Distribution and Ecology of Birds of Japan!

H!ROYOSHI HIGUCHI,2 JASON MINTON,3 AND CHIEKO KATSURA4

ABSTRACT: The effects of island biogeography are clearly seen in the avi fauna ofJapan. Species composition and distribution reflect Japan's geographic, climatic, vegetational, topographical, and geological characteristics. It is a country composed primarily of mountainous, forested islands that lies off the coast ofa continent rich in bird life. Though Japan has a wide range ofclimates and diverse forest habitats, the terrestrial and freshwater avifauna is de pauperate when compared with species, family, and order diversity on the nearby continent, which is both larger in total area and more diverse in hab itats. However, the bird groups that do have higher species diversity in Japan than in the Asian mainland are seabirds. The large, productive ocean area and small, isolated islands provide them with foraging and nesting sites, and the long geographic range of Japan allows seabirds from both northern and southern regions to nest in the Islands. Island biogeography also affects the ecology of many terrestrial species. Niche shift and expansion of foraging and parasitic behaviors are seen in populations established on islands where the species composition does not include certain competitors. The terrestrial species resident on small islands have developed unique breeding behavior, in com parison with their conspecifics on larger islands, such as smaller clutch size, exaggerated begging behavior, and longer parental care in small-island pop ulations of Varied Tits, Parus varius Temminck & Schlegel.

JAPAN LIES ALONG the east side of the Asian species distribution. Second, the species continent. The long island chain stretches composition of Japan is compared with that from Hokkaido in the north to the South of the Asian mainland. We pay particular West Islands in the south (Figure 1). The attention to the composition at the order, characteristics of Japanese avifauna have family, and species levels. The comparison been described (e.g., Blakiston 1883, Austin yields differences that are explained by the and Kuroda 1953, Brazil 1991), but most of differences in area sizes and habitat between those authors focused on taxonomic aspects Japan and the mainland. and did not discuss ecological relationships. Last, we report some ecological phenom The distribution and ecology of birds are af ena from our fieldwork. Characteristics such fected by the environmental features of birds' as foraging and breeding behavior are in habitat. fluenced by the presence or absence of other In this paper, we review the characteristics competing species. Species existing in areas of Japanese avifauna from the ecological without competitors show ecological shifts point of view. First, we describe the physical with morphological changes allowing them environment on which the Japanese avifauna to take advantage of resources left available depends; then we examine its influence on by the absence of competition. Further, breeding behavior changes for large- and small-island p_opulationsare described, and 1 Manuscript accepted 27 April 1994. climatic explanations are suggested. 2Laboratory of Wildlife Biology, University of To kyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113, Japan. 3Research Center, Wild Bird Society of Japan, 15-8 Features ofthe Japanese Environment Nanpeidai, Shibuya-ku, Tokyo 150, Japan. 4 Japan-China Cooperative Institute for Ornithology, The Japanese island chain and the Asian Nagahama 1-2-6-505, Chuo-ku Fukuoka 810, Japan. continent are separated by the Japan Sea, at 69 Russia

Japan Sea

Island

China Islands

Tokara Ogasawara Islands

Daito Islands ... .. i;,

FIGURE 1. Japan,neighboring islands, and nearby continental Asia.

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distances ranging from 200 to 800 kIn. The main types, broad-leaved evergreen forests in more than 3,500 Japanese Islands cover an the south and deciduous forests in the north. area from Sakhalin in the north, to Taiwan in The majority of Hokkaido and adjacent is the south, the Kurile Islands in the east, and lands is vegetated with typically subarctic the Korean Peninsula in the west. mixed forest of deciduous and coniferous The shapes and sizes of the Japanese Is trees. lands have changed many times in geologic There are both warm and cold currents in history, and most of the Japanese Islands the ocean surrounding Japan. Kuroshio, a were connected to the Asian continent at one southern warm current, flows north and di time (Minato et al. 1965). Honshu, Shikoku, vides at the southern tip of Kyushu, flowing and Kyushu were isolated from the continent into both the Sea of Japan and the Pacific and from Hokkaido, which was the last main Ocean. The cold Oyashio Current moves island to be separated from the continent, south from the subarctic, along the coast of after the latest Pleistocene of ca. 20,000 yr eastern Hokkaido and northern Honshu. ago. Since that time, all the islands have been These interacting currents have made the isolated from the continent and from each coastal and marine regions of Japan ex other. tremely productive (Ching 1991). Japan's terrestrial habitat is heavily vege tated. Forests cover 68% of the land area. Features ofthe Avifauna Relative to The topography of Japan is extremely Environmental Features mountainous, with 70% of the land area in mountain ranges. The altitudinal range is The distribution of avifauna in Japan is from sea level to 3,776 m. a function of the physical environment, Japan lies in three climate zones because particularly its island nature. The avifauna of its long north-south geographic range, of the Islands varies seasonally and region between 24° and 46° N latitude. There are ally. However, forest species predominate subtropical, temperate, and subarctic climate throughout the Islands. The forest landscape regions. The Ryukyu Islands, which are the supports a majority of Japan's terrestrial bird southernmost islands of the Japanese island species. Approximately 100 of the 150 land chain, lie in the subtropical zone. The islands and freshwater bird species are woodland extending northward from the Ryukyus to dwellers, such as hawks, pheasants, wood the southern tip of Kyushu are called the peckers, thrushes, warblers, flycatchers, South-West Islands. The majority of the finches, and buntings. main islands and land area of Japan lies in The seasonal climate of much of Japan the temperate zone. Northern Hokkaido and means that many species are migratory. several associated islands belong to the sub Some are winter or summer visitors, and arctic region north of45° N latitude. others, such as shorebirds, visit Japan only as The southern South-West Islands are cov a migration stopover. Thus, Japan's species ered with subtropical broad-leaved and man composition changes between summer and grove forests. The northern South-West Is winter. The number of species that arrive lands are covered with temperate mixed each season closely matches the number that evergreen forests intergrading with typically leave during the period (Figure 2). southern vegetation. In this latitudinal range, Regional species composition results from but to the east and much more remote, are the geographic situation of the area. The avi the Daito and Ogasawara (Bonin) Islands. fauna of the South-West Islands is influenced They are on the order of 1000 kIn from the by the tropical area and temperate regions. large northern islands of Japan and have no Tropical species such as the einmrmoll neighbors within 500 kIn. Bittern, Ixobrychus cinnamomeus (Gmelin); The temperate zone includes most of the Malay Night Heron, Gorsakius melanolophus main islands of Kyushu, Shikoku, Honshu, (Raffles); Purple Heron, Ardea purpurea L.; and southern Hokkaido, between 31 ° and 42° Barred Buttonquail, Turnix suscitator N latitude. The vegetation consists of two (Gmelin); White-breasted Waterhen, Amaur- 72 PACIFIC SCIENCE, Volume 49, January 1995

