Populations of tarnished plant bug, Lygus lineolaris (Palisot de Beauvois) (Hemiptera: Miridae), from the Lower Mississippi Delta regions of Arkansas, Louisiana, and Mississippi were evaluated from 2008 through 2015 for susceptibility to pyrethroid insecticides using a diagnostic-dose assay with permethrin. Resulting data add to the compilation of pyrethroid susceptibility data carefully tracked in this pest since 1994 and provide continuing evidence of high frequencies of pyrethroid resistance in field populations of the tarnished plant bug. Resistance levels are variable, and some populations remain susceptible suggesting practical value in the continued use of the diagnostic-dose assays prior to pyrethroid treatments. Recent studies with dose–response models suggest that levels of pyrethroid resistance in some populations may still be evolving, with some populations requiring higher doses to reach levels of control comparable to those observed 10 yr ago. Concerns for frequent use of multiple classes of insecticides and possible selection for tarnished plant bugs with metabolic resistance mechanisms capable of detoxifying available insecticide chemistries warrant continued efforts to manage resistance in this important crop pest. Associations among measured pyrethroid resistance levels, published data on annual use of pyrethroid insecticides, and annual estimates of cotton insect losses and control costs were explored and summarized for the 8 yr of this investigation. Mortality of tarnished plant bugs at the diagnostic-dose of permethrin was negatively correlated with kilograms of pyrethroids applied per acre of harvested cropland. Key words: Lygus lineolaris, pyrethroid, insecticide resistance The Mississippi Cooperative Extension Service recently recom- 1993 (Head 1993). This window-use strategy was developed initially mended specific tank-mixtures of pyrethroids in combination with in an effort to delay pyrethroid resistance evolution in the tobacco other insecticides for controlling tarnished plant bug, Lygus lineola- budworm (Anonymous 1986). Pyrethroid-resistant populations of ris (Palisot de Beauvois) (Hemiptera: Miridae) (Catchot 2017). This tobacco budworm were first detected in the Mississippi Delta in represents a major change in strategic use of pyrethroids, and an 1986 (Luttrell et al. 1987). example of the evolving interrelationships between resistance man- Pyrethroids were first recommended for use on cotton in agement practices for this highly polyphagous pest of cotton and Mississippi for control of bollworm and tobacco budworm in 1979 those for the heliothine pest complex [bollworm (Helicoverpa zea following a conditional registration (MCES 1979). Elliott (1989) Boddie) (Lepidoptera: Noctuidae) and tobacco budworm (Heliothis provides a summary of pyrethroids and his vision for the import- virescens F.) (Lepidoptera: Noctuidae)], a group of species previ- ance of these insecticides in modern agriculture including use in the ously dependent upon chemical control (Luttrell 1994) but now animal sector for control of ectoparasites as well as the health and largely controlled via widespread planting of Bt cottons (Luttrell household insecticide market. Palmquist et al. (2012) provides an and Jackson 2012, Luttrell et al. 2015). The Mississippi Cooperative updated evaluation of pyrethroid insecticides including use patterns Extension Service also no longer recommends pyrethroid insecticides and ecotoxicity, and they describe how the pyrethroids as a group for heliothine control (Catchot 2017), marking the end of 37 yrs of replaced many organophosphate insecticides due to better selectivity pyrethroids specifically applied for this purpose. A window-strategy on target pests and less persistence than organochlorine insecticides. for use of pyrethroids on cotton only after first-bloom is still rec- For all of these reasons, pyrethroids were preferred insecticides for ommended as it has been in the Mississippi recommendations since controlling many pests of cotton, not just heliothines. Snodgrass Published by Oxford University Press on behalf of Entomological Society of America 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/open-government-licence/version/2/). Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/29/4939105 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2 Journal of Insect Science, 2018, Vol. 18, No. 2 (2014) and Luttrell and King (2014) provide overviews of the some- the collected insects to the USDA ARS Southern Insect Management times controversial use of pyrethroids for early-season pests of Research Unit laboratory in Stoneville, MS. Insects were kept cotton. for 24 h in 3.8-liter cardboard containers with green bean pods Snodgrass (1994) first reported pyrethroid resistance in tarnished (Phaseolus vulgaris L.) as food prior to the assays on the following plant bugs collected from cotton near Schlater, MS during July and day. The diagnostic-dose assay was administered in 20-ml glass scin- August of 1993, 14 yr after the first use of pyrethroids on cotton tillation vials as described by Snodgrass and Scott (1999). Technical in Mississippi and 7 yr after the first documentation of pyrethroid grade permethrin purchased from Chem Service (West Chester, PA) resistance in tobacco