The perception of danger represents an essential ability of prey for gaining an informational advantage over their natural enemies. Especially in complex environments or at night, animals strongly rely on chemoreception to avoid predators. The ability to recognize danger by chemical cues and subsequent adaptive responses to predation threats should generally increase prey survival. Recent findings suggest that European catfish (Silurus glanis) introduction induce changes in fish community and we tested whether the direction of change can be attributed to differences in chemical cue perception. We tested behavioral response to chemical cues using three species of freshwater fish common in European water: rudd (Scardinius erythrophthalmus), roach (Rutilus rutilus), and perch (Perca fluviatilis). Further, we conducted a prey selectivity experiment to evaluate the prey preferences of the European catfish. Roach exhibited the strongest reaction to chemical cues, rudd decreased use of refuge and perch did not alter any behavior in the experiment. These findings suggest that chemical cue perception might be behind community data change and we encourage collecting more community data of tested prey species before and after European catfish introduction to test the hypothesis. We conclude that used prey species can be used as a model species to verify whether chemical cue perception enhances prey survival.

Biology Centre of the Academy of Sciences of the Czech Republic Institute of Hydrobiology České Budějovice Czech Republic

Department of Aquatic Ecology Lund University Lund Sweden

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Fisheries and Oceans Canada Gulf Fisheries Centre Moncton Canada

See more in PubMed

Abrahams, M. V. (1995). The interaction between antipredator behaviour and antipredator morphology: Experiments with fathead minnows and brook sticklebacks. Canadian Journal of Zoology, 73, 2209–2215. https://doi.org/10.1139/z95-261 DOI

Andraso, G. M. , & Barron, J. N. (1995). Evidence for a trade‐off between defensive morphology and startle‐response performance in the brook stickleback (Culaea inconstans). Canadian Journal of Zoology, 73, 1147–1153. https://doi.org/10.1139/z95-136 DOI

Apfelbach, R. , Blanchard, C. D. , Blanchard, R. J. , Hayes, R. A. , & McGregor, I. S. (2005). The effects of predator odors in mammalian prey species: A review of field and laboratory studies. Neuroscience and Biobehavioral Reviews, 29, 1123–1144. https://doi.org/10.1016/j.neubiorev.2005.05.005 PubMed DOI

Barry, T. P. , Dehnert, G. K. , Hoppe, P. D. , & Sorensen, P. W. (2017). Chemicals released by predation increase the growth rate of yellow perch, Perca flavescens . Journal of Fish Biology, 91, 1730–1736. https://doi.org/10.1111/jfb.13475 PubMed DOI

Benejam, L. , Carol, J. , Benito, J. , & García‐Berthou, E. (2007). On the spread of the European catfish (Silurus glanis) in the Iberian Peninsula: First record in the Llobregat river basin. Limnetica, 26, 169–171.

Boujard, T. (1995). Diel rhythms of feeding activity in the European catfish, Silurus glanis . Physiology & Behavior, 58, 641–645. https://doi.org/10.1016/0031-9384(95)00109-V PubMed DOI

Brönmark, C. , & Miner, J. G. (1992). Predator‐induced phenotypical change in body morphology in crucian carp. Science, 258, 1348–1350. https://doi.org/10.1126/science.258.5086.1348 PubMed DOI

Brönmark, C. , & Pettersson, L. B. (1994). Chemical cues from piscivores induce a change in morphology in crucian carp. Oikos, 70, 396–402. https://doi.org/10.2307/3545777 DOI

Brown, G. E. , Chivers, D. P. , & Smith, R. J. F. (1996). Effects of diet on localized defecation by Northern pike, Esox lucius . Journal of Chemical Ecology, 22, 467–475. https://doi.org/10.1007/BF02033649 PubMed DOI

Brown, G. E. , Poirier, J. F. , & Adrian, J. C. (2004). Assessment of local predation risk: The role of subthreshold concentrations of chemical alarm cues. Behavioral Ecology, 15, 810–815. https://doi.org/10.1093/beheco/arh084 DOI

Brown, G. E. , & Smith, R. J. F. (1998). Acquired predator recognition in juvenili rainbow trot (Oncorhynchus mykiss): Conditioning hatchery‐reared fish to recognize chemical cues of a predator. Canadian Journal of Fisheries and Aquatic Sciences, 55, 611–617. https://doi.org/10.1139/f97-261 DOI

Brown, J. S. , & Vincent, T. L. (1992). Organization of predator‐prey communities as an evolutionary game. Evolution, 46, 1269–1283. https://doi.org/10.1111/j.1558-5646.1992.tb01123.x PubMed DOI

