374

LIGHT AND SEASONAL REPRODUCTION IN ANIMALS

BY WILLIAM ROWAN, D.Sc., F.R.S.C., F.Z.S. (Professor of Zoology, University of Alberta)

(Received 6 November 1937)

CONTENTS

I. Introduction . . . . . . 11. Photoperiodism in plants . . .

111. Light, migration and reproduction in birds IV. Experiments in migration . . . V. Other light experiments . . . .

( I ) Birds . . . . . . (a) Light effects . . . (b) The eye as a receptor . . (c) Other receptors . . . (4 Lengthof day . . . (e) Methods of administering light

(2) Mammals . . . . . (3) Reptiles . . . . . (4) Amphibia . . . . . (5) Fish . . . . . . (6) Invertebrates . . . .

VI. Problems presented . . . . VII. Animals investigated . . . .

VIII. Summary . . . . . . IX. References . . . . . .

Addendum . . . . . .

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I. INTRODUCTION

THE extensive interest shown to-day in the readily demonstrable effects of light on the reproductive activities of various animals appears to owe its existence mainly to a general feeling that a fundamental principle is involved which is not yet clearly defined, while the contradictory nature of the fast accumulating experimental evidence affords a constant stimulus for further research. Investigations of one sort or another with direct bearing on the subject are proceeding in widely separated portions of the globe, while the reactions of over fifty species of animals have now been investigated in an attempt to find a solution. It is the purpose of this article briefly to review the history and to consider the present status of the subject.

Since it was first shown that it was possible to induce finches of the northern hemisphere (Junco hyernalis) and related birds, with a brief breeding season re- stricted to a few weeks in spring, to come into full breeding condition in mid-winter by means of artificial light while exposed to excessively low temperatures, the centre

Light and seasonal reproduction in animals 375 of interest has gradually shifted from repetition and corroboration of the original experiments, to attempts to elucidate the mechanism involved.

As will appear presently, the essential principle incorporated in the work de- scribed below lies in the length of time for which animals are exposed to illumination and the method of its administration. Other factors, such as wave-length and in- tensity, appear to be of secondary importance. A similar concept is the basis of what the American workers, Garner & Allard, have termed “ photoperiodism ” in plant husbandry. Their first paper appeared in 1920 and embodied data of great importance, which since then have been widely substantiated by other workers. Quite independently, on totally different lines and in complete ignorance of bo- tanical work then in progress, the same general concept had been formulated in the Department of Zoology in the University of Alberta in 1922 with special reference to the migration of birds. Two years later the idea was put to the experimental test and found to hold good. In both fields, plant and animal, the importance of light to the general welfare and especially the reproductive activities of the organism had been sensed for many years previously, and the idea, in one form or another, is very old in the realms both of botany and zoology.

In view of the patent dependence of plants on the visible rays of the spectrum and the amount of practical interest taken in the question for a century and a half, it is perhaps surprising that the exact nature of the relationship in plants should not have been determined earlier. That birds and their migrations have provided the key in the animal world is not inappropriate since no other vertebrates, migratory fish not excepted, enjoy the unlimited freedom of movement that enables birds to satisfy whatever desire they may have for days of greater or lesser duration.

11. PHOTOPERIODISM IN PLANTS

Although this article will concern itself primarily with the zoological aspects of the problem, a brief summary of the botanical side seems desirable.

Smith (1933), in a lengthy review, states that the first reference in the literature known to him of the influence of the length of day on plants occurs in LinnC’s Rtin om vaxters plantering grundat p a naturen, 1793. According to Smith, LinnC attributes the obvious effects on the maturity and growth of plants observable in the arctic, not to the great length of day, but to additional heat resulting from con- tinuous sunshine. This suggestion was revived 40 years later by Schiibeler in England (1880), while at the same time Siemens (1881) made what appears to have been the first attempt to substitute artificial light for sunshine and to examine the effects of artificially produced continuous illumination at low latitudes. Artificial light and its reactions on the growth of plants subsequently received much attention towards the end of the century, particularly in America, and investigations of this type soon became fairly general. Tournois (1912), working in France, was the first actually to note that it required a length of day of particular duration to bring certain species of plants to sexual maturity. Klebs (1918) in Germany carried on much more extensive investigations, but it was left to Garner & Allard (1920) finally to elucidate the

376 WILLIAM ROWAN problem systematically and to demonstrate the importance of relative length of day and night to the growth and maturity of various species of plants. They proposed the term phtopmjodisnt to designate the phenomena involved. Gamer (Duggar, 1936), in a comprehensive review of the entire subject, points out that what proves to be a correct determination for one species of plant may not apply to another and that no general rule can be formulated. This is an important point and, as will appear below, applies as much to animals as to plants. Failure to realize it obscured the correct viewpoint in the earlier plant investigations and until recently has fogged the issue in animal work as well.

111. LIGHT, MIGRATION AND REPRODUCTION IN BIRDS

The suggestion that daylight was a factor in inducing the annual migrations of birds goes back to the days of the Swedish poet, Runeberg (1804-77), as cited in the Academy of 1874. Seebohm (1888) is generally given credit for the original suggestion, but he is quite specific in his statement, attributing only the southern migrations of certain of the Charadriidae to a search for light during the winter months.

An essentially different concept was propounded by the late Sir E. Sharpey- Schafer in an address read to the Scottish Natural History Society on 7 November 1907 (Schafer, 1907). He assumed that the relation of light to darkness was not only the determining factor in producing the north-to-south migrations but might be held also to account for the regularity of the migrations themselves. He points out that climatic conditions are so variable that migration, so punctual in its inci- dence, can hardly be dependent upon them as inciting stimuli. He further suggests that the relationship of light to darkness may also be held to account for the regu- larity of the northern migrations as well as the southern. Schiifer, however, failed to see any connexion between the facts he so ably analyses and reproduction, and offers the opinion: “that it (the northern migration) is a result of developmental changes in the sexual organs is improbable.”

Eifrig (1924), as a result of encountering the work of Gamer & Allard, but evidently unaware of Schafer’s paper, propounds a similar hypothesis, and also comes to the conclusion that the reproductive .organs are not directly concerned in the mechanism of migration.

In the meantime many other authors had seen a connexion between the north- ward migration of birds in the northern hemisphere and reproduction. The fact has been commented upon and taken for granted since the days of Aristotle and even before him, for Anacreon (sixth century B.c.), as rendered by Moore (Godley, 1929) says :

Once in each revolving year, Gentle Bird! we find thee here; When nature wears her summer vest, Thou com’st to weave thy simple nest.

Biological authors have been less poetical and more specific. That there seems to be direct association between the recrudescence of the gonads and the northward

Light and seasonal reproduction in animals 377 passage was long ago pointed Out, e.g. by Chapman (1894), Eagle Clark (1912) and Phillips (1913).

The annual rhythm of the avian gonad, until 1924, was universally held to be due to annual changes in temperature, probably as an outcome of Loisel’s work (1900-1).

In the poultry world use has been made of artificial light for increased egg production for over a century (Baker & Ranson, 1932~). Although cqnsidered analogous by authors, the case is actually very different from those with which this review deals and which consist exclusively of birds or other animals with brief, well-defined, annual breeding seasons that cannot be extended beyond tbeir normal limits by any means at present known. The season can be experimentally shifted by the use of artificial light from spring to autumn or the middle of winter, but it runs its limited course and terminates automatically then as it does in spring. The effect of an extended length of day on hens in the autumn is, on the other hand, to protract the laying period.

