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Parasitism and oviposition of Melittobia acasta on Bombus terrestris: impact of larval overwintering and host status on pupation and adult emergence

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RESEARCH PAPER
Parasitism and oviposition of Melittobia acasta on
Bombus terrestris: Impact of larval overwintering and
host status on pupation and adult emergence
Yong Jung KWON, Md Ruhul AMIN and Nang Soi Lao INN
Department of Agricultural Biology, Kyungpook National University, Daegu, Korea
Correspondence
Md Ruhul Amin, Department of
Entomology, Hajee Mohammad Danesh
Science and Technology University,
Dinajpur 5200, Bangladesh. Email:
ruhul_hstu@yahoo.com
Received 11 August 2011;
accepted 1 November 2011.
doi: 10.1111/j.1748-5967.2011.00361.x
Abstract
Melittobia acasta (Walker) are microhymenopteran ectoparasitoids of the pupae
and prepupae of the commercially-used pollinator bumblebee species Bombus
terrestris L. The female parasitoids puncture the host cuticle with their sting and
feed oozing hemolymph. This study shows that M. acasta parasitize 100% pupae
and 84% prepupae of B. terrestris but are ineffective on the larvae of the bees. The
female parasitoids lay a significantly higher number of eggs on pupae (67.7 16.2
female-1) compared to prepupae (20.5 14.5 female-1). The parasitoids differ in
their choice for oviposition sites and fecundity on different locations of B. terrestris
pupae, and they show most preference for oviposition (32%) as well as fecundity
(34.9 15.1 female-1) on the petiole of the host. Larvae of the parasitoids over-
winter at low temperatures but larval overwintering duration and post-diapause
rearing on original or new hosts do not affect their pupation and adult emergence.
Larvae have a higher percentage of pupation (88.0–94.4%) and adult emergence
(84.4–92.9%) both on the original and the new host, thus indicate that the parasi-
toids are highly capable of reproduction in B. terrestris colonies.
Key words: Bumblebee, eulophid, parasitoid, reproduction.
Introduction
Bombus terrestris L. (Hymenoptera: Apidae) is a European
bumblebee species that has been widely used for pollination
of vegetable crops with a view to saving labor costs and
production of higher quality and quantity yield (Kanbe et al.
2008; Velthuis & van Doorn 2006). This European native
species been available in portable boxes for crop pollination
since 1988 and many countries, including Korea, Japan,
China, South Africa, Morocco, Tunisia, Mexico, Chile and
Argentina, have been importing colonies (Dafni 1998; Mit-
suhata 2000). In commercial rearing systems, bumblebees
suffer from attacks by different parasitic mites, protozoans,
Lepidopteran insects and Hymenopteran wasps (van der
Steen 2000). The parasitic wasp Melittobia acasta (Walker)
(Hymenoptera: Eulophidae) is a serious pest of bumblebees
and the species has been introduced from Europe to Argen-
tina, Canada, India, Japan, New Zealand, the USA and Ven-
ezuela (Boucek 1977; de Santis 1983; Husain & Khan 1986;
Salle 1993; Gonzalez 1994). M. acasta is reported as a
parasite of various insect orders, including Hymenoptera,
Diptera, Lepidoptera and Coleoptera (Alford 1975; Kalinin
& Molchanov 1987; MacFarlane & Donovan 1989; Dor-
oshina 1990; Schmid-Hempel 1998, 2001; Maeta 1999).
