Species Composition and Seasonal Abundance of Stink Bugs (Hemiptera: Pentatomidae) in Louisiana Soybean (2024)

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Abstract

Soybeans, Glycine max (L.) Merrill, is the leading oilseed crop consumed in the world (Wilcox 2004). In 2010, 31.3 million ha were planted in the United States with a production of 99 million tons. Louisiana is one of 31 states that produce soybeans in the United States and was ranked 18th in planted acreage for 2010. Soybean was the most abundantly planted crop in Louisiana during 2010, accounting for >445,000 ha with an average yield of 2,729 kg/ha (NASS 2011).

Soybeans grown in the southern United States are infested annually by a diverse complex of insects pests including velvetbean caterpillar, Anticarsia gemmatalis (Hübner), soybean looper, Chrysodeixis includens (Walker), corn earworm, Helicoverpa zea (Boddie), bean leaf beetle, Cerotoma trifurcata (Förster), lesser cornstalk borer, Elasmopalpus lignosellus (Zeller), threecornered alfalfa hopper, Spissistilus festinus (Say), and a complex of stink bug species (Funderburk et al. 1999). Among these insects, stink bugs are the most economically important pests infesting soybean in the southern United States. The predominant species include the green stink bug, Acrosternum hilare (Say); southern green stink bug, Nezara viridula L.; and brown stink bug, Euschistus servus (Say) (Funderburk et al. 1999). In a comprehensive survey of insect losses in mid-southern soybeans, Musser et al. (2010) found that stink bugs infested ≈80% of soybean acreage, caused losses of 126,000 tons in 2009, and were the primary insect pests in Arkansas, Mississippi, and Tennessee. Stink bugs were primary pests of Mississippi soybean from 2003 to 2009 with annual control costs ranging from 27 to US$49/ha (Musser and Catchot 2008; Musser et al. 2009, 2010).

Comprehensive surveys of stink bug species in soybean have been done across much of the southern soybean production region. During a 4 yr period in Georgia, McPherson et al. (1993) found that southern green stink bug, green stink bug, and brown stink bug comprised 98% of all species infesting soybean. Gore et al. (2006) reported southern green stink bug, green stink bug, and brown stink bug being the most abundant in Mississippi soybean, although Thyanta spp. were found in low numbers. During a southeast Texas survey (3 yr), southern green stink bug was the dominant species, but green stink bug; brown stink bug, Edessa bifida (Say); Euschistus crassus (Dallas); Euschistus ictericus L.; Euschistus quadrator Rolston; Oebalus pugnax (F.); Proxys punctulatus (Palisot); and Thyanta spp. were also recorded (Drees and Rice 1990). Smith et al. (2009) found southern green stink bug and brown stink bug to be the most abundant stink bug species in southern Arkansas soybean fields. In Louisiana, McPherson et al. (1979) reported four common species found in soybean including southern green stink bug, green stink bug; brown stink bug; and dusky stink bug, Euschistus tristigmus (Say). Boyd et al. (1997) and Peters et al. (2004) reported that the principal stink bug species were southern green stink bug, green stink bug, and brown stink bug, but southern green stink bug represented the highest proportion of the complex.

None of the previous comprehensive surveys mention the redbanded stink bug, Piezodorus guildinii (Westwood), in soybean. However, the redbanded stink bug has been reported previously in soybean across Florida, Georgia, New Mexico, and South Carolina but has not been considered an economic pest in those states (McPherson and McPherson 2000). During the last decade, this species has become more common across the soybean production region in Louisiana and surrounding states. This species was first reported in southern Louisiana during 2000 by crop consultants and Louisiana Cooperative Extension personnel (Baldwin 2004). By 2002, the redbanded stink bug exceeded the stink bug action threshold (9/25 sweeps) and justified the application of insecticide sprays on much of the soybean acreage in southern Louisiana (Baldwin 2004). Redbanded stink bugs now have been reported in all Louisiana soybean producing parishes at sufficient numbers to justify chemical control strategies. Before 2000, the redbanded stink bug had not been reported on Louisiana soybean and no voucher specimens collected in Louisiana were present in the Louisiana State Arthropod Museum. Therefore, the objective of this study was to determine the current species composition and seasonal abundance of stink bug species in Louisiana soybean.

