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Proximate constraints on clutch size in domestic pigeons
Applied Animal Behaviour Science, 15 (1986) 277--285
277
Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands
PROXIMATE CONSTRAINTS ON CLUTCH SIZE IN DOMESTIC PIGEONS
KERSTIN HOLMBERG and T H O R S T E N KLINT
University of Stockholm, Department of Zoology, S-106 91 Stockholm (Sweden) (Accepted for publication 12 June 1985)
ABSTRACT Holmberg, K. and Klint, T., 1986. Proximate constraints on clutch size in domestic pigeons. Appl. Anita. Behav. Sci., 15: 277--285. Factors limiting clutch size could in principle act at three different stages in the breeding cycle; namely (1) egg production, (2) incubation and (3) rearing of young. The present study examines proximate limiting factors under laboratory conditions in the domestic pigeon. The results imply that the domestic pigeon is a deterministic egg layer. The domestic pigeon is adapted to incubate a 2-egg clutch, but proximate constraints on clutch size are not obvious. For pigeons which started incubation immediately on laying the first egg, the time-lapse at hatching between the two eggs was always less than at the start of incubation. The heaviest young in a normal clutch had a much higher probability of survival. The relative weight difference between the two is related to synchronization of hatching, and thus ultimately to the start of incubation. Clutches with three young were the most productive in terms o f the number of fledged young.
INTRODUCTION
Clutch size varies between birds, and in pigeons and doves is limited to 1 or 2 eggs. Fruit pigeons, for example, usually lay 1 egg, whereas the "common" pigeon lays 2. Klomp (1970) has reviewed the factors determining cluth size. Lack (1954, 1966) has argued that natural selection favours cluth sizes which result in the greatest number of fledgelings, and which is best adapted on average to the available food resources. Variations in these resources over the year could affect both the number and timing of the breeding cycles. Limiting factors could in principle act at three different stages in the breeding cycle; namely (1) egg production, (2) incubation and (3) rearing of the young. The present experiment examined proximate limiting factors under laboratory conditions during these three stages in the domestic pigeon. (1) Egg production was studied by manipulating the number of eggs to see if the pigeons are prevented from laying more than 2 eggs by tactile and/or visual feedback. (2) Incubation was studied by comparing the development of eggs from 2- and 3-egg cluthes. (3) Rearing of the young was studied by
0168-1591/86/$03.50
© 1986 Elsevier Science Publishers B.V.
278
comparing growth and the number of surviving young from clutches of 1, 2 and 3 nestlings.
Comments on the breeding cycle o f the domestic pigeon (Columba livia var.) The breeding cycle of the domestic pigeon varies between 50 and 60 days, and a maximum of 5 cycles have been recorded in i year (Murton et al., 1974). The cycle starts with a courtship phase, described by Fabricius and Jansson (1963), which usually lasts about 10 days and includes construction of a nest. Thereafter, the female lays the first egg, followed by the second approximately 48 h later. During the 17-day incubation period, incubation is alternated by the male and female. After hatching, the young are fed exclusively on pigeon- or crop-milk, which is produced by both sexes, until the 6th or 7th day. During this period the young are also kept warm by the parents. The squabs' eyes open between the 2nd and 3rd day. A feeding sequence is initiated by a parent pecking the young gently on the top of the head. The young then stretches its head upward and the parent inserts the young's bill into its m o u t h . When the squabs' eyes have opened, they beg for food by pecking at the base of the parents' bill. The young are fledged approximately 30 days after hatching, and although they leave the nest they still rely mainly on the male for food for a couple of days (Whitman, 1919).
MATERIALS AND METHODS The study was carried out at the Zoological Research Station Tovetorp, University of Stockholm, Sweden, during 1978 and 1979. Two rooms were used in the experiments, each 5 X 4 X 2.5 m, with accompanying o u t d o o r aviaries 3 X 3 X 2.5 m. Day and night mean temperature was 18 + 3°C in each room. The first room contained 20 breeding shelves arranged in rows, and the second room had 40. Each shelf measured 40 X 40 X 40 cm and each compartment was equipped with a nesting bowl (diameter 21 cm). In the first room there were 20 sexually mature pigeons and 6 sub-adults, and in the second there were 24 mature and 21 sub-adult birds. During the experiment the birds had free access to nesting material (thin birch twigs and straw). Food, in the form of green peas, wheat and barley, and water were available ad libitum. The light schedule was regulated continuously to 14 h light. No differences were f o u n d between the two rooms in any measures of breeding success, such as numbers of breeding pairs, hatching success and survival of young. Therefore the data are pooled. Some experiments utilized a third room equipped with 12 breeding cages. These consisted of a larger wire-mesh cage (80 X 40 X 60 cm) combined with a smaller one (40 X 40 X 60 cm). The birds could move freely between the two compartments. All young were weighed within the same hour
279 every day. Eggs were weighed both when freshly laid and after 14 days' incubation. All eggs and young were individually marked.
