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Behavioral response of juvenile silver and bighead carp to conspecific and heterospecific alarm cues

Biological Invasions volume 23, pages 2233–2248 (2021)Cite this article

Abstract

Predation is an important factor influencing the strength and success of a year class in many prey fishes. Many adaptations, including chemical cues, benefit shoaling groups by informing members of a possible impending predatory threat. Bighead (Hypophthalmichthys nobilis) and silver carps (Hypophthalmichthys molitrix) are widely dispersed invasive fishes that spend much of their first year at a size vulnerable to predation. The objective of this study was to evaluate the fright response of juvenile bighead and silver carps when exposed to alarm cues from conspecific and heterospecific fishes. Groups of carps were exposed to 5 mL of alarm cue from either bighead carp, silver carp, golden shiner (Notemigonus crysoleucas), or fathead minnow (Pimephales promelas). Behavior was recorded before and after the application of the treatment. Our results indicate that both species were unable to recognize chemical alarm cues from North American cypriniforms, yet both were able to recognize conspecific alarm cues. However, the two species of bigheaded carps respond to conspecific chemicals differently. Silver carp increase distance among individuals, whereas bighead carp reduce distance between individuals. Both show a reduction in activity after chemical application. Though both species recognize conspecific alarm cues, bighead carp exhibit similar fright patterns when exposed to alarm chemicals of silver carp, yet no behavioral responses were detected in silver carp when exposed to alarm chemicals of bighead carp. An understanding of fright response in bighead and silver carps aids understanding of predator interactions and ecological roles of these fishes, and can be utilized in population management applications.

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References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson M, Gorley R, Clarke KP (2008) For PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Anderson C, Haun R, Lamer JT, et al. (2015) Juvenile asian carp as forage for native predators in the lagrange reach, Illinois River. In: 145th annual meeting of the American fisheries society. AFS

  • Anton A, Geraldi NR, Ricciardi A et al (2020) Global determinants of prey naiveté to exotic predators. Proc R Soc B 287:20192978

    Article  PubMed  PubMed Central  Google Scholar 

  • Baerwaldt K, Benson A, Irons K (2014) Asian carp distribution in North America. Asian Carp Regional Coordinating Committee

  • Beauchamp G (2007) Vigilance in a selfish herd. Anim Behav 73:445–451

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Brönmark C, Pettersson LB (1994) Chemical cues from piscivores induce a change in morphology in crucian carp. Oikos, 396–402

  • Brown BE, Inman I, Jearld A Jr (1970) Schooling and shelter seeking tendencies in fingerling channel catfish. Trans Am Fish Soc 99:540–545

    Article  Google Scholar 

  • Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234

    Article  CAS  Google Scholar 

  • Brown GE, Rive AC, Ferrari MCO et al (2006) The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. Behav Ecol Sociobiol 61:9–16

    Article  Google Scholar 

  • Bryer PJ, Mirza RS, Chivers DP (2001) Chemosensory assessment of predation risk by slimy sculpins (Cottus cognatus): responses to alarm, disturbance, and predator cues. J Chem Ecol 27:533–546

    Article  CAS  PubMed  Google Scholar 

  • Cabecinha E, Cortes R, Cabral JA et al (2009) Multi-scale approach using phytoplankton as a first step towards the definition of the ecological status of reservoirs. Ecol Indicators 9:240–255

    Article  CAS  Google Scholar 

  • Carthey AJR, Banks PB (2016) Naiveté is not forever: responses of a vulnerable native rodent to its long term alien predators. Oikos 125:918–926

    Article  Google Scholar 

  • Chivers D, Mirza R, Johnston J (2002) Learned recognition of heterospecific alarm cues enhances survival during encounters with predators. Behaviour 139:929–938

    Article  Google Scholar 

  • Chivers DP, Brown GE, Smith RJF (1995) Acquired recognition of chemical stimuli from pike, Esox lucius, by brook sticklebacks, Culaea inconstans (Osteichthyes, Gasterosteidae). Ethology 99:234–242

