Trichoplusia ni (Hiibner) Lepidoptera: Noctuidae
Distribution. The origin of cabbage looper is uncertain, but it is now found in Africa, Asia, Europe, and in the Americas. In North America, it is found throughout Canada, Mexico, and the United States wherever crucifers are cultivated. Overwintering in the United States apparently occurs only in the southernmost states, however. It is somewhat erratic in occurrence?typically very abundant one year, and then scarce for 2-3 years; this is likely due to nuclear polyhedrosis virus and differing success in dispersal from southern to northern areas. Cabbage looper is highly dispersive, and is sometimes found at high altitudes and far from shore. Flight ranges of approximately 200 km have been estimated.
Host Plants. Cabbage looper feeds on a wide variety of cultivated plants and weeds. As its common name implies, it feeds readily on crucifers, and has been reported damaging broccoli, cabbage, cauliflower, Chinese cabbage, collards, kale, mustard, radish, rutabaga, turnip, and watercress. Other vegetable crops injured include beet, cantaloupe, celery, cucumber, lima bean, lettuce, parsnip, pea, pepper, potato, snap bean, spinach, squash, sweet potato, tomato, and watermelon. Additional hosts are flower crops such as chrysanthemum, hollyhock, snapdragon, and sweetpea, and field crops such as cotton and tobacco. With such a wide range of crops serving as suitable hosts, it is not surprising that an extremely wide range of broadleaf weeds also serve as hosts (Eichlin and Cunningham, 1978; Soo Hoo et al. 1984), though the weeds vary somewhat with geographic locale, depending on availability. Surprisingly few common agricultural weeds are frequent hosts; among those that are suitable are lambsquarters, Chenopodium album; wild lettuce, Lactuca spp.; dandelion, Taraxacum officinale; and curly dock, Rumex crispus.
Despite the wide host range of cabbage looper, not all hosts are equivalent. For example, Elsey and Rabb (1967) compared the suitability of collards and tobacco and reported differing suitabilities. Adults preferred to oviposit on collards when given a choice, and early instar survival was higher on collards. However, once the third instar was attained, survival was equivalent on both hosts, and pupal weights were only slightly diminished when larvae were reared on tobacco. Sutherland (1966) studied the growth rate of cabbage looper fed on a wide variety of crops and weeds. He found relatively small differences among the different crucifer crops, and many other vegetable crops and some weeds were equally suitable for larval growth. Soo Hoo et al. (1984) conducted one of the most complete studies of relative suitability, and reported that only about one-third of the plants tested were suitable for complete development of larvae.
A survey of looper pests infesting crops in Alabama revealed that though cabbage looper could be recovered from numerous hosts (clover, cotton, crucifers, peanut, soybean, sweet potato, tomato), most were found on cotton and crucifer crops. Soybean looper, Pseudoplusia includens (Walker), an insect easily confused with cabbage looper and having a similar broad host range, occurred predominately on soybean (Canerday and Arant, 1966).
The adults feed on nectar from a wide range of flowering plants, including clover, Trifolium spp.; goldenrod, Solidago canadensis; dogbane, Apocynum spp.; sunflower, Helianthus spp.; and others.
Natural Enemies. Cabbage looper is attacked by numerous natural enemies, and the effectiveness of each seems to vary spatially, temporally, and with crop environment. Most studies noted the effectiveness of wasp and tachinid parasitoids, and a nuclear polyhedrosis virus (NPV). Predation has not been well-studied except in cotton.
In studies conducted on collards in North Carolina, Elsey and Rabb (1970a) observed considerable variation in the impact of natural enemies between years. They determined that Trichogramma (Hymenoptera: Trichogrammatidae) egg parasitoids were not very important; they were reared from less than 5% of the eggs. They identified no major mortality factors until the fifth instar, despite the presence of considerable disappearance during this period. Either predators or weather could account for these larval deaths. During the latter instars, Voria ruralis (Fallen) (Diptera: Tachinidae), an endoparasite attacking the medium-or large-size larvae, was the dominant cause of death, accounting for an average of about 53% mortality. Elsey and Rabb (1970b) presented the biology of this important parasitoid. Trichoplusia ni NPV caused about 12% mortality, and undetermined fungi about 10%. Copidosoma truncatellum (Dalman) (Hymenoptera: Encyrtidae) was the other significant mortality factor, but accounted for only 6-7% mortality. Copidosoma truncatellum oviposits in cabbage looper eggs, emerging from and killing the mature larvae or pre-pupae.
