Synchronized oviposition triggered by migratory flight intensifies larval outbreaks of beet webworm

Identifying the reproductive consequences of insect migration is critical to understanding its ecological and evolutionary significance. However, many empirical studies are seemingly contradictory, making recognition of unifying themes elusive and controversial. The beet webworm, Loxostege sticticalis L. is a long-range migratory pest of many crops in the northern temperate zone from 36 °N to 55 °N, with larval populations often exploding in regions receiving immigrants. In laboratory experiments, we examined (i) the reproductive costs of migratory flight by tethered flight, and (ii) the reproductive traits contributing to larval outbreaks of immigrant populations. Our results suggest that the beet webworm does not initiate migratory flight until the 2nd or 3rd night after emergence. Preoviposition period, lifetime fecundity, mating capacity, and egg hatch rate for adults that experienced prolonged flight after the 2nd night did not differ significantly from unflown moths, suggesting these traits are irrelevant to the severity of beet webworm outbreaks after migration. However, the period of first oviposition, a novel parameter developed in this paper measuring synchrony of first egg-laying by cohorts of post-migratory females, for moths flown on d 3 and 5 of adulthood was shorter than that of unflown moths, indicating a tightened time-window for onset of oviposition after migration. The resulting synchrony of egg-laying will serve to increase egg and subsequent larval densities. A dense population offers potential selective advantages to the individual larvae comprising it, whereas the effect from the human standpoint is intensification of damage by an outbreak population. The strategy of synchronized oviposition may be common in other migratory insect pests, such as locust and armyworm species, and warrants further study.     

不同水稻品种对稻纵卷叶螟生长发育、存活、生殖及飞行能力的影响

系统研究了稻纵卷叶螟在6种不同水稻品种(常规粳稻武育粳3号,杂交粳稻宁粳1号,常规籼稻TN1,杂交籼稻汕优63,超级杂交籼稻两优培九,超级杂交籼粳稻甬优9号)上取食后的发育历期、存活率、卵巢发育进度、繁殖力和飞行能力.结果表明,武育粳3号和宁粳1号能显著延长稻纵卷叶螟未成熟期的发育历期,降低其存活率,延缓卵巢发育进度,降低成虫繁殖率,并提高成虫的飞行能力;不同水稻品种间的影响存在显著差异,其影响从大到小排列为杂交粳稻＞常规粳稻＞常规籼稻＞杂交籼稻＞超级杂交稻.这说明,幼虫期营养对稻纵卷叶螟的生长发育、存活、生殖和飞行能力具有显著影响.     

Relationship of flight and reproduction in beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight syndrome

The beet armyworm, Spodoptera exigua, undertakes long-distance migration. We used flight mills to investigate the interaction between flight and reproduction in this species given the apparent absence of the oogenesis-flight syndrome. This syndrome, common in many migratory insects, is characterized by a suite of traits including migration during the pre-oviposition period followed by a switch to oogenesis. No negative effects of inter-ovipositional flight on lifetime fecundity were observed. Instead, adult reproductive output suffered when female flight was initiated the first day after eclosion and before oviposition, suggesting that migratory flight overlaps with the oviposition period rather than being confined to the pre-oviposition period. Mating status of both females and males had no negative influence on their flight performance except that flight distance and flight duration of 7-day-old mated females were significantly less than in unmated females. Furthermore, the number of eggs produced and mating frequency of females less than 7 days of age were not significantly correlated with flight performance, suggesting reproductive development paralleled and was independent of migratory behavior. This independent relationship between flight and reproduction of adults is consistent with the very short pre-oviposition period in this species, and suggests that resources are partitioned between these activities during pupal development. Together, our results uncovered neither obvious trade-offs nor mutual suppression between flight and reproduction in S. exigua, which indicates the lack of an oogenesis-flight syndrome for coordination of these two energy-intensive processes. We propose a conceptual model of migration for this species based on the current and previous studies.     

