Abstract
Knowledge on factors influencing traits during critical early growth periods is essential for predicting population persistence. Genetic effects and microhabitat stream conditions at female selected oviposition sites influence larval phenotypes. However, limited work has examined contributions of both factors across sequential ontogenetic stages for larvae of wild origin. Using a wild population of lake sturgeon (Acipenser fulvescens) from Black Lake, Michigan (USA), fertilized eggs were collected from stream substrate just prior to hatch at one-meter intervals along seven transect lines at an adult-selected spawning area. Microhabitat variables (depth, discharge, substrate size) were recorded at egg collection points. Body length, body area, and yolk-sac area were quantified for yolk-sac larvae (N = 359) at the time of hatch. Following the onset of exogenous feeding, larval growth was measured weekly for four weeks. Parentage was assigned using genetic-based analysis. Inter-individual variation in phenotypic traits quantified at hatch were attributed to stream microhabitat variables; mean depth had the largest influence. No additive genetic effects were detected at hatch. Post-emergence larval growth significantly varied within and among half-sibling groups with the greatest range in body size observed at 33 days post-hatch. Additive genetic variance and heritability increased with age. Results demonstrate that female-selected incubation habitats influenced traits at hatch for wild-origin fish, but effects do not persist to a sequential ontogenetic stage. Alternatively, growth after the onset of exogenous feeding was largely influenced by intrinsic (genetic) factors which must be considered when designing and implementing rehabilitation strategies for lake sturgeon and potentially other threatened riverine fishes.
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References
Allan JD, Castillo MM (2007) Stream ecology: structure and function of running waters. Springer, Dordrecht
Aubry LM, Rockwell RF, Cooch EG, Brook RW, Mulder CPH, Koons DN (2013) Climate change, phenology, and habitat degradation: drivers of gosling body condition and juvenile survival in lesser snow geese. Glob Change Biol 19:149–160
Baker EA, Scribner KT (2017) Cohort-specific estimates of first-year survival are positively associated with size at stocking for lake sturgeon Acipenser fulvescens (Rafinesque 1817) stocked in black Lake, Michigan, USA. J Appl Ichthyol 33:892–897
Baker DW, McAdam DSO, Boucher M, Huynh KT, Brauner CJ (2014) Swimming performance and larval quality are altered by rearing substrate at early life stages in white sturgeon, Acipenser transmontanus (Richardson, 1836). J Appl Ichthyol 30:1461–1472
Baras E, Lucas MC (2010) Individual growth trajectories of sibling Brycon moorei raised in isolation since egg stage, and their relationship with aggressive behaviour. J Fish Biol 77:985–997
Baril A-M, Buszkiewicz JT, Biron PM, Phelps QE, Grant JWA (2017) Lake sturgeon (Acipenser fulvescens) spawning habitat: a quantitative review. Can J Fish Aquat Sci:1–9
Bates D, Vasquez AI (2014) Pedigreemm: pedigree-based mixed-effects models. R package version 0.3–3. https://CRAN.R-project.org/package=pedigreemm
Benjankar R, Tonina D, Marzadi A, McKean J, Isaak DJ (2016) Effects of habitat quality and ambient hyporheic flows on salmon spawning site selection. J Geophys Res Biogeosci 121:1222–1235
Billard R, Lecointre G (2001) Biology and conservation of sturgeon and paddlefish. Rev Fish Biol Fish 10:335–392
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
Bocast C, Bruch RM, Koenigs RP (2014) Sound production of spawning lake sturgeon (Acipenser fulvescens Rafinesque, 1817) in the Lake Winnebago watershed, Wisconsin, USA. J Appl Ichthyol 30:1186–1194
Boucher MA, McAdam SO, Shrimpton JM (2014) The effect of temperature and substrate on the growth, development and survival of larval white sturgeon. Aquac 430:139–148
Bozek MA, Baccante DA, Lester NP (2011) Walleye and sauger life history. In: Barton BA (ed) Biology, management, and culture of walleye and sauger. USA pp, American Fisheries Society, Bethesda, Maryland, pp 233–301
