- Email: [email protected]
Biological control of Plodia interpunctella (Lepidoptera: Pyralidae) by single and double releases of two larval parasitoids in bulk stored wheat
Journal of Stored Products Research 51 (2012) 1e5
Contents lists available at SciVerse ScienceDirect
Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Biological control of Plodia interpunctella (Lepidoptera: Pyralidae) by single and double releases of two larval parasitoids in bulk stored wheat Charles Adarkwah*, Matthias Schöller 1 Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Ecological Chemistry, Plant Analysis and Stored Product Protection, Königin-Luise-Str. 19, 14195 Berlin, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 1 June 2012
The Indian meal moth, Plodia interpunctella is a world-wide economically important pest of storedproducts and processed food commodities including bulk grain. Two larval parasitoids, Habrobracon hebetor and Venturia canescens were studied under laboratory conditions to suppress small populations of P. interpunctella in 30-L polyethylene jar filled with 20 kg wheat. Twenty 3 to 4-week-old moth larvae were released into the jar and were allowed to produce webbings in the grain for 3e4 d. Then 10, 20 or 40 female parasitoids were added. A further batch of parasitoids was added to half of the jars 4 d after the first batch, 7e8 d after the introduction of P. interpunctella. Treatments comprised untreated control, only V. canescens or only H. hebetor released, and the combination of both parasitoids per release. After two weeks, the grains were sieved, the numbers of surviving parental parasitoids recorded and the cocoons of moths and parasitoids were collected from each jar and kept under controlled conditions of 25 C. The emerged moth adults and parasitoid progeny were recorded until day 42. The highest mortality (93%) was observed with a single release of 20 H. hebetor plus 20 V. canescens (host-parasitoid ratio 1:1 for each parasitoid species). The various numbers of H. hebetor and V. canescens alone or in combination, once or twice released, led to mortalities between 50% and 80% that did not differ significantly. The single release of 10 H. hebetor or 10 V. canescens resulted in the lowest mortalities of P. interpunctella ranging from 34% to 39%. The different treatments affected the number of parasitoid offspring produced. Venturia canescens progeny occurred in all trials with combinations of the two parasitoid species. The single release of 20 H. hebetor resulted in more progeny emerged compared to all other treatments. For application in biological control, our data suggest the combination could be as least as effective as the release of H. hebetor alone. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: Stored products Braconidae Habrobracon hebetor Ichneumonidae Venturia canescens
1. Introduction Insect pests can cause extensive damage to durable stored products, both qualitatively and quantitatively. Beside beetle pests, stored-product moths like the Indian meal moth, Plodia interpunctella (Hübner) and the rice moth Corcyra cephalonica (Stainton) are major pests throughout the world causing considerable losses to cereal grains, grain legumes and other high value crops such as
* Corresponding author. Present address: Division Urban Plant Ecophysiology, Faculty for Agriculture and Horticulture, Humboldt-University of Berlin, Lentzeallee 55, 14195 Berlin, Germany. Tel.: þ49 30 2093 46436; fax: þ49 30 2093 46440. E-mail addresses: [email protected], [email protected] (C. Adarkwah). 1 Present address: Biologische Beratung Ltd., Storkower Str. 55, 10409 Berlin, Germany. 0022-474X/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jspr.2012.06.001
cocoa beans and dried fruits. Female moths lay eggs directly into bulk stored products or on shelves and food packages inside storage buildings. The larvae enter the products, feed and then often leave the products and hide in crevices, building up residual populations (Mohandass et al., 2007). Grain storage managers use synthetic insecticides admixed to the grain or applied to the store by fogging or spraying, or fumigation to reduce losses of stored grain to moth pests (Arthur and Peckman, 2006). There are several reasons to search for alternatives to synthetic insecticides. This includes: consumer preference for food without insecticide residues, worker safety concerns, resistant insect populations, and deregistration of insecticidal products. De-registration of products containing dichlorvos, for example, resulted in a significant increase of infestation of bulk stored grain by P. interpunctella in Germany. To overcome the challenges faced by the stored-product industry, alternatives to pesticides such as the use of natural enemies may be
2
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5
a plausible approach for the management of storage insects (Brower et al., 1996; Schöller, 2010). Habrobracon hebetor (Say) and Venturia canescens (Gravenhorst) are natural enemies of several stored product moths including P. interpunctella (Schöller, 1998; Heinlein et al., 2002; Ghimire and Phillips, 2010). The two parasitoid species occur sympatrically e.g. in Central Europe and the Mediterranean area (Prozell and Schöller, 1998; Lukas, 2002). Habrobracon hebetor is a gregarious idiobiont parasitoid, about 5 parasitoid offspring develop per last instar pyralid moth host larva (Eliopoulos and Stathas, 2008; Akinkurolere et al., 2009). Long-range host finding is mediated by volatiles emitted by the mandibular gland secretions of the moth larvae (Strand et al., 1989; Parra et al., 1996). Significant suppression of moth populations has been documented in different types of storage, e.g. bulk stored peanuts (Brower and Press, 1990), bulk stored grain (Schöller, 2000b) or retail stores (Grieshop et al., 2006). Venturia canescens is known to attack and successfully develop within the larvae of several lepidopterous pests of stored food products, mainly pyralids. All larval instars are suitable hosts except for the first instars (Salt, 1975, 1976). In temperate regions, only asexual populations are found (Beukeboom et al., 1999), while from the Mediterranean area male V. canescens are known. Venturia canescens is a solitary koinobiont parasitoid, only one parasitoid develops per host larva. As in H. hebetor long-range host finding is mediated by volatiles emitted by the mandibular gland secretions of the moth larvae (Corbet, 1971). Venturia canescens is currently not applied commercially, but field studies showed it to frequently occur in bakeries and mills associated with stored product moths (Prozell and Schöller, 1998; Lukas, 2002). Habrobracon hebetor has been applied commercially in Central Europe since 2002 (Schöller, 2010). In bakeries and mills, H. hebetor is released at a rate of 25/ 10 m2/month for several months to suppress moth populations. The technique to use multiple cohorts of parasitoids is also applied for Trichogramma evanescens Westwood to control moth eggs (Grieshop et al., 2006; Schöller et al., 2006). However, for bulk stored wheat there are no studies so far comparing the effects of single and multiple releases of the parasitoids H. hebetor and V. canescens to control P. interpunctella. Therefore, the purpose of the present study is to determine the effectiveness of single and double releases of the two larval parasitoids alone or in combination to suppress P. interpunctella adult emergence in bulk stored wheat in an early stage of infestation. 2. Materials and methods 2.1. Culturing of insects The P. interpunctella originated from Berlin, Germany, and were reared in growth cabinets maintained at 25 1 C, 65 5% r.h. under a 16:8 h light:dark regime. They were reared in l-L glass jars on 250 g of wheat bran with a few broken almonds added. Two hundred and fifty eggs were added to each jar. After 3e4 weeks, third to 4th instar larvae were obtained for the bioassays. The original populations of V. canescens and H. hebetor were obtained from colonies maintained at the Biologische Beratung Ltd., Berlin, Germany, and reared in glass jars containing the larvae of Ephestia kuehniella. Habrobracon hebetor was originally collected in Berlin in 1995 and V. canescens in Schleswig-Holstein in 2009. A few drops of honey were added into the jars to enhance reproduction of the parasitoids.
Table 1 Percentage mortality of P. interpunctella in jars containing 20 kg of wheat, data are means (SD) of percentage emergence of adults from 20 three-week-old larvae, untreated or exposed to H. hebetor and V. canescens alone or in combination. 10Vc ¼ 10 V. canescens single release, 10Hh ¼ 10 female H. hebetor single release, 2 ¼ two releases, n ¼ 5. Treatment
% Mortality (meansa SD)
Untreated (control) 2 20Hh þ 20Vc 20Hh þ 20Vc 20Vc 20Hh 2 10Hh þ 10Vc 10Hh þ 10Vc 2 10Vc 10Vc 2 10Hh 10Hh
3.0 80.0 93.0 59.0 66.0 73.0 51.0 50.0 34.0 62.0 39.0
2.7a 5.0c 7.6d 14.7c 10.8c 9.7c 10.8c 6.1c 5.4b 12.6c 7.4b
a Means in the same column followed by the same lowercase letter do not differ significantly at P < 0.05 (Tukey Test).
