Southern Green Stink Bug Nezara viridula Linnaeus Hemiptera Pentatomidae

Natural History

Distribution. Southern green stink bug has a world-wide distribution. It is found on all continents where agriculture is practiced, but absent or rare from regions with cold winters. Its origin is probably eastern Africa, and was first observed in the western hemisphere in 1798. Distribution in North America is limited primarily to the southeastern United States — Virginia to Florida in the east, to Ohio and Arkansas in the midwest, and to Texas in the southwest. However, it has become established in Hawaii (in 1961) and California (in 1986), and occasional specimens have been found elsewhere outside the generally infested southeast. Southern green stink bug is a strong flier, and its range is expanding in many parts of the world.

Host Plants. The host range of this insect includes over 30 families of plants, though it shows a preference for legumes and crucifers. Preference among plants varies during the year, with this stink bug most attracted to plants that are producing pods or fruit. As plants senesce, the bugs move to more succulent hosts. Among vegetables attacked by southern green stink bug are artichoke, bean, Brussels sprouts, cabbage, cauliflower, collards, corn, cowpea, cucumber, eggplant, mustard, okra, pea, pepper, potato, radish, squash, sweet potato, tomato, and turnip. Outside of North America, this insect is most commonly known as "green vegetable bug,'' an indication of its most frequent host selection. However, it feeds readily on other crops, and is known to attack field crops such as corn, clover, cotton, peanut, soybean, sugarcane, rice, and tobacco as well as fruits such as blackberry, grapefruit, lime, mulberry, orange, and peach. In many tropical areas, this bug is considered a limiting factor in soybean production. Weeds commonly serve as hosts. Some of the wild plants fed upon by this bug are beggarweed, Desmodium tortuosum; castor bean, Ricinus communis; dock, Rumex sp.; nutgrass, Cyperus esculentus; lambsquarters, Chenopodium album; passion flower, Passiflora incarinata; pigweed, Amaranthus spp.; rattlebox, Crotalaria usaramoensis.; wild grape, Vitus sp.; and wild plum, Prunus sp.

Southern green stink bug, a long-lived and strong flier, moves readily among host plants. Some of the host associations are not true expressions of preference or suitability, but reflect availability. Also, host plants that are suitable for one stage may be unsuitable for another. Velasco and Walter (1992), for example, showed that castor bean was good for adult survival and egg production, but poor for nymphal survival. Corn also favors adult survival, but inhibits reproduction. Wild crucifers are not optimal hosts, but early in the season they are abundant and are the best hosts available, so they favor population increase. Soybean favors survival of both nymphs and adults, but is not especially attractive to these insects.

Natural Enemies. As might be expected of an insect with a world-wide distribution, numerous para-sitoids and predators are known. Over 50 species of parasitoids are known, most as egg parasitoids, and most not specific to southern green stink bug (Jones, 1918a). The most common parasitoids in North America tend to be the egg parasitoid Trissolcus basalis (Wol-laston) (Hymenoptera: Scelionidae) and the adult parasitoid Trichopoda pennipes (Fabricius) (Diptera: Tachinidae).

Trichopoda parasitizes high proportions of green stink bug populations on several crops, with the proportion parasitized increasing through the growing season (Todd and Lewis, 1976; Buschman and Whit-comb, 1980; McLain et al., 1990). This insect is thought by some to be a complex of cryptic species, however, so the ecological relationship is uncertain. Trichopoda spp. were introduced into Hawaii and were credited with providing effective biological control on most crops.

Other North American parasitoids include Anastatus sp. (Hymenoptera: Eupelmidae), Ooencyrtus sp. (Hymenoptera: Encyrtidae), Telenomus spp. (Hyme-noptera: Scelionidae), and others; Jones et al. (1996) provided a list of parasitoids. Hoffman et al. (1991b) reported on the successful introduction of Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) to California to aid in the suppression of southern green stink bug.

Predators of southern green stink bug are numerous, and Stam et al. (1987) gave a detailed assessment of predation in Louisiana soybean. Common egg predators were red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), grasshoppers (Or-thoptera: Acrididae and Tettigoniidae), and southern green stink bug nymphs. Common nymphal predators were big-eyed bug, Geocoris spp. (Hemiptera: Lygaei-dae); damsel bug, Reduviolus roseipennis Reuter (Hemi-ptera: Nabidae); and other insects in the orders Hemiptera and Coleoptera. Spiders sometimes caused significant predation. Predators, including birds, were also discussed by Drake (1920).

The relative importance of egg predators and parsitoids was examined by Shepard et al., (1994) in South Carolina. Stink bug egg clusters were introduced into several crops and their fate determined. The principal egg parasitoid was Trissolcus basalis, accouting for about 95% of parasitism. Predation (disappearance of eggs) and parasitism varied in relative importance among crops, seasons, and years; on average, predation and parasitism were about equally important. The action of natural enemies sometimes resulted in complete destruction of egg clusters.

