BIOLOGICAL CONTROL OF ARTHROPODS IN GRAPES
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Vitis vinifera L., the most widely cultivated species of grape, had been grown in Asia Minor between the Caspian and Black seas since the beginning of civilization (Winckler et al. 1974), flourishing especially in central Europe through the 14th Century. The invasion of grape phylloxera, Daktulosphaira vitifoliae (Fitch) from North America ca. 1886 markedly reduced the productive acreage in France, a plague that gradually spread to the Black Sea area within 10 years. Viticulturists were formed to develop resistant rootstocks and hybrid grapes that greatly sophisticated the industry (Gonzalez 1983).
In the some 10 million hectares of grapes worldwide, hundreds of clonal selections and hybrids have been produced to adapt varieties to various climatic and soil conditions found on all continents (Gonzalez 1983). Such diverse viticulture modifies vine microclimates to favor or inhibit pests that are indigenous to the ecosystem of the grape plant. These various ecological niches created by the biocenosis of the vine are occupied in each grape region by different pests (Bournier 1976). As pest resistance to synthetic organic pesticides developed, there has been an interest in biological control (Flaherty et al. 1985, Flaherty & Wilson 1999).
In a review of arthropod pests attacking grapes, Flaherty & Wilson (1999) consider major taxonomic groups as follows:
Cicadellidae.--There are nine species of leafhoppers that attack grapes (Bournier 1976). Erythroneura elegantula Osborn, the grape leafhopper, is the most common. Damage is caused by leaf chlorophyll reduction, vine defoliation, and damage of the surface of table grapes with excrement, and annoyance from leafhoppers to workmen (Jensen & Flaherty 1981a).
It was observed that grapes planted near streams and rivers, where wild blackberries, Rubus ursinus Chamisso & Schlecht and Rubus procerus Mueller, grow, do not sustain high grape leafhopper densities (Doutt & Nakata 1965, 1973). Principal reasons were the activity of Anagrus epos Girault parasitizing the eggs of both grape and blackberry leafhopper (Dikrella californica (Lawson)), a non economic species whose eggs are present year round on wild blackberries. This synchrony of blackberry leafhopper, grape leafhopper and A. epos phenology was reported by Williams (1984).
There was then considerable effort to establish effective blackberry refuges near commercial vineyards. However, successful control was not attained because overwintering numbers of A. epos were so few due to low D. californica egg production in winter (Flaherty et al. 1985). Effective overwintering of the parasitoid depended on continuous production of eggs by D. californica. Williams (1984) found a reproductive diapause in females of this species during winter. The importance of alternate host plants sustaining leafhoppers was reported by McKenzie & Beirne (1972), Kido et al. (1984) and Flaherty et al.(1985). Such host plants as apple, wild rose and French prune are important host plants for such leafhoppers. In the San Joaquin Valley of California, there is not an emphasis on the prune leafhopper, Edwardsiana prunicola (Edwards), as a major overwintering host of the parasitoid (Flaherty et al. 1985). Another species, Typhlocyba pomaria McAtee, on apple is also probably important.
Jensen & Flaherty (1981a) discuss how the parasitoid, A. epos importance varies with grape variety and its intended usage. High populations of grape leafhopper can be tolerated on Thompson Seedless grapes which are to be used for raisin or wine production, but only very low tolerance is on grapes grown for fresh market consumption. Spotting damage, which results from leafhopper feces, affects the value of the crop. On the table grape varieties Emperor and Ribier, the grape leafhopper populations increase to such high numbers even in the presence of the parasitoid, that control is unsatisfactory. Reasons for the parasitoid's greater effectiveness on Thompson Seedless are unknown, but some observations indicate that the smooth leaf surface of Thompson Seedless vines does not impede searching and oviposition of the parasitoid. Early maturing varieties also produce fewer newly mature leaves, sites which are favored by grape leafhopper for egg deposition. By comparison the later varieties such as Emperor and Ribier have tomentose (hairy) leaves that may interfere with the parasitoid. Leafhopper oviposition is also favored by the development of newly matured leaves late in the season. Later season irrigation in such vineyards also favors grape leafhopper (Jensen & Flaherty 1981a).
The parasitoid, Aphelopus albopictus Ashmead (= A. comesi Fenton) attacks all instars of the grape leafhopper (Cate 1975). Parasitoid eggs are placed between the nymph's 2nd and 3rd abdominal segments where they remain undeveloped until the nymph molts to the adult stage. The host appears normal during the parasitoid's larval development except for an elongating larval sack (the thylacium) that gradually protrudes from the abdomen with each parasitoid mold. By its 5th instar the parasitoid has developed mandibles and eviscerates the adult leafhopper. Prior to evisceration the adult leafhopper is functionally non-reproductive since gonads fail to develop in parasitized adults. Parasitism is usually between 10-40%, but Cate (1975) reported a high of 77%, and speculated that cultural practices might be altered to favor parasitism.
The variegated grape leafhopper, Erythroneura variabilis Beamer, is the principal vineyard pest in the lower Sonoran Desert of California, Arizona and Mexico. Infestations are severe in the Coachella Valley of California where the high temperatures allow for rapid development and as many as six generations per year (Barnes 1981). Activity of the parasitoid A. epos is low in this climate, becoming prominent only in the milder climates of the coastal plain where parasitism can reach 90% (Barnes 1981).
Variegated grape leafhopper invaded the San Joaquin Valley around 1980 and continues to spread. Defoliation occurs in Thompson Seedless vineyards especially where the grape leafhopper had been under good control by A. epos. The whole management strategy, built around the activity of this parasitoid, was altered with a renewed attention to chemical control. This caused outbreaks of secondary pests such as spider mites and mealybugs. The projected annual costs for control of variegated grape leafhopper were expected to be >$5-10 million, with yield and quality losses probably double that amount (Wilson et al. 1986, 1987).
Settle et al. (1986) commented "Variegated leafhopper is a more serious pest than the grape leafhopper, in part because of differences in egg-laying behavior. Variegated leafhopper eggs, deeply buried within the leaf tissue, are less likely to be detected by A. epos than grape leafhopper eggs, which stand out as blisters on the leaf surface."
