Biotypes B and Q of Bemisia tabaci and Their Relevance to Neonicotinoid and Pyriproxyfen Resistance
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216 Horowitz et al. Archives of Insect Biochemistry and Physiology 58:216–225 (2005)
Biotypes B and Q of Bemisia tabaci and Their
Relevance to Neonicotinoid and Pyriproxyfen
Resistance
A. Rami Horowitz,1* Svetlana Kontsedalov,2 Vadim Khasdan,1 and Isaac Ishaaya2
Resistance monitoring for Bemisia tabaci field populations to the juvenile hormone mimic, pyriproxyfen, was conducted from
1996 to 2003 in commercial cotton fields in two areas of Israel: the Ayalon Valley (central Israel) and the Carmel Coast
(northwestern Israel). Although the use of pyriproxyfen ceased in these areas in 1996–1997 (because of the resistance),
resistance levels to pyriproxyfen declined to some extent in the fields but remained quite stable, and the susceptibility has not
been totally restored. Two strains of B. tabaci collected from the Ayalon Valley in the late 1999 and 2002 cotton seasons
(AV99L, AV02L) were assayed for their susceptibility to pyriproxyfen at F1, and subsequently a line of each strain was kept
under controlled conditions without exposure to insecticides. After maintenance of more than 20 generations under laboratory
conditions, the resistance to pyriproxyfen in the untreated strains substantially declined. This decline was concurrent with a
replacement of Q biotype by B-type under non-insecticidal regimes; apparently B biotype was more competitive than the
pyriproxyfen-resistant Q-type. Selection under controlled conditions with neonicotinoids on these B. tabaci strains resulted in
continued pyriproxyfen resistance, predominantly of Q biotype. Based on our data, applications of either pyriproxyfen or
neonicotinoids may select for biotype Q, which would survive to a greater degree where these insecticides are applied. Arch.
Insect Biochem. Physiol. 58:216–225, 2005. © 2005 Wiley-Liss, Inc.
KEYWORDS: Bemisia tabaci; biotypes B and Q; pyriproxyfen; neonicotinoids; acetamiprid; thiamethoxam; resis-
tance to insecticides; selection to insecticides
INTRODUCTION been suggested as contributing to or arising from
the biological distinctiveness of biotypes (Brown
Biotypes of Bemisia tabaci (Gennadius) are mor- et al., 1995; Costa et al., 1993; Beitia et al., 1997;
phologically identical but differ in biochemical, Toscano et al., 1998; Devine et al., 2004). In south-
physiological, and life-history traits that may af- ern Europe and the Middle East, the two most
fect their phenology, host plant specificity, and vi- widespread biotypes are referred to as “B” and “Q”
rus transmission capability (Costa and Brown, (Guirao et al., 1997; Rosell et al., 1997). The B bio-
1991; Wool et al., 1993; Bedford et al., 1994; type has a broad geographical distribution and is
Brown et al., 1995; Frohlich et al., 1999). Further- considered to be a recent invader over much of its
more, barriers or limitations to interbreeding range. The Q biotype was originally considered to
among biotypes of B. tabaci have been reported be restricted to the Iberian Peninsula, but has re-
(Bedford et al., 1994; Costa et al., 1993; De Barro cently been established in other Mediterranean
and Hart, 2000; Devine et al., 2004). Differential countries (Brown et al., 2000; Palumbo et al., 2001;
susceptibility or resistance to insecticides has also Nauen et al., 2002), including Israel, alongside the
1
Department of Entomology, Agricultural Research Organization, Gilat Research Center, M.P. Negev, Israel
2
Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel
Presented at the International Congress of Plant Protection, Beijing, China, May 2004.
Contract grant sponsor: Chief Scientist of the Ministry of Agriculture, Israeli Cotton Board; Contract grant sponsor: Sumitomo Co., Tokyo, Japan; Contract grant
sponsor: Agan Chemicals, Israel.