Materials and Methods

Large plots (0.1–0.2 ha) of soybean representing three maturity groups (MG) were planted at three locations in 2008 including Baton Rouge, LA (Ben Hur Research Farm, southeast location), Alexandria, LA (Dean Lee Research Station, central location), and Winnsboro, LA (Macon Ridge Research Station, northeast location). In 2009 and 2010, additional locations were added including Jeanerette, LA (Iberia Research Station, southwest location) and Bossier City, LA (Red River Research Station, northwest location) for a total of five sites (Fig. 1). Cultivars representing the MG of soybean were planted (Table 1) during LSU AgCenter recommended planting dates and managed according to best agronomic practices at each location (Levy et al. 2011). Soybeans representing MG IV, V, and VI were planted at Alexandria, Baton Rouge, Bossier City, and Winnsboro. Maturity groups III, IV, and V were planted at the southernmost location, Jeanerette, according to typical production practices in that region. Native infestations of all species of arthropods were allowed to build within plots that were not treated with insecticides. Each large plot was divided into six equal size blocks. Each of the six blocks within a maturity group was sampled weekly from R1 (beginning bloom) to R8 (physiological maturity) with a standard (38 cm diameter) sweep net by taking six sets of 25 sweep samples (150 total/MG/wk). When plants within each plot reached R8, the plot was destroyed (harvested or mowed) and removed from the test area. Alternating rows were sampled within each block each week such that no single row was sampled more than once within a period of 4 wk.

On each sampling date, the soybean growth stages for each MG were recorded based on descriptions by Fehr et al. (1971). Each individual set of sweep net samples was bagged, labeled, taken to the laboratory, and frozen until it could be evaluated. Upon evaluation, samples were segregated by stink bug species and life stage (adult or ≥ second instar nymph) based on diagnostic keys from McPherson (1982) and McPherson and McPherson (2000). Data were summarized by species within each maturity group and sample location. The total number of all stink bugs within the pest complex was summarized by soybean growth stage within each MG at each sample location. For the purpose of summarizing these data, the southern green stink bug and green stink bug were combined and referred to as the “green complex.” All Euschistus species were combined and referred to as the “brown complex.” Other minor pentatomid pests (Thyanta accera, O. pugnax, E. bifida, and the beneficial Podisus maculiventris [Say]), representing <3.0% of all stink bugs sampled, were not summarized by MG or location. Chi-square analysis was used to determine predominant stink bug species collected by year and location within a year using PROC FREQ (SAS Institute 2003).

Results

From 2008–2010, 3,084 samples (77,100 sweeps) were taken from multiple soybean maturity groups at five geographical locations in Louisiana. During the study, a total of 13,146 stink bugs were captured and subsequently identified to species (Table 2). The dominant species were the redbanded stink bug (54.2%), southern green stink bug (27.1%), brown stink bug (6.6%), and green stink bug (5.5%). Other phytophagous pentatomids captured during the surveys included E. quadrator (1.6%), E. tristigmus (1.6%), T. accera (0.9%), O. pugnax (0.2%), E. bifida (0.1%), E. consperus (0.1%), and E. ictericus (0.1%). The spined soldier bug, P. maculiventris, a beneficial pentatomid, comprised 1.6% of the total stink bug population. The redbanded stink bug was the predominant stink bug species collected in all 3 yr (P < 0.0001).

In 2008, the redbanded stink bug was the primary species (χ²=159.8; P < 0.001) collected in all three MGs (IV, V, and VI) at the Baton Rouge (southeast) sample site (Fig. 2). Redbanded stink bug levels ranged from 68 to 79% across the three MGs and comprised 74% of total stink bugs collected at the Baton Rouge site during 2008. The green stink bug and brown stink bug complexes made up 21 and 5% of the total population, respectively, collected at Baton Rouge in 2008. At the Alexandria (central) location, the redbanded stink bug was the dominant species in MG IV (61%) and VI (47%) soybean while the green stink bug complex was most dominant in MG V (52%) soybean. Of the total stink bugs collected at Alexandria in 2008, the redbanded stink bug (50%) was the dominant species followed by the green stink bug complex (43%) and the brown stink bug complex (7%), however, redbanded stink bug numbers were not significantly different compared with the green complex (χ²=0.1; P < 0.72). At Winnsboro, the most northern site in 2008, the redbanded stink bug was the most abundant species in MG IV (83%) and MG V (68%) soybean while the green stink bug complex was most prevalent (52%) in MG VI soybean. Of the total stink bugs collected at Winnsboro in 2008, the redbanded stink bug and the green and brown stink bug complexes represented 69, 23, and 8%, respectively, of the total collections with redbanded populations significantly higher (χ²=546.1; P < 0.001).