N=536

• Resident II Winter visitor ~ Summer visitor 12] Transient 12] Straggler

FIGURE 2. Residential status of Japanese birds as a proportion of five categories. Based on Wild Bird Society of Japan (1982) and Takano (1985).

ornis phoenicurus (pennant); and Red-capped The distribution of species within each region Green Pigeon, Sphenurusformosae (Swinhoe) varies. Island size, island distance from emi (Brazil 1991), intergrade with Palearctic spe gration sources, and chance, as well as island cies such as Woodcock, Scolopax rusticola geology have determined the presence or ab L.; Japanese Robin, Erithacus akahige sence of species. The number of species on (femminck); and Carrion Crow, Corvus co each island differs. For example, in the rone L., in the northern South-West Islands. South-West Islands, 47 species have been In the subarctic region of Hokkaido, identified as resident, but only 17 of these are drastic seasonal variation in temperature found on five or more ofthe six major islands drives many birds south for the winter. But of this group (Ikehara 1991). Figure 3 shows many breeding and resident species of Hok the species-area relationship of the Japanese kaido are closely related to the northern cli Islands. The number of breeding species in mate and do not live elsewhere in Japan. The creases as the area of an island increases. White-tailed Sea Eagle, Haliaeetus albicilla However, in remote islands more than 300 (L.); Common Merganser, Mergus merganser km distant from any main island of Japan, L.; Tufted Puffin, Lunda cirrhata (pallas); fewer species are present than expected from Hazel Grouse, Tetrastes bonasia (L.); Blakis the size of the island. These are good exam ton's Fish Owl, Ketupa blakistoni (Seebohm); ples of island biogeographical theories Three-toed Woodpecker, Picoides tridactylus (MacArthur and Wilson 1963, 1967). (L.); and Willow Tit, Parus palustris L., are The relationship between island size, re breeders not seen south of Hokkaido. These moteness, and species presence is demon species are found on the adjacent Asian con strated by the colonization patterns of tinent, suggesting that Hokkaido was still woodpeckers (Higuchi 1980). The likelihood connected to the continent after Honshu had of their presence on small islands increases been separated. The biogeographical line with island size and proximity to one of the separating Hokkaido- and -Honshu is called main-islands ~Figure 4). -Fer example, the Blakiston's line (fokuda 1970). Japanese Pygmy Woodpecker, Dendrocopus Regional differences in avifauna are clear, kizuki (Temminck), is commonly found on but the effects of island biology are just as islands with an area of 10-99 km2 located strong, though less obvious without study. less than 10 km from a main island. One

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FIGURE 3. The relationship between the number of breeding species and sizes of Japanese Islands. Open circles represent remote islands that are> 300 Ian from any main island of Japan. Scales of the axes are logarithmic (from Higuchi 1979). 74 PACIFIC SCIENCE, Volume 49, January 1995

Picus awokera Dendrocopos leucotos

~100 0 0 0 0 0 0 0 20.0 % 910 912 0/6 0/4 0/10 Q'12 VI -. E 10-99 0 14.3 0 25.0 0 0 0 36.4 .::s:. - OJ.t VI

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FIGURE 4. Frequency distribution of the occurrence of woodpeckers in relation to the size and remoteness of is lands. Islands are placed into 12 classes based on island sizes and distances from the nearest main island. Occurrence rates (%) are calculated by dividing the number of islands in each class where the woodpeckers breed by the total number of islands in that class. The fraction shown at the lower right in each category is the number of islands sur veyed (from Higuchi 1980). hundred percent of those islands have this of relictual populations usually comes about species, but only 12.5% of islands the same through environmental change and inter size located 10-99 km distant from a main specific competition. Many species now con island do. The Japanese Green Woodpecker, sidered endemic were widespread in the past. Picus awokera Temminick, occurs on three During times of environmental change or in main islands and the outlying small islands terspecific competition with newly estab that were connected to the main islands in lished closely related species, these species re the latest Pleistocene. The White-backed treated from their ranges and were effectively Woodpecker, D. leucotos (Bechstein), is isolated in small areas to which they are found only on islands greater than 100 km2 now endemic. It is not easy to distinguish iil area. which of these two processes, speciation or Japan lias a nch endemic avifauna, With isoHHion, is responsible fur endemic Japanese 22 endemic residents or breeders. There are birds. A useful characteristic for determining two methods by which endemic species have which process occurred is the distribution of arisen: through speciation and through isola the species. Endemic species that speciated tion of relictual populations. The formation within an area have close relatives in neigh-

