BioControl (2009) 54:237–246
DOI 10.1007/s10526-008-9164-y
Predation by Nesidiocoris tenuis on Bemisia tabaci
and injury to tomato
Javier Calvo Æ Karel Bolckmans Æ Philip A. Stansly Æ
Alberto Urbaneja
Received: 16 January 2007 / Accepted: 14 April 2008 / Published online: 10 May 2008
Ó International Organization for Biological Control (IOBC) 2008
Abstract Tomato is the most important vegetable
crop in Spain. The mirid bug Nesidiocoris tenuis
(Reuter) commonly appears in large numbers in
protected and open-air tomato crops where little or no
broad-spectrum insecticides are used. Nesidiocoris
tenuis is known to be a predator of whiteflies, thrips
and several other pest species. However, it is also
Hanlding editor: Eric Lucas.
This research is part of an internal R&D project conducted at
Koppert Biological Systems S.L. in Spain. The main goal was
to improve control of Bemisia tabaci in protected crops of
southeastern Spain by bringing on a new biological control
agent.
considered a pest because it can feed on tomato
plants, causing necrotic rings on stems and flowers
and punctures in fruits. Our objectives were to
evaluate predation by N. tenuis on sweetpotato
whitefly Bemisia tabaci Gennadius under greenhouse
conditions and establish its relationship to N. tenuis
feeding on tomato. Two different release rates of
N. tenuis were compared with an untreated control
(0, 1 and 4 N. tenuis plant-1) in cages of 8 m2.
Significant reductions of greater than 90% of the
whitefly population and correspondingly high numbers of N. tenuis were observed with both release
rates. Regression analysis showed that necrotic rings
on foliage caused by N. tenuis were best explained by
the ratio of B. tabaci nymphs:N. tenuis as predicted
by the equation y = 15.086x - 0.6359.
J. Calvo A. Urbaneja
R & D Department, Koppert Biological Systems S.L.,
Finca Labradorcico del Medio, s/n. Apartado de Correos
286, 30880 Aguilas, Spain
Keywords Miridae Whitefly Biological control
Zoophytophagy
K. Bolckmans
R & D Department, Koppert B.V., Veilingweg 17,
2651 BE Berkel en Rodenrijs, The Netherlands
Introduction
P. A. Stansly
University of Florida-IFAS, 2686 State Road 29N,
34142 Immokalee, FL, USA
A. Urbaneja (&)
Unidad de Entomologı́a, Centro de Protección Vegetal y
Biotecnologı́a, Instituto Valenciano de Investigaciones
Agrarias (IVIA), Carretera de Moncada – Náquera Km.
4,5, 46 113 Moncada, Valencia, Spain
e-mail: aurbaneja@ivia.es
Tomato (Lycopersicon esculentum Mill.) is the most
important vegetable crop in Spain, with a production
area of close to 60,000 ha in 2002 and a total
production of 4 million metric tonnes. Almost 28%
of this volume is produced in the Comunidad
Autónoma de Murcia and in the adjacent province
of Almerı́a (INE 2002). In both regions, tomatoes are
grown primarily in plastic covered greenhouses. In
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recent years, the most harmful pest of tomato in these
regions has been the whitefly Bemisia tabaci (Gennadius) (Hem.: Aleyrodidae). This pest causes
damage by sucking the sap, thus weakening the
plant, and by secreting large amounts of honeydew
that favour the appearance of sooty mould. However,
the greatest impact on tomato is due to its role as
vector of tomato yellow leaf curl virus (TYLCV)
(SIFA 2004). Serious economic losses have been
caused in Spain by this geminivirus since its appearance in the 1990s (CARM 1996). Consequently,
permissible population levels of B. tabaci are minimal, such that implementation of biocontrol based
IPM programs is difficult (Stansly et al. 2004).
Nevertheless, interest in biological control continues
to increase in Spain (Castañé 2002; van der Blom
2002), thanks in part to adaptation of TYLCVtolerant varieties, development of pesticide resistance
(Cahill et al. 1996; Elbert and Nauen 2000) and
successful use of natural enemies against this pest
(Stansly et al. 2004, 2005a, b; Urbaneja et al. 2002;
Calvo and Belda 2006).
