Review

Phytoseiid dispersal at plant to regional levels: areview with emphasis on management of Neoseiulusfallacis in diverse agroecosystems

B.A. CROFT* and C. JUNGDepartment of Entomology, Oregon State University, Corvallis, OR 97331-2907, USA; *Author for cor-respondence (e-mail: croftb@bcc.orst.edu; phone: 541 737 5498; fax: 541 737 3643)

Received 5 July 2001; accepted in revised form 1 March 2002

Key words: Dispersal, Phytoseiidae, Predatory mites, Regional population dynamics, Spider mites, Tet-ranychidae

Abstract. Dispersal behaviors of phytoseiid and tetranychid mites are key factors in understandingpredator-prey dynamics and biological control of pest mites at different spatial levels in agricultural andnatural ecosystems. In this review, ambulatory and aerial dispersal of both mite groups are discussed atspatial levels of leaf, plant, crop and region. Emphasis is on dispersal of phytoseiids, and specifically,the specialist-predator, Neoseiulus fallacis (Garman), and two-spotted spider mite prey, Tetranychus ur-ticae (Koch). Dispersal aspects that are discussed are ambulation on a leaf; plant or in a prey patch;aerial dispersal between plants; behavior and aerodynamics of aerial take-off; modeling vs. monitoringof dispersal distance; fates of dispersing mites that land on soil substrates; plants as take-off platformsand landing targets for dispersers; and regional dispersal patterns and integrated mite management.

Introduction:

Predaceous phytoseiid mites are important biological control agents of spider mitepests (Acari: Tetranychidae) in agriculture and many other plant systems (Helle andSabelis (1985a, 1985b)). However, these predator-prey mite systems often are un-stable. Spider mites (Tetranychus urticae Koch) are patchily distributed. Phytosei-ids find prey patches and cause extinction of prey mostly because of their numeri-cal responses. As prey mites are eliminated, specialist phytoseiids (see definitionsof specialist-generalist phytoseiids in McMurtry and Croft (1997)) starve or dis-perse and thus open the crop to reinvasion by spider mites. Thereafter, spider mitepopulations can rebound and increase. With repeated local extinctions and coloni-zations, persistent biological control is greatly affected by the spatial-temporal cou-pling of prey-predator. Dispersal greatly affects these relationships. More under-standing of dispersal may lead to improved integrated mite management.

Phytoseiids disperse mostly by ambulatory and aerial means. Ambulatory dis-persal occurs in a local patch when food, shelter, and oviposition or wintering sites

Experimental and Applied Acarology 25: 763–784, 2001.© 2002 Kluwer Academic Publishers. Printed in the Netherlands.

are sought. Aerial dispersal often results in movement to new sites and spread of apopulation over a crop. Several aspects of mite interactions and phytoseiid dispersalattributes are discussed in this review (Figure 1; a simplified conceptual model ofprocesses and factors influencing dispersal). Traits that greatly affect biologicalcontrol success are dispersal frequency and distance, and predator survival and col-onization. The plant canopy form, height, size and density determine the plant plat-forms-interception targets for dispersal. Below, these and several related factors af-fecting dispersal are reviewed with emphasis on Neoseiulus fallacis (Garman), amoderately specialized predator of tetranychid spider mites. Dispersal patterns atleaf, plant, crop and regional spatial levels are discussed.

Ambulation on a leaf, plant or in a prey patch

Spider mites colonize individual leaves and form colonies in the canopies of plants.A large leaf can have one to a few pest colonies that are with or without preda-ceous mites. These intra-leaf colonies can merge to form a single, large colony. Ata larger scale, a single plant or group of closely interconnected plants is a patch(Nachman 1988). In a colony or patch, environmental conditions often are quitehomogeneous. Movement of mites in a colony or patch occurs frequently, is mostlyby ambulatory means, and has a low risk for mortality (Strong et al. 1999). Move-ment of mites from one isolated plant to another (interpatch) occurs less often andhas more risk for mortality than intrapatch movement (Nachman 1988). Within apatch, phytoseiid movement is affected by prey species (Sabelis and van de Baan1983), prey-mediated infochemicals and physical stimuli like prey feces and web-bing (Hislop and Prokopy 1981; Hoy and Smilanick 1981; Sabelis 1981; Sabelisand van de Baan 1983; Sabelis et al. 1984; Zhang and Sanderson 1992), prey den-

Figure 1. Components of ambulatory and aerial dispersal of phytoseiids from a local prey patch (leaf)to an isolated individual plant or crop canopy.

764

sity (Dover et al. 1979; Bernstein (1983, 1984); Berry and Holtzer 1990; Croft etal. 1995a), predator hunger (Jung and Croft 2001b), degree of food specializationof species (Pratt et al. 1998; Jung and Croft 2001a), walking patterns (Sabelis 1981;Berry and Holtzer 1990; Jung and Croft 2001b), temperature and humidity (Pen-man and Chapman 1980), wind (Sabelis and van der Weel 1993) and spatial struc-ture of the patch (Takafuji 1977; Strong et al. 1999; Pratt 1999). Phytoseiids lackeyes and thus visual stimuli may not affect movement but photo-orientation mayoccur (Bernstein 1983; Janssen 1999; Jung and Croft 2000). Different life stagesand sexes of phytoseiids show different ambulatory behaviors (Croft et al. 1995a;Monetti and Croft 1997).

When searching in a patch for T. urticae, adult female N. fallacis use odors thatare produced by an infested plant (Hislop and Prokopy 1981). However, once aprey colony (delimited by spider mite webbing) is found, movement is mostly byrandom search (Berry and Holtzer 1990), and predators perceive prey with mecha-noreceptors and contact chemoreceptors (Sabelis and Dicke 1985). Berry andHoltzer (1990) showed that N. fallacis used a random walking pattern when preydensity was high and more of an edge walking pattern when prey density was low.Edge walking was thought to lead to interleaf dispersal. Walking speed depends ontemperature and prey density (Penman and Chapman 1980; Berry and Holtzer 1990;Berry et al. 1991; Jung 2001). While N. fallacis is an “active” mite (Croft andZhang 1994), its walking speed at 25 °C is only 0.1–0.4 mm/s with a turning co-efficient (ratio of net speed divided by walking speed) of 0.3–0.6 (Bernstein 1983;Berry et al. 1991; Jung 2001); it requires ca. 10 h of continuous walking to go 1 mlinear distance. Specialist phytoseiids that feed mostly on spider mites (e.g., N. fal-lacis) search in a more circular or looping pattern with more turning than generalistspecies (Jung 2001). N. fallacis is intolerant to low humidity (Jung and Croft 2000)and a long time away from prey or a plant may be risky because of dehydrationand loss of energy. While specialists disperse more between patches than general-ists, ambulation by generalists may be more rapid when first disturbed; this moreintermittent movement may function more for escape from macro-predators thansearch for food (Jung and Croft 2001b).

Croft et al. (1995a) showed that the residency time of adult females of the spe-cialist phytoseiid N. fallacis was longer on a leaf with prey than for the generalists,Typhlodromus pyri Scheuten and Amblyseius andersoni Chant, and movement be-tween leaves depended on prey availability. Among immature phytoseiids, larvaemove little on leaves, but larvae that must feed to become nymphs (e.g., Galendro-mus occidentalis (Nesbitt), Schausberger and Croft (1999)) move more than larvaethat do not feed (T. pyri) (Croft and Croft 1993; Croft and Zhang 1994; Croft et al.1995a). Phytoseiid nymphs move much more than larvae. Nymphs of N. fallacisdispersed more between leaves than nymphs of T. pyri and G. occidentalis whenprey were scarce; also mortality was higher among immatures that moved fre-quently between leaves (Croft et al. 1995a)

Ambulatory dispersal is involved in other life history phases. In apple trees inspring, phytoseiids move from winter sites to foliage. For species hibernating intree buds or under bark (Typhlodromus caudiglans Schuster, G. occidentalis; Put-

765

man (1959) and Leetham and Jorgensen (1969)), the distance to foliage is only afew centimeters. In contrast, N. fallacis survives mostly in duff or ground cover ata tree base (Croft and McGroarty 1977; Nyrop et al. 1994). Colonization of foliagefor N. fallacis is probably by both ambulatory means and after aerial transport(Croft and McGroarty 1977). This trip can be hazardous because of the distanceand the inclement events that can occur (Johnson and Croft 1981; Nyrop et al.1994).

