Volume 7 2006 great lakes Great Lakes program Research Consortium Great Lakes Research Review Working together for Great Lakes research and education Monitoring Harmful Algal Blooms In This Issue: Toxic Cyanobacteria in the Great Lakes: More than Just the Western Basin of Lake Erie...APartnership Approach to Cyanobacteria Monitoring in Lake Champlain.... Mapping Variations of Algal Blooms in the Lower Great Lakes...Lake Champlain Phytoplankton and Algal Toxins: Past and Present...The Application of Molecular Tools to Freshwater Harmful Algal Blooms...The Occurrence of Cyanotoxins in the Nearshore and Coastal Embayments of Lake Ontario... Why do Cyanobacteria Produce Toxins? Great Lakes Research Review ABOUT THIS PUBLICATION: great lakes Several years ago, staff from the Great program Lakes Program, the Great Lakes Research Consortium, and New York Sea Grant real- ized an information gap existed between University of Buffalo 202 Jarvis Hall peer reviewed journal articles and newslet- Buffalo, NY14260-4400 ter type information related to Great Lakes Voice: (716) 645-2088 research. The Great Lakes Research Fax: (716) 645-3667 Review was created to fill that gap by pro- http://www.buffalo.edu/glp viding a substantive overview of research Director: Dr. Joseph F. Atkinson Associate Director: Helen M. Domske being conducted throughout the basin. It Administrative. Assistant: Monica S. Moshenko is designed to inform researchers, policy- makers, educators, managers and stake- holders about Great Lakes research efforts, particularly but not exclusively being con- Great Lakes ducted by scientists affilliated with the Research Consortium and its member institutions. Consortium Each issue has a special theme. Past issues SUNYCollege of ESF have focused on the fate and transport of 24 Bray Hall toxic substances, the effects of toxics, fish- Syracuse, NY13210 eries issues, and exotic species. The most Voice: (315) 470-6816 Fax: (315) 470-6970 recent volumes have focused on the Lake http://www.esf.edu/glrc Ontario, St. Lawrence River and Lake Erie Executive Director: Jack Manno ecosystems, and the research of the New Co-Director: Richard Smardon York Great Lakes Protection Fund. The Research Co-Director: Edward Mills present issue describes some of the research by the MERHAB Project. We gratefully acknowledge all of the con- tributing authors who willingly shared their research efforts for this publication, especially Greg Boyer for his assistance- with editing and organizing authors. We also wish to thank the SUNYESFOffice of News and Publications for assistance. SUNYat Stony Brook Dutchess Hall Stony Brook, NY11794-5001 THE UPCOMING ISSUE Voice: (631) 632-6905 For more information, contact Michael Fax: (631) 632-6917 Connerton at [email protected] http://www.seagrant.sunysb.edu/ Director: Dr. Jack Mattice Associate Director: Ms. Cornelia Schlenk ON THE COVER: Image of Microcystis bloom in Western Lake Erie, August 2003 Volume 7 2006 Great Lakes Research Review Monitoring Harmful Algal Blooms in the Great Lakes TABLEOFCONTENTS Introduction Gregory Boyer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1 Toxic Cyanobacteria in the Great Lakes: More than Just the Western Basin of Lake Erie Gregory L. Boyer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .2 APartnership Approach to Cyanobacteria Monitoring in Lake Champlain Mary C. Watzin, Emily Brines Miller, Angela D. Shambaugh, Meghan A. Kreider . . . . . . . . . . . . . . . . . . .8 Mapping Variations of Algal Blooms in the Lower Great Lakes R. Becker, M. Sultan, G. Boyer, and E. Konopko . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .14 Lake Champlain Phytoplankton and Algal Toxins: Past and Present Timothy B. Mihuc, Gregory L. Boyer, Jeffry Jones, Mike Satchwell, and Mary C. Watzin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .18 The Application of Molecular Tools to Freshwater Harmful Algal Blooms: Identifying and Quantifying Toxic Cyanobacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .22 Johanna Rinta-Kanto and Steven W. Wilhelm The Occurrence of Cyanotoxins in the Nearshore and Coastal Embayments of Lake Ontario 25 Joseph C. Makarewicz, Gregory L. Boyer, William Guenther, Mary Arnold and Theodore W. Lewis. . Why Do Cyanobacteria Produce Toxins? Investigating a Possible Trigger for Microcystin Production in a Harmful Algal Bloom . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 Michael R..T wiss and Sandra P. Gouvêa Editors, Design and Layout: Michael Connerton, and Christine Crysler GREAT LAKES NONPROFITORG. RESEARCH CONSORTIUM 24 BRAYHALL U.S. POSTAGE PAID SUNYCollege of Environmental Science and Foresty SYRACUSE, NY Syracuse, NY13210 PERMITNO 248 Introduction Gregory L. Boyer State Universty of New York College of Environmental Science and Forestry Syracuse, NY 13210 “And all the waters that were in the river turned to blood. the project combines the efforts of analytical And the fish that were in the rivers died; and the river chemists, classical taxonomists, molecular biologists, stank, and the Egyptians could not drink the water of the experts in satellite imagery, hydrodynamic modelers river, …” and outreach experts as it works towards a unified Exodus 7:20-21 approach to protecting the public. Sampling plat- forms range from the docks of local homeowners to Harmful algal blooms are not new. They have been large ships operating miles from shore for extended around centuries and their impacts on humans were periods of time. This is interdisciplinary science at its recorded in biblical times. These blooms can nega- best. tively impact our drinking waters, pets, livestock, fish and the enjoyment of our aquatic resources. The following articles provide a general introduction to these efforts, as well as summarize some of our Most research on harmful algal blooms has focused current work using citizen monitors, satellites, the on marine environments where the negative impacts microscope and the PCR thermocycler to protect our of “red tides” is both well studied and well under- waters from toxic blooms. While we may not be able stood. In 1993, the US government recognized that to stop our rivers from turning to blood, we will marine biotoxins represented a significant and know when and if it is safe to drink and swim in the expanding threat to human health and fisheries water. resources and established an interagency national plan to address both the research and monitoring needs of our nation (WHOI, 1993). This national plan spawned several national research agendas, most notably Ecology and Oceanography of Harmful Algal Blooms (ECOHAB) and Monitoring and Event Response for Harmful Algal Blooms (MERHAB). While much of ECOHAB and MERHAB’s efforts have focused on our coastal resources, great lakes issues are also recognized as an important compo- nent of these research agendas. ECOHAB and MERHAB fund both small individual investigator projects focusing on a single problem and large regional efforts that span across traditional disciplines and boundaries. In 2002, NOAA’s Coastal Ocean Program through MERHAB funded the first regional effort to look at toxic cyanobacteria in the lower Great Lakes ecosystem. This project, termed MERHAB-LGL, focuses on Lakes Erie, Ontario and Champlain. The MERHAB-LGL project has more than 30 specific objectives, all focused on the devel- opment of cost effective monitoring strategies to pro- tect our drinking and recreational waters from cyanobacterial blooms. No technique is off limits and Great Lakes Research Review, Volume 7, 2006 1 Toxic Cyanobacteria in the Great Lakes: More than just the Western Basin of Lake Erie Gregory Boyer State University of New York, College of Environmental Science and Forestry Syracuse, NY 13210 Cyanobacteria, or blue-green algae, are ubiquitous in nature and found in nearly all environments. Many species have selective advantages such as the ability to use atmospheric nitrogen for growth, or the produc- tion of gas vacuoles to control their exposure to light that allows them to dominate other phytoplankton during the later months of the season. These cyanobacterial blooms can lead to taste and odor prob- lems in drinking waters and the formation of surface scums. Cyanobacteria can also produce extremely potent toxins and if this occurs, the blooms can be haz- ardous to animals and humans alike. One need only look at their historical names: slow death factor, fast death factor and very fast death factor, to appreciate their effects. Saxitoxin (STX), one of several toxins produced by cyanobacteria, has a lethal dose (LD-50) of approxi- µ mately 8 g per kg body weight and is about 1000 times more toxic than a typical nerve agent such as Figure 1. LandSat image of