Stink Bug Species Composition and Relative Abundance of the Redbanded Stink Bug (Hemiptera: Pentatomidae) in Soybean in the Upper Gulf Coast Texas Author(s): Suhas S. Vyavhare, Michael O. Way, and Raul F. Medina Source: Environmental Entomology, 43(6):1621-1627. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EN14059
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SAMPLING
Stink Bug Species Composition and Relative Abundance of the Redbanded Stink Bug (Hemiptera: Pentatomidae) in Soybean in the Upper Gulf Coast Texas SUHAS S. VYAVHARE,1 MICHAEL O. WAY,2
AND
RAUL F. MEDINA1,3
Environ. Entomol. 43(6): 1621Ð1627 (2014); DOI: http://dx.doi.org/10.1603/EN14059
ABSTRACT Stink bugs are the primary arthropod soybean pests in the southern United States. Historically, important stink bug species damaging soybeans in the southern United States included the southern green stink bug Nezara viridula (L.), the green stink bug Chinavia hilaris (Say), and the brown stink bug Euschistus servus (Say) (Hemiptera: Pentatomidae). The redbanded stink bug, Piezodorus guildinii (Westwood), has recently become an economic pest of soybean in the southern region of the United States, especially in Louisiana and Texas. Little is known about current stink bug species composition and relative abundance in Texan soybean agro-ecosystems. To Þll this gap, commercial soybean Þelds in the Upper Gulf Coast of Texas were sampled weekly during the growing season using a sweep net throughout R2 (full ßowering) to R7 (beginning maturity) from 2011 to 2013. Adults and nymphs (third, fourth, and Þfth instars) of redbanded stink bug, southern green stink bug, green stink bug, and brown stink bug were counted per 25 sweeps. The relative abundance of redbanded stink bug was signiÞcantly higher than any other stink bug species throughout 2011Ð2013. Over 65% of the total population of major stink bugs collected during this period were redbanded stink bugs and ⬇19% were southern green stink bugs. The highest redbanded stink bug densities and the highest ratio of redbanded stink bug nymphs to adults were recorded at R7. Results from this study show that redbanded stink bug has become the predominant stink bug species in soybean in the Upper Gulf Coast of Texas. KEY WORDS Piezodorus guildinii, species composition, relative abundance
Stink bugs are polyphagous pests that feed on a wide range of cultivated crops including cotton (Gossypium hirsutum L.), soybean (Glycine max (L.) Merrill), and corn (Zea mays L.; Panizzi 1997). They also feed on a variety of wild and nonagronomic hosts (Panizzi 1997). Stink bugs have recently become primary pests of soybean in the southern United States (Drees and Rice 1990, Baur et al. 2000). The upsurge in stink bug populations in the southern United States is believed to be due to reduced number of insecticide sprays in cotton as a result of adoption of Bt crops combined with the boll weevil eradication program (Greene and Herzog 1999). Also, a shift in soybean production from May-planted maturity group (MG) V and VI in conventional soybean production systems to Aprilplanted MG III and IV in early season soybean production, may have contributed to stink bug population growth in recent years (Heatherly 2005). The increased pressure of stink bugs on early planted soybeans may be due to the early availability of pods (Baur et al. 2000). After colonizing early-planted soy1 Department of Entomology, Texas A&M University, 2475 TAMU College Station, TX 77843. 2 Texas A&M AgriLife Research and Extension Center, 1509 Aggie Dr., Beaumont, TX 77713. 3 Corresponding author, e-mail: [email protected].
beans, stink bugs successively move to later planted soybeans as the developing pods become available (Baur et al. 2000). Historically, the three key stink bug species viz. the southern green stink bug, Nezara viridula L.; the green stink bug, Chinavia hilaris Say; and the brown stink bug, Euschistus servus Say, have been known to be of substantial economic importance throughout the southern United States (McPherson et al. 1993). In the past, southern green stink bug, the most cosmopolitan of the pentatomids attacking soybean, has represented the highest proportion of all stink bug species in soybean Þelds from Texas in the west through southern Arkansas to Virginia in the east (Turnipseed and Kogan 1976). However, during the past decade, the redbanded stink bug, Piezodorus guildinii Westwood, has become more common than any other stink bug species in Louisiana (Temple et al. 2011) and may pose a threat to soybean production in other southern states. The redbanded stink bug was Þrst reported on the island of St. Vincent (Stoner 1922) and has been a serious pest of soybean in the Neotropics since the 1960s (Panizzi et al. 2000). In the late 1970s, redbanded stink bug began replacing southern green stink bug on Brazilian soybeans (Turnipseed and Kogan 1976, Kogan and Turnipseed 1987). The expan-
0046-225X/14/1621Ð1627$04.00/0 䉷 2014 Entomological Society of America
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sion of soybean cultivation in South America during the 1960s and 1970s could be the principal reason for the increase in redbanded stink bug populations (Panizzi and Slansky 1985a). Consequently, most of the information available about redbanded stink bug impact on soybean comes from Brazil (Panizzi et al. 1980; Panizzi and Slansky 1985a, b, c). In the United States, redbanded stink bug was Þrst reported in the 1960s in Florida (Genung et al. 1964). It was frequently observed in low numbers in Florida and Georgia in the1980s (Panizzi and Slansky 1985c), but it was never considered as an economic pest of soybeans until the late 1990s. Since its Þrst report in the United States, redbanded stink bug has expanded its distribution from Florida (Menezes 1981) to South Carolina (Jones and Sullivan 1982), Georgia (McPherson et al. 1993), Arkansas (Smith et al. 2009), Louisiana (Temple et al. 2009, 2013), and Missouri (Tindall and Fothergill 2011). IdentiÞcation and characterization of the species involved in the stink bug complex is important in designing proper management tactics. This is because different species within the stink bug complex have different damage potentials. For example, redbanded stink bug in soybean causes more damage per insect than any other stink bug species (Correa-Ferreira and de Azevedo 2002) while southern green stink bug and green stink bug cause similar damage, and brown stink bug cause comparatively less damage (Miner 1966, McPherson et al. 1979b). Nevertheless, the economic threshold level is the same for all these species in many of the soybean-producing states in United States including Texas, where redbanded stink bug populations have recently reached damaging levels (Vyavhare and Way 2013). No extensive Þeld surveys have been conducted to understand the current composition of stink bug species in Texas soybean. In Texas, an economic threshold of 8 stink bugs per 25 sweeps (38.1-cm-diameter sweep net) is used for the stink bug pest complex throughout all reproductive stages of soybean (Gouge et al. 1999). Although it is common to Þnd multiple stink bug species in the Þeld, little is known about how to incorporate species composition into considerations aimed at justifying use of chemical control against this pest complex. Also, it is important to understand the relative abundance of stink bug nymphs versus adults across different crop growth stages because the amount of injury per individual varies from nymphs to adults and the vulnerability of soybean to stink bug damage vary with plant growth stages. For example, both quality and yield loss are most affected when soybeans are exposed to stink bug feeding during R5ÐR6 (Fehr and Caviness 1977) while damage at R7 is much less than at earlier stages (McPherson et al. 1979b, Musser et al. 2011). Currently, stink bug control in soybean is mainly dependent on chemical applications (Davis et al. 2011). Susceptibility to insecticides has been reported to vary among stink bug species and life stages (McPherson et al. 1979a). For example, pyrethroids are more effective against southern green stink bug and green stink bug than against brown stink bug (Willrich et al. 2003). Also, LD50 values of methyl
