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Macroalgal and Cyanobacterial Chemical Defenses in Freshwater Communities

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Algal Chemical Ecology

Algae and cyanobacteria are important sources of primary production in freshwater systems and they figure prominently in estimates of carbon budgets, dissolved oxygen concentration, and nutrient recycling in those habitats (Howarth et al. 1988; Schippers et al. 2004). In recent years, these groups have garnered much negative attention as a result of their ability to dominate aquatic systems receiving chronic nutrient inputs. Freshwater blooms of these photoautotrophs have been shown to be positively influenced by an array of abiotic factors, including low N:P ratios, low light levels, high pH, and stratification of the water column (Elser 1999; Paerl et al. 2001). Nevertheless, there has been a growing understanding that biologically active secondary metabolites also play a role in mediating the persistence of these outbreaks by deterring herbivores and shifting grazing pressure toward chemically undefended species (Sterner 1989).

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References

  • Allen TF (1882) On some American forms of Chara coronata. Am Nat 16:358–369

    Article  Google Scholar 

  • Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91

    Article  CAS  Google Scholar 

  • Anthoni U, Nielsen PH, Smith-Hansen L, Wium-Andersen S, Christophersen C (1987) Charamin, a quaternary ammonium ion antibiotic from the green alga Chara globularis. J Org Chem 52:694–695

    Article  CAS  Google Scholar 

  • Aronstam RS, Witkop B (1981) Anatoxin-a interactions with cholinergic synaptic molecules. Proc Natl Acad Sci USA 78:4639–4643

    Article  PubMed  CAS  Google Scholar 

  • Babica P, Bláha L, Maršálek B (2006) Exploring the natural role of microcystins: a review of effects on photoautotrophic organisms. J Phycol 42:9–20

    Article  Google Scholar 

  • Batista T, de Sousa G, Suput JS, Rahmani R, Suput D (2003) Microcystin-LR causes the collapse of actin filaments in primary human hepatocytes. Aquat Toxicol 65:85–91

    Article  PubMed  CAS  Google Scholar 

  • Berger J, Schagerl M (2003) Allelopathic activity of Chara aspera. Hydrobiologia 501:109–115

    Article  CAS  Google Scholar 

  • Burks RL, Lodge DM (2002) Cued in: advances and opportunities in freshwater chemical ecology. J Chem Ecol 28:1901–1917

    Article  PubMed  CAS  Google Scholar 

  • Camacho FA, Thacker RW (2006) Amphipod herbivory on the freshwater cyanobacterium Lyngbya wollei: chemical stimulants and morphological defenses. Limnol Oceanogr 51:1870–1875

    Article  CAS  Google Scholar 

  • Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 2780:78–86

    Article  Google Scholar 

  • Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “the cyanoHABs”. Hum Ecol Risk Assess 7:1393–1407

    Article  Google Scholar 

  • Carmichael WW, Azevedo SFMO, An JS, Molica RJR, Jochimsen EM, Lau S, Rinehart KL, Shaw GR, Eaglesham GK (2001) Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ Health Persp 109:663–668

    Article  CAS  Google Scholar 

  • Codd GA, Bell SG, Kaya K, Ward CJ, Beattie KA, Metcalf JS (1999) Cyanobacterial toxins, exposure routes and human health. Eur J Phycol 34:405–415

    Article  Google Scholar 

  • Cronin G, Hay M (1996) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301

    Article  Google Scholar 

  • Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951

    Article  PubMed  CAS  Google Scholar 

  • DeMott WR, Moxter F (1991) Foraging on cyanobacteria by copepods: responses to chemical defenses and resource abundance. Ecology 72:1820–1834

    Article  Google Scholar 

  • DeMott WR, Zhang Q, Carmichael WW (1991) Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol Oceanogr 36:1346–1357

    Article  CAS  Google Scholar 

  • Dodds WK (1991) Community interactions between the filamentous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and epiphyte grazers. Oecologia 85:572–580

    Article  Google Scholar 

  • Dodds WK, Gudder DA (1992) The ecology of Cladophora. J Phycol 28:415–427

    Article  Google Scholar 

  • Elser JJ (1999) The pathway to noxious cyanobacterial blooms in lakes: the foodweb as the final turn. Freshwater Biol 42:537–543

    Article  Google Scholar 

  • Froscio SM, Humpage AR, Burcham PC, Falconer IR (2003) Cylindrospermopsin-induced protein synthesis inhibition and its dissociation from acute toxicity in mouse hepatocytes. Environ Toxicol 18:243–251

    Article  PubMed  CAS  Google Scholar 

  • Fulton III RS, Paerl HW (1987) Toxic and inhibitory effects of the blue-green alga Microcystis aeruginosa on herbivorous zooplankton. J. Plankton Res 9:837–855