Diseases of stink bug are poorly known. However, viruses affecting southern green stink bug were recently found in South Africa (Williamson and von Wechmar, 1995).

Life Cycle and Description. The southern green stink bug overwinters in the adult stage, and enters diapause when the length of photophase falls to 1213 h. The number of generations annually is estimated at 4-5, with considerable overlapping late in the season. About 45 days are required for a complete life cycle during the summer months. Todd and Herzog (1980) indicated the following "typical" pattern of stink bug phenology in the southeastern United States: inactive adults overwinter until February or March, and when they become active they feed on crucifers and small grains; first generation nymphs and adults are present in March and April and feed on clover; second and third are present from May through July and feed on tobacco, corn, and vegetables, especially tomato; third generation adults disperse to soybean, where fourth generation nymphs and adults and fifth generation nymphs feed and develop until October or November; fifth generation adults disperse to crucifers or other late season hosts, and overwinter. With the onset of warm days in the spring, overwintered adults begin to copulate. The process is protracted, often lasting more than a day, and multiple matings are commonplace. Following 2-3 weeks of feeding the egg production commences.

  1. The eggs are laid in clusters, generally on the lower surface of foliage, and with about 60 eggs (range 30-130 eggs) per cluster. Females normally produce 1-3 egg clusters, with total production ranging from 45 eggs when adults are provided only with relatively poor hosts, to 160 eggs when provided with good host plants. The eggs are deposited in regularly shaped, hexagonal clusters, with the individual eggs ordered in regular rows and glued together. They are affixed to the plant on end, with the top or visible end somewhat flattened, and the bottom end rounded. The eggs measure about 1.3 mm long and 0.9 mm wide. They are yellowish-white to pinkish-yellow and the top, or cap, is clearly indicated by a ring and 28-32 minute spines. The eggs darken in color as incubation proceeds, and hatching occurs after about 5 days. Hatching occurs synchronously in the egg cluster, so within 1.0-1.5 h all are hatched.
  2. There are five instars. At hatching the nymph is yellowish-orange, but soon it becomes brown. Each segment of the abdomen is marked, both dorsally and ventrally, with a pair of light spots. The appendages are yellow. The body length is about
  3. 6 mm. During most of this first instar the nymphs cluster tightly around the egg cluster and do not feed. Finally, just before the young insects are about to molt, the nymphs move from the cluster and commence feeding. In the second instar the head and thorax are black, with the abdomen reddish-black. Both the thorax and abdomen are marked with yellowish spots. The appendages are black. The body length is about 3.2 mm. Second instars remain near the egg cluster, and remain aggregated. The third instar is very similar to the second, differing principally in size, and measuring about 3.6 mm long. Third instars disperse away from the egg cluster, but remain aggregated. The fourth instar also may be relatively unchanged in appearance from the preceding instars, differing principally in body length of about 4.2 mm. However, the color of the fourth instar is highly variable, and may instead be greenish; the thorax is light green with black markings, and the abdomen is darker green with salmon shading and white spots. The appendages are brownish, with the tip of the antennae greenish. Unlike the preceding instars, fourth and fifth instars do not aggregate. The fifth instar is also highly variable, the head, thorax and wing pads ranging from light green to almost black. The abdomen tends to be colored light or dark, corresponding to the shade of the thorax, and marked with rose spots dorsally, and whitish spots laterally. The body length of fifth instars is about 10 mm. Mean duration (range) of instars 1-5 is about 4 (3-5), 5 (3-10), 5 (3-9), 8 (6-10), and 10 (7-13) days, respectively. Thus, total nymphal development time is about 32 days, and egg to adult development requires 35-37 days, depending on temperature and suitability of food. The optimal temperature for development is about 30°C.
  4. The adult is generally uniform light-green, both dorsally and ventrally, though the ventral surface is paler. Adults measure about 13-17 mm long and 8 mm wide. The thorax is the widest part of the body,
The Body Parts Stink Bug
Nymph of southern green stink bug, dark form.

and is rounded laterally. Sometimes the adults differ in having yellow or brown on the thorax or scutellum, and the brown color may extend onto the forewings. During the summer months, females begin egg production about 14-20 days after attaining the adult stage. (See color figure 145.)

Southern green stink bug, N. viridula, is easily confused with green stink bug, Acrosternum hilare (Say). However, the two species differ ecologically and morphologically. Acrosternum hilare is usually associated with trees and shrubs, rather than the herbaceous vegetation fed upon by N. viridula. Also, though A. hilare is found widely in North America, it is most abundant in the north. The two species can be differentiated by the shape of the abdominal spine. When viewed from below, A. hilare has a pointed spine protruding forward between the base of the hind legs, whereas in N. viridula the spine is rounded. A key to distinguish stink bugs commonly affecting vegetables is found in Appendix A.