The parasitoid Eretmocerus mundus Mercet (Hym.:
Aphelinidae) and the predator Nesidiocoris tenuis
Reuter (Hem.: Miridae) (Sánchez et al. 2003a, b; van
der Blom 2002) are endemic natural enemies of
B. tabaci that commonly appear in tomato crops in
Southern Spain. The biology, behaviour and effectiveness of E. mundus is well documented (Stansly
et al. 2004, 2005a, b; Urbaneja and Stansly 2004), and
this parasitoid is mass-reared and released to control
B. tabaci in greenhouse vegetable crops in this region
(Urbaneja et al. 2003a). In contrast, only limited
research has been reported on the potential of N. tenuis
for augmentative biological control of B. tabaci.
Often cited with regard to its polyphagous habit
(Goula 1985; Urbaneja et al. 2005) or zoophytophagous behaviour (Dolling 1991), N. tenuis has been
observed to contribute to the control of whiteflies,
thrips, leafminers, spidermites, and Lepidoptera species in greenhouses (Arzone et al. 1990; Calvo and
Urbaneja 2003; Carnero et al. 2000; Marcos and
Rejesus 1992; Solsoloy et al. 1994; Torreno 1994;
Trottin-Caudal and Millot 1997; Vacante and
Benuzzi 2002; Vacante and Grazia 1994). However,
N. tenuis has also been classified as a pest of tomato
(Malézieux et al. 1995) due to feeding damage such
as necrotic rings in both leaf and flower petioles, and
whitish halos on fruit (Arnó et al. 2006; El-Dessouki
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J. Calvo et al.
et al. 1976; Kajita 1978; Malausa 1989; Malausa and
Henao 1988; Vacante and Grazia 1994). The necrotic
rings on the flower petiole can result in under certain
conditions on floral abortion (Calvo and Urbaneja
2004; Sánchez et al. 2006). Intensity of injury to
tomato has been observed to decrease with increased
availability of prey (Arnó et al. 2006).
The aim of the present work is to evaluate the
efficacy of N. tenuis in controlling B. tabaci and to
characterize damage to tomato. This information could
then form a basis for management of N. tenuis that will
optimize benefits derived from predation on B. tabaci
while minimizing damage to the tomato crop.
Materials and methods
Test facilities
The experiment was conducted in a 40 9 10 m air
inflated double layered polyethylene covered Quonset
style greenhouse equipped with pad-and-fan cooling
and diesel-fired heating, located at the Koppert
Biological Systems S.A. facilities in Águilas, Murcia,
Spain. The plastic tunnel was accessed through a
double door and was divided into 36 experimental
cages constructed of ‘‘anti-thrips’’ polyethylene
screening with 220 9 331 lm interstices supported
by heavy guy wires connected to the greenhouse
superstructure. Each experimental cage was 4 9 2 9
3.5 m (l 9 w 9 h) and covered on the floor with a
2 mm-thick woven white polyethylene ground cloth.
Each cage was accessed by an independent door
secured with a zipper. Twelve cages were used for the
present study, six on either side of the centre aisle.
Dataloggers (model HOBO H8 RH/Temp, Onset
Computer Company, Bourne, MA, the USA) were
placed in four different cages to record temperature
and relative-humidity.
Environmental conditions
The average temperature during the experiment ranged
between 26°C, on 3 October 2002, to 20°C, on 16
January 2003, with an absolute minimum and maximum
of 14.5 and 38.3°C respectively during the test period
(Fig. 1A). Average relative humidity ranged from 84%,
on 31 October 2002 to 65% on 16 January 2003 with
absolute values of 100 and 22% respectively (Fig. 1B).
