Estimation of the Vulnerable Paddy Rate to Control Pecky Rice Damage Caused by <i>Stenotus rubrovittatus</i> and <i>Trigonotylus caelestialium</i>（Hemiptera: Miridae）

The rice leaf bug, Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae), is an important insect pest, causing pecky‐rice damage in Japan. This bug has a multivoltine life cycle and feeds on various species of the Poaceae. The phenology of the host‐plants differs between species and the plant quality of a single host species may change with the seasons. The fitness of the bug may be affected by these seasonal changes in host‐plant quality. In the current study, the effects of such quality changes on adult and nymphal performance were examined using a population of bugs collected in Joetsu, Niigata, Japan. Rearing of newly emerged adults collected from spring to autumn from Italian rye grass, Lolium multiflorum Lam., and southern crabgrass, Digitaria ciliaris (Retz.), showed that body size and performance of adults differed between collection seasons and plant species, indicating that nymphal conditions including host‐plant quality have crucial effects on their fitness. Rearing nymphs from hatching to adult emergence on various field‐collected grasses under laboratory conditions showed that the performance of nymphs depends on the plant species and varies greatly with the season, within a given species. In general, nymphs performed more poorly on most of the plants collected late in the season, but they performed well on some plants unavailable early in the season. Therefore, in T. caelestialium, seasonal and spatial variations are important factors that affect fitness of nymphs and adults, and this suggests that oviposition of diapause eggs in summer is an adaptation to deteriorating food conditions.

Although mating status affects future mating opportunities, the biochemical changes that occur in response to mating are not well understood. This study investigated the effects of mating status on the quantities of sex pheromone components found in whole-body extracts and volatile emissions of females of the rice leaf bug, Trigonotylus caelestialium. When sampled at one of four time points within a 4-day postmating period, females that had copulated with a male had greater whole-body quantities of sex pheromone components than those of virgin females sampled at the same times. The quantities of sex pheromone components emitted by virgin females over a 24-h period were initially high but then steadily decreased, whereas 24-h emissions were persistently low among mated females when measured at three time points within the 4 days after mating. As a result, soon after mating, the mated females emitted less sex pheromones than virgin females, but there were no significant differences between mated and virgin females at the end of the experiment. Thus, postmating reduction in the rate of emission of sex pheromones could explain previously observed changes in female attractiveness to male T. caelestialium.Electronic supplementary materialThe online version of this article (doi:10.1007/s00114-013-1141-3) contains supplementary material, which is available to authorized users.

Many grasses in the subfamily Pooideae form symbioses with Neotyphodium fungal endophytes. This relationship provides a competitive advantage for the host plant in many ways. The endophyte of meadow fescue (Festuca pratensis), Neotyphodium uncinatum, is considered to produce no mammalian toxins, but produces metabolites giving insect resistance and other ecological benefits. To determine the potential of N. uncinatum strains to reduce the development of rice leaf bug (Trigonotylus caelestialium), we investigated the effect of artificial inoculation of Italian ryegrass (Lolium multiflorum) with N. uncinatum on the feeding of T. caelestialium. T. caelestialium larvae significantly preferred endophyte‐free to endophyte‐infected plants. Survival of insects was very high on endophyte‐free plants, but it rapidly declined on infected plants. These results indicate that N. uncinatum‐infected Italian ryegrass has enough resistance to T. caelestialium and it means the control of T. caelestialium may be possible using this endophyte.

