MANAGEMENT AND CONTROL OF INSECTICIDE- RESISTANT PEAR PSYLLA (Cacopsylla pyri)

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Journal of Fruit and Ornamental Plant Research Vol. 14 (Suppl. 3), 2006 MANAGEMENT AND CONTROL OF INSECTICIDE- RESISTANT PEAR PSYLLA (Cacopsylla pyri) F r a n t i še k K o c o u r e k a n d J i t k a S t a r á Research Institute of Crop Production, Drnovská 507 Praha 16106, CZECH REPUBLIC e-mail: kocourek@vurv.cz (Received November 7, 2005/Accepted November 28, 2005) A B S T R A C T The efficacy of different insecticides on adults and nymphs of Cacopsylla pyri from two localities in the Czech Republic was evaluated in biological tests. Resistance of C. pyri populations originated from an orchard intensively treated by: Nomolt 15 SC (teflubenzuron), Dimilin 48 SC (diflubenzuron), Zolone 35 EC (phosalone) and Trebon 30 EC (etofenprox) was proved in the laboratory tests. Population of C. pyri from an untreated locality was susceptible to the all tested insecticides. The highest efficacy on C. pyri nymphs was shown in tests in net slives when Calypso 480 SC (thiacloprid) and Vertimec 1.8 EC (abamectin) were applied. The efficacy of the tested insecticides against C. pyri adults in tarsal test was sufficient except of Cascade 5 EC (flufenoxuron) and Zolone 35 EC, when the C. pyri population from the chemically treated orchard was tested. The level of resistance of nymphs to phosalone was much higher than in adults of the overwintering generation. The efficacy of Sanmite 20 WP (pyridaben) and Calypso 480 SC on new hatched nymphs of C. pyri showing multiple resistance in field experiments in two different localities was excellent. On the basis of results, Sanmite 20 WP, Calypso 480 SC and Cascade 5 EC were recommended for antiresistant strategy against C. pyri. Sanmite 20 WP was recommended for the registration in the Czech Republic against C. pyri in pear orchards. Key words: Cacopsylla pyri, pear psylla, resistance, antiresistant strategies INTRODUCT ION Psyllids are among the most serious pests in pear orchards, which have been intensively treated with pesticides. The species, which causes the most damage in central Europe, is Cacopsylla pyri. In the Czech Republic, C. pyri has caused economically important damage since the 1990s. The main agents used to control psyllids in pear orchards are non-selective insecticides and pyrethroids.

F. Kocourek and J. Stará Consequently, chemical control against psyllids has become ineffective in many parts of the country because of the selection of populations resistant to organophosphates and pyrethroids. Psyllids easily develop resistance to insecticides. Insecticide-resistant populations of C. pyricola were detected in the 1960s (Harries and Burts, 1965). Since the mid 1980s, populations of C. pyricola in North America and C. pyri in Europe were found to be resistant to a broad spectrum of insecticides (Berrada et al., 1995). At the beginning of the 1990s, Nomolt 15 SC was approved for use against psyllids in pear orchards in the Czech Republic. Nomolt was highly effective against psyllids and was used in combination with other selective insecticides to ensure effective pest control in pear orchards. In 2003, Nomolt failed to control psyllids in several localities at ones. It was suspected that C. pyri developed resistance to Nomolt after ten years of repeated exposure. The aims of this study were to evaluate C. pyri populations from treated and untreated orchards in terms of their resistance to insecticides with different modes of