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Applied Entomology and Zoology
ISSN 0003-6862
Appl Entomol Zool
DOI 10.1007/s13355-015-0372-5
Lower development threshold temperatures
and thermal constants for four species of
Asphondylia (Diptera: Cecidomyiidae) in
Japan and their larval developmental delay
caused by heat stress
Junichi Yukawa, Minami Ichinose,
Wanggyu Kim, Nami Uechi, Naohisa
Gyoutoku & Tomohisa Fujii
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Appl Entomol Zool
DOI 10.1007/s13355-015-0372-5
ORIGINAL RESEARCH PAPER
Lower development threshold temperatures and thermal
constants for four species of Asphondylia (Diptera:
Cecidomyiidae) in Japan and their larval developmental delay
caused by heat stress
Junichi Yukawa1 · Minami Ichinose1 · Wanggyu Kim1 · Nami Uechi2 ·
Naohisa Gyoutoku3 · Tomohisa Fujii4
Received: 9 July 2015 / Accepted: 28 September 2015
© The Japanese Society of Applied Entomology and Zoology 2015
infestation range expands every summer and autumn from
southern to northern Honshu, where winter–spring hosts
have never been detected. The larval development of A.
yushimai and A. baca, as well as those of two other uni-
voltine congeners, A. aucubae Yukawa and Ohsaki and A.
sphaera Monzen, was delayed at temperatures of 26, 28, or
29 °C. Global warming, when it becomes more prominent,
will reduce the number of generations and the survival rate
of multivoltine gall midges that spend summer without
diapause.
Keywords Gall midge · Heat stress · Host alternation ·
Soybean · Summer diapause · Temperature
Introduction
Among various direct and indirect effects of climate change
on insect life (e.g., Ladányi and Horváth 2010), heat stress
has been receiving more attention than before because it
had not been previously discussed intensively in relation
to global warming (e.g., Kingsolver et al. 2013; Kiritani
2012; Kiritani and Yukawa 2010). Bale et al. (2002) stated
that the effects of temperature change are frequently con-
tradictory. Higher temperatures can help to accelerate the
development of individuals and increase the survival rate,
but these can be accompanied by lower adult body mass
and lower fertility. Musolin et al. (2009) demonstrated that
the southern green stinkbug, Nezara viridula (Linnaeus)
(Hemiptera: Pentatomidae), suffered heat stress when it
was reared from egg to adult in an incubator set at a tem-
perature 2.5 °C higher than outdoor ambient temperature.
Heat stress affected N. viridula more severely in summer
than in other seasons: body size became much smaller than
that of outdoor populations, development was delayed, and
Abstract Lower development threshold temperatures
(LDT) of gall midges (Diptera: Cecidomyiidae) were
directly determined by comparing developmental stages
before and after incubation of galls for a definite period
under a range of temperatures sufficient to cover the bor-
ders of the linear response. The LDT was determined to
be 15 and 17 °C, respectively, for the soybean-pod gall
midge, Asphondylia yushimai Yukawa and Uechi, and the
ampelopsis fruit-gall midge, A. baca Monzen. They are
host-alternating multivoltine species, but their LDT did
not differ between generations on winter–spring and sum-
mer–autumn hosts, supporting the hypothesis that the value
of LDT is stable and species specific. Based on the LDT
and the 50 % emergence dates (ET50) of an overwintered
generation, we estimated the thermal constants from first
instars to adults to be 47.4 day-degrees for A. yushimai and
164.9 day-degrees for A. baca. The estimated thermal con-
stant enables A. yushimai to repeat many generations annu-
ally, which may support the possibility that the gall-midge
Electronic supplementary material The online version of this
article (doi:10.1007/s13355-015-0372-5) contains supplementary
material, which is available to authorized users.