The clock gene,period, influences migratory flight and reproduction of the oriental armyworm,Mythimna separata (Walker)

The oriental armyworm, Mythimna separata, is a major long-distance migratory insect pest of grain crops in China and other Asian countries. Migratory flights and reproductive behavior usually occur at night, regulated by a circadian rhythm. However, knowledge about the linkages between adult flight, reproduction, and clock genes is still incomplete. To fill this important gap in our knowledge, a clock gene (designated Msper) was identified and phylogenetic analysis indicated that the encoded protein (MsPER) was highly similar to PER proteins from other insect species. Quantitative RT-PCR assays demonstrated that significantly different spatiotemporal and circadian rhythmic accumulations of mRNA encoding MsPER occurred during development under steady 14 h : 10 h light : dark conditions. The highest mRNA accumulation occurred in adult antennae and the lowest in larvae. Msper was expressed rhythmically in adult antennae, relatively less in photophase and more entering scotophase. Injecting small interference RNA (siRNA) into adult heads effectively knocked down Msper mRNA levels within 72 h. Most siRNA-injected adults reduced their evening flight activity significantly and did not exhibit a normal evening peak of flight activity. They also failed to mate and lay eggs within 72 h. Adult mating behavior was restored to control levels by 72 h post injection. We infer that Msper is a prominent clock gene that acts in regulating adult migratory flight and mating behaviors of M. separata. Because of its influence on migration and mating, Msper may be a valuable gene to target for effective management of this migratory insect.     

Critical Flight Time for Switch from Flight to Reproduction in the Wing Dimorphic Cricket Velarifictorus aspersus

Flight dimorphism has been considered to result from a balance of costs and benefits between flight capability and reproduction. The validity of the hypothesis, however, has been challenged recently. In this study, we examined the effect of flight time on trade-off between flight capability and reproductive development in Velarifictorus aspersus and we found that flight of 5 min did not promote reproductive development of long-winged (LW) adults, but flight of 30, 60, or 120 min could promote reproductive development both in female and male crickets. The results indicate that flight time may serve as a signal for LW V. aspersus to switch from migration to reproduction, and trade-off between flight ability and reproduction may be attenuated when flight time reaches a critical threshold. In addition, rapid reproductive development occurred before dealation when LW insects were allowed to fly for 30 min, which indicates that flight may influence reproductive development directly. Food consumption of short-winged adults was significantly higher than that of unflown LW adults or LW adults with 5 min flight, but similar to that of LW adults with 30, 60, or 120 min flight, suggesting that difference of reproductive development may be positively correlated with their food consumption.     

Effects of age and mated status on flight potential of Helicoverpa armigera (Lepidoptera: Noctuidae)

Abstract The effects of ageing and female mated status on the flight potential of Helicoverpa armigera (Hübner), collected as larvae from a pigeonpea crop in southern India, were investigated using a tethered-flight technique. In non-mated moths fed sugar solution, from the first night after adult eclosion, the durations of both total and longest continuous flight per night increased up to night 4 and remained at this level until at least night 6. Ovarian maturation was rapid with 77% of unmated moths having commenced oviposition by the third night. On the basis of field evidence it is likely that most females would be mated by the third or fourth night, provided plants with nectar or sugary exudates were locally available. In successfully-mated females a 15-fold decrease in total flight duration and a 28-fold decrease in longest continuous flight duration was observed in contrast to non-mated females of similar age. As host plants suitable for adult feeding and oviposition were locally available during the time of feral adult emergence, synchronous pre-reproductive migration was unlikely to occur in the population studied.     

