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Conservation Biological Control of Rosy Apple Aphid, Dysaphis Plantaginea (Passerini), in Eastern North America

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Conservation Biological Control of Rosy Apple Aphid, Dysaphis Plantaginea (Passerini), in Eastern North America COMMUNITY AND ECOSYSTEM ECOLOGY Conservation Biological Control of Rosy Apple Aphid, Dysaphis plantaginea (Passerini), in Eastern North America 1 2 M. W. BROWN AND CLARISSA R. MATHEWS Environ. Entomol. 36(5): 1131Ð1139 (2007) ABSTRACT Because of the potentially serious damage rosy apple aphid, Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), can cause to apple fruit and branch development, prophylactic insecticides are often used for control. If biological control could be relied on, the amount of pesticide applied in orchards could be reduced. This study examined biological control of rosy apple aphid in eastern West Virginia and the potential for enhancement through conservation biological control, in particular, the effect of interplanting extraßoral nectar-bearing peach trees. By 20 d after Þrst bloom, only 2% of fundatrices initially present survived to form colonies based on regression of data from 687 colonies. Exclusion studies showed that many of the early colonies were probably destroyed by predation; the major predator responsible seemed to be adult Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Mortality before apple bloom was most important in controlling rosy apple aphid population growth but by itself is not sufÞciently reliable to prevent economic injury. Interplanting of extraßoral nectar-bearing trees did not increase biological control, and interplanting with 50% trees with extraßoral nectar glands reduced biological control. The number of leaf curl colonies in the 50% interplanted orchards was lower than in monoculture orchards, suggesting a preference of alate oviparae for more diverse habitats, supporting the resource concentration hypothesis but not at a level sufÞcient to prevent injury. Predation and parasitism after the formation of leaf curl colonies was not adequate to control rosy apple aphid populations. KEY WORDS interplanting, extraßoral nectar, Harmonia axyridis, Malus x domestica, Prunus persica Habitat management to increase conservation biolog- chogramma minutum (Hymenoptera: Trichogramma- ical control has been a popular topic in recent years tidae) in the laboratory (Shearer and Atanassov 2004) (Barbosa 1998, Landis et al. 2000). It has been rela- and the residence time of Chrysoperla plorabunda tively easy to show that by adding alternate food re- (Fitch) (Neuroptera: Chrysopidae) on almond, Prunus sources to a system, the abundance of predators and amygdalus Batsch, in the Þeld (Limburg and Rosenheim parasitoids can be increased (Nentwig 1988, White et 2001). Interplanting trees bearing extraßoral nectaries to al. 1995, MacLeod 1999, Nicholls et al. 2001). Showing manipulate biological control in apple orchards has yet an impact on biological control, although more difÞ- to be tested. cult, has been shown (Baggen and Gurr 1998, Ste- The rosy apple aphid, Dysaphis plantaginea (Passe- phens et al. 1998, Carmona and Landis 1999). In apple rini) (Homoptera: Aphididae), is a major pest of apple [Malus x domestica (Borkh.)] orchards, several re- in North America and Europe (Hull and Starner 1983, searchers have tested the potential for companion Hemptinne et al. 1994). Rosy apple aphids spend the plants to increase biological control (Bugg and Wad- winter as eggs on apple, the primary host. Egg hatch dington 1994, Wyss 1995, Stephens et al. 1998, Brown coincides with apple bud break in early spring (Hull and Glenn 1999, Jenser et al. 1999, Bostanian et al. and Starner 1983). The Þrst generation or two are 2004). Interplanting species of fruit trees with extra- exposed on apple buds and expanding leaves, but by ßoral nectaries into apple orchards has also been sug- the time trees bloom, the leaves begin to curl, thus gested (Brown and Mathews 2005). Mathews et al. providing protection to the remaining generations. (2007) showed that extraßoral nectaries can increase There are Þve to seven generations on apple in the biological control of oriental fruit moth [Grapholita spring and early summer (Baker and Turner 1916), molesta (Busck) (Lepidoptera: Tortricidae)] in peach with migration to the secondary host, Plantago spp., (Prunus persica Batsch). Extraßoral nectar from peach especially P. lanceolata L. (Blommers 1999), occurring also has been shown to increase Þtness of Tri- from mid-May through June. The aphids return to apple in late summer to early fall, where there is a 1 Corresponding author: USDAÐARS, Appalachian Fruit Re- sexual generation that produces oviparous females. search Station, 2217 Wiltshire Rd., Kearneysville, WV 25430 (e- Injury to apple can occur by deformation of growing mail: [email protected]). 