https://orcid.org/0000-0002-0125-6505
Abstract
The rice stink bug, Oebalus pugnax (Fabricius), is the most important late-season insect pest of rice in the southern United States. Nymphs and adults feed on rice grains, resulting in losses in yield and grain quality. Aspects of the biology, ecology, life history, and chemical ecology have been investigated in southern rice producing states but several outstanding questions remain. Standard economic threshold levels (ETLs) based on sweep net sampling for rice stink bug have been established depending on grain development stage and geographic location. However, recent studies on the relationship between rice stink bug densities, feeding damage, and its economic impacts suggests that changes to ETLs for rice stink bug may be needed. The primary management tactic for controlling rice stink bug infestations is the application of chemical insecticides, but alternative management tactics are needed because of the potential for development of insecticide resistance and impacts on non-target organisms. Biological control appears to be a promising strategy, even though it has remained largely untapped. Future research should focus on the biology, behavior, host plant preference, and chemical ecology of the rice stink bug, knowledge of which will aid in the development of integrated pest management strategies. This review article covers the biology, feeding behavior, sampling techniques, ETLs, management, knowledge gaps, and potential management tactics of rice stink bug.
The rice stink bug, Oebalus pugnax (F.) (Hemiptera: Pentatomidae), was first reported as a pest of rice by Riley (Riley 1882) and is presently the most important insect pest of reproductive-stage rice in the United States (Way 2003). Both nymphs and adults of O. pugnax use their piercing and sucking mouthparts to feed on developing grains of rice and other plants from heading (initial exsertion of the panicle, or grain-bearing structure) through grain maturity (Bowling 1979, Espino et al. 2007). From the anthesis (bloom) stage to the milk stage of grain development, rice stink bug feeding can cause significant losses in rough rice yields. At later stages of grain maturity (milk and dough stages), rice stink bug feeding causes localized discoloration of the grains called ‘peck’ (Swanson and Newsom 1962, Bowling 1963, Lee et al. 1993, Patel et al. 2006a, Awuni et al. 2015b) and can also weaken grains, resulting in increased breakage during the milling process and hence reductions in head rice (Wilson and Stout 2020). Currently, management of the rice stink bug is primarily accomplished through insecticide applications (Blackman et al. 2015a, Cherry et al. 2018), but the potential exists for incorporating alternative tactics into the management program. This review summarizes rice stink bug biology and management, with the goal of highlighting areas in need of further investigation to improve the current management program for this important pest.
Taxonomy and Geographic Distribution of the Genus
The rice stink bug was first described by Fabricius in 1775 under the scientific name ‘Cimex pugnax’. The genus name was later changed to ‘Oebalus’ by Stal in 1862. Following this change, the genus name was revised several times. Among several others, the genus name ‘Solubea’, which was first coined by Bergroth in 1891, was widely found in the older literature (Sailer 1944). The justification Bergroth provided for the name change was that the genus name ‘Oebalus’ Rafinesque 1815 already existed. However, Sailer suggested that the genus ‘Oebalus’ was still nomen nudum and the genus ‘Solubea’ should be changed back to ‘Oebalus’ (Sailer 1957). The genus Oebalus is native to the Neotropics (Sailer 1944). Three species of Oebalus, namely, O. pugnax, O. ypsilongriseus, and O. insularis, are found north of Mexico. Among the three species, O. pugnax is dominant and has been reported in all major rice growing regions of the United States (Sailer 1944, Jones and Cherry 1986) except California. Oebalus ypsilongriseus (DeGeer) was first intercepted in Homestead, Florida, in 1983 (Mead 1983). In 1988, it was found in Florida rice fields (Cherry et al. 1998). This species has two forms: a hibernating and a non-hibernating form. The development of the two forms is regulated by photoperiod (Vecchio 1994). The hibernating form can be differentiated from the non-hibernating form based on differences in yellowish spots on pronotum, markings on the callous areas on the scutellum, and the humeral angle of pronotum (Vecchio 1994, Musolin and Saulich 2018). Oebalus insularis (Stal), which is native to the Caribbean islands and Central and South America (Sailer 1944), was first reported in Florida rice fields in 2007 (Cherry and Nuessly 2010). So far, O. ypsilongriseus and O. insularis have been reported only from the Everglades region of Florida (VanWeelden et al. 2020). A 2-yr survey in Florida rice fields and adjacent graminaceous non-host crops using sweep nets showed that O. insularis is relatively more abundant than O. ypsilongriseus (VanWeelden et al. 2020). The three species can be differentiated based on lengths of the antennal segments, spines on the humeri and markings on the scutellum. In O. ypsilongriseus, the first antennal segment is twice as long as the second antennal segment. In both O. pugnax and O. insularis, the second antennal segment is longer (1.2×) than the first antennal segment. The scutellum of O. pugnax is yellow and has anterolateral spines while O. insularis has a reddish-brown scutellum with short lateral spines. The apex of scutellum, including the basal margins, is yellow and these markings extend up to the middle of the scutellum giving a U-shaped appearance in O. insularis (McPherson and Bundy 2018).
Morphology and Life History
Adults
Adults of O. pugnax are straw colored, shield-shaped bugs (Ingram 1927). They measure approximately 1.2 cm long and 0.6 cm wide. From each shoulder, a single sharp spine protrudes forward (Ingram 1927). Females are typically larger and heavier than males (Cherry et al. 2018). Females can be identified by the presence of a horizontal slit like opening on the abdominal sterna (Fig. 1a and b), and the abdominal sterna of reproducing females often appear green due to presence of eggs (Nilakhe 1976a).
Oebalus pugnax adult (a) female and (b) male. Females can be separated from males looking for the horizontal opening at the abdominal tip on females (black arrow).
Rice stink bugs overwinter as adults in weedy grass clumps (Nilakhe 1976a). Time of entry into overwintering differs based on geographic location. In Louisiana and Mississippi, adults enter overwintering sites beginning the first week of October and entrance is completed by the third week of the same month (Nilakhe 1976a). Hibernation is thought to be induced by shorter photoperiods and cooler days, and nymphs that experience such conditions overwinter after becoming adults (Vecchio 1994). According to Nilakhe (1976a), overwintering adult females have underdeveloped reproductive organs and large fat bodies. Adults do not mate before hibernation. Overwintering is terminated in April in Louisiana (Nilakhe 1976a). Emergence of males precedes that of females by 10 d. After emergence, adults initially feed on weedy grass hosts or other cultivated crops such as wheat that are in their reproductive stages. The adult premating period ranges between 1.5 and 3.8 d (Nilakhe 1976a). Matings are frequent in the evening but can occur anytime during the day (Nilakhe 1976a). Mating is followed by oviposition. Females oviposit their first egg mass about 5 d after emergence (Rashid et al. 2005b). Female fecundity, mating frequency, and daily oviposition are highly dependent on host plant (Rashid et al. 2005b). Female fecundity has not been studied over the full geographic range of the insect but females laid on an average of 915 eggs when fed on rice under greenhouse conditions in Louisiana with a day temperature of 31°C (Nilakhe 1976a). The mean oviposition period is 42 d. Adults can mate several times in their lifetime and if a female mates and oviposits on the same day, the latter is usually followed by the former (Nilakhe 1976a). The average adult lifespan of females is 50 d and that of males is 39 d (Nilakhe 1976a).
