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 flora Prowse, 2010) in case of the Nile system where, in show interesting biogeographic differences. In the contrast, distinctive floristic composition of phyto- Northern Hemisphere, unicellular centrics and chloro- plankton in headwater lakes was reflected in higher coccalean green algae are the commonest members of level of dissimilarities owing to more distinctive river phytoplankton (Schmidt, 1994; Abonyi et al., environmental features. 2012, 2014). In South American rivers, chain-forming Newly built reservoirs in their initial years of centrics (Unrein, 2002;Go´mez et al., 2004) are often operation often host species typical for the supplying found and blue-green algae are common in Australian river and its catchment; species not recorded in the rivers (Ho¨tzel & Croome, 1994; Bowling & Baker, catchment occur after a longer time (Atkinson, 1988). 1996; Mitrovic et al., 2003). Observations on the travel In a study by Chrisostomou et al. (2009), species length of species, which are not well adapted to river present in the local flora were found in experimental flow, are rare. According to Mitrovic et al. (2003), a tanks. However, young reservoirs may host apparently flow velocity of 0.05 ms-1 prevents development of ‘‘unfitted’’ species, as shown in case of a newly formed Dolichospermum circinalis (Rabenhorst ex Bornet & ornamental lake in Devecser, Hungary where in the Flahault) Wacklin, Hoffmann et Koma´rek, a species second year of operation, a bloom of Entomoneis typically growing in lakes. The successful dispersion paludosa var. subsalina (Cleve) Krammer, a species of the cyanoprokaryote Cylindrospermopsis raci- typical for inland saline lakes (soda pans), occurred in borskii (Woloszynska) Seenayya et Subba Raju, was high densities (Szalay, 2014). largely attributed to its ability to tolerate travel along river courses (Padisa´k, 1997). For example, parts of a Airborne algae—wind population from an inflow channel were present in quantitative samples from river Tisza (average flow Dispersal of algae by winds has for long been in focus velocity: 1 ms-1; Borics et al., 2007) 400 km down- of interest. Ehrenberg (1849) found 18 species of stream (Hamar, 1977). This indicates the extremely diatoms in dust collected by Darwin (1839) on the good tolerance of this species to survive travel HMS Beagle, 300 km from the nearest coast (viability conditions in river courses. was not tested). During his transatlantic flight in 1933, Although most rivers in the industrialized world are Lindberg collected samples from the air (Gisle´n, reduced to simple flow channels and therefore have 1948). Later, Overeem (1937) filtered air from a lost their retention zones where less-adapted species maximal height of 2000 m downward and found a may survive, reservoir construction counteracts and maximum concentration of algae at 500 m. The offers suitable environments for phytoplankton. Ac- samples contained aerophilic green algae like Chloro- cording to estimates, more than 50,000 reservoirs with coccum, Stichococcus, Pleurococcus, Hormidium and 123 6 Hydrobiologia (2016) 764:3–27 some cyanoprokaryotes. Long-distance dispersal of digestive enzymes. One of the most detailed studies diatoms in volcanic ash has recently been proven by was that of Sides (1973) cultivating materials obtained Van Eaton et al. (2013) after eruption of Taupa from feet, feathers, toes, and intestines (both esophagi volcano (New Zealand) using Cyclostephanos no- and colons) of 61 sea gulls (belonging to four species) vaezeelandiae (Cleve) Round, an endemic species to shot over land. The highest number of algal taxa was New Zealand’s North Island, as biomarker. Results found on feet, followed by intestines, toes, and supported dispersion distances of hundreds of kilo- feathers. Besides periphytic, metaphytic and aerophi- meters: however, viability of the diatoms, especially lic algae, and ‘‘green balls’’ supplied with different those that are not microaerophilic, under eruption names, a number of freshwater phytoplankton species conditions (abrupt heating up) and then atmospheric were identified in the cultures: Anabaena sp., Aphani- transport (abrupt cooling down, UV, desiccation) has zomenon flos-aquae (Linnaeus) Ralfs ex Bornet et been questionable (Pike, 2013). Most airborne algae Flahault, Aphanothece sp., Chroococcus sp., Gloeo- belong to the Chlorophyta (Sharma et al., 2007; trichia sp., Merismopedia elegans A. Braun ex Genitsaris et al., 2011) and occur in most biogeo- Ku¨tzing, Anacystis (Microcystis) aeruginosa, Actinas- graphic regions (Roy-Ocotla & Carrera, 1993) includ- trum hantzschii Lagerheim, Ankistrodesmus convolu- ing deserts (Lewis & Lewis, 2005). tus Corda, A. falcatus (Corda) Ralfs, Chlamydomonas The presence in aerosols of planktonic algae like sp., Chodatella sp., Oocystis sp., O. lacustris Chodat, ‘‘Chlorella’’ (for the reason of quote marks see Luo Scenedesmus sp., Campylodiscus clypeus (Ehrenberg) et al., 2010), Chalmydomonas, Nostoc, Anabaena, and Ehrenberg ex Ku¨tzing, Fragilaria construens (Ehren- Planctonema have also been demonstrated and re- berg) Grunow. A similar number of taxa were viewed by Kristiansen (1996b). A recent study aimed cultivated from esophagi and colons indicating that directly at an experimental research on capacity of many of the ingested taxa remain viable after passing phytoplankton to disperse through air found a number the guts. From the point of view of transporting algae, of phytoplankton species: (Jaaginema sp., Plank- esophagi are also of importance since gulls often tolyngbya limnetica (Lemmermann) Koma´rkova´-Leg- regurgitate food for their chicks and also for young nerova´ & Cronberg, Microcystis sp., M. aeruginosa females or when frightened, which facilitates short- (Ku¨tzing) Ku¨tzing, Limnothrix redekei (Goor) Mef- distance dispersal. In Schlichting’s (1960) ex- fert, Phormidium sp., Pseudanabaena cf. limnetica, periments, most algae transported externally survived Trachelomonas volvocina (Ehrenberg) Ehrenberg, for 4 h, there were some surviving for 8 h, but Tetraedron sp., Monoraphidium sp., Coelastrum sp., afterward there were hardly any left. Phytoplankton Coenococcus sp., Monoraphidium minutum (Na¨geli) species were found more sensitive to transport than Koma´rkova´-Legnerova´, Gleotila sp., Chlamydomonas others by Schlichting (1960); however, his taxon list sp., Scenedesmus ecornis (Ehrenberg) Chodat, S. includes a number of phytoplankton taxa like Doli- obliquus (Turpin) Ku¨tzing, Chlorella cf. vulgaris, chospermum affine (Lemmermann) Wacklin, L. Hoff- Didymocystis bicellularis (R. Chodat) Koma´rek, mann & Koma´rek, Aphanocapsa, Aphanothece, Rhodomonas lacustris Pascher et Ruttner, Cyclotella Chlorolobion braunii (Na¨geli) Koma´rek, Mono- cf. ocellata, Fragilaria capucina Desmazie`res), in raphidium convolutum (Corda) Koma´rkova´-Leg- experimental tanks exposed in vicinity of a river- nerova´, A. falcatus, Arthrospira, Chlamydomonas, reservoir system providing evidence that over short Closteriopsis, Dactylococcopsis, Euglena gracilis distances, the wind is an important dispersal agent for Klebs, E. minuta Prescott, Franceia, Glenodinium, phytoplankton, including bloom-forming or toxic Mougeotia, Nannochlorys, Oocystis, Planktolyngbya cyanobacteria, with different colonization potentials limnetica, several Oscillatoria spp. recently consid- and sizes (Chrisostomou et al., 2009). ered planktonic, several Scenedesmus spp., Phacus sp., Sphaerocystis schroeterii Chodat and Tetrae¨dron Animals minimum (A. Braun) Hansgirg. Schlichting (1960) observed phytoplankton taxa in Gloeocapsa mucilage Animals may transport phytoplankton on their body and concluded that such algae, apart from their surface, feet, (for birds) toes, or intestines. In guts, mucilage serves for their own protection, may extend desiccation is rather irrelevant, but algae have to resist survival times of other, more sensitive ones. 123 Hydrobiologia (2016) 764:3–27 7