budworm (Luttrell et al. 1987). Snodgrass was dissolved in acetone and pipetted in 0.5-ml aliquots into each (1996b) further evaluated the problem, reported expanding exam- vial (15 μg per vial). The vials were rolled on a hot dog roller with- ples of pyrethroid and organophosphate resistance in tarnished plant out heat under a fume hood until the permethrin residue was dry. All bug populations, and provided rationale for expanded monitoring of assays from 2008 through 2013 included 50 adult tarnished plant pyrethroid resistance given the impact of widespread pyrethroid use bugs from the previous day field collection. Two bugs were added to on multiple pests and efforts to preserve their critical role in cotton each vial and mortality was determined after 3 h of exposure. Each production. This monitoring effort spanned 25 yr of published scien- test vial contained a piece of green bean pod (~3-cm long) for food. tific works including Snodgrass (1994), Snodgrass and Elzen (1995), In 2014 and 2015, studies were focused more on linking the Snodgrass (1996a),b, Snodgrass and Scott (2000), Snodgrass et al. 2008–2013 data, and the previous collective work of the Snodgrass (2008), Snodgrass et al. (2009), and Parys et al (2017). Snodgrass laboratory on pyrethroid resistance, to future resistance studies and Scott (1999) developed a discriminating-dose assay that could focused more on field ecology and evolving population genetics. detect pyrethroid-resistant tarnished plant bug populations and Creating an experimental bridge to the previous work was essential, predict possible control problems before treatments were initiated. and thus repeating the procedures of Snodgrass et al. (2008 2009) as This assay was based on a 3-h observation of field-collected bugs much as possible was a high priority. However, we were also inter- exposed to glass-vials treated with 15 μg of permethrin. Snodgrass ested in re-evaluating dose–response models with multiple doses in et al. (2008) reported results of studies conducted with both the 2014 and 2015 as the more than two-decade long exposure to pyre- diagnostic-dose assay and traditional dose–response studies that rely throids may have selected for additional resistance mechanisms (Zhu on development of probit mortality regression lines. They concluded and Snodgrass 2003, Zhu and Luttrell 2012) and altered some of the that either a LC of 24 μg of permethrin per vial at 24 h or 60% or previous tight-relationships between diagnostic-dose procedures and less mortality at the diagnostic-dose (15 μg permethrin per vial at full dose–response models described by Snodgrass and Scott (2000) 3 h) could be used to predict field control problems with tarnished and Snodgrass et al. (2008). Thus, studies in 2014 and 2015 used a plant bugs exposed to pyrethroid insecticides. range of test concentrations (0-, 0.5-, 1.5-, 5-, 15-, and 50-μg per- Reported here are additional studies conducted from 2008 methrin per vial). They also included a laboratory reference colony through 2015 to further study the evolution of pyrethroid resistance as an additional experimental control. Observations of surviving in populations of the tarnished plant bugs from the Lower Mississippi insects were made at 3 and 24 h, thereby allowing data from the Delta. Studies in 2014 and 2015 also included dose–response regres- 15 μg per vial dose to be compared to that of the 2008–2015 studies. sions for comparison to those published by Snodgrass et al. (2008). Sample size was reduced in individual assays in 2014 and 2015 as Temporal and spatial patterns of plant bug mortality at the diag- other studies were being simultaneously conducted with other insec- nostic-dose were compared to reported use rates of pyrethroids for ticides, and insects were needed for multiple test concentrations in individual counties/parishes within the study area and estimates of the permethrin studies. A minimum of 10 individuals were tested at cotton insect losses and control costs annually accumulated by the each concentration (two per vial), and the test was repeated with National Cotton Council to explore linkages between tarnished additional replicates (up to a maximum of three) with the same col- plant bug resistance and cotton insect management practices. lection of insects. As a result of these procedures, the number of insects examined at the diagnostic dose of 15 μg per vial would have ranged from 10 to 30 for a given collection. Dose-mortality regres- Material and Methods sions were conducted on the 24-h observations using probit analysis Methods and procedures for collecting information on the suscepti- (PROC PROBIT, SAS 9.4, SAS Institute Incorporated, 2013). Data bility of tarnished plant bugs to pyrethroid insecticides were those were discarded for individual tests that failed chi-square tests for described in depth by Snodgrass (1996a,b), Snodgrass and Scott significance of slope or chi-square goodness of fit (P = 0.05). (1999, 2000), and Snodgrass et al. (2008, 2009) for 2008 through A USDA ARS laboratory colony was added to the monitoring 2013. Slightly different procedures were used in 2014 and 2015, assays as an additional experimental control (generally weekly) in and specific modifications are described below. Tarnished plant bug 2014 and 