Exp Appl Acarol (2006) 39:227–242 DOI 10.1007/s10493-006-9010-9

Immigration of phytoseiid from surrounding uncultivated areas into a newly planted vineyard

Marie-Ste´phane Tixier Æ Serge Kreiter Æ Brigitte Cheval Æ Sabine Guichou Æ Philippe Auger Æ Romain Bonafos

Received: 28 September 2004 / Accepted: 8 May 2006 / Published online: 28 June 2006 Springer Science+Business Media B.V. 2006

Abstract This study reports (1) a faunistic survey of phytoseiid mites observed inside a vine plot and in neighbouring vegetation (other vine plots and uncultivated areas) and (2) dispersal of phytoseiid mites into the plot studied. These data aim to raise some hypotheses concerning natural colonisation of a vineyard by predatory mites. The study was carried out over 3 years (1999, 2000 and 2001) in an experi- mental plot planted with two cultivars (Grenache and Syrah) and with Sorbus domestica in a framework of agroforestry investigations. Phytoseiid mites were collected in both cultivated and uncultivated areas surrounding the experimental plot, and their dispersal into the plot studied using ‘‘aerial’’ traps. Densities re- mained quite low compared to previous studies. The main species encountered in the uncultivated areas and in the traps was phialatus. Despite the low numbers of phytoseiid mites trapped, densities of phytoseiid mites into the vine field increased during 3 years. Typhlodromus phialatus, the species mainly found in the neighbouring uncultivated areas, was rarely found in vineyards. Another morpho- logically close species was predominant on vines: Typhlodromus exhilaratus. However, aberrans the main phytoseiid species in vineyards of Southern France was not found in the present survey. Hypotheses for this colonisation process are discussed.

Keywords Æ Uncultivated areas Æ Vineyards Æ Typhlodromus exhilaratus Æ Typhlodromus phialatus Æ Kampimodromus aberrans

M.-S. Tixier (&) Æ S. Kreiter Æ B. Cheval Æ S. Guichou Æ P. Auger Æ R. Bonafos Ecole Nationale Supe´rieure Agronomique/Institut National de la Recherche Agronomique, Unite´ Ecologie Animale et Zoologie Agricole, Laboratoire d’Acarologie, 2 place Pierre Viala, 34060 Montpellier cedex 01, France e-mail: [email protected] 123 228 Exp Appl Acarol (2006) 39:227–242

Introduction

Predatory mites belonging to the Phytoseiidae family are well known efficient predators of pest mites in several crops. They have often been reported in unculti- vated areas surrounding vineyards (Boller et al. 1988; Duso 1992; Coiutti 1993; Duso et al. 1993; Ragusa et al. 1995; Duso and Fontana 1996; Tixier et al. 1998, 2000a, b), assuming that such areas are reservoirs for these natural enemies. Their plant composition can affect the diversity and the abundance of phytoseiids, due to close relationships between plant characteristics (i.e., leaf pilosity) and mite development (Tixier et al. 1998, 2000b; Kreiter et al. 2002), especially for Kampimodromus aberrans (Oudemans), the main phytoseiid mite in vineyards of Southern Europe, including France (Camporese and Duso 1996; Perez Otero et al. 1997; Duso and Vettorazzo 1999; Kreiter et al. 2000). However, mite exchange between uncultivated and cultivated areas is poorly documented. Some studies using trappings showed that phytoseiid mites are wind dispersed into orchards and vineyards (Hoy et al. 1984, 1985; Tixier et al. 1998, 2000a). The link between phytoseiid mite occurrence in uncultivated and cultivated areas was also shown using faunistic surveys and population dynamics studies (Tixier et al. 1998, 2000a). At last, in some investiga- tions, gene exchange between mite populations living in these areas was assessed (Dunley and Croft 1994; Tixier et al. 2002). The present study aims at the coloni- sation of a newly planted vineyard carrying out faunistic surveys, population dynamics studies and trapping experiments over three consecutive years. Further- more, the plot studied is inter-planted with trees, Sorbus domestica L., in a framework of agroforestry investigations. Few studies deal with the influence of inter-cropping on mite communities and most of them concern herbaceous plants (Corbett et al. 1991; Toko et al. 1996; Castagnoli et al. 1997; Lozzia and Rigamonti 1998). The second objective of this study is to assess abundance and diversity of phytoseiid mites on these trees over 3 years and their potential utility for biological control of mite pests in vineyards.

