Frank, 2014; Meineke et al., 2014). Factors Influencing Insecticide Efficacy against Individuals tasked with protecting Armored and Soft Scales trees from scale insects in urban envi- ronments need to select and time pesticide applications so they target 1 Carlos R. Quesada , Adam Witte, and Clifford S. Sadof the most susceptible stages of scales while minimizing impact on natural enemies (Cloyd, 2010; Frank, 2012; ADDITIONAL INDEX WORDS. pine needle scale, oleander scale, calico scale, striped pine scale, chemical control, crawler duration Rebek and Sadof, 2003; Robayo- Camacho and Chong, 2015). As SUMMARY. Scale insects (Hemiptera: Coccoidea) are among the most economically such, pesticides that have been cate- important pests of ornamental plants. Soft scales (Coccidae) are phloem-feeding gorized by the U.S. Environmental insects that produce large amounts of honeydew. By contrast, armored scales (Diaspididae) feed on the contents of plant cells and produce a waxy test that covers Protection Agency (EPA) as reduced their bodies. We studied two species of armored scales [pine needle scale (Chionaspis risk to human health and the environ- pinifoliae) and oleander scale (Aspidiotus nerii)] and two species of soft scales [calico ment are favorable candidates for use scale (Eulecanium cerasorum) and striped pine scale (Toumeyella pini)] to compare in a pest management program (EPA, efficacy of selected insecticides. In addition, we assessed how the duration of first 2010). Although applications of re- instar emergence might influence insecticide efficacy. Several reduced-risk insecti- duced-risk products to the crawling cides (chlorantraniliprole, pyriproxyfen, spiromesifen, and spirotetramat), horti- scales can be as effective as those culture oil, and two broad-spectrum insecticide standards (bifenthrin and products with higher risk chemistries dinotefuran) were evaluated. Efficacy of insecticides was consistent within each scale (Frank, 2012; Xiao et al., 2016), the family. Bifenthrin and pyriproxyfen were the only insecticides that killed soft scale insects. By contrast, all insecticides killed armored scales when the crawler stage was relative effectiveness of low risk ma- the target of application. Armored and soft scales may differ in susceptibility to terials can vary. pesticides because of likely differences in the chemical composition of their Scale insects have flightless adult integuments and covers. Finally, we found that the effectiveness of a single females and winged adult males. application of insecticide declined by >15% when the duration of the crawling Winged males have undeveloped juvenile period was increased from 1 to 4 weeks. Increases in duration of a scale mouthparts and live just long enough crawling period decreased the efficacy of a pesticide application. to find mates [hours to days (Kosztarab, 1996; Miller and Davidson, 2005; cale insects are among the most Outbreaks of scale insects are Rosen, 1990)]. The mobile first instar destructive pests that feed on more frequent in protected culture will settle and feed on plant substrates Sleaves, stems, and fruit of vege- and disturbed habitats, such as in within 24–72 h or crawl to a leaf edge tative and woody plants (Fulcher greenhouses and urban landscapes, and disperse in the wind (Ben-Dov et al., 2012). High densities of scale than in natural forests (Hanks and and Hodgson, 1997). During this insects can slow the rate of carbohy- Denno, 1993; Tooker and Hanks, time, crawlers are subject to high rates drate assimilation (Speight, 1991; 2000). Outbreaks have been attrib- of mortality due to depletion of avail- Washburn et al., 1985) and reduce uted to a reduction of natural enemies able host material, adverse environ- plant vigor. This can result in leaf caused by low plant and prey diver- mental conditions such as heavy chlorosis, branch dieback, or even sity, pesticide residues, dust, and high rains, or pesticide use (Rosen, 1990). death of the plant due to direct injury temperature (Hanks and Denno, Both armored and soft scale species or outbreaks of other insects and 1993; Luck and Dahlstein, 1975; may have univoltine and multivoltine pathogens (Hanson and Miller, Meineke et al., 2013; Price et al., life cycles depending on the geographic 1984; Hubbard and Potter, 2005; 2011; Raupp et al., 2001). In addi- and climatic conditions (Ben-Dov and Rebek and Sadof, 2003). Armored tion, urban warming might contrib- Hodgson, 1997; Miller and Davidson, scales, mealybugs (Pseudococcidae), ute to pest outbreaks due to the effect 2005; Robayo-Camacho and Chong, and soft scales are the most econom- of temperature on the fecundity and 2015; Rosen, 1990). ically important insects in this group temporal synchrony of scale insects, Armored scales feed primarily on (Miller et al., 2005). and their natural enemies (Dale and the contents of plant cells (Sadof and