Atkinson (1970, 1971, 1980) experimentally fed 1904). Some bird species like bar-headed geese, may ducks with common species of phytoplankton (Aste- cross severe migration barriers like the Himalaya rionella formosa Hassall, Aulacoseira granulata (Bishop et al., 2015). (Ehrenberg) Simonsen, A. italica (Ehrenberg) Simon- Either transported by wind or externally on sen, Fragilaria crotonensis Kitton, Tabellaria floccu- animals, dormant forms (cysts, akinetes) might appear losa (Roth) Ku¨tzing, T. flocculosa var. actinastroides substantially more resistant to desiccation than vegeta- (Grunow) Knudson, Aphanizomenon flos-aquae) and tive forms. Comparative data are missing, but indirect found that most passed through the guts apparently in evidences provide support: Talling (1951) found a undamaged cells, but not all were cultivable after the correlation between widespread distribution and more passage. In subsequent experiments, in cultivation of resistant resting stages in desmids. Besides its well- material from droppings of ducks, these results were recognized ecological roles (antigrazing feature since largely supported. Resistance of species to digestive it increases size and ‘‘parachute’’ for minimizing enzymes is different as shown by Proctor et al. (1967). sinking loss due to its low specific density; Reynolds, Desmids remained viable for 3–4 h, Pandorina for 2007), production of mucilage might also be an 4h,Pediastrum for 8 h, and oospores of Chara for important adaptation to transport conditions. 24 h. The latter demonstrates that specialized life Some observations in areas located along the main cycle forms (spores, cysts, akinetes) as well as species migration routes of the waterfowl allow supposing that with thick, resistant cell walls will better survive birds are especially efficient vectors. They might be longer transport, either externally or internally, than responsible for the occurrences of tropical species like vegetative forms. Mallomonas portae-ferrae Pe´terfi et Asmund and M. If once the survival capacity of algae (Charalam- cyathellata Wujek et Asmund (Pe´terfi & Momeu, bidou & Santamarı´a, 2002; Figuerola & Green, 2002), 1996;Rˇ eza´cˇova´ et al., 2004) at their known northern- among which phytoplankton, is shown, the next issue most localities. Another example is the increasing to consider is dispersal distance. As apparent in the incidence of tropical phytoplankton species in certain above-cited studies, external survival is no longer than habitats [Planktolyngbya microspira Koma´rek et 8 h, while in intestines, it may reach 24 h. How far Cronberg, P. circumcreta (G.S. West) Anagnostidis animal vectors may travel within this timeframe? et Koma´rek, Cyanodictyon tropicale Senna et Sant’ Bearing in mind that movement distance is very Anna, Staurastrum excavatum var. planctonicum Wil- species-specific, it can be concluded that water beetles li Krieger] in Aquitaine lakes, France (Cellamare (Milliger & Schlichting, 1968) and water-living et al., 2010, 2013) where several long-migrating duck mammals (Maguire, 1963; Roscher, 1967; Ire´ne- species were considered as major carriers. Marie, 1938 cited in Kristiansen, 1996b) can carry algae only from one pond to a nearby one; they are The human vector short distance carriers. These are important to disperse algae among water bodies too small to be visited by There are a number of ways how our recent civilization waterfowl as supposed already by Ralfs (1848) for enhances dispersal including direct and indirect, inten- desmids. Such waters may well be suitable for tional and unintentional actions. We cannot mention phytoplankton and include an increasing number of any case when any phytoplankton species were inten- small garden ponds. tionally introduced to any ecosystem, but unintentional Dragonflies may be very effective vectors introductions are probably very common. Worldwide (Maguire, 1963), but certainly waterfowl are of prior tourism has been an important factor especially toys of importance. Many species of ducks may migrate as far children carried in plastic bags, bath suits rinsed only in as nearly 5000 km, but with many stops. The longest natural waters, and many other measures. non-stop distance was recorded for Anser albifrons Another important agent is the commerce of exotic (Scopoli, 1769) from West Greenland to Scotland. plants and animals. In the latter case, transport Bipolar distributions might be facilitated by non-stop, conditions are optimized for ensuring the survival of N–S migrating species like the south polar skua the intentionally transported biota. (Stercorarius maccormicki Saunders, H. 1893) and the Human actions as landscape engineering and antarctic tern (Sterna vittata georgiae Reichenow, modification of hydrological structures might 123 8 Hydrobiologia (2016) 764:3–27 substantially contribute to dispersal of phytoplankton remains local (Hoffmann, 1996). Phytoplankton spe- species. Reservoir construction was already men- cies have short generation times; thus, development of tioned in the pervious sections. Another action might new genotypes or species must be fast. They are small, be construction of canals between lakes (e.g., Meck- and therefore spread with relative ease. As a result, we lenburg Lake District in Germany; Padisa´k et al., may expect subcosmopolitan distribution for most 2003), which increases connectivity, similarly as phytoplankton species. However, it is not the case, and reservoirs do in arid regions. Construction of orna- at least four observations indicate the relevance of mental and garden ponds has been a controversial dealing with distribution types of phytoplankton: issue. Large areas of wetlands were dredged during the i) There are species thought to be endemic. recent centuries thus shrinking habitats for aquatic ii) Distribution patterns do exist. biota. Many of them may find refuges in ornamental iii) Lack of a species in a whole continent (while ponds (Hamer & Parris, 2011; Goertzen & Suhling, frequent elsewhere) cannot be explained sim- 2013) and the positive impact of such ponds on ply by temperature gradients. enhancing environmental awareness is inevitable. iv) There are ongoing invasions. However, these ponds are often populated by alien plants and fishes and can therefore serve as centers or pathways for radiation of alien species as evidenced in Subcosmopolitan species some cases (Kwik et al., 2013). Studies on phyto- plankton of such ponds are scarce; however, the According to the experience of the authors, if a authors’ personal observation is that they are often phytoplankton ecologist experienced in tropical phyto- dominated by species (e.g., Ankistrodesmus falcatus, plankton flora has to deal with a sample from the Kirchneriella contorta (Schmidle) Bohlin, Elaka- temperate region (or the opposite combination), he or tothrix lacustris Korsikov), which are of minor she will not be at a loss, since at least 70–80% of the flora quantitative importance in lakes with considerable will appear familiar. The case is quite different from that sizes. Plankton nets of biologists might be extremely observed in macrobotany. This common experience efficient dispersers (Talling, 1951). indicates that the relative proportion of subcosmopoli- Dispersal of halophilic species in temperate waters has tan taxa in phytoplankton is high. Species like Micro- been facilitated by winter de-icing of roads and improper cystis aeruginosa, M. wesenbergii (Koma´rek) Koma´rek treatment of industrial sewage (Kasˇtovsky´ et al., 2010). ex Koma´rek, Planktothrix agardhii, and many green Typical examples are some species expanding in the algae indeed have a wide geographic distribution. A twentieth century, like Skeletonema potamos (C.I.We- comparison of typical summer assemblages in temper- ber), Hasler (Duleba et al., 2014), S. subsalsum (Cleve- ate lakes indicates a great overlap with year-round Euler) Bethge, Thalassiosira lacustris (Grunow) Hasle associations in tropical lakes (Reynolds, 2006). Many (Korneva, 2014), and Cuspidothrix issatschenkoi P. species that are restricted to the warmest seasons in Rajaniemi, Koma´rek, R.Willame, P. Hrouzek, K. Kas- temperate zone can be perennial in the tropics [e.g., tovska´, L. Hoffmann & K. Sivonen (Kasˇtovsky´ et al., Urosolenia spp., Aulacoseira granulata var. angustis- 2010). Their success might be enhanced by gradual sima (O.F.Mu¨ller) Simonsen, Cylindrospermopsis raci- adaptation to typical freshwater environments and the borskii]. These species are commonly considered ongoing climate warming (Duleba et al., 2014). subcosmopolitan; however, very few of them are likely to populate polar or subpolar waters. A detailed survey by Vyverman (1996) in the Indo-Malayan region has Geographic distribution types shown that altitudinal gradients also exist: tropical lowland lakes are dominated by subcosmopolitan and Some species are widespread others are local. In the pantropical taxa, and composition of algal communities simplest logical way, it can be explained by contrasting changes markedly along an altitudinal gradient as speed of speciation (evolution of a new genotype) and tropical taxa are gradually replaced by others, charac- speed of dispersal. If the dispersal rate is higher than the teristic for cooler climates. The transition zone was rate of evolution, a subcosmopolitan distribution will between 1700 and 2500 m a.s.l. For example, the be the result; in the opposite case, the distribution typical temperate species, Ceratium hirundinella have 123 Hydrobiologia (2016) 764:3–27 9 been reported only from high mountain lakes in the Limnothrix redekei, Dolichospermumsolitarium Doli- Indo-Malayan region. chospermum solitarium (Klebahn) Wacklin, Hoff- mann et Koma´rek, D. flos-aquae Lyngbye Bre´bisson Pantropical species ex Bornet et Flahault) Wacklin, Hoffmann et Koma´rek, D. lemmermannii (Richter in Lemmer- Temperature is certainly a major selective factor mann) Wacklin, Hoffmann et Koma´rek, Anabaenopsis restricting species to occur within latitudinal bands. arnoldii Aptekar, A. milleri Voronichin, Aphani- For terrestrial biota, frost resistance is an ultimate zomenon flos-aquae, Cuspidothrix issatschenkoi), property shaping geographic distributions. As lakes etc., appear to be restricted to temperate zones rarely freeze from surface to bottom, frost resistance is (Hoffmann, 1996; Vyverman, 1996). Some of these not considered as a major selective constrain for species are found only in relatively warmer latitudes phytoplankton. In addition, it is also shown that some (e.g., C. issatschenkoi). Others are more common only species, like Microcystis viridis, remain viable after in colder temperate regions. An interesting example is being frozen within ice (Vasas et al., 2010). Planktothrix rubescens, which avoids warmer tem- Species occurring only roughly between the two peratures by forming deep chlorophyll maxima during Tropics are called pantropical. Numerous algae are the stratified periods in metalimnia or upper hy- found in this group like all Cylindrospermopsis polimnia of many dimictic lakes in Europe (Dokulil & species (except C. raciborskii), Arthrospira fusiformis Teubner, 2012). Its only certified occurrence in a (Voronikhin) Koma´rek & J. W. G. Lund, Anabaena shallow lake is the one in Hungary where it bloomed in fuellebornii Schmidle, A. iyengarii Bharadwaja, A. November (Vasas et al., 2014). leonardii Compe`re, A. oblonga De Wildeman, An- Some species occur in wide latitudinal range within abaenopsis tanganyikae (G.S. West) Woloszynska & the temperate zone, but there might be several V.V. Miller, Aulacoseira agassizii (Ostenfeld) Simon- phycogeographic regions where they do not occur. sen, A. ikapoensis (Otto Mu¨ller) Simonsen, Schroe- For example, Asterionella formosa has never been deria indica Philipose, Mallomonas bangladeshica (E. reported from the Indo-Malayan region even though Takahashi & T. Hayakawa) Siver & A. P. Wolfe, M. there are many lakes where it, theoretically, could tropica Du¨rrschmidt & Croome, Synura australiensis occur (Vyverman, 1996). Playfair, Ceratium bracyceros Daday, Peridinium Kristiansen & Vigna (1996) found a marked gutwinskii Woloszynaka, etc. (Padisa´k, 2003). bipolarity in geographic distribution of silica-scaled Restriction of these species to the warmest climatic chrysoflagellates with a high degree of similarity regions is, in all probability, related to their phys- between the floras of the climatically comparable iological rates (photosynthesis, respiration, membrane regions of the northern and southern hemispheres. fluidity, kinetics of nutrient uptake, etc.). However, Typical taxa are Mallomonas parvula Du¨rrschmidt, M. little is known about these background mechanisms. paxillata (D.E. Bradley) Pe´terfi & Momeu, M. trans- It is worthy to mention here that temperature, sylvanica Pe´terfi & Momeu, M. cristata Du¨rrschmidt, though apparent, is not necessarily the only designer of M. alata Asmund, Cronberg & Du¨rrschmidt, and M. pantropic distribution patterns. Besides, latitudinally/ alveolata Du¨rrschmidt. altitudinally restricted mixing types such as atelomixis (Barbosa & Padisa´k, 2003) may play a role especially Circumpolar species for species needing deep mixing to remain entrained in the mixed layers. Examples include a number of A rather restricted distributional type characterizes the desmids typical in atelomictic lakes both in tropical occurrence of Cyclotella tripartita Ha˚kansson. This (Borics et al., 2005; Souza et al., 2008) and high species is restricted to latitudes higher than 50° but mountain (Abera & Schagerl, 2015) lakes. only in the northern hemisphere (Scheffler & Padisa´k, 1997) and can be one of the dominant species in the Temperate species, bipolarity spring diatom peak. Such species are northern cir- cumpolar species. Desmids provide another example: Several well-known species (Planktothrix rubescens in contrast to arctic regions, the desmid flora of De Candolle ex Gomont) Anagnostidis & Koma´rek, Antarctica is extremely poor (Coesel, 1996). 123 10 Hydrobiologia (2016) 764:3–27

Occurrence of the southern circumpolar distribution crispa Coute´ & Bouvy in a reservoir in NE Brazil type is not very likely because practically only the (Coute´ & Bouvy 2004); C. catemaco Koma´rkova´- southernmost parts of South America offer climatic Legnerova´ & Tavera in Lake Catemaco, Mexico; conditions for existence of appropriate habitats. (Koma´rkova´-Legnerova´ & Tavera, 1996), and C. Species developing dense population under ice taverae Koma´rek & Koma´rkova´-Legnerova´ in Central during the winter stagnation period provide another Mexico (Koma´rek & Koma´rkova´-Legnerova´, 2002). example of northern circumpolar distributions. Some Nevertheless, there is a newly described species of endemic diatoms of Lake Baikal (see next session for Cylindrospermopsis also from Europe (C. sinuosa detail) belong to this type, and the best known example Coute´, Leita˜o & Sarmento; Coute´ et al., 2004) is probably Stephanocostis chantaicus Genkal & reflecting the fast evolution and radiation of this Kuzmin, a rare, small diatom species occurring only genus. in oligotrophic, calcareous lakes (Scheffler & Padisa´k, Australia, and especially Tasmania, hosts a consid- 2000) with winter ice cover. Its known southernmost erable number of endemic species and genera, includ- occurrence is in Lake Tovel, a cold-water lake at ing among them planktonic algae, called ‘‘flagship’’ 1178 m a.s.l. in N-Italy (M. Cellamare and G. Flaim, taxa by Tyler (1996). Such species are, for example, personal communication). Chrysonephele palustris Pipes, Tyler & Leedale, Prorocentrum playfairi Croome, P. foveolata Regional taxa, endemicity Croome, Thecadiniopsis tasmanica Croome, and Tes- sellaria volvocina Playfair) Playfair. Cyclotella tas- Endemism can have two quite different kinds of manica Haworth & Tyler occurs exclusively in origin: (1) the most pure form of endemism is when a Tasmania, but is widely distributed there (Haworth species evolves at a certain location and remains & Tyler, 1993). exclusive to that location. (2) The so-called relict Lake Baikal has been a hotspot of endemic endemism occurs as a result of habitat fragmentation phytoplankton species, especially diatoms like Aula- or destruction and a subsequent extinction from all coseira baicalensis (K. I. Meyer) Simonsen, and A. localities except one. Distinction is difficult because, skwortzowii (O. Mu¨ller) Haworth, which develop in most cases, no fossils remained. In addition, there is dense populations in spring when the lake has been quite a number of species that, for a long time, have still covered by ice, and it was evidenced by both been known only from the type locality (local paleolimnological and genetic methods that these two endemics), which cannot be considered as real species diverged during the lifetime of the lake endemics as long as floristic surveys in comparable (Popovskaya et al., 2006). habitats in other continents are missing. Peridinium baliense Lindemannmay serve as typical example. The species was described from the material collected Invasions by the Sunda-expedition in the Indo-Malayan islands (Lindemann, 1931) and was thought to be endemic If ‘‘everything is everywhere but environment selects’’ there until it was found in many lakes of the Rio Doce (Baas-Becking, 1934) ‘‘invasions’’ reflect only the Lake District (Brazil), even to the extent of being expansion of certain habitat types. This statement subdominant in one of them (Borics et al., 2005). certainly has to be contrasted to evolution of new Tyler (1996) differentiated between fragile en- genotypes, which may radiate without environmental demics with restricted distribution and robust en- change. Invasions are a major issue in both terrestrial demics that have a wider distribution. For example, and aquatic habitats, especially if invaders are macro- Aphanizomenon manguinii Bourrelly in Bourrelly & scopically visible species or produce phenomena Manguin, Trichormus subtropicus (N. L. Gardner) visible to naked eyes. When invading new areas, Koma´rek & Anagnostidis have so far been recorded phytoplankton species, like all others, are also able to only on several islands in the Caribbean region cause irreversible environmental changes by outcom- (Koma´rek, 1985) similar to many recently described peting native species, changing food-web structures species of Cylindrospermopsis which have so far been (Dufour et al., 2006), or reduce diversity (Borics et al., recorded only in Central America: C. acuminato- 2000, 2012). Reports on invasions by planktonic algal 123 Hydrobiologia (2016) 764:3–27 11 species are strikingly underrepresented in the lit- probably increasing ionic content) or global human erature. Reasons are manifold: activity (Duleba et al., 2014). Examples of global dispersion are rare, with the i) Phytoplankton species cannot be noticed by best-known example being Cylindrospermopsis raci- naked eyes during field trips and samplings, borskii. Its native area has not been known, but and subsequent microscopy work is needed. Padisa´k(1997) guessed it to be Africa since up to the ii) Samples for monitoring purposes are routinely end of the last millennium; this area possessed the fixed by Lugol right after sampling which may highest infrageneric diversity. Later, a number of new destruct some structures necessary for correct species were described from Central America, and identification. therefore, it can be considered as the most probable iii) Many species cannot be identified by light evolutionary centre, as also supported by a phyloge- microscopy either because the cells them- netic study (Moreira et al., 2014). Pantropical origin is selves or the cellular structures important for not questionable (see also Gugger et al., 2005). identification are too small. This species has become a flagship of invasions in iv) Society is largely uninterested in appearance the last two decades. Since the first comprehensive or disappearance of a species, which otherwise review on its distributional area and dispersal was does not make any scandal; therefore no funds published (Padisa´k, 1997), the species was documented are provided for such kind of basic research. in most parts of the word. In Europe, it followed the v) The native flora has to be based on reliably predicted invasion routes from Central Europe toward documented historical data, which are often the northern and western parts like Germany (Mischke, missing. 2001;Stukenetal.,2006), France (Briand et al., 2002; vi) Floristic or good monitoring data from any Druart & Briand, 2002; Cellamare et al., 2010), and macro-region of the world must reach some Poland (Stefaniak & Kokocynski, 2005;Dvora´k& ‘‘critical mass’’ for arriving at the suspicion or Hasler, 2007; Kokocinski & Soininen, 2012;Kobos conclusion that a given species has been et al., 2013); and southward to Mediterranean/sub- invasive. tropical regions including Portugal (Saker et al., 2004), Data fulfilling the last two conditions are available Algeria (Bouaicha & Nasri, 2004), Italy (Mugnai et al., practically only for Europe and, to a certain extent, for 2008; Barone et al., 2010), Tunisia (Fathalli et al., North and South Americas. Nevertheless, tools of 2010), Egypt (Hamed, 2005; Mohamed, 2007), and molecular genetics and metabolomics in exploring Israel (Zohary & Shlichter, 2009;Alsteretal.,2010). phylogeography of phytoplankton taxa (see later) have C. raciborskii was first found in North America in the potential to fill the gaps of non-existent knowledge Kansas, but this remained a solitary record for a long of initial floristic compositions. time (Prescott & Andrews, 1955). During the period For discussing invasions, first of all we need to 1966–1969, Hill (1970) found it in eight small, nearby identify the native area and a reference area toward lakes in Minnesota then Lind (1984) published the which species are invading. Latter might be a biogeo- species from Texas. These scattered data do not allow graphic region (Korneva, 2014), an ecoregion, or a outlining a dispersal route as was possible in Europe. county (Kasˇtovsky´ et al., 2010), or any sensibly Nevertheless, data on the presence of the species have defined geographic unit. Single lake invasions need begun to accumulate in the last 15 years covering some care. If incidence of a species is increasing Florida (Dobberfuhl, 2003), Indiana (Jones & Sauter, within its native distribution area, the species might be 2005), Canada (Hamilton et al., 2005; Kling, 2009), a newcomer in any particular lake, but not invasive. the Great Lakes region (Conroy et al., 2007), and Example can be Skeletonema potamos in Kasˇtovsky´ Louisiana (Rick et al., 2007; Fuentes et al., 2010). et al. (2010): in the first paragraph of the description of However, it remains unknown if series of invasions its history, it is considered cosmopolitan, and in the and extinctions occurred in North America or the second ‘‘non-native distribution in the World’’ is species was permanently present but ‘‘silent’’ as discussed. In such cases, the increase in the number of suggested for New Zealand by Wood et al. (2014). occurrences certainly reflects increase of appropriate Recent expansion of the species in South America habitats as a consequence of some local (in this case, (Vidal & Kruk, 2008; Fabre et al., 2010) and Africa 123 12 Hydrobiologia (2016) 764:3–27

