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The effect of flower morphology on the longevity of Diadegma semiclausum

(Hymenoptera: Ichneumonidae)

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DOI: 10.1088/1755-1315/694/1/012049

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The effect of flower morphology on the longevity of Diadegma

semiclausum (Hymenoptera: Ichneumonidae)
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International e-Conference on Sustainable Agriculture and Farming System IOP Publishing
IOP Conf. Series: Earth and Environmental Science 694 (2021) 012049 doi:10.1088/1755-1315/694/1/012049

The effect of flower morphology on the longevity of Diadegma

semiclausum (Hymenoptera: Ichneumonidae)

P P Asmoro1*, Dadang2, Pudjianto2 and I W Winasa2

1
Graduate Student of Department of Plant Protection, Faculty of Agriculture, IPB
University. Jl. Kamper, Kampus IPB Darmaga, Wing 7 Level 5, Bogor 16680,
Indonesia
2
Department of Plant Protection, Faculty of Agriculture, IPB University. Jl. Kamper,
Kampus IPB Darmaga, Wing 7 Level 5, Bogor 16680, Indonesia

*Email: prayogoasmoro@apps.ipb.ac.id

Abstract. Refugia plants can support the biological control of plant pests by
increasing the presence and fitness of parasitoids. One of the factors that determine the
suitability of refugia plants with parasitoids is the flower morphology. This study
used Diadegma semiclausum, a parasitoid of cabbage pest, Plutella xylostella. This
study aimed to determine the effect of refugia plants' flower morphology on the
longevity of D. semiclausum adults. Refugia plants used were Rorippa
indica, Brassica rapa, Ageratum conyzoides, and Sphagneticola trilobata. Research
methods consist of insect rearing and plant preparation, testing refugia flowers'
influence on parasitoid longevity, and measuring flower morphology (corolla length
and aperture, and nectar location). The results showed all refugia flower treatments
could increase the parasitoid longevity compared to control (1.71-3.69 times). The
best effect was demonstrate by the R. indica treatment, followed by B. rapa, A.
conyzoides, and S. trilobata. Correlation and regression analysis showed that the
increasing corolla aperture and length positively affected parasitoid longevity. Flowers
with exposed nectar positions (R. indica and B. rapa) makes the parasitoid easy to
access, even though the corolla flowers were longer than A. conyzoides and S.
trilobata.

1. Introduction
Biological control has been widely developing as pest control that is environmentally friendly and has
a low negative impact. One example of the application of biological controls is controlling the
diamondback moth Plutella xylostella L. (Lepidoptera: Yponomeutidae) using the
parasitoid Diadegma semiclausum Hellen (Hymenoptera: Ichneumonidae). The parasitization rate of
D. semiclausum against P. xylostella was relatively high, ranging from 70% -94% [1]. However,
several studies have shown that the parasitization rate of D. semiclausum fluctuates and tends to be
low under certain conditions [2][3]. The intensive use of insecticides, monoculture cultivation, and
insufficient understanding to conserve natural enemies caused the decrease of biological control
effectivity.
Modifying habitat or ecosystem can improve the continuity of biological control. Habitat
engineering can be done by planting refugia plants around cultivated plants. Refugia plants can act as
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International e-Conference on Sustainable Agriculture and Farming System IOP Publishing
IOP Conf. Series: Earth and Environmental Science 694 (2021) 012049 doi:10.1088/1755-1315/694/1/012049