    Article  Google Scholar 

  • Chivers DP, Mirza RS (2001) Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. Chemical Signals in Vertebrates 9. Springer, pp. 277–284

  • Chivers DP, Smith RJF (1994) Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Anim Behav 48:597–605

    Article  Google Scholar 

  • Chivers DP, Wisenden BD, Hindman CJ et al (2007) Epidermal ‘alarm substance’cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proc R Soc B Biol Sci 274:2611–2619

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke K, Warwick R (1994) Change in Marine assemblages: An approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  • Clarke KR, Gorley RN (2015) Getting started with PRIMER v7. PRIMER-E: Plymouth, Plymouth Marine Laboratory, 20

  • Crane DP, Farrell JM, Einhouse DW et al (2015) Trends in body condition of native piscivores following invasion of L akes E rie and O ntario by the round goby. Freshw Biol 60:111–124

    Article  Google Scholar 

  • Cresswell W (2008) Non-lethal effects of predation in birds. Ibis 150:3–17

    Article  Google Scholar 

  • Cunha C, Mesquita N, Dowling TE et al (2002) Phylogenetic relationships of Eurasian and American cyprinids using cytochrome b sequences. J Fish Biol 61:929–944

    Article  CAS  Google Scholar 

  • 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 behavior, pp 266–290

  • Dixson DL, Pratchett MS, Munday PL (2012) Reef fishes innately distinguish predators based on olfactory cues associated with recent prey items rather than individual species. Anim Behav 84:45–51

    Article  Google Scholar 

  • Eshel I, Sansone E, Shaked A (2011) On the evolution of group-escape strategies of selfish prey. Theor Popul Biol 80:150–157

    Article  PubMed  Google Scholar 

  • Ferrari MCO, Gonzalo A, Messier F et al (2007) Generalization of learned predator recognition: an experimental test and framework for future studies. Proc R Soc B Biol Sci 274:1853–1859

    Article  Google Scholar 

  • Ferrari MCO, Trowell JJ, Brown GE et al (2005) The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim Behav 70:777–784

    Article  Google Scholar 

  • Frisch KV (1941) Die Bedeutung des Geruchsinnes im Leben der Fische Natürwissenschaften 29:321–33

  • 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

    Article  Google Scholar 

  • George AE, Chapman DC (2013) Aspects of embryonic and larval development in bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. PLoS ONE 8:e73829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosal R, Xiong PX, Sorensen PW (2016) Invasive bighead and silver carps form different sized shoals that readily intermix. PLoS ONE 11:e0157174

    Article  PubMed  PubMed Central  Google Scholar 

  • Godard R, Wannamaker C, Bowers B (1998) Responses of golden shiner minnows to chemical cues from snake predators. Behaviour 135:1213–1228

    Article  Google Scholar 

  • Gomes LAP, Salgado PMP, Barata EN et al (2013) Alarm scent-marking during predatory attempts in the Cabrera vole (Microtus cabrerae Thomas, 1906). Ecol Res 28:335–343

    Article  Google Scholar 

  • Green BW, Smitherman RO (1984) Relative growth, survival and harvestability of bighead carp, silver carp, and their reciprocal hybrids. Aquaculture 37:87–95

    Article  Google Scholar 

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311

    Article  CAS  PubMed  Google Scholar 

  • Hara TJ (1994) The diversity of chemical stimulation in fish olfaction and gustation. Rev Fish Biol Fisheries 4:1–35

    Article  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat, 65–70

  • Holway DA, Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends Ecol Evol 14:328–330

    Article  CAS  PubMed  Google Scholar 

  • Hume JB, Meckley TD, Johnson NS et al (2015) Application of a putative alarm cue hastens the arrival of invasive sea lamprey (Petromyzon marinus) at a trapping location. Can J Fish Aquat Sci 72:1799–1806

    Article  CAS  Google Scholar 

  • Jang MH, Joo GJ, Lucas MC (2006) Diet of introduced largemouth bass in Korean rivers and potential interactions with native fishes. Ecol Freshw Fish 15:315–320

    Article  Google Scholar 

  • Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394

    Article  Google Scholar 

  • Kolar CS, Chapman DC, Courtenay Jr WR, et al. (2005) Asian carps of the genus Hypophthalmichthys (Pisces, Cyprinidae)―a biological synopsis and environmental risk assessment.

