Ann. appl. Biol.

(2003), 143:187-193
Printed in UK 187

Effects of Melia azedarach (Meliaceae) fruit extracts on the leafminer

Liriomyza huidobrensis (Diptera, Agromyzidae): Assessment in laboratory and
field experiments
By E BANCHIO1, G VALLADARES1*, M DEFAGÓ1, S PALACIOS2 and C CARPINELLA2
1
Centro de Investigaciones Entomológicas de Córdoba, FCEFYN, Universidad Nacional de Córdoba, Av.
Vélez Sársfield 299, (5000)-Córdoba, Argentina
2
Agencia Córdoba Ciencia, Unidad Ceprocor, Alvarez de Arenales 230, (5004)-Córdoba, Argentina

(Accepted 9 April 2003; Received 19 November 2002)

Summary

Control of the widely distributed pest Liriomyza huidobrensis is complicated due to the protected
habit of the leafmining larvae, and their resistance to insecticides. The effects of Melia azedarach
(Meliaceae) fruit extracts against adults and larvae of L. huidobrensis were investigated. In the laboratory,
leaves of Cucurbita sp. infested with first and third instar larvae were treated with different extract
solutions. Larval and pupal survival, as well as wing-spread of adults, were assessed. Female adult
behaviour towards the extract was also analysed in terms of number of feeding punctures and number
of offspring left on treated/untreated leaves. In the field, an infested Vicia faba crop was sprayed four
times at weekly intervals with plant extract, water, and a blank solution. The number of adult leafminers
and parasitoids emerging from sampled leaves from each treatment were compared. The laboratory
tests showed translaminar action of the extracts, which negatively affected leafminer pupal survival,
while body size was not affected. The extracts also deterred feeding by adult females and may also
have caused reduction in oviposition rates. All solutions and concentrations tested had similar effects.
In the field, extract effects were consistent with those from laboratory trials, number of pupae and
pupal survival being lower on treated plants. Percentage parasitism was not affected by plant extract
treatment, suggesting a selective activity.

Key words: Liriomyza huidobrensis, Melia azedarach, botanical pesticides

Introduction The use of conventional synthetic insecticides for

The leafminer Liriomyza huidobrensis (Blanchard)
(Diptera: Agromyzidae) was originally described
from central Argentina (Blanchard, 1926), and has
recently reached high levels of infestation on
different crops in the region (Salvo & Valladares,
1995; Valladares et al., 1996, 1999a). It is currently
known to occur throughout the Americas (Sanabria
de Arévalo, 1994), having been introduced to Europe
(Cabello et al., 1993), Hawaii (Schreiner, 1993) and
more recently to Israel, as a chemically resistant pest
(Weintraub & Horowitz, 1995), and continues
spreading to new areas (Weintraub, 2001a).
Though known as the “pea leafminer”, this highly
polyphagous species has been recorded from 14 plant
families (Spencer, 1990) and has a serious economic
impact on many crops along its distribution area
(Spencer, 1973; Parrella, 1982; Yabar, 1988). Larvae
and female adults damage plants, the former by
tunneling through the mesophyll thus reducing
photosynthetic rates, and the latter by puncturing
leaves with their ovipositor, for feeding and egg-
laying (Spencer 1973; Parrella et al., 1985).
controlling pests in the genus Liriomyza Mik, has
led to development of resistant leafminer strains
(Parrella et al., 1983; Keil et al., 1985; Mason &
Johnson, 1988; Parrella & Trumble, 1989) and rapid
elimination of their natural enemies, resulting in an
increase in the leafminer population (Johnson et al.,
1980; Suenaga et al., 1995). Besides, the larval stage
is protected from the effect of insecticides by being
located inside the foliar tissue (Harris et al., 1990).
Alternative means of leafminer pest control have
received attention in recent years, including plant
resistance (Suenaga et al., 1995, Dogimont et al.,
1999), selective translaminar insecticides (Weintraub
& Horowitz, 1998), and particularly botanical
pesticides, mainly from neem (Azadirachta indica)
extracts (Stein & Parrella, 1985; Lindquist et al.,
1986; Larew, 1988; Parkman & Pienkowski, 1990;
Weintraub & Horowitz, 1997).
Extracts from the chinaberry tree (Melia
azedarach L., Meliaceae) are known to affect
development and behaviour of various insect species
(Palacios et al., 1993; Huang et al., 1994; Lee &
Shih, 1995; Schmutterer, 1995; Valladares et al.,

