Proceedings
of The World Avocado Congress III, 1995 pp. 419 - 428
AVOCADO
PESTS IN ISRAEL
E. Swirski and M. Wysoki Y. Izhar
Department of Entomology Extension Service
A.R.O.,
The Volcani Center Ministry of
Agriculture
Bet
Dagan 50250, Israel Tel Aviv
61700, Israel
Contribution from the Agricultural Research
Organization, No. 1735-E, 1995 series.
Key Words: Avocado pests, natural enemies, integrated control,
Israel.
Abstract
A survey of avocado groves throughout Israel was
begun in 1969 and continued into 1995. During this period 94 species of avocado
pests belonging to 45 families of insects, mites, birds and mammals, were
recorded. Outbreaks of the long-tailed mealybug, Pseudococcus longispinus, resulting
from the drift of aerial sprays from adjacent cotton fields, were controlled by
limiting such sprays and by releases of the parasites Arhopoideus peregrinus
and Anagyrus Jusciventris. The Japanese bayberry whitefly, Parabemisia myricae, introduced into Israel in the
late 1970s, is successfully controlled by the imported Californian parasite Eretmocerus
debachi. Since 1980 the pyriform scale, Protopulvinaria pyriformis, has
been an important pestofavocado; itiscontrolled by the exotic parasite Metaphycus
stanleyi and by the application of mineral oils. As only young caterpillars
of the giant looper, Boarmia selenaria, are susceptible to Bacillus
thuringiensis preparations, a monitoring system was developed using virgin
female traps and scouting. B. thuringiensis is used as well against the
honeydew moth, Cryptoblabes gnidiella, and the carnation leafroller, Cacoecimorpha
pronubana. The parasite Thripobius semiluteus, imported from
California for biocontrol of the greenhouse thrips, Heliothrips
haemorrhoidalis, has become established in numerous groves. Sabadilla was
found to be effective against the black vine thrips, Retithrips syriacus. The
appearance of sporadic, minor and potential pests is discussed. An Integrated
Pest Management system has been developed in the avocado groves of Israel.
1. Introduction
The first comprehensive list
of avocado pests in Israel was published over 40 years ago by Avidov and Ben Haim
(1950). In order to prevent the possible sudden and unexpected appearance of a
new pest and/or outbreaks of a local one, owing to agrotechnical changes, a
survey of pests and their natural enemies was begun in 1969 and continued into
1995. During this period 94 species of potential pests of avocado belonging to
45 families of insects, mites, birds and mammals, were recorded (Swirski et
al., 1986, 1991; Wysoki and Izhar, 1978). In the present paper the current
status of arthropod pests in the avocado orchards of Israel is reviewed and
proposals for further progress in their control are presented.
2.
Results
2. 1. Mites(Acarina)
Red spider mites
(Tetranychidae) are rarely found in the avocado orchards of Israel, although
the avocado brown mite, Oligonychus punicae, and the six-spotted mite, Eotetranychus
sexmaculatus, are pests of avocados in California (McMurtry, 1985).
However, in the early 1980s the carmine mite, Tetranychus cinnabarinus, and
the two-spotted mite, Tetranychus urticae, were found in some avocado
plots adjacent to cotton fields, which were treated aerially with synthetic
pyrethroids. A drift of the pesticides to avocado plots caused outbreaks of the
red spider mites. The oriental spider mite, Anychus orientalis, was
found once in large numbers in the Jordan Valley on the leaves of Pinkerton
trees, causing considerable damage.
The broad mite, Polyphagotarsonemus
latus (Tarsonemidae), sometimes attacks avocado seedlings in glasshouses
and greenhouses, causing rolling and browning of the young leaves, severe harm
to the foliage of apical buds, development of shoots by lateral buds, as well
as dwarfing of the seedlings.
