Invasion of Nostocales (cyanobacteria) to Subtropical and Temperate Freshwater Lakes – Physiological, Regional, and Global Driving Forces

Similar to the increased number of studies on invasive plants and animals in terrestrial and aquatic ecosystems, many reports were recently published on the invasion of Nostocales (cyanobacteria) to freshwater environments worldwide. Invasion and proliferation of Nostocales in new habitats have the potential to significantly alter the structure of the native community and to modify ecosystem functioning. But most importantly, they influence the water quality due to a variety of toxic compounds that some species produce. Therefore a special attention was given to the invasion and persistence of toxic cyanobacteria in many aquatic ecosystems. Here we summarize the currently published records on the invasion of two Nostocales genera, Cylindrospermopsis and Aphanizomenon, to lakes and water reservoirs in subtropical and temperate zones. These invading species possess traits thought to be common to many invasive organisms: high growth rate, high resource utilization efficiency and overall superior competitive abilities over native species when local conditions vary. Assuming that dispersion routes of cyanobacteria have not been changed much in recent decades, their recent establishment and proliferation in new habitats indicate changes in the environment under which they can exploit their physiological advantage over the native phytoplankton population. In many cases, global warming was identified as the major driving force for the invasion of Nostocales. Due to this uncontrollable trend, invasive Nostocales species are expected to maintain their presence in new habitats and further expand to new environments. In other cases, regional changes in nutrient loads and in biotic conditions were attributed to the invasion events.

[1]  T. Hoffman.  Fifty Years of Invasion Ecology: The Legacy of Charles Elton , 2012 .

[2]  H. Paerl,et al.  Climate change: links to global expansion of harmful cyanobacteria. , 2012, Water research.

[3]  Lirong Song,et al.  Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation , 2012 .

[4]  H. Paerl,et al.  Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. , 2012, FEMS microbiology ecology.

[5]  M. Scheffer,et al.  Warmer climates boost cyanobacterial dominance in shallow lakes , 2012 .

[6]  H. Paerl,et al.  Determining the potential for the proliferation of the harmful cyanobacterium Cylindrospermopsis raciborskii in Currituck Sound, North Carolina , 2011 .

[7]  A. Ballot,et al.  Occurrence of non-cylindrospermopsin- producing Aphanizomenon ovalisporum and Anabaena bergii in Lake Kinneret (Israel) , 2011 .

[8]  C. Wiedner,et al.  Cylindrospermopsin production and release by the potentially invasive cyanobacterium Aphanizomenon ovalisporum under temperature and light gradients , 2011 .

[9]  V. Amaral,et al.  Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes , 2011 .

[10]  D. Griffin,et al.  The high life: Transport of microbes in the atmosphere , 2011 .

[11]  Rainer Brüggemann,et al.  Modelling life cycle and population dynamics of Nostocales (cyanobacteria) , 2011, Environ. Model. Softw..

[12]  Hans W Paerl,et al.  Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. , 2011, The Science of the total environment.

[13]  S. Watson,et al.  Bloom development and phytoplankton succession in Lake Winnipeg: a comparison of historical records with recent data , 2011 .

[14]  E. Litchman.  Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. , 2010, Ecology letters.

[15]  A. Kaplan,et al.  Enslavement in the Water Body by Toxic Aphanizomenon ovalisporum, Inducing Alkaline Phosphatase in Phytoplanktons , 2010, Current Biology.

[16]  Samuel Cirés,et al.  Competitiveness of invasive and native cyanobacteria from temperate freshwaters under various light and temperature conditions , 2010 .

[17]  P. Marvan,et al.  A review of the alien and expansive species of freshwater cyanobacteria and algae in the Czech Republic , 2010, Biological Invasions.

[18]  M. Laamanen,et al.  Life cycle strategies of bloom-forming, filamentous cyanobacteria in the Baltic Sea , 2010 .

[19]  Jacqueline Rücker,et al.  Impact of the inoculum size on the population of Nostocales cyanobacteria in a temperate lake , 2009 .

[20]  G. Shaw,et al.  PULSES OF PHOSPHATE PROMOTE DOMINANCE OF THE TOXIC CYANOPHYTE CYLINDROSPERMOPSIS RACIBORSKII IN A SUBTROPICAL WATER RESERVOIR 1 , 2009, Journal of phycology.

[21]  H. Paerl,et al.  Interactions between nitrogen dynamics and the phytoplankton community in Lake George, Florida, USA , 2009 .

[22]  T. Jurczak,et al.  First report of the cyanobacterial toxin cylindrospermopsin in the shallow, eutrophic lakes of western Poland. , 2009, Chemosphere.

[23]  David W. Schindler,et al.  Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37-year whole-ecosystem experiment , 2008, Proceedings of the National Academy of Sciences.

