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3-2012 (Coleoptera: Chrysomelidae) and Bean Pod Mottle irV us in : Biology, Ecology, and Management Buyung A. R. Hadi South Dakota State University, [email protected]

Jeffrey D. Bradshaw University of Nebraska, [email protected]

Marlin E. Rice Pioneer Hi-Bred International, [email protected]

John J. Hill Iowa State University, [email protected]

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Hadi, Buyung A. R.; Bradshaw, Jeffrey D.; Rice, Marlin E.; and Hill, John J., "Bean Leaf Beetle (Coleoptera: Chrysomelidae) and Bean Pod Mottle irV us in Soybean: Biology, Ecology, and Management" (2012). Faculty Publications: Department of Entomology. 610. http://digitalcommons.unl.edu/entomologyfacpub/610

This Article is brought to you for free and open access by the Entomology, Department of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications: Department of Entomology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Bean Leaf Beetle (Coleoptera: Chrysomelidae) and Bean Pod Mottle Virus in Soybean: Biology, ecology, and management Buyung A. R. Hadi,1,2 Jeffrey D. Bradshaw,3 Marlin E. Rice,4 and John H. Hill5 1Plant Science Department, South Dakota State University, Brookings, SD 57007. 2Corresponding author, e-mail: [email protected]. 3Department of Entomology, Panhandle Research and Extension Center, University of Nebraska, Scottsbluff, NE 69361. 4Pioneer Hi-Bred International, Inc., Johnston, IA 50131. 5Department of Plant Pathology, Iowa State University, Ames, IA 50011.

J. Integ. Pest Mngmt. 3(1): 2012; DOI: http://dx.doi.org/10.1603/IPM11007

ABSTRACT. Bean leaf beetle, Cerotoma trifurcata (Fo¨rster), is a pest of soybean found in many production areas in the United States. The bean leaf beetle larvae feed on soybean root nodules, whereas the adults feed on the above ground parts of soybean such as cotyledon, leaves, and pods. Bean leaf beetle is also a very efficient vector of Bean pod mottle virus, a widespread virus of soybean in the south and southeastern United States with recent expansion into the north central region of the country. This article summarizes bean leaf beetle biology, ecology, and its impact on soybean production in the United States. The management of this insect and Bean pod mottle virus as recommended in the north central states is also presented.

