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Biological Control 43 (2007) 7884 www.elsevier.

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Eects of a plant resistance protein on parasitism of the common bean bruchid Acanthoscelides obtectus (Coleoptera: Bruchidae) by its natural enemy Dinarmus basalis (Hymenoptera: Pteromalidae)
Guido Velten a, Anja S. Rott
a

a,*

sar Cardona b, Silvia Dorn , Ce

Institute of Plant Science, Applied Entomology, ETH Zurich, Schmelzbergstrasse 9/LFO, 8092 Zurich, Switzerland b Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia Received 14 March 2007; accepted 9 May 2007 Available online 17 May 2007

Abstract Dinarmus basalis is an important larval parasitoid of the bean bruchid Acanthoscelides obtectus, a major pest of stored legumes throughout the tropical belt. The use of a combination of dierent natural resources for protecting stored beans from attack by A. obtectus by non-toxic means is considered a promising alternative to the use of traditional chemical insecticides. The seed storage protein arcelin causes sub-lethal eects on the development of A. obtectus that are favorable for biological control. The present study aimed to validate the mutual compatibility between the plant resistance factor arcelin and the biological control candidate D. basalis. Development and performance of D. basalis attacking A. obtectus on beans with dierent relative arcelin concentrations were investigated in bioassays. The parasitoid accepted hosts on all tested bean lines, irrespective of the relative concentration of arcelin. No indications were found for an eect of arcelin on parasitoid ospring tness. The parasitoids capability to suppress bruchid development was investigated in a follow-up experiment mimicking the temporal complexity of bruchid infestations in the eld. Bruchid suppression was signicantly higher on arcelin containing bean lines than on arcelin-free cultivars. Our ndings demonstrate the potential of the candidate biological control agent D. basalis to contribute to a marked reduction of bruchid emergence in a proposed two-component integrated pest management system. 2007 Elsevier Inc. All rights reserved.
Keywords: Parasitoid; Bruchidae; Zabrotes subfasciatus; Storage; Phaseolus vulgaris; Arcelin; Biological control; Integrated pest management

1. Introduction Dry beans (Phaseolus vulgaris L.) are among the most important food legumes worldwide, providing one of the primary sources of dietary protein, particularly in developing countries (Cardona, 2004). Nearly, 90% of the worldwide dry bean production is cultivated in low-income countries (FAOSTAT, 2004), with Latin America being the centre of bean domestication. Almost 80% of dry bean production occurs on small-scale farms (Cardona and Kornegay, 1999). The common bean bruchid Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae) is a major
*

Corresponding author. Fax: +41 44 632 1171. E-mail address: anja.rott@ipw.agrl.ethz.ch (A.S. Rott).

post-harvest pest of dry beans throughout the tropics and parts of the subtropical belt. Initial infestation of common beans by A. obtectus occurs in the eld shortly before harvest (Schmale et al., 2002). However, this bruchid is able to go through multiple generations within storage. After 16 weeks storage total losses of harvest were reported (Schmale et al., 2002). Because of the destructive power of the bruchids, many farmers sell their crop immediately after harvest, when market prices are low, even without storing seeds for the next sowing and family consumption (Schmale et al., 2006). Post-harvest losses are particularly critical, as all investments for growing the crop have already been made at this stage. An integrated pest management for safe storage is expected to contribute to the stabilization of market prices (van Schoonhoven, 1977) and hence

