Hydrobiologia (2016) 764:3–27 DOI 10.1007/s10750-015-2259-4 PHYTOPLANKTON & SPATIAL GRADIENTS Review Paper Phycogeography of freshwater phytoplankton: traditional knowledge and new molecular tools Judit Padisa´k • Ga´bor Vasas • Ga´bor Borics Received: 29 November 2014 / Revised: 6 March 2015 / Accepted: 14 March 2015 / Published online: 31 March 2015 Ó Springer International Publishing Switzerland 2015 Abstract ‘‘Everything is everywhere, but environ- relevant for biogeography of freshwater phytoplank- ments selects.’’ Is this true? The cosmopolitan nature ton. The following topics are considered: dispersal of algae, including phytoplankton, has been highlight- agents and distances; survival strategies of species; ed in many textbooks and burnt into the minds of geographic distribution of different types; patterns of biologists during their studies. However, the accumu- invasions; tools of molecular genetics; and metabo- lating knowledge on the occurrence of individual lomics to explore dispersal patterns, island biogeog- phytoplankton species in habitats where they have not raphy, and associated species–area relationships for been seen before, reports on invasive phytoplankton algae. species, and the increasing number of papers with phylogenetic trees and tracing secondary metabolites, Keywords Distribution Á Dispersal Á Invasion Á especially cyanotoxins, contradict. Phytoplankton Island biogeography Á Genomics Á Bloom-forming species, with rare exceptions, are neither cosmopoli- cyanobacteria tan, nor ubiquists. In this review paper, we provide an overview of the basic patterns and the processes Introduction Guest editors: Luigi Naselli-Flores & Judit Padisa´k/ Biogeography and Spatial Patterns of Biodiversity of Freshwater Phytoplankton The Baas–Becking hypothesis, which states that ‘everything is everywhere—the environment selects’ J. Padisa´k(&) (Baas-Becking, 1934) has dominated the view on Department of Limnology & MTA-PE Limnoecology microbial distribution for decades, and has certainly Research Group of the Hungarian Academy of Sciences, University of Pannonia, Egyetem u. 10, Veszpre´m 8200, contributed to the prevailing notion that algae are Hungary cosmopolitan organisms (Harris, 1986; Pollingher, e-mail: [email protected] 1990; Graneli & Turner, 2006; Reynolds, 2006). It is true in a sense that they occur in almost each G. Vasas Department of Botany, University of Debrecen, Egyetem sufficiently illuminated habitat offered by this planet: te´r 1, Debrecen 4010, Hungary frozen rocks, caves, hotsprings, soil, inland waters. In terms of biogeography, those species are considered as G. Borics cosmopolitan which are characterized by global Department of Tisza River Research, MTA Centre for Ecological Research, Bem sqr. 18/c, Debrecen 4026, distribution or are spanning several biogeographic Hungary provinces (Dijoux et al., 2014). In terms of 123 4 Hydrobiologia (2016) 764:3–27 evolutionary biology, cosmopolitan means that either Recent evidences show that algae, including phy- such species have highly efficient means of dispersal toplankton, are neither cosmopolitan nor ubiquist and by being carried by wind or water (Fenchel & Finlay, the ‘‘everything is everywhere’’ hypothesis should be 2006) or their morphological characters are very static abandoned (Incagnone et al., 2015). Contemporane- through long evolutionary times (Ichimura, 1996). The ous knowledge in phytoplankton ecology clearly abundance–distribution relationships have long been contradicts ubiquity when matching morpho-function- in focus of ecology needing understanding of complex al adaptations of species with habitat properties based interrelations and feedbacks between ecological and on two assumptions: (1) a functionally well-adapted evolutionary processes that shape dispersal. Relevant species is likely to tolerate the constraining conditions eco-evolutionary forces can be found at all hierarchi- of factor deficiency more successfully than individuals cal levels: from landscapes to communities via of a less well-adapted species; and (2) a habitat shown populations, individuals, and genes (Kubisch et al., typically to be constrained by a certain factor is more 2014). likely to be populated by species with the appropriate Some phytoplankton species appear rather static in adaptations to be able to function there (Reynolds their morphological characters (‘‘good species’’, like et al., 2002; Padisa´k et al., 2009). For the above reason, Gloeotrichia echinulata), while others vary within a Padisa´k(2003) suggested replacing the term cos- wide range. Former taxonomic concepts weighed mopolitan by subcosmopolitan for species occurring minor morphological differences by giving them a throughout the world but always in environments taxonomic (usually