= .1 EELMAM&&!¥ a,¥A@ 4A Distribution and Ecology of Birds of Japan-HIGUCHI ET AL. 75 boring regions. Relict species are charac and Honshu, but its nearest relatives live on terized by a discontinuous distribution of Taiwan (the Mikado Pheasant, S. mikado relatives, because they retreated from a wide [Ogilvie-Grant]), in tropical China in Yun range to small pockets of suitable habitat. nan Province (Mrs. Hume's Pheasant, S. hu Many terrestrial Japanese endemic species miae [Hume]), and in the mountains of cen show the trait of discontinuous distribution tral eastern China (Elliot's Pheasant, S. ellioti and are considered relicts. Ijima's Willow [Swinhoe]) (Higuchi 1987, Sibley and Mon Warbler, Phylloscopus ijimae (Stejneger), roe 1990). breeds only on the Izu Islands off Honshu In contrast, another member of the and on the Tokara Islands in the South-West pheasant family obviously speciated within Islands, 500 km away from the Izus. These Japan. The Green Pheasant, Phasianus ver island populations are probably a more sicolor Vieillot, is endemic on Japan's main primitive species than many other Phyllosco islands (except Hokkaido), and its closest pus species occurring elsewhere and used to relative, the Common Pheasant, P. colchicus be widely distributed (Martens 1980, 1981, L., occurs on the Asian mainland (Delacour Higuchi and Kawaji 1989). Similarly, the 1977, Johnsgard 1986). These nearby pop Lidth's Jay, Garrulus lidthi Bonaparte, of u1ations of a close relative show that the Amami Island has no nearby relatives on Green Pheasant speciated in Japan. the mainland or Japan, but is closely related The origins of some Japanese endemics to the Black-throated Jay, G. lanceolatus are unclear. For example, the Japanese Vigors, of the Himalayas (Yamashina 1941, Wagtail, Motacilla grandis Sharpe, is closely Short 1973, Morioka 1974) (Figure 5). The related to the widely distributed White Wag Copper Pheasant, Syrmaticus soemmerringii tail, M. alba L., and this distribution pattern (Temminck), occurs on Kyushu, Shikoku, suggests that the Japanese Wagtail speciated

Japan

Black-throated Jay

,-, '~IIIIIIIIII"" '.\.;../' China o

Lidth's Jay

FIGURE 5. Distributions of the closely related Lidth's Jay (Garrulus lidthi) and the Black-throated Jay (G. lanceo latus) in Japan and the Himalayas, respectively. The discontinuous distribution is characteristic of relict species. 76 PACIFIC SCIENCE, Volume 49, January 1995 in Japan from the continental White Wagtail. pendix). The number of breeding species re However, the plumage and the courtship be corded in Japan is 248, and there are 972 in havior of the Japanese Wagtail is most sim China. There are no breeding bird orders in ilar to that of the Large Pied Wagtail, M. Japan that are not also present in China. maderaspatensis Gmelin, of India. These Twenty orders are present in China, and 18 characteristics suggest that these two species in Japan. The orders missing from Japan are are closer to each other than to the White Psittaciformes (parrots) and Trogoniformes Wagtail (Higuchi and Hirano 1988), and (trogons), both tropical. Japan's comparative their discontinuous distribution suggests that lack of extensive tropical avifauna explains they are relict species. Which of these inter much of the difference between the Islands pretations is correct is yet to be discovered. l;lnd the mainland at both the order and The biota of Japan is rich in relict en family levels. demics. Besides birds, there are many relict There are 22 families, containing a total of amphibians, reptiles, and mammals (Im 82 species, breeding in China and not in Ja aizumi 1962, 1985, Hikita 1985). pan. Fourteen of these families typically are tropical, and 56 (85%) of their 66 species present in China live in tropical habitats. Comparison ofthe Avifauna of China Some of these tropical families are Psittaci- . and Japan dae (parrots), Trogonidae (trogons), Bucer otidae (hombills), Capitonidae (barbets), The most important biogeographic fea Eurylaimidae (broadbills), and Irenidae tures of Japanese avifauna are those asso (leafbirds). Timaliinae, which is sometimes ciated with the island environments. This be treated as a separate family (e.g., Ali and comes clear when the Japanese avifauna is Ripley 1971, King and Dickinson 1975), is compared with the neighboring continental also a tropical group missing from Japan and avifauna. We use China's breeding bird spe is represented by 124 species in China. Sev cies as a representative of the avifauna of the eral other families absent from Japan contain Asian continent. China is a political region, grassland or arid-adapted species, such as and its size and habitats are remarkably dif Pteroclididae and Otidae. ferent from those of Japan, but we compare There is only one family present in Japan the two regions for three reasons: (1) main that is absent from China. Meliphagidae is land China is a major source for birds immi represented by a single endemic species from grating to Japan, (2) some closely related the Ogasawara Islands, the Bonin Islands species exist in Japan and on the mainland as Honeyeater, Apalopteron familiare (Kittlitz). far away as the Himalayas (e.g., Lidth's Jay However, there is some taxonomic un and Black-throated Jays), and (3) the general certainty about its status (Higuchi 1978). distribution of China's avifauna has been At the species level, the avifauna of Japan well studied by Cheng (1976, 1987) and Fan is quite depauperate. The largest differences (1990). As is common for continental island come from families that exist in both China chain avifauna, the birds of Japan are a sub and Japan, but that have fewer closely re set of continental avifauna. Japan's main lated species present in Japan (Table 1). We habitats are forest and coastal/marine, and find that even in predominantly forest-asso overall we find less diverse habitats in Japan; ciated families, such as the Fringillidae the species composition and diversity reflect (finches) and Phasianidae (pheasants), Japan this. The large area and variety ofhabitats in has drastically fewer species. Finch species in China support an equally large and diverse China number 47, but there are only 11 in avifauna;-~rnd thuugh-most-of theiapanese Japan. Even more drastic is the difference in Islands used to be connected to the continent, pheasant species, 54 and 7 for China and Ja the avifauna is depauperate. pan, respectively. The species diversity (and diversity of or In China, many more congeneric species ders and families) found on Japan is less than exist. For example, in the family Columbidae that found on the Chinese mainland (Ap- (pigeons), there are 27 species (eight in Ja- Distribution and Ecology of Birds of Japan-HIGUCHI ET AL. 77