Eggs
Female rice stink bugs deposit eggs on leaves, panicles, or seed heads of host plants (Nilakhe 1976a). Eggs are laid in two alternating rows (Bernhardt 2009) (Fig. 2a and b). The eggs adhere to each other and are kept in position by a secretion released during oviposition (Esselbaugh 1946). The number of eggs in a cluster ranges from 8 to 44 (Esselbaugh 1946). Eggs are barrel-shaped, 0.84 mm in height and 0.63 mm wide, with a transparent chorion and flat operculum (Bundy and McPherson 2000). Initially, eggs are green, but with embryonic development, the egg color gradually changes and becomes red prior to hatching (Bernhardt 2009) (Fig. 2a and b). These changes are clearly visible through the transparent chorion, including the first appearance of red markings in the form of the letter ‘W’ (Bernhardt 2009). Egg hatching time increases with decreasing temperature. At 29°C eggs hatch in 4–5 d (Rashid et al. 2005a). The minimum and maximum threshold temperature for egg hatching were found to be 15°C and 37°C, respectively (Rashid et al. 2005a, Bernhardt 2009). Egg hatching success is approximately 75% (Nilakhe 1976a).
Life stages of Oebalus pugnax: eggs on rice leaf – (a) egg are green and turn (b) red as they mature; (c) third instar (photo by N. Lord, Louisiana State University); and (d) fifth instar (photo by N. Lord, Louisiana State University).
Nymphs
Oebalus pugnax develops through five nymphal stages before adult emergence (Rashid et al. 2005a). Nymphs have piercing and sucking mouthparts and four-segmented antennae (Decoursey and Esselbaugh 1962) (Fig. 2c and d). Early instars can be differentiated from late instars based on body shape, color, and size. First and second instars are orange red and elliptical. The tylus is longer than jugus in early instars. Fourth and fifth instars are elongate, pale tan, and their tyla and juga are equal in length. The average length and width of first instar is 1.16 mm and 0.83 mm, respectively. Second instars are 2.00 mm long and 1.30 mm wide. Fourth instars are 3.2–5.1 mm in length, 2.0–2.8 mm in width and have small but visible wing pads. Wing pads grow with successive molts and fifth instars have larger wing pads with varying amounts of dark pigmentation. The fifth instar is about 4.7–8.6 mm in length and 3.0–4.1 mm in width (Decoursey and Esselbaugh 1962). At the fifth-instar stage, males can be separated from females by the presence of red testes that are clearly visible through abdominal sterna (Nilakhe 1976a).
Rice stink bug development, growth, and survival are largely dependent on temperature and host plant (Table 1). In general, rice stink bugs perform better on rice compared to other cultivated crops and weedy grass hosts (Rashid et al. 2005b, Awuni et al. 2014). Under field conditions, development time from egg to fifth instar on rice was approximately 21 d in Louisiana (Blackman and Stout 2017). The survival rate of nymphs to adulthood caged on panicles in the field was reported by Blackman and Stout (2017) to be 35%. However, under lab conditions development time is shorter and survival is higher. At 29°C when nymphs were reared on rice panicles, 80% of nymphs developed to adult stage in 18 d after emerging from eggs, equivalent to 249.4 degree days (Rashid et al. 2005a).
Adult and nymphal life history parameters of the rice stink bug, Oebalus pugnax, reared on different host plants
| Host plant | Temperature (°C) | Development stage | Development time (days) | Survival to adult (%) | Adult weight (mg) | References | |
|---|---|---|---|---|---|---|---|
| Male | Female | ||||||
| Oryza sativa | 28 | First instar - adult | 18.1 | 37.5 | 42.5 | Hamm (2011) | |
| 27 | First instar - adult | 16.2 | 51.4 | 26.5 | 35.7 | de Freitas et al. (2019) | |
| Sorghum vulgare | 27 | Egg-adult | 25.8 | 60a | Naresh and Smith (1983) | ||
| Leptochloa panicoides | 28 | First instar - adult | 22a | 22a | 22a | Hamm (2011) | |
| Echinochloa crusgalli | 28 | First instar - adult | 19a | 20a | 23a | Hamm (2011) | |
| Paspalum dilatatum | 25 | Second instar-adult | 19a | 36a | Awuni et al. (2014) | ||
| Echinochloa colona | 25 | Second instar-adult | 18a | 78a | Awuni et al. (2014) | ||
| Paspalum urvillei | 27 | Egg-adult | 28.8 | 30a | Naresh and Smith (1983) | ||
| Host plant | Temperature (°C) | Development stage | Development time (days) | Survival to adult (%) | Adult weight (mg) | References | |
|---|---|---|---|---|---|---|---|
| Male | Female | ||||||
| Oryza sativa | 28 | First instar - adult | 18.1 | 37.5 | 42.5 | Hamm (2011) | |
| 27 | First instar - adult | 16.2 | 51.4 | 26.5 | 35.7 | de Freitas et al. (2019) | |
| Sorghum vulgare | 27 | Egg-adult | 25.8 | 60a | Naresh and Smith (1983) | ||
| Leptochloa panicoides | 28 | First instar - adult | 22a | 22a | 22a | Hamm (2011) | |
| Echinochloa crusgalli | 28 | First instar - adult | 19a | 20a | 23a | Hamm (2011) | |
| Paspalum dilatatum | 25 | Second instar-adult | 19a | 36a | Awuni et al. (2014) | ||
| Echinochloa colona | 25 | Second instar-adult | 18a | 78a | Awuni et al. (2014) | ||
| Paspalum urvillei | 27 | Egg-adult | 28.8 | 30a | Naresh and Smith (1983) | ||
aValues are estimates from figures.
Adult and nymphal life history parameters of the rice stink bug, Oebalus pugnax, reared on different host plants
| Host plant | Temperature (°C) | Development stage | Development time (days) | Survival to adult (%) | Adult weight (mg) | References | |
|---|---|---|---|---|---|---|---|
| Male | Female | ||||||
| Oryza sativa | 28 | First instar - adult | 18.1 | 37.5 | 42.5 | Hamm (2011) | |
| 27 | First instar - adult | 16.2 | 51.4 | 26.5 | 35.7 | de Freitas et al. (2019) | |
| Sorghum vulgare | 27 | Egg-adult | 25.8 | 60a | Naresh and Smith (1983) | ||
| Leptochloa panicoides | 28 | First instar - adult | 22a | 22a | 22a | Hamm (2011) | |
| Echinochloa crusgalli | 28 | First instar - adult | 19a | 20a | 23a | Hamm (2011) | |
| Paspalum dilatatum | 25 | Second instar-adult | 19a | 36a | Awuni et al. (2014) | ||
| Echinochloa colona | 25 | Second instar-adult | 18a | 78a | Awuni et al. (2014) | ||
| Paspalum urvillei | 27 | Egg-adult | 28.8 | 30a | Naresh and Smith (1983) | ||
| Host plant | Temperature (°C) | Development stage | Development time (days) | Survival to adult (%) | Adult weight (mg) | References | |
|---|---|---|---|---|---|---|---|
| Male | Female | ||||||
| Oryza sativa | 28 | First instar - adult | 18.1 | 37.5 | 42.5 | Hamm (2011) | |
| 27 | First instar - adult | 16.2 | 51.4 | 26.5 | 35.7 | de Freitas et al. (2019) | |
| Sorghum vulgare | 27 | Egg-adult | 25.8 | 60a | Naresh and Smith (1983) | ||
| Leptochloa panicoides | 28 | First instar - adult | 22a | 22a | 22a | Hamm (2011) | |
| Echinochloa crusgalli | 28 | First instar - adult | 19a | 20a | 23a | Hamm (2011) | |
| Paspalum dilatatum | 25 | Second instar-adult | 19a | 36a | Awuni et al. (2014) | ||
| Echinochloa colona | 25 | Second instar-adult | 18a | 78a | Awuni et al. (2014) | ||
| Paspalum urvillei | 27 | Egg-adult | 28.8 | 30a | Naresh and Smith (1983) | ||
aValues are estimates from figures.
