Skip to main content
Log in

Warmed Winter Water Temperatures Alter Reproduction in Two Fish Species

  • Published:
Environmental Management Aims and scope Submit manuscript

Abstract

We examined the spawning success of Fathead Minnows (Pimephales promelas) and Johnny Darters (Etheostoma nigrum) exposed to elevated winter water temperatures typical of streams characterized by anthropogenic thermal inputs. When Fathead Minnows were exposed to temperature treatments of 12, 16, or 20 °C during the winter, spawning occurred at 16 and 20 °C but not 12 °C. Eggs were deposited over 9 weeks before winter spawning ceased. Fathead Minnows from the three winter temperature treatments were then exposed to a simulated spring transition. Spawning occurred at all three temperature treatments during the spring, but fish from the 16° and 20 °C treatment had delayed egg production indicating a latent effect of warm winter temperatures on spring spawning. mRNA analysis of the egg yolk protein vitellogenin showed elevated expression in female Fathead Minnows at 16 and 20 °C during winter spawning that decreased after winter spawning ceased, whereas Fathead Minnows at 12 °C maintained comparatively low expression during winter. Johnny Darters were exposed to 4 °C to represent winter temperatures in the absence of thermal inputs, and 12, 16, and 20 °C to represent varying degrees of winter thermal pollution. Johnny Darters spawned during winter at 12, 16, and 20 °C but not at 4 °C. Johnny Darters at 4 °C subsequently spawned following a simulated spring period while those at 12, 16, and 20 °C did not. Our results indicate elevated winter water temperatures common in effluent-dominated streams can promote out-of-season spawning and that vitellogenin expression is a useful indicator of spawning readiness for fish exposed to elevated winter temperatures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aegerter S, Jalabert B (2004) Effects of post-ovulatory oocyte ageing and temperature on egg quality and on the occurrence of triploid fry in rainbow trout, Oncorhynchus mykiss. Aquaculture 231:59–71

    Article  Google Scholar 

  • Ankley GT, Johnson RD (2004) Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. Inst Lab Anim Res J 45(4):469–483

    Article  CAS  Google Scholar 

  • Ankley GT, Villeneuve DL (2006) The fathead minnow in aquatic toxicology: past present and future. Aquat Toxicol 78:91–102

    Article  CAS  Google Scholar 

  • Becker GC (1962) Intra-specific variation in Rhinichthys c. cataractae (Valenciennes) and Rhinichthys atratulus meleagris Agassiz and anatomical and ecological studies of Rhinichthys c. cataractae. Dissertation. University of Wisconsin

  • Becker GC (1983) Fishes of Wisconsin. Madison, Wisconsin

  • Biales AD, Bencic DC, Flick RW, Lazorchak J, Lattier DL (2007) Quantification and associated variability of induced vitellogenin gene transcripts in fathead minnow (Pimephales promelas) by quantitative real-time polymerase chain reaction assay. Environ Toxicol Chem 26(2):287–296

    Article  CAS  Google Scholar 

  • Billard R (1986) Spermatogenesis and spermatology of some teleost fish species. Reprod Nutr Dev 26(4):877–920

    Article  Google Scholar 

  • Bobe J, Labbe C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165(3):535–548

    Article  CAS  Google Scholar 

  • Bonnet E, Fostier A, Bobe J (2007) Characterization of rainbow trout egg quality: a case study using four different breeding protocols, with emphasis on the incidence of embryonic malformations. Theriogenology 67(4):786–794

    Article  Google Scholar 

  • Breton B, Horoszewicz L, Billard R, Bieniarz K (1980) Temperature and reproduction in tench: effect of a rise in the annual temperature regime on gonadotropin level, gametogenesis and spawning. I. The male. Reprod Nutr Dev 20(1a):105–118

    Article  CAS  Google Scholar 

  • Brock ML, Shapiro DJ (1983) Estrogen regulates the absolute rate of transcription of the Xenopus laevis vitellogenin genes. J Biol Chem 258:5449–5455

    CAS  Google Scholar 

  • Bromage N, Porter M, Randall C (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197(1–4):63–98

    Article  CAS  Google Scholar 

  • Brooks BW, Riley TM, Taylor RD (2006) Water quality of effluent-dominated ecosystems: ecotoxicological, hydrological, and management considerations. Hydrobiologia 566:365–379

