Coastal ocean acidification and nitrogen loading facilitate invasions of the non-indigenous red macroalga, Dasysiphonia japonica

Abstract

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 δ13C content of regional populations of D. japonica was −30‰, 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 δ15N content of this macroalga (9‰) 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.

Inhibition of harmful algal blooms caused by Aureococcus anophagefferens (Pelagophyceae) using native (Gracilaria tikvahiae) and invasive (Dasysiphonia japonica) red seaweeds from North America

“…anophagefferens action. Our results suggest that the recent invasion of D. japonica in NY estuaries (Young and Gobler 2021), especially in Great South Bay, may be influencing the patterns of brown tide occurrence, potentially causing shorter and less intense blooms. Finally, the strategic deployment of G. tikvahiae as an element of open-water coastal aquaculture systems may be an environmentally friendly and revenue-generating option for preventing and/or controlling blooms caused by A. anophagefferens and likely other harmful algae.…”

“…This picoplankton achieves high densities within the open waters of estuaries, but its cell concentrations decline by orders of magnitudes in shallow tributaries where salinities are not significantly different from neighboring, open estuarine sites (SCDHS 1990(SCDHS -2020; a major difference between these environments is the presence of much higher densities of seaweeds in the tributaries (Tang and Gobler 2011). In addition, D. japonica has recently invaded the same south shore lagoons that host brown tides cause by A. anophagefferens (Young and Gobler 2021), and since this invasion has been documented (2018), brown tides in these lagoons have been less intense (10 5 cells mL −1 vs. 10 6 cells mL −1 ) and shorter in duration (weeks vs. months) compared to before the invasion (SCDHS 1990(SCDHS -2020. As such, it is possible that macroalgae influence the occurrence of brown tides in NY estuaries.…”

“…In addition to G. tikvahiae, Dasysiphonia japonica is a rhodophyte native to the western Pacific Ocean that invaded European waters in 1984 (Sjøtun et al 2008) and has since spread to the western Atlantic Ocean, being first documented in the waters around Rhode Island in 2007 (Schneider 2010). Dasysiphonia japonica experiences enhanced growth compared to other red macroalgae when exposed to elevated pCO 2 and nutrient levels, which may allow it to outcompete other algae in eutrophic estuaries (Young and Gobler 2021). The potential effects of D. japonica on HAB phytoplankton, including A. anophagefferens, have never been investigated.…”

Review of Harmful Algal Blooms (HABs) Causing Marine Fish Kills: Toxicity and Mitigation

“…For instance, it has been confirmed that some species of Gracilaria native to Asian seas limit the formation of numerous HABs by allelopathy [186,188,189]. Dasysiphonia japonica grows faster than other red macroalgae, which helps it compete with other types of algae in nutrient-rich estuaries [190]. No research has been conducted on the possible impacts of D. japonica on HABs phytoplankton, including A. anophagefferens [191].…”