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parathion for Þfth-instar nymphs of southern green stink bug, green stink bug, and brown stink bug are higher than for their corresponding adults (McPherson et al. 1979a). Therefore, knowledge of stink bug species involved, their relative abundance, and proportion of stink bug developmental stages across crop growth stages is needed. The occurrence of redbanded stink bug populations in Texas has been responsible for a substantial increase in the amount of insecticides applied to soybean (S.S.V. and M.O.W., unpublished data). This increase in chemical control threatens beneÞcial organisms in the soybean agro-ecosystem and could result in the development of insecticide resistance. The goals of this study were 1) to determine the predominant stink bug species and its abundance relative to other commonly known stink bug pest species in the Upper Gulf Coast of Texas and 2) to determine the relative abundance of stink bug nymphs and adults across R2ÐR6 stages of soybean. Materials and Methods Stink Bug Collection. Densities of stink bug species were monitored from 2011 to 2013 in commercial soybean Þelds across the Upper Gulf Coast of Texas. Each year Þve soybean Þelds under irrigated condition were chosen for the study. In 2011, study Þelds were located in Jefferson, Matagorda, Colorado, and Liberty Counties. In 2012, all Þelds were in Jefferson County. In 2013 soybean Þelds in Jefferson, Liberty, and Wharton counties were sampled. Soybeans in study Þelds represented primarily MG IV, V, and VI. Because the selected soybean Þelds were commercial, the breadth of conditions surveyed (i.e., Þeld sizes, varieties, seeding rates, plant spacing, etc.) varied substantially throughout the survey. Dates of seeding varied from mid-April to early-June depending on the soybean maturity groups. Fields were kept insecticide-free and sampled at weekly intervals from R2 (full ßowering) to R7 (beginning maturity) soybean growth stages (Fehr and Caviness 1977). Sampling began in mid-June and continued weekly through early October with Þve sets of 25 sweeps (38.1-cmdiameter sweep net) taken at random locations in each soybean Þeld on each sample date. Insect sampling was done by swinging the sweep net through the top of the canopy (Rudd and Jensen 1977). Each sample consisted of stink bugs collected in 25 consecutive sweeps taken in a row while walking forward. After collection, stink bugs were separated from foliage and placed in plastic zip-lock bags and brought to the laboratory. Plastic bags containing insects were stored at 3⬚C for further processing. Laboratory processing included identiÞcation of stink bug species and counting of nymphs (third, fourth, and Þfth instars only) and adults of each stink bug species found per sample. First and second nymphal instars were not included in counts because their impact on soybean damage is negligible (Simmons and Yeargan 1988). Stink bug species and developmental stages were identiÞed using diagnostic keys (McPherson and McPherson 2000, Kamminga et al. 2009). Only the
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VYAVHARE ET AL.: ABUNDANCE OF REDBANDED STINK BUG
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Fig. 1. Stink bug species composition across years (2011Ð2013) sampled from commercial soybean Þelds in Upper Gulf Coast region of Texas. Abundance of redbanded stink bugs was signiÞcantly higher every year.
number of redbanded stink bug, southern green stink bug, green stink bug, and brown stink bug from each sample were recorded. Sweep net samples also showed other minor pentatomid pest species such as Thyanta accera, Edessa bifida, Oebalus pugnax, Chlorochroa ligata, and the beneÞcial Podisus maculiventris. However, because the number of each of these species was negligible, relative abundances of each of the stink bug species considered in this study does not include these minor species in the denominator. Voucher specimens of each of the main stink bug species are kept in the Texas A&M University insect museum. Chi-square analysis was used to compare predominant stink bug species collected by year using PROC FREQ (SAS Institute 2010). Sampled Þelds were all located in the Upper Gulf Coast of Texas. Results Eighty-six percent of our Þeld samples (each sample ⫽ 25 sweeps) collected over 3 yr contained at least one of the major stink bug species (i.e., redbanded stink bug, southern green stink bug, green stink bug, or brown stink bug). Redbanded stink bug was the most abundant species consistently during 2011 (2 ⫽ 41.24, P ⫽ 0.04), 2012 (2 ⫽ 491.74, P ⬍ 0.0001), and 2013 (2 ⫽ 175.19, P ⬍ 0.0001; Fig. 1). Out of the major stink bug species collected (N ⫽ 4269) over our 3-yr Þeld survey, 65% were redbanded stink bug, followed by southern green stink bug (19%), brown stink bug (9%), and green stink bug (6%). The relative abundance of the major stink bug species varied depending on soybean growth stage (Fig. 2). In 2011, no signiÞcant differences were observed in relative abundance during R2 (2 ⫽ 15.06, P ⫽ 0.089), R3 (2 ⫽ 5.54, P ⫽ 0.480), R4 (2 ⫽ 11.74, P ⫽ 0.07), R5 (2 ⫽ 17.55, P ⫽ 0.480), R6 (2 ⫽ 31.3, P ⫽ 0.07), and R7 (2 ⫽ 27.88, P ⫽ 0.420). In contrast, in 2012,
relative abundance varied signiÞcantly across crop growth stages. Redbanded stink bug was the most abundant during R2 (2 ⫽ 57.15, P ⬍ 0.0001), R3 (2 ⫽ 53.91, P ⬍ 0.0001), R4 (2 ⫽ 75.18, P ⬍ 0.0001), R5 (2 ⫽ 139.21, P ⬍ 0.0001), R6 (2 ⫽ 240.21, P ⬍ 0.0001), and R7 (2 ⫽ 269.1, P ⬍ 0.0001) stages. Similarly, in 2013, relative abundance varied signiÞcantly during R2 (2 ⫽ 23.17, P ⫽ 0.0007), R3 (2 ⫽ 22.58, P ⫽ 0.007), R4 (2 ⫽ 25.38, P ⫽ 0.013), R6 (2 ⫽ 66.16, P ⫽ 0.004), and R7 (2 ⫽ 80.96, P ⫽ 0.002). At R5, no signiÞcant difference was observed in numbers of individuals of each species collected (2 ⫽ 23.13, P ⫽ 0.08). Mean number of stink bugs per 25 sweeps were least at R2 while they were highest during R7 stage of soybean for all four stink bug species (Table 1). In addition, the proportion of stink bug nymphs and adults varied across soybean growth stages (Table 2; Fig. 3). For the redbanded stink bug, the percentage of adults was signiÞcantly higher than the percentage of nymphs at R2 (2 ⫽ 44.08, P ⬍ 0.0001), R3 (2 ⫽ 17.84, P ⫽ 0.0005), and R4 (2 ⫽ 12.122, P ⫽ 0.0165). However, as the crop progressed toward maturity, numbers of nymphs per adult increased gradually. As a result, there were no signiÞcant differences between the percentage of adults and nymphs collected at R5 (2 ⫽ 8.250, P ⫽ 0.409) and R6 (2 ⫽ 28.70, P ⫽ 0.094). At R7, the percentage of redbanded stink bug nymphs was signiÞcantly higher than the percentage of adults (2 ⫽ 32.21, P ⫽ 0.0412). In the southern green stink bug, the percentage of adults was signiÞcantly higher than the percentage of nymphs at R2 (2 ⫽ 10.740, P ⫽ 0.0047). As the crop progressed toward maturity, the number of nymphs per adult showed a gradual increase. Consequently, the percentage of southern green stink bug nymphs and adults did not vary signiÞcantly during R3 (2 ⫽ 5.957, P ⫽ 0.055), R4 (2 ⫽ 2.0892, P ⫽ 0.554), and R5 (2 ⫽ 0.494, P ⫽ 0.920). Nymph to adult ratio reached
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Fig. 2. Relative abundance of stink bugs collected across R2ÐR7 stage soybeans in Upper Gulf Coast of Texas during 2011 (A), 2012 (B), and 2013 (C).