Aerial interplant movement

Many field studies have shown that phytoseiids disperse between isolated plants byaerial means (strawberry (Coop and Croft 1995; Croft and Coop 1998), mint (Mor-ris 1998), corn (Kogan et al. 1999), hop (Strong et al. (1997, 1999)), raspberry(Charles and White 1988), apple seedling (Pratt 1999), vineyard (Tixier et al. (1998,2000)), almond (Hoy et al. 1985), and apple (Johnson and Croft 1981; Walde et al.1992; Dunley and Croft 1992). The mated adult female is the main stage that isinvolved and it is usually the founder of new colonies (Dover et al. 1979; Sabelisand Dicke 1985). Coop and Croft (1995) reported that N. fallac is moved about thesame distance from a point of release either within a row of contiguous strawberryplants or between rows separated by 1 m bare ground. This species moves muchmore slowly across soil than foliage (Jung and Croft 2000; Jung 2001) so they in-terpreted their data to indicate that N. fallacis moved on foliage as much distanceaerially as by ambulatory plus aerial means. Although aerial dispersal has more riskof mortality than walking, the benefits of aerial dispersal for a specialist would bemore than the risks of starvation by staying where prey were declining (Nachman1988). In a comparative study, the specialist N. fallacis dispersed more rapidly be-tween plants by aerial means than Neoseiulus californicus (McGregor), which ismore of a generalist predator (Pratt et al. 1998). In a similar study, the aerial dis-persal rate of N. fallacis was greater than for the generalists, Kampimodromus ab-errans (Oudemans) and Euseius finlandicus (Oudemans) (Jung and Croft 2001b).Dunley and Croft (1990) observed earlier and higher rates of outward dispesal forthe specialist, G. occidentalis, from apple trees and farther dispersal and faster col-onization of mini-orchards at 10 and 100 m, than the generalist, T. pyri. Walde etal. (1992) also reported higher aerial and ambulatory dispersal rates for N. fallac isthan T. pyri on apple.

Behavior and aerodynamics of aerial take-off

Aerial take-off of mites from a leaf occurs when the drag of wind overcomes theforce of attachment. Jung (2001) calculated drag and attachment forces of Phy-toseiulus persimilis Athias-Henriot, N. fallacis and N. californicus. Force of attach-ment was calculated as the product of gravitational force and mite mass. Drag forcewas calculated with mite surface area, wind speed and a drag coefficient for aspherical shape. Results showed that aerial take-off should occur at a lower windspeed (lower drag force for a mite = ca. 1× 10−7 N) than expected by a force of

766

attachment calculation (= ca. 1× 10−4 N). Thus, some kind of active behavioral in-volvement in aerial take-off would seem to be likely. This could be achieved bybehavioral responses to wind and/or increased hunger and chemical cues from prey(Sabelis and van der Weel 1993).

Johnson and Croft (1976) reported aerial take-off for N. fallacis that involvedraising the body with the 3rd and 4th legs and facing away from the wind. Fre-quency of take-off was correlated to starvation and was higher in adult females thanin males or immature mites. Such behavior is not limited to N. fallacis, it also oc-curs in wingless first instar scale insects (Stephens and Aylor 1978; Washburn andWashburn 1983), spider mites (Smitley and Kennedy 1985; Margolies 1987), thephytoseiid mite G. occidentalis (Nesbitt) (Hoy 1982), and linyphiid spiders (tip-toebehavior reported by Weyman (1993)).

Synomone-induced suppression of aerial take-off was documented for phytosei-ids by Sabelis and Afman (1994), they found that volatiles from a plant damagedby spider mite feeding suppressed aerial take-off of the specialist, P. persimilis. Jungand Croft (2001b) found that plant-mediated cues from damaged plants suppressedtake-off of only specialist phytoseiids (P. persimilis, N. fallacis and N. californi-cus). With more generalist feeding species, such plant-related chemical cues eitherdid not influence dispersal (K. aberrans) or they actually increased dispersal for anextreme generalist (E. finlandicus). In these studies, only one prey species (T. ur-ticae) was tested for chemical cue effects and several of these phytoseiids preferother mite prey. More studies with a wider range of prey species are needed. How-ever, these initial studies suggest that there may be major differences between spe-cialist and generalist in dispersal responses to prey-mediated chemical cues.

It has been questioned whether a distinctive take-off behavior that launches aphytoseiid mite into the air is essential because some highly dispersive species likeP. persimilis do not show such behaviors (Sabelis and Afman 1994; Jung 2001),whereas other species do. For example, why does N. fallacis show such a take-offbehavior termed “standing”? Jung (2001) studied the fluid dynamics of mite dis-persal. Body profiles were assessed for N. fallac is (standing and walking), N. cali-fornicus and P. persimilis (walking only). When compared to P. persimilis, the bodyof N. fallacis is flatter, especially after being starved, and the latter has shorter legs.Also, the boundary layer of wind and the wind speed that corresponds to the heightof the mite’s body were determined. Using the above data, the drag forces that themite experiences in standing (N. fallacis only) and walking postures (all species)were calculated. Data indicated that with a more vertical profile (P. persimilis), aspecies that may not require standing to experience a wind force sufficient to be-come airborne, but one with a less vertical profile like N. fallacis would benefitmuch more from standing to become airborne.

Modeling and monitoring dispersal distance

Based on many field studies, it can be concluded that dispersing mites during asingle aerial episode traverse relatively short distances (100 m or less) (Johnsonand Croft (1979, 1981); Boykin and Campbell 1984; Brandenburg and Kennedy

767

1982; Hoy et al. 1985; Miller et al. 1985). Dispersal distance for a wingless organ-ism that moves on air currents can be determined from wind speed, wind variation,wind turbulence, falling speed and release height information (Turchin 1998). Afalling speed estimate takes into account gravitational force and friction of a fallingobject (mite) in air and is affected by size, shape, mass and appendage morphologyof a mite as well as any behavioral factor. Jung and Croft (2001a) found that fall-ing speeds for 13 phytoseiid adult females were 0.39–0.73 m/s and 0.79 m/s for T.urticae. Starved mites had lower falling speeds than fed mites. Also, falling speedsdiffered among species and between active and inactive mites (anesthetized) of thesame species for the specialists P. persimilis, Phytoseiulus macropilis Banks, Neo-seiulus longispinosus (Evans), G. occidentalis, and N. fallacis, and the generalistsT. pyri, A. andersoni, Neoseiulus cucumeris (Oudemans), Neoseiulus bakeri (Hugh-es), K. aberrans, E. finlandicus, and Euseius hibisci (Chant)). Jung and Croft(2001a) ascribed falling speed differences in active vs. inactive mites to within-airbehaviors, but these behaviors could not be observed directly. Using falling speeddata in models of dispersal distance, they found that a seed dispersal model (Greeneand Johnson 1989) was applicable to modeling mite dispersal. For validations de-termined in a wind tunnel, greenhouse and in the field, the seed dispersal modelgave good fits to dispersal distances of phytoseiids that were emanating from dif-ferent plant platforms (Jung and Croft 2001a). An application of the dispersal modelwas in predicting dispersal distances (Figure 2) and distributions of spider mitesand phytoseiids dispersing inward from nearby fields and adjacent border vegeta-tion. Such data are relevant to managing mites within crops and over large areasthat have both agricultural and riparian vegetation (see discussion of regional as-pects below).

By modeling, Jung and Croft (2001a) predicted similar dispersal distances forN. fallacis and N. californicus because of similar falling speeds but in experiments,

Figure 2. Median aerial dispersal distance of N. fallacis from different cropping platforms (predictionsfrom model of Jung and Croft (2001a)).

