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To Stephanitis Takeyai (Hemiptera: Tingidae) PLANT-INSECT INTERACTIONS Resistance Mechanisms in Pieris Taxa (Ericaceae) to Stephanitis takeyai (Hemiptera: Tingidae) 1,2 1 3 SHAKUNTHALA NAIR, S. KRISTINE BRAMAN, AND D. A. KNAUFT Environ. Entomol. 41(5): 1153Ð1162 (2012); DOI: http://dx.doi.org/10.1603/EN11323 ABSTRACT This study examines some of the potential mechanisms of resistance in selected Pieris (Ericaceae) taxa to the Andromeda lace bug, Stephanitis takeyai Drake and Maa, based on differences in resistance to lace bug feeding, and the possible role of leaf parameters such as leaf wax, toughness, nutrient composition, and stomatal characters in plant resistance. Experiments with extracts of leaf-surface lipids revealed that Pieris leaf wax did not have a role in resistance to lace bug feeding. Leaf wax extracts from a resistant species P. phillyreifolia (Hook.) DC. applied to leaves of a susceptible cultivar P. japonica (Thunb.) D.Don ex G.Don ÔTemple BellsÕ did not affect feeding, oviposition, or survival of S. takeyai; and neither the extracts from Temple Bells induce susceptibility in P. philly- reifolia. Leaf penetrometer measurements indicated that signiÞcantly higher force was required to puncture P. phillyreifolia leaves, which also had higher Þber, lignin, and cellulose, and lower leaf moisture contents. Ultrastructural examination of leaves of Pieris taxa revealed signiÞcant differences in the number and size of stomata. P. phillyreifolia leaves had the highest number of stomata per unit area but these were the smallest in size, whereas P. japonica (Thunb.) D.Don ex G.Don Temple Bells leaves had the fewest and largest stomata. Resistance in Pieris taxa to S. takeyai may be attributed to a combination of different factors including leaf toughness, moisture, and stomatal characters. The type of resistance may be described as antixenosis combined with antibiosis, because reduced adult survival and reproduction were observed on the taxa resistant to lace bug feeding. KEY WORDS Pieris, Stephanitis, resistance, stomata, toughness The Andromeda lace bug, Stephanitis takeyai Drake hybrids also are recognized (Dunbar 1974). The rea- and Maa, is an important pest of Pieris D. Don spp. sons for the preferences exhibited by S. takeyai are not (Johnson and Lyon 1991), a popular ericaceous orna- yet known. Leaf physical and chemical parameters mental plant. Lace bugs feed by sucking cell contents, like toughness, pubescence, stomatal size and density, resulting in yellowish white stipples on the abaxial leaf moisture content, and epicuticular wax are possible surfaces, and leave oily, black frass spots on the adaxial mechanisms of resistance to lace bugs and other suck- surfaces. Lace bug feeding leads to reduction in pho- ing pests. Differences in leaf-surface lipid components tosynthetic efÞciency (Buntin et al. 1996) and occa- were noted between resistant and susceptible azaleas sionally, plant death (Schread 1968). In ornamental (Balsdon et al. 1995, Wang et al. 1999) and studies with plants grown for foliage and ßowers, lace bug damage extracts of epicuticular leaf wax indicated that leaf wax to even few leaves affects the esthetic value and mar- serves as a primary mechanism of resistance of decid- ketability. uous azalea to S. pyrioides (Scott) (Chappell and Pieris taxa (species, cultivars, and hybrids) show Robacker 2006). Leaf pubescence (Wang et al. 1998b) differences in susceptibility to lace bug feeding (Dun- and stomatal characters (Kirker et al. 2008) could not bar 1974, Labanowski and Soika 2000, Nair et al. 2012). be correlated with resistance to S. pyrioides although When 60 Pieris taxa were compared for their suscep- they varied considerably among tested azaleas. Leaf tibility to lace bugs, the highest damage was observed toughness is a major source of protection in plants on P. japonica (Thunb.) D.Don ex G.Don, whereas P. against insect herbivores, and their avoidance of tough phillyreifolia (Hook.) DC. was least damaged. Among plant parts is a common observation (Howard 1988, P. japonica cultivars, S. takeyai showed clear prefer- Larsson and Ohmart 1988). Host plants are important ence for ÔTemple BellsÕ and ÔCavatineÕ, whereas ÔVar- sources of water and nutrients for phytophagous ar- iegataÕ and ÔPreludeÕ were less damaged (Nair et al. thropods and thus can inßuence herbivory (Bernays 2012). The low preference for P. floribunda and its and Chapman 1994). Insects can adapt well to new environments and their nutritional requirements may 1 Department of Entomology, University of Georgia, 1109 Experi- vary even within a species, which makes it difÞcult to ment St., GrifÞn, GA 30223. establish whether nutritional factors confer herbivory 2 Corresponding author, e-mail: [email protected]. 