PEsr MANAGEMENT AND SAMPLING

Overwintering and Comparative Sampling of Neoseiulus fallacis(Acari: Phytoseiidae) on Ornamental Nursery Plants

P. D.PRATI1AND B. A. CRO~

Environ. Entomol. 29(5): 1034-1040 (2000)ABSTRACT The predatory mite Neoseiulus fallacis (Gannan) is an important biological controlagent of spider mites in many agroecosystems, including ornamental nurseries. In this study, samplingmethods, tendencies to overwinter among a range of plant types, and the effect of winter protectivepractices were assessed for N.fallacis females. Ten spider mite-infested plant species representinga range of five plant types (conifer, shade tree, evergreen shrub, deciduous shrub, herbaceousperennial) were inoculated with 100 adult female N. fallacis in late autumn. Early the followingspring, N. fallacis was extracted from each plant species by either washing plant parts (leaves,branches, trunks-crowns) in 70% ethanol and filtering contents or placing plant parts into separateBerlese funnels for 5 d. The washing method extracted more N.fallacisthan the funnel method. Whencomparing overwintering among a range of plant types, higher densities of N. fallacis were extractedfrom conifers> evergreen shrubs> herbaceous perennials = deciduous shrubs = shade trees. Withrespect to overwintering location of N. fallacis within plants, higher densities of N. fallacis wererecovered on leaves than trunks-crowns; branches were intermediate. Densities of N. fallacis werepositively correlated with those of their spider mite prey. Higher densities of N. fallacis werecollected from plants that were held in a greenhouse versus those left unprotected or under a sheetof polyethylene plastic. Manipulating overwintering sites for the conservation of phytoseiid naturalenemies is discussed.

KEY WORDS Neoseiulus fallacis, diapause, Tetranychidae, biological control

PREDATORYMITESIN the family Phytoseiidae are impor-

tant biological control agents of plant-inhabiting pestmites (Helle and Sabelis 1985). Among the Phytosei-idae, only the adult female enters diapause, which intemperate zones is manifested as an arrestment inactivity and reproduction (Overmeer 1985). Overwin-tering sites sought out by diapausing female phyto-seiids within plant systems have been assessed often.In early studies, Chant (1959) suggested that over-wintering females do not fallwith leaves in autumn butmove to sites such as splintered twigs, crevices, orunder bark. Putman (1959) collected phytoseiids frompeach orchards and found that overwintering sitesvaried among species, ranging from orchard weeds tomany locations on trees. Overmeer (1985) suggestedthat most phytoseiid species show a locational pref-erence for overwintering on a plant. For example,Typhlodromus pomi (Parrot) and Amblyseius umbrati-CU8(Chant) preferred small twigs (Kinsley and Swift1971), whereas Typhlodromus bakeri (Garman) andTyphlodromus pyri Scheuten were found primarilyunder apple trunk bark.

In this study, we sought to assess tendencies ofNeoseiulus fallacis (Garman) to overwinter among arange of ornamental plants in temperate regions ofwestern Oregon, U.S. This species is distributed

I USDA-ARS. 3205 College Avenue, Fl Lauderdale, FL 33314-2 Department of Entomology, Oregon State University, Corvallis,

OR 97331-2907.

throughout North America and is an important pred-ator of spider mites on many plant types (McMurtryand Croft 1997). In Oregon, inoculative releases of N.fallaci.s are commonly made to reduce spider mites inapple, com, hops, strawberry, peppermint, and, mostrecently, nursery plants (Strong and Croft 1995,Mor-ris et al. 1996, Croft and Coop 1998, Pratt and Croft1998). In Michigan under severe winter conditions,Croft and McGroarty (1977) found that N. fallaci.soverwintered mainly in ground cover of apple or-chards. In New York apple orchards under similarconditions, Nyrop et al. (1994) found that N.fallaci.soverwintered on apple twigs and occasionally inground cover. Morris et al. (1996) found that in moremild, arid areas of Oregon, N.fallaci.s overwintered onpeppermint leaves in early winter, but as temperaturesdecreased the adult females either moved to or onlysurvived in debris near the soil surface.