Predation by Nesidiocoris tenuis on Bemisia tabaci
Fig. 1 Temperature (A)
and relative humidity (B) in
the greenhouse during the
experiment
A
239
40
Temp (°C)
30
20
10
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
12
13
14
15
Trial Week
Mean
B
Max
Min
100
RH (%)
80
60
40
20
0
1
2
3
4
5
6
7
8
9
10
11
Trial Week
Mean
Plant and pest management
Tomato seeds variety ‘Boludo’, tolerant to TYLCV
and TSWV (Seminis Vegetable Seeds Europe
Enkhuizen, The Netherlands), were sown on 1
September 2002. Seeds were deposited in 5.4 cm2
cells in expanded polystyrene trays of 11 9 19 cm
filled with peat. On 27 September, seedlings were
transplanted into polyethylene 6.3 l flowerpots filled
with cocopeat (coir) growing medium and placed
inside the experimental greenhouse in two rows of 5
plants per cage or 1.25 plants m-2. Plant densities in
commercial tomato crops in southern Spain vary from
1.25 to 3 plants m-2. However therefore, the release
rates for all the insects were calculated in individuals
per plant, so results could easily be transformed to
Max
Min
other plant, densities. Crop cultivation techniques
typical of tomato greenhouse-cultivation in Spain
were followed: a trellis of two wire-guides for each
plant to which the main stem was trained using black
polyethylene string, weekly pruning of secondary
shoots, application of a standard nutrient solution for
tomato by means of an automated-irrigation system
with an irrigation frequency adjusted to accumulated
radiation (800 W m-2), and an irrigation time of
8.5 min.
Whiteflies and predators
Bemisia tabaci adults came from an experimental
colony located in Águilas and identified as B. tabaci
biotype ‘‘Q’’ based on DNA analysis (J.L. Cenis,
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240
IMIDA La Alberca. Murcia, España, Personal
Communication). Less than 4-day-old N. tenuis
adults were obtained from an experimental colony
maintained at 25°C and 75% RH, maintained on
tobacco plants and fed with Ephestia kuehniella
Zeller (Lepidoptera: Pyralidae) eggs. The sex-ratio of
this colony was 0.5 female/total. The colony originated from specimens collected during summer 2002
in tomato greenhouses in the province of Murcia.
Experimental design
Three release rates of N. tenuis were compared in the 12
cages using a randomized complete block design with
three treatments replicated four times. The three treatments were a one time release of 1 or 4 N. tenuis plant-1
plus a control receiving no release. One N. tenuis per
plant is the recommended release rate (Calvo and
Urbaneja 2004), so the aim of the higher rate was to test
effects of an excessive number of predators.
Each cage was infested with 55 adult B. tabaci on
October 3rd, 2002, one week before the first evaluation. The infestation of 55 adult whiteflies per cage was
chosen to simulate a strong and early whitefly attack.
Two weeks later (just after the second evaluation),
N. tenuis was released inside the cages. Special care
was always taken to enter the control cages first, then
the cages with the lower release rate and finally the
ones with the higher release rate, to reduce risk of
accidental contamination among treatments.
Evaluations
Six randomly chosen plants per cage were sampled
weekly for 15 weeks, beginning 10 October, 2002.
First, the number of N. tenuis nymphs and adults and
the number of necrotic rings were counted from 7
apical leaves of the 6 plants (Castañé and Carnero
2002). Then a leaf belonging to the middle strata was
selected at random from each plant and cautiously
turned to count the number of B. tabaci adults. Finally
nymphs (N1–N4) were counted on this same leaf using
a 109 hand lens (Stansly et al. 2005a).
Statistical analysis
J. Calvo et al.
adults, and necrotic rings during the course of the trial
were calculated (Stansly et al. 2005a, b). The resulting
estimates of insect and damage accumulated 9 days
(= area under the weekly incidence curve) was then
subjected to a one-way analysis of variance joined with
a Tukey’s test for mean separation (P \ 0.05).
The number of necrotic rings per leaf was fitted to
the number of B. tabaci nymphs per leaf, the number
of N. tenuis individuals (adults and nymphs) per leaf
and the ratio of B. tabaci nymphs per leaf:number of
N. tenuis adults + nymphs per leaf using linear,
power, exponential, inverse and logarithmic regression analyses. All statistical analyses were carried out
with SPSS v12.0 (SPSS 2004).
