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Parasites and Invaders

Invasive species are a principal threat to biodiversity (Mack et al. 2000) that can alter the structure and function of recipient ecosystems. Mitigating the effects of biological invasions costs the UK around £1.7 billion per annum (Williams et al. 2012). The impact of invaders on native species can be exacerbated by co-introduced parasites, to which native hosts are often

immunoUntitledlogically naïve. These parasites can therefore cause mass mortalities of native hosts, thus threatening the preservation of resident biota and facilitating the establishment/spread of the invading host through reduced competition. Well-known examples of this include squirrel poxvirus and crayfish plague (Vilcinskas 2015). CRIPES Branchios gifresearch has largely focused on invasive parasites and hosts within aquatic environments, with the aim of highlighting the importance of preventing non-native introductions and understanding the effects of invasive hosts and parasites on native fauna.

Invasive fish pathogens

The UK harbours several non-native fish species, mostly introduced via aquaculture and the ornamental fish trade, as well as through angling and deliberate stocking. Non-native fish that harbour potentially damaging parasites include: the topmouth gudegon (Pseudorasbora parva) infected with Sphaerothecum destruens (see Britton et al. 2010);
sunbleak (Leucaspius delineates), which carry the parasite Neoergasilus japonicas (see Zięba et al. 2010); and the pumpkinseed sunfish (Lepomis gibbosus), which we found infected with the non-native parasite Onchocleidus dispar (see Hockley et al. 2011). Invasive parasites may directly alter the behaviour of native hosts, as we found for the generalist nematode Anguillicola crassus which infects the critically endangered European Eel, Anguilla anguillapseed (see Newbold et al. 2015). Alternatively, there can be indirect costs of invasion; if for example an introduced animal serves as an alternative host for an already established parasite. This was the case with Pseudamphistomum truncatum, common in fish intermediate hosts and established European otters in the UK, but also able to infect invasive mink (Sherrard-Smith et al. 2014).

We are currently investigating how invasive pumpkinseed fish interact with their parasite fauna and native fish species. In collaboration with Drs. Chris Williams and Gareth Davies (Environment Agency), this multi-disciplinary project by CRIPES PhD students Valentine Muhawenimana and Rhidian Thomas (supervised by Prof. Jo Cable, Dr. Siân Griffiths and Dr. Catherine Wilson), will use flume-based trials to determine the effects of parasites on the swimming performance of invasive pumpkinseed under different flow conditions.

Invasive crayfish and their pathogens

Since their introduction into the UK during the 1970’s invasive crayfish have spread Overland crayfish gif
rapidly, causing mass mortalities of Britain’s
only native crayfish, the white clawed crayfish (Austropotamobius pallipes) (James et al. 2014). Despite the implementation of stringent legislation banning the import of non-native crayfish into the UK, their abundance and diversity continues to increase (James et al. 2014). Former CRIPES PhD student, Dr Jo James and Prof. Jo Cable have teamed up with invertebrate conservation organisation Buglife (James et al. 2015a), to broadcast the threat invasive crayfish pose to white clawed crayfish (James et al. 2015b). A perhaps, hidden cost of these invasions is the co-introduction of novel parasites into the UK (James et al. 2015c). Recently CRIPES members published the first records of two Run away! Xv and Co
species of non-native branchiobdellidans (Annelida: Clitellata) on invasive signal crayfish (Pacifastacus leniusculus) in the UK (James et al. 2015bc).

Distribution of invasive signal crayfish in the UK. Red square highlights the approximate location of the branchiobdellidan infested population

Distribution of invasive signal crayfish in the UK. Red square highlights the approximate location of the branchiobdellidan infested population

Perhaps one of the greatest threats invasive crayfish pose to native ones is the transmission of the crayfish plague pathogen, Aphanomyces astaci. North American crayfishes, like the signal crayfish are largely resistant to infection with this pathogen but
in native crayfish it is reportedly 100% lethal. CRIPES members are currently working in collaboration with Prof. Adam Petrusek and PhD student Agata Mrugala (Charles University, Prague) and Dr. Birgit Oidtmann (CEFAS) to investigate the distribution of this deadly disease in the UK.