(van Vuuren & Kriel, 2008) toward higher latitudes is (Paulino et al., 2009), Central Italy (Messineo et al., also documented. 2006), Sicily (Naselli-Flores et al., 2007; Naselli- C. raciborskii has been probably the only phyto- Flores, 2014), Greece (Vareli et al., 2009), Turkey plankton species for which dispersal routes could be (Albay et al., 2003; Akcaalan et al., 2007), Poland reconstructed (see Padisa´k 1997 and the above data), (Krupa & Czernas, 2003; Lenard, 2009), and Hungary and the speed of the dispersal could be estimated. (Vasas et al., 2014). Latter is quite fast: less than a century was needed to colonize appropriate habitats all over the world. In accordance with observations on aquatic fauna Biogeography of toxin-producing cyanobacterial (Dumont et al., 2004), available data support a phytoplankton distinguished dispersal corridor through (or from) Central Asia toward west (Europe) and then through- Knowledge of the spatial and temporal distributions of out the Holarctic region. Species involved are cyanobacterial phytoplankton species in the environ- Chrysosporum bergii (Ostenfeld) Zapomelova´, Ska´- ment at local, regional, and continental scales has been celova´, Pumann, Kopp et Janecek (syn: Anabaena still limited, but because of several reasons, a number bergii), Cuspidothrix issatschenkoi, Sphaerospermop- of representatives of the taxa have been in focus of sis aphanizomenoides (Forti) Zapomelova´, Jezberova´, interest in the recent decades (Carmichael, 1992; Hrouzek, Hisem, Reha´kova´ et Koma´rkova´ and Cy- Moreira et al., 2013). clostephanos delicatus (Genkal) Casper (see details in Release of toxins, organoleptic compounds, water Kasˇtovsky´ et al., 2010; Korneva, 2014). discoloration, and accumulation of surface scums by A number of species expand from northern tem- bloom-forming cyanobacterial species can pose seri- perate regions toward south, such as Dolichospermum ous risks in water use and cause problems in economy compactum (Nygaard) Wacklin, Hoffmann et (Reynolds & Walsby, 1975; Neilan et al., 1995). Koma´rek, Gloeotrichia echinulata (J.E. Smith) P.G. Cyanotoxins occur in several genera of cyanobacteria Richter, Staurastrum planktonicum Telling (Kasˇ- and cause human illnesses and death of aquatic tovsky´ et al., 2010), and Gonyostomum semen (Ehren- animals as well as of wild and livestock animals berg) Diesing (Korneva, 2014). Some other species (Carmichael, 1992). These occurrences and conse- prolong eastward within similar latitudinal bands like quences called for research and provide more data on Synechococcus capitatus Bailey-Watts et Koma´rek dispersal of these harmful organisms than those known and Actinocyclus normanii f. subsalsus (Juhlin- for other phytoplankton species (Wilson et al., 2005). Dannfelt) Hustedt (Kasˇtovsky´ et al., 2010). Cyanobacterial toxins are classified as hepatotoxins There are some species with unknown native (microcystins, nodularins, and cylindrospermopsin), distribution area but with the increasing incidence, neurotoxins (anatoxin-a, saxitoxins), and dermal tox- suggesting invasive behavior. Examples are Peridin- ins (lyngbyatoxin, aplysiatoxin) (Chorus & Bartam, iopsis kevei Grigorszky et Vasas and Pleodorina 1999). Their production is not strain specific and can indica (Iyengar) Nozaki (Kasˇtovsky´ et al., 2010; be found in a diverse range of species. Among Korneva, 2014). cyanotoxins, the most widely studied are the hepato- Planktothrix rubescens represents an interesting toxins, microcystins, and cylindrospermopsin (Carmi- case. As described in detail by Kasˇtovsky´ et al. (2010), chael, 1994). the original distribution area covers southern central Microcystins have a worldwide distribution (found Norway and the western alpine area, especially large in all of the main continents) and are produced by a lakes in Switzerland, Austria Italy, Germany, Slove- variety of cyanobacterial genera (e.g., Microcystis, nia, and France (e.g., Barco et al., 2004; Jann-Para Nostoc, Anabaena, Planktothrix) (Chorus & Bartam, et al., 2004; Jacquet et al., 2005; Legnani et al., 2005; 1999). Ernst et al., 2009). Apart from it appears to proliferate Cyanobacterial taxonomy was traditionally based within its original area (Jacquet et al., 2005), increas- only on morphological characteristics examined by ing number of reports provide evidence for its microscopic techniques (Koma´rek, & Koma´rkova´, dispersal both southward and eastward to Spain 2004). Nowadays, molecular tools applied to cyanobac- (Almodo´var et al., 2004; Barco et al., 2004), Portugal teria and cyanotoxin investigations are widely used. 123 Hydrobiologia (2016) 764:3–27 13

These techniques made it possible to investigate gene cluster (mcyA, mcyD, and mcyG) from toxin- phylogenetic comparison of strains from diverse geo- producing M. aeruginosa strains across all the five graphic origins. A number of genetic markers have been continents. Their results provided valuable insight on used in phylogenetic studies in order to assess genetic the biogeography of M. aeruginosa-produced micro- diversity or phylogeographic structure in a given cystins. The Asian strains separated from strains of location (Neilan et al., 1995; Moreira et al., 2013). other continents’ groups as genetically unique popula- Biogeographic studies of toxic cyanobacteria are tions. Asian strains were closer related to European generally based on the comparative discovery of the and North American strains (Moreira et al., 2012) than occurrences of bloom-forming genera or species in to those from other regions. new and well-known environments, and define distinct characteristic toxin patterns and its genetic background Planktothrix of them (Cire´s et al., 2014; Kurmayer et al., 2014). Planktothrix is one of the most important MC-producing Microcystis genera in temperate lakes (Fastner et al., 1999). Of the MC-producing genotypes, the red-pigmented phyco- The most-studied microcystin (MC)-producing genus erythrin (PE)-rich genotypes are assigned to Plank- is the Microcystis. Several results showed that there tothrix rubescens, while the green-pigmented was no correlation between morphotypes and geno- phycocyanin (PC)-rich genotypes are frequently as- types. In addition, a high level of genetic diversity with signed to Planktothrix agardhii (Kurmayer et al., 2005; a high number of genotypes was detected in the genus Kurmayer & Gumpenberger, 2006). In general, Plank- (Bittencourt-Oliveira et al., 2001). Neilan et al. (1995) tothrix rubescens is found in deep, stratified, and oligo- proclaimed that several genetic lineages exist in the to mesotrophic waters in which metalimnetic deep phylogenetic tree of the restriction fragment length chlorophyll maxima can be built up. Planktothrix polymorphism (RFLP) profiles. The heterogeneity of agardhii has a broader distribution and inhabits shallow, the Microcystis genus from several countries is also polymictic water bodies in the mesotrophic to hyper- well established in studies with other genetic markers trophic range (Reynolds & Walsby, 1975). (Kondo et al., 2000; Wilson et al., 2005; El Herry Kurmayer et al. (2014) developed a framework for et al., 2008; Yoshida et al., 2008; Fathalli et al., 2011; an approach of cyanobacterial ecology based on Gaevsky et al., 2011). phylogeny, niche partitioning, and bioactive peptides M. aeruginosa is the most common bloom-forming and used it to address the question of how Planktothrix cyanobacterium species from this genus, which has populations adapt in diverse environments. In their been studied at a phylogeographic level. Studying study, Planktothrix strains isolated from Europe, strains from distinct geographic locations and using the North America, and East Africa were analyzed for 16S rRNA marker, Neilan et al. (1997) revealed a high the presence of the mcy gene cluster, the genetic degree of genetic similarity and concluded first that the variation within seven housekeeping gene loci, and the species has no apparent phylogeographic structure. In occurrence of MC and other bioactive oligopeptides. another work (Bittencourt-Oliveira et al., 2001), the They found that MC and peptide distribution depend- cpcBA-IGS genetic marker was applied for comparing ed on phylogeny, ecophysiological adaptation, and strains isolated from South-America, Europe, North geographic distance. These findings provide evidence America, and Japan. The results were similar: the that MC and peptide production are primarily related studied strains did not appear to form any distinct to speciation processes, while within a phylogenetic geographic pattern. Subsequent studies of Van Grem- lineage, the probability that strains differ in peptide berghe et al. (2011) by sequencing of DGGE bands of composition increases with the geographic distance the 16S-23S ITS marker and Haande et al. (2007) using (Kurmayer et al. 2014). two distinct genetic markers (PC-IGS and 16S-23S ITS) also concluded that, at a biogeographic level, the Cylindrospermopsis raciborskii species can be considered as subcosmopolitan. Moreira et al. (2012) compared phylogenetically The filamentous cyanobacterium C. raciborskii is one the nucleotide sequences of three genes of the mcy of the most notorious cylindrospermopsin (CYN) 123 14 Hydrobiologia (2016) 764:3–27 producers and can be found in freshwater habitats in raciborskii strains from Tunisia. The phylogeography the temperate, tropical, subtropical regions of the depicted by this study may indicate that, either world (Moreira et al., 2011). different C. raciborskii genotypes/ecotypes occur Dyble et al. (2002) compared C. raciborskii strains inside Europe, as has already been observed inside from Europe, Australia, and America by means of two America and Africa, or American and Spanish distinct genetic markers (nifH and cpcBA-IGS), and populations have undergone a relatively recent they were able to differentiate only the American transoceanic exchange by transport of trichomes or isolates. Neilan et al. (2003) published the phylogeog- akinetes by migratory birds or human activities (Cire´s raphy of this species based on information from the et al., 2014). 16S rRNA and cyanobacteria HIP1 PCR profiles. They This species is of major concern from a water- established that the 16S rRNA marker does not allow a quality and public health perspective due to its known good differentiation of the strains. Two major groups ability to produce different types of toxins at different were defined by the HIP1 PCR profiles that distinctly parts of the world, including the potent hepatotoxic separated the American strains from the European and alkaloid CYN, the highly toxic paralytic shellfish Australian strains. They concluded that in the Europe/ poisons (PsP) and an unidentified toxin with atypical Australia group there was a high degree of genetic toxicity (Moreira et al., 2011). CYN-producing strains divergence. were reported only from Australia, Asia, and New Based on information from the 16S-23S ITS Zealand, and strains producing saxitoxins were only marker, Gugger et al. (2005) showed that three main found in South America. The increasing number of clusters existed for this species: Europe, America, and reports on C. raciborskii in temperate regions justifies Australia/Africa. They suggested invasion of C. the toxicological studies of European strains (Moreira raciborskii from warm refuge areas on each continent. et al., 2013). Haande et al. (2008) published a work using C. Based on a pharmacological data, Vehovszky et al. raciborskii from four continents utilizing 16S-23S (2013) concluded that the cholinergic inhibitory ITS-L, nifH, and PC-IGS genetic markers in a effects of both a Hungarian bloom sample (Fancsika multigene analysis. Three distinct clusters were con- pond) and the isolated C. raciborskii strain suggest the structed, with the strains of Africa being closer to the presence of some yet unidentified anatoxin-a like Australian strains, the American strains being more neurotoxin(s). This suggestion corresponds with pre- divergent and the European strains being closer to the vious pharmacological data regarding another C. Australian/African group (Haande et al., 2008). Based raciborskii sample isolated from Lake Balaton in on the phylogenic, morphological, and toxicologic 1995 (Kiss et al., 2002; Vehovszky et al., 2012). data, they suggest that the spread of this species would Therefore, present knowledge suggests that the have been rather through radiation within continents cholinergic neurotoxic metabolite(s) producing than by recent exchange between continents. In a four- chemotype of C. raciborskii might be quite widely genetic marker (16S rRNA, 16S-23S ITS-L, 16S-23S distributed in this region. ITS-S rRNA, and rpoC1) analysis, Moreira et al. Although the cylindrospermopsin was named from (2011) identified three main clusters at a global scale: the genus Cylindrospermopsis, Aphanizomenon oval- Europe, Australia/Asia, and America/Africa and pro- isporum Forti (characterized by its genetic homogene- posed that Europe was probably colonized by strains ity worldwide) can be considered the main CYN from the Asian or Australian continents in accordance producer to date in subtropical and tropical areas of with dispersal route analysis based on floristic data Australia, the United States (Florida), Israel, and the (Padisa´k, 1997), suggesting colonization of Europe Mediterranean Europe (Cire´s et al., 2014). starting from Australia through Asia. The ITS1-L tree constructed by Cire´s et al. (2014) Nodularia confirmed that a Spanish strain (C. raciborskii UAM 544) was clearly separated from the rest of the The genus Nodularia (Nostocales) consists of filamen- European strains (from France, Germany, Hungary, tous, heterocytous, nitrogen-fixing, potent nodularin- and Portugal) and grouped very close to American producer cyanobacteria, which are found in brackish- strains, together with two other Mediterranean C. and freshwaters, as well as in terrestrial environments, 123 Hydrobiologia (2016) 764:3–27 15 worldwide. Nodularia strains were analyzed at a local than comparable smaller ones have) is considered the scale in the Baltic Sea, where blooms are common in most robust rule in ecology (Schoener, 1976). The late summers and may cover areas in excess of relationship has been demonstrated for almost all 60,000 km2 (Bolch et al., 1999). terrestrial macroscopic systems, but aquatic and In the study of Hayes & Barker (1997), population especially microscopic examples are seriously under- structure was determined for the Nodularia strains represented in the literature (Horner-Devine et al., isolated from nine sampling areas in the Baltic Sea, 2004). It is really surprising, because lakes, ponds, and and revealed the presence of two distinct genotypes pools can be considered as aquatic ‘islands’ in a that were spatially unequally distributed. terrestrial landscape (De Meester et al., 2005), and At a global scale, a worldwide comparison of thus, may serve as model systems for studying SARs Nodularia strains was conducted. In the work of Bolch or other island biographic theories (Borics et al., et al. (1999), by PCR–RFLP, RAPD, and PC-IGS 2015). The low number of studies dealing with DNA sequencing, clustering revealed that the Aus- microbial biogeographic patterns can be explained tralian Nodularia strains were distinct from the other by two major methodological difficulties: how to locations worldwide (Europe and North America). define species and how to standardize the sampling and sample-processing efforts. As regards the defini- Dolichospermum circinalis tion of species, algae are in privileged position because, in contrast to bacteria or fungi, most algae Blooms of the nitrogen fixing filamentous cyanobac- can reliably be identified by their visible morpho- terium Dolichospermum (Anabaena) circinalis are logical features. Regarding the sampling and sample- well known due to their production of neurotoxins as processing techniques commonly applied in lim- anatoxin-a and paralytic shellfish poisons (PSPs). nology, one can say that these techniques are well Beltran and Neilan (2000) identified a geographic elaborated, practically standardized. However, this is segregation of neurotoxin production in the D. circi- only partly true. During a conventional sample nalis, which has a worldwide distribution and blooms processing, approximately 400 units are counted. This frequently all over the world. They proclaimed that the number can be large enough to describe the basic American and European isolates of D. circinalis composition of the communities, but it is not sufficient produce only anatoxin-a, while Australian isolates to describe the overall richness or to deal with rarity produce exclusively PSPs. The reason for this geo- (Padisa´k et al., 2010). The number of captured species graphic segregation of neurotoxin production by D. is largely determined by the taxa distribution within circinalis has been unrevealed. In the same study, the the investigated communities (Chao & Jost, 2012). In phylogenetic structure by 16S rRNA gene sequences case of small-diversity assemblages, only a small of D. circinalis suggested a monophyletic group with portion of the species pool is captured, while in high- worldwide distribution; however, the PSP- and non- diversity communities where taxa are more or less PSP-producing D. circinalis formed two distinct 16S evenly distributed, the rate of captured species is rRNA gene clusters (Beltran & Neilan, 2000). considerably higher (Fig. 1). The above difficulties do not mean that island biogeographic theories cannot be tested and applied Outlook and perspectives for algae. Smith et al. (2005) demonstrated that if the SAR for algae is investigated along a large spatial Island biogeography and associated species–area scale (from laboratory microcosms to the oceans), the relations for algae relationship, similar to macroscopic systems, could be described by the well-known power model (Arrhenius, Besides the classical question of what the geographic 1921). Unlike this result, a slight linear relationship distribution of a given taxa is, biogeography addresses was found between lake area and phytoplankton several other space-related questions. Most of these species richness for lakes in the United States (Stomp are associated to island biogeography and area– et al., 2011). Up to now, these two studies are the only richness relationships. The species–area relationship ones that have documented relationships between lake (SAR) (i.e., large habitats typically have more species area and algal richness, which implies that this 123 16 Hydrobiologia (2016) 764:3–27