Trade-off between flight and reproduction in the African armyworm moth, Spodoptera exempta

ABSTRACT. The existence of a trade-off between flight and reproduction in the migratory noctuid, Spodoptera exempta (Wlk.), was examined in experiments in which female moths were flown on flight balances and then provided with distilled water or sucrose solution. For individuals flight-tested from the night of eclosion (night 0) through night 1 and fed only distilled water, there was a linear, negative relationship between weight-related fecundity and flight duration. When flight was recorded through night 2, a curvilinear relationship was obtained suggesting that highly active moths suffer a smaller decrease in fecundity than predicted from its rate of decline with increasing flight duration in less persistent fliers. The hypothesis that this reflects an energetically expensive, initial phase of each flight, followed by a less costly, cruising phase is examined. Fecundity was independent of flight duration in females provided with sucrose after flight but was related to moth weight, as it was in all unflown moths. Effects of flight and feeding on longevity and mating frequency are also reported.
There is a clear trade-off between flight and fecundity in S.exempta which is only evident in moths denied access to a source of carbohydrate after flight. The results indicate the importance of nectar sources in the field in allowing restoration of lipid reserves depleted during migratory flight. An important implication of this conclusion is that lipid is the resource limiting to fecundity in this species and not protein as is generally supposed for leaf-feeding insects. This might be expected in highly active species as lipid is the resource for which the energetically expensive functions of flight and reproduction must compete.     

Significance of haemolymph juvenile hormone titer changes in timing of migration and reproduction in adult Oncopeltus fasciatus

Previous studies had shown that both migratory flight and ovarian maturation in Oncopeltus fasciatus were stimulated by juvenile hormone (JH), yet the two behaviors were mutually exclusive. To understand the relationship of this hormone to these behaviors, haemolymph juvenile hormone titers were determined in both sexes of Oncopeltus throughout the adult stage by the Manduca pigmentation bioassay. Animals reared under long day conditions (17L:7D, 24°C) showed an immediate rise in haemolymph titers of JH after adult emergence whereas those reared in a short day photoperiod (12L:12D, 24°C) had a more gradual increase in hormone titers. Migratory flight behavior occurred during periods of intermediate hormone titers while oviposition did not begin until JH titers had reached their peak. It was concluded that lower JH titers normally stimulate flight in the prereproductive adult whereas higher titers are required for complete ovarian development. The corpus allatum in Oncopeltus thus coordinates migration and reproduction in response to the environmental cues of photoperiod, temperature, and food quality.     

Potential Reproductive Advantage of Short-over Long-Winged Adult Males of the Cricket <Emphasis Type="Italic">Velarifictorus ornatus</Emphasis>

A trade-off between flight capability and reproduction is well known in adult females of the wing-dimorphic cricket Velarifictorus ornatus, but it is not clear whether such a trade-off exists in adult males of the species. In the present study, we investigated sexual maturation time, mating frequency, and the fertilization success of spermatophores after sequential mating in long-winged (LW) and short-winged (SW) adult males of V. ornatus to evaluate the potential reproductive advantage of the SW over the LW male morph. We found that the SW males of V. ornatus attained sexual maturity earlier and produced heavier spermatophores during the early stage after adult emergence than their LW counterparts. Additionally, within a 24-h mating period, the SW males showed a higher mating frequency, greater spermatophore weight, and shorter intermating time interval compared with their LW counterparts. Although females copulated with the two male morphs produced eggs of similar size, fertilization success by SW males was significantly higher than by the LW males. These results provide support for a trade-off between dispersal capability and reproduction success in wing-dimorphic males of V. ornatus.     

Regulation of migration in Mythimna separata (Walker) in China: a review integrating environmental, physiological, hormonal, genetic, and molecular factors

