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Can Anastatus bifasciatus Be Used for Augmentative Biological Control of the Brown Marmorated Stink Bug in Fruit Orchards?

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  • Plant protection service of Modena

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The generalist egg parasitoid Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) is the most prevalent egg parasitoid of the invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in Europe. To assess its efficacy against the pest H. halys and to validate the potential risks for non-target species in a realistic field setting, inundative releases were conducted over three consecutive years in four fruit orchards in Switzerland and Italy. In total, more than 4300 A. bifasciatus females were released, which was equivalent to 11,000 to 26,000 females per hectare, depending on distances between trees in each orchard. Parasitism of freeze-killed sentinel H. halys eggs achieved with the current release strategy was on average 6% (range: 2%-16%) and considered not high enough to effectively suppress the pest. However, the overall impact of A. bifasciatus on the mortality of H. halys eggs was likely underestimated. If pre-imaginal parasitoid mortality (3.3%) and host feeding (6%) are added to the observed parasitism (6%), the actual induced mortality of H. halys eggs may reach more than 15%. Parasitism of lepidopteran non-target species reached an average of 8% and thus, some degree of non-target parasitism after mass releases may be expected. To quantify the impact of the parasitoids in the orchards more precisely, naturally laid egg masses should be used in future trials to include host-finding cues of the host and host plants, and larger scale releases with potentially higher densities of parasitoids should be considered.
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insects
Article
Can Anastatus bifasciatus Be Used for Augmentative
Biological Control of the Brown Marmorated Stink
Bug in Fruit Orchards?
Judith M. Stahl 1, 2, * , Dirk Babendreier 1, Cristina Marazzi 3, Stefano Caruso 4, Elena Costi 5,
Lara Maistrello 5and Tim Haye 1
1
CABI, Rue des Grillons 1, 2800 Del
é
mont, Switzerland; d.babendreier@cabi.org (D.B.); t.haye@cabi.org (T.H.)
2Institute of Ecology and Evolutionary Biology, University of Bremen, Leobener Str. NW2,
28359 Bremen, Germany
3
Servizio Fitosanitario Cantonale, Dipartimento Delle Finanze e Dell’economia, Sezione Dell’agricoltura Viale
S. Franscini 17, 6501 Bellinzona, Switzerland; cristina.marazzi@ti.ch
4Consorzio Fitosanitario Provinciale di Modena, Via Santi Venceslao 14, 41123 Modena, Italy;
stefano.caruso@regione.emilia-romagna.it
5
Dipartimento di Scienze della Vita, Centro BIOGEST-SITEIA, Universit
à
di Modena e Reggio Emilia, Via G.
Amendola 2, 42122 Reggio-Emilia, Italy; elena.costi@unimore.it (E.C.); lara.maistrello@unimore.it (L.M.)
*Correspondence: judithmstahl@gmail.com
Received: 20 March 2019; Accepted: 12 April 2019; Published: 15 April 2019


Abstract:
The generalist egg parasitoid Anastatus bifasciatus (Georoy) (Hymenoptera: Eupelmidae) is
the most prevalent egg parasitoid of the invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae)
in Europe. To assess its ecacy against the pest H. halys and to validate the potential risks for non-target
species in a realistic field setting, inundative releases were conducted over three consecutive years
in four fruit orchards in Switzerland and Italy. In total, more than 4300 A. bifasciatus females were
released, which was equivalent to 11,000 to 26,000 females per hectare, depending on distances
between trees in each orchard. Parasitism of freeze-killed sentinel H. halys eggs achieved with the
current release strategy was on average 6% (range: 2%–16%) and considered not high enough to
eectively suppress the pest. However, the overall impact of A. bifasciatus on the mortality of H. halys
eggs was likely underestimated. If pre-imaginal parasitoid mortality (3.3%) and host feeding (6%) are
added to the observed parasitism (6%), the actual induced mortality of H. halys eggs may reach more
than 15%. Parasitism of lepidopteran non-target species reached an average of 8% and thus, some
degree of non-target parasitism after mass releases may be expected. To quantify the impact of the
parasitoids in the orchards more precisely, naturally laid egg masses should be used in future trials to
include host-finding cues of the host and host plants, and larger scale releases with potentially higher
densities of parasitoids should be considered.
Keywords:
egg parasitoid; Halyomorpha halys; inundative release; invasive species; non-target
eects; persistence
1. Introduction
Egg parasitoids (e.g., Trichogramma spp.) are advantageous for augmentative biological control
because they reduce host populations before the damaging stages of the pest [
1
,
2
]. A less well-known
group of parasitoids is the genus Anastatus Motschulsky (Hymenoptera: Eupelmidae), which
comprises primary endoparasitoids of a wide variety of hosts in the insect orders Hemiptera,
Lepidoptera, Blattodea, Orthoptera, and Mantodea [
3
5
]. Anastatus species are part of biological
control programs worldwide and are used against a number of hemipteran pests such as fruitspotting
Insects 2019,10, 108; doi:10.3390/insects10040108 www.mdpi.com/journal/insects
Insects 2019,10, 108 2 of 14
bugs, Amblypelta nitida Stål and A. lutescens lutescens Distant (Coreidae), in Australian macadamia
orchards [
6
8
], the citrus green stink bug, Rhynchocoris humeralis Thunberg (Pentatomidae), in Nepal [
9
]
or the litchi stink bug, Tessaratoma papillosa Drury (Pentatomidae), in China [
10
12
]. In the Beijing
Province of China, Anastatus sp. has been successfully mass released against the brown marmorated
stink bug Halyomorpha halys (Stål) (Pentatomidae) with parasitism levels of more than 60% [13].
Halyomorpha halys is native to China, Japan as well as Korea, and has become invasive in the
Americas and Europe in the mid-1990s and early 2000s, respectively [
14
16
]. Since its arrival in
Switzerland, it has spread throughout many European countries [
17
]. It is a pest of a wide variety
of economically important vegetable, fruit, and leguminous crops as well as ornamentals in both
its native and invaded range [
18
,
19
]. Severe damage has been caused in fruit crops and hazelnuts
in the USA, Georgia, and Italy [
20
22
]. In response, the number of insecticide treatments in certain
regions has increased four-fold since the introduction of H. halys, thereby disrupting existing integrated
pest management (IPM) programs, which led to outbreaks of secondary insect pests [
20
]. Due to the
negative environmental eects of pesticide applications, environmentally friendly solutions such as
biological control are needed. Augmentative biological control using native natural enemies against
invasive species is a new approach and, to date, only a few examples exist, such as the use of Trichopria
drosophilae Perkins (Hymenoptera: Diapriidae) against the spotted wing drosophila Drosophila suzukii
(Matsumura) (Diptera: Drosophilidae) [
23
,
24
]. In Switzerland and Italy, Anastatus bifasciatus (Georoy)
is the most prevalent native parasitoid successfully parasitizing H. halys eggs in the field [
25
27
]. It is
one of the two European egg parasitoids capable of developing in viable H. halys eggs [
26
,
28
] and thus,
it was selected as a potential candidate for inundative biological control of H. halys in Europe. Its host
range, however, comprises more than 50 heteropteran and lepidopteran species and there are concerns
that mass releases of A. bifasciatus might lead to undesired non-target eects [29,30].
The present experimental field study aimed to assess the ecacy of A. bifasciatus against H. halys
and validate the potential risks for non-target species in a realistic field setting. Inundative releases
were conducted over three consecutive years in four fruit orchards in Switzerland and Italy to develop
a release strategy and answer the following questions: (1) What level of egg parasitism can be achieved
by releasing A. bifasciatus against H. halys in fruit orchards? (2) Are non-target species parasitized by
A. bifasciatus in the field? (3) Does A. bifasciatus persist in fruit orchards after releases?
2. Materials and Methods
2.1. Parasitoid Rearing
The laboratory rearing of A. bifasciatus originated from two parasitized H. halys egg masses
collected by S. Fischer (Agroscope Changins, Nyon, Switzerland) in the Canton of Valais, Switzerland,
in 2014 [
25
]. Individuals of the founder population were identified by L. Fusu (University of Iasi,
Romania). Approximately 50 adults (sex ratio 1:1) were kept in 100
×
115 mm mesh-top cylindrical
plastic containers, placed above a 90
×
20 mm Petri dish filled with 1:10 honey water solution, which
was provided to the parasitoids by two cotton wicks connecting the Petri dish to the plastic container.
The rearing containers were stored in an incubator at a light/temperature cycle of L 16 h/20
C and
D8h/15 C
. Twice a week the wasps in each container were provided with approximately 150 new host
eggs glued to cardboard pieces. The removed egg cards were stored at 26
C until the emergence of the
new generation. Newly emerged wasps were collected daily and transferred to the rearing containers.
In the first year of the study (2016), A. bifasciatus was reared on eggs of H. halys. When females were
seven days old, they were provided with new eggs until the day of release. In the second and third
year (2017/2018), to increase the rearing and produce larger females [
30
]A. bifasciatus females were
reared on a mix of H. halys and Dendrolimus pini (L.) (Lepidoptera: Lasiocampidae) eggs in Switzerland
and on a mix of H. halys and Manduca sexta (Lepidoptera: Sphingidae) in Italy. Halyomorpha halys eggs
were produced following the methods described in Reference [30].
Insects 2019,10, 108 3 of 14
2.2. Release Sites
Releases were conducted in three apple orchards in Switzerland and a single pear orchard in
Italy (Table 1). In each orchard, an area of 60 trees in 4 neighboring rows (15 trees per row) located in
the center of the orchard was selected as release plot. Depending on the distance between rows and
between trees within rows the size of the plots varied between 210 and 480 m
2
(Table 1). All sites were
equipped with a data logger (“HOBO Pendant Temperature/Light 64K”, Onset Computer Corporation,
Bourne, MA, USA), to record the ambient temperature for the length of the experiment.
Table 1. Field sites for experimental A. bifasciatus releases between 2016 and 2018.