In the wild birds dealt with below, sexual maturity is in direct relationship to the seasons. Age is a factor in so far as some birds do not breed till their second, third, fourth or even fifth year, but when maturity is finally attained, the breeding season is restricted to the spring. Pullets, on the other hand, hatched in March will commence laying in autumn if the weather is not severe. Sexual maturity is pri- marily in relation to age. The two cases no doubt have one or more factors in com- mon, but they are nevertheless fundamentally different.

In addition to its employment in the matter of increased egg production in poultry, the use of artificial light for the stimulation of the reproductive organs is extremely old in at least two other connexions. Miyazaki (1934~) points out that the practice of “yogai”, for instance, has been in vogue in Japan “from fairly ancient time”. It consists of exposing pet birds, such as Zosterops, to artificial illumination for 3 or 4 hours after sunset towards the close of the year in order to bring them into singing condition in January instead of at the normal period of spring.

Details of an old custom, widely practised at one time in Holland, but now almost forgotten, have kindly been given me by Dr G. J. van Oordt in whose laboratory an investigation of the problem is now proceeding. I ‘ Formerly, when in Holland very many song birds were caught in autumn by means of live decoys, the latter were put into the dark in the middle of June and were exposed to light again in September so that at this time and in October they were in full song. This was called by bird catchers ‘to put them into the “muit”,’ while in September they came out of the muit ’.”

IV. EXPERIMENTS IN MIGRATION

The series of experiments in migration commenced in 1924 owed their inception to a desire to induce reversed migration in some species of bird as a possible con- tribution to the Lamarckian hypothesis. The brief summary above is a statement of the pertinent knowledge as it then existed. Before any attempts to reverse migration

378 WILLIAM ROWAN could be contemplated, it was obviously necessary to know something concrete of the mechanism involved. Field investigations were started in 1919 in order to acquire first-hand knowledge of migratory movements and normal behaviour of actively migrating birds. The knowledge derived during the few ensuing years provided the key sought for. By 1922 a working hypothesis had been formulated but no funds were available for making the initial experimental attempt. When the opportunjty presented itself in 1924 the immediate object was merely to determine if the gonads of birds could be artificially stimulated to spring recrudescence in the autumn, in the belief that if this were possible, and the birds were liberated in such condition, they might migrate north on release. Knowledge of hormones and sexual behaviour, in spite of the enormous advances since that time, was already firmly established, and the assumption was made that the northward migration might legitimately be considered to be a phase of sexual behaviour which owed its seasonal recurrence to a hormone elaborated by the developing gonads.

The universally adopted viewpoint with reference to the annual rhythm of the avian gonad was that this depended on seasonal changes of temperature. Familiarity with the field facts of migration in the northern hemisphere, however, made it seem so highly improbable that this viewpoint could be substantiated that the attempt to apply it was never made. The concept was discarded as hopeless and manipulation of the length of day by means of artificial light substituted for manipulation of temperatures.

The basis of this conception lay primarily in the extreme regularity with which birds migrate north, possibly the most striking single aspect of the northward passage, and one that has been commented on since the days ofiPliny. There was no room for doubt that the impulse that brings birds north, if actually dependent on external factors, must be incited by stimuli of far greater regularity than seasonal temper- atures. After examining all the possible environmental influences, relative lengths of day alone appeared to meet the requirements, a suggestion subsequently found to have been made already by Schafer as long ago as 1907. Since the junco (the original species used) is subjected each spring on its wintering grounds in the middle States to days increasing at about the rate of 2-3 min. daily, it was decided to submit the birds to similar daily increases during the Alberta winter by means of artificial illumination. Below-zero temperatures (F.) are normal in Alberta in November and December, and the birds were kept in the garden without any extraneous sources of warmth in order to eliminate all doubt in the matter of high temperatures. By the end of December, in spite of a minimum reading of 52' below zero F. (84 degrees of frost) the birds that had been kept on increasing lengths of day were singing and their gonads maturing.

The gonads of controls in the meantime, receiving no artificial illumination and exposed to the shortening days characteristic of the early winter, remained completely undeveloped, while the birds made no attempts to sing.

The experiments commenced in 1924 (using mainly the junco) and terminated in 1928 (Rowan 1925, 1929). In 1925 and 1926 repetitions of the 1924 attempt were made with modifications of various kinds affecting mainly the intensity of illumination. By 1927 the optimum had been found and it proved possible, re-

Light and seasonal reproduction in animals 379 gardless of extremely low temperatures continuing over long periods of time, to induce a rate of recrudescence exactly comparable with that of spring material (that is, complete maturation and normal histology) with great uniformity, in a large number of birds. The sole source of illumination was ordinary electric light bulbs devoid of ultra-violet. The available daylight, decreasing continuously through November and December, was used from daybreak to dark, with electric light added at nights. A large aviary, erected from funds provided by the Royal Society of London, was used in 1926 and 1927.

The main point having been satisfactorily established that recrudescence of the gonads of the junco and various other migratory finches, as well as canaries, could be induced by exposing the birds to increasing lengths of day, a few related points were cursorily investigated as follows.

In January 1928, thirty-three birds remaining over from the main undertaking were given reduced days by means of a shutter used on a small aviary. Some were reduced from a 15 hr. to a 9 hr. day overnight: others had their light allowance reduced 15 min. daily till a g hr. day was reached. In both cases reversion of the gonads to winter condition took place.

The survivors were then again given increasing days (without artificial light, the days themselves in February and March being of sufficient duration) and by the end of May, when killed for examination, were found once more to be in full breeding condition, the third time in twelve months.

Another group of birds was given daily increases of 15 min. Developmental regularity ceased. The explanation is not clear, but this condition appeared to im- pose a physiological strain on many of the individuals as they failed to stay awake throughout the extension. A few individuals, however, did so, and a few showed an accelerated rate of recrudescence, presumably the same individuals, although the birds were not marked and the point was not established.

The distinction between actual breeding and the breeding condition should be recognized. The inhibitory effects of captivity, while but little understood, are at least very apparent in the breeding of wild animals, and birds of this sort-the junco and related finches-can seldom be induced to reproduce in aviaries even in the most ideal circumstances. They may be in perfect health, with gonads normal in all respects, actually confined within the habitual breeding range of the species and apparently fully able to reproduce, yet make no attempt to do so. The subject has been well dealt with by Marshall (1936). The fact that none of these birds attempted to breed is therefore no reflection on the outcome of the illumination experiments. The histology of the gonads was in every respect normal.

Low temperatures undoubtedly inhibit breeding, even in wild birds, and late nesting seasons are a common accompaniment of an inclement spring. In some species even migration dates may be affected though this is by no means universal. The canaries housed with the juncos failed to breed in the garden at low temperatures in January and February, but if transferred to the house, where temperatures are high, will nest during those months.

The essential point having been successfully established (in juncos) that the gonads could be artificially stimulated to spring recrudescence in the autumn by

380 WILLIAM ROWAN means of artificial illumination, despite low temperatures, the American crow ( C o w brachyhynchos) was next used in an attempt to induce reversed migration. Two separate undertakings materialized (Rowan, 1930, 1932). Only two points are im’mediately relevant to the present account. First, this species responded to light treatment in all essential respects as did the juncos. Secondly, castrated individuals, subjected to artificid illumination, failed to go north, evidently reflecting the removal of the reproductive organs.

V. OTHER LIGHT EXPERIMENTS

(a) Light effects. (I) Birh

The first investigator to repeat the experiments with light was Bissonnette, working at Hertford, Connecticut, U.S.A., and using the starling (Sturnw. mZgaris), a bird introduced from Europe into the State of New York in 1890. The species is non-migratory in the United States.”

