British Birds

Vol. 61 No. 10 OCTOBER 1968

Breeding biology of Rock Doves By R. K. Murton and S. P. Clarke Ministry of Agriculture, Fisheries and Food Infestation Control Laboratory, Worplesdon, Surrey

INTRODUCTION Just over twenty years ago Lees (1946) published an account of the breeding of Rock Doves Columba livia on the Cromarty coast of Scot­ land. He showed that eggs could be laid in every month of the year, giving the species the distinction of having the most extended breeding season of all British birds. Nevertheless, he did find that any particular 'doo-cave' (the Scots name for pigeon caves from which the young are farmed) would be unoccupied by breeding Rock Doves for short periods in the year; assuming that established breeders normally remain faithful to their nesting places, this suggested that each individual has spells of inactivity. Further evidence that this might be the case was provided by Lofts, Murton and Westwood (1966), who examined the histological condition of the gonads of a sample of Rock Doves shot throughout the year around Flamborough Head, Yorkshire. Most of these had inactive gonads at some time after the main summer breeding period, but this inactivity lasted only about two months. Moreover, because the onset of gonad regression was not synchronous throughout the whole population, it was evident that eggs could be found in all months to give the appearance of a continuous breeding cycle. A few individuals, however, did seem to possess the capacity for true con­ tinuous breeding, though their testes assumed a characteristic appear­ ance more typically seen in town populations of feral pigeons. Con­ tinuous breeding seemed to be more often associated with melanic morphs than with individuals displaying typical wild Rock Dove plumage characters. Hence it seemed likely that, in coastal Rock Dove populations, the apparent manifestation of a continuous breeding season might have been partly the result of an asynchronous pattern of post-nuptial gonad regression, and partly caused by individuals show­ ing evidence of a past domestication (Lees recorded such birds in the

429 BRITISH BIRDS population he studied). The present investigation was initiated at Flamborough Head, Yorkshire, to obtain more accurate information on the egg-laying season, the factors influencing it and the success of breeding: first, in order to help understand the processes involved in the evolution of continuous breeding as manifested by town pigeons; and second, to compare with our studies of the other British species of pigeons. Arguments about what constitutes a wild Rock Dove are to a large extent semantic. The Rock Dove, like the House Sparrow (Summers- Smith 1963), probably spread to Britain in the wake of neolithic man (Goodwin 1955) and has doubtless been exploited by human beings in one way or another since the earliest ages. Certainly it was common practice by Norman times to erect platforms in the dove caves to facilitate the collection of squabs for immediate eating or for stocking the manorial dove-cotes. So-called wild populations of Rock Doves in, for example, the Faeroe Islands (Salomonson 1935, Petersen and Wil­ liamson 1949) produce melanic morphs which, because they are deter­ mined by a dominant gene, would spread in the absence of strong selection against them. If there are no restrictive conditions, melanism is enabled to spread and town populations possess a high proportion (70% +) of such morphs (Lofts, Murton and Westwood 1966). It is important, therefore, to appreciate that town pigeons are not chance collections of individuals recently escaped from captivity, but instead are composed of those birds best fitted ecologically to occupy the urban niche. This does not imply that man-made effects of selective breeding, such as enlarged ceres, a pouter shape, feathered feet and so on do not appear in town populations, but they are selected against. Similarly, albinos, which are popular in captivity, represent only a very small proportion of town flocks and they can be shown to have a much lower survival than such melanic morphs as the various chequers. In contrast to their dominance in urban conditions, melanic morphs seem to be at a selective disadvantage in coastal areas (Petersen and William­ son 1949). 'Wild' coastal populations of C. livia are comprised pre­ dominantly of birds with wild-type characters. The proportion of wild-types varies from such areas as Flamborough Head where they form over 70% to remote cliffs in the north-west Highlands of Scotland where it is unusual to find any other type. To some extent, this variable proportion depends on the amount of past and present contact and interchange with town populations near-by or with the passage of racing birds, but probably also on local ecological conditions. This preamble has been intended to emphasise that so-called Rock Doves living at Flamborough Head are subject to strong selection, which ensures that they at least behave ecologically like a genuine wild line (Murton and Westwood 1966). It would be pedantic, therefore, to argue that this study is not pertinent to genuinely wild Rock Doves

430 BREEDING BIOLOGY OF ROCK DOVES simply because some individuals have dirty grey instead of pure white rumps (see also page 446). It is extremely likely that the Rock Dove in Britain has been influenced by agriculture since at least Roman times and it becomes difficult to draw the line between fully wild and fully feral stocks. The important point to appreciate is that the Rock Doves at Flamborough Head, as anywhere else, represent a dynamic popula­ tion just as dependent on, and adapted to, their environment as any other animal.

METHODS Many of the 'cliff' pigeons at Flamborough Head live on the inaccessible (at least as far as we were concerned) cliffs of Speeton, Bempton and Flamborough, roosting on the cliff face in natural fissures and small caves. These same cavities are also used for breeding, the doves often nesting behind Guillemots Una aalge, Razorbills Alca torda and Kittiwakes Rissa tridactyla. Few of the caves are easily entered, but we were able to make reasonably regular visits to one of them. Neverthe­ less, access could be gained only at low water on neap tides and some­ times North Sea gales made even these tide conditions impossible; this was the case from December to February in both years of study. Fortunately, some of the Flamborough Head Rock Doves nest in a disused beacon tower and we were able to arrange for this to be visited at regular fortnightly intervals from February 1965 to May 1967, while we also installed a new padlocked door to prevent superfluous dis­ turbance. (The age of the present tower is uncertain: probably it was built in the 18th century, but records suggest that a beacon has been present on the site since as early as 1400, possibly giving the village its former name of 'Flameburgh'; it is likely that Rock Doves have been associated with the site over a long period.) Whether they live on the cliffs or in the tower, the Rock Doves must flight inland to feed on the surrounding agricultural land and so there are no differences between the two groups, except in their choice of nesting or roosting sites. The diet of the Rock Doves at Flamborough Head has already been defined (Murton and Westwood 1966). During the fortnightly visit (if the cave was accessible, it was visited on the same day as the tower) a systematic search was made for nests and all those found were marked and plotted and their contents documented. Nests were located on the four floors of the tower, on the old connecting stairways and, in a few cases, on window sills or in old fireplaces; virtually all possible sites were utilised at some time. It was difficult to overlook nests, but care was taken to account for all pre­ viously numbered nest-sites. Further, because the same observers made consistent and regular visits, the records are free from many of the biases inherent in this kind of study. Thus, although breeding success estimation may be slightly exaggerated in favour of success, because

