BIOLOGICAL CONTROL

Hymenopterous Parasitoids of Leaf-Mining Liriomyza Spp.

(Diptera: Agromyzidae) on Tomato in Florida
D. J. SCHUSTER AND R. A. WHARTON!
Gulf Coast Research and Education Center, Institute of Food and Agricultural Sciences,
University of Florida, Bradenton, FL 34203

Environ. Entomol. 22(5): 1188-1191 (1993)

ABSTRACT Leaf-mining Liriomyza spp. and their associated hymenopterous parasitoids

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were surveyed during the fall of 1980 and spring of 1981 on fresh market tomatoes in
west-central Florida. L. sativae Blanchard was more abundant than L. tnfolii (Burgess) in
both seasons, accounting for 85.7 and 54.3% of the total reared in 1980 and 1981, respec-
tively. The parasitoids Diglyphus intermedius (Girault), D. begini (Ashmead), and
Neochrysocharis punctiventris (Crawford) were the most abundant larval parasitoids
reared from leafminer-infested foliage, accounting for 28.8, 26.3, and 15.6%, respectively.
D. begini was not detected in 1980, but was nearly as abundant as D. intermedius in 198!.
Opius dissitus (Muesebeck) was the most abundant larval-pupal parasitoid reared from
leafminer-infested foliage, accounting for 51.8 and 12.6% of the total parasitoids reared in
1980 and 1981, respectively.

KEY WORDS Liriomyza, biological control, pest management

Liriomyza trifolii (Burgess) and L. sativae Materials and Methods

Blanchard are the two most damaging species of
agromyzid leafminers on tomato in Florida. Both
are considered to be secondary pests because
populations have been observed to increase as
hymenopterous parasitoid populations have de-
creased after applications of broad-spectrum in-
secticides (Oatman & Kennedy 1976, Trumble &
Toscano 1983). Johnson & Hara (1987) summa-
rized the literature concerning the hymenop-
terous parasitoids reared from Liriomyza spp.
on several crops including tomato. The most
abundant parasitoids reared from leafminers
on tomato varied by location and included
Chrysocharis oscinidis (=parksi) Ashmead, Di-
glyphus begini (Ashmead), D. intermedius (Gi-
rault) , D. pulchripes (Crawford), Neochryso-
charis (=Chrysonotomyia) formosa (Westwood),
and N. punctiventris (Crawford) in the family
Eulophidae and Opius dimidiatus (Ashmead) in
the family Braconidae. The most abundant para-
sitoids reared from infested foliar samples in in-
secticide evaluation plots in Florida were D. in-
termedius, N. formosa, and N. punctiventris
(Poe et a1. 1978, Schuster et a1. 1979, Schuster &
Price 1985).
The objective of the investigation reported
here was to determine the hymenopterous para-
sitoids associated with leaf-mining Liriomyza
spp. on nonsprayed tomatoes in west-central
Florida.
1 Department of Entomology, Texas A&M University, Col-
lege Station, TX 77843.
The study was conducted during the fall pro-
duction season of 1980 and the spring production
season of 1981 on O.4-ha fields at the Gulf Coast
Research and Education Center. Transplants of
'Walter' fresh market tomatoes were set 9 Sep-
tember and 20 February on beds (20.3 em high
by 0.9 m wide) of EauGallie fine sand mulched
with polyethylene plastic film.
Approximately 3 wk after transplanting, the
fields were divided into 15 equal sections, and
one plant was selected twice weekly from each
of at least five sections selected at random. At
each sampling, all leaflets containing occupied
leafmines were excised, placed into O.9-liter
Fonda cardboard containers (The Fonda Group,
Union, NJ), and held in a laboratory for leafminer
and parasitoid adult emergence. These condi-
tions were similar to those of Larew (1989), who
found that emergence of leafminers from de-
tached chrysanthemum leaves was comparable
with emergence from undetached leaves if first
instars were present and if the foliage was held at
room temperature and high relative humidity
(about 80%). When all adults had emerged, they
were removed, counted, and identified. Sam-
pling continued for =7 wk in 1980 and 8 wk in
1981.
Leafminers were identified on the basis of
external characters (Spencer 1973), although a
small percentage (2%) of adults could not be
identified using them. Parasitoid specimens,
with the exception of Braconidae, were identi-

0046-225X/93/1188-1191$02.00/0 © 1993 Entomological Society of America

October 1993 SCHUSTER & WHARTON: PARASITOIDS OF LEAF MINERS ON TOMATO 1189

Table I. Number (%) of adull agromyzid leafminers and their hymenopterous parasitoids reared from tomato foliage
in west-central Florida