Diapause induction in multivoltine insects is an ecophysiological event that is generally triggered by seasonal cues such as photoperiod and temperature. The rice leaf bug, Trigonotylus caelestialium (Kirkaldy), feeds on various Poaceae grasses and produces several generations a year. Previous studies have shown that adults produce diapause and nondiapause eggs under short-day and long-day conditions, respectively. However, there is a distinct mid-summer peak in diapause incidence before an autumnal increase in diapause incidence in the field, which cannot be explained by the laboratory results. The present study was performed to examine the environmental factors affecting the diapause incidence in mid-summer and the adaptive significance of this phenomenon. Seasonal trends in diapause incidence differed significantly among three sites located 150-400 m apart from each other and with different host plants. The suitability of host plants differs depending on species and seasonally. Therefore, the microhabitat difference in diapause trend is believed to be due to the difference in host plants. When field-collected female adults laying diapause eggs in late June were fed a seasonally deteriorating host (the orange foxtail, Alopecurus aequalis Sobol. [Poales: Poaceae]), they kept laying diapause eggs, whereas when fed a suitable host (the wheat, Triticum aestivum L. [Poales: Poaceae]) for 5 d, they changed oviposition mode to lay nondiapause eggs. These results indicate that host-plant suitability affects the oviposition mode of T. caelestialium. Diapause-egg oviposition in mid-summer in T. caelestialium has adaptive significance as a bet-hedging strategy against unpredictable dietary conditions.

Volatiles were extracted from rice plants of various growth stages with solid-phase microextraction (SPME) and analyzed by gas chromatography-mass spectrometry (GC-MS) to identify attractants that cause invasion of the rice leaf bug Trigonotylus caelestialium (Kirkaldy) into paddy fields. The composition of volatile blends produced by rice plants changed with rice development. In addition, volatile blend compositions differed between the panicles and the stems and leaves. The relative geranyl acetone content was high in all plant structures analyzed. In volatiles from whole plants in the fourth-leaf stage and panicles in the full-ripe stage, the relative content of green leaf volatiles (GLVs) was higher than that found in other rice plant structures. In contrast, relative terpene levels emitted from whole plants in the panicle-formation stage and by panicles and stems and leaves in the flowering stage were higher than those of other rice plant structures. However, the type of terpenes found differed between the panicles and the stems and leaves. Relative levels of β-caryophyllene in whole plants in the panicle-formation stage and panicles in the flowering stage were much higher than that in stems and leaves in the flowering stage. Our previous studies demonstrated that the odor from whole plants in the panicle-formation stage and panicles in the flowering stage is attractive to rice leaf bugs. Here, the attractiveness of β-caryophyllene to adult bugs was investigated in olfactometer assays. Adult females were attracted to β-caryophyllene at a concentration of 0.001%, which is approximately equivalent to the concentration produced by flowering rice panicles. However, β-caryophyllene also was present in the odor of whole plants in the fourth-leaf stage and in stems and leaves in the flowering stage. Furthermore, the amounts of this compound emitted from these structures were similar. Therefore, we suggest that the relative abundance of this compound in a volatile blend is important for attractance of the bugs.

The rice leaf bug, Trigonotylus caelestialium (Kirkaldy), is a major species of stink bugs causing pecky rice. Seasonal prevalence of occurrence of this bug on rice plants in paddy fields was investigated by a sweeping method in Niigata Prefecture. The number of adult bugs captured by sweeping increased just after the rice plants reached the heading time, however it decreased quickly thereafter. The density of adults tended to be higher in an extremely early variety and an early variety of rice plant than a medium one. The number of males was more than the number of females, and the numbers fluctuated heavily. The nymphs appeared mainly from the middle to the end of the grain filling period. These nymphs originated from eggs laid by females which invaded the rice plants at the time of heading. The percentage of pecky rice grains tended to be high in the extremely early variety which showed a high hull-cracked rice rate. Most of the pecky rice grains were damaged at the top or suture of the grains. Hull-cracked rice began to appear 10 days after heading time and increased to the maturing stage. Pecky rice grains began to appear 15 days after the heading time. Damage at the top part of the grains did not increase after maturation. On the other hand, grains damaged at the suture increased markedly up to maturing stage.

