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HORTICULTURAL ENTOMOLOGY Influence of Intensity and Duration of Regulated Deficit Irrigation on Erythroneura elegantula (: Cicadellidae) on Grape

1 MICHAEL J. COSTELLO AND SHAWN T. VEYSEY

Horticulture and Crop Science Department, Cal Poly State University, San Luis Obispo, CA 93407

J. Econ. Entomol. 105(4): 1293Ð1301 (2012); DOI: http://dx.doi.org/10.1603/EC11321 ABSTRACT We conducted studies in a Paso Robles, CA, grape (Vitis vinifera L.) vineyard in 2002 and 2003 to estimate the impact of regulated deÞcit irrigation (RDI) intensity and duration on western grape , Erythroneura elegantula Osborn. Treatments were based on deÞcit intensity, 50 and 25% of standard irrigation (moderate and severe deÞcits, respectively), and deÞcit duration, 3 or 6 wk time, initiated at the grape phenological stage of berry set. The standard irrigation served as the control, and was intended to be as close to 100% of evapotranspiration (1.0 ETc) for grape in this area. Each week we took counts of leafhopper nymphs and estimated stomatal conductance, and at the end of each leafhopper generation we counted live, hatched and parasitized leafhopper eggs. Second generation leafhopper nymphal density was lowered by about 38 and 70% in 2002 and 2003, respec­ tively, but in 2003 only the severe deÞcit had a negative effect on the third generation. This same pattern was seen in oviposition: second generation egg density was reduced by about 44% in the deÞcit treatments, but in the third generation only the severe deÞcit was lower than the control. There was little difference between the 3 vs. 6 wk duration in nymphal or egg density. The differences among treatments in second generation peak nymphal density were greater than the differences in second generation hatched eggs, suggesting that in addition to egg mortality, the deÞcits also affected nymphal mortality. Management strategies for maintaining leafhopper density low in the second generation and third generations include maintaining a sub-1.0 ETc irrigation strategy after the main RDI period, or reinstating the RDI to correspond to the third generation.

KEY WORDS leafhopper, vineyard, water, regulated deÞcit irrigation (RDI)

Erythroneura spp. (Hemiptera: Cicadelli­ V. vinifera is the only commercial host plant for dae: ) are an economic concern for Erythroneura spp. in California. Eggs are laid under the commercial grape, Vitis vinifera L., growers in many leaf cuticle, and nymphs and adults feed on cells in the viticultural regions of the United States, including mesophyll region, causing loss of chlorophyll and po­ California, Arizona, Oregon, Washington, and upstate tentially a reduction in the rate of photosynthesis. In New York. In California, western grape leafhopper, California coastal regions, Erythroneura spp. have two Erythroneura elegantula Osborn, is found throughout to three generations per season, depending on the the state, whereas Erythroneura variabilis Beamer is climate and the weather in any given year. restricted to southern California, parts of the San Several cicadellids, including the Erythroneura spp., Joaquin Valley, and warmer regions of the North have been shown to be sensitive to host plant water Coast. Erythroneura spp. overwinter as reproductively stress, regardless of the type of plant tissue fed upon. diapausing adults, and females oviposit on newly pro­ Potato leafhopper, Empoasca fabae (Harris), feeds on duced grape tissue in the spring. In the Paso Robles phloem as well as mesophyll cells (Hunter and Backus region on the Central Coast, Þrst generation nymphs 1989) and has been shown to have reduced perfor­ eclose in early to mid-June. In this region, at least two mance on water-stressed alfalfa, Medicago sativa L. generations, and sometimes a third, occur annually. (Schroeder et al. 1988, Hoffman and Hogg 1992). For­ Treatment thresholds for wine grapes on the Central nasiero et al. (2012) found lower densities of Em­ Coast vary considerably, but they are typically in the poasca vitis (Go¨ the) on nonirrigated versus irrigated range of an average of 4 Ð10 nymphs per leaf. During grape in Italy. Glassy-winged sharpshooter, Homalo­ the time of this study, Erythroneura spp. were treated disca vitripennis (Germar), feeds on xylem and was for chemically on =93,000 ha of vineyards (California found to have lower densities on Þeld citrus (Citrus Department of Pesticide Regulation 2004). spp.) irrigated at 60% of estimated crop evapotrans­

piration (0.60 ETc) versus 0.8 ETc or 1.0 ETc (Krugner et al. 2009), and it was less abundant and had de­ 1 Corresponding author, e-mail: [email protected]. creased feeding rates on drought-stressed citrus in the

