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

Published online by Cambridge University Press:  12 February 2020

John Rhidian Thomas Open the ORCID record for John Rhidian Thomas [Opens in a new window] ,
Chloe V. Robinson ,
Agata Mrugała ,
Amy R. Ellison ,
Emily Matthews ,
Siân W. Griffiths ,
Sofia Consuegra  and
Jo Cable
John Rhidian Thomas*
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, CardiffCF10 3AX, UK
Chloe V. Robinson
Affiliation:
Department of Biosciences, Swansea University, Singleton Park, SwanseaSA2 8PP, UK
Agata Mrugała
Affiliation:
Department of Ecology, Faculty of Science, Charles University, Viničná 7, Prague 2 CZ-12844, Czech Republic
Amy R. Ellison
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, CardiffCF10 3AX, UK
Emily Matthews
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, CardiffCF10 3AX, UK
Siân W. Griffiths
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, CardiffCF10 3AX, UK
Sofia Consuegra
Affiliation:
Department of Biosciences, Swansea University, Singleton Park, SwanseaSA2 8PP, UK
Jo Cable
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, CardiffCF10 3AX, UK
*
Author for correspondence: John Rhidian Thomas, E-mail: Thomasjr6@cardiff.ac.uk
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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.

Keywords

Aphanomyces astacibehaviourcrayfish plagueinvasive speciesreservoir hostssignal crayfish
Type
Research Article
Information
Parasitology , Volume 147 , Issue 6 , May 2020 , pp. 706 - 714
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

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

References

Alderman, DJ (1982) In vitro testing of fisheries chemotherapeutants. Journal of Fish Diseases 5, 113–123.CrossRefGoogle Scholar
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.Google Scholar
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, 1098–1104.CrossRefGoogle Scholar
Barber, I, Mora, AB, Payne, EM, Weinersmith, KL and Sih, A (2017) Parasitism, personality and cognition in fish. Behavioural Processes 141, 205–219.CrossRefGoogle ScholarPubMed
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, 115–124.CrossRefGoogle ScholarPubMed
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, 70–75.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Cerenius, L and Söderhäll, K (1984) Repeated zoospore emergence from isolated spore cysts of Aphanomyces astaci. Experimental Mycology 8, 370–377.CrossRefGoogle Scholar
Cerenius, L, Söderhäll, K, Persson, M and Ajaxon, R (1987) The crayfish plague fungus Aphanomyces astaci – diagnosis, isolation, and pathobiology. Freshwater Crayfish 7, 131–143.Google Scholar
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, 353–357.CrossRefGoogle ScholarPubMed
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, 265–277.CrossRefGoogle ScholarPubMed
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, 547–553.Google ScholarPubMed
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, 219–228.CrossRefGoogle ScholarPubMed
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, 1688–1698.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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, 317–324.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 371–389.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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, 232–262.CrossRefGoogle Scholar
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, 1–9.CrossRefGoogle Scholar
Hudson, PJ, Dobson, AP and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecology & Evolution 21, 381–385.CrossRefGoogle Scholar
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, 1192–1199.CrossRefGoogle Scholar
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, 411–418.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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. 183–204.Google Scholar
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, 53–60.CrossRefGoogle Scholar
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, 682–691.CrossRefGoogle ScholarPubMed
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, 299–319.CrossRefGoogle Scholar
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, 113–125.CrossRefGoogle ScholarPubMed
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, 1–15.CrossRefGoogle Scholar
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, 1540–1548.CrossRefGoogle Scholar
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, 151–153.Google Scholar
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, 129–136.CrossRefGoogle ScholarPubMed
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, 750–755.CrossRefGoogle ScholarPubMed
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, 195–204.CrossRefGoogle Scholar
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, 459–468.CrossRefGoogle Scholar
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, 103–114.CrossRefGoogle Scholar
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, 353–366.CrossRefGoogle Scholar
Peay, S, Holdich, DM and Brickland, J (2010) Risk assessments of non-indigenous crayfish in Great Britain. Freshwater Crayfish 17, 109–122.Google Scholar
Preston, DL, Mischler, JA, Townsend, AR and Johnson, PTJ (2016) Disease ecology meets ecosystem science. Ecosystems 19, 737–748.CrossRefGoogle Scholar
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, 143–146.Google Scholar
Ramalho, RO and Anastácio, PM (2014) Factors inducing overland movement of invasive crayfish (Procambarus clarkii) in a ricefield habitat. Hydrobiologia 746, 135–146.CrossRefGoogle Scholar
R Core Team (2018) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Reynolds, JD (2002) Growth and reproduction. In Holdich, DM (ed.), Biology of Freshwater Crayfish. Oxford: Blackwell Science Ltd, pp. 152–191.Google Scholar
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, 9–11.CrossRefGoogle Scholar
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.Google Scholar
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, 99–107.CrossRefGoogle ScholarPubMed
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, 544–553.CrossRefGoogle Scholar
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, 792–801.CrossRefGoogle Scholar
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, 918–929.CrossRefGoogle Scholar
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, 127–140.CrossRefGoogle ScholarPubMed
Terry, M and Therneau, M (2018) Package ‘survival’. Available at https://CRAN.R-project.org/package=survival.Google Scholar
Thomas, LR (1965) Moulting behaviour of the western Australian crayfish Panulirus cygnus George (Decapoda, Reptantia). Crustaceana 11, 111–113.CrossRefGoogle Scholar
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, 74–79.CrossRefGoogle ScholarPubMed
Tompkins, DM, Dunn, AM, Smith, MJ and Telfer, S (2011) Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80, 19–38.CrossRefGoogle Scholar
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, 77–90.CrossRefGoogle Scholar
Vilcinskas, A (2015) Pathogens as biological weapons of invasive species. PLoS Pathogens 11, 1–5.CrossRefGoogle ScholarPubMed
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, 146–155.CrossRefGoogle Scholar