The effects of climate warming on the migratory status of early summer populations of Mythimna separata (Walker) moths: A case‐study of enhanced corn damage in central‐northern China, 1980–2016

Mythimna separata (Walker) moths captured in light traps were monitored in Luohe, central‐northern China, from 1980 to 2016. Annual average temperature recorded an increase of 0.298°C/10 years in this region in the period. Our results indicate that a rising April and May average temperature and earlier occurrences of days recording the highest day temperature (30°C) caused an advanced peak and increasing proportion of high ovarian development levels of first‐generation females in earlier summers. Results using Johnson's formulation of “oogenesis‐flight syndrome” indicate that increasing sexual maturity proportion has resulted in more emigrant individuals in the local first‐generation moth becoming residents, and then increased individuals rapidly in the local second‐generation moth since 2006. Consequences of this action have a boom in corn damage since 2007 in this region. Advanced peak dates of the first and second‐generation moth revealed the same response to increasing average monthly temperatures in the monitoring period. Increasing temperatures, the average May temperature exceeds or equal to 22°C, during the early 2000's may represent a physiological threshold for M. separata development. Our results suggest that climate warming may impact M. separata migratory status and cause a problem of crop production in this region.     

Effect of temperature and photoperiod on the calling behaviour of a migratory insect, the oriental armyworm Mythimna separata

Abstract The pre-calling period (PCP), between emergence and first release of pheromone, determines the number of nights over which female Mythimna separata (Walker) (Lepidoptera: Noctuidae) can express their migratory potential. In its seasonal migrations in eastern Asia, this armyworm penetrates to latitudes at which it is unable to over-winter but at which reliable photoperiodic and temperature cues anticipate the deterioration of conditions. The effect of these environmental factors on PCP was examined in moths descended from samples collected in Nanjing (32^oN) during the summer migration. Under LD 14:10h, a reduction in temperature, from 23^oC during larval development to 18^oC from 24 h after pupation, resulted in a twofold increase in PCP compared with insects held at 23^oC. At 23^oC, short days (LD 12:12 h) extended PCP but the magnitude of the response was increased under a regime of decreasing photoperiod, from LD 15:9h, to LD 12:12 h through larval, pupal and adult development. Further experiments demonstrated that the response depended on a decrease in photoperiod from pre-pupal stage to adult emergence (the pupal period is spent below ground). A reduction of 50–60min over the 13–15 day pupal period at 23^oC was effective. The significance of decreasing photoperiods, irrespective of absolute levels, as a cue for species whose migrations traverse substantial ranges of latitude is considered and the results are discussed in relation to the genetic determination of PCP in M.separata and to its seasonal migrations in eastern China.     

Adcyap1 polymorphism covaries with breeding latitude in a Nearctic migratory songbird,the Wilson's warbler (Cardellina pusilla)

Understanding the genetic background of complex behavioral traits, showing multigenic control and extensive environmental effects, is a challenging task. Among such traits, migration is known to show a large additive genetic component. Yet, the identification of specific genes or gene regions explaining phenotypic variance in migratory behavior has received less attention. Migration ultimately depends on seasonal cycles, and polymorphism at phenological candidate genes may underlie variation in timing of migration or other aspects of migratory behavior. In this study of a Nearctic–Neotropical migratory songbird, the Wilson's warbler (Cardellina pusilla), we investigated the association between polymorphism at two phenological candidate genes, Clock and Adcyap1, and two aspects of the migratory phenotype, timing of spring migration through a stopover site and inferred latitude of the breeding destination. The breeding destination of migrating individuals was identified using feather deuterium ratio (δ²H), which reliably reflects breeding latitude throughout the species' western breeding range. Ninety‐eight percent of the individuals were homozygous at Clock, and the rare heterozygotes did not deviate from homozygous migration phenology. Adcyap1 was highly polymorphic, and allele size was not significantly associated with migration date. However, Adcyap1 allele size significantly positively predicted the inferred breeding latitude of males but not of females. Moreover, we found a strong positive association between inferred breeding latitude and Adcyap1 allele size in long‐distance migrating birds from the northern sector of the breeding range (western Canada), while this was not the case in short‐distance migrating birds from the southern sector of the breeding range (coastal California). Our findings support previous evidence for a role of Adcyap1 in shaping the avian migratory phenotype, while highlighting that patterns of phenological candidate gene–phenotype associations may be complex, significantly varying between geographically distinct populations and even between the sexes.     

