Colonization and predation of thrips (Thysanoptera: Thripidae) by Orius spp. (Heteroptera: Anthocoridae) in sweet pepper greenhouses in Northwest Italy

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Biological Control 44 (2008) 331–340 www.elsevier.com/locate/ybcon

Colonization and predation of thrips (Thysanoptera: Thripidae) by Orius spp. (Heteroptera: Anthocoridae) in sweet pepper greenhouses in Northwest Italy Lara Bosco, Emanuela Giacometto, Luciana Tavella

*

Di.Va.P.R.A. Entomologia e Zoologia applicate all’Ambiente ‘‘Carlo Vidano’’, University of Torino, via L. da Vinci 44, 10095 Grugliasco (TO), Italy Received 12 July 2007; accepted 30 October 2007 Available online 5 November 2007

Abstract Frankliniella occidentalis (Pergande) and Thrips tabaci Lindeman (Thysanoptera: Thripidae) are major pests of sweet pepper for direct damage and tospovirus transmission. To control their infestations, Orius laevigatus (Fieber) (Heteroptera: Anthocoridae) is produced by many commercial insectaries and widely used on IPM vegetable crops of Europe. This predator is naturally widespread along the Mediterranean and Atlantic coasts, and not in more continental areas, where other Orius spp. are more common. Research was conducted in a continental area of Northwest Italy in 2002–2003 to assess the natural presence of anthocorids on pepper, and to compare their colonization and predatory ability with those of the species artificially introduced. Experiments were conducted in 12 sweet pepper greenhouses, in six of which O. laevigatus release was made. From late May to early October, thrips and anthocorids were sampled on pepper by collecting flowers; Orius spp. were also collected on neighboring wild flora. Independently of the releases, Orius specimens were found in all surveyed greenhouses, but O. niger Wolff, also captured on various wild plants, was the most abundant species. It naturally colonized crops from late June and proved to be the most efficient predator on sweet pepper in the surveyed area, if not disturbed by pesticide application. Contrarily, O. laevigatus was rarely found and only in the greenhouses in which it had been released. However its introduction resulted in thrips control before natural colonization by the native species occurred.  2007 Elsevier Inc. All rights reserved. Keywords: Frankliniella occidentalis; Orius laevigatus; O. niger; Thrips biological control; Seasonal abundance; Crop and noncrop plants

1. Introduction Thrips (Thysanoptera: Thripidae) are serious pests of ornamental, vegetable, and fruit crops both in the open field and greenhouses throughout the world (Tommasini and Maini, 1995). Feeding by thrips can cause distortion, discoloration, silvering and bronzing of leaves and fruits on vegetable crops reducing their market value. In Italy the cosmopolitan western flower thrips (WFT) Frankliniella occidentalis (Pergande), since its first appearance at the end of the 1980s (Arzone et al., 1989), has become one of the most important pests of sweet pepper crops, usually replacing the Mediterranean onion thrips (OT) *

Corresponding author. Fax: +39 011 0918535. E-mail address: [email protected] (L. Tavella).

1049-9644/$ - see front matter  2007 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2007.10.027

Thrips tabaci Lindeman. In fact, in addition to the direct damage to plant tissues, this species is a very efficient vector of Tomato spotted wilt virus (TSWV). This worldwide tospovirus infects several cultivated and wild plants including sweet pepper (Whitfield et al., 2005), and was detected in Italy just after the introduction of WFT (Vaira et al., 1993), although the first assessed vector of TSWV was T. tabaci (Tedeschi et al., 2001; Whitfield et al., 2005). Populations of F. occidentalis are difficult to control despite frequent applications of insecticides (Funderburk et al., 2000), which often result in the development of pesticide resistance (Immaraju et al., 1992; Brødsgaard, 1994; Broadbent and Pree, 1997). Furthermore, primary spread of TSWV is not prevented by chemical treatments because the insecticide-exposed