43i BRITISH BIRDS eggs laid just after a visit may have been lost before the next fortnightly visit, the error is judged to be small. In order to examine the diet of nestlings, samples of young Rock Doves were collected. We purposely chose nestlings that we judged to be nearly ready to fledge or, in most instances, were able to catch young which had just left their nests and were wandering about the tower or cave. In such cases the young were regarded as having fledged success­ fully so far as the estimation of breeding success was concerned. We were anxious not to interfere too much with the normal biology of the Rock Doves and so restricted our sample size as much as possible. As will be shown, it is unlikely that these activities interfered with the main conclusions of the work and they added considerably to our apprecia­ tion of the factors governing the normal breeding season.

Jon Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec FIG. I. Breeding season of Rock Doves Columba livia at Flamborough Head, Yorkshire, based on the percentage of clutches (392 in all) laid in each month of the year

BREEDING SEASON Visits to either site were not frequent enough to do more than confirm the incubation and nestling periods given in The Handbook of British Birds (Witherby et al. 1939-41). Similarly, our records do not materially add to information contained in The Handbook regarding nest sites or nest materials. Cave nests often incorporated grass and twigs collected inland, but rarely jetsam or other shore debris. Tower nests were usually little more than unlined scrapes in the droppings and other soilings that had accumulated on the floors. It was noticeable, however, that winter nests built from November to March, and especially those built in December and January, often contained much more nesting material and were sometimes even lined with finer grasses and detritus.

432 BREEDING BIOLOGY OF ROCK DOVES Table x. Percentage of eggs laid and young fledged to each month by Rock Doves Columba livia in the tower site at Flamborough Head, Yorkshire The total of eggs laid ot young fledged is given in brackets at the head of each column FEBRUARY I965-JANUARY 1966 FEBRUARY I966-JANUARY 1967 Percentage of Percentage of Percentage of Percentage of eggs laid young fledged eggs laid young fledged (370) (i44) (395) ("3)

February *% 0% *% 5% March *% 0% 9% 4% April 16% 3% «% 8% May "% w% 17% 5% June 7% 15% 10% 22% July 6% 3% . 6% 0% August 17% 6% ' 13% 15% September 16% 19% 17% 6% October 4% 18% *% n% November 10% 13% 8% 17% December 3% 10% 1% 7% January 6% 3% 3% 0%

It is not known whether thermal insulation was more important at this time, but it is difficult to find other explanations for this seasonal change in nesting habit. Fig. 1 illustrates the seasonal percentage distribution of laying for the period from February 1965 to December 1966 combined and is based on 75 5 eggs ^4. or 392 clutches (only 29 eggs were found in single-egg clutches). Table 1 gives details for the two years separately, running the years from February to January because no records were collected in January 1965. Although eggs were laid in all months of the year, it is apparent that the majority of the Rock Doves were more seasonal and were probably restricted to the March-November period. The first peak of laying was more sharply defined in 1965, occurring in April, than in 1966 when breeding began rather earlier but was less syn­ chronised. In both years egg-laying declined noticeably after Novem­ ber, which is the time of gonad regression for most Rock Doves (Lofts, Murton and Westwood 1966). A better way of appreciating the breeding season pattern is to con­ sider the number of occupied nests present on each visit to the tower, as that method also enables an estimate of the breeding population to be made if it is assumed that this is indicated by the maximum density of occupied nests. The assumption is probably reasonably justified with this species, because the adults can produce repeat clutches in about seven days. It is likely that, at any visit, less than 10% of the breeding pairs were not represented by eggs or young, assuming that once a clutch is laid its chances of being taken on any particular day stay constant and are around one in a hundred. (Table 3 on page 437 shows that 20% of eggs are predated and so, if a hundred clutches are laid,

433 BRITISH BIRDS

2 3 O 14 14 7 I 3 I 7 I 26 5 21 15 4 3 12 Jlilil, -4 O IO I 7 I 2 16 4 6 I 45 O 7 25 2 II 24 31 6 5 9

O O O O O O I 18

30- 1967

Number of young fledged 20- «• Number of nests with young • Number of nests with eggs

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec FIG. 2. Breeding season of Rock Doves Columba livia at Flamborough Head, Yorkshire, based on the number of nests occupied during each half-month. In 1966 there were no visits in the first half of July or the second half of October, and in 1967 none in early February, early March or early April. The total of young fledged at the top of each column is the number which had left nests since the previous visit