In 2009, two additional surveys sites were added including Jeanerette, located in southwestern Louisiana, and Bossier City, located in northwestern Louisiana (Fig. 1). At Jeanerette (southwest), the redbanded stink bug was the dominant species (60–81%) (χ²=341.2; P < 0.001) collected in all MGs (III, IV, and V) (Fig. 3). The redbanded stink bug, green stink bug complex, and brown stink bug complex comprised 70, 22, and 8%, respectively, of the population collected at Jeanerette in 2009. At Baton Rouge, the redbanded stink bug was found to be the most abundant species (63–81%) (χ²=78.6; P < 0.001) of the stink bug complex in all MGs (IV, V, and VI). The redbanded stink bug, green stink bug complex, and brown stink bug complex made up 73, 9, and 18%, respectively. At Alexandria in 2009, the green stink bug complex (48%) was predominant in MG IV soybeans while the redbanded stink bug was dominant in MG V (58%) and MG VI (55%) soybeans. The redbanded stink bug (50%) was the primary stink bug species (χ²=20.8; P < 0.001) collected at Alexandria, followed by the green stink bug complex (40%) and the brown stink bug complex (8%). In Winnsboro, redbanded stink bug numbers ranged from 53 to 67% of the total population across MGs (VI, V, and VI). The redbanded stink bug (57%) was the dominant species (χ²=56.1; P < 0.001) followed by the green stink bug complex (36%), and brown stink bug complex (7%). During 2009, Bossier City (northwest), the green stink bug complex was most abundant in all MGs (IV=69%, V=61%, and VI=59%). The green stink bug complex (65%) was most prevalent (χ²=150.6; P < 0.001) at Bossier City, followed by the redbanded stink bug (33%) and the brown stink bug complex (2%).

In 2010 at Jeanerette, the redbanded stink bug was the most abundant species (χ²=341.2; P < 0.001), ranging from 76 to 92% of the total stink bug population collected in all MGs (III, IV, and V) (Fig. 4). The redbanded stink bug and green and brown stink bug complexes made up 86, 13, and 1% of the population, respectively. At Baton Rouge, the green stink bug complex was most prevalent in MG IV (52%) soybean, while the redbanded stink bug was most abundant in MG V (49%) and VI (63%) soybean. The redbanded stink bug (56%) was the most abundant stink bug at Baton Rouge in 2010 (χ²=15.3; P < 0.001), followed by the green (37%) and brown (7%) stink bug complexes. At Alexandria, redbanded stink bug accounted for the majority of stink bugs sampled (43–49%) (χ²=11.4; P < 0.001) in all MGs (IV, V, and VI). At Winnsboro, the redbanded stink bug was the predominant species collected in MG IV (41%) soybean, while the green complex was most abundant in MG V (37%) and MG VI (63%) soybean. The green stink bug complex (50%) was most abundant (χ²=16.6; P < 0.001), followed by the redbanded stink bug (30%) and the brown stink bug complex (20%). At the most northern survey site in 2010 (Bossier City), the brown stink bug complex was the dominant stink bug complex in all three MGs (IV, V, and VI) (χ²=43.5; P < 0.001), ranging from 51 to 64% of the total population. The stink bug population in Bossier City predominately consisted of the brown stink bug complex (57%), the green stink bug complex (24%), and the redbanded stink bug (19%). Redbanded stink bugs made up the largest percentage of the total stink bug complex across all sampling dates and locations in soybean cultivars in MG III (86%), MG IV (60%), MG V (54%), and MG VI (50%) during the complete survey period (Fig. 5).

In 2008, stink bug densities did not reach an action threshold level (9/25 sweeps) in MG IV or V soybean at Baton Rouge (Fig. 6 A). Highest numbers were recorded during R5 to R6 growth stages (3.5–5.7 per sample). In the MG VI soybeans, the action threshold was exceeded during the R5 (13.7 per sample) growth stage and numbers remained above threshold through R6 (11.3 per sample). At the Alexandria site, the stink bug complex reached action threshold levels during R5 (8.5–15.0 per sample) and R6 (18.6–19.3 per sample), but declined during R7 (4.3–6.8 per sample) in MG IV and V (Fig. 6 B). In MG VI soybean, stink bug numbers (10.5 per sample) were above the action threshold only during R6. At Winnsboro, stink bugs exceeded action thresholds (Fig. 6 C) in all MGs (IV, V, and VI). Highest numbers were recorded during R6 (45.0 per sample) and R7 (10.3 per sample) in MG IV soybean and R5 (19.8–20.2 per sample) and R6 (9.2–15.1 per sample) in MGs V and VI.

