51

Invasion Status and Potential Ecological Impacts of an Invasive
Alien Bumblebee, Bombus terrestris L. (Hymenoptera: Apidae)
Naturalized in Southern Hokkaido, Japan
Chizuru MATSUMURA1, Jun YOKOYAMA2 and Izumi WASHITANI1
1

Laboratory of Conservation Ecology, Department of Ecosystem Studies
Institute of Agricultural and Life Sciences, The University of Tokyo
1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japane-mail: chizurum@msg.biglobe.ne.jp
2
Department of Ecology and Evolutionary Biology
Graduate School of Life Sciences, Tohoku University
Aoba, Aramaki, Aoba-ku, Sendai, Miyagi 980-8578, Japan

Abstract
In 1996, a naturally occurring nest of an introduced bumblebee, Bombus terrestris L., was found in
Monbetsu in the Hidaka region of southern Hokkaido, indicating that it had become naturalized in Japan.
In this region, monitoring of B. terrestris has been continued at two sites. The numbers of B. terrestris
captured or observed have increased rapidly during the eight years since the evidence of its
naturalization was found. Seasonally, the queens of naturalized B. terrestris have appeared as early as
mid-April each spring. Queens were observed continuously during the period from April to October,workers from May to October, and males from July to October. B. terrestris was shown to forage
among various flowering plants, 40% −70% of the species of flowering plants upon which native
bumblebees fed. Nine of ten natural nests of B. terrestris discovered during the study were found inabandoned underground rodent nests. The nest sites of this species were similar to those of B.
hypocrita sapporoensis Cockerell, and B. diversus tersatus Smith. B. terrestris clearly has thepotential to compete with native bumblebees for floral resources and nest sites. The mean number of
new queens born in the colonies of B. terrestris was 4.4 times larger than that of the native bumblebees.
This strongly suggested superior reproductive ability of B. terrestris compared with native bumblebees
in the region.
Key words: biological invasions, Bombus terrestris, ecological impacts, invasive alien bumblebee,
monitoring, pollination

1. Introduction
Claims of widespread declines in populations ofanimal pollinators have recently captured public andscientific attention (Buchmann & Nabhan, 1996;
Allen-Wardell et al., 1998; Keans et al., 1998).
Invertebrates, particularly native bees, are essential for
reproduction by seed of most wild and agricultural
plants that require pollinators. During their flights
between flowers of conspecific plants in search ofnectar, pollen, oil, or mates, bees and other insects
often move pollen to floral stigmas, thereby enhancing
fruit set and size, seed production and viability,
seedling vigor, and genetic diversity of plant
populations (Cane & Tepedino, 2001). Declines in
the abundance and distribution of bee populations arethought to have far-reaching effects on natural plant
Global Environmental Research8(1)/2004: 51-66
printed in Japan

communities and on the economic viability of some
agricultural practices (Williams, 1995).
Over the last few decades local extinction of
bumblebee species has been prevalent in agriculturalareas of Europe (Williams, 1986; Rasmont et al.,
1992; Williams, 1995; Corbet, 2000). In particular,
long-tongued bumblebee species which are irreplaceable pollinators of flowers with long corollas havemarkedly declined (Rasmont et al., 1992). Decreasing numbers of plants with long-tubed flowers due tohuman disturbance, the loss of nesting areas (Corbet
et al., 1994), and their restricted foraging radius compared to short-tongued generalist bumblebees(Walther-Hellwig & Frankl, 2000) might be among
important factors in the loss of long-tongued bumblebee species.
In contrast to these long-tongued species, the large©2004 AIRIES52

C. MATSUMURA et al.

earth bumblebee, Bombus terrestris L. (Fig. 1) is stilla widespread species in its native range (Williams,
1986). B. terrestris is a palaearctic species which is
widely distributed west of the Urals and also occurs in
the Mediterranean basin (Dafni & Shmida, 1996).
This short-tongued bumblebee shows several types ofadaptation which render it as a generalist, able toharvest floral resources from a large spectrum of plant
species in various habitats. The adaptations include:
earlier seasonal emergence, particularly of queens(Sladen, 1912; Prys-Jones & Corbet, 1991), longer
mean foraging distances (Walther-Hellwig & Frankl,
2000; Ne’eman et al., 2000; Kreyer et al., 2004), anda variety of effectual behavioral skills for nectar andpollen gathering, including nectar robbing and buzz
pollination, i.e., vibratory pollen collecting (PrysJones & Corbet, 1991; Proctor et al., 1996).
Since 1988 this efficient generalist pollinator has
been used commercially in many countries beyond its
natural range to improve pollination of greenhousecrops, particularly tomatoes Lycopersicon esculentum
Mill. (de Ruijter, 1997). Colonies of the species
have been imported into Korea, Japan, China, Taiwan,
Mexico (Dafni, 1998), Chile, Argentina, Uruguay,South Africa, Morocco and Tunisia (Hingston et al.,2002). In Japan, B. terrestris colonies were first commercially introduced for crop pollination in 1991 (Ono,
1998). Today colonies of the species have been used
for pollination in almost all parts of Japan and theannual importation is 60,000 colonies (Goka &Japanese Bumblebee Companies Association, 2003).
Japanese ecologists have continued to warn of thehigh risks of biological invasion of the species since
the first commercial introduction was considered byindustry (Kato, 1993; Washitani & Morimoto, 1993),
because B. terrestris is known to have great ecologicalflexibility and highly polylectic foraging habits enabling it to flourish in various habitats (Dafni & Shmida,

Fig. 1

Bombus terrestris (Hymenoptera, Apidae) visiting
flowers of Hylotelephium cauticolum (Crassulaceae)
in the Hidaka region of southern Hokkaido, Japan.