Bruch RM, Binkowski FP (2002) Spawning behavior of lake sturgeon (Acipenser fulvescens). J Appl Ichthyol 18:570–579
Bruch RM, Haxton TJ, Koenigs R, Welsh A, Kerr SJ (2016) Status of lake sturgeon (Acipenser fulvescens Rafinesque 1817) in North America. J Appl Ichthyol 32:162–190
Campeas A, Brun-Bellut J, Baras E, Kestemont P, Gardeur JN (2009) Growth heterogeneity in rearing sea bass (Dicentrarchus labrax): test of hypothesis with an iterative energetic model. An 3(9):1299–1307
Caroffino DC, Sutton TM, Elliott RF, Donofrio MC (2010) Predation on early life stages of lake sturgeon in the Peshtigo River, Wisconsin. Trans Am Fish Soc 139:1846–1856
Castanheira MF, Conceicao LEC, Millot S, Rey S, Begout ML, Damsgard B, Kristiansen T, Hoglund E, Overli O, Martins CIM (2017) Copings styles in farmed fish: consequences for aquaculture. Rev Aqua 9:23–41
Chiotti JA, Holtgren JM, Auer NA, Ogren SA (2008) Lake sturgeon spawning habitat in the big Manistee River, Michigan. North Am J Fish Manag 28:1009–1019
Choe MK, Yamazaki F (1998) Estimation of heritabilities of growth traits, and phenotypic and genetic correlations in juvenile Masu salmon Oncorhynchus masou. Fish Sci 64(6):903–908
Clifford D, McCullagh P (2014) The regress package R package version 1.3-15
Cummins KW (1962) An evaluation of some techniques for the collection and analysis of benthic samples with special emphasis on lotic waters. Am Midl Naturalist 67:477–504
Dammerman KJ, Steibel JP, Scribner KT (2015) Genetic and environmental components of phenotypic and behavioral trait variation during lake sturgeon (Acipenser fulvescens) early ontogeny. Environ Biol Fish 98:1659–1670
Dammerman KJ, Steibel JP, Scribner KT (2016) Increases in the mean and variability of thermal regimes result in differential phenotypic responses among genotypes during early ontogenetic stages of lake sturgeon (Acipenser fulvescens). Evol Appl 9(10):1258–1270
Dammerman KJ, Webb MAH, Scribner KT (2019) Riverine characteristics and adult demography influence female lake sturgeon (Acipenser fulvescens) spawning behavior, reproductive success, and ovarian quality. Can J Fish Aquat Sci 76:1147–1160
Dettlaff TA, Ginsburg AS, Schmalhausen OI (1993) Sturgeon fishes: developmental biology and aquaculture. Springer-Verlag, Berlin
Dormann CF, McPherson JM, Araújo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, Kühn I, Ohlemüller R, Peres-Neto PR, Reineking B, Schröder B, Schurr FM, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30(5):609–628
Dumont B, D’Amours J, Thibodeau S, Dubuc N, Verdon R, Garceau S, Bilodeau P, Mailhot Y, Fortin R (2011) Effects of the development of a newly created spawning ground in the des Prairies River (Quebec, Canada) on the reproductive success of lake sturgeon (Acipenser fulvescens). J Appl Ichthyol 27:394–404
Duong TY, Scribner KT, Crossman JA, Forsythe PS, Baker EA (2011) Environmental and maternal effects on embryonic and larval developmental time until dispersal of lake sturgeon (Acipenser fulvescens). Can J Fish Aquat Sci 68:643–654
Durham BW, Wilde GR (2008) Composition and abundance of drifting fish larvae in the Canadian River, Texas. J Freshw Ecol 23(2):273–280
Eckes OT, Aloisi DB, Sandheinrich MB (2015) Egg and larval development index for lake sturgeon. NA J Aquac 77:211–216
Falcy MR (2015) Density-dependent habitat selection of spawning Chinook salmon: broad-scale evidence and implications. J Anim Ecol 84:545–553
Fausch KD, Torgersen CE, Baxter CV, Li HW (2002) Landscapes to riverscapes: bridging the gap between research and conservation of stream fishes. BioScience 52(6):483
Finley AO, Forsythe PS, Crossman JA, Baker E, Scribner KT (2018) Assessing impact of exogenous features on biotic phenomena in the presence of spatial dependence: a lake sturgeon case study in natural stream settings. PLoSONE 13(12):e0204150
Flowers HJ, Pine WE III, Dutterer AC, Johnson KG, Ziewitz JW, Allen MS, Parauka FM (2009) Spawning site selection and potential implications of modified flow regimes on viability of gulf sturgeon populations. Trans Am Fish Soc 138:1266–1284