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L. Bosco et al. / Biological Control 44 (2008) 331–340

viruliferous adults can successfully transmit the virus before death (Momol et al., 2004). In contrast, biotic agents such as predatory mites and bugs, pathogenic fungi and nematodes, integrated with other physical and cultural tactics (i.e. screens, traps, nursery hygiene, resistant cultivars and agro-ecosystem manipulation) have been successful in thrips control inside greenhouses (Jacobson, 1997). Previous research showed that thrips populations increased more quickly on the crops where pesticides were largely used, compared to IPM or organic crops because of the presence of anthocorid predators feeding on thrips (Nagai, 1990; Tavella et al., 1991). In fact, some species of the genus Orius (Heteroptera: Anthocoridae) proved to be effective predators of thrips in both field and greenhouse crops throughout the world. Orius insidiosus (Say), a nearctic species widespread in the original area of WFT, has the intrinsic ability to suppress thrips populations (Sabelis and van Rijn, 1997); moreover, in both greenhouse and field pepper crops thrips populations remained suppressed because of the persistence of predators (van den Meiracker and Ramakers, 1991; Funderburk et al., 2000). Meanwhile in IPM crops of Liguria (north-western Italy) a native anthocorid Orius laevigatus (Fieber) proved to be very efficient in controlling thrips outbreaks when not disturbed by chemical treatments (Tavella et al., 1991, 1996). This species is an effective predator and its predatory effectiveness was surveyed also in other areas of Europe (Villevieille and Millot, 1991; Chambers et al., 1993; Vacante and Tropea Garzia, 1993; Riudavets, 1995; Frescata and Mexia, 1996). O. laevigatus is now produced by many commercial insectaries and largely used in IPM programmes as an important biological control agent. This anthocorid is a western palaearctic species, widespread along Mediterranean and Atlantic coasts, in areas with a marine influence; in Italy it has been recorded in all regions except some alpine zones (Pe´ricart, 1972). In fact, in Piedmont, a more internal region of north-western Italy, where O. laevigatus is usually released in IPM pepper greenhouses, other Orius species are more common on both crop and noncrop plants, such as O. niger Wolff and O. majusculus (Reuter) (Tommasini, 2004), already known as thrips control agents in other areas of Europe (Fischer et al., 1992; van de Veire and Degheele, 1992; Riudavets, 1995; Barbetaki et al., 1999). As a result, surveys were conducted to assess the natural presence and the seasonal abundance of Orius spp. on sweet pepper in a more continental area of north-western Italy without any marine influence, and to compare their colonization and predatory ability with that of the artificially introduced O. laevigatus. Moreover, to evaluate the effectiveness of Orius as biological agents for thrips control, their capacity to reduce thrips populations under field conditions was verified by studying prey– predator relationships.

2. Materials and methods 2.1. Surveyed crops Surveys were conducted on commercial sweet pepper grown under plastic tunnels in the province of Torino (Piedmont, north-western Italy, 4450–59 0 N, 740–44 0 E) during 2002–2003. As in several Mediterranean Countries, in this area greenhouses consist of simple plastic tunnel, often open on the sides during summer. Pepper plants are usually transplanted into greenhouses from mid-March to early April, and harvested starting from early July; seeds are provided and selected by farmers themselves, to maintain traditional cultivars. The 2-year surveys were conducted in a total of 12 commercial greenhouses of about 500 m2 in size: six in different farms and locations in 2002, and six in three different locations (2 tunnels · 3 farms) in 2003. The tunnels were integrated in different agro-ecosystems with other vegetable greenhouses (mostly sweet pepper, tomato, zucchini, strawberry), corn and wheat fields, and sometimes uncultivated surroundings. During the growing season, the standard horticultural practices for the region were used for irrigation, manuring, weed and disease management. Since many pests, such as the European corn borer (ECB), aphids and mites, are highly damaging in north-western Italy, pesticides (i.e. Azadirachtin, Chlorpyrifos-methyl, Cyfluthrin, Exitiazox, Fenazaquin, Imidacloprid, Lambda-cyhalothrin, Lufenuron, Methomyl, Pymetrozine, Thiamethoxam) and beneficial organisms (i.e. Aphidius colemani Viereck, Bacillus thuringiensis Berliner, and Phytoseiulus persimilis AthiasHenriot) were occasionally applied or not at all, depending on the pest management strategy adopted by each farmer. In addition, 3 tunnels in 2002 and 4 tunnels in 2003 were equipped with a screening (2 · 7 mm) to prevent the entrance of ECB and, consequently, to avoid chemical treatments. In both years, releases of commercially available O. laevigatus (Koppert, The Netherlands) were evaluated for thrips control. During 2002, from 1 to 3 fortnightly releases (at the rate of 0.5 adults/m2 each) of the predator were made in three of the six surveyed greenhouses. Moreover, to compare the effectiveness of the introduced species as a biological agent for thrips control with that of the wild species, during 2003 one release at the rate of 1.0 adult/ m2 was done in just one greenhouse for each location, whereas no releases were done in the other one. Therefore the comparison between greenhouses with or without releases was supported by the same environmental conditions. 2.2. Sampling of thrips and anthocorids To monitor the population dynamics on pepper crops, thrips and anthocorids were sampled every 14 days from mid-June to early October in 2002 and every 10 days from late May to late September in 2003, with a total of nine and