768

N. fallacis dispersed earlier and farther in air than N. californicus (Pratt et al. 1998).A distinctive take-off behavior in N. fallacis and not in N. californicus (Johnsonand Croft 1976; Jung 2001) may affect transport. Different take-off behaviors werenot included in models of Jung and Croft (2001a). The longer dorsomedial anddorsolateral-setae of N. fallacis (Sabelis and Bakker 1992; Croft et al. 1999) couldaffect buoyancy. Also, in-air behavioral differences could be involved. While nodifference in falling rates between these mites occurred in still air (Jung and Croft2001a), the effects of these factors may be different when mites are traveling morehorizontally and for longer (a few sec to min) in wind. Also, diet specialization andintra- or interspecific predation may contribute to dispersal differences between N.fallacis and N. californicus. Neoseiulus californicus has a broader diet range (Croftet al. 1997; Pratt et al. 1999), thus, it may stay in a patch with few prey and feedon other foods or wait for spider mites to return while minimizing starvation. Al-ternatively, N. fallacis may leave a patch earlier as prey levels decline. Greater in-terspecies predation on other phytoseiids may allow N. californicus to stay longerin a habitat with scarce prey; also, development would be slowed, but N. califor-nicus may survive longer when feeding on phytoseiid immatures (Croft et al. 1995b;Schausberger et al. 2000) and thus may persist longer until spider mites return. Agreater preference for eggs as prey in N. fallacis than N. californicus (Blackwoodet al. 2001 (in press)) may account for earlier dispersal as eggs disappear first froma patch when prey levels decline. Metabolic rate as reflected in starvation times ishigher for N. fallacis than N. californicus but starved N. fallacis lay eggs soonerwhen food again becomes available (Croft et al. 1995a). These physiological dif-ferences could affect the onset of dispersal. Also, other aspects of competition mayinfluence dispersal; in this regard, N. fallac is usually is displaced by N. californi-cus in mixed colonies (CJ personal observation).

A similar pattern to that seen for dispersal of N. fallacis and N. californicus wasobserved for the specialist G. occidentalis and generalist T. pyri (Dunley and Croft(1990, 1992)). Outward dispersal of T. pyri was less than for G. occidentalis andthe latter dispersed farther through air. Athough some dispersing T. pyri arrived ata distant sample site at 100 m whereas many G.occidentalis did, fewer T. pyri in-dividuals moved so far and how many aerial bouts occurred for either mite wasunknown. A model of dispersal distance (Jung and Croft 2001a) predicted similarvalues for these two species assuming that release height was equal. However, againdifferent dispersal rates could be explained by several factors. A similar standingaerial take-off like that of N. fallacis is known for G. occidentalis (Hoy et al. 1985),but not for T. pyri (Jung 2001). Also, if G. occidentalis were more sensitive to preydensity declines and moved about more within trees, then earlier and more distantdispersal might occur. Typhlodromus pyri also is less impacted by spider mite den-sity, it relies more on pollens for foods (McMurtry and Rodriguez 1987; Walde etal. 1992; Nyrop et al. 1994; McMurtry and Croft 1997), and thus it may disperselater and less frequently than does G. occidentalis.

769

Fates of dispersing mites landing on soil substrates

After aerial take-off, phytoseiids are transported and deposited on a substrate (Ra-worth et al. 1994; Jung and Croft 2001a). Some dispersing mites may land on acrop (Smitley and Kennedy 1985), thus their travel would be for a few s, and mor-tality would be low. Since dispersing mites likely cannot control landing, stochasticpatterns of fallout mean that many airborne mites do not land on a plant but ratherthey arrive in more hostile environments. For example, if they land on soil, thensurvival may be low. Even if mites land on a plant, prey may not be present andrepeated ambulatory and/or aerial dispersal are necessary. In field tests with N. fal-lacis on bare ground (Jung and Croft 2000), mortality increased log-linearly as dis-tance to a host plant with prey increased. Soil surface affected mortality–recoveryto host plants was higher in clod plots than in gravel or fine soil plots. Managementactions such as watering and mulching of vegetation allowed better survival thanseveral other treatments. Temperature and relative humidity affected survival ofmites that were on soil and seeking a prey inhabited plant: Predators suffered 10%mortality in a greenhouse under very favorable environmental conditions, but 90%occurred in the field under hot, dry arid conditions. Janssen (1999) reported 85%recovery of P. persimilis when placed on soil and recovered on cucumber plants0.4 m away. A trend of directional movement downwind in field studies but not inwindless laboratory tests indicated that movement from soil to plants involved bothambulatory and aerial means (Jung and Croft 2000).

Plants and crops as take-off platforms and interception targets for dispersants

The extent of phytoseiid dispersal within and between fields is affected by take-offplatforms and landing profiles that a plant or crop presents. Below, we discuss dis-persal dynamics of phytoseiids in 4 crops relative to these aspects and other relatedvariables.

Strawberrry

In this low-growing crop of rows and continuous within row foliage (in matureplants), N. fallacis disperses at rates that are dependent on temperature, prey den-sity and plant type (Coop and Croft 1995). As noted, when moderate to high levelsof T. urticae were present N. fallacis moved equidistantly within and between rowsacross bare soil. Data suggested that mites either were ambulating across soil ormore likely that some aerial transport was occurring even when prey were stillpresent on foliage. Under such conditions, N. fallacis remained aggregated withprey and moved only about 20–30 m per growing season from a release point; dis-persal distance doubled every 70 degree-days (minimum threshold = 10 °C). Inthese studies where spider mite densities were moderate to high, dispersal distanceswere limited as dense prey patches kept predators from moving out rapidly. At theseprey densities, N. fallac is spread faster in moderately-aged fields with dense foli-age than in young or old fields with more sparse foliage (Croft and Coop 1998).

770

Peppermint

In this crop of uniform coverage and 1 m height (like alfalfa or lucerne), move-ment of N. fallacis is almost a random process within a field except for when thepredator-T. urticae system is uncoupled by plant loss during harvest or winter(Morris 1998; Morris et al. (1996, 1999, 2000)). In entering the winter period, bothprey and predaceous mites move between live foliage and soil litter at the plantbase depending on temperature and snow cover. Mites stay on live foliage as longas possible. Sometimes during December-February, there is climate-related plantmortality and spider mites and predators are differentially affected. For example, T.urticae can tolerate low humidities and survive in less protected sites better than N.fallacis. Plant losses often require that wintering mites move to new sites and oftenthere is a redistribution of mites to nearby living plants in spring. During these in-clement times, considerable mortality can occur. In many cases, either mortality isnot highly discriminating to predators over spider mites or the spatial uncouplingdoes not last long enough to allow spider mites to become severe pests beforepredators find them again and then increase to substantial levels.

Later in summer, however, a peppermint field changes from being a lush plantcanopy to an arid condition where plants are cut near the soil level and stems andleaves are removed and harvested for oils (Morris et al. 2000). Usually what is leftis a stem of 2–8 cm with either no leaves or only a few leaves of poor quality.After harvest, stem and leaf growth may occur if irrigation is used but often plantsstay almost in dormancy until rain comes in fall. When harvest (plant destruction)occurs, spider mites and predators are decimated, and many are displaced to soil.Afterwards, some re-colonization of plants occurs, but the distributions of prey andpredator mites are different. Tetranychus urticae is more tolerant to low humiditythan is N. fallacis, and a spider mite can occupy all of the remaining plant parts.However, predators usually survive only on the first few leaves close to the soilinterface–this is a very restricted habitat in terms of conditions and size. In essencethe predator-prey system is uncoupled; spider mites can increase on all foliagewhereas predators are limited to lower leaves. Depending on when irrigation and/orrainfall occur, this uncoupling can last for months and predator-prey dynamics canbe affected greatly. To add to these severe disturbances, growers often “flame” fieldsto eradicate diseases and other pests, which selectively decimates predators evenmore (Morris et al. 2000). The net effect is that spider mites can reach outbreakproportions in late season. Sometimes the effect is severe enough that the outbreakspersist into spring and summer before predators disperse and respond to prey. Attimes, the spatial dynamics of mites are like a checkerboard of colonization andrecolonization among predator-prey patches. Also, dispersal behaviors and plantprofiles for take-off and landing affect re-establishment and population dynamics:Tall plants experience faster re-establishment than short plants with less foliage.Sometimes, short uncouplings can promote persistence and keep predators fromoverexploiting prey and not lead to predator-prey asynchronies where predators arefew and prey are abundant and vice versa (Morris et al. 2000)

771

Apple rootstock seedlings

This system is characterized by apple trees lying vertical in soil with shoots ex-tending horizontally up through a woodchip mulch. Dense rows of seedlings (2 mhigh) extend for 2 km with open areas of 1 m between rows. Ground mulch is wa-tered daily and remains moist all summer. In fall, spider mite and predator popu-lations are eradicated from fields when seedlings are harvested below the soil. Re-colonization of a field each spring is an almost random process of spider mites andpredators dispersing inward either from nearby or regional plant sources, or some-times, mass-reared predator mites are released at regular intervals on foliage (Pratt1999).

