Description: Rising anthropogenic CO2 in the atmosphere is accompanied by an increase in oceanic CO2 and a concomitant decline in seawater pH (ref. 1). This phenomenon, known as ocean acidification (OA), has been experimentally shown to impact the biology and ecology of numerous animals and plants2, most notably those that precipitate calcium carbonate skeletons, such as reef-building corals3. Volcanically acidified water at Maug, Commonwealth of the Northern Mariana Islands (CNMI) is equivalent to near-future predictions for what coral reef ecosystems will experience worldwide due to OA. We provide the first chemical and ecological assessment of this unique site and show that acidification-related stress significantly influences the abundance and diversity of coral reef taxa, leading to the often-predicted shift from a coral to an algae-dominated state4, 5. This study provides field evidence that acidification can lead to macroalgae dominance on reefs.

Description: While ocean acidification has different effects on herbivores and autotrophs, how acidification may influence herbivory is poorly understood. This study examined how grazing by the gastropod Lacuna vincta (hereafter Lacuna) on the macroalgae Ulva spp. (hereafter Ulva) is influenced by ocean acidification. Herbivory by Lacuna was significantly reduced under elevated partial pressure of carbon dioxide ( pCO2; 1500-2000 µatm) relative to ambient pCO2 (400 µatm). This significant decrease in herbivory was unrelated to the physiological status of Ulva but rather was specifically elicited when Lacuna was exposed to elevated pCO2 in the absence of food for 18 to 24 h prior to grazing Ulva. The negative effects of elevated pCO2 on Lacuna were absent at 400 to 800 µatm pCO2 or when fed but persisted for up to 72 h following a 24 h exposure to elevated pCO2 without food. Depressed respiration rates in Lacuna following exposure to high pCO2 without food indicated these conditions produced metabolic suppression potentially associated with acidosis. Collectively, the lasting (72 h) nature of grazing inhibition of Lacuna following brief exposure (18 h) to moderate pCO2 levels (〉1500 µatm) when food was not available suggests this process could have broad effects on the dynamics of macroalgae in estuaries where Lacuna is a dominant grazer; these effects will be amplified as climate change progresses.

Description: Acidification and deoxygenation are two consequences of climate change that also co-occur in eutrophied coastal zones and can have deleterious effects on marine life. While the effects of hypoxia on marine herbivores have been well-studied, how ocean acidification combined with hypoxia affects herbivory is poorly understood. This study examined how herbivory and survival by the gastropod Lacuna vincta grazing on the macroalgae Ulva rigida was influenced by hypoxia and ocean acidification, alone and in combination, with and without food limitation. Experiments exposed L. vincta to a range of environmentally realistic dissolved oxygen (0.7-8 mg/L) and pH (7.3-8.0 total scale) conditions for 3-72 h, with and without a starvation period and quantified herbivory and survival. While acidified conditions (pH 〈 7.4) reduced herbivory when combined with food limitation, low oxygen conditions (〈 4 mg/L) reduced herbivory and survival regardless of food supply. When L. vincta were starved and grazed in acidified conditions herbivory was additively reduced, whereas starvation and hypoxia synergistically reduced grazing rates. Overall, low oxygen had a more inhibitory effect on herbivory than low pH. Shorter exposure times (9, 6, and 3 h) were required to reduce grazing at lower DO levels (∼2.4, ∼1.6, and ∼0.7 mg/L, respectively). Herbivory ceased entirely following a three-hour exposure to DO of 0.7 mg/L suggesting that episodes of diurnal hypoxia disrupt grazing by these gastropods. The suppression of herbivory in response to acidified and hypoxic conditions could create a positive feedback loop that promotes 'green tides' whereby reduced grazing facilitates the overgrowth of macroalgae that cause nocturnal acidification and hypoxia, further disrupting herbivory and promoting the growth of macroalgae. Such feedback loops could have broad implications for estuarine ecosystems where L. vincta is a dominant macroalgal grazer and will intensify as climate change accelerates.