action and to determine which insecticides might be useful in controlling insecticide-resistant C. pyri populations on the basis of laboratory and field trials. MATERIAL AND M ETHODS Four experiments were carried out. In the first experiment, mean fertility was evaluated in two C. pyri populations. The first population was insecticide-resistant and came from a pear nursery in Litoměřice in which intensive pest management was carried using Nomolt 15 SC (teflubenzuron), Dimilin 48 SC (diflubenzuron), Zolone 35 EC (phosalone) and Trebon 30 EC (etofenprox). The second population was nonresistant and came from an abandoned pear orchard in Doksany. This population was susceptible to all of the insecticides tested. The evaluations were carried out in net sleeves. The average number of eggs laid per female was calculated for seven replicates of 56 females in 2004 and 8 replicates of 70 females in 2005 (Tab. 1). The second experiment was carried out in 2004 and 2005. Seven insecticides were evaluated in the laboratory in terms of their efficacy against C. pyri. The insecticides were tested on both the resistant and non-resistant populations of C. pyri. The insecticides evaluated were: Calypso 480 SC (thiacloprid); Zolone 35 EC (phosalone); Cascade 5 EC (flufenoxuron); Vertimec 1.8 EC (abamectin); Vaztac 10 SC (alpha-cypermethrin); Nomolt 15 SC (teflubenzuron); and Dimilin 48 SC (diflubenzuron). 168 J. Fruit Ornam. Plant Res. vol. 14 (Suppl. 3), 2006:167-174

Management and control of insecticide-resistant pear psylla The insecticides were applied at the rates recommended by the manufacturers and in increasing concentrations according to FAO procedures (Anonymous, 1974) (Fig. 1). The insecticides were applied against newly hatched nymphs on May 5 in 2004 and on April 19 in 2005. They were evaluated on May 15 in 2004, and on April 28 and May 5 in 2005. Fourteen adults of C. pyri were introduced into each net sleeve. Data recorded included the total number of eggs, the number of surviving nymphs and the number of dead nymphs (Tab. 1). Efficacy was calculated based on the number of nymphs which survived after the insecticide treatment and the number of nymphs in the untreated control (Fig. 1). In the third experiment, the contact toxic effect of insecticide residues on adults of the resistant strain of C. pyri was tested in the laboratory using the tarsal test. Adults were contaminated with filter paper impregnated with the seven insecticides. After 10 to 15 minutes, they were transferred to Petri dishes containing a pear bud or leaf. Mortality was evaluated after 24 hours. The insecticides were tested at the rates recommended by the manufacturers and in increasing concentrations (Tab. 2). The fourth experiment was carried out in 2005. A field trial was carried out to determine the efficacy of Sanmite 20 WP (pyridaben) and Calypso 480 SC against C. pyri (Tab. 3 and 4). The experiment was carried out in the pear nursery in Litoměřice and in a commercial pear orchard in Slaný. Application rates were 0.75 kg/ha for Sanmite and 0.25 l/ha for Calypso. At Litoměřice, Sanmite was applied on April 18, April 25, May 30 and June 8. Calypso was applied on April 18 and May 30. At Slaný, Sanmite was applied on April 22, June 2, and June 13. Calypso was applied on April 22 and June 2. The first treatment was directed against the first generation of C. pyri, and was carried out when the nymphs were beginning to hatch. The second treatment was carried out seven days after the first treatment. The third treatment was directed at