Hydrobiologia

, Volume 578, Issue 1, pp 113–129 | Cite as

Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics

  • Maiko Kagami
  • Arnout de Bruin
  • Bas W. Ibelings
  • Ellen Van Donk
Open Access
Phytoplankton Workshop

Abstract

Many phytoplankton species are susceptible to fungal parasitism. Parasitic fungi of phytoplankton mainly belong to the Chytridiomycetes (chytrids). Here, we discuss the progression made in the study of chytrids that parasitize phytoplankton species. Specific fluorescent stains aid in the identification of chytrids in the field. The established culturing methods and the advances in molecular science offer good potential to gain a better insight into the mechanisms of epidemic development of chytrids and coevolution between chytrids and their algal hosts. Chytrids are often considered to be highly host-specific parasites, but the extent of host specificity has not been fully investigated. Chytrids may prefer larger host cells, since they would gain more resources, but whether hosts are really selected on the basis of size is not clear. The dynamics of chytrids epidemics in a number of studies were partly explained by environmental factors such as light, temperature, nutrients, pH, turbulence and zooplankton grazing. No generalization was made about the epidemic conditions; some state unfavorable conditions for the host growth support epidemic development, while others report epidemics even under optimal growth conditions for the host. Phytoplankton is not defenseless, and several mechanisms have been suggested, such as a hypersensitivity response, chemical defense, maintaining a high genetic diversity and multitrophic indirect defenses. Chytrids may also play an important role in food webs, because zoospores of chytrids have been found to be a good food source for zooplankton.

Keywords

Host–parasite interactions Epidemics Host specificity Cell size Defense Food webs 