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to generate a better income for small-scale farmers, and to prevent human under- and malnutrition. Several control measures have been explored to protect stored legumes with non-toxic means, including the use of plant resistance factors (Appleby and Credland, 2004; Ignacimuthu et al., 2000; Schmale et al., 2003), botanical biocides (Boeke et al., 2004; Koona and Dorn, 2005; Raja et al., 2001) and biological control (Gauthier et al., 1999; Sanon et al., 1998; Schmale et al., 2006). Potential plantderived antibiosis factors that could limit seed predation by herbivores in P. vulgaris comprise seed storage proteins such as lectins (Janzen et al., 1976). The storage protein arcelin is a lectin homologous protein which has been identied from wild Mexican bean varieties as being highly resistant to bean weevils and was then successfully bred into cultivated bean lines (Cardona et al., 1990). Seven allelic arcelin variants with dierential value for insect resistance have been reported so far, with arcelin-1, which is expressed by the genotypes used in the present study, achieving high resistance levels (Acosta-Gallegos et al., 1998; Cardona et al., 1990; Hartweck et al., 1997). Arcelin causes toxic eects on the Mexican bean weevil Zabrotes subfasciatus (Boheman) (reviewed by Cardona and Kornegay, 1999), another important bean bruchid pest (Osborn et al., 1988), and sub-lethal eects on A. obtectus. The eects on A. obtectus alone are not sucient to control this devastating pest species, nevertheless they might be used as a tool in integrated pest management (Schmale et al., 2003). Combinations of mutually compatible natural resources for pest control are considered promising alternatives to traditional chemical insecticides (Copping and Menn, 2000; Cortesero et al., 2000; Dorn, 1998; Schmale et al., 2003). Research in the eld covers a broad range from synergistic or competitive interactions of pathogens, antimetabolites or, e.g. via genetic engineering, modulated plant attributes with parasitoids or predators (Flinn et al., 2006; Lord, 2006; Palyvos et al., 2006; Romeis et al., 2006). The combination of compatible control elements that complement each other is a desirable strategy in pest management, especially to control multi-infestations by several pest species (Flinn et al., 2006). Recent studies indicate that the combination of a plant-resistance factor and biological control by the parasitic wasp Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) is a promising integrated approach to control A. obtectus (Schmale et al., 2001, 2003). Bean genotypes containing arcelin are typically ranked on the basis of their Indices of Susceptibility (IS) (Dobie, 1974) to Z. subfasciatus (CIAT, 1989), with lower indices being correlated to higher relative arcelin concentrations (Cardona et al., 1990). There are some indications for a positive correlation between the indices of susceptibility to Z. subfasciatus and those to A. obtectus from a study using dierent arcelin variants (Hartweck et al., 1997). Arcelin not only prolongs the development of A. obtectus but also extends the period of adult emergence, thus contribut-

ing to a higher variation of host stages present at the same time (Schmale et al., 2003; Velten et al., 2007). These factors might enhance parasitoid eciency, due to an increase in the time window during which A. obtectus larvae are susceptible to attacking parasitoids (Schmale et al., 2003, 2005, 2006). The present study aims to validate the compatibility between the host plant resistance factor arcelin and biological control by D. basalis in an integrated pest management approach. Therefore, experiments were conducted to assess whether arcelin aects the development of D. basalis and/or its capability in suppressing bruchid development. 2. Materials and methods 2.1. Beans Phaseolus vulgaris L. (Leguminosae) genotypes with different arcelin-based resistance levels (RAZ-lines) were used. All genotypes have been bred and cultivated by the Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia following the methodology described by Cardona et al. (1990). All seven chosen RAZ-lines originate from crossing the same parental lines, and share a similar seed colour (rojo) and a similar seed weight (ranging from 23 to 29 g/100 seeds). Their arcelin-based resistance, expressed by the IS value, ranged from high to intermediate (RAZ-91: IS = 3.9; RAZ-88: IS = 1.8; RAZ-85: IS = 1.3; RAZ-94: IS = 0.9; RAZ-77: IS = 0; RAZ-84: IS = 0.8; RAZ-74: IS = 1.8). Two commonly used arcelin-free cultivars [P. vulgaris var. Diacol-Calima (Calima): IS = 10.1 and var. ICA-Pijao (Pijao): IS = 10.6] served as control. For insect rearing we used red kidney beans (RKB) purchased from a local retailer in Zurich, Switzerland. All beans were kept in a climatic room at 4 C to conserve seed quality. 2.2. Insect species The experiments were carried out with D. basalis and A. obtectus. The strains were maintained at ETH Zurich, Switzerland and both originated from locally collected colonies from the Bean Entomology Laboratory at CIAT, Cali, Colombia, and were periodically refreshed. Cultures were maintained on red kidney beans (RKB) purchased from a local retailer in Zurich, Switzerland, in climatic chambers at 26 C, 80% r.h. and a 12:12 light regime. Bruchid eggs were obtained by sieving beans on which bruchids had deposited eggs for 1 day. Dinarmus basalis is a solitary ectoparasitoid, which attacks several species of Bruchidae (Coleoptera). The female drills through the seed coat and lays a single egg on the host, which develops to adult around 18 days depending on abiotic factors and host quality (Gauthier et al., 1997, 2002; Schmale et al., 2001, 2005, 2006). Adults do not need to feed obligatorily, but as many other