1996; Hingston & McQuillan, 1998; Hingston et al.,2002).
The invasive potential of B. terrestris has been
demonstrated by its successful naturalization into New
Zealand (Donovan & Wier, 1978), Israel (Dafni &Shmida, 1996), and the Australian southern island of
Tasmania (Semmens et al., 1993). In Israel, Dafni
and Shmida (1996) reported that the numbers ofhoneybees and solitary bees declined during the lasttwo decades on Mt. Carmel where the range of B.
terrestris had expanded. There are indications ofcompetition for resources between B. terrestris andother bee species (Dafni & Shmida, 1996). B.
terrestris arrived in Tasmania in 1992 (Semmens et al.,1993). Since then one study (Semmens, 1996)
recorded B. terrestris workers foraging on 170 speciesof flowering plant, of which 156 were introduced and
14 were native. Another investigation reported that
foraging of B. terrestris ranged over 66 native plant
species from 21 families (Hingston & McQuillan,
1998), and concluded that the species therefore clearly
has the potential to compete with native pollinators,
including bees and nectivorous birds in Tasmania.
There is also evidence for novel life history
evolution in introduced B. terrestris. In its native
range, this species is univoltine, that is, there is one
cycle of colony foundation and sexual reproduction
per year, interrupted between years by the death of all
individuals except for the young, newly mated queensthat enter hibernation (Alford, 1975; Prys-Jones &Corbet, 1991). Bivoltinism, the occurrence of two
cycles of colony foundation and reproduction per year
is very rare in the native range of the species(Prys-Jones & Corbet, 1991). However, studies of B.
terrestris in New Zealand and Tasmania have suggested that bivoltinism is much more frequent(Donovan & Weir, 1978; Buttermore, 1997). In its
introduced range, B. terrestris appears to have rapidly
evolved to adapt to new environments, since its newly
obtained traits greatly enhance its productivity andhence presumably expand its ecological niche(Chapman & Bourke, 2001).
Japan is home to 15 species of native bumblebees(Ito, 1991), which form key elements in the coevolved
pollination guilds which service the native flora (Kato,
1988; Suzuki, 1992; Kato et al.,1993; Washitani et al.
1995; Matsumura & Washitani, 2000; Suzuki &Akazome, 2000). Invading B. terrestris may compete with the native species for vital resources, i.e.,
nectar, pollen and nest sites. Ecological theory(Elton, 1958) suggests that the strongest effects will
be exerted on closely related species, i.e., native
Japanese bumblebees (Thomson, 1997; Washitani,1998). Laboratory experiments showed that queensof B. terrestris usurped nest sites from queens of
native bumblebees (Ono, 1997).
In addition to competition, there are possibilities ofreproductive and genetic interferences that can havenegative impacts on the populations of native bumble-

Potential Ecological Impacts of an Alien Bumblebee

bee species (Washitani, 1998; Goka, 1998). Laboratory experiments have shown that males of B. terrestris can mate with queens of Japanese native species.
On rare occasions, B. terrestris and B. hypocrita
sapporoensis Cockerell can produce hybrids (Mitsuhata& Ono, 1996).
Another potential threat from introduced B. terrestris is the transmission of disease organisms to native
bees (Washitani, 1998). The endoparasitic mite
Locustacarus buchneri Stammer (Podapolipidae) was
found in commercially introduced colonies of B.
terrestris (Goka et al., 2000, 2001). L. buchneri
mites of European genotype have been found on wild
Japanese native bumblebees (Goka, 2002).
Indirect effects on plant reproduction that currently
rely on Japanese bees for pollination depend on themechanisms by which the Japanese bees are affected
through competition with B. terrestris (Thomson,1997). Thomson (1997) pointed out the following
possibilities. If B. terrestris reduces native bee populations through competition for nectar and pollen, theinvading bees may partially compensate for the role ofthe natives playing in pollination. However, thisspecies’ habit of nectar robbing, i.e., taking nectar bybiting a hole in the corolla tube of longer flowers
without effective pollination, may negatively affectseed production in the plants it exploits. Moreover,
if the invaders usurp limited nest sites or introduce
diseases, their negative effects may spread to bees
other than those with which they share floral hosts.
Therefore, B. terrestris has influences on the reproductive success of the long-tubed flowers that depend
on long-tongued bumblebees such as B. diversus
Smith for successful pollination, not only directly by
nectar robbing, but also indirectly through reducing
effectual pollinators.
In 1996, a naturally occurring nest of B. terrestris,i.e., the first evidence of the naturalization of thespecies in Japan, was found in Monbetsu (site A) inthe Hidaka region of Hokkaido prefecture, thenorthern part of Japan (Washitani, 1998). Since
then a total of more than 4,300 bees have beenrecorded captured or witnessed from one half of the
47 Japanese prefectures (Washitani, 1997; Washitani& Matsumura, 1998; Japanese Society of Conservation Ecology, 2004). B. terrestris has been escapedin the wide range of the Japanese Archipelago.
In census studies performed in Shizuoka prefectureof central Japan and Hokkaido, where a large numberof colonies of this species have been commerciallyintroduced for agricultural pollination, in 2002, B.
terrestris was ascertained to visit Rhododendron ×
obtusum (Lindl.) Planch. and Elaeagnus multiflora
Thunb. var. hortensis (Maxim.) Servettaz, respectively(Matsumura et al., 2003). The study was a part of along-term nationwide monitoring program that has
been in progress since 1997 to monitor the invasion of
B. terrestris in Japan (Japanese Society of Conservation Ecology, 1997). These monitoring activities

53

have revealed that B. terrestris has escaped and/or
become naturalized in at least two districts of Japan.
In particular, an accelerated increase in the number ofB. terrestris captured in Monbetsu (sites A and B)
from 1996 to 2002 indicates that B. terrestris has
become firmly established in this region (Matsumura& Washitani, 2002).
In the present study, we attempted to document themagnitude of the recent invasion by B. terrestris in the
Hidaka region according to several lines of data
including those obtained by monitoring, and to assess
the possible ecological impact of the invasive alien
bee on native bumblebees and plants with bumblebee-pollinated flowers.

2. Methods
2.1 Study area
The study area was located in Tomikawa in themunicipality of Monbetsu (42˚30'N, 142˚0'E, at anelevation of 10−40 m a.s.l.), and Nina, Shiunkotsu,
and Saruba in the municipality of Biratori (42˚31'N,
142˚03'E, at an elevation of 10−100 m a.s.l.) insouthern Hokkaido, Japan (Fig. 2). The annual mean
air temperature and annual precipitation as recorded at
the standard meteorological station in Monbetsu in
2002 were 7.3˚C (max. 27.1˚C, min. −20.1˚C), and845 mm year-1, respectively. In Nina, Shiunkotsu,
and Saruba, rice fields and other cultivated fields
extend on an alluvial fan formed by the River Saru.
In the area, B. terrestris has been introduced forpollination of greenhouse tomatoes during the past 10
years. Tomatoes are cultivated in plastic-covered
greenhouses that are ventilated by simple windows
through which the bees can freely leave the enclosure.
Therefore, certainly there have been many escapes ofB. terrestris. Since 2003, the tomato-cucumber section of one agricultural cooperative association of
Biratori has put union members under an obligation to
put up nets on their greenhouses to prevent bees fromescaping.
Tomikawa is a more urban residential area withintermingling of pastures and windbreak forests of
Quercus dentata Thunb. B. terrestris bees observedin Tomikawa are regarded as naturalized bees, because
Tomikawa is 5−6 km away from the area where B.
terrestris has been mass introduced.
2.2 Monitoring and censuses for Bombus terrestrisand native bumblebees
2.2.1 Long-term monitoring in Monbetsu
Monitoring of B. terrestris and native bumblebees
has been performed during their active seasons from1996 to 2002 in Monbetsu, mainly in private gardens,site A (7,398 m2) and B (4,624 m2) in Tomikawa area.
The garden owners have voluntarily participated in
our monitoring program and whenever they found B.
terrestris in their garden or its surrounding area, on
the flowers (including Rhododendron spp., Prunus
spp., Pieris japonica (Thunb.) D. Don, Elaeagnus