Rice stink bugs survive better and develop faster under warm temperatures than cool temperatures (Naresh and Smith 1983, Rashid et al. 2005a). At 25°C, first instars molt to second instars in about 2 d (Rashid et al. 2005a). First instars do not feed (Bowling 1979) and tend to aggregate on egg remnants (Ingram 1927) or highly humid places under laboratory conditions. Second instars show similar aggregation behavior but they start to feed. The minimum threshold temperature for development of second and third instars is 12°C and 14°C, respectively (Rashid et al. 2005a). Moreover, both nymphs and adults that developed in cooler temperatures were lighter than those that developed at warmer temperatures because of reduced feeding activity (Naresh and Smith 1983).
Ecology and Behavior
The rice stink bug is an oligophagous species that feeds on flowering plants in the family Poaceae. Rice is the primary cultivated host of the rice stink bug. Other cultivated crop hosts include barley, Hordeum vulgare (L); corn, Zea mays (L); oats, Avena sativa (L); rye, Secale cereale (L); sorghum, Sorghum bicolor (L); and wheat, Triticum aestivum (L) (Hall IV and Teetes 1982, Viator et al. 1983, Harper et al. 1993, McPherson et al. 1993, Tillman 2010b). In addition, weedy grasses serve as alternate hosts for the rice stink bug. Weed hosts include barnyard grass, Echinochloa crusgalli (L.); browntop millet, Urochloa ramosa; broadleaf signalgrass, U. platyphylla; crabgrass, Digitaria spp.; dallisgrass, Paspalum dilatatum Poir; fall panicum, Panicum dichotomiflorum; Italian ryegrass, Lolium perenne spp. multiflorum; jungle rice, Echinochloa colona (L.); prairie cupgrass, Eriochloa contracta Hitchc.; southwestern cupgrass, Eriochloa acuminata (J. Presl Kunth); and vaseygrass, Paspalum urvillei; yellow foxtail, Setaria pumila (Poir) (Naresh and Smith 1984, Cherry and Wilson 2011, Awuni et al. 2015a).
Adults emerging from overwintering feed on a wide range of weedy hosts and cultivated crops present in the heading stage. Awuni et al. (2015a) sampled several weedy grass hosts for rice stink bugs over 2 yr from April to August in Mississippi and reported that the relative abundance of rice stink bugs varied among weedy grass hosts in spring in Mississippi probably because of differences in feeding preferences and for suitability of grassy hosts. Choice experiments have shown that barnyard grass, jungle grass and vasey grass were the most preferred weedy hosts for feeding by rice stink bug, with Italian rye grass and dallis grass the least preferred hosts (Naresh and Smith 1984, Rashid et al. 2005b, Awuni et al. 2014). In addition, nymphal development and survival is better on barnyard grass and jungle rice than on other weeds (Table 1). Host availability and subsequent host switching between alternate weed hosts may be vital for optimal rice stink bug survival, development, and reproduction and, in turn, for seasonal abundance (Awuni et al. 2014, Awuni et al. 2015a). Two and sometimes three generations of rice stink bugs may be produced on weedy grass hosts. After emergence of rice panicles begin, rice stink bugs abandon weed grass hosts and disperse into rice fields. Considering the time necessary for stink bugs to develop on rice (ca. 3 wk) and the time needed for rice grains to mature in the field (ca. 3–4 wk in a given field given variation in heading dates among tillers), it is likely that O. pugnax passes through only a single generation in a given rice field; however, because planting of rice in spring and thus maturation of fields in the summer is staggered, populations of O. pugnax may pass through multiple generations on rice in a given region (Ingram 1927).
As their name suggests, stink bugs produce and emit volatile chemicals when they are disturbed. Secretions from the metathoracic glands (MTGs) of O. pugnax have not been as well characterized as those of other stink bugs. In O. pugnax, the scent secretions are produced by large, round and reddish-orange glands located on either side in the metathoracic region and extending to the second abdominal segment. These glands are well developed in adults but poorly developed in nymphs (Blum et al. 1960). The MTG secretions are released as orange yellow droplets (Blum et al. 1960). These secretions are composed of several short chain aldehydes, esters, and straight chain alkenes and alkanes. The most abundant compound in the MTGs of O. pugnax is n-tridecane (60%) and trans-2-heptenal (Blum et al. 1960, Hamm 2011). Other compounds that have been identified as components of MTG secretions include aldehydes such as (E)-2-hexenal, (E)-2-heptenal, (E)-2-octenal, (E)-2-decenal; esters such as (E)-2- hexenyl acetate, (E)-2-octenyl acetate, and the short chain alkane, n-dodecane (Hamm 2011). These secretions probably play an important role in intra-specific and defensive communication, but their functions in O. pugnax have not been fully investigated. Hamm (2011) prepared a four-compound blend of MTGs comprising of n-tridecane, (E)-2-hexenal, (E)-2-hexenyl acetate, and (E)-2-octenyl acetate and tested the influence of the blend on the behavior of adult rice stink bugs. They found that adult response to the blend was concentration-dependent: adults were attracted to lower concentrations but repelled by high concentrations. Moreover, MTG secretions had a repellant effect on predatory fire ants, with fire ants walking away from the odor source (Blum et al. 1960). In addition, MTG secretions are used as kairomones by natural enemies in other stink bugs (Laumann et al. 2009).
