Christina DiFonzo

Landscape diversity enhances biological control of an introduced crop pest in the north-central USA

Arthropod predators and parasitoids provide valuable ecosystem services in agricultural crops by suppressing populations of insect herbivores. Many natural enemies are influenced by non-crop habitat surrounding agricultural fields, and understanding if, and at what scales, land use patterns influence natural enemies is essential to predicting how landscape alters biological control services. Here we focus on biological control of soybean aphid, Aphis glycines Matumura, a specialist crop pest recently introduced to the north-central United States. We measured the amount of biological control service supplied to soybean in 26 replicate fields across Michigan, Wisconsin, Iowa, and Minnesota across two years (2005-2006). We measured the impact of natural enemies by experimentally excluding or allowing access to soybean aphid infested plants and comparing aphid population growth over 14 days. We also monitored aphid and natural enemy populations at large in each field. Predators, principally coccinellid beetles, dominated the natural enemy community of soybean in both years. In the absence of aphid predators, A. glycines increased significantly, with 5.3-fold higher aphid populations on plants in exclusion cages vs. the open field after 14 days. We calculated a biological control services index (BSI) based on relative suppression of aphid populations and related it to landscape diversity and composition at multiple spatial scales surrounding each site. We found that BSI values increased with landscape diversity, measured as Simpsons D. Landscapes dominated by corn and soybean fields provided less biocontrol service to soybean compared with landscapes with an abundance of crop and non-crop habitats. The abundance of Coccinellidae was related to landscape composition, with beetles being more abundant in landscapes with an abundance of forest and grassland compared with landscapes dominated by agricultural crops. Landscape diversity and composition at a scale of 1.5 km surrounding the focal field explained the greatest proportion of the variation in BSI and Coccinellidae abundance. This study indicates that natural enemies provide a regionally important ecosystem service by suppressing a key soybean pest, reducing the need for insecticide applications. Furthermore, it suggests that management to maintain or enhance landscape diversity has the potential to stabilize or increase biocontrol services.

Predators Suppress Aphis glycines Matsumura Population Growth in Soybean

Abstract The soybean aphid, Aphis glycines Matsumura, is an invasive pest of soybean, first discovered in North America in 2000. We studied the ability of the existing predator community in soybean to suppress A. glycines population growth during June–August 2002, in field studies using predator exclusion and sham cages or no-cage controls. Cages were infested with uniform initial densities of A. glycines adults, and subsequent populations of aphids and predators were monitored. After 2 wk, exclusion and sham cages were switched, with aphid and predator density followed for additional 2 wk. The experiment was repeated a second time, allowing observation of predator community response to both low and high density aphid populations over several time periods and stages of soybean development. Cages had minimal effects on temperature, relative humidity, or soybean growth. In contrast, predator communities and aphid populations were strongly affected by cage treatments. In the first trial, the activity of foliar-foraging predators effectively prevented A. glycines population growth maintaining populations below 10 aphids per plant (adult + nymphs) in sham cages, while populations exceeded 200 aphids per plant in exclusion cages. After cage switch, these high A. glycines populations in the former exclusion cages were rapidly colonized and reduced by nearly an order of magnitude within 2 wk by a combination of generalist and specialist predators. The second trial produced qualitatively similar results, but at much lower aphid densities. The most abundant predators in both trials included: Harmonia axyridis Pallas, Orius insidiosus (Say), and Leucopis spp. These studies demonstrate that existing predator communities comprised of a mixture of indigenous and naturalized species can suppress A. glycines population density in soybean. The impact of existing predator communities should be further investigated as a component of A. glycines management in United States soybean production systems.