Knowledge concerning the overwintering behav-iors of predator and prey mites is integral to devel-oping integrated pest management (IPM) strategiesboth within a single season and over several years(Hoy and Flaherty 1970). There are no studies thatcharacterize the suitability of plant types for overwin-tering of phytoseiids under similar environmental con-ditions. Many plants occur in multi cropping systemssuch as ornamental nurseries, and certain types (e.g.,conifers, herbaceous perennials) may provide hetteroverwintering sites than others. In addition, variouscultural practices are employed to minimize plant

October 2000 fun AND CROFT; OvERWJN1ERING OF N. faUacis 1035

damage from extremes of temperature, wind, and pre-cipitation. For instance, ornamentals may be placedunder protective plastic sheets, held in greenhouses,or left out of doors (unprotected) during winter.Therefore, the four specific objectives of our studywere as follows: (1) to compare methods of samplingornamental plants for overwintering N.fallacis, (2) tomeasure frequency of overwintering by N. fallacisamong 10 species of plants that included five generaltypes, (3) to determine overwintering location of N.fallacis within a plant, and (4) to compare effects ofplastic coverings, unheated greenhouses and unpro-tected plants on overwintering success of N. fallacis.

Materials and Methods

Ten ornamental species (with eight replicate plantseach) ranging from coniferous to herbaceous peren-nials (Table 1) were obtained from nurseries on 1October 1997 and placed into a greenhouse (10 by10 m) at 22:18 :!::SOC,75 :!::10%RH, and a photoperiodof 16:8 (L:D) h. All plants were potted in plasticcontainers and watered daily. The spider mites Olig-onychus iUicis (McGregor), O. ununguis (Jacobi), orTetranychus urlicae Koch were collected from field-grown ornamental plants and reared at 25°C,60 :!::10%RH, and a photoperiod of 16:8 (L:D) h for at least onegeneration and then inoculated into each test plantwithin the greenhouse on 2 October 1997 (Table 1).Specimens of N.fallacis, in an inert granular medium,were provided by Biotactics (Grand Terrace, CA).Upon arrival, a subsample of the predatory mites wereidentified to species (Schuster and Pritchard 1963)and allowed to disperse onto lima bean leaves infestedwith T. urlicae. Bean leaves were scanned using a 40Xmicroscope to quantify densities of N. fallacis, andmultiple leaves containing 100N.fallacis adult femaleswere inoculated into each test plant in the greenhouseon 8 October 1997. To evaluate mite densities afterrelease of N. faUacis, we reviewed (without removalfrom the plant) five leaves or branches (Table 1) perreplicate of each plant species with an optical visor atlOX magnification every 7 d for 2 wk. To conditionmites to external weather and possibly induce dia-pause, we incrementally decreased daylength by 2 hevery 10 d and adjusted temperatures within thegreenhouse until they approached those of the exter-nal environment. On 3 November 1997, we removedthe test plants from the greenhouse and randomlyplaced them outside on a gravel substrate (bed) with""1 m spaces between plants. Plants were wateredbelow the foliage as needed. We also monitored dailyhigh and low temperatures and rainfall during Octo-ber-February 1997-98 to compare with the prior 36yearly averages.

The following two methods of extracting overwin-tering phytoseiids from plant material were compared:(1) collecting mites from plant materials placed inBerlese funnels (the funnel method) or 2) washingplant materials with ethanol and collecting predatorsthrough filtration (the washing method). On 15 Feb-ruary we extracted N. fallacis from four randomly

selected replicates of each plant species by placing theplant parts, as described in Table 1,or the top 3 cm ofsoil and associated litter into separate Berlese funnelsfor 5 d under a 4O-Wlight bulb (Morris et al. 1996).Temperatures were 25 :!::2°C within the funnel Weplaced a bouquet of lima bean plants within the baseof each funnel, with stems resting in a 0.5-liter jar filledwith water. Bean leaves were infested with T. urticaeand the leaves were arranged to thoroughly cover thefunnel base to prevent predators from falling into thewater. Bean leaves were scanned every 24 h and eachphytoseiid mite was mounted on a glass slide for iden-tification under a phase-contrast microscope at 200Xmagnification.

