ARTICLE IN PRESS

Crop Protection 23 (2004) 701–712

Prospects for biological control of Bemisia tabaci

(Homoptera, Aleyrodidae) in greenhouse tomatoes of southern Spain
P.A. Stanslya,*, P.A. Sa! nchezb, J.M. Rodr!ıguezb, F. Cañizaresc, A. Nietoc,
!
M.J. Lopez Leyvad, M. Fajardoe, V. Sua! rezf, A. Urbanejab,1
a
University of Florida, Southwest Florida Research and Education Center, 2686 State Road 29 North, Immokalee, FL 34142-9515, USA
b !
Koppert Biological Systems S.L., Finca Labradorcico del Medio s/n, 30880 Aguilas (Murcia), Spain
c
Koppert Biological Systems S.L., c/Vicente Aleixandre, 15, 04738 Las Cabañuelas-V!ıcar (Almer!ıa), Spain
d
Koppert Biological Systems S.L., C/Antillas 12, Edf. Generalife 2 C. 18600 Motril (Granada), Spain
e
!
Koppert Biological Systems S.L., C/Obispo P!erez Caceres, 38611 San Isidro (Tenerife), Spain
f
Koppert Biological Systems S.L., Cruce de Arinaga, 35118 Las Palmas, Spain
Received 5 May 2003; received in revised form 20 November 2003; accepted 21 November 2003

Abstract

The whitefly Bemisia tabaci Gennadius is the key pest of protected tomato production in Spain. The predominant form is biotype
‘‘Q’’, an efficient vector of tomato yellow leafcurl virus (TYLCV), which is the principal cause of damage. Although management
has relied primarily on chemical control, factors such as overlapping crop cycles, insecticide resistance and public pressure have
spurred development of alternative management tactics. These include TYLCV-tolerant varieties and pest exclusion methods that,
along with more selective insecticides, have created a more compatible environment for biological control. Here we describe trials of
an integrated pest management (IPM) system conducted during the fall season in 12 commercial greenhouses throughout the
production area compared with 7 greenhouses utilizing only chemical control (termed ‘‘conventional’’). Each IPM greenhouse was
divided into 4 equal sections, two receiving weekly releases of the indigenous Eretmocerus mundus Mercet and two receiving the
exotic Eretmocerus eremicus Rose & Zolnerowich. Fewer and more selective pesticides were used in IPM greenhouses compared to
conventional greenhouses. Early use of broad-spectrum insecticides in IPM greenhouses appeared to be counterproductive in that
establishment of parasitioids was delayed with no real gain in control. Incidence of parasitized whiteflies in IPM greenhouses
averaged around 50%, with E. mundus predominating, compared to less than 3% in conventional greenhouses originating from
immigrating E. mundus. Whiteflies were on average more numerous on plants in IPM greenhouses although there were exceptions.
Also, whitefly populations in IPM greenhouses tended to decrease as the crop matured, in contrast to conventional greenhouses.
Biological control was most successful where TYLCV-resistant cultivars and exclusion strategies (insect netting) reduced whitefly
populations and the risk of virus disease. Continued acceptance of these tactics, and increasing public demand should create a
favorable climate for increased implementation of biologically based pest management in protected tomato culture.
r 2004 Elsevier Ltd. All rights reserved.

Keywords: Bemisia tabaci; Eretmocerus mundus; Eretmocerus eremicus; Biological control; Tomato; Spain

1. Introduction grown in greenhouses on the southern Mediterranean

coast in the communities of Andaluc!ıa and Murcia.
Spain is a major tomato producer, harvesting 3.7 Approximately 58% of these tomatoes were exported,
million tons from 147,000 acres in 1998. Almost 40% of primarily to northern Europe.
this production consisted of fresh market tomatoes Transplanting in greenhouses begins in late summer,
with a possible additional planting in late winter.
*Corresponding author. Tel.: +1-941-658-3400; fax: +1-941-658- Harvesting begins in October, peaks in March, but
3470. continues through early summer. The best prices usually
E-mail address: pstansly@ufl.edu, pas@ufl.edu (P.A. Stansly).
1
! Vegetal y Biotecno-
Present address: Departamento de Proteccion
occur in winter when there is little competition from
log!ıa. Instituto Valenciano de Investigaciones Agrarias (IVIA), greenhouses in northern Europe or elsewhere. Spanish
Apdo. Oficial. 46113 Moncada (Valencia), Spain production methods are steadily improving, principally

0261-2194/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cropro.2003.11.016
 ARTICLE IN PRESS
702 P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