434 BREEDING BIOLOGY OF ROCK DOVES about 20 will be taken at some time during the incubation period of 17 days; thus, very approximately, one clutch out of every hundred will be predated on each day of incubation.) Because Rock Doves replace lost eggs in about seven days, predation would affect the estimate only if it occurred during the week before a visit was made. Given that there is some breeding activity throughout the year, fig. 2 does suggest that the season has a bimodal form. In both years there was a period of activity from around March or April until June and a second build-up from June until mid-summer. The relative absence of egg-laying in June and July in both years (fig. 1, table 1) could not be attributed to the majority of the Rock Doves being engaged with nestlings and seems to have been caused by a genuine lull in breeding— even allowing that in 1966 one of the July visits could not be made. This lull in breeding is also reflected in the number and proportion of young fledged in late June and July (fig. 2, table 1). It should be mentioned that the low figure for occupied nest density in the second half of April 1966 was caused by a minor catastrophe which resulted in the loss of many nests. This may have been partly the consequence of a natural predator gaining access to the tower and the same thing happened in 1967 in late April or early May. But in both years, apart from many lost clutches, presumably predated, there was an abnormally high incidence of infertility at this time (see below). It may be suspected that environ­ mental conditions had stimulated the Rock Doves to begin breeding, but that these changed, causing many desertions and failures in proper mating ceremonies. Of the factors likely to be involved, it is most feasible that the birds were stimulated by the appearance of bountiful grain supplies on the spring cereal sowings, but that when these dis­ appeared food collection may have suddenly become difficult. Rock Doves require 8-14 days to go through their initial pairing and pre-incubation behaviour leading to laying (Fabricius and Jansson 1963; Murton, Thearle and Lofts, in press) and thereafter need 17J days for incubation; they tend their young in the nest for about 3J weeks (this study and Witherby et al. 1938-41)^ new cycle of laying is begun when nestlings are around 20 days old, and so, including about seven days for post-fledging care, the parents may be tending both eggs and young for up to two weeks. Provided with suitable conditions, Rock Doves could produce eggs at monthly intervals and fig. 2 suggests that this was the case at Flamborough Head. Peaks of laying alternated with peaks of brood care at roughly monthly intervals and the degree of synchronisation might have been greater but for some egg loss and the consequent need for some individuals to produce repeat clutches out of phase. If pairs bred throughout the year it would be possible for them to have twelve broods, though it seems unlikely that any did achieve such a high production rate. Histological evidence indicates that the gonads of most Rock Doves are regressed by November and

435 BRITISH BIRDS Table 2. Breeding success of Rock Doves Columba livia in the tower and cave sites at Flamborough Head, Yorkshire, in 1965 and 1966 X2(2)=9-°4i> P=>0.02, for differences in hatching success; x2(2)=°-988)not signifi­ cant, for differences in nestling success. The 'Percentage infertile' column includes some eggs which simply failed to hatch, as well as those which were broken open to confirm that there had V een no embryo development; the bracketed figure of u % for the cave site in this column also takes in 9% lost through other causes (such as, probably, flooding). The 'Percentage predated or lost' column is confined to young which were either known or suspected to have been taken by predators. Some young in the cave site were certainly or probably lost through flooding and these are included in the bracketed figure of 11% in the 'Percentage dead in nest' column Eggs Percentage Percentage Percentage Percentage laid hatched predated deserted infertile

Tower site 1965 346 61% 25% 9% 5% Tower site 1966 409 70% 15% 10% 5% Cave site 1965-66 57 77% 7% 5% (" %)

Percentage Percentage Percentage Young Percentage predated dead in fledged of hatched fledged or lost nest eggs laid

Tower site 1965 212 7°% 9% «% 43% Tower site 1966 285 7i% 7% "% 49% Cave site 1965-66 44 77% 11% ("%) 60% that they recrudesce again by March (though the onset of regression and recrudescence may show more temporal variation within the population than in the closely related Woodpigeon Columba palumbus or Stock Dove C. oenas). This agrees with fig. 2, which suggests that most Rock Doves at Flamborough Head have a breeding season lasting from late February, March or April until October or November. Fig. 2 also suggests that only about a quarter of the population breeds during the winter. The average number of clutches laid per pair may also be estimated by assuming that population size can be gauged from the maximum occupied nest density, which was 35 in 1965 and 39 in 1966. In 1966 409 eggs were laid, 285 eggs were hatched and 202 young were fledged (table 2): thus each pair that year produced about five clutches, hatched four of them and reared about five individual young to flying. From table 2 it can similarly be calculated that in 1965 35 pairs laid five clutches, hatched three of them and reared four young to flying. These estimates are in reasonable accord with the frequency of egg and nestling peaks in fig. 2. Insufficient records were obtained to justify separate treatment for the cave. Occupied nests were found on all visits and these spanned the period March-November. In 1966 there were as many occupied nests on 8th March as on 30th September and the indications were that the 436 BREEDING BIOLOGY OF ROCK DOVES breeding season was equally as extended as it was in the tower site.

BREEDING SUCCESS Hatching success Table 3 gives the seasonal variations in the percentage of eggs hatched in the tower for the three years combined and also the causes of egg failure. Hatching success varied rather little during the year and the variations showed no real pattern. There was generally more egg pre- dation, usually recorded as the disappearance of eggs, in the main breeding season from March to August than at other times—possibly because there was a higher density of breeding birds at this time and consequent intra-pair disturbance leading to deserted nests, which may then have been predated. Table 3 suggests that proportionately more eggs were lost in the periods when most eggs were laid (not significant with r4=o.775, P=>o.io). But in 1965, when there was a slightly lower average breeding population than in 1966 (fig. 2) and 346 eggs were laid, 25% were predated. This compares with a 15% loss of 409 eggs laid in 1966 (table 2). Most, if not all, egg predation seemed to be caused by Jackdaws Corvus monedula and there was no evidence that Brown Rats Kattus norvegicus had gained access to the tower (the entry door was 15 foot above ground level). Wood Mice Apodemus sylvaticus may have interfered with a few eggs. The amount of egg desertion was greatest at the time of gonad regression and in mid-winter, but, apart from being low from March to June, did not vary much throughout the year. The amount of infertility was also constant, with the exception of a high level in March and April, solely caused by the high figure in April 1966 which has already been discussed. Hatching success was higher in the cave than in the tower, primarily as a result of a lower predation rate (table 2). By its siting, the cave was less likely to attract attention from marauding Jackdaws and some nests were in almost total darkness. But there were not many sites