The plant washing method also was evaluated on 15February 1998.The method entailed placing the pre-viously mentioned plant parts (Table 1), but not soiland associated litter, in separate I-liter jars and adding300 ml of 70% ethanol (Zacharda 1989, Calkin 1991).Lids were placed on jars and shaken manually for 30 s,left to rest for 1 min, and then shaken again for 30 s.Plant material was removed with forceps and slowlyrinsed with 70%ethanol over the jars. The ethanol andassociated contents were poured into a Whatman #4filter paper funnel, gravity filtrated, and scanned formites within 5 min under a binocular microscope at40X magnification. All phytoseiid mites washed fromplant parts were mounted on glass slides for identifi-cation. Spider mites washed from plants also wererecorded.

To measure the effect of cultural practices on over-wintering N. fallacis, we collected 15 plants of eitherViburnum dtwidii or Piceaglauca 'Conica' on 3 Octo-ber 1998.Plant size and selection, inoculation of spidermites and predators, identification of predators, andconditioning in the greenhouse were performed asbefore. Plants were removed from the greenhouse on5 November 1998, and five plants of each ornamentalspecies were randomly placed in either an unheatedgreenhouse, left unprotected (as in the previous test) ,or placed under a sheet of protective plastic. Thegreenhouse consisted of an unlighted polyethylene-enclosed structure (15 by 7 m) with a shade clothdrawn over the roof to reduce solar radiation. Unpro-tected plants were placed 10 m from the greenhousein an outdoor nursery bed exactly as in 1997-1998 tests.The protective plastic treatment was similar to theunprotected treatment except that a 3 mil white plasticsheet was drawn over the plants and rested on foliage.The plastic sheet had O.5-cmholes spaced 0.5 m apartand was held secure with 2O-cmstakes at the cornersof the plastic. As is consistent with nursery practices,the plastic was removed on days when temperaturesexceeded 20°C but was replaced each night. In allcases, ornamental plants were placed directly on agravel bed and irrigated below foliage once a week. Inaddition, maximum and minimum air temperatureswere recorded three times a week in the greenhouse,under the plastic and near unprotected plants. Onlythe washing method was used to extract N.fallacisfrom overwintering sites in this test.

......o~Q)

Plant parts used for extraction of N.fallacis; L, leaves; B, branches; T, trunk; C, crown; (S), soil and associated litter, soil was only used in the funnel extraction method. Means followed by different lettersare significant at a = 0.05 (Tukey HSD)..Plastic plant container (pot) size in liters.

b Average height (in cm) of plants (n =8).C Average diameter (in centimeters) of plants at widest point of canopy (n =8).d Average number of N. fallacis extracted with the funnel method." Average number of N.fallacis extracted with the alcohol wash method.

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Table 1. Overwintering or N. follae;. on 10 ornamental pIanu with eomparloon or oamp\ing methodo

OrnamentalSpider mite Predator densities

Plant type plant partsContainer Plant htb Plant diamc Pest mite densities on: Avg (SD)

species sized10 Oct. 15 Feb. Washin Funnel"

Piceaglauca Conifer B, T, (S) 3.8 48 23 Ollgonychus ununguls 25.3 34.3 19.75 (4.43)a 13.00 (4.97)a'Conica'

'Ihuja oocidentalis Conifer B, T, (S) 3.8 42 23 Ollgonychus ununguls 18.5 15.1 10.75 (2.99)ab 6.50 (3.70)ab i'Pyramidalis'Viburnum davidii Evergreen shrub L, B, T, (S) 3.8 46 43 Tetranychus urticae 37.1 2.7 7.75 (2.63)ab 5.75 (2.75)abllex crenota Evergreen shrub L, B, T, (S) 3.8 66 48 Tetranychus urticae 8.5 1.26 5.25 (4.19)b 2.25 (O.58)bc

