Ice cover affects the growth of a stream-dwelling fish

Abstract

Protection provided by shelter is important for survival and affects the time and energy budgets of animals. It has been suggested that in fresh waters at high latitudes and altitudes, surface ice during winter functions as overhead cover for fish, reducing the predation risk from terrestrial piscivores. We simulated ice cover by suspending plastic sheeting over five 30-m-long stream sections in a boreal forest stream and examined its effects on the growth and habitat use of brown trout (Salmo trutta) during winter. Trout that spent the winter under the artificial ice cover grew more than those in the control (uncovered) sections. Moreover, tracking of trout tagged with passive integrated transponders showed that in the absence of the artificial ice cover, habitat use during the day was restricted to the stream edges, often under undercut banks, whereas under the simulated ice cover condition, trout used the entire width of the stream. These results indicate that the presence of surface ice cover may improve the energetic status and broaden habitat use of stream fish during winter. It is therefore likely that reductions in the duration and extent of ice cover due to climate change will alter time and energy budgets, with potentially negative effects on fish production.

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References

  1. Abbott JC, Dunbrack RL, Orr CD (1985) The interaction of size and experience in dominance relationships of juvenile steelhead trout (Salmo gairdneri). Behaviour 92:241–253

    Google Scholar 

  2. Acolas ML, Roussel JM, Lebel JM, Baglinière JL (2007) Laboratory experiment on survival, growth and tag retention following PIT injection into the body cavity of juvenile brown trout (Salmo trutta). Fish Res 86:280–284

    Article  Google Scholar 

  3. Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220

    Article  Google Scholar 

  4. Benson B, Magnuson J, Jensen O, Card V, Hodgkins G, Korhonen J, Livingstone D, Stewart K, Weyhenmeyer G, Granin N (2012) Extreme events, trends, and variability in Northern Hemisphere lake-ice phenology (1855–2005). Clim Change 112:299–323

    Article  Google Scholar 

  5. Berg OK, Bremset G (1998) Seasonal changes in the body composition of young riverine Atlantic salmon and brown trout. J Fish Biol 52:1272–1288

    Article  Google Scholar 

  6. 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

    CAS  Article  Google Scholar 

  7. Bonnet X, Fizesan A, Michel C (2013) Shelter availability, stress level and digestive performance in the aspic viper. J Exp Biol 216:815–822

    Article  PubMed  Google Scholar 

  8. Borgmann KL, Conway CJ, Morrison ML (2013) Breeding phenology of birds: mechanisms underlying seasonal declines in the risk of nest predation. PLoS One 8:e65909

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Borgstrøm R, Museth J (2005) Accumulated snow and summer temperature—critical factors for recruitment to high mountain populations of brown trout (Salmo trutta L.). Ecol Freshw Fish 14:375–384

    Article  Google Scholar 

  10. Briones-Fourzán P, Lozano-Álvarez E, Negrete-Soto F, Barradas-Ortiz C (2007) Enhancement of juvenile Caribbean spiny lobsters: an evaluation of changes in multiple response variables with the addition of large artificial shelters. Oecologia 151:401–416

    Article  PubMed  Google Scholar 

  11. Brown RS (1999) Fall and early winter movements of cutthroat trout, Oncorhynchus clarki, in relation to water temperature and ice conditions in Dutch Creek, Alberta. Environ Biol Fish 55:359–368

    Article  Google Scholar 

  12. Brown RS, Power G, Beltaos S, Beddow TA (2000) Effects of hanging ice dams on winter movements and swimming activity of fish. J Fish Biol 57:1150–1159

    Article  Google Scholar 

  13. Brown RS, Hubert WA, Daly SF (2011) A primer on winter, ice, and fish: what fisheries biologists should know about winter ice processes and stream-dwelling fish. Fisheries 36:8–26

    Article  Google Scholar 

  14. Cattanéo F, Lamouroux N, Breil P, Capra H (2002) The influence of hydrological and biotic processes on brown trout (Salmo trutta) population dynamics. Can J Fish Aquat Sci 59:12–22

    Article  Google Scholar 

  15. Coulson T, Albon S, Guinness F, Pemberton J, Clutton-Brock T (1997) Population substructure, local density, and calf winter survival in red deer (Cervus elaphus). Ecology 78:852–863

    Article  Google Scholar 

  16. Cunjak RA (1996) Winter habitat of selected stream fishes and potential impacts from land-use activity. Can J Fish Aquat Sci 53:267–282

