UK Biodiversity Indicators 2015 This documents supports D1c. Status of pollinating Insects Technical background document: Gary D. Powney, Tom A. August, Colin A. Harrower, Charlotte Outhwaite, Nick J.B. Isaac For further information on D1c. Status of pollinating insects visit http://jncc.defra.gov.uk/page-6851 For further information on the UK Biodiversity Indicators visit http://www.jncc.gov.uk/page-1824 D1c. Biodiversity and Ecosystem Services – Status of pollinating insects – technical background document Gary D. Powney, Tom A. August, Colin A. Harrower, Charlotte Outhwaite, Nick J. B. Isaac INTRODUCTION Pollination is a vital ecosystem service that benefits agricultural and horticultural production, and is essential for maintaining wild flower biodiversity. By improving the yield, quality and resilience of crops, insect pollination has been valued at £400 million per year to the UK economy (POST, 2010). 35 per cent of the World’s agricultural output, by volume, consists of 87 crop types that benefit from pollination by animals (insects, birds and mammals), but because most of these crops are not entirely dependent on animal pollination, the amount of production directly attributable to animals is lower than this value (Klein et al. 2007). There is growing concern regarding the population status of insect pollinators, and in turn the pollination service they provide (Potts et al. 2010; Garratt et al. 2014). As with most other areas of biodiversity, the main threats to pollinators include habitat loss, environmental pollution, climate change and the spread of alien species (Klein et al. 2007; Potts et al. 2010; Vanbergen & The Insect Pollinators Initiative 2013). The widespread application of pesticides is also perceived as a major threat to pollinator diversity (Brittain et al. 2010). In order for governments to act upon these threats they need robust metrics on the national-scale status of pollinators and pollination. Deriving such a metric has previously been limited by the availability of suitable data and analytical techniques. With the increase in citizen science, the availability of large-scale biological record data has increased (Silvertown 2009). Such data are collected without a standardized survey protocol and therefore extracting reliable trends from them can be difficult. However, with recent analytical advances it is now possible to estimate reliable trends from such data (van Strien et al. 2013; Isaac et al. 2014). METHODS Data sources Occurrence records of bee and hoverfly species within 1km grid squares in the UK were extracted from the Bees, Wasps and Ants Recording Society (BWARS) and the Hoverfly Recording Scheme biological records databases. The time-period used for the indicator was 1980 to 2010, as this represents a core period of recording for these taxa in the UK. A lag in submission and collation of records means that after 2010 the number of records per year tended to drop off. Bee species were filtered (following expert guidance from BWARS) so that only species considered to be wild pollinators were included. Species that had undergone taxonomic changes or had taxonomic issues during the time frame of the indicator were excluded from the analysis. The final composite indicator was based on 213 species of wild pollinator, see Appendix 1 for a list of species covered. Generating species’ trends and the composite indicator The data used to produce the indicator were not collected using a standardised protocol, but instead are a collation of unstructured biological observations collected by a large network of volunteer recorders. Such data tend to contain many forms of sampling bias and noise, making it hard to detect genuine signals of change (Tingley & Beissinger 2009; Hassall & Thompson 2010; Isaac et al. 2014). Recent studies have highlighted the value of Bayesian occupancy models for estimating species occurrence in the presence of imperfect detection (van Strien et al. 2013; Isaac et al. 2014). This approach uses two hierarchically coupled sub-models: an occupancy sub-model (i.e. presence verses absence), and a detection sub-model (i.e. detection verses non-detection). Together these sub-models estimate the conditional probability that a species is detected when present. A Bayesian occupancy model was applied to the data for each species, following van Strien et al. (2013) and Isaac et al. (2014). For each site-year combination the model estimates 1 presence or absence for the species in question given variation in detection probability: from this the proportion of occupied sites (‘occupancy’) was estimated for each year. These annual occupancy estimates were scaled so the value in 1980 was set to 100. The