VARIATION IN THE HABITAT REQUIREMENTS OF POLLINATING INSECTS IN SEMI-NATURAL MEADOWS TOLMELDAJATE ELUPAIGANÕUDLUSTE MITMEKESISUS POOLLOODUSLIKES KOOSLUSTES AVE LIIVAMÄGI A Thesis for applying for the degree of Doctor of Philosophy in Environmental protection Väitekiri filosoofiadoktori kraadi taotlemiseks keskkonnakaitse erialal Tartu 2014 EESTI MAAÜLIKOOL ESTONIAN UNIVERSITY OF LIFE SCIENCES VARIATION IN THE HABITAT REQUIREMENTS OF POLLINATING INSECTS IN SEMI-NATURAL MEADOWS TOLMELDAJATE ELUPAIGANÕUDLUSTE MITMEKESISUS POOLLOODUSLIKES KOOSLUSTES AVE LIIVAMÄGI A Thesis for applying for the degree of Doctor of Philosophy in Environmental protection Väitekiri fi losoofi adoktori kraadi taotlemiseks keskkonnakaitse erialal Tartu 2014 Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences According to the verdict No 172 of March 27, 2014, the Doctoral Committee of 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 Environmental Protection. Opponent: Prof. Miska Luoto Department of Geosciences and Geography University of Helsinki Helsinki, Finland Supervisor: Prof. Valdo Kuusemets Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences Tartu, Estonia Defence of the thesis: Estonian University of Life Sciences, room 1A5, Kreutzwaldi 5, Tartu. May 9, 2014, at 14:00. The English language was edited by Elsevier language editors and the Estonian language by Kristi Liivamägi. Publication of this thesis 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. © Ave Liivamägi, 2014 ISBN 978-9949-536-25-2 (trükis) ISBN 978-9949-536-26-9 (pdf) CONTENTS LIST OF ORIGINAL PUBLICATIONS .................................................7 ABBREVIATIONS .......................................................................................9 1. INTRODUCTION .................................................................................10 2. REVIEW OF THE LITERATURE ..................................................13 2.1. Relationships between habitat patch characteristics and pollinating insects ...........................................................................13 2.2. Relationships between landscape characteristics and pollinating insects ...........................................................................16 2.3. The threatened specialist butterfl y as surrogate species in conservation planning ....................................................................18 2.3.1. Species description and biology .......................................19 2.3.2. Distribution and status ......................................................20 2.3.3. Habitat requirements .........................................................21 3. AIMS OF THE THESIS ......................................................................22 4. MATERIAL AND METHODS .........................................................23 4.1. Pollinating insect study in Ida-Virumaa ......................................23 4.1.1. Study region and study sites .............................................23 4.1.2. Pollinating insect censuses ...............................................24 4.1.3. Patch and landscape characteristics ................................25 4.1.4. Data analysis .......................................................................25 4.2. Data collection and analysis of Clouded Apollo........................26 5. RESULTS .................................................................................................28 5.1. Pollinating insects in Ida-Virumaa...............................................28 5.1.1. Species richness and abundance of butterfl ies, day- active moths, and bumblebees (Paper I) ........................28 5.1.2. Relationships between habitat patch and landscape characteristics and Lepidoptera (Paper II) ....................29 5.1.3. Relationship between habitat patch and landscape characteristics and bumblebees (Paper III) ...................30 5.1.4. Connectivity patterns between pollinating insects and various factors at the patch and landscape scales (Papers II and III) .............................................................31 5.1.4.1. Butterfl y species richness and abundance .......31 5.1.4.2. Day-active moth species richness and abundance ............................................................33 5.1.4.3. Bumblebee species richness and abundance ..34 5.1.5. Models for the prediction of the richness and abundance of pollinating insect species (Papers II and III) .............................................................35 5.1.5.1. Butterfl ies .............................................................35 5.1.5.2. Day-active moths ................................................36 