Family and species Fall 1980 Spring 1981 Total

Leafminers
Agromyzidae
Liriomyza sativae Blanchard 721 (85.7) 960 (54.3) 1,681 (64.4)
L. tri£olii (Burgess) 120 (14.3) 808 (45.7) 928 (35.6)
Parasitoi s
Braconidae
Opius dissitus (Muesebeck) 351 (51.8) 508 (12.6) 859 (18.2)
O. broneipes Gahan 6 (0.9) 40 (1.0) 46 (1.0)
O. dimidiatus (Ashmead) 6 (0.9) 24 (0.6) 30 (0.6)
Opius, undescribed species 1 (O.l) 0 (0) 1 «0.1)
Cynipidae

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Cothonaspis sp. 0 (0) 1 «0.1) 1 «0.1)
Eulophidae
Chrysocharis majariana (Girault) 19 (2.8) 1 «0.1) 20 (0.4)
C. oscinidis Ashmead 18 (2.7) 29 (0.7) 47 (1.0)
Diaulinopsis callichmma Crawford 35 (5.2) 129 (3.2) 164 (3.5)
Diglyphus intennedius (Girault) 66 (9.7) 1,291 (32.0) 1,357 (28.8)
D. begini (Ashmead) 0 (0) 1,236 (30.6) 1,236 (26.2)
Diglyphus sp. 1 (0.1) II (0.3) 12 (0.3)
Neochrysocharis punctiventris (Crawford) 135 (19.9) 600 (14.9) 735 (15.6)
Pnigalio maculipes (Crawford) 14 (2.1) 6 (0.1) 20 (0.4)
Zagrammosoma multilineatum (Ashmead) 2 (0.3) II (0.3) 13 (0.3)
Pteromalidae
Halticoptera circulus (Walker) 23 (3.4) 152 (3.8) 175 (3.7)

fied using a key constructed by Carl Yoshimoto
(Biosystematic Research Centre, Agriculture
Canada, Ottawa, Ontario, Canada) after review-
ing representative specimens. After identifica-
tions were made, selected specimens of each
species were forwarded to Yoshimoto and John
LaSalle (CAB International, International Insti-
tute of Entomology, London, United Kingdom)
for confirmation of identifications. Braconid
specimens were identified by R.A.W. Voucher
specimens of the leafminers and parasitoids are
being held at the Florida Department of Agricul-
ture and Consumer Services, Florida State Col-
lection of Arthropods, Gainesville, FL.
Results and Discussion
More Liriomyza leafminers and their parasi-
toids were reared in the spring of 1981 than in
the fall of 1980 (Table 1). Differences between
the sampling periods most likely are seasonal
rather than annual. Similar differences between
the spring and fall were observed with leafminer
larvae in weed foliage (Schuster et al. 1991).
There were more L. sativae than L. trifolii in
both seasons. L. tnfoUi was present in low num-
bers throughout the season in 1980 (Fig. la), but
peaked early in the season in 1981 (Fig. 2a). L.
sativae peaked later in the 1981 season (Fig. 2a).
Adults of 14 species of hymenopterous paras i-
toids were reared from leafminer-infested tomato
foliage (Table 1). The larva-pupal parasitoid
Opius dissitus (Muesebeck) accounted for 51.8%
of reared parasitoid adults in 1980. Numbers of
adults peaked late in the season (Fig. Ib). In
1981 the species was not as numerous prop or-
tionally as it was in 1980 (Table 1), but was
present in relatively high numbers from mid- to
late season (Fig. 2c). O. dissitus accounted for
38% of the parasitoid adults reared from weed
foliage infested with agromyzid leafminers in
Florida (Schuster et al. 1991).
The larval parasitoids in the genera Diglyphus
and Neochrysocharis accounted for 62.8 and
14.9%, respectively, of the total parasitoid adults
reared in 1981 (Table 1). More N. punctiventris
were reared than Diglyphus spp. in 1980, but not
in 1981. It was present in low numbers through-
out the season in 1980 (Fig. Ib), but was more
abundant in 1981, peaking from mid- to late sea-
son (Fig. 2c).
D. begini did not occur in 1980, but repre-
sented 30.6% of the adults reared in 1981. D.
intermedius was more numerous early in the sea-
son, whereas D. begini was more numerous later
in the season (Fig. 2b). This corresponded to
similar fluctuations in densities of L. trifolii and
L. sativae in 1981 (Fig. 2a).
This study documents 14 species of paras ito ids
attacking Liriomyza spp. on nons prayed tomato
in Florida. All of the species, with the exeption
of Pnigalio maculipes (Crawford), had been re-
ported previously from leaf-mining Liriomyza
spp. (Minkenberg & van Lenteren 1986, Johnson
& Hara 1987). Only four species were abundant
in the study reported here. Of these, D. interme-
dius, D. begini, and N. punctiventris are larval
parasitoids that complete their development on
leafrniner larvae in the leafmines. The larval-
pupal parasitoid O. dissitus deposits eggs in leaf-
miner larvae in the leaves, but parasitoid larvae
1190 ENVIRONMENTAL ENTOMOLOGY Vol. 22, no. 5

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ao
Fig. 1. Average number ± SE of adults reared from
tomato foliage in Florida in 1980. (a) Liriomyza spe-
60
cies. (b) Parasitoid species.

