Effects of the Milling Degree of Rice and Storage Volume on the Interaction Between Plodia interpunctella (Lepidoptera: Pyralidae) and Its Parasitoid Bracon hebetor (Hymenoptera: Braconidae)

J. Asia-Pacific Entomol. 8 (3): 273-278 (2005) www.entomology.or.kr

ECOLOGY AND BEHAVIOR

Effects of the Milling Degree of Rice and Storage Volume on the Interaction Between Plodia inferpuncfella (Lepidoptera: Pyralidae) and Its Parasitoid Bracon hebefor (Hymenoptera: Braconidae) Eun Young Yoon, Youngwoo Nam and Mun II Ryoo* Division of Environmental Science and Ecological Engineering, College of Life and Environmental Sciences, Korea University, Seoul 136-701, Korea

Abstract The ability of Bracon hebetor Say, a larval parasitoid of certain stored product moths, to suppress a Plodia interpunctella (Hubner) population was studied in differing rice products. The larvae of P. interpunctella gathered on the topmost layer of the experiment cages filled with rice product (less than 3 em in depth), and were rarely observed in deeper depths (deeper than 3 cm). Without P. interpunctella, B. heetor did not show a preference for any of the three types of milled rice products used. In rice flour, the searching behavior of B. hebetor for P. interpunctella was limited, apparently due to the thick webbing prouced by the moth larvae. B. hebetor suppressed P. interpunctella population successfully in cracked rice kernels, but failed to suppress the moth population in rice flour. In whole rice kernels, B. hebetor suppressed the moth population only when the volume of rice in the cage was large enough to support a high population density of P. interpunctella (2.4 kg/cage). Success and failure of B. hebetor to suppress the moth population in the three different rice products are discussed in relation to the larval webbing and intraspecific cometition of P. interpunctella larvae. Key words Bracon hebetor, intraspecific competition, milled rice, Plodia interpunctella, suppression, webbing

1998; Na and Ryoo, 2000). McGaughey (1974) found that the reproduction rate of the Indian meal moth, Plodia interpunctella (Hubner), and of six other insect pests in rice, decreased with increasing the degree of milling process. Activity of Lariophagus distinguendus Forster, an ectoparasitoid of Sitophilus granarius L., is influenced by the storage depth of grains (Johannes et al., 2002) and by commodity type (Ryoo et al., 1990). Better knowledge of the relation between the population dynamics of stored product pests and the food and microhabitat characteristics would clarify host-parasitoid interactions and assist in conducting biological control of stored products. Here we study the suppression capability of B. hebetor Say against P. interpunctella, a well-known gregarious parasitoid of the pest, in relation to the milled types of rice that comprise the microhabitat as well for the both species. Specifically we tested the interaction between P. interpunctella and B. hebetor in relation to the three different storage volumes (0.6, 1.2 and 2.4 kg) of the three milled types of rice, variety 'Ilpum': (rice flour, cracked kernels and whole kernels). Long-term experiments conducted on studying the vertical distribution of B. hebetor and P. interpunctella larvae, preference of the parasitoid for the three milled types of rice with and without P. interpunctella larvae, and the subequent suppression ability of the parasitoid over about 5 months.

Introduction The type and volume of stored food products detemine the physical and nutritional characteristics of the microhabitat for pests that infest food stores. This in turn affects the interaction between the pests and their parasitoids (LeCato, 1976; Locatelli and Limonta, *Corresponding author. E-mail: [email protected] Tel: +82-2-3290-3062; Fax: +82-2-925-1970 (Received June 15, 2005; Accepted August 16, 2005)

Materials and Methods Insects A stock culture of P. in an acrylic box with m' (Sativa oryza L.) 1996, and with dried

interpunctella was maintained brown rice of the variety 'Ilpu (13-14% m.c.) from 1986 to vegetable commodities until

274 J. Asia-Pacific Entomol. \101. 8 (2005)

2003, and then with artificial diets consisting of ground rice, glycerin, brewer's yeast and honey in the ratio of 80: 10: 5:5 by weight (Hirashima et al., 2001). B. hebetor was reared on the fourth and fifth larval instars from the stock culture of P. interpunctella. For the present study, P. interpunctella adults adult moths were collected from the stock culture and reared for one further generation on whole kernels of brown rice to alleviate the effects of food change. B. hebetor was collected from the stock culture and raised individually in a Petri dish
Searching activity of B. hebetor on the three milled types of rice To study the activity of B. hebetor in the three milled types of rice (rice flour, cracked kernels which were about 1/5 of whole kernel size and whole kernels), an acrylic cage (18 X30 X 1:5 ern) was divided into three cells (18 x lOx5 em) by two vertical acrylic plates (18 x5 em). Then each milled type of rice of 0.6 kg was introduced into a randomly selected cell, and seven pairs of B. hebetor (females and males < 24 h old) per cell were introduced, Because the cells were partly separated by the vertical plates, the parasitoids could move freely to other cells containing different milled type of rice. After 72 h the parasitoids in each cell and on cage wall were counted and sexed. This test was replicated foir times. To study the searching activity of B. hebetor on existence of P. interpunctella larvae, experimental cages were prepared as the same manner above. Then, 100 P. interpunctella larvae of fourth and fifth instars were introduced into each cell. After the larvae had settled in the cells, seven pairs of B. hebetor were placed in each cell and allowed to attack P. interpunctella larvae for 72 h. Then, all the B. hebetor introduced were removed frem the cells. The number of P. interpunctella and B. hebetor adults emerged from the cells were recorded daily starting from the 4th d after introduction until both species had finished emergence. This test was replicated four times for each milled type of rice.