Material and methods

The experimental vineplot

The experimental plot was a vineyard located at Restinclie`res, 15 km North of Montpellier, Southern France. This plot (4,494 m2, plantation densities: 2.5 · 1m) was planted in 1997 (after reclaiming land for cultivation) with two cultivars, Syrah and Grenache, and six rows of S. domestica (Fig. 1). The two cultivars are equally representated (50% Grenache and 50% Syrah). Pesticides were applied mainly against powdery and downy mildew and Scaphoideus titanus Ball (vector of the phytoplasma inducing a grapevine disease called ‘‘Flavescence dore´e’’). However, pesticides were scarcely applied (2–4 fungicides and 2–3 insecticides per year) with concentrations recommended by the phytosanitary reglementary handbook (Acta 2003). The pesticides were selected according to their side effects on phytoseiid mites (Typhlodromus pyri Scheuten and Kampimodromus aberrans [Oudemans]), pyrethrinoids were avoided (Sentenac et al. 2002) and no acaricide was used during the 3-year study (Table 1). The experimental plot was surrounded by 123 Exp Appl Acarol (2006) 39:227–242 229

V1north North V2 V1south North uncultivated area (300m 2)

p 3 p 2 p 1

1 2 3 V3

p 4 p 5 p 6

West uncultivated p 9 p 8 p 7 area 2 (600m ) 4 5 6 V4

p 10 p 11 p 12

V5 7 8 9 p 15 p 14 p 13

South uncultivated area 10 m (40m2)

10 11 12

Aerial traps Samplings plots Sorbus domestica rows

Fig. 1 Experimental plot at Restinclie`res, South of France, V1-5 are the neighbouring vine plots and P1-15 correspond to sampled sub-units of the experimental plot

uncultivated areas, bearing essentially Pinus sp. and Quercus sp., and by other cultivated vine fields, also planted in 1997 on reclaimed land. Phytoseiid mite occurrence was studied in the experimental plot and in the various neighbouring areas during 3 years. However, prey densities were not accurately studied. Indeed, as almost all phytoseiid mites are generalist predators (McMurtry and Croft 1997), prey occurrence and distribution does not seem to greatly affect phytoseiid distribution (McMurtry 1992; McMurtry and Croft 1997). Furthermore, observa- tions during the seasons have shown that no tetranychid mite occurred in the experimental plot. 123 230 Exp Appl Acarol (2006) 39:227–242

Table 1 Active ingredients used and pests and diseases treated in 1999, 2000 and 2001 on the experimental plot in Restinclie`res (He´rault, France)

Pests and diseases 1999 2000 2001 treated

Powdery mildew Sulfur (25/VII) Pyrifenox (02/VI, 30/VI) Difenoconazole (16/V) Quinoxyfen (16/VI) Sulfur (27/VI, 15/VII) Sulfur (25/VII, 08/VIII) Downy mildew Copper (06/VII) Fosetyl aluminium (04/V) Fosetyl aluminium Folpel (06/V) Metalaxyl Folpel Metalaxyl Folpel Dimethoate, (06/VIII) (16/V, 02/VI) Mancozebe (20/VI) Zinebe and Copper Folpel (16/VI) Copper (30/VII) (03/VIII) Copper (30/VI, 25/VI) Azoxystrobine (17/VI) Zinebe and Copper (08/VIII, 23/VIII) Scaphoideus titanus Chlorpyrifos ethyl Chlorpyriphos ethyl (16/VI, 30/VI, 25/VII) (15/VI, 30/VI, 24/VII)

