Multisensory stimuli provide organisms with information to assess the threat present in the surroundings. Olfactory cues show dominance over other sensory modalities in the aquatic environment. The impact of chemical predator cues combined with experiences gained (learning) in species without previous contact is not fully understood. We investigated the foraging and shelter-seeking behaviour of naïve and experienced marbled crayfish Procambarus virginalis juveniles in response to the chemical signals of pumpkinseed Lepomis gibbosus alone and in combination with alarm chemicals produced by preyed-upon conspecifics. Naïve and experienced (previously exposed to pumpkinseed predation) juveniles were stocked in an arena with shelter and feed and exposed (1) to water from a tank containing a predator actively feeding on conspecifics, (2) water from a tank with predator only and (3) water only as control. Crayfish exposed to the combined stimuli avoided the inlet zone and gravitated to shelter zone of the arena to a greater extent than did those exposed to predator-only cues and the control. Regardless of the treatment, experienced crayfish showed significantly reduced interest in feeding. Our findings imply that crayfish response to threat-associated odours with the greatest potency when visual or tactile cues are present, while previous encounters with predators may make them more cautious.

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

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Acquistapace, P. , Hazlett, B. A. , Gherardi, F. , Animale, B. , & Pardi, L. (2003). Unsuccessful predation and learning of predator cues by crayfish. Journal of Crustacean Biology, 23(2), 364–370. 10.1126/science.1198111 DOI

Bairos‐Novak, K. R. , Ferrari, M. C. O. , & Chivers, D. P. (2019). A novel alarm signal in aquatic prey: Familiar minnows coordinate group defences against predators through chemical disturbance cues. Journal of Animal Ecology, 88(9), 1281–1290. 10.1111/1365-2656.12986 PubMed DOI

Bates, D. , Mächler, M. , Bolker, B. , & Walke, S. (2015). Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67(1), 1–48. 10.18637/jss.v067.i01 DOI

Beattie, M. C. , & Moore, P. A. (2018). Predator recognition of chemical cues in crayfish: Diet and experience influence the ability to detect predation threats. Behaviour, 155(6), 505–530. 10.1163/1568539X-00003501 DOI

Bergman, D. A. , Redman, C. N. , Fero, K. C. , Simon, J. L. , & Moore, P. A. (2006). The impacts of flow on chemical communication strategies and fight dynamics of crayfish. Marine and Freshwater Behaviour and Physiology, 39(4), 245–258. 10.1080/10236240600980608 DOI

Bobek, J. , Šmídová, K. , & Čihák, M. (2017). A waking review: Old and novel insights into the spore germination in Streptomyces. Frontiers in Microbiology, 8, 2205. 10.3389/fmicb.2017.02205 PubMed DOI PMC

Bouwma, P. , & Hazlett, B. A. (2001). Integration of multiple predator cues by the crayfish Orconectes propinquus . Animal Behaviour, 61(4), 771–776. 10.1006/anbe.2000.1649 DOI

Brown, C. , & Laland, K. N. (2003). Social learning in fishes: A review. Fish and Fisheries, 4(3), 280–288. 10.1046/j.1467-2979.2003.00122.x DOI

Brown, G. E. (2003). Learning about danger: Chemical alarm cues and local risk assessment in prey fishes. Fish and Fisheries, 4(3), 227–234. 10.1046/j.1467-2979.2003.00132.x DOI

Brown, G. E. , Chivers, D. P. , & Smith, R. J. F. (1995). Localized defecation by pike: A response to labelling by cyprinid alarm pheromone? Behavioral Ecology and Sociobiology, 36(2), 105–110. 10.1007/s002650050130 DOI

Clark, J. L. , & Moore, P. A. (2018). The role of sensory modalities in producing nonconsumptive effects for a crayfish–bass predator–prey system. Canadian Journal of Zoology, 96(7), 680–691. 10.1139/cjz-2017-0109 DOI

Copp, G. H. , & Fox, M. G. (2007). Growth and life history traits of introduced pumpkinseed (Lepomis gibbosus) in Europe, and the relevance to its potential invasiveness. In Gherardi F. (Ed.), Biological invaders in inland waters: Profiles, distribution, and threats (pp. 289–306). Springer Netherlands. 10.1007/978-1-4020-6029-8_15 DOI

Creed, R. P., Jr. , & Reed, J. M. (2004). Ecosystem engineering by crayfish in a headwater stream community. Journal of the North American Benthological Society, 23(2), 224–236.

