Multi-scale surveillance reveals substantial egg-laying winter activity in Aedes albopictus mosquito populations across temperate Europe

Daniele Da Re , Giovanni Marini, Alessandro Albieri, Paola Angelini, Karin Bakran-Lebl, Beniamino Caputo, Marco Carrieri, Maria Liliana Di Pasquale, Claudio De Liberato, Sarah Droghei, Irene Del Lesto, Alessandra Franceschini, Chiara Gentile, Peter Hufnag, Guillaume Lacour, Valeria Lencioni, Francesco La Russa, Riccardo Paolo Lia, Eleonora Longo, Mateusz Markowicz, Bruno Mathieu, Antoine Mignotte, Bianca Modespacher, Pie Müller, Francesca Paoli, Alessia Ricci, Federico Romiti, Barbara Seebacher, Rodolfo Veronesi, Roberto Rosà, Annapaola Rizzoli

The Asian tiger mosquito (Aedes albopictus), a competent vector for dengue, chikungunya, and Zika viruses, has expanded rapidly across temperate Europe. European vector surveillance typically operates May to October, assuming winter diapause precludes activity and transmission risk. However, recent field observations suggest sustained egg-laying winter activity in southern European populations, potentially extending arbovirus transmission risk. We aimed to quantify winter ovitrap activity patterns across temperate Europe and assess their implications for mosquito surveillance across temperate Europe. In this multi-scale observational study, we deployed standardised ovitraps from October 2024 to May 2025 across 12 locations spanning 35–48°N (Italy, France, Switzerland, Austria; n=345 trap-weeks), complemented by 14-year longitudinal surveillance (2011–2025) from Emilia-Romagna, northern Italy (n=1999 trap-weeks across 10 municipalities). We used binomial generalised additive models to quantify the effects of photoperiod, temperature, and precipitation on ovitrap positivity while accounting for spatial heterogeneity. We calculated trap effort requirements for reliable winter detection and assessed temporal trends in spring versus autumn activity. Winter ovitrap positivity was common and geographically structured. Photoperiod was the dominant driver (p<0.001), with southern Mediterranean sites maintaining detection probabilities >20% throughout December–January, while northern sites showed near-complete cessation. Temperature significantly modulated activity with reduced detection below 10°C. Substantial spatial heterogeneity persisted, indicating that local factors override climate variables. Spring positivity (January–May) was 73% lower than autumn (October–December; p<2×10⁻¹¹), reflecting overwintering population bottlenecks. Fourteen-year regional trends showed no significant autumn increase, but a modest spring increase, though confounded by temperature and potential surveillance artefacts. Power analysis revealed current surveillance (median 10 traps per site-week) substantially exceeds autumn requirements (4 traps for 80% detection) but falls short for spring (13 traps required). Ovipositing winter activity of Ae. albopictus in temperate Europe is widespread and structured by photoperiod and geography rather than being rare or negligible. Current May-October surveillance paradigms miss substantial autumn activity and likely underestimate population persistence capacity. Persistent egg-laying winter activity in Mediterranean climates, though homodynamicity was not detected, combined with recent evidence of lower-than-expected thermal transmission thresholds, suggests that arbovirus risk assessment should consider extended seasonal windows or better be estimated at an annual time frame. While our results demonstrate that winter monitoring is essential to uncover ecological patterns, multi-year continental surveys are required to confirm patterns and disentangle the drivers of seasonal variability. These results provide a foundation for adaptive surveillance strategies as Ae. albopictus continues expanding into increasingly temperate regions under climate change.