In studies conducted in California involving cabbage, Oatman and Platner (1969) reported that egg parasitism of cabbage looper by Trichogramma, while variable, could reach about 35%. Larval parasitism averaged 38.9%, and tended to increase toward the end of the year. The tachinid V. ruralis was the dominant parasitoid, and was especially abundant in the autumn and winter months. The other principal parasitoids, especially during summer and autumn, were C. truncatellum and Hyposoter exiguae (Viereck) (Hymenoptera: Ichneumonidae). The latter species is a solitary endoparasite that attacks small larvae. A total of 24 species of parasitoids were observed: 14 wasps and 10 flies. Despite the abundance of parasitoids, however, the authors concluded that T. ni NPV was the key factor affecting populations.
In Ontario, Harcourt (1963a) indicated that C. trun-catellum was the most important parasitoid. No data were provided, but cabbage looper populations were said to be "frequently destroyed" by NPV.
One of the most complete studies of cabbage looper natural enemies was conducted in California by Ehler (1977a,b), on cotton. He determined that the egg and early larval stages experience most of the generational mortality, and that predators and C. truncatellum were the most important elements contributing to this mortality. During the early larval instars, the minute pirate bug, Orius tristicolor (White) (Hemiptera: Anthocori-dae), the big-eyed bug, Geocoris palens Stal (Hemiptera: Lygaeidae), and the damsel bug, Nabis americoferis Carayon (Hemiptera: Lygaeidae) were the predators responsible for most of the mortality. Ehler documented several mortality factors during the middle larval instars. The parasitoid Microplitis brassicae Muesebeck (Hymenoptera: Braconidae), a solitary endoparasite attacking small larvae, was the dominant mortality factor, but rarely exceeded 20% mortality. Other factors included H. exiguae and T. ni NPV, but both at levels of less than 10% mortality. During the late larval instars C. truncatellum inflicted 40-50% mortality, and V. ruralis and T. ni NPV each caused less than 10% mortality. Pupal mortality was insignificant.
Predation is rarely studied as it is very difficult to measure accurately. Barry et al. (1974) attempted to assess the potential of selected predators of cabbage looper by using caged populations in Missouri. They reported that the damsel bug Nabis alternatus Parshley (Hemiptera: Nabidae) was most effective, the big-eyed bug Geocoris punctipes (Say) (Hemiptera: Lygaeidae) was intermediate, and the green lacewing Chrysoperla carnea (Stephens) was relatively ineffective in predation of cabbage looper on soybean. Sutherland (1966) suggested that general predators, including yellow-jackets (Hymenoptera: Vespidae) and birds, could be important mortality factors.
The T. ni NPV is well-studied. Larvae normally die within 5-7 days of consuming virus inclusion bodies. Early signs of larval infection are a faint mottling of the abdomen in the area of the third to the sixth abdominal segments. This is followed by a more generalized blotchy appearance, and the caterpillar eventually becomes creamy white swollen, and limp. Death usually follows within hours following the limp condition, and caterpillars are often found hanging by their prolegs. Dark blotches appear after death, and the integument becomes very fragile and eventually ruptures. The body contents, heavily contaminated with new inclusion bodies, drip onto foliage where they can be consumed by other larvae (Semel, 1956; Drake and McEwen, 1959). Hofmaster (1961) reported that looper populations in Virginia were highest during dry weather because rainfall assisted the spread of NPV, and that this virus greatly suppressed loopers. In New York, Sutherland (1966) indicated that though T. ni NPV was an important mortality factor, natural incidence did not appear adequate to protect crops from damage.
Life Cycle and Description. The number of generations completed per year varies from two to three in Canada, five in North Carolina, from five to seven in California. The generations overlap considerably, and therefore are indistinct. Development time (egg to adult) requires 18-25 days when insects are held at 32-21 ?C, respectively (Toba et al, 1973), so at least one generation per month could be completed successfully under favorable weather conditions. There is no diapause present in this insect, and though it is capable of spending considerable time as a pupa, it does not tolerate prolonged cold weather. It reinvades most of the United States and all of Canada annually after overwintering in southern latitudes. The lower limit for development is about 10-12?C, and 40?C is fatal to some stages. Cabbage looper is considered to be a warm-weather insect; even in areas where it successfully overwinters it rarely occurs in high numbers until there has been adequate time for 2-3 spring generations. Sutherland (1966) conducted a survey of entomologists along the Atlantic coast, and reported that looper populations were present year-round as far north as coastal South Carolina, and that looper infestations commenced in North Carolina and Maryland in May, in New Jersey in June, and in New York in July. Pennsylvania was not infested until August. Subsequent research by Chalfant et al. (1974) clarified the winter activity patterns of cabbage looper in the southeastern United States: continuous activity and reproduction occur only in the part of Florida south of Orlando; the part of Georgia south of Byron as well as southeast South Carolina have intermittent adult activity during the winter months, depending on weather; all points north of this have no winter activity.
