Seasonal migration to high latitudes results in major reproductive benefits in an insect

Abstract

Little is known of the population dynamics of long-range insect migrants, and it has been suggested that the annual journeys of billions of nonhardy insects to exploit temperate zones during summer represent a sink from which future generations seldom return (the "Pied Piper" effect). We combine data from entomological radars and ground-based light traps to show that annual migrations are highly adaptive in the noctuid moth Autographa gamma (silver Y), a major agricultural pest. We estimate that 10-240 million immigrants reach the United Kingdom each spring, but that summer breeding results in a fourfold increase in the abundance of the subsequent generation of adults, all of which emigrate southward in the fall. Trajectory simulations show that 80% of emigrants will reach regions suitable for winter breeding in the Mediterranean Basin, for which our population dynamics model predicts a winter carrying capacity only 20% of that of northern Europe during the summer. We conclude not only that poleward insect migrations in spring result in major population increases, but also that the persistence of such species is dependent on summer breeding in high-latitude regions, which requires a fundamental change in our understanding of insect migration.

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 compared 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 population increases (t = 1.81, P = 0.104). (E) Total number 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%).

Fig. 2.

Simulated nightly fall migration trajectories for adult Autographa gamma moths modeled to initiate flight from two radar sites in southern England during August 2003 and 2006. Each colored line is the mean trajectory of 100 simulated moths on a single night, taking off at 2000 hours GMT and flying until 0400 hours GMT (or 0600 hours if over the sea at 0400 hours). Different colors represent successive nights of migration (light blue, first night; dark blue, second night; green, third night) across Western Europe; numbers indicate degrees of longitude and latitude. (A) Thirteen migration trajectories in August 2006 from Chilbolton, Hampshire. (B) Seventeen migration trajectories in August 2003 and August 2006 from Rothamsted, Hertfordshire.

Fig. 3.

Population dynamics of Autographa gamma 1976–2009. (A) Observed spring (solid circles) and fall (open circles) mean numbers at UK light traps that sampled 68 consecutive generations. Colored points indicate abundance before emigration from southern winter-breeding grounds (blue) and the United Kingdom (red) predicted by our Bayesian state-space model, assuming no migratory losses between breeding grounds. (B and C) Plots of the net growth rate change on a log scale during summer breeding in the United Kingdom (B) or winter breeding in Africa and the Mediterranean basin (C), in the following year, regressed against log abundance in the current year. If populations are regulated, then it is expected that at high density net growth rate (on a log scale) should be negative (populations decline in size) and conversely at low density net growth should be positive (and populations should increase). The plots and associated analyses show that both populations are regulated by the same density-dependent process (i.e., migration losses in C are density independent and/or low): ANCOVA (n = 32) shows no significant season-by-density interaction (F_1,62 = 1.18, P = 0.281), only season (F_1,63 = 91.125, P < 0.001) and density effects (F_1,63 = 37.863, P < 0.0001). (D and E) Sensitivity test of effect of mortalities during migration, shown as the goodness-of-fit of model predictions to observed moth dynamics (A), assuming different combinations of loss on both migration journeys: (D) fit to UK population; (E) fit to African-Mediterranean population, where white-yellow indicates poorer fit, and red indicates best fit based on normalized root mean-square error.