Nezara viridula (green stink bug)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Notes on Natural Enemies
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Nezara viridula (Linnaeus)
Preferred Common Name
- green stink bug
Other Scientific Names
- Cimex smaragdulus Fabricius
- Cimex torquatus Fabricius
- Cimex viridulus Linnaeus
International Common Names
- English: green shield bug; green vegetable bug; southern green stink bug; tomato and bean bug
- Spanish: chinche hedionda verde; chinche verde de las hortalizas; chinche verde del algodonero (Mexico); maya verde
- French: punaise verte; punaise verte du sud
Local Common Names
- Brazil: fede-fede da soja; percevejo verde
- Dominican Republic: chinche verde del arroz
- Germany: gruene reis-wanze
- Indonesia: kepik ijo; lembing
- Iran: sene bereng (sabs rang); seyn (Iran)
- Israel: hapishpesh hayarok
- Italy: cimice verdastra
- Japan: minami-aokamemusi
- Mexico: cinche verde del algodonero
- Netherlands: groene tabakswants
- Turkey: pis kokulu yesil bocek
- NEZAVI (Nezara viridula)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Arthropoda
- Subphylum: Uniramia
- Class: Insecta
- Order: Hemiptera
- Suborder: Heteroptera
- Family: Pentatomidae
- Genus: Nezara
- Species: Nezara viridula
Notes on Taxonomy and NomenclatureTop of page
Freeman's (1940) revision of the genus Nezara provides an accessible review of the nomenclatural history of the species, which has since remained stable. Todd and Herzog's (1980) review has a key to the stink bugs in North American soyabeans.
Species in the genus have various colour forms. Several such forms have been described, with about 10 in Nezara viridula (Hokkanen, 1986). Three N. viridula (green vegetable bug) forms were originally described as species in their own right, so the names N. viridula var. smaragdula (green), N. viridula var. torquata (yellow) and N. viridula var. aurantiaca (golden) appear in the literature, although they have no formal taxonomic standing (DeWitt and Godfrey, 1972). Other varietal names that have been used are dealt with by Hokkanen (1986). The green variety is the usual colour form of the species. Ironically, Linnaeus' type specimen was a red colour form (Freeman, 1940), which explains why the green bugs are sometimes given only varietal status.
Indications have emerged that more than one species (i.e. cryptic or sibling species) is included under the single name N. viridula (Jeraj and Walter, 1998), but what this means for pest management remains unclear.
DescriptionTop of page
Eggs are deposited in tightly packed, single-layered rafts of about 60 (range of 30-130) eggs (Van den Berg et al., 1995). Each egg is tightly glued against other eggs and to the substrate, with no intervening gaps. Eggs are cream to yellow, slightly elongate, and circular from above. As they develop they become deep yellow, then pinkish, and finally bright orange. The head of the developing embryo becomes visible 3 days after oviposition, as a red crescent.
The antennae of nymphs have four segments. Adults were thought to have five (hence the name Pentatomidae), but recent investigations show that the second antennal segment has a false division (Jeram and Pabst, 1996). Nymphs have no wings, but wing pads are visible on fifth-instar nymphs. Nymphal colour changes progressively in successive instars. On hatching, the nymphs are mostly black. By the fifth instar, a considerable proportion of each is green. The instars can be differentiated from one another by colour and size variation (Kobayashi, 1959).
N. viridula adults are large green shield bugs, approxomately 15 x 8 mm in size. They are uniform apple-green above and a paler shade of green below. The green colour may be replaced by a red-brown. Three small white dots are usually evident on the front edge of the scutellum, where it joins the prothorax.
DistributionTop of page
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 25 Feb 2021
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Congo, Democratic Republic of the||Present|
|Congo, Republic of the||Present|
|São Tomé and Príncipe||Present|
|South Africa||Present, Widespread|
|-Jammu and Kashmir||Present|
|-Irian Jaya||Present, Localized|
|-Peninsular Malaysia||Present, Localized|
|Belgium||Absent, Formerly present|
|Federal Republic of Yugoslavia||Present|
|Antigua and Barbuda||Present|
|British Virgin Islands||Present|
|Saint Kitts and Nevis||Present|
|Saint Vincent and the Grenadines||Present|
|Trinidad and Tobago||Present|
|U.S. Virgin Islands||Present|
|-Maryland||Absent, Formerly present|
|-New York||Absent, Formerly present|
|-Ohio||Absent, Formerly present|
|-Virginia||Absent, Formerly present|
|Australia||Present||Present based on regional distribution.|
|-New South Wales||Present, Widespread|
|-Northern Territory||Present, Localized|
|-South Australia||Present, Few occurrences|
|-Tasmania||Present, Few occurrences|
|-Victoria||Present, Few occurrences|
|Federated States of Micronesia||Present, Widespread|
|New Zealand||Present, Localized|
|Papua New Guinea||Present|
|-Mato Grosso do Sul||Present|
|-Rio de Janeiro||Present|
|-Rio Grande do Sul||Present, Widespread|
Risk of IntroductionTop of page
N. viridula is known to transmit Nematospora spp. (in particular Nematospora coryli in Africa), which causes internal rots of cotton and beans (Ragsdale et al., 1979).
The feeding punctures made by green vegetable bugs provide access for fungal and bacterial infections (Todd and Herzog, 1980; Russin et al., 1988) some of which are toxic to vertebrates, for example, those that invade nut or maize kernels (Stringer et al., 1983; Payne and Wells, 1984). Even if the damage is not outwardly severe, the taste of the product may be badly affected, for example, hazelnuts (Genduso, 1974).
Hosts/Species AffectedTop of page
Although N. viridula is considered highly polyphagous, leguminous hosts are disproportionately represented (Todd and Herzog, 1980; Todd, 1989). Several species of Cruciferae, Poaceae, Malvaceae and Solanaceae are also attacked. Green vegetable bug performance varies significantly across species (Todd, 1989; Panizzi and Slansky, 1991; Velasco and Walter, 1992; Panizzi and Saraiva, 1993). Furthermore, various suitable host species affect nymphs differently from adults (Velasco and Walter, 1992).
Host species are perhaps most usefully treated as reproductive (or nymphal) hosts and/or hosts for adult maintenance. The major reproductive hosts include soyabean (wherever cultivated); wild radish in the USA, South America and Australia (Jones and Sullivan, 1982; Panizzi and Saraiva, 1993; Velasco et al., 1995); variegated thistles (Silybum marianum) in Australia (Clarke and Walter, 1993a) and rice (Kiritani et al., 1965).
