Dispersion, efficacy, and persistence of dichlorvos aerosol against two flour beetle life stages in a mill

Journal of Stored Products Research 59 (2014) 96e100

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Dispersion, efficacy, and persistence of dichlorvos aerosol against two flour beetle life stages in a mill Bhadriraju Subramanyam a, *, Dhana Raj Boina a, Frank H. Arthur b a b

Department of Grain Science and Industry, Kansas State University, Manhattan, KS 66506, USA USDA-ARS, Center for Grain and Animal Health Research, Manhattan, KS 66502, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Accepted 26 May 2014 Available online

The dispersion, efficacy, and persistence of dichlorvos applied as an aerosol inside the Kansas State University pilot flour mill was evaluated based on responses of adults of the confused flour beetle, Tribolium confusum, and pupae of the red flour beetle, Tribolium castaneum, during and after application. Dichlorvos was applied at the highest labeled rate of 0.35 g/m3. Concrete arenas with or without different life stages of the two species were placed in open, obstructed, and concealed mill locations during aerosol application. Knockdown and mortality of T. confusum adults was 99e100% and mortality of T. castaneum pupae was 97e100% in open and obstructed mill locations, indicating uniform dispersion of dichlorvos. In concealed locations, knockdown and mortality of T. confusum adults and mortality of T. castaneum pupae was 85e94%, indicating effective dispersion of dichlorvos into pieces of equipment. Holding insects directly exposed to dichlorvos for an additional 24 h in the same arenas did not increase knockdown or mortality. Exposure to dichlorvos residues aged for an additional 24 h on concrete resulted in moderate to poor knockdown and/or mortality of Tribolium spp. suggesting lack of residual activity. Results show dichlorvos will give immediate kill of exposed insects but will not offer effective residual control. © 2014 Elsevier Ltd. All rights reserved.

Keywords: Dichlorvos Aerosol distribution Residual activity Tribolium confusum Tribolium castaneum

1. Introduction The use of methyl bromide for structural fumigation has been discontinued in the United States, except for certain critical uses, as per the agreement reached under the Montreal Protocol (Fields and White, 2002; Anonymous, 2004). Alternative fumigants such as phosphine (ECO2FUME®) and sulfuryl fluoride (ProFume™), currently available for insect pest management in flour mills, have certain limitations. Phosphine reacts with exposed metals and electrical equipment causing corrosion (Bond et al., 1984) and some strains of stored-product insects have developed resistance to it (Arthur et al., 1988; Zettler, 1990). Eggs of stored-product insects are hard to kill at labeled rates of sulfuryl fluoride rendering it less economical (Bell and Saviddou, 1999; Small, 2007; Baltaci et al., 2009; Hartzer et al., 2010; Athanassiou et al., 2012). In addition, during fumigation food-processing facilities should not be in operation and must be sealed relatively air-tight. Structural heat

* Corresponding author. Tel.: þ1 785 532 4092; fax: þ1 785 532 7010. E-mail address: [email protected] (B. Subramanyam). http://dx.doi.org/10.1016/j.jspr.2014.05.005 0022-474X/© 2014 Elsevier Ltd. All rights reserved.

treatments are viable alternatives to fumigants but can be expensive and may not be suitable for use in all facilities (Subramanyam et al., 2011). In recent years, use of aerosols for managing insects in foodstorage and food-processing facilities is becoming popular as an alternative to fumigants and heat treatments (Jenson et al., 2010a, b; Sutton et al., 2011; Boina and Subramanyam, 2012). This technique is also known as space spray, fogging, or ultra-low volume (ULV) application depending on the equipment and insecticide formulation used and particle sizes dispersed. In a typical aerosol application, the formulated insecticide is dispensed as fine particles of 5e50 mm through an atomizer (Peckman and Arthur, 2006). In the present study, dispersion, efficacy and residual activity of a new formulation of dichlorvos, Vap-20® with carbon dioxide (Chem-Tech Ltd., Des Moines, IA, USA), applied as aerosol at the high labeled rate of 0.35 g/m3 (0.07 g(AI)/m3), was evaluated for control of adults of the confused flour beetle, Tribolium confusum (Jacquelin du Val), and pupae of the red flour beetle, Tribolium castaneum (Herbst), in a pilot flour mill. These two species are commonly associated with flour mills (Good, 1937; Salmond, 1956; Buchelos, 1981; Campbell and Arbogast, 2004).