References

  1. Abeliovich, A., Dikbuck, S. 1977Factors affecting infection of Scenedesmus-obliquus by a Chytridium sp in sewage oxidation pondsApplied and Environmental Microbiology34832836PubMedGoogle Scholar
  2. Alster, A., Zohary, T. 2007Interactions between the bloom-forming dinoflagellate Peridinium gatunense and the chytrid fungus Phlyctochytrium sp.Hydrobiologia578131139Google Scholar
  3. Anderson, S. A., Stewart, A., Allen, G. T. 1995Pseudosphaerita euglenae, a fungal parasite of euglena spp in the mangere oxidation ponds, auckland, new-zealandNew Zealand Journal of Marine and Freshwater Research29371379Google Scholar
  4. Bailey, S., Clokie, M. R. J., Millard, A., Mann, N. H. 2004Cyanophage infection and photoinhibition in marine cyanobacteriaResearch in Microbiology155720725PubMedCrossRefGoogle Scholar
  5. Barr, D. J. S. 1987Isolation, Culture, and Identificaiton of Chytridiales, Spizellomycetales, and HyphochytrialesSoutheastern Publishing CorporationAthens, GAGoogle Scholar
  6. Barr, D. J. S., Hickman, C. J. 1967aChytrids and algae. II. Factors influencing parasitism of Rhizophydium sphaerocarpum on SpirogyraCanadian Journal of Botany45431440Google Scholar
  7. Barr, D. J. S., Hickman, C. J. 1967bChytrids and algae. I. Host-substrate range and morphological variation of species of RhizophydiumCanadian Journal of Botany45423430Google Scholar
  8. Beakes, G. W., Canter, H. M., Jaworski, G. H. M. 1988Zoospore ultrastructure of Zygorhizidium affuens and Z. planktonicum, two chytrids parasitizing the diatom Asterionella-formosaCanadian Journal of Botany6610541067Google Scholar
  9. Beakes, G. W., Canter, H. M., Jaworski, G. H. M. 1992Comparative ultrastructural ontogeny of zoosporangia of Zygorhizidium affuens and Z. planktonicum, chytrid parasites of the diatom Asterionella-formosaMycological Research9610471059Google Scholar
  10. Beakes, G. W., Canter, H. M., Jaworski, G. H. M. 1993Sporangium differentiation and zoospore fine-structure of the chytrid Rhizophydium-planktonicum, a fungal parasite of Asterionella-formosaMycological Research9710591074Google Scholar
  11. Bell, G. 1982The Masterpiece of Nature: The Evolution and Genetics of SexualityUniversity of California PressBerkeley/Los AngelesGoogle Scholar
  12. Bertrand, C., Coute, A., Cazaubon, A. 2004Fungal parasitism of the diatom Asterionella formosa hassall (bacillariophyceae) by ChytridiomycotaAnnales de Limnologie-International Journal of Limnology406369Google Scholar
  13. Blaustein, A. R., Hoffman, P. D., Hokit, D. G., Kiesecker, J. M., Walls, S. C., Hays, J. B. 1994UV repair and resistance to solar UV-b in amphibian eggs—a link to population declinesProceedings of The National Academy of Sciences of The United States of America9117911795PubMedCrossRefGoogle Scholar
  14. Blaustein, A. R., Kiesecker, J. M. 2002Complexity in conservation: lessons from the global decline of amphibian populationsEcology Letters5597608CrossRefGoogle Scholar
  15. Blinn, D. W. 1973Effect of light and temperature on parasitism of Pandorina sp. by Dangeardia-mammillata-b schroder in an arizona mountain lakeJournal of Phycology944CrossRefGoogle Scholar
  16. Blinn, D. W., Button, K. S. 1973Effect of temperature on parasitism of Pandorina sp. by Dangeardia-mammillata-b schroder in an arizona mountain lakeJournal of Phycology9323326CrossRefGoogle Scholar
  17. Bowman, B. H., Taylor, J. W., Brownlee, A. G., Lee, J., Lu, S. D., White, T. J. 1992Molecular evolution of the fungi—relationship of the Basidiomycetes, Ascomycetes, and ChytridiomycetesMolecular Biology and Evolution9285296PubMedGoogle Scholar
  18. Bruning, K. 1991aEffects of phosphorus limitation on the epidemiology of a chytrid phytoplankton parasiteFreshwater Biology25409417CrossRefGoogle Scholar
  19. Bruning, K. 1991bEffects of temperature and light on the population-dynamics of the AsterionellaRhizophydium associationJournal of Plankton Research13707719CrossRefGoogle Scholar
