tk300012~9 TROPICAL PEST MANAGEMENT, 1987, X(4),...
tk300012~9
TROPICAL PEST MANAGEMENT, 1987, X(4), 290-297
Introduction of exotic parasitic wasps for the control of Liriomyza trifo/ii
(Dipt., Agromyzidae) in Senegal
,_ .”
*A.”
Keywords: Brologrcal control. Lrriomyza trlfoh, Senegal
I >’ .
P. NE.UENSCHWANDER, S. T. MURPHY* and E. V. COLY**
Dept. of Phytomedicine, Swiss Federal Institute of Technology, Zürich, Switzerland, consultant with the Food and
Agri;culture Organization (FAO), Rome, Italy.
Present address: fnternationai Institute of Tropical Agriculture, Ibadan, Nigeria.
* CAB International fnstitute of Biologicaf Controf (CIBC), West Indian Station, Curepe, Trinidad, W.I.
Present address: CIBC Kenya Station, Nairobi, Kenya.
** Centre pour le Développement de /‘Horticulture (CDH), Cambérène, Sénégal.
Abstract. Linornyza tr~fol~~ Burgess had frrst been reported from
Israel, Japan. the Philippines, and some Pacifie Islands (CIE
Senegal In 1980. Freld surveys In 1982 revealed its presence in
map 450, 1984).
ail vegetable growing areas of the country, heaviest damage
In America, L. frifofii and other Liriomyza spp. have
berng regrstered in the Cap Vert. Five indrgenous eulophrds (lar-
become major pests because of insecticide misuse. The
val parasrtords) plus five other rare parasitoids, frequently parasr-
mines of the larvae and feeding punctures by the adult
trred ever 90?:0 of the flres. These rates were higher in insectrcrde
free frelds. and very much above the 30-40% reported for 1981.
flies often lead to severe defoliation. However, under natu-
The rnost important parasitords were Hemrptarsensus semialbrc-
ral conditions most species are reasonably well control-
lave (Grrault), whrch dominated in the second half of the dry
led by their parasitoid complex (Spencer, 1973; Parrella
seasoh. and two Chrysonotomy\\a spp., which were more abund-
and Keil, 1984), whrch has been recently reviewed
ant rn the rarny season Surveys for exotrc parasitoids mdicated
(Murphy, 1984). Parasitotds of Lrriomyza spp. have been
B;e~f;rrpps~s ca///cnroma Crawford from Trrnidad to be a promis-
mg Especres for mtrodLrction in the New World. This parasitoid,
studied in order to develop integrated control (Stegmaier,
together wrth etght other chalcrdords (mostly larval parasitoids)
1972; Johnson et a/., 1980; Allen and Charlton, 1981). Bio-
and two braconrds (larval-pupal parasrtoids), were collected in
logical control of indrgenous agromyzid leafminers has
the 0eld OI recetved from estahlished insectary cultures. They
also received much attention in European glasshouse
were :studred and shrpped for reanng and release in Senegal.
cultures (Hendrikse et a/., 1980. Woets and van der Lin-
Nrne species were released at the end of 1982 and in 1983. Many
were ,*ecovered shortly after release, but only Op~us dissitus
den, 1982). Recently, these studres have been extended to
Muesebeck was recovered In later samples and became relativ-
the exotic L. frifofii (J. P. Lyon, pers. Comm.).
eiy nbundant.
There have been two classical biological control
attempts against Liriomyza spp., where natural enemies
trom the original home of an accidentally introduced pest
were transferred for permanent establishment in the field.
Introduction
These were limited to Hawaii, where both L. trifolii and L.
sativae were controlled on vegetable crops by exotic
In Senegal a large scale attack by an agromyzrd leafmi-
parasitoids introduced from the southern’U.S.A. and Cen-
ner, later rdentrfied as Linomyza trifofii Burgess, was
tral America (Lai, 1983) and to the Republic of South
reported from the Cap Vert region near Dakar in Decem-
Africa where attempts are presently being made to control
ber, 1980 By Aprrl 1981, severe damage had occurred,
L. trifolii on Chrysanfhemum spp. and tomatoes using
marnly on the African vegetables diakhatou (Solarium
Neotropical parasitoids (H. van Hamburg. pers. comm.).
aefkiopicom) and okhra (-gombo) (Hibiscus esculenfus),
A biological control project, funded by FAO, was con-
and on potatoes. Parasitization rates by indigenous eulo-
ducted at the CDH in Senegal, where the first studies on L.
phrds were low (Bourdouxhe, 1982).
trifofii had been done. Parasitoids of L. trifolii on vegetab-
The crnsumed origan of this fly (untrl recently confused
les were to be introduced from the New World into Sene-
with L. xr:ivae Blanchard) is in America, especially Florida
gal in collaboration with the CIBC West Indian Station.
and the Carribean (Spencer, 1973). The fly had been intro-
Given the short duration of this pilot project, only Trinidad
duced accidentally rnto Kenya on Chrysanthemum sp.
and a few other areas in the Americas could be searched.
cuttings around 1970. Later it reached the Canary Islcnds,
Cther parasitoids were received from established insec-
Malta. southern France, and commercial greenhouses in
tary cultures in the U.S.A. Meanwhile, in Senegal, insec-
central and northern Europe (D’Aguilar and Martinez,
tary facilities were constructed, and the extent of L. trifolii
1979). In 1978 it was first reported from Mauritius and
distribution and the abundance of indigenous parsitoids
Réunion,$where it did damage to a wide range of tropical
of this exotic host were evaluated. The present text descn-
garden çrops (Vercambre, 1980). In addition to the
bes the first results and reports on releases of exotic par-
countries mentioned. L. trifolri also occurs in South Africa,
sitoids and first recoveries.
Biological control of Liriomyza trifolii in Senegal
291
Materials and methods
cowpea leaves were taken at random from the respective
bags. All dipterous leafminers and their parasitoids were
Field surveys in Senegal
counted.
From July 1982 to July 1983, frequent surveys for L.
Two short collecting trips were made in late April/early
trifolii and its parasitoids were conducted in the Cap Vert
May 1983 to the Cauca Valley, Colombia, and in late May
region of Senegal, while other areas were searched only
to the Rio Grande Valley, Texas, U.S.A. Besides the CIBC
occaslonally. Mean rainfail at the Cap Vert during the last
surveys, collections of Liriomyza spp. parasitoids were
30 years was 518mm per year, but has recently dropped
made by the University of Florida, Homestead, in southern
to about 400mm (De Lannoy, 1982). The rainy season
Florida, and by the State Department of Agriculture,
lasts from June to October with the heaviest rains in
Hawaii, and sent to the CIBC West Indian Station for qua-
August-September. The long dry season is marked by low
rantine. Additional parasitoids were supplied from exist-
temperatures in January (mean minimum around 17“C)
ing cultures at the University of California, Berkeley and
and high temperatures in August-September-October
Riverside.
(mean maximum around 33°C). From November to March
Samples of all dipterous leafminers and their parasi-
a northeastern wind (‘harmattan’) sometimes lowers rela-
toids from the surveys in America and Africa were sent to
tive hurnidity to below 20%.
the CAB International Institute of Entomology (CIE) in
The Cap Vert is the main vegetable growing area of the
London for identification and comment.
country. Vegetables are grown mostly in fertile valleys
(‘niayes’) between the coastal dunes at sea level. They are
trrigated throughout the dry season by hand with water
from wells. The main vegetables grown are potatoes,
Rearing and Me-history studies of L. trifolii and
tomatoes and other Solanaceae, various beans, cabbages
exotic parasitoids
and leafy vegetables, all of which are hosts of L. trifolii.
Cultures of L. trifolii were maintained in Trinidad and
Infestation by L. trifolii varied very much from field to
Senegal. In Senegal, various plants (but mainly tomatoes
field. In each plot it was short lived, and sampling was
and beans) were grown in an insect-proof screenhouse.
often Interrupted by leaf fall or harvest. It was therefore not
They were then placed in a screened room of several m3
possible during the short period of the project to develop
where the leaves were stung by the flies. When leafmines
proper quantitative sampling plans for the different sub-
had reached the stage required by the parasitoids, the
strates. Wherever living infestations were highest, leaves
potted plants were placed in screened wooden cages in
were collected and brought to the laboratory. Infested
the laboratory where the fly larvae were exposed to the
plant material was stored in translucent cellophane bags
different parasitoids. In order to maintain cultures, various
which were placed over plastic pots and stored in a hori-
studies were conducted on the life-history of the fly,
zontal position SO that the humidity remained favourable.
including the effects of cold storage on larval and pupal
The emerging flies and parasitoids were collected and
development and adult longevity.
counted. Percent parasitism was calculated from the
At the CIBC West Indian Station, flies were reared in
number of emerged flres and parasitoids.
large cages in the laboratory. Attempts were made to rear
all the parasitoids received from surveys and existing cul-
tures at 22 and 27f 2°C in the following way: a small
Field surveys in the New World
number of mated females (usually 5-10) were introduced
Surveys for natural enemies of L. frifolii and other Lirio-
Into a 7.5 litre glass jar containing tut bean leaves in a
myza spp. on vegetables were made in low altitude horti-
glass of water. The leaves were infested with L. trifolii
cultural areas in Trinidad, Colombia and Texas, U.S.A. In
larvae of suitable age. The parasitoids were allowed to
Triniclad, the dry season lasts from January to May and is
search and oviposit for 3-4 days before being transferred
characterized by high temperatues and little rain. During
to a new jar. Studies were conductd on their life-histories
the rainy season from the end of May to December. heavy
in order to assess their suitability for introduction to
rains fall only for the first few months. The surveys were
Senegal.
conducted from October 1982 to July 1983, principally in
the three market gardens in the northern part of the island:
Aranguez Gardens, Macoya Gardens, and the University
of the West Indies Field Station. Among the many vegetab-
les grown at these sites, tomatoes and beans are particu-
Shipment, release, and recovery of parasitoids
larly mportant and are grown throughout the year.
