Book - Sex and internal secretions (1961) 21

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I have decided to take early retirement in September 2020. During the many years online I have received wonderful feedback from many readers, researchers and students interested in human embryology. I especially thank my research collaborators and contributors to the site. The good news is Embryology will remain online and I will continue my association with UNSW Australia. I look forward to updating and including the many exciting new discoveries in Embryology!
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



HORMONAL REGULATION OF PARENTAL

BEHAVIOR IN BIRDS AND

INFRAHUMAN MAMMALS

Daniel S. Lehrman, Ph.D.

PROFESSOR OF PSYCHOLOGY AND DIRECTOR, INSTITUTE OF ANIMAL

BEHAVIOR, RUTGERS, THE STATE UNIVERSITY,

NEWARK, NEW JERSEY


I.' Introduction 1269

11.^ Hormones and Parental Behavior in

Birds 1269

A. Nest-building 1269

1. Varieties of nest-building 1269

2. Correlations hplween nest-building

and other behavior 1271

3. Nest-l)uilding and gonadal cycles 1272

4. Physiologic induction of nest building behavior 1274

B. Egg-laying 1276

1. Egg-laying behavior in birds 1276

2. Hormonal relations in ovulation

and egg-laying 1277

3. Stimulation of ovulation 1278

C. Incubation 1284

1. Incubation patterns 1284

2. Hormonal regulation of incuba tion 1284

3. Interaction between internal and

external environments in the regulation of incubation behavior 1294

4. Some remarks on the onset of incu bation 1297

D. Care of the Young 1298

1. Types of young and methods of

feeding them 1298

2. Hormonal induction of parental be havior toward .young 1299

3. Induction of parental behavior to ward young by external stimuli 1300

4. Physiologic nonidentity of incuba tion behavior and brood}' care of

the young ' 1302

III. Hormones and Parental Behavior in

Infrahuman Mammals 1304

A. Nest-building 1305

1. Nest-building patterns in mam mals 1305

2. Hormonal basis of nest-building. 1305

3. Induction of nest-building behav ior by external stimuli 1309

B. Behavior during Parturition 1310

1268


1. Patterns of parturitive behavior. 1310

2. Physiologic aspects of parturitive

behavior 1312

C. Retrieving of the Young 1313

1. Retrieving behavior 1313

2. Physiologic regulation of retriev ing behavior 1314

]). Nursing and Suckling Behavior 1321

1. Behavior of the nursing mother. . 1321

2. Milk ejection 1321

3. Mother-young relationships and

the regulation of lactation 1325

4. Nursing behavior and the condi tion of the mammary gland 1330

IV. General Discussion: the PsychobioloGY OF Parental Behavior and the Role of Hormones 1332

A. Learning and Hormone-induced Pa rental Behavior 1332

1. General: formulation of the prob lems 1332

2. Learning and parental behavior . 1332

B. Hormone Secretion as a "Behavioral"

Response 1341

1. Neural conti'ol of hormone secre tion 1341

2. Hormone secretion as a reflex. . . . 1342

3. Hormone secretion as a condi tioned response 1343

4. Parental behavior and reflexly in duced hormone secretion 1343

C. Mechanisms of Hormonal Action on

Behavior 1344

1. Formulation of the problem 1344

2. Examples of peripheral contribu tions to hormonal effects on behavior 1345

3. Central hormonal effects on behav ior 1348

4. The importance of behavioral anal ysis 1351

D. Genetic and Evolutionary Aspects of

Hormone-induced Parental Behavior 1352


PARENTAL BEHAVIOR


1269


1. Taxonomic diftVitMifes in parental

behavior and in the mechanisms underlying it 1352

2. Strain differences and genetic factors 1354

E. The Role of Parental Behavior in the

Development of the Young 1355

1. In birds 1355

2. In mammals 1357

V. Scientific Names ok Animals Mentioned IN Text 1359

A. Birds 1359

B. Mammals 1360

VI. References 1360

I. Introduction

Almost all species of birds and mammals exhibit special behavior patterns the function of which is to warm, feed, protect, or otherwise foster the development of their eggs and/or young. Although these behavior patterns vary widely in form, physiologic organization, ontogenetic origin, and degree of psychologic complexity, it is nevertheless sometimes convenient to group them together under the rubric of "parental behavior." Such behavior is of course appropriate to, and ordinarily occurs only at, the stage of the reproductive cycle when there are eggs or young present or impending. Its regulation is, therefore, in part, a function of the reproductive cycle, and it is the purpose of this chapter to discuss the relationships between the (endocrine) reproductive cycle and the occurrence and organization of parental behavior.

Decisions about what should be included in such a discussion are not easy to make, because what we call parental behavior" is not always as clearly differentiated within the animal's repertoire of behavior patterns as it is in our own conceptions. For example, mice of almost any age, either sex, and any physiologic condition may do a certain amount of nest-building, which is, to the observer, only quantitatively different from the more intense nest-building of the preparturient animal. Should a detailed discussion of such behavior necessarily be included in a chapter on "parental behavior"? The nest-building of most species of birds is associated with the period of maximal sexual activity, and in some cases is incorporated into the courtship pattern. How do we, for purposes of a book like this, draw a shari) line between "sexual behavior" and


"parental behavior"? It is obvious that such decisions must sometimes be more or less arbitrary.

For the purpose of this discussion, "parental behavior" will include nest-building and behavior toward eggs and young, ending with the time at which the young are able to obtain food independently of their parents.

It is perhaps inevitable that detailed physiologic experimentation should be for the most part limited to a few species of animals which are cheap and easy to breed in the laboratory, like rats, mice, and guinea pigs; or economically important, like domestic chickens ; or similar to human beings, like monkeys and chimpanzees. This concentration of analytic work on a relatively few species has the effect of partially concealing from view the enormous diversity of behavioral and physiologic patterns that characterize the adaptation of animals to their environment. The diversity of behavior in different species, and of the physiologic mechanisms underlying the behavior, may be just as great as is their diversity of form. This is not the appropriate place for an exhaustive survey of the varieties of parental behavior found in nature, but it may help to put the available work on hormonal regulation of such behavior into perspective if we from time to time briefly indicate the types which can be found, and point out that they are by no means limited to those characteristic of domestic and laboratory animals.

II. Hormones and Parental Behavior in Birds

A. NEST-BUILDING

1. Varieties of Nest-biiilding

Structure and location. Each species of bird has its characteristic method of providing a place for the deposition and incubation of the eggs, and the variability of nest construction within species is quite small. Between species, however, there are very wide variations. Some species build only above the ground (American robin, Herrick, 1911) or over water (tricolored red-winged blackbird, Emlen, 1941), some build only on the ground (herring gull,


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HORMONAL REGULATION OF BEHAVIOR


Tinbergen, 1953) , in burrows that they make in the ground (bank swallow, Petersen, 1955) , or in natural cavities (purple martin, Allen and Nice, 1952). The pied-billed grebe builds a semifloating nest on the water (Glover, 1953) . The Baltimore oriole builds an elaborate covered woven nest of grasses (Herrick, 1911), the Florida jay a woven open cup (Amadon, 1944b), the storm petrel a simple scrape with a few scraps of material laid in it (Davis, 1957) , the black guillemot no nest at all, merely holding the egg on top of the webs of its feet (Storer, 1952). Swifts use their own saliva as cementing material, or in some species as almost the sole building material (Lack, 1956a). Various species of megapodes, instead of building nests, build large mounds of vegetable material which creates the incubation temperature when it rots (Fleay, 1937; Frith, 1956b). Most birds build individual nests, but some species build communal nests in which several birds lay (smooth-billed ani, Davis, 1940a) , or massive woven communal structures within which each pair has a separate chamber (sociable weaverbird, Friedmann, 1930).

Share of the sexes in building. Male and female may share in nest-building, either approximately equally, as in house sparrows (Daanje, 1941), Florida jays (Amadon, 1944b), and great crested grebes (Simmons, 1955a), or in a A-ariety of special ways. In a number of species, the male is more active in nest-building at first, with the female doing more of it later on (e.g., red-backed shrike, Kramer, 1950; herring gull, Paludan, 1951; cliff swallows, Emlen, 1954; blackheaded gull, Ytreberg, 1956). A frequently occurring special case is one in which the male builds the nest, and the female merely adds the lining (house wren, Kendeigh, 1941 ; graceful warbler, Simmons, 1954; coot, Kornowski, 1957) . In the green heron, the male at first selects the nest site, and does all of the gathering, carrying, and weaving of twigs into the nest. He does not permit the female to enter the nest until some time after he has taken up his territory. Once he has allowed her to enter the nest, however, he does most of the gathering and carrying of twigs, and the female does most of the building (Meyerriecks, 1960) .


The male may build the nest with little or no help from the female, as in the redshank (Grosskopf, 1958), the rook (Marshall and Coombs, 1957) , and many species of weaver finches (Friedmann, 1949). In the zebra finch (Morris, 1954), and the bronze mannikin (both of them weaver finches) (Morris, 1957), the male builds the covered nest, and the female shapes the inside by sitting in it and making appropriate turning movements. In most species of megapodes, it is the males alone that construct the large mounds in which the eggs are to be laid (Coles, 1937, Frith, 1956b).

An interesting variation of male nestbuilding is one in which the male builds several nests and the female selects one of them as the repository of the eggs. This occurs in several species of wrens, in which the nests are built by the male before the arrival of the female in the spring, and in which the female may line the nest she selects (long-billed marsh wren, Weller, 1935; house wren, Kendeigh, 1941 ; European wren, Armstrong, 1955). The male Carolina wren builds several such nests, but when the female arrives, both may build a new nest for the eggs (Kendeigh, 1941 ; Nice and Thomas, 1948). A similar pattern is found in many waders, in which the male makes several nests (mere scrapes in the sand) in the presence of the female, during courtship, and the female lays eggs in one of them (ringed plover, Laven, 1940a; lapwing, Laven, 1941).

Building by the unassisted female is far more common than building by the male alone. When the nest is built entirely by the female, the role of the male may vary greatly. In some species, the male and female associate only for the purposes of courtship and copulation, and nest-building and rearing of the young are done elsewhere entirely by the female (Gould's manakin. Chapman, 1935; boat-tailed grackle, McIlhenny, 1937; bower birds, Marshall, 1954; blackcock and rufi", Selous, quoted by Armstrong, 1947) . When the male and female associate on a territory during the breeding season, the role of the male may vary from complete indifference to the nest-building activities of the female (ovenbird, Hann, 1937), through merely accompanying her


PARENTAL BEHAVIOR


1271


on her trips when she collects material (great tit, Hinde, 1952; bullfinch, Nicolai, 1956) to collecting material, but not building (pied-billed grebe, Glover, 1953; Clark nutcracker, Mewaldt, 1956). Observers of some species have noted that the males show all the elements of the nest-building behavior in their courtship or other behavior, without ever integrating them into effective building (great reed warbler, Kluyver, 1955). Schantz (1937) observed a nest built by a male song sparrow, a species in which the nest is ordinarily built entirely by the female (Nice, 1943).

In some species of birds, the male may play an important part in the selection of the site, even when he does not participate in nest-building (Hinde, 1952; Haartman, 1957).

2. Correlations between Nest-building and Other Behavior

xA.s a first step in gaining some insight into the relationship between nest-building behavior and the reproductive cycle, let us consider how the occurrence of nest-building is related to other behavioral aspects of the cycle.

Copulation and nest-building. In a number of species, it has been reported that nestbuilding begins at about the time when the female becomes sexually receptive. The female snow bunting, after being vigorously courted by the male over a 2 to 3 week period, permits copulation for the first time on the same day on which she first picks up and carries nesting material (Tinbergen, 1939b). The female ruffed grouse, too, becomes sexually receptive the day she begins to build a nest (Allen, 1934) . In both species, the nest is built entirely by the female. Nestbuilding and copulation may also begin at the same time in species in which both sexes build (house sparrow, Daanje, 1941; cedar waxwing, Putnam, 1949; gulls, Paludan, 1951; Brewer's blackbird, Williams, 1952).

Many observers have noted that, in various species of birds, copulation is limited to the nest-building period, which comes to an end before the eggs are laid (tricolored redwinged blackbird, Emlen, 1941; purple martin, Allen and Nice, 1952) . This implies that the eggs, some of which may be ovu


lated 8 or 10 days after the last copulation, must be fertilized by spermatozoa held in the oviduct for at least that time. Elder and Weller (1954) found that domestic mallard ducks could lay fertile eggs up to 17 days after being isolated from drakes, and Riddle and Behre (1921) report female ring doves laying fertile eggs after up to 8 days of isolation. Domestic hens may lay fertile eggs after 20 or more days of isolation (Hartman, 1939) .

It will be recalled that the male house wren builds several nests before the arrival of the female in spring, and that the female finishes one of them some time after her arrival. In this species, copulation is limited to the period of female nest-building (Kendeigh, 1941). In the cliff swallow, another species in which the male does a substantial amount of nest-building before the pair is established in spring, copulation between members of the pair is not seen until the nest is well under way (the mechanics of copulation in this species are such that it cannot be performed at the nest-site vmless there is a partially built nest there) . However, promiscuous copulations not involving the members of the forming pair may be seen earlier, at the places where mud is being gathered for the nests (Emlen, 1954).

Female white-crowned sparrows seem to start building a few days before the first copulations are observed (Blanchard, 1941). In domestic canaries, the peak of copulatory activity is normally slightly later than that of nest-building activity. However, if the partially built nest is removed each day, so that no nest accumulates in the nestbowl, the peaks of copulation and of nestbuilding activity occur at the same time. This indicates that the peak of copulation usually occurs later than that of nest-building behavior only because the presence of the nest inhibits nest-building activity (Hinde, 1958).

Various elements of the nest-building behavior, such as the billing or carrying of nesting material, are sometimes observed as part of courtship activity early in the season (Noble, Wurm and Schmidt, 1938; Armstrong, 1947) .

Most of the correlations discussed in the foregoing paragraphs are derived from field


1272


HORMONAL REGULATION OF BEHAVIOR


observations, which vary widely with respect to the continuity of observation, number of birds observed, distribution of observations during the day and during the cycle, etc. There is nevertheless a strong impression that, in many species of birds, the physiologic conditions encouraging copulation {i.e., sexual receptivity of the female) are the same as those inducing nestbuilding.

Nest-building not correlated with copulation. There are some significant exceptions to this general impression. The female rook usually does not permit copulation until after the nest has been built by the male (Marshall and Coombs, 1957) . In the European coot, another species in which the nest is built by the male, copulation is also delayed until after the main shell of the nest is built (Kornowski, 1957) . In these cases it may be suggested that the nest-building activity of the male may play some role in stimulating those physiologic changes in the female which induce sexual receptivity (see below, p. 1275.

Nest-building during incubation. Cases in which nest-building continues into the incubation period are for the most part of two general types, (a) There are some species in which the main part of the nest is completed before any eggs are laid, and in which the lining of the nest (with a material different from that used for the main construction) may continue during incubation (Cape weaver, Skead, 1947; graceful warbler, Simmons, 1954; bank swallow, Petersen, 1955). This suggests that, in such species, the selection of the different materials may have different hormonal bases, a suggestion for which there is some experimental evidence (see below, p. 1274). (b) Many species of gulls, terns, and shorebirds continue to build up the nest during the incubation period by virtue of a tendency to pick up nesting materials and drop or incorporate them in the nest whenever the birds' need to sit on the eggs is frustrated, or in conflict with some other behavioral tendency. Such nestbuilding has been called "displacement nestbuilding" (Tinbergen, 1952). It may occur, for example, when the bird is sitting on eggs abnormal in shape, size, or number (Moynihan, 1955; Baggerman, Baerends, Heikens


and ]\Iook, 1956), or when the members of the pair relieve each other at the nest {e.g., Cuthbert, 1954; Ytreberg, 1956). Baerends (1959) found that such displacement nestbuilding by a sitting bird also occurs when the temperature of the eggs departs too much from an optimal level.

3. Nest-building and Gonadal Cycles

So far, we have established a probable temporal relationship between nest-building and copulation, at least in those species in which the female participates in nest-building. As a further step in the analysis of the cyclic basis of nest-building behavior, we may now look into the relationship between the timing of nest-building activity and of the maximal activity of the ovarian follicle. In the absence of very much direct evidence on this point, let us adopt the somewhat roundabout procedure of considering, first, the timing of follicle growth, and then the timing of nest-building activity, in the cycle.

Relation of follicle growth to time of egglaying (see chapter by van Tienhoven). The ovary of a bird at the egg-laying stage looks like a cluster of ova of varying size, the largest being the one that is nearest to being ovulated. If these ova are measured at the autopsy of a laying bird, the measurements form a graded series, which can be arranged in order, from most mature to least mature. If the interval between successive eggs is known for the species, and if the time of last ovulation is known for the individual, it is a simple matter to calculate the age (in days before ovulation) of each of the larger ova. The size of the ova can then be plotted as a function of pre-ovulatory age. In addition, the growth rate at each day before ovulation can be calculated by comparing the sizes of successive ova, the growth rate between day a and day b being a function of the increase in size of the ovum between day a and day b, in relation to the absolute size on day a (Romanoff, 1943).

In a wide variety of species of birds which have been studied, there is a sharp increase in follicle growth rate starting from 4 to 11 days pre-ovulation, depending on the species (Romanoff and Romanoff, 1949). Romanoff (1943) has shown that the actual


PARENTAL BEHAVIOR


1273


growth rates, and the changes in growth rates, are identical in a number of species.

Riddle (1916) found that the rate of growth of the ovum of the domestic hen increased quite suddenly by a factor of about 25, some 5 to 8 days before ovulation (cf. Stieve, 1919; ^Yarren and Conrad, 1939; Marza and Marza, 1935) . In seasonal breeding birds (including most wild birds) the picture is basically the same. The ovary remains in a regressed state during the offseason; ova increase in size slowly during the early part of the breeding season, then very rapidly during the few days before ovulation. Bissonnette and Zujko (1936) found that the size of the largest ovum of the female starling increases very slowly for about 108 days (from December to March), and then very rapidly for about 26 days. During the 108-day period of slow growth, the growth rate remains stable at about 0.009 mm. per day; it then increases quite suddenly to 0.285 mm. per day, an increase of about 31.6 times.

The 26-day period of rapid growth found by Bissonnette and Zujko is based on the average sizes of ova from many different birds, which may have been at slightly different stages of the cycle, although collected on the same days. When the sizes of the various ova in individual ovaries are plotted as a function of serial position, in birds that are already ovulating, it becomes apparent that the period of final rapid growth in any one ovum is about 10 to 11 days.

Riddle (1911) and Bartelmez (1912) rel^orted that the growth rate of ova in the domestic pigeon increases sharply (by 8 to 20 times) starting 5 to 8 days before ovulation {cf. Cuthbert, 1945). Stieve (19191 found that the volume of the largest ovum of the female jackdaw, after having remained quite constant during the months before the breeding season, increases from 24 cu. mm. to 1600 cu. mm. during the last 5 days before ovulation.

Paludan (1951) observed that the ova of two species of gull, observed in the wild, grew most rapidly during the last 9 to 10 days before ovulation.

It is clear that the characteristic pattern of growth of the avian follicle is that of a long period of slow, steady growth followed


by the sudden onset of a short period of extremely rapid growth which ends only when the ovum is ovulated. This final period of rapid growth lasts from about 4 to about 11 days, depending on the species.

Relation of nest-building behavior to time of egg-laying. In most species of wild birds, nest-building appears to be sharply limited to a few days during the cycle. Female ruffed grouse begin to build about 6 days before the first egg (Allen, 1934) . Tricolored red-winged blackbirds (Emlen, 1941) and song sparrows (Nice, 1937) start about 4 to 5 days before the first egg. Similar patterns are found in other species of passerine birds (e.g., Clark nutcracker, Mewaldt, 1956; snow bunting, Tinbergen, 1939b).

The usual description of this type of relationship in the literature of field ornithology merely states that nest-building takes place during the few days before the first egg. When more exact quantitative observations are made, however, the situation seems somewhat more complex. Hinde (1958) weighed the amount of nesting material built into the nest on each day of the cycle in a number of female domestic canaries. He found that the intensity of nest-building activity reached a peak some time before the laying of the first egg, and then waned. The timing of the peak was subject to considerable variation, ranging in different individuals from 7 to days before the first egg. Field observations on the cedar waxwing by Putnam (1949) show a similar pattern. In this species nest-building activity reached a peak 2 or 3 days before the laying of the first egg.

In some species the first egg appears, not immediately on the completion of the nest, but after an interval of several days following the last nest-building activity (purple martin, Allen and Nice, 1952; white-crowned sparrow, Blanchard, 1941 ; ovenbird, Hann, 1937; shrike, Miller, 1931). No information is available concerning possible differences in pre-ovulation changes in the ovary between species having the two different patterns.

Data on nest-building behavior and gonadal condition. The data so far presented clearly suggest that nest-building behavior is often associated with the period of maxi


1274


HORMONAL REGULATION OF BEHAVIOR


mal follicle growth. In a few cases, observations of follicle growth and of nest-building behavior have been made on the same species, and have usually led to the conclusion that this association does in fact exist. Emlen (1941, tricolored red-winged blackbird), Paludan (1951, herring gull), Petersen (1955, bank swallow), and Marshall and Coombs (1957, rook) have all noted that the period of nest-building coincides with that of maximal follicle growth. Mr. S. Glucksberg, in an unpublished study, destroyed the nests of several pairs of ring doves at the end of each day, and made daily counts of the number of pieces of nesting material built into the nest. He found that the amount of nest-building activity increased with increasing follicle size, reaching a peak at the time of ovulation. Similar observations have been made by Clausen (1959) on the homing pigeon.

Unfortunately, there are not yet any data on nest-building and male gonadal cycles to compare with those available for the relationship of this behavior to the female cycle. It is clear that the nest-building activity of seasonal breeding birds in which the male participates in building usually occurs during the part of the year when testicular secretory activity is at its height (Marshall and Coombs, 1957), but no observations have been made on detailed changes in testicular activity, correlated with detailed observations on behavior.

4. Physiologic Induction of Nest-building Behavior

The foregoing discussion makes it plain that, in the large number of species in which the female does most or all of the nestbuilding, nest-building behavior is associated with the final period of maximal follicle activity. We may now examine evidence bearing more or less directly on the problem of the hormonal induction of nestbuilding behavior. This evidence may be divided into two general categories: the induction of nest-building behavior by direct injection of hormones; and the elicitation of nest-building behavior by external stimuli.

Hormonal induction of nest-huilding behavior. The coincidence of nest-building behavior and the period of rapid follicle


growth just preceding egg laying strongly suggests that nest-building behavior is induced by ovarian hormones. We have gone into such detail about these and other coincidences because very little direct experimental evidence is available, but what evidence there is confirms the impression that ovarian hormones often provide the physiologic background for nest-building behavior.

Lehrman ( 1958b) reported that the injection of 0.4 mg. diethylstilbestrol daily over a 7-day period induces nest-building behavior in ring doves. Hinde and Warren (1959) indicate that the injection of estrogenic hormone into female canaries also induces nestbuilding behavior, but only in near-lethal doses. Hinde's observations on the nestbuilding behavior of canaries (1958) indicate that these birds change over from the use of grass to the use of feathers (which is the nest lining) shortly before egg-laying is due. This change-over occurs to some extent even though the stimulus situation in the cage remains the same (the nest is removed daily so that the birds cannot be stimulated by a completed nest) . This suggests that the change from the use of grass to the use of feathers is controlled in part by a change in hormonal condition, although such a change has not yet been induced by means of hormone administration. The suggestion is particularly interesting in view of the facts that, in some species of birds, the building of the main part of the nest stops abruptly with the beginning of egglaying, but the addition of a lining of different material may continue thereafter, and that in still other species, the male may l)uild the main part of the nest, whereas the female merely adds the lining (see above, page 1270.

Cole and Hutt (1953) studying a number of nonlaying hens, found on autopsy that some of them had ovulated, failing to lay because of interrupted oviducts, impacted oviducts, etc. Others had not ovulated. The ovulators among the nonlayers were seen to enter nests on about 47 per cent of the observed days (about the same percentage as in the case of normal laying hens) . Nonovulators entered the nests in only 5 per cent of the cases. This indicates that the be


PARENTAL BEHAVIOR


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havior toward the nest is influenced by hormones associated with ovidation, even in those birds in which the egg could not be l)roduced because of abnormalities in the oviduct.

Progesterone has not yet been shown to induce nest-building behavior in birds. Warren and Hinde (1959) found that this hormone had no effect upon nest-building in the domestic canary, either alone or in combination with estrogen.

In view of the correlation between nestl)uilding behavior, on the one hand, and, on the other hand, follicle growth, oviduct growth (Petersen, 1955) , and the readiness of the female to copulate, it is interesting to note that estrogenic hormone induces oviduct development in various birds (Brant and Nalbandov, 1956; Lehrman and Brody, 1957; see chapter by van Tienhoven), and female sex behavior in the domestic chicken (Adams and Herrick, 1955).

Although it is reasonably certain that estrogenic hormone is the principle physiologic initiator of nest-building in those typical species in which the female does most or all of the nest-building, the situation is most unclear in those cases in which the male participates. Although we have noted in our laboratory that nest-building can be induced in ring doves by estrogen injection, and not by testosterone (see above), we do not yet have adequate observational evidence concerning the specific effects of estrogen injections on the male and on the female. This evidence, when it is available, will be important and interesting, because in these birds the male typically brings the nesting material to the nest, and the female builds it into the nest (Goodwin, 1955). In the brush turkey, the male builds a large mound by scraping leaves, mold, soil, etc., backwards wdth his feet. The female later lays the eggs in holes burrowed into this mound, and they are incubated by heat generated by decaying leaves and mold. The male's head and neck are almost featherless, and covered with a red skin. This skin becomes brilliant red in each breeding season, a few days before the beginning of mound-building. This suggests, of course, that in this case male sex hormone is involved in nest-building activity. How


ever, during the period of most intense mound-building activity, the male does not allow the female near the area, which suggests further problems about the relationship between male sex behavior, moundbuilding, and the hormonal bases thereof (Fleay, 1937). In the black-crowned night heron both the male and the female normally participate in nest-building, incubation, and the rearing of the young. Noble and Wurm (1940) found that testosterone propionate would induce nest-building behavior in both males and females, whereas estrogenic hormones had no effect on the nest-building behavior of either sex. Further, they found that the change in color of the bills (yellowish to black) and legs (yellowish to rich pink), which normally occurs in both sexes at the beginning of the breeding season in the spring, can be induced in the off-season by injection of testosterone propionate, but not by estrogenic hormones. The hormonal background of nest-building behavior in this case is different from that of the species in which the female alone builds the nest, but it is also different from the situation in the ring dove, in which both sexes take part in building.

These cases indicate the complexity of patterns and mechanisms involved, and are only a sample of the considerable variety of unsolved problems posed by the nest-building behavior of many species of wild birds, problems which are only hinted at in the work so far done on domesticated birds.

Induction of nest-building by external stimnli. In species in which the female builds the nest unassisted (and this includes most of the species for which useful information is available), it seems that stimuli provided from the environment, including stimuli coming from the behavior of the male, may induce the hormonal changes which lead to the onset of nest-building. Howard (1920) described the typical breeding pattern of many species of songbirds, in which the male arrives first on the spring migration, and has his territory established by the time the female arrives some time later. The male appears to be ready to court and eager to copulate as soon as the female arrives, but the female at first does not permit copulation. There is a period of some


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days or weeks during which the courtship attempts of the male end in "sexual flights" during which the male chases the female through the territory in a characteristically zig-zag flight path, at the end of which contact is abruptly broken off. Only after a period of such flights is the female ready to copulate. Tinbergen (1939b) reported that the female snow bunting begins to build a nest (and to copulate) after about three weeks of this type of courtship stimulation by the male. Captive female chaffinches build nests and lay eggs more readily when the}^ are stimulated by males (Marler, 1956). Vaugien (1948), working with serins, and Polikarpova (19401, working with house sparrows, found that females placed in cages without males would build no nests, whereas the presence of a male bird in a cage stimulated the females to build. Male and female herring gulls both build, but the female seems to become stimulated to take a greater part in nest-building by the activities of the male, who is more active at the beginning (Paludan, 1951).

Lehrman (19o8a) reported that, when a jiair of ring doves which have had previous breeding experience are placed together in a breeding cage with an empty nest bowl and a supply of nesting material, nest-building occurs after a 1- to 3-day period of courtship. If a male and female are kept for several days in a cage containing no nest bowl and no nesting material, they will be ready to start building a nest immediately after the subsequent introduction of nesting material into the cage. If both birds have been pretreated with estrogen before being introduced into the cage (see above), the nest-building starts immediately, rather than after a preliminary period of courtship (Lehrman, 1958b). This suggests that participation in courtship may have brought the birds into nest-building condition because it stimulates the secretion of estrogen. This is confirmed by Lehrman, Brody and Wortis (1961), who found that the oviduct of the female ringdove increases in weight about 5-fold, solely as the result of association with a male for 7 days. Significant increases in oviduct weight can be seen after less than 48 hours of stimulation by the courting male.


Warren and Hinde (1960) found that the presence of the male domestic canary speeds up the development of nest-building behavior in the female in spring, when nestbuilding is presumably induced by endogenous estrogen. On the other hand, the l)resence of males has no effect upon nestbuilding behavior induced by estrogen injection in the winter. This undoubtedly means that the stimulation of nest-building behavior by the presence of the male is, at least in part, by way of the stimulation of estrogen secretion.

Lack (1956b) noted that the male and female members of a pair of swifts (which keep the same mates year after year) may arrive at the nesting place on different days, but that nest-building does not start until the second member of the pair arrives from the south, even though the two members of the pair collect and use the material independently of each other. Many field observers have noted that the songs and postures of male birds may stimulate nest-building behavior on the part of the female, but it is not always certain in these cases whether what is at issue is the stimulation of a hormonal change by the behavior of the male, or the stimulation of a behavioral response of which the female is capable as a result of hormonal changes which have already taken place. There is no doubt that both of these effects occur (Blanchard, 1941; Armstrong, 1955).

Other external factors, such as the occurrence of rainy seasons for tropical birds (Bullough 1951), the presence of suitable nesting sites (Lack, 1933; Marler, 1956), etc., seem to stimulate the onset of nestbuilding behavior.

B. EGG-LAYING

1. Egg-laying Behavior in Birds

The typical egg-laying pattern of the domestic hen, in which eggs are laid on several consecutive days, there is a gap of one or more days, and egg-laying is then resumed, and in which such clutches occur repeatedly during much of the year, is by no means typical of the egg-laying behavior of most species of birds. In fact, there occurs among wild birds just as great a vari


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cty of egg-laying patterns, and therefore of relevant endocrine situations, as we noted in the case of nest-building.

Size of clutch. Birds typically lay a clutch consisting of a definite number of eggs, and then incubate the eggs until they hatch. Some species of birds produce only one such clutch per year; others may breed twice, or even three times a year, but with the breeding always restricted to a definite part of the year. In the temperate zones breeding is always in the spring and summer; in the tropics some species may breed during the wet season, others during the dry season, and in a few cases breeding may be all year round.

The number of eggs constituting a clutch varies from species to species within wide limits. Some birds, such as the large penguins, most auks and murres, petrels, and some others lay only 1 egg. Some birds, such as most species of pigeons and doves, characteristically lay 2 eggs. Most gulls lay and incubate 3-egg clutches. Most songbirds lay from 4 to 7 eggs. Large clutches, rather variable in size, are laid by ducks and geese, and gallinaceous birds such as partridges, pheasants, etc., may lay up to 20 eggs in a clutch. The domestic chicken is, of course, derived by selection from ancestral birds of the latter type (Mayaud, 1950).

Laying pattern. In those species in which the clutch consists of more than one egg, the interval between eggs is subject to wide interspecific variation (Mayaud, 1950). Data on the exact time of egg-laying are not as generally available for wild birds, of course, as they are for domestic birds, but certain wild birds, such as some species of ducks, appear to have a pattern like that of the domestic hen — they lay eggs at intervals of 20 to 24 hours. Most pigeons lay their 2 eggs about 40 hours apart (Whitman, 1919) . Although the most common pattern appears to be for the birds to lay their eggs on successive days, there are species in which the interval is much longer such as the blackheaded gull, in which the interval is about 42 hours (Weidmann, 1956), some boobies, in which the interval may be 6 or 7 days (Mayaud, 1950) , and many others.

Brood parasitism. An unusually interest


ing jihenomenon which poses several unusual endocrinologic problems is the occurrence of brood jiarasitism in several families of birds. Parasitic birds do not build nests of their own, nor do they incubate their eggs. Instead, the female lays her eggs in the nests of other (host") species, and the hosts incubate the eggs and rear the young. This type of breeding habit appears to have evolved independently in several different families of birds. Of the 200 species of the order Cuculiformes, some 80 are to some degree jiarasitic (Makatsch, 1937) , including all 40 of the species of cuckoos living in the old world (Southern, 1954). Parasitism has also evolved among the cowbirds, a subfamily of blackbirds living in the new world (Friedmann, 1929), and in the honey guides of Africa (Friedmann, 1955). In addition, individuals of many other species of several families, especially ducks, quail, and pheasants, may breed parasitically more or less frequently (Weller, 1959).

i. Hormonal Relations in Ovulation and Egg-laying

This is not the place for a detailed discussion of the hormonal basis of ovulation and egg-laying, since these matters are extensively discussed in the chapter by van Tienhoven. However, a brief summary will serve as an introduction to certain problems concerning the regulation of egg-laying behavior.

The ovarian follicle grows under the influence of a gonadotrophic hormone from the pituitary gland, which is presumably similar to mammalian follicle-stimulating hormone (FSH). The growing follicle secretes estrogenic hormone, which in turn stimulates growth of the oviduct. When the follicle has reached ovulatory size, an ovulation-inducing hormone, presumably similar to luteinizing hormone (LH), induces the release of the egg. Traps <1955) suggests that progesterone (or a progestin) from the ovary induces the secretion of the ovulation-inducing hormone by the pituitary gland (Rothchild and Fraps, 1949). Progesterone has been found in the blood plasma of laying hens (Fraps, Hooker and Forbes, 1948; Layne, Common, Maw and Fraps, 1957; Lytle and Lorenz, 1958), non


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HORMONAL REGULATION OF BEHAVIOR


laying hens, and cocks (Fraps, Hooker and Forbes, 1949), but not in that of capons. In addition, progesterone induces the formation of secretion products by the albumen-secreting glands in the oviduct, the growth of which has been accomplished under the previous influence of estrogen (Brant and Nalbandov, 1956j. It thus seems probable that there is a short episode of progestin secretion by the ovary, just preceding ovulation, and that this follows a period of estrogen secretion. (See chapter by van Tienhoven.)

The actual laying of the egg appears to involve some posterior pituitary activity. Injection of posterior pituitary preparation induces the laying, within 2 to 25 minutes, of eggs already ovulated, but which would not normally have been laid for up to 20 hours (Burrows and Byerly, 1940, 1942). When the neurohypophysis is removed no oviposition takes place until after there has been time for the regeneration of the nerve connection between the hypothalamus and the pituitary gland (Shirley and Nalbandov, 1956a, b). Rothchild and Fraps (1944) removed the ruptured follicles and all the rapidly growing preovulatory follicles in hens, so that an ovulated egg was in the oviduct, but no more eggs could be ovulated. They then placed some of these hens in normally lighted rooms, others in rooms on reversed light cycles. The majority of eggs in both groups were laid during the daylight hours. They therefore concluded that a light-sensitive, nonovarian process was involved in the laying process, in addition to those factors controlling ovulation itself. (See chapter by van Tienhoven.)

3. Stimulation of Ovulation

Our interest in the nature of the conditions stimulating ovulation derives from the fact already pointed out, that nest-building activity is in part based on physiologic conditions induced by hormones coming from the developing egg follicle; and from the further fact that the physiologic events associated with ovulation somehow set the stage for the occurrence of incubation behavior, which normally follows egg-laying.

Neural stimulation of ovulation. It has become abundantly clear in recent vears


that the activity of the pituitary gland is controlled and influenced in considerable detail by the hypothalamus (Harris, 1955; see chapters by Greep, Everett, and van Tienhoven). The physiologic and anatomic details of the relationship between the hypothalamus and the pituitary gland are adecjuately discussed in these other chapters, and do not concern us here. We may, however, describe a striking example of the evidence for neural control of pituitary activity. Huston and Nalbandov (1953) sewed a loop of thread into the magnum of the oviducts of a group of domestic hens, and tied it into place, so that it provided a constant mechanical stimulation of the oviduct wall. Domestic hens normally ovulate 30 to 60 minutes after the laying of the previous egg. During the 25 days following the operation, however, 58 to 75 per cent of the operated birds laid no eggs. Among the operated birds which did lay eggs, the mean number of eggs laid was 1.5 per bird; in sham-operated birds wdth no loop sewed into the oviducts, the number of eggs laid was 5.5 ])er bird. LH or progesterone injection could induce ovulation at any time in those birds which were not laying because of the ]:)resence of the thread. The ova of the experimental birds did not degenerate, and their oviducts and combs remained normal. These data suggest that the mechanical stimulation of the oviduct wall inhibits LH secretion by the pituitary gland, without substantially interfering with the secretion of FSH. Huston and Nalbandov suggest that the jiresence of an egg in the oviduct acts in this way to prevent the ovulation of the succeeding egg until after the previous egg has been laid.

External stimuli and ovulation. Since the secretion of gonadotrophic hormones can be influenced and controlled by the hypothalamus, and by stimuli arising in the body outside of the central nervous system, it is reasonable to expect that external stimuli representing various environmental situations and events may have an influence, through this neurohypophyseal link, on the activity of the ovary.

(a) Light has long been known to influence gonadal activity. In seasonally reproducing birds, the increasing length of the


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day i^^ the most important factor which ensures that the reproductive system will be active in the spring. In addition, experimental work with domesticated birds indicates that the timing of ovulation and oviposition during the day are influenced by the day-night light cycle (Farner, 1955; see chapter by van Tienhoven). In addition, there is considerable evidence that other environmental variables, such as those related to temperature, food supply, and so on, play a significant role as regulators of the breeding season (Thomson, 1950; Marshall, 1959).

(b) Stimuli provided by the courting male apparently influence the secretion of gonadotrophic hormones by female birds. It will be recalled that, in our discussion of the hormonal basis of nest-building behavior, we pointed out that nest-building behavior is sometimes induced in the female as a result of stimulation by the courting male, and that there is reason to believe that the basis for this effect is that the courtship of the male stimulates the secretion of estrogenic hormones in the female. We may now examine some further evidence of the effect of stimuli provided by the mate upon the growth and ovulation of the egg. Bartelmez (1912) noted that the ovary of an unmated female domestic pigeon contains follicles which do not exceed 5.5 mm. in diameter. When such a pigeon is lilaced with a male, she lays an egg after about 8 days (Harper, 1904). The growth of the ovum to the ovulation size of about 20 mm. is clearly caused by stimuli provided by the male. Craig (1911, 1913) kept several pairs of doves so that the males and females could see each other from adjoining cages. The males were allowed in the cages of the females daily, but were prevented from copulating by the experimenter, who separatefl them with a wand at appropriate times. All of these females laid eggs within 9 days of the beginning of contact with the male, although, when these birds w^ere kept in isolation for a year preceding the beginning of the experiment, 5 out of the 6 females had laid no eggs at all. Matthews (19391 showed that the short period of tactual contact between male and female which Craig had allowed was not necessary for the


stimulation of ovulation. He showed that a female domestic pigeon would lay eggs as a result of seeing a male court her through a glass plate. We have found the same result in my laboratory, using ring doves. Both Matthews and Harper noted that, when two females are placed in a cage together, both may be stimulated to lay eggs. However, Collias (1950) found that ring doves in heterosexual groups laid more eggs than those in unisexual groups of the same size, indicating that the behavior of male doves is more stimulating to the secretion of gonadotrophins in females than is the pseudomale behavior which some of the female doves will adopt when no males are in the group.

