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Biological Control 21, 134 139 (2001) doi:10.1006/bcon.2000.0911, available online at http://www.idealibrary.

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Control Potential of Three Hymenopteran Parasitoid Species against the Bean Weevil in Stored Beans: The Effect of Adult Parasitoid Nutrition on Longevity and Progeny Production
Ine Schmale, Felix L. Wa ckers, 1 Cesar Cardona,* and Silvia Dorn
Institute of Plant Sciences, Applied Entomology, Swiss Federal Institute of Technology (ETH), CH-8092 Zu rich, Switzerland; and *Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia Received May 11, 2000; accepted December 13, 2000

INTRODUCTION We evaluated the longevity and progeny production of three hymenopteran parasitoids of Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae) when kept with or without food sources. In absence of adult food, Dinarmus basalis Ashm. (Pteromalidae) and Heterospilus prosopidis (Viereck) (Braconidae) lived longer than Anisopteromalus calandrae (Howard) (Pteromalidae). D. basalis produced the highest number of progeny and had the longest reproductive lifetime, making it the most promising parasitoid for the control of A. obtectus. A. calandrae performed poorly with A. obtectus and thus seems unsuitable as a control agent against this host. H. prosopidis had a shorter oviposition period than D. basalis, resulting in a lower lifetime progeny production. To determine the effect of food sources, either honey, sugarcane, or host larvae were offered to the parasitoids. Honey was a suitable food source for all three parasitoids. Honey as a food supplement for the synovigenic species D. basalis and A. calandrae increased their lifetime progeny production through an increase in reproductive lifetime, whereas in the proovigenic species H. prosopidis consumption of honey resulted in a higher number of progeny through an increase in daily oviposition rate rather than an increase in oviposition period. Positive effects of sugarcane and host-feeding were observed only for D. basalis. 2001 Academic Press Key Words: Dinarmus basalis; Anisopteromalus calandrae; Heterospilus prosopidis; Acanthoscelides obtectus; parasitoids; bean weevil; postharvest pest; biological control; nutrition; longevity; progeny production.

1 To whom correspondence should be addressed at CTO-N100, Boterhoeksestr. 48, 6666 GA Heteren, The Netherlands. Fax: 312647-23227. E-mail: waeckers@cto.nioo.knaw.nl.

The common bean (Phaseolus vulgaris L.) is produced in over 75% of developing countries, with the greatest concentration in Latin America. It is also one of the most important foods in the developing world, where small-scale farmers are the principal producers. The bruchids Acanthoscelides obtectus (Say) and Zabrotes subfasciatus (Boheman) are the major postharvest pests of dry beans in Latin America. A. obtectus attack the bean seeds in the eld and subsequently infest storage units, whereas Z. subfasciatus attack only stored seeds (Cardona, 1989). When left untreated, weevil populations grow exponentially and can completely destroy the stored crops within a few months (I. Schmale et al., unpublished). Whereas bean varieties with resistance against Z. subfasciatus have been identied (van Schoonhoven et al., 1983) and developed for use (Cardona et al., 1990), nontoxic methods for the control of A. obtectus are still lacking. Nontoxic means of control are of particular signicance for on-farm storage in developing countries (Dorn, 1998). Biological control can be a viable tool, as benecial insects may occur naturally or can be released where needed by farmers. Furthermore, biological control of A. obtectus is expected to be compatible with bean cultivars with resistance to Z. subfasciatus and thus can be used in integrated pest management programs in regions where both bruchid species occur together (Dorn, 1998). The effectiveness of natural enemies used in augmentative biological control can be optimized by selection of species based on several key criteria (Pak and van Lenteren, 1984). This study compared three bruchid parasitoids with respect to their longevity and progeny production. We included the synovigenic ectoparasitoid Dinarmus basalis Ashmead, which has previously been shown to be a promising control agent against Callosobruchus chinensis (L.) (Islam and Kabir, 1995) and Callosobruchus maculatus (F.) and

1049-9644/01 $35.00 Copyright 2001 by Academic Press All rights of reproduction in any form reserved.