Bissonnetie (193oa, 1931 a) commenced his experiments on 4 December 1928, when starlings were subjected to increasing instalments of daily illumination at the rate of 15 min. per day. The effect on the gonads was to induce recrudescence as with the junco.

Lighting suddenly increased by 6 hr. and kept there produced a similar effect, except that there was a noticeable death-rate among the birds used. With reference to testicular development, maturation of the germ cells was premature under this treatment and metamorphosed sperms were to be found in testes less than half their normal volume, while uniformity was slight.

Regression of the gonads in birds already on a long length of day could be brought about (as in juncos) by reduction of the light period. Moreover, when the gonads had once attained their maximum development, they thereafter again under- went regression (in about 6 weeks) in spite of any lighting conditions to which the birds might be further subjected.

These experiments with starlings thus in general confirmed the results obtained with juncos as far as artificial illumination was concerned.

Bissonnette (193 I b), investigating the effects of different light intensities, found that there was progressive acceleration in the rate of recrudescence with bulbs of 10, 15, 25 and probably up to 40 W., but with intensities of 40 W. and upwards the progressive effects ceased. Using weak coloured lights, Bissonnette (1932~) and Bissonnette & Wadlund (193 I) found that red was the most effective in inducing pro- gressive changes, with white next. Bissonnette’s evidence and figures have been critically examined elsewhere (Rowan, 1938) and it appears that the tenability of his conclusions is doubtfu1.t Development under green light did not occur at the low intensities used, an observation corroborated by Benoit (personal communication) with Rouen ducks, but the potency of red light requires further examination and substantiation.

I am informed by Dr E. R. Kalmbach that the starling now shows signs of becoming

t See Addendum. migratory in various parts of its American range.

Light and seasonal reproduction in animals 381 Clark et al. (1936) have used pheasant, quail and ruffed grouse and found both

sexes of all these birds to react readily. Martin (1935) had already induced premature breeding in pheasants by use of artificial light.

Miyazaki (1934a, b) has investigated the same general points, using the white- eye (Zosterops palpebrosa juponica), a species that has been caged as a songster in Japan for many centuries. On I December 1932 Miyazaki subjected twenty-six males to a 15 hr. day by means of artificial light. By 20 December the first bird was in song, while by 5 January 1933 all were singing. In the meantime ten controls had failed to come into song by that date. The testes of the experimentals were pro- ducing fully mature spermatozoa.

Using the same birds, a second “yogai” was initiated on I September 1933 and stopped on 30 October, when the birds were again in song. With the remnants of the same batch, a third yogai was started on I December, the birds reaching singing condition for the third time inside 12 months like the juncos above.

A point of interest is that the author states that during the hours of extra illumination the birds may sit and doze-presumably having their eyes closed-but are finally brought into condition. In the ordinary yogai of the Japanese bird- fancier the light used appears to be always relatively feeble.

Kirschbaum & Ringoen (1936), using the house sparrow (Passer domesticus), have demonstrated that an extension of length of day averaging 64 hr. during October, November and December, will in 6 weeks bring this species into breeding condition. Cole (1933) has demonstrated the same sort of thing in the mourning dove (Zenuidura mac~ou~a) , while ducks (various species) have shown similar reactions (Bell & Rowan, results unpublished).

Benoit (1934a), in the first of a long series of experiments with Rouen ducks, used three pens of immature birds, 5-7 months of age, exposed to different con- ditions for 20 days in November. (a) Five birds had complete freedom out of doors; (b) five received heat, 17-20’ C., with the same illumination as (a); (c) five received illumination for 16 hr. daily but without heat. At the close of the experimental period the left testes of all the birds respectively weighed: (a) 0.3, 0-4, 0.42, 0.85, 1.45 g.; (b) 0.29, 0.34, 0.68, 0.8, 1-45 g.; (c) 13’4, 17-2, 17’4, 28.6, 48.8 g. High temperatures evidently had no effect on the development of the gonads; added length of day, at lower temperatures, was effective. That reduction of light induces regression of the gonads had been shown by Rowan (1929), Bissonnette( 193oa,193 IU), Miyazaki (1934a, b), Benoit (1936~) and others, while Clark et al. (1937) found that pheasants and grouse failed to breed at all when kept in very weak light during their normal spring breeding season.

!b) The eye as a receptor. The mode of stimulation of the gonads through increasing periods of illumina-

tion is as yet unknown, although it may be taken for granted that the effect is produced via the pituitary. Evidence on the role of the pituitary is seemingly con- clusive. The literature is too extensive to quote adequately here, but such papers as Schokaert (rg31), Hill & Parkes (1933a), Benoit (1935g) may be taken as repre-

382 WILLIAM ROWAN sentative. The relationship is fully discussed by Marshall (1936), Martins (1936), Riddle and others. That this organ can be activated by a direct beam of light trans- mitted to it through an insulated quartz rod has been shown by Benoit (1936b). I t can be similarly stimulated-with resultant gonadal activity-by means of electric current (Harris, 1937) and probably by Rontgen rays (Volpe, 1936).

Llewellyn (1932), Marshall & Bowden (1934), Benoit (1934a), Bissonnette (1936~) and others have expressed the opinion that light falling on the eye is capable of stimulating the pituitary (presumably by nervous paths) resulting in the gonadal development that can be so readily demonstrated. A considerable amount of work, specifically designed to elucidate this question, has been undertaken in recent years and is still in progress.

Benoit ( 1 9 3 4 ~ ) was the first to investigate it experimentally. Two batches of Rouen ducks were used, each including young individuals of from 5 to 6 months of age and adults, sexually undeveloped. (a) Birds were draped entirely in light-proof cloth, including their eyes ; (b) birds were similarly clad but with perforations left for exposure of the eyes. The testes of the former weighed respectively 0.61,0-68, 0.85 and 0.99 g. : of the latter, 14.7, 21.8 and 29.3 g. The point is not specifically stated, but the account reads as though the two groups were separately caged, probably a matter of primary importance as will appear below.

Benoit (1g35a), in an attempt to procure relevant evidence with reference to my own opinion on this matter (Rowan, 1928), designed an experiment in which two batches of Rouen ducks were given similar lighting conditions with (a) birds permitted complete freedom within their enclosure, and (b) birds trussed in such a manner that free movement was impossible. Testicular development in both cases was practically identical. The undertaking is, however, actually irrelevant, since the trussed birds were fully awake and, physiologically speaking, in a state of activity as complete as the controls. Muscular activity was reduced to a minimum, but the point is immaterial and does not affect the argument.

Later (Benoit, 1935 b) other ducks were clad in light-proof materials while immobility was superimposed on this condition. Perforations were made over the region of the eyes. The testes developed at the same general rate as before.

Benoit (1935d) next tried extirpation of the eyes. Immature ducks and adults with gonads at the minimum stage of development were used. Three groups were employed : (a) birds entirely draped in black ; (6) illuminated at night with head only covered; (c) illuminated at night without any covering at all. In all three groups, three classes of birds were included, some with the optic nerve alone severed, others with the eye and orbital glands completely removed, and normals.

At the conclusion of the investigation, the average weight of the testes for each group respectively was: (a) 0-35, (b) 0.48, (c) 20.25 g. The author’s conclusion is that illumination of the head in the region of the eyes stimulates the pituitary, since illumination was equally effective in all members of group (c) whether normal or with optic nerve severed or orbit completely extirpated. Since, however, the blinded birds of this group were kept together with normal birds, disturbance and enforced wakefulness were imposed on the blinded individuals, a point of primary importance,

Light and seasonal reproduction in animals 383 and dealt with again below. No unhooded birds were run with the (a) and (b) groups. In effect they were all on a short day.

