Experimental & Applied Acarology, 22 (1998) 523-542 .~~84

Colonization of Languedoc vineyardsbyphytoseiid mites (Acari: Phytoseiidae):

influence of wind and'crop environment

Marie-StéphaneTixier, Serge Kreiter*, Philippe Auger and Marc WeberbaEcole Nationale Supérieure Agronomique de Montpellier/Institut National de la Recherche

Agronomique, Département d'Ecologie et de Protection des Plantes, Laboratoire d'Acarologie,2 Place Pierre Viala, 34060 Montpellier cedex Dl, France

bService Régional de la Protection des Végétaux du Languedoc-Roussillon, DRAF, 2 Rued'Alco, 34034 Montpellier cedex Dl, France

(Received 5 June 1997; accepted 21 November 1997)

ABSTRACT

A natural increase of phytoseiid mite populations (Kampimodromus aberrans, Typhlodromuspyriand Phytoseius plumifer) was observed in vineyards in Languedoc, Burgundy and Corsica underintegrated pest management strategies. The aim of the present study was to characterize themechanisms of this colonization in space and time in Languedoc. The abundance of phytoseiidmites in th.e vegetation close to three grape fields was determined twice a year (May and July).Aerial (funnels with water) and soil (felt strip) traps were placed in and around grape fields, inorder to assess the colonization potential provided by aerial dispersaI and ambulatory locomotion.The populations of phytoseiid mites in the crops were studied twiee a month in order to gaininformation on the make up of the dispersai populations. The species K. aberrans was found inlargest quantities in the traps, in the naturaI vegetation and in the crops. Predatory mite dispersaIoccurred essentiaIly by aerial dispersaI and was dependent on the wind intensity and winddirection. Identical sex ratios were observed in migrant populations and in populations present inthe grape fields, woody areas and hedges. A large proportion of immatures was found to move byaerial dispersaI. The colonization potential (rapidity, intensity and regularity) was directlyassociated with the abundance of the phytoseiids and the proximity of natural vegetation. A deep,dense and taIl woody area containing suitable host plants for predatory mites constituted the moststable source of phytoseiid mites. Natural colonization of vineyards provides considerablephytoseiid mite potential that could be managed in an agricultural landscape.Exp Appl Acarol 22: 523-542 @ 1998 Kluwer Academic Publishers

Key words: Vineyards, phytoseiid mites, Kampimodromus aberrans, Typhlodromus pyri,Phytoseius plumifer, dispersaI, woody areas, hedges, Phytoseiidae.

4

INTRODUCTION

Panonychus ulmi, Eotetranychus carpini and Tetranychus urticae are among themajor pests occurring in French vineyards (Sentenac et al., 1993). Systematic

* To whom correspondence should be addressed at: Tel: 00 33 4 99 61 2389; Fax: 00 33 4 67 52 1554;e-mail: kreiter@ensam.inra.fr

0168-8162 @ 1998 Kluwer Academie Publishers

- ------------ - -- - - - - - - - - -----

524 M.-S. TIXIER ET AL.

chemical control since the early 1950s has limited their damage (Delmas andRambier, 1954), but spraying presents economical and ecologicaI drawbacks whichmilitate for integrated pest management (Baillod, 1984). The main naturaI enemiesof phytophagous mites in grapevine in France are phytoseiid mites (Kreiter et al.,1993). AlI species are generalist predators, permanent inhabitants and ensure rapidcontrol of pest populations early in their development (McMurtry, 1992; Kreiterand Sentenac, 1995; McMurtry and Croft, 1997). Kampimodromus aberrans,Typhlodromus (Typhlodromus) pyri and Phytoseius plumifer are the three mainspecies and play a major role in European red mite control in French vineyards(Kreiter et al., 1993). lnoculative releases which have been shown to be successfulin controlling spider mite populations (Sentenac et al., 1993) are difficult andexpensive to apply to aImost 1 million ha subjected to spider mite infestation.Furthermore, mass breeding is not possible because of the low reproductive rate ofthese phytoseiid mites species. Corino (1989) in ltaly and Kreiter and Sentenac(1995) in Burgundy, France, reported on the rapid restoration of phytoseiid mitepopulations in vineyards farmed under integrated pest management. This phenom-enon, which appears to be linked to plot 'colonization', involves the maintenance ofa rich and varied surrounding vegetation from which natural enemies could dispersetowards the crops. Few studies actually deal with the colonization procedures ofphytoseiid mites. The large-scale movement of predatory mites has already beenstudied (Johnson and Croft, 1976, 1979 and 1981; Hoy et al., 1984, 1985; Dunleyand Croft, 1990, 1992, 1994). Phytoseiid mites are able to move by using aerialdispersaI and ambulatory locomotion (Sabelis and Dicke, 1985). These movementsare believed to occur because of a declining habitat, resulting from overcrowding,poor food quality, predator avoidance and yearly plant senescence (Price, 1984).Hamilton and May (1977) developed a dispersaI model and concluded that it was tothe advantage of insects living in both stable and unstable environments that aportion of its offspring disperses. Concerning phytoseiid mite habitats, severalauthors (Boller et al., 1988; Tuovinen and Rokx, 1991; Duso et al., 1993; Sentenacet al., 1993; Tuovinen, 1993a,b,c; Barret, 1994; Kreiter and Sentenac, 1995) haveshown that the natural vegetation near plots with crops is rich in phytoseiidmites.

The literature reports on plot colonization are scarce and do not concern the threemain species of predatory mites in French vineyards. ln order for colonization todevelop within a framework of conservation biocontrol, a national research projectwas set up over 3 years (1996-1998) in Corsica, Burgundy and Languedoc. Theaim of the study was to obtain answers to the following questions: what potentialis present in the vegetation surrounding the cultivated plots? Are phytoseiid mitescolonizing cultivated plots? Where do colonizing phytoseiid mites corne from?What is the magnitude of the colonizing flow? How does it vary in time? Whatfactors influence dispersaI? Which species are inclined to disperse?

_uu - n- -- -- --- -- _u --------

COLONIZATION OF VINEYARDS BY PHYTOSEIID MITES 525

MATERIALS AND METHODS

The vineyards studiedColonization was studied in three grapevine plots located in the Hérault (theLanguedoc region, south of France). The third plot yielded little information andresults dealing with this plot are not given here. The grape fields chosen aremaintained under an integrated pest management programme and are bordered by amore or less taU and thick vegetation which contained phytoseiid mites in 1995when the first samples were taken. The phytoseiid mite populations present in plot2 were kiUed by chemical treatments (dinocap) in 1995 (Table 1).