  20. Bruning, K. 1991cFungal parasitism in phytoplankton populationsUniversity of AmsterdamAmsterdamGoogle Scholar
  21. Bruning, K. 1991dInfection of the diatom Asterionella by a chytrid. 1. Effects of light on reproduction and infectivity of the parasiteJournal of Plankton Research13103117CrossRefGoogle Scholar
  22. Bruning, K. 1991eInfection of the diatom Asterionella by a chytrid. 2. Effects of light on survival and epidemic development of the parasiteJournal of Plankton Research13119129CrossRefGoogle Scholar
  23. Bruning, K., Lingeman, R., Ringelberg, J. 1992Estimating the impact of fungal parasites on phytoplankton populationsLimnology and Oceanography37252260Google Scholar
  24. Canter, H. M. 1946Studies on British chytrids. I. Dangeardia mammillata SchrödorTransactions of the British Mycological Society29128134Google Scholar
  25. Canter, H. M. 1947aOn Mysocytium megastomum DeWildemanTransactions of the British Mycological Society318084Google Scholar
  26. Canter, H. M. 1947bStudies on British chytrids. II. Some new monocentric chytridsTransactions of the British Mycological Society3194105Google Scholar
  27. Canter, H. M. 1947cStudies on British chytrids. III. Zygorhizidium willei Löwenthal and Rhizophydium columanaris n. SpTransactions of the British Mycological Society31128135Google Scholar
  28. Canter, H. M. 1949aStudies on British chytrids. V. On Olpidium hyalothecae Scherffel and Olpidium ultriculiforme ScherffelTransactions of the British Mycological Society322229Google Scholar
  29. Canter, H. M. 1949bStudies on British chytrids. VI. Aquatic SynchytriaceaeTransactions of the British Mycological Society326994Google Scholar
  30. Canter, H. M. 1949cStudies on British chytrids. VII. On Phlyctochytrium mucronatum n. spTransactions of the British Mycological Society32236240Google Scholar
  31. Canter, H. M. 1950aFungal parasites of the phytoplankton .I. Studies on British chytrids XAnnals of Botany14263289Google Scholar
  32. Canter, H. M. 1950bStudies on British chytrids. VIII. On Rhizophydium anomalum n. spNew Phytologist4998102CrossRefGoogle Scholar
  33. Canter, H. M. 1950cStudies on British chytrids. XI. Chytridium oedogonii couchTransactions of the British Mycological Society33354358Google Scholar
  34. Canter, H. M. 1951Studies on British chytrids. XII. Fungal parasites of the phytoplankton 2Annals of Botany15129&Google Scholar
  35. Canter, H. M. 1953Annotated list of British aquatic chytridsTransactions of the British Mycological Society36278303Google Scholar
  36. Canter, H. M. 1954Fungal parasites of the phytoplankton. III. The studies on British chytrids. XIIITransactions of the British Mycological Society37111133Google Scholar
  37. Canter, H. M. 1960Fungal parasites of the phytoplankton. V. Chytridiium isthmophilum sp. NovTransactions of the British Mycological Society43660664Google Scholar
  38. Canter, H. M. 1961Studies on British chytrids. XVII. Species occurring on planktonic desmidsTransactions of the British Mycological Society44163176Google Scholar
  39. Canter, H. M. 1966Studies on British chytrids XXV. Chytriomyces heliozoicola sp nov a parasite of Heliozoa in planktonTransactions of the British Mycological Society49633Google Scholar
  40. Canter, H. M. 1967Studies on British chytrids XXVI. A critical examination of Zygorhizidium melosirae canter and Z. planktonicum canterBiological Journal of the Linnean Society608597Google Scholar
  41. Canter, H. M. 1968Studies on British chytrids. XXVII. Rhizophydium fugax sp nov a parasite of Planktonic cryptomonads with additional notes and records of planktonic fungiTransactions of the British Mycological Society51699Google Scholar
  42. Canter, H. M. 1969Studies on British chytrids. XXIX. A taxonomic revision of certain fungi found on the diatom AsterionellaBiological Journal of the Linnean Society62267278Google Scholar
  43. Canter, H. M. 1971On Zygorhizidiu venustrum (Canter) n. comb. together with an illustrated list of chytrids occurring on chrysophycean algaeNova Hedwigia21577597Google Scholar
  44. Canter, H. M. 1972

