plant water stress, leaf temperature, and spider mite (acari: tetranychidae) outbreaks in california...

PLANTÐINSECT INTERACTIONS

Plant Water Stress, Leaf Temperature, and Spider Mite (Acari:Tetranychidae) Outbreaks in California Vineyards

MENELAOS C. STAVRINIDES,1,2,3 KENT M. DAANE,1 BRUCE D. LAMPINEN,4

AND NICHOLAS J. MILLS1

Environ. Entomol. 39(4): 1232Ð1241 (2010); DOI: 10.1603/EN09288

ABSTRACT We evaluated the relationships between plant water status and leaf temperature, andbetween leaf temperature and spider mite (Acari: Tetranychidae) and predatory mite (Acari: Phyto-seiidae) populations in eight vineyards in California in 2006 and 2007. Temperature of south-facingleaves increased signiÞcantly by 0.8�C for every 1.0�C increase in ambient air temperature, and by 5.3�Cfor every one MPa drop in leaf water potential. Peak population densities of PaciÞc spider mite,Tetranychus pacificus McGregor, increased signiÞcantly with increasing frequency of leaf tempera-tures above 31�C. In contrast, peak population densities of Willamette spider mite, Eotetranychuswillamettei (McGregor), showed no relationship with the frequency of leaf temperatures above 31�C.This differential relationship between the two mite species and high leaf temperatures is consistentwith their upper thresholds for development, which are 40�C forT. pacificus and 31�C forE.willamettei,as identiÞed in a previous study. Predatory mite population densities showed no relationship with peakpopulation densities of either spider mite species during the analysis period, but decreased with thefrequency of leaf temperatures above 31�C. In addition, predatory mite population densities weresigniÞcantly higher on south-facing than interior leaves after adjusting for the effect of leaf temper-ature. These results help to explain why outbreaks of T. pacificus occur in warmer or water-stressedvineyards, whereas E. willamettei develops higher populations in cooler or well-irrigated vineyards.In addition, these results suggest that regulated deÞcit irrigation should be implemented with caution,especially in those vineyards with a high risk of T. pacificus outbreaks.

KEY WORDS spider mites, predatory mites, plant water stress, grape plants, leaf temperature

Plant water stress has long been associated with out-breaks of plant-feeding arthropods in nature (Mattsonand Haack 1987). The effects of water stress on ar-thropod populations may vary from positive to nega-tive depending on the intensity of the stress (English-Loeb 1990, Daane and Williams 2003, Huberty andDenno 2004) and the arthropod or plant species (War-ing and Cobb 1992). Although numerous studies havefocused on effects of water stress on plant-feedingarthropods through changes in nutrient availability(Holtzer et al. 1988a, Waring and Cobb 1992, Hubertyand Denno 2004), water stress can also affect herbi-vores and predators through changes in leaf microcli-mate (Holtzer et al. 1988b).

Small arthropods like spider mites (Acari: Tet-ranychidae) live and experience environmental con-ditions within the boundary layer of plant leaves, athin layer of relatively still air that immediately sur-rounds a leaf. Conditions within the boundary layer

can be quite different from ambient conditions (Bou-lard et al. 2002), and depend, among other factors, onthe rate of transpiration (Lambers et al. 2008). Inresponse to water stress, plants close their stomata,leading to a reduction in transpiration and a subse-quent increase in leaf temperature and a drop in rel-ative humidity within the boundary layer (Holtzer etal. 1988b). Increases in leaf temperature resultingfrom water stress have been suggested as a factorenhancing population growth of spider mite specieson almonds and maize (Toole et al. 1984, Holtzer et al.1988b, Oi et al. 1989).

Covering an area of 315,000 ha (NASS 2008), grapesare the most economically important crop in Califor-nia, with an annual value in excess of $3 billion (CDFA2007). Many California vineyards are managed underperiodic conditions of intense water stress during thegrowing season, a result of water scarcity or the in-tentional application of water stress in the form ofregulated deÞcit irrigation to improve fruit quality(Fereres and Soriano 2007). Grape plants are attackedby two spider mite species: the PaciÞc spider mite,Tetranychus pacificus McGregor, and the Willamettespider mite, Eotetranychus willamettei (McGregor)(Bentley et al. 2006). T. pacificus infestations are morefrequent in hot inland and coastal vineyards, whereas

1 Department of Environmental Science, Policy, and Management,Mulford Hall, University of California, Berkeley, CA 94720.

2 Agricultural Research Institute, 1516 Nicosia, Cyprus.3 Corresponding author: Agricultural Research Institute, 1516 Ni-

cosia, Cyprus (e-mail: [email protected]).4 Department of Plant Sciences, University of California, Davis, CA

95616.