3 Department of Horticulture, University of Georgia, 1111 Plant resistance to plants (House 1961). Nevertheless, many Sciences Bldg., Athens, GA 30602. choices made by insects during their life processes are 0046-225X/12/1153Ð1162$04.00/0 ᭧ 2012 Entomological Society of America 1154 ENVIRONMENTAL ENTOMOLOGY Vol. 41, no. 5 inßuenced by nutritional needs (Slansky 1982) and Table 1. S. takeyai adult survival, leaf damage, and nymph therefore, determining foliar nutrient composition emergence in Assay A (Pieris leaves treated with Pieris leaf wax may provide explanation for resistance shown by extracts) (Averages from two repetitions, A1 and A2) plants. No. of live Lea No. of Because of the varying effects of different resistance Treatments adults damagea nymphs mechanisms, the general understanding is that resis- T6 solvent or control on P. japonica 1.17a 5.49a 2.81b tance is a combination of mechanisms. This paper ÔTemple BellsÕ T1 P. phillyreifolia extract on 0.67b 3.43b 5.56a examines some of the above mechanisms for their P. japonica ÔTemple BellsÕ potential role in resistance exhibited by Pieris taxa to T4 P. japonica ÔTemple BellsÕ extract 0.92ab 3.41b 1.63b on P. j. ÔTemple BellsÕ S. takeyai. T3 P. phillyreifolia extract on 0.08c 0.22c 0.00c P. phillyreifolia T5 solvent or control on 0.00c 0.08c 0.00c Materials and Methods P. phillyreifolia T2 P. japonica ÔTemple BellsÕ extract 0.00c 0.00c 0.00c Plant Material. Pieris taxa were obtained from the on P. phillyreifolia F 10.01 40.58 16.84 Department of Horticulture Pieris collection located P Ͻ0.0001 Ͻ0.0001 Ͻ0.0001 at the University of Georgia (UGA) Horticulture Farm Overall model F ϭ 5.31 F ϭ 20.55 F ϭ 9.12 df ϭ 10,61 df ϭ 10,61 df ϭ 10,61 in Watkinsville, GA and various commercial nurseries. Ͻ Ͻ Ͻ The plants were obtained in 11.3-liter (3 gallon) and P 0.0001 P 0.0001 P 0.0001 3.7-liter (1 gallon) pots and maintained in a screen a Percent leaf area damaged; means in the same column bearing house with regular irrigation. For the different exper- different letters are signiÞcantly different (␣ ϭ 0.05; LSD). iments, leaves were collected from plants with at least Þve branches. Lace Bugs. Stephanitis takeyai colonies were initi- and 3 the solvent alone was the control, whereas in ated from a population obtained from a landscape replications 4, 5, and 6 the control was no treatment. setting in Long Island, NY in April 2009. The colonies Thus, two controls were prepared. This was done to were maintained in plastic containers through the test for the effect, if any, of the solvent. In all, there period of study at 27 Ϯ 1ЊC and a photoperiod of 14:10 were three ÔdonorsÕ in Trial A, (P. phillyreifolia, P. (L:D) h, on Pieris cultivars P. japonica ÔDoddÕs Crystal japonica ÔTemple BellsÕ, and solvent) and two Ôrecip- Cascade FallsÕ, ÔTemple BellsÕ, and ÔScarlett OÕHaraÕ. ientsÕ (P. phillyreifolia and P. japonica ÔTemple BellsÕ). The host plants were rotated to avoid selection by lace Each donorÐrecipient combination was considered as bugs. For conducting the assays, 5Ð10-d-old adult lace a treatment, giving a total of six treatments. Two lace bugs were aspirated into plastic tubes and then trans- bugs were released into each petri dish. The dishes ferred to the assay dishes by using a brush. were arranged in a randomized complete block design Leaf Wax Extraction Studies. The procedure for and placed in a growth chamber under 27 Ϯ 1ЊC and leaf wax extraction was adopted from Chappell and a photoperiod of 14:10 (L:D) h. Observations on the Robacker (2006) and modiÞed suitably for different number of bugs alive were taken on day 2, 7, 9, and 13. assays, designated as Trials A and B. On day 13, the surviving adults were removed and the Trial A. Forty mature leaves (fourth or Þfth leaf leaves were scored for percent leaf area damage by from the bottom of a branch) from plants of a resistant using the scoring chart developed by Klingeman et al. (P. phillyreifolia) and a susceptible cultivar (P. ja- (2000), in which damaged leaves were chosen to rep- ponica ÔTemple BellsÕ) (Nair et al. 2012) were col- resent a range of lace bug feeding injury. After scoring, lected. These were air dried for 120 h and then im- the leaves were maintained and observed daily for mersed in 100 ml of chloroform for 15 s. Chloroform emergence of nymphs. Both treated and untreated was evaporated and remaining epicuticular wax re- sides of each leaf were observed separately for leaf suspended in 50 ml of a 2:1 mixture of ethanol and damage and nymph emergence. This trial was con- deionized water, under mild heating (32ЊC) and stir- ducted twice (designated as A1 and A2). ring. Upon cooling to room temperature (20ЊC), the Trial B. To measure the effect of differences in resulting solution was applied directly to the fresh extraction times and Pieris taxa, two sets of 40 leaves leaves by painting the leaf surface with a brush dipped each of plants of a resistant (P.
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