Table 3. Hatching success of eggs of Rock Doves Columba livia in the tower site at Flamborough Head, Yorkshire, February 1965-February 1967 X2(io)=l8'°28. P=

Eggs Percentage Percentage Percentage Percentage laid hatched predated deserted infertile

January-February 53 62% M% 19% 4% March-April 149 60% 21% 5% 13% May-June 175 67% *5% 5% 3% July-August '59 64% *o% 13% 3% September-October 151 65% 16% 16% 3% November-December 84 70% 15% 12% *% 769 65% 20% 10% 5% 437 BRITISH BIRDS available on ledges in the cave and this caused some pairs to attempt nesting on the sandy floor; such nests fell easy prey to Brown Rats and were also often destroyed at spring tides. The total level of egg loss in the Rock Dove is lower than in the other pigeons and doves so far studied (see Murton 1968 for discus­ sion). Egg loss seems to depend on the factors causing desertion rather than on an intensive predator pressure which, at least in the case of the Woodpigeon, results in unguarded eggs being rapidly eaten. Indeed, it is rare to find much evidence for desertion in the latter species or in the Turtle Dove Streptopelia turtur (Murton 1968), simply because eggs do not remain unattended long enough for this to be recorded. As a consequence of a relatively low predator pressure, partly, predated clutches in the form of single eggs were not often found. Thus in the Rock Dove, unlike the Woodpigeon and Turtle Dove, there is no suggestion that clutch si2e varies throughout the year from a variable risk of predation. In the two years combined 726 eggs were laid as two-egg clutches and, of these, 67% were hatched and 19% were predated, whereas only 29 single eggs (4% of the total eggs laid) were found, of which 38% were hatched and 48% were predated.

Nestling success While the doves displayed little seasonal variation in their ability to hatch eggs, this was not the case with their attempts to rear young (table 4). In the tower the amount of loss due to disappearance, again reckoned as predation, was roughly constant, but the proportion of young dying in the nest showed a definite seasonal trend. Death in the nest seemed attributable to starvation, because these young had empty crops and appeared to be underweight and in poor condition (see also page 444). Such deaths were most frequent in the winter period, when food stocks were presumably at their lowest, and were least apparent

Table 4. Fledging success of nestling Rock Doves Columba livia in the tower site at Flamborough Head, Yorkshire, February 1965-February 1967 X86=34-°36, P=>o.ooi (lumping 'predated' with 'dead'). The totals of eggs laid, from which the last column's percentages were calculated, are given in table 3

Young Percentage predated dead fledged of hatched fledged or lost in nest eggs laid

January-February 33 45% 6% 48% 28% March-April 89 64% 8% 28% 38% May-June 116 66% 13% «% 45% July-August 102 81% 4% 15% 52% September-October 98 86% 6% 8% 56% November-December 59 58% 8% 34% 40%

TOTALS 497 70% 8% «% 46% 438 BREEDING BIOLOGY OF ROCK DOVES during the season of abundant ripe cereal grain on stubbles. The seasonal variation in nest mortality can be also reconciled with the diet of the nestlings (pages 439-442). The rate of nestling loss attributable to predation was similar in the cave (11%) and the tower (8%), as is shown in table z, while most other loss was apparently caused by starvation. As all adults fed on the same feeding grounds, the propor­ tion of dying nestlings would be expected to be similar at the two sites, as should be the average nestling success. Allowing that it was less easy to account for nestlings in the cave and that records were collected only in the March-November period, this was the case. Table 2 shows that 77% of all nestlings hatched in the cave were fledged, while 74% (405) were fledged during March to October in the tower (table 4). As a result of the predation or infertility of single eggs, or through the early loss of one young, there were 5 4 young in one-chick broods and, of these, 67% (36) were fledged, 17% (nine) were predated and 17% (nine) died in the nest. Of 443 young in broods of two, 71% (314) were fledged, 7% (30) were predated and 22% (99) died in the nest. Allowing that broods of one suffered most predation, because they arose from clutches or broods which had already been exposed to a predator, it appears possible that the adults could raise single young slightly more efficiently, but the difference is not statistically significant. The sample was not large enough to examine the success of different- sized broods at different seasons, though the few figures did suggest the possibility that single chicks were proportionately much more successful in mid-winter.

Breeding success The percentage of eggs giving rise to fledged young varied seasonally, primarily as a result of the variable fortune of nestlings, but was generally higher in the cave where there was less egg predation (tables 2 and 4). During the period when most of the population attempted breeding, that is from April until September or October, there was not a great deal of variation in the prospects for successfully rearing young, and this was even more the case from May onwards. The likelihood of breeding successfully in mid-winter was about half as good as during the grain season from July to October. As a consequence of the rela­ tively slight seasonal changes in breeding success and the number of pairs breeding, the period over which young were fledged was extended, with 33% in April-July and 52% in August-November. Only 15% of all young produced left their nests in the winter season December- March and half of these did so in December (see also table 1).