'Convexa'

IRhododendron Evergreen shrub L, B, T, (S) 3.8 53 46 Ollgonychus iUicIs 16.2 10.1 3.75 (2.22)bc 3.00 (2.16)bc

'Ana Kruschke'Hernerocxdllshybrid Herbaceous perennial C, (S) 3.8 71 56 Tetranychus urticae 35.7 0 1.00 (1.15)cd 0.00 (O.OO)d

'Mary Todd'Viburnum opulus Deciduous shrub B, T, (S) 3.8 41 25 Tetranychus urticae 10.2 0 0.75 (0.96)cd 0.25 (0.50)00

'Sterile'Acer %freemanii Shade tree B, T, (S) 18.9 229 76 Tetranychus urticae 18.3 0 0.25 (O.50)d 0.50 (1.OO)cd

a'Jeffersred'Euonyrnous alatus Deciduous shrub B, T, (S) 3.8 53 36 Tetranychus urticae 22.7 0 0.25 (O.50)d 0.25 (0.50)00

'Compacta'Corylus tlVellana Deciduous shrub B, T, (S) 3.8 102 30 Tetranychus urticae 11.5 0 0.00 (o.OO)d 0.25 (O.50)cd

'Contorta'P<O.OOOI P<O.OOOI

October 2000 PRATr AND CROFT: OvmWlN'lERING OF N. fa1lacis 1037

Statistical Analyses. To compare sampling methods,we pooled all within-plant samples and log (x + 1)transformed the number of overwintering N. fa1lacisextracted from each method. We then used a pairedt-test to compare sampling methods. To graphicallycompare methods, we subtracted the densities ofpredatory mites recovered using the funnel methodfrom those of the washing method, and regressed thedifference on washing values. To compare overwin-tering N.fallacis among the 10plant species or amongprotective cultural practices, we log(x + 1) trans-formed all values and used analysis of variance and theTukey honestly significant difference (HSD) to dis-tinguish differences among treatments. Simple linearregression was used to estimate the correlation ofspider and predaceous mite densities collected on 15February. When comparing N. fallacis on differentplant types or locations within a plant, conventionalparametric statistics are not appropriate because ofunequal sample sizes and unknown underlying distri-butions of mites. One alternative to parametric tests isa randomization test, which Manly (1991) found morepowerful than other nonparametric tests. Therefore,using data from the washing technique only, we ran-domly reordered the numbers of N. fallacis foundwithin each plant type or plant part 1,000 times andacquired the mean and standard deviation for respec-tive distributions. We then compared distributions ofplant types and among plant parts with a two-samplet-test for means (Ramsey and Schafer 1997). We usedthe Sidak inequality formula to maintain a 0.05 exper-iment-wise a level when comparing overwinteringwithin and between plants (Jones 1984). Cautionshould be used when drawing inferences from statis-tical comparisons among plants because data were notstandardized to adjust for differences in plant size,morphology, humidity within plant canopies, or otherparameters that may influence overwintering.

Results and Discussion

Winter temperatures for the study period fell withinone standard deviation of the average of the previous36 yr in the Willamette Valley except during Novem-ber, which was warmer (Fig. 1). Similarly, precipita-tion fell within one standard deviation of the 36-yraverage except for December, which was somewhatlower. These data suggest that N.fallacis experiencedtypical winter conditions for ornamentals grown in theregion. With respect to diapause of N.fallacis, Rock etal. (1971) found that the critical photoperiod of twostrains was between 11.75and 12 h daylight at 15.6°C,which is within the range of this study. In addition, allpredators recovered by either method of collectionappeared to be consistent with descriptions of dia-pausing phytoseiids: pale colored, dorsally flattenedfemales without eggs in their idiosomas (Veerman1992). We assumed, therefore, that N. fa1lacis hadentered diapause during this study.