Most other hosts support relatively little reproduction. Polyphagy therefore seems to be a rather specific adaptation to sustain the adults through periods when reproductive hosts are not available (Velasco and Walter, 1992). In some areas (for example, the southern coastal plain of the USA), N. viridula populations increase on alternative hosts (including non-cultivated ones) prior to invading soyabeans and transgenic cotton in late summer (Todd and Herzog, 1980; Jones and Sullivan, 1982; Turnipseed and Greene, 1996). In other areas (for example, south-east Queensland), the majority of N. viridula entering soyabeans are those that survived summer periods during which reproductive host plant species are not readily available (Velasco and Walter, 1992). For information on hosts in Brazil and Argentina, see Panizzi and Slansky (1991), Panizzi and Rossi (1991), Panizzi and Saraiva (1993) and Antonino (1996).
Different host species sustain the spring generation of offspring in different localities. In south-east Queensland the nymphs develop mainly on wild radishes and variegated thistles (Clarke and Walter, 1993a; Velasco et al., 1995). In spring, Japanese N. viridula adults feed on rape, radishes, wheat and barley before moving briefly onto potatoes to oviposit, and then onto rice (Kiritani et al., 1965). Those on the south-eastern coastal plain of the USA develop on wild radishes and wheat (South Carolina: Jones and Sullivan, 1982) or mustard, turnips, beets and red clover (Newsom et al., 1980). Similarly, subsequent generations feed on a different range of species in different localities.
Interpretations of the host relationships of N. viridula warrant further testing. The situation is, however, confused by two observations on different populations of N. viridula. Firstly, different populations of N. viridula may have host relationships in one area that are significantly different from those of other populations, sometimes in the same general area (Todd and Herzog, 1980; Panizzi and Meneguim, 1989; Panizzi and Slansky, 1991). Whether such differences are imposed by host plant availability in the different localities needs investigation. Secondly, the bugs themselves may be genetically different among localities (See Biology and Ecology.)
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page
SymptomsTop of page
In general, their piercing and sucking mouthparts puncture the plant tissues and form minute, hard, brownish or blackish spots. Feeding retards the growth of immature fruits, which the bugs prefer to over-ripe fruit, and distorts them, causing, for example, catfacing of peaches (Johnson et al., 1985) or premature drop. Flower drop in ornamental or cut flowers is sometimes a problem (Gough and Hamacek, 1989; Parrini and Rumine, 1989).
The feeding punctures also provide access for fungal and bacterial infections (Todd and Herzog, 1980; Russin et al., 1988), some of which are toxic to vertebrates, for example, those that invade nut or maize kernels (Stringer et al., 1983; Payne and Wells, 1984). Some of the pathogens seem to be responsible for the fruit drop that follows feeding, for example, citrus (Ali et al., 1978). Even if the damage is not outwardly severe, the taste of the product may be badly affected such as hazelnuts (Genduso, 1974).
Green vegetable bug feeding on pecans causes black pit, in which the kernel goes black and the fruit abscises. After shell hardening in both pecans and macadamias, bug feeding causes kernel spot which is a localized lesion in the kernel surface that may extend into the embryo (Dutcher and Todd, 1983).
Developing soyabean seeds from which N. viridula have fed usually do not grow to full size and are shrivelled and deformed. Older green seeds suffer only a black mark in a depression (Todd and Herzog, 1980). Seeds with only slight to moderate N. viridula damage may germinate at significantly lower rates than undamaged seeds (Berger et al., 1990).
Rice grains affected by N. viridula feeding do not fill completely. They shrivel and become covered with brownish spots and fungal growth (Lim, 1970; Ito, 1986).
Feeding by N. viridula on young tomatoes induces early maturity and reduces fruit size and weight (Lye et al., 1988). A reddish-yellow spot appears where N. viridula inserts its sucking tube. When cut the fruit is full of lumps and has no flavour (Drake, 1920).
List of Symptoms/SignsTop of page
|Fruit / abnormal shape|
|Fruit / external feeding|
|Fruit / lesions: black or brown|
|Fruit / premature drop|
|Growing point / external feeding|
|Inflorescence / external feeding|
|Inflorescence / fall or shedding|
|Leaves / honeydew or sooty mould|
|Seeds / external feeding|
|Stems / external feeding|
Biology and EcologyTop of page
N. viridula has been widely investigated over a protracted period. The life cycle, ecology and behaviour of N. viridula have been reviewed (Todd and Herzog, 1980; Panizzi and Slansky, 1985; Waterhouse and Norris, 1987; Todd, 1989). N. viridula is classed by Todd (1989), as "... one of the most important pentatomid insect pests in the world ... It is cosmopolitan and highly polyphagous on many important food and fiber crops".
The ecology of N. viridula varies with locality, but the scale at which such variation manifests itself remains unclear. Interpretation of N. viridula ecology in any particular area requires considerably more information about the specific use made by both nymphs and adults of the various plant species available.
The life cycle of green vegetable bugs is mostly multivoltine, with the extent of voltinism related to local differences in climate and the availability of host plants suitable for reproduction (Todd, 1989; Velasco and Walter, 1992; Cividanes and Parra, 1994a; Velasco et al., 1995; Chang and Chen, 1997).
Most green vegetable bugs undergo winter diapause, invariably in the adult stage, but in southern Brazil they continue reproducing on alternative host plants (Panizzi and Meneguim, 1989). Overwintering individuals generally, but not invariably, assume a russet colour (Seymour and Bowman, 1994). During warm periods they may emerge from their hiding places under bark, in litter, in thick vegetation, or behind panels of buildings, to feed (Kiritani et al., 1966; Todd and Herzog, 1980), which enhances survival. Cold tolerance has not been extensively investigated, and would be of differential importance for bugs at different latitudes. The survival of green vegetable bugs in different geographical localities, and the factors that influence their survival, have been described by Todd (1989) and Elsey (1993).
Adults leave their hibernation sites permanently in spring, start feeding, mainly nocturnally (Shearer and Jones, 1996b) and soon mate and oviposit. Eggs are deposited in the upper canopy of the herbaceous host plants, mostly under leaves or fruiting structures. They may take as long as 2-3 weeks to hatch in spring and autumn, but as few as 5 days in summer.
The first-instar nymphs do not feed, and form tight clusters at their natal site. Second- and third-instar nymphs also cluster, perhaps for protection, but they disperse if disturbed. Fourth- and fifth-instar nymphs do not aggregate. These older nymphs, along with adult green vegetable bugs, bask on the outer surface of the canopy or on the sunny side of those fruiting structures that emerge from the canopy. In the middle of the day, most bugs retreat into the canopy or to the shaded side of fruiting structures.
Nymphs in the fifth instar are sensitive to day length, which (in combination with temperature) determines entry into adult diapause (Todd, 1989). The developmental rate of nymphs is dictated by temperature and nutritional quality. Some studies indicate optimal temperatures are about 30°C, when the nymphal stage lasts about 23 days, but almost 8 weeks is needed to complete this stage at 20°C (Todd, 1989). A daytime temperature of 30°C for 14 h and a 10 h reduction in night-time temperature to 20°C resulted in an intermediate nymphal duration of 5 weeks in Australian bugs (Velasco and Walter, 1993a).