*Correspondence to: A.R. Horowitz, Department of Entomology, ARO, Gilat Research Center, M.P. Negev, 85280, Israel. E-mail: hrami@volcani.agri.gov.il
© 2005 Wiley-Liss, Inc. Archives of Insect Biochemistry and Physiology
DOI: 10.1002/arch.20044
Published online in Wiley InterScience (www.interscience.wiley.com)Resistance in B. tabaci Biotypes 217
B biotype (Horowitz et al., 2003). In order to dis- Basel, Switzerland), obtained from C.T.S., Hod
tinguish between biotypes, several biochemical and Hasharon, Israel.
molecular markers have been developed. Multiple
arbitrary amplicon profiling (MAAP) techniques, Bemisia tabaci Strains
such as random amplified polymorphic DNA
(RAPD-PCR), are commonly used in defining B. The laboratory susceptible strain of B. tabaci
tabaci biotypes (e.g., Guirao et al, 1997; Horowitz (“S”) was reared on cotton seedlings (“Acala”) un-
et al., 2003), but other PCR techniques have been der standard controlled conditions of 26 ± 2°C,
also proposed (e.g., Frohlich et al., 1999; Brown, 60% RH, and a photoperiod of 14:10 (L:D). This
2000; Cervera et al., 2000). strain was collected from Israeli cotton fields dur-
To date, all confirmed cases of strong B. tabaci ing 1987 and has been maintained since then as a
resistance to pyriproxyfen have been associated laboratory culture without exposure to pesticides.
with the Q rather than the B biotype (Horowitz et It was used as a susceptible standard when evalu-
al., 2003). A pyriproxyfen-resistant B. tabaci strain ating the tolerance of field-collected strains of B.
originally collected from a rose greenhouse in the tabaci to neonicotinoids, pyriproxyfen, and other
western Negev in 1992, and since then kept under insecticides.
controlled conditions with no gene flow from out- Two strains of B. tabaci, AV99L and AV02L, were
side (Ishaaya and Horowitz, 1995), has been iden- collected from the Ayalon Valley in the late 1999
tified as the Q-biotype. It is, therefore, possible that and 2002 cotton seasons, respectively. They were
the present distribution of genes for pyriproxyfen assayed for susceptibility to pyriproxyfen at F1. A
resistance reflects, at least in part, the current dis- part of each population has been maintained un-
tribution of and gene flow between Q type popu- der controlled conditions without any exposure to
lations. Restrictions on interbreeding between Q insecticides while another part was selected with
and B biotypes would prevent the transfer of resis- neonicotinoids.
tance genes between biotypes.
This report analyzes the evolution of resistance Field Collections
to two novel groups of insecticides (neonicotin-
oids and pyriproxyfen) as associated with biotypes Adult whiteflies were collected from 1996 to
B and Q of B. tabaci. Selections for Biotype Q by 2003 from commercial cotton fields in two areas
these insecticides and the competitive advantage of Israel: the Ayalon Valley (central Israel) and the
of Biotype B under non-insecticide regimes are Carmel Coast (NW Israel). Leaves infested with B.
also discussed. tabaci adults and pupae were detached from cot-
ton plants, confined in a wooden rearing cage (50
MATERIALS AND METHODS by 35 by 35 cm), containing cotton seedlings, and
returned to the laboratory within 2–3 h.
Insecticides
Bioassays
The insecticides pyriproxyfen, acetamiprid, and
thiamethoxam were applied as formulated prod- Cotton seedlings (20–25 cm tall) were dipped
ucts: pyriproxyfen (“Tiger,” 10% EC [emulsion in aqueous concentrations of formulated insecti-
concentrate] Sumitomo Co. Tokyo, Japan) and cide, or in deionized water (untreated control). Fif-
acetamiprid (Mospilan SP [soluble powder], 200 teen B. tabaci females confined in clip-on leaf cages
g [AI]/ Kg, Nippon Soda Co., Tokyo, Japan), both were exposed to treated cotton seedlings for 48 h
obtained from Agan Chemical Company, Ashdod, and kept under standard laboratory conditions of
Israel; thiamethoxam (Actara 25 WG [water-dis- 26 ± 2°C, 60% RH, and a photoperiod of 14:10
persible granules], 250 g [AI]/ Kg, Syngenta AG, (L: D). For neonicotinoids, female adult mortality
April 2005218 Horowitz et al.
was determined; for pyriproxyfen, females were re- tional elongation of 5 min was carried out at 72°C
moved and fecundity was recorded. Egg viability for 5 min following the last cycle.