Microcystis bloom in Western sarin. A recent bloom of Anabaena circinalis from Lake Erie, August 2003 (Rinta-Kanto et al., 2005). -1 Australia contained up to 3,400 µg gdw of STX or related toxins, and was responsible for the death of 1600 cattle and sheep[7]. The microcystin peptides cystin-LR and microcystin-AR [3]. Since that initial produced by Microcystis and numerous other description, toxic Microcystis has continually reoc- cyanobacterial species are potent hepatotoxins. The curred in the western basin of Lake Erie with toxin occurrence of these toxins in drinking water has result- levels often exceeding the WHO advisory level of 1 µg ed in human fatalities and an increased incidence of L-1. These blooms have been studied as part of a liver cancer. The World Health Organization has estab- number of programs (See “For More Information” in lished an advisory threshold of 1 microgram per liter this article.) -1 (µg L ) for drinking waters and prepared an excellent review on the animal and human health aspects of The Microcystis blooms in the western basin of Lake Erie often span large areas and are readily visible from cyanobacterial toxins[6]. outer space (Figure 1). The occurrence of these cyanobacterial blooms represents an important health Cyanobacteria in the Great Lakes issue as the western basin of Lake Erie supplies drink- ing water for several major metropolitan areas (e.g. In 1995, Lake Erie experienced a large bloom of toxic Toledo, Cleveland), and serves as an important recre- cyanobacteria in the western basin. This bloom was ation area for millions of visitors to the Great Lakes caused by the species Microcystis aeruginosa, which area. However this issue is greater than just produced the hepatotoxin microcystin-LR and lesser Microcystis, the microcystins hepatotoxins and the amounts of two minor toxins, demethyl (Asp3) micro- western basin of Lake Erie. Here we review some of Great Lakes Research Review, Volume 7, 2006 2 Boyer the current findings on cyanobacterial toxins from the MELEE and MERHAB programs. Other articles in C y a n o b a c t e r i a this series deal in more depth with the issue of these toxins in Lakes Champlain and the embayments of Lake Ontario. Introduction to Cyanobacterial Toxins Chemically, cyanobacterial toxins fall into several diverse categories. Many phycologists learned the acronym “Anni, Fanni and Mike”, referring to the Microcystis production of anatoxin-a, saxitoxin, and microcystin by Anabaena flos-aquae, Aphanizomenon flos-aquae, and Microcystis aeruginosa. Unfortunately, the situation is much more complicated. In 1988, there were 10 reported microcystins. As of 2005, there were more than 70 different chemically identified microcystins (Figure 2). Microcystins have been reported in many Anabaena kinds of cyanobacteria including Microcystis, Anabaena, Oscillatoria (Planktothrix), Nostoc, Hapalosiphon, Anabaenopsis and new sources are appearing yearly. In addition to the microcystins, there are many closely related peptides such as the nodularins anabaenopeptins, aeruginopeptin, and other bioactive peptides. Many of the microcystin- type peptides are hepatotoxic- toxic to animals’ livers; though their lethal dose (LD-50) is highly dependent Aphanizomenon on the specific amino acids present [10]. For other compounds such as the anabaenapeptins or microginins, their biological activity toward humans is largely unknown. While the general conception is that microcystin-LR is the “major” microcystin pro- duced by cyanobacteria (see Figure 2 for a description of the nomenclature), that generalization is often unjustified when one looks at the microcystin chemi- Oscillatoria cal structure more closely. For example, while micro- cystin-LR was the major congener isolated from the 1996 Lake Erie Microcystis bloom [3], more recent samples have contained a much richer diversity in their toxins present (Boyer, unpublished). Microcystin derivatives vary over 100-fold in their biological activity [10] and human health decisions Anabaenopsis based on the toxicity of microcystin-LR are likely to be in error when the other congeners are considered. Separate from the hepatotoxic peptides are the neuro- toxic alkaloids. These consist of anatoxin-a, anatoxin- a(S), saxitoxin and related analogs (Figure 3). The most important of these compounds from an environ- Gleotrichia