Vertical distribution of P. interpunctella and B. hebetor in three milled types of rice A round plexi-glass cage (diameter 20 em, height 20 em) was divided vertically into five equal layers of 3 em height by four thin interseptal plastic plates,

which could be drawn in and out through the four horizontal slit holes on the side wall of the cage. The desired milled type of rice (rice flour, cracked kernels which were about 1/5 of whole kernel size or whole kernels) was filled to 15 em depth of the cage, with the wall slit holes closed by cotton cloth. Two hundred fourth larval instars of P. interpunctella were introduced into the cage, and held at 28±loC and 70-75% r.h. with a photoperiod of 16:8 (L:D) for 72 h. Then each was divided into five layers by inserting the interseptal plates, and the numbers of larvae in each layer were counted. Larvae were returned to the layer at which they had been found. The interseptal plates of the cage were drawn out and the slit holes were closed again with cotton cloth. After the larvae had settled in the layers, B. hebetor were placed on the upper of rice column in the cage, held for 72 h as the same manner above. The numbers of P. interpunctella larvae and B. hebetor adults distributed in each layer was counted. This test was replicated three times.

Suppression of P. interpunctella by B. hebe/or in three milled types of rice Quantities of 0.6, 1.2 or 2.4 kg of either rice flour, cracked kernels or whole kernels of brown rice (13-14 % m.c.) were introduced into an acrylic cage (18 X29 X15 em), with a plastic cover having a window (9 X 17 em) of nylon cloth for aeration. The depth of filled were about 1.0, 2.5 and 5.0 em corresponding to the amounts for 0.6, 1.2 and 2.4 kg, respectively. Ten pairs of P. interpunctella «24 h old) were introduced into each of nine treated cages (3 milled type of rice x 3 volumes). The cages were held at 28±OSC and 70-75% r.h. with a photoperiod of 16:8 (L:D) for 30 d. Then, three pairs of B. hebetor «24 h old) were added to each cage. The delayed introduction timing provided proper larval instars of P. interpunctella (4th and 5th instars) for B. hebetor. The numbers of P. interpunctella and B. hebetor in cages were counted every 10 d intervals up to 50 days and thereafter every 15 d intervals up to 110 d, with a minimum disturbance of experimental system. We could not count all the parasitoids emerging during the experimental period not to disturb the systems. Consequently, the numbers of B. hebetor at each observed time were regarded as a measure of the activity of B. hebe tor. This experiment was replicated three times. Twenty seven cages (3 milled types x 3 volumes x 3 replicates) which did not receive B. hebetor were used as untreated controls. The rice in each cage were not changed with fresh sources or topped up during the experimental period.

Interaction between P. interpunctella and B. hebetor

Data analysis The preference and searching actrvity of the parasitoids over the three milled type of rice were analyzed by the x 2- test and ANOVA (randomized block design). Mortality of the moth larvae in the three cells was compared using ANOVA (randomized block design). The vertical distribution of the moth and parasitoids in the rice products was compared by three way ANOVA (milled type of rice, presence of B. hebetor, layer and interactions) and means were separated by Tukey test (PROC GLM, SAS Institue, 1990). The suppression capability of B. hebetor in the long term observations was estimated based on the numbers of P. interpunctella in peaks of each treated cages and was compared by three way ANOVA as above.

Results Searching activity of B. hebetor in three milled types of rice Approximately half (55.4±5.3%) of the introduced B. hebetor were observed on the milled rice products

3 d after introduction when P. interpunctella was not introduced (Fig. 1). Significantly more females than males were found on the milled rice products; the mean percentage of females (±sd) was 83.3±8.2%, while males were 27.4 ± 4.6% (pooled data: x 2 =64.76; df=l; P
25

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(pooled data: x 2 =0.77; df=2; P>0.5). When 100 larvae of P. interpunctella were introduced into each cell containing the milled rice products, significantly more B. hebetor and fewer P. interpunctella emerged on the whole kernels than on both the cracked kernels and flour (F=26.40, df=2,9; P
Vertical distribution of P. interpunctella larvae and B. hebetor in three milled types of rice The numbers of larvae recovered per cage after 72 h ranged from 186 to 200. Most P. interpunctella larvae settled in the top layer (0-3 em in depth) of the cages in all the milled types of rice with and without B. hebetor (proportion of larvae settled in the top layer vs. those in the other layers, arcsine root transformation: F=lOl8.69; df=1,24; P
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Fig. 2. Number of Plodia interpunctella and Bracon hebetor emerging from three milled rice products. 100 moth larvae and 7 pairs of adult parasitoids per cell were introduced into the cage. Vertical bars indicate the standard error of the means based on four replications.