Site
Location
(Municipality,
Canton/Region,
Country)
GPS
Coordinates Management Host Plants in Plot
(Species, Variety)
H. halys
Presence
Release
Plot
Size
[m2]
Number
of
Releases
1Lindau, Zurich,
Switzerland
4726’52.0”N
840’47.6”E IPM Malus pumila, Golden
Delicious/Diwa/Braeburn
no 210 4
2
Bellinzona,
Ticino,
Switzerland
4609’42.1”N
858’12.2”E IPM Malus pumila, Golden
Delicious/Braeburn yes 288 2
3Manno, Ticino,
Switzerland
4601’52.8”N
855’20.4”E Organic
Malus pumila, unknown
varieties yes 212 1
4Carpi, Emilia-
Romagna, Italy
4443’46.8”N
1052’30.0”E Organic Pyrus communis, Abate
Fetel yes 480 1
2.3. Egg Exposure
2.3.1. Parasitoid Ecacy and Persistence
Halyomorpha halys eggs were collected daily from the laboratory rearing, frozen for no longer than
one month at 80 C and thawed earliest two days before the release date. For exposure, egg masses
with at least 20 eggs were used (mean
±
SE: 26.0
±
0.09). In each step of the experiment, sentinel
H. halys egg masses were glued directly on the underside of leaves of apple/pear trees at a height of
50 to 180 cm. Branches of various host plants with feeding traces of H. halys were taken from the
laboratory rearing cages and fixed next to the egg masses (one branch per egg mass) with a twist tie to
increase the chance of parasitism by adding chemical cues of the host. Exposure times varied between
four and seven days, depending on local weather conditions and phytosanitary treatment schedules
(Table 2).
Table 2.
Overview of H. halys egg masses exposed before parasitoid releases (“pre-release monitoring”),
directly after releases within the release plot (“release”) and two weeks after releases (“post-release
monitoring”).
Exposure Date Location Treatment
Mean
Temperature
(Min – Max) [C]
Egg Masses
(Eggs)
Exposed
Egg Masses
(Eggs)
Recovered 1
2016
23.–28. Jul
1 – Lindau
Pre-release
monitoring 22.4 (12.9–36.0) 25 (657) 22 (575)
28. Jul – 2. Aug Release 21.7 (12.4–38.3) 97 (2653) 93 (2409)
11.–16. Aug Post-release
monitoring 21.8 (9.6–36.6) 55 (1480) 54 (1459)
16.–21. Aug Release 20.4 (12.1–36.6) 90 (2410) 83 (2258)
Insects 2019,10, 108 4 of 14
Table 2. Cont.
Exposure Date Location Treatment
Mean
Temperature
(Min – Max) [C]
Egg Masses
(Eggs)
Exposed
Egg Masses
(Eggs)
Recovered 1
2017
17.–21. Jul
1 – Lindau
Pre-release
monitoring 23.0 (13.8–34.5) 25 (623) 15 (298)
29. Jul–3. Aug Release 23.2 (15.3–35.0) 90 (2273) 20 (479)
10.–17. Aug Post-release
monitoring 18.8 (10.2–32.7) 55 (1410) 23 (562)
2.–10. Aug
2 – Bellinzona
Pre-release
monitoring 23.4 (15.3–38.5) 25 (637) 20 (416)
14.–21. Aug Release 23.1 (10.9–35.2) 90 (2327) 89 (1897)
28. Aug–4. Sep Post-release
monitoring 21.2 (12.3–33.5) 55 (1387) 53 (774)
2018
19.–25. Jul
2 – Bellinzona
Pre-release
monitoring 25.0 (13.9–38.3) 25 (685) 22 (1371)
25.–30. Jul Release 26.1 (15.5–37.9) 90 (2418) 90 (2205)
8.–13. Aug Post-release
monitoring 23.7 (16.8–36.4) 55 (2697) 51 (1940)
19.–25. Jul
4 – Carpi
Pre-release
monitoring 25.0 (16.0–35.0) 25 (694) 25 (363)
25.–30. Jul Release 26.5 (17.0–36.5) 90 (2392) 82 (1780)
9.–14. Aug Post-release
monitoring 25.4 (17.0–35.5) 55 (1469) 55 (958)
25.–30. Jul
3 – Manno
Pre-release
monitoring 26.6 (15.3–44.5) 25 (752) 20 (545)
30. Jul–3. Aug Release 28.0 (17.5–39.4) 90 (2347) 68 (957)
13.–17. Aug Post-release
monitoring 23.1 (14.6–34.7) 55 (1677) 51 (1345)
6.–10. Aug
1 – Lindau
Pre-release
monitoring Na 25 (611) 10 (58)
11.–15. Aug Release Na 90 (2303) 85 (1026)
24.–28. Aug Post-release
monitoring Na 55 (1760) 51 (1536)
Total 1287 (35,662) 1082 (25,340)
1healthy looking eggs, neither collapsed nor predated on.
Five days prior releases, 25 H. halys egg masses were randomly distributed in each orchard,
independent of its size, to measure parasitism of potential natural A. bifasciatus populations at each
site (Table 2). On the day of the release, these egg masses were recollected, and 90 new egg masses
were exposed inside the experimental plot (Table 2). Within the plot, 15 trees each were randomly
equipped with 0, 1, 2, or 3 H. halys egg masses. During the first two releases in site 1 (2016), 32 H. halys
egg masses each were exposed on 16 trees outside of, but in close proximity to, the experimental plot
(up to eight meters distance) (Figure 1). Four to seven days after all parasitoid releases, exposed egg
masses were recollected (Table 2). Fourteen days after the release, an additional 55 egg masses were
placed out to monitor the persistence of the parasitoids (Table 2). Twenty-five of those egg masses
Insects 2019,10, 108 5 of 14
were randomly distributed over 25 trees within the entire orchard, while the remaining 30 egg masses
were placed on every second tree within the release plots.
Insects 2019, 10 FOR PEER REVIEW 5
Figure 1. Site 1 with release plot (golden square) for releases 2016
2018, position of H. halys
egg masses outside of release plot in 2016. Changed after Reference [31].
2.3.2. Non-target parasitism
Depending on the availability of non-target species in each year of the study, eggs of six different
lepidopteran species were exposed in the four release events (Table 3). In Switzerland, apart from
Euthrix potatoria (L.) (Lasiocampidae), all non-target species were obtained from commercial insect
breeders, the majority as pupae, and Macrothylacia rubi (L.) (Lasiocampidae) as eggs. Euthrix potatoria
caterpillars were collected in Bärschwil, Switzerland, and reared until the adult stage in 50 × 50 × 50
cm gauze cages (“BugDorm-4090 Insect Rearing Cage”, MegaView Science Co. Ltd., Taichung,
Taiwan) on Dactylis glomerata L. (Poaceae), which was replaced daily. Once the adult stage was
reached, all non-target species were kept in a 50 × 50 × 50 cm gauze cage for oviposition and provided
with honey water and if necessary, their associated host plants as oviposition stimulus. In Italy, adult
females of Macrothylacia rubi (L.) (Lasiocampidae) and Lasiocampa quercus (L.) (Lasiocampidae) were
collected in natural parks using light traps and placed in 50 × 50 × 50 cm gauze cages (one cage for
each species) together with their host plants as oviposition stimulus.
Newly laid eggs (<24 h) were frozen for no longer than one month at 80 °C and thawed no more
than two days before the release date. Freeze-killed non-target egg batches of three to six eggs (see
Table 3) were added to about half of the trees inside the release plot that were previously equipped
with H. halys egg masses (28 and 24 out of 45 trees in 2016 and 2017/18, respectively). The density of
non-target egg masses was matched with the densities of H. halys egg masses (0, 1, 2, or 3 egg masses),
but not with the total number of eggs within the egg masses (Table 3). Non-target egg masses were
randomly assigned to trees within the plot and egg batches were glued on the underside of leaves in
close vicinity of the H. halys egg masses.
In the first release event in 2016, mainly E. potatoria eggs were exposed, but to better understand
the potential influence of different non-target hosts, seven additional trees within the plot were
equipped with one H. halys and one Samia cynthia (Drury) (Saturniidae) egg mass each. In all
following release events, only eggs of single non-target species were used, apart from the release at
site 4, where each tree was equipped with three eggs of M. rubi and three eggs of Lasiocampa quercus
(L.) (Lasiocampidae) (Table 3).
Figure 1.
Site 1 with release plot (golden square) for releases 2016–2018, position of H. halys egg masses
outside of release plot in 2016. Changed after Reference [31].
2.3.2. Non-target parasitism
Depending on the availability of non-target species in each year of the study, eggs of six dierent
lepidopteran species were exposed in the four release events (Table 3). In Switzerland, apart from
Euthrix potatoria (L.) (Lasiocampidae), all non-target species were obtained from commercial insect
breeders, the majority as pupae, and Macrothylacia rubi (L.) (Lasiocampidae) as eggs. Euthrix potatoria
caterpillars were collected in Bärschwil, Switzerland, and reared until the adult stage in
50 ×50 ×50 cm
gauze cages (“BugDorm-4090 Insect Rearing Cage”, MegaView Science Co. Ltd., Taichung, Taiwan)
on Dactylis glomerata L. (Poaceae), which was replaced daily. Once the adult stage was reached, all
non-target species were kept in a 50
×
50
×
50 cm gauze cage for oviposition and provided with honey
water and if necessary, their associated host plants as oviposition stimulus. In Italy, adult females of
Macrothylacia rubi (L.) (Lasiocampidae) and Lasiocampa quercus (L.) (Lasiocampidae) were collected in
natural parks using light traps and placed in 50
×
50
×
50 cm gauze cages (one cage for each species)
together with their host plants as oviposition stimulus.
Newly laid eggs (<24 h) were frozen for no longer than one month at
80
C and thawed no more
than two days before the release date. Freeze-killed non-target egg batches of three to six eggs (see
Table 3) were added to about half of the trees inside the release plot that were previously equipped
with H. halys egg masses (28 and 24 out of 45 trees in 2016 and 2017/18, respectively). The density of
non-target egg masses was matched with the densities of H. halys egg masses (0, 1, 2, or 3 egg masses),
but not with the total number of eggs within the egg masses (Table 3). Non-target egg masses were
randomly assigned to trees within the plot and egg batches were glued on the underside of leaves in
close vicinity of the H. halys egg masses.
