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Effects of Insecticides on Populations of the vegetable leafminer and

Associated Parasites on Fall Pole Tomatoes

Article  in  Journal of Economic Entomology · February 1980

DOI: 10.1093/jee/73.1.67

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 Effects of Insecticides on Populations of the vegetable leafminer1 and
Associated Parasites on Fall Pole Tomatoes2
M. W. JOHNSON:!, E. R. OATMAN, AND J. A. WYMAN4
Dept. of Entomology, Univ. of California 92521
ABSTRACT

J. Econ. Enlomol. 73: 67-71 (1980)

Several insecticides that control lepidopterous pests were evaluated for their effects on
populations of Liriomyza sativae Blanchard and associated parasites in fall plantings of fresh
market tomatoes in southern California. All rates of methomyl tested caused increases in L.
sativae densities and reduced populations of 2 of its principal larval parasites, Diglyphus
begini (Ashmead) and Chrysonotomyia (Achrysocharella) punctiventris (Crawford). Chlor-
pyrifos gave excellent control of the leafminer, but decimated its parasite populations. Par-
asitization of L. sativae by the larval-pupal parasite, Chrysocharis parksi Crawford, was
reduced ca. 40% in plots treated with methomyl at 0.5 kg AI/ha. Dipel® did not adversely
affect either the vegetable leafminer or its parasites.
No significant tomato fruit yield reductions occurred in methomyl-treated plants, although
they had significantly more L. sativae mines than untreated plants.

Downloaded from http://jee.oxfordjournals.org/ at ESA Society Member on October 30, 2016

The vegetable leafminer, Liriomyza sativae Blan-
chard, is a secondary pest on fresh market tomatoes in
southern California. Leaflets may be severely injured by
high densities of the leafminer larvae which primarily
feed in the palisade layer (Oatman and Michelbacher
1958). Repeated applications of the broad spectrum in-
secticide, methomyl, on tomatoes resulted in leafminer
population increases and reduction of natural parasitiza-
tion (Oatman and Kennedy 1976). Prevention of leaf-
miner population increases was achieved by the use of
selective insecticidal materials (ovicides and larvicides)
for control of the primary pest, Heliothis zea (Boddie),
on summer-planted tomatoes (Johnson et aI. 1980).
However, such specific insecticides generally are inef-
fective against Keiferia lycopersicella (Walsingham) and
Spodoptera exigua (Hiibner), the primary pests in fall-
planted tomatoes in southern California.
Significant L. sativae-induced tomato yield reductions
were recorded by Schuster et aI. (1976) in Florida. John-
son et al. (1980) reported significantly higher fruit yields
of summer-grown tomatoes in methomyl-treated plots in
California, although L. sativae mine densities were sig-
nificantly higher than in the untreated check plot. How-
ever, their data showed that larval populations reached
a peak after 55% of the fruit were harvested. Fall-grown
tomatoes in southern California may be subjected to
higher populations of L. sativae than those that develop
in the summer because populations that develop on the
earlier crop may move to the fall crop at an earlier
growth stage. Subsequent yield reductions would thus
be more likely to occur in the fall crop, whereL. sativae
populations normally reach a peak prior to fruit produc-
tion.
Our objectives were to evaluate the effects of insecti-
cides used for lepidopterous pest control on populations
of L. sativae and its parasites and to determine the ef-
fects of L. sativae mine densities on fruit yield of fall-
grown tomatoes.
I Diptera: Agromy.idae.
I R•• eived for publication July 10. 1979.
, Garden City Exp. Sin., Kansas Slate Univ.• Garden City 67846.
• Dept. of Entomology, Univ. of Wisconsin. Madison 53706.
67
©1980 Entomological Society of America
Methods and Materials
Field studies were conducted at the Univ. of Calif.
South Coast Field Station, Irvine. All investigations
were made on poled fresh market tomatoes, Hybrid 6718
VF (Peto Seed Co., Saticoy, CA). Plants were grown,
using local, commercial practices. Insecticide treatments
were applied by a tractor-mounted boom sprayer (10
nozzles/row) operated at 58.6 kg/cm2, delivering 420 li-
ters water/ha.
Leaflets (7-13 cm long) were randomly sampled from
the inner sides of double-row plots in 1976 and 1977 and
from both sides of each row in 1978. Samples were
taken to the laboratory, examined, and placed in emer-
gence containers (Johnson et al. 1980).
The parasites reared from L. sativae were identified
by Dr. Gordon Gordh, Dept. of Entomology, Univ. of
Calif. Riverside, and by Dr. Carr Yoshimoto, Can. For-
estry Service, Dept. of the Environment, Ottawa, Can-
ada. L. sativae identifications were confirmed by K. A.
Spencer, London, England.
Data were analyzed by an analysis of variance on
transformed data. Mean separations were made by Dun-
can's multiple range test (P < 0.05).
Fall 1976
Tomato plants were transplanted on July I into 5, par-
allel, double rows (86 m long, 2.3 m apart). Double
rows were divided into five 12.2-m plots with 1.8-m
buffer spaces on each side. Plots were arranged in a ran-
domized complete block design with 4 replicates. The
following treatments were applied: methomyl (1.0 and
0.5 kg AI/ha); Dipel, Bacillus thuringiensis Berliner
var. kerstaki (0.56 kg AI/ha); and chlorpyrifos (1.12 kg
AI/ha). An untreated check was included. Plots were
sprayed weekly from Sept. 9 to Oct. 21. Twenty-five
leaflets/plot were collected weekly from Sept. 18 to Oct.
24. Numbers of live and externally parasitized (parasite
larvae or pupae in a mine) L. sativae larvae were re-
corded for each plot. After examination, leaflets were
held in emergence containers for 3 wk, then emerged
insects were identified.
0022-0493/80/0100-6705$00.75/0
68 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 73, no. 1