  • Krause J (1993) The effect of’Schreckstoff’on the shoaling behaviour of the minnow: a test of Hamilton’s selfish herd theory. Anim Behav 45:1019–1024

    Article  Google Scholar 

  • Kruskal JB (1964) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129

    Article  Google Scholar 

  • Larson JK, McCormick MI (2005) The role of chemical alarm signals in facilitating learned recognition of novel chemical cues in a coral reef fish. Anim Behav 69:51–57

    Article  Google Scholar 

  • Lehtiniemi M (2005) Swim or hide: predator cues cause species specific reactions in young fish larvae. J Fish Biol 66:1285–1299

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Little EE, Calfee RD, Puglis H et al (2014) Field Evaluation of Sex Pheromone Attractants to Control Asian Carp and Development of Protocols for Field Verification of Response. Quebec, Canada

    Google Scholar 

  • Magurran AE (1990) The adaptive significance of schooling as an anti-predator defence in fish. Annales Zoologici Fennici. JSTOR, pp. 51–66

  • Mandrak NE, Cudmore-Vokey BC (2004) Risk assessment for Asian carps in Canada. Fisheries & Oceans Canada, Science, Canadian Science Advisory Secretariat

  • Maniak PJ, Lossing RD, Sorensen PW (2000) Injured Eurasian ruffe, Gymnocephalus cernuus, release an alarm pheromone that could be used to control their dispersal. J Great Lakes Res 26:183–195

    Article  Google Scholar 

  • Mathis A, Chivers DP, Smith RJF (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51:185–201

    Article  Google Scholar 

  • McGhee KE, Pintor LM, Suhr EL et al (2012) Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback. Funct Ecol 26:932–940

    Article  PubMed  PubMed Central  Google Scholar 

  • Mirza RS, Chivers DP (2003) Predator diet cues and the assessment of predation risk by juvenile brook charr: do diet cues enhance survival? Can J Zool 81:126–132

    Article  Google Scholar 

  • Mirza RS, Scott JJ, Chivers DP (2001) Differential responses of male and female red swordtails to chemical alarm cues. J Fish Biol 59:716–728

    Article  Google Scholar 

  • Parker KA, Anderson MJ, Jenkins PF et al (2012) The effects of translocation-induced isolation and fragmentation on the cultural evolution of bird song. Ecol Lett 15:778–785

    Article  PubMed  Google Scholar 

  • Pavlov DS, Kasumyan AO (2000) Patterns and mechanisms of schooling behavior in fish: a review. J Ichthyol 40:S163

    Google Scholar 

  • Pettersson LB, Andersson K, Nilsson K (2001) The diel activity of crucian carp, Carassius carassius, in relation to chemical cues from predators. Environ Biol Fishes 61:341–345

    Article  Google Scholar 

  • Pitcher TJ (1986a) Functions of shoaling behaviour in teleosts. The behaviour of teleost fishes. Springer, pp. 294–337

  • Reebs SG, Leblond C (2006) Individual leadership and boldness in shoals of golden shiners (Notemigonus crysoleucas). Behaviour 143:1263–1280

    Article  Google Scholar 

  • Rice JA, Crowder LB, Marschall EA (1997) Predation on juvenile fishes: dynamic interactions between size-structured predators and prey. Early life history and recruitment in fish populations. Springer, pp. 333–356

  • Sanft E, Wahl DH (2014) Vulnerability of juvenile Asian carp to predation By largemouth bass.

