J . Zool., Lond. (1967) 151, 17-25

Interspecific differences in photosensitivity between three closely related species of pigeons

B. LOFTS

Department of Zoology and Comparative Anatomy, St. Bartholomew's Hospital Medical College, University of London, E.C.1

R. K. MURTON A N D N. J. WESTWOOD

Tangley Place, Worplesdon, Surrey Ministry of Agriculture, Fisheries and Food, Infestation Control Laboratory,

(Accepted 4 August 1966)

(With 1 plate in the text)

It is known from field observations that vernal gonad recrudescence begins in January for the Stock dove, a month later at the end of February for the Wood pigeon, while many town pigeons (Columba livia) have active gonads throughout the year.

Photostimulation experiments demonstrate that spermatogenesis can be stimulated in the Stock dove by exposure to an artificial daylength regimeincreasing from 9.1 to 10.8 hours over 28 days. This photoperiod is the approximate equivalent of natural daylength changes occurring from late January onwards at 52" N. The same phototreatment, however, was not stimulatory for the testes of Wood ,pigeons, which required the equivalent of a March photoperiod. Natural daylength changes occurring in late November and December failed to evoke gametogenetic recovery in Stock dove controls.

The gonads of feral pigeons in full breeding condition were unaffected when the subjects were transferred from full summer photoperiods to those found in midwinter and spermato- genesis was maintained in birds kept under winter daylengths for four months.

The discussion mentions the problem of intraspecific geographical variation in photo- sensitivity. Scottish Wood pigeons begin their gonad recovery earlier and by March have considerably larger testes than birds in the south of England. Furthermore, they achieve this more advanced condition before the vernal equinox when daylengths are shorter in Scotland than in the south of England.

Contents Page

Introduction . . . . . . . . . . . . . . . . . . . . .. 17 Materials and methods . . . . . . . . . . . . . . . . .. 18 Results . . . . . . . . . . . . . . . . . . . . . . 20 Discussion . . . . . . . . . . . . . . . . . . . . . . 22 References . . . . . . . . . . . . . . . . . . . . .. 25

Introduction

In a recent contribution to this journal (Lofts, Murton & Westwood, 1966) we showed that under natural conditions the Stock dove Columba oenas commences gonad recrudes- cence in January almost two months earlier than the closely related Wood pigeon C.

17

18 B. LOFTS, R. K. M U R T O N A N D N. J. W E S T W O O D

palimbus. The Stock dove consequently has a longer potential breeding season than the Wood pigeon and it was shown that this was correlated with a longer season during which young could be produced. The wild Rock dove C. livia at Flamborough possibly had an even longer physiological breeding season, while a high proportion of the feral pigeon C. h i u populations of Leeds and Liverpool stayed in full reproductive condition through- out the year.

In the case of the Wood pigeon we have demonstrated experimentally that outside the normal breeding season wild caught birds with regressed gonads can be photostimulated back into breeding condition by exposure to summer daylengths (Lofts, Murton & Westwood, in press). Furthermore, there appears to be no period of postnuptial refractori- ness when the pituitary is insensitive to photostimulation.

From the above observations it was reasonably certain that the physiological breeding seasons of these three Columbids could be accounted for in terms of a differential sensitivity to photostimulation and it remained to test this experimentally. Accordingly, male Wood pigeons and Stock doves with regressed testes were submitted to artificial light regimes, comparable with those experienced in the wild, at the time of the first gonad recrudescence, while some additional photostimulation experiments were undertaken with feral pigeons. In making these studies we were conscious of Marshall’s (1959) statement that “it is true, however, that no photo-experimentalist has yet influenced the sexual cycle of any vertebrate with an additional light-ration as small as that which must be influential in nature if, as seems probable, daylength is the primary accelerating factor in most birds of the north temperate zone”.

Materials and methods Subjects were 11 Stock doves and 12 Wood pigeons collected from a study area at Carlton,

Cambridgeshire and 30 feral pigeons taken from laboratory stocks maintained at Tangley Place. All birds were adult males.