Parhon & Coban (1935), in a somewhat similar undertaking in which four drakes were totally blinded, found that they attained sexual maturity at a greater rate than controls from January to March.

Ivanova (1g35), using the house sparrow, made a more elaborate investigation into the same problem. The birdswere kept in separate cages, the inmates of (a) being equipped with head coverings of silk with solid black blinkers fixed over the eyes; (b) mostly without caps, but some capped, the hoods provided with slits over the eyes in such manner that light could fall freely on the eyes themselves; ( c ) controls, whose cage was covered during the time that the (a) and (b) birds were being ex- posed to artificial illumination. (a) and (b) received a 14 hr. day, (c) one of 9 hr.

Four such series were run through from December to March, the period of added illumination varying from 3 to 6 hr. with different series. The controls (c) remained undeveloped throughout, although they showed slight enlargement in February and March, in spite of a constant period of 9 hr., (b) showed the greatest development in every case, but (a) birds were much nearer (b) birds in development than the controls (c), e.g. in series 4, January to March, with 6 weeks' illumination, the average testicular measurements were : (a) 5-03 x 3.56 mm., (b) 5-66 x 4-73 mm., (c) 2.38 x 1.80 mm. It is quite apparent from the figures produced by the author that even with the head and eyes completely covered, the rate of recrudescence was greatly in excess of that of the controls, and only slightly less than in the case of (b) birds without covering. Once again, the (a) and (b) birds were kept side by side, and disturbance and enforced wakefulness were presumably imposed on the hooded individuals (see below).

(c) Other receptors.

An additional feature of Ivanova's investigation was that in series 3 some of the birds of all groups had had the feathers of the back and breast shaved. Excepting in the controls, there was a greater rate of recrudescence among the nude birds than among those feathered. The author concludes that the effects of light on the reproductive system do not depend solely on exposure of the eyes, but of the body as well. An interesting point, however, not commented on by the author, lies in the fact that the rate of development among all controls was identical, whether they were feathered or not, yet they had been exposed to the full strength of daylight for g'hr.

( d ) Length of day. One more undertaking remains to be referred to. The question of the possible

mode of action of the extra light to which the birds were being exposed was already considered at the time of the original experiments (Rowan, 1925-9). It was then thought improbable that light, qua light, could provide the explanation. A cage was accordingly designed (Rowan, 1928), in which juncos could be kept on the move without light, or at least with light below the intensity that had already been shown

n R X I I I 26

384 WILLIAM ROWAN to be essential to induce gonadal development. Total exclusion of light proved impracticable.* The actual amount of exercise was slight, as the crucial element of the mechanism was a travelling bar that swept the perch and floor at regular in- tervals, occupying 40 sec. to complete a circuit, but the birds were kept fully awake, the important point. They soon got accustomed to it and merely hopped over it as it came round. A second bar was then attached to the belts, compelling the birds to move every 20 sec. The perch and bar were painted white to make them more visible and so permit a further reduction of light, which proved too feeble to measure by means of any instruments available and might adequately be described as a feeble glow. The motor was turned on nightly at 6 when the windows were shuttered and ran for 7 i min. the first night (17 March 1928), 15 the second, and so on till 10 p.m. had been reached when no further increases were made. By 28 April, when the undertaking terminated, the testes had attained a length of 3-4 mm. as against 1-3 mm. of the largest pair of control testes. Nine birds were used, no more being available at the time, but in spite of the small numbers the rate of progression was so uniform that its significance could hardly be doubted.

Additional periods of wakefulness added to a day of 9 hr. were thus similar in their effects to added periods of artificial illumination. The controls, exposed to the same feeble lighting as the experimental animals, but without disturbance, slept throughout the evening and showed no testicular development.

On account of the date of this experiment it has been suggested that the results were not strictly comparable to those in which light had been used and which had shown that gonadal development could be induced during the early winter months. In view of the experiments referred to above in which light curtailed in January and February had the effect of inducing regression of the organs, it seemed unlikely that the criticism was pertinent, but the undertaking was nevertheless repeated from 4 January to 28 February (Rowan, 1937), using again the junco and the same ap- paratus. The rate of development was slower than on the previous occasion but shipment of the birds to England had resulted in a high rate of mortality and only small numbers were again used. Only a single bird was available on the last day. A conclusive statement cannot be based on one measurement. The fact that re- crudescence of the gonads could be induced in the junco by means of additional daily periods of enforced wakefulness was, however, certainly confirmed.

This experiment has been repeated by Bissonnette (193 I a), using starlings, a non-migratory species introduced originally into the eastern United States from Europe. The apparatus used was virtually identical with that designed for the juncos, and the method similar except that the birds were given 15 min. additional disturbance nightly instead of 74 min. The results of the undertaking were negative, though not wholly so since a single bird showed enlarged testes. Only eight samples were taken in 5 months.

Besides failure to corroborate the results obtained on juncos the author records an excess of intertubular pigment. Starlings’ testes are peculiar in the presence of a dark green pigment between the tubules which colours the entire testis during its

See Addendum.

Lkht and seasonal reproduction in animals 385 winter stages. The colour gradually disappears as the testes enlarge and in the spring condition they no longer look green. The significance and function of this pigment are at present obscure but its excessive production, even if confined to the interstices of the tubules, indicates testicular activity of some sort. Although the author sees no significance in the behaviour of his birds, it differed essentially from that of the juncos. He describes in detail how they spent their time, while the motor was running, hanging on to the wires until completely exhausted, when they would take brief rests on the perches, promptly to return to the netting. The mechanism was ineffective with starlings. Protracted fright and muscular exhaustion were factors that did not enter into the junco experiment at all. The two undertakings were not comparable.

It has since been shown (Rowan, 1937) that starlings roosting on London buildings in the feeble illumination of the street lamps during the winter nights, where they are kept awake by the incessant passing of heavy traffic, show precocious development of the gonads in early February. There are several uncertain factors in this situation but in general it corresponds to the terms of Bissonnette's experi- ment, with fright and muscular fatigue eliminated, for the birds have selected these roosts with their continual disturbance of their own accord. The topic has been dealt with at length elsewhere (Rowan, 1938).

( e ) Methods of administering light. Benoit (1936a), in a paper to be commended for its lucidityand explicit statement

of fact, has given a lengthy account of his recent undertakings which contain much of interest. He again used Rouen ducks, and by means of laparotomy ascertained the state of the gonads in the case of each individual used at the outset.

A dark room, admitting a small quantity of light, was used for all birds subjected to darkness ; a light room, from which daylight was entirely excluded, was illumi- nated with six to eight electric light bulbs of IOO W., distributed over an area of 2 x 4 m. burning from 6 p.m. to 8 a.m., a period of 14 hr. In special cases cages were used of 50 x 80 x 60 cm., illuminated by single IOO W. bulbs.

The first undertaking described consisted of taking ducks in mid-February, with testes already on the road to development, and enclosing them in the dark chamber. Here they were retained either for I or 3 months. In all cases the testes continued to develop, but very slightly as compared with controls exposed to normal conditions outside.

The effects of various methods of administering the same quantity of light were next investigated. The author draws attention to the fact that there is a quantitative response to the intensity and duration of illumination and that the rate normal to ducks in the open in spring can be greatly exceeded by the use of electric light.

Five young ducks were confined for 4 or 5 days in the illuminated chamber referred to above (14 hr. light daily) and then transferredeto the dark chamber for a month or more. The development of the testes initiated by a few days' exposure to light, did not cease; the organs showing increases in weight of from 33 to 80 per cent., relatively slight in comparison with spring development.

