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Larval morphology of North American burbot (Lota lota maculosa) from two spatially separated populations

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Abstract

Burbot (Lota lota) are a freshwater fish that exhibits a circumpolar distribution and is considered an indicator species for climate change. Adult burbot were artificially fertilized from the Sturgeon River, Michigan and eggs were incubated until hatch. For 10 weeks following hatch larvae were photographed, along with comparable samples from the Kootenai River, Idaho. Geometric morphology was used to quantify significant morphological differences between groups (n = 510). During the yolk sac stages, body shape near yolk sacs varied, likely linked to absorption differences. In preflexion and flexion stages, variable body shape in the mid-body region coincided to head and tail positions. Mean linear morphological measurement (n = 919) showed significant differences, indicating variability of size at stage between groups. Sturgeon River preflexion larvae growth patterns were variable and exhibited allometric growth in comparison to Kootenai River larvae. This suggests that development of critical structures occurs at different rates allowing for flexibility in habitat settlement or environmental conditions. Both groups showed isometric growth patterns in the flexion stage, indicating that critical structures have developed, marking an important ontogenetic shift. Variability in larval burbot hatching, morphology, and developmental rates is important to their persistence throughout North America.

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References

  • Adams, D. C., M. L. Collyer, & A. Kaliontzopoulou, 2019. Geomorph: software for geometric morphometric analysis [available on internet at https://cran.r-project.org/package=geomorph].

  • Alix, M., D. Zarski, D. Chardard, P. Fontaine, & B. Schaerlinger, 2017. Deformities in newly hatched embryos of Eurasian perch populations originating from two different rearing systems. Journal of Zoology 302: 126–137.

    Article  Google Scholar 

  • Auer, N. A., 1982. Identification of Larval Fishes of the Great Lakes Basin with Emphasis on the Lake Michigan Drainage. Great Lakes Fisheries Commission, Ann Arbor, 776.

    Google Scholar 

  • Berner, D., D. C. Adams, A. C. Grandchamp, & A. P. Hendry, 2008. Natural selection drives patterns of lake–stream divergence in stickleback foraging morphology. Journal of Evolutionary Biology 21: 1653–1665.

    Article  CAS  PubMed  Google Scholar 

  • Bian, X., X. Zhang, Y. Sakurai, X. Jin, T. Gao, R. Wan, & J. Yamamoto, 2014. Temperature-mediated survival, development and hatching variation of Pacific cod Gadus macrocephalus eggs. Journal of Fish Biology 84: 85–105.

    Article  CAS  PubMed  Google Scholar 

  • Blumstein, D. M., D. Mays, & K. T. Scribner, 2017. Spatial genetic structure and recruitment dynamics of burbot (Lota lota) in eastern Lake Michigan and Michigan tributaries. Journal of Great Lakes Research 44: 8.

    Google Scholar 

  • Bogner, D. M., M. A. Kaemingk, & M. R. Wuellner, 2016. Consequences of hatch phenology on stages of fish recruitment. PLOS ONE 11: e0164980.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cott, P. A., T. A. Johnston, & J. M. Gunn, 2013. Stability in life history characteristics among burbot populations across environmental gradients. Transactions of the American Fisheries Society 142: 1746–1756.

    Article  Google Scholar 

  • Cureton, J. C., & R. E. Broughton, 2014. Rapid morphological divergence of a stream fish in response to changes in water flow. Biology Letters 10: 20140352–20140352.

    Article  PubMed Central  Google Scholar 

  • Day, T., J. Pritchard, & D. Schluter, 1994. A comparison of two sticklebacks. Evolution 48: 1723–1734.

    Article  PubMed  Google Scholar 

  • Donner, M. T., & R. Eckmann, 2011. Diel vertical migration of larval and early-juvenile burbot optimizes survival and growth in a deep, pre-alpine lake. Freshwater Biology 56: 916–925.

    Article  Google Scholar 

  • Fuiman, L. A., 1983. Growth gradients in fish larvae. Journal of Fish Biology 23: 117–123.

    Article  Google Scholar 

  • Grabowski, T. B., V. Thorsteinsson, B. J. McAdam, & G. Marteinsdóttir, 2011. Evidence of segregated spawning in a single marine fish stock: sympatric divergence of ecotypes in Icelandic cod. PLoS ONE 6: e17528.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haas, T. C., M. J. Blum, & D. C. Heins, 2010. Morphological responses of a stream fish to water impoundment. Biology Letters 6: 803–806.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hardy, R., & V. L. Paragamian, 2013. A synthesis of Kootenai River burbot stock history and future management goals. Transactions of the American Fisheries Society 142: 1662–1670.