0022-0493/12/1293Ð1301$04.00/0 © 2012 Entomological Society of America 1294 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 4

Table 1. Summary of estimated ETc and amount of water applied for each deficit period and for the season

Treatment

Standard irrigation Moderate (50% Severe (25% Moderate (50% Severe (25% Estimated ETc (control) irrigation) 3 wk irrigation) 3 wk irrigation) 6 wk irrigation) 6 wk

2002 314 (0.92 ETc) 262 234 231 191 340 2003 305 (0.94 ETc) 268 244 239 214 325

Standard irrigation period is 30 April 30 Ð1 October. laboratory (Nadel et al. 2008). Trichilo et al. (1990) of the vineyard, but because we observed a high soil and Daane and Williams (2003) found Erythroneura water buffering capacity in one block, in 2003 we spp. to have lower densities on vines watered at an moved the site to the northwestern corner, to achieve < irrigation level of 1.0 ETc over the course of the better soil uniformity. grape growing season. The design for the experiments was a randomized Regulated deÞcit irrigation (RDI) (Chalmers et al. complete block, split plot, with the main plot factor 1986) is a management technique designed to reduce intensity of deÞcit irrigation and the subplot factor the amount of applied water relative to 1.0 ETc during duration of the deÞcit. The three levels of the deÞcit key periods in the growing season of a perennial crop. intensity factor were 1) 50% of standard irrigation On wine grapes, RDI is typically initiated near berry (moderate deÞcit), 2) 25% of standard irrigation (se­ set (Prichard et al. 2004). The objectives of RDI in­ vere deÞcit), and 3) standard irrigation (the control). clude improvements in the ratio between shoot The two levels of deÞcit duration were 1) 3 wk after growth and fruit load, and fruit and wine quality deÞcit initiation and 2) 6 wk after deÞcit initiation. We (Chaves et al. 2007), and results have had varied ef­ replicated the treatments three times. Plot size was fects on grape vigor and yield. Recent RDI research 16.5 by 14.7 m (six rows by eight vines). Moderate and efforts have continued in a variety of viticultural re­ severe deÞcit treatment plots were divided into two gions worldwide, including Portugal (dos Santos et al. (i.e., the split plots) for the duration treatments (3 2007), Spain (Santesteban et al. 2011), Brazil (Dantas versus 6 wk). Subplots were separated by one vine et al. 2007), and Chile (Acevedo-Opazo et al. 2010). row, and two vines on either end of the subplot as Costello (2008) imposed RDIs of at least 50% of full buffers. irrigation (i.e., near 1.0 ETc) for a 6-wk period from The control or standard irrigation treatment for grape berry set to veraison (initiation of berry ripen­ intensity was based on the growerÕs normal practice at ing), Þnding second generation Erythroneura spp. the vineyard, i.e., to irrigate close to 1.0 ETc through­ = = X nymphal density lower by 40% at one Þeld site and out the season: ETc kc ETo, where kc is the crop = 51% at another, and egg density by 30% and 54% at coefÞcient and ETo is the estimated water use of a the same sites, respectively. However, in 1 yr com­ clipped grass crop. To estimate how accurate the prac­ paring 50 to 25% irrigation treatments, there was no tice was, we used the kc values published by Williams signiÞcant difference in nymphal or egg density. et al. (2003) and ETo values from the Paso Robles Costello (2008) did not vary the duration of the deÞcit Vintners and Growers Association weather station in treatments, nor did he look at the impact of the deÞcits Paso Robles, and we compared the values to the three on the third generation of leafhopper nymphs. treatments. The estimated ETc and amount of water The purpose of this study was to look not only at applied for each deÞcit period and for the season are RDI intensity but also at duration of deÞcit, comparing summarized in Table 1. We regulated irrigations using a short time period of 3 wk with the longer period of in-line programmed controllers (Gilmour, Somerset, 6 wk, on the density of second as well as third gen­ PA), and the amount of water applied was estimated eration nymphs and eggs of E. elegantula. Crop yield by placing a drip emitter into an 80-liter collection and quality results are presented in another paper container in each subplot; we monitored the subplots (Costello and Patterson 2012). weekly. Before the imposition of the RDI treatments, vines were watered according to the standard irriga­ tion. In 2002, deÞcit treatments began on 21 June, the Materials and Methods duration split began on 15 July, and deÞcits ceased on We conducted experiments in 2002 and 2003 at 6 August. In 2003, deÞcits began on 21 June, the du­ Steinbeck Vineyards, located =15 km east of Paso ration split began on 14 July, and deÞcits ceased on 10 Robles, in San Luis Obispo County, CA, in a vineyard August. for commercial wine grape production. The study Pesticides applied during the study consisted of vineyard was established in 1992, with ÔCabernet Sau­ elemental sulfur and demethylation inhibitor fungi­ vignon,Õ clone 8 on 5C rootstock. Rows were spaced cides for powdery mildew (Erysiphe necator Schwein) 3.3 m wide and vines spaced 2.1 m within the row. and glyphosate for weed management. None of these Vines were trained to quadrilateral cordons and spur pesticides is known to have a signiÞcant effect on pruned. Soil type at the sites was a San Ysidro loam leafhopper mortality. with a clay-to-clay loam subsoil at 58 Ð96 cm. In 2002, We estimated vine water stress by measuring sto­ 2 the study site was located on the southwestern corner matal conductance (moles CO2/m /s) with an LI­ August 2012 COSTELLO AND VEYSEY:REGULATED DEFICIT IRRIGATION AND E. elegantula DENSITY 1295