Rice Stink Bug Feeding Injury and Damage
Feeding Physiology
Rice stink bugs have piercing and sucking mouthparts, like other pentatomids. The mouthparts of pentatomids consist of pairs of modified mandibular and maxillary stylets surrounded by a beak or rostrum that forms a sheath. Saliva produced during feeding helps degrade the rice hull (lemma and palea) and grain contents. The stylet is then pushed through the saliva into developing grains. Eventually, the saliva surrounding the outer parts of the stylet solidifies, forming a cone shaped structure, which is commonly termed a stylet sheath, feeding sheath, flange, or collar (Bowling 1979). Stylet sheaths of rice stink bugs are tan colored and volcano shaped. Even after termination of feeding, stylet sheaths remain loosely attached to the structure on which rice stink bugs fed. However, the presence of a salivary sheath does not always mean successful penetration of the stylet into the hull (Hollay et al. 1987). According to Hollay et al. (1987) stylet sheaths are of different sizes, circa 50 µM to 250 µM in basal diameter. The former (50 µM stylet sheaths) cannot penetrate through the hull, are produced in large numbers, represent unsuccessful feeding attempts and hence are treated as exploratory feeding probes/probing activity. The latter (250 µM stylet sheaths) are capable of penetrating through the hull, and reach the interior grain contents and reflect prolonged feeding activity. These stylet sheaths are found typically on grains in fewer numbers. Hence, the presence of stylet sheaths is often used as an indicator of rice stink bug feeding activity (Bowling 1979). The differences in numbers of stylet sheaths on grains have sometimes been used to determine levels of host plant resistance (Bowling 1979). In addition, factors such as temperature and life stage influence rice stink bug feeding activity and in turn numbers of stylet sheaths produced. For example, greater numbers of stylet sheaths were found on rice grains at 25°C compared to 30°C and 32°C (Bowling 1979). Second instars compared to other life stages produce few stylet sheaths (except for first instars, which do not feed). Females feed for longer periods than males and produce twice as many stylet sheaths as males, owing to their larger body size (Bowling 1979).
Injury and Damage to Rice
Rice stink bugs are found on plants from heading (exsertion of the panicle from swollen sheath of the flag leaf, stage R3 in Counce et al. (2000)) to grain maturity and feed on rice kernels as they develop. The type and severity of injury depends on the maturity stage of the grain. Milk and soft dough stages of panicle development (R6 and R7 stages in Counce et al. (2000)) are deemed the most susceptible stages for rice stink bug feeding and damage (Espino et al. 2007). Choice tests have been conducted to investigate the relative attractiveness of different reproductive stages to rice stink bug. Espino and Way (2008) found that among the four stages (pre-heading, heading, milk, and soft dough) of rice plant development, more numbers of rice stink bug adults were located on plants at the milk and soft dough stages compared to the other stages. The authors concluded that the most attractive stages of the rice plant to both male and female O. pugnax are the milk and soft dough stages of panicle development. Rice stink bugs are less attracted to pre-heading and heading rice plants.
Feeding by the rice stink bug on developing rice grains causes two types of damage, the relative importance of which depends not only on levels of rice stink bug infestation but also on the timing of stink bug feeding relative to kernel and panicle development. Feeding by rice stink bugs on kernels from anthesis to the milk stage results in empty or atrophied grains due to partial or complete removal of grain contents and damage caused to ovaries. This type of damage results in quantitative losses due to decreases in numbers of filled grains and average grain weights that ultimately lowers rough rice yields (Patel et al. 2006a, Awuni et al. 2015b). The second type of damage involves reductions in grain quality that result from feeding during later stages of grain development. Rice stink bug feeding during the late milk and dough stages of grain development often causes black or brown discoloration, usually with a characteristic ‘bullseye’ shape (Fig. 3) (Helm 1954). This discoloration is clearly visible on dehulled rice and is termed ‘peck’ by trade (Swanson and Newsom 1962). Formation of peck is due to a combination of O. pugnax feeding and subsequent invasion by fungi at feeding sites and through undersides of stylet sheaths present on hulls (Lee et al. 1993). Douglas and Tullis (1950) suggested that fungi such as Curvularia lunata, Fusarium spp., Phoma spp., Trichoeonis caydata, and Helminthosporium oryzae might be responsible for kernel discolorations in rice. Two decades later, Lee et al. (1993) isolated several species of fungi, bacteria and yeast from field collected O. pugnax-damaged rice grains. In addition, isolates were also collected from bug stylets and saliva. These isolates were cultured separately and then inoculated into developing rice grains. Grains inoculated with fungi including F. oxysporum, Cochliobolus miyabeanus, C. lunata, Alternaria alternata, and A. padwickii developed kernel discolorations similar to peck in the field but no such discolorations were found on grains inoculated with bacteria or yeast. This study also proposed the possibility that rice stink bugs serve as vectors of these fungi; however, so far, very little is known about the role of the rice stink bug in vectoring these microorganisms. A single study conducted by Daugherty and Foster (1966) reported that the organism responsible for yeast spot disease, Nematospora coryli, might be transmitted from one plant to another by the rice stink bug during feeding.
Feeding by Oebalus pugnax results in discoloration of grains termed as ‘peck’.
Furthermore, pecky rice is structurally weak and often breaks at the site of feeding during the milling process, resulting in increased incidence of broken rice grains. Broken grains result in lower head rice yields, which in turn may result in reductions in USDA grade and finally reductions in prices. If injured grains escape breakage, peck on milled grains can result in reductions in rice grades (Awuni et al. 2015b). Based on the percentage of chalky kernels, peck, and broken grains, grades from U.S. No. # 1 to US No. # 6 are assigned (USDA 2009). With reductions in grade, the percent discount for milled rice increases, which can greatly impact profitability (Harper et al. 1993).
Sampling for Rice Stink Bug
Sampling is conducted to determine rice stink bug densities to inform timely management practices, in particular the application of insecticides. Sweep net sampling is by far the most widely used sampling method and is recommended in all rice producing states in the United States (Bowling 1969). This technique involves sweeping a 38 cm diameter net in a 180° arc over rice panicles. With each forward step, a single sweep is made and ten such consecutive sweeps constitute a sample unit. For reliable estimates of rice stink bug populations, conducting a minimum of 10 sample units is recommended (Bowling 1962, 1969), but for large areas, greater numbers of sample units are recommended (Espino et al. 2008). Recently, Cato et al. (2019) found that sweep length has an effect on rice stink bug captures. The authors reported that a short sweep length of 0.9 m captured on an average 2.2 fewer rice stink bugs than did a sweep length of 1.8 m. However, no such differences in stink bug catches were observed when a sweep length of 1.8 m was compared to a sweep length of 3.5 m. The latter is equivalent to the traditionally recommended practice of a 180° arc. A sweep length of 1.8 m was recommended to obtain reliable information on rice stink bug numbers in the field for pest population assessment and subsequent decision-making for ETLs (Cato et al. 2019).
Other methods of sampling include visual observations with long- and short-sweep sticks (Espino et al. 2008). A long sweep stick consists of a 1.5-m long, 2 cm wide PVC pipe. The pipe is gently passed through a canopy of rice panicles at 180° and the numbers of stink bugs that fly along the entire length of the pipe are counted. A similar procedure is followed for short sweep sticks except that the sweep stick is 1 m long and adults that fly from the tip up to 0.38 m of the 1 m long stick are counted (Espino et al. 2008). Comparisons among different sampling techniques showed that counts of rice stink bug with visual methods correlate well with sweep net sampling and that the former method is cheaper than latter. Likewise, Bowling (1969) reported that estimates of rice stink bug populations obtained by counting the insects that were visually observed on panicles positively correlated with the numbers of rice stink bugs captured by sweep net sampling.
