Abstract
In fishes, differences in early rearing environment can have a significant impact on phenotypic development. In the present study, we examined the effect of differences in egg incubation (adhered to substrate or non-adhered and tumbled) and water temperature during early rearing on the development of escape response and volitional swimming performance in lake sturgeon, Acipenser fulvescens, throughout the first year of life. Developing embryos were incubated at 12–14 °C and supplied with flow-through aquarium water and ambient light conditions in McDonald hatching jars or allowed to adhere to substrate. Upon hatch (~ 9 days post-fertilisation, dpf), larvae from each incubation treatment were then acclimated to 16, 18 or 20 °C at a rate of 0.5 °C·day−1 and held at those temperatures until approximately 33 dpf. All treatments were then transferred to a common garden experiment where tanks were fed flow-through river water at ambient temperature and natural light cycles. Sturgeon were fed ad libitum twice daily throughout the growing season and food was withheld when water temperature reached 1.5 °C (~ 6 months post-hatch). Food was reintroduced at the start of spring the following year when water temperature exceeded 2 °C (~ 10.5 months post-hatch). There was no consistent effect of treatment on either volitional swimming or escape responses suggesting significant phenotypic plasticity in these measured traits during the first year of life. There was however an effect of time on these performance metrics that was most likely the result of seasonal differences in temperature throughout the 13-month study.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data available on request from the authors.
Code availability
All statistical analyses were conducted in Rstudio using publicly available packages.
References
Abrahams MV (1995) The interaction between antipredator behaviour and antipredator morphology: experiments with fathead minnows and brook sticklebacks. Can J Zool 73:2209–2215. https://doi.org/10.1139/z95-261
Allen P, Hodge B, Werner I, Cech JJr, (2006) Effects of ontogeny, season, and temperature on the swimming performance of juvenile green sturgeon (Acipenser medirostris). Can J Fish Aquat Sci 63:1360–1369. https://doi.org/10.1139/f06-031
Arnqvist G, Johansson F (1998) Ontogenetic reaction norms of predator-induced defensive morphology in dragonfly larve. Ecology 79(6):1847–1858. https://doi.org/10.1890/0012-9658(1998)079[1847:ORNOPI]2.0.CO;2
Auer N, Baker E (2002) Duration and drift of larval lake sturgeon in Sturgeon River, Michigan. J Appl Ichthyol 18:557–564. https://doi.org/10.1046/j.1439-0426.2002.00393.x
Auer S (2010) Phenotypic plasticity in adult life-history strategies compensates for poor start in life in Trinidadian guppies (Poecilia reticulata). Am Nat 176:818–829. https://doi.org/10.1086/657061
Auer SK, Salin K, Anderson GJ, Metcalfe NB (2016) Flexibility in metabolic rate and activity level determines individual variation in overwinter performance. Oecologia 182:703–712. https://doi.org/10.1007/s00442-016-3697-z
Badyaev AV, Foresman KR, Fernandes MV (2000) Stress and development stability: vegetation removal causes increased fluctuating asymmetry in shrew. Ecology 81(2):336–345. https://doi.org/10.2307/177431
Baker D, McAdam D, Boucher M, Huynh K (1836) Brauner C (2014) Swimming performance and larval quality are altered by rearing substrate at early life phases in white sturgeon, Acipenser transmontanus (Richardson. J Appl Ichthyol 30(6):1461–1472. https://doi.org/10.1111/jai.12642
Batty RS, Blaxter JHS, Fretwell K (1993) Effect of temperature on the escape responses of larval herring, Clupea harengus. Mar Biol 115:523–528. https://doi.org/10.1007/BF00349358
Bjornson F, Earhart M, Anderson WG (2020) To feed or flee: early life-history behavioral strategies of juvenile lake sturgeon (Acipenser fulvescens) during risk-sensitive foraging. Can J Zool 98(8):541–550. https://doi.org/10.1139/cjz-2019-0181
Boysen K, Hoover J (2009) Swimming performance of juvenile white sturgeon (Acipenser transmontanus): training and the probability of entrainment due to dredging. J Appl Icthyol 25:54–59. https://doi.org/10.1111/j.1439-0426.2009.01247.x
Brooks S, Johnston IA (1993) Influence of development and rearing temperature on the distribution, ultrastructure and myosin sub-unit composition of myotomal muscle-fibre types in the plaice, Pleuronectes platessa. Mar Biol 117:501–513. https://doi.org/10.1007/BF00349326
Cai L, Johnson D, Fang M, Mandal P, Tu Z, Huang Y (2017) Effects of feeding, digestion and fasting on the respiration and swimming capability of juvenile sterlet sturgeon (Acipenser ruthenus, Linnaeus 1758). Fish Physiol Biochem 43:279–286. https://doi.org/10.1007/s10695-016-0285-4