In this apple system of almost contiguous foliage, natural inward dispersal of T.urticae begins in mid-June as temperatures increase. Within a few weeks in lateJune-early July, spider mite densities are still low (< 0.1 per leaf), and are repre-sented typically by a single adult female with 5–15 eggs (isolated, local prey patch).At this time, N. fallacis are released at 1,000 per ha. (on bean foliage with a fewprey mites) in small sprigs every 12 m of row. Dispersal and spread of releasedpredators across the field occurs so fast that it is difficult to keep non-release areas(50 m diameter) not colonized by predators for more than 1 week (Pratt 1999). Thiscoverage of fields occurs because of low prey densities that cause predators to re-disperse aerially several times before they find prey (contrast this rapid interplantdispersal with the slow rates observed (above) when prey were high to moderatelydense on strawberry). The tall platform and large profile that the apple seedlingspresent for the dispersing mites is a key to explaining rapid spread of predators inthe field. Virtually every mite that disperses hits a plant and survives until it findsprey or starves. In a short time, however, almost all prey patches are found and thepest mite level is reduced before it reaches >1 mite per leaf. The predator peaks atabout 1–3 per leaf and regulation of the pest at very low densities is maintaineduntil fall. Such rapid and efficient dispersal of predators is not common in manycrops for reasons relating to prey levels, predator distributions, plant take-off plat-forms and target profiles, etc.

Hops

In contrast to apple seedlings, the hop system is very unfavorable to predator dis-persal, even though as a take-off platform the system would seem to be ideal (highplant platform with dense over-story canopy). Hop typically has a rapid growthcycle. It begins as an isolated plant with only a few leaves at ground level anddevelops to a canopy of interplant foliage at 6 m height over 1–2 months. Becauseof rapid growth, wintering or mass-produced/released N. fallacis may colonize thelow plant parts but if many spider mites are present, the predator population willnot advance up the stem fast enough to disperse throughout the canopy (Strong andCroft 1995). For a predator that makes it to the canopy top, the platform is highlyfavorable for dispersing long distances (>100m; (Jung and Croft 2001a)), but it canbe a poor interception target for dispersing mites (Strong et al. 1999). The hop stem

772

usually (2–6 cm diameter) extends 2 m from the base with no leaves (leaves arestripped from the plant for disease control), and thus this small target is unlikely tobe hit by a free-falling mite. In tests where predator-free plants had lower leavesstripped or covered with soil (hilling), N. fallacis did not either increase nor dis-perse enough to suppress spider mites. However, if basal leaves were left intact,then a rosette at the base served as a landing pad for immigrant predators thatmoved rapidly up the stem and gave effective biological control (Strong et al. 1999).

In relation to metapopulations on hops, dispersal rates of predators and preywithin and between plants can greatly influence stability of interactions, and mod-erate dispersal rates are usually most effective (Sabelis et al. 1991; Janssen et al.1997; Strong et al. 1999; Pels and Sabelis 1999). As noted, if N. fallacis dispersestoo slowly in and between plants, then local T. urticae subpopulations will reachunacceptable levels. Conversely, if N. fallacis disperses too rapidly between plants,then populations of an entire hop yard may act as one large coherent populationleading to instability and lack of persistence of the predator. Pest resurgence islikely under these conditions. In practice, too much dispersal is unlikely becauseeach plant is separated by a soil “desert”, and plants do not touch until midseason.Rather, there is greater possibility of too little predator dispersal when the pad offoliage at the plant base is removed. Ideally, through proper management, the dy-namics of both the predator and prey may be adjusted to ensure stability of inter-actions on hops while maintaining acceptable control of T. urticae. Control of suchinteractions on hop could then greatly improve regional interactions on crops in anarea of diverse agriculture (see regional aspects below).

Regional mite dispersal and integrated mite management

Within a region, spider mites are not limited to a single field or plant type (Bran-denburg and Kennedy 1982). Pesticide-susceptible (SS) spider mites usually occurat low levels on native vegetation because predators regulate them there. However,in more disturbed settings, pesticide-resistant (RR) T. urticae move between cropsand cause problems, even on plants where endemic predators normally give goodcontrol. Two examples are on apple seedlings and grapes. Nursery stocks of appleseedlings are harvested at below ground in fall, which eliminates wintering mites;thus, mite infestations and subsequent control depends primarily on inward dis-persal of mites in early season (Pratt 1999). Spider mites can increase appreciablyin apple seedlings before predators arrive and thus much damage can occur depend-ing on where immigrant prey and predator mites are located. Also in vineyards,spider mites are seldom pests, but RR dispersant from nearby crops can cause se-vere damage because predators cannot reproduce fast enough to control them(Prischmann 2000). These examples indicate that a regional perspective is needed.Lastly, we discuss integrated mite management of T. urticae with the goals of sus-taining crop production, reducing control costs, and limiting pesticide resistanceevolution in spider mites.

Some background on crops and mite ecology is necessary to explain regionalintegrated mite management in the Willamette Valley, Oregon, where more than 90

773

economic plants are grown on many spatial scales and timings (Croft 1997; Koganet al. 1999). Among agricultural plants, ornamentals are of greatest value and mint,tree fruits and corn make up the most hectares. Within the region, the ecology ofmites is complex and includes their population dynamics in riparian and othernatural areas. Many non-agricultural plants harbor spider mites, predators and al-ternate foods or prey for predators (Table 1). Some that harbor phytophagous mitesmostly add to pests and predator inoculums (often of varying resistance status)while others mostly are recipients of immigrants. For example, hop and corn aretall plants that produce many spider mites. Initially, these crops usually have fewpredators, and without natural controls, spider mites build up quickly and dispersewidely. The predator, N. fallacis, also can build up rapidly in hop and corn anddisperse widely, but often this development is too late and of little consequence tobiological control of spider mites on crops that develop in mid-season. Mite dy-namics on hops and corn explains much about overall patterns of mite dispersal inthe region.

In contrast to N. fallacis, T. pyri is a phytoseiid in this regional ecosystem thatdisperses either less distant or less often (Johnson and Croft 1981; Boller et al.1988; Dunley and Croft 1990; Jung and Croft 2001b). This predator is producedmainly on blackberry and moderately-sprayed crops such as caneberry, apple andgrape where it can effectively control spider mites (Croft 1997; Prischmann 2000).Vegetation cuttings from wild blackberry and commercial crops with T. pyri can betransferred to new plants or crops from which predators have been eliminated.

Regionally, phytophagous and predaceous mites that occur on alternate hostplants with other prey, foods or pollens are of interest. The case with blackberryand T. pyri is a good example of such a plant. These plants with many kinds ofphytophagous and predaceous mites can be manipulated to affect biological controland pesticide resistance. Broadleaf weeds like dock and dandelion and riparianvegetation that occur next to heavily treated crops can be major sources for N. fal-lacis; not spraying these plants in early season can be important to biological con-trol. These sites can be refugia for SS spider mites that usually are vastly outnum-bered by RR spider mites. Hedgerows and trees (especially rosaceous plant types)harbor alternative prey for predaceous mites.

Another potential resource is the use of a banker plant that provides prey or foodfor predators; it usually can be moved to wherever spider mites are a problem.Usually a banker plant produces either pollen or a prey mite that is relatively spe-cific to the plant. It also is helpful if the predators do not suppress the prey mites tolow levels on the banker plant. An example is arborvitae (Thuja occidentalis) whichhabors Oligonychus ilicus (McGregor) that only feeds on conifers (Pratt 1999).Whereas N. fallacis will readily feed on active stages of O. ilicus, it does not usu-ally reduce it to low levels because it has an egg stage with a hardened chorion thatthe predator cannot readily feed upon. Thus, the arborvitae can harbor spider mitesand produce many N. fallacis over a long period, resulting in dispersal of thepredator and inoculation of ornamental plants and other crops. Castor bean (Rici-nus communis) is a banker plant that provides nectaries and pollen for Iphiseiusdegenerans (Berlese) that controls thrips on peppers (Ramakers and Voet 1995).

