HORMONES

AND BEHAVIOR,

3, 375-396 (1972)

The Way in Which Testosterone Controls the Social and Sexual

Behavior of the Red Deer Stag (Cervus elaphus)

G. A. LINCOLN,l

FIONA

GUINNESS,

and R. V. SHORT2

Department of Veterinary Clinical Studies,

Madingley Road, Cambridge, England

For 10 months of the year red deer stags live together in social
groups. These groups then break up, and the animals exhibit a complex
pattern of sexual behavior during a short rutting season in September and
October. We have utilized this clear separation between social and sexual
behavior to try and establish experimentally
in free-ranging wild animals the
way in which testosterone influences the two types of activity.
It was found that castration of adult stags at any season of the year
abolished all subsequent rutting behavior. The animals also became less
aggressive within the bachelor groups and thus dropped in social status.
When castrates were implanted with testosterone in December they developed all aspects of rutting behavior within a few weeks and showed
conspicuous aggressiveness to other stags, and regained their dominance on
returning to the bachelor group. When castrates were given implants of
testosterone in April and June, no immediate rutting response was elicited,
although increased social aggressiveness was again apparent; but subsequently these animals developed rutting behavior in the autumn at the normal
rutting time. Testosterone implants in intact stags at any season failed to
induce a second rut, but the animals did show striking changes in
aggression.
The results are complicated by the fact that the antler cycle of the
stag is controlled by the level of testosterone, and, therefore, many of the
experiments
have led to changes in the antlers which have themselves
affected behavior. Direct effects of testosterone on behavior can only be
inferred when the hormone treatment is unaccompanied by changes in the
antlers.
The general conclusion is that testosterone plays largely a permissive
role. in the control of rutting behavior; the presence of the hormone is
essential, but other factors act as an overriding control, and determine the
time of year at which rutting behavior is expressed. In contrast, testosterone has a direct inductive effect on social aggressive behavior, which can
be induced at any season of the year.
IPresent
Street, P.O. Box
2Present
Chalmers Street,

address: Unit of Reproductive

Biology, Life Sciences Building, Crown
147, Liverpool, L69 3BX, England.
address: Medical Research Council Unit of Reproductive
Biology, 39
Edinburgh, EH3 9ER, Scotland.

375
Copyright @ 1972 by Academic Press, Inc.
All rights of reproduction in any form reserved.

376

LINCOLN,GUINNESS,AND SHORT

Many studies have now been carried out in male laboratory rodents to
investigate the role of testosterone in social and sexual behavior (reviewed in
Garattini and Sigg, 1969), and a limited number of experiments have also
been performed in male dogs (Le Boeuf, 1970), cats (Rosenblatt and Aronson,
1958), sheep (Clegg, Beamer, and Bermant, 1969) and primates (Clark and
Birch, 1945; Goy, 1970; Rose, Holaday, and Bernstein, 1971; Michael, 1972).
The general conclusion from this work seems to be that aggressive social
behavior is undoubtedly under androgenic control, whereas copulatory
activity, once established, is less immediately influenced by testosterone. In
domestic animals and primates, some sexual behavior may persist for months
or years after castration. But one of the problems in this type of work is that
social and sexual behavior tend to be inextricably mixed, to the extent that a
sexual stimulus may even be used to elicit social aggression.
It should be possible to separate social fromsexual behavior by studying
male seasonal breeders during the period of the year when there is no sexual
activity, and by using a neutral stimulus such as competition for food in order
to initiate the aggression. During the period of sexual activity or rut, it should
also be possible to study the extent to which a variety of types of male sexual
behavior, rather than just copulatory activity, are controlled by the level of
testosterone.
It was for these reasons that we chose to study the role of testosterone
in controlling the social and sexual behavior of red deer stags (Cervus elqhus)
living in the wild. We had previously established that these animals show
pronounced changes in testosterone secretion during the year, with maximal
values during the rut in the autumn, and almost undetectable levels in the
spring and early summer (Lincoln, Youngson, and Short, 1970). Stags also
show pronounced changes in social and sexual behavior during the year, and
our observations suggested that the behavioral changes might be causally
related to the testosterone levels.
One obvious way in which testosterone controls aggression in the stag is
via the antlers. These structures are used primarily as weapons of offense and
defense, and changes in the state of the antler cause profound changes in the
degree and mode of aggression (Lincoln et al., 1970). Since the annual cycle
of antler growth and shedding is directly controlled by the testosterone level
(Lincoln, 1971), the antler also provides an invaluable external sign of the
level of testosterone secretion. A very low level of testosterone results in
antler casting, which is immediately followed by the growth of new antlers
in velvet , when they are covered by a richly innervated and vascular layer
of skin. Rising levels of testosterone cause this velvet to be sloughed off in a
process known as cleaning, which thus exposes the dead bone or hard
horn of the true antler.
The effects of testosterone on sexual behavior can be assessed by
recording the various components of rutting behavior. Normal rutting behavior