26-2

386 WILLIAM ROWAN Four further groups from the dark chamber were given a total of 40 hr. illumina-

tion during a period of 3 weeks in four different ways, thus: (a) 13 hr. 20 min. on each of three single nights, the Ist, 7th and 13th of the 3 weeks; (b) 24 hr. per night for 16days of the21 ; (c)30min. thefirstnight,followed byanightlyincreaseof 15 min. over 16 days of the 21 ; ( d ) I O ~ min. per hour, during 14 hr. of the night, over 16 days of the 21. In both sexes ( d ) was the most effective. Males with smaller and larger testes were used. Among the first the order of effectiveness was ( d ) (c) (a) (b ) : the latter, ( d ) (a) ( c ) (b) . The greatest increase in size was from 8.3 x 19 to 27.7 x 50.2 mm. (a ( d ) bird). (In comparison, a bird exposed to a 15-18 hr. day for 3 weeks in October to November, shows changes of the following order-from 8 x 27 to 25 x 53 mm.)

“On voit que pour une lumihe de qualit6 donnCe, son in tmi tk et la d u r b de son action ne reprksentent pas les seuls facteurs injluenpnt la rkponse du mCcanisme gonado-stimulant. Celle-ci depend en outre dans une large mesure de I’augmenta- tion progressive des doses octroyies et du fractionnement de ces doses. Remarquons que le premier principe se trouve rCalisC dans la nature, entre le solstice d’hiver et le solstice d’CtC. Quant au second, il corrobore A mon avis cette notion prCctdem- ment exposCe selon laquelle une incitation lumineuse passagkre dCclenche une activation physiologique d’une certaine dude ” (Benoit, 1936a, p. 528).

Two ducks only, exposed to long illumination for a period of 5 months, had testes far gone in regression and completely regressed. No laparotomies had been performed, but there seems no question in view of other results that they had attained a maximum at some time and regressed thereafter.

To sum up the effects of artificial illumination on the reproductive activities of birds, it may be stated, in general, that intensity of a certain, relatively feeble, standard is essential, and that increase beyond that point has no additive effect. It should, however, be noted, that Benoit consistently gets speedier development in Rouen ducks than the natural spring rate, while the same occurs in starlings. This may, however, be due to the fact that a long addition is made to the length of day at the start of the experiments and adhered to throughout. In starlings (and apparently some other species) germ cell activity under these conditions is accelerated and maturity is attained long before the testes have reached their normal size. In juncos complete normality depends on slight, progressive advances in the length of illumination, longer jumps affecting the birds adversely and resulting in complete irregularity. Such lack of uniformity is also very apparent in the results obtained by Benoit and Bissonnette.

The seemingly essential nature of small additional increments has been noted and commented on by various authors, including Rowan, Benoit (cited above), Whetham, Miyazaki, and others.

If the effects are not directly attributable to the action of light on the eye or other receptors, but are a matter of physiological changes induced by prolonged activity, the temperament of the species used and its nervous reactions to experi- mental treatment become a matter of importance. Rouen ducks are domesticated ; starlings are nervous ; juncos are not. Variation in detail from species to species can be legitimately expected; at all events it has been shown to exist.

Light and seasonal reproduction in animals 387

(2) Mammals

The first investigators to examine the effects of light on the reproduction of mammals were Baker & Ranson ( 1 9 3 2 ~ ) using the field mouse (Microttrs agrestk). They found that by shortening the daily period of exposure to light from 15 to 9 hr., reproduction almost ceased, the female being most noticeably affected.

In 1932 Bissonnette (1932b) applied the principle of extended length of day to the ferret (Putorius wukaris). The breeding period of these animals runs normally from March to August. He found that females could be brought to full oestrus in 38-64 days between October and January by subjecting them to 6-64 hr. artificial illumination additional to the regular daylight hours which by themselves produced no effect on controls. Males showed only a partial response. They exhibited willing- ness to copulate, and developed full accessory organs, but matings were sterile. In the testes, although interstitial tissue was well developed, spermatids were rare and spermatozoa not to be found at all. No ultra-violet rays were administered, and the extra illumination was given from the commencement in one extension of 6 hr.

Marshall & Bowden (1936) found that a z hr. increase in length of day with eight 60 W. bulbs was as successful in inducing winter breeding as a 16 hr. increase with one 60 W. bulb. The significance of this undertaking is not clear for the effects of a 2 hr. increase with a single bulb were not determined. It is possible, in view of results obtained on birds by various investigators, that a single bulb might have proved as effective as eight.

Bissonnette (1935 a) subsequently found that light applied in small progessively increasing instalments induced normal testicular development and fertile matings, a result obtained also by Allanson et al. (1934) by injection of pregnancy urine extract combined with a constant advance of light.

Hill & Parkes (1933 b), in corroborating the effects of light on ferrets, found that hypophysectomy eliminates the reaction completely, a result to be expected if the pituitary is intermediary in sexual stimulation.

Reduction of light has been experimentally applied by Hill & Parkes (1934), Marshall & Bowden (1934) and Bissonnette (1935a, b). Hill & Parkes failed to arrest oestrus in ten ferrets (five males and five females) subjected from the end of January to 234 hr. darkness per day. They conclude that “while additional light will induce oestrus in anoestrous animals, the onset of the breeding season in the spring is not dependent on the increasing length of daylight ”.

Marshall & Bowden found that of seven ferrets, four came on heat and three failed to do so when subjected to almost total darkness from Z I April till the end of July. Bissonnette’s figures and treatment are rather complex and it is difficult to agree with his own verdict that light reduction actually induced cessation of oestrus. Hoods over the eyes were used on some of his ferrets, but frequent r e m o d by the animals themselves complicated the issue.

Bissonnette (1936~) cut the optic nerves of ferrets and found that they came into oestrus although there was a lag in the dates. Le Gros Clark et al. (1937), in an investigation of unusual interest, have made experimental lesions in the brains of

388 WILLIAM ROWAN female ferrets as follows: (I) ablation of the visual cortex in both hemispheres; (2) destruction of both superior colliculi ; (3) bilateral section of the optic tracts at the ventral border of the lateral geniculate bodies, cortex and mid-brain ; and (4) retrobulbar section of both optic nerves. The animals were operated on in November and December and exposed to prolonged light. Those of classes (I) and (2) came into heat simultaneously with controls, at from 50 to 70 days, post-mortem ex- amination having shown the operations to be completely successful. Those of class (3) came in at the same time but there remains doubt on the completeness of the operation. Of two animals involved in class (4), one came on heat after 142 days, the second not at all.

Marshall & Bowden (1934), in investigating the effects of various wave-lengths in inducing oestrus in the ferret, found that “heat rays and the near infra-red ( A 7500) are comparatively inactive. The effect begins with the red radiation ( A 6500) and extends throughout the visible to the near ultra-violet ( A 3650). Over this range of the spectrum intensity appears to be more important than wave-length.

‘‘ None of the wave-lengths employed produced retardation in the recurrence of oestrus.”

Bissonnette and Csech (1937) have induced winter breeding in the raccoon. Reactions to light of the thirteen-lined ground squirrel (Spermophilus tridecem-

lineatus) have been investigated in America. This animal is interesting because it normally hibernates for some 6 months annually. During this time it is sexually inactive, although development of the gonads commences in December during the period of sleep, and the animals emerge sexually mature. Johnson & Gann (1933) subjected groups of these spermophiles, six males and six females in each group, to red, green, white, blue and ultra-violet light from I December to I July. In no case was there any apparent difference between the experimental animals and their controls. Other groups were kept in continuous red and continuous white light, and also in continuous darkness, in a cold room from 28 December to 23 March. All hibernated until 9 March, when the temperature of the room rose. All developed approximately similarly and synchronously with the controls.