Department of Entomology, Purdue University, 901 Units W State Street, West Lafayette, IN 47907 To convert U.S. to SI, To convert SI to U.S., We thank D. Richmond, M. Scharf, and R. Lopez for multiply by U.S. unit SI unit multiply by their comments on this manuscript; A. Caballero, A. Kissick, A. Rios, D. Peterson, E. Sorto, J. Realey, J. 29.5735 fl oz mL 0.0338 Prado, J. Wolf, O. Menocal, and R. Tuscan for their 0.3048 ft m 3.2808 help in the field and laboratory; and C. Bogran for 3.7854 gal L 0.2642 helpful discussions. The research was conducted in 2.54 inch(es) cm 0.3937 partial fulfillment of the requirements for PhD to C. 25.4 inch(es) mm 0.0394 Quesada who was supported by USDA APHIS Co- 6.4516 inch2 cm2 0.1550 operative Agreement 08-8218-0520-CA awarded to 1.6093 mile(s) km 0.6214 C. Sadof. 7.4892 oz/gal gÁL–1 0.1335 1Corresponding author. E-mail: cquesand@purdue. 11.1612 oz/inch gÁcm–1 0.0896 edu. 6.8948 psi kPa 0.1450 https://doi.org/10.21273/HORTTECH03993-18 ( F–32)/1.8 F C( C · 1.8) + 32
• June 2018 28(3) 267 RESEARCH REPORTS
Neal, 1993) and are characterized by and biology of armored and soft scales insecticides and 2) the duration of their waxy covering (Rosen, 1990). could explain why these two groups the scale crawler period. These wax covers, also called tests, of insects responded differently to start forming within 24–48 h after applications of insecticidal soap and Material and methods they settle to feed. The test is not horticultural oil (Quesada and Sadof, SCALE INSECTS AND INSECTICIDES. bound to the body of an armored 2017). For this reason, we hypothe- Reduced-risk insecticides (chloran- scale. It simply encloses the insect and size that armored and soft scales could traniliprole, pyriproxyfen, spiromesi- eggs. Within hours after armored respond differently to other pesticides fen, and spirotetramat) were chosen scales hatch, scale insects crawl under with that share a mode of action. In from a list provided by EPA (2016) or out of the test find, a place to settle addition, we hypothesize that tempo- because of their potential to be part and feed for the rest of their lives (Miller ral differences in the duration of the of an integrated pest management and Davidson, 2005; Rosen, 1990). dispersing crawler stage can affect the program that conserves beneficial Soft scales feed on phloem sap capacity of the insecticide applications insects (Cloyd et al., 2006; Frank, and produce honeydew (Ben-Dov to reduce scale populations. Armored 2012; Planes et al., 2013; Xiao and Hodgson, 1997; Kosztarab, and soft scales vary widely in the et al., 2016). Even though horti- 1996). Honeydew is composed duration of crawler periods because cultural oil can kill natural enemies mostly of sugars and amino acids of environmental conditions and bi- on contact (Oetting and Latimer, (Ben-Dov and Hodgson, 1997; ology (Frank et al., 2013). Thus, 1995), it was included in our list of Leroy et al., 2011; Volkl€ et al., because the crawler stage of scales is insecticides because of its ability to 1999; Woodring et al., 2004) and most vulnerable to insecticides, appli- kill scale insects with a minimal im- can lead to accumulation of black cation timing and frequency may pact on natural enemies due to the sooty mold on bark and leaves, which need to be adjusted to account for short-term residual toxicity (Raupp can reduce photosynthesis and plant differences in the biology of scale et al., 2001; Rebek and Sadof, 2003). growth (Ben-Dov and Hodgson, insects. Scale species, such as calico Dinotefuran and bifenthrin were chosen 1997; Hubbard and Potter, 2005). scale and pine needle scale, that lay all to represent the two most commonly In addition, honeydew supports sym- eggs at one time are more likely to be used broad-spectrum insecticide clas- biotic mutualisms with ants that pro- controlled with single application of ses, neonicotinoids, and pyrethroids vide protection from natural enemies insecticide if it is timed to coincide (Sparks and Nauen, 2015). All insec- (Hanks and Sadof, 1990; Vanek and with their brief crawler period. By ticides were applied using the highest Potter, 2010). Soft scale insects are contrast, other species, such as olean- labeled rate except for spirotetramat, covered mostly with honeydew (Ben- der and striped pine scale who lay which was applied to striped pine scale Dov and Hodgson, 1997; Kosztarab, a few eggs at a time, have a more at two different rates. A total of seven 1996). Once soft scales settle, some extended crawler period and are more insecticides with six different modes of species, such as striped pine scale, likely to avoid mortality from a single action were studied on either soft or remain in the same location (Clarke application of a short residual insecti- armored scale (Table 1). et al., 1989). Other species retain cide. Our laboratory colony of olean- We conducted experiments with functioning legs so they can move to der scale produced a continuous four species of economically impor- different parts of their host plant. For supply of crawlers that allowed us to tant scale insects to determine how example, second instar calico scales manipulate the crawler period to di- these different insecticides controlled feed on leaves during the summer and rectly test this hypothesis. soft and armored scales. Calico and move to the bark during the fall where The objectives of this research striped pine scales represented soft they complete their life cycle (Hubbard were to determine how the survival of scale, whereas pine needle and olean- and Potter, 2005). armored and soft scales was affected der scale represented armored scales. In previous studies, we found by 1) the application of selected re- Five experiments were conducted that differences in the morphology duced-risk and broader spectrum during 4 years in Indiana. Three of