HORMONES

AND BEHAVIOR

IN THE STAG

377

represents a complex sequence of changes lasting over several weeks which

may culminate in successful mating. These changes include wandering away
from the home range to the stags traditional rutting area, actively attempting
to acquire a group of hinds and vigorously defending the area around them
from incursions by other stags. The animals become extremely aggressive
during the rut, even when not in possession of hinds, and show a characteristic stiff-legged approach and lateral threat display toward other stags that is
not seen within the bachelor group (Lincoln, 1972). Rutting also produces a
complete change in the stags activity patterns; much time is now devoted to
herding and inspecting the hinds, showing flehmen, roaring, chasing off rivals,
and scent marking by thrashing the herbage with the antlers, urinating, and
wallowing. Little time is left for feeding, so that the stag rapidly declines in
condition, and rutting activity comes to an end after about 6 weeks. Although
all adult stags show some rutting behavior in the autumn, only those that are
in possession of hinds when they come into estrus will actually copulate. The
commencement of rutting behavior normally precedes the first estrus by
several weeks (Guinness, Lincoln, and Short, 197 1; Lincoln and Guinness,
1973). The rutting stag also develops a strong goat-like odor, and undergoes a
number of physical changes including hypertrophy of the neck musculature,
development of a long, shaggy neck mane, staining of the urethral orifice and
brisket, and darkening of the whole coat as a result of repeated wallowing.
The experiments described here were designed to show the extent to
which testosterone controls social and sexual behavior directly, by a central
action on the brain, and indirectly, by peripheral effects on secondary sexual
characteristics such as the antlers. Changes in social aggressive behavior were
quantitated by recording the position of the experimental animal in the social
hierarchy of its bachelor group. Sexual behavior was assessedby recording the
various components of rutting behavior exhibited by the animals.

MATERIALS

AND METHODS

The Study Population

The study was carried out on a free-ranging population of wild red deer
stags living on the Isle of Rhum (57 ON, 6 OW), Scotland. The island is a
National Nature Reserve, administered by the Nature Conservancy, and its
26,400 acres support a population of about 1200 red deer, whose numbers are
kept in check by an annual selective cull of 1/6th of the population. Work
began during the winters of 1965 and 1966, when two groups of stags
forming natural bachelor communities in the North of the island were
encouraged to take artificial feed (maize, potatoes, deer nuts). By studying the
behavior of the stags at the feeding sites it was possible to work out a social

378

LINCOLN,GUINNESS,AND SHORT

rank order or hierarchy; changes in rank were used as a measure of aggression

within the social group.
At the beginning of the rut in mid-September the bachelor communities
of stags broke up, and the animals began to wander all over the island to their
traditional rutting areas, to which they returned each year. All components of
rutting behavior were used as indices of sexual activity; it was not possible to
study copulatory behavior itself, since matings were rarely seen in the wild.
Experimental Animals
Seven stags from the two bachelor communities were selected for
experimental procedures. Three were castrated (Symmetry, Unilever, and
Manfred), and of these, two were subsequently implanted with testosterone
(Symmetry and Manfred). In addition, four intact stags (Aristotle, Ravel,
Blondin, and Tricky) were also implanted with testosterone.
Experimental Procedures
In order to carry out the experimental procedures the stags were
immobilized by darting them in the rump with a projectile syringe shot from
a crossbow (Short and King, 1964). The immobilizing solution was a mixture
of Etorphine (Reckitt & Sons, Hull) and acetylpromazine maleate (Boots Pure
Drug Co., Nottingham) dissolved in water (Lincoln et aZ., 1970). The animals were aged by making a plasticine impression of the lower molars after
they had been immobilized, and then preparing a plaster of Paris cast of the
impression. The degree of tooth wear was then compared with a set of jaws
from known-age animals. The animals were marked with colored ear tags with
attached nylon streamers, and latterly they were also fitted with a colored and
numbered plastic cattle collar around the neck. One animal was fitted with a
radio transmitter collar (S. L. Markusen, Minnesota, U.S.A.) that functioned
satisfactorily for several weeks.
Castration was performed under Etorphine narcosis. The spermatic cord
was clamped off with an emasculator, and in the case of the animal castrated
just before the rut, the spermatic cord was also ligated with catgut. Two tubes
of intramammary penicillin were squeezed into the empty scrotum before the
animals were released. All the three castrated animals made uneventful
recoveries.
Fused sterile cylindrical implants of 1 g testosterone (Organon) were
placed subcutaneously into the side of the neck while the animals were under
Etorphine narcosis. The skin incision was closed with a mattress suture, and
intramammary penicillin was squeezed into the wound. The manufacturers
claim that these implants release 2.5 mg testosterone/day for 57 weeks, and
that the rate of absorption is linear for about the first 3 months.