40

do not complete their development until the

leafminer larvae have exited leaves and pupated.
D. intermedius was the most abundant parasi-
toid recovered from leafminer-infested tomato
foliage in this study (28.5%) and in previous in-
secticide evaluation plots in tomato in Florida
(Poe et al. 1978, Schuster et al. 1979, Schuster &
Price 1985). D. begini was almost as abundant in
this study (26.0%) as D. intermedius. It had not
been reported in the earlier studies, but was re-
covered from foliar weed samples infested with
Liriomyza spp. at an incidence of twice that of
D. intermedius (Schuster et al. 1991). It is doubt-
ful whether insecticides were responsible for the
lack of D. begini in previous studies in Florida,
because this species was the most abundant par-
asitoid recovered in similar trials on tomato in
California (Oatman & Kennedy 1976, Johnson et
aI. 1980). Because D. begini tends to be more
abundant when L. sativae is abundant (Johnson
& Hara 1987; this study), it is possible that D.
begini has a preference for L. sativae. However,
it was not observed in tomato in Florida when L.
20
o
3/16 3/26 4/6 4/16 4/27 5/7
Date
Fig. 2. Average number ± SE of leafminer and
parasitoid adults reared from tomato foliage in Florida
in 1981. (a) Liriomyza species. (b) Diglyphus parasitoid
species. (c) Neochrysocharis and Opius parasitoid spe-
cies.
sativae was present in 1975 and 1977 (Poe et al.
1978, Schuster et al. 1979) and was nearly as
abundant as D. intermedius on celery when L.
trifolii was most abundant (Trumble & Nakaki-
hara 1983). LaSalle & Parrella (1991) suggested
that D. begini is more abundant in Canada and
the western United States than in the remainder
of the Nearctic Region. Whether the present data
suggest an increase in importance of this species
in Florida is not known.
October 1993 SCHUSTER & WHARTON: PARASITOIDS
The Opius spp. observed in previous studies
on tomato in Florida were not documented (Poe
et al. 1978, Schuster et al. 1979, Schuster & Price
1985); therefore, no comparison of species com-
plex in this genus can be made. However, O.
dissitus was the most abundant species in the
genus recovered from tomato in this study
(18.9% of all parasitoid species) and from weeds
in Florida (Schuster et al. 1991).
N. punctiventris was the fourth most common
parasitoid recovered in this study (15.5%), but
was the second most abundant parasitoid recov-
ered in an insecticide trial in 1979 (Schuster et
al. 1985). This species was not reported from
insecticide trials in 1975 and 1977 (Poe et al.
1978, Schuster et al. 1979), when N. formosa was
the second most abundant parasitoid reported.
Information regarding which species are abun-
dant in any given situation is important in mak-
ing pest management decisions because the par-
asitoids may respond differently to different
insecticides (Schuster & Price 1985). The pres-
ence of larval parasitoids as later instars or pupae
can be detected by careful examination of ex-
cised leaflets with a hand lens. The larval-pupal
parasitoids cannot be detected readily as larvae
or pupae because these life stages are not visible
in the puparia. Collecting puparia in styrofoam
trays (Johnson et al. 1980) and holding them for
leafminer and parasitoid emergence could pro-
vide information on the relative abundance of
both the leafminers and the larval-pupal paras i-
toids for future management decisions.
Acknowledgments
We thank Gordon Decou, Brian Cotterill, RickKelly,
and Jene Johnson for collecting the samples and sepa-
rating the specimens and Ann Newsome for assistance
in identifying the specimens. We also are indebted to
Carl Yoshimoto(BiosystematicResearch Centre, Agri-
culture Canada, Ottawa, Ontario, Canada) and John
LaSalle (CAB International, International Institute of
Entomology, London, United Kingdom)for their assis-
tance in confirming identifications of the Eulophidae.
This is Florida Agricultural Experiment Station Jour-
nal Series No. R-02848.
References Cited
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OF LEAFMINERS ON TOMATO 1191
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Received for publication 7 December 1992; ac-
cepted 2 June 1993.