Biological invasion is one of the major causes of biodiversity loss, biogenic homogenization and species endangerment (Wilcove et al. 1998; Keller et al. 2011; Lockwood et al. 2013; Olden et al. 2004). Biological invasions cause huge economic costs due to their impact on native species, agriculture and infrastructure (Pimentel et al. 2005; Marbuah et al. 2014; Hoffman and Broadhurts 2016). In addition, invasive species challenge the human and ecosystem health (Hulme et al. 2014; Mazza et al. 2014). In freshwater ecosystems, alien species have been recognized as primarily drivers of biodiversity reduction (e.g., Lockwood 2013) and the second leading cause of species extinction (MEA 2005). Especially in the areas of high endemism, invasive species have decreased local biodiversity severely (IPBES 2019).
There are several hypotheses on the success and mechanisms of bioinvasions (Jeschke and Heger, 2018), one of the prominent being the Enemy Release Hypothesis (ERH) (Elton 1958). The ERH suggests that the invaders are released from their natural enemies, e.g., predators, parasites or pathogens, during the invasion process, which will lead to a low enemy pressure on invaders in the invaded area and give the invaders an advantage when competing with local, native species (Elton 1958, Heger and Jeschke 2014). The host-parasite relationships can modify the invasion outcome, depending on several factors, e.g., whether the host or the parasite is the invader, or whether the parasite belongs to the invasive or the native host, and whether the negative effect of parasite in question is directed to the invader or to the native host—or towards the parasites of the native species— in the community of the introduced area (e.g., dilution effect, disease facilitation, parasite spillback and spill over, suppressive spillover; Chalkowski et al., 2018). Among the many hypotheses addressing the effect of parasites in invasion ecology the ERH has been very prominent (Chalkowski et al. 2018). Reduction in the invader’s parasite and pathogen pressure in invaded area when compared to the original area has been observed across a wide range of bioinvasions (Mitchell and Power 2003; Torchin et al. 2003; Liu et al. 2006; Blumenthal et al. 2013; Lowry et al. 2013).
There are three rationales behind the ERH related to parasites as enemies. First, parasites are harmful to host individuals and therefore can regulate the host populations. Indeed, such a regulation has been observed in natural populations (e.g., Grenfell and Dobson 1995). Second, parasites are generally highly host-specific, i.e., can only harbor certain species or even genotypes of hosts that exist in certain geographic area or environment, and with which they have had a common co-evolutionary history (e.g., Price 1980). Third, the invaders normally cannot bring their parasites with them, either because they were introduced as a larval stage which are frequently parasite-free, or because of the lack of suitable intermediate hosts the new environment in parasites having complex multi-host life cycle.
The invasion of alien bivalves is threatening freshwater mussels (Unionida), which is one of the most endangered animal groups worldwide (Lydeard et al. 2004, Lopes-Lima et al. 2017, Ferreira-Rodriguez et al. 2018). Unionid mussels are important part of freshwater ecosystems due to their filter feeding nature and potentially high biomass, so that they can influence nutrient cycling and provide many essential ecosystems services (Ökland 1963; Strayer 2014; Vaughn 2018; Zieritz et al. 2022). However, in spite of their importance, freshwater mussels are in urgent need of conservation actions (Aldridge et al. 2022; Sousa et al. 2023). Some freshwater bivalves, such as the Asia clam Corbicula fluminea (Müller 1774) and the zebra mussel Dreissena polymorpha (Pallas, 1771) are among the globally most problematic biological invaders threatening not only the native bivalve communities but interfering the whole aquatic ecosystem structure and functions (Karatayev et al. 1997; Strayer et al. 1998; Ward and Ricciardi 2007; Sousa et al. 2009; Higgins and Vander Zanden 2010 and 2018; Modesto et al. 2019). For example, biodiversity of the native freshwater mussel community of Lake Erie, North America, has decreased dramatically after the invasion of D. polymorpha (e.g., Bodis et al. 2014). The increase in the C. fluminea density may lead to lower growth and lower physiological condition of local freshwater mussels (Ferreira-Rodriguez et al. 2018). In many freshwater ecosystems, local mussel populations have collapsed after the invasion of C. fluminea due to the overlapping niche requirements and the high competitive ability of the invader (Modesto et al. 2021). The invasive bivalves C. fluminea and the Chinese pond mussel Sinanodonta woodiana – both frequently outperforming the native mussels – are rapidly expanding their range in Europe (Bespalaya et al. 2018; Karaouzas et al. 2020; Urbanska et al. 2021).
A number of characteristics has been connected to successful invading freshwater bivalves. These factors include fouling of native mussels (D. polymorpha), induction of cross-resistance in host fish of native mussels (S. woodiana), potentially longer breeding season, higher fecundity and a wide spectrum of suitable fish hosts (S. woodiana), as well as free-living instead of parasitic larva (D. polymorpha, C. fluminea) (e.g., Schloesser and Nalepa 1994; Schloesser et al. 1996; Donrovich et al. 2016; Dzierzynska-Białonczyk et al. 2018; Labecka and Domagala 2018; Urbańska et al. 2018; Yanovych 2015). The role of enemy release—a lower parasite pressure in invasive bivalves than in sympatric native mussels—as a factor contributing to the success of invasive bivalves has not received much attention. However, evidence for the ERH was recently provided for northern European waterbodies (Taskinen et al. 2021), such that in sympatric populations the invasive bivalves showed lower values of parasite pressure measures than the native freshwater mussels. In addition, in the recent review by Karatayev et al. (2024) more natural enemies of Dreissena spp., including parasites, were initially present in their native range in Europe compared to North America.
Within Europe, the decline of freshwater mussels is most alarming in the Mediterranean region (Nogueira et al. 2021; Benson et. al. 2021; Lopes-Lima et al. 2021), along with the general serious threatened nature of this biodiversity hotspot area (Cuttelod et al. 2009). Therefore, the aim of the present study was to extend the approach of Taskinen et al. (2021) to the Mediterranean area, to investigate the ERH in southern Europe by comparing the parasite loads of sympatric invasive and native bivalves. The target lakes were Lake Maggiore, Lake Varese and Lake Lugano in Italy, where the native mussel populations are rapidly declining (e.g., Riccardi et al. 2022). Importantly, sharp declines of native freshwater mussels in these lakes can be attributed to invasion by exotic bivalves. For instance, before the introduction of C. fluminea (Kamburska et al. 2013a) and Sinanodonta woodiana (Kamburska et al. 2013b) the density of native Unio population in Lake Maggiore remained stable even if subjected to periodic die-offs due to drought (Ravera et al. 2007), but after C. fluminea establishment it decreased by 75%. A similar trend was observed in Lake Varese and Lake Lugano after the invasion and establishment of C. fluminea and S. woodiana (N. Riccardi, personal communication). Many factors may be involved in the decline of native populations, including parasites which may be favored by recent increases in temperatures (see Taskinen et al. 2022) and droughts, as the adverse effects of parasites are commonly intensified by environmental stress (e.g., Jokela et al. 2005). In this case, the impact of parasites could reduce the fitness of native mussels, already affected by climate change, favoring invasive species if they were less infected, as predicted by ERH.
Our study hypothesis was that the invasive bivalves experience, on the average, lower parasite pressure than the native ones in these southern European lakes, as predicted by the ERH. To explore this hypothesis, we compared two parasite pressure indicators—parasite taxon richness and sum of prevalences of all parasite taxa (Lafferty et al. 2010; Torchin et al. 2003)—between the native and invasive bivalve populations living in sympatry in the three study lakes.