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EESTI MAAÜLIKOOL ESTONIAN UNIVERSITY OF LIFE SCIENCES EPIDEMIOLOGICAL INVESTIGATION OF PINE FOLIAGE DISEASES BY THE USE OF THE NEEDLE TRACE METHOD OKKAJÄLJEMEETODI KASUTAMISEST MÄNNI OKKAHAIGUSTE EPIDEMIOLOOGILISES UURIMISTÖÖS REIN DRENKHAN A Thesis for applying of the degree of Doctor of Philosophy in Forestry Väitekiri filosoofiadoktori kraadi taotlemiseks metsanduse erialal Tartu 2011 Institute of Forestry and Rural Engineering Estonian University of Life Sciences According to verdict No 74 of December 3, 2010 the Doctoral Committee of the Agricultural and Natural Sciences of the Estonian University of Life Sciences has accepted the thesis for the defence of the degree of Doctor of Philosophy in Forestry. Opponent: Dr. Risto Kasanen Faculty of Agriculture and Forestry Department of Forest Sciences Forest Pathology University of Helsinki Helsinki, Finland Supervisor: Dr. Märt Hanso Institute of Forestry and Rural Engineering Estonian University of Life Sciences Defence of the thesis: Estonian University of Life Sciences, room 1A5, Kreutzwaldi 5, Tartu on January 13, 2011, at 10:00. The English language was edited by Mr. Terry Bush (USA), and the Estonian by Tiiu Kukk. Publication of this dissertation is supported by the Estonian University of Life Sciences and by the Doctoral School of Earth Sciences and Ecology created under the auspices of European Social Fund. © Rein Drenkhan, 2011 ISBN 978-9949-426-93-5 CONTENTS LIST OF ORIGINAL PUBLICATIONS .....................................7 ABBREVIATIONS AND SOME DEFINITIONS ......................9 1. INTRODUCTION ...................................................................11 2. REVIEW OF LITERATURE .....................................................14 2.1. History and entity of the Needle Trace Method (NTM) .....14 2.2. Extractable by NTM foliage characteristics and growth rate of Scots pine ................................................................15 2.3. Needle loss related to the growth of Scots pine ...................16 2.4. Hitherto use of the NTM in forest pathology .....................17 2.5. Retrospective needle and growth data series in forest ecology ...............................................................................18 2.6. Lophodermium needle cast and its agent, Lophodermium seditiosum ..........................................................................20 2.7. New alien invasive pathogens .............................................21 2.7.1. Mycosphaerella pini ...................................................21 2.7.2. Mycosphaerella dearnessii ...........................................22 2.7.3. Diplodia pinea ..........................................................23 2.7.4. Cyclaneusma minus ...................................................24 2.8. Climatic excesses as the obvious trigger of the recent inva- sions ...................................................................................24 3. AIMS OF THE STUDY ............................................................27 4. MATERIAL AND METHODS .................................................28 4.1. Study sites and sample sizes ................................................28 4.2. Field and laboratory measurements ....................................31 4.2.1. NTM techniques and tree sampling .........................31 4.2.2. Collection of symptomatic needles and fungal species identifications ....................................................................32 4.2.3. Fungal isolates ..........................................................33 4.2.4. Molecular techniques ...............................................33 4.3. Data analysis ......................................................................34 5. RESULTS ...................................................................................38 5.1. Correlation between the needle sets and growth characteris- tics of Scots pine trees ........................................................38 5.2. The effect of productive foliage on the tree growth .............39 5.3. Needle loss dynamics during the study period ....................42 5.4. Impact of needle loss from productive foliage on the tree growth ...............................................................................42 5.5. Practical use of retrospective needle and weather datasets to distinguish outbreaks of needle pathogens of Scots pine .....45 5.6. New information about different aspects in Lophodermium needle cast epidemiology, extracted from the retrospective needle dataset .....................................................................46 5.7. New alien invasive foliar pathogens and their colonisation process of Estonia ...............................................................53 