The most remarkable migrants-systematic analysis of the Western European insect flyway at a Pyrenean mountain pass.

In autumn 1950 David and Elizabeth Lack chanced upon a huge migration of insects and birds flying through the Pyrenean Pass of Bujaruelo, from France into Spain, later describing the spectacle as combining both grandeur and novelty. The intervening years have seen many changes to land use and climate, posing the question as to the current status of this migratory phenomenon. In addition, a lack of quantitative data has prevented insights into the ecological impact of this mass insect migration and the factors that may influence it. To address this, we revisited the site in autumn over a 4 year period and systematically monitored abundance and species composition of diurnal insect migrants. We estimate an annual mean of 17.1 million day-flying insect migrants from five orders (Diptera, Hymenoptera, Hemiptera, Lepidoptera and Odonata) moving south, with observations of southward 'mass migration' events associated with warmer temperatures, the presence of a headwind, sunlight, low windspeed and low rainfall. Diptera dominated the migratory assemblage, and annual numbers varied by more than fourfold. Numbers at this single site hint at the likely billions of insects crossing the entire Pyrenean mountain range each year, and we highlight the importance of this route for seasonal insect migrants.

Invasion and spread of the neotropical leafhopper Curtara insularis (Hemiptera: Cicadellidae) in Africa and North America and the role of high-altitude windborne migration in invasive insects.

Invasive insects threaten ecosystem stability, public health, and food security. Documenting newly invasive species and understanding how they reach into new territories, establish populations, and interact with other species remain vitally important. Here, we report on the invasion of the South American leafhopper, Curtara insularis into Africa, where it has established populations in Ghana, encroaching inland at least 350 km off the coast. Importantly, 80% of the specimens collected were intercepted between 160 and 190 m above ground. Further, the fraction of this species among all insects collected was also higher at altitude, demonstrating its propensity to engage in high-altitude windborne dispersal. Its aerial densities at altitude translate into millions of migrants/km over a year, representing massive propagule pressure. Given the predominant south-westerly winds, these sightings suggest an introduction of C. insularis into at least one of the Gulf of Guinea ports. To assess the contribution of windborne dispersal to its spread in a new territory, we examine records of C. insularis range-expansion in the USA. Reported first in 2004 from central Florida, it reached north Florida (Panhandle) by 2008-2011 and subsequently spread across the southeastern and south-central US. Its expansion fits a "diffusion-like" process with 200-300 km long "annual displacement steps"-a pattern consistent with autonomous dispersal rather than vehicular transport. Most "steps" are consistent with common wind trajectories from the nearest documented population, assuming 2-8 hours of wind-assisted flight at altitude. Curtara insularis has been intercepted at US ports and on trucks. Thus, it uses multiple dispersal modalities, yet its rapid overland spread is better explained by its massive propagule pressure linked with its high-altitude windborne dispersal. We propose that high-altitude windborne dispersal is common yet under-appreciated in invasive insect species.

Effects of nocturnal celestial illumination on high-flying migrant insects.

Radar networks hold great promise for monitoring population trends of migrating insects. However, it is important to elucidate the nature of responses to environmental cues. We use data from a mini-network of vertical-looking entomological radars in the southern UK to investigate changes in nightly abundance, flight altitude and behaviour of insect migrants, in relation to meteorological and celestial conditions. Abundance of migrants showed positive relationships with air temperature, indicating that this is the single most important variable influencing the decision to initiate migration. In addition, there was a small but significant effect of moonlight illumination, with more insects migrating on full moon nights. While the effect of nocturnal illumination levels on abundance was relatively minor, there was a stronger effect on the insects' ability to orientate close to downwind: flight headings were more tightly clustered on nights when the moon was bright and when cloud cover was sparse. This indicates that nocturnal illumination is important for the navigational mechanisms used by nocturnal insect migrants. Further, our results clearly show that environmental conditions such as air temperature and light levels must be considered if long-term radar datasets are to be used to assess changing population trends of migrants. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Massive seasonal high-altitude migrations of nocturnal insects above the agricultural plains of East China.