    Article  Google Scholar 

  • Herbing, I. H. von, 2001. Development of feeding structures in larval fish with different life histories: winter flounder and Atlantic cod. Journal of Fish Biology 59: 767–782.

    Article  Google Scholar 

  • Hooker, O. E., J. Barry, T. E. Van Leeuwen, A. Lyle, J. Newton, P. Cunningham, & C. E. Adams, 2016. Morphological, ecological and behavioral differentiation of sympatric profundal and pelagic Arctic charr (Salvelinus alpinus) in Loch Dughaill Scotland. Hydrobiologia 783: 209–221.

    Article  CAS  Google Scholar 

  • Jude, D. J., Y. Wang, S. R. Hensler, & J. Janssen, 2013. Burbot early life history strategies in the Great Lakes. Transactions of the American Fisheries Society 142: 1733–1745.

    Article  Google Scholar 

  • Kamler, E., 2002. Ontogeny of yolk-feeding fish: an ecological perspective. Reviews in Fish Biology and Fisheries 12: 79–103.

    Article  Google Scholar 

  • Kendall, A. W., E. H. Ahilstrom, & H. G. Moser, 1984. Early Life History Stages of Fishes and Their Characters Ontogeny, Systematics, Phylogeny. Allan Press, Lawrence, KS.

    Google Scholar 

  • Koporikov, A. R., V. D. Bogdanov, L. E. Yalkovskaya, S. B. Rakitin, Yu. Ya. Khrunyk, A. S. Aldokhin, A. A. Chemagin, T. K. Tuneva, & A. V. Borodin, 2017. Ecological, morphological, and genetic diversity of burbot (Lota lota L., 1758) in large river basins of Western Siberia. Russian Journal of Ecology 48: 449–458.

    Article  Google Scholar 

  • Kristiansen, T., K. F. Drinkwater, R. G. Lough, & S. Sundby, 2011. Recruitment variability in North Atlantic cod and match-mismatch dynamics. PLoS ONE 6: e17456.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kupren, K., I. Trąbska, D. Żarski, S. Krejszeff, K. Palińska-Żarska, & D. Kucharczyk, 2014. Early development and allometric growth patterns in burbot Lota lota L. Aquaculture International 22: 29–39.

    Article  Google Scholar 

  • Laurel, B. J., T. P. Hurst, L. A. Copeman, & M. W. Davis, 2008. The role of temperature on the growth and survival of early and late hatching Pacific cod larvae (Gadus macrocephalus). Journal of Plankton Research 30: 1051–1060.

    Article  Google Scholar 

  • Mansfield, P. J., D. J. Jude, D. T. Michaud, D. C. Brazo, & J. Gulvas, 1983. Distribution and abundance of larval burbot and deepwater sculpin in Lake Michigan. Transactions of the American Fisheries Society 112: 162–172.

    Article  Google Scholar 

  • Marcil, J., D. P. Swain, & J. A. Hutchings, 2006a. Genetic and environmental components of phenotypic variation in body shape among populations of Atlantic cod (Gadus morhua L.). Biological Journal of the Linnean Society 88: 351–365.

    Article  Google Scholar 

  • Marcil, J., D. P. Swain, & J. A. Hutchings, 2006b. Countergradient variation in body shape between two populations of Atlantic cod (Gadus morhua). Proceedings: Biological Sciences 273: 217–223.

    Google Scholar 

  • Marr, J. C., 1956. The “critical period” in the early life history of marine fishes. ICES Journal of Marine Science 21: 160–170.

    Article  Google Scholar 

  • Marteinsdottir, G., & A. Steinarsson, 1998. Maternal influence on the size and viability of Iceland cod Gadus morhua eggs and larvae. Journal of Fish Biology 52: 1241–1258.

    Google Scholar 

  • McIntyre, T. M., & J. A. Hutchings, 2003. Small-scale temporal and spatial variation in Atlantic cod (Gadus morhua) life history. Canadian Journal of Fisheries and Aquatic Sciences 60: 1111–1121.