    Article  Google Scholar 

  • Brown NP, Shields RJ, Bromage NR (1995) The effect of spawning temperature on egg viability in the Atlantic Halibut (Hippoglossus hippoglossus). Aquaculture 261:993–1002

    Article  Google Scholar 

  • Bye VJ (1984) The role of environmental factors in the timing of reproductive cycles. In: Potts GW, Wootton RJ (eds) Fish reproduction: Strategies and tactics, Fisheries Society of the British Isles Academic Press, London; Orlando, p 187–206

  • Carlander KD (1969) Handbook of freshwater fishery biology. vol. 1: life history data on freshwater fishes of the United States and Canada, exclusive of the Perciformes. Iowa State University Press, Ames

  • Chatzifotis S, Papakaki M, Despoti S, Roufidou C, Antonopoulou E (2011) Effect of starvation and re-feeding on reproductive indices, body weight, plasma metabolites and oxidative enzymes of sea bass (Dicentrarchus labrax). Aquaculture 306:53–59

    Article  Google Scholar 

  • Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exper Bio 216(15):2771–2782

    Article  Google Scholar 

  • Clarkson RO, Childs MR (2000) Temperature effects of hypolimnial-release dams on early life stages of Colorado River basin big-river fishes. Copeia 2000(2):402–412

    Article  Google Scholar 

  • Cochran PA, Lyons J (1986) Temporal and spatial patterns of spawning site use by two cavity-spawning darters in a Wisconsin stream. Environ Biol Fish 15(2):131–139

    Article  Google Scholar 

  • Colorado Department of Public Health and Environment Water Quality Control Commission (2012) Regulation 31: The basic standards and methodologies for surface water. 5 CCR 1002–31

  • Cooke SJ, Bunt CM, Schreer JF (2004) Understanding fish behavior, distribution and survival in thermal effluents using fixed telemetry arrays: a case study of smallmouth bass in a discharge canal during winter. Environ Manage 33(1):140–150

    Article  Google Scholar 

  • De Vlaming V (1972) Environmental control of teleost reproductive cycles: a brief review. J Fish Biol 4:131–140

    Article  Google Scholar 

  • Dennehy KF, Litke DW, McMahon PB, Heiny JS, Tate CM (1995) Water-quality assessment of the South Platte River Basin, Colorado, Nebraska, and Wyoming—analysis of available nutrient, suspended-sediment, and pesticide data, water years 1980–92: U.S. Geological Survey Water-Resources Investigations Report 94–4095

  • Donaldson MR, Cooke SJ, Patterson DA, Macdonald JS (2008) Cold shock and fish. J Fish Biol 73:1491–1530

    Article  Google Scholar 

  • Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283

    Article  Google Scholar 

  • Farmer TM, Marschall EA, Dabrowski K, Ludsin SA (2015) Short winters threaten temperate fish populations. Nat Comm 6:7724

    Article  CAS  Google Scholar 

  • Filby AL, Tyler CR (2007) Appropriate ‘housekeeping’ genes for use in expression profiling the effects of environmental estrogens in fish. BMC Mol Biol 8:10

    Article  Google Scholar 

  • Gale WF, Buynak GL (1982) Fecundity and spawning frequency of the fathead minnow—a fractional spawner. Trans Am Fish Soc 111:35–40

    Article  Google Scholar 

  • Gillaspie, J (2015) Compliance options for Oregon wastewater treatment plants. Assoc Clean Water Agencies 1–18.  http://www.oracwa.org/documents/ComplianceOptionsupdate1115.pdf  Accessed 7 Nov 2017

  • Golovanov VK (2006) The ecological and evolutionary aspects of thermoregulation behavior on fish. J Ichthyol 46(2):S180–S187

    Article  Google Scholar 

  • Gotceitas V, Puvanendran V, Leader LL, Brown JA (1996) An experimental investigation of the ‘match/mismatch’ hypothesis using larval Atlantic cod. Mar Ecol Prog Ser 130:29–37

    Article  Google Scholar 

  • Grant JWA, Colgan PW (1982) Reproductive success and mate choice in the johnny darter, Etheostoma nigrum (Pisces: Percidae). Can J Zool 61:437–446

    Article  Google Scholar 

  • Haworth MR, Bestgen KR (2017) Flow and water temperature affect reproduction and recruitment of a Great Plains cyprinid. Can J Fish Aquat Sci 74:853–863

