs of inbreeding. Similar patterns
of voluntary dispersal of pubescent males in a
number of primate species may have an equivalent function (e.g. Japanese monkey, Itani 1972;
rhesus monkey, Drickamer & Vessey 1973),
though in others inter-male conflict may be a
proximate cause of subordinate male dispersal
(e.g. toque monkey, Dittus 1975).
Inbreeding avoidance also provides a possible
explanation for the female natal dispersal which
occurs in several social mammals. In the plains
zebra, males may have tenure of a group for
sufficiently long for their own daughters to come
into reproductive condition: Indeed, Klingel
(1969) considers the prominent oestrous posture
of young mares within their natal group to be a
means of eliciting their abduction by unrelated
stallions. Female transfer also occurs in the
gorilla, where a son may take over the natal
group when his father dies (Harcourt et al. 1976).
An alternative explanation for female transfer in
the gorilla as a means of reproductive enhancement is given by Baker (1978). Females move to
groups with a high ratio of silverback males to
females. Baker argues that this will result in
greater protection from predators to the transferring female. However, it seems more likely
that the initial impetus for leaving the natal
group is to avoid inbreeding and that choosing
the best available group is a secondary advantage. In the two species of mammals in which
males are philopatric and form cooperative kin
groups (African hunting dog, chimpanzee), the
dispersal of females has also been interpreted as
an inbreeding avoidance mechanism (Packer
1979; Pusey, in press).
Although there are exceptions, the prevailing
means of avoiding inbreeding in mammals is
through male dispersal. Packer (1979) believes
that the asymmetry originated and is maintained
through the advantages to males of gaining access to a large number of females (see below). In
birds, inbreeding avoidance is achieved in highly
social cooperative species by female natal dispersal (e.g. Zahavi 1974; Woolfenden 1975;
Gaston 1976, 1978; Woolfenden & Fitzpatrick
1151
1978) and may also contribute to the asymmetry
in dispersal in more asocial species (Greenwood
& Harvey 1976a; Greenwood et al. 1978).
Whether the dispersal functions to prevent close
inbreeding has yet to be elucidated but it is a
possible interpretation. The fidelity of a high
proportion of both sexes to their natal group in
the Mexican jay (J. L. Brown, personal communication) may be a rare example of endogamy in
higher vertebrates.
Whilst it is probable that sex differences in dispersal in some species are maintained by the
detrimental effects of inbreeding, it is obvious
that the avoidance of such matings does not provide much insight into the direction of the sex
bias. In polygynous species the costs of inbreeding are probably greater for females than for
males, as a consequence of the larger investment
by the former in offspring and their more limited
reproductive potential (Clutton-Brock & Harvey
1976; see also Bengtsson 1978; Maynard Smith
1978). If inbreeding avoidance is the sole basis
for dispersal then the sex subject to the greater
cost of inbreeding should be more likely to disperse. This is clearly not the case in mammals,
where most species are polygynous. In monogamous birds, on the other hand, females disperse even though the costs of inbreeding are
probably similar for males and females.
Access to Mates and Reproductive Enhancement
The problem of which sex should benefit most
from dispersal has been considered by CluttonBrock & Harvey (1976) and Packer (1979), and
briefly by Trivers (1972) and Wilson (1975). (A
much more detailed synthesis by Baker (1978) is
discussed in the next section.) Taking polygynous
mammals as the example, the arguments have
normally proceeded along the following lines.
Females invest heavily in offspring and are the
limiting sex; males invest relatively little and
compete for access to females. Greater benefits
thus accrue to males gaining access to a large
number of females than vice versa. One means
of achieving this is through greater mobility,
even at the expense of an increased risk of death
if this is offset by reproductive enhancement.
Since intra-sexual competition is also more intense among males than females, a large proportion of males may be denied access to females:
hence greater male dispersal in search of available mates or a pre-reproductive period spent
peripheral to groups of females.
The information that is available on polygynous mammals certainly makes these hypotheses
1152
ANIMAL
BEHAVIOUR,
appear plausible. Female rhesus monkeys live in
stable groups and sexually mature males frequently transfer between them during the breeding season. Those males which copulate the most
within one group are more likely to transfer to
another. There is also a tendency for the breeding dispersal to be from groups with few available
females to those with a larger number (Lindburg
1969; Drickamer & Vessey 1973). A similar picture emerges from Packer's (1979) detailed study
of the olive baboon. Breeding males which have
above average reproductive activity in one troop
regularly transfer into troops with larger numbers of oestrous females. Among adult male grey
squirrels, a higher proportion of copulations is
achieved by mobile individuals (i.e. those undergoing greater breeding dispersal) than sedentary
ones (Thompson 1977).
Considered in isolation, the explanations for
male biased dispersal in mammals may seem entirely appropriate. However, extrapolation of the
hypotheses to birds would similarly predict
greater male dispersal even though the majority
of species are monogamous. About one third of
male great tits are suspected of not breeding in
their first year (Bulmer & Perrins 1973) and the
inter-year differences in natal dispersal are consistent with the view that competition for territories is more severe among males than females
(Greenwood et al. 1979a). Nevertheless, female
natal dispersal is greater than that of males. In
the pied flycatcher, the female bias in dispersal is
more pronounced in populations where a higher
proportion of males are polygynous (cf.
Haartmann 1949; Berndt & Sternberg 1969;
Baker 1978), whereas inter-male competition in
mammals is associated with greater male dispersal (e.g. Sugiyama 1965; Sadleir 1965). Likewise, reproductive enhancement through dispersal is more characteristic of females in many
species of sedentary birds since they move more
readily than males between breeding sites following unsuccessful nesting attempts (Haartmann
1949; Richdale 1957; Catchpole 1972; Darley et
al. 1977).
Mating Systems and Dispersal
This section presents the hypotheses for the evolution of sex differences in dispersal based on
current interpretations of avian and mammalian
mating systems. Before proceeding with the
hypotheses it is worth drawing attention to a
recent publication by Baker (1978) which discusses at length intraspecific variation in the inci-
28, 4
dence of dispersal. Baker deals extensively with
age differences in dispersal and variations in the
tendencies to disperse between species living in
groups, in homes ranges and those undergoing
seasonal migrations. Independently, we have
reached similar conclusions for the evolution of
sex biased dispersal in birds (Greenwood &
Harvey 1976a; Greenwood 1978), although the
occurrence of greater female dispersal is much
more widespread than that indicated by Baker
(1978) if one considers more recent information
than was available to him. We differ in our explanations for the evolution of male biased dispersal in mammals. Baker (1978) concentrates
mainly on intra-sexual variation in mammalian
dispersal but also stresses the importance o f
polygamy and greater female investment in resources and offspring in contributing to a male
bias in dispersal. Some of the arguments are similar to those of Clutton-Brock & Harvey (1976)
and Packer (1979). I have attempted to derive a
more general hypothesis for sex biased dispersal
within the broader framework of the recent reappraisals of vertebrate mating systems (e.g.
Bradbury & Vehrencamp 1977a; Emlen & Oring
1977). This attempt has been aided, in part, by
access to information (unavailable to Baker) on
the social structure and dynamics of a number
of species of mammals with female biased dispersaI.
Resource Defence and Female Biased Dispersal
One feature common to bird species with female biased dispersal is that the male defends a
resource which is of paramount importance to
the acquisition of a mate or to the rearing of offspring. Competition between males for females
is mediated through their ability to hold a resource rather than their capacity to defend females. Female choice of mates is effectively
superimposed upon a mating system that involves the division of resources by males. The
resources themselves need not be of direct benefit
to the female, but could simply provide her with
a means of assessing the quality of a male. Such
a resource defence system (see J. L. Brown 1964;
Emlen & Oring 1977; Bradbury & Vehrencamp
1977a) provides little scope for male desertion,
but does not necessarily mean that males contribute to the rearing of offspring when considerable expenditure is required to secure and hold a
resource. Nevertheless, resource defence mating
systems, especially in birds, are often monogamous with both parents helping to raise young.