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Bruchidius atrolineatus (Pic) (Ouedraogo et al., 1996; Sanon et al., 1998) and is also reported on Callosobruchus subinnotatus (Pic), A. obtectus, Z. subfasciatus, and other grain-attacking beetles (Rasplus, 1989). The synovigenic ectoparasitoid Anisopteromalus calandrae (Howard) has been identied as one of the most promising candidates for biological control of a wide range of storage pests, including maize weevils, rice weevils, and several bruchid beetles in beans (Ghani and Sweetman, 1955; Williams and Floyd, 1971; Brower et al., 1996). The proovigenic solitary ectoparasitoid Heterospilus prosopidis (Viereck) is known to attack a wide range of bruchid beetles (Kistler, 1985). We measured longevity and progeny production for the above three candidate species. Both of these parameters can be strongly affected by food availability (Laetemia et al., 1995). Especially in storage systems, supplemental food can be expected to be an effective tool to enhance parasitoid efcacy (Wa ckers et al., 1998). We tested the effect of three different food sources on parasitoid longevity and progeny production.
MATERIALS AND METHODS

Beans. In all experiments we used the commonly cultivated susceptible bean variety P. vulgaris L. var. Diacol-Calima (Leguminosae). Seeds were obtained from the farm La Providencia in Restrepo, Valle de Cauca, Colombia. They were harvested the same year in which the experiments were conducted. Following harvest they were kept in the freezer at 12C for 1 week to remove any background pest infestation. Pest. The experiments were carried out with A. obtectus (Coleoptera: Bruchidae). A locally collected and periodically renewed colony of this species has been maintained by the Bean Entomology Laboratory at Centro Internacional de Agricultura Tropical (CIAT) Cali, Colombia on P. vulgaris for 15 years. Cultures were maintained using methods described by van Schoonhoven et al. (1983), at 26C and 80% RH. Fourth instar host larvae are the preferred stage for all three parasitoid species tested (Heong, 1981; MarWai and Fujii, 1990; Smith, 1993). To obtain fourth instars for the experiments, eight beans were infested with 20 5-day-old eggs of A. obtectus. The number of larvae penetrating the beans was indirectly assessed by subtraction of the number of unhatched eggs and dead rst instars from the number of eggs rst introduced. Larvae reached the fourth instar stage by day 13. Parasitoid species. D. basalis (Hymenoptera: Pteromalidae) was collected and reared from A. obtectus attacking P. vulgaris L. var. Diacol-Calima in a grain storage in Buga, Valle de Cauca, Colombia. Subsequently, this parasitoid was reared on A. obtectus on P. vulgaris L. var. Diacol-Calima by the Bean Entomology Laboratory in CIAT.

A. calandrae (Hymenoptera: Pteromalidae) and H. prosopidis (Hymenoptera: Braconidae) had been reared on C. chinensis on cowpea (Vigna unguiculata Walp.) by the Applied Entomology Group, ETH Zu rich. Before being used in the experiments a colony was established on A. obtectus on P. vulgaris L. var. DiacolCalima at the Bean Entomology Laboratory in CIAT. All parasitoid species were reared at 20 25C, 70% RH, and 12:12 L:D h by provision of freshly emerged parasitoid cohorts with beans containing fourth instars of A. obtectus. Under these conditions, emergence began approximately 18 days after parasitization. Experimental site. Conditions in experimental chambers were 20 25C, 70% RH, and 12:12 L:D h, which corresponds to the local natural habitat of the pest. Longevity. Newly emerged parasitoid females (0 24 h old) were kept in groups of ve individuals in a plastic vial (21 cm 3). The following potential food sources were offered: (1) a drop of honey, renewed weekly; (2) a mature sugarcane stem piece (approx. 1 cm 1 cm 0.5 cm), added one time at the beginning of the experiment; (3) bean seeds infested with fourth instar A. obtectus, renewed weekly; (4) bean seeds infested with fourth instar A. obtectus and a drop of honey, both renewed weekly; (5) uninfested bean seeds, added one time at the beginning of the experiment; or (6) control without food source. The number of surviving parasitoids was counted daily. Each treatment was repeated six times, resulting in 30 parasitoids per treatment and species. Progeny production. Upon emergence, female and male parasitoids were kept together for 16 24 h to allow for mating. Subsequently, each female was placed in a vial with eight beans containing approximately 20 fourth instars. The following food supplements were tested: (1) a drop of honey, renewed weekly; (2) a mature sugarcane stem piece (approx. 1 cm 1 cm 0.5 cm), added one time at the beginning of the experiment; or (3) control without food supplement. Beans were changed daily and parasitoids were provided with new unparasitized fourth instars until they died. Parasitized beans were kept in individual vials for 30 days to count the emerging parasitoids and bruchids. Parasitoid females that did not produce offspring or escaped during the experiment were not considered. Every treatment was repeated with 30 females. To obtain data with direct relevance to biological control, we assessed the number of progeny produced rather than fecundity. As a consequence our study does not reveal possible differential mortality during larval development under different treatment regimes. We measured the lifetime progeny production, i.e., the progeny that one female produces over the course of its life, and the cumulative progeny produc-