Long-distance migrations of insects contribute to ecosystem functioning but also have important economic impacts when the migrants are pests or provide ecosystem services. We combined radar monitoring, aerial sampling, and searchlight trapping, to quantify the annual pattern of nocturnal insect migration above the densely populated agricultural lands of East China. A total of ~9.3 trillion nocturnal insect migrants (15,000 t of biomass), predominantly Lepidoptera, Hemiptera, and Diptera, including many crop pests and disease vectors, fly at heights up to 1 km above this 600 km-wide region every year. Larger migrants (>10 mg) exhibited seasonal reversal of movement directions, comprising northward expansion during spring and summer, followed by southward movements during fall. This north-south transfer was not balanced, however, with southward movement in fall 0.66× that of northward movement in spring and summer. Spring and summer migrations were strongest when the wind had a northward component, while in fall, stronger movements occurred on winds that allowed movement with a southward component; heading directions of larger insects were generally close to the track direction. These findings indicate adaptations leading to movement in seasonally favorable directions. We compare our results from China with similar studies in Europe and North America and conclude that ecological patterns and behavioral adaptations are similar across the Northern Hemisphere. The predominance of pests among these nocturnal migrants has severe implications for food security and grower prosperity throughout this heavily populated region, and knowledge of their migrations is potentially valuable for forecasting pest impacts and planning timely management actions.

Novel pheromone-mediated reproductive behaviour in the stag beetle, Lucanus cervus.

The iconic European stag beetle (Lucanus cervus) (Coleoptera: Lucanidae) is one of the largest terrestrial beetles in Europe. Due to decreasing population numbers, thought to be a consequence of habitat loss, this beetle has become a near-threatened species across much of Europe, and a reliable monitoring system is required to measure its future population trends. As part of a programme aimed at conserving UK populations, we have investigated the chemical ecology of the beetle, with a view to developing an efficient semiochemical-based monitoring system. Such a scheme will be beneficial not only in the UK but across the European range of the species, where the beetle is of conservation concern. Here, we report on a surprising discovery of a male-produced pheromone, which provokes initial sexual receptivity in females, and which has not been previously identified in the animal kingdom. Furthermore, we assign sex pheromone function to a previously described female-specific compound.

Physiological and behavioral basis of diamondback moth Plutella xylostella migration and its association with heat stress.

BACKGROUND: Migration is a strategy that shifts insects to more favorable habitats in response to deteriorating local environmental conditions. The ecological factors that govern insect migration are poorly understood for many species. Plutella xylostella causes great losses in Brassica vegetable and oilseed crops, and undergoes mass migration. However, the physiological and behavioral basis for distinguishing migratory individuals and the factors driving its migration remain unclear. RESULTS: Daily light trap catches conducted from April to July in a field population of P. xylostella in central China revealed a sharp decline in abundance from late-May. Analysis of ovarian development levels showed that the proportion of sexually immature females gradually increased, while the mating rate decreased, indicating that generations occurring in May mainly resulted from local breeding and that emigration began in late-May. Physiological and behavioral analyses revealed that emigrant populations had a higher take-off proportion, stronger flight capacity and greater energy reserves of triglyceride compared to residents. Furthermore, a gradual increase in temperature from 24 °C to >30 °C during larval development resulted in a significant delay in oogenesis and increased take-off propensity of adults compared with the control treatment reared at a constant temperature of 24 °C. CONCLUSION: Our results provide the physiological and behavioral factors that underpin mass migration in P. xylostella, and demonstrate that exposure to increased temperature increases their migration propensity at the cost of reproductive output. This study sheds light on understanding the factors that influence population dynamics, migratory propensity and reproductive tradeoffs in migratory insects. © 2023 Society of Chemical Industry.

Bat activity correlated with migratory insect bioflows in the Pyrenees.