Stock doves. 8 Stock doves were caught with stupefying baits on their feeding grounds in June 1965, 1 in February 1965 and 2 were stupefied on their nests in the late summer of 1965. All were kept in outside aviaries until 18 November 1965, when they were sexed by an exploratory laparotomy under nembutal followed by ether anaesthesia. At this stage a few females taken in the original samples were discarded. A unilateral incision made between the eighth and ninth ribs was retracted to reveal the left testis. The size of the organ was estimated in situ. After suturing, healing was rapid within about 4 days. The subjects were divided into 2 groups as follows: 5 birds were left in outside flights experiencing natural photoperiods from 22 November until 16 December when they were killed, the testes dissected out measured and fixed for histological examination. These birds received a total of 229 h of daylight, excluding approximately another 29 h of twilight. 6 other birds were kept indoors in an unheated basement for 29 days from 22 November to 16 December and were subjected to an artificial light regime approximating to the sunrise and sunset times experienced in February at 52” N, but with no allowance for civil twilight (Table I). The time clock controlling the fluorescent lighting used was adjusted every Thursday and Monday. These birds received a total photoperiod of 280 h until they were killed on the 29th day.

Woodpigeons. These were caught with stupefying baits in early January 1966 and were laparo- tomized on 17 January, when testicular size was estimated in situ. 6 birds were kept under exactly the same light conditions as the artificially photostimulated Stock doves mentioned above from 24 January until 21 February, being maintained on natural daylengths from the time of capture

D I F F E R E N C E S I N P H O T O S E N S I T I V I T Y I N P I G E O N S 19

until the experiment started. 6 other birds were given a photoperiod equivalent to that occurring in March (minus civil time) again from 17 January to 21 February (Table I). All subjects were killed on the 29th day of the experiment and their gonads fixed.

Feralpigeons. 16 males were taken from outside holding aviaries and were Iaparotomized on 27 August 1964. All had large testes typical of birds in full breeding condition. They were then kept indoors on a 16 h photoperiod until 31 December when 6 birds were killed and their testes fixed. The remainder were laparotomized and their gonads examined in situ. 5 were then kept

TABLE I

Photoperiods employed during experiments with Stock doves arid Wood pigeons

Natural outdoor photo- period experienced by 5 Artificial photoperiod

Stock doves from 22 given to 6 Stock doves November-20 December from 22 November-20 Artificial photoperiod 1965 omitting twilight and December 1965 and 6 given to 6 Wood pigeons based on times of sunrise Wood pigeons from 24 from 24 January-21

Day time-clock and sunset (G.M.T.) January-21 February 1966 February 1966 adjusted h min h min h min

1 4 8

11 15 18 22 25 29

Total photoperiod including 2 h for the day when birds killed

8 34 9 6 8 26 9 17 8 16 9 30 8 10 9 46 8 2 10 1 7 59 10 16 I 53 10 32 I 51 10 52

229 h 280 h All subjects killed about 10.00 h

258 h allowing 1 h per day for twilight

10 53 11 4 11 20 11 32 11 48 12 0 12 16 12 28

329 h

Notes: (I) There was no time-clock change for birds kept under natural daylength at 52" latitude and the figures represent the total photoperiod between sunrise and sunset over the 28 days of the experiment.

(*) This photoperiod corresponded to the sunrise and sunset times found in February at 52" latitude. Allowing for twilight it would correspond approximately with the natural photoperiod found from late January onwards.

(9 This photoperiod corresponded to the sunrise and sunset times found in March at 52" latitude. AlIowing for twilight it would correspond approximately with the natural photoperiod found from late February onwards.

in outside flights experiencing natural photoperiods until 17 February 1965 when they were killed, that is they were transferred while still in breeding condition from warm indoor conditions with summer daylengths, to outside winter conditions for 1.5 months. The remaining 5 birds were kept indoors on a 16 h photoperiod until 17 February.

A separate batch of 14 males was selected from an outside holding flight on 9 April 1965 when the birds were laparotomized. 2 were killed immediately as controls. The remainder were maintained in an indoor basement on a winter photoperiod of 8 h. 2 were killed on 22 June

20 B. L O F T S , R. K. M U R T O N A N D N. J. W E S T W O O D

and the remainder laparotomized and their gonads measured in sifu. They were then used for some further experiments not entirely pertinent to the present paper, although the results will be mentioned briefly.

All testes were fixed in Bouin's fluid and were then wax embedded and sectioned at 4 p. Sections were stained with iron haematoxylin and counterstained with orange G to reveal the spermato- genetic condition.