    A guide to the fungi occurring on planktonic blue-green algae

    Desilachary, T. V. eds. Taxonomy and Biology of Blue-Green AlgaeUniversity of MadrasMadras145158
    Google Scholar
  45. Canter, H. M., Heaney, S. I. 1984Observations on zoosporic fungi of Ceratium spp. in lakes of the English lake district; Importance for phytoplankton population dynamicsNew Phytologist97601612CrossRefGoogle Scholar
  46. Canter, H. M., Ingold, C. T. 1984A chytrid on DacrymycesTransactions of the British Mycological Society82739742Google Scholar
  47. Canter, H. M., Jaworski, G. H. M. 1978Isolation, maintenance and host range studies of a chytrid Rhizophydium-planktonicum Canter emend, parasitic on Asterionella-formosa HassallAnnals of Botany42967979Google Scholar
  48. Canter, H. M., Jaworski, G. H. M. 1979Occurrence of a hypersensitive reaction in the planktonic diatom Asterionella-formosa Hassall parasitized by the chytrid Rhizophydium-planktonicum Canter emend., in cultureNew Phytologist82187206CrossRefGoogle Scholar
  49. Canter, H. M., Jaworski, G. H. M. 1980Some general observations on zoospores of the chytrid Rhizophydium planktonicum Canter emendNew Phytologist84515531CrossRefGoogle Scholar
  50. Canter, H. M., Jaworski, G. H. M. 1981The effect of light and darkness upon infection of Asterionella-formosa Hassall by the chytrid Rhizophydium-planktonicum Canter emendAnnals of Botany471330Google Scholar
  51. Canter, H. M., Jaworski, G. H. M. 1982Some observations on the alga Fragilaria-crotonensis Kitton and its parasitism by 2 chytridiaceous fungiAnnals of Botany49429446Google Scholar
  52. Canter, H. M., Jaworski, G. H. M. 1986A study on the chytrid Zygorhizidium-planktonicum Canter, a parasite of the diatoms Asterionella and SynedraNova Hedwigia43269298Google Scholar
  53. Canter, H. M., Jaworski, G. H. M., Beakes, G. W. 1992Formae speciales differentiation in the chytrid Zygorhizidium planktonicum Canter, a parasite of the diatoms Asterionella and SynedraNova Hedwigia55437455Google Scholar
  54. Canter, H. M., Lund, J. W. G. 1948Studies on plankton parasites .I. Fluctuations in the numbers of Asterionella-formosa Hass in relation to fungal epidemicsNew Phytologist47238261CrossRefGoogle Scholar
  55. Canter, H. M., Lund, J. W. G. 1951Studies on plankton parasites. III. Examples of the interaction between parasitism and other factors determining the growth of diatomsAnnals of Botany15359371Google Scholar
  56. Canter, H. M., Lund, J. W. G. 1953Studies on plankton parasites. II. The parasitism of diatoms with special reference to lakes in the English lake districtTransactions of the British Mycological Society361337Google Scholar
  57. Canter, H. M., Lund, J. W. G. 1968The importance of protozoa in controlling the abundance of planktonic algae in lakesProceedings for Linnean Society of London179203219Google Scholar
  58. Canter, H. M., Lund, J. W. G. 1969Parasitism of planktonic desmids by fungiOsterreichische Botanische Zeitschrift116351377CrossRefGoogle Scholar
  59. Canter, H. M., Willoughby, L. G. 1964A parasitic Blastocladiella from Windermere planktonJournal of Royal Microscopic Society83365372Google Scholar
  60. Canter Lund, H. M., Lund, J. W. G. 1995Freshwater algae: Their microscopic world exploredBiopressUKGoogle Scholar
  61. Cook, P. W. 1963Host range studies of certain Phycomycetes parasitic on desmidsAmerican Journal of Botany50580588CrossRefGoogle Scholar
  62. Bruin, A., Ibelings, B. W., Rijkeboer, M., Brehm, M., Donk, E. 2004Genetic variation in Asterionella formosa (bacillariophyceae): Is it linked to frequent epidemics of host-specific parasitic fungi?Journal of Phycology40823830CrossRefGoogle Scholar
  63. Dicke, M. 1999

