Surf smelt accelerate usage of endogenous energy reserves under climate change

indicators of overall marine system health. Any reductions to their population abundance can have cascading effects on marine ecosystem productivity and functioning [4, 5]. Despite their ecological importance, they are an understudied forage fish in the North Pacific ecosystem. Surf smelt spawn on gravel beaches during high tides, utilizing the upper third of a beach’s tidal range, typically at tidal heights of seven feet or above [4, 7, 9]. Female surf smelt deposit eggs which adhere to gravel substrate [4, 8]. Once deposited and fertilized, eggs and their developing embryos are subjected to daily exposure in both air and seawater throughout their maturation. Consequently, embryos experience a dynamic range of environmental conditions over diel cycles [8, 10]. During this critical time, surf smelt embryos develop by utilizing mater- nally provided (endogenous) energy in the form of yolk and lipid droplets for approximately 14 to 21 days depending on ambient temperature and sediment humidity [4, 10]. When embryos are fully developed, hatching is triggered by physical disturbance, primarily resulting from tidal activity and wave action [4, 7, 10]. Once hatched, the planktonic surf smelt larvae continue to utilize yolk reserves and lipids contained within an oil globule for energy and development [4] until exogenous feeding begins. Any accelerated usage of stored energy in for- age fish could negatively affect performance and survival, and ultimately, adult recruitment [11]. One mechanism that may force accelerated usage of endogenous energy reserves in surf

smelt embryos and larvae is energy demand for compensatory processes like maintaining physiological homeostasis under temperature stress [12, 13]. For an obligate beach spawner like surf smelt, this is reason for concern. Shoreline development is increasingly removing nearshore vegetation and the shading it provides for developing surf smelt embryos, causing a significant increase in beach gravel temperature and concurrent decreases in gravel humidity [7]. A survey of modified and natural beaches in the Salish Sea found that temperatures on modified beaches were, on average, 4.7˚C higher than temperatures of natural beaches [7]. Research on the effects of temperature on surf smelt have predominantly focused on the effects of air temperature and desiccation stress on mortality and hatching in the field [7, 10]. For example, increased air temperature was linked to increased developmental rates in surf smelt embryos [7], indirectly suggesting increased yolk utilization. The effects of temperature on larval fish fitness are often amplified under coincident envi- ronmental stressors [e.g. 14–16]. One potential concomitant stressor is ocean acidification (OA). OA is a suite of chemical changes in marine carbonate parameters (e.g. pH, pCO2, [CO32]) that are driven on a global scale by the rise in total seawater carbon (CT) through dis- solution of atmospheric CO2 into seawater. Exposure of embryonic and larval fish to both tem- perature stress and OA conditions may drive reallocation of energy reserves. OA is shown to

have wide-ranging effects on marine organisms across multiple taxonomic groups [17], including on related species of forage fish [18–20]. Temperate cold-water ecosystems like the northeast Pacific Ocean are vulnerable to OA due to the ability of cold water to absorb atmo- spheric gasses more efficiently than warm water [21]. Additionally, seasonal upwelling and strong tidal mixing introduce deep waters enriched in CO2 into surface waters [22, 23], acting to exacerbate global OA processes and signals. In the Salish Sea’s urbanized Puget Sound estu- ary, where surf smelt spawning is widespread [8], observed minimum pH in surface waters varied between 7.4 and 7.7 [22], indicating pCO2 values on the order of 1000–2000 μatm. Global ocean pH values are predicted to reach about 7.7 at the end of the century under a busi- ness as usual scenario (RCP8.5) [24]. Due to the intertidal spawning behavior of surf smelt, which in some locations across the northeast Pacific Ocean occurs year-round [4], embryos are not continuously submerged during embryogenesis. Thus, the high daily and seasonal vari- ability of pCO2 and pH exposure the embryos experience may select for embryo phenotypes that are robust to variable and at times high pCO2. However, the pelagic lecithotrophic larvae PLOS ONE Surf smelt response to climate co-stressors PLOS ONE | https://doi.org/10.1371/journal.pone.0270491 June 27, 2022 2 / 14 Funding: The project described in this publication was supported by the Department of the Interior Northwest Climate Adaptation Science Center (NW

CASC- https://nwcasc.uw.edu/) through a Cooperative Agreement (G17AC000218) from the United States Geological Survey (USGS). Its contents are solely the responsibility of the authors and do not necessarily represent the views of the NW CASC or the USGS. This manuscript is submitted for publication with the understanding that the United States Government is authorized to reproduce and distribute reprints for Governmental purposes. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Award #:33491 Competing interests: The authors have declared that no competing interests exist.