Results

Stock dove. All the Stock doves had small testes typical of winter regressed birds, when they were laparotomized on 18 November (Table 11). The testes of the five individuals

T A B L E I1

Efect of tt('o different e.uperirnerrtal photoperiods * 011 the testes of the Stock dove

Estimated size Size of of left testis left testis

Ref. on 18 Nov. on 20 Dec. Histological condition of no. (mm) (mm) testis when killed

Group 1

Kept in outside flights under natural daylength from 22 Nov. to 20 Dec. Total photoperiod about 258 h

Group 2 Given total

photoperiod of 280 h from 22 Nov. to 20 Dec. in indoor cages

1

2

3 4 5

6 7 8 9

10

1 1

1 1 .o ?( 2.0

10.0X2~0

9.0 x 2.0 8.0 >: 2.0 8.0 x 2.0

9.0 x 2.0 8.0 x 2.0 9.0 x 2.0 9.0 x 2.0 7.0 1.0

8.0 x 2.0

7.5 ;< 2.0

8.0 x 1.5

7.0 x 2.0 8.0 x 2.0 6.0 x 2.0

No primary spermatocytes but mitoses of spermatogonia

Few spermatogonia with mitotic figures in isolated tubules

Resting spermatogonia only Resting spermatogonia only Resting spermatogonia only

9.5 x4-5 Secondary spermatocytes present 8.0 x4.5 Secondary spermatocytes present 8.0 x 4.5 Secondary spermat ocyt es present 8.0 x4.5 Spermatids common 7.5 x4.0 Numerous primary and some

secondary spermatocytes 9.0 x4.5 Numerous primary and some

secondary spermatocytes

* See Table I for exact details of photoperiods given to these birds.

kept on a natural photoperiod during late November to December had not changed appreciably in size by 20 December, any differences, if they were valid, indicating some further regression over the period. Histological examination revealed that the testes of four birds were in a typical winter resting condition when examined, the tubules being at minimum diameter with a single layer of inactive spermatogonia. One bird was slightly more advanced, and some tubules contained spermatogonia undergoing mitotic division, though no primary spermatocytes had been formed (Table 11).

PLATE I-See caption opposite. %o face page 211

D I F F E R E N C E S I N PHOTOSENSITIVITY I N P l G E O N S 21

In contrast the six birds given the equivalent of late January/early February daylengths had all begun gametogenetic recovery and testis diameter had approximately doubled. Five birds had developed numerous primary spermatocytes and a few secondary spermato- cytes and the sixth had attained numerous spermatids (Plate I(a) and Table 11).

It is worth pointing out that the size of a testis, a character that has often been used in the past, is not always a reliable indicator of its gametogenetic activity. In particular,

TABLE I11

Efect of two &yerent experimental photoperiods * on the testes of the Wood pigeon

Estimated size Size of of left testis left testis

Ref. on 17 Jan. on 21 Feb. Histological condition of no. (mm) (mm) testis when killed

Group 1 1 12.0 x 2.0 6.0 X 2.0 Resting spermatogonia Given total 2 10.0 x 2.5 10.0 X 2.5 Resting spermatogonia

photoperiod of 3 10.0 x 2.0 6.0 X 2.0 Resting spermatogonia 280 h from 4 8.0 X 2.0 6.0 x 2.0 Few primary spermatocytes 24 Jan to 21 Feb. 5 7.0 x 1.0 6.0 X 2.0 Resting spermatogonia in indoor cages 6 6.0 x 2.0 6.0 X 2.0 Resting spermatogonia

Group 2 7 12.0 x 2.0 15.0x4.0 Secondary spermatocytes Given total 8 8.0 x 1.0 14.0 x 4.5 Few spermatozoa

photoperiod of 9 10.0 x 2.0 10.0 X 4.5 Numerous spermatids 329 h from 10 10.0 x 1.0 8.5 x 2.0 Primary spermatocytes 24 Jan. to 21 Feb. 11 8.0 x 2.0 8.5 X 3.0 Few secondary spermatocytes in indoor cages 12 10.0 x 2.0 10.5 x3.5 Few spermatids in isolated

tubules

* See Table I for exact details of photoperiods given to these birds.

small testes have often been described as resting or inactive, though this need not always be the case. The data in Table I1 demonstrate that a small testis (8-0 x 4.5 mm) can some- times be spermatogenetically well advanced and producing spermatids, though this is exceptional. However, under natural environmental conditions gonad size generally gives an approximate indication of spermatogenetic activity, especially during the times of maximal size achievement.