774

Tabl

e1.

Plan

tSy

stem

sin

the

Will

amet

teV

alle

yA

reaw

ide

Spid

erM

iteM

anag

emen

tPr

ojec

t.

Plan

tSy

stem

sPr

oduc

tion

ofsp

ider

mite

sPr

oduc

tion

ofpr

edac

eous

mite

sR

esis

tanc

est

atus

ofT.

urti

cae/

N.

fall

acis

Dis

pers

alof

T.ur

tica

e

PEST

SOU

RC

EPL

AN

TS

(gre

ates

tso

urce

sof

RR

(SS

inG

H)

pest

and

pred

ator

mite

inoc

ulum

)P

eren

nial

sH

ops

high

/late

seas

onlo

w/la

tese

ason

RR

/RR

*ve

ryhi

ghA

pple

(som

etim

es)

mod

erat

em

id-s

easo

nR

S/R

Rve

ryhi

ghG

reen

hous

em

ixed

none

orm

any

RR

/RR

low

Ann

uals

(or

act

like

annu

als)

Cor

nhi

gh/la

tese

ason

high

/late

seas

onR

R/R

Rm

oder

ate

Gre

enho

use

mix

edno

neor

man

yR

Ror

SSfo

rbo

thlo

wM

IXE

DSO

UR

CE

PLA

NT

S(r

efug

ean

dba

nker

plan

tsfo

rR

R/R

S/SS

mite

s)P

eren

nial

sM

int

high

/mid

-sea

son

high

/late

seas

onR

R/R

Rlo

wSt

raw

berr

yhi

gh/e

arly

seas

onhi

gh/m

id-s

easo

nR

R/R

Rlo

wC

onif

erm

oder

ate/

earl

ylo

w/la

tese

ason

RS/

SSm

oder

ate

SIN

KSO

UR

CE

PLA

NT

S(m

ayse

rve

asre

fuge

and

bank

erpl

ants

for

SSm

ites)

Per

enni

als

Gra

pelo

w/la

tese

ason

low

/late

seas

onSS

/SS

mod

erat

ePe

ach

low

/mid

-sea

son

low

/late

seas

onSS

/SS

high

Apr

icot

low

/mid

-sea

son

low

/late

seas

onSS

/SS

high

Can

eber

rylo

w/m

id-s

easo

nhi

gh/e

arly

seas

onSS

/SS

mod

erat

eA

pple

nurs

ery

low

/late

-sea

son

low

/late

seas

onSS

/SS

mod

erat

eA

LTE

RN

AT

EH

OST

S(n

atur

alre

fuge

san

dso

me

mob

ilere

fuge

sfo

rSS

/RS

mite

s)P

eren

nial

s Bla

ckbe

rry

none

high

/all

seas

on—

/SS

mod

erat

eO

rnam

enta

lsan

ytim

ene

eded

high

/all

seas

onSS

/RR

vari

able

Tre

eslo

w/m

id-l

ate

low

/mid

-lat

eSS

/SS

high

Ann

uals

Wee

ds(a

roun

dpr

oduc

erpl

ants

)lo

w/e

arly

seas

onlo

w/e

arly

seas

onR

S/R

Slo

w-m

od.

*RR

=hi

ghly

resi

stan

t,R

S=

mod

erat

ely

resi

stan

t,SS

=no

orlit

tlere

sist

ance

775

A refuge plant is another plant type that can be a source of SS spider mites thatmix and dilute resistant mites. Refuge plants are a type of alternate hosts that canprovide food or prey for predators. Another plant type that may be useful is a sen-tinel plant (30–50 bean seedlings held in a plastic bag in soil) that can be placed ingrid locations within a region. A sentinel plant can be used to monitor for immi-grant spider mites or can be seeded with SS T. urticae to monitor for immigrantpredators. It also can be used to maintain a reservoir or crops with susceptible spi-der mites for resistance management purposes. Whatever its use, collected mitescan be assessed for resistance. Finally, a small-scale predator unit is a plot of le-gumes grown early in the season that is seeded with SS spider mites and later withpredators. As T. urticae develops later in crops, these plants with predators (and afew SS prey) are used to inoculate and give pest control (Pratt 1999).

Densities, control problems and pesticide resistance of spider mites are knownfor many plant types in the region (Table 2). The tendency of hops and corn toproduce many resistant spider mites that inundate other crops was mentioned. Oncrops such as apple, mint, peach, caneberry and grape, the potential for nativepredators to provide biological control is good so long as selective tactics are used(Table 3) and immigrant spider mites are not excessive. Control of mites by naturalpopulations of predators is unlikely on greenhouse and ornamental plants becauseof intensive cultural methods. Predator releases can be effective on these intensivelymanaged plants (Table 3), but proper timing and densities of release are critical(see details for predator releases in apple seedlings and 30 ornamental plant speciesor cultivars in Pratt (1999))

Areas of applied research

Several management questions are being addressed about dispersal of predaceousmites in the context of regional population dynamics. Identification of integratedmite management measures that limit pests and yet conserve endemic phytoseiidsare the main goals of these programs; however, in greenhouse plants, outdoor or-namentals and strawberry fields, the focus of integrated mite management is moreon releasing mass-reared phytoseiids or in rearing these predaceous mites in smallfield plots. Some specific questions that we are asking in research are:

Can predator releases on crops with high profiles reduce T. urticae regionally?

Hop and corn are monitored and as spider mites increase, N. fallacis from com-mercial or grower small-scale rearing units are seeded when prey reach 0.5–3.0 perleaf. Predator release rates for hop are known (Strong and Croft 1995), but thosefor corn are under assessment. While biological control is occurring, dispersal ofpredator and prey mites into adjacent habitats can be assessed in nearby fields andon riparian vegetation. Also, a grid of sentinel plants is monitored weekly and im-migrants are assessed for densities and resistance status using standardized bioas-says (Flexner et al. 1995).

776

Tabl

e2.

Pest

Lev

els,

Con

trol

Met

hods

,R

esis

tanc

ean

dPo

tent

ial

Pred

ator

Rel

ease

Stra

tegi

es.

T.ur

tica

eL

evel

san

dPr

oble

ms

Con

trol

orR

elea

seSt

rate

gies

byPr

edat

ors

Cro

pPe

stL

evel

sPe

stco

ntro

lpr

oble

mR

esis

tanc

epr

oble

ms

Nat

ive

Pred

ator

sIn

ocul

ativ

eR

elea

sePe

riod

icR

elea

seIn

unda

tive

Rel

ease

App

leH

MM

HH

——

Apr

icot

LL

LM

L—

—

Can

eber

ryM

LL

HL

——

Con

ifer

MM

LM

ML

—

Cor

nH

HH

LH

M—

Gre

enho

use

veg.

/oth

ers

HH

VH

LH

HM

Hop

HH

HL

HM

—

Min

tH

HH

HM

L—

Orn

amen

tsM

HM

LH

ML

Peac

hL

LL

HL

——

Stra

wbe

rry

HM

MH

ML

—

Nat

ive

pred

ator

s=

nore

leas

esof

pred

ator

s;in

ocul

ativ

ere

leas

es=

one

rele

ase

offe

wpr

edat

ors;

peri

odic

rele

ase

=m

ore

than

one

rele

ase

ofpr

edat

ors;

inun

dativ

ere

leas

e=

one

orm

any

rele

ases

ofm

any

pred

ator

s.C

ateg

orie

sof

pest

leve

lsor

resi

stan

cepo

tent

ial

for

T.ur

tica

eor

biol

ogic

alco

ntro

lby

pred

ator

s:H

=hi

gh,

M=

med

ium

,L

=lo

w.

777

Tabl

e3.

Phyt

osei

idM

anag

emen

tSt

rate

gies

and

Tact

ics

inW

illam

ette

Cro

ppin

gSy

stem

s.