Stage 1. Egg production Regulation of egg number Two experiments were carried out. In 21 clutches, the first egg was removed as soon as possible after laying, to see if the female pigeon has the capacity to produce 3 eggs in a single clutch. Sixty-four unmanipulated clutches were used as controls. In the second experiment, a d u m m y egg was placed in a nestbowl after nestbuilding had been observed for two consecutive days and no egg had been laid. Twelve clutches were manipulated in this way. Thus, if some kind of tactile feedback mechanism is used by the female pigeon to regulate egg number, it could be expected that she should lay no, or at most one, further egg. Fifteen other clutches fulfilling the same criteria were used as controls and were not manipulated.
Stage 2. Incubation Development and hatching of eggs Three-egg clutches were formed by adding a third egg to an otherwise normal 2-egg clutch. The added egg was produced within the same 48-h period as the two other eggs. Seven days after the start of incubation, each egg was candled to determine embryonic development.
Synchronization of hatching The time-lapse between the start of incubation of the two eggs was compared with the time-lapse between their hatchings. Incubation and hatching were recorded once every 24 h, with some additional observations at hatching.
Stage 3. Rearing of young Survival within clutches The probability of survival for squabs from a normal clutch of two young was determined and comparisons made according to three criteria. (a) Whether the y o u n g were hatched on the same or different days. (b) Whether the squab was hatched first or second within the clutch. (c) The relative weight difference between squabs at hatching.
Development and survival of young Clutches of 1, 2 or 3 young were formed by transferring young from newly-hatched clutches. A third young, when added to a 2-young clutch, was matched for age and weight. Transfers were carried out within the first day after hatching.
280 RESULTS
Stage 1. Egg production Regulation of egg number N o f e m a l e p r o d u c e d m o r e t h a n 2 eggs, e i t h e r f r o m c l u t c h e s w h e r e t h e f i r s t egg w a s r e m o v e d o r f r o m u n m a n i p u l a t e d c o n t r o l c l u t c h e s . N o signif i c a n t d i f f e r e n c e w a s f o u n d in t h e n u m b e r o f 1- a n d 2 - e g g c l u t c h e s b e t w e e n t h e e x p e r i m e n t a l a n d c o n t r o l g r o u p s ( T a b l e I A , •2 = 2 . 9 7 , d f = 2, 0 . 2 5 > P
> 0.10). I n t h e e x p e r i m e n t in w h i c h a d u m m y egg w a s a d d e d , t h e r e w a s n o signif i c a n t d i f f e r e n c e b e t w e e n e x p e r i m e n t a l a n d c o n t r o l g r o u p s in t h e d i s t r i b u t i o n o f 0-, 1- a n d 2 - e g g c l u t c h e s ( T a b l e I B , ×z = 0 . 7 9 , d f = 2, 0 . 7 5 > P > 0.50). TABLE I A. Number o f pairs with 1, 2 or 3 eggs within the clutch, depending on whether the first egg had been removed or not (x ~ = 2.97, df = 2, 0.25 > P > 0.10)
No. o f eggs/pair
Total
1
2
3
Pairs with first egg removed
6
15
0
21
Control
8
56
0
64
B. Number o f pairs with 0, 1 and 2 eggs, depending on whether or not an extra egg was placed in the nestbowl 2 days before the expected start of egg-laying (×5 = 0.79, df = 2, 0.75 > P > 0.50) No. o f eggs/pair 0
1
Total
2
Dummy egg in nest before start of laying
5
2
5
12
Control
6
1
8
15
Stage 2. Incubation Development and hatching of eggs T e n a r t i f i c i a l 3-egg c l u t c h e s h a d a n a v e r a g e o f 2 . 5 f e r t i l i z e d eggs p e r c l u t c h . O f t h e s e f e r t i l i z e d eggs, 1 . 7 eggs w e r e d e v e l o p e d u n t i l h a t c h i n g . H o w e v e r , o n l y 1.0 y o u n g p e r c l u t c h w a s p r o p e r l y h a t c h e d . N o s i g n i f i c a n t
281
difference in hatching success was found between pairs which incubated a normal 2~gg clutch and those which incubated an artificial 3-egg clutch (X ~ = 1.35, df = 1, 0.25 > P > 0.10). Time of incubation was measured in 2- and 3-egg clutches from the laying of the second egg to the hatching o f the second egg. The mean time of incubation for the 3-egg clutches was 19.16 + 2.23 days (N=6), and for the normal 2-egg clutches it was 17.00 + 0.53 days (N--15). This difference in time of incubation is significant (/~ < 0.001, Mann--Whitney U-test).
Synchronization of hatching Table II shows that the time-lapse between the first and second egg is related to the stage of incubation (X2 = 18.0, df = 2, P < 0.001). Ifispection of the data shows that the time-lapse is less at hatching. For pairs which started their incubation when the first egg was laid, the time-lapse at hatching was always less than the expected time-lapse of 48 h. T A B L E II D i f f e r e n c e in t i m e (h) b e t w e e n start o f i n c u b a t i o n o f t h e first and s e c o n d egg c o m p a r e d w i t h t h e d i f f e r e n c e in t i m e at h a t c h i n g (x ~ = 18.0, d f = 2, P < 0.001)
D i f f e r e n c e (h) b e t w e e n 1st and 2nd egg > 48 Start o f i n c u b a t i o n Hatching
48--24
< 24
Total
12
9
4
25
1
6
18
25
Stage 3. Rearing of young Survival within clutches There was no significant difference between the proportion of young fledged when young hatched the same day were compared with young hatched on different days (×2 = 2.00, df = 1, P < 0.2), nor when young hatched first within a clutch were compared to those hatched second (×2 = 0.16, df = 1, P < 0.7). If both order of hatching and difference of hatching time are considered, the greatest chance of surviving seems to be if hatched as number one and hatched alone on that day. The relative weight difference of young within clutches at hatching was related to survival. Survival was significantly higher for the largest young compared to the smallest young (X 2 = 11.22, df = 2 , P < 0 . 0 1 ) .
