Responses of Algal Populations to Parasitism by Aphelidium Chlorococcarum and Chytrids in an Oregon Sewage Lagoon
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AN ABSTRACT OF THE THESIS OF Wendy W. Woods for the degree of Doctor of Philosophy in Botany and Plant Pathology presented on August 2, 1984. Title: Responses of Algal Populations to Parasitism by Aphelidium chlorococcarum and Chytrids in an Oregon Sewage Lagoon. Redacted for Privacy Abstract approved: Harry K. Phinney The abundance of algal species and their parasites was monitored weekly for two years in a sewage lagoon at the Corvallis Airport, Oregon. During the cooler months, Euglena species were dominant followed by a Chlamydomonas assemblage in the spring and a predominantly Scenedesmus assemblage in the summer and fall. Parasites infected 14 of the 35 most abundant species of algae. An unidentified chytrid parasitized Scenedesmus obliquus, and a Rhizophydium sp. infected Chlamydomonas species. The most common parasite, Aphelidium chlorococcarum Fott, infected 11 species, particularly species of Scenedesmus. Aphelidium chlorococcarum was isolated in culture for morphological and ultrastructuralstudy. Reclassification of Aphelidium as an Olpidiaceous chytridwas recommended. Only very severe infections had a significant impact on host populations and thesewere rare. Aphelidium chlorococcarum infected less than 10% of the host populations most of the year. The most severe infection observed (74%) was followed bya sharp decrease in the population of S. armatus fora month. Other declines after severe parasitism were small and lasted approximately one week. Certain climatological, chemical, and biological factors were related to the occurrence ofsevere infections. Of these, a dense host population favored severe parasitism the most. Increased precipitation was also associated with severe infections in the fall. Responses of Algal Populations to Parasitism by Aphelidium chlorococcarum and Chytrids in an Oregon Sewage Lagoon by Wendy W. Woods A THESIS submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Completed August 2, 1984 Commencement June 1985 APPROVED: Redacted for Privacy Professor of'"Botany and Plant Pathology in charge of major Redacted for Privacy Head of Department of Botany and Plant Pathology Redacted for Privacy Dean of Gradu School Date thesis is presented August 2, 1984 Typed by Christina W. O'Bryan for Wendy W. Woods ACKNOWLEDGEMENTS Many people have contributed to this project. Special thanks are extended tomy advisor, Harry K. Phinney, who stimulatedmy initial interest in algal culture in wastewater, and whose friendship,advice, criticism and support were invaluable. I also wish to thank C. David McIntire foryears of training and encouragement. Thanks also to the other members ofmy committee: Peter Bottomley, William Denison, JoAnn Leong, Ralph Quatrano, Anne Anderson and HughGardner for their guidance. I am grateful to my father, John Weller, for introducing me to natural history atan early age and for his continuing support. William Oswald and Robert McHugh contributed initially to defining thefocus of this project.Howard Whisler and Larry Gauriloff generously offered their time and suggestions for the taxonomy, culture and ultrastructural study of Aphelidium. I am particularly indebted to Abraham Held for a stimulating interchange of ideas and forhis careful critique of the Aphelidium manuscript. Data and assistance provided by the following people and organizations are appreciated. Nutrient analyses were performed by the Corvallis Environmental Protection Agency. Jerry DeKamm furnished the local climatological and light intensitydata. Larry Lamperti and Eben Owens of theCorvallis Wastewater Treatment Plant originally suggestedthe airport sewage lagoon as a study site, providedinformation on the design of the system and dataon the lagoon. Norman Bishop contributed the culturecollection strains of Scenedesmus. Al Soeldner, Jane Knoper and ChrisWeiss did the electron microscopy,and E. K. Fernald photo- graphed the plates. Hollis Fishelson-Holstinewas the statistical consultant and computerprogrammer. For their friendship and support,I especially thank Phil Larsen, Adrian Allen, Amy Rossman, and NancyAllred, who edited the manuscript, and ChrisO'Bryan for her extraordinary typing skills. Renata Fritz translated relevant German researchpapers, and Vontina Gurarie translated the Russian papers. Financial support for this research includedfunds for electron microscopy, computeranalysis, and a teaching assistantship from the Departmentof Botany and Plant Pathology at Oregon State University. Addi- tional funding for computer analysiswas granted by the Oregon State University Research Office. The Agri- cultural Experiment Station anda grant from Sigma Xi provided supplies. TABLE