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Crayfish plague affects juvenile survival and adult behaviour of invasive signal crayfish

  • John Rhidian Thomas (a1), Chloe V. Robinson (a2), Agata Mrugała (a3), Amy R. Ellison (a1), Emily Matthews (a1), Siân W. Griffiths (a1), Sofia Consuegra (a2) and Jo Cable (a1)...

Abstract

The spread of invasive, non-native species is a key threat to biodiversity. Parasites can play a significant role by influencing their invasive host's survival or behaviour, which can subsequently alter invasion dynamics. The North American signal crayfish (Pacifastacus leniusculus) is a known carrier of Aphanomyces astaci, an oomycete pathogen that is the causative agent of crayfish plague and fatal to European crayfish species, whereas North American species are considered to be largely resistant. There is some evidence, however, that North American species, can also succumb to crayfish plague, though how A. astaci affects such ‘reservoir hosts’ is rarely considered. Here, we tested the impact of A. astaci infection on signal crayfish, by assessing juvenile survival and adult behaviour following exposure to A. astaci zoospores. Juvenile signal crayfish suffered high mortality 4-weeks post-hatching, but not as older juveniles. Furthermore, adult signal crayfish with high-infection levels displayed altered behaviours, being less likely to leave the water, explore terrestrial areas and exhibit escape responses. Overall, we reveal that A. astaci infection affects signal crayfish to a much greater extent than previously considered, which may not only have direct consequences for invasions, but could substantially affect commercially harvested signal crayfish stocks worldwide.

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Corresponding author

Author for correspondence: John Rhidian Thomas, E-mail: Thomasjr6@cardiff.ac.uk

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Present address: Bangor University, School of Natural Sciences, Environment Centre Wales, Bangor LL57 2UW, UK.