In the first release event in 2016, mainly E. potatoria eggs were exposed, but to better understand the
potential influence of dierent non-target hosts, seven additional trees within the plot were equipped
Insects 2019,10, 108 6 of 14
with one H. halys and one Samia cynthia (Drury) (Saturniidae) egg mass each. In all following release
events, only eggs of single non-target species were used, apart from the release at site 4, where each
tree was equipped with three eggs of M. rubi and three eggs of Lasiocampa quercus (L.) (Lasiocampidae)
(Table 3).
Table 3. Exposure of non-target eggs during experimental A. bifasciatus field releases 2016–2018.
Species Site Year Egg Batch Size Total # Eggs Exposed/Site
Samia cynthia (Drury) (Saturniidae) 1 2016 6 42
Euthrix potatoria (L.) (Lasiocampidae) 1 2016 6 252
Odonestis pruni (L.) (Lasiocampidae) 1 2016 4 168
Dendrolimus pini (L.) (Lasiocampidae) 1, 2 2017 4 192
Lasiocampa quercus (L.) (Lasiocampidae)
1, 2, 3, 4 2018 6 (3 in site 4) 288 (144)
Macrothylacia rubi (L.) (Lasiocampidae) 4 2018 3 144
2.4. Parasitoid Releases
All females used for releases were considered experienced with the target host because they
were provided with H. halys eggs prior to releases. Females were deprived of hosts the week before
release, so they would store their eggs and have a higher egg load when released. The day before
release, females 1 to 5 weeks of age were transferred with glass pipettes into release devices and stored
overnight under the rearing conditions described above. Release devices were made of clear plastic
cups (8 cm high, 6 cm wide at the top). At the bottom, a small opening used for transferring the
parasitoids was covered with a piece of foam dipped in honey to provide parasitoids with food. The
top of the cup was covered with mesh wide enough (1.9
×
1.8 mm) to allow A. bifasciatus females to
pass. For transport, the cups were closed with screw lids. In addition, cups were wrapped with black
paper to ensure parasitoids would move upwards towards the natural light when cups were opened
for release. Twelve cups containing 45 females each were equally distributed along the four rows of
the plot (3/row) and placed at least five meters apart from each other. Cups were hung into the canopy
at a height of 80 cm and fixed with twist ties. For release, screw lids were removed, and within the first
hour, all parasitoids had left the containers.
2.5. Treatment of Recollected Eggs
Recollected eggs were stored individually in small 54
×
14 mm Petri dishes at 26
C, 70% RH, and
a 16L:8D photoperiod. Eggs were counted and assigned to one of the following categories: collapsed,
chewed, sucked (see Reference [
32
]) or intact eggs. Collapsed eggs were defined as eggs that looked
undamaged but had lost more than half of their volume.
Emerging wasps were counted, sexed and collected daily until no emergence was observed for
four weeks. Parasitism was measured by the total number of eggs producing ospring divided by the
sum of all intact eggs. Eggs that had been attacked by chewing or sucking predators or had collapsed
in the field were excluded from the analysis since it was not possible to detect whether these eggs
had been parasitized. Predation was calculated by the number of eggs showing signs of chewing or
sucking divided by the sum of eggs with signs of predation and intact eggs. Halyomorpha halys and
non-target egg masses recovered in 2017 were overwintered in 54
×
14 mm Petri dishes under outdoor
conditions in an open wooden shelter [Canton Jura, Switzerland (N47
22’23; E 7
19’32)] four weeks
after emergence had stopped. The following year, egg masses were checked daily for emergence from
May onwards.
2.6. Statistical Analyses
The influence of the distance to the closest release point on egg parasitism levels was analyzed for
the first two years of the experiment, using a linear regression with the Theil-Sen estimator modified
by Siegel repeated medians. The relationship between host density (measured as recovered H. halys
Insects 2019,10, 108 7 of 14
eggs from a tree) and host impact was investigated using a generalized linear model (GLM) with a
quasipoisson error distribution with the log link function. Statistical analyses were conducted with
R version 3.2.3 [
33
] using the development environment RStudio Version 1.0.136 [
34
]. The package
applied for the Theil-Sen estimator was ‘mblm’ [35].
3. Results
3.1. Parasitoid Ecacy and Persistence
Natural parasitism of sentinel egg masses prior to releases was overall low (site 2) or absent,
with the exception of site 4 (Carpi), where it reached 28% (7 out of 25 egg masses). At site 1 (Lindau),
parasitoids had been released in 2016, but no parasitism was detected in eggs exposed prior to releases
in 2017.
After releasing A. bifasciatus, parasitism of sentinel H. halys eggs was detected in each orchard
(Figure 2). On average, 22.04%
±
5.41% (SE) (range: 6.67%–37.6%) (n=8) of the recovered egg masses
were parasitized. Since only an average of 28.2%
±
4.15% (SE) (range: 18.4%–48.4%) (n=8) of the eggs
in parasitized egg masses yielded parasitoid ospring (host exploitation), the actual egg parasitism
was much lower, averaging 6.02%
±
1.70% (SE) (range: 2.00%–16.0%) (n=8) when data from all
years and release events were combined. Eggs that were exposed at sites 1 and 2 in July/August 2017
did not produce any A. bifasciatus ospring after overwintering in 2018. There was no significant
relationship between host density, measured as the number of recovered eggs per tree, and number of
parasitized eggs (quasipoisson GLM, df =1,80,
χ2
=0.00775, p=0.930). Both chewing and sucking
predation was recorded at all sites (Figure 3), averaging 5.29%
±
1.83% (SE) (range: 0.04%–13.1%) and
0.789% ±0.458% (SE)
(range: 0.00%–3.88%) (both n=8), respectively (Figure 3). Halyomorpha halys
egg masses placed outside the release plots in the first two releases (site 1, 2016) yielded parasitoid
ospring, but the level of parasitism was low. The number of parasitized H. halys eggs increased
with decreasing distance to the nearest release point (linear regression, df =119, v=254.5, p<0.001;
Figure 4).
Insects 2019, 10 FOR PEER REVIEW 7
3. Results
3.1. Parasitoid Efficacy and Persistence
Natural parasitism of sentinel egg masses prior to releases was overall low (site 2) or absent,
with the exception of site 4 (Carpi), where it reached 28% (7 out of 25 egg masses). At site 1 (Lindau),
parasitoids had been released in 2016, but no parasitism was detected in eggs exposed prior to
releases in 2017.
After releasing A. bifasciatus, parasitism of sentinel H. halys eggs was detected in each orchard
(Figure 2). On average, 22.04% ± 5.41% (SE) (range: 6.67%–37.6%) (n = 8) of the recovered egg masses
were parasitized. Since only an average of 28.2% ± 4.15% (SE) (range: 18.4%–48.4%) (n = 8) of the eggs
in parasitized egg masses yielded parasitoid offspring (host exploitation), the actual egg parasitism
was much lower, averaging 6.02% ± 1.70% (SE) (range: 2.00%–16.0%) (n = 8) when data from all years
and release events were combined. Eggs that were exposed at sites 1 and 2 in July/August 2017 did
not produce any A. bifasciatus offspring after overwintering in 2018. There was no significant
relationship between host density, measured as the number of recovered eggs per tree, and number
of parasitized eggs (quasipoisson GLM, df = 1,80, χ2 = 0.00775, p = 0.930). Both chewing and sucking
predation was recorded at all sites (Figure 3), averaging 5.29% ± 1.83% (SE) (range: 0.04%–13.1%) and
0.789% ± 0.458% (SE) (range: 0.00%–3.88%) (both n = 8), respectively (Figure 3). Halyomorpha halys egg
masses placed outside the release plots in the first two releases (site 1, 2016) yielded parasitoid
offspring, but the level of parasitism was low. The number of parasitized H. halys eggs increased with
decreasing distance to the nearest release point (linear regression, df = 119, v = 254.5, p < 0.001; Figure
4).
Figure 2. Parasitism measured by A. bifasciatus offspring emergence of sentinel H. halys egg
masses exposed after A. bifasciatus releases for 4–7 days between 2016 and 2018 in
Switzerland and Italy. Site numbers correspond with Table 1.
0
10
20
30
40
50
60
Site 1 Site 1 Site 1 Site 2 Site 1 Site 2 Site 3 Site 4
2016 2017 2018
Parasitism of H. halys [%]
parasitized egg masses
parasitized eggs within parasitized egg masses
total parasitized eggs
Figure 2.
Parasitism measured by A. bifasciatus ospring emergence of sentinel H. halys egg masses
exposed after A. bifasciatus releases for 4–7 days between 2016 and 2018 in Switzerland and Italy. Site
numbers correspond with Table 1.
Insects 2019,10, 108 8 of 14
Insects 2019, 10 FOR PEER REVIEW 8
Figure 3. Fate of sentinel H. halys eggs exposed inside the release plots in Switzerland and
Italy for 47 days after A. bifasciatus releases. Site numbers correspond with Table 1.
Figure 4. Number of H. halys eggs parasitized by A. bifasciatus depending on the distance to
the closest release point during the first two releases in 2016 (site 1).
Sentinel H. halys egg masses exposed two weeks after A. bifasciatus releases yielded parasitoid
offspring in three out of the eight release events. However, in the one case where natural A. bifasciatus
population were found in the orchard, it remains unclear if detected parasitism was caused by
released parasitoids or naturally occurring ones (site 4). On average, A. bifasciatus offspring emerged
from 3.24% ± 1.73% (SE) (range: 0.00%–16.7%) (n = 9) of the recovered egg masses and from 2.30% ±
1.75% (SE) (range: 0.00%–16.0%) (n = 9) of the recovered eggs.
3.2. Non-target Parasitism
Non-target parasitism occurred at all release sites, and five out of six non-target species yielded
A. bifasciatus offspring. There was no indication of parasitism of S. cynthia eggs (recovered n = 29
eggs). The average parasitism of non-target eggs over all the eight releases was 8.11% ± 2.42% (SE) (n
= 8), when eggs of the five parasitized species were combined (E. potatoria: 2.30%, n = 175; O. pruni:
6.70%, n = 120; D. pini: 7.58% n = 145; L. quercus: 11.7%, n = 103; M. rubi: 16.9%, n = 124) and ranged
0
500
1000
1500
2000
2500
Site 1 Site 1 Site 1 Site 2 Site 1 Site 2 Site 3 Site 4
2016 2017 2018
# H. halys eggs
lost collapsed chewed sucked parasitised healthy
0
5
10
15
20
25
30
0246810
# of parasitized H. halys eggs
Distance to next release point [m]
Figure 3.