0046-225X/10/1232Ð1241$04.00/0 � 2010 Entomological Society of America

E. willamettei causes more problems in cooler, coastalregions or earlier in the season in the inland valleys(Bentley et al. 2006). Although both mite species caninßict signiÞcant damage by reducing grape fruit sugarcontent and yield (Welter et al. 1989a, 1989b, 1991),T. pacificus is generally considered the most damagingof the two (Flaherty et al. 1992).

A recent study of the effects of temperature on thelife history parameters of the two mite species dem-onstrated thatT. pacificus is more heat tolerant with itsupper threshold for development at 40�C comparedwith 31�C for E. willamettei (Stavrinides 2009). Fieldobservations suggest that within the same region T.pacificus outbreaks are more common on water-stressed grape plants, whereas E. willamettei developshigher population densities in well-irrigated vine-yards. It is therefore possible that increases in leaftemperature because of water stress favor the devel-opment of T. pacificus overE.willamettei.Water stressmay also impact the effectiveness of predatory mites(Acari: Phytoseiidae) (Holtzer et al. 1988b, English-Loeb 1990). However, no studies have examined therelationship between water stress, leaf temperature,and populations of spider mites and predatory mites invineyards. Our aim in this study was to investigate therelationship between water stress and leaf tempera-ture in California vineyards and to identify the rela-tionship between leaf temperature and populationdensities of the two spider mites, T. pacificus and E.willamettei, and associated predatory mites. To ourknowledge, this is the Þrst study to address the effectsof water stress via leaf temperature on populations oftwo competing herbivores and their natural enemies.

Materials and Methods

Field Sites. We carried out observations in eightcommercial vineyards in Madera and Lodi Counties inCalifornia in 2006 and 2007. Vineyards in each countywere located within a 7-km radius. In 2006, observa-tions were made in two Madera vineyards planted toSyrah (M.S 06; planting distances were 3.3 � 2.1 mbetween and within rows, respectively) and FlameSeedless (M.FS 06; 3.6 � 2.4 m), and two Lodi vine-yards both planted to Zinfandel (L.Z1 06 and L.Z2 06;3.0 � 3.0 m). In 2007, observations were made in a newset of vineyards, two in Madera planted to ThompsonSeedless (M.TS1 07 and M.TS2 07; 3.6 � 2.3 m) andtwo inLodiplanted toPetiteSirah(L.PS107andL.PS207; 3.3 � 2.1 m). In general, the experimental plotswere located on the edge of each vineyard and con-sisted of 40 grape plants, eight in each of Þve neigh-boring rows. However, the experimental plots werelocated away from frequently traveled roads, andtherefore, dust deposition on the plants, which canfavor spider mite outbreaks (Flaherty et al. 1992), waslow. Most pesticide applications in the eight vineyardstargeted grape powdery mildew with sulfur and stro-bilurin/sterol inhibitor fungicides. In addition, M.S 06received an application of the insecticides methoxy-fenozide on 2 June 2006 and imidacloprid on 28 June2006; L. Z2 06 received an application of the insecti-

cide dinotefuran on 27 July 2006; and L.PS1 07 re-ceived an application of imidacloprid on 30 June 2007.No acaricide applications were carried out in the ex-perimental plots. The irrigation schedule in each vine-yard was determined by the grower based on wateravailability and commercial practices.Effects of Leaf Water Potential and Ambient Tem-perature on Leaf Temperature. Leaf water potentialmeasurements were recorded at approximatelymonthly intervals from May to September in 2006 and2007 using a plant pressure chamber (model 3005-1412, Soil Moisture Equipment, Goleta, CA). In eachvineyard, leaf water potential was measured between12:00 and 14:30 h from one south-facing, sun-exposedleaf per plant for 20 plants per vineyard; the third tothe seventh plant in rows 2Ð5. We bagged each leaf ina small plastic bag, cut the petiole within 3 s, and tooka reading of leaf water potential within 15 s of cuttingthe leaf (Williams and Araujo 2002). Just before cut-ting each leaf, we measured its temperature using aninfrared thermometer (Fluke 62 Mini IR thermome-ter, Fluke, Everett, WA). The infrared thermometerwas held perpendicularly to the center of the leaf ata distance of �25 cm to measure the temperature ofa 25-cm2 circular area of leaf surface. We used theinfrared thermometer to measure leaf temperatureduring leafwaterpotentialmeasurements, as itwasnotpractical to use thermocouples that were used forcontinuous measurements of leaf temperature. Ambi-ent temperature during the 30- to 40-min period ittook to measure leaf water potential and leaf temper-ature in each vineyard was obtained by averaging10-min measurements from a Hobo datalogger (HoboPro Series datalogger, Onset Computer, Pocasset,MA)thatwas shaded fromsunexposureby thecanopyand a cardboard cover.Effects of High Leaf Temperatures on Densities ofSpider Mites and Predatory Mites. Measurements ofLeaf Temperature Using Thermocouples.We measuredleaf temperature with copper-constantan thermocou-ples (thermocouple type: TT-T-36, Omega Engineer-ing, Stamford, CT). The tip of the thermocouple (4mm in length) was joined with a silver-bearing solder(64Ð035 E, Radio Shack, Fort Worth, TX). The lengthof the thermocouple wires did not exceed 7.5 m, andeight thermocouples were attached to a CR10 WP datalogger (Campbell ScientiÞc, Logan, UT) togetherwith an Omega zero reference (Omega CJ, cold junc-tioncompensator,OmegaEngineering, Stamford,CT)required for the calibration of thermocouple measure-ments. The data logger recorded leaf temperatureevery 10 min and stored temperature averages over90-min periods throughout the season.

