Abstract

While there is growing interest in understanding how marine life will respond to future ocean acidification, many coastal ecosystems currently experience intense acidification in response to upwelling, eutrophication, or riverine discharge. Such acidification can be inhibitory to calcifying animals, but less is known regarding how non-calcifying macroalgae may respond to elevated CO2. Here, we report on experiments performed during summer through fall with North Atlantic populations of Gracilaria and Ulva that were grown in situ within a mesotrophic estuary (Shinnecock Bay, NY, USA) or exposed to normal and elevated, but environmentally realistic, levels of pCO2 and/or nutrients (nitrogen and phosphorus). In nearly all experiments, the growth rates of Gracilaria were significantly increased by an average of 70% beyond in situ and control conditions when exposed to elevated levels of pCO2 (p<0.05), but were unaffected by nutrient enrichment. In contrast, the growth response of Ulva was more complex as this alga experienced significantly (p<0.05) increased growth rates in response to both elevated pCO2 and elevated nutrients and, in two cases, pCO2 and nutrients interacted to provide a synergistically enhanced growth rate for Ulva. Across all experiments, elevated pCO2 significantly increased Ulva growth rates by 30% (p<0.05), while the response to nutrients was smaller (p>0.05). The δ13C content of both Gracilaria and Ulva decreased two-to-three fold when grown under elevated pCO2 (p<0.001) and mixing models demonstrated these macroalgae experienced a physiological shift from near exclusive use of HCO3- to primarily CO2 use when exposed to elevated pCO2. This shift in carbon use coupled with significantly increased growth in response to elevated pCO2 suggests that photosynthesis of these algae was limited by their inorganic carbon supply. Given that eutrophication can yield elevated levels of pCO2, this study suggests that the overgrowth of macroalgae in eutrophic estuaries can be directly promoted by acidification, a process that will intensify in the coming decades.

Highlights

  • Ocean acidification is changing the chemistry of the ocean

  • Given that eutrophication can yield elevated levels of pCO2, this study suggests that the overgrowth of macroalgae in eutrophic estuaries can be directly promoted by acidification, a process that will intensify in the coming decades

  • C4 plants that utilize phosphenolpyruvate carboxylase (PEPC) experience little photorespiratory loss due to use of carbon concentrating mechanisms (CCM) and may not benefit from increased CO2 since PEPC is substrate-saturated at current CO2 levels [1, 7]

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Summary

Introduction

Ocean acidification is changing the chemistry of the ocean. Beyond reducing pH, the anthropogenic delivery of CO2 into surface oceans this century will differentially effect various pools of PLOS ONE | DOI:10.1371/journal.pone.0155152 May 13, 2016inorganic carbon, with CO2 and HCO3- expected to increase 260% and 20%, respectively, and CO32- levels expected to decrease 60% [1]. The extent to which uncalcified marine macroalgae benefit from anthropogenically-induced changes in carbonate chemistry is complex and not fully understood. C3 plants that utilize RuBisCO as their initial carboxylating enzyme experience loss of fixed carbon due to photorespiration and may benefit from increased CO2 concentrations since RuBisCO is not substrate-saturated at current CO2 levels [1, 7]. C4 plants that utilize phosphenolpyruvate carboxylase (PEPC) experience little photorespiratory loss due to use of carbon concentrating mechanisms (CCM) and may not benefit from increased CO2 since PEPC is substrate-saturated at current CO2 levels [1, 7]. Webber et al [11] and Roger et al [12] found that acclimation to elevated CO2 can result in decreased concentrations of RuBisCO, but results in an increase in soluble carbohydrate content that could enhance growth rates and alter the total carbon content of algal tissues

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