High altitude mountain passes in the Pyrenees are known to be important migratory hotspots for autumn migrating insects originating from large swathes of northern Europe. In the Pyrenees, prior research has focused on diurnal migratory insects. In this study, we investigate the nocturnal component of the migratory assemblage and ask if this transient food source is also used by bat species. Three seasons of insect trapping revealed 66 species of four different orders, 90% of which were Noctuid moths, including the destructive pest Helicoverpa armigera, otherwise known as the cotton bollworm. Acoustic bat detectors revealed that high activity of Nyctalus spp. and Tadarida teniotis bats were closely synchronized with the arrival of the migratory moths, suggesting this food source is important for both resident and migratory bats to build or maintain energy reserves. Bats of the Nyctalus spp. are likely migrating through the study site using fly-and-forage strategies or stopping over in the area, while resident T. teniotis may be exploiting the abundant food source to build fat stores for hibernation. This study shows that nocturnal migratory insects are abundant in the Pyrenees during autumn and interact during migration, not only with their co-migrant bats but also with resident bat species.

Changing patterns of the East Asian monsoon drive shifts in migration and abundance of a globally important rice pest.

Numerous insects including pests and beneficial species undertake windborne migrations over hundreds of kilometers. In East Asia, climate-induced changes in large-scale atmospheric circulation systems are affecting wind-fields and precipitation zones and these, in turn, are changing migration patterns. We examined the consequences in a serious rice pest, the brown planthopper (BPH, Nilaparvata lugens) in East China. BPH cannot overwinter in temperate East Asia, and infestations there are initiated by several waves of windborne spring or summer migrants originating from tropical areas in Indochina. The East Asian summer monsoon, characterized by abundant rainfall and southerly winds, is of critical importance for these northward movements. We analyzed a 42-year dataset of meteorological parameters and catches of BPH from a standardized network of 341 light-traps in South and East China. We show that south of the Yangtze River during summer, southwesterly winds have weakened and rainfall increased, while the summer precipitation has decreased further north on the Jianghuai Plain. Together, these changes have resulted in shorter migratory journeys for BPH leaving South China. As a result, pest outbreaks of BPH in the key rice-growing area of the Lower Yangtze River Valley (LYRV) have declined since 2001. We show that these changes to the East Asian summer monsoon weather parameters are driven by shifts in the position and intensity of the Western Pacific subtropical high (WPSH) system that have occurred during the last 20 years. As a result, the relationship between WPSH intensity and BPH immigration that was previously used to predict the size of the immigration to the LYRV has now broken down. Our results demonstrate that migration patterns of a serious rice pest have shifted in response to the climate-induced changes in precipitation and wind pattern, with significant consequences for the population management of migratory pests.

Adaptive migratory orientation of an invasive pest on a new continent.

Many species of insects undertake long-range, seasonally reversed migrations, displaying sophisticated orientation behaviors to optimize their migratory trajectories. However, when invasive insects arrive in new biogeographical regions, it is unclear if migrants retain (or how quickly they regain) ancestral migratory traits, such as seasonally preferred flight headings. Here we present behavioral evidence that an invasive migratory pest, the fall armyworm moth (Spodoptera frugiperda), a native of the Americas, exhibited locally adaptive migratory orientation less than three years after arriving on a new continent. Specimens collected from China showed flight orientations directed north-northwest in spring and southwest in autumn, and this would promote seasonal forward and return migrations in East Asia. We also show that the driver of the seasonal switch in orientation direction is photoperiod. Our results thus provide a clear example of an invasive insect that has rapidly exhibited adaptive migratory behaviors, either inherited or newly evolved, in a completely alien environment.

A cold high-pressure system over North China hinders the southward migration of Mythimna separata in autumn.