    Article  Google Scholar 

  • McPhail, J. D., & V. L. Paragamian, 2000. Burbot biology and life history In Paragamian, Vaughn L., & Willis, David W. (eds), Burbot: Biology, Ecology and Management. Fisheries Management Section of the American Fisheries Society, Spokane, WA: 11–23,

    Google Scholar 

  • Miler, O., & P. Fischer, 2004. Distribution and onshore migration behavior of burbot larvae in Lake Constance, Germany. Journal of Fish Biology 64: 176–185.

    Article  Google Scholar 

  • Miller, J. A., R. A. DiMaria, & T. P. Hurst, 2016. Patterns of larval source distribution and mixing in early life stages of Pacific cod (Gadus macrocephalus) in the southeastern Bering Sea. Deep Sea Research Part II: Topical Studies in Oceanography 134: 270–282.

    Article  CAS  Google Scholar 

  • Mion, J. B., R. A. Stein, & E. A. Marschall, 1998. River discharge drives survival of larval walleye. Ecological Applications 8: 17.

    Article  Google Scholar 

  • Neufeld, M. D., C. A. Davis, K. D. Cain, N. R. Jensen, S. C. Ireland, & C. Lewandowski, 2011. Evaluation of methods for the collection and fertilization of burbot eggs from a wild stock for conservation aquaculture operations: evaluation of methods for collection and fertilization of burbot eggs. Journal of Applied Ichthyology 27: 9–15.

    Article  Google Scholar 

  • Olsen, A., & M. W. Westneat, 2015. StereoMorph: an R package for the collection of 3D landmarks and curves using a stereo camera set-up [available on internet at https://aaronolsen.github.io/software/stereomorph.html].

  • Olsen, E. M., H. Knutsen, J. Gjøsæter, P. E. Jorde, J. A. Knutsen, & N. C. Stenseth, 2004. Life-history variation among local populations of Atlantic cod from the Norwegian Skagerrak coast. Journal of Fish Biology 64: 1725–1730.

    Article  Google Scholar 

  • Osse, J. W. M., J. G. M. van den Boogaart, G. M. J. van Snik, & L. van der Sluys, 1997. Priorities during early growth of fish larvae. Aquaculture 155: 249–258.

    Article  Google Scholar 

  • Palińska-Żarska, K., M. Woźny, M. Kamaszewski, H. Szudrowicz, P. Brzuzan, & D. Żarski, 2020. Domestication process modifies digestion ability in larvae of Eurasian perch (Perca fluviatilis), a freshwater Teleostei. Scientific Reports 10: 2211.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pampoulie, C., T. D. Jörundsdóttir, A. Steinarsson, G. Pétursdóttir, M. Ö. Stefánsson, & A. K. Daníelsdóttir, 2006. Genetic comparison of experimental farmed strains and wild Icelandic populations of Atlantic cod (Gadus morhua L.). Aquaculture 261: 556–564.

    Article  CAS  Google Scholar 

  • Paragamian, V. L., R. Hardy, & B. Gunderman, 2005. Effects of regulated discharge on burbot migration. Journal of Fish Biology 66: 1199–1213.

    Article  Google Scholar 

  • Politis, S. N., F. T. Dahlke, I. A. E. Butts, M. A. Peck, & E. A. Trippel, 2014. Temperature, paternity and asynchronous hatching influence early developmental characteristics of larval Atlantic cod, Gadus morhua. Journal of Experimental Marine Biology and Ecology 459: 70–79.

    Article  Google Scholar 

  • Price, S. A., S. T. Friedman, & P. C. Wainwright, 2015. How predation shaped fish: the impact of fin spines on body form evolution across teleosts. Proceedings of the Royal Society B: Biological Sciences 282: 20151428.

    Article  CAS  PubMed  Google Scholar 

  • R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria [available on internet at https://www.R-project.org/].

  • Rasband, W. S., 1997. ImageJ. U.S. National Institutes of Health, Bethesda, Maryland [available on internet at https://imagej.nih.gov/ij/].

  • Recknagel, H., A. Amos, & K. R. Elmer, 2015. Morphological and ecological variation among populations and subspecies of burbot (Lota lota [L, 1758]) from the Mackenzie River Delta, Canada. The Canadian Field-Naturalist 128: 377.

    Article  Google Scholar 

  • Roa-Varón, A., & G. Ortí, 2009. Phylogenetic relationships among families of Gadiformes (Teleostei, Paracanthopterygii) based on nuclear and mitochondrial data. Molecular Phylogenetics and Evolution 52: 688–704.