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2. Materials and methods 2.1. Insects Adults of T. confusum and pupae of T. castaneum used in the experiments were obtained from cultures maintained on 95% white wheat flour plus 5% brewer's yeast (by weight) at 28  C and 65% r.h. in the Stored-Product Insects Research and Education Laboratory (SPIREL), Department of Grain Science and Industry, Kansas State University, Manhattan, KS, USA. These insects have been in rearing since 1999 without insecticide exposure and are hence assumed to be insecticide-susceptible. Unsexed adults of mixed ages of T. confusum were collected directly from 0.94-L culture jars after sifting the bleached wheat flour plus 5% by weight of brewer's yeast diet using an 841-mm opening sieve (Seedburo Equipment Company, Chicago, IL. USA). To collect 1e2 day old pupae of T. castaneum, 50 unsexed adults of mixed ages were introduced into 150-ml plastic containers containing 30 g of bleached flour previously sifted through a 250-mm opening sieve. After 2 d at 28  C and 65% r.h., the flour was sifted through an 841-mm opening sieve to remove adults. The flour with eggs in containers was held at the rearing conditions for 24 d before sifting the flour through a 250mm sieve to collect pupae (Brijwani et al., 2012).

Table 1 Obstructed and concealed locations of concrete dishes among the five floors of the Hal Ross pilot flour mill.a Floor

Placement of concrete arenas

Location number within a floor

Location description

First

Obstructed

1 2

Beneath the roller mill Beneath the semolina bag station Beneath the air-lock hoppers Inside the roller mill Inside the roller mill Inside the roller mill Beneath flour transport screw conveyers Beneath scourer/aspirator Beneath patent/clears scales Inside the precision grader Inside the color sorter Inside the hopper Beneath the polisher Beneath the cylinder separator Beneath the spouting Inside the pneumatic piping Inside the cylinder separator Inside the disc separator Beneath the hand add station Beneath the flour bin Beneath the cyclones Inside the sifting station Inside the combi-cleaner Inside the sifter Beneath the first break scale Beneath bin-vent filter Beneath the cyclones Inside the cyclones Inside the micro ingredient feeders Inside the Carter Day screen separator

Concealed

Second

2.3. Bioassay methods (treatments) Ready-mix concrete (Rockite, Hartline Products Co. Inc., Cleveland, OH, USA) was mixed with water to make a slurry. The slurry was poured into Petri dishes (90-mm diam. and 15 mm high) to approximately half the height of the dish. The concrete was allowed to dry for several days in the laboratory at room conditions. These concrete arenas were used for insect exposure in the mill. The arenas had either no insects or 10 unsexed adults of mixed ages of T. confusum or 10 pupae of T. castaneum. Adults of T. castaneum were not used for direct aerosol exposure because of their tendency to fly. On each floor, arenas were placed at three open locations where they were not obstructed by equipment or mill structural components, three obstructed locations where aerosol deposition was partially obstructed by equipment or structural components, and three concealed locations where aerosol deposition was hindered because arenas were placed inside pieces of mill equipment. The obstructed and concealed locations on each floor are identified in Table 1. On each mill floor and location, four bioassay methods or insect exposure treatments were evaluated by placing two arenas with T. confusum adults and two arenas with T. castaneum pupae and four arenas without insects. There were a total of eight arenas per location and 72 arenas per floor and 360 arenas in the entire mill. Arenas without lids were placed in the mill 1 h prior to aerosol application. The four bioassay methods or treatments evaluated were: T1, direct exposure of arenas with insects to dichlorvos

Obstructed

Concealed

Third

Obstructed

Concealed

Fourth

Obstructed

Concealed

2.2. Dichlorvos application The aerosol treatments were made in the Hal Ross pilot flour mill at Kansas State University, Manhattan, KS, USA, which has five floors occupying a total volume of 9628 m3. The layout of the mill has been described in detail by Brijwani et al. (2012). The airhandling system was shut down during the aerosol treatment. The dichlorvos formulation (Vap-20®, 20% dichlorvos plus 80% carbon dioxide by weight) was applied as an aerosol at the highest labeled rate of 0.35 g/m3 by dispensing 614, 684, 717, 642, and 773 g of dichlorvos in the first (floor volume, 1756.4 m3), second (2088.7 m3), third (1946.3 m3), fourth (1946.3 m3) and fifth (2231.1 m3) mill floors, respectively. The mill temperature was 27  C and 42% r.h.