东北地区粘虫的季节性迁飞行为(英文)

粘虫Mythimna separata是我国农业生产上的重要害虫, 为了明确其季节性迁飞行为参数, 本研究采用垂直监测昆虫雷达（vertical-looking radar, VLR）及相关辅助设备的长期自动观测, 结合基于GIS的大区环流和轨迹模拟, 调查分析了2005年东北地区粘虫季节性迁飞行为。结果表明： 粘虫在不同季节和夜间不同时间空中飞行高度具有明显差异, 空中飞行行为受气象条件尤其是空中风场影响较大; 春季和秋季主要借助气流运载进行大规模长距离迁飞, 夜间持续飞行时间可达9 h, 多数个体能完成整夜飞行, 春季迁飞高度主要在300~600 m, 秋季飞行高度相对较低主要在300 m以下和400~500 m。夏季雷达回波有明显的成层现象, 最高可达1 000 m, 主要集中在500 m和700 m两个高度层。轨迹分析显示： 5月29日由山东潍坊、 临沂等虫源地起飞的黏虫, 顺西南气流越海迁飞, 6月1日在气旋天气影响下, 在吉林省白城等地降落; 7月中旬主要为当地黏虫受对流天气影响进行短距离迁飞扩散; 9月11日虫源来自内蒙古呼伦贝尔, 顺西北气流向吉林省东南方向迁飞。研究结果为东北地区粘虫的有效防控提供了技术支撑。     

Microsatellite‐based analysis of genetic structure and gene flow of Mythimna separata (Walker) (Lepidoptera: Noctuidae) in China

The oriental armyworm, Mythimna separata, is a serious agricultural pest in China. Seasonal and roundtrip migration has recently led to sudden, localized outbreaks and crop losses. To evaluate genetic differentiation between populations in eastern and western China and elucidate gene flow, the genetic structure of 20 natural populations from nine provinces was examined using seven microsatellite markers. The results indicated high genetic diversity. However, little to moderate (0 < F_ST < 0.15) genetic differentiation was detected, and there was no correlation between genetic distance and geographical distance. Bayesian clustering analysis identified three groups whereas discriminant analysis of principal components identified ten clusters that were considered as two clear‐cut clusters and one admixed group. Gene flow occurred frequently in most population pairs, and an asymmetrical migration rate was detected in several pairwise population comparisons. The bottleneck test showed that few populations had experienced recent bottlenecks. Correspondingly, large‐scale and long‐distance migration of M. separata has caused low genetic differentiation and frequent gene exchange. Our findings are important for studying genetic evolution and help to improve predictions of M. separata outbreaks in China.     

粘虫产卵前期的遗传特征

从田间采集的粘虫 Mythimna separata (Walker)种群在室内相同条件下饲养时 ,其后代雌蛾的产卵前期有较大程度的分化 ,最短的为 3d,最长的达 8d。通过亲子回归法 (雌性子代和亲本产卵前期的回归分析 )估算的粘虫蛾产卵前期遗传力值为0 .2 899,表明粘虫产卵前期受遗传因素的影响较小。对单雌系的双向选择所产生的选择响应表明 ,在一定的选择压力下 ,选择有利于产卵前期长的个体 ,即产卵前期长的个体进化速度要比短的个体快 ,但连续选择的响应较低。进一步通过家系间交互杂交来研究雌蛾产卵前期的遗传基础表明 ,产卵前期在很大程度上受雄性亲本的影响 ,即可能受 X-性染色体上的基因调控     

Does the onset of sexual maturation terminate the expression of migratory behaviour in moths? A study of the oriental armyworm, Mythimna separata

It is generally accepted that in most insects adults are sexually immature when they initiate migration and that migratory behaviour terminates with the onset of sexual maturation. However, a few studies examining the mating status of field collected moths have suggested that sexually mature individuals may continue migrating, but in these cases it was impossible to completely eliminate the possibility that the mated females captured came from local, non-migrant populations. In this study we examined the ovarian development of Mythimna separata females captured using a vertical pointing searchlight trap on Beihuang Island in the Bohai Gulf, China, a site >40 km from land. Moths were collected from May to October from 2003 to 2008 in order to test the hypothesis that the onset of sexual maturation resulted in the termination of migratory behaviour. While females at the end of the summer had little ovarian development and were unmated, a significant proportion of those migrating northward in the early summer had developed ovaries and often had at least one spermatophore. Given that theses insects were captured while flying up to 500 m above sea level, at a site with no local populations, the findings would not support the hypothesis and suggest that both ovarian development and mating may occur during migration.     