*Corresponding Author E-mail: grv@onenet.com.ar

© 2003 Association of Applied Biologists

188 E BANCHIO ET AL.

1997, 1999b; Abou-Fakhr Hammad et al., 2000a,b).
In a field study, Abou-Fakhr Hammad et al. (2000a)
reported a decrease in numbers of Liriomyza
huidobrensis larvae following applications of M.
azedarach extracts; the mechanisms involved in such
effects were not addressed. In the present paper we
analyse the effects of M. azedarach fruit extracts on
feeding and oviposition behaviours of L.
huidobrensis adult females, as well as translaminar
effects on leafminer larvae survival and size.
Materials and Methods
Plant extracts
Ripe fruits collected from trees of M. azedarach
in Córdoba city, Argentina, were air-dried and
Soxhlet extracted with ethanol after fat removal with
hexane (yield 28.8%). The extract was then
evaporated under vacuum and the residue was
diluted in water to obtain concentrations of 10% and
20%. The main active compound in this extract has
been described as meliartenin (Carpinella et al.,
2002) which was present in a concentration of 0.16
µg g-1 of crude extract.
The following treatments were used: 1) original
plant extract only (pH of 3-4) versus water as control;
2) plant extract plus 0.5% Tween-20, versus a control
of water + 0.5% Tween-20; 3) plant extract plus 0.5%
Tween-20, adjusted to pH 7 (control as for the
previous treatment).
Laboratory assays
Adults of L. huidobrensis reared from mined
leaves collected in Vicia faba crops in Córdoba,
central Argentina, were used in the laboratory trials,
within 3-6 days of their emergence. Seedlings of
Cucurbita maxima Duch. “courgettes”
(Curcubitaceae), grown in the laboratory, were used
for adult feeding and as the substrate for the
bioassays. All experiments were carried out at room
temperature and 12:12 h photoperiod.
Translaminar effects on first instar larvae were
assessed by exposing courgette seedlings (two
primary leaves) to a colony of L. huidobrensis (15
flies of each sex) for 24 h. Plants were examined
daily and, when larval mines appeared, leaves were
painted on both the upper and lower epidermis, with
either plant extract (“treatment” plants) or water
(with 0.5% Tween when corresponding)
(“controls”). After 7-10 days, as larvae appeared
fully grown, the leaves were cut and placed
individually in small plastic bags to allow leafminers
to pupate. For each plant and leaf, the initial number
of larvae, their pupation date, number of pupae, as
well as number, sex and wing length of adults were
recorded. Translaminar effects were also assessed
on third instar larvae by applying the treatments 7
days after plant exposure to the flies. In this case
leaves were cut and placed in bags on the day after
extract application. The number of replicates for each
treatment is indicated in Table 1.
Effects on feeding and oviposition by adult females
were assessed by exposing five seedlings, previously
painted with extract (10% and 20% concentration)
or water as a control, to colonies of the leafminer
for 24 h. The number of punctures per cm2 of foliar
area was estimated for each plant. Further effects
on oviposition and larval development were

Table 1. Larval mortality rates and adult body size of L. huidobrensis after foliar application of M. azedarach
fruit extract on C. maxima leaves containing a) first instar and b) third instar larvae
% Larval mortality* Female wing length (mm)* Male wing length (mm)*
Extract solution Extract ± SE (n) Control ± SE (n) Extract ± SE (n) Control ± SE (n) Extract ± SE (n) Control ± SE (n)
a) First instar
10% 26 ± 7 (46) 11 ± 4 (50) 2.05 ± 0.16 (8) 2.03 ± 0.06 (17) 1.73 ± 0.03 (16) 1.73 ± 0.04 (28)
10% + Tween 34 ± 8 (20) 25 ± 6 (33) 1.77 ± 0.05 (4) 1.86 ± 0.06 (18) 1.56 ± 0.06 (5) 1.65 ± 0.03 (27)
10 + Tween, pH 7 31 ± 5 (36) 29 ± 6 (33) 2.17 ± 0.14 (3) 1.96 ± 0.03 (37) 1.72 ± 0.02 (16) 1.65 ± 0.02 (27)
20% 11 ± 5 (31) 10 ± 3 (40) 1.93 ± 0.04 (11) 1.96 ± 0.08 (8) 1.59 ± 0.04 (11) 1.66 ± 0.04 (7)
20% + Tween 32 ± 6 (41) 20 ± 4 (46) 1.27 ± 0.01 (2) 2.00 ± 0.03 (21) 1.72 ± 0.03 (12) 1.73 ± 0.03 (22)
20 + Tween, pH 7 39 ± 8 (23) 41 ± 6 (32) 1.96 ± 0.06 (8) 2.09 ± 0.03 (27) 1.89 ± 0.02 (2) 1.79 ± 0.02 (21)