a source of nutrition for natural enemies. The existence of refugia plants has a positive effect on
natural enemies of pests [5]. The presence of flowering plants can have a positive effect on natural
enemies [6][7][8][9]. Centaurea cyanus (Asteraceae) could attract and provide nectar for the
Microplitis mediator (Hymenoptera: Braconidae). On the other hand, the flower can increase the
parasitism rate of the cabbage moth Mamestra brassicae (Lepidoptera: Noctuidae) [10].
The increased level of parasitization of Cotesia rubecula, Diaeretiella rapae, and Copidosoma
koehleri is closely related to the presence of nectar-producing plants [11][12][13]. Several types of
spiders are also known to consume nectar [14]. Pollen, nectar, and extrafloral nectar of flowers can
increase longevity, reproductive capacity, predators, and parasitoid ability to control insect pests. The
availability of nectar also increased the average reproductive life of the parasitoid Diadegma
semiclausum from 1.2 days (control) to 28 days [15].
The longevity of the parasitoid Copidosoma aretas Walker (Hymenoptera: Encyrtidae) was 1.4
times longer in Fagopyrum esculentum Moench (Polygonaceae) plants compared to controls. The
average length of life for D. semiclausum fed on F. esculentum was 30.3 days (male) and 25.6
(female) compared to water [6]. The longevity of the Diaeretiell rapae McIntosh (Hymenoptera:
Braconidae) could increase 3.4 times with feed sources Leptospermum sp., D. semiclausum increased
4.3 times with Myoporum parvifolium as feed sources, and Cotesia glomerata (Hymenoptera:
Braconidae) increased by 6.9 times with a feed source of Grevillea sp. [16].
Exploring and selecting refugia plants is the earliest stage determining pest control's success
[17][18]. Refugia plants used for habitat engineering need to be chosen to maximize their role as a
source of nutrition for natural enemies. The successful use of nectar sources by parasitoids depends on
several factors such as moth part morphology, flower morphology, and flower color [19][20][21][22].
Apart from the nectar's nutritional content, the accessibility of the parasitoids in the nectar is also
essential. The accessibility of parasitoids in nectar is closely related to flower morphology. Flowers
with exposed nectar will be more accessible to parasitoids. This flower will undoubtedly support the
parasitoids' continuity so that the pest population will be more viable.
Therefore, this study aims to determine the refugia plant longevity of D. semiclausum and changes
in the direction of refugia flower morphology. This study's results can be used to consider suitable
refugia plant species to manipulate the cabbage planting habitat, especially for D. semiclausum adult’s
survival.

2. Methods

2.1 Diadegma semiclausum rearing

The insects were taken from the cabbage plantations at the Research Station of the Faculty of
Agriculture IPB Pasir Sarongge, Pacet District, Cianjur Regency. The P. xylostella pupae taken were
pupae thought to have been parasitized by D. semiclausum. Pupae were obtained from the field and
placed in a gauze-framed iron cage (60 cm x 30 cm x 30 cm), then left for several days until the D.
semiclausum imago appeared. After the male and female D. semiclausum imago appeared, a plastic
container was inserted inside, which had P. xylostella instar II and III. D. semiclausum adults then
allowed to parasitize P. xylostella larvae. Larvae that have been parasitized and become pupae are
transferred to another cage and allowed to become a D. semiclausum adult.

2.2. Propagation of refugia plants

The refugia plants used have several criteria, including 1) can grow well in the same environment as
the cabbage plant, 2) plant height is about 10-40 cm (as tall as a cabbage plant) or not more than 80
cm, 3) Easy to grow or breed, 4) does not compete with the main crop. This study's refugia plants
consisted of four types of plants obtained from transplanting directly from the land or grown from
seeds. The four refugia plants were Rorippa indica (Brassicaceae), Brassica
rapa (Brassicaceae), Ageratum conyzoides (Asteraceae), and Sphagneticola trilobata (Asteraceae).

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International e-Conference on Sustainable Agriculture and Farming System IOP Publishing
IOP Conf. Series: Earth and Environmental Science 694 (2021) 012049 doi:10.1088/1755-1315/694/1/012049

Refugia plants are grown or transplanted into a planting medium with the soil's composition: compost
(1: 1). Plant maintenance was carried out by sufficient watering.

2.3. The effect of refugia plants on the longevity of D. semiclausum

The experiment was carried out on a gauze cage (60 cm x 30 cm x 30 cm). One flowered refugia plant
was placed into the cage. Then, a pair of 24 hours old D. semiclausum adults were put into the cage.
Observations were done every day until all adults died, and refugia plants were replaced every other
day. The positive control treatment used a 10% honey solution, while the negative control used water.
Each treatment was conducted as many as ten replications.

2.4. Relationship between refugia flower structure with D. semiclausum longevity

The corolla length and aperture width for a sample of 10 flowers (selected randomly) for each species
replicate were measured and used to relate it with the longevity of D. semiclausum (from the above
study).

2.5. Data analysis

The design used in this study was a completely randomized design (CRD). The treatment and
replication were adjusted for each type of test. Data analysis used Minitab software version 17 to
know each treatment's effect; a further test was carried out using the Tukey test (α=5%).

3. Results and discussion

The results showed that all refugia flower treatments showed higher longevity than the negative
control, but three flower treatments showed a better effect than the positive control. The treatment
of R. indica showed the best effect on the D. semiclausum adult's longevity, both male and female,
16.6 days and 14.8 days, respectively (Table 3). The effect of refugia flowers can be seen from the
survival probability of male and female adults. The survival probability of imago on R. indica
treatment showed the highest level compared to other flower treatments and control (Figure 1).

