Biological Control 54 (2010) 75–82 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Compatibility of Heterorhabditis indica (Rhabditida: Heterorhabditidae) and Habrobracon hebetor (Hymenoptera: Braconidae) for biological control of Plodia interpunctella (Lepidoptera: Pyralidae) George N. Mbata a,*, David I. Shapiro-Ilan b a Department of Biology, Fort Valley State University, 1005 University Drive, Fort Valley, GA 31030, USA b USDA, Agricultural Research Service, Southeastern Fruit and Tree Nut Research Laboratory, 21 Dunbar Road, Byron, GA 31008, USA article info abstract Article history: The potential for integrating the application of Heterorhabditis indica Poinar, Karunakar, and David (Homl Received 12 August 2009 strain) and release of Habrobracon hebetor (Say) in the management of the Indianmeal moth, Plodia inter- Accepted 22 April 2010 punctella (Hübner), was investigated in the laboratory. A combination of the nematode and the parasitoid Available online 27 April 2010 was observed to increase the mortality of P. interpunctella. The interaction between the nematodes and parasitoids was not antagonistic but could possibly be additive or synergistic. Release of parasitoids or Keyword: application of nematodes alone generated between 62.25% and 71.25% mortality of the P. interpunctella Biological control larvae whereas combination of the two resulted in 98.0–99.25% mortality. The nematode was found to Entomopathogenic nematodes be virulent to the larvae of the parasitoid but not to the pupae and the adults. Adult female parasitoids Heterorhabditis indica Plodia interpunctella that were exposed to both uninfected and nematode-infected P. interpunctella larvae in a free-choice Habrobracon hebetor arena were unable to distinguish between the two. In contrast, infective juvenile nematodes preferen- Stored-products tially infected parasitized host larvae compared with healthy non-parasitized host larvae. Nematode reproduction was not significantly different in parasitized and non-parasitized host larvae. The combined application of H. indica and H. hebetor for the control of P. interpunctella may be beneficial if the detrimen- tal effects of the nematode on the parasitoid can be minimized through optimum timing. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction breakfast cereals and candies made with nuts and chocolate (Platt et al., 1998). Among all stored-product moth pests the Indianmeal moth, Plo- Pest management in post-harvest systems in the USA, from raw dia interpunctella (Hübner) (Lepidoptera: Pyralidae), is especially grain storage to food processing to value-added retail products, is important in the US and worldwide. P. interpunctella is a pest in facing a critical situation. Chemical insecticides have been used milling machinery and other food processing plants, warehouses, historically at all facets of the post-harvest handling of commodi- bakeries, and it contributes significantly to losses caused by insects ties. Some insecticides are effective and needed in some cases; oth- of stored commodities, particularly stored peanuts, stored cereals ers are probably ineffective and only add potentially harmful and processed food (Mbata and Osuji, 1983; Mbata, 1985, 1986). residues to food, which is cause for public concern (Foschi, P. interpunctella larvae spin silken threads, and mat infested prod- 1989). The Food Quality Protection Act of 1996 (FQPA, Anonymous ucts together using their silken webs. Female moths lay large num- (1996)) called for a re-evaluation of all pesticide labels and is tar- bers of eggs in food and on the walls and roofs of storage buildings geting organophosphate insecticides among which are some resid- (Mbata and Osuji, 1983; Mbata, 1985, 1986). The moth larvae hide ual insecticides (chlorpyrifos methyl, chlorpyrifos ethyl and in crevices and build up residual populations, which are responsi- malathion) commonly used by the food industry. Methyl bromide, ble for infestation of uninfested fresh commodities. Female moths an important fumigant in the management of stored-product in- lay eggs on or near food packages in response to food odors and sects, is an ozone-depleting substance that falls under an interna- also prior larval contamination (Phillips and Strand, 1994). Storage tional ban along with other organo-halides as mandated by the moths such as the P. interpunctella are considered among the most Montreal Protocol (Bell, 1996). In addition to the environmental is- common and visually obvious invaders of pet food, baking mixes, sues surrounding chemical insecticides are the facts that many populations of stored-product insects are resistant to commonly used chemicals (Georgiou and Saito, 1983; Subramanyam and Hag- * Corresponding