Polikarpova (1940) placed 50 female house sparrows in cages in which they received additional illumination daily, starting in the late fall. Twenty-five of them had males in the cages, the other 25 were alone. After about 50 days, none of the isolated females had started to build a nest, and of 17 such birds killed for autopsy, only 3 showed enlarged oviducts. On the other hand, all the females with males in their cages had nests, and 5 out of 8 birds examined had fully developed oviducts. Burger (1942, 1949) kept female starlings in groups of various sizes, with or without males. He found that, when he provided additional illumination to such females either isolated or in groups, their ova were stimulated to grow to about 3 mm. When groups of males and females were caged together, the ova grew rather larger (5 mm.). When a single male and a single female were caged together, the ova of the female grew to about 10 mm. This indicates that the stimulus for the growth of the ovum is not merely the presence of a male, but probably also the presence of conditions which facilitate the formation of a pairing relationship normal for the species. When Lack ( 1940, 1941) caged two pairs of robins or chaffinches in one aviary, the dominant pair bred normally, the subordinate pair did not. In such birds, the full expression of normal male courtship behavior toward the female requires that the male be the territory holder, which in turn means that he must be the dominant bird, or the only male, in a con


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HORMONAL REGULATION OF BEHAVIOR


siderable space. Vaiigicn ( 1948) found that single female serins in individual cages would not lay eggs, but that eggs would be laid within a few days if a male was placed in a cage with the female. In the case of the shell parakeet, Vaugien (1951) showed that the sounds made by other birds influenced the growth of the oviduct. When female parakeets were kept isolated in small dark boxes of various sizes, they laid no eggs. When the box was placed inside an aviary containing a breeding pair (so that the experimental bird could hear, but not see the breeding birds) about half of the experimental birds laid eggs within 12 days. When the remaining birds were sacrificed for autopsy some 3 weeks later, they had enlarged oviducts, with the largest ova averaging 9 mm. in diameter. Controls kept out of hearing of breeding birds laid no eggs and, on autopsy, were found to have ova no larger than 1.5 mm. in diameter. Ficken, van Tienhoven, Ficken and Sibley (1959) verified this effect on ovarian activity of sounds made by other individuals in parakeet flocks, and also reported that testis development was stimulated. Marshall (1952, 1954) described the mating behavior of bower birds, in which the male has a special display ground, where he builds a bower and displays to the female. This display stimulates the female to go off and build her nest and rear her young alone.

It is clear from the above data that stimuli provided by the courting male induce the secretion of gonadotrophic hormones by the female, and that this is possibly a source of the synchronization of the sexual cycles of male and female birds during the breeding season.

(c) The presence of an appropriate nesting site and the availability of nesting material seem to be important factors in the conditions stimulating normal gonadotrophin secretion during the breeding season in birds. Lack (1933) observed three colonies of arctic terns at three different locations near a lake. The first location was permanently dry ; the second was water-logged for a short period in the spring, because of melting snows; the third was water-logged for a longer period, until a marshy area dried up. Although birds were present from


the beginning of the season in all three of these locations, the birds in the first colony laid their eggs earliest, those in the third colony latest. Similar observations were made by Linsdale (1938), who found that the yellow-headed blackbird, which builds its nest only over water, will abandon the nest in midbuilding if the water dries up while the nest is being built, and will then build a new nest elsewhere, this involving a delay in ovulation. However, if the eggs are laid first, so that incubation is in progress when the water dries up, the birds stay on. It can thus be stated that the presence of ai)propriate nesting conditions facilitates ovulation, and thus presumably the secretion of gonadoti'oi)hic hormones by the pituitary gland.

The induction of ovulation by the availability of nesting material has been shown experimentally in several species of birds. Like some other tropical species (Roberts, 1937; Bullough, 1951) , the red-billed weaver finch of central Africa breeds at irregular times, always following rainfall. Marshall and Disney (1957) showed that the stimulating factor following the rainfall is actually the availability of nesting material. During the dry season, when no reproduction was taking place in free-living birds of the species, Marshall and Disney kept groups of male and female red-billed weavers in four outdoor cages variously provided with combinations of the following: insect food, artificial "rain" from a sprinkler, dry grass of the type normally used by the birds as nesting material, and green grass of the same type. Birds having green nesting grass available built nests, regardless of whether "rain" was falling, and regardless of whether insect food was available. Furthermore, the only females to lay eggs during the experimental period were those in the cages in which the males were building nests. Clearly, manipulation of nesting material by the males induced in the females hormonal changes leading to ovulation. Marshall and Disney also noted that the bills of the females kept with such males assumed breeding color earlier than did other females. This change in color is, of course, under hormonal control (Witschi, 1938).


PARENTAL BEHAVIOR


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Whitman (1919) found that various species of doves and pigeons would not ovuhite unless nesting material and nesting locations were provided. Lehrman, Brody and Wortis (1961) found that the presence of nesting material plays a significant role in the stinmlation of ovulation. Female ring doves kept with males in cages not sui)plied with a nest bowl or nesting material will not ovulate as soon or in as high a percentage of the cases as will such females kept in cages with males and an ade(luate supply of nesting material (the incidence of ovulations after 6 days in the cage is 55 per cent without nesting material, 95 l)er cent with nesting material) . Differences in oviduct weight (and in frequency of ovulation) between the groups of birds with and without nesting material in the cage do not become apparent until some 5 or 6 days after the birds are placed in the cages, although, as reported above, increases in oviduct weight as a result of association or nonassociation with a male are to be seen within less than 48 hours. Since male doves collect most of the nesting material, while the females build most of it into the nest, and since no oviduct development is stimulated by nesting material in the absence of the male, it seems likely that the courtship behavior of the male ring dove which is not yet interested in nesting material causes estrogen secretion {i.e., FSH secretion by the pituitary gland of the female), whereas nesting material (or the behavior of the male which has nesting material available) later facilitates the secretion of progesterone (I.e., LH secretion by the female's pituitary gland). We may recall that progesterone induces both the final ovulatory pulse of LH from the hypophysis, and the histologic changes in the oviduct which occur after the albumen-secreting glands have been formed under the influence of estrogen.

From the above data, it is clear that in some species in which the male participates in nest-building, the presence of nesting material and/or the change in behavior of the male which is made possible by the presence of nesting material, helps to stimulate ovulation in the female. There is some evidence that, in those cases in which the female does most or all of the building, ovulation may


also depend to some extent on stimuli provided by the nesting material and/or by participation in nest-building. Polikarpova (1940) starting on January 1st kept 11 female house sparrows in cages supplied with a nest box and nesting material, while 10 females were kept in cages with neither nest box nor nesting material. On April 28th, when birds caught in the wild had fully developed oviducts and eggs ready to ovulate, 10 of the 11 birds with nesting material had enlarged oviducts with a fully formed shell gland, whereas none of the 10 birds without nesting material had advanced beyond the first stage of oviduct enlargement. Vaugien (1948) removed the nest from the cage of female serins while it was being built or just after it was built, and reported that this prevented the birds from laying eggs. When he later replaced nests in the cage, eggs were laid within a few days. Berry (1943, 1944) found that geese of several different species could be induced to lay eggs by the provision of artificial nests, although some of these birds had been in the park for years without laying. Hinde and Warren (1959) found that the absence of nesting material and a nest bowl delay ovulation in domesticated canaries.

The presence of a nest and/or nesting material clearly facilitates ovulation, at least in some species of birds. Further, the effect of the presence of nesting material is, at least in some cases, quantitatively or qualitatively different from the effects of stimuli provided by the courtship of the male.

(d) A special, and most interesting problem is posed by the egg-laying of brood parasites such as the cuckoos and cowbirds. How is the egg-laying behavior of such birds synchronized with the availability of host nests? Although there are some exceptions (Kabat, Buss and Meyer, 1948; Davis, 1958), most birds do not normally lay eggs unless they have first built a nest. Although, as we shall see later, the laying of eggs involves hormonal changes which facilitate the subsequent occurrence of incubation behavior, the brood parasites lay eggs without having built a nest, and without incubating the eggs afterwards.

Hann (1937, 1941) states that the female cowbird first finds the nest by seeing the


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HORMONAL REGULATION OF BEHAVIOR


host building it. She watches intently and for long periods during the nest-building. She visits the nest regularly in the absence of the owners before laying. Hann suggests that the development of the eggs, and their ovulation, in the cowbird are stimulated by the sight of the potential host building a nest, and that this accounts for the synchronization of the laying of the cowbird's and of the host's eggs (note that the parasite's eggs must be laid at a time when a host is prepared to incubate them). According to Hann's observations, the cowbird's egg is laid some 4 to 5 days after she first begins watching, so that his hypothesis about stimulation of ovulation is plausible. However, observation of the behavior of cowbirds (Nice 1949), as well as histologic studies of their ovaries (Davis, 1942a I, indicate that the cowbird's eggs are laid in clutches of 3 to 5 eggs, with a rest period of some 5 to 8 days between clutches. This suggests a possibility that the cowbird, when such a clutch is growing, must find a nest, and that it finds a series of host nests because it is about to lay the eggs, rather than laying the eggs because it has found the host nests. However, a series of studies by Chance (1940) on the European cuckoo indicates very strongly that a brood parasite may actually be stimulated to lay eggs by the availability of host nests. Chance induced cuckoos to lay abnormally long series of eggs (on the order of 20 to 25) by removing eggs from the nests of foster species {i.e., potential hosts) so that they built new nests and relaid. He thus managed the situation so that potential host nests were available to the cuckoo over a much longer period of time than that during which the cuckoo normally lays eggs, and during which it normally has hosts available. By this method, he induced cuckoos which normally lay 5 to 7 eggs to lay 20 to 25.

The anis are a New AVorld subfamily of cuckoo-like birds, closely related to the parasitic cuckoos. Although not themselves, for the most part, brood parasitic, their breeding habits are peculiar in that some of the species nest in communal nests, several females laying in one nest. In some species only a few of the females will incubate, even though many more have laid the eggs. Davis


(1940, 1942b) reported that these birds may lay their eggs on the ground, even quite far from the nest. Such eggs, of course, are not incubated. He also found that ovulation may be stimulated by the presence or activity of other birds. In several flocks, he noted that no egg-laying might take place for a long time, and that a sudden burst of egg-laying activity would occur after a new female joined the flock. Davis suggested that the breakdown of the normally rigid relationships between nest-building, egglaying, and incubation, and the ability of these birds to lay eggs in response to visual and/or auditory stimulation by other birds, regardless of whether they have built a nest and regardless of whether they will incubate, may be features of their reproductive cycle which encourage the development of brood parasitism.

Effect of eggs in the nest on ovulation. In nature each species of bird lays a characteristic number of eggs in a clutch, the variation within species sometimes being extremely narrow. In some cases the number of eggs laid is independent of the presence of other eggs in the nest. In other cases the number of eggs laid may be considerably extended by removing eggs as they are laid, the bird continuing to lay until the number of eggs present in the nest is approximately the normal clutch size. The term "determinate layer" is commonly used for those species in which the number of eggs laid is rather rigidly determined by physiologic relationships internal to the bird, whereas the term "indeterminate layer" is used for those species in which the size of the clutch may vary according to the situation in the nest (Cole, 1917; Laven, 1940b; Lack, 1947; Davis, 1955) . Among the domestic birds, the pigeon is a familiar example of a determinate layer, whereas the domestic hen is, of course, an indeterminate layer. Among wild birds, too, there are variations from species to species. For example, the lapwing (Klomp, 1951), and some songbirds (Davis, 1955) seem to be determinate layers, attempts to increase the size of the clutch by removing eggs as laid having been unsuccessful. On the other hand, female house sparrows have been reported to lay up to 50 eggs in regular succession when the eggs


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^vere removed daily (Pearl, 1912; Witschi, 1935), and a flicker from whose nest an egg was removed daily, starting with the 2nd egg, laid 72 eggs in 73 days (Phillips, 1887). The wryneck has similarly been reported to lay up to 48 eggs under the same conditions (quoted by Pearl, 1912). Goodwin (1948) reported that the golden pheasant may lay clutches of up to 40 eggs if eggs are removed as laid.

The best experimental work on indeterminate egg-laying has been done with gulls, which normally lay 3 eggs, at intervals of about 2 days (Goethe, 1937; Tinbergen, 1953). In the case of the black-headed gull, the average time between the laying of the 1st and the 3rd eggs is about 84 hours {ZV2 days) (Weidmann, 1956). The experiments of Weidmann on the black-headed gull may be summarized as follows (see also Ytreberg. 1956):

If the 1st egg is removed just after it is laid, the birds will lay a 4th egg, so that they end up with a 3-egg clutch. In these cases the 4th egg is laid at a normal interval after the 3rd. If successive eggs are removed as they are laid, most birds will lay more than 4 eggs, Weidmann having found birds laying up to 7 eggs. If the 1st egg is left in the nest, and subsequent eggs are removed as they are laid, no birds lay more than 3 eggs. If both eggs are removed after the 2nd <egg is laid, some of the birds will lay a 4th legg, others will stop at the 3rd egg and incubate it, although it is now the only egg in the nest. If the birds are allowed to lay 3 eggs, and the whole clutch is removed immediately after the laying of the 3rd egg, all birds desert, none laying a 4th egg.

In seeking to account for these results, it is important to note that gulls begin incubating with the laying of the 1st egg (Tinbergen, 1953; Weidmann, 1956). Weidmann suggested that no additional eggs are laid if the birds incubate, even though they are incubating an incomplete clutch. Since many birds will lay a 4th egg if the eggs are removed after the laying of the 2nd egg (when the birds have been incubating for about 2 days) , but will lay no 4th egg if the eggs are removed after the laying of the 3rd egg (when the birds have been incubating for about 4 days), Weidmann's suggestion


is that, in these birds, about 4 days of brooding will suppress the production of further eggs. Paludan's (1951) results on the herring gull are in general similar to those of Weidmann. When birds were killed for autopsy after the laying of the 1st egg, a 4th, and sometimes a 5th follicle were found maturing in the ovary ; but when the l)ird was not killed until after it had been incubating for 2 or 3 days these follicles were found degenerating.

If Weidmann is correct in suggesting that participation in incubation provides stimulation which suppresses the production of further eggs, we might expect to find that the addition of eggs to the nest before laying has started would suppress the laying of some or all of the clutch, and that this effect would be found only when the birds start to incubate them before they lay. There is some evidence that these assumptions are indeed true, although they have not yet been thoroughly exi)lored. Poulsen (1953b) found that, although he could not induce domestic pigeons to increase the size of the clutch beyond the normal 2 eggs by removing the 1st egg immediately after it was laid, he could suppress egg-laying altogether in about 50 per cent of the birds by placing 2 eggs in the finished, empty nest, whereui:)on all the birds immediately began to incubate. We have obtained similar results with the ring dove. Although barn swallows, American magpies (Davis, 1955), and tricolored redwinged blackbirds (Emlen, 1941) do not lay more eggs as a result of having the eggs removed as they are laid, there is some evidence that the addition of eggs near the beginning of egg-laying may inhibit the production of eggs. It may be pointed out that these birds normally do not incubate until after the entire clutch is laid.

It is apparent that stimuli provided by the egg, in all probability through the act of incubation, have, in many species, the ability to change the pattern of pituitary secretion in such a manner that the inhibition or suppression of the full maturation of some of the follicles is brought about. We shall reserve discussion of the nature of the stimulus and of the effect for our analysis of the physiologic basis of incubation behavior (see below, page 1295),


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HORMONAL REGULATION OF BEHAVIOR


C. INCUBATION

The eggs of birds are fertilized internally, and then laid within a few hours after fertilization. The development of the embryos within the eggs requires temperatures higher than normal environmental temperatures, and this temperature is, in almost all birds, provided by the body of the parent or parents. The parents provide warmth for the eggs by sitting on them in such a way that the eggs are brought into contact with a featherless area or areas on the ventral side of the body. The behavior of the bird in sitting on its eggs is called "incubation" or "incubation behavior," and it is the purpose of this section to discuss the physiologic bases, and the physiologic consequences, of incubation behavior.

1. Incubation Patterns

As in the case of the other types of behavior with which we are dealing, there is an extraordinary interspecific diversity in the patterns of incubation behavior to be found in nature. The roles of the parents, the pattern of attentiveness to the egg, the duration of incubation, etc., show the widest variation. The types of incubation behavior found in nature have been summarized by Kendeigh (1952), and by Skutch (1957), and the following abbreviated summary is adapted from their accounts.

In many species of birds, including most song birds, the female alone does all of the incubation. In most such cases, the incubating bird leaves the nest several or many times each day in order to feed, although there are birds, like some pheasants (Goodwin, 1948; Delacour, 1951 ) , which sit on the eggs for the entire incubation period, without taking any food. Female hornbills also sit on the eggs continuously, but they are fed by the male while doing so. There are some species in which the male does all of the incubation. In phalaropes, unlike most sexually dimorphic birds, the female is more l)rightly colored than the male, and the role of the sexes in sexual and parental behavior is reversed from the usual pattern: the female defends the territory and the male does all of the incubation, brooding, and caring for the young (Tinbergen, 1935). The male


emperor penguin sits on the eggs continuously for as long as two months, without taking any food (Stonehouse, 1953; Rivolier, 1956).

There are many groujxs of birds in which both parents share in the incubation activities. These include birds like gulls (Tinbergen, 1953) in which the male and female change places several times during the day, and birds like the Adelie penguin (Sladen, 1953) in which the males and females change places at intervals of several days. The male and female short-tailed shearwater change places on the eggs every 11 to 14 days (Marshall and Serventy, 1956). In pigeons and doves (Whitman, 1919) the female sits on the eggs from late afternoon through the night to midmorning, while the male sits for one long session (about 6 hours) during the day.

£. Horinonal Regulation of Incubation

It i.'^ obvious tliat the diversity of patterns of incul)ation behavior found among the various species of birds must depend on a considerable diversity of physiologic mechanisms. As usual, however, our information about these mechanisms is limited to relatively few species.

Relation of onset of incubation to time OF EGG-LAYING. Since the pattern of endocrine secretion changes so rapidly during the ])eriod of egg-laying, we may, as a first step in the analysis of the hormonal basis of incubation behavior, examine the relationship between egg-laying and the onset of incubation behavior in seasonal-breeding bii'ds. This temporal relationship should suggest the identity of the hormone or hormones which underlie the onset of incubation behavior.

The ornithological literature reveals wide variation from species to species with respect to the time when incubation starts. Some birds, such as the snow bunting (Tinbergen, 1939b) and the cedar waxwing (Lea, 1942) do not begin sitting on the eggs until after the last egg is laid. A much more common pattern is for incubation to start just before the laying of the last egg (blackcapped chickadee, Odum, 1941 ; shrikes, Miller, 1931 ; wliite-crowned sparrow, Blanchard, 1941; bullfinf^h. Nicolai, 1956; and


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many others). In other cases, incubation may start earlier, when only half the clutch has been laid (northern phalarope, Tinbergen, 1935; blackbird, Messmer and Mcssmer, 1956; yellow-headed blackbird, Fautin, 1941; etc.). Still other species are reported to begin incubating from the laying of the first egg. This is usually reported for water-birds in which both sexes share in incubation, such as gulls (Tinbergen, 1953; Barth, 1955; Ytreberg, 1956), terns (Hardy, 1957), herons (Verwey, 1930; Allen and Mangels, 1940), plovers (Rittinghaus, 1956), etc. There are, however, also occasional reports of songbirds in which incubation begins with the laying of the 1st egg {e.g., Amadon, 1944b; Simmons, 1954).

Field observers report that birds sometimes sit on the nest as if incubating, even before any eggs have been laid (Roberts, 1940; Simmons, 1955b; von Pfeffer-Hiilsemann, 1955) . This cannot be regarded as reliable evidence of incubation behavior before egg-laying, because the behavior of such l)irds may lack several important components on true incubation behavior (Simmons, 1955b) .The great crested grebe, for example, when sitting on an empty nest-platform before the eggs appear, does not fluff out the feathers on the ventral side of the body as does a sitting bird, nor does it show the characteristic settling-down movement (Simmons, 1955b). The male European jay often sits in the nest during nest-building, although in this species only the female sits on the eggs (Goodwin, 1951). There are, however, reliable experimental demonstrations of incubation behavior before egg-laying in gulls and pigeons. Tinbergen (1953) and Ytreberg (1956) have found that herring gulls and black-headed gulls will sit on eggs placed in the nest shortly before the laying of the bird's own eggs. Poulsen ( 1953 » placed 2 eggs in the finished nest of each of 10 pairs of pigeons which had not yet started to lay. All the birds immediately began to incubate. Lehrman (1958a) found that, when pairs of ring doves were placed in cages containing a nest bowl and nesting material, and tested 7 days later, all of the birds were ready to sit on eggs, although most of them had not yet laid eggs of theii- own.


The foregoing paragraphs undoubtedly give the impression that there are sharp, well defined, easily observed interspecific differences in the time of onset of incubation behavior, and that it is quite easy to tell when incubation behavior starts. Unfortunately, such is far from being the case. There are extraordinary difficulties in the way of determining when incul)ation behavior actually starts, and these difficulties have the effect of merging and blurring the distinctions which sometimes seem so easy on the basis of casual field observation (Heinroth, 1922; Nice, 1954). The onset of incubation behavior is often not abrupt, but quite gradual. For example Gurr (1954) reports that the blackbird begins to incubate with the 1st egg, but the proportion of time during which the bird is on the egg increases from about 7 per cent to about 90 per cent during the egg-laying period, with an increment on each day. Kendeigh (1952) studied the incubation behavior of the house wren by means of a device which recorded temperature changes of the eggs, so that he had records of the time actually spent warming the eggs. He showed that the number of periods during which the bird sits on the eggs increases gradually and progressively from about 10 on the first day of egg-laying to about 35 on the last day of the laying of the 5- or 6-egg clutch.

Even when the bird is reported to be sitting from the 1st egg, and where observation seems to indicate that the bird is in fact attending to the egg, analysis of the actual incubation period of the egg frequently reveals that the so-called "incubation" occurring during the early stages of egg-laying is actually not providing much heat for the eggs. Barth (1955) found that, although the 2nd egg of the common gull is laid, on the average, 46 hours after the first, and the 3rd egg 47 hours after the second, the 2nd egg hatches only 4 hours after the first, and the 3rd egg only 21 hours later, indicating that, although the birds are seen to be incubating from the 1st egg, incubation is probably not very effective until the last egg is laid. Similarly, Paludan (1951) found that the 3rd eggs of clutches of herring gulls contained embryos larger than 2nd eggs of the same age, and that embryos in 1st egs-s (again of


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HORMONAL REGULATION OF BEHAVIOR


the same age) were even smaller. This indicates that the 3rd egg laid has been incubated more effectively, presumably because effective incubation of the last egg of the clutch begins immediately, whereas the earlier eggs are not incubated with complete effectiveness until some days after they are laid. Holstein (quoted by Swanberg, 1950) found that the eggs of a European goshawk which he observed to begin incubating with the 1st egg, all hatched within 48 hours, although 9 days had elapsed between the laying of the 1st and last egg of the clutch.

The problem arises whether the relative ineffectiveness of observed incubation early in egg-laying is based on inadequate behavioral response of the birds to the eggs, or on inadequate temperature exchange between egg and adequately responding bird. I have already indicated that incubation behavior occurring early in egg-laying may be quantitatively very slight compared with that during the incubation period. There is, however, some evidence that, even when birds do sit on the eggs early during the egg-laying period, they may not actually transmit heat to them (Ryves, 1943a, b). Swanberg (1950) reported that, in several species, birds sitting on the eggs early during the egg-laying period do not actually warm the eggs, even though they may be sitting so tightly that it is rather difficult to frighten them away. Arnold (quoted by Swanberg, 1950) observed that blue jays sitting on the eggs early during the egg-laying period had the feathers of the ventral body surface between the body and the eggs, rather than being erected as in a normally incubating bird, so that the naked ventral skin could be applied to the eggs. It is apparent that the important problem of the basis for the ineffectiveness of incubation during the egglaying period is far from solved, but that the observational data at hand provide an adequate background for defining the problem for experimental attack.

We may summarize by saying that incubation behavior develops gradually during the egg-laying period, appearing at different rates and at different times in different species of birds. In spite of the interspecific differences, there is clearly some relationship between the hormonal changes associ


ated with egg-laying, and the onset of incubation behavior.

Onset of incubation behavior in the MALE. It is not unexpected that the onset of incubation behavior in female birds is related to the production of eggs, and presumably is regulated, in part, by the hormonal changes associated with ovulation and egg-laying. But what of those cases in which the male takes part in incubation? Is the onset of readiness to incubate in his case related to the time of production of eggs by the female? The situation is somewhat variable from species to species: in some cases the male begins to sit with the 1st egg (night heron, Noble, Wurm, and Schmidt, 1938; turnstone, Bergman, 1946; Kentish plover, Rittinghaus, 1956; etc.) ; in other cases the female begins to sit during the egg-laying period, with the male not incubating until some time later (common tern. Palmer, 1941; lapwing, Laven, 1941). In species in whicii the male does all of the incubating, it is variously reported that the male begins to incubate from the first egg (jacana, Hoffmann, 1949), or that he may not begin to incubate until some of the eggs have already been laid (northern phalarope, Tinbergen, 1935). These field observations are subject to the reservations which we noted above: "incubation" is poorly defined, and quantitative data about the development of the behavior arc usually lacking.

Noble, Wurm and Schmidt (1938) reported that male night herons will sit on eggs that are placed in the nest before the female has laid, and that the male does all of the incubating during the first few days. Poulsen (1953) found that both male and female pigeons would sit on eggs offered to them after the nest had been built, but before any eggs had been laid, and we have verified this in the ring dove. Lehrman, Brody and Wortis (1961) found that when a pair of ring doves is placed in a breeding cage with a nest bowl and nesting material, readiness to incubate develops gradually during the 6 to 9 day period before eggs are laid, and that this readiness develops earlier in males than in females.

It is obvious that available data on the development of incubation behavior in male birds are quite inadequate. However, they


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justify the impression that readiness to incubate by the male (in those species in which the male participates in incubation) is more or less synchronized with the laying of eggs by the female, although, understandably, not as closely synchronized as is the case with the incubation behavior of the female.

The incubation patch, (l) Structure and function. When a bird sits on its eggs, it erects the contour feathers on the lower ventral body surface, exposing an unfeathered area of skin which in the nonsitting bird is normally covered by the contour feathers lying flat along the body surface (Simmons, 1955b; Barth, 1955). This naked area, called the incubation patch, is applied to the surface of the eggs, and is the source of the heat which is exchanged between the body of the parent and the egg. Bailey (1952) has provided a detailed description of the incubation patch, which is not merely a nonfeathered area, but one in which there is a characteristic increase in dermal and subdermal vascularity, accompanied by edema and by a thickening of the smooth muscle layer of the dermal blood vessels (Petersen, 1955). The vascularity and edema are readily apparent to the naked eye: the skin of the incubation patch appears distinctly reddish, thickened, and is sometimes thrown into loose folds.

The area covered by the incubation patch corresponds to the ventral apterium. (The contour feathers of birds grow in definite tracts called pterylae; between these pterylae are areas called apteria, in which grow only down feathers, or in some cases no feathers at all.) The distribution and shape of the incubation patches in the various orders of birds correspond with the distribution and shape of their respective ventral apteria. Thus songbirds typically have a single ventral patch. Gulls and shorebirds have paired patches lateral to the midline of the body, sometimes accompanied by a small median patch. No incubation patches are found in the pelican-like birds, or in the ducks and their relatives.

The behavior of incubating birds suggests that contact between the ventral apterium and the eggs plays an important role. When starting to sit the bird makes side-to


side settling movements which suggest to the observer that it is adjusting the contact between the eggs and ventral body surface. The contour feathers remain erected until these settling movements subside, when the feathers are relaxed around the sides of the eggs. When Weller (1958) removed one of the eggs of a nighthawk, the bird, on returning to its eggs, poked with its bill at the incubation patch where the egg should have been, and failed to settle for a considerable time. Gulls have three incubation patches, and the eggs are moved in the nest by the settling motions of the bird and by poking with its bill until each egg is in contact with one of the incubation patches. By observing the under-surface of incubating blackheaded gulls from a trench dug under the nest. Beer (1961) found that the settling movements continue until each egg is firmly in contact with one of the patches.

{£) Incidence. In almost all cases, the occurrence of incubation patches in the male or in the female of a given species corresponds to the occurrence of incubation behavior. In most species of songbirds only the female incubates, and in almost all cases the incubation patch is found only in the female (Miller, 1931; Price, 1936; Davis, 1941; Dixon, 1949; Putnam, 1949; Brackbill, 1958; and others). In species in which only the male incubates, such as the tinamous (Pearson and Pearson 1955), phalaropes, and jacanas (Bailey, 1952) an incubation patch is seen only in the male. In many groups of birds, both the male and the female participate in incubation, and in these cases, both sexes have an incubation patch. This includes woodpeckers (Howell, 1952), petrels (FLsher, 1952), gulls (Johnston, 1956), and a number of other families (Bailey, 1952).

The coincidence between tiie occurrence of the incubation patch and of incubation behavior can be followed out in considerable detail. According to Holstein (quoted by Wingstrand, 1943), the male European goshawk has a poorly developed incubation patch, and takes part to only a slight extent in incubation. In the Clark nutcracker, in which the male and female both incubate the eggs (Mewaldt, 1956), unlike most members of its family in which only the fe


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HORMONAL REGULATION OF BEHAVIOR


male incubates (Araadon, 1944a j, both male and female have incubation patches, again unlike most members of the family (Bailey, 1952). Johnston (1956) collected a number of California gulls in the field in May and June when the breeding birds had eggs. All the adult birds that he collected had incubation patches. Of 13 subadult (3-year-old) males, which can be recognized by their plumage, 8 had incubation patches. This is about the same proportion as the proportion of subadult males that breed. Among subadult /e//iaies,which do not breed, no incubation patches were found.

Skutch (1957) points out that there are exceptions to the general trend, in that males of some species have been found to sit on the eggs, although they have no incubation patch. In most of these cases, data are lacking with respect to the details both of the behavior of the male bird and of the temperature of the eggs, so that it is not possible to say whether such birds are actually incubating. A partial exception is the bank swallow, in which Petersen (1955), by measuring the temperature with the bulb of the thermometer placed among the eggs, showed that the egg temperature in one nest rose substantially when the male entered the nest-burrow in the absence of the female. The male in this species has no incubation patch. Since these birds nest in deep burrows in the ground, no details are available about the behavior of the male bird. This observation of a single individual should, of course, be regarded with some caution. Kendeigh (1952) using a thermocouple in nests of the barn swallow and the purple martin, two species closely related to the bank swallow observed by Petersen, found that, although the male often came and stood over the eggs in the nest, the temperature was elevated only when the female was sitting.

In spite of the occasional exceptions, the pattern is generally consistent, and indicates that the physiological conditions giving rise to the formation of the incubation patch may illuminate the background of incubation behavior itself.

(3) Development. In several species of song birds the development of the incubation patch may be divided into the fol


lowing four stages (Bailey, 1952): (a) Defeatherization: the down feathers of the incubation patch area are molted several days before the first egg is laid, (b) Vascularization: the blood vessels of the area begin to increase in size and in number immediately after defeatherization. The vascularization is complete by the time the last egg is laid and incubation begins, (c) Edema: during incubation, the incubation patch continues to become more vascular and edematous. This edematous stage continues throughout incubation and during the period when the newly hatched young are brooded by the parent, (d) Recovery: the vascularity and edema in the dermis begin to subside gradually, starting when the young are about 4 or 5 days old.

Petersen (1955) weighed the skin of the ventral apterium in a number of bank swallows collected during the breeding season. Before egg-laying began, the average weight of the ventral apterium in both males and females was about 93 mg. This weight stayed the same in the males throughout the breeding season. In the females the weight began to increase just before egg-laying, reaching a maximal average weight of about 280 mg. during incubation. We may recall that this is the species in which egg temperatures were found to increase when a male was in the nest.

Some observers have stated that the incubation patch develops a week or so before the laying of the first egg (Nice, 1937; Brackbill, 1958), or that it persists through the summer until the fall molt (Odum, 1941). However, except for those by Bailey and Petersen, the observations on the incubation patch have lacked histologic verification. It is quite probable that observers reporting different time-relationships between the development of the incubation patch and of the ovary are merely referring to the loss of feathers, rather than to the development of vascularity and edema.

(4) Hormonal basis. Bailey (1952) studied the hormonal induction of the incubation patch in several species of sparrows and finches. He found that testosterone propionate, administered as pellets, had no effect on the development of the incubation patch. Hypophysectomized birds treated


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with estradiol pellets developed full vascularity within 6 to 11 days, although none of them showed either edema or defeatherization. Prolactin (luteotrophic hormone, LTH) injected daily into intact or into hypophysectomized Inrds had no effect on the \'entral apterium. However, when hyjiophysectomized birds wliose ventral apteria had become vascular as a result of treatment with estradiol were treated with prolactin, the apteria became defeathered and edematous within 3 to 4 days. When intact birds were treated with estradiol pellets, a normal l)rood patch, vascular and edematous, developed within 9 or 10 days. These data indicate not only that the brood patch is formed under the successive influence of estrogen (during egg-laying) and prolactin ( during incubation ) , but that, in these species at least, estrogenic hormone is capable of stimulating release of prolactin from the pituitary gland. An important point is that the effects of the hormones on the ventral apterium were the same in males and in females, although in these species an incubation patch is normally developed only by the female.

Pituitary hormones and incubation behavior. (1) The incidence of endogenous prolactin during the reproductive cycle seems to be closely associated with the occurrence of incubation behavior. Lienhart (1927) found that serum from incubating domestic hens, injected into nonincubating birds, could induce them to sit on eggs. Serum from nonincubating females was not capable of inducing incubation in other birds. This was, I think, the earliest demonstration that the blood of incubating birds contains a factor capable of inducing incubation, and that this factor is not present in the blood of nonincubating birds.

The prolactin content of any tissue or preparation is usually assayed in terms of its effect upon the crop w^all of pigeons or doves. The inactive crop wall of these birds is a thin, almost transparent sheet, consisting largely of a thin sheet of muscle with an ^nner epithelium. During incul)ation, the wall of the crop thickens and becomes vascular and opaque, largely because of the greatly increased rate of cell division in the epithelium, which becomes many layers


thick, with growth of blood vessels into the subjacent connective tissue. Toward the end of the incubation period, the superficial layers of the lining epithelium desquamate into the lumen, and the resulting cheesy mass of degenerating epithelial cells forms the food substance which is eventually regurgitated to the young (Beams and Meyer, 1931). This proliferation of the crop-sac epithelium is induced solely by prolactin, acting locally (Riddle, 1937; Riddle and Bates, 1939). The standard (Riddle's) method of assaying prolactin, which is used in defining the international unit, depends on the increase in the crop-weight of birds of a standard strain, when the material to be assayed is injected over a period of days (weight method). Other methods depend on the fact that, when a small amount of prolactin is injected intradermally over the crop, a small area of vascularization develops, which can be seen with the naked eye (local response methods) (Reece and Turner, 1936; Lyons, 1937; Riddle and Bates, 1939L

Burrows and Byerly (1936) removed the pituitary glands from domestic fowl and assayed them for prolactin content by Lyons' (local response) method. Considering the amount of prolactin in the pituitary glands of roosters as a unit-standard (1.00), they found that the pituitaries of laying hens contained on the average 1.46 units, and those of incubating hens 4.05 units. Saeki and Tanabe (1955) found that the pituitary glands of laying hens contained, on the average, 0.071 LU. of prolactin, whereas those of incubating hens contained 0.196 LU. (Saeki and Tanabe, 1954). Nakajo and Tanaka (1956) found that the prolactin content of the caudal lobe of the anterior pituitary gland was 0.8 ReeceTurner units in nonincubating domestic hens, and that it rose in incubating birds to 1.7 to 2.4 Reece-Turner units. They also found that wdien incubation was interrupted by continuous lighting of the cages, the level of prolactin in the pituitary gland fell. Breitenbach and Meyer (1959) obtained similar results in the ring-necked ]iheasant: the prolactin content of the pituitary gland rose sharply while the birds incubated eggs. Byerly and Burrows (1936)


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HORMONAL REGULATION OF BEHAVIOR


measured the prolactin content of the pituitary gland of laying hens in their second laying year, which had been judged genetically broody or nonbroody on the basis of whether they became broody during their first laying year. They found twice as much prolactin in the pituitary glands of the broody type as in those of the nonbroody type.

The growth of the crop of pigeons and doves during the incubation period is, of course, a priori evidence of increased prolactin production. Schooley and Riddle (1938) assayed the prolactin content of the pituitary glands of pigeons, their unit being the increase in crop weight of the host pigeon per milligram of implanted pituitary tissue. They found sexually active adult birds to have 0.14 units of prolactin per pituitary gland, whereas birds in midincubation had 2.50 units. Lahr and Riddle (1938) found a much higher rate of mitosis in the crop epithelium of incubating and of prolactin-injected pigeons than in that of nonincubating pigeons. The pituitary glands of female pigeons contain more prolactin than those of male pigeons (Hurst, Meites and Turner, 1943; Meites and Turner, 1947). Male and female doves both incubate, but the female spends three times as much time on the eggs as the male (Whitman, 1919).

Bailey (1952) assayed the prolactin content of the pituitary glands of California gulls by implanting them over the crops of domestic pigeons. He found that gulls which had brood patches when they were collected (both males and females) had more prolactin in their pituitary glands than those with no incubation patches.

A further indication of the occurrence of prolactin during incubation in birds other than domestic pigeons and chickens is provided by the fact that molting stops during incubation in canaries (as in other birds), and that prolactin inhibits molting when injected during other times of the reproductive cycle (Kobayashi, 1953b).

(2) Injection of prolactin induces incubation behavior in laying domestic hens of broody strains. Riddle, Bates and Lahr (1935) injected prolactin daily into 20 laying hens of broody races. Although clucking


followed by incubation behavior normally occurs only at or near the end of the egglaying period, all 20 began clucking within 2 to 4 days after the beginning of the injection, except for one bird which clucked on the 1st day, and 1 which did not begin until the 7th day. Sixteen of the 20 birds began sitting on eggs within less than 3 days after the beginning of clucking. When 10 laying hens of a nonbroody race (white Leghorn) were treated in the same way, 7 of the birds began clucking after 3 to 5 days, but only 1 of the 7 incubated on the following day. (Note that up to 15 per cent of broody hens are found in populations of nonbroody" races.) When prolactin was injected into nonlaying hens, most began clucking after a few days, but none was induced to incubate. The efficacy of prolactin in inducing incubation behavior in the domestic hen has been verified by other investigators (Eigemann, 1937; Riddle, 1937; Nalbandov and Card, 1945; Saeki and Tanabe, 1955).

^Ir. Philijj Brody and I have tested ring doves iin which both sexes normally incubate) for incubation behavior after injection of various amounts of prolactin. If each bird is injected over a 7-day period with a total of approximately 400 I.U. of prolactin, and the birds are then tested for their response to eggs in individual pairs, each in a single test cage, incubation behavior is seen in approximately 40 per cent of the pairs. In these birds, maximal crop-growth has occurred in response to the prolactin injections (increase in crop weight from ca. 900 mg. to ca. 3000 mg.). When the total amount of prolactin is reduced to 50 I.U., the number of birds in which incubation behavior is induced drops to about 20 per cent. Even with this dosage, however, the lowest we have yet tried, there is a 60 per cent increase in crop weight. Since, in a normal cycle, the birds begin to sit on the eggs some days hejore there has been any detectable increase in crop weight, these data do not indicate that prolactin plays a role in the onset of incubation behavior in this species. Dr. R. A. Hinde of Cambridge University informs me that, in experiments carried out with Dr. R. P. Warren, he failed to induce canaries of either sex to


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8it on eggs as a result of prolactin injection. These experiments with ring doves and with canaries were carried out with nonlaying birds and are being continued.

Attempts to induce incubation behavior by prolactin injection in male birds of species in which the male does not normally sit have not been successful. When roosters or capons are injected with prolactin, and then offered eggs, they do not sit, although, in most cases, they utter the clucking sounds characteristic of a hen in the process of becoming broody (Riddle, Bates, and Lahr, 1935;-Eigemann, 1937; Nalbandov, 1945; Nalbandov and Card, 1945; Saeki and Tanabe, 1955).

The fact that male domestic chickens do not incubate in response to prolactin injection, in distinction to laying hens, does not necessarily indicate that males and females differ in their capability of incubating, given the proper hormonal situation. We will recall that nonlaying hens do not incubate when injected with prolactin. Presumably the effect of prolactin in inducing incubation in laying hens depends on priming by ovarian hormones, or on recent attachment to the egg-laying place, or on some combination of these. It may well be that when these factors have been analyzed, they will be found to apply to males as well as to nonlaying females.