2015. Procedures were the same as those for the field populations across the Lower Mississippi Delta region of Arkansas, collections. The laboratory-reared insects were from a colony orig- Louisiana, and Mississippi (Fig. 1) were collected from multiple inally established in 1998 at the USDA-ARS Biological Control locations each year of the 8-yr study and exposed to a diagnos- Rearing and Research Unit in Starkville, MS. Insects were originally tic-dose assay using glass-vials treated with permethrin (15 μg per collected from weedy host plants in Chickasaw Co., MS (Cohen vial). A handheld GPS unit was used to record collection locations 2000). The colony was moved to the USDA-ARS National Biological (Garmin Monterra, Olathe, KS) in 2014 and 2015. Earlier collec- Control Laboratory in 2006 and to the USDA-ARS Southern Insect tions, those from 2008 through 2013, were associated with specific Management Research Unit in 2010 (Portilla et al. 2011). The colony latitudes and longitudes by identifying previous collection sites from is routinely reared under controlled abiotic conditions in environ- written records and locating the site on a digital Google Earth map. mental chambers (constant 27°C, 60% relative humidity (RH), and Insects were collected by sweeping known hosts [primarily the sea- a photoperiod of 16:8 [L:D] h) following details outlined in Portilla sonal sequence of broadleaf weeds described by Snodgrass et al. et al. (2011) to provide large numbers of even-aged insects. Assays (1984)], usually from road ditches and field borders described in with the USDA colony were conducted exactly as those with the the previous studies by Snodgrass and colleagues, and transporting field colonies, but the insects were mixed sex adults (50F: 50M) of a Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/29/4939105 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 3 Fig. 1. Sites of tarnished plant bug collections in the Arkansas, Louisiana, and Mississippi Delta. uniform age (1- to 2-d-old adults). Snodgrass (1996a) described the as a control comparison), North Mississippi Delta (samples from effects of age of tarnished plant bugs on susceptibility to insecticides. Mississippi Delta Counties north of US Highway 82), and South Survival rates observed at the diagnostic-dose were studied for Mississippi Delta (samples from Mississippi Delta Counties south influences of time of insect collection (year and month within year) of US Highway 82). Relationships to latitude and longitude were and geographic location of collection (latitude, longitude, and geo- studied via linear models using Multivariate Procedures in JMP, graphic groupings of the data). Collection areas were grouped for Version 11.1. analysis into regions, which included Arkansas (almost all samples Additional exploratory research was conducted by examining were from the Southeast Delta Region of Arkansas), Crossett (a loca- possible relationships between survival of plant bugs at the diag- tion in Arkansas used as a historical benchmark of susceptibility), nostic-dose, estimated pyrethroid-insecticide use by collecting East Mississippi Delta (Mississippi sample locations along the geo- county-level information from the USGS National Water Quality graphic boundary of the Delta and Hill regions), Louisiana (almost Assessment Program’s Pesticide National Synthesis Project (Stone all samples were from the Northeast Louisiana Delta region), the 2013, Thelin and Stone 2013, Baker and Stone 2015, USGS 2017), USDA ARS Laboratory colony reared on meridic diet (only included and annual estimates of cotton insect loss and control for the Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/29/4939105 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Journal of Insect Science, 2018, Vol. 18, No. 2 different regions (Williams 2017). The full USGS pesticide dataset the North and South Mississippi Delta for this analysis. There was was subset by FIPS code to only include states in the Midsouth using a significant effect (df = 7, F = 4.2677, P = 0.0002) of year (Fig. 2) the “EPest-high” estimates of insecticide application for individual with average mortality at the diagnostic-dose in 2011 (77.7%) and counties. Insecticides were categorized by their mode of action and 2008 (70.8%) exceeding that of 2015 (58.9%), 2014 (57.5%), 2010 pooled by state and county. The data presented here include all pyre- (53.9%), 2009 (53.6%), and 2013 (49.5%). The average mortality throids applied to harvested cropland. The grouping of regions dif- in 2012 (63.8%) was intermediate and not different from any other fered for insect loss and control cost estimates and included Arkansas year. The data were also studied for effects of months within years. (the entire state), Southeast Arkansas, Louisiana (the entire state), Month of collection had a significant effect on mortality (df = 8, Mississippi (the entire state), and the Mississippi Delta. Data were F = 5.009, P < 0.0001). Average mortality in April (82.6%), October also pooled across the South Delta Region (combination of estimates (80.0%), and May (78.4%) was greater than that of July (50.2%) from Louisiana, Mississippi Delta and Southeast Arkansas) and and September (50.2%). Average mortality in June (67.0%) and across all three states (Arkansas, Louisiana, Mississippi) for some August (67.9%) was intermediate between the two groups. During observations. Analyses using overlapping geographic areas were some years, samples were also collected in November (20% mor- completed using repeated measures analyses of variance (ANOVA) tality) and December (45% mortality), but by this time of the sea- to account for non-independence in JMP. Linear relationships be- son, tarnished plant bugs are generally entering diapause (Snodgrass tween observed survival at the diagnostic dose and county-level 2003) and accumulating fat reserves that may impact response to estimates of kg of pyrethroids used per acre of harvested cropland the insecticides. Based on the Snodgrass et al. (2008) suggestion that were developed and studied. Estimated use of pyrethroid insecticides field populations with less than 60% mortality at the diagnostic-dose was also studied by ANOVA to detect any differences in use pat- would cause field control problems, we estimate that the number of terns across the temporal and spatial scales of the study. Similarly, populations difficult to control would have ranged from 4% in 2011 temporal and spatial patterns of tarnished plant bug mortality at to 62% in 2013 (Table 1). the diagnostic-dose and recorded annual use of pyrethroid insecti- Mortality of tarnished plant bugs from the Crossett, AR, locations cides for each county within the study area were compared to the averaged 86.7%, a response similar to that previously reported by National Cotton Council’s annual cotton insect loss estimates for Snodgrass et al. (2008). Average responses for all geographic regions Arkansas, Louisiana, and Mississippi for the years 2008 through within the Delta and the USDA ARS laboratory colony fed solely on 2015 (Williams 2017). a meridic diet ranged from 48.8% (Arkansas) to 67% (Louisiana) and were less than that of the average for the Crossett control loca- tion (Table 2). Mortality of the USDA ARS laboratory colony also Results exhibited significant variable response across the different tests Geographic locations of the field sample sites are shown in Fig. 1. (range of 20–90% mortality, 95% CI of 46.7–65.2% mortality). Descriptive statistics associated with the samples over years and Average dose–response regressions obtained via probit analysis of groupings of geographic locations within the Delta are summa- the USDA ARS laboratory colony, and the field colonies collected in rized in Tables 1 and 2, respectively. Table 2 also includes compara- 2014 through 2015, indicated no difference in average responses at tive information on diagnostic-dose mortality of insects from the the 3-h observation time based on overlap of 95% confidence limits. Crossett, AR, control site and studies conducted against the USDA At 24 h, the USDA laboratory colony had significantly higher mor - ARS diet-reared colony in 2014 and 2015. When tarnished plant bug tality at the 50 μg per vial dose than the average of responses for the mortality at the diagnostic dose was studied by ANOVA for effect field colonies. There were no differences at lower doses, and average of region (Arkansas, Louisiana, North Mississippi Delta, and South slopes of the regression lines were similar (Table 3). Mortality at Mississippi Delta), there was no effect on resulting mortality (df = 3, the standard 3-h observation of insects exposed to 15 μg perme- F = 1.2785, P = 0.2825). There were also no significant influences of thrin per vial, at the 3-h observation of insects exposed to 50 μg of latitude (n = 234, r = 0.0065, F = 1.5360, P = 0.2165) or longitude permethrin per vial, and the calculated LC across all doses at 3 h (n = 234, r = 0.0025, F = 0.5907, P = 0.4429) of collection site on were compared via simple pairwise correlation to the measured 24 h resulting mortality at the diagnostic-dose across the study. Data for LC (Table 3). Across all colonies (n = 59), mortality at the 50 μg the East Mississippi Delta reported in Table 2 were grouped into dose at 3 h was more closely correlated to 24-h LC (r = −0.5286, Table 1. Summary statistics for diagnostic-dose response of tarnished plant bugs across all samples for each year 2008 through 2015 Year Number Mean ± Range in % 95% CI Number of % Populations Number of % Populations of samples SEM % mortality samples with % considered samples with % considered a b tested mortality observed mortality < 60 resistant mortality > 90 susceptible 2008 64 71 ± 3.11 6–98 64.72–76.91 16 25.0 12 18.8 2009 76 54 ± 3.84 2–98 46.05–61.11 40 52.6 14 18.4 2010 19 54 ± 7.25 0–94 39.68–68.11 9 47.4 2 10.5 2011 23 78 ± 2.15 53–97 73.32–81.75 1 4.3 2 8.7 2012 42 21 ± 3.66 4–96 14.27–28.62 18 42.9 4 9.5 2013 29 49 ± 5.17 14–98 39.35–59.61 18 62.1 4 13.8 2014 52 58 ± 3.95 0–100 49.76–65.24 24 44.4 3 5.6 2015 14 59 ± 7.37 0–100 44.50–73.39 8 42.1 4 21.1 Diagnostic response is mortality of adult tarnished plant bugs after three house of exposure to glass vials treated with 15 μg permethrin per vial. Resistance is based on the recommendation of Snodgrass et al. (2008) that mortality of 60% or less at the diagnostic dose would indicate field control problems. Susceptibility is based on the LC diagnostic dose of 15 μg per vial after 3 h of exposure (Snodgrass and Scott 