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Phytoparasitica (2010) 38:313–325

DOI 10.1007/s12600-010-0105-9

Influence of weedy field margins on abundance patterns


of the predatory bugs Orius spp. and their prey, the western
flower thrips (Frankliniella occidentalis), on faba bean
Ekrem Atakan

Received: 7 January 2010 / Accepted: 28 June 2010 / Published online: 22 July 2010
# Springer Science+Business Media B.V. 2010

Abstract The influence of weedy field strips on the predators, such as nectar, pollen, shelter and egg-
abundance patterns of western flower thrips, laying sites rather than as sources of insect prey.
Frankliniella occidentalis (Pergande) (Thysanoptera: Cultivation of faba bean could be useful for conserva-
Thripidae), and predatory bugs of Orius spp. (Hemi- tion and augmentation of beneficial insects, including
ptera: Anthocoridae), on faba bean and on weeds was Orius spp. Furthermore, field margins bearing flower-
investigated in Adana province, Turkey, during 2005– ing weeds such as S. arvensis and L amplexicaule
2006. There were two treatments: in one treatment, should be protected against destructive management
weeds at the margins and inside the plots were practices, because they host considerable numbers of
regularly controlled by tillage; in the other treatment the Orius species.
no weed control was done. Thrips and Orius were
sampled by beating faba bean plants and weeds. Orius Keywords Lamium amplexicaule . Prey-predator
niger (Wolff) was the most abundant predatory insect interactions . Polyphagous predators . Sinapis
species in faba bean and flowering weeds, with arvensis . Vicia faba . Weeds
numbers of adults and nymphs significantly greater in
plots with weedy margins than in weed-free plots.
Flowering weeds did not contribute to the abundance Introduction
of F. occidentalis on faba bean. Abundance of adults of
Orius spp. did not coincide with the abundance of Faba bean (Vicia faba L.) is an important nutritious
F. occidentalis on faba bean or weeds. There were human food crop containing high protein levels (Anon.
significant negative associations for numbers of Orius 2001). It is widely cultivated, together with other winter
spp. among faba bean and the weed species Lamium vegetable crops, in the eastern Mediterranean region of
amplexicaule L. or Sinapis arvensis L. (P<0.05), Turkey. Faba bean is also a good rotational crop for
indicating movement of Orius individuals from the fixing nitrogen and thus enhancing soil fertility. The
weeds to faba bean during March–April. Finally, faba production of this crop ranks fourth among leguminous
bean and weeds may provide some benefits to crops in Turkey. Faba bean is consumed as either green
pods or dried beans in the Aegean and Mediterranean
regions of Turkey (Anon. 2001).
E. Atakan (*) The polyphagous predators Orius spp. (Hemi-
Plant Protection Department, Faculty of Agriculture, ptera: Anthocoridae) are often considered important
Çukurova University,
Adana 01030, Turkey natural enemies of thrips (Riudavets et al. 1995). In
e-mail: eatakan@mail.cu.edu.tr Turkey, Orius niger (Wolff) effectively suppresses
314 Phytoparasitica (2010) 38:313–325

the Frankliniella flower thrips in cotton fields in the Materials and methods
Çukurova region that are not treated with insecti-
cides (Atakan 2006; Atakan and Gençer 2008). Study site This work was carried out on the Research
Orius spp. were also recorded on various vegetable and Application Farm (RAF) of the Faculty of
crops grown in different parts of Turkey (Bulut and Agriculture, University of Çukurova, during two
Göçmen 2000; Yaşarakıncı and Hıncal 2000). Orius growing seasons, 2004/05 and 2005/06. The experi-
spp. are important biological control agents that are mental area (37° 01.809´ N; 35° 21.694´ E) has high
able to regulate populations of the serious pestifer- plant biodiversity, i.e., it is a polyculture area which
ous thrips—the western flower thrips Frankliniella includes winter vegetables (onion, broccoli, lettuce
occidentalis (Pergande) (Thysanoptera: Thripidae)— and red cabbage), wheat, and annual summer crops
especially in protected crops (Tavella et al. 2000, (cotton and maize) grown in small plots. Various
2003; Tommasini 2004; van de Veire and Degheele citrus trees (lemon, orange, mandarin and grapefruit)
1992). It has been well established that O. niger can and olive trees are also grown there commercially.
manage F. occidentalis in glasshouse cultivation of Winter or annual summer crops are usually grown in
sweet pepper (van de Veire and Degheele 1992). In plots of 1.5 ha; citrus and olives are grown in plots of
contrast, the role of Orius spp. as predators of thrips 2.2 ha and 1.5 ha, respectively.
on winter crops, such as faba bean, or on weeds, has
not been well studied in the Mediterranean region. Experimental procedure The experimental area of faba
It is well known that weeds affect the popula- bean (cv. ‘Lara’) was located near citrus (mandarin and
tions of herbivorous insects and their natural orange) and olive trees. Wheat and lettuce (plots of 50 or
enemies by providing alternative food as well as 100 m2) and other winter vegetable crops (plots of
sites for mating, hibernation and shelter (Frank and 200 m2) were also grown nearby. There were two
Reichhart 2004; Gurr et al. 2005; Landis et al. 2000; treatments: in one treatment, weeds in the margins and
Marshall and Moonen 2002). Vegetative buffers such inside the plots were regularly controlled by tillage;
as weedy field margins are often recognized as and in the other treatment, no weed control was
having an important place in sustainable agriculture conducted in plot margins but weeds inside the plots
because of their role in an increasing functional were regularly managed. In the latter, weeds such as
biodiversity and in encouraging cyclic movements of Calendula arvensis L., Fumaria officinalis L., Lamium
predators between crops and the natural environment amplexicaule L., Melilotus officinalis (L.), Ochtodium
(Landis and Wratten 2002; K.Winkler, Ph.D. thesis, aegyptiacum (L.), Senecio vernalis Waldst. & Kit and
Wageningen Univ., 2005). The effect of weedy field Sinapis arvensis L. grew naturally in the margins of the
margins on thrips and their generalist predators in plots. The total size of the experimental area was
relation to crop plants has not been studied. Also, the 1,375 m2 (55 m×25 m). A split-plot design was used
relationships between winter–spring crops and with four replicates for each treatment. The size of
winter-flowering weeds on prey–predator dynamics each plot was 100 m2 (10 m×10 m). Each plot with
are not known. Faba bean flowers from early winter weedy margins (PWWM) was bounded on all four
to spring, and during this period various ecological sides by an untreated strip of 20 m2 (10 m long×2 m
interactions between F. occidentalis and Orius wide). Experimental plots were separated by a
populations are expected. This crop system may also 5-m-wide strip of bare ground.
allow us to understand the predation abilities of Faba bean was planted on 5 October 2004 and 15
Orius spp. on pestiferous insects of other arable October 2005. No pesticides were applied during the
crops in the region. course of the experiment.
The main objectives of this study were to assess the (a)
species composition of Orius spp. and other beneficial Sampling of insects on faba bean and weeds
insects on faba bean plots with and without weedy field Sampling of insects started when faba bean and weed
margins, (b) abundance patterns of F. occidentalis on species began to flower, because populations of both
faba bean plots with and without weedy field margins, Frankliniella spp. and Orius spp. occurred mostly on
and (c) preference of F. occidentalis and O. niger for the flowers of field crops such as cotton (Atakan et al.
certain faba bean plant parts. 1998; Atakan and Özgür 2004) and weeds (Atakan
Phytoparasitica (2010) 38:313–325 315