Within night correlations between radar and ground counts of migrating songbirds

ABSTRACT.   Studies comparing numbers of nocturnal migrants in flight with numbers of migrants at stopover sites have produced equivocal results. In 2003, we compared numbers of nocturnal migrants detected by radar to numbers of passerines observed at the Atlantic Bird Observatory in southwestern Nova Scotia, Canada. Numbers of nocturnal migrants detected by radar were positively correlated with numbers of migrants as determined by mist-netting, censuses, and daily estimated totals (daily estimates of birds present based netting and census results and casual observations) the following day. On nights with winds favorable for migration (tailwinds), the peak correlation between ground counts and radar counts the night before occurred just after sunset. On nights with unfavorable winds (headwinds), the correlation increased through the night, with a peak just before sunrise. The patterns of correlation are consistent with a scenario where birds accumulate at the coastline during periods of unfavorable wind, likely because they are not willing to cross a major ecological barrier, the Gulf of Maine. On nights with favorable winds, many birds departed, but some, possibly after testing wind conditions, apparently decided not to cross the Gulf of Maine and returned. Our results suggest that combining data collected using different methods to generate a daily estimated total provides the best estimate of the number of migrants present at a stopover site. Simultaneous studies at multiple locations where different census methods are used, making more effective use of temporal data (both from radar and diurnal counts), will more clearly elucidate patterns of flight behavior by migratory songbirds and the relationship between ground counts and counts of birds aloft.     

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.     

Basal metabolic rate and energetic cost of thermoregulation among migratory and resident blue tits

Metabolic rates may be informative of adaptations to migration or wintering at high latitudes and may therefore be particularly interesting in partial migrants requiring adaptations to both migration and residency. To study the extent of physiological adaptations in migratory and resident blue tits Cyanistes caeruleus during the period of autumn migration in southern Sweden, we measured basal metabolic rate (BMR) and cost of thermoregulation at 0°C (CTR0). In contrast to other migrants en route, migratory blue tits had lower BMR than residents. As migratory blue tits travel extraordinarily slowly on autumn migration and residents suffer from harsher climate and severe competition, residents may need dynamic adjustments that involve larger metabolic costs than migrants. Resident males had lower CTR0 than migrants and resident females. Resident males are socially dominant, which suggests that they have priority of access to food sources during summer and early autumn. They also spend more time on moult, which would give them the time and energy needed for molting into a plumage of higher insulation quality than is possible for migrants and resident females.     

Molecular characterization of DNA methyltransferase 1 and its role in temperature change of armyworm Mythimna separata Walker

DNA methylation refers to the addition of cytosine residues in a CpG context (5′-cytosine-phosphate-guanine-3′). As one of the most common mechanisms of epigenetic modification, it plays a crucial role in regulating gene expression and in a diverse range of biological processes across all multicellular organisms. The relationship between temperature and DNA methylation and how it acts on the adaptability of migratory insects remain unknown. In the present work, a 5,496 bp full-length complementary DNA encoding 1,436 amino acids (named MsDnmt1) was cloned from the devastating migratory pest oriental armyworm, Mythimna separata Walker. The protein shares 36.8–84.4% identity with other insect Dnmt1 isoforms. Spatial and temporal expression analysis revealed that MsDnmt1 was highly expressed in adult stages and head tissue. The changing temperature decreased the expression of MsDnmt1 in both high and low temperature condition. Besides, we found that M. separata exhibited the shortest duration time from the last instar to pupae under 36°C environment when injected with DNA methylation inhibitor. Therefore, our data highlight a potential role for DNA methylation in thermal resistance, which help us to understand the biological role adaptability and colonization of migratory pest in various environments.     

Susceptibility of Oriental armyworm,Mythimna separata (Lepidoptera: Noctuidae) larvae and pupae to native entomopathogenic nematodes

The Oriental armyworm, Mythimna separata Walker (Lepidoptera: Noctuidae) is a major pest of cereal crops, and its outbreaks result in complete crop loss. In this study, we tested the pathogenicity and reproductive potential of indigenous entomopathogenic nematodes (EPNs), Heterorhabditis indica Poinar, Karunakar, & David NBAIIH38, Steinernema abbasi Elawad NBAIISa01, S. carpocapsae Weiser NBAIISc05 and S. siamkayai Stock, Somsook and Reid NBAIRS92 against larval and pupal stages of M. separata under laboratory conditions. Steinernema carpocapsae caused significantly greater mortality in second- and fourth-instar larval stages than other EPNs species. Steinernema carpocapsae caused greatest mortality 100% in larval stages and 75% in pupal stages. Significant differences were observed in the lethal concentration values (LC₅₀ and LC₉₀) of EPNs species against different stages of M. separata. Differences in penetration and multiplication in the fourth-instar larval stages of M. separata were observed amongst the EPNs species. However, further studies are needed to reveal the field performance of EPN isolates tested to be included in the IPM programme of M. separata.     