Resistance to soybean aphid in early maturing soybean germplasm

yellow, and even drop. Other symptoms of direct feeding damage include plant stunting, poor pod fill, reduced Since 2000, the soybean aphid (Aphis glycines Matsumura) has pod and seed counts, smaller seed size, and nutrient become a major pest of soybean [Glycine max (L.) Merr.] in North America. In the USA, there are currently no commercial soybean deficiencies resulting in overall yield and quality reduccultivars with aphid resistance and there are no reported resistance tion (DiFonzo and Hines, 2002). Significant yield loss sources in early maturing soybean germplasm. The objectives of this (8–25%) occurs when the soybean plants are heavily study were to identify sources and types of resistance to soybean aphid infested by the aphid during the early reproductive stage from early maturing soybean germplasm. Over a 2-yr period, 2147 (DiFonzo and Hines, 2002). Honeydew, a sticky subsoybean accessions from maturity group (MG) 0 to III, originally stance excreted by soybean aphids onto the leaves, leads from northern China, were evaluated for aphid resistance in a greento the development of sooty mold, which affects photohouse and in field cages. The plants were hand-inoculated and aphid synthesis and results in yield loss (Baute, 2004). During populations were evaluated 10 d after inoculation. A damage index the feeding process, soybean aphids are capable of trans(0–100%) was calculated for each accession. After 2 yr of evaluation mitting viruses including Alfalfa mosaic virus, Soybean and confirmation in choice tests, four MG III accessions from Shandong province, PI 567543C, PI 567597C, PI 567541B, and PI 567598B, mosaic virus, and Bean yellow mosaic virus. These viwere found to be resistant to the soybean aphid. Two of these accesruses commonly occur together and form a disease comsions, PI 567541B and PI 567598B, possessed antibiosis resistance, plex that leads to plant stunting, leaf distortion and preventing the aphids from reproducing on the plants in a no-choice mottling, reduced pod numbers, and seed discoloration study. PI 567543C and PI 567597C possessed antixenosis resistance. (Glogoza, 2002). These resistant sources can be used to develop commercial cultivars In the USA, soybean aphid research is still in its early with aphid resistance for the North Central states. stages. The aphid was first found in 2000 and annual infestations have been unpredictable (Steffey and Gray, 2004). Insecticides are the only available method of conS is the leading oilseed crop produced and controlling soybean aphids in the USA. Although the use sumed worldwide (Wilcox, 2004). In the past half of insecticides can be a quick and easy way to control century, the USA has been the world’s leading producer. aphids, the ideal time to spray is not well defined. InsecIn 2003, the USA produced 35% (65.8 million Mg) of ticides also have many adverse effects such as killing the world’s total soybean (FAOSTAT, 2004). Soybean beneficial insects, environmental contamination, and inhas many insect pests limiting its production, including creased production costs (Sun et al., 2000). Aphid poputhe soybean aphid. A native to eastern Asia, the soybean lations may resurge when applications of insecticides aphid was not reported in the USA before July 2000. are poorly timed or applied. Developing soybean varieSince then, the insect has rapidly spread to the major ties that are resistant to the aphid is a long-term solution soybean production areas in the USA and Canada to the aphid problem. (Plant Health Initiative, 2004). Outbreaks have been To develop aphid resistant varieties, sources of resissevere in the northern part of the midwestern USA and tance must be identified. Sources of resistance to the in Ontario, particularly in 2001 and 2003. soybean aphid are reported in China. In the late 1980s, Several factors affect soybean aphid outbreaks, intwo highly resistant varieties were found among 181 variecluding environmental conditions, over-wintering sucties evaluated (Fan, 1988). In 1991, resistance was also cess, cultural practices, natural enemies, and the synreported in soybean germplasm in China (Sun et al., 1991). chronization of soybean and aphid development (Wu The type of resistance, antixenosis or antibiosis, was not et al., 1999). The soybean aphid is the only aphid in indicated in these studies. Antixenosis is nonpreference North America that develops large colonies on soybean. of insects for a host plant (Kogan and Ortman, 1978). Plant damage occurs when large numbers of aphids reAntibiosis includes all adverse effects on an insect’s life move significant amounts of water and nutrients as they history after a resistant host plant has been used for feed on leaves and stems, causing leaves to wilt, curl, food (Painter, 1951). Knowing the type of resistance is important to fully understand and utilize resistant accesC. Mensah and D. Wang, Dep. of Crop and Soil Science, Michigan sions in a breeding program. Hill et al. (2004) recently State Univ., East Lansing, MI 48824; C. DiFonzo, Dep. of Entomology, reported three lines with resistance to soybean aphid. Michigan State Univ., East Lansing, MI 48824; R.L. Nelson, USDAPI 71506 (MG IV) has antixenosis and the cultivars ARS, Soybean/Maize Germplasm, Pathology, and Genetics Research Dowling (MG VIII) and Jackson (MG VII) are reported Unit, Dep. of Crop Sciences, 1101 W. Peabody Dr., Univ. of Illinois, Urbana, IL 61801. Received 27 Nov. 2004. *Corresponding author to have antibiosis resistance. (wangdech@msu.edu). In 2002, when this research was initiated, there were no known sources of host plant resistance to soybean Published in Crop Sci. 45:2228–2233 (2005). aphid in the USA. The objectives of this study were to: Crop Breeding, Genetics & Cytology doi:10.2135/cropsci2004.0680

Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans

Top-down regulation of herbivores in terrestrial ecosystems is pervasive and can lead to trophic cascades that release plants from herbivory. Due to their relatively simplified food webs, agroecosystems may be particularly prone to trophic cascades, a rationale that underlies biological control. However, theoretical and empirical studies show that, within multiple enemy assemblages, intraguild predation (IGP) may lead to a disruption of top-down control by predators. We conducted a factorial field study to test the separate and combined effects of predators and parasitoids in a system with asymmetric IGP. Specifically we combined ambient levels of generalist predators (mainly Coccinellidae) of the soybean aphid, Aphis glycines Matsumura, with controlled releases of the native parasitoid Lysiphlebus testaceipes (Cresson) and measured their impact on aphid population growth and soybean biomass and yield. We found that generalist predators provided strong, season-long aphid suppression, which resulted in a trophic cascade that doubled soybean biomass and yield. However, contrary to our expectations, L. testaceipes provided minor aphid suppression and only when predators were excluded, which resulted in nonadditive effects when both groups were combined. We found direct and indirect evidence of IGP, but because percentage parasitism did not differ between predator exclusion and ambient predator treatments, we concluded that IGP did not disrupt parasitism during this study. Our results support theoretical predictions that intraguild predators which also provide strong herbivore suppression do not disrupt top-down control of herbivores.

Probability of Cost-Effective Management of Soybean Aphid (Hemiptera: Aphididae) in North America

ABSTRACT Soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is one of the most damaging pests of soybean, Glycine max (L.) Merrill, in the midwestern United States and Canada. We compared three soybean aphid management techniques in three midwestern states (Iowa, Michigan, and Minnesota) for a 3-yr period (2005–2007). Management techniques included an untreated control, an insecticidal seed treatment, an insecticide fungicide tank-mix applied at flowering (i.e., a prophylactic treatment), and an integrated pest management (IPM) treatment (i.e., an insecticide applied based on a weekly scouting and an economic threshold). In 2005 and 2007, multiple locations experienced aphid population levels that exceeded the economic threshold, resulting in the application of the IPM treatment. Regardless of the timing of the application, all insecticide treatments reduced aphid populations compared with the untreated, and all treatments protected yield as compared with the untreated. Treatment efficacy and cost data were combined to compute the probability of a positive economic return. The IPM treatment had the highest probability of cost effectiveness, compared with the prophylactic tank-mix of fungicide and insecticide. The probability of surpassing the gain threshold was highest in the IPM treatment, regardless of the scouting cost assigned to the treatment (ranging from

Impact of predation on establishment of the soybean aphid, Aphis glycines in soybean, Glycine max

0.00 to

Epidemiology and Field Control of PVY and PLRV

19.76/ha). Our study further confirms that a single insecticide application can enhance the profitability of soybean production at risk of a soybean aphid outbreak if used within an IPM based system.

