ONTOGENY OF EMBRYONIC BEHAVIOR I N AVES

111. 'I'llli: S'I'ItUC'r~Jl~ AT, AND Ji:NVTRONR4ENTAJl FACTORS IN IdMI1ItYONLC: LlldlLAVLOlZ,

ZING YANG ICUO
Nalional Central University, Nanking, China

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INTRODUCTION

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While it nppen.rs to l)e n hcnlt,hy nnd promising sign that a few biologists and psychologists have recently manifested some interest in the study of embryonic and fetal behavior in various vertebrates, it is rather disappointing that these investigators have almost entirely neglected the anatomical and environmental aspects in their studies of develanmental behavior. The work of Coghill (1024, 1926, 1929 and 1930) on the behavior of the larva of the Amblystoma has no reference t o its environment whatever. Those who have worked on the behavior of mammalian fetus (Angulo (1929 and 1930), Avery (1928), Brown (1914 and 1915)) Langworthy (1929)) Minkowski (1921, 1922, 1923, 1924 and f925), Pankrats (1930)) Swenson (1925, 1928, 1928a and 1929), and Windle (1930)) removed the fetus from the uterus and g:tthvl-c(I frngmcr~f.nry inforrnat,ion conccrning its body movcments (which movements, by the ~vay,are rather pathological. For detailed objections to their methods of study see Kuo (C)) without noting the effcct on behavior of the removal of the fetus from its normal fetal environment after the experimental delivery. That the nature of behavior can be understood only in terms of its causal relation with the environment should be obvious to every one. And yet these investigators have not felt the need of preserving and understanding normal embryonic and fetal environment in their behavior studies. And it is partly due either t o negligence or to ignorance of environmental factors that we, of late, so often find in current literature such a meaningless expres245

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sion as "pontaneous activities" as if animal activities could appear without cause or without preceding stimulation. We shall take up this question of spontaneous activities again a t the end of this paper. I n the adult animal changes in gross anatomyare not so apparent and profound, so that t,heir effects on behavior may be somct,imes ~~cgligible. 011 tl~c ot,I~(:r II:I,II(~, i11 LIIC y o t ~ r :t~~ , r ~ i ~ t l : l~:s11(:ci:~lly I, during the embryonic and fetal stages, metamorphosis is not complete, the general body form, the structure of different organs, and the relative size and proportion of different body parts are changed from time to time as a result of development and growth. Such changes have profound effects on the modes of behavior. Unfortunntely, this nspcct of the problem of the tlevclopmcnt of behavior has been ~~cglcctcd al tllough considerable attcrl tior1 has been recently paid by several investigators to the possible correlation between the development of the nervous system and the development of behavior. We shall in a later section discuss the relative importance in determining behavior between gross anntomicd changes of the body as a whole and the development of thc nervous system. From our studies on the origin and development of embryonic behavior in birds we have gathered sufficient evidences to demondetermined@ strate that indevelopment behavior is ~rimarily by changes in gross cuahmy, b - b y the nature of the environment, and @)by the past history of behavior of the organism. The effect of the past history of behavior on new bchavior will be dealt with elsewhere (see the fourth article of this series). In the following pages we shall present evidence concerning the effect of structural and cnvironrncntal factors on embryonic behavior in birds. While our studies have included both pigeon and duck embryos, besides chick embryos, the present report will be confined to the behavior of the Iatter alone. I t must be noted, ho~vcvcr, that there is practically no tlifI'crcncc bctwecn the pigeon or duck embryo and the chick embryo with regard to the structural and environmental factors in determining behavior. In view of the fact that in our investigations on the behavior of the bird embryo we have used several thousand eggs, it would be

impossible for us to report in this paper statistical details or individual cases; we have to be content with a somewhat summarized form of presentation. The methods of studying embryonic behavior in birds have been fully described in the first article of this series. To avoid unnecessnry rcpctition the render is rcferrcd to that article (Kuo, T).
STRUCTURAL EFFECTS O N EMBRYONIC BEIIAVIOR

H e a d nzovements a s e.flected by structural cilanges. We have reported elsewhere (Kuo, I) that head movements are the earliest physiological responses found in the chick embryo. They generally appear by the fourth day of incubation. But in many cases, head niovcmcnt,s nrc o1)servcd as early ns the third day of incuhation. I n the three- or four-day embryo head movements consist of lifting upward, and bending toward the breast. But from the fourth or fifth day on head lifting and head bending gradually disappear and a new mode of head movement takes their place, namely, the turning of the head to the sides. On the fourth day, head lifting is still the dominant response of the head although turning to the sides is also present in some embryos (table 1). I n the five-day embryo, the frequency and relative magnitude and the number of birds are decreased for head lifting but increased for side turning. In fact, the head movement of the five-day embryo has become semicircular, which motion is the direct result from the combination of the uplifting and side turning movements of thc head. Between the sixth and ninth days of incubation, head lifting disappears entirely (except 20 cases of six-day embryos, table 1) while side turning of the head has become the major response of the head although the bending of the head towards the breast is still observed occasionally. The question is immediately raised: what causes the transformation of the head movement from uplifting to side turning? The key to this question lies in the anatomical changes during these sta.ges of development. In the three- or four-day embryo, the head is not heavy and there is no neck. From the fifth day on the weight of the head increases enormously. Before the tenth day it is heavier than the weight of the body, and is more than 50 per

