AMER. ZOOL., 21:197-209 (1981)
Agonistic Encounters Among Male Elephant Seals:
Frequency, Context, and the Role of
Female Preference1
CATHLEEN R. COX 2
Department of Psychology, Stanford University,
Stanford, California 94305
SYNOPSIS. Aggressive interactions between male northern elephant seals, Mirounga angustirostris, observed during the course of three breeding seasons are analyzed from the
perspective of costs and benefits to individuals. Males spend less than one percent of their
time in aggressive activities and the overwhelming majority of agonistic interactions consist
only of visual and vocal threats rather than physical combat. Males are most likely to
threaten other males when the likelihood that they will be successful in displacing the
opponent is high. Males who are mounting females, or who are in close proximity to
females, are threatened more frequently than males who are otherwise occupied. However, high ranking bulls do regularly issue threats which are not provoked by the location
or behavior of the recipient. Despite the obvious costs of such threats, this behavior may
be favored as a result of female choice. Estrous females are more receptive when mounted
by a male who has just dominated another than when mounted by a male of similar rank
who has been resting or recently displaced by a still more dominant male.
A general argument is made that in species where social status of males is correlated
with their genetic fitness, female choice is likely to be based on social signals which are
used in competition between males.
INTRODUCTION
grouse (Kruijt et al., 1972); sage grouse
(Scott, 1942; Wiley, 1973); golden-headed
manakins (Lill, 1976); village indigobirds
(Payne and Payne, 1977); red deer (Clutton-Brock et al, 1979); elephant seals (Le
Boeuf and Peterson, 1969; Le Boeuf,
1974); baboons (Hausfater, 1975).
Because the correlation between aggression and reproductive success suggests that
aggressiveness among males will be strongly favored, a great deal of research has focused on the adaptive value of highly aggressive behavior. However, male-male
competition may also be costly to the participants. Contrary to the generalizations
of Lorenz (1966) and others, intraspecific
aggression among males may result in severe injuries (Gorsuch, 1934; Geist, 1974;
Clutton-Brock et al., 1979) or even death
(McHugh, 1958; Bannikov et al., 1967;
Geist, 1971; Potter etal, 1976; Wilkenson
and Shank, 1976). Since costs as well as
benefits are associated with aggressive in1
From the Symposium on Social Signals—Compar- teractions, we might expect the probability
ative and Endocrine Aspects presented at the Annual
Meeting of the American Society of Zoologists, 27— of one male threatening another to vary
with the particular situation and social set30 December, at Tampa, Florida.
2
Author's current address is: Department of Bi- ting. That is, males who initiate encounters
ology, University of California at Los Angeles, Los primarily when costs are minimal and/or
Angeles, CA 90024 and Department of Ornithology, when benefits are maximal should be faLos Angeles County Museum of Natural History, 900
vored by natural selection. At present
Exposition Blvd., Los Angeles, CA 90007.
In many species onset of breeding activity is characterized by intense competition
among males for access to females. Aggressive interactions play a very important
role with respect to the reproductive success of males in a wide variety of vertebrates and invertebrates. For example,
success in obtaining a high quality territory
or high social rank through aggressive interactions has been shown to be positively
correlated with the number of copulations
a male obtains in the following animals:
spider mites (Potter et al., 1976); dragonflies (Campanella and Wolf, 1974); bullfrogs (Howard, 1978); toads (Davies and
Halliday, 1977, 1979); anolis lizards (Trivers, 1976); pupfish (Kodric-Brown, 1977);
ruffs (Hogan-Warburg, 1966); prairie
chickens (Robel and Ballard, 1974); black
197
198
CATHLEEN R. COX
there is relatively little empirical data on
the specific contexts in which males threaten one another. The present paper describes rny attempt to approach this problem through observations on the frequency
and circumstances under which breeding
northern elephant seal males, Mirounga
angustirostris, initiate aggressive encounters.
this period she copulates with one or more
males. Males, however, attempt to mate females long before they become estrous (Le
Boeuf, 1972). Non-estrous females always
respond with resistance in the form of
threat vocalizations and attempts to ej£
cape, and estrous females typically respond in the same manner. This female
"protest" alerts surrounding males to the
attempted copulation, and if there is a
Biology of the elephant seal
more dominant male in the vicinity, he
Northern elephant seals are widely threatens and displaces the mounting male
known for their extreme polygyny, sexual (Cox and Le Boeuf, 1977).