54

C. MATSUMURA et al.

Fig. 2Land use map of the study area of municipalities Biratori andMonbetsu in the Hidaka region of southern Hokkaido. Palegreen, pale yellow, dark green, red, and blue areas are dominated by rice fields, other cultivated fields and pastures,
broad-leaved and coniferous forests, densely residential areas,
and rivers, respectively. Red lines indicate borders between
municipalities.

multiflora var. hortensis, Ligustrum obtusifolium
Siebold et Zucc., Dahlia pinnata Cav., Salvia officinalis L., Helianthus annuus L., and Cosmos bipinnatus Cav., and vegetable flowers such as, Cucurbita
spp. and Phaseolus coccineus L.), they captured thebees and sent the frozen specimens to the authors.
During the bees’ active seasons, such a voluntarycensus was continued almost everyday, as long as theweather permitted.
The authors also performed censuses on B.
terrestris and native bumblebees over a wider area ofMonbetsu for 14−21 days each month during May,
June, and July from 1996 to 2001. In 1996 and 1997,
C. Matsumura took the census of native bumblebees
from May to October in the area.
The censuses were performed in and aroundremnant woodlands of Quercus dentata, Q. crispula
Blume and Q. serrata Thunb. The date, location,and the species and caste (workers, males and queens)of bumblebees witnessed were recorded with information on plant species upon which they fed, the presence or absence of pollen in their corbiculae, thepresence or absence of nectar robbing behavior. The
bees of B. terrestris were captured. For native bees,
we captured the bees to identify the species and caste,
and released them after identification.
In addition to these censuses, Yokoyama et al.
(2003, 2004) took a census of B. terrestris at sites A
and B, with an effort of 2.6 man-days and 0.4 mandays in 2002, and 3.7 man-days and 0.7 man-days in
2003, respectively.
2.2.2 B. terrestris census in Monbetsu and Biratori
In 2002, a census of B. terrestris and native bumblebees by a relatively large group of observers was
initiated in the Tomikawa area of Monbetsu andmainly in Nina, Shiunkotsu, and Saruba of southern
Biratori (Yokoyama et al., 2003). The census was
performed during May to October on the flowers of
exotic and native plant species by the road, in deciduous forests and its edges, and in gardens. The samekinds of information as in the above monitoring wererecorded in this survey. The total amount of effort
made each month during May to October was 6.9, 0.4,
1.7, 0.5, 1.8, and 0.5 man-days in Monbetsu, and 2.9,
8.0, 2.2, 0.1, 3.0, and 1.3 man-days in Biratori. Data
from Monbetsu include the data collected at sites A
and B.
2.3 Foraging overlap with native bumblebees
We compared the ranges of flower utilization between B. terrestris and native bumblebee species.
Data were collected in Monbetsu and Biratori from1996 to 2002 (Appendix 1) on the occasion of the censuses described above. The number of plant species
visited by a given bumblebee species was compiled
from all the observation data. The potential degreeof competition for flower resources between two bumblebee species was evaluated according to patterns of
the proportion of plant species foraged by both bumblebees among the total number of plant species foraged by either of the bumblebee species.
2.4 Analyses of pollen load collected from one
B. terrestris nest
Forty pollen loads were collected from a total of 40
workers captured at the entrance to one B. terrestris
nest (Bt-2 in Table 1) during various periods of time
on four days from 29 June to 2 July 2002 (Matsumura
et al., unpublished).
Pollen grains from every load were acetolyzed andmounted in silicon oil on a slide. The slides wereobserved under a light microscope. From each of thePotential Ecological Impacts of an Alien Bumblebee

slides, 200 pollen grains were randomly chosen andidentified into plant species. According to themethod of O’Rourke and Buchmann (1991), the proportion of pollen volume represented by plant species
in every sample was calculated.
2.5 Nest sites and colony productivity
Ten B. terrestris nests have been found in the
Hidaka region from 1996 to 2003 (Table 1). Eightamong ten feral nests were found during one growing
season in 2003. For the common native Bombus
species in the study region (Table 2), seven B.
hypocrita sapporoensis nests, three B. diversus
tersatus Smith nests, seven B. pseudobaicalensis Vogt
nests, and two B. schrenck albidopleuralis Skorikov
nests were found in 2003. For the individual nests,
nest site characteristics and/or bee productivity werecompared and compiled according to Washitani(1998), Matsumura et al. (unpublished), Nakajima etal. (2004), and Matsumura et al. (2004).

3. Results
3.1 Numbers of B. terrestris recorded at long-termmonitoring sites in Monbetsu
At both monitoring sites A and B, the yearlysummed number of B. terrestris showed a marked
increase especially in 2002 and 2003 (Fig. 3). At site
A, the number increased from 0 in 1997 to 642 and565 in 2002 and 2003, respectively; and at site B, thenumber increased from 0 in 1996 to 203 in 2003. At
both sites, the number of queens increased steadily
during 1999 to 2003.
3.2 Seasonal flight activities of castes ofB. terrestris and native bumblebees
In 2002, B. terrestris was recorded in both
Monbetsu and Biratori during the months from April
to October (Fig. 4). In Biratori 996 B. terrestris55

individuals were collected. Possibly, most werereared bees which had escaped from greenhouses.
Workers and males were collected from May to
October, and queens, every month except August(Fig. 4). Although we could not collect queens of B.
terrestris in August, they foraged on the flowers ofPhaseolus coccineus L. (Leguminosae) in crop fields.
In Monbetsu 687 B. terrestris individuals werecollected.
Most of them were assumed to benaturalized bees, because Tomikawa is 5-6 km awayfrom the mass introduction site of southern Biratori.
Queens were captured every month from April to
October; workers, from May to October; and males,from July to October (Fig. 4).
Seasonal patterns of flight activities of B. terrestrisin Monbetsu and four common native Bombus species
in Monbetsu and southern Biratori are shown in Fig. 5.
For B. terrestris and native bumblebees, data on 862
and 689 observations were compiled from the longterm monitoring and censuses in Monbetsu during
1996 to 2002 and the censuses in Biratori in 2002.
The queens of B. terrestris were found from early
spring when queens of no other species appeared.
The flight activity period of B. terrestris was longer
than that of any native species. The period whenmales of B. terrestris were active overlapped withthose of new queens of all the native species, i.e., B.
ardens sakagamii Tkalců, B. hypocrita sapporoensis,
B. diversus tersatus, and B. pseudobaicalensis .
3.3 Foraging flower resources
During the seven-year monitoring program in
Monbetsu and Biratori, we recorded 168 plant species
visited by B. terrestris and four common native
bumblebees (Appendix 1). B. terrestris visited theflowers of 100 species across 26 families, 58% of
which were 12 alien wild plant species and 46
cultivated plant species. However, B. terrestris

Table 1 Nest sites of Bombus terrestris in the Hidaka region of southern Hokkaido, Japan.
‘Bt’ indicates B. terrestris. Blank indicates ‘lack of data.’
Nest
ID
Bt-1
Bt-2
Bt-3
Bt-4
Bt-5
Bt-6
Bt-7
Bt-8
Bt-9
Bt-10