Development and survival of young Table III gives the comparison of productivity for different clutch sizes. The productivity (Pr) was defined here as y o u n g fledged/pair (F) X number
282 TABLE III A. Number of surviving young from clutches with 1, 2 and 3 young. Difference in fledged young/pair between 1- and 2-young clutches was tested, P < 0.05; 2- vs. 3-young clutches, NS: 1 vs. 3,P < 0.1; Mann--Whitney U-test Original clutch size
No. of pairs
No. of young
No. of fledged young
Fledged young/pair
1 young 2 young 3 young
13 58 9
13 116 27
8 65 13
0.62 1.12 1.44
B. A comparison between weight of egg and young of different ages correlated with survival. 1Mann--Whitney U-test Weight (g) (mean -+ SD)
N
P
Weight of egg at laying
Fledged Dead
20.45 + 1.63 18.43 ± 1.75
8 8
NS
Weight of egg after 14 days of incubation
Fledged Dead
16.89 ± 0.71 16.33 -+ 1.83
6 8
NS
Weight of young at 1 day of age
Fledged Dead
16.15 ± 1.54 15.31 ± 1.72
6 10
NS
Weight of young at 5 days of age
Fledged Dead
77.31 +- 6.28 69.54 ± 14.64
7 8
NS
Weight of young at 10 days of age
Fledged Dead
190.74 ± 41.36 122.33 ± 42.25
8 8
P < 0.01
o f clutches p e r y e a r (B). F o r a detailed discussion o f t h e d e f i n i t i o n see Ricklefs and B l o o m (197 7). T h e n u m b e r o f fledgelings per pair was l o w e s t for 1 - y o u n g clutches {0.62) a n d a b o u t equal f o r 2- (1.12) and 3- (1.44) y o u n g clutches. The n u m b e r o f b r e e d i n g cycles per pair a n d y e a r was n o t m e a s u r e d , and t h u s t h e t o t a l p r o d u c t i v i t y c o u l d n o t be calculated (Table I I I A ) . A significant d i f f e r e n c e was f o u n d b e t w e e n 1- and 2 - y o u n g c l u t c h e s for the n u m b e r of fledged y o u n g / p a i r ( M a n n - - W h i t n e y U-test, P < 0.05), and a similar t r e n d b e t w e e n 1- and 3 - y o u n g clutches (P ~< 0.1). The d i f f e r e n c e b e t w e e n 2and 3 - y o u n g c l u t c h e s was n o t significant. T h e t w o categories fledged and dead y o u n g were c o m p a r e d f o r weights at d i f f e r e n t d e v e l o p m e n t a l stages (Table IIIB). The o n l y d i f f e r e n c e f o u n d was for y o u n g at 10 d a y s o f age, fledgelings being significantly heavier (P < 0 . 0 1 , M a n n - - W h i t n e y U-test).
283 DISCUSSION
Regulation of egg number No female pigeon laid more than 2 eggs in the first experiment. Neither did they p r o d u c e just 1 egg in the second experiment, which was expected if a tactile/visual feedback mechanism regulates clutch size. Nor would the inability of a female pigeon to increase her daily energy budget to produce more eggs seem a likely proximate cause. Other experiments by T. Klint and K. Holmberg (unpublished data) show that the energy costs for a female of producing an egg is very low compared to the average daily energy budget (DEB) (Pinowski and Kendeigh, 1977). The mean weight o f a female pigeon is 330 g (own stock) and that of an egg about 19 g. This means that an egg is only 5.8% of the female b o d y weight. Considering the small clutch size and small eggs, it is notable that the eggs are laid with a time-lapse o f 2 days. Many birds of comparable size lay their eggs with a much shorter time-lapse. Most other birds with small eggs have larger clutches, or alternatively birds with small clutches have larger eggs (Murton and Westwood, 1977). This implies that the domestic pigeon is a deterministic egg layer, and that the regulation of clutch size is probably an effect of limitations in another stage of the reproductive cycle.
Development and hatching of eggs Incubation places somewhat different demands on pigeons than on other birds since they have no actual brood patches. Instead, they cover the eggs with a kind of " f e a t h e r m u f f " which probably has an insulating function, preventing heat loss by radiation from the parent bird. As far as we know, the skin has no direct contact with the egg surface. Pairs incubating 3 eggs showed no difference in hatching success to those incubating 2 eggs. However, the time to hatching is prolonged for the 3-egg clutches, possibly because the feathermuff is t o o small and heat loss is thus increased. Energy costs for incubation could be a limiting factor. However, preliminary calculations (T. Klint and K. Holmberg, unpublished data) show that the energy produced by pigeons suffices for the development of 3-egg clutches. Kendeigh (1973) has argued that for some passerines incubation entails a considerable net energy cost, but this is disputed by Walsberg and King (1978), who argue that if the whole bird--nest complex is considered, the net costs are actually even smaller than for a bird merely perching beside the nest. The domestic pigeon is obviously adapted to incubate a 2-egg clutch, b u t on the other hand there does not seem to be any proximate reason w h y incubation should be a limiting factor for clutch size.