dimorphism, and aggressiveness. Each
year from December through March the Expected frequency and contexts
seals haul out on islands off the west coast of aggression
of North America where parturition and
In elephant seals some obvious costs as
breeding take place. During this period well as benefits are associated with agonismales engage in only three types of activ- tic interactions between males. There are
ity: threatening or avoiding the threats of a number of ways in which engaging in
other males, mounting and mating with aggressive interactions may ultimately refemales, and resting supine on the beach. duce a male's reproductive success. WhenA variety of movements, postures, and ever a male enters into combat, the risk of
vocalizations are used by males to signal injury is substantial. These injuries someaggressive intent (Bartholomew, 1952; times lead to death; more typically, males
Bartholomew and Collias, 1962; Le Boeuf, who become involved in escalated fights
1971, 1972; Sandegren, 1976; Shipley et suffer relatively superficial wounds but apal., 1981). Before or after issuing a pos- pear exhausted and subsequently avoid sotural or vocal threat, the challenging male cial interactions for several days. The loser
may move towards the target of his aggres- may fall substantially in social rank. Males
sion. Typically, the recipient moves away engaged in agonistic exchanges, whether
before physical contact becomes imma- simply threatening another male or acnent. Occasionally the challenged male re- tually engaged in combat, cannot simultasponds with a threat of his own, and the neously attend to other males who are likechallenger moves off. If neither male re- ly to enter the harem and are unable to
treats, direct combat ensues (see Le Boeuf, prevent such males from approaching and
mating females. These males may lose cop1971).
The aggregate result of dominance re- ulations that would otherwise have been
lations established through threats and available to them. Furthermore, since
fights between pairs of males is a linear males fast during the entire breeding seasocial dominance hierarchy. Each male at- son they are severely limited with respect
tempts to gain access and to mate with as to total energy expenditure; energy spent
many females as possible, and to prevent threatening other males may be more efother males from doing the same. As a fectively utilized by servicing females.
consequence, there is a strong, positive
There are at least two ways in which inicorrelation between aggressiveness, social tiating aggressive interactions may inrank, and the number of copulations a crease a male's reproductive success. When
male obtains (Le Boeuf and Peterson, one male threatens or displaces another,
1969; Le Boeuf, 1974).
he may prevent the subordinate male from
Females gather in dense aggregations gaining access to females. This is a highly
referred to as pods or "harems." Each fe- significant outcome for in an extremely
male remains on land for approximately polygynous species such as the northern
35 days, and during the last 3—5 days of elephant seal, the fitness of a male is pri-
CONTEXT OF AGONISTIC ENCOUNTERS
marily a function of the number of females
he can keep inaccessible to other males
(Williams, 1975). In addition, as is elaborated below, a male who demonstrates his
dominance by threatening other males
#tiay benefit from increased receptivity on
the part of nearby females.
At present it is not possible to directly
measure costs and benefits associated with
particular behaviors. However, it is possible to specify situations in which probable
costs will be relatively low, and situations in
which probable benefits will be relatively
high.
For example, costs could be minimized
by behavior that requires little energy expenditure and is not likely to result in injury. If males are acting in such a manner
we would expect to observe the following:
199
2. Males in the immediate vicinity of females should be threatened more frequently than males on the periphery of
the breeding beach.
3. Males mounting females should be
threatened more frequently than those
engaged in other activities.
4. Males mounting estrous females should
be threatened more frequently than
males mounting non-estrous females.
5. High ranking males should issue threats
prior to mounting females.
In order to determine if the behavior of
northern elephant seal males was consistent with these predictions, I observed a
breeding population of M. angustirostris
during three successive years.
STUDY SITE AND METHODS
All observations reported below were
1. Aggressive encounters should not be made on Ano Nuevo Island (ANI), San
initiated frequently and little time Mateo County, California. The study peshould be spent in aggressive interac- riod covered December through March of
tions.
1973, 1974, and 1975. Due to federal pro2. Threats should be directed to subordi- tection the elephant seal population exnate rather than to more dominant panded considerably during this period.
males.
The number of females present on ANI
3. The frequency with which threats are during the 1973, 1974, and 1975 breeding
given should be inversely proportional seasons was 370,436, and 556 respectively;
to the likelihood of being detected and number of males remained constant at
chased off by a more dominant male. 180. Breeding took place in three locaThat is, low ranking males should issue tions: the main (point) beach, a small cove,
fewer threats than high ranking males. and the sandy saddle of the island (areas
4. Encounters should be initiated with 17, 3W, and 19E in Fig. 6 of Reiter et al,
threats rather than by direct attack, and 1978). In all three years the largest breedescalation should occur only if the op- ing group assembled on the point beach.
ponent fails to respond.
At the beginning of each breeding sea5. Threat sequences should be terminated son all males were individually marked
as soon as the opponent indicates sub- with peroxide and assigned to one of three
mission.
age categories based on comparison of
overall
size and development of secondary
Benefits could be maximized by directsexual
characteristics
with tagged, knowning threats primarily to males who would
age
animals
(as
described
in Le Boeuf,
otherwise be likely to succeed in breeding.
