Book - Sex and internal secretions (1961) 20

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Young WC. Sex and internal secretions. (1961) 3rd Eda. Williams and Wilkins. Baltimore.
Section A Biologic Basis of Sex Cytologic and Genetic Basis of Sex | Role of Hormones in the Differentiation of Sex
Section B The Hypophysis and the Gonadotrophic Hormones in Relation to Reproduction Morphology of the Hypophysis Related to Its Function | Physiology of the Anterior Hypophysis in Relation to Reproduction
The Mammalian Testis | The Accessory Reproductive Glands of Mammals | The Mammalian Ovary | The Mammalian Female Reproductive Cycle and Its Controlling Mechanisms | Action of Estrogen and Progesterone on the Reproductive Tract of Lower Primates | The Mammary Gland and Lactation | Some Problems of the Metabolism and Mechanism of Action of Steroid Sex Hormones | Nutritional Effects on Endocrine Secretions
Section D Biology of Sperm and Ova, Fertilization, Implantation, the Placenta, and Pregnancy Biology of Spermatozoa | Biology of Eggs and Implantation | Histochemistry and Electron Microscopy of the Placenta | Gestation
Section E Physiology of Reproduction in Submammalian Vertebrates Endocrinology of Reproduction in Cold-blooded Vertebrates | Endocrinology of Reproduction in Birds
Section F Hormonal Regulation of Reproductive Behavior The Hormones and Mating Behavior | Gonadal Hormones and Social Behavior in Infrahuman Vertebrates | Gonadal Hormones and Parental Behavior in Birds and Infrahuman Mammals | Sex Hormones and Other Variables in Human Eroticism | The Ontogenesis of Sexual Behavior in Man | Cultural Determinants of Sexual Behavior
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Section F Hormonal Regulation of Reproductive Behavior

Gonadal Hormones and Social Behavior in Infrahuman Vertebrates

A. M. Guhl, Ph.D.

Professor Of Zoology, Kansas State University, Manhattan, Kansas


I. Introduction

Agonistic behavior is especially important

Most investigations of the influence of during the etstablishment of any degree of gonadal hormones on behavior have been intraspecific organization. Because it is so focused on reproductive behavior, probably conspicuous at such times, there is a ten because the various patterns are readily observable and follow a sequence or reaction which are organized on the basis of such tendency to report the behavior of animals chain which facilitates analysis. Social be- behavior. However, there are groups which behavior patterns, on the other hand, are often might be integrated as a social unit through less obvious; indeed, it was not until 1939 other behavior patterns; e.g., reciprocal in that their manifestation was related to teractions such as grooming, play, parent gonadal hormones (Allee, Collias and Lu- young relations (Carpenter, 1942, 1952; Scott, 1945), or what Schneirla (1946j includes under trophallactic relationships.

II. Social Organization

Social organizations can be classified into two general categories: social hierarchies and territories. Some species show either one or the other seasonally or throughout the year, whereas others may have elements of both concurrently. Still others have territories during the reproductive phase and hierarchy during the rest of the year. Once established, or even during the incipient stages, a pattern of social organization is typical for a given species. The variation is considerable from species to species, although comparable types of organization are found throughout the vertebrates.

Allee (1952) recognized two major kinds of hierarchies: one based on unidirectional (despotic) domination and the other based on relative despotism in which pecking between any two individuals is bidirectional. The former is often referred to as a "peckright" system, in which the individuals are ranked in an order according to the number of individuals each can dominate without any attack or threat in return. Such a dominance order is usually quite stable, and species so organized are suitable for experimentation insofar as controlled situations can be maintained. A hierarchy based on bidirectional pecking is more fluid because there is an exchange of aggressive acts, and the individual delivering the most "pecks" is considered the dominant member of the pair. In species so organized there is an overlap with territoriality, inasmuch as each individual becomes more dominant as it approaches the center of its territory.

Credit for the development of the concept of territoriality is usually given to Howard (1920), although Lack (1953) and Carpenter (1958) cite even older reports in which some aspects of this behavior were recognized. Evidences of territoriality are often reported in studies on reproductive behavior and have been found in ^-arious classes of vertebrates.

Territorial organization has many forms, depending on how it functions for a particular species. It is often defined as "a defended area." However, there is no evidence that it is the area per se that is defended. According to Emlen (1957), "the term territory is generally applied to an area or space in which a particular animal is aggressive and largely if not supremely dominant with respect to certain categories of intruders." The biologic significance of territory for birds has been discussed by Hinde (1956a), and for all vertebrates by Carpenter (1958). The latter concluded that territoriality apparently, when once established, reduces stress, pugnacity, and nonadaptive energy expenditure.

Aggressive behavior has the tendency to disperse the individuals, as manifested in territorialism. Such behavior is mediated by hormones. Some behavior patterns operate in the opposite direction and result in aggregations by members of the species (Allee, 1931). No gonadal hormones have been discovered which influence gregariousness (other than sexual and parental bonds). Emlen (1952) discussed the social forces which cause the centripetal and centrifugal actions in flocks of birds, and concluded that flocking responses have their physiologic basis in stereotyped neural patterns and are influenced by hormonal factors only so far as these incite disruptive responses associated with sexual or parental activity.

Tendencies to aggregate or to disperse may be seasonal or diurnal (Emlen, 1952), and physical factors such as temperature and light may exert an action (Allee, Emerson, Park, Park and Schmidt, 1949, p. 393). Species of vertebrates vary in the relative distance at which one individual will tolerate the presence of another. Hcdiger (1950, p. Ill) calls this "individual distance" and distinguishes betw^een "distance animals" and "contact animals." The relative proximity at which chaffinches tolerate each other varies with dominance rank and with sex (Marler, 1956). Dominant females allowed subordinate females to come closer than other females, and males permitted females to come closer than males. Submissive behavior promotes toleration. The forces of mutual attraction may develop early in life (Collias, 1952, 1956) by mechanisms that suggest imprinting (Lorcnz, 1935).

In many instances changes in agonistic behavior appear to precede sexual behavior and thereby to prepare the proper social environment for sexual and parental behavior. IVIoynihan (1958) described the behavior of several species of North American gulls in the process of pair formation. The hostility which precedes pairing is associated with the establishment of their territories. Pairformation activities seem to be followed by a reduction of intersexual hostility and the gradual emergence of sexual behavior. According to Tinbergen (1953), the prenuptial behavior of the female appeases the male, suppresses her escape behavior and, together with the courting by the male, facilitates the synchronization of sexual behavior patterns.

The selective value of aggressiveness has been discussed by Collias ( 1944) and Carpenter (1958). Selection may operate on the level of the individual, with the more aggressive ones usually having precedence to food, mates, and cover. On the group level the more socially stable units conserve energy and may leave more progeny.

III. Historical Background

The discovery of a social organization based on agonistic behavior was made by Schjelderup-Ebbe (1913) during a study of calls or sounds made by chickens. Later he summarized observations of the domestic fowl and other birds (Schjelderup-Ebbe, 1935). Many of these were repeated by Sanctuary (1932) and Masure and Allee (1934a), working with chickens. Masure and Allee (1934b) also observed common pigeons and shell parakeets and discovered, contrary to Schjelderup-Ebbe, that some birds do not show absolute dominance, but rather bidirectional pecking (called peckdominance in the earlier reports). Allee (1936) summarized these initial observations and suggested a plan for analytical studies, which included alteration of the physiologic state by hormonal treatment. Noble and his associates (Noble, 1939a, b; Noble and Curtis, 1939; Noble and Borne, 1940; Noble and Wurm, 1940; Noble and Greenberg, 1941) made extensive studies of behavior which stimulated a general interest in the relationship between the endocrines and social behavior in fishes, amphibians, reptiles, and birds. The social organization in baboons was described by Zuckerman (1932), and in monkeys by Maslow (1934). Carpenter (1934) reported the virtual absence of a dominance order in the howler monkey. Yerkes (1939) observed dominance relations between unisexual and heterosexual pairs of chimpanzees and related changes in dominancesubmission to the sexual status of the female.