Forsythe PS, Crossman JA, Bello NM, Baker EA, Scribner KT (2012a) Individual-based analyses reveal high repeatability in timing and location of reproduction in lake sturgeon (Acipenser fulvescens). Can J Fish Aquat Sci 68:1–13
Forsythe PS, Scribner KT, Crossman JA, Ragavendran A, Baker EA, Davis C, Smith KK (2012b) Environmental and lunar cues are predictive of timing of river entry and spawning site arrival in lake sturgeon. K Fish Biol 81:35–53
Forsythe PS, Scribner KT, Crossman JA, Ragavendran A, Baker EA (2013) Experimental assessment of the magnitude and sources of lake sturgeon egg mortality. Trans Am Fish Soc 142:1005–1011
Fox J, Weisberg S (2011) An R companion to applied regression, Second edn. Sage, Thousand Oaks
Fujimoto M, Crossman JA, Scribner KT, Marsh TL (2013) Microbial community assembly and succession on lake sturgeon egg surfaces as a function of simulated spawning stream flow rate. Microb Ecol 66:500–511
Fullerton AH, Garvey JE, Wright RA, Stein RA (2000) Overwinter growth and survival of largemouth bass: interactions among size, food, origin, and winter severity. Trans Am Fish Soc 129:1–12
Garrido S, Ben-Hamadou R, Santos AMP, Ferreira S, Teodósio MA, Cotano U, Irigoien X, Peck MA, Saiz E, Ré P (2015) Born small, die young: intrinsic, size-selective mortality in marine larval fish. Sci Rep 5:17065
Gerkens M, Thiel R (2001) Habitat use of age-0 twaite shad (Alosa fallax Lacepede, 1803) in the tidal freshwater region of the Elbe River, Germany. Bull Fr Pêche Piscic 362-363:773–784
Green BS, Anthony KRN, McCormick MI (2006) Position of egg within a clutch is linked to size at hatching in a demersal tropical fish. J Exp Mar Biol Ecol 329:144–152
Grutter AS, Blomberg SP, Fargher B, Kuris AM, McCormick MI, Warner RR (2017) Size-related mortality due to gnathiid isopod micropredation correlates with settlement size in coral reef fishes. Coral Reefs 36:549–559
Hastings RP, Bauman JM, Baker EA, Scribner KT (2013) Post-hatch dispersal of lake sturgeon (Acipenser fulvescens, Rafinesque, 1817) yolk-sac larvae in relation to substrate in an artificial stream. J Appl Ichthyol 29(6):1208–1213
Hay-Chmielewski EM, Whelan GE (1997) Lake sturgeon rehabilitation strategy. Special report 18, fisheries division, Michigan Department of Natural Resources, Ann Arbor
Hayes DB, Caroffino DC (2012) Michigan’s Lake sturgeon rehabilitation strategy. Michigan Department of Natural Resources, Fisheries Division Special Report 62, Lansing
Hjort, J (1914) Fluctuations in the great fisheries of northern Europe viewed in the light of biological research. Rapports Et Proces-Verbaux Volume XX
Houle D (1998) How should we explain variation in the genetic variance of traits? Genetica 103:241–253
Hurst TP, Conover DO (1998) Winter mortality of young-of-the-year Hudson River striped bass (Morone saxatilus) – size dependent patterns and effects on recruitment. Can J Fish Aquat Sci 55(5):1122–1130
Jensen AJ, Finstad B, Fiske P (2018) Evidence for the linkage of survival of anadromous Arctic char and brown trout during winter to marine growth during the previous summer. Can J Fish Aquat Sci 75:663–672
Jones OR, Wang JL (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1006
Kamler E (2008) (2008) resource allocation in yolk-feeding fish. Rev Fish Biol Fish 18:143–200
Kanno Y, Schmidt CU, Cook SB, Mattingly HT (2012) Variation in microhabitat use of the threatened spotfin chub (Erimonax monachus) among stream sites and seasons. 21: 363–374
Kemp P, Sear D, Collins A, Naden P, Jones I (2011) The impacts of fine sediment on riverine fish. Hydrol Process 25:1800–1821
Kempinger JJ (1988) Spawning and early life history of Lake sturgeon in the Lake Winnebago system, Wisconsin. Am Fish Soc Symp 5:110–122
Kern MM, Nassar AA, Guzy JC, Dorcas ME (2013) Oviposition site selection by spotted salmanders (Ambystoma maculatum) in an isolated wetland. J Herpetol 47(3):445–449
King TL, Lubinski BA, Spidle AP (2001) Microsatellite DNA variation in Atlantic sturgeon (Acipenser oxyrinchus) and cross-species amplification in the Acipenseridae. Cons Genet 2:103–119