M. acasta are small, gregarious ectoparasitoids and pri-
marily attack solitary bees and wasps, especially those that
build mud nests (Gonzalez et al. 2004a). They generally
attack the hosts at pupal stage but can parasitize hosts at the
prepupal and final larval stages (Dahms 1984a). They are
polyphagous and gregarious in nature and can easily propa-
gate at any time of the year on readily available hosts (Mat-
thews et al. 2009). As they are ectoparasites, the females
puncture the host cuticle with their sting and feed on the
oozing hemolymph (Gonzalez et al. 2004b). They lay
Entomological Research 42 (2012) 94–98
© 2011 The Authors
Entomological Research © 2011 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd
eggs on the surface of the host pupae or prepupae and hatch-
ing larvae develop there (Abe et al. 2003). Shape, size, color,
texture and chemicals associated with the hosts play an
important role in their host acceptance and oviposition
behavior (Vinson 1985; Vinson & Piper 1986; Tilden &
Ferkovich 1988).
Melittobia wasps depend on a series of adaptations for
survival when adverse environmental conditions affect the
ecological and the physiological status of their hosts (Hance
et al. 2007). Gonzalez et al. (2004b) report that second
instar larvae of M. acasta can enter diapause in host cocoons
at 15°C and diapausing larvae can resume normal develop-
ment when they are incubated at 25°C. Maeta (1978)
observes that the threshold development temperatures for
female and male Melittobia larvae are 14.2°C and 15.7°C,
respectively, and below these temperatures larvae stop
development and enter into diapause.
Some Melittobia species have been reported as a parasi-
toid of bumblebees in different regions of the world (deWael
et al. 1993; Whitfield & Cameron 1993; MacFarlane et al.
1994). Browne (1922) studies the life history of M. acasta
on different bees and wasps; Gonzalez et al. (2004b) reviews
the life history of this parasitoid on Sceliphron fistularium,
Trypoxylon politum,Megachile rotundata and Neobellieria
bullata. However, there is no record concerning the parasit-
ism and oviposition behavior of M. acasta on B. terrestris.
Moreover, we have discovered this parasitoid as a pest of
B. terrestris colonies in Korea and, therefore, we are prima-
rily interested in studying the parasitism and oviposition
behavior of this parasitoid with B. terrestris larvae, prepupae
and pupae. We predicted that Melittobia larvae and their
hosts would be affected by overwintering duration at
extremely low temperatures, which would result in a lower
number of larvae developing to adults. Therefore, we were
interested in determining the effects of larval overwintering
duration on pupation and adult emergence, focusing our
attention on larval responses to the original hosts or new
hosts.
Materials and methods
Collection and rearing of parasitoids
Sixteen B. terrestris colonies were imported from Koppert
B. V., the Netherlands in 2004 and the colonies were reared
for mass culture in the Agricultural Biology Laboratory,
Kyungpook National University, Daegu, Korea. The para-
sitic wasps, M. acasta, were found in our mass rearing colo-
nies of B. terrestris and therefore, parasitoids were collected
for stock culture in a climate controlled room at 25 1°C,
50% relative humidity and 12 h light : 12 h dark conditions.
Collected male and female parasitoids were kept pair-wise
in Petri dishes (35 ¥10 mm) for mating. After 2 days, female
parasitoids were placed individually in small Petri dishes,
with B. terrestris pupae provided as a host. Solo tape
was used to cover the space between the lips of the Petri
dish, which prevented the parasitoids from escaping. The
parasitoids that had laid eggs on the host pupae and pro-
duced male and female offspring were considered fertilized
females. All observations were made using an Olympus SZH
10 binocular microscope (Research Sterio Olympus Optical,
Japan).
Parasitism and oviposition of Melittobia acasta
on different life stages of Bombus terrestris
To determine a favorable host for parasitism and oviposition
of M. acasta, one mated parasitoid along with a B. terrestris
larva, prepupa or pupa were placed in a Petri dish. The Petri
dish along with the parasitoid and each host stage were
replicated 100 times and the Petri dishes were kept in a
climate controlled room under 25 1°C, 50% relative
humidity and 12 h light : 12 h dark conditions. After 1 week,
parasitized larvae, prepupae and pupae were separated, and
the percentage of parasitized larvae, prepupae and pupae
were calculated. The number of eggs deposited (fecundity)
on each parasitized host stage was counted.