through upgrading of greenhouses from traditional low of tactics such as TYLCV-resistant cultivars, whitefly
roofed structures (little more than grape arbors covered excluding structures, late planting to reduce migration
with polyethylene film) to large, high-roofed, multiple from the previous season’s crop, and selective insecti-
units often provided with automatically controlled cides. Integration of biological control with these
heating and ventilation, and with vents and doors often methods would decrease selection pressure against
fitted with pest-excluding screen. Nevertheless, they insecticides, reduce environmental and health risks
generally lag behind their counterparts in Northern associated with heavy insecticide use, and increase
Europe who generally grow in fully equipped glass consumer acceptance and market value of the product.
greenhouses and use biological control through most Commercially available options for biological control
if not all of the season. Therefore, the annual shift of B. tabaci include Eretmocerus eremicus Rose &
south for sources of tomatoes and other vegetables may Zolnerowich (Hymenoptera: Aphelinidae). This North
result in products of lesser quality, subjected to greater American species is mass reared on the greenhouse
pesticide use. whitefly Trialeurodes vaporariorum (Westwood) (Homo-
In response to customer demand, buyers are in turn ptera: Aleyrodidae) but is equally adapted to both
pressuring growers to reduce pesticide use and provide whitefly species as host (Greenberg et al., 2002).
some produce using Integrated pest management (IPM) However, E. eremicus released to control B. tabaci on
methods that include only natural enemies and selective greenhouse tomato and pepper is typically displaced by
chemicals. Fortunately, most tomato growers in the an indigenous cogenitor, Eretmocerus mundus Mercet
region are already conditioned to use selective insecti- (Hymenoptera: Aphelinidae), immigrating from outside
cides because of the almost universal practice of (Van der Blom, 2002). E. mundus is maladapted to
bumblebee pollination. Nevertheless, biological control T. vaporiarorum (Greeenberg et al., 2002) necessitating
has advanced more quickly against the western flower rearing systems based on B. tabaci. The objective of the
thrips Frankliniela occidentalis (Pergande) in greenhouse present study was to test the feasibility of biologically
pepper. This was especially true in the northern part of based IPM in greenhouse tomato using E. mundus for
the region around Cartagena, where pepper is planted in control of B. tabaci under a variety of commercial
late fall or early winter. This system allows sufficient conditions in southern Spain.
time early in the crop cycle for establishment of the mite
Amblyseis cucumeris (Oudemans) (Acari: Phytoseiidae)
and the minute pirate bug Orius laevigatus (Fieber) 2. Materials and methods
(Hemiptera: Anthocoridae) (Van der Blom et al., 1997).
Biological control in tomato presents a number of 2.1. Greenhouses
additional challenges.
As in most of the hot regions of the world where A total of 19 greenhouses were selected for the study
tomatoes are intensively cultivated, the whitefly Bemisia in four provinces of the southern Mediterranean coast
tabaci Gennadius is a key pest, due primarily to its role !
of Spain: Murcia (Aguilas, !
Mazarron), Almer!ıa (La
as a virus vector. In southern Spain this includes two Cañada, El Ejido) Granada (Motril), and the Canary
types of tomato yellow leaf curl virus (TYLCV), Israeli Islands (Tenerife, Las Palmas, Fig. 1, Table 1). All
and Sardinian (begonmoviridae = geminivirus) , as well greenhouses were covered with polyethylene film except
as tomato chlorosis virus (ToC), a crinivirus (Closter-
oviridae), (Navas-Castillo et al., 2000). Biotype ‘‘B’’ =
B. argentifolii has been detected in southern Spain but
has been completely or largely displaced by the native
biotype ‘‘Q’’ (Guirao et al., 1997; Simon, ! 2002). One
consequence of this predominance may be rapid spread
of TYLCV, given that biotype ‘‘Q’’ has been shown to
be the more efficient transmitter of the virus (Sa! nchez-
Campos et al., 1999). Cultural practices in Spain also
lend themselves to whitefly and virus problems. Over-
lapping crop cycles assure high pest and inoculum levels
and heavy pesticide use against captive pest populations.
Resistance against imidacloprid and other neonicoti-
noids has already been documented (Cahill et al., 1996;
Elbert and Nauen, 2000).
Biological control is directed at immature stages and
cannot control the spread of TYLCV by the adult. Virus
spread must first be controlled through a combination Fig. 1. Map of Spain showing location of study sites.
Table 1
Identification number, location and management system of greenhouse, its size and type, tolerance or susceptibility of tomato variety to TYLCV of tomato variety, planting date, duration of study,
release rates (no./m2 or kg/ha) of natural enemies and number of releases (applications) made

Greenhouse IPM (I), Size (m2) Typea Cultivar Planting Duration E. eremicus E. mundus M. caliginosus D. isaea P. persimilis
conventional (C) date (weeks) no./m2 (releases) no./m2 (releases) no./m2 (releases) no./m2 (releases) no./m2 (releases)

P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

1 !
Agilas1(I) 3600 L–P–M + Tolerant 15-Aug 17 16.7 ( 9) 11.7 ( 7) 0.61 (1) 1 (6) 19.4 (11)
2 !
Aguilas1(C) 9000 L–P–M ++ Tolerant 15-Aug 17 None None None None None
3 !
Agilas2 (I) 2700 L–P–S + Tolerant 28-Jul 16 3 (9) 9 (3) None None None
4 Canarias1 (I) 20,000 6  6+ Tolerant 9-Sep 20 10.5 (5) 10.5 (5) None None None

ARTICLE IN PRESS
5 Canarias2(C) 3000 12  14++ Susceptible 22-Sep 13 None None None None None
6 Canarias3 (C) 4000 6  10+ Susceptible 18-Sep 21 None None None None None
7 El Ejido (I) 8000 L–P–M ++ Susceptible 20-Aug 22 18.75 (8) 18.8 (8) 0.1 (1) None None
8 El Ejido (C) 8000 L–P–M ++ Susceptible 20-Aug 17 None None None None None
9 La Cañada1(I) 25,000 H–A–M +++ Susceptible 15-Aug 28 10.2 (4) 10.2 (4) None None None
10 La Cañada1(C) 22,000 H–A–M +++ Susceptible 30-Aug 26 None None 0.5 (3) 1 (5) None
11 La Cañada2 (I) 20,000 H–A–M +++ Susceptible 23-Aug 22 19.5 (8) 19.5 (8) 1 (2) 0.675 (5) None
12 La Cañada2 (C) 20,000 H–A–M +++ Susceptible 30-Aug 22 None None None None None
13 ! (I)
Mazarron1 1000 H–A–S +++ Tolerant 26-Sep 23 10 (4) 10 (4) 0.5 (1) 0.75 (3) None
14 ! (I)
Mazarron2 2500 L–P–S + Tolerant 15-Sep 21 33 (5) 33(5) None 0.3 (3) 3.75 (3)
15 Motr!ıl1 (I) 7000 H–A–M+++ Susceptible 14-Aug 23 6 (4) 6 (4) None None None
16 Motr!ıl2 (I) 10,000 H–A–M+++ Susceptible 14-Aug 29 6 (4) 6 (4) None None None
17 Motr!ıl2 (C) 10,000 H–A–M+++ Susceptible 16-Aug 29 None None None None None
18 Motr!ıl3a (I) 2500 L–P–S + Susceptible 7-Aug 21 8 (5) 8 (5)999 None None None
19 Motr!ıl3b (I) 3000 L–P–S + Susceptible 8-Aug 20 15 (5) 15 (5) None None None
a
Greenhouse types: height (L=low, H=high), pitch (F=flat, P=pitched, A=Arched), units (S=single, M=multiple), exclusion (poor +, fair ++, good +++).