Adult parasitoids were sent to Dakar by air freight. All
Infested leaves of all types of vegetables were collected
parcels were cleared by the Senegalese quarantine
every two weeks from October to February, and on an
authorities. Whenever surviving parasitolds were nume-
approximately monthly basis from April to July, and trans-
rous, some were released directly. The rest were taken to
ported in cloth bags. In the laboratory they were held in
the CDH for culture and for further study. Releases of a
ventilated plastic containers until all flies and their parasi-
few hundred adults of each species were made on several
toids had emerged. TO estimate the frequency of leafmi-
occasions. For monitoring, emergence samples were
ners in Aranguez, 10 branches of tomatoes and 50
taken on about a monthly basis.
~~~
___,_
._
..__
l__~l--ll_._-.-^<.-..-l------
------
2 9 2
P. Eleuensc:hwander
et a/.
Results
Cirrospi/us sp. near cinctiventris Ferrière (Eulo-
phidae)
Prerelease sfudies in Senegal
Diglyphus isaea Walker (Eulophidae)
In the 1982 survey, which covered most of the vegetable
Eucoilidea fetura Quinlan (Eucoilidae)
growing areas of the country, L. trifolii was found in abun-
Nordlanderia plowa Quinlan (Eucoilidae)
dance all over the Cap Vert to Mboro in the north-west
Allophrys sp (Ichneumonidae)
(100 km from Dakar) and Mbour in the south east (70 km
An unidentifiable braconid.
from Dakar). A very few, probably isolated, infestations
The last five species were recovered only on a few
were recorded from Kaolack (200 km south-east) ancl from
occasions from leaves with mines. C. cinctivenfris is per-
Djtbelor in the Casamance m the extreme south (500 km
haps hyperparasitic, and never common. The first four
south), as well as from a few gardens in Saint Louis in the
eulophids exhibited strong fluctuations in their relative
extreme north of the country (250 km north).
abundance (Table 1). Chrysonofomyia sp. near formosa
L. trifolli was reared from potato (Solarium tuberosum),
was dominant in the rainy season, and H. semialbiciava, in
tomato (Lycopersicum esculentum), diakhatou, okhra and
the second half of the dry season. The three main species
egg plant (S. melongena). where it did severe economic
were common on all host plants and throughout the
damage. Flies were also reared from the following vege-
region.
tables on which they caused minor damage: varrous cab-
Parasitism rates varied widely, but were usually lower on
b a g e s (Brass.;ca napus), s q u a s h (Citrullus vulgaris),
insecticide treated than on untreated fields (Table 2). No
cucumber and melon (mainly the cotyledons; Cucumis
influence of fungicide treatments on parasitoids could be
saliva and C. melo), celery (Apium graveolens), t,eans
detected in the sampling data.
(Phaseolus vulgaris), onion (Allium cepa), and carrot (D~U-
tus carota). In the wild vegetation around the gardens, L.
trifolii was at tirnes common on khekhem (Ricinus cornmu-
Survey and collection of parasitoids in the
nis) and on wild cowpea (Vigna coerulea). Occasionally,
this fly was also found on green and bell pepper (Capsi-
New World
cum frufescens and C. annuum), cowpea (Vigna unguicu-
Trinidad
lafa), different peas (Canavalia ensiformis and Fisum
sativum), beet (Beta vulgaris), lettuce (Lafuca safiva), pas-
L. frifolii was the only dipterous leafminer found. Its dis-
sion fruit (Passiflora foefida), basil (Ocimum basilicum),
tribution on the different crops is shown in Table 3. The
spinach (Amaranthus viridis and Perisfrophe bicalycu-
leafmtiner was found on a wide variety of vegetables in all
lafa), ma% (Zea mays), cotton (Gossypium herbaceum),
three gardens. but tomato and cowpea (bodibean. Vigna
and ~~sqq&,cidenfa/is, as well as on the ornamentals and
sesquipedalis) suffered the most severe infestation. Other
species, like gub gub bean (cowpea, V. sinensis), hyacinth
weprls pa?ura ‘qefel, Tagefes patula, and Sonchus hrun-
, f?.&&me of these hosts had already been reported ear-
bean (Lablab nager), ancl the other vegetables listed in
,” -EJdr ,fam Sen,eg’al (Bourdouxhe, 1982) and Réunion
Table 3, showed only minor damage. After the onset of the
rainy season in early May 1983, the overall abundance of
* ‘(Ve;ca’%‘breT 1980). Worldwide. the species has Ibeen
found. O’f? 4f genera in 10 families (Stegmaier, 1966).
L. trifolii fell drastically in ail gardens and the fly became
L. ,@olii inflestations were most severe during the
restricted to tornato and cowpea.
second part of the dry season, and almost non-existant
The following parasitoids were recovered, the first two
during the rainy season and in the early part of the next
being the most common:
dry season. L. brassicae (Riley) was also reared from cab-
Diaulinopsis callichroma (Eulophidae)
bage in the Cap Vert and Saint Louis.
C!osferocerus purpureus Howard (Eulophidae)
In the 1982 season, the original list of two parasitoids
Chrysonotomyia sp.F (Eulophioae)
found on L. frifolii (Bourdouxhe, 1982) was extended t’3 the
?Chrysocharis sp.J (Eulophidae)
following nine species:
Chrysocharis caribae BouEek (Eulophidae)
Hemiptarsenus semialbiclava Girault (Eulophidael
Elachertus sp.L (Eulophidae)
Haificopfera circuius Walker (Pteromalidae).
Chrysonotomyia SP., formosa group (Eulophidae)
Chrysonofomyia sp. near lepfocera Waterston (Eiulo-
Levels of parasitism (Figure 1) were lower during the
phidae)
two wet periods of the survey than in the dry season C.
Table 7. Relative abundance of indigenous pzrasitoids of Liriomyza trifolii fn the Cap Vert region of senegal
-
-
-
--.-
.---_---
Total number
of parasitoids
Chrysonotomyia
Period
(- 100%)
Hemiptarsenus
forrnosa leptocera
Cirrospilus
-~.
July-Sept. 82
629*
34.3
53.1 12.1
0.5
Oct.-Dec. 82
137
18.2
43.1 35.8
2.9
Jan.-March 83
2355
51.3
39.0 9.0
0.7
Apn-June 83
598
65.0
25.8
8.7
0.5
_ _ _ _-_- _-_._. -I__-----
* plus 1 Digfyphus isaea.
Biological control of Liriomyza frifoolii in Senegal
293
Table 2. Percentage parasitwn by indigenous parasitojds on Lirlomyza trlfolli in the Cap Vert of Senegal, or? insecflcide freated and
untreated fields
--_---
-
-
Insecticide treated field
Untreated fteld
~.-~ ---.--
-. - -
Total flies
Total flles
and
Percentage
and
Percentage
Month
Locality”
parasitoids
parasitism
Locality*
parasltoids
parasitism
_----.~-------
.--- .--..
~.- .-----.-_ _ _ _ _ _ _
July 82
a
163
26.4
* 13
53.8
e
54
33.3
52
55.8
f
77
10.4
Aug 82
b
142
38.0
145
68.3
a
46
39.1
167
50.9
156
96.2
Sept.- Nov. 82
0**
0**
Dec 82
a
20
45.0
Jan. 83
a
65
98.0
Feb 63
a
55
67.2
March 83
a
1036
96.7
C
48
98.0
b
434
57.8
Apr11 83
a
133
98.5
C
16
97.6
b
737
18.9
May 83
a
9
77.7
b
159
91.3
C
104
88.4
June 83
b
6
50.0
a
11
82.3
C
98
79.4
=a Camherene CDH. b Pikine-Yeumbeul, c Thiaroye sur mer, d tvlalika, e Nlaga, f Berr-Tialane.
* * fly populations very low.
Table 3. Dstrtbutron of Liriomyza trifolii and associated parasitoids in relation to vegetable crops in Trlnjdad,
II----~
Chryso-
?Chryso-
L.
C.
D.
notomyia
Char/s
Eiacherfus
Vegetable
trifolfi
purpureus
callichroma
sp.F
sp.J
C. caribea
sp.L
H. crrculus
-.
-.-I_--
Cowpea
t
t
-4
t
Gub gub
bear
t
t
Hyacmth
bean
t
-r
+
i
+
1-
Tomate
?
+
-t
?-
-t
Sweet
peser
t
t
r
Eggplant
+
+
Celery
L
r
t
Cucumber
t
+
t
Okhra
t
-c
+
t
-t
_.----
p r e s e n t
purpureas favoured the rainy season. when it was often
toids were found associated with this leafminer (Table 4),
the most abundant parasitoid. During the dry season D.
the only common ones being Chrysonotomyia sp. W. and
callichroma was the only abundant parasitoid. On toma-
Diglyphus websteri. Some of the species recorded were
toes, parasitism by this wasp exceeded 60%. The other
similar to those found by Chandler (1982) on melon and
species parasitized a maximum of 5% of all L. trifolii lar-
sweet pepper.
vae. Unfortunately. insecticides were used regularly in all
The Liriomyza parasitoids collected by the University of
of the gardens on most of the vegetables, thereby someti-
Florida and the State Department of Agriculture, Hawaii,
mes abruptly lowering the levels of parasitism.
are listed in Table 4. The parasitoids collected from horti-
cultural areas in Hawaii for this project had originally been
introduced from North, Central and South America in the
Colornbia and United States
late 1970’s for the control of L. trifolii and L. sativae (Lai,
In Colombta, dipterous leafminers were scarce and only
1983). The six species listed became established and are
Diglyphus begini was collected near Piendano (Table 4).
now quite common in the field. In addition, the parasitoids
In the Rio Grande Valley of Texas, Liriomyza ?sativae was
sent by the University of California, Riverside and Berke-
common on ail vegetables irrespective of whether they
ley, from existing cultures are indicated. The four institu-
had been sprayed with insecticide or not. Various parasi-
tions provided cultures of nine species.
