Abstract
Predator-prey interactions exert significant influence over the survival of juvenile fish cohorts. Therefore, susceptibility of a habitat to invasion is influenced by the capacity of native predators to regulate invasive species through consumption. Closely related predators often share similar characteristics (e.g., odors or body morphometry), and prey species capable of expressing generalized behavioral responses to predators with similar characteristics may increase their chances for survival. Here, we examined how naïve juvenile silver carp (Hypophthalmichthys molitrix), an invasive Asian carp, respond to three predator odors from predators commonly found in Midwestern lakes and rivers of the USA. We tested two congeneric species of bass (largemouth Micropterus salmoides and smallmouth M. dolomieu bass) and one outgroup, longnose gar (Lepisosteus osseus). Additionally, we tested how silver carp conditioned to recognize the odor of one group, largemouth bass, responded to the predator odors of the congeneric species and the outgroup. We found that juvenile silver carp showed no innate response to any of the three predator odors. Additionally, although they could be conditioned to recognize predator odors from largemouth bass, they were unable to generalize predator odors to smallmouth bass or longnose gar odor. These results suggest that invasive species could be less likely to persist in environments with diverse predator communities than environments of equal densities with uniform predator communities and that future studies should continue to explore this area as well as focus on understanding dynamics in predator-prey interactions of invasive species.
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References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26(1):32–46. https://doi.org/10.1046/j.1442-9993.2001.01070.x
Anderson M, Gorley R, Clarke K (2008) PERMANOVA+ for Primer. Primer-E. Plymouth, UK
Baeckens S, García-Roa R, Martín J, Van Damme R (2017) The role of diet in shaping the chemical signal design of lacertid lizards. J Chem Ecol 43(9):902–910. https://doi.org/10.1007/s10886-017-0884-2
Bajer PG, Chizinski CJ, Silbernagel JJ, Sorensen PW (2012) Variation in native micro-predator abundance explains recruitment of a mobile invasive fish, the common carp, in a naturally unstable environment. Biol Invasions 14(9):1919–1929. https://doi.org/10.1007/s10530-012-0203-3
Balaban-Feld J, Mitchell WA, Kotler BP, Vijayan S, Tov Elem LT, Rosenzweig ML, Abramsky Z (2019) Individual willingness to leave a safe refuge and the trade-off between food and safety: a test with social fish. Philos T R Soc B 286(1907):20190826. https://doi.org/10.1098/rspb.2019.0826
Berejikian BA, Tezak EP, LaRae AL (2003) Innate and enhanced predator recognition in hatchery-reared Chinook salmon. Environ Biol Fish 67(3):241–251. https://doi.org/10.1023/a:1025887015436
Boys CA, Williams RJ (2012) Succession of fish and crustacean assemblages following reinstatement of tidal flow in a temperate coastal wetland. Ecol Eng 49:221–232. https://doi.org/10.1016/j.ecoleng.2012.08.006
Brown GE, Chivers DP (2005) Learning as an adaptive response to predation. Ecology of predator/prey interactions. Oxford University Press, Oxford, pp 34–54
Brown BE, Inman I, Jearld A (1970) Schooling and shelter seeking tendencies in fingerling channel catfish. Trans Am Fish Soc 99(3):540–545. https://doi.org/10.1577/1548-8659(1970)99<540:sassti>2.0.co;2
Brown GE, Rive AC, Ferrari MCO, Chivers DP (2006) The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. Behav Ecol Sociobiol 61(1):9–16. https://doi.org/10.1007/s00265-006-0232-y