Fall 1977
Tomato plants were transplanted in early June into
double-row plots (10.7 m long on 2.3-m centers and 1.8-
m buffer zones) replicated 4 times in a randomized com-
plete block design. Methomyl (0.5 kg Altha) and a Di-
pel/methomyl combination (0.56 and 0.25 kg AUha)
were applied weekly from Sept. 2 to Oct. 27. An un-
treated check plot was included. Twenty-five leaflets/
plot were sampled weekly from Sept. 25 to Nov. 6.
Numbers of live and externally parasitized L. sativae
larvae and total number of mines were recorded for each
leaflet. After examination, leaflets were placed in open
bags in emergence containers. After 4 days, emerged L.
sativae pupae were removed, and numbers were re-
corded. After 3 wk, emerged insects were identified and
recorded.
planted on June I into eight 6-row plots (1.5-m centers,
12-m long) separated by 12 m of bare ground. Methomyl
(0.5 kg AUha) was applied weekly to 3 odd-numbered
rows of 4 plots from Aug. 4 to Sept. 22. Remaining
plots served as an untreated check. Forty leaflets were
sampled from the interior methomyl-treated rows and
corresponding rows in untreated plots on Sept. 4, II,
and 20, and the number of L. sativae mines was re-
corded. Mature green tomato fruit were harvested twice
weekly from Aug. 31 to Nov. 10, and weighed to obtain
yields.
Results and Discussion
Fall 1976
Live L. sativae larval densities were significantly
lower in the chlorpyrifos treatment than in the untreated

Downloaded from http://jee.oxfordjournals.org/ at ESA Society Member on October 30, 2016

Between Oct. 2 and Nov. 6, six styrofoam trays
check throughout the study (Table I). The high dosage
(22.9x27.9x 1.6 cm) (Johnson et al. 1980) were placed
methomyl treatment reduced larval densities during Sept.,
beneath plants in each plot on the inner sides of the dou-
but densities later increased and were significantly higher
ble row plots to monitor the numbers of pupating L. sa-
than those in the untreated check on Oct. 9 and 24. The
tivae larvae. After 5 days, the trays were taken to the
low rate of methomyl also increased larval populations
laboratory in separate paper bags. All pupae were re-
as compared to the untreated check late in the season
corded, but only those loose in the bags were placed in
with significant increases on Oct. 16 and 24. Larval
ventilated, 38-ml glass vials and held until emergence of
densities in the Dipel treatment were not significantly
adult leafminers or parasites.
different from the untreated check and were generally
Fall 1978 lower than those in the methomyl treatments.
To evaluate the effects of methomyl-induced L. sati- Externally parasitized (EP) L. sativae larval densities
vae upsets on tomato fruit yield, tomatoes were trans- were lowest in the chlorpyrifos treatment throughout the

Table I.-Mean numbers of live and externally parasitized Liriomyza sativae larvae, and larval parasites, Diglyphus
begini and Chrysonotomyia (Achrysocharella) punctiventris, per leaflet on pole tomatoes treated with various insecticides for
control of lepidopterous larvae, Irvine, CA 1976.