    Article  Google Scholar 

  • Gilbert JJ (1990) Differential effects of Anabaena affinis on cladocerans and rotifers: mechanisms and implications. Ecology 71:1727–1740

    Article  Google Scholar 

  • Giovannardi S, Pollegioni L, Pomati F, Rossetti C, Sacchi S, Sessa L, Calamari D (1999) Toxic cyanobacterial blooms in Lake Varese (Italy): a multidisciplinary approach. Environ Toxicol 14:127–134

    Article  CAS  Google Scholar 

  • Graham LE, Wilcox LW (2000) Algae. Prentice-Hall, New Jersey

    Google Scholar 

  • Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339

    Article  Google Scholar 

  • Haney JF, Sasner JJ, Ikawa M (1995) Effects of products released by Aphanizomenon flos-aquae and purified saxitoxin on the movements of Daphnia carinata. Limnol Oceanogr 40:263–272

    Article  CAS  Google Scholar 

  • Hansson, LA, Gustafsson S, Rengefors K, Bomark L (2007) Cyanobacterial chemical warfare affects zooplankton community composition. Freshwater Biol 52:1290–1301

    Article  CAS  Google Scholar 

  • Harvell CD (1986) The ecology and evolution of inducible defenses in a marine bryozoan: cues, costs, and consequences. Am Nat 128:810–823

    Article  Google Scholar 

  • Hay ME, Duffy JE, Fenical W (1990) Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant’s clothing. Ecology 71:733–743

    Article  Google Scholar 

  • Horner RA, Garrison DL, Plumley FG (1997) Harmful algal blooms and red tide problems on the U.S. West Coast. Limnol Oceanogr 42:1076–1088

    Article  Google Scholar 

  • Howarth RW, Marino R, Lane J, Cole JJ (1988) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnol Oceanogr 33:669–687

    Article  CAS  Google Scholar 

  • Irfanullah HM, Moss B (2005) Allelopathy of filamentous algae. Hydrobiologia 543:169–179

    Article  Google Scholar 

  • Izaguirre G, Hwang CJ, Krasner SW, McGuire MJ (1982) Geosmin and 2-methylisoborneol from cyanobacteria in three water supply systems. Appl Environ Microbiol 43:708–714

    PubMed  CAS  Google Scholar 

  • Jang M, Ha K, Joo G, Takamura N (2003) Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biol 48:1540–1550

    Article  Google Scholar 

  • Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286

    Article  Google Scholar 

  • Kao CY, Nishiyama A (1965) Actions of saxitoxin on peripheral neuromuscular systems. J Physiol 180:50–66

    PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Kearns KD, Hunter MD (2000) Green algal extracellular products regulate antialgal toxin production in a cyanobacterium. Environ Microbiol 2:291–297

    Article  PubMed  CAS  Google Scholar 

  • Kearns KD, Hunter MD (2001) Toxin-producing Anabaena flos-aquae induces settling of Chlamydomonas reinhardtii, a competing motile alga. Microb Ecol 42:80–86

    PubMed  CAS  Google Scholar 

  • Keating KI (1977) Allelopathic influence on blue-green bloom sequence in a eutrophic lake. Science 196:885–887

    Article  PubMed  CAS  Google Scholar 

  • Komárek J, Kling H (2003) Filamentous cyanobacteria. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America: ecology and classification. Academic, San Diego, CA, pp 117–196

    Chapter  Google Scholar 

  • Kotak BG, Zurawell RW, Prepas EE, Holmes CFB (1996) Microcystin-LR concentration in aquatic food web compartments from lakes of varying trophic status. Can J Fish Aquatic Sci 53:1974–1985

    Article  CAS  Google Scholar 

  • Krienitz L, Ballot A, Kotut K, Wiegand C, Pütz S, Metcalf JS, Codd GA, Pflugmacher S (2003) Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya. FEMS Microb Ecol 43:141–148

    Article  CAS  Google Scholar 

  • Krivan V, Vrkoc I (2000) Patch choice under predation hazard. Theor Popul Biol 58:329–340

    Article  PubMed  CAS  Google Scholar 

  • Kuiper-Goodman T, Falconer I, Fitzgerald J (1999) Human health aspects. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. WHO, E & FN Spon, London, pp 113–153

    Google Scholar 

  • Leflaive J, Ten-Hage L (2007) Algal and cyanobacterial secondary metabolites in freshwaters:. a comparison of allelopathic compounds and toxins. Freshwater Biol 52: 199–214

    Article  CAS  Google Scholar 

  • Legrand C, Rengefors K, Fistarol GO, Granéli E (2003) Allelopathy in phytoplankton. – biochemical, ecological and evolutionary aspects. Phycologia 42:406–419