Pred

ator

Man

agem

ent/R

elea

seTa

ctic

Type

Prod

uctio

n

Syst

emTy

pe

Nat

ive

Pred

ator

s

Inun

dativ

e

Rel

ease

Peri

odic

Rel

ease

Inoc

ulat

ive

Rel

ease

Ove

r-W

inte

rE

arly

-Ban

ker

Lat

e-B

anke

rPr

eyIn

ocul

ate

Alte

rnat

ePr

ey

App

leU

UU

U

App

lenu

rser

yU

UU

UU

UU

UU

Apr

icot

UU

UU

Can

eber

ryU

UU

U

Con

ifer

UU

UU

UU

S

Cor

nU

UU

US

Gre

enho

use

UU

UU

UU

SSS

SSS

SSS

SSS

SS

Hop

UU

UU

U

Min

tU

UU

UU

Orn

amen

tsU

UU

UU

UU

SS

Peac

hU

UU

U

Stra

wbe

rry

UU

UU

US

SSS

SS

U=

Use

rof

met

hod;

S=

supp

lier

ofpr

edat

orm

anag

emen

tm

etho

d,m

ultip

lesy

mbo

lsin

dica

tele

vel

ofus

eor

supp

ly.O

verw

inte

r=

over

win

teri

ngsu

pply

ofpr

edat

ors,

Ear

ly-B

anke

r=

earl

yse

ason

use

ofba

nker

plan

t,L

ate-

bank

er=

late

seas

onus

eof

bank

erpl

ant,

Prey

inoc

ulat

e=

inoc

ulat

epr

eyto

plan

tsea

rly

inse

ason

and

Alte

rnat

epr

ey=

alte

rnat

epr

eypr

esen

ton

plan

t.

778

Can strategically located rearing plots (0.3 ha) provide predator inoculums?

At experimental sites, legume (peas, beans) plots are inoculated with spider mitesin Feb-March. A few days later, predators from greenhouse colonies are added tofoliage at levels needed to control spider mites before they become dense and dis-perse, but few enough to allow maximum predator productions (or optimal fieldproduction). In early season, these plants with few spider mites and many predatorsare seeded into fields that have early-season spider mite problems (strawberry,rhododendron). Where pest mites develop later, predators are released in largeramounts and distributed more widely in the crop. Multiple plantings of legumesmay be staggered if predators are needed for later inoculations. To assess releaseeffectiveness, a surrounding untreated area and one that is treated are identified andspider mites and predators monitored at regional grid sites. While there is somerisk that inoculations of spider mites may pose a later problem if weather shouldselectively eliminate predators and not prey, this condition seldom occurs and theneither selective pesticides or another predator release may be used to restore a morefavorable ratio of predators to prey.

By moving plant residues, can predators on early-season crops be inoculums forother crops?

Mature strawberry plants have spider mite and predator populations that reproducein winter at low rates because plants moderate the environment. In spring, if preda-tors are not present at levels sufficient to give pest control, then spider mites canbuild up and thereafter, large predator populations are produced. If the timing isright, biological control can be successful, but the field also can be a predator pro-duction unit. In such cases, the grower harvests berries in June and then flails fo-liage and causes plants to send out runners. Flailed plant material dries and mitesthereon either die, or move to the new foliage (Coop and Croft 1995). Growers cancollect flailed plant material before it dries and place it in hop, apple seedlings,corn, etc. for inoculation of predators.

Can mid- to late-season predator releases add inoculums for the next year?

As noted, some plants allow for enhanced predator survival in winter, includingstrawberry, peppermint, and Viburnum, an ornamental flowering plant (Coop andCroft 1995; Morris et al. 1996; Pratt 1999). A canopy-effect contributes to devel-opment of N. fallacis on strawberry. Mint stems are good wintering sites (Morris etal. 1996). Viburnum has many wintering sites in bark and if placed in a semi-en-closed, insulated house, then there is even more protection and some increase ofpredators (Pratt 1999). Viburnum often is grown in movable pots and can be abanker plant. Each of these plants can receive low-level predator releases in late-season that subsequently buildup and disperse in the next spring.

779

Can sentinel plants with SS-T. urticae lessen pesticide resistance and be used tomonitor regional pesticide resistance?

Pesticide resistance is lessened when resistant mites interbreed with susceptiblemites that come from natural reservoirs (weeds or other host plants) or from intro-ductions of laboratory-reared mites. Since we use SS T. urticae to monitor move-ment of predaceous mites, we questioned how much effect the escape and dispersalof these spider mites would have on lessening pesticide resistance.

In summary, regional aspects of integrated mite management rely on understand-ing dispersal dynamics of pest and predaceous mites. Although we cannot yet ac-count for dispersal for all species in these complex systems, average behavior of T.urticae, N. fallacis and T. pyri can be predicted with some accuracy. Validations formodels and pest management applications have come from low growing strawberryand peppermint, taller apple seedlings and caneberry and even taller fruit trees andhop crops (Dunley and Croft 1990; Coop and Croft 1995; Strong et al. 1997; Prattet al. 1998). With data on crop vegetation, border plants, mite levels and distribu-tions, and wind parameters, probabilities of movement in a diverse plant settingcan be modeled as a modified diffusion process with different reproduction/mortal-ity in each plant component (Greene and Johnson 1989; Jung 2001). Managementmodels are under study that use dispersal data, geographic information and datalayers for vegetation, soils etc. These tools will aid in evaluation of integrated mitemanagement tactics for field implementation.

Acknowledgements

We thank S. Blackwood and J.A. McMurtry and two journal referees for criticalreviews of this paper.

References

Bernstein C. 1983. Some aspects of Phytoseiulus persimilis (Acarina: Phytoseiidae) dispersal behaviour.Entomophaga 28: 185–198.

Bernstein C. 1984. Prey and predator emigration responses in the acarine system Tetranychus urticae –Phytoseiulus persimilis. Oecologia 61: 134–142.

Berry J.S. and Holtzer T.O. 1990. Ambulatory dispersal behavior of Neoseiulus fallacis (Acarina: Phy-toseiidae) in relation to prey density and temperature. Exp. Appl. Acarol 8: 253–279.

Berry J.S., Holtzer T.O. and Norman J.M. 1991. Experiments using a simulation model of the Banksgrass mite (Acarina: Tetranychidae) and the predatory mite, Neoseiulus fallacis (Acarina: Phytosei-idae) in a corn microenvironment. Environ. Entomol. 20: 1174–1178.

Blackwood J.S., Croft B.A. and Schausberger P. 2001. Prey stage preference of adult female phytoseiidmites (Acari: Phytoseiidae) when offered eggs and larvae of Tetranychus urticae (Acari: Tetrany-chidae). Environ. Entomol. (in press).

780

Boller E.F., Remund U. and Candolfi M.P. 1988. Hedges as potential sources of Typhlodromus pyri,predatory mite in vineyards of northern Switzerland. Entomophaga 33: 247–255.

Boykin L.S. and Campbell W.V. 1984. Wind dispersal of the Two-spotted spider mite (Acari: Tetrany-chidae) in North Carolina peanut fields. Environ. Entomol. 13: 221–227.

Brandenburg R.L. and Kennedy G.G. 1982. Intercrop relationships and spider mite dispersal in a corn/peanut agro-ecosystem. Entomol. Exp. Appl. 32: 269–276.

Charles J.G. and White V. 1988. Airborne dispersal of Phytoseiulus persimilis (Acriana: Pytoseiidae)from a raspberry Garden in New Zealand. Exp. Appl. Acarol. 5: 47–54.

Coop L.B. and Croft B.A. 1995. Neoseiulus fallacis: dispersal and biological control of Tetranychusurticae following minimal inoculations into a strawberry field. Exp. Appl. Acarol. 19: 31–43.

Croft B.A. 1997. Management of spider mites for biological control and pesticide resistance: A case oflandscape IPM for diverse agriculture in the Pacific Northwestern United States. Cpt. 3. In: Saito T.and Croft. B.A. (eds), Implementing Spider Mite Resistance Management Programs. Japan CropProt. Assoc. Tokoyo, Japan, pp. 27–66.

Croft B.A. and Coop L.B. 1998. Heat units, release rate, prey density, and plant age effects on dispersalby Neoseiulus fallacis (Acari: Phytoseiidae) after inoculation into strawberry. J. Econ. Entomol. 91:94–100.