intraspecific) rank resulting in an corresponding to species-specific adaptations. The almost endless intraspecific diversification of some wide distribution of such species is, therefore, mosaic- taxa (see, e.g., the case of Scenedesmus in Padisa´k& like reflecting the distribution of corresponding Hegewald, 1992). This practice allowed Lange-Ber- habitats. talot & Simonsen (1978) to conclude that ‘‘the When dealing with phycogeography of phytoplank- traditional definition of species, because of lack of a ton, there is a bunch of facts, assumptions, and sufficient species concept, must lead to infinite separa- observations to consider. In this review, the following tion… finally to individuals.’’Recent investigators tend topics will be considered: phylogeny-based properties to place formerly considered separate species to like reproduction and survival strategy of species, synonymy. Without a deeper discussion of species geographic distribution of different types of habitats, concepts applicable for phytoplankton (see some existing knowledge on geographic distributions, dis- considerations in Kristiansen, 1996a) and results from persal agents, sensitivity/tolerance of dispersal condi- modern phylogenetics (see Krienitz, 2009), it is tions, patterns of invasions, tools of molecular necessary to realize that biogeographic qualifications genetics, metabolomics, and ecophysiology to explore (subtropical, polar, endemic, etc.) depend considerably dispersal patterns, island biogeography and associated on the taxonomic level and the species concept applied. species–area relationships for algae. The term, ubiquist (from the Latin ubique = occurs everywhere), is often used in biology as a synonym of cosmopolitan (Fenchel & Finlay, 2006) but other Dispersal agents and distances meanings are also found. In some works, it serves as synonym of ruderal (Gru¨newald & Schubert, 2007). In Vegetative forms of phytoplankton are permanently other publications, ubiquists are species having wide living in water. Open water, especially lakes, can be tolerance limits in contrast to others with narrow seen as islands on the terrain. Therefore, to move from niches (Gorthner & Meier-Brook, 1985); those occur- a certain water body to another, propagules have to ring both in standing and running waters (Goffart, travel over the land exposed to risk of desiccation. 2010) or ‘‘all kinds of’’ water (Lock et al., 2013). The Some groups of algae have specialized forms worst case is when ‘‘ubiquitous’’ is merely a vague (akinetes, cysts, spores) resistant to terrestrial condi- phrase (Posch et al., 2012). It is necessary to realize tions, but most do not have. Dispersal of phytoplank- that the term ubiquist carries a much broader meaning ton obligatorily needs some dispersal agent (river, air, than cosmopolitan because it often implies ecological animals, man) with travel distance and conditions preferences, tolerance ranges, or quantities. meeting with species’ tolerance of transport. 123 Hydrobiologia (2016) 764:3–27 5 River courses, reservoirs dams higher that 15 m exist at present in all continents. Many were constructed in arid regions Travel along river courses has been the most evident that used to represent migratory barriers for aquatic way of dispersal since risk of desiccation can be ruled biota. It was elegantly demonstrated for zooplankton out. The river phytoplankton flora can be extremely that reservoirs (especially in the arid regions) serve as rich. For example, Kusel-Fetzmann (1998) catalogued step-stones, thus facilitating their dispersal (Dumont, 2692 species in River Danube, with almost half of 1999). In South America, the proliferation of them being chlorophytes. In general, the river flora cyanobacteria as well as the recent invasion of does not contain any species that would not be found in Ceratium furcoides (Levander) Langhans and C. lakes (Reynolds et al., 1994), but it is similarly true hirundinella (O. F. Mu¨ller) Dujardin (Santos-Wis- that phytoplankton species are differently adapted to niewski et al., 2007; Matsumura-Tundisi et al., 2010; survive lotic conditions. Dead zones (Stoyneva, 1994) Bustamante et al., 2012; Gil et al., 2012; Cavalcante and lateral waters (Talling & Prowse, 2010) may offer et al., 2013) are largely a consequence of building a chance for less-adapted species to survive. In the cascades of reservoirs on large rivers. Floristic past, river channels had been wilder than they were similarity between rivers, reservoirs, and lateral lakes recently, thus offering a much higher proportion of especially with extended swamp areas allowed sup- dead zones, and therefore a higher habitat diversity for posing very efficient transport mechanisms (Talling & many species to survive. Main features of river