Site

Surroundings

Entrance tunnel
length (cm)Elevation from theground level (cm)Cavity in a roll of fiber glass
insulation on ground below thefloor of a house
Rodent nest underground in a bankof an irrigation channel
Rodent nest underground in a ridge
between rice fields
Rodent nest underground in a bankof an irrigation channel
Rodent nest underground in a bankRodent nest underground in a bankof an irrigation channel
Rodent nest underground in a bankof an irrigation channel
Rodent nest underground in a bankof an irrigation channel
Rodent nest underground in a bankof an irrigation channel
Rodent nest underground in a ridge
between rice fields

Residential area
125

-28

Rice fields, fields

33

-20

A dry riverbed
Rice fields

70
140

-15
-20

33

-20

Rice fields, fields
Rice fields

Rice fields
Rice fields
Rice fields
Rice fields

56

C. MATSUMURA et al.
Table 2

Nest sites of the four common native bumblebee species in the Hidaka region of southern Hokkaido,
Japan. ‘Bhs’, ‘Bdt’, ‘Bp’, ‘Bsa’ indicate Bombus hypocrita sapporoensis, B. diversus tersatus,
B. pseudobaicalensis, B. schrenck albidopleuralis, respectively.

Nest ID
Bhs-1
Bhs-2
Bhs-3
Bhs-4

Bp-2

Site
Rodent nest underground in a small bankRodent nest underground in a small bankRodent nest underground in a small bankRodent nest underground in a ridge
between rice fields
Cavity in leaf litter and moss
Rodent nest underground in a bank of anirrigation channel
Rodent nest underground in a riverbank
Rodent nest underground in a bank of anirrigation channel
Rodent nest underground in a small bankRodent nest underground in a small bank
Under litter at a bank of in irrigation
channelOn ground at a dry riverbed

Bp-3
Bp-4
Bp-5
Bp-6
Bp-7
Bsa-1
Bsa-2

Under litter at a dry riverbed
Under litter on ground
Under litter on ground in a riverbank
Under litter on ground
Under moss on ground
Under litter on ground
Under moss on ground

Bhs-5
Bhs-6
Bhs-7
Bdt-2
Bdt-3
Bdt-4
Bp-1

Surroundings
Deciduous forest edge, dwarf bamboo community
Deciduous forest edge, dwarf bamboo community
Rice fields
Rice fields
Deciduous forest floor
Rice fields, fields
Rice fields, weed community
Rice fields, fields
Deciduous forest edge
Deciduous forest edge, dwarf bamboo community
Rice fields
Festuca arundinacea-Trifolium repens-T. pratense
community
Festuca arundinacea community
Deciduous forest edge
weed community
Dwarf bamboo community, grassland
Dwarf bamboo community, deciduous forest floor
Deciduous forest edge, dwarf bamboo community
Deciduous forest edge, dwarf bamboo community

350

400

300

350
300

250

250

200

200
150

150

100

100

50

(a)

0

50
000

0 0 0

1996 1997 1998 1999 2000 2001 2002 2003

(a)

0

Years
350

400

300

350

250

300

Apr. May Jun. Jul. Aug. Sept. Oct.
Month

250

200

200

150

150
100

100

50

(b)

0

50
0 0

0 0

0 0

0

0

1996 1997 1998 1999 2000 2001 2002 2003

(b)

0

Years

Fig. 3 The numbers of Bombus terrestris captured orwitnessed during 1996 to 2003 in the gardens
at site A (a) and site B (b), in Monbetsu. Red
columns are for queens; blue columns, forworkers; green columns, for males; and graycolumns, for workers and males. At site A,
one natural nest of B. terrestris was found in
1996. In the summer and autumn seasons of
this year, many B. terrestris workers were observed at site A, but the number was notcounted.

Fig. 4

Apr. May Jun. Jul. Aug. Sept. Oct.
Month

Seasonal changes in the number of Bombus
terrestris collected in Monbetsu (a) andsouthern Biratori (b) in 2002. Black columns
are for queens; shaded columns, for workers;
and white columns, for males. Blank indicates‘lack of data.’

Potential Ecological Impacts of an Alien Bumblebee

Apr.

May

Jun.

Jul.

57

Aug.

Sept.

Oct.

B. terrestris×
B. ardens
sakagamii
B. hypocrita
sapporoensis
B. diversus
tersatus

××B.
pseudobaicalensis

×

Fig. 5 Seasonal occurrence of castes of Bombus terrestris in Monbetsu compared with four common native Bombus
species in Monbetsu and southern Biratori during 1996 to 2002. Red lines are for queens; green lines,
workers; and blue lines, males. ‘×’ indicates the end of the survey.

frequently visited native wild plant species in deciduous forests, such as Staphylea bumalda (Thunb.) DC.
(Staphyleaceae).
Figure 6 shows flower resource sharing patterns
among bumblebee species observed in Monbetsu andBiratori. Those comparisons indicate that 39.8% −68.1% of plant species foraged by native bumblebee
species were used as flower resources by B. terrestris,
while 73.3% − 61.6% of plant species used by B.
terrestris were not included in the diet menu of native
bumblebee species.
Figure 7 shows the proportions of pollen volumeof plant species, including native, alien naturalized,
and cultivated plants, in pollen loads collected fromthe workers of one B. terrestris nest. A total of 80%
by volume of the pollen grains was comprised bynative wild plant species, Actinidia arguta (Siebold etZucc.) Planch. ex Miq. (Actinidiaceae) and Chelidonium majus L. var. asiaticum (H. Hara) Ohwi
(Papaveraceae).
3.4 Nectar robbing
B. terrestris was occasionally observed to perforate
long corolla tubes and rob the nectar (i.e., primarynectar-robbery) from flowers of various wild andcultivated plant species. Nectar robbing by B.
terrestris was recorded for a native plant species, Vicia
cracca L. (Leguminosae), some exotic cultivated plant
species, Aquilegia vulgaris L. (Ranunculaceae),
Lonicera sempervirens L. (Caprifoliaceae), an aliennaturalized plant species, Symphytum officinale L.
(Boraginaceae), and several agricultural crop species,
Phaseolus coccineus L., P. vulgaris L. (Leguminosae)(Fig. 8(a)), and Lonicera caerulea L. subsp. edulis(Turcz.) Hult var. amphhyllocalyx (Maxim.) Nakai(Caprifoliaceae) (Fig. 8(b)).
3.5 Nest sites
Among ten B. terrestris nests (Table 1), only one(Bt-1) was located in man-made fiber glass insulation
above ground (Fig. 9 (a)) and was not furnished with a

Fig. 6

Flower resource sharing patterns between two bumblebee species. The shaded portions in the pies indicate the proportion of plant species foraged by both
A and B bumblebee species among the plant species
used by B bumblebee species. Surrounded pies
represent the sharing patterns between introduced
Bombus terrestris and native bumblebees. ‘Bt,’‘Bhs,’ ‘Bas,’ ‘Bdt,’ and ‘Bp’ indicate B. terrestris, B.
hypocrita sapporoensis, B. ardens sakagamii, B.
diversus tersatus, and B. pseudobaicalensis, respectively.
n=8000pollen grains(40 pollen loads)
0

0.2

0.4

0.6

0.8

1

Proportions of pollen volume

Fig. 7

The proportions of pollen volume of nine plant species in pollen loads collected from the workers ofone Bombus terrestris nest (Bt-2) on four days from
29-June to 2-July 2002. Red and orange indicate
native wild plant species, Actinidia arguta (Actinidiaceae) and Chelidonium majus var. asiaticum(Papaveraceae), respectively. Pink, black, and green
indicate alien naturalized plant species, Lupinus perrenis, Trifolium pretense, and T. repens (Leguminosae), respectively; pale blue, a cultivated plant species, Weigela florida (Caprifoliaceae); yellow, one
species in the family Liliaceae. Small proportionsof pollen grains, 0.0007 and 0.0001 were occupied
by a native wild plant species, Syringa reticulata(Oleaceae) and an alien naturalized plant species,
Symphytum officinale (Boraginaceae), respectively.