author. Fax: +1 (478) 825 6104. strum, 1995) and consumers continue to demand high quality food E-mail addresses: [email protected], [email protected] (G.N. Mbata). that is also pest and residue free. Since an efficient replacement for 1049-9644/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2010.04.009 76 G.N. Mbata, D.I. Shapiro-Ilan / Biological Control 54 (2010) 75–82 methyl bromide has yet to be found, it is reasoned that integration including Steinernema riobrave Cabanillas, Poinar, and Raulston, of IPM (integrated pest management) tools may be a plausible ap- which had previously been reported to possess the highest viru- proach. To overcome the challenges faced by the stored-product lence among several steinernematids (Ramos-Rodríguez et al., industry, alternatives to pesticides are proposed for the manage- 2006). ment of storage insects. The use of natural enemies such as parasit- Deployment of entomopathogenic nematodes with parasitoids oids, Habrobracon hebetor (Say) (Hymenoptera: Habrobraconidae), could be a pest management strategy against residual populations and entomopathogenic nematodes such as Heterorhabditis indica of P. interpunctella in warehouses or in other enclosed post-harvest Poinar, Karunakar, and David (Homl strain) (Rhabditida: Heteror- storage systems. Interactions between some hymenopteran para- habditidae), have the potential to become alternative pest manage- sitoids and entomopathogenic nematodes have been investigated, ment tools in post-harvest storage systems (Cline and Press, 1990; and the ensuing results were mixed with respect to virulence of Brower and Press, 1990; Mbata and Shapiro-Ilan, 2005; Shapiro- the nematodes to the beneficial insects (Shannag and Capinera, Ilan et al., 2009). 2000; Sher et al., 2000; Head et al., 2003; Lacey et al., 2003; Dillon Habrobracon hebetor is a gregarious, ectoparasitoid that attacks et al., 2008). Sher et al. (2000) found that eulophid parasitoid wasp the wandering stage of larvae of most stored-products moths Diglyphus begini Ashmead was not susceptible to infection by the (Akinkurolere et al., 2009; Benson, 1974; Eliopoulos and Stathas, entomopathogenic nematode Steinernema carpocapsae (Weiser). 2008). The life cycle of the parasitoid is characterized by a short Dillon et al. (2008) found that the entomopathogenic nematodes, larval stage and a long pupal stage (Payne, 1933). The pupa is ade- Heterorhabditis downesi Stock Burnell and Griffin, and S. carpocap- cticous and exarate and pupation takes place in a cocoon. When sae, did not affect natural populations of Bracon hylobii developing reared on the pyralid moth, Ephestia kühniella Zeller, at tempera- on Hylobius abietis. However, other studies observed antagonistic tures between 20 and 27 °C, eggs of H. hebetor hatched between relationship between parasitoids and entomopathogenic nema- 2 and 4 days, larval developmental period was between 5 and todes. Shannag and Capinera (2000) observed that S. carpocapsae 8 days, while pupae enclosed in 6–8 days (Payne, 1933). However, infected newly emerged and cocoon-spinning larvae of Cardichiles when reared on P. interpunctella at 25 °C and 70% RH, both larval diaphaniae Marsh, a solitary internal wasp parasitoid of the melon- and pupal developmental periods were slightly extended to about worm, Diaphania hyalinata (L.), and pickleworm D. nititalis (Stoll). 7–9 days and 8–10 days for larvae and pupae, respectively (Mbata, Lacey et al. (2003) found that S. carpocapsae caused 70.7–85.5% unpublished observation). H. hebetor has been investigated for its mortality in larvae of two ectoparasitic ichneumonid species of potential as a biological control agent (Ullyett, 1945; Press et al., the codling moth, Cydia pomonella (L.). 1974, 1982; Cline, 1989; Cline et al., 1984; Cline and Press, 1990; Our objective was to determine how P. interpunctella’s idiobiont Brower and Press, 1990). In laboratory tests, H. hebetor produced parasitoid, H. hebetor, might interact with the heterorhabditid a 97% reduction of residual population of Ephestia cautella (Walk- nematode, H. indica, in a concomitant use of the two for control er), a species related to P. interpunctella, in food debris (Reinert of residual moth populations. In laboratory experiments, we inves- and King, 1971; Press et al., 1982). Cline et al. (1984) and Cline tigated the effects of combined versus single applications of the and Press (1990) observed that H. hebetor caused a significant two biocontrol agents on P. interpunctella mortality, the impact of reduction in the level of E. cautella infestation in small experimen- combined application on nematode and parasitoid yield, direct vir- tal packages of corn meal and raisins by H. hebetor.