Parasitism and oviposition on different sites of
Bombus terrestris pupae
To determine a suitable site for oviposition, one mated
female parasitoid along with a B. terrestris pupa was kept in
a Petri dish. This procedure was replicated 100 times and the
Petri dishes were kept in a climate controlled room under
25 1°C, 50% relative humidity and 12 h light : 12 h dark
conditions. After 1 week, the mother parasitoids were
removed from the Petri dishes and the oviposition site on
each pupa was detected. Therefore, the percentage of para-
sitoids that laid eggs as well as their fecundity on thorax,
sternite, legs, frons, petiole or anal regions of the pupae were
calculated.
Effect of overwintering duration and host quality
on pupation and adult emergence
Five to seven full-grown larvae of M. acasta along with a
B. terrestris pupa were placed in each Petri dish and the Petri
dishes were kept in an incubator at 10 1°C, 50% relative
humidity for 30 or 45 days. To test the effect of larval
overwintering duration on pupation and adult emergence, 15
Petri dishes (for each of the 30 or 45 days overwintering
duration category), including larvae and their original hosts
were transferred to another incubator at 25°C and 50% rela-
tive humidity for breaking diapause. The Petri dishes were
monitored daily for collection of pupation and adult emer-
Parasitism of Melittobia acasta
95
Entomological Research 42 (2012) 94–98
© 2011 The Authors. Entomological Research © 2011 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd
gence data until the live larvae had become adults. To test
whether live or dead hosts influence pupation and adult
emergence, 30 or 45-day overwintered larvae were taken
away from their hosts. They were reared separately on live
pupae of B. terrestris. A new host and 5–7 larvae were
kept in each Petri dish, and this procedure was replicated 15
times for each overwintering duration category. The Petri
dishes were placed in an incubator at 25°C and 50% relative
humidity, and data on pupation and adult emergence were
collected by daily observation until the live larvae had
become adults.
Data analysis
Parasitism and fecundity on different host stages, oviposi-
tion site preference, pupation and adult emergence in rela-
tion to overwintering duration and host quality data were
analyzed by c2-test. One way analysis of variance (ANOVA)
and Duncan’s multiple range test were used to analyze the
data of the fecundity on different oviposition sites. All analy-
ses were performed using IBM SPSS Statistics 19.
Results and discussion
Melittobia wasps are idiobionts that generally attacking their
hosts at pupal stage, but they can parasitize at the prepupal
and the final larval stages of the hosts (Dahms 1984b). This
study shows that M. acasta parasitize on the prepupal and
pupal stages of B. terrestris, and the larval stage of the bee is
not effective for parasitism of this wasp (Fig. 1). Although
the parasitoids show a higher percentage of parasitism on
pupae (100%) compared to prepupae (84%), there is no
significant difference (c2=1.4, P>0.05).
Figure 2 shows that fecundity on different host stages
differs significantly (c2=24.0, P<0.001) and the pupa
stage is the most suitable stage for oviposition of the para-
sitoid. Female parasitoids lay an average 66.7 16.2 and
20.5 11.5 eggs on pupae and prepupae, respectively, and
no egg is deposited on the larvae. Therefore, results on the
parasitism and oviposition behavior of M. acasta of this
study indicate that the wasps are prepupal and pupal para-
sitoids of B. terrestris.
M. acasta show similar parasitism and oviposition behav-
ior to M. australica, which are gregarious ectoparasitc
wasps. Their primary hosts are the prepupae and pupae of
solitary wasps and bees that build nests above the ground
(Maeta & Yamane 1974). The species M. hawaiiensis exhib-
ited parasitism and oviposition on the larvae of Apis mel-
lifera under laboratory conditions (Varanda et al. 1984).
Female Melittobia lay eggs in batches of 4–12 or
sometimes singly along the intersegmental grooves in
Hymenoptera (Gonzalez & Matthews 2002; Gonzalez et al.