Grape field surroundingsTwo kinds of uncultivated areas surrounding the grape fields were studied: woodyareas with dense and woody trees and bushes and border hedges with narrow bandsof vegetation (Fig. 1). These were sampled twice a year: the woody areas on 21April and 23 July and the border hedges on 4 June and 7 August. AU of the plantswere sampled by taking at least 30 leaves randomly from at least one plant of eachspecIes.

An index called WR (woody richness) is proposed to estimate the phytoseiidmite abundance in the woody areas. The WR index inc1udes the abundance and

TABLE 1

Characteristics of the two experimental grape fields and their woody areas

Vine cultivar

Surface

Plantation density

Phytoseiid mites observedin grape fields in 1995

Treatments applied in 1996Fungicides

InsecticidesAcaricides

Woody areas sunace

Woody areas location

Phytoseiid mites present inthe woody areas in 1995

Grape field 1 Grape field 2

Syrah0.8 ha

2.5 X l.l m

Cabernet-Sauvignon

1.6 ha

2.5 X 1 m

KampimodremusK. aberrans (Dudemans)

T. (T.) phialatus Athias-HenriotK. aberrans

Nuarimol, ofurace, folpel,cymoxanyl, mancozebe, fosetyl AI,copper, zinebe and sulphurFlufenoxuron

Bromopropylate and cyhexatin1500 m2

Height: 12 mWest

K. aberrans

Fosetyl Al, folpel, flusilazole,penconazole and sulphur

Flufenoxuron

Propargite and tetradifon2000 m2

Height: 10 mNorth east

T. (T.) phialatus. T. (A.) intercalaris(Livschitz and Kuznetzov),E. stipulatus (Athias-Henriot),T. seiulus simplex (Berlese),T. (T.) pyri Scheuten and K. aberrans

--

526 M.-S. TIXIER ET AL.

"~::.:;r:':~~::~~~j::~'.(~:'::::i~:-'W'~::';;:. ~.!:':>';:~~~:~~~::~~~~~.!:':>';:~~~'.;~.!~

~p',*s.~\f~s.~~'îll.~~~~~1J~'"'~4:":--.':"1'3 fi -:.~:'I{~"..<~...::«. . ~...:.~. a.~o(.,:~..;.'r.,:~..;.'r.,:~

.~: ':>';"!~~':>.;?:~~:.~ "':~~:.~ "':~~;~)~~~~~(st,,~~~st"~J'~st,,~~::""':I\',,,,, ~\.".,~1.'\.".,- ~ .'';'~~y}~~r-~~"::r-~~"::~.

:5:t~~.~';j,~~.~';i\~~~';i,:

Scale

20 tvinestockst 1( .

7 vinestocks

tN.W. wind direction

Grape field 1

Scale

vines~ocks 11( .

20 vinestocks

Grape field 2

Fig. 1. Trap locations and surrounding environment characteristics of grape fields 1 and 2.

. arieltrapsI.':; neighbouring vine crops\îl}. woody margins. hedge margins. soi! traps

- --- ----

COLONIZATION OF VINEYARDS BY PHYTOSEIID MITES 527

dominance of the plant species and their richness in phytoseiid mites per leaf(Ph 1-1).

WR index = ~ (abundance-dominance of plant X richness (Ph 1-1)of each plant species present)

The scale of abundance and dominance used is as follows.

(1) Level 1: plants that are rare or not very abundant, comprising 5% ofcanopy.

(2) Level 2: abundant plants, comprising 5-25% of canopy.(3) Level 3: abundant plants, comprising 25-50% of canopy.(4) Leve14: very abundant plants, comprising 50-75% of canopy.(5) Level 5: very abundant plants, comprising 75-100% of canopy.

Samples (one leaf per 20 vine stocks) were taken on 18 July from other grape fieldssUIToundingthe experimental plots (Fig. 1).

Considering the number of leaf samples to collect, phytoseiid mites species toidentify and the number of mites °tocount, it was impossible to perfonn the varioussamplings at exactly the same time. However, the sampling dates were as close aspossible.

Phytoseiid mites were removed from the leaves by using the soak-washextraction method of Boller (1984) or by using the method of Berlese-Tullgren, forwhich escapes and losses are negligible (S. Kreiter, unpublished data). The miteswere placed on 100 J-Lmsieves and observed under a binocular microscope. Theywere then mounted on slides and identified. For identification, the works of deMoraes et ai. (1986) and Chant and McMurtry (1994) were used.

Phytoseiid mite dispersaiSixteen ground traps per hectare to measure the ambulatory dispersaI and sixteenaerial traps per hectare to assess the airbome dispersaI were placed in the grapefields.

Drugget strips (20 X 5 cm) imbibed with pine pollen with no olfactory attraction(P. Auger and S. Kreiter, unpublished data) were used as ground traps and placedin open-sided boxes (25 X 10 cm) to protect the strips against rain, so that theambulatory dispersaI of the mites could be the only explanation for their presencein the trap. Drugget is a coarsely woven felt cloth that acts as a shelter forphytoseiid mites, which remain inside the trap because of the food. The druggetstrips were renewed every week and after removaI placed in Berlese- Tullgrenfunnels for 1 week in order to extract phytoseiid mites.

For the study of aeriaI dispersaI, an experimental device similar to that used byFauvel and Cotton (1981) was chosen. Aerial traps were made with funnels (31 cmin diameter) filled with water and a wetting agent (Teepol~\ Le Blanc Mesnil,France). They were glued (The Tanglefoot@Company,.Grand Rapids, USA) tosupports and placed approximately 50 cm above the vines, approximately 2 m fromground level. This limited or excluded the possibility of trapping phytoseiid mites

- - - _u uu _u -

528 M.-S. TIXIER ET AL.

originating from the vine stocks in the experimental plot. Each week the contents ofthe funnels were filtered through a 100 fJ.msieve. The phytoseiid mites were thenidentified after c1earing and mounting in the laboratory. Data conceming the mitestrapped in the funnels throughout the season were anaIysed using an analysis ofvariance followed by a Newman and Keuls means comparison test (Sokal andRohlf, 1980).