b) Third instar
10% 31 ± 6 (46) 11 ± 4 (50) 1.93 ± 0.05 (3) 1.97 ± 0.04 (9) 1.64 ± 0.03 (9) 1.70 ± 0.02 (5)
10% + Tween 35 ± 8 (20) 25 ± 6 (33) 2.04 ± 0.04 (2) 2.13 ± 0.03 (19) 1.72 ± 0.05 (5) 1.76 ± 0.02 (25)
10 + Tween, pH 7 31 ± 5 (36) 29 ± 6 (33) 1.98 ± 0.11 (4) 2.06 ± 0.05 (22) 1.81 ± 0.03 (7) 1.69 ± 0.04 (27)
20% 11 ± 3 (31) 10 ± 3 (40) 2.10 ± 0.02 (6) 2.06 ± 0.06 (11) 1.76 ± 0.04 (10) 1.78 ± 0.02 (9)
20% + Tween 31 ± 6 (41) 20 ± 3 (46) 1.76 ± 0.02 (2) 2.02 ± 0.14 (2) 1.72 ± 0.02 (2) 1.62 ± 0.14 (3)
20 + Tween, pH 7 9 ± 3 (23) 16 ± 6 (32) 2.15 ± 0.15 (2) 2.08 ± 0.02 (33) 1.78 ± 0.04 (6) 1.79 ± 0.02 (32)
* Means (n in brackets) were not significantly different between extract and control treatments (Kruskall Wallis, P > 0.05).
 Effects of Melia azedarach extracts on Liriomyza huidobrensis
evaluated by assessing the initial number of mines,
number of pupae, pupal weight, as well as number
and wing length of adults. The experiment was
repeated three times.
Field assays
Within a crop of V. faba grown at the outskirts of
Córdoba city, plants in two rows (30 m long) were
sprayed four times at weekly intervals, with the
following treatments: i) extract (10% M. azedarach
and 0.5% Tween-20 at neutral pH), ii) water, or iii)
a solution of 0.5% Tween-20. The average
temperature during the experiment was 15°C (min.
7°C, max. 20°C) and only one slight precipitation
was recorded. Treatments were applied following
an alternate pattern and leaving three untreated plants
between treated ones. The apical third of each
treatment plant was marked with tape at the
beginning of the experiment, and only leaves above
the mark were sprayed with 7-10 cc of extract.
Thirteen plants were allocated to each treatment. The
leaf nearest to the mark was collected weekly from
the treated part of all experimental plants and from
13 plants randomly chosen within the main crop,
treated with the commercial pesticide Tamaron
(active ingredient Methamidophos). Leaves were
kept in plastic bags to obtain leafminer pupae and
larval parasitoids. Pupae were transferred to glass
tubes until adults (flies and larvo-pupal parasitoids)
emerged. Numbers of pupae, flies and parasitoids
obtained from each leaf were recorded.
Data analysis
Either t tests or Mann-Whitney U tests (if data
were not normally distributed) were used for
comparisons between extract treatments and their
respective controls. Comparisons among the
different extract treatments were made by Analysis
of Variance (ANOVA), or Kruskall Wallis followed
by the Mann-Whitney U test. Percentages were
angularly transformed and laboratory mortality rates
were corrected for those of the corresponding
controls by using Abbott´s formula (Abbott, 1925).
Results
Laboratory assays
Translaminar effects
No significant effects on larval mortality were
observed (Table 1), when the extracts were applied
on leaves containing either newly emerged or mature
larvae (Mann-Whitney tests, P > 0.05). However,
pupal mortality increased dramatically after extract
application on the leaves, being significantly higher
than that of the respective controls (Mann-Whitney
tests, P < 0.05), when either first or third instar larvae
were exposed to the treatments. Pupal mortality rates
(Fig. 1) corrected for control values (0.49 ± 0.03)
189
by Abbott’s formula did not differ significantly
among the studied concentrations and solutions
(ANOVA, F = 0.76, df = 5, n = 188, P = 0.58 , and F
= 1.07, df = 5, n = 189, P = 0.37, for first and third
instar application, respectively).
When body size (as indicated by wing length) was
considered, no consistent significant differences
(Mann-Whitney, P > 0.05) were detected between
insects developed on treated and untreated leaves
(Table 1).
Effects on feeding and oviposition by adult females
Leaves treated before exposure to L. huidobrensis
females received up to 90% fewer punctures (Fig.
2) than the controls (Kruskall Wallis, H = 159.37, P
< 0.001), with no obvious differences among extract
concentrations and/or solutions. Plants treated with
10% and 20% extract prior to oviposition resulted
in fewer pupae (Mann-Whitney, U10% = 142, U20% =
406, P < 0.05) but neither larval (Mann-Whitney,
U10% = 212.5, U20% = 556.5, P > 0.05) nor pupal
survival (Mann-Whitney, U10% = 173.5, U20% = 530,
P > 0.05) were affected (Table 2).
Field assays
Results from the field trials confirmed those
obtained in the laboratory. Plants treated with M.
azedarach extract (10% + Tween-20) yielded up to
50% fewer pupae (Fig. 3a) than any other treatment
(ANOVA, F = 7.32, df = 3, n = 202, P = 0.0001).
Pupal survival was also affected (ANOVA, F =
20.12, df = 3, n = 179, P = 0.0000), being lowest in
leaves treated with M. azedarach extracts, and
highest in those treated with Tamaron (Fig. 3b).
Parasitism rates were also affected (ANOVA, F =
11.03, df = 3, n =160, P = 0.0000), the most
noticeable difference concerning Tamaron treated
plants, where parasitism was lowest (Fig. 3b).
Discussion
In the laboratory trials, external application of M.
azedarach fruit extract on leaves containing L.
huidobrensis first or third instar showed a
translaminar effect, resulting in increased pupal
mortality rates (i.e. lower adult emergence), though
larval survival was unaffected.
Similar results were obtained whether extracts
were applied on first or third instar leafmining larvae.
These results resemble the effects recorded by using
the synthetic insecticides permethrin and parathion
(Parrella, 1982; Parrella et al., 1982), or the plant-
derived azadirachtin (Stein & Parrella, 1985), all of
which allowed larvae of Liriomyza trifolii (Burgess)
to pupate normally, but affected pupal survival.
Similarly, treatment with a juvenile hormone mimic
had no effect on pupation of L. trifolii, but adult
emergence was drastically reduced (Parrella et al.,
 190 E BANCHIO ET AL.