Key Words: bean leaf beetle, Cerotoma trifurcata, bean pod mottle virus, soybean

The bean leaf beetle, Cerotoma trifurcata (Fo¨rster), is a pest of , Life Cycle and Seasonal History. Bean leaf beetles overwinter as Glycines max (L.) in most soybean growing regions of the United States. adults and are able to withstand temperatures below the water freezing Adults feed on cotyledons, leaves, and pods, whereas larvae feed on point. In a laboratory study, Lam and Pedigo (2000a) found that soybean nodules attached to the roots. Furthermore, bean leaf beetles also exposing winter-acclimated adult beetles for 12 minutes below 14°F transmit Bean pod mottle virus, a widespread virus of soybean. Bean leaf (Ϫ10°C) resulted in 50% mortality, yet it took 400 hours at temper- beetles can be found in major soybean production areas in the United atures between 23° and 14°F (Ϫ5 and Ϫ10°C) to kill the same States (Turnipseed and Kogan 1976, Pedigo 1994). The biology of bean proportion of beetles. Carillo et al. (2005) reported that bean leaf leaf beetle, both as a pest of soybean and a vector of Bean pod mottle beetles collected in different months in a year had varying degrees of virus will be discussed, followed by a section of management of bean leaf cold hardiness. Most beetles collected between September to March beetle and Bean pod mottle virus with emphasize on recommendations were able to survive lower temperatures than beetles collected during for the north central states. the rest of the year. Bean leaf beetle adults survive winter under leaf Identification. The bean leaf beetle is a member of the family debris in woodlots and crop residue in soybean fields. Survival rate of Chrysomelidae in the order Coleoptera. Adults are variable in color, overwintering bean leaf beetles is higher in sheltered habitats (e.g., ranging from red to orange to light yellow (Fig. 1). When adults first woodlands) compared with exposed habitats (e.g., soybean fields) emerge from the soil, their elytra (wing covers) are soft and the body (Lam and Pedigo 2000b). A measurement of daily temperature during is often beige in color (Fig. 2). Four squarish black markings are winter in Iowa showed that woodland leaf litter can maintain temper- common on the elytra; however, these markings can be as few as two atures above 23°F (Ϫ5°C), which contributes to higher survival rate of or none. The elytra are usually rimmed by a black margin. A black overwintering bean leaf beetles in this habitat (Lam and Pedigo triangle, termed the scutellum, is always present immediately behind 2000a). In the extreme southern United States, the beetles may not the pronotum (Pedigo 1994) (Fig. 3) regardless of whether the insect even hibernate at all (McConnel 1915). has four, two, or no black “squares” on the elytra. Female beetles often Surviving adults begin to emerge from their overwintering sites at have black frons (face), whereas the male beetles usually have tan 50–55°F (10–12.7°C) (Boiteau et al. 1979a, Jeffords et al. 1983, frons (Kogan et al. 1980). In addition, the base of a male beetle’s first Loughran and Ragsdale 1986). The beetles mate and disperse to various tarsal segment has a patch of dense setae (hairs) thought to be involved hosts such as alfalfa (Medicago sativa L.) and other legumes such as tick in the mating process (Hammack and French 2007). Female beetles trefoil (Desmodium spp.) and clover (Smelser and Pedigo 1991, Brad- lack this morphological feature. shaw et al. 2007). Bean leaf beetle adults move to soybean, their apparent Bean leaf beetle eggs are lemon-shaped and orange in color, and they preferred host, as the soybean seedlings emerge (Figs. 5 and 6). are found in soil around the base of soybean plants (Pedigo 1994). The Female bean leaf beetles enter soybean fields gravid (i.e., mated subterranean larva is elongate, white in color with dark brown plates on and carrying eggs) and lay small clusters of eggs within 1.5 inches (3.8 both ends of the body (Fig. 4). The dark brown color comes from cm) of the soil surface and within a 2-inch (5.1 cm) radius of the sclerotization of the larva’s head and last abdominal segment. Larvae can soybean plant (Waldbauer and Kogan 1975). Each female lays 130– grow to 0.4 inch (10 mm) long, are cylindrical in shape, and similar 200 eggs throughout its lifetime (Pedigo 1994). When given a choice, looking to corn rootworm (Diabrotica spp.) larvae. The pupae are white, female beetles preferred to lay their eggs in an organic soil rather than Ϸ0.2 inch (5 mm) long, and enclosed within earthen cells. in sandy clay loam or loamy sand (Marrone and Stinner 1983a). In Host Plant. Bean leaf beetles have a large host range, mostly on addition, Marrone and Stinner (1983a) also found more eggs in wet or leguminous plants including clover (Trifolium spp.) and soybean moist soils than in dry soils. Bean leaf beetle eggs take a week to hatch (Bradshaw et al. 2007); however, they also have been reported to feed at 82.4°F (28°C). Both very wet and very dry soils are detrimental to on nonleguminous hosts such as cucurbits (Koch et al. 2004), stinging the eggs. Coincidental with oviposition preference, egg survival was nettle (Urtica dioica L.), and Canadian woodnettle [Laportea ca- the greatest when kept in saturated organic soil as compared with nadensis (L.)] (Helm et al. 1983). loamy sand and sandy clay loam (Marrone and Stinner 1983b). 2 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 3, NO. 1

Fig. 1. Variation in adult bean leaf beetle, Cerotoma trifurcata, body coloration.

Fig. 4. Bean leaf beetle, Cerotoma trifurcata, larvae. Fig. 2. Newly-emerged bean leaf beetle, Cerotoma trifurcata.