The influence of the wind was studied. Wind data were provided by the Frenchmeteorological office (Météo France, Pézénas) located 15 km from the grape fields.Winds from the north-north west and south-south east are the strongest and themost frequent, the former considered as the prevailing wind in the Languedoc. lnthe literature, dispersaI indices are usually used to describe the statisticaI distribu-tion of species. They do not take into account the factors causing dispersaI. AdispersaI index (DI) linking the number of migrants (by air) to the main factorscausing dispersaI (wind data and phytoseiid mites abundance in the surroundingvegetation) is proposed here. This index is based on the assumption that winddispersaI is at random. The velocity and frequency of the two directions mentionedabove over 1 week were chosen as the wind parameters. Only the woody vegetationwas used for the estimation of the dispersaI index as the abundancy of phytoseiidmites (number of mites per leat) was the largest in this vegetation. The develop-ment of phytoseiid mite populations was considered to be linear between the twosampling dates. The DI proposed is necessarily theoretical, as it takes into accountonly one providing area and a hypothetical increase in the number of phytoseiidmites.

DI = number of days of wind from south-south east or north-north west Xweekly mean velocity of wind from this direction X richness of woody area

in phytoseiid mites per leaf

ln order to define the populations of phytoseiid mites inside the plots with precisionat the beginning of the study, a pre-sampling (30 April) was done. An analysis ofvariance (a = 5%) followedby a Newmanand Keuls means comparisontest wascarried out to create homogeneous blocks. Samples were taken every 15 days. Themites were removed by Berlese- TuIlgren funnels or soak-wash extraction methods,and then identified.

The presence of phytoseiid mites on dead leaves found on the ground in thegrape fields was studied in the autumn (31 October). Vine leaves were distinguishedfrom those of other plants.

RESULTS

Characteristics of the surrounding environmentPhytoseiid mites were found in the immediate surroundings of the grape fields in aIlthree categories of veg~tation: woody areas, border hedges and neighbouring grapefields (Tables 3, 6 and 7).

-- d- -

COLONIZA TION OF VINEY ARDS BY PHYTOSEIID MITES 529

TABLE 2

Number and percentage of phytoseiid mites trapped in aerial and soil traps -iDthe grape fields: sex ratio andtrapped immatures during 1996 experiment (April-October)

The presence of phytoseiid mites was studied for each plant species. Ten plantsout of 67 sampled were found with high densities of predatory mites. The numberof phytoseiid mites per leaf was over 0.5. Eight of these plants harboured mainlyK. aberrans. The remarkably dense woody area bordering grape field 1 wascharacterized by a taU oak stand and the presence of Celtis australis L., Cornus sp.,Rubus sp., Agrimonia eupatoria L. and Euphorbia characias L. This area containedhigh densities of phytoseiid mites and had the highest WR index (Table 3). Thewoody area of grape field 2 is less dense and taU with only Quercus pubescensWilld., Rubus sp. and E. characias of the ten most suitable host plants. The WRindex in this case is lower. The woody areas of each grape field differed not onlyin their plant species and their richness in phytoseiid mites, but also in the speciesof predatory mites observed (Table 4). Kampimodromus aberrans occurred mostfrequently (90%) in the woody area of grape field 1. The woody area of grape field2 was characterized by smaU populations of K. aberrans and large numbersof Typhlodromus (Anthoseius) intercalaris and Typhlodromus (Typhlodromus)phialatus (Table 4).

The border hedges along each of the two fields harboured few phytoseiid mites(Table 6). They were low and narrow and contained few of the good host plants.The richest hedges were those of grape field 1, where K. aberrans was mostprevalent.

The surrounding vineyards all contained phytoseiid mites. Those surround-ing grape field 1 were particularly rich, notably the vineyard situated to the east

Grape field 1 Grape field 2

Aerial Soil Aerial Soil

Number of captured phytoseiid mites per trap 18.2 0.96 5 0.75K. aberrans 87% Trapped 66% TrappedT. (T.) pyria 1% 4%

T. (T.) phialatusa 6% 18%

T. (A.) intercalarisa 6% Trapped 2%

Paraseiulus soleiger (Ribaga)a 2%

S. simplex 4%

Neoseiulus aurescens (Athias-Henriot) 2%

Neoseiulus californicus (McGregor) 2%

Proprioseiopsis messor (Wainstein) Trapped TrappedTyphlodromus (Anthoseius) commenticius Trapped

(Livschitz and Kuznetzov)aNeoseiulus bicaudus (Wainstein) TrappedTyphlodromus (Anthoseius) recki (Wainstein)a Trapped Trapped

Sex ratio (female: male) 67.5: 32.5 71: 29 71 : 29 65: 35Immature forms 35% 1% 35% 0%

a After Chant and McMurtry (1994).

um --- --.

530 M.-S. TIXIER ET AL

TABLE 3

Richness of woody areas of the two experimental grape fields

WR index.

Number of sampled plantsProportion of plants with phytoseiid mites (%)Mean number of phytoseiid mites per leaf for plants with phytoseiid mitesPercentage of richness associated with the ten suitable host plants

Grape field 1

8.232945

0.4488

Grape field 2

2.9936300.13

83

. WR index =sum of (abundance-dominance X richness (Ph 1-1) of each plant species present).

TABLE 4

Percentage of phytoseiid mite species observed in woody areas

Grape field 1 Grape field 2

K. aberrans

T. (A.) intercalarisT. (T.) phialatusT. (T.) pyriE. stipulatusP. soleiger

90.02.51.04.52.0

4726137

7

TABLE 5

Number of phytoseiid mites per leaf (Ph 1-1)and species observed on suitable host plants

Woody areas %

of grape fields Ph 1-1 K. aberrans Other species

A. eupatoria L. 1 1.00 80.0 T. pyri (14%) T. phialatus (4%) andT. intercalaris (2%)

E. characias L. 1,2 1.00 92.5 T. pyri (7.5%)C. australis L. 1 0.80 100.0

Q. pubescens Willd. 1,2 0.70 80.0 T. intercalaris (20%)Cornus sp. 1 0.70 94.0 E. stipulatus (6%)Ulmus sp. l, 3 0.60 100.0

Rubus sp. 1, 2 0.30 72.0 T. pyri (16%) and E. stipulatus (12%)lnula viscosa L. 2 0.50 34.0 T. intercalaris (33%) and P. soleiger (33%)Prunus cerasus L. 3 0.50 0.0 P. soleiger (100%)Cydonia oblonga Mill. 3 0.50 100.0Mean 0.66 75.1Standard deviation 0.22 33.0

COLONIZATION OF VINEYARDS BY PHYTOSEIID MITES

TABLE 6

531

Percentage of phytoseiid mite species observed in narrow hedges around thegrape fields

K. aberrans

T. (T.) phialatusS. simplexT. (A.) intercalarisPhytoseiid mites per leaf

Grape field 1

100.0

0.3

Grape field 2

34.0030.00

8.0028.000.04

TABLE 7

Number of phytoseiid mites per leaf and phytoseiid mite proportions observed in neighbouring vine crops

Total area of the neighbouring vine crops (ha)Phytoseiid mite density in Ph 1-1 in the neighbouring vine crops

Number 12345

K. aberrans

T. (T.) pyri ScheutenT. (T.) phialatus Athias-HenriotT. (A.) intercalarisP. soleiger (Ribaga)

TABLE 8

Phytoseiid mites sex ratio in the three surrounding environments

(7.5 Ph 1-1) (Table 7). Kampimodromus aberrans was the main species in aIlvineyards. Slightly more species of phytoseiid mites were found in the vineyardsneighbouring grape field 2 (Table 7).