Influence of green light at night on Juvenile hormone in the oriental armyworm Mythimna separata (Lepidoptera: Noctuidae)

The oriental armyworm Mythimna separata is an agricultural insect pest in Eastern Asia. Mythimna separata moths have a high phototactic response to green (520 nm) light. The biological characteristics of insects living under light of a specific wavelength at night can change and, accordingly, Juvenile hormone (JH) levels may be influenced by this light. The present study evaluates changes in the total JH levels at different developmental stages (larvae, pupae and adults) of M. separata reared under green light with different exposure periods at night (or dark period). The results show that, when the exposure time per day of the green light at night is extended, the JH levels in the final‐instar larvae (22 days) and older age pupae (8 days) are significantly reduced, and the JH levels in earlier age pupae (4 days) and adults (3, 6 and 9 days) are significantly increased, compared with groups not exposed to green light. Additionally, the JH level of male moths significantly differs from that of the female moths. We suggest that the JH level of M. separata insects could be regulated by the green light at night (or dark period). The findings of the present study will help to explain the relationship between the light environment and biological characteristics in nocturnal moths.     

Insect migration: Variability and success in a capricious environment

Stochastic effects of climate and weather have a pervasive influence on the induction, performance and evolution of migration. In wing-dimorphic species, their influence on habitat quality, and on rates of development of the migrant itself, maintains variation in responses to environmental cues determining wing-form and migratory behaviour. Migrants flying above their flight boundary layer rely on winds to disperse them across landscapes in which their habitats are distributed. Patterns of distribution of habitat patches, and the influence of changing windspeeds and direction on the displacements of migrants, result in selection for variation in migratory potential at each migration. In subsequent migrations, this variation and stochastic effects of the winds on groundtracks of individual migrants ensure that their destinations ‘sample’ the landscapes they travel over. The extent and resolution of this sampling, by which migrants reach favourable habitats, depend on the components of migratory potential, their mode of inheritance, and genetic correlations between them, as well as on the characteristics of the winds on which they travel.     

Chromosome-level genomes of two armyworms,Mythimna separata and Mythimna loreyi,provide insights into the biosynthesis and reception of sex pheromones

Mythimna separata and Mythimna loreyi are global pests of gramineous cereals, heavily controlled with synthetic insecticides. Here, we generated two high-quality chromosome-level genome assemblies for M. separata (688 Mb) and M. loreyi (683 Mb). Our analysis identified Z and W chromosomes, with few genes and abundant transposable elements (TEs) found on the W chromosome. We also observed a recent explosion of long interspersed nuclear elements (LINEs), which contributed to the larger genomes of Mythimna. The two armyworms diverged ~10.5 MYA, with only three chromosomes have intrachromosomal rearrangements. Additionally, we observed a tandem repeat expansion of α-amylase genes in Mythimna, which may promote the digestion of carbohydrates and exacerbate their damage to crops. Furthermore, we inferred the sex pheromone biosynthesis pathway for M. separata, M. loreyi and Spodoptera frugiperda. We discovered that M. loreyi and S. frugiperda synthesized the same major constituents of sex pheromones through different pathways. Specifically, the double bonds in the dominant sex pheromone components of S. frugiperda were generated by Δ9- and Δ11-desaturase, while they were generated by Δ11-desaturase and chain-shortening reactions in M. loreyi. We also identified pheromone receptor (PR) genes and inferred their corresponding components. These findings provide a better understanding of sex pheromone communication and promote the development of a new pest control strategy involving pheromone traps, which are more effective and environmentally friendly than current strategies.     

Winds at departure shape seasonal patterns of nocturnal bird migration over the North Sea

On their migratory journeys, terrestrial birds can come across large inhospitable areas with limited opportunities to rest and refuel. Flight over these areas poses a risk especially when wind conditions en route are adverse, in which case inhospitable areas can act as an ecological barrier for terrestrial migrants. Thus, within the east-Atlantic flyway, the North Sea can function as an ecological barrier. The main aim of this study was to shed light on seasonal patterns of bird migration in the southern North Sea and determine whether departure decisions on nights of intense migration were related to increased wind assistance. We measured migration characteristics with a radar that was located 18 km off the NW Dutch coast and used simulation models to infer potential departure locations of birds on nights with intense nocturnal bird migration. We calculated headings, track directions, airspeeds, groundspeeds on weak and intense migration nights in both seasons and compared speeds between seasons. Moreover, we tested if departure decisions on intense migration nights were associated with supportive winds. Our results reveal that on the intense migration nights in spring, the mean heading was towards E, and birds departed predominantly from the UK. On intense migration nights in autumn, the majority of birds departed from Denmark, Germany and north of the Netherlands with the mean heading towards SW. Prevailing winds from WSW at departure were supportive of a direct crossing of the North Sea in spring. However, in autumn winds were generally not supportive, which is why many birds exploited positive wind assistance which occurred on intense migration nights. This implies that the seasonal wind regimes over the North Sea alter its migratory dynamics which is reflected in headings, timing and intensity of migration.     