Table 1. Insecticides and formulation rates tested for efficacy against armored and soft scale. Active ingredient Trade namez Rate (a.i.)y Application method IRAC mode of action no.x Water Horticultural oil Ultrafine Oil 20.00 gÁL–1 Foliar NA Pyriproxyfen Fulcrum 0.099 gÁL–1 Foliar 3A Spiromesifen Judo 0.067 gÁL–1 Foliar 23 Spirotetramat (low rate) Kontos 0.032 gÁL–1 Foliar 23 Spirotetramat (high rate) Kontos 0.063 gÁL–1 Foliar 23 Bifenthrin Talstar S 0.118 gÁL–1 Foliar 3A Chlorantraniliprole Acelepryn 0.058 gÁL–1 Foliar 28 Dinotefuran Transtect 70WSP 0.567 gÁcm–1 DBH Soil 4A zUltrafine Oil (Whitmire Micro-Gen Research Laboratories, St. Louis, MO), Fulcrum, Judo, and Kontos (OHP, Mainland, PA), Talstar S (FMC Corp., Philadelphia, PA), Acelepryn (E.I. du Pont de Nemours and Co., Wilmington, DE), and Transtect 70WSP (Rainbow Treecare Scientific Advancements, Minnetonka, MN). y1gÁL–1 = 0.1335 oz/gal, gÁcm–1 = 0.0896 oz/inch, DBH = diameter at breast height. xInsecticide Resistance Action Committee (IRAC): NA (smothering agents not included in IRAC classification), 3A (juvenile hormone mimics), 23 (inhibitors of acetyl-CoA carboxylase), 3A (sodium channel modulators), 28 (ryanodine receptor modulators), and 4A [nicotinic acetylcholine receptor (nAChR) competitive modulators].
268 • June 2018 28(3) the experiments were conducted un- 6 and 20 June and 16 and 30 July trees in downtown Indianapolis on 15 der field conditions on trees that were [0, 14, 40, and 58 d after treatment May and refrigerated at 4 C) were naturally infested with scale insects. (DAT), respectively]. On 2 May placed on each leaflet. After 12 h, The other two experiments were con- 2013, density of overwintering fe- females were removed, leaving only ducted in a shade house or laboratory males was assessed to determine the crawlers on the leaflets. Survival of using plants artificially infested with effect of insecticides from the pre- calico scale crawlers was estimated 7 d scale insects. vious year. Four branches were cho- later on 29 June. Crawlers that died sen randomly for each of the 25 trees before and after settling on the leaflet Soft scale studies and the number of live female scale were used to calculate survival (those CALICO SCALE. We selected 25 insects was counted on the terminal that crawled off the leaf into the honey locust trees (Gleditsia triacan- 30 cm of the branches. On 16 and 23 cotton substrate were not counted). thos), located in a restaurant parking May 2013 (14 and 21 DAT, respec- STRIPED PINE SCALE. The third lot in Fishers, IN (lat. 39.928119 N, tively), survival of overwintering fe- experiment was conducted on striped long. 86.0336224 W), that were nat- males was assessed to determine the pine scales feeding on scots pine trees urally infested with calico scale. Se- effect of the second application by (Pinus sylvestris). In 2014, a total of lected trees ranged in size from 6 to counting the number of dead and live 42 naturally infested trees were se- 16 inches in diameter at breast height females from four braches per each lected in a working Christmas tree treatment. If the scale was shriveled farm in Fort Wayne, IN. They were and had a buffer tree between them. The experiment was designed to tar- and the color was faded brown, it was 6 years old and 6 ft tall. The trees get first instar calico scales that had counted as dead. By contrast, if the were planted on 6-ft centers in rows settled on leaves in 2012 followed by scale was smooth and with white 10 ft apart. On 26 June, trees were applications that targeted overwinter- tufts, it was counted as live. Also, leaf blocked by location into groups ing females in Spring 2013. Five treat- samples were collected to assess the of six. Treatments were randomly effect of insecticides on the first and assigned to each tree in the block ments (chlorantraniliprole, bifenthrin, second instars on 17 June and 17 and (water, bifenthrin, pyriproxyfen, oil, dinotefuran, pyriproxyfen, and water) 29 July (46, 76, and 88 DAT, re- spirotetramat low rate, and spirote- were allocated to each of five trees in spectively). Densities of live scales tramat high rate) and applied at first a randomized complete block design. were calculated as during the previous observation on the crawler stage on Trees were blocked by location in the year. the selected trees. Applications were parking lot. Foliar and soil applications In addition to field tests, a labo- made to the canopy with a 3-gal were applied on 6 June 2012 and 2–3 ratory experiment was conducted in backpack sprayer until runoff. Efficacy May 2013. In both years, foliar in- 2012 on calico scale crawlers to de- of insecticides was assessed by collect- secticides were applied to each tree termine effects of fresh and aged in- ing three infested twigs from each canopy until runoff, using a high-pres- secticide residues on calico scale tree. Twigs were collected from sites sure sprayer (FMC John Bean, Phila- survival. In this study, we used scale- covered with sooty mold on 10 and delphia, PA) at 100 psi, whereas the free leaves collected on 21 June