1999) Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/29/4939105 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 5 Table 2. Summary statistics for diagnostic dose response of tarnished plant bugs across all samples for each sample area 2008 through 2015 Area Number Mean ± Range in % 95% CI Number % Populations Number % Populations of samples SEM % mortality of samples Considered of Samples Considered a b c tested mortality observed with % Resistant with % Susceptible mortality < 60 Mortality > 90 Arkansas 45 49 ± 4.38 4–94 40.68–57.87 28 61.4 4 8.9 Crossett, Arkansas 3 87 ± 3.33 80–90 80.13–93.20 0 0.0 0 0.0 East Mississippi Delta 20 66 ± 7.76 4–98 51.00–81.42 9 42.1 7 35.0 Louisiana 52 67 ± 3.82 2–100 59.51–74.47 15 28.8 8 15.4 USDA Lab Diet Reared 22 56 ± 4.73 20–90 46.67–65.20 10 50.0 0 0.0 North Mississippi Delta 85 62 ± 3.16 0–100 55.34–67.74 32 84.3 14 16.5 South Mississippi Delta 99 61 ± 3.06 8–100 54.65–66.66 40 40.0 12 12.1 Diagnostic response is mortality of adult tarnished plant bugs after three h of exposure to glass vials treated with 15 μg permethrin per vial. Resistance is based on the recommendation of Snodgrass et al. (2008) that mortality of 60% or less at the diagnostic dose would indicate field control problems. Susceptibility is based on the LC diagnostic dose of 15 μg per vial after 3 h of exposure (Snodgrass and Scott 1999). Fig. 2. Individual responses of tarnished plant bug populations in the Mississippi Delta to a diagnostic dose of permethrin in a glass vial assay, 1994 through 2015. Data for 1994 through 2005 were from Snodgrass (1994, 1996a), Snodgrass and Elzen (1995), Snodgrass et al. (1999, 2008, 2009), and Snodgrass and Scott (2000). P < 0.0001) than the standard 3-h observation at 15 μg per vial diagnostic-dose mortality when studied by linear regression using the (r = −0.2555, P = 0.05510) (Table 4). A similar trend was observed entire dataset (n = 233, F = 0.0831, P = 0.7734; Table 5). There was with pairwise comparisons across the field colonies only (n = 43), a significant negative linear relationship (n = 233, r = 0.0214, inter- but not with comparisons across the different tests with the USDA cept ± SE = 70.888 ± 3.682, slope = −55.677 ± 1.768, F = 5.1008, ARS laboratory colony where the relationship between observations P = 0.0248) between kg pyrethroid applied/acre of harvested crop- at 3 h with the 15 μg per vial dose and the 24-h LC was highly land across the study and resulting tarnished plant bug mortality at significant (r = −0.8818, P < 0.0001) and similar to that previously the diagnostic dose (Fig. 3, Table 5), though the low R indicates that reported by Snodgrass et al. (2008). The relationship between 3-h the data are highly variable. observation of mortality at the 50 μg per vial dose and the 24-h LC Since the empirical estimates of tarnished plant bug mortality at was not significant (P = 0.3653), as almost all insects were dead at the diagnostic-dose developed by Snodgrass et al. (2008) were pri- that concentration. marily from field samples taken in the South Delta (delta regions of Across the entire study period of 2008 through 2015, average Louisiana, Mississippi, and Southeast Arkansas), mean kg of pyre- annual use of pyrethroids was greater in the Mississippi Delta (0.0145- throids per acre of harvested cropland and mean mortality of tar- kg pyrethroid/acre of harvested cropland) than it was in Louisiana nished plant bugs at the diagnostic-dose were averaged for each year (0.0073-kg pyrethroid/acre of harvested cropland). Pyrethroid use in across the South Delta Region, and compared to averaged estimates Southeast Arkansas was more variable across years and was inter- of insect loss and control costs adjusted for the South Delta region. mediate between that of the Mississippi Delta Region and Louisiana Adjustments were relative to the annual cotton acreages for each (0.011 kg/acre of harvested cropland). Across the entire region, of the individual regions comprising the collective total (Table 6). pyrethroid use when studied by ANOVA, varied significantly by year When these data were studied by ANOVA, there were no significant (df = 7, F = 5.9358, P < 0.0001) with amounts applied during 2010 differences across years in amount of pyrethroid applied per har- (0.0163 kg/harvested acre), 2013 (0.0163 kg/harvested acre), 2012 vested crop acre, mean mortality of tarnished plant bugs at the diag- (0.0151 kg/harvested acre), and 2009 (0.0151 kg/harvested acre) nostic dose, mean number of insecticide applications for plant bugs, exceeding that applied in 2008 (0.0008 kg/harvested acre). Those for mean acres of cotton (although they were highly variable and there 2011 (0.0120 kg/harvested acre), 2014 (0.0115 kg/harvested acre), was a consistent decrease), mean estimated % crop loss to insects, and 2015 (0.0100 kg/harvested acre) were intermediate in amounts mean number of foliar applications for all pests, mean cost of all applied. There was no significant relationship between year and foliar insecticides per acre, or mean cost of individual insecticide Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/29/4939105 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Journal of Insect Science, 2018, Vol. 18, No. 2 Table 3. Summary statistics for dose-response regression of laboratory