the second generation of C. pyri. The fourth treatment was carried out eight or eleven days after the third treatment. For each variant, eggs and nymphs was counted on one 5.6 m length of pear branch and 28 leaf rosettes and recorded as the number of insects per meter of pear branch and per ten leaves (Tab. 3 and 4). Biological efficacy was recorded as a percentage and was calculated according to the following formula: x = 100 [(z/y-k)*100] where x is the biological efficacy, z is the number of surviving nymphs in the treated combinations, y is the total number of eggs and nymphs in the untreated control, and k is the total number of eggs in the treated combinations (Tab. 3 and 4). J. Fruit Ornam. Plant Res. vol. 14 (Suppl. 3), 2006: 167-174 169

F. Kocourek and J. Stará RESULTS AND DISCUSSION The insecticide-resistant population of C. pyri was about twice as fecund as the non-resistant population (Tab. 1). This is probably not due to genetic differences, but because the food quality in the intensively treated pear nursery was higher than in the untreated abandoned orchard. The non-resistant population might also have been less fecund because of the higher numbers of parasitic wasps in the abandoned orchard. T a b l e 1. Mean fecundity in C. pyri females in net sleeves in 2004 and 2005 (total number of eggs per female for the given period) Population Insecticideresistant (Litoměřice) Non-resistant (Doksany) 2004 2004 2005 2005 egg-laying total number of egg-laying period eggs period March 23 to March 18 to May 5 52.7 April 19 33.5 (43 days) (31 days) March 23 to May 5 (43 days) 20.3 March 18 to April 19 (31 days) total number of eggs 17.0 The most effective insecticides against both the insecticide-resistant and non-resistant populations were Sanmite, Calypso and Vertimec (Fig. 1). The efficacy of these insecticides ranged from 92 to 100%. The efficacy of Cascade ranged from 51 to 100 %. The efficacy of Zolone, Trebon, Dimilin and Nomolt differed between the two populations. These insecticides were significantly less effective against the insecticide- resistant population than against the non-resistant population (Fig. 1). Several of these insecticides were completely ineffective or only slightly effective against the insecticide-resistant population (Fig. 1, arrows). The efficacy of a given insecticide varied from year to year and from testing date to testing date within the same year. The contact toxic effect of the insecticides on adults of C. pyri was low except in the case of Cascade (Tab. 2). With some insecticides, mortality was noted after 24 hours. For example, when Nomolt was applied in Slaný in 2005, mortality reached 64% after five days (Tab. 2). C. pyri nymphs were much more resistant to Zolone than adults of the overwintering generation. Etiene et al. (1992) found that summer adults of C. pyri were less resistant to Avermectin B1 than winter adults. The overwintering stages of C. pyri were more resistant to the insecticide than the summer stages. The relative differences in resistance between populations is subject to seasonal variation (Bues et al., 1999). Resistance to deltamethrin among populations of C. pyri differed by a factor of 31 at the adult stage and by a factor of 135 at the last larval stage (Bues et al., 2003). 170 J. Fruit Ornam. Plant Res. vol. 14 (Suppl. 3), 2006:167-174