In coastal areas of the south, the adults of southern green stink bug are scarce during the winter months but not all are dormant, a few being found feeding on succulent plants. Even in these relatively warm areas, however, no nymphs are found. Overwintering occurs in sheltered locations, most commonly under bark of trees, but also beneath fallen leaves and in Spanish moss. Considerable winter mortality among southern green stink bug can occur at the northern limits of its range, and winter weather is considered to be an important variable in population abundance. High levels of mortality occur when bugs are exposed to —10 and —5°C for 3 and 55 h, respectively (Elsey, 1993).

Southern green stink bug displays a complex chemical ecology. Nymphs produce a bifunctional phero-mone that functions as an aggregation pheromone at low concentrations and a dispersant at high concentrations. Adult males produce an aggregation pheromone that attracts females, other males, and the parasitoid Trichopoda pennipes (Fabricius) (Diptera: Tachinidae). Presumably the principal function of this chemical is to enhance mate finding. However, there are visual, tactile, and acoustic stimuli that are a necessary prelude to mating (Harris et al., 1982). Finally, stink bugs secrete a defensive chemical that apparently is repellent to predators.

Descriptions and summaries of life history were provided by Jones (1918a) and Drake (1920), the developmental biology was given by Harris and Todd (1980), and a useful review of behavior and ecology was presented by Todd (1989). Information on stink bug culture was provided by Harris and Todd (1981) and Brewer and Jones (1985).

Adult southern green stink bug.

Damage

Southern green stink bug punctures plant tissue with its piercing-sucking mouthparts and removes sap, often feeding at night. Stem, leaf, blossom and fruit tissue may all be attacked, but fruiting structures are preferred and invariably the tissue selected is young and succulent. The feeding site, as it heals, becomes hard and darkened. Seeds may be shriveled, deformed, and shrunken, or may simply bear a dark mark and depression at the feeding site. Fruit may be deformed or dropped from the plant. Under high levels of feeding pressure, young plants and plant shoots may perish. Stink bugs are capable of introducing bacteria and yeasts into plants as they feed. Wounds also allow entry of secondary plant pathogens.

Vegetable crops are easily damaged by southern green stink bug. Studies of tomato fruit attack in Louisiana indicated that small fruit were preferred over large fruit, and green over red fruit (Lye and Story, 1988). There was an inverse linear relationship between bug density and fruit quality; fewer than two bugs on a tomato fruit for one day, or one bug for two days, resulted in decrease in fruit quality (Lye et al., 1988a,b). In corn grown in Louisiana, as few as two bugs per ear of corn during early ear development could result in damage (Negron and Riley, 1987). Cowpea and lima bean were studied in Georgia, and two days of feeding by one bug on a pod significantly reduced pod size and mean seed weight (Nilakhe et al., 1981a,b).

Management

  1. A comprehensive review of stink bug sampling was published by Todd and Herzog (1980), though soybean rather than vegetables is emphasized. Sweep nets and direct visual examination are techniques most useful for stinkbug sampling. Lye and Story (1989) studied southern green stink bug sampling in Louisiana tomatoes. They reported that bugs were moderately aggregated and that young fruit clusters were the most efficient sampling unit. They also developed a sequential sampling protocol.
  2. Insecticides are commonly applied to foliage, especially at blossoming and pod set, to protect susceptible crops from stink bug damage. Systemic insecticides applied to the soil tend to be less effective (Chalfant, 1973a). Insecticide resistance has become a problem in some areas of the world, so steps to minimize development of resistant populations should be followed. Insecticides can interfere with naturally occurring biological control, but research has shown that insecticides with a short residual life have a minimal impact on egg parasitoids (Orr et al., 1989).

Cultural Techniques. Consideration of early season feeding behavior is an important component of management. Cruciferous crops and weeds are potential sources of stink bugs for later legume crops, and should be monitored, treated, or destroyed. Legume cover crops or forage crops are another source of bugs that might invade vegetables, and should be treated similarly.

Farmers and entomologists have long attempted to use early-season crops, or late-season crops planted early, as trap crops to lure stink bugs from the principal crop. Early in the spring or late in the autumn cruciferous plants such as collards, mustard, radish, rape, and turnip are attractive to bugs, whereas late in the spring and during the summer legumes such as bean and cowpea are most attractive. Drake (1920) recommended radish and collards in the spring and rattle-box in the summer to protect tomato. McPherson and Newsom (1984) and Todd and Schumann (1988) reported that early-planted soybean or cowpea could serve as a trap crop for late-planted soybean. Stink bugs will disperse from trap crops, however, so usually they must be treated with insecticide before dispersal occurs in the adult stage.

Plant cultivars resistant to attack by stink bug generally are not available commercially, but genetic sources of resistance have been identified for cowpea (Schalk and Fery, 1986).

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