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synovigenic parasitoids, D. basalis females feed on potential hosts. The female discriminates between host larvae on basis of host quality, i.e. more female eggs are laid on larger host if dierent types of host are available, while suboptimal larvae are either used for male egg deposition or host feeding, as shown for many hymenopteran parasitoids (Gauthier et al., 2002; Heimpel and Rosenheim, 1998; Schmale et al., 2001). This host feeding behavior is of particular importance in the context of biological control. 2.3. Experimental conditions All experiments were carried out within climatic chambers (Conviron, Controlled Environment Ltd., Winnipeg, Canada) at a temperature of 26 C, 80% relative humidity and 12:12 L:D. 2.4. Parasitoid ospring tness and sex ratio In order to assess potential eects of the relative arcelin concentration on ospring tness and sex ratio of D. basalis, 50 seeds of each bean line were infested with one hundred 1-day-old A. obtectus eggs in 100 ml glass jars. When beetle larvae reached the favored fourth instar, a pair of mated 2- to 6-day-old D. basalis was introduced. After the maximum bruchid development time (i.e. 50 days) the numbers of male and female parasitoid ospring were recorded and the left hind tibia length and head width of female ospring were assessed as indicators of progeny tness. Additionally, the number of emerged bruchids was assessed. Ten replications were conducted per bean line. 2.5. Parasitoid performance in temporally complex bruchid infestations For the following experiment we chose the bean lines RAZ-77 and RAZ-85, which in experiment 2.4 suered high and low damage caused by bruchids (i.e. number of emerged adults), respectively. Both standard cultivars, Calima and Pijao, were used as control. Fifty seeds of each bean line were placed in 100 ml glass jars. To mimic the temporal complexity of natural eld infestations at harvest (Schmale et al., 2002), beans were consecutively infested at day 19, 12 and 5 before the start of the experiment with 29, 57 and 14 1-day-old eggs of A. obtectus, respectively (Schmale et al., 2003). Before each new infestation the beans were carefully mixed to achieve random distribution of host larvae. At the beginning of the experiment, three 26 day old mated pairs of D. basalis were introduced to each test jar. To increase the life expectancy in this situation where the availability of host larvae is temporarily scattered, honey (1 ml of a 1:1 solution) was provided as food supplement (Schmale et al., 2001) in small glass vials (2 ml) lled with cotton and covered with gauze (mesh size 1 mm2). This allowed parasitoids to pass through and feed on the honey, whilst excluding the bruchids. After two bru-

chid generations the number and sex of emerged parasitoid progeny was recorded and all emerged bruchids were counted. Ten replicates were conducted per bean line. 2.6. Data analysis Data were tested for normal distribution (KolmogornovSmirnov test) and homogeneity of variances (Levene test). Where requirements were fullled, dierences were analyzed using a one-way ANOVA followed by multiple comparisons of bean lines with Duncans post hoc test. Otherwise, data were analyzed for dierences using nonparametric KruskalWallis test followed by non-parametric multiple comparisons according to Zar (1999). 3. Results 3.1. Parasitoid ospring tness and sex ratio When D. basalis parasitoids were released on suitable fourth instar A. obtectus host larvae, they were able to develop on all bean lines (Fig. 1a). Although in some samples with arcelin containing seeds fewer parasitoid progeny were recorded as compared to the susceptible controls, the numbers were overall relatively low and no signicant dierence was found for mean progeny between dierent bean lines (KruskalWallis: v2 = 10.95, df = 8, P > 0.20). Overall, the sex ratio of parasitoid progeny was female biased, with the proportion of males ranging from 19% to 45%, except for bean line RAZ-84 (with a proportion of males of 62%). Dierences in mean proportion of male ospring between bean lines were not signicant (KruskalWallis: v2 = 8.48, df = 8, P > 0.38) (Fig. 1a). Measurements of hind tibia length of parasitoid ospring revealed no dierences between bean lines, with the exception of RKB, which yielded female parasitoid ospring with signicant longer hind tibia as compared to those emerging from RAZ-91 (KruskalWallis: v2 = 19.25, df = 8, P < 0.05, Tukey-type non-parametric multiple comparisons: P < 0.01) (Fig. 2a). A similar pattern was found for head width of female parasitoid ospring (Fig. 2b) (KruskalWallis: v2 = 31.83, df = 8, P < 0.001, Tukey-type non-parametric multiple comparisons: P < 0.05). Those individuals that emerged from RKB developed signicantly broader head capsules than those emerging from the arcelin containing lines RAZ-94, RAZ-85, RAZ-88 and RAZ-91. However, no signicant dierences of female parasitoid ospring head capsule width were observed between the susceptible standard cultivar Calima and the arcelin containing RAZ-lines. Adult bruchids emerged from all samples (Fig. 3a). Emergence rate followed a decreasing trend towards higher arcelin-based resistance, with the exception of line RAZ-91. Signicant dierences between arcelin-containing and arcelin-free bean lines were noted for RAZ-85 and RAZ-88, compared to the standards RKB and Calima.