1974).
These
categories
were
as follows:
And, if females are, in fact, more receptive
Subadult
3
(SA3),
6-7
yr
of
age;
Subadult
to males who demonstrate their domiage;
and
Adult
(AD), 84
(SA4),
7-8
yr
of
nance, males should issue threats prior to
mounting. If males are acting so as to max- 14+ yr of age. Since dominance was sizeimize these outcomes, we would expect to related and older males were larger than
younger males, there existed transitive
observe the following:
size-related dominance relationships be1. Males residing on breeding beaches tween males in the three categories. All
should be threatened more frequently adults were dominant to SA4s and SA3s;
all SA4s were dominant to SA3s.
than males on non-breeding beaches.
200
CATHLEEN R. COX
Qualitative observations on male-male
agonistic interactions were made during
each of the 3 yr from a blind overlooking
the point beach.
During 1974 frequency of agonistic encounters among males was sampled on
each of the three breeding beaches as well
as on three non-breeding beaches frequented by males (the latter beaches correspond to areas 3E, 19W, and 20 in Fig.
6 of Reiter et al, 1978). The basic procedure involved counting all threats and
fights which took place during a 30-min
period. In order to control for possible effects of crowding resulting from changes
in tide level, aggression was counted during each of three 30-min periods daily, at
times corresponding to low, medium, and
high tides. After the interactions were
counted, the number of males present in
each age category was noted, and mean
number of threats per male per hour was
calculated.
Relative frequency and types of threats
given by males in the three age categories
were sampled for 4 hr daily on each of 38
days in 1974. The procedure consisted of
scanning the point beach from left to right
until the start of an encounter was observed. The individuals involved, their activities just prior to the interaction, sequences of aggressive and/or submissive
signals exchanged, outcome of the encounter, and time from initiation to termination were noted. The position of the
challenged male relative to females was
also recorded. This was done by constructing an imaginary line around the perimeter of the female aggregation. If the male
was partially or entirely within the area
bounded by the line, he was considered to
be in the female harem. Otherwise he was
considered to be outside the harem. When
the description of the interaction was complete the scan was continued, starting from
the point where the last recorded interaction had taken place. At the end of each
hour of observation the number of males
present in each age category was recorded.
Interactions between males and 40
marked females were made on the point
beach during the 1975 breeding season.
The marked females were observed daily
from the time of their arrival through
their departure, a period of approximately
35 days. A female was categorized as nonestrous until her first copulation (approximately 24 days subsequent to parturition).
The female was considered to be estrou©
from the time of her first through her last
copulation, some 3-5 days later. Each time
a marked female was mounted, the male's
behavior prior to mounting, the female's
response, the outcome of the mount (selfterminated by the mounting male prior to
intromission, interruption by a neighboring male prior to intromission, or intromission), and time from start of mount to termination or intromission were recorded.
Female responses were categorized as follows: total protest—the female gave threat
vocalizations, attempted to escape, and
struck the male in his genital region with
her rear flippers for the entire duration of
the mount; partial protest—the female was
resistant for only part of the duration of
the mount; or no protest—the female was
passive or even facilitated intromission.
RESULTS
Minimizing energy expenditure and
risk of injury
Frequency of threats and time spent in aggressive interactions. On the point beach the
mean number of threats issued per male
per hour was 2.7 ± 1.4. The great majority
of agonistic interactions were very brief.
The mean duration of 188 interactions observed consecutively over a 3-day period
was 11.9 ± 11.7 sec. Using these figures I
calculate that on the average each male
spent 31.5 sec/hr or 0.9% of his time
threatening or fighting with other males.
Le Boeuf and Peterson (1969) reported
that the most dominant (alpha) male issued more threats than any other member
of the breeding assembly, and subsequent
observations on AN I have produced the
same finding. Therefore, in order to get
a picture of the way in which the most aggressive male budgeted his time I observed
MOO, the alpha male on the point beach,
continuously for 8 hr on 1 February 1974.
On this day MOO issued 80 threats, two of
which escalated to the point of delivering
201
CONTEXT OF AGONISTIC ENCOUNTERS
TABLE 1..
Age category
of initiator
P
Adult
SA4
SA3
Totals
Age category of recipient relative• to challenging male. *
Recipient older
4/67 == 6.0%
4/22 == 18.2%
8/428 = 1-9%
Recipient same age
162/339
23/67
18/22
203/428
=
=
=
=
47.8%
34.3%
81.8%
47.4%
Recipient younger
177/339 = 52.2%
40/67 = 59.7%
217/428 = 50.7%
* Threats directed to males who were older, the same age, or younger are shown as proportions and
percentages of total number of threats observed. Older males are dominant to younger males.
blows. He attempted 20 copulations and
succeeded in eight of these attempts. During the remainder of the observation period MOO rested in a prone position, apparently dozing. Direct measurement of
the time spent in these activities was as follows: threats to other males, 20.1 min; copulation or attempts to do so, 40.1 min; resting 419.8 min. Thus, during the course of
a typical day the alpha male spent 4.2% of
his time threatening other males, 8.3% of
his time attempting to mate, and 87.5% of
his time resting. In short, even the most
aggressive male on the island spent little
time and energy threatening other males.
