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.

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.

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.

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.

The 'migratory connectivity' concept, and its applicability to insect migrants.

Migratory connectivity describes the degree of linkage between different parts of an animal's migratory range due to the movement trajectories of individuals. High connectivity occurs when individuals from one particular part of the migratory range move almost exclusively to another localized part of the migratory range with little mixing with individuals from other regions. Conversely, low migratory connectivity describes the situation where individuals spread over a wide area during migration and experience a large degree of mixing with individuals from elsewhere. The migratory connectivity concept is frequently applied to vertebrate migrants (especially birds), and it is highly relevant to conservation and management of populations. However, it is rarely employed in the insect migration literature, largely because much less is known about the migration circuits of most migratory insects than is known about birds. In this review, we discuss the applicability of the migratory connectivity concept to long-range insect migrations. In contrast to birds, insect migration circuits typically comprise multigenerational movements of geographically unstructured (non-discrete) populations between broad latitudinal zones. Also, compared to the faster-flying birds, the lower degree of control over movement directions would also tend to reduce connectivity in many insect migrants. Nonetheless, after taking account of these differences, we argue that the migratory connectivity framework can still be applied to insects, and we go on to consider postulated levels of connectivity in some of the most intensively studied insect migrants. We conclude that a greater understanding of insect migratory connectivity would be of value for conserving threatened species and managing pests.

Diversity, dynamics, direction, and magnitude of high-altitude migrating insects in the Sahel.

Long-distance migration of insects impacts food security, public health, and conservation-issues that are especially significant in Africa. Windborne migration is a key strategy enabling exploitation of ephemeral havens such as the Sahel, however, its knowledge remains sparse. In this first cross-season investigation (3 years) of the aerial fauna over Africa, we sampled insects flying 40-290 m above ground in Mali, using nets mounted on tethered helium-filled balloons. Nearly half a million insects were caught, representing at least 100 families from thirteen orders. Control nets confirmed that the insects were captured at altitude. Thirteen ecologically and phylogenetically diverse species were studied in detail. Migration of all species peaked during the wet season every year across localities, suggesting regular migrations. Species differed in flight altitude, seasonality, and associated weather conditions. All taxa exhibited frequent flights on southerly winds, accounting for the recolonization of the Sahel from southern source populations. "Return" southward movement occurred in most taxa. Estimates of the seasonal number of migrants per species crossing Mali at latitude 14°N were in the trillions, and the nightly distances traversed reached hundreds of kilometers. The magnitude and diversity of windborne insect migration highlight its importance and impacts on Sahelian and neighboring ecosystems.

Migratory Take-Off Behaviour of the Mongolian Grasshopper Oedaleus asiaticus.

Oedaleus asiaticus is one of the dominant species of grasshoppers in the rangeland on the Mongolian plateau, and a serious pest, but its migratory behavior is poorly known. We investigated the take-off behavior of migratory O. asiaticus in field cages in the inner Mongolia region of northern China. The species shows a degree of density-dependent phase polyphenism, with high-density swarming populations characterized by a brown morph, while low-density populations are more likely to comprise a green morph. We found that only 12.4% of brown morphs engaged in migratory take-off, and 2.0% of green morphs. Migratory grasshoppers took off at dusk, especially in the half hour after sunset (20:00-20:30 h). Most emigrating individuals did not have any food in their digestive tract, and the females were mated but with immature ovaries. In contrast, non-emigrating individuals rarely had empty digestive tracts, and most females were mated and sexually mature. Therefore, it seems clear that individuals prepare for migration in the afternoon by eliminating food residue from the body, and migration is largely restricted to sexually immature stages (at least in females). Furthermore, it was found that weather conditions (particularly temperature and wind speed at 15:00 h) in the afternoon had a significant effect on take-off that evening, with O. asiaticus preferring to take off in warm, dry and calm weather. The findings of this study will contribute to a reliable basis for forecasting migratory movements of this pest.

Adaptive strategies of high-flying migratory hoverflies in response to wind currents.

Large migrating insects, flying at high altitude, often exhibit complex behaviour. They frequently elect to fly on winds with directions quite different from the prevailing direction, and they show a degree of common orientation, both of which facilitate transport in seasonally beneficial directions. Much less is known about the migration behaviour of smaller (10-70 mg) insects. To address this issue, we used radar to examine the high-altitude flight of hoverflies (Diptera: Syrphidae), a group of day-active, medium-sized insects commonly migrating over the UK. We found that autumn migrants, which must move south, did indeed show migration timings and orientation responses that would take them in this direction, despite the unfavourability of the prevailing winds. Evidently, these hoverfly migrants must have a compass (probably a time-compensated solar mechanism), and a means of sensing the wind direction (which may be determined with sufficient accuracy at ground level, before take-off). By contrast, hoverflies arriving in the UK in spring showed weaker orientation tendencies, and did not correct for wind drift away from their seasonally adaptive direction (northwards). However, the spring migrants necessarily come from the south (on warm southerly winds), so we surmise that complex orientation behaviour may not be so crucial for the spring movements.