(3) Other pituitary hormones do not seem to induce incubation behavior. This includes follicle - stimulating hormone (FSH). luteinizing hormone (LHl, and thyrotrophic hormone (TSHi (Riddle, Bates and Lahr, 1935; Riddle, 1937).

(41 The antigonad effect of prolactin may be considered relevant to its efficacy in imlucing incubation behavior, because the suppression of the secretion of gonadal hormones implies a reduction in gonad-stimulated sexual behavior, which might interfere with the onset of parental behavior (Lehrman, 1955). Bates, Lahr and Riddle (1935) found that injections of prolactin were followed by sharp decreases in the weight of the ovaries and oviducts, which did not occur when FSH was injected with the prolactin (Bates, Riddle and Lahr, 1937 ) . This implies that the antigonad action of prolactin is by way of the suppres


sion of the secretion of gonad-stimulating hormones by the pituitary glands. Similar effects were found in male domestic chickens (Nalbandov, 1945; Yamashina, 1952). In wild birds prolactin injections can prevent the normal increase in gonad weight caused by increasing light (Bailey, 1950). Prolactin injected during the breeding season is followed by the collapse of the testes and by the lipid metamorphosis (steatogenesis) of the tubules, which normally occur at the end of the breeding season (Coombs and Marshall, 1956; Lofts and Marshall, 1956j .

Gonadal hormones and incubation behavior. (1) Testosterone. The occurrence oi endogenous prolactin during incubation, the antigonad effect of prolactin, the effectiveness of prolactin in inducing incubation behavior, and the lack of sexual behavior during periods of incubation all suggest that the gonadal hormones responsible for sexual behavior and nest-building may be incompatible with the performance of incubation behavior, and experimental data in general support this impression.

Champy and Colle (1919) reported that the development of the crop-sac in incubating pigeons was accompanied in the male by a 90 per cent decrease in testis volume, and in the female by atresia of the ovarian follicles. In the domestic hen broody clucking occurs at a time when no eggs are being laid, comb size is minimal, and no copulations are taking place (Collias, 1950). In the wild bank swallow the beginning of incubation is accompanied by a sharp drop in the weight of the ovary (from about 300 mg. to about 53 mg.) and of the oviduct (from about 1500 mg. to about 200 mg.) ( Petersen, 1955 ) . Testis weights, which have increased during nest-building and egg-laying, remain high during incubation. Note that in this species the male develops no brood patch and does almost no incubation, unlike the situation in pigeons and doves in which the male participates in the care of the eggs. Marshall and Serventy (1956) found that the testis of the male shorttailed shearwater collapses very quickly after mating, coincident with the onset of his incubation duties (male and female shearwaters take turns in incubating the


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HORMONAL REGULATION OF BEHAVIOR


eggs) , whereas in the male satin bower-bird, which does not incubate or feed the young, this change in the testis is delayed several weeks, until the end of the breeding season. Collias (1940) found that the injection of 1 to 5 mg. per day of testosterone propionate into incubating hens caused the birds to desert their eggs within 3 to 13 days after the first injection. Kosin (1948) administered 10-mg. doses of testosterone propionate by injection into laying turkey hens at 2-week intervals, and found that this treatment prevented the onset of broodiness. On the other hand, male pigeons which normally take part in incubation are not prevented from incubating by testosterone propionate administration, nor do male pigeons discontinue established incubation when injected with as much as 2 mg. testosterone propionate daily (Collias, 1940, 1950, 1952). In the case of the black-crowned night heron, another species in which the male and female appear externally identical, and in which the male and female share the duties of incubation, Noble and Wurm (1940) found that testosterone propionate induced incubation behavior when injected into females or males. Riddle and Lahr (1944) similarly report that testosterone propionate, implanted into female ring doves, induced incubation in about 50 per cent of the birds. In unpublished experiments, I have failed to verify this observation. A consideration of the conditions of our experiments and of those of Riddle and Lahr and of Noble and Wurm may reveal a possible cause for the difference in results. The ring doves tested by Riddle and Lahr, and the black-crowned night herons tested by Noble and Wurm, were kept in pairs in the cage during the period of hormone administration. In the case of Riddle and Lahr's ring doves, the tests were performed with unisexual pairs of females. Our experiments, on the other hand, were done by injecting the hormone into the experimental birds during a 1-week period when each bird was alone in an isolation cage. At the end of the treatment period, the birds were placed in pairs in cages containing a nest and eggs. Under these conditions, birds treated with testosterone propionate failed to sit on the eggs, although other hormone treatments did in


duce incubation behavior (see below). I suggest the possibility that the testosterone propionate treatments, in Riddle and Lahr's experiment, actually induced male courtship behavior, which in those pairs in which the level of response was very different as between one bird and the other, would result in a faster formation of the pair than with untreated pairs of females, and that this courtship behavior, leading to pair formation, stimulated the secretion of endogenous hormones which in turn were responsible for the incubation behavior. When the birds were kept in isolation during the treatment period, the behavioral effects of the male hormone injection could have no stinuilating effect on the other bird (see below).

(3) Estrogens. Estrogens injected into laying or nonlaying hens failed to induce incubation behavior (Riddle, 1937; Nalbandov, 1945) , and FSH also was ineffective (Riddle, Bates and Lahr, 1935). The results from a number of studies have shown that estrogens administered to incubating domestic hens will cause them to discontinue sitting on the eggs. The most systematic of these was that by Godfrey and .Taap (1950) who injected each of 37 sitting hens with 15 mg. diethylstilbestrol. Twentyeight of the 37 had left the nest by the 4th or 5th day after the treatment. The birds had been sitting from 3 to 7 days at the time of the treatment. Although no untreated controls were used, it is clear that the treatment with diethylstilbestrol interrupted the incubation behavior, which normally lasts much longer than the 12-day maximum found in the responding birds. When the dosage was increased to 30 mg., 100 of 102 treated birds discontinued sitting. Among the 11 birds in the 15-mg. group in which incubation was not interrupted by diethylstilbestrol treatment, 5 left the nest during the 2nd day after injection and returned the following day. In 10 of the 11 incubation was discontinued as a result of a 2nd injection. This effect of exogenous estrogen has been verified for the domestic hen (Collias, 1940; Carson, Eaton and Bacon, 1956) and turkey (Blakely, Anderson and MacGregor, 1951). On the other hand, van Tienhoven (1958) reported that di


PARENTAL BEHAVIOR


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ethylstilbestrol injection failed to interrupt established broodiness in domestic turkeys. The conditions of his experiment were somewhat different from those of Godfrey and Jaap, since his birds were in broody coops with no nests or eggs.

Lehrman (1958b) found that untreated ring doves, with previous breeding experience, placed in pairs in cages containing nests and eggs, would begin to incubate the eggs after 4 to 7 days, during which they went through successive stages of courtship and nest-building. If the birds were injected with diethylstilbestrol (0.4 mg. per day) for 7 days while they were in individual isolation cages, and then immediately placed in the test cages, incubation took place in most of the birds within 1 to 3 days. The estrogen-treated birds immediately engaged in intensive nest-building behavior, in contrast to the untreated birds. It seems probable that the injected estrogen reduced the latency of the incubation response to the eggs, not by any ability to induce incubation behavior directly, but rather because it advanced the cycle from the courtship to the nest-building phase, so that events could occur which lead to the onset of incubation behavior within 2 or 3 days, and which normally do not occur until after the birds have been together for several days. The nature of these events will be discussed later. The fact that estrogen administered under these conditions reduced the latency of (or sped up the development of) the onset of incubation behavior does not necessarily mean that estrogen injected during incubation would not interrupt it in this species.

{3) Progesterone. Progesterone (or a gestagen) is of particular interest in connection with the onset of incubation behavior, because its involvement in ovulation (Rothchild and Fraps, 1949; Traps, 1955) and in the final stages of oviduct development (Mason, 1952; Brant and Nalbandov, 1956; Lehrman and Brody, 1957) indicates that it is present in the blood just before or at about the time when incubation normally starts.

Progesterone or corpus luteum preparations have been reported to be ineffective in inducing broodiness in domestic hens


(Riddle, 1937; Eigemann, 1937; Nalbandov, 1945) and canaries (Kobayashi, 1952), and actually to interrupt established broodiness in domestic turkeys (van Tienhoven, 1958) , although in all these cases the criterion was the existence of clucking and other broody behavior in birds that were not given an opportunity to sit on eggs.

Riddle and Lahr (1944) implanted pellets of progesterone into adult ring doves kept in unisexual pairs of males or of females in cages provided with a nest or eggs. All 18 doves tested in this way sat on the eggs, most of them within 3 to 7 days after the implantation of the pellets. None of the untreated control birds sat on the eggs during the 3-week test period. Riddle and Lahr allowed some of the progesterone-treated birds to continue sitting on the eggs for the normal incubation period of 14 days, and then at autopsy found that the crop-sac had increased in weight, as normally occurs during incubation. Since it had previously been demonstrated that prolactin induces incubation in laying hens, and that it is the hormone responsible for the growth of the crop. Riddle and Lahr concluded that progesterone induced incubation in their experiments because it had induced prolactin secretion by the birds' pituitary glands. However, Meites and Turner (1947) found that progesterone (and other sex hormones) when injected into pigeons, fail to increase either the crop weight or the prolactin content of the pituitary glands. Furthermore, Lehrman (1958a), who also found incubation behavior induced by progesterone in ring doves, kept the birds in isolation during a 7-day period of progesterone treatment, and then placed them in pairs in test cages with nests and eggs. These birds all quickly sat on the eggs, most of them within 20 minutes, and were killed for autopsy immediately after they were found sitting. These birds had crops no heavier than those of untreated control birds which did not incubate. It should be further noted that the crop does not normally begin to increase in weight until some days after incubation has already started. Since Patel (1936) showed that participation in incubation can itself stimulate the secretion of prolactin by the pituitary gland, it appears likely that pro


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HORMONAL REGULATION OF BEHAVIOR


gesterone induces incubation behavior by a means other than the stimulation of pituitary prolactin, and that the prolactin is secreted as a result of participation in incubation (see below). We will recall Marshall and Serventy's (1956) observation that in several species of seasonal-breeding wild birds, the lipid metamorphosis of the testis tubules coincides with the onset of incubation duties in a species in which the male takes part in incubation, and does not take place until some weeks later in a species in which the male does not take part in incubation. Paper chromatographic analysis by Lofts and Marshall (1957) indicates that the lipid contents of these metamorphosed tubules contain progesterone. Lofts and Marshall suggested that the postnuptial avian testis tubule may possess an endocrine function similar to that of the mammalian corpus luteum. At any rate, the association of progesterone with incubation behavior independently of prolactin, at least in some types of birds, needs to be taken seriously.

3. Interaction between Internal and External Environments in the Regulation of Incubation Behavior

Induction of incubation behavior by external stimuli. Male and female ring doves are brought into readiness to incubate by stimuli provided to each other, and by stimulation coming from the presence of the nesting material and/or nest bowl, even in the absence of eggs (Lehrman, 1958a, 1959b). Although doves kept singly in cages containing a nest with 2 eggs will show no interest in the eggs during a 6-week test period, pairs of birds kept in a cage with a nest bowl and nesting material will immediately sit upon eggs introduced into the cage by the experimenter after 7 days. If a pair of birds is kept together in a cage, but without a nest bowl or nesting material, they will, for the most part, not subsequently be ready to sit on eggs until after a short period of nest-building activity. Lehrman, Brody and Wortis (1961) tested doves for their response to eggs after varying periods in the cage with a mate or with a mate and nesting material. These birds were killed for autopsy immediately after the test. The data indicate that stimuli from


the male induce growth of the ovary and o^•iduct in the female and that this growth is additionally fostered by the presence of nesting material. Further, differences between the rates of oviduct growth in birds kept in the cage with and without nesting material closely parallel differences with respect to the rate of onset of incubation behavior. In addition, the onset of incubation behavior is closely related to the occurrence of ovulation, which conforms with and strengthens our earlier suggestion that l^rogesterone is involved in the beginning of incubation behavior in this species (Lehrman, 1959a, b).

Stimulation provided l)y the egg seems to play a considerable role in the maintenance of incubation behavior in many species of birds. In an often quoted but rather casual experiment Taibell (1928) forced 2 male turkeys to stay on a nest with eggs by holding them down by a cloth bag. These birds developed complete incubation behavior, including delicate treading on the nest, settling on the eggs, etc., in 1 to 4 days. On the other hand, Collias (1950) reported that confinement with eggs is relatively ineffective in stimulating incubation behavior in hens.

The importance of the egg in maintaining and stimulating incubation behavior can be seen from the fact that, when the eggs fail to hatch at the end of the normal incubation period, the bird will often continue sitting for a considerable time. Domestic hens will sit on sterile eggs up to 44 days, which is more than twice the normal incubation period (Saeki and Tanabe, 1954). Other observers (quoted by Katz, 1937) have found incubating hens sitting on artificial eggs for u]) to 4 months. Night herons breeding in captivity sit on sterile eggs for 40 to 51 days, as compared with the normal incubation period of 22 to 24 days (Noble and Wurm, 1942). Herring gulls, which normally incubate 26 to 27 days, will incubate 56 to 75 days on infertile eggs (Paludan, 1951). The sitting period of domestic pigeons can similarly be extended from 18 to 25 days (Kobayashi, 1953a). These data are especially interesting in view of the fact that, in a normal reproductive cycle, there is a rather striking change in the behavior of incubat


PARENTAL BEHAVIOR


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ing birds when tlie eggs hatch (see below, page 1300.

Adjustment of incubntlon behavior to the immediate stimulus situation. The hormonally induced modification of the ventral apterium (defeatherization, vascularization, edema) into the incubation patch, which, as we have noted, develops in most types of birds during the egg-laying period, is adapted for the production of localized higher skin temperatures and the transfer of heat between the bird and the eggs. There is much evidence that temperature regulation does in fact play a role in the regulation of the birds' behavior toward the eggs. Many field observations of wild birds indicate that the time spent sitting on the eggs is greater at lower ambient temperatures than at higher (Nice, 1937; Weston, 1947; Nice and Thomas, 1948; Skutch, 1957). Simmons (1954) found that the eggs of the graceful warbler are covered only 9 per cent of the time at an ambient temperature of 90°F., but 57 per cent of the time when the ambient temperature is 60 to 70°F. In the European wren the correlation between air temperature and the time spent on the eggs is -0.74 (P < 0.01) (Whitehouse and Armstrong, 1953; Armstrong, 1955). On very hot days, some birds may stand over the eggs without being in actual contact with them (Brackbill, 1958; Weller, 1958). Weller measured the temperature under an incubating nighthawk sitting on its eggs on the bare roof of a building (this species does not build a nest) and found that, during a very hot day, the temperature under the bird was lower than the temperature on the bare roof, indicating that the bird actually cooled the eggs by standing over them. At night, when the bird sat closely on the eggs, the egg temperatures were warmer than the temperatures on the bare roof. Irving and Krog (1956) found tiiat the average temperatures of eggs and young of various species of birds in the Arctic, measured in the nest, were about the same as those found in milder climates, indicating that the varying behavior of the parent in different climates tends to produce regulation of nest temperatures to about the same optimum.

Baerends (1959) experimentally altered


the temperatures of artificial eggs being incubated by herring gulls in the wild, by running water of various temperatures through tubes imbedded in the eggs. He found that temperature changes in the eggs (while ambient temperatures remain constant) induce temperature-regulating behavior of the bird {e.g., shivering, panting,, increase or decrease of body surface by erection or sleeking of feathers, etc.), as well as restlessness expressed by increased preening and "displacement nest-building," the latter resulting in improvement of the nest structure. In addition, abnormal egg temperatures induce movements which increase the isolation of the eggs from the surrounding air and improve the contact between the eggs and the incubation patches. For example, the bird wobbles from side to side on the eggs, resettles itself on the eggs, shifts the eggs with its bill, etc. Similar behavior is sometimes seen to increase on very hot days (Deusing, 1939).

Behavior which regulates the temperature of the eggs is not restricted to those birds having an incubation patch. The megapodes or mound- builders build large mounds of plant material, sometimes up to 35 feet in diameter and 15 feet high, and lay their eggs in holes dug in these mounds, which are then filled in. Incubation is accomplished by the heat produced by the rotting and fermentation of the materials of which the mound is built (Frith, 1956b). In one genus {Alectura) , the male works continuously to regulate the temperature, by digging holes in the mound, ramming his head into the hole (apparently to test the temperature), and then adding material (which raises the temperature) or digging oft' material from the top (which cools the mound), depending upon the temperature in the mound. The skin of the head and upper neck in this species is naked, and, in the male, turns brilliant red at the beginning of the breeding season (Frith, 1956a). It seems not unreasonable to suggest that this change is induced by changes in endocrine secretion, and that these changes in vascularity (and probably other characteristics) of this skin area make it more capable of serving as a temperature-sensing mechanism.

Physiologic effects of stimuli arising from


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HORMONAL REGULATION OF BEHAVIOR


incubation. We have pointed out that incubation behavior may be maintained long past its normal period by the presence of the eggs. What is the physiologic basis of this effect?

Saeki and Tanabe (1954, 1955) measured the prolactin content of the pituitary glands of domestic hens during different stages of the reproductive cycle under various experimental treatments. They found that the prolactin content of the gland, which is normally much higher during incubation than during laying (see above, page 1289), goes down sharply immediately after the hatching of the eggs. When birds were induced to sit for abnormally long times by substituting sterile eggs for their own eggs, the prolactin content of the pituitary gland remained high as long as the birds continued incubating. Further, they induced a number of laying hens to sit upon eggs by means of prolactin injection; some of these birds stopped sitting when the prolactin injection was discontinued, others continued to sit on the eggs. Autopsy data revealed that the pituitary glands of the birds which continued incubation after the end of the prolactin administration contained a high level of prolactin, whereas the pituitary glands of the birds which stopped incubating after the end of the prolactin injection had little prolactin. It is reasonably clear from these data that the eggs are capable of stimulating prolactin secretion by the pituitary gland of the sitting bird, and that this is probably part of the explanation for the control of incubation behavior by the presence or absence of the eggs.

In the domestic pigeon Patel (1936) showed that the crops of incubating birds increase in weight as long as the birds are sitting, but regress to the resting condition when the birds are removed from the eggs. The crops of ring doves induced to sit upon eggs by progesterone treatment will grow only if the birds are allowed to continue sitting upon the eggs (Riddle and Lahr, 1944; unpublished observations by D. S. Lehrman). In these birds, as in domestic hens, participation in incubation clearly stimulates the secretion of prolactin by the pituitary gland.

In the case of pigeons and doves, prolactin


is secreted under the influence of stimuli associated with incubation, even though the bird is not actually sitting on the egg. Patel (1936; Kuroda, 1956) found that the crop of a male pigeon removed from the breeding cage early in incubation, and placed in an adjacent cage from which he could see his mate, would develop as though he were sitting upon the egg himself. If a partition was placed between the two adjacent cages so that the male could not see the female sitting on the eggs, his crop would regress to the resting state. When the females were removed to the adjacent cages, the results were similar, except that some of the males left in the breeding cages abandoned the eggs. In those cases, the crops of the females failed to develop.

Effect of removal of eggs in midincubation. In many species of birds, even in those species which normally produce only one clutch of eggs per year, removal of the eggs during incubation is followed by the building of a new nest and the laying of a new set of eggs (Salomonsen, 1939; Blanchard, 1941; Simmons, 1954; Brackbill, 1958; Grosskopf, 1958; and many others). This clearly suggests that the removal of the eggs permits the secretion of gonadotrophic hormones which had been held under inhibition by stimuli coming from the eggs. Although the mechanism of this probable inhibition is not known, we may recall here the antigonad action of prolactin. The behavior of the male may be a factor in this renewal of gonadotrophic activity. Miller (1931j reports that the male, which is very quiet during the period when the female is sitting on eggs, shows a burst of renewed singing and courting activity when the nest and eggs are destroyed, possibly as a response to the renewed activity of the female released from the nest. Thus, in addition to the removal of any inhibiting effect of the eggs on the secretion of gonadotrophins by the pituitary gland of the female, there is a resurgence of the singing and courting activity of the male, which was partially responsible for the original secretion of gonadotrophin (see above, page 1279).

The time taken for laying new eggs after the destruction or removal of the old clutch varies. Most observers assert that the in


PARENTAL BEHAVIOR


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tei-A'al before laying of the new clutch bears no relationship to the age of the old clutch (Amantea, 1928; Nice, 1937, 1949; Kobayashi, 1953a; Giirr, 1954). For example, Paludan (1951) notes that, when 35 herring gull nests were destroyed by a storm, the laying of the first eggs of the new clutches was closely spaced between 11 and 14 days later, although the original clutches had varied in age from 1 to 21 days. However, quantitative data from studies of waterfowl (Sowls, 1949) and pheasants (Seubert, 1952) in wildlife preserves indicate that the interval before relaying is somew^hat longer, the older the original clutch at the time of its destruction.

4- Some Remarks on the Onset of Incubation

In the light of all the facts just presented, what may we say about the nature of the endocrine changes underlying the onset of incubation behavior during the normal breeding cycle?

The first point to be dealt with is the problem of the exact time when prolactin appears during the cycle. Saeki and Tanabe (1954, 1955) found that the prolactin content of the pituitary gland rises immediately after domestic hens begin to show incubation behavior. However, the spacing of their tests was such that it is not clear whether the prolactin content rises just before or just after the beginning of incubation. Similarly, Bailey's (1952) description of the development of the incubation patch in song birds permits the conclusion that prolactin is secreted during early incubation, but does not reveal whether the secretion of this hormone first reaches significant levels just before or just after the beginning of incubation behavior. Lahr and Riddle (1938) estimated the presence of prolactin in the blood of pigeons by arresting mitoses in the cropsac epithelium by means of colchicine injection, a method which gives a very sensitive indication of the effect of prolactin on the rate of growth in the epithelium (Leblond and Allen, 1937) . They found that the average number of mitoses ]ier high power microscopic field rose from about 4 just before the 1st egg to about 32 after the laying of the 2nd egg. They also found that the


injection of 60 l.V. of prolactin would increase the average number of mitoses per field from about 7 to about 25 within a half hour after the injection. Since pigeons (at least in captivity) begin to incubate sometime between the laying of the 1st and of the 2nd egg, these data again are not sufficiently exact to indicate whether the prolactin secretion began just before or just after the beginning of incubation behavior.

Inasmuch as the presence of eggs stimulates prolactin secretion, and placing eggs in the newly built nests of black-headed gulls suppresses the laying of subsequent eggs, provided the birds incubate (Weidmann, 1956), Eisner (1958) suggested that ])rolactin secretion starts as a result of the onset of incubation, which in turn is caused by other hormones such as progesterone (Cole, 1930; Riddle and Lahr, 1944; Lehrman, 1958b). This is a plausible suggestion, and should be considered in future research on this problem, despite some difficulties such as the fact that progesterone does not induce incubation behavior in domestic hens (see above, page 1293).

A second problem is the manner of hormone action in inducing incubation behavior. (This is, of course, a problem with respect to all hormone-induced behavior.) Some species of birds incubate eggs in spite of the absence of incubation patches (Bailey, 1952). Nevertheless, a number of coincidences suggest that the incubation patch should be investigated as a possible source of stimulation for incubation, or as a source of tension which is reduced by incubation behavior. First is the fact that the occurrence of incubation patches in male and in female birds generally corresponds to that of incubation behavior in the two sexes. Second, the incubation patch normally develoi)s just at the time when incubation behavior is beginning. Third, the characteristics of the incubation patch suggest that it is sensitive to temperature changes and adapted for heat exchange with the egg, and the effects of temperature changes on the incubation behavior of the bird suggest that the temperature-sensitivity of the incubation patch may be an important factor. Finally, prolactin induces incubation behavior in hens only if they are laying at


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HORMONAL REGULATION OF BEHAVIOR


the time of incubation, and prolactin causes change in the ventral apterium only after pretreatment with estrogen.

D. CARE OF THE YOUNG

1, Types of Young and Methods of Feeding Them

Birds vary widely with respect to the degree of development at hatching. Although all sorts of intermediates occur, two types of young are generally recognized among birds.

Precocial young, which emerge from the eggs after a relatively long incubation period, are hatched covered with body feathers, capable of locomotion within a few hours, and capable of picking up food, or in some cases even finding food without the assistance of the parents. Precocial young usually occur among families of water birds or of birds living and feeding on the ground, such as pheasants, cranes, sandpipers, ducks, grebes, etc. (Mayaud, 1950). Methods of feeding and caring for precocial young vary widely. For example, in some species of the mound-building megapodes, the young are completely independent, the parents playing no role in rearing them (Frith, 1956b). In other cases, such as the pheasants and ducks (and domestic chickens) , the young follow the parents, thus being led to food, and may be excited to feed by the behavior of the parents in the presence of food (Bent, 1923, 1925; Beebe, 1936). In still other families having precocial young, the young birds, although covered with down and capable of walking, may be fed for some time after hatching by food brought by the parents (terns, Hardy, 1957) , or by partially digested food regurgitated by the parents [e.g., penguins, Bagshawe, 1938; gulls, Tinbergen, 1953). Stonehouse (1953) reported that the emperor penguin feeds the young in part by regurgitating strips of epithelium or similar tissue invested with fat globules" presumably from the crop wall.

Altricial young are hatched naked of feathers, usually blind until the eyes open some days later, and incapable of locomotion or of finding or selecting food, so that they must be fed by the parents for a considerable number of days or weeks (May


aud, 1950; Kendeigh, 1952). Altricial young are fed by a variety of methods. Many insect-eating birds carry food to the young in their bills (Bent, 1942) . Other species may regurgitate food which they have carried in the throat (pelicans. Bent, 1922) or regurgitate from the crop or stomach food that has been partly digested (night heron, Allen and Mangels, 1940). In still other species, the regurgitated food may include substances secreted or produced in the digestive tract of the parents. Food regurgitated by the mother hummingbird contains digestive secretions mixed with ingested food (Mayaud, 1950) ; the young fulmar is fed partly on an oil secreted by the proventriculus of the parents (Fisher, 1952) ; food regurgitated to young pigeons just after hatching consists of epithelial cells desquamated into the lumen of the crop (Beams and Meyer, 1931).

Young birds are brooded by their parents, who sit on the nests containing the young and allow the young to huddle under them. The parents may cover them for some days after hatching, in a manner somewhat similar to the way in which they sit on eggs, although differences can usually be observed (Tinbergen, 1953). Parents of altricial young may continue to brood them for a number of days or weeks {e.g., Fisher, 1952), whereas precocial young may be brooded for only a short time after hatching or not at all (Kendeigh, 1952).

It is apparent that the types of behavior included in the expression "parental care" vary widely among different groups of birds, and therefore that analysis of the physiologic basis of this type of behavior in a few domesticated species will do no more than suggest the variety of mechanisms which are possible.

Roles of the parents. The roles of the parents in caring for the young need not necessarily be, in all respects, the same as their respective roles in incubating the eggs, a fact of considerable importance for its bearing on the problem of the role of hormones in the induction of behavior toward the young.

In the species in which the male and female both take part in incubation of the eggs, brooding and feeding of the young are


PARENTAL BEHAVIOR


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similarly carried out by both sexes. This is true in birds of a number of different families, such as cormorants (Mendell, 1936; Kortlandt, 1940), rails (Meise, 1934), gulls and terns (Tinbergen, 1953; Cuthbert, 1954; Hardy, 1957), doves (Whitman, 1919), swifts (Lack, 1956a j, petrels (Fisher, 1952; Davis, 1957), storks (Schiiz, 1943), herons (Allen and Mangels, 1940), woodpeckers (Bent, 1939), and others. There are a few api:)arent exceptions, such as the whitetailed kite, in which it is reported that the male sits on the eggs (for much less of the time than does the female), but does not brood the young (Hawbecker, 1942).

In some birds, such as most of the hummingbirds (Pitelka, 1942) and most of the ducks (Delacour and Mayr, 1945), the male takes no part in either incubation or any aspect of the care of the young. There are also a few birds, such as the phalaropes (Tinbergen, 1935), in which the male does all of the caring for the young.

There are many species in which the male, although he takes no part in incubation, regularly feeds the young (Ryves, 1934; Tinbergen, 1939b; Emlen, 1941; Skutch, 1953a; Armstrong, 1955; and many others). It is reported for a number of species that the males take no part in brooding the young, although they do the major share of feeding them (Nice, 1937; Rand, 1940; Odum, 1941; Lea, 1942; Hinde, 1952; Whitehouse and Armstrong, 1953) .

In many species of the order Galliformes, which includes the domestic chicken, the male neither broods nor feeds the (precocial) young, but accompanies the family, in effect taking part in leading them to food and in guarding them, although without the behavioral signs of "broodiness" {e.g., clucking, characteristic body position over the young, etc.) which are seen in the female (Kendeigh, 1952; see Kendeigh for survey of parental behavior in birds).

In general we may say that brooding the young, i.e., behavior which is associated with the provision of heat by the parents to young while they are still poikilothermic, is done only by the sex or sexes which, in that species, take part in incubation. Other aspects of parental behavior, such as feeding the young, leading them to food, guarding


them, etc., may be shown (although not necessarily so) by the other sex as well, even though it does not particii)ate in incubation.

2. Hormonal Induction of Parental Behavior toward Young

Prolactin and brooding in female birds. Nalbandov and Card (1945) reported that domestic hens injected with prolactin show a broody response to chicks (which consists of brooding them under body and wings, leading them to feed, calling them, and leading them away from danger by warning signals, etc.). Similar results have been obtained with pheasants (Crispens, 1956), and wild turkeys (Crispens, 1957). Crispens treated hen pheasants witli 6 mg. prolactin (presumably about 120 I.U.) per day for 3 days or more, and found that most of them (64 to 91 per cent in different groups) accepted and brooded 2-week-old Leghorn chicks. Two female wild turkeys similarly treated, except that the doses were larger, accepted either young turkeys or young Leghorn chicks.

None of these papers includes information about the status (laying or nonlaying) of the experimental birds beyond the fact that they were mature females.

Prolactin and brooding in male birds. Domestic cocks take no part in the care of the young, and sometimes even kill chicks that are confined with them. We have already noted that such cocks cannot be induced to sit on eggs by prolactin administration. However, a number of workers have reported that prolactin induces cocks to cluck, to lead, and to protect chicks under their body and wings (Nalbandov, 1945; Nalbandov and Card, 1945; Yamashina, 1952). According to Nalbandov and Card, prolactin injection causes cocks to become broody gradually over a 5-day period. On the other hand, hens injected with prolactin become broody quite suddenly, just as they normally do at the end of their egg-laying period.

Prolactin and parental feeding in doves. I have found that untreated male or female ring doves, placed singly in cages with 7day-old young, would make no attempt to feed them (Lehrman, 1955). When similar birds were injected with 400 to 450 I.U. pro


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lactin, and then placed in the cages with the squabs, 10 out of 12 fed the squabs by regurgitating the crop-milk which had been formed under the influence of the exogenous prolactin (Beams and Meyer, 1931 ; Riddle and Bates, 1939) . When birds were similarly injected with prolactin but their crops were anesthetized by the injection of a long-acting local anesthetic into the crop wall or into the skin over the crop, a significant number of birds failed to feed the squabs, compared with control birds in which the anesthetic was injected elsewhere than in the crop. I concluded that the ability of prolactin to elicit the regurgitation-feeding behavior of these birds toward the young depended on stimulation arising in the crop as a result of its engorgement by the action of prolactin (and on the antigonad action of prolactin, which prevented sexual or aggressive behavior from interfering with parental behavior toward the squabs) . Although I believe that this was probably correct, there are situations in which doves regurgitate when the crop is not engorged, and when there may be little or no prolactin present. The amount of crop-milk produced by parent pigeons decreases starting 2 or 3 days after the hatching of the young; after the young are 7 or 8 days old, the regurgitated crop contents consist entirely of grain, indicating that no crop-milk is being produced (Patel, 1936). Schooley and Riddle (1938) found that the amount of prolactin in the pituitary glands of pigeons with 7 to 15 day old young was considerably lower (1.05 of their units) than in the pituitarics of incubating birds (2.50 units), although it was not as low as in the pituitaries of sexually active birds (0.14 units). There are no data available to indicate whether this low level of prolactin (too low to cause the formation of crop-milk), may nevertheless stimulate regurgitation - feeding of ingested grain. When male pigeons are castrated they may still be able to induce the laying of eggs by females with which they were already mated, and they will sit on eggs and show crop development and crop-milk production during the first incubation period after castration (Kaufman and Dobrowska, 1931 ; Kaufman, 1932; Patel, 1936). During subsequent incubation periods, however, there


will be no crop development, although the birds may incubate. Since castration does not affect the sensitivity of the crop to prolactin (Riddle and Dykshorn, 1932), the effect of castration in preventing crop development during subsequent incubation periods is presumably due to a failure of prolactin secretion by the pituitary. It may be noted that the acidophilic cells which are associated with the periods when prolactin is being secreted (Schooley, 1937; Payne, 1943; Yasuda, 1953), gradually disappear from the pituitary glands of pigeons during the 2 or 3 months following castration (Schooley, 1937) . Kaufman (1932) reported that one such castrated male, after having taken part in incubation, fed the young with grain, although no crop development took place. The role of the condition of the crop in the occurrence of this regurgitation-feeding behavior obviously needs further investigation.

Gonadal hormones and the brooding of young. It is well known that androgenic hormones inhibit the brooding of the young. As long ago as 1916, Goodale observed that capons become broody when kept with chicks, and care for them in normal henfashion (Goodale, 1916, 1918). Saeki and Tanabe (1955) have confirmed this observation. Collias (1940) injected 4 mg. testosterone propionate per day into a hen with chicks, and found that she stopped clucking and caring for the chicks after 5 days. Nalbandov (1945) found that the injection of FSH or of 0.1 mg. methyltestosterone per day along with prolactin prevented broodiness from developing in response to the prolactin. Estradiol benzoate has an effect similar to that of testosterone in interrupting broody care of the young (Collias, 1940 1 .

3. Induction of Parental Behavior toward Young by External Stimuli

Changes in behavior of the parents at hatching. We have already pointed out that incubation behavior, and the associated prolactin secretion, can be maintained for abnormally long periods of time by stimuli coming from the eggs. This implies of course that changes in the behavioral and/or physiologic condition of the parent are stimu


PARENTAL BEHAVIOR


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latod by the change from the presence of eggs to the presence of young. Striking changes in behavior can be observed at the time of hatching. For example, a female duck sitting on eggs is very silent. As soon as the eggs are chipped, indicating the onset of hatching, frequent calls can be heard from the mother (Collias and Collias, 1956). It is often reported that in species in which the male takes no part in incubation, but does participate in the feeding of the yovmg, abrupt changes in behavior take place at the time of hatching. The male suddenly begins to spend much more time near the nest and to bring food to the young (Blanchard, 1941; Davis, 1941). Skutch (1953b) pointed out that the males of many species bring food to the female during the incubation period, or carry nesting material toward the nest, etc. thus maintaining a contact with the nest which provides the background for parental feeding by the male. In those species in which the male brings no food or other objects to the nest during the incubation period, he does not begin to bring food to the nest until he has seen the new nestlings, the sight of which stimulates the change in his activity. In the case of the tricolored red-winged blackbird the male leaves the colony area at the beginning of incubation, which is carried out entirely by the female, and then reappears after the eggs have hatched to participate in feeding the young (Emlen, 1941).

Observations of wild birds reveal that newly hatched young often interfere with the incubation of eggs not yet hatched. When the eggs of gulls hatch, for example, the parents appear at first to continue to treat the young just as they did the eggs, but the intensity of this incubation behavior is Cjuickly reduced by the behavior of the young, which crawl about in spite of the parent's effort to push them under its body (Paludan, 1951; Tinbergen 1953; Ytreberg, 1956). If there is a substantial interval between the hatching of the first and the third (last) egg, the incubation of the last egg may be interrupted, and it may die during the hatching process (James-Veitch and Booth, 1954; Ytreberg, 1956). The American coot, an aquatic bird which liuilds a number of nest-platforms in its marshy


territory, often broods the (precocial) young in a "brood nest" built when the eggs hatch and which is separate from the "egg nest." These birds often desert some of the eggs in the egg nest when enough of them have hatched to stimulate the beginning of brooding at the separate brood nest. The calls of the young appear to stimulate the adults to brood them instead of incubating the eggs (Gullion, 1954).

Stimulation of broodiness by the chicks. Broody behavior toward the chicks is induced in domestic hens by keeping them closely confined with the chicks (Burrows and Byerly, 1938; Collias, 1946; Ramsay, 19531. Broodiness induced by this method develops rather gradually, the bird first showing an incipient brooding posture, then clucking, then showing full broodiness including clucking and hovering over the young, and finally leading them to food, etc. (Ramsay, 1953). Confinement with the young also induces broody behavior in capons (Goodale, 1916) and immature hens, although in the latter the broody behavior develops more slowly than in adult birds (Saeki and Tanabe, 1955). Stanford (1952) induced adult bobwhite quail to become broody toward chicks by confining them in small cardboard boxes. In his experiment more of the males (46.7 per cent) than of the females (23.1 per cent) accepted the young.

In domestic chickens, the development of broodiness appears to be facilitated by keeping the birds in warm (80 to 90°r.), dark coops (Burrows and Byerly, 1938; Yamashina, 1952; Saeki and Tanabe, 1955).

Collias (1946) kept domestic hens brooding for months by repeatedly substituting young chicks for the growing chicks of the previous brood. (Older chicks are less effective in inducing broodiness than are newly hatched birds.) Emlen (1941) extended the parental feeding behavior of tricolored red-winged blackbirds from the normal 11 days to about 17 days by replacing the nestlings with younger birds. On the other hand, attempts to extend the period of crop-milk formation in pigeons by giving newly hatched squabs to the parents to replace the older birds which they were feeding have been unsuccessful (Patel, 1936).


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Hormonal correlates of broodiness induced by the young. It will be recalled that a high level of pituitary prolactin is associated with the normal occurrence of incubation behavior, and that when the presence of eggs causes the extension of incubation behavior past the normal period, the prolactin level remains high. The situation is strikingly different with respect to both normally occurring broodiness toward the young and broodiness experimentally induced by the presence of young. The prolactin content of the pituitary gland of hens goes down sharply after hatching, and remains down while the chicks are being brooded (Saeki and Tanabe, 1954) . Further, when hens are made broody by being kept with young, the prolactin content of their pituitary glands is not elevated (Burrows and Byerly, 1938; Saeki and Tanabe, 1955). The same is true of immature hens and capons. Both can be induced to become broody by being kept with young, without their pituitary glands showing increased prolactin content (Saeki and Tanabe, 1955).

Although the evidence discussed above indicates that the presence of young does not stimulate any detectable increase in prolactin in the pituitary gland, there is some evidence that the presence of young inhibits or delays the onset of the next cycle of nest-building and egg-laying, and therefore presumably inhibits the secretion of gonad-stimulating hormones by the parent's pituitary gland. In various species of wild birds, a recrudescence of sexual behavior can be noted after removal of the young (Howard, 1940; Blanchard, 1941; ^Armstrong, 1947). Kobayashi (1953a) found that removing the young of domestic pigeons would cause the laying of new eggs about 6 or 7 days later, although the feeding period is normally about 35 days long. The. European wren under normal conditions often produces a second brood during a single breeding season. If the nest is destroyed, the 1st egg of the new clutch will be laid some 5 to 8 days later. However, if the eggs are allowed to hatch normally, the 1st egg of the new brood will not be laid until some 10 to 14 days later. Therefore, the fact that the birds are caring for the nestlings delays the beginning of the new cycle (Armstrong, 1955).


4- Physiologic Nonidentity of Incubation Behavior and Broody Care of the Young

In much of the literature, including particularly the agricultural research literature, the term "broodiness" is used indiscriminately to refer to incubation behavior, brooding of the young, and caring for the young in other ways. I have been rather careful to use the term "incubation" or "incubation behavior" when referring to behavior toward the egg, and to restrict the term "broody" or "broodiness" to behavior toward the young. I believe this distinction is justified, and even necessitated, by a number of lines of evidence.

Distribution of incubation behavior and of parental care of the young. Perhaps the most striking evidence to be found in the natural history of birds for the distinctiveness of incubation behavior and of parental care of the young lies in the fact that in many species of birds the female does all of the incubating, whereas the male plays a major role in feeding the young. Skutch (1953b) points out that in many species of songbirds the male discovers the nestlings when the eggs hatch, in part as a result of his behavior during the incubation period. ]\Iales which do not incubate may stand guard at the nest, they may bring food to the female, they may visit the nest occasionally, they may escort the female to and from the nest when she leaves it to feed, etc. In some species it seems fairly clear that the behavior of feeding the nestlings has much in common with that of feeding the female while she is on the nest, as in the Florida jay, in which the male brings food to the female during the incubation period and, after the eggs hatch, brings food to the nest and may either give it to the young, or to the female, who then gives it to the young (Amadon, 1944b).