Wells (1934, 1935) has also found that progressively larger doses of artificial illumination have no stimulating effect on the reproductive organs of this species.

Dempsey et ul. (1933, 1934a, b) have used the guinea-pig for an investigation of the effects of light on reproduction. They have noted a nightly shift in the “heat peak ” of females at different times of the year and associate the tendency to copulation towards the later hours of the night in spring and earlier ones in the autumn with the lengthening days of the former and the shortening days of the latter season. When guinea-pigs were confined to a darkened room for 4 months continuously, it was found that the females came into heat quite regularly, while young females born under these conditions have shown normal vaginal rhythm and actually come into heat.

Smelser et al. (1934) subjected domestic rabbits for 30 days (a) to intense illumi- nation, and (b) to almost total darkness. Both groups showed equal mating response, ovulation and pseudo-pregnancy. Rabbits, given adequate food, and warmth and suitable quarters, normally breed all the year round and fail to show seasonal periodicity.

Light and seasonal reproduction in animals 389 (3) Reptiles

Clausen and Poris (1937) have induced increased spermatogenic activity in the lizard (Anolts carolinensis) by means of artificial illumination.

(4) Amphibia

Shapiro & Shapiro (1934) found that in the clawed toad (Xenopw lax&) the ovaries underwent regression under ordinary circumstances in the laboratory, but this did not occur when the room was continuously lit. Alexander & Bellerby (1935), however, believe that the developmental condition of the ovary depends directly upon the amount of food available, and that the periods of ovarian growth and retrogression under normal conditions can be explained on the basis of fluctua- tions in food supply. X e n o p normally aestivates in summer.

Prof. E. A. Spaul informs me that he has induced breeding in frogs (Rum tmporaria) and newts (Triton cristutw) in winter by the use of artificial light. H e also found that gravid females of the viviparous salamander (SuZumundra maculosa) gave birth to young if exposed to lengthy illumination, while others not so exposed retained them.

( 5 ) Fhh Craig-Bennett (193 I), when investigating the life history and reproductive

cycle of the three-spined stickleback (Gatemstew anrleatw), carried out experi- ments designed to discover the relative values of food, temperatures, and light in bringing about annual breeding in the spring. He concludes that temperatures are all important and the effects of light negligible. Various light intensities were employed but the maximum duration was only I& hr. It appears highly improbable that the method employed could have produced positive results.

The stickleback has since been induced to breed at low temperatures during the winter months by means of light by Prof. N. Tinbergen of Leiden University, to whom I am indebted for the information and for permission to announce his results.

Prof. Spaul has also kindly given me permission to refer to his unpublished results on minnows (Phoxinus lamis) which have shown response to light stimulation during autumn and winter months.

Hoover (Hoover, 1937; Hoover & Hubbard, 1937) has induced winter breeding in the brook trout (Sulwelinus fortinah) by means of extended illumination.

( 6 ) Invertebrates

An extremely interesting paper that seems only recently to have come to light is that of Marcovitch (1923). With the approach of cold weather in the United States in November, oviparous females of Aphtsforbesi, strawberry root louse, make their appearance. The eggs hatch in February. By keeping the days down artificially to 7.A-8 hr., oviparous females appeared 7 May and eggs were deposited 22 May. Migrant forms (sexuparae), antecedents of the sexual forms, were artificially

390 WILLIAM ROWAN produced at high June temperatures by shortening the days experimentally. Three species of two genera were employed. Their migration can thus be attributed to the length of day.

VI. PROBLEMS PRESENTED

The basic facts involved in the experiments dealt with in this review are rela- tively simple. It is possible, in a large number of vertebrates with annual breeding seasons normally restricted to spring, to induce activity of the reproductive organs during the winter months by subjecting the animals to days increased in duration by means of artificial light. With many species the opposite effect is obtainable in the spring, i.e. by artificially curtailing the days sexual development may be entirely suppressed. An explanation as to how the effects are brought about is not so simple, and a satisfactory answer has not yet been found.

That the varying state of the reproductive organs depends primarily on seasonal activity of the pituitary gland appears to be established. Atrophy of the sex organs in young and adults follows hypophysectomy while the gonadotropic action of the pituitary has been demonstrated by a large number of authors. Administration of light has no effect on hypophysectomized individuals and it may be taken as established that the pituitary is the organ directly stimulated, while activation of the gonads is indirect and secondary.

Two theories offered in explanation have received particular attention. The one most widely favoured has been that the eye, acting as a light receptor, stimulates the pituitary presumably by a nervous path. Opposed to this viewpoint are the results of various experiments involving the cutting of the optic nerve, destruction of correlated brain centres, covering the eyes with solid blinkers or even completely extirpating them, in which development of the gonads has proceeded at the same rate as in normal controls subjected to similar lighting conditions. The results have led to the further suggestions that the cut optic nerve or the region of the head round the eye are receptors, but no convincing evidence has been forthcoming.

It has also been suggested that the retina of the eye produces a hormone which activates the pituitary. This cannot be the case after the eye has been removed in toto for the retina goes with it.

Attempts to demonstrate light receptors other than the eyes, e.g. the skin, have not been convincing.

The visible rays of the spectrum appear to be the essential element in the illumination. Up to a certain point, apparently that at which full wakefulness is ensured, intensity is important, but augmentation beyond that point appears to be without enhancing or accelerating effect. To induce complete normality in rate of recrudescence and histology of the gonads, gradually increasing increments of daily illumination appear to be necessary. A number of authors have commented on the seemingly significant nature of this requirement (Rowan, Benoit, Whetham, Miyazaki, etc.). Sudden lengthy extensions of the length of day may be effective but generally induce abnormal development or they may prove detrimental or even

Light and seasonal reproduction in animals 39' lead to a noticeable rate of mortality among the birds subjected to them, The temperament of the species used appears to be a consideration of importance.

A second hypothesis, which has received less attention, is that the relative dura- tion of waking to sleeping hours provides the key to the situation, and that the stimulation of the pituitary is effected by changes of metabolism and physiology induced by lengthening the period of diurnal activity.

This viewpoint, the original one put forward, appears still to remain tenable since no method has yet been found of irradiating the eyes of birds with light, accompanied by the simultaneous elimination of wakefulness and its resulting physiological activity. Birds receiving illumination, but sleeping through it, show no sexual development. On the other hand, compulsory wakefulness, mechanically enforced in light below the intensity required to induce sexual development, has been shown to bring about gonadal development in juncos. The only similar experiment (with starlings) is not comparable as these birds showed continued alarm at the treatment, resulting in fright, fatigue and muscular exhaustion. They could not be considered physiologically normal subjects during the course of the undertaking. Starlings roosting in London, in feeble light but receiving constant disturbance from traffic, do actually show winter development of the gonads.

The assumption made by most authors that if the eye is not the functional receptor, other light receptors must in the nature of the case exist, is not necessarily correct. In most of the experiments in which blinded or hooded animals have been used, they have been kept together with untreated controls under identical condi- tions. The controls have been permitted to retain their eyesight and have stayed awake through the allotted period and shown the usual rate of testicular develop- ment. With juncos, a mechanical disturbing device, designed to keep them awake in almost complete darkness, induced normal recrudescence. In the experiments alluded to, normal, unoperated companion birds have in effect been substituted for machinery and provided the disturbing element for the blinded individuals. The question of a light receptor is therefore not necessarily involved at all since the factor of disturbance has been introduced. The point appears to have been totally overlooked by the organisers of the experiments.