The sex ratios for the phytoseiid mite populations present in those threeenvironments were not significantly different (X2 test, (ï = 5%) (Table 8).

....

....

Grape field 1 Grape field 2

4.70 1.60

2.37 2.807.50 1.020.60 3.720.70 0.06

0.0475.00% 97.40%23.75%

1.25% 0.60%1.2%0.80%

Woodyareas Border hedges Neighbouring vineyards(%) (%) (%)

Females 80 79 78Males 20 21 22

- --. -.-u---- --

532 M.-S. TIXIER ET AL.

AeriaI and ambuIatory dispersaIThe predatory mites were caught in aerial and soil traps, but the numbers caught inthe aerial traps were by far the largest (Table 2). Most of the mites were capturedin grape field 1 (Table 2). Kampimodromus aberrans was the most frequent speciestrapped in the aerial traps of this plot. A larger number of species was trapped ingrape field 2, where K. aberrans represented only 66% of the species (Table 2). Thesex ratios for the phytoseiid mites captured in grape fields 1 and 2 were similar(Table 2) and were not significantly different from that of the populations presentin the three types of surrounding vegetation (X2test, a = 5%). A significant numberof immatures were captured in the funnels (35%) (Table 2). The number of mitescaptured in time (Figs 2 and 3) increased regularly from 21 May in grape field 1and from 18 June in grape field 2, reaching a maximum number in early July (9 Julyin grape field 1 and 2 July in grape field 2). Some phytoseiid mites were trapped aslate as 30 October.

The DI for the prevailing winds (north-north west) appeared to be significantlycorrelated with the numbers of phytoseiid mites trapped each week in grape field 1(Fig. 2). ln grape field 2 the correlation index was lower (Fig. 3). There was nosignificant correlation in the case of the south east wind, which is rather rare in thereglOn.

There was a considerable variation in the number of mites trapped in the funnelswithin the same grape field. Details of the results are only given for grape field 1because of the largest number of mites (Table 2) trapped in this field. Twosignificantly different groups of traps are identified using the Newman and Keulstest (Fig. 4). The funnels located in the centre of the field have the lowest number

250

200 ~a.a.1\1.:::

150 ~ëi>en0

~100 a.

'0

~E

50 ~

c::::::::J Phytoseiid mites trapped

-ll-N-NW wind

-6-S-SE wind

0

04-jun 18-jun 02-jul 16-jul

Fig. 2. Correlations between the total number of phytoseiid mites trapped and the DI for thenorth-north west and south-south east directions in grape field 1: r =0.81 and 0.04 for north-nOrth west and south-south east, respectively.

90

80

70

60

x50

.

9 40

30

20

10

0

21 may

COLONIZATION OF VINEYARDS BY PHYTOSEIID MITES

60 14

50

40

12 ~a.a.

10 ~1/)

:g8 ci)1/)

0>-

6 -a.'0

4 Q).DE:J

2 Z

xQ)

"0.!; 30

q20

10

0

21 may

0

04-jun 18-jun 02-jul 16-jul

533

t:::::I Phytoseiid mites trappt

---N-NW wind--&-S-SE wind

Fig. 3. COlTelationsbetween the total number of phytoseiid llÙtes trapped and the DI for thenorth-north west and south-south east directions in grape field 2: ,-2=0.48 and 0.02 for north-north west and south-south east, respectively.

"U

~ 50a.~ 45Cf)

2 40

~ ~ 35.- ::J°Q)-Cf) L: 300 u

~ m 25a.c:0'- 20....a>.DE::JZ

East neighbouringvine crop (9 phil)

Woody.margins

.

1510

5

0

\

Traps at theeast border

Traps in the middleof the plot

Traps at thewest border

Fig.4. Number of phytoseiid llÙtestrapped between 13-V and Ol-X and location in grape field 1.

of trapped mites, while the funnels located near the border of the woody area(West) and near the adjacent vine plot to the east have the highest numbers oftrapped mites. The first phytoseiid mites trapped were also found in the funnelslocated near the woody area. Phytoseiid mites were trapped next in the funnelslocated in the eastem part of the field near the adjacent vine plot, and only later in

534 M.-S. TIXIER ET AL.

14

"0 12~a.~ 10CI):g°3j 8~~ 6ë~ 4E~ 2

-.-grape field 1

--0- grape field 2

o. .

13 21 28 04- 11- 18. 25- 09- 23- 30- 07 20 05- 01- 30-

maymaymay jun jun jun jun jul jul jul aug aug sep oct oct

Fig.50 Phytoseiid mites trapped in soi! traps of experimental grape fields 1 and 2 between 13-Vand 30-X.

the central part of the grape field. There was an apparent relation between thelocation of the funnels and particularly their c10seness to estimated pool areasandthe time lag between the first trappings.

Kampimodromus aberrans was trapped in aIl funnels in grape field l, whereasT. pyri, T. phialatus and T. intercalaris occurred in the funnels located near woodyareas. Typhlodromus phialatus was also present in the traps located along the vineplot adjacent to the field on the east.

The first soil trappings took place at approximately the same time in fields 1 and2. The variation of trappings over time was very irregular.(Fig. 5). Phytoseiid miteswere trapped mainly in the traps situated along the edges of the fields, particularlyalong the woody areas. Kampimodromus aberrans was never found in the trapslocated in the centre of the field, despite the fact that it is the prevalent species inthe vine plot. On the other hand, T. intercalaris occurred in the intrafield traps, Le.those located along the border of field 1 and the adjacent vine plot to the east. Thespecies found in the soil traps usually differed from those found in the aerial traps.Only T. intercalaris, K. aberrans and T.pyri were trapped in both the soil and aerialtraps (Table 2). The sex ratio of the mites found in the soil traps was notsignificantly different (X2test, ex= 5%) from the sex ratios of the mites trapped inthe funnels and the populations present in the surrounding vegetation. The numberof immatures found in these traps was very low (Table 2).

