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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 from’sexual 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

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’ O’N. so that the stag rapidly declines in condition. These changes include wandering away from the home range to the stag’s traditional rutting area. showing flehmen. by peripheral effects on secondary sexual characteristics such as the antlers. The animals become extremely aggressive during the rut. and indirectly. Sexual behavior was assessedby recording the various components of rutting behavior exhibited by the animals. The rutting stag also develops a strong goat-like odor. when two groups of stags forming natural bachelor communities in the North of the island were encouraged to take artificial feed (maize. Lincoln and Guinness. even when not in possession of hinds. whose numbers are kept in check by an annual selective cull of 1/6th of the population. and undergoes a number of physical changes including hypertrophy of the neck musculature. Work began during the winters of 1965 and 1966. only those that are in possession of hinds when they come into estrus will actually copulate. and darkening of the whole coat as a result of repeated wallowing. actively attempting to acquire a group of hinds and vigorously defending the area around them from incursions by other stags. and its 26. 1972). The commencement of rutting behavior normally precedes the first estrus by several weeks (Guinness. and show a characteristic stiff-legged approach and lateral threat display toward other stags that is not seen within the bachelor group (Lincoln.400 acres support a population of about 1200 red deer. Although all adult stags show some rutting behavior in the autumn. The experiments described here were designed to show the extent to which testosterone controls social and sexual behavior directly. The island is a National Nature Reserve. 197 1. Lincoln. roaring. and wallowing. and Short. By studying the behavior of the stags at the feeding sites it was possible to work out a social . shaggy neck mane. Changes in social aggressive behavior were quantitated by recording the position of the experimental animal in the social hierarchy of its bachelor group. Scotland. potatoes. Little time is left for feeding. 6” O’W). by a central action on the brain. Rutting also produces a complete change in the stag’s activity patterns. urinating. much time is now devoted to herding and inspecting the hinds. and rutting activity comes to an end after about 6 weeks. 1973). development of a long. administered by the Nature Conservancy. deer nuts). chasing off rivals. and scent marking by thrashing the herbage with the antlers.HORMONES AND BEHAVIOR IN THE STAG 377 represents a complex sequence of changes lasting over several weeks which may culminate in successful mating. staining of the urethral orifice and brisket.

The spermatic cord was clamped off with an emasculator. The manufacturers claim that these implants release 2. U. Experimental Animals Seven stags from the two bachelor communities were selected for experimental procedures. Markusen. 1970). .378 LINCOLN. The degree of tooth wear was then compared with a set of jaws from known-age animals. and of these. to which they returned each year. Unilever. Three were castrated (Symmetry.5 mg testosterone/day for 57 weeks. All components of rutting behavior were used as indices of sexual activity. In addition. it was not possible to study copulatory behavior itself. changes in rank were used as a measure of aggression within the social group. Two tubes of intramammary penicillin were squeezed into the empty scrotum before the animals were released..GUINNESS. The immobilizing solution was a mixture of Etorphine (Reckitt & Sons. Ravel. and intramammary penicillin was squeezed into the wound. Nottingham) dissolved in water (Lincoln et aZ.) that functioned satisfactorily for several weeks. and latterly they were also fitted with a colored and numbered plastic cattle collar around the neck.S. The animals were aged by making a plasticine impression of the lower molars after they had been immobilized. 1964). One animal was fitted with a radio transmitter collar (S. since matings were rarely seen in the wild. 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. four intact stags (Aristotle. two were subsequently implanted with testosterone (Symmetry and Manfred). and Manfred). and then preparing a plaster of Paris cast of the impression. The skin incision was closed with a mattress suture. and that the rate of absorption is linear for about the first 3 months. Blondin. At the beginning of the rut in mid-September the bachelor communities of stags broke up. and in the case of the animal castrated just before the rut. and the animals began to wander all over the island to their traditional rutting areas. Hull) and acetylpromazine maleate (Boots Pure Drug Co. L.. and Tricky) were also implanted with testosterone. Minnesota. 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.A. The animals were marked with colored ear tags with attached nylon streamers. Castration was performed under Etorphine narcosis. the spermatic cord was also ligated with catgut. All the three castrated animals made uneventful recoveries.AND SHORT rank order or hierarchy.