Phytoseiid mites in the surrounding environment

The uncultivated environment

Sampling was carried out during 3 years (from 1999 to 2001) in the uncultivated surrounding areas, two or three times per year (1999: 25/V, 06/VII, 17/VIII; 2000: 02/ V, 05/VI; 2001: 15/V, 10/VII, 21/VIII). All plant species were sampled, taking at least 50 leaves per plant species for each sample date. The leaves (50–500 depending on plants) were sampled on different plants belonging to the same species. Each plant species had different Phytoseiidae densities and plant species were not equally represented in each uncultivated area. Thus, in order to compare the total densities of phytoseiid mites in the several uncultivated areas, an index called ‘‘Woody Richness’’ (WR) was used: WR = S (abundance-dominance of a plant species · the density of phytoseiid mites on this species/leaf), where: 1 = plants are rare, 5% of the canopy; 2 = abundant, 5–25%; 3 = moderately abundant, 25–50%; 4 = very abundant, 50–75%; and 5 = dominant, >75% (Tixier et al. 1998). Also, the occurrence of phytoseiid mites in more remote uncultivated areas was studied. Sampling was carried out in 2000 and 2001 in three directions (North-East, North-West, South), each 100 m, 1 km long (10 samplings). At each collecting site, all plant species were sampled taking at least 50 leaves per species.

The neighbouring vine plots

Sampling was carried out in the six neighbouring vine plots, equally planted with Syrah and Grenache cultivars. Each plot was sampled three times in 2000 and 2001 (2000: 09/V, 20/VI, 01/VIII; 2001: 22/V, 17/VII, 21/VIII). In 1999, the vine plants were young and no leaf was sampled to avoid damage on the plantations. Each neighbouring vine field was divided in several small plots of 400–600 vinestocks each, and at least 30 leaves were collected in each plot for each sampling date (Fig. 1). Each small plot was planted with a single cultivar. 123 Exp Appl Acarol (2006) 39:227–242 231

Phytoseiid mite populations in the experimental vine plot

The experimental plot was divided into 15 small plots of 100 vinestocks each to characterise differences in phytoseiid mite densities according to distance from the uncultivated areas. At least 20 leaves were randomly collected in these plots for each sample date (1999: 18/V, 22/VI, 22/VII, 31/VIII; 2000: 16/V, 27/VI, 25/VII, 22/VIII; 2001: 24/IV, 29/V, 26/VI, 24/VII, 04/IX). At the same dates, samplings were also carried out on the six rows of S. domestica, taking randomly at least 30 leaves per row. The leaves collected in cultivated and uncultivated areas were brought back to the laboratory. Phytoseiid mites were removed from leaves using Berlese-Tullgren funnels or the washing method (Boller 1984). Then, phytoseiid mites were counted with a binocular microscope at 20· magnification, and mounted in Hoyer’s medium on slides. Twelve traps were disposed in the experimental plot to characterise phytoseiid mite arrival in the plot during 3 years. They were constituted of plastic funnels (31 cm in diameter) filled with water and placed 1 m above the vegetation on glued sticks (Tixier et al. 1998, 2000a) (Fig. 1). The contents of the funnels were weekly filtered through 100 lm sieves and the mites were counted, mounted on slides and identified.

Phytoseiid identifications

Phytoseiid mites have been identified with taxonomic keys following the generic concepts of Chant and McMurtry (1994) for the and Phytoseiinae, of Chant and McMurtry (2003a, b) for Amblyseiinae Neoseiulini and Kampimo- dromini, and of Moraes et al. (2004) for other Amblyseiinae.

Statistical analysis

Statistical analyses were carried out to compare (1) the WR indexes of the different uncultivated areas, (2) the densities of phytoseiid mites in the 15 parts of the experimental plot, (3) the densities of phytoseiid mites in the neighbouring vine plots, (4) the phytoseiid mite densities on the two vine cultivars, and (5) the mite densities captured in the 12 traps. For all these comparisons, dates were used as replicates. Although not true replicates, dates allow comparisons because phytoseiid density variation in time is the same in all the parts compared. As these data do not follow a normal distribution, non-parametric tests were used (Kruskal & Wallis ANOVA) (Statistica 2001). Mite numbers trapped were converted to mite numbers migrating per leaf (Tixier et al. 2000a). This conversion was based on the estimation of the vegetation area that could be reached by phytoseiid mites and on the transformation of this surface into a leaf number on which migrants are able to develop. The estimate of the landing surface of phytoseiid mites was based on Carbonneau (1995), who defined the foliar surface exposed to solar radiation, assumed to be similar to that exposed to the wind. The values used to establish this estimation were: vegetation height, 1 m; vegetation width, 0.5 m; funnel area, 0.0707 m2; average number of leaves/ vinestock, 200. 123 232 Exp Appl Acarol (2006) 39:227–242