The populations of phytoseiid mites within the grape fieldsPhytoseiid mites were observed in both grape fields but the largest populations wereobserved in grape field 1. The populations increased early in the season until18 June. The numbers dropped then probably due to the application of severalfungicides to control downy and powdery mildew and of an acaricide to control

COLONIZA TION OF VINEY ARDS BY PHYTOSEIID MITES 535

0.7

0.1

~grape field2

~grape field 1

0.6

16~ 0.5

~VI

"t)

:~ 0.4VI0>.~c.0 0.3

ZE~ 0.2

0

02

may

28

may

18-

jun

02-

jul

16-

jul

30-

jul21

aug

05-sep

01-oct

Fig.6. Number of phytoseiid mites sampled in the two experimental grape fields between 02-Vand Ol-X.

the swarms of E. carpini which were very abundant in 1996 (Fig. 6). Until theapplication of the fungicides, the population development and the number ofphytoseiid mites trapped showed a relatively identical increase, although thisphenomenon was less clear for the mites collected in the soil traps.

Kampimodromus aberrans accounted for 99% of the phytoseiid mites found infield 1 and 88% of those found in field 2. Typhlodromus phialatus (9%) occurredrelatively abundantly in this latter field. A X2 test (ex= 5%) showed that the sexratio of the phytoseiid mites present in the experimental grape fields was notsignificantly different from that of the mites present in the surrounding vegetationor from that of the trapped phytoseiid mites (in both aerial and soil traps).

Eight K. aberrans individuals were observed on fallen oak leaves in the sectionof the plot near the woody area of the grape field 1. One K. aberrans individual wasalso found in the centre section of field 2, but it was not found on a vine leaf.

DISCUSSION

Characteristics of the surrounding vegetationPhytoseiid mites were present on the vegetation surrounding the grape fields. Thepredatory mites found around each field varied in species and density. The richnessof phytoseiid mites in the bordering woody areas seemed to depend on three main

--no_. ---------- - -. - - ---

536 M.-S. TIXIER ET AL.

factors: plant composition, the structure of the environment and the pesticides usedin the grape fields.

The plant composition and dominance and abundance of the host plants forpredatory mites seems to be particularly important. AIl plant species observed havealready been mentioned as suitable host plants for phytoseiid mites, with theexception of E. characias and A. eupatoria. The occurrence of K. aberrans hadalready been observed only on Q. pubescens, C. australis and Rubus sp. (Boller etal., 1988; Duso et al., 1993; Sentenac et al., 1993; Barret, 1994). The present studyhas extended the list of phytoseiid mites and of suitable host plants, notably thoseof K. aberrans. The ten suitable plant species are perennials and annuals andshrubby and herbaceous species. However, they aIl have hairy foliage. Barret(1994) showed the importance of phylloplane architecture, in particular of the hairystructure, for the development of small phytoseiid mite species. Kampimodromusaberrans, T.phialatus and T.pyri occur in higher densities on leaves with pubescentunder surfaces and well-developed domatiae (Barret and Kreiter, 1992; Barret,1994; Camporese and Duso, 1996). Complex hairy structures act as shelters forpredatory mites and seem to capture pollen on which the mites feed (S. Kreiter,D. Barret and S. Rousset, unpublished data). Only these small species have accessto the surface where they can feed without interspecific competition with moreprolific and voracious macropredators. The phytoseiid mite abundance also seemsto depend on the structure of the woody areas. Environments with tall, dense anddeep vegetation like those bordering field 1 ensure greater phytoseiid mite potential.Chemical treatments reach areas surrounding the fields, but such a deep and tallenvironment limits the impact of spraying on phytoseiid mites. At the same time,these structural factors could be an explanation for the small phytoseiid mitespopulations observed in border hedges. The greater density also explains the timegaps in the first trappings inside the two fields, as captures occurred earlier in thetraps near environments with greater numbers of phytoseiid mites.

The diversity of phytoseiid mite species found on the vine leaves and in thefunnels seemed to reflect that of the species in the surrounding vegetation. The sexratios of phytoseiid mites in the 'source' and 'pool' environments and those trappedwere not significantly different. DispersaI probably links the crop plots and theareas with natural vegetation. Of the surrounding areas, the woody areas appear tobe the more efficient 'source'. The strong correlation between the DI and thenumbers trapped in field 1 seemed to confirm that the woody areas were the mainphytoseiid mites 'source'. ln grape field 2, the weaker correlation could not only belinked to a bad woody area orientation but this result may also show the existenceof other secondary 'source' areas that were not determined. Because of theirstructure and plant composition, the narrow border hedges are apparently not agood 'source' of phytoseiid mites. Although the neighbouring vineyards were richin phytoseiid mites, they did not appear to influence the phytoseiid mite dispersaIsignificantly except when the vineyards were actually adjacent and had particularlyhigh phytoseiid mite densities (vineyard adjacent to the east of grape field 1). Theheight of the surrounding vegetation might also have an influence on dispersaI,

COLONIZA TION OF VINEY ARDS BY PHYTOSEIID MITES 537

taller vegetation like that of the woody areas being more sensitive to air currents. lnaddition to structural differences, vine plots are less stable and more randomenvironments because of the chemicaI treatments previously used in the fields.Consequently, the phytoseiid mite abundance in these areas was less constant anddispersaI from these zones was more random than that from the woody areas.

Phytoseiid mite dispersaiSeveraI species of phytoseiid mites are liable to disperse in an aerial and/orambulatory manner. These results comply with previous observations on otherphytoseiid mite species in the laboratory (Sabelis and Dicke, 1985) and in the field(Hoy et al., 1984, 1985). Furthermore, aeriaI dispersai occurs to a greater extentthan ambulatory dispersai. This result may be due to a better capacity of phytoseiidmites to disperse by air, but it can also be linked to the presence of few phytoseiidmites in the soil and/or an insufficient number of soil traps which, moreover,covered smaller surfaces than the aerial traps. Dead fallen leaves could alsotransport phytoseiid mites, but this dispersai mode appeared relatively insignificant.The numbers of dispersed mites and the numbers of those observed in the crop plotsincreased together. However, it cannot be established that dispersing phytoseiidmites colonized the fields. These observations could reflect an identicaI naturaIpopulation increase both inside the fields and in the reservoir areas, with con-sequences for the numbers found in the traps. The increases would then be directlyrelated to the climatic conditions in the fields.

