Breeding Ecology of the Black-eared Kite Milvus migrans lineatus in the Nagasaki Peninsula, Kyushu Kimiya KOGA, Satoshi SIRAISHI* and Tern Aki UCHIDA Zoological Laboratory, Faculty of Agriculture, Kyushu University 46-06, Fukuoka 812 The Black-eared Kite Milvus migrans is one of the world's most successful and numerous birds of prey and occurs as a common resident in Japan. In Europe and India, there have been extensive studies on the kite's breeding ecology, including pair density and breeding success (FICZYNSKI & WENDLAND 1968, MEYBURC 1969, DESAI & MALHOTRA 1979, FIUCZYNSKI 1981). In Japan the ecology and parental behaviour were studied in a mountainous region (HANEDA& KOIZUMI 1965), but no information has been available on the pair density and productivity of the kites nesting in the vicinity of a fishing-port, which is suitable for breeding of the kite because of food abundance. The purpose of this study is to investigate the number of pairs, nesting tree species, clutch size, number of fledglings and parental behaviour of Black-eared Kites M. m. lineatus living near a fishing-port, and to discuss our results in relation to the food availability in a fishing-port and plenty of trees on the nearby hill as important environmental factors for dispersion of pairs and breeding success. MATERIALS AND METHODS A large number of Black-eared Kites inhabit the Nagasaki Peninsula in Nagasaki Prefecture, Kyushu. During the breeding season, mating and territorial defence of the kites occur here and there around fishing-ports at the southern edge of the peninsula. The present study was carried out in part of a hill (ca. 0.4 km2) neighboring the Wakimisaki fishing-port during the periods from February to July in 1983-1986. The dominant tree species in the study area is Castanopsis cuspidata; there are also small stands of Quercus glauca, Persea thunbergii or Q. acutissima. A communal roost site of 40-50 non-breeding kites was located within the study area. Since the pairs of the kites in our study area depended mainly on fishes (KOGA & SHIRAISHI 1987) and many kites foraged in the fishing-port, the fishing-port probably provided abundant food to the kites and served as the communal feeding area. In order to estimate the pair density in the study area, the number of pairs was counted in 1985 and 1986 by watching mating behaviour, courtship feeding, and * Renrint requests to the second author.
58 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. Vol.38 J. Ornithol. No.2 territorial defence. Efforts were also made to find as many of their nests as possible. Altogether 32 nests were examined: one nest in 1983, eight in 1984, 12 in 1985, and 11 in 1986. The laying date of the first egg was inferred on the basis of changes in the behaviour of the female parent, and the number of eggs in the nest was counted about one week after the presumed laying date of the first egg. To ascertain the number of hatchlings, the nest was visited at the expected hatching date of the first egg (31-32 days after the presumed laying date) and then checked at an interval of 2-3 days until all eggs of the clutch hatched. When the eggs did not hatch 2-3 days after the expected dates, subsequent visits to the nest were made at intervals of 7-10 days. When the eggs had already hatched on the expected hatching date, the hatching date was calculated from the presumed age of the nestling, which was estimated by fitting the tarsus and culmen lengths to their growth curves in the known-age nestlings, or by assessing the phase of plumage development. All nests were visited at least twice in the nestling period (2-3 weeks and 6-7 weeks after hatching of the first nestling), and some of them were visited frequently to examine nestling growth and parental care. In order to determine the fledging success, daily observations were made after 52-56 days of the first nestling. Nests containing at least one egg were termed 'active'. The behavioural data of the parents from incubation to the post-fledging period (from March to July) were obtained from one nest in 1985 and two in 1986. Of