97

Fifth

Obstructed

Concealed

3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3

a Open locations where concrete arenas were placed included mill areas free of obstruction or concealment from any pieces of equipment or structures.

during fogging and until the facility was cleared 24 h later; T2, direct exposure of insects to dichlorvos during fogging and until the facility was cleared plus an additional 24 h exposure in the same arenas that were held in a laboratory growth chamber at 28  C and 65% r.h. (48 h); T3, exposure of insects for 24 h in the laboratory at 28  C and 65% r.h. to dichlorvos residues in arenas that were exposed to dichlorvos aerosol in the mill without insects; and T4, which was same as T3, except that arenas were held at 28  C and 65% r.h. for 24 h before exposing insects for another 24 h at controlled conditions. After aerosol application, arenas were collected the following day (24 h) after the mill was ventilated. Adults of T. confusum or pupae of T. castaneum were added (10 insects/arena) immediately after bringing dishes to the laboratory (T3) or after aging residues for 24 h (T4). For each of the treatments T1eT4, a set of nine untreated arenas (3 each corresponding to open, obstructed, and concealed locations) with 10 adults of T. confusum or nine arenas with 10 pupae of T. castaneum per dish, held at 28  C and 65% r.h. in a laboratory growth chamber, served as the control treatment. After the exposure periods mentioned above, all arenas including untreated controls, were examined to assess insect knockdown and/or mortality. Adults of T. confusum that could not walk or right themselves when gently stimulated with a camel's hair brush were considered knocked down. After this assessment, all adults of T. confusum and pupae of T. castaneum in treatments T1eT4 were transferred to untreated arenas with 3 g of bleached flour plus 5% by weight of brewer's yeast diet. These arenas were incubated at 28  C and 65% r.h. for 7 d to assess mortality. Adults of

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2.4. Statistical analyses Knockdown and mortality data for T. confusum was not corrected for control mortality as the mean ± SE (n ¼ 9) knockdown and mortality in the control treatment ranged from 0 to 3.3 ± 1.7%. However, mean ± SE control mortality of T. castaneum in T1, T2, T3, and T4 treatments was 14.2 ± 2.9, 13.3 ± 3.7, 12.2 ± 3.2, and 12.2 ± 2.2%, respectively. Mortality of T. castaneum pupae in T1eT4 treatments was corrected for corresponding control mortality using Abbott's (1925) formula. Percentage knockdown and mortality data for T. confusum and corrected mortality data for T. castaneum in treatments were transformed to angular values for normalizing heteroscedastic treatment variances and subjected to a two-way analysis of variance (ANOVA) to determine significant differences among the four treatments and three locations (main effects) and their interaction (SAS Institute, 2005). All differences were considered significant at a ¼ 0.05. The treatment and location interaction was not significant (P > 0.05) for knockdown and/or mortality responses for both species. Therefore, differences in insect responses among the four bioassay methods and three locations were determined using one-way ANOVA, and treatment means were separated using Bonferroni t-tests (SAS Institute, 2005). 3. Results The main effects of treatment (df ¼ 3, 48) and location (df ¼ 2, 48) for T. confusum were significant for knockdown (F ¼ 256.68 (treatment) and 6.04 (location); P ¼ 0.0046) and mortality (F ¼ 148.55 and 3.71; P  0.0316). However, the treatment and location interaction effect (df ¼ 6, 48) was not significant for knockdown (F ¼ 1.30; P ¼ 0.2734) or mortality (F ¼ 0.91; P  0.4950). One-way ANOVA showed significant differences among the four treatments and the three locations for T. confusum knockdown (F ¼ 71.81; df ¼ 11, 48; P < 0.0001) and mortality (F ¼ 41.69; df ¼ 11, 48; P < 0.0001). The knockdown of T. confusum adults was 99e100% when adults were directly exposed to dichlorvos in the mill (T1) at open and obstructed locations, and it was significantly lower (85%) in dishes that were exposed at concealed locations (Fig. 1). Knockdown of insects exposed in the mill and held on the same arenas in the laboratory (T2) was similar to that observed in the T1 treatment. Irrespective of the location, exposure of adults to 0- and 24-h-old residues of dichlorvos (T3 and T4) for 24 h in dishes showed a significant reduction in knockdown which ranged from 0 to 43%. None of the knocked down adults recovered and all eventually died, and trends in adult mortality mirrored that of knockdown. In the T3 treatment, mortality of adults was 12e19% higher when compared with percentage knocked down (Fig. 2). Dichlorvos residues on arenas held for an additional 24 h before insect exposure showed little or no insecticidal activity (T4). Results for T. castaneum showed significant differences among the four treatments (F ¼ 151.53; df ¼ 3, 48; P < 0.0001) and the three locations (F ¼ 4.49; df ¼ 2, 48; P ¼ 0.0163), but the treatment and location interaction was not significant (F ¼ 0.77; df ¼ 6, 48; P ¼ 0.5899). One-way ANOVA showed significant differences in T. castaneum mortality among treatments and locations (F ¼ 42.57; df ¼ 11, 48; P < 0.0001). Mortality of T. castaneum pupae in T1 and T2 treatments was essentially similar among the three locations,