OF CONTENTS Page INTRODUCTION 1 LITERATURE REVIEW 4 Parasites of Freshwater Algae 5 Impact of Chytrids on Algae 12 Environmental Factors That Favor Chytrid Epidemics 17 Summary 28 DESCRIPTION OF SEWAGE LAGOON 31 MATERIALS AND METHODS 34 Selection of Stations and Sampling Procedure 34 Physical and Chemical Data 35 Enumeration of Algae 36 Enumeration of Parasites 38 Taxonomy of the Algae and Parasites 40 Culture and Ultrastructural Study of Aphelidium chlorococcarum 43 RESULTS 46 Physical and Chemical Data 46 Abundance of Algae 54 Abundance of Parasites 67 Description of Parasites 99 DISCUSSION 143 Impact of Aphelidium chlorococcarum on Algae 143 Impact of Parasitism on the Succession of Species in the Lagoon 150 Environmental Factors that Favor Epidemics 153 Conclusions 168 Recommendations for Control of Para- sitism in Large-Scale Cultures of Algae Grown in Sewage 171 BIBLIOGRAPHY 174 APPENDICES 185 Appendix A: Field Notes 185 Appendix B: Abundance of Algae 190 Appendix C: Abundance of Parasites 201 LIST OF FIGURES Figure Page 1. The Corvallis Airport Sewage Lagoon 32 2. Climatic data for 1979 and 1980 at Corvallis, Oregon 47 3. Influent to Pond I 50 4. Effluent from Pond II 51 5. The concentrations of major nutrients in Pond II from July to October, 1980 53 6. Abundance of the total phytoplankton 55 7. Dominant species of phytoplankton in Pond I of the sewage lagoon 65 8. Dominant species of phytoplankton in Pond II of the sewage lagoon 66 9. The abundance of Scenedesmus obliquus and its parasites: Aphelidium chlorococcarum and Chytrid Species 1 70 10. The abundance of Scenedesmus armatus and its parasite, Aphelidium chlorococcarum 74 11. The abundance of Scenedesmus acuminatus and its parasite, Aphelidium chlorococcarum 78 12. The abundance of Actinastrum hantzschii and its parasite, Aphelidium chlorococcarum 80 13. The abundance of Ankistrodesmus falcatus and its parasite, Aphelidium chlorococcarum 82 14. The abundance of Tetraedron minimum and its parasite, Aphelidium chlorococcarum 84 LIST OF FIGURES (continued) Figure Page 15. The abundance of Dictyosphaerium ehrenbergianum and its parasite, Aphelidium chlorococcarum 86 16. The abundance of Pteromonas angulosa and its parasite, Aphelidium chlorococcarum 88 17. The abundance of Pteromonassp. 1 and its parasite, Aphelidium chloro- coccarum 90 18. The abundance of Chlamydomonas pertusa and its parasite, Rhizophydium sp. 92 19. The abundance of Chlamydomonas ovata and its parasite, Rhizophydium sp. 93 20. The total number of Aphelidium chlorococcarum and Chytrid Species 1 zoospores relative to the host abundance and climatic factors each week 96 21. Stages in the infection of Scenedesmus obliquus by Chytrid Species 1 102 22. Aphelidium chlorococcarum observations 106 LIST OF TABLES Table Page 1. Dominant species in Pond I 57 2. Dominant species in Pond II 58 3. Host range of parasites fromthe sewage lagoon 68 4. Summary of the most significantepisodes of parasitism 94 5. Comparative light microscopic traitsof Aphelidium species 115 6. Ultrastructure of Aphelidium, Rozella and Olpidium 123 LIST OF PLATES I. Differential interference contrast micrographs of Aphelidium chloro- coccarum 129 II. Transmission electron micrographs of early stages of infection by A. chlorococcarum parasitizing S. acuminatus 131 III. Electron micrographs of early stages of infection by A. chlorococcarum parasitizing Scenedesmus armatus (III - 1 and 2) and S. obliquus (III - 3 to 6) 133 IV. Electron micrograph of a zoosporan- gium of A. chlorococcarum parasi- tizing S. acuminatus 135 V. Electron micrographs of A. chloro- coccarum parasitizing S. acuminatus: zoosporangium and dead host cells 137 VI. Serial sections through a zoosporan- gium of A. chlorococcarum in a cell of S.obli3uus UT72.. 139 VII. Differential interference contrast micrographs of Rhizophydium sp. infecting Chlamydomonas ovata 141 RESPONSES OF ALGAL POPULATIONS TO PARASITISM BY Aphelidium chlorococcarum AND CHYTRIDS IN AN OREGON SEWAGE LAGOON INTRODUCTION As the world population increases, so does the need for the more efficient use of diminishing resour- ces. Current wastewater treatment methods are expen- sive and waste valuable nutrients which could be recovered by harvesting algae grown in the sewage. Algae are a concentrated source of high quality protein that can produce greater yields per acre than any other agricultural crop (Venkataraman, 1969). Culturing algae in wastewater is appealing since it is inexpen- sive and it simultaneously addresses the issues of waste disposal, nutrient recovery, water purification and new sources of protein. Research on the culture of algae in wastewater began in the 1950's (Oswald et al., 1953). Since then, demonstration ponds have been built in the USA, Israel, India, Australia, the USSR, Singapore and the Philip- pines. A lack