In 2009, stink bugs did not reach the action threshold in MG III soybean, but exceeded action threshold levels during R6 (9.9 per sample) in MG IV and R6 (15.4 per sample) and R7 (11.3 per sample) in MG V soybean at Jeanerette (Fig. 7 A). At Baton Rouge, stink bugs in each MG remained below the action threshold level throughout the sampling period, and peak numbers ranged from 3.8 to 4.4 per sample (Fig. 7 B). At Alexandria, peak levels (8.1–18.8 per sample) were recorded during R6 in all MGs. Action threshold levels were reached in MG IV and VI soybean (Fig. 7 C). At Winnsboro, only stink bugs in MG V soybean exceeded the action threshold (32.0 per sample) (Fig. 7 D). Peak numbers of stink bugs were detected at R7 in MGs IV and V and at R5 in MG VI. In Bossier City, stink bug numbers were highest during R6 (8.8–32.7 per sample), with action threshold levels exceeded in MG IV and VI soybean (Fig. 7 E).

In 2010, action thresholds were exceeded in MG IV and V soybean, with peak stink bugs collected during R6 in MG III (7.4 per sample) and MG IV (14.5 per sample) soybean and during R7 (17.3 per sample) in MG V soybean at Jeanerette (Fig. 8 A). At Baton Rouge, stink bugs remained relatively low (0–5 insects per sample) in MG IV and V soybean but were above the action threshold during R6 (13.7 per sample) and R7 (10.5 per sample) in MG VI soybean (Fig. 8 B). At Alexandria, peak stink bug numbers (6.8–12.0 per sample) were recorded at R6 in all MGs (IV, V, and VI), with populations exceeding action thresholds in MG IV and VI soybean (Fig. 8 C). At Winnsboro, stink bugs were low in MG IV and V soybean, ranging from 0 to 2.1 per sample (Fig. 8 D). Stink bug populations were slightly higher in MG VI soybean (0–7.3 per sample), peaking at R6, but remained below the action threshold. At Bossier City, stink bug numbers peaked at R7 in all MGs (IV, V, and VI) but only reached action threshold in the MG V soybean (Fig. 8 E). Total stink bugs collected at the five sample sites decreased 58% from 2009 to 2010 (Table 2).

Summarized across all MGs and survey sites, action thresholds for the stink bug complex were detected only during the R4 (pod elongation) to R7 (beginning maturity) soybean growth stages (Fig. 9). Low levels were detected during R1 (first flower) to R3 (pod initiation) or during R8 (full maturity) soybean growth stages (Fig. 9), but action thresholds were never reached during those periods. Only 5% of the samples collected at R4 had stink bug numbers above an action threshold, while 25, 51, and 25, of samples collected at R5, R6, and R7, respectively, had stink bug above an action threshold. Mean numbers of stink bugs ranged from a low of 0.3 per sample during R1 to a high of 10.9 per sample during R6.

Discussion

The redbanded stink bug was the dominant stink bug species sampled in Louisiana soybean during this study. This is the first report of the redbanded stink bug as a primary pentatomid pest of soybean at locations within the United States. Previously, this insect was not considered to be an economically important pest within the United States despite being reported in Florida, Georgia, New Mexico, and South Carolina (McPherson and McPherson 2000).

Redbanded stink bugs have been found above action thresholds in all Louisiana soybean-producing parishes. In this study, the redbanded stink bug was the primary species collected at four of the five survey sites during the 3 yr period. This species was found at the highest levels in the southern-most survey sites of Jeanerette and Baton Rouge where it has been established since 2000 and detected at its lowest levels at the northern-most site of Bossier City where it was not found until the summer of 2006. The expansion of this insect's range has not been limited to Louisiana. Redbanded stink bugs have now reached soybean pest status in all states bordering Louisiana and have been reported as far north as Missouri and Tennessee (Stalcup 2007, Bailey 2009, Catchot 2009, Smith 2009, Smith et al. 2009).

Interestingly, the redbanded stink bug has only been a significant soybean pest and not of other southern row crops such as cotton, field corn, grain sorghum, or rice. Redbanded stink bug has been observed in these crops, but only at very low levels and only when soybean is not available in adjacent fields. This observation differs from that of other stink bugs typically associated with soybean such as southern green, green, and brown stink bugs, which are more generalized feeders and may reach damaging levels in other crops including field corn, cotton, and grain sorghum (McPherson and McPherson 2000, Panizzi et al. 2000). With limited alternate hosts available to redbanded stink bug during the summer months, populations remain concentrated in soybean fields where they are capable of quickly building to economically important levels.

