Effect of a Plant Growth Regulator Prohexadione-Calcium on ... - BioOne

HORTICULTURAL ENTOMOLOGY

Effect of a Plant Growth Regulator Prohexadione-Calcium on Insect Pests of Apple and Pear G. S. PAULSON,1 L. A. HULL,2

AND

D. J. BIDDINGER2

J. Econ. Entomol. 98(2): 423Ð431 (2005)

ABSTRACT The effect of prohexadione-calcium, a plant growth regulator that inhibits gibberellin metabolism, on Cacopsylla pyricoloa (Foerster) in pear trees, and Choristoneura rosaceana (Harris) and Aphis spireacola Patch, in apple trees was studied. C. pyricoloa and A. spireacola populations were signiÞcantly reduced in prohexadione-calcium-treated pear and apple, respectively. Insecticide control of both pests with imidacloprid was synergized in treatments with prohexadione-calcium. In apples treated with prohexadione-calcium, there was a signiÞcant reduction in the number of C. rosaceana shelters per tree and amount of fruit injury at harvest attributable to the C. rosaceana. There was an additive effect when tebufenozide was used to control C. rosaceana in trees treated with prohexadionecalcium. Prohexadione-calcium signiÞcantly reduced vegetative growth in both pears and apples. Synergistic and additive treatment effects of prohexadione-calcium and pesticides used in this study may be due to better penetration and coverage of pesticides due to reduced foliar growth or to changes in the nutritional quality of the host plants. KEY WORDS prohexadione-calcium, leafroller, pear psylla, spirea aphid

MODIFICATION OF A TREE FRUIT host plant as a horticultural tactic of “integrated crop management” is generally associated with selective breeding programs for disease- and insect-resistant varieties. Other horticultural control tactics, however, such as summer pruning of water sprouts in pears to reduce pear psylla, Cacopsylla pyricoloa (Foerster), populations have been used in many fruit-growing regions for decades (Burts 1970, Hull 1993). Direct damage to pear fruit by pear psylla has been shown with higher tree nitrogen availability (Pfeiffer and Burts 1983, 1984), which has resulted in recommendations to reduce nitrogen fertilization to the minimum necessary for proper tree growth and fruit production (Hull 1993). Several species of aphids, including the apple aphid, Aphis pomi De Geer, also are known to prefer newly developing leaves on shoots rather than older mature leaves, because of the higher nitrogen content (Hukusima and Ando 1967, Takeda et al. 1967). Brown and Welker (1992) found A. pomi and spirea aphid, Aphis spireacola Patch, to be less abundant in unmanaged orchards than in commercially managed orchards because of lower tree vigor and fewer succulent shoots. Chemical modiÞcation of a host plant through the application of the plant growth hormone daminozide (Alar) to reduce shoot growth was successful in reducing populations of apple aphid on apple 31 yr ago (Hall 1972) and pear psylla populations on pear 23 yr ago (Wes1 Department of Biology, Shippensburg University, Shippensburg, PA 17257. 2 Penn State Fruit Research and Extension Center, Biglerville, PA 17307.

tigard et al. 1980). However, daminozide was voluntarily withdrawn from registration in 1989 due to intense public concern over the safety of residues on fruit to children. The recent registration of another plant growth regulator, prohexadione-calcium (Apogee, BASF Corp., Research Triangle Park, NC) in the United States offers a new opportunity in the use of host plant modiÞcation as a tactic in controlling pest populations in apple and pear orchards. Prohexadione-calcium reduces vegetative growth by interfering with the biosynthesis of the plant hormone gibberellin, which regulates cell elongation (Griggs et al. 1991, Nakayama et al. 1992). Due to a very low mammalian toxicity, low propensity for crop residues, a benign ecotoxicological proÞle, and nonpersistence in the environment due to rapid photodegradation and microbial metabolism, prohexadionecalcium has been classiÞed as a “reduced risk” pesticide by the Environmental Protection Agency (Winkler 1997). Prohexadione-calcium was registered for use in apples in 2000 but is not yet certiÞed for use in pears. As a plant growth regulator exerting powerful effects on apple and pear physiology, it is important to understand the effects of these host modiÞcations on both disease and arthropod pests. Prohexadione-calcium, by reducing tree canopy density, has been shown to enhance control of apple and pear diseases through improved coverage of fungicide applications and by reducing leaf wetness duration (Byers et al. 1997, Cooley et al. 1997, Yoder et al. 1999). Chemical control of several apple and pear insect pests also could be enhanced by a reduction in tree vigor. Excessive vegetative growth produces a