1. Fig. 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. Time of year when the antlers were growing in velvet. results for 26 stags in 1971 related to age. Each curve represents the mean of at least 10 30-min recording periods. In 1968 and 1969 records were Fig. 2. 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. . The shaded bar above shows the overah mean period of antler growth for the group. Relationship between social rank and the frequency of dominance moves over food piles.HORMONES AND BEHAVIOR IN THE STAG 379 Observational Techniques Detailed observations on the stags lasted from January 1968 until December 1971. Results from stags in hard horn in the two separate bachelor groups in spring 1968.

(a)Secondary sexual characteristics. and the social rank of an animal reflected its ability to compete with the other members of the group. 1970). l). and a social hierarchy for each bachelor group was constructed from these data (Lincoln et al. irrespective of age or the time of year. AND SHORT Manfred Symmetry I i- I I JFMAMJJA Velvet :“---PY-Y-~“* 1 Un1lW3 Rut 1 I Months Fig. with two animals showing a reduced number of antler points due to the lack of branched tops (Fig. and December (Fig.. 4). cleaning. notes were kept on the dates of antler casting and cleaning (see Fig. and all of them cast their antlers 18-20 days later. kept of the number of interactions and the types of threat shown by each stag toward all others during the competition for food. and rutting in the normal population. 2) and the dates when animals showed aspects of rutting behavior. For this reason changes in social rank alone were recorded in 1970 and 1971. and with the growth of the winter coat in the autumn. RESULTS I. The shape of the castrates’ antlers was abnormal in each case. but then a new mane failed to develop. New antlers immediately began to grow in velvet. 4 and 5). and these have been used to illustrate the effects of the experimental procedures within the bachelor group. GUINNESS. September.380 LINCOLN. The other secondary sexual characteristics of the stags showed more gradual changes after castration. The two stags castrated in December and January (Unilever and Symmetry) failed to . 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. 3. The three stags were in hard horn at the time of castration. “cleaning” did not occur. In addition to these observations. and although their growth was completed after a normal period of 3-4 months. and they remained permanently in velvet. Dates of castration of three mature stags in relation to the expected times of casting. 3 and Table 1). The neck mane and thick winter coat were retained until molting at the normal time in early summer. the animals acquired a hind-like appearance (Figs. It was found that the more dominant stags exhibited the greatest number of aggressive moves (Fig. Effects of Castration Three mature stags were castrated in January.

Age at castration (i-1 5 11 7 Animal Symmetry Manfred Unilever Dec. 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 .1969 Hard horn Sept. 4. 2. 1969 Hard horn Jan. 22.

February 1970. they were at a severe disadvantage compared to the antlered stags and were quickly relegated to near the bottom of the social hierarchy. and they showed none of the swelling of the neck musculature characteristic of a rutting stag. none of the animals showed any change in social rank within the bachelor group. and it was noticeable how the animal’s neck girth decreased in the weeks after castration. The first changes in behavior came when the antlers were cast. an 8-year-old stag castrated for 2 years. showing the hind-like winter coat and short neck mane typical of a castrate. 4. the animals immediately reverted to “velvet” behavior. they did not produce the rutting odor during the next rutting season. using the forefeet when interacting with the other stags. During the first fortnight after castration. (b) Social aggressive behavior. Symmetry. but these features soon disappeared. Note that the antlers are in velvet and lack some of the normal antler points. The castrates retained a low social status throughout the period when the rest of the group was in hard horn and . or in the type of threats used to enforce dominance (Fig. The animal castrated a fortnight before the rut developed slight staining and a faint smell during the next few weeks. None of these secondary sexual characteristics redeveloped during the rut in the next year. 6). develop a black-stained area in front of the penis and over the belly and brisket.382 LINCOLN. and although they tried to maintain their rank. GUINNESS AND SHORT Fig.

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. suggesting that he might have been thrashing. showing the coarse winter coat. or scent mark with urine. and hard-horn antlers characteristic of a sexually mature animal. usually remaining at the periphery of the group. an 11-year-old stag. Caesar. they developed a very submissive behavior.HORMONES AND BEHAVIOR IN THE STAG 383 Fig. yet even when castration was performed only 2 weeks before the beginning of the rut (Manfred). long shaggy mane. . although never returning to the position they had held prior to the operation (Fig. thrash the herbage with their antlers. subsequent sexual behavior was almost entirely abolished. but this was not true of the other two stags. although the September castrate (Manfred) was once observed with peat on his antlers. All three animals had shown normal rutting behavior prior to the experiment. February 1970. 5. One of the animals (Symmetry) did wander away from the home range of the bachelor group during the rutting season. 7). None of them was seen to show interest in the hinds at any time. (c)Sexual behavior. They were never seen to roar. show flehmen. However.