Results
Bemisia tabaci populations
The greatest number of whitefly adults per leaf
(93.1 ± 24.7) were observed in the control treatment
the last week of the test (Fig. 2A). This compared to a
maximum of 17.4 ± 5.0 adults per leaf observed in
week 12 in cages receiving 1 N. tenuis plant-1,
representing a relative reduction of 81%. The
maximum number of B. tabaci adults in cages
receiving 4 N. tenuis plant-1, observed in week 9,
was only 3.3 ± 0.6, representing a 96% reduction
compared to the maximum in the control treatment.
Accumulated B. tabaci adult per day reflected these
relationships although differences between the 1 and
4 N. tenuis plant-1 release rates were not significantly different (F = 43.16; d.f. = 2, 53; P \ 0.001)
(Table 1).
Similar trends were observed in numbers of
B. tabaci nymphs, with maxima at the end of the
experiment reaching 744.5 ± 116.1, 297.0 ± 89.2 and
92.9 ± 12.6 for the control treatment, and the 1 and 4
N. tenuis plant-1 treatments respectively representing
reductions of 62% and 87% respectively (Fig. 2B).
Again, the number of accumulated nymph per day was
significantly different between the control and the two
release rates with no differences between the latter
(F = 28.94; d.f. = 2, 53; P \ 0.001) (Table 1).
Nesidiocoris tenuis populations
Values are expressed as mean ± standard error of the
mean. The accumulated number of whitefly nymphs
plus pupae, whitefly adults, N. tenuis nymphs and
123
Most adult N. tenuis were initially observed in cages
receiving the high release rate. However, their numbers
Predation by Nesidiocoris tenuis on Bemisia tabaci
Fig. 2 Average whitefly
adults (A) and nymphs (B)
per leaf in each week (±SE)
for treatments receiving 0, 1
and 4 N. tenuis plant-1.
Whiteflies were released in
week 0 and N. tenuis was
released just after the
second evaluation in week 2
241
125
B. tabaci Adults / leaf
A
100
75
50
25
0
1
2
3
4
5
6
7
8
9
10 11 12 13 14 15
Trial Week
0 Nt/pl
1 Nt/pl
4 Nt/pl
900
B. tabaci Nymphs / leaf
B
750
600
450
300
150
0
1
2
3
4
5
6
7
8
9
10 11 12 13 14 15
Trial Week
0 Nt/pl
Table 1 Average nymphs
and adults of B. tabaci
(±SE), nymphs and adults
of N. tenuis (±SE) and
necrotic rings (±SE)
accumulated per day for
treatments receiving 0, 1
and 4 N. tenuis per plant
1 Nt/pl
4 Nt/pl
Release rate (Ind. plant-1)
0 N. tenuis plant-1
1 N. tenuis plant-1
4 N. tenuis plant-1
B. tabaci
Adults
Nymphs
2360.4 ± 251.4 a
741.4 ± 164.1 b
161.0 ± 13.0 b
32795.2 ± 4573.5 a
10732.6 ± 1821.0 b
3339.0 ± 338.0 b
N. tenuis
Means in the same row
followed by the same letter
are not significant different
(Tukey, P \ 0.05)
Adults
5.0 ± 1.03 b
25.2 ± 1.9 a
31.0 ± 1.8 a
Nymphs
7.5 ± 1.4 c
31.4 ± 2.0 b
57.2 ± 2.4 a
12.6 ± 2.1 c
56.7 ± 3.1 b
88.2 ± 3.1 a
Necrotic rings
declined after week 11 compared to low release cages
(Fig. 3A) although differences in number of accumulated adults per day did not differ significantly between
the two release rates (F = 70.52; d.f. = 2, 251;
P \ 0.001) (Table 1). Peak numbers of mirid nymphs
were considerably greater in response to the
4 N. tenuis plant-1 release rate (Fig. 3B). Furthermore,
more cumulative nymphs per day were observed with
4 N. tenuis plant-1 compared to 1 N. tenius plant-1
(Table 1) (F = 157.61; d.f. = 2, 251; P \ 0.001). As
many as 0.2 ± 0.1 adults and 0.4 ± 0.1 nymphs per
terminal were seen in cages where no N. tenuis were
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1,5
N. tenuis Adults / leaf
Fig. 3 Average
Nesidiocoris tenuis adults
(A) and nymphs (B) per leaf
in each week (±SE) for
treatments receiving 0, 1
and 4 N. tenuis plant-1.
