Myriad tiny insect species take to the air to engage in windborne migration, but entomology also has its 'charismatic megafauna' of butterflies, large moths, dragonflies and locusts. The spectacular migrations of large day-flying insects have long fascinated humankind, and since the advent of radar entomology much has been revealed about high-altitude night-time insect migrations. Over the last decade, there have been significant advances in insect migration research, which we review here. In particular, we highlight: (1) notable improvements in our understanding of lepidopteran navigation strategies, including the hitherto unsuspected capabilities of high-altitude migrants to select favourable winds and orientate adaptively, (2) progress in unravelling the neuronal mechanisms underlying sun compass orientation and in identifying the genetic complex underpinning key traits associated with migration behaviour and performance in the monarch butterfly, and (3) improvements in our knowledge of the multifaceted interactions between disease agents and insect migrants, in terms of direct effects on migration success and pathogen spread, and indirect effects on the evolution of migratory systems. We conclude by highlighting the progress that can be made through inter-phyla comparisons, and identify future research areas that will enhance our understanding of insect migration strategies within an eco-evolutionary perspective.

Many insects undertake long-range seasonal migrations to exploit temporary breeding sites hundreds or thousands of kilometers apart, but the behavioral adaptations that facilitate these movements remain largely unknown. Using entomological radar, we showed that the ability to select seasonally favorable, high-altitude winds is widespread in large day- and night-flying migrants and that insects adopt optimal flight headings that partially correct for crosswind drift, thus maximizing distances traveled. Trajectory analyses show that these behaviors increase migration distances by 40% and decrease the degree of drift from seasonally optimal directions. These flight behaviors match the sophistication of those seen in migrant birds and help explain how high-flying insects migrate successfully between seasonal habitats.

Mass movement of “invisibles” We know a lot about vertebrate migrations globally. However, the majority of animals that live on this planet are invertebrates, and we know very little about their movements. Hu et al. monitored the migration of large and small insects over the southern United Kingdom for a decade. They found that more than a trillion insects move across this region annually. The movement of such a large biomass has considerable impacts on the ecosystems between which the insects migrate. Science , this issue p. 1584

For organisms that fly or swim, movement results from the combined effects of the moving medium - air or water - and the organism's own locomotion. For larger organisms, propulsion contributes significantly to progress but the flow usually still provides significant opposition or assistance, or produces lateral displacement ('drift'). Animals show a range of responses to flows, depending on the direction of the flow relative to their preferred direction, the speed of the flow relative to their own self-propelled speed, the incidence of flows in different directions and the proportion of the journey remaining. We here present a classification of responses based on the direction of the resulting movement relative to flow and preferred direction, which is applicable to a range of taxa and environments. The responses adopted in particular circumstances are related to the organisms' locomotory and sensory capacities and the environmental cues available. Advances in biologging technologies and particle tracking models are now providing a wealth of data, which often demonstrate a striking level of convergence in the strategies that very different animals living in very different environments employ when moving in a flow.

Radar has been used to study insects in flight for over 40 years and has helped to establish the ubiquity of several migration phenomena: dawn, morning, and dusk takeoffs; approximate downwind transport; concentration at wind convergences; layers in stable nighttime atmospheres; and nocturnal common orientation. Two novel radar designs introduced in the late 1990s have significantly enhanced observing capabilities. Radar-based research now encompasses foraging as well as migration and is increasingly focused on flight behavior and the environmental cues influencing it. Migrant moths have been shown to employ sophisticated orientation and height-selection strategies that maximize displacements in seasonally appropriate directions; they appear to have an internal compass and to respond to turbulence features in the airflow. Tracks of foraging insects demonstrate compensation for wind drift and use of optimal search paths to locate resources. Further improvements to observing capabilities, and employment in operational as well as research roles, appear feasible.

Over the past two decades, control efforts have halved malaria cases globally, yet burdens remain high in much of Africa and elimination has not been achieved even where extreme reductions have occurred over many years, such as in South Africa 1,2 . Studies seeking to understand the paradoxical persistence of malaria in areas where surface water is absent for 3-8 months of the year, suggested that certain Anopheles mosquitoes employ long-distance migration 3 . Here, we confirmed this hypothesis by aerial sampling of mosquitoes 40-290 m above ground, providing the first evidence of windborne migration of African malaria vectors, and consequently the pathogens they transmit. Ten species, including the primary malaria vector Anopheles coluzzii, were identified among 235 anophelines captured during 617 nocturnal aerial collections in the Sahel of Mali. Importantly, females accounted for >80% of all mosquitoes collected. Of these, 90% had taken a blood meal before their migration, implying that pathogens will be transported long distances by migrating females. The likelihood of capturing Anopheles species increased with altitude and during the wet seasons, but variation between years and localities was minimal. Simulated trajectories of mosquito flights indicated mean nightly displacements of up to 300 km for 9-hour flight durations. Annually, the estimated numbers of mosquitoes at altitude crossing a 100-km line perpendicular to the winds included 81,000 An. gambiae s.s., 6 million An. coluzzii, and 44 million An. squamosus. These results provide compelling evidence that millions of previously blood-fed, malaria vectors frequently migrate over hundreds of kilometers, and thus almost certainly spread malaria over such distances. Malaria elimination success may, therefore, depend on whether sources of migrant vectors can be identified and

Highlights d Between 1 and 4 billion hoverflies migrate into and out of southern Britain each year d These migrants provide important pest control by consuming 3-10 trillion aphids d They also provide extensive pollination services and longrange pollen transfer d Migrant hoverflies play a vital role due to declines of other beneficial insects

Jason W. 2013 Multi-generational longdistance migration of insects: studying the painted lady butterfly in the Western Palaearctic. Ecography, 36 (4). 474-486. 10.1111/j.1600-0587.2012.07738.x Contact CEH NORA team at noraceh@ceh.ac.ukThe NERC and CEH trademarks and logos ('the Trademarks') are registered trademarks of NERC in the UK and other countries, and may not be used without the prior written consent of the Trademark owner. (up to 60 degrees of latitude). The cycle comprises an annual poleward advance of the 73 populations in spring followed by an equatorward return movement in autumn, with returning 74 individuals potentially flying thousands of kilometres. We show that many long-distance 75 migrants take advantage of favourable winds, moving downwind at high elevation (from 76 some tens of metres from the ground to altitudes over 1,000 m), pointing at strong similarities 77 in the flight strategies used by V. cardui and other migrant Lepidoptera. Our results reveal the 78 highly successful strategy that has evolved in these insects, and provide a useful framework 79 for a better understanding of long-distance seasonal migration in the temperate regions 80 worldwide. 81 82 5