Seasonal migration to high latitudes results in major reproductive benefits in an insect Jason W. Chapmana,b,1, James R. Bella, Laura E. Burginc, Donald R. Reynoldsa,d, Lars B. Petterssone, Jane K. Hillf, Michael B. Bonsallg, and Jeremy A. Thomasg,h aDepartment of AgroEcology, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, United Kingdom; bEnvironment and Sustainability Institute, University of Exeter, Penryn, Cornwall TR10 9EZ, United Kingdom; cAtmospheric Dispersion Research and Response Group, Met Office, Exeter, Devon EX1 3PB, United Kingdom; dNatural Resources Institute, University of Greenwich, Chatham, Kent ME4 4TB, United Kingdom; eBiodiversity Unit, Department of Biology, Lund University, SE-223 62 Lund, Sweden; fDepartment of Biology, University of York, York YO10 5DD, United Kingdom; gDepartment of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom; and hCentre for Ecology and Hydrology, Wallingford OX10 8BB, United Kingdom Edited by David L. Denlinger, Ohio State University, Columbus, OH, and approved July 23, 2012 (received for review April 30, 2012) Little is known of the population dynamics of long-range insect gamma (the silver Y). This abundant moth is a major pest of migrants, and it has been suggested that the annual journeys of a range of crops, including beet, potato, maize, brassica, and billions of nonhardy insects to exploit temperate zones during legumes, that breeds continuously with five or more generations summer represent a sink from which future generations seldom per year (26). Spring migrants use fast-moving airstreams, 200– return (the “Pied Piper” effect). We combine data from entomo- 1,000 m above ground, to travel ∼300 km northward per night logical radars and ground-based light traps to show that annual to colonize temporary summer-breeding grounds in northern migrations are highly adaptive in the noctuid moth Autographa Europe (22–25), from their winter-breeding grounds in North gamma (silver Y), a major agricultural pest. We estimate that Africa and the Middle East (27–30). This species cannot survive 10–240 million immigrants reach the United Kingdom each spring, the winter in the United Kingdom or similar latitudes in north- but that summer breeding results in a fourfold increase in the ern Europe (31), and all of the evidence indicates that only small abundance of the subsequent generation of adults, all of which remnant populations can survive through the hot and dry sum- emigrate southward in the fall. Trajectory simulations show that mers of its wintering areas (27–30) (Results). There is evidence 80% of emigrants will reach regions suitable for winter breeding that at least some of the progeny of summer breeders embark on in the Mediterranean Basin, for which our population dynamics southward-directed migrations in the fall (22–25), but there is no model predicts a winter carrying capacity only 20% of that of evidence as yet that these migrants regularly reach the winter- northern Europe during the summer. We conclude not only that breeding areas or what proportion of the summer population poleward insect migrations in spring result in major population engages in return migration. Thus, there are two competing hy- increases, but also that the persistence of such species is depen- potheses that could explain the annual recolonization of the dent on summer breeding in high-latitude regions, which requires high-latitude regions by immigrants. The first hypothesis postu- a fundamental change in our understanding of insect migration. lates an absence of returns to winter-breeding regions and that continuous breeding by remnant populations that survive the windborne migration | source-sink dynamics summer in low-latitude refugia is responsible for resupplying the high-latitude regions anew each year (the Pied Piper hypothesis). igration arises when the reproductive benefits accrued from The second hypothesis states that population growth at each end Mmoving exceed those of remaining in the current habitat (1). of the migration route resupplies the opposite breeding area in Numerous insect species, comprising members of several insect each year (the “return migration” hypothesis). orders, migrate poleward from lower-latitude winter habitats each To distinguish between these hypotheses, we used a national spring to exploit temporary resources where they can reproduce network of light traps (32) to quantify intra- and interannual during the summer but are unable to survive over winter (2–9). variation in A. gamma populations at ground level during 1976– Compared with our knowledge of the energetic costs, mortality 2009 and specially developed vertical-looking entomological risks, and reproductive benefits of bird migration (10–16), the radars (9) to quantify the intensity of high-altitude migrations adaptive benefits and population dynamics consequences of insect into and out of the United Kingdom in 2000–2009 (Fig. 1). The migration are poorly understood (6–9). For most migratory insects, radars show that A. gamma moths undergo a period of intense