(egg hatch suppression) was determined eight Single 10-mer oligonucleotide primers of arbi-
days after treatment (Ishaaya and Horowitz, trary sequence were tested: OPA-04, -05, -06, -09,
1992). Each bioassay was done with at least four -11; OPB-20; OPC-03; F-12; H-9 (Operon Tech-
concentrations, each with three replicates, on dif- nologies, Alameda, CA). Among them, the primer
ferent days. Mortality curves along with LC val- OPA-06 was used largely to determine the white-
ues were then determined. flies biotypes B and Q.
CAPS (Cleaved Amplified Polymorphic Sequences) on
Selection Procedures the Basis of a Mitochondrial Cytochrome Oxidase I (mtCOI)
Sequence. Using C1-J-2195 and L2-N-3014 primers
The B. tabaci strain that was collected in the (Frohlich et al., 1999), mtCOI gene sequences (~800
Ayalon Valley in the late cotton-growing 1999 sea- bp) from the two biotypes were amplified. Cycle
son (AV99L) was selected with acetamiprid, and parameters for this PCR reaction consisted of 1 min
that collected in 2002 (AV02L) was selected partly at 94°C, 1 min at 52°C, and 1 min at 72°C. After
with acetamiprid and another part with thiameth- cloning and analyzing gene sequences from B and
oxam. A concentration of LC10 of each neonicotin- Q biotypes and comparing them to mtCOI se-
oid was applied on cotton seedlings to every third quences from GenBank, we developed and applied
generation of each strain. A relatively low LC value CAPS using the restriction endonuclease VspI. The
was used in order to avoid eradication of the colony. existing inter-sequence polymorphism between the
two biotypes was visualized by cutting ~350 bp frag-
Determination of B. tabaci Biotypes ments from PCR products in the case of the Q bio-
type and ~50 in the case of B-type (Fig. 1).
Two molecular techniques were used to deter-
mine B. tabaci biotypes B and Q: the more com- Data Analysis
mon RAPD-PCR, and CAPS (cleaved amplified
polymorphic sequences) on the basis of a mito- Probit analyses of the concentration-dependent
chondrial cytochrome oxidase I (mtCoI) sequence. mortality data were made using POLO-PC (LeOra
Recombinant DNA methods. DNA modification and Software, 1987) after correction with Abbott’s
restriction enzymes (MBI Fermentas) were used as (1925) formula. Failure of 95% C.L. (confidence
recommended by the suppliers and carried out as limits) to overlap at a particular lethal concentra-
described by Sambrook and Russell (2001). Com- tion indicated a significant difference.
petent cells were prepared and plasmids isolated
by standard procedures. Transformants of E. coli
RESULTS
strains XL-Blue MRF’ were selected on Luria-Bertani Stability of Resistance in Bemisia tabaci to
plates containing ampicillin (100 µg ml-1). DNA Pyriproxyfen Under Field and Laboratory Conditions
was analyzed by electrophoresis on horizontal 1–
2% agarose slab gels with 1 × TBE buffer for 3 h at Figure 2 presents the resistance monitoring data
80 V and visualized with ethidium bromide. to pyriproxyfen for B. tabaci populations collected
RAPD-PCR Reactions. Each amplification was car- from the Ayalon Valley from 1996 to 2003. By
ried out with Taq DNA Polymerase in a T Gradi- 1996, high resistance to this insecticide had evolved
ent Thermocycler (Biometra, Gottingen, Germany) (Horowitz et al., 1999); consequently, pyriproxyfen
for a 30-reaction cycle. Cycling parameters con- use ceased in this area. The resistance level to
sisted of 1 min at 94°C, 1 min at 37°C, and 2 min pyriproxyfen declined to some extent from 1999
at 72°C. Denaturation at 94°C was carried out for to 2002 but remained quite stable and the initial
2 min prior to the initial PCR cycle and an addi- susceptibility has not been restored (Fig. 2).