Fate of sentinel H. halys eggs exposed inside the release plots in Switzerland and Italy for
4–7 days after A. bifasciatus releases. Site numbers correspond with Table 1.
Insects 2019, 10 FOR PEER REVIEW 8
Figure 3. Fate of sentinel H. halys eggs exposed inside the release plots in Switzerland and
Italy for 47 days after A. bifasciatus releases. Site numbers correspond with Table 1.
Figure 4. Number of H. halys eggs parasitized by A. bifasciatus depending on the distance to
the closest release point during the first two releases in 2016 (site 1).
Sentinel H. halys egg masses exposed two weeks after A. bifasciatus releases yielded parasitoid
offspring in three out of the eight release events. However, in the one case where natural A. bifasciatus
population were found in the orchard, it remains unclear if detected parasitism was caused by
released parasitoids or naturally occurring ones (site 4). On average, A. bifasciatus offspring emerged
from 3.24% ± 1.73% (SE) (range: 0.00%–16.7%) (n = 9) of the recovered egg masses and from 2.30% ±
1.75% (SE) (range: 0.00%–16.0%) (n = 9) of the recovered eggs.
3.2. Non-target Parasitism
Non-target parasitism occurred at all release sites, and five out of six non-target species yielded
A. bifasciatus offspring. There was no indication of parasitism of S. cynthia eggs (recovered n = 29
eggs). The average parasitism of non-target eggs over all the eight releases was 8.11% ± 2.42% (SE) (n
= 8), when eggs of the five parasitized species were combined (E. potatoria: 2.30%, n = 175; O. pruni:
6.70%, n = 120; D. pini: 7.58% n = 145; L. quercus: 11.7%, n = 103; M. rubi: 16.9%, n = 124) and ranged
0
500
1000
1500
2000
2500
Site 1 Site 1 Site 1 Site 2 Site 1 Site 2 Site 3 Site 4
2016 2017 2018
# H. halys eggs
lost collapsed chewed sucked parasitised healthy
0
5
10
15
20
25
30
0246810
# of parasitized H. halys eggs
Distance to next release point [m]
Figure 4.
Number of H. halys eggs parasitized by A. bifasciatus depending on the distance to the closest
release point during the first two releases in 2016 (site 1).
Sentinel H. halys egg masses exposed two weeks after A. bifasciatus releases yielded parasitoid
ospring in three out of the eight release events. However, in the one case where natural A. bifasciatus
population were found in the orchard, it remains unclear if detected parasitism was caused by released
parasitoids or naturally occurring ones (site 4). On average, A. bifasciatus ospring emerged from
3.24% ±1.73% (SE)
(range: 0.00%–16.7%) (n=9) of the recovered egg masses and from 2.30%
±
1.75%
(SE) (range: 0.00%–16.0%) (n=9) of the recovered eggs.
3.2. Non-target Parasitism
Non-target parasitism occurred at all release sites, and five out of six non-target species yielded
A. bifasciatus ospring. There was no indication of parasitism of S. cynthia eggs (recovered
n=29 eggs
).
The average parasitism of non-target eggs over all the eight releases was 8.11%
±
2.42% (SE)
(n=8)
,
when eggs of the five parasitized species were combined (E. potatoria: 2.30%, n=175; O. pruni: 6.70%,
n=120; D. pini: 7.58% n=145; L. quercus: 11.7%, n=103; M. rubi: 16.9%, n=124) and ranged from
1.63% to 22.2% (n=8) between release events (Figure 5). On average, 12.3%
±
4.20% (SE) (range:
Insects 2019,10, 108 9 of 14
3.3%1–39.4%) (n=8) of the recovered non-target egg masses were parasitized, and an average of
51.3% ±8.84% (SE)
(range: 19.2%–100%) (n=8) of the eggs in parasitized egg masses yielded parasitoid
ospring (Figure 5).
Insects 2019, 10 FOR PEER REVIEW 9
from 1.63% to 22.2% (n = 8) between release events (Figure 5). On average, 12.3% ± 4.20% (SE) (range:
3.3%1–39.4%) (n = 8) of the recovered non-target egg masses were parasitized, and an average of
51.3% ± 8.84% (SE) (range: 19.2%–100%) (n = 8) of the eggs in parasitized egg masses yielded
parasitoid offspring (Figure 5).
Figure 5. Parasitism measured by A. bifasciatus offspring emergence of sentinel non-target
egg masses exposed after A. bifasciatus releases for 4–7 days between 2016 and 2018 in
Switzerland and Italy. Site numbers correspond with Table 1.
4. Discussion
After experimental releases of A. bifasciatus females, moderate parasitism of sentinel H. halys
eggs was detected in all eight release events at the four experimental sites. In two out of eight release
events parasitism of sentinel eggs by natural A. bifasciatus populations was detected prior to releases.
Accordingly, for these releases, it was impossible to distinguish if the observed parasitism following
the releases was indeed caused by the released parasitoids or naturally occurring ones. In
comparison, field releases of another European egg parasitoid, Ooencyrtus telenomicida (Vassiliev)
(Hymenoptera: Encyrtidae) only elicited parasitism at 3 out of 6 release sites [26]. When estimating
parasitism as the proportion of trees carrying at least one parasitized sentinel egg mass, A. bifasciatus
was recovered from 30% of the trees. This is comparable with the results of experimental releases of
Anastatus sp. in Australian macadamia orchards against fruitspotting bugs Amblypelta nitida Stål and
A. lutescens lutescens Distant (Hemiptera: Coreidae), where parasitized host eggs were recovered from
24% of the plot trees [8].
Host exploitation (proportion of parasitized eggs within an egg mass) by A. bifasciatus was rather
low (28%), which may be explained by the low weekly fecundity of the parasitoids [36], assuming
that parasitized egg masses were visited by single or few females. In the present study, A. bifasciatus
females were deprived of host eggs for one-week prior releases to increase the number of stored eggs
and parasitoids’ host searching motivation [37], but this approach did not result in higher host
exploitation. Unfortunately, there is no information about the behavior of A. bifasciatus in the field
that might help explain the low exploitation values and improve release efficacy. To increase host
exploitation by decreasing patch-leaving stimuli, dispersal capacities can be reduced by arresting
natural enemies within the patch with chemical cues [37].
When data from all releases were combined, total egg parasitism was on average 6%. Based on
the mean host exploitation value in the field (6.70 eggs), only 1% of the 540 released females would
have been responsible for the observed parasitism if each of the egg masses was found by only one
female. This could also be connected to the small experimental plots, where dispersal is more likely
than from bigger areas such as a whole orchard. Calculations carried out by Reference [38] after
0
20
40
60
80
100
Site 1 Site 1 Site 1 Site 2 Site 1 Site 2 Site 3 Site 4
2016 2017 2018
Parasitism of non-target species [%]
parasitized egg masses
parasitized eggs within parasitized egg masses
total parasitized eggs
Figure 5.
Parasitism measured by A. bifasciatus ospring emergence of sentinel non-target egg masses
exposed after A. bifasciatus releases for 4–7 days between 2016 and 2018 in Switzerland and Italy. Site
numbers correspond with Table 1.
4. Discussion
After experimental releases of A. bifasciatus females, moderate parasitism of sentinel H. halys
eggs was detected in all eight release events at the four experimental sites. In two out of eight release
events parasitism of sentinel eggs by natural A. bifasciatus populations was detected prior to releases.
Accordingly, for these releases, it was impossible to distinguish if the observed parasitism following
the releases was indeed caused by the released parasitoids or naturally occurring ones. In comparison,
field releases of another European egg parasitoid, Ooencyrtus telenomicida (Vassiliev) (Hymenoptera:
Encyrtidae) only elicited parasitism at 3 out of 6 release sites [
26
]. When estimating parasitism as the
proportion of trees carrying at least one parasitized sentinel egg mass, A. bifasciatus was recovered
from 30% of the trees. This is comparable with the results of experimental releases of Anastatus sp.
in Australian macadamia orchards against fruitspotting bugs Amblypelta nitida Stål and A. lutescens
lutescens Distant (Hemiptera: Coreidae), where parasitized host eggs were recovered from 24% of the
plot trees [8].
Host exploitation (proportion of parasitized eggs within an egg mass) by A. bifasciatus was rather
low (28%), which may be explained by the low weekly fecundity of the parasitoids [
36
], assuming that
parasitized egg masses were visited by single or few females. In the present study, A. bifasciatus females
were deprived of host eggs for one-week prior releases to increase the number of stored eggs and
parasitoids’ host searching motivation [
37
], but this approach did not result in higher host exploitation.
Unfortunately, there is no information about the behavior of A. bifasciatus in the field that might help
explain the low exploitation values and improve release ecacy. To increase host exploitation by
decreasing patch-leaving stimuli, dispersal capacities can be reduced by arresting natural enemies
within the patch with chemical cues [37].
When data from all releases were combined, total egg parasitism was on average 6%. Based on the
mean host exploitation value in the field (6.70 eggs), only 1% of the 540 released females would have
been responsible for the observed parasitism if each of the egg masses was found by only one female.
This could also be connected to the small experimental plots, where dispersal is more likely than
from bigger areas such as a whole orchard. Calculations carried out by Reference [
38
] after releases of
Insects 2019,10, 108 10 of 14
Trichogramma nubilale Ertle and Davis (Hymenoptera: Trichogrammatidae) revealed that every day 40%
of the parasitoid females disappeared, which was attributed to the hot and dry weather conditions. In
the present study, weather conditions at release sites were extremely hot and dry over the three years
of the study and may have caused some degree of adult mortality. Another factor that might have
influenced observed parasitism levels is intraguild predation. Some sentinel eggs that showed signs of
predation also had A. bifasciatus host feeding marks, indicating that at least some parasitized eggs had
been eaten by predators. As interactions between parasitoids and predators of H. halys have not been
studied so far [28], future studies on the subject could provide valuable input.
