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Role of winter severity on juvenile Bighead Carp and Silver Carp growth and survival across latitudes

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Abstract

Population dynamics and ecological effects of invasive fishes are affected by offspring survival to sexual maturity (recruitment). Recruitment is oftentimes determined by conditions experienced during early life, and winter conditions become increasingly influential as species invade north in temperate regions. Bighead Carp (Hypophthalmichthys nobilis) and Silver Carp (H. molitrix) have invaded mid-latitudes of North America and threaten to invade farther north. We conducted pond experiments and bioenergetic simulations to: (1) assess the effects of mild winters on juvenile Bighead Carp and Silver Carp at mid-latitudes; (2) determine how conspecific density affects juveniles during mild winters; and, (3) determine effects of increased winter severity at increasing latitudes. Both species displayed high overwinter survival (85%) in pond experiments. Bighead Carp grew in length (mean 2 mm) and maintained initial body mass and percent dry mass (index of energy content). Silver Carp maintained initial length and mass and remained in high condition (dry mass). Conspecific densities tested did not affect growth, condition, or survival. Simulations suggest juvenile Bighead Carp could energetically survive the longest, coldest winter simulated (48° latitude); however, energy reserves at the start of winter became increasingly important for survival as latitude increased. Bighead Carp and Silver Carp recruitment success at mid-latitudes is likely driven by non-winter factors. If these species invade farther north, winter severity may play a stronger role in offspring survival, recruitment, and population dynamics. However, warmer and shorter winters at high latitudes caused by climate change will minimize this potential bottleneck and increase chances of successful recruitment.

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References

  • Almany GR, Webster MS (2006) The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25(1):19–22

    Article  Google Scholar 

  • Anderson DA, Scharf FS (2013) The effect of variable winter severity on size-dependent overwinter mortality caused by acute thermal stress in juvenile red drum (Sciaenops ocellatus). ICES J Mar Sci 71:1010–1021

    Article  Google Scholar 

  • Anderson KR, Chapman DC, Wynne TT, Masagounder K, Paukert CP (2015) Suitability of Lake Erie for bigheaded carps based on bioenergetic models and remote sensing. J Great Lakes Res 41:358–366

    Article  Google Scholar 

  • Anderson KR, Chapman DC, Wynne TT, Paukert CP (2017) Assessment of phytoplankton resources suitable for bigheaded carps in Lake Michigan derived from remote sensing and bioenergetics. J Great Lakes Res 43:90–99

    Article  Google Scholar 

  • Bates D, Sarkar D (2006) Lme4: Linear mixed-effects models using S4 classes. R package version 0.9975-9

  • Biro PA, Morton AE, Post JR, Parkinson EA (2004) Over-winter lipid depletion and mortality of age-0 rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 61:1513–1519

    Article  CAS  Google Scholar 

  • Boulion VV (2003) Dependence of the annual phytoplankton production on latitude. Doklady Biol Sci 389:130–133

    Article  CAS  Google Scholar 

  • Brylinsky M, Mann K (1973) An analysis of factors governing productivity in lakes and reservoirs. Limnol Oceanogr 18:1–14

    Article  CAS  Google Scholar 

  • Cargnelli LM, Gross MR (1996) The temporal dimension in fish recruitment: birth date, body size, and size-dependent survival in a sunfish (bluegill: Lepomis macrochirus). Can J Fish Aquat Sci 53:360–367

    Article  Google Scholar 

  • Chen P, Wiley EO, Mcnyset KM (2007) Ecological niche modeling as a predictive tool: silver and bighead carps in North America. Biol Invasions 9:43–51

    Article  Google Scholar 

  • Chick JH, Pegg MA (2001) Invasive carp in the Mississippi River basin. Science 292:2250–2251

    Article  CAS  Google Scholar 

  • Chipps SR, Wahl DH (2008) Bioenergetics modeling in the 21st century: reviewing new insights and revisiting old constraints. Trans Am Fish Soc 137:298–313