a recent review by Salmaso et al., 2015). Consequent- ly, only the FG method has to be considered in context of biogeography. Sorting species to FGs is a pooling method, and biogeographic studies need an opposite approach: separating not only species, but in many cases, strains or chemotypes. A species that occurs very rarely has no or little effect on any conclusion that comes from FG analyses, but single records can be crucial for biogeography considerations. The only consequence here is that the species-specific data required by the FG approach allow for different types of analyses in contrast to either the MFG or the MBFG methods, and the original counting protocols must be carefully documented and saved. Even if species are identified at the possible highest accuracy, doubts may arise. Three well-known species are easy to allocate formally to FG-s: Cylindrosper-

mopsis raciborskii to SN, Raphidiopsis mediterranea Skuja to S1 and Cuspidothrix issatschenkoi to H1. Although results of some molecular studies have not been consolidated yet, they allow supposing quite serious difficulties. In a study by Moustaka-Gouni et al. (2009), Raphidiopsis mediterranea was shown to be a life-cycle stage of Cylindrospermopsis raci- borskii, while Hodoki et al. (2012) defined at least some strains of Raphidiopsis mediterranea as eco- types of non-heterocytous Cuspidothrix issatschenkoi. Formal logics lead to the identities of Cylindrosper- mopsis raciborskii and Cuspidothrix issatschenkoi Fig. 1 Number of taxa encountered in theoretical samples of that would hardly be accepted by taxonomists. This different diversities using the traditional sampling processing case exemplifies difficulties arising from our incom- techniques plete knowledge of phylogeny, value of morpho- logical markers, and in interpretation of results by research field is only at its infancy and requires phylogenetic and chemotaxonomic results. additional investigations. Interpretation of phylogenetic and toxicological Biogeography of phytoplankton versus functional results in biogeographic studies grouping There is no doubt that the widely used molecular tools One of the most recent trends in phytoplankton applied to cyanobacteria and cyanotoxin investiga- ecology is explaining community responses to chang- tions help us solve many problems in the taxonomy, ing environments by means of functional grouping of phylogeny, and biogeography of this group (Neilan taxa. Three such methods are offered and widely used et al., 1995; Moreira et al., 2013; Kurmayer et al., (FG: Reynolds et al., 2002; MFG: Salmaso & Padisa´k, 2014). However, we face a number of controversies. 2007; and MFBG: Kruk et al., 2010). An often-cited For example, some species were shown to have a advantage of the MFG and MBFG methods is that they definite spatial distribution in several studies, while in do not need species-specific identifications, and another, it was defined as a subcosmopolitan group therefore a high level of taxonomic competence (see (Moreira et al., 2013).