L. Bosco et al. / Biological Control 44 (2008) 331–340

12 sampling dates during 2002 and 2003, respectively. Since populations of both thrips and Orius spp. were reported to occur mostly in the flowers of sweet pepper, and sampling flowers was reported to reflect population trends accurately (Shipp and Zariffa, 1991; Shipp et al., 1992), during each survey, 10 open flowers were randomly collected in 5 different sectors of each greenhouse: overall 50 flowers per greenhouse were collected on each sampling date in both years. Each sample of 10 flowers was placed into a single vial containing 70% ethyl alcohol, and transferred to the laboratory for further processing. In 2002 Orius spp. were sampled also on the wild flora growing in the surroundings of the surveyed crops, to assess the natural host plants alternative to pepper in north-western Italy. The sampling on wild flora was carried out twice a month by beating the flowers, when present, or the terminal buds onto a white plastic board (350 · 250 mm); Orius adults and nymphs were then collected with an aspirator and taken back to the laboratory. All plant species sampled in the hedgerows and wastelands were brought to the laboratory and determined according to Pignatti (1997). 2.3. Laboratory analysis In the laboratory, the samples collected in the field were examined: pepper flowers were fragmented and the vial contents rinsed through a series of sieves of decreasing mesh size. The sieves were then examined under a stereomicroscope at 40· magnification, and thrips and anthocorids were separated and counted. Adult thrips were identified to the species level according to Palmer et al. (1989). Adult anthocorids collected on both sweet pepper and wild plants

333

were dissected to extract the genital clasper in males and the copulatory tube in females, and identified to the species level by comparing their genitalia under a stereomicroscope at 100· magnification according to Pe´ricart (1972). 2.4. Statistical analysis Numbers of thrips and Orius spp. in the pepper flowers of each greenhouse were analyzed using a one-way analysis of variance (ANOVA), with a 5% significance threshold, after tests of homogeneity of variance and normality. Means were separated by Tukey-test (SPSS 12.0 version) when ANOVA was significant. To compare the abundance of Orius species, thrips and anthocorid numbers, and prey/ predator ratios in the surveyed tunnels, means were analyzed over time because of strong time and density interactions. Within each greenhouse the sampling sector was considered as a pseudoreplication since there were no statistically significant differences between the five sampling sectors (ANOVA, P = 0.069‚0.997). In 2002 prey/predator ratios were log-transformed to satisfy the assumption of normality. In 2003 means between greenhouses with and without releases were compared and separated with a t-test (SPSS 12.0 version). 3. Results 3.1. Orius population dynamics on sweet pepper Orius populations were surveyed in all greenhouses; besides the introduced O. laevigatus, three other species were collected during both years: O. niger, O. majusculus,

Table 1 Numbers (means per sampling sector over time ± SE) of Orius nymphs and adults sampled on pepper, and adults dissected for identification, in the tunnels with (R) or without (N) releases surveyed during 9 dates in 2002 and 12 dates in 2003 Tunnels

Individuals collected per sector

Adults dissected O. laevigatus a

2002

1R 2R 3R 4N 5N 6N Total No. SED (df 39)

42.6 ± 5.6 37.0 ± 3.8 24.2 ± 3.3 7.6 ± 1.4 10.4 ± 2.2 24.2 ± 2.0 730 4.73

a ab bc d cd bc

5.2 ± 1.5 6.4 ± 1.4 4.6 ± 0.4 0.0 ± 0.0 0.0 ± 0.0 0.0 ± 0.0 81 1.21

2003

1N 1R 2N 2R 3N 3R Total No. SED (df 29)