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tree canopy that is too dense for effective penetration of pesticide sprays and may result in increased fruit loss due to damage caused by insects and diseases that are not adequately controlled. In addition, it is difÞcult to maintain a pesticide residue on vigorously growing shoots without repeated pesticide applications (Cooley et al. 1997, Hogmire 1998, Waldstein 2000). Of particular interest are the effects of prohexadionecalcium on populations of the obliquebanded leafroller, Choristoneura rosaceana (Harris), and A. spireacola on apple and C. pyricola on pear. These pests have life histories that are strongly linked with the production of lush succulent leaves associated with new growth (Westigard et al. 1980, Brown and Welker 1992, Hull et al. 1995, Pfeiffer et al. 1995, Waldstein 2000). We, therefore, evaluated the effect of prohexadione-calcium on the efÞcacy of current insecticide control programs used for obliquebanded leafroller and spirea aphid control in apple and for pear psylla control in pears. Materials and Methods Apple. Studies were carried out at the Pennsylvania State University Tree Fruit Research and Extension Center in Biglerville, PA, between May and September 1999 and 2000. Six treatments were applied to single-tree plots of apple in a randomized complete block design. In 1999, the block consisted of three replicates of ÔGolden DeliciousÕ and three replicates of ÔFugiÕ for each treatment. In 2000, three replicates of ÔGolden DeliciousÕ, three replicates of ÔFugiÕ, and three replicates of ÔGranny SmithÕ were used for each treatment. Treatments were similar in 1999 and 2000. There were slight differences in the rates and timing of prohexadione-calcium (Apogee) applications between years. The treatments were as follows: two treatments with three applications of prohexadionecalcium starting out at a high rate (0.13 and 0.26 g [AI]/liter in 1999 and 2000, respectively) and progressing to a lower rate (0.08 and 0.07 g [AI]/liter in 1999 and 2000, respectively) with and without the insecticides imidacloprid (0.06 g [AI]/liter) to control aphids (2000 only) and/or tebufenozide (0.34 g [AI]/ liter) to control lepidopteran pests (1999 and 2000), two treatments with three applications of a single rate of prohexadione-calcium (0.13 g [AI]/liter) with and without imidacloprid and tebufenozide, imidacloprid (2000 only) and tebufenozide without the use of prohexadione-calcium, and the untreated control. LI-700 was added at 0.94 ml/liter water, and ammonium sulfate was added at an equal weight to the prohexadione-calcium rate in each treatment. Latron B-1956 was added at 0.125 ml/liter water in the tebufenozide treatments as a spreader/sticker. Trees were planted in 6 by 9-m spacing and were 7 yr old at the start of this study. Prohexadione-calcium treatments were applied to runoff with a handgun from a truck-mounted hydraulic sprayer at 28.0 kg/ cm2. An average spray volume of 11.4 liters was applied per tree. Insecticide treatments were applied with a Durand-Wayland airblast sprayer calibrated to deliver

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935 liters/ha at 3.9 km/h. A routine schedule of fungicides was maintained throughout the duration of the study (Anonymous 2000 Ð2001). Treatment effects on shoot growth were assessed by randomly choosing 10 actively growing shoots, tagging them, and measuring shoot length at 2-wk intervals from May to August. Treatment effects on obliquebanded leafroller were evaluated by counting the number of previously undiscovered leaf shelters during a 12-min search per tree at weekly intervals from mid-June to August. Leaf shelters were ßagged at discovery to determine whether shelter location and movement of obliquebanded leafroller larvae was affected by treatments. The location of each shelter in old versus new (bud and Þrst four full sized leaves) vegetation was noted, and shelters were examined to determine whether they contained living obliquebanded leafroller larvae. Fruit damage was assessed on 8 August 1999 and 7 September 2000 by counting all of the fruit on each tree and removing damaged fruit for further examination. In the laboratory, damaged fruit were evaluated to determine the cause of damage and percentage of fruit damaged by obliquebanded leafroller. Shoots also were inspected to determine treatment effects on both spirea aphid and aphid natural enemy densities. Spirea aphid populations were evaluated by choosing 10 growing shoots from the east side of each tree and counting the number of spirea aphid-infested leaves per terminal. The number of spirea aphid on the most heavily infested leaf was categorized as follows: 0, no spirea aphids; 1, 1Ð20 spirea aphids; 2, 21Ð100 spirea aphids; 3, 101Ð200 spirea aphids; and 4, ⱖ200 spirea aphids. The number of aphid natural enemies was estimated by counting the number observed in a 3-min examination around the periphery of each plot tree. Data were collected on 30 June 1999 and biweekly from May to July in 2000. Two-way analysis of variance (ANOVA) was carried out on the following dependent variables: shoot length, cumulative number of obliquebanded leafroller shelters per tree, proportion of leafroller shelters on new vegetation (versus old), proportion of leafroller shelters that were empty (versus occupied), proportion of fruit damaged by leafroller, number of infested leaves per shoot, and the number of spirea aphids on the most infested leaf per shoot. Independent variables were treatment and cultivar. FisherÕs protected least signiÞcant difference (LSD) test also was performed on each dependent variable and the arcsine transformation of all variables except number of leafroller shelters and shoot length (SuperANOVA 1989). SigniÞcance level was set at P ⱕ 0.05. Pear. In 1999, four treatments were applied to single-tree plots in a randomized complete block design consisting of four replicates of ÔBartlettÕ for each treatment. Trees were planted on a 7 by 7-m spacing and were 21 yr old. Treatments were applied to runoff with a handgun from a truck-mounted hydraulic sprayer at 28.0 kg/cm2. An average spray volume of 11.4 liters was applied per tree. The experiment consisted of four treatments: three applications each of prohexadione-

April 2005 Table 1.