A search for new parasitoids of variegated grape leafhopper was begun in 1985 in southern California, Arizona, Colorado, Texas, New Mexico and Mexico. The variety of species and biotypes of leafhopper parasitoids collected from diverse climatic zones and in different seasons were found (Gonzalez et al. 1988). It was found that A. epos had evolved a wide range of biotypes, differing in relative preference for the grape leafhopper and variegated grape leafhopper. Pickett et al. (1987) indicated that the San Joaquin Valley biotype had a 6.9X greater preference for grape leafhopper than for variegated grape leafhopper. On the basis of preference, biotypes from the Coachella Valley and Colorado would respectively choose, provided equal numbers of eggs of both hosts, 2-4.3 times more variegated grape leafhopper eggs.
Erythroneura ziczac Walch is the most important insect on grapes in the Okanagan Valley, British Columbia (McKenzie & Beirne 1972). Two cultural procedures which prevented damage by leafhoppers were (1) destroying overwinter sites around the vineyards and (2) providing A. epos
Generalist predators, primarily spiders such as Theridion sp., may significantly impact leafhoppers in vineyards with cover crops (Settle et al. 1986). In San Joaquin Valley studies, twice as many spiders were recorded in a vineyard with a weed cover crop. Settle et al. (1986) also found that Thompson seedless grapes grown on its own roots showed greatly reduced attractiveness to leafhoppers, resulting in a nearly 8X reduction in leafhopper numbers compared with the more vigorous vines on Saltcreek rootstock. Reduced leafhopper pressures afforded by cultural practices suggest a potential for biological control.
Pierce’s Disease spread by sharpshooter leafhopper [Please refer to ch-120.htm]
Pseudococcidae.--Two mealybug species causing problems in California vineyards are the grape mealybug, Pseudococcus maritimus (Ehrhorn) and the obscure mealybug, Pseudococcus affinis (Mackell) (= P. obscurus Essig). The first species is principally a pest of table grape varieties whose bunches make contact with vine bark and become infested (Flaherty et al. 1981b). Before the late 1940's occasional losses occurred in table grapes, which were mostly spotty and generally nonproblematic. The problem gradually increased in the late 1940's with extensive use of DDT and other pesticides to control grape pests. The obscure mealybug, which has been recorded on a large number of hosts, was recently found to be a problem in unsprayed vineyards in San Luis Obispo County, a more coastal climate. The absence of effective parasitoids attacking obscure mealybug points to it as a recently introduced species that will require the importation of new natural enemies.
Clausen (1924) reported five primary endoparasitoids from grape mealybug in the central San Joaquin Valley, where late summer and autumn parasitism was >90% in 1919. Flaherty & Wilson (1999) reexamining Clausen's (1924) data concluded that Zarhopalus corvinus (Girault) was the most active. In the 1960's a ranking of host parasitism from samples of Doutt & Natata (unpublished) showed that Acerophagus notativentris (Girault) was the principal species, that Acerophagus subalbicornis (Girault) was occasionally found and that Z. corvinus was uncommon (Flaherty et al. 1976). Parasitoids were not reared from mealybug samples collected from an Emperor variety vineyard where heavy treatments. of pesticides were made.
Another mealybug, Maconellicoccus hirsutus (Green), is a pest of grape in India (Manjunath 1985). It attacks the varieties Thompson Seedless, Anab-e-Shahi and Bangalore Blue. Up to 90% of the clusters are destroyed, and chemical control is not effective. The encyrtid, Anagyrus dactylopii Howard, seems to offer some biological control potential. In late season samples at Bangalore, parasitization ranges from 60-70%, although fields are regularly treated with insecticides. Manjunath (1985) recommended the introduction of Anagyrus kamali Moursi and Prochiloneurus sp. which reportedly give complete control of M. hirsutus in Egypt (Kamal 1951).
Planococcus citri (Risso) damages >20 species of plants in the Soviet Union (Niyazov 1969). The parasitoid Anagyrus pseudococci (Girault) is active in the region, destroying up to 75% of the host populations in untreated areas. Allotropa mecrida (Walker) was responsible for 20% parasitism of P. citri in Turkemenia and Georgia. The encyrtids Leptomastidea abnormis (Girault) and Leptomastix dactylopii Howard were introduced into Georgia and Turkemia from the United States in 1960, but native hyperparasitoids reduced their effectiveness. In Transcaucasia and Soviet Central Asia, Thysanus (Chartocerus) subaeneus Forster was responsible for up to 20% hyperparasitism of A. mecrida. Rzaeva (1985) reported that L. abnormis successfully established on Planococcus ficus Signoret, a mealybug pest of grapes in eastern Transcaucasus. The introduction of Clausenia josefi Rosen also was recommended (Niyazov 1969), as well as A. notativentris from California.
The effectiveness of predators in California vineyards is generally unknown. Mealybug egg masses have been attacked by cecidomyiid fly larvae (Flaherty et al. 1982). Adults of Chrysoperla spp. (= Chrysopa spp.) are often abundant on grapevines with mealybugs, adults being attracted to mealybug honeydew. Cryptolaemus montrouzieri Mulsant (the mealybug destroyer) is rare in California vineyards. The use of this predator for mealybug control in the Soviet Union was reviewed by Yanosh & Mjavanadze (1983). Cryptolaemus was particularly effective on Chloropulvinaria floccifera Westwood on tea, with adult beetles being field released. Niyazov (1969) reported that one of the most effective predators of mealybugs on grape in the Soviet Union was C. montrouzieri which had been introduced from Egypt in 1932. Other coccinellids of importance in Turkemenia were Coccinella spetempunctata L., Scymnus apetzi Mulzant, Hyperaspis polita Weise, Scymnus subvileosus (Goeze), Nephus bipunctatus Kugelann and Scymnus biguttatus Mulsant. Larvae of Leucopis (Leucopomya) alticeps Czerny and Chrysoperla carnea (Stephens) were active on all mealybug stages. The coccinellids were parasitized by Homalotylus sp. and the chrysopids by Telenomus acrobates Girard.
