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  1. Free, publicly-accessible full text available July 1, 2024
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  4. Abstract Background Climate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to the ecosystem level. While mixotrophic phytoplankton, organisms that combine photosynthesis and heterotrophy to meet their energetic and nutritional needs, are expected to become more heterotrophic with warmer temperatures due to heterotrophy increasing at a faster rate than photosynthesis, it is unclear how evolution will influence how these organisms respond to warmer temperatures. In this study, we used adaptive dynamics to model the consequences of temperature-mediated increases in metabolic rates for the evolution of mixotrophic phytoplankton, focusing specifically on phagotrophic mixotrophs. Results We find that mixotrophs tend to evolve to become more reliant on phagotrophy as temperatures rise, leading to reduced prey abundance through higher grazing rates. However, if prey abundance becomes too low, evolution favors greater reliance on photosynthesis. These responses depend upon the trade-off that mixotrophs experience between investing in photosynthesis and phagotrophy. Mixotrophs with a convex trade-off maintain mixotrophy over the greatest range of temperatures; evolution in these “generalist” mixotrophs was found to exacerbate carbon cycle impacts, with evolving mixotrophs exhibiting increased sensitivity to rising temperature. Conclusions Our results show that mixotrophs may respond more strongly to climate change than predicted by phenotypic plasticity alone due to evolutionary shifts in metabolic investment. However, the type of metabolic trade-off experienced by mixotrophs as well as ecological feedback on prey abundance may ultimately limit the extent of evolutionary change along the heterotrophy-phototrophy spectrum. 
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  5. Abstract

    Mounting evidence suggests that fishing can be a major driver of coral‐to‐macroalgae regime shifts on tropical reefs. In many small‐scale coral reef fisheries, fishers target herbivorous fishes, which can weaken coral resilience via reduced herbivory on macroalgae that then outcompete corals. Previous models that explored the effects of harvesting herbivores revealed hysteresis in the herbivory–benthic state relationship that results in bistability of coral‐ and macroalgae‐dominated states over some levels of fishing pressure, which has been supported by empirical evidence. However, past models have not accounted for the functional differences among herbivores or how fisher selectivity for different herbivore functional groups may alter the benthic dynamics and resilience. Here, we use a dynamic model that links differential fishing on two key herbivore functional groups to the outcome of competitive dynamics between coral and macroalgae. We show that reef state depends not only on the level of fishing but also on the types of herbivores targeted by fishers. Selectively fishing browsing herbivores that are capable of consuming mature macroalgae (e.g., unicornfish) increases precariousness of the coral state by moving the system close to the coral‐to‐macroalgae tipping point. By contrast, selectively harvesting grazing herbivores that are only capable of preventing macroalgae from becoming established (e.g., parrotfishes) can increase catch yields substantially more before the tipping point is reached. However, this lower precariousness with increasing fishing effort comes at the cost of increasing the range of fishing effort over which coral and macroalgae are bistable; increasing hysteresis makes a regime shift triggered by a disturbance more difficult or impractical to reverse. Our results suggest that management strategies for small‐scale coral reef fisheries should consider how functional differences among harvested herbivores coupled with fisher selectivity influence benthic dynamics in light of the trade‐off between tipping point precariousness and coral recovery dynamics following large disturbances.

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  6. Abstract Mixotrophs, organisms that combine photosynthesis and heterotrophy to gain energy, play an important role in global biogeochemical cycles. Metabolic theory predicts that mixotrophs will become more heterotrophic with rising temperatures, potentially creating a positive feedback loop that accelerates carbon dioxide accumulation in the atmosphere. Studies testing this theory have focused on phenotypically plastic (short‐term, non‐evolutionary) thermal responses of mixotrophs. However, as small organisms with short generation times and large population sizes, mixotrophs may rapidly evolve in response to climate change. Here, we present data from a 3‐year experiment quantifying the evolutionary response of two mixotrophic nanoflagellates to temperature. We found evidence for adaptive evolution (increased growth rates in evolved relative to acclimated lineages) in the obligately phototrophic strain, but not in the facultative phototroph. All lineages showed trends of increased carbon use efficiency, flattening of thermal reaction norms, and a return to homeostatic gene expression. Generally, mixotrophs evolved reduced photosynthesis and higher grazing with increased temperatures, suggesting that evolution may act to exacerbate mixotrophs' effects on global carbon cycling. 
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  7. Abstract Acquired phototrophs, organisms that obtain their photosynthetic abilities by hosting endosymbionts or stealing plastids from their prey, are omnipresent in aquatic ecosystems. This acquisition of photosynthetic metabolism allows for niche expansion, and can therefore influence competition outcomes by alleviating competition for shared resources. Here, we test how acquired metabolism alters competitive outcomes by manipulating light availability to control the energetic contribution of photosynthesis to acquired phototrophs. Using freshwater protists that compete for bacterial prey, we demonstrate light‐dependent competition outcomes of acquired phototrophs ( Paramecium bursaria ) and strict heterotrophs ( Colpidium sp.) in laboratory model experiments. We then synthesize these findings using a series of mathematical models, and show that explicitly accounting for resource competition improves model fits. Both empirical and mathematical models predict that the acquired phototroph should increase in competitive dominance with increasing light availability. Our results highlight the importance of acquired metabolism to community dynamics, highlighting the need for more empirical and theoretical studies of this mechanism for niche expansion. 
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  8. Abstract

    Mixotrophs are ubiquitous and integral to microbial food webs, but their impacts on the dynamics and functioning of broader ecosystems are largely unresolved.

    Here, we show that mixotrophy produces a unique type of food web module that exhibits unusual ecological dynamics, with surprising consequences for carbon flux under warming. We develop a generalizable model of a mixotrophic food web module that incorporates dynamic switching between phototrophy and phagotrophy to assess ecological dynamics and total system CO2flux.

    We find that warming switches mixotrophic systems between alternative stable carbon states—including a phototrophy‐dominant carbon sink state, a phagotrophy‐dominant carbon source state and cycling between these two. Moreover, warming always shifts this mixotrophic system from a carbon sink state to a carbon source state, but a coordinated increase in nutrients can erase early warning signals of this transition and expand hysteresis.

    This suggests that mixotrophs can generate critical carbon tipping points under warming that will be more abrupt and less reversible when combined with increased nutrient levels, having widespread implications for ecosystem functioning in the face of rapid global change.

    Read the freePlain Language Summaryfor this article on the Journal blog.

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  9. Abstract

    Phago-mixotrophy, the combination of photoautotrophy and phagotrophy in mixoplankton, organisms that can combine both trophic strategies, have gained increasing attention over the past decade. It is now recognized that a substantial number of protistan plankton species engage in phago-mixotrophy to obtain nutrients for growth and reproduction under a range of environmental conditions. Unfortunately, our current understanding of mixoplankton in aquatic systems significantly lags behind our understanding of zooplankton and phytoplankton, limiting our ability to fully comprehend the role of mixoplankton (and phago-mixotrophy) in the plankton food web and biogeochemical cycling. Here, we put forward five research directions that we believe will lead to major advancement in the field: (i) evolution: understanding mixotrophy in the context of the evolutionary transition from phagotrophy to photoautotrophy; (ii) traits and trade-offs: identifying the key traits and trade-offs constraining mixotrophic metabolisms; (iii) biogeography: large-scale patterns of mixoplankton distribution; (iv) biogeochemistry and trophic transfer: understanding mixoplankton as conduits of nutrients and energy; and (v) in situ methods: improving the identification of in situ mixoplankton and their phago-mixotrophic activity.

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