Growth and Development of the Black-eared Kite Milvus migrans lineatus

Jap. J. Ornithol. 38: 31-42, 1989 Growth and Development of the Black-eared Kite Milvus migrans lineatus Kimiya KOGA, Satoshi SHIRAISHI* and Teru Aki UCHIDA Zoological Laboratory, Faculty of Agriculture, Kyushu University 46-06, Fukuoka 812 Since growth and development are closely related with a mode of life in a given species, the study on such events is important for understanding its life cycle. Nevertheless, there have been few researches on the growth and development of the Black-eared Kite Milvus migrans nestlings, except for reports of DESAI & MALHOTRA (1977) on changes in body dimensions and behavioural development in ten captive nestlings of a subspecies, M. m. govinda, and of KOGA et al. (1989) on the weight increase in a captive nestling of another subspecies, M. m. lineatus. The purpose of this study is to describe the pattern of growth and development in wild Black-eared Kites and to discuss the specific characters of this species by comparison with those in other diurnal raptors. MATERIALS AND METHODS Data on the body weight and outermost primary length of Black-eared Kite nestlings were taken from known-age, nine nestlings at four nests (Nests 1-4) in the vicinity of the Wakimisaki fishing-port, situated at the southern edge of the Nagasaki Peninsula, Nagasaki Prefecture, during the breeding season in 1984. We recorded the development of body plumage by noting the age in days dating from the time when the second down emerged from the sheaths, and when body feathers on various parts of the body firstly emerged from the sheaths and became noticeable. The data on the behavioural development of nestlings were obtained from four nestlings at two nests (Nests 1 and 2). These nests were observed from a blind approximately 15 and 35 m away from the nests, respectively, using a binocular (7*35) and telescopes (25*, 60*). To compare the ranking of the nestlings within a brood in relation to the body weight increase and the growth of the outermost primary with the hatching order within the brood, linear regression equations were calculated for the straight line portions of the growth curves, and differences between the siblings within broods in the slopes and elevations (i.e. the vertical portions on a graph) of the lines were examined in accordance with the method of ZAR (1984). Furthermore, to allow interspecific comparisons of the patterns in the * Reprint requests to the second author.

32 weight K. increase, the data KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. on the body weight were matched by J..Ornithol. 39 No. 1Vol a logistic equation, where W is nestling body weight at the age t (days), A is asymptotic body weight, is the age at which the rate of growth is maximum (inflection point), and tik is a growth rate constant. RICKLEFS'(1967) method was adopted to fit the equation to the 67th growth data. RESULTS 1) Clutch size, brood size, and fledging age in days Nests 1-3 each contained two eggs, Nest 4 had three eggs, and all eggs hatched. The hatching intervals between the first and second nestlings were two days at Nests 1 and 2, and three days at Nest 3. At Nest 4, there were the hatching intervals of three days between the first and second nestlings and between the second and third nestlings. The second nestling at Nest 1 died of disease at 40 days after hatching. At Nest 3, the second nestling starved to death at 11 days of age, and the first nestling flew out of the nest at 54 days after hatching, because the investigator's climbing to the nest supplied the stimulus for the take-off. The first nestling at Nest 1 fledged on 61st day, the first and second nestlings each at Nest 2 on 64th and 61st days, and the first, second and third nestlings at Nest 4 on 68th, and 73rd days, respectively. 2) Growth The rate of weight gain increased slowly for the first week, then more rapidly and linearly, and tapered off with some or great day-to-day fluctuations after 5 to 6 weeks (Fig. 1). The logistic equation reasonably approximated the body weight data for the individual nestlings. The data were fitted also by GOMPERTZand BERTALANFFY equations, but the logistic equation gave a closer fit to the data. The growth rate constant (K), the age at the inflection point (ti) and the asymptotic body weight (A) of the logistic equation averaged 0.133 (SD=±0.018, n=8), 23.8 days (SD=±3.4), and 965g (SD=±60), respectively. Only the straight line portion of the growth curve was used for a statistical comparison between the siblings within each brood. At Nest 1, there was no difference between the slopes of the lines for the first nestling (10th-38th days) and the second one (12th-36th days) (t=0.254, P>0.05), but the elevation of the line for the first nestling was higher than that for the second one (t=3.890, P<0.05); that is, the rapid weight gain of the first nestling occurred earlier than that of the second one. At Nest 2, the slope of the line for the first nestling (9th-36th days) was greater than that for the second one (12th-42nd days) (t=4.150, P<0.05). At Nest 4, the slope of the line for the first nestling (7th-30th days) was steeper than that for the second one (15th-46th days) (q=4.181, P<0.05). At this nest no difference in the slope of the line (q=1.457, P>0.05) was detectable between the second and third nestlings (18th-43rd days), but the elevation of the line for the second nestling was higher than that for the third one (q=5.297, P<0.05). The length of the outermost primary, which was measured until about 50-55 days after hatching, increased linearly at the rate of about 5-6 mm/day (Fig. 2). The slopes of the linear regressions did not differ statistically between the siblings within broods (Ps>0.05), but the elevations of the regression lines showed a significant difference between the siblings (Ps<0.05). These indicated that the emergence of the