The species trapped at the ground level were generaIly not the same as thosetrapped in the air. Some species seemed to disperse only by ambulatory displace-ment and others by aerial dispersaI. The species trapped in the drugget strips weresoil or herbaceous stratum species (de Moraes et al., 1986). Those trapped in thefunnels seemed to be tree inhabitants (de Moraes et al., 1986) and therefore morelikely to be carried by air currents. However, T. intercalaris, K. aberrans and T.pyriwere trapped in aerial and soil traps. After an aeriaI dispersaI the species wouldwalk in order to reach a new host plant. This result seems to indicate the greaterdispersaI capacity of these three species, particularly of T. intercalaris andK. aberrans.

Among the eight species trapped, K. aberrans seems to be the most mobile.Some data (M.-!. Perrot-Minnot, L. Grassart, D. Barret and S. Kreiter, unpublisheddata) has revealed that this species has a low rate of dispersaI in relatively stableenvironments. It is possible that population dispersaI is variable and depends on theenvironment. ln a less suitable, less stable environment, dispersing populationsbecome more numerous, if not predominant. Some authors (Hamilton and May,1977) have shown that dispersai contributes to environmental stability. An environ-ment particularly rich in K. aberrans would send its excess population to disperseto poorer environments (source-pool theory). It was not possible in the frameworkof our experiment to specify the portion of a given phytoseiid mite population thatdispersed, nor to conclude on the dispersaI capacity of the different species trapped.

-

- - -----

538 M.-S. TIXIER ET AL

The numbers of K. aberrans trapped, which seemed very important, could representonly a very small proportion of the populations present in the sources.

The sex ratio of the species found in the soil and aerial traps shows that malesand females have similar dispersal properties in air and on land. The same types ofresults concerning the aerial dispersion of Neoseiulus fallacis (Johnson and Croft,1979) and Typhlodromus occidenta/is (Hoy.et al., 1984, 1985) have been obtained.However, most of the literature to date presents the females, particularly gravidfemales, as being the most dispersing. Gravid females would be solely responsiblefor ensuring the development of a colony and therefore population expansion andsurvival in the face of unsuitable environmental conditions (Sabelis and Dicke,1985). The fact that those results were obtained in the laboratory and concemedspecies of phytoseiid mites other than those trapped in our experiment mightexplain these differences. Equally, a considerable number of immatures was foundin the aerial traps. Dispersion in these stages was shown for N. fallacis by Johnsonand Croft (1979) and for Phytoseiulus persimilis by Van de Vrie and Price (1995).However, tests carried out under laboratory conditions for other species ofphytoseiid mites have not led to the same conclusions. Immatures, however, seemlittle inclined to ambulatory dispersaI. Perhaps this mean of locomotion requires toomuch energy for these stages, which would tend to adopt aerial transport as lesstaxing and 'more passive'. ,

The distribution of the soil and aerial captures supports the hypothesis thatphytoseiid mites corne from woody areas. The heterogeneous distribution of theaerial captures leads to the hypothesis that the phytoseiid mites did not corne fromvery far away. Phytoseiid mite species were trapped at 30 m from the supposedsource areas in grape field 1 and at 90 m in grape field 2. Aerial movement mightbe adopted for long-distance dispersai, whereas ambulatory dispersai would bebetter adapted to shorter displacements. However, T. intercalaris was found twice insoil traps far (60 m) from areas rich in this species. This might be a case ofparticularly long-distance ambulatory dispersaI. A combination of the two dispersaImodes, aerial at first and then ambulatory, would seem to be the most probablehypothesis. However, even in this case, the distances covered in aerial dispersaIvaried according to the species. Kampimodromus aberrans was observed todisperse the furthest, whereas T.pyri and T. intercalaris were found mostly in trapslocated near the border of the woody area. This would confirm observations thatT. pyri only disperses over short distances (12 m) (Dunley and Croft, 1990, 1992).Typhlodromus phialatus was also found mostly in the traps bordering the woodyarea, but equally in traps far from this area. This could indicate the existence ofother source areas or a strong dispersal capacity in this species. The dispersaIcharacteristics of the various species observed in the funnels was not studied indepth. Previous research has been carried out on the dispersaI of T. occidenta/is(Hoy et al., 1984, 1985) and N. fallacis (Johnson and Croft, 1979). Typhlodromusoccidenta/is disperses easily and has been observed to cover distances of 800 m byaerial movement. Neoseiulus fallacis travels less, dispersing aerially by up to 70 m.

----

- ----------

COLONIZA nON OF VINEY ARDS BY PHYTOSEIID MITES 539

Kampimodromus aberrans seems to have dispersai characteristics similar to thislatter species.

Types of dispersalAccording to the correlation found between the DI of the prevailing winds and thenumbers of mites trapped, wind seems to be the vector of the aerial dispersai ofphytoseiidmites and in particularof K. aberrans.Windplaysan importantrole, butother means of displacement, such as phoresy, cannot be exc1uded.These dispersaImovements have been rarely observed. They concern only some phytoseiid mitespecies, notably K. aberrans (Krantz, 1973; Sabelis and Dicke, 1985) transportedby the hazel tree aphid Myzocallis coryli. The experimental technique of our studydid not enable us to conc1ude whether the mites colonized directly by air or byphoresy. It is possible that each species needs different wind intensities to disperse,depending on their morphological, physiological and behavioural characteristics.Winds of 3.6 km h-I are sufficient to carry P.persimilis (Sabelis and Afman, 1994).Johnson and Croft (1976) showed that the maximum dispersai rates of N. fallaciswere observed for winds varying from lOto 22 km h-1. ln our study, the velocitiesof the north-north west winds, varying from 14 to 31 km h-1, made it possiblefor the species trapped to disperse, in particular K. aberrans. A comparison withP. persimilis is hazardous, since this is a more competitive specifie predator(McMurtry and Croft, 1997) and certainly more able to disperse. Kampimodromusaberrans appears to disperse with relatively low wind velocities, even a baretrembling of leaves suffices to make it airborne.