    Evolution of induced indirect defence of plants

    Tollrian, R.Harvell, C. D. eds. Ecology and Evolution of Inducible DefensesPrinceton University PressPrinceton6288
    Google Scholar
  64. Doggett, M. S., Porter, D. 1994Observations of Zygorhizidium sp parasitic on Pediastrum-duplexMycologia86199202Google Scholar
  65. Doggett, M. S., Porter, D. 1995Further evidence for host-specific variants in Zygorhizidium-planktonicumMycologia87161171Google Scholar
  66. Doggett, M. S., Porter, D. 1996Sexual reproduction in the fungal parasite, Zygorhizidium planktonicumMycologia88720732Google Scholar
  67. Fabbro, L. D., Duivenvoorden, L. J. 1996Profile of a bloom of the cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) seenaya and subba raju in the fitzroy river in tropical central queenslandMarine and Freshwater Research47685694CrossRefGoogle Scholar
  68. Geller, W., Müller, H. 1981The filtration apparatus of cladocera: Filter mesh-sizes and their implications of food selectivityOecologia49316321CrossRefGoogle Scholar
  69. Gromov, B. V., Mamkaeva, K. A., Pljusch, A. V. 2000Mesochytrium penetrans Gen. Et sp. Nov. (chytridiales)—a parasite of the green alga Chlorococcum minutum (chlorococcales), with an unusual behaviour of the sporangiaNova Hedwigia71151160Google Scholar
  70. Gromov, B. V., Pljusch, A. V., Mamkaeva, K. A. 1999aCultures of Rhizophydium spp. (chytridiales)—parasites of chlorococcalean algaeAlgological Studies95115123Google Scholar
  71. Gromov, B. V., Pljusch, A. V., Mamkaeva, K. A. 1999bMorphology and possible host range of Rhyizophydium algavorum sp. Nov. (chytridiales)—and obligate parasite of algaeProtistology16265Google Scholar
  72. Grover, J. P. 1995Competition, herbivory, and enrichment—nutrient-based models for edible and inedible plantsAmerican Naturalist145746774CrossRefGoogle Scholar
  73. Hamm, C. E., Merkel, R., Springer, O., Jurkojc, P., Maier, C., Prechtel, K., Smetacek, V. 2003Architecture and material properties of diatom shells provide effective mechanical protectionNature421841843PubMedCrossRefGoogle Scholar
  74. Heaney, S. I., Lund, J. W. G., Canter, H. M., Gray, K. 1988Population dynamics of Ceratium spp. in three English lakes, 1945–1985Hydrobiologia161133148CrossRefGoogle Scholar
  75. Holfeld, H. 1998Fungal infections of the phytoplankton: Seasonality, minimal host density, and specificity in a mesotrophic lakeNew Phytologist138507517CrossRefGoogle Scholar
  76. Holfeld, H. 2000aInfection of the single-celled diatom Stephanodiscus alpinus by the chytrid Zygorhizidium: Parasite distribution within host population, changes in host cell size, and host-parasite size relationshipLimnology And Oceanography4514401444Google Scholar
  77. Holfeld, H. 2000bRelative abundance, rate of increase, and fungal infections of freshwater phytoplanktonJournal of Plankton Research22987995CrossRefGoogle Scholar
  78. Ianora, A., Miralto, A., Poulet, S. A., Carotenuto, Y., Buttino, I., Romano, G., Casotti, R., Pohnert, G., Wichard, T., Colucci-D’Amato, L., Terrazzano, G., Smetacek, V. 2004Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatomNature429403407PubMedCrossRefGoogle Scholar
  79. Ibelings, B. W., Bruin, A., Kagami, M., Rijkeboer, M., Brehm, M., Donk, E. 2004Host parasite interactions between freshwater phytoplankton and chytrid fungi (Chytridiomycota)Journal of Phycology40437453Google Scholar
  80. Ichise, S., Wakabayashi, T., Matsuoka, Y., Yamanaka, S., Fujiwara, N., Tanaka, K. 1995A simple method for the estimation of phytoplankton biomass based on cell morphology in Lake BiwaReport of Shiga Prefectural Institute of Public Health and Environmental Science302635Google Scholar
  81. Ingold, C. T. 1940Endocoenbium eudorinae Gen. et sp. Nov., a chytridiaceous fungus parasitizing Eudorina elegans EhrenbNew Phytologist3997103CrossRefGoogle Scholar
  82. Ingold, C. T. 1941Studies on British chytrids. I. Phlyctochytrium proliferum sp. Nov. and Rhizophydium lecythii sp. NovTransactions of the British Mycological Society254148Google Scholar
  83. Ingold, C. T. 1944Studies on British chytrids. II. A new chytrid on Ceratium and PeridiniumTransactions of the British Mycological Society279396Google Scholar
  84. Itakura, S., Imai, I., Itoh, K. 1997“Seed bank” of coastal planktonic diatoms in bottom sediments of Hiroshima Bay, seto inland sea, JapanMarine Biology128497508CrossRefGoogle Scholar
  85. Jewson, D. H. 1992Size-reduction, reproductive strategy and the life-cycle of a centric diatomPhilosophical Transactions of The Royal Society of London Series B-Biological Sciences336191213CrossRefGoogle Scholar
  86. Johns, R. M. 1964A new polyphagus in algal cultureMycologia56441451Google Scholar
  87. Johnson, P. T. J., Chase, J. M. 2004Parasites in the food web: Linking amphibian malformations and aquatic eutrophicationEcology Letters7521526CrossRefGoogle Scholar
  88. Kagami, M., Ibelings, B. W., Bruin, A., Donk, E. 2005Vulnerability of Asterionella formosa to daphnia grazing: Impact of a fungal parasiteVerhandlungen IVL29350354Google Scholar
  89. Kagami, M., Urabe, J. 2001Phytoplankton growth rate as afunction of cell size: an experimental test in Lake BiwaLimnology2111117CrossRefGoogle Scholar
  90. Kagami, M., Urabe, J. 2002Mortality of the planktonic desmid, Staurastrum dorsidentiferum, due to interplay of fungal parasitism and low light conditionsVerhandlungen IVL2810011005Google Scholar
  91. Kagami, M., Donk, E., Bruin, A., Rijkeboer, M., Ibelings, B. W. 2004Daphnia can protect diatoms from fungal parasitismLimnology and Oceanography49680685Google Scholar
  92. Kazama, F. Y. 1972Ultrastructure and phototaxis of zoospores of Phlyctochytrium sp, an estuarine chytridJournal of General Microbiology71555566Google Scholar
  93. Kiørboe, T. 1993Turbulence, phytoplankton cell-size, and the structure of pelagic food websAdvances in Marine Biology, Vol 29 Advances in Marine Biology29172Google Scholar
  94. Koob, D. B. 1966Parasitism of Asterionella formosa Hass by a chytrid in two lakes of Rawah wild area of ColoradoJournal of Phycology24145Google Scholar
  95. Kudoh, S. 1990. Studies on the population control mechanisms of a planktonic diatom, Asterionella formosa Hassall, by fungal parasitism in natural waters. University of Tokyo.Google Scholar
  96. Kudoh, S., Takahashi, M. 1990Fungal control of population-changes of the planktonic diatom Asterionella-formosa in a shallow eutrophic lakeJournal of Phycology26239244CrossRefGoogle Scholar
  97. Kudoh, S., Takahashi, M. 1992An experimental test of host population size control by fungal parasitism in the planktonic diatom Asterionella formosa using mesocosms in a natural lakeArchiv fur Hydrobiologie124293307Google Scholar
  98. Kuhn, S. F., Hofmann, M. 1999Infection of Coscinodiscus granii by the parasitoid nanoflagellate Pirsonia diadema. III. Effects of turbulence on the incidence of infectionJournal of Plankton Research2123232340CrossRefGoogle Scholar
  99. Kumar, C. R. 1978aAuxospore formation in species of the marine diatom Licmophora agardhVeroffentlichungen des Instuts fur Meeresforschungin Bremerhaven171520Google Scholar
  100. Kumar, C. R. 1978bPhysiology of infection of the marine diatom Licmophora by the fungus Ectrogella perforansVeroffentlichungen des Instuts fur Meeresforschungin Bremerhaven17114Google Scholar
  101. Kumar, C. R. 1980An ultrastructural-study of the marine diatom Licmophora-hyalina and its parasite Ectrogella-perforans. 1. Infection of host-cellsCanadian Journal of Botany-Revue Canadienne De Botanique5812801290Google Scholar
  102. Lampert, W. 1974A method for determination of food selection by zooplanktonLimnology and Oceanography18995998CrossRefGoogle Scholar
  103. Legendre, L., Fevre, J. 1991