Since this early period, many investigations have been directed at a clarification of the relationship between the gonadal hormones and social, but particularly agonistic, behavior. Something of the progress that has been made will be apparent from what follows. However, many reviews already exist^ and in this place a particular effort will be made to present a contemporary cross-sectional view of the subject that will contain an indication of the many problems that are in need of study.

IV. Methods

Many experimental techniques have been used in studies of agonistic behavior. As would be expected, they vary greatly, depending on the species, the question it is hoped the experiments will answer, and the connotation of aggressiveness that is accepted. Potter and Allee (1953), Kislack and Beach (1955), Scott and Fredericson (1951), and Scott (1958b) considered aggressiveness as a tendency to start fights. According to this view, the levels of aggressiveness would be measured by latency, i.e., the time between the meeting of two individuals in a test situation and the first overt display of agonistic behavior. However, the term as it is used in this chapter refers to the ability to be self-assertive or to display independence of action (Collias, 1944) . Aggressiveness in this sense is a tendency whereas aggression is an activity. Factors which evoke aggression seem to vary among species and may inchide such as close proximity, training, sex hormone, and pain resulting from attack. The pattern of response may depend on the stimulus situation, the strength of the stimulation received, and the physiologic state or level of response threshold.

  • Comprehensive reviews of aggressive behavior

among vertebrates, including a discussion of hormonal factors, have been prepared by Collias (1944, 1950). Social organization and related phenomena in vertebrates were considered bv Allee, Emerson, Park, Park and Schmidt (1949), Allee (1952), Tinbergen (1953) and Scott (1956, 1958a). General information bearing on the territorial behavior of vertebrates has been brought together by Bourliere (1952) and Carpenter (1958). Other reviews deal with the social behavior of fishes (Aronson, 1957; Baerends, 1957), birds (Hinde, 1956a), ungulates (Darling, 1952), other lower mammals (Hediger. 1952), and subhuman primates (Carpenter, 1952)



In general, in studies of aggressiveness, conditions are best controlled when the animals are observed in pairs or in small groups and this has long been done by many investigators. Paired encounters were used by Maslow (1936) to determine dominance relationships among subhuman primates. If the pairings were made between unacquainted individuals, they were called initial encounters or initial contacts. These were used by Collias (1943) to determine tlie factors which make for success in establishing dominance in chickens, and by Braddock and Braddock (1955) in their work on the fish, Betta splendens. Pairings of mice were used to analyze the effects of thiamine deficiency on fighting success (Beeman and Allee, 1945) and to condition individuals to win or to lose encounters (Ginsburg and Allee, 1942) . Pairings of chimpanzees were made in order to ascertain the effects of the female sexual cycle in female pairs (Crawford, 1940) and between mates (Yerkes, 1940; Young and Orbison, 1944). Corresponding techniques served to test the effects of gonadal hormones in chickens (Allee, Collias and Lutherman, 1939; Allee and Collias, 1940) and of androgen in mice (Beeman, 1947).

Support for the opinion that staged initial pair contests in neural areas, or cages, give better estimates of levels of aggressiveness than rank in a social order or the frequency and intensity of aggression comes from a recounting of what has been found during work with chickens. In a flock of chickens the frequency of pecks delivered by an individual on others is not a measure of the individual's native aggressiveness. In the determination of a peck-order the tabulation of pecks delivered by each bird usually shows no apparent correlation with rank in the social order. Those in the top rank have more individuals to peck and therefore the highest rate of pecking may be expected.


However, the highest rates of pecking by one bird on another may occur between birds at any level above the lowest ranks. These interindividual interactions have been called "antipathies." Unexpected toleration, i.e., low rates of pecking, also may be found at any level. Antipathies may develop when the flock is assembled as a result of a hard fight, or later when a revolt is unsuccessful. Toleration may follow a passive submission in the initial meeting of unacquainted birds. Furthermore, the rate at which one bird pecks another may vary from week to week according to incidents which arise. The peck-order is learned and the laws of reinforcement and extinction apply.

Rank in the hierarchy, or the number of individuals dominated, may be used as a measure of aggressiveness, and may agree with the results of paired encounters (Guhl, 1953). However, the reliability of estimates based on rank in the hierarchy or the number of individuals dominated may depend on the conditions under which the flock was first assembled. At the first meeting the birds engage in initial encounters by pairs which meet at random. Fatigue may set in early for those engaged in lengthy fights, and such individuals may refrain from fighting, or lose subsequent encounters. If new individuals are added after the peck-order is formed, they usually assume low rank. A significant correlation was found by Guhl and Allee (1944) between seniority and social position. These results lead to the conclusion that stimulus situations and other factors (Allee, Collias and Lutherman, 1939) which make for winning encounters need to be controlled and that this can best be done in initial paired encounters.

When groups of animals were employed in the study of aggressive behavior the desirability of certain practices became apparent. Sanctuary (1932) found, when strange hens were added to organized flocks, that the fewer the newcomers in relation to the residents, the greater was the disadvantage to the introduced hens. Flocks of equal size could be combined with the least disparity. In another study social organization was kept in a state of flux by regularly shifting hens from isolation to a flock or between flocks (Giihl and Allee, 1944). The degree of domination or subordination of a hen may be measured by the number of individuals it pecks or avoids. The top-ranking hen habitually pecks all and submits to none, whereas the one lowest in rank has a strong habit for avoidance and does no pecking. Those in intermediate ranks show varying degrees of both habits commensurate with social status. Therefore, the frequency with which individuals display dominance or submissiveness may be altered by subflocking without disrupting the dominance relations among the birds in the smaller groups (Guhl, 1950).

Of extreme importance in the methodology for studying aggressive behavior is the control of what we will refer to as the elements composing the substrate. The problem can be explained, Init it will l)e at some length.

V. Elements Comprising Substrate

The study of animal behavior is beset with problems of multifactorial relationships. This produces either a perplexing situation or an intriguing one, depending on the viewpoint. It is virtually impossible to control all of the known factors in a single experiment, and some apparently minor ones may gain in their influence when others are controlled. There is a continual interaction between the environment and the organism. The experimenter is one of the factors. The importance of this fact, which is also recognized clinically (Matarozzo, Saslow, Matarozzo and Phillips, 1958), has not always been appreciated. The presence of the investigator, his mannerisms, and the methods of handling the animals may alter behavior. It must be recognized, too, that behavior is the expression of an effort to adapt or to adjust, and different conditions may lead to different results. Animals are often maintained in one location and moved to another for experimentation. Many animals can adapt readily to such technicjues, but the time required for adjustments should be considered. In general, domestic species adjust to laboratory conditions with less diflficulty than do wild animals; Hediger (1950) suggests that the confined environment of wild animals requires certain features of their natural environment. Other parts of the substrate are the genie background, meteorologic conditions, and the interaction of drives. All these factors will be considered in the discussion of the influence of the endocrines on social behavior which follows.

A. Heredity and Levels of Aggressive Behavior

The wealth of information from comparative studies provides abundant evidence that the genie background influences the character of an animal's behavior. We will mention only a few: phylogenetic studies of social behavior patterns have been made for orders of insects (Michener, 1953), termites (Emerson, 1938; Schmidt, 1955), bees (Michener and Michener, 1951 ; Michener, 1953), fishes (Winn, 1958), and birds, e.g., anis (Davis, 1942) and tits (Hinde, 1952). The importance of the genie factor is also apparent from observations of and experiments with hybrids {e.g., finches, Hinde, 1956b j, from the existence of species differences {e.g., fishes, Schlosberg, Duncan and Daitch, 1949; Clark, Aronson and Gordon, 1954) and breed differences (e.g., dogs, Scott and Charles, 1953, 1954; chickens. Potter, 1949; Hale, 1954; Allee and Foreman, 1955). Scott (1954) discussed the effects of selection and domestication on various behavior patterns in the dog. In genetically different stocks of male guinea pigs, factors peculiar to the strains affected the behavioral responses to testosterone propionate (Riss, Valenstein, Sinks and Young, 1955). Strain differences were also found in the response of female guinea pigs to estradiol and progesterone (Goy and Young, 1957). Most of the studies cited above were not concerned with agonistic behavior per se, but it must be presumed that strain differences would be as important for the display of agonistic behavior as for all other social behavior including reproductive behavior.