19.4 ± 1.2 45.2 ± 1.7 29.6 ± 1.1 33.8 ± 1.9 18.8 ± 5.2 12.6 ± 1.5 797 3.60

cd a bc bc cd d

0.8 ± 0.2 5.8 ± 1.1 0.8 ± 0.4 5.8 ± 1.1 0.4 ± 0.2 0.6 ± 0.2 71 0.95

b a b a b b

O. niger

O. majusculus

O. minutus

5.6 ± 0.5 13.8 ± 1.6 4.4 ± 0.8 1.4 ± 0.5 1.6 ± 0.8 9.0 ± 1.1 179 1.38

bc a c c c b

0.6 ± 0.4 1.2 ± 0.7 0.4 ± 0.2 1.0 ± 0.3 4.2 ± 1.1 3.2 ± 0.6 53 0.90

bc bc c bc a ab

0.4 ± 0.4b 0.8 ± 0.2 0.2 ± 0.2 0.2 ± 0.2 0.2 ± 0.2 0.0 ± 0.0 9

11.8 ± 1.0 19.8 ± 2.0 12.6 ± 1.0 13.4 ± 1.8 10.6 ± 1.8 7.8 ± 0.7 380 2.04

b a b b b b

0.6 ± 0.4 0.8 ± 0.5 11.2 ± 1.6 4.2 ± 1.4 2.4 ± 0.7 3.0 ± 1.0 111 1.47

b b a b b b

0.0 ± 0.0b 0.0 ± 0.0 0.6 ± 0.2 0.0 ± 0.0 1.0 ± 0.5 0.0 ± 0.0 8

Within a column, means followed by different letters are significantly different at P < 0.05 with the Tukey-test. a Mean values of O. laevigatus in 2002 did not pass the equal variance test required for ANOVA, even after data transformation. b No statistically analyses were performed on O. minutus data in 2002 and 2003, because the mean values were few.

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L. Bosco et al. / Biological Control 44 (2008) 331–340

and O. minutus L (Table 1). Except for one tunnel in 2002 where O. majusculus prevailed, the most abundant species was always O. niger, accounting for 56% of adult anthocorids totally collected in 2002 and 67% in 2003. O. majusculus followed with 19% in 2002 and 21% in 2003, whereas O. minutus reached only 3% in 2002 and 1% in 2003. Despite the releases, in 2002 O. laevigatus was seldom found and only in the tunnels where it had been introduced (37% of the collected adults). In 2003 O. laevigatus represented 20% of adult anthocorids in

the tunnels where released, and it could migrate also in the nearby ones in which, even if no releases were made, it was rarely collected (4%). The Orius population was generally higher in the greenhouses where O. laevigatus was released (Table 1). In both years the presence/absence of O. laevigatus did not change significantly the amounts of O. niger and O. minutus (±3%); on the contrary, when O. laevigatus overcame 6% of the adult anthocorids, O. majusculus decreased from 40% to 5% in 2002 and from 33% to 9% in 2003.

O. laevigatus 5.0 1N

4.5

1R

4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 5.0

2N

4.5

2R

4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 5.0 4.5

3N

4.0

3R

3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 30-May 10-Jun 20-Jun 01-Jul 11-Jul

22-Jul 01-Aug 12-Aug 22-Aug 02-Sep 12-Sep 24-Sep

Fig. 1. Seasonal abundance (means per 10 flowers each sampling sector ± SE) of O. laevigatus in 2 tunnels, with (R) and without (N) releases, in the 3 farms surveyed in 2003. The arrows indicate the release in the R tunnels.

L. Bosco et al. / Biological Control 44 (2008) 331–340

Orius laevigatus, O. niger, and O. majusculus were present on most sampling dates during the growing season but no O. laevigatus specimens were found before the release date in both years. The distribution and abundance of O. laevigatus and O. niger were compared in 2003 between the 2 nearby tunnels of the same farm with (‘‘R’’) and without (‘‘N’’) release (Figs. 1 and 2). In the R greenhouses, O. laevigatus was mostly collected 10–15 days after the release: at this time the population reached a maximum of

335

0.36 Orius/flower. Since the release, O. laevigatus colonized pepper plants for not more than 6 weeks, disappearing since mid-August (Fig. 1). O. niger seasonal abundance did not show any considerable difference between the R and N tunnels; this species colonized naturally the greenhouses settling on pepper crops from mid-June to September. The largest numbers of O. niger per flower were found between early July and early August (0.32–0.70 Orius/flower), generally earlier in the R than in the N greenhouses (Fig. 2).