PAULSON ET AL.: EFFECT OF PROHEXADIONE-CALCIUM ON PEAR AND APPLE PESTS

425

Mean (ⴞSE) growth of apple shoots treated with different prohexadione-calcium programs in 1999

Treatment

Rate(g 关AI兴/liter)

Application date

Prohexadione-calcium

0.13 0.08 0.13 0.13 0.08 0.34 0.13 0.34 0.34

14 May 26 May, 8 June 14 and 26 May, 8 June 14 May 26 May, 8 June 1 July 14 and 26 May, 8 June 1 July 1 July

Prohexadione-calcium Prohexadione-calcium Tebufenozide Prohexadione-calcium Tebufenozide Tebufenozide Control

Mean shoot length (cm) 18 May

23 June

21 July

20.7 ⫾ 0.0b

26.5 ⫾ 0.8a

27.0 ⫾ 0.7a

19.4 ⫾ 0.4a 20.5 ⫾ 0.4ab

25.8 ⫾ 0.5a 27.5 ⫾ 0.2a

27.3 ⫾ 0.7a 27.9 ⫾ 0.7a

21.0 ⫾ 0.4b

26.3 ⫾ 0.8a

27.8 ⫾ 0.7a

20.9 ⫾ 0.4b 20.1 ⫾ 0.5ab

32.2 ⫾ 1.1b 32.8 ⫾ 1.20b

34.8 ⫾ 1.1b 32.9 ⫾ 1.3b

Means in columns followed by the same letter are not signiÞcantly different (P ⱕ 0.05; FisherÕs protected LSD).

calcium (one application at 0.21 g [AI]/liter and two at 0.06 g [AI]/liter) and the insecticide imidacloprid (0.08 g [AI]/liter), three applications each of a single rate of prohexadione-calcium (0.12 g [AI]/liter) and imidacloprid (0.08 g [AI]/liter), three applications of imidacloprid (0.08 g [AI]/liter), and an untreated control. All trees received a regular fungicide maintenance schedule (Anonymous 2000 Ð2001). LI-700 was added at 0.94 ml/liter water, and ammonium sulfate was added at an equal weight to the prohexadione-calcium rate in each treatment. Treatment effects on shoot growth were assessed by measuring shoot growth through the course of the season. Ten actively growing pear shoots were tagged and measured periodically throughout the study to determine the effect of prohexadione-calcium on shoot growth. Treatment effects in pear were evaluated by estimating pear psylla nymph and adult densities. Nymphs were counted from leaf samples by using a binocular microscope under 10⫻ magniÞcation at 6 Ð9-d intervals. Counts were made on samples of 15 spur leaves on 13 May, on seven spur and eight third-most distal leaf samples on 24 May, and on 15 third-most distal leaf samples from 1 to 24 June. The cumulative number of pear psylla nymph days (CPPND) per leaf was calculated for each treatment from 13 May to 24 June by using the formula CPPND ⫽ ⌺ 0.5(Pa ⫹ Pb)Da ⫺ b, where Pa is the population density (mean pear psylla nymphs per leaf) at time a, Pb is the population density at time b, and Da ⫺b is the number of days between time a and time b. Adult pear psylla were sampled by making a 2-min observation around the periphery of each tree. Twoway ANOVA and FisherÕs protected LSD test was performed on pear psylla nymphs per leaf, cumulative pear psylla nymphs, pear psylla adults per 2 min-count, and shoot length. SigniÞcance level was set at P ⬍ 0.05 (SuperANOVA 1989). Results and Discussion Apple Shoot Growth. In both 1999 (18 May: F ⫽ 1.86; df ⫽ 1, 348; P ⫽ 0.100; 23 June: F ⫽ 2.62; df ⫽ 1, 348; P ⫽ 0.094; 21 July: F ⫽ 2.32; df ⫽ 1, 348; P ⫽ 0.230) and 2000 (27 March: F ⫽ 0.85; df ⫽ 2, 522; P ⫽ 0.358; 11 May: F ⫽ 8.89; df ⫽ 2, 522; P ⫽ 0.060; 7 June: F ⫽

1.19; df ⫽ 2, 522; P ⫽ 0.275; 7 July: F ⫽ 1.65; df ⫽ 2, 522; P ⫽ 0.200; 2 August: F ⫽ 1.77; df ⫽ 2, 522; P ⫽ 0.184), cultivar did not signiÞcantly affect shoot growth. Data from 1999 (Table 1) (18 May: F ⫽ 2.45; df ⫽ 5, 354; P ⫽ 0.047; 23 June: F ⫽ 12.92; df ⫽ 5, 354; P ⫽ 0.024; 21 July: F ⫽ 23.16; df ⫽ 5, 354; P ⫽ 0.001) and 2000 (Table 2) (27 March: F ⫽ 2.02; df ⫽ 5, 534; P ⫽ 0.041; 11 May: F ⫽ 25.52; df ⫽ 5, 534; P ⫽ 0.001; 7 June: F ⫽ 53.91; df ⫽ 5, 534; P ⫽ 0.001; 7 July: F ⫽ 87.45; df ⫽ 5, 534; P ⫽ 0.001; 2 August: F ⫽ 77.78; df ⫽ 5, 534; P ⫽ 0.001) indicated that prohexadione-calcium signiÞcantly reduced shoot growth in apples. The greatest differences in shoot growth were seen in 2000 when prohexadionecalcium was applied earlier in the growing season than it was in 1999 (April versus May). In 2000, trees not treated with prohexadione-calcium had shoots that were about twice the length of those from prohexadione-calcium-treated trees. In 2000, there also were signiÞcant differences in late summer shoot growth between the prohexadione-calcium treatments. The two treatments with the high-low rates of prohexadione-calcium had signiÞcantly longer shoots than the two treatments with prohexadione-calcium at a single rate. This is probably because the single-rate prohexadione-calcium treatments had higher rates applied in late May and early June than did the high-low prohexadione-calcium treatments. Obliquebanded Leafroller. Apple cultivar did not have a signiÞcant effect on the data in 1999 (shelters per tree: F ⫽ 0.54; df ⫽ 1, 34; P ⫽ 0.466; % fruit injury: F ⫽ 2.29; df ⫽ 1, 34; P ⫽ 0.14; % shelters in new vegetation: F ⫽ 0.02; df ⫽ 1, 34; P ⫽ 0.88; % empty shelters: F ⫽ 0.93; df ⫽ 1, 34; P ⫽ 0.34) or 2000 (shelters per tree: F ⫽ 0.10; df ⫽ 2, 51; P ⫽ 0.271; % fruit injury: F ⫽ 1.011; df ⫽ 2, 51; P ⫽ 0.453; % shelters in new vegetation: F ⫽ 0.90; df ⫽ 2, 51; P ⫽ 0.350; % empty shelters: F ⫽ 2.09; df ⫽ 2, 51; P ⫽ 0.133). Trees treated with both prohexadione-calcium and tebufenozide had signiÞcantly lower numbers of obliquebanded leafroller shelters (F ⫽ 6.08; df ⫽ 5, 30; P ⫽ 0.01) than other treatments (Table 3). Treatments in which only prohexadione-calcium or tebufenozide was applied also had signiÞcantly lower numbers of obliquebanded leafroller shelters per tree than the untreated control but were not signiÞcantly different from each other. These results were mirrored in the fruit damage

