The craving for phosphorus in heterotrophic dinoflagellates and its implications for biogeochemical cycles: Coastal P-cycling and dinoflagellates

By altering the nutritional quality of primary producers, nutrient availability indirectly influences herbivores’ population dynamics. In turn, the resulting relationship between diet, growth, and wastes has consequences for nutrient cycling at the ecosystem level. We studied the link between dinoflagellates nutritional requirements and feeding behavior, and its influence on nutrient cycling. We show that long-term shifts in dissolved PO4 concentration in the North Sea are closely linked to biomass trends of heterotrophic dinoflagellates and support this observation with experimental data indicating particularly high phosphorus requirements in dinoflagellates. At the seasonal scale, we observe a negative correlation between natural dinoflagellate abundances and the concentration of dissolved P, and we estimate that, in spring, up to 30% of dissolved P can end up in microzooplankton biomass. Our study highlights that accounting for organismal metabolic requirement provides significant insight in interpreting and predicting nutrient cycles at the ecosystem level. Food quality is a major driver of zooplankton population dynamics (Gulati and Demott 1997; Danielsdottir et al. 2007). Because phytoplankton nutritional value strongly varies with the abiotic environment (Sterner and Elser 2002; Persson et al. 2010), herbivore zooplankton often feed on prey not matching their metabolic requirements. While autotrophs’ carbon (C), nitrogen (N), and phosphorus (P) contents are influenced by the relative accessibility of light, carbon dioxide, and dissolved nutrients and as a result are highly variable (Sterner and Elser 2002), the elemental composition of heterotrophic plankton is less plastic (Meunier et al. 2012a, 2014). Differences between prey C : N : P stoichiometry and predator metabolic requirements thus cause a mismatch which may have consequences for zooplankton population dynamics as it directly influences feeding rates and growth (Hantzsche and Boersma 2010; Jeong et al. 2010; Zhang et al. 2017). Since the 1970s, a succession of conventions and directives (e.g., OSPAR, Water Framework Directive) has been adopted in Europe to reduce N and P inputs to areas affected or likely to be affected by eutrophication. The consequences of these measures can be seen in the North Sea where dissolved P concentrations increased until 1978 and decreased afterwards (Sarker and Wiltshire 2017). The overall phytoplankton carrying capacity of the North Sea was shown to be related to the shift in dissolved P concentration (Sarker and Wiltshire 2017). Interestingly, there is also a parallel trend in time between the concentration of dissolved PO4 and the biomass of heterotrophic dinoflagellates in the same area (Fig. 1). This observation indicates that, on a long time scale, there is a positive correlation between the nutrient concentration of the water (here measured as dissolved PO4) and the density of heterotrophic dinoflagellates. Fast growth is a universal trait in heterotrophic dinoflagellates (Landry and Calbet 2004; Sherr and Sherr 2007), also in those found in the North Sea (Mieruch et al. 2010), which, according to the Growth Rate Hypothesis, suggests that these organisms *Correspondence: cedric.meunier@awi.de Present address: Natural History Museum, London, UK LOCEAN Laboratoire d’Oc�eanographie et du Climat Exp� erimentations et Approches Num� eriques, Universit� e Pierre et Marie Curie, Paris, France SINTEF Ocean, Marine Resources Technology, Trondheim, Norway Additional Supporting Information may be found in the online version of this article. 1 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 00, 2018, 00–00 VC 2018 Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10807 Limnol. Oceanogr. 63, 2 18, 1774–1784 © 2018 A sociation for the Sciences f i l i: . l . xxxxx