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Mean parasitoid offspring

Male offspring Female offspring

Mean tibia length (mm)


RAZ-85 RAZ-88 RAZ-91

0.9

0.8

0.7

0.6

0 Calima 'RKB' RAZ-74 RAZ-84 RAZ-77 RAZ-94

0.5 0.7

Mean head width (mm)

2.5

0.6

Mean parasitoid offspring

2.0

0.5

1.5

0.4

1.0

0.3
N =17 7 9 3 6 10 5 5 15

RAZ-74

RAZ-84

RAZ-77

RAZ-94

RAZ-85

RAZ-88

0.5

0.0 Calima Pijao RAZ-77 RAZ-85

Bean lines
Fig. 1. (a) Mean number (SE) and sex of ospring of the parasitoid D. basalis emerging from dierent bean lines after one generation of the bruchid A. obtectus. One pair of parasitoids was released on 50 seeds infested with one hundred bruchid eggs at the time host larvae had reached the fourth instar, N = 10. (b) Mean number (SE) and sex of parasitoid ospring emerging from dierent bean lines after two bruchid generations. Three pairs of parasitoids were released on 50 seeds consecutively infested at day 19, 12 and 5 before the start of the experiment with 29, 57 and 14 1day-old eggs, respectively, mimicking the temporal complexity of eld infestations, N = 10.

Fig. 2. (a) Mean hind tibia length (SE) and (b) mean head width (SE) of female ospring of the parasitoid D. basalis emerging from dierent bean lines after one generation of the bruchid A. obtectus. One pair of parasitoids was released on 50 seeds infested with one hundred bruchid eggs at the time host larvae had reached the fourth instar. Dierent letters indicate signicant dierences between bean lines ((a) KruskalWallis: v2 = 19.25, df = 8, P < 0.01, Tukey-type non-parametric multiple comparisons: P < 0.05; (b) KruskalWallis: v2 = 31.83, df = 8, P < 0.001, Tukey-type non-parametric multiple comparisons: P < 0.05).

3.2. Parasitoid performance in temporally complex bruchid infestations The follow-up experiment on parasitoid performance in temporally complex bruchid infestations focused on the bean lines, which suered high and low bruchid damage. Again, the parasitoid D. basalis was able to reproduce on hosts provided in seeds of any of the bean lines, indicating the availability of suitable host stages (Fig. 1b). However, overall a much lower amount of bruchids and wasps developed in these samples. Parasitoid reproduction did not exceed six ospring per sample and thus, was lower than in the rst experiment, in which single pairs of parasitoids were provided with fourth instar host larvae after a single infestation event. Mean parasitoid ospring did not dier between bean lines (KruskalWallis: v2 = 4.08, df = 8, P > 0.25). The mean proportion of male ospring did not

dier signicantly between bean lines (KruskalWallis: v2 = 3.39, df = 8, P > 0.33). The rate of bruchid emergence in this set-up was greatly reduced and interestingly, despite the low parasitism rate, signicantly fewer bruchids emerged from either of the arcelin containing bean lines (RAZ-77 and RAZ-85) as compared with the susceptible controls (Fig. 3b). 4. Discussion The natural storage protein arcelin causes sub-lethal eects to the bruchid A. obtectus (Kornegay and Cardona, 1991; Paes et al., 2000; Schmale et al., 2003). Although it does not prevent beans from bruchid attack, it prolongs immature development of young bruchid larvae and extends the period of adult emergence (Velten et al., 2007). However, potential consequences for the performance of its natural enemy D. basalis were virtually unknown. The present study aims to elucidate the inuence of dierent arcelin-based resistance levels on the larval parasitoid D. basalis and its capability to suppress the bruchid

RAZ-91

Calima

RKB'