O. niger

9.0

1N

8.0

1R

7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0 9.0

2N

8.0

2R

7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0 9.0

3N

8.0

3R

7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0

30-May 10-Jun 20-Jun 01-Jul 11-Jul

22-Jul 01-Aug 12-Aug 22-Aug 02-Sep 12-Sep 24-Sep

Fig. 2. Seasonal abundance (means per 10 flowers each sampling sector ± SE) of O. niger in 2 tunnels, with (R) and without (N) releases, in the 3 farms surveyed in 2003.

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L. Bosco et al. / Biological Control 44 (2008) 331–340

2003; the population was greater at the beginning of both seasons, declining gradually toward extinction. During 2002 thrips and Orius populations were very variable in the 6 surveyed farms (Fig. 3). Orius abundance was higher and prey/predator ratios were significantly lower in the greenhouses where O. laevigatus was released, except for farm 6. In this farm, where no insecticides were applied on pepper crops during the whole season, the mean number of Orius was equal to that in farm 3 R, and the ratio prey/ predator was statistically equivalent with all the R farms. In the other N farms ratios were significantly higher; even if the mean numbers of Orius were not statistically different between farms 4 and 5 (Table 1 and Fig. 3), severe infestations of thrips occurred in the first one despite several insecticide applications. During 2003 thrips populations were greater in N than in R greenhouses (Table 3): in both farms 1 and 2 the mean number of thrips in N greenhouses was respectively 1.8 and 2.3 times greater than in R greenhouses, while in the farm 3 thrips populations did not significantly differ between N and R greenhouses. The mean number of Orius totally collected was greater in the R greenhouses for farms 1 and 2, although only in farm 1 the difference was statistically significant (2.3 time greater); on the contrary in the farm 3 the number of Orius totally collected was lower in the R greenhouse, even though the difference between R and N was not statistically significant. Therefore the mean values of prey/predator ratios ranged greatly in the greenhouses, from 1 (tunnel 2 R) to 76 (tunnel 1 N). The farm 1 showed the greatest difference

3.2. Orius distribution and abundance on wild flora In the flora surrounding the surveyed greenhouses, 23 plant species of 14 plant families, flowering during the pepper growing season, were sampled in 2002 (Table 2). Not all plant species were present at every greenhouse each sampling date or in the same quantity, resulting in different numbers of plants. Adult Orius spp. were collected in different amounts in the flowers of 14 plant species of 9 plant families. A total of 88 Orius specimens were collected on the wild flora: 76% O. niger, 16% O. majusculus, and 8% O. minutus, whereas O. laevigatus was never found. O. niger was sampled on 13 different plant species, O. majusculus and O. minutus on 7 plant species each. Independent of Orius population abundance, only Urtica dioica L., Sinapis arvensis L., and Matricaria chamomilla L. hosted all the three Orius species. Medicago sativa L., Sambucus ebulus L., and Vicia sativa L. hosted the majority of the Orius. 3.3. Thrips control by Orius spp. Over 97% of the thrips sampled in the pepper flowers in both years belonged to F. occidentalis and T. tabaci. Thrips infestations were in general more severe in 2003 than in 2002, probably favoured by the unusual high temperatures recorded throughout the summer 2003. F. occidentalis reached 82% of adult thrips totally collected in 2002 and 90% in 2003; generally populations peaked twice during both years: in mid-July and in late September. T. tabaci reached 15% of adult thrips collected in 2002 and 9% in

Table 2 Orius species collected on wild flora growing around the surveyed pepper tunnels in 2002 (+ = presence,  = absence of adults) Families

Urticaceae Polygonaceae Chenopodiaceae Amaranthaceae Portulacaceae Caryophyllaceae Papaveraceae Brassicaceae