Linking Small-Scale Flight Manoeuvers and Density Profiles to the Vertical Movement of Insects in the Nocturnal Stable Boundary Layer.

Huge numbers of insects migrate over considerable distances in the stably-stratified night-time atmosphere with great consequences for ecological processes, biodiversity, ecosystem services and pest management. We used a combination of meteorological radar and lidar instrumentation at a site in Oklahoma, USA, to take a new look at the general assistance migrants receive from both vertical and horizontal airstreams during their long-distance flights. Movement in the nocturnal boundary layer (NBL) presents very different challenges for migrants compared to those prevailing in the daytime convective boundary layer, but we found that Lagrangian stochastic modelling is effective at predicting flight manoeuvers in both cases. A key feature for insect transport in the NBL is the frequent formation of a thin layer of fast-moving air - the low-level jet. Modelling suggests that insects can react rapidly to counteract vertical air movements and this mechanism explains how migrants are retained in the jet for long periods (e.g. overnight, and perhaps for several hours early in the morning). This results in movements over much longer distances than are likely in convective conditions, and is particularly significant for the reintroduction of pests to northern regions where they are seasonally absent due to low winter temperatures.

Characterizing animal anatomy and internal composition for electromagnetic modelling in radar entomology.

The use of radar as an observational tool in entomological studies has a long history, and ongoing advances in operational radar networks and radio-frequency technology hold promise for advances in applications such as aerial insect detection, identification and quantification. Realizing this potential requires increasingly sophisticated characterizations of radio-scattering signatures for a broad set of insect taxa, including variability in probing radar wavelength, polarization and aspect angle. Although this task has traditionally been approached through laboratory measurement of radar cross-sections, the effort required to create a comprehensive specimen-based library of scattering signatures would be prohibitive. As an alternative, we investigate the performance of electromagnetic modelling for creating such a database, focusing particularly on the influence of geometric and dielectric model properties on the accuracy of synthesized scattering signatures. We use a published database which includes geometric size measurements and laboratory-measured radar cross-sections for 194 insect specimens. The insect anatomy and body composition were emulated using six different models, and radar cross-sections of each model were obtained through electromagnetic modelling and compared with the original laboratory measurements. Of the models tested, the prolate ellipsoid with an internal dielectric of homogenized chitin and hemolymph mixture best replicates the measurements, providing an appropriate technique for further modelling efforts.

Windborne long-distance migration of malaria mosquitoes in the Sahel.

Over the past two decades efforts to control malaria have halved the number of cases globally, yet burdens remain high in much of Africa and the elimination of malaria has not been achieved even in areas where extreme reductions have been sustained, such as South Africa1,2. Studies seeking to understand the paradoxical persistence of malaria in areas in which surface water is absent for 3-8 months of the year have suggested that some species of Anopheles mosquito use long-distance migration3. Here we confirm this hypothesis through aerial sampling of mosquitoes at 40-290 m above ground level and provide-to our knowledge-the first evidence of windborne migration of African malaria vectors, and consequently of the pathogens that they transmit. Ten species, including the primary malaria vector Anopheles coluzzii, were identified among 235 anopheline mosquitoes that were captured during 617 nocturnal aerial collections in the Sahel of Mali. Notably, females accounted for more than 80% of all of the mosquitoes that we collected. Of these, 90% had taken a blood meal before their migration, which implies that pathogens are probably transported over long distances by migrating females. The likelihood of capturing Anopheles species increased with altitude (the height of the sampling panel above ground level) and during the wet seasons, but variation between years and localities was minimal. Simulated trajectories of mosquito flights indicated that there would be mean nightly displacements of up to 300 km for 9-h flight durations. Annually, the estimated numbers of mosquitoes at altitude that cross a 100-km line perpendicular to the prevailing wind direction included 81,000 Anopheles gambiae sensu stricto, 6 million A. coluzzii and 44 million Anopheles squamosus. These results provide compelling evidence that millions of malaria vectors that have previously fed on blood frequently migrate over hundreds of kilometres, and thus almost certainly spread malaria over these distances. The successful elimination of malaria may therefore depend on whether the sources of migrant vectors can be identified and controlled.

Mass Seasonal Migrations of Hoverflies Provide Extensive Pollination and Crop Protection Services.

