In this study, we experimentally evaluated how the feeding behaviour of marbled crayfish Procambarus virginalis is influenced by cues from conspecifics and the round goby Neogobius melanostomus, a fish predator, in tanks that permitted chemical communication but not visual recognition. We used four experimental groups with different combinations in two sub-tanks. The first sub-tank always contained a crayfish and prey (40 individuals of the water louse Asellus aquaticus). The other sub-tanks were set up as follows: (i) empty, serving as a control (C); (ii) with a conspecific crayfish (Cr); (iii) with a round goby (G) to simulate predator-only odour; and (iv) a round goby and three small conspecific crayfish (G + Cr) to simulate the presence of a predator and/or the alarm odour. Two sub-treatments were defined for the fourth group, categorised as 'injured' or 'not injured' depending on whether prey crayfish were visibly injured or not, respectively. We observed a significant decline in the consumption of water lice in the G and G + Cr treatments compared to the C and Cr treatments (up to 47% on average). There were no significant differences in consumption between the G and G + Cr treatments, or C and Cr treatments. No significant differences in food consumption parameters were detected between sub-treatments with 'injured' and 'not injured' conspecific crayfish. Knowledge of modifications in the feeding behaviour of marbled crayfish in the presence of round goby (and fish predators in general) is essential for ecologists attempting to understand the changes and impacts occurring in invaded freshwater ecosystems.

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses University of South Bohemia in České Budějovice Zátiší 728 2 389 25 Vodňany Czech Republic

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Reynolds J, Souty-Grosset C, Richardson A. Ecological roles of crayfish in freshwater and terrestrial habitats. Freshw. Crayfish. 2013;19:197–218. doi: 10.5869/fc.2013.v19-2.197. DOI

Veselý L, et al. The crayfish distribution, feeding plasticity, seasonal isotopic variation and trophic role across ontogeny and habitat in a canyon-shaped reservoir. Aquat. Ecol. 2020;54:1169–1183. doi: 10.1007/s10452-020-09801-w. DOI

Costantini ML, et al. The role of alien fish (the centrarchid Micropterus salmoides) in lake food webs highlighted by stable isotope analysis. Freshw. Biol. 2018;63:1130–1142. doi: 10.1111/fwb.13122. DOI

Reynolds JD. A review of ecological interactions between crayfish and fish, indigenous and introduced. Knowl. Manag. Aquat. Ecosyst. 2011 doi: 10.1051/kmae/2011024. DOI

Gherardi F. Biological Invaders in Inland Waters: Profiles, Distribution, and Threats. Springer; 2007.

Kouba A, Petrusek A, Kozák P. Continental-wide distribution of crayfish species in Europe: Update and maps. Knowl. Manag. Aquat. Ecosyst. 2014 doi: 10.1051/kmae/2014007. DOI

EU. Commission Implementing Regulation (EU) 2016/1141 of 13 July 2016 adopting a list of invasive alien species of Union concern pursuant to Regulation (EU) No 1143/2014 of the European Parliament and of the Council. Off. J. Eur. Union, L189, 4–8 (2016).

EU. Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Off. J. Eur. Union57, 35–55 (2014).

Weiperth A, et al. Hungary: A European hotspot of non-native crayfish biodiversity. Knowl. Manag. Aquat. Ecosyst. 2020 doi: 10.1051/kmae/2020035. DOI

Weiperth A, et al. Cambarellus patzcuarensis in Hungary: The first dwarf crayfish established outside of North America. Biologia. 2017;72:1529–1532. doi: 10.1515/biolog-2017-0159. DOI

Veselý L, et al. Trophic niches of three sympatric invasive crayfish of EU concern. Hydrobiologia. 2021;848:727–737. doi: 10.1007/s10750-020-04479-5. DOI

Brown GE, Paige JA, Godin JGJ. Chemically mediated predator inspection behaviour in the absence of predator visual cues by a characin fish. Anim. Behav. 2000;60:315–321. doi: 10.1006/anbe.2000.1496. PubMed DOI

Chivers DP, Smith RJF. Chemical alarm signalling in aquatic predator-prey systems: A review and prospectus. Ecoscience. 1998;5:338–352. doi: 10.1080/11956860.1998.11682471. DOI

Schoeppner NM, Relyea RA. Interpreting the smells of predation: How alarm cues and kairomones induce different prey defences. Funct. Ecol. 2009;23:1114–1121. doi: 10.1111/j.1365-2435.2009.01578.x. DOI

Kats LB, Dill LM. The scent of death: Chemosensory assessment of predation risk by prey animals. Ecoscience. 1998;5:361–394. doi: 10.1080/11956860.1998.11682468. DOI