Some breeds of domestic animals have been developed by selection for particular behavior patterns. Terriers among dogs, gamecocks among chickens, and Siamese fighting fish have a long, and largely unknown, history of selection for fighting ability. Scott (1942) found that inbred strains of C57/10 black, C3H agouti, and C (Bagg) mice differed in aggressiveness, activity, and other traits. When C57/10 and C progeny were cross-fostered the behavior characteristic of the strains remained true to heredity (Fredericson, 1952) .

A selective breeding program for levels of aggressiveness in Leghorn chickens was conducted by Guhl, Craig and Mueller ( 1960) . The males and females of the parent generation were of different strains merely because these were available, and there was no information on the relative aggressiveness of either strain. Selection in each generation was based on the percentage of initial encounters won, as supported by rankings in the peck-order. Individuals ranking highest and lowest were used for breeding. This technicjue limited the number of individuals wdiich could be tested. Some of the results are indicated in Figure 20.1 for four generations of selection. Reciprocal crosses were made with the breeders of the F3 generation, and their offspring tended to be intermediate in aggressiveness. These results are indicated by four })oints in the F4 . However, due to uncontrollable circumstances, only a few of these chicks lived to sexual maturity and testing. The upper points are means of 7 males and 8 females from "high" dams, and the lower two points are the means of 3 males and 1 female from "low" dams. The number of individuals selected for breeding and their tested progeny is given beneath the figure for all generations except the crosses. A x" analysis based on the mean percentage of encounters won by individuals from the "high" and "low" lines showed statistically significant differences between the two lines of selection from the F2 through the F4 in both sexes.

Calhoun (1956) made an interesting attempt to determine the extent to which heredity might modify social behavior. He used physiologically unstable DBA/2 and physiologically stable C57BL/10 inbred mice. Among other differing traits, the DBA/2 mice have a high incidence of mammary tumors and marked susceptibility to lethal audiogenic seizures, whereas the C57BL 10 strain has a low incidence of mammary tumors and susceptibility to audiogenic seizures. Both lines had been through extensive artificial selection and always reared in small cages with a restricted social environment. He wished to ascertain whether exposure to a more complex physical and social milieu than previously experienced in many generations of rearing would provide a marked taxing of the physiologic homeostatic mechanisms available to the mice. Four colonies, two of each strain, were established in standardized pens with 17.5 M.- of floor space. The arrangement of nests, food, and water encouraged social interactions. The DBA's fought more frequently and intensely than did the C57's, and the latter developed more toleration and made more passive social adjustments. The C57 mice were more successful in reproduction and died off at a lower rate than did the more aggressive DBA mice.



Fig. 20.1. Result.? of selective breeding for high and low levels of aggressiveness in White Leghorn chickens. Figures show the percentage of initial encounters won by sires, dams, and their progeny. All encounters were between individuals of high and low hnes.


B. Meteorologic Factors

Some of the more immediate effects of meteorologic factors on reproductive and parental behavior can be readily observed. Modification of other forms of social behavior, such as shifts between group living and territoriality, have been reported in some vertebrates to be associated with marked changes in the weather. Petersen (1955 1 noted that the activity of migratory bank swallows on arrival in the spring was influenced by weather conditions. Days of fair weather with temperatures near or above normal appeared to be necessary for taking up territories. Collias and Taber (1951 j found that ring-necked pheasants roosted closer together and in larger groups when the weather was very cold. According to Stoddard (1931), the male of the bobwhite quail {Colinus virginianus) tolerates other males until the first warm days of February. Actions preliminary to pairing may be noted, although the coveys do not break up normally until late April, and even then may reassemble to a certain extent when the weather is cold and raw.


Apparently, adverse weather conditions exert some suppressive effect on aggressiveness, and with increased toleration the territorialism reverts to flocking. Scott and Fredericson (1951) concluded that heat and probably cold tend to reduce the amount of fighting behavior in mice and rats. Combats between mice were more sluggish and shorter at temperatures over 28°C. ; inexperienced mice did not fight at 27 to 28° C.

C. Psychologic Factors

In a social organization based on domination, each individual forms special habits toward each member of the group. As these habits of domination or subordination become well established, the agonistic behavior patterns are reduced in intensity and become symbolic. This mutual interindividual adaptation promotes toleration and has been called social inertia. Such adjustments have been demonstrated in small flocks of chickens (Guhl and Allee, 1944; Guhl, 1958). Evidence that the principles of complex learning apply to agonistic behavior would seem to have been provided following the training of chickens (Radlow, Hale and Smith, 1958), mice, rats (Ginsburg and Allee, 1942; Scott and Fredericson, 1951) , and rhesus monkeys (Miller, Murphy and Mirsky, 1955; Murphy, Miller and Mirsky, 1955) to be either dominant or subordinate. In connection with all this, it is appropriate to ask what effect the psychologic state associated with social inertia has on the behavioral response to hormonal treatment, be it reproductive or social.

Taking the former first, Baerends and Baerends-Van Roon (1950) found in the cichlid fish, Hemichromis, that males that were unsuccessful in establishing territories lacked color markings, but when the dominant and territorial male was removed one of these showed reproductive markings and set up territory. When the new dominant was removed a third male reacted similarly. They concluded that although many of the members of the school are physiologically able to assume reproductive markings and to perform reproductive activities, in a number of them the reproductive motivation was suppressed by the activities of the territorial fish." In chickens, males ranking lowest in the peck-order among the cocks may show varying degrees of suppression of sexual behavior to the point of psychologic castration (Guhl, Collias and Allee, 1945; Guhl and Warren, 1946). One male failed to mate with the hens of the flock even when his social superiors were temporarily removed, but he did mate with strange hens from another flock. Similar situations have been reported by Darling (1952j among wild white cattle of Northumberland, England, and water buffalo of southeast Asia. It is pertinent to the point being discussed that the dominant bull water buffalo must have two other bulls to dominate before he is potent.

The habits associated with the independence of action at top levels in a peckorder may suppress receptivity in females of some species. Hens at upper ranks in the flock tended to be least receptive and those at the lowest levels the most receptive. The females at the top of the hierarchy were in the habit of dominating, whereas those at the bottom submitted readily. The submissive attitude is a component of receptivity. When the degree of domination or submissiveness was altered by subflocking, the differences in the rates of displaying the submissive sexual crouch were reversed (Guhl, 1950). With fewer birds to dominate there was less reinforcement of the aggressive habit and the sexual crouch was evoked. Similar tests with other species of vertebrates should be made to determine the extent to which this psychologic effect is applicable. Relationships between physiologic and psychologic aspects of display behavior in birds have been discussed by Armstrong (1947, Ch. 22). He states that the interconnection of internal and environmental factors has the broad effect of bringing the birds into breeding condition, and the fine adjustments which achieve the final sexual synchronization are given by psychologic factors.

D. Social Inertia and the Development of Social Behavior

To answer the second part of the question, social inertia is also important for the development of social behavior. Chicks reared in groups established certain behavior patterns in relation to each other (Guhl, 1958), the social inertia mentioned above, and required 8 to 13 weeks to develop a new peck-order. Similar chicks reared in partial isolation and assembled at 8 to 10 weeks of age were devoid of such habits. They engaged in fighting and pecking, and formed peck-orders in a matter of hours. Chicks treated with an androgen while reared together established peck-orders somewhat earlier than normal group-reared chicks.