Washing plants with ethanol extracted more N. fal-lacis than did the funnel extraction method (t = 2.67,df = 39, P = 0.005). When graphically compared (Fig.

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Fig. 1. Comparison of tempemture and precipitation forthe winter months of 1997-1998 versus the mean of the

previous 36 yr in the Willamette Valley, Oregon, U.S.

2), both methods appeared equally effective at lowpredator densities, although washing recovered moreN. fallacis than the funnel method when N.fallacisdensities were high. These findings are consistent withprevious reports that washing and filtering is as effec-tive as visually scanning plant material when samplingphytoseiids (Calkin 1991). In addition, washing re-covered spider mite adults and overwintering eggs(Table 1). Therefore, this technique may be wellsuited for monitoring overwintering pest and predatormite densities on a variety of plant types (Calkin1991).

Among individual plants, N.fallacis was more abun-dant on Piceaglauca than all others tested except Thujaoccidentalis and Viburnum davidii (Table 1). Using thewashing method, more N.fallacis were recovered fromV. davidii and Ilex cranata than Hemerocallis and thebroad leaf deciduous species. Regardless of samplingmethod, few N.fa1lacis were recovered from Hemero-callis and broadleaf deciduous plants. Also, both sam-pling methods provided an identical sequence of the

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N. fallacls extracted withwashing method Iog(x+1)

Fig. 2. Comparison among extraction methods of over-wintering N.fallacis from ornamental plants. The differenceof washing method minus funnel method is plotted againstthe washing method. The positive trend line suggests thatwashing extracts more overwintering N. fallacis than thefunnel method as mite densities increase.

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ENvIRONMENTAL ENToMOLOGY Vol 29, no. 5

Conifer ES HP DS STPlant Type

Fig. 3. Number of N.fal/m;;s overwintering on four dif-ferent plant types after inoculation of100 adult females in lateautumn. ES, evergreen shrub; HP, herbaceous perennial; DS,deciduous shrub; ST, shade tree. Columns followed by dif-ferent letters are significant at a = 0.05.

five plant species harboring the most N.fallacis (Table1).

When data from the washing technique werepooled into plant types, N.fallacis overwintered moston conifers (Fig. 3). These data were surprising con-sidering that N.fallacis is not common on conifers inthe region (Hadam et al.1986, Calkin 1991). However,N. fallacis is found in the eastern United States onconifers and can provide adequate control of O. un-unguis (Boyne and Rain 1983). Broadleaf evergreensharbored more N.fallacis than herbaceous perennialsand deciduous plants (t = 5.44,df = 26,P< 0.001;t =4.25, df = 14, P = 0.001, respectively). Amongbroadleaf evergreens, N. fallacis were common on V.davidii but scarce on 1.cranata and on rhododendron(Table 1). Herbaceous perennials and broadleaf de-ciduous plants did not differ in densities of N.fallacis(t = 1.19,df = 18,P = 0.25).

When comparing overwintering locations as col-lected from the washing technique, more N. fallaciswere found on leaves than on trunks (t = 2.89,df =46, P = 0.001); levels of predators on branches wereintermediate (Fig. 4). No N. fallacis were extractedfrom soil and associated litter using the funnel method.This is contrary to reports that N. fallacis commonlyoverwinters in litter or soil (Putman 1959,Morris et al1996). One explanation may be that there were dif-ferent environmental conditions present among thesestudies, which may have affected the depth of dia-pause entered into by N.fallacis (Veerman 1992). Forexample, Morris et al (1996) showed that N. fallacismoved from leaves to the soil as temperatures de-creased. The effect of temperature on selection andpersistence in overwintering sites is unclear.