Fig. 3. Adult bean leaf beetle, Cerotoma trifurcata, can always be recognized by the black triangular spot behind the pronotum (A). Fig. 5. Overwintered generation of bean leaf beetle, Cerotoma Most adults also have four large squarish markings on the elytra (B), trifurcata, moving to soybean seedlings. and a black rim on the elytra (C). year in the southern United States (Pedigo 1994), two generations in Bean leaf beetle larvae feed in the soil on soybean roots and root the central states of Illinois (Waldbauer and Kogan 1976), Iowa nodules (Pedigo 1994, Lundgren and Riedell 2008). Larvae develop (Smelser and Pedigo 1991), and Nebraska (Danielson et al. 2000), and through three stages before pupating in the soil. The larvae are capable only one generation in Minnesota (Loughran and Ragsdale 1986). of moving in the soil and under dry soil conditions can move up to Adults readily disperse by flight. In a laboratory study character- 11.8 inches (30 cm) per hour in search of moisture (Marrone and izing the beetle’s flight capacity, the majority of sampled beetles Stinner 1983c). The type of soil in which the larvae forage for food showed short distant flight of Ͻ167 feet (Ͻ51 m) in a 24-hour period. affects the larval survivorship. Cuticle abrasion associated with the A little over 11% of the beetles showed medium range flight capacity soil’s sand content is detrimental to larvae. Under moist soil condi- Ͼ987 feet (Ͼ301 m) and one beetle flew 3 miles (4.9 km) in a 24-h tions, larvae survived best in organic soil (0–4% mortality) compared period (Krell et al. 2003b). with loamy sand (87–100% mortality) and sandy clay loam (0–20% In the field, bean leaf beetle populations are often highly aggre- mortality) (Marrone and Stinner 1983c). gated along field edges (Kogan et al. 1974, Boiteau et al. 1979b, Development from egg to adult requires 674–740 DD in °F (374– Smelser and Pedigo 1992a). It is not known whether the aggregated 411 DD in °C), with the lower development threshold at 46°F (7.8°C) spatial pattern of bean leaf beetle in the field is maintained under very (Zeiss et al. 1996). Beetles emerging from the soil form the first high population levels as observed in outbreak years. generation of adults for a given year. Depending on the timing of Plant Injury and Damage. Bean leaf beetle larvae feed on soybean emergence in relation to the stage of soybean development, adult root nodules. Soybean compensates for larval feeding by producing beetles may mate again and deposit eggs or they may overwinter until additional nodules. However, high larval infestation (19 larvae per the subsequent year. Bean leaf beetles produce three generations per plant) may cause smaller root nodules and reduce leaf and pod MARCH 2012 HADI ET AL.: BEAN LEAF BEETLE AND VIRUS IN SOYBEAN 3

Fig. 6. Leaf injury and cotyledon scarring because of adult bean leaf beeetle, Cerotoma trifurcata, feeding. Fig. 8. Defoliation inflicted by bean leaf beetle, Cerotoma trifurcata.

Fig. 9. Pod injury from bean leaf beetle, Cerotoma trifurcata, feeding. Fig. 7. Soybean seedling injury from bean leaf beetle, Cerotoma trifurcata. manually between blooming and pod set (R1-R4) to show that yield nitrogen content (Lundgren and Riedell 2008). The potential eco- loss occurs at high levels of defoliation (above 50%). Adults feeding nomic damage because of root feeding by larvae is not clearly on later stage soybean plants may contribute additively to the overall understood. impact of defoliation when they occur with other leaf feeding insects. Adults feed on the above ground parts of soybean such as cotyle- It has been estimated that, on average, an adult beetle feeding on R6 dons, leaves and pods (Figs. 7-9). Beetle feeding may commence at soybean for two weeks may reduce as much as 0.0074 ounce (0.21 g) the leaflet edge or in the middle of the leaflet producing round holes of seed weight (Smelser and Pedigo 1992c). in the tissues between leaf veins. The round holes produced by adult During seed filling, bean leaf beetles may feed on the pod surface. feeding are generally distinct from more jagged-edged feeding holes Although root-feeding larvae and leaf-feeding adults may affect seed produced by grasshoppers and caterpillars (Smelser and Pedigo yield and quality, pod feeding inflicts direct injury on the seeds. The 1992b). feeding injury on the pod surface acts as an entry point for bacterial The impact of adult feeding is dependent on the plant’s growth and fungal secondary infection, and the scarring of soybean pods stage. A single adult feeding on soybean during vegetative stages exposes the seeds to excess moisture. The seeds on scarred pod may (V1-V3, Ϸ14 days) is estimated to consume up to 5.48 inches2 (13.93 become shrunken, discolored, and moldy. Bean leaf beetles also feed cm2) of foliage (Hunt et al. 1995). Hunt et al. (1994) found that a on the soybean pod peduncle, sometimes clipping the pod in the reduction of cotyledon and seedling tissue delays canopy development process. Smelser and Pedigo (1992c) found no significant difference and reduces yield. Sequential removal of 68% soybean seedling tis- in seed weight, and number of seeds per plant between several levels sues between V1-V3 stages resulted in a 12% yield reduction (Hunt et of bean leaf beetle infestation. However, in a drought year of 1988, al. 1994). It has been noted that soybean plants tolerate defoliation Smelser and Pedigo (1992b) documented that an average of 0.125 pod either by delayed leaf senescence or compensatory leaf regrowth. This per beetle was lost each day because of beetle feeding on pod compensatory response can offset foliage loss because of bean leaf peduncles. beetle feeding (Haile et al. 1998). Defoliation tolerance seems to Bean leaf beetle as Bean pod mottle virus vector. Bean pod mottle depend on an optimum growth environment, thus in drought years this virus is a member of the genus in the family tolerance may be limited. Turnipseed (1972) removed soybean leaves (Sanfacon et al. 2009). The first incidence of Bean pod mottle virus in 4 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 3, NO. 1