TABLE I TABLE 2

SOME EXAMPLES OF BIRD FAMILIES HAVING FEWER COMPARISON OF BREEDING SPECIES OF HAWK AND EAGLE BREEDING SPECIES IN JAPAN THAN IN CHINA GENERA PRESENT IN BOTH JAPAN AND CHINA

NO. OF SPECIES NO. OF SPECIES

FAMILY CHINA JAPAN GENUS CHINA JAPAN

Accipitridae 41 13 Haliaeetus (Sea Eagles) 4 I Phasianidae 54 7 Aquila (Eagles) 4 I Colurnbidae 27 8 Spizaetus (Hawk-eagle) I I Cuculidae 17 4 Spilornis (Serpent-eagle) I I Strigidae 22 7 Pernis (Honey Buzzard) I I Picidae 28 11 Milvus (Kite) I I Pycnonotidae 16 2 Butastur (Buzzard) I I Corvidae 27 7 Buteo (Soaring Hawk) 3 I Muscicapidae Circus (Harrier) 6 I (I) Turdinae 72 13 Accipiter (Forest Hawk) 6 3 (2) Timaliinae 124 o (3) Sylviinae 79 15 (4) Muscicapinae 35 5 Paridae 16 5 Ploceridae 13 2 est mountain is less than 4000 m in altitude. Fringillidae 47 11 In China, desert, grassland, taiga, tundra, agriculture, rivers, and mountain ranges oc cur in many climate zones, a much greater diversity and total area than in Japan. pan). Ten of these are genus Columba, six The potential of bird families to establish Streptopelia, and eight Treron (Sphenurus). populations in Japan is limited by the lack of These genera have only three, three, and two habitat diversity. Because a viable population species in Japan, respectively. Family Acci cannot exist on an island without the appro pitridae (hawks) is similar: Japan has 10 priate type and amount of habitat, Japan's genera, and China has 18. Japan has one-half islands lack many of the species that are to one-third the species diversity within hawk present on the Asian mainland because of a genera existing in both China and Japan for lack of some habitat types and the small area which there is more than a single species of others. present in China (Table 2). Genus Accipiter, Japan has no arid regions such as deserts a forest-adapted genus of hawks, shows one or barren plateaus and thus lacks a diversity half the species diversity present in China. of arid-adapted species such as larks (Alau Even for that woodland-adapted genus the didae) and sandgrouse (pteroclididae). China species diversity is less than that in China. has 10 species of larks, mostly living in areas For Columbidae, Accipitridae, and many described as rocky, steppe, or grassland (De other families, the family is represented in Schaunsee 1984), whereas Japan has one Japan, but the diversity at the genus and species, the Skylark (Alauda arvensis L.). The species levels is low. presence of three species of sandgrouse in The species diversity of China is greater China further attests to the diversity of hab than Japan's because of the greater number itats. Japan has no breeding species of this of closely related species that live in China's arid-adapted family, widespread in desert great diversity of habitats and larger total and arid regions of the Old World. Old area. China's land area- is 26 times greater World Warblers (Sylviinae) also haVe ano than Japan's (Table 3). As a landscape, adapted species present in China [Sylvia China provides arctic, subarctic, temperate, minula Hume and S. nana (Hemptich & Eh subtropical, and tropical climates. China has renberg)], but not in Japan. Similarly, finches many high mountains and plateaus of more have species present in China, ranging in than 5000 m altitude, whereas Japan's high- habitats from open grasslands, woodlands, 78 PACIFIC SCIENCE, Volume 49, January 1995

TABLE 3 COMPARISON OF THE PHYSICAL FEATURES OF JAPAN AND CHINA

LARGER/SMALLER PHYSICAL FEATURES JAPAN CHINA RATIO

2 Area (km ) 372,197 9,561,000 25.7 Climatic zones Subarctic-subtropical Arctic-tropical Highest altitude (m) 3,776 8,848 2.3 Largest river 2 Water area (km ) 15,760 1,775,000 112.6 Length (m) 322 5,200 16.1 Range of terrestrial habitats Grassland-forest Desert-forest Length of coast line (m) 28,000 18,000 1.6 semideserts, barren plateaus, or forests up to depauperate in terrestrial species. The only treeline. Japan has a primarily woodland bird groups with a greater number of species subset of Fringillidae. in Japan than the mainland are those that China's vast area and variety of habitats utilize the marine or coastal habitats. In di has produced speciation within the Order rect contrast with the families that are de Galliformes on a scale unmatched in Japan. pauperate in Japan, seabirds have found the The Galliformes is a group of nonmigratory islands much more accessible. Japan's coast grouse, pheasants, and quail common in for line is 1.6 times longer than China's. The est and mountain habitats. China has 54 isolation of islands by the sea is an asset for species, including 16 endemics, which are them, not a barrier. Four families from two resident in habitats from semidesert to alpine orders have a total of 20 breeding species meadows over 5000 m (fang 1989). Their throughout Japan, 15 more than China endemicity shows that they responded to the (Table 4). The sea areas ofChina do not have variety of habitats by adapting to them. In a diverse or populous seabird population and Japan Phasianidae is represented by three are especially depauperate in species that native species and one introduced. Two of breed only on small islands. There are only these are endemic to Japan, and the third is two species of seabirds common in Chinese found in China as well. Even if those species waters, the Streaked Shearwater, Calonectris living at altitudes and climates not found in leucomelas (femminck), and Bulwer's Petrel, Japan are not considered, there are over 20 Bulweria bulweria (Jardine & Selby) (Melville species more in China. Although a land mass 1984). These common seabirds of China are 26 times smaller is expected to have fewer coastal breeders and are also widespread in species, Japan is depauperate in Galliformes, Japan. even for this primarily woodland subset of the pheasant family (those found at compar able altitudes in Japan and nontropical). TABLE 4 The majority of Galliformes live only on SOME EXAMPLES OF BIRD FAMILIES HAVING MORE the large, main islands of Japan, which have BREEDING SPECIES IN JAPAN THAN IN CHINA a relatively homogeneous habitat when com pared with China and lack severe isolation NO. OF SPECIES that could pressure them to speciate within FAMILY CHINA JAPAN -Japan.-- . It is clear that the pattern of existing avi Diomedeidae 1 3 fauna in Japan is heavily affected by its is Procellariidae 2 5 Hydrobatidae 1 5 land biogeography. Its birds are a subset of Alcidae 1 7 mainland avifauna, and the composition is