Rank of recipient relative to initiator. In
more than 98% of the interactions observed the initiator challenged a male who
was of approximately the same age or
younger (Table 1). Although more than
half of the males on the point beach were
adults, less than 5% (4/89) of the threats
issued by subadults were directed to
adults. Clearly subadults were not threatening others in a random fashion. In each
of the four cases where an adult male was
challenged by a younger male, the subadult moved very rapidly away when the
adult reared-up and returned the challenge. The alacrity of the subadult's retreat
made it appear as though he had mistakenly challenged the adult. In two of these
cases the subadult's sharp retreat was not
speedy enough and the subordinate was
bitten on the hindquarters as he fled. Since
older males are dominant to younger ones,
these observations are consistent with the
notion that males avoid challenging or interacting with more dominant males.
Frequency of threats by males varying in so-
cial rank. When one male threatens
another, the action also alerts neighboring
males. If there is a more dominant male in
the vicinity he may chase off one or both
of the males involved in the agonistic exchange. Indeed, this occurred in 11.2%
(41/366) of the encounters observed in
1973. The lower a male's social rank, the
greater the number of males capable of
and likely to threaten him. For this reason
the probable cost of threatening another
male, even a subordinate one, will be correspondingly greater for lower ranking
males. Because of the relationship between
age and dominance we would expect older
males to initiate a greater number of encounters than younger males. Table 2
shows that adults issued more than three
times the number of threats that subadults
did and SA4s issued more than twice the
number of threats that SA3s did.
Data presented by Le Boeuf and Peterson (1969) deliniates a similar relationship
between social rank and number of threats
issued by the four highest ranking males
present on ANI in 1968. The most dominant male gave more than twice the number of threats than the second ranking
male did, the second and third ranking
males gave an equal number of threats,
and the fourth ranking male gave still fewer threats.
Initiation of encounters. The sequence of
signals exchanged in agonistic encounters
was described in detail for 428 interactions. Most challenges (93.9%) were initiated with postural or vocal threats rather
than by direct attack. The categories into
which initial challenges fell were as follows: simply turning to face the recipient
of the threat (2.8%), turning towards the
recipient and rearing up (21.9%), moving
towards the recipient and then pausing
(32.5%), vocal threat (36.7%), moving to-
202
CATHLEEN R. COX
TABLE 2. Relative number of threats issued by males in
three age categories. *
Mean
Age
of
initiator
Adult
SA4
SA3
Totals
No.
threats males
observed present
339
67
22
428
22.3
11.3
8.8
42.3
Mean
no.
per
male
15.2
6.0
2.5
10.1
No. threats by
older males
No. threats by
younger males
15.2/4.6 = 3.34%
6 .0/2.5 = 2.37%
* Data gathered by scan sampling on point beach.
wards and striking the recipient (6.1%).
Only 2.3% of the encounters initiated by
threat rather than by direct attack subsequently escalated to the point where blows
were given. The effect of initiating challenges with postural threats was to reduce,
or at least delay costs associated with direct
combat.
Termination of encounters. Typically the
challenging male ceased his threats very
shortly after the recipient moved away and
thus signaled submission. Time from submission to termination of threat by the
challenging male was recorded for 90 interactions; mean interval was 2.1 ± 3.7 sec.
By terminating his threats in this manner,
the dominant male avoided unnecessary
energy expenditure.
Preventing others from breeding
Aggression on breeding versus non-breeding
beaches. The number of aggressive interactions per male per hour was compared
for beaches on which females resided and
on beaches occupied only by males. The
respective means were 2.1 ± 1.6 and 0.2
± 0.3 (t = 5.23; df, 97; P < .01). In short,
males hauled-out on breeding beaches
challenged others and were themselves
challenged considerably more frequently
than males on non-breeding beaches.
Threats to males in the harem versus periph-
ery of beach. On average there were 44
males on the point beach, 16 in the female
harem and 28 outside of it. I observed 347
agonistic encounters within the harem and
187 elsewhere on the beach. Thus during
the period of time covered by my observations, males within the harem were
threatened 21.7 (347/16) times each, while
males on the periphery of the beach received only 6.7 (187/28) threats apiece.
The data clearly show that males in close
proximity to females were challenged considerably more frequently than those at a
greater distance. This was true e v e ^
though males on the periphery were spatially closer to one another than those residing in the harem.