Further perspectives on the breeding distribution of migratory birds: South American austral migrant flycatchers

1. Patterns of distribution of breeding austral migrant tyrant-flycatchers in temperate South America were quantified and analysed in conjunction with a variety of ecological, biogeographical and climatic variables.
2. The pattern of proportion of migratory to total breeding tyrannids was most strongly associated with latitude and two temperature variables, mean temperature of the coldest month and relative annual range of temperature.
3. The strong associations of latitude and temperature with percentage of migrants are consistent with the results of most similar investigations of the breeding distributions of migratory birds, both for migrants breeding in North America and in Europe, but contradict the hypothesis that habitat complexity plays a major role in structuring the proportion of migrants in communities of breeding birds.
4. The consistency of results among studies of migrants on different continents suggests that temperature and latitude, presumably a surrogate for one or more climatic variables, are globally significant factors in the breeding distributions of migratory birds.
5. The results for austral migrant flycatchers are consistent with the hypothesis that the prevalence of migration at any particular locality is ultimately dependent on the abundance of resources in the breeding season and the severity of the winter season, or on the difference in resource levels between summer and winter.     

Reproductive biology of the microtype tachinid fly Zenillia dolosa (Meigen) (Diptera: Tachinidae)

Reproductive biology including mating, adult longevity, fecundity and development of the tachinid fly Zenillia dolosa was investigated for optimizing rearing procedures using Mythimna separata as a host in the laboratory. Females lay microtype eggs containing a first instar larva on food plants of the host and then the eggs must be ingested by the host for parasitization. Mating success was 58.5% with mating duration of 80.7 min. Mating was most successful when day 0–1 females were kept with day 2–4 male flies. Female body size was positively correlated with its fecundity but not with longevity. However, females that survived longer produced more eggs during their lifetime. Parasitoids successfully developed in 4th to 6th instar host larvae. Host instars at the time of parasitoid egg ingestion significantly influenced development time of the immature parasitoid, but did not affect body size of the emerging parasitoid. We suggest that pairing newly emerged females with day 2–4 males should result in higher mating success and using the last instar hosts for parasitization should minimize development time of the parasitoid for rearing.     

Independent evolution of migration on the South American landscape in a long-distance temperate-tropical migratory bird, Swainson's flycatcher (Myiarchus swainsoni)

Aim To understand the evolution of long‐distance temperate–tropical migration in a South American bird, Swainson's flycatcher (Myiarchus swainsoni). Methods A total of 842 base pairs of the mitochondrial DNA genes ATPase 8 and 6 were sequenced from forty‐nine individuals of the M. swainsoni complex from most of its range. Analyses measured the phylogenetic signal in the data, and tools of population genetics, phylogeography and phylogeny were used to interpret the evolution of the bird and its migration on the South American landscape. Results Migratory populations in the M. swainsoni complex are not each other's closest relatives. The migratory subspecies M. s. swainsoni, which breeds in south‐eastern South America, is not closely related to the rest of the complex. The remaining migratory populations of the subspecies M. s. ferocior and two intergrade populations are extremely closely related to non‐migratory populations with which they form a well‐supported clade despite substantial morphological differentiation from each other. Within this clade of migrants and non‐migrants, net divergence across 4000 km of lowland South America is zero and most diversity is distributed among individuals not populations. Mismatch analyses and significant values of Tajima's D and Fu's Fs suggest the clade has undergone a very recent range expansion. Migration and the shifts of breeding distribution that accompanied its evolution evolved twice within what has recently been considered the polytypic species M. swainsoni. Furthermore, these shifts of range probably occurred at very different times as parts of different southward ‘pulses’ of humid, Amazonian taxa. Main conclusions Evolution of temperate‐tropical migration in the M. swainsoni complex has been spatio‐temporally layered on the South American landscape. The analysis cautions that the historical biogeography underlying a single present‐day migration system need not have been driven by a single set of environmental factors operating at one time. We suggest directions for further study of ecology and demography in zones of apparent contact between various migratory and non‐migratory populations.