DIET OF NESTLINGS Table 5 shows the seasonal changes in the diet of nestlings for 1965 and 1966 combined and is based on the percentage composition by dry

439 BRITISH BIRDS weight, while table 6 lists the food items consumed on a frequency basis. (Although we examined only nestlings that were near to fledging, there was no evidence to suggest that the diet varied as the young grew except, of course, that the proportion of milk decreased; milk apart, therefore, it was considered that the diet recorded was typical of that of nestlings of any age except the newly hatched which are fed entirely on milk.) As was the case with adults (Murton and Westwood 1966), cereal grains were overwhelmingly the most important single item of diet. Much wheat was collected from winter sowings in January, but from February onwards barley became more important, barley normally constituting the bulk of the spring sowings by March and April. The typical weed seeds of cultivated land were the next most important constituent in the diet, particularly seeds of black bindweed Polygonum convolvulus, knotgrass P. avkulare and persicaria P. perskaria, charlock Sinapsis arvensis and chickweed Stellaria media. Earthworm cocoons featured very prominentiy in the nestlings' food throughout the spring, but disappeared during the dry months of June and July, when many earthworms aestivate or move deep into the soil. Earthworm cocoons did not reappear in the diet until the late autumn, at the beginning of the earthworm breeding season. The diet of nestlings in May, June and July differed little from that in mid-winter except that a wider range of weed seeds was fed to them, including seeds of buttercups Ranunculus spp., various species of grasses, and melilots Melilotus spp. In addition, the total quantity of weed seeds increased by June, this being particularly noticeable in the case of the chickweed. In May grain was still being obtained from late sowings, principally of barley; in June unripe corn was collected, wheat now predominating presumably because it develops and ripens earlier than barley. Oats were clearly obtained from sowings, standing crops and stubbles, but from July until January a proportion of these were the wild species Ave liana fatua.

Table 5. Diet of nestling Rock Doves Columba livia in the tower site at Flamborough Head, Yorkshire, based on percentage composition by dry weight The total dry weight (in grams) of each monthly sample is given in brackets at the head of the column. The small percentage against 'Other' in the September column involves the tic beans and the'peas in table 6; two more casual items in table 6—the maize and the chick mash—do not feature here because the amounts were minute Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec (8.34) (12.12) (47.29) (18.11) (23.67) (24.77) — (24-91) (38-84) ("-77) (27-7o) (20.75)

Wheat 88.4% 7.4% 4.2% 17.9% 9.1% 46.2% — 48.9% 74.7% 57.5% 5i-7% 3-7% Barley 8.9% 82.5% 94.5% 62.3% 74.5% 28.0% — 26.6% 23.6% 42.5% 39.3% 91.6% Oats 0.4% 5.0% — 14.7% 12.8% 19.7% — 23.2% 0.1% — 8.3% 4.4% Weed 1.9% 5.0% 0.3% 0.9% 1.3% 6.1% — j.i% 0.6% — — — Animal 0.4% — 1.0% 4.2% 2.3% — — 0.2% 0.2% — 0.7% 0.3% Other — — — — — _ _ _ 0.8% — — —

440 BREEDING BIOLOGY OF ROCK DOVES Table 6. Diet of nestling Rock Doves Columba livia in the tower site at Flamborough Head, Yorkshire, based on frequency of occurrence of items The figures show the numbers of individual nestlings in which each food item was found, the totals examined in each two-month period (excluding birds with empty crops) being given in brackets at the head of the column. The weeds specified were represented by seeds only Jan-Feb Mar-Apr May-Jun Jul-Aug Sep-Oct Nov-Dec («) (18) (38) (9) (3°) (31)

Wheat 10 11 25 9 29 22 Barley 19 15 36 9 24 29 Oats 2 11 17 4 4 13 Maize 1 Tic beans 1 Peas 1 Polygonum convolvulus 9 4 6 5 7 1 Polygonum aviculare 4 2 5 4 2 Stellaria media 3 2 14 3 2 Brassica or Sinapsis 3 1 4 2 1 Galium aparine 1 1 2 Rumex 3 1 Chenopodium 1 3 1 Ranunculus 1 2 1 1 Melilotus 5 Grass seeds 8 2 Other weed seeds 1 3 4 2 Weed leaves 2 3 3 1 Earthworm cocoons 12 15 6 1 16 Earthworms 1 1 1 Snails 1 1 1 6 Slugs 1 3 1 2 2 Other animals 1 Chick mash 2

The diet of the nestlings was therefore very similar to that of the adults and differed mainly in containing a higher proportion of animal material—chiefly in the form of earthworm cocoons. Earthworms proper and a single lepidopterous chrysalis were probably picked up by chance, but slugs and snails are a regular feature of the diet of all the British pigeons and doves, at least during the breeding season. The slugs were kindly identified by A. E. Ellis as Agriolimax reticulatus and Arion hortensis. The snails were Helicella caperata and H. itala, these being xerophilous species occurring on downs, dunes, cornfields and roadsides, but not in woodland or marshland. In addition to these species which were picked up live, the nestlings were also fed empty shells of the same species and of Trichia hispida. It is possible that the adults either did not distinguish live from dead snails or that dead shells were selected as grit; the former seems more likely. Compared with the Woodpigeon and especially with the Stock Dove (Murton, Westwood and Isaacson 1964), the Rock Dove shows a remarkable

441 BRITISH BIRDS ability to find cereals throughout the year. From a general experience of seasonal changes in grain availability, it might be reckoned that supplies reach a minimum level on the last of the stubbles in January, before the spring sowing season begins, and again in June and early July, when only unripe corn is available. The absence of green vegetation in the nestlings' diet at any season is notable, and conforms with what was also found in the case of the adults; in this respect the Rock Dove's diet differs markedly from that of the Woodpigeon. The diet of the Rock Dove resembles that of the Stock Dove as far as the weed seed component is concerned, but otherwise cereals seem to be far more important for it, in which respect it resembles the Woodpigeon. The diet of the Rock Dove nestlings thus combined the important cereal elements of the Woodpigeon's diet (but not the green food) with the weed seeds favoured by the Stock Dove and thus it is not surprising that the breeding season showed the features of both these other species (see DISCUSSION). In making inter-specific comparisons, however, it should be emphasised that the period of cereal availability is generally longer at Flamborough Head than in East Anglia where the Stock Dove and Woodpigeon were intensively studied. This depends on a later harvest on the exposed north-east coast, which hinders extensive autumn ploughing so that proportionately more stubbles are left for spring cultivation. In addition, a much higher proportion of undersown barley is purposely left for sheep folding in winter (about 2 5 % of the barley crop is under- sown). In the Flamborough Head district 50% of the area is in cereals, 33% in grassland and 17% in fodder roots and other crops.