a)
100
% adjusted pupal mortality

80

60
40

20

0
Extract (10%) Extract (10%) + Extract (10%) + Extract (20%) Extract (20%) + Extract (20%) +
Tween-20 Tween-20 (pH 7) Tween-20 (pH 7) Tween-20 (pH 7)
Treatments

b)
100
% adjusted pupal mortality

80

60
40

20

0
Extract (10%) Extract (10%) + Extract (10%) + Extract (20%) Extract (20%) + Extract (20%) +
Tween-20 Tween-20 (pH 7) Tween-20 (pH 7) Tween-20 (pH 7)
Treatments
Fig. 1. Adjusted (by Abbott´s formula) mean (± SE) pupal mortality of L. huidobrensis after application of various
solutions of M. azedarach fruit extract on leaves infested with a) first instar larvae and b) third instar larvae.

25
No. punctures cm-2

20
15
10
5
0
Control Extract (10%) Extract (10%) Extract (10%) Extract (20%) Extract (20%) Extract (20%)
+ Tween-20 + Tween-20 + Tween-20 + Tween-20
(pH 7) (pH 7)
Treatments
Fig. 2. Mean (± SE) number of L. huidobrensis feeding punctures per cm2 on C. maxima leaves treated with various
solutions of M. azedarach fruit extract. Data on control plants were pooled since they did not show significant
differences.