We attached thermocouples to the underside of onesouth-facing and one interior leaf on each of fourplants, the third to the sixth plant in the third of theÞve rows. The thermocouple was attached to theleaves using a red plastic double-prong hair clip(Magic Collection, Bee Sales, Chicago, IL; pronglength 3.2 cm and width 4 mm) from which both sidesof the right prong were removed to form a single-prong clip. The thermocouple was securely attached

August 2010 STAVRINIDES ET AL.: SPIDER MITE RESPONSE TO WATER STRESS 1233

to the lower prong with a piece of beige soft Velcrotape (Stickyback, Velcro, Manchester, NH) 4 mm inwidth and 20 mm in length such that it protrudedthrough a small hole in the tape located 7 mm awayfrom the tip of the prong. The upper prong was alsocovered with Velcro tape. We attached the hair clipsonto grape leaves with the thermocouple tips in fullcontact with the lower surface of the leaf close to itscenter and at least 10 mm away from leaf veins. Ther-mocouples were installed on uninfested leaves onlyand were moved to new uninfested leaves as soon asany spider mites were detected, as both T. pacificusandE.willamettei reduce stomatal conductance (Wel-ter et al. 1989a), which could inßuence leaf temper-ature. In general, stomatal conductance of uninfestedleaves located adjacent to infested leaves is not sig-niÞcantly different from that of control leaves on un-infested grape plants (Welter et al. 1989a). The ther-mocouple wires were attached to the petioles of theleaves with electrical tape, and the weight of a ther-mocouple clip plus 25 cm of wire (1.2 g) had minimaleffect on leaf movement.Estimation of Mite Densities. To determine the re-

lationship between leaf temperature and spider mitepopulations, mite densities were measured every 2 wkduring the growing season. On each sample date, wecollected two south-facing and two interior leavesfrom the four thermocouple-equipped plants in eachvineyard, and counted all mobile stages of plant-feed-ing and predatory mites under a binocular micro-scope. We sampled both south-facing and interiorleaves, as the two mite species differ in their within-plant distribution, with E. willamettei preferring inte-rior over south-facing leaves and T. pacificus prefer-ring south-facing over interior leaves (Hanna et al.1996). Leaves were collected from the mid length ofshoots, as these tend to have the highest densities ofbothT. pacificus andE.willamettei (Hanna et al. 1996).The leaves were stored in a refrigerator at 4�C untilmites were counted. Spider mites were identiÞed tospecies following descriptions in Flaherty et al.(1992).

In 2006, we counted mites on whole leaves for theMadera vineyards and up to the Þrst week of Septem-ber in the two Lodi vineyards. After the Þrst week ofSeptember 2006 for the two Lodi vineyards and in2007, we counted mites on a circular area of 27 cm2 oneach leaf placed centrally over the main vein such thatthe perimeter of the circle reached the petiole. Thelength of each leaf (from petiole to leaf tip) used in thewhole leaf mite counts was recorded to estimate leafarea and express mite densities per leaf as number ofmites per cm2. We calibrated the linear relationshipbetween leaf length and leaf area (measured using thesoftware SigmaScan Pro v.4 [Jandel ScientiÞc Soft-ware, San Rafael, CA]) using 30 leaves for each of thethree varieties sampled in 2006.Predatory Mite Species Composition. Adult female

predatory mites were collected for identiÞcation fromtwo interior, south- and north-facing leaves from 12plants in the experimental plots of each vineyard onone sample date when average predatory mite densi-

ties peaked during the season, with the exception ofM.S 06, in which samples were collected at the thirdhighest density. These 12 plants included the fourplants that we monitored with thermocouples and aset of four plants on each of the two neighboring rows.Leaves were sampled, as described previously. Foreach vineyard, up to 16 adult females were identiÞedto species following Chant and McMurtry (2007) anda key to the species of phytoseiid mites on crop plantsin California that is currently under development (E.Grafton-Cardwell and J. McMurtry, personal commu-nication). Voucher specimens have been placed at theEssig Museum of Entomology of the University ofCalifornia, Berkeley.Statistical Analyses. A linear mixed effects model