Whiteflies were released in
week 0 and N. tenuis was
released just after the
second evaluation in week 2
J. Calvo et al.
A
1,0
0,5
0,0
1
2
3
4
5
6
7
8
9
10 11 12 13 14 15
Trial Week
0 Nt/pl
1 Nt/pl
4 Nt/pl
2,0
N. tenuis Nymphs / leaf
B
1,5
1,0
0,5
0,0
1
2
3
4
5
6
0 Nt/pl
released due to unintentional contamination, although
fewer N. tenuis day-1 were accumulated in these cages
compared to release cages.
Plant injury
The first necrotic rings were observed in week 6 with
the greatest incidence always in cages receiving
4 N. tenuis plant-1 (Fig. 4). Maxima observed per
leaf were 3.9 ± 0.2, 1.6 ± 0.1and 0.5 ± 0.1 for
the high, low and zero release rates respectively.
Differences were significant among all treatments in
the number of accumulated necrotic rings day-1
(Table 1) (F = 181.67; d.f. = 2, 251; P \ 0.001).
Regression analysis showed best fit between
number of necrotic rings and the ratio of B. tabaci
nymphs to N. tenuis adults + nymphs (Table 2).
123
7 8 9 10 11 12 13 14 15
Trial Week
1 Nt/pl
4 Nt/pl
R2 and F values were highest using power regression.
The regression equation was y = 15.086x - 0.6359,
where y was the number of necrotic rings per leaf and
x was the ratio of B. tabaci nymphs to N. tenuis
adults + nymphs (Fig. 5).
Discussion
Nesidiocoris tenuis was highly effective in controlling B. tabaci on tomato under these experimental
conditions, with little difference observed between
the two release rates evaluated. Whitefly reductions
of up 81% and 96% were recorded with only one
release of 1 or 4 N. tenuis plant-1 respectively.
Furthermore, N. tenuis established well in the tomato
crop under the experimental conditions, reaching
Predation by Nesidiocoris tenuis on Bemisia tabaci
Fig. 4 Average necrotic
rings per leaf in each week
(±SE) for treatments
receiving 0, 1 and
4 N. tenuis plant-1.
Whiteflies were released in
week 0 and N. tenuis was
released just after the
second evaluation in week 2
243
Necrotic Rings / Leaf
5
4
3
2
1
0
1
2
3
4
5
6
7
8
9
Trial Week
0 Nt/pl
Table 2 Lineal, power,
exponential, inverse and
logarithmic regression
analysis of the number of
necrotic rings observed with
the number of B. tabaci
nymphs per leaf, with the
number of N. tenuis
individuals (adults and
pupae) per leaf and with the
quotient B. tabaci nymphs
per leaf/individuals of
N. tenuis per leaf
R2 is the r square parameter;
d.f. are the degrees
freedom; F is the Fisher’s
parameter; P is the
significant level and a and b
are the constant and the
dependent parameter of the
curve (±SE)
Curve type
R2
d.f.