Densities of overwintering N. fallacis collected on15 February were positively correlated with those of

Leaves Branch Trunk! Crown

Overwintering location of N.fallacis among all plants

Fig. 4. Overwinteringlocation of N.fallacis within 10ornamental plants after inoculation of 100 adult females inlate autumn. Data are from an ethanol washing method only.Columns followed by different letters are significant at a =0.05

spider mites (F= 33.87;df= 1,8;P = 0.0004;Table1).Highest densities of N.fallacis were associated with O.ununguis, a species that develops large populations inspring and fall (Calkin 1991). These results may indi-cate that overwintering survival of N.fallacis is relatedin part to feeding on warm winter days. Insufficientprey densities during warm periods in winter or earlyspring may result in starvation or dispersal of thepredator from plants (Pratt et al. 1998). In other stud-ies of different plants and climates, overwintering sitesofN.fallacis varied according to severity of conditionsand presence of prey. For example, in mild fruit-growing regions of New Zealand, the major wintermortality of N. fallacis was thought to be a result ofoverexploitation of prey and starvation rather thancold temperatures (Penman and Chapman 1980). Inthe more severe fruit-growing regions of New York,U.S., Nyrop et al. (1994) found that N. fallacis over-wintered within orchard trees when prey werepresent but dispersed to ground cover or orchardmargins in the absence of prey. Similarly, Morris et al.(1996) showed that overwintering N. fallacis weremost prevalent when high densities of spider mitesalso were collected, and as colder temperatures oc-curred, diapaused mites moved from leaves to moreprotected sites in debris near the soil. As previouslyreported, various nonspider mite prey or foods willenhance survival of N.fallacis when tetranychid mitedensities are low (Pratt et all999). What role thesealternative foods play in overwintering survival is un-known.

Significantly more N. fallacis were collected fromplants in the greenhouse than under protective plasticor unprotected (Fig. 5). These differences may be theresult ofless variable and warmer temperatures withinthe greenhouse (Fig. 6). Also, there was very littlewind in the greenhouse and this may have reducedaerial dispersal of mites from plants (Pratt et all998).Lowest levels of overwintering mites were found un-

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October 2000 PRATr AND CRoFf: OvERWINTERING OF N.fallllCis 1039

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Fig. 5. Densities of N.fallacis collected from Viburnumdavidii and Picea glauca Conica under different protectivecultural practices.

der protective plastic (Fig. 5). On warm days, somepredators that move from foliage to plastic may notreturn to plants. As described above, warmer condi-tions may have also caused predators to come out ofdiapause and feed more on spider mites, thus deplet-ing the food supply and consequently resulting instarvation (Pruszynski and Cone 1973). These findingssuggest that covering cold-sensitive plants with pro-tective plastic may negatively affect overwintering ofN. fallacis in ornamental plants.

In summary, our findings on overwintering survivalof N. fallacis have relevance to cultural practices, bi-ological control, and overall ornamentallPM. Becauseincreased predator densities in early spring improves

Maximum and minimum temperatures:In greenhouse

30

20

10

o

-10

-20

under protective plastic

unprotected plants30

20

10

o

-10

-20

Fig. 6. Maximum and minimum temperatures recordedunder three winter cultural practices.

biological control of some pest mites (Collyer 1964),using plants that are known to harbor overwintering N.fallacis may result in early pest suppression and mayaid in conservation of the predator within the agri-cultural system. For instance, coniferous trees (e.g.,Thuja occidentalis) are commonly used as hedgerowsin ornamental systems, and in our study this plant typeprovided the highest overwintering survival. Strategi-cally placed hedgerows may also assist in the coloni-zation of spider mite infested plants by phytoseiids viaaerial dispersal (lung and Croft 1999). Manipulation ofthese highly managed systems to enhance overwin-tering of phytoseiid mites has not been evaluated(Veerman 1992).

Acknowledgments

We thank J. A. McMurtry, G. W. Krantz, D. H. Slone, andtwo anonymous reviewers for their comments on the manu-script. This research was funded in part by grants from theOregon Association of Nurseryrnen and Northwest NurseryCrops Research Center (USDA).

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Rereived for publication 11 January 2000; accepted 23 June2000.