284
Synchronization of hatching For those pigeons which started incubation immediately on laying the first egg, the time-lapse at hatching between the two eggs was always less than at the start of incubation. Incubation is perhaps inefficient during the first 2 days, and consequently the development of the first egg is not necessarily in advance of the second. Lack of experience on the part of some birds could give rise to such individual differences in incubation behaviour, b u t the effect of experience on the onset of incubation is not known. The importance of synchronization could lie in its effect on offspring survival, by way of the weight-differences between young that result from delayed hatching of the second egg (see below). As to the adaptiveness of the phenomenon, one could speculate that synchronization is advantageous when food is abundant and disadvantageous when food is in short supply.
Survival within clutches The heaviest of the two young in a normal clutch had a much higher probability of survival. The relative weight difference between the two is of course strongly related to synchronization of hatching, and thus ultimately to the start of incubation. Increasing synchronization leads to decreasing weight differences. The absolute weight of the egg or young was not important for survival until the young were 10 days of age, at which time heavier young survived more often. However, the weight difference at 10 days seems mainly to be an effect of the relative weight difference at hatching, and suggests that competition between the y o u n g might be of importance. Absolute weight per se seems to be of little importance for survival. Murton et al. (1974) found that in w o o d pigeons the mean weight of hatched eggs was higher than for eggs which failed to hatch, b u t that there was no relationship between egg weight and fledgeling survival of hatched squabs. Nor was there any correlation between the squab weight at hatching and at 6 days of age. We believe that this implies that variation in egg weight within w o o d pigeon clutches is only adaptive in conjunction with appropriate incubation behaviour. In this context, it could be appropriate to delay the start of incubation until the clutch is completed.
Development and survival of young The birds in the present study lived with a superabundance of food, and the effects of food supply on productivity thus cannot be gauged. Young pigeons demand heavy energy investments by the parents, and under sub-optimal natural conditions this might reduce the optimal clutch size if life-time productivity is considered (Haukioja and Hakala, 1979). Thus, the present finding that the 3-young clutch is the most productive
285 in t e r m s o f t h e n u m b e r o f fledged y o u n g d o e s n o t necessarily m e a n t h a t it is t h e m o s t p r o d u c t i v e in t e r m s o f t o t a l r e p r o d u c i n g offspring. T h a t d i f f e r e n c e s in p r o d u c t i v i t y w e r e f o u n d in t h e p r e s e n t s t u d y i m p l i c a t e o t h e r p r o x i m a t e f a c t o r s besides f o o d s u p p l y in t h e l i m i t a t i o n o f clutch size. M u r t o n et al. ( 1 9 7 4 ) f o u n d a higher t o t a l p r o d u c t i v i t y f o r artificial 3y o u n g c l u t c h e s in w o o d pigeons, b u t t h a t t h e i r m e a n w e i g h t at fledging was l o w e r t h a n f o r birds f r o m b r o o d s o f t w o . T h e s e a u t h o r s t h e r e b y argue t h a t p o s t - f l e d g i n g m o r t a l i t y c o u l d be a limiting f a c t o r on clutch size. ACKNOWLEDGEMENTS We wish t o t h a n k Prof. A. E n e m a r f o r useful c o m m e n t s on t h e m a n u s c r i p t a n d L. C h a p m a n f o r an extensive revision o f t h e English language.
REFERENCES Fabricius, E. and Jansson, A.M., 1963. Laboratory observations on the reproductive behaviour of the pigeon (Columba livia) during the pre-incubation phase of the breeding cycle. Anita. Behav., 11: 534--547. Haukioja, E. and Hakala, T., 1979. On the relationship between avian clutch size and life span. Ornis Fenn., 56: 45--55. Kendeigh, S.C., 1973. Energetics of reproduction in birds. In: D.S. Farner (Editor), Breeding Biology of Birds. National Academy of Sciences, Washington, DC, pp. 111--117. Klomp. H., 1970. The determination of clutch-size in birds: a review. Ardea, 58: 1--124. Lack, D., 1954. The Natural Regulation of Animal Numbers. Clarendon Press, Oxford. Lack, D., 1966. Population Studies of Birds. Clarendon Press, Oxford. Murton, R.K. and Westwood, N.J., 1977. Avian Breeding Cycles. Clarendon Press, Oxford. Murton, R.K., Thearle, R.J.P. and Coombs, C.F.B., 1974. Ecological studies of the feral pigeon Columba livia var. III. Reproduction and plumage polymorphism. J. Appl. Ecol., 11: 841--854. Pinowski, J. and Kendeigh, S.C., 1977. Granivorous Birds in Ecosystems. Cambridge University Press, Cambridge, International Biological Program 12. Ricklefs. R.E. and Bloom, G., 1977. Components of avian breeding productivity. Auk, 94: 86--96. Walsberg, G.E. and King, J.R., 1978. The energetic consequences of incubation for two passerine species. Auk, 95: 644--655. Whitman, C.O., 1919. The Behaviour of Pigeons. Posthumous work edited by H.A. Carr, Carnegie Institute, Washington.