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cent of the total weight of t.he embryo (48.6 per cent of total weight hy thc rtirltli tlny whcrc:~sit is only 18.3 per ccnt a t t,hc t h e of hntclii~rg,(tnblc 2). 'I'hc riccl<, too, is Icngtlicncd considct.nbly after the fifth day, but its diameter is relatively s~nall (table 3), and its weight relatively light (table 2). With such a large and hcnvy hcnd and wit11 such n. s~nnll and light but 1o11g neck, it is, of cout-sr, cstrclrlc>lyclillicr~lt, if ~ ~i~~~l)ossil)lc>, o t T o t 011c(.1111)ryo to
TADLE 1 Averaged Jrequency and magnilude of head lifting and head ltsrning (lo sides) in 414 chick embryos from the third day oJ incubation lo hatching

of two kinds of movements: (1) the bending and extension of the trunk on the long axis of the body, and (2) the twisting of the body to the sides (in twisting the anterior region is bent to the opposite direction in which the posterior region is bent) (Kuo, I). Both kinds of trunk movement begin to diminish in frequency, magnitude aad in the number of cases by the tenth day and disnppcnr ant,ircly by t,hc t,wclfth dny (table 4). With thc disnppearance of these two types of trunk movement, the jerking and
TABLE 2 Averaged weights of head, neck and body of chick embryos
-.
I EMRRYOR T

1 1
.... -. WEICIRT
gram8

Per cont I'nr cotit

Wcinl~t

W e i a l ~ t Por cont

nODY

Weight

,-

'

raise its head upon the neck, and so the head movement is transfornled illto lateral tur~iing. (It nus st be noted t11:~t duri~~ iticug bation the weight of the head in proportio~i to the total w i g h t of the embryo is decreased day after day while that both for the neck and for tho body is increased (table 2).) Eflects of slructzcral changes on trunlc ntove??zenls. Trunk movement appears by the fourth day of incubation. I t consists

wriggling movements of the body are increased in frequency and become the major or almost the only movements of trunk through the rest of the incubation period. I t must be pointed out that although jerking and wriggling movements are observed even as early as the fifth or sixth day of incubakion, they are rather minor and relatively infrequent responses of the trunk until after about the tenth day. The disappearance of the bending and extension and of the
COIIPARATIVE PBYCIIOI.OCiY, VOL. XIIT. N O .

ZING YANG KUO

TABLE 3 Averaged tenglh of different parts of the body of the chick embryo

ONTOGENY OF EMBRYONIC BEHAVIOR IN AVES

251

mm.

16.4 23.1 28.2 34.9 39.8 46.2 53.5 59.9 68..5 75.2 80.7 88.8 98.2 105.5 113.7 116.0 118.5

TABLE 4
T R U N K MOVEMENTS A O E OP E M D R Y O B

Frequency per minute

Estimated magnitude
mm.

Number of embryw

4 5 6 7 8 9 10 11 12 13 14

4.2

6.9
8.7 12.2 12.8 11.2 6.8 2.2

1.9 3.1 3.3 3.2 3.8 3.6 3.0 2.2

24 1 440 446 446 446 446 221 124

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lateral twisting of the trunk is a necessary result of the changes both in structure and in the embryonic environment. I n the first half of incubation the body is relatively light in weight and small

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in size so that it floats, as i t were, on the top of the yolk sac. There is thus sufficient space in the egg for extensive trunk movements. But after the tenth day the embryo grows rapidly both in size and in weight, its head is bent on the breast permanently. After the eleventh day, it comes to lie with its dorsal surface in contact with the egg shell, the ventral wall and left side (and a srnall part o f the right Ride) of the body being covered b y the yolk sac (see Kuo, 11). I n such a position it is obviously impossible for any extensive movement of the body and the only possible mode of motion for the trunk is jerking, and wriggling (wriggling differs from jerking only in the degree of violence). &fled of strucLural changes on limb movements. Active movemcrlts of l)ot,h nntcrior nrid posterior limbs are observed on the forit.I,1i thy of iricuI):~t,ion. As tlit: Iitril~stire ~ h o r and t rudirncntary, they a t first move in a vibrating fashion. But in the fiveor six-day embryo, the limbs are longer so that they can move cephalad and cnudnd. Adducting and abducting movements are also seen during these days. By the eighth or ninth day, the movement of the forelimbs takes a new form. Now they are much longer than the nntcrior limbs of the six- or seven-day embryo; the main divisions are well defined, and they appear decidedly wing-like. As a result of such structural changes, the former modes of motion of the anterior limbs on the sixth and seventh day are now transformed into flapping and slashing movements. In these later movements, the wings can be extended f~illy, iicndward 3 r d tsilw:~rclns well as laterally. By the oighth day separate niovcnicnts of the arms, hand, arid digits, though not independent of the movements of other parts of the body, are also seen. Furthernlore, in the five- or six-day embryo, the forelimbs are always straight both a t rest and in motion. But by the eighth or ninth day, due to lengtherling of the limbs and the appearance to their divisions, their movements consist chiefly of extensions and flexions. After the ninth day, the forelimbs are further lengthened so that they are held tightly against the body walls by the environmental conditions to be described below. Under such conditions

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the wings can not be extended laterally and so the flapping movements practically disappear. Now the wings can only be extended headward, upward, tailward or toward the breast. When columes 8 and 9, table 3, are examined the relation between the lengthening of both fore- and hindlimbs and the changes in the mode of limb movements should be very obvious. As to the rnovclncnts of t,lic iliritllilubs, tltc cfTccts of sLr.ucturn1 changes are very much the same. In the four- to six-day embryo the modes of motion of thc hindlirnbs are similar to those of the forelirnbs. At first thc posterior limb buds move also in a vibrating fashion. By the fifth and sixth days of incubation, inward and outward, and headward and tailward movements arc observed, the limbs always being straight. Aftcr the sixth day, the main divisions of the legs begin to become well defined. The legs are much lengthened. As a result, the legs are no longer in a straight condition; flexion and extension take the place of the headward and tailward motions. The inward and outward movements also disappear for the amnion interferes with such movements after the legs are lengthened. With the appearance of the divisions of the legs separate movements of the toes and shanks (but not independent of the movements of other parts of legs) are also recorded. On the eighth day, the legs are straightened in extension. But from the ninth day on, the legs are further lengthened and begin to be folded on the breast so that they can not be fully extended dtlc to thc obstruction of t,llc l~tritlio~i lttld yolk s:tc or tllc cgg ~ltcll as the case may be.
ENVIRONMENTAL EFFECTS ON EMBRYONIC BEHAVIOR

The egect of yollc sac o n behavior a. The eflects of the movement of the yolk sac, and of the contraction o j the amnion. The yolk sac movement nnd amnion contraction have been described in the first report of the series (Kuo, I).

