Stephen C. Welter
Division of Insect Biology, University of California
Berkeley, CA 94720
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The commercial strawberry (Fragaria x ananassa Duchesne) traces its ancestry to two species, F. chiloensis and F. virginiana, that are native to the New World. These traveled to the Old World where they accidentally hybridized sometime during the mid-1700's (Darrow 1966). The strawberry returned to North America as the domesticated hybrid and, with further breeding, produced the modern large-fruited berry which is now raised all over the world.
Strawberries are commercially grown in over a dozen states but California and Florida account for the majority of US strawberries. In California, 22,000 acres are under strawberry cultivation primarily along the central and southern coast. Ever bearing cultivars raised on the central coast are harvested every three days from April till the end of the year and, as a result, California contributes over 80 % of fresh and frozen berries to the domestic market.
In the US, cultivation, marketing, and pest management practices vary depending on geographic location. In several locations in the North East and the Midwest, the crop is raised on small farms along with diverse other crops and with minimal pest control. Berries are harvested primarily in the summer and are often sold at the farm or as pick-your-own berries. In contrast, on the central coast in California, there are large monocultures of strawberries, the crop is intensely managed, and, after harvest the berries are sent to coolers before being shipped long distances. While the strawberry plant is a perennial herb, it is commercially raised as an annual in California since quality and yield are highest in the first year. Besides, after the first year, certain pest problems increase. Annual strawberries are typically transplanted in fall after the soil is fumigated for control of weeds and soil borne pathogens.
Arthropod pests that attack strawberries cause varying levels of damage. In the past, control strategies applied for suppression of one pest have led to secondary pest outbreaks thus emphasizing the importance of adopting an integrated approach to pest management. Chemical control options are limited to those with short re-entry periods because berries are harvested at three day intervals. On the other hand, due to the high cash value of the crop, augmentative biological control is economically feasible and is currently adopted widely for spider mite suppression. Strategies for control of other pests need to be selected so as to be least disruptive to the spider mite biological control program. Management tactics for individual arthropod pests are outlined below.
Strawberries are attacked by the western tarnished plant bug, Lygus hesperus Knight (Hemiptera: Miridae), in the west, and the closely related L. lineolaris (Palisot de Beauvois) in the rest of the United States (Allen and Gaede 1963). Both species are native and polyphagous and feed on several weeds. The adults appear nomadic, moving from one plant to another as each plant begins to flower. In central coastal California, L. hesperus overwinter as adults in weeds. In spring when the rains cease and the weeds dry out, the adults rapidly colonize strawberries. Whereas strawberries are not a preferred host of Lygus in California, the absence of other more attractive plants in late spring is perhaps the basis for extensive colonization of strawberries. At least two generations develop between April and August in strawberries in this area.
Lygus adults are about 6 mm long and variable in color. They are characterized by a conspicuous yellow or pale green 'v' on the scutellum. Female insert eggs into various host plant tissues and often only the operculum is visible externally and hence the eggs are not easily detectable. The first and second instars are pale green with a distinct red terminal antennal segment. The third through fifth instars are green and have five black dots on the back (1939).
Feeding by all five nymphal instars and by adults causes distortion of the berries, known as catfacing, rendering the fruits unacceptable for fresh market sale. Distortion of the berries occurs when feeding by Lygus destroys developing embryos in achenes (seeds) during early fruit development, preventing growth of the fruit tissue beneath and surrounding the damaged achenes. Lygus nymph densities are estimated by beating plants onto a clean enclosed surface such as a white pan. Since adults are very mobile, their numbers are best estimated by vacuuming plants using a leaf blower modified to act as a vacuum. Economic damage occurs when there are 1 or 2 Lygus per 20 plants (UCIPM 1994).
Chemical Control: Insecticides that are available for use in strawberries are most effective against the early instars hence applications need to be timed to periods soon after egg hatch. Lygus adults migrate to strawberries from weeds when flowering commences hence plants need to be monitored in spring to determine the first appearance of Lygus adults. Egg hatch can be estimated using the degree-day (DD) model (Pickel et al. 1990). Using a base temperature of 54° F, eggs hatch is estimated to occur at 252° F DD, and on the central coast in California this translates to approximately 3 - 4 weeks under cool spring temperatures. The insecticides available for use in strawberries include the organophosphates malathion and naled, the carbamate methomyl and the pyrethroids, fenpropathrin and bifenthrin. The pyrethroids provide control for extended periods but there is concern about their negative impacts on existing natural enemies. Naturally occurring predators at risk include bigeyed bugs, Geocoris spp., minute pirate bugs, Orius spp., green and brown lacewings, Chrysoperla and Hemerobius spp., damsel bugs, Nabis spp., the convergent lady beetle, Hippodamia convergens Guérin-Méneville and several species of spiders, which feed on aphids, white flies and lepidopteran pests besides feeding on Lygus nymphs and eggs.