2 9 4
P. Neuenschwander et a/.
access to plants, and oviposited and aged faster. In the
refrigerator, survival at 12’C was 3 or 7 days according to
whether they were fed or not before cooling. At 4”C, survi-
val was 8 and 10 days, respectively. It is concluded that
adults cannot be stored for a long time and need sugar
water or honey even when they have access to plants.
Cool storage of pupae depended on their age (Table 5).
Before the pupal moult rnside the puparium, the larvae
proved very sensitive to cold. Pupae held at 12°C l-3 days
after puparium formation, survived better, but because of
early emergence in the refrigerator, cool storage beyond 1
month is not recommended. When pupae were stored at
4”C, survival was only 1% after 2 weeks. Similarly, larvae
inside the leaves could not be stored; all died within 2-4
weeks at 12°C. This information allowed us to ensure a
reliable supply of flies in the insectary.
O
N
D
J
F
M
A
M
J
J
I
I
Exotic parasitoids
8O r rainy
I
dry
1 rainy saasort
I
I
The life-history characteristics, host age preference,
and developmental time of parasitoids brought success-
fully into culture, are Iisted in Table 6. All species attack
and ovipost in/on the host larvae and are solitary. Most of
the eulophids kil1 the host in its mine, but the braconids and
the pteromalid do not kill it until it has formed a pupa from
which the adult parasitoid eventually emerges. Some of
the species listed seem to prefer a particular instar for
oviposition.
II
11
11
11
11
t
Shipment, culture, release and recovery in Senegal
0 N
D J F
M A
M J
J
1982
1983
Species shipped from the Americas to Senegal, and
Figure 7a. Number of Liriomyza trifolii larvae on 70 branches of
their condition at arriva1 and in subsequent cultures in the
fomato (T) and 50 cowpea leaves (C), together with cumulative
insectary, are indicated in Table 7. Of tire 11 species
parasitization rates by Diaulinopsis callichroma (0.c.) and
received, two were lost before releases could be made.
Closterocerus purpureus (Cp.) on lb. tomate and Ic. cowpea, at
Most were kept in culture for a few generations for relea-
Aranguez Gardens, Trinidad.
ses on later dates, Opius dissitus remained in a viable
culture for more than a year.
A few specimens of most species were recovered
Life-history studies
within a few weeks of release, indicating successful
Liriomyza trifolii
breeding in the field. Only Opius dissitus was found regu-
larly. The first small samples taken in May-July 1983 in the
At 27 + 2”C, the eggs of L. trifolii hatched within 2-3
release fields (which are not the same as the extensively
days, and the 3 larval instars fed for 4 days insiae their
sampled fields in Tables 1 and 2) indicate that this exotic
leafmines before dropping to the ground for pupation.
parasitoid became the third most important parasitoid,
Adults emerged about 6-8 days later, whereby emergence
after the indigenous f-l. semialbiclava and Chrysonotomyia
was limited to the period from 6 a.m. to 2 p.m. with a mar-
sp. near formosa.
ked peak from 10-l 1 a.m. This life-cycle of 12-15 days
was not altered significantly when tut bean or tomato lea-
ves were used, provided that proper humidity was main-
tained. These results are in accordance with those
Discussion
reported by Charlton and Allen (1981).
Following its accidental introduction into Senegal, L.
At 27”C, mean survival of unfed adults was 2 days. Flies
trifolii spread throughout the main vegetable growing area
provided with sugar water lived 16 days which corrobora-
of the Cap Vert region which grows about 4500 ha of
tes more extensive data by Vercambre (1980). When flies
vegetables. Additional isolated infestations were found
were given the opportunity to make nutritional stings on
throughout the country. In the Cap Vert, losses in 1981
tomato leaves, survival was 10 days with, and only 2 days
had been dramatic and parasitization rates by H. semial-
without, sugar. Protein hydrolysate (Bumina?) was net
biclava and Chrysonotomyia sp. were relatively low, at 30-
accepted and did not prolong the life span. Thus, ilies fed
40°h (Bourdouxhe, 1982). By the time the biological control
with sugar water alone survived longer than those having
project was initiated in 1982, losses had diminished
Biological control of Liriomyza trifolii in Senegal
2 9 5
Table 4. Survey for parasitoids of Lmomyza spp. in America
-
-
SpecieS
Orlgin
Host plant
Host fly”
-~-~~-
- - - -
Eulophtdae:
Chrysochans carlbea BouEek
Hawaii
vegetables
L.l, L.S.
Chrysochans sp. nr. caribea**
Texas
tomato
L.?S.
Chrysocham parksi (Crawford)
Hawaii
vegetables
L.t., L.S.
southern California
chrysanthemume
L.t.
Chrysonotomyia punctiventris
(Crawford)
Hawaii
vegetables
LI, L.S.
Chrysonotomyfa sp W
Texas
tomate. sweet
pepper, melon
L.?s.
Ciosterocerus purpureus
(Homard)
Texas
sweet pepper
L.?s.
fhg/yphUS
begim Ashmead
central Callfornia
?*
L.t.
Coiombia
chrysanthemum
L.t.
r3glyphus mtermedius
iGirault)
southern California
chrysanthemum*
?
Florida
beans
L.?.
Dlglyphus websteri
(Crawtord)
Texas
tomato, sweet pepper
L.?s.
Pteromalldae.
Haiticoptera Vcfrcutus
(Walker)§
Hawaii
vegetables
LI., L.S.
Eucollldae:
7Dsorqgna sp.@
Hawaii
vegetables
LS., L.S.
3Drsorygna sp. BB
Texas
tomato
L.?s.
Braconrdae.
Op/us drmldiatus (Ashmead)
Florida
chrysanthemuma
3
Oprus dissitus Muesebeck
Florida
beans
L.?t.
Hawaii
vegetables
LS., L.S.
* L.t.
L. tnfoli,, L.s. L L. sat/vae.
** sent as Chrysocharis sp. near girau/tiYoshimoto.
5 sent as Halticopterapatellana(Dalman).
$3 sentas
Cothonasp/s sp.
l from established laboratory cultures.
Table 5 Emergence and mortatity of Liriomyza trifolii larvae (L,) and pupae (P) of different ages following cold storage of 3 months at 72°C.
300 insects per treatment (= 100%) Cambéréne, 7982
-
-
Percentage mortality as
Age at start of
Percentage Flies
cold siorage
Adults inside
Adults emerged
emerged
m day:j
L3 and P
the puparium
in cold storage*
at 25”C**
-_-.--.-.-- .--------.-
L,
untreated
0
3.0
-
97.0
L 99.0
1 . 0
0
0
P
114
d-old
40.0
55.0
2.0
3.0
1 a.7
69.0
3.7
18.6
2 3.7
63.3
23.7
9.3
3 1.7
45.7
41.3
11.3
* after an average of 4.7 weeks for 3 d-old pupae to 7.0 weeks for 1/4 d-old pupae.
** after an average of 2.3 d for 3 d-old pupae to 3.9 d for 1/4
d-old pupae. Control= 5.9 d.
somewhat, and parasitization rates by indigenous parasi-
for introduction into France (J. P. Lyon, pers. Comm.).
toids surpassed the 1981 values rn ail sampled fields
Some of the parasitoids received had already been
which had not been treated with insecticides. Rates of
investigated in the Americas and shown promising attri-
parasitism seemed even higher in thefirst half of 1983. It is
butes. In Trinidad, Diaulinopsis callichroma reached the
conciuded that indigenous eulophids had transferred
highest level of parasitism among seven species. Chryso-
successfully from other leafminers to this new host within
charis parksi had been reported to have a density depen-
a relatively short period. This confirms the polyphagy
dent relationship to L. trifolii populations (Johnson et a/.,
shown by many agromyzid parasitoids (Stegmaier, 1972;
1980) and is now being used in European glasshouses (J.
Murphy, 1984). Thus, rates of parasitism in Africa often
Woets and A. van der Linden, pers. Comm.). Diglyphus
surpassed those recorded from Trinidad (see Figure 1)
begini was the most abundant parasitoid in Southern Cali-
and other countries in the Americas (Pohronezny et a/.,
fornia (Allen and Charlton, 1981), and Halticoptera sp. lis-
1978; Tryon and Poe, 1979; Johnson et a/., 1980) where
ted as aenea (Walker) was dominant in Arizona (Hills and
insecticide pressure is probably higher than in the Cap
Taylor, 1951). The two Opius spp., which were received
Vert. In fact, the African H. semialbiclava has been chosen
from other insectaries, are larval-pupal parasitoids of
.-.-- 1..1_ .” ,... “.~““-----l_.__l--.--
296
P. Neuenschwander et al.
Table 6. Life-hislories of Liriomyza parasitoids
--.-
-
-
Host instar preferred
Species
Life-history
for ,Wiposition
Develepment time*
Additional reference
-
-
-
~..
Chrysocharis
Larval-pupal
Early instars
13da:27”C
a
parksi
endoparsitoid
Chrysonofomyia
Larval
Early instars
11 d ai. 27°C
sp.w
ectoparasitoid?