Carol, J. , Zamora, L. , & García‐Berthou, E. (2007). Preliminary telemetry data on the movement patterns and habitat use of European catfish (Silurus glanis) in a reservoir of the River Ebro, Spain. Ecology of Freshwater Fish, 16, 450–456. https://doi.org/10.1111/j.1600-0633.2007.00225.x DOI

Chapman, B. B. , Hulthén, K. , Brodersen, J. , Nilsson, P. A. , Skov, C. , Hansson, L. A. , & Brönmark, C. (2012). Partial migration in fishes: Causes and consequences. Journal of Fish Biology, 81, 456–478. https://doi.org/10.1111/j.1095-8649.2012.03342.x PubMed DOI

Chesson, J. (1978). Measuring preference in selective predation. Ecology, 59, 211–215. https://doi.org/10.2307/1936364 DOI

Chivers, D. P. , & Smith, R. J. F. (1994). Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Animal Behaviour, 48, 597–605. https://doi.org/10.1006/anbe.1994.1279 DOI

Copp, G. H. , Robert Britton, J. , Cucherousset, J. , García‐Berthou, E. , Kirk, R. , Peeler, E. , & Stakėnas, S. (2009). Voracious invader or benign feline? A review of the environmental biology of European catfish Silurus glanis in its native and introduced ranges. Fish and Fisheries, 10, 252–282. https://doi.org/10.1111/j.1467-2979.2008.00321.x DOI

Crooks, K. , & Soulé, M. (1999). Mesopredator release and avifaunal extinctions in a fragmented system. Nature, 400, 563–566. https://doi.org/10.1038/23028 DOI

Domenici, P. , Turesson, H. , Brodersen, J. , Brönmark, C. , & Bronmark, C. (2008). Predator‐induced morphology enhances escape locomotion in crucian carp. Proceedings of the Royal Society of London B: Biological Sciences, 275, 195–201. https://doi.org/10.1098/rspb.2007.1088 PubMed DOI PMC

Eklöv, P. , & Hamrin, S. F. (1989). Predatory efficiency and prey selection: Interactions between pike Esox lucius, perch Perca fluviatilis and rudd Scardinus erythrophthalmus . Oikos, 56, 149–156. https://doi.org/10.2307/3565330 DOI

Eklöv, P. , & Persson, L. (1995). Species‐specific antipredator capacities and prey refuges: Interactions between piscivorous perch (Perca fluviatilis) and juvenile perch and roach (Rutilus rutilus). Behavioral Ecology and Sociobiology, 37, 169–178. https://doi.org/10.1007/BF00176714 DOI

Ferrari, M. C. O. , Messier, F. , & Chivers, D. P. (2006). The nose knows: Minnows determine predator proximity and density through detection of predator odours. Animal Behaviour, 72, 927–932. https://doi.org/10.1016/j.anbehav.2006.03.001 DOI

Ferrari, M. C. O. , Messier, F. , & Chivers, D. P. (2008). Can prey exhibit threat‐sensitive generalization of predator recognition? Extending the predator recognition continuum hypothesis. Proceedings of the Royal Society of London B: Biological Sciences, 275, 1811–1816. https://doi.org/10.1098/rspb.2008.0305 PubMed DOI PMC

Ferrari, M. C. O. , Wisenden, B. D. , & Chivers, D. P. (2010). Chemical ecology of predator–prey interactions in aquatic ecosystems: A review and prospectus. Canadian Journal of Zoology, 88, 698–724. https://doi.org/10.1139/Z10-029 DOI

Gjelland, K. Ø. , Říha, M. , Rosten, C. , Baktoft, H. , Sandlund, O. T. , Vejřík, L. , … Peterka, J. (2017) Flexible behaviour in sympatric pike (Esox lucius) and wels (Siluris glanis) in lakes suggest various mechanisms for niche partitioning. 4th International Conference on Fish Telemetry, Cairns, p. 62.