Table 2. Effects of foliar application of M. azedarach fruit extracts to C. maxima seedlings before exposure to L.
huidobrensis
10% extract 20% extract
Treatment ± SE (n) Control ± SE (n) Treatment ± SE (n) Control ± SE (n)
Mines 2.50 ± 0.22 (28)a* 4.66 ± 0.37 (24)b 2.93 ± 0.47 (30)a 4.27 ± 0.27 (40)b
% Larval mortality 4 ± 4 (22)a 15 ± 6 (24)a 17 ± 6 (30)a 20 ± 5 (40)a
% Pupal mortality 35 ± 7 (21)a 53 ± 7 (23)a 59 ± 8 (27)a 56 ± 7 (37)a
Pupae 2.45 ± 0.27 (21)a 4.00 ± 0.43 (23)b 2.36 ± 0.47 (27)a 3.50 ± 0.31 (37)b
* Means followed by the same letter were not significantly different between extract and control (Mann-Whitney, P > 0.05).
 Effects of Melia azedarach extracts on Liriomyza huidobrensis 191

6 azedarach extracts can penetrate the leaf tissues

without any added surfactant; moreover, the
5 observed effects could not be attributed to the acidity
of the extracts. Lower concentrations should be
tested in order to further assess dose dependent
No. pupae leaf-1

4
effects.
3 Since female body size can be related to potential
fecundity of leafminers (Valladares & Lawton,
2 1991), the lack of significant effects on body size
(based on wing length) suggests that chinaberry
1 extract might not affect such potential in L.
huidobrensis. However, effects on reproduction of
0 L. trifolii have been shown for neem extracts
Pupae (Parkman & Pienkowsky, 1990), and can not be ruled
out from the information available in our case.
b) 80 Melia azedarach extracts also acted as oviposition
and feeding deterrents for the leafmining females.
These effects seem stronger than what could be
60 expected for neem insecticides, from the reports of
Weintraub & Horowitz (1997) on L. huidobrensis,
Percentage

and those of Larew (1988) and Webb et al. (1983)