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Meaning of embryonic environment. The term "embryonic environment" is here used to refer to those extra-embryonic factors confined in the egg shell which exert influence on the behavior of the bird embryo. They include the extra-embryonic membranes, the shell rnembranks, the egg - - shell, the yolk, the albumen, and the fluids in the extra-embryonic cavities. 'I'he movements of certain parts of the body which serve as stimuli for movements of certain other body parts are also considered in this report as cnviron~nr.ntal fnctors in bchnvior.

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AGE OF EMBRYOS (IN DAYS)

Here we wish to merely present some data concerning the relation between activities and the movements of the yolk sac and amnion. Table 5 gives the average frequency per minute and magnitude of the swinging movements and movements of the yolk sac and of

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the amnion for 328 chick embryos from the fourth to the fourteenth days of incubation. It will be clearly seen that the frequency and magnitude for the passive swinging of thc embryo are in correspondence with those for yolk sac movements and
TABLE 5
Conlraclio7hq of n ~ ~ t t r i o yolk n , ant: n~ovnntc~rln nnrl pnnnitrc .~ini?rgi~rgn r , j thr: chick embruo f r o m the fourth dav to the Jourleenth dav o f inclibalion

the amnion and of the yolk sac. Table 6 gives the average frequency of active body movements per minute for 328 embryos fro~n the third day of incubation to hatching. Attention is called to the fact that in the chick embryo the body generally moves as a

OF EMBRYOE

*on

P ~ - - - - . -

I 1 1
Fre-

BWlNOINO

1
Number

A M N I O N C O N T R A C T I O N Frequency

YOLK S A C M O V E Y P I N T

Eati-

quency

meted

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1 x1
Eatimated

Number

Frcquency

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Number of

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TABLE 6
Averaged frequency of loin2 body activities per minute of 598 chick embryos jrom the third dnij o f incnbation lo hnlchinn
AOQ O F B M A R T O A

a
Frequency

lo

11

12

13

14

15

16 17

is

19

20

of activities ....... 1 . 3 4 . 3 6 . 2 8 . 8 1 2 . 1 1 2 . 4 1 1 . 9 6 . 1 2 . 3 3 . 1 2 . 2 3 . 3 3 . 3 2 . 9 3 . 1 2 . 8 2 . 9 3 . 5

6 7 e s t o t , 1213 lslsist7,crmso AGE O F EMBRYOS (IN DAYS)

amnion contraction. This correlatiorl appears more striking in figure 1. Not only is thepamive swing effected by the yolk sac movements and amnion contraction, but also the active movemerits of the embryo are increased or decreased according to the movements of

whole (Kuo, V). The movements recorded in table 6 are also movements of such a nature. It will be noted that the number of activities is increased between the fifth and the tenth days of incubation, especially between the seventh and ninth days, that is, during the period of forceful amnion contractions and yolk

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f we plot curves for the frequency of the sac movements. I amnion contraction and yolk sac movements and for the frequency of activity during incubation, again we find the two curves running almost parallel (fig. 2). I n observation we find that the movements of the amnion and of the yolk sac not only start the passive swinging of the embryo, but also stimulate active movements of the wliole body. Indeed, during the pcriotl of active amnion contraction (and yolk sac movements) body movements of amnion are almost ceaseless. As thc frcqucncy and mag~iitudc contraction begin to decline, the embryo becomes less active. b. Leg movenzents. We have stated that from about the ninth day on, due to the irlcrcasc in length, the legs begin to bc folded ciow~i on the brcnsl, 1)y tIlo :urit~iori. Ilrrf, :~fI,t:rral)ollI,I,hc t~lcvcrrt,h day, the yolk sac is ge~ierslly moved over the ventral side of the embryo (Kuo, 11) so that the legs are directly under the yolk sac. Under these conditions the extent and frequency of leg movements are reduced; the more the yolk sac is pushed over them, the more difficult i t is for the legs to be extended. Under the yolk sac, the legs, in their upward and tailward cxtensiotl have to push up the amnion and the yolk sac. Sometimes the latter may be pushed up from 4 to 6 mm. But the weight of the yolk and yolk sac presses the legs down to fold on the breast again. I n the second article of this series we have pointed out that during the latter half of incubation as the legs are too strong to be kept in proper configuration by the amnion alone, the yolk sac is chiefly responsible for pressing down the legs on the brcast. Thus in those abnormal cases in which the yolk sac fails to come over the ventral side, the legs may be extended as far as the shell, or fully extended and twisted in any direction. I n such cascs, the legs generally acquire an abnormal configuration. Between the eleventh and the fourteenth days, after the legs are foldtd under the yolk sac, a new mode of leg movements appears which is much more extensive and frequent than the upward extension. This is the forward thrusting of the legs. I n the forward thrusting movement, the legs are extended cephalxd. They may be extended over tlie beak, the head, or toward the neck at any level of the cervical vertebrae (sometimes both legs are