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References

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Alderman, DJ (1982) In vitro testing of fisheries chemotherapeutants. Journal of Fish Diseases 5, 113123.
Aydin, H, Kokko, H, Makkonen, J, Kortet, R, Kukkonen, H and Jussila, J (2014) The signal crayfish is vulnerable to both the As and the PsI-isolates of the crayfish plague. Knowledge and Management of Aquatic Ecosystems 3.
Bakker, TCM, Mazzi, D and Zala, S (1997) Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 10981104.
Barber, I, Mora, AB, Payne, EM, Weinersmith, KL and Sih, A (2017) Parasitism, personality and cognition in fish. Behavioural Processes 141, 205219.
Becking, T, Mrugała, A, Delaunay, C, Svoboda, J, Raimond, M, Viljamaa-Dirks, S, Petrusek, A, Grandjean, F and Braquart-Varnier, C (2015) Effect of experimental exposure to differently virulent Aphanomyces astaci strains on the immune response of the noble crayfish Astacus astacus. Journal of Invertebrate Pathology 132, 115124.
Belgrad, BA and Griffen, BD (2015) Rhizocephalan infection modifies host food consumption by reducing host activity levels. Journal of Experimental Marine Biology and Ecology 466, 7075.
Cable, J, Barber, I, Boag, B, Ellison, AR, Morgan, ER, Murray, K, Pascoe, EL, Sait, SM, Wilson, AJ and Booth, M (2017) Global change, parasite transmission and disease control: lessons from ecology. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160088.
Cerenius, L and Söderhäll, K (1984) Repeated zoospore emergence from isolated spore cysts of Aphanomyces astaci. Experimental Mycology 8, 370377.
Cerenius, L, Söderhäll, K, Persson, M and Ajaxon, R (1987) The crayfish plague fungus Aphanomyces astaci – diagnosis, isolation, and pathobiology. Freshwater Crayfish 7, 131143.
Cerenius, L, Bangyeekhun, E, Keyser, P, Söderhäll, I and Söderhäll, K (2003) Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to crayfish plague fungus, Aphanomyces astaci. Cellular Microbiology 5, 353357.
Cromarty, SI, Mello, J and Kass-Simon, G (2000) Molt-related and size-dependent differences in the escape response and post-threat behavior of the American lobster, Homarus americanus. Biological Bulletin 199, 265277.
Dikkeboom, R, Knaap, WPWVD, Meuleman, EA and Sminia, T (1985) A comparative study on the internal defence system of juvenile and adult Lymnaea stagnalis. Immunology 55, 547553.
Edsman, L, Nyström, P, Sandström, A, Stenberg, M, Kokko, H, Tiitinen, V, Makkonen, J and Jussila, J (2015) Eroded swimmeret syndrome in female crayfish Pacifastacus leniusculus associated with Aphanomyces astaci and Fusarium spp. infections. Diseases of Aquatic Organisms 112, 219228.
Ercoli, F, Ruokonen, TJ, Koistinen, S, Jones, RI and Hämäläinen, H (2015) The introduced signal crayfish and native noble crayfish have different effects on sublittoral macroinvertebrate assemblages in boreal lakes. Freshwater Biology 60, 16881698.
Filipová, L, Petrusek, A, Matasová, K, Delaunay, C and Grandjean, F (2013) Prevalence of the crayfish plague pathogen Aphanomyces astaci in populations of the signal crayfish Pacifastacus leniusculus in France: evaluating the threat to native crayfish. PLoS One 8, e70157.
Grandjean, F, Vrålstad, T, Diéguez-Uribeondo, J, Jelić, M, Mangombi, J, Delaunay, C, Filipová, L, Rezinciuc, S, Kozubíková-Balcarová, E, Guyonnet, D, Viljamaa-Dirks, S and Petrusek, A (2014) Microsatellite markers for direct genotyping of the crayfish plague pathogen Aphanomyces astaci (oomycetes) from infected host tissues. Veterinary Microbiology 170, 317324.
Grey, J and Jackson, MC (2012) ‘Leaves and eats shoots’: direct terrestrial feeding can supplement invasive red swamp crayfish in times of need. PLoS One 7, e42575.
Gruber, C, Kortet, R, Vainikka, A, Hyvärinen, P, Rantala, MJ, Pikkarainen, A, Jussila, J, Makkonen, J, Kokko, H and Hirvonen, H (2014) Variation in resistance to the invasive crayfish plague and immune defence in the native noble crayfish. Annales Zoologici Fennici 51, 371389.
Haddaway, NR, Wilcox, RH, Heptonstall, REA, Griffiths, HM, Mortimer, RJG, Christmas, M and Dunn, AM (2012) Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish. PLoS One 7, e32229.
Hatcher, MJ, Dick, JTA and Dunn, AM (2014) Parasites that change predator or prey behaviour can have keystone effects on community composition. Biological Letters 10. https://doi.org/10.1098/rsbl.2013.0879.
