Abstract
Successful invasive species compete for the same available resources with related native species, frequently driving the latter to the cusp of extirpation because of a lack of adaptive response. In this paper we analysed the behavioural relationships between two species of crayfish, the native Astacus leptodactylus and the invasive Orconectes limosus in an ongoing invasion process in the Lower Danube, in Eastern Europe. We tested the species’ ability to acquire shelter and food in laboratory experiments in both intra- and interspecific confrontations. The dominant behaviour of the invasive species is obvious even towards its own congeners, while the native species display a more tolerant conspecific behaviour. With respect to interspecific confrontation, the invasive crayfish males and females were inclined to sex-specific dominance regarding shelters. A roughly balanced behaviour was noted for intersexual confrontations. The results of this study also highlight that the occupancy of a shelter is more disputed than food resources, which appear to be opportunistically acquired. In the context of the current invasion process, we hypothesised that the effect caused by interference competition might lead to a decline of the native species. Further investigations may reveal if there is any hope for recovery of the native species.
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Ackefors H. 1996. The development of crayfish culture in Sweden during the last decade. Freshwater Crayfish 11 1): 627–654.
Aquiloni L., Gonçalves V., Inghilesi A.F. & Gherardi F. 2012. Who’s what? Prompt recognition of social status in crayfish. Behav. Ecol. Sociobiol. 66 5): 785–790. DOI: https://doi.org/10.1007/S00265-012-1326-3
Barki A. & Karplus I. 2016. The behavioral mechanism of competition for food between tilapia (Oreochromis hybrid) and crayfish (Cherax quadricarinatus). Aquaculture 450: 162–167. DOI: https://doi.org/10.1016/j.aquaculture.2015.07.031
Bergman D.A. & Moore P.A. 2003. Field observations of intraspe-cific agonistic behavior of two crayfish species, Orconectes rusticus and Orconectes virilis, in different habitats. Biol. Bull. 205 (1): 26–35. DOI: https://doi.org/10.2307/1543442
Bouckaert E.K., Auer N.A., Roseman E.F. & Boase J. 2014. Verifying success of artificial spawning reefs in the St. Clair- Detroit River System for lake sturgeon (Acipenser fulvescens Rafinesque, 1817). J. Appl. Ichthyol. 30: 1393–1401. DOI: https://doi.org/10.1111/jai.l2603
Broennimann O., Treier U.A., Müller-Schärer H., Thuiller W., Peterson A.T. & Guisan A. 2007. Evidence of climatic niche shift during biological invasion. Ecol. Lett. 10: 701–709. DOI: https://doi.org/10.1111/j.1461-0248.2007.01060.x
Bufic M., Kouba A. & Kozák P. 2013. Reproductive plasticity in freshwater invader: from long-term sperm storage to parthenogenesis. PLoS One 8 (10): e77597. DOI: https://doi.org/10.1371/journal.pone.0077597
Bufic M., Kozák P. & Kouba A. 2009. Movement patterns and ranging behavior of the invasive spiny-cheek crayfish in a small reservoir tributary. Fundam. Appl. Limnol. 174 (4): 329–337. DOI: https://doi.org/10.1127/1863-9135/2009/0174-0329
Christy J.H. 1987. Competitive mating, mate choice and mating associations of brachyuran crabs. Bull. Mar. Sci. 41 (2): 177–191.