Results

Phytoseiid mites in the uncultivated surrounding environment

During 3 years, the phytoseiid mite abundances (WR indexes) in the three uncul- tivated areas bordering the experimental vine field were not significantly different (F(2,21) = 0.55, P = 0.58) (Fig. 2). From 1999 to 2000, phytoseiid mite density in- creased in all areas, but in 2001, the density was very low everywhere. The density of phytoseiid mites was high early in the season (May) and then decreased during summer, except in 2001. The declining trend is typical for phytoseiid mites (Ivancich- Gambarro 1987; Malison 1994), due to their susceptibility to dry conditions during summer. Among the 24 plants sampled, only Lonicera sp., Viburnum tinus L., Rubus sp. and Cornus sp. had substantial phytoseiid mite densities (Table 2). Thirty-one phytoseiid mite species were found in the uncultivated areas sampled (Table 3). The number of species observed decreased from 1999 to 2001 and Typhlodromus phialatus Athias-Henriot was the most abundant species. Typhloseiella isotricha (Athias-Henriot) only found on Inula viscosa L., was quite frequently collected. Typhlodromus phialatus was also the main species sampled in more remote areas. High densities of K. aberrans were observed on some plants at least 800 m away from the plot (Celtis australis L., Juniperus sp. and Quercus pubescens Willdenow). The greater densities were observed on C. australis with a mean density per leaf of 0.98, K. aberrans corresponding to 75% of the species found on this plant.

Phytoseiid mites in the cultivated environment

Phytoseiid mites were found in the six neighbouring vine plots and densities were not significantly different in the vine plots over the 3 years (F(5,24) = 1.10; P = 0.34),

WR 1.0

0.8

0.6

0.4

0.2

0.0

–0.2 North area West area South area Fig. 2 Abundance of phytoseiid mites (woody richness index) obtained for the three uncultivated areas surrounding the experimental plot in 1999, 2000 and 2001 (mean ± SE) 123 Exp Appl Acarol (2006) 39:227–242 233

Table 2 Densities of phytoseiid mites (numbers per leaf) on each host plant for the different sampling dates from 1999 to 2001 in the uncultivated surrounding areas at Restinclie`res (He´rault, France)