0.9 2002 Standard irrigation 0.8 Moderate deficit-3 weeks Severe deficit-3 weeks 0.7 ± SEM 1 - 0.6 sec 2 m-

2 0.5

0.4 mol CO

0.3 Deficit period

0.2 20 27 3 11 18 25 1 8 15 22 29 June July August -2 -1 : Fig. 1. Stomatal conductance (mean mol CO2 m s SE) over time, 2002, 3-wk deÞcit duration.

6200 portable photosynthesis system (LI-COR Biosci­ which was just 1.4% lower than the severe deÞcit at ences, Lincoln, NE), taking Þve readings per plot per three weeks duration in 2002 and 2.0% lower in 2003 week between 1100 and 1400 hours, between 20 June (Table 1). and 29 August in 2002, and between 25 June and 3 Stomatal Conductance. Results of stomatal conduc­ September in 2003. We took weekly counts of leaf­ tance indicate an effect of RDI in each year, but there hopper nymphs from 20 June to 19 September (Þrst was not a consistent correspondence between stoma­ and second generations) in 2002 and from 25 June to tal conductance and the deÞcit irrigation period. In 15 October (Þrst, second, and third generations) in 2002 (Figs. 1 and 2), there was no signiÞcant effect for 2003, sampling 20 leaves per plot until the irrigation the Þrst two postdeÞcit samplings, but the following duration split, and thereafter on 15 leaves per plot. We week (11 July) the deÞcit treatments showed a 21.0% did not sample leafhopper adults. We counted leaf­ reduction in stomatal conductance from the control hopper eggs after the end of the Þrst, second, and third (contrast: F = 8.29; df = 1, 22; P < 0.01), and the generations, sampling 20 mature leaves per subplot. moderate deÞcit treatment was lower than the severe We brought the leaves back to the laboratory, cut deÞcit by 20.4% (contrast: F = 5.47; df = 1, 22; P = them in half, and counted eggs on the half-leaves 0.02). There was an overall effect for the three weeks under a 40X dissecting microscope, and doubled that (18 JulyÐ1 August) after the cessation of the 3-wk number to get an estimate of eggs per leaf. Eggs were deÞcit (repeated measures ANOVA: F = 14.78; df = 2, scored as hatched, live or parasitized by the egg para­ 49; P < 0.01), with the deÞcit treatments 18% lower sitoids Anagrus spp. In 2002, very few eggs were re­ than the control (contrast: F = 28.21; df = 1, 49; P < corded, and the data are not included here. 0.01), but no difference between moderate and severe Stomatal conductance and nymphal density data deÞcits (contrast: F = 1.35; df = 1, 49; P = 0.25). There were log10 transformed, and we analyzed data by re­ was also a deÞcit duration effect, with the 6-wk time peated measures analysis of variance (ANOVA), with 7.6% lower than the 3-wk time (F = 6.57; df = 1, 42; mean separation by orthogonal contrasts (SAS Insti­ P = 0.01), but no interaction between intensity and tute 2010). Contrasts compared the combined deÞcit duration (F = 1.64; df = 2, 42; P = 0.20). For the treatments to the control, the intensity (moderate postdeÞcit period of 8 Ð29 August, there was no overall versus severe) deÞcits, or the duration (3 versus 6 wk) effect of intensity (F = 2.06; df = 2, 49; P = 0.13), but deÞcits. Leafhopper egg density was analyzed by there was an effect of duration (F = 37.44; df = 1, 28; ANOVA, with mean separation using TukeyÕs honestly P < 0.01), with deÞcit effect at 6 wk 15.8% lower than signiÞcant difference. We considered differences sta­ that at 3 wk. tistically signiÞcant at P < 0.05. In 2003, there was a signiÞcant difference among treatments for the Þrst 3 wk (25 JuneÐ14 July) (re­ peated measures ANOVA: F = 9.16; df = 2, 22; P < Results 0.01) (Figs. 3 and 4), with the contrast between the Applied Water. Water applied in each year and a control and the deÞcits signiÞcant (F = 17.70; df = 1, < comparison with estimated ETc is shown in Table 1. 22; P 0.01), and the deÞcit treatments lowered by The control treatment was 92.16% of estimated ETc in 26.1% compared with control, but no difference be­ 2002 and 93.75% in 2003. The greatest difference tween the moderate and severe deÞcit treatments among deÞcit treatments was between the severe def­ (F = 0.62; df = 1, 22; P = 0.44). For the subsequent 3 icit at 6-wk duration, which was 26.9% lower than the wk (23 JulyÐ 6 August), there was a signiÞcant effect moderate deÞcit at 6-wk duration in 2002 and 20.3% of deÞcit intensity for the 3-wk duration (F = 6.23; lower in 2003 (Table 1). The treatments that differed df = 2, 22; P < 0.01), with the deÞcits 10.3% lower than the least were the moderate deÞcit at 6-wk duration, the control (contrast: F = 11.39; df = 1, 22; P < 0.01), 1, was mated primarily ( was For 1296 3.18; icit but duration at there (Figs. generation 1, lower 211; than 0.01) F 172; Leafhopper 211; the = treatments the no no P no the df 0.28; (Figs. was < than 5 6-wk P the P difference overall subsequent signiÞcant and = 0.01), = and < control Fig. Fig. between no df 1, second 0.06), the deÞcit 0.01) duration 6). 5 14; = intensity signiÞcant 2. 3. and with deÞcit severe Nymphal However, (F 1, P Stomatal Stomatal (contrast: (Figs. with 14; between 6), = = intensity effect generation 8 4 the August wk P 0.09). (F