Another experiment was devised to compare the effects of androgen with those of social inertia. The specific question was whether chicks treated with androgen during partial isolation from hatching would form a i^eck-order earlier than treated chicks reared as a group. There were 5 groups of chicks (Fig. 20.2). Two groups of 11 each were pen-reared controls; the individuals of one group received 0.5 mg. testosterone propionate daily, those in the other group were normal controls. Three groups composed of 10 chicks each were reared in partial isolation and treated with the androgen. One was assembled when 31 days old, another at 41 days, and the third when 51 days old. The establishment of dominance relationships (peck-rights) was observed for 56 days in the pen-reared groups and for 7 days after assembly in the case of the 3 isolation-reared groups.

The results are shown in Figure 20.2. The ratios at each curve indicate the number of peck-rights established at that point in relation to the possible number of unidirectional dominance relations in the flock. The group assembled on day 31 nearly completed a peck-order in 1 week, and exceeded the treated males reared as a group. The treated chicks assembled on day 41 failed to establish any dominance relations on the first day and formed only 20 out of a possible 45 pecking relationships by the end of a week. This performance was inferior to the normal pen-reared controls. The results with the group assembled on day 31 indicate that in the absence of social inertia, androgen treatment resulted in some in a certain sequence; sexual behavior usually follows agonistic behavior. However, the typical behavior of this group was sexual. Attempts to mount were frequent and the birds showed strong avoiding reactions. The indications were that at this age there was a conflict between aggressive behavior and the newly developed sexual behavior, which had not yet been subjected to any adjustment. The group assembled on day 51 showed both aggressive and sexual behavior, but with somewhat better adjustment to the conflicting drives. Untreated females (not shown in Fig. 20.2) assembled from isolation did not show this complication, because sexual behavior patterns appear much later in the female. The significant point is that hormonal treatment may shorten the time between the appearance of sequential behavior patterns to the point where psychologic adjustments cannot be made and an imbalance of drives occurs. Endogenous hormones rise more slowly in concentration and allow more time for experience, or learning the adaptive process. In large groups the variability of individuals in development is also a complicating factor.



Fig. 20.2. The total number of peck-rights established at various ages among males reared as a group and others reared in partial isolation and assembled at different ages. The isolated chicks and one group, reared together, were injected with an androgen (Guhl, 1958).



In the same series of experiments an attempt was made to demonstrate the influence of social inertia on the development of social behavior bv normal male chicks.



Fig. 20.3. Differences in the frequency of some behavior patterns of male chicks rotated between isolation and a group, and of others rotated from group to group. The results of group-to-group rotation for each of these two groups are shown separately, and these show social inertia (Guhl, 1958).


Four groups of 10 chicks each were used. The cages were similar except that one was jiartitioned for partial isolation. Two types of rotating group memberships were devised. Every other day, from the 3rd day of age, 1 chick was taken from isolation and placed with one group and a group member was placed in isolation. Chicks were also shifted between the other two groups which were maintained as flocks. Rotation followed a schedule and a chick was in isolation (or in one of the three group cages) for 20 days. Those returned to isolation had nearly 3 weeks during which any social habits or individual recognition might be extinguished, whereas those rotated between flocks continued to have social contacts but with different individuals. The results are given in Figure 20.3 and show that the group into which isolates were rotated had the highest frecjuency of agonistic behavior. In addition to the reduced social inertia, the newcomers from isolation acted as a greater stimulus for aggression than did newcomers from the cages containing flocks of chicks.

E. Interaction of Drives

The tendencies toward aggressiveness and submissiveness may be viewed as drives in the sense that they are forces prompting an animal to activity directed toward certain ends. In a flock of goats (Scott, 1948), delayed feeding increased the amount of fighting in dominant animals, and recent feeding decreased the amount of aggression in dominant animals. In subordinate individuals, delaved feeding caused them to take more punishment but almost never caused aggression. It was concluded that dominance sti-ongly modified the effect of frustration in causing aggression, and that frustration caused aggression in situations in which animals were in the habit of being aggressive. In goats there was no fighting and no dominance when they were given plenty of food scattered about to prevent crowding while feeding.

In mice hunger and thirst did not affect the tendency to fight (Ginsburg and Allee, 1942), nor did vitamin Bi deficiency cause a loss of social status in high ranking individuals until they were in an advanced stage of avitaminosis (Beeman and Allee, 1945). Aggressive behavior was not affected until the individual was physically weakened, and staged pair contacts were strongly influenced by psychologic factors. In the chaffinch (Marler, 1955) starvation, however, reduced the tendency of subordinates to avoid dominant individuals. Inasmuch as females are less aggressive than males, and avoidance reactions are less intense, the toleration which developed toward low ranking individuals was more pronounced in female flocks. In rats Hall (1936) found that nonhungry individuals display greater emotionality than do hungry rats. He concluded that needs, other than the need to escape, inhibit the display of emotional behavior by distracting the animal from the fear-provoking aspects of the situation."

Among birds there are a number of situations in which two or more drives are in conflict. The conflict may be between aggressive and sexual activities, or between attacks and escape behavior. What makes the conflict apparent is that sometimes the resultant pattern of behavior is atypical of the drives in conflict. These patterns are called displacement activities and have been variously named and defined. According to Bastock, Morris and Moynihan (1953) "displacement activities apparently can occur in two situations. (1) Displacement activities may be performed by an animal in which two or more incompatible drives are strongly activated; each drive prevents the expression of the other (s). (2) Displacement activities may also be performed by an animal in which one drive is, at the same time, both activated and thwarted." A number of such conflicting situations is mentioned by Armstrong (1947, pp. 99lOlj.

An interesting study of the conflict between the tendencies of attacking, fleeing, and courting in the male chaffinch was made by Hinde (1953). The male is dominant over the female in winter, and in the spring the dominance is reversed. The male's display occurs in those situations in which his tendencies to approach (court) and to flee from the female are in approximate balance. A similar analysis can be applied to the female. Attempts to copulate may be unsuccessful if the sex drives of both individuals are not sufficient to inhibit aggressive behavior.

The presentation of the material which follows is given with the assumption that the many factors enumerated above have been controlled.

VI. Gonadal Hormones and Social Behavior

A. Social Behavior and the Reproductive Cycle

The stimulating action of gonadal hormones on social behavior might long ago liave been postulated from the close relationship between reproductive state and behavior, in wild species in which reproduction is generally seasonal, and in many laboratory and domesticated species in which cyclic activity is continuous without intervening periods of anestrum. Relationships of this sort are well known in birds (Armstrong, 1947) and many mammals: the red deer, Cervus elaphus (Darling, 1937), the wapiti, Cervus canadensis, the moose, Alces americana shirasi, the chamois, Rwpicapra rupicapra, the wild boar, Sus scrofa europ. (Altmann, 1952, 1956), and others. Territorialism may develop during the breeding cycle among frogs (Martof, 1953; Test, 1954) and reptiles (Greenberg and Noble, 1944). In fish, seasonal modification in breeding aggregations has been described by Aronson ( 1957 ) . It is common knowledge that the males of many species show combative behavior during the breeding season. Rowan (1931) observed that the male bobo link attacks other males in the spring, although peaceful unisexual flocks are formed when the breeding season wanes. Fighting during the reproductive phase was reported in the gentoo penguin, Pygoscelis papua (Roberts, 1940) and in the herring gull, Lams argentatus (Boss, 1943).

Studies have been made which show a cyclic relationship between changes in the size of the gonads and the sequence of social and reproductive behavior patterns occurring before and during the breeding season. Such a relationship is presumed to be universal in seasonal breeders — the exception would be the cause celebre. Changes in the grouping and dominance relations among free ranging ring-necked pheasants {Phasianus colchiciis) are related to sea


sonal increase in the weight of the testes (Collias and Taber, 1951 j. During the gonadal quiescence of winter the birds remain in marshes as small groups with shifting memberships. Evidence of peck-orders among cocks and hens was found. The males pecked the females during competition for food. As the breeding season advanced there was a gradual increase in antagonism between members of the same sex and in attraction between individuals of opposite sexes (Fig. 20.4). With an increase in testis weight the male groups broke up, territories were established, and harems were formed. Cocks that ranked high in the winter dominance order established territories, whereas those of low social status failed to do so. Genelly (1955) reported on a study of the annual cycle of the California quail {Lophortyx calif ornica) . Of particular interest is the shift from a peckorder type of organization during sexual quiescence to territoriality during the breeding season. The establishment of breeding territories by the Anna hummingbird {Calypte anna) has been correlated with testis volume and histologic changes (Williamson, 1956).