Each year the Mythimna separate (Walker), undertakes a seasonal, long-distance, multigeneration roundtrip migration between southern and northern China. Despite its regularity, the decision to migrate is facultative, and is controlled by environmental, physiological, hormonal, genetic, and molecular factors. Migrants take off on days 1 or 2 after eclosion, although the preoviposition period lasts ≈7 d. The trade-offs among the competing physiological demands of migration and reproduction are coordinated in M. separata by the "oogenesis-flight syndrome." Larvae that experience temperatures above or below certain thresholds accompanied by appropriate humidity, short photoperiod, poor nutrition, and moderate density tend to develop into migrants. However, there is a short window of sensitivity within 24 h after adult eclosion when migrants can be induced to switch to reproductive residents if they encounter extreme environmental factors including starvation, low temperature and long photoperiod. Juvenile hormone (JH) titer is low before migration but high titers are associated with termination of migratory behavior and the switch to reproduction. Early release of JH by the corpora allata in environmentally stressed 1-d old adults, otherwise destined by larval conditions to be migrants, switches them to residents. Offspring inherit parental additive genetic effects governing migratory behavior. However, they also retain flexibility in expression of both flight and reproductive life history traits. The insect neuropeptide, allatotropin, which activates corpora allata to synthesize JH, controls adult flight and reproduction. Future research directions to better understand regulation of migration in this species are discussed.     

Warm‐night temperature alters paternal allocation strategy in a North temperate‐zone butterfly

Warming temperatures are greatly impacting wild organisms across the globe. Some of the negative impacts of climate change can be mitigated behaviorally, for example, by changes in habitat and oviposition site choice. Temperatures are reportedly warming faster at night than during the day, yet studies assessing the impacts of increasing night temperature are rare. We used the Finnish Glanville fritillary butterfly (Melitaea cinxia) as study species and exposed adult butterflies of both sexes to warmer night conditions. Under a seminatural outdoor enclosure, we assessed whether females base their oviposition choices primarily on habitat site characteristics (open, suggestive of dry meadows, versus covered by a coarse canopy, suggestive of pastures) or on plant condition (dry vs. lush), and if their choice is altered by the thermal conditions experienced at night. As exposure to warmer environmental conditions is expected to increase resting metabolic rate and potentially reduce life expectancy, we further assessed the fitness implications of warm‐night temperatures. We found that females prefer open sites for oviposition and that females do not switch their oviposition strategy based on the thermal conditions they experienced at night prior to the reproductive event. Exposure to warm nights did not influence female lifespan, but the egg hatching success of their offspring was reduced. In addition, we found that males exposed to warm nights sired larger clutches with higher hatching rate. As warm‐night exposure reduced male lifespan, this may imply a switch in male resource allocation strategy toward increased offspring quality. The present work adds on to the complex implications of climate warming and highlights the importance of the often‐neglected role of males in shaping offspring performance.     

Effects of precocene I and II on flight behaviour in Oncopeltus fasciatus, the migratory milkweed bug

Treatment of newly emerged adult Oncopeltus fasciatus with the corpus allatum inhibitors. 7-methoxy-2,2-dimethyl chromene or 6,7-dimethoxy-2,2-dimethyl chromene (preocene I and II) results in an inhibition of long-term flight (presumed migratory) behaviour in both males and females and inhibition of oögenesis in females. Treatment of reproductive females with precocene briefly stimulates flight behaviour (which ceases in such females as oviposition begins) and then subsequently inhibits it. Oviposition also ceases in such females and oöcyte resorption occurs. Topical application or injections of JH III to precocenetreated animals results in immediate restoration of the tendency to make long tethered flights while corpora cardiaca extract injections, corpora cardiaca implantation, sham implantation, sham injections and sham topical applications were ineffective in restoring prolonged flight behaviour to precocene-treated animals.Restoration of flight by JH III injection was observed within 1 hr after treatment with the hormone. These results indicate that JH is necessary for prolonged flight and presumably migratory behaviour in this species and its stimulatory effect on flight behaviour is immediate. Possible mechanisms of action of the hormone on flight behaviour are discussed.     