was used to evaluate the inßuence of ambient tem-perature and leaf water potential on the leaf temper-atures measured with the infrared thermometer. Am-bient temperature and leaf water potential were theÞxed effects, and vineyard was incorporated as a ran-dom effect to account for repeated measurements ofleaf temperature and leaf water potential within eachvineyard. As described by Pinheiro et al. (2008), themodel was Þtted to the data using the lme function andtreatment contrasts in the package nlme of the statis-tical software R v. 2.7.1 (R Core Development Team2008).

We used a paired t test to compare average leaftemperature measurements recorded with the infra-red thermometer during leaf water potential evalua-tion in each vineyard to measurements recorded withthermocouples during the equivalent 90-min period.Thermocouple temperature measurements werebased on average measurements on one south-facingleaf per plant for the four thermocouple-equippedplants per vineyard. Infrared temperature measure-ments were based on average measurements on onesouth-facing leaf per plant for the same four thermo-couple-equipped plants.

We estimated linear regressions between leaflength and leaf area using the function “lm” in the statspackage of R v. 2.7.1.

To analyze the inßuence of high leaf temperatureson mite densities, we used a weighted mean based onmite densities for the three sample dates during the4-wk period leading up to peak phytophagous mitedensities in each vineyard. The weighted mean cor-rected for variation in the intervals between sampledates (13Ð15 d) and was estimated as follows: x� �[{(s1 � s2) � t1}/{2 � (t1 � t2)}] � [{(s2 � s3) �t2}/{2 � (t1 � t2)}], where si is mean mite density per

150 cm2 (an average-sized grape leaf) for the ith of thethree samples, and ti is the interval in days betweensamples si and si�1. High leaf temperature was repre-sented as the average number of degree hours above31�C per day monitored from the four thermocoupleson interior and south-facing leaves during the same4-wk periods leading up to peak phytophagous mitedensities. Degree hours above 31�C were calculated asthe mean number of hours per day that leaf temper-ature exceeded 31�C during the 4-wk analysis period.

1234 ENVIRONMENTAL ENTOMOLOGY Vol. 39, no. 4

We chose 31�C because it is the upper threshold tem-perature for E. willamettei development, but muchlower than the upper threshold for T. pacificus devel-opment (40�C) (Stavrinides 2009). Average degreehours �31�C per day were based on measurementsfrom at least three working thermocouples per leafposition, with the exception of L.PS2 07 between 23July and 6 August 2007 when data from only twothermocouples were available.

As mite densities could also be inßuenced by severalother Þxed and random effects in addition to leaftemperature, the relationship between mite densitiesand degree hours �31�C per day was analyzed usinga linear mixed effects model in the nlme package of Rv. 2.7.1 using the function lme and treatment contrasts.For each spider mite species, leaf position, mean com-petitor density, and mean predatory mite density wereincluded in the model as additional Þxed effects, andvineyard as a random effect. A similar model was usedfor the predatory mites for the 4-wk period leading upto peak phytophagous mite densities with degreehours �31�C per day, leaf position, mean T. pacificus,and mean E. willamettei densities as the Þxed effects,and vineyard as the random effect. Only main effectswere included in the analysis, as sample size limita-tions did not allow us to test for interactions. ThesigniÞcance of each factor was assessed with a mar-ginal F test that evaluated its importance in the pres-ence of all other factors in the model (Pinheiro andBates 2000). We reportP values for the simplest modelin which a factor was either retained or removedduring the process of model simpliÞcation. Both theweighted mean mite densities and degree hours�31�C per day were ln (x � 1) transformed for allanalyses. Diagnostic plots of Þtted values against stan-dardized residuals and normal probability plots for theÞxed and random effects for all models showed nomajor departures from the assumptions of normalityand variance homogeneity.

Results

Effects of Leaf Water Potential and Ambient Tem-perature on Leaf Temperature. Both ambient tem-perature and leaf water potential had a signiÞcantinßuence on leaf temperature measured with the in-frared thermometer (Table 1 and Fig. 1). The param-eter estimates from the lme model suggested that forevery 1�C increase in ambient temperature, the tem-perature of south-facing leaves would increase by

