The study indicates that the quagga mussel has recently invaded lakes Lugano and Maggiore. In addition, it illustrates the usefulness of using eDNA based approaches for the detection of invasive mussels at the beginning of the colonization process. In this initial stage the organisms are still difficult to detect by conventional monitoring, due to low biomass, whereas eDNA approaches are more sensitive, being able to detect scarce molecular “traces” left behind by mussels. The large water volumes needed to detect the species (> 10 L) and the high real-time PCR Ct values suggest that both the lakes are experiencing the first stages of colonization by quagga mussel.
The molecular approach used in this study shows a great potential to help detect and localize alien species in lakes. For example, compared to previous eDNA studies, in which fewer liters of water were collected, the use of VigiDNA, or similar cartridges, which allow to filtrate more than 10 L, probably increased the sensibility of the eDNA approach. Moreover, we suggest that the closed capsules used in this study are less subjected to contamination compared to open filtration (e.g. glass fiber filter). In previous studies, filtration capsules were kept at room temperature with preservation buffer until DNA extraction (Pont et al. 2018), especially to stabilize cell-free DNA, more subjected to fragmentation (Saito and Doi 2021). However, this approach required short term storage to avoid DNA degradation. In this study, we showed that eDNA can be efficiently retrieved from frozen filters, even when target DNA is expected at low quantities, which increases the storage period for environmental samples. Finally, the sampling strategy adopted in this study (i.e. pooled samples and transects) showed to be able to efficiently detect and localize DNA of alien mussels. The approach based on pooled samples was able to detect quagga’s DNA in all the basins analysed and proved to be an efficient method for screening for the presence of alien organisms present at low densities. The approach based on transects subsequently allowed to narrow down the colonization area of alien mussels, which are usually patchily distributed, especially in the first settlement stages.
Both PCR and real-time PCR are used in eDNA based monitoring protocols, as a cost-effective alternative to traditional survey (Goldberg et al. 2013). In this study, PCR was able to detect the presence/absence of quagga mussel in environmental samples. However, real-time PCR resulted more sensitive and proved to be more suitable for detecting target organism at low biomass.
The study provides the first evidence of the presence of quagga mussel in Western Europe south of the Alps. Our findings confirm the high invasiveness of this species, which easily attaches to boats and, during its larval stage, can be transported in ballast waters. Indeed, despite the recommendations to avoid the diffusion of quagga mussel and mandatory preemptive policies, such as the cleaning of boats and equipment moving from one lake to another, this species has been probably accidentally introduced in lakes Maggiore and Lugano by human mediated transport. These lakes attract large numbers of tourists every year, especially from Central and Northern Europe, which can facilitate the dispersal of alien species. As a result, during the last decades, the deep lakes south of the Alps have experienced invasions by several organisms, such as the Asiatic clams, Corbicula fluminea and Sinanodonta woodiana (Kamburska et al. 2013; Ciutti et al. 2011), the amphipod crustacean native to the Ponto-Caspian region, Dikerogammarus villosus (Ciutti et al. 2011; Altermatt et al. 2019), and the bryozoan native to North America, Pectinatella magnifica (Lepori et al. 2021). ). Due to proximity and trade-tourism, the spread of this invasive dreissenid to other subalpine lakes is expected.
Consistent with what happened in perialpine lakes north of the Alps (Haltiner et al. 2022) and in the Great Lakes of North America (Nalepa et al. 2010), the population of quagga mussel in lakes Maggiore and Lugano will probably grow and replace the zebra mussel during the next years, with potentially significant consequences for the ecosystem and the services provided. For example, dreissenid mussels have been associated with increases in harmful cyanobacteria blooms due to selective filtering (Vanderploeg et al. 2013), which may have important water quality implications. The management of the quagga mussel, and invasive species in general, is particularly challenging in transboundary lakes, which are subject to different national laws and regulations. An internationally coordinated program for the management of quagga mussel would facilitate the sharing of knowledge and solutions and would help in avoiding its further spread in Southwestern Europe. The early detection of this species based on eDNA approach provides water managers with a powerful tool to monitor the colonization status and plan actions to minimize ecological and economic impacts.