    Article  Google Scholar 

  • Healy TM, Schulte PM (2012) Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Phys Biochem Zool 85(2):107–119

    Article  CAS  Google Scholar 

  • Heino J, Erkinaro J, Huusko A, Luoto M (2015) Climate change effects on freshwater fishes, conservation and management. In: Closs GP, Krkosek M, Olden JD (eds) Conservation of freshwater fishes. Cambridge University Press, Cambridge, p 76–106

  • Hester ET, Doyle MW (2011) Human impacts to river temperature and their effects on biological processes: a quantitative synthesis. J. Am Water Resour Assoc 47(3):571–587

    Article  Google Scholar 

  • Hirshfield MF (1980) An experimental analysis of reproductive effort and cost in the Japanese medaka, Oryzias Latipe. Ecology 61(2):282–292

    Article  Google Scholar 

  • Hokanson KE, McCormick JH, Jones BR, Tucker JH (1973) Thermal requirements for maturation, spawning, and embryo survival of the brook trout Salvelinus fontinalis. J. Fish Resour Board Can 30:975–984

    Article  Google Scholar 

  • Hovel RA, Carlson SM, Quinn TP (2017) Climate change alters the reproductive phenology and investment of a lacustrine fish, the three-spine stickleback. Glob Change Biol 23(6):2308–2320

    Article  Google Scholar 

  • Huss M, Byström P, Strand Å, Eriksson LO, Persson L (2008) Influence of growth history on the accumulation of energy reserves and winter mortality in young fish. Can J Fish Aquat Sci 65(10):2149–2156

    Article  Google Scholar 

  • Ingersoll CG, Claussen DL (1984) Temperature selection and critical thermal maxima of the fantail darter Etheostoma flabellare, and johnny darter, E. nigrum, related to habitat and season. Environ Biol Fishes 11(2):131–138

    Article  Google Scholar 

  • Jin Y, Shu L, Sun L, Liu W, Fu Z (2010) Temperature and photoperiod affect the endocrine disruption effects of ethinylestradiol, nonylphenol and their binary mixture in zebrafish (Danio rerio). Comp Biochem Phys C 151(2):258–263

    Google Scholar 

  • Justus JA, Fox MG (1994) The cost of early maturation on growth, body condition and somatic lipid content in a lake pumpkinseed (Lepomis gibbosus) population. Ecol Freshw Fish 3(1):9–17

    Article  Google Scholar 

  • Kinouchi T, Yagi H, Miyamoto M (2007) Increase in stream temperature related to anthropogenic heat input from urban wastewater. J Hydrol 335:78–88

    Article  Google Scholar 

  • Kocovsky PM, Carline RF (2001) Influence of extreme temperatures on consumption and condition of walleyes in Pymatuning Sanctuary, Pennsylvania. N Am J Fish Manage 21(1):198–207

    Article  Google Scholar 

  • Lewis WM, McCutchan JH (2012) Regulatory temperature compliance for the South Platte River Downstream of the Metro District R.W. Hite Treatment Facility (RWHTF). Metro Wastewater Reclamation District Report 326

  • Lessard JL, Hayes DB (2003) Effects of elevated water temperature on fish and macroinvertebrate communities below small dams. River Res Appl 19(7):721–732

    Article  Google Scholar 

  • Lukšienė D, Sandström O, Lounasheimo L, Andersson J (2000) The effects of thermal effluent exposure on the gametogenesis of female fish. J Fish Biol 56:37–50

    Article  Google Scholar 

  • Lyons J, Rypel A, Rasmussen PW, Burzynski TE, Eggold BT, Myers JT, Paoli TJ, McIntyre PB (2015) Trends in the reproductive phenology of two Great Lakes Fishes. Trans Am Fish Soc 144(6):1263–1274

    Article  Google Scholar 

  • Mackay ME, Lazier CB (1993) Estrogen responsiveness of vitellogenin gene expression in rainbow trout (Oncorhynchus mykiss) kept at different temperatures. Gen Comp Endocr 89:255–266

    Article  CAS  Google Scholar 

  • McDonald RI, Green P, Balk D, Fekete BM, Revenga C, Todd M, Montgomery M (2011) Urban growth, climate change, and freshwater availability. Proc Natl Acad Sci USA 108(15):6312–6317