HORMONES AND BEHAVIOR IN THE STAG

379

Observational Techniques
Detailed observations on the stags lasted from January 1968 until
December 1971. The study area was visited at least six times each week in
1970 and 1971, and about half as frequently in the previous 2 years. On each
occasion an attempt was made to attract the stags to two feeding sites where
token feed was provided in the form of small piles of maize laid out at the
perimeter of a circle about 20 yd in diameter. In 1968 and 1969 records were

Fig. 1. Relationship between social rank and the frequency of dominance moves
over food piles. Results from stags in hard horn in the two separate bachelor groups in
spring 1968. Each curve represents the mean of at least 10 30-min recording periods.

Fig. 2. Time of year when the antlers were growing in velvet; results for 26 stags
in 1971 related to age. The shaded bar above shows the overah mean period of antler
growth
for the group.

380

LINCOLN, GUINNESS, AND SHORT

Manfred

Symmetry
I
i-

I
I
JFMAMJJA

Velvet
:---PY-Y-~*

Un1lW3
Rut

Months

Fig. 3. Dates of castration of three mature stags in relation to the expected times
of casting, cleaning, and rutting in the normal population.

kept of the number of interactions and the types of threat shown by each
stag toward all others during the competition for food, and a social hierarchy
for each bachelor group was constructed from these data (Lincoln et al.,
1970). It was found that the more dominant stags exhibited the greatest
number of aggressive moves (Fig. l), and the social rank of an animal
reflected its ability to compete with the other members of the group. For this
reason changes in social rank alone were recorded in 1970 and 1971, and
these have been used to illustrate the effects of the experimental procedures
within the bachelor group. In addition to these observations, notes were kept
on the dates of antler casting and cleaning (see Fig. 2) and the dates when
animals showed aspects of rutting behavior. On any occasion when an
experimental stag was not seen for 1 or 2 days a special search was made for
it elsewhere on the island.

RESULTS
I. Effects of Castration
Three mature stags were castrated in January, September, and December
(Fig. 3 and Table 1).
(a)Secondary sexual characteristics. The three stags were in hard horn
at the time of castration, and all of them cast their antlers 18-20 days later,
irrespective of age or the time of year. New antlers immediately began to
grow in velvet, and although their growth was completed after a normal
period of 3-4 months, cleaning did not occur, and they remained permanently in velvet. The shape of the castrates antlers was abnormal in each case,
with two animals showing a reduced number of antler points due to the lack
of branched tops (Fig. 4).
The other secondary sexual characteristics of the stags showed more
gradual changes after castration. The neck mane and thick winter coat were
retained until molting at the normal time in early summer, but then a new
mane failed to develop, and with the growth of the winter coat in the
autumn, the animals acquired a hind-like appearance (Figs. 4 and 5). The two
stags castrated in December and January (Unilever and Symmetry) failed to

Age at
castration
(i-1

11

Animal

Symmetry

Manfred

Unilever

Dec. 4,1969
Hard horn

Sept. 2, 1969
Hard horn

Jan. 22, 1968

Hard horn

Date of
castration and
state of antlers

Cast 19 and 20
days later

Cast 19 and 20
days later

Cast 18 and
19 days later

Short-term
Long-term

Antlers developed
fairly normally and remained in velvet

Antlers developed
with no top branches
and remained in
velvet

Antlers developed
with no top branches
and remained in
velvet

Antlers
Social

Fell in hierarchy at
antler casting and left
the group

Fell in hierarchy at
antler casting and remained very submissive

Sexual

No rutting behavior

No rutting behavior

No rutting behavior although wandered from

normal haunts

Behavior

Fell in hierarchy at
antler casting and remained very submissive

Effect on

Effects of Castration on Antler Growth and Behavior of Red Deer Stags

TABLE 1

382

LINCOLN, GUINNESS AND SHORT

Fig. 4. Symmetry, an 8-year-old stag castrated for 2 years, showing the hind-like
winter coat and short neck mane typical of a castrate. Note that the antlers are in velvet
and lack some of the normal antler points. February 1970.