from 19 July, 24 Aug. 2014, and 6 May systemic insecticide (dinotefuran) was honey locust trees located in a nursery 2015 (14, 23, 59, and 314 DAT, applied at 20 psi with a subsoil injector in Westfield, IN (lat. 40.020767 N, respectively). We chose branches with whose probe penetrated 8 inches be- long. 86.188962 W). These trees remnants of sooty mold because it low the soil surface at four points had been treated with a foliar insecti- indicated that scales were present at within 1 ft of the trunk (Eliason and cide (chlorantraniliprole, bifenthrin, the start of the study. We assessed Potter, 2000; Hubbard and Potter, or pyriproxyfen) on 8 June, 2 weeks effects on male and female striped 2006). before the laboratory assay. Foliar pine scales separately because females Live scale densities were esti- applications were made with a 3-gal develop on stems, whereas males de- mated from 30 leaflets per tree. Leaf- sprayer (Solo Inc., Newport News, velop on the needles (Clarke et al., lets were obtained from five leaves VA) to runoff. Leaves that were 1989). In the laboratory, three 5-cm collected from different locations on treated on the day of the assay were twig sections were used to estimate trees from each treatment near sites collected from untreated trees and densities of striped pine scale females. where there was evidence of egg- sprayed to runoff with one of three Also, six needles were randomly se- laying females. Six leaflets from the foliar insecticides using a 32-fl oz lected from twigs to evaluate densities middle of each leaf were used. Each bottle sprayer (The Bottle Crew, of males, using the number of live scale was visually examined to deter- Farmington Hills, MI) on 22 June scales and length of needles. mine if it was dead or alive based on and allowed to dry. On 16 June 2015, a second ap- color (Hubbard and Potter, 2006). Leaflets from each treatment plication of insecticide was made Scales that were yellow were counted were placed in petri dishes atop of when crawlers were observed for the as live, whereas those brown to or- cotton wool dampened with water at first time on the trees. Effects of ange were counted as dead. The leaf a constant temperature of 25 Cand insecticides were examined as in the area of each sample was measured 16/8 h (light/dark). There were six previous year by collecting twigs on 1 using a leaf area meter (LI-COR Bio- replications for each of the eight and 15 July and 5 Aug. (15, 30, and sciences, Lincoln, NE) and the den- treatments arranged in a completely 50 DAT, respectively). In addition, sity of live scales was defined as the randomized design. On the day of the percentage of dead branches was total number per square centimeter of assay, 22 June, ovipositing female cal- assessed by visually estimating the leaf. In 2012, leaves were collected on ico scales (previously collected from percentage of brown needles on 26
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May and 15 July after the normal house located at the Throckmorton insect survival was assessed as de- period of spring needle drop (Sadof, Purdue Agricultural farm, 15 km scribed previously at 14 and 21 DAT. 1997). south of the West Lafayette campus of Purdue University. The plants were Data analysis Armored scale studies fertilized by mixing 15 mL of 19N– The effects of insecticides on Scots pine trees infested with 2.6P–10K slow-release fertilizer (Start- densities, mortality, and survival of were used in our fourth experiment N-Grow 19–6–12; Ferti-lome, Bonham, scale insects were examined using a re- located in a Christmas tree farm in TX) into the top 3 cm of soil at the peated measures analysis of variance Thorntown, IN. Naturally infested time of planting at the labeled rate and (ANOVA) with PROC MIXED (SAS trees were 6 ft tall. In 2015, a total watered as needed. version 9.3; SAS Institute, Cary, NC) of 48 trees were selected and grouped On 14 Sept., 42 plants were when response variables were quan- into eight blocks of six trees. The six selected to create a population of tifiedmorethanonce.One-way different treatments (water, bifen- scales that mimicked a week-long ANOVA was used to analyze the thrin, pyriproxyfen, spiromesifen, crawler emergence period during laboratory assay and the effect of in- horticultural oil, and spirotetramat) which scales could colonize plants. secticides on females the following were randomly allocated to trees in The plants were taken to the labora- year after application. Also, a two- the eight replicate blocks. On 12 tory for 1 week to infest them with the way factorial ANOVA was used to May, applications were made with crawler stage of oleander scales by determine the effect of 1- vs. 4-week a 3-gal backpack sprayer to the can- brushing live crawlers from a colony crawler period on the efficacy of the opy until runoff, targeting young of scale-infested butternut squash six treatments. Before data analysis, crawlers of the first generation of pine each day for 5 d. Enough scales were Shapiro–Wilk and Levene’s tests were needle scale insects. Three old needles transferred to assure a visually even conducted to determine normality (previous year’s growth) and three dusting of crawlers across treatments. and homogeneity of variance, respec- young needles (current year’s growth) The actual number of scales trans- tively. If data did not meet these were randomly selected from each ferred was not counted because of assumptions, square-root or arcsine plant and taken to the laboratory to logistical difficulties in counting mov- square-root transformations were ap- assess the number of live scale insects ing scale crawlers. After infestation, plied to densities or proportion (mor- per cm length on 0, 15, 30, and 77 plants were returned to the shade tality or survival) of scale insects, DAT. Under stereoscopic inspection, house and randomly assigned to one respectively. Live scale densities, mor- an ultrafine needle (12.7 mm) was of the six treatments (water, bifen- tality, and survival were used as a used to remove the shell of the insect thrin, pyriproxyfen, spiromesifen, response variable and insecticide treat- and perforate its body. Scale insects horticulture oil, or spirotetramat) on ment as the independent variable. were considered dead if the body was 21 Sept. 2015 in a completely ran- MeanswerecomparedwithaFisher’s dry and dark colored. By contrast, domized design. Applications were protected least significant difference. scales were counted as alive if it was made with a 3-gal sprayer until runoff In addition, linear contrasts were yellowish to orange and excreted he- targeting first instars between 2 and used to compare means of armored molymph when their bodies were per- 7 d old. At 15 and 21 DAT, five leaves scales that survived when the host forated with an ultrafine needle. infested with oleander scale were se- plant was colonized for 1 or 4 weeks LEANDER SCALE Oleander lected from each plant and taken to O . after insecticide application. scales were used to compare how the the laboratory to assess scale survival. duration of the crawler emergence Under a stereoscope, an ultrafine Results period affected effectiveness of a sin- needle (12.7 mm) was used to punc- gle insecticide application. Oleander ture the first 100 scale insects encoun- SOFT SCALE STUDIES. Compared scales produce crawlers continuously tered to determine if it was alive. with the water control, densities of year round (Uygun and Elekcxioglu, Insects that expulsed hemolymph when live immature calico scales were sig- 1998). The life cycle is completed in punctured were considered alive. nificantly reduced (F = 3.35; df = 4, 26 d and the seasonal oviposition On 16 Oct., a second set of 42 20; P = 0.030) by bifenthrin (45%) period of a population can last up to plants were taken to the laboratory to when applications targeted settled 126 d (Uygun and Elekcxioglu, 1998). establish an infestation of scales that crawlers in 2012 (Fig. 1A). During We used a laboratory colony of ole- mimicked a 4-week crawler emer- Spring 2013, density of live overwin- ander scale (Quesada and Sadof, gence period. This was achieved by tering females on branches was also 2017) maintained on the fruit of continually transferring scales from significantly reduced (F = 4.49; df = 4, butternut squash (Curcurbita max- the colony to the plants every other 24; P = 0.009) on trees treated with ima) to artificially infest english ivy day for 4 weeks, the approximate bifenthrin (43%) and pyriproxyfen (Hedera helix) plants to mimic either duration of oviposition by an olean- (58%) compared with the water con- 1 or 4 weeks of crawler emergence. der scale (Miller and Davidson, trol (Fig. 1B). Plants were purchased as plugs 2005). By Nov. 16, when the six In 2013, after a second applica- obtained from Midwest Ground- pesticides were applied, each infested tion targeted egg-laying adult females covers LLC (Chicago, IL) because plant contained first instar, second calico scale, bifenthrin was the only they had no history of pesticide use. instar, and adult stages. Treatments insecticide that significantly reduced These were transplanted into 1-gal were applied and allocated in a com- scale survival compared with the wa- pots during Summer 2015. The pletely randomized design as described ter control [F = 16.9; df = 4, 20; P > plants were maintained in a shade previously. Effect of insecticide on 0.001 (Fig. 2A)]. However, all the
270 • June 2018 28(3) treatments of adult scales except for chlorantraniliprole, ultimately re- duced the density of crawlers on leaves (F = 5.13; df = 4, 20; P = 0.005) compared with the control. The greatest reduction was produced by pyriproxyfen (57%) and bifenthrin (48%) followed by dinotefuran (36%) (Fig. 2B). Laboratory assays of calico scale survival showed significant differ- ences among treatments [F = 11.83; df = 8, 53; P < 0.001 (Fig. 3)]. As a group, survivorship on 7- and 21-d- old residues were not statistically dif- Fig. 1. Effects of insecticide applications on mean ± SE of settled (A) crawlers on ferent (F = 0.14; df = 1, 40; P = leaves and (B) adult females on branches, when applied to calico scale crawlers on 0.712). However, both 7- and 21-d- honey locust trees on 6 June 2012. Means followed by the same letter are not old residues significantly reduced sur- significantly different (P < 0.05) according to Fisher’s protected least significant vivorship compared with the water difference test; 1 nymph/cm2 = 6.4516 nymphs/inch2, 1 adult female/30 cm = control [(F = 11.69; df = 