58

C. MATSUMURA et al.

(a)

(a)

(b)
Fig. 9(b)
Fig. 8(a) Phaseolus vulgaris (Leguminosae) and (b)Lonicera caerulea subsp. edulis var. amphyllocalyx(Caprifoliaceae) flowers that were robbed of theirnectar by Bombus terrestris through a bitten hole inthe corolla tube of the flowers without effective
pollination. Arrows indicate holes formed bybiting.

tunnel. The other nine nests were made in abandoned rodent nests with entrance tunnels undergroundin ridges between rice fields or other cultivated fields,
and a dry riverbed (Fig. 9 (b)). Similarly, six B.
hypocrita sapporoensis nests and three B. diversus
tersatus nests were found to be built in abandoned
rodent nests with entrance tunnels underground inridges between rice fields or other cultivated fields
and in deciduous forest edges (Table 2). Only one
nest of B. h. sapporoensis was built in a cavity in leaf
litter and moss (Bhs-5, Table 2). All nine nests of B.
pseudobaicalensis and B. schrenck albidopleuralis
were under litter or moss on the ground (Table 2).
3.6 Colony reproductive success inferred fromcollected nests
The total number of cocoons of the five B.
terrestris nests collected (Table 3) ranged from 89 to
582 (mean ± s.d., 335.4 ± 179.7) and the total numberof individuals at collection ranged from 334 to 911

Bombus terrestris nests located in (a) fiber glass
insulation above ground below the floor of a privatehouse (Bt-1, Table 1), and in (b) a rodent nest
underground in a bank of an irrigation channel
between rice fields (Bt-2, Table 1) in the Hidaka
region of southern Hokkaido.

(mean ± s.d., 548.2 ± 250.4). Among seven B.
terrestris nests observed, five nests produced newqueens (Table 4). In Bt-2, 5, 6, and 10, new queen
production ranged from 78 to 151 (mean ± s.d., 110.00± 30.32). These nests were collected just before theircycles completed. Bt-2 produced new queens as
early as mid-July. In Bt-5 a live foundress queen anda dead body of queen were present.
The total number of cocoons of the four B.
pseudobaicalensis nests and one B. schrenck
albidopleuralis nest (Table 3) rangedfrom 49 to 376(mean ± s.d., 191 ± 120.8) and the total number ofindividuals at collection ranged from 6 to 63 (mean ±s.d., 40.6 ± 24.4). Among 19 nests of native
bumblebees, 12 nests produced new queens (Table 4).
In Bhs-4, Bdt-2, and Bp-4, 5, the numbers of newqueens produced ranged from 19 to 36 (mean ± s.d.,
25.00 ± 7.79).
Although there was no significant difference in the
proportion of colonies with new queen production
between B. terrestris and native bumblebees (Fisher’s
exact probability test: p > 0.9999), the mean numberPotential Ecological Impacts of an Alien Bumblebeeof new queens in the colonies of B. terrestris was
significantly larger (Mann-Whitney U test: p = 0.021),
and 4.4 times that of the native bumblebees(Matsumura et al., 2004).

4. Discussion
4.1 Presumable rapid population growth
The discovery of eight feral colonies of B.
terrestris discovered during one growing season as
well as the accelerated increase in the number of B.
terrestris captured in the Tomikawa area of Monbetsu
during the past eight years strongly suggests that B.
terrestris has already established a feral population in
the study region. The mean number of new queens
produced per mature nest of B. terrestris was shown tosurpass 100, and such reproductive success is comparable to that observed for laboratory-reared nests ofthe species (Goodwin & Steiner, 1997). Such a highreproductive advantage of B. terrestris coincides withthe accelerated increase in the number of B. terrestrisbees captured in the study area. On forty days from
26-April to 5-June 2004 in the study area and surroundings, 976 newly emerged queens of B. terrestris
were collected. One hundred forty five of them carried pollen loads in their corbiculae, indicating thatthey had established colonies (Matsumura et al., unpublished). It is likely that the rapid population
growth of B. terrestris continues in the study region.
Among the B. terrestris feral nests studied, one
reached full maturity and produced new queens in as
early as mid July. Such early summer maturationsuggests the possibility of production of a second generation in the year, since Beekman et al. (1999) andBeekman and van Stratum (2000) showed the possibility of production of a second generation without aperiod of diapause under laboratory conditions. In
New Zealand (Donovan & Weir, 1978) and Tasmania(Buttermore, 1997), yearly second generations are notexceptional during warmer months. However, theegg-laying capability of the new queens produced
early in summer should be examined before any firm
conclusion on the possibility of two yearly generationsin the study area is drawn.
4.2 Potential for floral resource competition withnative bumblebees
B. terrestris was shown to be highly polylectic in
the study region, as is the case within its native range(Fussell & Corbet, 1992; Dafni & Shmida, 1996) andin Tasmania (Hingston & McQuillan, 1998). At Mt.
Carmel in Israel, the species was reported to forage on
almost all plants with nectar-producing flowers (Dafni& Shmida, 1996).
The analyses of pollen loads collected from a B.
terrestris nest in the present study demonstrated thatsome native plant species are important pollen
resources for B. terrestris colonies. Most plant
species that were foraged by native bumblebees were
utilized also by B. terrestris, whereas B. terrestris was