* Junichi Yukawa
JZS02305@nifty.ne.jp
1 Entomological Laboratory, Faculty of Agriculture, Kyushu
University, Fukuoka 812-8581, Japan
2 NARO Institute of Fruit Tree Science, National Agriculture
and Food Research Organization, Tsukuba, Ibaraki 305-8605,
Japan
3 Yamagawa, Kurume, Fukuoka 839-0817, Japan
4 Biosystematics Laboratory, Graduate School of Social
and Cultural Studies, Kyushu University, Motooka,
Fukuoka 819-0395, Japan
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the rate in molt failure increased. Life tables of N. viridula
recorded in the 1960s demonstrated that its natural popu-
lations regularly suffered heat stress during the summer
in spite of its subtropical origin (Kiritani 2011). Kiritani
(2010) emphasized that heat stress affects insects at lower
temperatures than previously predicted.
The high development threshold temperature has barely
been determined, because it varies with ecological and
physiological characters tested (Kiritani 2010). In contrast,
the lower development threshold temperature (LDT) has
been determined for many arthropods by assuming a lin-
ear relationship between developmental speed and temper-
ature. In Japan, the LDT has been determined for at least
400 arthropod species, and about 25 % of them have the
LDT ranging from 10 to 12 °C (Kiritani 1997).
As to gall midges (Diptera: Cecidomyiidae), the LDT
has been determined for at least 13 species as far as we
know (see references in Table 1), including the following
two univoltine species of the genus Asphondylia: 14 °C for
A. aucubae Yukawa and Ohsaki, which induces fruit galls
on Aucuba japonica Thunbergii (Garryaceae) (Fig. 1a)
and 13 °C for A. sphaera Monzen (Ohtani et al. 1983) that
induces fruit galls on Ligustrum spp. (Oleaceae) (Fig. 1b).
Because univoltine species of Asphondylia are known to
pass through the summer in the galls as diapausing first
instars (Yukawa 1987) (Fig. 2), they may not suffer heat
stress. However, some questions arise as to multivoltine
species. Do they suffer heat stress in summer? Are their
LDTs similar to those of the two aforementioned univoltine
species? If so, what happens to their developmental speed
under extremely warm conditions, such as ≥30 °C in the
summer of southwestern Japan? Most multivoltine Asphon-
dylia species inevitably change host plants between sum-
mer–autumn and winter–spring because ovipositing sites
are not always available on a single host plant (particularly
on tree species) throughout the year (Uechi and Yukawa
2006; Uechi et al. 2004; Yukawa et al. 2003) (Fig. 2). In the
case of host alternation, does the LDT differ between dif-
ferent host plants and different seasons?
In order to answer these questions, we selected two uni-
voltine and two multivoltine species of Asphondylia as
research targets. The aforementioned A. aucubae and A.
Table 1 Known lower development threshold temperatures for gall-inducing cecidomyiids
a This data should be replaced with current data because of underestimation (see text)
Gall midge Locality Host plant (family) Low development
threshold temperature
(°C)
Developmental stage References
Asphondylia sphaera Japan Ligustrum japonicum
(Oleaceae)
13 Overwintered 1st instar
to pupa
Ohtani et al. 1983
Asphondylia aucubae Japan Aucuba japonica
(Garryaceae)
14 Overwintered 1st instar
to pupa
Ohtani et al. 1983
Asphondylia yushimai Japan Glycine max (Fabaceae) 10.4–10.8aPupa to adult Matsui 1987
Contarinia nasturtii USA Brassica oleracea
(Brassicaceae)
7.2 Egg to adult Noll 1959
UK 10.45 Readshaw 1966
Dasineura oxycoccana North America Vaccinium corymbosum
(Ericaceae)
9.8 Overwintered 3rd instar
to pupa
Craig and Oscar 2010
Dasineura tetensi Sweden Ribes nigrum
(Grossulariaceae)
7 Overwintered 3rd instar
to adult
Hellqvist 2001
Illiciomyia yukawai Japan Illicium anisatum
(Schisandraceae)
14 Overwintered 3rd instar
to adult
Yukawa et al. 2013
Macrodiplosis selenis Japan Quercus serrata
(Fagaceae)
10 Egg to 1st instar Kim et al. 2015
Mayetiola destructor USA Triticum aestivum
(Poaceae)
1.6 Egg to adult Foster and Taylor 1975
Rhopalomyia sp. Switzerland Matricaria recutita
(Asteraceae)
7.02 Egg to adult Hinz 1998
Sitodiplosis mosellana USA Triticum aestivum
(Poaceae)
9 Overwintered 3rd instar
to adult
Wise and Lamb 2004
Thecodiplosis
japonensis
South Korea Pinus thunbergii and
Pinus densiflora
(Pinaceae)
5.1, 6.1 Overwintered 3rd instar
to pupa
Son et al. 2007 ; Nam
and Choi 2014
Tokiwadiplosis
matecola
Japan Lithocarpus edulis
(Fagaceae)
>16 Overwintered 3rd instar
to pupa
Okuda and Yukawa
2000
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sphaera are univoltine, and A. yushimai Yukawa and Uechi
and A. baca Monzen are multivoltine. A. yushimai, the soy-
bean-pod gall midge, alternates hosts between fabaceous
plants, such as Glycine max (Linnaeus) Merrill (Fig. 1c),
Sophora flavescens Aiton (Fabaceae), and others in summer–
autumn and between Laurocerasus zippeliana (Miquel) Bro-
wicz (Rosaceae) (Fig. 1d) and Osmanthus heterophyllus (G.