Dalesman, S. , & Inchley, C. J. (2008). Interaction between olfactory and visual cues affects flight initiation and distance by the hermit crab, Pagurus bernhardus . Behaviour, 145(10), 1479–1492. 10.1163/156853908785765836 DOI

Ferrari, M. C. O. , Messier, F. , & Chivers, D. P. (2007a). Degradation of chemical alarm cues under natural conditions: Risk assessment by larval woodfrogs. Chemoecology, 17(4), 263–266. 10.1007/s00049-007-0381-0 DOI

Ferrari, M. C. O. , Messier, F. , & Chivers, D. P. (2007b). First documentation of cultural transmission of predator recognition by larval amphibians. Ethology, 113(6), 621–627. 10.1111/j.1439-0310.2007.01362.x DOI

Fox, M. G. , Vila‐Gispert, A. , & Copp, G. H. (2007). Life‐history traits of introduced Iberian pumpkinseed Lepomis gibbosus relative to native populations. Can differences explain colonization success? Journal of Fish Biology, 71, 56–69. 10.1111/j.1095-8649.2007.01683.x DOI

Galib, S. M. , Sun, J. , Twiss, S. D. , & Lucas, M. C. (2022). Personality, density and habitat drive the dispersal of invasive crayfish. Scientific Reports, 12(1), 1114. 10.1038/s41598-021-04228-1 PubMed DOI PMC

Gaynor, K. M. , Brown, J. S. , Middleton, A. D. , Power, M. E. , & Brashares, J. S. (2019). Landscapes of fear: Spatial patterns of risk perception and response. Trends in Ecology and Evolution, 34(4), 355–368. 10.1016/j.tree.2019.01.004 PubMed DOI

Gherardi, F. , Mavuti, K. M. , Pacini, N. , Tricarico, E. , & Harper, D. M. (2011). The smell of danger: Chemical recognition of fish predators by the invasive crayfish Procambarus clarkii . Freshwater Biology, 56(8), 1567–1578. 10.1111/j.1365-2427.2011.02595.x DOI

Glover, C. N. , Bucking, C. , & Wood, C. M. (2013). The skin of fish as a transport epithelium: A review. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 183(7), 877–891. 10.1007/s00360-013-0761-4 PubMed DOI

Gosselin, L. A. , & Qian, P. Y. (1997). Juvenile mortality in benthic marine invertebrates. Marine Ecology Progress Series, 146(1–3), 265–282. 10.3354/meps146265 DOI

Häberli, M. A. , Aeschlimann, P. B. , & Milinski, M. (2005). Sticklebacks benefit from closer predator inspection: An experimental test of risk assessment. Ethology Ecology and Evolution, 17(3), 249–259. 10.1080/08927014.2005.9522595 DOI

Hazlett, B. A. (2003). Predator recognition and learned irrelevance in the crayfish Orconectes virilis . Ethology, 109(9), 765–780. 10.1046/j.1439-0310.2003.00916.x DOI

Hazlett, B. A. , Acquistapace, P. , & Gherardi, F. (2002). Differences in memory capabilities in invasive and native crayfish. Journal of Crustacean Biology, 22(2), 439–448. 10.1163/20021975-99990251 DOI

Holdich, D. M. (2002). Biology of freshwater crayfish (Vol. 702, pp. 125–138). Blackwell Science.

Holmes, T. H. , & McCormick, M. I. (2010). Smell, learn and live: The role of chemical alarm cues in predator learning during early life history in a marine fish. Behavioural Processes, 83(3), 299–305. 10.1016/j.beproc.2010.01.013 PubMed DOI

Hossain, M. S. , Buřič, M. , & Moore, P. A. (2020). Exposure paradigm of fluoxetine impacted the Faxonius virilis agonistic behavior differently. Science of the Total Environment, 699, 134300. 10.1016/j.scitotenv.2019.134300 PubMed DOI

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

Iqbal, A. , Ložek, F. , Soto, I. , Kaur, D. , Grabicová, K. , Kuklina, I. , Randak, T. , Malinovska, V. , Buřič, M. , & Kozák, P. (2023). Effect of psychoactive substances on cardiac and locomotory activity of juvenile marbled crayfish Procambarus virginalis . Ecotoxicology and Environmental Safety, 260, 115084. 10.1016/j.ecoenv.2023.115084 PubMed DOI