Table 1. Summary statistics for linear mixed effects models

Response/explanatoryvariables

Parameterestimate, 95% CI

F value P valueStandard deviation, 95% CI

Random effect (vineyard) Error

a) Leaf tempAmbient temp 0.75, 0.52Ð0.98 45.71; df � 1, 27 �0.001

0.81, 0.22Ð3.06 2.01, 1.54Ð2.62Leaf water potential 5.26, 0.76Ð9.75 5.76; df � 1, 27 0.02

b) T. pacificus densityDegree hr �31�C 1.67, 0.56Ð2.79 14.86; df � 1, 5 0.01

1.06, 0.57Ð2.00 0.54, 0.30Ð1.00Leaf position NS 0.18; df � 1, 2 0.72E. willamettei density NS 0.66; df � 1, 3 0.48Predatory mite density NS 1.37; df � 1, 4 0.31

c) E. willamettei densityDegree hr �31�C NS 1.60; df � 1, 4 0.27

Ñ ÑLeaf position NS 1.25; df � 1, 5 0.31T. pacificus density NS 0.28; df � 1, 2 0.65Predatory mite density NS 5.74; df � 1, 3 0.10

d) Predatory mite densityDegree hr �31�C �0.68, �0.94-�0.42 31.29; df � 1, 16 �0.001

0.05, 3.1 � 10�7Ð8.4 � 103 0.38, 0.27Ð0.54Leaf position 0.48, 0.13Ð0.82 8.58; df � 1, 16 0.01T. pacificus density NS 0.13; df � 1, 14 0.72E. willamettei density NS 1.78; df � 1, 15 0.20

This table investigates the relationship between a) leaf temp, ambient temp, and leaf water potential; b)T. pacificusdensity, degree hr �31�C,leaf position, E. willamettei density, and predatory mite density; c) E. willamettei density, degree hr �31�C, leaf position, T. pacificus density,and predatory mite density; and d) predatory mite density, degree hr �31�C, leaf position, T. pacificus density, and E. willamettei density.

Fig. 1. Relationshipbetween leaf temperature, leafwaterpotential, and ambient temperature for eight vineyards inMadera and Lodi. Each point represents average measure-ments of leaf temperature and leaf water potential from 20plants per vineyard, and ambient temperature recorded by aHobo data logger, at approximately monthly intervals fromMay to September during the 2006 and 2007 growing seasons.The mesh plot represents model predictions of leaf temper-ature based on model parameters for the Þxed effects of leafwater potential and leaf temperature presented in Table 1.


0.75�C, and for every one MPa decrease in leaf waterpotential, the temperature of south-facing leaveswould increase by 5.26�C (Table 1). The average mea-surements of the leaf temperature of south-facingleaves using the infrared thermometer (34.1 0.7�C,mean 1 SE, n � 35) did not differ signiÞcantly(paired t test, t � 1.94, df � 34, P � 0.06) from thoserecorded by the thermocouples (34.6 0.7�C,n� 35).

Thermocouple records showed that the tempera-ture of south-facing leaves was higher than that ofinterior leaves from noon to approximately 18:00 h(Fig. 2), although actual differences varied betweenvineyards and between dates within vineyards (datanot shown).Effects of High Leaf Temperatures on Densities ofSpiderMites andPredatoryMites.Mite densities wereestimated from separate calibrations of the linear re-lationships between leaf length and leaf area for eachvariety. The results were as follows (estimate SE):M.S 06 (intercept � �70.70 12.41, slope � 18.32 1.34, F1,28 � 188.30, P � 0.001, r2 � 0.87), M.FS 06(intercept � �91.26 39.89, slope � 22.31 2.81,F1,28 �63.10, P� 0.001, r2 � 0.69), and L.Z2 06 (intercept ��73.33 22.52, slope � 21.25 1.83, F1,28 � 134.9, P�0.001, r2 � 0.83).

In general, populations of T. pacificus reachedhigher levels than those of E. willamettei, as indicatedby changes in mite abundance through time for inte-rior and south-facing leaves in each of the eight vine-yards (Figs. 3 and 4). In most cases, the increase in

Fig. 2. An example of the daily pattern of variation intemperature (mean SE, n � 4) of interior and south-facingleaves in theM.FS06vineyardoverconsecutive3d in July2006.

Fig. 3. Average mite densities (mean SE, n � 4) per leaf (150 cm2) for interior and south-facing leaves at biweeklyintervals through the 2006 season in four vineyards in Lodi and Madera. Note the different scales for spider mite densitiesin the Lodi versus Madera vineyards.


spider mite populations was followed by an increase inpopulations of predatory mites.

Degree hours �31�C had a signiÞcant positive in-ßuence on mean T. pacificus density during the 4-wkperiod leading up to peak T. pacificus abundance (Ta-ble 1 and Fig. 5A). Leaf position, mean E. willametteidensity, and mean predatory mite density were notsigniÞcant (Table 1). None of the Þxed effects had asigniÞcant inßuence on mean E. willamettei densityduring the 4-wk period leading up to peakE.willamet-tei abundance (Table 1 and Fig. 5B).