annual values of the composite indicator were calculated as the arithmetic mean of scaled species-specific occupancy estimates, and uncertainty in the species-specific annual occupancy estimates was propagated through to the final indicator. A detailed description of the occupancy model, and the creation of the composite indicator, can be found in the technical document on Bayesian indicator development. Species-specific trends Species were grouped into one of five categories based on both their short-term (over the most recent five years of data) and long-term (all years) mean annual change in occupancy (Table 1). Table 1. Thresholds used to define individual species trends. Category Thresholds Threshold – equivalent Strong increase Above +2.81% per annum +100% over 25 years Weak increase Between +1.16% and +2.81% p.a. +33% to +100% over 25 years Stable Between -1.14 % and +1.16% p.a. -25% to +33% over 25 years Weak decrease Between -2.73% and -1.14% p.a. -50% to -25% over 25 years Strong decrease Below -2.73% p.a. -50% over 25 years Asymmetric percentage change thresholds are used to define these classes as they refer to proportional change, where a doubling of a species index (an increase of 100%) is counterbalanced by a halving (a decrease of 50%). The threshold values for each category were based on those of the wild bird indicator; whether an individual species is increasing or decreasing has been decided by its rate of annual change over the time period (long or short) of interest. If the rate of annual change would lead to an occupancy increase or decrease of between 25 per cent and 49 per cent over 25 years, the species is said to have shown a ‘weak increase’ or a ‘weak decline’ respectively. If the rate of annual change would lead to a population increase or decrease of 50 per cent or more over 25 years, the species is said to have shown a ‘strong increase’ or a ‘strong decline’ respectively. These thresholds are used in the Birds of Conservation Concern status assessment for birds in the UK. See the technical document on the Bayesian indicator development for further detail on the calculation of the species-specific trends. RESULTS The indicator shows the average relative change in distribution of 213 species of pollinator, as measured by the number of 1km grid squares across the UK in which they were recorded – this is referred to as the ‘occupancy index’. Based on the unsmoothed data, there was an overall decrease in the indicator from 1987 onwards. In 2010, the occupancy indicator had declined to 68 per cent of the value in 1980. Between 1980 and 2010, 27 per cent of pollinator species became more widespread (14 per cent showed a strong increase), and 51 per cent became less widespread (36 per cent showed a strong decrease). Similar patterns occurred between 2005 and 2010, but with a greater proportion increasing and decreasing strongly. As individual pollinator species become more or less widespread, the communities in any given area become more or less diverse, and this may have implications for pollination as 2 more diverse communities are, in broad terms, more effective in pollinating a wide range of crops and wild flowers. The occupancy index was also produced for the bee (Figure 2) and hoverfly (Figure 3) species separately. The wild bee index was relatively stable up to 2005, it then increased before a sharp decline. In 2010, the wild bee index had declined to 62 per cent of the original value in 1980. The occupancy index was declining for a greater number of wild bee species than were increasing over both the long- and short-term. The sharp decline in the occupancy index in the three years up to 2010 of the indicator plot is reflected in the large (70 per cent) proportion of wild bee species showing strong declines in occupancy over the short-term. In contrast to the bees, the hoverfly index (Figure 3) shows a gradual decline from 1987 to 2007 onwards, reaching a low of 59 per cent of the value in 1980 in 2007. This trend was reversed in the last three years to 2010, ending at 76 per cent. A greater proportion of hoverflies have declined in occupancy over the long-term than have increased, but in the short-term 59 per cent of hoverflies show strong increases in occupancy between 2005 and 2010. The annual variability in the data is likely to be partly explained by annual variation in weather conditions. Pollinators tend to respond positively to temperature but negatively to rainfall. Hot dry periods are likely to have a greater negative impact on hoverflies than bees, as the exposed larvae of hoverflies are more vulnerable to desiccation compared to the larvae of bees that tend to be protected within an enclosed nest. The