Phylogenetic and environmental DNA insights into emerging aquatic parasites: implications for risk management

Abstract

Species translocation leads to disease emergence in native species of considerable economic importance. Generalist parasites are more likely to be transported, become established and infect new hosts, thus their risk needs to be evaluated. Freshwater systems are particularly at risk from parasite introductions due to the frequency of fish movements, lack of international legislative controls for non-listed pathogens and inherent difficulties with monitoring disease introductions in wild fish populations. Here we used one of the world's most invasive freshwater fish, the topmouth gudgeon, Pseudorasbora parva, to demonstrate the risk posed by an emergent generalist parasite, Sphaerothecum destruens. Pseudorasbora parva has spread to 32 countries from its native range in China through the aquaculture trade and has introduced S. destruens to at least five of these. We systematically investigated the spread of S. destruens through Great Britain and its establishment in native fish communities through a combination of phylogenetic studies of the host and parasite and a novel environmental DNA detection assay. Molecular approaches confirmed that S. destruens is present in 50% of the P. parva communities tested and was also detected in resident native fish communities but in the absence of notable histopathological changes. We identified specific P. parva haplotypes associated with S. destruens and evaluated the risk of disease emergence from this cryptic fish parasite. We provide a framework that can be applied to any aquatic pathogen to enhance detection and help mitigate future disease risks in wild fish populations.

Impact of the invasive alien topmouth gudgeon (Pseudorasbora parva) and its associated parasite Sphaerothecum destruens on native fish species

“…Zoospore concentrations and zoosporulation duration of S. destruens are known to increase at temperatures between 4 and 15°C (Andreou et al 2009). Detection of S. destruens eDNA is limited in turbid conditions, due to absorption of the DNA to soil particles and detection is also more difficult with low P. parva densities (Sana et al 2018). Furthermore, we found that sites where S. destruens was detected were significantly smaller in surface area than sites where S. destruens was not detected.…”

“…This is possibly due to co-existence with P. parva that has inhabited this area for 20 years. Sana et al (2018) found that B. barbatula, Cottus gobio and G. aculeatus all tested negative as a host for S. destruens, even though S. destruens presence in the sampled stream was proven by eDNA detection.…”

“…Sphaerothecum destruens is a generalist and known to have a broad host species spectrum (Arkush et al 2003;Gozlan et al 2009;Andreou et al 2012;Andreou and Gozlan 2016) and it is being found in an increasing number of fish species in wild populations: Oncorhynchus tshawytscha, Oncorhynchus kisutch (Arkush et al 1998), P. parva (Gozlan et al 2005), L. delineatus (Andreou et al 2011), Dicentrarchus labrax, Lepomis gibbosus, Oxynoemacheilus sp., Petroleuciscus smyrnaeus, Squalius fellowesii (Ercan et al 2015), Leuciscus leuciscus, Rutilus rutilus, Squalius cephalus and Salmo trutta (Sana et al 2018). In experimental or hatchery conditions, several other fish species have proven to act as hosts: Oncorhynchus mykiss (Arkush et al 1998), Salmo salar (Paley et al 2012), A. brama and C. carpio (Andreou et al 2012).…”

“…For example, more samples are required to determine spatial genetic variation of S. destruens in more detail. Environmental DNA is a promising, noninvasive, sensitive and specific method to detect S. destruens (Sana et al 2018) as the species has a freeliving zoospore stage with a broad temperature tolerance (Andreou et al 2009) and (nested) PCRamplification is extremely sensitive in detecting this particular zoospore life stage (Mendonca and Arkush 2004;Bass et al 2015). Sampling techniques can be of great influence on the outcomes of eDNA studies (Hinlo et al 2017;Goldberg et al 2016).…”

“…Since we amplified a relatively large DNA fragment for detecting S. destruens, due to DNA degradation this might have yielded negatives meaning that our results are conservative. In addition, Sana et al (2018) used longer primers that were more specific to detect S. destruens and real-time PCR, which is therefore recommended for use in future eDNA studies. Optimizing the eDNA sampling and analysis protocol in accordance with Mendonca and Arkush (2004) and Sana et al (2018) is important as it can be useful to better understand the scale of S. destruens distribution, providing information for risk analysis and setting up control programs.…”