Cabecinha E, Cortes R, Cabral JA, Ferreira T, Lourenco M, Pardal MA (2009) Multi-scale approach using phytoplankton as a first step towards the definition of the ecological status of reservoirs. Ecol Indic 9(2):240–255. https://doi.org/10.1016/j.ecolind.2008.04.006
Calkins HA, Tripp SJ, Garvey JE (2012) Linking silver carp habitat selection to flow and phytoplankton in the Mississippi River. Biol Invasions 14(5):949–958. https://doi.org/10.1007/s10530-011-0128-2
Carey MP, Wahl DH (2010) Native fish diversity alters the effects of an invasive species on food webs. Ecology 91(10):2965–2974. https://doi.org/10.1890/09-1213.1
Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18(1):117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Clarke K, Warwick R (1994) An approach to statistical analysis and interpretation. Change in marine communities. PRIMER-E Ltd, Plymouth, United Kingdom
Collins SF, Detmer TM, Nelson KA, Nannini MA, Sass GG, Wahl DH (2018) The release and regulation of rotifers: examining the predatory effects of invasive juvenile common and bighead carp. Hydrobiologia 813(1):199–211. https://doi.org/10.1007/s10750-018-3526-y
Deacon AE, Magurran AE (2016) How behaviour contributes to the success of an invasive Poeciliid fish: the Trinidadian guppy (Poecilia reticulata) as a model species. Biological Invasions and Animal Behaviour:266–290
Degrandchamp KL, Garvey JE, Colombo RE (2008) Movement and habitat selection by invasive Asian carps in a large river. Trans Am Fish Soc 137(1):45–56. https://doi.org/10.1577/t06-116.1
Detmer TM, Wahl DH (2021) Effects of habitat and fish type and diet on the behavior of Daphnia. Inland Waters 11(1):57–66. https://doi.org/10.1080/20442041.2020.1766919
Edwards, EA, Gebhart G, Maughan OE (1983) Habitat suitability information: smallmouth bass. United States Fish and Wildlife Service, FWS/OBS-82/10.36
Elton CS (1958) The ecology of invasions by plants and animals. Springer Nature, London pp 1–181
Ferrari MCO, Messier F, Chivers DP, Messier O (2008) Can prey exhibit threat-sensitive generalization of predator recognition? Extending the predator recognition continuum hypothesis Proceedings of the Royal Society B-Biological Sciences 275(1644):1811–1816. https://doi.org/10.1098/rspb.2008.0305
Ferrari MCO, Trowell JJ, Brown GE, Chivers DP (2005) The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim Behav 70:777–784. https://doi.org/10.1016/j.anbehav.2005.01.009
Ferrari MCO, Gonzalo A, Messier F, Chivers DP (2007) generalization of learned predator recognition: an experimental test and framework for future studies. Proceedings of the Royal Society B-Biological Sciences 274(1620):1853–1859. https://doi.org/10.1098/rspb.2007.0297
Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88(7):698–724. https://doi.org/10.1139/z10-029
Ferrari MCO, Crane AL, Chivers DP (2016) Certainty and the cognitive ecology of generalization of predator recognition. Anim Behav 111:207–211. https://doi.org/10.1016/j.anbehav.2015.10.026
Fuselier L, Rugg M, Korpi N et al (2009) Lab and field estimates of active time of chemical alarm cues of a cyprinid fish and an amphipod crustacean. Behaviour 146:1423–1442. https://doi.org/10.1163/156853909X440998
Ghosal R, Xiong PX, Sorensen PW (2016) Invasive bighead and silver carps form different sized shoals that readily intermix. PLoS One 11(6):e0157174. https://doi.org/10.1371/journal.pone.0157174
Gomez-Mestre I, Diaz-Paniagua C (2011) Invasive predatory crayfish do not trigger inducible defenses in tadpoles. P Roy Soc B-Biol Sci 278(1723):3364–3370. https://doi.org/10.1098/rspb.2010.2762
Hambright KD, Drenner RW, McComas SR, Hairston NG (1991) Gape-limited piscivores, planktivore size refuges, and the trophic cascade hypothesis. Archiv Fur Hydrobiologie 121(4):389–404