    Article  Google Scholar 

  • Collins SF, Wahl DH (2017) Invasive planktivores as mediators of organic matter exchanges within and across ecosystems. Oecologia 184:1–10

    Article  Google Scholar 

  • Collins SF, Nelson KA, DeBoom CS, Wahl DH (2017) The facilitation of the native bluegill sunfish by the invasive bighead carp. Freshw Biol 62:1645–1654

    Article  Google Scholar 

  • Cooke SL, Hill WR, Meyer KP (2009) Feeding at different plankton densities alters invasive bighead carp (Hypophthalmichthys nobilis) growth and zooplankton species composition. Hydrobiologia 625:185–193

    Article  Google Scholar 

  • Coulter AA, Keller D, Bailey EJ, Goforth RR (2016) Predictors of bigheaded carp drifting egg density and spawning activity in an invaded, free-flowing river. J Great Lakes Res 42:83–89

    Article  Google Scholar 

  • Coulter AA, Schultz D, Tristano E, Brey MK, Garvey JE (2017) Restoration versus invasive species: bigheaded carps’ use of a rehabilitated backwater. River Res Appl 33:662–669

    Article  Google Scholar 

  • Coulter DP, MacNamara R, Glover DC, Garvey JE (2018) Possible unintended effects of management at an invasion front: reduced prevalence corresponds with high condition of an invasive bigheaded carp. Biol Conserv 221:118–126

    Article  Google Scholar 

  • Cremer MC, Smitherman RO (1980) Food habits and growth of silver and bighead carp in cages and ponds. Aquaculture 20:57–64

    Article  Google Scholar 

  • Cudmore B, NE Mandrak, J Dettmers, DC Chapman, CS Kolar 2012. Binational Ecological Risk Assessment of Bigheaded Carps (Hypophthalmichthys spp.) for the Great Lakes Basin. DFO Can. Sci. Advis. Sec. Res. Doc. 2011/114. vi + 57 p

  • DeGrandchamp KL, Garvey JE, Csoboth LA (2007) Linking adult reproduction and larval density of invasive carp in a large river. Trans Am Fish Soc 136:1327–1334

    Article  Google Scholar 

  • Feiner ZS, Bunnell DB, Höök TO, Madenjian CP, Warner DM, Collingsworth PD (2015) Non-stationary recruitment dynamics of rainbow smelt: the influence of environmental variables and variation in size structure and length-at-maturation. J Great Lakes Res 41:246–258

    Article  Google Scholar 

  • Feiner ZS, Chong SC, Fielder DG, Hoyle JA, Knight C, Lauer TE, Thomas MV, Tyson JT, Höök TO (2017) Sex-based tradeoffs between growth, mortality, and maturation in Great Lakes yellow perch stocks. Can J Fish Aquat Sci 74:2059–2072

    Article  Google Scholar 

  • Fetzer WW, Brooking TE, Jackson JR, Rudstam LG (2011) Overwinter mortality of gizzard shad: evaluation of starvation and cold temperature stress. Trans Am Fish Soc 140:1460–1471

    Article  Google Scholar 

  • Ficke AD, Myrick CA, Hansen LJ (2007) Potential impacts of global climate change on freshwater fisheries. Rev Fish Biol Fish 17:581–613

    Article  Google Scholar 

  • Figueira WF, Booth DJ (2010) Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Glob Change Biol 16:506–516

    Article  Google Scholar 

  • Garvey JE, Wright RA, Stein RA (1998) Overwinter growth and survival of age-0 largemouth bass (Micropterus salmoides): revisiting the role of body size. Can J Fish Aquat Sci 55:2414–2424

    Article  Google Scholar 

  • Gibson-Reinemer DK, Solomon LE, Pendleton RM, Chick JH, Casper AF (2017) Hydrology controls recruitment of two invasive cyprinids: bigheaded carp reproduction in a navigable large river. PeerJ 5:e3641

    Article  Google Scholar 

  • Glover DC, DeVries DR, Wright RA, Davis DA (2010) Sample preparation techniques for determination of fish energy density via bomb calorimetry: an evaluation using largemouth bass. Trans Am Fish Soc 139:671–675