In other words, monogamy and female biased
GREENWOOD: MATING SYSTEMS AND DISPERSAL
dispersal can both be a consequence of a resource
defence mating system.
I propose that the philopatry of males is the
result of two factors. First, the comparative ease
with which a male can acquire the resources
necessary to attract females. This assumes that
an individual is more able to establish a breeding
territory in its natal area than elsewhere. It could
be facilitated through familiarity with the locality
that would by implication engender costs to dispersing to unknown areas (e.g. lower feeding
rates, higher risks of predation). A further possibility is that prior residency or familiarity are
important factors, in terms of inter-male competition, in the acquisition of a territory. In some
instances the securing of a resource could be assisted by the close proximity of relatives. Philoparry would thus be a consequence of resource
competition with the advantages accruing to the
sedentary rather than the dispersing individual.
In the event of selecting and holding a substandard territory, there would be little opportunity to
vacate an area to seek a better one (breeding
dispersal). This should be particularly evident
when competition for resources is high and a
proportion of males are prevented from breeding
(for a similar viewpoint see Baker 1978). The
second factor that may impose philopatry on
males may be the result of female choice. Though
females may refrain from breeding with close relatives they may preferentially mate with males of
as similar a genotype as possible without incurring the costs of inbreeding depression (Shields
1979). Males which disperse may be able to acquire a territory but not a mate because they are
recognized or ignored as unfamiliar. Both proposals are amenable to experimentation, though
the second factor may be of lesser importance in
producing sex differences in dispersal. It could
however explain why both sexes in many species
have a tendency to be philopatric.
A mating system that results from the partitioning of resources by males prior to the selection of mates by females should result in female
dispersal. Females do not normally have the
costly constraint of establishing a territory. Instead they have the capacity to choose between
the available resources of different males. Females will have greater flexibility both as juveniles undergoing natal dispersal and as adults
enhancing their reproductive success by breeding
dispersal. When females are the limiting sex,
their potential for rejecting particular males or
the resources they hold should be greater than a
male's potential for rejecting a female. By impli-
1153
cation, the costs of male dispersal are extremely
high and where dispersal has evolved primarily
as an inbreeding avoidance mechanism, females
rather than males would be expected to leave
their natal site or group.
Evidence to support the hypotheses for the
evolution of female biased dispersal is largely
circumstantial. Supportative data can be extracted piecemeal from a number of studies.
Population density in the great tit is positively
related to the number of territories moved by
natal dispersing males but not females, suggesting that competition for territories is more intense among the former. There is additional evidence that males preferentially occupy their natal
territory when there is the chance to do so
(Greenwood et al. 1979a). Whether males prevented from breeding in their natal area are less
successful in securing a territory elsewhere is unknown.
The greater philopatric tendencies of males in
species such as the great tit may be a step on the
evolutionary route to the patrilineal cooperative
systems of species such as babblers and the
Florida scrub jay. In these, a male's breeding
options are restricted to assisting in and eventually inheriting the natal group, budding off from
the natal territory or attempting to form a new
group by attracting females. Females, on the
other hand, may succeed in joining another
group (Zahavi 1974; Woolfenden 1975; Gaston
1976, 1978; Woolfenden & Fitzpatrick 1978).
The reluctance of individuals in many species
to undergo breeding dispersal even though their
initial reproductive site is inadequate (e.g.
Tenaza 1971) is not surprising if the costs of
dispersal are high. When males are the primary
resource defenders their options should be considerably fewer than those of females. Both sexes
usually reoccupy or retain sites following successful nesting attempts. Females in a number of
species have a greater tendency to move to a new
location following unsuccessful breeding attempts (e.g. Haartmann 1949; Richdale 1957;
Catchpole 1972). They should also be expected
to disperse when subject to variability in the
quality of nesting areas (e.g. Verner 1964) and
when there are no long term advantages from
re-pairing with the same individual. In this context it is worth noting the greater effective natal
dispersal of females in polygynous populations
of the pied flycatcher (Haartmann 1949) compared to monogamous ones (Berndt & Sternberg
1969). This could indicate a higher variance in the
quality of the resources defended by different
1154
ANIMAL
BEHAVIOUR,
males in the former group both within and between breeding seasons (see Orians 1969). Selection of good territories by females or a reluetance
to mate bigamously with a male could well be the
source of greater female dispersal. A parallel
situation prevails in the white-bearded manakin,
where males compete for positional status in one
lek whereas females have the capacity to choose
different males both within and between leks
(Lill 1974).
A number of species of mammals with female
biased dispersal have a mating system which
seems similar to that of most birds. In the whitelined bat, single males control access to a large
foraging range which serves to attract groups of
females (Tannenbaum 1975; Bradbury &
Vehrencamp 1977a, b). Competition for male
territories is intense and the acquisition of a territory and subsequently a harem near to the natal
one by male offspring may be mediated by the
presence of the parental male; females disperse
in this species: The social dynamics of the gorilla
are analogous to those of cooperative birds (see
above). Females which disperse can join adjacent
groups; males either inherit their natal group or
have to establish a new one (Harcourt et al.
1976). In the pika, the territories of a male and
female overlap in the breeding season to become
one common area. Juvenile males live close to
their birth site, but peripheral to the defended
patches of vegetation, until a vacancy arises.
Natal dispersal is more likely to occur among females and they often pair with single males defending a territory (A. T. Smith 1978). Again,
this arrangement appears similar to that of
monogamous territorial birds with male philopatry and female biased dispersal. It is uncertain
whether the chimpanzee and wild hunting dog,
both with cooperative male groups and female
transfer, should be included amongst those with
a resource defence mating system.
A large number of ungulates do have resource
defence systems (Owen-Smith 1977), but it is in
territorial mammals of this kind that extensive
information on dispersal is lacking. For instance,
the majority of ungulates in Table III do not have
this type of mating system. There is some evidence from the study of the white rhinoceros by
Owen-Smith (1975) that females do wander
through male territories; those males holding
larger, better quality areas achieve most matings.
Female flexibility in choosing between the different defended areas of males has been reported in
a number of other ungulates (e.g. Jarman 1974).
Whether this means that dispersal is biased in
28,
4
favour of females and that males are more philopatric is unclear.
Mate Defence and Male Biased Dispersal
In many species of mammals the social system
is not one in which males defend resources in
order to attract females. Instead, females form
the stable nucleus with males as an adjunct to it
adopting strategies to maximize their access to
females. This type of mating system is rare
among birds (Emlen & Oring 1977) with the
probable exception of the Anatidae (see below).
The defensibility of females and not resources
has been considered a key component in the evolution of the males' reproductive tactics (Emlen
& Oring 1977; Bradbury & Vehreneamp 1977a).
Male dispersal can be viewed as a consequence
of the dispersion of females. Thus the hypotheses
of Baker (1978), Clutton-Brock & Harvey (1976)
and Packer (1979) for the origins of male biased
dispersal in the majority of mammals can perhaps be modified.