BACKGROUND: In warm regions or seasons of the year, the planetary boundary layer is occupied by a huge variety and quantity of insects, but the southward migration of insects (in East Asia) in autumn is still poorly understood. METHODS: We collated daily catches of the oriental armyworm (Mythimna separata) moth from 20 searchlight traps from 2014 to 2017 in China. In order to explore the autumn migratory connectivity of M. separata in East China, we analyzed the autumn climate and simulated the autumn migration process of moths. RESULTS: The results confirmed that northward moth migration in spring and summer under the East Asian monsoon system can bring rapid population growth. However, slow southerly wind (blowing towards the north) prevailed over the major summer breeding area in North China (33°-40° N) due to a cold high-pressure system located there, and this severely disrupts the autumn 'return' migration of this pest. Less than 8% of moths from the summer breeding area successfully migrated back to their winter-breeding region, resulting in a sharp decline of the population abundance in autumn. As northerly winds (blowing towards the south) predominate at the eastern periphery of a high-pressure system, the westward movement of the high-pressure system leads to more northerlies over North China, increasing the numbers of moths migrating southward successfully. Therefore, an outbreak year of M. separata larvae was associated with a more westward position of the high-pressure system during the previous autumn. CONCLUSION: These results indicate that the southward migration in autumn is crucial for sustaining pest populations of M. separata, and the position of the cold high-pressure system in September is a key environmental driver of the population size in the next year. This study indicates that the autumn migration of insects in East China is more complex than previously recognized, and that the meteorological conditions in autumn are an important driver of migratory insects' seasonal and interannual population dynamics.

Individual tracking reveals long-distance flight-path control in a nocturnally migrating moth.

Each year, trillions of insects make long-range seasonal migrations. These movements are relatively well understood at a population level, but how individual insects achieve them remains elusive. Behavioral responses to conditions en route are little studied, primarily owing to the challenges of tracking individual insects. Using a light aircraft and individual radio tracking, we show that nocturnally migrating death's-head hawkmoths maintain control of their flight trajectories over long distances. The moths did not just fly with favorable tailwinds; during a given night, they also adjusted for head and crosswinds to precisely hold course. This behavior indicates that the moths use a sophisticated internal compass to maintain seasonally beneficial migratory trajectories independent of wind conditions, illuminating how insects traverse long distances to take advantage of seasonal resources.

Genome-wide transcriptomic changes reveal the genetic pathways involved in insect migration.

Insects are capable of extraordinary feats of long-distance movement that have profound impacts on the function of terrestrial ecosystems. The ability to undertake these movements arose multiple times through the evolution of a suite of traits that make up the migratory syndrome, however the underlying genetic pathways involved remain poorly understood. Migratory hoverflies (Diptera: Syrphidae) are an emerging model group for studies of migration. They undertake seasonal movements in huge numbers across large parts of the globe and are important pollinators, biological control agents and decomposers. Here, we assembled a high-quality draft genome of the marmalade hoverfly (Episyrphus balteatus). We leveraged this genomic resource to undertake a genome-wide transcriptomic comparison of actively migrating Episyrphus, captured from a high mountain pass as they flew south to overwinter, with the transcriptomes of summer forms which were non-migratory. We identified 1543 genes with very strong evidence for differential expression. Interrogation of this gene set reveals a remarkable range of roles in metabolism, muscle structure and function, hormonal regulation, immunity, stress resistance, flight and feeding behaviour, longevity, reproductive diapause and sensory perception. These features of the migrant phenotype have arisen by the integration and modification of pathways such as insulin signalling for diapause and longevity, JAK/SAT for immunity, and those leading to octopamine production and fuelling to boost flight capabilities. Our results provide a powerful genomic resource for future research, and paint a comprehensive picture of global expression changes in an actively migrating insect, identifying key genomic components involved in this important life-history strategy.

Flight Capability and the Low Temperature Threshold of a Chinese Field Population of the Fall Armyworm Spodoptera frugiperda.