277
Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands
PROXIMATE CONSTRAINTS ON CLUTCH SIZE IN DOMESTIC PIGEONS
KERSTIN HOLMBERG and T H O R S T E N KLINT
University of Stockholm, Department of Zoology, S-106 91 Stockholm (Sweden) (Accepted for publication 12 June 1985)
ABSTRACT Holmberg, K. and Klint, T., 1986. Proximate constraints on clutch size in domestic pigeons. Appl. Anita. Behav. Sci., 15: 277--285. Factors limiting clutch size could in principle act at three different stages in the breeding cycle; namely (1) egg production, (2) incubation and (3) rearing of young. The present study examines proximate limiting factors under laboratory conditions in the domestic pigeon. The results imply that the domestic pigeon is a deterministic egg layer. The domestic pigeon is adapted to incubate a 2-egg clutch, but proximate constraints on clutch size are not obvious. For pigeons which started incubation immediately on laying the first egg, the time-lapse at hatching between the two eggs was always less than at the start of incubation. The heaviest young in a normal clutch had a much higher probability of survival. The relative weight difference between the two is related to synchronization of hatching, and thus ultimately to the start of incubation. Clutches with three young were the most productive in terms o f the number of fledged young.
INTRODUCTION
Clutch size varies between birds, and in pigeons and doves is limited to 1 or 2 eggs. Fruit pigeons, for example, usually lay 1 egg, whereas the "common" pigeon lays 2. Klomp (1970) has reviewed the factors determining cluth size. Lack (1954, 1966) has argued that natural selection favours cluth sizes which result in the greatest number of fledgelings, and which is best adapted on average to the available food resources. Variations in these resources over the year could affect both the number and timing of the breeding cycles. Limiting factors could in principle act at three different stages in the breeding cycle; namely (1) egg production, (2) incubation and (3) rearing of the young. The present experiment examined proximate limiting factors under laboratory conditions during these three stages in the domestic pigeon. (1) Egg production was studied by manipulating the number of eggs to see if the pigeons are prevented from laying more than 2 eggs by tactile and/or visual feedback. (2) Incubation was studied by comparing the development of eggs from 2- and 3-egg cluthes. (3) Rearing of the young was studied by
0168-1591/86/$03.50
© 1986 Elsevier Science Publishers B.V.
278
comparing growth and the number of surviving young from clutches of 1, 2 and 3 nestlings.
Comments on the breeding cycle o f the domestic pigeon (Columba livia var.) The breeding cycle of the domestic pigeon varies between 50 and 60 days, and a maximum of 5 cycles have been recorded in i year (Murton et al., 1974). The cycle starts with a courtship phase, described by Fabricius and Jansson (1963), which usually lasts about 10 days and includes construction of a nest. Thereafter, the female lays the first egg, followed by the second approximately 48 h later. During the 17-day incubation period, incubation is alternated by the male and female. After hatching, the young are fed exclusively on pigeon- or crop-milk, which is produced by both sexes, until the 6th or 7th day. During this period the young are also kept warm by the parents. The squabs' eyes open between the 2nd and 3rd day. A feeding sequence is initiated by a parent pecking the young gently on the top of the head. The young then stretches its head upward and the parent inserts the young's bill into its m o u t h . When the squabs' eyes have opened, they beg for food by pecking at the base of the parents' bill. The young are fledged approximately 30 days after hatching, and although they leave the nest they still rely mainly on the male for food for a couple of days (Whitman, 1919).
MATERIALS AND METHODS The study was carried out at the Zoological Research Station Tovetorp, University of Stockholm, Sweden, during 1978 and 1979. Two rooms were used in the experiments, each 5 X 4 X 2.5 m, with accompanying o u t d o o r aviaries 3 X 3 X 2.5 m. Day and night mean temperature was 18 + 3°C in each room. The first room contained 20 breeding shelves arranged in rows, and the second room had 40. Each shelf measured 40 X 40 X 40 cm and each compartment was equipped with a nesting bowl (diameter 21 cm). In the first room there were 20 sexually mature pigeons and 6 sub-adults, and in the second there were 24 mature and 21 sub-adult birds. During the experiment the birds had free access to nesting material (thin birch twigs and straw). Food, in the form of green peas, wheat and barley, and water were available ad libitum. The light schedule was regulated continuously to 14 h light. No differences were f o u n d between the two rooms in any measures of breeding success, such as numbers of breeding pairs, hatching success and survival of young. Therefore the data are pooled. Some experiments utilized a third room equipped with 12 breeding cages. These consisted of a larger wire-mesh cage (80 X 40 X 60 cm) combined with a smaller one (40 X 40 X 60 cm). The birds could move freely between the two compartments. All young were weighed within the same hour
279 every day. Eggs were weighed both when freshly laid and after 14 days' incubation. All eggs and young were individually marked.
Stage 1. Egg production Regulation of egg number Two experiments were carried out. In 21 clutches, the first egg was removed as soon as possible after laying, to see if the female pigeon has the capacity to produce 3 eggs in a single clutch. Sixty-four unmanipulated clutches were used as controls. In the second experiment, a d u m m y egg was placed in a nestbowl after nestbuilding had been observed for two consecutive days and no egg had been laid. Twelve clutches were manipulated in this way. Thus, if some kind of tactile feedback mechanism is used by the female pigeon to regulate egg number, it could be expected that she should lay no, or at most one, further egg. Fifteen other clutches fulfilling the same criteria were used as controls and were not manipulated.