Effects of the availability of food and water on reproduction in the African army worm, Spodoptera exempta

ABSTRACT. Female Spodoptera exempta (Walker) (Lepidoptera: Noctuidae) moths require access to water to achieve hydration and maturation of their oocytes if they are to achieve their potential fecundity. For moths provided with water, the main factor limiting fecundity is moth weight. There is some evidence that sucrose in the adult diet can increase fecundity, particularly in lighter moths from a suboptimal larval feeding regime. Moths fed sucrose live longer, but complete oviposition at about the same age as moths provided only with water. Dietary protein and amino acids have no effect on fecundity or longevity. Although- multiple matings are frequent in the laboratory, female S.exempta only need to mate once to complete oviposition. Differences are apparent in the relative contribution of larval and adult feeding to reproduction in Noctuidae. Some species, like S.exempta , require only water to achieve their reproductive potential, while others (e.g. Heliothis spp.) are dependent on sugars in the adult diet. Female S.exempta denied access to water or food until night 3 after eclosion and then provided with water or sucrose, commence oviposition on night 4 and have fecundities comparable with those moths fed from emergence.     

The reproduction-flight syndrome and the inheritance of tethered-flight activity in the cotton-bollworm moth, Heliothis armigera

Abstract. To test the hypothesis that the flight activity of Heliothis armigera (Hiibner) (Lepidoptera: Noctuidae) conforms to the 'oogenesis-fiight syndrome', female moths from India and Malawi were flight tested on nights 2, 4 and 6 after eclosion, using a tethered-flight technique. Maximum flight activity in the Indian strain occurred on night 2, that of the Malawian strain was not significantly different on the three nights of flight. This difference is explained by the Indian females reaching reproductive maturity c . 48 h before the Malawian females. The existence of a 'reproduction-flight syndrome' was confirmed by flight testing males and females of different maturity status on the fourth night after eclosion. Immature moths flew significantly more than did either mature-virgin or mature-mated moths. The inheritance of tethered-flight activity in a late-maturing line of Malawian H. armigera was investigated. Significant estimates of heritability, by offspring on mid-parent regressions, were obtained for both the total flight time (0.39 æ 0.083) and the longest flight (0.15 ± 0.058). The significance of such tethered-flight data to noctuid migration in the field is discussed, and the conclusion drawn that the current experimental design does not index migratory flight satisfactorily.     

A technique for studying flight behaviour of tethered Spodoptera exempta moths

ABSTRACT. A new apparatus was developed for studies on flight behaviour of the African armyworm, Spodoptera exempta (Wlk.), to record the time and duration of all flights continuously for up to several days. A technique for attaching the mounting bracket to the pharate adult before eclosion allowed flight recording to commence within 1–2h of emergence without the need for anaesthesia. Results obtained using the apparatus indicate that migratory flight does not occur on the night of emergence. The time of take-off of tethered moths in the laboratory agrees closely with observations of flight behaviour in the field.     

Effects of larval density and food stress on life‐history traits of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae)

High population density and nutrition restriction can lead to phase variation in morphology and development, and subsequently induce changes in the reaction norms of adult flight in migrant insects. However, response of migratory propensity to such stress in Endopterygote insects, especially in several species of Lepidoptera, remains unclear. In this study, larval and adult developmental responses to crowding and food stress were investigated in the migratory moth, Cnaphalocrocis medinalis (Guenée). A high larval rearing density significantly reduced pupal mass, survival rate and female fecundity. Larvae developed rapidly under crowding conditions, and time to pupation was 2 days earlier than individuals reared alone. By contrast, short‐term starvation and associated compensatory growth prolonged larval duration by 3–4 days and pupal duration by 1–2 days. It also reduced the pupal mass, but showed no detectable effects on female reproductive performance. Both sexes had similar development strategies; however, females seemed to be more sensitive to crowding and food shortage than males. A positive effect was expected if such stress factors acted as cues that triggering a behavioural or physiological shift to a distinct migratory phase. To the contrary, we found no proof that crowding and starvation caused maturation delay in female reproductive development. All treatments did not significantly increase female pre‐oviposition period. Therefore, we concluded that life developmental responses to crowding and food shortage in this species were different. Adult migration propensity was not enhanced under such stress conditions during the larval phase.     