The fall armyworm, Spodoptera frugiperda (J. E. Smith), is capable of long-distance migration; thus, evaluation of its flight capability is relevant to the design of monitoring and control strategies for this pest. Previous studies have quantified the flight ability of lab-reared populations under controlled conditions, but less is known about the flight capability of natural populations. In addition, the low temperature threshold for flight in natural populations also needs to be determined. In this study, the flight capability of S. frugiperda adults emerging from field-collected larvae in South China was measured by a flight mill system. The results show that the flight capability of S. frugiperda moths varied greatly between individuals, and that some adults are capable of flying great distances. The longest self-powered flight distance was 116.7 km with a cumulative flight duration of 36.51 h during a 48-h period. Typically, the flight activity of tethered individuals was relatively stable during the first 12 h, indicating that migrating moths can fly through an entire night. Based on the accumulated flight duration in the first 12 h, moths can be clearly divided into two groups (<5 h and ≥5 h flight duration), and 58% of individuals belonged to the latter group with strong migratory tendency. Further, flight activity under low temperature conditions was tested, and the results of a logit generalized linear model indicate that the low temperature flight threshold of S. frugiperda is 13.1 °C under declining temperatures. Our results provide a scientific basis for further elucidating the flight biology and migration mechanism of S. frugiperda.

Male nutritional status does not impact the reproductive potential of female Cnaphalocrocis medinalis moths under conditions of nutrient shortage.

In addition to sperm, some accessory substances transferred to females during copulation act as nuptial gifts by passing on valuable nutrients in many insect species. The nutritional status of the males can thus have a great effect on the mating behavior, fecundity and even the longevity of females. However, little is known about the effect of male nutritional status on the female reproductive traits in migratory insect species, particularly when females experience nutrient shortage and have to choose between reproduction and migration. Here, Cnaphalocrocis medinalis, a migratory rice pest in Asia, was studied to explore this issue. Our results showed that in male moths fed with honey solution, their gonads had higher energy content than gonads of starved males, resulting in increased energy content of the bursa copulatrix of females after mating with fed males. Such females showed increased mating frequency, fecundity and longevity compared to females mating with starved males, indicating that male moths deliver nuptial gifts to females and improve their reproductive performance. However, when females were starved, only about 45% mated, with just a single copulation, regardless of male nutritional status. Starved females showed lower fecundity, and a longer pre-oviposition period (indicating a greater propensity to migrate), compared to fed females. However, copulation still significantly extended their longevity. These results suggest that starved females invest in migration to escape deteriorating habitats, rather than investing the nuptial gift to increased fecundity. Our results further our understanding of the reproductive adaptability of migratory insects under conditions of food stress.

The development of an unsupervised hierarchical clustering analysis of dual-polarization weather surveillance radar observations to assess nocturnal insect abundance and diversity.

Contemporary analyses of insect population trends are based, for the most part, on a large body of heterogeneous and short-term datasets of diurnal species that are representative of limited spatial domains. This makes monitoring changes in insect biomass and biodiversity difficult. What is needed is a method for monitoring that provides a consistent, high-resolution picture of insect populations through time over large areas during day and night. Here, we explore the use of X-band weather surveillance radar (WSR) for the study of local insect populations using a high-quality, multi-week time series of nocturnal moth light trapping data. Specifically, we test the hypotheses that (i) unsupervised data-driven classification algorithms can differentiate meteorological and biological phenomena, (ii) the diversity of the classes of bioscatterers are quantitatively related to the diversity of insects as measured on the ground and (iii) insect abundance measured at ground level can be predicted quantitatively based on dual-polarization Doppler WSR variables. Adapting the quasi-vertical profile analysis method and data clustering techniques developed for the analysis of hydrometeors, we demonstrate that our bioscatterer classification algorithm successfully differentiates bioscatterers from hydrometeors over a large spatial scale and at high temporal resolutions. Furthermore, our results also show a clear relationship between biological and meteorological scatterers and a link between the abundance and diversity of radar-based bioscatterer clusters and that of nocturnal aerial insects. Thus, we demonstrate the potential utility of this approach for landscape scale monitoring of biodiversity.

Diversity, composition, altitude, and seasonality of high-altitude windborne migrating mosquitoes in the Sahel: Implications for disease transmission.