Degree hours �31�C had a signiÞcant negative in-ßuence on mean predatory mite density, and signiÞ-cantly more predatory mites were found on south-facing than interior leaves during the 4-wk periodleading up to peakT. pacificus andE.willamettei abun-dance (Table 1 and Fig. 5C). The inßuence of meanT. pacificus density and meanE. willamettei density onmean predatory mite density was not signiÞcant (Ta-ble 1). Model simpliÞcation for the predatory mitemodel resulted in large conÞdence intervals for thestandard deviation of the random effect (vineyard)(Table 1) that suggested a possible problem with

model speciÞcation (Pinheiro and Bates 2000). How-ever, thePvaluesandparameterestimates for theÞxedeffects of degree hours �31�C and leaf position thatwere retained in the simpliÞed model were similar tothose estimated in the full model that had reasonably-sized conÞdence intervals (0.02Ð1.26) for the standarddeviation of the random effect (0.17).PredatoryMite SpeciesComposition.Table 2 shows

the species composition of phytoseiid females col-lected from the eight vineyards. Galendromus occi-dentalis (Nesbitt) was among the most common spe-cies and was present in six of the eight vineyards.Other common species included Euseius quetzaliMc-Murtry and Metaseiulus flumenis (Chant), whereasEuseius hibisci (Chant), Euseius tularensis Congdon,and Metaseiulus citri (Garman and McGregor) wereless common (Table 2).

Discussion

We showed that both ambient temperature andwater stress play a signiÞcant role in inßuencing leaftemperature, as graphically described in Fig. 1. These

Fig. 4. Average mite densities (mean SE, n � 4) per leaf (150 cm2) for interior and south-facing leaves at biweeklyintervals through the 2007 season in four vineyards in Lodi and Madera. Note the different scale for spider mite densities inthe L.PS1 vineyard.


Þndings conÞrm previous studies that documented anincrease in leaf temperature in response towater stressin grape and other plants (Van Zyl 1986, Holtzer et al.1988b, Leinonen and Jones 2004). Although not stud-ied in this work, we expect that water stress would alsoresult in an increase in the temperature of interiorleaves (Holtzer et al. 1988a). However, the change intemperature of interior leaves would possibly be lessthan that of south-facing leaves at the same ambient

temperature because of the lower exposure of interiorleaves to solar radiation (Lambers et al. 2008).

Degree hours �31�C was the only variable mea-sured in the vineyards that had a signiÞcant effect onmean T. pacificus density (Fig. 5A). More speciÞcally,mean T. pacificus density showed a positive relation-ship with degree hours �31�C indicating that thisspecies beneÞts from higher leaf temperatures, as itsoptimum temperatures for development and upperdevelopment threshold are 33.4�C and 40.3�C, respec-tively (Stavrinides 2009). In contrast, mean E. wil-lamettei density showed no relationship with degreehours �31�C (Fig. 5B), nor with any of the othervariables measured. Temperatures above 31�C are notsuitable forE. willamettei development, as this specieshas an optimum temperature for development of26.1�C and an upper development threshold of 31�C(Stavrinides 2009). However, the range of degreehours �31�C observed may not have been highenough to generate a negative relationship with E.willamettei densities, as brief periods of high leaf tem-peratures are also associated with increases in min-imum and daily average temperatures that couldpositively inßuence the population growth of E.willamettei.

There was also considerable variability in mean E.willamettei density in relation to numbers of degreehours �31�C (Fig. 5B). The variability inE.willametteidensities may have resulted from differences in sus-ceptibility of the grape cultivars, which are more pro-nounced for E. willamettei than for T. pacificus forZinfandel and Thompson/Flame Seedless (English-Loeb et al. 1998). In addition, water stress not onlyincreases leaf temperature, but also decreases relativehumidity within the boundary layer of a leaf (Holtzeret al. 1988b), which can have nonlinear effects on mitemortality (Walzer et al. 2007). Furthermore, waterstress may affect the nutritional quality of plants as aresult of changes in the concentration of nitrogen andother nutrients (Holtzer et al. 1988a, Waring and Cobb1992, Huberty and Denno 2004). Different species ofmites respond differentially to changes in plant nu-tritional quality (Waring and Cobb 1992) and relativehumidity (Holtzer et al. 1988b, Mangini and Hain1991). Therefore, these two factors are worthy ofgreater consideration in future studies aimed at a bet-ter understanding of the effects of water stress onmites and insect pests.

Fig. 5. Mean mite densities and degree hours �31�C perday (transformed) for interior and south-facing leaves (150cm2) during the 4 wk leading up to peak abundance of eachspider mite species for (A) T. pacificus, (B) E. willamettei,and (C) predatory mites. Note that for (C) data are includedfor the 4 wk leading up to peak abundance of bothT. pacificusand E. willamettei in each vineyard. Fitted lines are based onsigniÞcant parameters only; degree hours �31�C forT. pacifi-cus, and degree hours �31�C and leaf position for predatorymites (Table 1).