2.2. Thrips (Thysanoptera:
Thripidae)
Large
populations of the greenhouse thrips, Heliothrips haemorrhoidalis, usually start
on pest-susceptible trees, such as seedling trees of the Mexican cultivars, or
trees of the cvs. 'Benik' and 'Hass'. From these foci the thrips disperse to
trees of the commercial cvs. 'Fuerte', 'Nabal' and 'Ettinger'. Recently, heavy
damage to cv. 'Ardit' was recorded (Izhar et al., 1990a). The cvs. 'Stuart',
'Nahlat' and 'Horshim' are also susceptible. The rate of damage to Tuerte'
fi-uits is probably correlated with the yield: the greater the yield and
density of fruits, the higher the rate of infestation. Mortality rate of the
thrips is high at relative humidities below 60% and at temperatures above 27ºC
(Rivnay, 1935). Thus it seems that outbreaks of the greenhouse thrips at
certain sites and years are influenced also, or mainly, by climatic factors. It
is found on avocado trees in all seasons of the year and the infestation peak
usually occurs in autumn. During the winters, and mainly relatively warm ones,
its population may reach considerable numbers.
The following local natural
enemies of the greenhouse thrips have been recorded in Israel: predaceous mites
Typhlodromus athiasae and Amblyseius swirskii (Phytoseiidae); the thrips
Franklinothrips megalops; and spiders and predaceous bugs of the family
Anthocoridae. However the local natural enemies are not sufficiently efficient
in curbing the pest populations. Therefore, attempts were made to import exotic
natural enemies. The wasp Thripobius semiluteus (Eulophidae) was
imported to Israel in 1991. It had been introduced into California in 1986 from
Australia and in 1988 from Brazil, and became well established there. It is
recorded also from India and the western coast of Africa. The female inserts
its egg inside the body of first or second stage nymphs. In the laboratory the
development of the parasite is completed at 230C within 22-25 days (McMurtry et
al., 1991), Thripobius was mass-reared at Bet Dagan and released in many
avocado plots, became well established, and most probably can be considered an
effective natural enemy. Spraying with endosulfan - a partially selective
pesticide - is recommended for infested trees only. In our trials the initial
kill of the postembryonic stages of the thrips by pyrethrum was very high, but
the eggs hidden under the plant cuticle were not affected and a population build
up was observed after 15 and 22 days. Oil gave similar results, but was not so
effective as pyrethrum. Two treatments of pyrethrurn at an interval of 21 days
gave good results. However, due to the high price of pyrethrum, farmers are
reluctant to use it (Ben-Yehuda et al., 1994). In trials carried out in avocado
orchards in California in 1985 and 1986, pyrethrum. gave inconsistent results
against the greenhouse thrips (Goodall et al., 1987). In the past, in the USA,
oil was combined with pyrethrum in order to carry the toxicant to the eggs
(Ebeling, 1959).
The black vine
thrips, Retithrips syriacus, has recently caused damage to avocado
fruits and leaves, cvs. 'Horshim', TX-531, 4102, 4203, and T-142 being the most
heavily infected ones. The thrips can be readily controlled with Sabadilla
(Izhar et al., 1992).
2.3. Bugs (Heteroptera)
The variegated caper bug, Stenozygum
coloratum (Pentatomidae), develops generally on wild caper-bush, Capparis
spinosa, sometimes migrating to various cultivated plants, including
avocado (mainly cv. 'Hass', but also 'Fuerte' and 'Ettinger'). The damage to
fruit is accompanied by heavy secretion of persein and by the appearance of
black spots (Izhar et al., 1990b). Although the cottonseed bug, Oxycaraenus
hyalinipennis (Lygaeidae), develops on plants of the family Malvaceae, it
sometimes feeds on leaves and stem of avocado seedlings and may even cause
their Wilt.