  • Schaerf TM, Dillingham PW, Ward AJW (2017) The effects of external cues on individual and collective behavior of shoaling fish. Sci Adv 3:e1603201

    Article  PubMed  PubMed Central  Google Scholar 

  • Shirkhorshidi AS, Aghabozorgi S, Wah TY (2015) A comparison study on similarity and dissimilarity measures in clustering continuous data. PLoS ONE 10:e0144059

    Article  PubMed  PubMed Central  Google Scholar 

  • Šmejkal M, Ricard D, Sajdlová Z et al (2018) Can species-specific prey responses to chemical cues explain prey susceptibility to predation? Ecol Evol 8:4544–4551

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith RJF (1997) Does one result trump all others? A response to Magurran, Irving and Henderson. Proc R Soc Lond Ser B Biol Sci 264:445–450

    Article  Google Scholar 

  • Sorensen PW, Johnson NS (2016) Theory and application of semiochemicals in nuisance fish control. J Chem Ecol 42:698–715

    Article  CAS  PubMed  Google Scholar 

  • Sorensen PW, Rue MCP, Leese JM et al (2019) A blend of f prostaglandins functions as an attractive sex pheromone in silver carp. Fishes 4:27

    Article  Google Scholar 

  • Sorensen PW, Stacey NE (1999) Evolution and specialization of fish hormonal pheromones. Advances in chemical signals in vertebrates. Springer, pp. 15–47

  • Stacey NE, Cardwell JR, Liley NR, et al. (1994) Hormones as sex pheromones in fish. Perspect Comp Endocrinol, 438–448

  • Tan M, Armbruster JW (2018) Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei: Ostariophysi). Zootaxa 4476:6–39

    Article  PubMed  Google Scholar 

  • Tsehaye I, Catalano M, Sass G et al (2013) Prospects for fishery-induced collapse of invasive Asian carp in the Illinois River. Fisheries 38:445–454

    Article  Google Scholar 

  • Wagner CM, Stroud EM, Meckley TD (2011) A deathly odor suggests a new sustainable tool for controlling a costly invasive species. Can J Fish Aquat Sci 68:1157–1160

    Article  Google Scholar 

  • Wainwright PC, Lauder GV (1986) Feeding biology of sunfishes: patterns of variation in the feeding mechanism. Zool J Linn Soc 88:217–228

    Article  Google Scholar 

  • Williamson CJ, Garvey JE (2005) Growth, fecundity, and diets of newly established silver carp in the middle Mississippi River. Trans Am Fish Soc 134:1423–1430

    Article  Google Scholar 

  • Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666

    Article  Google Scholar 

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Acknowledgements

We thank Curt Byrd and Duane Chapman of the USGS Columbia Environmental Research Center and Steve Kahrs of Osage Catfisheries, Inc. for providing bigheaded carps used in this study. We also thank Naveen Parthiban and two anonymous reviewers for their efforts to provide constructive comments on this manuscript.

Funding

The study was supported in part by the funding from the Great Lakes Research Initiative, administered through the Illinois Department of Natural Resources (CAFWS‐93).

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Author notes

  1. Jared C. Wilson and Dalon P. White were co-first authors.

Authors and Affiliations

  1. Department of Natural Resources, University of Illinois, Urbana, IL, 61801, USA

    Jared C. Wilson & David H. Wahl

  2. Program in Ecology, Evolution, and Conservation Biology, University of Illinois At Urbana-Champaign, 1816 S. Oak Street, Champaign, IL, 61820, USA

    Dalon P. White & David H. Wahl

  3. Kaskaskia Biological Station, Illinois Natural History Survey, Sullivan, IL, 61451, USA

    Jared C. Wilson, Dalon P. White, Thomas M. Detmer & David H. Wahl

  4. Department of Natural Resources, Cornell University, Ithaca, NY, 14853, USA

    Thomas M. Detmer

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  1. Jared C. Wilson
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Contributions

JW, TD, and D. Wahl conceived and designed the experiments. JW conducted the experiment and analyzed the data. JW and D. White wrote the manuscript.

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Correspondence to Dalon P. White.

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All study procedures adhered to the University of Illinois at Urbana-Champaign Institutional Animal Care and Use guidelines for ethical treatment of animals under the protocol #17068.

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Wilson, J.C., White, D.P., Detmer, T.M. et al. Behavioral response of juvenile silver and bighead carp to conspecific and heterospecific alarm cues. Biol Invasions 23, 2233–2248 (2021). https://doi.org/10.1007/s10530-021-02502-x

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