recent decline in bees from 2007–2010 is striking. A number of pressures are known to impact on local pollinator behaviour, distribution and abundance: weather, climate, land use change and pesticide use, for example (Vanbergen et al. 2014; Stanley et al. 2015). There was a decline in the indicator between 2007 and 2010. It is not known whether this change in distribution is the start of a longer term trend or short term fluctuation, and if the former, whether it is linked to one particular pressure or to a combination of pressures. Despite the inter-annual variation, the overall trend for pollinators remains downward. This indicator is a composite measure across 213 species (Appendix 1) and therefore covers a large proportion of the pollinator species within the UK. Not all species contribute to all years (see No. spp. column in Tables 2, 3 and 4 for the overall, bee and hoverfly indices respectively). 3 Figure 1. Change in the distribution of pollinators in the UK between 1980 and 2010. The shaded region is the 90 per cent credible intervals of the annual occupancy estimates and represents the uncertainty surrounding the annual estimates. The solid line illustrates a smoothed trend estimated from a GAM fitted to the rescaled indicator values (dashed line). The proportion of pollinator species in each trend category is based on mean change in occupancy over both a) the long term (all years) and b) the short term (the most recent five years). 4 Table 2. Change in the distribution of pollinators in the UK between 1980 and 2010. The indicator values per year are presented alongside their uncertainty (upper and lower 90 per cent credible intervals), and the number of species contributing to the annual index value. The number of species contributing has been split into those with an interpolated estimate and those with an actual occupancy estimate. Year Indicator Lower CI Upper CI 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 100 100 100 100.76 95.78 92.44 97.92 99.80 104.36 106.19 99.17 94.72 94.74 86.48 92.46 85.13 95.40 91.47 93.58 86.59 85.31 86.04 84.89 76.93 83.33 87.99 85.50 77.29 82.45 84.40 89.14 84.65 68.49 90.24 86.24 82.89 87.18 89.09 93.86 95.51 89.33 84.23 84.91 77.85 82.70 76.73 85.80 82.15 84.63 78.27 77.16 77.71 76.70 69.47 75.30 79.73 77.82 69.89 73.98 75.83 80.21 76.13 60.56 112.37 106.87 102.86 109.43 111.00 116.07 117.92 109.58 105.40 104.94 96.41 102.92 94.17 105.39 101.22 103.78 95.88 94.26 95.20 93.55 84.72 91.61 96.84 94.26 85.35 91.54 93.35 98.92 94.01 76.50 No. Sp. Estimated 184 180 192 189 195 190 194 197 197 193 198 188 203 202 197 204 199 202 201 202 201 202 210 201 202 190 196 203 200 199 193 5 No. Sp. Interpolated 0 4 12 20 15 21 18 16 16 20 15 25 10 11 16 9 14 11 12 11 12 11 3 12 11 23 17 10 12 10 0 Figure 2. Change in the distribution of pollinating wild bee species in the UK between 1980 and 2010. The shaded region is the 90 per cent credible intervals of the annual occupancy estimates and represents the uncertainty surrounding the annual estimates. The solid line illustrates a smoothed line from a GAM fitted to the rescaled indicator values (dashed line). The proportion of pollinating bee species in each trend category is based on mean change in occupancy over both a) the long term (all years) and b) the short term (the most recent five years). 6 Table 3. Change in the distribution of pollinating wild bee species in the UK between 1980 and 2010. The indicator values per year are presented alongside their uncertainty (upper and lower 90 per cent credible intervals), and the number of species contributing to the annual index value. The number of species contributing has been split into those with an interpolated estimate and those with an actual occupancy estimate. Year Indicator Lower CI Upper CI 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 100 107.09 94.65 94.36 105.81 105.30 104.52 107.04 98.74 99.24 100.08 93.53 90.64 93.49 104.70 103.72 107.36 108.69 99.52 95.27 109.97 87.09 92.83 98.91 107.53 102.81 115.17 121.05 109.38 94.38 61.87 100 91.19 80.18 80.06 90.63 89.75 89.05 91.20 84.12 84.07 84.86 79.50 77.37 79.89 89.30 89.64 92.68 93.47 85.94 82.34 95.17 75.15 80.49 85.49 92.62 87.98 98.81 104.93 93.36 80.81 51.85 100 123.68 110.10 109.78 121.26 121.60 121.05 125.26 115.26 116.09 117.04 109.42 105.33 108.84 120.18 119.55 123.05 124.25 114.35 109.01 125.87 99.57 105.45 112.43 123.15 117.75 132.10 137.80 125.21 107.84 72.81 No. Sp. Estimated 97 90 91 93 98 97 95 92 95 91 101 92 103 103 98 102 100 105 103 100 100 101 104 99 100 93 93 102 103 101 97 7 No. Sp. Interpolated 0 7 10 9 4 6 9 13 10 14 4 13 2 2 7 3 5 0 2 5 5 4 1 6 5 12 12 3 2 4 0 Figure 3. Change in the distribution of hoverfly species in the UK between 1980 and 2010. The shaded region is the 90 per cent credible intervals of the annual occupancy estimates and represents the uncertainty surrounding the annual estimates. The solid line illustrates a smoothed line from a GAM fitted to the rescaled indicator values (dashed line). The proportion of hoverfly species in each trend category is based on mean change in occupancy over both a) the long term (all years) and b) the short term (the most recent five years). 