Simulating Effects of Variable Stoichiometry and Temperature on Mixotrophy in the Harmful Dinoflagellate Karlodinium veneficum

Abstract

Results from a dynamic mathematical model are presented simulating the growth of the harmful algal bloom (HAB) mixotrophic dinoflagellate Karlodinium veneficum and its algal prey, Rhodomonas salina. The model describes carbon-nitrogen-phosphorus-based interactions within the mixotroph, interlinking autotrophic and phagotrophic nutrition. The model was tuned to experimental data from these species grown under autotrophic conditions and in mixed batch cultures in which nitrogen:phosphorus stoichiometry (input molar N:P of 4, 16, and 32) of both predator and prey varied. A good fit was attained to all experimentally derived carbon biomass data. The potential effects of temperature and nutrient changes on promoting growth of prey and thus K. veneficum bloom formation were explored using this simulation platform. The simulated biomass of K. veneficum was highest when they were functioning as mixotrophs and when they consumed prey under elevated N:P conditions. The scenarios under low N:P responded differently, with simulations showing larger deviation between mixotrophic and autotrophic growth, depending on temperature. When inorganic nutrients were in balanced proportions, lower biomass of the mixotroph was attained at all temperatures in the simulations, suggesting that natural systems might be more resilient against Karlodinium HAB development in warming conditions if nutrients were available in balanced proportions. These simulations underscore the need for models of HAB dynamics to include consideration of prey; modeling HAB as autotrophs is insufficient. The simulations also imply that warmer, wetter springs that may bring more N with lower N:P, such as predicted under climate change scenarios for Chesapeake Bay, may be more conducive to development of these HABs. Prey availability may also increase with temperature due to differential growth temperature responses of K. veneficum and its prey.

Differences in physiology explain succession of mixoplankton functional types and affect carbon fluxes in temperate seas

“…Our simulated values are within the range of values observed in the literature; however, these studies are speciesspecific and are based upon experimental conditions which differ among studies (e.g., temperature, light, nutrient, and prey conditions). Considering the diverse mixotrophic strategies adopted by protists, including within functional types (Table S8), further studies are necessary to estimate not only carbon but also nitrogen and phosphorus budgets (Carvalho and Granéli, 2010;Lin et al, 2018). These studies will require plankton ecologists to develop new methodologies, which will potentially involve the combination of different techniques, to quantify mixoplanktonic activity both under controlled conditions in the laboratory and within natural assemblages in the field (Worden et al, 2015;Beisner et al, 2019;Flynn et al, 2019).…”

Assessing risks and mitigating impacts of harmful algal blooms on mariculture and marine fisheries

“…However, the effects of nutrient inputs may be confounded by many other factors, including natural occurrence of HABs, transport of HAB species via mariculture and other marine activities, variable meteorological forcing, and longer-term climate change (Callaway et al 2012;Gowen et al 2012). There is increasing evidence that many HAB species can use dissolved and particulate organic forms of N and P (through prey ingestion), in addition to autotrophy; this combination of trophic modes is termed mixotrophy (Burkholder 1998;Anderson et al 2002;Lin et al 2018). Mixotrophic HAB species are therefore able to proliferate both under high organic N concentrations and by engulfing prey under nutrient limited conditions.…”

Microzooplankton Communities in a Changing Ocean: A Risk Assessment

“…These authors reported that heterotrophy increased more strongly with temperature than phototrophy, suggesting that, under a future scenario of ocean warming, mixotrophic organisms may rely more on heterotrophy to sustain growth [47,149,150]. Likewise, the modelled mixotrophic maximum growth rate of Karlodinium veneficum exceeded that of its heterotrophic form while warming was predicted to enhance mixotrophic over heterotrophic growth only under nutrient-limiting conditions [86]. In such cases, future warming may increase the grazing pressure on phototrophic communities and even constrain the magnitude of algal blooms.…”

“…A mesocosm study revealed that the addition of nitrogen and glucose produced little effects on microzooplankton abundance and compositions and that nutrient effects were overridden by a high diversity of both protistan and metazoan grazers [241]. Likewise, experimental [242] and modelling [86] approaches revealed that, under nutrient starvation, heterotrophy in primarily phototrophic dinoflagellates is stimulated.…”