100

Knockdown (% Mean + SE)

T. confusum that did not respond when prodded with a camel's hair brush or T. castaneum pupae that failed to emerge as adults were counted as dead. Mortality counts were converted to percentage values for analysis. Each treatment combination was replicated five times (five floors).

a a

a a Open Obstructed Concealed

a

a

80 60

b

40

b

bc

20 c c c

0 T1

T2

T3

T4

Treatments Fig. 1. Mean þ SE (n ¼ 5) percent knockdown of T. confusum adults exposed directly in concrete arenas to dichlorvos until the facility was cleared (24 h) (T1); direct exposure of insects to dichlorvos until the facility was cleared plus an additional 24 h exposure to the same dishes in a laboratory growth chamber at 28  C and 65% r.h. (48 h) (T2); exposure of insects for 24 h in the laboratory to 0-h-old dichlorvos residues on dishes collected at 24 h from the mill (T3); and exposure of insects for 24 h in the laboratory to 24-h-old dichlorvos residues (T4). Means among treatments and open, obstructed, and concealed locations with different letters are significantly different from one another (P < 0.05; by Bonferroni t-tests).

and was significantly greater than mortality observed at three locations in treatments T3 and T4 (Fig. 3). However, pupal mortality in the T4 treatment was essentially zero and was lower than mortality observed in the T3 treatment, irrespective of the location. 4. Discussion The significant differences observed in knockdown and/or mortality among the bioassay methods is due to significantly lower knockdown and/or mortality observed in T3 and T4 treatments relative to T1 and T2 treatments. The significant difference observed among locations was due to insects in concrete arenas at concealed locations, especially in the T1 and T2 treatments, showing lower knockdown and/or mortality when compared to

100

Mortality (% Mean + SE)

98

aa

a a

Open Obstructed Concealed

ab

ab

80

bc c

60

cd

40 20

d dd 0 T1

T2

T3

T4

Treatments Fig. 2. Mean þ SE (n ¼ 5) percent mortality of T. confusum adults in T1eT4 treatments (see caption to Fig. 1). Means among treatments and open, obstructed, and concealed locations with different letters are significantly different from one another (P < 0.05; by Bonferroni t-tests).

B. Subramanyam et al. / Journal of Stored Products Research 59 (2014) 96e100

100

a a

a a

ab

ab

Mortality (% Mean + SE)

Open Obstructed Concealed

80

bc

60

c cd

40 20

d d d

0 T1

T2

T3

T4

Treatments Fig. 3. Mean þ SE (n ¼ 5) percent mortality of T. castaneum pupae in T1eT4 treatments (see caption to Fig. 1). Means among treatments and open, obstructed, and concealed locations with different letters are significantly different from one another (P < 0.05; by Bonferroni t-tests).