At least in birds with altricial young a distinction must be made between the parental behavior of feeding the young and that of brooding them (i.e., sitting on them so as to provide heat during their early poikilothermic days). The usual situation in songbird species in which the female incubates and the male feeds the young is that the female also does all of the brooding of the young (Lack, 1946; Putnam, 1949;


PARENTAL BEHAVIOR


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Allen and Nice, 1952 ; Whitehouse and Armstrong, 1953). However, the assumption that the physiologic bases of incubation and of brooding are somewhat different is supported by the fact that, in some species in which both sexes share in incubation and in brooding, the relative share of the sexes in these two behaviors is quite different. For example, although male and female pied-billed grebes both incubate the eggs, the female does most of the brooding of the newly hatched young (Deusing, 1939). In the bank swallow, in which the female does most of the incubating, the male and the female may share more nearly equally in the brooding of the young, although there are no data which indicate whether the male actually provides heat to the young (Petersen, 19551 .

Experimental induction of incubation behavior and of broody behavior. The most striking evidence for the distinctness of incubation behavior and of broody care of the young comes from the work of Nalbandov (Nalbandov, 1945; Nalbandov and Card, 1945) who found that prolactin would not induce domestic cocks to sit on eggs, regardless of dosage, but that this hormone induces cocks to adopt chicks, to protect them under their body and wing, to lead them to feed and water, to cluck to them, to protect them against intruders, etc. Further, confining cocks with eggs did not induce them to incubate, although confining them with chicks effectively caused them to become broody and to care for the chicks. Schjelderup-Ebbe (1924) noted great individual differences among domestic hens with respect to the efficiency and intensity of their broody care of chicks. Some hens which incubated eggs very devotedly until hatching showed no interest whatever in the chicks after hatching. Lashley (1915) found that sooty terns who were sitting on eggs less than 2 weeks old would not adopt young chicks. A colony of emperor penguins always includes some nonincubating birds. When the eggs hatch, these birds suddenly become very aggressive and try to get the young. The actual parents sometimes give up the young to such other birds, which then feed the chicks by regurgitation. Further, birds which have played no role in incubating the eggs, and which have been feed


ing at sea for some weeks or months during the incubation period, may feed the young birds by regurgitation immediately after their arrival in the colony at the end of the incubation period, indicating that the ability to feed the young by regurgitation is not continuous with or conditioned by incubation (Prevost, 1953; Stonehouse, 1953). There are other cases, however, in which behavior toward the eggs and the young may be more or less interchangeable. Allen and Mangels (1940) exchanged eggs and young (age not reported) between different pairs of black-crowned night herons and found that the new contents of the nest were accepted and brooded by both groups of parents, although the sudden appearance of young caused considerable disturbance to the parents. Emlen (1941) similarly found that young tricolored redwinged blackbirds introduced into nests in which the incubation of eggs had just begun would readily be accepted and fed.

Hormonal concomitants of incubation and of broodiness. Another indication that the physiologic bases of incubation and broodiness are different may be found in the fact that normally occurring incubation behavior is associated with a high level of prolactin in the pituitary gland, whereas broody care of the young is not (see above) . Further, when broody behavior is induced by keeping hens, capons, or cocks with young birds, no increase in prolactin content of the pituitary gland accompanies the onset of this broodiness (Saeki and Tanabe, 1955) in contrast to the situation when incubation is extended by the presence of eggs. Finally, Ramsay (1953) reports that broodiness induced by confinement with young is not associated with the formation of the incubation patch which occurs along with normal broodiness.

Conclusion. Although many more data are obviously needed on the whole range of problems connected with the hormonal basis of inculcation and broodiness, it is reasonably clear that incubation behavior, on the one hand, and parental care of the young, on the other, are not identical tendencies. They are differently distributed in the natural history of birds, they are not induced in the same way by external stimuli or by hormone treatment, and they are not ac


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companied by the same hormonal changes. It is probable that brooding of the young (providing heat) has more in common with incubation behavior than do other aspects of parental care (feeding the young, leading them, protecting them, allowing them to huddle under the wing, etc.), but information which might clarify this point is still inadequate.

Nalbandov (1945) suggested that prolactin induces "broodiness" largely or solely through its antigonad (or, more properly, antigonadotrophic) effect. It should be pointed out, however, that hypophysectomy interrupts incubation behavior of sitting hens within 23 hours (Prohaszka, quoted by Saeki and Tanabe, 1955) thus indicating that the maintenance of incubation behavior does not depend merely on the removal of pituitary gonadotrophins. On the other hand, castration alone makes male domestic chickens capable of being rendered broody by confinement with chicks, and this effect is not accompanied by increased prolactin secretion. Note also that prolactin induces incubation behavior in hens only if they were laying at the time of treatment, and that it does not induce incubation behavior at all in males, whereas care of the young is induced by prolactin alone. These data suggest that incubation behavior may be induced by some positive action of prolactin on a tissue previously primed by ovarian hormones, whereas broody care of the young may be facilitated merely by the antigonad action of prolactin.

In any event it now seems desirable to distinguish sharply between behavior toward the eggs (incubation behavior) and behavior toward the young (brooding and parental care) . Our knowledge of these matters has now reached the point where the use of the general term "broodiness" to cover all aspects of parental behavior toward the eggs and young may be misleading.^

^ A number of additional references to work on hormonal regulation of behavior in birds may be found in the review by Eisner (1960), which appeared too late to be considered in the preparation of this chapter.


III. Hormones and Parental Behavior in Infrahunian Mammals

The reader will soon become aware of a rather unfortunate difference between our material relating to birds and that relating to mammals. Several rich sources of information with respect to parental behavior and its physiologic bases, on which we have drawn in our discussion of birds, simply do not exist for mammals, or, if so, only to a very restricted degree. The relationship between egg production and broodiness in domestic hens has stimulated a good deal of research on these problems in an agricultural setting, of which we have taken advantage. Farm mammals do not seem to have stimulated interest in the same type of problem except for the case of the control of lactation. Another striking difference between the available information on birds and that on mammals stems from the existence of a large and enthusiastic supply of amateur, semiprofessional, and professional bird-watchers whose contributions range from systematic descriptive accounts of the behavior of various species of birds through a variety of more or less casual experiments which, although usually rather anecdotal, are often extremely suggestive, to excellent experimental studies carried out in the field on relatively undisturbed free-living birds. The natural history of mammals simply has not excited nearly so widespread or so intense an interest in such a variety of people (including the present author). In addition, the places in which most mammals rear their young are very much less accessible than is usually the case with birds, so that opportunities for observation are much more sharply restricted. There are, of course, notable exceptions, such as Darling's (1956) classic field study of the Scottish red deer, Hediger's (1950) interesting and fruitful studies of the behavior of mammals in zoos, EiblEibesfeldt's (1958) remarkably detailed studies of the behavior of a variety of mammals under simulated natural conditions in a research institute, and a number of others.

Another difference between our treatment of birds and of mammals depends on the fact that the relationship between ovula


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tioii and other events in the reproductive cycle is typically somewhat different in the two groups. The obvious functional relationships between nest-building and incubation behavior led us to include a treatment of nest-building behavior, even though a strict (and artificial) attempt at definition might result in the conclusion that nestbuilding was a part of sexual, rather than parental behavior. In birds, ovulation occurs between the building of the nest and the incubation of the eggs, and since the physiologic events associated with ovulation are very much involved both in nestbuilding behavior and in the onset of incubation behavior, various aspects of ovulation in birds necessarily attracted our attention. In mammals, on the other hand, ovulation and fertilization occur long before the emergence of the fetus from the mother. Since nest-building tends to occur late in pregnancy (see below), the physiology of ovulation does not play the role in establishing parental behavior in mammals that it typically does in birds, and we will therefore need no discussion of ovulation in this part of the chapter.

A. NEST-BUILDING

1. Xest-building Patterns in Mammals

Many mammals build shelters or "nests" of various types, the building and occupation of which is not necessarily closely associated with any particular time in the breeding cycle, as it is in birds. Although laboratory data and some scattered field observations indicate that, in some cases at least, changes in the pattern of building behavior do occur in association with reproduction, most of the data from field observations are not sufficiently detailed to permit any differentiation between the building of shelters and reproductive nesting behavior.

Some types of mammals live the year round without constructing any type of nest or shelter. This mode is characteristic of aquatic mammals in general (Fisher, 1940; Bourliere, 1954) and most ungulates (e.g., Murie, 1951). Other mammals make temporary shelters, which they may change from day to day, or at somewhat longer in


tervals. The European hare digs small trenches in the ground or in grass, in which it spends most of its time during the day (Eibl-Eibesfeldt, 1958). Many tropical bats take shelter during the day in abandoned bird nests or mammal burrows, or cut the blades of large leaves with their teeth so that part of the leaf falls around the clinging animal (Allen, 1939; Bourliere, 1954). Many of the higher primates build sleeping shelters of light branches, twigs, leaves, etc., in which they take shelter during the night ; in most cases a new one is built each day at a different location. The orang-utang and chimpanzee build such nests in trees (Reichenow, 1921; Aschemeier, 1922; Nissen, 1931), whereas the gorilla may build either in trees or on the ground (Yerkes and Child, 1927) .

The most common type of shelter among mammals is the burrow (Wunder, 1937; Bourliere, 1954; Krumbiegel, 1955) which is used by mammals of many different orders. These burrows range from the simple holes used by many carnivores (Hamilton, 1939) to the elaborate underground networks of tunnels and galleries dug by many rodents (Eisentraut, 1928; Grasse and Dekeyser, 1955; Eibl-Eibesfeldt, 1958).

Some mammals, mostly rodents, build nests of grass, twigs, and leaves in trees (American red squirrel, Hatt, 1929) , on the ground about the bases of trees (duskyfooted wood-rat, Linsdale and Tevis, 1951), on the surface of the water (European water vole, Wunder, 1937), or partly submerged in the water (American beaver, Warren, 1927) .

Thorough descriptions of the building, burrowing, and nesting behavior of many species of mammals may be found in the monographs and textbooks by Wunder (1937), Hamilton (1939) , Bourliere (1954), Grasse (1955), and Krumbiegel (1955).

2. Hormonal Basis of Nest-building

Timing of nest-building during the reproductive cycle. We have already noted that the building of shelters, burrows, and "nests" usually seems not to be particularly related to pregnancy or to the care of the young. There are some indications, however, even in the observations on the behavior of free-living wild mammals, that behavior


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with respect to shelters and nests does change about the time of parturition. For example, many female ungulates, which normally live in herds on open range, leave the herd and seek isolation and shelter at the time of parturition {e.g., American elk, Murie, 1951). The wood-mouse lives in a hollow, globular nest of leaves and grass. A male and female may both frequent the same nest, but the female will usually force the male to leave when the litter arrives (Nicholson, 1941). Female domestic mice observed in the laboratory can similarly sometimes be seen, just after parturition, to keep other animals out of a previously common nest (Leblond, 1940) .

As the following data secured from laboratory animals suggest, it may well be that our failure more often to relate the nestbuilding activity of wild mammals to the reproductive cycle is partly a function of the lack of quantitative data.

The female domestic rabbit builds a nest by piling up grasses, hay or straw, burrowing into it, and hollowing it out. She then plucks hair from the ventral surface of her body and lines the nest with it. Sawin and Crary (1953) reported that this nest-building activity takes place about the time of parturition, just before or just after the appearance of the litter, depending on the strain. The plucking of hair is associated with a marked loosening of the hair on the belly, dewlap, and thighs (Sawin and Crary, 1953; Klein, 1956). By weighing the amount of hair obtained on different days by a standard combing technique, it can be shown that the loosening of the hair reaches a peak during the 5 days before parturition (Sawin, Denenberg, Ross, Hafter and Zarrow, 1960). The pregnant African lioness also pulls hair from her belly and around her nipples just before parturition. In this species, gestation lasts about 109 days, and this type of hair-pulling is seen from about 100 days onward (Cooper, 1942). Loosening of the hair in late pregnancy has also been found in the Asiatic squirrel (Landry, 1959) .

Similarly, nest-building behavior in the domesticated rat is clearly related to the endocrine condition of the animal. Kinder (1927) measured the amount of nest-building in laboratory rats by counting the num


ber of strips of crepe paper used by them for constructing the nest. She found that males and nonpregnant females, on the average, perform the same amount of nestbuilding activity per day. However, the amount in the jemale is subject to a 5-day cyclic variation, being minimum at estrus, and maximum midway between the two estrous periods.

Li pregnant females there is a sudden rise in nest-building activity about 5 days prepartum, the nest-building continuing at a high level during lactation. Preparturient and lactating females spend almost all their time in nest-building, except w^hen suckling young or eating. Similar observations were made by Sturman-Hulbe and Stone (1929), and by Beach (1937). Obias (1957) compared the nest-building behavior of rats just before and just after parturition, and reported that the amount of nest-building increases at the time of parturition.

Koller (1952, 1956) kept individual domestic mice in cages 40 cm. square. Mice kept under such conditions, and provided with hay as building material, will build a nest each night, which can be removed and weighed the next morning. Koller observed that immature mice (beginning 1 to 2 weeks before maturity), adult males, and nonpregnant females all built small nests which he called "sleeping nests" iSchlafnester), the amount of nesting material used per night ranging from about 7 to about 11 gm. Pregnant females, on the other hand, build much larger nests, averaging 45 to 50 gm. per night, starting quite abruptly on the 4th to the 5th day of pregnancy, and therefore about the time when the corpus luteum of pregnancy becomes histologically demonstrable. As in the rats studied by Kinder, the building of these larger nests, which Koller called "brood nests (Brutnester) , continued during lactation.

Pearson (1944) states that pregnant shrews in captivity build nests no different from those built by nonpregnant animals. However, no quantitative data are given, nor do we have sufficient information about the breeding of these animals to judge the adequacy of the laboratory conditions as a setting for the natural behavior pattern.

Hypophyseal hormones and nest-building behavior. Richter and Eckert (1936) found


PARENTAL BEHAVIOR


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that hypophyscctomy greatly increases the amount of nest-building activity in rats. The 12 animals used in their principal exl)erimcnt performed about 178 per cent more ne^t-building behavior (measured by the amount of paper used) after removal of the pituitary gland than before. After more extensive later experiments, Richter (1937) reported that many rats did five times as much nest-building after hypophysectomy as before. These experiments were done with nonpregnant animals, and the amount of nest-building behavior reported after hypophysectomy is comparable with the maximal amount normally seen in pregnant animals. Similar results were obtained by Stone and his co-workers (Stone and King, 1954; Stone and Mason, 1955) who rated the nests built by intact 60-day-old male albino rats, and compared them with the nests built by rats of the same age which had been hypophysectomized at 35 days of age. These ratings were based, not only on the amount of nesting material used, but also on the type of construction, higher ratings being given to nests which, from the point of view of compactness, cover, etc., appeared to be better insulating or heat-conserving devices. When rated in this way hypophysectomized animals were judged to have built "better" nests. In their original paper, Richter and Eckert had noted that normal nonpregnant rats built loose and shapeless nests, whereas hypophysectomized animals constructed woven balls with single small openings to an inner chamber.

An apparent contradiction to the general agreement that hypophysectomy increases both the quantity and the quality of nestbuilding in domestic rats appears in the study of Obias (1957j, who hypophysectomized pregnant rats on the 13th day of gestation. Of his 11 experimental animals, 5 died at parturition. Obias rated the nests built by the hypophysectomized animals and by intact controls during the 10 days before parturition, and the nests built by the surviving hypophysectomites and by the controls during the 10 days after parturition, and found no differences between the intact and the hypophysectomized animals. The failure of hypophysectomy to affect the nature of the nest in pregnant rats, in contrast to the striking effect of this op


eration in non-pregnant animals, is presumably due to the fact that placental hormones can have the same effect as the relevant pituitary hormones.

Information about the effect of exogenous pituitary or pituitary-like hormones on nest-building activity is scanty. Tietz (1933) injected pregnancy urine into 14 nonpregnant female rabbits, and found that 50 per cent of them built nests, using in part hair which had become loosened as a result of the treatment and which the rabbits pulled out from their bodies. Inspection of the ovaries of these animals through exploratory laparotomies showed that some of the treated rabbits developed corpora lutea, and that the fur became loosened only in those animals in which the corpora lutea developed.

Prolactin did not induce nest-building behavior in either male or female domestic mice (Roller, 1952).

Oddly enough, investigators interested in this subject do not seem to have injected pituitary extracts into hypophysectomized rats, in order to see which pituitary fractions would prevent the increase in nestbuilding activity after hypophysectomy. However, as will be seen from the next section, data on the effects of nonpituitary hormones on nest-building permit a reasonably good guess as to the nature of the effects of hypophysectomy.

Gonadal and thyroid hormones and nestbiiilding behavior. Removal of the thyroid glands in rats induces a rise in the quantity of nest-building behavior of the same order as that induced by hypophysectomy (Richter and Eckert, 1936; Richter, 1937, 1941). Further, thyroid extract administered to intact rats is capable of inhibiting their nest-building behavior (Richter, 1943). Richter suggests that the enhanced nestbuilding activity resulting from hypophysectomy is due to the loss of thyroid function, a point which we shall discuss in more detail elsewhere (p. 1346).

The effect of thyroidectomy in the rabbit appears to be different from that in the rat, although data in exactly comparable situations are not available. Chu (1945) removed the thyroid glands from female rabbits which were then allowed to become pregnant from 17 to 108 days later. These ani


1308


HORMONAL REGULATION OF BEHAVIOR


mals eventually delivered young normally, but did not build nests or i^luck any of their fur.

Richter (1937; Richter and Eckert, 1936) reported that gonadectomy and adrenalectomy both produced very small increases in nest-building behavior in rats. On the other hand, Roller (1956) reported that removal of the gonads of male and nonpregnant female mice caused no change in their nestbuilding behavior: the low-level nest-building behavior ("sleeping nests") characteristic of such animals before treatment continued unchanged.

In contrast to the failure of gonadectomy to affect the level of nest-building behavior in nonpregnant mice, the striking increase in nest-building behavior during pregnancy ("brood-nests") is definitely under gonadal control (Roller, 1952, 1956). Injection of progesterone into intact or gonadectomized female mice very quickly (after 2 or three daily injections of 1.5 I.U. each) induced a marked increase in the amount of nesting material used per night, on the same order as the increase which occurs naturally during pregnancy (from about 10 to 15 gm. to about 50 to 60 gm. ) . Note that this effect of progesterone did not require previous priming with an estrogen. Large doses of estrone (200 I.U. per animal per day) caused no increase in nest-building activity in spayed female mice ; on the contrary. Roller's graphs suggest a slight but consistent depression of nest-building activity. If the same treatment is given to intact adult female mice, the same slight depression of nest-building activity occurs, but when the injections are discontinued after a 10-day treatment period, a marked increase in nest-building activity is seen (from about 8 gm. to about 20 gm.). It seems likely that this increase in nest-building activity is a result of the secretion of endogenous progesterone stimulated by the estrone injections.

An important finding in Roller's work is that male mice, whether intact or castrated, cannot be made to build "brood nests" {i.e., increase the amount of nest-building activity) by treatment with progesterone or with an estrogen. This sex difference is in contrast to the effects of hypoiihysectomy or


thyroidectomy in rats, which are the same in males as in females.

A relationship also exists in the domestic rabbit between progesterone and nest-building behavior, but it seems to be quite different from that which Roller demonstrated in the mouse. Rlein (1952, 1956) found that removal of the corpus luteum during pregnancy would induce rabbits to show immediate nest-building behavior, including plucking of fur. Removal of the gravid uterus was followed by involution of the corpus luteum, with subsequent nestbuilding behavior (Zarrow, Sawin, Ross and Denenberg, 1960). Hammond (in Rlein, 1952) found that pseudopregnant rabbits often build a nest during the involution of the corpus luteum (after about 16 days of pseudoprcgnancy). If the uterus and cervix of such a rabbit are removed, the corpus luteum undergoes involution, and the nest is built, after 24 to 29 days instead of after 16 days. These data seem to indicate that nestbuilding behavior in the female rabbit occurs as a result of, or in association with, the cessation of progesterone secretion, rather than being stimulated by progesterone, as in the mouse. We may note here that, in a normal breeding cycle, the characteristic nest-building behavior of the pregnant mouse starts suddenly about the 4th or 5th day of pregnancy (Roller, 1956), whereas in the rabbit nest-building occurs just before or just after parturition (Sawin and Crary, 1953) .

Fisher ( 1956) has induced nest-building behavior (and other aspects of maternal behavior) in rats by local injection of minute amounts of a testosterone salt (sodium testosterone sulfate) directly into the hypothalamus. At the time of this writing, only a preliminary report of Fisher's work is available, in which he reports the occurrence of nest-building behavior in 19 of 130 male rats tested in this manner. Fisher's description leaves no doubt that strongly motivated behavior of various types, normally maternal, was induced by these injections, but since this hormone does not normally cause such behavior on systemic injection, it is not yet possible to state what contribution these observations make to an understanding of the normal relationships between


PARENTAL BEHAVIOR


1809


endogenous hormones and nest-building behavior,

3. Induction of Nest-huilding Behavior by External Stiinidi

Temperature changes and nest-huilding behavior. Kinder (1927) kept rats at various temperatures, and found that the amount of nest-building activity was inversely proportional to the environmental temperature. For example, at room temperatures around 90°F. rats used, on the average, 6 to 11 stri])s of paper per 6-hour period; when the room temperature fell to 40 to 60°F. the consumption of nesting material rose to 38 to 50 strips during a like period. Nests built at temperatures of 90°F. were small, scattered, and loose, in contrast to the large compact nests built by rats kept in the lower temperatures. Roller (1956) observed similar effects in mice. He found that nest-building did not occur at temperatures above 85°F., and that the amount of nest-building increased with decreasing temperature down to about 50°F.

This effect of temperature on nest-building activity, plus the fact that thyroidectomy increases, and exogenous thyroid extract inhibits, such activity, has suggested to all workers on this problem that nestbuilding activity serves in part a thermoregulatory function, and that the cyclic variations in nest-building behavior in rats and mice can be partly explained as temperature-regulating devices (Kinder, 1927; Richter, 1937; Koller, 1956). We shall return to this point later, in our discussion of the mechanisms of hormonal effects on behavior (see below, p. 1346).

The effect of the young. Koller (1952, 1956) reported that the introduction of young mice (less than 15 days old) into the cage with an adult female causes an abrupt increase in the amount of nest-building behavior on the following night and on subsequent nights. Females that had been using an average of about 7 gm. of nesting material per night increased their consumption to al)out 25 gm. This increase in nest-building activity appears to be a consequence of the "adoption" of the young by the female. If the young animals are placed in the cage under a wire cover, so that the female can


not retrieve them or touch them, they do not cause any increase in nest-building activity. Further, about 25 per cent of Roller's subjects killed or ate the young, and in those cases there was no increase in nest-building activity on the night following the introduction of the young. Nest-building activity is normally maintained at a high level after parturition, during the period when the young are being cared for by the mother. Roller found that when the young were removed immediately after parturition the level of nest-building activity (which is very high during the last half of pregnancy) abruptly dropped back to the nonbreeding level.

Leblond (1940) similarly reported that introduction of young mice into the cage induced nest-building behavior in the adults, but beyond this statement his data are ambiguous on this point because his quantitative scores were arrived at by lumping nest-building behavior together with other aspects of maternal behavior."

Roller reported that male mice kill and eat young animals left in the cage with them, and therefore that no increase in nest-building behavior was induced by this treatment. On the other hand, Leblond and Nelson (1937a; Leblond, 1940) found that "maternal behavior" (which included an undefined amount of nest-building behavior) was induced in male mice by keeping young in their cages. It is not apparent whether this difference between the results of Leblond and Nelson and those of Roller is due to a difference in the strain of mice used or in the conditions of their exjieriments.

One is temi)ted to suggest that the ability of young mice to stimulate increased nestbuilding behavior in adults is due to a hormonal change induced by stimuli coming from the young, but this does not seem very likely. To begin with, the presence of young mice maintains a high level of nest-building behavior in their mothers after parturition, when the level of progesterone (which can induce the nest-building behavior) has fallen abruj^tly. The presence of the young is known to stimulate and maintain the secretion of prolactin (see below, p. 1325) , but ]irolactin administered to adult females does


1810


HORMONAL REGULATION OF BEHAVIOR


not induce nest-building behavior. Further, Leblond and Nelson (1937a, b) found that nest-building behavior was induced in hypophysectomized adults when they were caged with young mice, which rather effectively disposes of the possibility of induced hormone secretions. It appears rather that stimuli from the young and the effect of progesterone are complementary mechanisms for maintaining nest-building behavior at a high level during the whole period when such behavior is adaptive.

B. BEHAVIOR DURING PARTURITION

1. Patterns of Parturitive Behavior

Behavior before 'parturition. In addition to the nest-building behavior already discussed, other changes in behavior take place during late pregnancy. Unfortunately, not much attention has been paid to these aspects of behavior, but it is clear that the special physiologic conditions of pregnancy foster behavioral changes which contribute to the preparation for behavior towards the neonate. According to Schneirla (1950) a pregnant cat reacts differently to her own body from a nonpregnant female. More attention is paid to the licking and grooming of the body, the abdominal and pelvic regions in particular being licked significantly more than in nonpregnant cats. Schneirla suggests that this licking, occurring well before parturition, helps to focus the behavior of the animal toward that part of its body. Later, during parturition, its licking responses to stimuli from the pelvic region will make a significant contribution to the parturition itself.

The preparturient female American elk, which at other times lives gregariously in closely integrated herds, goes into isolation, avoiding other animals, with the result (among others) that the newborn elk at first associates only with its own mother (Altmann, 1952). Similar observations have been made on the European red deer (Darling, 1956) and other ungulates (Bourliere, 1954).

During pregnancy, chimpanzees become increasingly quiet, gentle, and friendly, and less aggressive, both toward human keepers and toward other chimpanzees (Yerkes and Tomilin, 1935; Yerkes and Elder, 1937).


This uncharacteristic gentle behavior persists during lactation, except that if the infant is removed shortly after birth, the mother quickly returns to the usual type of behavior (Nissen and Yerkes, 1943). On the other hand, Wimsatt (1960) stated that pregnant bats become restless and irritable some time before parturition.

It is probable that closer study of the behavior of preparturient animals will yield significant clues to the nature of the physiologic preparation for postparturitive behavior.

Behavior at parturition. Although observations of behavior during parturition have been made on only very few species, it is clear that different types of mammals give birth in different positions, and that the position taken by the mother during parturition is a relatively constant characteristic of the species. A number of ungulates, and the elephant, give birth in a standing position (Hediger, 1952). Other ungulates, such as the American elk (Altmann, 1952), and the guanaco (Hediger, 1952), may give birth in a reclining position. Rodents characteristically give birth sitting or crouching on the hind legs ( Eibl-Eibesfeldt, 1958; Dieterlen, 1959), whereas domestic cats crouch and recline in different stages of the process (Cooper, 1944). Some kangaroos and other marsupials lie on the back during parturition (Hediger, 1958). In some species, such as the American buffalo, considerable individual differences are seen; some individuals give birth while standing, others while lying down (McHugh, 1958).

As will be seen, the positions taken by animals of different species are related to the manner in which they establish care of the young, and may be of considerable importance for the analysis of the development of maternal care. Rowell (1960a) observed that when the golden hamster pup begins to emerge, the mother licks it with the rest of her genital area, and that, at this stage, the young appears to be treated as an extension of this area of the mother's body. The parturient American elk lies down and licks her flanks, vulva, and the adjoining area before the calf has begun to emerge. Then, when the calf emerges, the cow licks it (Altmann, 1952). Likewise in domestic goats, the mother licks the kid as the kid


PARENTAL BEHAVIOR


1311


is leaving her body, the licking appearing to be continuous with that which occurred before the emergence of the kid began (Blauvelt, 1955). Tinklepaugh and Hartman ( 1930, 1932 1 provided a detailed description of the behavior of the rhesus monkey during liarturition. The mother monkey gets fetal fluids on her hands by touching her vulva at the beginning of delivery, then vigorously licks the fluid off her hands. The cleaning of the newborn monkey seems to be a continuation of this process. After delivery the mother alternately cleans her own hands and licks the baby's body.

Self-licking and licking of the emerging fetal membranes and young are often associated with maternal assistance to the emerging fetus. The domestic rabbit during parturition stands in a bowed, somewhat crouching position with the back strongly arched, the hind limbs flexed ventrally, and the head bent down between the front legs. In this posture the birth canal is so oriented that a fetus during birth is propelled forwards and downwards between the rabbit's hind-limbs and comes to rest not far from her mouth. When maternal assistance in freeing the newborn young from the fetal membranes is necessary, the mother's mouth is thus automatically in the correct position (Franklin and Winstone, 1954) . Tinklepaugh and Hartman (1930) observed that rhesus monkeys actually help pull the young out of the birth canal and then may pull on the cord with the hands, sometimes thus pulling out the placenta. The California sea lion has been observed to turn her head to her vulva and pull with her teeth at the hind flippers which were the only part of the fetus that has emerged. The mother elephant seal may assist during birth by ])ulling at the emerging young with her liind flippers (Slijper, 1956).

Not all mammals lick the fetal membranes or newborn young, or assist the young during birth. Hartman (1920) reported that the young opossum receives no assistance from its mother, in fact moving from the uterus to the mother's pouch without assistance. In the red kangaroo considerable interindividual variability may be seen (Hediger, 1958), but several observers have seen individuals of tiiis species which gave no direct assistance to the emerging


young (the mother lies on her back during parturition), but which, starting with licking in the neighborhood of the vulva when the placental membranes ruptured, continued to lick the underside of the body in a craniad direction, making a narrow track of fur saturated with saliva, which the young followed, thus reaching the pouch (Dathe, 1934; Grasse, Bourliere, and Viret, 1955).

Not all mammals lick the emerging fetus and assist it to emerge. The camelids (camels, llamas, etc.) neither lick the young nor appear to be attracted to the fetal membranes or fluids (Filters, 1954). Aquatic mammals such as the pinnipeds (seals, etc.) , although they sometimes assist in birth, do not lick the young. On the other hand, the hippopotamus, which also gives birth in the water, normally does not assist in birth or \m\\ on or bite the umbilical cord, but it may lick the young (Slijper, 1956).

The fact that in some mammals suckling relationships between mothers and young are adequately established in the absence of any tendency to lick the fetal membranes or the neonate, whereas in other species the licking activity of the mother clearly plays a role in establishing the relationship between mother and young (see below, p. 1312), suggests that (a) the processes of establishment of mother-young relationships vary widely from species to species, and (b) in those species in which licking does play a role, the possibility of the existence of other factors making a substantial contribution should not be minimized.

Interaction between mother and young at birth. In many species of mammals, the mother begins to react to the emerging young during parturition, and the mother's behavior toward the young at this stage is, in part, a continuation of her reactions to her own body at the end of pregnancy and the beginning of parturition. The behavior of the young is, of course, also characteristic of the species, both because of differences between the young themselves and because of differences in the situation in which they are placed by the varying behavior of the mother. This leads to different kinds of interaction between young and mothers in different species at the earliest stages of parturition and prenatal care.


1312


HORMONAL REGULATION OF BEHAVIOR


Behavior during and just after parturition is thus a mutual affair, involving the structure and behavior both of the mother and of the neonate. Young mammals vary widely with respect to the level of development at birth, some being born very small, blind, and helpless, others larger, well furred, and ready to take solid food within a day or two after birth (Hamilton, 1939). The young of some s]:)ecies are not capable of standing or walking for some time after birth, and thus can suckle only while lying under the mother (Wiesner and Sheard, 1933; Schneirla, 1956). The young of other species can stand almost immediately after birth and characteristically suckle in a standing position (Altmann, 1952; Hediger, 1952) . Clearly the behavior of the immediately i:)ostparturitive mother and that of the neonate must be adapted to each other. It will be recalled that the mother goat licks the newborn kid as the kid is leaving her body. After parturition, the (standing) mother continues to lick the kid, which is also standing, licking along the kid's back to its anus which is especially vigorously licked. When the mother is licking in the neighborhood of the kid's anus, the head of the kid is in the neighborhood of the mother's teats, and according to Blauvelt (1955), this arrangement of the licking behavior contributes to the first establishment of suckling. Somewhat similar observations are recorded by Altmann (1952) in the American elk. As Schneirla (1956) describes the behavior of the domestic cat during parturition, intervals of intense activity which facilitate the expulsion of the fetuses are interspersed with intervals of exhaustion and rest, which facilitate the initiation of a suckling relationship between the mother and the neonate. The neonate is brought into contact with the abdomen of the mother partly through the behavior of the mother (licking, lying down, etc.), and partly by its own crude orienting responses to tactual and thermal stimuli from the mother (Rosenblatt, cjuoted by Schneirla, 1956). Rowell (1960a) has made similar observations on the golden hamster.

Although information on behavior during parturition, and on the very earliest stages of mother-young relationship, are available for only very few species of mammals, it is


apparent that a wide variety of patterns of such behavior can be found in nature, and that a great deal yet remains to be learned about them.

2. Physiologic Aspects of Parturitive Behavior

In many species of mammals the mother, after licking herself and the emerging young, may tear the fetal membranes, bite through the umbilical cord, and eat the placenta. Placentophagy is widespread, occurring in many different families and orders. Thus the habit of eating the placenta is found among such widely differing mammals as bats (Allen, 1939; Wimsatt, 1945; Ramakrishna, 1950), ungulates (Hediger, 1942, 1955), rodents (Eibl-Eibesfeldt, 1958; Dieterlen, 1959), carnivores (Tembrock, 1957), monkeys (Tinklepaugh and Hartman, 1930; Carpenter, 1934), chimpanzees (Yerkes, 1935; Nissen and Yerkcs, 1943), and others.

Placentophagy is, however, by no means universal. In species in which it does occur, it may not occur in every case. For example, Nissen and Yerkes (1943) report that of 29 chimpanzee births observed by the authors, the whole placenta was eaten in 13 cases, bits of the placenta in 4 cases, and there was no eating of the placenta in 10 cases. In all 29 cases, however, the fluids associated with the placenta and amnion were licked up from the floor and from the infants. The camels and their relatives neither lick the young nor eat the placenta (Filters, 1954; Koford, 1957). In a number of aquatic animals, such as seals (Slijpcr, 1956), dolphins (McBride and Hebb, 1948; Tavolga and Essapian, 1957), the hippopotamus (Slijpcr, 1956), etc., the mother pays no attention to the placenta, neither licking it, eating it, or touching it, although she may in some of these animals bite through the cord.

It will not have escaped the attention of the reader that some of these animals which eat the placenta are, at all other times of their life, strictly herbivorous. Hediger (1955) describes how various ungulates, immediately after having given birth, "fall on the amniotic sac and devour it." He adds, "in this situation, the most decided herbivore turns carnivore all of a sudden. I saw


PARENTAL BEHAVIOR


1313


bison and antelo})e cows swallow such large mouthfuls that I was afraid they would choke." The domestic rabbit is also a voracious placentophage (Sawin and Crary, 1953 ) .

It is remarkable that practically no attention has been paid to the prol)lem of how a herbivorous animal is induced to become carnivorous at the time of parturition. A beginning is found in unpublished observations by Dr. Thales Martins, made at the American Museum of Natural History (quoted by Riess, 1950), who offered various diets to groups of guinea pigs, and found that pregnant females showed a significant preference for meat compared with other groups of these animals. Wiesner and Sheard (1933) offered fetuses obtained by cesarian section, with their membranes and with the l^lacenta attached, to some female rats which had given birth about 12 hours previously. The majority of these animals did not respond to the fetus or placenta, although they had, on the day before, delivered and cleaned their own young. They further report that nulliparous females never cleaned or ate fetuses in membranes offered to them, although they accepted pieces of raw meat.

Allan and Wiles (1932) hypophysectomized 12 pregnant cats. Eleven of these animals ignored the kittens at birth, doing no licking, tearing of the membranes, or eating of the placenta. The 12th animal abandoned its kittens when they were 2 days old. Similar results were obtained by Smith (1954) who hypophysectomized 10 pregnant rhesus monkeys, and found that pregnancy and ])arturition were carried through normally except for unusually difficult labor (sec Cross, 1959). Nine of the animals failed to eat the afterbirth, although a few licked it. These data certainly suggest that licking of the fetus and eating of the afterbirth depend on the hormonal condition of the parturient mother. It is to be noted that nutritional requirements of pregnant rats differ in some respects from those of nonpregnant animals, for example, in increased need for salt (Richter and Barelare, 1938), and future research may show some relationship between these changes in nutritional needs and the tendency to lick and eat the placenta. It should he noted that most animals seem to be able to select varying diets in


accordance with varying nutritional needs (Young, 1949, 1959). When the sympathetic ganglia of i^regnant cats were removed, the animals did not lick or clean the kittens after parturition (Simeone and Ross, 1938). We might speculate on whether this is due to an effect of maternal sympathectomy on the characteristics of the kitten, on those characteristics of the mother's body which lead to self-licking, or on characteristics of her central nervous system.

Mothers may occasionally eat their neonate young. This happens not infrequently in the domestic rat (Wiesner and Sheard, 1933) and in the domestic mouse (Brown, 1953), and is also seen in the domestic rabbit (Sawin and Crary, 1953). It is not clear what factors contribute to this form of cannibalism, although usually the eating of the infant follows the eating of the placenta and umbilical cord (Wiesner and Sheard, 1933). Indeed, in an animal which is, at the moment, so voraciously carnivorous, the question of why the mothers do not usually eat their young may be just as reasonable a question as that of why the mothers sometimes do eat them. Eibl-Eibesfeldt (1958), on the basis of his (nonexperimental) observations of parturitions in the domestic rat, believes that the eating of the young is inhil)ited by a vocalization emitted by the young, which is in part stimulated by the mother's eating of the umbilicus.

It is clear that the behavior of the mother toward the newly born young and toward the placenta, particularly in herbivorous animals, presents a number of problems the investigation of which is now at its earliest stage. C. RETRIEVING OF THE YOUNG

1. Retrieving Behavior

The retrieving to the nest of young which have strayed or become scattered is characteristic of many species of mammals (Causey and Waters, 1936; Wunder, 1937). Different species normally have different ways of managing to retrieve the young. Everyone is familiar with the way domestic cats

" Much additional information on parturition may hv found in the monograph by SUjper (1960), which appeared too late to be considered in the preparation of this chapter.


1314


HORMONAL REGULATION OF BEHAVIOR


pick up their kittens by the nape of the neck (Leyhausen, 1956) . Various species of rodents characteristically pick up the young with the mouth, seizing them in the middle of the back, by the skin of the belly, or on the flank (Curio, 1955; Eibl-Eibesfeldt, 1958) . At least in the domestic rat, considerable individual differences can be seen, these animals having been seen to pick up young by about 20 different parts of their bodies (Wiesner and Sheard, 1933; Causey and Waters, 1936) . Retrieving of the young may be done very vigorously and persistently. One European yellow-necked mouse has been seen to retrieve, in quick succession, 148 young which had been placed in different parts of the living space by the experimenters (Zippelius and Schleidt, 1956).

Some mammals use methods of retrieving the young other than carrying them in the mouth. Some opossums carry their young on the back (Wunder, 1937). Blair (1941) observed that young northern pigmy mice become attached to the nipples of the mother and are dragged about wherever she goes. Similar methods are seen in some bats, in which the young either cling to the underside of the mother's body or attach themselves to the nipple, and are carried by the mothers on their hunting trips (Wunder, 1937; Hamilton, 1939). Beach (1939b) reported that young Central American opossums remain continuously attached to the mother's nipples. When one of the young becomes detached, the mother noses it back under her belly, upon which the young animal rolls over on his back, grasps the mother's ventral hair, and moves over her ventral surface until it finds a nipple and becomes attached.

Young bicolored white-toothed shrews sometimes follow the mother in a "caravan," in which the first young grasps the mother's tail near its base, and the successive young each similarly grabs in its mouth the tail of the young in front of it (Wahlstrom, 1929; Zippelius, 1957).