Chuang A. & Peterson C.R. 2016. Expanding population edges: theories, traits, and trade-offs. Glob. Change Biol. 22 (2): 494–512. DOI: https://doi.org/10.1111/gcb.13107
Chucholl C. 2013. Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol. Invasions 15 (1): 125–141. DOI: https://doi.org/10.1007/sl0530-012-0273-2
Chucholl C. 2016. The bad and the super-bad: prioritising the threat of six invasive alien to three imperilled native crayfishes. Biol. Invasions 18 7): 1967–1988. DOI: https://doi.org/10.1007/sl0530-016-1141-2
Figler M.H., Blank G.S. & Peeke H.V. 1997. Maternal aggression and post-hatch care in red swamp crayfish, Procambarus clarkii (Girard): The influences of presence of offspring, fostering, and maternal molting. Mar. Freshwater Behav. Physiol. 30 (3): 173–194. DOI: https://doi.org/10.1080/10236249709379023
Garvey J.E., Stein R.A. & Thomas H.M. 1994. Assessing how fish predation and interspecific prey competition influence a crayfish assemblage. Ecology 75 (2): 532–547. DOI: https://doi.org/10.2307/1939556
Gherardi F. 2006. Crayfish invading Europe: the case study of Procambarus clarkii. Mar. Freshwater Behav. Physiol. 39 3): 175–191. DOI: https://doi.org/10.1080/10236240600869702
Grow L. & Merchant H. 1980. The burrow habitat of the crayfish, Cambarus diogenes diogenes (Girard). Am. Midi. Nat. 103 (2): 231–237. DOI: https://doi.org/10.2307/2424621
Groza M.I., Pop-Vancia V. & Miretan V. 2016. Diel activity and use of multiple artificially constructed shelters in Astacus lep-todactylus (Decapoda: Astacidae). Biologia 71 (12): 1369–1379. DOI: https://doi.org/10.1515/biolog-2016-0167
Guan R.Z. 1994. Burrowing behaviour of signal crayfish, Pacifas-tacus leniusculus (Dana), in the River Great Ouse, England. Freshwater Forum 4 3): 155–168.
Hirsch P.E., Burkhardt-Holm P., Töpfer I. & Fischer P. 2016. Movement patterns and shelter choice of spiny-cheek crayfish (Orconectes limosus) in a large lake’s littoral zone. Aquat. Invasions 11 (1): 55–65. DOI: https://doi.org/10.3391/ai.2016.11.1.06
Hudina S., Galic N., Roessink I. & Hock K. 2011. Competitive interactions between co-occurring invaders: identifying asymmetries between two invasive crayfish species. Biol. Invasions 13 (8): 1791–1803. DOI: https://doi.org/10.1007/sl0530-010-9933-2
Hudina S., Zganec K. & Hock K. 2015. Differences in aggressive behaviour along the expanding range of an invasive crayfish: an important component of invasion dynamics. Biol. Invasions 17 (11): 3101–3112. DOI: https://doi.org/10.1007/sl0530-015-0936-x
Ilhéu M., Acquistapace P., Benvenuto C. & Gherardi F. 2003. Shelter use of the Red-Swamp Crayfish (Procambarus clarkii) in dry-season stream pools. Arch. Hydrobiol. 157 (4): 535–546. DOI: https://doi.org/10.1127/0003-9136/2003/0157-0535
Imhoff E.M., Mortimer R.J.G., Christmas M. & Dunn A.M. 2011. Invasion progress of the signal crayfish Pacifastacus leniusculus (Dana) and displacement of the native white-clawed crayfish Austropotamobius pallipes (Lereboullet) in the River Wharfe, UK. Freshwater Crayfish 18: 45–53. DOI:https://doi.org/10.5869/fc.2011.vl8.45
Kaczer L., Pedetta S. & Maldonado H. 2007. Aggressiveness and memory: subordinate crabs present higher memory ability than dominants after an agonistic experience. Neurobiol. Learn. Mem. 87 1): 140–148. DOI: https://doi.org/10.1016/j.nlm.2006.08.002
Kawai N., Kono R. & Sugimoto S. 2004. Avoidance learning in the crayfish (Procambarus clarkii) depends on the predatory imminence of the unconditioned stimulus: a behavior systems approach to learning in invertebrates. Behav. Brain Res. 150 (1-2): 229–237. DOI: https://doi.org/10.1016/S0166-4328(03)00261-4