Recent studies have reported Anopheles mosquitoes captured at high-altitude (40-290 m above ground) in the Sahel. Here, we describe this migration modality across genera and species of African Culicidae and examine its implications for disease transmission and control. As well as Anopheles, six other genera-Culex, Aedes, Mansonia, Mimomyia, Lutzia, and Eretmapodites comprised 90% of the 2,340 mosquitoes captured at altitude. Of the 50 molecularly confirmed species (N = 2,107), 33 species represented by multiple specimens were conservatively considered high-altitude windborne migrants, suggesting it is a common migration modality in mosquitoes (31-47% of the known species in Mali), and especially in Culex (45-59%). Overall species abundance varied between 2 and 710 specimens/species (in Ae. vittatus and Cx. perexiguus, respectively). At altitude, females outnumbered males 6:1, and 93% of the females have taken at least one blood meal on a vertebrate host prior to their departure. Most taxa were more common at higher sampling altitudes, indicating that total abundance and diversity are underestimated. High-altitude flight activity was concentrated between June and November coinciding with availability of surface waters and peak disease transmission by mosquitoes. These hallmarks of windborne mosquito migration bolster their role as carriers of mosquito-borne pathogens (MBPs). Screening 921 mosquitoes using pan-Plasmodium assays revealed that thoracic infection rate in these high-altitude migrants was 2.4%, providing a proof of concept that vertebrate pathogens are transported by windborne mosquitoes at altitude. Fourteen of the 33 windborne mosquito species had been reported as vectors to 25 MBPs in West Africa, which represent 32% of the MBPs known in that region and include those that inflict the heaviest burden on human and animal health, such as malaria, yellow fever, dengue, and Rift Valley fever. We highlight five arboviruses that are most likely affected by windborne mosquitoes in West Africa: Rift Valley fever, O'nyong'nyong, Ngari, Pangola, and Ndumu. We conclude that the study of windborne spread of diseases by migrating insects and the development of surveillance to map the sources, routes, and destinations of vectors and pathogens is key to understand, predict, and mitigate existing and new threats of public health.

Hoverflies use a time-compensated sun compass to orientate during autumn migration.

The sun is the most reliable celestial cue for orientation available to daytime migrants. It is widely assumed that diurnal migratory insects use a 'time-compensated sun compass' to adjust for the changing position of the sun throughout the day, as demonstrated in some butterfly species. The mechanisms used by other groups of diurnal insect migrants remain to be elucidated. Migratory species of hoverflies (Diptera: Syrphidae) are one of the most abundant and beneficial groups of diurnal migrants, providing multiple ecosystem services and undergoing directed seasonal movements throughout much of the temperate zone. To identify the hoverfly navigational strategy, a flight simulator was used to measure orientation responses of the hoverflies Scaeva pyrastri and Scaeva selenitica to celestial cues during their autumn migration. Hoverflies oriented southwards when they could see the sun and shifted this orientation westward following a 6 h advance of their circadian clocks. Our results demonstrate the use of a time-compensated sun compass as the primary navigational mechanism, consistent with field observations that hoverfly migration occurs predominately under clear and sunny conditions.

Environmental drivers of annual population fluctuations in a trans-Saharan insect migrant.

Many latitudinal insect migrants including agricultural pests, disease vectors, and beneficial species show huge fluctuations in the year-to-year abundance of spring immigrants reaching temperate zones. It is widely believed that this variation is driven by climatic conditions in the winter-breeding regions, but evidence is lacking. We identified the environmental drivers of the annual population dynamics of a cosmopolitan migrant butterfly (the painted lady Vanessa cardui) using a combination of long-term monitoring and climate and atmospheric data within the western part of its Afro-Palearctic migratory range. Our population models show that a combination of high winter NDVI (normalized difference vegetation index) in the Savanna/Sahel of sub-Saharan Africa, high spring NDVI in the Maghreb of North Africa, and frequent favorably directed tailwinds during migration periods are the three most important drivers of the size of the immigration to western Europe, while our atmospheric trajectory simulations demonstrate regular opportunities for wind-borne trans-Saharan movements. The effects of sub-Saharan vegetative productivity and wind conditions confirm that painted lady populations on either side of the Sahara are linked by regular mass migrations, making this the longest annual insect migration circuit so far known. Our results provide a quantification of the environmental drivers of large annual population fluctuations of an insect migrant and hold much promise for predicting invasions of migrant insect pests, disease vectors, and beneficial species.