Description: The laminarialean kelp, Saccharina latissima, is a common macroalgae along rocky shorelines that is also frequently used in aquaculture. This study examined how ocean acidification may alter the growth of S. latissima as well as grazing on S. latissima by the gastropod, Lacuna vincta. Under elevated nutrients, S. latissima experienced significantly enhanced growth at pCO2 levels 〉1,200 µatm compared to ambient pCO2 (400 µatm). Elevated pCO2 (〉830 µatm) also significantly reduced herbivory of L. vincta grazing on S. latissima relative to ambient pCO2. There was no difference in grazing of S. latissima previously grown under elevated or ambient pCO2, suggesting lowered herbivory was due to harm to the gastropods rather than alteration of the biochemical composition of the kelp. Decreased herbivory was specifically elicited when L. vincta were exposed to elevated pCO2 in the absence of food for 〉18 h prior to grazing, with reduced grazing persisting 72 h. Elevated growth of S. latissima and reduced grazing by L. vincta at 1,200 µatm pCO2 combined to increase net growth rates of S. latissima by more than four-fold relative to ambient pCO2. L. vincta consumed 70% of daily production by S. latissima under ambient pCO2 but only 38% and 9% at 800 µatm and 1,200 µatm, respectively. Collectively, decreased grazing by L. vincta coupled with enhanced growth of S. latissima under elevated pCO2 demonstrates that increased CO2 associated with climate change and/or coastal processes will dually benefit commercially and ecologically important kelps by both promoting growth and reducing grazing pressure.

Description: Coastal ecosystems can experience acidification via upwelling, eutrophication, riverine discharge, and climate change. While the resulting increases in pCO2 can have deleterious effects on calcifying animals, this change in carbonate chemistry may benefit some marine autotrophs. Here, we report on experiments performed with North Atlantic populations of hard clams (Mercenaria mercenaria), eastern oysters (Crassostrea virginica), bay scallops (Argopecten irradians), and blue mussels (Mytilus edulis) grown with and without North Atlantic populations of the green macroalgae, Ulva. In six of seven experiments, exposure to elevated pCO2 levels (  1700 µatm) resulted in depressed shell- and/or tissue-based growth rates of bivalves compared to control conditions, whereas rates were significantly higher in the presence of Ulva in all experiments. In many cases, the co-exposure to elevated pCO2 levels and Ulva had an antagonistic effect on bivalve growth rates whereby the presence of Ulva under elevated pCO2 levels significantly improved their performance compared to the acidification-only treatment. Saturation states for calcium carbonate (Ω) were significantly higher in the presence of Ulva under both ambient and elevated CO2 delivery rates, and growth rates of bivalves were significantly correlated with Omega in six of seven experiments. Collectively, the results suggest that photosynthesis and/or nitrate assimilation by Ulva increased alkalinity, fostering a carbonate chemistry regime more suitable for optimal growth of calcifying bivalves. This suggests that large natural and/or aquacultured collections of macroalgae in acidified environments could serve as a refuge for calcifying animals that may otherwise be negatively impacted by elevated pCO2 levels and depressed Omega.