Relyea RA. How prey respond to combined predators: A review and an empirical test. Ecology. 2003;84:1827–1839. doi: 10.1890/0012-9658(2003)084[1827:Hprtcp]2.0.Co;2. DOI

Covich AP, Crowl TA, Alexander JE, Vaughn CC. Predator avoidance responses in freshwater decapod–gastropod interactions mediated by chemical stimuli. J. N. Am. Benthol. Soc. 1994;13:283–290. doi: 10.2307/1467246. DOI

Pettersson LB, Nilsson PA, Bronmark C. Predator recognition and defence strategies in crucian carp, Carassius carassius. Oikos. 2000;88:200–212. doi: 10.1034/j.1600-0706.2000.880122.x. DOI

Brown GE, Dreier VM. Predator inspection behaviour and attack cone avoidance in a characin fish: The effects of predator diet and prey experience. Anim. Behav. 2002;63:1175–1181. doi: 10.1006/anbe.2002.3024. DOI

Mirza RS, Chivers DP. Do juvenile yellow perch use diet cues to assess the level of threat posed by intraspecific predators? Behaviour. 2001;138:1249–1258. doi: 10.1163/15685390152822201. DOI

Bryer PJ, Mirza RS, Chivers DP. Chemosensory assessment of predation risk by slimy sculpins (Cottus cognatus): Responses to alarm, disturbance, and predator cues. J. Chem. Ecol. 2001;27:533–546. doi: 10.1023/a:1010332820944. PubMed DOI

McCarthy TM, Fisher WA. Multiple predator-avoidance behaviours of the freshwater snail Physella heterostropha pomila: Responses vary with risk. Freshw. Biol. 2000;44:387–397. doi: 10.1046/j.1365-2427.2000.00576.x. DOI

Berg LS. Freshwater fishes of the USSR and adjacent countries. Isr. Program Sci. Transl. Jerusalem. 1949;2:496.

Stráňai I, Andreji J. The first report of round goby, Neogobius melanostomus (Pisces, Gobiidae) in the waters of Slovakia. Folia Zool. 2004;53:335–338.

Borcherding J, et al. Non-native Gobiid species in the lower River Rhine (Germany): Recent range extensions and densities. J. Appl. Ichthyol. 2011;27:153–155. doi: 10.1111/j.1439-0426.2010.01662.x. DOI

Janáč M, Šlapanský L, Valová Z, Jurajda P. Downstream drift of round goby (Neogobius melanostomus) and tubenose goby (Proterorhinus semilunaris) in their non-native area. Ecol. Freshw. Fish. 2013;22:430–438. doi: 10.1111/eff.12037. DOI

Jude DJ, Reider RH, Smith GR. Establishment of Gobidae in the Great Lakes basin. Can. J. Fish. Aquat. Sci. 1992;49:416–421. doi: 10.1139/f92-047. DOI

Kornis MS, Mercado-Silva N, Vander Zanden MJ. Twenty years of invasion: A review of round goby Neogobius melanostomus biology, spread and ecological implications. J. Fish Biol. 2012;80:235–285. doi: 10.1111/j.1095-8649.2011.03157.x. PubMed DOI

Bij de Vaate A, Jazdzewski K, Ketelaars HAM, Gollasch S, Van der Velde G. Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can. J. Fish. Aquat. Sci. 2002;59:1159–1174. doi: 10.1139/f02-098. DOI

Galil BS, Nehring S, Panov V. Biological Invasions. Springer; 2008. pp. 59–74.

Hirsch PE, N'Guyen A, Burkhardt-Holm P. Hobbyists acting simultaneously as anglers and aquarists: Novel pathways for non-native fish and impacts on native fish. Aquat. Conserv. Mar. Freshw. Ecosyst. 2021;31:1285–1296. doi: 10.1002/aqc.3557. DOI

Laverty C, et al. Assessing the ecological impacts of invasive species based on their functional responses and abundances. Biol. Invasions. 2017;19:1653–1665. doi: 10.1007/s10530-017-1378-4. DOI

Roje S, et al. Comparison of behavior and space use of the european bullhead Cottus gobio and the round goby Neogobius melanostomus in a simulated natural habitat. Biology. 2021 doi: 10.3390/biology10090821. PubMed DOI PMC

Gebauer R, et al. Prediction of ecological impact of two alien gobiids in habitat structures of differing complexity. Can. J. Fish. Aquat. Sci. 2019;76:1954–1961. doi: 10.1139/cjfas-2018-0346. DOI

Prášek V, Jurajda P. Expansion of Proterorhinus marmoratus in the Morava River basin (Czech Republic, Danube R. watershed) Folia Zool. 2005;54:189–192.