Management and control of insecticide-resistant pear psylla a a 100 90 80 70 60 50 40 30 20 10 0 Sa 05a - 0,075 Sa05a - 0,128 Sa 05b - 0,075 Sa 05b - 01285 Sa 05a -0,075 Sa 05b - 0,075 Cal04-0,063 C al04-0,108 Cal04-0,063 Cal04-0,108 Ve 04-0,1 Ve 04-0,1 Ca04-0,15 Ca 05a - 0,15 Ca 05b - 0,15 Ca 05a - 0,256 Ca 05b - 0,256 Ca04-0,15 Ca 05a - 0,15 Ca 05b - 0,15 b 100 90 80 70 60 50 40 30 20 10 0 Zo 04-0,2 Zo05a - 0,2 Zo 05b - 0,2 Zo04-0,2 Zo 05a - 0,2 Zo 05b - 0,2 No 04-0,25 No 05a - 0,25 No 05b - 0,25 No 04-0,25 N o 05a - 0,25 N o 05b - 0,25 N o 05a - 0,73 N o 05b - 0,73 Di 04-0,025 Di 04-0,025 Tr 05a - 0,05 Tr 05b - 0,05 Tr 05a - 0,05 Tr 05b - 0,05 Figure 1a, b. Toxicity of insecticides against C. pyri nymphs populations from Litoměřice and Doksany in 2004 expressed in percentage of relative mortality to untreated control (04 evaluated 10 days after the treatment) and in 2005 (05a evaluated 10 days after treatment, 05b evaluated 17 days after treatment). Black column Litoměřice, white column Doksany. Sa Sanmite, Cal Calypso, Ve Vertimec, Ca Cascade, Zo Zolone, No Nomolt, Di Dimilin, Tr Trebon The biological efficacy of Sanmite and Calypso generally ranged from 96 to 99%. Sanmite and Calypso were effective against the insecticide-resistant population of C. pyri in the field (Tab. 3 and 4). J. Fruit Ornam. Plant Res. vol. 14 (Suppl. 3), 2006: 167-174 171

F. Kocourek and J. Stará T a b l e 2. Mortality in insecticide-resistant C. pyri adults 24 hours after insecticide treatment under laboratory conditions Insecticide treatment Litoměřice March 23 (after Cascade March 18) Origin of insect population Litoměřice April 19 (after Oleoekol and Cascade May 7 ) Litoměřice April 19 Litoměřice May 4 (after Neem Azal) Untreated control 0 35.4 20 53.3 Calypso 0.25% 50-60 93.3 Zolone 0.2% 92.8-60 66.7 Cascade 0.15% 32 - - - Cascade 0.25% 89.3 95.2 100 80 Vertimec 0.1% - 35.1 - - Vaztac 0.15% 33.3-26.7 46.7 Nomolt 0.25% 18.5 40.7 - - Nomolt 0.43% 35.3 - - - Nomolt 0.73% 54.8-13.3 33.3 Nomolt 1.248% - 69 - - Dimilin 0.025% 11.5-13.3 53.3 Dimilin 0.043% 25 - - - T a b l e 3. Number of C. pyri eggs and nymphs and biological efficacy of Sanmite and Calypso in samples of pear branches or leaf rosettes collected three or ten days after spraying at Litoměřice in 2005 Treatment Number of C. pyri per meter of branch length Biological efficacy Eggs Nymphs Total [%] Untreated control (April 21) 194.3 24.5 218.8 x Sanmite (April 21) 22.9 7.3 30.2 96.6 Calypso (April 21) 14.3 1.4 15.7 99.0 Untreated control (April 25) 23.2 137.5 160.7 x Untreated control (April 25) 4.6 6.17 10.7 96.3 Sanmite (April 25) 6.4 0.9 7.3 99.5 Number of P. pyri per 10 leaves Sanmite (May 5) 2.1 0.1 2.2 99.9 Sanmite (May 27) 13.7 0.4 14.1 99.9 Untreated control (June 2) 34.8 15.4 51.9 x Sanmite (June 8) 9.7 10.9 20.6 79.0 Calypso (June 8) 35.6 1.3 36.9 97.5 Cross resistance to organophosphates, pyrethroids and amitraz has been found in populations of C. pyri in Europe (Bues et al., 1999). After many years of exposure to insecticides such as Nomolt and Zolone, a population of C. pyri can develop resistance to several insecticides at the same time, including growth regulators such as Nomolt and Dimilin, organophosphates 172 J. Fruit Ornam. Plant Res. vol. 14 (Suppl. 3), 2006:167-174