Archives of Insect Biochemistry and PhysiologyResistance in B. tabaci Biotypes 219
Fig. 1. CAPS analysis based on
primers complementary to the
mtCOI gene sequence. M: 1-kb
DNA ladder; C: control without
DNA. Lanes 2, 4, 6, 8, 11, 13, and
15 digested with VspI. a: Lanes 1–
8, 10, 11: Samples of populations
from the Carmel Coast (early sea-
son, 2003); all samples were iden-
tified as B biotype. Lanes 12, 13:
Samples of B biotype from Pyri-S
strain (standard); Lanes 14, 15:
samples of Q biotype from Pyri-R
strain (standard). b: Lanes 3, 5, 7,
9, 11 digested with VspI. Lanes 2–
7: Samples of populations from the
Carmel Coast (late season, 2003);
all samples were identifies as Q bio-
type. Lanes 8, 9: Samples of Q bio-
type from Pyri-R strain (standard);
Lanes 10, 11: samples of B biotype
from Pyri-S strain (standard).
In another area, the Carmel Coast (NW Israel), ceptibility to pyriproxyfen at F1, and subsequently
resistance monitoring to pyriproxyfen in B. tabaci a line of each strain was kept under controlled con-
populations was recorded from 1999 to 2003 ditions without any exposure to insecticides. After
(Table 1) as part of the integrated resistance man- maintenance of 26 generations under laboratory
agement (IRM) program in Israeli cotton. Similarly conditions, the resistance to pyriproxyfen in the
to the Ayalon Valley, although the use of this in- untreated strain (that originated from the Ayalon
secticide ceased in 1997, high resistance to py- Valley in 1999) was fully declined (Fig. 3). The
riproxyfen has still been observed in this location toxicity data for pyriproxyfen of AV02L strain un-
since then, except in the early 2003 season when til the 21st generation are presented in Table 2 and
high susceptibility to this insecticide was observed Fig. 4. In the first generation, high resistance to this
in one field in this area (Table 1). insecticide of 375- and 280-fold for LC50 and LC90,
Two strains of B. tabaci were collected from the respectively, was observed. Starting from the third
Ayalon Valley in the late 1999 and 2002 cotton generation, the resistance in B. tabaci declined gradu-
seasons (AV99L, AV02L). They were assayed for sus- ally until generation 18, when the susceptibility of
April 2005220 Horowitz et al.
Fig. 2. Log concentration-response
curves (on a probit scale) for the ef-
fect of pyriproxyfen on Bemisia tabaci
populations collected from 1996 to
2003 from cotton fields in the Ayalon
Valley, Israel.
pyriproxyfen was almost restored (3- and 6-fold re- separately to either acetamiprid or thiamethoxam;
sistance ratio for LC50 and LC90, respectively). this resulted in acetamiprid resistance ratios of ap-
proximately 50-fold in the 21st generation at ei-
Selection for Resistance of B. tabaci (AV-Strains) ther LC50 or LC90 and thiamethoxam resistance of
with Neonicotinoids Linked with Resistance to 40- and 160-fold in the 21st generation at LC50 and
Pyriproxyfen LC90, respectively.
The untreated AV99L strain lost most of its re-
Selection with acetamiprid, which was con- sistance to pyriproxyfen after 26 generations; on
ducted until the 26th generation with a line of the the other hand, when selected with acetamiprid,
strain collected from the Ayalon Valley in the late the resistance to pyriproxyfen was fully maintained
1999 cotton season (AV99L), resulted in approxi- (Fig. 3). Similar results were observed in the 2002
mately 30-fold (LC50 = 134 [72–201] and LC90 = strain (AV02L); selection with either acetamiprid or
1,577 [973–3317]) resistance to this insecticide. thiamethoxam maintained resistance to pyriproxy-
Moreover, a line of the AV02L strain was selected fen (Fig. 4).
TABLE 1. Resistance Monitoring to Pyriproxyfen in Bemisia tabaci Populations Collected from 1999 to 2003 in the Carmel Coast (NW Israel)*
Strain n Slope ± SEM LC50 LC90 RR50 RR90 Biotype
Lab (S) 9,308 1.41 ± 0.03 0.043 0.35 1 1 B
(0.027–0.062) (0.23–0.70)
1999 3,360 2.23 ± 0.20 18.7 70.3 435 199 —
(—)a (—)a
2000 4,006 1.79 ± 0.09 27.4 142.1 637 402 Q
2001 7,482 1.45 ± 0.04 7.3 55.5 170 159 Q
(4.3–10.7) (33.5–137.3)
2002 early season 2,584 0.90 ± 0.06 2.9 76 67 217 Q
(1.1–5.1) (38–278)
2002 late season 7,210 1.63 ± 0.07 12 74 279 211 Q
(6–19) (43–305)
2003 early season 2,744 0.82 ± 0.05 0.05 1.7 1.2 5 B
(0.002–0.13) (0.6–97)
2003 late season 5,052 1.31 ± 0.06 8 76 186 217 Q
(3–13) (44–257)
*LC50 and LC90 values are in ppm (CL 95%). RR (resistance ratio = LCs field population/LCs susceptible strain.
a
Data did not fit the probit model.