Diaulinopsis
Larval
Middle-late
Males 11 d
callichroma
ectoparasitoid?
instars
Females 13-l 4 d at 27’ C
Diglyphus
Larval
Lata instars
12 d ai 22°C
b
begini
ectoparasitoid
11-13 cl at 29°C
Diglyphus
Larval
Late instar
13 d at 22°C
d,e
intermedius
ectoparasltoid
14-15 d at 29°C
Halficopfera
Larval-pupal
Early instars
19-23 d at 29°C
circulus
endoparasitoid?
opius
Larval-pupal
All instars
lOdat27”C
f
dimidiatus
endoparasitoid
13-14 d at 29°C
opius
Larval-pupal
Firsl instar
11 dat27”C
dissitus
endoparasitoid
12-14 d at 29°C
-
-.
* agg to adult; at 22 and 27°C from ClBC, Trinidad, at 29”CfrDm CDH, Senegal. a Christieand Parrella. 1982; b Do~n. 1957; c Allen and Charlton,
1981; d Hendrickson and Bath, 1978; e Gordh and Hendrickson, 1979; f Lema and Poe, 1979.
‘Table 7. Cr@in, survival, release, and recovery of Liriomyza trifolii parasitoids sent from Amenca to Sanegal
-
~-
Total
Percentage
Quality of
Local ity and
number
Number of
survival
culture in
dates of
Species
Origin
dispatched
shipments*
at arriva1
Senegal**
releasess
Recovery
-
~-
---. ._~
C caribea
Hawaii
750
3
a5
a
c 4-83
*
C parksi
Hawaii
1360
3
65
b
D 12-82; C 4-83
*
California
154
2
5
C. punctiventris
Hawaii
1100
3
90
a
c 4-83
*?
c.
sp. w
Texas
95
50
a
0. callichroma
Trinidad
885
4
95
b
A l-83 (2x); D l-83,
2-83
*
D. begini
California
100
‘1
90
b
D 10-82; E 2-83
*?
Colombia
163
Z!
70
0. intermedius
Florida
292
%!
95
b
B 2-83, 4-83: C 5-83
California
65
‘1
80
(2x); E 5-83
*§§
H. circulus
Hawaii
1250
3
90
a
A 12-82, 3-83; B 4-83;
C 4-83. 5-83 (2x)
*§§
Disorygna sp.
Hawaii
500
1
20
a
0. dimidiafus
Florida
52
1
95
C
C 9-83 (2x)
*?
0. dissitus
Florida
808
0r,,
90
C
A l-83 (2x), 3-83 (4x),
Hawaii
700
il r,
90
4-83; B 3-83. 4-83
(2x); C 4-83, 5-83 (3x),
6-83 (2x): E 2-83
*§§
--.
*ail parcels arrived within 2-4 d.
**a - lost after a few generations in culture; b .=. maintained at low inumbers in a steady culture; c = good
culture.
§A Cambéréne, B Pikine, C Thiaroye sur mer, D Yeumbeul, E Gueno Mbao.
$5 recovery confirmed by CIE specialist.
wl?ich 0. dimidiatus at least does not prefer the same host
culture and frequent releases at many sites over a long
stages for oviposition as some other species, e.g. Chryso-
period, as well as the fact that it could fil1 an unoccupied
notomyia sp. (Lema and Poe, 1979). Therefore these spe-
ecological niche. The greatest difficulty for these exotic
cies fil1 a n e c o l o g i c a l n i c h e w h i c h w a s v i r t u a l l y
parasitoids in achieving permanent establishment will be
unoccupied in Africa and have a special interest for intro-
the rainy season when host populations are exceedingly
duction. However, a literature review by Murphy (1984)
low. Permanent establishment of any of the exotic spe-
shows that many more candidate species should be tried
cies, their competition with indigenous parasitoids, and,
which could not be imported into Senegal during this pre-
finally, their evenltual efficiency remain to be evaluated.
liminary study.
Biological control with indigenous and exotic parasi-
The first results of the biological control project repor-
toids seems particularly promising for L. trifolii in Africa
ted here indicate that most species passed through at
because insecticide use is still less frequent than in
least one generation in the field following release. Opius
Europe and North America, and because Liriomyza spp.
dissifus did especially weil during the first dry season.
seem’ to reduce yield of vegetables like tomatoes only at
Possible reasons for this achievement are its successful
very high infestation ievels (Levins et a/., 1975).
Biological control of Liriomyza trifolii in Senegal
297
Acknowledgements
GORDH. G. and HENDRICKSON. Jr. R.. 1979. New specles ot
Diglyphus, a world Iist of the specles, taxonomie notes and a
This study was executed in the framework of a one year
key to new world species of Dfglyphus and Daulinopsis
PTC project funded by FAO with a subcontract for explo-
(Hymenoptera: Eulophidae). Proceedings of the Entomologi-
ration work to CIBC. We thank F. Faye and M. Ly, subse-
cal Society of Washington 81, 666-684.
HENDRIKSE, A., ZUCCHI, R., VAN LENTEREN, J. and WOETS, J.,
quept directors of the CDH, and H. van der Veken of the
1980. Dacnusa sibirxa Telenga and Op~us palhpes Wesmael
Senegal/FAO/Belgian
project at the CDH for their conti-
(Hym., Braconidae) In the control of the tomato leafminer
nuoL;s support, J. Beniest and L. de Maeyer from the CDH
Liriomyza bryoniae Kalt. Bullefin S.R.O.P./W.P.R.S. 3, (3). 83-
for their help tn editing the manuscript. J. Woets, Naald-
98.
HENDRICKSON, R. M. Jr. and BATH. S E., 1978. Notes on the
wijk, for information, and particularly S. Diop, CDH, for his
biology of Diglyphus intermedlus (Hymenoptera: Eulophi-
able technical assistance. We also thank the following
dae). a parasite of the alfalfa blotch leafminer, Agromyza
CIEIBritish Museum entomologists for identifications: 1.
frontella (Diptera, Agromyzidae). Proceedings of the Entomo-
M. White (Agromyzidae), Z. BouEek (Eulophidae), B. R.
logical Society of Washington 80, 210-215.
Subba Rao (Pteromalidae), A. D. Austin and G. E. J. Nixon
HILLS, D. A. and TAYLOR, E. A.. 1951 Parasitization of dipterous
leafminers in cantaloups and lettuce in the Salt River Valley,
(Braconidae). J. Quinlan (Eucoilidae), and R. A. Wharton
Arizona. Journal of Economie Entomology 44, 759-762.
from Texas A&M University for additional comments on
JOHNSON, M. W.. OATMAN, E. R. and WYMAN, J. A., 1980. Natu-
the braconids. Finally we would like to thank all the ento-
ral control of Liriomyza sativae (Dip: Agromyzldae) in pole
molog!sts in the collaborating institutions who provided
tomatoes in southern California. Entomophaga 25, 193-198.
us with help and species from their cultures, and D. J.
LAI, P., 1983. Biological control of hiomyza In Hawaii. Biocontrol
News and Information 4 (3), 195.. 196.
Greathead (CIBC, London) and L. Brader (FAO, Rome) for
LEMA, K. M. and POE, S. L., 1979. Age specific mortality of L/rio-
coordinating the project and for reviewing the manuscript,
myza sativae due to Chrysonotomy/a formosa and parasitiza-
tion by Opius dimidlatus and Chrysonotomy/a formosa.
Environmental Entomology 6, 935-937.
LEVINS, R. A., POE, S. L. and JONES, J. P.. 1975. Effectlveness of
a leafminer control program for Florida tomato production.
Journal of Economie Entomology 62, 772-774.
MURPHY, S. T., 1984. Final report on surveys in the Neotropical-
/Nearctic region for natural enemies of Liriomyza trifolii and
References
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Trinidad, 29 pp.
ALLEN, W. W and CHARLTON, C. A.. 1981. The biology of Dlgly-
PARRELLA, M. P. and KEIL. C. B., 1984. Insect pest management:
phus begm and its performance in cage releases on chry-
The lesson of Liriomyza. Bulletin of the Entomolog~cal Soci-
saqthemums. pp. 75-81. In Proceedings of IFAS-fndustry
ety of America 30, 22-25.
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POHRONEZNY, K.. WADDILL, V. H., STALL. W., and DANKERS,
13 J Schuster. Ed.), IFAS. University of Florida.
W.. 1978. Integrated control of the vegetable leafminer (Llrio-
BOURDOUXHE, L, 1982. La mineuse nord-amencaine des feuil-
myza sativae Blanchard) durrng the 1977-78 tomato season
les (Lirjomyza trifoli!), diptère, Agromyzidae, sur cultures
in Dade County, Florida. Proceedings of the Florida Hort~~l-
maraîchéres au Sénégal. Bulletin Phytosanitaire FAO 30,81-
tural Society 91. 264-267.
82
SPENCER, K. A., 1973. Agromyzidae (Dlptera) of economic impor.
CHANDLER. L D.. 1982. Parasltlzation of cantaloup mfesting
tance. The Hague: Junk. 418 pp
agromyzid leafminers in the lower Rio Grande Valley, Texas,
STEGMAIER. C. E. Jr., 1966. Host plants and parasites of Lirlo-
Southwestern Entomologist 7, 94-97.
myza trifolii in Florida (Diptera: Agromyzidae). Florida Enfo-
CHARLTON C. A. and ALLEN. W. W. 1981. The bioiogy of L~rro-
mologist 49, 75-80.
myza trifol/ on beans and chrysanthemums. pp. 42-49. In
STEGMAIER, C. E. Jr., 1972. Parasitic Hymenoptera bred from the
Proceedings of IFAS-lndustry conference on biology and
family Agromyzidae (Dipt.) wlth special reference to southern
control of Llriomyza leafminers (D. J. Schuster, Ed.). IFAS, Uni-
Florida. The Florida Entomofogist 55. 273-282.
versity of Flonda.
