LETTER  pez-Man Reply to Lo ~ as et al.: Spatial population models of migrants should be underpinned by phenology, behavior, and ecology Constanti Stefanescua,b,1 , Gao Huc,1 , Tom H. Oliverd, Don R. Reynoldse,f and Jason W. Chapmanc,g,h,1 Lo pez-Man ~ as et al. (1) raise concerns about our recent www.gbif.org) for botanical records produces >1,000 occur- paper (2) documenting environmental drivers of annual rences of Asteraceae and ∼3,000 occurrences of Malvaceae variation in the abundance of immigrant painted ladies [families including the principal V. cardui larval hosts (6)] (Vanessa cardui) reaching southern Europe each spring. We within our “kernel areas” during January–February. We address their concerns, and further suggest that the ratio- nale behind their critique is predicated upon unrealistic assumptions. Author affiliations: aNatural Sciences Museum of Granollers, E08402 Granollers, Spain; b Centre de Recerca Ecolo  gica i Aplicacions Forestals, E08193 Bellaterra, Spain; cDepartment Firstly, Lo pez-Man~ as et al. (1) state that our identifica- of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, People’s Republic of China; dSchool of Biological Sciences, University of Reading, Reading tion of Savannah/Sahel “kernel areas” as important winter- RG6 6AS, United Kingdom; eNatural Resources Institute, University of Greenwich, Chatham breeding locations “challenges previous research in Africa” ME4 4TB, United Kingdom; fDepartment of Computational and Analytical Sciences, Rothamsted Research, Harpenden AL5 2JQ, United Kingdom; gCentre for Ecology and by these authors (3, 4). This is a somewhat surprising and Conservation, University of Exeter, Penryn TR10 9FE, United Kingdom; and hEnvironment contradictory viewpoint, as stable isotope analyses from and Sustainability Institute, University of Exeter, Penryn TR10 9FE, United Kingdom the same group (5) pinpointed exactly the same location as our “kernel areas” as the source of late-winter arrivals in North Africa and Spain. Lo  pez-Man ~ as et al. further surmise Author contributions: G.H. analyzed data; and C.S., T.H.O., D.R.R., and J.W.C. wrote the paper. The authors declare no competing interest. that high January–February normalized difference vegeta- Copyright © 2022 the Author(s). Published by PNAS. This article is distributed under tion index (NDVI) values in the Savannah/Sahel in outbreak Creative Commons Attribution License 4.0 (CC BY). years correspond only to growth of woody plants, and that 1 To whom correspondence may be addressed. Email: j.chapman2@exeter.ac.uk, canliro@ herbaceous larval hosts of V. cardui will be absent. Yet, a gmail.com, or hugao@njau.edu.cn. search of the Global Biodiversity Information Facility (https:// Published May 5, 2022. Fig. 1. (A) January NDVI values in the western “kernel area” of the Savannah/Sahel during our study period (1994–2015); the red dashed lines indicate the 3 y with the largest spring arrivals in southern Europe, that is, the highest spring painted lady log-collated index values in NE Spain (2), within our study period. (B) The mean log abundance of painted ladies (PL) reaching NE Spain in each spring plotted against January NDVI in the west “kernel area”; there is a significant positive relationship (linear regression; n = 815, r2 = 0.073, P < 0.0001). (C). The January NDVI anomaly (compared to the overall mean between 1994 and 2015) across Africa for the three mass immigration years indicated in A; the outline of the west “kernel area” is delimited by the red polygons. Highly positive January NDVI anomalies can be seen in at least some parts of the west “kernel” in each of these years, indicating that conditions would have been more suitable for painted lady larval development than in more typical years. PNAS 2022 Vol. 119 No. 19 e2203349119 https://doi.org/10.1073/pnas.2203349119 1 of 2 conclude that suitable larval hosts would be present at this knowledge of the migratory cycle (2, 9, 10), is more appro- key time, in at least some parts of the Savannah/Sahel, dur- priate than ignoring feasible linkages between locations