703
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704 P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

those in the Canary Islands, which were covered with greenhouse was measured as the sum of the ratings (1–4)
polyethylene mesh screen. Size ranged from 0.1 to 2.5 ha for pupae and adults of E. eremicus or the closest
and design was classified as (1) high or low roofed, (2) other species given (usually Encarsia formosa Gahan
!
flat (‘‘parral’’), pitched capilla or arch-roofed (tunel), (Hymenoptera: Aphelinidae), and the mean number of
and (3) either single or multiple unit. Effectiveness of weeks of residual effect. The sum of these 3 numbers
pest exclusion was rated as poor, good or excellent varied between 2 and 18 (Table 2). For example, the side
based on installation of screened vents and double doors effects of abamectin on E. eremicus were rated as 1 for
and sticky card captures. pupae, 4 for adults and 3 for weeks of persistence, giving
a total rating of 8 for each application. For the fungicide
2.2. Pest management dinocap, values for E. eremicus are incomplete but are
given for E. formosa as 1, 4 and 1 (effects on pupae,
Natural enemies were released to control whiteflies adults and persistence respectively), giving an overall
and other pests in 12 of the greenhouses designated rating of 6. These impact ratings were summed for each
‘‘IPM’’. The 7 remaining greenhouses relied totally on greenhouse and then divided by the number of weeks of
insecticidal control and were termed ‘‘conventional’’. In monitoring to give an index of incompatibility (II)
five cases, an IPM and conventional greenhouse shared during the period of study.
the same location, grower/operator, and growing con-
ditions for paired comparison. Each greenhouse was 2.4. Monitoring
divided into 4 equal-sized sectors for sampling purposes.
In addition, sectors in IPM greenhouses were used for Each of the 4 sectors of each greenhouse was
two replicates each of two treatments in a Latin square monitored weekly for pests and diseases by the assigned
design. E. eremicus (Ercal, Koppert Biological Systems, consultant. Eight yellow and eight blue sticky traps
Berkel en Rodenrijs Holland) (reared on T. vaporarior- (Hombio BVBA, Sint-Katelijne Waver, Belgium) were
um) was released in 2 of the sectors and E. mundus placed at canopy height in each sector, exposing a single
(Bemipar, Koppert Biological Systems S.A., Aguilas! fresh 20  12 cm surface every week. Whiteflies (yellow
(Murcia), Spain) (reared on B. tabaci) was released in card) and thrips (blue card) were counted up to 25,
the remaining two. Release rates and timing (based on or classified as medium (26–100) or high (100+).
weekly counts of whiteflies) were made at the discretion Adult whiteflies and nymphs on an upper, middle and
of the Koppert consultant responsible for the green- lower leaf of 8 plants in each sector were counted until
house, subject to the grower’s approval. 10 per leaf or classified as medium (11–25) or high
Additional natural enemy species that may have been (25+). Larvae of Lepidoptera and several species
released included Macrolophus caliginosus Wagner of beneficial insects including adults of Aphelinidae
(Heteroptera: Miridae) for whiteflies, Diglyphus isaea (Encarsia spp., Eretmocerus spp.) and predaceous
(Walker) (Hymenoptera: Eulophidae) for leafminers, Miridae (M. caliginosus, Nesidiocoris [Cyrtopeltis] tenuis
Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseii- [Reuter]) were also counted on these leaves. Infestations
dae) for spider mites. Cooperating growers purchased of spider mites (Tetranychus urticae Koch), leafminers
these biological control agents from Koppert Biological (Liriomyza bryoniae [Kaltenbach] and L. trifolii [Bur-
!
Systems, Aguilas (Murcia) Spain. Decisions on pesticide gess]), and thrips (F. occidentalis) were estimated as
applications in conventional greenhouses were made by light, medium or heavy according to the consultant’s
the grower and in the IPM greenhouses jointly by the criteria. The presence of foliar or vascular diseases was
grower and Koppert consultant. noted. Production data, when available, were supplied
by the grower.
2.3. Pesticide impact The incidence of parasitism was estimated from
samples taken between mid-October and February.
Pesticide applications were noted and their likely Leaves with late 4th instar whitefly nymphs (wingbuds
impact on natural enemies assessed according to the visible, heretofore referred to as ‘‘pupae’’) were collected
Koppert Side Effects Guide (Anonymous, 2002). In at random by sector, placed in plastic bags, and
this guide, effects of pesticides are rated for pupae transported to the laboratory in an insulated cooler.
or nymphs and adults of each natural enemy as: Whitefly pupae and exuviae were classified to species
(1) harmless (reduction in control capacity o 25%), and as parasitized (presence of parasitoid pupa) or not
(2) slightly harmful (25–50% reduction in control parasitized (presence of whitefly wingbuds) using a
capacity), (3) moderately harmful (50–75% reduction stereoscopic microscope. Leaves were then placed in a
in control capacity), or (4) very harmful (>75% paper envelope (17  22.5 cm) from which a lower
reduction in control capacity). A third rating for corner had been cut out to receive a 1.5 mm poly-
persistence in weeks is given as a single number or propylene snap cap Eppendorf-type centrifuge tube. The
as a range. The impact of each application in the inside of the tube had been smeared with a mixture of
 ARTICLE IN PRESS
P.A. Stansly et al. / Crop Protection 23 (2004) 701–712 705

Table 2
Pesticides used in greenhouses under study and side effects ratings of: (1) harmless, (2) slightly harmful, (3) moderately harmful, or (4) very harmful
(Anonymous, 2002) summed for pupae and adults E. eremicus or the closest other species plus mean number of weeks of residual effect

Broad-spectrum insecticide Side effect rating Selective insecticide (w) Rating Fungicide Side effect rating
targeted whitefly