Egg. Cabbage looper eggs are hemispherical in shape, with the flat side affixed to foliage. They are deposited singly on either the upper or lower surface of the leaf, though clusters of 6-7 eggs are not uncommon. The eggs are yellowish-white or greenish, bear longitudinal ridges, and measure about 0.6 mm wide and 0.4 mm high. They hatch in about two, three, and five days at 32?, 27?, and 20?C, respectively, but require nearly 10 days at 15?C (Jackson et al, 1969).
Larva. Young larvae initially are dusky white, but become pale green as they commence feeding on foliage. They are somewhat hairy initially, but the number of hairs decreases rapidly as larvae mature. Larvae have three pairs of prolegs, and crawl by arching their back to form a loop and then projecting the front section of the body forward. The mature larva is predominantly green, but is usually marked with a distinct white stripe on each side. The thoracic legs and head capsule are usually pale green or brown. Dorsally, the larva bears several narrow, faint white stripes clustered into two broad white bands. In some cases the mature larva is entirely green. The body is narrower at the anterior end, and broadens toward the posterior. It measures 3-4 cm long at maturity. Cabbage looper is easily confused with other loopers, but can be distinguished from most by the presence of small, nipple-like structures (vestigial prolegs) located ventrally on abdominal segments three and four. Soybean looper, Pseudoplusia includens (Walker), also bears these structures, but usually has dark thoracic legs. Also, under high magnification it is possible to observe micro-spines on the body of soybean looper?a feature lacking from cabbage looper.
The number of instars was given as 4-7 by Shorey et al. (1962), but many authors indicated only five. McEwen and Hervey (1960) gave mean head capsule width measurements as 0.29, 0.47, 0.74, 1.15, and 1.79 mm, respectively, for instars 1-5. Larval development required 17.8 and 19.9 days when reared on bean and held at 23? and 32?C, respectively. When reared on cabbage at the same two temperatures, larval development required 19.9 and 20.8 days, respectively (Shorey et al., 1962). Development was also studied by Toba et al. (1973), who determined that the number of larval instars could be increased from five to six by exposing the larvae to cooler temperature. Cool temperature also resulted in lowered egg production by ensuing adults. (See color figure 45.)
Pupa. At pupation, a white, thin, fragile cocoon is formed on the underside of foliage, in plant debris, or among clods of soil. The pupa contained within is initially green, but soon turns dark brown or black. The pupa measures about 2 cm long. Duration of the pupal stage is about 4, 6, and 13 days at 32?, 27?, and 20?C, respectively.
Adult. The front wings of the cabbage looper moth are mottled gray-brown; the hind wings are light brown at the base, with the distal portions dark-brown. The forewing bears silvery white spots centrally: a "U"-shaped mark and a circle or dot that are often connected. The forewing spots, though slightly variable, serve to distinguish cabbage looper from the most other crop-feeding noctuid moths. The moths have a wingspan of 33-38 mm.
After a pre-oviposition period of about 1-2 days, females begin depositing their eggs, initially at about 80 per night. During the adult stage, which averages 10-12 days, 300-600 eggs are produced by females having access to food, and less than 100 when only water is provided (Shorey, 1963). Moths are considered seminocturnal because feeding and oviposition sometimes occurs about dusk. They may become active on cloudy days or during cool weather, but are even more active during the night-time hours. They oviposit readily at temperatures as low as 15.6?C (Henneberry and Kishaba, 1967), but flight activity is higher on warmer evenings (Sutherland, 1966). (See color figures 230 and 231.)
Rearing procedures was given by McEwen and Hervey (1960) for plant-based culture, and Shorey and Hale (1965) for artificial diet. Cabbage looper larvae are included in the keys by Okumura (1962) and Capinera (1986), and are included in a key to common loopers in Appendix A. Adults are included in the keys of Rings (1977a) and Capinera and Schaefer (1983).
Cabbage looper replaced imported cabbageworm, Pieris rapae (Linnaeus), as the dominant cabbage caterpillar in the 1950s, apparently due to greater susceptibility of the latter to most insecticides. In recent years, diamondback moth has emerged as a more important caterpillar pest than cabbage looper; nevertheless, T. ni can be a serious problem. In studies conducted in South Carolina, diamondback moth was the major caterpillar pest in the spring crucifer crop, whereas cabbage looper predominated in the autumn crop (Reid and Bare, 1952). In Florida and Texas, however, spring populations of cabbage loopers can be damaging-
Cabbage loopers are leaf feeders, and in the first
three instars they confine their feeding to the lower leaf surface, leaving the upper surface intact. The fourth and fifth instars chew large holes, and usually do not feed at the leaf margin. For cabbage, however, they feed not only on the wrapper leaves, but also may bore into the developing head. Larvae consume three times their weight in plant material daily (McEwen and Hervey, 1960). Feeding sites are marked by large accumulations of sticky, wet fecal material.