No. of L. sativae and parasites present ona

Rate
Treatment (kg AIlha) Sept. 18 Sept. 25 Oct. 4 Oct. 9 Oct. 16 Oct. 24

Live L. sativae larvaeb

Untreated 0.44a 1.54a l.05b l.63be 0.67b 1.75e
Dipel 0.56 0.50a 1.34ab 1.18b 1.48e I.OOab l.97be
Methomyl 0.50 0.56a 1.36ab 1.42ab 2.28ab 1.58a 2.93a
Methomyl 1.00 0.30a O.80b l.65ab 2.40a 1.15ab 3.36ab
Chlorpyrifos 1.12 O.DOb O.DOc O.DOc 0.02d 0.03e 0.02d

Externally parasitized L. sativae larvaeb

Untreated 0.09b 0.07a O.15be 0.34ab O.44a O.44a
Dipel 0.56 0.09b O.03a O.63a 0.49a 0.42ab O.29ab
Methomyl 0.50 0.16ab 0.09a O.24be 0.23be 0.22be O.13be
Methomyl 1.00 O.06b O.lla 0.16be 0.12ed 0.20ed 0.06c
Chlorpyrifos 1.12 O.04b O.Ola O.DOc 0.0Dd 0.0Dd O.DOc

D. begini
Untreated 0.5Oc l.ooa 2.50b 2.75a 4.00a 5.75a
Dipel 0.56 0.25d 0.25d 4.00a 0.25d 2.25b 5.00b
Methomyl 0.50 l.OOa 0.75b l.DOc 1.50b 1.00c 0.5Oc
Methomyl 1.00 0.75b 0.5Oc O.05d 0.75e 0.25d 0.0Dd
Chlorphyrifos 1.12 0.25d D.OOe O.ODe 0.0De 0.0De 0.0Dd

C. punctiventrisC
Untreated 0.75a O.ooa 4.25a 6.ooa 3.25ab 2.75a
Dipel 0.56 0.75a l.00a 5.25a 5.25a 4.50a 2.50a
Methomyl 0.50 l.ooa 0.50a 5.50a 5.75a 2.50ab O.OOb
Methomyl l.oo O.ooa 0.25a 3.00a 1.50ab 1.25ab O.OOb
Chlopyrifos 1.12 O.ooa O.ooa O.OOa O.OOb O.OOb O.OOb