Effects of Testosterone Implantation in Intact Stags Four mature stags were implanted l-2 g of fused testosterone in Aprii. t _ I EL&T ] XLvFf 1 -I Fig. 6. Arl9otle Tricky RW@ Blondm 1 J F M Velvet 1 A’M’J’J’A Rut 5‘0 I1 N 13 Months Fig. 8 and Table 2). and December with (Fig. GUINNESS AND SHORT I 1 VELVET VELVET . . cleaning. and rutting in the normal population. 8. Dates of testosterone implantation of four mature stags in relation to the expected times of casting.384 LINCOLN. The positions within the social hierarchy are shown on the vertical scale. June. II. 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. The curved arrows represent nonlinear. Change in the social rank of Symmetry (a) and Manfred (b) after castration.

7. One of the stags retained the same set of antlers until the next October. (a) Secondary sexual characteristics. March 1970. subsequent antler development was fairly normal. The two stags implanted in December while in hard horn (Blondin and Tricky) showed no sudden changes in their secondary sexual characters. when he disappeared (Blondin). With Ravel implanted in June when the antlers were already three-quarters grown. 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. Symmetry (L).HORMONES AND BEHAVIOR IN THE STAG 385 Fig. and were extremely stunted. The castrate. Aristotle cast his antler stumps at the usual time a year later and redeveloped a normal pair of antlers. However. rearing up on his hind legs and attempting to regain dominance over a normal stag (Sam) which had recently cast. Both animals cleaned their antlers 6-8 weeks after the operation. The other animal was very late in casting (Table 2). in which the front feet are used as weapons. presumably in response to the animal’s own testosterone secretion. they both failed to cast their antlers at the normal time in the next spring. operated on in June. These antlers had completed less than a quarter of their usual growth. However. and after a short period of antler growth lasting only 6 weeks the new set of antlers were “cleaned” in late August. . This behavior. this resulted in severe stunting of the antlers. The antler cycle returned to normal the next year after casting in April. is typical of an animal in velvet. In the case of Aristotle who was implanted in April when his antlers were just beginning to grow. Ravel.

3. dose of Age at implanta. bNext antler cycle normal.Oct. 9.8 6 5 Ravel Tricky Blondin Antler stumps cast Mar.1969 2g Hard horn Dec. 1969 No rutting until Sept. 17. 1970 Behavior z E 5 0 C •. 11 Aristotle Animal Date of implantation.197O 2g Full velvet Dec.Oct.Oct. 1970. antlers stunted Cleaned after 5 1 days. next antlers stuntedb Still not cast when disappeared Oct. 1970 2g Early velvet Long-term Antlers Short-term aAnimal died Spring 1971. 18. 1970 NO rutting until Sept. 1971. 1969 Cleaned after 43 days.testosterone. 1970 No rutting until Sept. antlers normal No change No change June 11. 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. next antler stunteda Cast July 8-l 1. 1971b One antler cast July 10.Oct. “z E 3 5 .196s lg Hard horn Apr. 1971 and the other lost Oct.