37.1 ⫾ 1.8c 34.3 ⫾ 1.6a

Imidacloprid Tebufenozide Prohexadione-calcium Imidacloprid Tebufenozide Imidacloprid Tebufenozide Control

Prohexadione-calcium Prohexadione-calcium

0.26 0.13 0.07 0.13 0.26 0.13 0.07 0.06 0.34 0.13 0.06 0.34 0.06 0.34

Means in columns followed by the same letter are not signiÞcantly different (P ⱕ 0.05; FisherÕs protected LSD).

16.6 ⫾ 0.8c 5.1 ⫾ 0.3ab

24.2 ⫾ 1.0b

33.9 ⫾ 1.9c 31.7 ⫾ 1.6a 16.7 ⫾ 0.8c 4.5 ⫾ 0.4a

23.6 ⫾ 1.1b

14.4 ⫾ 0.7a 13.9 ⫾ 0.6a 12.9 ⫾ 0.5a 10.3 ⫾ 0.5ab 5.4 ⫾ 0.5ab

14.7 ⫾ 0.6a 17.3 ⫾ 0.9b 13.8 ⫾ 0.5a 15.3 ⫾ 0.5a 9.5 ⫾ 0.5a 11.3 ⫾ 0.5b 4.7 ⫾ 0.4a 5.3 ⫾ 0.4ab

12.8 ⫾ 0.5a 13.5 ⫾ 0.5a

15.1 ⫾ 0.6a

5 July 7 June

11.3 ⫾ 0.6b 5.5 ⫾ 0.4b

Mean shoot length (cm)


24 April 8 May 26 May, 12 June 24 April, 8 and 26 May, 12 June 24 April 8 May 26 May, 12 June 27 June 14 July 24 April, 8 and 26 May, 12 June 27 June 14 July 27 June 14 July

11 May 27 Mar. Application date Rate (g [AI]/liter) Treatment

Mean (ⴞSE) growth of apple shoots treated with different prohexadione-calcium programs in 2000 Table 2.

