Metabolic impacts of climate change on marine ecosystems: Implications for fish communities and fisheries

Aim:Climate change will reshape marine ecosystems over the 21st century through diverse and complex mechanisms that are difficult to assess quantitatively. Here, we characterize expectations for how marine community biomass will respond to the energetic consequences of changes in primary production and temperature-dependent metabolic rates, under a range of fishing/conservation scenarios. Location: Global ocean. Time period: 1950-2100.Major taxa studied: Commercially harvested marine ectotherms ('fish'). Methods: We use a size-structured macroecological model of the marine ecosystem, coupled with a catch model that allows for calibration with global historical data and simulation of fishing. We examine the four energetic mechanisms that, within the model framework, determine the community response to climate change: net primary production, phytoplankton cell size, and the temperature dependencies of growth and natural mortality. Results: Climate change decreases the modelled global fish community biomass by as much as 30% by 2100. This results from a diminished energy supply to upper trophic levels as photosynthesis becomes more nutrient limited and phytoplankton cells shrink, and from a temperature-driven increase of natural mortality that, together, overwhelm the effect of accelerated somatic growth rates. Ocean circulation changes drive regional variations of primary production, producing patterns of winners and losers that largely compensate each other when averaged globally, whereas decreasing phytoplankton size drives weaker but more uniformly negative changes. The climate impacts are similar across the range of conservation scenarios but are slightly amplified in the strong conservation scenarios owing to the greater role of natural mortality. Main conclusions: The spatial pattern of climate impacts is mostly determined by changes in primary production. The overall decline of community biomass is attributed to a temperature-driven increase of natural mortality, alongside an overall decrease in phytoplankton size, despite faster somatic growth. Our results highlight the importance of the competition between accelerated growth and mortality in a warming ocean.


Introduction 72
Energy is supplied at the base of the marine ecosystem by Net Primary Produc-73 tion (NPP), generally thought to be dependent on water temperature, sunlight, and 74 the availability of nutrient elements at the ocean surface (Moore et al., 2013). This 75 energy, embodied as organic matter, is then transferred to marine heterotrophic or-76 ganisms, which span many orders of magnitude in size, through feeding relationships. 77 At each trophic step in the ecosystem, some portion of the biomass-energy is used ) and is commonly expected to produce more rapid growth alongside more rapid 111 respiration, activity, and predation (Pepin, 1991). Different species react differently 112 to changes in temperature, a process that can further depend on other physiological,  The wild-capture fishery offers a perspective on the global marine ecosystem that 117 can help resolve these questions, while simultaneously playing a major role as the filter requires a framework that can simultaneously take into account both the natural 130 ecosystem dynamics and the behaviour of fishers. At the same time, fisheries reshape 131 the ecosystem directly in a way that will interact with future climate change.

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Here we apply a number of macroecological principles with broad empirical sup-133 port to better understand some of the interactive impacts that climate change and 134 fishing activities could have on marine ecosystems. Specifically, we present a first-135 order assessment of how changes in water temperature and NPP could affect the 136 global marine fish community through ecosystem metabolism, considering multiple 137 future fisheries regulation scenarios. We use BOATS, a bioenergetically-constrained  The model does not explicitly resolve individual species, which are certain to migrate 142 7 and evolve as conditions change (Sunday et al., 2012). Instead, the model implicitly 143 assumes that, on a multi-decadal timescale, migration and evolution will adjust local 144 ecosystems to result in a stationary relationship with a given set of environmental 145 conditions. In other words, the model assumes that as environmental conditions 146 shift, the ecosystem shifts along with them, which is likely to be an optimistic as-147 sumption. Nor do we resolve changes in species assemblage, which are likely to be    Information Appendix S1 provides a descriptive example for the use of the BOATS.

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BOATS is designed to run on a 2-dimensional horizontal grid of the ocean, and In BOATS, the total energy input to growth (somatic and reproductive) of an 185 9 individual fish is determined by the local primary production and ecosystem trophic 186 transfer efficiency, to an upper limit that is the maximum rate at which a well-fed 187 fish can grow (von Bertalanffy, 1949; Andersen and Beyer, 2015). Water tempera-188 ture modifies the upper limit growth rate through a van't Hoff-Arrhenius tempera-189 ture dependence, which is parameterised with a representative activation energy of  The trophic transfer of NPP to fish depends on the size structure of phytoplank-197 ton, which we estimate using the empirical algorithm of Dunne et al. (2005). This 198 algorithm predicts the fraction of primary production that is generated by large phy-199 toplankton in each grid cell from the in situ NPP and water temperature. We employ 200 this large fraction to estimate the average phytoplankton size. The trophic level of a 201 fish of a given size is then calculated from the mass ratio of that fish to the average 202 phytoplankton, and using an average predator-to-prey mass ratio for the community.

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The fraction of NPP that can be taken up by fish of a given size is then given by its 204 trophic level and the average trophic efficiency. This simple approach captures the 205 basic size-dependence of energy distribution within the community, while avoiding 206 the complexity of explicit feeding relationships. Implicitly, it assumes that most fish 207 are opportunistic feeders, and that variations in predator-to-prey mass ratios tend 208 to be approximately compensated by opposing changes in trophic efficiency, leading 209 to constant efficiencies of total energy transfer to fish of a given size.

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To represent natural mortality, defined here as all non-harvesting sources of fish 211 mortality and including losses to predation, parasitism, disease, old age, and star- to an Open Access dynamic. Using one of these two general frameworks for the 226 fishing rate, we consider four fishing scenarios that are described further below and 227 summarized in Table 1.        Simulation design 306 We force the six optimal model ensemble members described above with net pri-307 mary production and temperature output from the Institut Pierre Simon Laplace    The pattern of net change closely resembles the responses driven by primary 386 production (simulation NPP, Figure 5b), and to a lesser extent by phytoplankton 387 size structure (PhytoSize, Figure 5c). However, the latter are generally shifted to-388 ward more negative values due to the effect of warming, which tends to decrease 389 phytoplankton size everywhere. Thus, whereas NPP changes result in regional pat-390 terns that largely cancel each other out, phytoplankton size changes produce weaker 391 18 regional contrasts but a more significant negative global impact.

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The uniquely temperature-dependent impacts on growth and mortality (simula-393 tions TempGrowth and TempMortality, Figure 5d,e) are more spatially homogeneous 394 than those driven by net primary production, due to the homogeneous distribution of 395 warming ( Figure 2) and have opposite and nearly compensating effects on biomass.

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The activation energy of mortality is more sensitive to temperature than that of importance of growth when fish populations are greatly impoverished. 415 We find significant regional variability in the impacts of climate change, mostly 416 driven by the spatial patterns of NPP changes simulated by the Earth System Model. In addition, as fishing becomes a major loss term for biomass, it reduces the 462 impact of natural mortality relative to the case without harvest. Instead, the impor-463 tance shifts to the rate at which fish can grow from juveniles to adulthood, which 464 limits the replacement rate of harvested fish. As a result, the positive impact of 465 warmer temperatures on growth rates becomes increasingly significant as fishing in-466 tensifies, counterbalancing the negative impacts of NPP and natural mortality.

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The real world outcomes would undoubtedly be more nuanced than in this simple In summary, our model predicts that climate change will reduce the total supply 504 of energy to upper trophic levels, and will accelerate the rate at which energy flows