    Article  Google Scholar 

  • Had**ikolova L (2008) Investigations on the chemical composition of carp (Cyprinus carpio L.), bighead carp (Aristichthys nobilis Rich.) and pike (Esox lusius L.) during different stages of individual growth. Bulg J Agric Sci 14:121–126

    Google Scholar 

  • Hanson PC, Johnson TB, Schindler DE, Kitchell JF (1997) Fish Bioenergetics 3.0 for Windows. University of Wisconsin Sea Grant Institute, Report WISCU-T-97-001, Madison, WI

  • Hayer CA, Breeggemann JJ, Klumb RA, Graeb BD, Bertrand KN (2014) Population characteristics of bighead and silver carp on the northwestern front of their North American invasion. Aquat Invasions 9:289–303

    Article  Google Scholar 

  • Herborg LM, Mandrak NE, Cudmore BC, MacIsaac HJ (2007) Comparative distribution and invasion risk of snakehead (Channidae) and Asian carp (Cyprinidae) species in North America. Can J Fish Aquat Sci 64:1723–1735

    Article  Google Scholar 

  • Hintz WD, Glover DC, Szynkowski BC, Garvey JE (2017) Spatiotemporal reproduction and larval habitat associations of nonnative silver carp and bighead carp. Trans Am Fish Soc 146:422–431

    Article  Google Scholar 

  • Höök TO, Rutherford ES, Mason DM, Carter GS (2007) Hatch dates, growth, survival, and overwinter mortality of age-0 alewives in Lake Michigan: implications for habitat-specific recruitment success. Trans Am Fish Soc 136:1298–1312

    Article  Google Scholar 

  • Höök TO, Rutherford ES, Croley TE, Mason DM, Madenjian CP (2008) Annual variation in habitat-specific recruitment success: implications from an individual-based model of Lake Michigan alewife (Alosa pseudoharengus). Can J Fish Aquat Sci 65:1402–1412

    Article  Google Scholar 

  • Hurst TP (2007) Causes and consequences of winter mortality in fishes. J Fish Biol 71:315–345

    Article  Google Scholar 

  • Hurst TP, Conover DO (1998) Winter mortality of young-of-the-year Hudson River striped bass (Morone saxatilis): size-dependent patterns and effects on recruitment. Can J Fish Aquat Sci 55:1122–1130

    Article  Google Scholar 

  • Irons KS, Sass GG, McClelland MA, Stafford JD (2007) Reduced condition factor of two native fish species coincident with invasion of non-native Asian carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? J Fish Biol 71:258–273

    Article  Google Scholar 

  • Ivan LN, Höök TO (2015) Energy allocation strategies of young temperate fish: an eco-genetic modeling approach. Can J Fish Aquat Sci 72:1243–1258

    Article  Google Scholar 

  • Jiménez-Valverde A, Peterson AT, Soberón J, Overton JM, Aragón P, Lobo JM (2011) Use of niche models in invasive species risk assessments. Biol Invasions 13:2785–2797

    Article  Google Scholar 

  • Jones LA (2017) Modelling survival and establishment of grass carp, Ctenopharyngodon idella, in the Great Lakes basin. Canadian Science Advisory Secretariat

  • Kearney M, Porter W (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol Lett 12:334–350

    Article  Google Scholar 

  • Kittel EC, Small BC (2014) Effect of altering dietary protein: Energy ratios on juvenile pallid sturgeon growth performance. N Am J Aquac 76:28–35

    Article  Google Scholar 

  • Kokotovich A, Andow D, Aadland L, Bertrand K, Coulter A, Frohnauer N, Hoff M, Hoxmeier J, O’Hara M, Phelps Q, Reeves K, Rutherford E, Weber M (2017) Minnesota Bigheaded Carps Risk Assessment. Minnesota Aquatic Invasive Species Research Center, University of Minnesota, Minneapolis