Table 2. Species composition of predatory mites from eight vineyards in Lodi and Madera during the 2006 and 2007 growing seasons

Vineyard Sampling date No. identiÞed Species composition

L.Z1 06 16 Oct. 2006 14 100% Galendromus occidentalisL.Z2 06 16 Oct. 2006 15 73% Metaseiulus flumenis, 27% G. occidentalisM.FS 06 6 Sept. 2006 3 100% G. occidentalisM.S 06 19 Sept. 2006 6 67% G. occidentalis, 16.5% Euseius hibisci,

16.5% M. flumenisL.PS1 07 4 Sept. 2007 16 94% Euseius quetzali, 6% Metaseiulus citriL.PS2 07 20 Aug. 2007 13 77% G. occidentalis, 23% E. quetzaliM.TS1 07 26 June 2007 3 67% E. quetzali, 33% Euseius tularensisM.TS2 07 26 June 2007 1 100% G. occidentalis


The increase in leaf temperature with both ambienttemperature and water stress (Fig. 1) and the positiverelationship between T. pacificus populations and leaftemperature (Fig. 5A) are in agreement with Þeldobservations linking T. pacificus outbreaks to warmeror water-stressed vineyards. Furthermore, this studyprovides a better understanding of the ability of E.willamettei to build higher populations in cooler orwell-irrigated vineyards, given its lower tolerance forhigh temperatures (Stavrinides 2009). Previous stud-ies have also reported increases in spider mite popu-lations as a result of increased leaf temperature. Hannaet al. (1997b) proposed that higher leaf temperaturesmay be one of the reasons for a greater abundance ofT. pacificus on low versus high vigor grape plants.Similarly, Oi et al. (1989) demonstrated that water-stressed almond trees had an average leaf temperature2.1�C higher than nonstressed trees, and that this dif-ference in temperature led to faster development ofT.pacificus. Furthermore, using a simulation model,Toole et al. (1984) showed that increases in leaf tem-perature because of water stress were the main reasonfor the rapid increase of the Banks grass mite (Olig-onychuspratensis) on water-stressed maize plants. OurstudyconÞrms theÞndingsofprevious studies andalsoshows that the effects of leaf water stress via leaftemperature may depend on the species of the her-bivore as T. pacificus densities increased with leaftemperature, unlike densities of E. willamettei (Fig. 5,A and B).

We found no effect of mean predatory mite densityon the relationship between either T. pacificus or E.willamettei density and leaf temperature (number ofdegree hours �31�C). The population densities ofpredatory mites remained generally low during the4-wk period, leading up to peak T. pacificus or E.willamettei abundance in each of the vineyards (Figs.3 and 4), and this may account for their lack of con-founding inßuence in this study. However, in manyvineyards, the increase in spider mite densities wasfollowed by an increase in predatory mite densities,showing a time lag that is typical of prey-predatorinteractions (Figs. 3 and 4). Whereas a time seriesanalysis (Lingeman and van de Klashorst 1992) couldbetter characterize the relationship between predatorand prey population densities in these vineyards, it isbeyond the scope of the current study.

In addition, we detected no relationship betweenE.willamettei density and T. pacificus density in either ofthe mixed effects models for the two spider mites.Studies in the 1990s had shown, however, that undercertain conditions either species can induce defensesin grape plants against its competitor (e.g., English-Loeb et al. 1998, Hougen-Eitzman and Karban 1995,Hanna et al. 1997a, Karban et al. 1997). The low pop-ulation densities of spider mites in some vineyards(Figs. 3 and 4) together with differences betweenvineyards in factors inßuencing defense induction,such as the timing of infestation and grape variety(English-Loeb et al. 1998), spider mite populationdensities (Hanna et al. 1997a), and possibly temper-ature (Yang et al. 2007) may have prevented us from

establishing a negative association between the twospider mites. Further studies on the effects of leaftemperature and water stress on the ability of eitherspider mite to induce defenses against its competitorwould be needed to clarify this issue.

Hanna et al. (1996) showed that T. pacificus devel-ops higher populations on south-facing than interiorleaves, whereas E. willamettei populations are usuallyhigher on interior leaves. The same pattern was evi-dent in our study for mean mite densities during the4-wk period leading up to peak abundance of eitherspider mite (Figs. 3 and 4). Furthermore, removingdegree hours �31�C from the mixed effects modelsresulted in leaf position being signiÞcant for mean T.pacificus density (F � 11.55; df � 1, 5; P � 0.02),although not signiÞcant for E. willamettei (F � 1.25;df � 1, 5; P� 0.31). Although in some vineyards therewas a trend of higher mean E. willamettei densities oninterior than south-facing leaves (Figs. 3 and 4), thesedifferences may have been too low overall to be sta-tistically signiÞcant. Nonetheless, the higher temper-ature on south-facing than interior leaves (Fig. 2)together with the higher temperature tolerance of T.pacificus compared with E. willamettei (Stavrinides2009) could be the reason for the differential distri-bution of the two spider mites on grape plants.