Harvey, M. C. , & Brown, G. E. (2004). Dine or dash? Ontogenetic shift in the response of yellow perch to conspecific alarm cues. Environmental Biology of Fishes, 70, 345–352. https://doi.org/10.1023/B:EBFI.0000035432.12313.87 DOI

Hölker, F. , Dörner, H. , Schulze, T. , Haertel‐Borer, S. S. , Peacor, S. D. , & Mehner, T. (2007). Species‐specific responses of planktivorous fish to the introduction of a new piscivore: Implications for prey fitness. Freshwater Biology, 52, 1793–1806. https://doi.org/10.1111/j.1365-2427.2007.01810.x DOI

Horppila, J. , & Nurminen, L. (2009). Food niche segregation between two herbivorous cyprinid species in a turbid lake. Journal of Fish Biology, 75, 1230–1243. https://doi.org/10.1111/j.1095-8649.2009.02359.x PubMed DOI

Hulthén, K. , Chapman, B. B. , Nilsson, P. A. , Hollander, J. , & Brönmark, C. (2014). Express yourself: Bold individuals induce enhanced morphological defences. Proceedings of the Royal Society B: Biological Sciences, 281, 20132703. PubMed PMC

Johansson, J. , Turesson, H. , & Persson, A. (2004). Active selection for large guppies, Poecilia reticulata, by the pike cichlid, Crenicichla saxatilis . Oikos, 105, 595–605. https://doi.org/10.1111/j.0030-1299.2004.12938.x DOI

Krause, J. , & Godin, J. G. J. (1992). Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey. Behavioral Ecology, 7, 264–271.

Lima, S. L. (1992). Strong preferences for apparently dangerous habitats? A consequence of differential escape from predators. Oikos, 64, 597–600. https://doi.org/10.2307/3545181 DOI

Lima, S. L. (1998). Nonlethal effects in the ecology of predator‐prey interactions. BioScience, 48, 25 https://doi.org/10.2307/1313225 DOI

Lima, S. , & Bednekoff, P. (1999). Back to the basics of antipredatory vigilance: Can nonvigilant animals detect attack? Animal behaviour, 58, 537–543. https://doi.org/10.1006/anbe.1999.1182 PubMed DOI

Mathis, A. , & Smith, R. J. F. (1993a). Chemical alarm signals increase the survival time of fathead minnows (Pimephales promelas) during encounters with northern pike (Esox lucius). Behavioral Ecology, 4, 260–265. https://doi.org/10.1093/beheco/4.3.260 DOI

Mathis, A. , & Smith, R. J. F. (1993b). Fathead minnow, Pimephales promelas, learn to recognize northern pike, Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike's diet. Animal Behaviour, 46, 645–656. https://doi.org/10.1006/anbe.1993.1241 DOI

Matsumoto, T. , & Kawamura, G. (2005). The eyes of the common carp and Nile tilapia are sensitive to near‐infrared. Fisheries Science, 71, 350–355. https://doi.org/10.1111/j.1444-2906.2005.00971.x DOI

Mehner, T. , Diekmann, M. , Bramick, U. , & Lemcke, R. (2005). Composition of fish communities in German lakes as related to lake morphology, trophic state, shore structure and human‐use intensity. Freshwater Biology, 50, 70–85. https://doi.org/10.1111/j.1365-2427.2004.01294.x DOI

Meuthen, D. , Rick, I. P. , Thünken, T. , & Baldauf, S. A. (2012). Visual prey detection by near‐infrared cues in a fish. Naturwissenschaften, 99, 1063–1066. https://doi.org/10.1007/s00114-012-0980-7 PubMed DOI

Mikheev, V. N. , Wanzenbock, J. , & Pasternak, A. F. (2006). Effects of predator‐induced visual and olfactory cues on 0+ perch (Perca fluviatilis L.) foraging behaviour. Ecology of Freshwater Fish, 15, 111–117. https://doi.org/10.1111/j.1600-0633.2006.00140.x DOI

Miller, L. A. , & Surlykke, A. (2001). How some insects detect and avoid being eaten by bats: Tactics and countertactics of prey and predator. BioScience, 51, 570 https://doi.org/10.1641/0006-3568(2001)051[0570:HSIDAA]2.0.CO;2 DOI

Mills, L. S. , Soulé, M. E. , & Doak, D. F. (1993). The keystone‐species concept in ecology and conservation. BioScience, 43, 219–224. https://doi.org/10.2307/1312122 DOI

Mirza, R. S. , & Chivers, D. P. (2000). Predator‐recognition training enhances survival of brook trout: Evidence from laboratory and field‐enclosure studies. Canadian Journal of Zoology, 78, 2198–2208. https://doi.org/10.1139/z00-164 DOI

Mirza, R. , & Chivers, D. (2001). Do juvenile yellow perch use diet cues to assess the level of threat posed by intraspecific predators? Behaviour, 138, 1249–1258. https://doi.org/10.1163/15685390152822201 DOI

Persson, L. , Roos, A. M. De. , Claessen, D. , Byström, P. , Lövgren, J. , Sjogrën, S. , … Westman, E. (2003). Gigantic cannibals driving a whole‐lake trophic cascade. Proceedings of the National Academy of Sciences of the United States of America, 100, 4035–4039. https://doi.org/10.1073/pnas.0636404100 PubMed DOI PMC