Cultural control: Efforts to suppress Lygus populations using methods alternative to that of insecticide applications involve the use of a tractor mounted vacuum device, the BugVac (Pickel et al. 1994). These remove adults but have limited impact on the early instars. Lygus adults are mobile and rapidly migrate into strawberries after passage of the vacuum. In addition, frequent use of the BugVac, which is necessary for effective control, makes this an expensive strategy. A strategy that has been tested in cotton (Sevacherian and Stern 1974; Godfrey and Leigh 1994) and is now being evaluated in strawberries is the use of trap crops. Since Lygus adults do not prefer strawberries, it may be possible to trap adults in preferred crops planted adjacent to strawberries thereby reducing Lygus numbers in strawberries. Control measures can then be concentrated in the trap crop. Biological control: Naturally occurring predators listed above feed on Lygus eggs and nymphs but do not keep populations below the economic injury level. L. hesperus and L. lineolaris are native and are attacked by a few native parasitoids including the egg parasitoid, Anaphes iole Girault (Hymenoptera: Mymaridae), and the nymphal braconid parasitoids Leiophron uniformis (Gahan), Peristenus pallipes (Curtis) and P. pseudopallipes, which are present in low numbers in different regions in the US (Clancy and Pierce 1966; Gordon et al. 1987; Day 1996) but, under non-manipulated conditions, do not provide adequate Lygus control.
Of these native species, A. iole appears to have the greatest potential for suppressing Lygus populations in strawberries. Adult wasps are minute (0.6 mm) and black. The species is widely distributed in North America (Huber and Rajakulendran 1988). Natural parasitism of Lygus eggs in alfalfa ranges from around 50 to 85 % (Jones and Jackson 1990). The wasps are commercially available and have been released for Lygus suppression in strawberries raised in small acreages under sustainable systems of farming in California and on the east coast. In experimental plots in conventional strawberries augmentative releases of adult wasps @ 37,500/ha/wk provided 43 % Lygus suppression (Norton and Welter 1996) and efforts are under way to modify release strategies and enhance performance of the parasitoid. Integration of Anaphes releases with chemical control aimed at nymph suppression may be possible by use of a selective insecticide and appropriate timing of parasitoid releases to minimize the negative impacts of the spray applications. Of the insecticides that are registered for use in strawberries, the organophosphate naled appears to be the most compatible with releases of A. iole (pers. obs.) Another possible approach is integrative biological control. Classical biological control of L. lineolaris with the nymphal braconid parasitoid Peristenus digoneutis (Day et al. 1990; Day 1996) is under evaluation on the east coast. If Lygus populations can be suppressed in the weeds with a classical biological control agent, colonization of strawberries will be reduced and effective biological control with Anaphes may be achieved. Another strategy under consideration is control of Lygus nymphs in strawberries with the fungal pathogen Beauveria bassiana (Balsamo) Vuillemin which has potential in areas with high humidity, such as central coastal California, since moisture is critical for development of the fungus.
The twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is a serious pest of strawberries in all California growing areas. Spider mites live on a wide variety of crops and weeds and are carried from crop to crop by the wind. In strawberries the mites can be detected primarily on the underside of the leaves.
Adults are less than 0.5 mm, yellow or pale green with a large dark spot on each side of the abdomen. Immatures are smaller in size but similar in appearance though the dark spots are absent in the earliest stage (Allen 1959). Eggs laid on the leaves are spherical and translucent and visible with a hand lens.
Twospotted spider mites attack new strawberry plantings in fall and their populations build up rapidly. Adults and immatures suck juices from the plant and feeding by mites causes plants to lose vigor ultimately resulting in decreased fruit yield and size. When infestation is severe, plants die if spider mites are uncontrolled. Early detection is critical hence plants need to be monitored regularly by examination of leaves under magnification. In addition mite populations can be estimated using a mite brush. The economic threshold is 5-10 active mites per leaflet (UCIPM 1994).
Chemical Control: Since spider mites are present primarily on the lower leaf surfaces, for chemical control to be effective, good coverage of the undersides of leaves is critical. However, options for chemical control are limited. In 1995 avermectin was the only miticide that was available. In the past two years, the pyrethroids fenpropathrin and bifenthrin have been registered for use in strawberries. These pyrethroids are also registered for L. hesperus control but a higher concentration is required for spider mite suppression. While pyrethroids are effective, minimal use is recommended due to the negative impacts on beneficials in the system.