develop a black-stained area in front of the penis and over the belly and
brisket; they did not produce the rutting odor during the next rutting season,
and they showed none of the swelling of the neck musculature characteristic
of a rutting stag. The animal castrated a fortnight before the rut developed
slight staining and a faint smell during the next few weeks, but these features
soon disappeared, and it was noticeable how the animals neck girth decreased
in the weeks after castration. None of these secondary sexual characteristics
redeveloped during the rut in the next year.
(b) Social aggressive behavior. During the first fortnight after castration,
none of the animals showed any change in social rank within the bachelor group,
or in the type of threats used to enforce dominance (Fig. 6). The first changes in
behavior came when the antlers were cast; the animals immediately reverted to
velvet behavior, using the forefeet when interacting with the other stags,
and although they tried to maintain their rank, they were at a severe
disadvantage compared to the antlered stags and were quickly relegated to
near the bottom of the social hierarchy. The castrates retained a low social
status throughout the period when the rest of the group was in hard horn and

HORMONES AND BEHAVIOR IN THE STAG

383

Fig. 5. Caesar, an 11-year-old stag, showing the coarse winter coat, long shaggy
mane, and hard-horn antlers characteristic of a sexually mature animal. February 1970.

they developed a very submissive behavior, usually remaining at the periphery

of the group. However, when the other stags came into velvet in the spring the
castrates were able to regain a few places in the hierarchy for a short period,
although never returning to the position they had held prior to the operation
(Fig. 7).
(c)Sexual behavior. All three animals had shown normal rutting behavior prior to the experiment, yet even when castration was performed only
2 weeks before the beginning of the rut (Manfred), subsequent sexual behavior
was almost entirely abolished. One of the animals (Symmetry) did wander
away from the home range of the bachelor group during the rutting season,
but this was not true of the other two stags. None of them was seen to show
interest in the hinds at any time. They were never seen to roar, show flehmen,
thrash the herbage with their antlers, or scent mark with urine, although the
September castrate (Manfred) was once observed with peat on his antlers,
suggesting that he might have been thrashing.

384

LINCOLN, GUINNESS AND SHORT

I
1

VELVET
VELVET

;
t

EL&T

XLvFf

-I

Fig. 6. Change in the social rank of Symmetry (a) and Manfred (b) after
castration. The positions within the social hierarchy are shown on the vertical scale. The
curved arrows represent nonlinear, triangular relationships in which a subordinate
individual acquires dominance to one particular animal of higher rank The upper shaded
bars show the period when the experimental animal (2) or the bachelor group (1) had
antlers in velvet.

II. Effects of Testosterone Implantation in Intact Stags

Four mature

stags were implanted

l-2 g of fused testosterone

in Aprii,

June, and December

with

(Fig. 8 and Table 2).

Arl9otle

Tricky

RW@

Blondm
1
J

Velvet

AMJJA

Rut
50

I1
N

13

Months

Fig. 8. Dates of testosterone implantation of four mature stags in relation to the

expected times of casting, cleaning, and rutting in the normal population.

HORMONES AND BEHAVIOR IN THE STAG

385

Fig. 7. The castrate, Symmetry (L), rearing up on his hind legs and attempting to
regain dominance over a normal stag (Sam) which had recently cast. This behavior, in
which the front feet are used as weapons, is typical of an animal in velvet. March 1970.

(a) Secondary sexual characteristics. The two stags implanted in

December while in hard horn (Blondin and Tricky) showed no sudden changes
in their secondary sexual characters. However, they both failed to cast their
antlers at the normal time in the next spring. One of the stags retained the
same set of antlers until the next October, when he disappeared (Blondin).
The other animal was very late in casting (Table 2), and after a short period
of antler growth lasting only 6 weeks the new set of antlers were cleaned in
late August, presumably in response to the animals own testosterone secretion. These antlers had completed less than a quarter of their usual growth,
and were extremely stunted. The antler cycle returned to normal the next
year after casting in April, and a normal pair of antlers developed during the
summer months.
The two stags implanted while in velvet (Aristotle and Ravel) also
showed long-term effects on the antler cycle. Both animals cleaned their
antlers 6-8 weeks after the operation. In the case of Aristotle who was
implanted in April when his antlers were just beginning to grow, this resulted
in severe stunting of the antlers. With Ravel implanted in June when the
antlers were already three-quarters grown, subsequent antler development was
fairly normal. Aristotle cast his antler stumps at the usual time a year later
and redeveloped a normal pair of antlers. However, Ravel, operated on in June,

Ravel

Tricky

Blondin

Antler stumps cast

Mar. 18, 1971b

One antler cast July

10, 1971 and the
other lost Oct. 1971;
next antler stunteda
Cast July 8-l 1, 1970,
next antlers stuntedb
Still not cast when
disappeared Oct.
1969

Cleaned after
43 days,
antlers
stunted
Cleaned after
5 1 days, antlers
normal
No change

No change

June 11,197O
2g
Full velvet

Dec. 3,1969
2g
Hard horn

Dec. 9,196s
lg
Hard horn

Apr. 17, 1970

2g
Early velvet

Long-term

Antlers
Short-term

aAnimal died Spring 1971.

bNext antler cycle normal.