and field populations of tarnished plant bug exposed to permethrin in glass vial assays in 2014 and 2015 experiments a a No. of regressions Mean ± SEM Minimum value observed Maximum value observed 95% CI USDA Lab Diet-Fed Colony 24-h Slope 16 2.4 ± 0.15 1.5 3.5 2.14–2.74 24-h LC 16 7.6 ± 1.21 1.5 18.2 5.26–9.99 24-h LC 15 22 ± 3.91 0.5 44.0 14.32–29.66 24-h % Mort (0 μg per vial) 16 0 0 0 0 24-h % Mort (0.5 μg per vial) 16 6.6 ± 2.69 0 40 1.29–11.83 24-h % Mort (1.5 μg per vial) 16 18.9 ± 6.27 0 70 6.62–31.2 24-h % Mort (5 μg per vial) 16 39.1 ± 6.55 10 100 26.22–51.9 24-h % Mort (15 μg per vial) 16 71.6 ± 5.99 20 100 59.83–83.29 24-h % Mort (50 μg per vial) 16 99.2 ± 0.44 95 100 98.36–100.08 3-h Slope 15 2.29 ± 0.94 0 4.2 1.81–2.77 3-h LC 15 9.07 ± 5.09 1.3 18.2 6.39–11.74 3-h LC 15 33.81 ± 22.31 5.3 29.95 22.12–45.49 3-h % Mort (0 μg per vial) 15 0 0 0 0 3-h % Mort (0.5 μg per vial) 15 4 ± 2.14 0 30 0–8.19 3-h % Mort (1.5 μg per vial) 15 16.3 ± 6.77 0 80 3.07–29.6 3-h % Mort (5 μg per vial) 15 41.8 ± 8.11 0 90 25.94–57.73 3-h % Mort (15 μg per vial) 15 68 ± 5.78 20 100 56.68–79.32 3-h % Mort (50 μg per vial) 15 97 ± 1.53 80 100 94.01–99.99 Field Colonies 24-h Slope 43 2.1 ± 0.19 0.5 5.4 1.75–2.49 24-h LC 43 6.1 ± 1.56 0.3 55.5 3.02–9.12 24-h LC 42 164.4 ± 101.95 0.0 4277.0 0–364.27 24-h % Mort (0 μg per vial) 43 1.1 ± 0.57 0 20 0–2.2 24-h % Mort (0.5 μg per vial) 43 13.4 ± 2.57 0 60 8.35–18.43 24-h % Mort (1.5 μg per vial) 43 32.9 ± 2.98 0 80 27.06–38.75 24-h % Mort (5 μg per vial) 43 64.4 ± 3.80 0 100 56.9–71.81 24-h % Mort (15 μg per vial) 43 80 ± 3.79 10 100 72.56–87.44 24-h % Mort (50 μg per vial) 43 93.7 ± 1.67 60 100 90.46–96.98 3-h Slope 42 3.47 ± 4.48 0.1 19.1 2.12–4.82 3-h LC 42 15.92 ± 24.92 0.92 145.81 7.99–23.84 3-h LC 42 771.92 ± 4255.19 2.94 26303 0-2124.88 3-h % Mort (0 μg per vial) 42 0.2 ± 0.24 0 10 0–0.7 3-h % Mort (0.5 μg per vial) 42 2.4 ± 1.48 0 60 0–5.28 3-h % Mort (1.5 μg per vial) 42 14.3 ± 2.46 0 70 9.46–19.11 3-h % Mort (5 μg per vial) 42 38.9 ± 4.19 0 100 30.72–47.13 3-h % Mort (15 μg per vial) 42 66.4 ± 4.87 0 100 56.89–75.96 3-h % Mort (50 μg per vial) 42 84.5 ± 3.39 10 100 77.87–91.18 LC and LC values are expressed as microgram of permethrin per vial. 50 90 applications. Significant differences across years were detected in Table 4. Correlation coefficients between observations of mortality the mean number of insecticide applications for bollworms and the at 3-h test concentrations of 15- and 50-μg permethrin per vial, esti- mated LC values at 3- and 24-h measured LC s in 2014 through mean yield in kilograms of lint per acre. More insecticide applica- 50 50 2015 glass vial assays with an USDA Laboratory colony and field tions for bollworm were made in 2010 (1.95/acre) than in 2008 colonies from the Mississippi Delta (0.64/acre), 2012 (0.55/acre), and 2013 (0.53/acre). Yield was high- est in 2013 (545 kg lint/acre), which was significantly greater than Correlation Significance that of 2008 (346 kg lint/acre) and 2009 (371 kg lint/acre). When coefficient (r) probability these South Delta metrics were studied by pairwise simple correl- All 2014–2015 Dose–response regressions (n = 59) ation using Multivariate Procedures in JMP Version 11.1, signifi- 3-h Mort 15 μg 24-h LC −0.2555 0.0551 cant or near-significant correlations were detected between acres 3-h Mort 50 μg 24-h LC −0.5286 <0.0001* 50 of cotton and kg of pyrethroid/acre of harvested cropland (n = 32, 3-h LC 24-h LC −0.0663 0.624 50 50 r = 0.3549, P = 0.0463), number of applications for plant bugs and 2014–2015 Dose–response regressions for field colonies (n = 43) year (n = 32, r = 0.3252, P = 0.0694), and acres of cotton and year 3-h Mort 15 μg 24-h LC −0.2829 0.0695 (n = 32, r = −0.3553, P = 0.0460). All other pairwise comparisons 3-h Mort 50 μg 24-h LC −0.5355 0.0003* were not significant (P = 0.05). 3-h LC 24-h LC −0.0615 0.6989 50 50 2014–2015 Dose–response regressions for USDA Lab (n = 16) 3-h Mort 15 μg 24-h LC −0.8818 <0.0001* Discussion 3-h Mort 50 μg 24-h LC −0.2518 0.3653 3-h LC 24-h LC 0.6036 0.0172* Results of this study confirm the continued presence of pyrethroid 50 50 resistance in tarnished plant bug populations in the Lower Mississippi *Significant correlation at P=0.05. Delta. Levels (or frequencies) of resistance appear to be as great as or Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/29/4939105 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 7 Table 5. Regression equations describing diagnostic dose mortality (DD 3 h) as a function of pyrethroid use (kg pyrethroid/acre) and diag- nostic dose mortality and pyrethroid use as functions of assay sample year, month, latitude and longitude Dependent variable Independent variable n r Intercept ± SE Slope ± SE F Ratio Prob > F DD 3 h kg pyrethroid/acre 233 0.0214 70.89 ± 3.61 −55.68 ± 1.77 5.1008 0.0248* DD 3 h sample year 233 0.0003 7.13 ± 18.79 −0.002 ± 0.009 0.0831 0.7734 DD 3 h sample month 233 0.0988 104.08 ± 8.212 −5.75 ± 1.14 25.3121 <0.0001* DD 3 h sample latitude 233 0.0066 164.91 ± 81.67 −3.02 ± 2.44 1.536 0.2165 DD 3 h sample longitude 233 0.0025 248.31 ± 240.19 −2.03 ± 2.64 0.5907 0.4429 kg pyrethroid/acre sample year 233 0.0058 −23.00 ± 21.45 0.01 ± 0.011 1.3561 0.2454 kg pyrethroid/acre sample month 233 0.0132 0.01 ± 0.002 0.001 ± 0.0003 3.1053 