and Uygur 2004) in the region. Sampling of flowers Distribution of thrips and Orius on plant parts of faba
was reported to show the population trends of both bean To determine the abundance of thrips and
thrips and Orius spp. accurately (Shipp and Zariffa Orius on two plant parts, plants were sampled
1991; Shipp et al. 1992). Faba bean and weeds were weekly on eight different dates in February (four
sampled from January to April of both years. Sample sampling dates) and March (four sampling dates) of
size was five randomly selected plants per plot of faba both years. Five plants were randomly selected from
bean and of each of the four prevalent weed species, each plot. Six leaflets or flowers (two leaflets or
C. arvensis, L. amplexicaule, O. aegyptiacum and flowers from each of three plant sections, upper,
S. arvensis in the plots' margins. Insect species were middle and lower) from each plant were collected
sampled by beating the plants vigorously over a white from each section and kept frozen. For extraction of
plastic container (37×28×7 cm) for about 5 s. insects, plant parts were submerged in 2% detergent
Collected F. occidentalis and Orius species were solution and agitated for 25 s. The solutions were
counted in the field using a hand lens. Most Orius then poured through a standard testing sieve No. 80
specimens were returned to the plots and a few were (180 μm). Thrips and predators extracted from
taken to the laboratory for identification. Insects that solution were transferred into small vials containing
could not be identified in the field were collected and 60% ethanol for subsequent processing. Each empty
kept in 60% ethanol. bag was rinsed two times in the same way. The thrips
In the laboratory, the thrips samples were trans- and predators were identified according to the
ferred to vials containing AGA solution (10 parts procedures detailed by Atakan (2006). Identified
60% ethanol, one part glacial acetic acid, and one insect specimens were counted separately under a
part glycerin) and kept for 1 day. Thrips species were stereomicroscope with ×45 magnification.
slide-mounted and identified under a binocular
microscope. Data analysis The abundance of other insect
species, including thrips and other predators, was
Insect identification Thrips species were identified not evaluated because their numbers were too few
by the author. Orius spp. were identified following on most sampling dates. Data collected on thrips
Önder (1982) and Tommasini (2004). Other preda- larvae were not analyzed because their numbers
tors or pest insect species collected were identified were very low on faba bean or weeds.
by using reference material deposited at the Ento- Effects of treatment and sampling dates on the
mology Laboratory of the Plant Protection Depart- abundance of Orius spp. adults (pooled) and Orius
ment, Faculty of Agriculture, University of spp. nymphs (pooled) and F. occidentalis adults
Çukurova, Adana, Turkey. Representative adult were analyzed by General Linear Model (GLM)-
thrips were slide-mounted for identification. Imma- repeated measure statistical analysis. Weekly com-
ture thrips (thrips larvae) and nymphs of the Orius parisons of the numbers of thrips and Orius on faba
specimens were pooled into a single category beans throughout the sampling period between the
because no comprehensive keys are available for two treatments were done using Student’s t-test at
their identification. P < 0.05.
Orius niger was the most easily distinguishable Numbers of F. occidentalis and Orius spp. on each
species, being almost entirely black except for the plant part (leaves and flowers) were pooled over
antennae and front tibiae or the knee and distal part of sampling dates and sampling years. Their mean
the front femur, which are light yellow-brown. Body numbers were grouped by Tukey’s honestly signifi-
color of Orius laevigatus (Fieber) was dark or light cant difference (HSD) test at P<0.05.
brown. In O. laevigatus the legs were completely dark Seasonal comparisons of the numbers of thrips and
or light yellow-brown. In some specimens, a yellow- Orius on the weed species were quantified by one-
ish prothoracic femur and dark brown mesothoracic way analysis of variance (ANOVA) at P<0.05. Their
and metathoracic femurs with yellowish distal parts mean numbers were grouped by the Tukey’s HSD test
were observed. at P<0.05.
Identified insect samples were counted separately Relationships between the numbers of Orius and
under a stereomicroscope with ×45 magnification. F. occidentalis in four weed species and in faba bean
316 Phytoparasitica (2010) 38:313–325

were evaluated by quadratic regression analysis at species (O. niger and O. laevigatus) were collected
P<0.05. from S. arvensis and L. amplexicaule, whereas the
All analyses were performed using the Microsoft numbers of Aeolothrips collaris Priesner on four weeds
statistics program SPSS 15.0. (SPSS, 2006). were usually similar in both years (Table 2).

