INFLUENCE OF ABIOTIC AND BIOTIC FACTORS AT PATCH AND LANDSCAPE SCALE ON BUMBLEBEES (BOMBUS SPP.) IN SEMI-NATURAL MEADOWS ABIOOTILISTE JA BIOOTILISTE FAKTORITE MÕJU KIMALASTE POPULATSIOONIDELE POOLLOODUSLIKEL KOOSLUSTEL: MAASTIKULINE ANALÜÜS ISABEL DIAZ FORERO A Thesis for applying for the degree of Doctor of Philosophy in Environmental Protection Väitekiri filosoofiadoktori kraadi taotlemiseks keskkonnakaitse erialal Tartu 2011 EESTI MAAÜLIKOOL ESTONIAN UNIVERSITY OF LIFE SCIENCES INFLUENCE OF ABIOTIC AND BIOTIC FACTORS AT PATCH AND LANDSCAPE SCALE ON BUMBLEBEES (BOMBUS SPP.) IN SEMI-NATURAL MEADOWS ABIOOTILISTE JA BIOOTILISTE FAKTORITE MÕJU KIMALASTE POPULATSIOONIDELE POOLLOODUSLIKEL KOOSLUSTEL: MAASTIKULINE ANALÜÜS ISABEL DIAZ FORERO A Thesis for applying for the degree of Doctor of Philosophy in Environmental Protection Väitekiri filosoofiadoktori kraadi taotlemiseks keskkonnakaitse erialal Tartu 2011 Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences According to the verdict No 85 of October 31, 2011, the Doctoral Committee of Ag- ricultural 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. Dave Goulson Institute of Biological and Environmental Sciences University of Stirling Stirling, Scotland Supervisors: Prof. Valdo Kuusemets Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences Tartu, Estonia Prof. Marika Mänd 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. December 16, 2011, at 10:00. The English language was edited by Ingrid H. Williams, and the Estonian language by Kadri Kask. 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. © Isabel Diaz Forero, 2011 ISBN 978-9949-484-09-6 To my dear husband and my loving family CONTENTS LIST OF ORIGINAL PUBLICATIONS 9 ABBREVIATIONS 10 1. INTRODUCTION 11 2. REVIEW OF THE LITERATURE 13 2.1. The importance and decline of bumblebees 13 2.2. The use of patch and landscape factors in ecological studies 16 2.3. Habitat quality: definition and importance 17 3. AIMS OF THE STUDY 19 4. MATERIALS AND METHODS 20 4.1 Study region 20 4.2. Bumblebee survey 22 4.3. Patch-scale factors 23 4.3.1. Vegetation structure 23 4.3.2. Spatial characteristics 23 4.4. Landscape-scale factors 24 4.4.1. Landscape composition 24 4.4.2. Landscape configuration 24 4.5. Data analysis 25 5. RESULTS 28 5.1. Total bumblebee species richness and abundance 28 5.1.1. Bumblebee species richness and abundance in northeast Estonia 28 5.1.2. Relations between bumblebees and patch-scale factors (Paper II) 30 5.1.3. Relations between bumblebees and landscape-scale fac- tors (Paper II) 30 5.1.4. Connectivity patterns between bumblebees and the fac- tors at patch and landscape scale (Paper II) 31 5.1.5. Models to predict bumblebee species richness and abun- dance (Paper II) 32 5.2. Relations between long-tongued bumblebees and the factors at patch and landscape scale 34 5.3. Relations between the local abundance of bumblebee species and forest habitats 35 5.3.1. Proportion of forest (Paper IV) 35 5.3.2. Proportion of brushwood (Paper IV) 36 5.3.3. Landscape indices (Paper IV) 37 5.3.4. Joint effects of landscape factors related to forest (Paper IV) 37 6. DISCUSSION 39 6.1. Influence of patch-scale factors on bumblebees 39 6.2. Influence of landscape composition on bumblebees 41 6.3. Influence of landscape configuration on bumblebees 43 6.4. Influence of forest habitats on the local abundance of bumblebee species 45 6.5. Bumblebees as potential indicators of habitat quality 48 7. CONCLUSIONS AND IMPLICATIONS FOR CONSERVATION 50 REFERENCES 53 Appendix 1 61 Appendix 2 63 SUMMARY IN ESTONIAN 66 ACKNOWLEDGEMENTS 68 Publications 69 CURRICULUM VITAE 130 ELULOOKIRJELDUS 132 LIST OF PUBLICATIONS 134 LIST OF ORIGINAL PUBLICATIONS The present thesis is based on the following research papers, which are referred to by their Roman numerals in the text. I Diaz-Forero, I., Liivamägi, A., Kuusemets, V. and Luig J. 2010. Pollinator richness and abundance in Northeast Estonia: bum- blebees, butterflies and day-flying moths. Forestry Studies | Met- sanduslikud Uurimused 53, 5–14. II Diaz-Forero, I., Kuusemets, V., Mänd, M., Liivamägi, A., Kaart, T. and Luig, J. 2011. Influence of local and landscape factors on bumblebees in semi-natural meadows: a multiple-scale study in a forested landscape. Journal of Insect Conservation. (Submitted). III Diaz-Forero, I., Kuusemets, V., Mänd, M. and Luig, J. 2011. Bumblebees as potential indicators for the evaluation of habitat quality. Sustainable Development and Planning V. WIT Trans- actions on Ecology and the Environment. WIT Press. Vol 150, 409-417. IV Diaz-Forero, I., Kuusemets, V., Mänd, M., Liivamägi, A., Kaart, T. and Luig, J. 2011. Effects of forest habitats on the local abundance of bumblebee species: a landscape-scale study. Baltic Forestry 17(2), ISSN 1392-1355. (In press). The papers are reproduced by kind