Archives of Insect Biochemistry and PhysiologyResistance in B. tabaci Biotypes 221
Fig. 3. Log concentration-response curves (on a probit another part was selected with acetamiprid and kept un-
scale) for the effect of pyriproxyfen on Bemisia tabaci strain der the same conditions (G-26, Sel). The following bio-
originated from the Ayalon Valley during the late 1999 types were defined in each line: S, susceptible strain = B;
cotton season (AV99L). A part of this strain was main- G-1, the original strain after one generation (F1) in the
tained for 26 generations under standard laboratory con- laboratory = Q, B; G-26, B; G-26, Sel = Q.
ditions without exposure to any insecticides (G-26);
Linkage of Biotypes of Bemisia tabaci with Resistance and Q-type (although Q-type was predominant).
to Pyriproxyfen and Neonicotinoids The untreated strain that lost its resistance to
pyriproxyfen (in generations 20–26) was defined
The strain that originated from the Ayalon Val- as B biotype; the same strain that was selected with
ley 1999 (AV99L) was defined as a mixture of B- acetamiprid was defined as Q-type (in generation
TABLE 2. Susceptibility of Strain of Bemisia tabaci to Pyriproxyfen that was Collected in the Late Season 2002 from the Ayalon Valley of Israel and
Maintained Without Exposure to Insecticides Under Controlled Chamber Conditions*
Generation n Slope ± SEM LC50 LC90 RR50 RR90 Biotype
S-strain 9,308 1.41 ± 0.03 0.04 0.35 1 1 B
(0.03–0.06) (0.23–0.70)
1 1,568 1.57 ± 0.12 15 98 375 280 Q, B
(4–26) (57–298)
3 1,905 1.25 ± 0.09 3 34 75 97 Q, B
(—)a (—)a
6 2,878 0.92 ± 0.05 0.21 5 5 14 B
(0.09–0.37) (3–10)
9 1,193 0.76 ± 0.07 0.21 10 5 29 B
(0.15–0.29) (6–23)
12 1,927 0.71 ± 0.05 0.20 13 5 37 B
(0.01–0.68) (—)a
15 1,118 0.60 ± 0.05 0.11 15 3 43 B
(0.001–0.61) (—)a
18 1,502 1.04 ± 0.07 0.11 2 3 6 B
(0.05–0.20) (1–5)
21 2,764 0.99 ± 0.05 0.11 2 3 6 B
(0.06–0.18) (1–5)
*LC50 and LC90 values are in ppm (CL 95%). RR (resistance ratio) = LCs field population/LCs susceptible strain.
a
Data did not fit the probit model.
April 2005222 Horowitz et al.
Fig. 4. Log concentration-response curves (on a probit with neonicotinoids, one with acetamiprid (Msp) and the
scale) for the effect of pyriproxyfen on Bemisia tabaci strain second with thiamethoxam (Act), and kept under the same
that originated from the Ayalon Valley during the late 2002 conditions. The following biotypes were defined in each
cotton season (AV02L). A part of this strain was main- line: S, susceptible strain = B; G-1, the original strain after
tained for 21 generations under standard laboratory con- one generation (F1) in the laboratory = Q, B; Unt = B;
ditions without exposure to any insecticides (Unt); two Msp = Q; Act = Q.
other parts of this strain were selected for 21 generations
26). We were not aware of the second biotype in 2003 season, which were found susceptible to
Israel until late 2000 (Horowitz et al., 2003); pyriproxyfen and defined as B-type (Table 1).
hence, none of the previous generations had been
examined for biotype status. In the AV02L strain, DISCUSSION
the biotype of every third generation was defined
along with its resistance situation. Table 2 demon- The resistance situation to pyriproxyfen in B.
