Accelerated and Synchronized Oviposition Induced by Flight of Young Females May Intensify Larval Outbreaks of the Rice Leaf Roller

Physiological management of migration-reproduction trade-offs in energy allocation often includes a package of adaptions referred to as the oogenesis-flight syndrome. In some species, this trade-off may be overestimated, because factors like flight behavior and environmental conditions may mitigate it. In this study, we examined the reproductive consequences induced by different flight scenarios in an economically-important Asian migrant insect, Cnaphalocrocis medinalis. We found that the influences of flight on reproduction are not absolutely positive or negative, but instead depend on the age at which the moth begins flight, flight duration, and how many consecutive nights they are flown. Adult flight on the 1st or 2nd night after emergence, flight for 6 h or 12 h nightly, and flight on the first two consecutive nights after emergence significantly accelerated onset of oviposition or enhanced synchrony of egg-laying. The latter can contribute to subsequent larval outbreaks. However, flight after the 3rd night, flight for 18 h at any age, or flight on more than 3 consecutive nights after adult emergence did not promote reproductive development, and in some scenarios even constrained adult reproduction. These results indicate that there is a migration/reproduction trade-off in C.medinalis, but that it is mitigated or eliminated by flight under appropriate conditions. The strategy of advanced and synchronized oviposition triggered by migratory flight of young females may be common in other migratory insect pests.     

粘虫飞行对生殖及寿命的影响

该文报道了粘虫Mythimna separata（Walker）成虫飞行后产卵、交配及寿命的研究结果。1日龄成虫飞行6 h、12 h、18 h、24 h后的产卵前期均显著短于对照的,其中飞行6 h、12 h的比对照的短2天以上,产卵量均比对照的高。对1～5日龄成虫分别飞行23.5 h后的研究结果表明,1日龄飞行的产卵前期和上述结果相一致。2～4日龄飞行的与对照的没有显著差异,但产卵量则随飞行日龄的延迟而逐渐减少。5日龄飞行的产卵前期显著延长,产卵量已不到对照的一半。所有经过飞行的成虫产卵高峰日比对照的早1天。不同日龄成虫飞行时间、距离与成虫产卵量的关系为：1～3日龄飞行时间、距离长的个体产卵量也高;但4～5日龄的成虫飞行时间与距离越长,其产卵量越少,表现出明显的卵子发生飞行拮抗症(oogenesis-flight syndrome)。除了5日龄飞行的成虫交配率有所下降以外,所有经过飞行的成虫产卵历期、交配率及寿命与对照的没有显著差异。最后,根据这些结果,对粘虫迁飞的起飞时期,迁飞在粘虫生殖、种群动态及成灾规律中的作用进行了讨论。     

Fecundity,longevity and caloric patterns in female Heliothis virescens: Changes with age due to flight and supplemental carbohydrate

Bomb calorimetry, survivorship and fecundity analysis of female moths indicated that feeding on 5% sucrose reduces the impact of flight activity on longevity and oviposition. Flight has only a slight to moderate effect on longevity or reproductive capacity in fed females; but in unfed females, flight significantly decreased longevity and fecundity. By comparisons to unfed or unflown females, it is concluded that female moths use lipids as the primary flight fuel prior to the initiation of oviposition. Once oviposition begins the female increases its usage of carbohydrates as the flight fuel. Older females which are unable to obtain nectar cannot maintain their flight capacity, resulting in decreased reproductive potential. Therefore, nectar quantity, quality, and likelihood of availability can be important factors determining moth longevity and reproductive and flight capacities in the field.     

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.     

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.     