thrusted to one side of the neck) or in front of the lower jaw or the ventral aspect of the neck. I n such movements the legs may be extended as far a s 10 or 12 mm. The forward thrusting movement of the legs is most frequent and extensive by the twelfth day of incubation. But both extent and frequency are reduced almost by half by the end of the thirteenth day. They are further reduccd by the fourteenth day. By the thirteenth or fourtcerlth day the legs in thrusting can not be extended much below the eye level. Aftser the embryo turns so as to lie lengthwise of the egg, the greater part of the yolk sac is pulled over on the legs which are folded on the breast. The yolk by the eighteenth day of incubation still weighs several grams. With such a heavy yolk pressing down on t,hc I ( : ~ R , it is nnt11rn.l thnt they nrc forccd to rcmnin in n folded position throughout the rest of incubation. I n this position, not only the upward extension but also the forward thrusting of the legs are reduced to a minimum. I n most cases, after the turning of the body, the legs can not be observed. But in a few chicks, the legs are seen to perform only very slight movements together with the scratching motion of the toes. In the second article of this series we have reported the fact that if the yolk sac does not come over to cover the ventral side of the body and the legs between the twelfth and fourteenth days, the body of the embryo can not be turned to lie lengthwise of the egg, as the turning of the body very much depends upon the movement of the legs to push the yolk sac upward so that the body under the yolk snc can slip townrd the small end. I t need not be mentioned that if the legs a t this stage are still under the shell instead of being under the yolk sac, their upward extension is impeded by the shell. I n the second article we also reported that in the attempt on the part of the hatching chick to gain egress from the shell, the movemerits of the legs played an important rBle, but that such movements are not effective until after the yolk sac covering the legs is drawn into the body cavity. I n the fifth article we shall describe how the progressive movements of the legs are acquired after the yolk sac has been pushed to cover the legs.

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c. Wing movements. We have shown that as a result of lengthening of the wings and of environmental conditions, flapping movements disappcar, and a new mode of movement takes its place (extension headward or toward the breast). Here both the amnion and yolk sac play their part. In the later period of incubation, the wings are held tightly against the body walls by by the amnion. Aftcr tjllc tcntll dny thc body of the cmbryo is generally so fixated that the yolk sac presses from the left, the chorio-allantois and the inrier shell membranes next to the air cell press from the right. By about the fourteenth day a small portion of the yolk sac is pushed over the ventral wall to cover a small part of the right side of the body, including a large portion of the right wing. The flsppilig movements of the wings are thus interfered with, and the wings now can only be drawn up and down lightly against the body walls. When the wing is drawn up it may be extended cephalad or toward the breast. This mode of wing movement remains throughout the rest of incubation. d. Head movements. We have already shown that due to anatomical changes, head lifting is transformed into side turning between the fifth and tenth days of incubation. Now after the tenth day the proportional size and weight of the head is not so large and heavy as before and it would seem possible to reinstate the head lifting movement. But this is not the case owing to the fact that between the tenth and twelfth days, the body whose anterior and posterior ends are bent toward the middle region sinks into the yolk sac so that the dorsal side of the neck and of the body is in direct contact with the yolk sac while the head which is bent on the breast is very close to the shell. In this position the raising up of the head upon tlic neck is diiiicult although lifting of the beak has been frequently observed. After the twelfth day a portion of the yolk sac has come over, as has been repeatedly stated, to cover the ventral wnll as well ns the beak and the head, while the dorsal side of the neck is now in direct contact with the shell. Here again, head lifting is practically impossible. This condition persists until the yolk sac in the large end of the egg has been withdrawn which generally takes place between the eighteenth and nineteenth days. But even

after the withdrawal of the yolk sac from the large end, head lifting is still extremely difficult as the neck has now acquired a double bend. However, slight lifting and forward thrusting of the beak are frequently observed during this stage, and these movements are responsible for the piercing of the membranes (Kuo, XI). In a word, structural, positionnl and environmental conditions have caused a permanent disa.ppearance of the head lifting movement after about the fifth day of incubation.
TABLE 7 Average frequency of right and left turning of the head i n thirty minutes i n 344 chick embryos
AOE OF EMBRYO RIOnT TURNING LEFT TURNINO

5
6

30 100 170
281

23 71 60
61

7
8 9 10 11 12

350
316 142 137 84 86

40

ao
12 12 4 6

13
14 15 16 17 18 19

93
82 87 1.5 10

3
6 3

0
0

21

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The yolk sac Ilas also a, great effect on the laternl turning of the head. As a result of torsion, the embryo comes to lie with its left side on the yolk. After the fourth da.y of incubation the embryo sinks down into the yolk sac so that in normal cases it lie8 with its back on the yolk sac while the left side of the body and of the head is in direct contact with the yolk sac. In this position the turning of t,he head becomes almost unilateral, that is, the head tends to turn away from the yolk sac, in other words, it tends to turn to the right rather than to the left. This tendency is especially

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./

strong after the stage of fixation of position (Kuo, 11). Table 7 shows the relative frequency of turning of the head to the left and to the right between the fourth and nineteenth days of incubation. It will be seen that during practically every day of incnhatian_ right turning is by far more frequent than left It must be noted nlso that in prncticallv every rasp g s i r h ,t a greater magnitude tllnn lcft turning. It is very probable that such an unilateral turning of the head helps it to acquire the position, namely, the bending of the head toward the right, which position is a prerequisite to hatching (Kuo, 11). In most cases of the bird embryo which we have observed, bending of the head to the right has become almost a fixed posture in the lntcr stnge of incubntion. e. Beak moventent. In the first report we have shown that the beak can open and close by the seventh day. Now after the yolk sac has been pushed over to cover the ventral wall and the beak which is bent on the breast, beak opening is reduced both in frequency and magnitude. In this position, the head sometimes turns out from the yolk sac, making it and the beak free from the yolk sac. The beak is then often observed to open widely. But when it is turned in under the yolk sac again, bill opening is also diminished. However, when the beak is under the yolk sac, it acquires a new mode of motion, namely, the clapping of the bill. I n clapping the beak is only very slightly opened. It claps frequently; the embryo is often observed to clap its beak every few seconds, nnd mnkes severnl clnppings consecutively. j. Trunk movements. The effects on trunk movements of the yolk sac has already been pointed out. When the body grows in size and weight, it sinks down into the yolk sac so as to lie with its back and left side in contact with the yolk sac. The extension and lateral twisting of the body is thus impeded by the yolk sac, and so. the trunk movements are transformed into jerking and wriggling, as has been previously stated. Before the eleventh day wriggling is possible only when the embryo lies with its dorsal side on the yolk sac. In younger embryos, if the body lies under the yolk and the yolk sac, it is so pressed by the latter that bodily movements are reduced to a

