Competition for nutrients and light: testing advances in resource competition with a natural phytoplankton community.

A key challenge in ecology is to understand how nutrients and light affect the biodiversity and community structure of phytoplankton and plant communities. According to resource competition models, ratios of limiting nutrients are major determinants of species composition. At high nutrient levels, however, species interactions may shift to competition for light, which might make nutrient ratios less relevant. The "nutrient-load hypothesis" merges these two perspectives, by extending the classic model of competition for two nutrients to include competition for light. Here, we test five key predictions of the nutrient-load hypothesis using multispecies competition experiments. A marine phytoplankton community sampled from the North Sea was inoculated in laboratory chemostats provided with different nitrogen (N) and phosphorus (P) loads to induce either single resource limitation or co-limitation of N, P, and light. Four of the five predictions were validated by the experiments. In particular, different resource limitations favored the dominance of different species. Increasing nutrient loads caused changes in phytoplankton species composition, even if the N:P ratio of the nutrient loads remained constant, by shifting the species interactions from competition for nutrients to competition for light. In all treatments, small species became dominant whereas larger species were competitively excluded, supporting the common view that small cell size provides a competitive advantage under resource-limited conditions. Contrary to expectation, all treatments led to coexistence of diatoms, cyanobacteria and green algae, resulting in a higher diversity of species than predicted by theory. Because the coexisting species comprised three phyla with different photosynthetic pigments, we speculate that niche differentiation in the light spectrum might play a role. Our results show that mechanistic resource competition models that integrate nutrient-based and light-based approaches provide an important step forward to understand and predict how changing nutrient loads affect community composition.

Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics.

Harmful algal blooms (HABs) cause significant economic and ecological damage worldwide. Despite considerable efforts, a comprehensive understanding of the factors that promote these blooms has been lacking, because the biochemical pathways that facilitate their dominance relative to other phytoplankton within specific environments have not been identified. Here, biogeochemical measurements showed that the harmful alga Aureococcus anophagefferens outcompeted co-occurring phytoplankton in estuaries with elevated levels of dissolved organic matter and turbidity and low levels of dissolved inorganic nitrogen. We subsequently sequenced the genome of A. anophagefferens and compared its gene complement with those of six competing phytoplankton species identified through metaproteomics. Using an ecogenomic approach, we specifically focused on gene sets that may facilitate dominance within the environmental conditions present during blooms. A. anophagefferens possesses a larger genome (56 Mbp) and has more genes involved in light harvesting, organic carbon and nitrogen use, and encoding selenium- and metal-requiring enzymes than competing phytoplankton. Genes for the synthesis of microbial deterrents likely permit the proliferation of this species, with reduced mortality losses during blooms. Collectively, these findings suggest that anthropogenic activities resulting in elevated levels of turbidity, organic matter, and metals have opened a niche within coastal ecosystems that ideally suits the unique genetic capacity of A. anophagefferens and thus, has facilitated the proliferation of this and potentially other HABs.

Stable coexistence of equivalent nutrient competitors through niche differentiation in the light spectrum.

Niche-based theories and the neutral theory of biodiversity differ in their predictions of how the species composition of natural communities will respond to changes in nutrient availability. This is an issue of major environmental relevance, as many ecosystems have experienced changes in nitrogen (N) and phosphorus (P) due to anthropogenic manipulation of nutrient loading. To understand how changes in N and P limitation may impact community structure, we conducted laboratory competition experiments using a multispecies phytoplankton community sampled from the North Sea. Results showed that picocyanobacteria (Cyanobium sp.) won the competition under N limitation, while picocyanobacteria and nonmotile nanophytoplankton (Nannochloropsis sp.) coexisted at equal abundances under P limitation. Additional experiments using isolated monocultures confirmed that Cyanobium sp. depleted N to lower levels than Nannochloropsis sp., but that both species had nearly identical P requirements, suggesting a potential for neutral coexistence under P-limited conditions. Pairwise competition experiments with the two isolates seemed to support the consistency of these results, but P limitation resulted in stable species coexistence irrespective of the initial conditions rather than the random drift of species abundances predicted by neutral theory. Comparison of the light absorption spectra indicates that coexistence of the two species was stabilized through differential use of the underwater light spectrum. Our results provide an interesting experimental example of modern coexistence theory, where species were equal competitors in one niche dimension but their competitive traits differed in other niche dimensions, thus enabling stable species coexistence on a single limiting nutrient through niche differentiation in the light spectrum.