123 Hydrobiologia (2016) 764:3–27 17

The methods for biogeographic studies in The need for more ecophysiology cyanobacteria and cyanotoxins are based on the identification and subsequent phylogenetic analyses Incomplete knowledge in ecophysiology raises sub- of the isolates or environmental samples using prede- stantial difficulties in understanding distribution pat- termined genetic markers to establish their genetic terns as can be distilled from the below three diversity and geographic interaction (Neilan et al., examples. 2003; Moreira et al., 2012). However, care is needed in As mentioned afore and evidenced by several studies selection of appropriate genetic marker(s). By using (e.g., Kasˇtovsky´ et al., 2010), winter de-icing of roads more than one genetic marker, the accuracy and and release of insufficiently treated industrial sewage reliability of the phylogenetic inference is increased along with the increasing aridity experienced or fore- since more genetic information can be analyzed. This seen at some regions due global climate change open approach often results clear agreement between all the niche to proliferation of salt-tolerant, brackish taxa. applied markers, but in other cases causes contradic- Species in mesohaline environments might be especial- tory relationships, which call for further analyses and ly important since many become potentially invasive as methods to resolve the contradiction (Moreira et al., a consequence of these changes. Up to now, almost 2013). nothing is known about response of these species to Till now, nearly 100 genomes from cyanobacterial overall salinity changes or simply to changes in ionic strains have been sequenced. These genomes and new composition at the same salinity level. Our recent partial and complete sequences of cyanobacterial experiments allow supposing different effect–response DNA are accessible through databases sufficing the patterns along salinity and ionic composition gradients, growing use of molecular methods in cyanobacteria and this area of research needs a lot more attention. and cyanotoxin research. Before we assign molecular Ceratium hirundinella served as a model species in genetics and/or metabolomics data to a sample/ the 1970s–1980s to understand a single species’ success organism, proper identification becomes inevitable. (e.g., Heaney & Talling, 1980). The species has a quite Omitting it and ignoring morphological criteria-based conservative ontogenetic cycle: vegetative cells encyst microscopic techniques and/or the judgment of an when water temperature falls below some 16–18°C experienced observer may lead to false results, wrong during autumnal cooling; spend a maturation period of conclusions, and inappropriate references in the 4–5 months in the sediments; and then excystment database. That is why before we completely buried starts at temperatures exceeding 6°Casshownin the classical approaches, it is crucial to mention the laboratory studies by Rengefors & Andersen (1998). importance of the appropriate documentation or, if it is Although perennial behavior of C. hirundinella has possible, to define the voucher specimen in a been documented in many reservoirs in the Mediter- molecular-approach-relating phytoplankton study. ranean region (Pe´rez-Martı´nez & Sa´nchez-Castillo, As previously mentioned, phytoplankton species or 2001), the ongoing invasion of the species in South genera with interesting properties or phenomena (like America calls for research concerning conditions of the bloom-forming or toxin production) provide more data dormant period and the possible evolution of a different on dispersal of these organisms than those known for ecotype. In general, more attention is needed to other phytoplankton species. For this reason, it is understand role of dormant stages, also in other groups worthy to take into account these observations even if (Cire´setal.,2013). our knowledge of the phytoplankton metabolom has Defining ranges of environmental variables from been very incomplete (Kurmayer et al., 2014). field studies and comparing them to the presence or Due to the growing use of new generation-sequenc- abundance of a given taxon have been a widely ing methods and high-performance analytic instru- distributed practice in defining habitat preferences or ments, a large amount of genomic and metabolomic explaining geographic distributions (e.g., Padisa´k 1997; data can be expected from the phytoplankton research. Scheffler & Padisa´k 1997, 2000). It is implicit in these The proper evaluation and combination of the results studies that species are supposed to have an optimum in of traditional and modern techniques and monitoring their frequency distribution along each single environ- could be an acceptable way in phytogeographic mental gradient. A recent study, however, did clearly research over the next period. show that optima of essential environmental factors 123 18 Hydrobiologia (2016) 764:3–27 might depend on each other. For example, the minimum level) of alkaline phosphatases produced in response required light for attaining maximum photosynthetic to P limitation and lack (or low level) of carbon rates of Aphanizomenon flos-aquae depended on tem- anhydrases enabling the use of HCO3 as inorganic perature in laboratory studies allowing high level of carbon source prevents them of occurring in substan- shade tolerance at low temperatures in contrast to high tial amounts in waters with pH higher than about 7.5, temperatures when light demand was much higher but in return, they are potentially mixotrophic (Sand- (U¨ veges et al., 2012). This physiological plasticity of gren, 1988; Maberly et al., 2009). ‘‘Appropriate’’ lakes this species allows it to bloom either in mixed layers in are well represented in cold-temperate climates with summer or under ice in winter; therefore, environmental granitic bedrock. Their island-like occurrence in areas field data are rather useless to understand its ecological with dominantly calcareous bedrocks is also well preferences even along the two simplest (light and known and can be easily explained by edaphic reasons. temperature) gradients. Most such ecological islands appear as biodiversity hotspots for this group (e.g., Pe´terfi & Momeu, 1996; Which group is good for what? Pe´terfi et al., 1998, 2002; Barreto, 2005). The number of known species of silica-scaled Reading the above sections of this review, it is chrysophytes has been approximately in the range of apparent that our knowledge on biogeography of 250–300. Taxonomy is based on well-defined silica phytoplankton is fragmented. There are groups, like structures needing EM technique, and allowing archiv- cyanoprokaryotes and especially their potentially ing of samples. Although coupling species and cysts toxic species with sufficient data for generalization; have been among the unresolved issues concerning other higher taxa (like diatoms) are represented only chrysophytes in general, most importantly they do have by some examples (Duleba et al., 2014). There are cysts enabling survival of temporal dry conditions and groups with apparent importance in ecosystem studies overland transport. As discussed above, species with (like cryptophytes or coccal green algae) but without well-defined geographic distributions, including cir- almost any knowledge of their geographic distribu- cumpolar, pantropic, and bipolar, are known. tions. Without going into details of difficulties arising The above properties qualify silica-scaled flagel- from fluid taxonomy in some groups (the ever- lates an ideal model group for studying biodiversity increasing number of diatom taxa or results from issues. Because of obligate use of EM and ignorance of genomics revolutionizing taxonomy of green algae; their typical habitats, for example, by size limits of the Krienitz & Bock, 2012), one may wonder if there is Water Framework Directive in many regions, targeted any higher taxonomic group of planktonic algae more research is necessary. suitable for biogeographic studies than others. Theo- retical requirements are relatively easy to outline: Middle-scale ecoregional differences high, but not extraordinarily high species number with dominantly planktonic species; relatively clear fea- The agents that play crucial role in the formation of tures for sufficiently correct taxonomic identifications; lake basins usually act in geographically well-delin- sufficient dispersal capacity; and global distribution at eated areas, and create hundreds of lakes of similar group level. It is not a matter of chance that Jørgen type. Examples are the glacial lakes in the boreal Kristiansen, the worldwide-acknowledged expert of region, or the shallow deflation lakes in the arid and silica-scaled flagellates organized the first focussed semiarid regions of the world (Hammer, 1986; Wetzel, discussion on biogeography of freshwater algae 2001). Phytoplankton composition of these lakes show (Kristiansen, 1996a), since this group seems to fulfil similar characteristics both at functional and taxo- most criteria raised above. nomic level. Dominance of cryptomonads and chry- Silica-scaled flagellates are invariantly grouped to sophytes in the boreal lakes (Lepisto¨ & Rosenstro¨m, functional group E and X(Ph), and the habitat tem- 1998) and dominance of meroplanktonic diatoms in plate is defined as usually small, shallow, base-poor the very shallow wind-affected lakes of the arid lakes, or heterotrophic ponds (Reynolds et al., 2002) regions (Hecky & Kilham, 1973; Iltis, 1993; Padisa´k including temporary ones. They do not occur in lakes & Dokulil, 1994; Wen et al., 2005) are published in the with high-wind-induced kinetics. The lack (or low literature. However, within these large-scale patterns 123 Hydrobiologia (2016) 764:3–27 19 the climatic constraints of the regions result in middle- in trophic conditions have been considered to be of or small-scale differences in the distribution of major importance worldwide. organisms. Weyhenmeyer et al. (2013) demonstrated It is documented in many studies, that as P-load is latitudinal differences in the phytoplankton diversity exceeding a certain level, ecosystemic need for inor- in Swedish lakes. Comparing the phytoplankton of ganic N arises giving chance to heterocytic European Nordic lakes, Marttunen et al. (2006) found cyanoprokaryotes to appear and fulfil this functional considerable differences in the phytoplankton com- gap. It was exemplified in Lake Balaton (Padisa´k& position and biomass between the Finnish and Reynolds, 1998) that species that appear in such cases Swedish lakes. The shallow lakes in the Carpathian are interestingly mostly those which have an original Basin are especially sensitive to changes in precipita- distribution area in at least relatively warm climates tion and evaporation, more so than lakes of similar (Cylindrospermopsis raciborskii, Raphidiopsis type in the Western part of Europe where higher mediterranea, Cuspidothrix issatschenkoi, etc.). Floris- precipitation and regular flushing coincide with lower tic and vegetational changes, consequent upon the nutrient load. Because of these climatic differences, opposite trend (oligotrophication), have received much Borics et al. (2014) highlighted that lakes in the less attention probably because the newly appearing lowland of the Carpathian Basin should be considered species were not considered harmful or managers as the Westernmost representatives of the Eurasian considered compositional changes as insignificant steppe lakes which spread along a line of *7000 km details compared to TP or chlorophyll-a decrease. Data from Central Europe to Eastern part of continental are sporadic but interesting. In Lake Balaton, species Asia. (Dolichospermum compactum and Aphanizomenon Differences in the phytoplankton composition of gracile (Lemmermann) Lemmermann) with original European lakes are seriously considered in lake distribution at cold temperate climates appeared. management. Comparisons of the methods used for Abundant increase of Mougeotia sp. in lakes that ecological state assessment of the lakes are organized underwent successful eutrophication management in Geographical Intercalibration Groups (Van de Bund (Tapolczai et al., 2014) represents an exception since et al., 2004) in which regions of similar climatic this species is a troublemaker (clogging nets, etc.). conditions are merged, and thus, should be considered Whether Mougeotia simply proliferates or is invasive as European Lake Ecoregions. The ecoregional dif- cannot be decided as long as exact taxonomic identity ferences have been expressed both in different has remained unknown. More attention on floristic biomass boundaries (Poikane et al., 2010) and various changes after remediation would substantially increase compositional metrics applied by the member states knowledge on biogeographic issues. for quality assessment (Carvalho et al., 2013). Regarding the phytoplankton, revealing biogeo- graphic differences which are not solely artifacts of the General conclusion differences in lake-use or use of the watershed is a really challenging task, considering that water pollu- Although biogeography is one of the most important tion overrides differences in the natural compositional historical branches of biological science, spatial of phytoplankton in lakes belonging to different distribution patterns of microscopic organisms, in- geographic regions. Therefore, we conclude that cluding phytoplankton, have been still poorly known. studying small-scale biogeographic differences in This review considered a number of issues related to phytoplankton distribution, combination of the analy- distribution and dispersal of phytoplankton species; sis of recent patterns, and paleolimnological approach- however, the development of a more generalized view es are needed. needs (i) increasing the accuracy of species identifi- cation with traditional microscopic methods; (ii) more Eutrophication–oligotrophication in view research using new generation sequencing and multi- of biogeography gene approach in molecular studies; (iii) careful selection of species or groups that appear more Although floral change or change of planktonic suitable for phycogeographic studies than others; (iv) vegetation may have a number of reasons, changes more attention to species–area relationships including 123 20 Hydrobiologia (2016) 764:3–27 focus on spatial processes in distribution of phyto- in a Spanish drinking water reservoir by LC/ESI-MS. plankton, and (v) a much greater effort to understand Toxicon 44: 881–886. Barone, R., G. Castelli & L. Naselli-Flores, 2010. Red sky at ecophysiological adaptations. night cyanobacteria delight: the role of climate in struc- turing phytoplankton assemblage in a shallow, Mediter- ranean lake (Biviere di Gela, southeastern Sicily). Hydrobiologia 639: 43–53. References Barreto, S., 2005. The silica-scaled chrysophyte flora of Hun- gary. Nova Hedwigia Beiheft 128: 11–41. Beltran, E. C. & B. A. Neilan, 2000. Geographical segregation Abera, F. D. & M. Schagerl, 2015. The phytoplankton com- of the neurotoxin-producing cyanobacterium Anabaena munity of tropical high-mountain crater Lake Wonchi, circinalis. Applied and Environmental Microbiology 66: Ethiopia. Hydrobiologia. doi:10.1007/s10750-015-2233-1. 4468–4474. Abonyi, A., M. Leita˜o, A.-M. Lancon & J. Padisa´k, 2012. Bishop, C. M., R. J. Spivey, L. A. Hawkes, N. Batbayar, B. Phytoplankton functional groups as indicators of human Chua, P. B. Frappell, V. K. Milsom, T. Natsagdorj, S. impacts along the River Loire (France). Hydrobiologia H. Newman, G. R. Scott, J. Y. Takekawa, M. Wikelski & P. 698: 233–249. J. Butler, 2015. The roller coaster flight strategy of bar- Abonyi, A., M. Leita˜o, I. Stankovic´, G. Borics, G. Va´rbı´ro´ &J. headed geese conserves energy during Himalayan migra- Padisa´k, 2014. A River Loire (France) survey to compare tions. Science 347(6219): 250–254. three frequently used phytoplankton functional classifica- Bittencourt-Oliveira, M. C., M. C. Oliveira & C. J. S. Bolch, tions. Do they reflect longitudinal processes in similar 2001. Genetic variability of Brazilian strains of the Mi- ways? Ecological Indicators 46: 11–22. crocystis aeruginosa complex (Cyanobacteria/Cyanophy- Akcaalan, R., M. Albay, C. Gu¨revin & F. C¸ evik, 2007. The ceae) using the phycocyaninin tergenic spacer and flanking influence of environmental conditions on the morpho- regions (cpcBA). Journal of Phycology 37: 810–818. logical variability of phytoplankton in an oligo-me- Bolch, C. J. S., P. T. Orr, G. J. Jones & S. I. Blackburn, 1999. sotrophic Turkish lake. Annales de Limnologie- Genetic, morphological and toxicological variation among International Journal of Limnology 43: 21–28. globally distributed strains of Nodularia (Cyanobacteria). Albay, M., R. Akcaalan, H. Tufekci, J. S. Metcalf, K. A. Beattie Journal of Phycology 35: 339–355. & G. A. Codd, 2003. Depth profiles of cyanobacterial Borics, G., I. Grigorszky, S. Szabo´ & J. Padisa´k, 2000. Phyto- hepatotoxins (microcystins) in three Turkish freshwater plankton associations in a small hypertrophic fishpond in lakes. Hydrobiologia 505: 89–95. East Hungary during a change from bottom-up to top-down Almodo´var, A., G. G. Nicola & M. Nuevo, 2004. Effects of a control. Hydrobiologia 424: 79–90. bloom of Planktothrix rubescens on the fish community of Borics, G., I. Grigorszky, J. Padisa´k, F. A. R. Barbosa & Z. a Spanish reservoir. Limnetica 23: 167–178. Z. Doma, 2005. Dinoflagellates from tropical Brazilian Alster, A., R. N. Kaplan-Levy, A. Sukenik & T. Zohary, 2010. lakes with description of Peridinium brasiliense sp. nov. Morphology and phylogeny of a non-toxic invasive Algological Studies 118: 47–61. Cylindrospermopsis raciborskii from a Mediterranean Borics, G., G. Va´rbı´ro´, I. Grigorszky, E. Krasznai, S. Szabo´ &K. Lake. Hydrobiologia 639: 115–128. T. Kiss, 2007. A new evaluation technique of potamo-plank- Arrhenius, O., 1921. Species and area. Journal of Ecology 9: ton for the assesment the ecological status of rivers. Archiv fu¨r 95–99. Hydrobiologie, Supplement Large Rivers 161: 465–486. Atkinson, K. M., 1970. Dispersal of phytoplantkton by ducks. Borics, G., B. To´thme´re´sz, B. A. Luka´cs & G. Va´rbı´ro´, 2012. Wildfowl 21: 110–111. Functional groups of phytoplankton shaping diversity of Atkinson, K. M., 1971. Further experiments in dispersal of shallow lake ecosystems. Hydrobiologia 698: 251–262. phytoplankton by birds. Wildfowl 22: 2. Borics, G., B. A. Luka´cs, I. Grigorszky, Z. La´szlo´-Nagy, L. Atkinson, K. M., 1980. Experiments in dispersal of phyto- G-To´th, A´ . Bolgovics, S. Szabo´,J.Go¨rge´nyi & G. Va´rbı´ro´, plankton by ducks. British Phycological Journal 15: 49–58. 2014. Phytoplankton-based shallow lake types in the Atkinson, K. M., 1988. The initial development of net phyto- Carpathian basin: steps towards a bottom-up typology. plankton in Cow Green Reservoir (Upper Teesdale), a new Fundamental and Applied Limnology 184: 23–34. impoundment in northern England. In Round, F. E. (ed.), Borics, G., B. To´thme´re´sz, G. Va´rbı´ro´, I. Grigorszky, A. Algae and the Aquatic Environment. Biopress, Bristol: Cze´bely & J. Go¨rge´nyi, 2015. Functional phytoplankton 30–40. distribution in hypertrophic systems across water body Baas-Becking, L. G. M., 1934. Geobiologie of inleiding tot de size. Hydrobiologia. doi:10.1007/s10750-015-2268-3. milieukunde. van Stockum and Zoon, The Hague: 263 pp. Bouaicha, N. & A. B. Nasri, 2004. First report of cyanobac- Barbosa, F. A. R. & J. Padisa´k, 2003. The forgotten lake terium Cylindrospermopsis raciborskii from Algerian stratification pattern: atelomixis, and its ecological im- freshwaters. Environmental Toxicology 19: 541–543. portance. Verhandlungen der Internationale Vereinigung Bowling, L. C. & P. D. Baker, 1996. Major cyanobacterial fu¨r theoretische und anewandte Limnologie 28: bloom in the Barwon-Darling River, Australia, in 1991, 1385–1395. and underlying limnological conditions. Marine and Barco, M., C. Flores, J. Rivera & J. Caixach, 2004. Determi- Freshwater Research 47: 643–657. nation of microcystin variants and related peptides present Briand, J. F., C. Robillot, C. Quiblier-Lloberas, J. F. Humbert, in a water bloom of Planktothrix (Oscillatoria) rubescens A. Coute & C. Bernard, 2002. Environmental context of 123 Hydrobiologia (2016) 764:3–27 21

Cylindrospermopsis raciborskii (Cyanobacteria) blooms in Coute´, A. & M. Bouvy, 2004. A new species of the genus a shallow pond in France. Water Research 36: 3183–3192. Cylindrospermopsis, C. acuminato-crispa spec.nova Bustamante,G.C.R.J.J.,A.BoltovskoyRamı´rez & A. Vallejo, (Cyanophyceae, Nostocales) from Ingazeira reservoir, 2012. Spatial and temporal change characterization of Cer- Northeast Brazil. Algological Studies 113: 57–72. atium furcoides (Dinophyta) in the equatorial reservoir Rio- Coute´, A., M. Leitao & H. Sarmento, 2004. Cylindrospermopsis grande II, Colombia. Acta Limnologica Brasiliensia 24: sinuosa spec.nova (Cyanophyceae, Nostocales), une nuo- 207–219. velle espece du sud-ouest de la France. Algological Studies Carmichael, W. W., 1992. Cyanobacteria secondary metabolites 111: 1–15. – the cyanotoxins. Journal of Applied Bacteriology 72: Darwin, C., 1839. Journal of Researches in the Geology and 445–459. Natural History of the Various Countries Visited by H. Carmichael, W. W., 1994. The toxins of cyanobacteria. Scien- M. S. Beagle. Henry Colburn, London: 615 pp. tific American 270: 78–86. De Meester, L., S. Declerck, R. Stoks, G. Louette, F. Van de Carvalho, L., S. Poikane, A. Lyche Solheim, G. Phillips, G. Meutter, T. De Bie, E. Michels & L. Brendonck, 2005. Borics, J. Catalan, C. De Hoyos, S. Drakare, B. J. Dudley, Ponds and pools as model systems in conservation biology, M. Ja¨rvinen, C. Laplace-Treyture, K. Maileht, C. ecology and evolutionary biology. Aquatic Conservation: McDonald, U. Mischke, J. Moe, G. Morabito, P. Noges, T. Marine and Freshwater Ecosystems 15: 715–725. Noges, I. Ott, A. Pasztaleniec, B. Skjelbred & S. Dijoux, L., F. Viard & C. Payri, 2014. The more we search, the more J. Thackeray, 2013. Strength and uncertainty of phyto- we find: discovery of a new lineage and a new species complex plankton metrics for assessing eutrophication impacts in in the genus Asparagopsis. PLoS One 9(7): e103826. lakes. Hydrobiologia 704: 127–140. Dobberfuhl, D. R., 2003. Cylindrospermopsis raciborskii in Cavalcante,K.P.,J.C.Zanotelli,C.C.Mu¨ller, K. D. Scherer, J. three Central Florida Lakes: population dynamics, con- K. Frizzo, T. A. V. Ludwig & L. de Souza Cardoso, 2013. First trols, and management implications. Lake and Reservoir record of expansive Ceratium Schrank, 1793 species (Dino- Management 19: 341–348. phyceae) in Southern Brazil, with notes on their dispersive Dokulil, M. & K. Teubner, 2012. Deep living Planktothrix patterns in Brazilian environments. Check List 9: 862–866. rubescens modulated by environmental constraints and Cellamare, M., M. Leita˜o, M. Coste, A. Dutartre & J. Haury, climate forcing. Hydrobiologia 698: 29–46. 2010. Tropical phytoplankton taxa in Aquitaine lakes Druart, J. C. & J. F. Briand, 2002. First record of Cylindros- (France). Hydrobiologia 639: 129–145. permopsis raciborskii (Woloszynska) Seenayya et Subba Cellamare, M., P. Tezanos Pinto, M. Laita˜o, M. Coste, S. Bontry Raju (Cyanobacteria) in a lotic system in France. Annales & J. Haury, 2013. Using functional approaches to study de Limnologie. International Journal of Limnology 38: phytoplankton communities in a temperate region exposed 339–342. to tropical species dispersal. Hydrobiologia 702: 267–282. Dufour, P., G. Sarazin, C. Quiblier, S. Sane & C. Leboulanger, Chao, A. & L. Jost, 2012. Coverage-based rarefaction and ex- 2006. Cascading nutrient limitation of the cyanobacterium trapolation: standardizing samples by completeness rather Cylindrospermopsis raciborskii in a Sahelian lake (North than size. Ecology 93: 2533–2547. Senegal). Aquatic Microbial Ecology 44: 219–230. Charalambidou, I. & L. Santamarı´a, 2002. Waterbirds as en- Dumont, H. J., 1999. The species richness of reservoir plankton dozoochorous dispersers of aquatic organisms: a review of and the effect of reservoirs on plankton dispersal (with experimental evidence. Acta Oecologica 23: 165–176. special emphasis on rotifers and cladocerans). In Tundisi, J. Chorus, I. & J. Bartam, 1999. Toxic Cyanobacteria in Water – A G. & M. Straskraba (eds), Theoretical Reservoir Ecology. Guide to Their Public Health Consequences, Monitoring Backhuys Publishers, Leiden: 505–528. and Management. E & FN Spon, London. Dumont, H. J., T. A. Shiganova & U. Niermann, 2004. Aquatic Chrisostomou, A., M. Moustaka-Gouni, S. Sgardelis & T. La- Invasions in the Black, Caspian, and Mediterranean Seas. naras, 2009. Air-dispersed phytoplankton in a Mediter- Kluwer Academic Publishers, Dordrecht. ranean river-reservoir system (Aliakmon-Polyphytos, Duleba, M., L. Ector, Z. Horva´th, K. T. Kiss, L. F. Molna´r, Z. Greece). Journal of Plankton Research 31: 877–884. Pohner, Z. Szila´gyi, B. To´th, F. C. Vad, G. Va´rbı´ro´ &E´ . Cire´s, S., L. Wo¨rmer, R. Agha & A. Quesada, 2013. Overwin- A´ cs, 2014. Biogeography and phylogenetic position of a tering populations of Anabaena, Aphanizomenon and Mi- warm-stenotherm centric diatom, Skeletonema potamos crocystis as potential inocula for summer blooms. Journal (CI Weber) Hasle and its long-term dynamics in the River of Plankton Research 35: 1254–1266. Danube. Protist 165: 715–729. Cire´s, S., L. Wo¨rmer, A. Ballot, R. Aghaa, C. Wiedner, D. Dvora´k, P. & P. Hasler, 2007. Occurrence and morphological Vela´zque, M. C. Casero & A. Quesada, 2014. Phylogeog- variability of Cylindrospermopsis raciborskii (Wolosz.) raphy of cylindrospermopsin and paralytic shellfish toxin- Seenayya et Subba Raju (Cyanophyta, Nostocales) near producing Nostocales cyanobacteria from Mediterranean Olomouc in 2006. Fottea 7: 39–42. Europe (Spain). Applied and Environmental Microbiology Dyble, J., H. W. Paerl & B. A. Neilan, 2002. Genetic charac- 80: 1359–1370. terization of Cylindrospermopsis raciborskii (Cyanobac- Coesel, P. F. M., 1996. Biogeography of desmids. Hydrobi- teria) isolated from diverse geographic origins based on ologia 336: 41–53. nifH and cpcBA-IGS nucleotide sequence analysis. Ap- Conroy, J. D., E. L. Quinlan, D. D. Kane & D. A. Culver, 2007. plied and Environmental Microbiology 68: 2567–2571. Cylindrospermopsis in Lake Erie: testing its association Ehrenberg, C. G., 1849. Passatstaub und Blutregen. Abhand- with other cyanobacterial genera and major limnological lungen der ko¨niglichen Akademie der Wissenschaften in parameters. Journal of Great Lakes Research 33: 519–535. Berlin 1847: 269–460. 123 22 Hydrobiologia (2016) 764:3–27