    From individual plankton cells to pelagic ecosystems and to global biogeochemical cycles

    Demers, S. eds. Particle Analysis in OceanographySpringer-VerlagBerlin261300
    Google Scholar
  104. Leibold, M. A. 1989Resource edibility and the effects of predators and productivity on the outcome of trophic interactionsAmerican Naturalist134922949CrossRefGoogle Scholar
  105. Leibold, M. A. 1996A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence, and diversity patterns in communitiesAmerican Naturalist147784812CrossRefGoogle Scholar
  106. LopezLlorca, L. V., Hernandez, P. 1996Infection of the green alga Oocystis lacustris chod with the chytrid fungus Diplochytridium deltanum (Masters) Karling. An SEM studyMicron27355358CrossRefGoogle Scholar
  107. Lukavsky, J. 1970Phlyctidium scenedesmi, a chytrid destroying an outdoor mass culture of Scenedesmus obliqusNova Hedwigia19775777Google Scholar
  108. Maberly, S. C., Hurley, M. A., Butterwick, C., Corry, J. E., Heaney, S. I., Irish, A. E., Jaworski, G. H. M., Lund, J. W. G., Reynolds, C. S., Roscoe, J. V. 1994The rise and fall of Asterionella-formosa in the south basin of Windermere—analysis of a 45-year series of dataFreshwater Biology311934CrossRefGoogle Scholar
  109. Malone, T. C. 1980

    Algal size

    Morris, I. eds. The Physiological Ecology of PhytoplanktonUniversity of California PressBerkeley/Los Angeles433463
    Google Scholar
  110. Marcogliese, D. J., Cone, D. K. 1997Food webs: A plea for parasitesTrends in Ecology & Evolution12320325CrossRefGoogle Scholar
  111. Masters, M. J. 1971aEcology of Chytridium-deltanum and other fungus parasites on Oocystis sppCanadian Journal of Botany497587CrossRefGoogle Scholar
  112. Masters, M. J. 1971bOccurrence of chytridium-marylandicum on botryococcus-braunii in school of delta marshCanadian Journal of Botany4914791485Google Scholar
  113. Masters, M. J. 1971cOccurrence of phlyctidium-scenedesmi on pediastrum-boryanum and scenedesmus-quadricauda in school bay of delta marshCanadian Journal of Botany4916051608Google Scholar
  114. Masters, M. J. 1976