13.6 ⫾ 0.6a

2 Aug.

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assessments with the least fruit damage occurring in trees treated with both prohexadione-calcium and tebufenozide (F ⫽ 2.48; df ⫽ 5, 30; P ⫽ 0.04). Treatments did not signiÞcantly effect the location of shelters in new versus old vegetation (F ⫽ 2.88; df ⫽ 5, 30; P ⫽ 0.31) or the proportion of empty versus occupied shelters (F ⫽ 6.26; df ⫽ 5, 30; P ⫽ 0.25). In 2000, obliquebanded leafroller infestations were very low, and no signiÞcant differences were found for any variables (shelters per tree: F ⫽ 5.85; df ⫽ 5, 48; P ⫽ 0.480; % fruit injury: F ⫽ 1.66; df ⫽ 5, 48; P ⫽ 0.880; % shelters in new vegetation: F ⫽ 1.36; df ⫽ 5, 48; P ⫽ 0.302; % empty shelters: F ⫽ 1.80; df ⫽ 5, 48; P ⫽ 0.347). It is unclear why prohexadione-calcium applications without the use of pesticides resulted in lower obliquebanded leafroller population levels, but it is probably due to changes in host suitability for neonate obliquebanded leafroller larvae due to reduced terminal growth. One concern regarding the use of prohexadione-calcium was the possibility that it might alter the behavior of obliquebanded leafroller larvae causing them to be more active or to favor new versus old vegetation. Our data indicated that this was not the case. Obliquebanded leafroller larvae in prohexadione-calcium-treated trees did not abandon shelters at a greater rate than in nontreated trees nor did they show increased preference for new (terminal) growth. This is especially important because movement of obliquebanded leafroller larvae to terminal foliage can reduce the efÞcacy of some pesticides (Waldstein and Reissig 2001), and there is a positive relationship between fruit damage and the number of shelters in a tree (our unpublished data). Lawson et al. (1998) found that summer pruning reduced obliquebanded leafroller damage in a commercial apple orchard in New York. This was possibly due to increasing the efÞcacy of pesticides by improving canopy penetration and coverage during application. In our study, prohexadione-calcium may have increased the efÞcacy of tebufenozide in a similar manner, which may explain why the lowest obliquebanded leafroller populations were found on trees treated with both compounds. This study indicates that prohexadione-calcium may play an important role in obliquebanded leafroller management by increasing the efÞcacy of pesticides. Spirea Aphid. Apple cultivar did not have a significant effect on the data in 1999 (infested leaves per terminal [ILT]: F ⫽ 1.91; df ⫽ 1, 348; P ⫽ 0.244; number of aphids on most infested leaf [AIL]: F ⫽ 1.17; df ⫽ 1, 348; P ⫽ 0.82) or 2000 (ILT-26 June: F ⫽ 2.35; df ⫽ 2, 522; P ⫽ 0.096; 5 July: F ⫽ 5.86; df ⫽ 2, 522; P ⫽ 0.060; 27 July: F ⫽ 5.23; df ⫽ 2, 522; P ⫽ 0.060; AIL-26 June: F ⫽ 4.49; df ⫽ 2, 522; P ⫽ 0.076; 5 July: F ⫽ 1.72; df ⫽ 2, 522; P ⫽ 0.181; 27 July: F ⫽ 2.94; df ⫽ 2, 522; P ⫽ 0.062). On 30 June 1999, the only spirea aphid sampling date of 1999, prohexadione-calcium-treated trees had signiÞcantly fewer infested leaves per terminal (F ⫽ 21.46; df ⫽ 5, 354; P ⬍ 0.001) and fewer spirea aphids on the infested leaves (F ⫽ 20.28; df ⫽ 5, 354; P ⬍ 0.001) than nonprohexadione-calciumtreated trees (Table 4). There were similar results in

Imidacloprid Tebufenozide Prohexadione-calcium Imidacloprid Tebufenozide Imidacloprid Tebufenozide Imidacloprid Tebufenozide Control


Tebufenozide Prohexadione-calcium Tebufenozide Tebufenozide Control Prohexadione-calcium

0.26 0.13 0.07 0.13 0.26 0.13 0.07 0.06 0.34 0.13 0.06 0.34 0.06 0.34 0.06 0.34

0.13 0.08 0.13 0.13 0.08 0.34 0.13 0.34 0.34

Rate (g [AI]/liter)

24 April 8 May 26 May, 12 June 24 April, 8 and 26 May, 12 June 24 April 8 May 26 May, 12 June 27 June 14 July 24 April, 8 and 26 May, 12 June 27 June 14 July 27 June 14 July 27 June 14 July


Application date

0.0 ⫾ 0.0a 0.0 ⫾ 0.0a 0.0 ⫾ 0.0a 0.0 ⫾ 0.0a

5.8 ⫾ 3.4a 5.8 ⫾ 3.4a 3.1 ⫾ 0.7a

0.0 ⫾ 0.0a 0.0 ⫾ 0.0a

4.3 ⫾ 1.1a 6.7 ⫾ 4.3a

1.1 ⫾ 0.4a

1.1 ⫾ 0.3b 2.6 ⫾ 0.6c 0.0 ⫾ 0.0a

12.2 ⫾ 4.3b 37.7 ⫾ 10.3c 1.7 ⫾ 0.8a

1.2 ⫾ 0.5b 0.5 ⫾ 0.3a

13.8 ⫾ 2.2b 6.8 ⫾ 2.7a 0.4 ⫾ 0.2a

1.0 ⫾ 0.3b

12.7 ⫾ 2.4b

3.5 ⫾ 0.4a

% fruit injury

Shelters/tree

Means in columns followed by the same letter were not signiÞcantly different (P ⱕ 0.05; FisherÕs protected LSD).

2000


1999


Treatment

Effect of prohexadione-calcium applications to apple trees on obliquebanded leafroller larval populations

Year

Table 3.

19.4 ⫾ 10.4ns

0.0 ⫾ 0.0ns

0.0 ⫾ 0.0ns

20.0 ⫾ 20.0ns

39.9 ⫾ 12.8ns 3.8 ⫾ 2.6ns

37.5 ⫾ 12.8ns 27.6 ⫾ 4.7ns 0.00 ⫾ 0.0ns

55.2 ⫾ 18.7ns

21.0 ⫾ 5.3ns 44.0 ⫾ 10.2ns

47.7 ⫾ 7.4ns

% shelters in new vegetation

Mean ⫾ SE

43.1 ⫾ 12.5ns

0.0 ⫾ 0.0ns

0.0 ⫾ 0.0ns

16.7 ⫾ 10.5ns

17.9 ⫾ 9.3ns 20.6 ⫾ 13.9ns

68.1 ⫾ 7.9ns 72.4 ⫾ 7.0ns 38.1 ⫾ 32.7ns

57.7 ⫾ 8.1ns

42.9 ⫾ 9.0ns 47.8 ⫾ 11.5ns

58.4 ⫾ 6.0ns

% empty shelters

April 2005 PAULSON ET AL.: EFFECT OF PROHEXADIONE-CALCIUM ON PEAR AND APPLE PESTS 427

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Table 4.