[24]  Petr Pyšek,et al.  Fifty years of invasion ecology – the legacy of Charles Elton , 2008 .

[25]  D. Bird,et al.  DOES ALLELOPATHY CONTRIBUTE TO CYLINDROSPERMOPSIS RACIBORSKII (CYANOBACTERIA) BLOOM OCCURRENCE AND GEOGRAPHIC EXPANSION? 1 , 2007 .

[26]  A. Ricciardi,et al.  The invasiveness of an introduced species does not predict its impact , 2007, Biological Invasions.

[27]  R. Brüggemann,et al.  Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions , 2007, Oecologia.

[28]  Z. Mohamed.  First report of toxic Cylindrospermopsis raciborskii and Raphidiopsis mediterranea (Cyanoprokaryota) in Egyptian fresh waters. , 2007, FEMS microbiology ecology.

[29]  I. Chorus,et al.  Occurrence of the cyanobacterial toxin cylindrospermopsin in northeast Germany , 2007, Environmental toxicology.

[30]  P. Leavitt,et al.  Landscape‐scale effects of urban nitrogen on a chain of freshwater lakes in central North America , 2006 .

[31]  P. Leavitt,et al.  Spatial variation of nitrogen fixation in lakes of the northern Great Plains , 2006 .

[32]  Inga Hense,et al.  Towards a model of cyanobacteria life cycle—effects of growing and resting stages on bloom formation of N2-fixing species , 2006 .

[33]  A. Quesada,et al.  Incorporation of Different N Sources and Light Response Curves of Nitrogenase and Photosynthesis by Cyanobacterial Blooms from Rice Fields , 2006, Microbial Ecology.

[34]  Anna Traveset,et al.  Biological invasions as disruptors of plant reproductive mutualisms. , 2006, Trends in ecology & evolution.

[35]  Antonio Quesada,et al.  Toxicity of Aphanizomenon ovalisporum (Cyanobacteria) in a Spanish water reservoir , 2006 .

[36]  H. Paerl,et al.  Zooplankton community structure, micro-zooplankton grazing impact, and seston energy content in the St. Johns river system, Florida as influenced by the toxic cyanobacterium Cylindrospermopsisraciborskii , 2005, Hydrobiologia.

[37]  R. Molica,et al.  Genetic Diversity of Cylindrospermopsis Strains (Cyanobacteria) Isolated from Four Continents , 2005, Applied and Environmental Microbiology.

[38]  Tamar Zohary,et al.  Changes to the phytoplankton assemblage of Lake Kinneret after decades of a predictable, repetitive pattern , 2004 .

[39]  Daniel E. Schindler,et al.  CLIMATE CHANGE UNCOUPLES TROPHIC INTERACTIONS IN AN AQUATIC ECOSYSTEM , 2004 .

[40]  G. Livingston,et al.  Do cyanobacteria dominate in eutrophic lakes because they fix atmospheric nitrogen , 2004 .

[41]  M. Kawachi,et al.  Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. , 2004, FEMS microbiology ecology.

[42]  C. Bernard,et al.  CYLINDROSPERMOPSIS RACIBORSKII (CYANOBACTERIA) INVASION AT MID‐LATITUDES: SELECTION, WIDE PHYSIOLOGICAL TOLERANCE, ORGLOBALWARMING? 1 , 2004 .

[43]  Robert I. Colautti,et al.  A neutral terminology to define ‘invasive’ species , 2004 .

[44]  V. Vasconcelos,et al.  Accumulation and depuration of the cyanobacterial toxin cylindrospermopsin in the freshwater mussel Anodonta cygnea. , 2004, Toxicon : official journal of the International Society on Toxinology.

[45]  S. Wood,et al.  First identification of the cylindrospermopsin‐producing cyanobacterium Cylindrospermopsis raciborskii in New Zealand , 2003 .

[46]  D. Dobberfuhl.  Cylindrospermopsis racihorskii in Three Central Florida Lakes: Population Dynamics, Controls, and Management Implications , 2003 .

[47]  David P. Hamilton,et al.  Recent occurrence of Cylindrospermopsis raciborskii in Waikato lakes of New Zealand , 2003 .

[48]  S. Lavorel,et al.  Mechanisms underlying the impacts of exotic plant invasions , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  B. Burns,et al.  Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii , 2002, Molecular ecology.

[50]  S. Azevedo,et al.  Toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) isolated from Tabocas reservoir in Caruaru, Brazil, including demonstration of a new saxitoxin analogue , 2002 .

[51]  H. Paerl,et al.  Genetic Characterization of Cylindrospermopsis raciborskii (Cyanobacteria) Isolates from Diverse Geographic Origins Based on nifH and cpcBA-IGS Nucleotide Sequence Analysis , 2002, Applied and Environmental Microbiology.