Croft B.A. and Croft M.B. 1993. Larval survival and feeding by immature Metaseiulus occidentalis,Neoseiulus fallacis, Amblyseius andersoni and Typhlodromus pyri on life stage groups of Tetrany-chus urticae Koch and phytoseiid larvae. Exp. Appl. Acarol. 17: 685–693.

Croft B.A., Kim S.S. and Kim D.I. 1995a. Leaf residency and interleaf movement of four Phytoseiidmites (Acari: Phytoseiidae) on apple. Environ. Entomol. 24: 1344–1351.

Croft B.A., Kim S.S. and Kim D.I. 1995b. Absorption and cannibalism: do phytoseiids conserve eggresources when prey densities decline rapidly? Exp. Appl. Acarol. 19: 347–356.

Croft B.A., Luh H.-K. and Schausberger P. 1999. Larval size relative to larval feeding, cannibalism oflarvae, egg or adult female size and larval-adult setal patterns among 13 phytoseiid mite species.Exp. Appl. Acarol. 23: 1–12.

Croft B.A. and McGroarty D.L. 1977. The role of Amblyseius fallacis in Michigan apple orchards. Res.Rept. 33 Mich. Agric. Exp. Stn.: 48.

Croft B.A., Messing R.H., Dunley J.E. and Strong W.B. 1993. Effects of humidity on eggs and imma-tures of Neoseiulus fallacis, Amblyseius andersoni, Metaseiulus occidentalis and Typhlodromus pyri(Phytoseiidae): implications for biological control on apple, caneberry, strawberry and hop. Exp.Appl. Acarol. 17: 451–459.

Croft B.A., Monetti L.N. and Pratt P.D. 1997. Comparative life histories and predation types: Are Neo-seiulus californicus and N. fallacis (Acari: Phytoseiidae) similar Type II selective predators of spidermites? Environ. Entomol. 27: 531–538.

Croft B.A. and Zhang Z.Q. 1994. Walking, feeding and interaction of larvae of Metaseiulus occidenta-lis, Typhlodromus pyri, Neoseiulus fallacis and Amblyseius andersoni held with and without eggs ofTetranychus urticae. Exp. Appl. Acarol. 18: 567–580.

Dover M.J., Croft B.A., Welch S.M. and Tummala R.L. 1979. Biological control of Panonychus ulmi(Acarina: Tetranychidae) by Amblyseius fallacis (Acarina: Phytoseiidae) on apple: a Prey-PredatorModel. Environ. Entomol. 8: 282–292.

Dunley J.E. and Croft B.A. 1990. Dispersal between and colonization of apple by Metaseiulus occiden-talis and Typhlodromus pyri (Acarina: Phytoseiidae). Exp. Appl. Acarol. 10: 137–149.

Dunley J.E. and Croft B.A. 1992. Dispersal and gene flow of pesticide resistance traits in phytoseiid andtetranychid mites. Exp. Appl. Acarol. 14: 313–326.

Flexner J.F., Westigard P.H., Hilton R. and Croft B.A. 1995. Experimental evaluation of resistance man-agement for twospotted spider mite (Acari: Tetranychidae) on southern Oregon pear: 1987–1993. J.Econ. Entomol. 88: 1517–1524.

Greene D.F. and Johnson E.A. 1989. A model of wind dispersal of winged or plumed seeds. Ecol. 70:339–347.

Helle W. and Sabelis M.W. (eds) 1985a. Spider mites. Their Biology, Natural Enemies and Control.Elsevier, Amsterdam.

781

Helle W. and Sabelis M.W. (eds) 1985b. Spider mites. Their Biology, Natural Enemies and Control.Elsevier, Amsterdam.

Hislop R.G. and Prokopy R.J. 1981. Mite predator responses to prey and predator-emitted stimuli. J.Chem. Ecol. 7: 895–904.

Hoy M.A. 1982. Aerial dispersal and field efficacy of a genetically improved strain of the spider mitepredator Metaseiulus occidentalis. Entomol. Exp. Appl. 32: 205–212.

Hoy M.A. and Smilanick J.M. 1981. Non-random prey location by the phytoseiid predator Metaseiulusoccidentalis: differential responses to several spider mite species. Entomol. Exp. Appl. 26: 291–300.

Hoy M.J., Groot J.J. and van de Baan H.E. 1985. Influence of aerial dispersal on persistence and spreadof pesticide-resistant Metaseiulus occidentalis in California almond orchards. Entomol. Exp. Appl.37: 17–31.

Janssen A. 1999. Plants with spider-mite prey attract more predatory mites than clean plants undergreenhouse conditions. Entomol. Exp. Appl. 90: 191–198.

Janssen A., Bruin J., Jacobs G., Schraag R. and Sabelis M.W. 1997. Predators use volatiles to avoidprey patches with conspecifics. J. Anim. Ecol. 66: 223–232.

Johnson D.T. and Croft B.A. 1976. Laboratory study of the dispersal behavior of Amblyseius fallacis(Acarina: Phytoseiidae). Ann. Entomol. Soc. Am. 69: 1019–1023.

Johnson D.T. and Croft B.A. 1979. Factors affecting the dispersal of Amblyseius fallacis in an apple treeecosystem. In: Rodriguez J.G. (ed.), Recent advances in Acarology. Academy Press, New York, pp.477–483.

Johnson D.T. and Croft B.A. 1981. Dispersal of Amblyseius fallacis (Acarina: Phytoseiidae) in an appleEcosystem. Environ. Entomol. 10: 313–319.

Jung C. 2001. Ambulatory and aerial dispersal among specialist and generalist phytoseiid mites. PhDDissertation, Oregon State University, Corvallis, USA.

Jung C. and Croft B.A. 2000. Survival and plant-prey finding by Neoseiulus fallacis (Acari: Phytosei-idae) on soil substrates after aerial dispersal. Exp. Appl. Acarol. 24: 579–596.

Jung C. and Croft B.A. 2001a. Aerial dispersal of phytoseiid mites (Acari: Phytoseiidae): Estimatingfalling speed and dispersal distance of adult females. Oikos submitted.

Jung C. and Croft B.A. 2001b. Ambulatory and aerial dispersal among specialist and generalist preda-tory mites (Acari: Phytoseiidae). Environ. Entomol. (in prep).

Kogan M., Croft B.A. and Sutherst R.F. 1999. Applications of ecology for integrated pest management.In: Huffaker C.B. and Gutierrez A.P. (eds), Ecological entomology. 2nd edn. John Wiley & Sons,INC., New York, pp. 681–738.

Leetham J.W. and Jorgensen C.D. 1969. Overwintering phytsoseiid mites in central Utah apple orchards.Grt. Basin Nat. 29: 96–104.

Margolies D.C. 1987. Conditions eliciting aerial dispersal behavior in Banks Grass Mite, Oligonichuspratensis (Acari: Tetranychidae). Environ. Entomol. 16: 928–932.

McMurtry J.A. and Croft B.A. 1997. Life-styles of phytoseiid mites and their roles in biological control.Ann. Rev. Entomol. 42: 291–321.

McMurtry J.A. and Rodriguez J.G. 1987. Nutritional ecology of phytoseiid mites. In: F.S. Jr and Rod-riguez J.G. (eds), Nutritional ecology of insects, mites, spiders and related invertebrates. John Wiley& Sons, New York, pp. 609–644.

Miller R.W., Croft B.A. and Nelson R.D. 1985. Effects of early-season immigration on cyhexatin andformetanate resistance in Tetranychus urticae on strawberry in California. J. Econ. Entomol. 78:1379–1388.

Monetti L. and Croft B.A. 1997. Mating, cross-mating and related behaviors of Neoseiulus californicusand N. fallacis (Acari: Phytoseiidae). Exp. Appl. Acarol. 20: 67–71.

Morris M.A. 1998. Biological control of Tetranychus urticae (Koch) on peppermint by Neoseiulus fal-lacis (Garman): Density relationships, overwintering, habitat manipulation and pesticide effects. En-tomology. Oregon St. Univ., Corvallis, pp. 79.

Morris M.A., Croft B.A. and Berry R.E. 1996. Over-wintering and effects of autumn habitat manipula-tions and carbofuran on Neoseiulus fallacis and Tetranychus urticae in peppermint. Exp. Appl. Ac-arol. 20: 249–257.