2 -1 1.07; and

± duration mol CO m- sec SEM deÞcit 2 (F no 0.2 0.4 0.6 0.8 1.0 1.2 = deÞcit 5 difference = (13 mol CO m-2 sec-1 ± SEM = conductance conductance of 2 0.60) Density. there and interaction the 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 df 3.04; F moderate 0.35; deÞcit AugÐ3 and effect (contrast: = = June treatments 6). moderate to 25 or effect Deficit period was 69.7; df 1, 12 J df 20 Severe deficit-3weeks have Moderate deficit-3weeks OURNAL Standard irrigation 6-wk June = 22; (F September), in = September. intensity In an df 7 14 2, (mean (mean 1, 2003 between deÞcit and 27 ( = P 2002, been overall F duration F 172; 22; = = deÞcit 44.0; = OF = 36.3% severe 1, 3 P 0.31), 3.68; 18.2; mol mol P E intensity between for 211; we July = Deficit period CONOMIC = df second deÞcit There 11 lower 22.8% 0.07). there CO CO 0.55) 23 3 (F df df = esti­ July def­ P and wk 2 2 = = = < 2, 18 m m 31 - - E 2 2 s s NTOMOLOGY ber deÞcit tember, than df leafhoppers 0.01) 6). moderate the no treatments effect ration there second lower the ( such 25 - - F 1 1 In = = : : signiÞcant For 6 severe and moderate the that 1 but 2, 2003, SE) SE) 3.51; was of than and intensity generation 216; the and deÞcit 8 control 13 not Severe deficit-6 weeks Moderate deficit-6 weeks Moderate deficit-6weeks Standard irrigation there over over uut Sept August deÞcit 8 signiÞcant October. intensity df (F deÞcit 3 we third to the P August between wk = 2002 = time, time, 15 and < overall 20 have duration, was for estimated third 1, 2.19; (contrast: (F (F 0.01), generation, treatment (F 84; the severe 22 2003, 2002, = = no (F There been 27 df = interaction generation 15.81; the 4.12; P deÞcit second = signiÞcant 0.43; with = 29 = 3-wk 6-wk with 14.89; moderate between 1, deÞcit F the 0.06) 3 was df df 216; = df was the deÞcit deÞcit duration the = there generation = 226.07; = second df a 1, (Fig. P between deÞcits 1, between 1, 44% signiÞcant 6-wk difference treatments = = 172; 30 84; 172; duration. duration. and was 1, 0.14). df July 5), lower P 172; Vol. treatment P generation effect P severe < = a 69.6% = ( = but 16 F and 0.01) deÞcit There 1, signiÞcant P 105, 0.04), 0.51), = between effect than Septem­ 216; < at at for 114.13; deÞcit 3 lower 0.01), 3 no. (Fig. 6 Sep­ 12% was P but but du­ the the wk wk of of < 4 lower total with 13.50; 2003, moderate there P 1, 35.16; signiÞcant (Table deÞcit lower eggs action August 1.31; no moderate < 232; Leafhopper interaction 0.01) the (F eggs df there was than df in df between P lower 2), 2012 = = deÞcit hatched = = = Fig. and (F and deÞcit a 1, 7.33; the but 2, 0.31), effect was 2, signiÞcant 172; = 232; 4. than Fig. the 216; severe control no between Eggs. treatments 35.2; a df duration Stomatal eggs (F P signiÞcant and P of severe 5. signiÞcant = the P = C < = df OSTELLO deÞcit < 2, 2 -1 For by deÞcit 0.25). Leafhopper 0.01), Mean leafhopper nymphs per leaf ± SEM (F mol CO m- sec ± SEM (contrast: 