These authors consider sex differences in dispersal to be derived from polygyny, where males
invest little in offspring and gain most from dispersal, while females invest heavily and should
gain most from being sedentary. With this asymmetry and the additional possibility that males
may be uncertain of their offspring (Alexander
1974) it is not difficult to envisage the evolution
of the matrilineal social structure commonly
found in mammals (see Eisenberg 1966). The
crucial point, however, is that a matrilineal social
organization and male biased dispersal are not
inextricably linked. What is important is that
mate dispersal is a consequence of a mating
system in which males do not primarily determine the distribution of females by partitioning
resources amongst themselves. Instead it is the
distribution of females that influences the dispersion of males. The origins of such a system
may well be derived from marked differences in
parental investment by the sexes, where philopatry is more advantageous to females than to
males. It does not necessarily follow though that
a matrilineal structure consisting of mobile
groups of females cannot be retained when males
do defend resources to attract females. In other
words, male biased dispersal cannot automatically be assumed to be a consequence of
polygyny. Instead, it depends upon the means
through which the polygyny is achieved (cf. resource defence single male harem of the whitelined bat with female dispersal (Bradbury &
Vehrencamp 1977a, b) versus mate defence single
GREENWOOD: MATING SYSTEMS AND DISPERSAL
male/multi-female troops of the Hanuman langur with male dispersal (Hrdy 1977)).
A mate defence system with male biased dispersal is well exemplified by the open social
organization of the round-tailed ground squirrel
(Dunford 1977). A female during pregnancy and
lactation maintains sole use of her home range.
During the mating season, ranges are permeable
to males which compete for non-exclusive access
to females. (This species also illustrates the fact
that females in some species can prevent competition for food from males during the period
of maximum investment in offspring.) Among
mammals with more structured and closed
organizations, males may temporarily or semipermanently append themselves to a group of
sedentary females and for a period have exclusive
access to them (e.g. Kaufmann 1962; Lindburg
1969; Schaller 1972; I. & O. Douglas-Hamilton
1975; Hrdy 1977; Packer 1979).
In species of birds with male biased natal or
breeding dispersal, the mating system also appears to be one of mate defence. In the lesser
snow goose and the long-tailed duck, males do
not arrive on the breeding grounds unmated and
partition the available habitat into territories. Instead, pairs form on the wintering grounds before
the nesting season (Alison 1975; Cooke et al.
1975). Male long-tailed ducks do defend small
areas in the early part of the breeding cycle, but
these are of little value to females which commonly nest in an area other than that defended
by their mate. A female's investment in offspring
is considerably greater than a male's, and the
male often deserts while she is incubating (Alison
1975). A male's reproductive tactics are geared
to maintaining access to the female prior to egg
laying and not to any associated resource. In
both the lesser snow goose and the shelduck,
male parental duties are more extensive and entail the defence of resources and a longer association with offspring and young (e.g. Young
1970). Nevertheless, a mate defence mating system, particularly in monogamous species, does
not exclude the possibility of males adopting
additional strategies, such as the defence of feeding areas, to maximize their reproductive success.
The crucial point is that in the absence of a mate
such actions during the breeding season are
superfluous. It is therefore females which determine the dispersion of males. Conversely, for a
resource defence mating system, comparable actions are essential for the attraction and acquisition of mates.
1155
Problems
In at least two species of mammals, natal dispersal is male biased even though males defend
resources to attract females. Male yellow-bellied
marmots defend overwintering sites important
for hibernation, allowing access by females but
excluding other males (Downhower & Armitage
1971). In the vicuna, males hold feeding territories with an average harem of four females.
Dispersal is male biased although young females
also leave their natal unit (Koford 1957;
Franklin 1974). There may be two reasons for
these sex differences in dispersal. First, in marmots, the harem system has probably evolved
from the matrilineal organization common in
other sciurids in which male dispersal is to be
expected. As a consequence, they may have retained the earlier mode of dispersal. In other
words, the mating system may be primarily one
of mate defence but secondarily resource defence. Second, in both the marmot and vicuna,
male dispersal may be a direct result of the degree
ofpolygyny. When most females can be monopolized by relatively few dominant males and breeding sites are a limiting resource, then a high proportion of subordinate males may be excluded.
Females, though, should retain the propensity to
select males on the quality of their resources.
Natal dispersal may be biased in favour of males
whereas effective natal dispersal could be biased
in favour of females.
These two species illustrate more general
problems for a comparative survey of dispersal.
Very few studies have distinguished between
gross and effective dispersal (see Methods). A
study of the water vole by Leuze (1976, and in
press) is a mammalian exception; the costs of
female dispersal are much higher than male dispersal. Conversely, in the blackbird, the costs of
male dispersal are probably higher than female
dispersal (Greenwood & Harvey 1976b), Differential costs are crucial components in the proposed relationships between mating systems and
sex biased dispersal (see also Baker 1978). Both
sexes will derive benefits from familiarity with an
area. Which sex disperses may be the outcome
of a conflict between the sexes, where the relative
costs and benefits of dispersal and philopatry to
the sexes determine the outcome. Until more
studies are available which have distinguished
between gross and effective dispersal it will be
difficult to assess the veracity of the hypotheses
for the evolution of sex biased dispersal. Even
so, it may be unrealistic to expect all species to
fall within the proposed framework. Exceptions
1156
ANIMAL
BEHAVIOUR,
will include those already mentioned and others
which have been inadvertently assigned to the
wrong mating system, pattern of dispersal or
both. More detailed studies of mammals with
female biased dispersal and birds with male
biased dispersal should be illuminating. However, further examples of birds or mammals with
the prevalent mating system and sex biased dispersal of their taxon will not constitute tests of
the hypotheses. A comparative survey of another
taxon (e.g. fishes, reptiles) would be a more appropriate as well as independent test.
The Consequences of Philopatry and Dispersal
The philopatry of individuals to their natal group
or area produces conditions that facilitate the
evolution of altruistic traits among close relatives
(Hamilton 1964, 1971, 1972). Perhaps the most
striking example so far reported in mammals is
the alarm calling of females for the benefit of
their immediate offspring and other same-sex
relatives in Belding's ground squirrel; here females are sedentary and males disperse (Sherman
1977). In the patrilineal Florida scrub jay, male
offspring remain in their natal group longer than
females and during that time assist in the rearing
of broods other than their own. Some of the
males eventually inherit their natal territory
(Woolfenden 1975, and quoted in Emlen 1978).
No doubt many more examples of sex biased
cooperation or altruism will be discovered. These
should be predominantly male biased in birds
and female biased in mammals as a result of the
differences in dispersal between the two groups.
Nevertheless, it should not be assumed that relatives will automatically derive benefits from their
close proximity. For example, male great tits
which nest in territories adjacent to those of close
relatives do not have a reproductive success
higher than expected (Greenwood et al. 1979b).
However, it still remains possible that the securing of territories in relatively asocial monogamous birds can be assisted by relatives nearby,
by analogy with the situation for males in the
Florida scrub jay (Woolfenden & Fitzpatrick
1978) and probably also for females in
Richardson's ground squirrel (Yeaton 1972).
The likelihood that relatives are in close association is reduced by dispersal unless related
individuals which disperse remain together.
This is the case in the lion, where male siblings
leave their natal group at the same time and they
copulate with the same lionesses in a new pride
following successful dispersal (Bertram 1975,
1976). The estimated average degree of related-
28, 4
ness between reproductive males in a pride is
greater than that between females (Bertram
1976). This result is probably rather unusual in
species with male biased dispersal.
The proximity of unrelated individuals as a
result of dispersal may have profound consequences. It is not surprising that various disruptive acts accompany such movements, particularly
when the interests of philopatric and dispersing
animals differ. Infanticide by males taking over
groups has been observed in a number of species
of mammals. The evolutionary significance of
such action has been extensively reviewed by
Hrdy (1974, 1977). In summary, it may be advantageous to incoming males to kill unrelated offspring and curtail further maternal investment
when, as a consequence, females come into
oestrus and are mated by the new males. A
successful takeover by males may also result in
the expulsion (enforced dispersal) of resident
males (e.g. I-Ianuman langur, Hrdy 1977). In the
purple-faced langur, males in high density populations do not have access to female groups for
long enough for juvenile females to reach maturity during their tenure; young females are also
expelled (Rudran 1973). It has been argued that
this enforcement of female natal dispersal reduces competition for food within the group
(Hrdy 1977).