Fig. 20.4. Expicssions of display or dominance between and within sexes of ring-necked pheasants, from January through April. Broken lines represent infrequent occurrence; solid line, frequent occurrence. The sequence of behavior changes is superimposed upon the increase in testis size (Collias and Taber, 1951).



An extensive study in which behavior was related to the seasonal cycle was made by Petersen (1955) with the migratory bank swallow (Riparia riparia). These birds arrived in the spring in flocks which congregated at breeding sites on warm days.



Fig. 20.5. Summary of behavior elements in the breeding cycle of tlio Ijank .swallow (Petersen, 1955).



Fig. 20.6. Summary (Petersen, 1955).

Unpaired birds, proba])ly males, selected burrowing sites and set up limited territory. Pairing resulted from the persistent returning by the female to an area in the face of aggressive attack. After the pair-bond was formed, both mates shared in the attack on trespassers. After the reproductive cycle was comjileted, and after the end of nesting, toleration of other individuals was restored and flocking ensued. Peterson related the sequence of social, sexual, and ])arental behavior patterns (Fig. 20.5) to physiologic and morphologic changes (Fig. 20.6).

Modifications in agonistic behavior occur in continuous breeders and under the nonseasonal conditions of the laboratory. The non-spawning cichlid fish, Aeguidens latifrens, fights the male more often than does the gravid female (Breder, 1934) . Female guinea pigs become submissive to, or tolerant of, the male during estrus (Young, Dempsey and Myers, 1935). According to Pearson (1944) the female short-tailed shrew, Blarina brevicauda, fights the male when nonreceptive, but during estrus is quite docile, as is the golden hamster (Kislack and Beach, 1955) . Female chimpanzees become dominant (in the sense of attaining a response priority during food-getting tests) over other females during the period of maximal genital swelling (Crawford, 1940).

Not to be overlooked is the probable significance of the fact that such changes in behavior are seen in females, in which ovarian activity is cyclic, rather than in males in which testicular activity is continuous.

B. Androgens and Aggressiveness

In most subhuman vertebrates which have been observed in sociobiologic studies the males are more aggressive than the females and aggressiveness increases during the sexual development of maturing animals as well as during the breeding season. That early castration of domestic male animals reduces pugnacity has long been known (Rice, 1942). Goodale (1913) noted the lack of combativeness in the capon, and Scott and Payne (1934) found that castration eliminates fighting in the tom of the bronze turkey, Meleagris gallopavo. According to Uhrich (1938), male mice castrated as adults continue to fight, whereas those gonadeetomized prepubertally rarely fight. Evans (1936) observed that castrated males of the lizard, Anolis carolinensis, continue to fight, and that females rarely fight unless they are ovariectomized. From this, he concluded that ovarian hormones inhibit fighting. However, Greenberg and Noble (1944) expressed the opinion that both sexes are innately aggressive and that the seasonal increase in testicular hormone in the male transforms mere antagonism into territoriality. Castration of the male gobiid fish, Bathygobius soporator, results in the disappearance of combative behavior, but courtship is not impaired. Nonspawning males show normal combat, and hypophysectomy is followed by a cessation of both combat and courtship (Tavolga, 1955). A continued display of pugnacity was observed in castrated starlings, Sturnus vulgaris (Davis, 1957a), and in castrated male pigeons (Carpenter, 1958) . Geldings ranked among mares in a common dominance order (Montgomery, 1957). These observations point to androgen concentration in the blood as influencing the level of combativeness. Apparently, however, the extent to which castration affects the level of aggressiveness varies among species, and according to the age at which the animal is gonadectomized. The experimenter's connotation of aggressive behavior and the method of its measurement may result in variations in the interpretation of the effects of castration.

The administration of androgen often produces an increase in aggressiveness in normal adults and in castrates, and precocity in immature individuals of either sex. Treatment of fishes has been followed mostly by observations of sexual behavior (Aronson, 1957, p. 286), but Noble and Borne (1940) reported advancement in rank by spayed and intact female swordtails, Xiphophorus helleri, after implanting pellets of testosterone. Juvenile and young adult urodeles, Tritunis viridescens, treated with whole pituitary and luteinizing hormone (LH) fraction pre-empted first place in their hierarchies (Evans, 1956). Male Anolis treated with testosterone propionate fought more than the controls (Noble and Greenberg, 1941). Subordinate males of Sceloponis grammicus received an androgen (Perandrenj and rose in their respective hierarchies (Evans, 1946). Among birds, androgen treatment caused an increase in aggressiveness in the ringdove, Streptopelia risoria (Bennett, 1940), the herring gull, Larus argentatus (Boss, 1943) , and in poulards (Davis and Domm, 1943). Female rats injected with androgen became irritable and pugnacious (Ball, 1940; Huffman, 1941; Beach, 1942). Tollman and King (1956) injected an androgen into young gonadectomized male and female C57BL/10 mice and found that the males responded more aggressively toward each other than did the females. They concluded that either the nervous systems of both sexes responded differentially to the hormone or that females do not provide as adequate a stimulus for aggressive responses as do males.

Increase in the social status of androgentreated individuals has been recorded for chickens (Allee, Collias and Lutherman, 1939; Douglis, 1948), mice (Beeman, 1947), and chimpanzees (Clark and Birch, 1945; Birch and Clark, 1946). However, three males of free-living valley quail which received pellets of testosterone propionate became pugnacious toward other males but failed to alter their positions in the peckorder of the covey (Emlen and Lorenz, 1942). Hens receiving androgen also failed to rise in the social order (Williams and McGibbon, 1956) . In both of these instances the group remained intact, and presumably the social habits withstood the influence of lowered thresholds for aggressive action l^'oduced by the androgen. These results differ from those obtained by Allee, Collias and Lutherman (1939), as did the procedure, because in the latter experiment pair contests were conducted between individuals of different flocks containing the treated birds. It is possible that a treated hen, if promptly returned to her flock from an initial encounter (which she usually won) , was still highly stimulated, and if she engaged in fighting with a threatening superior penmate, a reversal of dominance would occur.

An experiment which is the converse of those described above has recently been performed, but not previously reported, by Robert Buchholz of Kansas State University. He attempted to determine whether a low ranking bird could be made the dominant individual in the flock by varying the psychologic state rather than by treatment with androgen. The chickens used were males which had been reared together. The lowest ranking bird, which had never been observed to peck a penmate, was selected for experimentation. When 11 weeks old, 7 birds were isolated for 33 days to extinguish the memory of past associations. When approximately 16 weeks old, the lowest ranking male was placed into a pen for 1 week to give him the advantage associated with prior residence. When a female was added he dominated her without any difficulty. After 2 days she was removed and a former penmate, which was immediately above him in rank previously, was introduced. The formerly subordinate male gained dominance over him and all of his other former penmates which were introduced during the course of 1 day in the reverse of the former peck-order. By this method the original lowest ranking male became the top ranked bird. It is apparent that the chicken as well as the mouse (Ginsburg and Allee, 1942) is a species in which psychologic factors can be instrumental in the attainment of a state that formerly would have been thought of as solely the consequence of hormonal action.