Water stress may also impact the effectiveness ofpredatory mites (Holtzer et al. 1988b, English-Loeb1990). Our analysis on the impact of different variableson mean predatory mite density suggested a signiÞ-cant effect of degree hours �31�C and leaf position,but no effect of mean T. pacificus or E. willametteidensities (Table 1 and Fig. 5C). Spider mite:predatorymite ratios were generally high during the 4-wk periodleading up to peak spider mite abundance, and there-fore, spider mites may have not been a limiting factorfor predatory mite population growth (Figs. 3 and 4).Furthermore, some of the predatory mites present inhigh numbers in our samples, such as species in thegenus Euseius (Table 2), can feed and reproduce onpollen (McMurtry and Croft 1997), and therefore,their populations may not be coupled strongly withspider mite populations (see, for example, vineyardL.PS1 07 in Fig. 4). The data on species compositionof predatory mites (Table 2) are based on a sampletaken toward theendof the season, and therefore,maynot be representative of predatory mite speciespresent earlier in the season (Prischmann et al. 2005).WhereasG. occidentalis has been considered the mostimportant predatory mite in vineyards (Flaherty et al.1992), our results (Table 2) together with other on-going studies (L. Varela, personal communication)suggest that other species may also be important forspider mite biological control.

Mean predatory mite densities followed a negativerelationship with degree hours �31�C (Fig. 5C). Hightemperatures can negatively affect predatory miteseither directly by reducing their intrinsic rate of in-crease (Stavrinides 2009), or indirectly by alteringtheir dispersal and foraging behavior (Berry andHoltzer 1990; Skirvin and Fenlon 2003a, 2003b). Thus,the lower mean predatory mite densities observed on


leaves with higher degree hours �31�C in this study(Fig. 5C) may have resulted from reduced populationgrowth at higher temperatures (Stavrinides 2009), orfrom behavioral avoidance of leaves with high tem-peratures, as some predatory mites are also known toavoid intense light (Weintraub et al. 2007). An addi-tional factor that may have negatively affected pred-atory mite populations is the lower relative humiditywithin the leaf boundary layer (Walzer et al. 2007)caused by reduced transpiration of water-stressedplants (Holtzer et al. 1988b).

Another factor that affected mean predatory mitedensity was leaf position, with south-facing leaves ac-cumulating greater predatory mite densities than in-terior leaves (Fig. 5C). Differential distribution ofpredatory mites within plants has been shown forvarious species (Weintraub et al. 2007, Fitzgerald et al.2008, Onzo et al. 2009). The greater abundance ofpredatory mites on south-facing than interior leaves inthis study most likely reßects their accumulation inareas with higher availability of food resources (Mc-Murtry and Croft 1997), such as spider mites andpollen, but further studies would be required to fullyunderstand this pattern.

In conclusion, this study has demonstrated that wa-ter stress leads to increased leaf temperatures (VanZyl 1986, Holtzer et al. 1988b, Leinonen and Jones2004), and that high leaf temperatures are associatedwith increased densities of T. pacificus, reduced den-sities of predatory mites, and no apparent inßuence ondensities of E. willamettei. These Þeld observationstogether with those from a previous laboratory studyon the inßuence of temperature on development of T.pacificus (Stavrinides 2009) demonstrate a link be-tween T. pacificus outbreaks and warmer or water-stressed vineyards. Consequently, regulated deÞcit ir-rigation should be applied with caution, especially inthose vineyards with a high risk of T. pacificus out-breaks.

Acknowledgments

We thank Margarita Hadjistylli, Jennifer King, RickyLara, and the Daane laboratory at Kearney AgriculturalCenter for help with Þeld and laboratory observations.Sam Metcalf of University of California, Davis, helped withthermocouple setup for measuring leaf temperature. Wealso thank Greg Burns, Walt Cranston, Samuel Curran, PhilHagopian, and Bruce Mettler, who kindly allowed us to usetheir vineyards for this study. This work was supported bya scholarship to M.C.S. from the Cyprus-America Schol-arship program administered by the Fulbright Commissionin Cyprus. Funding was also provided by the AmericanVineyard Foundation, the Viticulture Consortium West,the California Raisin Marketing Board, and the MargaretC. Walker Fund for teaching and research in systematicentomology.

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Received 5 October 2009; accepted 31 March 2010.


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