Host location of parasitoids is facilitated by a number of cues that can either be emitted by the host
plant [
39
], the host itself [
40
] or a combination of the two factors. The experimental design of the current
study was aimed to provide natural conditions and include host cues provided by branches with
feeding and walking traces of H. halys next to the sentinel egg masses, assuming that these traces guide
parasitoids to their hosts, as demonstrated for Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae)
locating egg masses of Nezara viridula (L.) (Heteroptera: Pentatomidae) [
41
]. At the beginning of the
release experiments, the factors influencing the host finding of A. bifasciatus were unknown, but in the
meantime [
42
] demonstrated that A. bifasciatus positively responded to adult H. halys male volatiles
and to H. halys-induced plant volatiles, indicating ability to exploit cues associated with the new host
for egg location. Consequently, sentinel H. halys egg masses exposed in this study may have lacked
important chemical cues associated with H. halys egg masses in nature, resulting in much lower host
finding and thus, lower parasitism by A. bifasciatus. In a preliminary trial at site 4, reproductive H. halys
adults were set up in sleeve cages on randomly selected trees two days before the A. bifasciatus release
with the aim to expose naturally laid and frozen egg masses simultaneously. Although the number of
egg masses laid in the sleeve cages (n=8) was too low to obtain meaningful results, parasitism of
naturally laid eggs (n=99) was remarkably higher (48.5%) compared to the frozen sentinel eggs (16%),
indicating the importance of considering naturally laid egg masses in future release trials (LM, EC, SC,
unpublished data).
Apart from trying to increase host exploitation, releasing higher numbers of parasitoids is another
alternative to increase pest suppression. In the present study, the release density was 540 female
A. bifasciatus per 60 trees, which translates to 11,000 (site 4) to 26,000 (site 1) females per hectare,
depending on the distances between rows and trees within rows. In comparison, many commercial
and experimental releases involve larger quantities of parasitoids, such as several times 100,000
Trichogramma per hectare [
43
]. In China, commercial releases of the closely related A. japonicus against
less severe infestations of the litchi stink bug, T. papillosa, required180 females per medium-sized tree,
which is significantly more than in the present experiments, and yield an average of 52–94% parasitism
in the first year of its releases [44].
Measuring parasitism by ospring emergence is less labor-intensive than dissections, but
underestimates the actual levels of parasitism if a proportion of individuals cannot undergo complete
development. Dissections of parasitized hosts often have the disadvantage that tiny eggs and early
instar larvae of parasitoids can be hard to detect inside hosts, and remains of dead parasitoids may be
dicult to recognize when hosts decay. An alternative method to detect parasitoids inside their hosts is
the use of molecular markers [
45
,
46
]. The analysis of remaining unemerged eggs from parasitized egg
masses from site 1 in 2017 showed that 14% contained dead developmental stages of A. bifasciatus [
47
],
suggesting that host exploitation was indeed much higher than what was measured by ospring
emergence. Another important behavioral trait of A. bifasciatus is host feeding [
36
]. Since many
parasitoids kill hosts by host feeding as well as parasitism, this is a factor that should not be neglected
when estimating the ecacy of a parasitoid. To avoid additional damage by increasing H. halys
densities in the fruit orchards, freeze-killed H. halys egg masses had to be used for the experiments.
As a consequence, it was not possible to assess the number of host eggs killed by A. bifasciatus host
feeding in the field. However, data from previous laboratory studies suggest that the number of eggs
killed by host feeding is nearly as high as the number of eggs killed by parasitization, which may
Insects 2019,10, 108 11 of 14
double the estimated host mortality [
36
,
48
]. In addition, parasitoid ecacy might be distinctly higher
in a real infestation situation because using sentinel egg masses may underestimate parasitism [
49
]. If
preimaginal parasitoid mortality (3.3%) and host feeding (6%) are added to the observed parasitism
(6% ospring emergence), the actual induced mortality of H. halys eggs may have been 15.3%.
Higher parasitism of H. halys may be accompanied by higher non-target parasitism since the host
impact values for non-targets (8%) and the target (6%) are similar. These findings agree with studies on
the physiological host range of A. bifasciatus, showing that most non-target species where as frequently
parasitized and suitable for development as the target host [36]. Even though arthropod biodiversity
in apple orchards tends to be higher than in annual crops [
50
,
51
], reviewed by [
52
], insect diversity,
in other words, the number of potential non-targets, was still comparably low at our experimental
sites. Consequently, potential dispersal of released A. bifasciatus into habitats outside the orchards
is a more important factor in its risk assessment [
53
]. In this study, the parasitoid movement could
only be confirmed up to eight meters from the closest release point. Other Anastatus species, however,
can disperse up to 60 meters [
8
,
44
] and, with wind dispersal, up to 100 meters [
44
]. Since parasitism
levels of sentinel eggs were low, the results of the experiment looking at parasitoid movement are not
conclusive and further investigations are needed. As A. bifasciatus has the potential longevity of three
months (97.5 days when provided with honey water) [
36
], released wasps were expected to persist
in the fruit orchards, but their presence was only retained for two weeks in three out of eight release
events which could also be attributed to dispersal. Since releases were conducted in late summer,
nectar sources were hardly available in the orchards, which may have caused a large proportion of
parasitoids to leave the orchards and disperse into other habitats.
5. Conclusions
Field releases of A. bifasciatus can increase parasitism of H. halys eggs in fruit orchards, but
parasitism levels achieved with the current release strategy were not high enough to eectively
suppress the pest. However, the overall impact is likely higher when mortality of parasitoid eggs and
larvae inside host eggs and host egg mortality by host feeding are taken into account. Consequently,
releasing higher densities of parasitoids, and at a larger scale to reduce the impact of dispersal,
should be considered. In addition, naturally laid egg masses should be used in future trials to
include host-finding cues of the host and host plants and avoid potential adverse eects of frozen
sentinel eggs. If those changes result in an increase of overall parasitism under field conditions,
future augmentative releases should be carried out in correspondence with the egg laying peak of
the overwintered generation in May/June to have a greater impact in reducing H. halys populations
along the entire season. Some degree of non-target parasitism after mass releases can be expected,
but whether non-targets would be negatively aected at the population level will require further
investigations, including dispersal studies.
Author Contributions:
Conceptualization, T.H., D.B. and J.M.S.; methodology, T.H., D.B., J.M.S., E.C., S.C. and
L.M.; formal analysis, J.M.S.; investigation, J.M.S., T.H., CM, E.C., S.C. and D.B.; resources, T.H., CM, S.C. and
L.M.; data curation, J.M.S. and E.C.; writing—original draft preparation, J.M.S.; writing—review and editing, T.H.,
D.B. and L.M.; visualization, J.M.S.; supervision, T.H. and D.B.; project administration, J.M.S.; funding acquisition,
T.H., D.B., CM and L.M.
Funding:
This project has received funding from the European Union’s Horizon 2020 research and innovation
programme under the Marie Sklodowska-Curie grant agreement No 641456. Additional funding was provided by
the Phytosanitary Service of the Canton Ticino, and the Associazione frutticoltori ticinesi. For the Italian part,
funding was granted by the Consorzio Fitosanitario Provinciale di Modena.
Acknowledgments:
The authors are grateful to Serge Fischer (Agroscope Changins, Nyon, Switzerland) for
providing the original A. bifasciatus colony. For Switzerland, we would like to thank Warren Wong, Giorgia Frei,
Patrick Mrazek, Taylor Kaye, Chelsey Blackman, Darren Blackburn, Jessica Fraser, Lindsay Craig, Christie Laing,
Anna Grunsky, Mariah Ediger and Giorgia Mattei for technical assistance. For Italy, we thank Giacomo Vaccari,
Luca Casoli (Consorzio Fitosanitario Provinciale di Modena) and Emanuele Di Bella, Giacomo Bulgarini, Marina
Cortiello and Cristiano Carapezzi (UNIMORE) for technical assistance in the field and in the laboratory. We are
grateful to all growers, especially Cesare Bassi, for allowing us to use their orchard for our studies in Switzerland
and Mauro Magnanini for allowing to use his orchard in Italy. We appreciate the taxonomic guidance oered by
Insects 2019,10, 108 12 of 14
Lucian Fusu (University of Iasi, Romania). We gratefully acknowledge the funding provided for this research
by the following organizations and agencies: CABI is an international intergovernmental organization, and we
gratefully acknowledge the core financial support from our member countries (and lead agencies) including
the United Kingdom (Department for International Development), China (Chinese Ministry of Agriculture),
Australia (Australian Centre for International Agricultural Research), Canada (Agriculture and Agri-Food Canada),
Netherlands (Directorate-General for International Cooperation), and Switzerland (Swiss Agency for Development
and Cooperation). See http://www.cabi.org/about-cabi/who- we-work- with/key-donors/for full details.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
publish the results.
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Hoebeke, E.R.; Carter, M.E. Halyomorpha halys (
Insects 2019, 10 FOR PEER REVIEW 12
and Mauro Magnanini for allowing to use his orchard in Italy. We appreciate the taxonomic guidance offered
by Lucian Fusu (University of Iasi, Romania). We gratefully acknowledge the funding provided for this research
by the following organizations and agencies: CABI is an international intergovernmental organization, and we
gratefully acknowledge the core financial support from our member countries (and lead agencies) including the
United Kingdom (Department for International Development), China (Chinese Ministry of Agriculture),
Australia (Australian Centre for International Agricultural Research), Canada (Agriculture and Agri-Food
Canada), Netherlands (Directorate-General for International Cooperation), and Switzerland (Swiss Agency for
Development and Cooperation). See http://www.cabi.org/about-cabi/who-we-work-with/key-donors/ for full
details.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
publish the results.
References
1. Bigler, F.; Wajnberg, E.; Hassan, S.A. Quality control in Trichogramma production. In Biological Control with
Egg Parasitoids; CAB International: Wallingford, UK, 1994.
