Episodic nutrient enrichments stabilise protist coexistence in planktonic oligotrophic conditions

Abstract

Seasonal compositional changes in plankton communities are usually considered as species replacements. Given the enormous number of individuals integrating the communities and our limited capacity to count and determine most of them, we likely observe only alternative population peaks of some of the coexisting species. The contemporary coexistence theory addresses coexistence in communities of competing species, considering relative fitness inequalities and stabilising niche differences as components of average long‐term growth rates. Here, we experimentally show that the response patterns predicted by the theory occur when varying nutrient pulses fertilise the planktonic community. We used gently self‐filling 100‐L enclosures to minimise the disturbance of the initial community and different pulse P and N additions to manipulate the apparently species‐poor epilimnetic community of an ultraoligotrophic P‐limited lake. We measured and compared the protist species growth response to gradients of P enrichment and N stoichiometric imbalance. The P and N levels used in most treatments were within the oligotrophic seasonal and inter‐annual variations of the lake and were higher in a few extreme treatments that provided mesotrophic conditions of the remote regions affected by N atmospheric contamination. We alternatively replicated all treatments using ammonium or nitrate as the N source. Most protist species, recorded in this lake across seasons in previous studies, were recovered, indicating a persistent assemblage of species that is seasonally hidden from observation. Recovery included some rare species observed only in the slush layers of the seasonal snow and ice cover. The coexistence‐stabilising mechanisms were indicated by treatment response features, such as frequency‐dependent growth, inverse relationship between fitness inequality and niche differentiation proxies, high‐rank taxonomic levels clustering across the limiting‐nutrient gradient but segregation at the species level according to the type of N supply and resting stage development depending on nutrient conditions. The response similarities between autotrophic and heterotrophic organisms indicate a network of interactions that may reinforce coexistence. Synthesis. The results indicate that many planktonic protist species in oligotrophic waters can show stable long‐term non‐equilibrium coexistence by alternately recovering from very low densities when episodic nutrient enrichments, of varying P and N amounts and composition, occur.

Bacterioplankton seasonality in deep high-mountain lakes

“…Our findings also contrast the idea of a succession of communities that replace each other across seasons ( Fuhrman et al, 2006 ; Crump et al, 2009 ; Eiler et al, 2012 ). Instead, the environmental oscillations seem to foster coexistence similar to what has been found for protists ( Zufiaurre et al, 2021 ). Three main types of community members concerning seasonal patterns were found: (i) OTUs with stable abundance, non-sensitive to seasonal environmental fluctuations and depth gradients; (ii) OTUs with high abundance under ice and in the hypolimnion, declining only in the summer epilimnion, and (iii) OTUs with a low abundance that increased in the epilimnion when many other OTUs declined.…”

“…The bacterial core community can be seen as a stable non-equilibrium coexistence of many taxa in a fluctuating environment ( Chesson, 2000 ), in which environmental seasonality might play a central role in shaping the community ( Mathias and Chesson, 2013 ; Zufiaurre et al, 2021 ). According to the theory, the taxa coexistence is based on compensating fitness advantage by niche differentiation.…”

Phytoplankton assemblage shifts with dissolved organic matter properties: A functional perspective for sentinel lakes

“…Species richness substantially increased, and diversity was at a peak. Changes in phytoplankton community structure have previously been observed after snowmelt as a consequence of meltwater inputs in oligotrophic lakes (Williams et al, 2016), and episodic nutrient enrichments can increase species richness (Zufiaurre et al, 2021). Although DIN and SRP concentrations did not significantly increase during the OP, the increased richness and diversity observed during this period was likely the result of allochthonous inputs occurring early during snowmelt.…”

“…after snowmelt as a consequence of meltwater inputs in oligotrophic lakes (Williams et al, 2016), and episodic nutrient enrichments can increase species richness (Zufiaurre et al, 2021).…”

Self-filling enclosures to experimentally assess plankton response to pulse nutrient enrichments

“…The planktonic community in Lake Redon is P-limited due to the long-range atmospheric transport of reactive nitrogen ( Camarero and Catalan, 2012 ). The primary objective of the ENEX experiment was to evaluate the effects of the fluctuations in P availability and N:P imbalance on the structure of the planktonic protist community ( Zufiaurre et al ., 2021 ) and its stoichiometry ( Giménez-Grau et al ., 2020 ). We first describe the enclosure design and use as performed in the ENEX experiment, and, in the discussion, we comment on alternative options and designs according to other objectives and lake characteristics.…”