Actions by dispersing males may jeopardize
the immediate reproductive success of both resident males and females. Less attention has been
paid to the strategies employed by dispersing
females. Males would be expected to accept incoming adult females and possibly dependent female offspring if there was a high probability
that the latter would reach maturity during t h e
males' tenure. Resident females should attempt
to repel incoming females. If females are successful in gaining admission to a group, then disruptive or at least non-cooperative actions may occur between them and other unrelated females
within the group, The possibility of infanticide
cannot be excluded.
Sex biased philopatry may also have important
consequences for other life history traits. In the
thick-tailed bushbaby, sedentary females occupy
home ranges adjacent to those of close relatives.
If it is assumed that females are competing for
resources then they are more expensive to produce than males. In line with this assumption,
secondary sex ratios are biased in favour of males
which disperse ,(Clarke 1978). Clearly, where
males are the philopatric sex and compete with
each other the opposite bias in the sex ratio
GREENWOOD: MATING SYSTEMS AND DISPERSAL
would be predicted. The sex ratio bias should
reverse in situations where offspring of the philopatric sex are cooperating rather than competing
with close relatives. The need for appropriate
data to test these hypotheses is clear.
A more detailed discussion of the evolutionary
consequences of philopatry and sex biased dispersal in relation to mating systems can be
found elsewhere (Greenwood, in press).
Conclusion
The observed sex differences in natal and breeding dispersal in birds and mammals are associated with a number of interrelated variables:
t a x o n o m y , differences in the sex chromosomes,
the pair bond and mating systems. There is no
justification for believing that the predominance
of female biased dispersal in birds and male
biased dispersal in mammals is the product of
some taxonomic constraint, i.e. alternative and
evolutionarily stable means o f solving similar
problems. N o r is there a basis for assuming that
the asymmetry in the sex chromosomes is the
source of the bias. Neither could satisfactorily
account for the exceptions in the two classes. We
are therefore compelled to investigate the significance of the difference in behavioural or ecological terms. The broad distribution of the
1157
traits indicates that the answers must also be
sought on a similarly broad base that transcends
species-specific life history idiosyncracies.
The vast majority of birds are monogamous;
the majority of mammals are polygamous. Most
of the former have female biased dispersal, the
latter male biased dispersal. I have argued though
that both the nature of the pair bond and the sex
differences in dispersal are a consequence of the
type of mating system. (I have not dealt in detail
with the more complex problem of why species
have a particular mating system (see Emlen &
Oring 1977; Bradbury & Vehrencamp 1977a;
Bradbury, in press).) Resource defence by one
sex to attract members of the other sex will not
only favour m o n o g a m y but also philopatry of
the former (resource defender) and greater dispersal of the latter. A mate defence mating system, in which members of the limited sex are
primarily concerned with gaining access to and
defending members of the limiting sex, will favour polygamy, the philopatry of the limiting
sex and greater dispersal of the limited sex. A
summary of the salient features of dispersal associated with each mating system is shown in
Table V. Whether mating systems prove to be
the best predictors of sex biased dispersal awaits
further field observations and experiments.
Table V. Mating Systems and Dispersal in Birds and Mammals: A Summary of the
Main Features Associated with Resource Defence and Mate Defence Mating
Systems
Resource Defence
Mate Defence
High male investment in
resources, in presence or
absence of mate(s)
Low male investment in
resources, particularly in
absence of mate(s)
Low female investment
in resources
High female investment
in resources
Inter-male competition
for resources
Inter-male competition
for mates
Mainly monogamous
(but includes leks .9)
Mainly polygamous
Male philopatry
High cost to male dispersal ?
Female philopatry
High cost to female dispersal ?
Greater female natal and
breeding dispersal:
(i) Reproductive enhancement - female choice of male resources
(ii) Inbreeding avoidance
Greater male natal and
breeding dispersal;
(i) Reproductive enhancement - increase access to females
(ii) Inbreeding avoidance
Evolution of patrilineal
social organization
Evolution of matrilineal
social organization
1158
ANIMAL
BEHAVIOUR,
Acknowledgments
M y m a j o r debt is to Paul Harvey a n d G e o r g i n a
Mace who have been a n i n v a l u a b l e source of
e n c o u r a g e m e n t a n d criticism d u r i n g the paper's
long gestation. I a m also grateful to a n u m b e r of
other people who, in diverse ways, have helped
me clarify m y thoughts: J. M a y n a r d Smith, J.
Bradbury, S. Vehrencamp, N. K n o w l t o n , W.
Shields, P. Sherman, E. Mayr, T. C l u t t o n - B r o c k
a n d J. Krebs. The work was supported in p a r t by
a g r a n t to Paul Harvey from the Science Research Council a n d a N a t u r a l E n v i r o n m e n t
Research Council post-doctoral fellowship held
at the Edward Grey Institute, Oxford.
REFERENCES
Alexander, R. D. 1974. The evolution of social behaviour.
Ann. Rev. Ecol. Syst., 5, 325-383.
Alison, R. M. i975. Breeding biology and behaviour of
the Oldsquaw (Clangula hyemalis L.). Ornithol.
~4onogr., 18, 1-52.
Alison, R. M. 1977. Homing of subadult Oldsquaws. Auk,
94, 383-384.
Altmann, S. A. & Altmann, J. 1970. Baboon Ecology,
African FieM Research. Chicago: University of
Chicago Press.
Anderson, A. H. & Anderson, A. 1973. The Cactus Wren.
Tucson: University of Arizona Press.
Archer, J. 1970. Effects of population density on behaviour in rodents. In: ,Social Behaviour in Birds and
Mammals (Ed. by J. H. Crook), pp. 169-210.
London: Academic Press.
Armitage, K. B. 1973. Population changes and social
behaviour following colonization by the yellowbellied marmot. J. Mammal., 54, 842-854.
Armitage, K. B. 1974. Male behaviour and territoriality
in the yellow-bellied marmot. J. ZooL, Lond., 172,
233-265.
Austin, O. L. 1949. Site tenacity, a behaviour trait of the
common tern. Bird-Banding, 20, 1-39.
Austin, O. L. 1951. Group adherence in the common
tern. Bird-Banding, 22, 1-15.
Baker, M. C. & Mewaldt, L. R. 1978. Song dialects as
barriers to dispersal in white-crowned sparrows,
Zonotrichia leucophrys nuttalli. Evolution, 32, 712722.
Baker, R. R. 1978. The Evolutionary Ecology of Animal
Migration. London: Hodder & Stoughton.
Barash, D. P. t973. The social biology of the Olympic
marmot. Anita. Behav. Monogr., 6, 171-249.
Bengtsson, B. O. 1978. Avoiding inbreeding: at what
cost? J. theoret. Biol., 18, 439-444.
Berger, A. J. & Radabaugh, B. E. 1968: Returns of
Kirtland's warblers to the breeding grounds. BirdBanding, 39, 161-186.
Berndt, R. & Sternberg, H. 1969. Alters- und Geschlechtsunterschiede in der Dispersion des Trauerschn~ippers (Ficedula hypoleuca). J. Orn., 110, 256-269.
Bertram, B. C. 1975. Social factors influencingreproduction in wild lions. J. Zool. Lond., 177, 463-482.