mEG; 4 .:;;46 i@@44tM%4 Distribution and Ecology of Birds of Japan-HIGucm ET AL. 79

Twenty species of Procellariiformes and such as wide niche utilization, host expan Alcidae nest on Japanese isles. Different spe sion/shift of parasites, and morphological cies utilize different regions of Japan's geo changes resulting from species composition. graphic range. Northern alcid species such as Further, the case of the Varied Tit, Parus Rhinoceros Auklets, Cerorhinca monocerata varius, is discussed with regard to ecological (Pallas), and Spectacled Guillemots, Cepphus and behavioral differences caused by abiotic carbo Pallas, nest on the coast of Hokkaido factors. or northern Honshu, but never range south of those points. At the other extreme, the ECOLOGICAL SIllFfS BASED ON SPECIES COM northernmost range boundary for Audubon's POSITION. Some populations show increased niche width in the absence of other species. Shearwaters, Puffinus lherminieri Lesson, and For example, the Bonin Islands Honeyeater Wedge-tailed Shearwaters, P. pacificus (Apalopteron familiare) exhibits foraging be (Gmelin), is southern Japan. The latter two havior similar to that of birds not occurring species breed only on small islands and find sympatrically. The Ogasawara (Bonin) Is ample nest sites on the Ogasawara Islands, lands lack tits, nuthatches, small robins, and 900 km south of Honshu. woodpeckers (paridae, Sittidae, Muscicapi One seabird species is endemic to Japan, dae, and Picidae, respectively). The hon and one is an endemic breeder. The Japanese eyeater exhibits foraging behavior similar to Murrelet, Synthliboramphus wumizusume (Temminck), is endemic, and the Short-tailed Albatross, Diomedea albatrus Pallas, has its last known breeding sites on Japan's Tor ishima and Senkaku Islands. Both are en (a) dangered because of human perturbation in the past. The environment of Japan is ideal for seabirds. For coastal- or islet-breeding spe cies, there are suitable breeding areas in a large range of geographic locations, and as a result, both northern Alcidae and southern Procellariiformes can nest in Japan. The rich oceans and small land area are benefits to seabirds, which have quality foraging areas 8 to support breeding.

Ecological Features ofLand Birds on (b) Small Islands Populations of birds on small islands have developed ecological and behavioral traits that differentiate them from populations on larger islands in Japan. These ecological characteristics have been investigated in studies on foraging, breeding, and parasitism of several species (Higuchi 1976, Higuchi and Momose 1981, Higuchi and Sato 1984). GharaGteristiGs that diffeF between popula 8 tions of the same species can be caused by differences in species composition of con FIGURE 6. Clutch sizes of the Varied Tit (Porus generics or by abiotic factors. Some examples vorius) on Honshu (0) and Miyake Island of the Izu Is are given below for ecological characteristics lands (b), Japan (after Higuchi 1976). 80 PACIFIC SCIENCE, Volume 49, January 1995 that of tits among twigs and leaves, to that of Brown Trembler, Cinclocerthia ruficauda nuthatches or woodpeckers on trunks and (Gray), on Dominica Island of the West In branches, and to that of small robins on the dies (Zusi 1969). ground (Higuchi 1978). It is probable that Host changes are found among Cuculus the absent species have not colonized the cuckoos on islands where they do not occur Ogasawara Islands because of their great sympatrically. There are four breeding spe distance from the Japanese main islands (900 cies of cuckoos in Japan. They are all brood km south of Honshu). A similar case of for parasites, and their main host species are aging behavior expansion is known in the segregated within their range of sympatry.

FIGURE 7. Begging postures of Honshu (a) and Miyake Island (b) Varied Tit (Parus varius) fledglings (from Higu chi and Momose 1981).

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However, on some islands, host shifts or host small Izu Islands demonstrate this. Honshu expansions are found in the absence of has four breeding species of cuckoos, which closely related species of cuckoos (Higuchi segregate host choice between 12 species or 1986). more. Honshu Little Cuckoos mostly para Host expansion is found in central Japan sitize two species. The Izu Islands have only between large- and small-island populations the Little Cuckoo, and they lay eggs in nests of the Little Cuckoo, Cuculus poliocephalus of seven or more different species, including Latham. Populations on Honshu and on the those parasitized by Himalayan Cuckoos, C.