TRYON, E. H. Jr. and POE, S. L. 1979. Sample size, age of celery
CHRISTIE. G. D. and PARRELLA. M. P., 1982. Biology of Chryso-
petiole and rearing conditions affect emergence of vegetable
Char!s parksi(Hymenoptera: Eulophidae), an interna1 parasite
leafminers and parasltes. Proceedings of the Florida State
çf Lirfomyza trifolii (Diptera. Agromyzidae), and its compati-
Horticultural Society 92, 108-l 10.
bility with selected msect growth regulators. pp. 174-179. In
VERCAMBRE, B., 1980. Études réalisées â la Réunion sur la
F’roceedings of the 3rd annuaf conference on the leafminer
mouche maraichaire: Liriomyra trifoli! Burgess. Revue
Sponsored by SAF-Alexandria, Virginia.
Agricole et Sucrière de /‘/le Maurfce 59, 147- 157.
D’AGUILAR. J. and MARTINEZ, M.. 1979. Sur la présence en
WOETS, J. and VAN DER LINDEN, A. 1982. On the occurrence of
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Opius pallipes Wesmael and Dacnusa sibirica Telenga
6u:lelrn de /a Société Entomologique de France 64. 143- 146.
(Braconidae) in cases of natural control of the tomato leafmi-
DE LANNOY, G., 1982. Les rapports météorologiques du CDH.
ner Linomyza bryoniae Kalt. (Agromyzidae) In some large
(rnimeograph).
greenhouses in the Netherlands. Mededlingen van de Facul-
DOUTT, R. E 1957 Biology of Sofenotus begmi (Ashmead). Jour-
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533-540.
TROPICAL PEST MANAGEMENT, 1987, X(4), 290-297
Introduction of exotic parasitic wasps for the control of Liriomyza trifo/ii
(Dipt., Agromyzidae) in Senegal
,_ .”
*A.”
Keywords: Brologrcal control. Lrriomyza trlfoh, Senegal
I >’ .
P. NE.UENSCHWANDER, S. T. MURPHY* and E. V. COLY**
Dept. of Phytomedicine, Swiss Federal Institute of Technology, Zürich, Switzerland, consultant with the Food and
Agri;culture Organization (FAO), Rome, Italy.
Present address: fnternationai Institute of Tropical Agriculture, Ibadan, Nigeria.
* CAB International fnstitute of Biologicaf Controf (CIBC), West Indian Station, Curepe, Trinidad, W.I.
Present address: CIBC Kenya Station, Nairobi, Kenya.
** Centre pour le Développement de /‘Horticulture (CDH), Cambérène, Sénégal.
Abstract. Linornyza tr~fol~~ Burgess had frrst been reported from
Israel, Japan. the Philippines, and some Pacifie Islands (CIE
Senegal In 1980. Freld surveys In 1982 revealed its presence in
map 450, 1984).
ail vegetable growing areas of the country, heaviest damage
In America, L. frifofii and other Liriomyza spp. have
berng regrstered in the Cap Vert. Five indrgenous eulophrds (lar-
become major pests because of insecticide misuse. The
val parasrtords) plus five other rare parasitoids, frequently parasr-
mines of the larvae and feeding punctures by the adult
trred ever 90?:0 of the flres. These rates were higher in insectrcrde
free frelds. and very much above the 30-40% reported for 1981.
flies often lead to severe defoliation. However, under natu-
The rnost important parasitords were Hemrptarsensus semialbrc-
ral conditions most species are reasonably well control-
lave (Grrault), whrch dominated in the second half of the dry
led by their parasitoid complex (Spencer, 1973; Parrella
seasoh. and two Chrysonotomy\\a spp., which were more abund-
and Keil, 1984), whrch has been recently reviewed
ant rn the rarny season Surveys for exotrc parasitoids mdicated
(Murphy, 1984). Parasitotds of Lrriomyza spp. have been
B;e~f;rrpps~s ca///cnroma Crawford from Trrnidad to be a promis-
mg Especres for mtrodLrction in the New World. This parasitoid,
studied in order to develop integrated control (Stegmaier,
together wrth etght other chalcrdords (mostly larval parasitoids)
1972; Johnson et a/., 1980; Allen and Charlton, 1981). Bio-
and two braconrds (larval-pupal parasrtoids), were collected in
logical control of indrgenous agromyzid leafminers has
the 0eld OI recetved from estahlished insectary cultures. They
also received much attention in European glasshouse
were :studred and shrpped for reanng and release in Senegal.
cultures (Hendrikse et a/., 1980. Woets and van der Lin-
Nrne species were released at the end of 1982 and in 1983. Many
were ,*ecovered shortly after release, but only Op~us dissitus
den, 1982). Recently, these studres have been extended to
Muesebeck was recovered In later samples and became relativ-
the exotic L. frifofii (J. P. Lyon, pers. Comm.).
eiy nbundant.
There have been two classical biological control
attempts against Liriomyza spp., where natural enemies
trom the original home of an accidentally introduced pest
were transferred for permanent establishment in the field.
Introduction
These were limited to Hawaii, where both L. trifolii and L.
sativae were controlled on vegetable crops by exotic
In Senegal a large scale attack by an agromyzrd leafmi-
parasitoids introduced from the southern’U.S.A. and Cen-
ner, later rdentrfied as Linomyza trifofii Burgess, was
tral America (Lai, 1983) and to the Republic of South
reported from the Cap Vert region near Dakar in Decem-
Africa where attempts are presently being made to control
ber, 1980 By Aprrl 1981, severe damage had occurred,
L. trifolii on Chrysanfhemum spp. and tomatoes using
marnly on the African vegetables diakhatou (Solarium
Neotropical parasitoids (H. van Hamburg. pers. comm.).
aefkiopicom) and okhra (-gombo) (Hibiscus esculenfus),
A biological control project, funded by FAO, was con-
and on potatoes. Parasitization rates by indigenous eulo-
ducted at the CDH in Senegal, where the first studies on L.
phrds were low (Bourdouxhe, 1982).
trifofii had been done. Parasitoids of L. trifolii on vegetab-
The crnsumed origan of this fly (untrl recently confused
les were to be introduced from the New World into Sene-
with L. xr:ivae Blanchard) is in America, especially Florida
gal in collaboration with the CIBC West Indian Station.
and the Carribean (Spencer, 1973). The fly had been intro-
Given the short duration of this pilot project, only Trinidad
duced accidentally rnto Kenya on Chrysanthemum sp.
and a few other areas in the Americas could be searched.
cuttings around 1970. Later it reached the Canary Islcnds,
Cther parasitoids were received from established insec-
Malta. southern France, and commercial greenhouses in
tary cultures in the U.S.A. Meanwhile, in Senegal, insec-
central and northern Europe (D’Aguilar and Martinez,
tary facilities were constructed, and the extent of L. trifolii
1979). In 1978 it was first reported from Mauritius and
distribution and the abundance of indigenous parsitoids
Réunion,$where it did damage to a wide range of tropical
of this exotic host were evaluated. The present text descn-
garden çrops (Vercambre, 1980). In addition to the
bes the first results and reports on releases of exotic par-
countries mentioned. L. trifolri also occurs in South Africa,
sitoids and first recoveries.
Biological control of Liriomyza trifolii in Senegal
291
Materials and methods
cowpea leaves were taken at random from the respective
bags. All dipterous leafminers and their parasitoids were
Field surveys in Senegal
counted.
From July 1982 to July 1983, frequent surveys for L.
Two short collecting trips were made in late April/early
trifolii and its parasitoids were conducted in the Cap Vert
May 1983 to the Cauca Valley, Colombia, and in late May
region of Senegal, while other areas were searched only
to the Rio Grande Valley, Texas, U.S.A. Besides the CIBC
occaslonally. Mean rainfail at the Cap Vert during the last
surveys, collections of Liriomyza spp. parasitoids were
30 years was 518mm per year, but has recently dropped
made by the University of Florida, Homestead, in southern
to about 400mm (De Lannoy, 1982). The rainy season
Florida, and by the State Department of Agriculture,
lasts from June to October with the heaviest rains in
Hawaii, and sent to the CIBC West Indian Station for qua-
August-September. The long dry season is marked by low
rantine. Additional parasitoids were supplied from exist-
temperatures in January (mean minimum around 17“C)
ing cultures at the University of California, Berkeley and
and high temperatures in August-September-October
Riverside.
(mean maximum around 33°C). From November to March
Samples of all dipterous leafminers and their parasi-
a northeastern wind (‘harmattan’) sometimes lowers rela-
toids from the surveys in America and Africa were sent to
tive hurnidity to below 20%.
the CAB International Institute of Entomology (CIE) in
The Cap Vert is the main vegetable growing area of the
London for identification and comment.
country. Vegetables are grown mostly in fertile valleys
(‘niayes’) between the coastal dunes at sea level. They are
trrigated throughout the dry season by hand with water
from wells. The main vegetables grown are potatoes,
Rearing and Me-history studies of L. trifolii and
tomatoes and other Solanaceae, various beans, cabbages
exotic parasitoids
and leafy vegetables, all of which are hosts of L. trifolii.