Germany, was filled into a 30-L polyethylene jar (height 42 cm 30 cm diameter 108 cm circumference) with an opening of 12 cm diameter. The wheat was kept at 15 C for two weeks to kill any living insects. After this period, the grains were removed and kept under the experimental temperature and humidity conditions for 1 week before being used in the experiments. The wheat grain moisture content at the start of the experiment was 12e14%. The moisture content was determined by using Pfeuffer Mess-Prüfgeräte HOH-Express HE 50 obtained from Pfeuffer GmbH, Kitzingen, Germany. The jars were placed in a climatic chamber at 25 1 C, 65 5% r.h. Twenty 3e4-week-old moth larvae were released into each jar. Larvae were allowed to enter the grain and produce webbings for 3e4 d. A drop of honey was added into each jar to provide parasitoids with food. Then the freshly emerged parasitoids were added at rates of 10, 20 or 40 females. The jars were immediately covered with nylon gauze held in place with rubber bands. In some of the trials, a second batch of parasitoids was released 4 d after the first release i.e. 7e8 d after the introduction of the moth larvae. The following treatments were used: control without parasitoids (untreated), V. canescens treated grain, H. hebetor treated grain and H. hebetor þ V. canescens treated grain. All parasitoid treatments had single and double releases, i.e. there were a total of seven different treatments. Each treatment and the untreated control had 5 replicates. After the two-week experimental period, the grains were sieved and the numbers of surviving parental parasitoids at the time of sieving counted. The sievings of each jar containing the cocoons of the moth larvae and the parasitoids were collected and placed in a Petri-dish which was kept under controlled conditions of 25 1 C and 65 5% r.h. The emerged adults of P. interpunctella and adult parasitoid progeny were recorded until day 42. 2.3. Statistical analysis Percentage natural mortality data of P. interpunctella adults were not corrected for control mortality, because mortality in the control treatment was <5%. Percentage mortality data were transformed to arcsine square root to stabilize heteroscedastic treatment variances. Data were subjected to one-way analysis of variance (ANOVA) using SigmaStatÒ 3.1 software. Treatments were considered significantly different at the 5% level. Means were separated using the Tukey Test.
2.2. Effectiveness of H. hebetor and V. canescens
3. Results
In the first bioassay, 20 kg of Bio-wheat (Toni, cv) obtained from Erzeugergemeinschaft Biokorntakt GmbH & Co. KG, Berlin,
Natural mortality of the 3-week-old P. interpunctella larvae as assessed by counting emerged adults was low, i.e. 3% (Table 1). The
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5
parasitoid releases significantly affected larval mortality (one-way ANOVA, df ¼ 10, F ¼ 36.08, P ¼ <0.001). The highest mortality of 93% was achieved by a single release of 20 H. hebetor plus 20 V. canescens. Exposure to various numbers of H. hebetor and V. canescens alone or in combination, once or twice released, led to mortalities between 50 and 80% that did not differ significantly. The single release of 10 H. hebetor or 10 V. canescens resulted in the significantly lowest mortalities of P. interpunctella ranging from 34 to 39% (Table 1). No difference in natural mortality of the total number of parental parasitoids per jar was detected at the time of sieving the grain depending on treatment (one-way ANOVA, df ¼ 9, F ¼ 1.959, P ¼ 0.071). However, analysing the mortality for the respective parasitoid species, effects of the different treatments were detected both for V. canescens (one-way ANOVA, df ¼ 6, F ¼ 2.827, P ¼ 0.028) and H. hebetor (one-way ANOVA, df ¼ 6, F ¼ 2.609, P ¼ 0.039). Only 28% of the V. canescens released survived in the double release of 10 V. canescens and 10 H. hebetor, while the survival ranged from 40% to 58% in the other treatments. In H. hebetor, most parasitoids, i.e. 78% survived in the double release of 20 V. canescens and 20 H. hebetor, while survival ranged from 50% to 63% in the other treatments (Table 2). The different treatments significantly affected the mean total number of parasitoid offspring produced from the 20 host larvae exposed (one-way ANOVA, df ¼ 9, F ¼ 34.655, P < 0.001). The highest number of offspring resulted from the release of 20 H. hebetor, i.e. 46.8, and more than 40 parasitoid offspring were counted in the other treatments including the release of 20 H. hebetor at a time, too. Significantly fewer offspring were produced in the treatments with 10 H. hebetor released at a time, i.e. 21e33. The fewest progeny were produced in the trials with V. canescens only, i.e. 6e11 (Table 3). The mean number of V. canescens progeny emerging significantly differed in the various treatments (one-way ANOVA, df ¼ 6, F ¼ 4.7, P ¼ 0.002). Significantly more V. canescens progeny, i.e. more than 10, were produced in the trials with 20 V. canescens at a time compared to trials with 10 V. canescens at a time (Table 3). The mean number of H. hebetor progeny emerging also differed significantly in the various treatments (one-way ANOVA, df ¼ 6, F ¼ 10.242, P < 0.001). In the trials with a single release of 20 H. hebetor, significantly more progeny emerged compared to all other treatments. The repeated release of 10 H. hebetor resulted in significantly more progeny compared to a single release of 10 H. hebetor, but only when H. hebetor was released alone and not in combination with V. canescens (Table 3). The different treatments significantly affected the number of progeny per female (one-way ANOVA, df ¼ 13, F ¼ 45.04, P < 0.001).
3
Table 3 Mean number (SD) of total parasitoid offspring, and respective H. hebetor and V. canescens offspring, that emerged from 20 three-week-old larvae of P. interpunctella. A total of 10, 20, 40 or 80 female parasitoids, H. hebetor alone or in combination with V. canescens, by single, or double (¼2) releases; 10Vc ¼ 10 V. canescens single release, 20Hh ¼ 20 H. hebetor single release, 10Vc þ 10Hh ¼ 10 V. canescens and 10 H. hebetor single release, n ¼ 5. Treatment
Mean numbera SD parasitoid offspring Total
2 20Hh þ 20Vc 20Hh þ 20Vc 2 10Hh þ 10Vc 10Hh þ 10Vc 2 10Hh 20Hh 10Hh 2 10Vc 20Vc 10Vc
41.2 44.2 27.4 25.2 33.2 46.8 20.6 9.6 11.0 5.8
V. canescens 14.2b 7.3ab 2.3cd 4.0de 5.8c 4.8a 3.1e 1.1fg 1.2f 1.6g
12.2 10.2 5.6 6.4
3.3a 5.4ab 1.5c 2.6bc
H. hebetor 29.0 34.0 21.8 18.8 33.2 46.8 20.6
14.0cd 7.2b 2.9d 3.0d 5.8bc 4.8a 3.1d
9.6 1.1ac 11.0 1.2ab 5.8 1.6c
a Means in the same column followed by the same lowercase letter do not differ significantly at P < 0.05 (Tukey Test).