Kenison, E. K. , Weldy, P. Y. , & Williams, R. N. (2018). There must be something in the water: Assessing the behavioral responses of rusty crayfish (Orconectes rusticus) to fish and amphibian predator kairomones. Journal of Ethology, 36(1), 77–84. 10.1007/s10164-017-0529-5 DOI

Keppel, E. , & Scrosati, R. (2004). Chemically mediated avoidance of Hemigrapsus nudus (Crustacea) by Littorina scutulata (Gastropoda): Effects of species coexistence and variable cues. Animal Behaviour, 68(4), 915–920. 10.1016/j.anbehav.2003.11.020 DOI

Kubec, J. , Kouba, A. , & Buřič, M. (2019). Communication, behaviour, and decision making in crayfish: A review. Zoologischer Anzeiger, 278, 28–37. 10.1016/j.jcz.2018.10.009 DOI

Larson, J. K. , & McCormick, M. I. (2005). The role of chemical alarm signals in facilitating learned recognition of novel chemical cues in a coral reef fish. Animal Behaviour, 69(1), 51–57. 10.1016/j.anbehav.2004.04.005 DOI

Lima, S. L. , & Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology, 68(4), 619–640. 10.1139/z90-092 DOI

Lima, S. L. , & Bednekoff, P. A. (1999). Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. American Naturalist, 153(6), 649–659. 10.1086/303202 PubMed DOI

Lipták, B. , & Vitázková, B. (2014). A review of the current distribution and dispersal trends of two invasive crayfish species in the Danube Basin. Water Research and Management, 4(1), 15–22.

Little, E. E. (1975). Chemical communication in maternal behaviour of crayfish. Nature, 255(5507), 400–401. 10.1038/255400a0 PubMed DOI

Lukas, J. , Romanczuk, P. , Klenz, H. , Klamser, P. , Arias Rodriguez, L. , Krause, J. , & Bierbach, D. (2021). Acoustic and visual stimuli combined promote stronger responses to aerial predation in fish. Behavioral Ecology, 32(6), 1094–1102. 10.1093/beheco/arab043 PubMed DOI PMC

Lunt, J. , & Smee, D. L. (2015). Turbidity interferes with foraging success of visual but not chemosensory predators. PeerJ, 2015(9), 1–12. 10.7717/peerj.1212 PubMed DOI PMC

MacKay, R. N. , Wood, T. C. , & Moore, P. A. (2021). Running away or running to? Do prey make decisions solely based on the landscape of fear or do they also include stimuli from a landscape of safety? Journal of Experimental Biology, 224(19), jeb242687. 10.1242/jeb.242687 PubMed DOI

Martin, P. , Kohlmann, K. , & Scholtz, G. (2007). The parthenogenetic marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften, 94, 843–846. 10.1007/s00114-007-0260-0 PubMed DOI

Momot, W. T. (1984). Crayfish production: A reflection of community energetics. Journal of Crustacean Biology, 4(1), 35–54. 10.2307/1547894 DOI

Moore, P. A. , Edwards, D. , Jurcak‐Detter, A. , & Lahman, S. (2021). Spatial, but not temporal, aspects of orientation are controlled by the fine‐scale distribution of chemical cues in turbulent odor plumes. Journal of Experimental Biology, 224(7), jeb240457. 10.1242/jeb.240457 PubMed DOI

Nevitt, G. A. , Losekoot, M. , & Weimerskirch, H. (2008). Evidence for olfactory search in wandering albatross, Diomedea exulans . Proceedings of the National Academy of Sciences of the United States of America, 105(12), 4576–4581. 10.1073/pnas.0709047105 PubMed DOI PMC

Ondračkovć, M. , Dćvidovć, M. , Přikrylovć, I. , & Pečínkovć, M. (2011). Monogenean parasites of introduced pumpkinseed Lepomis gibbosus (Centrarchidae) in the Danube River Basin. Journal of Helminthology, 85(4), 435–441. 10.1017/S0022149X10000805 PubMed DOI

Pecor, K. W. , Deering, C. M. , Firnberg, M. T. , Pastino, A. K. , & Wolfson, S. J. (2010). The use of conspecific and heterospecific alarm cues by virile crayfish (Orconectes virilis) from an exotic population. Marine and Freshwater Behaviour and Physiology, 43(1), 37–44. 10.1080/10236241003658353 DOI