Don) P.S. Green (Oleaceae) in winter–spring (Uechi et al.
2005; Yukawa et al. 2003). A. baca, the ampelopsis fruit-gall
midge, also does so between some vitaceous plants, such
as Ampelopsis glandulosa (Wallich) Momiyama var. het-
erophylla (Maximowicz) Momiyama (Vitaceae) (Fig. 1e) in
summer–autumn and Weigela spp. (Caprifoliaceae) (Fig. 1f)
in winter–spring (Uechi et al. 2004).
Fig. 1 Galls induced by species of Asphondylia. Arrow points toward
galls. a Fruit galls of A. aucubae on Aucuba japonica, b fruit galls of
A. sphaera on Ligsturum japonicum, c a pod gall of A. yushimai on
Glycine max (summer–autumn host), d fruit galls of A. yushimai on
Laurocerasus zippeliana (winter–spring host), e fruit galls of A. baca
on Ampelopsis glandulosa var. heterophylla (summer–autumn host), f
bud galls of A. baca on Weigela holtensis (winter–spring host)
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The purposes of this study were to:
(1) Determine the LDT for A. yushimai and A. baca on
winter–spring and summer–autumn host plants
(2) Examine the developmental speed of the four
Asphondylia species under high-temperature conditions
(3) Assess the thermal constant for overwintered first
instars of host-alternating species to complete their devel-
opment to the adult stage based on their 50 % emergence
date (ET50)
(4) Estimate the number of generations per year
Based on the estimated number of generations per
year, we also refer to the recent remarkable infestation of
A. yushimai on soybean in northern Honshu and southern
Hokkaido where its winter–spring hosts have never been
detected.
Materials and methods
Collecting, rearing, and dissecting galls
Larvae of gall midges with a type II life history strategy
(Yukawa 1987) are seldom reared outside their galls for the
entire period of the larval stage because of difficulties in
feeding them with galled tissues of the host plants. There-
fore, we did not adopt the conventional method of rearing
insects to find a linear relationship between developmental
speed and environmental temperature. Instead, we directly
determined the LDT of gall midges based on larval devel-
opmental data under various temperature conditions.
We collected galls of A. yushimai, A. baca, A. aucubae,
and A. sphaera from various localities in Fukuoka Prefec-
ture, Kyushu, Japan, from 2012 to 2015 (“Appendix 1”).
Before incubation, 15–70 galls for each sampling unit
were dissected to record the developmental stages of gall
midges at the time of collecting galls. The remaining galls
collected were incubated for 14 days under different tem-
perature conditions, except for fruit galls on A. glandulosa,
which were incubated for 10 days because they quickly
decayed at high temperatures (“Appendix 1”). Larvae of
A. yushimai and A. baca were incubated at temperatures
between 13 and 29 °C, while larvae of A. aucubae and A.
sphaera were incubated at temperatures >21 °C because
their LDT was already determined as 14 and 13 °C, respec-
tively (Ohtani et al. 1983). Then, the galls were dissected
under a binocular microscope after incubation to examine
developmental stages of the gall midges. Lighting condi-
tions were determined according to natural day length at
the time galls were collected.