Stage 2. Incubation Development and hatching of eggs Three-egg clutches were formed by adding a third egg to an otherwise normal 2-egg clutch. The added egg was produced within the same 48-h period as the two other eggs. Seven days after the start of incubation, each egg was candled to determine embryonic development.
Synchronization of hatching The time-lapse between the start of incubation of the two eggs was compared with the time-lapse between their hatchings. Incubation and hatching were recorded once every 24 h, with some additional observations at hatching.
Stage 3. Rearing of young Survival within clutches The probability of survival for squabs from a normal clutch of two young was determined and comparisons made according to three criteria. (a) Whether the y o u n g were hatched on the same or different days. (b) Whether the squab was hatched first or second within the clutch. (c) The relative weight difference between squabs at hatching.
Development and survival of young Clutches of 1, 2 or 3 young were formed by transferring young from newly-hatched clutches. A third young, when added to a 2-young clutch, was matched for age and weight. Transfers were carried out within the first day after hatching.
280 RESULTS
Stage 1. Egg production Regulation of egg number N o f e m a l e p r o d u c e d m o r e t h a n 2 eggs, e i t h e r f r o m c l u t c h e s w h e r e t h e f i r s t egg w a s r e m o v e d o r f r o m u n m a n i p u l a t e d c o n t r o l c l u t c h e s . N o signif i c a n t d i f f e r e n c e w a s f o u n d in t h e n u m b e r o f 1- a n d 2 - e g g c l u t c h e s b e t w e e n t h e e x p e r i m e n t a l a n d c o n t r o l g r o u p s ( T a b l e I A , •2 = 2 . 9 7 , d f = 2, 0 . 2 5 > P
> 0.10). I n t h e e x p e r i m e n t in w h i c h a d u m m y egg w a s a d d e d , t h e r e w a s n o signif i c a n t d i f f e r e n c e b e t w e e n e x p e r i m e n t a l a n d c o n t r o l g r o u p s in t h e d i s t r i b u t i o n o f 0-, 1- a n d 2 - e g g c l u t c h e s ( T a b l e I B , ×z = 0 . 7 9 , d f = 2, 0 . 7 5 > P > 0.50). TABLE I A. Number o f pairs with 1, 2 or 3 eggs within the clutch, depending on whether the first egg had been removed or not (x ~ = 2.97, df = 2, 0.25 > P > 0.10)
No. o f eggs/pair
Total
1
2
3
Pairs with first egg removed
6
15
0
21
Control
8
56
0
64
B. Number o f pairs with 0, 1 and 2 eggs, depending on whether or not an extra egg was placed in the nestbowl 2 days before the expected start of egg-laying (×5 = 0.79, df = 2, 0.75 > P > 0.50) No. o f eggs/pair 0
1
Total
2
Dummy egg in nest before start of laying
5
2
5
12
Control
6
1
8
15
Stage 2. Incubation Development and hatching of eggs T e n a r t i f i c i a l 3-egg c l u t c h e s h a d a n a v e r a g e o f 2 . 5 f e r t i l i z e d eggs p e r c l u t c h . O f t h e s e f e r t i l i z e d eggs, 1 . 7 eggs w e r e d e v e l o p e d u n t i l h a t c h i n g . H o w e v e r , o n l y 1.0 y o u n g p e r c l u t c h w a s p r o p e r l y h a t c h e d . N o s i g n i f i c a n t
281
difference in hatching success was found between pairs which incubated a normal 2~gg clutch and those which incubated an artificial 3-egg clutch (X ~ = 1.35, df = 1, 0.25 > P > 0.10). Time of incubation was measured in 2- and 3-egg clutches from the laying of the second egg to the hatching o f the second egg. The mean time of incubation for the 3-egg clutches was 19.16 + 2.23 days (N=6), and for the normal 2-egg clutches it was 17.00 + 0.53 days (N--15). This difference in time of incubation is significant (/~ < 0.001, Mann--Whitney U-test).
Synchronization of hatching Table II shows that the time-lapse between the first and second egg is related to the stage of incubation (X2 = 18.0, df = 2, P < 0.001). Ifispection of the data shows that the time-lapse is less at hatching. For pairs which started their incubation when the first egg was laid, the time-lapse at hatching was always less than the expected time-lapse of 48 h. T A B L E II D i f f e r e n c e in t i m e (h) b e t w e e n start o f i n c u b a t i o n o f t h e first and s e c o n d egg c o m p a r e d w i t h t h e d i f f e r e n c e in t i m e at h a t c h i n g (x ~ = 18.0, d f = 2, P < 0.001)
D i f f e r e n c e (h) b e t w e e n 1st and 2nd egg > 48 Start o f i n c u b a t i o n Hatching
48--24
< 24
Total
12
9
4
25
1
6
18
25
Stage 3. Rearing of young Survival within clutches There was no significant difference between the proportion of young fledged when young hatched the same day were compared with young hatched on different days (×2 = 2.00, df = 1, P < 0.2), nor when young hatched first within a clutch were compared to those hatched second (×2 = 0.16, df = 1, P < 0.7). If both order of hatching and difference of hatching time are considered, the greatest chance of surviving seems to be if hatched as number one and hatched alone on that day. The relative weight difference of young within clutches at hatching was related to survival. Survival was significantly higher for the largest young compared to the smallest young (X 2 = 11.22, df = 2 , P < 0 . 0 1 ) .