Fabaceae

Hypericaceae Solanaceae Caprifoliaceae Asteraceae

Poaceae

Plant species

Urtica dioica Polygonum persicaria Chenopodium album Amaranthus retroflexus Portulaca oleracea Stellaria media Papaver rhoeas Capsella bursa-pastoris Brassica napus Sinapis arvensis Vicia sativa Medicago sativa Trifolium repens Hypericum perforatum Solarium nigrum Sambucus ebulus Erigeron annum Conyza canadiensis Galinsoga ciliata Matricaria chamomilla Sonchus oleraceus Phleum pratense Echinoclhoa crus-galli

Tunnel 1

Tunnel 2

On

Oma

Omi

+





 

 

 

Tunnel 3

Om

Omi

On

Oma

Omi

+ +  + 

+   + 

+    

  

  

  







+ +

 

+ 

+





+

Tunnel 5

Tunnel 6

On

Oma

Omi

On

Oma

Omi

On

Oma







 

 

+ 

  +

+  

  











 

 

 

+



 









+

  +







+   +

+   

   

+

On, O. niger; Oma, O. majusculus; Omi, O. minutus.

Tunnel 4

On

 



 +





+ 

+

 

+

 

+ + + +

  + +

   -

 +

 +

 +













L. Bosco et al. / Biological Control 44 (2008) 331–340

337

50

220

Orius spp. thrips/Orius

45

200

174.3 a

180

40

160 140

30

120 25 100 20

ratio

mean number

35

80

15

60

10

40

22.2 b

5

3.5

cd

3.9

1.0 d

3.4 cd

c

0

20 0

1

3

2

4

farms R

5

6

farms N

Fig. 3. Orius abundance and prey/predator ratio (±SE) in the 6 farms, with (R) and without (N) releases, surveyed during 9 dates in 2002. Ratios followed by different letters are significantly different at P < 0.05 with the Tukey-test. Analyses of ratios are based on log-transformed data but raw values are given.

Table 3 Comparison of thrips and Orius populations (mean numbers per sampling sector over time), and thrips/Orius ratios between the tunnels with (R) and without (N) releases in the 3 farms surveyed during 12 dates in 2003 Farm 1

df = 8 Thrips SED (sig.) Orius spp. SED (sig.) Thrips/Orius SED (sig.)

Farm 2

Farm 3

N

R

N

R

N

R

1465.80 121.81(**) 19.40 2.12(**) 76.15 5.22(**)

794.20

78.00 8.77(*) 29.60 — 2.62 0.26(**)

33.00

639.80 — 18.80 — 42.69 —

472.40

45.20 17.56

33.80 1.00

12.60 40.09

Standard error difference (SED) values followed with an asterisk (*) or two (**) are significantly different at P < 0.05 or P < 0.001, respectively, with the ttest. When SED value is missing (—) there were no statistically significant differences between tunnels R and N.

between the two treatments, followed by the farm 2 in which the thrips/Orius ratios were very low; in the farm 3 although in the R greenhouse there was a lower ratio, once more the difference among the two treatments was not statistically different. Overall, during both growing seasons, when the thrips/ Orius value was 650, thrips populations were effectively suppressed within the next sampling date, if chemical control did not affect negatively anthocorid populations. 4. Discussion During the two growing seasons, the presence of thrips and anthocorids was very variable in the surveyed commercial sweet pepper greenhouses. Both the native T. tabaci and the nearctic F. occidentalis were found in the crops, but only the latter species caused high infestation levels

confirming to be the most harmful thrips on pepper also in this area of north-western Italy, as observed in other regions of Italy and Europe (Tommasini and Maini, 1995; van Rijn et al., 1995). Biological control using Orius (artificial releases or natural crop colonization) plays an important role in thrips management, since chemical treatments are not always able to keep thrips populations under the economic threshold. In fact, irrespective of the species, Orius proved an effective biological control agent with prey/predator ratios = 50, as reported in prediction models (Sabelis and van Rijn, 1997), and consistent with both laboratory and pepper field experiments with O. insidiosus preying on F. occidentalis (Xu et al., 2006; Funderburk et al., 2000). For successful thrips control by Orius introduction, the timing of releases is very important: releases that are either too early or too late do not help the establishment of the predator and a good interaction between