F
1 Nt/pl
P
10 11
12 13 14
15
4 Nt/pl
a
b
Necrotic rings depending on the number of nymphs of B. tabaci/N. tenuis
Lineal
0.191
53
12.288
0.001
-0.001 ± 0.000
1.647 ± 0.149
Logarithmic
0.705
53
124.270
\0.001
-0.630 ± 0.057
4.163 ± 0.259
Inverse
0.675
53
107.914
\0.001
26.867 ± 2.586
0.651 ± 0.113
Power
0.745
53
151.842
\0.001
-0.636 ± 0.052
15.086 ± 3.565
Exponential
0.351
53
28.101
\0.001
-0.001 ± 0.000
1.278 ± 0.168
Necrotic rings depending on the number of nymphs of B. tabaci
Lineal
Logarithmic
0.308
0.477
53
53
23.139
47.473
\0.001
\0.001
-0.005 ± 0.001
-0.761 ± 0.110
1.994 ± 0.172
4.675 ± 0.484
Inverse
0.297
53
21.953
\0.001
26.289 ± 5.611
0.846 ± 0.176
Power
0.350
53
27.959
\0.001
-0.640 ± 0.121
14.617 ± 7.750
Exponential
0.257
53
18.021
\0.001
-0.004 ± 0.001
1.587 ± 0.278
1.295 ± 0.165
-0.90 ± 0.218
Necrotic rings depending on the number of N. tenuis
Lineal
0.543
53
61.674
\0.001
Logarithmic
0.418
53
37.278
\0.001
0.849 ± 0.139
1.488 ± 0.115
Inverse
0.187
53
11.926
0.001
-0.164 ± 0.048
1.720 ± 0.160
Power
0.649
53
96.348
\0.001
1.040 ± 0.106
1.028 ± 0.090
Exponential
0.584
53
73.129
\0.001
1.320 ± 0.154
0.203 ± 0.041
high population levels with both release rates
assayed. These results are consistent with studies
showing that tomato plants are good host plants for
N. tenuis (Carnero et al. 2000; El-Dessouki et al.
1976; Goula 1985; Goula and Alomar 1994; Sánchez
et al. 2003a, b; Urbaneja et al. 2005).
We found in an earlier study that no N. tenuis
developed successfully on tomato plants without prey
(Urbaneja et al. 2003a, b, 2005). Dicyphus hesperus
Knight (Het.: Miridae) was also unable to complete
its development when fed exclusively on tomato
leaves (Gillespie and McGregor 2000). Conversely,
Macrolophus pygmaeus Rambur and Dicyphus
tamaninii Wagner (Het.: Miridae), were able to reach
adulthood feeding on tomato leaves and fruits,
respectively (Perdikis and Lykouressis 2000; Lucas
and Alomar 2001).
In the present experiment, the number of accumulated N. tenuis adults per day was not significantly
different between both release rates, although more
nymphs were observed with the high rate. Prey
availability per predator must have been lower at the
higher release rate, since the number of whitefly
nymphs was not significantly different. This would
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244
5
4
Necrotic rings / leaf
Fig. 5 Observed and
empirical distribution based
on a power model for the
number of necrotic rings
caused by N. tenuis on
depend of the prey
availability
J. Calvo et al.
3
2
Empirical: y = 15,086x -0,6359
1
0
0
500
1000
1500
2000
2500
3000
3500
Nymphs B. tabaci / N. tenuis (Adults + Nymphs)
OBSERVED
result in reduced survivorship of mirid nymphs, either
directly through poorer nutrition or indirectly through
competitive interactions such as cannibalism,
although our observations did not allow us to
distinguish between these possibilities. However,
cannibalism in zoophytophagous species is not common under field conditions (Castañé et al. 2002;
Lucas and Alomar 2002).
The first necrotic rings surrounding the pedicel
were detected on tomato leaves by week 6 of the test.
The cumulative number of necrotic rings per leaf was
significantly greater in the high release rate treatment.
Shipp and Wang (2006) in a similar trial also
obtained a strong correlation between tomato damage
and prey availability when they tested different
release rates of D. hesperus Knight (Het.: Miridae)
against the western flower thrips, Frankliniella occidentalis (Pergande) (Thy.: Thripidae).
Gillespie and McGregor (2000) proposed three
simple models for feeding behaviour in omnivorous
Heteroptera: (1) the amount of plant feeding
decreases with increased prey feeding, (2) the amount
of plant feeding increases with increased prey feeding
and (3) the amount of plant feeding is independent of
the amount of prey feeding. Nesidiocoris tenuis
appears to follow the first model because damage to
tomato decreased in response to greater availability
of B. tabaci. These results agreed with those of Arnó
et al. (2006) based on observations made under
laboratory conditions. Hence, it seems that N. tenuis
feeds on tomato plants when there is a lack of prey.