HORMONES AND BEHAVIOR IN THE STAG 387 did not cast in the next spring. and a new antler immediately began to grow in an abnormal fashion on the cast side. During the rut this short antler snapped off. and merely wandered about on their own. Besides these immediate behavioral changes. The other animal was the most dominant stag even before the operation and so it was difficult to record changes in his behavior. When the normal animals came into hard horn again. The neck girth. and climbed to second place in the group hierarchy (Fig. all the animals showed changes in social rank that were presumably a result of hormone-induced changes in their antlers. one of them (Aristotle) became obviously more aggressive and gained status within the group. and no conspicuous rutting odor developed as a result of the implants. When the experimental stags eventually cast their antlers after the implants had been absorbed. This aggressive behavior continued until he cast his antlers in July. they showed the usual drop in social status. Within 11 days of the operation. and winter coat were normal. but they were unable to secure hinds. When the animals failed to cast at the normal time in the spring. two showed a conspicuous increase in aggressivenesswithin l-2 months of the operation. They were seen to fight with other rutting stags on several occasions but were invariably defeated. growth of the neck mane. and adopted a very submissive behavior. 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. presumably because the implant was still releasing significant amounts of testosterone. he fought and defeated a more dominant stag. Of the four intact animals implanted with testosterone. (b) Social aggressive behavior. we did not observe any other changes in the secondary sexual characteristics of the four intact stags. leaving the animal totally without antlers. the experimental stags fell back to their usual position. they climbed to the top of the social hierarchy as the normal animals cast. and the remaining “old” antler was also knocked off during a fight in the rut. or as a result of delayed casting. Three of the four stags given testosterone developed grossly stunted antlers at some stage after the operation. and over the next few months he tackled all the animals of higher rank one by one. One antler was eventually cast in July. 9). Apart from these complex changes in the antlers. Of the two stags implanted when in velvet. 9). The most dramatic change occurred in the stag given 2 g of testosterone in December when in hard horn (Tricky). this was then cleaned in late August after having grown only a few inches. spending much of their time grazing alone. The other animal implanted in December with only 1 g of testosterone showed no increase in aggressiveness. either through the direct effect of the implant. During the rutting season these stags with deformed antlers showed the characteristic aggressive behavior typical of the rut. .

during the rutting season they also showed a disrupted pattern of behavior and did not settle down normally with a harem of hinds. It . when these animals had redeveloped normal antlers. Two of the stags continued to show rather submissive behavior and were several positions lower in rank than they had been before implantation. 4. was interesting that even a year later. with the exception that the animals with severely stunted antlers were unable to secure a harem of hinds for themselves. GUINNESSAND SHORT : fb ’I I : 2 [VELVET/ VELVET I IvELvq IVELVET j Fig. their behavior had not always returned to normal. Change in the social rank of two intact stags Tricky (a) and Aristotle (b) after implantation with 2 g testosterone. 9. (c) SCXWZZbehavior. However. None of the four intact stags implanted with testosterone showed any form of rutting behavior within l-2 months of the operation. they all rutted normally at the usual time.388 LINCOLN. These effects OR behavior were apparent up to 2 years after the time of implantation. For explanation of figure see Fig.

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

5. 3. 8/22.-Oct. 1968 7 Animal Date of castration Age at implantation Cast Mar. 1969 Jan. 1968 13 11 5 Symmetry Manfred Manfred Symmetry Sept.197l 2g Full velvet Dec.-Oct. 2. 13.-Feb.1969 3661380 days after implant and redeveloped castrate-like antlers Cast Mar.-Feb.1972 267 days after implant and redeveloped castrate-like antlers Cast Oct. dose of testosterone and state of antlers Effects of Testosterone TABLE Rutted Jan. 2. 15. 1969 2g Full velvet Dec. 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. 22. 1971 Slight activity after l-2 months rutted Sept. 7. 31/Apr.Sept. 1970 Sexual . 1968 lg Full velvet Cast Dec. 22.349/351 days after implant and redeveloped castrate-like antlers Cleaned after 23 days Apr. 1. 1969 Jan. 1970 Rutted Sept.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 3 Date of imolantation. 1971. 1969 Rutted Jan.

6. they both took part in a spectacular series of aggressive encounters. Changes in the social rank of two castratesSymmetry (a) and Manfred (b) after implantation with testosterone. and all the other stags avoided his aggressive approaches. but he was less dominant than Manfred. The second castrate (Symmetry) also showed aggressive behavior while away from the bachelor group.HORMONES AND BEHAVIOR IN THE STAG 391 shown no obvious change in behavior in the hard-horn group. and he showed the very aggressive stiff-legged approach threat. developed very aggressive behavior toward the neighboring stags. 11). On the day when these two castrates subsequently returned to the bachelor group. Manfred appeared in Glen Harris. They both cleaned their antlers while away from the group. and then was accepted as the most dominant animal in the glen. and step by step the castrates regained status and Fig. The initial encounters were with the most subordinate animals. 11. Manfred was involved in 10 fights and he convincingly won five of them. in January or February. For explanation of figure see Fig. characteristic of a rutting stag. many miles from his home range but in his normal rutting area. and they even began rutting (Fig. toward some of the local animals. He was involved in at least two fights. .

