Pollen metabarcoding reveals the origin and multigenerational migratory pathway of an intercontinental-scale butterfly outbreak.

Migratory insects may move in large numbers, even surpassing migratory vertebrates in biomass. Long-distance migratory insects complete annual cycles through multiple generations, with each generation's reproductive success linked to the resources available at different breeding grounds. Climatic anomalies in these grounds are presumed to trigger rapid population outbreaks. Here, we infer the origin and track the multigenerational path of a remarkable outbreak of painted lady (Vanessa cardui) butterflies that took place at an intercontinental scale in Europe, the Middle East, and Africa from March 2019 to November 2019. Using metabarcoding, we identified pollen transported by 264 butterflies captured in 10 countries over 7 months and modeled the distribution of the 398 plants detected. The analysis showed that swarms collected in Eastern Europe in early spring originated in Arabia and the Middle East, coinciding with a positive anomaly in vegetation growth in the region from November 2018 to April 2019. From there, the swarms advanced to Northern Europe during late spring, followed by an early reversal toward southwestern Europe in summer. The pollen-based evidence matched spatiotemporal abundance peaks revealed by citizen science, which also suggested an echo effect of the outbreak in West Africa during September-November. Our results show that population outbreaks in a part of species' migratory ranges may disseminate demographic effects across multiple generations in a wide geographic area. This study represents an unprecedented effort to track a continuous multigenerational insect migration on an intercontinental scale.

The Afrotropical breeding grounds of the Palearctic-African migratory painted lady butterflies (Vanessa cardui).

Migratory insects are key players in ecosystem functioning and services, but their spatiotemporal distributions are typically poorly known. Ecological niche modeling (ENM) may be used to predict species seasonal distributions, but the resulting hypotheses should eventually be validated by field data. The painted lady butterfly (Vanessa cardui) performs multigenerational migrations between Europe and Africa and has become a model species for insect movement ecology. While the annual migration cycle of this species is well understood for Europe and northernmost Africa, it is still unknown where most individuals spend the winter. Through ENM, we previously predicted suitable breeding grounds in the subhumid regions near the tropics between November and February. In this work, we assess the suitability of these predictions through i) extensive field surveys and ii) two-year monitoring in six countries: a large-scale monitoring scheme to study butterfly migration in Africa. We document new breeding locations, year-round phenological information, and hostplant use. Field observations were nearly always predicted with high probability by the previous ENM, and monitoring demonstrated the influence of the precipitation seasonality regime on migratory phenology. Using the updated dataset, we built a refined ENM for the Palearctic-African range of V. cardui. We confirm the relevance of the Afrotropical region and document the missing natural history pieces of the longest migratory cycle described in butterflies.

Environmental controls on butterfly occurrence and species richness in Israel: The importance of temperature over rainfall.

Butterflies are considered important indicators representing the state of biodiversity and key ecosystem functions, but their use as bioindicators requires a better understanding of how their observed response is linked to environmental factors. Moreover, better understanding how butterfly faunas vary with climate and land cover may be useful to estimate the potential impacts of various drivers, including climate change, botanical succession, grazing, and afforestation. It is particularly important to establish which species of butterflies are sensitive to each environmental driver. The study took place in Israel, including the West Bank and Golan Heights. To develop a robust and systematic approach for identifying how butterfly faunas vary with the environment, we analyzed the occurrence of 73 species and the abundance of 24 species from Israeli Butterfly Monitoring Scheme (BMS-IL) data. We used regional generalized additive models to quantify butterfly abundance, and generalized linear latent variable models and generalized linear models to quantify the impact of temperature, rainfall, soil type, and habitat on individual species and on the species community. Species richness was higher for cooler transects, and also for hilly and mountainous transects in the Mediterranean region (rendzina and Terra rossa soils) compared with the coastal plain (Hamra soil) and semiarid northern Jordan Vale (loessial sierozem soil). Species occurrence was better explained by temperature (negative correlation) than precipitation, while for abundance the opposite pattern was found. Soil type and habitat were insignificant drivers of occurrence and abundance. Butterfly faunas responded very strongly to temperature, even when accounting for other environmental factors. We expect that some butterfly species will disappear from marginal sites with global warming, and a large proportion will become rarer as the region becomes increasingly arid.