    Article  CAS  Google Scholar 

  • McMillan VE, Smith RJF (1974) Agonistic and reproductive behavior of the fathead minnow (Pimephales promelas Rafinesque). Z Tierpsychol 34(1):25–58

    CAS  Google Scholar 

  • Miller DH, Jensen KM, Villeneuve DL, Kahl MD, Makynen EA, Durhan EJ, Ankley GT (2007) Linkage of biochemical responses to population-level effects: A case study with vitellogenin in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 26(3):521–527

    Article  CAS  Google Scholar 

  • Neill WH, Magnuson JJ (1974) Distributional ecology and behavioral thermoregulation of fishes in relation to heated effluent from a power plant at Lake Monona, Wisconsin. Trans Am Fish Soc 103(4):663–710

    Article  Google Scholar 

  • Nelson KC, Palmer MA (2007) Stream temperature surges under urbanization and climate change: Data, models, and responses. J Am Water Resour Assoc 43(2):440–452

    Article  Google Scholar 

  • Okuzawa K, Furukawa K, Aida K, Hanyu I (1989) Effects of photoperiod and temperature on gonadal maturation and plasma steroid and gonadotropin levels in a cyprinid fish the honmoroko Gnathopogon caerulescens. Gen Comp Endocr 75(1):139–147

    Article  CAS  Google Scholar 

  • Pankhurst NW, Porter MJR (2003) Cold and dark or warm and light: Variations on the theme of environmental control of reproduction. Fish Physiol Biochem 28:385–389

    Article  CAS  Google Scholar 

  • Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshw Res 62(9):1015–1026

    Article  CAS  Google Scholar 

  • Pankhurst NW, Purser GJ, Van der Kraak GT, Thomas PM, Forteath GNR (1996) Effect of holding temperature on ovulation, egg fertility, plasma levels of reproductive hormones, and in vitro ovarian steroidogenesis in the rainbow trout Oncorhynchus mykiss. Aquaculture 146:277–290

    Article  CAS  Google Scholar 

  • Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol Part A 132(4):739–761

    Article  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315(5808):95–97

    Article  Google Scholar 

  • Post JR, Evans D (1989) Size-dependent overwinter mortality of young-of-year yellow perch (Perca flavescens): Laboratory, in situ enclosure, and field experiments. Can J Fish Aquat Sci 46(11):1958–1968

    Article  Google Scholar 

  • Propst DL, Carlson CA (1989) Life history notes and distribution of the johnny darter, Etheostoma nigrum (Percidae), in Colorado. Southwest Nat 34(2):250–259

  • Rader RB, Belish T, Young MK, Rothlisberger J (2007) The scotopic visual sensitivity of four species of trout: a comparative study. West N Am Nat 67(4):524–537

    Article  Google Scholar 

  • Rahel FJ (2002) Using current biogeographic limits to predict fish distributions following climate change. In: McGinn N (ed) Fisheries in a changing climate. American Fisheries Society Symposium, Bethesda, MD, vol 32 pp 99–110

    Google Scholar 

  • Reimers E, Kjørrefjord AG, Stavøstrand SM (1993) Compensatory growth and reduced maturation in second sea winter farmed Atlantic salmon following starvation in February and March. J Fish Biol 43(5):805–810

    Article  Google Scholar 

  • Reynolds WW, Casterlin ME (1979) Behavioral thermoregulation and the “final preferendum” paradigm. Am Zool 19:211–224

    Article  Google Scholar 

  • Saylor ML (1973) Effect of harvesting methods on production of fingerling fathead minnows. Progress Fish Cultur 35(2):110–114

    Article  Google Scholar 

  • Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocr 165:549–556

    Article  CAS  Google Scholar 

  • Schmid T, Gonzalez-Valero J, Rufli H, Dietrich DR (2002) Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). Toxicol Lett 131(1):65–74

    Article  CAS  Google Scholar 

  • Schwindt AR, Winkelman DL, Keteles K, Murphy M, Vajda AM (2014) An environmental estrogen disrupts fish population dynamics through direct and transgenerational effects on survival and fecundity. J Appl Ecol 51(3):582–591

    Article  CAS  Google Scholar 

  • Secor DH, Houde ED (1995) Temperature effects on the timing of striped bass egg production, larval viability, and recruitment potential in the Patuxent River (Chesapeake Bay). Estuaries 18(3):527–544