Fig. 12. Normal soybean seed (left) and infected seed with Bean pod mottle virus (right) showing the “bleeding” hilum.

the highest yield reduction (Ziems et al. 2007). The seeds produced by Bean pod mottle virus-infected soybean may show mottled seed coats Fig. 10. Soybean leaf distorted by Bean pod mottle virus. (Fig. 12), reducing the quality of the seed (Hobbs et al. 2003, Hill et al. 2007). Bean pod mottle virus infection on soybean also increases the risk of Phomopsis seed infection (Abney and Ploper 1994). Co- the United States was reported on common bean (Phaseolus vulgaris infection of Bean pod mottle virus and leads to L.) in South Carolina (Zaumeyer and Thomas 1948) and the first synergistic infection where Soybean mosaic virus presence increases reported incidence on soybean was from Arkansas (Walters 1958). the titer of Bean pod mottle virus (Anjos et al. 1992), which translates The incidence of Bean pod mottle virus is widespread in major into dramatic reduction of yield (Ross 1968) and root nodules (Tu et soybean growing regions in the south and southeastern United States; al. 1970) of co-infected soybean plants. more recently increased incidence has been documented in soybean Bean pod mottle virus is transmitted by several leaf feeding beetles throughout the north central United States (Giesler et al. 2002). in North America, including bean leaf beetle, grape colaspis [Colaspis Depending on the soybean variety and the virus strain, infected brunnea (F.)], banded cucumber beetle (Diabrotica balteata Le- soybean may show symptoms ranging from chlorotic mottling, severe Conte), spotted cucumber beetle (Diabrotica undecimpunctata how- mosaic to leaf distortion (Fig. 10) and leaf necrosis. The most obvious ardi Barber), striped blister beetle [Epicauta vittata (F.)], and Mexican symptoms occur in plants infected early in the season or during bean beetle (Epilachna varivestis Mulsant) (Gergerich 1999). Bean periods of rapid growth. Symptoms are more clearly shown in low leaf beetle is an extremely efficient Bean pod mottle virus vector; up ambient temperatures (Gergerich 1999). Bean pod mottle virus infec- to 80% of beetles feeding on Bean pod mottle virus-infected soybean tion has been associated with a disorder known as “green stem”. The for three days were able to transmit the virus to healthy plants (Giesler stems of plants showing green stem disorder stay green (Fig. 11) even et al. 2002). In addition, bean leaf beetle transmits Cowpea mosaic as they bear normal mature pods. This condition may have an impact virus and Southern bean mosaic virus (Boethel 2004). Of all the on soybean harvest as the green stems are more difficult for harvesting soybean viruses transmitted by bean leaf beetle, Bean pod mottle virus machinery to cut. Contradictory results have been reported on the is considered to be the most prevalent and widespread in the U.S. relationship between Bean pod mottle virus infection and green stem soybean producing regions (Tolin and Lacy 2004). disorder (e.g., Goh et al. 2004, Hobbs et al. 2006), and the precise Theoretically, there are at least three sources of primary Bean pod cause of the green stem disorder remains unclear. mottle virus inoculum in summer soybean introduction: soybean seeds Soybean infected by Bean pod mottle virus produces 3–52% less infected with the virus, virus from previous year’s epidemic retained yield depending on the soybean variety and the time of infection. in overwintering bean leaf beetles, and virus-infected leguminous Virus infection occurring in early vegetative stages (VC-V3) causes weeds. Seed infection of Bean pod mottle virus occurs at a very low rate and seed coat mottling is not a good indicator of seed infection as mottling may still occur without virus presence within the seed (Krell et al. 2003a). Overwintering bean leaf beetles have been shown to retain Bean pod mottle virus from the previous year albeit in a very low frequency (Krell et al. 2003a). Bean pod mottle virus infects a range of mostly leguminous hosts including soybean and dry bean. Tick trefoil, a perennial leguminous weed, was found to host Bean pod mottle virus in nature (Krell et al. 2003a, Bradshaw et al. 2007). Beetles emerging from overwintering habitats and feeding on infected perennial tick trefoil may acquire the virus. When soybean seedlings emerge, the beetles move to these plants, transmitting the virus. The subsequent generation(s) of bean leaf beetle may continue to spread the virus within and between soybean fields during the growing season. Management Approaches. The first part of this section describes management approaches of bean leaf beetle in the absence of Bean pod mottle virus. If a particular field’s history included incidences of Bean pod mottle virus and virus-related loss of yield quantity and quality, a different management approach is recommended. Bean leaf beetle management in the presence of Bean pod mottle virus history Fig. 11. Soybean field (foreground) showing a streak of “green is discussed under the heading “Management of Bean Leaf Beetle in stem”. the Presence of Bean Pod Mottle Virus.” MARCH 2012 HADI ET AL.: BEAN LEAF BEETLE AND VIRUS IN SOYBEAN 5