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Effect of prohexadione-calcium applications to apple trees on spirea aphid populations in 1999

Treatment

Prohexadione-calcium Prohexadione-calcium Prohexadione-calcium Tebufenozide Prohexadione-calcium Tebufenozide Tebufenozide Control

Mean ⫾ SE

Rate (g 关AI兴/liter)

Application date

0.13 0.08 0.13 0.13 0.08 0.34 0.13 0.34 0.34


No. aphid infested leaves/terminal

No. aphids on the most infested leaf a

30 June 0.3 ⫾ 0.1a

30 June 0.2 ⫾ 0.1a

0.2 ⫾ 0.1a 1.1 ⫾ 0.3b

0.2 ⫾ 0.1a 0.5 ⫾ 0.1b

0.1 ⫾ 0.0a

0.1 ⫾ 0.0a

1.6 ⫾ 0.2c 2.0 ⫾ 0.3c

0.7 ⫾ 0.1c 0.9 ⫾ 0.1d

Means in columns followed by the same letter were not signiÞcantly different (P ⱕ 0.01; FisherÕs protected LSD). Categories for aphids/most infested leaf include 0, no aphids; 1, 1Ð20 aphids; 2, 21Ð100 aphids; 3, 101Ð200 aphids; and 4, ⬎200 aphids.

a

2000 except that imidacloprid was incorporated into the experimental design (Table 5). Prohexadione-calcium signiÞcantly reduced spirea aphid infestations compared with nonprohexadione-calcium-treated trees before the application of imidacloprid on 27 June 2000 (ILT-26 June: F ⫽ 9.12; df ⫽ 5, 534; P ⬍ 0.001; AIL: F ⫽ 6.35; df ⫽ 5, 534; P ⬍ 0.001). After that date, treatments that included imidacloprid had spirea aphid populations that were signiÞcantly lower than all other treatments but were not signiÞcantly different from each other and treatments with prohexadione-calcium that did not include imidacloprid had signiÞcantly lower spirea aphid populations than the control on 5 July 2000 (ILT-5 July: F ⫽ 87.64; df ⫽ 5, 534; P ⬍ 0.001; AIL: F ⫽ 93.64; df ⫽ 5, 534; P ⬍ 0.001). Aphid populations in different treatments were no longer signiÞcantly different from each other after an abrupt population decline in late July across all treatments (ILT-27 July: F ⫽ 1.66; df ⫽ 5, 534; P ⫽ 0.142; AIL: F ⫽ 1.55; df ⫽ 5, 534; P ⫽ 0.172) ostensibly due to the natural hardening off of shoot growth at this time of the season and probably due to the presence of large numbers of Campylomma verbasci (Meyer), which were not effected by prohexadione-calcium or imidacloprid treatments (our unpublished data). C. verbasci has been reported as a generalist predator of pear psylla, mites, and aphids (McMullen and Jong 1970, Beers et al. 1993), and we have seen relatively high populations of this predator feeding on spirea aphid populations in recent years. It seems that prohexadione-calcium can contribute to the control of spirea aphid by keeping population densities low early in the growing season. In years with low spirea aphid pressure, prohexadione-calcium alone may sufÞciently limit spirea aphid population growth until populations of natural enemies build to a level at which they are capable of controlling spirea aphid. Pear Shoot Growth. Shoot length was signiÞcantly shorter on prohexadione-calcium-treated trees than nonprohexadione-calcium-treated trees (Table 6) (20 May: F ⫽ 3.25; df ⫽ 3, 156; P ⫽ 0.024; 28 May: F ⫽ 6.65; df ⫽ 3, 156; P ⬍ 0.001; 10 June: F ⫽ 8.73; df ⫽ 3, 156; P ⬍ 0.001; 9 July: F ⫽ 11.22; df ⫽ 3, 156; P ⬍ 0.001) with the exception of 23 June 1999 on which shoot

growth in prohexadione-calcium-treated trees was not signiÞcantly different from shoot growth in the control trees but was signiÞcantly different from shoot growth in the other nonprohexadione-calcium treatment (F ⫽ 10.42; df ⫽ 3,156; P ⫽ 0.001). It is unclear why this relationship developed. Our data indicates that prohexadione-calcium can signiÞcantly control shoot growth in pears, but it does not have as persistent an effect on pears as it does on apples in which shoot growth was controlled the entire season. Pear Psylla. The number of pear psylla nymphs was not signiÞcantly different across all sprayed treatments until 7 June 1999 when the number of nymphs on the control trees had markedly increased (Table 7) (13 May: F ⫽ 0.34; df ⫽ 3, 236; P ⫽ 0.86; 1 June: F ⫽ 0.54; df ⫽ 3, 236; P ⫽ 0.65; 7 June: F ⫽ 1.15; df ⫽ 3, 236; P ⫽ 0.43; 16 June: F ⫽ 3.18; df ⫽ 3, 236; P ⫽ 0.023; 24 June: F ⫽ 3.25; df ⫽ 3, 236; P ⫽ 0.019). Nymph populations on the two prohexadione-calcium/imidacloprid treatments continued to remain low throughout June, whereas the number of nymphs increased on the imidacloprid only treatment. The number of cumulative pear psylla nymph days per leaf was the lowest on the high rate treatment of prohexadione-calcium and imidacloprid followed by low rate of the same two chemicals (F ⫽ 12.67; df ⫽ 3, 236; P ⫽ 0.05). A similar trend in treatment response for pear psylla adults was found on 7 June (F ⫽ 9.78; df ⫽ 3,12; P ⫽ 0.005); otherwise, no signiÞcant differences in adult populations were found during the study (13 May: F ⫽ 1.62; df ⫽ 3, 12; P ⫽ 0.23; 1 June: F ⫽ 1.23; df ⫽ 3 12; P ⫽ 0.28; 16 June: F ⫽ 1.93; df ⫽ 3, 12; P ⫽ 0.16; 24 June: F ⫽ 2.54; df ⫽ 3, 12; P ⫽ 0.11). Treatments with both prohexadione-calcium and imidacloprid had signiÞcantly lower pear psylla nymph populations than those found in the imidacloprid only trees. Pear psylla nymphal populations continued to increase after the application of imidacloprid in the absence of prohexadione-calcium but dropped in the imidacloprid with prohexadione-calcium treatments. As in apples, prohexadione-calcium may allow for better canopy penetration and coverage by pesticides, resulting in more effective control of pear psylla. Because prohexadione-calcium did not affect the