    Article  CAS  PubMed  Google Scholar 

  • Rohlf, F., 2015. The tps series of software. Hystrix, the Italian Journal of Mammalogy:, doi: 10.4404/hystrix-26.1-11264.

    Article  Google Scholar 

  • Rohlf, F. J., & D. Slice, 1990. Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39: 40–59.

    Article  Google Scholar 

  • Schludermann, E., M. Tritthart, P. Humphries, & H. Keckeis, 2012. Dispersal and retention of larval fish in a potential nursery habitat of a large temperate river: an experimental study. Canadian Journal of Fisheries and Aquatic Sciences 69: 1302–1315.

    Article  Google Scholar 

  • Stanley, R., P. V. R. Snelgrove, B. deYoung, & R. S. Gregory, 2012. Dispersal patterns, active behavior, and flow environment during early life history of coastal cold water fishes. PLoS ONE 7: e46266.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stapanian, M. A., W. H. Edwards, M. J. Porta, M. T. Bur, & P. M. Kocovsky, 2008. Status of burbot populations in the Laurentian Great Lakes. American Fisheries Society Symposium 59: 111–130.

    Google Scholar 

  • Stapanian, M. A., V. L. Paragamian, C. P. Madenjian, J. R. Jackson, J. Lappalainen, M. J. Evenson, & M. D. Neufeld, 2010. Worldwide status of burbot and conservation measures. Fish and Fisheries 11: 34–56.

    Article  Google Scholar 

  • Synder, D., 1998. Burbot larval evidence for more than one North American species. Colorado State University, Fort Collins, Colorado.

    Google Scholar 

  • Synder, D. E., K. R. Bestgen, & S. C. Seal, 2005. Native Cypriniform Fish Larvae of the Gila River Basin. Colorado State University, Larval Fish Laboratory, Ft. Collins, 191,

    Google Scholar 

  • Trippel, E., G. Kraus, & F. Köster, 2005. Maternal and paternal influences on early life history traits and processes of Baltic cod Gadus morhua. Marine Ecology Progress Series 303: 259–267.

    Article  Google Scholar 

  • Underwood, Z. E., E. G. Mandeville, & A. W. Walters, 2016. Population connectivity and genetic structure of burbot (Lota lota) populations in the Wind River Basin, Wyoming. Hydrobiologia 765: 329–342.

    Article  Google Scholar 

  • Van Houdt, J., 2003. Phylogenetic relationships among Palearctic and Nearctic burbot (Lota lota): Pleistocene extinctions and recolonization. Molecular Phylogenetics and Evolution 29: 599–612.

    Article  CAS  PubMed  Google Scholar 

  • Voesenek, C. J., F. T. Muijres, & J. L. van Leeuwen, 2018. Biomechanics of swimming in developing larval fish. The Journal of Experimental Biology 221: jeb149583.

    Article  PubMed  Google Scholar 

  • Voss, R., H.-H. Hinrichsen, & K. Wieland, 2001. Model-supported estimation of mortality rates in Baltic cod (Gadus morhua callarias L.) larvae: the varying impact of “critical periods.” BMC Ecology 1:4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang, N., & A. Appenzeller, 1998. Abundance, depth distribution, diet composition and growth of perch (Perca fluviatilis) and burbot (Lota lota) larvae and juveniles in the pelagic zone of Lake Constance. Ecology of Freshwater Fish 7: 176–183.

    Article  Google Scholar 

  • Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer, New York.

    Book  Google Scholar 

  • Wold, P. A., K. Hoehne‐Reitan, J. Rainuzzo, & E. Kjørsvik, 2008. Allometric growth and functional development of the gut in developing cod Gadus morhua L. larvae. Journal of Fish Biology 72: 1637–1658.

    Article  Google Scholar 

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Acknowledgements

We would like to thank the Kootenai Tribe of Idaho Native Fish Conservation Program and the Bonneville Power Administration Northwest Power and Conservation Council for supplying us with samples from their hatchery. Funding provided for this project was acquired through the Northern Michigan University (Development Fund, Excellence in Education, Spooner Award) and the Northern Michigan University Biology Department. Fish holding facilities, handling protocols, and experimental protocols were all approved by the Northern Michigan University Institutional Animal Care and Use Committee (IACUC # 328).

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Ritz, T.A., Jensen, N.R. & Leonard, J.B.K. Larval morphology of North American burbot (Lota lota maculosa) from two spatially separated populations. Hydrobiologia 847, 2981–2998 (2020). https://doi.org/10.1007/s10750-020-04288-w

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