59

shown to forage on a range of plant species less likely
to be used by native bumblebees. Moreover, nativeplant species utilized by B. terrestris are increasing
year after year (Yokoyama et al., 2003, 2004).
Frequent visitations by B. terrestris queens to theflowers of native forest plant species, Erythronium
japonicum Decne. (Liliaceae), Corydalis ambigua
Lidén et Zetterlund (Papaveraceae), and Prunus
sargentii Rehder (Rosaceae) were recorded fromobservations in 2003 in the study area (Yokoyama
et al., 2004). These plant species are importantresources for queens of B. ardens sakagamii and B. h.
sapporoensis newly emerged from hibernation(Yokoyama et al., 2004). In 2003, a springtime
forest herb Corydalis incisa Pers. (Papaveraceae)
frequently foraged by newly emerged queens of B. d.
tersatus were used as flower resources by B. terrestris
queens in the study area (Matsumura et al., unpublished).
These results suggest that all the native bumblebee
species may be affected by the competition for plantresources from B. terrestris, and that they will sufferfrom resource deficiency if the rapid population
growth of B. terrestris continues.
4.3 Potential for nest site competition with native
bumblebees
Most of the nests of B. terrestris discovered in thisstudy were found under the ground. Similarly, mostJapanese native bumblebee species use undergroundnests abandoned by small mammals (Katayama &Ochiai, 1980; Ito, 1991). Similarity in nest site
selection with B. terrestris was noted for the
short-tongued B. h. sapporoensis, and long-tongued B.
d. tersatus in the present study. It is likely that B.
terrestris will compete for nest sites at least with these
species. Furthermore, B. terrestris queens have amarked advantage in occupying suitable nest sites
over native queens because of their early emergencefrom hibernation. Preemption of the nest sites by B.
terrestris queens, the population of which is rapidly
growing, will inevitably pose a serious threat to thenative species.
On the other hand, according to Prys-Jones andCorbet (1991), B. terrestris is more adaptable fortaking advantage of man’s artifacts (e.g., rolled-up
carpets and heaps of coal). In the present study, aB. terrestris nest was found in a cavity of a fiberglass
insulation roll left on the ground. In Shimane
prefecture of western Japan, a B. terrestris nest was
found in a fold of a vinyl tarpaulin on the floor of agreenhouse (Hosoda, 1999). These facts indicatethat B. terrestris chooses nest sites more flexibly thanmost native bumblebee species and is presumably lesssusceptible to nest site shortage.
Nest invasion by queens of either the same oranother species is rather common in bumblebees(Sladen, 1912), and the habit was ascertained for B.
terrestris in the present study. Of the five nests of B.
terrestris collected and dissected, one had two

60

C. MATSUMURA et al.
Table 3

Nest ID
Bt-1
Bt-2
Bt-3
Bt-4
Bt-5
Bt-6
Bt-7
Bt-8
Bt-9
Bt-10
Bhs-1
Bhs-2
Bhs-3
Bhs-4
Bhs-5
Bhs-6
Bhs-7
Bdt-2
Bdt-3
Bdt-4
Bp-1
Bp-2
Bp-3
Bp-4
Bp-5
Bp-6
Bp-7
Bsa-1
Bsa-2

Nest size and the number of individuals of B. terrestris and native bumblebee nests in the Hidaka region ofsouthern Hokkaido. ‘No. of cocoons’ indicates total numbers of opened and un-opened cocoons. ‘No. of
individuals’ indicates total number of live eggs, larvae, cocoons, and bees at time of collection. ‘.’
indicates ‘not collected’ and blank indicates ‘lack of data.’ Symbols as in Tables 1 and Table 2.
Date found
4-Jun-02
4-Jun-03
3-Jul-03
8-Jul-03
4-Aug-03
4-Aug-03
5-Aug-03
5-Aug-03
27-Aug-03
5-Jul-03
5-Jul-03
8-Jul-03
8-Jul-03
25-May-03
4-Aug-03
6-Aug-03
3-Jul-03
20-Sept-03
21-Sept-03
4-Jul-03
7-Jul-03
9-Jul-03
25-Aug-03
29-Aug-03
16-Sept-03
17-Sept-03
21-Sept-03
23-Sept-03

Date collected
20-Oct-96
17-Jul-02.
2-Aug-03
2-Aug-03
23-Aug-03.
.
.
28-Aug-03
.
.
.
.
.
.
.
.
.
.
.
.
.
12-Oct-03
23-Sept-03
12-Oct-03
12-Oct-03.
24-Sept-03

Nest size (cm)LengthWidth

HeightNo. of cocoons

No. of individuals

20

20

5

582

405

11
20

8
13

6
8

89
321
403

334
708
911

20

13

8

282

383

11
13
7
11
10
10

10
11
6
8
10
9

10
13
4
6

180
376
49
216

60
63
6
25

6

134

49

conspecific foundress queens (a live queen and a deadqueen body). One might be the original foundress,
and another, a usurper.
4.4 Presumable impacts on plant-pollinatormutualisms
Competitive displacement of native bees by B.
terrestris has already been recorded in Tasmania(Hingston & McQuillan, 1999) and in parts of Israel
where B. terrestris has recently expanded its naturalrange (Dafni & Shmida, 1996). Considering the highcompetitive abilities of B. terrestris, displacement ofshort- and long-tongued native bumblebee species by
B. terrestris through competition will be highly likely
in near future.
Reduction in the long-tongued bumblebee species
population will cause reproductive failure of longtubed flowers that depend on these bumblebee species.
Furthermore, nectar robbing by B. terrestris, which
was recorded in several wild plant species, may
disturb the reproduction of these plants. Nectar
robbing by B. terrestris was also ascertained for somecrop plants, Phaseolus coccineus, P. vulgaris, andLonicera caerulea subsp. edulis var. amphhyllocalyx.
Nectar robbing by B. terrestris from the flowers of theField Bean (Vicia fava L.) has been frequently
observed in Europe and New Zealand (Newton & Hill,1983). Therefore, the bees have the potential tonegatively influence seed production not only of wild
plants but also of agricultural crops by hinderingnormal pollination.
As discussed above, enhanced negative impacts of
the rapidly growing population of B. terrestris on
native bumblebees and bumblebee-pollinated plants
are anticipated. To avoid such impacts, not only prevention of further escape, but also control of established populations is urgently needed.

Acknowledgements
We express our cordial thanks to S. Honda, K.
Ogawa, S. Umezawa, M. Tanizaki, and Mr. and Ms.

Potential Ecological Impacts of an Alien Bumblebee
Table 4

Nest ID
Bt-2
Bt-3
Bt-4
Bt-5
Bt-6
Bt-7
Bt-8
Bt-9
Bt-10
Bhs-1
Bhs-2
Bhs-3
Bhs-4
Bhs-5
Bhs-6
Bhs-7
Bdt-2
Bdt-3
Bdt-4
Bp-1
Bp-2
Bp-3
Bp-4
Bp-5
Bp-6
Bp-7
Bsa-1
Bsa-2

61

The number of live un-opened new queen cocoons and adult new queens in individual nests of Bombus
terrestris and native bumblebees. Blank indicates ‘lack of data.’ Symbols as in Tables 1 and Table 2.
No. of new queens
Un-opened
Adultscocoons
33
118
+
0
0
108
0
103
0
0
0

24
0

0

0
0
0
9
0
0
0
+
+

54
+
0
+
36
0
+
+
25
+
+
0
0
0
10
20
0
0
+
4

Fukuhara, for their help in long-term monitoring in
Monbetsu. This work was partly funded by Japanese
Ministry of Education, Science and Culture
Grant-in-Aid for Scientific Research 15370008, and
the Pro Natura Foundation.
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Month
8,9
8,9
7
6
7
8
5
5
5,6
9
7
5,6
7,8,9
6
9
8,9
9
9
8
7