Progeny of V. canescens per female ranged from 0.28 to 0.64, V. canescens had significantly fewer progeny per female compared to H. hebetor in all treatments except for two, i.e. 2 20Vc 20Hh and 2 10Vc 10Hh. Most progeny per female were produced in the treatments with 20 or 10 H. hebetor, i.e. 2.34 and 2.06, respectively (Fig. 1). 4. Discussion Habrobracon hebetor can suppress pyralid moths in bulk stored products (Brower and Press, 1990; Schöller, 2000b; Adarkwah et al., 2011), but there is no information for V. canescens. Venturia canescens does not enter into the bulk grain. The females only walk over the grain surface. In response to host kairomonal signals, they insert the abdomen between the grain kernels for oviposition (Schöller, 2000a). This behaviour restricts the availability of hosts to those located in the very top layer of the grain, ca. 1 cm deep, and those that leave the grain bulk for pupation. Habrobracon hebetor was found to penetrate a grain column up to 30 cm deep in rye (Schöller, 2000b) and 14 cm deep in rice (Adarkwah et al., 2010). As these were the maximum depths tested, the braconids may
Table 2 Mean percentage (SD) surviving parental parasitoids 14 d after start of the experiment when 10, 20, 40 or 80 parasitoids, H. hebetor alone or in combination with V. canescens, were released at day 3e4 after introduction of host larvae in single and at day 3e4 and 7e8 in double release treatments, n ¼ 5. Treatment
Meana SD percentage surviving parental parasitoids Total
2 20Hh þ 20Vc 20Hh þ 20Vc 2 10Hh þ 10Vc 10Hh þ 10Vc 2 10Hh 20Hh 10Hh 2 10Vc 20Vc 10Vc
45.8 59.0 42.0 56.0 62.0 63.0 52.0 58.0 42.0 56.0
3.9a 2.9a 7.8a 12.5a 12.6a 5.7a 25.9a 8.4a 9.7a 18.2a
V. canescens 41.0 40.0 28.0 54.0
2.9ab 6.1ab 16.0bc 19.5a
H. hebetor 50.5 78.0 56.0 58.0 62.0 63.0 52.0
9.3 a 4.5bc 6.5ab 8.4ab 12.6ab 5.7ab 25.9a
58.0 8.4a 42.0 9.7ab 56.0 18.2a
a Means in the same column followed by the same lowercase letter do not differ significantly at P < 0.05 (Tukey Test).
Fig. 1. Mean (SD) number of parasitoid progeny per female, AeG Venturia canescens, HeN Habrobracon hebetor, depending on the following treatments: A ¼ 2 10Vc 10Hh, B ¼ 2 20Vc 20Hh, C ¼ 2 10Vc, D ¼ 20Hh 20Vc, E ¼ 20Vc, F ¼ 10Vc, G ¼ 10Vc 10Hh, H ¼ 2 20Vc 20Hh, I ¼ 2 10Vc 10Hh, J ¼ 2 10Hh, K ¼ 20Hh 20Vc, L ¼ 10Vc 10Hh, M ¼ 10Hh, N ¼ 20Hh, with Hh ¼ H. hebetor, Vc ¼ V. canescens, 2 ¼ two releases.
4
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5
penetrate deeper. Assuming parasitism in wheat is similar to that in rye, it is unlikely moth larvae could have escaped parasitism at the bottom of the jars as they were filled to a height less than 30 cm. Moreover, late instar larvae of pyralid stored-product moths are active in the top layers of bulk grain (Richards and Waloff, 1946). Three components of structures are relevant for foraging parasitoids: the surface area, the structural heterogeneity (e.g. flowers, nectaries and leaves in green plants), and the structural complexity (Andow and Prokrym, 1990). In bulk grain, the surface and the structural complexity are large, but the structural heterogeneity is low. In a simple environment with a small surface area and negligible heterogeneity and complexity like a 5 cm diameter Petri-dish, observations during rearing of H. hebetor showed two females completely suppress adult emergence from 20 last instar larvae of P. interpunctella exposed (host:parasitoid-ratio 10:1). In the experiment reported here, about 65% parasitism only was achieved by a host:parasitoid-ratio of 1:1 for H. hebetor. In bulk rye, Schöller (2000b) achieved 85% parasitism in about 100 kg rye filled to a depth of 10 cm and a host:parasitoid-ratio of 1:1. This data suggest a negative effect of depth of bulk grain on effectiveness by H. hebetor. At 25 C and honey available, a single V. canescens can parasitise 100 P. interpunctella larvae. However, when 10 larvae of P. interpunctella were exposed in a simple environment with a small surface area, V. canescens parasitised a mean of 76% of the hosts, while some were left unparasitised and others were superparasitised (Heinlein et al., 2002). In a simple 8 m3 environment with a larger surface area, V. canescens proved to effectively find host larvae, while effectiveness of H. hebetor was less than V. canescens (Paust et al., 2006). Two larval parasitoids of P. interpunctella using the same kairomone are expected to compete for hosts. Press et al. (1977) studied both species in small boxes and found the reproduction of H. hebetor not to be affected by the presence of V. canescens, but the reproduction of V. canescens was significantly reduced by the presence of H. hebetor. They predicted the extinction of V. canescens after release of H. hebetor in commercial warehouses and granaries. This was not confirmed in our experiment, V. canescens progeny were produced in all the four trials with combinations of the two species. Moreover, no difference in mortality of the total number of parasitoids/jar was detected at the time of sieving the grain depending on treatment, indicating no mortality of the parental adult parasitoids due to the presence of the second parasitoid species. This experiment simulated a low infestation level, and the reproduction of both parasitoid species was host-limited. Under these conditions, the reproductive fitness of individual female V. canescens was not affected by the different treatments. However, the lowest numbers of progeny/female were observed for the two treatments including two simultaneous releases of H. hebetor indicating a competition effect. Venturia canescens-parasitised hosts could also be parasitized by H. hebetor. On the other hand, V. canescens is not able to develop within H. hebetor parasitized moth larvae. For H. hebetor, the lowest numbers of progeny per female were also recorded in the treatments including two releases of H. hebetor. This might be due to immature mortality caused by superparasitism. Benson (1973) and Yu et al. (2003) found parasitoid larval mortality to increase if the number of eggs on a host exceeded 8 and 10, respectively. Interestingly, the treatments achieving the second and third most suppression of P. interpunctella adult emergence resulted in low reproductive fitness of individual female V. canescens and H. hebetor; below 0.9 progeny per female. This indicates a threshold between inoculative and inundative biological control for this system between host:parasitoid-ratios of 4:1 and 2:1. In inoculative biological control, the pest suppression is mainly performed by the
progeny of the added beneficial, while in inundative biological control, the laboratory-reared beneficials perform the control (Franz and Krieg, 1982). A more effective parasitoid population build-up could therefore be achieved with lower release rates, while faster control could be achieved with higher release rates. However, the population dynamics under different temperature conditions are complex and will be better addressed with a simulation model. For the application in biological control, our data suggest the two-parasitoid combination could be as effective as H. hebetor alone, or the combination could be even more effective. The higher number of progeny per female in H. hebetor could allow this species to establish in aggregations of P. interpunctella, whereas V. canescens should also be able to persist in small scattered populations of P. interpunctella due to its good long-range host finding and thelytokous mode of reproduction. In large warehouses, the better long-range host finding of V. canescens might be of special importance. However, the data suggest also that large numbers of parasitoids have to be applied in warehouses or silos with bulk-stored grain, and the parasitoid releases will need to be integrated with other control methods. Acknowledgements Agnes Paul from the Julius Kühn-Institut assisted in the insect rearing for what we are most grateful. References Adarkwah, C., Büttner, C., Reichmuth, C., Obeng-Ofori, D., Prozell, S., Schöller, M., 