Chiasson W, Noakes D, Beamish F (1997) Habitat, benthic prey and distribution of juvenile lake sturgeon (Acipenser fulvescens) in northern Ontario rivers. Can J Fish Aquat Sci 54(12):2866–2871. https://doi.org/10.1139/cjfas-54-12-2866
Chittenden CM, Biagi CA, Davidsen JG, Davidsen AG, Kondo H, McKnight A, Pedersen O-P, Raven PA, Rikardsen AH, Shrimpton JM, Zuehlke B, McKinley RS, Devlin RH (2010) Genetic versus rearing-environment effects on phenotype: hatchery and natural rearing effects on hatchery- and wild-born coho salmon. PLoS ONE 5(8):e12261. https://doi.org/10.1371/journal.pone.0012261
Claireaux G, Lefrançois C (2007) Linking environmental variability and fish performance: integration through the concept of scope for activity. Philos T Royal Soc B 362:2031–2041. https://doi.org/10.1098/rstb.2007.2099
Côté G, Perry G, Blier P, Bernatchez L (2007) The influence of gene-environment interactions on GHR and IGF-I expression and their association with growth in brook charr, Salvelinus fontinalis (Mitchill). BMC Genet 8:87. https://doi.org/10.1186/1471-2156-8-87
Crossin GT, Devlin RH (2017) Predation, metabolic priming and early life-history rearing environment affect the swimming capabilities of growth hormone transgenic rainbow trout. Biol Lett 13:20170279. https://doi.org/10.1098/rsbl.2017.0279
De Mendiburu F (2020) “agricolae: statistical procedures for agricultural research. R package version 1.3–3. https://CRAN.R-project.org/package=agricolae Accessed 1 May 2021
Deslauriers D, Keiffer J (2012) The effects of temperature on swimming performance of juvenile shortnose sturgeon (Acipenser brevirostrum). J Appl Icthyol 28:176–181. https://doi.org/10.1111/j.1439-0426.2012.01932.x
Deslauriers D, Svendsen J, Genz J, Wall A, Baktoft H, Enders E, Anderson WG (2018) Environmental calcium and variation in yolk sac size influence swimming performance in larval lake sturgeon (Acipenser fulvescens). J Exp Biol 221:jeb164533. https://doi.org/10.1242/jeb.164533
Deslauriers D, Yoon GR, Earhart ML, Long C, Klassen CN, Anderson WG (2018b) Over-wintering physiology of age-0 sturgeon (Acipenser fulvescens) and its implications for conservation stocking programs. Environ Biol of Fishes 101:623–637. https://doi.org/10.1007/s10641-018-0724-4
Domenici P, Lefrançois C, Shingles A (2007) Hypoxia and the antipredator behaviours of fishes. Philos T Royal Soc B 362:2105–2121. https://doi.org/10.1098/rstb.2007.2103
Earhart M, Bugg W, Wiwchar CE, Kroeker J, Jeffries K, Anderson G (2020) Shaken, rattled and rolled: the effects of hatchery-rearing techniques on endogenous cortisol production, stress-related gene expression, growth and survival in larval lake sturgeon, Acipenser fulvescens. Aquaculture 735116https://doi.org/10.1016/j.aquaculture.2020.735116
Fox J, Weisberg S (2019) An {R} companion to applied regression, third edition. Sage, Thousand Oaks, CA. https://socialsciences.mcmaster.ca/jfox/Books/Companion Accessed 1 May 2021
Gadomski D, Parsley J (2005) Laboratory studies on the vulnerability of young white sturgeon to predation. N Am J Fish Manag 25:667–674. https://doi.org/10.1577/M03-220.1
Galloway TE (1999) Muscle growth in yolk-sac larvae of the Atlantic halibut as influenced by the temperature in the egg yolk-sac. J Fish Biol Supp A 55:26–43. https://doi.org/10.1111/j.1095-8649.1999.tb01044.x
Galloway TF, Kjørsvik E, Kryvi H (1998) Effect of temperature on viability and axial muscle development in embryos and yolk sac larvae of the northeast Arctic cod (Gadus morhua). Mar Biol 132:559–567. https://doi.org/10.1007/s002270050421
Gessner J, Kamerichs CM, Kloas W, Wuertz S (2009) Behavioural and physiological responses in early life phases of Atlantic sturgeon (Acipenser oxyrhinchus Mitchel 1815) towards different substrates. J Appl Ichthyol 25:83–90. https://doi.org/10.1111/j.1439-0426.2009.01246.x
Hale ME (1999) Locomotor mechanics during early life history: effects of size and ontogeny on fast-start performance of salmonid fishes. J Exp Biol 202:1465–1479
Johnson JH, LaPan SR, Klindt RM, Schiavone A (2006) Lake sturgeon spawning on artificial habitat in the St Lawrence River. J Appl Ichthyol 22:465–470. https://doi.org/10.1111/j.1439-0426.2006.00812.x
Johnston IA (1981) Quantitative analysis of muscle breakdown during starvation in the marine flatfish, Pleuronectes platessa. Cell Tissue Res 214:369–386. https://doi.org/10.1007/BF00249218
Johnston IA (2006) Environment and plasticity of myogensesis in teleost fish. J Exp Biol 209(19):2249–2264. https://doi.org/10.1242/jeb.02153
Johnston IA, Cole NJ, Abercromby M, Vieira VLA (1998) Embryonic temperature modulates muscle growth characteristics in larval and juvenile herring. J Exp Biol 201:623–646
Johnston IA, Dunn J (1987) Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish, in Temperature and Animal Cells (ed. K. Bowler), Symp Soc Exp Biol XXXI 67–93.