Wood pigeon. Although vernal recrudescence was well under way in those Stock doves which were given a total photoperiod of 280 hours, Table 111 shows that the Wood pigeons were unaffected by the same amount of photostimulation. Six birds had mean gonad dimensions of 6.7 x 2.1 mm (length and breadth) on 21 February which was less than

PLATE I. (a) Testis of Stock dove, Colurnba oenas, kept under a February photoperiod. Spermatogenesis is well advanced and spermatids can be seen in the seminiferous tubules. (b) Testis of Wood pigeon, C. palurnbus, kept under the same February photoperiod as the Stock dove shown in (a). The seminiferous tubules are still regressed and spermatogenetically inactive. (c) Testis of a feral pigeon, C. Zivia, kept under a winter photoperiod. The seminiferous tubules are in full breeding condition.

22 B. LOFTS, R. K. M U R T O N A N D N. J. W E S T W O O D

when they were collected from the field on 17 January (8.8 x 1.9 mm). One bird had begun spermatogonial division, but the other five all had regressed testes, typical of winter birds (Plate I(b)), with inactive spermatogonia. Six birds subjected to the equivalent of a natural February/March photoperiod for 29 days (total photoperiod 329 hours) had all begun spermatogenesis most having passed the primary spermatocyte stage (see Table 111). Feralpigeans. All the 16 males examined on 27 August 1964 had testes at or near their

maximum size. This was also the case after the birds had been held on a 16 hour photo- period until 31 December, when ten of them were again laparotomized and mean gonad size estimated in situ at 23.4 x 10.7 mm. Six birds were autopsied and had testes averaging 20.2 x 8.8 mm in length and breadth (range of five birds 24-5 x 12.0 to 19.5 x 8.0 mm omitting one bird mentioned below). Histological examination of the gonads of these six birds revealed that all but one were producing spermatozoa, though secondary spermato- cytes were numerous relative to sperm numbers in some tubules. The sixth bird had just begun spermatogenesis and had produced only a few primary spermatocytes. Its larger testis measured 14.5 x 5-0 mm (included in average given above for the six birds).

The five birds transferred from a summer photoperiod on 31 December and kept in outside flights under natural winter seasonal conditions still had large testes when they were killed on 17 February (mean 21-4 x 9.3 mm). All five had numerous spermatozoa when their gonads were examined histologically (Plate I(c)). In fact, the tubule lumina were blocked with undischarged spermatozoa from a previous generation and a further wave of sperm was being produced in many tubules. The condition of the gonads did not differ from that of the five other birds kept indoors on a 16 hour photoperiod until 16 February, except that in these the tubule lumina appeared less blocked with spermatozoa. Mean gonad size in these birds was 23.4 x 10.7 mm.

In the second experiment with feral pigeons mean testes size of the 14 birds taken from outside holding flights and laparotomized on 9 April 1965 was estimated at 21.9 x 7.5 mm. Two 3f these birds which were killed and their gonads sectioned were producing masses of spermatozoa. The larger left gonads of these two birds measured 2 4 . 0 ~ 11.0 and 21.0 x 9.0 mm. After 2.5 months on a winter photoperiod the remaining 12 birds still had testes averaging about the same size (23.7 x 8.9 mrn) while two specimens which were killed for autopsy were producing masses of spermatozoa, and had the larger left testes measuring 25.5 x 10.0 and 2 4 . 0 ~ 15.0 mm. It is worth mentioning in passing that the remaining birds were then given various doses of prolactin until they were killed between 2 to 18 August. Prolactin is known to have antigonadal properties (Lofts & Marshall, 1958) but even following this treatment gonad size was unaffected (mean testis size of five birds remaining on 18 August was 23.5 x 11.4 mm) and all were still producing spermatozoa (unpublished work, in progress).

Discussion

The results demonstrate that three closely related pigeon species, living at about the same latitude, have evolved different levels of sensitivity to light stimulation. As a result the same seasonal changes in the natural photoperiod can stimulate the pituitary in the three species at different times of the year and so mediate gonad development at appropriate seasons.