Development and survival of young Table III gives the comparison of productivity for different clutch sizes. The productivity (Pr) was defined here as y o u n g fledged/pair (F) X number
282 TABLE III A. Number of surviving young from clutches with 1, 2 and 3 young. Difference in fledged young/pair between 1- and 2-young clutches was tested, P < 0.05; 2- vs. 3-young clutches, NS: 1 vs. 3,P < 0.1; Mann--Whitney U-test Original clutch size
No. of pairs
No. of young
No. of fledged young
Fledged young/pair
1 young 2 young 3 young
13 58 9
13 116 27
8 65 13
0.62 1.12 1.44
B. A comparison between weight of egg and young of different ages correlated with survival. 1Mann--Whitney U-test Weight (g) (mean -+ SD)
N
P
Weight of egg at laying
Fledged Dead
20.45 + 1.63 18.43 ± 1.75
8 8
NS
Weight of egg after 14 days of incubation
Fledged Dead
16.89 ± 0.71 16.33 -+ 1.83
6 8
NS
Weight of young at 1 day of age
Fledged Dead
16.15 ± 1.54 15.31 ± 1.72
6 10
NS
Weight of young at 5 days of age
Fledged Dead
77.31 +- 6.28 69.54 ± 14.64
7 8
NS
Weight of young at 10 days of age
Fledged Dead
190.74 ± 41.36 122.33 ± 42.25
8 8
P < 0.01
o f clutches p e r y e a r (B). F o r a detailed discussion o f t h e d e f i n i t i o n see Ricklefs and B l o o m (197 7). T h e n u m b e r o f fledgelings per pair was l o w e s t for 1 - y o u n g clutches {0.62) a n d a b o u t equal f o r 2- (1.12) and 3- (1.44) y o u n g clutches. The n u m b e r o f b r e e d i n g cycles per pair a n d y e a r was n o t m e a s u r e d , and t h u s t h e t o t a l p r o d u c t i v i t y c o u l d n o t be calculated (Table I I I A ) . A significant d i f f e r e n c e was f o u n d b e t w e e n 1- and 2 - y o u n g c l u t c h e s for the n u m b e r of fledged y o u n g / p a i r ( M a n n - - W h i t n e y U-test, P < 0.05), and a similar t r e n d b e t w e e n 1- and 3 - y o u n g clutches (P ~< 0.1). The d i f f e r e n c e b e t w e e n 2and 3 - y o u n g c l u t c h e s was n o t significant. T h e t w o categories fledged and dead y o u n g were c o m p a r e d f o r weights at d i f f e r e n t d e v e l o p m e n t a l stages (Table IIIB). The o n l y d i f f e r e n c e f o u n d was for y o u n g at 10 d a y s o f age, fledgelings being significantly heavier (P < 0 . 0 1 , M a n n - - W h i t n e y U-test).
283 DISCUSSION
Regulation of egg number No female pigeon laid more than 2 eggs in the first experiment. Neither did they p r o d u c e just 1 egg in the second experiment, which was expected if a tactile/visual feedback mechanism regulates clutch size. Nor would the inability of a female pigeon to increase her daily energy budget to produce more eggs seem a likely proximate cause. Other experiments by T. Klint and K. Holmberg (unpublished data) show that the energy costs for a female of producing an egg is very low compared to the average daily energy budget (DEB) (Pinowski and Kendeigh, 1977). The mean weight o f a female pigeon is 330 g (own stock) and that of an egg about 19 g. This means that an egg is only 5.8% of the female b o d y weight. Considering the small clutch size and small eggs, it is notable that the eggs are laid with a time-lapse o f 2 days. Many birds of comparable size lay their eggs with a much shorter time-lapse. Most other birds with small eggs have larger clutches, or alternatively birds with small clutches have larger eggs (Murton and Westwood, 1977). This implies that the domestic pigeon is a deterministic egg layer, and that the regulation of clutch size is probably an effect of limitations in another stage of the reproductive cycle.
Development and hatching of eggs Incubation places somewhat different demands on pigeons than on other birds since they have no actual brood patches. Instead, they cover the eggs with a kind of " f e a t h e r m u f f " which probably has an insulating function, preventing heat loss by radiation from the parent bird. As far as we know, the skin has no direct contact with the egg surface. Pairs incubating 3 eggs showed no difference in hatching success to those incubating 2 eggs. However, the time to hatching is prolonged for the 3-egg clutches, possibly because the feathermuff is t o o small and heat loss is thus increased. Energy costs for incubation could be a limiting factor. However, preliminary calculations (T. Klint and K. Holmberg, unpublished data) show that the energy produced by pigeons suffices for the development of 3-egg clutches. Kendeigh (1973) has argued that for some passerines incubation entails a considerable net energy cost, but this is disputed by Walsberg and King (1978), who argue that if the whole bird--nest complex is considered, the net costs are actually even smaller than for a bird merely perching beside the nest. The domestic pigeon is obviously adapted to incubate a 2-egg clutch, b u t on the other hand there does not seem to be any proximate reason w h y incubation should be a limiting factor for clutch size.
