Bird Research News

Vol.8 No.11

2011.11.18.

Arctic Warbler Ko-mushikui (Jpn) Phylloscopus borealis
Kamchatka Leaf Warbler Oh-mushikui (Jpn) P. examinandus
Japanese Leaf Warbler Meboso-mushikui (Jpn) P. xanthodryas
Morphology and classification
Classification: Passeriformes Phylloscopidae
Recent molecular phylogeny has established the family of Phylloscoipdae to which the leaf warblers were moved from conventional
Sylviidae (Parkin & Knox 2010, Terry et al. 2010).
The Arctic Warbler (Phylloscopus borealis) was described by
Blasius in 1858 and have been treated as a polytypic species with 3-7 subspecies. However, the author and his coworkers studied themolecular phylogeny, external morphology and vocalization of thisspecies in almost all the populations of the breeding range, andproposed that P. borealis should be divided into the following
three independent species (Saitoh et al. 2008, 2010, Alström et al.
2011, Saitoh et al. 2012):
・Arctic Warbler (Ko-mushikui) P. borealis
・Kamchatka Leaf Warbler (Oh-mushikui) P. examinandus
・Japanese Leaf Warbler (Meboso-musikui) P. xanthodryas
Hereafter, the species names are used according to this classification. Our proposition is based on that these leaf warblers are distinguished into three different groups in vocalization, molecular phylogeny and morphology (Saitoh 2009). For example, three types ofsongs and calls have been known for the leaf warblers. The DNA
analysis suggested that they diverged in the old period of 1.9-2.5
million years ago (from late Pliocene to early Pleistocene epochs).
The discriminant analysis showed that it was possible to distinguish between them with 90% accuracy based on the morphological measurements.
In Japan, Japanese Leaf Warblers breed in the subalpine zone
south of Honshu (the largest main island) and Kamchatka Leaf
Warblers breed in the Shiretoko Peninsula, Hokkaido (the northernmost main island) (Fig. 1). The third species of the Arctic Warbler is confirmed to pass Japan in the migration season of autumn(Saitoh 2004).

Vocalization:
Arctic Warblers sing a simple song in a thick voice repeatedly like
"Jee-jee-jee-jee-jee-jee". Kamchatka Leaf Warblers sing a songwith the three syllables of "Jijir-jijir" in a thick voice. Japanese
Leaf Warblers warble "Cho-cho-cho-ri" with an accent in the second syllable in a thick voice, which is memorized (mnemonics) as"Zenitori, zenitori (money collector)" in Japanese.

Distribution and Habitat

Fig. 1. Breeding distributions of the three species. Circles show the study
sites of the species (phylogenetic groups). Blue: Arctic Warblers, Yellow: Kamchatka Leaf Warblers, Red: Japanese Leaf Warblers. The
background coloration shows the former demarcation of the subspecies.
Modified from Saitoh et al. 2010.

Photo 1. Arctic Warbler

Distribution:

Wing length: 65.9mm (63.6-68.1) n = 18
Tail length: 47.3mm (41.5-52.2) n = 18
Tarsus length: 18.6mm (17.5-20.6) n = 16
Length, P10-PC: -1.2mm (-3.4- 0.9) n = 8
Weight:9.6g (8.5-11.5) n = 17Japanese Leaf Warblers breed in Honshu, Shikoku and Kyushu(three of the main four islands of Japan). Kamchatka Leaf Warblers breed in the Far East regions in Kamchatka, Sakhalin as wellas Hokkaido, Japan. The breeding range of Kamchatka Leaf Warblers in Japan is limited to the Shiretoko Peninsula in the northeastern Hokkaido (Saitoh et al. 2010). This population is importantas the southernmost population of this species in terms of conservation biology. Arctic Warblers widely breed in the Arctic regions
from Scandinavia to western Alaska.
The three species winter in Japan (the Yaeyama Islands), Taiwan,
the Philippines, Southeast Asia and Indonesia. There is detailed
information about the wintering distribution of each species in
Ticehurst (1938), but no in-depth study with a DNA analysis has
been carried out in their wintering grounds.

Photo 2. Kamchatka Leaf Warbler
Wing length: 66.3mm (60.3-71.7) n = 16
Tail length: 49.1mm (46.3-52.3) n = 16
Tarsus length: 20.0mm (18.5-21.3) n = 15
Length, P10-PC: 0.1mm (-4.0-3.0) n = 16
Weight:11.1g (9.0-13.0) n = 17

Photo 3. Japanese Leaf Warbler
Wing length: 70.8mm (68.6-75.5) n = 45
Tail length: 51.3mm (45.0-54.6) n = 45
Tarsus length: 20.3mm (18.6-21.8) n = 45
Length,P10-PC: 2.7mm (0.4-4.9) n = 37
Weight:11.9g (9.8-13.0) n=39

The measurements of male adults are based on Saitoh et al. 2008. Those of
Arctic Warblers include the subspecies Phylloscopus borealis kennicotti.
The length of P10-PC indicates a difference between the length of theoutermost primary flight feather (P10) and the longest feather of the primary wing covert.

