From storms to warming seas: a long-term metabarcoding survey in port communities unveils high genetic diversity and ecological resilience of non-indigenous species

Abstract

Ports are key gateways for the introduction and spread of non-indigenous species (NIS), yet the ecological and genetic temporal dynamics of these introductions remain poorly understood. Long term temporal monitoring is essential to unravel invasion processes, anticipate biodiversity shifts, and inform effective management and biosecurity strategies. In this study, we conducted a five-year (2019-2024) monthly metabarcoding survey in a northwestern Mediterranean port using artificial collectors. By sequencing a fragment of the Cytochrome Oxidase I gene, we identified 2,225 Molecular Operational Taxonomic Units (MOTUs), including 93 NIS. In addition, we examined both interspecific temporal patterns and intraspecific trends of genetic diversity over time. Although NIS accounted for only 4% of total species richness, they represented over 26% of total read abundance, underscoring their strong influence on community structure. Interestingly, NIS had a significantly more homogeneous species composition through time than native species. In 2020, the passage of the Gloria storm reshaped community dynamics, triggering a temporary rise in species richness and MOTU counts, likely due to an influx of native taxa and a gradual decline and increased NIS dominance. Genetic analyses revealed that NIS exhibited higher haplotypic diversity and lower genetic differentiation than native taxa, suggesting sustained gene flow, likely facilitated by maritime transport. MOTUs with longer temporal persistence, particularly among NIS, also showed greater intraspecific diversity, supporting the "insurance hypothesis" and highlighting the role of genetic variability in resilience and invasion success. Overall, our findings showed that NIS, despite their low species richness, maintain high abundances, connectivity, and genetic diversity over time. These attributes likely enhance the NIS ability to persist in dynamic and disturbed port environments, and provide key information for understanding the invasion process. This study highlights the need to integrate genetic diversity metrics into marine biomonitoring assessments and management.