82

G. Velten et al. / Biological Control 43 (2007) 7884

100

80

a ab abc bc abc bc c c

ab

60

40

20 RAZ-74 RAZ-84 RAZ-77 RAZ-94 RAZ-85 RAZ-88 RAZ-91 Calima 'RKB'

250 200 150


a

100
b

50 0 Calima Pijao RAZ-77

RAZ-85

Bean lines
Fig. 3. (a) Mean number (SE) of A. obtectus emerging from dierent bean lines after one generation. One pair of the parasitoid D. basalis was released on 50 seeds infested with one hundred bruchid eggs at the time host larvae had reached the fourth instar, N = 10. (b) Mean number (SE) of bruchids emerging from dierent bean lines after two bruchid generations. Three pairs of parasitoids were released on 50 seeds consecutively infested at day 19, 12 and 5 before the start of the experiment with 29, 57 and 14 1-day-old eggs, respectively, mimicking the temporal complexity of eld infestations, N = 10. Dierent letters indicate signicant dierences between bean lines ((a) ANOVA: F = 3.11, df = 8, P < 0.01, Duncan post hoc multiple comparisons; (b) KruskalWallis: v2 = 27.71, df = 3, P < 0.001, Tukey-type non-parametric multiple comparisons).

pest. The results show that when mated female parasitoids are provided with suitable host stages, ospring will develop irrespective of the presence or absence of arcelin in host larval diet. Sex allocation theory predicts that host quality inuences ospring sex ratio as a result of manipulation of egg fertilization by females during the oviposition phase (Charnov et al., 1981). Indeed, Gauthier et al. (1997) showed that D. basalis females which were provided with cowpeas infested by Bruchidius atrolineatus (Pic) adjusted the number of fertilized eggs laid depending on host quality. However, arcelin had no aect on the sex ratio of the parasitoids progeny in the present study, indicating that mothers accepted hosts as suitable irrespective of whether those ingested arcelin or not. Furthermore, an analysis of

the size (i.e. head width and hind tibia length) of female parasitoid progeny as a surrogate for ospring tness demonstrates that the exposition of host larvae to arcelin did not aect the tness of the parasitoid ospring. From that we conclude that arcelin does not have any direct eect on the parasitoids development. In fact, arcelin is thought to be indigestible for bruchids (Minney et al., 1990), and although it disrupts the midgut of Z. subfasciatus, it does not so in A. obtectus and thus does not inltrate the haemolymph (Paes et al., 2000). The ectoparasitoid D. basalis, however, feeds on larval haemolymph, hence it is unlikely that the parasitoid larvae would come in contact with arcelin. Arcelin-containing host larval diet could therefore only indirectly inuence the parasitoids progeny production through its diminishing eect on host larval size. As a result, the decrease of host quality could increase host feeding frequency, shift the parasitoid ospring sex ratio or lower parasitoid ospring size; although, all these consequences would contribute to the alleviation of bruchid development. In contrast, the application of traditional botanical pesticides causes direct negative eects on the parasitoids (Boeke et al., 2003; Sanon et al., 2002), thus disrupting the natural suppression of bruchid pests (Boeke et al., 2003; Sanon et al., 2002; van Alebeek, 1996). The capability of D. basalis to contribute to a signicant reduction of bruchid emergence was proven in an experiment mimicking the temporal distribution of host larvae in natural infestations. Treatments combining biological control and host plant resistance resulted in a highly significant reduced number of bruchids after two generations, compared to the release of parasitoids to samples with arcelin-free seeds. This nding provides evidence for a synergistic eect on bruchid suppression, although only few parasitoid ospring emerged. Low reproductive success of the parasitoid can be explained by the fact that deposition of eggs is inuenced by the age of encountered hosts, and that adult host feeding on suboptimal hosts is a key factor involved in reducing the bruchid population when parasitoids were released on younger host larvae (Schmale et al., 2005). Seeds with arcelin contain a higher variation of host larvae regarding their age and size due to their delayed development (Velten et al., 2007). Our assumption, that this variation in A. obtectus development in arcelin containing seeds would be desirable for biological control by D. basalis, is conrmed in a situation where parasitoids were released to consecutively infested seeds simulating the natural conditions at the time of harvest. Our ndings support the idea that the combination of mutual compatible elements in integrated pest management is a particular valuable strategy to overcome the burden of pest species against which no single method provides adequate control. Acknowledgments We are grateful to Silke Hein, Gerorge E. Heimpel and an anonymous referee for useful comments on a

Emerged bruchids

Emerged bruchids

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