We investigated the feeding behavior-stimulating properties of starch and related substances, namely, rice starch, soluble starch, amylopectin, and d-glucose, in the mirid bugs Trigonotylus caelestialium (Kirkaldy) and Stenotus rubrovittatus (Matsumura). Using an electrical penetration graph, feeding behaviors were roughly categorized into three distinct processes: test probing, ingestion, and resting. Rice starch strongly stimulated the feeding behavior of S. rubrovittatus at all concentrations tested (10–50%), prompting an increase in ingestion behavior and a decrease in resting behavior. Rice starch stimulated the feeding behavior of T. caelestialium at a concentration of 10%. Soluble starch also elicited feeding-stimulant activity in S. rubrovittatus at all concentrations tested (10–30%), but did not stimulate feeding behavior at any concentration tested in T. caelestialium. Amylopectin, a main component of rice starch, showed feeding-stimulant activity in S. rubrovittatus only at a concentration of 10%. In T. caelestialium, amylopectin did not stimulate ingestion, but did decrease resting behavior. d-Glucose, the building block of amylopectin, stimulated feeding behavior in S. rubrovittatus, leading to an increase in the duration and frequency of ingestion at concentrations of 10% and 10–20%, respectively. These findings indicate that starch is one of the main feeding stimulants for rice-ear bugs, particularly S. rubrovittatus.

We investigated the vegetation management and occurrence of two mirid bugs, Trigonotylus caelestialium（Kirkaldy）（Hemiptera: Miridae）and Stenotus rubrovittatus（Matsumura）（Hemiptera: Miridae）, causing pecky rice, in rice paddy levees over an area measuring 10 ha in Niigata Prefecture, Japan. Mowing and herbicide application were carried out on the levees several times to manage weeds during the growing period of rice. Major poaceous plants on the investigated levees were Poa annua, Alopecurus aequalis, Digitaria ciliaris, and Echinochloa crus-galli. The two mirid bug species existed either separately or together on levees infested with ear-emerged poaceous plants. In July and August, which are important periods for forecasting the two bugs, D. ciliaris was the major plant and occurrence of the two mirid bugs was almost entirely restricted to the levees infested with ear-emerged D. ciliaris. Ears of D. ciliaris vanished after mowing or herbicide application and re-emerged with growth. As a result, the locations of levees infested with ear-emerged D. ciliaris changed over short periods. The observation results were similar over 3 years, and there were no significant changes in weed management, vegetation, and occurrence of the two bugs in the area. In levees infested with ear-emerged D. ciliaris, the spatial distribution pattern of T. caelestialium was aggregated, and that of S. rubrovittatus was even more aggregated. Despite the difference in the distribution, the locations and areas of levees infested with ear-emerged poaceous plants could be used in indices for regionally forecasting the occurrence of the two bugs.

Relationships among Pecky Rice, Hull-Cracked Rice and Rice Leaf Bug, <I>Trigonotylus caelestialium</I> (Heteroptera: Miridae)

The rice leaf bug, Trigonotylus caelestialium (Kirkaldy), is an important species of stink bugs causing pecky rice. Control of this bug with fenitrothion is insufficient in paddy fields of Niigata Prefecture. Therefore, susceptibility to fenitrothion was assayed in populations sampled from seven regions of Niigata Prefecture in 2001 and 2002. LD50 values of five populations ranged from 50.6 to 146.2 μg/g, and these values were remarkably higher than 18.8 μg/g of the most susceptible population tested. I concluded that resistance to fenitrothion developed with continuous applications of fenitrothion.

Establishment of pastures for cattle grazing adjacent to rice crops may increase the abundance of rice pests, because some cultivated grass species are host plants to these insects. In this study, we investigated assemblages of Hemiptera potentially causing pecky rice in paddy fields in Japan, and the effects of converted grasslands on surrounding rice fields. We systematically sampled Hemiptera in five land‐use types, comprising riverside vegetation, rice fields, forage rice paddies, fallow fields and pasture in a fine‐scale agricultural mosaic. We also examined the abundance of the two main rice bug species, in relation to the proportion of pecky rice and distance to pasture. Converted pastures that contained cultivated bahia grass (Paspalum notatum Flügge) and Italian ryegrass (Lolium multiflorum Lam.), had the greatest abundance of three rice bug species; Stenotus rubrovittatus (Matsumura), Trigonotylus caelestialium (Kirkaldy) and Cletus punctiger (Dallas). The percentage of damaged pecky grains was significantly greater in rice fields near pasture (within 200 m) than in those farther away. Our study provides evidence that the main source of rice bugs in agricultural croplands was pasture; and suggests that managing food sources for these insect pests in pastures close to rice paddies could help reduce their detrimental impact on rice crops.