1, 40; P < 1.0160 adult female/ft. 0.001) and (F = 21.19; df = 1, 40; P < 0.001), respectively]. Survival of crawlers exposed to 7 and 21 DAT residues was significantly reduced by bifenthrin (to 15% and 16%) and chlorantraniliprole (to 28% and 19%, respectively) when compared with water control (70% surviving). In 2014, application of insecti- cides that targeted the peak of striped pine scale crawler emergence signifi- cantly reduced the number of females that settled on the branches [F = 7.02; df = 5, 36; P > 0.001 (Fig. 4A)] and males that settled on the needles [F = 4.69; df = 5, 35; P = 0.002 (Fig. 4B)]. Fig. 2. Effects of insecticide applications on mean ± SE of (A) egg-laying females on Bifenthrin reduced immature female branches and (B) settled crawlers on leaves, when applied to overwintering stages populations by 78% and immature of female calico scales on honey locust trees on 2–3 May 2013. Means followed by male populations by 57% compared the same letter are not significantly different (P < 0.05) according to Fisher’s with the controls. Pyriproxyfen re- protected least significant difference test; 1 nymph/cm2 = 6.4516 nymphs/inch2. duced the same groups by 48% and 25%, respectively. None of the insecticides applied Trees treated with a low rate of spi- to striped pine scale crawlers in 2014 rotetramat and horticultural oil had reduced the density of overwintering 5% and 10% branch mortality, re- adult females when compared with spectively. Later in the summer on the control in Spring 2015 [F = 15 July, water control (36%), horti- 3.51; df = 5, 37; P = 0.012 (Fig. cultural oil (32%), spirotetramat low 4C)]. However, pyriproxyfen pro- rate (13%), and spirotetramat high vided the same level of control as rate (8%) showed increase in branch bifenthrin at this time. Densities of mortality. By contrast, bifenthrin and adult scales on untreated control trees pyriproxyfen had no dead branches were low in 2015 because striped pine (Fig. 5). scales were already causing tree mor- ARMORED SCALE STUDIES. Under tality. Comparison of tree canopy field conditions, densities of live pine mortality showed statistically signifi- needle scales were significantly re- cant differences (F = 3.41; df = 5, 36; duced (F = 4.68; df = 5, 36; P = Fig. 3. Mean ± SE survivorship of P = 0.013) among treatments. All 0.002) by all the insecticides that calico scale crawlers on leaves with targeted peak crawler activity com- 7- and 21-d-old insecticide residues. treatments produced significantly less Means followed by the same letter are branch mortality than the water con- pared with the water control. Horti- not significantly different (P < 0.05) trol (27%). No branch mortality was cultural oil, pyriproxyfen, bifenthrin, according to Fisher’s protected least detected for bifenthrin, pyriproxyfen, and spiromesifen showed the greatest significant difference test; DAT = days and the high rate of spirotetramat. reduction of 52%, 45%, 39%, and 38%, after treatment.
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Fig. 4. Effects of insecticide applications on mean ± SE of striped pine scale crawlers and females on scots pine trees applied on 26 June 2014. A and B represent the effect for each insecticides on immature and C represents the effect on adults. Means followed by the same letter are not significantly different (P < 0.05) according to Fisher’s protected least significant difference test; LR = low rate, HR = high rate, 1 live settled female or male/cm = 2.54 live settled females or males/inch. respectively, followed by spirotetramat Davidson, 2005; Rosen, 1990; Sadof with a 34% reduction (Fig. 6A). and Neal, 1993). In addition, we found Survival of oleander scale on en- that prolonged periods of crawler ac- glish ivy was significantly lowered by tivity decreased insecticide efficacy. all insecticidal treatments [F = Both soft scale species, calico and 108.90; df = 5, 65; P < 0.001 (Fig. striped pine scales, were consistently 7A and B)]. Also, when insecticide controlled by bifenthrin and pyri- was applied to plants inoculated with proxyfen. Pyrethroids, such as bifen- crawlers for 1-week crawler survivor- thrin, affect the nervous system of the ship was 15% lower than when insect by preventing the closure of crawlers were inoculated for a 4-week sodium channel voltage gates in period [F = 42.80; df = 1, 65; P < membranes (Ishaaya, 2001; Yu, 0.001 (Fig. 8)]. There was no signif- 2015). In this study, bifenthrin was Fig. 5. Mean ± SE of mortality of scots icant interaction between insecticide the only insecticide that killed imma- pine trees due to a striped pine scale treatments and crawler period (F = ture stages and ovipositing adult soft infestation. Trees were sprayed on 26 108.90; df = 5, 65; P < 0.001). Plants June 2014 and 16 June 2015. scale insects. It produced rapid and Uppercase letters represent mortality treated with bifenthrin or horticul- long-lasting effects in the field and on 26 May and lowercase letters tural oil were the treatments with laboratory. When bifenthrin was ap- represent mortality on 15 July 2015. lowest survivorship of oleander scale plied early in the season to target Means followed by the same letter are followed by spiromesifen, spirotetra- ovipositing females, its residues on not