Wind is only the vector of the dispersaI. One may ask whether the dispersaI israndom, submitted to no regulation by internai and/or external factors or whetherpredatory mites develop behaviour which favours dispersaI, by making theirmovements more active. Indeed, it appears that some phytoseiid mites showparticular behaviour that induces their dispersaI such as a standing posture (Johnsonand Croft, 1976) or a walking behaviour near the edge of leaves (Hoy et al., 1984,1985; Sabelis and Dicke, 1985; Mueller and Hoy, 1987; Berry and Holtzer, 1990).ln other experiments, it wouId be interesting to study this behaviour for K.aberrans. Furthermore, this active behaviour might be triggered by biotic or abioticsignaIs such as the perception of air currents (Johnson and Croft, 1976), tem-perature (Berry and Holtzer, 1990), leaf senescence, prey availability, predatordensity and starvation. ln the same way, further research deaIing with kairomone orintraspecific chemical messengers involvement should be considered.

CONCLUSION

Typhlodromus intercalaris, Typhloseiulus simplex and Typhlodromus (Anthoseius)commenticius can be added to the list of phytoseiid mites species already known inFrance and reported by Kreiter (1991). We were also able to observe the

n-u- nu un -nu - n - - n - -- - - -

540 M.-S. TIXIER ET AL

displacement methods of some phytoseiid mites species. The colonization of grapefields was ensured mainly by the aerial dispersal of K. aberrans from areas ofdense, deep and tall vegetation particularly rich in species. The revelation thatdisplacement occurred regardless of sex or development stage constitutes anothernew element in phytoseiid mite dispersaI.

The dispersal rate of K. aberrans was shown to depend on the characteristics ofthe source area structure and plant composition as well as on the impact of theprevailing winds in the region. The colonization of vineyards by the dispersingpopulation is associated with previous chemical treatments. Grape field 1, forexample, was sprayed three times with fungicides (sulphur, mancozebe and zinebe)which are toxic for the species observed and in particular for K. aberrans (Kreiteret al., 1997). These results, which are similar to those in grape field 2, highlightedthe importance of rationalizing chemical control with the aim of optimizingcolonization in vineyards.

This study is only a first step. Data gathered in 1996 must be confirmed, whilesupplementaryfactors,particularlythe dispersaIcharacteristicsof K.aberrans,arestill to be determined. To this end, it might be of interest to use genetic markers ofK. aberrans populations, as carried out by Dunley and Croft (1992, 1994), alongwith dispersal behaviour studies in the laboratory. Studies concerning the side-effects of chemical controls on phytoseiid mites should be pursued and extended toother specific chemicals (Kreiter et al., 1997). As a follow-up to the study of theimpact of source areas on phytoseiid mites colonization, an appraisal appearsnecessary of the possible role of these areas in harbouring pests and diseasesharmful to grapevines under limited chemical controi.

The ultimate aim of using orchestrated colonization as an integrated element inpest management appears far in the future. However, the results obtained from ayear' s observation are encouraging enough to warrant sustainable management ofthis phenomenon as a new element in control techniques and entail the introductionof a new parameter: land management of vineyard borders.

ACKNOWLEDGEMENTS

We are very grateful to E. Bonnafé, J. Rouquette and R. Puerto, the three farmersinvolved in the project in Languedoc. We also thank P. Barreron, B. Cheval,H. Vanaerde and J. Valéra for technical assistance and E. Roland for translation ofthis paper. This study was financed in part by the French Research Ministry (grantnumber 95.G.OI29).

REFERENCES

Baillod, M. 1984. Lutte biologique contre les acariens phytophages. Revue Suisse Viticult.Arboricult. Horticult. 16: 137-142.

pU-- n

COLONIZA nON OF VINEY ARDS BY PHYTOSEIID MITES 541

Barret, D. 1994. Influence de l'architecture du phylloplan dans l'organisation des peuplements dePhytoséiides (Acari) et dans leurs associations avec les plantes. PhD Thesis. Ecole SupériereAgronomique de Montpellier.

Barret, D. and Kreiter, S. 1992. Rôle des relations morphométriques dans la coopération entrecertaines plantes et des acariens prédateurs Phytoseiidae (Acari). Bull. Soc. Ecophysiol.XVII(2): 129-143.

Berry, J.S. and Holtzer, T.O. 1990. Ambulatory dispersaI behavior of Neoseiulus fallacis(Acarina: Phytoseiidae) in relation to prey density and temperature. Exp. Appl. Acarol. 8:253-274.

Boller, E.F. 1984. Eine ainfache Ausschwemm-methode zur schnellen Erfassung von Raumilben,Thrips und anderen Kleinarthropoden im Weinbau. Schweiz. Zeitschr. Obstund Weinbau120: 16-17.

Boller, E.F., Remund, U. and Candolfi, M.P. 1988. Hedges as potentiaI sources of Typhlodromuspyri, the most important predatory mite in vineyards of northern Switzerland. Entomophaga33(2): 249-255.

Camporese, P. and Duso, C. 1996. Different colonization patterns of phytophagous and predatorymites (Acari: Tetranychidae, Phytoseiidae) on three grape varieties: a case study. Exp. Appl.Acarol. 20: 1-22.

Chant, D.A. and McMurtry, J.A. 1994. A review of the subfamilies Phytoseiinae andTyphlodriminae (Acari: Phytoseiidae). Int. 1. Acarol. 20(4): 223-316.

Corino, L. 1989. Les acariens phytophages sur vigne en Italie: évolution des populations etéquilibres naturels avec les acariens prédateurs. Colloque sur les acariens des cultures,Montpellier, 24-26 Octobre 1989. Ann. ANPP 2(1): 116-123.

de Moraes, G.I., McMurtry, J.A. and Denmark, H.A. 1986. A Catalog of the Mite FamilyPhytoseiidae: References to Taxonomy, Synonymy, Distribution and Habitat. Embrapa,Brasilia.

Delmas, R. and Rambier, A. 1954. L'invasion des 'araignées rouges' sur la vigne. ProgrèsAgricole et Viticole. 34-35: 101-104.

Dunley, J.E. and Croft, B.A. 1990. DispersaI between and colonization of apple by Metaseiulusoccidentalis and Typhlodromus pyri (Acarina: Phytoseiidae). Exp. Appl. Acarol. 10:137-149.

Dunley, J.E. and Croft, B.A. 1992. DispersaI and gene flow of pesticide resistance traits inphytoseiid and tetranychid mites. Exp. Appl. Acarol. 14: 313-325.