Coccidae.--Gonzalez (1983) reported that grape quality can be affected by copious amounts of honeydew produced by Parthenolecanium persicae (F.) in Chile, but natural enemies are important in minimizing damage. The principal parasitoids were Coccophagus caridei (Brethes) and Metaphycus flavus (Howard). These and other parasitoids were common natural enemies of lecanium coccids on other plants including P. corni (Bouché) which is also a pest of grapes in Chile.
Phylloxeridae.--The coccinellid Scymnus cervicalis Mulsant is the only natural enemy considered important as a predator of the leaf-feeding form of grape phylloxers, D. vitifoliae, on wild grapes in Erie County, Pennsylvania (Wheeler & Jubb 1979).
Tetranychidae.--Spider mites became serious grape pests after World War II, at the same time that synthetic organic insecticides appeared (Flaherty et al. 1985). Two spider mite species which are commonly found on California grapes are the Pacific spider mite, Tetranychus pacificus McGregor, and the Willamette spider mite, Eotetranychus willamettei (Ewing) (Flaherty et al. 1981a). Two-spotted spider mite, T. uriticae Koch. is rare on grapes in California.
In the eastern United States, European red mite, Panonychus ulmi (Koch), is the principal spider mite problem (Jubb et al. 1985). This species is also a pest in Europe. Schruft (1986) listed E. carpini vitis Boisduval, T. urticae, T. mcdanieli McGregor and T. turkestani Ugarov & Nikolski also as pests in Europe. Oligonychus vitis Zaher & Shehata was reported serious on grapes in Egypt and Chile (Rizk et al. 1978, Gonzalez 1983). In the Soviet Union spider mite pests are P. ulmi, Eotetranychus pruni (Oudemans), T. turkestani and Bryobia praetiosa Koch . Schruft (1986) reported that E. pruni is important as a pest in Bulgaria. In India there are four species, Oligonychus. mangiferus (Rahman & Sapra), O. punicae (Hirst), T. urticae, and E. truncatus Estebanes & Baker (Schruft 1986). In Japan grapes are hosts for B. praetiosa, E. smithi Pritchard & Baker, T. kanzawai Kishida and T. urticae (Schruft 1986).
In San Joaquin Valley, California vineyards, the most important natural enemy of spider mites us the predatory mite Metaseiulus occidentalis (Nesbitt) (Flaherty et al. 1981a). Amblyseius californicus (McGregor) is important in the Salinas Valley and M. mcgregori (Chant) in the Sacramento Valley. Although these predators prey on the Willamette spider mite, their effectiveness is unknown. In the eastern United States the most common predatory mites on Concord grapes (Vitis labrusca L.) are the phytoseiids, Neoseiulus (Amblyseius) fallacis (Garman) and Amblyseius andersoni (Chant), and the stigmaeid Zetzellia mali (Ewing). Neoseiulus fallacis and Z. mali may be important in natural control of P. ulmi (Jubb et al. 1985). In Europe the cost common phytoseiids are Typhlodromus pyri Scheuten, Euseius (Amblyseius) finalndicus (Oudemans), Amblyseius aberrans (Oudemans) and A. andersoni, but only T. pyri is of importance in biological control (Schruft 1986). However, A. aberrans is very important in Italy (Gambaro 1972). Rizk et al. (1978) reported that Agistemus exsertus Gonzalez, Amblyseius gossipi El-Badry and Tydeus californicus (Banks) are very abundant in middle Egypt, while in Chile Amblyseius chilenensis (Dosse) is very important (Gonzalez 1983).
Spider mite control can be somewhat predicted by the ratio of the number of predators to spider mites. For any system there exists a particular predator/prey ratio at which the pest population will be controlled. For example, Tanigoshi et al. (1983) reported that a 1:10 ratio of Neoseiulus fallacis to P. ulmi provided control in Red Delicious apples. In another orchard with a different apple variety, Tanigoshi et al. (1983) found a 1:20 ratio was sufficient, and indicated that relatively fewer predaceous mites were required to provide control as a result of reduced spider mite fecundity on this variety. Wilson et al. (1984) found that a 1:11 ratio of Metaseiulus occidentalis to Tetranychus spp. provided control in almonds within two weeks when the spider mites were at densities of >5 mites per leaf. At lower densities an increasingly higher predator/prey ratio was required.
It is very tedious to estimate spider mite abundance and predator effectiveness, because mites are extremely small, and often numerous. Schruft (1986) found that it is possible to estimate the risk of damage by P. ulmi or E. carpini vitis using a method developed by Baillod et al. (1979). The method tests the relationship between the number of spider mites per leaf and the proportion of leaves in a sample occupied by mites. Therefore, instead of counting the mites themselves, the number of leaves with one or more mites is recorded. The same sampling procedure has been used to evaluate predaceous mites (Baillod & Venturi 1980). Flaherty et al. (1981a) used an infested leaf (binomial) predator/prey ratio, together with information on the relative level of spider mites in the vineyard. Based on observations over several years, they found that a 1:2 (0.5) binomial ratio of predator to spider mite infested leaves was sufficient for control. This ratio was less conservative than the ratios derived using the Wilson et al. (1984) procedure for almonds. A binomial ratio of ca. 1:1 is equivalent to a 1:10 count ratio at densities between 15-50 spider mites per leaf. A binomial ratio closer to that reported by Flaherty et al. (1981a) was calculated when using a 1:20 count ratio . The lower ratio for grapes may indicate a lowered reproductive capacity for spider mites on grapes compared to that found on almonds, or perhaps for that found by Tanigoshi et al. (1983) on apples.