Buřič M, Bláha M, Kouba A, Drozd B. Upstream expansion of round goby (Neogobius Melanostomus) - first record in the upper reaches of the Elbe river. Knowl. Manag. Aquat. Ecosyst. 2015 doi: 10.1051/kmae/2015029. DOI

Hossain MS, Patoka J, Kouba A, Buřič M. Clonal crayfish as biological model: A review on marbled crayfish. Biologia. 2018;73:841–855. doi: 10.2478/s11756-018-0098-2. DOI

Patoka J, et al. Predictions of marbled crayfish establishment in conurbations fulfilled: Evidences from the Czech Republic. Biologia. 2016;71:1380–1385. doi: 10.1515/biolog-2016-0164. DOI

Szendőfi B, et al. Occurrence of exotic fish and crayfish species in Barát and Dera creeks and their adjacent section of the River Danube. Pisces Hungarici. 2018;12:47–51.

Stein RA. Selective predation, optimal foraging, and the predator-prey interaction between fish and crayfish. Ecology. 1977;58:1237–1253. doi: 10.2307/1935078. DOI

Pirtle JL, Eckert GL, Stoner AW. Habitat structure influences the survival and predator-prey interactions of early juvenile red king crab Paralithodes camtschaticus. Mar. Ecol. Prog. Ser. 2012;465:169–184. doi: 10.3354/meps09883. DOI

Preisser EL, Bolnick DI, Benard MF. Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology. 2005;86:501–509. doi: 10.1890/04-0719. DOI

Hamrin SF. Seasonal crayfish activity as influenced by fluctuating water levels and presence of a fish predator. Holarct. Ecol. 1987;10:45–51.

Blake M, Hart P. The behavioural responses of juvenile signal crayfish Pacifastacus leniusculus to stimuli from perch and eels. Freshw. Biol. 1993;29:89–97. doi: 10.1111/j.1365-2427.1993.tb00747.x. DOI

Acquistapace P, Daniels WH, Gherardi F. Behavioral responses to 'alarm odors' in potentially invasive and non-invasive crayfish species from aquaculture ponds. Behaviour. 2004;141:691–702. doi: 10.1163/1568539042245204. DOI

Hazlett BA, Acquistapace P, Gherardi F. Differences in memory capabilities in invasive and native crayfish. J. Crustac. Biol. 2002;22:439–448. doi: 10.1651/0278-0372(2002)022[0439:Dimcii]2.0.Co;2. DOI

Helfman GS. Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav. Ecol. Sociobiol. 1989;24:47–58. doi: 10.1007/bf00300117. DOI

Beattie MC, Moore PA. Predator recognition of chemical cues in crayfish: Diet and experience influence the ability to detect predation threats. Behaviour. 2018;155:505–529. doi: 10.1163/1568539x-00003501. DOI

Jurcak AM, Moore PA. Sensory signals and the reaction space in predator-prey interactions. Hydrobiologia. 2018;816:137–152. doi: 10.1007/s10750-018-3574-3. DOI

Wood TC, Kelley RE, Moore PA. Feeding in fear: Indirect effects of predatory fish on macrophyte communities mediated by altered crayfish foraging behaviour. Freshw. Biol. 2018;63:1523–1533. doi: 10.1111/fwb.13181. DOI

Veselý L, et al. Effects of prey density, temperature and predator diversity on nonconsumptive predator-driven mortality in a freshwater food web. Sci.c Rep. 2017;7:18075. doi: 10.1038/s41598-017-17998-4. PubMed DOI PMC

Christensen, R. H. B., & Christensen, M. R. H. B. Package ‘ordinal’. Stand, 19 (2015).

Ferincz A, et al. Risk assessment of non-native fishes in the catchment of the largest Central-European shallow lake (Lake Balaton, Hungary) Hydrobiologia. 2016;780:85–97. doi: 10.1007/s10750-016-2657-2. DOI

Church K, Iacarella JC, Ricciardi A. Aggressive interactions between two invasive species: The round goby (Neogobius melanostomus) and the spinycheek crayfish (Orconectes limosus) Biol. Invasions. 2017;19:425–441. doi: 10.1007/s10530-016-1288-x. DOI

Adámek Z, Mikl L, Šlapanský L, Jurajda P, Halačka K. The diet of predatory fish in drinking water reservoirs—How can they contribute to biomanipulation efforts? J. Vertebr. Biol. 2019;68:215–224. doi: 10.25225/fozo.014.2019. DOI

Franta P, et al. The invasive round goby Neogobius melanostomus as a potential threat to native crayfish populations. Animals. 2021 doi: 10.3390/ani11082377. PubMed DOI PMC