11

Aristotle

Animal

Date of implantation, dose of

Age at
implanta- testosterone, and
tion (yr) state of antlers
Social

No change

Rose in hierarchy
until antlers cast

No change

Rose in hierarchy
after cleaning but
later dropped in rank

Effects on

Effects of Testosterone Implantation on Antler Growth and Behavior of Intact Stags

TABLE 2

Sexual

No rutting until Sept.Oct. 1969

No rutting until Sept.Oct. 1970

No rutting until Sept.Oct. 1970

NO rutting until Sept.Oct. 1970

Behavior

5
0
C
,
z

E
3
5

HORMONES

AND BEHAVIOR

IN THE STAG

387

did not cast in the next spring, presumably because the implant was still
releasing significant amounts of testosterone. One antler was eventually cast in
July, and a new antler immediately began to grow in an abnormal fashion on
the cast side; this was then cleaned in late August after having grown only a
few inches. During the rut this short antler snapped off, and the remaining
old antler was also knocked off during a fight in the rut, leaving the animal
totally without antlers.
Apart from these complex changes in the antlers, we did not observe
any other changes in the secondary sexual characteristics of the four intact
stags. The neck girth, growth of the neck mane, and winter coat were normal,
and no conspicuous rutting odor developed as a result of the implants.
(b) Social aggressive behavior. Of the four intact animals implanted with
testosterone, two showed a conspicuous increase in aggressivenesswithin l-2
months of the operation. The most dramatic change occurred in the stag given
2 g of testosterone in December when in hard horn (Tricky). Within 11 days
of the operation, he fought and defeated a more dominant stag, and over the
next few months he tackled all the animals of higher rank one by one, and
climbed to second place in the group hierarchy (Fig. 9). This aggressive
behavior continued until he cast his antlers in July. The other animal
implanted in December with only 1 g of testosterone showed no increase in
aggressiveness.
Of the two stags implanted when in velvet, one of them (Aristotle)
became obviously more aggressive and gained status within the group. The
other animal was the most dominant stag even before the operation and so it
was difficult to record changes in his behavior.
Besides these immediate behavioral changes, all the animals showed
changes in social rank that were presumably a result of hormone-induced
changes in their antlers. When the animals failed to cast at the normal time in
the spring, they climbed to the top of the social hierarchy as the normal
animals cast. When the normal animals came into hard horn again, the
experimental stags fell back to their usual position. When the experimental
stags eventually cast their antlers after the implants had been absorbed, they
showed the usual drop in social status.
Three of the four stags given testosterone developed grossly stunted
antlers at some stage after the operation, either through the direct effect of
the implant, or as a result of delayed casting. In each case this apparently
made them unable to compete successfully with the fully antlered animals and
SO they fell to close to the bottom of the hierarchy (Fig. 9), and adopted a
very submissive behavior, spending much of their time grazing alone. During
the rutting season these stags with deformed antlers showed the characteristic
aggressive behavior typical of the rut, but they were unable to secure hinds,
and merely wandered about on their own. They were seen to fight with other
rutting stags on several occasions but were invariably defeated.

388

LINCOLN. GUINNESSAND SHORT

:
fb

[VELVET/

VELVET

IvELvq
IVELVET

Fig. 9. Change in the social rank of two intact stags Tricky (a) and Aristotle (b)
after implantation with 2 g testosterone. For explanation of figure see Fig. 4.
was interesting that even a year later, when these animals had
redeveloped normal antlers, their behavior had not always returned to normal.
Two of the stags continued to show rather submissive behavior and were
several positions lower in rank than they had been before implantation; during
the rutting season they also showed a disrupted pattern of behavior and did
not settle down normally with a harem of hinds. These effects OR behavior
were apparent up to 2 years after the time of implantation.
(c) SCXWZZbehavior. None of the four intact stags implanted with
testosterone showed any form of rutting behavior within l-2 months of the
operation. However, they all rutted normally at the usual time, with the
exception that the animals with severely stunted antlers were unable to secure
a harem of hinds for themselves.
It