Klocker C.A. & Strayer D.L. 2004. Interactions among an invasive crayfish (Orconectes rusticus), a native crayfish (Orconectes limosus), and native bivalves (Sphaeriidae and Unionidae). Northeast. Nat. 11 (2): 167–178. DOI: https://doi.org/10.1656/1092-6194(2004)011[0167:IAAICO]2.0.CO;2
Kouba A., Petrusek A. & Kozák P. 2014. Continental-wide distribution of crayfish species in Europe: update and maps. Knowl. Managt. Aquatic Ecosyst. 413: article number 05, 21 pp. DOI: https://doi.org/10.1051/kmae/2014007
Lee C.E. 2002. Evolutionary genetics of invasive species. Trends Ecol. Evol. 17 (8): 386–391. DOI: https://doi.org/10.1016/S0169-5347(02)02554-5
Leon M., Merner M.J., Dreyer A.A., Cooper A., Scott L., Berendzen P.B., McCullough D.A. & Merten E.C. 2016. Range expansion of the invasive rusty crayfish Orconectes rusticus (Girard, 1852) (Decapoda: Astacoidea) in northeastern Iowa (USA) rivers. J. Crust. Biol. 36 1): 99–104. DOI: https://doi.org/10.1163/1937240X-00002397
Lodge D.M., Deines A., Gherardi F., Yeo D.C., Arcella T., Baldridge A.K., Barnes M.A., Chadderton W.L., Feder J.L., Gantz C.A. & Howard G.W. 2012. Global introductions of crayfishes: Evaluating the impact of species invasions on ecosystem services. Annu. Rev. Ecol. Evol. Syst. 43: 449–472. DOI: https://doi.org/10.1146/annurev-ecolsys-111511-103919
Mathers K.L., Chadd R.P., Dunbar M.J., Extence C.A., Reeds J., Rice S.P. & Wood P.J. 2016. The long-term effects of invasive signal crayfish (Pacifastacus leniusculus) on instream macroinvertebrate communities. Sci. Total Environ. 556: 207–218. DOI: https://doi.org/10.1016/j.scitotenv.2016.01.215
Matsuzaki S.I.S., Sakamoto M., Kawabe K. & Takamura N. 2012. A laboratory study of the effects of shelter availabil ity and invasive crayfish on the growth of native stream fish. Freshwater Biol. 57 (4): 874–882. DOI: https://doi.org/10.1111/j.1365-2427.2012.02743.x
Meade M.E. & Watts S.A. 1995. Weight gain and survival of juvenile Australian crayfish Cherax quadricarinatus fed formulated feeds. J. World Aquacult. Soc. 26 4): 469–474. DOI: https://doi.org/10.1111/j.1749-7345.1995.tb00845.x
Momot W.T. 1995. Redefining the role of crayfish in aquatic ecosystems. Rev. Fish. Sci. 3 1): 33–63. DOI: https://doi.org/10.1080/10641269509388566
Moore P.A. & Bergman D.A. 2005. The smell of success and failure: the role of intrinsic and extrinsic chemical signals on the social behavior of crayfish. Integr. Comp. Biol. 45(4): 650–657. DOI: https://doi.org/10.1093/icb/45.4.650.
Musil M., Buřič M., Policar T., Kouba A. & Kozák P. 2010. Comparison of diurnal and nocturnal activity between noble crayfish (Astacus astacus) and spinycheek crayfish (Orconectes limosus). Freshwater Crayfish 17: 189–193.
Oidtmann B., Heitz E., Rogers D. & Hoffmann R.W. 2002. Transmission of crayfish plague. Dis. Aquat. Org. 52: 159–67. DOI: https://doi.org/10.3354/dao052159
Pârvulescu L., Paloş& Molnar P. 2009. First record of the spiny-cheek crayfish Orconectes limosus (Rafinesque, 1817) (Crustacea: Decapoda: Cambaridae) in Romania. North-West. J. Zool. 5 2): 424–428.
Pârvulescu L., Pîrvu M., Moroşan L.G. & Zaharia C. 2015. Plasticity in fecundity highlights the females’ importance in the spiny-cheek crayfish invasion mechanism. Zoology 118 (6): 424–432. DOI: https://doi.org/10.1016/j.zool.2015.08.003
Pârvulescu L., Schrimpf A., Kozubíková E., Cabanillas Resino S., Vrålstad T., Petrusek A. & Schulz R. 2012. Invasive crayfish and crayfish plague on the move: first detection of the plague agent Aphanomyces astaci in the Romanian Danube. Dis. Aquat. Org. 98 1): 85–94. DOI: https://doi.org/10.3354/dao02432.