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Sequential changes in the number of P. interpunctette and B. hebetor emerging in three milled types 01 rice product Emerging of P. interpunctella in the cages without parasitoids peaked during 40-50 days after the introduction of P. interpunctella in all the cages of storage volumes and millec types of rice (Figs. 4, 5 and 6). The numbers of 1'. interpunctella in peaks were significantly different with milled types of rice, storage volume and parasitoid introductions (F=43.51; df=2, 34; P
Fig. 4. Sequential changes in the number of adult Plodia interpunctella (host) and Bracon hebetor (parasitoid) observed from three milled rice products in the cages with volume 0.6 kg. A, Band C indicate whole kernels, cracked kernels and flour, respectively. Vertical bars indicate standard error of the means based on three replications.

kernels, and the numbers ranged from 1,014.0 ± 78.23 to 825.33 ± 55.48. The lowest number of P. interpunctella adults was produced in the cage containing 0.6 kg-whole kernels (105.33 ± 6.74). Regardless of the milled type of rice and storage volume, the parasitoids were active in all the cages into which they were introduced. However, the parasitoids suppressed P. interpunctella populations significantly only in the cages containing cracked kernels of 0.6 kg, 1.2 kg and 2.4 kg and whole kernels of 2.4 kg (based on 95 confidence interval of the means) (Figs. 4, 5 and 6). Fig. 7 presents the suppressed rate of P. interpunctella in B. hebetor treated cages compared with untreated control cages based on the number of P. interpunctella in peaks.

Discussion Many studies have found that P. interpunctella is sensitive to available food substrate (LeCato, 1976; Locatelli and Limonta, 1988; Na and Ryoo, 1998, 2000; Subramanyam and Hagstrom, 1993). Reproduction of P. interpunctella decreased with increasing

Interaction between P. interpunctella and B. hebetor 277

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the degree of rice milling (McGaughey, 1974). Mbata and Osuji (1983) reported that the biology of P.

interpunctella varied with differing types of groundnut products; cracked nuts were more favorable than whole nuts or groundnuts meal. The present study supports the influence of substrate on P. interpunctella population. The type of rice product affected reproduction of the moth; of the three rice products used here, rice flour was the most favorable diet for the moth, in accordance with the finding of Lecato (1976) on cereals and soybeans, but in contrasts to the results of Locatelli and Limonta (1998) on groundnuts and buckwheat. The suppression ability of B. hebetor was related to type of rice product. P. interpunctella populations on the rice flour were not suppressed by B. hebetor, whereas the population on 2.4 kg-whole rice kernels and cracked rice kernels was suppressed significantly.

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1. Asia-Pacific Entomol. Vol. 8 (2005)

This phenomenon is clearly due in part to the differing webbing produced by the moth larvae. Larvae on the rice flour made a thick web-cover on the flour surface, severely inhibiting the parasitoids' searching activity (Plate 1). As well as the differences in webbing on the types of rice product, interaction between intraspecific competition among larvae and parasitism would be another factor in suppression of P. interpunctella population by B. hebetor. The moth population is sensitive to food shortage (I'odoler, 1974), and larval cannibalism is expected at high density (Boots, 1998; Sait et al., 1994). Under atack by B. hebetor, the moth larvae decreased in density such that the mortality due to the larval competition became low enough that it compensated for mortality due to parasitism. The number of moths in the next generation was therefore not reduced, The success of B. hebetor in suppressing the moths in the cage containing 2A-kg whole rice kernels, and the failure in the cage containing 0.6-kg and 1.2-kg whole rice kernels, supports this consideration. Suppression of the moth population in the cages containing cracked kernels, which are more favorable for the moth than whole kernels but less favorable than rice flour, can be explained by a combination of weaker intraspecific competition and parasitism. Yoon et al. (2001) reported a similar phenomenon in which a significantly higher number of moths were produced in a mixed culture with rice weevils than in a monoculture without rice weevils. They suggested that interspecific competition between rice weevils and young moth larvae on brown rice reduces the intraspecific larval mortality of the moth induced by food shortage. Although not so clear, the vertical distribution of P. interpunctella larvae seemed to be influenced by parasitism in the cages containing whole rice kernels (Fig. 3), suggesting a weak behavioral response to escape from the parasitoids. Deeper refuges could contribute to coexistence of Indian meal moth and parasitoid populations as suggested in Figs. 5 and 6. This relation between the quantity and type of rice products, and suppression capability of the parasitoid, suggests that the food quality and quantity involving intraspecific competition, and the related webbing behavior of moth larvae, should be taken into account in biological control programming of the moth by its parasitoid, B. hebetor.

Acknowledgements This study was supported financially by the Korea University Research Fund grant to the MI Ryoo. We appreciate greatly the reviewers' critical readings of the earlier draft and their valuable suggestions.

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