2010. Ability of the larval ectoparasitoid Habrobracon hebetor (Say, 1836) (Hymenoptera: Braconidae) to locate the rice moth Corcyra cephalonica (Stainton, 1865) (Lepidoptera: Pyralidae) in bagged and bulk stored rice. Journal of Plant Diseases and Protection 117, 67e70. Adarkwah, C., Obeng-Ofori, D., Adler, C., Büttner, C., Reichmuth, C., Schöller, M., 2011. Integration of Calneem oil and parasitoids to control Cadra cautella and Corcyra cephalonica in stored grain cereals. Phytoparasitica 39, 223e233. Akinkurolere, R.O., Boyer, S., Chen, H., Zhang, H., 2009. Parasitism and host-location preference in Habrobracon hebetor (Hymenoptera: Braconidae): role of refuge, choice, and host instar. Journal of Economic Entomology 102, 610e615. Andow, D.A., Prokrym, D.R., 1990. Plant structural complexity and host finding by a parasitoid. Oecologia 82, 162e165. Arthur, F.H., Peckman, P.S., 2006. Insect management with residual insecticides. In: Heaps, J.W. (Ed.), Insect Management for Food Storage and Processing, second ed. AACC International, St. Paul, Minnesota, pp. 167e173. Benson, J.F., 1973. Intraspecific competition in the population dynamics of Bracon hebetor Say. Journal of Animal Ecology 42, 193e197. Beukeboom, L.W., Driessen, G., Luckerhoff, L., Bernstein, C., Lapchin, L., van Alphen, J.J.M., 1999. Distribution and relatedness of sexual and asexual Venturia canescens (Hymenoptera). Proceedings of the Section Experimental and Applied Entomology 10, 23e28. Brower, J.H., Press, J.W., 1990. Interaction of Bracon hebetor Say (Hymenoptera: Braconidae) and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) in suppressing stored-product moth populations in small in-shell peanut storage. Journal of Economic Entomology 83, 1096e1110. Brower, J.H., Smith, L., Vail, P.V., Flinn, P.W., 1996. Biological control. In: Subramanyam, B., Hagstrum, D.W. (Eds.), Integrated Management of Insects in Stored Products. Marcel Dekker, New York, pp. 223e286. Corbet, S.A., 1971. Mandibular gland secretion of larvae of the flour moth, Anagasta kühniella contains an epideictic pheromone and elicits oviposition movements in a hymenopteran parasite. Nature 232, 481e484. Eliopoulos, P.A., Stathas, G.J., 2008. Life tables of Habrabracon hebetor (Hymenoptera: Braconidae) parasitizing Anagasta kuehniella and Plodia interpunctella (Lepidoptera: Pyralidae): effect of host density. Journal of Economic Entomology 101, 982e988. Franz, J.M., Krieg, A., 1982. Biologische Schädlingsbekämpfung, third ed. Parey, Berlin. Ghimire, M.N., Phillips, T.W., 2010. Suitability of different lepidopteran host species for development of Bracon hebetor (Hymenoptera: Braconidae). Environmental Entomology 39, 449e458. Grieshop, M.J., Flinn, P.W., Nechols, J.W., Campbell, J.F., 2006. Effects of shelf architecture and parasitoid release height on biological control of Plodia interpunctella (Lepidoptera: Pyralidae) eggs by Trichogramma deion (Hymenoptera: Trichogrammatidae). Journal of Economic Entomology 99, 2202e2209. Heinlein, G., Schöller, M., Prozell, S., Reichmuth, Ch, 2002. Oviposition of Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) parasitizing the
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5 Indian meal moth Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). In: Adler, C., Navarro, S., Schöller, M., Stengard-Hansen, L. (Eds.), Integrated Protection in Stored Products. IOBC wprs Bulletin 25(3), pp. 109e114. Lukas, J., 2002. Parasitoids occurring in food processing factories and grain stores. In: Zdarkova, E., Wakefield, M., Lukas, J., Hubert, J. (Eds.), Proceedings of the Second Meeting of Working Group 4, Cost Action 842, Prague, May 30e31, 2002, pp. 83e86. Mohandass, S., Arthur, F.H., Zhu, K.Y., Throne, J.E., 2007. Biology and management of Plodia interpunctella (Lepidoptera: Pyralidae) in stored products. Journal of Stored Products Research 43, 302e311. Parra, J.R.P., Vinson, S.B., Gomes, S.M., Consoli, F.L., 1996. Flight response of Bracon hebetor (Say) (Hymenoptera: Braconidae) in a wind tunnel to volatiles associated with infestations of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Biological Control 6, 143e150. Paust, A., Reichmuth, C., Büttner, C., Prozell, S., Adler, C.S., Schöller, M., 2006. Spatial effects on competition between the larval parasitoids Habrobracon hebetor (Say) (Hymenoptera: Braconidae) and Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) parasitising the Mediterranean flour moth, Ephestia kuehniella. In: Lorini, I., Bacaltchuk, B., Beckel, H., Deckers, D., Sundfeld, E., dos Santos, J.P., Biagi, J.D., Celaro, J.C., Faroni, L.R.D.’A., Bortolini, L. de O.F., Sartori, M.R., Elias, M.C., Guedes, R.N.C., da Fonseca, R.G., Scussel, V.M. (Eds.), Proceedings of the 9th International Working Conference on Stored Product Protection, 15 to 18 October 2006, Campinas, São Paulo, Brazil. Brazilian Postharvest Association e ABRAPOS, Passo Fundo, RS, Brazil, pp. 797e803. Press, J.W., Flaherty, B.R., Arbogast, R.T., 1977. Interactions among Nemeritis canescens (Hymenoptera: Ichneumonidae), Bracon hebetor (Hymenoptera: Braconidae), and Ephestia cautella (Lepidoptera: Pyralidae). Journal of the Kansas Entomological Society 50, 259e262. Prozell, S., Schöller, M., 1998. Insect fauna of a bakery, processing organic grain and applying Trichogramma evanescens Westwood. In: Adler, C., Schöller, M. (Eds.), Integrated Protection of Stored Products. IOBC wprs Bulletin 21, pp. 39e44. Richards, O.W., Waloff, N., 1946. The study of a population of Ephestia elutella living on bulk grain. Transactions of the Royal Entomological Society London 97, 253e298.
5
Salt, G., 1975. The fate of an internal parasitoid, Nemeritis canescens, in a variety of insects. Transactions of the Royal Entomological Society London 127, 141e461. Salt, G., 1976. The hosts of Nemeritis canescens, a problem in the host specificity of insect parasitoids. Ecological Entomology 1, 163e167. Schöller, M., 1998. Biologische Bekämpfung vorratschädlicher Arthropoden mit Räubern und Parasitoiden e Sammelbericht und Bibliographie. In: Reichmuth, Ch (Ed.), 100 Jahre Pflanzenschutzforschung. Wichtige Arbeitsschwerpunkte im Vorratsschutz. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft, Heft 342. Parey, Berlin, pp. 85e189. Schöller, M., 2000a. Biologische Bekämpfung der Speichermotte Ephestia elutella in gelagertem Getreide. In: Agrarökologie 35, Bern, ISBN 3-909192-15-7, 143 pp. Schöller, M., 2000b. Forager in the rye: biological control of Ephestia elutella in bulk grain. In: Adler, C., Schöller, M. (Eds.), Integrated Protection in Stored Products. IOBC Buletin 23, pp. 149e160. Schöller, M., Flinn, P.W., Grieshop, M.J., Zdarkova, E., 2006. Biological control of stored product pests. In: Heaps, J.W. (Ed.), Insect Management for Food Storage and Processing. American Association of Cereal Chemists International, St. Paul, Minnesota, USA, pp. 67e87. Schöller, M., 2010. Biological control of stored-product insects in commodities, food processing facilities and museums. In: Carvalho, M.O., Fields, P.G., Adler, C.S., Arthur, F.H., Athanassiou, C.G., Campbell, J.F., Fleurat-Lessard, F., Flinn, P.W., Hodges, R.J., Isikber, A.A., Navarro, S., Noyes, R.T., Riudavets, J., Sinha, K.K., Thorpe, G.R., Timlick, B.H., Trematerra, P., White, N.D.G. (Eds.), Proceedings of the 10th International Working Conference on Stored Product Protection, 27 Junee2 July 2010, Estoril, Portugal, Julius Kühn-Archiv 425. Julius Kühn-Institut, Berlin, pp. 596e606. Strand, M.R., Williams, H.M., Vinson, S.B., Mudd, A., 1989. Kairomonal activities of 2acylcyclohexane-1,3 diones produced by Ephestia kuehniella Zeller in eliciting searching behavior by the parasitoid Bracon hebetor (Say). Journal of Chemical Ecology 15, 1491e1500. Yu, S.H., Ryoo, M.I., Na, J.H., Choi, W.I., 2003. Effect of host density on egg dispersion and sex ratio of progeny of Bracon hebetor (Hymenoptera: Braconidae). Journal of Stored Products Research 39, 385e393.