Several factors influence rice stink bug captures with sweep nets. The most fundamental of these factors is the inherent efficiency of the method itself. Blackman (2014) seeded small rice plots at densities of 3–10 rice stink bug per 10 sweeps (ca 100 ft2), and found that efficiency ranged between 19 and 21% when sweeps were performed at the recommended width of 1.5 m per sweep. The results from this mark-recapture study suggest that about 80% of rice stink bugs in the field are unaccounted for when sampling with sweep net. Another factor that influences the efficiency of sweep-netting is time of sampling. Greater numbers of rice stink bugs were captured at cooler times of the day (i.e., 0900 h and 1900 h) than at warmer times (i.e., 1300 h) of the day in a study by Rashid et al. (2006) in Arkanasas rice fields. A similar trend was also observed by Espino et al. (2008) in Texas but Cherry and Deren (2000) reported that time of day had no impact on rice stink bug catch by sweepnet in rice fields in Florida. In addition, sampling for rice stink bugs within 9 m of field borders overestimated populations (Espino et al. 2008), probably because of the presence of weedy grass on levees, differences in field length and width, and distance between levees, all of which affect rice stink bug movement in and out of rice fields. Sampling at least 50 m away from field margins is optimal (Foster et al. 1989). Moreover, Foster et al. (1989) observed differences in adult and nymph counts in sweep net captures from main crop and ratoon crop rice. Captures in the former included more numbers of adults while in the latter greater numbers of nymphs were detected. Furthermore, rice phenology also influences rice stink bug captures. Numbers of rice stink bugs found in sweep nets were higher from anthesis to soft dough stages of grain development than from hard dough stage to maturity (Douglas 1939, Rashid et al. 2006). It is speculated that adult migration and subsequent in-field reproduction are responsible for this pattern (Jones and Cherry 1986).
Current recommendations call for sweep net sampling of rice stink bug populations to begin when at least 75% of rice plants are headed. This time corresponds with rice stink bug dispersal into rice fields (Douglas 1939). This was further corroborated by Rashid et al. (2006), who used yellow pyramid traps to monitor rice stink bug movement in and out of rice fields. The trap captures revealed that movement of rice stink bug into rice fields was maximal when panicles started to emerge and continued until at least 75% of rice plants had headed. In addition, Cherry and Wilson (2011), using black light traps, found that, compared to other months of the year, flight activity of stink bug species in Florida was maximal in the month of July, the period when the majority of panicle emergence occurs.
Economic Thresholds for Rice Stink Bug
Development of improved thresholds for application of insecticides is a pressing need for the development of a sustainable management program for O. pugnax in rice. Current action thresholds are similar throughout the rice producing states of the southern United States. In Louisiana and Florida, thresholds of 3 bugs per 10 sweeps during the first 2 wk of heading and 10 bugs per 10 sweeps thereafter are recommended, while in Mississippi and Arkansas the thresholds are 5 bugs per 10 sweeps during the first 2 wk of heading and 10 bugs per 10 sweeps thereafter (Gore et al. 2014, Lorenz et al. 2018, Wilson 2019). Dynamic thresholds were developed in Texas in the late 1980s (Harper et al. 1993, Harper et al. 1994) that incorporated costs of insecticide application, rice value, loan value, expected yield, and rice growth stage, but in practice growers use action thresholds similar to those used throughout the rest of the South (M.O. Way, personal communication). These thresholds rarely result in levels of qualitative damage that result in penalties during the grading process.
Despite the relative unanimity in thresholds used across the south, the historical derivation and empirical bases for these thresholds are uncertain. Numerous attempts have been made over the past six decades to elucidate the relationship between rice stink bug density and economic impacts. These studies have generally found that higher densities of rice stink bugs result in higher levels of quantitative damage (Bowling 1963), qualitative damage (Harper et al. 1993, Espino et al. 2007), or more commonly, both (Swanson and Newsom 1962, Patel et al. 2006a, Awuni et al. 2015b, Wilson and Stout 2020). A single study, however, reported negligible impacts for both quantitative and qualitative damage, thereby concluding that the species is not an economic pest (Odglen and Warren 1962). Discrepancies in the results of multiple studies are the result of variation in research methodologies and failure to adequately relate damage measurements to field sampling techniques. Studies that confined stink bugs in large or small cages have produced widely varying and collectively inconclusive results. Further, results from these studies are difficult to relate to sweep net captures during pest scouting.
The use of cages typically results in high levels of injury and damage to infested panicles, because infestation densities used in cages are often much higher than levels typically found in rice fields. Moreover, the use of cages may interfere with grain development, insect feeding behavior, and other yield-related physiological processes. Swanson and Newsom (1962) documented a 50% reduction in rough rice yield and levels of peck of 41–51% in cages that received a stink bug density of approximately one adult for every three rice panicles. Sleeve cages infested with much greater densities of one to two adults per panicle reduced panicle weights by approximately 50% in two separate studies (Patel et al. 2006a, Awuni et al. 2015b), but these studies reported lower levels of peck (15–25%) relative to the Swanson and Newsom (1962) study. Cage trials conducted by Douglas and Tullis (1950) reported levels of peck as high as 76% despite having a stink bug density of only one adult for every two rice plants. This study also reported percentages of sterile florets as high as 78%, though rice yields were not directly measured. In contrast, several cage studies utilizing similar methods have produced strikingly different results. Bowling (1963) used nearly identical methods to Swanson and Newsom (1962), but reported reductions in rough rice yield of <5% and levels of peck <1%. Espino et al. (2007) reported levels of peck ranging from 1 to 15% in cage trials, but no impacts on rough rice yield were detected. This finding was also supported by cage studies conducted by Odglen and Warren (1962) who reported no reduction in rough rice yield and levels of peck to be <1% even at high pest densities. More recently, Blackman (2014) conducted cage trials over a 3-yr period that included infestation levels estimated to be 20-fold greater than the sweep net threshold, but still found no relationships between O. pugnax densities and rice yield or any of the rice quality parameters measured. Thus, of eight cage studies conducted over the past six decades, four have reported high levels peck with substantial reductions in rough rice yields by rice stink bug and four have found little to no clear impact. Collectively, these studies are confounding and inconclusive. Alternative methodologies to study O. pugnax impacts on rice yield are needed to better elucidate this relationship.
To date, only two studies have attempted to relate densities of rice stink bugs in field plots to qualitative and quantitative damage. Harper et al. (1993) varied rice planting date, variety, and insecticide regimes to develop damage functions relating stink bug densities as determined by sweep samples to yield, head yield, and peck. Similarly, Wilson and Stout (2020) used different regimens of insecticide applications to quantify relationships among stink bug densities (sweep sampling), yield, head yield, and peck. These studies found similar relationships between sweep net captures and head yields with a decline of 0.3–0.5% in head yield for each one stink bug per 10 sweeps. Wilson and Stout (2020) reported a 0.015 g reduction in panicle weight for each stink bug per 10 sweeps, but acknowledged that this may not translate to rough rice yields on a per acre basis. Harper et al. (1993) reported no relationship between sweep net captures and rough rice yields. Wilson and Stout (2020) also reported peck response to be approximately 10-fold greater (0.3% per stink bug per 10 sweeps) than Harper et al. (1993), though this discrepancy likely resulted from the latter including peck values determined from milled rice rather than brown rice as is assessed by rice mills (USDA 2009).