Species compositon of Orius on weeds and faba


bean. Orius niger was the main predatory bug on all
Results four weed species sampled on most sampling dates.
O. laevigatus was the most common on S. arvensis
Predatory insect species on faba bean and weeds and L. amplexicaule on some sampling dates in
Seasonal total numbers of predators identified in faba March in both years. O. niger was the most prevalent
bean plots and weeds naturally grown in the plot insect predator on faba bean on most sampling dates,
margins are summarized in Tables 1 and 2. A total of in all plots in both years. However, in March,
ten predaceous insect species were identified in O. laevigatus was relatively more abundant.
PWWM and plots with no weedy margins (PNWM)
(Table 1). Seasonal numbers of both Orius species in Abundance of Frankliniella occidentalis and Orius on
the plots were clearly different while numbers of weeds Trends in population dynamics of either total
coccinellids, chrysopids, mirids, staphylinids and pred- adults of Orius or F. occidentalis in abundance in all
atory thrips in abundance in both plots were usually sampled weed species growing in plot margins were
similar. Faba bean plots had rich insect fauna (Table 1) similar in both years (Fig. 1a, b, c, d). Mean numbers
as compared with the insect species composition found of F. occidentalis were very low on C. arvensis and
in weed species, where only three predator species L. amplexicaule throughout the sampling dates in
were detected (Table 2). The majority of both Orius both years (Fig. 1a, b). F. occidentalis were collected

Table 1 Numbers of predators identified and sampled in faba bean plots with or without weeds during the winter–spring period of
2005–2006 in Adana province, Turkey

Predatory insects [Order/family] Total no. of predatory insects on faba bean

Year 2005 Year 2006

Plot with Plot without Total Plot with Plot without Total
weeds weeds weeds weeds

Coccinella semptempunctata L. [Coleoptera/ 7 3 10 3 1 4


Coccinellidae]
Scymnus levaillanti Mulsant [Coleoptera/ 7 2 9 3 1 4
Coccinellidae]
Scymnus pallipediformis Goeze [Coleoptera/ 2 1 3 0 0 0
Coccinellidae]
Paederus litoralis Gravenhorst [Coleoptera/ 2 1 3 3 1 4
Staphylinidae]
Tachyporus sp. [Coleoptera/Staphylinidae] 6 2 8 25 14 39
Orius niger (Wolff) [Hemiptera/Anthocoridae] 74 33 107 174 83 257
Orius laevigatus (Fieber) [Hemiptera/Anthocoridae] 18 9 27 34 4 38
Orius nymphs 148 85 233 103 28 131
Campylomma sp. [Hemiptera/Miridae] 4 1 5 3 2 5
Chrysoperla carnea (Stephens) [Neuroptera/ 6 1 7 8 3 11
Chrysopidae]
Aeolothrips collaris Priesner [Thysanoptera/ 16 12 28 12 10 22
Aeolothripidae]
Total 290 150 440 368 147 515
Phytoparasitica (2010) 38:313–325 317

Table 2 Numbers of
predators sampled on weed Weed species Total no. of predators on weeds
species during the
winter–spring period of Aeolothrips collaris Orius niger Orius laevigatus
2005–2006 in Adana
province, Turkey 2005 2006 Total 2005 2006 Total 2005 2006 Total

Calendula arvensis 2 1 3 9 33 42 4 2 6
Lamium amplexicaule 1 3 4 48 55 103 13 19 32
Ochtodium aegyptiacum 8 12 20 12 18 30 1 6 7
Sinapis arvensis 21 19 40 67 62 129 16 25 41
Total 32 35 67 136 168 304 34 52 86

mainly from O. aegyptiacum and S. arvensis in both F. occidentalis on O. eagyptiacum and S. arvensis
years (Fig. 1c, d). Mean numbers of F. occidentalis increased steadily to considerable levels after late
increased clearly on both weed species after the first March, when Orius individuals were absent or their
week of April. Thrips were very few or nonexistent numbers were very low in both years (Fig. 1c, d).
until the end of March in the presence of high Most adults of Orius spp. were detected on
densities of total Orius spp. Population densities of L. amplexicaule and S. arvensis during the sampling

Fig. 1 Infestation levels of


adult Frankliniella occiden-
talis and Orius spp. on
weeds grown on the mar-
gins of faba bean plots:
Calendula arvensis a, Lam-
ium amplexicaule b, Ochto-
dium aegyptiacum c and
Sinapis arvensis d, in 2005–
2006
318 Phytoparasitica (2010) 38:313–325

Table 3 Regression analysis among mean numbers of Orius spp. and Frankliniella occidentalis in four weed species growing in the
margins of faba bean plots in Adana province, Turkey, in 2005–2006