This behaviour differs from D. hesperus for which
damage to tomato increased in response to increased
prey availability (model 2) due to the need to obtain
123
Empirical
water from the plant for external digestion of prey
(Gillespie and McGregor 2000). In contrast to both
these mirids, D. tamaninii seems to damage tomato
fruits independently of prey availability (model 3)
(Lucas and Alomar 2002).
The ratio of B. tabaci nymphs and N. tenuis
individuals was the best predictor of incidence of
damage by N. tenuis. Therefore, to avoid undue
injury to a tomato crop by N. tenuis, special attention
should be paid to this ratio. Shipp and Wang (2006)
observed that damage caused by D. hesperus
increased exponentially when a ratio of 1:10 (predator:prey) was exceeded. Alomar et al. (1991) came
to a similar conclusion for D. tamaninii preying on
greenhouse whitefly Trialeurodes vaporariorum
(Westwood) (Hem: Aleyrodidae) in tomato greenhouses. They recommended close monitoring of the
relative abundance of predator and prey to avoid
damage to tomato fruit (Lucas and Alomar 2002).
Alomar and Albajes (1996) provided a decision chart
indicating that insecticidal control against D. tamanini was required when it exceeded 4 per plant and
adult whitefly were less than 20 per plant. We
focused on whitefly nymphs rather than adults in our
study, but could not provide a decision chart for
N. tenuis because no information is available to relate
injury from this species to tomato yield or fruit
quality. When such information becomes available,
threshold ratios of B. tabaci nymphs to N. tenuis
could be established.
This predator, like most mirid predators, displays a
high degree of polyphagous behaviour and is able to
feed on several different pest species. Urbaneja et al.
(2003b, 2005) showed that on tomato leaves and
Predation by Nesidiocoris tenuis on Bemisia tabaci
under laboratory conditions at 25°C, N. tenuis was
able to complete its life cycle in 12.8, 13.21, 20.61
and 23.44 days feeding on the eggs of E. kuehniella,
B. tabaci nymphs, larvae of F. occidentalis and
immatures and adults of Tetranychus urticae Koch
(Acari: Tetranychidae), respectively. Thus, the presence of these other pests could potentially increase
the tolerance level for N. tenuis per plant without
significant increase in plant damage.
Mirid predators respond differently to different
plant types as well. For instance, D. tamaninii
damages tomato but not cucumber (Gabarra et al.
1995; Castañé et al. 1996). Thus, the balance
between plant injury and biological control is determined by both the quantity and quality of plant and
prey types (Eubanks and Denno 1997; Agrawal et al.
1999). As a consequence, the status of a mirid species
such as N. tenuis as pest or biological control agent
will depend on crop, pest complex, and possibly other
circumstances. Thus, further studies may be necessary to evaluate the utility of N. tenuis as biological
control agent in particular agroecosystems.
Acknowledgments The authors thank Ana Gallego, Gervasio
Tapia and David Beltrán (Koppert B.S.; Spain) for technical
assistance with experiments and maintenance of insect colonies.
This work was partially funded by the MCYT (Ministerio
Ciencia y Tecnologı́a, Spain: Programa PROFIT) through
project number of FIT-010000-2002-18.
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Author Biographies
Javier Calvo is an entomological researcher at Koppert B.S.
charged with evaluating biological control systems for
management of vegetable pests.
Karel Bolckmans heads International R&D and production
activities of Koppert and is based at the Koppert headquarters
in the Netherlands.
Philip A. Stansly conducts research and extension on pest
integrated management for the University of Florida and
became involved in the project during a sabbatical year with
Koppert B.S.
Alberto Urbaneja is biological control specialist at the PVYB
of the Valencian Institute of Agricultural Research (IVIA,
Spain) and previously worked as R&D manager at Koppert
B.S. in Spain.
Karel Bolckmans