Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Abstract

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.

Introduction

Insect natural enemies that are transported by host or non-host organisms can contribute to biological control. For example, entomopathogenic nematodes are distributed by non-host organisms, ensuring a broad geographical coverage and associated control of multiple insect pests (Eng et al., 2005, Campos-Herrera et al., 2006). Phoretic egg parasitoids belonging to the families Trichogrammatidae and Scelionidae attach to mobile adult stages of insect pests and consequently enhance geographic distribution of the parasitoid (Arakaki et al., 1996, Buschman and Whitcomb, 1980, Fatouros et al., 2005, Orr, 1988). The dispersal of parasitoids through flight of their host could aid the recovery of natural enemy populations in frequently disturbed or highly-dynamic systems (Rauwald and Ives, 2001), and likely contributes to more effective arthropod biological control, especially in the case of highly mobile insect pests.

One highly mobile pest is the soybean aphid, Aphis glycines, a key insect pest of soybeans in North America (Ragsdale et al., 2004, Wu et al., 2004b). Although A. glycines was first reported in the North-Central US in 2000, it has rapidly spread throughout the principal soybean production regions of the US and Canada (Ragsdale et al., 2004, Ragsdale et al., 2007, Venette and Ragsdale, 2004). The spread of A. glycines in North America is facilitated by both passive and active flight (Venette and Ragsdale, 2004, Zhang et al., 2008). While the distance flown by A. glycines is not known, the existence of long-distance flight is indicated by frequent capture of winged A. glycines far from either soybeans or the overwintering host of A. glycines, Rhamnus spp. shrubs (G.E. Heimpel, unpublished). Other migratory aphids can be carried by the wind for up to hundreds of kilometers (Elton, 1925, Kring, 1972, Irwin and Thresh, 1988, Riley et al., 1995, Zhu et al., 2006).

Classical biological control is currently being implemented against A. glycines (Heimpel et al., 2004b) including releases of the exotic parasitoid Binodoxys communis (Hymenoptera: Aphidiinae) in several US states (Wyckhuys et al., 2007). Additionally, other aphid parasitoids including various Aphelinus species (Hymenoptera: Aphelinidae) have either been experimentally released against soybean aphid or are being considered for potential future releases (Heimpel et al., 2004a, Wu et al., 2004a, Heraty et al., 2007, Wyckhuys et al., 2007). For future releases, priority will be given to Aphelinus spp. with narrow host range, high A. glycines control potential and presence of selected behaviors that may aid their subsequent establishment or geographical spread.

Field-caught alate aphids are frequently infested with aphid pathogens or immature parasitoids, with parasitized alates yielding viable parasitoid mummies (Feng et al., 2004, Feng et al., 2007, Chen et al., 2008). Koinobiont parasitoids, including all aphid parasitoids, allow movement and growth of the host upon parasitism, potentially permitting flight of parasitized aphids over considerable distances provided that the alate stage bears parasitoid offspring (Feng et al., 2007, Chen et al., 2008). However, certain aphid parasitoids disrupt the formation of host wings, impeding subsequent host flight (Christiansen-Weniger and Hardie, 1998, Christiansen-Weniger and Hardie, 2000, Rauwald and Ives, 2001, Demmon et al., 2004). Little is known about how A. glycines parasitism affects subsequent aphid wing development and flight performance.

Here, we investigate the effects of parasitism by Aphelinus varipes on flight capacity of alate A. glycines using a laboratory flight mill (Zhang et al., 2008, Zhang et al., 2009). We determine the effect of parasitism on aphid wing development and we compare flight performance of alate A. glycines that were parasitized at different times during their development.