5.1.5.3. Bumblebees ..........................................................38 5.2. Study of Clouded Apollo ...............................................................39 5.2.1. Distribution of the butterfl y in Estonia (Paper IV) .....39 5.2.2. Habitat preferences of the butterfl y (Paper V) .............41 6. DISCUSSION ..........................................................................................43 6.1. Effects of patch-scale factors on pollinating insects ................43 6.2. Effects of landscape composition on pollinating insects ........44 6.2.1. Proportion of forests ........................................................44 6.2.2. Proportion of meadows ....................................................46 6.2.3. Proportion of arable land and human settlements .......47 6.3. Effects of landscape confi guration on pollinating insects .......48 6.4. Clouded Apollo ...............................................................................49 7. CONCLUSIONS .....................................................................................52 REFERENCES ............................................................................................55 APPENDIX ..................................................................................................66 SUMMARY IN ESTONIAN ....................................................................69 ACKNOWLEDGEMENTS......................................................................72 PUBLICATIONS .........................................................................................73 CURRICULUM VITAE...........................................................................133 ELULOOKIRJELDUS ............................................................................135 LIST OF PUBLICATIONS .....................................................................137 6 LIST OF ORIGINAL PUBLICATIONS The thesis is based on the following articles, which are referred to in the text by their Roman numerals. I. Diaz-Forero, I., Liivamägi, A., Kuusemets, V. & Luig, J. 2010. Pollinator richness and abundance in Northeast Estonia: bumblebees, butterfl ies and day-fl ying moths. Forestry Studies | Metsanduslikud Uurimused 53: 5-14. II. Liivamägi, A., Kuusemets, V., Kaart, T., Luig, J. & Diaz-Forero, I. Infl uence of habitat and landscape on butterfl y diversity of semi-natural meadows within forest-dominated landscapes. Submitted. III. Diaz-Forero, I., Kuusemets, V., Mänd, M., Liivamägi, A., Kaart, T. & Luig, J. 2013. Infl uence of local and landscape factors on bumblebees in semi-natural meadows: a multiple-scale study in a forested landscape. Journal of Insect Conservation 17 (1): 113- 125. IV. Liivamägi, A., Kuusemets, V., Luig, J. & Kask, K. 2013. Changes in the distribution of Clouded Apollo Parnassius mnemosyne (Lepidoptera: Papilionidae) in Estonia. Entomologica Fennica 24 (3): 186-192. V. Kuusemets, V., Meier, K., Luig, J. & Liivamägi, A. 2005. Habitat and landscape structure of Clouded Apollo (Parnassius mnemosyne). Kuchn, E., Thomas, J., Feldmann, R. & Settele, J. (Eds.) Studies on the Ecology and Conservation of Butterfl ies in Europe. Vol.1. General Concepts and Case Studies. Pensoft Publishers, Sofi a- Moscow, p 18-21. 7 Contributions I II III IV V Idea and AL, ID-F, AL, ID-F, AL, ID-F, AL, VK KK, VK study design VK VK VK Data AL, JL, AL, JL, AL, ID-F AL, ID-F AL, ID-F collection KK, VK KK, VK Analysis of AL, ID-F, AL, ID-F, AL, ID-F, AL, VK KK, VK data JL JL, TK JL, MM, TK Manuscript AL, ID-F, AL, ID-F, ID-F, MM, AL, VK KK, VK preparation VK TK, VK TK, VK AL – Ave Liivamägi; ID-F – Isabel Diaz-Forero; JL – Jaan Luig; KK – Kadri Kask (former name Kadri Meier); MM – Marika Mänd; TK – Tanel Kaart; VK – Valdo Kuusemets 8 ABBREVIATIONS AREA Patch area AREA_MN Mean patch area of forest AvCoverFP Average percent cover of the plants in the fl owering stage AvGrassH Average vegetation height ED Edge density ED_LAND Edge density at landscape level FRAC Fractal dimension index GIS Geographic information system IJI Interspersion and juxtaposition index PArLand Proportion of patches that are arable land Pbrushw Proportion of patches that are brushwood PForest Proportion of patches that are forest PHumSet Proportion of patches that are human settlement PMeadows Proportion of patches that are meadow PERIM Perimeter of the patch PLS Partial least squares PRD Patch richness density SHAPE Shape index SHDI Shannon’s diversity index SRFFlowPlants Species richness of fl owering plants 9 1. INTRODUCTION The pollinating insects considered in this thesis are bumblebees (Hymenoptera: Apidae, Bombus spp.), butterfl