mental health aspect is probably anatoxin-a. Anatoxin-a was originally isolated from Anabaena flos- Great Lakes Research Review, Volume 7, 2006 3 Toxic Cyanobacteria in the Great Lakes aquae, but is also reported in A. planktonica, Oscillatoria response criteria to protect human health. The struc- species, and Cylindrospermum [13]. Traditionally turally unrelated compound, anatoxin-a (S), is a natu- thought to primarily occur in North America in the rally occurring organo-phosphate (Figure 3) produced highly eutrophic prairie pothole lakes, in recent years by A. flos-aquae strain NRC 525-17 and a number of anatoxin-a has been associated with the deaths of sev- other Anabaenastrains. It acts as an inhibitor of acetyl- eral dogs that came in contact with low-biomass cholinesterase, a chemical necessary for proper nerve blooms in oligo- or mesotrophic Lake Champlain [1]. function in animals. Significant levels of anatoxin-a have also been report- ed in the Great Lakes [16], particularly in the western Toxic cyanobacteria can also contain the Paralytic basin of Lake Erie where values have exceeded 0.5 µg Shellfish Poisoning (PSP) toxins saxitoxin and neosax- -1 itoxin (Figure 3). These toxins are identical to those L . While these values do not seem high in compar- produced by some “red-tide-forming” marine -1 ison to those observed for microcystins (i.e. 20 µg L ), dinoflagellates, and which accumulate in shellfish they are about 5-fold higher than the values measured that feed on those algae. The PSPtoxins are actually a for Lake Champlain that were associated with the dog large family of 18-24 different analogs that are highly fatalities [15]. variable in their biological activity. Not all of the PSP analogs currently identified in marine dinoflagellates Understanding which organisms produce anatoxin-a, and shellfish have been reported in freshwater their bloom dynamics and the stability of this toxin in cyanobacteria but several of the most toxic such as situ is essential for designing monitoring and saxitoxin, neosaxitoxin, and GTX1-4 have all been A Q u i c k C h e m i s t r y L e s s o n Microcystin Figure 2. The generic chemical structure of a microcystin. Amino acid variations in the core ring occur primarily at the positions 1 and 2. For example, Microcystin-LR has the amino acids leucine (L) and arginine (R) at positions 1 and 2 respectively. Microcystin-RR has arginine at both positions. Nodularins are similar, with the five amino acids Adda-gGlu-Mdhb-bMeAsp-Arg mak- ing up the core ring system (Harada, 1996). Neurotoxic alkaloids Figure 3. The chemical structure of the alkaloid cyanobacteria toxins. Anatoxin-a (ATX-a), anatox- in-a(S) and the PSP family of toxins, including sax- itoxin (STX), neosaxitoxin (N-1- OH-STX), and the sulfated gonyautoxins (GTX1-4) are all neurotoxic. Less toxic PSP analogs include C1 and C2. Cylindrospermopsin (CYL) has hepatotoxic activity similar to the microcystins. αβχδεφγηιϕκλµ Great Lakes Research Review, Volume 7, 2006 4 Boyer reported in freshwater cyanobacteria including Aphanizomenon flos-aquae, Anabaena circinalis, Planktothrix sp., Lyngbya wollei, and a Brazilian isolate of Cylindrospermopsis raciborskii. Cylindrospermopsis raciborskii from Hungary or Australia instead pro- duces the hepatotoxic alkaloid cylindrospermopsin (Figure 3). An outbreak of this organism in the drink- ing water supply on Palm Island, Queensland Australia, led to a severe outbreak of hepatoenteritis among the inhabitants of the island [6]. The toxin cylindrospermopsin has also been reported from Umezakia natansin Japan, and Aphanizomenon ovalispo- rum in Israel [13]. Toxic cylindrospermopsin-forming species are generally associated with semi-tropical or arid environments such as Florida and Arizona but there are increasing reports of C. raciborskii occurring in the temperate zones of Europe and the USA includ- Figure 4: Distribution of microcystin toxins in Lake ing New York and Michigan[9]. Both Erie in August 2003. Three distinct regions of the Cylindrospermopsis and Raphidiopsis species have been lake showed measurable levels of microcystins. identified in the phytoplankton flora of Lake Erie and the toxin cylindrospermopsin was detected in August The Distribution of Cyanobacterial samples collected from Lake Erie. Toxins in Lake Erie Since the initial report of microcystins in