HORMONES AND BEHAVIOR IN THE STAG

III. Effects of Testosterone Implantation

389

in Castrated Stags

Two adult stags which had been castrated for at least 3 months were
implanted on a total of four occasions with 1-2 g of fused testosterone in
April, June, or December (Fig. 10 and Table 3).
(a) Secondary sexual characteristics. The castrates were all in velvet at
the time of implantation, with fully grown antlers. They cleaned 23-35 days
after the operation, and the antlers were then retained in hard horn for 9-12
months. Casting occurred at various times of the year, and on two occasions
over a week elapsed between the loss of the two antlers. New growth began
immediately, and these antlers once more resembled those of a normal
castra, 0 (V.P above) although they tended to develop more points.
rnges in the other secondary sexual characters were more difficult
T
to folio:.+. 1ALetwo castrates implanted in April and June developed a stag-like
winter coat that autumn, with a fairly conspicuous neck mane. Similar
changes were not noticed after implantation in December, although Manfred
still retained his winter coat and mane that was already present when he was
castrated 3 months previously. Swelling of the neck musculature was apparent
in all the castrates but it was most pronounced in Manfred. This animal also
showed the most conspicuous staining around the urethral orifice, which
developed in all the animals to a very minor extent. The rutting odor did not
develop noticeably after implantation.
(b) Social aggressive behavior. The castrates always showed an obvious increase in agg:i;ssion within l-2 months of testosterone implantation.
The two animals implanted in the spring and summer remained with the
bachelor group, and began to climb in social rank within 12-14 days of the
operation. The normal stags all had antlers in velvet at this time, but the
experimental castrates began to gain dominance even before their own antlers
cleaned. Symmetry, for example, showed his first changes in behavior 12 days
after receiving the implant, when he was involved in a series of boxing
contests with a stag of higher rank that he defeated; he gained a further four
places in rank before he cleaned. Both castrates came into hard horn while the
other stags were still in velvet, and so this resulted in a further rise to near the
top of the hierarchy.
When the two castrates were implanted in December, they both left
their normal haunts 2-3 weeks later, but before cleaning their antlers, having
Symmetry

I
J

Manfred

1 Velvet
,,---,
M
A MJ

Manfred
ymmetry

I
<,

Rut
J

ASOND

Months

Fig. 10. Dates of testosteroneimplantation of two castrated stags in relation to

the expected times of casting, cleaning and rutting in the normal population.

Sept. 2,
1969

Jan. 22,
1968

13

11

Symmetry

Manfred

Manfred

Symmetry

Sept. 2,
1969

Jan. 22,
1968

Animal

Date of
castration

Age at
implantation

Cast Mar. 5,1972

267 days after implant and redeveloped castrate-like
antlers
Cast Oct. 13, i970
3 14 days after implant and redeveloped castrate-like
antlers

Cleaned
after 35
days

Cleaned
after less
than 28
days
Cleaned
after less
than 30
days

June 11,197l
2g
Full velvet

Dec. 3, 1969
2g
Full velvet

Dec. 7, 1968
lg
Full velvet

Cast Dec. 8/22,1969

3661380 days after
implant and redeveloped castrate-like
antlers

Cast Mar. 31/Apr. 1,

1971,349/351
days
after implant and
redeveloped castrate-like antlers

Cleaned
after 23
days

Apr. 15,197O
2g
Full velvet

Long-term

Social

Behavior

Rose in hierarchy
in first 4 months
and later dropped
again

Rose in hierarchy
in first 4 months
and later dropped
again

Rose in hierarchy
in fist 34 months

Rose in hierarchy
in first 3-4 months
and later dropped
again

Effects on

and Behavior of Castrated Stags

Antlers

on Antler Growth

Short-term

Implantation

Date of imolantation, dose of

testosterone and
state of antlers

Effects of Testosterone

TABLE

Rutted Jan.-Feb.
1969

Rutted Jan.-Feb.
1970

Rutted Sept.-Oct.
1971

Slight activity
after l-2 months
rutted Sept.-Oct.
1970

Sexual

HORMONES AND BEHAVIOR IN THE STAG

391

shown no obvious change in behavior in the hard-horn group. They both

cleaned their antlers while away from the group, developed very aggressive
behavior toward the neighboring stags, and they even began rutting (Fig. 11).
Manfred appeared in Glen Harris, many miles from his home range but in his
normal rutting area, and he showed the very aggressive stiff-legged approach
threat, characteristic of a rutting stag, toward some of the local animals. He
was involved in at least two fights, and then was accepted as the most
dominant animal in the glen, and all the other stags avoided his aggressive
approaches. The second castrate (Symmetry) also showed aggressive behavior
while away from the bachelor group, but he was less dominant than Manfred.
On the day when these two castrates subsequently returned to the
bachelor group, in January or February, they both took part in a spectacular
series of aggressive encounters; Manfred was involved in 10 fights and he
convincingly won five of them. The initial encounters were with the most
subordinate animals, and step by step the castrates regained status and

Fig. 11. Changes in the social rank of two castratesSymmetry (a) and Manfred (b)
after implantation with testosterone. For explanation of figure see Fig. 6.