Statistical analysis
Developmental stages were divided into the following
seven categories: tiny first instar, second instar (distinctly
larger than the first instar but without sternal spatula),
third instar (with a sternal spatula on the prothoracic
Fig. 2 Life-history patterns
exhibited by univoltine and
host-alternating multivoltine
species of Asphondylia. 1 first
instar, 2 second instar, 3 third
instar, P pupa, A adult, E egg
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sternite; Fig. 2 in Yukawa et al. 2003), early pupal sta-
dium (without pigmentation), midpupal stadium (with
pigmented eyes), late pupal stadium (with pigmented
head and wings), and adult emergence indicated by a
pupal case left at the emergence hole on the gall. To the
seven categories from first instar to adult, the following
scores were given respectively: 1.0, 2.0, 3.0, 4.0, 4.3, 4.7,
and 5.0. The pupal stage was temporarily divided almost
evenly into three stadia for convenience. The average
scores of development at respective temperature condi-
tions were calculated after the dissection of galls. We then
compared scores before and after incubation to determine
LDT and rate of development under different temperature
conditions. Significant differences in scores were tested
using one-way analysis of variance (ANOVA) corrected
with the Bonferroni method. This rearing and scoring
method was used to determine the LDT and the rate of
development for some gall-inducing cecidomyiids (Kim
et al. 2015; Ohtani et al. 1983; Okuda and Yukawa 2000;
Yukawa et al. 2013) (Table 1).
Thermal constant
The thermal constant was calculated by accumulating tem-
peratures above LDT for the period of time when overwin-
tered first instars had started to develop until the ET50 of
respective gall midge populations. To determine the ET50,
we referred to the emergence curve of A. yushimai sur-
veyed in Fukuoka City in 2000, provided in Yukawa et al.
(2003). As to A. baca, prior to this study, NU surveyed its
emergence from overwintered bud galls on Weigela hort-
ensis (Siebold and Zuccarini) K. Koch (Caprifoliaceae)
every other day from May to July in 2000 at Nagatani
Dam, Fukuoka City. In this survey, a gall midge emergence
hole was distinguished from that of parasitoids because the
gall midge left a pupal case at the opening. Information on
daily mean temperature was obtained from data recorded at
Fukuoka Meteorological Observatory, Fukuoka City.
Results
LDT and developmental delay
Asphondylia yushimai on Laurocerasus zippeliana
(winter–spring host)
Overwintered larvae of A. yushimai inhabiting fruit galls
of L. zippeliana did not develop during a 14–day incuba-
tion at 13 and 15 °C but developed slowly at 16, 17, 18,
and 19.5 °C and significantly faster at 23, 25, and 27 °C
(Fig. 3). However, the mean developmental code was sig-
nificantly lower at 29 °C than at 25 and 27 °C. These results
indicated that the LDT of A. yushimai can be determined as
15 °C, and its development was delayed at 29 °C.
Asphondylia yushimai on Glycine max (summer–autumn
host)
In 2013, larvae of A. yushimai inhabiting pod galls of G.
max only developed slightly during 14 days of incuba-
tion at 15 °C but developed distinctly at 18, 23, and 26 °C
(Fig. 4, left side). However, mean developmental code was
not significantly higher at 26 °C than at 18 and 23 °C. In
2014, the mean developmental code was significantly lower
at 28 °C than at 23 °C (Fig. 4, right side). Similarly, the lar-
val development was delayed at 28 °C.
Asphondylia baca on Weigela hortensis (winter–spring
host)
Overwintered larvae of A. baca inhabiting bud galls of W.
hortensis did not develop during 14 days of incubation at
14 and 16 °C but developed slightly at 22 °C and distinctly
at 25 and 27 °C (Fig. 5). However, the mean developmental
code was not significantly higher at 29 °C than at 22, 25, or
27 °C. These results indicated that the LDT of A. baca can
be determined as 17 °C and its development was delayed at
29 °C.