On primary host plant species (for example, soyabean), nymphs may develop up to twice as fast as on other species (for example, clover) at 27±5°C (Velasco and Walter, 1992). Brazilian nymphs, in contrast, do not survive well at 30°C, and oviposition by Brazilian bugs was greatest at 20°C, which led Cividanes and Parra (1994b) to conclude the species is better adapted to lower temperatures. Harris and Todd (1980a) discussed possible causes of such differences among studies of N. viridula.
The performance of N. viridula on some other host plants, and on various combination diets, has become available (Velasco and Walter, 1993b; Koymen and Karsavuran, 1995; Panizzi et al., 1996; Roychoudhury and Joshi, 1996; Shearer and Jones, 1996a; Panizzi and Mourao, 1999). Tests on macadamia demonstrate that N. viridula may be a pest on a crop, despite that crop species being a poor host and not supporting successful development of the nymphs (Shearer and Jones, 1996a) and though a host may be good for reproductive development of adult females, it may be relatively poor for nymphal development, as has been documented for Brazilian bugs on Japanese privet (Panizzi et al., 1996; Panizzi and Mourao, 1999).
Populations of N. viridula may have host relationships in one area that are significantly different from those of other populations, sometimes in the same general area (Todd and Herzog, 1980; Panizzi and Meneguim, 1989; Panizzi and Slansky, 1991). It is not known whether these are genetically different sibling species of N. viridula or whether these differences are imposed by host plant availability. Until recently, differences between populations in sound production and pheromone composition have been assumed to be produced by local adaptation within that locality. However, an alternative to that view has been suggested; the taxon N. viridula may contain unrecognized sibling species (Ryan et al., 1996) and recent tests support this interpretation (Jeraj and Walter, 1998).
That sibling species and not local adaptation may be involved is supported by the considerable migratory potential of the bugs, which means that the potential for gene flow among localities is thus considerable. In parts of Africa, they migrate in large groups under the influence of the Inter-Tropical Front (Bowden, 1973). Anecdotal evidence in Australia suggests that mass migration to overwintering sites may take place (Gu and Walter, 1989). Females in Japan reputedly fly up to a kilometre per day when moving between feeding and oviposition sites (Kiritani et al., 1965). Records of extended flights of hundreds of kilometres by individuals have also been documented (Hokkanen, 1986; Gu and Walter, 1989; Aldrich, 1990).
Nymphs have dorsal abdominal glands that secrete n-tridecane, which functions in nymphal aggregation and, at high concentrations, in dispersal (Lucchi and Solinas, 1990). Adults secrete n-tridecane from their paired metathoracic glands, as well as some (E)-2-hexenal and (E)-2-hexenyl acetate, which are adult alarm pheromones. These three compunds play a defensive role against certain potential predators including fire ants (Lucchi and Solinas, 1990; Pavis et al., 1994). Nymphs in aggregations suffer less predation than isolated nymphs (Todd, 1989). Another adult metathoracic gland compound, (E)-2-decenal, also attracts female egg parasitoids (Trissolcus basalis) (Mattiacci et al., 1993).
Questions remain, however, about the sex pheromones and the structures that secrete them. The pheromone gland is not discrete, but made up of numerous minute glands in the ventral subcuticular tissues (Lucchi, 1994). Several compounds are secreted by sexually active males (Aldrich et al., 1989; Borges, 1995). Evidence conflicts over their precise function. Field tests show that they attract adults of both sexes as well as fifth-instar nymphs and are thus said to be aggregation pheromones (Harris and Todd, 1980b).
In laboratory experiments, only sexually mature adult males are attracted by the compounds (Mitchell and Mau, 1971; Brezot et al., 1993). Most attention has been given to the cis- and trans-forms of bisabolene epoxide (Brezot et al., 1994) because bugs from different parts of the world were recorded having different ratios of these enantiomers (Aldrich et al., 1989, 1993). Two lines of evidence question this interpretation. Within-population variation in ratios is as great as that recorded among populations (Ryan et al., 1995) and different ratios of the cis- and trans-epoxides did not affect the attraction of females to males (Brezot et al., 1994).
The sexes communicate by means of substrate-borne vibrations in the form of a duet (Ota and Cokl, 1991; Ryan et al., 1996), which takes place after they arrive on a plant and have to locate one another (Ota and Cokl, 1991). Different strains have been documented (Harris et al., 1982; Kon et al., 1988) but recent research suggests that sibling species are involved. At least two species are known in the taxon N. viridula; bugs in Australia have significantly different songs and song alternation sequences from Slovenian bugs, and bugs from the two areas do not communicate effectively with one another even in confined spaces (Jeraj and Walter, 1998).
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Anthicus cervinus||USA; Louisiana||soyabeans|
|Bacillus thuringiensis kurstaki||Pathogen|
|Conocephalus fasciatus||Predator||USA; Louisiana||soyabeans|
|Geocoris punctipes||Predator||USA; Louisiana||soyabeans|
|Geocoris uliginosus||Predator||USA; Louisiana||soyabeans|
|Largus succinctus||Predator||USA; Louisiana||soyabeans|
|Nabis capsiformis||Predator||USA; Louisiana||soyabeans|
|Nabis roseipennis||Predator||USA; Louisiana||soyabeans|
|Oecophylla smaragdina||Predator||China; Fujian||Citrus|
|Ooencyrtus submetallicus||Parasite||Eggs||Brazil; Parana; Hawaii; Louisiana||maize; soyabeans|
|Orchelimum nigripes||Predator||USA; Louisiana||soyabeans|
|Phidippus audax||Predator||USA; Louisiana||soyabeans|
|Solenopsis invicta||Predator||USA; Louisiana||soyabeans|
|Telenomus mormideae||Parasite||Brazil; Parana; Brazil; Rio Grande do Sul||soyabeans|
|Theridion albidum||Predator||USA; Louisiana||soyabeans|
|Trichopoda giacomellii||Parasite||Adults/Nymphs||Argentina; Australia||soyabeans|
|Trichopoda pennipes||Parasite||Adults/Nymphs||Antigua; Australia; Fiji; Hawaii; New Zealand; Papua New Guinea||cotton; fruits; maize; ornamental plants|
|Trichopoda pilipes||Parasite||Adults/Nymphs||Antigua; Hawaii; Papua New Guinea; South Africa; Western Australia||cotton; maize; ornamental plants; vegetables|
|Trissolcus basalis||Parasite||Eggs||Argentina; Australia; Brazil; Parana; Brazil; Rio Grande do Sul; Cook Islands; Fiji; Guam; Hawaii; Italy; Kiribati; Louisiana; Micronesia; New Caledonia; New Zealand; Papua New Guinea; Pitcairn; South Africa; Taiwan; USA; Louisiana; Western Australia; Western Samoa; Zimbabwe; South Carolina||fruits; maize; ornamental plants; soyabeans; tobacco; vegetables|
|Trissolcus mitsukurii||Parasite||Eggs||Brazil; Hawaii; Montserrat; St Kitts Nevis||cotton; maize; soyabeans|
|Trissolcus scuticarinatus||Parasite||Brazil; Parana||soyabeans|
|Xenoencyrtus niger||Parasite||Antigua; Hawaii||cotton; maize|
Notes on Natural EnemiesTop of page
Several egg parasitoids have been recorded parasitizing N. viridula. Some have been introduced to other countries, but establishment and rates of parasitism have been low (Bennett, 1990). Relatively few parasitoids attack N. viridula regularly and at relatively high rates. Trissolcus basalis does so in several parts of the world (for example, Brazilian and Argentinian soyabeans: Foerster and de Queiroz, 1990; Liljesthröm and Camean, 1992; Corrêa-Ferreira and Moscardi, 1995). (E)-2-decenal, a compound secreted by the adult metathoracic gland of N. viridulis, attracts the female T. basalis (Mattiacci et al., 1993). Psix striaticeps in Togo also attacks N. viridulis at relatively high rates (Poutouli, 1995).