swing a sweep net upward and downward on a row (not across rows) with successive steps (Video Clip 1: Sweep net sampling technique on soy- bean [video-Marlin E. Rice]). Count each stroke of the net as a sweep and 10–20 sweeps per sampling site should be conducted. Bean leaf beetles are counted after each sampling unit. At the end of sampling, the average count of bean leaf beetles per sample site can be calculated. An example of equipment used for ground cloth sampling consists of a white cloth measuring 36 by 42 inches (0.91 by 1 m) with strips of wood, Ϸone-half by 1 inch (1.27 by 2.54 cm) wide, stapled to each long side of the cloth. Sample at least five randomly chosen sampling sites across the field. In each site, roll the cloth beneath the canopy from one row over to the next row without disturbing the foliage (Fig. 13). Vigorously shake the plants from both rows over the ground cloth by using both hands and forearms. Count the beetles collected on the cloth. This way, two 3-row feet (0.91 row m) sections (a total of 6 feet, or 1.82 m) are sampled. If some insects can’t be identified on the field, collect several specimens for later identification. By the end of sam- pling, the average count of beetle per row-foot or row-meter can be Fig. 13. Drop cloth positioning for bean leaf beetle sampling in calculated. soybean. Hunt et al. (1995) reported a matrix of EILs of overwintered bean leaf beetle on early soybean seedlings (VC-V2) for various scenarios Scouting and Threshold. Scouting for bean leaf beetle can be done of market value per production unit and control cost per area. Assum- by direct observation, sweep net, or ground cloth. The description of ing the economic threshold to be equal to 75% of the economic injury scouting techniques described here is drawn largely from Kogan et al. level (EIL) presented by Hunt et al. (1995), Rice et al. (2005) sum- (1980). Some thresholds are based on the field estimation of percent marized the economic threshold values as represented in Table 1. The defoliation or pods injured from beetle feeding activity while other thresholds are directly based on the sampling of bean leaf beetle economic threshold values in Table 1 represent uncommonly high population in the field. population densities of overwintered bean leaf beetles (Hunt et al. Direct observation may accurately estimate early-season (VC–V4 1995). stage) bean leaf beetle populations. This observation estimates the In areas where there are only two generations of bean leaf beetles abundance of overwintering beetles from the previous year. Randomly per year, the need to control the second generation beetle can be select five 16–32 feet (5–10 m) row-lengths from across the entire determined by sampling the first generation (Lam et al. 2000). This field. At each sampling site, walk slowly and carefully count all sampling scheme was developed in Iowa and its validity has not been beetles. Make sure that beetles on the underside of the leaves are tested elsewhere. This scheme is based on a positive correlation counted by gently turning the leaves over. Cool early-morning hours between the population size of first generation beetle and the popu- are probably the best time to conduct the observation as the beetles are lation size of second generation beetle in a given year in Iowa (Lam relatively inactive. At the end of sampling, the average number of et al. 2001, 2008). Using the Lam et al. (2000) sampling plan, scouting beetles per row-foot or, given a fixed inter-row spacing, the number of should begin 1 wk after the peak emergence of first generation beetles. beetles per plant can be calculated. The peak emergence time can be estimated by accumulating 1,212 DD In conventional soybean cropping system (the rows are Ϸ30 inches in °F (673 DD in °C), with base temperature of 46°F (7.78°C), starting [76 cm] apart), the ground cloth technique is reliable in moderate to at soybean emergence. First generation bean leaf beetles can be high beetle population levels (defined as the number of beetles per sampled using sweep net or ground cloth. A set of threshold values for row-3 feet [1 m] Ͼ10) while the sweep net is reliable at all population the first generation beetle, represented as the number of beetles caught levels. Both techniques are used when the soybean plants are too large using drop cloth and sweep net, are given consecutively in Table 2 and for direct observation. These techniques are essential in estimating the 3 (Lam et al. 2000). If in the first scouting the beetle population does first and subsequent generations of bean leaf beetles in soybean fields. not exceed the threshold, scouting should be repeated 1 week later. If Deighan et al. (1985) noted that ground cloth sampling produced in the second scouting the beetle population still does not exceed the better estimates of bean leaf beetle population in conventional crop- threshold, scouting is repeated in the third and final week. If after three ping system than in drill-planted soybean. scouting efforts the bean leaf beetle population never exceeds the Five to eight sampling sites should be chosen randomly across the threshold, no economic damage should occur from the second gener- field for sweep net scouting. On each site, walk between two rows and ation bean leaf beetle infestation and no control action is necessary the