when the other animals in the group were especially aggressive. both the castrates gradually lost interest. Symmetry (R). 12. After frequently pursuing the hinds to begin with. who rutted quite close to the Fig. they usually dropped further in rank and adopted the submissive behavior typical of a castrate in velvet living among stags in hard horn. and migrated to Glen Harris about 5 miles south. 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. Here he was seen to roar and wallow. 12). When the castrates’ antlers were finally cast. and spent much of their time resting or grazing alone. . and pursue hinds. In all of the four experiments the castrates maintained a high social status for several months and continued to exert their dominance (Fig. The castrate. Symmetry. both castrates climbed still further. August 1969. to almost the same spot where he had rutted before he was castrated. for a time he even herded up a harem and pushed away the local stags. only joining the hinds occasionally. GUINNESS AND SHORT returned to a position similar to that held before castration (Fig. The younger castrate implanted with only 1 g of testosterone showed all these aspects of rutting but in a less intense manner. (c)Sexual behavior. in hard horn after receiving an implant of testosterone 8 months earlier. But then they began to fall in rank. using his antlers effectively against an older and larger stag (Aristotle) stili in vehet. 11).392 LINCOLN. even though they still retained their hard-horn antlers (Fig. This was particularly noticeable at the time of the rut. 11). Manfred becoming the most dominant stag in the group. When the other stags in the group cast their antlers in the spring.

or it could be due to seasonal changes in the sensitivity of the brain to testosterone. they began to rut a few weeks later. They moved away from the bachelor group in mid-September when the other stags were also beginning to rut. Yet. The animal implanted in April (Symmetry) was seen with a small harem on several occasions and he roared. therefore. and migrated to their respective rutting areas. DISCUSSION Testosterone seems to play an important part in regulating both the social and sexual behavior of the red deer stag. The seasonal pattern of sexual responsiveness shown by the castrates in our study could result from the influence of previous sexual experience. giving further proof of his movements. at the time of the normal rut. Manfred was twice seen in his rutting haunts. at a time of year when the normal stags had finished rutting and the hinds were all pregnant. and chased hinds in the manner characteristic of a rutting stag. where they stayed until October-December. and they showed no further aspects of sexual behavior. and this was true even when the operation was performed only 2 weeks before the normal rutting season. actually returned to the group on odd occasions while still showing some rutting behavior. and that overt sexual activity can be induced by the hormone only at certain times of the year. Our results. and his identification collar was found lying in Glen Harris close to his usual rutting area. The older animal implanted in June showed no sexual behavior whatsoever. However. wallowed. 3-5 months later. Past experience of seasonal changes in the environment such as the . in the autumn and at the time of the normal rut. they failed to show any sexual response until the next autumn. The fact that the castrates returned to their old rutting haunts after treatment with testosterone clearly illustrates one influence of experience on behavior. We found that castration of adult stags abolished almost all aspects of rutting behavior. suggest that testosterone must play a permissive role in the control of rutting behavior. when implants were subsequently given to these same two animals in April or June there was little immediate effect on sexual behavior.HORMONESANDBEHAVIORINTHESTAG 393 bachelor group. In contrast to the conspicuous effects on sexual behavior of testosterone implantation in December. while the younger animal operated on in April showed only some slight interest in hinds that grazed nearby on occasions. both the castrates developed rutting behavior. although the ways in which it controls these two types of behavior may be different. Both animals finally rejoined the other stags after a period of nearly 2 months. When castrates were implanted with testosterone in December. when the same castrates were implanted with testosterone in the spring or summer.