Changes in agonistic behavior after the cessation of hormonal treatment have been investigated. Birch and Clark (1946) noted a reversal of dominance to the pretreatment status in adult ovariectomized chimpanzees, whether they were given methyl testosterone or estradiol. In ringdoves Bennett (1940) also found a tendency of previously treated birds to return to their former social rank. However, Allee, Collias and Lutherman (1939) reported that the social position which treated hens won persisted as long as these flocks were under observation. These contrasting results on the two species of birds may perhaps be explained on the basis of qualitative differences in the social inertia of these species. In the peck-right system found in chickens, repeated pecking reinforces the unidirectional pecking and maintains dominance relations, whereas the bidirectional pecking characteristic of doves results in a more fluid social order. Thus, the relative permanence of social gains or losses induced by exogenous hormone may be influenced, among other factors, by the type of social behavior patterns peculiar to the species.

C. Estrogens and Submissiveness

The reports that have been made following observations and experiments on the relationship between estrogens and the social order have resulted in a confused picture. There are species such as the red-necked ])halarope, Phalaropus lobatus, in which the female in the reproductive phase is the more colorful, sings, fights, and entices the male (Tinbergen, 1935) . But in the case of many of the lower mammals that have been studied, the female is submissive when follicular development is at its height, and resistant to the male or even strongly aggressive at other times. This was long ago noted in the female guinea pig (Young, Dempsey and Myers, 1935) and has more recently been recorded for other species. The female opossum has been observed after a heat period to attack and kill a male double her weight (Hartman, 1945). Pearson (1944) states that the nonreceptive female short-tailed shrew faces the male whenever he is near and repulses his advances with lunges, loud squeaks, and sometimes a long, shrill chatter. Evans' (1937) observation that ovariectomy of the lizard, Anolis carolinensis, increased the territorial response, may not be unrelated. The change in behavior at estrus, such as that described for the guinea pig, opossum, and shrew, was made the subject of an investigation by Kislack and Beach (1955). Intact, estrous and diestrous females, and estrogen-treated spayed animals were tested in pairs with males. Spayed hamsters were continually aggressive, although somewhat less so than intact diestrous females. The administration of estrogen alone was followed by a slight increase in aggressiveness, but progesterone injected after estrogen eliminated fighting and reduced other forms of aggression. Progesterone alone had no influence on the behavior of spayed hamsters. It was concluded that there is a negative relationship between sexual receptivity and aggressiveness, w^iich depends in large measure on ovarian secretions. In the words of the authors, the ovarian hormones that render the female receptive also inhibit her tendency to attack the male.

In other experiments the results of treatment with estrogens were ambivalent or negative. Allee and Collias (1940) injected estradiol into intact hens and discovered only a slight tendency toward reduced aggressiveness and lowered status in the peckorder, even w^hen large amounts were given. Both male and female chicks of the domestic fowl injected with an estrogen formed a hierarchy which was determined largely by avoidance reactions (Guhl, 1958). Individuals of both sexes gave the submissive sexual crouch when a hand was held over them. Pecking was rare and the social order was called an avoidance-order rather than a peck-order. Emlen and Lorenz (1942), on the other hand, did not observe a behavioral response in valley quail given estrogen. Shoemaker (1939) and Noble and Wurm (1940) also obtained negative results with canaries and night herons, respectively.

Young rhesus monkeys were tested with an androgen and an estrogen (Mirsky, 1955). Unisexual social groups of 5 were organized on a hierarchial system. Those in ranks 5 and 2 received implanted pellets of the androgen or the estrogen in two different periods separated by an interval without treatment. Two pairs of males and two pairs of females of known dominance relations were tested. The subordinate member of each pair was given either androgen or estrogen. In no case was hormone administration accompanied by a significant decrease in either dominance or subordinate l)ehavior scores.

Except for the report that a prepubertally castrated male showed enhanced dominance status under androgen therapy, and subordinate status as a result of estradiol administration (Clark and Birch, 1945), investigations on the chimpanzee have yielded results that are not clear. According to Yerkes (1939), the importance of the sexual condition was established. The dominant female of a pair, w^hen in estrus, ordinarily grants privilege to her subordinate companion, whereas the subordinate female, when in estrus, may achieve privilege and act as if temporarily in control. The statement is not made that the subordinate member of a pair becomes dominant when she is in estrus. Crawford (1940) provided additional evidence that a response priority in a food competition situation is related to the sexual status of the females. In 9 of 13 pairs in which changes in response priority occurred, the subordinate member obtained food more often when in the follicular phase of the cycle. Again, the behavior was described as a yielding of priority by the dominant subject with only the weak suggestion of an increase in aggressiveness on the part of the subordinate animal. However, Birch and Clark (1946, 1950) and Clark and Birch (1945) state that estrogens increase the aggressiveness and dominance tendency of female chimpanzees and that the granting-of-privilege concept is superfluous.

Certain circumstances should be noted in any consideration of these latter studies. Only three females were used and Yerkes and Crawford had observed much variability in their experiments. Further, the subjects had been ovariectomized postpubertally and had been together intermittently for several years. The dominance order was Lia, Nira, May. Nira was paired with Lia in a food competition situation before, during, and after treatment, and May was tested similarly in pairings with both of her social superiors. Nira obtained higher competition scores during treatment, whereas May failed to show any changes. Before ovariectomy. May mated readily with the males when she was in the swelling phase, whereas Nira during 5 years as a mature female had been known to copulate only once despite frequent attempts to breed her. Two questions arise: Did Nira's failure to breed before ovariectomy indicate abnormality? Did agonistic experiences before ovariectomy augment or suppress any probable effects of estrogenic treatment?

D. Are Aggressiveness and Submissiveness Separate Behavior Patterns?

Before leaving the subjects of estrogens and submissiveness, and androgens and aggressiveness, the alternative possibilities must be considered that these antithetical behaviors are (1) independent tendencies or (2) extremes on the same scale of social interactions. As a starting point for the discussion, the reader will be reminded that, except for the claim by Birch and Clark that estrogens increase the aggressiveness of the female chimpanzee, opinion is general that dominance is lowered (or submissiveness is increased) by these hormones (Collias, 1944; Beach, 1948). To the holder of this view who also accepts the conclusion that androgens enhance aggressiveness, it is only a step to the hypothesis that aggressiveness and submissiveness are independent traits, that aggressiveness is essentially but by no means exclusively masculine and submissiveness essentiallv but bv no means ex


clusively feminine. But the alternative concept that aggressiveness and submissiveness are merely opposites on the same scale of social interactions must be considered. Sup{)ort for such an opinion might come from the fact that both types of reaction are shown by the same individual in appropriate situations. However, this is also true of sexual behavior, but in the case of sexual behavior, a rather convincing body of evidence has accumulated that two mechanisms are involved (for a review of the subject see the chapter by Young, and for new data obtained during an investigation of the patterns of inheritance of masculine and feminine behavior in female guinea pigs see Goy and Jakway, 1959). A solution of the problem may come from further work with gamecocks which have been selected for persistence in fighting and may fight to the death without showing avoidance behavior. It was a strain of guinea pigs (strain 2), in which the females normally display little or no masculine behavior, that provided the genetical evidence for the independence of masculine and feminine components of sexual behavior (Goy and Jakway, loc. cit.).

E. GONADAL HORMONES AND THE

DEVELOPMENT OF SOCIAL

BEHAVIOR

A discussion of the development of social behavior should be related to the heredityenvironment or instinct-learning controversy, which, however, is beyond the scope of this chapter. Should there be a need for references to recent views on this subject, several publications are available (Tinbergen, 1951; Lehrman, 1953; and Emlen, 1955). Some observational studies on the socialization of young animals have been reported for birds (Collias, 1952), mice (Williams and Scott, 1953), sheep (Scott, 1945), sheep and goats (Collias, 1956), and dogs (Scott and Marston, 1950) . Most of the experimental studies have been focused on the precocious display of sexual behavior and are discussed in the chapter by Young.