minimum. Not only the movements of the head and extremities and extension and lateral twisting of the trunk are impossible, but also jerking and wriggling movements are rarely observed. On the other hand, wriggling after the eleventh day and throughout the rest of incubation takes place only when the ventral wall is under the yolk sac. We have described the processes of turning of the body to lie lengthwise of the egg and of the protrusion of the neck into the air cell (Kuo, 11). These are accomplished by wriggling movements which are always performed under the yolk sac. Thus, we have found that if the yolk sac does not come over to properly cover the ventral wall and the legs after the fourteenth day (that is, if the yolk sac is still under the back, or one or both lcgg are not covered by the yolk sac, or the whole yolk sac is behind the left of the embryo (Kuo, 11)) not only does the body fail to turn to lie parallel to the long axis of the egg, but also wriggling movements are greatly reduced both in frequency and strength. g. Turning to the body. I n the second article we reported that when the embryo began .to turn to lie lengthwise of the egg, the turning movement was always caudal, that is, the tail end was shifted leftward toward the small end of the egg. This was found to be due to the fact that a t this stage, the neck of the embryo was between the yolk sac (left) and the chorio-allantoise and inner shell membranes next to the air cell so that the neck was held in place during the turning of the body.
l'he effectof Ihe membranes a. Amnion. We have already shown that amnion contraction serves as a stimulus for active bodily movements. The period of frequent and powerful amnion contraction is also the period of frequent and violent body movements. When one observes for several minutes a six- to nine-day chick embryo, one can not fail to see that whenever the amnion contracts or the yolk sac moves, the embryo is set in both passive swinging and active massive movement. During these days one frequently observes that when the amnion contraction ceases, the embryo also rests quietly. (Body movement may also in turn stimulate amnion contractions.)

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b. The chorio-allantois and the inner shell membrane. As far as behavior is concerned, only that part of the chorio-allantois and inner shell membrane which separates the air-chamber from the rest of egg is important. We have already referred to the fact that during the turning of the body to lie lengthwise of the egg, this part of the mexn1)rnne keeps the neck from moving. Thus, ns rcl)orlcd in tlic scco~ldru.Liclc, tlr~rit~g Ol~is ~Lrigo,if t,llc ~nclribranes are too loose or are punctured to allow air to run in, the body may immediately fall to the left or turn so as to acquire an abnormal position. The protrusion of the neck forward and downward into the air-chamber under the membranes (Kuo, 11) depends on the wriggling movcment,~. Now, if during this stage, thc membranes are lightly applied on the left side of the head and neck, wriggling as well as movements of the head, beak and the right wing are reduced to a minimum and the embryo generally fails to pass this stage. Under this condition, lifting and forward thrusting of the beak are rarely observed. Beak opening is also infrequent, and the only relatively frequent motions observed are eyelid movements and bill clappings. On the other hand, if, before and after the protrusion of neck, the membranes are loose, all above mentioned movements are increased.

But if the head is too close to the shell, or still bent on the breast, or tilted to the left or right, or is in the small end of the egg, any movement of the head and the beak (except bill clapping) becomes impossible, as there is no room for movements. After the protrusion of the neck, if the head is tucked under the right wing, bill movements are increased both in frequency and nrtiplit,udc. OLIicrwi~e, tlicy nrc diminished (Kuo, 11). b. Positions of the wings and legs. The effect on behavior of the positions of the wings and legs has been discussed in previous sections. It remains to be stated that if, in the later period of incubation, the legs are not folded on the breast under the yolk sac, the normal leg movements previously described are not observed and coordi~~atcd walking movements (ICuo, V) can not be acquired. The efect of the beating of the heart and of the scratching of the toes on head movements a. The beati . the early stage of development r e m o the thorax (generally about the eighth day of incubation) its movement often serves as a stirnula, tion for head movements. In the first article of this series we have already described the passive vibrating movements of the head and the body which are produced by the beating of the heart.\ I n the four- to sevendav embrvo the head is bent down close to 1 the heart so that cardiac movements often touch the head. Thej hcnd i~ then stimul:~ted,nnd motion i~ observed, that i ~the , head turns away from the source of stimulation, namely, the heart. The turning of the head away from the heart results in the lifting of the head, or turning to the side, as the cnse may be. Such head movements are almost always accompanied by massive movements of the body. In fact, from continuous observations on many hundreds of chick embryos between fourth and nineth days of incubation we have come to the conclusion that the fact that the activity curve of the embryo reaches its highest peak in this stage is to be explained by the fact that in this stnge the contraction of the amnion, the movement of yolk sac and the passive swinging of the embryo as well as the beating of the heartp

The eflect of position on behavior a. Position of the h,ead. In the later period of incubation, the hcn.d is gcncrally bent on tlic brcnst, t11c forchcnd bcirig under thc turns to the side. The yolk sac. I n this position the head o~lly beak may be able to lift up a little but the head can not raise upon the neck. After the yolk sac has been drawn into the body cavity, raising of the head is also extremely difficult as its dorsal side is rather close to the shell. After the protrusion of the neck the double bending of the neck is rather pronounced (that is, the neck is bent on the breast, whiIe the head turns away from it so that the right face faces the membranes (see Kuo, 11)). In this position, the head can neither lift up nor turn to side, and no other movements than upward lifting, opening and slight forward thrusting of the beak are observed.