Asephate 15 Abamectine 8 Benomyl 2

Bifentrin 18 Amitraz 8 Bromopropylate 2
Chlorpyrifos 17 Azadiractin (w) 4 Captan 2
Cypermethrin 18 B. thuringiensis 2 Carbendazim 3
Deltametrin 18 Buprofezin (w) 3 Clorothalonil 2
Endosulfan 15 Cyromazine. 2 Copper 2
Fenitrotion 14 Fenbutatin Oxide 2 Cymanazil 5
Fenpropatrin 18 Flufenoxuron 8 Cymoxanil 3
Imidacloprid (foliar) 10 Heptenofos 8 Cyproconazol 3
Malathion 18 Hexithiozox 3 Cyprodinil 2
Methomil 16 Imidacloprid (soil) (w) 5 Dimethomorph 3
Oxamil (foliar) 18 Lufenuron 4 Dinocap 6
Tau Fluvalinate 14 Oxamil (soil) (w) 5 Fludioxonil 2
Tralometrine 16 HMOa(w) 4 Folpet 2
Potassium Soap (w) 4 Iprodion 2
Pymetrozine (w) 3 Mancozeb 2
Pyridaben (w) 8 Metalaxil 3
Pyriproxyfen (w) 5 Metiram 6
Tebufenpyrad 3 Myclobutanil 2
Teflubenzuron 2 Nuarimol 3
Nuarimol 3
Procimidon 2
Procloraz 2
Propamocarb 2
Pyrimethanil 2
Sulfur 7
Thiofanate methyl 2
Tiram. 4
Triadimenol 2
Vinclozolin 2
Zineb 2
a
Horticultural mineral oil.

honey, glycerol (10%) and a small amount of methyl- (SAS Institute, 2000). One-way analysis of variance was
cellulose to attract and hold emerging parasitoids and also used to evaluate whitefly and incidence of parasit-
whiteflies. The envelope was sealed with cellophane tape ism within IPM greenhouses between sectors receiving
and held, tube upright, in a controlled temperature E. mundus or E. eremicus. Consistency of sex ratio with
cabinet (2572 C, 7575% RH, 16:8 h L:D) for 3 weeks the 1:1 null hypothesis was tested using chi-square
to allow parasitiods to emerge. All parasitoids and (Sokal and Rohlf, 1981). Correlation analysis was
whiteflies found inside or outside the tube, stuck to the used to look for relationships between pesticide
cellophane tape or lose within the envelope were use and incidence of pests. Data are reported as mean
counted and preserved in 65% EtOH and 5% glycerol. 7 standard error throughout.
Whitefly parasitoids (n=750 total) were mounted on
microscope slides directly into Hoyers mounting med-
ium and identified at 100 and 400  (Polaszek et al., 3. Results
1992; Schauff et al., 1996; Rose and Zolnerowich, 1997;
Zolnerowich and Rose, 1998). 3.1. Pesticide use

2.5. Analysis Whitefly and TYLCV inoculum pressure was greatest

in the early season due to migration from senescing
Mean incidence of each parameter was compared summer crops and rapid insect reproduction caused by
between IPM and conventional greenhouses over all high temperatures. Most growers either planted
sample weeks using a one-way analysis of variance with TYLCV-resistant cultivars or used broad-spectrum
the greenhouse  week interaction as the error term insecticides early in the season (September–October).
 ARTICLE IN PRESS
706 P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

Only one did both. IPM growers were more likely to use Incidence of parasitized pupae from leaf samples
resistant cultivars, tended to spray less often and used taken in IPM greenhouses where Eretmocerus spp. were
products that were more selective when they did spray released was estimated at 50.773.7% (n=108), com-
(Table 3). pared to 2.270.97% (n=16) in conventionally managed
Frequency of pesticide applications varied from 5 in greenhouses. The corresponding numbers for emerged
23 weeks to 27 in 41 weeks (Table 3), or a mean (7SE) adult parasitoids were 41.673.5% (n=113) and
of 0.6970.11 applications per week in conventional 0.7370.46% (n=20) respectively. In IPM greenhouses,
greenhouses and 0.4970.64 per week in IPM green- no differences were observed by either measure between
houses. Total number of products employed in these sectors where E. mundus or E. eremicus was released
applications ranged from 9 to 74 (40.079.8 and 20.47 (F=1.39, P=0.27, df=1,10 and F=0.22, P=0.65,
2.5 per greenhouse, conventional and IPM respectively). df=1.11 respectively). Of 570 Eretmocerus spp. adults
Broad-spectrum insecticides were applied in 5 or 42% of that emerged from IPM greenhouse leaf samples,
the IPM greenhouses and 5 or 71% of conventional 85.073.7% (n=113) were E. mundus. Overall, the
greenhouses, mostly for whitefly control early in the percentage of E. mundus rose from 47.5720.6% (n=4)
cropping season. All but one of these 10 greenhouses during the last 2 weeks of October to 100% the last 2
was planted to TYLCV-susceptible cultivars. The most weeks of January. However there were no differences in
frequently used pesticide in this category was methomyl, incidence of parasitism over all dates between sectors
followed by endosulfan and tralomethrin (Table 4). The regardless of which Eretmocerus species was released
remaining 9 greenhouses where no broad-spectrum (F=0.001, P o 0.98, df=1,10).
insecticides were used either contained tolerant varieties Sex ratio of E. mundus favored females by 1.39:1
or were tightly screened against whiteflies. The one which deviated significantly from 1:1 (X2=7.67,
exception to this pattern was a conventionally managed Po0.01, df=1). Sex ratio of the 52 E. eremicus that
!
greenhouse (Aguilas 1) where mixtures of 3 or 4 emerged from leaf samples also was skewed 1.48:1
products were sprayed once or twice weekly even towards females (X2=4.81, Po0.05, df=1). We found
though a resistant cultivar was planted. 122 Encarsia sophia (Girault & Dodd) = Encarsia
Nine of the 20 selective insecticides used also targeted transvena (Timberlake), mostly from one location in
whiteflies early season (14.675.6 conventional; Motril late in the season. The sex ratio of this
8.671.4, IPM). Pymetrozine was the most frequently heteronomous hyperparasitoid was strongly male biased
used of these, followed by buprofezin, horticultural (0.37:1, X2=12.9, Po0.01, df=1) indicating that many
mineral oil, oxymyl applied through drip irrigation and Eretmocerus spp. were being parasitized. No other
pyriproxyfen (Table 4). Other selective pesticides targeted aphelinids were observed from samples taken on the
spider mites, Noctuidae, and agromyzid leafminers. mainland, although one small sample from Tenerife
Fungicides (16.973.3, 9.671.4 IPM, conventional) contained 2 female Encarsia lutea (Masi).
were applied mostly late season (November–January)
when cool, humid conditions in the greenhouses were
especially conducive to fungal disease. 3.3. Pest and natural enemy incidence: IPM vs
The index of incompatibility (II) in IPM greeenhouses conventional
varied from 1.1 to 8.7 for a mean of 4.570.7 and in
conventionally managed greenhouses from 1.1 to 35.7 Numbers of adults captured on sticky traps were not
for a mean of 11.274.4 (F=3.8, df=1,17, Po0.067). different between IPM and conventional greenhouses.
Differences in II between IPM and conventional green- Thus, movement of whiteflies (and presumable ingress
houses among the 5 paired comparisons ranged from 30 into greenhouses) was not affected overall by the pest
!
(Aguilas 1) to 0 (Cañada 2). management system employed (F=0.09, df=1,23,
Po0.77, Table 5). Nevertheless, almost twice as many
whitefly adults and 3 times as many nymphs were
3.2. Whitefly species and incidence of parasitism observed overall on plants in IPM greenhouses com-
pared to conventional greenhouses (F=36.1 and 35.1
Bemisia tabaci was the most frequent whitefly respectively, df=1,23, Po0.001). Although scouts had
observed and the only one seen in the most southerly difficulty discerning parasitized whitefly nymphs or
mainland locations of Motr!ıl and El Ejido. Trialeurodes seeing adult whitefly parasitoids, they did observe
vaporarirum was most often observed during the cooler significantly more in IPM greenhouses compared to
!
months in Aguilas, and to a lesser extent in the Canary conventional greenhouses (F=26.7 and 21.8, respec-
! and rarely in La Cañada. Only 29 of
Islands, Mazarron tively, df=1,23, Po0.0001). Numbers of the whitefly
1885 pupae observed in leaf samples were T. vaporiar- predator Nesidiocoris tenuis were also greater in IPM
iorum, reflecting in part the fact that almost 2/3 of the greenhouses (F=8.04, df=1,23, Po0.009). No signifi-
samples came from Motr!ıl. cant differences were observed in numbers of other pests
Table 3
Duration of study, number of pesticide applications and products included, and the number of those classified as broad-spectrum insecticides (score of 9 or more), selective insecticides/acaracides or
fungicides, sum of side effect ratings for all pesticides used, and index of incompatibility of pesticide regime with Eretmocerus spp. or similar parastitoids