5.7.1. Mycosphaerella pini ...................................................53 5.7.2. Mycosphaerella dearnessii ...........................................53 5.7.3. Diplodia pinea ..........................................................54 5.7.4. Cyclaneusma minus ...................................................55 6. DISCUSSION ...........................................................................56 6.1. Needle age, productive foliage and growth of Scots pine ....56 6.2. Loss of needles from the productive foliage and its impact on the tree growth ...................................................................58 6.3. Epidemiology of Lophodermium needle cast and the retro- spective needle dataset ........................................................60 6.3.1. Recurring of Lophodermium needle cast epidemics ...60 6.3.2. Seasonal development of Lophodermium needle cast ...60 6.3.3. Forecasting of Lophodermium needle cast epidemics ...61 6.3.4. Highest vulnerable age limit of pine toward Lophoder- mium needle cast ................................................................62 6.3.5. Impact of Lophodermium needle cast and of herbivo- rous insect pests to tree growth ...........................................63 6.4. New foliar diseases of pines and their spreading in Estonia ...64 6.5. Invasive versus native foliar diseases of pines and evaluation of their possible risk in the natural conditions of Estonia ...66 6.5.1. Droughts and invasions ............................................66 6.5.2. Epidemic versus chronic diseases ..............................66 6.6. Future prospects .................................................................68 7. CONCLUSIONS ......................................................................69 REFERENCES ..........................................................................73 SUMMARY IN ESTONIAN .....................................................89 ACKNOWLEDGEMENTS ......................................................97 PUBLICATIONS ......................................................................99 ELULOOKIRJELDUS ............................................................198 CURRICULUM VITAE ..........................................................200 LIST OF PUBLICATIONS .....................................................202 PRESENTATIONS .................................................................205 LIST OF ORIGINAL PUBLICATIONS The thesis is based on the following papers; in the text the references to these papers are given in Roman numerals. The papers in this thesis are reproduced by the kind permission of the publishers. I Drenkhan, R., Kurkela, T., Hanso, M. 2006. The relationship bet- ween the needle age and the growth rate in Scots pine (Pinus sylvest- ris): a retrospective analysis by needle trace method (NTM). Euro- pean Journal of Forest Research 125: 397–405. II Hanso, M., Drenkhan, R. 2007. Retrospective analysis of Lopho- dermium seditiosum epidemics in Estonia. Acta Silvatica & Lignaria Hungarica, Special Edition: 31-45. III Hanso, M., Drenkhan, R. 2008. First observations of Mycosphae- rella pini in Estonia. Plant Pathology 57: 1177. IV Kurkela, T., Drenkhan, R., Vuorinen, M., Hanso, M. 2009. Growth response of young Scots pines to needle loss assessed from productive foliage. Forestry Studies/ Metsanduslikud Uurimused 50: 5–22. V Hanso, M., Drenkhan, R. 2009. Diplodia pinea is a new pathogen on Austrian pine (Pinus nigra) in Estonia. Plant Pathology 58: 797. VI Drenkhan, R., Hanso, M. 2009. Recent invasion of foliage fungi of pines (Pinus spp.) to the Northern Baltics. Forestry Studies / Metsanduslikud Uurimused 51: 49–64. VII Hanso, M., Drenkhan, R. 2010. Epidemiology of Lophodermium needle cast of Scots pine (Pinus sylvestris L.) in Estonia. Forest Pat- hology (manuscript, submitted). The contributions of the authors to the papers were as follows: Paper Original idea Data Data Preparation of and study design collection analysis manuscript I TK, RD, MH RD, TK, MH, MV TK, RD TK, RD, MH II MH, RD RD, MH RD, MH MH, RD III RD, MH RD, MH RD MH, RD IV TK, RD, MH RD, TK, MH, MV TK, RD TK, RD, MH V MH, RD RD RD RD, MH VI RD, MH RD, MH RD MH, RD VII MH, RD RD, MH RD, MH MH, RD RD – Rein Drenkhan, MH – Märt Hanso, TK – Timo Kurkela, MV – Martti Vuorinen. 7 The connections via different subjects between the papers presented in this thesis I 3 1;3 II VII 3 2 3 3 1; 2 1 3 III 2 VI 3 1; 2 2 2 2 IV V 1. Investigation of the impact of needle longevity and of needle loss solely from the productive foliage to the growth characteristics of Scots pine. 2. New alien invasive foliage fungi of pines in Estonia: the fungi (e.g. Mycosphaerella pini et al.), the process of colonisation in the country, the exotic hosts as vectors of new pathogens to the native Scots