The main hosts and sites of oviposition for the two bugs, Trigonotylus caelestialium (Kirkaldy) (Hemiptera: Miridae) and Stenotus rubrovittatus (Matsumura) (Hemiptera: Miridae), that cause pecky rice were investigated in 24 poaceous plants. Nymphs of T. caelestialium emerged from both spikelets and leaf sheaths, while nymphs of S. rubrovittatus emerged almost exclusively from spikelets. Suitable plants for oviposition by T. caelestialium are Lolium multiflorum, Digitaria violascens and Hordeum murinum, while Poa annua, Anthoxanthum odoratum, Alopecurus aequalis and D. violascens were preferentially used by S. rubrovittatus. There was a greater difference in the number of nymphs emerging from different plants for S. rubrovittatus than for T. caelestialium. This difference may be because T. caelestialium can oviposit on leaf sheaths if the spikelets are not suitable for oviposition, whereas S. rubrovittatus only oviposits on spikelets. Although both bugs oviposited on spikelets, the internal oviposition sites were different. In D. ciliaris, T. caelestialium laid all eggs between the lemma of the first floret and the second floret, whereas S. rubrovittatus laid eggs almost exclusively inside the second floret. In contrast, in P. annua, T. caelestialium laid all eggs inside the florets, whereas S. rubrovittatus laid eggs both between and inside the florets.

Neotyphodium fungal endophytes form mutualistic symbiotic associations with many grasses of the subfamily Pooideae, including important forage and turfgrass species. This relationship provides a competitive advantage to the host plant by increasing abiotic/biotic stress tolerance, such as its resistance to drought, diseases, and insect pests. The insect deterrent effects of endophytes are now receiving attention in Japan, as insect pests growing in meadows are causing problems in adjacent rice paddies. One of the most serious problems is the kernel spotting of rice grains caused by the rice leaf bug, Trigonotylus caelestialium Kirkaldy (Heteroptera: Miridae), which reproduces on Lolium species grown as forage. To determine the potential of Neotyphodium endophytes to reduce the invasion of rice crops by T. caelestialium from adjacent Lolium crops, we carried out choice and no‐choice feeding tests using endophyte‐infected and endophyte‐free clonal perennial ryegrass (Lolium perenne L.) (Poaceae). Our experiments revealed that the presence of the Neotyphodium endophyte strongly deterred the feeding of both first‐instar larvae and adults of T. caelestialium. These results show the potential of Neotyphodium endophytes to reduce the number of T. caelestialium in forage fields and grasslands, and thus to reduce the damage to rice grains caused by this insect pest.

The effects of supplying grains as supplementary food on nymphal development and the fecundity of adults in the rice leaf bug, Trigonotylus caelestialium (Kirkaldy), were investigated under laboratory conditions. The emergence rate of adults was 3.3% when nymphs were reared on rice seedlings alone, while the rate was 93.1–96.7% when nymphs were reared on rice seedlings with wheat grains or hulled rice. As compared with bugs reared on wheat seedlings alone, the developmental periods of nymphs reared on wheat seedlings with wheat grains or hulled rice were shorter, and the forewing length of the emerged adults was longer. The number of eggs produced by females fed on wheat seedlings with grains was 3.3–5.2-fold that of females fed on wheat seedlings alone. It was concluded that grains are very important food for the rice leaf bug, and that grain feeding raises its reproduction rate. It is suggested that the availability of seeds on the host plant affects the development and fecundity of this bug.

Occurrence of White Spots in Rice Caused by Rice Leaf Bug <i>Trigonotylus caelestialium</i>