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Phenotypic responses to piscivory in invasive gibel carp populations

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Abstract

The establishment of introduced fishes can be inhibited by the biotic resistance from species in the receiving environment, including strong consumptive resistance from specific piscivorous fishes. In response to predation pressure, prey fish population responses include predator-induced morphological changes, where an extreme example is seen in the crucian carp Carassius carassius, which forms deep-bodied morphs in predator presence that reduces individual predation risk. As its congener, gibel carp Carassius gibelio is a highly invasive fish across in its non-native range in Eurasia. Here we test whether their introduced populations also respond to the presence of piscivorous fishes by altering their body shape and trophic ecology by testing differences across 16 non-native lentic populations in Turkey that provided groups of piscivorous fish presence versus absence. In piscivore presence, gibel carp had a higher ratio of body length-to-depth than in piscivore absence, but with their body condition factor being higher in absence. Stable isotope mixing models predicted that gibel carp had diets that were more animal based (gastropods and zooplankton) in piscivore absence, but plant based in piscivore presence. Moreover, diet predictions of piscivore diet suggested gibel carp were consistently consumed less than other prey fishes. These results suggest that these alien gibel carp were responding to piscivory as per crucian carp, reducing their predation risk at the individual level by forming deep-bodied morphs. We suggest these morphological responses then decrease the strength of the biotic resistance against their invasion at the population level.

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All data generated or analyzed during this study are included in this published article and are available from the corresponding author.

References

  • Alofs KM, Jackson DA (2014) Meta-analysis suggests biotic resistance in freshwater environments is driven by consumption rather than competition. Ecology 95:3259–3270

    Article  Google Scholar 

  • Andersson J, Johansson F, Söderlund T (2006) Interactions between predator-and diet-induced phenotypic changes in body shape of crucian carp. Proc R Soc B-Biol Sci 273:431–437

    Article  Google Scholar 

  • Bates DM (2010) lme4: Mixed-effects modeling with R

  • Britton JR (2023) Contemporary perspectives on the ecological impacts of invasive freshwater fishes. J Fish Biol. https://doi.org/10.1111/jfb.15240

    Article  PubMed  Google Scholar 

  • Brönmark C, Miner JG (1992) Predator-induced phenotypical change in body morphology in crucian carp. Science 258:1348–1350

    Article  PubMed  Google Scholar 

  • Brönmark C, Pettersson LB (1994) Chemical cues from piscivores induce a change in morphology in crucian carp. Oikos 70:396–402

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Domenici P (2002) The visually-mediated escape response in fish: predicting prey responsiveness and the locomotor behaviour of predators and prey. Mar Freshw Behav Phys 35:87–110

    Article  Google Scholar 

  • Domenici P, Turesson H, Brodersen J, Brönmark C (2008) Predator-induced morphology enhances escape locomotion in crucian carp. Proc R Soc B-Biol Sci 275:195–201

    Article  Google Scholar 

  • Emiroğlu Ö, Tarkan AS, Top N, Başkurt S, Sülün Ş (2012) Growth and life history traits of a highly exploited population of non-native gibel carp, Carassius gibelio from a large eutrophic lake (Lake Uluabat, NW Turkey): is reproduction the key factor for establishment success? Turk J Fish Aquat Sci 12:925–936

    Google Scholar 

  • Gaygusuz Ö, Tarkan AS, Aydın H, Dorak Z, Top N, Karakuş U, Vilizzi L (2015) Stocking of Common Carp (Cyprinus carpio) into some newly-established reservoirs of north-west Anatolia may enhance the spread of non-native Fish. Turk J Fish Aquat Sci 15:833–840

    Article  Google Scholar 

  • Haubrock PJ, Balzani P, Matsuzaki SS, Tarkan AS, Kourantidou M, Haase P (2021) Spatio-temporal niche plasticity of a freshwater invader as a harbinger of impact variability. Sci Total Environ 777:145947

    Article  CAS  PubMed  Google Scholar 

  • Henriksson A, Yu J, Wardle DA, Englund G (2015) Biotic resistance in freshwater fish communities: species richness, saturation or species identity? Oikos 124:1058–1064

    Article  Google Scholar 

  • Holopainen IJ, Tonn WM, Paszkowski CA (1997) Tales of two fish: the dichotomous biology of crucian carp (Carassius carassius (L.)) in northern Europe. Ann Zool Fenn 34:1–22

    Google Scholar 

  • Ioannou CC, Ramnarine IW, Torney CJ (2017) High-predation habitats affect the social dynamics of collective exploration in a shoaling fish. Sci Adv 3:pe1602682

    Article  Google Scholar 

  • Karachle PK, Stergiou KI (2012) Morphometrics and allometry in fishes. Morphometrics (c):65–86.  http://www.intechopen.com/books/morphometrics