Table 1. The longevity of D. semiclausum adult in the flower of refugia plants

Longevity average (days)
Plant species
Female Male
Positive control (honey solution 10%) 10.2 ± 1.69 c 9.1 ± 1.66 cb
Negative control (aquades) 3.6 ± 1.26 d 3.4 ± 0.96 db
R. indica 16.6 ± 1.17 a 15.8 ± 2.39 ab
S. trilobata 9.8 ± 1.69 c 9.2 ± 1.99 cb
A. conyzoides 12.2 ± 1.40 b 12.0 ± 1.70 bb
B. rapa 14.1 ± 1.73 b 13.6 ± 1.51 ab
The numbers in the same column, followed by the same letters, show that they are not significantly different
based on Tukey's test at the level of α = 5%.

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International e-Conference on Sustainable Agriculture and Farming System IOP Publishing
IOP Conf. Series: Earth and Environmental Science 694 (2021) 012049 doi:10.1088/1755-1315/694/1/012049

1.0 A B
Survival probability of D. semiclausum adults

0.9
0.8
0.7
K+
0.6 K-
0.5 Rid
Str
0.4 Aco
0.3 Brp

0.2
0.1
0.0
0 2 4 6 8 10 12 14 16 18 20 22 0 2 4 6 8 10 12 14 16 18 20 22

Longevity (days) Longevity (days)

Figure 1. Survival probability of D. semiclausum adults. (A) Female, (B) Male. K+: positive
control, K-: negative control, Rid: R. indica, Str: S. trilobata, Aco: A. conyzoides, Brp: B. rapa.

Nectar in refugia flowers generally has a positive effect on D. semiclausum longevity. Refugia
flower nectar can increase D. semiclausum adults' longevity to 1.7 - 3.7 times compared to the
negative control (water treatment). Several flowers affected increasing the imago's longevity, which
was not significantly different from the positive control treatment (10% honey solution). Flower nectar
and other carbohydrate sources can increase life and parasitoid meridians length in laboratory and
field-scale tests [23][24]. The presence of flower nectar is vital as a source of nutrition that determines
parasitoid survival. Parasitoids generally emerge first from their host with limited energy availability,
so they can only last 1-2 days without food [25][26]. Research by Winkler et al. [27] also stated that
the adult of D. semiclausum could only survive less than two days without eating. This causes, after
leaving the host, the parasitoid will start searching for food sources first rather than searching for the
host [28][29]. The parasitoids D. semiclausum is synovigenic parasitoids [30]. This parasitoid must
continuously ripen eggs during their reproductive period so that the presence of nectar as a nutrition
source will benefit from increasing fecundity and reproductive rate of eggs and increasing longevity
[31][32].
The R. indica flower had the best effect on the D. semiclausum adults' longevity, followed by the
treatment of B. rapa and A. conyzoides flowers. Brassicaceae family plants, such as R. indica and B.
rapa, have been reported to have had a fairly good effect on Diadegma adults' longevity. The nectar of
kale flowers as a source of carbohydrates can increase the survival of Diadegma insulare imago (4-28
days) and not different with 15% honey treatment (27-28 days), while water treatment is only 0-1 days
[33]. The results of Johanowicz and Mitchell's [34] study showed that the survival of D. insulare was
supported by Lobularia maritima (L.) Desc (1-53 days) compared to water treatment (1-4
days). Barbarea vulgaris, Brassica kaber, and Dacus carota, common in cabbage planting areas, can
affect D. insulare. Barabarea vulgaris can increase the longevity up to more than 20 days, not
significantly different from the honey solution treatment, while water treatment is only about two days
[24]. Longevity average of D. semiclausum adults feeding on the Fagopyrum esculentum Moench cv.
Katowase flowers are 15 / 14.2 (male / female) times higher (30.3 / 25.6 days), compared to water
treatment (2 / 1.8 days), flower treatment was not significantly different from honey [35].