    Freshwater phycomycetes on algae

    Jones, E. B. G. eds. Recent Advances in Aquatic MycologyElek ScienceLondon489512
    Google Scholar
  115. McQuiod, M. R., Godhe, A., Nordberg, K. 2002Viability of phytoplankton resting stages in the sediment of a coastal Swedish FjordEuropian Journal of Phycology37191201CrossRefGoogle Scholar
  116. Muehlstein, L. K., Amon, J. P., Leffler, D. L. 1988Chemotaxis in the marine fungus Rhizophydium-littoreumApplied and Environmental Microbiology5416681672PubMedGoogle Scholar
  117. Müller-Navarra, D. C., Brett, M. T., Liston, A. M., Goldman, C. R. 2000A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumersNature4037477PubMedCrossRefGoogle Scholar
  118. Müller, U., Sengbusch, P. 1983Visualization of aquatic fungi (Chytridiales) parasitizing on algae by means of induced fluorescenceArchiv fur Hydrobiologie97471485Google Scholar
  119. Murray, A. G. 1995Phytoplankton exudation—exploitation of the microbial loop as a defense against algal virusesJournal of Plankton Research1710791094CrossRefGoogle Scholar
  120. Noble, R. T., Fuhrman, J. A. 1998Use of SYBR green I for rapid epifluorescence counts of marine viruses and bacteriaAquatic Microbial Ecology14113118Google Scholar
  121. Paterson, R. A. 1960Infestation of chytridiaceous fungi on phytoplankton in relation to certain environmental-factorsEcology41416424CrossRefGoogle Scholar
  122. Pohnert, G. 2000Wound-activated chemical defence in unicellular planktonic algaeAngewandte Chemie International Edition3943524354CrossRefGoogle Scholar
  123. Powell, M. J. 1994Production and modifications of extracellular structures during development of ChytridiomycetesProtoplasma181123141CrossRefGoogle Scholar
  124. Puneva, I., Christov, C., Bozhkova, M. 2000The effect of abscisic acid and methyl jasmonate on the host-parasite relationship in the system Scenedesmus acutus Phlyctidium scenedesmiRussian Journal of Plant Physiology47664667Google Scholar
  125. Raghukumar, C. 1986Fungal parasites of the marine green-algae, Cladophora and RhizocloniumBotanica Marina29289297CrossRefGoogle Scholar
  126. Raven, J. A. 1998The twelfth tansley lecture. Small is beautiful: the picophytoplanktonFunctional Ecology12503513CrossRefGoogle Scholar
  127. Raven, J. A., Waite, A. M. 2004The evolution of silicification in diatoms: inescapable sinking and sinking as escape?New Phytologist1624561CrossRefGoogle Scholar
  128. Reynolds, C. S. 1973The seasonal periodicity of planktonic diatoms in a shallow eutrophic lakeFreshwater Biology389110CrossRefGoogle Scholar
  129. Reynolds, C. S. 1984The ecology of freshwater phytoplanktonCambridge University PressCambridgeGoogle Scholar
  130. Richards, M. 1951The life history of Diplophlyctis laevisTransactions of the British Mycological Society34483488Google Scholar
  131. Sen, B. 1987aFungal parasitism of planktonic algae in Shearwater I. Occurrence of Zygorhizidium affluens Canter on Asterionella formosa Hass. in relation to the seasonal periodicity of the algaArchiv fur Hydrobiologie/ Suppliment76101127Google Scholar
  132. Sen, B. 1987bFungal parasitism of planktonic algae in Shearwater II. A study of the chytrid parasites of the diatom Fragilaria crotonensis KittonArchiv fur Hydrobiologie/ Suppliment76129144Google Scholar
  133. Sen, B. 1988aFungal parasitism of planktonic algae in Shearwater. IV. Parasitic occurrence of a new chytrid species on the blue-green algaArchiv fur Hydrobiologie/Suppliment79177184Google Scholar
  134. Sen, B. 1988bFungal parasitism of planktonic algae in Shearwater. III. Fungal parasites of centric diatomsArchiv fur Hydrobiologie/ Suppliment79167175Google Scholar
  135. Sen, B. 1988cFungal parasitism of planktonic algae in shearwater. V. Fungal parasites of the green algaeArchiv fur Hydrobiologie Suppliment79185205Google Scholar
  136. Shin, W., Boo, S. M., Longcore, J. E. 2001Entophlyctis apiculata, a chytrid parasite of Chlamydomonas sp (Chlorophyceae)Canadian Journal of Botany-Revue Canadienne de Botanique7910831089CrossRefGoogle Scholar
  137. Smayda, T. J. 1970The suspension and sinking of phytoplankton in the seaAnnual Review of Oceanography & Marine Biology8353414Google Scholar
  138. Smetacek, V. 1999Diatoms and the ocean carbon cycleProtist1502532PubMedCrossRefGoogle Scholar
  139. Sommer, U. 1987Factors controlling the seasonal variation in phytoplankton species composition—a case study for a deep, nutrient rich lakeProgress in Phycological Research5124178Google Scholar
  140. Sommer, U., Gliwicz, Z. M., Lampert, W., Duncan, A. 1986The PEG-model of seasonal succession of planktonic events in freshwatersArchiv fur Hydrobiologie106433471Google Scholar
  141. Sparrow, F. K. 1936A contribution to our knowledge of the aquatic Phycomycetes of Great BritainBiological Journal of the Linnean Society50417478Google Scholar
  142. Sparrow, F. K. 1952Phytomycetes from the douglas lake region of northern MichiganMycologia44759772Google Scholar
  143. Stein, J. 1973Handbook of Phycological Methods. Culture Methods and Growth MeasurementsCambridge University PressLondonGoogle Scholar
  144. Sterner, R. W. 1989