Other egg parasitoids are more sporadic or less abundant (or both). For example, Telenomus podisi accounts for only 2% of the parasitism of N. viridula in Brazil, even though parasitism rates overall reached 62% (Corrêa-Ferreira and Moscardi, 1995). Even in the laboratory, parasitism rates by this species are relatively low on N. viridula (Pacheco and Corrêa-Ferreira, 1998). Other bugs are attacked at much higher rates by T. podisi (and also T. mormideae), so these parasitoids are not primarily adapted to N. viridula.
Various other egg parasitoid species, such as Ooencyrtus johnsoni, O. californicus, Trissolcus brochymenae and T. urichi, also parasitize N. viridula only at low levels and erratically (Moreira and Becker, 1986; Hoffmann et al., 1991; Corrêa-Ferreira and Moscardi, 1995). Jones (1988) categorizes the host relationship with regard to N. viridula of most parasitoids recorded from the bug; most species have only been rarely recorded or are incidental parasitoids of N. viridula. Some of the parasitoid species have only recently been recorded and their status in relation to N. viridula awaits further clarification.
Flies in the family Tachinidae also attack the nymphs and adults, but few species are involved. The species most important in relation to N. viridula are mainly in the genus Trichopoda. A few species have been used in biological control or have been investigated for this purpose, for example, the recent introduction of T. giacomellii [Eutrichopodopsis nitens] from Argentina to Australia for release (Liljesthröm, 1994; Coombs, 1997) and the fortuitous establishment of T. pennipes in Italy (Colazza et al., 1996).
Rates of parasitism by T. giacomellii may vary across different host plants of N. viridula (Panizzi, 1988; La Porta, 1990). Despite reaching peaks as high as 80 or 100%, parasitism rates are usually lower than this (La Porta and de Crouzel, 1984; Corrêa-Ferreira, 1984; Panizzi, 1988; Liljesthröm and Bernstein, 1990; La Porta, 1990; Jones et al. 1996; Panizzi and Oliveira, 1999). Another aspect of Trichopoda parasitism is the proportionately greater parasitism rate of adult males of N. viridula (Corrêa-Ferreira, 1984; Menezes et al., 1985; La Porta, 1990; McLain et al., 1990; Salles, 1991) perhaps because the flies home in on the sex pheromone released by N. viridula males (Aldrich et al., 1989). Indeed, the risk of females being parasitized (by T. pennipes) derived primarily from their association with males during mating (McLain et al., 1990). The effect of parasitism by the tachinid on survival and reproductive output of bugs has been extensively quantified (Harris and Todd, 1982; Coombs and Khan, 1998b).
Rearing methods for T. pennipes have been described by Gianguiliani and Farinelli (1995) and adult food (Coombs, 1997), temperature requirements (Liljesthrom, 1996a, b) and host discrimination (Liljesthrom, 1996c) have been investigated. Various tachinid parasitoids use the sex pheromone to locate potential hosts, i.e. as kairomones (Aldrich et al., 1989). Patents have been taken out on these sesquiterpene epoxides and on the preparation process (Aldrich et al., 1990).
A considerable diversity of predators has been recorded attacking N. viridula in various stages of its development (Drake, 1920; Kiritani and Hokyo, 1962; Stam et al., 1987; Van den Berg et al., 1995) but because of the nature of predation the number of observations is quite low. Virtually all of these predators are generalists, or are suspected of being so, but their impact (alone or in combination) has not been convincingly determined. See Todd (1989) and Waterhouse (1998) for information and a discussion of general predators.
There are increasing claims that ants have a strong impact on N. viridula eggs and nymphs, both in orchards (Yang, 1984; Seymour and Sands, 1993; Jones, 1995) and in soyabean fields (Krispyn and Todd, 1982; van den Berg et al., 1995). The thoughtful manipulation of ant populations could contribute considerably to achieving acceptable levels of biological control. Spiders may also contribute significantly to reducing N. viridula populations, but the data are not convincing (Kiritani and Hokyo, 1962).
Other Natural Enemies
To date, relatively few studies of N. viridula pathogens have been published, and no product has been developed for field use. For information on pathogens isolated from field-collected N. viridula, see Singh et al. (1991) on fungi, Williamson and von Wechmar (1992, 1995) and Nakashima et al. (1998) on viruses, and Bhatnagar et al. (1985) on nematodes. The virulence against N. viridula of several entomogenous fungi (for example, Beauveria bassiana, Metarhizium and Paecilomyces spp.) derived from other insects, has been investigated in the laboratory (Leite et al., 1987; Shimaxu et al., 1994; Sosa et al. 1997). However, field trials show little promise (Sosa-Gomez and Moscardi, 1998).
For further information on natural enemies of N. viridula, see Waterhouse (1998) and Jones et al. (1996).
ImpactTop of page
N. viridula is highly polyphagous, although leguminous plants are preferred. In the absence of control measures, it is a major pest of soyabeans, macadamia, pecans and beans; and often an important pest of a wide range of grain, fruit, and vegetable crops. N. viridula is an economic pest in most areas where it occurs, especially in the southern USA, Central and South America, the Mediterranean, the Middle East, Africa, Malaysia, the Philippines, Indonesia, Japan, and the Pacific Islands. It often occurs on a crop as one component, although frequently the most damaging, of a stink bug (pentatomid) complex.