July ] 1989 Growth and Development of the Black-eared Kite 33 Age in days Fig. 1. Changes of body weight in the Black-eared Kite nestlings. =first nestling; O= second nestling; *=third nestling. outermost primary was delayed for the younger nestling as compared to the older one. 3) Plumage and behavioural development At hatching the nestlings were covered with the first down (prepennae down), which was sepia on the back, black around the eyes, and buff on the head, neck and underparts. The first down was gradually replaced by the brownish-gray second down (preplumulae down). By 9th-12th days (mean=11 days, n=7) the second down began to appear on the whole body, except for the top of the head. The body feathers on the back, neck and wing firstly emerged on 18th-22nd days (mean =20 days, n=7). The feathers on the top of the head became noticeable between 24th and 29th days (mean=25, days, n=7). By about 40th day of age, the second down was scarcely visible on the body. However, the emergence of the body feathers in the third nestling at Nest 4 tended to be retarded as compared with that of the other nestlings. The body feathers on the back of the third nestling grew on 20th day, and the feathers on the wings, neck and top of the head on 30th-32nd days. The third nestling was almost entirely covered with the body feathers at about 50th day. The four nestlings from Nests 1 and 2, which were used for behavioural observa-

34 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. J. Ornithol. Vo1.38 No.l Age in days Fig. 2. Growth of the outermost primary in the Black-eared Kite nestlings. Symbols are the same as in Fig. 1. tions, developed feeding skills gradually. They picked up fallen pieces of food from the bottom of the nest cup and fed on them on 21st-27th days (mean=24 days, n= 4). They began to tear flesh from prey animals on 33rd-39th days (mean=37 days, n=4), and to eat them on 45th-47th days (mean=46 days, n=3) as adults do. With respect to the development in other skills, the nestlings began standing on both legs on 17th-19th days (mean=18 days, n=4) and flapping their wings on 27th-31st days (mean=8 days, n=4). They tried to stand on one leg on 29th-35th days (mean= 32 days, n=3), and stood stably on one leg and became possible to scratch the face and head with the other leg in a standing position on 33rd-39th days (mean=36 days, n=4). They moved onto branches near the nest on 50th-51st days (mean=50 days, n=3), and then spent a lot of time in resting on the branches with increasing age. DISCUSSION 1) Comparison of the growth within a brood Asynchronous hatching is a common phenomenon in birds, particularly among top-level consumers such as birds of prey, and it is regarded as an adaptation to unpredictable food supply (LACK 1954, O'CONNOR 1978). On the other hand, sibling aggression, which is known in many diurnal raptors, is considered another