    Article  Google Scholar 

  • Lembi CA (2003) Control of nuisance algae. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America: ecology and classification. Academic, San Diego, CA, pp 805–834

    Chapter  Google Scholar 

  • Lipkin GM, Fozzard HA (1994) A structural model of the tetrodotoxin and saxitoxin binding site of the Na+ channel. Biophys J 66:1–13

    Article  Google Scholar 

  • Lürling M, van Geest G, Scheffer M (2006) Importance of nutrient competition and allelopathic effects in suppression of the green alga Scenedesmus obliquus by the macrophytes Chara, Elodea and Myriophyllum. Hydrobiologia 556:209–220

    Article  CAS  Google Scholar 

  • Meeks JC (1998) Symbiosis between nitrogen-fixing cyanobacteria and plants. BioScience 48:266–276

    Article  Google Scholar 

  • Moffitt MC, Neilan BA (2004) Characterization of the nodularin synthetase gene cluster and proposed theory of the evolution of cyanobacterial hepatotoxins. Appl Environ Microbiol 70:6353–6362

    Article  PubMed  CAS  Google Scholar 

  • Mohamed ZA (2002) Allelopathic activity of Spirogyra sp.: stimulating bloom formation and toxin production by Oscillatoria agardhii in some irrigation canals, Egypt. J Plankton Res 24:137–141

    Article  CAS  Google Scholar 

  • Mulderij G, Van Donk E, Roelofs JGM (2003) Differential sensitivity of green algae to allelopathic substances from Chara. Hydrobiologia 491:261–271

    Article  Google Scholar 

  • Negri AP, Jones GJ (1995) Bioaccumulation of paralytic shellfish poisoning (PSP) toxins from the cyanobacterium Anabaena circinalis by the freshwater mussel Alythria condola. Toxicon 33:667–678

    Article  PubMed  CAS  Google Scholar 

  • Negri AP, Jones GJ, Blackburn SI, Oshima Y, Onodera H (1997) Effect of culture and bloom development and of sample storage on paralytic shellfish poisons in the cyanobacterium Anabaena circinalis. J Phycol 33:26–35

    Article  CAS  Google Scholar 

  • Newman RW (1991) Herbivory and detritivory on freshwater macrophytes by invertebrates:. a review. J N Am Benthol Soc 10:89–114

    Article  Google Scholar 

  • Oberemm A, Becker J, Codd GA, Steinberg C (1999) Effects of cyanobacterial toxins and aqueous crude extracts of cyanobacteria on the development of fish and amphibians. Environ Toxicol 14:77–88

    Article  CAS  Google Scholar 

  • Onodera H, Oshima Y, Henriksen P, Yasumoto T (1997) Confirmation of anatoxin-a(s) in the cyanobacterium Anabaena lemmermanni as the cause of bird kills in Danish lakes. Toxicon 35:1645–1648

    Article  PubMed  CAS  Google Scholar 

  • Onodera H, Satake M, Oshima Y, Yasumoto T, Carmichael WW (1997) New saxitoxin analogues from the freshwater cyanobacterium Lyngbya wollei. Nat Toxins 5:146–151

    Article  PubMed  CAS  Google Scholar 

  • Paerl HW, Fulton III RS, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci World 1:76–113

    CAS  Google Scholar 

  • Pouria S, de Andrade A, Barbosa J, Cavalcanti R, Barreto V, Ward C, Preiser W, Poon G, Neild G, Codd G (1998) Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. Lancet 352:21–26

    Article  PubMed  CAS  Google Scholar 

  • Preußel K, Stüken A, Wiedner C, Chorus I, Fastner J (2006) First report of cylindrospermopsin producing Aphanizomenon flos-aquae (Cyanobacteria) from two German lakes. Toxicon 47:156–162

    Article  PubMed  CAS  Google Scholar 

  • Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Vaitomaa J, Börner T, Sivonen K (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci USA 101:568–573

    Article  PubMed  CAS  Google Scholar 

  • Reisner M, Carmeli S, Werman M, Sukenik A (2004) The cyanobacterial toxin cylindrospermopsin inhibits pyrimidine nucleotide synthesis and alters cholesterol distribution in mice. Toxicol Sci 82:620–627

    Article  PubMed  CAS  Google Scholar 

  • Resh VH, Houp RE (1986) Life history of the caddisfly Dibusa angata and its association with the red alga Lemanea australis. J N Am Benthol Soc 5:28–40

    Article  Google Scholar 

  • Rinehart KL, Harada K, Namikoshi M, Chen C, Harvis CA, Munro MHG, Blunt JW, Mulligan PE, Beasley VR, Dalhem AM, Carmichael WW (1988) Nodularin, microcystin, and the configuration of Adda. J Am Chem Soc 110:8557–8558