40
20
0 with neem extract application on L. trifolii (Stein &
Pupal mortality Parasitism
Fig. 3. Results from field application of M. azedarach
extract on a) mean (± SE) number of pupae and b)
mortality and parasitism rates of L. huidobrensis
developing in a V. faba crop at central Argentina.
Unshaded bars = Extract (10%) + 0.5 Tween-20; light
grey bars = 0.5 Tween-20; dark grey bars = synthetic
insecticide; black bars = water.
1983). Physiological studies should be undertaken
to discern whether a hormonal mechanism is
involved in the effects of M. azedarach extracts on
L. huidobrensis. The same trend (no effects on
pupation but significant reduction in adult
emergence), was recorded for a neem insecticide
applied as a leaf dip on plants containing first instar
larvae of L. huidobrensis (Weintraub & Horowitz,
1997). In that study, soil drenching with the neem
compound also resulted in more dramatic effects on
pupal eclosion than on larval mortality, particularly
for treatments on first instar larvae. It should be noted
that larvicidal effects of neem extracts on L.
huidobrensis and other Liriomyza species have also
been recorded in some cases (Webb et al., 1983;
Larew, 1986; Weintraub & Horowitz, 1997);
differences from the results discussed above could
be attributed to a number of variables including
solutions and application protocols.
In laboratory bioassays, results were independent
of the solution employed indicating that M.
on L. sativae and L. trifolii. The strong deterrency
of M. azedarach extracts here reported agrees with
previous observations on other insects (Valladares
et al., 1997, 1999a, and a manuscript under revision),
showing antifeedant and repellent activities as the
main extract effect. Similar effects were observed
Parrella, 1985) and with the application of synthetic
insecticides on the same leafminer (Robb & Parrella,
1985; Smith, 1986).
The lack of noticeable effects on leafminer survival
when leaves were treated before exposure to L.
huidobrensis contrasts with the high mortality
observed when leaves infested with larvae I or III
were treated. This observation suggests a shorter
residual activity for M. azedarach extracts than that
of a neem insecticide used against L. huidobrensis
in a comparable experiment (Weintraub & Horowitz,
1997). Moreover, a steady decline in mortality from
day 0 to day 7 after treatment with neem has been
observed for L. sativae (Webb et al., 1983). In our
work, larval development of L. huidobrensis took
7-12 days, so weekly applications might be
necessary if M. azedarach extracts were to be used
to protect a crop from this leafminer. Such a
treatment schedule has been proposed for other
phytochemical pesticides with relatively quick
degradability (Abou-Fakhr Hammad et al., 2000a).
Vicia faba plants that were sprayed with M.
azedarach extract in the field allowed for fewer
pupae to be reared from extract treated leaves. As
larval survival was not affected by extract treatment
in laboratory experiments, and considering the strong
deterrent effects on leafminer females, these
differences could be attributed to a dissuasive effect
on oviposition. The relative decrease in adult
emergence from those pupae, as compared with all
192 E BANCHIO ET AL.
other field treatments, agrees with the laboratory
findings. Although incorporating Tween-20 did not
show effects on extract activity in the laboratory,
the extract by itself might have behaved differently
under field conditions. Further tests should be carried
out to analyse possible extract and surfactant additive
or synergetic effects in the field.
The delayed action of these extracts, with
leafminers being allowed to pupate and slowly killed,
could be advantageous in conserving parasitoid
populations, since fast acting compounds might kill
the hosts before parasitoids had a chance to develop
(Weintraub, 1999). This hypothesis appears to be
supported by the lack of noticeable effects of
chinaberry extract on parasitism rates. Detrimental
effects on parasitoids of Liriomyza spp., as shown
here for the synthetic insecticide Tamaron, represent
a serious drawback of many known insecticides, not
just conventional ones (Johnson et al., 1980) but also
selective translaminar insecticides like cyromazine
and abamectin (Weintraub & Horowitz, 1998;
Weintraub, 2001b; but see Parrella et al., 1983).
The results we report are important considering
the great diversity of crops being affected by the