Contents lists available at SciVerse ScienceDirect
Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Biological control of Plodia interpunctella (Lepidoptera: Pyralidae) by single and double releases of two larval parasitoids in bulk stored wheat Charles Adarkwah*, Matthias Schöller 1 Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Ecological Chemistry, Plant Analysis and Stored Product Protection, Königin-Luise-Str. 19, 14195 Berlin, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 1 June 2012
The Indian meal moth, Plodia interpunctella is a world-wide economically important pest of storedproducts and processed food commodities including bulk grain. Two larval parasitoids, Habrobracon hebetor and Venturia canescens were studied under laboratory conditions to suppress small populations of P. interpunctella in 30-L polyethylene jar filled with 20 kg wheat. Twenty 3 to 4-week-old moth larvae were released into the jar and were allowed to produce webbings in the grain for 3e4 d. Then 10, 20 or 40 female parasitoids were added. A further batch of parasitoids was added to half of the jars 4 d after the first batch, 7e8 d after the introduction of P. interpunctella. Treatments comprised untreated control, only V. canescens or only H. hebetor released, and the combination of both parasitoids per release. After two weeks, the grains were sieved, the numbers of surviving parental parasitoids recorded and the cocoons of moths and parasitoids were collected from each jar and kept under controlled conditions of 25 C. The emerged moth adults and parasitoid progeny were recorded until day 42. The highest mortality (93%) was observed with a single release of 20 H. hebetor plus 20 V. canescens (host-parasitoid ratio 1:1 for each parasitoid species). The various numbers of H. hebetor and V. canescens alone or in combination, once or twice released, led to mortalities between 50% and 80% that did not differ significantly. The single release of 10 H. hebetor or 10 V. canescens resulted in the lowest mortalities of P. interpunctella ranging from 34% to 39%. The different treatments affected the number of parasitoid offspring produced. Venturia canescens progeny occurred in all trials with combinations of the two parasitoid species. The single release of 20 H. hebetor resulted in more progeny emerged compared to all other treatments. For application in biological control, our data suggest the combination could be as least as effective as the release of H. hebetor alone. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: Stored products Braconidae Habrobracon hebetor Ichneumonidae Venturia canescens
1. Introduction Insect pests can cause extensive damage to durable stored products, both qualitatively and quantitatively. Beside beetle pests, stored-product moths like the Indian meal moth, Plodia interpunctella (Hübner) and the rice moth Corcyra cephalonica (Stainton) are major pests throughout the world causing considerable losses to cereal grains, grain legumes and other high value crops such as
* Corresponding author. Present address: Division Urban Plant Ecophysiology, Faculty for Agriculture and Horticulture, Humboldt-University of Berlin, Lentzeallee 55, 14195 Berlin, Germany. Tel.: þ49 30 2093 46436; fax: þ49 30 2093 46440. E-mail addresses: [email protected], [email protected] (C. Adarkwah). 1 Present address: Biologische Beratung Ltd., Storkower Str. 55, 10409 Berlin, Germany. 0022-474X/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jspr.2012.06.001
cocoa beans and dried fruits. Female moths lay eggs directly into bulk stored products or on shelves and food packages inside storage buildings. The larvae enter the products, feed and then often leave the products and hide in crevices, building up residual populations (Mohandass et al., 2007). Grain storage managers use synthetic insecticides admixed to the grain or applied to the store by fogging or spraying, or fumigation to reduce losses of stored grain to moth pests (Arthur and Peckman, 2006). There are several reasons to search for alternatives to synthetic insecticides. This includes: consumer preference for food without insecticide residues, worker safety concerns, resistant insect populations, and deregistration of insecticidal products. De-registration of products containing dichlorvos, for example, resulted in a significant increase of infestation of bulk stored grain by P. interpunctella in Germany. To overcome the challenges faced by the stored-product industry, alternatives to pesticides such as the use of natural enemies may be
2
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5
a plausible approach for the management of storage insects (Brower et al., 1996; Schöller, 2010). Habrobracon hebetor (Say) and Venturia canescens (Gravenhorst) are natural enemies of several stored product moths including P. interpunctella (Schöller, 1998; Heinlein et al., 2002; Ghimire and Phillips, 2010). The two parasitoid species occur sympatrically e.g. in Central Europe and the Mediterranean area (Prozell and Schöller, 1998; Lukas, 2002). Habrobracon hebetor is a gregarious idiobiont parasitoid, about 5 parasitoid offspring develop per last instar pyralid moth host larva (Eliopoulos and Stathas, 2008; Akinkurolere et al., 2009). Long-range host finding is mediated by volatiles emitted by the mandibular gland secretions of the moth larvae (Strand et al., 1989; Parra et al., 1996). Significant suppression of moth populations has been documented in different types of storage, e.g. bulk stored peanuts (Brower and Press, 1990), bulk stored grain (Schöller, 2000b) or retail stores (Grieshop et al., 2006). Venturia canescens is known to attack and successfully develop within the larvae of several lepidopterous pests of stored food products, mainly pyralids. All larval instars are suitable hosts except for the first instars (Salt, 1975, 1976). In temperate regions, only asexual populations are found (Beukeboom et al., 1999), while from the Mediterranean area male V. canescens are known. Venturia canescens is a solitary koinobiont parasitoid, only one parasitoid develops per host larva. As in H. hebetor long-range host finding is mediated by volatiles emitted by the mandibular gland secretions of the moth larvae (Corbet, 1971). Venturia canescens is currently not applied commercially, but field studies showed it to frequently occur in bakeries and mills associated with stored product moths (Prozell and Schöller, 1998; Lukas, 2002). Habrobracon hebetor has been applied commercially in Central Europe since 2002 (Schöller, 2010). In bakeries and mills, H. hebetor is released at a rate of 25/ 10 m2/month for several months to suppress moth populations. The technique to use multiple cohorts of parasitoids is also applied for Trichogramma evanescens Westwood to control moth eggs (Grieshop et al., 2006; Schöller et al., 2006). However, for bulk stored wheat there are no studies so far comparing the effects of single and multiple releases of the parasitoids H. hebetor and V. canescens to control P. interpunctella. Therefore, the purpose of the present study is to determine the effectiveness of single and double releases of the two larval parasitoids alone or in combination to suppress P. interpunctella adult emergence in bulk stored wheat in an early stage of infestation. 2. Materials and methods 2.1. Culturing of insects The P. interpunctella originated from Berlin, Germany, and were reared in growth cabinets maintained at 25 1 C, 65 5% r.h. under a 16:8 h light:dark regime. They were reared in l-L glass jars on 250 g of wheat bran with a few broken almonds added. Two hundred and fifty eggs were added to each jar. After 3e4 weeks, third to 4th instar larvae were obtained for the bioassays. The original populations of V. canescens and H. hebetor were obtained from colonies maintained at the Biologische Beratung Ltd., Berlin, Germany, and reared in glass jars containing the larvae of Ephestia kuehniella. Habrobracon hebetor was originally collected in Berlin in 1995 and V. canescens in Schleswig-Holstein in 2009. A few drops of honey were added into the jars to enhance reproduction of the parasitoids.
Table 1 Percentage mortality of P. interpunctella in jars containing 20 kg of wheat, data are means (SD) of percentage emergence of adults from 20 three-week-old larvae, untreated or exposed to H. hebetor and V. canescens alone or in combination. 10Vc ¼ 10 V. canescens single release, 10Hh ¼ 10 female H. hebetor single release, 2 ¼ two releases, n ¼ 5. Treatment
% Mortality (meansa SD)
Untreated (control) 2 20Hh þ 20Vc 20Hh þ 20Vc 20Vc 20Hh 2 10Hh þ 10Vc 10Hh þ 10Vc 2 10Vc 10Vc 2 10Hh 10Hh
3.0 80.0 93.0 59.0 66.0 73.0 51.0 50.0 34.0 62.0 39.0
2.7a 5.0c 7.6d 14.7c 10.8c 9.7c 10.8c 6.1c 5.4b 12.6c 7.4b
a Means in the same column followed by the same lowercase letter do not differ significantly at P < 0.05 (Tukey Test).