    Article  Google Scholar 

  17. Cunjak RA, Power G (1987) The feeding and energetics of stream-resident trout in winter. J Fish Biol 31:493–511

    Article  Google Scholar 

  18. Day CC, Westover MD, Mcmillan BR (2015) Seasonal diet of the northern river otter (Lontra canadensis): what drives prey selection? Can J Zool 93:197–205

    Article  Google Scholar 

  19. Ellis TR, Linnansaari T, Cunjak RA (2013) Passive integrated transponder (PIT) tracking versus snorkeling: quantification of fright bias and comparison of techniques in habitat use studies. Trans Am Fish Soc 142:660–670

    Article  Google Scholar 

  20. Finstad AG, Forseth T, Faenstad TF, Ugedal O (2004) The importance of ice cover for energy turnover in juvenile Atlantic salmon. J Anim Ecol 73:959–966

    Article  Google Scholar 

  21. Finstad AG, Einum S, Forseth T, Ugedal O (2007) Shelter availability affects behaviour, size-dependent and mean growth of juvenile Atlantic salmon. Freshw Biol 52:1710–1718

    Article  Google Scholar 

  22. French WE, Vondracek B, Ferrington LC, Finlay JC, Dieterman DJ (2014) Winter feeding, growth and condition of brown trout Salmo trutta in a groundwater-dominated stream. J Freshw Ecol 29:187–200

    CAS  Article  Google Scholar 

  23. Garvey JE, Ostrand KG, Wahl DH (2004) Energetics, predation, and ration affect size-dependent growth and mortality of fish during winter. Ecology 85:2860–2871

    Article  Google Scholar 

  24. Gerell R (1967) Food selection in relation to habitat in mink (Mustela vison Schreber) in Sweden. Oikos 18:233–246

    Article  Google Scholar 

  25. Giacomini HC, Shuter BJ (2013) Adaptive responses of energy storage and fish life histories to climatic gradients. J Theor Biol 339:100–111

    Article  PubMed  Google Scholar 

  26. Gregory JS, Griffith JS (1996) Winter concealment by subyearling rainbow trout: space size selection and reduced concealment under surface ice and in turbid water conditions. Can J Zool 74:451–455

    Article  Google Scholar 

  27. Gustafsson P, Bergman E, Greenberg LA (2010) Functional response and size-dependent foraging on aquatic and terrestrial prey by brown trout (Salmo trutta L.). Ecol Freshw Fish 19:170–177

    Article  Google Scholar 

  28. Harvey BC, Nakamoto RJ (2013) Seasonal and among-stream variation in predator encounter rates for fish prey. Trans Am Fish Soc 142:621–627

    Article  Google Scholar 

  29. Hedger RD, Næsje TF, Fiske P, Ugedal O, Finstad AG, Thorstad EB (2013) Ice-dependent winter survival of juvenile Atlantic salmon. Ecol Evol 3:523–535

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Heggenes J, Borgstrøm R (1988) Effect of mink, Mustela vison Schreber, predation on cohorts of juvenile Atlantic salmon, Salmo salar L., and brown trout, S. trutta L., in three small streams. J Fish Biol 33:885–894

    Article  Google Scholar 

  31. Heggenes J, Krog OMW, Lindas OR, Dokk JG, Bremnes T (1993) Homeostatic behavioral responses in a changing environment—brown trout (Salmo trutta) become nocturnal during winter. J Anim Ecol 62:295–308

    Article  Google Scholar 

  32. Hicks F (2009) An overview of river ice problems: CRIPE07 guest editorial. Cold Reg Sci Technol 55:175–185

    Article  Google Scholar 

  33. Hodgkins GA, Dudley RW, Huntington TG (2005) Changes in the number and timing of days of ice-affected flow on northern New England rivers, 1930–2000. Clim Change 71:319–340

    CAS  Article  Google Scholar 

  34. Houston AI, Mcnamara JM (1993) A theoretical investigation of the fat reserves and mortality levels of small birds in winter. Ornis Scand 24:205–219

    Article  Google Scholar 

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

    Article  Google Scholar 

  36. Huusko A, Greenberg L, Stickler M, Linnansaari T, Nykanen M, Vehanen T, Koljonen S, Louhi P, Alfredsen K (2007) Life in the ice lane: the winter ecology of stream salmonids. River Res Appl 23:469–491

    Article  Google Scholar 

  37. Huusko A, Mäki-Petäys A, Stickler M, Mykrä H (2011) Fish can shrink under harsh living conditions. Funct Ecol 25:628–633

    Article  Google Scholar 

  38. Johnson JH, Douglass KA (2009) Diurnal stream habitat use of juvenile Atlantic salmon, brown trout and rainbow trout in winter. Fish Manag Ecol 16:352–359