those in open and obstructed locations. The lack of treatment and location interaction was due to the trends in knockdown and/or mortality for each species being consistent among the four treatments and the three locations. Dispersion of dichlorvos applied as an aerosol was uniform throughout each mill floor, because of similar level of mortality of life stages of Tribolium spp. observed in open and obstructed locations. Gillenwater et al. (1971), Harein et al. (1970, 1971), and Cogburn and Simonaitis (1975) conducted chemical analysis of air samples in warehouses treated with dichlorvos and confirmed uniform dispersion of dichlorvos in facilities containing packaged foods. Arthur (2010) documented that the degree of mortality of T. confusum and T. castaneum larvae was more or less equal in concrete arenas that collected pyrethrin plus pyriproxyfen aerosol residues at open and obstructed locations in a flour mill. The 85e94% knockdown and/or mortality of the Tribolium spp. observed in concealed locations suggests that dichlorvos aerosol particles did disperse inside pieces of equipment where the dishes with insects were placed. Similar observations were made by Arthur (2008) and Jenson et al. (2010a, b) in their field trials. Mortality was slightly higher than knockdown in treatment T3 for T. confusum, suggesting delayed toxic effects. However, this brief toxic effect is lost when residues were aged for an additional 24 h. Similarly, some residual activity against T. castaneum pupae was observed with 0-h residues (T3 treatment). The additional mortality effects observed in the T3 treatment for T. confusum were camouflaged in the T2 treatment, because in the T2 treatment adult mortality was 100% or close to 100%, hence there were no benefits to exposing insects after removal from the mill for an additional 24 h. The relationship between the lack of residual activity of dichlorvos and resistance development in insects is unknown. Dichlorvos aerosol had been used extensively in the southeastern United States in bulk flat storages containing in-shell peanuts, primarily for control of Plodia interpunctella (Hübner), the Indianmeal moth, and Cadra caultella (Walker), the almond moth (Arthur et al., 1988). Timed application systems released the aerosol into the headspace of a warehouse on a regular basis, often daily, but effects were probably limited to the headspace and the top portion of the surface layer of the peanuts. Resistance assessments done during the 1980s and 1990s all indicated some level of resistance in

99

T. castaneum to dichlorvos (Halliday et al., 1988; Zettler and Arthur, 1997). However, there have been no further assessments of resistance to dichlorvos in any postharvest system in the United States. There is a need to determine the possibility of resistance development in insects if dichlorvos aerosol is used on a regular basis in flour mills. Dichlorvos offered immediate control of T. confusum adults and T. castaneum pupae that were directly exposed to the aerosol in the flour mill, but showed poor residual activity 24e48 h after application. Therefore, dichlorvos may need to be reapplied frequently to control insect populations in a flour mill. The label suggests weekly application, but the timing of application should be based on insect monitoring data. Combining dichlorvos application with an insect growth regulator such as methoprene or pyriproxyfen may improve residual activity. Adding pyriproxyfen or methoprene to synergized pyrethrins increased residual activity by 10e16 weeks and significantly reduced the emergence of adults from 4-wk-old larvae of T. castaneum and T. confusum exposed to the residues collected in concrete arenas with flour during aerosol application (Arthur, 2010; Sutton et al., 2011). In our study, food was not provided to insects during dichlorvos exposure, but in other studies, the presence of food (flour) during exposure increased recovery of Tribolium spp. Addition of food to arenas with exposed adults or transfer of exposed adults to new dishes with or without flour resulted in recovery of T. castaneum and T. confusum life stages when they were exposed to diatomaceous earth (Arthur, 2000a), a non-aerosol formulation of cyfluthrin (Arthur, 2000b), an aerosol formulation of pyrethrins, synergized pyrethrins plus an insect growth regulator, permethrin, d-phenothrin, and esfenvalerate (Kirkpatrick and Gillenwater, 1979, 1981; Arthur and Campbell, 2008; Toews et al., 2010). The recovery of insects increased with an increase in the amount of food provided (Arthur and Campbell, 2008; Toews et al., 2010). However, irrespective of exposure location in the mill, we did not see recovery of knocked down T. confusum adults even after transfer to food for 7 d. Therefore, the presence of food may play an important role in survival of these species when they are directly exposed to dichlorvos aerosol, but this assumption needs to be verified under field conditions. In summary, dichlorvos was effective in controlling adults of T. confusum and pupae of T. castaneum in a flour mill environment, mostly in open and obstructed locations. Dichlorvos lacks residual effectiveness and dispensing it with either approved synthetic pyrethroids or insect growth regulators may improve its residual activity against Tribolium spp. Acknowledgements The authors thank Monika Brijwani for technical assistance, and the Industrial Fumigant Company, LLC, Lenexa, KS, USA, for making the dichlorvos aerosol applications in the flour mill. Research reported here was partially supported by a grant from the United States Department of Agriculture-National Institute of Food and Agriculture (USDA-NIFA) Methyl Bromide Transitions Program under agreement number 2010-511-02-21660. We thank Dr. Kun Yan Zhu for reviewing the paper prior to journal submission. This paper is contribution number 13-224-J of the Kansas State University Agricultural Experiment Station. References Abbott, W.S., 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265e267. Anonymous, 2004. Notice of proposed rulemaking-protection of stratospheric ozone: process for exempting critical uses from the phase out of methyl bromide. Fed. Regist. 69, 52365e52402.

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