El Herry, S., H. Nasri & N. Bouaı¨cha, 2008. Morphological and Go´mez, N., P. R. Hualde, M. Licursi & D. E. Bauer, 2004. phylogeneticanalysis of colonies of Microcystis morphos- Spring phytoplankton of Rio de la Plata: a temperate es- pecies isolated from the Lebna Dam, Tunisia. African tuary of South America. Estuarine, Coastal and Shelf Sci- Journal of Microbiology Research 2: 340–348. ence 61: 301–309. Ernst, B., S. J. Hoeger, E. O’Brien & D. R. Dietrich, 2009. Gorthner, A. & C. Meier-Brook, 1985. The Steinheim Basin as a Abundance and toxicity of Planktothrix rubescens in the paleo-ancient lake. In Bayer, U. & A. Seilacher (eds), pre-Alpine Lake Ammersee, Germany. Harmful Algae 8: Sedimentary and Evolutionary Cycles. Springer, Berlin: 329–342. 322–334. Fabre, A., C. Carballo, E. Hernandez, P. Piriz, L. Bergamio, L. Graneli, E. & J. T. Turner, 2006. Ecology of Harmful Algae. Mwllo, S. Gonzalez, G. Pe´rez, J. G. Leo´n, S. Bonilla & C. Ecological Studies Series 189. Springer, Heidelberg. Kruk, 2010. El nitrogeno y la relacio´n zona eufo´tica de Gru¨newald, R. & H. Schubert, 2007. The definition of a new mezcia explican la presencia de cianobacterias en pe- plant diversity index ‘‘H0 dune’’ for assessing human quenos lagos subtropicales, artificiales de Uruguay. Pan- damage on coastal dunes – derived from the Shannon index Ameriacan Journal of Aquatic Sciences 5: 112–125. of entropy H0. Ecological Indicators 7: 1–21. Fastner, J., M. Erhard, W. W. Carmichael, F. Sun, K. L. Rine- Gugger, M., R. Molica, B. Le Berre, P. Dufour, C. Bernard & J.- hart, H. Ro¨nicke & I. Chorus, 1999. Characterization and F. Humbert, 2005. Genetic diversity of Cylindrospermop- diversity of microcystins in natural blooms and strains of sis strains (Cyanobacteria) isolated from four continents. the genera Microcystis and Planktothrix from German Applied and Environmental Microbiology 71: 1097–1100. freshwaters. Archiv fu¨r Hydrobiologie 145: 147–163. Haande, S., A. Ballot, T. Rohrlack, J. Fastner, C. Wiedner & B. Fathalli, A., A. B. Jenhani, S. Cires, M. Saker, M. Romdhane & Edvardsen, 2007. Diversity of Microcystis aeruginosa V. Vasconcelos, 2010. First observation of the potentially strains (Chroococcales, Cyanobacteria) from East-African toxic and invasive cyanobacterium Cylindrospermopsis waterbodies. Archives of Microbiology 188: 15–25. raciborskii in Tunisan freshwaters: toxicity assessement Haande, S., T. Rohrlack, A. Ballot, K. Roberg, R. Skulberg, M. and molecular characterization. Fresenius Environmental Beck & C. Wiedner, 2008. Genetic characterization of Bulletin 19: 1074–1083. Cylindrospermopsis raciborskii (Nostocales, Cyanobacte- Fathalli, A., A. B. R. Jenhania, C. Moreira, M. Welker, M. ria) isolates from Africa and Europe. Harmful Algae 7: Romdhane, A. Antunes & V. Vasconcelos, 2011. Mole- 692–701. cular and phylogenetic characterization of potentially toxic Hamar, J., 1977. Data on the knowledge of the blue-green alga cyanobacteria in Tunisian freshwaters. Systematic and Anabaenopsis raciborskii Wolosz. Tiscia (Szeged) 12: Applied Microbiology 34: 303–310. 17–20. Fenchel, T. & B. J. Finlay, 2006. The ubiquity of small species: Hamed, A. F., 2005. Survey of distribution and diversity of blue- patterns of local and global diversity. BioScience 54: green algae (Cyanobacteria) in Egypt. Acta Botanica 777–784. Hungarica 47: 117–136. Figuerola, J. & A. J. Green, 2002. Dispersal of aquatic organ- Hammer, U. T., 1986. Saline Lake Ecosystems of the World. isms by waterbirds: a review of past research and priorities Junk, Dordrecht. for future studies. Freshwater Biology 47: 483–494. Hamer, A. J. & K. M. Parris, 2011. Local and landscape deter- Fuentes, M. S., J. J. Rick & K. H. Hasenstein, 2010. Occurrence minants of amphibian communities in urban ponds. Eco- of a Cylindrospermopsis bloom in Louisiana. Journal of logical Applications 21: 378–390. Great Lakes Research 36: 458–464. Hamilton, P. B., L. M. Lay, S. Dean & F. R. Pick, 2005. The Gaevsky, N. A., V. I. Kolmakov, O. I. Belykh, I. V. Tikhonova, occurrence of the cyanobacterium Cylindrospermopsis Y. Joung, T. S. Ahn, V. A. Nabatova & A. S. Gladkikh, raciborskii in Constance Lake: an exotic cyanoprokaryote 2011. Ecological development and genetic diversity of new to Canada. Phycologia 44: 17–25. Microcystis aeruginosa from artificial reservoir in Russia. Harris, G. P., 1986. Phytoplankton Ecology: Structure, Function The Journal of Microbiology 49: 714–720. and Fluctuation. Chapman and Hall, London. Genitsaris, S., M. Moustaka-Gouni & K. A. Kormas, 2011. Haworth, E. Y. & P. A. Tyler, 1993. Morphology and taxonomy of Airborne microeukaryote colonists in experimental water Cyclotella tasmanica spec. nov., a newly described diatom containers: diversity, succession, life histories and estab- from Tasmanian lakes. Hydrobiologia 269(270): 49–56. lished food webs. Aquatic Microbial Ecology 62: 139–152. Hayes, P. K. & G. L. A. Barker, 1997. Genetic diversity within Gil, C. B., J. J. R. Restrepo, A. Boltovskoy & A. Vallejo, 2012. Baltic Sea populations of Nodularia (Cyanobacteria). Spatial and temporal change characterization of Ceratium Journal of Phycology 33: 919–923. furcoides (Dinophyta) in the equatorial reservoir Rio- Heaney, S. I. & J. F. Talling, 1980. Ceratium hirundinella – grande II, Colombia. Acta Limnologica Brasiliensia 2: ecology of a complex, mobile and successful plant. Report 207–219. of the Freshwater Biological Association 48: 27–40. Gisle´n, T., 1948. Aerial plankton and its conditions of life. Hecky, R. E. & P. Kilham, 1973. Diatoms in alkaline, saline Biological Reviews 23: 109–126. lakes: ecology and geochemical implications. Limnology Goertzen, D. & F. Suhling, 2013. Promoting dragonfly diversity & Oceanography 18: 53–72. in cities: major determinants and implications for urban Hill, H., 1970. Anabaenopsis raciborskii Woloszynska in Min- pond design. Journal of Insect Conservation 17: 399–409. nesota lakes. Journal of the Minnesota Academy of Sci- Goffart, P., 2010. Southern dragonflies expanding in Wallonia ences 36: 80–82. (south Belgium): a consequence of global warming? Hodoki, Y., K. Ohbayashi, Y. Kobayashi, H. Takasu, N. Okuda BioRisk 5: 109–126. & S. Nalano, 2012. Anatoxin-a-producing Raphidiopsis 123 Hydrobiologia (2016) 764:3–27 23