In the Stock dove spermatogenesis could be initiated with a daily photoperiod of 9 hours

D I F F E R E N C E S IN PHOTOSENSITIVITY I N PIGEONS 23

increasing to 11 hours over about one month, a photoperiod naturally experienced from late January onwards at 52" N. This finding agrees very well with the time of vernal gonad recovery recorded for birds living under natural conditions, (Lofts, Murton & Westwood, 1966). Stock doves as would be expected, could not be stimulated by a winter photo- period decreasing from 84 to approximately 8 hours over one month, and it is not, there- fore, surprising that wild birds have regressed gonads from November until late January. Wood pigeons were not stimulated by a photoperiod sufficient to cause spermatogenesis in Stock doves and required daylengths of nearly 11 hours increasing to 126 hours over one month before their gonads would respond. This agrees with field observations that gonad recrudescence in the Wood pigeon does not occur until late February and through- out March. Thus 280 hours of light given over 29 days could stimulate Stock doves but not Wood pigeons, which were stimulated by another 49 hours of light over the same period. Feral pigeons were not affected by exposure to natural midwinter daylengths and remained in full breeding condition. Even the sudden transference from a full summer photoperiod at indoor temperatures (about 20°C) to midwinter daylengths and temperatures in outside flights caused no gonad regression whatsoever. Again the finding agrees with the fact that adult feral pigeons living in the cities of Leeds and Liverpool remain in breeding condition throughout the year (Lofts, Murton & Westwood, 1966) but whether daylengths even shorter than those experienced in nature would be detrimental is not known. Dunmore & Davis (1963) have noted that apparently adult feral pigeons in Pennsylvania, U.S.A. at 40" 48' N also had fully active gonads throughout the winter 1961 to 1962 when mean temperatures ranged from -1.5 to -3.5"C in the December to February period. Schein (1954) also demonstrated winter breeding for the feral pigeon in Baltimore, Maryland.

Colquhoun (1951) measured the testis size of Wood pigeons collected in Oxfordshire and in Aberdeenshire and found that Scottish birds had larger testes than those of the Oxfordshire birds at the start and end of the season. Thus 20 birds collected in Oxfordshire in February 1944 had testes with a mean volume of 37 mm3 and this compares with a mean of 23 mm3 for 163 birds taken in the Carlton study area over the years 1959 to 1964 (data for Carlton summarized in Lofts, Murton & Westwood, 1966). In contrast nine Scottish birds averaged 193 mm3, a mean volume not achieved until March at Carlton. Colquhoun also produced evidence that autumn regression occurred later in the season in Aberdeen- shire. Some further unpublished records obtained by Colquhoun in 1943 covering Oxford- shire and parts of Scotland are given in Table IV and compared with summarized records from Carlton for the 1959 to 1964 period extracted from Lofts & Murton (1966). There are certain drawbacks in the data, for example, the wide range of gonad sizes recorded in Oxfordshire suggests that some first-winter birds were not being identified and were being included. Nevertheless, it seems reasonable to conclude that gonad recovery occurs earlier in Scotland than in England. If Scottish Wood pigeons display the same response to daylength changes as do English birds an increased photoperiod should only have manifestations after the vernal equinox on about 21 March. Thus by responding more in February and for most of March Scottish birds were reacting to a lower level of photo- stimulation than that experienced in England. The discrepancy could be explained if Scottish birds were subjected to other more favourable accelerating factors than the English birds. Thus it is known that high temperatures, and temperature increases, good food supplies and bright weather can accelerate gametogenesis in Wood pigeons, while

24 B. LOFTS, R. K. M U R T O N A N D N. J. WESTWOOD

sudden cold spells and low temperatures conversely retard gametogenesis. But wide variations in these factors in the Carlton study area in different years did not result in such big difference as those recorded between birds from Scotland and England (Lofts & Murton, 1966). The alternative explanation is that birds in Scotland have a lower threshold of sensitivity to a given photoperiod. There is, of course, no reason why local populations should not evolve characteristic differences in photosensitivity in the same way as has been done by closely related species, and such differences would be expected in species inhabiting a wide range. The acquisition of locally adapted photoresponses would require birds to stay in or to return to the same general area for breeding, a situation generally true for Aves. It would be of interest to know the range of sensitivity to a given photoperiod shown by birds reared in the same area, assuming that the mechanisms

TABLE IV Mean volume of lefr testis in mma of Wood pigeons collected in different areas

Oxfordshire 1943 Scotland 1943 Carlton, Cambs. 1959-1964 Mean Range2 Mean Range Mean Range3

February 114(7) 13-377 475(4) 149-755 23(163) 18-59 March 428(31) 47-942 695(17) 348-1190 136(116) 58-302 April 750(18) 45-1232 955(11) 737-1178 450(88) 273-806

Notes : (l) Specimens were collected in Roxburgh, Haddington, Linlithgow, Stirlingshire, Perthshire, Morayshire

(*) The ranges given for these figures refer to different individuals.