    Article  CAS  Google Scholar 

  • Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50:1565–1570

    Google Scholar 

  • Sasner JJ, Ikawa M, Foxall TL (1984) Studies on Aphanizomenon and Microcystis toxins. In: Ragelis EP (ed) Seafood toxins. American Chemical Society, Washington, DC, pp 391–406

    Chapter  Google Scholar 

  • Schagerl M, Unterrieder I, Angelier DG (2002) Allelopathy among Cyanoprokaryota and other algae originating from Lake Neusiedlersee (Austria). Int Rev Hydrobiol 87:365–374

    Article  Google Scholar 

  • Schippers P, Lürling M, Scheffer M (2004) Increase of atmospheric CO2 promotes phytoplankton productivity. Ecol Lett 7:446–451

    Article  Google Scholar 

  • Schopf JW (2000) The fossil record: tracing the roots of the cyanobacterial lineage. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic, Netherlands, pp 13–35

    Google Scholar 

  • Seifert M, McGregor G, Eaglesham G, Wickramasinghe W, Shaw G (2007) First evidence for the production of cylindrospermopsin and deoxy-cylindrospermopsin by the benthic freshwater cyanobacterium Lyngbya wollei (Farlow ex Gomont) Speziale and Dyck. Harmful Algae 6:73–80

    Article  CAS  Google Scholar 

  • Sheath RG (2003) Red Algae. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America: ecology and classification. Academic, San Diego, CA, pp 197–224

    Chapter  Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. WHO, E & FN Spon, London, pp 41–111

    Google Scholar 

  • Sklenar KS, Horne AJ (1999) Effect of the cyanobacterial metabolite geosmin on growth of a green alga. Water Sci Tech 40:225–228

    CAS  Google Scholar 

  • Stal LJ (2000) Cyanobacterial mats and stromatolites. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic, Netherlands. pp 61–120

    Google Scholar 

  • Sterner RW (1989) Resource competition during seasonal succession toward dominance by cyanobacteria. Ecology 70:229–245

    Article  Google Scholar 

  • Stibor H, Navarra DM (2000) Constraints on the plasticity of Daphnia magna influenced by fish-kairomones. Func Ecol 14:455–459

    Article  Google Scholar 

  • Thacker RW, McLeod AM, McLeod SW (2005) Herbivore-induced saxitoxin production in the freshwater cyanobacterium Lyngbya wollei. Algol Studies 117:415–425

    Article  Google Scholar 

  • Thacker RW, Starnes S (2003) Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponges, Dysidea spp. Mar Biol 142:643–648

    CAS  Google Scholar 

  • Thomas P, Stephens M, Wilkie G, Amar M, Lunt GG, Whiting P, Gallagher T, Pereira E, Alkondon M, Albuquerque EX, Wonnacott S (1993) (+)-Anatoxin-a is a potent agonist at neuronal nicotinic acetylcholine receptors. J Neurochem 60:2308–2311

    Article  PubMed  CAS  Google Scholar 

  • Vagnoli L, Margheri MC, Allotta G, Materassi R (1992) Morphological and physiological properties of symbiotic cyanobacteria. New Phytol 120:243–249

    Article  CAS  Google Scholar 

  • Van Dolah FM (2000) Marine algal toxins: origins, health effects, and their increased occurrence. Environ Health Persp 108:1132–1136

    Google Scholar 

  • Watson SB (2003) Cyanobacterial and eukaryotic algal odour compounds: signals or by-products? A review of their biological activity. Phycologia 42:332–350

    Article  Google Scholar 

  • Wehr JD (2003) Brown algae. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America: ecology and classification. Academic, San Diego, CA, pp 757–773

    Chapter  Google Scholar 

  • Whitton BA, Potts M (2000) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic, Netherlands

    Google Scholar 

  • WHO (World Health Organization) (2003) Guidelines for safe recreational water environments, vol 1: Coastal and freshwaters. WHO, Geneva

    Google Scholar 

  • Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Phil Trans R Soc Lond B 355:1205–1208

    Article  CAS  Google Scholar 

  • Zurawell RW, Chen H, Burke JM, Prepas EE (2005) Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. J Toxicol Env Heal B 8:1–37

    Article  CAS  Google Scholar 

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  1. Marine Laboratory, University of Guam, UOG Station, 96923, Mangilao, GU, USA

    Frank A. Camacho

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  1. University of Alabama at Birmingham, 35294-1170, Birmingham, AL, USA

    Charles D. Amsler

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Camacho, F.A. (2008). Macroalgal and Cyanobacterial Chemical Defenses in Freshwater Communities. In: Amsler, C.D. (eds) Algal Chemical Ecology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-74181-7_5

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