Direct feeding is the main cause of yield losses. Stylet penetration and the injection of saliva damage plant tissue, causing blemishes, discoloration, and malformation; while sucking removes plant nutrient resources resulting in retarded growth. Blemishes reduce quality and marketability of many crops. Feeding contributes to reduced seed number and weight, and premature seed and fruit drop. Stylet sheaths can be counted as an indicator of feeding activity on many crops, and this can often be correlated with yield loss. All plant parts are fed on, but the preference is for growing shoots and developing fruit and seeds.
N. viridula is known to carry spores of fungal diseases from plant to plant, and can also transfer plant pathogens mechanically during feeding (Kaiser and Vakili, 1978; Waterhouse and Norris, 1987). It transmits spores of fungal species of Nematospora which cause internal rots of cotton, soyabeans, tomato, citrus, beans (Phaseolus vulgaris) and other crops. In Brazil, for example, it is reported to transmit Nematospora coryli, the causal agent of yeast-spot disease in soyabeans (Corso et al., 1975).
In soyabean, the stink bug complex includes N. viridula, and species of Piezodorus, Acrosternum, Euschistus and Riportus. The species composition varies with locality. A range of pests other than stink bugs can also be associated with N. viridula in crops (Waterhouse and Norris, 1987). Stink bugs reduce seed yield, often expressed as 1000-seed weight, increase the proportion of seedless pods, and decrease germinability of seed (Miller et al., 1977; Waterhouse and Norris, 1987). Pods punctured during early endosperm formation are largely drained of their contents. The main cause of empty pods in South America is usually attack by N. viridula (Vicentini and Jimenez, 1977; Erejomovich, 1980). On infested plants, seed biomass can decrease considerably, although plants can show compensatory reactions to feeding at the early pod growing stage (Suzuki et al., 1991). In one study, damage-free seeds compensated for damaged seeds by exhibiting mean increases in weight of as much as 43.8% (Russin et al., 1987).
In practically all of the soyabean-growing regions of Brazil, the stink bug complex, in combination with the velvetbean caterpillar (Anticarsia gemmatalis), accounted for over 90% of the insecticides applied (Moscardi, 1993). Early maturing genotypes showed lower yields due to pentatomid damage in a study of host-plant resistance in Brazil (Gazzoni and Malaguido, 1996). In one experiment with Brazilian cultivars, a tolerant line (IAC100) gave the highest yield (2.7 and 3.1 t/ha with and without insecticide, respectively), the lowest percentage weight of totally deformed seeds, and the lowest foliar retention index (Fernandes et al., 1994). Heavy feeding damage can cause the retention of foliage, a condition bought on by the failure of seeds to develop properly (Todd and Herzog, 1980).
In the USA, N. viridula can cause considerable yield loss. During the early 1970s, N. viridula reduced soyabean yields by around 10% in South Carolina, which equalled the combined losses due to all other soyabean pests (Jones and Sullivan, 1982). Stink bugs have also caused significant quality and yield losses annually in Georgia, Florida, and Louisiana. Growers in Georgia, for example, lose around US$13 million annually (McPherson et al., 1995). Significant correlations occurred in Georgia for stink bug population peaks with percentage kernel damage, yield reductions and 100-seed weight reductions (McPherson, 1996). Studies of natural infestations in Louisiana showed that pentatomids fed preferentially on seeds in the upper halves of plants until high infestation levels forced them to feed lower; while even low infestation levels (1.5 bugs per metre of row) impacted seed weight (Russin et al., 1987). In laboratory studies, feeding punctures were more numerous on the proximal seeds of soyabean pods (Panizzi et al., 1995).
The extension of soyabean cultivation in central Italy has resulted in frequent heavy attack by N. viridula, with damage consisting of seed weight loss, altered seed composition, and reduced germinability (Colazza et al., 1986). In one survey, the mean yield loss was 17.6%, the oil content fell to 17.8% and the protein content rose in infested plants, while the rate of germination varied from 80% in resistant soyabean strains to 5% in susceptible ones (Colazza et al., 1985). N. viridula has also been recorded as a pest in France (Le Page, 1996).
In soyabean in Indonesia, high infestations of pentatomids (18-20 per plant) caused between 19 and 39% pod and seed damage (Supriyatin, 1992). A stink bug complex damaged soyabeans in Kagoshima Prefecture, Japan, with N. viridula causing concentrated attacks on the late season crop (Setokuchi et al., 1986).
In Australia, N. viridula can cause serious losses in soyabean (Passlow and Waite, 1971). In field experiments in Queensland, with caged soyabean plants infested with N. viridula, reduced seed yield and oil content occurred during pod fill, but not during pod elongation or pod ripening. Densities as high as 16 adults/m of row did not reduce yield at the late pod ripening stage (Brier and Rogers, 1991). That infestations do not reduce yield loss during the pod-ripening stage has been shown previously, but the situation regarding the pod elongation stage is less clear, with some evidence suggesting yield is lost and other results suggesting the opposite (Brier and Rogers, 1991).
Cowpeas (Vigna unguiculata) can also suffer significant losses due to N. viridula. In screen-cage field tests in the southern USA, for example, initial infestations of cowpeas at early bloom with 3 adults/plant resulted in 100% pod damage, 99% average rate of seed abortion, and 100% loss in total seed yield (Schalk and Fery, 1982). Densities of 12 insects/row metre caused significant yield loss in another US study (Nilakhe et al., 1981).
Macadamias and Pecan
Damage by N. viridula to macadamia (Macadamia integrifolia) can be considerable. Yield loss varies with cultivar. In one study in Hawaii, USA, with seven cultivars of smooth-shell macadamia, two cultivars had 86 and 75% of their kernels damaged by N. viridula in a single month (September 1990), while another (Makai) had a maximum of 5.5% damaged during the entire 10 months in which the orchard was sampled (Jones and Caprio, 1992). Feeding by N. viridula resulted in a significant increase in macadamia nut abortion rates in smaller nuts (10-28 mm diameter) but not in full-size nuts. Studies also showed that, for full-size nuts, damage could occur both in the tree canopy and on the ground, generally within 1 week of nut drop (Jones and Caprio, 1994). Effective insecticidal control of N. viridula in a field trial in macadamia in South Africa reduced the incidence of damaged nuts from 29 to 10% (de Villiers and du Toit, 1984).
In Georgia, USA, the average estimated loss of pecans (Carya illinoinensis), at 1979 US$ values, to sucking bug kernel damage was US$216,000 per year (Dutcher and Todd, 1983). When caged on pecan before shell-hardening in Georgia, N. viridula caused between 34 and 53% fruit drop, while adults feeding on pecan kernels ingested, on average, 14 calories per feeding site (Dutcher and Todd, 1983). In a survey in South Africa, N. viridula accounted for only 0.4% of the 982 specimens collected in pecan orchards (Joubert and Neethling, 1994).