Holdich, DM, James, J, Jackson, C and Peay, S (2014) The North American signal crayfish, with particular reference to its success as an invasive species in Great Britain. Ethology Ecology & Evolution 26, 232262.
Huang, TS, Cerenius, L and Söderhäll, K (1994) Analysis of genetic diversity in the crayfish plague fungus, Aphanomyces astaci, by random amplification of polymorphic DNA. Aquaculture 126, 19.
Hudson, PJ, Dobson, AP and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecology & Evolution 21, 381385.
James, J, Cable, J and Slater, F (2014) A.L.I.E.N. databases: addressing the lack in establishment of non-natives databases. Crustaceana 87, 11921199.
James, J, Nutbeam-Tuffs, S, Cable, J, Mrugała, A, Viñuela-Rodriguez, N, Petrusek, A and Oidtmann, B (2017) The prevalence of Aphanomyces astaci in invasive signal crayfish from the UK and implications for native crayfish conservation. Parasitology 144, 411418.
Jussila, J, Kokko, H, Kortet, R and Makkonen, J (2013) Aphanomyces astaci Ps1-genotype isolates from different Finnish signal crayfish stocks show variation in their virulence but still kill fast. Knowledge and Management of Aquatic Ecosystems 411, 10.
Jussila, J, Vrezec, A, Makkonen, J and Kortet, R (2015) Invasive crayfish and their invasive diseases in Europe with the focus on the virulence evolution of the crayfish plague. In Canning-Clode, J (eds), Biological Invasions in Changing Ecosystems Vectors, Ecological Impacts, Management and Predictions. Warsaw/Berlin: DeGruyter Open Ltd, pp. 183204.
Jussila, J, Tiitinen, V, Edsman, L, Kokko, H and Fotedar, R (2016) Signal crayfish in Lake Saimaa could be maladapted to the local conditions due to Aphanomyces astaci infection: a seven-year study. Freshwater Crayfish 22, 5360.
Kozubíková-Balcarová, E, Koukol, O, Martín, MP, Svoboda, J, Petrusek, A and Diéguez-Uribeondo, J (2013) The diversity of oomycetes on crayfish: morphological vs. molecular identification of cultures obtained while isolating the crayfish plague pathogen. Fungal Biology 117, 682691.
Kozubíková-Balcarová, E, Beran, L, Ďuriš, Z, Fischer, D, Horká, I, Svoboda, J and Petrusek, A (2015) Status and recovery of indigenous crayfish populations after recent crayfish plague outbreaks in the Czech Republic. Ethology Ecology & Evolution 26, 299319.
Kozubíková, E, Vrålstad, T, Filipova, L and Petrusek, A (2011) Re-examination of the prevalence of Aphanomyces astaci in North American crayfish populations in Central Europe by TaqMan MGB real-time PCR. Diseases of Aquatic Organisms 97, 113125.
Longshaw, M, Bateman, KS, Stebbing, P, Stentiford, GD and Hockley, FA (2012) Disease risks associated with the importation and release of non-native crayfish species into mainland Britain. Aquatic Biology 16, 115.
Macnab, V and Barber, I (2012) Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Global Change Biology 18, 15401548.
Makkonen, J, Kokko, H, Henttonen, P and Jussila, J (2010) Crayfish plague (Aphanomyces astaci) can be vertically transferred during artificial incubation of crayfish eggs: preliminary results. Freshwater Crayfish 17, 151153.
Makkonen, J, Jussila, J, Kortet, R, Vainikka, A and Kokko, H (2012) Differing virulence of Aphanomyces astaci isolates and elevated resistance of noble crayfish Astacus astacus against crayfish plague. Diseases of Aquatic Organisms 102, 129136.
Makkonen, J, Strand, DA, Kokko, H, Vrålstad, T and Jussila, J (2013) Timing and quantifying Aphanomyces astaci sporulation from the noble crayfish suffering from the crayfish plague. Veterinary Microbiology 162, 750755.
McGrew, M and Hultgren, KM (2011) Bopyrid parasite infestation affects activity levels and morphology of the eusocial snapping shrimp Synalpheus elizabethae. Marine Ecology Progress Series 43, 195204.
Mrugała, A, Veselý, L, Petrusek, A, Viljamaa-Dirks, S and Kouba, A (2016) May Cherax destructor contribute to Aphanomyces astaci spread in Central Europe? Aquatic Invasions 11, 459468.
Mrugała, A, Kawai, T, Kozubíková-Balcarová, E and Petrusek, A (2017) Aphanomyces astaci presence inJapan: a threat to the endemic and endangered crayfish species Cambaroides japonicus. Aquatic Conservation: Marine and Freshwater Ecosystems 27, 103114.