• Mean separations in vertical columns by Duncan's multiple range test on transformed data P < 0.05
b Numbers per leaflet determined from leaflet examination; transformed (In 10 (x + I).
, Total numbers ream! from foliage samples; transformed (x + 1).
February 1980 JOHNSON ET AL.: L. sativae
Table 2.-Mean total numbers" of Diglyphus intermedius, Chrysocharis parksi, and C. ainsliei reared from Liriomyztl
sativae in pole tomatoes treated with various insecticides for control of lepidopterous larvae at Irvine, CA, 1976 and 1977,
Dipet
Species Untreated (0.56)
1976
D. intermedius 14.00a 9.75ab
C. parksi 5.00a 2.75b
C. ainsliei 4.25a 4.00a
1977
D. intermedius 4.25a
C. parksi 11.25b
C. ainsliei I. SOb
• From 25 leaflets/plol.
• Mean separations in horizontal rows by Duncan's multiple range lest on transfonned data (x
study, being significantly lower than the untreated check
from Oct. 9-24 (Table I). EP larval densities were sig-
nificantly lower in both methomyl treatments than in the
untreated check on the last 2 survey dates. Densities in
the Dipel treatment did not differ significantly from the
untreated check, except on Oct. 4 when they were sig-
nificantly higher.
The larval parasites, Diglyphus begini (Ashmead), D.
intermedius (Girault), and Chrysonotomyia (Achryso-
charella) punctiventris (Crawford), and the larval-pupal
parasites, Chrys,ocharis parksi Crawford, C. ainsliei
Crawford, and Halticoptera sp. were reared from L. sa-
tivae in the foliage samples.
D. begini adults were not obtained from chlorpyrifos-
treated foliage after Sept. 18 (Table 1). Significantly
more D. begini were present in both methomyl treat-
ments as compared to the untreated check on Sept. 18,
but were significantly fewer thereafter. The number of
D, begini reared was significantly higher in the Dipel
treatment than in the other insecticide treatments on Oct.
4, 16, and 24, but was significantly lower than in the
untreated check on every survey date except Oct. 4,
Prior to Oct. 9, there were no significant differences
between the number of C. punctiventris reared from L.
sativae in foliage collected in any treatment, and none
emerged from chlorpyrifos-treated foliage (Table I).
From Oct. 9-24, fewer C. punctiventris were present in
the methomyl treatments than in the untreated check, but
differences were significant only on Oct. 24, Numbers
of C. punctiventris did not differ significantly between
the Dipel treatment and untreated check throughout the
study.
D. intermedius populations were highest in the un-
treated check, and lowest in the chlorpyrifos (Table 2).
The number of C. parksi in the untreated check was not
significantly different from that in the methomyl treat-
ments. There were significantly fewer C. parksi adults
in the Dipel and chlorpyrifos treatments as compared to
the untreated check. The highest number of C. ainsliei
were in the low dosage methomyl treatment, but its
numbers were not significantly different from those in
the untreated check. None were recovered from the
chlorpyrifos-treated plants.
ON FALL TOMATOES 69
Trealmenlsb
(kg Altha)
Melhomyl Methomyl Dipel-methomyl Chlorpyrifos
(0.5) (1.0) (0.56+0.25) (1.12)
6.00abc 3.25bc 0.25c
3.50ab 4.50a O.OOb
6.50a 4.50a O.OOb
2.25a 4.25a
17.75ab 24.50a
4.25ab 8.25a
Downloaded from http://jee.oxfordjournals.org/ at ESA Society Member on October 30, 2016
+ I), P < 0.05.
The data thus show that L. sativae larval densities in-
creased in both methomyl treatments, and that densities
in the Dipel treatments generally were intermediate be-
tween those in the untreated check and methomyl treat-
ments.
The data also show that D. begini and C, punctiventris
were the most numerous parasites reared, occurring al-
most equally in the untreated check. Late in the season,
densities of both parasites were higher in the Dipel treat-
ment than in both methomyl treatments. D. intermedius,
C. parksi, and C. ainsliei populations were almost elim-
inated in the chlorpyrifos treatment, but other treatments
did not reduce them greatly. Similar results were re-
ported for summer-crop tomatoes by Johnson et al.
(1980). The increase in L. sativae populations in meth-
omyl treatments apparently was due primarily to a de-
crease in parasite populations. Dipel did not increase the
L. sativae populations.
Fall 1977
Live L. sativae larval densities were highest in all
treatments on Oct. 2 (Table 3). More larvae were present
in the foliage treated with methomyl and Dipel-metho-
my I than in the untreated check, with significant differ-
ences occurring from Sept. 25 to Oct. 16. There was no
significant difference between Dipel-methomyl and
methomyl.
The number of externally parasitized (EP) L. sativae
larvae was significantly higher in the untreated check
than in the methomyl-treated plots from Sept. 25 through
Oct. 16. Although lower, densities in the Dipel-metho-
my I treatment were not significantly different from the
untreated check on any date and were significantly
higher than in the methomyl treatment on Sept. 25, Oct.
2, and 16.
Densities of L. sativae mines in the Dipel-methomyl
treatment were highest on all dates, except Nov. 6, and
lowest in the untreated check on all dates, except Oct.
16. Except for Oct. 16 and Sept. 6, mines in the meth-
omyl treatment were intermediate between those in the
untreated check and Dipel-methomyl treatment.
The number of D. begini reared from L. sativae larvae
in the foliage was highest in'the untreated check on all
70 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 73, no. J

Table 3.-Mean numbers of live and externally parasitized Liriomyza sativae larvae, leaf mines, and larval parasites,
Diglyphus begini and Chrysonotomyia (Achrysocharella) punctiventris, per leaflet on pole tomatoes treated with methomyl
and Dipel/methomyl combination at Irvine, CA, 1977.