Bertram, B. C. 1976. Kin selection in lions and in evolution. In: Growing Points in Ethology (Ed. by
P. P. G. Bateson & R. A. Hinde), pp. 281-301.
Cambridge: Cambridge University Press.
28,
4
Bischof, N. 1975. Comparative ethology of incest avoidance. In: Biosocial Anthropology (Ed. by R. Fox),
pp. 37-67. London: Malaby.
Boelkins, R. C. & Wilson, A. P. 1972. Intergroup social
dynamics of the Cayo Santiago rhesus (Macaca
mulatta) with reference to changes in group
membership by males. Primates, 13, 125-140.
Bradbury, J. W. In press. The evolution of leks. In:
Natural Selection and Social Behaviour (Ed. by R. D.
Alexander & D. Tinkle). New York: Chiron Press.
Bradbury, J. W. & Vehrencamp, S. L. 1976. Social
organization and foraging in Emballonurid bats.
I. Field studies. Behav. Ecol. Sociobiol., 1, 337-381.
Bradbury, J. W. & Vehrencamp, S. L. 1977a. Social
organisation and foraging in Emballonurid bats.
III. Mating systems. Behav. EcoL SociobioL, 2,
1-17.
Bradbury, J. W. & Vehrencamp, S. L. 1977b. Social
organisation and foraging in Emballonurid bats.
IV. Parental investment patterns. Behav. Ecol.
SoeiobioL, 2, 19-29.
Bronson, F. H. 1964. Agonistic behaviour in woodchucks.
Anim. Behav., 12, 470-478.
Brooke, M. de L. 1978. The dispersal of female Manx
shearwaters Puffinus puffinus. Ibis, 120, 545-551.
Brown, B. A. 1974. Social organisation in male groups of
white-tailed deer. In: The Behaviour of Ungulates
and its Relation to Management (Ed. by V. Geist
& F. Walther), pp. 436-446. Morges, Switzerland:
I.U.C.N. Publications.
Brown, J. L. 1964. The evolution of diversity in avian
territorial systems. Wilson Bull., 76, 160-169.
Brown, J. L. 1974. Alternate routes to sociality in jays
with a theory for the evolution of altruism and
communal breeding. Am. Zool., 14, 63-80.
Budnitz, N. & Dainis, K. 1975. Lemur catta, ecology and
behaviour. In: Lemur Biology (Ed. by I. Tatersall
& R. W. Sussman), pp. 219-236. New York:
Plenum Press.
Bulmer, M. G. 1973. Inbreeding in the great tit. Heredity,
30, 313-325.
Bulmer, M. G. & Perrins, C. M. 1973. Mortality in the
great tit, Parus major. Ibis, 115, 277-281.
Carpenter, C. R. 1940. A field study in Siam of the behaviour and social relations of the gibbon (Hylobates lar). Comp. Psyehol. Monogr., 16, 1-212.
Carpenter, C. R. 1965. The howlers of Barro Colorado
Island. In: Primate Behaviour. Field Studies on
Monkeys andApes (Ed. by I. Devote), pp. 250-291.
New York: Holt, Rinehart & Winston.
Catchpole, C. K. 1972. A comparative study of territory
in the reed warbler (Acrocephalus scirpaceus) and
sedge warbler (,4. schoenobaenus). Jr. Zool., Lond.,
166, 213-231.
Chabrzyk, G. & Coulson, J. C. 1976. Survival and recruitment in the herring gull Larus argentatus. Y.
dnim. Ecol., 45, 187-203.
Cheney-Seyfarth, D. 1976. Social development of immature baboons. Unpublished Ph.D. thesis,
University of Cambridge.
Clarke, A. B. 1978. Sex ratio and local resource competition in a prosimian primate. Science, N.Y., 201,
163-165.
Clutton-Brock, T. H. & Harvey, P. H. t976. Evolutionary
rules and primate societies. In: Growing Points in
Ethology (Ed. by P. P. G. Bateson & R. A. Hinde),
pp. 195-237. Cambridge: Cambridge University
Press.
G R E E N W O O D : MATING SYSTEMS A N D DISPERSAL
Cooke, F., MacInnes, C. D. & Prevett, J. P. 1975. Gene
flow between breeding populations of the lesser
snow goose. Auk, 92, 493-510.
Daly, M. & Daly, S. 1975. Behaviour of Psammomys
obesus (Rodentia: Gerbillinae) in the Algerian
Sahara. Z. Tierspsychol., 37, 298-321.
Darley, J. A., Scott, D. M. & Taylor, N. K. t977. Effects
of age, sex and breeding success on site fidelity of
gray catbirds. Bird-Banding, 48, 145-151.
Darling, F. F. 1937. A Herd of R e d Deer. London: Oxford
University Press.
Davies, C. E. 1976. Dispersion and nest-site fidelity in
breeding swallows, Hirundo rustica. Ibis, 118, 470
(abstract).
Davies, P. W. & Snow, D. W. 1965. Territory and food of
the song thrush. Brit. Birds, 58, 161-175.
Delius, J. D. 1965. A population study of skylarks Alauda
arvensis. Ibis, 107, 446--492.
Dhondt, A. A. & Hubl6, J. 1968. Fledging date and sex
in relation to dispersal in young tits. Bird Study,
15, 127-134.
Dice, L. R. & Howard, W. E. 1951. Distance of dispersal
by prairie deer mice from birthplaces to breeding
sites. Contrib. Lab. Vert. BioL Univ. Mich., 50,
1-15.
Dittus, W. P. J. 1975. Population dynamics of the toque
monkey, Macaca sinica. In: Socioecology and
Psychology of Primates (Ed. by R. H. Tuttle), pp.
125-151. Chicago: Aldine.
Doty, H. A. & Lee, F. B. 1974. Homing to nest baskets by
wild female mallards. J. Wildl. Mgmt, 38, 7t4-719.
Douglas-Hamilton, I. & O. 1975. Among the Elephants.
London: Collins.
Downhower, J. F. & Armitage, K. B. 1971. The yellowbellied marmot and the evolution of polygamy.
Am. Nat., 105, 355-370.
Drickamer, L. C. & Vessey, S. H. 1973. Group changing
in free ranging male rhesus monkeys. Prhnates, 14,
359-368.
Dunbar, R. & Dunbar, P. 1975. Social dynamics of
gelada baboons. Contributions to Primatology, 6~
1-158. Basel: Karger.
Dunford, C. 1977. Behavioural limitation of round-tailed
ground squirrel density. Ecology, 58, 1254-1268.
Eisenberg, J. F. 1966. The social organization of mammals.
Handbueh der Zoologic, 10, 1-92.
Emlen, S. T. 1978. The evolution of cooperative breeding
in birds. In: Behavioural Ecology: An Evolutionary
Approach (Ed. by J. R. Krebs & N. B. Davies),
pp. 245-281. Oxford: Blackwell.
Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection and the evolution of mating systems. Science,
N.Y., 197, 215-223.
Fisher, H. I. 1971. Experiments on homing in Laysan
albatrosses, Diomedea immutabilis. Condor, 73,
389-400.
Fiuezynski, D. 1978. Zur Populations6kologie des
Baumfalken (Faleo subbuteo L., 1758). Zool..lb.
Syst. Bd., 105, S, 193-257.
Frame, L. H. & Frame, G. W. 1976. Female African
wild dogs emigrate. Nature, Lond., 263, 227-229.
Frank, F. 1957. The causality of microtine cycles in
Germany. J. Wildl. Mgmt, 21, 113-121.
Franklin, W. L. 1974. The social behaviour of the vicuna.
In: The Behaviour of Ungulates and its Relation
to Management (Ed. by V. Geist & F. Walther),
pp. 477-487. Morges, Switzerland: I.U.C.N.