Kinghorn BP (1983) A review of quantitative genetics in fish breeding. Aquac 31:283–304
Kruuk LEB, Hadfield JD (2007) How to separate genetic and environmental causes of similarity between relatives. J Evol Biol 20:1890–1903
Letcher BH, Rice JA, Crowder LB, Rose KA (1996) Variability in survival of larval fish: disentangling components with a generalized individual-based model. Can J Fish Aquat Sci 53:787–801
Lowerre-Barbieri SK, Brown-Peterson NJ, Murua H, Tomkiewicz J, Wyanski DM, Saborido-Rey F (2011) Emerging issues and methodological advances in fisheries reproductive biology. Mar Coast Fish: Dyn Manag Ecosyst Sci 3:32–51
Martell DJ, Kieffer JD (2007) Persistent effects of incubation temperature on muscle development in larval haddock (Melanogrammus aeglefinus L.). J Exp Biol 210:1170–1182
Martell DJ, Kieffer JD, Trippel EA (2005) Effects of temperature during early life history on embryonic and larval development and growth in haddock. J Fish Biol 66:1558–1575
Martins CIM, Schrama JW, Verreth JAJ (2005) Inherent variation in growth efficiency of African catfish Clarias gariepinus (Burchell, 1822) juveniles. Aquac 36:868–875
McAdam SO (2011) Effects of substrate condition on habitat use and survival by white sturgeon (Acipenser transmontanus) larvae and potential implications for recruitment. Can J Fish Aquat Sci 68(5):812–822
McCluney KE, Poff NL, Palmer MA, Thorp JH, Poole GC, Williams BS, Williams MR, Baron JS (2014) Riverine macrosystems ecology: sensitivity, resistance, and resilience of whole river bains with human alterations. Front Ecol Environ 12(1):48–58
McDonald R, Nelson J, Paragamian V, Barton G (2010) Modeling the effect of flow and sediment transport on white sturgeon spawning habitat in the Kootenai River, Idaho. J Hydraul Eng 136(12):1077–1092
McQuown EC, Sloss BL, Sheehan RJ, Rodzen J, Tranah GJ, May B (2000) Microsatellite analysis of genetic variation in sturgeon: new primer sequences for Scaphirhynchus and Acipenser. Trans Am Fish Soc 129:1380–1388
McQuown EC, Gall GAE, May B (2002) Characterization and inheritance of six microsatellite loci in lake sturgeon. Trans Am Fish Soc 131:299–307
Meyer K, Hill WG (1997) Estimation of genetic and phenotypic covariance for longitudinal data by restricted maximum likelihood. Livest Prod Sci 47:185–200
Miller TJ, Crowder LB, Rice JA, Marschall EA (1988) Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can J Fish Aquat Sci 45(9):1657–1670. https://doi.org/10.1139/f88-197
Mitchell TS, Warner DA, Janzen FJ (2013) Phenotypic and fitness consequences of maternal nest-site choice across multiple early life stages. Ecology 94(2):336–345. https://doi.org/10.1890/12-0343.1
Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc B 363:1635–1645
Nilsson J (1994) Genetics and growth of juvenile Arctic char. Trans Am Fish Soc 123:430–434
Paragamian VL, McDonald R, Nelson GJ, Barton G (2009) Kootenai River velocities, depth, and white sturgeon spawning site selection – a mystery unraveled? J Appl Ichthyol 25(6):640–646
Parsley MJ, Beckman LG, McCabe GT (1993) Spawning and rearing habitat use by white sturgeon in the Columbia River downstream from McNary dam. Trans Am Fish Soc 122:217–227
Pollock MS, Carr M, Kreitals NM, Phillips ID (2015) Review of a species in peril: what we do not know about lake sturgeon may kill them. Environ Rev 23:30–43
Refsnider JM, Janzen FJ (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Ann Rev Ecol Evol Syst 41:39–57
Ribeiro PJ Jr, Diggle PJ (2018) geoR: analysis of geostatistical data. R package version 1:7–5.2.1 https://CRAN.R-project.org/package=geoR
Roseman EF, Manny B, Boase J, Child M, Kennedy G, Craig J, Soper K, Drouin R (2011) Lake sturgeon response to a spawning reef constructed in the Detroit river. J Appl Ichthyol 27:66–76
Rudolf VHW, Rödel MO (2005) Oviposition site selection in a complex and variable environment: the role of habitat quality and conspecific cues. Oecol 142:316–325
Schaeffer LR (2004) Application of random regression models in animal breeding. Livest Prod Sci 86:35–45