Nyhlén, L and Unestam, T (1975) Ultrastructure of the penetration of the crayfish integument by the fungal parasite, Aphanomyces astaci, Oomycetes. Journal of Invertebrate Pathology 26, 353366.
Peay, S, Holdich, DM and Brickland, J (2010) Risk assessments of non-indigenous crayfish in Great Britain. Freshwater Crayfish 17, 109122.
Preston, DL, Mischler, JA, Townsend, AR and Johnson, PTJ (2016) Disease ecology meets ecosystem science. Ecosystems 19, 737748.
Puky, M (2014) Invasive crayfish on land: Orconectes limosus (Rafinesque, 1817) (Decapoda: Cambaridae) crossed a terrestrial barrier to move from a side arm into the Danube River at Szeremle, Hungary. Acta Zoologica Bulgarica 66, 143146.
Ramalho, RO and Anastácio, PM (2014) Factors inducing overland movement of invasive crayfish (Procambarus clarkii) in a ricefield habitat. Hydrobiologia 746, 135146.
R Core Team (2018) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.
Reynolds, JD (2002) Growth and reproduction. In Holdich, DM (ed.), Biology of Freshwater Crayfish. Oxford: Blackwell Science Ltd, pp. 152191.
Söderhäll, K, Svensson, E and Unestam, T (1978) Chitinase and protease activities in germinating zoospore cysts of a parasitic fungus, Aphanomyces astaci, oomycetes. Mycopathologia 64, 911.
Stasinopoulos, M, Rigby, RA and Akantziliotou, C (2008) Instructions on how to use the GAMLSS package in R, second edition. Available at http://www.gamlss.com/wp-content/uploads/2013/01/gamlss-manual.pdf.
Strand, DA, Jussila, J, Viljamaa-Dirks, S, Kokko, H, Makkonen, J, Holst-Jensen, A, Viljugrein, H and Vrålstad, T (2012) Monitoring the spore dynamics of Aphanomyces astaci in the ambient water of latent carrier crayfish. Veterinary Microbiology 160, 99107.
Strand, DA, Jussila, J, Johnsen, SI, Viljamaa-Dirks, S, Edsman, L, Wiik-Nielsen, J, Viljugrein, H, Engdahl, F and Vrålstad, T (2014) Detection of crayfish plague spores in large freshwater systems. Journal of Applied Ecology 51, 544553.
Svoboda, J, Kozubíková-Balcarová, E, Kouba, A, Buřič, M, Kozák, P, Diéguez-Uribeondo, J and Petrusek, A (2013) Temporal dynamics of spore release of the crayfish plague pathogen from its natural host, American spiny-cheek crayfish (Orconectes limosus), evaluated by transmission experiments. Parasitology 140, 792801.
Svoboda, J, Strand, DA, Vrålstad, T, Grandjean, F, Edsman, L, Kozák, P, Kouba, A, Fristad, RF, Koca, SB and Petrusek, A (2014) The crayfish plague pathogen can infect freshwater-inhabiting crabs. Freshwater Biology 59, 918929.
Svoboda, J, Mrugała, A, Kozubíková-Balcarová, E and Petrusek, A (2017) Hosts and transmission of the crayfish plague pathogen Aphanomyces astaci: a review. Journal of Fish Diseases 40, 127140.
Terry, M and Therneau, M (2018) Package ‘survival’. Available at https://CRAN.R-project.org/package=survival.
Thomas, LR (1965) Moulting behaviour of the western Australian crayfish Panulirus cygnus George (Decapoda, Reptantia). Crustaceana 11, 111113.
Tilmans, M, Mrugała, A, Svoboda, J, Engelsma, MY, Petie, M, Soes, DM, Nutbeam-Tuffs, S, Oidtmann, B, Rossink, I and Petrusek, A (2014) Survey of the crayfish plague pathogen presence in the Netherlands reveals a new Aphanomyces astaci carrier. Journal of Invertebrate Pathology 120, 7479.
Tompkins, DM, Dunn, AM, Smith, MJ and Telfer, S (2011) Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80, 1938.
Unestam, T and Weiss, DW (1970) The host-parasite relationship between freshwater crayfish and the crayfish disease fungus Aphanomyces astaci: responses to infection by a susceptible and a resistant species. Journal of General Microbiology 60, 7790.
Vilcinskas, A (2015) Pathogens as biological weapons of invasive species. PLoS Pathogens 11, 15.
Vrålstad, T, Knutsen, AK, Tengs, T and Holst-Jensen, A (2009) A quantitative TaqMan® MGB real-time polymerase chain reaction based assay for detection of the causative agent of crayfish plague Aphanomyces astaci. Veterinary Microbiology 137, 146155.

Keywords

Crayfish plague affects juvenile survival and adult behaviour of invasive signal crayfish

  • John Rhidian Thomas (a1), Chloe V. Robinson (a2), Agata Mrugała (a3), Amy R. Ellison (a1), Emily Matthews (a1), Siân W. Griffiths (a1), Sofia Consuegra (a2) and Jo Cable (a1)...

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