the western basin of Lake Erie, a number of research cruises have looked at the distribution of microcystins and other toxins in Lake Erie and nearby Great lakes. Initial reports of microcystins in the western basin of Lake Erie were soon followed by Lake-wide surveys that identified three areas of concern, all with different characteristics (Figure 4). The western basin of Lake Erie is characterized by high biomass blooms of Microcystis aeruginosa that produced microcystins at µ -1 concentrations exceeding 20 g L . The origin of these blooms is unknown, but there have been sugges- tions that they are coming from the region of the Maumee River [2]. They may also be stimulated by the presence of zebra mussels or by recent changes in the light and phosphate regimes in this basin [14, 12]. Asecond area of concern is the region in and around Sandusky Harbor. This region is characterized by high nutrient loads and a vibrant population of cyanobacteria. Microcystisis only one of many species present and the blooms in Sandusky Bay are often dominated by Aphanizomenon and Anabaena species. Microcystins are again present in this region but molecular techniques indicate that the species respon- MERHAB researchers collect samples from Lake sible for toxin production is not Microcystis but rather Erie onboard the USEPA Lake Guardian Planktothrix species [11], (Rinta-Kanto, personal com- munication). Great Lakes Research Review, Volume 7, 2006 5 Toxic Cyanobacteria in the Great Lakes In the eastern basin, toxic blooms have been reported off the Buffalo shoreline but the only documented blooms to our knowledge are in and around Long Point Bay. There again the toxins seem to be associat- ed with Microcystisspecies but there has been very lit- tle sampling for cyanobacterial toxins in the inner basin due to its shallow waters. The extent of these blooms is currently unknown and remains to be investigated. Other Lakes and Other Toxins Microcystin toxins have also been reported in the Saginaw Bay of Lake Huron [14] and in both Hamilton Harbor and the Bay of Quinte of Lake Ontario [5, 8], (S. Watson and G.L. Boyer, unpub- lished). In 2003, a large bloom of toxic Microcystis occurred in the eastern basin of Lake Ontario off of Oswego NY. This bloom produced microcystin con- Figure 5. The occurrence of microcystin toxins in the east- centrations that exceeded the WHO advisory limit of ern basin of Lake Ontario during August 2003. µ -1 Microcystin values for the Oswego Station (OS; 0.93 mg 1 g L and was located very near the Onondaga -1 -1 L ) and Selkirk Shores (SS: 1.1 mg L ) were both near County water intakes (Figure 5). Blooms containing -1 other toxins such as anatoxin-a and cylindrosper- the WHO advisory limit of 1 mg L for drinking water. 1 mopsin have been increasingly reported in the lower Lower levels (0.2-0.4 mg L- ) were observed at Mexico great lakes watershed. Anatoxin-a has been found in Point (MP), Sodus Bay (SB) and Port Bay (PB). basins in Lake Ontario, Lake Champlain and Lake Erie [16]. While the concentration of the other toxins and the neurotoxin anatoxin-a in these systems. µ -1 are often well below the 1 g L advisory threshold These toxins have resulted in a number of animal established for microcystins, they illustrate that the fatalities, though their impacts on humans and move- problem of toxic cyanobacteria in the lower Great ment through the food chain remains to be deter- Lakes goes far beyond simply Microcystis in the west- mined. ern basin of Lake Erie. How the occurrence of this multitude of cyanobacterial toxins in potential drink- References ing water supplies and recreational waters will impact management decisions, as well as their trans- 1. Boyer, G., M. C. Watzin, A. D. Shambaugh, M. F. port through the food chain remains to be deter- Satchwell, B. R. Rosen, and T. Mihuc (2004) The mined. occurrence of cyanobacterial toxins in Lake Champlain. In: "Lake Champlain: Partnerships and Research in the New Millennium. T. Manley, Summary P. Manley, T. Mihuc, Eds., Kluwer Acad, p 241- 257. The presence of Microcystis aeruginosaand the hepato- toxic microcystin was initially reported in the mid- 2. Bridgeman, T. (2005) The Microcystis blooms of 1990s in the western basin of Lake Erie. Since that western Lake Erie (2003-2004). Abstracts, time, the presence of toxigenic or potentially toxic