Germany, was filled into a 30-L polyethylene jar (height 42 cm 30 cm diameter 108 cm circumference) with an opening of 12 cm diameter. The wheat was kept at 15 C for two weeks to kill any living insects. After this period, the grains were removed and kept under the experimental temperature and humidity conditions for 1 week before being used in the experiments. The wheat grain moisture content at the start of the experiment was 12e14%. The moisture content was determined by using Pfeuffer Mess-Prüfgeräte HOH-Express HE 50 obtained from Pfeuffer GmbH, Kitzingen, Germany. The jars were placed in a climatic chamber at 25 1 C, 65 5% r.h. Twenty 3e4-week-old moth larvae were released into each jar. Larvae were allowed to enter the grain and produce webbings for 3e4 d. A drop of honey was added into each jar to provide parasitoids with food. Then the freshly emerged parasitoids were added at rates of 10, 20 or 40 females. The jars were immediately covered with nylon gauze held in place with rubber bands. In some of the trials, a second batch of parasitoids was released 4 d after the first release i.e. 7e8 d after the introduction of the moth larvae. The following treatments were used: control without parasitoids (untreated), V. canescens treated grain, H. hebetor treated grain and H. hebetor þ V. canescens treated grain. All parasitoid treatments had single and double releases, i.e. there were a total of seven different treatments. Each treatment and the untreated control had 5 replicates. After the two-week experimental period, the grains were sieved and the numbers of surviving parental parasitoids at the time of sieving counted. The sievings of each jar containing the cocoons of the moth larvae and the parasitoids were collected and placed in a Petri-dish which was kept under controlled conditions of 25 1 C and 65 5% r.h. The emerged adults of P. interpunctella and adult parasitoid progeny were recorded until day 42. 2.3. Statistical analysis Percentage natural mortality data of P. interpunctella adults were not corrected for control mortality, because mortality in the control treatment was <5%. Percentage mortality data were transformed to arcsine square root to stabilize heteroscedastic treatment variances. Data were subjected to one-way analysis of variance (ANOVA) using SigmaStatÒ 3.1 software. Treatments were considered significantly different at the 5% level. Means were separated using the Tukey Test.
2.2. Effectiveness of H. hebetor and V. canescens
3. Results
In the first bioassay, 20 kg of Bio-wheat (Toni, cv) obtained from Erzeugergemeinschaft Biokorntakt GmbH & Co. KG, Berlin,
Natural mortality of the 3-week-old P. interpunctella larvae as assessed by counting emerged adults was low, i.e. 3% (Table 1). The
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5
parasitoid releases significantly affected larval mortality (one-way ANOVA, df ¼ 10, F ¼ 36.08, P ¼ <0.001). The highest mortality of 93% was achieved by a single release of 20 H. hebetor plus 20 V. canescens. Exposure to various numbers of H. hebetor and V. canescens alone or in combination, once or twice released, led to mortalities between 50 and 80% that did not differ significantly. The single release of 10 H. hebetor or 10 V. canescens resulted in the significantly lowest mortalities of P. interpunctella ranging from 34 to 39% (Table 1). No difference in natural mortality of the total number of parental parasitoids per jar was detected at the time of sieving the grain depending on treatment (one-way ANOVA, df ¼ 9, F ¼ 1.959, P ¼ 0.071). However, analysing the mortality for the respective parasitoid species, effects of the different treatments were detected both for V. canescens (one-way ANOVA, df ¼ 6, F ¼ 2.827, P ¼ 0.028) and H. hebetor (one-way ANOVA, df ¼ 6, F ¼ 2.609, P ¼ 0.039). Only 28% of the V. canescens released survived in the double release of 10 V. canescens and 10 H. hebetor, while the survival ranged from 40% to 58% in the other treatments. In H. hebetor, most parasitoids, i.e. 78% survived in the double release of 20 V. canescens and 20 H. hebetor, while survival ranged from 50% to 63% in the other treatments (Table 2). The different treatments significantly affected the mean total number of parasitoid offspring produced from the 20 host larvae exposed (one-way ANOVA, df ¼ 9, F ¼ 34.655, P < 0.001). The highest number of offspring resulted from the release of 20 H. hebetor, i.e. 46.8, and more than 40 parasitoid offspring were counted in the other treatments including the release of 20 H. hebetor at a time, too. Significantly fewer offspring were produced in the treatments with 10 H. hebetor released at a time, i.e. 21e33. The fewest progeny were produced in the trials with V. canescens only, i.e. 6e11 (Table 3). The mean number of V. canescens progeny emerging significantly differed in the various treatments (one-way ANOVA, df ¼ 6, F ¼ 4.7, P ¼ 0.002). Significantly more V. canescens progeny, i.e. more than 10, were produced in the trials with 20 V. canescens at a time compared to trials with 10 V. canescens at a time (Table 3). The mean number of H. hebetor progeny emerging also differed significantly in the various treatments (one-way ANOVA, df ¼ 6, F ¼ 10.242, P < 0.001). In the trials with a single release of 20 H. hebetor, significantly more progeny emerged compared to all other treatments. The repeated release of 10 H. hebetor resulted in significantly more progeny compared to a single release of 10 H. hebetor, but only when H. hebetor was released alone and not in combination with V. canescens (Table 3). The different treatments significantly affected the number of progeny per female (one-way ANOVA, df ¼ 13, F ¼ 45.04, P < 0.001).
3
Table 3 Mean number (SD) of total parasitoid offspring, and respective H. hebetor and V. canescens offspring, that emerged from 20 three-week-old larvae of P. interpunctella. A total of 10, 20, 40 or 80 female parasitoids, H. hebetor alone or in combination with V. canescens, by single, or double (¼2) releases; 10Vc ¼ 10 V. canescens single release, 20Hh ¼ 20 H. hebetor single release, 10Vc þ 10Hh ¼ 10 V. canescens and 10 H. hebetor single release, n ¼ 5. Treatment
Mean numbera SD parasitoid offspring Total
2 20Hh þ 20Vc 20Hh þ 20Vc 2 10Hh þ 10Vc 10Hh þ 10Vc 2 10Hh 20Hh 10Hh 2 10Vc 20Vc 10Vc
41.2 44.2 27.4 25.2 33.2 46.8 20.6 9.6 11.0 5.8
V. canescens 14.2b 7.3ab 2.3cd 4.0de 5.8c 4.8a 3.1e 1.1fg 1.2f 1.6g
12.2 10.2 5.6 6.4
3.3a 5.4ab 1.5c 2.6bc
H. hebetor 29.0 34.0 21.8 18.8 33.2 46.8 20.6
14.0cd 7.2b 2.9d 3.0d 5.8bc 4.8a 3.1d
9.6 1.1ac 11.0 1.2ab 5.8 1.6c
a Means in the same column followed by the same lowercase letter do not differ significantly at P < 0.05 (Tukey Test).