Unfortunately the details of the methods of housing are not always included by authors and it cannot be stated whether the above argument applies in all the experi- ments concerned, but it is certainly so in the majority. London starlings provide a comparable series of circumstances, with motor traffic as the source of disturb- ance.

An experiment of Benoit's (1935e) stands out as inexplicable on these grounds, unless the full details of housing were considered to be immaterial and were omitted. He found that ducks with eyes removed, but wearing hoods during illumination, showed no testicular development, yet if the hood were later perforated so that light fell into the sockets, development proceeded in typical manner.

While low intensities of the visible rays are in themselves sufficient to produce the results, Marshall (1936) has demonstrated that ultra-violet may exert an acces- sory effect in ferrets. From what is known of the biological action of ultra-violet

392 WILLIAM ROWAN radiation, this seems to be a reason&le expectation. It appears probable that two different principles are involved.

There are ~ W G complicating factors that enter into many of these experiments. The first is that of rhythms. Birds that do not migrate to or across the equator, and other vertebrates of the northern hemisphere that do not migrate at all and hence are permanently confined to the northern hemisphere, are subjected annually to length- ening days in the spring and shortening ones in the autumn. If their season of reproduction is restricted to the spring and its incidence is primarily dependent on length of day, it would appear to be a reasonable expectation that, if the seasons were artificially reversed, a reversal of the breeding season would be an immediate accompaniment. That this is so in a number of species has now been demonstrated in two ways-by the experimental use of artificial light in sihr in the northern hemisphere : by introduction of northern species into the southern hemisphere, and vice versa. Yet it is quite patent, as was pointed out many years ago (Rowan, 1926), that this simple relationship cannot hold in the m e of trans-equatorial migrants among birds. Such immediate response to the long days of the southern hemi- sphere would be fatal to their scheme of existence which depends essentially on a single breeding season in the spring of the northern hemisphere only. The gonads of such species actuallyremain small during their residence in the south, in spite of long days, not commencing to enlarge till March immediately prior to departure for the north (Rowan & Batrawi, 1938) when the southern days are actually shortening. The reproductive rhythm appears to be fixed and inherent. Yet this is but partially the case for retention of such species in the southern hemisphere, for a period of years can ultimately break it. The subject has been dealt with at length by Marshall (1937), and Baker & Ranson (1938).

Persistence, moreover, may vary with age in a single species. Riley (1936), for instance, has shown that in the sparrow (Passer domesticus), while the young exhibit prompt response to increased illumination in October, adults that have presumably bred, fail to do so till November. This is probably a particular case reflecting exhaustion and associated physiological changes as a result of breeding.

The point obtrudes itself in many of the experiments dealt with in this review that have been carried out in early spring, although its full significance cannot yet be estimated.

The second point of importance lies in the negative results obtained by various investigators and that have been considered by other authors to contradict some of the positive evidence, yet they are not necessarily contradictory. The methods employed by Craig-Bennett (1931), for example, could not have led to positive results with the stickleback. Winter breeding of this fish has actually since been suc- cessfully induced at low temperatures by the use of artificial light differently applied.

It also seems wholly unlikely that animals of tropical orikin, adapted to days of constant length, when imported into the northern hemisphere should show re- actions to light similar to those of northern species. That guinea-fowls, for example (Scott, in Bissonnette 1936c), and guinea-pigs (Dempsey et al. 1933, 1934a, b) have proved wholly negative in this type of experiment, seems to be no reflection on the

Light and seasonal reproduction in animals 3 93 results obtained with animals of the northern or southern hemisphere. A positive response would, in fact, be more unexpected than a negative. The same comments apply to the case of the non-seasonal rabbit (Smelser et al. 1934) and probably to hibernating mammals such as spermophiles (Moore et al. 1934) or aestivating amphibia (Alexander and Bellerby, 1938).

Generalizations on the effects of artificial illumination on the reproductive activities of animals would at present be premature. The response to light condi- tions reflects an adaptation to an environmental factor of the northern hemisphere that would appear to be a necessary condition for survival in the north (or high latitudes in the southern hemisphere). Spring, with its increasingdays, is with most species the appropriate season of reproduction. Many ungulates, with a lengthy period of gestation, must mate in the autumn to ensure birth at spring. The end- product-adaptation to length of day-must inevitably be similar in vast numbers of unrelated species, but the means by which that end i s attained may vary as greatly as the constitutions of the animals concerned. The mode of stimulation of the pituitary by light may prove to be similar in many forms but dissimilarities must in the nature of things be looked for. One feels for instanee, after perusal of the literature with its patchy experimental evidence, that differences have already been shown to exist in the mechanism of ferrets as compared with birds.

VII. ANIMALS INVESTIGATED The following species of animals have been used in investigations into the

effects of artificial illumination on the reproductive processes. (Full reference will be found in the bibliography.)

Mammals (A) Domestic : Ferret, Putorius wukaris. Allanson ; Bissonnette ; Hammond & Marshall ;

Guinea-pig, Camk cutleri. Dempsey, Young, Meyers & Jennison. Rabbit, Lepus cuniculus. Smelser, Walton & Whetham.

Hammond & Walton ; Hill & Parkes ; Marshall & Bowden ; McPhail.

(B) Wild : Field-mouse, Minotus agrestis. Baker & Ranson. Hedgehog, Erinaceas europaeus. Allanson & Deanesly. Raccoon, Procyon lotor. Bissonnette & Csech. Spermophile, 13-lined; Citellus tridecemlineatus. Johnson & Gann ; Moore,

Simmons, Wells, Zalesky & Nelson ; Wells. White-footed mouse, Peromyscus leucopus. Whitaker.

Birds (A) Domestic : Canary, Serinus canarius. Rowan. Ducks, Rouen. Benoit. Other breeds. Parhon & Coban; Shockaert. Fowl, Gallus domesticus. Parhon & Coban ; Whetham.

394 WILLIAM ROWAN Guinea-fowl, Numida meleagris. Scott, as cited by Bissonnette (1936 b). Turkey, M e l e e gallopavo. Scott, as cited by Bissonnette (1936 b).

(B) Wild : Crow, Corvus brachyrhynchos. Rowan. Dove, Mourning, Zenaidura macroura. Cole.

Duck, mallard, Anas platyrhynchos ,,

,, lesser scaup, Nyroca afinis Bell & Rowan. Results unpublished. ,, pintail, A. m t a

,, canvasback, N . valisimia ,, redhead, N. americana

Grouse, ruffed, Bonasa umbellus. Clark, Leonard & Bump. Junco, Junco hyemalis. Rowan. Mejero : white-eye, Zosterops palpebrosa. Miyazaki. Pheasant, Phasianus sp. Bissonnette & Csech; Clark, Leonard & Bump. Quail, Colinus virgihianus. Bissonnette & Csech; Clark, Leonard & Bump;

Redpoll, common, Acanthis linaria. Rowan. ,, hoary, A. hornemanni. Rowan.

Sparrow, American tree, Spizella monticola. Rowan.

Collared, Turtur risorius. Marshall (1933).

I Martin.

,, Harris’s, Zonotrichia p e r d u . Rowan, unpublished. ,,

,, Lincoln’s, Melospiza lincolni. Rowan, unpublished. ,, savannah, Passerculus sandwichensis. Rowan. ,, song, Melospiza melodia. Rowan. ,, white-crowned, Zonotrichia leucophrys. Rowan. ,, white-throated, Zonotrichia albicollis. Rowan.

house, Passer domesticus. Ivanova ; Keck; Kirschbaum & Ringoen ; Miller; Riley ; Ringoen; Witchi & Keck; Rowan, unpublished.