In sorghum, the greatest yield reductions attributed to N. viridula take place during early development, from the milk stage of panicle development to maturity. Direct feeding on the grain accounts for most yield loss (Hall and Teetes, 1982a, 1982b). Field experiments in Louisiana, USA, on wheat, showed that feeding by N. viridula, at both the milk and soft dough stages, decreased germination, kernel weight and baking quality; although damaging levels of bugs are rare, at least in Louisiana (Viator et al., 1983). Similarly, in Pakistan, N. viridula causes only occasional economic damage to wheat (Anwar-Cheema et al., 1973).
In Orissa, India, grain damage to rice in paddy fields caused by three stink bug species including N. viridula was between 3 and 15% in the dry season, and 3 and 12% in the wet season (Gupta et al., 1993). Populations of pentatomids greater than economic threshold levels were found in 50% of the main rice crop and 100% of the ratoon crop in southern Florida, USA (Jones and Cherry, 1986). Serious outbreaks of N. viridula occurred on rice growing in several localities in Peninsular Malaysia in 1968-69 (Lim, 1970).
In field experiments in Louisiana, USA, N. viridula feeding on maize (Zea mays) caused significant reductions in ear weight and ear length, with two adults or more per plant. Feeding damage was most intense in younger plants. Yield reductions were mainly attributed to total ear loss, rather than to reductions in kernel weight (Negron and Riley, 1987). N. viridula is a superficial pest of maize in Brazil (Cruz et al., 1999).
Fruit and Vegetables
Feeding on young tomatoes by N. viridula induced early maturity and reduced fruit size and weight, as demonstrated in a study in Louisiana, USA (Lye et al., 1988). Green fruit were preferred to red fruit (Lye and Story, 1988). Older tomatoes that are even lightly attacked are unmarketable (Waterhouse and Norris, 1987). N. viridula is generally far less damaging to potato and other root crops; for example, being only a minor pest of potato in Brazil (Barbosa et al., 1983).
N. viridula can occur sporadically in large numbers in orchards of granadilla in South Africa. In experiments with cages of 2 bugs/cage around parts of purple granadilla (Passiflora edulis), flower loss, along with internal and external damage of the fruit, occurred (Froneman and Crause, 1989). On peaches (Prunus persica), N. viridula and other stink bugs feed on rapidly developing young fruit, causing fruit to be scarred and malformed, a condition known as 'catfacing' (Johnson et al., 1985).
A stink bug complex in South Africa caused significant losses in avocado (Persea americana) orchards. Before flowering and until the end of December, 10 or more bugs per tree are potentially harmful. From January until about 14 days before harvest, 20 or more bugs per tree led to large scale fruit damage (van den Berg et al., 1999). In a previous report, only 1.8% of avocados reaching the packing house in South Africa were rejected because of N. viridula feeding damage (Dennill and Erasmus, 1992). A heavy and damaging outbreak of N. viridula was reported on Citrus in Egypt (Attiah et al., 1974).
A linear relationship was observed between stink bug infestation of green gram (Vigna radiata) and seed loss in the field in Assam, India, with N. viridula being one of the most damaging pests (Hussain and Saharia, 1994).
Transgenic Cotton and Castor
The switch to transgenic cotton (Gossypium hirsutum) in the USA has seen N. viridula and other stink bugs invade this crop, due to reduced insecticide spraying. Damage to bolls in untreated Bt transgenic cotton in South Carolina in 1995, for example, ranged from 15 to 71%, resulting primarily from pentatomid damage. The yield losses from pentatomids were associated with the abundance of alternative hosts near the study sites (Greene and Turnipseed, 1996; Turnipseed and Greene, 1996). N. viridula is responsible for significant boll damage, to both lint and seeds, by external marking and internal feeding that leads to wart-like growth complexes (Bundy et al., 1999). N. viridula and other stink bugs damage young bolls in mid to late season, and a study in South Carolina concluded that treatment was necessary if more than 20% of bolls are penetrated during this time (Greene et al., 1997). In field-cage studies, boll damage by 5th instar N. viridula, the most damaging stage, decreased as boll age increased from 4 to 18 days from white bloom; although damage to 18-day-old and above bolls was negligible. Exposure of 13-day-old bolls singly to 5th instars for 7 days reduced boll yield by 59% compared with unexposed bolls (Greene et al., 1999).
N. viridula is a pest of castor (Ricinus communis) in the tropics, and a potential pest of this crop in recently planted orchards in Europe. In field plots in France and Italy that were artificially infested, typical damage was observed, with increased capsule shedding and, consequently, a decreased number of capsules and seeds, and reduced seed yield. Shedding and seed yield were not affected if infestations occurred at later stages (Conti et al., 1997).
Detection and InspectionTop of page
The various sampling methods and their relative merits are discussed at length by Todd and Herzog (1980). Simple methods remain the most reliable, including sweep-netting and ground cloth methods (for example, Greene et al., 1997, 1998). Searching for eggs and damage is labour intensive and unreliable because they are not readily detected. Under the leaves should be searched especially. Nath and Dutta (1994) studied the optimum sample size in green gram.
In some low-growing crops, such as tomatoes, visual estimates of density are possible (Lye and Story, 1989), whereas in other low-growing crops such as soyabean, rice and cotton, green vegetable bugs are most readily detected by visual inspection, sweep-netting or shaking the insects onto a ground cloth. Kogan and Pitre (1980) give full details on these (and other) methods to sample arthropods from soyabean, including equipment construction and data conversion. Sweep-netting probably gives the best coverage for time spent in low-growing crops (Rudd and Jensen, 1977) and is useful if the bugs are patchily distributed.
Visual inspection is likely to be most efficient if it is timed to coincide with the basking behaviour of the bugs early in the day. The older nymphs, along with adult bugs, bask on the outer surface of the canopy or on the sunny side of the fruiting structures that emerge from the canopy. In the middle of the day, most bugs retreat into the canopy or to the shaded side of fruiting structures (Lockwood and Story, 1986).
General host plant surveys present serious problems because comparison of bug densities across plant species is required, and different species can rarely be sampled in a standard way. See Jones and Sullivan (1982) and Velasco et al. (1995) for examples of how this problem has been overcome.
Similarities to Other Species/ConditionsTop of page
N. viridula and the closely related N. antennata, which occurs sympatrically in Asia, can be differentiated from one another on the basis of colour and size variation (Kobayashi, 1959). The two species were distinguished one from the other by Freeman (1940) on the basis that N. attenata had black bands on antennal segements 3, 4 and 5 and prominent prothoracic angles, both of which N. viridula did not have. Differences in mating behaviour between N. antennata and N. viridula have been described by Kon et al. (1988) and Kon and Numata (1994).