two eggs laid in each nest, only one egg hatched, and the three nestlings fledged at the age of 61 days on an average. These nests were in direct sunlight from about 08:00 to 15:00. The observation was conducted through the window of a blind set on an opposite side of the ravine, 150-230m away from the nest. A binocular (8 *30) and telescopes (25* and 60*) were used for the observations, the duration of which was two hours at minimum, 13 at maximum, but commonly five to six between 06:00 and 19:00. The activities of the parents were classified into two categories, i.e. within and outside the territory. The activities within the territory consisted of nest maintenance, incubation or brooding, sitting and standing on the nest, feeding young (prey animals are tore into small pieces of flesh and then passed to the young), mating, courtship feeding (transfer of flesh pieces from the male to the female), feeding, collecting nest materials, perching on branches, uttering the alarm on the branches (screaming against intruders), soaring with or near intruders, aggressive flights (chasing, diving, and/or kicking with feet against intruders), and miscellaneous flights. The activities outside the territory included foraging, collecting nest materials, and soaring around the territory. The behavioural data were obtained from the three nests, but they were combined and then analysed in accordance with the following three periods: the incubation period (from the laying day to one day before hatching); the nestling period divided into the early nestling phase (from the hatching day to 19 days after hatching), the middle nestling phase (20-39 days), and the late nestling phase (from 40 days after hatching to one day before fledging); the post-fledging period separated into the early post-fledging phase (from the fledging day to subsequent 29 days) and the late post-fledging phase (30-ca. 60 days after fledging).
September] Breeding Ecology of the Black-eared Kite 59 1989 RESULTS 1) The number of pairs and nesting tree species Within the study area of ca. 0.4 km2, 33 pairs were found in both 1985 and 1986 (Fig. 1). Of these 33 pairs, 31 and 29 nests were discovered in 1985 and 1986, respectively. The mean distance to the nearest nest was 80±40m (range 50-150m) in 1985 and 80±30 m (50-180m) in 1986. During the study period in 1983-1986, 77 nests were built on 17 tree species (Table 1). Dominant C. cuspidata trees were most frequently used. The mean nest height from the ground was 7.1±2.0 m (range 3.5-14.4m) for 71 nests (six nests fell from the tree before measurement). 2) Clutch size and the number of fledglings Of the 32 nests examined, 28 were active nests containing at least one egg. The clutch size ranged from one to three eggs and averaged 2.2 eggs per active nest (Table 2). At 26 nests, one or more nestlings hatched, and 24 of the 26 nests produced at least one fledgling (Table 3). The mean number of fledglings was 1.0 per nest (per pair) and 1.1 per active nest. Of 61 eggs laid, 18 failed to hatch: 10 disappeared from the nests, two addled, two were broken, one contained a dead embryo and three were not successful with unknown causes. Of the 43 nestlings hatched, 11 failed to fledge: five disappeared, three died of diseases, two died by sibling aggression, and one was killed Fig. 1. Map showing the location of the study area (a solid square in the inset) where the number of pairs was counted in 1985 (above) and 1986 (below). Thick solid line= boundary of the study area; broken line=ridges of the hill; solid circle=nest sites; P= pairs whose nest sites were not located; R=communal roost of non-breeding kites.
60 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. VoI J. Ornithol..38 No.2 Vol.38.No.2 Table t. Tree species used by Black-eared Kites for nesting during the study period in 1983-1986. Table 2. Frequency distribution and mean of the clutch size in 28 active nests1 of Black-eared Kites. 1 Nests containing at least one egg. Table 3. Breeding performance of Black-eared Kites. 1 See Table 2. 2 Nests from which at least one young fledged.