Progeny of V. canescens per female ranged from 0.28 to 0.64, V. canescens had significantly fewer progeny per female compared to H. hebetor in all treatments except for two, i.e. 2 20Vc 20Hh and 2 10Vc 10Hh. Most progeny per female were produced in the treatments with 20 or 10 H. hebetor, i.e. 2.34 and 2.06, respectively (Fig. 1). 4. Discussion Habrobracon hebetor can suppress pyralid moths in bulk stored products (Brower and Press, 1990; Schöller, 2000b; Adarkwah et al., 2011), but there is no information for V. canescens. Venturia canescens does not enter into the bulk grain. The females only walk over the grain surface. In response to host kairomonal signals, they insert the abdomen between the grain kernels for oviposition (Schöller, 2000a). This behaviour restricts the availability of hosts to those located in the very top layer of the grain, ca. 1 cm deep, and those that leave the grain bulk for pupation. Habrobracon hebetor was found to penetrate a grain column up to 30 cm deep in rye (Schöller, 2000b) and 14 cm deep in rice (Adarkwah et al., 2010). As these were the maximum depths tested, the braconids may
Table 2 Mean percentage (SD) surviving parental parasitoids 14 d after start of the experiment when 10, 20, 40 or 80 parasitoids, H. hebetor alone or in combination with V. canescens, were released at day 3e4 after introduction of host larvae in single and at day 3e4 and 7e8 in double release treatments, n ¼ 5. Treatment
Meana SD percentage surviving parental parasitoids Total
2 20Hh þ 20Vc 20Hh þ 20Vc 2 10Hh þ 10Vc 10Hh þ 10Vc 2 10Hh 20Hh 10Hh 2 10Vc 20Vc 10Vc
45.8 59.0 42.0 56.0 62.0 63.0 52.0 58.0 42.0 56.0
3.9a 2.9a 7.8a 12.5a 12.6a 5.7a 25.9a 8.4a 9.7a 18.2a
V. canescens 41.0 40.0 28.0 54.0
2.9ab 6.1ab 16.0bc 19.5a
H. hebetor 50.5 78.0 56.0 58.0 62.0 63.0 52.0
9.3 a 4.5bc 6.5ab 8.4ab 12.6ab 5.7ab 25.9a
58.0 8.4a 42.0 9.7ab 56.0 18.2a
a Means in the same column followed by the same lowercase letter do not differ significantly at P < 0.05 (Tukey Test).
Fig. 1. Mean (SD) number of parasitoid progeny per female, AeG Venturia canescens, HeN Habrobracon hebetor, depending on the following treatments: A ¼ 2 10Vc 10Hh, B ¼ 2 20Vc 20Hh, C ¼ 2 10Vc, D ¼ 20Hh 20Vc, E ¼ 20Vc, F ¼ 10Vc, G ¼ 10Vc 10Hh, H ¼ 2 20Vc 20Hh, I ¼ 2 10Vc 10Hh, J ¼ 2 10Hh, K ¼ 20Hh 20Vc, L ¼ 10Vc 10Hh, M ¼ 10Hh, N ¼ 20Hh, with Hh ¼ H. hebetor, Vc ¼ V. canescens, 2 ¼ two releases.
4
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5
penetrate deeper. Assuming parasitism in wheat is similar to that in rye, it is unlikely moth larvae could have escaped parasitism at the bottom of the jars as they were filled to a height less than 30 cm. Moreover, late instar larvae of pyralid stored-product moths are active in the top layers of bulk grain (Richards and Waloff, 1946). Three components of structures are relevant for foraging parasitoids: the surface area, the structural heterogeneity (e.g. flowers, nectaries and leaves in green plants), and the structural complexity (Andow and Prokrym, 1990). In bulk grain, the surface and the structural complexity are large, but the structural heterogeneity is low. In a simple environment with a small surface area and negligible heterogeneity and complexity like a 5 cm diameter Petri-dish, observations during rearing of H. hebetor showed two females completely suppress adult emergence from 20 last instar larvae of P. interpunctella exposed (host:parasitoid-ratio 10:1). In the experiment reported here, about 65% parasitism only was achieved by a host:parasitoid-ratio of 1:1 for H. hebetor. In bulk rye, Schöller (2000b) achieved 85% parasitism in about 100 kg rye filled to a depth of 10 cm and a host:parasitoid-ratio of 1:1. This data suggest a negative effect of depth of bulk grain on effectiveness by H. hebetor. At 25 C and honey available, a single V. canescens can parasitise 100 P. interpunctella larvae. However, when 10 larvae of P. interpunctella were exposed in a simple environment with a small surface area, V. canescens parasitised a mean of 76% of the hosts, while some were left unparasitised and others were superparasitised (Heinlein et al., 2002). In a simple 8 m3 environment with a larger surface area, V. canescens proved to effectively find host larvae, while effectiveness of H. hebetor was less than V. canescens (Paust et al., 2006). Two larval parasitoids of P. interpunctella using the same kairomone are expected to compete for hosts. Press et al. (1977) studied both species in small boxes and found the reproduction of H. hebetor not to be affected by the presence of V. canescens, but the reproduction of V. canescens was significantly reduced by the presence of H. hebetor. They predicted the extinction of V. canescens after release of H. hebetor in commercial warehouses and granaries. This was not confirmed in our experiment, V. canescens progeny were produced in all the four trials with combinations of the two species. Moreover, no difference in mortality of the total number of parasitoids/jar was detected at the time of sieving the grain depending on treatment, indicating no mortality of the parental adult parasitoids due to the presence of the second parasitoid species. This experiment simulated a low infestation level, and the reproduction of both parasitoid species was host-limited. Under these conditions, the reproductive fitness of individual female V. canescens was not affected by the different treatments. However, the lowest numbers of progeny/female were observed for the two treatments including two simultaneous releases of H. hebetor indicating a competition effect. Venturia canescens-parasitised hosts could also be parasitized by H. hebetor. On the other hand, V. canescens is not able to develop within H. hebetor parasitized moth larvae. For H. hebetor, the lowest numbers of progeny per female were also recorded in the treatments including two releases of H. hebetor. This might be due to immature mortality caused by superparasitism. Benson (1973) and Yu et al. (2003) found parasitoid larval mortality to increase if the number of eggs on a host exceeded 8 and 10, respectively. Interestingly, the treatments achieving the second and third most suppression of P. interpunctella adult emergence resulted in low reproductive fitness of individual female V. canescens and H. hebetor; below 0.9 progeny per female. This indicates a threshold between inoculative and inundative biological control for this system between host:parasitoid-ratios of 4:1 and 2:1. In inoculative biological control, the pest suppression is mainly performed by the
progeny of the added beneficial, while in inundative biological control, the laboratory-reared beneficials perform the control (Franz and Krieg, 1982). A more effective parasitoid population build-up could therefore be achieved with lower release rates, while faster control could be achieved with higher release rates. However, the population dynamics under different temperature conditions are complex and will be better addressed with a simulation model. For the application in biological control, our data suggest the two-parasitoid combination could be as effective as H. hebetor alone, or the combination could be even more effective. The higher number of progeny per female in H. hebetor could allow this species to establish in aggregations of P. interpunctella, whereas V. canescens should also be able to persist in small scattered populations of P. interpunctella due to its good long-range host finding and thelytokous mode of reproduction. In large warehouses, the better long-range host finding of V. canescens might be of special importance. However, the data suggest also that large numbers of parasitoids have to be applied in warehouses or silos with bulk-stored grain, and the parasitoid releases will need to be integrated with other control methods. Acknowledgements Agnes Paul from the Julius Kühn-Institut assisted in the insect rearing for what we are most grateful. References Adarkwah, C., Büttner, C., Reichmuth, C., Obeng-Ofori, D., Prozell, S., Schöller, M., 