63

Journal of Ecology, 48: 73-78. (in Japanese)
Washitani, I., M. Kato, J. Nishihiro and K. Suzuki (1995)
Importance of queen bumble bees as pollinators facilitatinginter-morph crossing in Primula sieboldii. Plant Species
Biology, 9: 169-176.
Washitani, I. and C. Matsumura (1998) European bumblebeesighting information. Japanese Journal of Conservation
Ecology, 3: 176-177. (in Japanese)
Washitani, I. and N. Morimoto (1993) Alien Plants andAnimals Naturalized in Japan. Hoikusya, Tokyo. (inJapanese)
Williams, C. S. (1995) Conserving Europe’s bees: why all the
buzz? Trends in Evolution & Ecology, 10: 309-310.
Williams, P. H. (1986) Environmental change and the distributions of British bumble bees (Bombus Latr.). Bee World, 67:
50-61.
Yokoyama, J., C. Matsumura, N. Sugiura, M. Matsumoto, M.
Kato, K. Suzuki and I. Washitani (2003) Evaluation ofpresent status on naturalization of introduced bumblebee,
Bombus terrestris, and development of extermination procedure against the species for conservation of native bumblebee species. Annual Report of Pro Natura Fund, 12: 3-10. (inJapanese with English summary)
Yokoyama, J., C. Matsumura, M. Nakajima, N. Sugiura, M.
Matsumoto, M. Kato, K. Suzuki and I. Washitani (2004)
Evaluation of present status on naturalization of introduced
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Plant species visited by bumblebees from 1996 to 2002 in Monbetsu and Biratori in the present study. ’Bt’, ‘Bas’,‘Bhs’, ‘Bdt’, ‘Bp’ indicate Bombus terrestris, B. ardens sakagami, B. hypocrita sapporoensis, B. diversus tersatus, B.
pseudobaicalensis, respectively. Q indicates queens; W, workers; M, males; and U, unidentified caste. ‘p’indicates ‘pollen carrying bees were observed.’ *Alien naturalized plant species, **cultivated plants, ***cultivatedvarieties of native plants. Plant family arrangement is based on Melcheior ‘A. Engler’s Syllabus derPflanzenfamilien’ (1964).

FamilySpecies(Herbaceous plant species)
Caryophyllaceae Silene latifolia subsp. alba*
Ranunculaceae
Aconitum yesoense
Ranunculaceae
Aquilegia flabellate
Ranunculaceae
Aquilegia vulgaris**
Ranunculaceae
Thalictrum minus var. hypoleucum
Guttiferae
Hypericum erectum
Papaveraceae
Chelidonium majus var. asiaticum
Papaveraceae
Corydalis ambigua
Papaveraceae
Corydalis incise
Papaveraceae
Eschscholzia californica**
Papaveraceae
Papaver rhoeas**
Cruciferae
Barbarea vulgaris*
Cruciferae
Brassica oleracea**
Cruciferae
Cardamine leucantha
Cruciferae
Lobularia maritima**
Cruciferae
Raphanus sativus**
Crassulaceae
Hylotelephium cauticolum
Crassulaceae
Hylotelephium telephium
Saxifragaceae
Astilbe × arendsii**
Saxifragaceae
Astilbe thunbergii var. congesta

Bt

Bas

Bumblebee species
Bhs
Bdt
W
Wp, M

W

Bp

W

W

Qp,Wp
Wp
W
Qp,Wp
Q
Wp
Wp
Q,Wp,M
W

Q

Q
Q
Q

Q

Q

Q
W
Q

Q
Wp
Q,M
Wp,M
W

W,M

W
Wp,M

W

64

C. MATSUMURA et al.

Appendix 1 Continued.
7
Rosaceae
5
Rosaceae
9
Rosaceae
6
Leguminosae
7,8,9
Leguminosae
8Leguminosae
6
Leguminosae
6
Leguminosae
6,7,8,9,10 Leguminosae
6,7,8,10 Leguminosae
8Leguminosae
7,8Leguminosae
8Leguminosae
8Leguminosae
6,7Leguminosae
9
Geraniaceae
5
9
7,8,9
8,9
9
5,6
5
7,9
7
7,8
7,8
5,6
9
5,6,7,97,8
8

Geraniaceae
Balsaminaceae
Balsaminaceae
Balsaminaceae
Balsaminaceae
Violaceae
Violaceae
Tropaeolaceae
Cucurbitaceae
Cucurbitaceae
Cucurbitaceae
Primulaceae
Convolvulaceae
Boraginaceae
Labiatae
Labiatae

8
9
5,6
7
7
7
9
8
7
8,9
7
7
7
7

Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae
Labiatae

8,9
9
7
7
7
7

Solanaceae
Scrophulariaceae
Scrophulariaceae
Scrophulariaceae
Scrophulariaceae
Scrophulariaceae

Filipendula yezoensis
Potentilla discolor
Sanguisorba tenuifolia var. alba
Lathyrus japonicus subsp. japonicus
Phaseolus coccineus**
Phaseolus vulgaris**
Thermopsis lupinoides
Trifolium hybridum*
Trifolium pretense*
Trifolium repens*
Vicia amoena
Vicia cracca
Vicia nipponica
Vicia unijuga
Lupinus perrenis*
Geranium nepalense subsp.
thunbergii
Geranium phaeum**
Impatiens glandulifera**
Impatiens noli-tangere
Impatiens textori
Impatiens walleriana**
Viola hirtipes
Viola × wittrockiana**
Tropaeolum majus**
Cucumis sativus**
Cucurbita maxima**
Cucurbita maxima × moschata**
Primula sieboldii
Ipomoea purpurea**
Symphytum officinale*
Agastache rugosa
Clinopodium chinense subsp.
grandiflorum var. parviflorum
Clinopodium sachalinense
Elsholtzia ciliate
Glechoma hederacea subsp. grandis
Hissopus officinalis**
Lamium maculatum**
Mentha sp.**
Origanum vulgare**Physostegia virginiana**
Prunella vulgaris subsp. asiatica
Rabdosia inflexa
Salvia officinalis**
Scutellaria strigillosa
Stachys riederi var. intermedia
Thymus serpyllum subsp.
quinquecostatus
Lycopersicon esculentum**
Antirrhinum majus**
Digitalis purpurea**
Mimulus hybridus**
Verbascum thapsus*
Veronicastrum sibiricum subsp.
japonicum

W
Q
Wp
Q
Qp,Wp,M M
W,M

W,M

W
Q

Wp
Qp,Wp,MQp,Wp,M

Q,Wp
Q,Wp,M

W,M

Wp

Wp

Qp,Wp,M Q,Wp,M
Qp,Wp
Q,Wp
Wp
Wp
W
W
Wp
Wp
W
W

Q,W
W

W
W,Q
W
W,M
Q
Qp,Wp,M Wp

Q,Wp

W
Q,Wp,M
W,M
Q,W,M
Q
Q
Q,W
W
W
Q
Q
Qp,W,M
Wp
W

Q

Q
Q
W

W
W,M

W
M
W,M
W
M

M
Q
W

W
Qp
W,M

W

Wp,M
W
W
W
Wp
Q
Wp
Wp
Wp
Wp

Wp
W

Potential Ecological Impacts of an Alien Bumblebee
Appendix 1 Continued.
7
Orobanchaceae
8
Phrymaceae
8Campanulaceae
8Campanulaceae
7Campanulaceae
9Compositae
9Compositae