2.4. White-flies (Homoptera:
Aleyrodoidea)
The Japanese bayberry whitefly, Parabemi .sia myri.cae, was
discovered in Israel in 1978, causing heavy damage to avocado and citrus trees
(Stemlicht, 1979). Since predaceous mites of the family Phytoseiidae, lacewings
(Neuroptera), ladybeetles (Coccinellidae), predaceous bugs of the family
Anthocoridae and parasitic wasps were unable to suppress the whitefly
effectively, exotic natural enemies were imported. The parasite Eretmocerus
debachi (Aphelinidae) was discovered in 1982 by M. Rose in southern
California. It was released in various citrus orchards, curbed the populations
of the pest successfully and thereby solved the problem (Rose and DeBach,
1992). E. debachi was introduced into Israel by D. Blumberg in June
1982, mass-reared in the laboratory at Bet Dagan, colonized in 61 localities,
and within 2 years of the parasite's
introduction the Japanese bayberry whitefly had been controlled. The following
exotic natural enemies were colonized in numerous avocado and citrus groves and
probably did not become established: the parasitic wasps Eretmocerus sp.,
Encarsia sp., Encarsia ? bemisiae (Aphelinidae) (from Japan); the lady
beetles Nephaspis oculatus and Delphastus pusillus (from Hawaii, sent by
Po Yung Lai); the beetle Cybocephalus binotatus (Cybocephalidae) (bred by
D. Blumberg); and the fungus Aschersonia aleyrodis (investigated in
cooperation with R. Kenneth) (Swirski et al., 1987). In 1992, outbreaks of the
Japanese bayberry whitefly were recorded in some avocado orchards of Western
Galilee. They were caused by drift of baits containing insecticides
(malathion), which were applied aerially against the Mediterranean fruit fly, Ceratitis
capitata (Trypetidae), in adjacent groves of citrus, deciduous fruit trees or subtropical fruit
trees. In a few plots considerable damage was inflicted to fruit and foliage.
However, the high efficiency of E. debachi was manifested also in this
case and within a short period the populations of the pest declined.
2.5. Aphids (Homoptera:
Aphidoidea)
In the spring of 1990 an
outbreak of the melon aphid, Aphis gossypii, and of the spirea aphid, Aphis
spiraecola, on avocado trees was observed. The most heavily infested cvs.
were Nabal' and 'Horshim'. The attack was concentrated on young foliage, but
sometimes involved damage to inflorescences (Swirski et al., 1991).
2.6.
Mealybugs..(Homoptera: Coccoidea: Pseudococcidae)
In the late 1960s and early
1970s, avocado plots in close proximity to cotton fields were heavily damaged
by the long-tailed mealybug, Pseudococcus longispinus. Drift of broad-spectrum
insecticides from aerially sprayed fields killed natural enemies, interfered
with the biological equilibrium and resulted in severe outbreaks of the
mealybug. Moreover, females of the honeydew moth, Cryptoblabes gnidiella,
are attracted to the honeydew of the mealybug and their caterpillars nibble
at the fruit. These spray-induced
outbreaks of the mealybug were successfully curbed by forbidding aerial
applications of broad-spectrum insecticides within 200 m of avocado orchards,
and by the release of the parasitic wasps Anarhopus peregrinus and
Anagyrusfisciventris. The latter was sent to us by Mr. G.O. Furness
(Loxton, S. Australia) in 1971 (Swirski et al., 1980).
2.7. Soft scales (Homoptera:
Coccoidea:Coccidae)
The pyriform
scale, Protopulvinaria pyriformis, was first detected in Tel Aviv in
1980 on a single avocado tree (Ben-Dov and Amitai, 1980), and is now recorded
from the avocado orchards of Western Galilee, the central and southern Coastal
Plain, Shefela and Ramat Menashe. It has not yet been found in the eastern
Yi2re'el, Jordan and Hula valleys. This coccid sometimes causes serious damage
to avocado trees in Florida (Ebeling, 1959) and to citrus and avocado trees in
Spain (Del Rivero, 1966). Variations have been found in the susceptibility of
avocado cvs. to the attack by the pyriform scale. 'Nabal' is the most
susceptible cultivar, followed by 'Ein Vered', 'Reed', 'Hass' and 'Fuerte;
whereas 'Ettinger' trees are sometimes attacked when located close to infested
trees of the susceptible cvs. In laboratory trials, the pyriform scale
completed development and reproduced on 'Nabal' and 'Ein Vered' seedlings, and
to a lesser extent on those of 'Hass'. Survival of the scale was rather poor on
'Fuerte', 'Horshim' and 'Wurz! cvs. and higher on 'Ettinger' 'Pinkerton' and
'Reed' (de Meijer et al., 1989). The pyriform scale produces on avocado two
generations annually - a winter generation with a peak in November-December and
a summer generation with a high level in June-July (Hadar, 1993).