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prey and predator. As assessed in previous research in north-western Italy (Tavella et al., 1996), the best time for the release on pepper crops is nearly one month after transplanting (i.e. in our region between mid-May and mid-June), when the plants are flowering and fully grown. Orius laevigatus is the most common species in several regions of the Mediterranean basin (Afifi et al., 1976; Villevieille and Millot, 1991; Riudavets and Castan˜e´, 1998; Tavella et al., 1991,2000). In the surveyed area, it was scarcely found, only in the tunnels in which it was released (or in the nearby ones), and never on the wild flora growing in the surroundings of the greenhouses. According to Pe´ricart (1972), that did not report the presence of O. laevigatus in some alpine zones of Italy, in this more continental region, not subject to the marine influence, other Orius spp. are widespread on crop and noncrop plants: O. niger, O. majusculus, and O. minutus. Therefore, the most important role in preying thrips is carried out by these wild Orius species, not because they are more effective predators, but obviously better adapted to local climatic conditions. This fact has to be considered particularly in the crops under plastic tunnels, where climatic conditions are similar to outdoor environmental conditions, differently from what occurs in the high technology greenhouses of CentralNorth Europe. Moreover, the plastic tunnels, as well as the open greenhouses of the Mediterranean area, allow the indigenous natural enemies to move easily in and out the crops. In this study, O. laevigatus colonized pepper plants for not more than 6 weeks, disappearing since mid-August. As in other comparative studies between introduced and native anthocorids, the former often struggles to reproduce and establish on the crop, even if its efficiency as a predator is well known and reported. So in Europe, compared to the nearctic O. insidiosus, all the native palaearctic O. albidipennis (Reuter), O. laevigatus, and O. niger showed a better colonization ability replacing totally the introduced anthocorid at the end of the growing season (van de Veire and Degheele, 1992; van de Veire, 1995; Tavella et al., 2000). In the surveyed area, both on sweet pepper (56% in 2002 and 67% in 2003 of all the collected adults) and on wild flora (76% of all the collected adults) the most abundant species was always O. niger, which managed to establish in all tunnels and proved to be the most suitable predator, as it was observed also in central and southern Greece (Barbetaki et al., 1999) and in Belgium (van de Veire and Degheele, 1992). Starting from late June this species colonized the crops naturally and, compared to the introduced O. laevigatus, could reproduce and develop throughout the whole growing season, if not disturbed by chemical treatments. In fact, many classes of insecticides, including several synthetic pyrethroids largely used on vegetable crops, are toxic to species of Orius and the negative side-effects of broad-spectrum pesticides on these beneficial predators are known (Delbeke et al., 1997; Silveira et al., 2004). Starting from August, several sprays with insecticides (i.e. Thiamethoxam and Lambda-cyhalothrin, toxic for Orius spp.,

according to Biobest, 2004) were applied in the greenhouses surveyed in 2003 to control ECB, aphids and southern green stink bug infestations: the insecticide applications probably affected negatively Orius spp. which disappeared from crops before the end of the growing season. Although O. laevigatus does not seem to establish on the crop, the release can have a positive effect on the early establishment of wild anthocorids: in 2003, O. niger peaked earlier in tunnels of farms 2 and 3, in which releases were made. Moreover, the introduced species did not show any intra-guild competition with O. niger, whereas a kind of competition could be hypothesized between O. laevigatus and O. majusculus. In fact, when O. laevigatus was >6% of the adult anthocorids, O. majusculus population decreased from 40% to 5% in 2002 and from 33% to 9% in 2003. Competition between Orius species, particularly between the introduced and the native species, is a matter of crucial importance for biological control tactics. A previous study on intra-guild predation and cannibalism between the exotic O. insidiosus and the native O. laevigatus under laboratory conditions showed no differences: for both species predation was never higher than cannibalism (Tommasini et al., 2002). However, competition and its possible mechanisms have been poorly investigated so far, and therefore need to be further studied. The Orius population was generally higher in the greenhouses where O. laevigatus was released (Table 1), probably due to the adopted pest management strategy and to the reduction of insecticide applications. In fact, after the release of O. laevigatus, growers reduced chemical treatments and chose more selective insecticides, so Orius populations increased both as the effect of releases, and as a spontaneous colonization of the crops by wild species. Pest control strategies play a more important role than the release itself. For example, in 2003 in farm 1 the application of Imidacloprid (toxic for Orius spp., according to Biobest, 2004) at the beginning of July only in the tunnel without anthocorid releases can explain the lower number of O. niger in that tunnel than in the tunnel where O. laevigatus was introduced. On the other hand, in 2002 the populations of Orius recorded in farm 6, in which no pesticides were used, equalled the amounts observed in the farms in which releases were made. The opportunity and the economic suitability of O. laevigatus releases has still to be assessed in crop conditions of this area of north-western Italy, even if it seems to anticipate thrips control before crop colonization by wild Orius spp. which generally enter sweet pepper greenhouses too late in the growing season for a successful control. In fact, if not promptly controlled, thrips populations increase rapidly reaching high infestation levels detrimental for the yield. Moreover, early thrips infestations are the most harmful for the spread of TSWV that is now the major concern for pepper in Piedmont. Better results could be obtained with the preservation of Orius populations naturally present: no insecticides or only selective ones should be applied to allow the predators to establish on the crops