Weed species Associations/years df R2 F P Equations

Calendula arvensis Orius adult and thrips adult/2005 2, 15 0.06 0.397 0.681 Y ¼ 18:715x2 þ 5:9127x þ 0:3558
Orius adult and thrips adult/2006 2, 16 0.25 2.269 0.143 Y ¼ 7:8802x2  2:9955x þ 0:3099
Lamium amplexicaule Orius adult and thrips adult/2005 2, 15 0.15 1.785 0.371 Y ¼ 1:2436x2  1:198x þ 0:1819
Orius adult and thrips adult/2006 2, 16 0.25 2.266 0.143 Y ¼ 1:092x2  1:5723x þ 0:4128
Ochtodium aegyptiacum Orius adult and thrips adult/2005 2, 15 0.30 2.636 0.113 Y ¼ 303:89x2  97:032x þ 0:5931
Orius adult and thrips adult/2006 2, 16 0.08 0.169 0.559 Y ¼ 49:705x2 þ 25:167x þ 1:6804
Sinapis arvensis Orius adult and thrips adult/2005 2, 15 0.76 23.854 0.0001 Y ¼ 54:632x2  66:693x þ 17:771
Orius adult and thrips adult/2006 2, 16 0.40 4.326 0.036 Y ¼ 15:369x2  21:728x þ 7:8689

dates in both years (Fig. 1b, d). In general, the and F. occidentalis on the other weed species sampled
numbers of Orius individuals peaked on the weed (Table 3 and Fig. 2a, b, c).
species in early March in 2005 and 2006.
Overall, the numbers of F. occidentalis and Orius spp. Distribution of Frankliniella occidentalis and Orius
(adults + nymphs) were significantly higher on S. on two plant parts of faba bean. Frankliniella
arvensis than on other weed species sampled in 2005 occidentalis (adults) and Orius spp. (adults +
(F. occidentalis: F=655.562, d.f.=3, 76, P=0.0001; nymphs) were collected mainly from the flowers of
Orius spp.: F=30.206, d.f.=3, 76, P=0.0001, respec- faba bean in PWWM (Fig. 3a) and in PNWM
tively) and in 2006 (F. occidentalis: F=469.236, d.f.=3, (Fig. 3b) in both years. Orius nymphs were found
76, P=0.0001; Orius spp.: F=12.882, d.f.=3, 76, only on flowers, but their numbers were very low on
P=0.0001, respectively). most sampling dates in all plots.
Seasonal population patterns of Orius spp. were
significantly compatible with the population fluctua- Abundance of Frankliniella occidentalis and Orius
tions of F. occidentalis only on S. arvensis in both populations on faba bean Plot type, sampling dates,
years (Table 3 and Fig. 2d; P<0.05). No relationship sampling years and various interactions had significant
was detected among the mean numbers of Orius spp. effects on the abundance of F. occidentalis (Table 4).

Fig. 2 Relationships among


mean numbers of Orius spp.
and numbers of Frankli-
niella occidentalis in Ca-
lendula arvensis a, Lamium
amplexicaule b, Ochtodium
aegyptiacum c and Sinapis
arvensis d, in 2005–2006
Phytoparasitica (2010) 38:313–325 319

Fig. 3 Distributions of
adults of Frankliniella occi-
dentalis and Orius spp.
(mean±SE) on faba bean in
plots with a and without b
weedy margins, in 2005–
2006. Asterisk denotes the
level of significance; t-test
at *P<0.05, **P<0.001

Early colonization of F. occidentalis on faba bean was thrips peaked (0.22±0.12 per plant) on 14 March 2005
detected in PWWM in both years (Fig. 4a). The and 23 March 2006 (0.61±0.30 per plant) (Fig. 4a). In
number of adult thrips peaked (1.21±0.22 per plant) on 2005, the mean numbers of thrips in PWWM were
14 March 2005 and 11 March 2006 (2.52±0.61 per significantly higher than the numbers in PNWM on 21
plant) in PWWM. In PNWM, the number of adult February, 7 March and 14 March (t 38 = 3.230,

Table 4 Effects of plot


type, year and sampling Sources df MS F
date on population densities
of adult Frankliniella occi- Frankliniella occidentalis
dentalis and Orius spp. Plot type (with weeds and without weeds) 1 36.053 76.524 ***
(nymphs + adults) Year 1 8.670 18.402 ***
Plot type x year 1 4.083 8.667 **
Error 76 0.741
Date 14 6.907 14.089 ***
Date x plot type 14 2.050 4.181 *
Date x year 14 1.513 3.086 *
Date x plot type x year 14 2.883 5.882 *
Error (date) 1064 0.490
Orius spp.
Plot type 1 126.101 55.113 ***
Year 1 0.041 0.018 NS
Plot type x year 1 6.601 2.885 NS
Error 76 2.288
Date 14 14.388 7.413 ***
Date x plot type 14 13.403 6.605 ***
Date x year 14 17.253 8.889 ***
* P<0.05, ** P<0.01, *** Date x plot type x year 14 29.313 15.102 ***
P<0.001
Error (date) 1064 1.941
NS: not significant
320 Phytoparasitica (2010) 38:313–325

Fig. 4 The effects of weedy margins on the infestation levels of adult Frankliniella occidentalis a and Orius spp. b (mean±SE) on
faba bean in plots with and without weedy margins, in 2005–2006

P=0.0002; t38 =2.508, P=0.01; t38 =3.946, P=0.0003, P=0.001; t38 =4.328, P=0.0001, t38 =3.928, P=0.0003,
respectively; Fig. 4a). In 2006, mean numbers of thrips respectively; Fig. 4a).
in PWWM were significantly higher on 12 January, 11 Plot type, sampling dates, sampling years and
March and 30 March than in PNWM (t38 =3.321, various interactions had significant effects on the

Table 5 Regression analysis between mean numbers of Orius spp. and Frankliniella occidentalis in faba bean plots with weedy
margins or plots without weedy margins in Adana province, Turkey, in 2005–2006