In some aquatic mammals, the mother may retrieve the young by swimming after them and guiding them back into place when they get too far away. When the young bottle-nosed dolphin strays from its mother's side she swims after it and pushes


it gently, guiding its direction until it is close to her side again (Tavolga and Essapian, 1957) . Mother dolphins support the young to the surface after parturition (McBride and Hebb, 1948; :\lcBride and Kritzler, 1951), and mother dolphins have been seen thus supporting dead young or the remains of dead young (Hubbs, 1953; Moore, 1955).

The domestic rabbit does not seem to retrieve its young (Ross, Denenberg, Frommer and Sawin, 1959), unlike rats which do retrieve, although both nest in burrows.

Retrieving by the male. In most mammals the mother alone attends to the rearing of the young, the father paying little or no attention to them (Bourliere, 1954; Hediger, 1955). In some species, however, retrieving of young by the male has been noted. Horner ( 1947 1 reported that male deer mice in captivity often retrieve the young, and Frank (1952) observed the same thing in the common vole of Europe, as did Leblond (1940) in the domestic mouse. On the other hand, the male laboratory rat, at least under the conditions in which such animals are normally kept in the laboratory, does not appear to retrieve the young (Seitz, 1958). ^lale Galapagos sea lions take part in the care of the young, shepherding them back to shore when they swim far off (Eibl-Eibesfeldt, 1955c), in contrast to most seals, in which the male pays no attention to the young (Bartholomew, 1952, 1953).

£. Physiologic Regulation of Retrieving Behavior

Correlation of retrieving behavior and PHYSIOLOGIC CONDITION. There is considerable evidence that the tendency to retrieve young is linked to, or somehow dependent on, the physiologic conditions associated with the end of pregnancy and the period of lactation. Rabaud (1921a, b) found that pregnant domestic mice began to retrieve young mice offered by the experimenter at about the middle of pregnancy (9 or 10 days) . He noted further that retrieving becomes more intense just after parturition, and that, when a pregnant female and a recently postparturitive female were both in a cage, the pregnant one always gave way when both animals attempted to re


PARENTAL BEHAVIOR


1315


trieve young. Wiesner and Sheard (1933) found that 19 of 21 primiparous rats tested just after parturition showed the retrieving response to the young, whereas of 21 pregnant nulliparous rats tested 1 to 7 days before parturition, only 4 retrieved young. In another test, they found that only 6 of 34 pregnant nulliparous females tested 1 to 9 days before parturition showed any retrieving behavior. Rowell ( 1960b) found that ]iregnant and nonpregnant female golden liamsters accepted and retrieved only 3 out of 33 pups, in contrast to postparturitive animals, which usually accepted and retrieved young pups. In a somewhat similar series of observations Labriola (1953) offered young rats to 10 nonpregnant nulliparous females and to 10 females which had given birth 24 hours previously. None of the nonpregnant animals retrieved any young; all of the postparturitive animals did.

Herter and Herter (1955) found that a pscudopregnant polecat retrieved domestic kittens. Retrieving by pseudopregnant animals has also been noted in the domestic rat (Herold, 1954) and in the dog (Lang, 1931).

Retrieving, of course, continues during the lactation period (Wiesner and Sheard, 1933). The data presented so far might suggest that retrieving behavior is limited to the period at the end of pregnancy and the lactation period following parturition. Unfortunately, the situation is not quite that simple. About 20 per cent of domestic rats retrieve regardless of sex or reproductive condition (Wiesner and Sheard, 1933; Riddle, Hollander, Miller, Lahr, Smith and Marvin, 1942; Riddle, Lahr and Bates, 1942). Frank (1952) found that males and nonpregnant females of the common vole often retrieve young, although not as often as postparturitive females. Leblond (1938, 1940) presented young rats to 12 female rats that were some 6 to 24 weeks past their last parturition, and in which lactation had ceased. Ten of the 12 animals retrieved, retrieving occurring in 90 per cent of the tests.

Rowell (1960b) found that young golden hamsters begin to retrieve younger pups as soon as they are strong enough, and that this retrieving behavior disappears with the onset of aggressive l)ehavior, which ap


pears at different ages in animals reared under different conditions.

The incidence of retrieving behavior suggests a parallel with that of nest-building behavior. Both types of behavior are observed to occur in the mouse starting at 9 or 10 days of pregnancy, whereas in the rat the onset is later, closer to the time of parturition. Both types of behavior are also seen in males and in nonpregnant females, to a lesser degree, and to varying extents by different observers, probably under different conditions. Unfortunately, there does not exist a good study of the correlation between these two types of behavior during a normal reproductive cycle. The best studies of nest-building behavior, such as those of Roller (1952, 1956), were done under conditions in which retrieving was not readily observed, and the best studies of retrieving, such as those of Wiesner and Sheard (1933) and of Beach and Jaynes ( 1956a, b, c) , w^ere done on animals in which nest-building behavior was not being studied. In a number of other studies, nestbuilding and retrieving were lumped together in order to construct a "maternal behavior" score, which was then used without further differentiation of its components (Leblond, 1940). Closer study of the details of variation between individuals, between species, and during the breeding cycle should be rewarding.

Hormonal induction of retrieving behavior, (a) Hypophyseal hormones. Collip, Selye and Thomson (1933) hypophysectomized female rats shortly after parturition, or later during lactation. Lactation ceased and the mammary glands regressed, but retrieving and other aspects of maternal care continued. Other observers have noted that hypophysectomy does not interfere with retrieving behavior (Leblond and Nelson, 1937a; Obias, 1957), even though lactation is suppressed (Leblond, 1940).

Using a more quantitative approach than the earlier investigators, Riddle, Lahr and Bates (1942) found that hypophysectomy actually increased retrieving behavior. In both male and female rats, hypophysectomized animals retrieved on 68 to 75 per cent of the tests, compared with only 21 to 23 per cent for intact animals.

The apparently contradictory results of


131()


HORMONAL REGULATION OF BEHAVIOR


Allan and Wiles ( 1932) must be mentioned at this point. They found that cats hypophysectomized during pregnancy deserted their kittens immediately after parturition. Since hypophysectomized rats retrieve apparently normally, even when the hypophysectomy was accomplished during pregnancy (Obias, 1957), the different results obtained by Allan and Wiles presumably represent a difference between cats and rats with respect to the method of control of the mother's behavior toward the young.

Erhardt (1929) induced a nonpregnant female rhesus monkey to adoi)t a neonatal guinea pig by injecting her with an anterior l^ituitary extract. Since that time, considerable additional evidence has accumulated implicating hypophyseal hormones in the regulation of retrieving behavior. Riddle, Lahr and Bates (1942) found that prolactin caused substantial increases in retrieving behavior in both male and female rats, whether intact or gonadectomized (Riddle, Lahr and Bates, 1935a, b; Riddle, Hollander, Miller, Lahr, Smith and Marvin, 1942). Luteinizing hormone was similarly able to increase retrieving behavior. The fact that the luteinizing hormone increased retrieving even in gonadectomized animals suggests that there was present in this preparation some material capable of acting directly on nongonadal parts of the soma, and Riddle and Bates (1939) note that Riddle's luteinizing hormone preparations contained "some" prolactin. Prolactin, of course, exerts a luteotrophic action on the ovary (Meites and Shelesnyak, 1957), but since it is effective in inducing retrieving behavior in gonadectomized animals, its luteotrophic effect cannot be the only source of its action in this situation.

FSH seems to have no effect on retrie\-ing behavior (Riddle, Lahr and Bates, 1935a). Animals injected with this substance retrieved young in about the same percentage of cases as did untreated animals (Riddle, Lahr and Bates, 1935b).

ih) r/iyro/f/. McQueen-Williams (1935a, b ) found that removal of the thyroid glands in male rats induced retrieving and other aspects of parental care of the young, a finding confirmed by Riddle, Lahr and Bates (1936). Thyroidectomy increased the incidence of retrieving in tests of male rats


from about 21 per cent to about 45 per cent (Riddle, Lahr and Bates, 1942).

Dispensa and Hornbeck (1941) injected desiccated thyroid into rats during pregnancy and found no effect on retrieving or other aspects of maternal care. Chu (1945) found that rabbits that became pregnant after thyroidectomy Jailed to care for the young. It should be noted, however, that the behavior of the rabbit differs from that of the rat in that retrieving does not normally occur in this species (Ross, Denenl)erg, Frommer and Sawin, 1959).

(c) Gonads. Castrated male mice show retrieving behavior after some association with the young (Leblond, 1940), but no data are available to indicate whether this behavior is more frecjuent or more intense than that normally shown by intact males in the same laboratory. Riddle, Lahr and Bates (1942) noted that castration does not itself appreciably increase retrieving behavior in either male or female rats. However, almost all of the substances which, in their study, were found to increase retrieving behavior ie.g., prolactin, "luteinizing iiormone" etc.) were more effective in gonadectomized (whether male or female) than in intact animals.

Testosterone injections cause some increase in retrieving behavior in castrated males, intact females, and ovariectomized females, but not in intact males (Riddle, Lahr and Bates, 1942). Fisher's (1956) local injections of sodium testosterone sulfate into the hypothalamus induced retrieving behavior in some cases. As I noted in connection with the induction of nest-building in Fisher's experiment, no data yet exist for comparison of the effects of this androgen with those of other hormones applied in the same manner.

Riddle, Lahr and Bates (1936) found that progesterone was as effective in increasing retrieving behavior as was prolactin.

Retrieving behavior seems to be supjiressed by the administration of estrogenic substances. Riddle, Lahr and Bates (1942) treated virgin female rats with estrone for 20 to 26 days. Under this treatment, the mammary glands developed to a degree similar to that found late in pregnancy, but none of the experimental animals would retrieve 3-day-old young rats during the pe


parp:xtal behavior


1317


liod of estrone treatment. Retrieving, and other aspects of maternal behavior, were shown by these animals after withdrawal of the estrone treatment. Weicliert and Kerrigan (1942) found that mother rats mjected with estrogen during the lactation l)eriod allowed the young to become scattered over the cage without retrieving them, and that the young were often found cold outside the nest. Similarly Riddle, Hollani\cr, Miller, Lahr, Smith and Marvin (1942) found that estrone tends to terminate established maternal behavior. They report, however, that this does not happen in hypophysectomized rats.

Apparently contradictory results have l)een reported by Leblond (1938) who found tliat male domestic mice showed retrieving behavior after estrin treatments or the implantation of ovarian grafts. Moore (1919) implanted ovaries in gonadectomized male rats, and reported that they subsequently showed maternal behavior, including retrieving. Intact male rats similarly implanted with ovaries did not exhibit such behavior. Similar treatment failed to induce maternal behavior in the guinea pig (Moore, 1921).

(d) Summary remarks. These data on the hormonal induction of retrieving are rather confused, chaotic, and in many cases contradictory. There has not yet been a study of this problem with a design in which the experience gained during the early experiments was utilized, or in which the imjiortance of statistical analysis was anticipated, or in which a broad range of causal factors was comprehended.

In spite of these inadequacies, a number of points may tentatively be made. The fact that hypophysectomy and prolactin administration both increase the incidence of retrieving behavior suggests that prolactin acts by means of its antigonadotrophic effect. However, prolactin increases retrieving behavior both in hypophysectomized and in gonadectomized animals, which renders it unlikely that prolactin affects retrieving through either antigonadotrophic or luteotrophic effects. The alternative possibility is that hypophysectomy and prolactin, although they both cause increases in retrieving behavior, do so in different ways, or through different kinds of


effects on the animal. Closer qualitative analysis of the fine details of the behavior of animals treated in the various ways reported here will undoubtedly reveal many differences that have been obscured in the relativelv crude treatments undertaken so far.

Certain similarities between the physiologic bases of nest-building behavior and of retrieving should be noted. Hypophysectomy and thyroidectomy enhance both types of behavior. Progesterone induces both retrieving in rats and nest-building in mice. Even more suggestive, estrogen treatnrent seems to have the same effect on both types of behavior. It inhibits it during treatment, but causes it to rise above the pretreatment level after withdrawal of the hormone treatment. However, the fact that prolactin induces retrieving behavior (at least in rats), whereas it does not have any effect upon nest-building behavior in the mouse, suggests that the physiologic bases of the two types of behavior are not entirely identical. Coordinated study of both types of behavior in both species would obviously be useful.

Induction of retrieving behavior by external STIMULI. As Beach (1951) pointed out, the stimulation of retrieving behavior by stimuli provided by the young really presents two quite different problems. First, it is possible that stimuli provided by the young can induce a physiologic state which underlies the capacity to display retrieving behavior. Secondly, there is the problem of what stimuli induce an animal that is physiologically capable of retrieving to do so, and to retrieve some objects rather than others. We shall discuss these problems separately.

ia) Induction of readiness to retrieve by stimuli from the young. Wiesner and Sheard (1933), who found that only about 20 per cent of nulliparous, nonpregnant female rats would retrieve young offered to them by the experimenter, succeeded in arousing readiness to retrieve in many of the "nonretrievers" by confining them in cages with young rats for several days, the young being replaced every 2 days by fresh ones. By this procedure, which Wiesner and Sheard called "concaveation," retrieving behavior was induced in 25 out of the 74 nonreactors


1318


HORMONAL REGULATION OF BEHAVIOR


so tested. Retrieving behavior began from 1 to 4 days after the young were introduced into the cage. Leblond (1938) made similar observations in domestic mice. When he tested 14 virgin female mice, none retrieved young. After concaveation for 2 to 4 days with young mice, 12 of the 14 began to retrieve. This procedure also induced retrieving behavior in previously nonretrieving hypophysectomized mice (Leblond and Nelson, 1936, 1937a), and male mice (Leblond, 1940).

The question arises whether the concaveation procedure really induced a change in underlying physiologic condition, conducive to the onset of retrieving behavior, or whether it merely represents the sampling effects of testing on a number of different days, thus increasing the probability of finding retrieving behavior in animals whose readiness to retrieve varies from day to day. As Wiesner and Sheard (1933) point out, the evidence clearly favors the assumption that exposure to the young does in fact change the condition of the adult being tested. Animals which are found to retrieve without concaveation usually continue to retrieve throughout the period of observation. In addition, removal of the young after retrieving behavior has been established through concaveation results in the disappearance of the retrieving response, as determined by tests some days later.

The nature of the physiologic change induced by concaveation is not clear. Since concaveation induces retrieving behavior in hypophysectomized mice (Leblond, 1937, 1940), we cannot assume that its effect is through the stimulation of hormone secretion. As we have noted in connection with other aspects of retrieving behavior, there are certain similarities between effects of the young on retrieving behavior and on the nest-building behavior observed by Roller (1952, 1956). Both can be induced by confining young with the animals being tested, and both can be induced in hypophysectomized animals. However, Weisner and Sheard (1933) found that individual rats in which retrieving was induced by concaveation would not necessarily show aiiv onset of nest-building behavior associated with this retrieving. We must thus reiterate


that, whereas the physiologic bases of nestbuilding and of retrieving (at least in domestic rats and mice) undoubtedly have much in common, they are probably not identical.

(6) Stimuli eliciting retrieving responses. The stimuli by means of which young animals induce retrieving behavior on the part of the parents may vary considerably from species to species, although information on this problem is fragmentary and incomplete, even for most of the widely used experimental animals. Scott (1945) reported that domestic sheep respond to the sounds of their bleating lambs, and Beach (1951) observed that the squeals uttered by young laboratory rats in response to painful stimulation elicit greatly increased activity in the lactating female. Similar observations have been made on wild meadow mice (Bailey, 1924) and rice rats (Svihal, 1931). According to Zippelius and Schleidt (1956), young of the common vole, domestic mouse, and European yellow-necked mouse induce retrieving behavior on the part of their parents, in part, by uttering supersonic cries with frequencies in the neighborhood of 70 to 80 kc. Domestic cats retrieve their young in response to the cry given by a kitten separated from its mother (Leyhausen, 1956).

Auditory and visual stimuli are also effective. Anesthetized young European yellow-necked mice may be found and retrieved by their mothers, although only if the mother passes close to them, in contrast to active young, wdiich attract the mothers from a considerable distance by their supersonic calls (Zii)pelius and Schleidt, 1956 1. Dieterlen (1959) and Eibl-Eibesfeldt (1958) have made observations which suggest that olfactory stimuli are effective in inducing retrieving behavior in the golden hamster and laboratory rat.

Beach and Jaynes ( 1956a, c) have shown that several different sensory modalities contribute to the stimulation of maternal retrieving behavior in the laboratory rat. The importance of olfaction is demonstrated by the following facts: peripherally blinded females spent more time investigating a small cage made of fine copper-wire mesh containing a young rat than they did a similar cage containing no young rat, whereas arosmic females failed to distin


PARENTAL BEHAVIOR


1319


guish between the two cages: young rats sprayed with oil of hivender, and subsequently dried, were retrieved by most females less efficiently and less rapidly than untreated young. Visual stimulation is also significant: when female rats were placed in cages each containing a pair of glass bottles sealed to the floor of the cage, only one of which contained a young rat, 17 of the 25 females which investigated the bottles spent more time at the bottle containing a live young rat than at the empty bottle; on retrieving tests in which intact females were oftered normal young and motionless young, there was a tendency for the active young to be retrieved more rapidly. Although freshly killed young were retrieved almost as quickly as normal young, young refrigerated for a short time after being killed were retrieved significantly more slowly. It is not possible to say whether this difference in reaction is based upon olfactory, temperature, or tactual cues. Although a number of stimulus modalities are clearly important, the rats could retrieve in the absence of any one of the modalities tested {i.e., vision, olfaction, cutaneous sensitivity around the mouth). Animals deprived of any 2 of these sensory capacities retrieved less efficiently than animals deprived of only 1, and animals rendered blind, anaptic, and anosmic were the poorest retrievers of all. It is clear from this and other work {e.g., McHugh, 1958) that a variety of different stimuli in different sensory modalities may contribute to the stimulation of retrieving behavior.

Younger mice apparently stimulate more retrieving and other aspects of maternal care than older animals (Wiesner and Sheard, 1933). Leblond (1940) found that 0- to 1 -day-old mice were retrieved by lactating females 83 to 85 per cent of the time, whereas 15-day-old young were retrieved only 11 to 15 per cent of the time, the decrease being a steady and gradual one, as revealed by tests using young of intermediate ages. Younger animals provide stronger stimuli for retrieving than older ones even for lactating mothers whose own young are older. Indeed, Wiesner and Sheard (1933) report that, at the end of lactation, the grown-up litter no longer represents an adequate stimulus for retrieving, although the


mother may vigorously retrieve newborn young presented to her. Menzel and Menzel (1953) replaced older puppies with very young ones, and found an increase in maternal care by the mother dog. Presented with newborn puppies, she acts just like an immediately postpartum female. This replacement of older by younger puppies can be effected twice in one lactation period, with the same results.

The most exact and quantitative study of this problem is the very recent one by Rowell (1960c), who studied the retrieving responses of lactating female golden hamsters at various ages postpartum, in response to young of various ages. She found that variations in the amount of maternal retrieving are influenced by three types of variables: (a) the time since the birth of her own litter; (b) similarity between the age of her own young and that of the test young; and (c) variations in the stimuli coming from the test young, which elicit retrieving responses when they are 7 to 10 days old more efficiently than they do at any other age, regardless of the kind of female being tested. Rowell further found that the amount of time spent licking the young, after having retrieved them, decreased steadily and reliably during lactation. Using a litter-replacement technique, she kept various groups of mothers with young of different ages, so that, e.g., some mothers constantly had 2- to 6-day-old litters, some 10- to 14-day-old litters, etc. Under these conditions, the decrease in licking time, characteristic for normal litters, did not occur. Further, these females licked their pups for approximately the same amount of time as was characteristic, in a normal litter, for young of the same age as the test pups. Thus the change in licking time, which always occurs postpartum, is a function of growth changes in the ability of the young to stimulate licking behavior, rather than of physiologic changes in the mother.

The stimuli inducing retrieving behavior are not necessarily specific to the species, as there are many instances recorded of small mammals retrieving young of other species. The laboratory rat readily retrieves young mice (Wiesner and Sheard. 1933; Shadle, 1945; Herold, 1954; Beach and Jaynes, 1956b). When mother laboratory


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HORMONAL REGULATION OF BEHAVIOR


rats are simultaneously given young mice and rats to retrieve, they show some preference for the rats (Wiesner and Sheard, 1933). The common vole retrieves young red-backed voles or field voles offered by the experimenter (Frank, 1952). Cotton rats adopt young laboratory rats (Meyer and Meyer, 1944). Dogs readily adopt puppies of other strains (Menzel and Menzel, 1953) , and a polecat has adopted domestic kittens (Herter and Herter, 1955). Kallmann and von Frisch (1952) and Eibl-Eibesfeldt (1958) have summarized observations from many different sources which indicate that many small mammals may adopt young belonging to different species, genera, and even families.

Rats will, however, not retrieve young of all other species. Wiesner and Sheard ( 1933 1 offered pairs of 1- to 6-day-old rabbits and rats simultaneously to each of 49 lactating female rats, and found that 28 retrieved both the young rat and the young rabbit whereas in 21 cases only the rat was retrieved. In no case did the mother rat retrieve a rabbit while leaving the young rat. Beach and Jaynes (1956b) report that rats will not retrieve young guinea pigs, which, of course, are much larger and more active than 1- to 6-day-old rabbits or rats.

In spite of the fact that they may retrieve young of other species, lactating females of at least some species of mammals discriminate between their own young and other young of the same species, and tend to prefer their own young. When Beach and Jaynes (1956c) tested 16 lactating female rats in several situations in which the retrieving of their own young could be compared with retrieving of other young rats the same age as their own, all but one of the mother rats tended to prefer their own young. When "own" and "alien" young were presented separately, there was a tendency for the own young to be retrieved faster; when the own and the alien young were presented to the mother rat together, there was a tendency for the own young to be retrieved first. Wiesner and Sheard (1933) had found no evidence of preference for retrieving of their own young, but as Beach and Jaynes i)oint out, the earlier tests were considerably less sensitive than the tests used by them. Domestic mice, although they


may retrieve alien young of their own species, will often subsecjuently eat them (Eibl-Eibesfeldt, 1950). When golden hamsters are offered strange young they often eat them (Lauterbach, cjuoted by EiblEibesfeldt, 1958). Leblond (1937) points out that domestic mice at first accept alien young as readily as they do their own, and that attachment to their own young develops later.

The stimuli on the basis of which mothers recognize their own young may vary among different types of mammals. In the Galapagos sea lion, maternal care is restricted to the mother's own young. Eibl-Eibesfeldt ( 1955c) observed that mothers respond only to the calls of their own young, and that they apparently also recognize their young by sniffing at them. In the case of the American elk, on the other hand, Altmann (1952) found that mothers reject strange young on the basis of olfactory and probably also visual cues, whereas the calls of any young are reacted to by many females. Observations by McHugh (1958) indicate that olfactory, visual, and auditory cues are all used by female American bisons in identifying their young.

Beach (1951) noted that considerable individual variability may be seen in the laboratory rat with respect to recognition of the young. Although some females consistently retrieve their own young in preference to others, other individuals seem to make no such distinctions. Similarly, Menzel and Menzel (1953) find that some female dogs only accept their own young, whereas others will readily accept strange puppies. It is not known whether such individual differences exist among nondomesticated species.

Although it may at first seem somewhat contradictory to state that animals which readily adopt young of other species are capable of discriminating their own young from other young of the same species and age, the contradiction is more apparent than real. Most of the experiments on "adoption" of young of other species have involved the presentation of the strange young under conditions in which there was no possibility of choosing between the alien species and the mother's own species. Where such choices are possible, the tendency to prefer


PARENTAL BEHAVIOR


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young of the iiiothei-'s own species is readily seen.

D. NURSING AND SUCKLING BEHAVIOR

In discussing the l)ehavioral and physiologic aspects of mother-young relationships centering around feeding, I shall use the terminology suggested by Cowie, FoUey, Cross, Harris, Jacobsohn and Richardson (1951). "Nursing" means behavior on the part of the mother which fosters access to the nipples by the young. "Suckling" is the activity of the young animal sucking the nipple. "Suckling stimulus" is the sum of the stimuli applied by suckling.

1. Behavior of the Nursing Mother

The duration of the period of lactation, which starts about the time of parturition, varies considerably in different species. The young of some species of rodents may feed independently of the mother by the time they are 10 to 14 days old. In other species the nursing period is much longer. Herdliving animals usually nurse the young for several months, whereas some aquatic mammals, such as the sea lions, may continue nursing for up to a year. These differences in duration of the nursing period are, in part, correlated with the conditions of the animal's life. The young of mammals which live in burrows are usually able to get food without the help of the mother by the time they are old enough to leave the burrow; grazing herd-living types tend to remain with their mothers in the herd for a much longer time. The differences in kind and duration of the mother-young relations in these two types of mammals are undoubtedly relevant to the differences in gregariousness which characterize them as adults (Krumbiegel, 1955). This rather general statement is about as far as we can go, because detailed studies of motheryoung relationships, suitable for comparative analysis, exist for only a few mammalian species.

I have already pointed out (see al)0ve, p. 1312) that the establishment of a nursingsuckling relationship between mother and young is a mutual affair, depending on the behavioral characteristics of both participants. Changes in both the mother and young also contribute to the changfintr i-cln


tionships during the later stages of lactation. The best and most detailed analysis of such a relationship is to be found in still unpublished studies on the domestic cat carried out by Rosenblatt, Wodinsky, Turkewitz and Schneirla, at the American Museum of Natural History, and partially summarized by Schneirla (1956, 1959). These workers found that the kittens begin to discriminate among the mother's nipples very shortly after birth. Significant and persistent preferences of individual kittens for specific nipples can be detected before they are 2 days old (Ewer, 1959). In the early days of the kittens' life, nursing episodes tend to be initiated by the behavior of the mother, whereas later nursing episodes are initiated by approaches of the kittens to the mother. The transition is not entirely gradual, but occurs fairly abruptly between the 18th and 27th days after birth.

The mother domestic cat, like many other animals, spends most of her time with the young during the first few days after parturition. Depending on the species, other patterns are also found. The domestic rabbit and European hare, for example, visit the nest only to nurse the young, leaving it at the end of the nursing episode (Cross and Harris, 1952; Krumbiegel, 1955). Bartholomew and Hoel (1953) found that mother Alaska fur seals stay ashore with their young for 1 to 3 days, then leave and stay at sea for 3 to 10 days (Bartholomew, 1959).

Tiie decline of lactation is associated with changes in nursing behavior. The time spent on the nest by domestic mouse mothers decreases from parturition to about 15 days postpartum, and this decrease is paralleled by a decrease in the average length of the nursing episode (Bateman, 1957). Similar observations have been made on dogs which, as lactation declines, assume the nursing liosture less and less frequently (Martins, 1949). Hafez (1959), in a brief report, states that day-to-day variations in nursing intervals in the domestic pig are small compared with the individual differences between animals.

'£. ^filk Ejection

The physiology of milk ejection and of lactation are fully discussed in the chapter


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by Cowie and Folley, and we need not consider them exhaustively here. However, it will be useful to consider certain aspects of the physiology of milk production which directly influence, or are influenced by, the behavioral interaction between mother and young.

The viUk-eiection reflex. When a young mammal suckles, and thus withdraws milk from the mammary gland of its mother, only a small portion of the milk present in the mammary gland at the beginning of the nursing episode is available near the nipple so that it can be withdrawn by the young without active participation on the part of the mother. Most of the milk cannot be extracted without some active participation by the mammary gland, which normally occurs in response to the suckling stimulus (Folley, 1956; Harris, 1958). This active participation of the mammary gland in the ejection of milk, in response to a suckling stimulus, is called "the milk-ejection reflex" (Cowie, Folley, Cross, Harris, Jacobsohn and Richardson, 1951).

The phenomenon of milk ejection has long been known among dairy workers, by whom it has been called "milk let-down" (Ely and Petersen, 1941), a term referring to the sudden flow of milk which occurs 30 to 90 seconds after the beginning of suckling (Harris, 1958). This is commonly observed in the milking of dairy cows, and has been described as occurring in the domestic rabbit (Cross, 1952), in which the suckling young are veiy active for 30 to 90 seconds after the beginning of suckling, then suddenly become motionless, simultaneously with the beginning of a characteristic gulping sound which indicates that substantial milk flow has begun. By removing the puppies from the nipples of a lactating dog once every minute during a nursing episode, replacing them with other puppies, and then weighing the puppies which had just been allowed to suckle, Gaines (1915) was able to estimate the amount of milk produced by the lactating bitch during each minute of the suckling episode. He found that the flow of milk was very slow during the first minute or so, but then quickly increased. These observations make it clear that the flow of milk during nursing is in part an active response of the mammary gland to


the suckling stimulus, with a latency of 30 to 90 seconds.

Gaines (1915) allowed puppies to suckle an anesthetized lactating bitch, and found that they could not withdraw milk from the mammary gland. Similarly, Cross and Harris (1952) anesthetized a lactating female rabbit, and found that suckling young could obtain no milk from her even after 6 minutes of vigorous suckling, although in normal nursing most of the milk is withdrawn within the first 5 to 6 minutes (Cross, 1952). The milking of amputed cow udders yields considerably less than half the amount which can be got from the same udders, containing the same amount of milk, in the intact cow (Hammond, quoted by Harris, 1958) . It is clear that not much milk can be withdrawn, even by normal suckling behavior, from an inactive, nonparticipating mammary gland.

Tgetgel (1926) measured the pressure of milk in the cistern of the mammary gland of a cow (see chapter by Cowie and Folley) , and showed that it rose gradually between one milking episode and the next. This is, of course, a consequence of the gradual increase in the amount of milk present in the gland as milk is produced in the alveoli (milk-secreting tubules) to replace that withdrawn at the last milking episode. However, in addition to this gradual rise in pressure between milking episodes, Tgetgel noted an abrupt increase in intramammary pressure as a response to the application of the milking stimulus, even when it was applied shortly after milking when the overall pressure in the gland was low. Gaines (1915) had earlier made similar observations on the goat. This rise in milk pressure tends to squeeze the milk out through the nipple. Normally, the nipple's sphincter offers resistence to this pressure, which must be overcome by the mouth of the suckling. However, if a cannula is inserted through the nipple opening, the milk can actually l)e seen to spurt out of the nipple (Usuelli and Plana, quoted by Folley, 1956).

This increase in intramammary pressure no doubt constitutes the milk-ejection reflex.

Mechanism of milk ejection. What stimulates the mammary gland to eject milk


PARENTAL BEHAVIOR


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and how is this stimidation conveyed to the ghxnd?

The now generally accepted interpretation of the physiologic basis of the milkejection reflex was first suggested by Ely and Petersen (1941j. They found that motor denervation of one half of the udder of a lactating cow had no effect on either lactation or milk ejection. Further, injection of oxytocin, which is normally produced by the posterior lobe of the pituitary gland, caused milk ejection in cows that were not being milked or suckled. They therefore suggested that the sensory side of the milk ejection reflex consists of stimulation of the nipple by the suckling stimulus, whereas the motor side consists of the release of oxytocin by the posterior lobe of the pituitary gland, which, when it reaches the mammary gland in the circulating blood, directly causes an increase in intramammary pressure and the subsequent ejection of milk.

Andersson (1951a, b) demonstrated that milk ejection in sheep and goats can be induced by direct stimulation of the anterior hypothalamus by implanted electrodes. Cross and Harris (1951, 1952) obtained similar results in the rabbit. They showed that milk ejection occurred in response to electrical stimulation of the supra-opticohypophyseal tract, and that electrolytic lesions in this region interfered with its occurrence. Lesions in the dorsal and posterior hypothalamus did not have this effect (see also Shimizu, Ban and Kurotsu, 1956 ». Cross and Harris (1951) also found milk ejection following electrical stimulation of the pituitary stalk. Benson and Cowie ( 1956) found that removal of the posterior lobe of the pituitary gland abolished the milk ejection response, and that later, after hypertrophy and reorganization of the cut end of the neural stalk, the response was restored. These observations provide confirmation of Ely and Petersen's (1941) hypothesis that the ejection of milk is stimulated in the mammary gland by a hormone secreted by the posterior pituitary. Further evidence is found in the fact that direct stimulation of the hypothalamus increases milk ejection in denervated udders as well as in udders whose neural connection to the central nervous system is intact (Andersson, 1951a). Even more dramatic is the fact


that an isolated perfused mammary gland ejects milk when perfused with blood from a cow that has just been suckled, and does not do so when perfused with blood from a cow that was not ejecting milk at the time the blood was withdrawn (Petersen and Ludwick, 1942).

Cross (1950, 1951) found that suckling in rabbits caused an inhibition of urine flow similar to that caused by the injection of posterior pituitary extracts. Andersson and McCann (1955) observed that milk ejection elicited by hypothalamic stimulation in the goat is accompanied by this antidiuretic effect. Hawker and Roberts (quoted by Harris, 1958) assayed the blood in the jugular veins of goats and cows before, during, and after milking. They found the amount of oxytocic hormone in the blood of goats to be higher during milking than before or after. In cows the level of oxytocic hormone activity rises some minutes before the beginning of milking, presumably in response to stimuli associated with the preparations for milking.

It is abundantly clear that milk ejection is stimulated by posterior pituitary substances secreted into the blood in response to suckling stimulation. It is beyond the scope of this chapter to consider in detail which of the substances secreted by this gland is the milk ejection hormone, but overwhelming evidence suggests that it is oxytocin (see chapter by Cowie and Folley; Folley, 1956; Harris, 1958). We may ask how this hormone induces milk ejection.

The walls of the milk-secreting alveoli in the mammary gland of the goat contain a network of contractile myo-epithelial fibers, and Richardson (1949) demonstrated that these contract in response to local electrical stimulation, resulting in contraction of the alveoli. Cross (1954) found that a mechanical tap on the mammary gland of a rabbit in the neighborhood of a milk-distended lobule causes a sharp rise in the intralobular pressure. The latency of this rise in pressure is very short, on the order of 1 second compared with 30 to 90 seconds for the milk-ejection reflex. Gaines (1915) had found that the butting of the mammary gland by the kid contributed to the efficiency of milk ejection in the goat, and it may be that the local response of the myo


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epithelial cells plays some role here. Linzell (1955j found that oxytocin applied locally in very small amounts induced local contraction of the alveoli. Acetylcholine also produced local contraction. Although the mammary glands of sheep and goats are extensively innervated by sympathetic nerve fibers (but seem to receive no parasympathetic innervation) (Linzell, 1959), these fibers are vasomotor in their effect ; no secretomotor fibers to the mammary gland are known (Harris, 1958) and contraction of the myo-epithelial cells is not induced by stimulating the existing nerves. It therefore seems very likely that the effector end of the milk-ejection reflex consists of the direct action of oxytocin in the alveoli, where it causes contraction by way of its effect on the myo-epithelial cells of the alveolar walls. Further light may be cast on this mechanism by a consideration of the effects of emotional disturbance on the milk ejection reflex.

Emotional inhibition of milk ejection. Ely and Petersen (1941) reported that stimuli which seemed to frighten lactating cows inhibited the milk-ejection reflex. Whittlestone (1951, quoted by Whittlestone, 1954) found that electric shocks administered to a nursing sow interfered with milk ejection, and that the degree of interference was roughly proportional to the intensity of the shock. According to Cross (1952, 1953), emotional disturbance induced in lactating rabbits by electric shock, unfamiliar handling procedures and surroundings, forcible restraint during nursing, etc., greatly reduced the amount of milk got by the suckling pups.

Braude and Mitchell (1952) found that adrenaline, injected before oxytocin, inhibits the occurrence of the milk-ejection response which normally follows oxytocin injection. Adrenaline also inhibits milk ejection in the cow and in the rabbit (Ely and Petersen, 1941; Cross, 1953). This influence of adrenaline is, of course, consistent with the effects of emotional disturbance.

How does emotional disturbance inhibit milk ejection? There are three general possibilities, (a) Emotional excitation might block or inhibit the secretion of oxytocin by influencing the central neural mechanisms for its release, (b) Adrenaline might, by


causing constriction of the blood vessels in the mammary gland, prevent oxytocin circulating in the blood from reaching the myoepithelial cells of the milk-secreting tubules, (c) Adrenaline might inhibit milk ejection by a direct effect on the myo-epithelial cells.

The last possibility (direct inhibition of the myoepithelial cells by adrenaline) seems unlikely. Linzell (1955) found that oxytocin caused local contraction when applied in extremely small amounts to a mouse mammary gland exposed by dissection. Acetylcholine and other parasympathomimetic drugs were also effective in producing contraction on local application. On the other hand, adrenaline, when applied locally, caused local vasoconstriction in the capillaries and arterioles, but no constriction of alveoli or myo-epithelial cells. Adrenaline did not prevent the contraction of the alveoli when oxytocin was applied locally at the same locus to which adrenaline had just been applied, and at which vasoconstriction was at a maximum. Further, Cross (1955a t and Yokoyama (1956) found that mechanical taps on a lobule of the mammary gland of a rabbit produced a rise in intralobular milk pressure, even though adrenaline had just been injected, and when as a consequence of the adrenaline injection, milk ejection could not be elicited by a suckling stimulus. It therefore seems that the reactivity of the contractile elements themselves is not suppressed by adrenaline.

It is likely, however, that adrenaline can interfere with the effect of injected oxytocin on the milk-ejection reflex. Pi'ior systemic injection of adrenaline inhibits the milkejection response to subsequent injections of oxytocin in the rabbit (Cross, 1953) and sow (Whittlestone, 1954). In this connection it should be noted again that no secretomotor fibers are known in the innervation of the mammary gland (Harris, 1958), that there is no parasympathetic innervation to the gland tissue, and that the sympathetic innervation seems to consist largely of vasomotor fibers (Linzell, 1959). These observations, together with the failure of local application of adrenaline to inhil)it contraction of the myo-epithelial cells, suggest that the peripheral effect of adrenaline on milk ejection is largely through its


PARENTAL BEHAVIOR


1325


vasoconstrictor action, which interferes witli the access of oxytocin-carrying blood to the alveoli.

It should, however, not be concluded tliat there is no central inhibition of oxytocin secretion as a consequence of emotional arousal. Cross (1955b) found that when rabbits were suckled while forcibly restrained, the amount of milk removed (estimated from the weights of the pups) was substantially reduced (by 20 to 100 per cent in different animals). This reduction, however, could be restored in about 80 per cent of the 35 subjects by the injection of oxytocin. This suggests that part of the effect of emotional inhibition is the reduction of oxytocin secretion. Cross suggested that the experiments involving exogenous adrenaline probably involved much more adrenaline than is usually present in the blood as a result of emotional disturbance, and that the vasoconstrictor effect of adrenaline in those experiments may thus have been greater than that which normally occurs.

In any event it seems probable that both peripheral effects of adrenaline on the mammary glands and central inhibition of oxytocin secretion are involved in the mechanism of emotional inhibition of milk ejection.

3. Mother-young Relationships and the Regulation of Lactation

Sickling and the duration of lactation. Hammond and Marshall (1925) observed that the mammary glands of rabbits became inactive when the young were removed, whereas lactation was prolonged when the young were kept with the mother. Selye (1934) removed young rats from their mothers at 3 days of age, and found that milk secretion disappeared within 3 to 5 days, and that the alveoli began to disappear after 6 to 8 days. When young were left with the parents, lactation continued for the normal period of aj^proximately 3 weeks (Nicoll and Mcites, 1959). Similar results were obtained in the guinea pig (Hesselberg and Loeb, 1937a). Selye and McKeown (1934a) repeatedly replaced young mice by younger litters, so that the mothers were provided with yoimg of suckling age for a much longer period than nor


mal. Under these conditions, lactation was considerably prolonged, although the mammary glands could not be maintained indefinitely solely by continuously offering new young: signs of degeneration of the alveoli were to be noted by about 28 days postpartum. Nicoll and Meites (1959) repeated this experiment with rats, and found that they could maintain active mammary glands during a 70-day lactation period (compared with the normal 20-day period) by repeatedly replacing the litters.

It is apparent that the normal duration of lactation is in part regulated by stimuli provided to the lactating mother by the suckling young. This implies, of course, that the suckling stimulus must be capable of stimulating not only the posterior pituitary substances responsible for the milk ejection reflex, but also, directly or indirectly, must play a role in stimulating the secretion of the anterior pituitary hormones responsible for lactation (see chapter by Cowie and Folley).