2 3-wk effect 36.95; 0 1 2 3 4 5 6 = 0.2 0.4 0.6 0.8 1.0 1.2 232; 0.01), duration 69.5% = and deÞcit conductance 2, 44.4% the 23.1; 355; For effect 0 27 20 again P deÞcit duration, treatments. intensity of df AND difference June June with < 25 second for Deficit period Severe deficit-3weeks Moderate deficit-3weeks Standard irrigation deÞcit = 41.4% the df F lower P 0.01), nymphs Severe deficit-6 weeks Moderate deficit-6weeks Standard irrigation Standard V with and = < of hatched 1, = by EYSEY the 2002 third 33.36; 0.01), deÞcit 7 14 31 13 27 216; 2, (mean 3 2003 (F lower with intensity 60.1% than intensity no with generation 355; deÞcits Deficit period between :R per There = 11 P generation, interaction df July and eggs EGULATED control 1.20; < intensity, mol P the leaf no than = July for 18 < 0.01). 1, 38.7% 32.0% inter­ was CO ( 0.01) (mean 23 (F ( 6-wk total df F 216; F 25 the the 2 in in = = = = a m D - 1 : EFICIT 2 s ( generation, control moderate intensity, withtheseveredeÞcit23.6%lowerthan between 2). and stress parasitism P found ( hatched deÞcit the - SE) F F 1 = Our 8 = = : 6 There second the August over 0.3). 2.68; I 1.79; SE) RRIGATION 15 intensity a treatment study negative in severe eggs duration time, over uut Sept August df deÞcit There total 22 for df was or = there conÞrms = (F deÞcit time, 2002, 1, third 29 20 deÞcit eggs no (Schroeder AND 1, = response 232; was treatment and and 232; was 18.17; 5 signiÞcant 2003, 3-wk (F generation E P intensity Discussion no 35.2% . 30.5% intensity Sept the = P = 12 elegantula a 6-wk deÞcit 0.10) df = difference 13.74; signiÞcant by results 3 19 = 0.18), and lower et lower cicadellids deÞcit 2, (Table difference nor al. duration. df (F (Table 28.1% 355; of with D 1988, = than duration = than ENSITY duration. in others P 2, effect 1.08; 2). < lower 355; no percentage 2). the to the Hoffman For 0.01) in plant df interaction P control who moderate for of = the duration than < (Table deÞcit 2, either water 0.01), third have 1297 232; and the of in ( Generation berry (3 generation deÞcit we Generation parasitism sities. response Krugner the Erythroneura 1298 Hogg is, (2008), stressed Williams results (1990) wide P 3-wk 6-wk Severe Moderate Control 3-wk 6-wk Severe Control Moderate Means The Table > an wk). (25% (50% (25% (50% Generation found 0.05). work RDI water set And, 1992, duration duration duration duration with for overall 2. and followed deÞcit deÞcit our irrigation) irrigation) irrigation) irrigation) grapevines by (6 2003, 3 2 between et deÞcit deÞcit between little Effect in of the Anagrus study wk) Daane Al-Dawood nymphs deÞcits, a al. a spp. much Fig. Costello Costello by variation effect entire difference versus of 2009), the found 6. spp. treatments 11.86 : 10.80 : 12.85 : 13.66 : moderate and are berry 9.81 : 7.16 : 2.85 : 5.16 : 9.00 : 4.85 : Mean eggs/leaf (Trichilo reduced same the in Mean lea

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