Cultures of L. trifolii were maintained in Trinidad and
Infestation by L. trifolii varied very much from field to
Senegal. In Senegal, various plants (but mainly tomatoes
field. In each plot it was short lived, and sampling was
and beans) were grown in an insect-proof screenhouse.
often Interrupted by leaf fall or harvest. It was therefore not
They were then placed in a screened room of several m3
possible during the short period of the project to develop
where the leaves were stung by the flies. When leafmines
proper quantitative sampling plans for the different sub-
had reached the stage required by the parasitoids, the
strates. Wherever living infestations were highest, leaves
potted plants were placed in screened wooden cages in
were collected and brought to the laboratory. Infested
the laboratory where the fly larvae were exposed to the
plant material was stored in translucent cellophane bags
different parasitoids. In order to maintain cultures, various
which were placed over plastic pots and stored in a hori-
studies were conducted on the life-history of the fly,
zontal position SO that the humidity remained favourable.
including the effects of cold storage on larval and pupal
The emerging flies and parasitoids were collected and
development and adult longevity.
counted. Percent parasitism was calculated from the
At the CIBC West Indian Station, flies were reared in
number of emerged flres and parasitoids.
large cages in the laboratory. Attempts were made to rear
all the parasitoids received from surveys and existing cul-
tures at 22 and 27f 2°C in the following way: a small
Field surveys in the New World
number of mated females (usually 5-10) were introduced
Surveys for natural enemies of L. frifolii and other Lirio-
Into a 7.5 litre glass jar containing tut bean leaves in a
myza spp. on vegetables were made in low altitude horti-
glass of water. The leaves were infested with L. trifolii
cultural areas in Trinidad, Colombia and Texas, U.S.A. In
larvae of suitable age. The parasitoids were allowed to
Triniclad, the dry season lasts from January to May and is
search and oviposit for 3-4 days before being transferred
characterized by high temperatues and little rain. During
to a new jar. Studies were conductd on their life-histories
the rainy season from the end of May to December. heavy
in order to assess their suitability for introduction to
rains fall only for the first few months. The surveys were
Senegal.
conducted from October 1982 to July 1983, principally in
the three market gardens in the northern part of the island:
Aranguez Gardens, Macoya Gardens, and the University
of the West Indies Field Station. Among the many vegetab-
les grown at these sites, tomatoes and beans are particu-
Shipment, release, and recovery of parasitoids
larly mportant and are grown throughout the year.
Adult parasitoids were sent to Dakar by air freight. All
Infested leaves of all types of vegetables were collected
parcels were cleared by the Senegalese quarantine
every two weeks from October to February, and on an
authorities. Whenever surviving parasitolds were nume-
approximately monthly basis from April to July, and trans-
rous, some were released directly. The rest were taken to
ported in cloth bags. In the laboratory they were held in
the CDH for culture and for further study. Releases of a
ventilated plastic containers until all flies and their parasi-
few hundred adults of each species were made on several
toids had emerged. TO estimate the frequency of leafmi-
occasions. For monitoring, emergence samples were
ners in Aranguez, 10 branches of tomatoes and 50
taken on about a monthly basis.
~~~
___,_
._
..__
l__~l--ll_._-.-^<.-..-l------
------
2 9 2
P. Eleuensc:hwander
et a/.
Results
Cirrospi/us sp. near cinctiventris Ferrière (Eulo-
phidae)
Prerelease sfudies in Senegal
Diglyphus isaea Walker (Eulophidae)
In the 1982 survey, which covered most of the vegetable
Eucoilidea fetura Quinlan (Eucoilidae)
growing areas of the country, L. trifolii was found in abun-
Nordlanderia plowa Quinlan (Eucoilidae)
dance all over the Cap Vert to Mboro in the north-west
Allophrys sp (Ichneumonidae)
(100 km from Dakar) and Mbour in the south east (70 km
An unidentifiable braconid.
from Dakar). A very few, probably isolated, infestations
The last five species were recovered only on a few
were recorded from Kaolack (200 km south-east) ancl from
occasions from leaves with mines. C. cinctivenfris is per-
Djtbelor in the Casamance m the extreme south (500 km
haps hyperparasitic, and never common. The first four
south), as well as from a few gardens in Saint Louis in the
eulophids exhibited strong fluctuations in their relative
extreme north of the country (250 km north).
abundance (Table 1). Chrysonofomyia sp. near formosa
L. trifolli was reared from potato (Solarium tuberosum),
was dominant in the rainy season, and H. semialbiciava, in
tomato (Lycopersicum esculentum), diakhatou, okhra and
the second half of the dry season. The three main species
egg plant (S. melongena). where it did severe economic
were common on all host plants and throughout the
damage. Flies were also reared from the following vege-
region.
tables on which they caused minor damage: varrous cab-
Parasitism rates varied widely, but were usually lower on
b a g e s (Brass.;ca napus), s q u a s h (Citrullus vulgaris),
insecticide treated than on untreated fields (Table 2). No
cucumber and melon (mainly the cotyledons; Cucumis
influence of fungicide treatments on parasitoids could be
saliva and C. melo), celery (Apium graveolens), t,eans
detected in the sampling data.
(Phaseolus vulgaris), onion (Allium cepa), and carrot (D~U-
tus carota). In the wild vegetation around the gardens, L.
trifolii was at tirnes common on khekhem (Ricinus cornmu-
Survey and collection of parasitoids in the
nis) and on wild cowpea (Vigna coerulea). Occasionally,
this fly was also found on green and bell pepper (Capsi-
New World
cum frufescens and C. annuum), cowpea (Vigna unguicu-
Trinidad
lafa), different peas (Canavalia ensiformis and Fisum
sativum), beet (Beta vulgaris), lettuce (Lafuca safiva), pas-
L. frifolii was the only dipterous leafminer found. Its dis-
sion fruit (Passiflora foefida), basil (Ocimum basilicum),
tribution on the different crops is shown in Table 3. The
spinach (Amaranthus viridis and Perisfrophe bicalycu-
leafmtiner was found on a wide variety of vegetables in all
lafa), ma% (Zea mays), cotton (Gossypium herbaceum),
three gardens. but tomato and cowpea (bodibean. Vigna
and ~~sqq&,cidenfa/is, as well as on the ornamentals and
sesquipedalis) suffered the most severe infestation. Other
species, like gub gub bean (cowpea, V. sinensis), hyacinth
weprls pa?ura ‘qefel, Tagefes patula, and Sonchus hrun-
, f?.&&me of these hosts had already been reported ear-
bean (Lablab nager), ancl the other vegetables listed in
,” -EJdr ,fam Sen,eg’al (Bourdouxhe, 1982) and Réunion
Table 3, showed only minor damage. After the onset of the
rainy season in early May 1983, the overall abundance of
* ‘(Ve;ca’%‘breT 1980). Worldwide. the species has Ibeen
found. O’f? 4f genera in 10 families (Stegmaier, 1966).
L. trifolii fell drastically in ail gardens and the fly became
L. ,@olii inflestations were most severe during the
restricted to tornato and cowpea.
second part of the dry season, and almost non-existant
The following parasitoids were recovered, the first two
during the rainy season and in the early part of the next
being the most common:
dry season. L. brassicae (Riley) was also reared from cab-
Diaulinopsis callichroma (Eulophidae)
bage in the Cap Vert and Saint Louis.
C!osferocerus purpureus Howard (Eulophidae)
In the 1982 season, the original list of two parasitoids
Chrysonotomyia sp.F (Eulophioae)
found on L. frifolii (Bourdouxhe, 1982) was extended t’3 the
?Chrysocharis sp.J (Eulophidae)
following nine species:
Chrysocharis caribae BouEek (Eulophidae)
Hemiptarsenus semialbiclava Girault (Eulophidael
Elachertus sp.L (Eulophidae)
Haificopfera circuius Walker (Pteromalidae).
Chrysonotomyia SP., formosa group (Eulophidae)
Chrysonofomyia sp. near lepfocera Waterston (Eiulo-
Levels of parasitism (Figure 1) were lower during the
phidae)
two wet periods of the survey than in the dry season C.
Table 7. Relative abundance of indigenous pzrasitoids of Liriomyza trifolii fn the Cap Vert region of senegal
-
-
-
--.-
.---_---
Total number
of parasitoids
Chrysonotomyia
Period
(- 100%)
Hemiptarsenus
forrnosa leptocera
Cirrospilus
-~.
July-Sept. 82
629*
34.3
53.1 12.1
0.5
Oct.-Dec. 82
137
18.2
43.1 35.8
2.9
Jan.-March 83
2355
51.3
39.0 9.0
0.7
Apn-June 83
598
65.0
25.8
8.7
0.5
_ _ _ _-_- _-_._. -I__-----
* plus 1 Digfyphus isaea.
Biological control of Liriomyza frifoolii in Senegal
293
Table 2. Percentage parasitwn by indigenous parasitojds on Lirlomyza trlfolli in the Cap Vert of Senegal, or? insecflcide freated and
untreated fields
--_---
-
-
Insecticide treated field
Untreated fteld
~.-~ ---.--
-. - -
Total flies
Total flles
and
Percentage
and
Percentage
Month
Locality”
parasitoids
parasitism
Locality*
parasltoids
parasitism
_----.~-------
.--- .--..
~.- .-----.-_ _ _ _ _ _ _
July 82
a
163
26.4
* 13
53.8
e
54
33.3
52
55.8
f
77
10.4
Aug 82
b
142
38.0
145
68.3
a
46
39.1
167
50.9
156
96.2
Sept.- Nov. 82
0**
0**
Dec 82
a
20
45.0
Jan. 83
a
65
98.0
Feb 63
a
55
67.2
March 83
a
1036
96.7
C
48
98.0
b
434
57.8
Apr11 83
a
133
98.5
C
16
97.6
b
737
18.9
May 83
a
9
77.7
b
159
91.3
C
104
88.4
June 83
b
6
50.0
a
11
82.3
C
98
79.4
=a Camherene CDH. b Pikine-Yeumbeul, c Thiaroye sur mer, d tvlalika, e Nlaga, f Berr-Tialane.