  • Le Cren ED (1951) The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol 20:201–219

    Article  Google Scholar 

  • Lusková V, Lusk S, Halačka K, Vetešník L (2010) Carassius auratus gibelio—the most successful invasive fish in waters of the Czech Republic. Russ J Biol Invasions 1:176–180

    Article  Google Scholar 

  • Nilsson PA, Brönmark C, Pettersson LB (1995) Benefits of a predator-induced morphology in crucian carp. Oecologia 104:291–296

    Article  PubMed  Google Scholar 

  • Ogle DH, Wheeler P, Dinno A (2000) FSA: fisheries stock analysis. R package. https://github.com/droglenc/FSA

  • Parnell A, Parnell MA (2019) Package ‘simmr’. In: (2016) Aquaculture big numbers. Food and Agriculture Organization of The United Nations Rome, Italy

  • Perdikaris C, Ergolavou A, Gouva E, Nathanailides C, Chantzaropoulos A, Paschos I (2012) Carassius gibelio in Greece: the dominant naturalised invader of freshwaters. Rev Fish Biol Fish 22:17–27

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    Article  PubMed  Google Scholar 

  • Rolla M, Consuegra S, Garcia de Leaniz C (2020) Trophic plasticity of the highly invasive topmouth gudgeon (Pseudorasbora parva) inferred from stable isotope analysis. Front Ecol Evol 8:212

    Article  Google Scholar 

  • Saç G, Okgerman H (2015) Growth and reproduction of a non-native fish species Carassius gibelio (Bloch, 1782) from Büyükçekmece Lake (İstanbul, Turkey). IUFS J Biol 74:1–12

    Google Scholar 

  • Scharnweber K, Watanabe K, Syväranta J, Wanke T, Monaghan MT, Mehner T (2013) Effects of predation pressure and resource use on morphological divergence in omnivorous prey fish. BMC Evol Biol 13:132

    Article  PubMed  PubMed Central  Google Scholar 

  • Stabell OB, San Lwin M (1997) Predator-induced phenotypic changes in crucian carp are caused by chemical signals from conspecifics. Environ Biol Fish 49:145–149

    Google Scholar 

  • Tarkan AS, Copp GH, Top N, Özdemir N, Önsoy B, Bilge G, Filiz H, Yapıcı S, Ekmekçi FG, Kırankaya Ş, Emiroğlu Ö, Gaygusuz Ö, Gürsoy Gaygusuz Ç, Oymak A, Özcan G, Saç G (2012) Are introduced gibel carp Carassius gibelio in Turkey more invasive in artificial than in natural waters? Fish Manag Ecol 19:178–187

    Article  Google Scholar 

  • Tarkan AS, Gaygusuz Ö, Gürsoy Gaygusuz Ç, Saç G, Copp GH (2012) Circumstantial evidence for gibel carp Carassius gibelio reproductive competition exerted on native fish species in a mesotrophic reservoir. Fish Manag Ecol 19:167–177

    Article  Google Scholar 

  • Vilizzi L, Ekmekçi FG, Tarkan AS, Jackson Z (2015) Growth of common carp Cyprinus carpio in Anatolia (Turkey), with a comparison to native and invasive areas worldwide. Ecol Freshw Fish 24:165–180

    Article  Google Scholar 

  • Walls M, Kortelainen I, Sarvala J (1990) January. Prey responses to fish predation in freshwater communities. In: Annales Zoologici Fennici. Finnish Zoological Publishing Board, formed by the Finnish Academy of Sciences, Societas Scientiarum Fennica, Societas Biologica Fennica Vanamo and Societas pro Fauna et Flora Fennica, pp 183–199

  • Záhorská E, Kováč V, Falka I, Beyer K, Katina S, Copp GH, Gozlan RE (2009) Morphological variability of the Asiatic cyprinid, topmouth gudgeon Pseudorasbora parva, in its introduced European range. J Fish Biol 74:167–185

    Article  PubMed  Google Scholar 

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Acknowledgements

This work has been supported by Eskişehir Osmangazi University Scientific Research Projects Coordination Unit under grant number FBA-2021-2227 and FCD-2021-2146.

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AST: Conceptualization, methodology, writing – original draft, review and editing. SA and ÖE: Conceptualization, methodology, visualization. OM, EK, IK, SB, EÇ, PÖV: Investigation and data curation. PH and PB: Methodology, visualization, writing – original draft, review and editing. RB: Conceptualization, writing – review and editing, supervision.

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Correspondence to Ali Serhan Tarkan.

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Tarkan, A.S., Mol, O., Aksu, S. et al. Phenotypic responses to piscivory in invasive gibel carp populations. Aquat Sci 85, 75 (2023). https://doi.org/10.1007/s00027-023-00974-8

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