1999 2000 2001 25/V 06/VII 17/VIII 02/V 05/VI 15/V 10/VII 21/VIII

South area Clematis flamula 0 0 0 0 0.02 0 0 0 Cornus sp. 0.065 0 0 0.005 0.043 0.005 0.030 0.02 Daphne gnidium 0 0 0 0 0.005 0 0 0 Dorychnium suffroticosum 00 0 00 00 0 Euphorbia peplus 00 0 00 00 0 Genista scorpius 0 0 0 0 0 0 0.005 0 Juniperus oxycedrus 0 0 0 0 0.003 0 0.003 0 Ligustrum vulgarae 0 0 0 0.003 0 0 0.020 0 Lonicera sp. 0.023 0 0 0.02 0 0 0 0.01 Phyllirea media 0.002 0 0 0 0.003 0 0.003 0 Pinus halepensis 0 0 0.006 0 0 0 0 0 Prunus dulcis 00 0 00 00 0 Quercus coccifera 0 0 0 0.067 0 0 0.005 0 Rubia peregrina 0 0 0 0 0 0 0.005 0 Rosmarinus officinalis 0 0 0 0.007 0 0 0.003 0.001 Rubus sp. 0.057 0 0 0.01 0.02 0 0 0 Ulmus sp. 0.01 0 0 0 0.155 0 0 0 Viburnum tinus 0.008 0.045 0.04 0.280 0.060 0 0.060 0.05 North area Daphne gnidium 0 0 0 0 0 0.01 0 0 Dorychnium suffroticosum 0 0 0 0 0 0 0 0.002 Euphorbia peplus 0.012 0 0 0 0.033 0 0 0 Genista scorpius 0.000 0 0 0 0 0 0 0 Inula viscosa 0.011 0.039 0.11 0.02 0.05 0.000 0.03 0.000 Juniperus sp. 0 0 0 0 0.005 0 0 0 Lonicera sp. 0 0 0 0 0 0.01 0.000 0.000 Phyllirea media 0 0 0 0 0.003 0 0 0.003 Pinus halepensis 0 0 0.005 0 0 0 0 0 Pistacia lentiscus 0.013 0.000 0 0 0 0 0 Quercus coccifera 0 0.01 0 0 0 0 0 0 Quercus ilex 0 0.04 0 0.080 0 0.010 0 0.01 Rosmarinus officinalis 0 0 0.002 0.003 0.013 0 0 0 Rubus sp. 0.08 0 0 0.02 0.110 0 0 0 Viburnum tinus 0.36 0.04 0 0.400 0.040 0 0.040 0.04 West area Dorychnium suffroticosum 0 0 0 0 0.002 0 0 0 Juniperus sp. 0.004 0 0 0 0 0.003 0 0 Lonicera sp. 0.012 0 0 0.03 0.01 0 0 0.01 Phyllirea media 0 0 0.01 0 0 0 0 0 Phyllirea angustifolia 0 0 0.012 0 0.003 0 0 0.003 Pinus halepensis 0.009 0 0.003 0 0 0 0 0 Pistacia lentiscus 00 0 00 00 0 Quercus coccifera 0.043 0.006 0.02 0.005 0.005 0 0 0 Quercus ilex 0.008 0 0 0 0.005 0 0 0 Rosmarinus officinalis 0 0.05 0.002 0.003 0.005 0 0 0 Rubus sp. 0 0.027 0 0.075 0.138 0 0 0 Viburnum tinus 0.22 0 0 0.080 0.080 0.020 0 0.03 nor between cultivars (Grenache and Syrah) (F(1,42) = 3.02; P = 0.89). From 2000 to 2001, the populations increased in all plots (except V5), on average from 0.065 to 0.18 phytoseiid/leaf (Fig. 3) (F(1,9) = 0.03; P = 0.035). 123 234 Exp Appl Acarol (2006) 39:227–242

Table 3 Percentage of phytoseiid mite species sampled in the uncultivated areas surrounding the experimental plot, at Restinclie`res (South of France) in 1999, 2000 and 2001

1999 2000 2001

Amblyseiinae andersoni 2.5 – – finlandicus – 0.3 – Euseius stipulatus – 0.3 – Kampimodromus aberrans 4.2 1.7 13.1 aurescens 0.4 – – Neoseiulus bicaudus 0.5 – – Neoseiulus californicus 0.6 0.7 – 0.7 – – Neoseiulus graminis – – 0.8 persimilis 0.4 – – messor 0.4 – – Typhloseiella isotricha 10.1 12.9 8.5 Phytoseiinae echinus 0.4 – – Phytoseius juvenis 0.5 – – Phytoseius finitimus 0.6 – – Typhlodrominae tiliarum 0.7 – – soleiger – 0.3 – Paraseiulus triporus – 0.3 – Typhlodromus (Anthoseius) cryptus 1.3 0.7 – Typhlodromus (Anthoseius) ilicis 0.4 – – Typhlodromus (Anthoseius) recki 16.0 18.6 2.3 Typhlodromus (Anthoseius) rhenanoides 3.0 – – Typhlodromus (Anthoseius) rhenanus 0.8 – 3.1 Typhlodromus athiasae 0.4 – – Typhlodromus baccettii 0.8 0.7 – Typhlodromus ernesti 0.8 – – Typhlodromus exhilaratus – 2.4 5.4 Typhlodromus phialatus 55.3 60.7 66.2 Typhlodromus pyri ––– carmonae – 0.3 – Typhloseiulus eleonorae – – 0.8 Species numbers 22 13 8

Four species were found but their proportions greatly changed over the years. In 2000, Neoseiulus californicus (McGregor) was the prevailing phytoseiid. In 2001, Typhlodromus exhilaratus Ragusa was the only species collected in all the plots (Fig. 3).

