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Freshwater Phytoplankton Diversity: Models, Drivers and Implications for Ecosystem Properties

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Freshwater Phytoplankton Diversity: Models, Drivers and Implications for Ecosystem Properties Hydrobiologia https://doi.org/10.1007/s10750-020-04332-9 (0123456789().,-volV)( 0123456789().,-volV) COLIN S. REYNOLDS’ LEGACY Review Paper Freshwater phytoplankton diversity: models, drivers and implications for ecosystem properties Ga´bor Borics . Andra´s Abonyi . Nico Salmaso . Robert Ptacnik Received: 25 February 2020 / Revised: 9 June 2020 / Accepted: 13 June 2020 Ó The Author(s) 2020 Abstract Our understanding on phytoplankton diver- experiments helped understand species coexistence and sity has largely been progressing since the publication of maintenance of diversity in phytoplankton. The non- Hutchinson on the paradox of the plankton. In this paper, equilibrium nature of phytoplankton and the role of we summarise some major steps in phytoplankton disturbances in shaping diversity are also discussed. ecology in the context of mechanisms underlying Furthermore, we discuss the role of water body size, phytoplankton diversity. Here, we provide a framework productivity of habitats and temperature on phytoplank- for phytoplankton community assembly and an over- ton species richness, and how diversity may affect the view of measures on taxonomic and functional diversity. functioning of lake ecosystems. At last, we give an We show how ecological theories on species competition insight into molecular tools that have emerged in the last together with modelling approaches and laboratory decades and argue how it has broadened our perspective on microbial diversity. Besides historical backgrounds, some critical comments have also been made. Guest editors: Judit Padisa´k, J. Alex Elliott, Martin T. Dokulil & Luigi Naselli-Flores / New, old and evergreen frontiers in freshwater phytoplankton ecology: the legacy of Keywords Community assembly Á Diversity Colin S. Reynolds maintenance Á Ecosystem functioning Á Functional diversity Á Molecular approaches Á Taxonomic Electronic supplementary material The online version of diversity this article (https://doi.org/10.1007/s10750-020-04332-9) con- tains supplementary material, which is available to authorized users. G. Borics (&) A. Abonyi Á R. Ptacnik Department of Tisza Research, Centre for Ecological WasserCluster Lunz – Biologische Station GmbH, Dr. Research, Danube Research Institute, Bem te´r 18/c, Carl Kupelwieser-Promenade 5, 3293 Lunz am See, 4026 Debrecen, Hungary Austria e-mail: [email protected] N. Salmaso G. Borics Research and Innovation Centre, Fondazione Edmund GINOP Sustainable Ecosystems Group, Centre for Mach, Via E. Mach 1, 38010 San Michele all’Adige, Italy Ecological Research, Klebelsberg Kuno u. 3, 8237 Tihany, Hungary A. Abonyi Centre for Ecological Research, Institute of Ecology and Botany, Alkotma´ny u. 2-4, 2163 Va´cra´to´t, Hungary 123 Hydrobiologia Introduction (Wilson, 1990). Wilson reviewed evidences for twelve possible mechanisms that potentially could explain the Phytoplankton is a polyphyletic group with utmost paradox for indigenous New Zealand vegetation, and variation in size, shape, colour, type of metabolism, found that four of them, such as gradual climate and life history traits. Due to the emerging knowledge change, cyclic successional processes, spatial mass in nutritional capabilities of microorganisms, our view effect and niche diversification, were the most impor- of phytoplankton has drastically changed (Flynn et al., tant explanations. By now, the paradox has been 2013). Phagotrophy is now known from all clades considered as an apparent violation of the competitive except diatoms and cyanobacteria. At the same time, exclusion principle in the entire field of ecology ciliates, which have not been considered as part of (Hening & Nguyen, 2020). ‘phytoplankton’, span a gradient in trophic modes that Although Hutchinson’s contribution (Hutchinson, render the distinction between phototrophic phyto- 1961) has given a great impetus to research on species plankton and heterotrophic protozoa meaningless. coexistence, the number of studies on phytoplankton This complexity has been expressed in the high diversity that time did not increase considerably diversity of natural phytoplankton assemblages. (Fig. 1), partly because in this period, eutrophication Diversity can be defined in many different ways and studies dominated the hydrobiological literature. levels. Although the first diversity measure that Understanding the drivers of diversity has been encompassed the two basic components of diversity substantially improved from the 70 s when laboratory (i.e., the number of items and their relative frequen- experiments and mathematical modelling proved that cies) appeared in the early forties of the last century competition theory