July]1989 Growthand Development of the Black-earedKite 35 adaptation to enhance the function of asynchronous hatching (NEWTON 1977). In other words, the younger sibling may soon die as a result of sibling aggression (brood reduction), when the amount of food supplied by the parents is short owing to lack of hunting and breeding experience, or to scarcity of food in the breeding habitat. Consequently, wastage of food and energy on the young destined to die is minimized, thereby increasing the reproductive success of the parents (STINSON1979, EDWARDS& COLLOPY1983). The oldest nestling of the Black-eared Kite attacks its smaller nest-mates only at the time of great hunger during feeding, and monopolizes parent-provided resources (KOLA & SHIRAISHI 1987). Accordingly, at the nest where the rate of weight gain did not differ between two siblings (Nest 1), the parents might have supplied each nestling with enough food; at the nests where the younger nestling(s) exhibited lower weight gains than the older one (Nests 2 and 4), or where the younger nestling died of starvation (Nest 3), the parents might have been unable to feed the younger adequately. Judging from the fact that the nest-sites of the four nests were situated under the same feeding condition in relation to food availability, the foraging ability of the parents might vary with the individual, and this was presumed to be one of the factors which influence the growth and survival of younger nestlings. 2) Interspecific comparison of growth and development Growth equations which can be fitted to growth curves are powerful and useful tools for making interspecific comparisons of growth (RICKLEFS 1967, 1968). Three equations, i.e. the logistic, GOMPERTZand BERTALANFFYequations, are commonly used to apply growth curves. Each of the growth equations has three parameters: growth rate constant (K), age at the inflection point (ti), and asymptote of the growth curve (A). Among them, the growth rate constant is directly comparable between species, because it is an overall measure of growth rate. Strictly speaking, the rate constants from different growth equations cannot be compared directly. However, a value of the growth rate constant for a certain equation can be converted to correspond with values for different equations (RICKLEFS 1973). Body weight has been considered to be the single criterion for the growth of the whole organism (RICKLEFS 1979a), and it has been common to utilize body weight as an index of growth in vertebrates (RICKLEFS1968, 1973, CASE 1978). Therefore, we also employed here the growth rate constants of growth equations fitted to the growth curves of body weight for comparisons among species. Birds are usually divided into two types according to their conditions at hatching: precocial and altricial. The young of the altricial birds are incapable of maintaining their body temperatures and walking for some time after hatching, and depend on their parents for food until they become independent. In contrast, the precocial young hatch in an advanced state from the egg, have high capabilities of thermoregulation and locomotion and take food by themselves soon after. To be exact, the Black-eared Kite represents a semi-altricial state characterized by the nestlings covered with down at hatching. In general, altricial and semi-altricial birds grow more rapidly than do precocial ones. The present study revealed that the observed growth rate constant for the body weight of the kite (0.133) was about two to seven times greater than that of the following similar-sized precocial species: Mallard Anas platyrhynchos (0.083), Redhead Aythya americana (0.060), Ruddy Shelduck Tadorna ferruginea (0.019), Pheasant Phasianus colchicus (0.047) (RICKLEFS 1973). The reason

36 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. J. Ornithol.Vol.38 No. 1 for such relationships between the growth rate and the mode of development has been explained as follows. 1) Since the precocial chicks consume more of their energy for activity and thermoregulation, the energy for growth is limited (RICKLEFS1968). 2) The growth rate of the body weight in chicks must be constrained by the growth rate of skeletal muscles, because the tissue, providing for heat production and for locomotory power in flying, walking and swimming, makes up a larger proportion of the adult body than does any other tissue. The postnatal growth of the muscles is accompanied with proliferation of undifferentiated cells, and their functions are directly related to the proportion of differentiated cells in the tissue; in this connection, the proportion of the undifferentiated cells is lower in the precocial neonates than in the altricial ones, and thus altricial chicks grow faster than do the precocial ones (RICKLEFS1973, 1979a, 1979b). A negative correlation is found between the logarithms of growth rate constant and asymptotic body weight (regarded as the adult body weight) in altricial passerine birds and semi-altricial raptors, and much of the variations in the avian growth rate constant is attributable to the adult body size (RICKLEFS 1968). However, included in his analysis are only five species of the order Falconiformes, and none has reported the equation correlating the growth rate constant with the asymptotic body weight for diurnal raptors. Therefore, in order to clarify whether or not the pattern of weight increase in the Black-eared Kite differs from those of other diurnal raptors, it is necessary to know the relationship between the growth rate constant and the asymptotic body weight in diurnal raptors. In large diurnal raptors, the prey delivery rate per nestling (number of prey animals delivered to one nestling per day) for the species which rear only one young (B1 species=species with brood size of one, e.g. the Crowned Eagle Stephanoaetus coronatus) is lower than those for the species raising two or more young (B2 species, e.g. Black-eared Kite and Bald Eagle Haliaeetus leucocephalus). The young of the B1 species adaptively depress their growth rate in order to correspond to poor food supply, thus growing more slowly than do those of the B2 species (BORTOLOTTI1986). The parents of the Black-eared Kite can fledge even two or more young so that the relationship between the growth rate constant and the asymptotic body weight was examined among 27 species of the B2 diurnal raptors (Fig. 3 and Appendix) and formulated as follows: This equation almost completely coincided with the RICKLEFS' (1968) one (K= 1.11 A-0.278). Based on the equation for diurnal raptors, the Black-eared Kite had an expected growth rate constant of 0.169. The observed growth rate constant for the body weight (0.133) was slightly lower than the expected value, but it lies between the 95% confidence limits for the regression line (Fig. 3). Nestlings must complete various functions of many characters by the end of the nestling period. The development is influenced by habitat, reproductive pattern, and so forth. Thus, it is important to investigate the changes in both external characters and behaviours. Of the various developmental events, only the following four items were able to be compared among 9 species of the order Falconiformes: 1) the emergence of the body feathers, 2) the initiation of food tearing (self-feeding), 3) standing on both legs, and 4) stable standing on one leg (Table 1). The age in days should not be used as an indicator for making direct comparisons between species, because the duration of the nestling period varies with the species. There-