significantly different (P < 0.05) mat, pyriproxyfen, and the water con- leaves were toxic enough to kill according to Fisher’s protected least trol (Fig. 7A and B). crawlers for at least 3 weeks. Pyriprox- significant difference test; LR = low yfen also provided consistent control rate, HR = high rate. Discussion of both species of soft scales. This We found the efficacy of insecti- insect growth regulator mimics juve- nile hormone activity (Ishaaya, 2001; insects. Its reported low residual tox- cides with different modes of action icity to natural enemies can eventually differed between soft scales and ar- Yu, 2015), and it is considered to be spare the natural enemies that facili- mored scales. Yet, it is common to a reduced-risk insecticide (EPA, tate sustained rates of scale insect find U.S. labels of insecticides with 2016). By contrast to bifenthrin, pyr- generalized instructions for manag- iproxyfen is an insect growth regula- mortality (Ellsworth and Martinez- ing all scale insects. These instructions tor. As such, it took longer to kill the Carrillo, 2001; Frank, 2012; Naranjo, can result in ineffective control be- insects and affected molting imma- 2001; Naranjo and Ellsworth, 2009). cause they underestimate biological ture stages only. However, our data Similar findings of what has been variability among species of scale can showed that several months after ap- termed bioresidual activity have been affect susceptibility to a particular in- plication, both pyriproxyfen and reported in other studies of hemipterans secticide. Scale insects differ greatly in bifenthrin had reduced population treatedwithpyriproxyfen(Naranjo, their external morphology and mode densities of soft scales to the same 2001; Naranjo and Ellsworth, 2009). of feeding on plant tissues. Soft scales levels. These findings are similar to Spirotetramat is a tetramic acid lack the waxy cover of armored scales, those reported by others working on derivative that inhibits lipogenesis and are phloem feeders, whereas ar- soft scales (Hubbard and Potter, in treated insects (Lummen€ et al., mored scales feed on other plant 2006). The effectiveness of pyriprox- 2014). Its efficacy against striped pine tissues (Ben-Dov and Hodgson, yfen may be attributed to more than scale was not different from water 1997; Kosztarab, 1996; Miller and its acute capacity to kill the scale controls. However, in the following
272 • June 2018 28(3) year, it depressed populations of over- females before leaves fully expanded. cover (Ben-Dov and Hodgson, wintering females and reduced dead Soil applications in early summer 1997; Kosztarab, 1996). Both cover canopy to the same extent as bifen- when crawlers were active failed to and integument together can contain thrin and pyriproxyfen. Like the control scales. Although failure may as much as 86% honeydew in wax long-term effects of pyriproxyfen, have been due to a lack of uptake scales (Coccidae), such as white wax this bioresidual activity might also during the historic drought of 2012 scale (Ceroplastes destructor), noted be explained by the purportedly low that occurred in Indiana at the time of for its high content of wax (13%) impact of spirotetramat on natural the study, others have also shown (Hackman, 1951; Tamaki and Kawai, enemies (Frank, 2012; Planes et al., inconsistencies with the efficacy of 1969). This honeydew is 95% water, 2013). Chlorantraniliprole and hor- soil-applied neonicotinoids against which can make the scale insect in- ticultural oil failed to control either soft scales (Hubbard and Potter, tegument highly polar (Ben-Dov and of the two soft scale insects. 2006). Thus, successful use of this Hodgson, 1997; Leroy et al., 2011; Dinotefuran performed incon- systemic material seems dependent Volkl€ et al., 1999; Woodring et al., sistently against calico scale on honey on following manufacturer’s recom- 2004). By contrast, armored scales locust. This highly mobile neonicoti- mendations for providing adequate feed primarily on the contents of noid affects insect nicotinic acetylcho- moisture after application. plant cells (Sadof and Neal, 1993). line receptors and can be applied as Like our studies of soft scales, These insects do not produce honey- a foliar, soil, or trunk applied systemic both species of armored scale dew and are characterized by a waxy (Simon-Delso et al., 2015). Dinote- responded to each insecticide in a con- cover, which forms within 24–48 h furan reduced calico scale densities sistent manner. However, unlike the after they settle and envelopes the when it was applied to the soil early soft scales, all the insecticides we top of their body. Covers are 50% in the spring against egg-laying tested had a negative effect on pine wax and quite hydrophobic (Miller needle scale and oleander scale pop- and Davidson, 2005; Rosen, 1990). ulations. Bifenthrin and horticultural We hypothesized that this reported oil gave the best control against both variation in chemical composition of armored scales. However, pyriproxy- integuments may be partly responsible fen, spirotetramat, and spiromesifen for observed differences in insecticide also significantly reduced the abun- efficacy between soft and armored dance of scales when compared with scales. The active ingredients of most