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all serve as external stimuli for active movements of the embryo. I n the sixth article we shall present evidences to show that the rate of heart beat is also highest when the embryo is most active. On the other hand, in the later half of incubation, the heart is enclosed in the thorax, amnion contraction, yolk sac movement nnd pnssive swinging are either greatly reduced in frequency and in xrlng~~itude or cclisc nltogctlicr, r~ridthe body grcatly ilicl.cnscs in size so that extensive movements are not permitted by the external cnvironmcnt; nnd so the ernbryo becomes rather quiet; it may be motionless for many minutes, and when it moves occasionally, its movements are not extensive. b. The moventent of the toes. By about the fourteenth day the body of the embryo which origirlally is a t right angles to thc long axis of the egg, turns to lie lengthwise of the egg. As a result, the head is bent away from the breast with the right face turned forward toward the membranes next to the air cell (for details see Kuo, 11). In this position, the toes of both legs are just behind the left side of the head. Now it often happens that when the toes move, they scratch the left side of the head. This stimulates the head which turns out toward the membranes. (In this stage the head and the beak is generally under the yolk sac so that in turning out toward the membranes, the head is temporarily removed from the yolk sac.) This is another reason why the head, after the turning of the body, makes so few turnings to the left (tabIe 7).
m

5. The contraction of the amnion and the movement of the yolk sac all serve to stimulate m0vement.s of the bird embryo so that the period of greatest amnion contraction is also the period of greatest behavioral activity in the embryo. 6. The mode of leg movements is also determined by its positional rclation with the yolk sac. 7. Movcrncnt~ of othcr parts of tlic body nrc nlso partly cffectcd by their positional relation with the yolk sac. 8. The movements of the toes and the contraction of the heart, the positions of the hcnd, neck and the legs and the extra-embryonic membranes all play their part in determining embryonic behavior.
DISCUSSION

SUMMARY

& I n this paper data are presented to show that structural and environmental changes are always accompanied by behavioral changes in the embryonic chick. 3. As a result of the enormous increase in the size of the head, head lifting is transformed into side turning. 3. Bending and extension and lateral twisting of the trunk disappear and jerking and wriggling come to take their place when the size of the embryo is increased. 4. The modes of movements of both the anterior and posterior limbs are partly determined by the length and sha.pe of the limbs n t cncli stngc?of dcvcloprnc~~t..

Enough facts have been presented to demonstrate that changes in gross anatomy and environment are important factors in determining embryonic behavior in birds. We are firmly convinced that in the study of the development of behavior these two factors ,as well as the effect of past behavior and the development of the physiology of different organs must be taken into consideration. It is regrettable that recent investigators on embryonic and fetal behavior in amphibians and mammals do not go beyond the mere noting of the appearance of certain movements. They make no attempt whatever to find out the causal factors for such movements. The historical, anatomical, physiological and environmental factors are all ignored, and the appearance of movements is described as "spontaneous a~tivities."~ One has only to observe a chick embryo for several days to be reasonably convinced that external (i.e., extra-embryonic) stimuli play a very important part in determining embryonic behavior and that embryonic activities are rarely spontaneous. I n fact, in the caye 01 the avian embryo, food and oxygen supply is relatively
Some writers, e.g. (Tracy (X926)), have attached a new meaning to the term are s ostensibly caused by "spontaneous," that is to say, when certain m o ~ e m e n t ~ internal stimuli within the organism, they are referred t o as "spontaneous activities." But even so, i t can not escape the criticism t h a t "spontaneous activity" is nothinu more t h n n n nnrnc for our ignorance of the t-tctual physiological factors
u11tlcrlyi11~ I)cl~nvior.

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constant and movements activated by lack of metabolic materials are rather rare exceptions. The neglect of environmental factors in embryonic life has led many writers to believe that prenatal movements are innate or hereditary. That this is not the case has been clearly demonstrated by our observations on the behavior of the bird cmbryo. We shnll discuss rnorc fully thc qucstion of licrcdity in rcl : L t'1011 to embryonic behavior in the fourth article of this series and especially in a book cntitlcd "The Mccha.nics of Embryonic Behavior in Birds." Suffice it to point out here that practically every prenatal movement is shaped and determined in part, a t least, by the nature of the embryonic environment. The importance of analysis of environmental factors in behavior study can not be overstressed. Every movement is caused by some environmental stimulation intra-organic or extra-organic. There is no such a thing as "spontaneous actiwily," any more than is there such a thing as "spontaneous generation." To understand the nature of the environlnent and hiw it shapes and determincs behavior is the key to the understanding of the causal relation of animal activities. Too many behavior studies, especially those dealing with prenatal behavior or behavior of the newborn, have been carried out with environmental factors either entirely neglected or treated only in a casual manner. The importance of nnatomica.1 and physiological factors in embryonic bcllravior I I : ~ ~dso 1)c:oll ovcrlooltcct. 'I'll(: trr~.tlitioncal view that the development of the nervous system alone is correlated with the devclopmcnt of bchavior is partly responsible for such a neglect. Recent studies by Coghill and others otl tIic correlation between the development of the nervous system and development of behavior chiefly in amblystoma, and cats and rats have been carried out without reference whatever to the changes in the environment, in gross anatomy2 and in the physiology of various organs. The effect of previous reaction on later movements has also not been taken into consideration. While it