Management and control of insecticide-resistant pear psylla such as Zolone, and pyrethroids such as Trebon. On the basis of our results, the following insecticides are recommended for controlling insecticideresistant populations of C. pyri: Sanmite 20 WP, Calypso 480 SC and Cascade 5 EC. T a b l e 4. Number of C. pyri eggs and nymphs and biological efficacy of Sanmite and Calypso in samples of pear branches or leaf rosettes collected three or ten days after spraying at Slaný in 2005 Treatment Number of C. pyri per meter of branch length Biological efficacy Eggs Nymphs Total [%] Untreated control (April 21) 398.3 5.3 403.6 x Sanmite (May 2) 59.6 7.3 72.4 99.8 Calypso (May 2) 85.8 4.8 180.7 99.9 Number of C. pyri per ten leaves Untreated control (May 27) 36.8 0.5 37.3 x Sanmite (June 9) 12.9 2.0 14.9 97.4 Calypso (June 9) 10.7 1.7 12.4 97.5 Sanmite (June 21) 0.8 0.06 0.86 99.9 Calypso (June 21) 0.0 0.01 0.01 99.8 Acknow ledgements. This work was supported by the Czech Ministry of Agriculture, Project No. 0002700603. REFERENCES Anonymous 1974. Recommended Method for the Detection and Measurement of Resistance of Agricultural Pests to Pesticides. FAO Method No. 11, FAO PLANT PROT. BULL. 22(5/6): 108-111. Berrada S., Nguyen T.X., Merzoug D., Fournier D. 1995. Selection for Monocrotophos resistance in pear psylla, Cacopsylla pyri (L) (Hom, Psyllidae). J. APPL. ENTOMOL. 119(7): 507-510. Bues R., Boudinhon L., Toubon J.F., Faivre D. Arcier F. 1999. Geographic and seasonal variability of resistance to insecticides in Cacopsylla pyri L. (Hom., Psyllidae). J. APPL. ENTOMOL. 123(5): 289-297. Bues R., Boudinhon L., Toubon J.F. 2003. Resistance of pear psylla (Cacopsylla pyri L., Hom., Psyllidae) to deltametrin and synergism with piperonyl butoxide. J. APPL ENTOMOL. 127(5): 305-312. Etiene J.C., Nguyen T.X., Burts E.C. 1992. Susceptibility of Cacopsylla pyri and C. pyricola (Homoptera, Psyllidae) to Avermectin B1 applied topically and as residues on pear foliage. J. ECONOM. ENTOMOL. 85(1): 182-186. Harries F.H., Burts E.C. 1965. Insecticide resistance in pear psylla. J. ECONOM. ENTOMOL. 58: 172. J. Fruit Ornam. Plant Res. vol. 14 (Suppl. 3), 2006: 167-174 173

F. Kocourek and J. Stará TAKTYKA ZWALCZANIA POPULACJI MIODÓWKI GRUSZOWEJ PLAMISTEJ (Cacopsylla pyri) ODPORNEJ NA INSEKTYCYDY F r a n t i še k K o c o u r e k i J i t k a S t a r á S T R E S Z C Z E N I E Na podstawie testu biologicznego dokonano oceny efektywności różnych insektycydów w odniesieniu do owadów dorosłych i larw Cacopsylla pyri pochodzących z dwóch różnych miejsc Czech. Odpornośćosobników populacji C. pyri pochodzących z sadu intensywnie opryskiwanego preparatami: Nomolt 15 SC (teflubenzuron), Dimilin 48 SC (diflubenzuron), Zolone 35 EC (fosolon) i Trebon 30 EC (etofenproks) zostało potwierdzone w teście laboratoryjnym. Osobniki populacji C. pyri pochodzące z nieopryskiwanego sadu były wrażliwe na wszystkie testowane insektycydy. Największą efektywność w wyniszczaniu larw C. pyri wykazano w teście wykonanym w izolatorach z zastosowaniem preparatu Calypso 480 SC (tiachlopryd) i Vertimec 18 EC (abamectin). Efektywnośćtestowanych insektycydów w odniesieniu do owadów dorosłych C. pyri była wystarczająca z wyjątkiem preparatu Cascade 5 EC i Zolone 35 EC, w przypadku populacji pochodzącej z sadu intensywnie opryskiwanego. Odporności larw w stosunku do preparatu Zolone 35 EC była znacznie wyższa niż owadów dorosłych generacji zimującej. Efektywność preparatu Sanmite 20 WP (pyridaben) i Calypso 480 SC była znakomita w stosunku do nowo wylęgniętych larw populacji C. pyri wykazującej zwielokrotnionąodporność w doświadczeniach polowych w dwóch różnych lokalizacjach. Na podstawie wyników Sanmite 20 WP, Calypso 480 SC i Cascade 5 EC były polecane przeciwko C. pyri w strategii antyodpornościowej. Sanmite 20 WP byłrekomendowany do zarejestrowania przeciwko C. pyri w sadach gruszowych w Czechach. Słowa kluczowe: Cacopsylla pyri, odporność, insektycydy, sady gruszowe 174 J. Fruit Ornam. Plant Res. vol. 14 (Suppl. 3), 2006:167-174