Alternate foods of predaceous mites have been considered in predator/prey relations. Flaherty (1969) reported that M. occidentalis was better able to regulate low densities of Willamette mites in the presence of small number of T. urticae that moved from weeds onto grape leaves. Flaherty et al. (1981a) recommended that Willamette spider mite be considered as an important alternate prey because it is a much less serious pest of grapes than Pacific spider mite. Metaseiulus occidentalis also preys on other mites, such as tydeids, eriophyids and perhaps tarsonemids. In Europe additional food for T. pyri includes eriophyids, tydeids, pollen and pearls of the grape (Schruft 1972). The possible benefits of augmenting pollen feeding tydeids by pollen applications or planting cover crops that produce wind borne pollen exists (Flaherty & Hoy 1971, Calvert & Huffaker 1974). Gambaro (1972) reported that Amblyseius aberrans was able to live and reproduce in the absence of prey and thus could maintain spider mite populations at low densities.
Viticultural practices influence spider mite outbreaks (Flaherty et al. 1981a). Emphasis is placed on avoiding problems associated with low vine vigor, dusty conditions and water stress, which can greatly increase the chance of Pacific spider mite outbreaks. Although 10 species of phytoseiid mites are known in commercial vineyards of the San Joaquin Valley, only M. occidentalis seems to pay a significant role in natural control of spider mites (Flaherty & Huffaker 1970). The predaceous mite Amblyseius nr. hibisci becomes abundant where triadimefon replaced sulfur for control of powdery mildew, Uncinula necator Burrill. The predaceous mite is common in wild grapes where sulfur is not applied (Flaherty et al. 1985). English-Loeb et al. (1986) showed that A. nr. hibisci was not only the dominant phytoseiid species where sulfur was not applied but it also maintained lower numbers of Willamette spider mites than M. occidentalis where sulfur was used. The phytoseiid Typhloseiopsis smithi (Schuster) was also recorded on non sulfur treated grape foliage (English-Loeb et al. 1986).
Arthropod predators, such as predaceous insects and spiders, are considered as ineffective natural enemies of spider mites (Flaherty et al. 1981a), because they appear too late in the season or increase in numbers too slowly. However, their contribution to natural control in vineyards might be significant. Sometimes six-spotted thrips, Scolothrips sexmaculatus (Pergande) destroys Pacific spider mite populations. This predator is unpredictable, however, which may be related to periodic low prey densities. In Italy anthocorids and coccinellids are considered effective at high prey densities (Duso & Girolami 1985). Schruft (1986) reported that predaceous insects, Scymnus sp., Oligota sp., Scolothrips longicornis Priesner, Anthocoris nemorum (L.) and Orius minutus (L.) are found on grapes infested with P. ulmi, but their importance for biological control of red spider mite populations is unknown. However, it is certain that some chrysopids, particularly Chrysoperla carnea, are effective predators of red spider mites during summer and late autumn (Schruft 1986).
Spider mite control by insect predators may be subtle as well as important, because observations in vineyards and laboratory studies revealed that western flower thrips, Frankliniella occidentalis (Pergande) which is a pest of grapes, feeds on Pacific spider mite eggs and may actually affect the pest's population in vineyards (Flaherty et al. 1981a). Franklineilla occidentalis predation is apparently also important in cotton on spider mites (Gonzalez et al. 1982, Gonzalez & Wilson 1982, Trichilo 1986).
Mass releases of M. occidentalis for control of Pacific spider mites are not practical (Flaherty et al. 1985), but an autumn release program may be more useful. Flaherty & Huffaker (1970) showed that late season predator activity in vineyards is essential to spider mite balance. A fall release of M. occidentalis resulted in excellent biological control of Willamette spider mite the following spring and summer. Hoy & Flaherty (1970, 1975) considered late season diapause induction important for the successful overwintering of M. occodentalis populations. Flaherty et al. (1985) thought that a fall release of predators reared under diapausing conditions would minimize the timing and survivorship problems associated with early summer releases because immediate control of Pacific spider mite in the fall is not a factor and diapausing predators require little food. In Italy, Girolami & Duso (1985) reported on the establishment of predator/prey equilibrium in pesticide-disturbed vineyards with reintroductions of A. aberrans. Baillod et al. (1982) described methods for reintroduction of T. pyri into vineyards in Switzerland and recommended their use for biological control of phytophagous mites. Schruft (1986) reported the artificial release of T. pyri by the introduction of infested canes or foliage.
Tenuipalpidae.--Brevipalpus chilensis Baker is serious on grapes in Chile, which developed as a consequence of indiscriminate use of pesticides (Gonzalez 1983). Important to consider preserving is the predaceous mite A. chilenensis. In Victoria, Australia, B. lewisi McGregor causes a superficial scaring of bunch and berry stems (Buchanan et al. 1980). A close relationship between B. lewisi and its most common phytoseiid predator Amblyseius reticulatus (Oudemans) did not reveal regulation of B. lewisi numbers by A. reticulatus during the growing season. However, large numbers of A. reticulatus during the end of the growing season may reduce the number of B. lewisi that can overwinter. The false spider mite Tenuipalpus granati Sayed has been considered a serious pest of grapes in Egypt (Rizk et al. 1978), which was blamed mostly on pesticide upsets. The predators Agistemum exsertus, Amblyseius gossipi and Tydeus californicus were observed to be associated with T. granati.
Eriophyidae.--The eriophyid mite Colomerus vitis (Pagenstecher) attacks various species and hybrids of grapes. Different biotypes of the eriophyid have been found in California, separated by injury type (Kido 1981). The phytoseiid mite M. occidentalis was reported effective in reducing populations of C. vitis. Schruft (1972) reported that C. vitis and Calepitrimerus vitis (Nalepa) also eriophyid pests in Europe, were destroyed by the tydeids Tydeus götzi Schruft and Pronematus stärki Schruft.
Tortricidae.--Grape clusters are often attacked by tortricids worldwide. The orange tortrix, Argyrotaenia citrana (Fernald), is a major pest in cooler coastal regions of California. Larvae cause damage by feeding in grape clusters and permitting rots to invade (Kido et al. 1981c). Kido et al. (1981b) assessing biological control sampled Gamay Beaujolais vines in Salinas Valley vineyards. One vineyard (Soledad) had a history of injurious infestations that required treatments. The other (Greenfield) had very light infestations and no treatments were required. Samples of clusters from the Greenfield vineyard contained few orange tortrix larvae and pupae, with 53.5% parasitism, while the Soledad vineyard with a high orange tortrix density had 16% parasitism. Exochus nigripalpus subobscurus Townes was the predominant parasitoid in both vineyards. Apanteles aristoteliae Viereck was less frequent.