* * fly populations very low.
Table 3. Dstrtbutron of Liriomyza trifolii and associated parasitoids in relation to vegetable crops in Trlnjdad,
II----~
Chryso-
?Chryso-
L.
C.
D.
notomyia
Char/s
Eiacherfus
Vegetable
trifolfi
purpureus
callichroma
sp.F
sp.J
C. caribea
sp.L
H. crrculus
-.
-.-I_--
Cowpea
t
t
-4
t
Gub gub
bear
t
t
Hyacmth
bean
t
-r
+
i
+
1-
Tomate
?
+
-t
?-
-t
Sweet
peser
t
t
r
Eggplant
+
+
Celery
L
r
t
Cucumber
t
+
t
Okhra
t
-c
+
t
-t
_.----
p r e s e n t
purpureas favoured the rainy season. when it was often
toids were found associated with this leafminer (Table 4),
the most abundant parasitoid. During the dry season D.
the only common ones being Chrysonotomyia sp. W. and
callichroma was the only abundant parasitoid. On toma-
Diglyphus websteri. Some of the species recorded were
toes, parasitism by this wasp exceeded 60%. The other
similar to those found by Chandler (1982) on melon and
species parasitized a maximum of 5% of all L. trifolii lar-
sweet pepper.
vae. Unfortunately. insecticides were used regularly in all
The Liriomyza parasitoids collected by the University of
of the gardens on most of the vegetables, thereby someti-
Florida and the State Department of Agriculture, Hawaii,
mes abruptly lowering the levels of parasitism.
are listed in Table 4. The parasitoids collected from horti-
cultural areas in Hawaii for this project had originally been
introduced from North, Central and South America in the
Colornbia and United States
late 1970’s for the control of L. trifolii and L. sativae (Lai,
In Colombta, dipterous leafminers were scarce and only
1983). The six species listed became established and are
Diglyphus begini was collected near Piendano (Table 4).
now quite common in the field. In addition, the parasitoids
In the Rio Grande Valley of Texas, Liriomyza ?sativae was
sent by the University of California, Riverside and Berke-
common on ail vegetables irrespective of whether they
ley, from existing cultures are indicated. The four institu-
had been sprayed with insecticide or not. Various parasi-
tions provided cultures of nine species.
2 9 4
P. Neuenschwander et a/.
access to plants, and oviposited and aged faster. In the
refrigerator, survival at 12’C was 3 or 7 days according to
whether they were fed or not before cooling. At 4”C, survi-
val was 8 and 10 days, respectively. It is concluded that
adults cannot be stored for a long time and need sugar
water or honey even when they have access to plants.
Cool storage of pupae depended on their age (Table 5).
Before the pupal moult rnside the puparium, the larvae
proved very sensitive to cold. Pupae held at 12°C l-3 days
after puparium formation, survived better, but because of
early emergence in the refrigerator, cool storage beyond 1
month is not recommended. When pupae were stored at
4”C, survival was only 1% after 2 weeks. Similarly, larvae
inside the leaves could not be stored; all died within 2-4
weeks at 12°C. This information allowed us to ensure a
reliable supply of flies in the insectary.
O
N
D
J
F
M
A
M
J
J
I
I
Exotic parasitoids
8O r rainy
I
dry
1 rainy saasort
I
I
The life-history characteristics, host age preference,
and developmental time of parasitoids brought success-
fully into culture, are Iisted in Table 6. All species attack
and ovipost in/on the host larvae and are solitary. Most of
the eulophids kil1 the host in its mine, but the braconids and
the pteromalid do not kill it until it has formed a pupa from
which the adult parasitoid eventually emerges. Some of
the species listed seem to prefer a particular instar for
oviposition.
II
11
11
11
11
t
Shipment, culture, release and recovery in Senegal
0 N
D J F
M A
M J
J
1982
1983
Species shipped from the Americas to Senegal, and
Figure 7a. Number of Liriomyza trifolii larvae on 70 branches of
their condition at arriva1 and in subsequent cultures in the
fomato (T) and 50 cowpea leaves (C), together with cumulative
insectary, are indicated in Table 7. Of tire 11 species
parasitization rates by Diaulinopsis callichroma (0.c.) and
received, two were lost before releases could be made.
Closterocerus purpureus (Cp.) on lb. tomate and Ic. cowpea, at
Most were kept in culture for a few generations for relea-
Aranguez Gardens, Trinidad.
ses on later dates, Opius dissitus remained in a viable
culture for more than a year.
A few specimens of most species were recovered
Life-history studies
within a few weeks of release, indicating successful
Liriomyza trifolii
breeding in the field. Only Opius dissitus was found regu-
larly. The first small samples taken in May-July 1983 in the
At 27 + 2”C, the eggs of L. trifolii hatched within 2-3
release fields (which are not the same as the extensively
days, and the 3 larval instars fed for 4 days insiae their
sampled fields in Tables 1 and 2) indicate that this exotic
leafmines before dropping to the ground for pupation.
parasitoid became the third most important parasitoid,
Adults emerged about 6-8 days later, whereby emergence
after the indigenous f-l. semialbiclava and Chrysonotomyia
was limited to the period from 6 a.m. to 2 p.m. with a mar-
sp. near formosa.
ked peak from 10-l 1 a.m. This life-cycle of 12-15 days
was not altered significantly when tut bean or tomato lea-
ves were used, provided that proper humidity was main-
tained. These results are in accordance with those
Discussion
reported by Charlton and Allen (1981).
Following its accidental introduction into Senegal, L.
At 27”C, mean survival of unfed adults was 2 days. Flies
trifolii spread throughout the main vegetable growing area
provided with sugar water lived 16 days which corrobora-
of the Cap Vert region which grows about 4500 ha of
tes more extensive data by Vercambre (1980). When flies
vegetables. Additional isolated infestations were found
were given the opportunity to make nutritional stings on
throughout the country. In the Cap Vert, losses in 1981
tomato leaves, survival was 10 days with, and only 2 days
had been dramatic and parasitization rates by H. semial-
without, sugar. Protein hydrolysate (Bumina?) was net
biclava and Chrysonotomyia sp. were relatively low, at 30-
accepted and did not prolong the life span. Thus, ilies fed
40°h (Bourdouxhe, 1982). By the time the biological control
with sugar water alone survived longer than those having
project was initiated in 1982, losses had diminished
Biological control of Liriomyza trifolii in Senegal
2 9 5
Table 4. Survey for parasitoids of Lmomyza spp. in America
-
-
SpecieS
Orlgin
Host plant
Host fly”
-~-~~-
- - - -
Eulophtdae:
Chrysochans carlbea BouEek
Hawaii
vegetables
L.l, L.S.
Chrysochans sp. nr. caribea**
Texas
tomato
L.?S.
Chrysocham parksi (Crawford)
Hawaii
vegetables
L.t., L.S.
southern California
chrysanthemume
L.t.
Chrysonotomyia punctiventris
(Crawford)
Hawaii
vegetables
LI, L.S.
Chrysonotomyfa sp W
Texas
tomate. sweet
pepper, melon
L.?s.
Ciosterocerus purpureus
(Homard)
Texas
sweet pepper
L.?s.
fhg/yphUS
begim Ashmead
central Callfornia
?*
L.t.
Coiombia
chrysanthemum
L.t.
r3glyphus mtermedius
iGirault)
southern California
chrysanthemum*
?
Florida
beans
L.?.
Dlglyphus websteri
(Crawtord)
Texas
tomato, sweet pepper
L.?s.
Pteromalldae.
Haiticoptera Vcfrcutus
(Walker)§
Hawaii
vegetables
LI., L.S.
Eucollldae:
7Dsorqgna sp.@
Hawaii
vegetables
LS., L.S.
3Drsorygna sp. BB
Texas
tomato
L.?s.
Braconrdae.
Op/us drmldiatus (Ashmead)
Florida
chrysanthemuma
3
Oprus dissitus Muesebeck
Florida
beans
L.?t.
Hawaii
vegetables
LS., L.S.
* L.t.
L. tnfoli,, L.s. L L. sat/vae.
** sent as Chrysocharis sp. near girau/tiYoshimoto.
5 sent as Halticopterapatellana(Dalman).
$3 sentas
Cothonasp/s sp.
l from established laboratory cultures.
Table 5 Emergence and mortatity of Liriomyza trifolii larvae (L,) and pupae (P) of different ages following cold storage of 3 months at 72°C.
300 insects per treatment (= 100%) Cambéréne, 7982
-
-
Percentage mortality as
Age at start of
Percentage Flies
cold siorage
Adults inside
Adults emerged
emerged
m day:j
L3 and P
the puparium
in cold storage*
at 25”C**
-_-.--.-.-- .--------.-
L,
untreated
0
3.0
-
97.0
L 99.0
1 . 0
0
0
P
114
d-old
40.0
55.0
2.0
3.0
1 a.7
69.0
3.7
18.6
2 3.7
63.3
23.7
9.3
3 1.7
45.7
41.3
11.3
* after an average of 4.7 weeks for 3 d-old pupae to 7.0 weeks for 1/4 d-old pupae.