its peak (1.85) at R6 when the percentage of nymphs was signiÞcantly higher than that of adults (2 ⫽ 22.520, P ⫽ 0.001). No signiÞcant difference in percentage of nymphs and adults was observed at R7 (2 ⫽ 10.87, P ⫽ 0.209). In the green stink bug, the percentage of adults was signiÞcantly higher than the percentage of nymphs at R2 (2 ⫽ 8.25, P ⫽ 0.041). The number of nymphs per Table 1. Crop stage 2011 R2 R3 R4 R5 R6 R7 2012 R2 R3 R4 R5 R6 R7 2013 R2 R3 R4 R5 R6 R7
adult increased gradually as the crop progressed toward maturity. Consequently, no signiÞcant differences were observed in their relative abundance during R3 (2 ⫽ 2.977, P ⫽ 0.084), R4 (2 ⫽ 4.23, P ⫽ 0.120), R5 (2 ⫽ 4.53, P ⫽ 0.209), R6 (2 ⫽ 2.041, P ⫽ 0.360), and R7 (2 ⫽ 6.387, P ⫽ 0.270). Finally, the percentage of brown stinkbug adults remained signiÞcantly higher than the percentage of
Mean number of stink bugs (nymphs and adults) per 25 sweeps ⴞ SEM across soybean growth stages Redbanded stink bug
Southern green stink bug
Brown stink bug
Green stink bug
0.50 ⫾ 0.11 0.60 ⫾ 0.13 1.00 ⫾ 0.22 1.95 ⫾ 0.44 3.05 ⫾ 0.68 3.85 ⫾ 0.56
0.10 ⫾ 0.02 0.35 ⫾ 0.08 0.70 ⫾ 0.16 1.50 ⫾ 0.34 2.00 ⫾ 0.45 2.50 ⫾ 0.56
0.65 ⫾ 0.15 0.55 ⫾ 0.12 1.10 ⫾ 0.25 1.35 ⫾ 0.30 1.15 ⫾ 0.26 1.90 ⫾ 0.42
0.60 ⫾ 0.13 0.25 ⫾ 0.06 0.75 ⫾ 0.17 1.55 ⫾ 0.35 0.90 ⫾ 0.20 1.85 ⫾ 0.41
0.35 ⫾ 0.06 0.70 ⫾ 0.11 1.85 ⫾ 0.29 7.00 ⫾ 1.11 22.90 ⫾ 3.62 18.33 ⫾ 2.90
0.10 ⫾ 0.02 0.35 ⫾ 0.06 0.40 ⫾ 0.06 0.85 ⫾ 0.13 3.85 ⫾ 0.61 6.60 ⫾ 1.04
0.35 ⫾ 0.06 0.45 ⫾ 0.07 0.40 ⫾ 0.06 0.60 ⫾ 0.09 0.65 ⫾ 0.10 1.00 ⫾ 0.16
0.00 ⫾ 0.00 0.05 ⫾ 0.01 0.35 ⫾ 0.06 0.75 ⫾ 0.12 0.60 ⫾ 0.09 0.50 ⫾ 0.08
0.60 ⫾ 0.07 0.64 ⫾ 0.09 0.73 ⫾ 0.13 1.45 ⫾ 0.32 5.87 ⫾ 1.07 13.15 ⫾ 2.94
0.29 ⫾ 0.03 0.60 ⫾ 0.08 0.73 ⫾ 0.13 0.95 ⫾ 0.21 1.93 ⫾ 0.35 2.70 ⫾ 0.60
0.13 ⫾ 0.02 0.33 ⫾ 0.04 0.40 ⫾ 0.07 0.60 ⫾ 0.13 1.07 ⫾ 0.19 1.30 ⫾ 0.29
0.01 ⫾ 0.00 0.22 ⫾ 0.03 0.13 ⫾ 0.02 0.35 ⫾ 0.08 0.53 ⫾ 0.10 0.60 ⫾ 0.13
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Table 2. Ratio of stink bug nymphs to adults across soybean growth stages (2011–2013) Crop stage R2 R3 R4 R5 R6 R7
Ratio of nymphs to adults Redbanded stink bug
Southern green stink bug
Brown stink bug
Green stink bug
0.26 0.45 0.55 0.93 1.30 1.41
0.31 0.53 0.82 1.11 1.85 1.59
0.07 0.34 0.45 0.51 0.98 1.03
0.00 0.50 0.50 0.59 0.82 0.64
nymphs during R2 (2 ⫽ 27.899, P ⬍ 0.0001), R3 (2 ⫽ 14.224, P ⫽ 0.0008), R4 (2 ⫽ 10.1433, P ⫽ 0.006), and R5 (2 ⫽ 8.825, P ⫽ 0.031). During R6 (2 ⫽ 5.083, P ⫽ 0.165) and R7 (2 ⫽ 4.877, P ⫽ 0.181), no signiÞcant difference was observed in the percentage of brown stink bug adults and nymphs. Interestingly, although the mean abundance of stink bugs was found to vary substantially across soybean growth stages, very few samples reached the economic threshold (i.e., 8 stink bugs per 25 sweeps) during R2ÐR4 (Table 3). However, during later growth stages (R5ÐR7), the majority of samples were found to have stink bug densities at or above economic threshold. The highest percentage of samples with stink bug populations at or above the economic threshold occurred during R7. In 2011, 2012, and 2013, 75, 100, and 85% of our samples collected at R7 contained stink bug numbers at or above the economic threshold, respectively. At R6, 45, 100, and 50% of our samples contained stink bug numbers at or above the economic threshold during the same years. Overall, redbanded stink bug density reached the economic threshold in 21% of the samples, while southern green stink bug reached the economic threshold in only 3%
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Table 3. Percentage of samples in which stink bug counts reached economic threshold (ET) Crop stage R2 R3 R4 R5 R6 R7
Percentage of samples at or above ET (8 stink bugs/25 sweeps) 2011
2012
2013
0 0 0 40 45 75
0 3 5 60 100 100
0 2 0 10 50 85
Percentages include nymphs and adults of redbanded stink bug, southern green stink bug, brown stink bug, and green stink bug.
of our samples. Brown stink bug and green stink bug never reached threshold levels. Discussion Earlier surveys done in soybean Þelds in Texas had never reported the occurrence of redbanded stink bug. A survey done during 1981Ð1983 in soybean in south eastern Texas reported southern green stink bug as the most abundant stink bug species (Drees and Rice 1990). Our study shows that the redbanded stink bug is now the most abundant stink bug species in Texas soybean. Similarly, in Louisiana soybean, the redbanded stink bug was never reported in surveys done before 2000. However, currently the redbanded stink bug is the most abundant stink bug species in Louisiana soybean (Temple et al. 2013). The shift in the composition and relative abundance of the stink bug complex in these states calls for a revised economic threshold for the stink bug complex (McPherson et al. 1994). The currently used economic threshold for the soybean stink bug complex has limitations,
Fig. 3. Percentage of nymphs and adults of four stink bug species: redbanded stink bug, southern green stink bug, brown stink bug, and green stink bug across R2ÐR7 soybean growth stages in the Upper Gulf Coast of Texas, 2011Ð2013.