Threats to mounting males. Within the har-
em 40.6% (141/347) of all threats given
were directed to males who were mounting
or copulating and 59.4% (206/347) were
directed to males otherwise engaged (resting or threatening other males). If males
are challenged irrespective of their activities, the number of threats a male receives
during a given activity should be proportional to the amount of time spent in that
activity. Based on data collected in 1973 I
estimate that males in the harem spend
about 5% of their time in sexual activities.
(MOO, the alpha male described earlier,
obtained the greatest number of copulations in 1974 and spent 9% of his time
mounting and copulating.) Since 40.6% of
all threats were directed to males engaged
in sexual activities, it is clear that these
males were threatened at a disproportionately high rate. Furthermore, males who
were threatened while mounting females
continued to be threatened after they had
moved away for longer periods than males
who had simply been resting in proximity
of females. Mean duration of threats subsequent to submission for these two groups
was 3.3 ± 3.8 sec and 1.1 ± 3.4 sec respectively (t = 2.49; df, 74; P < .01).
Threats to males mounting estrous versus
non-estrous females. T h e r e was no signifi-
cant difference in the percent of mounts
to estrous and non-estrous females which
were interrupted: 40.4% (115/285) and
48.0% (135/281) respectively (z = 1.84,
P > .05). However, all mounts to non-estrous females were totally protested while
only 62.7% of those to estrous were totally
protested. A mount in which the female
protests is far more likely to be detected
and interrupted than a mount in which the
female responds passively (Cox and Le
Boeuf, 1977). Do interrupting males preferentially respond to protesting estrous fe-
CONTEXT OF AGONISTIC ENCOUNTERS
203
TABLE 3. Proportion and percent of mounts to which estrous females responded receptively (partial or no protest).
Activity of male prior to mounting
Age category of male
Dominated another male
Adult
49/80 = 61.3%
2/4 = 50.0%
0/1 = 0.0%
51/85 = 60.0%
SA4
•
SA3
Total
males over protesting non-estrous females?
The data suggests they do: 58.1% (97/167)
of protested mounts involving estrous females were interrupted, as compared with
48.0% (135/281) protested mounts involving non-estrous females (z = 2.05, P <
.05).
Male aggression and female receptivity
Previously published data (Table 3 in
Cox and Le Boeuf, 1977) shows that elephant seal females tend to behave more
receptively towards older and more dominant males than towards lower ranking
males. How might a female distinguish
among males? One possibility is on the basis of size; another possibility is on the basis
of behavior. If females do distinguish
among males on the basis of their behavior, they may act as a selective force favoring the evolution of the preferred type of
male behavior. In the following section of
the paper the relationships between age
category and behavior of males prior to
mounting, the response of females, the effects of the female's response on the male's
reproductive success, and the association
between aggression and attempts to mate
are explored.
Male-male aggression and female receptivity.
In 177 cases I was able to record the activity of the male prior to mounting and the
response of the female. Table 3 shows that
females responded differentially to males
on the basis of both their age and their
behavior. Comparison of female responses
to mounts by males who varied in age but
behaved similarly shows that females were
more likely to respond receptively to older,
larger males than to younger, smaller
males. Females uniformly rejected mounts
by SA3 males, however, their response to
SA4 and adult males depended greatly on
No interaction
16/43
4/15
0/9
20/67
= 37.2%
= 26.7%
= 0.0%
= 29.9%
Subordinate to another male
3/17
0/3
0/5
3/25
= 17.7%
= 0.0%
= 0.0%
= 12.0%
the behavior of the male prior to mounting. Females were much more likely to respond receptively to an adult male who
had just dominated another male than to
one who had been dominated (z = 15.56,
P < .01).
When a female protested, the male often
dismounted but remained nearby and after a brief interlude again attempted to
mate with the female. In 85 such cases I
observed the activity of the male during
the interval between mounts, and the subsequent response of the female. In only
6.6% (8/22) of the cases in which the male
simply rested or was dominated by another
male did the female subsequently become
more receptive. However, in 44.4% (28/63)
of the cases where the male threatened
and dominated another, the female showed
increased receptivity when remounted
(z = 6.08, P < .01). This observation suggests that the female was responding to the
male on the basis of his behavior rather
than on the basis of individual recognition.
Effect of female receptivity on male repro-
ductive success. Female protests increase the
probability that the mounting male will be
interrupted, with the effect of decreasing
the reproductive success of subordinate
males. However, high ranking males are
not likely to be interrupted, and they frequently mate females despite their protests. Since this is the case, we must ask if
the behavior of the female affects the outcome of attempts to mate by dominant
males in any way. To explore this question
the outcomes of all mounts to estrous females by adult males which were not terminated as a result of interruption by other males were tabulated. (Uninterrupted
mounts were either terminated by the
mounting male of his own accord or led to
intromission.) The data show that the fe-
204
CATHLEEN R.