Kassambara A (2021) Rstatix: pipe-friendly framework for basic statistical tests. R Package Version 0.7.0. https://CRAN.R-project.org/package=rstatix. Accessed 1 May 2021
Kieffer JD, Penny FM, Papadopoulos V (2014) Temperature has a reduced effect on routine metabolic rates of juvenile shortnose sturgeon (Acipenser brevirostrum). Fish Physiol Biochem 40:551–559. https://doi.org/10.1007/s10695-013-9865-8
Kim MK, Lovell RT (1995) Effect of overwinter feeding regimen on body weight, body composition and resistance to Edwardsiella ictaluri in channel catfish, Ictarulus punctatus. Aquaculture 134:237–246. https://doi.org/10.1016/0044-8486(95)00045-4
Kopf SM, Humphries P, Watts RJ (2014) Ontogeny of critical and prolonged swimming performance for the larvae of six Australian freshwater fish species. Can J Fish Biol 84:1820–1841. https://doi.org/10.1111/jfb.12399
MacNutt MJ, Hinch SG, Lee CG, Phibbs JR, Lotto AG, Healey MC, Farrell AP (2006) Temperature effects on swimming performance, energetics, and aerobic capacities of mature adult pink salmon (Oncorhynchus gorbuscha) compared with those of sockeye salmon (Oncorhynchus nerka). Can J Zool 84:88–97. https://doi.org/10.1139/Z05-181
Macqueen DJ, Robb DH, Olsen T, Melstvert L, Paxton CG, Johnston IA (2008) Temperature until the ‘eyed stage’ of embryogenesis programmes the growth trajectory and muscle phenotype of adult Atlantic salmon. Biol Lett 4(3):294–298. https://doi.org/10.1098/rsbl.2007.0620
Marras S, Killen SS, Claireaux G, Domenici P, McKenzie DJ (2011) Behavioural and kinematic components of the fast-start escape response in fish: individual variation and temporal repeatability. J Exp Biol 214:3102–3110. https://doi.org/10.1242/jeb.056648
Martin SB, Leberg PL (2011) Influence of environmental stress on age- and size-at-maturity: genetic and plastic responses of coastal marsh fishes to changing salinities. Can J Fish Aquat Sci 68:2121–2131. https://doi.org/10.1139/f2011-119
McClelland G, Craig P, Dhekney K, Dipardo S (2006) Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J Physiol 739-751https://doi.org/10.1113/jphysiol.2006.119032
McCollum SA, Van Buskirk J (1996) Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50(2):583–593. https://doi.org/10.1111/j.1558-5646.1996.tb03870.x
Moran C, Young C, Gerry S (2019) Effects of overwintering temperatures on the escape response in cunner (Tautogolabrus adsperus). J Exp Zool 331:319–325. https://doi.org/10.1002/jez.2269
Nathanailides C, Lopez-Albors O, Abellan E, Vazquez JM, Tyler DD, Rowlerson A, Stickland NC (1996) Muscle cellularity in relation to somatic growth in the European sea bass Dicentrarchus labrax (L.). Aquac Res 27:885–889. https://doi.org/10.1046/j.1365-2109.1996.t01-1-00819.x
Ogle DH, Wheeler P, Dinno A (2020) FSA: fisheries stock analysis. R package version 0.8.30. https://github.com/droglenc/FSA. Accessed 1 May 2021
Pang X, Fu S-J, Li X-M, Zhang Y-G (2016) The effects of starvation and re-feeding on growth and swimming performance of juvenile black carp (Mylopharyngodon piceus). Fish Physiol Biochem 42:1203–1212. https://doi.org/10.1007/s10695-016-0210-x
Peterson D, Vecsei P, Jennings C (2007) Ecology and biology of the lake sturgeon: a synthesis of current knowledge of a threatened North American Acipenseridae. Rev Fish Biol Fisher 16:386–404. https://doi.org/10.1007/s11160-006-9018-6
Ramsay JO, Heckman N, Silverman BW (1997) Spline smoothing with model-based penalties. Behav Res Methods Instrum Comput 29:99–106. https://doi.org/10.3758/BF03200573
R Core Team (2020) R: a language and environment for statistical computing. Vienna, Austria. https://www.R-project.org
Richmond A, Kynard B (1995) Ontogenetic behaviour of shortnose sturgeon, Acipenser brevirostrum. Copeia 1:172–182. https://doi.org/10.2307/1446812
RStudio Team (2020) RStudio: integrated development for R. Boston, MA. http://www.rstudio.com