September] 1989 Breeding Ecology of the Black-eared Kite 61
62 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap. Vol J. Ornithol.. 38 No. 2 Vol.38.No.2 Table 5. Number of prey animals foraged per hour within or outside the territory by parent Black-eared Kites. 1 Numerals in parentheses show the number of prey animals obtained during the observation. probably by the weasel. Several pairs of the Jungle Crow Corvus macrorhynchos also occurred in the study area, and interference with the kite's pair was observed only once. Accordingly, disappearance of eggs and nestlings might be partially blamed on the crow, although there was no direct evidence supporting this presumption. 3) Behaviour of the parents The female parent remained within the territory for about 92-99% of the daytime during the time from the incubation period to the early post-fledging phase and for about 44% during the late post-fledging phase (Table 4). The female parent rarely soared in the incubation period and the early nestling phase; she spent most of the daytime on her nest. During the middle nestling, early nestling and early postfledging phases, the female parent tended to increase the time spent in flying and in perching on the branches within the territory. On the other hand, the male parent was present within the territory for approximately 44-63% of the daytime through the time from the incubation period to the post-fledging period; he perched on the branches for about 26-41% of the daytime. The egg was incubated by either the female or the male parent for 97% of the daytime. However, the female parent undertook almost all the daytime incubation (about 90% of the daytime); the male parent incubated the egg only when the female parent was feeding or resting on the branches. The nestling was brooded by the female parent and fed chiefly by her. The male parent also gave the pieces of food to the nestling, but he devoted less time to feeding the young than did the female parent. The time required for the parents to feed the young decreased gradually towards the end of the breeding season. Foraging prey animals was responsible to the male parent during the incubation period and the early nestling phase (Tables 4, 5). In the subsequent four phases, the female parent also hunt within and near the territory, but almost all the prey was supplied by the male parent probably in the fishing-port. DISCUSSION 1) Pair dispersion Diurnal raptors vary in the dispersion pattern of pairs from solitary species,
September 1989 Breeding Ecology of the Black-eared Kite 63 whose pairs widely space themselves out, to colonial species (NEWTON 1979). In general, most raptor species, feeding on live vertebrates, defend wider areas including the nesting territory and hunting places, whereas scavengers such as Ruppell's Griffons Gyps rueppellii breed in colony and forage gregariously (HOUSTON 1976). Black-eared Kites take a great variety of prey from small mammals to reptiles, fishes, insects and carrions (KOGA & SHIRAISHI 1987), exclusively defend a small radius of the nest and often forage with other individuals in feeding areas near the nesting territory (HANEDA& KOIZUMI 1965). In other words, the dispersion pattern of the kites is intermediate between those of the typically solitary species such as Accipiter spp. and the typically colonial species. Accordingly, it is possible that the pairs of Black-eared Kites may nest close together as compared with the diurnal raptors having wider territories. The pair density also varies with regions even in a given species in relation to prey density and the availability of nest sites. The nests of Black-eared Kites are usually solitary and well separated from one another (BROWN& AMADON 1968), but are found also within a very short distance of one another in some food-abundant places (FIUCZYNSKI& WENDLAND 1968, MEYBURG 1969, DELIBES CASTRO 1975). In M. m. govinda occurring in India the number of pairs in the city of Delhi (ca. 150 km2) is estimated at 2,400 in total; the majority of the pairs breed in tree-covered areas where the amount of food available to the kites is plentiful, but the pair density is low in areas with sparse trees and/or poor food supply (GALUSHIN 1971). Therefore, aggregation of the Black-eared Kite's pairs in our study area is probably due to the following two environmental factors of the habitat, i.e. abundant food available at the fishing-port and plenty of trees suitable for nesting in the nearby forest. 2) Breeding success Available information indicates that the number of fledglings per pair of the Black-eared Kite is 0.9-1.2 in different localities (Table 6). With knowledge of the annual mortality rates for adults (Am) and juveniles (Jm) and of the age of the first breeding, it is possible to calculate the average number of fledglings which each pair must produce annually to maintain a stable population (recruitment rate: r) (HENNY et al. 1970). The kite can raise the young for the first time at the end of the second year of life, so that the following formula is used for it. r= 2Am (1-Am)(1-Jm) In Europe, the values of Am and Jm derived from ring recoveries in M. m. migrans are 0.25 and 0.30, respectively (SCHIFFERLI 1967), and consequently the recruitment Table 6. Breeding success of the Black-eared Kite in different areas.