    Google Scholar 

  • Kolar CS, Chapman DC, Courtenay WR, Housel CM, Williams JD, Jennings DP (2007) Bigheaded carps: a biological synopsis and environmental risk assessment. American Fisheries Society Special Publication 33, Bethesda

    Google Scholar 

  • Kurbanov A, Kamilov BG (2015) Age and growth of bighead carp (Hypophthalmichthys nobilis R.) in Tudakul reservoir, Uzbekistan. Int J Fish Aquat Stud 3:229–232

    Google Scholar 

  • Lenaerts AW, Coulter AA, Feiner ZS, Goforth RR (2015) Egg size variability in an establishing population of invasive silver carp Hypophthalmichthys molitrix (Valenciennes, 1844). Aquat Invasions 10:449–461

    Article  Google Scholar 

  • Lenth RV (2013) lsmeans: least-squares means. R package version 1.10-2

  • Livingstone D (2003) Impact of secular climate change on the thermal structure of a large temperate central European lake. Clim Change 57:205–225

    Article  Google Scholar 

  • Lohmeyer AM, Garvey JE (2009) Placing the North American invasion of Asian carp in a spatially explicit context. Biol Invasions 11(4):905–916

    Article  Google Scholar 

  • MacNamara R, Glover D, Garvey J, Bouska W, Irons K (2016) Bigheaded carps (Hypophthalmichthys spp.) at the edge of their invaded range: using hydroacoustics to assess population parameters and the efficacy of harvest as a control strategy in a large North American river. Biol Invasions 18:3293–3307

    Article  Google Scholar 

  • MacNamara R, Coulter DP, Glover DC, Lubejko AE, Garvey JE (2018) Acoustically derived habitat associations of sympatric invasive bigheaded carps in a large river ecosystem. River Res Appl. https://doi.org/10.1002/rra.3279

    Article  Google Scholar 

  • Madenjian CP, Höök TO, Rutherford ES, Mason DM, Croley TE, Szalai EB, Bence JR (2005) Recruitment variability of alewives in Lake Michigan. Trans Am Fish Soc 134:218–230

    Article  Google Scholar 

  • McCormick MJ, Fahnenstiel GL (1999) Recent climatic trends in nearshore water temperatures in the St. Lawrence Great Lakes. Limnol Oceanogr 44:530–540

    Article  Google Scholar 

  • Murphy SC, Collins NC, Doka SE (2012) The effects of cool and variable temperatures on the hatch date, growth and overwinter mortality of a warmwater fish in small coastal embayments of Lake Ontario. J Great Lakes Res 38:404–412

    Article  Google Scholar 

  • Oliver JD, Holeton GF, Chua KE (1979) Overwinter mortality of fingerling smallmouth bass in relation to size, relative energy stores, and environmental temperature. Trans Am Fish Soc 108:130–136

    Article  Google Scholar 

  • Opuszynski K, Shireman JV (1993) Food habits, feeding behaviour and impact of triploid bighead carp, Hypophthalmichthys nobilis, in experimental ponds. J Fish Biol 42:517–530

    Article  Google Scholar 

  • Pendleton RM, Schwinghamer C, Solomon LE, Casper AF (2017) Competition among river planktivores: are native planktivores still fewer and skinnier in response to the silver carp invasion? Environ Biol Fish 100:1213–1222

    Article  Google Scholar 

  • Phelps QE, Graeb BDS, Willis DW (2008) First year growth and survival of common carp in two glacial lakes. Fish Manag Ecol 15:85–91

    Article  Google Scholar 

  • Post JR, Evans DO (1989) Size-dependent overwinter mortality of young-of-the-year yellow perch (Perca flavescens): laboratory, in situ enclosure, and field experiments. Can J Fish Aquat Sci 46:1958–1968

    Article  Google Scholar 

  • Post JR, Parkinson EA (2001) Energy allocation strategy in young fish: allometry and survival. Ecology 82:1040–1051