The coyote brush, Baccharis pilularis DeCandolle also sustained orange tortrix infestations. Large numbers of another tortricid species Aristoteliae argentifera Busck were found on coyote brush located near the Greenfield vineyard and several parasitoids were recovered from larvae and pupae (Exochus sp. and Apanteles sp.). Coyote brush was much less abundant near the Soledad vineyard and consisted mainly of young plants and no infestation of A. argentifera.
The omnivorous leafroller, Platynota stultana Walsingham, has become a major pest in the warmer inland valleys of California since 1960 (Kido et al. 1981a). It causes a rot similar to that of the orange tortrix. A number of insect parasitoids have been recorded on omnivorous leafroller in vineyards, but parasitoids seldom accounted for >10% mortality even on very high worm infestations. Flaherty et al. (1985) recommended the importation and augmentation of natural enemies of this insect in the San Joaquin Valley.
Trichogramma spp. have been mass released to augment biological control of omnivorous leafroller and orange tortrix. Makhmudov et al. (1977) reported that Trichogramma sp. releases gave good control of Lobesia botrana (Schiff), a tortricid attacking grapes in the Soviet Union. Marcelin (1985) reported significant reductions of L. botrana and Eupoecilia ambiguella (Hübner) populations with Trichogramma sp. releases. The selective control of tortricids in grapes with Bacillus thuringiensis Berliner and mating disruption has been stressed in Europe.
Damage by Proeulia auraria (Clarke) was reported from Chile by Gonzalez (1983) when natural enemies were destroyed by pesticides. A complex of five species of egg and larval parasitoids are associated with this pest. The encyrtid, Encarsia sp. attacked eggs. Larval parasitoids included eulophids Elachertus and Bryopezus, a braconid Apanteles, and unidentified ichneumonid, and a tachinid, Ollacheryphe aenea (Aldrich).
The western grapeleaf skeletonizer, Harrisina brillians Barnes & McDunnough, was originally distributed throughout the southwestern United States and northern Mexico. It was first found in California in San Diego in 1941, where it severely defoliated wild grapes, Vitis girdiana Munson in the canyons. Soon it became a serious pests in commercial vineyards. The larvae are voracious feeders and can devastate a crop by defoliating an entire vineyard.
In 1950 efforts were initiated in the University of California to control grapeleaf skeletonizer biologically. Parasitoids were introduced, with two species, the braconid, Apanteles harrisinae Muesebeck and the tachinid, Ametadoria miscella (Wulp) (= Sturmia harrisinae Coquillett) predominating (Clausen 1961). A virulent granulosis virus was also accidentally introduced.
Surveys in San Diego County in 1982-1983 revealed that it was necessary to spray grapeleaf skeletonizer in commercial vineyards (Flaherty et al. 1985). Abandoned untreated vineyards and backyard vines were severely defoliated despite the activity of the imported parasitoids. Symptoms of virus infection were not observed in the survey. Grapeleaf skeletonizer was not found in wild grapes, V. girdiana, except where they were in close proximity to heavily infested commercial V. vinifera vineyards.
The skeletonizer invaded the San Joaquin Valley in 1961 (Clausen 1961), and new infestations appeared thereafter throughout the Central Valley in spite of eradication efforts. Renewed efforts to introduce natural enemies were made in the 1980's, which resulted in the translocation of parasitoids from southern California and the acquisition of new species and strains from Torreón vicinity in Mexico (E. F. Legner and B. Villegas, unpub. data). Extensive insecticide treatment during introduction, however, precluded establishment in most areas. Some success was achieved outside the principal grape production area near Redding, with the establishment of Apanteles spp. and Ametadoria spp. This insect is now regarded a serious pest of commercial vineyards and backyard vines, as well as in wild grapes, Vitis californica Bentham. Apanteles harrisinae and A. miscella were not successfully established in the San Joaquin Valley (Flaherty et al. 1985). Only a few parasitoid recoveries were made at release sites which may be related to heavy spray pressure during the introduction period (E. F. Legner, unpub. data). Samples of larvae taken from heavily infested and abandoned vineyards in San Diego County showed only 13% parasitism, which is below the 42-62% reported by Clausen in 1953-54 (Clausen 1961). There was also no evidence of virus present. Clausen (1961) thought that the virus must be credited with the major role in reducing grapeleaf skeletonizer populations to low levels and exterminating many small infestations. Flaherty et al. (1985) considered that at that time the virus was more widespread and had reduced grapeleaf skeletonizer populations to levels that made it more manageable by the parasitoids. This may account for the greater parasitism reported by Clausen (1961) and that found by Flaherty et al. (1985). However, the present absence of virus in abandoned vineyards in San Diego County and the absence of observable grapeleaf skeletonizer in wild grapes is considered an enigma. The grapeleaf skeletonizer has been known to show cyclic abundance, however, and the surveys conducted in San Diego County could have been during one of the cyclic outbreaks. Surveys by Legner (unpub. data) during other years have shown this insect to be as rare as reported by Clausen earlier. Also, widespread application of insecticides to vineyards in the south could be responsible for minimizing natural enemy activity. In the San Joaquin Valley the virus of grapeleaf skeletonizer is extremely virulent and has the potential of becoming incorporated into an areawide biological control effort, including wild grapes, backyard vines and commercial vineyards (Flaherty et al. 1985).
Pyralidae.--The grape leaffolder, Desmia funeralis (Hübner), is a pest of grapes in the central and southern San Joaquin Valley. The larvae rolling and feeding on the leaves cause injury. Some feeding on fruit occurs at high densities, but economic damage usually occurs only with massive, late season infestations (Jensen & Flaherty 1981b). The larval parasitoid Bracon cushmani (Muesebeck) commonly attacks grape leaffolder. Parasitism ranges from 30-40% and higher. Bracon cushmani usually increases in summer and frequently reduces the size of the second and third brood to such small numbers that little increase in host populations is detectable (Jensen & Flaherty 1981b).