** after an average of 2.3 d for 3 d-old pupae to 3.9 d for 1/4
d-old pupae. Control= 5.9 d.
somewhat, and parasitization rates by indigenous parasi-
for introduction into France (J. P. Lyon, pers. Comm.).
toids surpassed the 1981 values rn ail sampled fields
Some of the parasitoids received had already been
which had not been treated with insecticides. Rates of
investigated in the Americas and shown promising attri-
parasitism seemed even higher in thefirst half of 1983. It is
butes. In Trinidad, Diaulinopsis callichroma reached the
conciuded that indigenous eulophids had transferred
highest level of parasitism among seven species. Chryso-
successfully from other leafminers to this new host within
charis parksi had been reported to have a density depen-
a relatively short period. This confirms the polyphagy
dent relationship to L. trifolii populations (Johnson et a/.,
shown by many agromyzid parasitoids (Stegmaier, 1972;
1980) and is now being used in European glasshouses (J.
Murphy, 1984). Thus, rates of parasitism in Africa often
Woets and A. van der Linden, pers. Comm.). Diglyphus
surpassed those recorded from Trinidad (see Figure 1)
begini was the most abundant parasitoid in Southern Cali-
and other countries in the Americas (Pohronezny et a/.,
fornia (Allen and Charlton, 1981), and Halticoptera sp. lis-
1978; Tryon and Poe, 1979; Johnson et a/., 1980) where
ted as aenea (Walker) was dominant in Arizona (Hills and
insecticide pressure is probably higher than in the Cap
Taylor, 1951). The two Opius spp., which were received
Vert. In fact, the African H. semialbiclava has been chosen
from other insectaries, are larval-pupal parasitoids of
.-.-- 1..1_ .” ,... “.~““-----l_.__l--.--
296
P. Neuenschwander et al.
Table 6. Life-hislories of Liriomyza parasitoids
--.-
-
-
Host instar preferred
Species
Life-history
for ,Wiposition
Develepment time*
Additional reference
-
-
-
~..
Chrysocharis
Larval-pupal
Early instars
13da:27”C
a
parksi
endoparsitoid
Chrysonofomyia
Larval
Early instars
11 d ai. 27°C
sp.w
ectoparasitoid?
Diaulinopsis
Larval
Middle-late
Males 11 d
callichroma
ectoparasitoid?
instars
Females 13-l 4 d at 27’ C
Diglyphus
Larval
Lata instars
12 d ai 22°C
b
begini
ectoparasitoid
11-13 cl at 29°C
Diglyphus
Larval
Late instar
13 d at 22°C
d,e
intermedius
ectoparasltoid
14-15 d at 29°C
Halficopfera
Larval-pupal
Early instars
19-23 d at 29°C
circulus
endoparasitoid?
opius
Larval-pupal
All instars
lOdat27”C
f
dimidiatus
endoparasitoid
13-14 d at 29°C
opius
Larval-pupal
Firsl instar
11 dat27”C
dissitus
endoparasitoid
12-14 d at 29°C
-
-.
* agg to adult; at 22 and 27°C from ClBC, Trinidad, at 29”CfrDm CDH, Senegal. a Christieand Parrella. 1982; b Do~n. 1957; c Allen and Charlton,
1981; d Hendrickson and Bath, 1978; e Gordh and Hendrickson, 1979; f Lema and Poe, 1979.
‘Table 7. Cr@in, survival, release, and recovery of Liriomyza trifolii parasitoids sent from Amenca to Sanegal
-
~-
Total
Percentage
Quality of
Local ity and
number
Number of
survival
culture in
dates of
Species
Origin
dispatched
shipments*
at arriva1
Senegal**
releasess
Recovery
-
~-
---. ._~
C caribea
Hawaii
750
3
a5
a
c 4-83
*
C parksi
Hawaii
1360
3
65
b
D 12-82; C 4-83
*
California
154
2
5
C. punctiventris
Hawaii
1100
3
90
a
c 4-83
*?
c.
sp. w
Texas
95
50
a
0. callichroma
Trinidad
885
4
95
b
A l-83 (2x); D l-83,
2-83
*
D. begini
California
100
‘1
90
b
D 10-82; E 2-83
*?
Colombia
163
Z!
70
0. intermedius
Florida
292
%!
95
b
B 2-83, 4-83: C 5-83
California
65
‘1
80
(2x); E 5-83
*§§
H. circulus
Hawaii
1250
3
90
a
A 12-82, 3-83; B 4-83;
C 4-83. 5-83 (2x)
*§§
Disorygna sp.
Hawaii
500
1
20
a
0. dimidiafus
Florida
52
1
95
C
C 9-83 (2x)
*?
0. dissitus
Florida
808
0r,,
90
C
A l-83 (2x), 3-83 (4x),
Hawaii
700
il r,
90
4-83; B 3-83. 4-83
(2x); C 4-83, 5-83 (3x),
6-83 (2x): E 2-83
*§§
--.
*ail parcels arrived within 2-4 d.
**a - lost after a few generations in culture; b .=. maintained at low inumbers in a steady culture; c = good
culture.
§A Cambéréne, B Pikine, C Thiaroye sur mer, D Yeumbeul, E Gueno Mbao.
$5 recovery confirmed by CIE specialist.
wl?ich 0. dimidiatus at least does not prefer the same host
culture and frequent releases at many sites over a long
stages for oviposition as some other species, e.g. Chryso-
period, as well as the fact that it could fil1 an unoccupied
notomyia sp. (Lema and Poe, 1979). Therefore these spe-
ecological niche. The greatest difficulty for these exotic
cies fil1 a n e c o l o g i c a l n i c h e w h i c h w a s v i r t u a l l y
parasitoids in achieving permanent establishment will be
unoccupied in Africa and have a special interest for intro-
the rainy season when host populations are exceedingly
duction. However, a literature review by Murphy (1984)
low. Permanent establishment of any of the exotic spe-
shows that many more candidate species should be tried
cies, their competition with indigenous parasitoids, and,
which could not be imported into Senegal during this pre-
finally, their evenltual efficiency remain to be evaluated.
liminary study.
Biological control with indigenous and exotic parasi-
The first results of the biological control project repor-
toids seems particularly promising for L. trifolii in Africa
ted here indicate that most species passed through at
because insecticide use is still less frequent than in
least one generation in the field following release. Opius
Europe and North America, and because Liriomyza spp.
dissifus did especially weil during the first dry season.
seem’ to reduce yield of vegetables like tomatoes only at
Possible reasons for this achievement are its successful
very high infestation ievels (Levins et a/., 1975).
Biological control of Liriomyza trifolii in Senegal
297
Acknowledgements
GORDH. G. and HENDRICKSON. Jr. R.. 1979. New specles ot
Diglyphus, a world Iist of the specles, taxonomie notes and a
This study was executed in the framework of a one year
key to new world species of Dfglyphus and Daulinopsis
PTC project funded by FAO with a subcontract for explo-
(Hymenoptera: Eulophidae). Proceedings of the Entomologi-
ration work to CIBC. We thank F. Faye and M. Ly, subse-
cal Society of Washington 81, 666-684.
HENDRIKSE, A., ZUCCHI, R., VAN LENTEREN, J. and WOETS, J.,
quept directors of the CDH, and H. van der Veken of the
1980. Dacnusa sibirxa Telenga and Op~us palhpes Wesmael
Senegal/FAO/Belgian
project at the CDH for their conti-
(Hym., Braconidae) In the control of the tomato leafminer
nuoL;s support, J. Beniest and L. de Maeyer from the CDH
Liriomyza bryoniae Kalt. Bullefin S.R.O.P./W.P.R.S. 3, (3). 83-
for their help tn editing the manuscript. J. Woets, Naald-
98.
HENDRICKSON, R. M. Jr. and BATH. S E., 1978. Notes on the
wijk, for information, and particularly S. Diop, CDH, for his
biology of Diglyphus intermedlus (Hymenoptera: Eulophi-
able technical assistance. We also thank the following
dae). a parasite of the alfalfa blotch leafminer, Agromyza
CIEIBritish Museum entomologists for identifications: 1.
frontella (Diptera, Agromyzidae). Proceedings of the Entomo-
M. White (Agromyzidae), Z. BouEek (Eulophidae), B. R.
logical Society of Washington 80, 210-215.
Subba Rao (Pteromalidae), A. D. Austin and G. E. J. Nixon
HILLS, D. A. and TAYLOR, E. A.. 1951 Parasitization of dipterous
leafminers in cantaloups and lettuce in the Salt River Valley,
(Braconidae). J. Quinlan (Eucoilidae), and R. A. Wharton
Arizona. Journal of Economie Entomology 44, 759-762.
from Texas A&M University for additional comments on
JOHNSON, M. W.. OATMAN, E. R. and WYMAN, J. A., 1980. Natu-
the braconids. Finally we would like to thank all the ento-
ral control of Liriomyza sativae (Dip: Agromyzldae) in pole
molog!sts in the collaborating institutions who provided
tomatoes in southern California. Entomophaga 25, 193-198.
us with help and species from their cultures, and D. J.
LAI, P., 1983. Biological control of hiomyza In Hawaii. Biocontrol
News and Information 4 (3), 195.. 196.
Greathead (CIBC, London) and L. Brader (FAO, Rome) for
LEMA, K. M. and POE, S. L., 1979. Age specific mortality of L/rio-
coordinating the project and for reviewing the manuscript,
myza sativae due to Chrysonotomy/a formosa and parasitiza-
tion by Opius dimidlatus and Chrysonotomy/a formosa.
Environmental Entomology 6, 935-937.
LEVINS, R. A., POE, S. L. and JONES, J. P.. 1975. Effectlveness of
a leafminer control program for Florida tomato production.
Journal of Economie Entomology 62, 772-774.
MURPHY, S. T., 1984. Final report on surveys in the Neotropical-
/Nearctic region for natural enemies of Liriomyza trifolii and
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