The following
local natural enemies, amongst others, were unable to curb the populations of
the pyriform scale below the economic threshold: Parasitic wasps - Microterys
flavus, Metaphycus flavus (Encyrtidae),
Coccophagus lycimnia (Aphelinidae); predators - Chilocorus
bipustulatus, Oenopia conglobata and Scymnus (ladybeetles, Coccinellidae), Anisochrysa
carnea (green lacewings, Chrysopidae), spiders and the Rmgus Verticillium
lecanii (Hadar, 1993). Thus, efforts were exerted to import various natural
enemies. Metaphycus swirskii (imported from Kenya), initially the most abundant parasite, was soon replaced
by Metaphycus stanleyi (imported from USA, S. Africa and Spain), which
is today the dominant natural enemy of the pyriform scale in Israel. Metaphycus
helvolus (imported from USA) is rare in the avocado orchards and M.
galbus (from S. Africa) probably failed to become established. Two
ladybeetles were imported from Spain: Cryptolaemus niontrouzieri is
sporadically found in the avocado orchards, whereas Nephus peyerimhoffi is
rare. The two secondary parasites Mariettajavensis and Pachyneuron concolor have
an adverse effect on the efficiency of Metaphycus spp. In some avocado
plots 70% of the total parasite fauna may consist of these two secondary
parasites. Population studies of the active parasitization of the scale by M stanleyi
showed an increase in September, with high levels during the winter, a peak
in May and a decline in summer. The high rates of encapsulation of Metaphycus
eggs by the pyriform scale during the summer, may interfere with efficient
biocontrol of the pest (Blumberg and Blumberg, 1991; Hadar, 1993). The site,
duration and rate of
oviposition, as well as host marking-and preference of host stages in the
various species of Metaphycus, were studied by Hadar (1993). Since local
and exotic natural enemies are not sufficiently effective in suppressing the
pyriform scale populations, mineral oil - the selective scalicide - is
recommended. It kills the three nymphal stages of the pest, but does not affect
the ovipositing females. Oil sprays are likely to produce satisfactory results
if applied in December-January (or January-February) and July-August, when the
pest populations consist mainly of young nymphal stages (Hadar, 1993). Only
heavily infested trees are treated with broad-spectrum scalicides.
2.8. Lepidoptera
In Israel the giant looper, Boarmia selenaria (Geometridae),
is the most important pest of avocado in the regions where cotton is grown. It
produces five generations a year, of which the most destructive ones are the
first (spring) and second (early summer) (Wysoki and Izhar, 1986). Its
reproductive behavior was studied by Hadar (1983). Long list of the natural
enemies of the giant looper in Israel was compiled in earlier publications
(Swirski et al., 1988; Wysoki and Izhar, 1980). The spiders are very common in
the avocado groves, and contribute to some extent to biocontrol of the pest
(Mansour et al., 1985). The wasp Apanteles cerialis (Braconidae) oviposits in young
caterpillars of the giant looper. Observations carried out in avocado groves
revealed that the rate of parasitization is highest in October and November and
may reach 70% of the caterpillars (Wysoki and Izhar, 1981). Females of the
tachinid flies (Tachinidae), such as Compsilura concinnata and Exorista nr.
sorbillans, attack advanced stages of the giant looper caterpillars; the
rate of parasitization reaches its peak in late summer or autumn. Since local
egg parasites of the giant looper had not been recorded in Israel, endeavours
were made to import exotic ones. Two wasps, Ooencyrtus ennomophagus (Encyrtidae)
and Telenomus alsophilae (Scelionidae), which parasitize eggs of
loopers, were sent by A.T. Drooz from North Carolina (USA). However, they did
not attack eggs of the giant looper (Wysoki and Izhar, 1980). During 1983 to 1984 several shipments of Trichogramma
platneri (Trichogrammatidae ) were sent to us by E.R. Oatman. This egg
parasite is used in avocado groves of California for controlling the western
avocado leafroller, Amorbia cuneana (Tortricidae), and the omnivorous
looper, Sabulodes aegrotata (Geometridae) (Oatman et al., 1983). In the
laboratory, eggs of the giant looper and of the honeydew moth were attacked by
T platneri (Wysoki et al., 1988). During 1988-1990 approximately 16
million wasps were released in the avocado groves but have not yet been
recovered. In Israel, natural enemies suppress giant looper populations in the
avocado groves effectively, but in regions where cotton is widely grown
pesticide-induced outbreaks of the looper may occur owing to the disrupted
balance with its natural enemies by the drift of pesticides from aerially
sprayed cotton fields in the vicinity. Infestations are controlled, when
necessary, by preparations containing Bacillus thuringiensis (B.t.) var.