their low-latitude winter habitats are considered to be the major northward migration in spring (May and June), followed by breeding grounds. In fact, some authors have previously suggested greatly reduced randomly orientated flights during midsummer that seasonal poleward shifts to exploit temperate ecosystems (July), and another period of intense southward migration in the represent a population sink from which progeny seldom returned: fall (August and September) (Fig. 2, Fig. S1, and Table S1). We a phenomenon known as the “Pied Piper” effect (17, 18). This therefore restricted analyses of migration intensities to radar notion made little evolutionary sense, however, and has been data collected during the spring and fall journeys. contested (7, 8, 19); moreover, return flights have been observed in many species (5, 7–9, 20–25). However, it is unclear whether high- Results and Discussion latitude breeding results in net reproductive benefits to migrating Summer A. gamma populations in the United Kingdom showed species or whether significant proportions of the progeny produced a pronounced pattern of annual abundance: during 2000–2009, over the summer successfully make it back to regions where they can breed again, and there is no information on population sizes and migration intensities between zones. These are vital issues Author contributions: J.W.C., D.R.R., J.K.H., and J.A.T. designed research; J.W.C. and J.A.T. because billions of insects immigrate annually to, or within, the performed research; J.W.C., J.R.B., L.E.B., L.B.P., and M.B.B. analyzed data; and J.W.C., D.R.R., temperate zone, providing major ecosystem services as well as, in J.K.H., M.B.B., and J.A.T. wrote the paper. some cases, causing serious crop damage and spreading diseases of The authors declare no conflict of interest. humans and their livestock (9). This article is a PNAS Direct Submission. Here we combine analyses of long-term field data, migration 1To whom correspondence should be addressed. E-mail: [email protected]. trajectory simulations, and population dynamic modeling to This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. study these questions in the Palaearctic noctuid moth Autographa 1073/pnas.1207255109/-/DCSupplemental. 14924–14929 | PNAS | September 11, 2012 | vol. 109 | no. 37 www.pnas.org/cgi/doi/10.1073/pnas.1207255109 Downloaded by guest on September 30, 2021 Fig. 1. Seasonal changes in Autographa gamma populations and migrations. (A) Annual variation in the mean nightly flux per square kilometer of high- altitude spring immigrants to the United Kingdom recorded at two radar stations in 2000–2009 com- pared with measurements by 25 light traps of the adult spring populations established at ground level. Mass invasions (open circles) occurred in 2000, 2003, and 2006 (y = 33.78 + 0.00664x, n = 10, F = 19.11, P = 0.002, r2 = 70.5%). (B–D) seasonal changes in the United Kingdom (n = 10 y): (B) mean number recorded at ground level by light traps in spring and fall (Student’s paired t = −5.6, P = 0.000); (C) mean nightly flux per square kilometer of high-altitude spring immigrants and fall emigrants measured by radar (t = −2.53, P =0.032);(D) mean annual pop- ulation increases (t =1.81,P =0.104).(E) Total num- ber of emigrants that migrated southward measured by radar against the estimated total UK A. gamma population each fall (dashed line = 1:1, y =2.231+ 0.714x, n =10,F =23.39,P =0.001,r2 =74.5%). three mass invasion years (2000, 2003, and 2006) had high im- winter in the United Kingdom (or at similar latitudes across − migrant migration fluxes in spring—775,000 ± 15,000 moths km 2 Europe), we conclude that the entire population emigrates an- (mean ± 1 SE), corresponding to an estimated 225–240 million nually toward its winter-breeding grounds. adult A. gamma immigrating into the whole United Kingdom— For the apparent reproductive benefits of high-latitude whereas the other 7 y received roughly one-ninth that number: breeding (fourfold population increase) to be realized, moths are − 88,000 ± 12,000 moths km 2, corresponding to ∼10–40 million dependent upon successful return migrations in the fall. To immigrants (Table S2). This variation correlates closely with light- evaluate these migrations, we used a version of the atmospheric trap monitoring of the size of the population founded at ground dispersion model “Numerical Atmospheric-dispersion Modeling level by these immigrants each spring (Fig. 1A and Table S3). Environment” (NAME) (Methods) that combines the effect of In 2000–2009, each moth arriving in the spring (first genera- wind currents with A. gamma flight behavior [e.g., selection of tion) produced 4.3 ± 0.7 adults in the next (second) UK gener- favorable airstreams and beneficial flight headings (22–25)] to ation (Fig. 1 B and D), with similar (mean = 4.8) seasonal simulate migration pathways of emigrants leaving the United increases occurring over all of the 34 consecutive years for which Kingdom on 30 nights when mass return migrations were detec- we possess light-trap data (Fig.