Publications.
1159
Fritzell, E. K. 1978. Aspects of racoon (Procyon lotor)
social organisation. Can. J. Zool., 56, 260-271.
Gaston, A. J. 1976. Factors affecting the evolution of
group territories in babblers (Turdoides) and longtailed tit. Unpublished D. Phil. thesis, University
of Oxford.
Gaston, A. J. 1978. Ecology of the common babbler
Turdoides caudatus, lbis, 120, 415-432.
Gates, J. M. 1962. Breeding biology of the gadwall in
northern Utah. Wilson Bull., 74, 43-67.
Gauthreaux, S. A. Jr. 1978. The ecological significance of
behavioural dominance. In: Perspectives in
Ethology, Vol. 3 (Ed. by P. P. G. Bateson & P. H.
Klopfer), pp. 17-54. London: Plenum Press.
Geist, V. 1971. Mountain Sheep: A Study in Behaviour and
Evolution. Chicago: University of Chicago Press.
Greenwood, P. J. 1978. Functions of dispersal in birds
and mammals. Unpublished D. Phil. thesis,
University of Sussex.
Greenwood, P. J. In press. Mating systems and the
evolutionary consequences of dispersal. In: The
Ecology of Animal Movement (Ed. by I. R.
Swingland & P. J. Greenwood). Oxford: Oxford
University Press.
Greenwood, P. J. & Harvey, P. H. 1976a. The adaptive
significance of variation in breeding area fidelity
of the blackbird (Turdus merula L.). J. Anita. Ecol.,
45, 887-898.
Greenwood, P. J. & Harvey, P. H. 1976b. Differential
mortality and dispersal of male blackbirds. Ring.
Migr., 1, 75-77.
Greenwood, P. J. & Harvey, P. H. 1977. Feeding strategies and dispersal of territorial passerines: a comparative study of the blackbird Turdus merula and
the greenfinch Carduelis ehloris. Ibis, 119, 528-531.
Greenwood, P. J., Harvey, P. H. & Perrins, C. M. 1978.
Inbreeding and dispersal in the great tit. Nature,
Lond., 271, 52-54.
Greenwood, P. J., Harvey, P. H. & Perrins, C. M. 1979a.
The role of dispersal in the great tit (Parus major):
the causes, consequences and heritability of natal
dispersal. J. Anim. Ecol., 48, 123-142.
Greenwood, P. J., Harvey, P. H. & Perrins, C. M. 1979b.
Kin selection and territoriality in birds? A test.
Anim. Behav., 27, 645-651.
Grosskopf, G. 1959. Zur Biologic des Rotschenkels
(Tringa t. totanus) II.d. Orn., 100, 210-236.
Grubb, P. & Jewell, P. A. 1966. Social grouping and
home range in feral Soay sheep. Symp. zool. Soc.
Lond., 18, 179-210.
Haartmann, L. von. 1949. Der Trauerfliegenschn/ipper 1
Ortstrene und Rassenbildung. Acta Zool. Fenn.,
56, 1-104.
Hall, K. R. L. 1965. Behaviour and ecology of the wild
patas monkey, Erythrocebus patas, in Uganda. J.
Zool. Lond., 148, 15-87.
Hamilton, W. D. 1964. The genetical evolution of social
behaviour I, II., J. theoret. Biol., 7, 1-52.
Hamilton, W. D. 1971. Selection of selfish and altruistic
behaviour in some extreme models. In: Man and
Beast: Comparative Social Behaviour (Ed. by J. F.
Eisenberg & W. S. Dillon), pp. 57-91. Washington:
Smithsonian.
Hamilton, W. D. 1972. Altruism and related phenomena,
mainly in social insects. Ann. Rev. Ecol. 63~st., 3,
193-232.
1160
ANIMAL
BEHAVIOUR,
Harcourt, A. H., Stewart, K. J. & Fossey, D. 1976. Male
emigration and female transfer in wild mountain
gorilla. Nature, Lond., 263, 226-227.
Harvey, P. H., Greenwood, P. J. & Perrins, C. M. 1979.
Breeding area fidelity of the great tit (Paras major).
J. Anita. EcoL, 48, 305-313.
Haukioja, E. 1971. Short-distance dispersal in the reed
bunting Emberiza schoeniclus. Ornis Fennica, 48,
45-67.
Hendrichs, H. 1975. Changes in a population of dikdik,
Madoqua (Rhynchotragus) kirki (Giinther 1880).
Z. TierpsychoL, 38, 55-69.
Hill, J. L. 1974. Peromyscus: effect of early pairing on
reproduction. Science, N.Y., 186, 1042-1044.
Hodson, K. A. 1975. Some aspects of the nesting ecology
of Richardson's merlin (Falco columbarius
richardsonii) on the Canadian prairies. Unpublished M.Sc. thesis, University of British Columbia.
Horr, D. A. 1975. The Borneo orang-utah: population
structure and dynamics in relationship to ecology
and reproductive strategy. In: Primate Behaviour:
Developments in Field and Laboratory Research,
Vol. 4 (Ed. by L. A. Rosenblum), pp. 307-323.
London: Academic Press.
Housten, D. B. 1974. Aspects of the social organisation
of moose. In: The Behaviour of Ungulates and its
Relation to Management (Ed. by V. Geist & F.
Walther), pp. 690-696. Morges, Switzerland:
I.U.C.N. Publications.
Howard, W. E. 1949. Dispersal, amount of inbreeding
and longevity in a local population of prairie deer
mice on the George reserve, southern Michigan.
Contrib. Lab. Vert. Biol. Univ. Mich., 43, 1-50.
Howard, W. E. 1960. Innate and environmental dispersal
of individual vertebrates. Am. Midl. Nat., 63, 152161.
Hrdy, S. B. 1974. Male-male competition and infanticide
among the langurs (Presbytis entellus) of Abu,
Rajasthan. Folia Primatol., 22, 19-58.
Hrdy, S. B. 1977. The Langurs of Abu. Harvard: Harvard
University Press.
Itani, J. 1972. A preliminary essay on the relationship
between social organisation and incest avoidance
in non-human primates. In: Primate Socialization
(Ed. by F. E. Poirier), pp. 165-171. New York:
Random House.
Jarman, P. J. 1974. The social organisation of antelope in
relation to their ecology. Behaviour, 58, 215-267.
Jolly, A. 1972. The Evolution of Primate Behaviour. New
York: Macmillan.
Kammermeyer, K. E. & Marcbinton, R. L. 1976. Notes
on dispersal of male white-tailed deer. J. Mammal.,
57, 776-778.
Kaufman, G. W., Siniff,. D. B. & Reichle, R. 1975.
Colony behaviour of Weddell seals, Leptonychotes
weddelli, at Hutton Cliffs, Antarctica. Rapp. P.V. Reun. Cons. int. Explor. Mer, 169, 228-246.
Kaufmann, J. H. 1962. Ecology and social behaviour of
the coati, Nasaa narica, on Barro Colorado Island,
Panama. Univ. Calif. Publ. Zool., 60, 95-222.
Kaufmann, J. H. 1974. Social ethology of the whiptail
wallaby, Macropus parryi, in northeastern New
South Wales. Anim. Behav., 22, 281-369.
Kavanagh, M. 1977. Some interpopulation variation in
the behavioural ecology of Cercopithecus aethiops
tantalus. Unpublished D. Phil. thesis, University
of Sussex.
28,
4
Kendeigh, S. C. 1941. Territorial and mating behaviour
of the house wren. 11l. Biol. Monogr., 18, 1-120.
Kendeigh, S. C. & Baldwin, S. P. 1937. Factors affecting
yearly abundance of passerine birds. Ecol. Monogr.