粘虫飞行与产卵的关系

利用昆虫飞行数据微机采集系统对粘虫Mytkimna separata(W&lker)蛾飞行能力的测定结果表明：产卵前,雌蛾的飞行能力随蛾龄的增长而增加;产卵后,以产卵l天后的飞行能力最强,之后随产卵历期延长和产卵量的增加而下降。产卵超过6天或1 200粒的成虫飞行能力已基本丧失。由此认为：粘虫蛾的迁飞是在产卵前进行;成虫的飞行能力与卵巢发育同步,因而在粘虫中可能不存在卵子发生飞行拮抗症。最后对粘虫产卵后仍具有一定飞行能力的生物学意义进行了探讨。     

标记回收法确认我国北方地区草地螟的迁飞

为了证实草地螟Loxostege sticticalis L.（鳞翅目： 螟蛾科）由我国华北越冬区向东北迁飞危害的假说并提供直接的证据, 采用网捕成虫喷雾染料标记释放回收的方法,于2009年越冬代草地螟成虫盛发期间（6月1-4日）分别在内蒙古武川县（41.07°N, 111.42°E）和察右中旗（41.13°N, 112.58°E）的6个标放点共标记当地越冬代草地螟成虫约181万头并自然释放。标记释放后, 在东北、 西北和华北11个草地螟常发省（市、 区）组织各级监测预警部门利用虫情测报灯、 捕虫网和性诱剂诱捕器等多种器械进行回收, 先后于2009年6月7-29日在内蒙古科右中旗、 乌兰浩特、 扎兰屯分别回收到由察右中旗标记释放的成虫9头, 在辽宁省北票市回收到由武川县标记释放的成虫1头。标记释放点至回收点直线距离为725~1 117 km。这是迄今为止世界上确认的草地螟最远迁飞距离。这些证据不仅证实了我国越冬代草地螟成虫能从华北迁往东北危害, 而且为进一步了解草地螟的种群动态规律, 改善草地螟的预测预报技术提供了重要的科学依据。     

Reproduction-flight relationship in the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae)

To evaluate the relationship between reproduction and migratory flight, we examined ovaries, tethered flight, and egg laying in the beet armyworm, Spodoptera exigua (Hübner). Ovarian development in female S. exigua was classified into five stages in relation to the postemergence age of the moths. Oviposition peaked at ovarian stages III and IV. Mating accelerated ovarian development in this species, and thus the mated females developed faster than the virgin moths in ovaries. In virgin adults, flight capacity increased from the first day to the third day after emergence and remained at a high level until the moths were 7 d old. In contrast, the mated moths reached the maximum flight capacity in 2 d after emergence and maintained a high level until the age of 7 d. However, mating status could not influence the flight capacity of the beet armyworm, although there were general differences in flight capacity between virgin and mated adults at the same age. Moreover, significant correlations between the number of eggs laid and the flight capacity were not performed by the mated moths. These results showed that mating status and ovarian development did not seem to influence flight capacity in the beet armyworm, which was not in agreement with the definitions of the oogenesis-flight syndrome observed in many other migratory insects.     

Longevity,flight ability and reproductive performance of the diamondback moth,Plutella xylostella (L.) (Lepidoptera: Yponomeutidae), related to adult body size

Plutella xylostella in the temperate zone shows a clear seasonal change in adult body size. In the laboratory, large and small moths were produced during immature stages at 15°C and 25°C, respectively. These moths were then used to evaluate longevity, age-specific flight ability, flight ability of mated and unmated females, and the influence of flight experience on the subsequent reproductive success. The large moths lived longer and displayed a greater flight ability over 3 weeks. Irrespective of body size, unmated females flew for a longer time than mated females, and flight experience affected their subsequent reproductive success. Females of both sizes mated and laid eggs soon after emergence, without any obvious pre-reproductive period. More flight experience did not delay oviposition, but did reduce egg production. It is likely that large moths with a longer adult life span and greater flight ability are better fitted for long-distance flight and more fecund than small ones. These experimental results may explain why long-distance migration ofP. xylostella is mostly seen during cool seasons, when relatively large moths with long forewing appear in the field.     

Downwind migration of the African army worm moth, Spodoptera exempta, studied by mark-and-capture and by radar

Abstract. 1. About 166,000 African armyworm moths, Spodoptera exempta (Walk.), were marked at an emergence site near Nairobi when they fed at night on trees baited with dyed molasses.
2. Six marked moths were captured in pheromone traps, including one at 90 km after flying for only one night, and another at 147 km.
3. Moth flight trajectories deduced from radar and from marking showed that migration was downwind.
4. During migration, moths become dispersed; hence the high densities that lead to outbreaks must be produced by concentration.
5. Some moths were ready to mate on the same night they completed their long-distance flight.     