Collias (1950) began treatment of male and female domestic chicks with testosterone and estradiol when they were 2 days old. Dosages of 0.1, 0.3, 0.5, and 0.7 mg. of


1258


HORMONAL REGULATION OF BEHAVIOR


either hormone were given daily to different chicks for 30 days. The number of aggressive pecks observed was proportional to the dosage of androgen given to male chicks. With the lower dosage, pecking was more frequent than attempted matings. Testosterone was more effective than estradiol in inducing aggressive behavior. Males were much more responsive to the androgen than females. Submissive behavior was not reported. The conditions under which these chicks were reared were not given, nor were the dominance relations mentioned.

Experiments to determine the approximate age at which chicks develop agonistic behavior and establish a social order, and the effects of gonadal hormones and social inertia on the precocity of such behavior were reported by Guhl (1958). In small groups of chicks the males developed aggressive behavior earlier than the females; in mixed flocks there were heterosexual peck-orders, with males pecking more frequently than females. There was a gradual trend toward unisexual pecking. Some chicks were reared in partial isolation from the second day after hatching and assembled into groups when their respective control flocks of the same sex established a peck-order (8 to 9 weeks for males, 10 weeks for females). These birds formed a peckorder in a matter of hours, indicating that it did not require 8 to 10 weeks of learning to form a dominance order. This difference between group-reared and assembled isolation-reared birds may have been related to either the maturation of the endocrine and nervous systems, or it may be that social inertia in the group-reared chicks suppressed the influences of developmental processes thereby producing a time lag in the evocation of agonistic behavior.

As a part of the same investigation, individuals in small unisexual groups were injected with either testosterone or diethylstilbestrol. Each treated group was matched with a control group from the same hatch. In all but one group the injections were begun the 2nd or 3rd day after hatching. Dominance or subordination was established somewhat earlier in the treated groups, depending on the hormone used. The androgen-treated chicks, irrespective of sex.


showed increased aggressiveness, whereas the estrogen-treated chicks, again irrespective of sex, were more submissive and the social order was determined by the consistent avoidance by each chick of speciflc penmates. However, the differences between the means of experimentals and controls are small and do not suggest any marked precocity in agonistic behavior as a result of treatment with gonadal hormones.

In the same study (Guhl, 1958) capons were used to determine the age at which dominance-subordination relations (peckrights) may be established in the absence of androgen (Table 20.1). For comparison there was one group of normal males and one group of capons receiving large dosages of testosterone propionate daily (0.5 mg. beginning the 10th clay which was increased by 0.5 mg. weekly for 4 weeks) . Caponization was on the 9th day of age, and therefore the untreated capons had little or no endogenous androgen (Breneman and Mason, 1951). The mean age at which the untreated capons established peck-rights was 13.7 weeks, whereas the mean for the normal males was 9.9 weeks, and for the treated capons 7.8 weeks. It is of interest that a social order developed by the 17th week in the apparent absence of androgen, and that the high level of treatment enhanced the formation of a peck-order over the controls by only 1 week, the 12th week compared with the 13th week for the normal males.

VII. Releasers and Other Mechanisms in Social Behavior

Secondary sex characters such as adornment and color, postures, odors, and certain sounds, have a place in the mediation of social behavior and are thought to function as releasers of specific behavior patterns. Such stimuli may be simple or very complex configurations (Tinbergen, 1951).

In an excellent review of the behavior of cichlid fishes, Baerends and Baerends-Van Roon (1950) related chromatophores to behavior patterns. Six types of chromatophores were discussed showing various methods of development and control. In Tilapia natalensis the black reproductive markings developed under the physiologic conditions typical of the reproductive pe


GONADAL HORMONES AND SOCIAL BEHAVIOR


1259


TABLE 20.1 The effect of androgenic treatment on the development of peck-rights in caponized chicks as compared with normal cockerels and capons of the same age Arrows indicate deviations from a straight-line peck-order.


Number Pecked


Weeks of Age


Normal males


8


GV





1


3


3


1








7


GY



1



3


2



1








6


VY




2


1




1


1


1






5


V








2


2


1






3


^ ^







1




2






3


Cvv






1



1



1






3


\ry




1


1






1






1


YY





1












BB















36


Total



1


3


7


6


4


6


3


« 






Androgen-treated capons, 10th day to 63rd day


45


GB GV

B ^ R VB,

Y BB-^

V GR VY


Total


3


2


1


2




1







5


2


1 1


1 2



1 2








2


1


1

1


1 2

1


1

1

1


1 1

1 1


2 1


1 1






10


5


5


»


3


7


4


2






Capons


8


R










2


1


4


1



7


GV




1


1



1


2



2






6


GY





1




1


1


2





1


4


_GR








1


1


1





1


4


\VY









1





1


2


4












1



3


2


GB












1



1


1


GG














1



G















36


Total




1


2



1


4


3


7


1


6


2


9


riod, but contraction and expansion were controlled by the nervous system. The bright red markings of Hemichromis were also shown only when the fish engaged in courtship. The reproductive colors function in fighting displays and in territoriality during the breeding season. Nonterritorial fish were pale, and individuals crossing territorial boundaries were not molested if their


chromatophores were contracted. It was suggested that the development of these chromatophores probably is under the control of the pituitary.

Noble and Curtis (1939) found that ripe females of Hemichromis himaculatus selected bright red males when given a choice among females and males in different stages of maturity. Tests by Tinbergen (1951, p.


r2()0


HORMONAL REGULATION OF BEHAVIOR


27) showed that the red undersides of the three-spined stickleback, Gasterosteus aculeatur, elicited aggression irrespective of the size or shape of the models. Apart from color, a head-downward posturing was also effective. The hormonal relation to color or posturing was not established. In Gambusia hurtadoi the intensity of yellow markings on the dorsal fin, at the base of the caudal fin, and on the ventral portion of the caudal peduncle were correlated with rank in the social hierarchy (McAlister, 1958).

Evans (1955) discussed various types of releasers found among reptiles, which included postures, colors, and sounds. Many of these occur only in sexually mature individuals. Nocturnal species tend to use auditory cues whereas diurnal species do much posturing, often with pigmented areas drawing attention to these movements. The close relationship between hostile and sexual behavior patterns was shown by Greenberg and Noble (1944) in Anolis carolinensis, because reaction patterns may shift readily from one form to the other in either direction. The crest in this species was stimulated by testosterone propionate.

Color in birds was one of the first of the secondary sex characters to receive attention in its relation to agonistic behavior (Huxley, 1934). The songs of birds are generally accepted as indicators of the reproductive phase and often are related to territoriality (Armstrong, 1947, p. 293).

Lorenz (1950, p. 242) , in his discussion of the subject, defined a social releaser as a "device — either a property of color and/or shape, or a special sequence of movements, or, for that matter, of sounds, or a scent — specifically differentiated to the function of eliciting a response in a fellow member of the species. To every releaser, as an organ for sending out sign stimuli, there corresponds a perceptual correlate, an 'organ' to receive sign stimuli and to activate the answering reaction." The latter he called a releasing mechanism. The point of interest is whether any of the releasers, or the socalled releasing mechanisms, are influenced by gonadal hormones.

With respect to the former, when they are clearly defined secondary sex characters, the answer has been given in countless in


vestigations and reviews (see particularly Lipschiitz, 1924, chapter 2; Allen, Danforth and Doisy, 1939, p. 185, 251, 340, 499, 545; Beach, 1948, chapter 10; and the chapters by Forbes and van Tienhoven in this book). Whether the functioning of releasing mechanisms, that is, visual, auditory, olfactory, and tactile receptors, and central neural tissues, is influenced by gonadal hormones is less certain. The subject is discussed at length by Lehrman and Young in the parts of their chapters dealing with the mechanism of the hormone actions which stimulate parental and mating behavior. Briefly, the opinion has been expressed that gonadal hormones act on peripheral receptors (Carter, Cohen and Shorr, 1947 ; Beach and Levinson, 1950) and olfactory sensitivity (LeMagnen, 1952a, b, 1953). Tavolga (1955) castrated males of the gobiid fish, Bathygobius soporator, and noted that they act as though they do not "perceive" the difference between males, gravid females, and nongravid females. He concluded that testicular hormones affect the threshold of visual, chemical, and possibly auditory sense organs.

