Ocean acidification and the loss of phenolic substances in marine plants.

Thomas Arnold,Christopher Mealey,Kelly Maers,Hannah Leahey,A Whitman Miller,Jason M Hall-Spencer,Marco Milazzo,Richard K.F Unsworth

doi:10.1371/journal.pone.0035107

Thomas Arnold, Christopher Mealey + Show 6 more

Open Access

https://doi.org/10.1371/journal.pone.0035107

Copy DOI

Abstract

Rising atmospheric CO2 often triggers the production of plant phenolics, including many that serve as herbivore deterrents, digestion reducers, antimicrobials, or ultraviolet sunscreens. Such responses are predicted by popular models of plant defense, especially resource availability models which link carbon availability to phenolic biosynthesis. CO2 availability is also increasing in the oceans, where anthropogenic emissions cause ocean acidification, decreasing seawater pH and shifting the carbonate system towards further CO2 enrichment. Such conditions tend to increase seagrass productivity but may also increase rates of grazing on these marine plants. Here we show that high CO2 / low pH conditions of OA decrease, rather than increase, concentrations of phenolic protective substances in seagrasses and eurysaline marine plants. We observed a loss of simple and polymeric phenolics in the seagrass Cymodocea nodosa near a volcanic CO2 vent on the Island of Vulcano, Italy, where pH values decreased from 8.1 to 7.3 and pCO2 concentrations increased ten-fold. We observed similar responses in two estuarine species, Ruppia maritima and Potamogeton perfoliatus, in in situ Free-Ocean-Carbon-Enrichment experiments conducted in tributaries of the Chesapeake Bay, USA. These responses are strikingly different than those exhibited by terrestrial plants. The loss of phenolic substances may explain the higher-than-usual rates of grazing observed near undersea CO2 vents and suggests that ocean acidification may alter coastal carbon fluxes by affecting rates of decomposition, grazing, and disease. Our observations temper recent predictions that seagrasses would necessarily be “winners” in a high CO2 world.

Highlights

Increasing levels of atmospheric CO2 can trigger accumulations of plant phenolic substances such as lignins, tannins, and phenolic acids and glycosides which serve as structural or chemical defenses against grazers and disease organisms [1,2,3,4,5,6]
P values between 0.05 and 0.10 are noted in the tables. In these natural and manipulative experiments, we observed that high CO2/low pH conditions were associated with a dramatic loss, rather than the predicted accumulations, of tannins and related phenolics in undersea vegetation
In the Mediterranean, we found that levels of phenolic substances were significantly decreased in Cymodocea nodosa near CO2 vents on the island of Vulcano, Italy (Table 1)

Summary

Introduction

Increasing levels of atmospheric CO2 can trigger accumulations of plant phenolic substances such as lignins, tannins, and phenolic acids and glycosides which serve as structural or chemical defenses against grazers and disease organisms [1,2,3,4,5,6]. Acidification occurs in estuaries where trends of decreasing pH have been detected amid the daily fluctuations driven by biological processes and tides [13,14]. Such high CO2 / low pH conditions can stimulate the productivity of many marine photoautotrophs, including seagrasses which lack effective carbon-concentrating mechanisms [15,16,17,18,19,20]. Studies of high CO2 communities near submerged volcanic vents reveal luxurious seagrass beds with increased shoot densities and biomass, and leaves devoid of calcifying fouling organisms [22,23,24]

Methods

Results

Conclusion