Biological Control: In strawberries, the two spotted mite can be suppressed with augmentative releases of the introduced predator mite, Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae). P. persimilis is commercially available from several sources either mixed with vermiculite or on bean plants that are placed among strawberry plants. Predatory mites released @ 10-20,000 per acre early in the season when mite populations are low provide effective control (Decou 1994). Releases of P. persimilis provide an economically feasible control option due to the limited number of pesticide options. Also, with increase in demand, the price of P. persimilis has reduced by over 50 % in the past 10 years.
Occasionally strawberries are damaged by the cyclamen mite, Phytonemus pallidus Banks (Acari: Tarsonemidae). The cyclamen mite is extremely small and not visible with a hand lens. The immature stages are translucent while the mature mites are pink and shiny (Allen 1959). They are found in the midvein of unopened leaves and under the calyx of emerging flower buds. Heavy infestation causes stunting and distortion of fruits and plants. Infestations are generally localized until higher densities of cyclamen mites are obtained hence early detection is beneficial. Cyclamen mites were a serious problem in the late fifties (Allen 1959) when strawberry plants were maintained for several years but are less of a problem with the shift to annual plantings.
The western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) are frequently found feeding in strawberry flowers but usually do not cause significant damage. When populations build up, blossoms may fall or fruit development may be affected resulting in a 'seedy' berry condition or in fruit-bronzing (Allen 1959) but most cultivars can tolerate western flower thrips populations without economic damage and treatment is usually not recommended.
The strawberry whitefly, Trialeurodes packardi (Morrill), the greenhouse whitefly, T. vaporariorum (Westwood), and the iris whitefly, Aleyrodes spiroeoides Quaintance (Homoptera: Aleyrodidae) attack strawberries especially when plants are stressed. Adults are powdery white and about 2 mm long. Eggs are white and laid vertically on the underside of leaves. Nymphs are flattened and pale yellow in color. The nymphs suck on plant juices and secrete sticky honeydew on which sooty mold grows.
Whitefly populations are usually kept under control by naturally occurring parasitic wasps and generalist predators. However, chemical control of other pests such as the tarnished plant bugs or the two spotted mite can have a negative impact on the natural enemies, leading to whitefly outbreaks. Removal and destruction of older leaves will reduce whitefly populations and this may facilitate build up of natural enemies. Chemical control of whiteflies in strawberries is not recommended.
Several aphid species, including the strawberry aphids, Chaetosiphon fragaefolii (Cockerell) and C. thomasi Hille RisLambers, the cotton / melon aphid, Aphis gossypii Glover, the potato aphid Macrosiphon euphorbiae (Thomas) and the green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae) attack strawberries in California. Immatures suck the juice of the plants and deposit honey dew on fruits which permit development of soot mold. Strawberry plants can tolerate high aphid populations without causing direct injury (Allen 1959). Coccinellids, lacewing larvae and other general predators and parasitoids attack aphids and keep populations from reaching damaging levels.
Occasionally strawberries are attacked by lepidopteran pests such as the corn earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) which can cause serious damage since the caterpillars bore into the fruit soon after hatching and feed within. Control measure need to be applied before the caterpillar enters the fruit hence monitoring of adults is critical. Adults are nocturnal hence they can best be monitored with pheromone traps. The cutworms, Agrotis ipsilon (Hufnagel) and Athetis mindara (Barnes & McDunnough), and the beet armyworm Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) can cause considerable damage in localized areas of strawberry fields. Larvae feed voraciously at night but hide during the day usually beneath the soil surface. They attack the crowns of young plants but they are most damaging when they feed on the fruits. Larval control of armyworms can be achieved with the microbial insecticide Bacillus thuringiensis Berliner subsp. kurstaki. while baits treated with insecticide can be used for cutworms.
The strawberry root weevil, Otiorhynchus ovatus (Linnaeus) and other weevils such as Nemocestes incomptus (Horn) and Asynonychus godmani Crotch (Coleoptera: Curculionidae) are minor pests in California. Adults are gray to black, less than 1 cm long with a curved snout and elbowed antennae. Damage is caused by larvae which are white or pink, C-shaped and legless. They feed on strawberry roots and crowns causing plants to wilt and die. Larvae overwinter in the soil and are destroyed by soil fumigation and hence root weevils are usually not a problem in California.
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