Plot type Associations/years df R2 F P Equations

Plot with weeds Orius adult and thrips adult/2005 2, 15 0.22 1.767 0.212 Y ¼ 1:0533x2 þ 2:0675x þ 1:5536
Orius adult and thrips adult/2006 2, 16 0.12 0.944 0.414 Y ¼ 0:3618x2 þ 1:1617x þ 1:7071
Orius nymph and thrips adult/2005 2, 15 0.02 0.153 0.860 Y ¼ 0:1477x2  0:5624x þ 0:7421
Orius nymph and thrips adult/2006 2, 16 0.05 0.400 0.679 Y ¼ 0:1477x2 þ 22x þ 0:9667
Plot without weeds Orius adult and thrips adult/2005 2, 15 0.19 1.489 0.264 Y ¼ 96:667x2  14x þ 0:1333
Orius adult and thrips adult/2006 2, 16 0.29 2.758 0.100 Y ¼ 2:6138x2 þ 3:6013x þ 0:7868
Orius nymph and thrips adult/2005 2, 15 0.42 4.515 0.035 Y ¼ 68:330x2  14x þ 0:1333
Orius nymph and thrips adult/2006 2, 16 0.13 0.995 0.396 Y ¼ 0:4786x2  0:5754x þ 0:1415
Phytoparasitica (2010) 38:313–325 321
Fig. 5 Relationships be-
tween mean numbers of
Orius spp. and numbers of
Frankliniella occidentalis
on faba bean in plots with a
and without b weedy mar-
gins, in 2005–2006

abundance of Orius spp. (Table 4). Populations of second week of March in all plots. Mean numbers of
Orius spp. adults fluctuated throughout the sampling Orius nymphs peaked on 28 March in both PWWM
period in all plots during 2005 (Fig. 4b). In 2005, the and PNWM in 2005 (2.93±0.33 and 1.22±0.31 per
numbers of adult Orius spp. peaked on 28 March plant, respectively), while in 2006, the peak was on
(3.21±0.21 per plant) in PWWM and on 11 April 30 March (2.50±0.20 per plant) in PWWM and on
(3.22±0.51 per plant) in PNWM. The numbers of 6 April (0.52±0.21 per plant) in PNWM. In 2005,
Orius adults in PWWM were significantly greater the numbers of Orius nymphs in PWWM were
than in PNWM on most sampling dates of January significantly higher than in PNWM on 28 March
and February in 2005 (P<0.001). The numbers of (t38 = 4.917, P= 0.0001) and 4 April (t38 = 3.596,
Orius adults in PNWM were significantly higher P=0.0009) (Fig. 4b). In 2006, numbers of nymphs
than in PWWM only on 4 April and 11 April in 2005 in PWWM were significantly higher on most
(t38 =2.367, P=0.023; t38 =4.681, P=0.0001, respec- sampling dates (Fig. 4b; P<0.001).
tively). In 2006, the numbers of adult Orius spp. Populations of Orius spp. (adults + nymphs) were
peaked on 30 March (3.24 ± 0.51 per plant) in greater than those of thrips on all sampling dates in
PWWM and on 19 January (2.42±0.42 per plant) both years, and numbers of thrips were very low or
in PNWM (Fig. 4b). Mean numbers of Orius adults negligible in the presence of high numbers of Orius
in PWWM were greater on most sampling dates, populations in both plots. Population densities of
after excluding 2 March, 11 March and 30 March, thrips were very low when the numbers of Orius
compared with numbers in PNWM. Mean numbers nymphs or adults attained the highest levels in both
of Orius adults in PNWM were significantly higher plots. Population trends of adults of Orius spp. in
on 9 February and 16 February (t 38 = 4.368, abundance did not follow the population patterns of
P=0.0001; t38 =2.997, P=0.004, respectively) than F. occidentalis in both treatments in both years
in PWWM (Fig. 4b). (Table 5 and Fig. 5a, b). However, there was a
Nymphs of Orius species could not be identified significant relationship between the population fluc-
to the species level in this study. However, most tuation of adult F. occidentalis and the Orius
nymphs probably belonged to O. niger because this nymphal population only in PNWM in 2005 (Table 5
bug was the most prevalent predator on the weeds and Fig. 5b; P<0.05).
and faba bean on most sampling dates in all plots
and in both years (Fig. 4b). The first nymphs of Other predators on faba bean Other predators that
Orius were detected on faba bean in the first or were identified occurred sporadically and their
322 Phytoparasitica (2010) 38:313–325