since hinds on Rhum can come into estrus and conceive from October to March (Guinness et al. amputation of the antlers of intact stags usually produces a marked fall in social rank (Lincoln et al. This has certain disadvantages. For example. the roebuck (Bramley. an olfactory cue from the hinds might be important (Lincoln and Guinness. Littlejohn. 1973). 1971. the presence of an estrous hind can induce red deer stags to rut in the winter. In addition..394 LINCOLN. Unlike a testosterone injection. Lincoln. Thus. 1913.. 1970). April. 1972). or June. demonstrating that female cues are not essential. 1971) it now seems more probable that other factors such as photoperiod. Also. The intact stags were not induced to rut by testosterone treatment in December. However. and rutting will ensue provided that testosterone is present. and past sexual experience represent proximate stimuli. then the hormone may actually produce a fall in social rank. Consequently. or even summer (Millais. 1967. yet they clearly did not experience the rise and fall in testosterone secretion that usually occurs during the rut. we have used social rank as an index. Marshall. an animal with antlers in velvet is always at a serious social disadvantage . this leads to a marked depletion of fat reserves. 1973). Lincoln et aZ.. sheer physical exhaustion may set a limit to the duration of rutting behavior. A rutting stag is very active and spends virtually no time feeding. or perhaps previous experience has conditioned them to show rutting behavior only at a certain time of the year. Neither the commencement of rutting activity nor its duration is necessarily influenced by quantitative changes in the levels of testosterone. 1937. 1971) and fatty infiltration of the liver. normal stags are capable of showing rutting behavior in complete isolation from hinds. as in the case of the stag Aristotle. This could indicate that they become refractory to hormonal stimulation. 1970. Lincoln and Guinness. since social rank is also influenced by the size and state of the antlers. if antler development is inhibited by the administration of testosterone at an inappropriate time of the year. and interfere with sexual behavior. 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. and experiments with two other seasonal breeders. 1971) it may be significant that the implanted castrates in the present study showed rutting activity only during this period. 1972) and can also seriously interfere with rutting behavior (Lincoln.. loss in body weight (Mitchell.of season. The stags on Rhum normally begin to rut in mid-September whereas the hinds first come into estrus in early October (Guinness et aZ. 1970) and the Uganda kob (Leuthold. GUINNESS. Although we originally suggested that the rut was initiated in the stags by the rapidly rising level of testosterone (Lincoln et al. Lincoln. AND SHORT length of day or state of the vegetation could dictate the period when the castrates showed rutting activity. odor from the hinds. 1970. In order to quantitate the effects of testosterone on social aggression. spring. 1966) have also failed to induce sexual activity out .

Kelly and Miss J. This can be demonstrated even in the intact animal. the Royal Society International Biological Programme and the Ford Foundation. In the natural state. and furthermore it appears to be dose dependent. and hormone level. animals with a high level of testosterone are apparently obliged to use their antlers in aggressive encounters. even though they may never encounter their bachelor companions during the rut because of the fragmentation of and widespread emigation from the bachelor group. 1970) but this cannot be true of the red deer stag. ACKNOWLEDGMENTS This work was made possible by generous financial support from the Natural Environment Research Council. 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. and to what extent both are influenced by the common variables of body size. G. Lincoln. 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. MacNaughton.. and casting are all under the control of testosterone (Lincoln et aZ. 1970. It is difficult to say to what extent social and sexual behavior are causally related. the hormone will inevitably have a number of indirect effects on social rank. experience. As the effects of the implant in the castrate. also showed greatly impaired sexual performance. and are unable to initiate threats by using their fore feet. since the velvet antlers cannot be used as weapons. Mr. Millar for secretarial assistance. and we thank Mrs. There can be little doubt from our results that testosterone does have a direct inductive effect on social aggression. W. Tindall of Organon. P. J. began to wear off. stags such as Tricky and Aristotle. it appears that the hormone has a direct effect on the mode of aggression of the stags. By studying a seasonal breeder. Fears have sometimes been expressed that all social aggression is merely a reflection of underlying sexual behavior (Hill. Symmetry. But it is true that even in red deer there are a number of possible interactions between social and sexual behavior. age. Since antler growth. who were low in social rank at the beginning of the rut because of stunted antler growth.HORMONES AND BEHAVIOR IN THE STAG 395 when compared with an animal in hard horn. These points must be borne in mind when trying to interpret the results. and our particular thanks go to the wardens. In addition. 197 1j. it is possible to dissociate these two influences. J. cleaning. . so he fell in social rank. whose sexual activity is confined to certain times of the year. even though there was no change in the state of his antlers. antler size. animals that are high in social rank are usually the most successful sexually. Wormell and Mr. The Nature Conservancy generously placed all their facilities on Rhum at our disposal. The testosterone implants used in the study were generously donated by Dr. or when they are in hard horn with low testosterone levels. as they do when they are in velvet.

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