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Publications and references

Britton JR, Davies GD, Brazier M (2010) Towards the successful control of the invasive Pseudorasbora parva in the UK. Biological Invasions. 12:125-131

Hockley FA, Williams CF, Reading AJ, Taylor NGH, Cable J (2011) Parasite fauna of invasive pumpkinseed fish: first UK record of Onchocleidus dispar (Monogenea). Diseases of Aquatic Organisms 97:65-73.

King TA and Cable J (2007) Experimental infections of the monogenean Gyrodactylus turnbulli indicate that it is not a strict specialist. International Journal for Parasitology 37:663-672.

James J, Slater F, Cable J (2014) A.L.I.E.N. Databases: Addressing the Lack In Establishment of Non-Natives Databases. Crustaceana 87 (10):1192-1199. http://dx.doi.org/10.1163/15685403-00003329

James, J., Thomas, J. R., Ellis, A., Young, K. A., England, J., Cable, J. (2015) Over-invasion in a freshwater ecosystem: newly introduced virile crayfish (Orconectes virilis) outcompete established invasive signal crayfish (Pacifastacus leniusculus). DOI:10.1080/10236244.2015.1109181

James J, Cable J, Slater FM, Gilvear J (2015a) The distribution of crayfish species in the UK. Buglife – The invertebrate conservation trust https://www.buglife.org.uk/sites/default/files/Crayfish%20distrib%20UK_JG.pdf

James J, Slater F, Vaughan IP, Young KA, Cable J (2015b) Comparing the ecological impacts of native and invasive crayfish: could native species’ translocation do more harm than good? Oecologia 178:309-316 doi: 10.1007/s00442-014-3195-0

James J, Cable J, Ricardson G, Davidson KE, Mackie ASY (2015c) Two alien species of Branchiobdella (Annelida: Clitellata) new to the British Isles: a morphological and molecular study. Aquatic Invasions http://www.aquaticinvasions.net/2015/ACCEPTED/AI_2015_James_etal_correctedproof.pdf

Mack, RN, Simberloff D, Lonsdale, WM, Evans, H, Clout, M, Bazzaz, FA (2000) Biotic invasions: causes, epidemiology, global consequences and control. Ecological Applications. 10:689-710

Newbold LR, Hockley FA, Williams CF, Cable J, Reading AJ, Auchterlonie N, Kemp PS (2015) Non-native parasites alter European eel Anguilla anguilla swimming behaviour on encountering accelerating flow. Journal of Fish Biology 86 DOI: 10.1111/jfb.12659

Sherrard-Smith E, Chadwick EA, Cable J (2014) The impact of introduced hosts on parasite transmission: opisthorchiid infections in American mink (Neovison vison). Biological Invasions DOI 10.1007/s10530-014-0709-y.

Thomas, J. R., James, J., Newman, R. C., Riley, W. D., Griffiths, S. W., Cable, J. (2015) The impacts of streetlights on an aquatic invasive species: Artificial light at night alters signal crayfish behavior. Applied Animal Behaviour Science. doi:10.1016/j.applanim.2015.11.020

Vilcinskas A. (2015) Pathogens as Biological Weapons of Invasive Species. PLoS Pathogens DOI:10.1371/journal. ppat.1004714

Williams F, Eschen R, Harris A, Djeddour D, Pratt C, Shaw RS, Varia S, Lamontagne-Godwin J, Thomas SE, Murphy ST (2010) The Economic Cost of Invasive Non-Native Species on Great Britain. Knowledge for Life.

Zięba, G, Copp, GH, Davies, GD, Stebbing, P, Wesley, KJ, Britton, JR (2010) Recent releases and dispersal of non-native fishes in England and Wales, with emphasis on sunbleak Leucaspius delineates (Heckel, 1843) Aquatic Invasions 5:155-161

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