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and to carry out an efficient thrips control throughout the growing season. Further research is needed to understand how to anticipate the natural colonization of pepper by anthocorids, especially using a correct management of the agro-ecosystem enclosing fields: wild plants in the surroundings may positively influence the occurrence of natural enemies on crops. With this aim, the knowledge of natural host plants preferred by Orius spp. becomes very important; in fact, it is known that among vegetables predatory bugs show a preference for some crops such as sweet pepper, eggplant, bean, melon, and strawberry, whereas they have never or rarely been found on tomato (Tommasini, 2004), on which despite bi-weekly releases at a rate of 10 adults per plant O. insidiosus failed to reduce the thrips population to economically acceptable levels (Shipp and Wang, 2003). As in Tommasini (2004), O. niger occurred on a large range of host plants, almost all the plant species sampled (Table 2). Therefore this species, well adapted to the local climate and to the main plant species, seems a good candidate for biological control of thrips pests in this area of north-western Italy. Acknowledgments The authors are grateful to E. Faure, Gruppi Coltivatori Sviluppo of Torino, for the technical assistance. This research was supported by grants of Provincia di Torino. References Afifi, A.M., Farghali, H.T., Rezk, G.N., Ragab, Z.A., 1976. Seasonal abundance of certain pests and predators in clover fields in Egypt. Bulletin of the Entomological Society of Egypt 60, 273–278. Arzone, A., Alma, A., Rapetti, S., 1989. Frankliniella occidentalis (Perg.) (Thysanoptera Thripidae) nuovo fitomizo delle serre in Italia. Informatore fitopatologico 39 (10), 43–48. Barbetaki, A., Lykouressis, D., Perdikis, D., 1999. Predatory species of the genus Orius recorded in fields of vegetable crops in Greece. IOBC/ WPRS Bulletin 22 (5), 97–101. Biobest, 2004. Side Effects Manual. Biobest, fourth edition. Broadbent, A.B., Pree, D.J., 1997. Resistance to insecticides in populations of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) from greenhouses in the Niagara region of Ontario. The Canadian Entomologist 129, 907–913. Brødsgaard, H.F., 1994. Insecticide resistance in European and African strains of Western Flower Thrips (Thysanoptera: Thripidae) tested in a new residue-on-glass test. Journal of Economic Entomology 87, 1141– 1146. Chambers, R.J., Long, S., Heyler, N.L., 1993. Effectiveness of Orius laevigatus (Hem.: Anthocoridae) for the control of Frankliniella occidentalis on cucumber and pepper in UK. Biocontrol Science and Technology 3, 295–307. Delbeke, F., Vercruysse, P., Tirry, L., de Clercq, P., Degheele, D., 1997. Toxicity of diflubenzuron, pyriproxyfen, imidacloprid and diafenthiuron to the predatory bug Orius laevigatus (Het.: Anthocoridae). Entomophaga 42, 349–358. Fischer, S., Linder, C., Freuler, J., 1992. Biologie et utilisation de la punaise Orius majusculus Reuter (Heteroptera, Anthocoridae) dans la lutte contre les thrips Frankliniella occidentalis Perg. et Thrips tabaci Lind., en serre. Revue Suisse de Viticulture, d’Arboriculture et d’Horticulture 24 (2), 119–127.

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