COX
TABLE 4. Activities of males during 3-min period prior to mounting shoxvn as proportions and percentages.
Age category
of mounting male
Adult
SA4
SA3
All males
Threatened another male
80/140
4/22
1/15
85/177
= 57.1%
= 18.2%
= 6.7%
= 48.0%
male's response greatly influenced the outcome of mating attempts by adult males.
The percent of mounts which were unprotested, partially protested, and totally protested which led to intromission were 78.1
(25/32), 65.5 (36/55), and 19.3 (11/57) respectively. Uninterrupted mounts which
were not protested, or only partially protested were more than three times as likely
to culminate with intromission than uninterrupted totally protested mounts (z =
13.76, P < .01).
The importance of the female's behavior
can also be seen by considering the time it
took successful males to obtain intromission. Time from initiation of the mount to
intromission was recorded for 191 cases.
Mean durations were as follows: unprotested mounts, 93.6 ± 82.6 sec; partially
protested mounts, 125.4 ± 100.3 sec; totally protested mounts, 165.6 ± 133.9 sec
{F = 3.75; df, 2,188; P < .05). Males
mounting receptive females obtained intromission considerably more rapidly than
males mounting unreceptive females.
Activity of males prior to mounting. Taken
together the above data suggest that estrous females are most receptive to males
who have just demonstrated their social
dominance, and least receptive to males
who have just been dominated. Female receptivity is important to males in so far as
it increases the likelihood and speed of obtaining intromission. Accordingly it would
be to the advantage of high ranking males
to express their dominance prior to
mounting. However, it would be to the advantage of low ranking males to avoid interactions with other males prior to
mounting. Table 4 shows the activities of
males during the 3-minute period prior to
mounting. Adult males most frequently
displaced another male prior to mounting,
Rested—no interaction
Threatened by another male
43/140 = 30.7%
15/22 =68.2%
17/140= 12.1%
9/15 = 60.0%
67/177 = 37.9%
3/22 = 13.6%
5/15 =33.3%
25/177 = J4.1%
while subadults typically rested. Indeed,
the few subadult males who were successful in breeding were typically unaggressive
towards other males (Cox, unpublished
data).
DISCUSSION
An observer overlooking a breeding aggregation of elephant seals on a crowded
rookery such as AN I cannot help but be
impressed with the apparently high level
of aggression among males. The dramatic
impact of 2 two-ton males slamming up
against one another is great and for this
reason male-male aggression has been described in considerable detail in earlier
publications (Bartholomew, 1952; Le Boeuf
and Peterson, 1969; Le Boeuf, 1971,
1972). The importance of aggressive interactions with respect to establishing social
dominance and thereby gaining access to
females has been convincingly demonstrated (Le Boeuf and Peterson, 1969; Le
Boeuf, 1974) and frequently cited.
Although there is almost always one or
more aggressive interaction in progress on
a large breeding beach at any particular
moment, the frequency with which individuals engage in such interactions is actually quite low. On average males present
during the breeding season spend less
than one percent of their time in agonistic
activities. Threats are typically directed by
larger (older) and more dominant males to
smaller (younger) and more subordinate
males, and not vice versa. Blows are rarely
exchanged, primarily because aggressive
enounters are typically initiated by threat
rather than direct contact, and the recipient, usually a less dominant male avoids
the approach of the challenger. As soon as
the recipient moves away, the challenging
male ceases to threaten him and the inter-
CONTEXT OF AGONISTIC ENCOUNTERS
action ends. These data are consistent with
the idea that males generally threaten one
another when the probable costs, as estimated by time occupied, energy expended
and risk of injury, are low.
0 A variety of measures indicates that
among elephant seals the probability that
one male will threaten another also varies
with the location and activity of the other.
For example, males on breeding beaches
are more likely to be threatened than
males on non-breeding beaches, males in
close proximity to females are threatened
more frequently than those on the periphery of the breeding beach, male mounting
females, regardless of their estrous state,
are threatened more frequently than those
otherwise occupied, and males mounting
protesting estrous females are threatened
more frequently than those mounting protesting non-estrous females. The amount
of energy spent threatening others also
tends to vary with the activity of the recipient. Aggression towards a male who is
mounting or in copula is particularly direct
and intense. For example, instances where
one male approaches and attacks another
without first giving vocal and visual signals
are rare. It is my impression that this occurs only when the recipient is moving
within the female harem or attempting to
copulate. High ranking males may even interrupt their own copulations to threaten
others under these circumstances (Bartholomew, 1952; Le Boeuf, 1971, 1972). In
short, the greater the likelihood that a
male will succeed in copulating, the greater the probability he will be threatened,
and the greater the intensity of the threat.