Phytoseiid mites dispersal into the experimental vine plot

Phytoseiid mites were found in all traps. The densities were significantly different between the 3 years (F(2,33) = 6.11; P = 0.005) (Fig. 4), highest numbers being trapped in 1999 (3.01 phytoseiids/trap) compared to 1.08 phytoseiids/trap in 2000 and 1.25 phytoseiids/trap in 2001. These densities correspond to an average arrival rate of 0.23 phytoseiid per leaf per year (range: 0.18–0.33). The mite numbers captured were not significantly different between the 12 traps (F(11,24) = 0.66; P = 0.75). Unlike 1999 and 2000, in which the highest densities of mites were trapped in July, the peak abundance of phytoseiid mites in 2001 occurred in May. Seventeen species of phytoseiid mites were trapped during 3 years (Table 4). However, two species (T. phialatus and K. aberrans) were the most abundant. 123 Exp Appl Acarol (2006) 39:227–242 235

Number of phytoseiid Neoseiulus californicus mites / leaf Typhlodromus recki 0.4 Kampimodromus aberrans Typhlodromus exhilaratus 0.35

0.3 2000 2001 0.25

0.2

0.15

0.1

0.05

0 h 2 h h out V V3 V4 V5 out V2 V3 V4 V5 S Nort S 1 1 1 V1 NorthV V V Fig. 3 Phytoseiid mite densities and diversity in the neighbouring vine fields in 2000 and 2001, at Restinclie`res, South of France

1999 Numbers of mites trapped

8 2000

2001 6

4

2

0 1 2 3 4 5 6 7 8 9 10 11 12 Trap numbers Fig. 4 Numbers of phytoseiid species trapped in the 12 aerial traps located inside and outside the experimental vine plot in 1999, 2000 and 2001, at Restinclie`res, South of France

Phytoseiid mites in the experimental vine plot

The mite densities did not significantly differ in the 15 small plots (F(14,174) = 0.64; P = 0.82) (Fig. 5). Significant differences occurred between the numbers on Syrah (0.14 phytoseiid/leaf) and on Grenache (0.05 phytoseiid/leaf). (F(1,187) = 9.68; P = 0.02). Even if vine leaf pilosity effect on phytoseiid mite abundance is well known (Duso 1992; Karban et al. 1995; Camporese and Duso 1996; Castagnoli et al. 123 236 Exp Appl Acarol (2006) 39:227–242

Table 4 Number and proportions of phytoseiid mites captured in aerial traps in 1999, 2000 and 2001 in Restinclie`res, South of France

1999 2000 2001 Total %

Amblyseiinae Amblyseiella rusticana 1–– 1 1.7 Euseius stipulatus –11 2 3.4 Kampimodromus aberrans 0 7 1 8 13.8 Neoseiulus aurescens 2–1 3 5.2 Neoseiulus cucumeris ––1 1 1.7 Proprioseiopsis sp. – 1 – 1 1.7 Typhloseiella isotricha 1–– 1 1.7 Typhlodrominae Typhlodromus athiasae –1– 1 1.7 Typhlodromus barkeri 2–– 2 3.4 Typhlodromus corticis ––1 1 1.7 Typhlodromus cryptus 6 – – 6 10.3 Typhlodromus exhilaratus 012 3 5.2 Typhlodromus intercalaris 2–– 2 3.4 Typhlodromus phialatus 2481422.6 Typhlodromus recki 12– 3 5.2 Typhlodromus rhenanus ––3 3 5.2 Typhloseiulus carmonae –2– 2 3.4 Immatures 6 1 1 8 13.8

Numbers of phytoseiid mites per leaf

0.35

0.3 2000 0.25 2001 0.2

0.15

0.1

0.05 0 2 3 4 5 5 6 1 1 1 1 P1 P2 P3 P4 P P P7 P8 P9 P10 P11 P P P P

Sampled plots Fig. 5 Phytoseiid mite densities sampled in the 15 small plots inside the experimental vine field in 2000 and 2001

1997; Kreiter et al. 2002), this result must be interpreteted with caution due to the low densities, the absence of specific protocol design and the ubiquity of T. exhila- ratus also observed on glabrous leaf cultivars (Castagnoli et al. 1997). Mite density was high in May and decreased during summer. In August, a great increase was observed especially in 2001. Typhlodromus exhilaratus was the main species sampled. Some K. aberrans were observed during 3 years, but their location in the plot changed each year. From 1999 to 2001, phytoseiid mite density increased from 0.042 phytoseiid per leaf on average in 1999 to 0.15 phytoseiid per leaf in 2001 (Fig. 6). 123 Exp Appl Acarol (2006) 39:227–242 237