July 1989] Growth and Development of the Black-eared Kite 37 Asymptotic body weight (g): A Fig. 3. Relationships between the growth rate constant and the asymptotic body weight among diurnal raptors. Dashed lines show the 95% confidence limits about individual predictions. Each number corresponds to the number given for each species which is listed in Appendix. Table 1. Comparison of the percentages of nestling weight to the asymptotic body weight (A) in 9 species of the order Falconiformes. 1 The percentages of nestling weight are calculated by us using the growth equation determined by three parameters (see Appendix), except for those which were described in H. leucocephalus by BORTOLOTTI (1984), and the age (in days) shows the time when the following events occur; B=appearance of the body feather, T=tearing of food, S=standing on both legs, O=standing on one leg: the age is cited from NEWTON (1978) for A. nisus, from ELLIS (1979) for A. chrysaetos, and from references in Appendix for other species. fore, the interspecific comparisons of the developmental events were conducted, using the percentage of nestling weight to asymptotic body weight. Each species reached more than 80% of the asymptotic body weight at the beginning of self-feeding and standing on one leg, suggesting that the nestlings must almost

38 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. J. Ornithol. V ol. 38 No. 1 fully grow their body to perform these behaviours. On the other hand, in large raptors the emergence of the body feathers and the initiation of standing on both legs tended to occur at an earlier growth stage than in small ones, and the timing of these two events in the Black-eared Kite, one of the medium-sized raptors, nearly agreed with that in large species. Although this reason remains unanswered, it is likely that the Black-eared Kite nestlings benefit from such early development of the body feathers. In raptors, the male parent usually provides the female parent and the nestling(s) with all or almost all the food during the early nestling period (NEWTON 1978, LEVENSON1979, COLLOPY1984). Because the food requirements of nestlings increase with their growth, the female parent must assume the responsibility for foraging together with the male parent to supply the nestlings with enough food during and after the middle nestling period (NEWTON 1979). However, the female parent does not leave the nest until the nestlings acquire homeothermy. Furthermore, she must shade her nestlings from rain, strong wind and direct sunlight, because thermal insulation is not yet well developed until the nestlings feather (BROWN & AMADON 1968, KOGA & SH RAISHI 1987, KOGA et al. 1989). If the female parent leaves the nest for a long time to forage elsewhere in this period, she may increase the risk to her young from inclement weather (FITCH et al. 1946, Moss 1979). Therefore, early development of the body feathers in the kite nestlings allows the parents to prolong their foraging duration from a relatively early time of the nestling period, and thus it probably gives a good nutritive effect on the growth and survival of the nestlings. From the above considerations, it is concluded that the development of the Black-eared Kite is characterized by both the emergence of the body feathers and the initiation of standing on both legs occurring at an earlier growth stage than in small and other medium-sized raptors. ACKNOWLEDGEMENTS We are much indebted to Professors T. SENTAand Y. MIYA, Nagasaki University, for a variety of kindness; to Professor E. W. JAMESON, JR, University of California, for comments on the manuscript; to Mr. K. SHIOYA,a graduate student in our laboratory, for assistance in computer programming. SUMMARY The growth and development of known-age, nine Black-eared Kite nestlings from four nests were investigated in the vicinity of the Wakimisaki fishing-port, situated at the southern edge of the Nagasaki peninsula, Nagasaki Prefecture, in 1984. The results obtained are summarized as follows. 1) The second down appeared on the body by 9-12 days after hatching, and the body feathers emerged at 18-22 days. The nestlings began standing on both legs at 17-19 days and flapping their wings at 27-31 days. They began to eat prey animals by themselves at 45-47 days. 2) Some diurnal raptors rear a young each brood (B1 species) and some others raise two or more young (B2 species). Of the four nests examined, three nests each contained two nestlings, and a nest had three. Therefore, the Black-eared kite belongs to the B2 species. At one nest the younger and elder nestlings increased their body weight at the same growth rate; at two nests the younger sibling(s) gained slower their body weight than did the elder. At the other nest, the younger chick died of starvation. Judging from the uniformity of the environmental condition in relation to food availability among the four nests, it seemed that the foraging ability of the parent kites varied with the individual and influenced the survival and growth of younger