No. of L. sativae larvae, mines, and parasites present ona

Treatment Sept. 25 Oct. 2 Oct. 9 Oct. 16 Oct. 23 Oct. 30 Nov. 6
Live L. sativae larvaeb
Untreated 4.42b 5.92b 2.95b 2.95b 2.50b 3.22a 2.23a
Dipel-methomyl 7.89a 1O.78a 5.29a 3.95a 5.48a 4.40a 4.06a
Methomyl 7.24a 11.24a 5.13a 3.82a 3.68ab 4.29a 4.08a
Externally parasitized L. sativae larvaeb
Untreated 2.46a 1.00a 2.01a 1.18a 0.51a 0.67a 0.53a
Dipel-methomyl 1.79a 1.24a 1.34ab 0.97a 0.48a 0.43a 0.17a
Methomy] 0.51b 0.38b 0.99b 0.46b 0.36a 0.23a 0.22a
L. sativae minesb

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Untreated 16.89a 16.85c ]2.44a 1O.76a 7.93b 8.85b 6.99a
Dipe]-methomyl 22.47a 23.54a 15.75a 13.13a 12.01a 10.56a 8.67a
Methomyl 17.17a 20.06b 13.93a 9.67a 9.27a 9.I3b 9.03a
D. beginiC
Untreated 21.00a 12.508 12.ooa 1O.25a 3.33a 8.ooa 1O.25a
Dipe]-methomy] 15.50b 8.ooa 7.50b 3.50b 3.33a 0.75b 9.75a
Methomy] 5.75c 3.67b 4.50b 1.75b 0.50a 0.75b 9.75a
C. punctiventrisC
Untreated 13.50a 6.ooa 6.75a 3.50a 0.75a 3.25a 2.75a
Dipel-methomyl 9.75ab 7.25a 7.50a 3.75a 2.25a 1.25ab 2.ooa
Methomyl 5.25b 2.75a 3.75a 2.25a 0.75a 0.25b 3.75a
• Meanseparation
invertical
columns byDuncan's
multiple
rangetestontransfonned data.P < 0.05.
b Numbersperleafletdetennioed
fromleafletexamination;
transfonned(In10 (x + 1).
, Totalnumbers
rearedfromfoliagesamples;
transfonned
(x + I).

dates, except on Oct. 23 (Table 3). There were signifi- which emerged was significantly higher in the untreated
cantly less D. begini in the methomyl-treated plots on check than that in the methomyl and Dipel-methomyl
Sept. 25, Oct. 2, 9, 16, and 30 than in the untreated treatments on all survey dates (Table 5). The percentage
check. Populations in the Dipel-methomyl treatment in the Dipel-methomyl treatment was intermediate be-
were higher than those in the methomyl treatment prior tween the untreated check and methomyl treatment and
to Oct. 30. was significantly higher than that in the methomyl treat-
On Sept. 25 and Oct. 30, the number of C. punetiv- ment on Oct. 2 and 30.
enlris reared from L. sativae larvae in the untreated Low numbers of puparia in trays were preyed on by
check were significantly higher than in the methomyl green lacewing larvae, but their loss was minor as only
treatment (Table 3). There was no significant difference fluids were removed by this predator. No other predation
between Dipel-methomyl and untreated check. was observed.
There were no significant differences in D. interme- C. parksi parasitized a large proportion of the L. sa-
dius numbers between treatments (Table 2). Signifi- tivae larvae in the untreated check. Methomyl reduced
cantly more C. parksi and C. ainsliei were present in the parasitization by C. parksi ca. 40% during the survey
Dipel-methomyl treatment than in the untreated check.
Throughout the study, the mean number of L. sativae
pupae per tray was significantly higher in the methomyl Table 4.-Mean number of Liriomyza sativae pupae per
and Dipel-methomyl treatments than in the untreated tray in pole tomatoes treated with methomyl and Dipel.
methomyl combination at Irvine, CA, 1977.
check (Table 4). Of the total number of insects which
emerged from L. sativae pupae, the percentage of L.
Treatments·
sativae adults was significantly lower in the untreated Survey
check than in the methomyl and Dipel-methomyl treat- Date Untreated Dipel-methomyl Methomyl
ments on all survey dates (Table 5). The percentage of
L. sativae emergence in the Dipel-methomyl treatment Oct. 2 26.0b 214.4a 302.7a
Oct. 9 37.4b 216.1a 244.9a
was intermediate between that in the untreated check and Oct. 16 21.2b 143;7a 177.5a
the methomyl treatment, being significantly lower than Oct. 23 12.9b 81.6a 81.0a
in the methomyl treatment on Oct. 2 and 30. Approxi- Oct. 30 9.6b 68.3a 53.7a
mately 95% of the parasites reared from L. sativae pupae Nov. 6 1O.6b 31.7a 25.0a
were C. parksi, the remaining 5% being primarily C. • Meanseparationinborizontal rowsbyDuncan's
multiple
rangetestontrans·
ainsliei and Halticoptera sp. The percentage ofC. parksi fonneddata(In10 (x = J) ), P < 0.05.
 February 1980 JOHNSON ET AL.: L. sativae ON FALL TOMATOES 71