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as it is based on outdated data which excludes redbanded stink bug. Only Louisiana and Mississippi have lowered their action threshold for stink bugs from nine to six stink bugs per 25 sweeps due to the occurrence and damage potential of redbanded stink bug (Baur and Baldwin 2006). All other states have action thresholds based upon historical data when the stink bug complex was mainly composed by southern green stink bug, green stink bug, and brown stink bug (McPherson et al. 1994). Our study shows that redbanded stink bug alone represented ⬎65% of the stink bugs found in our samples from 2011 to 2013, while southern green stink bug, brown stink bug, and green stink bug altogether accounted for ⬍35%. The redbanded stink bug is not only more damaging than other phytophagous stink bug species (CorreaFerreira and de Azevedo 2002) but also more tolerant to insecticides available for stink bug control on soybeans (Davis et al. 2011). As a result, insecticide applications have increased in regions where redbanded stink bug has become a soybean pest. For example, the average number of insecticide applications in Louisiana soybean has increased from one or two per season during the late 1990s to three to Þve per season in 2013, with the bulk of those targeting redbanded stink bug (Temple et al. 2011). Similarly, the relatively recent predominance of redbanded stink bug in Texas, has been responsible for a signiÞcant increase in the amount of insecticides applied in soybean (S.S.V. and M.O.W., unpublished data). Under these circumstances, insecticide resistance is possible. Increased insecticide use may also have negative impacts on natural enemies and may increase soybean production costs. Because susceptibility to insecticides varies with stink bug developmental stages, knowing the relative abundance of less mobile immatures and more mobile adult stink bugs across soybean growth stages may impact the efÞciency of insecticide applications. For example, knowing proportions of stink bug nymphs and adults could aid in selecting insecticides, especially insect growth regulators (IGRs) that selectively target particular insect developmental stages. This knowledge can also impact timings of insecticide applications especially for insecticides such as IGRs that need to be applied when insects are still in susceptible developmental stages. It is not clear why redbanded stink bug geographic range has expanded since the Þrst report of this insect in the United States in the 1960s (Panizzi and Slansky 1985c). It is also unclear what has caused the rise in redbanded stink bug populations resulting in this insect becoming the most serious pest of soybean in Louisiana and Texas in recent years. The predominance of redbanded stink bug in Texas and Louisiana soybeans could be due to higher rates of reproduction of this insect when compared with other stink bugs. Alternatively, differences in insecticide resistance between the redbanded stink bug and the other stink bugs commonly present in soybean, may explain the dramatic increase in redbanded stink bug populations. Greater insecticide susceptibility of southern green
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stink bug, brown stink bug, and green stink bug as compared with redbanded stink bug, may make it difÞcult for them to compete with redbanded stink bug, which might displace them from the crop. Thus, more research needs to be conducted to fully understand the geographic expansion and increased abundance of redbanded stink bug and its interactions with other stink bug species in soybean. Acknowledgments We thank Herb Dishman, Randy Waligura, Ray Stoesser, Carey Orsack, and Brent Batchelor for assistance and cooperation with Þeld sites. Without their support we would not have been able to study insect populations under a commercial crop production environment. The Þnancial support for this study was provided by United Soybean Board grant 0000406770.
References Cited Baur, M., and J. Baldwin. 2006. Redbanded stink bugs trouble Louisiana. Louis. Agric. 48: 9 Ð10. Baur, M. E., D. J. Boethel, M. L. Boyd, G. R. Bowers, M. O. Way, L. G. Heatherly, J. Rabb, and L. Ashlock. 2000. Arthropod populations in early soybean production systems in the Mid-South. Environ. Entomol. 29: 312Ð328. Correa-Ferreira, B. S., and J. de Azevedo. 2002. Soybean seed damage by different species of stink bugs. Agric. For. Entomol. 4: 145Ð150. Davis, J. A., K. L. Kamminga, A. R. Richter, and B. R. Leonard. 2011. New integrated pest management strategies for stink bug control in Louisiana soybean. Louis. Agric. (http:// text.lsuagcenter.com/en/communications/publications/ agmag/Archive/2011/Spring/New-Integrated-PestManagement-Strategies-for-Stink-Bug-Control-inLouisiana-Soybean.htm). Drees, B. M., and M. E. Rice. 1990. Population dynamics and seasonal occurrence of soybean insect pests in southeastern Texas. Southwest. Entomol. 15: 49Ð56. Fehr, W. R., and C. E. Caviness. 1977. Stages of soybean development. Special report 80, Iowa State University Co-operative Extension Series, Ames, IA. Genung, W. G., E. Green Jr., and C. Welberg. 1964. Interrelationship of stinkbugs and diseases to Everglades soybean production. Proc. Soil Crop Sci. Soc. Fla. 24: 131Ð 137. Gouge, D. H., M. O. Way, A. Knuston, G. Cronholm, C. Patrick. 1999. Managing soybean insects. Texas Agriculture Extension Series College Station, TX. (https://insects. tamu.edu/extension/bulletins/b-1501.html#Soybean). Greene, J. K., and G. A. Herzog. 1999. Management of stink bugs using symptoms of boll injury as a monitoring tool, pp. 1041Ð1044. In Proceedings of the Beltwide Cotton Conference, 3Ð7 January 1999, Orlando, FL. National Cotton Council, Memphis, TN. Heatherly, L. 2005. Mid-south soybean yield trends up. Delta Farm Press. (http://deltafarmpress.com/midsouth-soybean-yield-trends). Jones, W. A., and M. J. Sullivan. 1982. Role of host plants in population dynamics of stink bug (Hemiptera, Pentatomidae) pests of soybean in South Carolina. Environ. Entomol. 11: 867Ð 875. Kamminga, K., D. A. Herbert, S. Malone, T. P. Kuhar, and G. J. 2009. Field guide to stink bugs of agricultural importance in the Upper Southern Region and Mid-Atlantic
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States. (https://pubs.ext.vt.edu/444/444 Ð356/444 Ð356_ pdf.pdf). Kogan, M., and S. G. Turnipseed. 1987. Ecology and management of soybean arthropods. Annu. Rev. Entomol. 32: 507Ð538. McPherson, J. E., and R. M. McPherson. 2000. Stink bugs of econonric importance in America north of Mexico. CRC, Boca Raton, FL. McPherson, R. M., G. K. Douce, and R. D. Hudson. 1993. Annual variation in stink bug (Heteroptera: Pentatomidae) seasonal abundance and species composition in Georgia soybean and its impact on yield and quality. J. Entomol. Sci. 28: 61Ð72. McPherson, R. M., J. B. Graves, and T. A. Allain. 1979a. Dosage mortality responses and Þeld control of seven pentatomids associated with soybean, exposed to methyl parathion. Environ. Entomol. 8: 1041Ð1043. McPherson, R. M., L. D. Newsom, and B. F. Farthing. 1979b. Evaluation of four stink bug species(Heteroptera,Pentatomidae) from 3 genera affecting soybean yield and quality in Louisiana. J. Econ. Entomol. 72: 188 Ð194. McPherson, R. M., J. W. Todd., and K. V. Yeargan. 1994. Stink bugs, pp. 87Ð90. In L. G. Highley and D. J. Boethel (eds.), Handbook of soybean insect pests. ESA, Lanham, MD. Menezes, E. B. 1981. Population dynamics of the stink bug (Hemiptera: Pentatomidae) complex on soybean and comparison of two relative methods of sampling. Ph.D. dissertation, University of Florida, Gainesville. Miner, F. D. 1966. Biology and control of stinkbugs on soybeans. Arkansas Agriculture Experiment Station Bulletin 708, Little Rock, AR. Musser, F. R., A. L. Catchot, B. K. Gibson, and K. S. Knighten. 2011. Economic injury levels for southern green stink bugs (Hemiptera: Pentatomidae) in R7 growth stage soybeans. Crop Prot. 30: 63Ð 69. Panizzi, A. P. 1997. Wild hosts of Pentatomids: Ecological signiÞcance and role in their pest status on crops. Annu. Rev. Entomol. 42: 99 Ð122. Panizzi, A. R., and F. Slansky. 1985a. Legume host impact on performance of adult Piezodorus guildinii (Westwood) (Hemiptera, Pentatomidae). Environ. Entomol. 14: 237Ð242. Panizzi, A. R., and F. Slansky. 1985b. New host plant records for the stink bug Piezodorus guildinii in Florida (Hemiptera, Pentatomidae). Fla. Entomol. 68: 215Ð216. Panizzi, A. R., and F. Slansky. 1985c. Review of phytophagous pentatomids (Hemiptera, Pentatomidae) associated with soybean in the Americas. Fla. Entomol. 68: 184 Ð214. Panizzi, A. R., M.H.M. Galileo, H.A.O. Gastal, J.F.F. Toledo, and C. H. Wild. 1980. Dispersal of Nezara viridula Hemiptera, Pentatomidae and Piezodorus guildinii Hemiptera, Pentatomidae nymphs in soybeans. Environ. Entomol. 9: 293Ð297.
