First Scientific Records of the Invasive Red Swamp Crayfish, Procambarus clarkii (Girard, 1852) (Crustacea: Cambaridae) in Malta, a Threat to Fragile Freshwater Habitats

Abstract

This study reports the first records of the invasive fresh water red swamp crayfish, Procambarus clarkii in Malta, first spotted in the wild in summer 2016. In spring 2017, 26 specimens of P. clarkii were collected, sexed, measured and identified both morphologically and genetically. The distribution and density of the species along the same valley were investigated at Fiddien Valley and Chadwick Lakes. As these two locations are associated with one of the major valley systems that cross the island, the presence of this prolific, aggressive and opportunistic feeding crayfish species increases the vulnerability of native freshwater species.

Keywords

• Procambarus clarkii
• freshwater crayfish
• invasive; new record
• Malta

References

1. Alcorlo, P., Geiger, W., Otero, M., (2004). Feeding preferences and food selection of the red swamp crayfish, Procambarus clarkii in habitats differing in food item diversity. Crustaceana, 77, 435-453.
2. Aquiloni, L., Martin, M.P., Gherardi, F., Dieguez-Uribeondo, J. (2011). The North American crayfish Procambarus clarkii the carrier of the oomycete Aphanomyces astaci in Italy. Biological Invasions, 13, 359-367.
3. Bohman, P., Edsman, L., Martin, P., Scholtz, G. (2013). The first Marmorkrebs (Decapoda: Astacida: Cambaridae) in Scandinavia. BioInvasions Records, 2(3), 227-232.
4. Capolongo, D., Cilia, J.L. (1990). Potamon fluviatile lanfrancoi, a new subspecies of a Mediterranean freshwater crab from the Maltese Islands (Crustacea, Decapoda, Potamidae). Annalen Naturhististorisches Museum, Wien. 91B, 215-224.
5. Cilenti, L., Alfonso, G., Gargiulo, M., Chetta, F.S., Liparoto, A., D’Adamo, R., Mancinelli, G. 2017. First records of the crayfish Procambarus clarkii (Girard, 1852) (Decapoda, Cambaridae) in Lake Varano and in the Salento Peninsula (Puglia region, SE Italy), with review of the current status in southern Italy. BioInvasions Records, 6(2), 153-158.
6. D’Angelo, S., Lo Valvo, M. (2003). On the presence of the red swamp crayfish Procambarus clarkii in Sicily. Il Naturalista Siciliano, 27, 325-327.
7. Di Leo, C., Faraone, F.P., Lo Valvo, M. (2014). A new record of the Red swamp crayfish, Procambarus clarkii (Girard, 1852) (Crustacea Cambaridae), in Sicily, Italy. Biodiversity Journal, 5(3), 425-428.
8. Dieguez-Uribeondo, J., Huang, T.S., Cerenius, L., Soderhall, K. (1995). Physiological adaptation of an Aphanomyces astaci strain isolated from the freshwater crayfish Procambarus clarkii. Mycological Research, 99, 574-578.