is not our intention to minimize the importance of the nervous system in connection with the development of behavior, we wish to express our doubt concerning the view that morphological development of the nervous system can be used as the absolute index of behavioral development. The prepared scctions of the nervous system of the amblystoma by Cogl~ill arc, of coursc, objcctivc. n u t mnny of his interpretations are open to objections. I n the fifth article of this series we shall point out that his explanations of dominance of trunk movements over the gill movement are far-fetched. We wish to give here another instance to show that Coghill's views are far from being adequate. Coghill believes that the development of behavior is solely determined by the growth of the nervous system. He says: "Growth o f the terminals of axones and dendrites through microscopic dimensions is sufficient to have profound effect in behavior. This we have demonstrated in the first lecture in a vertebrate of such primitive f nerve cells form as Amblystoma, which, by the growth of the terminal o f a millimeter, transover a distancc of less than one one-hundredth o forms itself from an animal that must lie helpless where chance places it into one that can explore its environment in response to impulses from within or stimulation from without. This is for amblystoma a discovery, so to speak, o f incalculable significance. It is to all intents and purposes a solution of one o f the crucial problems of life" (1929, pp. 84-85).
Tf t,l~is it~t~cr.prcl;ntron of Coghill i~ corrcct, indccd, if the mere growth of 0.01 Inm. of the terminal of nerve cells is really responsible for the capacity of the amblystoma larva to swim, this 0.01 mm. of ncrvc ter~ninnls must be nothing short of a miracle. But has Coghill taken into account other morphological, physiological and even environmental changes which have taken place before the amblystoma can swim? During this stage, are there not changes in the amblystoma in general metabolism, and in the morphology and physiology of the muscular system? Do these changes effect the swimming movement of the amblystoma? In this paper we have presented enough evidence to show that such changes are a t least just as important as the morphological

* The workers on mammalian fetal behavior have not gone beyond the mere measurement of body length of fetuses under observation.

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changes in the nervous system. And yet in Coghill's work such important factors are entirely ignored. To make my point clear, I will cite one simple experiment on the chick embryo. One or two days before hatching, the entire shell and both the outer and inner shell membranes are removed (in some cases a small portion of the chorio-allnntoic membrane is nlso pierced to ndti~it t~ir for brcntliilig) so t ~ s to c~llowthe clliclc to get out earlier than the control ones whose egg shell and shell membranes are intact. But, contrary to our expectation, these experimental chicks do not attempt to get out any sooner than the control ones (not even half an hour earlier); they lie motionless and much more helpless than Coghill's amblystoma before the Intter cnn swim. And t,llcrc is not tho slightest nt,tcmpt on the part of tlic exycrimc~ital chick to "explore its environrncnt" bcfore the time when the control chicks attempt to gain egress from the shell. Is this failure on the part of the experimental chick to solve its "crucial problem of life"# sooner than the control ones due to the fact that 0.01 mm. of nerve terminal has not arrived to perform the miracle? Of course, no one denies the possibility of morpho1ogica.l growth of the nervous system during the interval between the operation and the time of hatching. But that such a growth of nerve cells is solely responsible for the ability of the chick to hatch is, a t least, very questionable. A much simpler but more correct explanation of the case is this: The hatching chick must have gained sufficient muscular vigor before it can emerge from tllc ~llell. This cnn only i>cgnincd nitor long l~oars of pulmonary respiration which takes the place of chorio-allantoic respiration one or two d ~ y bcfore s hatching. Thus, many chicks s a result of the faTlure to e s t a b m have died before hatching a o n p . i u Besides, before hatching, there is still a considerable amount of yolk sac over the folded legs and the ventral wall. The liquid content and the extra-embryonic membranes, too, are not sufficiently dry until the moment of hatching. All these tend to impede the movement of the chick. I n other words, it is the environmental changes, such as the enclosure of
Indeed, if one is teleological-minded enough, one should think t h a t the problem is by far more crucial for the hatching chick than for the amblystoma Inrva.

the yolk sac into body cavity, etc. (see Kuo, 11), and especially, changes in' respiratory metabolism that account for the ability of the chick to "solve one of the crucial problems of life." It is very doubtful that the growth of nerve terminals plays an important part in such cases; for the movements by means of which the chick gains egress from the shell are the very movements whicli hnvc bccn in cxistcncc rnorc than tcri days bcforc hr~tching.4 I n other words, no new movements which would come about as a possible result of the growth of the nervous system are required for the chick to be a.ble to emerge from the shell. Coghill goes even so far as to assert that "the normal experience of thc animal with reference to the outside world appears to hn.vo noU~ing to (lo with t h o dctcrminntion of thc form into which thc bcllnvior of tlie allinin1 is cast" (1'320, p. 87). One h,?a only to consider the evidences presented in this paper as well as in the fourth and fifth articles in order to be reasonably convinced that Coghill's view is erroneous and wholly inadequate. Certainly the development of behavior, in higher vertebrates a t least, is too complex and complicated to be explained solely or even mainly by anatomical growth of the nervous system.
REFERENCES
ANQULO, A. W., Y GONZALEZ: Neurological interpretation of fetal behavior. Anat. Rec., 1929, xlii, 17. ANGOLO, A. W., Y GONZALEZ: Neurological interpretation of fetal behavior. Annt. Jtnc., 1030, xlv, 254. Avmnr, G. 1 ' . :~ t n ~ ~ ) o n of ~ fntnl c f i ~ ~ l i n cpi^^. n Gcnot. I'~ycho1. Monog., 1928, iii, No. 4. RICHAT,X.: Allgemeine anatomic angewandt nuf die Physiologic und Arzneiwissenschnft. u b e r V. Pfnff. Lcipzig, 1803. BOLAFFLO, hl., AND ARTOM, G.: Ricerche sulln fisiologia del sistemn nervosa del feto umnno. Arch. d. Scienze biol., 1924, v, 457. BROWN, G. T.: On the nature of the fundamental activity of the nervous centers, togethcr with nn nndysis of the conditioning activity in progression and a theory of the evolution of function in the nervous uystcm. Jour. Physiol., 1914, xlviii, 18. BROWN, G. T.: On the activities of the central nervous system of the unborn foetus of the cnt with n discussion of the question whether progression is a "learnt" reflex. Jour. Physiol., 1915, xlix, 208.

