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With Special Reference to Its Competitive And THE ECOLOGY OF RHODODENDRON FONTICLNL. WITH SPECIAL REFERENCE TO ITS COMPETITIVE AND INVASIVE CAPABILITIES. by IAN DOUGLAS ROTHERHAM Department of Botany, University of Sheffield Thesis for the Degree of Doctor of Philosophy SEPTEMBER 1983 PLATE 1 : Rhododendron pon ti cum in flower . PLATE 2 : Invasive R.ponticum at Cordwell near Sheffield . DEDICATION To my parents and my brothers, Neil and Stewart. CONTENTS PAGE SUMMARY ACKNOWLEDGEMENTS CHAPTER 1 : INTRODUCTION 1-12 CHAPTER 2 NOTES ON THE STATISTICAL ANALYSIS 2.1 Introduction and spread in Peak and Sheffield Area 13-20 2.2 Spread at 3 sites in the Sheffield area 21-24 CHAPTER 3 MYCORRHIZAL INFECTION IN RHODODENDRON PONTICUM 25-67 Introduction 25-29 Method 30-33 Experimental work and results 34-62 Isolation of the endophyte 34-38 Experiment 1. Effects of mycorrhizal infection on growth of Rhododendron ponticum 39-45 Experiment 2. Effects of mycorrhizal infection on growth of Rhododendron ponticum, with and without nutrient addition 46-53 Occurrence of Rhododendron endophyte in a range of field soils 54-60 Ascocarp formation by Rhododendron endophyte 61-62 Discussion 63-67 CHAPTER 4 THE POSSIBLE IMPORTANCE OF ALLELOPATHY IN THE ECOLOGY OF RHODODENDRON PONTICUM 68-124 Introduction 68-72 Summary of the field observations and experimental work 73 A qualitative comparison of vegetation in Winterton grassland and Winterton Rhododendron interference zone 74 Investigation into residual toxicity of Rhododendron soil and litter 75-87 Investigation into interference caused by Rhododendron under artificial conditions 88-114 Summary in tabular form of the major findings of experiments 3, 4, 5 and 6 114a et seq. Investigation into the interference phenomenon in the field 115-124 CONTENTS PAGE CHAPTER 5 THE OCCURRENCE OF PHENOLIC COMPOUNDS IN RHODODENDRON PONTICUM AND IN ASSOCIATED SOIL, LITTER AND CANOPY THROUGHFALL 125-247 Introduction 125-131 Method 132-135 Quantitative analysis of the 'free' phenolic content of Rhododendron ponticum and of a range of associated higher plant species 136-152 Qualitative analysis of the 'free' phenolic compounds of Rhododendron ponticum 1" 170 Extractions from field and artificial soils 178-218 Aqueous leachate and alkaline ethanolic extraction of field soils 181-192 Extractions from sandy soil and acid-washed sand in pots with and without Rhododendron seedlings 193-216 The collection and analysis of canopy throughfall 219-247 CHAPTER 6 GENERAL DISCUSSION 248-261 REFERENCES APPENDICES (SEE NEXT PAGE) APPENDICES: APPENDIX 1 : EFFECTS OF HEAT TREATMENT ON ENDOPHYTE AND ON SOIL MICROFLORA APPENDIX 2 : SOIL ANALYSIS APPENDIX 3 : BIOASSAY TESTS OF RHODODENDRON CANOPY THROUGHFALL APPENDIX 4 : NUTRIENT SOLUTIONS OR MEDIA USED APPENDIX 5 : PREPARATION OF ACID-WASHED SAND APPENDIX 6 : THE REGENERATION OF VEGETATION IN ARTIFICIAL GAPS WITHIN DENSE RHODODENDRON BUSHES APPENDIX 7 : STATISTICAL ANALYSIS. SUMMARY A survey of the current status of Rhododendron ponticum in the Peak District and Sheffield area was carried out. It was found to be widespread over much of the area, particularly on free-draining, nutrient-poor, acidic soils, in sheltered, moist situations. It was largely absent from the Carboniferous and Magnesian Limestone Series, from the high altitude Kinder/Bleaklow massif and from areas subject to intensive agricultural or industrial development. Disturbance of habitats through forestry, grazing or recreational activity seems to encourage invasion of suitable areas. The role of mycorrhizal infection in R. ponticum was investigated. Mycorrhizal plants had lower Root/Shoot Ratios, higher Relative Growth Rates and showed increased yield compared to non-mycorrhizal plants. The benefits of infection were strongest on nutrient-poor soils without added nutrients. Infection of roots was visible after around six weeks and the effects of mycorrhizas were increasingly apparent during the following six weeks. The source of fungal inoculum was investigated and considered. The 'interference' phenomenon described by earlier workers was investigated. A mixture of competitive and allelopathic influences upon test seedlings in bioassays was demonstrated. The toxicity . found, was closely related to the presence of R. ponticum roots in the soil. Both living or dead roots produced the effects. These were not removed by nutrient addition. Interference was not dependent on mycorrhizal infection of the R. ponticum roots. To help an understanding of the interference demonstrated, a survey was undertaken of the 'free' phenolic compounds occurring in R. ponticum tissues, associated soil and litter, and in canopy throughfall. These compounds have been implicated in allelopathic interactions involving other members of the Ericaceae. R. ponticum tissues were found to have very high concentrations of 'free' phenolic compounds compared to other plant species examined. Considerable variation in form and amount was found with tissue type and age. Phenolic compounds were detected in associated soil and litter, as well as in canopy throughfall from R. ponticum. It was shown that the interference cannot