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Participation in soyabean IPM programmes in Georgia, USA, have been low, probably because of the risk involved (Szmedra et al., 1990). In contrast, a soyabean IPM programme developed in Brazil is seen as a 'spectacular success story of IPM implementation for a major crop over a wide area', and has returned substantial economic, ecological and social benefits (Moscardi, 1993). The N. viridula component involves release of Trissolcus basalis (at least in the state of Paraná), which are produced centrally. See section on Egg Parasitoids for more information on these releases. Insecticides are applied at half the recommended doses with 0.5% NaCl added to the spray tank (Corso, 1993).
In the southern states of Brazil, early-maturing soyabean varieties are planted to escape N. viridula attack. Such varieties have also been used successfully as trap crops to concentrate bugs before the true crop matures, when they are treated chemically or with mass-released T. basalis. But this tactic is still at the experimental stage in relation to IPM in Brazil. Biological control efforts against N. viridula are likely to be enhanced if carried out in association with selective plantings of species that encourage both N. viridula and its parasitoids (Bennett, 1990). Different tillage treatments for soyabean plantings did not influence N. viridula population dynamics, so the tilling operations can be selected for predator conservation (Funderburk et al., 1990).
The possible use of neem seed extract (azadirachtin) in IPM programmes in pecans has been investigated by Seymour et al. (1995). This plant-derived compound seems to reduce feeding by the bugs even at low concentrations, so may well prove useful.
Cultural Control and Sanitary Methods
Crop sanitation has been advised (Waterhouse and Norris, 1987).
Limited use has been made of trap crops to reduce the impact of N. viridula on soyabean, but the approach has good potential (Drake, 1920; Todd and Herzog 1980; Todd, 1989). Early-maturing varieties can be used as trap crops to protect the later maturing, true crop, but insecticides should be applied to the trap crop before the main crop reaches pod set (Kobayashi and Cosenza, 1987; Todd and Schumann, 1988). Adjustment of the planting date of crops, as well as row width (Hussain and Saharia, 1993), allows a degree of manipulation of N. viridula numbers (Rizk et al., 1990; McPherson and Bondari, 1991). Sesbania rostrata has been tested as a trap crop for soybean in Indonesia (Naito, 1996). Intercropping of soyabean with other crops has been tested. The most promising combinations of crops are non-related ones (Das and Dutta, 1996).
In orchards, planting species more attractive to N. viridula than the crop itself shows some promise (Umana et al., 1993). Weed control is thought to reduce catfacing damage to peaches (Killian and Meyer, 1984) but does not reduce damage in soyabean (Altieri et al., 1981). The recommendation for transgenic cotton in the USA is to plant early and avoid areas where alternative hosts are growing (Turnipseed and Greene, 1996).
Todd (1989) lists three further approaches to cultural control of N. viridula that offer substantial benefit:
- use of alternatives crops that are less attractive than soyabean;
- attraction of N. viridula bugs to localized areas of highly attractive hosts late in the soyabean season, with their subsequent eradication with insecticides;
- elimination of preferred overwintering sites.
Soyabean germplasm with resistance to N. viridula has been identified, but little progress has been made in the development of agronomically acceptable resistant cultivars or in quantifying the impact of resistant varieties on N. viridula abundance and pest status (Todd, 1989). In Brazil, a variety (IAC-100) resistant to stink bugs in general has been released to growers, and transfer of resistant genes into otherwise more suitable genotypes shows promise (Moscardi, 1993). Soyabean genotypes with resistance to N. viridula may influence parasitism rates negatively, at least to some extent, and warrants consideration (Orr et al., 1985). Recent emphasis has been on the local testing of different soyabean genotypes for resistance in Brazil (Lourencao et al., 1997, 1999), the USA and Thailand (Suwanpornskul and Khadkao, 1996). Correlated measures have also been sought to facilitate selection for resistance (Lopes et al., 1997).
Other crops are also being tested such as spine gourd and summer green gram in India (Sarma and Dutta, 1997; Shaw et al., 1998). Different pecan and macadamia cultivars show differential susceptibility to green vegetable bug attack, which in turn is related to shell thickness of the nuts (Dutcher and Todd, 1983; Jones and Caprio, 1992).
Fourth- and fifth-stage N. viridula nymphs and adults bask outside the plant canopy until about mid-day, so application of insecticides is most effective at that time. Damage to nut crops may not be restricted to the time they are on the tree. For example, full-sized macadamia nuts may be damaged whilst on the tree, but even more so up to 1 week after they drop to the ground, and this needs to be taken into account when applying chemical treatment (Jones and Caprio, 1994).
A range of carbamates and organophosphates may control N. viridula, but their persistence is too low to prevent subsequent outbreaks (Waterhouse and Norris, 1987; Martins et al., 1990).
Alternative insecticides (tralomethrin, lambda-cyhalothrin and acephate) are less toxic and may reduce production costs, increase yield and improve soyabean quality (Chyen et al., 1992; Le Page, 1996; McPherson, 1996). Some of the synthetic pyrethroids tested gave greater residual control than acephate; however, permethrin, did not control N. viridula in soyabean (McPherson et al., 1995).
Peaches have been protected effectively with chlorpyrifos (Johnson et al., 1985).
The permissible amount of stained rice grains (including pecky rice) is too low to establish reliable control thresholds, and prophylactic applications of insecticides tend to be made against hemipteran rice pests in Japan, with N. viridula being the principal species in southern Japan (Ito, 1986).
Trials on insecticidal plant extracts such as azidarachtin do not compare in efficiency with synthetic insecticides (Ivbijaro and Bolaji, 1990). Some research has been conducted on insect growth regulators but they do not appear to be effective (Canela et al., 1995; McPherson and Gascho, 1999).
Disease transmission by N. viridula to citrus fruits has resulted in the use of insecticidal control methods in Cuba (Grillo and Alvares, 1983).
In South America, the addition of NaCl to insecticides is recommended because it lowers the required dosage (see IPM Programmes).
Resistance and chemical control in soyabean were evaluated by Gazzione (1995) and Rosso et al. (1995).
Field Monitoring and Economic Threshold Levels
Control strategies against N. viridula in soyabean should be related to the stage of pod development (Brier and Rogers, 1991). Early pod fill (stage R5: Kogan and Turnipseed, 1980) is the most sensitive stage, and the only one in which yield, seed weight and oil content was significantly reduced (Brier and Rogers, 1991). Bugs should be controlled before this stage is reached, i.e. towards the end of pod elongation. Once pod fill is completed, soyabeans are not at risk and control is not warranted unless planting seed or edible seed is being grown (Brier and Rogers, 1991; Suzuki et al., 1991). For further specific information on when control methods are warranted on soyabean, see Kogan et al. (1977), Kobayashi (1981), Panizzi and Slansky (1985) and McPherson et al. (1993).