Asphondylia baca on Ampelopsis glandulosa (summer–
autumn host)
In 2012 at Inunaki, larvae of A. baca inhabiting fruit galls
of A. glandulosa did not develop distinctly during 10 days
of incubation at 18 °C, but developed at 20, 23, and 26 °C
(Fig. 6, left side). However, the mean developmental code
Fig. 3 Development of Asphondylia yushimai larvae in fruit galls on
Laurocerasus zippeliana under different temperature conditions. Dif-
ferent letters above bars show significant differences (0.5 % level;
one-way analysis of variance corrected with the Bonferroni method)
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was not significantly higher at 28 °C than at 18, 20, and
23 °C. In 2014 at Nishinoura, the mean developmental
codes were significantly higher at 20 and 23 °C than at the
time of collecting galls (ATC in Figs. 4, 5, 6, 7) but not at
28 °C (Fig. 6, right side). Similarly, larval development was
delayed also at 28 °C.
Asphondylia aucubae on Aucuba japonica
Larvae of A. baca developed distinctly during 14 days
of incubation at 22, 25, 27, and 29 °C, but the mean
developmental code at 29 °C was not significantly higher
than at 22 and 25 °C and was significantly lower than at
27 °C (Fig. 7, left side). These results indicated that the lar-
val development was significantly delayed at 29 °C in the
univoltine gall midge, which passes through summer as
diapausing first instars.
Asphondylia sphaera on Ligustrum japonicum Thunbergii
(Oleaceae)
Larvae of A. sphaera developed distinctly during 14 days
of incubation at 23 25, 27, and 29 °C, but the mean devel-
opmental code at 29 °C was not significantly higher than
at 23 and 27 °C (Fig. 7, right side). Similarly, these results
indicated that larval development was significantly delayed
at 29 °C, even in the univoltine gall midge, which passes
through summer as diapausing first instars.
Fifty percent emergence date, thermal constant,
and estimated number of generations
Asphondylia yushimai
From data provided in Yukawa et al. (2003), we deter-
mined the ET50 for the A. yushimai population to be 9
May in 2000 (see Fig. 9b in Yukawa et al. 2003). Tem-
peratures above the LDT of A. yushimai accumulated dur-
ing the period from the time at which overwintered first
instars had started developing until the ET50 was 47.4 day-
degrees (thermal constant from the first instar to adult). If
we include unknown thermal constant for the egg stage
(about 7 days based on our field observation in 2013), the
Fig. 4 Development of Asphon-
dylia yushimai larvae in pod
galls on Glycine max under dif-
ferent temperature conditions.
Different letters above bars
show significant differences
(0.5 % level; one-way analysis
of variance corrected with the
Bonferroni method)
Fig. 5 Development of Asphondylia baca larvae in bud galls on
Weigela hortensis under different temperature conditions. Different
letters above bars show significant differences (0.1 % level; one-way
analysis of variance corrected with the Bonferroni method)
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estimated total thermal constant from egg to adult could
be at most 60 day-degrees. In Fukuoka City, the thermal
total above the LDT of A. yushimai was 1443 day-degrees
in 2000 (Fukuoka Meteorological Observatory), which is
available for A. yushimai to repeat about 24 generations a
year. Previously A. yushimai was thought to have only sev-
eral generations during summer–autumn seasons in north-
ern Honshu (e.g., Shibuya 1997), possibly because of poor
field data. Larval developmental delay at high temperatures
during the summer may reduce the number of generations
to some extent but cannot fill the large gap between 24 and
several generations a year.
Asphondylia baca
Figure 8 shows the emergence curve and ET50 of A. baca
in 2000 at Nagatani Dam, Fukuoka City. The thermal con-
stant from the first instar to adult was 164.9 day-degrees.
If we include unknown thermal constant for the egg stage
(about 7 days based on our field observation in 2013), the
estimated total thermal constant from egg to adult could be
at most 180 day-degrees. In Fukuoka City, the thermal total
above the LDT of A. baca was 1169 day-degrees in 1980
(Fukuoka Meteorological Observatory), which is available
for A. baca to repeat at least six generations a year (Fig. 8).
Fig. 6 Development of Asphon-
dylia baca larvae in fruit galls
on Ampelopsis glandulosa var.
heterophylla under different
temperature conditions. Differ-
ent letters above bars show sig-
nificant differences (0.5 % level;
one-way analysis of variance
corrected with the Bonferroni
method)
Fig. 7 Development of Asphon-
dylia aucubae larvae in fruit
galls on Aucuba japonica and
of A. sphaera in fruit galls on
Ligustrum japonicum under dif-
ferent temperature conditions.