Table 1. Economic threshold of overwintered bean leaf beetle in 30-inch row early-stage soybean (beetles per plant) (Hunt et al. 1995, Rice et al. 2005) Growth stage/cost of treatment, $/acre ($/bu) Market value VC V1 V2 $/Bu ($/kg) 6 (14.8) 10 (24.7) 14 (34.6) 18 (44.5) 6 (14.8) 10 (24.7) 14 (34.6) 18 (44.5) 6 (14.8) 10 (24.7) 14 (34.6) 18 (44.5) 5.00 (0.18) 2.5 4.1 5.8 7.4 3.8 6.3 8.9 11.4 6.0 9.9 13.9 17.9 10.00 (0.36) 1.2 2.1 2.9 3.7 1.9 3.2 4.4 5.7 3.0 5.0 7.0 9.0 15.00 (0.54) 0.8 1.4 1.9 2.5 1.3 2.1 3.0 3.8 2.0 3.3 4.6 6.0 These values are calculated by using the formula: ET ϭ 0.75*(C/VIDK). Where ET is Economic threshold, C ϭ cost of management per production unit, V ϭ market value per production unit, I ϭ injury units per insect per production unit, D ϭ damage per production unit and K ϭ proportionate reduction of the insect population. It is assumed that for VC growth stage, D ϭ 1.33 (from regression based on an expected yield of 34.4 bu/acre), I ϭ 18.79, and K ϭ 1 (total control); for V1, D ϭ 1.33, I ϭ 12.20 and K ϭ 1; for V2, D ϭ 1.33, I ϭ 7.78 and K ϭ 1 (Hunt et al. 1995). 6 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 3, NO. 1