In addition, the importance of nymphs relative to adults as causes of quantitative and qualitative damage is uncertain. Adults caused higher percentages of peck than nymphs in all stages of panicle development in a study by Espino et al. (2007). Blackman and Stout (2017) found that first instars that were caged on a single panicle until development to the adult stage decreased numbers of filled grains and increased broken grains and peck. Conversely, Harper et al. (1993), found that nymphs were not associated with reductions in rough rice yields and head yields. However, nymphal densities were not directly reported in this study and may have been too low to have measurable impact. Wilson and Stout (2020) did not distinguish adults from nymphs in sweep net capture relationships.
Another consistent finding in these studies is the importance of infestation timing (relative to panicle development) on levels of quantitative and qualitative damage. Generally speaking, vulnerability to quantitative (yield) losses is greatest at the bloom/anthesis and early milk stages, while incidence of peck is highest when rice stink bug feeding infestations occur during milk and soft dough stages (Patel et al. 2006a, Espino et al. 2007, Awuni et al. 2015b). Patel et al. (2006a), Harper et al. (1993), and Wilson and Stout (2020) found evidence that peck can result from infestations at the hard dough stage, although the latter two studies noted that some of the peck observed may have resulted from uncontrolled bug populations earlier in development. Recently, Cato et al. (2020) conducted field experiments in Arkansas to examine the vulnerability to peck of panicles with 20%, 40%, 60%, 80%, and 100% of their grains at the hard dough stage, and found that much less qualitative damage occurred once panicles reached 60% hard dough.
While field studies provide improved assessments of damage relationships over cage studies, future research should compare sweep net captures from commercial fields and head yield and peck measurements taken by rice mills. There may be some disparity between quality ratings made by researchers and those made by mill personnel or even differences between mills in how quality penalties are enforced (Wilson and Stout 2020).
One final difficulty in developing economic thresholds for rice stink bugs is translating the damage observed in studies to economic losses. Translation of yield losses to economic losses is relatively straightforward for rough rice yields (notwithstanding the questions of whether stink bugs actually cause losses in rough rice yields). Assessing economic losses resulting from peck and reduced head yields is more difficult, because the penalties assessed for peck and low head yields can vary from mill to mill and from year to year. Further, small increases in peck can result in large economic impacts as rice quality declines into lower grades according to peck limits (USDA 2009). Thus, the relationship between peck and revenue loss is nonlinear making it difficult to relate economic loss back to sweep net captures.
Taken together, the literature related to economic thresholds for the rice stink bug in rice indicates that reducing the amount of insecticide applied for stink bug management by raising thresholds may be feasible goal. Clearly, however, more studies are needed to characterize the relationship between rice stink bug population densities and damage. Moreover, adoption of standard methods for manipulating stink bug infestations, evaluating qualitative and quantitative damage, and assigning economic impacts to damage will be needed to improve upon currently used action thresholds.
Management
Cultural Practices
Weed management is a recommended practice for reducing O. pugnax populations. This is because, as described above, graminaceous weeds are alternate hosts for rice stink bugs. Presence of weed populations in and around rice fields facilitates early movement of rice stink bug populations into rice fields (Tindall et al. 2004). In addition, the phenology of weedy grass hosts relative to rice plants plays an important role in the abundance of rice stink bug in rice fields. Cherry and Bennett (2005) found that unmowed, headed weeds in Florida harbored greater numbers of rice stink bugs than mowed weeds around rice fields. To demonstrate how the presence of weedy grass hosts affects rice stink bug densities on rice, Tindall et al. (2004) conducted a field study in Louisiana by growing rice in plots as a stand-alone crop or in mixture with barnyard grass. These authors found higher densities of rice stink bugs in mixed plots of rice and barnyard grass compared to plots containing only rice. Moreover, a relationship between the presence of barnyard grass and rice stink bug numbers was established. Presence of 10–23 weeds/m2 during the milk stage and 1 weed/m2 at later stages of grain development was associated with an increase in 1 rice stink bug per 7 m2 plot and 1% peck, respectively (Tindall et al. 2005). Hence, weed management either using herbicides or mowing weed grasses before flowering during early and late stages of rice crop development is advantageous for reducing stink bug damage (Tindall et al. 2005, Awuni et al. 2015a). Consistent with the above work, another study demonstrated that conventional tillage compared to minimum tillage resulted in lower densities of O. pugnax in sorghum, probably because, in the latter fields, stink bugs were sustained on weed hosts (Chilcutt and Matocha 2007).
Host Plant Resistance
The use of resistant varieties against the rice stink bug is an under-explored tactic. In the past, screenings of rice lines for rice stink bug damage were conducted in fields. None of the tested rice cultivars had high levels of resistance to rice stink bug (Nilakhe 1976b, Bernhardt et al. 2004). However, relative levels of resistance among different cultivars were established and some conclusions were drawn. In general, short- and medium-grain varieties were more damaged by rice stink bug relative to long-grain varieties. The proportion of pecky kernels was also higher in medium grain varieties than in long grain varieties in Arkansas (Bernhardt et al. 2004). Very early maturing and early maturing varieties of rice pass through the grain-filling stages more quickly than late maturing varieties, and as a result the former sustained less damage than latter. In addition, nymphal development and subsequent survival to adult stage on rapidly maturing rice varieties may be affected because the time from grain filling to grain maturity is shorter. Nymphs may not be able to successfully complete development, which under field conditions typically takes approximately 3 wk (Blackman and Stout 2017).
Nilakhe (1976b) attempted to document antibiosis among several rice cultivars. On each rice line, four panicles were selected and two first instars were reared until their emergence as adults. In the first experiment, nymphal development time was prolonged by as much as 4 d on resistant rice lines including PI 247949, CI 8292, CI 8927, and PI 242804 relative to the susceptible rice line ‘Starbonnet’. In the second experiment, nymphs that fed on the susceptible check, ‘Saturn’, emerged as adults 4 d earlier than those reared on rice line PI 202994.
Previous research has documented the emission of volatiles by rice panicles injured by rice stink bug. A study conducted by Singh et al. (2006) in which 20 adult stink bugs were caged on 4 rice panicles for 3 d or 5 d demonstrated that rice stink bug feeding induced the emission of several volatiles, including limonene, methyl-salicylate, and caryophyllene. Further analysis revealed that the resistant cultivar ‘Kaybonnet’ produced greater amounts of limonene compared to the susceptible varieties, ‘Cocodrie’ and ‘Bengal’. Release of limonene and methyl-salicylate may be associated with resistance to rice stink bug. A follow-up study was conducted to determine the attractiveness/repellency of limonene by Singh (2007). It was reported that traps baited with limonene, methyl-salicylate, and combination of limonene and methyl-salicylate captured fewer rice stink bugs compared to unbaited yellow traps.
Recently, a greenhouse study was carried out to document the effects of salicylic acid (SA), a compound involved in plant signaling, on rice stink bug development and growth (de Freitas et al. 2019). When third instars were fed with rice panicles treated with 16mmol/L SA, nymphal development was extended by 1.5 d compared to those reared on untreated plants with no noticeable effects on survival and adult weight, indicating a possible antibiotic or repellant effect of SA. Furthermore, the authors reported that gas chromatography–mass spectrometry analysis of plant volatiles showed that plants treated with 16 mmol/L SA released higher amounts of SA compared to untreated plants. No apparent effect of SA on rice stink bug immatures was found at a lower concentration of 8 mmol/L.