(3) The ranges given for these figures refer to the range in means experienced in different years. (Data for Oxfordshire and Scotland from Colquhoun unpublished, data for Carlton from Lofts & Murton, 1966.)

and Aberdeenshire.

causing characteristic photoresponses are inherited, and to what extent selection has to operate to maintain the typical local pattern. It is also of interest to speculate on the role of a specific photoresponse in ensuring that birds return to appropriate latitudes to breed. The importance of another kind of light sensitivity for navigation and homing is well documented and the two mechanisms could be intimately related via the little understood neural-pituitary complex.

Baker (1938) found that, in general, the breeding seasons of a wide range of bird species were later at higher latitudes. The Wood pigeon could be an exception although it should be remembered that a physiological ability to breed and actual egg-laying are not the same and other factors are involved in finally stimulating breeding in this species (Murton, Isaacson & Westwood, 1963). However, if Wood pigeons have a longer physiological breeding season in Scotland this implies that selection has favoured the production of offspring over a longer period than in the south, otherwise there seems no reason why the physiological breeding season should not also be longer in the south if no disadvantages exist. Threadgold (1960) found no orderly retardation of the gonad cycle in the House sparrow Passer domesticus at more northern latitudes but he considered that geographical variations in sunshine and temperature were having a very pronounced affect and were modifying the direct photoresponse.

D I F F E R E N C E S I N P H O T O S E N S I T I V I T Y IN P I G E O N S 25

There are considerable differences in the maximum size normally achieved by the testes of the three pigeon species when in full reproductive condition. The feral pigeon has the largest organs, the mean testis size achieved by seven birds in full breeding condition measured during this study was 22-4 x 9.6 equivalent to a volume of 1081 mm3. Two wild Rock doves from Flamborough in July averaged 1236 mm3 and seven birds in August averaged 891 mm3. Twenty-nine Stock doves in June and July averaged 733 mm3 while 220 Wood pigeons in July and August averaged 798 mm3 (all data re-analysed from Lofts, Murton & Westwood, 1966). All birds were actively producing spermatozoa and were in full breeding condition. Allowing for differences in body weight (Wood pigeons average about 500 g, while Rock and Stock doves range between 300 to 350 g) it is clear that relative gonad size is greatest in the feral pigeon, decreases in the Rock dove and Stock dove and is least in the Wood pigeon. This sequence follows the same order in which these species show sensitivity to light stimulation. It may be conjectured that the gonads of feral pigeons are largest because this species responds more readily to short photo- periods so that the pituitary is stimulated to produce gonadotrophic hormones to a proportionately greater extent than in the other species.

R E F E R E N C E S

Baker, J. R. (1938). The relation betweenlatitude and breeding seasons in birds. Proc. zool. SOC. Lond. 1 0 8 ~ : 557-582. Colquhoun, M. K. (1951). The Woodpigeon in Britain. London: H.M.S.O. Dunmore, R. & Davis, D. E. (1963). Reproductive condition of feral pigeons in winter. Auk 80: 374. Lofts, B. & Marshall, A. J. (1958). An investigation of the refractory period of reproduction in male birds by means

Lofts, B. & Murton, R. K. (1966). The role of weather, food and biological factors in timing:the sexual cycle

Lofts, B., Murton, R. K. & Westwood, N. J. (1966). Gonadal cycles and the evolution of breeding seasons in

Lofts, B., Murton, R. K. & Westwood, N. J. (In press.) Photoresponses of the wood-pigeon Columba palumbus

Marshall, A. J. (1959). Internal and environmental control of breeding. Ibis 101: 456478. Murton, R. K., Isaacson, A. J. & Westwood, N. J. (1963). The food and growth of nestling wood-pigeons in relation

Schein, M. W. (1954). Survival records of young feral pigeons. Auk 71: 318-320. Threadgold, L. T. (1960). A study of the annual cycle of the house sparrow at various latitudes. Condor 62: 190-201.

of exogenous prolactin and follicle stimulating hormone. J. Endocr. 17: 91-98.

of the wood-pigeon. Br. Birds 59: 261-280.

British Columbidae. J. Zool., Lond. 150: 249-272.

in relation to the breeding season. Ibis.

to the breeding season. Proc. zool. SOC. Lond. 141 : 747-182.

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