ADULT AND JUVENILE MORTALITY Very few wild Rock Doves have been ringed, so it is impossible to calculate their average age and the dependent statistics of mortality rate and life expectancy from ringing recoveries. Such information is of interest in view of the apparently high productivity of the species, which follows from its long breeding season. The adult mortality rate can be inferred if the population is stable, so that the number of in­ dividuals breeding for the first time is equal to the number of adults lost. Problems arise in obtaining an unbiased sample in which first-year individuals (those entering their first breeding season) are not over- represented. Experience has shown that juvenile Woodpigeons are more easily shot than adults and that this greater risk from shooting does not disappear until they reach about their first February of life. A sample of Woodpigeons shot just before the breeding season may be unbiased due to the method of collection, but by this time many first- year individuals can no longer be recognised as such by plumage characters. Similar difficulties arise with Rock Doves, except that some may breed before they are six-months old (at least this is true of domes-

442 BREEDING BIOLOGY OF ROCK DOVES tic strains). Furthermore, the identification of juveniles by plumage characters is not so easy with Rock Doves as it is with Woodpigeons. Finally, Rock Doves have not been caught other than by shooting to enable tests to be made for any obvious biases. A sample of Rock Doves was shot at Flamborough Head by an experienced shooter as the birds passed over the cliff top when return­ ing to their roosting caves or nest holes from inland feeding flights; the gunner stationed himself behind a concealing bank adjacent to the cliff edge and faced inland. It is likely that this method was less biased in favour of young individuals than any other (for example, shooting from a boat), because the birds were unable to see the shooter who shot at all that passed close enough; there is no reason to think that a dis­ proportionate number of young approached to within gun-shot range in the circumstances. On the other hand, with shooting from boats, which relies on the Rock Doves being flushed from their ledges and caves, it might be expected that inexperienced young birds would flush later and run a greater risk of being killed. Of the Rock Doves shot, 27% (22) during January-March were in their first year of life, as were 24% (33) during May-August, 33% (21) during September-November and 36% (22) during December. In all cases where the juvenile plumage was not readily identifiable, males which had not yet bred could be recognised by the juvenile appearance of the testis tunic (this consists of a smooth and thin layer of fibroblasts in individuals whose testes have experienced seasonal enlargement for the first time, because after the first breeding season a new tunic is formed and the old one acquires a characteristic shabby and worn appearance: for details see Lofts, Murton and Westwood 1966). Females breeding for the first time could not be checked in this way, but it was assumed that their ratio in the population was equal to that of the males. The adult mortality rate of British Woodpigeons is 36% per annum (Murton 1966a), and that of the Rock Doves would thus appear to be very similar, possibly slightly less and of the order of 30% (in December not all adults would be dead, while by the January- March period some juveniles might have been reckoned as adults, in spite of the care taken). A slightly lower adult mortality rate would be commensurate with the higher degree of residency shown by Rock Doves compared with Woodpigeons, it being known that the more migratory continental populations of Woodpigeons have a higher mortality rate than British stocks (Murton 1965). On page 436 it was estimated that a pair of Rock Doves can produce an average of four or five young in a year. Thus given that 100 adults produce 200-250 offspring, of which only about 30 are needed to replace adult losses, it is evident that the first-year mortality rate of the Rock Dove at Flamborough Head must be of the order of 85-88% per annum, which is much higher than that of the other British pigeons and

443 BRITISH BIRDS doves. Hence a very high productivity is offset by a very high juvenile mortality and not by an exceptional rate of adult losses, a situation generally true for birds and probably other animals as well.

DISCUSSION Stock Doves begin breeding in March and peak laying takes place in May and June to ensure that the majority of young are being fed in June and July when weed seeds are abundant. Woodpigeons lay most eggs in July and August and fledge most young in the good cereal months of August and September (Murton 1966b). The Rock Dove seems to benefit from both sources of food and its egg-laying season spans the whole period. More precisely, the Rock Dove appears to have two main egg-laying periods, the first in April and May corres­ ponding to the Stock Dove peak and the second in August and September corresponding to the Woodpigeon peak. At Flamborough Head breeding success remained fairly constant over this entire period and, if this was also the case for post-fledging survival, it is evident that there could be no strong selection operating to restrict the breeding season, as is the case with the Stock Dove and Woodpigeon (Murton 1966b). Indeed, breeding success remained high until November and a large proportion of the population continued breeding until this time. It might be suspected that the Woodpigeon could also breed success­ fully as late in the year as this, but it is prevented from so doing because its gonads regress in response to the daylength decrease in September (it is responsive only to photoperiods above the level found from March to September). Rock Doves are sensitive to shorter photoperiods and remain gametogenetically active from February to November; in fact, the gonads of a few individuals do not regress at all (Lofts, Murton and Westwood 1966). The differences between the species may depend on the need for Woodpigeons to migrate, an active gonad not being conducive to fat deposition and movement (see Murton 1966b for discussion of this topic). While ringing recoveries are not available to prove the point, it seems reasonably certain that the Rock Dove is the most strictly resident of all the British pigeons and doves. Equipped with a neuro-endocrine apparatus sensitive to short photoperiods, and with some individuals being independent of the natural photoperiod for gametogenesis, the species has the capacity to breed during much of the winter, provided suitable grain supplies exist. Some individuals obviously attempt winter breeding, although the low success at this time indicates that this is difficult. The short- term loss of physiological breeding condition by most members of the population, which prevents winter nesting, may well be only a margin­ ally advantageous adaptation, as otherwise the existence of a few con­ tinuous breeders would not be expected. Changes in agricultural practice are tending to extend the growing season and period of cereal

