Phenological responses of British orchids and their pollinators to climate change: an assessment using herbarium and museum collections Karen M. Robbirt B.Sc., M.Sc. A thesis submitted for the degree of Doctor of Philosophy September 2012 Centre for Ecology, Evolution and Conservation School of Biological Sciences University of East Anglia © This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. 1 Abstract Climate change might de-couple plant-pollinator relationships if species respond differentially to environmental cues, such as temperature, but studies have been hindered by lack of long-term data. This research validates natural history collections as a source of long-term phenological data and, using these data, investigates the phenological responses to temperature of flowering in British orchids and flight in their pollinators. Herbarium specimens of O. sphegodes collected in the UK between 1848 and 1958 were compared to direct observation of peak flowering time in one population located in Southern England between 1975 and 2006. The response of flowering time to variation in mean spring temperature was statistically identical in both sets of data, providing the first direct validation of the use of herbarium collections to examine the relationships between phenology and climate. Using three important pollinator models: the solitary bee Andrena nigroaenea the digger wasp Argogorytes mystaceus, and the moth Euclidia glyphica, museum specimens and field observation gave statistically identical results, confirming the value of museum collections as a source of long-term phenological data for insects. For twelve of the fifteen orchid species studied, flowering advanced between 4.2 and 8.6 days for each 1°C increase in mean spring temperature, establishing phenological signals of flowering response to temperature. For all species mean monthly temperature in March, April or May was identified as a key temperature variable. For the sexually deceptive orchid O. sphegodes there is considerable potential for a loss of synchrony between peak flowering time and peak flight of the primary pollinator, males of A. nigroaenea with further rises in spring temperature. The advancement in peak flight of the female bee with climate warming exacerbates the potential for disruption of pollination success. Findings of this research reaffirm the need for detailed knowledge at species level in understanding the consequences of climate-driven phenological shifts for plants and their pollinators. Key words: Central England Temperature (CET), climate change, flight time, flowering time, herbarium specimens, Hymenoptera, Lepidoptera, museum records, natural history collections, Orchidaceae, phenology 2 Contents Acknowledgements.......................................................................................................11 Published paper from this thesis....................................................................................12 Chapter 1 1.1 Background to the phenology of orchids and their pollinators................ 13 1.1.1 Climate change and phenology................................................................ 13 1.1.2 Datasets for phenological research........................................................... 16 1.1.3 The role of herbaria and museum collections........................................... 17 1.1.4 Plant-pollinator biology within the Orchidaceae..................................... 18 1.1.5 Food deception......................................................................................... 19 1.1.6 Sexual deception...................................................................................... 20 1.1.7 Orchid species within the UK.................................................................. 20 1.2 Thesis outline........................................................................................... 21 1.2.1 Theme and Hypothesis........................................................................... 21 1.2.2 Thesis aims............................................................................................... 22 1.2.3 Thesis structure........................................................................................ 23 1.3 Orchid and pollinator species in this study.............................................. 25 1.4 References................................................................................................ 26 Chapter 2 2.1 Introduction............................................................................................. 33 2.2 Methods................................................................................................... 35 2.2.1 The study species...................................................................................... 35 2.2.2 Herbarium data......................................................................................... 37 2.2.3 Field data.................................................................................................. 39 2.2.4 Meteorological data.................................................................................. 40 2.2.5 Geographical variation............................................................................. 42 2.2.6 Analysis.................................................................................................... 42 2.3 Results...................................................................................................... 43 2.3.1 Herbarium data......................................................................................... 43 2.3.2 Field data.................................................................................................. 44 2.3.3 Comparing herbarium and field-based data for flowering response........ 47 2.3.4 Geographical effects................................................................................. 48 2.3.5 Using herbarium data to predict flowering phenology............................. 50 2.4 Discussion................................................................................................ 51 2.5 References................................................................................................ 56 Chapter 3 3.1 Introduction............................................................................................. 60 3.2 Methods................................................................................................... 61 3.2.1 Herbarium data......................................................................................... 61 3.2.2 The study species...................................................................................... 64 3.2.3 Meteorological data.................................................................................. 80 3.2.4 Geographical effects................................................................................. 80 3.2.5 Analysis.................................................................................................... 80 3.3. Results...................................................................................................... 81 3.3.1 Quality of herbarium data........................................................................ 81 3.3.2 Median and range of flowering times....................................................... 81 3 3.3.3 Correlation analysis.................................................................................. 84 3.3.4 Multiple regression analysis..................................................................... 91 3.3.5 Linear regression analysis........................................................................ 93 3.4 Discussion................................................................................................ 103 3.5 References................................................................................................ 109 Chapter 4 4.1 Introduction............................................................................................. 116 4.2 Methods................................................................................................... 118 4.2.1 The study species...................................................................................... 118 4.2.2 Museum and herbarium data.................................................................... 120 4.2.3 Field observations of insects.................................................................... 122 4.2.4 Meteorological data.................................................................................. 123 4.2.5 Geographical effects................................................................................. 124 4.2.6 Analysis.................................................................................................... 124 4.3 Results...................................................................................................... 127 4.3.1 Correlation and multiple regression analysis.......................................... 127 4.3.2 The Ophrys sphegodes-Andrena nigroaenea pollination system............. 131 4.3.3 The Ophrys insectifera-Argogorytes mystaceus pollination system........ 136 4.3.4 Correspondence between flying and flowering dates.............................. 138 4.4 Discussion...............................................................................................