Pettersson, L. B. , Andersson, K. , & Nilsson, K. (2001). The diel activity of crucian carp, Carassius carassius, in relation to chemical cues from predators. Environmental Biology of Fishes, 61, 341–345. https://doi.org/10.1023/A:1011073518350 DOI

Pettersson, L. B. , Nilsson, P. A. , Bronmark, C. , & Brönmark, C. (2000). Predator recognition and defence strategies in crucian carp, Carassius carassius . Oikos, 88, 200–212. https://doi.org/10.1034/j.1600-0706.2000.880122.x DOI

Pohlmann, K. , Atema, J. , & Breithaupt, T. (2004). The importance of the lateral line in nocturnal predation of piscivorous catfish. The Journal of Experimental Biology, 207, 2971–2978. https://doi.org/10.1242/jeb.01129 PubMed DOI

Pohlmann, K. , Grasso, F. W. , & Breithaupt, T. (2001). Tracking wakes: The nocturnal predatory strategy of piscivorous catfish. Proceedings of the National Academy of Sciences of the United States of America, 98, 7371–7374. https://doi.org/10.1073/pnas.121026298 PubMed DOI PMC

Pollock, M. S. , Chivers, D. P. , Mirza, R. S. , & Wisenden, B. D. (2003). Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans . Environmental Biology of Fishes, 66, 313–319. https://doi.org/10.1023/A:1023905824660 DOI

Prchalová, M. , Kubečka, J. , Vašek, M. , Peterka, J. , Sed'a, J. , Jůza, T. , … Hohausová, E. (2008). Distribution patterns of fishes in a canyon‐shaped reservoir. Journal of Fish Biology, 73, 54–78. https://doi.org/10.1111/j.1095-8649.2008.01906.x DOI

R Core Team (2015). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Savino, J. F. , & Stein, R. A. (1989). Behavior of fish predators and their prey: Habitat choice between open water and dense vegetation. Environmental Biology of Fishes, 24, 287–293. https://doi.org/10.1007/BF00001402 DOI

Short, J. , Kinnear, J. E. , & Robley, A. (2002). Surplus killing by introduced predators in Australia ‐ Evidence for ineffective anti‐predator adaptations in native prey species? Biological Conservation, 103, 283–301. https://doi.org/10.1016/S0006-3207(01)00139-2 DOI

Sinclair, A. R. E. , Mduma, S. , & Brashares, J. S. (2003). Patterns of predation in a diverse predator‐prey system. Nature, 425, 288–290. https://doi.org/10.1038/nature01934 PubMed DOI

Turesson, H. , & Persson, A. (2002). Prey size selection in piscivorous pikeperch (Stizostedion lucioperca) includes active prey choice. Ecology of Freshwater Fish, 11, 223–233. https://doi.org/10.1034/j.1600-0633.2002.00019.x DOI

Vejřík, L. , Vejříková, I. , Blabolil, P. , Eloranta, A. P. , Kočvara, L. , Peterka, J. , … Čech, M. (2017). European catfish (Silurus glanis) as a freshwater apex predator drives ecosystem via its diet adaptability. Scientific Reports, 7, 15970. PubMed PMC

Westin, L. , & Aneer, G. (1987). Locomotor activity patterns of nineteen fish and five crustacean species from the Baltic Sea. Environmental Biology of Fishes, 20, 49–65. https://doi.org/10.1007/BF00002025 DOI

Whittaker, R. H. , Levin, S. A. , & Root, R. B. (1973). Niche, habitat, and ecotope. The American Naturalist, 107, 321–338. https://doi.org/10.1086/282837 DOI

Wirsing, A. J. , Cameron, K. E. , & Heithaus, M. R. (2010). Spatial responses to predators vary with prey escape mode. Animal Behaviour, 79, 531–537. https://doi.org/10.1016/j.anbehav.2009.12.014 DOI

Wisenden, B. (2008). Active space of chemical alarm cue in natural fish populations. Behaviour, 145, 391–407. https://doi.org/10.1163/156853908783402920 DOI

Wysujack, K. , & Mehner, T. (2005). Can feeding of European catfish prevent cyprinids from reaching a size refuge? Ecology of Freshwater Fish, 14, 87–95. https://doi.org/10.1111/j.1600-0633.2004.00081.x DOI

Long-lines for research monitoring and efficient population regulation of an invasive apex predator, European catfish (Silurus glanis)

Predicting the potential implications of perch (Perca fluviatilis) introductions to a biodiversity-rich lake using stable isotope analysis