Appearance:
Males and females are similar in plumage coloration. Japanese
Leaf Warblers are olive-colored and most strongly tinged withyellow on the upper- and underparts among the three4

similar species. Arctic Warblers are grayish green brown lacking
yellow tint on the upperpart and strongly tinged with white on theunderpart. Kamchatka Leaf Warblers are somewhere in-between inplumage coloration. The plumage coloration alone is not sufficient
to distinguish between the three species because it has individual
and regional variations. If a genetic analysis is not possible, it isadvisable to determine their species based on comprehensive information about vocalization (call and/or song), morphological measurements and plumage coloration.

Habitat of breeding area:
In Japan, Japanese Leaf Warblers breed in the forests of the subalpine conifer zone (Abies mariesii and Tsuga diversifolia) at analtitude of 1,500-2,500m, and the alpine zone (Pinus pumila, Betula ermanii and Alnus maximowiczii). Kamchatka Leaf Warblers
also breed in the birch-dwarf pine zone of the sub-alpine forest linein the Shiretoko Peninsula. In Sakhalin and Kamchatka, however,Kamchatka Leaf Warblers commonly occur in broad-leaved deciduous forests (willows and birches) along a river in the lowlands aswell. In the Eurasian Continent, Arctic Warblers are found in themixed shrubs of conifers and broad-leaved trees of the Taiga zone,
but they prefer the waterside with willows and birches (Cramp
1992).

♪ http://www.bird-research.jp/1_shiryo/koe/meboso_060722_marunuma_hirano.mp3 ♪ http://www.bird-research.jp/1_shiryo/koe/mebosomushikui2_1005_hyogo_kaji.mp3
Japanese Leaf Warbler: Toshiaki Hirano

Kamchatka Leaf Warbler: Kyoko Kajimoto

Bird Research News

Vol.8 No.11

2011.11.18.

© Japan Bird Research Association
Sumiyoshi 1-29-9, Fuchu, Tokyo, Japan

バードリサーチ生態図鑑

Life history1

2 3 4
non-breeding
season5

6 7 8 9breeding season

10

11 12

capture insects perched in the tree or flying around it by gleaning or
jumping at the underside of leaves and twigs, as they move from alower branch to another. (Nakamura & Nakamura 1995).

Topics of ecology, behavior and conservation

Breeding system:
The three species are said to be monogamous, but some Arctic Warbler males are synchronous polygamists (males that have two nests
with nestlings simultaneously) in Finland and the Yamal Peninsula,
Russia (Cramp 1992). In Japan, some Japanese Leaf Warbler males
are also suspected of being polygamous (Haneda & Kiuchi 1969).

Territory:
Japanese Leaf Warbler males establish a territory and defend it bysinging within it. The density of male territories were estimated tobe 103.3 per 1km2 in Japan.

Nest:
Japanese Leaf Warblers usually build a nest in a mossy hollow, aspace between the roots of a tree, at the base of Sasa spp. (bamboo
grass) and in a gap in a pile of fallen twigs on the ground. The nest
is globe-shaped and has an entrance on the side. They use mosses
for the exterior and root rhizomorph, fine roots and animal fur for
the inner cup.

Egg:
The clutch size is 4-5 eggs in Japanese Leaf Warblers. The egg has
minute flecks on a white ground. The clutch size is 6-7 eggs in Arctic Warblers. In Alaskan population of Arctic Warblers (subspecies,
P. b. kennicotti) , on the other hand, the clutch size is 5.9 eggs on
average (range = 5-7 eggs, n = 18) (Ring et al. 2005).

Nestling period:
In Japanese Leaf Warblers, females alone incubate their eggs for 1213 days. Both males and females feed the young. The nestlings arebrood over by the female for a few days, and fledge 13-14 days after
hatching (Haneda & Kiuchi 1969).

Natural enemy:
Japanese Leaf Warblers are frequently parasitized by the Oriental
Cuckoo (Cuculus optatus). A study showed that 40% of Japanese
Leaf Warbler nests were parasitized by this cuckoo (Haneda & Kiuchi 1969). They often suffer the nest predation of snakes as well, but
the author has recorded a marten (Martes melampus) preying on
Japanese Leaf Warbler nestlings on video.

Migration:
Japanese Leaf Warblers arrive at the breeding grounds around early
to mid-May and leave there from August to October. Kamchatka
Leaf Warblers pass through Japan to the breeding grounds from mid-May to early June and return to the wintering grounds from midAugust to early October. Arctic Warblers also travel through Japan
during the autumn migration season, but their number is smaller
than those of the other two leaf warblers (Saitoh 2004).