Schiemer F, Keckeis H, Kamler E (2003) The early life history stages of riverine fish: ecophysiological and environmental bottlenecks. Comp Biochem Physiol Part A 133:439–449
Siddique MAM, Psenicka M, Cosson J, Dzyuba B, Rodina M, Golpour A, Linhart O (2014) Egg stickiness in artificial reproduction of sturgeon: an overview. Rev Aquac 6:1–12
Smith KM, King DK (2005) Dynamics and extent of larval lake sturgeon Acipenser fulvescens drift in the upper Black River, Michigan. J Appl Ichthyol 21:161–168
Svanbäck R, Schluter D (2012) Niche specialization influences adaptive phenotypic plasticity in the threespine stickleback. Am Nat 180(1):50–59
Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourth edn. Springer, New York
Volkman ET, Pangle KL, Rajchel DA, Sutton TM (2004) Hatchery performance attributes of juvenile Lake sturgeon fed two natural food types. NA J Aquac 66(2):105–112
Wang N, Hayward RS, Noltie DB (1998) Variation in food consumption, growth, and growth efficiency among juvenile hybrid sunfish held individually. Aquac 167:43–52
Wassink L, Huerta B, Li W, Scribner K (2020) Interaction of egg cortisol and offspring experience influences stress-related behaviour and physiology in lake sturgeon. Anim Behav 161:49–59
Welsh AB, Blumberg M, May B (2003) Identification of microsatellite loci in lake sturgeon, Acipenser fulvescens, and their variability in green sturgeon, A. medirostris. Mol Ecol Notes 3:47–55
Wentworth CK (1922) A scale of grade and class terms for clastic sediments. J Geol 30:377–392
Wilson AJ, Réale D (2006) Ontogeny of additive and maternal genetic effects: lessons from domestic mammals. Am Nat 167:E23–E38
Wilson AJ, Kruuk LEB, Coltman DW (2005) Ontogenetic patterns in heritable variation for body size: using random regression models in a wild ungulate population. Am Nat 166:E177–E192
Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26
Withers JL, Sesterhenn TM, Foley CJ, Troy CD, Höök TO (2015) Diets and growth potential of early stage larval yellow perch and alewife in a nearshore region of southeastern Lake Michigan. J Gt Lakes Res 41(3):197–209
Yi Y, Wang Z, Yang Z (2010) Two-dimensional habitat modeling of Chinese sturgeon spawning sites. Ecol Model 221(5):864–875
Yongsheng T, Tianjun X, You L, Songlin C (2011) Estimates of genetic and phenotypic parameters for weight and length in Paralichthys olivaceous (Temminck et Schlegel). Act Oceanol Sin 30(6):58–64
Zarri LJ, Palkovacs EP (2019) Temperature, discharge, and development shape the larval diets of threatened green sturgeon in a highly managed section of the Sacramento River. Ecol Freshw Fish 28(2):257–265
Acknowledgements
Funding for this study was provided by The Great Lakes Fishery Trust, Michigan Department of Natural Resources, International Association for Great Lakes Research, and U.S. Fish and Wildlife Service. All procedures performed in the study involving animals were conducted under animal use and care procedure number (03/14-042-00), and were in accordance with the ethical standards of the Michigan State University Institutional Animal Care and Use Committee. Thank you to Nathan Barton, John Bauman, Jim Holser, James Garavaglia, Adam Umstead, Troy Smith, Lindsey Adams, Sarah Walton, and Jared Militello for assistance in collection of the data. Additionally, thank you to the Scribner lab members, two anonymous reviewers, and the advisory editor for review of the manuscript.
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Funding for this study was provided by The Great Lakes Fishery Trust, Michigan Department of Natural Resources, International Association for Great Lakes Research, and U.S. Fish and Wildlife Service.
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Dammerman, K.J., Steibel, J.P. & Scribner, K.T. Relative influences of microhabitat incubation conditions and genetic parentage effects on lake sturgeon (Acipenser fulvescens) offspring traits during early ontogeny. Environ Biol Fish 103, 1565–1581 (2020). https://doi.org/10.1007/s10641-020-01047-7
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DOI: https://doi.org/10.1007/s10641-020-01047-7