Starling, Sturnus vulgaris. Bissonnette ; Rowan. Tit, great, Parus major. Suomalainen. Weaver finch. Witschi. Whydah. Witschi.

Anolis, Anolis carolinensis. Clausen & Poris (1937). Reptiles

Amphibia Frog, leopard, Rana pipiens. Rowan, unpublished. ,, common, R. temporaria. March.

Newt, Triton cristatus. 1- Prof. Spaul (personal communication). Salamander, Salamandra maculosa. I Toad, clawed, Xenopus laevis. Alexander & Bellerby ; Bellerby ; Shapiro &

Shapiro; Zwarenstein & Shapiro.

L+ht and seasonal reproduction in animals Fish

Catfish, Amerius nebulow. Hoover (personal communication). Trout, Sdvelinus fontinah. Hoover, (1937); Hoover & Hubbard (1937). Minnow, Phoxinus l a e v k SpauL(persona1 communication). Stickleback, Gasterosteus aculeatus. Craig-Bennett.

,, Gasterosteus sp. Prof. Tinbergen (personal communication).

Invertebrates Strawberry louse, Aphis forbesi. Marcovitch.

395

VIII. SUMMARY Some fifty species of animals have provided the material for the investigations

reviewed. The majority have been birds, but mammals, reptiles, amphibia, fish and invertebrates have also been used. A list is provided.

Most of the animals investigated have been species with short breeding seasons restricted to the spring in the northern hemisphere. In their main aspects the results have shown considerable uniformity, exceptions coming primarily from species that normally have no breeding periodicity, such as domestic rabbits, or animals of tropical origin. Species hibernating during the winter, or aestivating in summer, and in their natural state removed from exposure to daylight for several months of the year, have also provided exceptions.

The underlying principle is to be found in the fact that when such periodically breeding species are subjected to artificially lengthened days in the winter or late autumn they can be brought from the sexually quiescent condition characteristic of winter into the breeding condition typical of spring. The basic factor appears to be the length of day to which they are exposed.

The analogous phenomenon in plants has been termed photoperiodism by botanists. A brief review of this phase is given.

Until 1924 the reproductive rhythm in birds was attributed to the rising temperatures of spring, yet in the practice of yogai in Japan, many centuries old, and the induction of the muit in Holland, also going back a long way in history, light had been applied practically to induce winter singing. The underlying principle was unrecognized. Increased egg production in hens through the use of artificial light, first practised a century ago in Spain, is shown to be essentially different from the principle here dealt with.

It may be stated in general that animals (primarily birds) of the northern hemi- sphere, with short reproductive periods, show analogous responses in the following respects :

Days increased to spring duration by means of artificial illumination in mid- winter induce development of the sex organs.

Spring days artificially curtailed to winter length induce regression. Various birds may be brought into breeding condition two or even three times

in a year, but a specific period of rest is required by the organs between one developmental peak and another.

396 WILLIAM ROWAN It has been shown by numerous investigators that the reproductive rhythm

depends on pituitary activity and that upon removal of this organ atrophy of the sex organs follows. The effect of extended lengths of day thus appears to be secondary as far as the gonads are concerned, ceasing after hypophysectomy.

Methods of administering artificial light seem to be important. Small graduated increases result in highly developed organs completely normal in size and histology. Longer increases induce irregularities and premature maturation of the spermatic elements in the testes (of birds) and have, in an extreme case, resulted in a significant rate of mortality in the animals employed (starlings).

Wave-length, beyond certain limits, is of doubtful significance, the visible rays generally being effective provided they are of sufficient intensity.

Intensity, once a certain quite low value has been reached, appears to be of no further significance, and increased intensity, if duration remains the same, has no augmenting effect.

Ultra-violet light, administered in the form of " sun-lamp ", induces develop- ment in birds at the same rate as an ordinary electric light bulb (devoid of ultra- violet) of similar intensity, if given in comparable doses. The case is somewhat doubtfully analogous in mammals.

Temperatures, with birds, appear to be immaterial, but low temperatures in fish may exert a retarding effect.

The most highly favoured theory put forward to account for the observed facts is that light falling on the eye stimulates the pituitary (presumably through nervous channels) which in turn induces gonadal development. Numerous authors believe light, qua light, to be an integral factor in the results obtained. Experiments to determine the issue have. taken the form of blinding the experimental animals either by the use of opaque hoods over the head, or by severance of the optic nerve, or by total removal of the eye, or by lesion of certain nerve tracts of the brain. The results have been largely contradictory and the question remains open.

An alternative viewpoint is that light is concerned only in so far as it provides a means of keeping the animals awake and physiologically active, but is in itself of no further significance, and that increasing diurnal activity, induced by increasing increments of illumination, is the stimulating factor that activates the pituitary. This hypothesis is supported by experiments in which birds (juncos) have been brought to full breeding condition by mechanical disturbance in feeble light far below the intensities required to bring about development when light alone is employed as the agent to induce wakefulness. Also by the fact that when (in the experiments alluded to in the previous paragraph) blinded birds have been kept together with unblinded individuals, the gonads of all have developed at the same rate, yet if the blinded birds are kept by themselves, and then given additional light, development of the organs does not take place. It is suggested that the disturbance forced on the blinded individuals by the unblinded kept with them is, in effect, similar to the mechanical disturbance imposed on juncos. When the source of dis- turbance (unblinded birds) is removed, there is no gonadal demlopment. It may reasonably be assumed that with the eyes removed light can no longer be perceived

Light ond seasonal reproduction in animals 397 and that only disturbance remains as the means of inducing wakefulness over the allotted period of time.

London starlings, roosting in the city nightly in light derived from street lamps below the minimum required to induce sexual development, may attain breeding condition in early February. The birds roost over main traffic thoroughfares and are kept in a state of wakefulness until the theatre crowds have subsided some time after midnight. Traffic disturbance is an undoubted factor in forcing these birds to a daily period of wakefulness beyond normal winter duration.

How far an inherent reproductive rhythm has influenced the numerous expeti- ments involved in this review is open to question. It has been shown with more than one species that if the animal be kept on a short length of day into the spring, a small increase of the gonads occurs nevertheless and evidently reflects an incipient rhythm independent of the immediate effects of length of day. Little is known of this factor but its presence has been demonstrated on various occasions and may add greater significance to the time of year at which experiments are undertaken.

Adaptation to light conditions, of such profound importance in the matter of successful reproduction, appears to be the keynote to reproductive cycles in the northern hemisphere. Wholly unrelated animals have inevitably developed similar reactions. The method by which such adaptations have become established in various groups or species is, however, not necessarily the same, and generalizations, in our present state of knowledge, may be entirely fallacious.

The writer is very greatly indebted to Professor J. P. Hill, F.R.S., for extending to him the hospitality of his Department during his residence in England, where this article was written, and making it possible for him to use the extensive library and other facilities of University College, London.

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ADDENDUM

Papers with direct bearing on the subject of light and reproduction that have appeared since the above article went to press have been incorpoiated in the list of references The most notable is Benoit’s (1937), which deals at length with the viewpoint that the! complete removal of the vertebrate eye or destruction of the optic nerve do not affect the issue (stimulation of the pituitary) since the author believes that the administered light is capable of penetrating the tissues of the head and bones of the skull and so reaching the pituitary gland directly (or at least the hypothalamus) without the intermediation of

27-2