or intermediate disturbance (Fisher et al., 1943), in phytoplankton ecology, hypothesis (IDH) provided explanations for species taxonomic richness has been used the most often as coexistence. Many field studies also demonstrated the diversity estimates. Until the widespread use of the role of disturbances in maintaining phytoplankton inverted microscopes, phytoplankton ecologists did diversity, and these results were concluded by not have accurate abundance estimation methods and Reynolds and his co-workers (Reynolds et al., 1993). the net plankton served as a basis for the analyses. From the 2000 s a rapid increase in phytoplankton Richness of taxonomic groups of net samples, and research appeared (Fig. 1), which might be explained their ratios were used for quality assessment (Thun- by theoretical and methodological improvements in mark, 1945, Nygaard, 1949). ecology. The functional approaches—partly due to The study of phytoplankton diversity received a Colin Reynolds’s prominent contribution to this field great impetus after Hutchinson’s (1961) seminal paper (Reynolds et al., 2002)—opened new perspectives in on the paradox of the plankton. The author not only phytoplankton diversity research. Functional trait and contrasted Hardin’s competitive exclusion theory functional ‘group’-based approaches have gained (Hardin, 1960) with the high number of co-occurring considerable popularity in recent years (Weithoff, species in a seemingly homogeneous environment, but outlined possible explanations. He argued for the non- equilibrium nature of the plankton, the roles of 800 disturbances and biotic interactions, moreover the 700 importance of benthic habitats in the recruitment of phytoplankton. The ‘paradox of the plankton’ largely 600 influenced the study of diversity in particular and the 500 development of community ecology in general 400 (Naselli-Flores & Rossetti, 2010). Several equilibrium 300 and non-equilibrium mechanisms have been devel- 200 oped to address the question of species coexistence in 100 pelagic waters (reviewed by Roy & Chattopadhyay, 0 2007). The paradox and the models that aimed to 1960 1970 1980 1990 2000 2010 2020 explain the species coexistence in the aquatic envi- ronment have been extended to terrestrial ecosystems Fig. 1 Annual number of hits on Google Scholar for the keywords ‘‘phytoplankton diversity’’ 123 Hydrobiologia 2003; Litchman & Klausmeier, 2008; Borics et al., enough to describe both aspects, but these can be 2012; Vallina, et al., 2017; Ye et al., 2019). clearly defined by the mathematical formulas that we Analysis of large databases enabled to study use as diversity measures. diversity changes on larger scales in lake area, productivity or temperature (Stomp et al., 2011). Richness metrics Recent studies on phytoplankton also revealed that phytoplankton diversity was more than a single metric The simplest measure of diversity is species richness, by which species or functional richness could be that is, the number of species observed per sampling described, instead, it was an essential characteristic, unit. However, this metric can only be used safely which affects functioning of the ecosystems, such as when the applied counting approach ensures high resilience (Gunderson 2000) or resource use efficiency species detectability. (Ptacnik et al., 2008; Abonyi et al., 2018a, b). In case of phytoplankton, species detectability The widespread use of molecular tools that reor- depends strongly on counting effort, therefore, mea- ganise phytoplankton taxonomy and reveal the pres- sures that are standardised by the number of individ- ence of cryptic diversity, has changed our view of uals observed, e.g. Margalef and Mehinick indices phytoplankton diversity. In this study, we aim to give (Clifford & Stephenson, 1975) safeguard against an overview of the above-mentioned advancements in biased interpretations. Ideally, standardization should phytoplankton diversity. Here we focus on the take place in the process of identification. Pomati et al. following issues: (2015) gave an example how a general detection limits could be applied in retrospect to data stemming from • measures of diversity, variable counting efforts. • mechanisms affecting diversity, Species richness can also be given using richness • changes of diversity along environmental gradients estimators. These can be parametric curve-fitting (area, productivity, temperature), approaches, non-parametric estimators, and extrapo- • the functional diversity–ecosystem functioning lation techniques using species accumulation or relationship, and species-area curves (Gotelli & Colwell, 2011; Magur- • phytoplankton diversity using molecular tools. ran, 2004). These approaches have been increasingly More than eight thousand studies have been pub- applied in phytoplankton ecology (Naselli-Flores lished on ‘‘phytoplankton diversity’’ since the term et al.,
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