Roje S, et al. Round goby versus marbled crayfish: Alien invasive predators and competitors. Knowl. Manag. Aquat. Ecosyst. 2021 doi: 10.1051/kmae/2021019. DOI

Gherardi F, Mavuti KM, Pacini N, Tricarico E, Harper DM. The smell of danger: Chemical recognition of fish predators by the invasive crayfish Procambarus clarkii. Freshw. Biol. 2011;56:1567–1578. doi: 10.1111/j.1365-2427.2011.02595.x. DOI

Gherardi F, Aquiloni L, Tricarico E. Behavioral plasticity, behavioral syndromes and animal personality in crustacean decapods: An imperfect map is better than no map. Curr. Zool. 2012;58:567–579. doi: 10.1093/czoolo/58.4.567. DOI

Reisinger LS, Elgin AK, Towle KM, Chan DJ, Lodge DM. The influence of evolution and plasticity on the behavior of an invasive crayfish. Biol. Invasions. 2017;19:815–830. doi: 10.1007/s10530-016-1346-4. DOI

Hazlett BA. Predator recognition and learned irrelevance in the crayfish Orconectes virilis. Ethology. 2003;109:765–780. doi: 10.1046/j.1439-0310.2003.00916.x. DOI

Ferrari MCO, Wisenden BD, Chivers DP. Chemical ecology of predator-prey interactions in aquatic ecosystems: A review and prospectus. Can. J. Zool. 2010;88:698–724. doi: 10.1139/z10-029. DOI

Pauwels K, Stoks R, De Meester L. Coping with predator stress: Interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna. J. Evol. Biol. 2005;18:867–872. doi: 10.1111/j.1420-9101.2005.00890.x. PubMed DOI

Barton BA. Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integr. Comp. Biol. 2002;42:517–525. doi: 10.1093/icb/42.3.517. PubMed DOI

Hawlena D, Schmitz OJ. Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am. Nat. 2010;176:537–556. doi: 10.1086/656495. PubMed DOI

Ramberg-Pihl NC, Yurewicz KL. Behavioral responses of northern crayfish (Faxonius virilis) to conspecific alarm cues and predator cues from smallmouth bass (Micropterus dolomieu) Mar. Freshw. Behav. Physiol. 2020;53:1–16. doi: 10.1080/10236244.2020.1717338. DOI

Pecor KW, Deering CM, Firnberg MT, Pastino AK, Wolfson SJ. The use of conspecific and heterospecific alarm cues by virile crayfish (Orconectes virilis) from an exotic population. Mar. Freshw. Behav. Physiol. 2010;43:37–44. doi: 10.1080/10236241003658353. DOI

Ferrari MCO, Brown GE, Chivers DP. Understanding the effect of uncertainty on the development of neophobic antipredator phenotypes. Anim. Behav. 2018;136:101–106. doi: 10.1016/j.anbehav.2017.11.024. DOI

Parsons MH, et al. Biologically meaningful scents: A framework for understanding predator-prey research across disciplines. Biol. Rev. 2018;93:98–114. doi: 10.1111/brv.12334. PubMed DOI

Clark JL, Moore PA. The role of sensory modalities in producing nonconsumptive effects for a crayfish-bass predator-prey system. Can. J. Zool. 2018;96:680–691. doi: 10.1139/cjz-2017-0109. DOI

Bouwma P, Hazlett BA. Integration of multiple predator cues by the crayfish Orconectes propinquus. Anim. Behav. 2001;61:771–776. doi: 10.1006/anbe.2000.1649. DOI

Ferrari MCO, Messier F, Chivers DP, Messier O. Can prey exhibit threat-sensitive generalization of predator recognition? Extending the predator recognition continuum hypothesis. Proc. R. Soc. B-Biol. Sci. 2008;275:1811–1816. doi: 10.1098/rspb.2008.0305. PubMed DOI PMC

Kubec J, Kouba A, Buřič M. Communication, behaviour, and decision making in crayfish: A review. Zool. Anz. 2019;278:28–37. doi: 10.1016/j.jcz.2018.10.009. DOI

Didonato GT, Lodge DM. Species replacements among Orconectes crayfishes in wisconsin lakes: The role of predation by fish. Can. J. Fish. Aquat. Sci. 1993;50:1484–1488. doi: 10.1139/f93-169. DOI

Stein RA, Magnuson JJ. Behavioral response of crayfish to a fish predator. Ecology. 1976;57:751–761. doi: 10.2307/1936188. DOI

Keller TA, Moore PA. Context-specific behavior: Crayfish size influences crayfish-fish interactions. J. N. Am. Benthol. Soc. 2000;19:344–351. doi: 10.2307/1468076. DOI