mediterranea Skuja var. grandis Hill is one ecotype of non- raciborskii (Nostocales, Cyanophyta) at the north-eastern heterocytous Cuspidothrix issatschenkoi (Usacˇev) Ra- limit of its geographical range. European Journal of Phy- janiemi et al. in Japanese lakes. Harmful Algae 21–22: cology 47: 12–21. 44–53. Koma´rek, J., 1985. Do all cyanophytes have a cosmopolitan Hoffmann, L., 1996. Geographic distribution of freshwater blue- distribution? Survey of freshwater cyanophyte flora of green algae. Hydrobiologia 336: 33–40. Cuba. Algological Studies 75: 11–29. Horner-Devine, M. C., M. Lage, J. B. Hughes & B. J. M. Bo- Koma´rek, J. & J. Koma´rkova´-Legnerova´, 2002. Contribution to hannan, 2004. A taxa–area relationship for bacteria. Nature the knowledge of planktic cyanoprokaryotes from central 432: 750–753. Mexico. Preslia 74: 207–233. Ho¨tzel, G. & R. Croome, 1994. Long-term phytoplankton Koma´rek, J. & J. Koma´rkova´, 2004. Taxonomic review of the monitoring of the Darling River at Burtundy, New South cyanoprokaryotic genera Planktothrix and Planktothri- Wales: incidence and significance of cyanobacterial coides. Czech Phycology, Olomouc 4: 1–18. blooms. Marine and Freshwater Research 45: 747–759. Koma´rkova´-Legnerova´, J. & R. Tavera, 1996. Cyanoprokaryota Ichimura, T., 1996. Genome rearrangement and speciation in (Cyanobacteria) in the phytoplankton of Lake Catemaco freshwater algae. Hydrobiologia 336: 1–17. (Veracruz, Mexico). Algological Studies 83: 403–422. Iltis, A., 1993. Recent limnological changes in a saline lake of Kondo, R., G. Kagiya, S. Hiroishi & M. Watanabe, 2000. Ge- the Bolivian Altiplano, Lake Poopo. International Journal netic typing of a bloom-forming cyanobacterial genus of Salt Lake Research 2: 17–28. Microcystis in Japan using 16S rRNA genesequence ana- Incagnone, G., F. Marrone, R. Barone, L. Robba & L. Naselli- lysis. Plankton Biology and Ecology 47: 1–6. Flores, 2015. How do freshwater organisms cross the ‘‘dry Korneva, L. G., 2014. Invasions of alien species of planktonic ocean’’? A review on passive dispersal and colonization microalgae into the fresh waters of Holarctic (review). processes with a special focus on temporary ponds. Hy- Russian Journal of Biological Invasions 5(2): 65–81. drobiologia 750: 103–123. Krienitz, L., 2009. Algae. In Likens, G. E. (ed.), Encyclopedia of Jacquet, S., J.-F. Briand, C. Leboulanger, C. Avois-Jacquet, L. Inland Waters. Elsevier, Oxford: 103–113. Oberhaus, B. Tassin, B. Vincon-Leite, G. Paolini, J.-C. Krienitz, L. & C. Bock, 2012. Present state of the systematics of Druart, O. Anneville & J.-F. Humberta, 2005. The prolif- planktonic coccoid green algae of inland waters. Hydro- eration of the toxic cyanobacterium Planktothrix rubescens biologia 698: 295–326. following restoration of the largest natural French lake Kristiansen, J., 1996a. Bigeography of freshwater algae. Pro- (Lac du Bourget). Harmful Algae 4: 651–672. ceedings of the Workshop on Biogeography of Freshwater Jann-Para, G., I. Schwob & M. Feuillade, 2004. Occurrence of Algae, held during the Fifth International Phycological toxic Planktothrix rubescens blooms in lake Nantua, Congress, Qingdao, China, June 1994. Developments in France. Toxicon 43: 279–285. Hydrobiology 118, Kluwer Academic Publishers, Dordrecht. Jones, W. W. & S. Sauter, 2005. Distribution and abundance of Kristiansen, J., 1996b. Dispersal of freshwater algae – a review. Cylindrospermopsis raciborskii in Indiana lakes and Hydrobiologia 336: 151–157. reservoirs. Indiana Department of Environmental Man- Kristiansen, J. & M. S. Vigna, 1996. Bipolarity in the distribu- agement 4/05, Indiana: 46. Status Report: http://www.spea. tion of silica-scaled chrysophytes. Hydrobiologia 336: indiana.edu/clp/finalcylindro%20web.pdf. 121–126. Kasˇtovsky´, J., T. Hauer, J. Maresˇ, M. Krautova´, T. Besˇta, J. Kruk, C., V. L. M. Huszar, E. T. H. M. Peeters, S. Bonilla, L. Koma´rek, J. Desortova´, J. Hetesˇa, A. Hinda´kova´, V. Houk, Costa, M. Lu¨rling, C. S. Reynolds & M. Scheffer, 2010. A E. Janecˇek, R. Kopp, P. Marvan, P. Pumann, O. Ska´celova´ morphological classification capturing functional variation & E. Zapomelova´, 2010. A review of the alien and ex- in phytoplankton. Freshwater Biology 55: 614–627. pansive species of freshwater cyanobacteria and algae in Krupa, D. & K. Czernas, 2003. Mass appearance of cyanobac- the Czech Republic. Biological Invasions 12: 3599–3625. terium Planktothrix rubescens in Lake Piaseczno, Poland. Kiss, T., A. Vehovszky, L. Hiripi, A. Kova´cs & L. Vo¨ro¨s, 2002. Water Quality Research Journal of Canada 38: 141–152. Membrane effects of toxins isolated from a cyanobacteri- Kubisch, A., R. D. Holt, H. J. Poethke & E. A. Fronhofer, 2014. um, Cylindrospermopsis raciborskii, on identified mol- Where am I and why? Synthesizing range biology and the luscan neurones. Comparative Biochemistry and eco-evolutionary dynamics of dispersal. Oikos 123: 5–22. Physiology Part C 131: 167–176. Kurmayer, R., J. Blom, L. Deng & J. Pernthaler, 2014. Inte- Kling, H., 2009. Cylindrospermopsis raciborskii (Nostocales, grating phylogeny, geographic niche partitioning, and Cyanobacteria): a brief historic overview and recent dis- secondary metabolite synthesis in bloom-forming Plank- covery in the Assiniboine River (Canada). Fottea 9: 45–47. tothrix. The ISME Journal. doi:10.1038/ismej.2014.189. Kobos, J., A. Błaszczyk, N. Hohlfeld, A. Torun´ska-Sitarz, A. Kurmayer, R., G. Christiansen, M. Gumpenberger & J. Fastner, Krakowiak, A. Hebel, K. Sutryk, M. Grabowska, M. To- 2005. Genetic identification of microcystin ecotypes in porowska, M. Kokocinski, B. Messyasz, A. Rybak, A. toxic cyanobacteria of the genus Planktothrix. Microbi- Napiorkowska-Krzebietke, L. Nawrocka, A. Pelechata, A. ology 151: 1525–1533. Budzynska, P. Zagajewski & H. Mazur-Marzec, 2013. Kurmayer, R. & M. Gumpenberger, 2006. Diversity of micro- Cyanobacteria and cyanotoxins in Polish freshwater bod- cystin genotypes among populations of the filamentous ies. Oceanological and Hydrobiological Studies 42: cyanobacteria Planktothrix rubescens and Planktothrix 358–378. agardhii. Molecular Ecology 15: 3849–3861. Kokocinski, M. & J. Soininen, 2012. Environmental factors Kusel-Fetzmann, E., 1998. Das Phytoplankton. In Kusel-Fetz- related to the occurrence of Cylindrospermopsis mann, E., W. Naidenov & B. Russev (eds), Plankton und 123 24 Hydrobiologia (2016) 764:3–27

Benthos der Donau, Ergebnisse der Dounau-Forschung. Milliger, L. E. & H. E. Schlichting, 1968. The passive dispersal Band 4, Wien: 11–161. of viable algae and protozoa by an aquatic beetle. Trans- Kwik, J. T., Z. Y. Kho, B. S. Quek, H. H. Tan & D. C. Yeo, 2013. actions of the American Microscopical Society 87: Urban stormwater ponds in Singapore: potential pathways 443–448. for spread of alien freshwater fishes. BioInvasions Records Mischke, U., 2001. Der Neophyt Cylindrospermopsis raci- 2: 239–245. borskii: eine Blaualge aus tropischen Regionen in Lange-Bertalot, H. & R. Simonsen, 1978. A taxonomic revision Gewa¨ssern des Spree-Dahme Einzugsgebietes. In Krum- of Nitzschiae lanceolatae Grunow 2. European and related beck, H. & U. Mischke (eds), Gewa¨sserreport (Nr. 6): extra-European fresh water and brackish water taxa. Entwicklungen der Gewa¨sser im Scharmu¨tzelseegebiet Bacillaria 1: 11–111. und angewandte Probleme des Gewa¨sserschutzes. BTUC- Legnani, E., D. Copetti, A. Oggioni, G. Tartari, M.-T. Palumbo AR 6/2001, ISSN 1434-6834. & G. Morabito, 2005. Planktothrix rubescens’ seasonal Mitrovic, S. M., R. L. Oliver, C. Rees, L. C. Bowling & R. dynamics and vertical distributionin Lake Pusiano, North T. Buckney, 2003. Critical flow velocities for the growth Italy. Journal of Limnology 64: 61–73. and dominance of Anabaena circinalis in some turbid Lenard, T., 2009. Metalimnetic bloom of Planktothrix rubes- freshwater rivers. Freshwater Biology 48: 164–174. cens in relation to environmental conditions. Oceanologi- Mohamed, Z. A., 2007. First report of toxic Cylindrospermopsis cal and Hydrobiological Studies 38: 45–53. raciborskii and Raphidiopsis mediterranea (Cyanoprokary- Lepisto¨, L. & U. Rosenstro¨m, 1998. The most typical phyto- ota) in Egyptian fresh waters. FEMS Microbial Ecology 59: plankton taxa in four lakes in Finland. Hydrobiologia 749–761. 369(370): 89–97. Moreira, C., A. Fathalli, V. Vasconcelos & A. Antunes, 2011. Lewis, L. A. & P. O. Lewis, 2005. Unearthing the molecular Genetic diversity and structure of the invasive toxic phylo-diversity of desert soil green algae (Chlorophyta). cyanobacterium Cylindrospermopsis raciborskii. Current Systematic Biology 54: 936–947. Microbiology 62: 1590–1595. Lind, O. T., 1984. Patterns of phytoplankton populations and Moreira, C., V. Vasconcelos & A. Antunes, 2012. Phylogeny of their relationships to trophic state in an elongate reservoir. microcystins: evidence of a biogeographical trend. Current Verhandlungen der Internationale Vereinigung fu¨r Microbiology 66: 214–221. theoretische und angewandte Limnologie 22: 1465–1469. Moreira, C., V. Vasconcelos & A. Antunes, 2013. Phylogeny Lindemann, E., 1931. Die Peridinen der Deutchen Lim- and biogeography of cyanobacteria and their produced nologischen Sunda-Expedition nach Sumatra, Java und toxins. Marine Drugs 11: 4350–4369. Bali. Archiv fu¨r Hydrobiologie Supplement 8: 1–691. Moreira, C., A. Fathalli, V. Vasconcelos & A. Antunes, 2014. Lock, K., T. Adriaens, F. Van De Meutter & P. Goethals, 2013. Phylogeny and biogeography of the invasive cyanobac- Effect of water quality on waterbugs (Hemiptera: Gerro- terium Cylindrospermopsis raciborskii. Archives of Mi- morpha & Nepomorpha) in Flanders (Belgium): results crobiology. doi:10.1007/s00203-014-1052-5. from a large-scale field survey. Annales de Limnologie- Moustaka-Gouni, M., K. A. Kormas, E. Vardaka, M. Katsiapi & International Journal of Limnology 49: 121–128. S. Gkelis, 2009. Raphidiopsis mediterranea Skuja repre- Luo, W., T. Pro¨schold, C. Bock & L. Krienitz, 2010. Generic sents non-heterocytous life-cycle stages of Cylindrosper- concept in Chlorella-related coccoid green algae mopsis raciborskii (Woloszynska) Seenayya et Subba Raju (Chlorophyta, Trebouxiophyceae). Plant Biology 12: in Lake Kastoria (Greece), its type locality: evidence by 545–553. morphological and phylogenetic analysis. Harmful Algae Maberly, S. C., L. A. Ball, J. A. Raven & D. Su¨ltemeyer, 2009. 8: 864–872. Inorganic carbon acquisition by chrysophytes. Journal of Mugnai, M. A., M. C. Margheri, C. Sili, S. Turicchia, E. Soldati, Phycology 45: 1052–1061. E. Maffettone, E. Funari, S. Scardala, M. Di Brizio & S. Maguire, B., 1963. The passive dispersal of small aquatic or- Ventura, 2008. The cyanobacterial community of Lake ganisms and their colonization of isolated bodies of water. Trasimeno. Algological Studies 128: 37–64. Ecological Monographs 33: 161–185. Naselli-Flores, L., 2014. Morphological analysis of phyto- Marttunen, M., S. Hellsten, B. Glover, A. Tarvainen, L. Klint- plankton as a tool to assess ecological state of aquatic wall, H. Olsson & T. S. Pedersen, 2006. Heavily Regulated ecosystems: the case of Lake Arancio, Sicily, Italy. Inland Lakes and the European Water Framework Directive – Waters 4: 15–26. Comparisons from Finland, Norway, Sweden, Scotland Naselli-Flores, L., R. Barone, I. Chorus & R. Kurmayer, 2007. and Austria. E-Water Official Publication of the European Toxic cyanobacterial blooms in reservoirs under a semiarid Water Association (EWA): 1–22. Mediterranean climate: the magnification of a problem. Matsumura-Tundisi, T., J. G. Tundisi, A. P. Luzia & R. M. De- Environmental Toxicology 22: 399–404. gani, 2010. Occurrence of Ceratium furcoides (Levander) Neilan, B. A., D. Jacobs, A. E. Goodman, P. T. Cox & P. Langhans 1925 bloom at the Billings Reservoir, Sa˜o Paulo Hawkins, 1995. Genetic diversity and phylogeny of toxic State, Brazil. Brazilian Journal of Biology 70: 825–829. cyanobacteria determined by DNA polymorphism within Messineo, V., D. Mattei, S. Melchiorre, G. Salvatore, S. Bo- the phycocyanin locus. Applied and Environmental Mi- gialli, R. Salzano, R. Mazza, G. Capelli & M. Bruno, 2006. crobiology 61: 3875–3883. Microcystin diversity in a Planktothrix rubescens popula- Neilan, B. A., D. Jacobs, T. del Dot, L. L. Blackall, P. tion from Lake Albano (Central Italy). Toxicon 48: R. Hawkins, P. T. Cox & A. E. Goodman, 1997. rRNA 160–174. sequences and evolutionary relationships among toxic and