Management of Bean Leaf Beetle in the Presence of Bean Pod st Table 2. Ground cloth economic threshold for 1 generation bean Mottle Virus. Delayed soybean planting date has been suggested as a 2 leaf beetles scouting in soybean (beetles per m ) (Smelser and Bean pod mottle virus management tactic (Giesler et al. 2002), but 3-yr Pedigo 1992, Lam et al. 2000). If the beetle population is higher field data from Iowa showed that delayed planting did not consistently than the threshold value, control action should be conducted upon result in lower Bean pod mottle virus infection (Krell et al. 2005). the emergence of the second generation bean leaf beetles The use of soybean varieties with antixenosis (i.e., physical resis- Market Cost of treatment/acre ($/acre) tance) against bean leaf beetles does not sufficiently reduce Bean pod value mottle virus incidence and spread in the field (Redinbaugh et al. ($/Bu) 7 8 10 12 15 18 2010). No soybean varieties with resistance against Bean pod mottle 5.00 5.8 6.7 8.3 10.0 12.5 15.0 virus have been reported although some varieties have some tolerance 6.00 4.9 5.6 6.9 8.3 10.4 12.5 (Hill et al. 2007, Ziems et al. 2007). 8.00 3.7 4.3 5.3 6.4 8.0 9.6 Insecticide seed treatment by using neonicotinoid insecticides (Video 10.00 2.9 3.4 4.2 5.0 6.3 7.6 13.00 2.2 2.6 3.2 3.8 4.8 5.8 Clip 2: The effect of seed treatment on soybean on overwintered bean leaf 15.00 1.9 2.2 2.8 3.3 4.2 5.0 beetle [video-Marlin E. Rice]) or foliar pyrethroid insecticides between These values were calculated by using the formula: ET ϭ 0.75*EIL. Where emergence and first trifoliolate reduces total Bean pod mottle virus EIL is Economic injury levels. The economic injury levels used here were incidence, likely by protecting soybean seedlings from early beetle pop- based on the work of Smelser and Pedigo (1992), where a beetle feeding on ulations (Krell et al. 2004, Bradshaw et al. 2008). Additional applications late season soybean was found to cause an average seed yield reduction of 0.000306 kg. of foliar insecticides by using foliar pyrethroid insecticides midseason (around blooming), aimed at controlling the first generation of bean leaf beetle, may further suppress virus incidence (Krell et al. 2004, Bradshaw et al. 2008). Table 3. Sweep net economic threshold for 1st generation bean Summary. The bean leaf beetle is an occasional pest of soybean but leaf beetles in soybean (beetles per 20 sweeps) (Lam et al. 2000). If occurs in most soybean producing areas of the United States. Thus, the the beetle population is higher than the threshold value, control action should be conducted upon the emergence of the second potential for economic injury exists in many soybean production generation bean leaf beetles systems, especially in the north central states. The biology, sampling, and management considerations described are intended to reduce the Market Cost of treatment/acre ($/acre) economic impact of this pest, including its role in transmitting Bean value pod mottle virus. Effective management of the insect requires an ($/bu) 7 8 10 12 15 18 understanding of pest ecology, timely scouting, and the application of 5.00 17.4 19.9 24.8 29.8 37.2 44.7 appropriate control measures when economically warranted. 6.00 14.5 16.6 20.7 24.8 31.0 37.2 8.00 11.1 12.7 15.9 19.0 23.8 28.5 10.00 8.8 10.0 12.5 15.0 18.8 22.5 References Cited 13.00 6.7 7.6 9.5 11.5 14.3 17.2 Abney, T. S., and L. D. Ploper. 1994. Bean pod mottle virus effects on soybean 15.00 5.8 6.6 8.3 9.9 12.4 14.9 seed maturation and seedborne Phomopsis spp. Plant Disease 78: 33–37. Anjos, J. R., U. Jarlfors, and S. A. Ghabrial. 