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

Abstract

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.

Keywords: Lepidoptera; insect migration; painted lady butterfly; population dynamics.

Fig. 1.

Painted lady population data in western Europe. (A) Phenology of painted ladies in Europe showing peaks that correspond to either migrants or local generations. In the Mediterranean region (NE Spain), the light-blue period corresponds to the spring immigration and the dark-blue period to the summer emergence of a locally bred generation. In NW Europe (NL: the Netherlands; Eng & Wal: England and Wales), the light-pink period corresponds to the early-summer immigration and the dark-pink period to the late-summer emergence of a locally bred generation. (B) Log-collated annual index (across all sites in each country) for NE Spain in spring (1 March to 30 May) and summer (1 June to 31 July) and for NW Europe in early summer (15 May to 15 July) and late summer (16 July to 30 September). Abundance indices are expressed on a log scale, with zero reflecting the average for that region and season across all years. See Fig. 4 for the factors explaining years of peak abundance (e.g., 1996, 2003, 2006, 2009, and 2015).

Fig. 2.

Correlations between spring painted lady counts in NE Spain with the NDVI, precipitation, and temperature. Red areas on the maps indicate regions that have positive significant correlations between the variable plotted and spring painted lady counts in NE Spain, while blue areas are negative correlations. See also Fig. 3 and SI Appendix, Fig. S2 for plots of painted lady spring numbers against the winter NDVI. These correlation plots were used to identify the ecoregions that were likely to be important (see delineation of these ecoregions in Fig. 3 and SI Appendix, Fig. S1) and to select the most important variables for the modeling (SI Appendix, Tables S1 and S2).

Fig. 3.

Migration arena of the painted lady. Regions implicated in driving population abundance of painted ladies in the western section of the Afro-Palearctic migratory range, according to the results of our preliminary correlation analyses. Regions labeled and outlined in purple are either potential source areas for winter breeding of painted ladies (“tropical forest,” “West Sudanian Savanna,” “Western Sahel,” “Maghreb,” and “Southern Iberia”) or regions where butterfly monitoring data were collected (green crosses in “NE Spain,” “Netherlands,” and “England & Wales”). Red and pink points superimposed on the map indicate areas with positive significant correlations between January NDVI values and spring painted lady counts in NE Spain, whereas dark- and light-blue points indicate areas with positive significant correlations with February NDVI values. The gray squares represent the “west kernel” (red) and “east kernel” (blue) used in our final models. See SI Appendix, Fig. S1 for a close-up view of the sub-Saharan region and the kernel areas.

Fig. 4.

Schematic representation of some processes modeled in the analysis of the environmental drivers of painted lady migration intensity and population dynamics. The figure provides a summary of key results in understanding the northward migration of painted ladies from West Africa into western Europe. Environmental variables that positively affected population abundance are represented by solid red arrows for direct effects and dashed red arrows for an interaction effect, while variables that negatively affected population abundance are represented by blue arrows. Effects inferred but not directly studied (due to lack of population data in Africa) are indicated by dotted arrows. At the end of the summer breeding season, the European populations embark on a long fall migration back to the African winter-breeding grounds.

Fig. 5.

Simulated migration trajectories across the Sahara Desert. Forward migration trajectories for painted ladies from sub-Saharan West Africa during the spring of three recent years of mass immigration to NW Europe. The 4-d trajectories were started from each 1° × 1° cell (black crosses) in the west kernel of the Savanna/Sahel region: red lines show trajectories starting from the southern subregion of the kernel, while orange lines show trajectories from the northern subregion on the Sahel/Sahara border. Trajectory calculations involved daytime flight only for four successive days, including a self-powered flight vector of 6 m ⋅ s⁻¹ toward the north at flight altitudes of 1,000, 1,500 and 2,000 m above ground level. In these plots, only “successful” trajectories are shown—these are defined as trajectories that cross the Sahara (reaching 28°N) from either subregion or reach the northern subregion from the southern part of the west kernel. The full 12-y dataset of successful trajectories from the west kernel is shown in SI Appendix, Fig. S4, while the complete sets of all trajectories (successful and unsuccessful) from the west and east kernels are shown in SI Appendix, Figs. S5 and S6, respectively.