strates the biotype status of the untreated line of tabaci has been reported extensively in Israel
AV02L strain in each third generation along with (Horowitz and Ishaaya, 1994; Horowitz et al.,
its toxicity data. Accordingly, in the first and third 1999, 2002). In 1996–1997, the use of this insec-
generations a mixture of B- and Q-type was noted, ticide ceased in areas such as the Ayalon Valley and
but from generation 6 to 21, all the B. tabaci indi- the Carmel Coast; however, levels of resistance to
viduals tested were defined as B. Figure 3 illustrates pyriproxyfen have remained high in those areas,
the situation of each strain in the 21st generation, despite some degree of decline. In other cotton ar-
where the first generation was defined as a mix- eas in Israel, pyriproxyfen is still in use and effec-
ture of B and Q biotypes and was highly resistant tively controls whitefly (Horowitz et al., 2002). In
to pyriproxyfen. As with AV99L, the two strains that a recent study, Horowitz et al. (2003) demonstrated
had been selected separately with either neo- an empiric relationship between resistance to
nicotinoids stayed resistant to pyriproxyfen and pyriproxyfen and the presence of biotype Q; in ar-
were defined as Q-types. eas where resistance to pyriproxyfen rapidly evolved,
Table 1 summarizes resistance monitoring data the Q-type was predominant. Similarly, Q biotype
in B. tabaci populations collected from 1999 to was linked with high resistance and cross-resistance
2003 in the Carmel Coast (NW Israel) together to neonicotinoids in southern Spain (Nauen et al.,
with their biotype status. Bemisia tabaci populations 2002; Rauch and Nauen, 2003). Guirao et al.
collected from the Carmel Coast were defined ex- (1997) determined the status and distribution of
clusively as Q-type, except for those early in the Spanish populations of B. tabaci B-type and non-B
Archives of Insect Biochemistry and PhysiologyResistance in B. tabaci Biotypes 223
(=”Q”). After a few years, the Q-type almost dis- on our data, applications of these insecticides may
placed the B-type, especially in southern Spain select for biotype Q, which would survive to a
(Simón et al., 1999), probably because of the in- greater degree where treatments of either pyri-
creased use of neonicotinoids against whiteflies. proxyfen or neonicotinoids were applied.
Although resistance to pyriproxyfen in some cot- Although some beneficial characteristics have
ton areas in Israel did not decline substantially (Fig. been associated with Q biotype from Spain (e.g.,
2; Table 1), our laboratory studies clearly showed Moñiz, 2000; Moñiz and Nombela, 2001), the fit-
that under controlled conditions, without exposure ness of both biotypes in the field is unknown;
to insecticides, susceptibility to pyriproxyfen was hence, in-depth study is needed on this issue. We
fully restored (Figs. 3, 4; Table 2). We relate this expect that a mixture of B and Q biotypes exists in
decline in resistance to pyriproxyfen to replacement the fields and that B-type may survive better than
of Q biotype by B-type under the above conditions. Q-type under untreated conditions. However, ap-
We hypothesize that B biotype of B. tabaci is more plications of particular insecticides encourage Q-
competitive and may exhibit higher fitness than type and depress B-type. Accordingly, early in the
the Q-type where non-insecticide regimes are season (spring), prior to application of insecticides,
implemented (and this may also explain the broad B-types apparently would be predominant until
global distribution of the B biotype). Our results treatments with the above-mentioned insecticides
are at variance with the findings of Moñiz (2000) occurred. This may explain our findings in the early
and Moñiz and Nombela (2001) who stated in gen- cotton season 2003, in the Carmel Coast (Table
eral that the reproductive capacity (e.g., develop- 1) where a B-type was recognized along with a high
mental rate, duration of generation) of B. tabaci Q susceptibility of a field of B. tabaci population to
biotype on some common weeds and sweet pep- pyriproxyfen. Although no Q-type was sampled
per is greater than B-type. On the other hand, a from this location at this time, we assume that a
more recent study (Pascual and Callejas, 2004) in- small portion of this biotype had existed in the
dicated a higher reproductive potential of biotype field. It is possible that the B-type was established
B populations, grown on tomato plants under labo- in the early season prior to insecticide applications.