Diet and foraging behavior
The diet of the three species consists primarily of insects, which is
responsible for the Japanese name of the Phylloscopus warblers"mushikui (insect eater)". In summer, Japanese Leaf Warblers principally consume invertebrates such as spiders, the larvae and imagoes of beetles, flies, butterflies and cicadas. In late autumn, on theother hand, they also feed off the fruits from plants (Kiyosu 1952).
In Alaska, the staple diet of Arctic Warblers are larvae and imagoes
of mosquitoes (Ring et al. 2005).
Japanese Leaf Warblers feed in the understory of a coniferous forest, such as bushes and shrubs. In a birch forest, on the other hand,
they also use the overstory as a foraging site. In the alpine zone,
they use the broad-leaved trees scattered in a coniferous forest, and● Interesting behavior
Japanese Leaf Warblers sing for an exceptionally long time as asummer resident, which extends from late May to early October.
This is a remarkable breeding behavior because passerines in general stop singing or rarely sing in the late breeding period. However,
the reasons behind their long-term singing are not clear yet. Whenmales show a courtship display moving the wing and tail up anddown, they sometimes pick up mosses or twigs from the ground in
the bill and throw them at females (Nakamura 1979). I saw a similar
behavior, however, when I was playing back their song to capturethem for a study. I was very surprised to see a male pick up andthrow a fallen leaf at the replaying speaker.

Literature
Alström P., Saitoh T., Williams D., Nishiumi I., Shigeta Y., Ueda K., Irestedt M.,
Bjorklund M. & Olsson U. 2011. The Arctic Warbler Phylloscopus borealis - three
anciently separated cryptic species revealed. Ibis 153:395-410.
Cramp S. (ed.) 1992. The Birds of the Western Palearctic, Vol. 6. Oxford University
Press, Oxford.
Haneda K. & Kiuchi K. 1969. A study on the life history of the Japanese Leaf Warbler. I. Outline of breeding life. Japanese Journal of Ecology 19:116-125. [J]Kiyosu Y. 1952. Great Reference of Japanese Birds I. Kodansha, Tokyo. [J]Nakamura T. 1979. The behavior patterns of aggressive, courtship and nestinvitations displays in Phylloscopus warblers. Bull. Inst. Nature Edc. Shiga
Heights 18:61-64. [J+E]
Nakamura T. & Nakamura M. 1995. Illustrated Book on the Ecology of JapaneseBirds [Land birds]. Hoikusha, Osaka. [J]Parkin D.T. & Knox A.G. 2010. The status of birds in Britain and Ireland. Christopher Helm, London.
Ring R., Sharbaugh S. & Dewitt N. 2005. Breeding ecology and habitat associationsof the Arctic Warbler in Interior Alaska. Alaska Bird Observatory, Fairbanks, AK.
Saitoh T. 2004. Migration of breeding group that is understood from DNA-Japanese
Leaf Warbler. Hint of 101 learnt from Wild Bird in the forest:162-163. Japan
Forest Technology Association, Tokyo. [J]Saitoh T., Shigeta Y. & Ueda K. 2008. Morphological differences among populationsof the Arctic Warbler with some intraspecific taxonomic notes. Ornithol Sci 7:135142.
Saitoh T. 2009. Invitations to systematic geography of birds- An example of theJapanese Leaf Warbler- Bird Research News 6(11):23. [J]Saitoh T., Alström P., Nishiumi I., Shigeta Y., Williams D., Olsson U. & Ueda K.
2010. Old divergences in a boreal bird supports long-term survival through the Ice
Ages. BMC Evolutionary Biology 10:35 doi:10.1186/1471-2148-10-35. [ http://
www.biomedcentral.com/1471-2148/10/35 ]Saitoh T., Nishiumi I., Shigeta Y. & Ueda K. 2012. Re-examination of the taxonomyof the Arctic Warbler Phylloscopus borealis (Blasius): three separate species
within the Phylloscopus [borealis] superspecies. Jpn. J. Ornithol. 61:46-59. [J+E]
Terry C.R., Banks R.C., Barker F.K., Cicero C., Dunn J.L., Kratter A.W., Lovette I.J.,
Rasmussen P.C., Remsen J.V., Rising J.D., Stotz D.F. & Winker K. 2010. Fiftyfirst supplement to the American Ornithologists' Union Check-List of North American Birds. Auk 127(3):726-744.
Ticehurst C.B. 1938. A systematic review of the genus Phylloscopus. British Museum(Natural History), London.

AuthorTakema SAITOH Yamashina Institute for Ornithology
More than ten years have passed since I
started to study Japanese Leaf Warblers ingraduate school. I owe it to the warblers that
I could visit Russia, Mongolia and various
areas of Japan and make many acquaintances. I would like to continue phylogeographic
studies of warblers and other taxonomicalgroups, while respecting the connections ofpeople and communities.
saitoh@yamashina.or.jp5