Sesiidae.--The grape root borer, Vitacea polistiformis (Harris) is a pest of grapes east of the Rocky Mountains. Larvae prune and girdle grape roots by excavating irregular burrows (Jubb 1982). Saunders & All (1985) showed an inverse correlation between the severity of V. polistiformis and the activity of entomophilic rhabditoid nematodes in vineyard soils. Laboratory and field bioassays determined the susceptibility of 1st instar larvae to the nematode Steinernema feltiae Filipjev, and the insect nematode interaction was considered a type of natural control on larvae. Augmentation of entomophilic rhabditoid nematodes during the critical period of oviposition and eclosion was suggested as a technique for control.
Curculionidae.--Adults of Naupactus xanthographus (Germar) consume grape buds and leaves in Chile (Gonzalez 1983). Damage also occurs when feces adheres to foliage and fruit clusters. Combined damage by adult and larval feeding on root-weakened vines. A complex of pathogens (bacteria, fungi), nematodes and insects attack larvae and pupae in the soil. A nematode of the family Rhabditidae parasitizes 4th-5th instars. The same nematode attacks other Coleoptera and can be reared on wax moth larvae, Galleria melonella (L.). Gonzalez (1983) reported that larvae are often attacked by nematodes that are transported in irrigation water, but the degree of control was not evaluated. Of importance as a natural enemy is Platystasius sp (Fidiobia sp.). Up to 60% of the egg masses under the bark can be attacked. Gonzalez (1983) reported that its action in conjunction with the complex of other natural enemies is sufficient to keep N. xanthographus below the economic threshold.
Otiorhynchus sulcatus (F.), the black vine weevil, is important in horticultural crops in Europe, the United States, Canada, Australia and New Zealand. Adults seriously damage berry pedicels and cluster stems and larvae feed on roots in Europe and central Washington (Bedding & Miller 1981). The application of aqueous suspensions of infective juvenile Heterorhabditis heliothidis (Khan, Brooks & Hirschmann) to the soil resulted in up to 100% parasitism of larvae of O. sulcatus in potted grapes in nurseries. Pupae and newly emerged adults were also parasitized. Steinernema bibionis (Bovien) was found less effective.
Bostrichidae.--Medalgus confertus (LeConte), a branch and twig borer, is found in California associated with many species of cultivated and native trees and shrubs. In grapes both adult and larval stages cause injury to grapevines (Joos 1981). Little is known about the natural enemies of M. confertus, but a neuropteran predator in the Rhaphidiidae, and two coleopterans in the families Carabidae and Ostomidae may be very active. Recent studies have shown that the entomophagous nematode, S. feltiae, can move through frass tubes to infect larvae.
Thripidae.--Several species of thrips, such as Frankliniella spp. and Drepanothrips reuteri Uzel, can be pestiferous on grapes worldwide (Flaherty & Wilson 1988). Jensen et al. (1981) report that little is known about their natural control in California, however. Some studies in California citrus show that phytoseiid mites Euseius tularensis Cugdon can control the citrus thrips Scirtothrips citri (Moulton). Schwartz (1987) reported that Amblyseius citri van der Merwe & Ryke preyed on Scirtothrips aurantii Faure in South Africa. Schwartz (1987) also found that Amblyseius addoensis van der Merwe & Ryke most likely preyed on Thrips tabaci Lindemann in South African table grapes, although it was not sufficiently effective during mid summer.
Baillod, M., J. P. Bassino & P. Piganeau. 1979. L'estimation du risque provoqué par l'acarien rouge (Panonychus ulmi Koch) et l'acarien des charmilles (Eotetranychus carpini Oud.) en viticulture. Revue Suisse Vitic. Arboric. Hortic. 11: 123-30.
Baillod, M., A. Schmid, E. Guignard, P. Antonin & R. Caccia. 1982. Lutte biologique contre l'acarien rouge en viticulture. II. Equilibres naturels, dynamique des populations et expériences de lachers de typhlodromes. Revue Suisse Vitic. Arboric. Hortic. 14: 345-52.
Baillod, M. & I. Venturi. 1980. Lutte biologique contre l'acarien rouge en viticulture. I. Répartition, distribution et métode de controle des populations de prédateurs typhlodromes. Rev. Suisse Vitic. Arboric. Hortic. 12: 231-38.
Barnes, M. M. 1981. Variegated grape leafhopper of southern California. p. 137-39. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Bedding, R. A. & L. A. Miller. 1981. Use of a nematode, Heterorhabditis heliothidis, to control black vine weevil, Otiorhynchus sulcatus, in potted plants. Ann. Appl. Biol. 99: 211-16.
Bellows, T. S., Jr. & T. W. Fisher, (eds) 1999. Handbook of Biological Control: Principles and Applications. Academic Press, San Diego, CA. 1046 p.
Bournier, A. 1976. Grape insects. Ann. Rev. Ent. 22: 355-76.
Buchanan, G. A., M. Bengston & E. M. Exley. 1980. Population growth of Brevipalpus lewisi McGregor (Acarina: Tenuipalpidae) on grapevines. Aust. J. Agric. Res. 31: 957-65.
Calvert, D. J. & C. B. Huffaker. 1974. Predator (Metaseiulus occidentalis) - prey (Pronematus spp.) interactions under sulfur and cattail pollen applications in a non-commercial vineyard. Entomophaga 19: 361-69.
Cate, J. R. 1975. Ecology of Erythroneura elegantula Osborn (Homoptera: Cicadellidae) in grape agroecosystems in California. Ph.D. dissertation, Univ. of California, Berkeley.
Clausen, C. P. 1924. The parasites of Pseudococcus maritimus (Ehrhorn) in California (Hymenoptera, Chalcidoidea). Part II. Biological studies and life histories. Univ. Calif. Publ. Ent. 3: 253-88.
Clausen, C. P. 1961. Biological control of western grape leaf skeletonizer (Harrisina brillians B. & McD.) in California. Hilgardia 31: 613-37.