ratory conditions, as compared with biotype Q. A Thereafter, during the mid-2003 season, three treat-
higher mortality of females and immatures of Q ments (two with acetamiprid and one with dia-
biotype along with a lower fecundity and progeny fenthiuron) were applied in this field, resulting in
size, as compared with B-type, may explain the a change in the biotype status (Q-type) accompa-
competition advantage of the latter on tomatoes nied by resistance to pyriproxyfen (although no
(Pascual and Callejas, 2004). pyriproxyfen treatment had been applied in this
Our laboratory data showed that resistance to area since 1997). In the early 2004 season (June)
pyriproxyfen did not decrease when various neo- after a period of time with a very low level of white-
nicotinoids (acetamiprid and thiamethoxam) were flies, no insecticide treatments against them were
applied serially (Figs. 3, 4). The stability of pyriproxy- applied; a recent survey conducted in this area in-
fen resistance that was reported from cotton fields dicated a mixture of B and Q types (ARH, unpub-
in Israel (Horowitz et al., 2002) probably resulted lished data).
from the use of neonicotinoids as demonstrated Some questions are still open. How does the
by our laboratory studies. One possible explana- competition between the two biotypes occur and
tion could be cross-resistance between pyriproxyfen how does the B-type take over the Q-type (with-
and neonicotinoids. But according to Ishaaya et al. out exposure to insecticides)? Which traits would
(2005, this issue), no appreciable cross-resistance encourage B-type to yield advantage to Q-type?
was observed between the two types of insecticides. Does a resistant strain of Q biotype “suffer” from
There are more decisive effects of both pyriproxyfen fitness costs because of the resistance? Also, how
and neonicotinoids on biotype B than Q. Based does the slight inbreeding between both biotypes
April 2005224 Horowitz et al.
enable the heterozygous progeny to survive in the global tracking of whitefly vector: Begomovirus complexes.
field? Furthermore, the long and short migration Virus Res 71:233–260.
and dispersion of each biotype are unknown. Brown JK, Frohlich DR, Rosell RC. 1995. The sweet-potato
In spite of these unsolved issues, we can sur- or silverleaf whiteflies: biotypes of Bemisia tabaci or a spe-
mise the following scenario: appearance of Q bio- cies complex. Annu Rev Entomol 40:511–534.
type accompanies resistance to pyriproxyfen and/
or neonicotinoids. When the farmer treats the field Brown JK, Perring TM, Cooper AD, Bedford ID, Markham
PG. 2000. Genetic analysis of Bemisia (Hemiptera: Aley-
with insecticides in accordance with IRM programs,
rodidae) populations by Isoelectric Focusing Electrophore-
he moderates selection for resistance to the new in-
sis. Biochem Genet 38:13–25.
secticides and simultaneously restricts the appear-
ance of the Q-type. Reuse of the above-mentioned Cervera MT, Cabezas JA, Simon B, Martinez-Zapater M, Beitia
insecticides against B. tabaci may increase the oc- F, Cenis JL. 2000. Genetic relationships among biotypes
currence of the Q-type and the development of re- of Bemisia tabaci (Hemiptera:Aleyrodidae) based on AFLP
sistance to one or another group of insecticides. This analysis. Bull Entomol Res 90:391–396.
does not mean that selection to insecticides in B Costa HS, Brown JK. 1991. Variation in biological character-
biotype of B. tabaci is impossible (e.g., Li et al., istics and in esterase patterns among populations of
2003), but it is probably slower than in the Q type. Bemisia tabaci Genn. and the association of one popula-
tion with silverleaf symptom development. Entomol Exp
ACKNOWLEDGMENTS Appl 61:211–219.
Costa HS, Brown JK, Sivasupramaniam S, Bird J. 1993. Re-
We thank Janis Joseph (Agricultural Research
gional distribution, insecticide resistance, and reciprocal
Organization, Gilat Research Center, Israel) for her
crosses between the A and B biotypes of Bemisia tabaci.
valuable editing of the paper, and Sophia Kleitman Insect Sci Appl 14:255–266.
and Mario Rippa for their technical assistance. The
authors gratefully acknowledge the Chief Scientist De Barro PJ, Hart PJ. 2000. Mating interactions between two
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