Biological Control
In a small-plot field experiment conducted in Louisiana, Patel et al. (2006b) compared the efficacies of different isolates of Beauveria bassiana Vuillemin against the rice stink bug. Among different isolates tested, isolate LRC28 and RSB isolate (a fungal isolate collected from naturally infested rice stink bug from rice fields) were moderately effective in suppressing densities of nymphs after 7 d of application. However, adults were less susceptible to these isolates. A single application of B. bassiana gave similar levels of control as insecticides. Application of B. bassiana along with chemical insecticide had an additive effect, and was more effective in reducing rice stink bug populations. Beauveria bassiana thus shows promise as a management option against rice stink bug.
A parasitic wasp in the family Scelionidae, Telenomus podisi (Ashmead) (Hymenoptera), has been reported to parasitize rice stink bug eggs (Ingram 1927). Parasitized eggs turn black and eventually fail to hatch. It is an important natural enemy of the rice stink bug and natural suppression of rice stink bug populations by T. podisi is often high. For example, Tillman (2010a), in a multi-year study in corn, found that in corn O. pugnax eggs were exclusively parasitized by T. podisi and parasitism rates reached up to 90%. Moreover, Sudarsono et al. (1992) reported parasitism of rice stink bug by T. podisi on weedy grass hosts in Arkansas and rates of parasitism increased with increases in rice stink bug densities. Parasitism by T. podisi was also reported in rice (Bowling 1963). However, field parasitism rates were usually low, probably because of the sensitivity of T. podisi to insecticides. Prior to implementation of a ban on methyl parathion use for management of O. pugnax in rice, Sudarsono et al. (1992) conducted a field study and demonstrated that methyl parathion increases T. podisi adult mortality, which in turn affected the parasitism rates. At 7 d after insecticide application, parasitism rates in insecticide treated plots were as low as 5% compared to 21% parasitism rates in control plots. In addition, canopy height also influences T. podisi survival and immature T. podisi that were situated 70 cm above water level had lower survival compared to those at 40 cm from water surface (Sudarsono et al. 1992). Other egg parasitoids of O. pugnax include Ooencyrtus anasae (Ashmead) (Hymenoptera: Encyrtidae) (Ingram 1927).
In addition, adult stink bugs are parasitized by tachinid flies, including Beskia aelops (Brauer and Bergenstamm), Gymnosoma spp. and Gymnoclytia spp (Ingram 1927, McPherson and Mohlenbrock 1976). Nilakhe (1974) found that 13% and 17% of non-hibernating adult males and females, respectively, collected from P. urvillei plants around rice fields were parasitized by B. aelops. Most of the parasitized females did not carry eggs. A single fly develops in the abdomen of an adult rice stink bug and when mature exits the host body and pupates. The same study also reported that B. aelops overwinters as larvae in hibernating adult rice stink bugs. Parasitism by B. aelops was higher in overwintering rice stink bug adults. About 23% of rice stink bug adults collected were found to be parasitized by B. aelops.
Predators of rice stink bug include birds such as the red-winged blackbird, Agelaius phoeniceus littoralis (L.) (Passeriformes: Icteridae) (Borkhataria et al. 2012), dragonflies, grasshoppers, and the green tree frog, Hyla cinerea (Garman) (Anura: Hylidae) (Ingram 1927). Nilakhe (1974) conducted a field cage study in Louisiana to determine the potential of grasshoppers, which are often considered pests of rice, as predators of rice stink bugs. The author selected different species of long- and short-horned grasshoppers that are commonly seen in and around rice fields and reported that among several species of grasshoppers, Conocephalus fasciatus fasciatus (De Geer) (Orthoptera: Tettigoniidae), Neoconocephalus sp., Orchelium laticauda (Redtenbacher) (Orthoptera: Tettigoniidae), and Melanoplus differentialis (Thomas) (Orthoptera: Acrididae) consumed rice stink bug egg masses, but the time taken to feed after exposure to rice stink bug egg masses and the number the egg masses consumed differed among the grasshopper species. Moreover, C. fasciatus also fed on rice stink bug nymphs. The study concluded that some grasshopper species eat rice stink bug egg masses and nymphs and caution should be used when applying insecticide to manage grasshoppers. These studies indicate that enhancing natural enemies through biological control tactics could be a promising alternative for management of O. pugnax. However, the effectiveness of these agents in rice might be limited by the fact that most damage to rice is probably done by feeding adults that enter the field after heading rather than by immature rice stink bugs that result from eggs laid after rice heads.
Chemical Control
Application of chemical insecticides is the most widely used strategy to manage O. pugnax populations. The thresholds currently used to initiate insecticide applications were discussed previously. Insecticides that are currently registered for use in Louisiana against O. pugnax are listed in Table 2. Insecticides target both nymphs and adults. Foliar application of pyrethroids, the most common practice, is effective in suppressing rice stink bug populations (Blackman et al. 2015a, Cherry et al. 2018). However, recently it has been reported that some rice stink bug populations in Texas (Miller et al. 2010, Blackman et al. 2015a) and Arkansas (Moldenhauer et al. 2020) were less susceptible to, and difficult to control with, pyrethroids, suggesting incipient resistance. Blackman et al. (2015b) conducted a field study in Louisiana to determine the efficacy of several insecticides against O. pugnax and found that malathion @ 1.5 lb of active ingredient per acre, alpha-cypermethrin, and lambda-cyhalothrin were effective and gave similar levels of control while a low application rate of malathion (0.9 lb of active ingredient per acre) was ineffective.
Insecticides registered for rice stink bug management in Louisiana on rice
| Trade name | Active ingredient | Application rate (fluid ounce/acre) | Class | IRAC mode of actiona |
|---|---|---|---|---|
| Warrior II | Lambda-cyhalothrin | 1.6–2.56 | Pyrethroid | 3 A |
| Proaxis | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Declare | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Fastac EC | Alpha-cypermethrin | 3.2–3.8 | Pyrethroid | 3 A |
| Mustang Maxx | Zeta-cypermethrin | 3.2–4.0 | Pyrethroid | 3 A |
| Sevin 80S | Carbaryl | 1.25–1.88 | Carbamate | 1 A |
| Sevin 4F | 1.0–1.5 quarts/acre | |||
| Tenchu 20SG | Dinotefuran | 7.5–10.5 oz/acre | Neonicotinoid | 4 A |
| Malathion 57% EC | Malathion | 1.0–1.5 Pt/A | Organophosphate | 1 B |
| Trade name | Active ingredient | Application rate (fluid ounce/acre) | Class | IRAC mode of actiona |
|---|---|---|---|---|
| Warrior II | Lambda-cyhalothrin | 1.6–2.56 | Pyrethroid | 3 A |
| Proaxis | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Declare | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Fastac EC | Alpha-cypermethrin | 3.2–3.8 | Pyrethroid | 3 A |
| Mustang Maxx | Zeta-cypermethrin | 3.2–4.0 | Pyrethroid | 3 A |
| Sevin 80S | Carbaryl | 1.25–1.88 | Carbamate | 1 A |
| Sevin 4F | 1.0–1.5 quarts/acre | |||
| Tenchu 20SG | Dinotefuran | 7.5–10.5 oz/acre | Neonicotinoid | 4 A |
| Malathion 57% EC | Malathion | 1.0–1.5 Pt/A | Organophosphate | 1 B |
Table adapted from Louisiana insect pest management guide (Anonymous 2020).
aInsecticide Resistance Committee Mode of Action, 1A & 1B – acetylcholinesterase inhibitor; 3A – sodium channel modulators; 4A – Nicotinic acetylcholine receptor competitive modulators (IRAC 2020).