Number of phytoseiid mites per leaf

0.3

0.25

0.2

0.15ph/l 0.15 0.045ph/l 0.10 0.042ph/l

0.05

0 1999 2000 2001 Fig. 6 Variation of phytoseiid mite densities sampled in the experimental vine field in 1999, 2000 and 2001. Numbers above the curves correspond to the mean number of mites per leaf sampled for each year

The density of mites on S. domestica was very low (mean: 0.05 phytoseiid/leaf) and not significantly different between rows (F(5,42) = 0.36; P = 0.87). Typhlodromus exhilaratus was the main species encountered. Typhlodromus phialatus, K. aberrans and T. recki were also sometimes found on these trees. Furthermore, one species of Tetranychidae, Tetranychus turkestani Ugarov & Nikolski, was observed several times on S. domestica.

Discussion

This survey raises several points of discussion, concerning (1) the presence of phy- toseiid mites on S. domestica, (2) the colonisation process, (3) the dominance of T. exhilaratus in the vineyards and of T. phialatus in the uncultivated neighbouring areas, and (4) the absence of K. aberrans in the present study, as this species is the main phytoseiid mite encountered in vineyards in Southern France.

Phytoseiid mite occurrence on S. domestica

Trees inter-planted with vine harboured low densities of phytoseiid mites and no conclusion could be drawn on their role as reservoir. However, T. exhilaratus occurred both on S. domestica and surrounding vines. This observation could mean that (1) the trees are colonised in the same way as the surrounding vine, (2) popu- lations on vine and on inter-planted trees possibly exchange mites. Tetranychid mites were observed on these trees. However, the species mainly encountered, T. turke- stani, is rarely found on vine in France (Bolland et al. 1998). It would be interesting to assess the development of T. exhilaratus on this prey to determine if the presence of this tetranychid could enhance the densities of the predator into the plot. 123 238 Exp Appl Acarol (2006) 39:227–242

Colonisation process

The results differ from those obtained earlier in another region of southern France (1998, 2000a and 2002), lower mite densities being observed in the present survey. The main trees surrounding the plot were Pinus sp. and Quercus ilex L., both harbouring low densities of phytoseiid mites. Only some plants (V. tinus L., Lonicera sp., Rubus sp.), generally scattered, had quite high densities of predatory mites. On the opposite, in the previous study the environment hosted numerous trees and shrubs suitable for phytoseiid mite development, especially Q. pubescens, C. australis, Rubus sp. and Ulmus sp. (Tixier et al. 1998, 2000a). These differences tend to confirm the effect of plant composition on the abundance of phytoseiid mite occurrence in uncultivated areas (Duso and Pasqualetto 1993; Tixier et al. 2000a, 2000b). The densities of phytoseiid mites were higher in neighbouring vine crops than in the woody margins. Vineyards could then constitute higher reservoirs for colonisa- tion. However, nothing is known about phytoseiid mite exchange between vine fields and the study of gene flow between vine plots including molecular typing would be required. This study confirms the aerial dispersal of phytoseiid mites into crops (Hoy et al. 1984, 1985; Tixier et al. 1998, 2000a). However, fewer mites were trapped than in the previous study. This result can be directly linked to the lower intensity of wind and to lower abundance of mites (WR indexes) in the surrounding environment. Some species, like T. phialatus and K. aberrans, were regularly captured. This result seems to be obvious for T. phialatus as it was the main species found in the surrounding uncultivated environment. Kampimodromus aberrans, however, was rare in the neighbouring areas and was only observed in remote places. Although this species is not known as a dispersive mite (Fauvel and Cotton 1981), the present data seem to suggest a possible long distance dispersal of this species. The presence of several phytoseiid mite species was observed the first year of plantation, indicating a rapid colonisation. The diversity of phytoseiids then decreased rapidly, T. exhilaratus becoming the only species found. This lost of diversity could be the result of selection pressure due to agricultural practices (pesticide applications, for example) leading to the disappearance of the uncom- petitive species. The density of phytoseiid mites increased in all parts of the plot from 1999 to 2001, irrespective of their distance from the uncultivated areas. Again, this differs from previous results. Possible explanations for this difference are the structuring of the plot and its environment (smaller plot, plot surrounded on the three sides by uncultivated areas), the same densities of mites arriving at whatever part of the plot (linked to the structure of the plot), the species involved (T. exhil- aratus/K. aberrans) and their dispersal ability inside the plot. Although the density of phytoseiid mites increased in the plot, it is difficult to link this increase with densities trapped. Mite arrival brings 0.23 mite per leaf per year, which is higher than the increase really observed on vine leaves. However, the species found in the vineyard (T. exhilaratus) was scarcely trapped. We can thus assume that the low densities of this species arriving in the plot were sufficient to provide the rapid and total colo- nisation of the plot. These results are quite similar to that found for the study of vineyard colonisation in Burgundy (France) by T. pyri (Sentenac and Valot 1999). With this type of colonisation, gene flow is supposed to be greater between popu- lations within a vine field than between populations within and outside the vine field. Population genetics studies are needed to test this hypothesis. 123 Exp Appl Acarol (2006) 39:227–242 239