Daane, K. M., D. Gonzalez, D. L. Flaherty, H. Andris, G. Leavitt & W. Bentley. 1990a. Biological control of the variegated leafhopper: II. Field Evaluation. Calif. Table Grape Comm. & Calif. Raisin Adv. Bd., Ann. Crop. Rept. 1989.
Daane, K. M., D. Gonzalez, D. L. Flaherty, G. Y. Yokota & R. F. Gill. 1990b. New Anagrus epos biotypes for variegated leafhopper control in California. 74th Ann. Meet., Pacific Br. Ent. Soc. Amer., Spokane, WA.
Doutt, R. L. & J. Nakata. 1965. Overwintering refuge of Anagrus epos (Hymenoptera: Mymaridae). J. Econ. Ent. 58: 586.
Doutt, R. L. & J. Nakata. 1973. The Rubus leafhopper and its egg parasitoid: An endemic biotic system useful in grape-pest management. Environ. Ent. 2: 381-86.
Duso, C. & V. Girolami. 1985. Strategie di controllo biologico degli acari tetranichidi su vite. Atti XIV Congr. naz. Ital. Ent., Palermo, Erice, Bagheria. p. 719-28.
English-Loeb, G. M., D. L. Flaherty, L. T. Wilson, W. W. Barnett, G. M. Leavitt & W. H. Settle. 1986. Pest management changes affect spider mites in vineyards. Calif. Agric. 40: 28-30.
Flaherty, D. L. 1969. Ecosystem trophic complexity and Willamette mite, Eotetranychus willamettei Ewing (Acarina: Tetranychidae), densities. Ecology 50: 911-16.
Flaherty, D. L. & M. A. Hoy. 1971. Biological control of Pacific mites and Willamette mites in San Joaquin Valley vineyards: Part III. Role of tydeid mites. Res. Popul. Ecol. 8: 80-96.
Flaherty, D. L. & C. B. Huffaker. 1970. Biological control of Pacific mites and Willamette mites in San Joaquin Valley vineyards. I. Role of Metaseiulus occidentalis. II. Influence of dispersion patterns of Metaseiulus occidentalis. Hilgardia 40: 267-330.
Flaherty, D. L. & L. T. Wilson. 1999. Biological control of insects and mites on grapes. In Fisher, T. W. & T. S. Bellows, Jr. (eds) 1999. Handbook of Biological Control: Principles and Applications. Academic Press, San Diego, CA
Flaherty, D. L., M. A. Hoy & C. D. Lynn. 1981a. Spider mites. p. 111-25. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Flaherty, D., F. Jensen & J. Nakata. 1976. Grape mealybug. Grape pest management in the southern San Joaquin Valley. San Joaquin Valley Agr. Res. Ext. Center Publ. 13 p.
Flaherty, D. L., F. L. Jensen, W. L. Peacock & L. Bettiga. 1981b. Grape mealybug. p. 160-64. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H.
Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Flaherty, D. L., W. L. Peacock, L. Bettiga & G. M. Leavitt. 1982. Chemicals losing effect against grape mealybug. Calif. Agric. 36: 15-16.
Flaherty, D. L., L. T. Wilson, V. M. Stern & H. Kido. 1985. Biological control in San Joaquin Valley vineyards. p. 501-20. In: M. A. Hoy & D. C. Herzog (eds.), Biological Control in Agricultural IPM Systems. Academic Press. 589 p.
Gambaro, P. I. 1972. Il ruolo del Typhlodromus aberrans Oudm. (Acarina, Phytoseiidae) nel controllo biologico degli Acari fitofagi dei vigneti del Vernonese. Boll. di Zool. Agraria e di Bachictura Ser. 11: 151-65.
Girolami, V. & C. Duso. 1985. Controllo biologico degli acari nei vigneti. L'Informatore Agrario 41: 83-9.
Gonzalez, D. & L. T. Wilson. 1982. A food-web approach to economic thresholds: A sequence of pests and predaceous arthropods on California cotton. Entomophaga 27: 31-43.
Gonzalez, D., B. R. Patterson, T. F. Leigh & L. T. Wilson. 1982. Mites: A primary food source for two predators in San Joaquin Valley cotton. Calif. Agric. 36: 18-20.
Gonzalez, D., W. White, C. Pickett, V. Cervenka, M. Moratorio & L. T. Wilson. 1988. Biological control of variegated leafhopper in grape IPM program. Calif. Agric. 42: 23-5.
Gonzalez, D., K. M. Daane & D. L. Flaherty. 1990. Biological control of the variegated leafhopper: I. Insectary Production. Calif. Table Grape Comm. & Calif. Raisin Advisory Bd., Ann. Crop Rept. 1989.
Gonzalez, R. H. 1983. Manejo de plagas de la vid. Ciencias Agri. 13, Univ. de Chile. 115 p.
Hoy, M. A. & D. L. Flaherty. 1970. Photoperiodic induction of diapause in a predaceous mite, Metaseiulus occidentalis. Ann. Ent. Soc. Amer. 63: 960-63.
Hoy, M. A. & D. L. Flaherty. 1975. Diapause induction and duration in vineyard-collected Metaseiulus occidentalis. Environ. Ent. 4: 262-64.
Jensen, F. L. & D. L. Flaherty. 1981a. Grape leafhopper. p. 98-110. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Jensen, F. L. & D. L. Flaherty. 1981b. Grape leafroller. p. 147-54. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Jensen, F. L., D. L. Flaherty & D. A. Luvisi. 1981. Thrips. p. 176-88. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Joos, J. L. 1981. Branch and twig borer. p. 201-02. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Jubb, G. L., Jr. 1982. Occurrence of the grape root borer Vitacea polistiformis, in Pennsylvania. Melsheimer Ent. Ser. 32: 20-4.
Jubb, G. L., Jr., E. C. Masteller & R. D. Lehman. 1985. Survey of arthropods in vineyards of Erie County, Pennsylvania. Acari. Intl. J. Acarol. 11: 201-08.