For sorghum, the damage threshold is about four N. viridula adults per panicle for infestation from the milk stage of grain development to maturity, but about 16 adults from the soft dough stage to maturity (Hall and Teetes, 1982b).
When milk-stage wheat kernels are infested at levels of more than two adults per 20 spikes, control measures are warranted (Viator et al., 1983). In maize, two N. viridula adults per V15 stage plant causes significant reduction in yield (Negron and Riley, 1987). In contrast, the permissible levels of stained rice grains are too low for reliable thresholds to be established (Ito, 1986).
Cowpeas suffer significant yield loss only when N. viridula density reaches 12 per metre of row (Nilakhe et al., 1981), whereas passion fruit is treated at one pentatomid per metre (Neethling, 1992). In transgenic cotton, an arbitrary threshold of 1 bug/6 feet of row has been used (Greene and Turnipseed, 1996).
Prediction of population peaks has been attempted with a day degree temperature model (Cividanes and Figueiredo, 1997).
The geographical origin of N. viridula is a matter of debate, which warrants attention because accurate knowledge of its original distribution may yield specific parasitoids useful to control efforts. The most likely origin is the Mediterranean area and/or the African mainland (Hokkanen, 1986; Jones, 1988). Biological control efforts across the world have been summarized in detail by Waterhouse (1998).
N. viridula has long been a target for biological control, mainly through the introduction of parasitic wasps and flies (see Waterhouse and Norris (1987), Bennett (1990), Clarke (1990)). Although success has been widely claimed, especially in Australia and Hawaii (Caltagirone, 1981; Waterhouse and Norris, 1987; Todd, 1989; Bennett, 1990) the degree of that success has been seriously questioned through the research of Clarke (1990, 1992) in Australia, and Jones (1995) in Hawaii.
The problems with the claims of success are as follows:
- The parasitoid said to have achieved successful control in Australia was the so-called Pakistan strain of Trissolcus basalis. However, T. basalis does not exist in Pakistan. The wasps sent originally from Pakistan to Australia are morphologically distinct from T. basalis and represent a new species, T. crypticus (Clarke, 1993). These are evidently parasitoids of species other than N. viridula in Pakistan (although they parasitize N. viridula eggs successfully in the laboratory) and have probably not established in Australia (Clarke, 1993).
- Parasitism of N. viridula eggs by T. basalis is relatively low in many situations, for example, in Hawaiian macadamia orchards (Jones, 1995) and soyabean in south-east Queensland (Clarke and Walter, 1993b).
- In many studies, most of the destruction of N. viridula eggs in the field was attributable to predators, mainly ants (Jones (1995) in Hawaii; Van den Berg et al. (1995) in Sumatra, Indonesia).
- Adequate post-release studies were never conducted on N. viridula populations, so the impact of the released natural enemies was never quantified. Any decline in N. viridula numbers at the time of natural enemy releases (at least in Australia) can be explained by changing agricultural practices, including the widespread introduction and prophylactic use of synthetic organic insecticides. Reduced use of synthetic organics in Australian vegetable crops has seen the re-emergence of N. viridula as a pest in areas where it was considered to have been under good biological control, but this has not been quantified.
The widely accepted success of T. basalis as a biological control agent led to it being distributed around the world for release, despite inaccurate claims of its inability to parasitize N. viridula eggs efficiently on soyabean (Turner, 1983) and its being restricted to coastal areas (Jones, 1988). The species achieves high levels of parasitism in soyabean in several parts of the world and is sometimes also abundant inland (Seymour and Sands, 1993).
As a consequence of its reputed success as a biological control agent in Australia and Hawaii (Waterhouse and Norris, 1987) T. basalis has been imported for release into places where it was already present, including Brazil (from Australia: Corrêa-Ferreira and Zamataro, 1989). The impact of such multiple strain introductions has never been accurately assessed (Clarke and Walter, 1995).
That the claimed results of these biological control projects are being questioned does not imply that T. basalis is not worth importing, and it has, since 1980, been introduced into Argentina from Australia (de Crouzel and Saini, 1983) and into California from France, Spain and Italy (Hoffmann et al., 1991). The species evidently causes high levels of parasitism in parts of South America (Corrêa-Ferreira and Moscardi, 1995, 1996), Pohnpei (Esguerra et al., 1993) and in Australian pecan orchards (Seymour and Sands, 1993).
The influence of T. basalis as a biological control agent will possibly be enhanced by the development of mass-release programmes for situations in which N. viridula populations breed up in a crop and thus attain pest status. Release programmes in Brazilian soyabean are reputedly successful (Moscardi, 1993; Corrêa-Ferreira and Moscardi, 1996) and the strategy has been tested elsewhere on other crops (Justo et al., 1997; Cameron and Rea, 1998).
Techniques to facilitate the production of egg parasitoids are quite advanced. In addition to mass-rearing techniques (Oi, 1991; Awadalla, 1996), storage of frozen hosts (Corrêa-Ferreira and Moscardi, 1993; Corrêa-Ferreira and de Oliveira, 1998), identification and development of kairomones (Sales, 1985; Bin et al., 1993; Mattiacci et al., 1993) and development of artificial hosts (Volkoff et al., 1992) have all been tackled, but none is yet available for commercial use.
Biological control by egg parasitoids is virtually never hampered by the influence of hyperparasitism, because hyperparasitoids of egg parasitoids are unusual. However, researchers should be aware that two species of pteromalids in the genus Acroclisoides parasitize T. basalis in the field in Australia (Clarke and Seymour, 1992).
Parasites of stages other than eggs
Parasitoids that attack nymphs and adults of N. viridula have also been used in biological control, and these organisms are being increasingly investigated for biocontrol purposes (see Parasitoids). These organisms show some potential but, to date, none has proved as successful as the egg parasitoids. Species from the area of origin of N. viridula may worth trying. In particular, of the species present in Africa, the most promising may be Bogosia antinorii, as it is apparently specific to N. viridula (Waterhouse, 1998).
An increasing number of publications claim that ants have a strong impact on N. viridula eggs and nymphs, both in orchards (Yang, 1984; Seymour and Sands, 1993; Jones, 1995) and in soyabean fields (Krispyn and Todd, 1982; van den Berg et al., 1995). The thoughtful manipulation of ant populations could contribute considerably to achieving acceptable levels of biological control. Spiders may also contribute significantly to reducing N. viridula populations, but the data are not convincing (Kiritani and Hokyo, 1962) and they are still being investigated in the laboratory (Sarma and Dutta, 1996b).
To date, no practical use has been made of N. viridula pheromones, either for monitoring or control purposes. Disagreement still exists as to the identity of the functional components in the pheromone blend.
ReferencesTop of page
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