8 Table 4. Change in the distribution of hoverfly species in the UK between 1980 and 2010. The indicator values per year are presented alongside their uncertainty (upper and lower 90 per cent credible intervals), and the number of species contributing to the annual index value. The number of species contributing has been split into those with an interpolated estimate and those with an actual occupancy estimate. Year Indicator Lower CI Upper CI 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 100 94.29 95.85 90.08 89.79 93.84 103.14 104.36 98.77 89.73 88.62 79.58 93.64 76.75 86.04 80.37 81.29 68.67 72.57 77.25 65.44 67.46 74.47 77.85 67.69 57.84 59.01 58.89 72.45 75.87 76.23 100 79.14 81.02 75.51 74.82 77.98 86.13 87.60 82.87 75.70 74.37 66.88 78.82 64.40 72.23 67.72 67.58 57.79 60.73 65.03 54.92 56.87 62.58 65.91 56.65 48.83 49.24 49.55 60.93 64.02 64.71 100 110.15 112.67 106.28 107.62 110.52 122.77 122.61 115.51 106.25 103.87 93.84 110.44 90.44 100.81 95.28 95.33 80.92 85.27 91.47 76.68 78.82 87.92 91.21 79.41 67.81 69.93 69.41 85.53 88.90 89.51 No. Sp. Estimated 87 87 101 96 97 93 99 105 102 102 97 96 100 99 99 102 99 97 98 102 101 101 106 102 102 97 103 101 97 98 96 9 No. Sp. Interpolated 0 0 2 11 11 15 9 3 6 6 11 12 8 9 9 6 9 11 10 6 7 7 2 6 6 11 5 7 10 6 0 FUTURE WORK Bees and hoverflies are key pollinators in the UK and are presented here as an indicator of the overall trend in pollinators. Other taxonomic groups (e.g. some butterflies and moths) can provide pollination services but are not yet included in the indicator. Future updates of the pollinator indicator could include trends from other taxonomic groups known to provide pollination services. All species were given equal weight in the pollinator indicator – effectively the indicator assumes all species are equally valuable in terms of their contribution to pollination services. However, contribution to pollination is known to vary between species and is dependent on inherent life history and ecological characteristics of the species, but also on total population abundance (Breeze et al. 2011; Woodcock et al. 2013). Future work could examine the feasibility of weighting the indicator to take account of this variation in species importance as pollinators. REFERENCES Breeze, T.D., Bailey, A.P., Balcombe, K.G. & Potts, S.G. (2011) Pollination services in the UK: How important are honeybees? Agriculture, Ecosystems & Environment, 142, 137–143. Brittain, C. A., Vighi, M., Bommarco, R., Settele, J. & Potts, S.G. (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic and Applied Ecology, 11, 106– 115. Garratt, M.P.D., Truslove, C.L., Coston, D.J., Evans, R.L., Moss, E.D., Dodson, C., Jenner, N., Biesmeijer, J.C. & Potts, S.G. (2014) Pollination deficits in UK apple orchards. Journal of Pollination Ecology, 12, 9–14. Hassall, C. & Thompson, D.J. (2010) Accounting for recorder effort in the detection of range shifts from historical data. Methods in Ecology and Evolution, 1, 343–350. Isaac, N.J.B., van Strien, A.J., August, T.A., de Zeeuw, M.P. & Roy, D.B. (2014) Statistics for citizen science: extracting signals of change from noisy ecological data. Methods in Ecology and Evolution, 5, 1052–1060. Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A, Kremen, C. & Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings. Biological sciences / The Royal Society, 274, 303–13. POST (2010) Insect Pollination, London. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25, 345–53. Silvertown, J. (2009) A new dawn for citizen science. Trends in Ecology & Evolution, 24, 467–471. Stanley, D.A. Garratt, M.P.D., Wickens, J.B., Wickens, V.J., Potts, S.G. & Raine, N.E. (2015) Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature, online early. Van Strien, A.J., van Swaay, C.A.M. & Termaat, T. (2013) Opportunistic citizen science data of animal species produce reliable estimates of distribution trends if analysed with occupancy models. Journal of Applied Ecology, 50, 1450–1458. Tingley, M.W. & Beissinger, S.R. (2009) Detecting range shifts from historical species occurrences: new perspectives on old data. Trends in Ecology & Evolution, 24, 625–633. Vanbergen, A.J. & The Insect Pollinators Initiative. (2013) Threats to an ecosystem service: pressures on pollinators. Frontiers in Ecology and the Environment, 11, 251–259. Woodcock, B.A., Edwards, M., Redhead, J., Meek, W.R., Nuttall, P., Falk, S., Nowakowski, M. & Pywell, R.F. (2013) Crop flower visitation by honeybees, bumblebees and solitary bees: Behavioural differences and diversity responses to landscape. Agriculture, Ecosystems & Environment, 171, 1–8. 