1 Influence of Warming Temperatures on Coregonine Embryogenesis Within and Among Species

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1 Influence of Warming Temperatures on Coregonine Embryogenesis Within and Among Species bioRxiv preprint doi: https://doi.org/10.1101/2021.02.13.431107; this version posted February 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Influence of warming temperatures on coregonine embryogenesis within and among species 2 3 Taylor R. Stewart1,5, Mikko Mäkinen2, Chloé Goulon3, Jean Guillard3, Timo J. Marjomäki2, 4 Emilien Lasne4, Juha Karjalainen2, and Jason D. Stockwell5 5 6 1Department of Biology, University of Vermont, Burlington, VT, USA 7 2University of Jyväskylä, Jyväskylä, Finland 8 3University Savoie Mont Blanc, INRAE, CARRTEL, Thonon-les-Bains, France 9 4UMR ESE Agrocampus Ouest-INRAE, Rennes, France 10 5Rubenstein Ecosystem Science Laboratory, University of Vermont, Burlington, VT, USA 11 12 Correspondence: Taylor R. Stewart, Department of Biology, Rubenstein Ecosystem Science 13 Laboratory, University of Vermont, 3 College St, Burlington, VT 05401, USA. Email: 14 [email protected] 15 16 ABSTRACT: 17 The greatest response of lakes to climate change has been the increase in water temperatures on a 18 global scale. The responses of many lake fishes to warming water temperatures are projected to 19 be inadequate to counter the speed and magnitude of climate change, leaving some species 20 vulnerable to decline and extinction. We experimentally evaluated the responses of embryos 21 from a group of cold, stenothermic fishes (Salmonidae Coregoninae) – within conspecifics 22 across lake systems, between congeners within the same lake system, and among congeners 23 across lake systems – to a thermal gradient using an incubation method that enabled global 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.13.431107; this version posted February 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 24 comparisons. Study groups included cisco (Coregonus artedi) from lakes Superior and Ontario 25 (USA), and vendace (C. albula) and European whitefish (C. lavaretus) from Lake Southern 26 Konnevesi (Finland). All species spawn in the fall and their embryos incubate over winter before 27 hatching in spring. Embryos were incubated at water temperatures of 2.0, 4.5, 7.0, and 9.0°C, 28 and the responses to the incubation temperatures were quantified for life-history (i.e., embryo 29 survival and incubation period) and morphological traits (i.e., length-at-hatch and yolk-sac 30 volume). We found contrasting reaction norms to temperature in embryo survival and similar 31 reaction norms to temperature for incubation period, length-at-hatch, and yolk-sac volume in 32 conspecific and congeneric coregonines. For example, congeneric responses differed in 33 embryonic survival in the same system, suggesting species differences in adaptability to 34 warming winter temperatures. Differential levels of parental effects were found within and 35 among study groups and traits suggesting population biodiversity may provide more flexibility 36 for populations to cope with changing inter-annual environmental conditions. Our results suggest 37 coregonines may have a wide range of embryo responses to changing winter conditions as a 38 result of climate change. 39 40 Keywords: climate change, embryo incubation, water temperature, thermal habitat, plasticity, 41 reaction norm, parental effect, Coregonus 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.13.431107; this version posted February 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 42 INTRODUCTION: 43 Freshwater lakes are one of the most sensitive ecosystems to climate change (Jenny et al., 2020; 44 Woolway et al., 2020). One of the greatest threats of climate change to lakes is the 45 unprecedented rise of water temperatures on a global scale (Austin & Colman, 2007; Maberly et 46 al., 2020; O’Reilly et al., 2015; Woolway et al., 2017), although the rise is not projected to be 47 consistent across regions, seasons, or lake types (McCullough et al., 2019; O’Reilly et al., 2015). 48 The greatest seasonal increase in water temperature of seasonally ice-covered lakes is projected 49 to take place during the spring (Schindler et al., 1990; Winslow et al., 2017), and the greatest 50 seasonal increase in air temperature is expected during winter in northern Europe and North 51 America (Christensen et al., 2007). 