Insecticides registered for rice stink bug management in Louisiana on rice
| Trade name | Active ingredient | Application rate (fluid ounce/acre) | Class | IRAC mode of actiona |
|---|---|---|---|---|
| Warrior II | Lambda-cyhalothrin | 1.6–2.56 | Pyrethroid | 3 A |
| Proaxis | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Declare | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Fastac EC | Alpha-cypermethrin | 3.2–3.8 | Pyrethroid | 3 A |
| Mustang Maxx | Zeta-cypermethrin | 3.2–4.0 | Pyrethroid | 3 A |
| Sevin 80S | Carbaryl | 1.25–1.88 | Carbamate | 1 A |
| Sevin 4F | 1.0–1.5 quarts/acre | |||
| Tenchu 20SG | Dinotefuran | 7.5–10.5 oz/acre | Neonicotinoid | 4 A |
| Malathion 57% EC | Malathion | 1.0–1.5 Pt/A | Organophosphate | 1 B |
| Trade name | Active ingredient | Application rate (fluid ounce/acre) | Class | IRAC mode of actiona |
|---|---|---|---|---|
| Warrior II | Lambda-cyhalothrin | 1.6–2.56 | Pyrethroid | 3 A |
| Proaxis | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Declare | Gamma-cyhalothrin | 1.28–2.05 | Pyrethroid | 3 A |
| Fastac EC | Alpha-cypermethrin | 3.2–3.8 | Pyrethroid | 3 A |
| Mustang Maxx | Zeta-cypermethrin | 3.2–4.0 | Pyrethroid | 3 A |
| Sevin 80S | Carbaryl | 1.25–1.88 | Carbamate | 1 A |
| Sevin 4F | 1.0–1.5 quarts/acre | |||
| Tenchu 20SG | Dinotefuran | 7.5–10.5 oz/acre | Neonicotinoid | 4 A |
| Malathion 57% EC | Malathion | 1.0–1.5 Pt/A | Organophosphate | 1 B |
Table adapted from Louisiana insect pest management guide (Anonymous 2020).
aInsecticide Resistance Committee Mode of Action, 1A & 1B – acetylcholinesterase inhibitor; 3A – sodium channel modulators; 4A – Nicotinic acetylcholine receptor competitive modulators (IRAC 2020).
The potential for development of resistance in the rice stink bug to pyrethroids, necessitated the introduction of other insecticides with different modes of action for O. pugnax management. Neonicotinoids bind to the acetylcholine site of nicotinic acetylcholine receptors leading to disturbance of neurotransmission and resulting in hyperexcitation, lethargy, paralysis, and eventual death of an insect (IRAC 2020). Because of their systemic activity and ability to transport within the plant, these insecticides are usually effective against piercing and sucking insects. The neonicotinoid dinotefuran was found to be effective against O. pugnax and may have longer residual toxicity compared to pyrethroids (Blackman et al. 2015a). In 2016, dinotefuran was included in the list of insecticides for use against O. pugnax.
Because of short residual toxicity of most of the registered insecticides and high dispersal ability of adult rice stink bugs, a second insecticide application is often recommended 7 d after an initial application, depending on rice stink bug densities and grain development stage. The best time for insecticide application is in the morning before 9 a.m. or late in the evening (after 7 p.m.) when rice stink bugs are most active in rice fields in Arkansas (Rashid et al. 2006, Lorenz et al. 2018). When choosing insecticides, deleterious effects of insecticides on aquaculture and beneficial insects should be taken into consideration, especially in crawfish production regions (Cano et al. 1999, Halstead et al. 2015, Lidova et al. 2019).
Conclusions and Directions for Further Research
The rice stink bug is an important late-season pest of rice in southern United States. Damage is caused by nymphs and adults by feeding on developing rice grains resulting in yield losses and reductions in grain quality, which in turn has a significant economic impact on rice producers. Given the fact that rice stink bug infestations in rice fields occur during a narrow window of time, the primary management tactic of this pest has been foliar application of chemical insecticides. In addition, cultural practices including mowing of weeds and application of herbicides are also practiced to some extent, owing to the positive relationship between weed availability in and around rice fields and rice stink bug population densities. However, overreliance and repeated use of chemical insecticides may have already led to the development of resistance to pyrethroids in populations of rice stink bugs in Texas and Louisiana. Furthermore, chemical insecticides used for controlling rice stink bug, especially pyrethroids, can have a deleterious impact on crawfish production, which is a major issue in areas where cropping systems are diversified. Together, the above factors call for a renewed search for updated management tactics. Host plant resistance, biological control, and attract-and-kill strategies are potential management tactics that need to be explored further. Research conducted in the past on host plant resistance has yielded limited success. However, future applications in this area may benefit from research on novel aspects of rice stink bug interactions. Moreover, the rice stink bug feeds on a variety of weedy hosts. There is a clear effect of weed host on nymphal survival and subsequent adult fecundity and longevity. Differences in amounts of plant primary and secondary metabolites that may act as phagostimulants or feeding deterrents have an influence on rice stink bug feeding. Identifying these compounds in weed hosts may provide insights about secondary metabolites that could influence rice stink bug development. Similar work should be followed up in different rice cultivars. Owing to the higher parasitization rates of rice stink bug by T. podisi in the wild, biological control appears to be promising strategy and research should be conducted to better understand the biology and behavior of T. podisi. However, perhaps an even more fundamental need is elucidation of relationships among stink bug population densities, injury, and damage, which may result in revised thresholds that would allow for improved efficiency of insecticide use.
Research on the rice stink bug has implications not only for southern United States, but also other rice-producing regions of the world. Heteropteran bugs that feed on rice panicles are also a serious issue in Asia and South America posing a global threat. In Japan, mirid bugs, sorghum plant bug, Stenotus rubrovittatus (Matsumura) (Hemiptera: Miridae), and rice leaf bug Trigonotylus caelestialium (Kirkaldy) (Hemiptera: Miridae), are known to attack rice plants and feed on developing grains causing significant economic damage to rice crops (Inagaki et al. 2020). Likewise, O. poecilus in Brazil (Krinski and Foerster 2017) and O. insularis in Central American countries (Zachrisson et al. 2019) are serious pests of rice among several others. Feeding by these stink bugs cause damage comparable to that caused by the three species of Oebalus in the United States, and research on management of the rice stink bug may be applicable to these other pests.
Acknowledgments
This work was supported by funds from the Louisiana State Agricultural Center, USDA National Institute of Food and Agriculture, Hatch project accession No. 1011556 (MJS), and the Louisiana Rice Research Board. Approved for publication by the Director of the Louisiana Agricultural Experiment Station. The manuscript was improved by the comments of two anonymous reviewers.