be fully explained by competition for water and/or nutrients. In some situations a toxic influence perhaps due to aromatic and aliphatic acids released from the roots, has a major effect on the interaction between R. ponticum and associated vegetation. Competition for nutrients and/or water clearly occurs in some field situations, particularly when R. ponticum bushes are encroaching on established vegetation. However, with bare-zones (either • in the field or under artificial conditions) competition factors may be almost totally eliminated by the toxicity which inhibits root formation. Since the seedlings have very restricted root development, they are barely able to compete for nutrients or moisture, and the toxic effects dominate the interaction. The natural situation in the field is complicated by the acidification of soils associated with R. ponticum, the physical and chemical effects of its litter, shading and the overall influence of the plant on soils and nutrient cycling. The large quantity of 'free' phenolic compounds in R. ponticum tissues (especially new leaves and new stems) probably have anti-herbivore and/or anti-pathogen functions. This would explain the observed lack of damage to the plant by invertebrate herbivores, diseases or parasites. These compounds would thereby enhance the growth and competitive ability of R. ponticum. The ecological success and invasive nature of R. ponticum may be attributed to a mixture of factors. It has a high fecundity with effective dispersal. The high phenolic content of its tissues gives resistance to attack from invertebrate (and possibly vertebrate) herbivores or diseases. Mycorrhizal infection produces more effective growth under the conditions in which R. ponticum is usually found in the field. The highly competitive ability in favourable habitats may be aided in at least some situations by an allelopathic influence on competing plants. It is a remarkable attribute of R. ponticum that (as demonstrated) it can actively modify its environment to make it more suitable. Through processes such as the acidification of associated soil, the edaphic range exploited by R. ponticum (and indeed other ericaceous plants) is expanded. These factors are discussed, and their importance in terms of the ecological success and invasive nature of R. ponticum as an alien in the British Isles, is assessed. ACKNOWLEDGEMENTS I am indebted to Professor A.J. Willis for the generous provision of laboratory facilities in the Botany Department and to Dr. D.J. Read for the initial idea of this investigation and patient supervision, particularly during the final stages. Dr. M.A.F. Jalal gave invaluable guidance for the work on phenolic compounds. The work was supported by an NERC grant. I would like to thank the many people who helped through access to facilities, to land for research purposes, or by giving advice and information. Thanks particularly to Chatsworth Estates (access to their woodlands), Dr. D.W. Yalden and Penny Anderson (for information on R. ponticum in the west Peak District) and to both the Nature Conservancy Council and Winterton Estates for access to Winterton Dunes. Thanks also to all the staff at Tapton Experimental Gardens, for their cheerful assistance throughout much of the experimental work; to Mr Rob Bradley for technical assistance, to Mr Glynn Woods for help with photography; and to the other technical and clerical staff for . their patient help and advice. Anne E. Speigal helped with the mapping of R. • ponticum at two of the sites. I would like to thank my family and all my friends without whom this work would not have been completed. Most importantly this applies to my parents and my brother Neil. I am particularly grateful to Mike, Martyn and especially Midge, and also to Shafik, Al C. and Pam for their friendship during a difficult period. Finally, my sincere thanks and gratitude to Mrs Denise Thomson for her speedy and efficient typing of the thesis, with such patience and cheerfulness, and particularly at such short notice. 1 CHAPTER 1 INTRODUCTION The status of Rhododendron ponticum in the British Isles and north-west Europe is that of an alien. Now widely naturalized, its invasive nature in both managed and semi-natural habitats, gives it ecological and financial interest. It is an extremely important weed of commercial forest plantations and a threat to some semi-natural oakwoods. The genus Rhododendron is a large group of shrubs in the family Ericaceae. This rather extensive family includes other well-known genera such as Erica, Calluna, Vaccinium and Gaultheria. The family is of almost world-wide distribution. Its largest genus is Rhododendron, with around 1200 species. The bulk of these are found in the Far East where China, Tibet, Burma and Assam all meet. A much smaller number are native to southern Europe and the Middle East. It is this latter group which includes R. ponticum. R. ponticum was divided into two sub-species: R. ponticum ponticum, native to the Mediterranean region around Turkey, Asia Minor and Lebanon, and R: ponticum baeticum occurring in a small area of south-west Spain, central and southern Portugal.
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