444 BREEDING BIOLOGY OF ROCK DOVES availability, while winters were becoming more open up to 1950 with a phase of climate amelioration, a process which has reversed since the early 1960's. Such conditions could be favouring more winter breeding and enabling strains showing no gonad regression to be selected, although it is also possible that a balanced polymorphism has long existed. Lofts, Murton and Westwood (1966) have already shown that melanic morphs are more likely to be continuous breeders than wild- types and this may partly account for their dominance in town popula­ tions where continuous breeding is favoured. At present those birds most resembling wild-types are much the most common at Flam- borough Head, and there could be physiological advantages in not being in reproductive condition in mid-winter. A physiological breed­ ing state is associated with the mobilisation of various body reserves, loss of lipid deposits and a generally high energy demand, and this could impose too great a demand at the worst feeding time of the year. The deposition of migratory fat is also photoperiodically controlled, so that the loss of a photo-response might adversely affect such a vital mechanism, quite apart from emancipating the breeding cycle from a dependence on a fixed day length regime. Failing a partially physiological explanation, it is difficult to appreci­ ate the selective advantage of wild-type plumage which is genetically determined by a recessive gene. Many authors (e.g. Mainardi 1964) have suggested the wild-type plumage to be cryptic, but it is not easy to believe that this is the complete explanation, as a perched bird is usually very prominent on a cliff face, while in flight the white rump alone makes it conspicuous; D. Goodwin (in lift.) also agrees with this scepticism. Nonetheless, Lees (1946) gave an instance of a Sparrowhawk Accipiter nisus taking a melanic Rock Dove and claimed that this was the general case, although he produced no quantitative support for this view. The chief predator of the Rock Dove in Britain is undoubtedly the Peregrine Falco peregrinus: so-called domestic strains and homers are outstandingly the chief prey items of this falcon and occur about seven times more frequently in the diet than wild Rock Doves over the country as a whole, but in coastal districts of the Scottish Highlands wild Rock Doves are, with Puffins Fratercula arctica, the chief prey in spring and summer (RatclifFe 1963). Without the benefit of more comparative field data on the relative proportions of different-plumaged pigeons at risk with those taken by falcons, it might be unwise to dismiss the possibility that the plumage is the best compromise possible in cryptic colouring. Falcons attack from above and the pale-grey upper plumage may merge with the sea below, while other and equally powerful selective forces might be favouring the retention of the white rump (which must serve as a signalling device) and black wing bars. But it seems unlikely that the same arguments could be applied to the inland rock dwelling birds of

445 BRITISH BIRDS Spain and the ancestral Afro-Asian populations. An additional problem is posed by some of the races: for example, C livia negkcta from Turkes­ tan and north-west India and C. I. scbimperi from the Nile Valley have grey rumps, while C. I. gymnocydus {torn Senegal and C. I. lividor from the French Sudan to Ghana are small dark birds with very prominent white rumps. Pale or dark plumage and white or grey rumps are not obviously correlated with habitat or geographical distribution, except that the desert races are generally pale. Finally, the melanic population of the Azores (C. livia 'atiantis'), which is usually held to be derived from domestic stock, survives perfecdy well. Even if an anti-predator colouring was once important, it is not clear what prevents the emanci­ pation of melanism in northern populations today in view of the situa­ tion in urban environments. Sexual isolation would not appear to be important because even in its ancestral haunts the species is sufficiently removed from closely related forms. Mainardi (1964) therefore suggested that the colour differences between wild and town populations result from two opposing selection forces. First, he and many authors (e.g. Goodwin 1958) have pointed out that, in pairing, the colour preferences shown by Columba livia are largely determined by imprinting on both parents. An assortive mating system favours the selection of dominant characters so that in towns sexual selection based on imprinting actually favours the dominant chequers and black forms. Second, in the wild, where many predators are claimed to be present (Mainardi did not elaborate, but see above), a cryptic colour is said to be overwhelmingly advantageous and so the recessive blue is favoured. For the reasons stated, Mainardi's explana­ tion would also be acceptable if, instead of invoking an anti-predator selection for cryptic characters, wild-type recessives were being selected for physiological fitness, but this could apply only if there were some degree of linkage between the genes for plumage determination and those regulating photo-responses. There is clearly a need for experi­ mental study. Further, melanic plumage is stronger and abrades less easily than other kinds, which is why many gulls have black wing tips in spite of the adaptative advantage of a white plumage to facilitate a closer approach to fish prey (Tinbergen 1967). As melanics are dominant to the wild-type, it would be expected that a dark-plumaged Rock Dove was the ancestral form because at some time and in some situation the dominant gene must have had a selective advantage. Some authorities (e.g. Whitman 1919) have indeed argued that domestic pigeons are descended from a wild-type having the appearance of a chequer (the so-called C. affinis which is, of course, only a variation of C. livia). The comments made in the introduction to this paper regarding the status of variant plumage types are also relevant here. It has been suggested that Rock Dove populations are resident and rather insular units. Although lost racing pigeons do frequently attach 446 BREEDING BIOLOGY OF ROCK DOVES themselves to the coastal colonies, it is probable that such individuals do not long survive the competition from established birds. At Flam- borough Head it was interesting to note how a large flock of racing pigeons, with many of the more btearre plumage variations, became stranded and to some extent mingled with the local population. Yet within a few days stability returned and there was no lasting change in the plumage ratio of the local population. We picked up about 50 dead adults in the tower during the course of our studies and eight had homing rings. It is probably significant that five of these were found dead within a two-month period in the summer of 1966. We elicited details from the owners of four of them and found that three were actually lost in July and August 1966, indicating they were ill-equipped to survive for long under wild conditions. One was lost at about ten weeks when flying out from its loft at Grimsby; another, with a loft near Sheffield, was lost on a training flight from Derby; and a third, with a loft near Mablethorpe, Lincolnshire, disappeared during its first race from Scarborough. The fourth came from Shotton Colliery, Co. Durham, and was lost in a race from Hatfield: this was the pool bird (betting stakes are often placed on racing pigeons) and the grateful owner, in thanking us for our trouble, enclosed a five- shilling postal order and signed himself 'Yours in sport' 1