782

Morris M.A., Berry R.E. and Croft B.A. 1999. Phytoseiid mites on peppermint and effectiveness ofNeoseiulus fallacis to control Tetranychus urticae in arid growing regions. J. Econ. Entomol. 92:1072–1078.

Morris M.A., Berry R.E. and Croft B.A. 2000. Fall flaming effects on densities, distributions and dis-persal of Tetranychus urticae and Neoseiulus fallacis (Acari: Tetranychidae, Phytoseiidae) on pep-permint. Environ. Entomol. 29: 95–100.

Nachman G. 1988. Regional persistence of locally unstable predator/prey populations. Exp. Appl. Ac-arol. 5: 293–318.

Nyrop J.P., Minns J. and Herring C. 1994. Influence of ground cover on dynamics of Amblyseius falla-cis Garman (Acarina: Phytoeiidae) in New York apple orchards. Agric. Ecosys. Environ. 50: 61–72.

Pels B. and Sabelis M.W. 1999. Local dynamics, overexploitation and predator dispersal in an acarinepredator-prey system. Oikos 86: 573–583.

Penman D.R. and Chapman R.B. 1980. Effect of temperature and humidity on the locomotory activityof Tetranychus urticae (Acari: Tetranychidae), Typhlodromus occidentalis and Amblyseius fallacis(Acarina: Phytoseiidae). Acta Ecologica 1: 253–269.

Pratt P.D. 1999. Biological control of spider mites by the predatory mite Neoseiulus fallacis (Acari:Phytoseiidae) in ornamental nursery plant systems. PhD Dissertation, Oregon State University, Cor-vallis, USA.

Pratt P.D., Monetti L.N. and Croft B.A. 1998. Within- and Between-Plant dispersal and distributions ofNeoseiulus californicus and N. fallacis (Acari: Phytoseiidae) in simulated bean and apple plant sys-tems. Environ. Entomol. 27: 148–153.

Pratt P.D., Schausberger P. and Croft B.A. 1999. Prey-food types of Neoseiulus fallacis (Acari: Phy-toseiidae) and literature versus experimentally derived prey-food estimates for five phytoseiid spe-cies. Exp. Appl. Acarol. 23: 551–565.

Prischmann D. 2000. Biological control of spider mites (Acari: Tetranychidae) on grape emphasizingregional aspects. MS thesis, Oregon State University, Corvallis, USA.

Putman W.L. 1959. Hibernation sites of phytoseiids (Acarina: Phytoseiidae) in Ontario peach orchards.Can. Entomol. 91: 735–741.

Ramakers and Voet 1995. Use of castor bean, Ricinus communis, for the introduction of the thripspredator Amblyseius degenerans on glasshouse grown sweet peppers. Med. Fac. Landbouw. Univ.Gent 60: 885–891.

Raworth D.A., Fauvel G. and Auger P. 1994. Location, reproduction and movement of Neoseiulus cali-fornicus (Acari: Phytoseiidae) during the autumn, winter and spring in orchards in the south ofFrance. Exp. Appl. Acarol. 18: 593–602.

Sabelis M.W. 1981. Biological control of two-spotted spider mites using phytoseiid predators. Agricul-tural research reports 910 pudoc., Wageningen.

Sabelis M.W. and Afman B.P. 1994. Synomone-induced suppression of take-off in the phytoseiid mitePhytoseiulus persimilis Athias-Henriot. Exp. Appl. Acarol. 18: 711–721.

Sabelis M.W. and van de Baan H.E. 1983. Location of distant spider mite colonies by phytoseiid preda-tors: Demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi.Entomol. Exp. appl. 33: 303–314.

Sabelis M.W. and Bakker F.M. 1992. How predatory mites cope with the web of their tetranychid prey:a functional view on dorsal chaetotaxy in the Phytoseiidae. Exp. Appl. Acarol. 16: 203–225.

Sabelis M.W. and Dicke M. 1985. Long-range dispersal and searching behaviour. In: Helle W. and Sa-belis M.W. (eds), Spider mites. Their biology, natural enemies and control. Elsevier, Amsterdam, pp.141–157.

Sabelis M.W., Diekmann O. and Janssen V.A.A. 1991. Metapopulation persistence despite local extinc-tion: predator-prey patch models of the Lotka-Volterra type. Biol. J. Linn. Soc. 42: 267–283.

Sabelis M.W., Vermaat J.E. and Groeneveld A. 1984. Arrestment responses of the predatory mite, Phy-toseiulus persimilis, to steep odour gradients of a kairomene. Physiological Entomology 9: 437–446.

Sabelis M.W. and van der Weel J.J. 1993. Anemotactic response of the preatory mite, Phytoseiulus per-similis Athias-henriot, and their role in prey finding. Exp. Appl. Acarol. 17: 521–529.

783

Schausberger P. and Croft B.A. 1999. Predation on and discrimination between con- and heterospecificeggs among specialist and generalist phytoseiid mites (Acari: Phytoseiidae). Environ. Entomol. 28:523–528.

Schausberger, Peter and Croft B.A. 2000. Nutritional benefits of intraguild predation and cannibalismamong generalist and specialist phytoseiid mites. Ecol. Entomol. 25: 473–480.

Smitley D.R. and Kennedy G.G. 1985. Photo-oriented aerial dispersal behavior of Tetranychus urticae(Acari: Tetranychidae) enhnaces escape from the leaf surface. Ann. Entomol. Soc. Am. 78: 609–614.

Stephens G.R. and Aylor D.E. 1978. Aerial dispersal of Red Pine Scale, Matsucoccus resinosae (Ho-moptera: Margarodidae). Envron. Entomol. 7: 556–563.

Strong W.B. and Croft B.A. 1995. Inoculative release of phytoseiid mites (Acarina: Phytoseiidae) intothe reapidly expanding canopy of hops for control of Tetranychus urticae (Acarina: Tetranychidae).Environ. Entomol. 24: 446–453.

Strong W.B., Croft B.A. and Slone D.H. 1997. Spatial aggregation and refugia of the mites and Tet-ranychus urticae and Neoseiulus fallacis (Acari: Tetranychidae, Phytoseiidae) on hop. Environ. En-tomol. 26: 859–865.

Strong W.B., Slone D.H. and Croft B.A. 1999. Hops as a metapopulation landscape for tetranychid-phytoseiid interactions: perspectives of intra- and interplant dispersal. Exp. Appl. Acarol. 23: 581–597.

Takafuji A. 1977. The effect of the rate of successful dispersal of a phytoseiid mite, Phytoseiulus per-similis Athias-Henriot (Acarina: Phytoseiidae) on the persistence in the interactive system betweenthe predator and its prey. Res. Popul. Ecol. 18: 210–222.

Tixier M.-S., Kreiter S. and Auger P. 2000. Colonization of vineyards by phytoseiid mites: their dis-persal patterns in the plot and their fate. Exp. Appl. Acarol. 24: 191–211.

Tixier M.-S., Kreiter S., Auger P. and Weber M. 1998. Colonization of Languedoc vineyards by phy-toseiid mites (Acari: Phytoseiidae): influence of wind and crop environment. Exp. Appl. Acarol. 22:523–542.

Turchin P. 1998. Quantitative analysis of movement. Measuring and modeling population redistributionin animals and plants. Sinauer Ass. Inc., Sunderlaand, MA.

Walde S.J., Nyrop J.P. and Hardman J.M. 1992. Dynamics of Panonychus ulmi and Typhlodromus pyri:factors contributing to persistence. Exp. Appl. Acarol. 14: 261–292.

Washburn J.O. and Washburn L. 1983. Active aerial dispersal of min wingless arthropods: Exploitationof boundary-layer velocity gradients. Science 23: 1088–1089.

Weyman G.S. 1993. A review of the possible causative factors and significance of ballooning in spiders.Ethol. Ecol. Evol. 5: 279–291.

Zhang Z.-Q. and Sanderson J.P. 1992. Short-distance location of spider mite colonies by three predatorymites (Acari: Tetyranychidae, Phytoseiidae): predator responses to prey-and preator-associated stim-uli. Environ. Entomol. 21: 799–807.

784