of ing years when NDVI was higher than average and large pop- successive generations. In particular, our analyses strongly ulations reached southern Europe in the spring (Fig. 1). suggest that positive winter NDVI anomalies in the Savan- Secondly, Lo pez-Man~ as et al. (1) assert that V. cardui has nah/Sahel “kernel areas,” together with the assistance of “low philopatry” with unpredictable spatiotemporal distri- southerly winds, are important in seeding or reinforcing bution patterns. Based upon their hypothesis, they con- the generation developing in the spring in the Maghreb tend that our population models (2) are flawed due to and, ultimately, in explaining population levels recorded in “predetermined spatiotemporal partition.” Their premise is Europe in spring and summer (Fig. 1). erroneous, however, as the timing and general region of We do not dispute additional populations of V. cardui successive generations is, in fact, highly predictable and migrants across Africa and the Middle East, although we consistent across years. Irrefutable evidence for this come do believe correlative analyses should be based on sound from 1) comprehensive long-term butterfly monitoring ecological theory and existing observations, such as of the scheme data from multiple European countries (2); and 2) massive spring emergence areas in Morocco (11)—the final numerous published studies documenting dependable leg of the African migration into Europe. Additional ground occupation of the same geographical regions, at the same truthing through developing local monitoring capacity seasons, across multiple years (3–5, 7, 8). Thus, we contend across Africa will provide further mechanistic understand- that constraining population models to realistic spatiotem- ing of the impressive transcontinental migration patterns poral distributions, as we do based upon our extensive of this butterfly. 1. R. Lopez-Ma~nas et al., Erratic spatiotemporal vegetation growth anomalies drive population outbreaks in a trans-Saharan insect migrant. Proc. Natl. Acad. Sci. U.S.A., 10.1073/pnas.2121249119 (2022). 2. G. Hu et al., Environmental drivers of annual population fluctuations in a trans-Saharan insect migrant. Proc. Natl. Acad. Sci. U.S.A. 118, e2102762118 (2021). 3. G. Talavera, R. Vila, Discovery of mass migration and breeding of the painted lady butterfly Vanessa cardui in the sub-Sahara: The Europe–Africa migration revisited. Biol. J. Linn. Soc. Lond. 120, 274–285 (2016). 4. M. Menchetti, M. Gueguen, G. Talavera, Spatio-temporal ecological niche modelling of multigenerational insect migrations. Proc. Biol. Sci. 286, 20191583 (2019). 5. G. Talavera, C. Bataille, D. Benyamini, M. Gascoigne-Pees, R. Vila, Round-trip across the Sahara: Afrotropical painted lady butterflies recolonize the Mediterranean in early spring. Biol. Lett. 14, 20180274 (2018). 6. P. R. Ackery, Host-plants and classification: A review of nymphalid butterflies. Biol. J. Linn. Soc. Lond. 33, 95–203 (1988). 7. C. Stefanescu et al., Back to Africa: Autumn migration of the painted lady butterfly Vanessa cardui is timed to coincide with an increase in resource availability. Ecol. Entomol. 42, 737–747 (2017). 8. M. Cuadrado, Assessing year-round phenology and reproduction of the migratory painted lady butterfly, Vanessa cardui (Lepidoptera: Nymphalidae), in a Mediterranean area in southern Spain. Eur. J. Entomol. 118, 288–296 (2021). 9. C. Stefanescu et al., Multi-generational long-distance migration of insects: Studying the painted lady butterfly in the Western Palaearctic. Ecography 36, 474–486 (2013). 10. C. Stefanescu, D. X. Soto, G. Talavera, R. Vila, K. A. Hobson, Long-distance autumn migration across the Sahara by painted lady butterflies: Exploiting resource pulses in the tropical savannah. Biol. Lett. 12, 20160561 (2016). 11. C. Stefanescu, M. Alarcon, R. Izquierdo, F. Paramo, A. Avila, Moroccan source areas of the painted lady butterfly Vanessa cardui (Nymphalidae: Nymphalinae) migrating into Europe in spring. J. Lepid. Soc. 65, 15–26 (2011). 2 of 2 https://doi.org/10.1073/pnas.2203349119 pnas.org