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Panizzi, A. R., J. E. McPherson., D. G. James., M. Javahery., and R. M. McPherson. 2000. Stink bugs (Pentatomidae), pp. 421Ð474. In C. W. Schaefer and A. R. Panizzi (eds.), Heteroptera of economic importance. CRC, Boca Raton, FL. Rudd, W. G., and R. L. Jensen. 1977. Sweep net and ground cloth sampling for insects in spybeans. J. Econ. Entomol. 70: 301Ð304. SAS Institute. 2010. SAS/STAT userÕs guide, version 9.4. SAS Institute, Cary, NC. Simmons, A. M., and K. V. Yeargan. 1988. Feeding frequency and feeding duration of the green stink bug (Hemiptera: Pentatomidae) on soybean. J. Econ. Entomol. 81: 812Ð 815. Smith, J. F., R. G. Luttrell, and J. K. Greene. 2009. Seasonal abundance, species composition, and population dynamics of stink bugs in production Þelds of early and late soybean in South Arkansas. J. Econ. Entomol. 102: 229 Ð 236. Stoner, D. 1922. Report on the Scutelleroidea collected by the Barbados-Antigua expedition from the University of Iowa in 1918. Univ. Iowa Stud. Nat. Hist. Iowa City, IA. (http://www.archive.org/stream/universityoÞowa10univ/ universityoÞowa10univ_djvu.txt). Temple, J. H., B. R. Leonard, J. Davis, and K. Fontenot. 2009. Insecticide efÞcacy against red banded stink bug, Piezodorus guildinii (Westwood), a new stink bug pest of Louisiana soybean. Midsouth Entomol. 2: 68 Ð 69. Temple, J., J. A. Davis, J. Hardke, P. Price, S. Micinski, C. Cookson, A. Richter, and B. R. Leonard. 2011. Seasonal abundance and occurrence of the redbanded stink bug in Louisiana soybeans. Louis. Agric. (http://www.lsuagcenter. com/en/communications/publications/agmag/Archive/ 2011/Spring/Seasonal-Abundance-and-Occurrence-ofthe-Redbanded-Stink-Bug-in-Louisiana-Soybeans.htm). Temple, J. H., J. A. Davis, S. Micinski, J. T. Hardke, P. Price, and B. R. Leonard. 2013. Species composition and seasonal abundance of stink bugs (Hemiptera: Pentatomidae) in Louisiana soybean. Environ. Entomol. 42: 648Ð657. Tindall, K. V., and K. Fothergill. 2011. First records of Piezodorus guildinii in Missouri. Southwest. Entomol. 36: 203Ð205. Turnipseed, S. G., and M. Kogan. 1976. Soybean entomology. Annu. Rev. Entomol. 21: 247Ð282. Vyavhare, S., and M. O. Way. 2013. Populations of Redbanded Stink Bug on Durana Clover and Soybean. (https://beaumont.tamu.edu/elibrary/Newsletter/2013_ Highlights_in_Research.pdf). Willrich, M. W., B. R. Leonard, and D. R. Cook. 2003. Laboratory and Þeld evaluations of insecticide toxicity to stink bugs (Heteroptera: Pentatomidae). J. Cott. Sci. 7: 156 Ð163. Received 7 March 2014; accepted 8 September 2014.
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SAMPLING
Stink Bug Species Composition and Relative Abundance of the Redbanded Stink Bug (Hemiptera: Pentatomidae) in Soybean in the Upper Gulf Coast Texas SUHAS S. VYAVHARE,1 MICHAEL O. WAY,2
AND
RAUL F. MEDINA1,3
Environ. Entomol. 43(6): 1621Ð1627 (2014); DOI: http://dx.doi.org/10.1603/EN14059
ABSTRACT Stink bugs are the primary arthropod soybean pests in the southern United States. Historically, important stink bug species damaging soybeans in the southern United States included the southern green stink bug Nezara viridula (L.), the green stink bug Chinavia hilaris (Say), and the brown stink bug Euschistus servus (Say) (Hemiptera: Pentatomidae). The redbanded stink bug, Piezodorus guildinii (Westwood), has recently become an economic pest of soybean in the southern region of the United States, especially in Louisiana and Texas. Little is known about current stink bug species composition and relative abundance in Texan soybean agro-ecosystems. To Þll this gap, commercial soybean Þelds in the Upper Gulf Coast of Texas were sampled weekly during the growing season using a sweep net throughout R2 (full ßowering) to R7 (beginning maturity) from 2011 to 2013. Adults and nymphs (third, fourth, and Þfth instars) of redbanded stink bug, southern green stink bug, green stink bug, and brown stink bug were counted per 25 sweeps. The relative abundance of redbanded stink bug was signiÞcantly higher than any other stink bug species throughout 2011Ð2013. Over 65% of the total population of major stink bugs collected during this period were redbanded stink bugs and ⬇19% were southern green stink bugs. The highest redbanded stink bug densities and the highest ratio of redbanded stink bug nymphs to adults were recorded at R7. Results from this study show that redbanded stink bug has become the predominant stink bug species in soybean in the Upper Gulf Coast of Texas. KEY WORDS Piezodorus guildinii, species composition, relative abundance
Stink bugs are polyphagous pests that feed on a wide range of cultivated crops including cotton (Gossypium hirsutum L.), soybean (Glycine max (L.) Merrill), and corn (Zea mays L.; Panizzi 1997). They also feed on a variety of wild and nonagronomic hosts (Panizzi 1997). Stink bugs have recently become primary pests of soybean in the southern United States (Drees and Rice 1990, Baur et al. 2000). The upsurge in stink bug populations in the southern United States is believed to be due to reduced number of insecticide sprays in cotton as a result of adoption of Bt crops combined with the boll weevil eradication program (Greene and Herzog 1999). Also, a shift in soybean production from May-planted maturity group (MG) V and VI in conventional soybean production systems to Aprilplanted MG III and IV in early season soybean production, may have contributed to stink bug population growth in recent years (Heatherly 2005). The increased pressure of stink bugs on early planted soybeans may be due to the early availability of pods (Baur et al. 2000). After colonizing early-planted soy1 Department of Entomology, Texas A&M University, 2475 TAMU College Station, TX 77843. 2 Texas A&M AgriLife Research and Extension Center, 1509 Aggie Dr., Beaumont, TX 77713. 3 Corresponding author, e-mail: [email protected].