0.0794 kg pyrethroid/acre sample latitude 233 0.0311 −0.04 ± 0.02 0.002 ± 0.0001 7.4453 0.0068* kg pyrethroid/acre sample longitude 233 0.0152 0.13 ± 0.06 −0.001 ± 0.0002 3.6406 0.0576 *Statistically significant regression model (P = 0.05). The Crossett control location still appears to be susceptible to permethrin (87% mortality at the diagnostic-dose). Snodgrass et al. (2008) reported mortality of 92% for the Crossett colony exposed to the diagnostic-dose. The USDA ARS laboratory colony fed solely on meridic diet is not susceptible and exhibits variability from test to test (Tables 2 and 3) comparable to the variability in response among field populations. This laboratory colony is known to be more tolerant than many field colonies to several classes of insec- ticide chemistries (Parys et al. 2015, Parys et al. 2017). The physio- logical basis for this variability and general tolerance to permethrin is deserving of further investigation, especially since the current diagnostic-dose assay utilizes insects directly from the field with no knowledge of insect age or previous food source. Nutrition and host plant effect insect susceptibility to a number of different insec- ticides (Gordon 1961, Wood et al. 1981, Yu 1982, Liang et al. 2007, Jensen et al. 2016). An alternative approach would be to rear tar- nished plant bugs on green beans or other plant materials similar Fig. 3. Relationship between tarnished plant bug mortality at the diagnotic to the procedures used by Snodgrass and Scott (1999) in developing dose (DD of 15 μg of permethrin per vial for 3 h) and kg pyrethoid applied per acre of cropland across the 2008–2015 study period. (Regression the glass-vial assay for tarnished plant bugs and perhaps compare Y = 70.89 – 575.68X.) field control of cotton infested with the USDA Laboratory colony to that of feral field populations. Our recent field collections of insects greater than those previously reported. Snodgrass et al. (2008) tested from the Crossett area were all made in May and early-June. Perera 20 field populations (excluding the Crossett control location) and et al. (2015) studied the population genetics of 15 tarnished plant found that 45% of the populations had mortalities less than 60% bug populations in the Mississippi Delta by using 13 microsatellite at the 15 μg per vial diagnostic dose of permethrin. They also found markers and found a general trend for increased gene flow between 20% of the populations to be susceptible with mortalities greater than populations later in the season. They also postulated that selection 90% at the diagnostic dose. Over the 8 yr of this study, a total of 301 by insecticide sprays in cotton could have played a role in the tem- field populations were collected and assayed at the diagnostic-dose. poral variation observed in genetic structure. Perhaps, populations Of these, 41% were classified as resistant (<60% mortality), and 14% of tarnished plant bug from Crossett location later in the year would were classified as susceptible (>90% mortality) using Snodgrass’ crite- express more resistance. ria. Those populations between 60 and 90% mortality were not clas- Comparison of the diagnostic-dose response at 3 h with 24 h sified as either resistant or susceptible. While differences among years dose–response regressions yielded different results from that reported were evident (Table 1: range of 4 to 62% of populations resistant), the by Snodgrass et al. (2008). Mortality of bugs after 3 h of exposure to percent of tarnished plant bug populations considered to be resistant the 15 μg per vial dose of permethrin was highly correlated with the (42.1%) and susceptible (21.1%) in 2015 were almost identical to LC at 24 h across 16 experiments with the USDA Laboratory col- those reported by Snodgrass et al (2008) (45 and 20%, respectively). ony as reported for the field populations in Snodgrass et al. (2008). Differences in average mortality at the diagnostic dose were not signif- However, with the 43 field populations studied in 2014 and 2015 icant in analyses, but the percentage of populations considered to be (Table 3), mortality of bugs exposed to a 50 μg per vial dose was resistant suggested that sample sites in Arkansas (primarily Southeast more strongly correlated to 24-h LC s than that for the 15 μg per Arkansas) and the North Mississippi Delta had higher frequencies vial dose. This may suggest continued selection for additional resist- of resistant populations (61 and 84%, respectively) than Louisiana ance mechanisms. Zhu and Snodgrass (2003) measured elevated (28%), East Mississippi Delta areas bordering the Hills (42%), and cytochrome P450 levels in pyrethroid resistant strains of the tar- South Mississippi Delta (40%). The percent of populations consid- nished plant bug. Zhu and Luttrell (2015) and Fleming et al. (2016) ered to be susceptible was numerically greatest for the East Mississippi reported elevated levels of esterases and glutathione-S transferase Delta (35%). Populations susceptible in other regions were less than in Mississippi populations of the tarnished plant bug. Additional the 20% of populations reported to be susceptible (>90% mortality at research is needed to determine the impact of selection on tarnished diagnostic-dose) by Snodgrass et