In this study, redbanded stink bugs made up the largest percentage of the stink bug complex in earlier maturing soybean varieties, MGs III (86%) and IV (60%). Numbers declined slightly in later maturing soybeans, MGs V (54%) and VI (50%). This may be because of the absence of other suitable hosts for the redbanded stink bug, while the southern green, green, and brown stink bugs have a wider variety of crop and noncrop hosts available during the period MG III and IV soybean are most susceptible. These species may become more distributed across the farm scape, leaving redbanded stink bug populations concentrated in soybean.

The early soybean production system that is widely used on much of Louisiana acreage may allow the overwintering and first-generation populations of redbanded stink bug to have a suitable host with little competition from other stink bug species that inhabit a wide range of alternate hosts. In 2010, a significant portion of Louisiana soybean acreage was planted to early maturing varieties; 64% to MGs III and IV, while 35% were planted to V, and 1% to VI. Historically, Louisiana has planted later maturing varieties (MGs V, VI, and VII) but began a transition to more of an early soybean production system during the late 1990s to early 2000s (Honeycutt 1996, Heatherley 1999, Baur et al. 2000). In the mid-south, the early production system has been adopted to reduce late season drought stress, insect problems, and inclement weather that were often encountered in early August and mid-September (Heatherly 1999).

In 2010, stink bug numbers in this survey and in many Louisiana production fields were generally lower compared with populations in 2009. This reduction in total stink bug numbers could be attributed to lower-than-normal temperatures during the winter months of 2009–2010 and drought conditions during the following spring that reduced the availability and quality of alternate noncrop hosts (Robinson 2011). The proportion of brown stink bugs within the stink bug complex was higher in 2010 (20%) compared with 2008 (7%) and 2009 (8%), which could have been related to an overall colder winter from 2009 to 2010. Green and brown stink bugs are more tolerant to cold temperatures, have a wider geographical range, and can successfully overwinter in the northern United States (Greene et al. 2006). Overwintering mortality is the major limiting factor for southern green stink bug populations (Jones and Sullivan 1981, Elsey 1993, McPherson and McPherson 2000 d). Although stink bug numbers declined sharply from 2009 to 2010, the redbanded stink bug remained the predominant pest species collected in Louisiana soybean. Little is known about the northern range of redbanded in the United States at this time, and these data indicate that this stink bug has become established in Louisiana as a perennial pest of soybean with populations fluctuating annually because of environmental conditions.

Since the redbanded stink bug has become more prevalent in Louisiana soybean, the frequency of insecticide applications has increased from one to two per season during the late 1990s to a current average of three to five per season. The bulk of these applications have targeted redbanded stink bugs (Bechtel 2000, Paxton 2005, Paxton et al. 2007, Guidry 2010). The redbanded stink bug is more difficult to control in soybean with currently available insecticides compared with the southern green stink bug, which has historically been the predominant stink bug pest of soybean in Louisiana (Baur et al. 2010). Difficulty controlling the redbanded stink bug with currently available insecticides, coupled with reports from South America indicating that this species has the ability to cause greater injury to soybean than southern green stink bug, have resulted in a reduction of the action threshold for initiating insecticide applications from nine to six stink bugs per sample (Vicentini and Jimenez 1977, Correa–Ferreira and Azevedo 2002, Baur and Baldwin 2006). Additional research is needed to fully understand the biology of redbanded stink bug in Louisiana soybean agro-ecosystems and to determine how this species became the dominant pest of soybean in only a decade.

This study was partially funded by the Louisiana Soybean and Grain Promotion Board and the Louisiana State University Agricultural Center. The authors thank Ralph Sheppard, Kyle Fontenot, Karla Emfinger, Betsy Lowe, Sara Beth Lowe, Courtney Jackson, Nathan Grammes, Matt Foster, and the numerous student workers at the Macon Ridge Research Station for their assistance with these studies. We would also like to express our appreciation to Colleen Cookson (Red River Research Station); Darrell Franks (Dean Lee Research Station); Jim Griffin, Joey Boudreaux, and Matt Baerle (Ben Hur Research Station); and Art Richter, Sebe Brown, and Geoffrey Tate and the student workers of Soybean Entomology Lab (Louisiana State University Department of Entomology) for their participation in sampling field plots. This article was approved for publication by the Director of the Louisiana Agricultural Experiment Station as manuscript No. 2011-234-6240.

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