Hara TJ (1994) The diversity of chemical-stimulation in fish olfaction and gustation. Rev Fish Biol Fish 4(1):1–35. https://doi.org/10.1007/bf00043259
Hawkins LA, Magurran AE, Armstrong JD (2004) Innate predator recognition in newly-hatched Atlantic salmon. Behaviour 141(10):1249–1262. https://doi.org/10.1163/1568539042729694
Hill JE, Nico LG, Cichra CE, Gilbert CR (2004) Prey vulnerability to peacock cichlids and largemouth bass based on predator gape and prey body depth. Proceedings of the Annual Conference of the Southeastern Association of Fish and Wildlife Agencies, 68:47–56. https://pubs.er.usgs.gov/publication/70161786
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6(2):65–70
Kolar CS, Chapman DC, Courtenay WR, Housel CM, Williams JD, Jennings DP (2005) Asian carps of the genus Hypothalmichthys (Pisces, Cyprinidae): a biological synopsis and environmental risk assessment. US fish and wildlife service per interagency agreement 94400-3-0128. US Geological Survey, LaCrosse, Wisconsin. http://www.fws.gov/contaminants/OtherDocuments/ACBSRAFinalReport2005.pdf
Kruskal JB (1964) Nonmetric multidimensional-scaling - a numerical-method. Psychometrika 29(2):115–129. https://doi.org/10.1007/bf02289694
Lampo EG, Knights BC, Vallazza JM, Anderson CA, Rechkemmer WT, Solomon LE, Casper AF, Pendleton RM, Lamer JT (2017) Using pharyngeal teeth and chewing pads to estimate juvenile silver carp total length in the La Grange Reach, Illinois River. N Am J Fish Manag 37(5):1145–1150. https://doi.org/10.1080/02755947.2017.1350221
Leblond C, Reebs SG (2006) Individual leadership and boldness in shoals of golden shiners (Notemigonus crysoleucas). Behaviour 143:1263–1280. https://doi.org/10.1163/156853906778691603
Mandrak NE, Cudmore B (2010) The fall of native fishes and the rise of non-native fishes in the great lakes basin. Aquat Ecosyst Health Manag 13(3):255–268. https://doi.org/10.1080/14634988.2010.507150
McCormick MI, Manassa R (2008) Predation risk assessment by olfactory and visual cues in a coral reef fish. Coral Reefs 27(1):105–113. https://doi.org/10.1007/s00338-007-0296-9
McGrath PE, Hilton EJ, Musick JA (2013) Temporal and spatial effects on the diet of an estuarine piscivore, longnose gar (Lepisosteus osseus). Estuar Coasts 36(6):1292–1303. https://doi.org/10.1007/s12237-013-9637-9
Mirza RS, Scott JJ, Chivers DP (2001) Differential responses of male and female red swordtails to chemical alarm cues. J Fish Biol 59(3):716–728. https://doi.org/10.1111/j.1095-8649.2001.tb02375.x
Oksanen JFG, Blanchet R, Kindt P, Legendre PR, Minchin RB, O’Hara GL, Simpson P, Solymos MH, Stevens H, Wagner H (2016) Vegan: community ecology package. R packageversion 2.3-4. (Available from: https://CRAN.R-project.org/packagepvegan)
Olson MH, Young BP (2003) Patterns of diet and growth in co-occurring populations of largemouth bass and smallmouth bass. Trans Am Fish Soc 132(6):1207–1213. https://doi.org/10.1577/t02-146
Philipp DP, Childers WF, Whitt GS (1979) Evolution of patterns of differential gene-expression - comparison of the temporal and spatial patterns of isoenzyme locus expression in 2 closely related fish species (northern largemouth bass, Micropterus salmoides, and smallmouth bass, Micropterus dolomieui). J Exp Zool 210(3):473–487. https://doi.org/10.1002/jez.1402100310
Raibley PT, O’Hara TM, Irons KS, Blodgett KD, Sparks RE (1997) Largemouth bass size distributions under varying annual hydrological regimes in the Illinois River. Trans Am Fish Soc 126(5):850–856. https://doi.org/10.1577/1548-8659(1997)126<0850:nlbsdu>2.3.co;2
Reader SM, Laland KN (2003) Animal innovation. Oxford University Press Oxford, pp 3–35
Rehage JS, Barnett BK, Sih A (2005) Behavioral responses to a novel predator and competitor of invasive mosquitofish and their non-invasive relatives (Gambusia sp.). Behav Ecol Sociobiol 57(3):256–266. https://doi.org/10.1007/s00265-004-0850-1