permission of the corresponding journal or publisher. Authors’ contributions to the papers: Paper Idea and study Data Analysis of data Manuscript design collection preparation I ID-F, VK AL, ID-F, JL ID-F, AL ID-F, AL, VK II ID-F, VK, MM AL, ID-F, JL ID-F, AL, MM, TK ID-F, MM, VK, TK III ID-F, VK, MM ID-F, JL ID-F, MM ID-F, MM, VK IV MM, ID-F, VK AL, ID-F, JL ID-F, AL, MM, TK ID-F, MM, VK, TK AL – Ave Liivamägi; ID-F – Isabel Diaz-Forero; JL – Jaan Luig; MM – Marika Mänd; TK – Tanel Kaart; VK – Valdo Kuusemets 9 ABBREVIATIONS AREA patch area AREA_MN-Forest mean patch area of forest ED edge density at patch level ED_Forest edge density of forest ED_LAND edge density at landscape level FRAC fractal dimension index IJI interspersion and juxtaposition index PERIM patch perimeter PLS Partial Least Squares PRD patch richness density SHAPE shape index SHDI Shannon’s diversity index 10 1. INTRODUCTION Bumblebees (Bombus spp.) and other bees are considered a vital element of global biodiversity and an important group of pollinators in agro- ecosystems. They are valuable pollinators of cultivated crops as well as wild plants (Sepp et al. 2004, Goulson et al. 2006, Rundlöf et al. 2008, Knight et al. 2009). Compared with the majority of bees, bumblebees have particularly large and hairy bodies; due to these characteristics, they are well adapted to places with low temperatures (Goulson 2010). That is why bumblebees are mostly found in temperate, alpine and arctic zones. Mainly due to the intensification of farming practices in agriculture, bumblebees and other pollinators have declined (Mänd et al. 2002, Goulson et al. 2006, Holzschuh et al. 2008, Xie et al. 2008). Agricul- tural intensification is characterised by the use of fertilisers and pesti- cides and the reduction of flowering plants; causing the fragmentation of landscapes and the loss of suitable habitats for insects (Krewenka et al. 2011). Agri-environmental schemes are being applied in many European countries to mitigate the negative consequences of the intensification of farming practices on biodiversity. The development of more effective ag- ri-environmental measures has become an issue of great concern among decision makers, mainly due to the growing interest of politicians, farm- ers and consumers in more environmentally-friendly farming practices (Kleijn et al. 2006, Holzschuh et al. 2008). According to Goulson et al. (2011), bumblebees have been well-studied in modern agricultural landscapes of Western Europe, the United King- dom, Japan and North America. However, very little is known about the conservation and ecology of most of the bumblebee species elsewhere (Goulson et al. 2011). Those areas that have been well-studied gener- ally consist of large monoculture fields separated by field margins and small patches of woodland. In contrast, the landscape in Estonia has a very mosaic pattern, where approximately 32% of the whole territory is constituted by agricultural land (Mander and Palang 1994), but only a small proportion is cultivated and it contains many patches of natural habitats (Mänd et al. 2002). Moreover, there is evidence that the propor- tion of forest increased substantially during the 20th century (from 14% to 42%) (Palang et al. 1998). Understanding the associations between bumblebees and the surrounding landscape is relevant for the conserva- tion of this group of pollinators, particularly in countries that have frag- 11 mented landscapes with high proportions of forest and natural habitats. The species abundance and distribution are influenced by processes that occur at multiple spatial scales. Some drivers of biodiversity loss, such as habitat destruction and fragmentation, are likely to operate at large spatial scales (Jones 2011); that is why multiple scale studies are current- ly needed. Even more, conservation strategies may be enhanced when properly defined landscape-scale variables are included (Mazerolle and Villard 1999). Considering that Estonia has a very patchy landscape pattern with a sig- nificant presence of natural and semi-natural habitats (Mänd et al. 2002), the aim of this thesis is to analyse the influence of biotic and abiotic fac- tors, at patch and landscape scale, on bumblebees. At the patch scale, factors that describe the vegetation structure and spatial characteristics of the study sites, such as area, perimeter and shape, were considered. At the landscape scale, a set of factors describing the composition and configuration of the landscape matrix were calculated at various spatial scales. This study was developed to determine which variables should be considered when designing biodiversity conservation strategies and agri- environmental measures for this type of landscape mosaic (i.e., which factors have a greater influence on bumblebees in forested landscapes).