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TABLE 1 Mean Longevity of Dinarmus basalis, Anisopteromalus calandrae, and Heterospilus posopidis Females Kept with Different Food Sources
D. basalis Food sources Infested beans and honey Honey Sugarcane Infested beans Uninfested beans No food source
a

A. calandrae Mean a 64.4a 23.0b 22.0b 23.7ab 12.3c 15.5c Range 365 1390 215 418 513 613 Mean a 40.7a 49.8a 10.4b 10.3b 10.1b 10.4b

H. prosopidis Range 622 1021 721 315 1018 719 Mean a 14.6a 16.7a 16.1a 11.3b 14.6a 15.7a

Range 1999 18113 1427 1535 518 720

In each column, means followed by different letters are signicantly different according to Dunns method ( P 0.05).

tion, i.e., the progeny that one female produces daily, recorded over its lifetime. Data analysis. For statistical analysis of longevity and mean lifetime progeny production, we used the Friedman repeated-measures analysis of variance on ranks. To test for differences between the median values, we used Dunns method. For statistical analysis of cumulative progeny production, we used polynomial regression analysis.
RESULTS

Longevity. When kept without food sources, D. basalis and H. prosopidis both lived approximately 50% longer than A. calandrae (Table 1). Food sources signicantly inuenced the longevity of all species tested. D. basalis had the longest average lifespan when kept with infested beans plus honey. This lifespan was three times as long as that of individuals kept with honey, sugarcane, or infested beans. D. basalis kept with uninfested beans or without food source had a signicantly shorter lifespan than the individuals in other treatments. The lifespan of A. calandrae kept with infested beans plus honey and with honey alone was four to ve times as long as that of individuals kept with sugarcane, infested beans, uninfested beans, or no food source. Unlike in D. basalis, there was no signicant difference

between the treatment with honey and that with honey plus host larvae for A. calandrae. The lifespan of H. prosopidis kept with infested beans was signicantly shorter than that with the other treatments. Lifetime progeny production. Of the three species investigated, D. basalis showed the highest mean lifetime progeny production, twice as high as that of H. prosopidis and seven times as high as that of A. calandrae (Table 2). Food supplements had a signicant effect on the progeny production of all species tested. D. basalis females kept with honey produced signicantly more offspring than females deprived of food. No signicant differences were detected among the other treatments. Both A. calandrae and H. prosopidis had signicantly higher progeny production when kept with honey than with sugarcane or no food supplements. Neither of the three species showed a signicant difference between the treatment with sugarcane and the treatment without food supplements (Table 2). Cumulative progeny production. D. basalis laid eggs during its entire lifetime (Fig. 1A). The majority of the eggs were laid in the rst 10 days after adult emergence. The highest average offspring production in 1 day was 2.7 (honey), 2.5 (sugarcane), and 2.2

TABLE 2 Mean Lifetime Progeny Production of Dinarmus basalis, Anisopteromalus calandrae, and Heterospilus prosopidis Females Kept with Different Food Supplements
D. basalis Range Honey Sugarcane No food supplement
a

A. calandrae Mean a 28.0a 23.2ab 18.7b Range 212 17 16 Mean a 6.6a 2.4b 2.6b Range 126 116 216

H. prosopidis Mean a 13.5a 8.1b 8.3b

253 241 440

In each column, means followed by different letters are signicantly different according to Dunns method ( P 0.05).

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FIG. 1. Cumulative progeny production of the parasitoid species Dinarmus basalis (A), Anisopteromalus calandrae (B), and Heterospilus prosopidis (C) over their lifetime. Treatments with different food supplements.

(without food supplement). Up to day 25 the cumulative progeny production curve of D. basalis kept with honey and sugarcane did not differ signicantly ( F 2.043, 0.2 P 0.25). Around day 25 the females kept with sugarcane and without food supplement died, while those females kept with honey laid occasional eggs up to day 79 (Fig. 1A), which raised their lifetime progeny production by 32%. A. calandrae also laid eggs during its whole lifetime (Fig. 1B). When kept with honey, the number of eggs that a parasitoid laid during 1 day was nearly constant throughout its lifetime. Kept with sugarcane and without food supplement, the daily rate of offspring production decreased until the females death. The highest average offspring production in 1 day was 0.4 (honey), 0.5 (sugarcane), and 0.9 (without food supplement) (Fig. 1B). H. prosopidis laid eggs over the rst 9 days (Fig. 1C). The highest average offspring production in 1 day was