64 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap.J.Ornithol.Vol.38 No.2 o.2 rate is calculated at 1.1 young per pair, which approximately coincides with the actual breeding rates examined in various regions (Table 6). From this, it is likely that the recruitment rate of 1.0 young per pair is sufficient for maintaining a stable population in the Black-eared Kites in our study area. 3) Behavioural pattern of the female parent In M. m. govinda inhabiting India, the male parent perfoms about 30% of incubation. On the other hand, the male parent of the same species in other regions barely shares incubation with the female parent (HANEDA& KOIZUMI1965, MEYBURG 1967, present study). In the Black-eared Kite, the female parent usually broods her nestlings. However, some male parents occasionally spend his time in brooding; unlike other raptors, the male parent frequently feeds the young directly (HANEDA& KOIZUMI1965, KOGA & SHIRAISHI1987). During the nestling period, the female parent behaves responding to needs of the young. While the young are unable to control their body temperature, the female parent must brood them almost continuously; as the nestling develops its thermoregulatory ability, the female parent decreases gradually her time spent in brooding, and while the female parent does not brood the nestling, she remains near the nest; the male parent supplies all of the food for his mate and nestlings during this period (NEWTON 1979, KOGA et al. 1989). Thereafter, both parents must get enough food to fill the increasing demand of the growing nestlings. If the male parent is able to provide his family with enough food by himself, the female parent needs not fly out of the vicinity of the nest in order to obtain prey animals; if the male parent is undependable, the female parent must turn out from the nest to hunt in places at a considerable distance (NEWTON1978, 1979, Moss 1979). The female parent of the Black-eared Kite breeding near a river at the mountainous region in Japan shares with the male parent in foraging during and after the early nestling phase, and spends approximately 15-24% of her daytime outside the territory (HANEDA & KOIZUMI1965). In contrast, the female parent in our study area foraged in the vicinity of the nest during and after the middle nestling phase and remained within the territory for almost all her time throughout the nestling period. Such regional variations in the behavioural pattern of the female parent are probably due to the differences in the food availability among the areas concerned. Thus, the male parent in such an area provided with abundant food as in our study area can obtain enough food to raise at least one young, and consequently the female parent does not need to forage outside the territory. From the above considerations, it is concluded that in the area with a plenty of food and nesting trees, the Black-eared Kite can nest aggregatively and produce enough young to maintain a stable population. Furthermore, since the male parent can supply his family with enough food, the female parent needs not forage during the time from the incubation period to the early post-fledging phase, and spends almost all her time within the territory. ACKNOWLEDGEMENTS We are deeply indebted to Prof. T. SENTA,Prof. Y. MIYA, and Dr. A. ISHIMATU, Nagasaki University, for a variety of kindness; to Prof. E. W. JAMESON, JR., University of California, for comments on the manuscript; to Dr. T. SETSU,Miyazaki Forests, Faculty of Agriculture, Kyushu University for assistance in identification of nesting tree species.