Particularly pertinent to the subject is the discussion presented by Birch and Clark (1950) following their investigation of the mechanism of estrogen-induced dominance in chimpanzees. As they wrote, the problem centers around the differential effectiveness of estrogen in producing changes in the dominance status of males and females. Testosterone, whether given to males or females, was assumed to facilitate aggressive behavior by an action on the central nervous tissues. Estradiol reduced aggressive tendency in the two sexes and the effect was assumed to be central. But there is a second effect on the female which is peripheral and results in the swelling and increased irritation of the sex skin. The facts that dominance-status paralleled the engorgement of the sex skin, and that prevention of the latter by the simultaneous administration of progesterone reduced the dominancestatus, were the basis for concluding that the peripheral effectiveness of estrogens accounts for their effects on dominance. The case is weakened, unfortunately, by the authors' failure to eliminate the possibility that the progesterone given to inhibit sex


GONADAL HORMONES AND SOCIAL BEHAVIOR


1261


skin tumescence may also have antagonized other actions of the estrogen (for a discussion of this action of progesterone see the chapters by Hisaw, Villee and Young on the ovary). If progesterone had this effect in these animals, the reduction in dominance which followed its administration was not necessarily related in any direct way to the prevention of swelling.

VIII. Social Stress and the Endocrine System

Heretofore, discussion has been limited to the gonadal hormones and aggressiveness. There remains another axis, i.e., the effect of aggressiveness on reproduction. The nature of the relationship does not appear to l)e that of a feed-back, as our statement of the problem suggests. Females as well as males are affected, and much of what has been done indicates that the pituitiary-adrenal axis is involved. Mammals with cyclic populations seem most susceptible.

Christian (1950) reviewed the symptoms and conditions associated with the die-offs in mammals having population cycles. These were related to the general-adaptation syndrome of Selye (1947). A working hypothesis was developed for the population crash which terminates the cycle. "Exhaustion of the adrenopituitary system resulting from increased stresses inherent in a high population, especially in winter, plus the late winter demands of the reproductive system, due to increased light and other factors, precipitate population-wide death with the symptoms of adrenal insufficiency and hypoglycemic convulsions." Elements of this hypothesis are supported by rather impressive evidence.

Southwick, (1955a, bl, in a carefully controlled experiment with house mice {Mus tnuscuhis) , found that the amount of aggressive activity increased as the density of the population increased. Crowcraft and Rowe (1957) in a similar experiment, but with some modifications, found that reduced fecundity of the females was the most important single factor limiting population growth. They concluded that some factor other than fighting or food shortage appears to inhibit ovarian activity. Christian (1955) showed that mice mantaincd in groups have


heavier adrenal glands than mice kept in isolation, and that the adrenals and reproductive organs of wild house mice are more responsive to stress than those of laboratory albino mice. In a subsequent study of populations of different sizes and of isolated controls, and with food and water in excess, Christian (1956) analyzed the endocrine responses. The results were indicative of an amount of stress proportional to population density. The secretion of adrenocorticotrophin increased in response to stress and gonadotrophin decreased. Increased adrenal size and low eosinophil counts were taken as evidence for an increase in adrenocortical activity in a dense population of the meadow vole, Microtus pennsylv aniens (Louch, 1958). The results from one study of the chicken (Siegel, 1959) suggests that the response of this species may perhaps be similar to that of the mouse and meadow vole. The adrenals were heavier in birds under crowded conditions than in those with more floor space per bird. With progressive decrease in the density of the flocks, adrenal weights declined.

Three urban populations of Norway rats {Rattus norvegicus) with histories of stable high population densities were reduced by trapping to an average of 32 per cent below the maximal density. There was a mean decline of 28.3 per cent in the adrenal weights immediately following population reduction, and 7 months later the adrenal weights were 22.4 per cent below the original values (Christian and Davis, 1955). Richter (1954) found that the cortexes of adrenal glands were much smaller in the domesticated laboratory rat than in the wild Norway rat. Population cycles of the vole {Microtus arvalis Pallus) in Germany were investigated by Frank (1957). He concluded that intraspecific social behavior was of great importance for the events of population dynamics. Crowding favored competition and caused a state of psychologic excitement which was transformed by the pituitaryadrenocortical system into physical stress. This, acutely combined with the stress of food shortage, produces a "readiness" for a crash in the vole population. The ultimate trigger was an additional stress of meteorologic events. Davis (1957b) stated that


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competition and fighting increase as the population increases and this results in a number of responses including the hypertrophy of the adrenal cortex. A number of ensuing responses reduces the reproductive rate and increases mortality. Thus reproduction is reduced or, if the behavior patterns and physiologic responses are not precisely adjusted, a population decline may occur. In this manner, behavior acts as a homeostatic mechanism for populations.

Conceivably, this important generalization is premature, at least in this form. The extensive data on the Iowa muskrat, Ondatra zibethicus (Errington, 1957), do not indicate that social stress is a major factor in the population cycle of this species. There may be other exceptions. In addition, the application of newer tests of adrenal function would be desirable.

IX. Concluding Remarks

Much work has been done in an effort to ascertain whether a relationship exists between gonadal hormones and the social behavior which is displayed so conspicuously at the time of reproduction. There will be disappointment that more exact information has not been obtained. This can be explained in part by the circumstance that endocrinologic, neurologic, and psychologic processes of the most complex types are involved. Such being the case, any analysis of the many problems requires the utilization of endocrinologic, neuroanatomic, neurophysiologic, and psychologic techniques. Unfortunately, however, application of the rigorous tests which are a part of these techniques has not been possible. The end points thus far available to the investigator of social behavior are not as sharp as those on which the endocrinologist would insist; neural centers which might be inactivated or stimulated electrically or chemically are not known to exist, and the psychologist is handicapped by the variables inherent in any study of a behavior involving interaction with other animals. On the other hand, it may be expected that as more work is done, the handicaps imposed by these restrictions will be overcome and a more gratifying progress may be anticipated.


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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
Young WC. Sex and internal secretions. (1961) 3rd Eda. Williams and Wilkins. Baltimore.
Section A Biologic Basis of Sex Cytologic and Genetic Basis of Sex | Role of Hormones in the Differentiation of Sex
Section B The Hypophysis and the Gonadotrophic Hormones in Relation to Reproduction Morphology of the Hypophysis Related to Its Function | Physiology of the Anterior Hypophysis in Relation to Reproduction
The Mammalian Testis | The Accessory Reproductive Glands of Mammals | The Mammalian Ovary | The Mammalian Female Reproductive Cycle and Its Controlling Mechanisms | Action of Estrogen and Progesterone on the Reproductive Tract of Lower Primates | The Mammary Gland and Lactation | Some Problems of the Metabolism and Mechanism of Action of Steroid Sex Hormones | Nutritional Effects on Endocrine Secretions
Section D Biology of Sperm and Ova, Fertilization, Implantation, the Placenta, and Pregnancy Biology of Spermatozoa | Biology of Eggs and Implantation | Histochemistry and Electron Microscopy of the Placenta | Gestation
Section E Physiology of Reproduction in Submammalian Vertebrates Endocrinology of Reproduction in Cold-blooded Vertebrates | Endocrinology of Reproduction in Birds
Section F Hormonal Regulation of Reproductive Behavior The Hormones and Mating Behavior | Gonadal Hormones and Social Behavior in Infrahuman Vertebrates | Gonadal Hormones and Parental Behavior in Birds and Infrahuman Mammals | Sex Hormones and Other Variables in Human Eroticism | The Ontogenesis of Sexual Behavior in Man | Cultural Determinants of Sexual Behavior


Reference: Young WC. Sex and internal secretions. (1961) 3rd Eda. Williams and Wilkins. Baltimore.


Cite this page: Hill, M.A. (2020, August 7) Embryology Book - Sex and internal secretions (1961) 20. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Sex_and_internal_secretions_(1961)_20

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