Different letters above bars
show significant differences
(0.5 % level; one-way analysis
of variance corrected with the
Bonferroni method)
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Discussion
Bergant and Trdan (2006) argued that thermal constants,
based on laboratory experiments, commonly suffer from a
great amount of uncertainty and should be used with caution
in practice. In particular, they emphasized that a sufficient
temperature range should be covered in the experiment to
approach the borders of the linear response as closely as pos-
sible. We reared gall midge larvae under various temperature
conditions that could decrease the uncertainty in determin-
ing LDT around the borders. The results of our experiments
indicated the borders and nonlinear relationships between
developmental speed and temperature (Figs. 3, 4, 5).
Matsui (1987) estimated the LDT of A. yushimai pupae
to be 10.4 °C in males and 10.8 °C in females and ther-
mal constant of pupae to be 94.5 day-degrees in males and
84.8 day-degrees in females. These LDTs are distinctly
lower than ours, even though his experiments were limited
to the pupal stage, which tends to have higher LDT than
the other stages (Kiritani 1997); ours included the entire
developmental stages from first instars to adults. To esti-
mate the LDT, Matsui (1987) used data obtained from the
linear relationship in the laboratory and ET50 in the field,
which may include more uncertainties than our direct rear-
ing methods. As a result, the thermal constant proposed by
Matsui does not fit well with the life history pattern of A.
yushimai, possibly because of underestimation of LDT. In
Kagoshima, larvae remained as first instars in the galls until
mid-March (Yukawa and Masuda 1996), even though mean
daily temperatures frequently exceeded 11 °C from late
February to mid-March. Therefore, we adopted our results
for further discussion, as below.
We determined the LDT to be 15 and 17 °C, respec-
tively, for A. yushimai and A. baca. The LDT of these
host-alternating multivoltine species did not differ between
winter–spring and summer–autumn hosts and generations,
supporting the tendency that the LDT is species specific
(e.g., Hodek and Honeˇk 1996; Kiritani 2012).
It is remarkable that the LDT is relatively high in spe-
cies of Asphondylia compared with species of other genera
(Table 1). As pointed out by Yukawa (2000) and Yukawa
and Akimoto (2006), the synchronization of herbivores
with their host-plant phenology is a critical event, in par-
ticular for such short-lived insects as gall midges. The high
LDT can delay and synchronize the spring emergence sea-
son of Asphondylia with the flowering or fruiting season of
their summer hosts. Thus, late emergence is advantageous
for fruit gallers, such as most species of Asphondylia in the
temperate zone. In contrast, leaf gallers have lower LDT
and emerge earlier, synchronizing well with leaf-opening
or shoot-extending seasons (e.g., Macrodiplosis selenis
Kim and Yukawa (Diptera: Cecidomyiidae) on Quercus
spp.: Kim et al. 2015). Of course, there are some excep-
tions to this explanation as to leaf gallers that have rela-
tively high LDT (Table 1). The LDT of Illiciomyia yukawai
Tokuda (Diptera: Cecidomyiidae) is 14 °C because shoots
of Illicium anisatum Linnaeus (Schisandraceae) extend
late in the spring season (Yukawa et al. 2013). The emer-
gence of Tokiwadiplosis matecola Simbolon and Yukawa
(Diptera: Cecidomyiidae) cannot synchronize with spring
shoots but with lammas shoots of Lithocarpus edulis (Mak-
ino) Nakai (Fagaceae) because it its LDT is >16 °C (Okuda
and Yukawa 2000).