mean numbers in both plots of faba bean were very cotton (Atakan 2006). While O. niger was found to be
low throughout the sampling periods. Coccinellid the most common anthocorid species in all parts of
and chrysopid predators were detected together Turkey, O. laevigatus was recorded mostly in the
with aphids on the leaves in April. Most adults of southeastern part of Turkey (Önder 1982). O. niger,
the staphylinid predators (mainly Tachyphorus sp.) O. laevigatus, Orius majusculus (Reuter) are the
were observed on the leaves in both plots in commonly found anthocorid species in the Mediter-
February 2006. Their numbers ranged between ranean basin. However, the predominance of any of
0.05 and 0.90 individuals per plant in both plots in these species may depend on location. For instance, in
February. The first females of predatory thrips A. Italy, O. niger predominated in the northwest,
collaris occurred in both plots in the first week of whereas O. laevigatus predominated in the warmest
March. The population sizes of Aeolothrips in both locations of the country (Bosco et al. 2008; Bosco and
plots were relatively large in March when the Tavella 2008; Tommasini 2004).
numbers of thrips were also relatively high. Mean In general, population trends of both thrips or
numbers of Aeolothrips in both plots were similiar, Orius spp. on the weeds were similiar but their
ranging between 0.05 and 0.50 individuals per plant. density levels were different in both years. S.
arvensis bore high numbers of both thrips and Orius
Relationships between numbers of Orius spp. or in both years. The data related to thrips and Orius
Frankliniella occidentalis on weed species and faba seasonal abundance on only S. arvensis allowed us
bean Mean numbers of Orius on S. arvensis were to establish statistical relationships in both years
significantly negatively associated with the numbers (Table 3 and Fig. 2d). Previous studies reported that
on faba bean (2005: R2 = 0.42, F =4.403, d.f.=2, weeds served as alternative sources of prey, and on
14; P=0.041, Y=–4.4616x2 +5.79.34x+ 0.6607 and which Orius spp. and thrips populations interacted
2006: R2 = 0.42, F = 4.943, d.f. = 2, 15, P= 0.025; very well, in Spain (Lacasa et al. 1995) and in Japan
Y= –7.3578x2–6.8758x + 3.224). There were also (Kakimoto et al. 2006). In the present study, the
significant negative relationships between the presence of Orius spp. on other major weed species,
numbers of Orius spp. on L. amplexicaule and the C. arvensis and L. amplexicaule, which host no or
numbers on faba bean in 2005 (R2 =0.64, F =10.913, extremely low numbers of thrips, suggests that such
d.f. = 2, 14 P = 0.002; Y = –0.0073x 2 + 0.1173x– weeds may play some other role. For example, they
0.1025) and in 2006 (R2 =0.51, F =6.802, d.f.=2, may provide nectar and pollen or shelter sites in
15, P= 0.010; Y= –5.415x 2 + 7.01918x + 0.9879). supporting Orius spp. regardless of the presence of
These significant and negative relationships mean F. occidentalis.
that the numbers of Orius spp. found on these two Orius species were more abundant on flowering
weed species were decreasing while the numbers on weeds in the winter—early spring period (Fig. 1).
faba bean were increasing during March–April. After mid-March the numbers of Orius species on
No relationship appeared among the mean numbers these weeds were very low. These findings are
of F. occidentalis on four weed species and the similar to those of previous work done at the same
numbers on faba bean in both years (P>0.05). location (Atakan and Uygur 2004). The first Orius
nymphs were found only in the flowers of S.
arvensis in late April, whereas Orius nymphs were
Discussion present on faba bean in both plots in early March.
This may indicate that Orius spp. may prefer faba
The results show that Orius niger was the main Orius bean plants as a site for egg-laying; therefore, they
species on both faba bean and weeds. Here, O. niger may move from wild plants to faba bean in the early
appeared to be the more active predator in the hard spring despite the greater availability of flowers and
winter months in the region. This may be a result of the presence of reasonable numbers of thrips prey
both year round availability of its thrips prey (Atakan on most weed species (Atakan and Uygur 2005).
and Uygur 2005) and supporting weedy plants and The relationship between abundance of Orius spp.
arable crops in the region, e.g. various vegetables and on the flowering weeds and faba bean that yielded a
fruits (Atakan 2008a, b) and field crops, including significant negative correlation, may be evidence of
Phytoparasitica (2010) 38:313–325 323

movements of Orius from the weedy plants to the sporadically in both years. Colonization of the
faba bean. Many polyphagous predators often move flowers by greater numbers of Orius spp. compared
between arable crops and native habitats, thus to colonization of the leaves may be evidence for
exhibiting cyclic colonization patterns (Bommarco this (Fig. 3). Faba bean, rather than other arable
and Ekbom 2000; Murdoch et al. 1985; Thomas et crops, may be a good host plant in the winter–spring
al. 1991). Such movements from native habitats to period for growth and reproduction of Orius spp.
arable crops include redistribution to early season because no or few Orius spp. (mostly O. niger) were
crop habitats where pests are beginning to be detected on the flowers of various winter vegetables
established, enabling generalist predators to sup- (e.g. broccoli, garden cress, lectuce, red and white
press agricultural pests (Ekbom et al. 1992; Ives and cabbage, radish and spinach) grown in the same area
Settle 1997; Murdoch et al. 1985). (Atakan 2008a). Faba bean also had a rich fauna of
Despite the large populations of Orius spp. in predatory insects (Table 1). Similarly, Nuessly et al.
PWWM, the numbers of F. occidentalis were (2004) found that numerous beneficial insect
relatively higher there than in PNWM in both years species, including Orius, visited faba bean plants
(Fig. 4). This may be due to the flowering of some growing in southern Florida (USA).
weed species bearing F. occidentalis. The numbers In conclusion, controlling weeds can create a
of thrips on faba bean were low, especially in problem in many cases because destruction of
PNWM, where the populations of Orius spp. were weeds surrounding agricultural crops could cause
less abundant in both years. In fact, thrips in both rapid dispersal of pestiferous thrips such as F.
plots of faba bean were less abundant throughout occidentalis to crops and disturbance of the natural
the growing season. This may be due to the enemies of thrips on the weeds. Proper management
unsuitability of this crop as a host for thrips growth of mowing, including timing, is recommended
and reproduction, rather than to predation by Orius during the entire season in order to protect and
species or the other sampled and identified preda- encourage the development of insect predators
tors. Individuals of Orius spp., especially nymphs, (Burgio et al. 2006). With respect to the results of
were more abundant on faba bean grown in the the present study, removing flowering weedy strips
PWWM. This may be due to the presence of bearing high numbers of predators (mainly Orius
flowering weed species, some of which host species) by different control methods before early
considerable numbers of Orius spp. and thrips prey April in the region could be destructive to beneficial
(Fig. 1). Several studies have shown that vegetative insects, and management procedures of field borders
buffers that provide ecological benefits such as should take into account the phenology of the
nectar and pollen can improve the reproductive beneficials (Hodek and Honek 1996; Honek 1982).
success of natural enemies and that this may lead to On the other hand, control measures should be taken
lower abundance of pest arthropods in the crop for the weeds which host only a few predators but
plants (Coll 2009; Gurr et al. 2005; Heimpel and high numbers of thrips (e.g. O. aegyptiacum).
Jervis 2005). Control of such weeds should be done at an
Mean numbers of both Orius spp. (adults + appropriate phenological stage, that is, before they
nymphs) were greater than the numbers of F. are colonized by thrips (e.g. before flowering),
occidentalis on faba bean in both plots throughout because their destruction after bearing high numbers
the sampling periods in both treatments (Fig. 4). of thrips may lead to rapid and serious infestation of
Orius populations were not related to thrips pop- crop plants.
ulations in both faba bean plots, even where there In this study, faba bean appared to be the more
was a weak relationship between populations of attractive plant species, hosting considerable numbers
Orius nymphs and thrips in PNWM in 2005 of Orius spp. in winter. Cultivation of faba bean in
(Table 5). This may indicate that Orius spp. agricultural locations, especially in monoculture areas
benefited more from the faba bean plants for plant in the Mediterranean region or other countries with
meal, shelter, mating and ovipositon sites than from similar ecological conditions, could be useful for
thrips prey or other insect prey species such as conservation and augmentation of beneficial insects,
aphids, whose numbers were low and were detected including Orius spp.
324 Phytoparasitica (2010) 38:313–325