52 53 Warming spring water temperatures and increases in the length of the frost-free season can 54 prolong annual growing seasons with warmer summers, longer and warmer autumns, and shorter 55 ice-cover duration (Sharma et al., 2019, 2020). Temperature is an abiotic master factor for 56 aquatic ecosystems because water temperature directly affects the physical and chemical 57 properties of water, and phenology, reproductive events, metabolic rates, growth, and survival of 58 aquatic organisms (Brett, 1979; Brown et al., 2004; Busch et al., 2012; Gillooly et al., 2002; 59 Little et al., 2020; Ohlberger et al., 2007). Although the broader impacts of climate-derived 60 changes in lake dynamics remain unclear (Shatwell et al., 2019), the responses of many lake 61 organisms are projected to be inadequate to counter the speed and magnitude of climate change, 62 leaving some species vulnerable to decline and extinction (Hoffmann & Sgrò, 2011). These 63 pressures present challenges for biodiversity conservation and sustainability of ecosystem 64 services. To navigate challenges, a foundational understanding of the primary threats to aquatic 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.13.431107; this version posted February 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 65 ecosystems and organisms across a range of spatial scales from local to global is needed 66 (Halpern et al., 2015; Langhans et al., 2019; Vörösmarty et al., 2010). 67 68 The effects of increasing temperature on lake fishes are predicted to lead to declines in cold- 69 water species and increases in warm-water species (Comte et al., 2013; Hansen et al., 2017). 70 Species that possess narrow optimal thermal ranges, live near their thermal limits, or have long 71 development times at cold temperatures are at-risk under warming climate scenarios as 72 temperature can have strong direct and indirect effects at early-life stages (Blaxter, 1991; Dahlke 73 et al., 2020; Ficke et al., 2007; Lim et al., 2017; Mari et al., 2016; Pepin, 1991). Unlike their 74 marine counterparts, most freshwater fishes are restricted to their lake system, where their ability 75 to evade the effects of climate change is impeded due to the isolated nature of lakes (Ficke et al., 76 2007) and limited swimming capacity during early-life stages (Downie et al., 2020; Herbing, 77 2002). Fundamental questions for eco-evolutionary and conservation biologists in a global 78 change context include how lake fishes will respond to rising water temperatures and what 79 adaptive mechanisms may be involved (Hairston et al., 2005; Kinnison & Hairston, 2007; 80 Pelletier et al., 2009). Shifts in physiology of lake fish populations living close to their upper 81 thermal limits will be required if species are to persist under increasingly stressful thermal 82 conditions (Howells et al., 2016; Woolsey et al., 2015). 83 84 Freshwater whitefishes, Salmonidae Coregoninae (hereafter coregonines), are of great socio- 85 economic value (Ebener et al., 2008; Lynch et al., 2015, 2016; Nyberg et al., 2001; Vonlanthen 86 et al., 2009, 2012), and are also considered to be critically sensitive to the effects of climate 87 change because they are cold, stenothermic fishes (Elliott & Bell, 2011; Isaak, 2014; Jeppesen et 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.13.431107; this version posted February 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 88 al., 2012; Jonsson & Jonsson, 2014; Karjalainen et al., 2015; Karjalainen, Jokinen, et al., 2016; 89 Stockwell et al., 2009). Coregonine fisheries worldwide have experienced population declines 90 due to highly variable and weak year-class strengths (Anneville et al., 2015; Myers et al., 2015; 91 Nyberg et al., 2001; Vonlanthen et al., 2012). In the 20th century, causes of decline included 92 fishing and stocking practices (Anneville et al., 2015) and eutrophication causing poor 93 incubation conditions (Müller, 1992; Vonlanthen et al., 2012). Today, the trophic state of lakes 94 and fisheries management practices are improving, but coregonines continue to be the focus of 95 reintroduction, restoration, and conservation efforts in many lakes (Bronte et al., 2017; Favé & 96 Turgeon, 2008; Zimmerman & Krueger, 2009). Reasons for declining recruitment are unknown, 97 but climate change, increasing water temperatures, and habitat degradation are hypothesized as 98 causal factors (Anneville et al., 2015; Jeppesen et al., 2012; Karjalainen et al., 2015; Karjalainen, 99 Jokinen, et al., 2016; Marjomäki et al., 2004; Nyberg et al., 2001). 100 101 Coregonines generally spawn during late-autumn, embryos incubate over winter, and hatch in 102 late-spring (Karjalainen et al., 2015; Stockwell et al., 2009). The time
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