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returned to a position similar to that held before castration (Fig. 11). When
the other stags in the group cast their antlers in the spring, both castrates
climbed still further, Manfred becoming the most dominant stag in the group.
In all of the four experiments the castrates maintained a high social
status for several months and continued to exert their dominance (Fig. 12).
But then they began to fall in rank, even though they still retained their
hard-horn antlers (Fig. 11). This was particularly noticeable at the time of the
rut, when the other animals in the group were especially aggressive. When the
castrates antlers were finally cast, they usually dropped further in rank and
adopted the submissive behavior typical of a castrate in velvet living among
stags in hard horn.
(c)Sexual behavior. Both the castrates that were given testosterone in
December developed rutting behavior in January or February. The older
animal (Manfred) wandered away from the bachelor group after 2-3 weeks,
and migrated to Glen Harris about 5 miles south, to almost the same spot
where he had rutted before he was castrated. Here he was seen to roar and
wallow, and pursue hinds; for a time he even herded up a harem and pushed
away the local stags. The younger castrate implanted with only 1 g of
testosterone showed all these aspects of rutting but in a less intense manner.
After frequently pursuing the hinds to begin with, both the castrates gradually
lost interest, and spent much of their time resting or grazing alone, only
joining the hinds occasionally. Symmetry, who rutted quite close to the

Fig. 12. The castrate, Symmetry (R), in hard horn after receiving an implant of
testosterone 8 months earlier, using his antlers effectively against an older and larger stag
(Aristotle) stili in vehet. August 1969.

HORMONESANDBEHAVIORINTHESTAG

393

bachelor group, actually returned to the group on odd occasions while still
showing some rutting behavior. Both animals finally rejoined the other stags
after a period of nearly 2 months, and they showed no further aspects of
sexual behavior.
In contrast to the conspicuous effects on sexual behavior of testosterone
implantation in December, when implants were subsequently given to these
same two animals in April or June there was little immediate effect on sexual
behavior. The older animal implanted in June showed no sexual behavior
whatsoever, while the younger animal operated on in April showed only some
slight interest in hinds that grazed nearby on occasions. However, 3-5 months
later, in the autumn and at the time of the normal rut, both the castrates
developed rutting behavior. They moved away from the bachelor group in
mid-September when the other stags were also beginning to rut, and migrated
to their respective rutting areas, where they stayed until October-December.
The animal implanted in April (Symmetry) was seen with a small harem on
several occasions and he roared, wallowed, and chased hinds in the manner
characteristic of a rutting stag. Manfred was twice seen in his rutting haunts,
and his identification collar was found lying in Glen Harris close to his usual
rutting area, giving further proof of his movements.

DISCUSSION
Testosterone seems to play an important part in regulating both the
social and sexual behavior of the red deer stag, although the ways in which it
controls these two types of behavior may be different.
We found that castration of adult stags abolished almost all aspects of
rutting behavior, and this was true even when the operation was performed
only 2 weeks before the normal rutting season. When castrates were implanted
with testosterone in December, they began to rut a few weeks later, at a time
of year when the normal stags had finished rutting and the hinds were all
pregnant. Yet, when the same castrates were implanted with testosterone in
the spring or summer, they failed to show any sexual response until the next
autumn, at the time of the normal rut.
Our results, therefore, suggest that testosterone must play a permissive
role in the control of rutting behavior, and that overt sexual activity can be
induced by the hormone only at certain times of the year.
The seasonal pattern of sexual responsiveness shown by the castrates in
our study could result from the influence of previous sexual experience, or it
could be due to seasonal changes in the sensitivity of the brain to testosterone. The fact that the castrates returned to their old rutting haunts after
treatment with testosterone clearly illustrates one influence of experience on
behavior. Past experience of seasonal changes in the environment such as the