Greenhouse Cultivar Production Duration (w) Applications Products Broad Selective fungicides Sum of Indexb of
IPM (I), tolerance to (kg/m2) (no.) (no.) spectrum side effect incompatibility
ratingsa

P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

conventional TYLCV
(C)
!
Aguilas 1(I) Tolerant 8.7 17 12 28 0 17 11 77 4.5
!
Aguilas 1(C) Tolerant 8.9 19 22 71 41 7 23 679 35.7

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!
Agilas 2 (I) Tolerant 16 6 14 0 7 7 48 3.00
Cañada 1(I) Susceptible 28 9 25 4 3 18 116 4.14
Cañada 1(C) Susceptible 26 10 26 5 2 19 134 5.2
Cañada 2 (I) Susceptible 22 7 9 0 2 7 25 1.14
Cañada 2 (C) Susceptible 22 7 9 0 2 7 25 1.14
Canarias 1 (I) Tolerant 20 6 20 0 5 15 64 4.00
Canarias 2(C) Susceptible 33 13 38 2 15 21 160 4.8
Canarias 3 (C) Susceptible 23 25 74 2 45 27 287 13.7
El Ejido (I) Susceptible 4.0 17 7 17 0 11 6 68 3.09
El Ejido (C) Susceptible 3.9 17 7 14 0 11 3 95 5.6
Mazarron! 2 (I) Tolerant 21 10 16 0 10 6 56 2.67
Mazarron! 1 (I) Tolerant 23 5 10 0 2 8 26 1.13
Motr!ıl 1 (I) Susceptible 14.9 23 19 24 5 11 8 155 6.7
Motr!ıl 2 (I) Susceptible 12.9 29 27 41 7 16 18 253 8.7
Motr!ıl 2 (C) Susceptible 10.3 29 32 48 10 20 18 377 13.0
Motr!ıl 3a (I) Susceptible 4.6 11 21 21 6 9 6 151 7.2
Motr!ıl 3b (I) Susceptible 5.4 10 20 20 5 10 5 149 7.5
a
Sum of ratings from Table 2 for all pesticides used.
b
Score/weeks.

707
 ARTICLE IN PRESS
708 P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

Table 4
Number of applications of broad-spectrum and selective insecticides directed at whitefly per greenhouse in 19 greenhouses

Broad spectrum Applications Selective Applications

mean7SE (max) mean7SE (max)

Methomil 1.3770.89 (17) Pymetrozine 1.4270.68 (10)

Endosulfan 0.7970.47 (8) Buprofezin 0.7970.36 (5)
Tralometrine 0.6370.29 (3) HMOa 0.7470.37 (5)
Tau Fluvalinate 0.3770.26 (4) Oxamyl (injected) 0.7470.32 (5)
Malathion 0.2670.26 (5) Soap 0.7470.26 (4)
Methamidophos 0.2170.14 (2) Pyriproxyfen 0.6370.29 (5)
Fenitrotion 0.1670.16 (3) Pyridaben 0.5870.19 (3)
Fenpropatrin 0.1670.16 (3) Azadiractin 0.3770.22 (3)
Asephate 0.1170.07 (1) Imidacloprid 0.1170.07 (1)
Bifentrin 0.1170.07 (1)
Deltametrin 0.1170.07 (1)
Cypermethrin 0.0570.05 (1)
Heptenofos 0.0570.05 (1)
a
Horticultural mineral oil.