the water control. Our findings are insecticides are nonpolar and thus consistent with other studies of insec- more likely to penetrate the hydro- ticides against armored scales (Frank, phobic integument of the armored 2012; Raupp et al., 2001; Rebek and scale (Yu, 2015). Sadof, 2003; Xiao et al., 2016). Therefore, it is not surprising to Differences among the patterns find that more of the products we of susceptibility to insecticides among tested killed armored scales rather Fig. 6. Effects of insecticide armored and soft scales support our than soft scales. The reason that applications on mean ± SE of pine hypothesis that biological differences bifenthrin and pyriproxyfen killed needle scale crawlers on scots pine between these families of scale insects both kinds of scales may be because trees treated on 12 May 2015. Means followed by the same letter are not can alter insecticide efficacy. When their modes of action were unaffected significantly different (P < 0.05) soft scale insects feed on phloem sap, by the differences in the properties according to Fisher’s protected least they produce a liquid excrement of armored and soft scale integu- significant difference test; 1 nymph/ called honeydew which together with ments. Beyond differences in penetra- cm2 = 6.4516 nymphs/inch2. other substances form their bulky tion due to integument composition (Benezet and Forgash, 1972; LeRoux and Morrison, 1954), other factors to consider may include differences in internal distribution, metabolism, target site interaction, and excretion of insecticides or their metabolites (Yu, 2015). For example, differences in the capacity of armored and soft scales to produce honeydew may be linked to fundamental differences in their excre- tion physiology that could affect in- secticide metabolism, excretion, and ultimately, toxicity. Soft and armored scales are among the most difficult insect pests Fig. 7. Effects of insecticide applications on mean ± SE survival of oleander scale to control (Fulcher et al., 2012). mimicking (A) 1-week and (B) 4-week emergence periods on english ivy plants in Timing of application is important Summer 2015. Means followed by the same letter are not significantly different (P < for effective management of scales be- 0.05) according to Fisher’s protected least significant difference test. cause they can become less susceptible to
• June 2018 28(3) 273 RESEARCH REPORTS
of wax to penetrate than older scales. By Frank, S.D. 2012. Reduced risk in- contrast, although crawlers were still the secticides to control scale insects and most susceptible stage of soft scale, the protect natural enemies in the production high polarity of soft scale integuments and maintenance of urban landscape may have increased their tolerance to plants. Environ. Entomol. 41:377–386. some insecticides. Thus, by contrast to Frank, S.D., W.E. Klingeman, S.A. White, armored scales, both timing and pesti- and A. Fulcher. 2013. Biology, injury and cide influenced the efficacy of the in- management of maple tree pests in nurs- secticides we tested for soft scales. For eries and urban landscapes. J. Integr. Pest this reason, it is important for practi- Mgt. 4:B1–B14. tioners to consider that differences be- Fritz,R.S.,N.E.Stamp,andT.G.Halverson. tween the biology and life history of scale 1982. Iteroparity and semelparity in insects. Fig. 8. Effect of 1- and 4-week insects could alter the efficacy of prod- Amer. Nat. 120:264–268. emergence periods on insecticide ucts labeled for scale insects. efficacy against oleander scale feeding Fulcher, A., W.E. Klingeman, J.H. Chong, A. on english ivy plants in 2015. Means LeBude, G.R. Armel, M. Chappell, S. Frank, (±SE) followed by the same letter are Literature cited F. Hale, J. Neal, S. White, and J. Williams- not significantly different (P < 0.05) Woodward. 2012. Stakeholder vision of fu- Ben-Dov, Y. and C.J. Hodgson. 1997. according to Fisher’s protected least ture direction and strategies for southeastern Soft scale insects: Their biology, natural significant difference test. US nursery pest research and extension pro- enemies and control. Vol. 7B. Elsevier gramming. J. Integr. Pest Mgt. 3:1–8. Science, Amsterdam, The Netherlands. insecticides as they age (Ebeling, 1936; Hackman, R.H. 1951. The chemical Benezet, H.J. and A.J. Forgash. 1972. composition of the wax of the white wax Phillips and Smith, 1963; Quesada and Penetration and distribution of topically Sadof, 2017). Our results are consis- scale, Ceroplastes destructor (Newstead). applied malathion in the house fly. J. Arch. Biochem. Biophys. 33:150–154. tent with findings by others who in- Econ. Entomol. 65:53–57. dicate that targeting armored scale Hanks, L.M. and R.F. Denno. 1993. at the crawler stage is critical to the Clarke, S.R., G.L. DeBarr, and C.W. Natural enemies and plant water relations Berisford. 1989. The life history of Tou- effectiveness of several insecticides with influence the distribution of an armored meyella pini (King) (Homoptera: Cocci- scale insect. Ecology 74:1081–1091. different active ingredients and classes dae) in loblolly pine seed orchards in (Fondren and McCullough, 2005; Georgia. Can. Entomol. 121:853–860. Hanks, L.M. and C.S. Sadof. 1990. 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