5 • • M- 1 4 \ M-2 QJ • '- 3 3 ....::J Vl \ 2 2 \ 0 • • a. 1 \ 1 \ .~Ol ." -_. 0 .- , 00 10 20 30 40 50 60 70 80 90 0 10 20 30 40 50 60 70 80 90 Ol Ol QJ .0 _ 5 • 5 0 • >,4 ". M-3 4 M-4 \ \ ~ 3 • 3 • QJ ::J \ 2 c:r • QJ 1 1 '- \ LL 0 • ----. 0 \ 0 10 20 30 40 50 60 70 80 90 0 10 20 30 40 50 60 70 80 90 Days after leaving nest

5 •

QJ 4 \ M-5 ' • ....::J 3 \ Vl • o 2 \ a. 1 ." Ol c 0 ." 0 10 20 30 40 50 60 70 80 90 Ol Ol QJ .0 -5o ~e_. 5 >,4 "- 1-1 4 1 - 2 ~3 \ 3 ~ 2 .-.-./."--. 2 c:r . ---. QJ 1 ~ 1 LL'- 00l----.---r---.--.----.---=--.--?--.- .....90 0o+---.----.----r--r---.----.----r--r----. 10 20 30 40 50 60 70 80 10 20 30 40 50 60 70 80 90 DQ-Ys a.fter leaving nest

FIGURE 8. The decline with age of the begging posture in main-island (M-I to M-5) and small-island (1-1 and 1-2) captive fledglings (Higuchi and Momose 1981). The ordinate indicates the number of mealworms eaten that were accompanied by the begging posture in five trials each day. Begging behavior declined sharply with age in Honshu young, but it lasted for a longer period, ca. 3 months, in small-island young. 82 PACIFIC SCIENCE, Volume 49, January 1995

saturatus Blyth, and Common Cuckoos, C. TABLE 5 canorus L., on Honshu (Higuchi 1979). DURATION OF POSTFLEDGING CARE FOR HONSHU AND Host shifts and changes in egg mimicry MIYAKE ISLAND POPULATIONS OF VARIED TITS occur where the species composition ofbrood (Parus varius) parasites is different. On Honshu, Little Cuckoos often parasitize Bush Warblers, NO. OF CASES Cettia diphone (Kittlitz), and lay a chocolate DURATION brown egg closely matching that of the war (DAYS AFTER FLEDGING) HONSHU MIYAKE ISLAND bler host. Sympatric Himalayan Cuckoos do 5-9 2 not parasitize the Bush Warbler and lay eggs 10-14 3 that are white with brown spots. However, in 15-19 4 most parts of Hokkaido there are no Little 20-29 2 30-39 2 Cuckoos, and eggs of the Himalayan Cuckoo 40-49 2 population are chocolate brown or orange 50-59 1 brown, like those ofthe Bush Warbler and its 60-69 2 Honshu parasite, the Little Cuckoo, and 70-80 1 completely unlike the eggs of Himalayan From Higuchi and Momose (1981). Cuckoos on Honshu (Higuchi and Sato 1984). Egg mimicry is facilitated by the dis vertically (Figure 7). The begging behavior of tinguishing ability of the hosts (Harrison small-island young can be sustained up to 3 1968, von Haartman 1981, Mason and months after fledging, 2 months longer than Rothstein 1987, Davies and Brooke 1988). that of main-island young (Figure 8). Par Experiments performed with Brush Warblers ental care is prolonged for a similar length of showed that they were more likely to reject time on small islands (Table 5). eggs that were least like their own egg's These ecological and behavioral differences chocolate brown color (Higuchi 1989). The between island populations may be the result host shifts and subsequent morphological of ecological factors, such as the difference in changes seem to be common phenomena on primary production between large and small the Japanese Islands, where each island has a islands. Seasonal fluctuation in food pro different species composition. ductivity is expected to be smaller in the marine climate of the small lzu Islands. ECOLOGICAL AND BEHAVIORAL DIFFERENCES Temperate marine islands are similar to RELATED TO ABIOTIC FACTORS. The ecology tropical regions in that the food supply is and behavior of island populations are also relatively stable throughout the year and the subject to interpopulation variation caused population is usually near carrying capacity. by abiotic factors. The Varied Tit (Parus The breeding density of Varied Tits is two to varius) shows different breeding character three times as high in the Izu Islands as in 2 istics between the Honshu (228,000 km ) and Honshu (Higuchi 1976), thus the small in 2 Miyake Island (Izu Islands) (55 km ) pop crease of food during the breeding season, ulations. Clutch size is smaller on the lzu Is when divided among the large numbers of lands than on Honshu; the most common pairs, does not provide a large excess for number ofeggs is four on Miyake Island and breeding (Figure 9) (Ricklefs 1980, Perrins six on Honshu (Figure 6). The fledglings and Birkhead 1983). Under such conditions from these small-island clutches exhibit an of lower food availability, smaller clutch size exaggerated begging behavior. Main-island will produce more young than larger clutch - Varied-Tityoung flutter their half~open-wings size. -Fledglings -eegging-mQre-furiQusl¥ and or shake the posterior tips of the wings side for longer periods would increase their ways, whereas young from the lzu Islands chance of survival because the parents would stretch both wings sideways and flutter them continue to feed them. Thus, smaller clutch

HE .& Distribution and Ecology of Birds of Japan-HIGUCHI ET AL. 83

(a) resou rce level in (b) resource level in breeding season breeding season ------.-r-......

U regulated by resource level '" '"