3.8 (honey), 2.4 (sugarcane), and 2.0 (without food supplement). There was a signicant difference in the daily progeny production between the treatment with honey and the treatments with sugarcane ( F 14.785, P 0.0005) and without food supplement ( F 15.225, P 0.0005), but there was no difference in the reproductive period (Fig. 1C).
DISCUSSION

Based on egg maturation, parasitoids can be classied as synovigenic or proovigenic (Godfray, 1994). Females of synovigenic parasitoids continue to mature and deposit eggs during their adult lifetime. Females of proovigenic species complete oogenesis prior to eclosion and generally are capable of laying their entire egg supply soon after emergence (Thompson, 1999). The two synovigenic species in our experiments, D. basalis and A. calandrae, responded to a honey supple-

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ment with a 1.5- and a 5-fold increase in lifespan, respectively. Given continued egg deposition over their complete lifetimes, such enhanced longevity translates into an increase of mean lifetime progeny production by the factors 1.5 and 2.5, respectively. Under the conditions in our trial, D. basalis engaged in hostfeeding. Females with access to both host hemolymph and honey increased their lifetime 3-fold compared to females feeding on only one of these resources. These two food sources seem to contain complementary nutrients for this species. This corresponds to ndings of Morales-Ramos et al. (1996) for Catolaccus grandis, a parasitoid of the boll weevil. In this species, however, the effect of host-feeding is restricted to egg production as it fails to increase parasitoid longevity (MoralesRamos et al., 1996). For the proovigenic species H. prosopidis, which does not engage in host-feeding, access to adult food sources increases the number of progeny by increasing oviposition rates. Honey likely provides the energy required during oviposition. The lower offspring production in absence of this energy source indicates that parasitoids in these treatments covered their energetic needs through egg resorption. Thompson (1999) suggested that food sources allow proovigenic species to increase their lifetime progeny production through oviposition of the complete egg load. In absence of food sources females may die with nonoviposited eggs in their ovaries. This situation may apply under natural conditions, when the host encounter rate can be low. However, our experiments show that carbohydrate-feeding can also increase lifetime progeny production through an increase in daily offspring production. In our study, the effect of honey on H. prosopidis longevity was lower than expected from previous work (Wa ckers et al., 1998). This difference might be due to seed suitability, parasitoid source, environment, and/or honey composition. Sugarcane seems to be less suitable than honey. Whereas D. basalis could still utilize this carbohydrate source, other species tested did not benet from sugarcane. This is likely due to the fact that the sugar source solidies when the sugarcane stem dries out, reducing food accessibility to the parasitoid (Wa ckers, 2000). A. calandrae is considered inferior to D. basalis as a control agent since it produces a lower number of progeny over its lifetime in bean storage systems. In our studies, the longevity of A. calandrae did not increase in the presence of host larvae. This species is known to engage in host-feeding on Sitophilus granarius L. (Cotton, 1923; Ghani and Sweetman, 1955) and C. chinensis (Wa ckers et al., 1998). Our longevity and progeny production data indicate either that A. calandrae was impaired in locating or reaching the host larvae or that its acceptance of A. obtectus is poor. Several authors (Cotton, 1923; Ghani and Sweetman, 1955; Smith, 1992; Smith and Press, 1992; Wa ckers et al., 1998), the

latter using the same parasitoid strain, reported good performance by A. calandrae on different seed-host systems, as suggested by higher longevity and fecundity of parasitoids. It is unclear which component of the tritrophic systemplant, pest, or parasitoid strain contributes to the low effectiveness of A. calandrae in our system. However, our studies demonstrate conclusively that A. calandrae would be unsuitable for the control of A. obtectus on P. vulgaris L. var. Diacol-Calima seeds. Based on our studies, the pteromalid parasitoid D. basalis appears to be a promising candidate for biological control of A. obtectus in stored beans. Under comparable conditions it produced consistently more progeny than A. calandrae and H. prosopidis. Furthermore, the fact that it had the longest lifetime under nearly all conditions should give D. basalis a competitive advantage over H. prosopidis. In the eld, A. obtectus scatters oviposition over a period of approximately 2 to 3 weeks. As the susceptible fourth instar of the bean weevil is available during 4 to 5 days (CIAT, unpublished records), parasitoids introduced at the time of storage have to cover a period of up to 4 weeks. Our data show that only D. basalis reaches sufcient longevity and progeny production to cover this entire period, especially when used in combination with suitable food sources.
ACKNOWLEDGMENTS
Financial support was provided by the Swiss Centre for International Agriculture (ZIL), ETH Zu rich. We thank Jose Flower Valor for assistance with the experiments. We are grateful to Dr. Hainan Gu for helpful comments on the manuscript.

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