123 Hydrobiologia (2016) 764:3–27 25

nontoxic cyanobacteria of the genus Microcystis. Interna- Treyture, A. Lyche Solheim, J. Ortiz-Casas, I. Ott, G. tional Journal of Systematic Bacteriology 47: 693–697. Phillips, A. Pilke, J. Pa´dua, S. Remec-Rekar, U. Ried- Neilan, B. A., M. L. Saker, J. Fastner, A. To¨ro¨kne´ &B. mu¨ller, J. Schaumburg, M. Luisa Serrano, H. Soszka, D. P. Burnes, 2003. Phylogeography of the invasive Tierney, G. Urbanicˇ & G. Wolfram, 2010. Defining cyanobacterium Cylindrospermopsis raciborskii. Mole- chlorophyll-a reference conditions in European lakes. cular Ecology 12: 113–140. Environmental Management 45: 1286–1298. Overeem, M. A., 1937. On green organisms occurring in the lower Pollingher, U., 1990. Effects of latitude on phytoplankton com- trophosphere. Acta Botanica Neerlandica 34: 388–442. position and abundance in large lakes. In Tilzer, M. & C. Padisa´k, J., 1997. Cylindrospermopsis raciborskii (Woloszyn- Serruya (eds), Large Lakes. Springer, Heidelberg: 368–402. ska) Seenayya et Subba Raju, an expanding, highly adap- Popovskaya, G. I., Y. V. Likhoshway, S. I. Genkal & A. tive cyanobacterium: worldwide distribution and review of D. Firsova, 2006. The role of endemic diatom algae in the its ecology. Archiv fu¨r Hydrobiologie/Supplement 107 phytoplankton of Lake Baikal. Hydrobiologia 568: 87–94. (Monographic Studies): 563–593. Posch, T., O. Ko¨ster, M. M. Salcher & J. Pernthaler, 2012. Padisa´k, J., 2003. Phytoplankton. In O’Sullivan, P. E. & C. Harmful filamentous cyanobacteria favoured by reduced S. Reynolds (eds), The Lakes Handbook 1. Limnology and water turnover with lake warming. Nature Climate Change Limnetic Ecology. Blackwell Science Ltd., Oxford: 2: 809–813. 251–308. Prescott, G. W. & T. F. Andrews, 1955. A new species of An- Padisa´k, J. & M. Dokulil, 1994. Meroplankton dynamics in a abaenopsis in a Kansas lake with notes on limnology. saline, turbulent, turbid shallow lake (Neusiedlersee, Hydrobiologia 7: 60–63. Austria and Hungary). Hydrobiologia 289: 23–42. Proctor, V. W., C. Malone & V. L. DeVlaming, 1967. Dispersal Padisa´k, J. & E. Hegewald, 1992. In memoriam dr. h.c. dr Tibor of aquatic organisms: viability of disseminules from the Hortoba´gyi. Botanikai Ko¨zleme´nyek 79: 99–120. digestion tract of captive killdeer. Ecology 48: 672–676. Padisa´k, J. & C. S. Reynolds, 1998. Selection of phytoplankton Ralfs, J., 1848. The British Desmidieae. Reeve, Benham & associations in Lake Balaton, Hungary, in response to eu- Reeve, London, 226 pp. trophicatioon and restoration measures, with special ref- Rengefors, K. & D. M. Andersen, 1998. Environmental and erence to cyanoprokaryotes. Hydrobiologia 384: 41–53. endogenous regulation of cyst germination in two fresh- Padisa´k, J., F. A. R. Barbosa, R. Koschel & L. Krienitz, 2003. water dinoflagellates. Journal of Phycology 34: 568–577. Deep layer cyanoprokaryota maxima are constitutional Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge features of lakes: examples from temperate and tropical University Press, Cambridge. regions. Archiv fu¨r Hydrobiologie Advances in Limnology Reynolds, C. S., 2007. Variability in the provision and function 58: 175–199. of mucilage in phytoplankton: facultative responses to the Padisa´k, J., L. O. Crossetti & L. Naselli-Flores, 2009. Use and environment. Hydrobiologia 578: 37–45. misuse in the application of the phytoplankton functional Reynolds, C. S., J.-P. Descy & J. Padisa´k, 1994. Are phyto- classification: a critical review with updates. Hydrobiolo- plankton dynamics in rivers so different from those in gia 621: 1–19. shallow lakes? Hydrobiologia 289: 1–8. Padisa´k, J., E´ . Hajnal, L. Krienitz, J. Lakner & V. U¨ veges, 2010. Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Rarity, ecological memory, rate of floral change in phyto- Melo, 2002. Towards a functional classification of the plankton – and the mystery of the Red Cock. Hydrobiologia freshwater phytoplankton. Journal of Plankton Research 653: 45–67. 24: 417–428. Paulino, S., E. Vale´rio, N. Faria, J. Fastner, M. Welker, R. Reynolds, C. S. & A. E. Walsby, 1975. Waterblooms. Biological Tenreiro & P. Pereira, 2009. Detection of Planktothrix Reviews 50: 437–481. rubescens (Cyanobacteria) associated with microcystin Rˇ eza´cˇova´, M., J. Neustupa & L. Sˇejnohova, 2004. Five species productionin a freshwater reservoir. Hydrobiologia 621: of Mallomonas (Synurophyceae) new to the algal flora of 207–211. the Czech Republik. Preslia 76: 175–181. Pe´rez-Martı´nez, C. & P. Sa´nchez-Castillo, 2001. Temporal oc- Rick, H. J., S. Rick, S. Fuentes & J. L. Noel, 2007. The invasive currence of Ceratium hirundinella in Spanish reservoirs. cyanobacterium Cylindrospermopsis raciborskii in south- Hydrobiologia 452: 101–107. ern Louisiana. Gulf of Mexico Science 25: 61–81. Pe´terfi, S. L. & L. Momeu, 1996. Three Mallomonas species Roscher, J. P., 1967. Alga dispersal by muskrat intestinal con- (Synurophyceae), with special distribution patterns. Hy- tents. Transactions of the American Microscopical Society drobiologia 336: 143–150. 86: 497–498. Pe´terfi, L. S., J. Padisa´k, L. Momeu & G. Borics, 1998. Silica- Roy-Ocotla, G. & J. Carrera, 1993. Aeroalgae: responses to scaled chrysophytes from the bog-lake Bala´ta-to´,SW some aerobiological questions. Grana 32: 48–56. Hungary. Nordic Journal of Botany 18(6): 727–733. Saker, M. L., I. C. G. Nogueira & V. M. Vasconcelos, 2004. Pe´terfi, L. S., L. Momeu, J. Padisa´k & A. L. To¨ro¨k, 2002. Silica- Distribution and toxicity of Cylindrospermopsis raci- scaled flagellates (Synurophyceae) of the ,,Mestecanisu de borskii (Cyanobacteria) in Portuguese freshwaters. Lim- la Reci’’, Covasna County, Transsylvania, Romania. netica 22: 129–136. Contributii Botanice 37: 113–118. Salmaso, N., L. Naselli-Flores & J. Padisa´k, 2015. Functional Pike, J., 2013. Of volcanoes and diatoms. Geology 41: classifications and their application in phytoplankton 1199–1200. ecology. Freshwater Biology 60: 603–619. Poikane, S., M. Helena Alves, C. Argillier, M. Van Den Berg, F. Salmaso, N. & J. Padisa´k, 2007. Morpho-functional groups and Buzzi, E. Hoehn, C. de Hoyos, I. Karottki, C. Laplace- phytoplankton development in two deep lakes (Lake 123 26 Hydrobiologia (2016) 764:3–27

Garda, Italy and Lake Stechlin, Germany). Hydrobiologia Germany: Cylindrospermopsis raciborskii, Anabaena bergii 578: 97–112. and Aphanizomenon aphanizomenoides. Phycologia 45: Sandgren, C. D., 1988. The ecology of chrysophyte flagellates: 696–703. their growth and perennation as freshwater phytoplankton. Szalay, G., 2014. Characteristics of phytoplankton in an artifi- In Sandgren, C. D. (ed.), Growth and Reproductive cial lake (Devecser). M.Sc. Thesis, Department of Lim- Strategies of Freshwater Phytoplankton. Cambridge nology, University of Pannonia. University Press, Cambridge: 9–104. Talling, J. F., 1951. The element of chance in pond populations. Santos-Wisniewski, M. J., L. C. Silva, I. C. Leone, R. Laudares- The Naturalist 1951: 157–170. Silva & O. Rocha, 2007. First record of the occurrence of Talling, J. F. & G. A. Prowse, 2010. Selective recruitment and Ceratium furcoides (Levander) Langhans 1925, an invasive resurgence of tropical river phytoplankton: evidence from species in the hydroelectricity power plant Furnas Reser- the Nile system of lakes, rivers, reservoirs and ponds. voir, MG, Brazil. Brazilian Journal of Biology 67: 791–793. Hydrobiologia 637: 187–195. Scheffler, W. & J. Padisa´k, 1997. Cyclotella tripartita Tapolczai, K., O. Anneville, J. Padisa´k, N. Salmaso, T. Zohary Ha˚kansson (Bacillariophyceae), a dominant diatom species & F. Rimet, 2014. Occurrence and mass development dy- in the oligotrophic Stechlinsee (Germany). Nova Hedwigia namics of Mougeotia spp. in large, deep lakes. Hydrobi- 65: 221–232. ologia 745: 17–29. Scheffler, W. & J. Padisa´k, 2000. Stephanocostis chantaicus Tyler, P. A., 1996. Endemism in freshwater algae with special (Bacillariophyceae): morphology and population dynamics reference to the Australian region. Hydrobiologia 336: of a rare centric diatom growing in winter under ice in the 127–135. oligotrophic Lake Stechlin, Germany. Algological Studies Unrein, F., 2002. Changes in phytoplankton community along a 133: 49–69. transversal section of the Lower Parana floodplain, Ar- Schlichting, H. E., 1960. The role of waterfowl in dispersal of gentina. Hydrobiologia 468: 123–134. algae. Transactions of the American Microscopical Society U¨ veges, V., K. Tapolczai, L. Krienitz & J. Padisa´k, 2012. 79: 160–166. Photosynthetic characteristics and physiological plasticity Schmidt, A., 1994. Main characteristics of the phytoplankton of of an Aphanizomenon flos-aquae (Cyanobacteria, Nosto- the Southern Hungarian section of the River Danube. Hy- caceae) winter bloom in a deep oligo-mesotrophic lake drobiologia 28: 97–108. (Lake Stechlin, Germany). Hydrobiologia 698: 263–272. Schoener, T. W., 1976. The species-area relationship within Van de Bund, W., A. C. Cardoso, A. S. Heiskanen & P. No˜ges, archipelagoes: models and evidence from island birds. 2004. Overview of common intercalibration types. http:// Proceedings of the XVI International Ornithological Con- wfd-reporting.jrc.cec.eu.int/Docs/typesmanual. ress 6: 629–642. Van Eaton, A. R., M. A. Harper & C. J. Wilson, 2013. High- Sharma, N. K., A. K. Rai, S. Singh & R. M. Brown Jr, 2007. flying diatoms: widespread dispersal of microorganisms in Airborne algae: their present status and relevance. Journal an explosive volcanic eruption. Geology 41: 1187–1190. of Phycology 43: 615–627. Van Gremberghe, I., F. Leliaert, J. Mergeay, P. Vanormelingen, Sides, S. L., 1973. Internal and external transport of algae and K. van der Gucht, A.-E. Debeer, G. Lacerot, L. de Meester protozoa by sea gulls. Transactions of the American Mi- & W. Vyverman, 2011. Lack of phylogeographic structure croscopical Society 92: 307–311. in the freshwater cyanobacterium Microcystis aeruginosa Smith, V. H., B. L. Foster, J. P. Grover, R. D. Holt, M. A. Lei- suggests global dispersal. PLoS One 6(5): e19561. bold & F. de Noyelles Jr., 2005. Phytoplankton species Van Vuuren, S. J. & G. P. Kriel, 2008. Cylindrospermopsis raci- richness scales consistently from laboratory microcosms to borskii, a toxic invasive cyanobacterium in South African the world’s oceans. Proceedings of the National Academy fresh waters. African Journal of Aquatic Science 33: 17–26. of Sciences of the United States of America 102: Vareli, K., E. Briasoulis, G. Pilidis & I. Sainis, 2009. Molecular 4393–4396. confirmation of Planktothrix rubescens as the cause of Souza, M. B. G., C. F. A. Barros, F. A. R. Barbosa, E´ . Hajnal & intense, microcystin – synthesizing cyanobacterial bloom J. Padisa´k, 2008. The role of atelomixis in phytoplankton in Lake Ziros, Greece. Harmful Algae 8: 447–453. assemblages’ replacement in Dom Helve´cio Lake, South- Vasas, G., I. Ba´csi, G. Sura´nyi, M. M. Hamvas, C. Ma´the´,S. East Brazil. Hydrobiologa 607: 211–224. A. Nagy & G. Borbe´ly, 2010. Isolation of viable cell mass Stefaniak, K. & M. Kokocynski, 2005. Occurrence of invasive from frozen Microcystis viridis bloom containing micro- Cyanobacteria species in polimictic lakes of the cystin-RR. Hydrobiologia 63: 147–151. Wielkopolska region (Western Poland). Oceanological and Vasas,G.,O.Farkas,G.Borics,T.Felfo¨ldi, G. Sramko, G. Batta, I. Hydrobiological Research 34(Supplement 3): 137–148. Ba´csi & S. Gonda, 2014. Appearance of Planktothrix rubes- Stomp, M., J. Huisman, G. Mittelbach, E. Litchman & C. cens bloom with [D-Asp3, Mdha7] MC-RR in gravel pit pond Klausmeier, 2011. Large-scale biodiversity patterns in of a shallow lake dominated area. Toxins 5: 2434–2455. freshwater phytoplankton. Ecology 92: 2096–2107. Vehovszky, A., A. W. Kova´cs, H. Szabo´,J.Gyori} & A. Farkas, Stoyneva, M. P., 1994. Shallows of the lower Danube as addi- 2012. Neurotoxic effects evoked by cyanobacterial extracts tional sources of potamoplankton. Hydrobiologia 289: suggest multiple receptors involved in electrophysiological 171–178. responses of molluscan (CNS, heart) models. Acta Biolo- Stuken, A., J. Ru¨cker, T. Endrulat, K. Preussel, M. Hemm, B. gica 63: 160–170. Nixdorf, U. Karsten & C. Wiedner, 2006. Distribution of three Vehovszky, A., A. W. Kova´cs, A. Farkas, J. Gyori,} H. Szabo´ & alien cyanobacterial species (Nostocales) in northeast G. Vasas, 2013. Pharmacological studies confirm

123 Hydrobiologia (2016) 764:3–27 27

neurotoxic metabolite(s) produced by the bloom-forming Wilson, A. E., O. Sarnelle, B. A. Neilan, T. P. Salmon, M. Cylindrospermopsis raciborskii in Hungary. Environmen- M. Gehringer & M. E. Hay, 2005. Genetic variation of the talToxicology. doi:10.1002/tox.21927. bloom-forming cyanobacterium Microcystis aeruginosa Vidal, L. & C. Kruk, 2008. Cylindrospermopsis raciborskii within and among lakes: Implications for harmful algal (Cyanobacteria) extends its distribution to Latitude blooms. Applied and Environmental Microbiology 71: 34°530S: taxonomical and ecological features in Uru- 6126–6133. guayan eutrophic lakes. Pan-American Journal of Aquatic Wood, S. A., X. Pochon, L. Luttringer-Plu, B. N. Vant & P. Sciences 3: 142–151. Hamilton, 2014. Recent invader or indicator of environmental Vyverman, W., 1996. The Indo-Malaysian North-Australian change? A phylogenetic and ecological study of Cylindros- phycogeographical region revised. Hydrobiologia 336: permopsis raciborskii in New Zealand. Harmful Algae 39: 107–120. 64–74. Wen, Z., Z. Mian-Ping, X. Xian-Zhong, L. Xi-Fang, G. Gan- Yoshida, M., T. Yoshida, M. Satomi, Y. Takashima, N. Hosoda Linand & H. Zhi-hui, 2005. Biological and ecological & S. Hiroishi, 2008. Intra-specific phenotypic and geno- features of saline lakes in northern Tibet, China. Hydro- typic variation in toxic cyanobacterial Microcystis strains. biologia 81: 1–14. Journal of Applied Microbiology 105: 407–415. Wetzel, R. G., 2001. Limnology: Lake and River Ecosystems, Zohary, T. & M. Shlichter, 2009. Invasion pf Lake Kinneret by 3rd ed. Academic Press, San Diego. the N2-fixing cyanobacterium Cylindrospermopsis. Ver- Weyhenmeyer, G., H. Peter & E. Wille´n, 2013. Shifts in phy- handlungen der Internationale Vereinigung fu¨r theoretis- toplankton species richness and biomass along a latitudinal che und angewandte Limnologie 30: 1251–1254. gradient – consequences for relationships between biodi- versity and ecosystem functioning. Freshwater Biology 58: 612–623.

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