9. Dörr, A.J.M., La Porta, G., Pedicillo, G., Lorenzoni, M. (2006). Biology of Procambarus clarkii (Girard, 1852) in Lake Trasimeno. Bulletin Français de la Pêche et de la Pisciculture, 380, 1155-1167.
10. EUR-Lex (2017). Access to European Union Law. [http://eur-lex.europa.eu/homepage.html]. Accessed 5th May, 2017. Folmer, O., Black, M., Hoeh, W., Lutz, R., Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294-299.
11. Garcia, C., Montgomery, E., Krug, J., Dagit, R. (2015). Removal Efforts and Ecosystem Effects of Invasive Red Swamp Crayfish (Procambarus clarkii) in Topanga Creek. Bulletin of the Southern California Academy of Sciences. 114(1), 12-21.
12. Garzoli, L., Paganelli, D., Rodolfi, M., Savini, D., Moretto, D., Occhipinti-Ambrogi, A., Picco, A.M., (2014). First evidence of microfungal extra oomph in the invasive red swamp crayfish Procambarus clarkii. Aquatic Invasions, 9, 47-58.
13. Gherardi, F. (2006). Crayfish invading Europe: the case study of Procambarus clarkii. Marine and Freshwater Behaviour and Physiology, 39, 175-191.
14. GISD (2017). Global Invasive Species Database. Species profile: Procambarus clarkii. [http://www.iucngisd.org/gisd/speciesname/Procambarus+clarkii]. Accessed on: 10 May, 2017.
15. GoogleEarth (2013). Rabat, Malta. 35°53’24.24’’N, 14°22’58.06’’E. Accessed on: 15 April 2017.
16. Government Notice 473 (2011). Environment and Development Planning Act (CAP. 504); Trees and Woodlands Protection Regulations, 2011. [Available on http://www.doi-archived.gov.mt/EN/ gazetteonline /2011/05/gazts/GG%2024.5Mepa.pdf].
17. Grey, J., Jackson, M.C. (2012). ‘Leaves and Eats Shoots’: Direct Terrestrial Feeding Can Supplement Invasive Red Swamp Crayfish in Times of Need. PLoS ONE, 7(8), e42575.
18. Haslam, S.M., Borg, J. (1998). The River Valleys of the Maltese Islands: environment and human impact. Foundation for International Studies (Malta). Islands and Small States Institute; International Centre for Advanced Mediterranean Agronomic Studies (CIHEAM) (Italy). Valletta. 330p.
19. Hobbs, H.H. (1989). An Illustrated Checklist of the American crayfish (Decapoda: Astacidae, Cambaridae & Parastacidae). Smithsonian Contributions to Zoology. Smithsonian Institute Press, Washington, D.C., 480, 236p.
20. Holdich, D., Reynolds, J., Souty-Grosset, C., Sibley, P. (2009). A review of the ever increasing threat to European crayfish from non- indigenous crayfish species. Knowledge and Management of Aquatic Ecosystems, 11, 394-395.
21. Ilheu, M., Acquistapace, P., Benvenuto, C., Gherardi, F. (2003). Shelter use of the Red-Swamp Crayfish (Procambarus clarkii) in dry-season stream pools. Archiv fur Hydrobiologie, 157, 535-546.
22. Kambhampati, S., Smith, P.T. (1995). PCR Primers for the amplification of four insect mitochondrial gene fragments. Insect Molecular Biology, 4(4), 233-236.
23. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P., & Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647-1649.
24. Li, Y., Guo, X., Cao, X., Deng, W., Luo, W., Wang, W. (2012). Population genetic structure and post-establishment dispersal patterns of the red swamp crayfish Procambarus clarkii in China. PLoS One, 7(7), e40652.
25. Magro, D. (2016) http://www.inewsmalta.com/article.php?ID1=40062 in iNEWS, published 22 September, 2016. Accessed on: 15th April 2017.
26. Malta Aquarist Society (2011). Malta Aquarist Society Forum. [http://www.maltaaquarist.com/site/ Forum/tabid/76/forumid/16/threadid/15877/scope/posts/Default.aspx]. Accessed on: 5th May 2017.
27. Marcal Correia, A. (2003). Food choice by the introduced crayfish Procambarus clarkii. Annales Zoologici Fennici, 40, 517-528.
28. Martin, P., Dorn, N., Kawai, T., van der Heiden, C., Scholtz, G. (2010). The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contributions to Zoology, 79, 107-118.