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International e-Conference on Sustainable Agriculture and Farming System IOP Publishing
IOP Conf. Series: Earth and Environmental Science 694 (2021) 012049 doi:10.1088/1755-1315/694/1/012049

12
Corolla length
Corolla aperture
10
Flower measurments (mm)

0
R. indica B. rapa A. conyzoides S. trilobata
Refugia flower

Figure 2. The size of refugia corolla length and aperture

The B. rapa corolla flower length is most extended compare to other flowers, followed by R.
indica, S. trilobata, and A. conyzoides (Figure 2). Likewise, the corolla flower aperture, the widest
aperture, was shown by B. rapa flower, and the narrowest was shown by A. conyzoides flower. The
regression analysis results between the D. semiclausum longevity and the flower's morphological
character showed that the length and aperture of refugia flowers are positively related to the length
of D. semiclausum longevity (Figure 3).
The result indicates that the longer and wider (aperture) of flower corolla causes an increase in
parasitoids' longevity. This result differs from the initial assumption, which stated that a shorter flower
corolla would make it easier for parasitoids to exploit flower nectar, thus increasing the longevity.
According to Idris and Grafius [24] research, the longevity of D. insulare has a significant positive
correlation with corolla opening and length, even though a negative correlation was expected with
corolla length if a narrow corolla limited access to nectar by D. insulare
Nectar is generally found in the basal part of petal flowers [36]. The flowers of R. indica and B.
rapa, which are plants in the Brassicaceae family, have flower characters with separate petals and
sepals. These characters causing the flower openings to be quite broad, so even though they have a
corolla (flower crown) that is longer than the mouth part of the parasitoid, the nectar can still be
accessed easily.
Meanwhile, the mouth part of D. semiclausum is shorter and relatively unspecialized so that it is
less able to access the nectar of S. trilobata or A. conyzoides. Most of the suborder Apocrita
parasitoids (order Hymenoptera) have a short mouth part [37][38]. Most parasitoids are less abundant
in flowers where the nectar is completely hidden or not exposed [39]. Winkler et al. [40] stated
that Cotesia glomerata and D. semiclausum do not have an elongated mouthpart, which is an
important morphological limiting factor for accessing flower nectar is head width. The mean head
width of D. semiclausum was 0.77 ± 0.01 mm. Insect access to flower nectar is closely related to

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 International e-Conference on Sustainable Agriculture and Farming System IOP Publishing
IOP Conf. Series: Earth and Environmental Science 694 (2021) 012049 doi:10.1088/1755-1315/694/1/012049

flower shape or morphology. Flower petals and sepal's position can influence nectar access. As
reported on Brassica kaber flowers by Idris and Grafius [24], B. rapa and R. indica flowers have
separate petals and sepals, causing the nectar found in the basal part of the flower to be exposed. This
character causes the nectar of B. rapa to remain accessible to D. semiclausum imago even though it
has a long (deep) corolla.
20
18
16
longevity (days)

14
12
10
8 y = 0.6138x + 10.682
R² = 0.1323 (Female)
6
4
y = 0.5528x + 10.338
2 R² = 0.105 (Male)

0
0 1 2 3 4 5 6 7 8
Corolla lenght (mm)

20
18
16
14
Longevity (days)

12
10
8 y = 0.4438x + 11.648
R² = 0.2482 (Female)
6
4 y = 0.4253x + 11.115
Female Male
R² = 0.2231 (Male)
2 Linear (Female) Linear (Male)
0
0 1 2 3 4 5 6 7 8 9 10 11 12
Corolla aperture (mm)

Figure 3. Regression analysis between D. semiclausum longevity and flower morphology. (A)
corolla length, (B) corolla aperture.

The long flower corolla should make it more difficult for the parasitoids to access the nectar
because it does not have mouthparts to reach the nectar. However, due to the exposed flower
characteristic (sepals and petals are separate), parasitoids can still access. Based on the observation,

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International e-Conference on Sustainable Agriculture and Farming System IOP Publishing
IOP Conf. Series: Earth and Environmental Science 694 (2021) 012049 doi:10.1088/1755-1315/694/1/012049

the parasitoid will have easier access to a flower even though it has a long corolla, but with the width
aperture and the exposed nectar location. Even though the flower has a short corolla, but the nectar is
hidden, the parasitoid cannot access it, so that the longevity will be shorter.

4. Conclusion
All refugia flower tested could increase D. semiclausum longevity than the negative control treatment.
The R. indica flower showed the best effect in increasing D. semiclausum longevity compared to other
treatments (female: 3.69 times, male: 3.65 times). The length and aperture of corolla flowers are
positively correlated with the longevity of parasitoids. The exposed flower nectar will make it easier
for the parasitoid to exploit it. The corolla aperture and the nectar location have more substantial
effects than the corolla length.

Acknowledgments
The authors wish to thank the Ministry of Education and Culture and the Ministry of Research and
Technology through the PMDSU Batch IV scholarship program for providing research grants.

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