Suckling and the onset of lactation. Although it is thus clear that suckling stimuli stimulate the maintenance of lactation, it seems that the onset of lactation at the time of parturition does not reciuire suckling stimuli (Meites and Turner, 1942b). Klein and Mayer (quoted by Mayer and Canivenc, 1951) tied off the uterine horns of pregnant rats, so that no parturition occurred. Lactation was nevertheless initiated at the normal time for parturition, without any stimulation of the nipples. Meites and Turner (1942c) noted that lactation begins at the time of parturition in nonsuckled rabbits, although it is not maintained unless the animals are suckled. Similarly, Williams (1945) observed milk secretion in the mammary glands of immediately postparturitive, unsuckled mice. The glands are empty of milk within 48 hours, and the alveoli have completely disappeared by the 6th day postpartum. Further, lactation is not initiated by i)resenting foster young during pregnancy (Masson, 1948; Mayer and Canivenc, 1951), even when the condition of the nipple indicates that active suckling has taken place.

The prolactin content of the pituitary gland normally rises just after parturition,


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HORMONAL REGULATION OF BEHAVIOR


in association with the onset of lactation (Reece and Turner, 1937a). In the rabbit, this initial rise in pituitary prolactin, from about 12 pigeon units per gland to about 23 pigeon units, occurs between the 28th day of pregnancy and the 2nd day postpartum. The rise is the same in suckled and nonsuckled rabbits. However, after the 2nd day postpartum, suckled rabbits have more prolactin in their pituitary glands, and produce more milk from the mammary gland, than nonsuckled animals (Meites and Turner, 1942c; Meites, 1954). Similar data have been obtained from the rat (Meites and Turner, 1948) .

In the dairy cow, which is of course highly selected for milk production, lactation can sometimes be started in nonpregnant or even virgin cows by regular manipulation of the teat. In general, however, it is clear that suckling stimuli are not effective in inducing lactation, and that the initiation of lactation, as distinct from its maintenance, must be explained on the basis of the hormonal changes occurring at the time of parturition.

The nature of the suckling stimulus. Selye, Collip and Thomson (1934) removed the nipples of the mammary glands on one side of a group of rats and tied off the main milk ducts on the other side. When lactating animals so treated were kept with their young, no involution of the milk-secreting tissue occurred on either side, indicating that the effect of the suckling stimulus on the mammary glands was through a systemic relationship, rather than being local to the tissues in the neighborhood of the stimulation. Ingelbrecht (1935) later demonstrated the same point in an ingenious group of experiments. He sectioned the spinal cord of 10 rats 2 days postpartum between the last thoracic and first abdominal segments, thus ensuring that the 6 posterior nipples were anesthetized, whereas the 6 anterior nipples retained their sensitivity to stimulation. If the anterior (unanesthetized) nipples were covered, so that the young could only suckle from the posterior nipples, all the young died within 48 hours, with empty stomachs. Replacement litters suffered the same fate. If only 4 of the unanesthetized nipples were covered, leaving 2 unanesthetized nipples free for


access by the suckling young, then all parts of the mammary glands continued to secrete milk. After two or three groups of young died while attempting to suckle on the posterior nipples, the anterior nipples were uncovered, and a new litter presented to the experimental mothers. They survived, and lactation was maintained throughout the mammary gland tissue. Eayrs and Baddeley (1956) repeated, in essence, the experiment of Ingelbrecht, except that they anesthetized some of the nipples by cutting the dorsal roots of their spinal nerves, rather than by sectioning the spinal cord, and then removed the unanesthetized nipples, whereupon lactation stopped altogether, although the remaining (anesthetized) nipples were vigorously suckled. Lactation was re-established in later broods, the re-establishment of the ability of stimulation of the nipples to induce lactation corresponding with the regeneration of tactual sensitivity in the nipple area. Ernst (1929) showed that denervation of the mammary glands of a dog resulted in regression of the milk-secreting tissue.

Hooker and Williams (1940) and Mixner and Turner (1941) stimulated the nipples of lactating mice, whose young had been removed, by applying turpentine on the nipple surface. Both groups of experimenters found that this treatment retarded the involution of the mammary gland which normally follows the removal of the young. Mixner and Turner suggested that the turpentine acted by inducing hyperemia locally, but Hooker and Williams' observation that, when turpentine was applied only to some of the nipples, involution was prevented in all the mammae indicates that the action of turpentine is not local, but is through the central effect of the sensory irritation of the nipples.

These experiments clearly demonstrate that the suckling stimulus consists primarily of mechanical and tactual stimuli applied to the nipple, and that its effect is not local on the mammary glands, but through the central effect of the afferent inflow from the nipples.

The effects of the suckling stimulus. (a) On the pituitary gland. A number of investigators have studied the effect of


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suckling stimulation on the prohiftin content of the pituitary gland. Meites and Turner (1942a) divided parturitive rats into two groups. The mothers composing the control group were allowed to suckle their young normally, whereas the young of the experimental group were taken away at parturition. At 7 days postpartum, the pituitary glands of all the animals were removed and assayed for prolactin content by a pigeon-crop method. The average amount of prolactin per pituitary gland in the control (suckled) group was 10.75 Reece-Turner units, whereas in the experimental (nonsuckled) group, it was 5.10. In a more recent study, the same authors (Meites and Turner, 1948) repeated this experiment, and extended it to rabbits, with similar results. In the latter species, the prolactin content of the pituitary gland rose to a peak about 5 days postpartum in nonsuckled as well as in suckled animals, but the peak was much higher (87 per cent more prolactin per pituitary gland) in the suckled animals and the prolactin content fell to the prepartum level much more rapidly in the nonsuckled animals (Meites and Turner, 1942c, 1948; Meites, 1954). Rabbits nursing larger numbers of young (5 to 11) had no more prolactin in their pituitary glands than did those nursing only two young (Meites, Bergman and Turner, 1941).

As might be inferred from the observations on lactation described earlier, suckling stimulation, although necessary for the maintenance of prolactin secretion during lactation, does not seem to be necessary for the induction of the immediate postpartum rise in pituitary prolactin content. Reece and Turner (1937b) found that the postpartum increase in pituitary prolactin content, measured 51 hours after parturition, was the same in animals that had been normally suckled and in animals whose young had dropped through a wide wire-mesh screen as thev w^ere born.

Although suckling stimulation thus undoubtedly contributes to the maintenance of a high level of prolactin in the pituitary during the lactation period, the immediate effect of a single suckling episode is to deplete the ])rolactin content of the gland. Recce and Turner (1936, 1937a, b) re


moA'cd young rats from their mothers at 36 hours postpartum. At 48 hours postpartum, the young of some of the mothers were permitted to remain with their mothers for 3 hours, during which they suckled. The pituitary glands of these mothers assayed at 5.20 Reece-Turner units of prolactin, compared with 9.20 units in mothers treated exactly the same way, except that they were not allowed the 3-hour suckling period with their young. Clearly, the suckling stimulus causes the release of prolactin from the pituitary gland, and the depletion of its prolactin content. Grosvenor and Turner (1957) found similar results in animals tested 14 days postpartum. These mother rats were isolated from their young for 10 hours. At the end of this isolation period, the control animals were killed for autopsy, whereas the experimental animals were suckled for exactly 30 minutes. The results indicate that the prolactin content of the pituitary gland was reduced about H by this suckling stimulation.

Suckling stimulation seems to affect the cytologic appearance of the pituitary gland. Gonadectomy in the female rat induces an increase in the number of basophilic cells in the pituitary gland, in many of which large nucleoli form (see chapter by Purves). Desclin (1936, 1947) removed the ovaries of female rats at parturition. Half of his animals were allowed to keep and nurse their young, whereas the young were removed from the other half. The suckled animals did not develop castration signs in their pituitary glands. Dawson (1946) found that cytologic changes in the pituitary gland of the cat which normally occur during lactation, do not occur after parturition unless the mother cat is allowed to suckle her young (see chapter by Purves).

( h I On the mammary gland. Most of the studies to which we have referred seem to contain the implication that the principal effect of suckling stimulation with respect to the stimulation of lactation is the stimulation of prolactin secretion by the pituitary gland. It is, of course, quite clear that prolactin has a substantial influence on milk secretion. The involution of the mammary glands which follows forced weaning in mice can be delayed by prolactin injection (Hooker and Williams, 1941), and local


1328


HORMONAL REGULATION OF BEHAVIOR


milk formation can be induced in single ducts of the proprely prepared rabbit mammary gland by small local injections of prolactin (Bradley and Clarke, 1956). However, it is now clear that other hormones normally play a role in the maintenance of lactation. Prolactin alone cannot maintain complete milk production in rats hypophysectomized on the fourth day of lactation, whereas adrenocorticotrophic hormone (ACTH) and probably growth hormone have synergistic effects with prolactin on milk production (Cowie, 1957; Williams, 1945).

The recent reviews and experiments by Folley (1956), and by Lyons, Li and Johnson (1958) make it plain that a considerable number of hormones secreted by the pituitary gland and by the ovary participate in the onset and maintenance of milk secretion. There is some evidence that at least one of these hormones, in addition to prolactin, is released in response to suckling stimulation. Gregoire (1947a, b) found that the involution of the thymus which occurs during pregnancy can be maintained after parturition by suckling, wdiereas the thymus regenerates if suckling is prevented. Injected prolactin does not maintain the involution of the thymus in the absence of suckling. This suggests that the effect of suckling on the condition of the thymus is through the stimulation of the secretion of some other hormone, probably ACTH (Folley, 1956).

Further details of the effects of various hormones on the mammary gland are contained in the chapter by Cowie and Folley. It is sufficient for our purposes to point out that the effects of suckling stimulation are probably somewhat more complex than the stimulation of the secretion of a single hormone by the pituitary.

Loeb and his co-workers found that, when the mammary gland of a laetating guinea l^ig was ligated on one side, so that suckling took place only on the other side, the gland on the ligated side regressed, whereas only the one on the suckled side was maintained in a secretory condition (Kuramitsu and Loeb, 1921; Hesselberg and Loeb, 1937a, b). They concluded that the stimulation of secretory activity in the mammary gland by suckling is a local effect, probably de


pendent on milk removal. Somewhat similar observations were made on the rat by Weichert (1942) who noted that, when a laetating rat has a small litter, the pups tend to use the anterior nipples only. In the third week of lactation, the mammary tissue in the neighborhood of the suckled nipples is engorged whereas that in the neighborhood of the nonsuckled nipples is regressed. This regression is not prevented by prolactin injection.

Such data seem to contradict numerous observations (already referred to above) indicating that maintenance of the mammary gland through suckling stimulation is a systemic effect, and that nonsuckled as well as suckled glands in the same animal are maintained by the suckling stimulus (Selye, 1934; Selye, Collip and Thomson, 1934; Turner and Reineke, 1936). This contradiction can readily be resolved by a consideration of the effect of mammary engorgement on the access of circulating hormones to the mammary tissue. Williams (1941) ligated at their midpoints the main ducts of some of the mammary glands in laetating mice, thus preventing milk drainage beyond the ligation, while permitting it up to the ligation. He found that the obstructed portion of the gland became inflamed and necrotic, and that the maintenance of the milk-secreting parenchyma in response to suckling stimulation w^as considerably reduced. Selye, Collip and Thomson (1934) tied off the milk duct of the mammary gland on one side of laetating rats and removed the nipples on the other side. They found that secretion was continued in both glands, indicating that stimulation on one side maintained secretion on the other side, and also that secretion could be maintained in the engorged gland. However, after about 3 weeks, the milk pressure in the gland seemed to damage the secretory epithelium, resulting in its involution. Cross and Silver (1956) and Cross (1957) ligated the teat duct in rats, resulting in a maximal engorgement of the duct after 24 hours. At this stage, if the ligatures were loosened, milk ejection could be elicited by intravenously injected oxytocin. After 40 hours of such ligation, no response to intravenous oxytocin was observed, and the mammary gland became whitish (instead of pinkish).


PARENTAL BEHAVIOR


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Histologic examination showed that the capillary bed was collapsed and almost without blood cells. However, oxytocin directly applied to the alveoli still caused local contraction. Therefore, the engorgement had resulted in a failure of blood circulation of the mammary glands. It seems likely that obstruction of circulation in the mammary gland caused by engorgement by nonwithdrawn milk is adequate to explain the failure of suckling stimulation in some animals so treated to maintain milk secretion. It should be noted that the guinea pig produces relatively little milk, and does not have large cisterns for the storage of milk. Therefore, it might be expected that local engorgement would have more serious effects in such a species than in some others.

The mechanism of suckling-induced lactation. The material just presented, plus the fact that suckling stimulation induces pseudopregnancy (Selye and McKeown, 1934b) and prolongs gestation (Weichert, 1939), clearly indicates that suckling stimulation induces the secretion of prolactin. We may now inquire into the mechanism of this effect.

Herold (1939) reported that section of the pituitary stalk in lactating rats was followed by the gradual cessation of milk secretion and involution of the mammary gland, although the young continued attemps at suckling. Jacobsohn and Westman (1945) and Jacobsohn (1949) sectioned the pituitary stalk in rats and in rabbits, and, like Herold, found that all the young died. However, the involution of the mammary gland was only partial, some of the alveoli in each animal remaining secretory. This is in contrast to the result of forcible weaning of the young or of hypophysectomy, both of which treatments result in cessation of milk secretion and complete involution of the mammary gland. These experiments seem to imply the continuation, after stalk section, of some secretion of lactation-stimulating hormone (s) by the pituitary gland. Desclin (1940) found that the young of 13 out of 22 lactating rats whose pituitary stalks were transected 5 to 6 days postpartum survived, although theii- weight was abnormally low. Everett (1954, 1956) found tiiat pituitary glands transplanted to the renal capsule continued to seercte prolactin,


and he suggested that neural connections are unnecessary for the maintenance of the secretion of this hormone, and that possibly the neural effect is inhibition under appropriate stimulation (Nikitovitch-Winer and Everett, 1958) . This is consistent with the results of Jacobsohn's observations, except that the amount of prolactin apparently secreted when the stalk is transected in lactating rats is small compared to the amount produced under suckling stimulation. Rothchild (1960a) showed that rat pituitaries autotransplanted to the renal capsule can secrete enough prolactin to maintain lactation, again at a lower level than in intact lactating animals. He also showed that suckling stimuli cause a reduction of gonadotrojihin secretion, and that this effect is probably independent of the effect of such stimuli on prolactin secretion.^

Although the experiments cited thus far make it clear that both milk ejection and lactation occur as a response to suckling stimulation, it is not so clear whether both phenomena are primary effects of suckling stimulation (Folley, 1947). Petersen (1948) suggested that suckling might stimulate lactation by inducing the secretion of a posterior pituitary hormone which in turn might stimulate the secretion of the lactogenic hormone (s). Benson and Folley (1956, 1957) have provided evidence that oxytocin, the secretion of which is undoubtedly stimulated by suckling (see above), itself stimulates the secretion of prolactin. They removed rat litters at 4 days postpartum, when the treatment of the mothers began. (Oxytocin was injected, at various dosage levels, for 9 days, at the end of which time the oxytocin-treated animals had more secretory tissue in their mammary glands (40 to 46 per cent of the area of histologic sections) than did the controls (about 16 j^er cent). The diameter of the alveoli was also greater in the oxytocin-treated animals (about 50 ijl) than in the controls (about 15 fi) . Injected prolactin maintained ap • These experiments were described in a series of important papers on the corpus luteum-pituitary relationship, which appeared too late to be fully considered in the preparation of this chapter Rothchild, 1960b: Rothchild and Dickey, 1960; Rothcliild and QuiUigan, I960: Quilhgan and Rothchild, 1960).


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HORMONAL REGULATION OF BEHAVIOR


proximately the same level of secretory tissue (48 per cent of section area) as did oxytocin injection. Oxytocin injected into hypophysectomized females had no effect on the mammary secretory tissue. It should be pointed out that prolactin has a local lactogenic effect when introduced directly into the milk-secreting ducts, whereas oxytocin, as well as other anterior and posterior principles, has no such effect. McCann, Mack and Gale (1959) found that hypothalamic lesions in the supra-opticohypophyseal tracts of lactating rats prevented milk ejection and milk secretion. The loss of milk secretion was noted even when the anterior hypophysis and its portal vessels, as well as the median eminence, all appeared histologically normal. Oxytocin injected into such animals delayed the involution of the mammary glands. Similarly, Donovan and van der Werff ten Bosch (1957) found that destruction of the pituitary portal blood vessels did not result in loss of lactation when oxytocin was administered regularly after the operation, and Desclin (1956a, b) found that oxytocin injected into virgin rats made possible the development of deciduomas in response to irritation of the uterine wall.

It must be concluded that oxytocin is capable of acting as a neurohumor stimulating the secretion of a lactogenic hormone by the pituitary gland.

Tverskoy (1953) milked a goat by injecting oxytocin, then draining the cisterns directly with catheters. The milk yield continued normal, indicating that external stimuli to the nipples were not necessary. When he arranged the catheters for continuous drainage (without oxytocin injection) , the milk secretion declined. When the catheters were arranged for continuous drainage, but oxytocin was nevertheless administered twice a day, the milk secretion increased. Tverskoy interpreted this as indicating that the rise in alveolar pressure, caused by the oxytocin injection, was a source of afferent sensory inflow which was the stimulus for the reflex secretion of prolactin. This is an ingenious interpretation, but the simpler conclusion by Benson and Folley from their experiment, namely that


oxytocin acts directly as a neurohumor to induce the secretion of prolactin, could apply to this experiment as well.

Cross (1960) points out that other effects of suckling stimulation than the specifically endocrine ones may be related to the maintenance of milk secretion. Suckling induces increased eating and weight gains in mother rats, even when milk withdrawal is prevented by cutting the milk ducts (Cotes and Cross, 1954), and this effect cannot be duplicated by prolactin injection. Nursing mother rats consume more food than nonnursing rats (Slonaker, 1925) (although Bateman (1957) reports that lactating mice spend no more time feeding than do nonlactating ones) .

Such effects might contribute to the amount of milk secretion without reference to the stimulation of pituitary hormone secretion. Nevertheless, it is clear that the stimulation provided by suckling causes the release of lactogenic hormones from the pituitary gland, and it now seems likely that this effect is not an effect separate from the stimulation of oxytocin secretion, but rather that the oxytocin secreted by the posterior pituitary as a result of suckling is, at least to some degree, involved in the stimulation of prolactin secretion by the anterior pituitary.^

4. Xursing Behavior and the Condition of the Mammary Gland.

Cross (1952) found that rabbits, which normally nurse the young once a day, could not be induced to nurse more often unless loss of milk was prevented by sealing the teats with collodion. He concluded that mammary distension was a factor in the motivation of nursing. Such a conclusion seems reasonable, and there is considerable evidence in its favor. Many observers have noted that the frequency with which young are nursed is in part a function of the stage of lactation, and thus of the amount of milk being produced, although it is not clear

'Rothchild and Quilligan (1960) have failed to verify either the induction of pseudopregnancy or the formation of deciduomas by oxytocin injection in the rat. They therefore independently suggested the same explanation as had Tverskoy for the type of results found bj- Benson and Folley.


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wlu'thcr the milk pressure is res))()nsibl(' for the amount of nursing or vice versa, or whether there is a I'eciprocal relation between the two. Bartliolomew and Hoel (1953), for ('xam})le, found that mother Alaska fur seals stay at sea for 3 to 10 days, then ashore with their pups for 1 to 3 days. As the season progresses (after the birth of the young), the females spend about the same time ashore at each visit, but the time spent at sea between visits increases. Bartholomew and Hoel suggested that the mothers may return when the mammary glands are full, and the diminution of the rate of secretion, or the increase in the pup's demands, could cause the female to stay at sea longer as the season progresses. Similar observations have been made on many mammals (Krumbiegel, 1955) .

In many cases a correspondence is observed between the occurrence of lactation and of nursing behavior in response to physiologic stimulation. Allan and Wiles (1932) found that cats hypophysectomized during pregnancy (which, of course, produced no milk) paid no attention to the young, and made no attempt to nurse them. Cannon and his co-workers found that sympathectomized dogs and cats, if they were made pregnant very soon after sympathectomy, might lactate normally after parturition, and in such cases would nurse their young. On the other hand, if parturition did not occur until some time after sympathectomy {e.g., 6 months postoperatively) the mammary glands failed to develop, lactation was not established, and no attempts were made by the mothers to nurse their young. In the case of a cat which had 3 kittens 20 months after sympathectomy, the animal withdrew from the kittens as soon as possible, even after the kittens were forcibly put to her nipples to suckle (Cannon, Newton and Bright, 1929; Cannon, 1930; Cannon and Bright, 1931). Labate (1940) sympathectomized rabbits, then allowed them to mate and delivered the young by cesarian section. In these animals, lactation was normal, as was nursing behavior.

In other cases, however, it is clear that nursing behavior does not necessarily depend on a distended condition of the mam


mary gland, or on the presence of milk secretion. Hain (1935) found that estrone injected into lactating rats caused the cessation of suckling behavior, although the involution of the mammary glands did not occur until after the suckling behavior had stopped. Weichert and Kerrigan (1942) similarly found that estrone injected into rats caused parental care to become sporadic, the pups occasionally being scattered over the cage and inadequately warmed. Intervals between nursing episodes became less and less frequent as the estrone injections continued. These authors also had the impression that the decrease of lactation was a secondary effect of the behavioral disturbance in the mother. Obias (1957) found that rats hypophysectomized during gestation delivered young at the normal time. All nursed their young, although all the young died because no milk was produced. Collip, Selye and Thomson (1933) hypophysectomized lactating rats and found that, although the mammary glands regressed, maternal behavior, including nursing, was not impaired and the young continued to attempt to suckle until they died. Eayrs and Baddeley (1956), who anesthetized the nipples by cutting the dorsal roots of their spinal nerves, found that lactation stojjped altogether, although the rats continued to attempt to nurse their young, and the anesthetized nipples were vigorously suckled.

Nelson and Smelser (1933) induced lactation in male guinea pigs by injecting estrone, followed by pituitary extracts. Animals lactating as a result of such treatment refused to nurse young, even though the young animals vigorously tried to suckle.

Although there are many suggestive observations indicating a relationship between mammary engorgement and the motivation to nurse the young, it is apparent that this cannot be the only factor, and, in some species, may not even be an important factor. The exact contribution, if any, which mammary engorgement makes to the regulation of nursing behavior, and the manner in which it may interact with other physiologic factors and with previous experience, remain to be investigated.


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IV. General Discussion: the Psychobiol ogy of Parental Behavior and

the Role of Hormones

A. LEARNING AND HORMONE-INDUCED PARENTAL BEHAVIOR

1. General: FoDiiulation of the Problems

We have presented a great deal of evidence that the patterns of parental behavior vary in characteristic ways from species to species, and are relatively constant within species. Obviously, then, genetic differences between the species must play a considerable role in the establishment of these differences. Discussions of the role of learning in the development of such behavior patterns are often the occasion for vigorous controversy because various investigators differ with respect to the relative heuristic value which they assign to the formal identification of characters as being "innate" (or "inherited") or "learned" (or "acquired"), and with respect to their method of approach to the study of ontogeny, to the terminology they use to identify the effects of environment and the effects of genetic differences, to the type of behavior which interests them, etc. We cannot go into details of this "nature-nurture" problem here, except for the purpose of bringing into perspective our discussion of the role of learning in the development of parental behavior patterns (for discussion of these problems see Lorenz, 1937; Tinbergen, 1951 ; Lehrman, 1953, 1956b; Hebb, 1953; Kennedy, 1954; Koehler, 1954; Schneirla, 1956; Eibi-Eibesfeldt and Kramer, 19581.

A first stage in the study of the effect of experience on any behavior pattern is to determine whether and in what ways the pattern can develop w4ien the environment is restricted in various ways, so that particular kinds of experience are not available to the animal. Such experiments may illuminate the contribution of various kinds of environmental experience to the development of the behavior. Furthermore, when we find that particular kinds of experience do 7tot contribute to the development of the behavior pattern, we have also learned something significant about the behavior (Tinbergen, 1955). However, since the central problem is that of the development of


the behavior, experiments of this type do not give a final answer to the question of what has contributed to the formation of the behavior (Schneirla, 1956). We do not by any means know all the possible varieties of learning processes (Maier and Schneirla, 1942) , and this limits our ability to perceive the most significant relationships during development. Furthermore, we are just beginning to appreciate the variety and subtlety of the ways in which very early experience contributes to the development of adult behavioral capacities in various kinds of animals (Hebb, 1949, 1953; Beach and Jaynes, 1954) .

This means that the question of whether any particular kind of learning has or has not contributed to the development of a behavior pattern is only one step in the analysis of its ontogeny. Unfortunately, for the great majority of behavior patterns, this is the only step that has yet been taken.

In dealing with the problem of the contribution of learning to the development of patterns of parental behavior, therefore, we are simply analyzing, to the extent that the available data permit, one of the influences on the ontogeny of the behavior. It should not be thought that we are seeking answers to, or even formulating, "final" questions about the nature of environmental influences. Later parts of this discussion will indicate some of the ways in which exjieriential influences may be related to various kinds of organic factors during development.

2. Learning and Parental Behavior

Behavior of inexperienced and of experienced MOTHERS, (a) Comparison of primipara and multipara. Chimpanzee mothers who have previously borne young appear to be much more efficient and skillful in caring for their infants than are primiparous animals (Yerkes, 1935; Yerkes and Tomilin, 1935; Yerkes and Elder, 1937; Nissen and Yerkes, 1943). Primiparous chimpanzees, when first confronted with their own young, usually appear indifferent to or fearful of the newborn, and handle them clumsily, or not at all. Such an animal is likely to act "surprised, puzzled, baffled, and at a loss as to what to do," and may do such things as holding the infant head down, biting its


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feet, appearin<2; annoyed when it clings to the mother's body, etc. In contrast, an experienced chimpanzee mother shows a high degree of assurance, directness, and skill in accepting, placing, grooming, cuddling, and in general caring for the young. As Yerkes and Tomilin (1935) say, "the contrast is that of bewilderment and relative uncertainty versus familiarity." Similar differences between primiparous and multiparous mothers can be seen in the rhesus monkey (Tinklepaugh and Hartman, 1930), in which primiparous animals seem frightened, excited, and disorganized in the presence of the neonate, compared with multiparous mothers. However, Yerkes (1915) noted that a primiparous rhesus monkey which bore a still birth kept the dead young animal and carried it about the cage for a long pei^od.

Observations in zoos (Hediger, 1955) indicate a similar improvement in maternal care in experienced as compared with inexperienced mothers, in many other animals. Hediger says, "a considerable difference . . . may often be seen between the behavior of experienced mothers and those with their first-born young. This distinction is often indeed, so sharp that the first birth might be considered as something like a dress rehearsal, not counting for the propagation of the species, but a preparation for subsequent births."

Ross, Denenberg, Sawin and Meyer (1956) rated the quality of nest-construction of 84 rabbits of various strains, each of which reared four litters of young. They found that the quality of the nest, as rated by various observers, improved linearly up to the third litter. (Deutsch, 1957, felt justified in objecting to this conclusion on the basis of his own observations of two female rabbits w^hich were primiparous at the beginning of his observations, and a third which had had an unstated number of previous litters, and which w^ere able to construct "fairly uniform nests perfectly, even without any previous experience of digging.") On the other hand, a "maternal protection" score, based on ratings of the intensity of the mothers' resistance to the observer's attempts to manipulate the young, did not change from litter to litter


(Denenberg, Sawin, Frommer and Ross, 1958).

Data on the differences between experienced and inexperienced laboratory rats, mice, and guinea pigs are rather contradictory. Primaparous animals seem to care for and retrieve the young perfectly adequately, with a full range of appropriate behavior patterns (Avery, 1925; Wiesner and Sheard, 1933; Lashley, 1938; Beach and Jaynes, 1956a). Some investigators nevertheless report differences between primiparous and multiparous animals. Leblond (1940) tested lactating mice by presenting them with young of various ages. In both mice and rats, younger pups are much stronger stimuli for the retrieving response than are older pups (Wiesner and Sheard, 1933). Leblond found that the average age of the young which his lactating mice would retrieve was greater in multiparous than in primiparous animals. He interpreted this as meaning that the multiparous animals could retrieve in response to somewhat weaker stimulation than that required by the primiparous subjects. Frank (1952) reported that primiparous common voles retrieved less readily and intensely than did multipara.

Beniest-Noirot (1958), studying domestic mice, found no difference in retrieving (or other aspects of maternal behavior) among groups of primiparous females, virgin females, pregnant females, and males, but her data are based on the presence or absence of the behavior in various individuals, and do not include any measure of frequency or intensity. Similarly, Rowell (1960c) found no differences in the proportions of various kinds of responses given to young by primiparous and by multiparous female golden hamsters. Beach and Jaynes (1956a) made a very careful and quantitative comparison of maternal behavior in primiparous and multiparous rats. They graded the rats on the number of pups poorly cleaned, number of pups found outside the nest, quality of the nest, etc. They also tested them for retrieving behavior by a method which yielded data on both the latency and the frequency of retrieving during a test period. They found no difference with respect to any of these measures between primiparous and multiparous animals. The multiparous rats of Beach and Jaynes' experiment had


1334


HORMONAL REGULATION OF BEHAVIOR


bred in small cages, and had not been tested for retrieving during their first breeding experience; therefore, they had had practically no experience in retrieving. Beach and Jaynes found that retrieving efficiency increased during the first 7 days postpartum, for both primiparas and multiparas. This improvement was a function of practice, because it did not occur unless repeated testing provided practice. Animals tested 1 day postpartum during their first and their second lactation periods showed no improvement.

On the basis of these data, it is not possible to say whether the difference between Beach and Jaynes' conclusions and those of Leblond are due to differences in the amount of retrieving practice obtained by the animals during the first lactation period, to differences in testing methods, or to differences between rats and mice.

Nice (1937) observed that inexperienced song sparrows building their first nests seemed to build just as well as did experienced birds. Marais (quoted by Armstrong, 1947) reared four generations of weaver finches, a bird which normally builds a very elaborate nest, without giving them the opportunity to see any nesting material. Their descendents plaited their elaborate nests in a normal manner. Hinde (quoted by Thorpe, 1956) found that canaries that had never had an opportunity to manipulate nesting materials would, when given grass for the first time, pick it up and carry it to the nest-pan within a minute or so. Observations such as these indicate that, in many birds, nest-building behavior is rather rigidly determined by organic influences. However, Lorenz (quoted by Thorpe, 1956) noted that ravens and jackdaws that are building nests for the first time are uncertain what material to use, and must learn to pick material that can be woven into the nest. Hinde (1958) found that a chaffinch kept in a cage without nesting material developed the habit of plucking its own feathers to use as nesting material (as do many canaries). In the following year, when it was kept in an aviary with plenty of nesting material, it plucked its own feathers nevertheless. Lehrman (1955) reported that ring doves breeding for the second time tended to feed their squabs sooner after


hatching of the eggs than they liad at thciifirst breeding.

(6) Learning or physiologic change? It is reasonably clear that, in many animals, there is some improvement in the efficiency of parental behavior between the first and subsequent breeding experiences. However, the method used for collecting most of these data is unsatisfactory in several respects. Fii'st, the fact that animals engaged in parental behavior are in a constantly changing physiologic condition means that changes in behavior occurring, for example, late in lactation, which might be influenced by experiences earlier in lactation, cannot be expected to be transferred intact to the beginning of the next lactation period (when the animal is in a different jihysiologic condition). Thus, it would be very difficult, by this method alone, to demonstrate the possible importance of concurrent experiences as a factor in the changing pattern of behavior which is so characteristic of the parent-young relationship.

Secondly, many of the conclusions about imiM-oved eflSciency of maternal behavior in second and later parturitions are based on observations in which there is no adequate control for the age of the animal at the time of the observation, and for the purely physiologic effects of the animal's having gone through the endocrine changes associated with the first breeding experience. Dieterlen ( 1959) reports that female golden hamsters which give birth for the first time before they are 80 days old often build abnormally small nests, and fail to care for the young properly because they are easily frightened. However, females that do not give birth until they are more than 3 months old are almost always more careful and quieter, even during their first lactation period. Seitz (1954, 1958) found that scores indicating the efficiency and intensity of maternal behavior were higher in rats breeding for the second time than in those breeding for the first time. This difference is associated with a tendency toward increased litter size and greater frequency of litters as the mother matures. Seitz states that as the mother rat grows still older, litter size and maternal behavior tend to decrease. This raises the question as to whether the increase observed between the first and sec


PARENTAL BEHAVIOR


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ond litters may not be due to jjliysiologic changes associated with maturity, which are in turn to some extent reversed or overridden by approaching senility. Hauschka (1952) states that female mice of a strain in which there is a certain amount of cannibalism toward the young showed a higher frecjuency of eating the young with increasing age. Hauschka defines age in terms of the litter number, from the first litter through the eighth. In this study, as in some of the other experiments we have mentioned, age is confounded with experience, so that it is not possible to say whether the changing pattern of behavior is due to the animals' experience or to growth changes, or to some interaction between the two. Controls for age and for previous pregnancy and parturition without opportunity to relate to the young would be relatively simple to arrange, but this has not been done.

Similar problems are found in the few reports of such work with birds. Verlaine (1934) reported that domestic canaries which built successive nests tended to build better nests later in the season. He implied that this is the result of practice, but it is by no means certain that this is so, because there is no control for the effects of seasonal changes in hormone secretion.

Saeki and Tanabe (1955) found that prolactin injected into adult hens with previous brooding experience induced incubation l)ehavior, whereas the same treatment administered to immature pullets did not have this effect. Here again, the relative effects of previous experience, of age, and of endocrine condition (the experienced hens were laying eggs before being injected) are not clear.

Craig (1913, 1918) reported that a female ring dove which was never bred, nor had a nest or nesting material, may lay an egg on the floor, but an experienced dove will withhold the egg until a nest is available. Mr. Philip Brody and I, in the course of an experiment on a different problem, have verified this; in our observations, the experienced and inexperienced birds were of the same age.

It is apparent that, although there are many suggestive indications that the first breeding experience may have an influence on the nature and efficiency of subsequent


breeding behavior, the problem of behavioral changes between first and later breeding episodes deserves much closer and better controlled study than has yet been given to it. Attention should also be paid to the probability that phyletic differences in the role of such experience may be very important (Beach, 1947a, b; Aronson, 1959).

Nature of changes in behavior during THE breeding EPISODE. Beach and Jaynes' (1956a) oijservations indicate that some improvement in retrieving behavior occurs as a result of practice during the lactation period (see also Seitz, 1958). A number of other observations and experiments suggest that, at least in many mammals, the experience of the mother during each stage of the period of maternal care, from parturition on, contributes to the development of behavior during successive stages.

Blauvelt (1955) reported that the association between newborn domestic goats and their mothers during the period immediately after birth seems to be a very important part of the process leading to the establishment of the mother-young relationship. A parturitive mother of this species licks the kid as the kid leaves her body. The kid, lying on the ground, bleats, and the mother stands with her head pointing at the kid until it can stand and walk to her. If the mother's head is held so that she cannot lick the kid during parturition, and she is taken away for a short time, she does not lick the kid again when she has returned, and contact with the kid takes a long and variable time to establish. If a 1-hour-old kid is separated from its mother for just a few minutes, the mother is very disturbed when the kid is reintroduced. If the kid is fed by the mother before the two are separated, then the re-establishment of their relationship occurs much more quickly after the kid is returned than if the two are separated before the kid is fed. In 6 cases in which the kids were separated from their mothers for 20 or 30 minutes starting at birth, none was able to establish a successful relationship without help from the experimenter. Hersher, Moore and Richmond (1958) removed 24 newborn kids from their domestic goat mothers for periods ranging from Vk to 1 hour, starting 5 to 10 minutes immediately following birth. When the kids were re


1336


HORMONAL REGULATION OF BEHAVIOR


turned to the mothers, they were helped to suckle from their own mothers. A control group of 21 mothers was allowed to rear their kids normally. The flock was not further interfered with until 2 or 3 months later when the animals were tested by placing a mother in an experimental room with three kids, including her own. In this situation, the mothers which had been separated from their kids during the hour following birth nursed their own kids less than those mothers which had not been so separated, and nursed other kids more.

Collias (1956) found that sheep are attracted to newborn young by their odor. A ewe could be attracted by a rag rubbed in fresh birth membranes. Collias, like Blauvelt, found that separation of newborn goats and sheep from their mothers for a short period of time resulted in rejection of the infants when they were returned to the mothers, although he found it necessaiy to keep mother and young separated for somewhat longer times (2 to 4 hours) than had Blauvelt.

Unpublished observations by Tobach, Failla, Cohen and Schneirla at the American Museum of Natural History show that the maternal licking of the neonate kitten appears to be in some respects an extension of her self-licking immediately before parturition. The relationship between mother and young, established in part through such processes, forms the basis for the development of detailed perceptual responses of the animals to each other, as the mother and young become mutually conditioned (Schneirla, 1950, 1959).

The results from an experiment by Labriola (1953) warn us that the type of process described in the preceding paragraphs is by no means the only one contributing to the development of the mother-young relationship, or at any rate that it is not of the same relative importance in all animals. Labriola compared the maternal behavior of primiparous female rats who were allowed to deliver their young normally with the behavior of females whose young were delivered by cesarean section. A further comparison was made with nulliparous nonpregnant animals. The animals were tested for retrieving 24 hours postpartum, after having remained with the young since par


turition; the test was repeated at 24, 48, and 72 hours postpartum. All the normal controls retrieved young on the first test. Five of 7 cesarean-operated animals retrieved on the first test, 1 on the second, and the last on the third. It is clear that, at least in the rat, the events associated with parturition and the cleaning of the young are not essential for the establishment of retrieving behavior in a majority of the animals. Labriola's subjects were kept with their pups from the time of parturition until the first test, and no observations are available to show what happened during this time. The cesarean-operated females did not lactate, but no observations are availal)le from which we could decide whether this was due to the effects of the operative interference on the animals' endocrine condition, or to the possible nonestablishment of suckling stimulation immediately after delivery.

We may also remind ourselves that camels, llamas and their relatives establish suckling relationships with their young in the complete absence of any tendencies to lick the young, eat the placenta, tear the membranes, or bite the imbilical cord (Filters, 1954).

Recognition of young. The development of recognition of their own young by mother animals is another indication of the occurrence of learning based on originally partially hormone-induced parental behavior patterns. Earlier, in connection with our discussion of the stimulation of retrieving by external stimuli, we discussed a number of cases in which such individual recognition of the young had been demonstrated. It became clear from those cases that many animals are able to recognize their own young (Beach and Jaynes, 1956c), even in species which, under other circumstances, readily adopt young of other species (Frisch and Kahmann, 1952). Some mother chimpanzees have been found to react to their own young differently from any other infants after one year of separation, starting at about one year after birth (Spence, 1937).

Ramsay (1951) found that various domesticated and semidomesticated species of ducks will readily adopt birds of other species hatching from eggs incubated by the


PARENTAL BEHAVIOR


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experimental birds. In such cases, the parent birds often chase and peck at young which were unlike the ones they had adopted, even though the "strange" young are of their own species. Tinbergen (1939a I found that parent herring gulls react to all young gulls indiscriminately until their young are about 5 days old, after which they recognize their own and attack others.

It is thus apparent that individual recognition of, and response to, particular young animals frequently develops on the basis of originally relatively undifferentiated responses, based in part on the i)hysiologic condition of the parent.

Possible effects of earlier experience. Experience gained earlier in life, before parturition, may of course have an effect on the development of parental behavior, and several attempts have been made to demonstrate this. Riess (1950, 1954) reared female rats without access to anything manipulatable; their food was finely pulverized, no nesting material or bedding was permitted in the cages, and the floor was constructed of wide-mesh wire, so that the feces would fall through the floor and be unavailable for carrying. The animals were isolated from other rats. Riess found that animals so reared, when made pregnant and given nesting material, showed no nest-building behavior and decreased retrieving behavior ; there was an infant mortality of 75 per cent due to the absence of nursing behavior. The experimental animals did tear the strips of paper (provided as nesting material) from their holders, but carried them about and left them at random on the floor of the testing chamber. The pups were likewise carried about the cage without being gathered into one area. In a less drastic limitation of the animals' environment during development. Kinder (1927) had found that rats reared in cages without paper did as much nest building, when later tested, as those reared in cages with paper, but that the amount of nest-building on the first day of testing was less for the animals reared with restricted experience.