al. (2008). plant bugs by one class of insecticide on resistance of tarnished plant Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/29/4939105 by Ed 'DeepDyve' Gillespie user on 16 March 2018 8 Journal of Insect Science, 2018, Vol. 18, No. 2 Table 6. Mean (SEM) pyrethroid use, tarnished plant bug mortality at a diagnostic dose, and estimates of insecticide use and cotton acre- age for the South Delta Region of the Midsouth Year Mean ± SEM kg pyrethroid/ Mean ± SEM % tarnished plant bug Mean ± SEM acres of cotton acre cropland mortality at diagnostic dose 2008 0.008 ± 0.0017 66.3 ± 6.9 411758 ± 114465.4 2009 0.013 ± 0.0022 55.9 ± 10.1 318819 ± 100748.4 2010 0.021 ± 0.0081 53.5 ± 3.1 375333 ± 84994.8 2011 0.011 ± 0.0019 76.6 ± 1.4 451667 ± 96709.8 2012 0.012 ± 0.0036 58.4 ± 7.1 384167 ± 105122.3 2013 0.011 ± 0.0042 48.7 ± 3.4 220333 ± 54913.1 2014 0.006 ± 0.004 71.2 ± 14.6 260936 ± 47290.4 2015 0.009 ± 0.0015 76.6 ± 0.9 185000 ± 22546.2 ANOVA df = 7; F = 1.3105; P = 0.3073 df = 7; F = 1.8434; P = 0.1515 df = 7; F = 1.2973; P = 0.3129 Year Mean ± SEM no. insecticide applications for Mean ± SEM no. all foliar Mean ± SEM no. insecticide bollworm insecticide applications applications for plant bugs 2008 0.64 ± 0.054 b 5.3 ± 1.2 3.18 ± 0.907 2009 1.14 ± 0.308 ab 7 ± 1.1 4.02 ± 1.081 2010 1.95 ± 0.479 a 7.2 ± 1.3 3.84 ± 1.027 2011 1.42 ± 0.385 ab 8.6 ± 0.4 4.97 ± 1.021 2012 0.55 ± 0.161 b 11 ± 1 4.85 ± 0.676 2013 0.53 ± 0.07 b 10.8 ± 0.8 4.85 ± 0.93 2014 0.77 ± 0.035 ab 7 ± 2.4 4.84 ± 0.463 2015 0.93 ± 0.066 ab 7.6 ± 1.7 5.25 ± 0.627 ANOVA df = 7; F = 3.7809; P = 0.0130 df = 7; F = 1.1801; P = 0.3620 df = 7; F = 0.6712; P = 0.6937 *Means within a column followed by a common letter do not differ significantly, Tukey’s HSD test (P = 0.05). bugs to other classes of insecticide, especially since current chemical county/parish. There were no major differences among the states in controls are failing and growers are applying increased numbers of estimated numbers of insecticide applications made for plant bugs applications for control of these bugs on cotton (Gore et al. 2014, or all insects. Fleming et al. 2016). The presence of multiple resistance mechanisms Collectively, this study confirms the previous trends documented would not be surprising given the nearly 40 yr of exposure of tar- by Snodgrass et al. (2008) and suggests that tarnished plant bug nished plant bugs to pyrethroids and the recognition that control resistance to pyrethroids is still present. Given the extensive use of problems were associated with multiple classes of insecticides when insecticides to control tarnished plant bug in the Delta region and pyrethroid resistance was first detected (Snodgrass 1996b, Scott and the risk of selection for detoxifying mechanisms that may render Snodgrass 2000). In a review of insecticide trials for tarnished plant multiple classes of insecticide ineffective, efforts should be intensified bugs in 1999, Reed et al. (1999) reported that pyrethroids provided to develop management systems less dependent on insecticides. The 94% control of tarnished plant bugs in 1982, 73% in 1986, and development of the diagnostic-dose assay by Snodgrass and Scott about 56% in the late 1990s. They also reported a sharp decline (1999) provided a tool to determine if a plant bug population was in efficacy of organophosphates for control of tarnished plant bug. susceptible or resistant prior to treatment. Our work indicates that The exploration of possible associations among measured pyre- this diagnostic tool is still relevant and needed for monitoring. These throid susceptibility in tarnished plant bug populations, recorded tools can provide important information reasonably quickly regard- county/parish level use of pyrethroids and annual estimates of cotton ing the value of applying pyrethroid treatments for tarnished plant insect loss and control costs provided a few statistically significant bug in cotton. relationships. Mortality at the diagnostic dose was negatively cor- related with kilogram of pyrethroid applied per acre of harvested cropland and month of sample indicating that resistance levels Acknowledgments increase with increased use of pyrethroids and expanded exposure Nathan Little and K. Clint Allen provided early reviews of this manuscript. over the growing season. This is logical and a likely influence given Arnell Patterson, Charles Lanford, and Kenya Dixon are recognized for their the dynamics of cotton acreage and the sequence of multiple insec- significant effort in collecting and assaying insects throughout the course of ticide treatments used in cotton. Pyrethroid use was positively cor- these studies. Essanya Winder and Tabatha Nelson reared the USDA diet-fed laboratory colony. This collective work was supported through two National related with latitude indicating that more northern sample sites (i.e., Program 304 Crop Protection and Quarantine projects of the Agricultural North Delta) were associated with more use of pyrethroids. This Research Service. again could be indirectly associated with concentrations of cotton acreage within the landscape. Linear relationships between meas- ured plant bug mortality and cotton insect loss estimates were not References Cited observed. 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