10 APPENDICES Appendix 1. The list of 213 species included in the pollinator indicator. Species Anasimyia contracta Anasimyia lineata Anasimyia transfuga Andrena apicata Andrena argentata Andrena barbilabris Andrena bicolor Andrena bimaculata Andrena bucephala Andrena carantonica Andrena chrysosceles Andrena cineraria Andrena clarkella Andrena dorsata Andrena flavipes Andrena florea Andrena fucata Andrena fulva Andrena fuscipes Andrena haemorrhoa Andrena hattorfiana Andrena helvola Andrena humilis Andrena labialis Andrena lapponica Andrena marginata Andrena minutula Andrena nigroaenea Andrena nitida Andrena nitidiuscula Andrena ovatula Andrena praecox Andrena semilaevis Andrena subopaca Andrena synadelpha Andrena tarsata Andrena thoracica Andrena tibialis Andrena trimmerana Anthidium manicatum Anthophora bimaculata Anthophora plumipes Anthophora quadrimaculata Arctophila superbiens Baccha elongata Bombus distinguendus Bombus hortorum Bombus humilis Bombus jonellus Bombus lapidarius Bombus muscorum Bombus pascuorum Bombus pratorum Bombus ruderarius Bombus soroeensis Bombus sylvarum Bombus terrestris Brachyopa scutellaris Brachypalpoides lentus Brachypalpus laphriformis Caliprobola speciosa Ceratina cyanea Chalcosyrphus nemorum Cheilosia albitarsis Cheilosia antiqua Cheilosia bergenstammi Cheilosia fraterna Cheilosia illustrata Cheilosia impressa Cheilosia longula Cheilosia pagana Cheilosia proxima Cheilosia scutellata Cheilosia soror Cheilosia variabilis Cheilosia vernalis Cheilosia vulpina Chelostoma campanularum Chelostoma florisomne Chrysogaster cemiteriorum Chrysogaster solstitialis Chrysogaster virescens Chrysotoxum arcuatum Chrysotoxum bicinctum Chrysotoxum cautum Chrysotoxum elegans Chrysotoxum festivum Colletes cunicularius Colletes daviesanus 11 Colletes fodiens Colletes halophilus Colletes marginatus Colletes similis Colletes succinctus Criorhina asilica Criorhina berberina Criorhina floccosa Criorhina ranunculi Dasypoda hirtipes Dasysyrphus albostriatus Dasysyrphus tricinctus Dasysyrphus venustus Didea fasciata Epistrophe eligans Epistrophe grossulariae Episyrphus balteatus Eristalinus aeneus Eristalinus sepulchralis Eristalis abusivus Eristalis arbustorum Eristalis horticola Eristalis interruptus Eristalis intricarius Eristalis pertinax Eristalis rupium Eristalis tenax Eucera longicornis Eumerus funeralis Eumerus ornatus Eumerus strigatus Eupeodes corollae Eupeodes latifasciatus Eupeodes luniger Halictus confusus Halictus rubicundus Halictus tumulorum Heriades truncorum Lasioglossum albipes Lasioglossum calceatum Lasioglossum cupromicans Lasioglossum fratellum Lasioglossum fulvicorne Lasioglossum laevigatum Lasioglossum lativentre Lasioglossum leucopus Lasioglossum leucozonium Lasioglossum malachurum Lasioglossum minutissimum Lasioglossum morio Lasioglossum parvulum Lasioglossum pauxillum Lasioglossum prasinum Lasioglossum punctatissimum Lasioglossum puncticolle Lasioglossum rufitarse Lasioglossum smeathmanellum Lasioglossum villosulum Lasioglossum zonulum Lejogaster metallina Leucozona glaucia Leucozona laternaria Leucozona lucorum Macropis europaea Megachile leachella Megachile maritima Megachile versicolor Megachile willughbiella Melangyna arctica Melangyna lasiophthalma Melanogaster hirtella Melanostoma mellinum Melanostoma scalare Meliscaeva auricollis Meliscaeva cinctella Melitta haemorrhoidalis Melitta leporina Melitta tricincta Merodon equestris Microdon analis Myathropa florea Neoascia geniculata Neoascia interrupta Neoascia meticulosa Neoascia obliqua Neoascia podagrica Neoascia tenur Orthonevra geniculata Orthonevra nobilis Osmia aurulenta Osmia bicolor Osmia bicornis Osmia caerulescens Osmia leaiana Osmia spinulosa Panurgus banksianus Panurgus calcaratus Paragus haemorrhous 12 Parasyrphus punctulatus Parasyrphus vittiger Parhelophilus frutetorum Parhelophilus versicolor Pelecocera tricincta Pipiza noctiluca Pipizella viduata Platycheirus albimanus Platycheirus angustatus Platycheirus clypeatus Platycheirus fulviventris Platycheirus granditarsus Platycheirus manicatus Platycheirus peltatus Platycheirus rosarum Platycheirus scambus Platycheirus tarsalis Portevinia maculata Rhingia campestris Riponnensia splendens Scaeva pyrastri Sericomyia lappona Sericomyia silentis Sphaerophoria batava Sphaerophoria interrupta Sphaerophoria philanthus