[52]  A. Kaplan,et al.  Physiological variables determined under laboratory conditions may explain the bloom of Aphanizomenon ovalisporum in Lake Kinneret , 2002 .

[53]  Wayne W. Carmichael,et al.  Health Effects of Toxin-Producing Cyanobacteria: “The CyanoHABs” , 2001 .

[54]  Alexandre Meinesz,et al.  The Introduced Green Alga Caulerpa Taxifolia Continues to Spread in the Mediterranean , 2001, Biological Invasions.

[55]  D. Pimentel,et al.  Economic and environmental threats of alien plant, animal, and microbe invasions , 2001 .

[56]  T. Berman,et al.  The role of DON and the effect of N: P ratios on occurrence of cyanobacterial blooms: Implications from the outgrowth of Aphanizomenon in Lake Kinneret , 2001 .

[57]  Diogo Falcão,et al.  Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought , 2000 .

[58]  P. Domingos,et al.  Cyanoprokaryote assemblages in eight productive tropical Brazilian waters , 2000, Hydrobiologia.

[59]  M. Présing,et al.  Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures , 2000 .

[60]  Moshe Gophen,et al.  Nitrogen deficiency, phosphorus sufficiency, and the invasion of Lake Kinneret, Israel, by the N2-fixing cyanobacterium Aphanizomenon ovalisporum , 1999, Aquatic Sciences.

[61]  S. Azevedo,et al.  The first evidence of paralytic shellfish toxins in the fresh water cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. , 1999, Toxicon : official journal of the International Society on Toxinology.

[62]  A. Kaplan,et al.  Limnological and ecophysiological aspects of Aphanizomenon ovalisporum bloom in Lake Kinneret, Israel , 1999 .

[63]  G. Eaglesham,et al.  The accumulation of cylindrospermopsin from the cyanobacterium Cylindrospermopsis raciborskii in tissues of the Redclaw crayfish Cherax quadricarinatus. , 1999, Toxicon : official journal of the International Society on Toxinology.

[64]  G. Shaw,et al.  Blooms of the cylindrospermopsin containing cyanobacterium, Aphanizomenon ovalisporum (Forti), in newly constructed lakes, Queensland, Australia , 1999 .

[65]  T. Berman.  Dissolved organic nitrogen utilization by an Aphanizomenon bloom in Lake Kinneret , 1997 .

[66]  A. Chapman,et al.  RECENT APPEARANCE OF CYLINDROSPEMOPSIS (CYANOBACTEIUA) IN FIVE HYPEREUTROPHIC FLORIDA LAKES 1 , 1997 .

[67]  M. Callisto,et al.  Eutrophication of Lakes , 2014 .

[68]  A. Sukenik,et al.  Akinetes: Dormant Cells of Cyanobacteria , 2010 .

[69]  H. Kling.  Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria): A brief historic overview and recent discovery in the Assiniboine River (Canada). , 2009 .

[70]  C. Kruk,et al.  Cylindrospermopsis raciborskii (Cyanobacteria) extends its distribution to Latitude 34°53'S: taxonomical and ecological features in Uruguayan eutrophic lakes , 2008 .

[71]  W. W. Jones,et al.  Distribution and Abundance of Cylindrospermopsis raciborskii in Indiana Lakes and Reservoirs , 2005 .

[72]  Maria Rosa Miracle,et al.  Population dynamics and ecology of subdominant phytoplankton species in a shallow hypertrophic lake (Albufera of Valencia, Spain) , 2004, Hydrobiologia.

[73]  Z. Ramezanpoor.  ECOLOGICAL STUDY OF PHYTOPLANKTON OF THE ANZALI LAGOON (N IRAN) AND ITS OUTFLOW INTO THE CASPIAN SEA , 2004 .

[74]  Charles C. Elton,et al.  The Ecology of Invasions by Animals and Plants , 2004, Biodiversity & Conservation.

[75]  Komárek,et al.  Phenotype diversity of the cyanoprokaryotic genus Cylindrospermopsis (Nostocales); review 2002 , 2003 .

[76]  V. Smith,et al.  Nitrogen deficiency, phosphorus sufficiency, and the invasion of Lake Kinneret, Israel, by the N , 1999 .

[77]  T. Berman,et al.  Phytoplankton development and turbulent mixing in Lake Kinneret (1992–1996) , 1998 .

[78]  U. Pollingher,et al.  Aphanizomenon ovalisporum (Forti) in Lake Kinneret, Israel , 1998 .

[79]  Judit Padisák,et al.  Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium : worldwide distribution and review of its ecology , 1997 .

[80]  N. Abdelahad,et al.  Caractérisation morphométrique et statistique de deux populations d' Aphanizomenon du groupe Aphanizomenon ovalisporum Forti des lacs de Nemi et Albano (Italie). , 1994 .