Impact of reassociation with a coevolved herbivore on oviposition deterrence in a hostplant

Although selection by herbivores for increased feeding deterrence in hostplants is well documented, selection for increased oviposition deterrence is rarely examined. We investigated chemical mediation of oviposition by the parsnip webworm (Depressaria pastinacella) on its principal hostplant Pastinaca sativa to determine whether ovipositing adults choose hostplants based on larval suitability and whether hostplants experience selection for increased oviposition deterrence. Webworms consume floral tissues and florivory selects for increased feeding deterrents; moths, however, oviposit on leaves of pre-bolting plants. Exclusive use of different plant parts for oviposition and larval feeding suggests oviposition should select for increased foliar deterrents. Recent webworm colonization of New Zealand (NZ) allowed us to assess phenotypic changes in foliar chemicals in response to webworm oviposition. In a common garden experiment, we compared NZ populations with and without a history of infestation from 2004 to 2006 for changes in leaf chemistry in response to oviposition. Three leaf volatiles, cis- and trans-ocimene, and β-farnesene, elicit strong responses in female moth antennae; these compounds were negatively associated with oviposition and are likely oviposition deterrents. Leaf β-farnesene was positively correlated with floral furanocoumarins that deter florivory; greater oviposition on plants with low floral furanocoumarins indicates that moths preferentially oviposit on parsnips most suitable for larval growth. Unlike florivory, high oviposition on leaves did not lower plant fitness, consistent with the fact that NZ parsnip foliar chemistry was unaffected by 3–6 years of webworm infestation. Thus, in this system, selection by ovipositing moths on foliar chemistry is weaker than selection by larvae on floral chemistry.     

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.     

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.     

Effects of larval density on flight potential of the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae)

Tethered-flight techniques were used to investigate the flight potential of 1-d-old adult beet webworm, Loxostege sticticalis L. (Lepidoptera: Pyralidae), reared at densities of1, 10, 20, 30, and 40 larvae per 650-ml jar. Larval density had a significant effect on the flight potential, including total flight duration, distance, average velocity, and longest flight duration. Adults reared at a density of 10 larvae per jar, and those reared in isolation displayed the greatest and poorest flight capacity,respectively, relative to the other density treatments. Larval density also significantly affected length of the preoviposition period. Females with longer preoviposition period usually showed greater flight potential, and preoviposition period was positively correlated with flight potential. Body weight, water content, and triglyceride content of the moths were significantly affected by larval density, whereas glycogen content was not. Triglyceride content of adults reared at the different larval densities corresponded to the observed differences inflight potential, whereas water content and body weight were not related to their flight potential. These results suggest that larval density exerts a significant influence on preoviposition period and triglyceride content, which in turn influence flight potential of adult L. sticticalis.     

Oviposition site selection and effect of meteorological conditions on flight of Eudonia sabulosella (Lepidoptera: Scopariinae) with implications for pasture damage

Abstract

Eudonia sabulosella (Walker) is economically the most important hill country sod webworm in New Zealand. Female moths selected long, sparse pasture cover for oviposition. Adult flight patterns were assessed in relation to meteorological factors (temperature, humidity, rainfall, barometric pressure, wind speed and direction, and cloud cover) as well as lunar cycle phase. Moths were responsive to wind speed and direction, aggregating on slopes from east through south to west (i.e., 180° arc) particularly those of SW orientation, at wind speeds of ≤ 10 km/h. At higher wind speeds adults were confined to leeward slopes only within the 180° arc. Light rain was correlated with increased flight and oviposition. In sites where rainfall coincided with strong winds which confined adults, especially over favourable (long, sparse) pasture types, much oviposition occurred. Grasses in these sites were susceptible to larval sod webworm feeding damage several months later. Pasture management to remove the favoured sward type may therefore constitute an effective means of pest control for E. sabulosella on hill country.     

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.     

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.     

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.     

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.