adult population regulated by reSource level in non·breeding season

FIGURE 9. Resource availability in main-island (a) and small-island (b) populations. Clutch size is proportional to the ratio of the resource levels in breeding and nonbreeding seasons (after Ricklefs 1980 and Perrins and Birkhead 1983). size, exaggerated begging behavior, and pro LITERATURE CITED longed parental care of small-island Varied Tits are adaptations to these ecological con Au, S., and S. D. RIPLEY. 1971. Handbook ditions (Higuchi and Momose 1981). Honshu of the birds of India and Pakistan, Vol. 6. Varied Tit populations experience a larger Oxford University Press, London. seasonal flush of food, which allows a larger AUSTIN, O. L., and N. KURODA. 1953. The clutch size. A larger brood is optimal if the birds of Japan: Their status and distribu parents can feed the young successfully, tion. Bull. Mus. Compo Zool. Harv. Univ. which is more likely with greater food re 109(4): 279-613. sources. BLAKISTON, T. W. 1883. Zoological indica These patterns of interspecific variation in tions of ancient connection of the Japan populations are influenced by the particular Islands with the continent. Trans. Asiatic environment found on islands. Host shifts Soc. Jpn 2: 126-140. and morphological changes seen in cuckoo BRAZIL, M. A. 1991. The birds of Japan. species are a result of the presence or absence Christopher Helm, London. of congenerics. Similarly, behavioral dif CHENG, T. 1976. Distributional list of Chi ferences are related to climate differences of nese birds, 2nd ed. Scientific Press, Beijing. islands and the available food resources. The ---. 1987. A synopsis of the avifauna of biogeographic relationship between islands China. Paul Parey Scientific Publishing, and birds strongly affects the ecology and Hamburg. behavior of island avifauna. CHING, K. 1991. Temperate deciduous forests in East Asia. Pages 539-555 in E. Rohrig and B. Ulrich, eds. Ecosystems of the World 7, Temperate deciduous forests. ACKNOWLEDGMENTS Elsevier Science Publishers, Amsterdam. We thank Sheila Conant, Kris D'Atri, and DAVIES, N. B., and M. DE L. BROOKE. 1988. Thane-:&;Pratt-for reviewirrgthe manuscript; - eucko·os· versus-teeo- watDlers:--Kdapla~ Reiko Kurosawa for preparing the map; and tions and counteradaptations. Anim. Be Yao-Kuang for useful comments on Chinese hav. 36: 262-284. birds. DELACOUR, J. 1977. The pheasants of the 84 PACIFIC SCIENCE, Volume 49, January 1995

World, 2nd rev. ed. Saiga Publishing Co., egg colour of cuckoos Cuculus spp. in Ja- Surrey, U.K. pan. Ibis 126: 398-404. DE SCHAUNSEE, R. 1984. The birds of China. HIKITA, T. 1985. Japan is a country of sala- Oxford University Press, Oxford. manders. Anima 13(3): 39-42(in Japanese). FAN, Z., ED. 1990. Species of Chinese birds. lKEHARA, S. 1991. Report on the survey and Liaoning Science and Technology Press, conservation of the birds of the Nansei Shenyang. Islands. Pages 211-229 in World Wildlife HARRISON, C. 1968. Egg mimicry in British Fund-Japan, eds. Study of essential fac- cuckoos. Bird Study 15: 22-28. tors for preservation of wildlife in Nansei HIGUCHI, H. 1976. Comparative study on the Islands. Japanese Environment Agency, breeding of mainland and island sub- Tokyo. species of the Varied Tit, Parus varius. IMAIZUMI, Y. 1962. The relationships be- Tori Bull. Ornithol. Soc. Jpn. 25: 11-20. tween endemic species and geographic ---. 1978. Ecology and evolution of isolation in Japanese mammals. Shizenka- birds. Shisaku-sha, Tokyo (in Japanese). gaku to Hakubutsukan 29: 39-46 (in ---. 1979. The ecology of island birds. Japanese). Saiensu (Japanese ed. of Sci. Am.) 9(8): ---. 1985. Origin of the Japanese fauna. 74-88 (in Japanese). Anima 13(3): 28-34 (in Japanese). ---. 1980. Colonization and coexistence Johnsgard, P. A. 1986. The pheasants of the of woodpeckers in the Japanese Islands. World. Oxford University Press, Oxford. Misc. Rep. Yamashina Inst. Ornithol. 12: King, B. F., and E. C. DICKINSON. 1975. A 139-156. field guide to the birds ofSouth-East Asia. ---. 1986. Adaptations for brood para- Collins, London. sitism in Cuculus cuckoos. Pages 1-31 in MACARTHUR, R. H., and E. O. WILSON. S. Yamagishi, ed. Breeding strategies of 1963. An equilibrium of insular zoogeog- birds, Vol. 2. Tokai University Press, To- raphy. Evolution 17:373-387. kyo (in Japanese). ---. 1967. The theory of island bio- ---. 1987. The nature and birds ofJapan. geography. Princeton University Press, Yacho 52(4): 16-21 (in Japanese). Princeton, New Jersey. ---. 1989. Responses of the Bush War- MARTENS, J. 1980. Lautausserungen, ver- bIer Cettia diphone to artificial eggs of wandtschaftliche Beziehungen und Ver- Cuculus cuckoos in Japan. Ibis 131: 94- breitungsgeschichte asiatischer Laubsanger 98. (Phylloscopus). Fortschr. Verhaltensforsh. HIGUCHI, H., and T. HIRANO. 1988. Breeding 22. season, courtship behavior, and territor- ---. 1981. Searching the evolutionary iality of White and Japanese Wagtails process of Phylloscopus Willow Warblers Motacilla alba and M. grandis. Ibis 131: through their song. Anima 98:25-31 (in 578-588. Japanese). HIGUCHI, H., and N. KAwAn. 1989. Iijima's MASON, P., and S. ROTHSTEIN. 1987. Crypsis Willow Warbler Phylloscopus ijima of the versus mimicry and the color of Shiny Tokara Islands, a new breeding locality, in Cowbird eggs. Am. Nat. 130: 161-167. southwest Japan. Bull. Biogeogr. Soc. Jpn. MELVILLE, D. 1984. Seabirds of China and 44: 11-15. the surrounding seas. Pages 501-511 in J. HIGUCHI, H., and H. MOMOSE. 1981. De- P. Croxall, P. G. H. Evans, and R. W." ferred independence and prolonged in- Schreiber, eds. ICBP Technical Publica- fantile behaviour in Varied Tits, Parus tion No.2. International Council for Bird varius; of-an-island population.--Anim.-Be~- - --Preservation,-€ambridge;---- hav. 29: 523-528. MINATO, M., M. USHIKU, and M. FUNABA- HIGUCHI, H., and S. SATO. 1984. An example SHI. 1965. The geologic development ofthe of character release in host selection and Japanese Islands. Tsukiji-Shokan, Tokyo.