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... Adventive populations of the Asian egg parasitoids Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) have been recently detected in Europe (the first one in Italy, Switzerland and Germany, the second in Italy, Western Slovenia and France) and these findings have led to reconsider classical biological control methods to manage H. halys (Sabbatini Peverieri et al., 2018;Stahl et al., 2019aStahl et al., , 2019bMoraglio et al., 2020;Scaccini et al., 2020;Zapponi et al., 2020Zapponi et al., , 2021Bout et al., 2021;Dieckhoff et al., 2021;Rot et al., 2021). However, the use of exotic biological control agents is strictly regulated. ...
... Nevertheless, little information is available on its efficacy in field conditions following inundative or inoculative releases. Some studies, although promising, were conducted releasing a low number of parasitoids and using frozen sentinel egg masses as a method to assess parasitization (Stahl et al., 2019b). Another open question is whether the releases of A. bifasciatus can affect parasitoid guilds and in particular the adventive populations of T. japonicus and T. mitsukurii, which have been recently recorded in some Italian regions, including Trentino-Alto Adige (Zapponi et al., 2020) where this study was carried out. ...
... As suggested by Stahl et al. (2019b), measuring parasitism only by offspring emergence could lead to underestimating the real level of pest suppression. Given that the main goal of biological control is the reduction of the pest populations (van Lenteren et al., 2018), we reported the percentage of unhatched eggs (i.e. ...
Article
We report the first large-scale augmentative biological control project carried out in Europe against Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) using the native egg parasitoid Anastatus bifasciatus (Geoffroy) (Hyme- noptera: Eupelmidae). During summer 2020, a total of 325,000 adults of A. bifasciatus were released at a rate of 1000 individuals/ha of orchard in 11 sites in Trentino-Alto Adige (Northern Italy). Parasitism parameters were compared between release and control (no release) sites, in which at least three egg masses naturally laid by H. halys were collected (for a total of 262 egg masses). Anastatus bifasciatus and Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) were the dominant parasitoids, but parasitism by both species fluctuated widely among sites. At release sites, A. bifasciatus showed a significantly higher discovery efficiency (31.4%) and parasitism rate (16.7%) of H. halys egg masses than at control sites (1.7% and 1.2%, respectively). Parasitism by A. bifasciatus was not dependent on egg mass abundance at release sites, but at control sites a host density- dependent response was revealed by a positive relationship between parasitism and number of H. halys egg masses. On the other hand, parasitism by the adventive T. mitsukurii was not affected by either the releases of A. bifasciatus or by the abundance of H. halys egg masses per site. In conclusion, augmentative releases of A. bifasciatus contributed to increasing its parasitization of H. halys, without causing any negative effects on parasitization by naturally occurring species.
... Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) is another egg parasitoid that has been observed exploiting H. halys in Japan with a performance similar to that of T. japonicus (Lee et al., 2013), thus it can be considered as another candidate for biological control programs Sabbatini Peverieri et al., 2020a). Adventive populations of both species were already observed in Europe (Sabbatini Peverieri et al., 2019;Scaccini et al., 2020a;Stahl et al., 2019aStahl et al., , 2019bZapponi et al., 2021;Zapponi et al., 2020), while only T. japonicus has so far been detected in North America (Talamas et al., 2015). Where introduced, both species are currently expanding their geographic distribution Gariepy and Talamas, 2019;Moraglio et al., 2020;Morrison et al., 2018;Rot et al., 2021;Scaccini et al., 2020a;Tillman et al., 2020;Zapponi et al., 2021). ...
... Trissolcus kozlovi Rjachovskij (Hymenoptera: Scelionidae) are two native egg parasitoids that showed some potential for the control of H. halys and have been considered for augmentative biological control strategies (Costi et al., 2019;Haye et al., 2015;Moraglio et al., 2021;Stahl et al., 2019aStahl et al., , 2019bZapponi et al., 2021). ...
... The introduction of exotic biological control agents is currently being studied as a solution for the long-term management of this pest . Nevertheless, adventive populations of the two egg parasitoids T. japonicus and T. mitsukurii are already present in Europe (Moraglio et al., 2020;Sabbatini Peverieri et al., 2018;Scaccini et al., 2020a;Stahl et al., 2019aStahl et al., , 2019bZapponi et al., 2021), but only T. mitsukurii was observed in the orchards surveyed in our study. ...
Article
The invasive alien species Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a major pest of kiwifruit and other fruit crops. Adventive populations of the Asian egg parasitoid Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) were found in the north of Italy in 2016. Halyomorpha halys abundance was monitored in 14 kiwifruit orchards located in north-eastern Italy, and H. halys egg masses were sampled within kiwifruit orchards to assess the impact of egg parasitoids. Both H. halys populations and parasitoid impacts were evaluated considering the influence of ecological structures, and in particular the distance from semi-natural habitats constituted by riparian vegetation buffers and the presence of hedgerows surrounding the orchard. Halyomorpha halys populations fluctuated during the two seasons surveyed, and adults were more abundant during the first year of the study. In addition, more adults were detected in kiwifruit orchards located close to the riparian vegetation and decreased along with the distance from this habitat. Trissolcus mitsukurii had higher parasitism rates on H. halys eggs than the native Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae). No effect of hedgerows was observed on parasitoid impacts in orchards, while a relationship was detected with distance from riparian vegetation: a high T. mitsukurii parasitism rate was observed in kiwifruit orchards close to riparian vegetation buffers. Our findings demonstrate that semi-natural habitats constituted by large patches of unmanaged vegetation promote biological control of H. halys by the introduced egg parasitoids.
... However, so far, the level of parasitism by native species is too low to reduce pest population below economic thresholds [34,39]. Anastatus bifasciatus (Geoffroy) is the most widespread native egg parasitoid in Europe capable of developing on viable H. halys eggs [33,36,[39][40][41] and is considered as the most suitable candidate for augmentative biological control in Europe. The first findings of adventive populations of Tr. japonicus occurred in Switzerland in 2017 and in Northern Italy in 2018 [42,43], where another important H. halys natural enemy, Tr. mitsukurii, was found in Friuli Venezia Giulia, the northeastern Italian region bordering Slovenia, and have brought new prospects for biological control of H. halys in Europe [43,44]. ...
... Furthermore, non-native Trissolcus species, which are known to be effective biocontrol agents of H. halys in its native range, indigenous species can play an important role in pest population reduction in an invaded area. This study supports previous work that suggested An. bifasciatus as a potential biological control agent of H. halys in Europe [33,40,41,65]. ...
... However, the overall impact of A. bifasciatus on the mortality of H. halys found in the study was actually greater. Together with pre-imaginal parasitoid mortality (3.3%) and host feeding (6%), the overall H. halys mortality could reach an average of 15% [41]. ...
Full-text available
Article
Halyomorpha halys (Hemiptera: Pentatomidae), native to East Asia, has become a globally invasive pest, as a serious threat to agricultural production and a notorious nuisance pest in urban areas. Considerable efforts have been made so far to develop effective pest control measures to prevent crop damage. Biological control of this invasive stink bug by egg parasitoids has proven to be the most environmentally sustainable long-term solution. Knowledge of the native egg parasitoid fauna is of key importance when implementing a biological control program. Therefore, the main objective of our study was to detect egg parasitoid species associated with H. halys in the Goriška region (Western Slovenia) and to evaluate their impact on the pest population under field conditions. In the years 2019 and 2020, around 4600 H. halys eggs were collected in the wild and more than 3400 sentinel eggs were exposed to detect parasitoids in the field. Five egg-parasitoid species emerged from H. halys eggs: Anastatus bifasciatus (Hymenoptera: Eupelmidae), Telenomus sp., Trissolcus basalis, Trissolcus mitsukurii (Hymenoptera: Scelionidae) and Ooencyrtus telenomicida (Hymenoptera: Encyrtidae), all of them are new records for Slovenia. The native species, An. bifasciatus, dominated in urban and suburban areas, while non-native Tr. mitsukurii prevailed in agricultural areas. Overall parasitism rates of naturally laid eggs by the parasitoid species complex in 2019 and 2020 was 3.0 and 14.4%, respectively. Rapid recruitment of native parasitoids, early detection of an effective alien parasitoid species and increasing overall parasitism rates are very encouraging results, which need to be followed and verified in future research.
... 25 Furthermore, field releases of Anastatus bifasciatus in apple and pear orchards in Switzerland and Italy, respectively, did not achieve promising results, causing only 2-16% parasitism of sentinel Halyomorpha halys eggs. 26 Anastatus japonicus is widely distributed throughout the entire Palaearctic region, attacking over 15 host insects in the Hemiptera and Lepidoptera. 19 The parasitoid, misidentified previously as Anastatus bifasciatus, is also present in Canada and the United States (Nearctic region). ...
... The developmental time of Anastatus japonicus from egg to adult was 27.5 days on average at 25°C, which was about 5 days longer than for either Anastatus japonicus and Anastatus bifasciatus when reared on Halyomorpha halys eggs at the same temperature and over 6 days longer than Anastatus japonicus in Riptortus pedestris (Fabricius) (Hemiptera: Alydidae). 26,30,38 This increase in developmental time might be due to the larger size of Antheraea pernyi eggs, which allows the parasitoid larva to feed longer than that in smaller eggs, such as those of Halyomorpha halys or R. pedestris. ...
Full-text available
Article
Background: Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae) is a solitary egg endoparasitoid that has been studied for inundative biological control of Halyomorpha halys Stål (Hemiptera: Pentatomidae) in China. In this study, we assessed the reproductive attributes and functional response of A. japonicus on a factitious host, Antheraea pernyi (Guérin-Méneville) (Lepidoptera: Anthelidae) at 25 ± 1 °C, 70 ± 5% RH and 16L:8D photoperiod. Results: The mean lifetime fecundity of A. japonicus females was 404.3 progeny produced over an average oviposition period of 42.3 days. The sex ratio of adult progeny was slightly male biased (51.2%), whereas more female progeny were produced before day 20 of a female's life. Single 1-day-old mated A. japonicus females exhibited a type II functional response to increasing host densities (1-50 eggs), with an inverse host density-dependent pattern of percent parasitism. The upper limit to the daily attack rate was estimated as 7.6 A. pernyi eggs. Furthermore, mutual interference among A. japonicus females occurred when increasing densities of parasitoids (1, 2, 4, 8, 16) were exposed to 30 host eggs. Conclusion: Laboratory functional response result revealed that individual A. japonicus might be unable to respond effectively to increasing host density in the field, which could be compensated by releasing larger numbers of wasps. Strong mutual interference among foraging A. japonicus females should be considered in any future inundative biological control programme for the sustainable management of H. halys or other host insect pests. This article is protected by copyright. All rights reserved.