Preisser E.L., Bolnick D.I. & Benard M.F. 2005. Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86 2): 501–509. DOI: https://doi.org/10.1890/04-0719
Puky M. & Schád P. 2006. Orconectes limosus colonises new areas fast along the Danube in Hungary. Bull. Fr. Pêche Piscic. 380–381: 919–926. DOI: https://doi.org/10.1051/kmae:2006031
R Core Team. 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org.
Rahel F.J. & Stein R.A. 1988. Complex predator-prey interactions and predator intimidation among crayfish, piscivorous fish, and small benthic fish. Oecologia 75 (1): 94–98. DOI: https://doi.org/10.1007/BF00378819
Rebrina F., Skejo J., Lucic A. & Hudina S. 2015. Trait variability of the signal crayfish (Pacifastacus leniusculus) in a recently invaded region reflects potential benefits and tradeoffs during dispersal. Aquat. Invasions 10 (1): 41–50. DOI: https://doi.org/10.3391/ai.2015.10.1.04
Schrimpf A., Pârvulescu L., Copilaş-Ciocianu D., Petrusek A. & Schulz R. 2012. Crayfish plague pathogen detected in the Danube Delta — a potential threat to freshwater biodiversity in southeastern Europe. Aquat. Invasions 7 4): 503–510. DOI: https://doi.org/10.3391/ai.2012.7.4.007
Skurdal J. & Taugbøl T. 2002. Crayfish of commercial importance: Astacus, Part II, pp. 467–510. In: Holdich D.M. (ed.), Biology of Freshwater Crayfish, Blackwell Science, Oxford and Maiden, Massachusetts, 702 pp. ISBN: 1405123494, 9781405123495
Snedden W.A. 1990. Determinants of male mating success in the temperate crayfish Orconectes rusticus: chela size and sperm competition. Behaviour 115 (1): 100–113. DOI: https://doi.org/10.1163/156853990X00301
Soderback B. 1994. Interactions among juveniles of two freshwater crayfish species and a predatory fish. Oecologia 100 (3): 229–235. DOI: https://doi.org/10.1007/BF00316949.
Stebbing P.D., Bentley M.G. & Watson G.J. 2003. Mating behaviour and evidence for a female released courtship pheromone in the signal crayfish Pacifastacus leniusculus. J. Chem. Ecol. 29 2): 465–475. DOI: https://doi.org/10.1023/A:1022646414938
Stocker A.M. & Huber R. 2001. Fighting strategies in crayfish Orconectes rusticus (Decapoda, Cambaridae) differ with hunger state and the presence of food cues. Ethology 107 (8): 727–736. DOI: https://doi.org/10.1046/j.1439-0310.2001.00705.x
Václavík T. & Meentemeyer R.K. 2012. Equilibrium or not? Modelling potential distribution of invasive species in different stages of invasion. Divers. Distrib. 18 (1): 73–83. DOI: https://doi.org/10.1111/j.1472-4642.2011.00854.x
Vorburger C. & Ribi G. 1999. Aggression and competition for shelter between a native and an introduced crayfish in Europe. Freshwater Biol. 42 1): 111–119. DOI: https://doi.org/10.1046/j.1365-2427.1999.00465.x
Walles B., Troost K., van den Ende D., Nieuwhof S., Smaal A.C. & Ysebaert T. 2016. From artificial structures to self-sustaining oyster reefs. J. Sea Res. 108: 1–9. DOI: https://doi.org/10.1016/j.seares.2015.11.007
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Lele, SF., Pârvulescu, L. Experimental evidence of the successful invader Orconectes limosus outcompeting the native Astacus leptodactylus in acquiring shelter and food. Biologia 72, 877–885 (2017). https://doi.org/10.1515/biolog-2017-0094
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DOI: https://doi.org/10.1515/biolog-2017-0094