These data clearly support the idea that
males are more likely to threaten others
when the benefits, as measured by likelihood of preventing other males from copulating are great.
Intraspecific aggression has been among
the most frequently described and thoroughly studied aspects of animal behavior
during the past century. Research in the
area was nicely summarized by Collias in
1944 who noted that aggression among
groups of animals was most likely to be
observed in connection with competition
for food, mates, or territory, and that
205
amount of aggression varied with degree
of resource shortage. In recent years researchers have begun to focus on the question of when individual members of a
group are likely to initiate or avoid aggressive interactions. Using this approach
Maynard Smith and Price (1973), Parker
(1974), and Maynard Smith and Parker
(1976) have formulated optimization
models of contest behavior based on game
theory. This model has already stimulated
research on contest behavior in situations
where either the cost of entering into an
agonistic exchange or the probable benefits vary. Some examples follow.
Several researchers have presented data
concerning the cost of an encounter and
the probability that one of the combatants
will retreat. In each of these studies it is
shown that success in winning is positively
associated with size, and it is assumed that
the potential cost of a lengthy interaction
is greater for the smaller individual who is
more likely to sustain injury (Helfman,
1977; Brace and Pavey, 1978; Davies and
Halliday, 1978). The willingness of individuals to persist in display or combat as
a function of the likely benefit of winning
has also been treated (Davies, 1978; Clutton-Brock et al, 1979; Itzkowitz, 1979;
Reichert, 1979).
In the study of contest behavior, certain
benefits of winning, such as direct access
to a limited resource may be obvious. But,
other benefits may be less direct and therefore easily overlooked. This point is well
illustrated in elephant seals where it is
common to observe threats which do not
appear to be precipitated by any particular
activity on the part of the recipient. Displacing a harmless male would seem to be
costly with respect to energy expenditure
and to have little obvious payoff. However,
consideration of this behavior from the female's point of view, and her response to
these males can help us to understand the
persistence of such behavior.
In elephant seals social dominance is a
function both of age (through increase in
size) and physical fitness. To the extent
that ability to survive to an old age in
sound physiological condition is genetically transmitted, females who mate with the
206
CATHLEEN R. COX
most dominant males will bear offspring
who will also be likely to survive and reproduce. In short, mating with dominant
males will be favored in females by natural
selection. One way the female can achieve
this end is by rejecting all males with the
effect that only the most dominant male is
able to mate with her despite her protest
(Cox and Le Boeuf, 1977). However, if a
female can identify high ranking males in
some other fashion, particularly a less
stressful one, we might expect females to
behave receptively towards them. Data
presented in this paper show that estrous
females are more likely to respond receptively (with only partial or no protest) if
the mounting male has just dominated
another male. When the female protests
only partially, or not at all, the male is
more likely to gain intromission and he
gains it more quickly. Thus the behavior
of the female is a potentially strong selective force which acts to favor aggression
prior to mounting—at least by high ranking males.
From the female point of view, any male
in the midst of the harem who can threaten others without himself being displaced
is a potentially good mate. Female preferences for males of this sort may select
for the display of aggression prior to
mounting. Such selection pressure may so
favor aggressiveness that males will threaten other males even when they are resting
quietly some distance from the nearest female, accounting for the apparently unprovoked aggression between males which
does regularly occur. Female preferences
for males who express their dominance
may also help to explain a behavior which
has previously been labeled "in vacuo";
that is, the behavior of high ranking males
who frequently rear-up and issue clapthreats in an undirected manner, without
challenging any male in particular. If such
bellows result in greater receptivity on the
part of females, as the preliminary data
suggests they do, the evolution of "in vacuo" threats will be favored.
It is of particular interest that the corpus
of behavior which is involved in displacing
males simultaneously affects the receptivity of females. An analogy with bird song
is immediately apparent. In many territorial birds the male's song functions both to
prevent potential male rivals from approaching and also to attract females to the
territory of the singer (Thorpe, 1961;
Armstrong, 1973). Observation of specif
which sing complicated songs, or many different songs, have shown this effect in
some detail. Payne and Payne (1977) report that village indigobird males, Vidua
chalybeata, who sing at higher rates and for
longer periods are more successful in defending their call sites from other males
and attract more females. Similarly, in
mockingbirds, Mimus polyglottos, the greater the number of songs a male sings the
higher the quality of the territory which he
is able to defend, and the more rapidly he
obtains a mate (Howard, 1974).