2010. Ability of the larval ectoparasitoid Habrobracon hebetor (Say, 1836) (Hymenoptera: Braconidae) to locate the rice moth Corcyra cephalonica (Stainton, 1865) (Lepidoptera: Pyralidae) in bagged and bulk stored rice. Journal of Plant Diseases and Protection 117, 67e70. Adarkwah, C., Obeng-Ofori, D., Adler, C., Büttner, C., Reichmuth, C., Schöller, M., 2011. Integration of Calneem oil and parasitoids to control Cadra cautella and Corcyra cephalonica in stored grain cereals. Phytoparasitica 39, 223e233. Akinkurolere, R.O., Boyer, S., Chen, H., Zhang, H., 2009. Parasitism and host-location preference in Habrobracon hebetor (Hymenoptera: Braconidae): role of refuge, choice, and host instar. Journal of Economic Entomology 102, 610e615. Andow, D.A., Prokrym, D.R., 1990. Plant structural complexity and host finding by a parasitoid. Oecologia 82, 162e165. Arthur, F.H., Peckman, P.S., 2006. Insect management with residual insecticides. In: Heaps, J.W. (Ed.), Insect Management for Food Storage and Processing, second ed. AACC International, St. Paul, Minnesota, pp. 167e173. Benson, J.F., 1973. Intraspecific competition in the population dynamics of Bracon hebetor Say. Journal of Animal Ecology 42, 193e197. Beukeboom, L.W., Driessen, G., Luckerhoff, L., Bernstein, C., Lapchin, L., van Alphen, J.J.M., 1999. Distribution and relatedness of sexual and asexual Venturia canescens (Hymenoptera). Proceedings of the Section Experimental and Applied Entomology 10, 23e28. Brower, J.H., Press, J.W., 1990. Interaction of Bracon hebetor Say (Hymenoptera: Braconidae) and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) in suppressing stored-product moth populations in small in-shell peanut storage. Journal of Economic Entomology 83, 1096e1110. Brower, J.H., Smith, L., Vail, P.V., Flinn, P.W., 1996. Biological control. In: Subramanyam, B., Hagstrum, D.W. (Eds.), Integrated Management of Insects in Stored Products. Marcel Dekker, New York, pp. 223e286. Corbet, S.A., 1971. Mandibular gland secretion of larvae of the flour moth, Anagasta kühniella contains an epideictic pheromone and elicits oviposition movements in a hymenopteran parasite. Nature 232, 481e484. Eliopoulos, P.A., Stathas, G.J., 2008. Life tables of Habrabracon hebetor (Hymenoptera: Braconidae) parasitizing Anagasta kuehniella and Plodia interpunctella (Lepidoptera: Pyralidae): effect of host density. Journal of Economic Entomology 101, 982e988. Franz, J.M., Krieg, A., 1982. Biologische Schädlingsbekämpfung, third ed. Parey, Berlin. Ghimire, M.N., Phillips, T.W., 2010. Suitability of different lepidopteran host species for development of Bracon hebetor (Hymenoptera: Braconidae). Environmental Entomology 39, 449e458. Grieshop, M.J., Flinn, P.W., Nechols, J.W., Campbell, J.F., 2006. Effects of shelf architecture and parasitoid release height on biological control of Plodia interpunctella (Lepidoptera: Pyralidae) eggs by Trichogramma deion (Hymenoptera: Trichogrammatidae). Journal of Economic Entomology 99, 2202e2209. Heinlein, G., Schöller, M., Prozell, S., Reichmuth, Ch, 2002. Oviposition of Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) parasitizing the
C. Adarkwah, M. Schöller / Journal of Stored Products Research 51 (2012) 1e5 Indian meal moth Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). In: Adler, C., Navarro, S., Schöller, M., Stengard-Hansen, L. (Eds.), Integrated Protection in Stored Products. IOBC wprs Bulletin 25(3), pp. 109e114. Lukas, J., 2002. Parasitoids occurring in food processing factories and grain stores. In: Zdarkova, E., Wakefield, M., Lukas, J., Hubert, J. (Eds.), Proceedings of the Second Meeting of Working Group 4, Cost Action 842, Prague, May 30e31, 2002, pp. 83e86. Mohandass, S., Arthur, F.H., Zhu, K.Y., Throne, J.E., 2007. Biology and management of Plodia interpunctella (Lepidoptera: Pyralidae) in stored products. Journal of Stored Products Research 43, 302e311. Parra, J.R.P., Vinson, S.B., Gomes, S.M., Consoli, F.L., 1996. Flight response of Bracon hebetor (Say) (Hymenoptera: Braconidae) in a wind tunnel to volatiles associated with infestations of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Biological Control 6, 143e150. Paust, A., Reichmuth, C., Büttner, C., Prozell, S., Adler, C.S., Schöller, M., 2006. Spatial effects on competition between the larval parasitoids Habrobracon hebetor (Say) (Hymenoptera: Braconidae) and Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) parasitising the Mediterranean flour moth, Ephestia kuehniella. In: Lorini, I., Bacaltchuk, B., Beckel, H., Deckers, D., Sundfeld, E., dos Santos, J.P., Biagi, J.D., Celaro, J.C., Faroni, L.R.D.’A., Bortolini, L. de O.F., Sartori, M.R., Elias, M.C., Guedes, R.N.C., da Fonseca, R.G., Scussel, V.M. (Eds.), Proceedings of the 9th International Working Conference on Stored Product Protection, 15 to 18 October 2006, Campinas, São Paulo, Brazil. Brazilian Postharvest Association e ABRAPOS, Passo Fundo, RS, Brazil, pp. 797e803. Press, J.W., Flaherty, B.R., Arbogast, R.T., 1977. Interactions among Nemeritis canescens (Hymenoptera: Ichneumonidae), Bracon hebetor (Hymenoptera: Braconidae), and Ephestia cautella (Lepidoptera: Pyralidae). Journal of the Kansas Entomological Society 50, 259e262. Prozell, S., Schöller, M., 1998. Insect fauna of a bakery, processing organic grain and applying Trichogramma evanescens Westwood. In: Adler, C., Schöller, M. (Eds.), Integrated Protection of Stored Products. IOBC wprs Bulletin 21, pp. 39e44. Richards, O.W., Waloff, N., 1946. The study of a population of Ephestia elutella living on bulk grain. Transactions of the Royal Entomological Society London 97, 253e298.
5
Salt, G., 1975. The fate of an internal parasitoid, Nemeritis canescens, in a variety of insects. Transactions of the Royal Entomological Society London 127, 141e461. Salt, G., 1976. The hosts of Nemeritis canescens, a problem in the host specificity of insect parasitoids. Ecological Entomology 1, 163e167. Schöller, M., 1998. Biologische Bekämpfung vorratschädlicher Arthropoden mit Räubern und Parasitoiden e Sammelbericht und Bibliographie. In: Reichmuth, Ch (Ed.), 100 Jahre Pflanzenschutzforschung. Wichtige Arbeitsschwerpunkte im Vorratsschutz. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft, Heft 342. Parey, Berlin, pp. 85e189. Schöller, M., 2000a. Biologische Bekämpfung der Speichermotte Ephestia elutella in gelagertem Getreide. In: Agrarökologie 35, Bern, ISBN 3-909192-15-7, 143 pp. Schöller, M., 2000b. Forager in the rye: biological control of Ephestia elutella in bulk grain. In: Adler, C., Schöller, M. (Eds.), Integrated Protection in Stored Products. IOBC Buletin 23, pp. 149e160. Schöller, M., Flinn, P.W., Grieshop, M.J., Zdarkova, E., 2006. Biological control of stored product pests. In: Heaps, J.W. (Ed.), Insect Management for Food Storage and Processing. American Association of Cereal Chemists International, St. Paul, Minnesota, USA, pp. 67e87. Schöller, M., 2010. Biological control of stored-product insects in commodities, food processing facilities and museums. In: Carvalho, M.O., Fields, P.G., Adler, C.S., Arthur, F.H., Athanassiou, C.G., Campbell, J.F., Fleurat-Lessard, F., Flinn, P.W., Hodges, R.J., Isikber, A.A., Navarro, S., Noyes, R.T., Riudavets, J., Sinha, K.K., Thorpe, G.R., Timlick, B.H., Trematerra, P., White, N.D.G. (Eds.), Proceedings of the 10th International Working Conference on Stored Product Protection, 27 Junee2 July 2010, Estoril, Portugal, Julius Kühn-Archiv 425. Julius Kühn-Institut, Berlin, pp. 596e606. Strand, M.R., Williams, H.M., Vinson, S.B., Mudd, A., 1989. Kairomonal activities of 2acylcyclohexane-1,3 diones produced by Ephestia kuehniella Zeller in eliciting searching behavior by the parasitoid Bracon hebetor (Say). Journal of Chemical Ecology 15, 1491e1500. Yu, S.H., Ryoo, M.I., Na, J.H., Choi, W.I., 2003. Effect of host density on egg dispersion and sex ratio of progeny of Bracon hebetor (Hymenoptera: Braconidae). Journal of Stored Products Research 39, 385e393.