Sugar feeding by the aphid parasitoid Binodoxys communis: How does honeydew compare with other sugar sources?
Introduction
Many insect parasitoids are obligate consumers of plant-derived foods, including carbohydrate-rich solutions such as nectar and homopteran honeydew (Wäckers, 2005). Although sugar sources are largely used to cover energetic needs (Jervis et al., 1993; Steppuhn and Wäckers, 2004), parasitoids can benefit in multiple ways from sugar feeding. Aside from enhancing longevity and fecundity (e.g., Heimpel et al., 1997; Lewis et al., 1998; Wäckers, 2001; Costamagna and Landis, 2004; Winkler et al., 2006), carbohydrate consumption also affects other aspects of reproductive success (see Azzouz et al., 2004). Through these effects, availability of sugar sources can potentially be important in host-parasitoid population dynamics (Krivan and Srivot, 1997; Wäckers, 2003), and could play a role in herbivore suppression in agro-ecosystems (Stapel et al., 1997; Baggen and Gurr, 1998; Baggen et al., 1999; Heimpel and Jervis, 2005; Olson et al., 2005).
Floral nectar, extra-floral nectar, and honeydew are widely available in the field and regularly exploited by parasitoids (Elliott et al., 1987; Idoine and Ferro, 1988; Gilbert and Jervis, 1998; Jervis, 1998; Singh et al., 2000; Heimpel et al., 2004a; Lee et al., 2006). However, the suitability of food hinges on species-specific degrees of gustatory acceptance and metabolization of consumed compounds (Ferreira et al., 1998; Baggen et al., 1999; Olson et al., 2000; Hausmann et al., 2005; Wäckers, 2005; Winkler et al., 2005; Chen and Fadamiro, 2006). The value of honeydew as a food source also needs to be better understood. While there is evidence that, for most parasitoids, honeydew represents an inferior sugar source compared to nectar, sugar solutions and honey, a recent analysis of the literature supports the hypothesis that parasitoids of honeydew-producing hosts are better able to use honeydew than are parasitoids that attack hosts not producing honeydew (Wäckers et al., in press).
Sugar feeding substantially affects sugar, glycogen, and lipid levels of parasitoids (e.g., Olson et al., 2000; Lee et al., 2004; Fadamiro and Chen, 2005; Chen and Fadamiro, 2006). In contrast to lipids (which apparently cannot be synthesized de novo by Hymenoptera, Giron and Casas, 2003), carbohydrate (sugar, glycogen) levels consistently increase upon consumption of sugar-rich foods and are considered indicatory of parasitoid nutritional status (Fadamiro and Heimpel, 2001; Lee et al., 2004). As fructose levels are typically very low in unfed insects, this sugar has clear potential value as a marker for sugar feeding (van Handel, 1984; Olson et al., 2000). Certain biochemical assays, e.g., anthrone tests, have been developed to characterize carbohydrate metabolism (Jervis et al., 1992; Heimpel et al., 2004a). These assays have yet to be fine-tuned for minute arthropods such as aphidiine wasps, although simpler ‘qualitative’ cold anthrone tests that can determine whether an insect has fed upon sugar or not have been used for fairly small parasitoids (Heimpel et al., 2003, Heimpel et al., 2004a; Heimpel and Jervis, 2005; Jepsen et al., 2007).
Until recently, homopteran-synthesized honeydew sugars were thought a reliable tool for identifying honeydew consumption in field-collected insects (Jervis et al., 1992, Jervis et al., 2004; Heimpel et al., 2004a). However, Wäckers et al. (2006) and Hogervorst et al. (2007) found that certain parasitoids synthesize common honeydew saccharides that were previously considered to be ‘signature sugars’. This stresses a need to assess the indicatory value of these sugars for parasitoids that consume both honeydew and nectar, such as aphid parasitoids (Hågvar and Hofsvang, 1991; Azzouz et al., 2004).
Within the context of classical biological control, an in-depth assessment is needed for the effects of non-host foods on natural enemy fitness, efficacy and ultimately the likelihood of establishment (Gurr and Wratten, 1999; Wäckers, 2003; Van Lenteren et al., 2006; but see also Fadamiro and Chen, 2005). Data on parasitoid nutritional ecology could also be indicatory of non-crop habitat associations and aid in predicting non-target effects at the landscape level (Costamagna and Landis, 2004). Classical biological control is in progress against the soybean aphid, Aphis glycines, an invasive species from Asia that is as a destructive pest in US soybean production (Heimpel et al., 2004b; Ragsdale et al., 2004). A Chinese strain of Binodoxys communis (Gahan) (Hymenoptera: Braconidae) was identified for release as it achieves high levels of parasitism of A. glycines, while maintaining a comparatively narrow host range (Desneux et al., unpublished data; Wyckhuys et al., 2007a, Wyckhuys et al., 2007b; Wyckhuys and Heimpel, 2007). During the summer of 2007, the first releases of this parasitoid were conducted in the United States.
The objectives of this study were fourfold: (1) quantify gustatory acceptance of honeydew, honey, and sucrose solution; (2) investigate the suitability of these sugars as food sources for B. communis; (3) determine carbohydrate metabolism of B. communis under various feeding regimes; and (4) examine the value of A. glycines honeydew sugars as ‘signature sugars’ by establishing the sugar spectrum of A. glycines honeydew and quantifying changes in the overall sugar spectrum of B. communis following consumption of honeydew, honey or a sucrose solution.
Section snippets
Insect cultures
A Chinese strain of B. communis was initiated from collections by K. Hoelmer, K. Chen, W. Meikle, and L.A. Pin in late August 2002 in the Chinese province of Heilongjiang. This strain was maintained at the USDA-ARS Beneficial Insect Introduction Research Laboratory in Newark, Delaware, and moved to the Minnesota Department of Agriculture/Minnesota Agricultural Experiment Station (MDA/MAES) Quarantine Facility in St. Paul, MN, USA, in 2003. The parasitoid colony in Minnesota was initiated from a
Gustatory acceptance
The duration of a single feeding bout differed significantly among the various foods (ANOVA, F3.96=20.350, P<0.001). Female B. communis fed longest on honey, and the least amount of time on water droplets (Fig. 1).
Parasitoid longevity
Access to water had a significant and positive effect on B. communis longevity (χ2=71.79, df =1, P<0.001), as did diet (χ2=109.09, df=1, P<0.001). However, no significant effect was recorded for sex (χ2=0.08, df=1, P=0.778). Significant interactions were obtained for sex and access to
Discussion
Insects can vary considerably with respect to the range of nectar and honeydew sugars they can utilize (Wäckers, 2005). The soybean aphid parasitoid, B. communis gains a nutritional benefit from feeding on honeydew, sucrose, and honey. However, this species attains a considerably longer lifespan on honey or sucrose than on honeydew. Although B. communis females feed for similar amounts of time on wet honeydew as on sucrose, honeydew-fed individuals have consistently lower nutrient profiles than
Acknowledgments
We would like to thank Laura Stone and Jo Barta for help in parasitoid rearing, and Erika Commers for help with A. glycines colony maintenance. We are grateful to Kim Hoelmer for co-ordinating the collection of B. communis, and Keith Hopper for culturing B. communis before we brought it to Minnesota. This work was funded in part by a multi-state USDA-RAMP project, in part by the North Central Soybean Research Council, and in part by the Minnesota Agricultural Experiment Station.
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