Ramberg‐Pihl, N. C. , & Yurewicz, K. L. (2020). Behavioral responses of northern crayfish (Faxonius virilis) to conspecific alarm cues and predator cues from smallmouth bass (Micropterus dolomieu). Marine and Freshwater Behaviour and Physiology, 53(1), 1–16. 10.1080/10236244.2020.1717338 DOI

Schmidt, M. , & Mellon, D. (2010). Neuronal processing of chemical information in crustaceans. In Breithaupt T. & Thiel M. (Eds.), Chemical communication in crustaceans (pp. 123–147). Springer New York. 10.1007/978-0-387-77101-4_7 DOI

Sih, A. (1986). Antipredator responses and the perception of danger by mosquito larvae. Ecology, 67(2), 434–441. 10.2307/1938587 DOI

Smith, R. J. F. (1992). Alarm signals in fishes. Reviews in Fish Biology and Fisheries, 2(1), 33–63. 10.1007/BF00042916 DOI

Sterud, E. , & Jørgensen, A. (2006). Pumpkinseed Lepomis gibbosus (Linnaeus, 1758) (Centrarchidae) and associated parasites introduced to Norway. Aquatic Invasions, 1(4), 278–280. 10.3391/ai.2006.1.4.10 DOI

Tetzlaff, J. C. , Roth, B. M. , Weidel, B. C. , & Kitchell, J. F. (2011). Predation by native sunfishes (Centrarchidae) on the invasive crayfish Orconectes rusticus in four northern Wisconsin lakes. Ecology of Freshwater Fish, 20(1), 133–143. 10.1111/j.1600-0633.2010.00469.x DOI

Tierney, A. J. , & Andrews, K. (2013). Spatial behavior in male and female crayfish (Orconectes rusticus): Learning strategies and memory duration. Animal Cognition, 16(1), 23–34. 10.1007/s10071-012-0547-1 PubMed DOI

Turner, A. M. , Turner, S. E. , & Lappi, H. M. (2006). Learning, memory and predator avoidance by freshwater snails: Effects of experience on predator recognition and defensive strategy. Animal Behaviour, 72(6), 1443–1450. 10.1016/j.anbehav.2006.05.010 DOI

Ueda, H. (2014). Homing ability and migration success in pacific salmon: Mechanistic insights from biotelemetry, endocrinology, and neurophysiology. Marine Ecology Progress Series, 496, 219–232. 10.3354/meps10636 DOI

Vogt, G. (2011). Marmorkrebs: Natural crayfish clone as emerging model for various biological disciplines. Journal of Biosciences, 36, 377–382. 10.1007/s12038-011-9070-9 PubMed DOI

Vogt, G. , Huber, M. , Thiemann, M. , van den Boogaart, G. , Schmitz, O. J. , & Schubart, C. D. (2008). Production of different phenotypes from the same genotype in the same environment by developmental variation. Journal of Experimental Biology, 211(4), 510–523. 10.1242/jeb.008755 PubMed DOI

Wagner, M. J. , & Moore, P. A. (2022). Are you scared yet? Variations to cue indices elicit differential prey behavioral responses even when gape‐limited predators are relatively small. Canadian Journal of Zoology, 100(9), 583–595. 10.1139/cjz-2022-0050 DOI

Wei, X. , & Zhang, Z. Q. (2022). Level‐dependent effects of predation stress on prey development, lifespan and reproduction in mites. Biogerontology, 23(4), 515–527. 10.1007/s10522-022-09980-z PubMed DOI PMC

Wisenden, B. D. (2000). Olfactory assessment of predation risk in the aquatic environment. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 355(1401), 1205–1208. 10.1098/rstb.2000.0668 PubMed DOI PMC

Wisenden, B. D. , Chivers, D. P. , & Smith, R. J. F. (1997). Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. Journal of Chemical Ecology, 23(1), 137–151. 10.1023/B:JOEC.0000006350.66424.3d DOI

Wood, T. C. , & Moore, P. A. (2020). Fine‐tuned responses to chemical landscapes: Crayfish use predator odors to assess threats based on relative size ratios. Ecosphere, 11(9), e03188. 10.1002/ecs2.3188 DOI

Zulandt Schneider, R. A. , & Moore, P. A. (2000). Urine as a source of conspecific disturbance signals in the crayfish Procambarus clarkii . Journal of Experimental Biology, 203(4), 765–771. 10.1242/jeb.203.4.765 PubMed DOI

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