... Its ability to develop on previously parasitized H. halys eggs demonstrates its potential negative influence on the success of biological control program against the brown marmorated stink bug [30,31]. In Europe, native egg parasitoids such as A. bifasciatus cannot provide satisfactory control of H. halys, even following augmentation programs [15,17,42]. The two Asian parasitoids, T. mitsukurii and T. japonicus, show higher performances and Figure 7. Polynomial regression (y = 0.0001x 5 − 0.0077x 4 + 0.1583x 3 − 1.5044x 2 + 6.7273x − 0.1388) of mature egg development in ovaries of Acroclisoides sinicus dissected females at different periods after the emergence from the host. ...
... Its ability to develop on previously parasitized H. halys eggs demonstrates its potential negative influence on the success of biological control program against the brown marmorated stink bug [30,31]. In Europe, native egg parasitoids such as A. bifasciatus cannot provide satisfactory control of H. halys, even following augmentation programs [15,17,42]. The two Asian parasitoids, T. mitsukurii and T. japonicus, show higher performances and are currently considered for biological control programs that promise to provide higher control of H. halys [12,14,32]. ...
Full-text available
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Halyomorpha halys (Stål) is an invasive Asian pest that causes severe crop losses on various crops. Nowadays, management strategies against this pest mainly rely on pesticide use, but biological control with egg parasitoids is considered the most promising long-term and sustainable solution. Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) are Asian egg parasitoids already present in Europe and are the most effective biological control agents of H. halys. Therefore, these two species are considered for biological control programs in Europe and other parts of the world. Acroclisoides sinicus (Huang and Liao) is a pteromalid parasitoid wasp that frequently emerged from H. halys egg masses collected in northern Italy. This species has been hypothesized to be a hyperparasitoid of Trissolcus spp. parasitoids. This study was carried out under laboratory conditions where A. sinicus was tested in no-choice and two-choice experiments to assess the host preference between T. japonicus and T. mitsukurii. Olfactory responses of A. sinicus from volatiles emitted from different potential hosts were also tested. In all trials, A. sinicus showed a clear preference for parasitizing H. halys eggs previously parasitized by T. mitsukurii compared to T. japonicus. In no-choice experiments, the impact of the hyperparasitoid on T. japonicus was low, showing an exploitation rate of 4.0%, while up to a 96.2% exploitation rate was observed on T. mitsukurii. Acroclisoides sinicus was also attracted by volatiles emitted by egg masses parasitized by T. mitsukurii, while no response was observed to egg masses parasitized by T. japonicus or not parasitized. Therefore, according to the results obtained here, A. sinicus could limit the population development of T. mitsukurii, while lesser effects are expected on T. japonicus.
... 1,2 Among them, some are important biological control agents for lepidopterous and hemipterous pests and have the potential to be used in augmentative biological control programs against fruit tree pests. [3][4][5][6] For example, several Anastatus parasitoids have been evaluated for biological control of some invasive agricultural and forestry pests, such as Anastatus bifasciatus (Geoffroy) for the brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Europe, 7,8 Anastatus disparis Ruschka (= Anastatus japonicus Ashmead) for the gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae) in the USA, 9 and, mostly recently, Anastatus orientalis Yang and Choi for the spotted lanternfly, Lycorma delicatula White (Hemiptera: Fulgoridae) in the USA. 10,11 A notable example is Anastatus fulloi Sheng & Wang, which has been used for successful control of the litchi stink bug, Tessaratoma papillosa Stål (Hemiptera: Tessaratomidae) in China since the late 1960s. ...
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BACKGROUND Eupelmid egg parasitoids in the genera Anastatus and Mesocomys are important biological control agents for lepidopterous and hemipterous pests worldwide. The egg of Chinese oak silkworm Antheraea pernyi has been widely used for mass rearing of Trichogramma parasitoids. This study evaluated the suitability and optimal use methods of A. pernyi egg as a factitious host for the rearing of six eupelmid egg parasitoids (A. fulloi, A. gansuensis, A. japonicus, A. meilingensis, M. albitarsis and M. trabalae). Each parasitoid was tested for its oviposition preference and offspring performance on various differently treated host eggs (extracted from virgin moths or laid naturally by virgin or mated moths, and washed or unwashed prior to the use) in both no-choice and choice tests. RESULTS All treated A. pernyi eggs were readily parasitized by the six parasitoids. In general, A. gansuensis and M. trabalae preferred washed over unwashed eggs regardless of the fertilization status of host eggs; A. fulloi and A. meilingensis parasitized more unfertilized than fertilized host eggs; and A. japonicus and M. albitarsis did not show a preference among differently treated host eggs. Host egg treatment did not significantly affect offspring fitness (development time, survival, sex ratio and body size) nor reproductive potential of developed adult females for each parasitoid species, except for M. albitarsis (whose females contained more eggs when reared from unfertilized than fertilized host eggs). CONCLUSION Results suggest that manually extracted, unfertilized and washed A. pernyi eggs are most suitable for mass rearing of these eupelmid egg parasitoids in biological control programs.
... In Europe, the generalist egg parasitoid A. bifasciatus has been reported on, with more than thirty-five hosts in the orders of Hemiptera, Lepidoptera, and Orthoptera [35,36]. It is among the most widespread native egg parasitoids of H. halys, and due to its ability to develop successfully on viable H. halys eggs, it can be considered a potential candidate for biological control [7,23,27,31,32,37,38]. Furthermore, Anastatus sp. is also part of the natural parasitoid community of H. halys in its native range in China [19]. ...
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Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an endemic species of East Asia; it was introduced into Europe in 2007. It has a wide range of hosts as it feeds on over 170 host plant species and significantly impacts crop production. In Greece, H. halys causes significant losses in the production of kiwi, peaches, and green beans; thus, control of this species (including biological control) is essential. Here, we focus on the potential impact of native natural enemies of H. halys in Greece. From June to October 2020, we sampled naturally field-laid H. halys egg masses to recover native parasitoids. A total of 20 egg masses of H. halys were collected from infested fields from different locations in northern Greece. Out of 529 eggs, 45 parasitoids managed to hatch successfully. The overall parasitism rate was 8.5%. We found two species of Hymenopteran egg parasitoids attacking H. halys eggs—Anastatus bifasciatus (Geoffrey) (Hymenoptera: Eupelmidae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), with the former comprising 58% of all parasitoids that were recovered. These results contribute to the knowledge about the natural enemy community that attacks H. halys in Greece, and the use of these native egg parasitoids in biological control programs may be a viable H. halys management strategy.
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The brown marmorated stink bug Halyomorpha halys is a polyphagous insect, which has a devastating impact on agricultural production in many countries. The alteration of symbiont vertical transmission, by removing symbionts from stink bug eggs (symbiotic control), has been recently introduced in control programmes against this insect. A major advantage of this strategy is the compatibility with natural enemies, since it allows an insecticide-free approach that is not harmful to other agroecosystem components. However, the effect of anti-symbiont products on parasitism by egg parasitoids is still unexplored. Here, we investigated the impact on parasitism by native (Anastatus bifasciatus, Ooencyrtus telenomicida and Trissolcus kozlovi) and exotic (Trissolcus japonicus and Trissolcus mitsukurii) parasitoids that attack H. halys eggs, after treatment with the micronutrient biocomplex Dentamet®, used for symbiotic control. The native wasp species were tested in no-choice bioassays, showing that treatment of the egg masses did not affect emergence percentages, but the non-reproductive effects were often reduced by the biocomplex. The exotic species T. japonicus and T. mitsukurii were used in no-choice and paired choice bioassays, showing an opposite influence of Dentamet® on emergence percentage and preference in the two species. No-choice tests indicated the highest successful parasitoid emergence on biocomplex-treated egg masses for T. japonicus, while no preference in the paired comparison with eggs treated with water or untreated. In contrast, T. mitsukurii displayed the lowest parasitism after Dentamet® treatment in no-choice tests, and preferred egg masses without Dentamet® in paired choice tests. We did not record any natural symbiont acquisition by the parasitoids emerged from H. halys egg masses, indicating that the wasp fitness is very unlikely to be altered by dysbiotic effects resulting from treatments. Therefore, our results support a further implementation of symbiotic control in different crops in combination with biological control, as sustainable options for H. halys integrated pest management.
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Japanese giant silkworm (JGS), Caligula japonica Moore, is an emerging defoliator pest of forest and fruit trees in East Asia, causing severe economic losses. To develop a cost-effective biological control program against JGS, we used eggs of the Chinese oak silkworm (COS) Antheraea pernyi Guérin-Méneville as an alternative host to rear the most dominant JGS egg parasitoid Anastatus japonicus Ashmead. We compared the demographic parameters and total parasitism (killing) rates of A. japonicus parasitizing JGS and COS eggs using an age-stage, two-sex life table method. The results showed that A. japonicus performed differently on these two different hosts. Anastatus japonicus reared from COS eggs had a higher fecundity (369.7 eggs per female) and a longer oviposition period (35.9 days) on the COS than JGS eggs (180.9 eggs; 24.0 days). Consequently, A. japonicus parasitizing COS eggs had a higher intrinsic rate of increase (r = 0.1466 d−1), finite rate of increase (λ = 1.1579 d−1) and net reproductive rate (R0 = 284.9 offspring) than those parasitizing JGS eggs (r = 0.1419 d−1, λ = 1.1525 d−1, R0 = 150.0 offspring). The total net parasitism rate (the number of parasitized hosts in which the parasitoids successfully developed) of A. japonicus parasitizing COS eggs was 284.9, significantly higher than that of A. japonicus parasitizing JGS eggs (150.0), while the net non-effective parasitism rate (the number of parasitized hosts in which the parasitoids failed to develop) of the former (0.0) was significantly lower than that of the latter (9.6). These results suggest that A. japonicus can be efficiently reared on the alternative (or factitious) COS eggs, and the reared parasitoids have a high biological control potential against the target JGS.