2004b,c). Our study shows that 32, 18, 17, 16, 10 and 7% of
parasitoids lay eggs on pupal petiole, sternite, thorax, legs,
frons and anal region, respectively (Fig. 3), and the results
differ significantly (c2=22.5, P<0.0001). This result indi-
cates that the petiole of a pupa is the most preferable site for
oviposition of the parasitoids.
The mean fecundity of M. acasta on different regions of
B. terrestris pupae shows significant difference (ANOVA:
F5, 94 =12.3, P<0.001). The fecundity on petiole, sternite,
thorax, legs, frons and anal regions of the pupae are 26.4
Figure 1 Parasitism of Melittobia acasta on different life stages of
Bombus terrestris.
Figure 2 Fecundity of Melittobia acasta on different life stages of
Bombus terrestris.
Figure 3 Oviposition site preference of Melittobia acasta reared on
Bombus terrestris pupae.
Y. J. Kwon et al.
96 Entomological Research 42 (2012) 94–98
© 2011 The Authors. Entomological Research © 2011 The Entomological Society of Korea and Blackwell Publishing Asia Pty Ltd
11.3, 28.1 11.3, 13.6 8.8, 10.1 7.1, 34.9 15.1 and
13.4 5.6 female-1, respectively (Fig. 4).
In the onset of insect diapauses, falling temperatures can
play a role in determining in which state insects increase
tolerance to environmental extremes (Delinger 1985; Saun-
ders et al. 2002). Host–parasitoid systems react in changing
temperatures, but the reaction is not an immediate response
to environmental conditions. If the immature stages of the
parasitoids are subject to proper overwintering conditions
for entering diapause, they show little or no reaction with
long exposure to low temperature (Hance et al. 2007).
M. acasta usually overwinters at the larval stage and the
diapausing larvae start further development at approxi-
mately 20°C (Maeta 1978). Figure 5 shows the effect of
larval overwintering duration and host quality on pupation
and adult emergence of M. acasta. Results show that 89.5
and 88.0% of larvae turn to pupae when they overwinter for
30 or 45 days and feed on their original hosts. In contrast,
94.4 and 93.1% of larvae transform into pupae when they
overwinter for 30 or 45 days and feed on new hosts. These
results show that overwintering duration and host quality
have no effect on pupation to a significant level (c2=0.24, P
>0.05). There is no significant effect of larval overwintering
duration and host quality on adult emergence (c2=0.24, P>
0.05). Results show that 87.2 and 84.4% of pupae emerge as
adults when their larvae overwinter for 30 or 45 days and
feed on their original hosts. In contrast, 92.9 and 92.2% of
pupae emerge as adults when their larvae overwinter for 30
or 45 days and feed on new hosts. These results indicate that
diapausing hosts might remain as a physical refuge for the
parasitoids and parasitoid activity might be temporally sus-
pended. When conditions are favorable, parasitoids start
development and emerge as adults. Gonzalez et al. (2004b)
report that M. acasta larvae feeding on S. fistularium show
faster development with higher temperatures and the parasi-
toids occur widely under a broad range of environmental
conditions from tropical to temperate regions.
B. terrestris may be considered an ideal host for M. acasta
because female parasitoids show extreme parasitism (100%)
on the pupal stage of the bees. Petiole of a pupa is the most
favorable site for parasitism and oviposition. The female
parasitoids start oviposition within a short period of their
emergence and show a high level of fecundity in a relatively
short time. At a moderate temperature (25°C), overwintering
larvae transform into pupae then adults and overwintering
duration does not affect larval development. Higher percent-
ages of larvae emerge as pupae and then adults when they
feed on new hosts or their original hosts. Hence, the para-
sites show high reproductive capacity on B. terrestris pupae,
indicating that bumblebee colonies might be attacked by
M. acasta, especially where populations of these pollinators
are artificially manipulated.
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