Good tidings for red tides? Responses of toxic and calcareous dinoflagellates to global change

Abstract

Atmospheric CO2 partial pressure (pCO2) rises at a yet unprecedented rate, which enhances the uptake of CO2 by the surface ocean and concomitantly lowers the pH. Due to the latter, these changes are often referred to as "ocean acidification" (OA). In the last decades, consequences of OA on marine phytoplankton have been intensively studied from cellular to ecosystem level. These investigations have, however, largely focused on coccolithophores, diatoms and cyanobacteria. Little is known about the responses of dinoflagellates to OA, even though they represent an important component of phytoplankton assemblages. Moreover, owing to their type II RubisCO, a carboxylating enzyme with very low affinities for its substrate CO2, dinoflagellates may be particularly sensitive to changes in CO2 concentrations. In my first publication, I therefore investigated the impact of OA on two dinoflagellate species, the calcareous Scrippsiella trochoidea and the paralytic shellfish poisoning (PSP) toxin producing Alexandrium fundyense (previously A. tamarense). The results show that, besides species-specific differences, growth characteristics remained largely unaltered with rising pCO2 (Publication I). To understand these responses, several aspects of inorganic carbon (Ci) acquisition were investigated, revealing effective yet differently expressed carbon concentrating mechanisms (CCMs). These CCMs were moreover adjusted to the respective CO2 environment, which enabled both species to keep their growth rates relatively unaffected over a broad range of pCO2. In addition to OA, rising CO2 causes global warming, which in turn will lead to a rise in sea surface temperatures. Consequences will be an enhanced thermal stratification and a lowered nutrient resupply from nutrient-rich deep waters. Nutrient limitation may alter the response of dinoflagellates towards elevated pCO2. In Publication II, I therefore investigated the effects of rising CO2 and nitrogen (N) limitation on S. trochoidea and A. fundyense. The findings indicate a close coupling between C and N assimilation and showed a CO2-dependent increase in N assimilation in both species. Although N-rich compounds per cell were highest at high pCO2, this came at the expense of higher N requirements and lower N affinities, which will reduce the competitive ability of both species that potentially translate to changes in the phytoplankton community composition in a future ocean. To test the effect of OA on the productivity of phytoplankton in a natural community, a five months mesocosm study was conducted at the coast of the Swedish North Sea (Publication III). Besides early spring blooms of diatoms, dinoflagellate blooms often occur in these waters in late summer. During the experimental phase from March until July, we observed two major phytoplankton bloom events, which were both dominated by diatoms. Dinoflagellates usually overwinter as resting cysts in the sediment and as the applied mesocosms were closed in early spring, the initial inoculum of dinoflagellates was low. Weekly attempts to introduce seed populations of dinoflagellates to the mesocosms were not effective enough for species to subsist in these systems. Concerning the overall phytoplankton community, impacts of OA on primary production were generally small, though total primary production increased during the second phytoplankton bloom when nutrients were depleted to very low concentrations. In conclusion, OA seems to have an effect on the photosynthetic activity of marine dinoflagellates, and furthermore cause changes in various physiological processes also related to nutrient acquisition. Even though these changes may appear a smalla , at least when compared to OA-responses of other taxa, they can nonetheless influence the competitive abilities of species, especially when being exposed to nutrient limitation. On an ecosystem level, OA therefore has the potential to stimulate primary production and alter the phytoplankton community structure in coastal waters, especially at times when the availability of nutrients is limited.