Table 5 greenhouse. However, parasitism rose to over 40% in

Mean incidence of whiteflies, parasitoids, N. tenuis, leafmines spider
the IPM greenhouse and whitefly populations tended to
mites and larvae of Lepidoptera observed by scouts in IPM and
conventional greenhouses decrease toward the end of the crop cycle, finishing
the season at 0.6070.087 nymphs per leaf, well below
Conventional IPM the overall mean of 2.370.18 nymphs per leaf. This
Adults whiteflies (no./trap/wk) 30.271.52a a
28.471.01a decrease was not seen in the conventional greenhouse
Adult whiteflies (no./leaf) 0.2970.011b 0.5470.014a where whitefly populations were maintained at near the
Whitefly nymphs (no./leaf) 0.3970.02b 0.9970.03a mean of 0.5870.08 nymphs per leaf toward the end of
Parasitized ‘‘pupae’’ (%) 0.9070.08b 3.770.13a
the growing season.
Eretmocerus sp. (adults/leaf) 0.000370.0002b 0.008370.0008a
N. tenuis (no./leaf) 0.00470.001b 0.05370.003a Although similar pesticide regimes were also used in
a
both greenhouses at El Ejido, only selective materials
Means in the same row followed by the same letter are not
were applied. These consisted of the insect growth
significantly different (P o 0.05).
regulators (IGR)s azadiractin, buprofezin and pyripor-
xyfen as well as pyridaben and insecticidal soap.
monitored, including thrips, leaf miners, spider mites However, seven more such sprays were applied in the
and caterpillars (data not shown). conventional greenhouse than in the IPM greenhouse, a
Comparisons between individual IPM-conventional difference of 1.5 incompatibility units (Table 3). Both
greenhouse pairs illustrated some effects not evident greenhouses were initially screened against whiteflies,
in the overall comparison. Similar pesticide regimes but the netting was removed in week 44 to increase
were used in IPM and conventional greenhouses in 4 of ventilation and reduce fungal disease, causing an influx
the 5 locations (Table 3) including La Cañada 2, where of whitefly adults mainly into the IPM greenhouse as
low counts on yellow sticky traps reflected tight indicated by higher trap counts (Table 6). Consequently,
construction and screening (Table 6). Numbers of more than twice as many nymphs were seen in the IPM
whiteflies were also low on plants at this location, greenhouse compared to the conventional greenhouse
although more adults were observed in the IPM although numbers of adults on plants were similar.
greenhouse. The apparent failure of parasitoids to Apparently, the effect of extra IGR insecticides on
reduce the whitefly population in the IPM greenhouse whitefly nymphs in the conventional greenhouse coupled
may have been due to relatively low incidence of both with fewer immigrating whiteflies outweighed the addi-
whiteflies and parasitism 28.8710.3% (N=9). tional parasitism occurring in the IPM greenhouse.
At nearby La Cañada 1 the grower used broad- Broad-spectrum insecticides were extensively used on
spectrum insecticides early in the crop cycle to control the TYLCV-susceptible tomatoes in both greenhouses at
whiteflies and virus on his TYLCV-susceptible tomatoes Motr!ıl 2, especially early in the season (II=8.7 and 13.7,
(Table 3). Almost 5 times fewer whiteflies were seen on IPM and conventional greenhouses respectively,
traps in the conventional greenhouse compared to the Table 3). Incidence of parasitized whitefly ‘‘pupae’’
IPM greenhouse where the common entrance to both was low and similar in both greenhouses: 2.272.2%,
greenhouses was located (Table 6). As a likely result, n=9 and 3.972.0%, n=5 IPM and conventional
more whiteflies were also seen on plants in the IPM respectively). Whitefly numbers were similar in both.
 ARTICLE IN PRESS
P.A. Stansly et al. / Crop Protection 23 (2004) 701–712 709

Table 6
Mean7SE number of adult whiteflies per yellow sticky trap, B. tabaci adults and nymphs per leaf from in field monitoring and percent parasitized
whitefly ‘‘pupae’’ from leaf samples

Greenhouse Management system B. tabaci

Whiteflies/Trap/wk Adults/leaf Nymphs/leaf Parasitized pupae (%)

La Cañada 1 IPM 7.971.2 0.1770.01 0.1870.02 28.8710.3

Conventional 8.671.6 0.09770.002 0.1170.03 2.1472.14

La Cañada 2 IPM 7.572.9 0.2370.02 2.2770.18 41.1711.6

Conventional 1.670.4 0.1270.03 0.5870.08 070

El Ejido IPM 50.674.8 0.8970.05 2.0270.19 51.3712.6

Conventional 40.475.0 0.6870.04 1.07670.14 5.4572.2

Motr*ıl 2 IPM 14.971.7 0.270.02 0.2670.04 2.2270

Conventional 20.672.27 0.2470.03 0.2670.03 3.972.04

!
Aguilas 1 IPM 21.572.9 0.2670.02 0.2070.03 43.3712.9
Conventional 14.372.4 0.2170.02 0.1470.02 070