    Article  Google Scholar 

  • Shimizu A (2003) Effect of photoperiod and temperature on gonadal activity and plasma steroid levels in a reared strain of the mummichog (Fundulus heteroclitus) during different phases of its annual reproductive cycle. Gen Comp Endocrinol 131(3):310–324

    Article  CAS  Google Scholar 

  • Shuter BJ, Finstad AG, Helland IP, Zweimüller I, Hölker F (2012) The role of winter phenology in shaping the ecology of freshwater fish and their sensitivities to climate change. Aquat Sci 74:637–657

    Article  CAS  Google Scholar 

  • Shuter BJ, Post JR (1990) Climate, population viability, and the zoogeography of temperate fishes. Trans Am Fish Soc 119(2):314–336

    Article  Google Scholar 

  • Sinclair M, Tremblay MJ (1984) Timing of spawning of atlantic herring (Clupea harengus harengus) populations and the match-mismatch theory. Can J Fish Aquat Sci 41:1055–1065

    Article  Google Scholar 

  • Speare EP (1965) Fecundity and egg survival of the central johnny darter (Etheostoma nigrum nigrum) in southern Michigan. Copeia 1965(3):308–314

  • van der Kraak G, Pankhurst NW (1997) Temperature effects on the reproductive performance of fish. In: Wood CM, McDonald DG (eds) Global warming: Implications for freshwater and marine Fish. Cambridge University Press, Cambridge, p 159–176

  • van der Meeren T, Ivannikov VP (2006) Seasonal shift in spawning of Atlantic cod (Gadus morhua L.) by photoperiod manipulation: egg quality in relation to temperature and intensive larval rearing. Aquac Res 37(9):898–913

    Article  Google Scholar 

  • van Vliet MTH, Ludwig F, Zwolsman JJ, Weedon GP, Kabat P (2011) Global river temperatures and sensitivity to atmospheric warming and changes in river flow. Water Resour Res 47(2):32–51

    Google Scholar 

  • Vikingstad E, Anderson E, Hansen TJ, Norberg B, Mayer I, Stefansson SO, Fjelldal PG, Taranger GL (2016) Effects of temperature on the final stages of sexual maturation in Atlantic salmon (Salmo salar L.). Fish Phys Biochem 42(3):895–907

    Article  CAS  Google Scholar 

  • Walsh CJ, Roy AH, Feminella JW (2005) The urban stream syndrome: current knowledge and the search for a cure. J N Am Benthol Soc 24(3):706–723

    Article  Google Scholar 

  • Webb MAH, VanEenennaam JP, Feist GW, Linares-Casenave J, Fitzpatrick MS, Schreck CB, Doroshov SI (2001) Effects of thermal regime on ovarian maturation and plasma sex steroids in farmed white sturgeon, Acipenser transmontanus. Aquaculture 201:137–151

    Article  CAS  Google Scholar 

  • Xin Z, Kinouchi T (2013) Analysis of stream temperature and heat budget in an urban river under strong anthropogenic influences. J Hydrol 489:16–25

    Article  Google Scholar 

Download references

Acknowledgements

We thank Brandon Taro from Wyoming Game and Fish for disease diagnostics and treatment assistance; Kyle Wilson and Riley Miller for assistance with lab work and daily fish care; James Dorsch, Jordan Parman, and the rest of the environmental monitoring and assessment crew at the Metro Wastewater Reclamation District, Denver, Colorado for assistance in collecting fish for our study. Steve DeVries and Joe Bobbitt from the University of Wyoming Red Buttes Environmental Biology Laboratory provided assistance with equipment use and construction of the exposure system. Funding was provided by the Metro Wastewater Reclamation District in Denver, CO. Tyler Firkus also received support from the George T. Baxter Award and the Vern Bressler Fisheries Scholarship of the University of Wyoming. We also acknowledge the anonymous reviewers for their valuable comments that helped improve the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tyler Firkus.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Firkus, T., Rahel, F.J., Bergman, H.L. et al. Warmed Winter Water Temperatures Alter Reproduction in Two Fish Species. Environmental Management 61, 291–303 (2018). https://doi.org/10.1007/s00267-017-0954-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00267-017-0954-9

Keywords

Navigation