7, 91-123.
Kenyon, K. W. 1960. Territorial behaviour and homing
in the Alaska fur seal. Mammalia, 24, 431-444.
Kikkawa, J. 1964. Movement, activity and distribution of
the small rodents Clethrionomys glareolus and
Apodemus sylvaticus. J. Anim. Ecol., 33, 259-299.
King, J. A. 1955. Social behaviour, social organisation
and population dynamics in a black-tailed prairiedog town in the Black Hills of South Dakota.
Contrib. Lab. Fert. Biol. Univ. Mich., 67, 1-123.
Kleiman, D. G. 1977. Monogamy in mammals. Q. Rev.
BioL, 52, 36-69.
Klingel, H. t967. Soziale Organisation und Verhalten
freilebender Steppenzebras. Z. TierpsychoL, 24,
580-624.
Klingel, H. 1969. Reproduction in the plains zebra, Equus
burchelli boehmi: behaviour and ecological factors.
J. Reprod. Fert. Suppl., 6, 339-345.
Klingel, H. 1975. Social organisation and reproduction in
equids. J. Reprod. Fert. Suppl., 23, 7-11.
Koford, C. B. 1957. The vicuna and the puna. Ecol.
Monogr., 27, 153-219.
Kozakiewicz, M. 1976. Migratory tendencies in population of bank voles and description of migrants.
Acta theriol., 21, 321-336.
Krebs, C. J., Wingate, I., LeDuc, J., Redfield, J. A., TaRt,
M. & Hilborn, R. 1976. Microtus population
biology: dispersal in fluctuating populations of
M. townsendii. Can. J. Zool., 54, 79-95.
Kruuk, H. 1972. The Spotted Hyena: A Study of Predation and Social Behaviour. Chicago: University
of Chicago Press.
Kummer, H. 1968. Social Organisation of Hamadryas
Baboons. Chicago: University of Chicago Press.
Kurland, J. In press. Matrilines: the primate sisterhood
and the human avunculate. In: Sociobiology and
the Social Sciences (Ed. by I. Devote). Chicago:
Aldine-Atherton.
Lack, D. 1968. Ecological Adaptations for Breeding in
Birds. London: Methuen.
Lawick, H. van, & Lawick-Goodall, J. van. 1971.
lnnocent Killers. London: Collins.
Lenington, S. & Mace, T. 1975. Mate fidelity and nesting
site tenacity in the killdeer. Auk, 92, 149-151.
Leuze, C. 1976. Social behaviour and dispersion in the
water vole Arvicola terrestris (Lacepede). Unpublished Ph.D. thesis, University of Aberdeen.
Leuze, C. In press. Dispersal and predation in water voles.
Ecology.
Lidicker, W. Z. Jr. 1962. Emigration as a possible
mechanism permitting the regulation of population
density below carrying capacity. Am. Nat., 96,
29-33.
Lidicker, W. Z. Jr. 1975. The role of dispersal in the
demography of small mammals. In: Small Mammals: Productivity and Dynamics of Populations
(Ed. by K. Petrusewicz, E. B. Golley & L.
Ryszkowski), pp. 103-128. London: Cambridge
University Press.
Lidicker, W. Z. Jr. 1976. Social behaviour and density
regulation in house mice living in large enclosures.
J. Anita. Ecol., 45, 677-697.
G R E E N W O O D : MATING SYSTEMS A N D DISPERSAL
Lill, A. 1974. Sexual behaviour of the lek-forming whitebearded manakin (Manacus manacus trinitatis
Hartert). Z. Tierpsychol., 36, 1-36.
Lincoln, F. C. 1934. The operation of homing instinct.
Bird-Banding, 5, 149-155.
Lindburg, D. G. 1969. Rhesus monkeys: mating season
mobility of adult males. Science, N. Y., 166, 11761178.
Lowe, V. P. W. 1966. Observations on the dispersal of
red deer on Rhum. Syrup. Zool. Soc. Lond., 18,
211-228.
MacDonald, D. W. 1977. The behavioural ecology of the
red fox. In: Rabies. The Facts (Ed. by C. Kaplan),
pp. 70--90. London: Oxford University Press.
Mayhew, W. W. 1958. The biology of the cliff swallow in
California. Condor, 60, 7-37.
Maynard Smith, J. 1978. The Evolution of Sex. Cambridge:
Cambridge University Press.
Maza, B. G., French, N. R. & Aschwanden, A. P. 1973.
Home range dynamics in a population of heteromyid rodents. J. MammaL, 54, 405-425.
Michener, G. R. & Michener, D. R. 1977. Population
structure and dispersal in Richardson's ground
squirrel. Ecology, 58, 35%368.
Mills, J. A. 1973. The influence of age and pair-bond on
the breeding biology of the red-billed gull, Larus
novaehollandiae seopulinus. J. Anim. Ecol., 42, 147163.
Myers, J. H. 1974. Genetic and social structm'e of feral
house mouse populations on Grizzly Island,
California. Ecology, 55, 747-759.
Myers, J. H. & Krebs, C. J. 1971. Genetic, behavioural
and reproductive attributes of dispersing field
voles, Microtus pennsylvanieus and Microtus
ochrogaster. EcoL Monogr., 41, 53-78.
Myllym~ki, A. 1977. Intraspecific competition and home
range dynamics in the field vole Microtus agrestis.
Oilcos, 29, 553-569.
Nelson, B. 1978. The Gannet. Berldlamstead: T. & A. D.
Poyser.
Nice, M. M. 1937. Studies in the life history of the song
sparrow. Trans. Linn. Soc. N. Y., 4, 1-247.
Nice, M. M. 1943. Studies in the life history of the song
sparrow. Trans. Linn. Soc. IV. Y., 6, 1-328.
Nicholls, D. G. 1970. Dispersal and dispersion in relation
to the birthsite of the southern elephant seal,
Mirounga leonina (L) of Macquarie Island.
Mammalia, 34, 598-616.
Nishida, T. In press. The social structure of chimpanzees
of the Mahali mountains. In: The Great Apes:
Perspectives on Human Evohttion, VoI. 4 (Ed. by
D. A. Hamburg & E. R. McCowan). Menlo
Park: Benjamin.
Oates, J. F. 1977. The social life of the black and white
colobus monkey, Colobus guereza. Z. Tierpsychol.,
45, 1-60.
Orians, G. H. 1969. On the evolution of mating systems
in birds and mammals. Am. Nat., 103, 589-603.
Owen-Smith, R. N. 1975. The social ethology of the white
rhinoceros Ceratotherium simum (Burchell, 1817).
Z. Tierpsychol., 38, 337-384.
Owen-Smith, N. 1977. On territoriality in ungulates and
an evolutionary model. Q. Rev. Biol., 52, 1-38.
Packer, C. 1975. Male transfer in olive baboons. Nature,
Loud., 255, 219-220.
Packer, C. t979. Inter-troop transfer and inbreeding
avoidance in Papio anubis. Anita. Behav., 27 1-36.
1161
Poirier, F. E. 1969. The Nilgiri langur troop: its composition, structure, function and change. Folia
PrimatoL, 10, 20--47.
Pusey, A. E. In press. Intercommunity transfer of chimpanzees in Gombe national park. In: The Great
Apes: Perspectives on Human Evolution, Vol. 4
(Ed. by D. A. Hamburg & E. R. McCowan).
Menlo Park: Benjamin.
Ralls, K. 1976. Mammals in which females are larger than
males. Q. Rev. Biol., 51, 245-276.
Richard, A . 1974. Patterns of mating in Propithecus verreauxi verreauxi. In: Prosimian Biology (Ed. by
R. D. Martin & G. A. Doyle), pp. 49-74. London :
Duckworth.