Weight Loading and Reproductive Status Affect the Flight Performance of Pieris napi Butterflies

Weight-induced mobility reductions can have dramatic fitness consequences and winged animals are especially sensitive to the trade-off between mass and locomotion. Data on how natural weight fluctuations influence a flying insect’s ability to take off are scarce. We therefore quantified take-off flight ability in Pieris napi butterflies in relation to reproductive status. Take-off flight ability (velocity and take-off angle) under suboptimal temperature conditions was recorded with a 3D-tracking camera system and was predicted to decrease with relatively larger weight loads. Our results show that relatively larger weight loads generally reduce flight speed in male butterflies and lower take-off angles in females. However, despite having a lower wing loading, mated male butterflies flew slower than unmated males. Our study suggests that retention of weight loads associated with reproduction impairs insect flight performance.     

Increased juvenile hormone levels after long-duration flight in the grasshopper, Melanoplus sanguinipes

Although, in many insects, migration imposes a cost in terms of timing or amount of reproduction, in the migratory grasshopper Melanoplus sanguinipes performance of long-duration flight to voluntary cessation or exhaustion accelerates the onset of first reproduction and enhances reproductive success over the entire lifetime of the insect. Since juvenile hormone (JH) is involved in the control of reproduction in most species, we examined JH titer after long flight using a chiral selective radioimmunoassay. JH levels increased on days 5 and 8 in animals flown to exhaustion on day 4 but not in 1-h or non-flier controls. No difference was seen in the diel pattern of JH titer, but hemolymph samples were taken between 5 and 7 h after lights on. Treatment of grasshoppers with JH-III mimicked the effect of long-duration flight in the induction of early reproduction. The increased JH titer induced by performance of long-duration flight is thus at least one component of flight-enhanced reproduction. To test the possibility that post-flight JH titer increases are caused by adipokinetic hormone (AKH) released during long flights, a series of injections of physiological doses of Lom-AKH I were given to unflown animals to simulate AKH release during long flight. This treatment had no effect on JH titers. Thus, although AKH is released during flight and controls lipid mobilization, it is not the factor responsible for increased JH titers after long-duration flight.     

Transgenic Bt Rice Does Not Challenge Host Preference of the Target Pest of Rice Leaffolder,Cnaphalocrocis medinalis (Lepidoptera: Pyralidae)

Background

Transgenic Bt rice line T2A-1 expresses a synthesized cry2A gene that shows high resistance to Lepidoptera pests, including Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae). Plant volatile orientation cues and the physical characteristics of the leaf surface play key roles in host location or host-plant acceptance of phytophagous insects. These volatile compounds and physical traits may become altered in Bt rice and it is not known whether this influences the behavior of C. medinalis when searching for oviposition sites.

Results

The results of electronic nose analysis showed that the Radar map of Bt rice cultivars was analogous to the non- Bt rice cultivars at each growing stage. PCA analysis was able to partly discriminate between some of the Bt vs. non-Bt rice sensors, but could not to separate Bt cultivars from non-Bt cultivars. The total ion chromatogram between Bt and non-Bt rice cultivars at the seedling, booting and tillering stages were similar and 25 main compounds were identified by GC-MS. For most compounds, there was no significant difference in compound quantities between Bt and non-Bt rice cultivars at equivalent growth stages. The densities of the tubercle papicles and the trichomes on the upper and lower surfaces were statistically equal in Bt and non-Bt rice. The target pest, C. medinalis, was attracted to host rice plants, but it could not distinguish between the transgenic and the isogenic rice lines.

Conclusions

There were no significant differences between the Bt rice line, T2A-1 and the non-Bt rice for volatiles produced or in its physical characteristics and there were no negative impacts on C. medinalis oviposition behavior. These results add to the mounting evidence that Bt rice has no negative impact on the target insect oviposition behavior.