Internal. Assoc. Great Lakes Res. Annual organisms, as well as the chemical identification of a Meeting. Ann Arbor MI, May 2005. number of cyanobacterial toxins, has increased to 3. Brittain, S. M., J. Wang, L. Babcock-Jackson, W. W. include all three basins of Lake Erie as well as Lake Carmichael, K. L. Rinehart, and D. A. Culver Ontario, Lake Huron and Lake Champlain. The pres- (2000) Isolation and characterization of micro- ence of hepatotoxic microcystins has become com- cystins, cyclic heptapeptide hepatotoxins from a mon in these systems and there are confirmed reports Lake Erie Strain of Microcystis aeruginosa. J. Great of both the alkaloid hepatotoxin cylindrospermopsin Lakes Res. 26:241-249. Great Lakes Research Review, Volume 7, 2006 6 Boyer 4. Harada, K. (1996) Chemistry and detection of tions between the zebra mussel, Dreissena poly- microcystins. In: "Toxic Microcystis" M. F. morpha, and the harmful phytoplankter, Watanabe, K. Harida, W. W. Carmichael, and H. Microcystis aeruginosa. Limnol. Oceanogr. 50:896- Fujiki, Eds., CRC Press, Boca Raton, FL, pp. 103- 904. 148. 13. Sivonen, K., and G. Jones (1999) Cyanobacterial 5. Howell, T., L. Heintsch, and J. Winter (2002) Toxins. In: "Toxic Cyanobacteria in Water" I. Abundance and distribution of cyanobacteria in Chorus, and J. Bartram, Eds., World Health Hamilton Harbor and adjoining areas of Lake Organization, London., pp. 41-112. Ontario on September 6 and 20, 2001. Abstract 14. Vanderploeg, Henry A.; Liebig, James R.; presented to Environmental Monitoring and Carmichael, Wayne W.; Agy, Megan A.; Johengen, Reporting Branch, Ontario Ministry of Thomas H.; Fahnenstiel, Gary L.; Nalepa, Environment and Energy. Thomas F. Zebra mussel (Dreissena polymorpha) 6. Kuiper-Goodman, T., I. Falconer, and J. Fitzgerald selective filtration promoted toxic Microcystis (1999) Human Health Aspects. In: "Toxic blooms in Saginaw Bay (Lake Huron) and Lake Cyanobacteria in Water" I. Chorus, and J. Erie. Can. J. Fish. Aquat. Sci., 58(6), 1208-1221. Bartram, Eds., World Health Organization, 15. Yang, X., M. F. Satchwell, and G. L. Boyer (2001) London, pp. 113-153. The identification of anatoxin-a from a toxic blue- 7. Negri, A. P., G. J. Jones, and M. Hindmarsh (1995) green algae bloom in Lake Champlain, USA. In Sheep mortality associated with paralytic shell- Abstracts, Fifth international Conference on Toxic fish poisons from the cyanobacterium Anabaena Cyanobacteria, Noosa Lakes, Queensland, AU. circinalis. Toxicon 33:1321-1329. July 15, 2001. 8. Nicholls, K. H.; Heintsch, L.; Carney, E. (2002) 16. Yang, X (2005) Occurrence of the cyanobacterial Univariate step-trend and multivariate assess- neurotoxin, Anatoxin-a, in the Lower Great ments of the apparent effects of P loading reduc- Lakes. Ph.D. Dissertation. State University of tions and zebra mussels on the phytoplankton of New York College of Environmental Science and the Bay of Quinte, Lake Ontario. J. Great Lakes Forestry. Res., 28(1), 15-31. Rinehart, K. L., M. Namikoshi, and B. Choi (1994) Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). J. Appl. Phycol. 6:159-176. For more information Visit the websites of programs that have 9. Padisak, J. (1997) Cylindrospermopsis raciborskii studied algal blooms in the Great Lakes: (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: The Microbial Ecology of Lake Erie (MELEE) worldwide distribution and review of its ecology. Arch Hydrobiol., Suppl. 107:563-593 Working Group web.bio.utk. edu/wilhelm/melee.htm 10. Rinehart, K.L., M. Namikoshi, and B. Choi (1994) Structure and biosynthesis of toxins from blue- NOAA’s MERHAB-Lower Great Lakes green algae (Cyanobacteria). J. Appl. Pycol. 6:159- Project www. esf.edu/merhab 176. NOAA’s Center of Excellence for Great 11. Rinta-Kanto, J. M., A. J. A. Ouellette, M. R. Twiss, G. L. Boyer, T. Bridgeman, and S. W. Wilhelm Lakes and Human Health at the Great Lakes (2005) Quantification of toxic Microcystis spp. Environmental Research Laboratory during the 2003 and 2004 blooms in western Lake www.glerl.noaa.gov/res/Centers/HumanH Erie using quantitative real-time PCR. Environ. ealth/ Sci. Technol. 39:4198-4205 International Field Year on Lake Erie (IFYLE) 12. Sarnelle, O., A. E. Wilson, S. K. Hamilton, L. B. 2005 Knoll, and D. F. Raikow (2005) Complex interac- www.glerl.noaa.gov/ifyle/ Great Lakes Research Review, Volume 7, 2006 7