The higher LDT may be advantageous for multivoltine
species to pass through hot summers without diapause, as
has been noted for a tropical species, Stenodiplosis sorghi-
cola (Coquillett) (Diptera: Cecidomyiidae) (= sorghum
midge), which develops normally at temperatures from 20
to 34 °C (Baxendale et al. 1984). In this sense, the LDT
of A. yushimai and A. baca seems to be not high enough
compared with 14 and 13 °C of the two univoltine species,
A. aucubae and A. sphaera, respectively. In addition, these
four species of Asphondylia suffered larval developmen-
tal delay at high temperatures of 26, 28, or 29 °C, even
though the univoltine species enter summer diapause in
the galls as first instars (Yukawa 1987). In this study, we
referred only to developmental speed at high temperatures,
but the developmental delay may be associated with other
deleterious effects, such as reduction of survival rate, body
size and fecundity, and the failure of molting, as noted
in Kiritani (2011), Mason and Strait (1998), and Muso-
lin et al. (2009). Global warming, when it becomes more
prominent, may reduce the number of generations and sur-
vival rates of multivoltine gall midges that spend summer
without diapause.
There are many examples of a tradeoff between LDT
and thermal constant, in which insects with relatively
low LDT require larger amounts of thermal constant than
those with high LDT (Honeˇk 1996; Kiritani and Yamashita
Fig. 8 Percentage emergence curve and 50 % emergence date (ET50)
of Asphondylia baca inhabiting bud galls on Weigela hortensis (win-
ter–spring host). TC thermal constant for overwintered first instars to
become adults = 164.9 day-degrees
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2008). Of course, this is not always true; LDT is not corre-
lated with thermal constant in other cases because thermal
constants are variable with food quality, sex, and other fac-
tors (Kiritani 2012). Our study found that A. yushimai with
a lower LDT, 15 °C, requires a smaller amount of thermal
constant (47.4 day-degrees), while A. baca, which has
higher LDT (17 °C) requires a greater amount of thermal
constant (164.9 day-degrees).
These different combinations of LDT and thermal con-
stant resulted in a great difference in the number of annual
generations between the two species. Many generations of
A. yushimai can be hosted by a wide variety of its summer–
autumn hosts across various genera of Fabaceae (Tamura
1952; Yukawa and Masuda 1996), which means that young
pods are available for oviposition continuously throughout
the seasons. In contrast, the several summer–autumn gen-
erations of A. baca are hosted by only two species of vita-
ceous plants (Yukawa and Masuda 1996). Thus, host-plant
availability may also be related to the number of possible
generations reflected by LDT and thermal constant.
A. yushimai is one of the major pests of soybean in Japan
(e.g., Yukawa and Masuda 1996; Yukawa et al. 2003). In
recent years, its infestation on soybean has become increas-
ingly prominent, particularly in Akita Prefecture, northern
Honshu (Kikuchi H, 2013 and 2014, personal communica-
tion), and it was found for the first time in southern Hok-
kaido in 2013 (Hokkaido Plant Protection Office 2013).
However, winter–spring hosts for A. yushimai have not yet
been found in northern Honshu and southern Hokkaido
because the two known winter–spring hosts, Laurocer-
asus zippeliana (Rosaceae) and Osmanthus heterophyllus
(Oleaceae), are not distributed in these areas (Uechi et al.
2005; Yukawa et al. 2003). Therefore, A. yushimai may
not be able to overwinter in northern Honshu and southern
Hokkaido. The high number of summer–autumn genera-
tions (our data) in A. yushimai, together with its flight abil-
ity (Yukawa et al. 2003), may support the possibility that
infestation of A. yushimai on soybean expands northward
every summer and autumn. In southwestern Japan, our data
on LDT and thermal constant will enable applied entomol-
ogists to control A. yushimai at the time of adult emergence
from the winter–spring hosts by predicting its emergence
season more accurately than before.
Acknowledgments We express our thanks to Dr. K. Kiritani (Emer-
itus Researcher, NARO Institute for Agro-environmental Sciences,
Japan), Dr. K. M. Harris (former Director of the International Insti-
tute of Entomology, UK), and Prof. T. Hirowatari (Kyushu University,
Japan) for their critical reading of an early draft. We thank the late
Mr. Y. Ariyoshi, Mr. H. Ueda (Botanical Garden of Fukuoka City),
and Ms. S. Seto, Ms. A. Sugita, and Mr. D. Yamaguchi (Kyushu Uni-
versity) for their help in collecting, rearing, and dissecting galls. We
are grateful to Dr. M. Tuda (Kyushu University) for providing us with
incubators for rearing experiments.
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