Performance and prospects of Rag genes for management of soybean aphid

The soybean aphid, Aphis glycines Matsumura is a new invasive pest of soybean in North America. We studied the ability of the existing predator community in soybean to reduce A. glycines establishment in field studies using either predator exclusion, open, or leaky cages that allowed aphid emigration but limited predation. Cages were infested with uniform initial densities of A. glycines adults and subsequent populations of aphids and predators were monitored over 24 h. The most abundant predators in these trials included the carabid beetles Elaphropus anceps (Le Conte), Clavina impressefrons Le Conte, Bembidion quadrimaculatum Say and spiders (Salticidae and Lycosidae). Foliar predators were less abundant and included; Harmonia axyridis Pallas, Coccinella septempunctata (L.), and Orius insidious (Say). Over the 2-year study, we found statistically significant predation on adult A. glycines in one out of six trials at 15 h and two out of six trials at 24 h. There was never significant evidence for predation of nymphs in any trial, however overall survival (adults + nymphs) was significantly reduced in one out of six trials at 15 h and three out of six trials at 24 h. Based on these results we suggest that generalist predators can be a significant but variable factor influencing the establishment of A. glycines populations in soybean. The impact of existing predator communities should be further investigated as a means of managing A.␣glycines populations in North American soybean production systems.

Soil Potassium Deficiency Affects Soybean Phloem Nitrogen and Soybean Aphid Populations

Viral diseases of potatoes can cause significant yield and quality losses for the commercial producer but are of particular concern to the seed potato producer. Potato virus Y (PVY) and Potato leafroll virus (PLRV) are the most common of the 28 viral diseases known to infect potato (Salazar, 1996). Current season (primary) infection with PVY causes little yield loss (Hane and Hamm, 1999; Salazar, 1996) especially if initial infection occurs after flowering. Quality loss caused by PVY results from an increase in the number of undersized tubers (Hane and Hamm, 1999). With PLRV, primary infection rarely reduces yield (Beemster and Rozendaal, 1972) but it can affect tuber quality by causing phloem net necrosis. Net necrosis is expressed in tubers as a darkening of the vascular bundle that becomes more pronounced during storage. Net necrosis is particularly severe in the cultivars Russet Burbank, Norgold Russet, and Green Mountain (Douglas and Pavek, 1972), the former being the most widely grown cultivar in the U.S.

Western Corn Rootworm (Coleoptera: Chrysomelidae) Feeding on Corn and Soybean Leaves Affected by Corn Phenology

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an invasive insect pest of soybean [Glycine max (L.) Merr. (Fabaceae)] in North America, and it has led to extensive insecticide use in northern soybean‐growing regions there. Host plant resistance is one potential alternative strategy for managing soybean aphid. Several Rag genes that show antibiosis and antixenosis to soybean aphid have been recently identified in soybean, and field‐testing and commercial release of resistant soybean lines have followed. In this article, we review results of field tests with soybean lines containing Rag genes in North America, then present results from a coordinated regional test across several field sites in the north‐central USA, and finally discuss prospects for use of Rag genes to manage soybean aphids. Field tests conducted independently at multiple sites showed that soybean aphid populations peaked in late summer on lines with Rag1 or Rag2 and reached economically injurious levels on susceptible lines, whereas lines with a pyramid of Rag1 + Rag2 held soybean aphid populations below economic levels. In the regional test, aphid populations were generally suppressed by lines containing one of the Rag genes. Aphids reached putative economic levels on Rag1 lines for some site years, but yield loss was moderated, indicating that Rag1 may confer tolerance to soybean aphid in addition to antibiosis and antixenosis. Moreover, no yield penalty has been found for lines with Rag1, Rag2, or pyramids. Results suggest that use of aphid‐resistant soybean lines with Rag genes may be viable for managing soybean aphids. However, virulent biotypes of soybean aphid were identified before release of aphid‐resistant soybean, and thus a strategy for optimal deployment of aphid‐resistant soybean is needed to ensure sustainability of this technology.