beans, stink bugs successively move to later planted soybeans as the developing pods become available (Baur et al. 2000). Historically, the three key stink bug species viz. the southern green stink bug, Nezara viridula L.; the green stink bug, Chinavia hilaris Say; and the brown stink bug, Euschistus servus Say, have been known to be of substantial economic importance throughout the southern United States (McPherson et al. 1993). In the past, southern green stink bug, the most cosmopolitan of the pentatomids attacking soybean, has represented the highest proportion of all stink bug species in soybean Þelds from Texas in the west through southern Arkansas to Virginia in the east (Turnipseed and Kogan 1976). However, during the past decade, the redbanded stink bug, Piezodorus guildinii Westwood, has become more common than any other stink bug species in Louisiana (Temple et al. 2011) and may pose a threat to soybean production in other southern states. The redbanded stink bug was Þrst reported on the island of St. Vincent (Stoner 1922) and has been a serious pest of soybean in the Neotropics since the 1960s (Panizzi et al. 2000). In the late 1970s, redbanded stink bug began replacing southern green stink bug on Brazilian soybeans (Turnipseed and Kogan 1976, Kogan and Turnipseed 1987). The expan-
0046-225X/14/1621Ð1627$04.00/0 䉷 2014 Entomological Society of America
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sion of soybean cultivation in South America during the 1960s and 1970s could be the principal reason for the increase in redbanded stink bug populations (Panizzi and Slansky 1985a). Consequently, most of the information available about redbanded stink bug impact on soybean comes from Brazil (Panizzi et al. 1980; Panizzi and Slansky 1985a, b, c). In the United States, redbanded stink bug was Þrst reported in the 1960s in Florida (Genung et al. 1964). It was frequently observed in low numbers in Florida and Georgia in the1980s (Panizzi and Slansky 1985c), but it was never considered as an economic pest of soybeans until the late 1990s. Since its Þrst report in the United States, redbanded stink bug has expanded its distribution from Florida (Menezes 1981) to South Carolina (Jones and Sullivan 1982), Georgia (McPherson et al. 1993), Arkansas (Smith et al. 2009), Louisiana (Temple et al. 2009, 2013), and Missouri (Tindall and Fothergill 2011). IdentiÞcation and characterization of the species involved in the stink bug complex is important in designing proper management tactics. This is because different species within the stink bug complex have different damage potentials. For example, redbanded stink bug in soybean causes more damage per insect than any other stink bug species (Correa-Ferreira and de Azevedo 2002) while southern green stink bug and green stink bug cause similar damage, and brown stink bug cause comparatively less damage (Miner 1966, McPherson et al. 1979b). Nevertheless, the economic threshold level is the same for all these species in many of the soybean-producing states in United States including Texas, where redbanded stink bug populations have recently reached damaging levels (Vyavhare and Way 2013). No extensive Þeld surveys have been conducted to understand the current composition of stink bug species in Texas soybean. In Texas, an economic threshold of 8 stink bugs per 25 sweeps (38.1-cm-diameter sweep net) is used for the stink bug pest complex throughout all reproductive stages of soybean (Gouge et al. 1999). Although it is common to Þnd multiple stink bug species in the Þeld, little is known about how to incorporate species composition into considerations aimed at justifying use of chemical control against this pest complex. Also, it is important to understand the relative abundance of stink bug nymphs versus adults across different crop growth stages because the amount of injury per individual varies from nymphs to adults and the vulnerability of soybean to stink bug damage vary with plant growth stages. For example, both quality and yield loss are most affected when soybeans are exposed to stink bug feeding during R5ÐR6 (Fehr and Caviness 1977) while damage at R7 is much less than at earlier stages (McPherson et al. 1979b, Musser et al. 2011). Currently, stink bug control in soybean is mainly dependent on chemical applications (Davis et al. 2011). Susceptibility to insecticides has been reported to vary among stink bug species and life stages (McPherson et al. 1979a). For example, pyrethroids are more effective against southern green stink bug and green stink bug than against brown stink bug (Willrich et al. 2003). Also, LD50 values of methyl
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parathion for Þfth-instar nymphs of southern green stink bug, green stink bug, and brown stink bug are higher than for their corresponding adults (McPherson et al. 1979a). Therefore, knowledge of stink bug species involved, their relative abundance, and proportion of stink bug developmental stages across crop growth stages is needed. The occurrence of redbanded stink bug populations in Texas has been responsible for a substantial increase in the amount of insecticides applied to soybean (S.S.V. and M.O.W., unpublished data). This increase in chemical control threatens beneÞcial organisms in the soybean agro-ecosystem and could result in the development of insecticide resistance. The goals of this study were 1) to determine the predominant stink bug species and its abundance relative to other commonly known stink bug pest species in the Upper Gulf Coast of Texas and 2) to determine the relative abundance of stink bug nymphs and adults across R2ÐR6 stages of soybean. Materials and Methods Stink Bug Collection. Densities of stink bug species were monitored from 2011 to 2013 in commercial soybean Þelds across the Upper Gulf Coast of Texas. Each year Þve soybean Þelds under irrigated condition were chosen for the study. In 2011, study Þelds were located in Jefferson, Matagorda, Colorado, and Liberty Counties. In 2012, all Þelds were in Jefferson County. In 2013 soybean Þelds in Jefferson, Liberty, and Wharton counties were sampled. Soybeans in study Þelds represented primarily MG IV, V, and VI. Because the selected soybean Þelds were commercial, the breadth of conditions surveyed (i.e., Þeld sizes, varieties, seeding rates, plant spacing, etc.) varied substantially throughout the survey. Dates of seeding varied from mid-April to early-June depending on the soybean maturity groups. Fields were kept insecticide-free and sampled at weekly intervals from R2 (full ßowering) to R7 (beginning maturity) soybean growth stages (Fehr and Caviness 1977). Sampling began in mid-June and continued weekly through early October with Þve sets of 25 sweeps (38.1-cmdiameter sweep net) taken at random locations in each soybean Þeld on each sample date. Insect sampling was done by swinging the sweep net through the top of the canopy (Rudd and Jensen 1977). Each sample consisted of stink bugs collected in 25 consecutive sweeps taken in a row while walking forward. After collection, stink bugs were separated from foliage and placed in plastic zip-lock bags and brought to the laboratory. Plastic bags containing insects were stored at 3⬚C for further processing. Laboratory processing included identiÞcation of stink bug species and counting of nymphs (third, fourth, and Þfth instars only) and adults of each stink bug species found per sample. First and second nymphal instars were not included in counts because their impact on soybean damage is negligible (Simmons and Yeargan 1988). Stink bug species and developmental stages were identiÞed using diagnostic keys (McPherson and McPherson 2000, Kamminga et al. 2009). Only the
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VYAVHARE ET AL.: ABUNDANCE OF REDBANDED STINK BUG
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Fig. 1. Stink bug species composition across years (2011Ð2013) sampled from commercial soybean Þelds in Upper Gulf Coast region of Texas. Abundance of redbanded stink bugs was signiÞcantly higher every year.
