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Effects of plankton community structure on energy pathways and trophic efficiency

Final Report Summary - TROPHIC EFFICIENCY (Effects of plankton community structure on energy pathways and trophic efficiency)

A current challenge to ecologists is to predict how compositional shifts at the base of the aquatic food web propagate up to higher trophic levels. The overall objectives of TROPHIC EFFICIENCY were to investigate how shifts in plankton composition affect carbon and nutritional transfer efficiency to primary consumers and how this transfer is affected by climate change. Trophic efficiency is estimated from production rates, dietary sources and nutritional transfer using biomarkers, which was investigated in various multidisciplinary experiments using small-scale laboratory and larger ecosystem-scale mesocosm experiments. Plankton communities were manipulated by exposing communities to climate change scenarios of increasing temperature and ocean acidification (OA). We have also used biological tracers of combined fatty acid-specific δ13C isotope biomarkers (δ13C-FA) to characterize flow of essential nutrients and production rates in food webs.

Major outcomes of TROPHIC EFFICIENCY were:

Elevated CO2 significantly changed the FA concentration and composition of the diatom Thalassiosira pseudonana, which constrained growth and reproduction of the copepod Acartia tonsa. A significant decline in both total FAs (28.1 to 17.4 fg cell-1) and the ratio of long-chain polyunsaturated to saturated fatty acids (PUFA:SFA) of food algae cultured under elevated (750 µatm ) compared to present day (380 µatm) pCO2 was directly translated to copepods. The proportion of total essential FAs declined almost tenfold in copepods and the contribution of saturated fatty acids (SFAs) tripled at high CO2. This rapid and reversible CO2-dependent shift in FA concentration and composition caused a decrease in both copepod somatic growth and egg production from 34 to 5 eggs female-1 day-1. Because the diatom-copepod link supports some of the most productive ecosystems in the world, our study demonstrates that OA can have far-reaching consequences for ocean food webs by changing the nutritional quality of essential macromolecules in primary producers that cascade up the food web.

Following, results from multiple mesocosm experiments with multi-trophic levels showed diverse responses, depending on the origin of community composition. Using a plankton community of the Kiel Fjord we showed that this community was tolerant to pCO2 levels projected by the end of this century (<1400 µatm), and only subtle differences were observed at extreme high values of 4000 µatm. We found similar phyto- and microzooplankton biomass and copepod abundance and egg production across all CO2 treatment levels. Stoichiometric phytoplankton food quality was minimal different at the highest pCO2 treatment, which was however far from being potentially limiting for copepods. These results contrast studies including single species that observed strong indirect CO2 effects for herbivores, suggesting limitations of biological responses at the organism to the community level. A dampening of CO2-effects can be expected for coastal communities adapted to strong natural fluctuations in pCO2, typical for productive coastal habitats. Although this coastal plankton community was highly tolerant to high fluctuations in pCO2, increase in hypoxia and CO2 uptake by the ocean can aggravate acidification and may lead to pH changes outside the experienced range for coastal organisms.

We also investigate how OA affects phytoplankton community composition and fatty acid profile of a North Sea offshore plankton community that experience more constant CO2 conditions, and how changes at the primary producers level transfer to higher trophic levels using biomarkers. Results showed that community composition of primary producers changed towards an increase of pico-sized cells, primarily picoeukaryote at high pCO2 level, while nano-size coccolitophores decreased. This shift in species composition and size structure was related to a decline in the relative polyunsaturated fatty acids (PUFA) content of the nano- and picophytoplankton size fractions. These changes in phytoplankton reduced PUFA content of a dominant copepod species, and thus indicate that changes at the base of the food web affect production at higher trophic levels.

Using a North Sea community, we also investigate the response of gelatinous zooplankton to climate change, which may have significant ecosystem implications as they can alter biogeochemical cycling compared to classical copepod dominated food webs. We find an increase in the dominance of gelatinous zooplankton at higher temperature and CO2, which removed particles from the water column that might otherwise nourish copepods and fish by increasing carbon transport to depth from the continuous discarding of their mucous filtration houses and fecal pellets. This helps to remove CO2 from the atmosphere, but may also have significant fisheries implications.

We also conduced a similar experiment with brackish water communities of the Baltic Sea as they are expected to be less affected by OA as these communities are typically adapted to high fluctuations in CO2 and pH. Seston FA composition was influenced by community composition, which in turn was driven by silicate and phosphate limitation in the mesocosms, and showed no difference between CO2 treatments. These results suggest that CO2 effects are dampened in coastal communities that already experience high natural fluctuations in pCO2.

In order to determine the long-term interactive effects of CO2 and temperature on PP, we analyzed FA in the diatom Cylindrotheca fusiformis exposed for >250 generations to climate scenarios. We find deleterious effects of temperature and CO2 on the essential FA, which corroborates with previous studies.

Finally, we investigated algal fatty and amino acids across major taxonomic groups, which is important because phytoplankton species composition varies greatly over the season. Phytoplankton are the primary producer of essential biomolecules and their composition differs largely between major taxonomic groups, yet a detailed analysis of several essential biomolecules is lacking. Our findings indicate that major taxonomic groups differ in the concentrations of important biochemical compounds, creating trade-offs for herbivore consumers. These differences in compound concentrations explain why a more diverse nutrition leads to higher production rates of consumers than mono-specific diets. Thus, growth and reproduction of consumers (zooplankton, fish larvae) can be constrained by taxonomic composition or food quality of primary producers.

Together, these investigations with diverse communities provide an improved understanding on how shifts in food web structure at the base of the aquatic food web affect carbon flux through the plankton food web, which is important because these processes have profound influence on fisheries and climate.