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AND SHORT

length of day or state of the vegetation could dictate the period when the
castrates showed rutting activity. In addition, an olfactory cue from the hinds
might be important (Lincoln and Guinness, 1973); since hinds on Rhum can
come into estrus and conceive from October to March (Guinness et al, 1971)
it may be significant that the implanted castrates in the present study showed
rutting activity only during this period. However, normal stags are capable of
showing rutting behavior in complete isolation from hinds, demonstrating that
female cues are not essential.
The stags on Rhum normally begin to rut in mid-September whereas the
hinds first come into estrus in early October (Guinness et aZ., 1971; Lincoln
and Guinness, 1973). Although we originally suggested that the rut was
initiated in the stags by the rapidly rising level of testosterone (Lincoln et al.,
1970; Lincoln, 1971) it now seems more probable that other factors such as
photoperiod, odor from the hinds, and past sexual experience represent
proximate stimuli, and rutting will ensue provided that testosterone is present.
Neither the commencement of rutting activity nor its duration is
necessarily influenced by quantitative changes in the levels of testosterone. In
the present study the castrated stags implanted with testosterone tended to
rut for 4-8 weeks in much the same way as normal animals, yet they clearly
did not experience the rise and fall in testosterone secretion that usually
occurs during the rut. A rutting stag is very active and spends virtually no time
feeding; this leads to a marked depletion of fat reserves, loss in body weight
(Mitchell, 1971) and fatty infiltration of the liver. Thus, sheer physical
exhaustion may set a limit to the duration of rutting behavior.
The intact stags were not induced to rut by testosterone treatment in
December, April, or June, and experiments with two other seasonal breeders,
the roebuck (Bramley, 1970) and the Uganda kob (Leuthold, 1966) have also
failed to induce sexual activity out .of season. This could indicate that they
become refractory to hormonal stimulation, or perhaps previous experience
has conditioned them to show rutting behavior only at a certain time of the
year. Unlike a testosterone injection, the presence of an estrous hind can
induce red deer stags to rut in the winter, spring, or even summer (Millais,
1913; Marshall, 1937; Littlejohn, 1967; Lincoln et aZ., 1970).
In order to quantitate the effects of testosterone on social aggression,
we have used social rank as an index. This has certain disadvantages, since
social rank is also influenced by the size and state of the antlers. For example,
amputation of the antlers of intact stags usually produces a marked fall in
social rank (Lincoln et al., 1970; Lincoln, 1972) and can also seriously
interfere with rutting behavior (Lincoln, 1972). Consequently, if antler
development is inhibited by the administration of testosterone at an inappropriate time of the year, as in the case of the stag Aristotle, then the hormone
may actually produce a fall in social rank, and interfere with sexual behavior.
Also, an animal with antlers in velvet is always at a serious social disadvantage

HORMONES AND BEHAVIOR IN THE STAG

395

when compared with an animal in hard horn, since the velvet antlers cannot
be used as weapons. These points must be borne in mind when trying to
interpret the results; direct effects of testosterone on behavior can be inferred
only when the administration of the hormone produces a change in social
rank without any alteration in the antlers. Since antler growth, cleaning, and
casting are all under the control of testosterone (Lincoln et aZ., 1970; Lincoln,
197 1j, the hormone will inevitably have a number of indirect effects on social rank.
There can be little doubt from our results that testosterone does have a
direct inductive effect on social aggression. This can be demonstrated even in
the intact animal, and furthermore it appears to be dose dependent. As the
effects of the implant in the castrate, Symmetry, began to wear off, so he fell
in social rank, even though there was no change in the state of his antlers. In
addition, it appears that the hormone has a direct effect on the mode of
aggression of the stags; animals with a high level of testosterone are apparently
obliged to use their antlers in aggressive encounters, and are unable to initiate
threats by using their fore feet, as they do when they are in velvet, or when
they are in hard horn with low testosterone levels.
The fact that intact and castrated stags can respond socially to the
effects of testosterone while showing no change in their sexual behavior
emphasizes the essential difference between these two behavioral patterns.
Fears have sometimes been expressed that all social aggression is merely a
reflection of underlying sexual behavior (Hill, 1970) but this cannot be true
of the red deer stag. By studying a seasonal breeder, whose sexual activity is
confined to certain times of the year, it is possible to dissociate these two
influences. But it is true that even in red deer there are a number of possible
interactions between social and sexual behavior; stags such as Tricky and
Aristotle, who were low in social rank at the beginning of the rut because of
stunted antler growth, also showed greatly impaired sexual performance. In
the natural state, animals that are high in social rank are usually the most
successful sexually, even though they may never encounter their bachelor
companions during the rut because of the fragmentation of and widespread
emigation from the bachelor group. It is difficult to say to what extent social
and sexual behavior are causally related, and to what extent both are
influenced by the common variables of body size, age, antler size, experience,
and hormone level.
ACKNOWLEDGMENTS
This work was made possible by generous financial support from the Natural
Environment Research Council, the Royal Society International Biological Programme
and the Ford Foundation. The Nature Conservancy generously placed all their facilities
on Rhum at our disposal, and our particular thanks go to the wardens, Mr. P. Wormell
and Mr. G. MacNaughton. The testosterone implants used in the study were generously
donated by Dr. W. J. Tindall of Organon, and we thank Mrs. J. Kelly and Miss J. Millar
for secretarial assistance.

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