Kamal, M. 1951. Biological control projects in Egypt, with a list of introduced parasites and predators. Bull. Soc. Fouad ler Ent. 35: 205-20.
Kido, H. 1981. Grape erineum mite. p. 217-20. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Kido, H., D. L. Flaherty, W. W. Barnett & H. L. Andris. 1981a. Omnivorous leafroller. p. 126-36. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H.
Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Kido, H., D. L. Flaherty, D. F. Bosch & K. A. Valero. 1984. French prune trees as overwintering sites for grape leafhopper egg parasite. Amer. J. Enol. Vitic. 35: 156-60.
Kido, H., D. L. Flaherty, C. E. Kennett, N. F. McCalley & D. F. Bosch. 1981b. Seeking the reasons for differences in orange tortrix infestations. Calif. Agric. 35: 27-8.
Kido, H., N. F. McCalley & J. L. Joos. 1981c. Orange tortrix. p. 155-59. In: D. L. Flaherty, F. L. Jensen, A. N. Kasimatis, H. Kido, & W. J. Moller (eds.), Grape Pest Management. Univ. Calif., Berkeley, Agric. Sci. Publ. 4105. 312 p.
Makhmudov, D., A. Azimov, A. Z. Abdulagatov & K. G. Ataev. 1977. Control of the grape moth. Zashchita Rastenii 7: 24-5. [in Russian].
Manjunath, T. M. 1985. India - Maconellicoccus hirsutus on grapevine. FAO Plant Prot. Bull. 33: 74.
Marcelin, H. 1985. La lutte contre les tordeuses de la grape. Phytoma 370: 29-32.
McKenzie, L. M. & B. P. Beirne. 1972. A grape leafhopper, Erythroneura ziczac (Homoptera: Cicadellidae), and its mymarid (Hymenoptera) egg-parasite in the Okanagan Valley, British Columbia. Canad. Ent. 104: 1229-33.
Niyazov, O. D. 1969. The parasites and predators of grape mealybug. Zashchita Rastenii 14: 38-40. [in Russian].
Pickett, C. H., L. T. Wilson, D. Gonzalez & D. L. Flaherty. 1987. Biological control of variegated grape leafhopper. Calif. Agric. 41: 14-16.
Rizk, G. A., I. B. Sheta & M. A. Ali. 1978. Chemical control of mites infesting grape-vine in middle Egypt. Bull. Ent. Soc. Egypt, Econ. Ser. 11: 105-11.
Rzaeva, L. M. 1985. Parasites and predators of the grape mealybug (Planococcus ficus Signoret) and introduction of new natural enemies into the eastern Transcaucasus. Biologicheskikh Nauk 4: 34-9.
Saunders, M. C. & J. N. All. 1985. Association of entomophilic rhabditoid nematode populations with natural control of first instar larvae of the grape root borer, Vitacea polistiformis, in concord grape vineyards. J. Invert. Path. 45: 147-51.
Schruft, G. 1972. Les tydéidés (Acari) sur vigne. OEPP/EPPO Bull. 3: 51-5.
Schruft, G. A. 1986. Grape. p. 359-66. In: W. Helle & M. W. Sabelis (eds.), Spider Mites Their Biology, Natural Enemies and Control. Vol. 1B. Elsevier, Amsterdam. 458 p.
Schwartz, A. 1987. Seasonal occurrence of a predaceous mite Amblyseius addoensis Van der Merwe & Ryke (Acari: Phytoseiidae) on table grapes. S. Africa J. Enol. Vitic. 8: 78-9.
Settle, W. H., L. T. Wilson, D. L. Flaherty & G. M. English-Loeb. 1986. The variegated leafhopper, an increasing pest of grapes. Calif. Agric. 40: 30-2.
Tanigoshi, L. K., S. C. Hoyt & B. A. Croft. 1983. Basic biological and management components for mite pests and their natural enemies. p. 153-202. In: B. A. Croft & S. A. Hoyt (eds.), Integrated Management of Insect Pests of Pome and Stone Fruits. John Wiley-Interscience, New York. 454 p.
Trichilo, P. 1986. Influence of the host plant on the interaction of spider mites with their natural enemies in a cotton agroecosystem. Ph.D. dissertation, University of California, Davis.
Wheeler, A. G., Jr., & G. L. Jubb, Jr. 1979. Scymnus cervicalis Mulsant, a predator of grape phylloxera, with notes on S. brullei Mulsant as a predator of woolly aphids on elm (Coleoptera: Coccinellidae). The Coleopterist Bull. 33: 199-204.
Williams, D. W. 1984. Ecology of a blackberry-leafhopper-parasite system and its relevance to California grape agroecosystems. Hilgardia 51: 1-32.
Wilson, L. T., D. L. Flaherty, H. Andris, W. W. Barnett, D. Gonzalez & W. Settle. 1986. The variegated leafhopper: An increasing pest of grapes in the San Joaquin Valley. Proc. 1986 San Joaquin Valley Grape Symposium. p. 27-9.
Wilson, L. T., D. L. Flaherty, W. Settle, C. Pickett & D. Gonzalez. 1987. Managing the variegated leafhopper and grape leafhopper. Proc. Table Grape Symposium 1987: 5-11.
Wilson, L. T., M. A. Hoy, F. G. Zalom & J. M. Smilanick. 1984. Sampling mites in almonds: I. Within-tree distribution and clumping pattern of mites with comments on predator-prey interactions. Hilgardia 51: 1-13.
Winkler, A. J., J. A. Cook, W. M. Kliewer & L. A. Lider. 1974. General Viticulture. Univ. Calif. Press. 710 p.
Yasnosh, V. A. & V. I. Mjavanadze. 1983. On the efficiency and rational use of Cryptolaemus montrouzieri against plant pests in the Georgia SSR. In: Proc. 10th Intern. Cong. Plant Protection 2: 798 p.
Zheng, Y., K. Daane, W. Barnett, K. Hagen, H. Andris & W. Peacock. 1990. Evaluation of release with Chrysoperla carnea for control of variegated leafhopper. USDA-ES Smith Lever Integrated Pest Management Proj. Develop., Interim. Rept. 1990.