Phacellanthus tubiflorus
Phryma leptostachya var. asiatica
Adenophora triphylla var. japonica
Codonopsis ussuriensis
Platycodon grandiflorum
Ammobium alatum**
Aster ageratoides subsp. ovatus var.
yezoensis
Aster novae-angliae*
Aster novi-belgii*
Breea setosa
Cacalia hastata subsp. orientalis
Centaurea cyanus**
Cirsium kamtschaticum
Cirsium oligophyllum subsp.
aomorense
Cirsium pendulum
Cirsium vulgare*
Cosmos bipinnatus**
Cosmos sulphureus**
Dahlia hybrida**
Helianthus annuus**
Helianthus debilis**
Leucanthemum × superbum**
Rudbeckia laciniata*
Solidago gigantea var. leiophylla*
Tagetes erecta **Taraxacum hondoence
Taraxacum officinale*
Liatris spicata**
Zinnia elegans**
Cardiocrinum cordatum var. glehnii
Disporum sessile
Disporum smilacinum
Erythronium japonicum
Hosta albo-marginata
Hosta sieboldiana var.
sieboldiana***
Hosta sp.***Polygonatum odoratum var.
maximowiczii
Iris sanguinea
Iris setosa

9,10
9
7
6
7
6,7,8
8,9,10Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae

9
9
9,10
7
7,8,9,10
7
7
7
8,9
7,8,9
9
5,6
5,6
8
9
8
6
6
5
8
7

Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Compositae
Liliaceae
Liliaceae
Liliaceae
Liliaceae
Liliaceae
Liliaceae

86Liliaceae
Liliaceae

75

Iridaceae
Iridaceae

969Commelinaceae
Commelina communis
PoaceaeDactylis glomerata*
Cannaceae
Canna indica hybrid**(Woody plant species)
Berberidaceae
Berberis canadensis**
Berberidaceae
Berberis sp.**Actinidiaceae
Actinidia arguta
Saxifragaceae
Hydrangea paniculata
Saxifragaceae
Hydrangea sp.**
Rosaceae
Chaenomeles speciosa
Rosaceae
Kerria japonica
Rosaceae
Malus baccata
Rosaceae
Prunus maximowiczii

5
6
7
7
8
5
5,6
5,6
5

65
Qp
W,M
W,M
W

W

U
W
W
M

Wp,M

Wp,M
W,M

Q,Wp,M
Q
Wp,M

M
M,Wp

W
Qp,Wp

Wp,M

Qp,Wp
Wp,M

M,U

Wp
M
Q,Wp,M
M
Q,Wp,M
W,M
Wp,M
W
Q,Wp,M
Wp,M

Q,Wp,M
W
Q

Q,U

W,M
Wp,M

U
Wp
Wp
Wp

M

W,U
Wp,M,U

Q

Q

Q,Wp,M
Wp
Q,W,M
Q
Q

Wp,U
W
W
Q
Q

Wp
Q
Q
Q
Wp
W

Q
W
Wp

M
W

W

Q

Q

Qp
Q
Wp
Wp
U
Q,Wp
Q
Wp
W,M
Q
Q
Wp
Qp

Q

Q
W

Q

Q

Q

U

Qp,Wp
U

U

66

C. MATSUMURA et al.

Appendix 1 Continued.
5
Rosaceae
5
Rosaceae
7
Rosaceae
7
Rosaceae
8
Rosaceae
6,7
Rosaceae
6
Rosaceae
6
Rosaceae
7
Rosaceae
5
Rosaceae
6,8
Rosaceae
8,9Leguminosae
7
Leguminosae
6,7Leguminosae
6
Leguminosae
5
Aceraceae
5
Aceraceae
6
Hippocastanaceae
6
Celastraceae
6
Staphyleaceae
10
Malvaceae
9
Malvaceae
5,6Elaeagnaceae
6
Ericaceae
5
Ericaceae
8
Ericaceae
5
Ericaceae
5
Ericaceae
7
4,5
5
6
5,6
5
5,6
5
5

Ericaceae
Ericaceae
Ericaceae
Ericaceae
Ericaceae
Ericaceae
Ericaceae
Ericaceae
Ericaceae

5
6,7,8
6
6
5,6

Ericaceae
Oleaceae
Oleaceae
Oleaceae
Caprifoliaceae

777Caprifoliaceae
Caprifoliaceae
Caprifoliaceae

Prunus sargentii
Prunus sp.***Rosa multiflora
Rosa rugosa
Rosa sp.**
Rubus crataegifolium
Rubus idaeus**
Rubus parvifolius
Rubus phoenicolasius
Sorbus sambucifolia
Spiraea salicifolia
Lespedeza bicolor
Lespedeza sp.***Robinia pseudoacacia*
Wisteria floribunda
Acer japonicum
Acer mono
Aesculus turbinata
Celastrus orbiculatus
Staphylea bumalda
Hibiscus moscheutos**
Hibiscus syriacus**
Elaeagnus multiflora var. hortensis
Enkianthus campanulatus
Enkianthus perulatus
Erica sp.**
Pieris japonica
Rhododendron auream ×
brachycarpum
Rhododendron brachycarpum
Rhododendron dauricum
Rhododendron dilatatum
Rhododendron japonicum
Rhododendron kaempferi
Rhododendron kiusianum
Rhododendron × mucronatum
Rhododendron obtusum***
Rhododendron yedoense var.
yedoense**
Rhododendron sp.***Ligustrum obtusifolium
Syringa reticulata
Syringa vulgaris**
Lonicera caerulea subsp. edulis var.
amphyllocalyx
Lonicera sempervirens**
Weigela coraeensis
Weigela decora

Q
W

W

Q

W

Qp,W

Q
Wp

W
Q
W
M
M
W
Qp,Wp
Wp
Wp
Wp
Wp

Wp,M
Q,Wp,M
W
W
Q,Wp,M
Q
Qp
Wp,M
Qp
Qp,Wp
Wp,M
Q,W
Qp
W
Wp
Q,Wp
Q
Q
Qp
Wp,M
Wp

W

W

W

Wp
Wp

Wp

W
W
W
W
Wp

Q,Wp
W
Q

Q,W

Q,W

Q,Wp

Q
Q

Wp

Q,W

Q

Q

Q

Q

Q

Q
Q

M
Q,Wp

W
Q

W
Q

W
Wp
M
M
M
Q

Q
Q,W

W
Qp
Q
Q
Qp

M

Wp
Wp

Q

Wp

Wp
Q

Qp,Wp,M

Q

W
W

Qp
W
(Received 7 January 2004, Accepted 26 April 2004)