    Article  Google Scholar 

  39. Jonsson B, Jonsson N (2009) A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. J Fish Biol 75:2381–2447

    CAS  Article  PubMed  Google Scholar 

  40. Kollberg I, Bylund H, Huitu O, Björkman C (2014) Regulation of forest defoliating insects through small mammal predation: reconsidering the mechanisms. Oecologia 176:975–983

    Article  PubMed  PubMed Central  Google Scholar 

  41. Larranaga N, Steingrímsson SÓ (2015) Shelter availability alters diel activity and space use in a stream fish. Behav Ecol 26:578–586

    Article  Google Scholar 

  42. Linnansaari T, Cunjak RA (2010) Patterns in apparent survival of Atlantic salmon (Salmo salar) parr in relation to variable ice conditions throughout winter. Can J Fish Aquat Sci 67:1744–1754

    Article  Google Scholar 

  43. Linnansaari T, Cunjak RA (2013) Effects of ice on behaviour of juvenile Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 70:1488–1497

    Article  Google Scholar 

  44. Linnansaari T, Roussel JM, Cunjak RA, Halleraker JH (2007) Efficacy and accuracy of portable PIT-antennae when locating fish in ice-covered streams. Hydrobiologia 582:281–287

    Article  Google Scholar 

  45. Linnansaari T, Cunjak RA, Newbury R (2008) Winter behaviour of juvenile Atlantic salmon Salmo salar L. in experimental stream channels: effect of substratum size and full ice cover on spatial distribution and activity pattern. J Fish Biol 72:2518–2533

    Article  Google Scholar 

  46. Linnansaari T, Alfredsen K, Stickler M, Arnekleiv JV, Harby A, Cunjak RA (2009) Does ice matter? Site fidelity and movements by Atlantic salmon (Salmo salar L.) parr during winter in a substrate enhanced river reach. Riv Res Appl 25:773–787

    Article  Google Scholar 

  47. Magnuson JJ, Robertson DM, Benson BJ, Wynne RH, Livingstone DM, Arai T, Assel RA, Barry RG, Card V, Kuusisto E, Granin NG, Prowse TD, Stewart KM, Vuglinski VS (2000) Historical trends in lake and river ice cover in the Northern Hemisphere. Science 289:1743–1746

    CAS  Article  PubMed  Google Scholar 

  48. Mäki-Petäys A, Erkinaro J, Niemelä E, Huusko A, Muotka T (2004) Spatial distribution of juvenile Atlantic salmon (Salmo salar) in a subarctic river: size-specific changes in a strongly seasonal environment. Can J Fish Aquat Sci 61:2329–2338

    Article  Google Scholar 

  49. Marchand PJ (2014) Life in the cold: an introduction to winter ecology, 4th edn. University Press of New England, Lebanon

    Google Scholar 

  50. McNamara JM, Houston AI (2008) Optimal annual routines: behaviour in the context of physiology and ecology. Philos Trans R Soc Lond B Biol Sci 363:301–319

    Article  PubMed  PubMed Central  Google Scholar 

  51. Millidine KJ, Armstrong JD, Metcalfe NB (2006) Presence of shelter reduces maintenance metabolism of juvenile salmon. Funct Ecol 20:839–845

    Article  Google Scholar 

  52. Palm D, Brännäs E, Nilsson K (2009) Predicting site-specific overwintering of juvenile brown trout (Salmo trutta) using a habitat suitability index. Can J Fish Aquat Sci 66:540–546

    Article  Google Scholar 

  53. Prentice EF, Flagg TA, Mccutcheon CS (1990) Feasibility of using implantable passive integrated transponder (PIT) tags in salmonids. Am Fish Soc Symp 7:317–322

    Google Scholar 

  54. Reid DG, Code TE, Reid ACH, Herrero SM (1994) Food habits of the river otter in a boreal ecosystem. Can J Zool 72:1306–1313

    Article  Google Scholar 

  55. Reid D, Bilodeau F, Krebs C, Gauthier G, Kenney A, Gilbert BS, Leung MY, Duchesne D, Hofer E (2012) Lemming winter habitat choice: a snow-fencing experiment. Oecologia 168:935–946

    Article  PubMed  Google Scholar 

  56. Riley WD, Ives MJ, Pawson MG, Maxwell DL (2006) Seasonal variation in habitat use by salmon, Salmo salar, trout, Salmo trutta and grayling, Thymallus thymallus, in a chalk stream. Fish Manag Ecol 13:221–236

    Article  Google Scholar 

  57. Schindler DE, Scheuerell MD (2002) Habitat coupling in lake ecosystems. Oikos 98:177–189

    Article  Google Scholar 

  58. Skierczyński M, Wiśniewska A, Stachura-Skierczyńska K (2008) Feeding habits of American mink from Biebrza wetlands affected by varied winter conditions. Mammalia 72:135–138