    The role of grazers in phytoplankton succession

    Sommer, U. eds. Plankton Ecology: Succession in Plankton CommunitiesSpringer-VerlagBerlin107170
    Google Scholar
  145. Strom, S., Wolfe, G., Holmes, J., Stecher, H., Shimeneck, C., Lambert, S., Moreno, E. 2003Chemical defense in the microplankton i: Feeding and growth rates of heterotrophic protists on the DMS-producing phytoplankter Emiliania huxleyiLimnology and Oceanography48217229CrossRefGoogle Scholar
  146. Suttle, C. A., Chan, A. M. 1994Dynamics and distribution of cyanophages and their effect on marine Synechococcus sppApplied and Environmental Microbiology6031673174PubMedGoogle Scholar
  147. Taylor, F. J. 1976Fungal parasite in marine diatom Coscinodiscus-oculus-iridisBotanica Marina196162Google Scholar
  148. Tehler, A., Farris, J. S., Lipscomb, D. L., Kallersjo, M. 2000Phylogenetic analyses of the fungi based on large rDNA data setsMycologia92459474Google Scholar
  149. Donk, E. 1989

    The role of fungal parasites in phytoplankton succession

    Sommer, U. eds. Plankton Ecology: Succession in Plankton CommunitiesSpringer-VerlagBerlin171194
    Google Scholar
  150. Donk, E. 2005Planktonic interactions: developments and perspectivesVerhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie296172Google Scholar
  151. Donk, E., Bruning, K. 1992

    Ecology of aquatic fungi in and on algae

    Reiser, W. eds. Algae and Symbioses—Plants, Animals, Fungi, Interactions ExploredBiopress LimitedBristol567592
    Google Scholar
  152. Donk, E., Lurling, M., Lampert, W. 1999

    Consumer-induced changes in phytoplankton: inducibility, costs, benefits, the impact on grazers

    Tollrian, R.Harvell, C. D. eds. The Ecology and Evolution of Inducible DefensesPrinceton university pressPrinceton89103
    Google Scholar
  153. Donk, E., Ringelberg, J. 1983The effect of fungal parasitism on the succession of diatoms in lake Maarsseveen-I (The Netherlands)Freshwater Biology13241251CrossRefGoogle Scholar
  154. Webster, J. 1970Introduction to FungiCambridge University PressCambridgeGoogle Scholar
  155. White, F. F., Yang, B., Johnson, L. B. 2000Prospects for understanding a virulence gene functionCurrent Opinion in Plant Biology3291298PubMedCrossRefGoogle Scholar
  156. Wilson, W. H., Mann, N. H. 1997Lysogenic and lytic viral production in marine microbial communitiesAquatic Microbial Ecology1395100Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Maiko Kagami
    • 1
    • 2
  • Arnout de Bruin
    • 1
  • Bas W. Ibelings
    • 1
  • Ellen Van Donk
    • 1
  1. 1.Department of Food Web StudiesCenter for Limnology, Netherlands Institute of Ecology (NIOO-KNAW)NieuwersluisThe Netherlands
  2. 2.Department of Environmental Science, Faculty of ScienceToho UniversityFunabashiJapan

Personalised recommendations