1992. Soybean mosaic potyvirus These values were calculated by using the formula: ET ϭ 0.75*EIL. Where EIL is Economic injury levels. The economic injury levels used here were enhances the titer of two in dually infected soybean plants. based on the work of Smelser and Pedigo (1992), where a beetle feeding on Phytopathology 82: 1022–1027. late season soybean was found to cause an average seed yield reduction of Boethel, D. J. 2004. Integrated pest management of soybean insects, pp. 0.000306 kg. 853–881. In: H. R. Boerma and J. E. Specht (eds.). Soybeans: improvement, production and uses, 3rd ed. ASA/CSSA/SSSA, Madison, WI. Boiteau, G., J. R. Bradley, and J. W. Van Duyn. 1979a. Bean leaf beetle: next (e.g., second) generation. If the threshold is exceeded in one of Emergence patterns of adults from overwintering sites. Environmental En- the three scouting efforts, Lam et al. (2000) recommends a control tomology 8: 427–431. action; however, the timing of control action should correspond with Boiteau, G., J. R. Bradley, J. W. Van Duyn, and R. E. Stinner. 1979b. Bean leaf the emergence of the later second generation population in the soy- beetle: micro-spatial patterns and sequential sampling of field populations. bean field (Rice et al. 2005). Environmental Entomology 8: 1139–1144. A more general approach to set an economic threshold for bean Bradshaw, J. D., M. E. Rice, and J. H. Hill. 2007. No-choice preference of Cerotoma trifurcata (Coleoptera: Chrysomelidae) to potential host plants of leaf beetle is by using the defoliation rate because of bean leaf beetle Bean pod mottle virus (Comoviridae) in Iowa. Journal of Economic Entomol- feeding activity. Overwintered beetles feed on seedling soybean and ogy 100: 808–814. treatment is warranted if over 20–30% of the seedlings in the field are Bradshaw, J. D., M. E. Rice, and J. H. Hill. 2008. Evaluation of management destroyed. Treatment is also warranted if defoliation exceeds 30–50% strategies for bean leaf beetles (Coleoptera: Chrysomelidae) and Bean pod during other vegetative stages of soybean development. Adults from mottle virus (Comoviridae) in soybean. Journal of Economic Entomology the first generation bean leaf beetles feed on soybean leaf around July 101: 1211–1227. Carrillo, M. A., R. L. Koch, E. C. Burkness, K. Bennett, D. W. Ragsdale, and in the north central United States and should be treated if defoliation W. D. Hutchison. 2005. Supercooling point of bean leaf beetle (Coleoptera: rate exceeds 15–35% during bloom (R1-R2). During pod-set and Chrysomelidae) in Minnesota and a revised predictive model for survival at pod-fill (R3-R6), a field should be treated if defoliation exceeds 25%. low temperatures. Environmental Entomology 34: 1395–1401. Because bean leaf beetles also feed on pods, damage to pods should Danielson, S. D., J. R. Brandle, L. Hodges, and P. Srinivas. 2000. Bean leaf beetle also be monitored. Control is warranted if pod injury exceeds 10% (Coleoptera: Chrysomelidae) abundance in soybean fields protected and unpro- during pod-fill (Zeiss and Klubertanz 1994, University of Minnesota tected by shelterbelts. Journal of Entomological Science 35: 385–390. Deighan, J., R. M. McPherson, W. F. Ravlin. 1985. Comparison of sweep-net and Extension 2006, Knodel et al. 2009). ground-cloth sampling methods for estimating arthropod densities in different Cultural Methods. Delayed soybean planting date may reduce bean soybean cropping systems. Journal of Economic Entomology 78: 208–212. leaf beetle abundance (Pedigo and Zeiss 1996). Planting soybean as Gergerich, R. C. 1999. Bean pod mottle, pp. 61–62. In G. L. Hartman, J. B. late as possible within the recommended planting period for a variety Sinclair, and J. C. Rupe (eds.), Compendium of soybean diseases, 4th ed. may reduce initial and subsequent beetle densities, although main- APS Press, St. Paul, MN. taining yield potential. A potential risk is of note when late-planted Giesler, L. J., S. A. Ghabrial, T. E. Hunt, and J. H. Hill. 2002. Bean pod mottle virus: a threat to U.S. soybean production. Plant Disease 86: 1280–1289. soybean fields were located next to early-planted fields. In this situ- Goh, Y. K., J. S. Russin, S. A. Ghabrial, J. P. Bond, and M. E. Schmidt. 2004. ation, beetles from early-planted fields may easily migrate to late- Soybean green stem caused by selected strains of Bean pod mottle virus. planted fields, rendering planting date strategy ineffective. Phytopathology 94: S158. MARCH 2012 HADI ET AL.: BEAN LEAF BEETLE AND VIRUS IN SOYBEAN 7

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Received 14 February 2011; accepted 6 December 2011.