From Ecological Stoichiometry to Biochemical Composition: Variation in N and P Supply Alters Key Biosynthetic Rates in Marine Phytoplankton.

One of the major challenges in ecological stoichiometry is to establish how environmental changes in resource availability may affect both the biochemical composition of organisms and the species composition of communities. This is a pressing issue in many coastal waters, where anthropogenic activities have caused large changes in riverine nutrient inputs. Here we investigate variation in the biochemical composition and synthesis of amino acids, fatty acids (FA), and carbohydrates in mixed phytoplankton communities sampled from the North Sea. The communities were cultured in chemostats supplied with different concentrations of dissolved inorganic nitrogen (DIN) and phosphorus (DIP) to establish four different types of resource limitations. Diatoms dominated under N-limited, N+P limited and P-limited conditions. Cyanobacteria became dominant in one of the N-limited chemostats and green algae dominated in the one P-limited chemostat and under light-limited conditions. Changes in nutrient availability directly affected amino acid content, which was lowest under N and N+P limitation, higher under P-limitation and highest when light was the limiting factor. Storage carbohydrate content showed the opposite trend and storage FA content seemed to be co-dependent on community composition. The synthesis of essential amino acids was affected under N and N+P limitation, as the transformation from non-essential to essential amino acids decreased at DIN:DIP ≤ 6. The simple community structure and clearly identifiable nutrient limitations confirm and clarify previous field findings in the North Sea. Our results show that different phytoplankton groups are capable of adapting their key biosynthetic rates and hence their biochemical composition to different degrees when experiencing shifts in nutrient availability. This will have implications for phytoplankton growth, community structure, and the nutritional quality of phytoplankton as food for higher trophic levels.

Termination of a toxic Alexandrium bloom with hydrogen peroxide.

The dinoflagellate Alexandrium ostenfeldii is a well-known harmful algal species that can potentially cause paralytic shellfish poisoning (PSP). Usually A. ostenfeldii occurs in low background concentrations only, but in August of 2012 an exceptionally dense bloom of more than 1millioncellsL-1 occurred in the brackish Ouwerkerkse Kreek in The Netherlands. The A. ostenfeldii bloom produced both saxitoxins and spirolides, and is held responsible for the death of a dog with a high saxitoxin stomach content. The Ouwerkerkse Kreek routinely discharges its water into the adjacent Oosterschelde estuary, and an immediate reduction of the bloom was required to avoid contamination of extensive shellfish grounds. Previously, treatment of infected waters with hydrogen peroxide (H2O2) successfully suppressed cyanobacterial blooms in lakes. Therefore, we adapted this treatment to eradicate the Alexandrium bloom using a three-step approach. First, we investigated the required H2O2 dosage in laboratory experiments with A. ostenfeldii. Second, we tested the method in a small, isolated canal adjacent to the Ouwerkerkse Kreek. Finally, we brought 50mgL-1 of H2O2 into the entire creek system with a special device, called a water harrow, for optimal dispersal of the added H2O2. Concentrations of both vegetative cells and pellicle cysts declined by 99.8% within 48h, and PSP toxin concentrations in the water were reduced below local regulatory levels of 15µgL-1. Zooplankton were strongly affected by the H2O2 treatment, but impacts on macroinvertebrates and fish were minimal. A key advantage of this method is that the added H2O2 decays to water and oxygen within a few days, which enables rapid recovery of the system after the treatment. This is the first successful field application of H2O2 to suppress a marine harmful algal bloom, although Alexandrium spp. reoccurred at lower concentrations in the following year. The results show that H2O2 treatment provides an effective emergency management option to mitigate toxic Alexandrium blooms, especially when immediate action is required.