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The invasive Halyomorpha halys (Heteroptera: Pentatomidae) is a key pest of fruits in the Emilia‐Romagna region of Italy. For the development of a sustainable management programme, knowledge of its native natural enemy community and its efficacy is essential. A three‐year field survey was conducted exposing H. halys egg masses in different types of habitats to investigate the efficacy of native natural enemies in reducing the H. halys populations in the Emilia‐Romagna region, where the stinkbug was first detected in 2012. Over the first year of the study, sentinel eggs from laboratory cultures were stapled to the underside of leaves in various host trees, whereas in following years H. halys adults were directly caged on branches in sleeve cages to allow natural oviposition. Over the examined years, low rates of parasitism (1%–3%) and predation (2%–5%) were observed. Parasitism was caused exclusively by the generalist parasitoid Anastatus bifasciatus.
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Anastatus bifasciatus (Geoffroy) is the most widespread native egg parasitoid of the invasive agricultural pest Halyomorpha halys (Stål) in Europe and considered as promising candidate for augmentative biological control. In this context, the parasitoid’s reproductive parameters, longevity, phenology, and temperature requirements for development were studied. In addition, the potential of using stored frozen H. halys eggs for mass production was investigated. In northwestern Switzerland, A. bifasciatus was able to complete three overlapping generations between June and October, which covers the entire oviposition period of its host. After an average pre-oviposition period of 11.9 days the mean potential lifetime fecundity of A. bifasciatus females was 52 eggs over an average oviposition period of 46 days. The number of H. halys eggs killed by either oviposition or host feeding was nearly the same. Females provided only with honey water lived on average 97.5 days. Development from egg to adult was possible from 15°C to 32°C, the lowest developmental time (15.9 days) being at 30°C. Halyomorpha halys eggs of all ages yielded parasitoid offspring, but offspring emergence decreased with increasing age. Eggs stored up to 24 months at -80°C were still suitable for parasitoid development. The wealth of information obtained on the life history of A. bifasciatus should be highly relevant to develop a release strategy of this parasitoid against its host, H. halys.
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The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), has been causing massive damage to various fruit and vegetable crops after its arrival in the USA, and more recently in Europe. To provide an alternative control measure to pesticides, the native egg parasitoid Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) was considered as a candidate biological control agent for inundative releases in Europe. In the risk assessment study presented here, all nine heteropteran and 14 out of 19 tested lepidopteran non-target species produced viable A. bifasciatus offspring. The proportion of A. bifasciatus females producing offspring did not differ between non-target and target for 19 out of the 28 non-target species. Larger host eggs corresponded to increased female-biased sex ratio of the offspring as well as an increase in size, particularly for females, with hind tibia lengths varying from 645.5 ± 46 to 1084 ± 28.5 μm. Larger females were also found to have higher offspring production and increased life expectancy. The results of this study confirmed the polyphagous nature of A. bifasciatus and suggest that a number of non-target species, including Lepidoptera of conservation interest, may be attacked in the field. Thus, non-target effects cannot entirely be ruled out, but more information is needed from semi-field and field studies to fully assess potential environmental risks due to inundative releases of this native parasitoid.
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The brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), is an invasive pentatomid introduced from Asia into the United States, Canada, multiple European countries, and Chile. In 2010, BMSB populations in the mid-Atlantic United States reached outbreak levels and subsequent feeding severely damaged tree fruit as well as other crops. Significant nuisance issues from adults overwintering inside homes were common. BMSB is a highly polyphagous species with a strong dispersal capacity and high reproductive output, potentially enabling its spread and success in invaded regions. A greater understanding of BMSB biology and ecology and its natural enemies, the identification of the male-produced aggregation pheromone, and the recognition that BMSB disperses into crops from adjacent wooded habitats have led to the development of behavior-based integrated pest management (IPM) tactics. Much is still unknown about BMSB, and continued long-term collaborative studies are necessary to refine crop-specific IPM programs and enhance biological control across invaded landscapes. Expected final online publication date for the Annual Review of Entomology Volume 63 is January 7, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Following its first detection, Halyomorpha halys has become a key pest in many crops in NW Italy. In this area, one of the most important crops is hazelnut, in which the species can cause severe damage through feeding on nuts. Therefore, semi-field trials were carried out in NW Italy to compare the harmfulness of H. halys with that of the local hazelnut bug species, such as Gonocerus acuteangulatus, Nezara viridula, and Palomena prasina. Additionally, a 2-year field survey was conducted in hazel groves in NW Italy and W Georgia, another important hazelnut cropping area, to assess the presence and abundance of the new invasive species and to evaluate the damage at harvest. Monitoring was carried out by plant beating and by commercial traps throughout the growing season. In semi-field trials, H. halys was the most harmful species, causing the highest damage in kernels, and was able to survive and reproduce at higher rates. During field surveys in NW Italy, H. halys was sampled in groves late in the season in 2015 and, with higher populations, throughout the season in 2016. In W Georgia, bug population levels consistently increased in the 2-year period, resulting in a significant increase in damage at harvest in 2016. A similar trend is hence expected also in NW Italy in the following years. Moreover, data on individuals collected in different points of the hazelnut groves confirmed the border-driven behavior of this pest, leading to consideration of potential integrated pest management solutions.
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Halyomorpha halys is an invasive polyphagous pest with a high negative impact on fruit orchards and other agricultural crops in the USA. In Italy, it was first detected in 2012 in Emilia Romagna, a northern region that is among the major European tree fruit production areas. A specific monitoring programme using active techniques was carried out in pear orchards and adjacent uncultivated areas between 2014 and 2016 to assess the abundance, seasonality and impact of H. halys and other phytophagous Heteroptera in the field. It emerged that just a few years after first discovery, this invasive species already largely outnumbers all the other Heteroptera and that it is a season-long pest for pear crops. Severe yield losses are reported in different farms, especially on the orchard borders, with more than 50% deformed fruits. Mirids are mostly found in the grassy areas and crops, and the other phytophagous Heteroptera, only occasionally detected in the orchard trees, occur mainly on hedges and other crops. Our survey demonstrates for the first time the great damaging potential of H. halys as a new key pest of orchards in southern Europe. The study also identified the patterns of seasonal abundance of adults and nymphs in the orchards and their uncultivated surroundings, providing baseline data for the development of specific strategies for sustainable management.
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Abstract Since the establishment of the brown marmorated stink bug, Halyomorpha halys (Sta°l) (Hemiptera: Pentatomidae) in North America and Europe, there has been a large, multi-group effort to characterize the composition and impact of the indigenous community of arthropod natural enemies attacking this invasive pest. In this review, we combine 98 indigenous natural enemy datasets spanning a variety of sampling methods, habitats, and geographic areas. To date, the vast majority of H. halys biological control research has focused on the egg stage, using sentinel egg masses to characterize indigenous parasitoid and predator communities and their contribution to H. halys egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are low (typically\10% each) in most surveys, total egg mortality attributable to natural enemies can be higher (typically between 5 and 25%; up to 83%)—even though these values were likely underestimated in most cases because some mortality due to biological control was not recognized. In North America, where the most data are available, it appears that the relative prevalence of different indigenous parasitoid species varies among habitat types, particularly between crop and non-crop habitats. Predator species responsible for egg mortality are much less commonly identified, but appear to include a wide variety of generalist chewing and sucking predators. To date, studies of natural enemies attacking H. halys nymphs and adults are relatively rare. Based on our review, we identify a number of key research gaps and suggest several directions for future research.
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Globally, Anastatus species (Hymenoptera: Eupelmidae) are associated with the invasive agricultural pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). In Europe, the polyphagous Anastatus bifasciatus (Geoffroy) is the most prevalent native egg parasitoid on H. halys eggs and is currently being tested as a candidate for augmentative biological control. Anastatus bifasciatus frequently displays behavior without oviposition, and induces additional host mortality through oviposition damage and host feeding that is not measured with offspring emergence. This exacerbates accurate assessment of parasitism and host impact, which is crucial for efficacy evaluation as well as for pre‐ and post‐release risk assessment. To address this, a general Anastatus primer set amplifying a 318‐bp fragment within the barcoding region of the cytochrome oxidase I (COI) gene was developed. When challenged with DNA of three Anastatus species —A. bifasciatus, Anastatus japonicus Ashmead, and Anastatus sp.—, five scelionid parasitoid species that might be encountered in the same host environments and 11 pentatomid host species, only Anastatus DNA was successfully amplified. When applied to eggs of the target host, H. halys, and an exemplary non‐target host, Dendrolimus pini L. (Lepidoptera: Lasiocampidae), subjected to host feeding, no Anastatus amplicons were produced. Eggs of the two host species containing A. bifasciatus parasitoid stages, from 1‐h‐old eggs to pupae, and emerged eggs yielded Anastatus fragments. Confirmation of parasitoid presence with dissections and subsequent PCRs with the developed primer pair resulted in 95% success for 1‐h‐old parasitoid eggs. For both host species, field‐exposed sentinel emerged eggs stored dry for 6 months, 100% of the specimens produced Anastatus amplicons. This DNA‐based screening method can be used in combination with conventional methods to better interpret host‐parasitoid and parasitoid‐parasitoid interactions. It will help address ecological questions related to an environmentally friendly approach for the control of H. halys in invaded areas.
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Biological control agents may play an important role in regulating Drosophila suzukii Matsumura (Diptera: Drosophilidae), particularly after the winter population bottleneck. Here we test the ability of the cosmopolitan pupal parasitoid, Trichopria drosophilae (Perkins) (Hymenoptera: Diapriidae), to reduce early season D. suzukii populations. We performed augmentative releases of the parasitoid during late March–April and carried out extensive monitoring activity on both parasitoid and fly populations. Results clearly showed a mitigation of the D. suzukii population in the treated areas, associated with a higher T. drosophilae parasitism. A 34% reduction in fruit infestation was observed in the unmanaged vegetation surrounding orchards. Accordingly, pest eclosion was significantly lower in the treated area compared to the untreated one. Our results suggest that augmentative release of T. drosophilae can improve pest control of D. suzukii in the unmanaged areas surrounding the crops, thus lowering the severity of pest outbreaks in the orchards.