Description: Coastal ecosystems are prone to multiple anthropogenic and natural stressors including eutrophication, acidification, and invasive species. While the growth of some macroalgae can be promoted by excessive nutrient loading and/or elevated pCO2, responses differ among species and ecosystems. Native to the western Pacific Ocean, the filamentous, turf-forming rhodophyte, Dasysiphonia japonica, appeared in estuaries of the northeastern Atlantic Ocean during the 1980s and the northwestern Atlantic Ocean during the late 2000s. Here, we report on the southernmost expansion of the D. japonica in North America and the effects of elevated nutrients and elevated pCO2 on the growth of D. japonica over an annual cycle in Long Island, New York, USA. Growth limitation of the macroalga varied seasonally. During winter and spring, when water temperatures were 〈 15 °C, growth was significantly enhanced by elevated pCO2 (p 〈 0.05). During summer and fall, when the water temperature was 15–24 °C, growth was significantly higher under elevated nutrient treatments (p 〈 0.05). When temperatures reached 28 °C, the macroalga grew poorly and was unaffected by nutrients or pCO2. The delta 13C content of regional populations of D. japonica was −30 per mil, indicating the macroalga is an obligate CO2-user. This result, coupled with significantly increased growth under elevated pCO2 when temperatures were 〈 15 °C, indicates this macroalga is carbon-limited during colder months, when in situ pCO2 was significantly lower in Long Island estuaries compared to warmer months when estuaries are enriched in metabolically derived CO2. The delta 15N content of this macroalga (9 per mil) indicated it utilized wastewater-derived N and its N limitation during warmer months coincided with lower concentrations of dissolved inorganic N in the water column. Given the stimulatory effect of nutrients on this macroalga and that eutrophication can promote seasonally elevated pCO2, this study suggests that eutrophic estuaries subject to peak annual temperatures 〈 28 °C may be particularly vulnerable to future invasions of D. japonica as ocean acidification intensifies. Conversely, nutrient reductions would serve as a management approach that would make coastal regions more resilient to invasions by this macroalga.

Description: Coastal zones can be focal points of acidification where the influx of atmospheric CO2 can be compounded by additional sources of acidity that may collectively impair calcifying organisms. While the photosynthetic action of macrophytes may buffer against coastal ocean acidification, such activity has not been well-studied, particularly among aquacultured seaweeds. Here, we report on field and laboratory experiments performed with North Atlantic populations of juvenile hard clams (Mercenaria mercenaria), eastern oysters (Crassostrea virginica), and blue mussels (Mytilus edulis) grown with and without increased CO2 and with and without North Atlantic kelp (Saccharina latissima) over a range of aquaculture densities (0.3 – 2 g/L). In all laboratory experiments, exposure to elevated pCO2 (〉1,800 µatm) resulted in significantly reduced shell- and/or tissue-based growth rates of bivalves relative to control conditions. This impairment was fully mitigated when bivalves were exposed to the same acidification source but also co-cultured with kelp. Saturation states of aragonite were transformed from undersaturated to saturated in the acidification treatments with kelp present, while the acidification treatments remained undersaturated. In a field experiment, oysters grown near aquacultured kelp were exposed to higher pH waters and experienced significantly faster shell and tissue based growth rates compared to individuals grown at sites away from kelp. Collectively, these results suggest that photosynthesis by S. latissima grown at densities associated with aquaculture increased pH and decreased pCO2, fostering a carbonate chemistry regime that maximized the growth of juvenile bivalves. As S. latissima has been shown to benefit from increased CO2, growing bivalves and kelp together under current or future acidification scenarios may be a synergistically beneficial integrated, multi-trophic aquaculture approach.

Description: This study reports on experiments performed with a Northwest Atlantic species of the macroalgae, Ulva, and the seagrass, Zostera marina, grown under ambient and elevated levels of pCO2, and subjected to competition with each other. When grown individually, elevated pCO2 significantly increased growth rates and productivity of Ulva and Zostera, respectively, beyond control treatments (by threefold and 27%, respectively). For both primary producers, significant declines in tissue δ13C signatures suggested that increased growth and productivity were associated with a shift from use of HCO3− toward CO2 use. When grown under higher pCO2, Zostera experienced significant increases in leaf and rhizome carbon content as well as significant increases in leaf carbon-to-nitrogen ratios, while sediments within which high CO2 Zostera were grown had a significantly higher organic carbon content. When grown in the presence of Ulva; however, above- and below-ground productivity and tissue nitrogen content of Zostera were significantly lower, revealing an antagonistic interaction between elevated CO2 and the presence of Ulva. The presence of Zostera had no significant effect on the growth of Ulva. Collectively, this study demonstrates that while Ulva and Zostera can each individually benefit from elevated pCO2 levels, the ability of Ulva to grow more rapidly and inhibit seagrass productivity under elevated pCO2, coupled with accumulation of organic C in sediments, may offset the potential benefits for Zostera within high CO2 environments.