In a previous discussion of this prol)lem (Lehrman, 1953, 1956b) I implied that Riess showed that the animals must learn to carry nesting material, and that practice in carrying food pellets is, for this purpose, equiva


lent to practice in carrying nesting material. Eibl-Eibesfeldt (1955a, 1956) has shown that this conclusion is incorrect, and has thrown further light on the nature and limitations of the learning process involved. He reared female rats in a manner similar to that devised by Riess, and tested them at the age of 10 to 12 weeks by placing nesting material in their living cages, instead of by moving the animals to a test cage, as had Riess. He thus avoided any interference of exploratory behavior with maternal behavior. Of 29 animals so tested, 8 began building immediately, whereas 3 additional animals began within the first hour. Eleven acted like Riess' rats, carrying nesting material to and fro in the cage, eventually dropping it at random. These animals, however, began to restrict themselves to a single location in the cage after a few hours of such activity, and had built nests by the following morning. Five animals carried nesting material to a single corner of the cage, and there gnawed and played with it, but did not build a nest until the following day. Two of the 29 animals did no building at all. Observations carried out before the introduction of the nesting material showed that 9 of the 29 had established sleeping places in the cage, although the remaining animals had no fixed sleeping locations. The 8 animals which began to build immediately belonged to the group which had fixed sleeping locations. For a further group of experimental animals, Eibl-Eibesfeldt placed a small vertical partition in a corner of the cage so as to make a cubicle open to the rest of the cage. Of the 19 animals tested with this partition, 18 built in this corner immediately after nesting material was introduced for the first time.

It appears from Eibl-Eibesfeldt's data that the failure of nest-building by some of the animals in his and Riess' experiments was due not to a lack of development of the basic responses of picking up and carrying nesting material, but to the failure of the animals to develop an attachment to a particular place in the cage. Further, the more differentiated the living space, and therefore the more stimulation it can offer to attract the animal into one part of the cage, compared to other areas, the less necessity there is for an extended period of development of


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HORMONAL REGULATION OF BEHAVIOR


an attachment to a particular sleeping location.

Birch (1956j raised female rats with wide rubber collars around their necks, which prevented them from licking any part of the body behind the neck. In particular, these collars prevented access to the genital area, which is intensively licked during pregnancy and during the events associated with parturition. The collars were removed 1 to 2 hours before parturition. Birch states that "because of the inadequacy of maternal behavior no offspring survived the nursing period. The latent periods for the initial licking of the young were abnormally long." Birch's hypothesis is that "the self-licking of pregnancy is the experiential basis for the self-licking . . . and the pup-licking of parturition, and the pup-licking of the nursing period." Birch's data have never been reported in full ; the report here quoted lacks any statement about how many animals were used, the duration of latent periods, details of the survival of the young, quantitative details of the behavior of the mothers, etc. Coomans, in an unpublished study cited by Eibl-Eibesfeldt (1958j repeated Birch's study, using hooded rats (Birch used white rats), and obtained quite different results. He states that no disturbance of maternal behavior was found if the collar was removed before parturition, and that the disturbances that were found when the collars were left on could be attributed solely to mechanical interference with the normal behavior pattern. Since neither the Birch nor the Coomans study has been reported in sufficient detail to permit a replication, it is to be hoped that further work on this problem will provide data that will allow a more confident interpretation. I have gone into detail here only because so many authors have referred to this experiment (Lehrman, 1953, 1956b; Hebb, 1953; Schneirla, 1956 j.

Beach (1937) found that removal of various amounts of cerebral cortex in female rats caused a degree of disorganization of maternal behavior which was roughly proportional to the amount of cortex removed. This conclusion is based on measures of the amount and the efficiency of nest-building behavior, the time when nest-building behavior starts, efficiency of retrieving young, measures of the amount of licking and clean


ing of the young, survival of the young, etc. The disturbance of maternal behavior caused by these lesions is due to more than a specifically sensory deficit, since, e.g., animals with lesions of the visual cortex show more disturbance of maternal behavior than do peripherally blinded animals. Beach (1938) further found that animals operated on in infancy were superior in performance to animals undergoing the same operation as adults, although both were deficient when compared with intact animals. The larger the lesions, the greater was the degree of superiority of animals operated on at infancy over those in which the lesion of the same size was made after they became adults.

These findings of Beach on the relative effects of cortical lesions on maternal behavior when the lesions are made early in life or later (greater effect of lesion in adults than in infants, greater disparity between the two groups with larger lesions than with small lesions, effect of lesion a function of size rather than of location, etc.) are strikingly similar to those found by Lashley (1929, 1933) who studied the effects of cortical lesions of various sizes on the learning of complex maze problems in rats; the lesions were made in some animals after the problem was learned and in others before the problem was learned. Damage to the cerebral cortex interferes much more with the retention of a previously learned problem than does a lesion of the same size with the subsequent learning of the same problem. Further, the disparity is greater, the larger the lesion. Benjamin and Thompson (1959) found that the ability of cats to discriminate different degrees of roughness of sandpaper was more seriously impaired by lesions in the somatic sensory cortex when the lesions were made at maturity than when they were made at birth. Beach (1939a) found that the performance of female rats in a maze-learning situation was correlated with the efficiency of their maternal behavior. For example, of 40 rats tested, the 5 which made the fewest errors on the maze retrieved their first pups after an average latency of 3.2 minutes; the 5 poorest maze learners took on the average 360.4 minutes to start retrieving their young.

These experiments of Beach hint that


PARENTAL BEHAVIOR


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some generalized learning about the environment which occurs during early life may participate in the organization of maternal behavior.

Stamm (1955) found that lesions in the median cerebral cortex caused more disturbance in the maternal behavior of rats than did lesions of similar size elsewhere on the cortical surface. Rats so treated licked their young and severed the umbilical cords, but did not retrieve the litters together into a nest after parturition and did not permit the young to suckle. However, introduction of foster pups with preA'ious suckling experience markedly changed tlie behavior of the operated mothers. The foster pups, by hanging onto the nipples of the mother rats, induced lactation, and the operated animals subsequently hovered over the litters, permitting the young to nurse; they then collected and retrieved the pups, which survived. These observations may indicate that the cortical lesion did not interfere with the ability to carry out the maternal behavior, but perhaps reduced the impact of the stimulation which normally elicits this behavior.

Interaction of hormonal and experiential INFLUENCES. Froiii the foregoing discussion, it is apparent that some behavior patterns are simultaneously influenced by various endocrine conditions and by previous experience. This fact raises some interesting problems concerned with the interrelations of such influences.

Uyldert (1946) allowed 35 primiparous rats to deliver their young on a floor made of wide-mesh wire screen, through which the newborn pups fell, so that the mother had no contact with them. Animals of a control group were allowed to retain their young and to nurse them normally. After the young of the control group were weaned, both groups were allowed to rest for several weeks, following which each animal was injected with 200 fjig. of estrone per day for 20 days, which induced mammary development. One day after the cessation of this treatment, rats of both groups were provided with newborn young. Eight of the 9 control animals (animals with previous normal nursing experience) reared from 5 to 8 young each; only 12 of the 35 experimental animals (animals with no previous


experience of nursing young) succeeded in rearing young, and these reared only from 1 to 3 young each. Of the control animals 56 per cent kept all their young alive, compared with 11 per cent of the experimental animals. Clearly, the previous experience of nursing and rearing the young had an effect on the animals' response to the combination of estrone treatment and stimuli from the young. Observations are lacking, however, that would indicate whether the difference between the experimental and control groups resided in the animals' responsiveness to suckling stimulation, or in their behavior toward the young, which might determine whether suckling could take place or not.

Riddle, Lahr and Bates (1935a, b, c, 1952) , reported that some virgin rats show retrieving behavior in response to prolactin injection. They stated that the care of the young shown by such animals is not equivalent to that usually seen in multiparous rats, but they did not make a comparison of the effects of the hormone injection on the behavior of virgin and of experienced rats. Loisel (1906) found that a bitch which began to lactate after a pseudopregnancy accepted three young rabbits which were placed with her, licked them, and facilitated their approach to her nipples (they could not suckle). This animal had never seen young before. Fisher (1956) found that a testosterone salt injected locally into the hypothalamus induced intense nest-building and retrieving behavior in some male rats. These animals were presumably quite inexperienced.

In connection with studies of mammalian parental behavior, it is unfortunate that no use has been made of the technique of comparing behavior elicited by hormone treatment in animals without previous experience with that elicited from animals with various amounts and kinds of previous experience. Such a technique has been extremely valuable in studies of sexual behavior. As I have pointed out, comparison of parental behavior at first and at later breeding episodes may not reveal the role of experiential factors in the changing pattern of behavior during each episode. This is sometimes because the experience of the animals during an early phase of the cycle


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HORMONAL REGULATION OF BEHAVIOR


may set the stage for its behavior at a later stage, so that the behavior at the later stage may appear quite normal, even though it is the animal's first experience, and even though learning did play a role in the development of the animal's capability for jierforming this behavior. If, by hormone treatment, we can put the animal directly into the physiologic condition characteristic of a later stage in the cycle, and then confront it with the situation characteristic of that stage, when it has not had any experience of the earlier stage, it is sometimes possible to throw into startling relief the role of experience in the progression of stages which normally occurs effectively even in the first breeding episode.

Rosenblatt and Aronson (1958a, b) have shown that previous sexual experience is an important variable affecting the induction of sexual behavior by androgen administration in male cats, and Valenstein, Riss and Young (1955) and Valenstein and Young (1955) found somewhat similar results in the guinea pig. The importance of considering species differences in such matters is seen in the fact that such previous experience appears to be unimportant in rats, compared to the other animals mentioned (Kagan and Beach, 1953; Beach, 1958b I. These studies are reported more fully in the chapter by Young.

Lehrman (1955) found that ring doves with previous breeding experience could be induced to feed young doves (by regurgitation) by the injection of approximately 450 I.U. prolactin over 7 days. Similar treatment of birds of the same age, but without previous breeding experience, failed to induce parental feeding behavior. Inexperienced birds so treated showed a striking suppression of sexual behavior, compared with untreated birds, and gave several behavioral signs of tension that are normally seen in animals before they regurgitate. However, they failed to make the approaches to the young which were reliably induced in experienced birds. The experienced birds did a great deal of gentle pecking at the head and body of the stimulus squabs, mostly concentrated on the head (the squabs normally respond to gentle pecking on the head by making the "beg


ging" movements which elicit regurgitation feeding). The inexperienced birds, on the other hand, did very little pecking of the young (no more than they did at other objects in the cage) , and what pecking they did was not in any way directed at or concentrated on the head of the squabs. It was apparent that the prolactin injection had induced in both these groups of birds a condition of tension, probably associated with the engorgement of the crop by the cropmilk produced in response to prolactin treatment, but that the inexperienced birds could not respond differentially to that part of the environment (the squabs) which could potentially provide stimulation which would reduce this tension.

Lehrman and Wortis (1960) used the same method in dealing with incubation behavior induced by progesterone injection. It will be recalled that experienced ringdoves can reliably be induced by progesterone administration to sit on eggs. We have compared the reaction of ring doves with and without previous experience to eggs presented by the experimenter, after the birds were injected with 100 /xg. per day of progesterone for 7 days before being tested. Striking differences were found between the behavior of the experienced and of the inexperienced birds. The experienced birds are all recorded as standing near the nest in less than one minute after being introduced into the test cage, whereas the median latency for this behavior in the inexperienced birds was 35 minutes. All of the experienced birds settled on the eggs for the first time within 26 minutes, whereas no inexperienced bird sat on the eggs in less than 56 minutes, and half of them did not sit at all. Birds riot injected with progesterone pay no attention to the eggs on the first day after being placed in the test cage, regardless of whether they are experienced or not.

It is clear that the animal's previous experience can alter the ways in which its behavior is influenced by hormone treatment, and that the interaction between the effects of previous experience and of hormone treatment is capable of providing a fruitful approach to the analysis of the development of the behavior patterns and of their physiologic bases.


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B. HORMONE SECRETION AS A BEHAVIORAL RESPONSE

At various points in our discussion, it has become apparent that external stimuli of various kinds, including some produced by other members of the species, may be influential in eliciting the secretion of various hormones. It may be helpful if we briefly discuss the physiologic basis of such re


1. Xeural Control of Hormone Secretion

Both the anterior lobe and the posterior lobe of the pituitary gland are connected to the hypothalamus, althougli in quite different ways.

It will be recalled that electrical stimulation of the anterior hypothalamus (Andersson, 1951b), or of the pituitary stalk (Cross and Harris, 1950), induces milk ejection due to the secretion of oxytocin by the posterior pituitary. The principal functional connection between the brain and the posterior lobe is by way of the hypothalamohypophyseal nerve tracts in the pituitary stalk (Green, 1951a). (The secretory cells of the neurohypophysis are themselves neural in embryonic origin.) Harris (1947b) implanted electrodes with their tips in various locations in the hypothalamus, pituitary stalk, and neurohypophysis; the electrodes were connected to a coil imbedded in the skull, so that they could be activated by holding a second coil near the animal's head without actually touching the animal. Harris was able to produce an antidiuretic effect in water-loaded animals by stimulating the neurohypophysis, the supra-opticohypophyseal tract of the hypothalamus, or any part of the intervening nerve pathway. The effects of such electrical stimulation could be duplicated by the injection of posterior pituitary extracts. This and other evidence (Harris, 1955) indicates that the secretory activity of the posterior lobe of the pituitary gland is under neural control, and that the nerve connection between the hypothalamus and the neurohypophysis plays an essential role in the regulation of neurohypophyseal activity.

In contrast to the situation in the pos


terior hyi)ophysis, the anterior lobe is very sparsely innervated, both in mammals (Rasmussen, 1938; Green, 1951b) and in birds (Wingstrand, 1951). On the basis of a thorough survey of the evidence, Harris (1955) concludes that there is no evidence of a secretomotor innervation of the secretory cells of the anterior hypophysis.

The principal connection between the hypothalamus and the anterior hypophysis appears to be by a portal blood system. In mammals, small branches of the internal carotid arteries form a plexus at the base of the pituitary stalk, from which capillary loops arise and penetrate into the tissue of the median eminence, where they come into intimate relationship with the nerve fibers of various hypothalamic tracts (Harris, 1955). The vessels of this plexus merge to form i^ortal vessels which lie on the surface of the pituitary stalk. Lower down on the stalk, these trunks divide again to distribute their blood to the cells of the anterior hypophysis. The arrangement in birds is similar, except that the capillary network lies on the surface of the median eminence, and its relationship with the nerve fibers of the hypothalamus is accomplished by the looping of nerve fibers from deeperlying cells to the surface and back (Benoit and Assenmacher, 1955).

Electrical stimulation applied directly to the anterior hypophysis of the female rabbit is ineffective in inducing ovulation (equivalent to stimulation of LH secretion) , whereas stimulation of tlie hypothalamus does induce this response (Markee, Sawyer, and Hollinshead, 1946; Harris, 1948). Since direct stimulation of the pituitary stalk is also ineffective, it seems that the effect of electrically stimulating the hypothalamus is to cause the transmission to the anterior pituitary gland of an excitatory effect by way of structures which are not themselves sensitive to electrical stimulation. (This, it will be seen, is in contrast to the neural excitation of the posterior pituitary.) Harris (1947a) and Green and Harris (1947) suggested that hypothalamic control of anterior pituitary secretion is accomplished through neurosecretory products of hyjiotlialamic cells, which are carried by tlie portal system fi'om the liyjiothalanuis down


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HORMONAL REGULATION OF BEHAVIOR


to the secretory cells of the pituitary gland. There is now abundant additional evidence of the correctness of Harris' concept of the neurohumoral relationship between the hypothalamus and the anterior pituitary gland (Harris, 1955).

In summary, there is ample anatomic and physiologic basis for concluding that the nervous system exercises detailed control over the activity of both the anterior and the posterior lobe of the pituitary gland.

2. Hormone Secretion as a Reflex

The preceding remarks imply that it should be possible for endocrine secretion to occur as a reflex response to stimulation of afferent neural structures and, therefore, hormone secretion may, in some situations, occur as a reflex response to external stimuli of the kind which we ordinarily know to give rise to behavioral responses. There is considerable direct evidence that this is indeed so.

In his classic papers on sexual cycles, F. H. A. Marshall (1936, 1942, 1956) pointed out the role which external stimuli might play in the regulation of breeding periods. The importance of such factors is becoming increasingly clear, not only in determining the timing of breeding periods during the year, but also in organizing the succession of changes within the breeding season itself (Maschkowzew, 1940; Aschoff, 1955).

Most animals breed only during a particular season of the year, and it has long been known that, in many species of birds and mammals, changes in light stimulation due to the changing length of the day constitute one of the principal regulators of the timing of the breeding season (Rowan, 1926, 1931; Bissonnette, 1937; Farner, 1955). Other factors, such as temperature, also play a role (Pitt, 1929; Marshall and Coombs. 1952; Engels and Jenner, 1956; Marshall and Disney, 1956).

Some tropical and Australian birds breed irregularly, whenever heavy rains occur (Baker, 1938; Marshall, 1951). In such species, the gonads of birds collected in the same locality just before a rainy period are inactive, whereas one or two months after a rainy period, birds of the same species have active gonads, but only in the


locality in which the rain has occurred (Keast and Marshall, 1954; Benoit, 1956). We have already discussed (see above, p. 1280) the experimental demonstration by Marshall and Disney (1957) of the nature of this effect.

Stimuli provided by the mate are of importance in the development of gonadal activity in many animals. Although the increasing length of the day in spring initiates gonad development in many birds, it is commonly found that they do not come into full breeding condition unless further stimulated by the presence of the mate (Riley and Witschi, 1938; Bissonnette, 1939; Burger, 1953; for review see Lehrman, 1959a). In colonial birds, mutual stimulation among the members of the colony appears to have the effect of synchronizing their reproductive cycles (Darling, 1938), so that larger colonies have shorter over-all breeding seasons than smaller ones; in very large colonies, groups of birds in any one part of the colony may have their breeding times more closely synchronized than those of the colony as a whole (Neff, 1937; Lack and Emlen, 1939; Disney and Marshall, 1956).

Female rabbits and domestic cats ovulate as a result of the stimulus provided by participation in copulation (Heape, 1905), which causes the release of gonadotrophic hormone from the animal's hypophysis. This effect can be duplicated by artificial mechanical stimulation of the vagina in cats, although less readily in rabbits (Greulich, 1934; Sawyer, 1949; Sawyer and Markee, 1959). Whitten (1956a) has shown that the timing of the estrous cycle of the female mouse can be modified by stimuli provided by male mice. This stimulation is probably olfactory, inasmuch as the length of the estrous period can be changed by placing a male in a small basket within the female's cage for several days, or by placing the females in cages recently vacated by males. Further, removal of the olfactory bulbs causes regression of the ovaries although it seems to have no such effect on the male gonads (Whitten, 1956b; Lamond, 1958, 1959). Conversely, forcing the association of female mice in large groups appears to suppress gonadotrophic activity (Whitten, 1959) .


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3. Hormone Secretion as a Conditioned Response

It is possible for the secretion of a hormone to occur as a response to a conditioned stimulus.

Grachev (1952) inserted a catheter into one mammary gland of a goat, and found that when he milked the other mammary gland, milk was ejected through the catheter. He then arranged to have a bell ring starting 15 seconds before the beginning of milking, and continuing through the milking session. After 18 such pairings of the bell and of the milking stimulus, the sound of the bell, without any accompanying milking stimulus, elicited an ejection of milk from the catheterized gland similar to that usually caused by the milking of the other gland. It is well known to dairy workers that milk ejection can occur in response to stimuli normally associated with the preparations for milking, such as the rattling of buckets, the washing of the udders, etc. (Ely and Petersen, 1941). Clinical reports indicate that lactating human mothers may eject milk in response to stimuli such as the sound of the baby's crying (Newton and Newton, 1948j, the sound of the nurse opening the door to bring the baby into the mother's room (Waller, 1938), and other stimuli associated with the anticipation of putting the baby to the breast (Newton and Newton, 1950; Campbell and Petersen, 1953).

The conditioning of anterior pituitary secretions is more difficult to demonstrate, and would not be expected to occur in the same form as the conditioning of posterior pituitary secretion, since the nature of the neurohumoral link between the hypothalamus and the anterior pituitary is such that the interval between external stimulus and hormonal response might be on the order of hours or fractions of an hour, rather than, as in the elicitation of oxytocin secretion from the posterior pituitary, on the order of minutes or fractions of a minute. Nevertheless, Freud and Uyldert (1948a) suggest that the superiority of the maternal care given to adopted young rats, and the higher survival rate of the young, when the foster mothers had had suckling experience, compared with those which had


borne young without being allowed to suckle them (Uyldert, 1943, 1946), is evidence of a conditioned elicitation of lactation. As I indicated earlier (see above p. 000), the data as presented do not demand such an interpretation, but the possibility is one which should be investigated. Craig (1913) and Whitman (1919) reported that doves reared solely by human keepers, or by foster parents of other species, might, when mature, lay eggs in response to stimulation by a human hand, or by a courting male of the foster species. In this case, we are undoubtedly dealing with some form of conditioning of the secretion of gonadotrophic hormones to external stimuli, but the nature of this conditioning and the course of its development are entirely obscure.


4. Parental Behavior and Refleiiy Induced Hormone Secretion

It is clear from the preceding discussion that there exists a well established anatomic and physiologic basis for the control of endocrine secretion by the nervous system, that this control in fact exists, and that it is therefore possible for an extensive variety of external stimuli, including stimuli provided by other members of the animal's species, to elicit different types of hormone secretion. Many of these stimulus-response relationships, involving the stimulation of hormone secretion, are important features of the physiologic basis of parental behavior and of the establishment of parentyoung relationships.

We have pointed out that external stimuli provided by the male may induce endocrine changes in many female birds, which in turn induce nest-building behavior. In some cases, stimuli provided by the nest contribute, in turn, to the stimulation of egglaying. Stimuli coming from the egg may then elicit the secretion of the pituitary hormone (s) W'hich maintain the bird in a state of readiness to incubate. After the eggs hatch, the presence of the young contributes to the maintenance of the physiologic condition appropriate for parental care of the young, and to the suppression of the secretion of those pituitary hormones


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HORMONAL REGULATION OF BEHAVIOR


which could induce a new cycle of courtship and nest-building. Thus, the succession of changes in behavior patterns which characterizes the breeding cycle depends partly on changes in hormone secretion which are in turn partially stimulated by the changing conditions of the environment (Lehrman, 1959a, b).

In mammals, the ability of stimuli i)rovided by the young to induce the maintenance of lactation, and to suppress the recurrence of estrus, further indicates that the changing pattern of the behavior of the mother is kept appropriate to the external situation partly through the fact that the endocrine changes which influence her behavior are themselves capable of being influenced by the external situation.

The readiness with which milk ejection can be conditioned poses a number of problems of special interest in connection with the development of mother-young relationships in mammals. If the sensations of tension arising from mammary engorgement play a role, as has been suggested, in the motivation of maternal nursing behavior, it must be borne in mind that the milk-ejection response is itself an increase in tension in the mammary glands. Since young animals characteristically become active just before and during the time when they are fed, it seems likely that changes in intramammary tension will occur as conditioned responses to the sights and sounds characteristic of the young. The occurrence of such conditioned responses, their manner of formation, and the contribution they make to the maintenance of mother-young relationships are all problems which should be most rewarding to the investigator who attacks them.

Both in birds and in mammals, tlie establishment and maintenance of relations between the parent and the young (or eggs) is a process, or series of processes, of great complexity, involving a reciprocal interaction between, on the one hand, hormonal effects on behavior, and on the other, the effects of external stimuli (including those arising from the behavior of the animal and of its species-mates) on the patterns of hormone secretion.


C. MECHANISMS OF HORMONAL ACTION ON BEHAVIOR

1. Formulation of the Problem

The interpretation of the manner in which hormones infiuence behavior patterns is an extremely complex problem. As Beach (1948j has pointed out, and as must be apparent from much of the data presented in earlier' sections of this chapter, a behavioral response does not typically depend on one and only one hormone, nor is any hormone known which produces one and only one effect on the organism. However, when we know that a hormone has an influence on the development or occurrence of a behavior pattern, we may usefully ask which of the various organic effects the hormone is known to have are relevant to its effect on the behavior pattern, and whether additional organic effects must be assumed in order to explain the fact that the hormone has the observed effect on the behavior.

Hormones may influence behavior patterns through either peripheral or central effects. By "peripheral" effects, I mean that the hormone may change the animal's behavior by causing changes in structures or processes external to the central nervous system, which changes in turn result in alterations in the pattern of afferent inflow. Such changes may consist of grow^th changes in structures used in the behavior (Lehrman, 1955) , of changes in vascularity which influence the conditions of tension in the tissues concerned (Clark and Birch, 1946; Birch and Clark, 1946, 1950) , of changes in sensitivity of a sensory surface (Freud and Uyldert, 1948b; Schneider, Costiloe, Howard and Wolf, 1958), of the development of sensitive structures (Beach and Levinson, 1950) , etc.

By "central" effects, I mean that a hormone may influence the animal's behavior by a direct effect on structures of the central nervous system which are in some way involved in the organization and production of the behavior. Such effects may be relatively unspecific excitatory effects influencing "arousal" systems such as the reticular activating system (Magoun, 1952a, b; Dell,


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19o81)), or they may be more si)ecific effects on brain structures involved in the organization of specific behavior patterns (Fisher, 1956; Harris, Michael and Scott, 1958).

Morgan (1943, 1957, 1959) proposed the concept of "central motive state," by which he means a state of arousal of a center in the central nervous system which, once aroused, persists without outside support from sensory or other input, which predisposes the organism to react in certain ways to particular stimuli and not to react to others, and which "emits" specific patterns of behavior. This theory is, in many resj)ects, remarkably similar to that of Lorenz (1950) (Beach, 1942; Tinbergen, 1951).

The relevance of Morgan's theory for our problem arises from the fact that he regards as an important corollary of the theory the statement that chemical and hormonal conditions of the blood directly activate the central nervous system and induce central motive states, and that this is the major way in which hormonal effects are exerted upon behavior. In an earlier discussion (Lehrman, 1956b) , I heavily emphasized the role of peripheral effects of hormones as the means by which they influence behavior, and implied that direct central effects are of little or no imi)ortance. This was in the context of a critical discussion of a theory of behavior which depended, at that time, on the assumption of almost exclusively central forms of organization for most major behavior activities. In this context, I believe I unduly underemphasized the importance of central influences of hormones, and subsequent research confirms this view. On the other hand, Morgan's central theory is in part a reaction against the very influential earlier theory of Cannon a929, 1934), who believed that most states of motivation depend solely or primarily on the perception of the condition of peripheral structures. In this context, I believe that Morgan somewhat underemphasized the importance of pt'i'iphcral factors in the (lcvch)pment of motive states. At this point, it does not seem to me to be very profitable to attempt to determine which is in general "more im


portant," central or i)eripheral influences, since central and peripheral contributions are undoubtedly both involved in many cases, and are of varying importance in others. I shall attempt to illustrate the ways in which hormones may influence behavior patterns by selecting several patterns of behavior, including some discussed earlier in this chapter, for a further discussion of the mechanisms involved.

i2. Examples of Peripheral Contributions to Hormonal Effects on Behavior

Parental feeding behavior in ring doves. Injection of prolactin into ring doves with previous breeding experience causes them to feed young doves provided by the experimenter (Lehrman, 1955). Prolactin has many other effects on doves, some of which may be relevant to this behavioral effect. Prolactin causes the crop to become engorged with the substance which the Inrds regurgitate to their young (Riddle and Braucher, 1931); it causes a substantial temjiorary overgrowth of the liver and intestine (Bates, Riddle, Lahr and Schooley, 1937) ; it inhibits the secretion of FSH by the pituitary gland (Bates, Riddle and Lahr, 1937) , resulting in the suppression of gonadal activity (Bates, Lahr and Riddle, 1935).

Riddle (1935) assumed that, if this hormone influences a behavior pattern, it must be because of some interaction between the hormone and nerve tissue itself. In the case of the behavior we are considering, this is not necessarily so, since some of the effects already enumerated might be adequate to account for the arousal of parental feeding behavior. Lehrman (1955) injected prolactin into a group of doves with previous breeding experience and then, before testing them for regurgitation-feeding behavior toward squabs, anesthetized their crops by injecting a long-acting local anesthetic directly into the crop wall. These birds showed a sharply reduced incidence of regurgitation-feeding behavior, and a corresponding reduction in apparent "parental" interest in the squabs, as compared with a control group in which the same amount of the anesthetic was injected into the skin


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HORMONAL REGULATION OF BEHAVIOR


of the back. Lehrman concluded that the prolactin injections had induced regurgitation- feeding behavior through two main effects: it had induced the crop to become engorged by an accumulation of the degenerating epithelial cells which the birds regurgitate to their young (Beams and Meyer, 1931) ; and, by suppressing gonadal activity (Riddle and Bates, 1933; Nalbandov, 1953) it had eliminated sexual and aggressive behavior which would interfere with the parental behavior (Carpenter, 1933a, b). The fact that emetic responses in the pigeon are easily conditioned to external stimuli (Riddle and Burns, 1931) may be related to the fact that doves with previous breeding experience direct their behavior toward the head of the stimulus squab in such a way as to stimulate it to perform the movements which cause the parents to regurgitate food to it, whereas inexperienced birds show no such behavior.

Now, this experiment does not demonstrate conclusively that prolactin does not have any direct effects on the central nervous system which might be relevant to the elicitation of parental feeding behavior. It does show, however, that some of its peripheral effects play an important role. Prolactin has metabolic relations with some other tissues, w-hich are not shared by nerve tissue. Sgouris and Meites (1952) found that prolactin is inactivated (rendered incapable of inducing the development of the pigeon crop) by being incubated in vitro with slices of mammary gland, pigeon crop, ovary, or liver, all of which are known to be affected by prolactin in vivo. Slices of muscle (which is not known to be changed by prolactin) did not inactivate prolactin solutions. Further, brain slices had no effect.

It should be noted that the distinction between "central" and "peripheral" effects is not a rigid one, and that the behavioral effect of the hormone is not conceivable except in terms of a network of interrelationships between central and peripheral influences. For example, it is not known whether the antigonadotrophic effect of prolactin is exerted directly on the pituitary gland, or on the hypothalamus. Further, is the disappearance of sexual behavior be


cause of the suppression of gonad secretion caused by changes in peripheral structures, or in central ones? Finally, even in cases where peripheral effects are the most important ones, they can only act by altering the activities of central structures.

Nest-building behavior in rats. Hypophysectomy or thyroidectomy causes striking increases in the amount of nest-building activity in rats (Richter, 1937, 1941), in spite of the fact that these operations cause decreased "general activity," as measured in an activity wheel (Richter and Wislocki, 1930) . What is the basis of this effect?

It will be recalled that Kinder (1927) found that rats tended to do more nestbuilding at lower temperatures than at higher, and that similar results were obtained in mice by Koller (1956). This, plus the fact that thyroidectomy, which reduces body temperature (Richter, 1941), also causes increased nest-building, led Richter and others to suggest that nest-building behavior is in part a thermoregulatory mechanism, and that its regulation is closely related to factors affecting body temperature. There is a great deal of evidence in support of this view.

Richter (1941) found that thyroidectomized or hypophysectomized rats would die if the ambient temperature was kept only a few degrees below normal room temperatures, unless the rats had nesting material available, and could build nests. Stone and Mason (1955) tested hypophysectomized and intact rats in an apparatus in which the rats could rest in either of two chambers, which were kept at different temperatures. Temperatures varied from about 45°F. to about 95°F. The hypophysectomized rats selected the warm box significantly more often than did the controls.

Koller (1956) shaved the hair from the bodies of mice whose nest-building behavior had been measured. In all cases, the amount of nest-building on the next night after the shaving was higher than on the preceding night. Here, too, the amount of nest-building is apparently related to the body's need for heat regulation. In this connection, it may be noted that temperature preferences have been related to hair density in a quite different experimental


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situation. Herter (1936, 1952 j tested the temperature preferences of a number of small mammals in a gradient in which they could come to rest at any temperature in a considerable range. He found that mice and rats of different strains and species have characteristically different temperature preferences, and that these preferences are correlated with the thickness of the skin (Herter, 1941) and with the density of the hair, expressed in terms of number of hairs per unit of area (Herter and Sgonina, 1939) . When strains with different temperature preferences are hybridized, variations in the temperature preferences of the offspring are correlated with variations in the density of their body-hair (Herter and Sgonina,' 1939; Wolburg, 1952). Hair growth is in part under hormonal control (Mohn, 1958; Rennels and Callahan, 1959), although different skin areas are characterized by specific intrinsic growth properties of the hair and different areas of the body may thus respond differently to the same hormonal conditions (Whiteley, 1958). Hair growth in the domestic mouse is inhibited in late pregnancy (Danneel and Kahlo, 1947; Nay and Fraser, 1955). Progesterone inhibits hair growth in male mice (Danneel and Kahlo, 1947), although it does not seem to do so in rats (Yazaki, 1956; Mohn, 1958). We may recall that nest-building behavior in mice occurs earlier in pregnancy (KoUer, 1952) than it does in rats (Wiesner and Sheard, 1933), and that progesterone induces nest-building behavior in mice (Roller, 1952).

It is clear that at least some of the effects of pituitary hormones on nest-building behavior in mammals may be due to alterations in thermoregulatory mechanisms. This, of course, refers only to the regulating effect on the amount of nest-building behavior, and does not necessarily imply anything about the neural organization of the behavior patterns themselves, which is not illuminated by this type of work. Further, we are not justified in assuming that hormonal effects on thermoregulatory processes do not include effects by way of the central nervous system; we can merely say that any such effects are probably not specific to nest-building behavior.


Some further -problems. We have already remarked that the presence of incubation patches is, in many species of birds, correlated with the occurrence of incubation behavior (Tucker, 1943; Davis, 1945; Mewaldt, 1952; Parkes, 1953). Since the incubation patch is an area the increased vascularity of which is undoubtedly related to the transmission of heat to the egg, and since variations in ambient temperature (Nice and Thomas, 1948) and in egg temperature (Baerends, 1959) affect the intensity with which the birds sit on the eggs, it may be suggested that a change in skin temperature coinciding with the development of the incubation patch, and the cooling effect on it of sitting on the eggs, may be factors in the motivation of incubation behavior. Prolactin, which contributes to the maintenance of incubation behavior, raises the body temperature of roosters from 2 to 4°F. (Nalbandov, 1953). The rectal temperatures of incubating domestic fowl are not higher than those of nonincubating birds (Simpson, 1911), but Nalbandov (1953) suggests that this is probably the result of the lack of activity of incubating birds. It is unlikely that aff'erent inflow from the incubation patch is the most important source of motivation to incubate, because some species of birds incubate without possessing such patches. The contribution of such factors to the regulation of incubation behavior should nevertheless be further investigated.

There are other examples of peripheral effects of hormones on behavior, not related to parental behavior, which I have discussed elsewhere (Lehrman, 1956b). We may briefly cite one of them. Adult female dogs squat to urinate ; adult males raise one leg (Berg, 1944). Males castrated in infancy do not raise their legs to urinate, but will do so if injected with male hormone. Female puppies and spayed female dogs also show the male micturition pattern if injected with male hormone (Martins and Valle, 1948). Freud and Uyldert (1948b) showed that local anesthesia of the olfactory epithelium caused the disappearance of the male micturition pattern and its replacement by the female pattern. When the anesthesia wore off, the male pattern reappeared.


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HORMONAL REGULATION OF BEHAVIOR


They suggest that the hormone acts, not by activating or sensitizing a motor structure in the central nervous system, but by changing the pattern of afferent controL Changes in olfactory acuity and in the nasal mucosa characterize different stages of the human menstrual cycle (Elsberg, Brewer and Levy, 1935; Henderson, 1956), and olfactory acuity is affected by sex hormone administration to hypogonadal women (Schneider, Costiloe, Howard and Wolf, 1958; for review see Le Magnen, 1953).

As Morgan (1959) has pointed out, it is not at all necessary that a hormonal effect on behavior be through either exclusively peripheral or exclusively central influences. Both types of effect of the same hormone may contribute. We earlier presented evidence that the condition of mammary engorgement makes some contribution to the regulation of maternal nursing behavior. When Seward and Seward (1940) tested I'ictating guinea pigs in a device in whicli they had to cross a l)arrier to get to their young, and used the stiength of the tendency to cross the barrier as an estimate of the intensity of motivation to nurse, they found that animals tested just after being milked consistently showed less of this "drive"" than those tested when their mammary glands were full of milk. However, abdominal sympathectomy, which renders the mammary glands incapable of res])onding to hormone stimulation (Bacq, 1932a, 1); Coujard, 1943; Champy, Coujard and Demay, 1950), often fails to prevent the appearance of maternal attempts to nurse the young, although, in most of these reports, it is not clear whether diffei'ences between animals with and without previous nursing experience may be important. It is nevertheless clear that, although the state of mammary engorgement, induced by hormones, prol)ably contributes to the regulation of maternal nursing behavior, other factors, possibly including central effects, are also present.

3. Central Hormonal Effects on Behavior

In recent years, a good deal of evidence has been accumulating to show that many of the effects of hormones on behavior patterns are by wav of direct chemical effects


of the hormones on the central nervous system.

The development oj neural mechanisms. Kollros (1942, 1943) found that the implantation of small pellets of thyroxinesaturated agar into the brain of the frog tadpole could cause the lid-closure reflex, the appearance of which is associated with metamorphosis, to develop earlier on the side of the animal on which the pellet was im{)l anted than on the other side, where a control pellet without thyroxine was implanted. Kaltenbach (1953a, b) showed that a variety of structures could be made to metamorphose earlier than normal by local application of thyroxine. Weiss and Rossetti (1951 ) found that local application of thyroxine in immature tadpoles caused the premature atrophy of Mauthner's cells, accompanied by accelerated growth of neighboring nerve cells, both phenomena associated with normal metamorphosis.

Additional evidence that humoral influences associated with the actions of hormones play a role in the differentiation of neural structures mediating various beliavior patterns may be found in a recent important study by Phoenix, Goy, Gerall and Young (1959). These workers administered testosterone propionate to mother guinea pigs during pregnancy, and then studied the sexual behavior of their offspring after they reached adulthood. No effects were observed on male offspring. Genetically female offspring showed greatly reduced capacity for female sexual beliavior, and increased tendencies to perform male sexual behavior. The androgen treatment similarly resulted in morphologic hermaphrodites, genetic females in which the external genitalia were, at birth, not distinguishable from those of untreated males. Since the amount of male hormone re(iuired to cause suppression of female sexual behavior was less than that required to cause morphologic abnormalities, it is not likely that the effects on sex behavior were mediated by changes in the sex organs. Various abnormalities of the ovarian cycle were also noted (Tedford and Young, 1960), which together with the disturbances of sexual behavior suggest that the effect of the androgen treatment was, or included.


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an action on the liyi)otlialamiis. The involvement of the hypothalamus (or at least of extra-ovarian factors) is suggested by the fact that the ovaries appeared histologically normal until puberty, when the abnormal estrous cycles began (Turner, 1939; Tedford and Young, 1960). At this point it may be remarked that the differences in secretory activity and in responsiveness to gonadal hormones between male and female pituitary glands (Pfeiffer, 1936, 1937) are apparently due, not to sexual differentiation of the hypophysis during development, but to differentiation of the hypothalamus (Harris and Jacobsohn, 1952; Martinez and Bittner, 1956). There is evidence, summarized by Harris (1955), that the hypothalamus is differentiated into male and female types of activity (with respect to its relationship with the pituitary gland), very early in life.

Stimulation and regulation of behavior by central effects. In addition to these effects upon the ontogeny of central mechanisms, evidence has recently accumulated that some of the effects of hormones in arousing and regulating behavior in adult animals are exerted through direct effects on central nervous structures.

Fisher (1956) injected sodium testosterone sulfate into various hypothalamic loci by a cannula introduced through an implanted electrode. In a number of male rats tested by this method, he found various combinations of "maternal" and "sexual" behavior, sometimes occurring simultaneously. Among the responding animals, Fisher noted that the overt responses were characterized by exaggerated speed, compulsiveness, and frequency, as compared with the normal sexual and maternal behavior of untreated animals. In some animals, the behavior continued without decrement for 90 minutes after the chemical stimulus was supplied.