The occurence of T. exhilaratus and T. phialatus

Why would habitat separation exist between T. exhilaratus and T. phialatus? Both species are found in vineyards in the South of Europe (Castagnoli et al. 1989; Papaioannou-Souliotis et al. 1999; Pereira et al. 2003). Both species are group III generalist predators, as defined by McMurtry and Croft (1997) (Ragusa 1981; Castagnoli and Liguori 1986; Ferragut et al. 1987; Castagnoli et al. 1989; Liguori and Guidi 1990; Ferragut et al. 1992; Ragusa and Tsolakis 1995). Both species are very common in hot dry climatic conditions. For T. exhilaratus,at25C and 55% relative humidity (RH), more than 50% of the eggs hatch (Liguori and Guidi 1995). For T. phialatus, 88.5% of hatching is observed at 60% RH at 25C (Ferragut et al. 1987). None of the life-history elements known of the two species allow to explain their specific distributions. Additional studies on ecology, behaviour and competitive ability of these two species in pesticide disturbed environments are in process in the lab.

The absence of Kampimodromus aberrans in the present site

Kampimodromus aberrans is scarcely found in the site studied, whereas this species is prevailing in the vineyards of the South of France (Kreiter et al. 1993, 2000) Tsolakis et al. (1997) have shown that K. aberrans is more abundant in cultivated plots borders than in more remote uncultivated places. It is also rarely found in old unsprayed vine plots in France (Tixier et al. 2000a). This species is assumed to be adapted to crop practices and especially to pesticide sprays. In the present study, very few pesticides were applied and K. aberrans may be outcompeted by T. exhilaratus in such an environment. However, other factors like local climatic conditions could also be involved: K. aberrans seems to be less tolerant to drought than T. exhilaratus. Schausberger (1998) observed a mortality rate of K. aberrans of 30% at 65% RH, and 50% mortality at 55% RH. Furthermore, Malison (1994) showed that the development of K. aberrans is affected on water stressed vine plants. In the present study, micro-climatic conditions are particularly dry, the soil does not allow water accumulation and the small size of vine plants limited the humidity at the canopy level. In the surrounding environment, wild plants are also adapted to dry conditions. This type of environment and plants encountered could be unfavourable for K. aberrans. Finally, K. aberrans numbers at a distance from the plot may have been too low to enable settlement within the plot.

Conclusion

This study monitors the successful colonisation of a newly planted vine plot by phytoseiid mites. These observations differ from results of previous studies, with respect to densities trapped, species involved and vegetation structure. This study emphasises the diversity of situations and the difficulty to modelise this process. To assess the factors involved in colonisation success, a large-scale study would be required. The present study is one of the first into the impact of habitat diversification on phytoseiid communities within a field. The impact of inter-planted trees in vine plots was not clearly shown and more data are needed for instance on population differentiation of T. exhilaratus, based on molecular typing. 123 240 Exp Appl Acarol (2006) 39:227–242

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