Richdale, L. E. 1957. A Population Study of Penguins.
Oxford: Clarendon Press.
Rodman, R. S. 1973. Population composition and adaptive organisation among orang-utans of the Kutai
reserve. In : Comparative Ecology and Behaviour of
Primates (Ed. by R. P. Michael & J. H. Crook),
pp. 171-209. London: Academic Press.
Rogers, L. L. 1974. Movement patterns and social organisation of black bears in Minnesota. Unpublished
Ph.D. thesis, University of Minnesota.
Rongstad, O. J. 1965. A life history study of thirteenlined ground squirrels in southern Wisconsin. J.
MammaL, 46, 76-87.
Rowe, F. P., Taylor, E. J. & Chudley, A. H. J. 1963. The
numbers and movements of house mice (Mus
musculus L.) in the vicinity of four corn ricks. 3..
Anita. EcoL, 32, 87-97.
Rowley, L 1965. The life history of the superb blue wren,
Malurus eyaneus. Emu, 64, 251-297.
Rudran, R. 1973. Adult male replacement in one-male
troops of purple faced langurs (Presbytis senex
senex) and its effect on population structure. Folia
Primatol., 19, 166-192.
Ruiter, C. J. S. 1941. Waarnemingen omtrent de levenswijze van de Gekraagde Roodstaart, Phoenieurus
ph. phoenieurus (L.). Ardea, 30, 175-2t4.
Sadleir, R. M. F. S. 1965. The relationship between
agonistic behaviour and population changes in the
deermouse, Peromyscus maniculatus (Wagner). J.
Anim. Ecol., 34, 331-352.
Schaller, G. B. 1972. The Serengeti Lion. Chicago:
University of Chicago Press.
Schloeth, R. & Burckhardt, D. 1961. Die Wanderungen
des Rotwildes Cervus elephus L. im Gebiet des
Schweizerischen Nationalparkes. Rev. Suisse Zool.,
68, 146-155.
Schmidt, K. v o n & Hantge, E. 1954. Studien an einer
farbig beringten Population des Braunkehlchens
(Saxicola rubetra). J. Orn., 95, 130--173.
Sherman, P. W. 1977. Nepotism and tile evolution of
alarm calls. Science, IV. Y., 197, 1246-1253.
Shields, W. M. 1979. Philopatry, inbreeding and the
adaptive advantages of sex. Unpublished Ph.D.
thesis, Ohio State University.
Sinclair, A. R. E. 1974. The social organisation of the
East African buffalo (Syncerus caffer Sparrman).
In : The Behaviour of Ungulates and its Relation to
Management (Ed. by V. Geist & F. Walther), pp.
678-689. Morges, Switzerland: LU.C.N. Publications.
Sittman, K., Abplanalp, B. & Fraser, R. A. 1966. Inbreeding depression in Japanese quail. Genetics,
54, 371-379.
1162
ANIMAL
BEHAVIOUR,
Smith, A. T. 1974. The distribution and dispersal of pikas :
consequences of insular population structure.
Ecology, 55, 1112-1119.
Smith, A. T. 1978. Comparative demography of pikas
(Ochotona): effect of spatial and temporal agespecific mortality. Ecology, 59, 133-139.
Smith, S. F. 1977. Social structure of chipmunk populations and its relation to resource availability and
exploitation. Unpublished Ph.D. thesis, University
of California.
Smith, S. M. 1978. 'The underworld' in a territorial
sparrow: adaptive strategy for floaters. Am. Nat.,
112, 571-582.
Soikkeli, M. 1970. Dispersal of dunlin Calidris alpina in
relation to sites of birth and breeding. Ornis
Fennica, 47, 1-9.
Sowls, L. K. 1955. Prairie Ducks. Harrisburg,
Pennsylvania: Stackpole.
Struhsaker, T. T. 1967. Social structure among vervet
monkeys (Cercopithecas aetbiops). Behaviour, 29,
83-121.
Sugiyama, Y. 1965. Behavioural development and social
structure in two troops of hanuman langurs
(Presbytis entellus). Primates, 6, 213-247.
Sugiyama, Y. 1973. The social structure of wild chimpanzees: a review of field studies. In: Comparative
Ecology and Behaviour of Primates' (Ed. by R. P.
Michael & J. H. Crook), pp. 375-410. London:
Academic Press.
Sugiyama, Y. 1976. Life history of male Japanese monkeys. Adv. Stud. Behav., 7, 255-284.
Tannenbaum, B. R. 1975. Reproductive strategies in the
white-lined bat. Unpublished Ph.D. thesis, University of Cornell.
Taylor, L. R. & Taylor, R. A. J. 1977. Aggregation,
migration and population mechanics. Nature,
Lond., 265, 415-421.
Tenaza, R. 1971. Behaviour and nesting success relative
to nest location in Adelie penguins (Pygoscelis
adeliae). Condor, 73, 81-92.
Thompson, D. C. 1977. Reproductive behaviour of the
grey squirrel. Can. J. Zool., 55, 1176-1184.
Trivets, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man
(Ed. by B. Campbell), pp. 136-179. London:
Heinemann.
28,
4
Vermeer, K. 1963. The breeding ecology of the glaucouswinged gull (Larus glaucescens) on Mandarte
Island, B.C. Occ. Papers Brit. Col. Prov. Mus., 13,
1-90.
Verner, J. 1964. Evolution of polygamy in the long-billed
marsh wren. Evolution, 18, 252-261.
Warneke, R. M. 1975. Dispersal and mortality of juvenile
fur seals, Arctocephalus pusilhts doriferus in Bass
strait, Southeastern Australia. Rapp. P. -V. Reun.
Cons. int. Explor. Mer, 169, 296-302.
Watson, A. & Moss, R. 1970. Dominance, spacing behaviour and aggression in relation to population
limitation in vertebrates. In: Animal Populations
in Relation to their Food Resources (Ed. by A.
Watson), pp. 167-200. Edinburgh: Oliver & Boyd.
Werth, I. 1948. The tendency of blackbirds and song
thrushes to breed in their birthplaces. Brit. Birds,
40~ 328-330.
Whitney, G. 1976. Genetic substrates for the initial evolution of human sociality 1. Sex chromosome
mechanisms. Am. Nat., 110, 867-875.
Wilcox, L. R. 1959. A twenty year study of the piping
plover. Auk, 76, 129-152.
Wilson, E. O. 1975. Sociobiology: The New Synthesis.
Cambridge, Mass. : Belknap.
Woolfenden, G. E. 1975. Florida scrubjay helpers at the
nest. Auk, 92, 1-15.
Woolfenden, G. E. & Fitzpatrick, J. W. 1978. The inheritance of territory in group-breeding birds.
Bioscience, 28, 104-108.
Wooller, R. D. & Coulson, J. C. 1977. Factors affecting
the age of first breeding of the kittiwake, Rissa
tridactyla. Ibis, 119, 339-349.
Wright, S. 1943. Isolation by distance. Genetics, 28,
114-138.
Wright, S. 1946. Isolation by distance under diverse
systems of mating. Genetics, 31, 39-59.
Yeaton, R. I. 1972. Social behaviour and social organisation in Richardson's ground squirrel (Spermophilus
richardsonii) in Saskatchewan. J. MammaL, 53,
139-147.
Young, C. M. 1970. Territoriality in the common
shelduck Tadorna tadorna, lbis, 112, 330-335.
Zahavi, A. 1974. Communal nesting by the Arabian
babbler. Ibis, 116, 84-87.
(Received 21 November 1978; revised 1 November 1979;
MS. number: 1838)