2 Shepherd University, Institute for Environmental Studies, 35 shoots and fruit that develop on those shoots through Snyder Hall, Shepherdstown, WV 25443. the secretion of plant hormone-mimicking com- 1132 ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 5 pounds in the aphidsÕ saliva (Parrott et al. 1919). The chards had 50% of the trees as peach (ÔLoring/LovellÕ) rosy apple aphid is a difÞcult pest to control in all but or sweet cherry, Prunus avium L., all having extraßoral the Þrst few generations because of the protection nectaries; and 50% apple (ÔGranny Smith/EMLA 26Ј provided by the tightly curled leaves in which it feeds and ÔRoyal Empire/M9/EMLA 111Ј) or pear, Pyrus (Blommers 1999). Although chemical control can be communis L. The paired monoculture for these two effective, it must be applied before the formation of interplanted orchards only had a mixture of the two curled leaves (Hull and Starner 1983, Hemptinne et al. apple species. These four orchards were planted in 1994). April 1997 and each was 0.5 ha in size. The other Recently there have been several studies on the interplanted orchard had 9% peach trees (ÔCrimson biological control of rosy apple aphid in apple or- RocketÕ on its own roots) and the apple cultivars chards. In Europe, the most abundant natural enemies Enterprise/EMLA26 and Liberty/EMLA26. The in the spring have been the predators Episyrphus bal- paired monoculture had the two apple cultivars and teatus (DeGeer) (Diptera: Syrphidae), Adalia bipunc- was separated from the interplanted orchard by Þve tata L. (Coleoptera: Coccinellidae), and Aphidoletes apple trees. These two orchards were planted in April aphidimyza (Rondani) (Diptera: Cecidomyiidae) 2002 and each was 0.15 ha in size. (Wyss et al. 1999b, Min˜ arro et al. 2005). Both E. bal- Four studies were done to evaluate the effect of teatus and A. bipunctata were effective in reducing interplanting on biological control of rosy apple aphid rosy apple aphid populations in Þeld cages (Wyss et al. and to identify the primary species involved. Colony 1999b), but none of the predators provided sufÞcient abundance estimates were made to compare the abun- control in orchards of northwest Spain (Min˜ arro et al. dance of colonies in apple monoculture orchards with 2005). Habitat manipulation in the form of ßowering abundance in orchards interplanted with 50% peach. companion plant strips was effective in reducing rosy Nondestructive sampling was used to track the fate of apple aphid populations by increasing predation rates cohorts of colonies from egg hatch to the formation of in the spring and fall (Wyss 1995). Augmentative re- leaf-curling to estimate early spring population devel- lease of larval A. bipunctata in early spring (Wyss et al. opment. An exclusion study was done to separate the 1999a) and autumn (Kehrli and Wyss 2001) has also effects of predators from other possible population shown positive results. It was suggested that the plant- regulating factors during the early egg hatch to leaf- ing of rowan trees (Sorbus aucuparia L.) could in- curl colony stage. Destructive sampling was done after crease biological control of rosy apple aphids by in- leaf curling began to estimate the possible impact of creasing the abundance of the parasitoid Ephedrus biological control in these larger, protected colonies persicae Froggatt (Hymenoptera: Braconidae) by pro- and identify natural enemies involved. viding the alternate, congeneric host Dysaphis sorbi Colony Abundance. On 13Ð14 May 1998 and 11Ð14 Kaltenbach (Bribosia et al. 2005). May 2001, all rosy apple aphid colonies (leaf curl The predator Harmonia axyridis Pallas (Coleoptera: stage) on all apple trees in the two 50% interplanted Coccinellidae) has been dominant in eastern North orchards and the two paired monocultures were American apple orchards since 1995 (Brown and counted. All shoots or ßower clusters with curled Miller 1998). This coccinellid is the most effective leaves from rosy apple aphid feeding were counted predator of spirea aphid, Aphis spiraecola Patch (Ho- without determining if aphids were present to include moptera: Aphididae), in West Virginia (Brown 2004). all active and inactive colonies. Adult H. axyridis were found to be the most effective Colony abundance data were analyzed witha2by predator in controlling spirea aphid because it arrives 4 ␹2 because of the lack of normality in the distribution early during the aphid colonization phase on apple of colony counts (a large number of zero counts re- and is very mobile and voracious (Brown 2004). This sulted in a truncated distribution). The variable used study was conducted to assess the adequacy of bio- for analysis was number of rosy apple aphid colonies logical control of rosy apple aphid populations in east- per 100 trees to standardize for the different number ern North American apple orchards and the potential of apple trees in each orchard (n ϭ 114Ð140).
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