number of redbanded stink bug, southern green stink bug, green stink bug, and brown stink bug from each sample were recorded. Sweep net samples also showed other minor pentatomid pest species such as Thyanta accera, Edessa bifida, Oebalus pugnax, Chlorochroa ligata, and the beneÞcial Podisus maculiventris. However, because the number of each of these species was negligible, relative abundances of each of the stink bug species considered in this study does not include these minor species in the denominator. Voucher specimens of each of the main stink bug species are kept in the Texas A&M University insect museum. Chi-square analysis was used to compare predominant stink bug species collected by year using PROC FREQ (SAS Institute 2010). Sampled Þelds were all located in the Upper Gulf Coast of Texas. Results Eighty-six percent of our Þeld samples (each sample ⫽ 25 sweeps) collected over 3 yr contained at least one of the major stink bug species (i.e., redbanded stink bug, southern green stink bug, green stink bug, or brown stink bug). Redbanded stink bug was the most abundant species consistently during 2011 (2 ⫽ 41.24, P ⫽ 0.04), 2012 (2 ⫽ 491.74, P ⬍ 0.0001), and 2013 (2 ⫽ 175.19, P ⬍ 0.0001; Fig. 1). Out of the major stink bug species collected (N ⫽ 4269) over our 3-yr Þeld survey, 65% were redbanded stink bug, followed by southern green stink bug (19%), brown stink bug (9%), and green stink bug (6%). The relative abundance of the major stink bug species varied depending on soybean growth stage (Fig. 2). In 2011, no signiÞcant differences were observed in relative abundance during R2 (2 ⫽ 15.06, P ⫽ 0.089), R3 (2 ⫽ 5.54, P ⫽ 0.480), R4 (2 ⫽ 11.74, P ⫽ 0.07), R5 (2 ⫽ 17.55, P ⫽ 0.480), R6 (2 ⫽ 31.3, P ⫽ 0.07), and R7 (2 ⫽ 27.88, P ⫽ 0.420). In contrast, in 2012,
relative abundance varied signiÞcantly across crop growth stages. Redbanded stink bug was the most abundant during R2 (2 ⫽ 57.15, P ⬍ 0.0001), R3 (2 ⫽ 53.91, P ⬍ 0.0001), R4 (2 ⫽ 75.18, P ⬍ 0.0001), R5 (2 ⫽ 139.21, P ⬍ 0.0001), R6 (2 ⫽ 240.21, P ⬍ 0.0001), and R7 (2 ⫽ 269.1, P ⬍ 0.0001) stages. Similarly, in 2013, relative abundance varied signiÞcantly during R2 (2 ⫽ 23.17, P ⫽ 0.0007), R3 (2 ⫽ 22.58, P ⫽ 0.007), R4 (2 ⫽ 25.38, P ⫽ 0.013), R6 (2 ⫽ 66.16, P ⫽ 0.004), and R7 (2 ⫽ 80.96, P ⫽ 0.002). At R5, no signiÞcant difference was observed in numbers of individuals of each species collected (2 ⫽ 23.13, P ⫽ 0.08). Mean number of stink bugs per 25 sweeps were least at R2 while they were highest during R7 stage of soybean for all four stink bug species (Table 1). In addition, the proportion of stink bug nymphs and adults varied across soybean growth stages (Table 2; Fig. 3). For the redbanded stink bug, the percentage of adults was signiÞcantly higher than the percentage of nymphs at R2 (2 ⫽ 44.08, P ⬍ 0.0001), R3 (2 ⫽ 17.84, P ⫽ 0.0005), and R4 (2 ⫽ 12.122, P ⫽ 0.0165). However, as the crop progressed toward maturity, numbers of nymphs per adult increased gradually. As a result, there were no signiÞcant differences between the percentage of adults and nymphs collected at R5 (2 ⫽ 8.250, P ⫽ 0.409) and R6 (2 ⫽ 28.70, P ⫽ 0.094). At R7, the percentage of redbanded stink bug nymphs was signiÞcantly higher than the percentage of adults (2 ⫽ 32.21, P ⫽ 0.0412). In the southern green stink bug, the percentage of adults was signiÞcantly higher than the percentage of nymphs at R2 (2 ⫽ 10.740, P ⫽ 0.0047). As the crop progressed toward maturity, the number of nymphs per adult showed a gradual increase. Consequently, the percentage of southern green stink bug nymphs and adults did not vary signiÞcantly during R3 (2 ⫽ 5.957, P ⫽ 0.055), R4 (2 ⫽ 2.0892, P ⫽ 0.554), and R5 (2 ⫽ 0.494, P ⫽ 0.920). Nymph to adult ratio reached
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Fig. 2. Relative abundance of stink bugs collected across R2ÐR7 stage soybeans in Upper Gulf Coast of Texas during 2011 (A), 2012 (B), and 2013 (C).
its peak (1.85) at R6 when the percentage of nymphs was signiÞcantly higher than that of adults (2 ⫽ 22.520, P ⫽ 0.001). No signiÞcant difference in percentage of nymphs and adults was observed at R7 (2 ⫽ 10.87, P ⫽ 0.209). In the green stink bug, the percentage of adults was signiÞcantly higher than the percentage of nymphs at R2 (2 ⫽ 8.25, P ⫽ 0.041). The number of nymphs per Table 1. Crop stage 2011 R2 R3 R4 R5 R6 R7 2012 R2 R3 R4 R5 R6 R7 2013 R2 R3 R4 R5 R6 R7
adult increased gradually as the crop progressed toward maturity. Consequently, no signiÞcant differences were observed in their relative abundance during R3 (2 ⫽ 2.977, P ⫽ 0.084), R4 (2 ⫽ 4.23, P ⫽ 0.120), R5 (2 ⫽ 4.53, P ⫽ 0.209), R6 (2 ⫽ 2.041, P ⫽ 0.360), and R7 (2 ⫽ 6.387, P ⫽ 0.270). Finally, the percentage of brown stinkbug adults remained signiÞcantly higher than the percentage of
Mean number of stink bugs (nymphs and adults) per 25 sweeps ⴞ SEM across soybean growth stages Redbanded stink bug
Southern green stink bug
Brown stink bug
Green stink bug
0.50 ⫾ 0.11 0.60 ⫾ 0.13 1.00 ⫾ 0.22 1.95 ⫾ 0.44 3.05 ⫾ 0.68 3.85 ⫾ 0.56
0.10 ⫾ 0.02 0.35 ⫾ 0.08 0.70 ⫾ 0.16 1.50 ⫾ 0.34 2.00 ⫾ 0.45 2.50 ⫾ 0.56
0.65 ⫾ 0.15 0.55 ⫾ 0.12 1.10 ⫾ 0.25 1.35 ⫾ 0.30 1.15 ⫾ 0.26 1.90 ⫾ 0.42
0.60 ⫾ 0.13 0.25 ⫾ 0.06 0.75 ⫾ 0.17 1.55 ⫾ 0.35 0.90 ⫾ 0.20 1.85 ⫾ 0.41
0.35 ⫾ 0.06 0.70 ⫾ 0.11 1.85 ⫾ 0.29 7.00 ⫾ 1.11 22.90 ⫾ 3.62 18.33 ⫾ 2.90
0.10 ⫾ 0.02 0.35 ⫾ 0.06 0.40 ⫾ 0.06 0.85 ⫾ 0.13 3.85 ⫾ 0.61 6.60 ⫾ 1.04
0.35 ⫾ 0.06 0.45 ⫾ 0.07 0.40 ⫾ 0.06 0.60 ⫾ 0.09 0.65 ⫾ 0.10 1.00 ⫾ 0.16
0.00 ⫾ 0.00 0.05 ⫾ 0.01 0.35 ⫾ 0.06 0.75 ⫾ 0.12 0.60 ⫾ 0.09 0.50 ⫾ 0.08
0.60 ⫾ 0.07 0.64 ⫾ 0.09 0.73 ⫾ 0.13 1.45 ⫾ 0.32 5.87 ⫾ 1.07 13.15 ⫾ 2.94
0.29 ⫾ 0.03 0.60 ⫾ 0.08 0.73 ⫾ 0.13 0.95 ⫾ 0.21 1.93 ⫾ 0.35 2.70 ⫾ 0.60
0.13 ⫾ 0.02 0.33 ⫾ 0.04 0.40 ⫾ 0.07 0.60 ⫾ 0.13 1.07 ⫾ 0.19 1.30 ⫾ 0.29
0.01 ⫾ 0.00 0.22 ⫾ 0.03 0.13 ⫾ 0.02 0.35 ⫾ 0.08 0.53 ⫾ 0.10 0.60 ⫾ 0.13
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VYAVHARE ET AL.: ABUNDANCE OF REDBANDED STINK BUG
Table 2. Ratio of stink bug nymphs to adults across soybean growth stages (2011–2013) Crop stage R2 R3 R4 R5 R6 R7
Ratio of nymphs to adults Redbanded stink bug
Southern green stink bug
Brown stink bug
Green stink bug
0.26 0.45 0.55 0.93 1.30 1.41
0.31 0.53 0.82 1.11 1.85 1.59
0.07 0.34 0.45 0.51 0.98 1.03
0.00 0.50 0.50 0.59 0.82 0.64