Harris, Michael and Scott (1958) im]ilanted into the brains of ovariectomized female cats a fine platinum wire which had been dipped into a molten fatty acid ester of stilbesterol, so that the tip of the needle was coated with a thin film of the estrogenic substance. Of 17 animals so treated, in which the tip of the implanted wire was


in the posterior hypothalamus, 13 developed estrous behavior, including complete mating responses to male cats. In a control group in which the same implant was made into regions of the brain other than the hypothalamus, only one of the 19 animals showed any estrous response. Although on systemic administration of estrogens, mating behavior is stimulated only after a fully cornified vaginal smear has developed (Harris, 1959), 9 of the 13 animals which showed mating behavior in response to the hypothalamic implant had reproductive tracts completely indistinguishable from those of untreated control animals, as shown by vaginal smears, weight of the genital tract, and endometrial development. This experiment makes it seem likely that, although estrous behavior normally occurs at a time when the reproductive tract is in an estrous condition, the behavior itself is aroused not by afferent effects of the condition of the reproductive tract, but by the direct effects of gonadal hormones on the brain.

A number of other experiments show that humoral conditions which are known to affect behavior have direct and, to some extent, local effects on central nervous structures. Flerko and Szentagothai (1957) implanted small fragments of ovarian tissue into various regions of the hypothalamus and hypophysis of female rats. Estrogenic hormone produced by the ovary is capable of inhibiting the secretion of FSH by the pituitary gland (see chapter by Greep). Flerko and Szentagothai found that ovarian fragments implanted into the anterior lobe of the hypophysis had no effect on FSH secretion. Implants in the mammillary region of the hypothalamus failed to induce a significant change in FSH secretion (as indicated by uterine weights), whereas imi)Iants into the neighborhood of the paraventricular nuclei caused a significant decrease in uterine weights. From this experiment, it seems probable that the effect of the ovarian hormone on pituitary secretion is mediated by its effect on hypothalamic activity.

Andersson (1953) found that the injection of very small amounts of hypertonic saline solution into the third ventricle of


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the brain of goats would cause them to drink. Miller, Richter, Bailey and Southwick (Miller, 1957b) repeated this observation in cats, and found that the injection of no more than 0.15 cc. of slightly hypertonic (2 per cent) NaCl solution caused an increase in the volume of water drunk by the animals, whereas injection of the same amount of distilled water decreased consumption. Cross and Green (1959) observed the activity of single neurones in the hypothalamus of rabbits, and found that the rate of firing of neurones in the supra-optic nuclei was increased by small injections of hypertonic NaCl into the carotid arteries, whereas the rate of firing of neurones in the paraventricular nuclei was reduced. These authors were primarily interested in the effects of blood tonicity on posterior pituitary secretion, but their results, taken in conjunction with those of Andersson and of Miller, further indicate the existence of local effects on hypothalamic activity, exerted by humoral conditions known to be relevant to the elicitation of various behavior patterns.

With the exception of the brief report by Fisher (1956), none of the material on direct central behavioral effects of hormones has been related directly to the elicitation of parental behavior. However, the general background of evidence clearly indicates that central influences of the relevant hormones will be an important factor in future research on this, as on other types of behavior.

The problem of the specificity of central neuro-endocrine mechanisms. Some of the evidence cited above has been noted by Morgan (1959) as supporting the concept of "centers" for motivation and for behavior, as places in which "drive" or motivation is aroused, and also from which behavior is "emitted" (Stellar, 1954). As Hinde (1959) points out, the evidence at hand does not permit the firm conclusion that all the important aspects of either the motivation or the organization of the types of behavior patterns we are discussing are gathered together into single loci.

Copulation, or artificial stimulation of the vagina, are followed by changes in electrical activity which can be detected


by electroencephalographic techniques, in both the female domestic cat (Porter, Cavanaugh, Critchlow and Sawyer, 1957) and rabbit (Sawyer and Kawakami, 1959). These aftercoital effects can be induced by treatment with some pituitary hormones, such as gonadotrophins and posterior pituitary hormones, which are known to be released as a result of stimuli associated with copulation (Kawakami and Sawyer, 1959a). Sawyer (1959) and his co-workers therefore conclude that these changes in central nervous activity are induced by the effects of the hormones on the nervous system, in effect a feed-back system. Kawakami and Sawyer (1959b) found that various hormones affect the threshold for the arousal of these electroencephalographic changes by electrical stimulation of the brain.

Now, Sawyer (1959) points out that the effects of ovarian hormones on the thresholds for brain stimulation are very widespread and generalized. Effects of hormones on the brain-stem reticular formation (Dell, 1958a, b; Sawyer, 1958) or in other parts of the brain may result in quite specific changes in the activity of, say, a hypothalamic nucleus, although the effects of the injected or endogenous hormone might not themselves be specific to that "center."

The work on the injection of minute quantities of hormones into specific loci, such as that of Harris, Michael, and Scott (1958), and Flerko and Szentogothai (1957), does not yet demonstrate that specific "centers" are selectively sensitive to the particular hormones which normally arouse behavior mediated by those centers. The fact that ovarian fragments cause suppression of pituitary activity when implanted into one hypothalamic area, and not in another, may mean either that the two areas are differentially sensitive to estrogen, or that the nuclei of that region of the brain are all sensitive to estrogen, but only some of them are so related to the pituitary gland that their activity can cause J

changes in pituitary secretion. Similarly, *

the demonstration that small amounts of estrogen released into certain hypothalamic nuclei induce female sex behavior should undoubtedly be followed by attempts to determine whether other kinds of chemical


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stimulation at the same locus will induce the same kind of behavior, and whether stimulation by the same substances at different loci will induce different kinds of behavior. A suggestive indication is found in the paper by Fisher (1956) who found that injection of the same testosterone salt into different hypothalamic loci would result, in some cases, in maternal behavior, in other cases in sexual behavior. Obviously, we must be cautious about interpreting the available data on central effects of hormones as if they demonstrated the existence of different "centers," each specific for a particular behavior pattern, and each selectively sensitive to a particular kind of humoral influence.

Evidence from the effects of brain lesions on various types of motivated behavior, and on the effects of various drugs (reviewed by Miller, 1957a, b; Hinde, 1959) indicate that some treatments appear to have different effects upon a "motive state," depending on how the state is measured. For example, some lesions in the hypothalamus increase the amount of food consumed, whereas they decrease other measures of "hunger," such as the rate at which the animal will press a bar in order to get food. As Hinde (1959) has pointed out, this suggests the need for caution in interpreting evidence that behavior is both motivated and organized in centers specific for the behavior patterns.

An additional reason for reserve in interpreting the effects of hormones upon "centers" lies in the fact that the sensitivity and activity of peripheral sense organs may often be affected by centrifugal influences from the central nervous system (Granit, 1955) , and thus that humoral factors influencing the activity of central structures may nevertheless be influencing the character of the behavior by a process which includes peripheral contributions (Lehrman, 1956a; Prechtl, 1956). Although this does not mean that the hormones are not themselves acting on a central state, it does mean that the behavior resulting from the change in the central state is not necessarily organized within, or "emitted" from, the "center."


4. The Importance of Behavioral Analysis

Proper definition of the behavior variables which are influenced by hormones requires a careful analysis of the organization of the over-all behavior pattern of the animal as a prerequisite to studying the behavioral effects of various hormone treatments. For example, in some birds, such as the black-headed gull (Moynihan, 1953) and herring gull (Baerends, 1959) a good deal of nest-building often occurs as a "displacement activity," when the birds are disturbed on the nest by extreme egg temperatures, eggs abnormal in size, shape, or number, and other disturbances at the nest. Since, as I have pointed out, the endocrine condition during the pre-ovulation nestbuilding period and that during the incubation period are quite different, nest-building during the incubation period may have a very different physiologic basis from that during the normal period of nest-building. If analysis of the behavior had not itself revealed differences in the way in which building takes place at these two periods, the undifferentiated statement that "nestbuilding" takes place at both of these periods would lead to confusion in the analysis of the hormonal basis of the behavior.

Courting male canaries sometimes dangle a piece of string or cotton before the female. Behavior of this type is sometimes referred to as "incipient nest-building" in the ornithological literature. Shoemaker (1939) found that female canaries injected with testosterone propionate postured like courting males, and also engaged in this string-carrying behavior, reminiscent of the carrying of nesting material. Such birds did not, however, build nests. In this case the nest-building-like behavior of courtship, and real nest-building, are quite differently affected by hormones.

These examples show that a clear understanding of the organization of the behavior, based on an analysis of the over-all behavior pattern, is an important prerequisite for analysis of hormonal effects upon behavior. Simple counts of "carrying nest material," or "nest-building behavior," and studies of the effects upon such counts of hormone injections, could lead to mislead


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ing results in the hands of observers who did not have an accurate conception of the organization of the animal's behavior patterns.

D. GENETIC AND EVOLUTIONARY ASPECTS OF HORMONE-INDUCED PARENTAL BEHAVIOR

1. Taxonomic Differences in Parental Behavior and in the Mechanisms Underlying It

Taxonomic variation in parental behavior patterns. Throughout our discussions of parental behavior, it has been clear that each component of the over-all pattern of parental behavior can occur in a wide variety of forms, and that these forms of behavior are characteristic of the species of animals in which they occur. Generally speaking, patterns of behavior, including parental behavior, may be characteristic not only of species, but also of the higher taxonomic categories, such as genera, families, orders, and even classes. Indeed, in spite of the fact that scattered exceptions may be found, the statements that mammals nurse their young, and that birds incubate their eggs, may be used to characterize membership in these two classes with almost as much precision as any single statement about structure.

Characteristic differences can be found between different orders of mammals with respect to their parental behavior and the structure of parent-young relationships. For example, the herd-living ungulates are usually characterized by a high degree of individual recognition of the young, by a long period of association between mother and young, and by the continuation of occasional nursing behavior long after the young have become capable of grazing for themselves (Altmann, 1952). In most rodents, on the other hand, relations between mother and young are not so long-lasting, "adoption" of young by strange mothers, even of other species, occurs very easily, and the transition between suckling and the eating of solid food is fairly abrupt (Eibl-Eibesfeldt, 1958). Relations between the male and the young, too, are different in different families of mammals. For example, among bears, the male is likelv to attack and even


to eat its own young when association between them is forced, as in a zoo cage, although in the various species of wolves, the males often take an active role in the care of the young. Different groups of mammals also have characteristic ways of carrying their young when retrieving them, some carrying the young by the scruff of the neck, some by the belly, and some holding the young in the hands (Curio, 1955; Hediger, 1959).

The type of nest built by birds, the methods and patterns of incubating, and the pattern of parental care of the young may all be characteristic of particular families or genera. For example, Mayr and Bond (1943) noted that different genera of swallows reliably use different methods of nestbuilding, some laying eggs in natural hollows, some excavating burrows in sand- or mud-banks, others constructing nests of mud. All swifts use their saliva for sticking nesting materials together (Lack, 1956a), and their salivary glands develop and regress seasonally (Johnston, 1958). It is possible to trace, within one family, evolutionary changes in the patterns of parental behavior, as in the ease we have already discussed (see above, p. 1277), of the New World cuckoos in which some species are parasitic, others communal nesters, and still others nest in colonies of individual nests (Davis, 1942b).

Although patterns of parental behavior may characterize entire families, we can also find many ways in which closely related animals have differing patterns. For example, the male Galapagos sea lion takes part in the care of the young, unlike other species of seal (Eibl-Eibesfeldt, 1955c). Hohn (1957) reports that female Pacific eiders always fly from the nest when an observer approaches within a few feet, whereas incubating king eiders sit so tight on the eggs that some allow themselves to be picked off the eggs by the observer. Watson (1908) observed that male and female noddy terns change places on the eggs about every two hours, although the closely related sooty terns change places only once a day. Van Oordt (1934) found that common terns began incubating after the laying of the first egg, whereas arctic terns did


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not begin incubating until the full clutch had been laid. The kittiwake, a species of gull, differs from other gulls with respect to many behavior patterns, most of them adaptations to the kittiwake's peculiar (for a gull) habit of nesting on cliffs (Cullen, 1957). For example, in most gulls, the l)arent regurgitates food for the young, which picks it up from the ground; the young kittiwake takes the food directly from the bill of its parents.

Differences in hormonal mechanisms in different animals. Beach (1958a) points out that identical hormone treatment may, in many cases, cause quite different forms of behavior in different kinds of animals, and that the evolutionary changes in behavior between different species have therefore affected, not the nature of the endocrine mechanisms inducing the behavior, but rather the nature of the neural and o^her structures which respond to the hormones. For example, injection of testosterone propionate induces male sex behavior in valley quail (Emlen and Lorenz, 1942) and in ring doves (Bennett, 1940); but the form of the behavior which is induced is quite different in the two species.

However, in spite of the fact that the nature of the endocrine secretions does not appear to change very much during evolution (at least in warm-blood animals) , there are many cases in which the patterning of these secretions and the nature of the somatic responses are very different in different animals. We may thus find cases in which the nature of the endocrine mechanisms underlying various behavior patterns itself changes, or is different in different types of animals.

Eckstein (1949) points out that different species of mammals show very different relationships between environmental cycles and the reproductive system. Thus, some breed in spring, some in the autumn, and some breed aperiodically. Some ovulate spontaneously, some only on stimulation (Asdell, 1946). In addition to species differences in the way in which endocrine patterns themselves occur, there are striking differences in the ways in which the hormones influence behavior in different specie*. For example, ]\Ioore (1920) trans


planted ovaries into castrated young rats and guinea pigs. When adult, the rats showed female-like maternal behavior toward young animals, although no such behavioral changes were induced in the guinea pigs. Pregnant mice build substantial nests starting about the middle of pregnancy, whereas the corresponding behavior in rats does not occur until just before parturition (Roller, 1952; Wiesner and Sheard, 1933). This suggests that the hormonal basis of nest-building is different in the two species. Progesterone induces nest-building in mice (Roller, 1956), although it does not appear to have this effect in rabbits (Zarrow, Sawin, Ross and Denenberg, unpublished). Indeed, the fact that experimental removal of the corpus luteum during pregnancy induces nest-building behavior in the rabbit (Rlein, 1956) suggests that progesterone might have quite opposite effects in the rabl)it and in the mouse.

In birds, too, there are many examples of different hormonal responses to similar situations, and of different effects of hormones on patterns of behavior, in different species. Rept under similar conditions of light and temperature, ring doves breed all year, and the related mourning dove breeds only in the spring and summer (Cole, 1933) . When sitting on infertile eggs, mourning doves abandon the nest after about 17 days, whereas domestic pigeons continue to sit for about 22 days (Cole and Rirkpatrick, 1915). Progesterone, which induces incubation behavior in ring doves (Riddle and Lahr, 1944; Lehrman, 1958b), has no effect on incubation behavior in chickens (Riddle, 1937) or canaries (Robayashi, 1952; Robayashi and Okubo, 1954). Testosterone propionate interrupts established broodiness in hens, but seems to have no effect on established incubation behavior in pigeons (Collias, 1940, 1950). Treatment with estrogen and prolactin, which induces the formation of the incubation patch in finches (Bailey, 1952), fails to induce it in the cowbird, which normally does not incubate eggs (Selander, 1960). Since the pituitary glands of cowbirds have been found to contain prolactin (Hohn, 1959), the failure of broodpatch formation in these parasitic birds is apparently due to the fact that the ventral


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skin is not sensitive to the hormones which induce it in other species.

It is apparent that, both in birds and in mammals, a variety of hormonal mechanisms, and of types of tissue responsiveness to hormones, may be found in different species, and that, as a consequence, similar behavior patterns in different animals may sometimes be underlain by rather different physiologic mechanisms.

2. Strain Differences and Genetic Factors

Although the study of behavior genetics has been growing very rapidly in recent years (Fuller, 1960; Fuller and Thompson, 1960), little information is available about genetic factors influencing parental behavior. It is to be hoped that this deficiency will soon be remedied.

Different strains of domestic hens differ sharply with respect to the number of birds which become "broody," thus interrupting their egg production (Pearl, 1914). For example, Goodale (1916) noted that only 2 to 3 per cent of White Leghorn hens ever become broody, compared with 93 per cent of Rhode Island Red hens. Riddle, Bates and Lahr (1935) found that prolactin injected into laying hens induced incubation behavior in 16 out of 20 birds of a broody race, but in only 1 out of 10 birds of a nonbroody race. Similarly, Nalbandov and Card (1945) found that the amount of prolactin required to induce roosters to care for chicks was much greater when the birds came from a nonbroody race than when they were of a broody race. For example, White Leghorn roosters required 500 to 700 I.U. of prolactin, whereas Cornish roosters required only 300. (Note that 50 I.U. is sufficient to induce broodiness in a laying heji.) Bates, Riddle, and Lahr (1939) found that different races and strains of pigeons differ markedly in their response to prolactin. Some strains required as much as 5 to 8 times as much prolactin as did others, for the same effect on the crop-sac. Byerly and Burrows (1936) found that the pituitary glands of genetically broody hens contained more prolactin than did those of nonbroody birds. This suggests that the broody and nonbroody races may differ not only in their responsiveness to prolactin, but also in their production of this hormone.


Carson, Bacon, Beall and Ryan (1960) found that broodiness interferes with egg production in some strains of fowl, but not in others.

Goodale, Sanborn and White (1920) showed that a nonbroody strain could be quickly developed from a broody one by selective breeding. Yamashina (1956a, b) selected nonbroody females from among a flock of Plymouth Rocks, and mated them with males which could not be made broody by prolactin injection. By this method, he reduced the percentage of broodiness in the flock from 84.5 per cent to 3.8 per cent. Various investigators have shown that broodiness depends on several pairs of genes, some sex-linked, some autosomal (Punnett and Bailey, 1920; Roberts and Card, 1934; Hays, 1940; Kaufman, 1948).

Leopold (1944) compared the behavior of wild turkeys with that of domesticated and hybrid strains. Wild mother birds with young tended to crouch quietly at the approach of a human, whereas the domestic and hybrid mothers noisily led their young away. Leopold related the differences in wildness between the two strains of turkeys in ])art to differences in adrenal physiology, the ratio of adrenal weight to body weight being more than twice as great in the wild birds as in the domestic strain.

Sawin and Curran (1952) found that various strains of rabbits, developed in their laboratory, differed with respect to the time of nest-building, the average quality of the nest, the choice of location of the nest, and the extent to which young were scattered, or in some cases eaten. The strains which they studied had been produced by selection for studies of growth and differentiation, not for breeding characteristics. As we might expect, they found no evidence of a single factor for "maternal behavior," since various of the characters with respect to which they found race differences were correlated with each other in some races, and not in others. In a later study, Sawin and Crary (1953) suggested at least two or three genetic factors, one influencing the time of building and lining the nest, others determining the nature of the nest, the quantity of the lining, etc. Hauschka (1952), studying strains of mice


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developed for cancer research, found strain differences with respect to the frequency of "cannibahsm" — eating of the young.

King (1958) found that females of two closely related subspecies of deer mouse differed with respect to the intensity with which they would protect the young against an intruder. The difference between these two subspecies may be a difference in aggressiveness, which is known to be capable of alteration by selective breeding (Scott, 1958), and which might here be seen to be influencing the expression of parental behavior. A number of other behavioral and physiologic characters which may be related to the expression of parental behavior have been shown to be susceptible of alteration by selective breeding: prolactin content of the pituitary gland (Grosvenor and Turner, 1957) ; temperature preferences (Wolburg, 1952) ; exploratory behavior (Carr and Williams, 1957; McClearn, 1959) ; efficiency of lactation (Falconer, 1953) ; hoarding (Stamm, 1954, 1956) ; various aspects of "emotionality" (Broadhurst, 1958), etc. (Fuller, 1960). It may be suggested that systematic study of the genetics of parental behavior may soon be as rewarding as has been the study of various genetic aspects of sexual behavior (Young, 1957).

E. THE EOLE OF PARENTAL BEHAVIOR IN THE DEVELOPMENT OF THE YOUNG

The biologic function of parental behavior is, of course, to provide conditions which foster the development of the eggs and young. The requirements of the eggs and young thus form part of the complex of environmental conditions, in adaptation to which parental behavior has evolved. The characteristics of the parent are, of course, also a source of selection pressure guiding the evolution of the characteristics of the young. This is not the place for a full discussion of this problem, but we may briefly indicate some of the ways in which parental behavior is adapted to the requirements of the development of the young. It is apparent that experience gained from contact with other animals including the parents is prerequisite for the normal display of much of hormonally induced behavior.


1. In Birds

Incubation behavior is clearly related to the fact that most bird embryos require for their development temperatures higher than the usual environmental temperatures. Egg temperatures are consistently maintained at a high level by the transfer of heat between the ventral surface of the incubating parent's body and the surface of the egg (Kossack, 1947). We have already pointed out that the average temperature of eggs during incubation is approximately the same in birds of the same species breeding in different climates, probably indicating that the varying incubation behavior of the parents produces an approximately constant temperature of the eggs (Irving and Krog, 1956). Farner (1958) measured the temperature at the egg-body surface in the nests of incubating yelloweyed penguins, and compared them with cloacal temperatures. He found that, although the body temperature of the bird did not change during the incubation period, the incubation temperature (temperature at the egg-body interface) gradually increased from about 20 to 25°C. to about 38°C. during the incubation period. This gradual increase in temperature is presumably due to some combination of increasing efficiency of incubation behavior and increasing vascularity of the incubation patch. Metabolic activity of the developing embryo does not seem to be involved, because the curve of temperature change was the same for nests with eggs which failed to develop as for nests with live eggs.

There is great interspecific variation in the speed of development of avian embryos, and in the incubation behavior of the parents (Stresemann, 1934). Some indication of the significance of the details of parental incubation behavior in fostering the development of the eggs may be seen in the fact that great difficulties are encountered in attempting to incubate eggs of wild birds in artificial incubators. Daniel (1957) found that the eggs of red-winged blackbirds developed well in artificial incubators up to the 7th day, and that eggs collected after the 7th day could be brought to hatching in such an incubator, but that it


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was extremely difficult to keep the embryo alive over the 7th day. It is not known exactly how the behavior of the parent during this period makes it so superior to the best efforts of a human being using an artificial incubator. In the domestic hen, there are several critical periods, during which most deaths of embryos occur in artificial incubators (Romanoff, 1949). New (1957) found that eggs recjuired regular turning lietween the 4th and 7th day of incubation in order to hatch. Eggs turned only on those 4 days had the same degree of hatchability as eggs turned throughout incubation (21 of 35 eggs so treated hatched, compared with 24 out of 35 eggs turned throughout incubation). If the eggs are turned only between the 8th and 11th day of incubation, the number of eggs which hatch (6 of 35) is the same as in the case of eggs which are not turned at all during incubation. Clearly the behavior of the parents in regularly turning the eggs is an essential prerequisite for the successful development of the embryos (Westerskov, 1956) .

Newly hatched altricial birds, such as the house wren (Kendeigh and Baldwin, 1928; Baldwin and Kendeigh, 1932) are poikilothermic at hatching, with the capacity for temperature regulation developing gradually, starting at 3 days post-hatching, and continuing up to about 9 to 12 days of age. The field sparrow becomes homoiothermic at about 7 to 10 days of age (Dawson and Evans, 1957). Precocial birds, such as the western gull (Bartholomew and Dawson, 1952) are in part homoiothermic at hatching; there are some indications that these birds may begin to develop the ability for temperature regulation before hatching. The parents of altricial birds characteristically brood the young much more attentively, and for a longer period, than do the parents of precocial birds (Kendeigh, 1952). Bartholomew and Dawson (1954) studied the development of temperature regulation in young browm pelicans and great blue herons, both altricial species, and in western gulls, a precocial species, all nesting on the same hot, dry island in the Gulf of California. When they deprived the birds of the care of their parents, they found that the young gulls had a consistently greater ca


pacity for temperature regulation than did either the pelicans or the herons. In the words of these authors, "the successful nesting of these three species in the same area at the same time despite their differences in capacities for temperature regulation, emphasizes the importance of behavior as a supplement for physiological mechanisms in birds."

The feeding behavior of parent birds of different species is differentiated in ways which correspond to the different ways in which their young take food. For example, young passerine birds, such as the European blackbird, at first "beg" for food by lifting the head vertically and opening the gape wide, simultaneously uttering a characteristic sound; the parents of such species feed the young by dropping food into the open mouth (Tinbergen and Kuenen, 1939). Parent gulls, on the other hand. regurgitate fish which they hold in the bill in front of the young, which peck at the bill, stimulated by various aspects of its color and shape (Tinbergen and Perdeck, 1950; Collias and Collias, 1957). Chicks of some such species cannot pick up the food if it is dropped on the ground, but must get it from the bill of the parent (Hardy, 1957) . We could compile, from the ornithological literature, a considerable list of the varying details of the manner in which parent birds feed their young, and the correspondences with the forms of behavior of the young.

The development of feeding behavior in young birds seems, in some species at least, to be partly influenced by the behavior of the parents toward the begging young. Rand (1942) reared four loggerhead shrikes by hand to the age of 21 days, when the first signs of pecking at food (instead of simply receiving it from the "parent") appeared. Two of the birds were subsequently kept in a cage with food always present, and handfeeding was stopped as soon as possible. The remaining two birds had no food in their cage, and were fed exclusively by hand. The first group of two birds never begged after 45 days of age, whereas the second pair of birds (fed by hand) was still begging from their keeper at the age of 7^2 months, although they could pick up food from the floor. Rand (1941) found similar


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results with young curve-billed thrashers: the greater the amount of care devoted to the birds, the longer the period of begging. Craig (1908) stated that the first learning of young pigeons to differentiate individuals comes about because the mother becomes unwilling to feed the young long before the father does so. Petersen (1955) observed that the first flights of nestling bank swallows were induced in part by the increasing reluctance of the parents to feed them.

Of course, these may be largely effects on the rate of development of the change from begging to independent feeding, which change may nevertheless occur without being stimulated by any change in the parent's behavior. Miller (1921) found that young house finches being reared by hand abruptly changed from begging to self-feeding without any change in the treatment which they were getting.

Young birds of many species apparently become conditioned to follow parents having particular characteristics by means of a very rapid learning process occurring during a particularly sensitive period shortly after hatching. This is the phenomenon of "imprinting" (Lorenz, 1935; Hinde, Thorpe and Vince, 1956; Hess, 1959).

The experiences of young birds with their l)arents sometimes also contribute to the nature of their mating preferences in later life, although it has not yet been demonstrated that this effect depends upon as sharp a critical period of learning as does the development of the following response of the young birds themselves. Craig ( 1914) noted that male ring doves reared by human keepers directed their courtship disl-)lays toward men, and particularly toward the human hand. When later allowed to associate with doves, they gave up their attachment to humans very slowly and incompletely, and not in all cases. Nicolai (1956) found that bullfinches reared in isolation accept a human keeper as the "mate." This attachment can be reversed during the bird's first autumn and winter if it meets other bullfinches, but becomes irreversible during the first mating season. The importance of such learned attachments to individuals of the species, based upon


early experience with the parent, has been pointed out by a number of authors (Cushing, 1941; Cushing and Ramsay, 1949; Beach and Jaynes, 1954) .

In some species of birds, such as the chaffinch, young birds appear to learn several aspects of the species' song through parental example (Thorpe, 1954, 1958), even though the actual expression of the song may not appear until much later, under the influence of androgenic hormone (Poulsen, 1953a). Frisch (1959) found that young redshanks reared from the egg by lapwing foster-parents learned to respond appropriately to the calls of the foster species.

Naturally, the actual physical survival of the young depends on the display of appropriate parental behavior by the parents. Leopold (1944) found a much higher survival ratio among young wild turkeys, whose mothers squat and crouch at the approach of man, than among liberated domestic turkeys in which the mothers scold and noisily herd their young away at the approach of humans. Nalbandov and Card (1945) found that, when young domestic chicks were being cared for by males which had been made "broody" by prolactin injection, the young tended to die of neglect or of attack after the cessation of the injections. This point is so obvious that it requires no further discussion.

2. In Mammals

Although many young mammals at first attempt to suck whatever object they come in contact with after birth (Colhasj 19561, the establishment of a suckling relationship with a particular mother, or even a particular nipple, is accomplished very rapidly (Ewer, 1959). Collias (1956) points out that the repeated making and breaking of contact with the nipple during the first hours of the young goat's life seems to facilitate the learning of both the mother and the kid. Frank (1952) noted that young common voles resist being retrieved by other than their own mothers, apparently basing the discrimination on olfactory stimuli. King (quoted by Scott, 1953) found that guinea pigs removed from their mothers immediately after birth, and then replaced after 3 days can no longer develop


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suckling behavior. Beagle puppies, on the other hand, can be replaced with the mothers as late as 2 to 4 weeks of age, and develop normal suckling. Note that the guinea pig is normally much more precocious in its development than the puppy. Nevertheless, Levy (1934) found that dogs removed from their mothers at birth and returned to them at about 13 days of age had considerable difficulty in establishing suckling.

The licking of newborn young by the mother is, in many species of mammals, an essential condition for the establishment of urination and defecation. Reyniers (1953) found that baby rats isolated at birth die within a few days because they do not urinate, but that the survival of the animals can be assured by stroking the genitals, which reflexly elicits urination; after a few such experiences, urination occurs normally without stimulation by the keeper. Similarly, newborn polecats (EiblEibesfeldt, 1955b) and wood rats (Richardson, 1943) are stimulated to urinate and defecate for the first time by the mother's licking.

In herd-living animals, the experience of the young animal with its mother during very early life apparently plays a vitally important role in enabling it to become integrated with the herd. Scott (1945) took two lambs from their mothers at birth and bottle-fed them for 8 or 9 days, then returned them to the flock. These animals showed little tendency to play with other lambs, and little tendency to stay with the flock while grazing. Similar observations have been made on a foal by Grzimek (1945). Murie (1944) observed that a Dall sheep reared by human beings from a few hours of age later showed no interest in joining nearby sheep. Altmann (1952, 1958) observed that the nursing interactions between baby elks and moose and their mothers form strong conditioned attachments between mother and calf which persists even after weaning. In this connection, Denniston (1956) found that moose calves which lose their mothers at the age of 7 or 8 months have a lower survival rate than do calves which continue to live with their mothers, even though weaning occurs at about 2 months of age. He suggests that protection


by the mother is an important factor in ensuring the calf's access to foraging places.

It is well known that the early experiences of animals, including experiences with the parents, have substantial effects on their behavior in later life. Beach and Jaynes (1954) have reviewed most of the literature on this subject, and we need make only a few comments here. Mice reared in isolation are, when adults, more aggressive toward other mice than are those reared by their mothers (Kahn, 1954). It has now been demonstrated many times that handling of rats during infancy causes them to develop into adults showing less signs of emotionality," and less organic damage under severe stress, than animals reared without such handhng (Weininger, 1956; see also Levine, 1959, I960). Seitz (1954) found that rats reared in small litters and those reared in large litters differed in many significant respects in adulthood. Animals from small litters tended to eat more and to go after food more quickly when hungry than those raised in large litters. The animals raised in large litters hoarded more food in adulthood than those from small litters. Those reared in small litters reacted to new experiences with less "anxiety" and more exploratory behavior in adulthood than those from larger litters. A number of other differences were observed, undoubtedly stemming from the differences in relationships between mother and young, and among the young, which are characteristic of the different litter sizes. In a later paper, Seitz (1959) described the effect on the behavior of cats, when adults, of separating them from their mothers at various ages. Kittens separated from their mothers at 2 weeks of age developed into adults which were more active, more disturbed by novel situations, more aggressive, and slower to learn simple routines, than were kittens which remained with their mothers for 6 or 12 weeks.

Harlow and his students (Harlow and Zimmermann, 1958, 1959; Harlow, 1959) have succeeded in rearing young rhesus monkeys from birth with artificial mothers from which the young could suckle. However, in later (unpublished) observations at the University of Wisconsin, Dr. Harlow


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has found that monkeys so reared failed to develop sexual behavior at the normal time, that they do not become capable of playing with other young monkeys, and that they remain attached to the "mother" for a very much longer time than do normally reared monkeys. Apparently some aspects of the behavior of the real mother toward the infant, which play a crucial role in the development of various aspects of the behavior of the young, are lacking in the artificial "mothers."

From this small sampling of a very large body of research, it is apparent that the behavior of parents toward the young, both in birds and in mammals, plays an important role in permitting and, to various extents in different kinds of animals, in guiding the development of the behavior of the young in their response to hormonal stimulation and in their integration into relationshijis with other members of the species.

V. Scientific Names of Animals Mentioned in Text


Adelie penguin

American coot

American magpie

American robin

Anis

Arctic tern

Auks

Baltimore oriole

Bank swallow

Barn swallow

Blackbird

Blackbirds

Black-capped chickadee

Blackcock

Black-crowned night heron

Black guillemot

Black-headed gull

Blue jay

Boat-tailed grackle

Bobwhite

Boobies

Bower birds

Brewer's blackbird

Bronze mannikin

Brown pelican

Brush turkey

Bullfinch

California gull

Cape weaver

Carolina wren


Pygoscelis adeliae

Fuiica americana

Pica pica

Tardus migratorius

Crotophaginae

Sterna paradisaea

A Icidae

Icterus galbula

Riparia riparia

Hirundo rustica

Turdus merula

Icteridae

Paras atricapillus

Lyruris tetrix

N ycticorax nycticorax

Cepphus grylle Lams ridibundus Cyanocitia cristata Cassidix mexicanus Colinus virginianus Salidae

Ptilonorhynchidae Enphagus cyanocephalus Lonchura cacullata Pelicanus occidenlalis Alectara lathami Pyrrhula pyrrhula Larus californicus H yphanlornis capensis Thryothoras ladovicianus


Cedar waxwing

Chaffinch

Clark nutcracker

Cliff swallow

Common gull

Common tern

Coot

Cormorants

Cowbird

Cranes

Cuckoo

Cuckoos

Curve-billed

thrasher Doves Ducks

Emperor penguin European cuckoo European coot European goshawk European jay European wren Field sparrow Flicker Florida jay Fulmar Geese

Golden pheasant Gould's manakin Graceful warbler Great blue heron Great crested grebe Great reed warbler Great tit Grebes Green heron Gulls Herons Herring gull Honey guides Hornbills House finch House sparrow House wren Hummingbirds Jacana Jacanas Jackdaw Kentish plover King eider Kittiwake Lapwing

Loggerhead shrike Long-billed marsh

wren Mallard Megapodes Mourning dove Murres Night hawk Night heron Noddy (tern) Northern phalarope Ovenbird Pacific eider


Bombycilla cedrorum Fringilla coelebs Nucifraga columbiana Petrochelidon pyrrhonota Larus canus Sterna hirundo Fuiica atra Phalacrocoracidae Molothrus ater Gruidae

Caculus canorus Cucalidae Toxostoma curvirostre

Coluinhidae

Anatidae

Aptenodytes forsteri

Cuculus canorus

Fuiica atra

Accipiter gentilis

Garraias glandarius

Troglodytes troglodytes

Spizella pusilla

Colaptes aaratus

Aphelocoma coerulescens

Fubnaris glacialis

Anserinae

Chrysolophus pictus

Manacus vitellinus

Prinia gracilis

Ardea herodius

Podiceps cristatus

Acrocephalus arundinaceus

Parus major

Podicipedidae

Butorides virescens

Larinae

A rdeidae

Larus argentatus

Indicatoridae

Bucerotidae

Carpodacus mexicanus

Passer domesticus

Troglodytes aedon

Trochilidae

Jacana spinosa

Jacanidae

Corvus monedula

Charadrius alexandrinus

Somateria spectabilis

Rissa tridactyla

Vanellus vanellus

Lanius ladovicianus

Telmatodytes palustris

Anas platyrhynchos Megapodiidae Zenaidura macroura A Icidae

Chordeiles minor Nycticorax nycticorax A nous stolidus Lobipes lobatus Seiaras aurocapilus Somateria mollissima


1360


HORMONAL REGULATION OF BEHAVIOR


Partridges Pelicans Penguins Petrels Phalaropes Pheasants Pied-billed grebe Pigeons Plovers Purple martin Rails Raven

Red-backed shrike Red-billed weaver Redshank

Red-winged blackbird Ring dove Ringed plover Ring-necked pheasant Robin Rook Ruff

Ruffed grouse Sandpipers Satin bower bird

Serin

Shearwaters

Shell parakeet

Short-tailed shearwater

Shrikes

Smooth-billed ani

Snow bunting

Sociable weaverbird

Sooty tern

Song sparrow

Starling

Storks

Storm petrel

Swift

Swifts

Terns

Tinamous

Tricolored redwinged blackbird

Turkey

Turnstone

Valley quail

Waders

Weaver finches

Western gull

White-crowned sparrow

White-tailed kite

Woodpeckers

Wrens

Wryneck

Yellow-eyed penguin

Yellow-headed blackbird

Zebra finch


Phasianidae Prlininidae Sphrnisnilar Hu'liolxiljilac Phalaropodidae Phasianidae Podili/inhiis podiceps Cohnnhnlnr Cfuirni/rlnhie Progne subis Rallidae Corvus cor ax Lanius collurio Quelea quelea Tringa tolanus Agelaius phoeniceus

Streptopelia risoria Charadrius hiaticula Phasianus colchicus

Erilhacus rubecula Connis frugilegus Philomachtis pugnax Bonasa umbellus Scolopacidae

P/ilnii(irlii//ichus violaceus Sen II IIS (■(iiKiria Pioctlluriidae Melopsittacus undulatus Puffinus tenuirostris

Laniidae Crotophaya ani Plectrophenax nivalis Philetairus socius Sterna fuscata Melospiza melodia Sturnus vulgaris Ciconiidae

Hydrobates pelagicus Apus apus Apodidae Sterninae Tinamidae Agelaius tricolor

Meleagris gallopavo

Arenaria interpres

Lophortyx californica

Scolopacidae

Ploceidae

Larus occidentalis

Zonotrichia leucophrys

Elanus leucurus Picidae Troglodytidae Jynx torquilla Megadyptes antipodes Xanthocephalus xantho cephalus Poephila guttata


American beaver

American bison

American buffalo

American elk

American red squirrel

Antelopes

Asiatic scjuirrel

Bats

Bicolored white toothed shrew

Bottle-nosed dolphin

California sea lion

Camels

Carnivores

Central American opossum

Chimpanzee

Common vole

Cotton rat

Dall sheep

Deer mouse

Dusky-footed woodrat

Elephant

Elephant seal

European hare

European water vole

European j^ellownecked mouse

Field mouse

Field vole

Galapagos sea lion

Golden hamster

Gorilla

Guanaco

Hippopotamus

Kangaroos

Llamas

Meadow mouse

Moose

Northern pigmy mouse

Opossum

Orang-utang

Polecat

Red deer

Red kangaroo

Rhesus monkey

Rice rat

Rodents

Seals

Sea lions

Shrew

Ungulates

Wood-mouse

Wood-rat


Castor canadensis Bison bison Bison bison Cervus canadensis Sciunis hudsonicus

Borirlar

Cdlliisri urns leucomus Vcxpi rlilioiiidae Crocidura leucodon

Tursiops truncatus Zalophus californianus Camelidae Carnivora Marmosa cinerea

Pan troglodytes Microtus arvalis Sigmodon hispidus Ovis dalli

Peromyscus maniculatus Neotoma fuscipes

Loxodonta africana Mirounga angustirostris

Lepiis I'liiDpac.iis Arrirnhi li rrrslns Apoilniiiis Jlnrirollis

Microtus arvalis

Mivinliis aiiirstis

Zalophus irnllvlinrki

Mcsiirriniiis aural us

Gorilla gorilla

Lama yuanicoe

Hi ppapnlaiii us amphibius

Marropoiliilar.

Cuiitclidar

Microtus pennsylvanicus

Alces americana

Baiomys taylori

Didelphus virginiana Pongo pygmaeus Mustela putorius Cerrii.^ chiphus Miicriipiis riifus Macacu mulatta Oryzomys palustris Rodentia Phocidae Otariidae

Blarirui brevicauda Ungulata

Peromyscus leucopus Neotoma albigula


African lion Alaska fur seal


B. MAMMALS

Felis leo

Callorhinus alascanus


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1363


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Acknowledgments. Work from the author's laboratory, described in this chapter, was accomplished with the support of research grants from the National Science Foundation (G2546), the National Institutes of Health of the United States Public Health Service (M2271 and C3617), the Rockefeller Foundation, and the Rutgers University Research Council (261), to all of whom grateful acknowledgment is made.

Dr. I. Eibl-Eibesfeldt, Dr. R. A. Hinde, and Dr. J. S. Rosenblatt each read various parts of the chapter, and made many helpful suggestions.

Miss June Thomas typed the manuscript. Miss Thomas and Miss Nina Lehrman assisted with the difficult task of proof-reading.






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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


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


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