284
Synchronization of hatching For those pigeons which started incubation immediately on laying the first egg, the time-lapse at hatching between the two eggs was always less than at the start of incubation. Incubation is perhaps inefficient during the first 2 days, and consequently the development of the first egg is not necessarily in advance of the second. Lack of experience on the part of some birds could give rise to such individual differences in incubation behaviour, b u t the effect of experience on the onset of incubation is not known. The importance of synchronization could lie in its effect on offspring survival, by way of the weight-differences between young that result from delayed hatching of the second egg (see below). As to the adaptiveness of the phenomenon, one could speculate that synchronization is advantageous when food is abundant and disadvantageous when food is in short supply.
Survival within clutches The heaviest of the two young in a normal clutch had a much higher probability of survival. The relative weight difference between the two is of course strongly related to synchronization of hatching, and thus ultimately to the start of incubation. Increasing synchronization leads to decreasing weight differences. The absolute weight of the egg or young was not important for survival until the young were 10 days of age, at which time heavier young survived more often. However, the weight difference at 10 days seems mainly to be an effect of the relative weight difference at hatching, and suggests that competition between the y o u n g might be of importance. Absolute weight per se seems to be of little importance for survival. Murton et al. (1974) found that in w o o d pigeons the mean weight of hatched eggs was higher than for eggs which failed to hatch, b u t that there was no relationship between egg weight and fledgeling survival of hatched squabs. Nor was there any correlation between the squab weight at hatching and at 6 days of age. We believe that this implies that variation in egg weight within w o o d pigeon clutches is only adaptive in conjunction with appropriate incubation behaviour. In this context, it could be appropriate to delay the start of incubation until the clutch is completed.
Development and survival of young The birds in the present study lived with a superabundance of food, and the effects of food supply on productivity thus cannot be gauged. Young pigeons demand heavy energy investments by the parents, and under sub-optimal natural conditions this might reduce the optimal clutch size if life-time productivity is considered (Haukioja and Hakala, 1979). Thus, the present finding that the 3-young clutch is the most productive
285 in t e r m s o f t h e n u m b e r o f fledged y o u n g d o e s n o t necessarily m e a n t h a t it is t h e m o s t p r o d u c t i v e in t e r m s o f t o t a l r e p r o d u c i n g offspring. T h a t d i f f e r e n c e s in p r o d u c t i v i t y w e r e f o u n d in t h e p r e s e n t s t u d y i m p l i c a t e o t h e r p r o x i m a t e f a c t o r s besides f o o d s u p p l y in t h e l i m i t a t i o n o f clutch size. M u r t o n et al. ( 1 9 7 4 ) f o u n d a higher t o t a l p r o d u c t i v i t y f o r artificial 3y o u n g c l u t c h e s in w o o d pigeons, b u t t h a t t h e i r m e a n w e i g h t at fledging was l o w e r t h a n f o r birds f r o m b r o o d s o f t w o . T h e s e a u t h o r s t h e r e b y argue t h a t p o s t - f l e d g i n g m o r t a l i t y c o u l d be a limiting f a c t o r on clutch size. ACKNOWLEDGEMENTS We wish t o t h a n k Prof. A. E n e m a r f o r useful c o m m e n t s on t h e m a n u s c r i p t a n d L. C h a p m a n f o r an extensive revision o f t h e English language.
REFERENCES Fabricius, E. and Jansson, A.M., 1963. Laboratory observations on the reproductive behaviour of the pigeon (Columba livia) during the pre-incubation phase of the breeding cycle. Anita. Behav., 11: 534--547. Haukioja, E. and Hakala, T., 1979. On the relationship between avian clutch size and life span. Ornis Fenn., 56: 45--55. Kendeigh, S.C., 1973. Energetics of reproduction in birds. In: D.S. Farner (Editor), Breeding Biology of Birds. National Academy of Sciences, Washington, DC, pp. 111--117. Klomp. H., 1970. The determination of clutch-size in birds: a review. Ardea, 58: 1--124. Lack, D., 1954. The Natural Regulation of Animal Numbers. Clarendon Press, Oxford. Lack, D., 1966. Population Studies of Birds. Clarendon Press, Oxford. Murton, R.K. and Westwood, N.J., 1977. Avian Breeding Cycles. Clarendon Press, Oxford. Murton, R.K., Thearle, R.J.P. and Coombs, C.F.B., 1974. Ecological studies of the feral pigeon Columba livia var. III. Reproduction and plumage polymorphism. J. Appl. Ecol., 11: 841--854. Pinowski, J. and Kendeigh, S.C., 1977. Granivorous Birds in Ecosystems. Cambridge University Press, Cambridge, International Biological Program 12. Ricklefs. R.E. and Bloom, G., 1977. Components of avian breeding productivity. Auk, 94: 86--96. Walsberg, G.E. and King, J.R., 1978. The energetic consequences of incubation for two passerine species. Auk, 95: 644--655. Whitman, C.O., 1919. The Behaviour of Pigeons. Posthumous work edited by H.A. Carr, Carnegie Institute, Washington.