kurstaki. Since these preparations are toxic only to young caterpillars,
other varieties of Rt., as well as various strains of B.t. var. kurstaki, were
evaluated for the control of more developed caterpillars as well. Timing of the
control measures is based on traps baited with virgin females (attracting
males) and scouting the groves for young caterpillars. Since mass production of
giant looper virgin females for monitoring purposes is laborious and expensive,
efforts were made to replace the virgin females by synthetic pheromone (in
cooperation with the Technion - Israel Institute of Technology, Haifa, and
Institut für Organische Chemie, Universität Erlangen, Nürnberg, Germany).
(Z,Z)-6,9-cis-3S,4R epoxynonadecadiene and (Z,Z,Z)-3,6,9-nonadecatriene were
identified as sex pheromone components (Becker et al., 1990). Bioassays performed by
electroantennograph (EAG) and in a wind tunnel gave positive results, but in
field tests males were not sufficiently attracted to these two compounds.
Following experiments involving
decapitation of the giant looper and subsequent PBAN injections, a third
compound was revealed (in cooperation with the Department of Stored Products,
ARO and the Insect Neurobiology and Hormone Laboratory, USDA, Beltsville, NM,
USA).
Females of the honeydew moth,
Cryptoblabes gnidiella (Pyralidae), are attracted to the honeydew of
mealybugs and coccids, and the moths caterpillars gnaw at the avocado fruit.
Sometimes the fruit is damaged even when no honeydew-producers are present. The
honeydew moth prefers fruits of cv. 'Hass' to those of other avocado cvs.
Besides avocado, many fruit trees in Israel are known to serve as hosts of the
honeydew moth, including: loquat, persimmon, Annona spp., citrus, etc.
The honeydew moth has the potential to survive throughout the year in an
avocado orchard, feeding on the fruits or on leaves infested with the pyriform
scale, and on Paspalum dilatatum weeds infected by the fungus Claviceps
paspali. Adult moths probably fly between avocado orchards and neighboring
host-crops. The pest can produce five generations a year and overwinters in the
larval stage in fresh or dry avocado fruits (which remain on the trees). The
extent of damage varies from year to year and from site to site
(Ben-Yehuda, 1990). The
reproductive behavior of the honeydew moth was studied by Wysoki et al. (1992).
No studies have been carried out in Israel of the natural enemies of the
honeydew moth. In the laboratory, its eggs were attacked by the exotic wasp T platneri
(see giant looper). R t. var. kurstaki preparations are very
effective against honeydew moth caterpillars of all stages.
The young caterpillars of the
carnation leaf roller, Cacoecimorpha pronubana (Tortricidae), tunnel
through the avocado fruits and the more developed ones gnaw at them
superficially. They can be found also on the young foliage of the trees or on
suckers. The life history of the carnation leaf roller in Israel has not been
investigated. In this country the caterpillars of the pest are parasitized by
the wasp Elachertus lateralis . (Eulophidae) and consumed by spiders and
by larvae of lacewings (Chrysopidae). Preparations of R t. var. kurstaki are
used to control the pest.
Great numbers of
large caterpillars of the Egyptian cotton worm, Spodoptera littoralis (Noctuidae),
from defoliated cotton fields may migrate to adjacent avocado plots and gnaw
holes in the leaves and fruit. In order to prevent such damage, safety belts on
the ground may be treated with insecticides and/or poison baits.