!The only differencelies in the fact that these movements a t hatching are much more vigorous than before the establishment of pulmonary respiration.

f '

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COQHILL, G. E.: Correlated anatomical and physiological studies of the growth of the nervous system in amphibia. 111. The Floor Plate of Amblystoma. Jour. Comp. Neurol., 1924, xxxvii, 37-69. C o o r r ~ ~ rG. , , E.: Thc growth of functional ncurones and its relation to the development of behavior. I'roc. Amer. I'hil. Soc., 1926, Ixv, 51-55. COGI~ILL, G. E.: Correlated anatomical, etc. V. The growth of the pattern of motor mechanism of Amblystoma punctatum. Jour. Comp. Neurol., 1926a, XI, 71. C o a r r r ~ G. ~ , E.: Corrrlntcd nnntornirnl, rtc. VJ. The mrrhnniam of intc~rntion in Amblystoma punctatum. Jour. Comp. Neurol., 1920h, xl, No. 1. COOHILL, G. E.: Anatomy nnd the Problem of Behavior. Cambridge University Press, 1929. COQEILL, G. E.: Correlated anatomical, ete. IX. The mechanism of association of Amblystoma punctatum. Jour. Comp. Neurol., 1930, li, No. 2. Icuo, Z. Y.: Ontogeny of eml~ryonic behavior of nves. I. The chronology and ~ c n e r n lrrnturr of tllc 1,rhnvior of tlrr clriclc rrnl~ryo. (To npl)cnr in .lot~r. 11:~l)t. Zool.) Icuo, Z. Y.: Ontogeny of einbryonie behnvior in nves. 11. Thc mcchnnical factors in the various stages leading to hatching. (To appear in Jour. Expt. Zool.) Kuo, Z. Y.: Ontogeny of cmhryonie behavior in aves. IV. The influence of prenatal behavior upon postnatal life. (To appear in this JOURNAL.) Kuo, Z. Y.: Ontogeny of embryonic behavior in aves. V. The reflex concept in the light of the behavior of the avnin embryo. (To appear in Psychol. Rev.) Icuo, Z. Y.: Ontogeny of embryonic behavior in aves. VII. Experimental control of embryonic positions. (To appear soon.) Kuo, Z. Y.: (a) The effects of malpositions on the morphological development in the bird eml~ryo. (?'o appear in Anat. Ree.) Icuo, Z. Y.: (b) Causes and prevention of embryonic mortality in the fowl. (TO appear soon.) Kuo, Z. Y.: (c) The mechanics of embryonic behavior in birds. (To be pu1,lished soon.) LAN~~ORT 0. I I 12.: Y , A rnrrclr~tcd st~ldy of thc clcvcloprnrnt of roflcu nctivity in fetal and young kittens and the myelinization of tracts in the nervous t o Embryolom, 1929, xx, 127. ~ y ~ t e mContril)rltion . MINKOWSKI, M.: u b e r Uewegi~rlgenund Iteflcx des menechlicben footus wallrend der ersten Halfte senier Enlwicklung Schweig. Arch fur neurol. und Psychiate., 1921, viii, 148. M~NKOWSKI, &I.: u b e r fruhseitige Ben~egungen, Reflex and muskulare Reaktionen beim menschlichen fotus und muskelcsystem. Schweiz. Mcd. Wochenschrift, 1922, 721 and 725. MINKOWSKI, hI.: Zur Entwicklungs geschichte, Lokalization and Klinik des Fussonleureflexes. Schweizer Arehiv fiir Neurol. U. Psychiat., 1923, xiii, 475-514. MINKOWSKI, M.: Zum gegenwiirtigen Stand der Lehre von den Reflexen. U. S. W., ibid., 1924, xv, 239-259.

MINKOWSKI, M.: Zum gegenwiirtigen Stand der IJehre von den Reflexen. Neurolog. U. Psychiats. Abhandlungen (Fussli, Zurich) Heft, 1925, i. PANKRATZ, D. S.: The possible relations of the development of the suprarenal gland to the origin of the foetal movements in albino rat. Aunt. Rec., 1930, xliii, 235. PATON, S.: The reaction of the vertebrate embryo t o stimulation and the nssociated changes in the nervous system. RIitteiI. a. d. 2001. State. Z. Neapel., 1907, xviii, 535. I'REYER, W.: Spcciclle J'hy~iologiet l c ~ Emljryo. T,eipzipl, 1885. SWENSON, E. A . : The simple movements of the trunk of the albino-rat fetus. Anat. Rec., 1928, xxxviii, 31. SRENSON, E. A,: Motion pictures of activities of living albino-rat, fetuses. Anat. Ree., 1928, xxxviii, 63. SWENSON, E. A.: The active simple movements of the albino-rat fetus. Anat. Rcc., 1929, xlii, 40. Tnhc:~, 11. C.: 'I'll(: tlrvrlo~)~r~rrif, o f tnotilit,y n.ntl I~nhnvior rrnction~ i r i l,lrr tondfish ( O ~ " ! I . ~trui). I I S .lour. Corn!). Ncrlrol., 1920, XI, 253. WINDLE,W. F.: The earliest fetal movements in the eat correlnted with the neurofibrillar development of the spinal cord. Anat. Rec., 1930, xlv, 249. ZUNTZ, N.: u b e r die Respiration des Saugethierfoetus. Pfluger's Archiv. f. d. Ges. Physiol., 1877, xiv, 605.