    Google Scholar 

  59. Staines BW (1976) The use of natural shelter by red deer (Cervus elaphus) in relation to weather in North-east Scotland. J Zool 180:1–8

    Article  Google Scholar 

  60. Valdimarsson SK, Metcalfe NB (2001) Is the level of aggression and dispersion in territorial fish dependent on light intensity? Anim Behav 61:1143–1149

    Article  Google Scholar 

  61. Valdimarsson SK, Metcalfe NB, Thorpe JE, Huntingford FA (1997) Seasonal changes in sheltering: effect of light and temperature on diel activity in juvenile salmon. Anim Behav 54:1405–1412

    Article  PubMed  Google Scholar 

  62. Watz J, Piccolo JJ (2011) The role of temperature in the prey capture probability of drift-feeding juvenile brown trout (Salmo trutta). Ecol Freshw Fish 20:393–399

    Article  Google Scholar 

  63. Watz J, Piccolo JJ, Greenberg L, Bergman E (2012) Temperature-dependent prey capture efficiency and foraging modes of brown trout Salmo trutta. J Fish Biol 81:345–350

    CAS  Article  PubMed  Google Scholar 

  64. Watz J, Bergman E, Piccolo JJ, Greenberg L (2013) Effects of ice cover on the diel behaviour and ventilation rate of juvenile brown trout. Freshw Biol 58:2325–2332

    Google Scholar 

  65. Watz J, Bergman E, Piccolo JJ, Greenberg L (2014a) Prey capture rates of two species of salmonids (Salmo trutta and Thymallus thymallus) in an artificial stream: effects of temperature on their functional response. Mar Freshw Behav Phy 47:93–99

    Article  Google Scholar 

  66. Watz J, Piccolo J, Bergman E, Greenberg L (2014b) Day and night drift-feeding by juvenile salmonids at low water temperatures. Environ Biol Fishes 97:505–513

    Article  Google Scholar 

  67. Watz J, Bergman E, Calles O, Enefalk Å, Gustafsson S, Hagelin A, Nilsson PA, Norrgård JR, Nyqvist D, Österling EM, Piccolo JJ, Schneider LD, Greenberg L, Jonsson B (2015) Ice cover alters the behavior and stress level of brown trout Salmo trutta. Behav Ecol 26:820–827

    Article  Google Scholar 

  68. Webb PW (1978) Temperature effects on acceleration of rainbow trout (Salmo gairdneri). J Fish Res Board Can 35:1417–1422

    Article  Google Scholar 

  69. Weyhenmeyer G, Westöö A-K, Willén E (2008) Increasingly ice-free winters and their effects on water quality in Sweden’s largest lakes. Hydrobiologia 599:111–118

    CAS  Article  Google Scholar 

  70. Wise MH, Linn IJ, Kennedy CR (1981) A comparison of the feeding biology of mink Mustela vison and otter Lutra lutra. J Zool 195:181–213

    Article  Google Scholar 

  71. Young RA (1976) Fat, energy and mammalian survival. Am Zool 16:699–710

    Article  Google Scholar 

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Acknowledgments

We deeply thank Oscar Askling, Teemu Collin and Lena Watz for their much appreciated help with the field work. We are also grateful to Anders Andersson, Lisette Carlsson, Åsa Enefalk, Anna Hagelin, David Höök, Simon Jonsson, Fredrik Laaksonen, Adam Lewenhaupt, Pia Larsson, Emmy Norrman, Raimo Neergard, Johnny Norrgård, Daniel Nyqvist and Anna Watz for assistance in the field. Karlskoga fiskevårdsförening, Sveaskog, Karlstad stift and the County Board of Örebro län generously let us work in their stream. We especially thank Jim Hellquist at Sveaskog, Martin Engström at the County Board of Örebro län and Peter Randén at Kedjeåsen Uteliv, who were all very supportive throughout the study.

Author contribution statement

JW formulated the idea, had a leading role in the study design, collected and analysed the data and wrote the paper. EB, JJP and LG contributed to the idea and to the study design and provided editorial advice.

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Correspondence to Johan Watz.

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Communicated by Brian Shuter.

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Watz, J., Bergman, E., Piccolo, J.J. et al. Ice cover affects the growth of a stream-dwelling fish. Oecologia 181, 299–311 (2016). https://doi.org/10.1007/s00442-016-3555-z

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Keywords

  • Climate change
  • Energy budget
  • Global warming
  • Salmonid
  • Winter