0.26 0.13 0.07 0.13 0.26 0.13 0.07 0.06 0.34 0.13 0.06 0.34 0.06 0.34

24 April 8 May 26 May, 12 June 24 April, 8 and 26 May, 12 June 24 April 8 May 26 May, 12 June 27 June 14 July 24 April, 8 and 26 May, 12 June 27 June 14 July 27 June 14 July

Application date

0.03 ⫾ 0.02a 0.12 ⫾ 0.02a 3.77 ⫾ 0.19d

3.23 ⫾ 0.17b 3.14 ⫾ 0.18b

1.89 ⫾ 0.15b 0.10 ⫾ 0.03a

1.86 ⫾ 0.15a 1.96 ⫾ 0.13a

2.20 ⫾ 0.37a

5 July 2.39 ⫾ 0.14c

26 June 2.02 ⫾ 0.14a

0.17 ⫾ 0.05ns

0.06 ⫾ 0.02ns

0.04 ⫾ 0.02ns

0.19 ⫾ 0.08ns 0.10 ⫾ 0.05ns


1999

0.21 0.06 0.08 0.12 0.08 0.08

Rate (g [AI]/liter) 11 May 25 May, 7 June 11 May, 3 and 14 June 11 and 25 May, 7 June 11 May, 3 and 14 June 11 May, 3 and 14 June

Application date

18.3 ⫾ 1.5a 26.6 ⫾ 1.6b 24.3 ⫾ 1.3b

21.6 ⫾ 1.0b 21.0 ⫾ 1.5b

20.1 ⫾ 1.0a

17.6 ⫾ 1.0a 17.0 ⫾ 1.3a

28 May

20 May

Means in columns followed by the same letter were not signiÞcantly different (P ⱕ 0.05; FisherÕs protected LSD.).

Imidacloprid Prohexadione-calcium Imidacloprid Imidacloprid Control

Treatment

Growth of pear shoots (mean ⴞ SE) treated with different prohexadione-calcium programs

Year

Table 6.

a

31.3 ⫾ 2.6b 29.4 ⫾ 2.5b

20.1 ⫾ 1.4a

21.2 ⫾ 0.7a

10 June

Mean shoot length (cm)

1.73 ⫾ 0.09b

1.69 ⫾ 0.08b

1.17 ⫾ 0.27a

1.06 ⫾ 0.07a 1.20 ⫾ 0.05a

34.5 ⫾ 2.2b 29.4 ⫾ 3.9ab

21.6 ⫾ 1.6a

22.3 ⫾ 0.6a

23 June

2.26 ⫾ 0.10c

0.17 ⫾ 0.05a

0.03 ⫾ 0.02a

1.47 ⫾ 0.09b 0.18 ⫾ 0.06a

5 July 1.53 ⫾ 0.06b

35.6 ⫾ 1.9b 29.4 ⫾ 3.6b

21.5 ⫾ 3.2a

21.8 ⫾ 1.3a

9 July

0.13 ⫾ 0.04ns

0.06 ⫾ 0.02ns

0.04 ⫾ 0.02ns

0.14 ⫾ 0.05ns 0.08 ⫾ 0.03ns

27 July 0.07 ⫾ 0.03ns

No. aphids on the most infested leafa 26 June 1.23 ⫾ 0.08a

Mean ⫾ SE 27 July 0.06 ⫾ 0.03ns

No. aphid infested leaves/terminal

Means in columns followed by the same letter were not signiÞcantly different (P ⱕ 0.05; FisherÕs protected LSD). Categories for aphids/most infested leaf include 0, no aphids; 1, 1Ð20 aphids; 2, 21Ð100 aphids; 3, 101Ð200 aphids; and 4, ⬎200 aphids.

Imidacloprid Tebufenozide Prohexadione-calcium Imidacloprid Tebufenozide Imidacloprid Tebufenozide Control



Rate (g [AI]/liter)

Effect of prohexadione-calcium applications to apple trees on spirea aphid populations in 2000

Treatment

Table 5.