3. Discussion and conclusions
Long-term studies have shown
that in Israel, as elsewhere, many arthropod species may inflict damage to
avocado trees. In the past a "blessed biological equilibrium" was
maintained in the avocado orchards between potential pests and their natural
enemies. However, on this agro-ecosystem the following four pressures, among
others, were applied: cotton, new pests, new avocado cultivars and the human
factor. "Bad neighborly relations" existed between avocado and
aerially sprayed cotton, resulting from the drift of broad-spectrum pesticides
which killed natural enemies and disrupted the biological equilibrium in the
avocado orchards. The avocado trees were victims of newly introduced pests,
e.g. the Japanese bayberry whitefly and the pyriform scale. Pest-susceptible
avocado cultivars, such as 'Ardit', which is heavily attacked by the greenhouse
thrips, have been imported and cultivated on a large commercial scale. The
above mentioned factors pressed upon those involved in the avocado industry to
choose chemical control, as though it would solve all their problems, but they
preferred to remain with the biological and integrated control methods.
It is recommended
to include the following elements in the IPM program of avocado pests in
Israel: (i) importation of additional natural enemies against the pyriform
scale and greenhouse thrips; (ii) conservation and augmentation of local
natural enemies in the avocado orchards by the use of selective pesticides
only, and by observance of the regulations dealing with the limitation of
pesticide drift from adjacent cotton fields; (iii) further studies to identify
the giant looper sex pheromone for use in developing a monitoring system; (iv)
continuation of surveys of pests and their natural enemies in the avocado
groves, in order to prevent the possible sudden and unexpected appearance of a
new pest and/or outbreaks of a local one owing to changes in agrotechnical
practices; and (v) thorough studies of the biology and dynamics of population
of pests and their natural enemies.
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Wysoki, M., 1991. Appearance of Aphis gossypii Glover and Aphis
spiraecola Patch (Rhynchota: Aphidoidea) on avocado, persimmon and
macadarnia. Alon haNotea 45:413-416 (Hebrew, with English summary).
Swirski, E., Izhar, Y.,
Wysoki, M., Gurevitz, E., and Greenberg, S., 1980. Integrated control of the
long-tailed mealybug, Pseudococcus longispinus [Hom.: Pseudococcidae],
in avocado plantations in Israel. Entomophaga 25:415-426.
Swirski, E., Wysoki, M., and
Izhar, Y., 1986. Biological and integrated control of subtropical fruit pests
in Israel. Alon haNotea 40:664-674 (Hebrew, with English summary).
Swirski, E., Wysoki, M., and
Izhar, Y., 1988. Integrated Pest Management in the avocado orchards of Israel.
Appl. Agric. Res. 3:1-7.
Swirski., E., Wysoki, M., and
Izhar, Y., 1991. [Twelve years survey of avocado pests and their natural
enemies (1978-1990).] Alon haNotea 46:65-103 (in Hebrew).
Wysoki, M., Ben-Yehuda, S.,
and Rosen, D., 1992. Reproductive behavior of the honeydew moth, Cryptoblabes
gnidiella (Lep., Pyralidae).] Alon haNotea 47:2-10 (in Hebrew).
Wysoki, M., de Jong, M., and
Rene, S., 1988. Trichogramma platneri Nagarkatti (Hymenoptera:
Trichogrammatidae), its biology and ability to search for eggs of two
lepidopterous avocado pests, Boarmia (Ascotis) selenaria Schiff. (Geometridae)
and Cryptoblabes gnidiella (Milli6re) (Phycitidae) in Israel. Trichogramma
and Other Egg Parasites; IInd Int. Symp. (Guanghzou, China, Nov. 10- 15,
1986). Ed. INRA, Paris (Les Colloques de l'INRAS, no. 43).
Wysoki, M., and Izhar, Y.,
1978. A list of arthropod pests of avocado and pecan trees in Israel.
Phytoparasitica 6:89-93.
Wysoki, M., and Izhar, Y.,
1980. The natural enemies of Boarmia (Ascotis) selenaria Schiff. (Lepidoptera:
Geometridae) in Israel. Acta Oecol., Oecol. Appl. 1:283- 290.
Wysoki, M., and Izhar, Y.,
1981. Biological data on Apanteles cerialis Nixon (Hymenoptera:
Braconidae), a parasite of Boarmia (Ascotis) selenaria Schiff. (Lepidoptera:
Geometridae). Phytoparasitica 9:19-25.
Wysoki, M., and Izhar, Y.,
1986. Fluctuation of the male population of Boarmia (Ascotis) selenaria (Lepidoptera:
Geometridae) estimated by virgin female baited traps. Acta Oecol., Oecol. Appl.
7:251-259.