nymphs during R2 (2 ⫽ 27.899, P ⬍ 0.0001), R3 (2 ⫽ 14.224, P ⫽ 0.0008), R4 (2 ⫽ 10.1433, P ⫽ 0.006), and R5 (2 ⫽ 8.825, P ⫽ 0.031). During R6 (2 ⫽ 5.083, P ⫽ 0.165) and R7 (2 ⫽ 4.877, P ⫽ 0.181), no signiÞcant difference was observed in the percentage of brown stink bug adults and nymphs. Interestingly, although the mean abundance of stink bugs was found to vary substantially across soybean growth stages, very few samples reached the economic threshold (i.e., 8 stink bugs per 25 sweeps) during R2ÐR4 (Table 3). However, during later growth stages (R5ÐR7), the majority of samples were found to have stink bug densities at or above economic threshold. The highest percentage of samples with stink bug populations at or above the economic threshold occurred during R7. In 2011, 2012, and 2013, 75, 100, and 85% of our samples collected at R7 contained stink bug numbers at or above the economic threshold, respectively. At R6, 45, 100, and 50% of our samples contained stink bug numbers at or above the economic threshold during the same years. Overall, redbanded stink bug density reached the economic threshold in 21% of the samples, while southern green stink bug reached the economic threshold in only 3%
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Table 3. Percentage of samples in which stink bug counts reached economic threshold (ET) Crop stage R2 R3 R4 R5 R6 R7
Percentage of samples at or above ET (8 stink bugs/25 sweeps) 2011
2012
2013
0 0 0 40 45 75
0 3 5 60 100 100
0 2 0 10 50 85
Percentages include nymphs and adults of redbanded stink bug, southern green stink bug, brown stink bug, and green stink bug.
of our samples. Brown stink bug and green stink bug never reached threshold levels. Discussion Earlier surveys done in soybean Þelds in Texas had never reported the occurrence of redbanded stink bug. A survey done during 1981Ð1983 in soybean in south eastern Texas reported southern green stink bug as the most abundant stink bug species (Drees and Rice 1990). Our study shows that the redbanded stink bug is now the most abundant stink bug species in Texas soybean. Similarly, in Louisiana soybean, the redbanded stink bug was never reported in surveys done before 2000. However, currently the redbanded stink bug is the most abundant stink bug species in Louisiana soybean (Temple et al. 2013). The shift in the composition and relative abundance of the stink bug complex in these states calls for a revised economic threshold for the stink bug complex (McPherson et al. 1994). The currently used economic threshold for the soybean stink bug complex has limitations,
Fig. 3. Percentage of nymphs and adults of four stink bug species: redbanded stink bug, southern green stink bug, brown stink bug, and green stink bug across R2ÐR7 soybean growth stages in the Upper Gulf Coast of Texas, 2011Ð2013.
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as it is based on outdated data which excludes redbanded stink bug. Only Louisiana and Mississippi have lowered their action threshold for stink bugs from nine to six stink bugs per 25 sweeps due to the occurrence and damage potential of redbanded stink bug (Baur and Baldwin 2006). All other states have action thresholds based upon historical data when the stink bug complex was mainly composed by southern green stink bug, green stink bug, and brown stink bug (McPherson et al. 1994). Our study shows that redbanded stink bug alone represented ⬎65% of the stink bugs found in our samples from 2011 to 2013, while southern green stink bug, brown stink bug, and green stink bug altogether accounted for ⬍35%. The redbanded stink bug is not only more damaging than other phytophagous stink bug species (CorreaFerreira and de Azevedo 2002) but also more tolerant to insecticides available for stink bug control on soybeans (Davis et al. 2011). As a result, insecticide applications have increased in regions where redbanded stink bug has become a soybean pest. For example, the average number of insecticide applications in Louisiana soybean has increased from one or two per season during the late 1990s to three to Þve per season in 2013, with the bulk of those targeting redbanded stink bug (Temple et al. 2011). Similarly, the relatively recent predominance of redbanded stink bug in Texas, has been responsible for a signiÞcant increase in the amount of insecticides applied in soybean (S.S.V. and M.O.W., unpublished data). Under these circumstances, insecticide resistance is possible. Increased insecticide use may also have negative impacts on natural enemies and may increase soybean production costs. Because susceptibility to insecticides varies with stink bug developmental stages, knowing the relative abundance of less mobile immatures and more mobile adult stink bugs across soybean growth stages may impact the efÞciency of insecticide applications. For example, knowing proportions of stink bug nymphs and adults could aid in selecting insecticides, especially insect growth regulators (IGRs) that selectively target particular insect developmental stages. This knowledge can also impact timings of insecticide applications especially for insecticides such as IGRs that need to be applied when insects are still in susceptible developmental stages. It is not clear why redbanded stink bug geographic range has expanded since the Þrst report of this insect in the United States in the 1960s (Panizzi and Slansky 1985c). It is also unclear what has caused the rise in redbanded stink bug populations resulting in this insect becoming the most serious pest of soybean in Louisiana and Texas in recent years. The predominance of redbanded stink bug in Texas and Louisiana soybeans could be due to higher rates of reproduction of this insect when compared with other stink bugs. Alternatively, differences in insecticide resistance between the redbanded stink bug and the other stink bugs commonly present in soybean, may explain the dramatic increase in redbanded stink bug populations. Greater insecticide susceptibility of southern green
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stink bug, brown stink bug, and green stink bug as compared with redbanded stink bug, may make it difÞcult for them to compete with redbanded stink bug, which might displace them from the crop. Thus, more research needs to be conducted to fully understand the geographic expansion and increased abundance of redbanded stink bug and its interactions with other stink bug species in soybean. Acknowledgments We thank Herb Dishman, Randy Waligura, Ray Stoesser, Carey Orsack, and Brent Batchelor for assistance and cooperation with Þeld sites. Without their support we would not have been able to study insect populations under a commercial crop production environment. The Þnancial support for this study was provided by United Soybean Board grant 0000406770.
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