Despite the fact that migratory insects dominate aerial bioflows in terms of diversity, abundance, and biomass [1-6], the migration patterns of most species, and the effects of their annual fluxes between high- and low-latitude regions, are poorly known. One important group of long-range migrants that remain understudied is a suite of highly beneficial species of hoverfly in the tribe Syrphini, which we collectively term "migrant hoverflies." Adults are key pollinators [7-10] and larvae are significant biocontrol agents of aphid crop pests [11], and thus, it is important to quantify the scale of their migrations and the crucial ecosystem services they provide with respect to energy, nutrient, and biomass transport; regulation of crop pests; and pollen transfer. Such assessments cannot be made by sporadic observations of mass arrivals at ground level, because hoverflies largely migrate unnoticed high above ground. We used insect-monitoring radars [12] to show that up to 4 billion hoverflies (80 tons of biomass) travel high above southern Britain each year in seasonally adaptive directions. The long-range migrations redistribute tons of essential nutrients (nitrogen [N] and phosphorus [P]) and transport billions of pollen grains between Britain and Europe, and locally produced populations consume 6 trillion aphids and make billions of flower visits. Migrant hoverfly abundance fluctuated greatly between years, but there was no evidence of a population trend during the 10-year study period. Considering that many beneficial insects are seriously declining [7, 10, 13-19], our results demonstrate that migrant hoverflies are key to maintaining essential ecosystem services.

Long-term seasonal forecasting of a major migrant insect pest: the brown planthopper in the Lower Yangtze River Valley.

Rice planthoppers and associated virus diseases have become the most important pests threatening food security in China and other Asian countries, incurring costs of hundreds of millions of US dollars annually in rice losses, and in expensive, environmentally harmful, and often futile control efforts. The most economically damaging species, the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae), 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 interaction of these waves of migrants and synoptic weather patterns, driven by the semi-permanent western Pacific subtropical high-pressure (WPSH) system, is of critical importance in forecasting the timing and intensity of immigration events and determining the seriousness of subsequent planthopper build-up in the rice crop. We analysed a 26-year data set from a standardised light trap network in Southern China, showing that planthopper aerial transport and concentration processes are associated with the characteristics (strength and position) of the WPSH in the year concerned. Then, using N. lugens abundance in source areas and indices of WPSH intensity or related sea surface temperature anomalies, we developed a model to predict planthopper numbers immigrating into the key rice-growing area of the Lower Yangtze Valley. We also demonstrate that these WPSH-related climatic indices combined with early-season planthopper catches can be used to forecast, several months in advance, the severity of that season's N. lugens infestations (the correlation between model predictions and outcomes was 0.59), thus allowing time for effective control measures to be implemented.

Movement Ecology of Pest Helicoverpa: Implications for Ongoing Spread.

The recent introduction and spread of Helicoverpa armigera throughout South America highlight the invasiveness and adaptability of moths in the Helicoverpa genus. Long-range movement in three key members, H. armigera, H. zea, and H. punctigera, occurs by migration and international trade. These movements facilitate high population admixture and genetic diversity, with important economic, biosecurity, and control implications in today's agricultural landscape. This is particularly true for the spread of resistance alleles to transgenic crops expressing Bacillus thuringiensis (Bt) toxins that are planted over vast areas to suppress Helicoverpa spp. The ability to track long-distance movement through radar technology, population genetic markers, and/or long-distance dispersal modeling has advanced in recent years, yet we still know relatively little about the population trajectories or migratory routes in Helicoverpa spp. Here, we consider how experimental and theoretical approaches can be integrated to fill key knowledge gaps and assist management practices.

The movement of small insects in the convective boundary layer: linking patterns to processes.

In fine warm weather, the daytime convective atmosphere over land areas is full of small migrant insects, among them serious pests (e.g. some species of aphid), but also many beneficial species (e.g. natural enemies of pests). For many years intensive aerial trapping studies were the only way of determining the density profiles of these small insects, and for taxon-specific studies trapping is still necessary. However, if we wish to determine generic behavioural responses to air movements shown by small day-migrating insects as a whole, the combination of millimetre-wavelength 'cloud radars' and Doppler lidar now provides virtually ideal instrumentation. Here we examine the net vertical velocities of > 1 million insect targets, relative to the vertical motion of the air in which they are flying, as a succession of fair-weather convective cells pass over the recording site in Oklahoma, USA. The resulting velocity measurements are interpreted in terms of the flight behaviours of small insects. These behaviours are accounted for by a newly-developed Lagrangian stochastic model of weakly-flying insect movements in the convective boundary layer; a model which is consistent with classic characterisations of small insect aerial density profiles. We thereby link patterns to processes.

From Agricultural Benefits to Aviation Safety: Realizing the Potential of Continent-Wide Radar Networks.

Migratory animals provide a multitude of services and disservices-with benefits or costs in the order of billions of dollars annually. Monitoring, quantifying, and forecasting migrations across continents could assist diverse stakeholders in utilizing migrant services, reducing disservices, or mitigating human-wildlife conflicts. Radars are powerful tools for such monitoring as they can assess directional intensities, such as migration traffic rates, and biomass transported. Currently, however, most radar applications are local or small scale and therefore substantially limited in their ability to address large-scale phenomena. As weather radars are organized into continent-wide networks and also detect "biological targets," they could routinely monitor aerial migrations over the relevant spatial scales and over the timescales required for detecting responses to environmental perturbations. To tap these unexploited resources, a concerted effort is needed among diverse fields of expertise and among stakeholders to recognize the value of the existing infrastructure and data beyond weather forecasting.