!
Only at Aguilas 1 was there a great disparity in monitored. Although only insecticidal soap was used,
pesticide use between the IPM and conventional green- fewer adults and nymphs were seen on plants than in
house even though a resistant cultivar was planted many greenhouses where trap counts were lower and
in both (Table 3). The grower ordered mixtures of broad-spectrum insecticides used. Thus, considerable
broad-spectrum insecticides to be applied once or twice control could be attributed to parasitism that averaged
a week against whiteflies in the conventional green- 50% and the mirid predator N. tenuis that was found on
house, accumulating an incompatibility index of 35.7 an average of 1 every 2 leaves (Table 7). Nevertheless,
(Table 3). In contrast, only selective pesticides were used losses due to TYLCV would probably have been great
in the IPM greenhouse, resulting in an incompatibility had not a resistant variety been used.
index of only 4.5. Although captures on sticky traps Mazarron! 2 was a small, open-sided greenhouse
were 50% higher in the IPM greenhouse (Table 6, where whitefly captures reached a peak of 80 per trap
Fig. 2a), probably because of wind damage to the plastic in week 38. However, these numbers were not sustained
roof, there was little difference in numbers of adults or (mean 16.9572.18) and numbers on plants remained
nymphs of B. tabaci overall. Furthermore, almost 5 low (Table 7). Index of incompatibility was low (2.67,
times fewer B. tabaci adults plus nymphs were observed Table 3), with only imidacloprid applied at planting,
on leaves in the IPM greenhouse (0.08370.0, Fig. 2b) and pyridaben and buprofezin sprayed 2 weeks later.
compared to the conventional greenhouse at the end of Incidence of parasitized whitefly ‘‘pupae’’ was only 30%
the crop cycle (Fig. 2b). The decline of the whitefly (Table 7), but samples were probably taken too early,
population in the IPM greenhouse may have been due to just after the release period (weeks 45 and 47). Thus,
the effect of parasitism which averaged 43% (Table 6). there was little other than parasitism to explain declining
In contrast to B. tabaci, greenhouse whitefly was whitefly numbers over the course of the season.
eliminated in the conventional greenhouse but rose TYLCV-susceptible cherry tomatoes typical of the
toward the end of the crop cycle in the IPM greenhouse, region were grown at Motr!ıl 1 and broad-spectrum
probably because E. mundus is not effective against this insecticides were freely used early in the crop cycle
species (Greenberg et al., 2002) (Fig. 2c). (II=6.74, Table 3). As a likely result, releases of
Eretmocerus spp. resulted in little (3.5773.57%) para-
3.4. Additional greenhouses sitism being observed. Although the greenhouse was
tightly constructed and whitefly counts on plants were
Experiences in the remaining greenhouses receiving generally low (Table 7), an early influx in week 41
Eretmocerus spp. further illustrated the role of pest resulted in 30 whiteflies per trap and a high incidence of
exclusion in determining whitefly numbers, of virus TYLCV, requiring over 700 infected plants to be
resistance in influencing pesticide use, and of the removed by week 45.
interplay of these factors on the effectiveness of Both IPM greenhouses at Motr!ıl 3 were open-sided
biological control. Trap captures at Aguilas 2 averaged allowing free entry of whiteflies and both were treated
88 per week (Table 7), higher than in any greenhouse extensively with broad-spectrum insecticides early in the
 ARTICLE IN PRESS
710 P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

110
Traps IPM
100
Traps CHEM
90

80
WF/trap/week

70

60

50

40

30

20

10

0
(A) 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50

1.4
B. ta ba ci IPM
B. ta ba ci CHEM
1.2

1
WF/Leaf

0.8

0.6

0.4

0.2

0
(B) 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50

0.8
T. vaporiarom IPM
T. vaporiarom CHEM
0.7

0.6

0.5
WF/Leaf

0.4

0.3

0.2

0.1

0
35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50

(C) Week
Fig. 2. (A) Mean (SE) number of whiteflies per trap per week, (B) mean (SE) number of B. tabaci nymphs per tomato leaf, and (C) mean number of
!
T. vaporiariorum nymphs and pupae per tomato leaf in the IPM and conventionally managed greenhouses at Aguilas 1 IPM Sep.–Dec. 2001.

crop cycle, preventing early establishment of parasi- have contributed to the failure of biological control at
toids. Only horticultural mineral oil was used later but this location.
whitefly numbers remained high on sticky traps and The greenhouse Canarias 1 was planted to a TYLCV-
plants, despite an ultimately high incidence of parasitism resistant cultivar and covered with coarse mesh screen
(Table 7). Extensive hyperparasitism, (17% of all that did not exclude whiteflies. Pesticide use was limited
parasitoids observed were E. sophia males) may also to fungicides and selective insecticides, none directed
 ARTICLE IN PRESS
P.A. Stansly et al. / Crop Protection 23 (2004) 701–712 711

Table 7
Mean7SE number of adult whiteflies per yellow sticky trap, number of B. tabaci adults and nymphs per leaf, parasitized ‘‘pupae’’ (%), and number
of Nesidiocorus tenius per leaf in 5 IPM greenhouses and 2 conventional greenhouses

Greenhouse Management B. tabaci (no.) N. tenuis

a
Adults/trap/wk Adults/leaf Nymphs/leaf Parasitized (%) No./leaf

Aguilas 2 IPM 88.074.11 1.0470.07 1.6670.16 50.4477.05 0.487 0.03

Mazarron 2 IPM 17.072.18 0.4270.03 0.3370.06 30.2713.9 0
Motr!ıl 1 IPM 6.770.80 0.0970.01 0.1170.02 3.673.6 0
Motr!ıl 3 IPM 60.572.68 1.2370.06 1.9670.09 79.374.3 0
Canarias 1 Conventional 37.173.8 0.2570.02 1.570.12 84.675.8 0.1570.09
Canarias 2 Conventional 76.278.3 0.0670.01 0.1770.03 NA 0.0270.01
Canarias 3 Conventional 69.178.5 0.8370.09 0.6270.08 NA 0.0170.00
a
% parasitized from leaf samples.

against whiteflies. Whitefly numbers peaked at 73 per !