April 2005 PAULSON ET AL.: EFFECT OF PROHEXADIONE-CALCIUM ON PEAR AND APPLE PESTS 429

17.8 ⫾ 9.0ns 9.3 ⫾ 7.0ns 15.3 ⫾ 7.8ns 22.5 ⫾ 4.6ns


Means in columns followed by the same letter were not signiÞcantly different (P ⱕ 0.05; FisherÕs protected LSD). Adult data was collected on 28 May. a

281.3 ⫾ 46.9ns 267.5 ⫾ 37.8ns 124.3 ⫾ 40.3ns 189.3 ⫾ 22.0ns

213.0 ⫾ 33.63b 226.0 ⫾ 54.6b

11.5 ⫾ 4.1ns 7.5 ⫾ 2.2ns 85.3 ⫾ 6.3a 182.3 ⫾ 31.3ns 105.8 ⫾ 27.6ns

5.3 ⫾ 2.8ns 9.0 ⫾ 1.5ns 183.0 ⫾ 9.1ns 122.8 ⫾ 27.8ns

11 May 25 May, 7 June 11 May, 3 and 14 June 11 and 25 May, 7 June 11 May, 3 and 14 June 11 May, 3 and 14 June 0.21 0.06 0.08 0.12 0.08 0.08 Prohexadione-calcium 1999



Pear psylla adults/2 min 63.3 ⫾ 9.0a

9.0 ⫾ 2.3b 7.6 ⫾ 2.2b 6.7 ⫾ 2.7b 9.9 ⫾ 2.85b 1.2 ⫾ 0.3ns 1.5 ⫾ 0.4ns 1.1 ⫾ 0.5ns 3.1 ⫾ 0.6ns

4.0 ⫾ 0.9a 18.1 ⫾ 1.8b

2.1 ⫾ 0.2a 1.5 ⫾ 0.6a 2.5 ⫾ 0.9a 0.8 ⫾ 0.1ns 1.4 ⫾ 0.5ns

1.4 ⫾ 0.5a

16 June 7 June

0.7 ⫾ 0.3ns 0.7 ⫾ 0.3ns

Pear psylla nymphs/leaf

1999

0.21 0.06 0.08 0.12 0.08 0.08

11 May 25 May, 7 June 11 May, 3 and 14 June 11 and 25 May, 7 June 11 May, 3 and 14 June 11 May, 3 and 14 June

1 June 13 Maya Application date Rate (g [AI]/liter) Treatment Year

Effect of prohexadione-calcium applications to pear trees on pear psylla populations Table 7.

3.1 ⫾ 1.4a

24 June

JOURNAL OF ECONOMIC ENTOMOLOGY 1.7 ⫾ 0.7a

430

Vol. 98, no. 2

number of pear psylla adults found in the trees, we assume that observed differences in pear psylla nymph populations were due to the effects of pesticides and not to differential oviposition by adults, especially because pear psylla nymph populations in the imidacloprid treatments were not signiÞcantly different before insecticide application. In 2001, one year after its initial registration during spring 2000, prohexadione-calcium was applied an average of 1.4 times to ⬎4,047 hectares of apples in the four major fruit-growing states of the United States (National Agricultural Statistics Service 2002). Although this accounts for only 3% of the total U.S. apple acreage, the general use of this product is expected to increase substantially in the future because of the productÕs ability to modify the host plant (i.e., reduced shoot growth equals less pruning and lower labor costs for the orchardists). Despite the commercial use of prohexadione-calcium in apple orchards since its introduction, little research has been published about its effects in reducing pest populations in deciduous tree fruits, and all of these are in the form of nonrefereed publications or Þeld research reports. Two such reports substantiate our Þndings that prohexadione-calcium reduces spirea aphid populations (Walgenbach and Palmer 1999, Krawczyk and Greene 2001), even without the addition of aphidicides. Two more studies report similar reductions of leafroller populations and fruit injury in trials by using prohexadione-calcium alone or in synergy with an insecticide (Krawczyk and Greene 2001, Wise and Gut 2001). Wise and Gut (2001) indicated signiÞcant short-term mortality to C. rosaceana larvae from prohexadione-calcium, but it was tested only in combination with ammonium sulfate, which also may have had some effect on C. rosaceana. Leahy et al. (2002) also found signiÞcant reductions in potato leafhopper, Empoasca fabae (Harris), injury on apple treated with prohexadionecalcium alone or in combination with imidacloprid. A reduction in the populations of several types of apple and pear pests with prohexadione-calcium is of signiÞcance to growers and should be incorporated into existing insect pest management programs to improve the performance of current control measures and to help slow the development of insecticide resistance in key pests such as the pear psylla. Currently, we do not fully understand why prohexadione-calcium inhibits pest populations other than reducing the rate of shoot development and making the shoot less attractive for developing pest populations. We measured reductions in shoot growth with prohexadione-calcium in both apple and pear and found reduction in some pest populations and increases in pesticide efÞcacy, but we did not measure the nitrogen content of prohexadione-calcium treated shoots. Nitrogen levels in apple and pear are known to affect development and reproduction in both A. pomi (Hukusima and Ando 1967, Takeda et al. 1967) and P. pyricola (Hodkinson 1974), and high levels of nitrogen promote both succulent shoot growth and increased aphid and psylla populations (Pfeiffer and Burts 1983, 1984; Brown and Welker 1992). Behavioral

April 2005

PAULSON ET AL.: EFFECT OF PROHEXADIONE-CALCIUM ON PEAR AND APPLE PESTS

studies to determine changes in host plant suitability, palatability, or detection in some of these pest species are necessary to understand and possibly enhance these effects for pest control. Acknowledgments We thank David Zapotak, Jeanette Armour, and Marco Marisic for assistance with this project. This projected was funded in part by a Shippensburg University Professional Development Grant.

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