July 1989] Growth and Development of the Blacḵeared Kite 39 sibling(s). 3) The growth rate constant of the logistic equation fitted to weight data for each nestling averaged 0.133. This value did not differ significantly from the expected value of 0.169, which was calculated by the equation correlating the growth rate constant with the asymptotic body weight for 27 species of the B2 diurnal raptors. 4) The emergence of body feathers and the initiation of standing on both legs tended to occur at an earlier growth stage in large raptors than in small ones. In this connection, it was concluded that the Black-eared Kite, in spite of being a medium-sized raptor, possesses about the same developmental pattern as that of the large raptors rather than that of small or other medium- sized ones. LITERATURE CITED BORTOLOTTI, G. R., 1984. Physical development of nestling Bald Eagles with emphasis on the timing of growth events. Wilson Bull. 96: 524-542. - 1986. Evolution of growth rates in eagles: sibling competition vs. energy considerations. Ecology 67: 182-194. BROWN, L. H., & D. AMADON, 1968. Eagles, hawks and falcons of the world 1. London, Country Life Books. CASE, T. J., 1978. On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Quart. Rev. Biol. 53: 243-282. COLLOPY, M. W., 1984. Parental care and feeding ecology of Golden Eagle nestlings. Auk 101: 753-760. DESAI, J. H., & A. K. MALHOTRA, 1977. Growth and development of the Pariah Kite Milvus migrans govinda. Misc. Rep. Yamashina Inst. Ornithol. 9: 88-96. EDWARDS, T. C., JR., & M. W. COLLOPY, 1983. Obligate and facultative brood reduction in eagles: an examination of factors that influence fratricide. Auk 100: 630-635. ELLIS, D. H., 1979. Development of behavior in the Golden Eagle. Wild. Monogr. (70): 1-94. FITCH, H. S., F. SWENSON, & D. F. TILLOTSON, 1946. Behavior and food habits of the Red-tailed Hawk. Condor 48: 205-237.

40 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. J. Ornithol. Vol.38 No.1 KOGA, K., & S. SHIRAISHI, 1987. Parental care of nestlings in the Black-eared Kite Milvus migrans. Jap. J. Ornithol. 36: 87-97. (In Japanese with English summary.) KOGA, K., S. SHIRAISHI, & T. A. UCHIDA, 1989. Acquisition of homeothermy in the Black-eared Kite, Milvus migrans lineatus. J. Fac. Agr. Kyushu Univ. 33: 235-242. LACK, D., 1954. The natural regulation of animal numbers. London, Oxford University Press. LEVENSON, H., 1979. Time and activity budget of Ospreys nesting in northern California. Condor 81: 364-369. Moss, D., 1979. Growth of nestling Sparrowhawks (Accipiter nisus). J. Zool., Lond. 187: 297-314. NEWTON, I., 1977. Breeding strategies in birds of prey. Living Bird 16: 51-82. 1978. Feeding and development of Sparrowhawk Accipiter nisus - nestlings. J. Zool., Lond. 184: 465-487. 1979. Population - ecology of raptors. Berkhamsted, T. & A. D. Poyser. O'CONNOR, R. J., 1978. Brood reduction in birds: selection for fratricide, infanticide and suicide? Anim. Behav. 26: 79-96. RICKLEFS, R. E., 1967. A graphical method of fitting equations to growth curves. Ecology 48: 978-983. -1968. Patterns of growth in birds. Ibis 110: 419-451. 1973. Patterns of growth in birds. II. Growth - rate and mode of development. Ibis 115: 177-201. -1979a.Adaptation, constraint, and compromise in avian postnatal development. Biol. Rev. 54: 269-290. -1979b. Patterns of growth in birds. V. A comparative study of development in the Starling, Common Tern, and Japanese Quail. Auk 96: 10-30. STINSON, C. H., 1979. On the selective advantage of fratricide in raptors. Evolution 33: 1219-1225. ZAR, J. H., 1984. Biostatistical analysis. 2nd ed. Englewood Cliffs, Prentice-Hall. (Received 15 November 1989)

July1989] Growth and Development of the Black-eared Kite 41