Table 5.-Mean percentages· of Liriomyza sativae and dates (Sept. 4, 11 and 20), being significantly lower on
Chrysocharis parksi which emerged from L. sativae pupae Sept. 4 and 20. Although total fruit yield was lower in
collected in pole tomatoes treated with methomyl and Di· the methomyl treatment (140.2 kg/plot), it was not sig-
pel-methomyl combination at Irvine, CA, 1977.
nificantly different from that in the untreated check
(150.6 kg/plot). These data thus showed that in southern
Collection dates
California, densities of L. sativae mines (up to 29.5/lea-
Treatments Oct. 2 Oct. 9 Ocl. 23 Ocl. 30 flet) did not significantly reduce fruit yield in fall-grown
tomatoes.
L. sativae
Overall, the data show that, as in summer-planted to-
Untreated 6.Oc 12.5b 4.7b 7.2c
42.0b matoes (Johnson et al. 1980), the use of methomyl for
Dipel-methomyl 42.0a 32.0a 31.2b
Methomyl 62.2a 51.7a 43.7a 61.0a control of lepidopterous larval pests resulted in higher
populations of L. sativae and lower populations of its
C. parksi
principal parasites but that these increases did not result
Untreated 88.7a 79.7a 92.5a 88.5a
Dipel-methomyl 55.2b 54.2b 65.5b 69.5b in significantly lower fruit yield.
Methomyl 33.5c 45.0b 55.5b 38.5c

• Mean separation in verticoJ columns by Duncan's multiple range test. P < 0.05;

Downloaded from http://jee.oxfordjournals.org/ at ESA Society Member on October 30, 2016

Ocl. 6 and Noy. 6 not included due to missing data.
period. The low rate of methomyl combined with Dipel
resulted in a 26% reduction. However, this decrease
caused significantly higher L. sativae densities. Thus,
the use of methomyl, even at reduced rates in combina-
tion with Dipel, did not prevent increases in L. sativae
populations.
Fall 1978
L. sativae mine densities were lower in the untreated
check than in the methomyl treetment on all 3 sample
REFERENCES CITED
Johnson, M. W., E. R. Oatman, and J. A. Wyman. 1980.
Effects of insecticides on populations of the vegetable
leafminer and associated parasites on summer pole toma-
toes. J. Econ. Entomol. 73: 61-6.
Oatman, E. R., and G. G. Kennedy. 1976. Methomyl in-
duced outbreak of Liriomyza sativae on tomato. Ibid. 69:
667-8.
Oatman, E. R., and A. E. Michelbacher. 1958. The melon
leaf miner, Liriomyza pictella (Thomson) (Diptera: Agro-
myzidae). Ann. Entomol. Soc. Am. 51: 557-66.
Schuster, D. J., J. P. Jones, and P. H. Everett. 1976. Effect
of leafminer control on tomato yield. Proc. Fla. State Hor-
tic. Soc. 89: ]54-6.

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