Evidence of threat to European economy and biodiversity following the introduction of an alien pathogen on the fungal–animal boundary

Abstract

Recent years have seen a global and rapid resurgence of fungal diseases with direct impact on biodiversity and local extinctions of amphibian, coral, or bat populations. Despite similar evidence of population extinction in European fish populations and the associated risk of food aquaculture due to the emerging rosette agent Sphaerothecum destruens, an emerging infectious eukaryotic intracellular pathogen on the fungal–animal boundary, our understanding of current threats remained limited. Long-term monitoring of population decline for the 8-year post-introduction of the fungal pathogen was coupled with seasonal molecular analyses of the 18S rDNA and histological work of native fish species organs. A phylogenetic relationship between the existing EU and US strains using the ribosomal internal transcribed spacer sequences was also carried out. Here, we provide evidence that this emerging parasite has now been introduced via Pseudorasbora parva to sea bass farms, an industry that represents over 400 M€ annually in a Mediterranean region that is already economically vulnerable. We also provide for the first time evidence linking S. destruens to disease and severe declines in International Union for Conservation of Nature threatened European endemic freshwater fishes (i.e. 80% to 90 % mortalities). Our findings are thus of major economic and conservation importance.

First report of the intracellular fish parasite Sphaerothecum destruens associated with the invasive topmouth gudgeon (Pseudorasbora parva) in France

“…More recent studies have also reported infections in cyprinids (sunbleak, Leucaspius delineatus; bream, Abramis brama; carp, Cyprinus carpio; roach, Rutilus rutilus) (Gozlan et al, 2009). Given its potential to infect diverse other species, S. destruens has become a major worldwide threat for fish biodiversity (Arkush et al, 2003;Al-Shorbaji et al, 2015).…”

“…This invasive fish has spread at a high rate, invading five new countries each decade, and is classified as a worldwide pest (Welcomme, 1992;Gozlan et al, 2010). Furthermore, a recent study demonstrated that the topmouth gudgeon has transmitted S. destruens to sea bass (Dicentrarchus labrax) farms, leading to significant economic losses (Ercan et al, 2015). Its colonization success can be attributed to its early maturity, high fecundity and ability to adapt to new pathogens and environmental conditions (Gozlan et al, 2010).…”

“…Sphaerothecum destruens, a unicellular eukaryotic parasite of fish, is a pathogen on the fungal-animal boundary that has been implicated in severe infectious disease in salmonids in North America (Ercan et al, 2015). This parasite was first described in Chinook salmon (Oncorhynchus tshawytscha) held in seawater net pens in the state of Washington, USA, causing systemic disease leading to high mortality (over 80%) in 3-year-old fish broodstock (Harrell et al, 1986).…”

“…Furthermore, this parasite was detected in an invasive fish species, P. parva. Reports from other countries of this host-parasite couple based on molecular methods are rare and only recent: the Netherlands (Spikmans et al, 2013) and Turkey (Ercan et al, 2015). Given that pathogen concentrations in healthy carrier fish are generally very low, diagnostic tests frequently fail to detect the presence of the pathogen (Gozlan et al, 2005).…”

“…A survey of fish populations in metropolitan France between 1990 and2009 showed that this non-native species has spread dramatically (Poulet et al, 2011), colonizing many French rivers.…”