29. Mazza, G., Reboleira, A.S.P.S., Goncalves, F., Aquiloni, L., Inghilesi, A.F., Spigoli, D., Stoch, F., Taiti, S., Gherardi, F., Tricarico, E. (2014). A new threat for the groundwater ecosystems:first occurrences of the invasive crayfish Procambarus clarkii (Girard, 1852) in the European caves. Journal of Cave and Karst Studies, 76, 62-65.
30. McClain, R.W. (2013). Effects of simulated precipitation extremes on crayfish (Procambarus clarkii Girard) oviposition in artificial burrows. Aquaculture, 44, 612-617.
31. Morehouse, R., Tobler, M. (2013). Crayfishes (Decapoda : Cambaridae) of Oklahoma: Identification, distributions, and natural history. Zootaxa, 3717(2), 101-157.
32. Mueller, K.W. (2007). Reproductive habits of non-native red swamp crayfish (Procambarus clarkii) at Pine Lake, Sammamish, Washington. Northwest Science, 81(3), 246-250.
33. NCBI (2017). Blastn suite. [https://blast.ncbi.nlm.nih.gov/Blast.cgi?PAGE_TYPE=BlastSearch]. Accessed: 5th May, 2017.
34. Nunes, A.L., Tricarico, E., Panov, V.E., Cardoso, A.C., Katsanevakis, S. (2015). Pathways and gateways of freshwater invasions in Europe. Aquatic Invasions, 10(4), 359-370.
35. Quan, A.S., Pease, K.M., Breinholt, J.W., Wayne, R.K. (2014). Origins of the invasive red swamp crayfish (Procambarus clarkii) in the Santa Monica Mountains. Aquatic Invasions, 9(2), 211-219.
36. Ratnasingham, S., Hebert, P.D.N. (2007). BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7, 355-364. [BOLD database accessed: 5th May, 2017].
37. Savini, D., Occhipinti-Ambrogi, A., Marchini, A., Tricarico, E., Gherardi, F., Olenin, S., Gollasch, S. (2010). The top 27 alien animal species intentionally introduced by European aquaculture and related activities: stocking, sport fishery and ornamental purposes. Journal of Applied Ichthyology, 26, 1-7.
38. Schrimpf, A., Pârvulescu, L., Copila-Ciocianu, D., Petrusek, A., Schulz, R. (2012). Crayfish plague pathogen detected in the Danube Delta - a potential threat to freshwater biodiversity in southeastern Europe. Aquatic Invasions, 7(4), 503-510.
39. Shen, Y., Kang, J., Chen, W., He, S. (2015). DNA barcoding for the identification of common economic aquatic products in Central China and its application for the supervision of the market trade. Food Control, 61, 79-91.
40. Souty-Grosset, C., Anastácio, PM., Aquiloni, L., Banha, F., Choquer, J., Chucholl, C., Tricarico, E. (2016). The red swamp crayfish Procambarus clarkii in Europe: Impacts on aquatic ecosystems and human well-being. Limnologica, 58, 78-93.
41. Suárez-Serrano, A., Alcaraz, C., Ibáñez, C., Trobajo, R., Barata, C. (2010). Procambarus clarkii as a bioindicator of heavy metal pollution sources in the lower Ebro River and Delta. Ecotoxicology and Environmental Safety, 73(3), 280-286.
42. Sundseth, K. (2014). Invasive Alien Species. A European response. [http://ec.europa.eu/environment/ nature/invasivealien/docs/ias-brochure-en-web.pdf]. Accessed 5th May, 2017.
43. Svoboda, J., Strand, D.A., Vrålstad, T., Grandjean, F., Edsman, L., Kozák, P., Kouba, A., Fristad, R.F., Bahadir Koca, S., Petrusek, A. (2014) The crayfish plague pathogen can infect freshwater inhabiting crabs. Freshwater Biology, 59, 918-929.
44. Torres, E., Alvarez, F. (2010). Genetic variation in native and introduced populations of the red swamp crayfish Procambarus clarkii (Girard, 1852) (Crustacea, Decapoda, Cambaridae) in Mexico and Costa Rica. Aquatic Invasions, 7(2), 235-241.
45. Van der Wal, J.M., Dorenbosch, M., Immers, A.K., Vidal Forteza, C., Geurts, J.J.M., Peeters, E.T.H., Koese, B., Bakker, E.S. (2013). Invasive crayfish threaten the development of submerged macrophytes in lake restoration. PLoS One, 8(10), e78579.
46. Vojkovská, R., Horká, I., Tricarico, E. Ďuriš, Z. (2014). New record of the parthenogenetic marbled crayfish Procambarus fallax f. virginalis from Italy. Crustaceana, 87, 1386-1392.
47. Wizen, G., Galil, B.S., Shlagman, A., Gasith A. (2008). First record of red swamp crayfish, Procambarus clarkii (Girard, 1852) (Crustacea: Decapoda: Cambaridae) in Israel - too late to eradicate? Aquatic Invasions, 3(2), 181-185.