Nitrogen fixation by cyanobacteria stimulates production in Baltic food webs

Abstract

Filamentous, nitrogen-fixing cyanobacteria form extensive summer blooms in the Baltic Sea. Their ability to fix dissolved N2 allows cyanobacteria to circumvent the general summer nitrogen limitation, while also generating a supply of novel bioavailable nitrogen for the food web. However, the fate of the nitrogen fixed by cyanobacteria remains unresolved, as does its importance for secondary production in the Baltic Sea. Here, we synthesize recent experimental and field studies providing strong empirical evidence that cyanobacterial nitrogen is efficiently assimilated and transferred in Baltic food webs via two major pathways: directly by grazing on fresh or decaying cyanobacteria and indirectly through the uptake by other phytoplankton and microbes of bioavailable nitrogen exuded from cyanobacterial cells. This information is an essential step toward guiding nutrient management to minimize noxious blooms without overly reducing secondary production, and ultimately most probably fish production in the Baltic Sea.

Fig. 1

Bloom-forming diazotrophic cyanobacteria stimulating secondary production in the Baltic Sea. By fixing dissolved N₂, these cyanobacteria are important suppliers of bioavailable nitrogen to the pelagic and benthic food webs that support fish production. The bioavailable nitrogen enters the food web through direct grazing on fresh or decaying filamentous cyanobacteria by various invertebrates and by cyanobacterial cells releasing bioavailable nitrogen (denoted by R) that is taken up by other phytoplankton and microbes, which are in turn eaten by animals in the water column and sediments

Fig. 2

δ ¹⁵N and isotopic niche in pelagic and benthic consumers in the northern Baltic proper as a function of cyanobacterial biomass. a δ ¹⁵N in zooplankton (copepods and cladocerans, filled circles) decreases significantly with increasing mean cyanobacteria biovolume (mm³ l⁻¹) indicating uptake of diazotrophic nitrogen by zooplankton. Line indicates the trend. Data for June–August, 1976–2010, Askö area, station B1; see Appendix S1 for details. Published data on δ ¹⁵N in crustacean zooplankton in summer (open squares) support the trend; numbers inside the squares indicate the study (1 Hansson et al. ; 2 Rolff and Elmgren ; 3 Rolff ; 4 Holliland et al. ; and 5 Hansen et al. 2012). b Diet diversity measured as isotopic niche size in the deposit-feeding amphipod Monoporeia affinis in October increases significantly with annual bloom biovolume calculated as the area under the curve for plots of cyanobacteria biovolume over time (May to September, 2000–2011, Himmerfjärden Bay, see Appendix S2 for details). Line indicates the trend. Larger values of isotopic niche estimated as convex hull area suggest larger trophic diversity and greater dietary breadth. a Spearman r = −0.85, p < 0.001; b Spearman r = −0.79, p < 0.001

Fig. 3

Uptake of cyanobacteria-fixed nitrogen by pelagic and benthic consumers inferred from seasonal changes in their δ ¹⁵N values and stomach content analysis in relation to the cyanobacterial bloom in different areas of the Baltic Sea. a δ ¹⁵N (mean ± SD) in invertebrates and fish from three coastal areas: Åland Islands (Nordström et al. 2009), Curonian Lagoon (Lesutiene et al. 2014), and Askö area (Rolff 2000), in relation to the cyanobacteria bloom. Invertebrate species and groups: Cr Crangon crangon; Ne Nereis diversicolor; Ma Macoma balthica; Ba Bathyporeia pilosa; Ch Chironomidae; Dr Dreissena polymorpha; Va Valvata; Ol Oligochaeta; Mz mesozooplankton; PL4 zooplankton, size 100–200 µm (nauplii, rotifers, ciliates); PL5 zooplankton, size 200–500 µm (copepodites, cladocerans); and PL6 zooplankton, size > 500 µm (adult copepods). Fish: Pl Platichthys flesus and Ga Gasterosteus aculeatus; b δ ¹⁵N values of zooplankton (bars, primary Y-axis on the left side; mean ± SD, n > 3) and grazing on cyanobacteria derived from qPCR-based estimates of N. spumigena abundance in zooplankton stomachs (circles; secondary Y-axis on the left side; mean ± SD, n > 4) sampled throughout cyanobacteria bloom (green line) in the open sea (Landsort Deep, station BY31; year 2011; Motwani ; see Appendix S3). c δ ¹⁵N values in deposit-feeders (mean ± SD, n > 10) sampled before and after a cyanobacteria bloom (green line) in a coastal area (Askö, station B1; year 2010; modified from Karlson et al. (2014)

Fig. 4

Effects of cyanobacteria on fitness-related traits (EPR egg production rate and EV% egg viability) and growth-related biochemical indices (BI) in Baltic copepods (Acartia bifilosa, A. tonsa, and Eurytemora affinis; studies 1–4, and 6) and amphipods (Monoporeia affinis; studies 5 and 7–8). Only studies that used feeding conditions with cyanobacteria concentrations approximating those during summer bloom in the Baltic Sea and animals pre-exposed to the bloom are presented. Effects are expressed as % deviation from the control (non-cyanobacterial diet, green line); non-significant effects (p > 0.05) are marked ns. Numbers on the X-axis indicate study reporting the effect; 1 Schmidt and Jonasdóttir (1997), 2 Koski et al. (2002), 3 Vehmaa et al. (2013), 4 Schmidt et al. (2002), 5 Wiklund et al. (2008), 6 Hogfors et al. (2011), 7 Karlson (unpubl.) (see Appendix S4), and 8 Karlson et al. (2014). The biochemical indices of growth status: ORAC:TBARS ratio [ORAC total antioxidative status measured as oxygen radical absorbance capacity and TBARS lipid peroxidation measured as production of thiobarbituric acid reactive substances; (Vehmaa et al. 2013)] is a proxy for oxidative status, RNA:DNA ratio is a proxy for protein synthetic capacity, and the C:N ratio reflects lipid storage in amphipods

Fig. 5

Seasonal development of a phytoplankton biomass, including cyanobacteria, b zooplankton biomass, and c estimated food consumption by zooplanktivorous fish in the Baltic Sea. In June–September, cyanobacteria contribute substantially to the phytoplankton communities, which coincides with the highest zooplankton stocks, and the highest food consumption by fish. The phytoplankton and zooplankton data are long-term means (1992–2011) for the Askö area (station B1), and fish estimated food consumption data are from Arrhenius and Hansson (1993). See Appendix S1 for details on plankton sampling and analysis. a Black line total phytoplankton, grey shading cyanobacteria; c grey shading sprat, black shading herring