Dunley, J.E. and Croft, B.A. 1994. Gene flow measured by allozymic anaIysis in pesticideresistant Typlodromus pyri occurring within and near apple orchards. Exp. Appl. Acarol. 18:201-21 i.

Duso, c., Torresan, L. and Vettorazzo, E. 1993. La vegetazione spontanea corne riserva diausiliari: considerazioni sulla diffusione degli Acari Fitoseidi (Acari: Phytoseiidae) in unvigneto e sulle piante spontanee contigue. Boll. Zool. Agric. Bachic. 25: 183-203.

Fauvel, G. and Cotton, D. 1981. Evolution des populations de typhlodromes, Amblyseiusaberrans essentiellement, dans une haie d'ormes et un verger de pommiers et observationsde leur transport par le vent. ln Proc. 6e journeé phytiatrie. Phytopharmacie. Circum-mediterranéennes. J. Lhoste (ed.), pp. 471-479. Technic Offset pub. St Georgesd'Orques.

Hamilton, W.D. and May, R.M. 1977. DispersaI in stable habitats. Nature 269: 578-581.Hoy, M.A., Van De Baan, H.E., Groot, R.J.I. and Field, R.P. 1984. Aerial movements of mites

in almonds: implications for pest management. California Agricult. 9: 21-24.Hoy, M.A., Groot, R.I.I. and Van De Baan, H.E. 1985. Influence of aeriaI dispersaI on persistence

and spread of pesticide and spread of pesticide resistant Metaseiulus occidentalis inCaIifomia almond orchards. Exp. Appl. Acarol. 37: 17-31.

Johnson, D.T. and Croft, B.A. 1976. Laboratory study of the dispersaI behavior of AmblyseiusfaIlacis (Acarina; Phytoseiidae). Ann. Entomol. Soc. Am. 69(6): 1019-1023.

--- --------

-1

542 M.-S. TIXIER ET AL.

10hnson, D:T. and Cr()ft; B.A. 1979. Factors affecting the dispersaI of Amblyseius fallacis in anapple tree ecosystem. ln Recent advances in Acarology, Vol. 1, J.G. Rodriguez (ed.),pp. 477-483. Academic Press, New York.

Johnson, D.T. and Croft, B.A. 1981. Dispersal of Amblyseius fallacis (Acarina: Phytoseiidae) inan apple ecosystem. Environ. Entomoi. 10(3): 313-319.

Krantz, G.W. 1973. Dissemination of Kampimodromus aberrans by the Filbert Aphid. J. Econ.Entomoi. 66(2): 575-576.

Kreiter, S. 1991. Les caractéristiques biologiques des acariens prédateurs d'acariens et leurutilisation en lutte biologique. Prog. Agricult. Viticult. 108(11): 247-261.

Kreiter, S. and Sentenac, G. 1995. Gestion des populations d'auxiliaires: recolonisation naturelleou introduction des Phytoséiides en vignoble. ANPP journée d'information sur lesauxiliaires entomophages. F. Ledent and l-N. Reboulet (eds). Valence 15-XI-1995: 49-63.ANPP. pub. Paris.

Kreiter, S., Sentenac, G., Weber, M. and Valentin, G. 1993. Les Phytoseiidae des vignoblesfrançais. Synthèse de 8 années de recensement. ln Proceedings of the Third InternationalConference on Pests in Agriculture, F. Ledent and J.-N. Reboulet (eds) pp. 597-609. ANPP.pub. PARIS.

Kreiter, S., Sentenac, G., Weber, M., Rinville, C., Barthes, D. and Auger, P. 1997. Effetsnon intentionnels de quelques produits phytomarceutiques sur Typhlodromus pyri,Kampimodromus aberrans et Phytoseius plumifer. Phytoma. La Défense des Végétaux 493:51-58.

McMurtry, lA. 1992. Dynamics and potential impact of 'generalist' phytoseiids in agroeco-systems and possibilities for establishment of exotic species. Exp. Appi. Acarol. 14:371-382.

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

Mueller, B.D. and Hoy, M.A. 1987. Activity levels of genetically manipulated and wild strains ofMetaseiulus occidentalis (Nesbitt) (Acarina: Phytoseiidae) compared as a method to assayquality. Hilgardia 55: 1-23.

Price, P. 1984. Insect Ecology, 2nd edn. Wiley, New York.Sabelis, M.W. and Afman, B.P. 1994. Synomone-induced suppression of take-off in the

Phytoseiid mite Phytoseiulus persimilis Athias Henriot. Exp. Appl. Acarol. 18: 711-721.Sabelis, M.W. and Dicke, M. 1985. Long range dispersaI and searching behavior. ln Spider mites:

their biology, natural enemies and control, Vol. IB, W. Helle and M.W. Sabelis (eds),pp. 141-160. Elsevier, Amsterdam.

Sentenac, G., Kreiter, S., Weber, M., Barthes, D. and Jacquet, C. 1993. Protection intégrée contreles acariens de la vigne. ln Proc. Int. Congo Euroviti 7th. I.T.V. Latles (ed.), pp. 135-174.Transcomp Montpellier Pub.

Sokal, R.R. and Rohlf, F.J. 1980. Biometry. The Principles and Practice of Statistics in BiologicalResearch, 2nd. edn. W.H. Freeman and Company Editions, New York.

Tuovinen, T. 1993a. Identification and occurrence of phytoseiid mites (Gamasida: Phytoseiidae)in Finnish apple plantations and their surroundings. Entolomoi. Fenn. 31(4): 95-113.

Tuovinen, T. 1993b. Phytoseiid mites (Acari: Gamasina) in Finnish apple plantations withreference to integrated control of phytophagous. Agricult. Sei. FinI. 2(1): 7-31.

Tuovinen, T. 1993c. Influence of surrounding trees and bushes on the Phytoseiid mites fauna onapple orchard trees in Finland agriculture. Agricult. Sci .Finl. 2(1): 47-56.

Tuovinen, T. and Rokx, J.A.H. 1991. Phytoseiid mites (Acari: Phytoseiidae) on apple trees andin surrounding vegetation in southern Finland. Densities and speeies composition. Exp.Appl. Acarol. 12: 35-46.

Van de Vrie, M. and Price, J.F 1995. Dispersai behaviour of the predacious mite Phytoseiuluspersimilis in strawberry fields in Florida. ln The Acari: physiological and ecological aspectsof acari-host relationships, D. Kropczynska, 1. Boczek and A. Tomczyk (eds), pp. 323-329.oficyna DABOR. Warszawa.

'-