September] 1989 Breeding Ecology of the Black-eared. Kite 65 SUMMARY During the periods from February to July in 1983-1986, the breeding ecology of the Blackeared Kite Milvus migrans lineatus was studied in the vicinity of the Wakimisaki fishing-port, situated at the edge of the Nagasaki Peninsula, Nagasaki Prefecture, Kyushu. The results obtained are summarized as follows: 1) In 1985 and 1986, the number of pairs inhabiting the study area (ca. 0.4 km2) was found to be 33 each year. Such aggregation of pairs seemed to be due to abundant food available at the fishing-port and plentiful trees suitable for nesting on the nearby hill. 2) The breeding success was determined based on 32 nests examined in 1983-1986. Of the 32 nests, 28 contained at least one egg, and the mean clutch size was 2.2. At least one nestling fledged at 24 nests. The mean number of fledglings was 1.0 per nest, and this breeding productivity seemed sufficient to maintain a stable population. 3) The behaviour of the parents was observed during the period from incubation to postfledging. The female parent spent almost all the time within the territory until the early postfledging phase. Although she resumed to hunt within or near the territory during and after the middle nestling phase, the prey animals were chiefly foraged by the male parent, suggesting that in such an area provided with abundant food, the male parent was able to supply enough food for his family by himself. 4) From the above it is concluded that in an area with a plenty of food and nesting trees, the kite can nest aggregatively and produce sufficient young to maintain a stable population, and that the female parent remains within the territory during the time from the incubation period to the early post-fledging phase because of the sufficient supply of food by the male parent. LITERATURE CITED BAKER-GABB, D. 3., 1983. The breeding ecology of twelve species of diurnal raptor in northwestern Victoria. Aust. Wild[. Res. 10: 145-160. BROWN, L. H., & D. AMADON, 1968. Eagles, hawks and falcons of the world 1. London, Country Life Books. DELBES CASTRO, M., 1975. Alimentacion del Milano Negro (Milvus migrans) en Donana (Huelva, Espana). Ardeola 21: 183-207.
66 K. KOGA, S. SHIRAISHI and T. A. UCHIDA [Jap.J.Ornithol.Vol.38 VNo.2 ol.38 No.2 DESAI, J. H., & A. K. MALHOTRA, 1979. Breeding biology of the Pariah Kite Milvus migrans at Delhi Zoological Park. Ibis 121: 320-325. FIUCZYNSKI, D., 1981. Berliner Milan-Chronik (Milvus migrans and Milvus milvus). Beitr. Vogelkd. 27: 161-196. FIUYNSKI, D., & V. WENDLAND, 1968. Zur Populationsdynamik des Schwarzen Milans (Milvus migrans) in Berlin Beobachtungen 1952-1967. J. Orn. 109: 462-471. GALUSHIN, V. M., 1971. A huge urban population of birds of prey in Delhi, India. Ibis 113: 522. HANEDA, K., & M. KOIUMI, 1965. Life history of the Black-eared Kite (Milvus migrans lineatus). I. Breeding season. Jap. J. Ecol. 15: 199-208 and 221-228. (In Japanese with English summary.) HENNY, C. J., W. S. OVERTON, & H. M. WIGHT, 1970. Determining parameters for populations by using structural models. J. Wildl. Manage. 34: 690-703. HOUSTON, D. C., 1976. Breeding of the White-backed and Ruppell's Griffon Vultures, Gyps africanus and G. rueppellii. Ibis 118: 14-40. KOGA, K., & S. SHIRAISHt, 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 Blackeared Kite, Milvus migrans lineatus. J. Fac. Agr., Kyushu Univ. 33: 235-242. MEYBURG, B: -U., 1967. Beobachtungen zur Brutbiologie des Schwarzen Milans (Milvus migrans). Vogelwelt 88: 70-85. 1969. Die Besiedlung des Naturschutzgebietes Kuhkopf-Knoblochsaue mit Greifvogeln im Jahre 1967. Orn. Mitt. 21: 223-230. Moss, D., 1979. Growth of nestling Sparrowhawks (Accipiter nisus). J. Zool., Lond. 187: 297-314. NEWTON, 1., 1978. Feeding and development of Sparrowhawk Accipiter nisus nestlings. J. Zool., Land. 184: 465-487. 1979. Population ecology of raptors. Berkhamsted, T. & A. D. Poyser. SCHIEFERLI, A., 1967. Vom Zug schweizerischer and deutscher Schwarzer Milane Milvus migrans nach Ringfunden. Orn. Beob. 64: 34-51. LLAY, J.-M., 1976. Les rapaces THIO d'une zone de contact savane-foret en Cote-d'Ivoire: Modalites et succes de la reproduction. Alauda 44: 275-300. (Received 31 February 1989)