tomato (Lopez, 2002), and probably relate to differences
sticky trap followed by a peak of B. tabaci nymphs to in suitability of B. tabaci as a host (Greenberg et al.,
3.970.78 per leaf 2 weeks later. Incidence of parasitized 2000).
B. tabaci pupae also rose to 84.6%75.8 (n=8) and the Fewer and more selective pesticides were used in IPM
predator N. tenuis appeared spontaneously. In contrast, greenhouses than in conventional greenhouses included
pesticide use was intense in the two conventional in this study, although there were some exceptions.
screenhouses in the Canaries (Table 3). Trap catches Where the index of incompatibility exceeded 5 as it did
and numbers of adults observed on leaves were greater in the ‘‘IPM’’ greenhouses of Motr!ıl and Cañada 1, little
in the conventionally managed greenhouse, although benefit from biological control of whitefly could be
there were more nymphs overall in the IPM greenhouse demonstrated. The strategy in these greenhouses was to
(Table 7). Again, whitefly numbers tended to increase utilize broad-spectrum insecticides early to bring down
over the season in the conventional greenhouses but whitefly populations to a low level before initiating
declined in the IPM greenhouse. biological control. However, residues from these mate-
rials typically persist 8–12 weeks (Anonymous, 2002).
Consequently, E. mundus either did not establish or
4. Discussion established too late to provide adequate control. The
residual secondary effect on parasitoids is probably
E. mundus from either adjacent plots and/or outside shorter for whiteflies than for E. mundus, allowing
the greenhouse replaced E. eremicus in the IPM green- the pest to build up in the crop. Thus, ‘‘pesticide first’’
houses where both were released. These IPM green- strategy using broad-spectrum chemistry was not
houses ranged in size from 25,000 to 1000 m2 for an compatible with biological control using E. mundus.
average of 8775 m2. When divided into fourths, the In contrast, incidence of parasitism was moderate to
average plot size would have been 2194 m2. Assuming a high and whitefly populations on plants remained
square plot, the average distance to a neighboring plot moderate to low in IPM greenhouses where the index
would be equal to 12 the square root of the area or 23.4 m. !
of incompatibility was less than 5, (Aguilas 1 and 2,
There are no published reports on movement of !
Mazeron2, El Ejido, Canarias 1), in spite of often high
E. mundus although E. eremicus has been observed to levels of whitefly immigration. Predation by N. tenuis
fly an average of 35 minutes and to move at least 10 m in !
provided additional whitefly control at Aguilas 2 and
the open field (Byrne and Bellamy, 1999). Thus, Canaria 1 where no broad-spectrum insecticides were
considerable dispersal among plots could have occurred. used. The observed tendency of whitefly populations to
Additional evidence for dispersal of E. mundus within decline in the latter half of the season in IPM
the greenhouse came from the two adjacent greenhouses greenhouses (in contrast to conventional greenhouse)
at Cañada 1, both of which covered 2 ha, were tightly was consistent with an increasing influence of natural
sealed against insects and received the same minimal enemies over the crop cycle. Factors contributing to this
pesticide regime (II=1.14). Incidence of parasitism increasing influence could include absence of interfer-
was only 2% in the conventional greenhouse compared ence from insecticides late in the crop and a higher
to 29% in the IPM greenhouse where only 7 of inherent rate of increase exhibited by E. mundus
73 parasitoids emerging from leaf samples were compared to B. tabaci (Stansly et al., 2002a; Urbaneja
E. eremicus. These observations of apparent competitive et al., 2003). Early establishment of natural enemies in
superiority of E. mundus over E. eremicus are in accord the absence of interfering insecticides was the best
with single generation cage studies on pepper and biological control strategy.
 ARTICLE IN PRESS
712 P.A. Stansly et al. / Crop Protection 23 (2004) 701–712

The ability of E. mundus to control whiteflies in Guirao, P., Beitia, F., Cenis, J.L., 1997. Biotype determination of
Spain has been in demonstrated in commercial-scale Spanish populations of Bemisia tabaci (Hemiptera: Aleyrodidae).
trials in pepper and green beans (Calvo et al., 2002; Bull. Entomol. Res. 87, 587–593.
!
Lopez, J., 2002. Eficacia y competencia de Eretmocerus mundus y
Urbaneja et al., 2002; Te! llez et al., 2003). Parasitoid- Eretmocerus eremicus (Hymenoptera, Aphelinidae) parasitando
induced mortality of whiteflies above 80% was com- Bemisia tabaci (Homoptera, Aleyrodidae) en tomate y pimiento.
monly observed, and populations were controlled with Proyecto Final de Carrera, EUITA, Universidad Polit!ecnica de
no recourse to insecticides. E. mundus appears to be Cartagena, Murcia (Spain).
equally well adapted to tomato as to pepper (Stansly Navas-Castillo, J., Camero, R., Bueno, M., Moriones, E., 2000. Severe
yellowing outbreaks in tomato in Spain associated with infections
et al., 2002a; Urbaneja et al., 2003) although higher of the tomato chlorosis crinivirus. Plant Dis. 84, 835–837.
release rates appear to be necessary in tomato due to Polaszek, A., Evans, G.A., Bennett, F.D., 1992. Encarsia parasitiods of
more rapid whitefly population growth on that crop Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyro-
(Stansly et al., 2002b). Unfortunately, some growers in didae): a preliminary guide to identification. Bull. Entomol. Res.
82, 375–392.
this study had little faith in the resistant cultivars they
Rose, M., Zolnerowich, G., 1997. Eretmocerus Haldeman (Hymenop-
were using for the first time, and their exclusion methods tera: Aphelinidae) in the United States, with descriptions of
gave inconsistent results. Increased adoption of such new species attacking Bemisia (Tabaci complex) (Homoptera:
tactics and consequently of biological control should be Aleyrodidae). Proc. Entomol. Soc. Washington 99, 1–27.
favored in the future by improved technology and S!anchez-Campos, S., Navas-Castillo, R., Camero, R., 1999. Displace-
continued movement towards fewer and more selective ment of tomato yellow leaf curl virus (TYLCV)-Sr. by TYLCV-Is
in tomato epidemics in Spain. Phytopathology 89, 1038–1043.
insecticides. SAS Institute, 2000. SAS/STAT User’s Guide. Cary, NC, USA.
Schauff, M.E., Evans, G.A., Heraty, J.M., 1996. A pictorial guide to
the species of Encarsia (Hymenoptera: Aphelinidae) parasitic on
whiteflies (Homoptera: Aleyrodidae) in North America. Proc.
Acknowledgements
Entomol. Soc. Wash. 98, 1–35.
Simon,! B., 2002. Los biotipos de Bemisia tabaci (Hemiptera:
Thanks are due to the cooperating growers for their Aleyrodidae) en la Cuenca Mediterr!anea. Ph.D. dissertation,
willingness to participate in the study, and to R.G. Van Universidad de Murcia, Departamento de Gen!etica y Microbiolog-
Driesche and 2 anonymous reviewers of the manuscript. !ıa. Murcia España.
The Ministry of Science Technology of Spain provided Sokal, R.R., Rohlf, F.J., 1981. Biometry. W. H. Freeman, New York,
859pp.
partial funding through grant number CDTI 00-0152. Stansly, P.A., Urbaneja, A., Sanchez, E., 2002a. Fecundity and
Florida Experiment Station Journal Series Number survivorship of Eretmocerous mundus Mercet (Hymenoptera:
R-09997. Aphelinidae) on Bemisia tabaci biotype ‘‘Q’’ (Homoptera:
Aleyrodidae) using sweet pepper and tomato. EWSN Abstract
Compendium 1 (6).
Stansly, P.A., Urbaneja, A., Calvo, J., 2002b. Calibration of release
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