    Article  Google Scholar 

  • Roswell CR, Pothoven SA, Höök TO (2014) Patterns of age-0 yellow perch growth, diets, and mortality in Saginaw Bay, Lake Huron. J Great Lakes Res 40:123–132

    Article  Google Scholar 

  • Sammons SM, Bettoli PW (2000) Population dynamics of a reservoir sport fish community in response to hydrology. N Am J Fish Manage 20:791–800

    Article  Google Scholar 

  • Schrank SJ, Guy CS (2002) Age, growth, and gonadal characteristics of adult bighead carp, Hypophthalmichthys nobilis, in the lower Missouri River. Environ Biol Fish 64:443–450

    Article  Google Scholar 

  • Stainsby EA, Winter JG, Jarjanazi H, Paterson AM, Evans DO, Young JD (2011) Changes in the thermal stability of Lake Simcoe from 1980 to 2008. J Great Lakes Res 37:55–62

    Article  Google Scholar 

  • Stuck JG, Porreca AP, Wahl DH, Colombo RE (2015) Contrasting population demographics of invasive silver carp between an impounded and free-flowing river. N Am J Fish Manag 35:114–122

    Article  Google Scholar 

  • Sullivan CJ (2016) Asian Carp population characteristics and dynamics in the Mississippi River watershed. Master’s thesis, Iowa State University

  • Sullivan CJ, Camacho CA, Weber MJ, Pierce CL (2017) Intra-annual variability of Silver Carp populations in the Des Moines River, USA. N Am J Fish Manag 37:836–849

    Article  Google Scholar 

  • US Geological Survey (2017) Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov. 22 Sept 2017

  • Thieltges DW, Strasser M, van Beusekom JE, Reise K (2004) Too cold to prosper—winter mortality prevents population increase of the introduced American slipper limpet Crepidula fornicata in northern Europe. J Exp Mar Biol Ecol 311:375–391

    Article  Google Scholar 

  • Thompson JM, Bergersen EP, Carlson CA, Kaeding LR (1991) Role of size, condition, and lipid content in the overwinter survival of age-0 Colorado Squawfish. Trans Am Fish Soc 120:346–353

    Article  Google Scholar 

  • Van der Veer HW, Berghahn R, Miller JM, Rijnsdorp AD (2000) Recruitment in flatfish, with special emphasis on North Atlantic species: progress made by the flatfish symposia. ICES J Mar Sci 57:202–215

    Article  Google Scholar 

  • Weber MJ, Brown ML (2013) Density-dependence and environmental conditions regulate recruitment and first-year growth of common carp in shallow lakes. Trans Am Fish Soc 142:471–482

    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 

  • Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Glob Change Biol 10:1844–1856

    Article  Google Scholar 

  • Wright RA, Garvey JE, Fullerton AH, Stein RA (1999) Predicting how winter affects energetics of age-0 largemouth bass: how do current models fare? Trans Am Fish Soc 128:603–612

    Article  Google Scholar 

  • Wuenschel MJ, Jugovich AR, Hare JA (2006) Estimating the energy density of fish: the importance of ontogeny. Trans Am Fish Soc 135:379–385

    Article  Google Scholar 

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Acknowledgements

Funding was provided by the Great Lakes Restoration Initiative, via the Illinois Department of Natural Resources (Grant CAFWS-106D). All procedures involving animals were approved by Southern Illinois University’s Institutional Animal Care and Use Committee.

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  1. Center for Fisheries, Aquaculture, and Aquatic Sciences, Southern Illinois University, Life Science II Room 251, 1125 Lincoln Drive, Carbondale, IL, 62901, USA

    David P. Coulter, Elizabeth P. Tristano, Alison A. Coulter, Justin R. Seibert & James E. Garvey

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  1. David P. Coulter
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Correspondence to David P. Coulter.

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Coulter, D.P., Tristano, E.P., Coulter, A.A. et al. Role of winter severity on juvenile Bighead Carp and Silver Carp growth and survival across latitudes. Biol Invasions 20, 3357–3371 (2018). https://doi.org/10.1007/s10530-018-1781-5

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