ACKNOWLEDGEMENTS It is a pleasure to record our thanks and appreciation to R. A. R. Matthews who helped with some of the nest recording and, in addition, shot the adult sample on our behalf. We are also indebted to N. J. Westwood and various students for assistance with the analysis of the food remains in the nestling crops; to A. E. Ellis for identifying the snails; and to A. G. Jenson, MBE, for preparing the text-figures. Finally, we thank Bridlington Municipal Borough Council for allowing us unrestricted access to the beacon tower.

SUMMARY The breeding biology of Rock Doves Columba livia inhabiting a cave and an old beacon tower at Flamborough Head, Yorkshire, was investigated. The validity of considering these subjects as representative of so-called wild Rock Doves is discussed and established. Egg-laying occurred throughout the year, confirming the observations of Lees (1946) at Cromarty, Scotland, but only about one quarter of the population engaged in winter breeding and the main season was from March to November, with a tendency for a lull in breeding activity in June and July. On average, each pair produced five clutches of two eggs, hatched three or four of these clutches and reared four or five individual young to flying. Of the young fledged, 85% left their nests between April and November and 8% of the remainder in December. Of the eggs laid, 65 % were hatched, 20% were predated and 10% were deserted; desertion was more noticeable in winter. Of the nestlings hatched, 70% fledged and 22% were found dead in their nests. Nestling deaths were much more frequent in winter. The total breeding success was 46% and this showed little variation over the 447 BRITISH BIRDS main breeding season, though it did decline in winter. The diet of nestlings is defined and shown to resemble that of the adults (Murton and Westwood 1966) except for containing more animal material. The diet of the Rock Dove combines the weed seed component of the Stock Dove C. oenas with the cereal element of the Woodpigeon C. palumbus and the breeding season overlaps that of both these species. The adult mortality is probably slightly less than that of the Woodpigeon and is estimated, from the age composition of a shot sample, at about 30% per annum. As the productivity rate is high, the juvenile mortality must be higher than in the Wood­ pigeon to ensure population stability. The discussion considers the selective advantage of the physiological loss of breeding condition by about three-quarters of the population in winter and attributes this to the need to conserve energy supplies. The factors responsible for maintaining the wild-type plumage, which depends on a recessive gene, are also discussed (selective predation and physiological adaptability may both be involved), especially in comparison with urban populations. The latter have become emancipated from a seasonal breeding cycle and are largely composed of melanic birds exhibiting dominant genetical traits.

REFERENCES FABRICIUS, E., and JANSSON, A.-M. (1963): 'Laboratory observations on the repro­ ductive behaviour of the pigeon {Columba livid) during the pre-incubation phase of the breeding cycle'. Anim. Behav., 11: 534-547. GOODWIN, D. (1^955): 'Notes on European wild pigeons'. Avic. Mag., 61: 54-85. (19 5 8):' The existence and causation of colour preferences in the pairing of feral and domestic pigeons'. Bull. Brit. Orn. CI., 78: 136-139. LEES, J. (1946): 'All the year breeding of the Rock-Dove'. Brit. Birds, 39: 136-141. LOFTS, B., MURTON, R. K., and WESTWOOD, N. J. (1966): 'Gonadal cycles and the evolution of breeding seasons in British Columbidae'. /. Zool. Lond., 150: 249-272. MAINARDI, D. (1964): 'Effetto evolutivo della selezione sessuale basata su imprinting in Columba livid'. Riv. Ital. Orn., 34: 213-216. MURTON, R. K. (1965): The Wood-Pigeon. London. — (1966a): 'A statistical evaluation of the effect of wood-pigeon shooting as evidenced by the recoveries of ringed birds'. Statistician, 16: 183-202. (1966b): 'Natural selection and the breeding seasons of the Stock Dove and Wood Pigeon'. Bird Study, 13: 311-327. (1968): 'Breeding, migration and survival of Turtle Doves'. Brit. Birds, 61: 193-212. —• and WESTWOOD, N. J. (1966): 'The foods of the Rock Dove and Feral Pigeon'. Bird Study, 13: 130-146. — and ISAACSON, A. J. (1964): 'The feeding habits of the Wood­ pigeon Columba palumbus, Stock Dove C. oenas and Turtle Dove Streptopelia turtur'. Ibis, 106: 174-188. PETERSEN, N. F., and WILLIAMSON, K. (1949): 'Polymorphism and breeding of the Rock Dove in the Faeroe Islands'. Ibis, 91: 17-23. RATCLIFFE, D. A. (1963): 'The status of the Peregrine in Great Britain'. Bird Study, 10: 56-90. SALOMONSON, F. (1935): 'Aves'. Zoology Faroes, part 64. SUMMERS-SMITH, D. (1963): The House Sparrow. London. TINBERGEN, N. (1967): 'Adaptive features of the Black-headed Gull Larus ridibundus L.' Int. Orn. Congr., 14: 43-59. WHITMAN, C. O. (1919): The Behaviour of Pigeons. Posthumous works of C. O. Whitman, published by the Carnegie Institute, Washington, vol. 3. WITHERBY, H. F., JOURDAIN, F. C. R., TICEHURST, N. F., and TUCKER, B. W. (1939-41): The Handbook of British Birds. London, vol. 4: 137-141. 448