leaf miner L. huidobrensis and its resistance to
synthetic insecticides. Particularly encouraging is the
feeding and ovipositing deterrent activity exhibited
by the fruit extract of M. azedarach, and its negative
effect on pupal survival which can be related to
possible growth regulatory effect, which pose
interesting perspectives for the use of this extract
within a leafminer management programme.
Acknowledgements
We are grateful to A Mangeaud for statistical
advice, to the Torres family for letting us use their
field, and to two anonymous referees. This research
was supported by Secretaría de Ciencia y Tecnología,
Universidad Nacional de Córdoba.
References
Abbott W S. 1925. A method of computing the effectiveness
of an insecticide. Journal of Economic Entomology 18:265-
267.
Abou-Fakhr Hammad E M, Nemer N M, Kawa R N S.
2000a. Efficacy of Chinaberry tree (Meliaceae) aqueous
extracts and certain insecticides against the pea leafminer
(Diptera: Agromyzidae). Journal of Agricultural Science
134:413-420.
Abou-Fakhr Hammad E M, Nemer N M, Hawi Z K, Hannal
L T. 2000b. Responses of the sweetpotato whitefly, Bemisia
tabaci, to the chinaberry tree (Melia azedarach L.) and its
extracts. Annals of Applied Biology 137:79-88.
Blanchard E. 1926. A dipterous leaf-miner on Cineraria, new
to science. Revista de la Sociedad Entomológica Argentina
1:10-11.
Cabello T, Jaimez R, Belda J, Pascual F. 1993. El minador
sudamericano, una nueva plaga de los cultivos hortícolas.
Hortofruticultura 5:43-46.
Carpinella M C, Ferrayoli G C, Valladares G, Defagó M,
Palacios S. 2002. Potent insect antifeedant limonoid from
Melia azedarach. Bioscience, Biotechnology, and
Biochemistry 66:1731-1736.
Dogimont C, Bordat D, Pages C, Boissot N, Pitrat M. 1999.
One dominant gene conferring the resistance to the leafminer
Liriomyza trifolii (Burgess) Diptera: Agromyzidae in melon
(Cucumis melo L.). Euphytica 105:63-67.
Harris M A, Begley J W, Warkentin D L. 1990. Liriomyza
trifolii (Diptera: Agromyzidae) supression with foliar
applications of Steinernena carpocapsae (Rhabditida:
Steinernematidae) and abamectin. Journal of Economic
Entomology 86:2380-2384.
Huang R C, Okamura H, Iwagawa T, Nakatani M. 1994.
The structures of Azedarachtins, limonoid antifeedants from
Chinese Melia azedarach Linn. Bulletin of the Chemical
Society of Japan 67:2469-2472.
Johnson M W, Oatman E R, Wyman J A. 1980. Effects of
insecticides on populations of the vegetable leafminer and
associated parasites on fall pole tomatoes. Journal of
Economic Entomology 73:67-71.
Keil C B, Parrella M P, Morse J G. 1985. Method for
monitoring and establishing baseline data for resistance to
permethrin by Liriomyza trifolii (Burgess). Journal of
Economic Entomology 78:419-422.
Larew H G. 1986. Use of neem seed kernel extract in a
developed country: Liriomyza leafminer as a model case.
Proceedings of the 3rd International Neem Conference,
Nairobi, Kenya, pp. 375-385.
Larew H G. 1988. Limited occurrence of foliar, root, and seed
applied Neem seed extract toxin in untreated plant parts.
Journal of Economic Entomology 81:593-598.
Lee S Z, Shih C J. 1995. Antifeedant and repellent effects of
Melia azedarach seed kernel extracts on Spodoptera litura.
Plant Protection Bulletin 37:227-232.
Lindquist R, Casey M, Kruger H. 1986. Evaluation of neem
seed extract, a natural plant product, for leafminer control on
chrysanthemum. Ohio Florist’s Association 680:7-8.
Mason G A, Johnson M W. 1988. Tolerance to permethrin and
fenvalerate in hymenopterous parasitoids associated with
Liriomyza spp. (Diptera: Agromyzidae). Journal of Economic
Entomology 81:123-126.
Palacios S, Valladares G, Ferreyra D. 1993. Preliminary results
in the searching for an insecticide from Melia azedarach
extracts. In Practice Oriented Results on Use and Production
of Neem-Ingredients and Pheromones, pp. 99-105. Ed. H
Kleeberg. Wezlar, Germany: Trifolio-N.
Parkman P, Pienkowski R. 1990. Sublethal effects of neem
seed extract on adults of Liriomyza trifolii (Diptera:
Agromyzidae). Journal of Economic Entomology 83:1246-
1249.
Parrella M P. 1982. A review of the history and taxonomy of
economically important serpentine leafminers (Liriomyza
spp.) in California (Diptera: Agromyzidae). Pan-Pacific
Entomology 58:302-308.
Parrella M P, Trumble T J. 1989. Decline of resistance in
Liriomyza trifoIii (Diptera: Agromyzidae) in the absence of
insecticide selection pressure. Journal of Economic
Entomology 82:365-368.