Tytell E, Lauder G (2002) The c-start escape response of Polypterus senegalus: bilateral muscle activity and variation during stage 1 and 2. J Exp Biol 205:2591–2603
Vázquez M, Rodríquez F, Domezian A, Salas C (2002) Development of the brain of the sturgeon Acipenser naccarii. J Appl Ichthyol 18:275–279. https://doi.org/10.1046/j.1439-0426.2002.00375.x
Voesenek C, Muijres F, van Leeuwen J (2018) Biomechanics of swimming in developing larval fish. J Exp Biol 221:1–14. https://doi.org/10.1242/jeb.149583
Wakeling J (2001) Biomechanics of fast-start swimming in fish. Comp Biochem Phys A 131:31–40. https://doi.org/10.1016/s1095-6433(01)00461-5
Walker JA (1998) Estimating velocities and accelerations of animal locomotion: a simulation experiment comparing numerical differentiation algorithms. J Exp Biol 201:981–995
Walker J, Ghalambor C, Griset O, McKenney D, Reznicks D (2005) Do faster starts increase the probability of evading predators? Funct Ecol 19:808–815. https://doi.org/10.1111/j.1365-2435.2005.01033.x
Waraniak JM, Baker EA, Scriber KT (2018) Molecular diet analysis reveals predator–prey community dynamics and environmental factors affecting predation of larval lake sturgeon Acipenser fulvescens in a natural system. J Fish Biol 93:616–629. https://doi.org/10.1111/jfb.13726
Wiley RW, Whaley RA, Satake JB, Fowden M (1993) An evaluation of the potential for training trout to increase poststocking survival in streams. N Am J Fish Manag 13:171–177. https://doi.org/10.1577/1548-8675(1993)013%3c0171:AEOTPF%3e2.3.CO;2
Wishingrad V, Chivers D, Ferrari M (2014a) Relative cost/benefit trade-off between cover-seeking and escape behaviour in an ancestral fish: the importance of structural habitat heterogeneity. Ethology 120:973–981. https://doi.org/10.1111/eth.12269
Wishingrad V, Ferrari M, Chivers D (2014b) Behavioural and morphological defences in a fish with a complex antipredator phenotype. Anim Behav 95:137–143. https://doi.org/10.1016/j.anbehav.2014.07.006
Zubair SN, Peake SJ, Hare JF, Anderson WG (2012) The effect of temperature and substrate on the development of the cortisol stress response in lake sturgeon, Acipenser fulvescens. Rafinesque (1817). Environ Biol Fish 93:577–587. https://doi.org/10.1007/s10641-011-9951-7
Acknowledgements
The authors thank the staff at the Grand Rapids Fish Hatchery for their help with caring for the sturgeon in this yearlong study. We also thank Forrest Bjornson, Amber Hiebert and Thomas Roberts for assistance in running experiments at the hatchery.
Funding
This research was supported by a NSERC/Manitoba Hydro Industrial Research Chair program in conservation aquaculture of lake sturgeon and NSERC Discovery grant #05348–15 awarded to WGA. CB was supported by an NSERC Canadian Graduate Student—Master’s Program award, a University of Manitoba Faculty of Graduate Studies’ Fellowship for Educational Purposes Award, Tri-council Supplement Award and Tri-council Top-up award, a University of Manitoba Department of Biological Sciences’ G.A. Lubinsky Award, and a Fish Futures Inc.’s Ken Stewart Memorial Scholarship; WB was supported by a University of Manitoba Graduate Fellowship Award.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
All described procedures and experiments were approved by the University of Manitoba’s animal care committee (protocol#: F015-007) pursuant to the guidelines established by the Canadian Council for Animal Care.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Appendix 1
Appendix 1
Table 1
Rights and permissions
About this article
Cite this article
Brandt, C., Bugg, W., Groening, L. et al. Effects of rearing temperature on volitional and escape response swimming performance in lake sturgeon, Acipenser fulvescens, from hatch to age 1. Environ Biol Fish 104, 737–750 (2021). https://doi.org/10.1007/s10641-021-01112-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-021-01112-9