Despite their voracious appetite, larvae are not always as destructive as presumed. In California studies, feeding on celery during the first one-half of the growing season did not constitute loss because these petioles were routinely stripped from the plant at harvest (van Steenwyk and Toscano, 1981). With cabbage, moderate defoliation before head formation is similarly irrelevant. In Texas, average population densities of 0.3 larvae per plant justify control (Kirby and Slos-ser, 1984). In New York, Ohio, and Ontario, a density of 0.5 larvae per plant has been used as a treatment threshold (Shelton et al, 1983b). In Florida and Georgia, one new feeding site per head is considered the damage threshold (Workman et al, 1980). Recent work in Canada suggested that an appropriate action threshold was 40% of plants infested (Dornan et al, 1995). Cabbage looper can be a serious contaminant of fresh market broccoli and processed peas.
Sampling. Various sampling strategies have been developed for cabbage looper, and many approaches include consideration of the other crucifer-feeding caterpillars. Fixed sample units of at least 40 plants are sometimes recommended. However, sequential sampling (Shepard, 1973a) and variable intensity sampling (Hoy et al., 1983) protocols have been developed to minimize the amount of sampling required to make appropriate management decisions. Dornan et al. (1995) recommended a binomial (presence-absence) approach because it eliminated counting and insect identification.
Blacklight traps and pheromone traps have been used in an attempt to predict looper population densities. Moth catches are monitored effectively by light traps (Hofmaster, 1961), but NPV, spread by rain, affects larval abundance and damage, thereby reducing predictability. The cabbage looper sex pheromone has at least seven chemical components, but not all are required to elicit attraction (Linn et al., 1984). Pheromone releasers and blacklight traps can be combined to increase moth catches, an approach that has been studied for area-wide suppression of cabbage loopers (Gentry et al., 1971). Although numerous moths have been trapped by such techniques, and insects significantly decreased, suppression has not proven to be adequate to protect lettuce from damage (Debolt et al, 1979).
Insecticides. Insecticide resistance has become a problem in cabbage looper control, but susceptibility varies widely among locations (Shelton and Soder-lund, 1983). Botanical insecticides such as rotenone are less effective against cabbage looper than other cabbage-feeding Lepidoptera (Dills and Odland, 1948), but neem functions as both a feeding deterrent and growth regulator (Isman, 1993).
Biological Control. Microbial insecticides currently play a role in cabbage looper management, and their potential role has yet to be fully realized. Bacillus thuringiensis has long been used for effective suppression of cabbage looper (Kennedy and Oatman, 1976; Gharib and Wyman, 1991; Leibee and Savage, 1992), and has the advantage of not disrupting populations of beneficial insects. T. ni NPV is effective (Hall, 1957), but it has not been commercialized because of the narrow host range. Home gardeners sometimes collect loopers dying of T. ni NPV, grind up the larval cadavers, and concoct their own effective microbial control agent. A nuclear polyhedrosis virus from alfalfa looper, Autographa californica (Speyer), has a wide host range, including cabbage looper (Jaques, 1977; Vail et ah, 1980; Tompkins et ah, 1986); it likely will become a useful tool for cabbage looper management.
Mass release of Trichogramma spp. has been investigated for cabbage looper suppression. Looper egg parasitism can be increased several-fold by careful timing of parasitoid release (Oatman and Platner, 1971). Effectiveness varies among crops, however. This approach was most suitable in tomato, but also effective in crucifers and pepper (Martin et al., 1976b).
Cultural Practices. Some differences in crucifer susceptibility have been observed. In New York, Dick-son and Eckenrode (1975) found few significant differences, but red cabbages tended to be more resistant than kale or Chinese cabbage. In Wisconsin, Chinese cabbage, mustard, rutabaga, and turnip were less preferred for oviposition, whereas cabbage, Brussels sprouts, and collards were highly preferred. Unfortunately, there was no correlation between crops and varieties resistant to cabbage looper, and resistance to imported cabbageworm (Radcliffe and Chapman, 1966). Among cabbage cultivars studied in North Carolina, mammoth red rock and savoy perfection drumhead cultivars are considered to be relatively resistant, but this resistance dissipated under heavy insect feeding pressure. Interestingly, in this case the resistant varieties received high numbers of cabbage looper eggs, but larval survival was poor (Chalfant and Brett, 1967). In studies of broccoli susceptibility in Virginia, Vail et al. (1991) found that early maturing varieties were less subject to attack than late maturing varieties. Row covers, where economically practical, are effective at preventing cabbage looper moths from depositing eggs on crops.