Acknowledgments I would like to thank Dr. David Ben-Yakir houses in Northwest Italy. Biological Control, 44, 331–
(Department of Entomology, Agricultural Research Organization, 340.
The Volcani Center, Bet Dagan, Israel) for reviewing an earlier Bulut, E., & Göçmen, H. (2000). Pests and their natural
draft of the manuscript and Murat Ölçülü (Institute of Basic and enemies on greenhouse vegetables in Antalya. IOBC/
Applied Sciences, Çukurova University, Adana, Turkey) for field WPRS Bulletin, 23, 33–37.
assistance. I would like also to thank three anonymous reviewers Burgio, G., Ferrari, R., Pozzati, M., & Boriani, L. (2006). The role
for their valuable comments and suggestions which improved the of ecological compensation areas on predator populations: an
manuscript. analysis on biodiversity and phenology of Coccinellidae
(Coleoptera) on non-crop plants within hedgerows in
Northern Italy. Bulletin of Insectology, 57, 1–10.
Coll, M. (2009). Conservation biological control and the
References management of biological control services: are they the
same? Phytoparasitica, 37, 205–208.
Anon. (2001). 8th Plan of the improvement of Turkey’s Ekbom, B. S., Wiktelius, S., & Chiverton, P. A. (1992). Can
economy for five years: Plant production. Report of Sub- polyphagous predators control the bird cherry-oat aphid
Commission of Cereals and Legumes, DPT: 2644-ÖİK: (Rhopalosiphum padi) in spring cereals? Entomologia
652. Ankara, Turkey (in Turkish). Experimentalis et Applicata, 65, 215–223.
Atakan, E. (2006). Associations between Frankliniella spp. and Frank, T., & Reichhart, B. (2004). Staphylinidae and Carabidae
Orius niger populations in cotton. Phytoparasitica, 34, overwintering in wheat and sown wildflower areas of different
221–234. age. Bulletin of Entomological Research, 94, 209–217.
Atakan, E. (2008a). Thrips (Thysanoptera) species occurring on Gurr, G. M., Wratten, S. D., Tylianakis, J., Kean, J., & Keller,
winter vegetables crops in Çukurova region of Turkey. M. (2005). Providing plant foods for natural enemies in
Acta Phytopathologica Entomologica Hungarica, 43, farming systems: Balancing practicalities and theory. In F.
227–234. L. Wäckers, P. C. J. van Rijn, & J. Bruin (Eds.), Plant-
Atakan, E. (2008b). Thrips (Thysanoptera) species occur- provided food for carnivorous insects: A protective
ring on fruit orchards in Çukurova region of Turkey. mutualism and its applications (pp. 341–347). New York,
Acta Phytopathologica Entomologica Hungarica, 43, NY: Cambridge University Press.
235–242. Heimpel, G. E., & Jervis, M. A. (2005). Does nectar improve
Atakan, E., & Özgür, A. F. (2004). Within-plant distributions of biological control by parasitoids? In F. L. Wäckers, P. C. J. van
predators Chrysoperla carnea (Stephens) (Neuroptera: Rijn, & J. Bruin (Eds.), Plant-provided food for carnivorous
Chrysopidae), Deraeocoris pallens Reut. (Heteroptera: insects: A protective mutualism and its applications (pp. 267–
Miridae) and Orius niger (Wolff) (Heteroptera: Anthocor- 304). New York, NY: Cambridge University Press.
idae) on cotton. Türkiye Entomoloji Dergisi, 24, 267–277 Hodek, I., & Honek, A. (1996). Ecology of Coccinellidae.
(in Turkish, with English summary). Dordrecht, the Netherlands: Kluwer Academic.
Atakan, E., & Uygur, S. (2004). Seasonal abundance of some thrips Honek, A. (1982). Aphidophagous Coccinellidae (Coleoptera)
species and their predators on weeds. Türkiye Entomoloji and Chrysopidae (Neuroptera) on three weeds: factors
Dergisi, 28, 123–132 (in Turkish, with English summary). determining the composition of populations. Acta Ento-
Atakan, E., & Uygur, S. (2005). Winter and spring mologica Bohemoslovaca, 78, 303–310.
abundance of Frankliniella spp. and Thrips tabaci Ives, A. R., & Settle, W. H. (1997). Metapopulation dynamics
Lindeman (Thysan., Thripidae) on weed host plants in and pest control in agricultural systems. American Natu-
Turkey. Journal of Applied Entomology, 129, 17–26. ralist, 149, 220–246.
Atakan, E., & Gençer, O. (2008). Influence of planting date on Kakimoto, K., Inoue, H., Yamaguchi, T., Ohno, K., & Takagi,
the relationship between populations of Frankliniella M. (2006). Population trends of Orius sauteri (Poppius)
flower thrips and predatory bug Orius niger in cotton. (Heteroptera: Anthocoridae) on weeds in spring. Japanese
Journal of Pest Science, 81, 123–133. Journal of Applied Entomology and Zoology, 50, 68–71.
Atakan, E., Özgür, A. F., & Kersting, U. (1998). Frankliniella (in Japanese, with English summary).
occidentalis (Thysanoptera: Thripidae) on cotton in Lacasa, A., Contreras, J., Sanchez, J. A., Lorca, M., & Garcia,
Çukurova Region. In: Proceedings of the Sixth Interna- F. (1995). Ecology and natural enemies of Frankliniella
tional Symposium on Thysanoptera (Antalya, Turkey), occidentalis (Pergande, 1895) in the Southeast Spain.
pp. 7–12. Folia Entomologica Hungarica, 57, 67–74.
Bommarco, R., & Ekbom, B. (2000). Landscape management and Landis, D., & Wratten, S. (2002). Conservation of biological
resident generalist predators in annual crop systems. In B. controls. In D. Pimentel (Ed.), Encyclopedia of pest
Ekbom, M. Irwin, & Y. Robert (Eds.), Interchanges of management (pp. 138–140). New York, NY: Marcel
insects between agricultural and surrounding habitats (pp. Dekker.
169–182). Dordrecht, the Netherlands: Kluwer Academic. Landis, D., Wratten, S., & Gurr, G. (2000). Habitat manipu-
Bosco, L., & Tavella, L. (2008). Collection of Orius species in lation to conserve natural enemies in arthropod pests in
horticultural areas of northwestern Italy. Bulletin of agriculture. Annual Review of Entomology, 45, 173–199.
Insectology, 61, 209–210. Marshall, E. J. P., & Moonen, A. C. (2002). Field margins in
Bosco, L., Giacometto, E., & Tavella, L. (2008). Colonization northern Europe: their functions and interactions with
and predation of thrips (Thysanoptera: Thripidae) by Orius agriculture. Agriculture, Ecosystem and Environment, 89,
spp. (Heteroptera: Anthocoridae) in sweet pepper green- 5–21.
Phytoparasitica (2010) 38:313–325 325