202:iU!JI&£ i ! ttt=i'S¥ eaRin.ah MMl Distribution and Ecology of Birds of Japan-HIGUCHI ET AL. 85

MORIOKA, H. 1974. Avifauna of the Ryukyu APPENDIX

Islands and its origin. Mem. Natl. Sci. NUMBER OF BREEDING SPECIES FOR EACH ORDER AND Mus. (Tokyo) 7:203-211 (in Japanese FAMILY IN CHINA AND JAPAN with English summary). ORNITHOLOGICAL SOCIETY OF JAPAN. 1974. NO. OF Check-list ofJapanese birds, 5th & rev. ed. SPECIES Gakken, Tokyo. PENG, Y, D. YAN, and B. KUANG. 1981. A ORDER FAMILY CIDNA JAPAN distributional list of Yunnan birds. Yun Podicipedifonnes Podicipedidae 5 3 nan Science and Technology Press, Ku Procellariiformes Diomedeidae 1 3 min. Procellariidae 2 5 PERRlNS, c., and T. BIRKHEAD. 1983. Avian Hydrobatidae 1 5 Pelecanifonnes Phaethontidae 1 1 ecology. Blackie and Sons, Glasgow. Pelecanidae 1 o RICKLEFS, R. 1980. Geographical variation Sulidae 2 1 in clutch size among passerine birds: Ash Phalacrocoracidae 3 4 mole's hypothesis. Auk 97: 38-49. Fregatidae 2 o Ciconiifonnes Ardeidae 19 16 SHORT, L. L. 1973. Notes on Okinawa birds Ciconiidae 3 1 and Ryukyu Islands zoogeography. Ibis Threskiornithidae 2 1 115: 264-267. Anserifonnes Anatidae 27 13 SmLEY, C. G., and B. L. MONROE, JR. 1990. Falconifonnes Accipitridae 41 13 Distribution and taxonomy of birds of the Falconidae 9 3 Gallifonnes Phasianidae 54 7 world. Yale University Press, London. Gruifonnes Turnicidae 3 1 TAKANO, S., ED. 1985. Birds of Japan in nat Gruidae 6 1 ural color. Yama-to-keikoku-sha, Tokyo Rallidae 16 10 (in Japanese). Otididae 3 o Charadriifonnes Jacanidae 2 o TANG, C. 1989. The distribution of pheasants Rostratulidae 1 1 and partridges in China. Pages 16-17 in Haematopodidae 1 o D. Hill, ed. Pheasants in Asia. Institute of Ibidorhynchidae 1 o Zoology, Academia Sinica, Beijing. Charadriidae 9 5 TOKUDA, M. 1970. Biogeography. Tsukiji Scolopacidae 12 5 Recurvirostridae 2 1 shokan, Tokyo (in Japanese). Glareolidae 2 1 VON HAARTMAN, L. 1981. Co-evolution of the Larifonnes Laridae 20 10 Cuckoo Cuculus canorus and a regular Alcidae 1 7 Cuckoo host. Omis Fenn. 58: 1-10. Colurnbifonnes Pteroclididae 3 o WILD BIRD SOCIETY OF JAPAN. 1982. A field Colurnbidae 27 8 Psittacifonnes Psittacidae 4 o guide to the birds of Japan. Wild Bird So Cuculifonnes Cuculidae 17 4 ciety of Japan, Tokyo. Strigifonnes Tytonidae 2 o YAMASHINA, Y 1941. On the three endemic Strigidae 22 7 birds in the Ryukyu Islands-Their clas Caprimulgifonnes Caprimulgidae 5 1 Apodifonnes Apodidae 9 3 sificatory position and zoogeographical Trogonifonnes Trogonidae 3 o meaning. Trans. Biogeogr. Soc. Jpn. Coraciiformes Alcedinidae 9 4 3:319-328. Meropidae 6 o ZHAO, Z., ED. 1988. The birds of Northeast Coraciidae 2 1 China. Liaoning Science and Technology Upupidae 1 1 Bucerotidae 3 o Press, Shenyang. Picifonnes Capitonidae 8 o Zusi, R. 1969. Ecology and adaptation of the Picidae 28 11 'Frembler- on-the island of Bominica. ~:tiv~ Passerifonnes ~ Eurylairnidae- -2 o ing Bird 8: 137-164. Pittidae 5 1 Alaudidae 10 1 Hirundinidae 9 5 Motacillidae 13 6 Campephagidae 10 1 86 PACIFIC SCIENCE, Volume 49, January 1995

APPENDIX (continued)

NO. OF SPECIES

ORDER FAMILY CffiNA JAPAN

Passeriformes (continued) Pycnonotidae 16 2 Irenidae 6 0 Bombycillidae 1 0 Laniidae 10 3 Orolidae 5 0 Dicruridae 7 0 Sturnidae 15 2 Artamidae 1 0 Corvidae 27 7 Cinclidae 2 1 Troglodytidae 1 1 Prunellidae 7 2 Muscicapidae (1) Turdinae 72 13 (2) Timaliinae 124 0 (3) Sylviinae 79 15 (4) Muscicapinae 35 5 Paridae 16 5 Sittidae 9 1 Certhiidae 4 1 Remizidae 2 0 Dicaeidae 6 0 Nectariniidae 12 0 Zosteropidae 3 1 Meliphagidae 0 1 Estrildidae 4 0 Ploceidae 13 2 Fringillidae 47 11 Emberizidae 18 8 Aegithalidae 4 1 Totals 20 78 996 254

Compiled from Ornithological Society of Japan (1974) and Wild Bird Society of Japan (1982) for Japanese birds and from Cheng (1976, 1987), Peng et al. (1981), Zhao (1988), and Fan (1990) for Chinese birds.