Parrella M P, Robb K L, Bethke J. 1983. Influence of
selected host plants on the biology of Liriomyza trifolii
(Diptera: Agromyzidae). Annals of the Entomological Society
of America 76: 112-115.
Parrella M P, Robb K L, Morishita P. 1982. Response of
Liriomyza trifolii (Diptera: Agromyzidae) larvae to
insecticides, with notes about efficacy testing. Journal of
Economic Entomology 75:1104-1108.
Parrella M P, Jones V P, Youngman R R, Lebeck L M. 1985.
Effect of leaf mining and leaf stippling of Liriomyza spp. on
photosynthetic rates of chrysanthemum. Annals of the
 Effects of Melia azedarach extracts on Liriomyza huidobrensis
Entomological Society of America 78:90-93.
Robb K, Parrella M P. 1985. Antifeeding and oviposition-
deterring effects of insecticides on adult Liriomyza trifolii
(Diptera: Agromyzidae). Journal of Economic Entomology
78:709-713.
Salvo A, Valladares G. 1995. Complejo parasítico
(Hymenoptera: Parasitica) de Liriomyza huidobrensis
(Diptera: Agromyzidae) en haba. Agriscientia 12:39-47.
Sanabria de Arévalo I. 1994. Insectos minadores (Diptera:
Agromyzidae) de la sabana de Bogotá (Cundinamarca,
Colombia). Revista Colombiana de Entomología 20:61-100.
Schmutterer H. 1995. The Neem Tree. Azadirachta indica A.
Juss. and Other Meliaceous Plants. Weinheim: VCH. 696
pp.
Schreiner I. 1993. Impact of Liriomyza trifolii (Diptera:
Agromyzidae) and other pest on yields of yard-long beans.
Proceedings of the Hawaiian Entomological Society 32:131-
138.
Smith R. 1986. Efficacy of selected insecticides against
Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) a
leafminer of chrysanthemum. Canadian Entomologist
118:761-766.
Spencer K A. 1973. Agromyzidae (Diptera) of Economic
Importance. Vol. 9. Dr W Junk: The Hague. 418 pp.
Spencer K A. 1990. Host Specialization in the World
Agromyzidae (Diptera). London: Kluwer Academic
Publishers. 444 pp.
Stein U, Parrella M P. 1985. Seed extract shows promise in
leafminer control. California Agriculture July-Agust, pp. 19-
21.
Suenaga H, Ishida K, Tanaka A. 1995. Comparison of
susceptibility of Dendranthema grandiflora (Tzvel) cultivars
to leafminer, Liriomyza trifolii (Burgess) (Diptera:
Agromyzidae). Japanese Journal of Applied Entomology and
Zoology 39:245-251.
Valladares G, Lawton J H. 1991. Host-plant selection in the
holly leaf-miner: does mother know best? Journal of Animal
Ecology 60:227-240.
Valladares G, Pinta D, Salvo A. 1996. La mosca minadora
Liriomyza huidobrensis (Blanchard) en cultivos hortícolas
de Córdoba. Horticultura Argentina 15:1-6.
193
Valladares G, Salvo A, Videla M. 1999a. Moscas minadoras
en cultivos de Argentina. Horticultura Argentina 18: 56-61
Valladares G, Defagó M T, Palacios S, Carpinella M C. 1997.
Laboratory evaluation of Melia azedarach (Meliaceae)
extracts against the Elm leaf beetle (Coleoptera,
Chrysomelidae). Journal of Economic Entomology 90:747-
750.
Valladares G, Ferreyra D, Defagó M T, Carpinella M C,
Palacios S. 1999b. Effects of Melia azedarach on Triatoma
infestans. Fitoterapia 70:421-424.
Webb R E, Hinebaugh M A, Lindquist R K, Jacobson M.
1983. Evaluatioin of aqueous solution of Neem seed extract
against Liriomyza sativae and L. trifolii (Diptera:
Agromyzidae). Journal of Economic Entomology 76:357-
362.
Weintraub P G. 1999. Effects of cyromazine and abamectin
on the leafminer Liriomyza huidobrensis and its parasitoid,
Diglyphus isaea, in celery. Annals of Applied Biology
135:547-554.
Weintraub P G. 2001a. Changes in the dynamics of the
leafminer, Liriomyza huidobrensis, in Israeli potato fields.
International Journal of Pest Management 47:95-102.
Weintraub P G. 2001b. Effects of cyromazine and abamectin
on the pea leafminer Liriomyza huidobrensis (Diptera:
Agromyzidae) and its parasitoid Diglyphus isaea
(Hymenoptera: Eulophidae) in potatoes. Crop Protection
20:207-213.
Weintraub P G, Horowitz A R. 1995. The newest leafminer
pest in Israel, Liriomyza huidobrensis. Phytoparasitica
23:177-184.
Weintraub P G, Horowitz A R. 1997. Systemic effects of a
Neem insecticide on Liriomyza huidobrensis larvae.
Phytoparasitica 25:283-289.
Weintraub P G, Horowitz A R. 1998. Effects of translaminar
and conventional insecticides on Liriomyza huidobrensis
(Diptera: Agromyzidae) and Diglyphus isaea (Hymenoptera:
Eulophidae) populations in celery. Journal of Economic
Entomology 91:1180-1185.
Yabar E. 1988. La Mosca minadora de la Papa en el Perú.
Lima: Instituto Nacional de Investigación Agraria y
Agroindustrial.
194 E BANCHIO ET AL.