Murdoch, W. W., Chesson, J., & Chesson, P. L. (1985). SPSS. (2006). SPSS base 15.0 user’s guide. Chicago, IL, USA:
Biological control in theory and practice. American Prentice Hall.
Naturalist, 125, 344–366. Tavella, L., Bosco, L., & Faure, E. (2003). Distribution and
Nuessly, G. S., Hentz, M. G., Beiriger, R., & Scully, B. T. (2004). population dynamics of Orius spp. in sweet pepper green-
Insects associated with faba bean, Vicia faba (Fabales: houses in north-west Italy. IOBC/WPRS Bulletin, 26, 153–158.
Fabaceae), in southern Florida. Florida Entomologist, 87, Tavella, L., Tedeschi, R., Arzone, A., & Alma, A. (2000).
204–211. Predatory activity of two Orius species on the western
Önder, F. (1982). Contribution to the study of Turkish flower thrips in protected pepper crops (Ligurian Riviera,
Anthocoridae (Heteroptera). Bornova, İzmir, Turkey: Ege Italy). IOBC/WPRS Bulletin, 23, 231–240.
Üniversitesi, Ziraat Fakültesi Ofset Basımevi (in Turkish, Thomas, M. B., Wratten, S. D., & Sotherton, N. W. (1991).
with English summary). Creation of ‘island’ habitats in farmland to manipulate
Riudavets, J. (1995). Predators of Frankliniella occidentalis populations of beneficial arthropods: predator densities
(Perg.) and Thrips tabaci Lind.: a review. In: A. J. M. and emigration. Journal of Applied Ecology, 28, 906–917.
Loomans, J. C. Van Lenteren, M. G. Tommasini, S. Maini Tommasini, M. G. (2004). Collection of Orius species in Italy.
& J. Riudavets (Eds.), Biological control of thrips pests Bulletin of Insectology, 57, 65–72.
(pp. 49–87). Wageningen Agricultural University Papers, van de Veire, M., & Degheele, D. (1992). Biological control of the
95.I, Wageningen, the Netherlands. western flower thrips Frankliniella occidentalis (Pergande)
Shipp, J. L., & Zariffa, N. (1991). Spatial patterns of and sampling (Thysanoptera: Thripidae), in glasshouse sweet peppers
methods for western flower thrips (Thysanoptera: Thripidae) with Orius spp. (Hemiptera: Anthocoridae): a comparative
on greenhouse sweet pepper. Canadian Entomologist, 123, study between O. niger (Wolff) and O. insidiosus (Say).
989–1000. Biocontrol Science and Technology, 2, 281–283.
Shipp, J. L., Zariffa, N., & Ferguson, G. (1992). Spatial patterns Yaşarakıncı, N., & Hıncal, P. (2000). The studies on pests, their
of and samplings methods for Orius spp. (Hemiptera: natural enemies and population developments on protected
Anthocoridae) on greenhouse sweet pepper. Canadian pepper in İzmir province. Bitki Koruma Bülteni, 40, 135–
Entomologist, 124, 887–894. 152 (in Turkish, with English abstract).