Rice JA, Crowder LB, Marschall EA (1997) Predation on juvenile fishes: dynamic interactions between size-structured predators and prey. In: Chambers RC, Trippel EA (eds) Early life history and recruitment in fish populations. Chapman and Hall, London, pp 333–356
Sanft E, Parkos JJ, Collins SF, Porreca AP, Wahl DH (2018) Vulnerability of juvenile bighead and silver carps to predation by largemouth bass. Trans Am Fish Soc 147(6):1207–1214. https://doi.org/10.1002/tafs.10117
Sass GG, Hinz C, Erickson AC, McClelland NN, McClelland MA, Epifanio JM (2014) Invasive bighead and silver carp effects on zooplankton communities in the Illinois River, Illinois, USA. J Great Lakes Res 40(4):911–921. https://doi.org/10.1016/j.jglr.2014.08.010
Schaerf TM, Dillingham PW, Ward AJW (2017) The effects of external cues on individual and collective behavior of shoaling fish. Sci Adv 3(6):e1603201. https://doi.org/10.1126/sciadv.1603201
Schake CL, Dembkowski DJ, Wuellner MR (2014) Gape: body size relationship for smallmouth bass. The Prairie Naturalist 42(2):100
Shirkhorshidi AS, Aghabozorgi S, Teh Ying W (2015) A comparison study on similarity and dissimilarity measures in clustering continuous data. PLoS One 10(12):e0144059. https://doi.org/10.1371/journal.pone.0144059
Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator-prey naivete, antipredator behavior, and the ecology of predator invasions. Oikos 119(4):610–621. https://doi.org/10.1111/j.1600-0706.2009.18039.x
Tsehaye I, Catalano M, Sass G, Glover D, Roth B (2013) Prospects for fishery-induced collapse of invasive Asian carp in the Illinois River. Fisheries 38(10):445–454. https://doi.org/10.1080/03632415.2013.836501
Williamson CJ, Garvey JE (2005) Growth, fecundity, and diets of newly established silver carp in the middle Mississippi River. Trans Am Fish Soc 134(6):1423–1430. https://doi.org/10.1577/t04-106.1
Wilson, JC, White DP, Detmer TM, Wahl DH (2021) Behavioral response of juvenile silver and bighead carp to conspecific and heterospecific alarm cues. Biol Invasions 23:2233–2248. https://doi.org/10.1007/s10530-021-02502-x
Wright TF, Eberhard JR, Hobson EA, Avery ML, Russello MA (2010) Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol Ecol Evol 22(4):393–404. https://doi.org/10.1080/03949370.2010.505580
Xie P, Chen YY (2001) Invasive carp in China’s plateau lakes. Science 294(5544):999–1000
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The study was supported in part by funding from the Great Lakes Research Initiative, administered through the Illinois Department of Natural Resources (CAFWS-93).
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All authors contributed to development of concept and study design. JCW carried out experiments. JCW and TMD analyzed data. JCW developed initial manuscript, and all authors provided scientific input and contributed to editing and revision of the manuscript.
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Institutional Animal Care and Use Committee (#14069) approval was obtained before commencement of the study. All fishes were acquired, retained, and used in compliance with federal, state, and local laws and regulations.
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Jared C. Wilson and Thomas M. Detmer co-lead authors.
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Wilson, J.C., Detmer, T.M., White, D. et al. Non-native silver carp fail to generalize behavior when exposed to odors from three North American predators. Environ Biol Fish 104, 1033–1043 (2021). https://doi.org/10.1007/s10641-021-01124-5
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DOI: https://doi.org/10.1007/s10641-021-01124-5