Analysis of monitoring data where butterflies fly year-round.

Butterfly Monitoring Schemes (BMSs) engage the public in conservation and provide data sets that cover broad geographical areas over long timescales. Most existing BMSs are in temperate climates; however, the Israeli Butterfly Monitoring Scheme (BMS-IL), established in 2009, is a notable exception as it encompasses a large climatic gradient from Euro-Siberian through Mediterranean to hyper-arid regions. Israel's climate poses challenges in analyzing data from year-round butterfly activity, as in other tropical or arid countries. The Regional Generalized Additive Model (Regional GAM) is a butterfly phenology and abundance model based on repeat visits throughout species' flight season. We tested the applicability of Regional GAM for species with complex flight seasonality (e.g., multivoltine) by comparing estimated abundance and seasonal indices for the full data set and rarefied subsets. We assessed the reliability of modeled flight seasons and compared abundance estimates per site resulting from biologically plausible and unreliable seasonal models. The reliability of Regional GAM rises with the number of observations, and the model tends to produce more biologically plausible models for species with simple phenologies (e.g., univoltine with a single peak in activity). Abundance estimates based on unreliable models produce values with inter-quartile ranges of 90%-153% compared with biologically plausible models, while peak time changes with an interquartile range of 0-22.5 d when comparing all rarefied models with the full data set. Regional GAM should be applied with great caution for rare species and those with a complex flight season, and the date of year start needs to be carefully chosen for species that are active year-round. We identified the key sources of error and propose an operational workflow to address them. With few adaptations, Regional GAM can support new BMSs in analyzing data where butterflies are active year-round, including tropical climates. We propose guidelines for analyzing BMS data for species or regions with long activity periods and complex phenologies.

Round-trip across the Sahara: Afrotropical Painted Lady butterflies recolonize the Mediterranean in early spring.

The Palearctic-African migratory circuit has been typically associated with birds. Very few insects are known to endure annual trans-Saharan circuits, but the Painted Lady butterfly (Vanessa cardui) is an exception. While it was demonstrated that this species massively migrates from Europe to the Afrotropics during the autumn, the existence of a reverse migration from the Afrotropics to Europe in the early spring remains hypothetical. Here, we analysed wing stable hydrogen isotope values (δ2H) of V. cardui migrants collected from February to April across the circum-Mediterranean region. We assessed their region of natal origin by comparing their wing isotope signature predicted δ2H values (isoscape). The results unambiguously demonstrate a sub-Saharan origin for many individuals, especially those collected in February, representing the first tangible evidence for a reverse northwards trans-Saharan migration in spring. This work supports the view that the Afrotropics (mostly exploited from September to February) is key in the V. cardui Palearctic-African population dynamics. This species relies on both temperate and tropical habitats to complete their multigenerational cycle, an unprecedented adaptation for butterflies and for most migratory insects. Such a migratory circuit has strong parallelisms with those of migratory birds.

Phylogeny and palaeoecology of Polyommatus blue butterflies show Beringia was a climate-regulated gateway to the New World.

Transcontinental dispersals by organisms usually represent improbable events that constitute a major challenge for biogeographers. By integrating molecular phylogeny, historical biogeography and palaeoecology, we test a bold hypothesis proposed by Vladimir Nabokov regarding the origin of Neotropical Polyommatus blue butterflies, and show that Beringia has served as a biological corridor for the dispersal of these insects from Asia into the New World. We present a novel method to estimate ancestral temperature tolerances using distribution range limits of extant organisms, and find that climatic conditions in Beringia acted as a decisive filter in determining which taxa crossed into the New World during five separate invasions over the past 11 Myr. Our results reveal a marked effect of the Miocene-Pleistocene global cooling, and demonstrate that palaeoclimatic conditions left a strong signal on the ecology of present-day taxa in the New World. The phylogenetic conservatism in thermal tolerances that we have identified may permit the reconstruction of the palaeoecology of ancestral organisms, especially mobile taxa that can easily escape from hostile environments rather than adapt to them.