This analogy may also hold for other
groups in which acoustical communication
is important. For example, in the Pacific
tree frog, Hyla regilla, male mating calls
discourage other males from establishing
mating territories nearby (Whitney and
Krebs, 1975a) and attract females (Whitney and Krebs, 19756). Calling functions
in the same way in H. versicolor (Fellers,
1975, 1979). Calling by male field crickets,
Gryllus integer, inhibits calling by neighboring males and attracts females (Cade,
1979). Purring sounds made by male satinfin shiners, Notropis analostanus, stimu-
late aggressive interactions between males,
and courtship by females (Stout, 1963).
Other displays, for example particular
color patterns or ritualized movements,
may also function simultaneously as threats
to males and invitations to females. During
the breeding season male corkwing wrasses, Crenilabrus melops, develop bright blue
and yellow coloration about the head and
opercular regions which warn other males
against entering the territory and attract
females to breeding males (Potts, 1974). It
is well known that the red nuptial coloration or the belly of the male threespine
sticklebacks, Gasterosteus aculeatus, inhibits
territorial intrusion by conspecific males
and stimualtes courtship in females (Tinbergen, 1951). More recently Semler
(1971) has reported that in a population of
sticklebacks which is polymorphic with re-
CONTEXT OF AGONISTIC ENCOUNTERS
spect to nuptial coloration, females preferentially pair with red-bellied males. The
antlers of red deer stags, Cervus elaphits,
and of caribou stags, Rangifer tarandus
granti, are thought to inhibit challenges by
0val males and attract hinds (Lincoln,
1972; Bubenik, 1975). McKinney (1975)
describes the up-down display which is given by a male green-winged teal, Anas carolinensis, when both his mate and a male
rival are present and he concludes that the
display serves both to threaten the rival
and attract the attention of the female.
Hogan-Warburg (1966) reports that reeves,
Philomachus pugnax, may be stimulated to
crouch for copulation when the territorial
ruff gives agonistic displays or attacks
males outside his residence.
Many more examples of social signals
which function both in competition and in
courtship could be given. My point in listing a number of them is to suggest that the
response of Mirounga females to aggressive males is not a unique one. Furthermore, it is not likely that this dual function
of certain social signals which is observed
in many species across a wide range of
taxonomic groups is the result of chance
alone. It is often argued that social dominance and fitness of males are positively
correlated (Trivers, 1972). If this is so, females who mate with the most dominant
males will be favored by natural selection.
How might females judge the status of a
male? The signals which are used by males
to express their dominance over other
males should be precisely those by which
the female can assess a male's status. Such
signals may be relatively stereotyped, as in
bird song, or quite variable, as in aggressive interactions among male elephant
seals. In any case, in order for selection for
favor female choice on the basis of such
signals, the signals must be positively correlated with the male's ability to defeat other males. This could occur in two ways: (1)
if the quality of the signal, for example
brightness of coloration, size, or resonant
frequency of vocalization is a reflection of
the male's overall vigor, physiological
soundness, and probable ability to overcome other males in combat, or (2) if by virtue of giving the signal, as in the case of
207
vocal and visual threats issued by elephant
seals, the male reveals his location and
breeding condition to other males who
may challenge him. As a consequence, the
male's ability to maintain his spatial location over time reflects his ability to dominate other males. As Dawkins and Krebs
(1978) remark in their discussion of bird
song, "the fact that the same music is used
both to repel (rivals) and attract (females)
need not surprise us."
In species where the same social signals
function both in intraspecific aggression
and in courtship, the study of agonistic interactions among males, and its analysis
with respect to game theory may be considerably more complicated than previously realized. When observing aggression
between males it is important to note the
setting in which it occurs. If members of
the species in question are within visual or
auditory range of one another, a signal
which is directed primarily to one individual may be detected by others as well. Although threats directed by one male to
another may function immediately to displace a competitor from a limited resource, females in the vicinity may also be
attentive to the interaction and may subsequently alter their response to these
males accordingly. The reproductive benefits to be gained by a male through aggressive interactions with other males can
only be fully understood if the responses
of females are also considered.
ACKNOWLEDGMENTS
Special thanks are due to Burney J. Le
Boeuf who introduced me to the study of
Mirounga and to theories of social behavior. Field assistance was provided by Mark
Pierson, Mike Bonnell, Joanne Reiter, and
Nell Lee Stinson. Howard F. Andrews, Jeffrey J. Wine, Edward H. Miller, and Robert A. Pugsley have reviewed and made
valuable comments on various drafts of the
manuscript. The field work was supported
in part by a Stanford University Fellowship
to the author and by NSF Grant BMS 7401363A02 to B. J. Le Boeuf. Subsequent
analysis was made possible by NIMH
Grant T32 MH14280 to the Animal Behavior/Biopsychology Training Program
208
CATHLEEN R. COX
of the American Museum of Natural History and the City University of New York.
Geist, V. 1971. Mountain sheep. University of Chicago
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