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BioRisk 6: I-18 (201 1) : =
doi: 10.3897/biorisk.6. 1325 RESEARCH ARTICLE & B | O R IS k

www.pensoft.net/journals/biorisk

Assessing continental-scale risks for generalist and
specialist pollinating bee species under climate change

Stuart P.M. Roberts', Simon G. Potts', Koos Biesmeijer?, Michael Kuhlmann’,

Bill Kunin’, Ralf Ohlemiiller*

| Centre for Agri-Environmental Research, University of Reading, RG6 GAR, UK 2 Earth & Biosphere Insti-
tute, IICB, Faculty of Biological Sciences, University of Leeds, Leeds LS2 91, UK 3 The Natural History Mu-
seum, Cromwell Road, London SW7 5BD, UK 4 School of Biological and Biomedical Sciences, and Institute
of Hazard, Risk and Resilience, Durham University, South Road, Durham DH1 3LE, UK

Corresponding author: Stwart PM. Roberts (s.p.m.roberts@reading.ac.uk)

Academic editor: Josef Settele | Received 30 March 2011 | Accepted 4 October 2011 | Published 19 December 2011

Citation: Roberts SPM, Potts SG, Biesmeijer K, Kuhlmann M, Kunin B, Ohlemiiller R (2011) Assessing continental-
scale risks for generalist and specialist pollinating bee species under climate change. BioRisk 6: 1-18. doi: 10.3897/
biorisk.6.1325

Abstract

Increased risks of extinction to populations of animals and plants under changing climate have now
been demonstrated for many taxa. This study assesses the extinction risks to species within an important
genus of pollinating bees (Colletes: Apidae) by estimating the expected changes in the area and isolation
of suitable habitat under predicted climatic condition for 2050. Suitable habitat was defined on the basis
of the presence of known forage plants as well as climatic suitability. To investigate whether ecological spe-
cialisation was linked to extinction risk we compared three species which were generalist pollen foragers
on several plant families with three species which specialised on pollen from a single plant species. Both
specialist and generalist species showed an increased risk of extinction with shifting climate, and this was
particularly high for the most specialised species (Colletes anchusae and C. wolfi). The forage generalist
C. impunctatus, which is associated with Boreo-Alpine environments, is potentially threatened through
significant reduction in available climatic niche space. Including the distribution of the principal or sole
pollen forage plant, when modelling the distribution of monolectic or narrowly oligolectic species, did
not improve the predictive accuracy of our models as the plant species were considerably more widespread

than the specialised bees associated with them.

Keywords

Colletes, bee, climate change, Europe, risk assessment, pollinator

Copyright Stuart PM. Roberts et al. This is an open access article distributed under the terms of the Creative Commons Attribution License 3.0
(CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

2 Stuart PM. Roberts et al. / BioRisk 6: 1-18 (2011)

Introduction

There is general consensus that the most pressing environmental problem that faces
the world today is climatic change and it is widely acknowledged that this change is
likely to have major impacts both on biodiversity (Green et al. 2003) and on human
society in general (Stern 2007). Many animal and plant species are expected to show
major shifts in abundance, distribution and phenology and this could lead to extinc-
tions at the local, regional, continental or even global scale (Flenner and Sahlen 2008;
Graham- Taylor et al. 2009; Hegland et al. 2009; Settele et al. 2008). Accurate predic-
tion of likely risks under a shifting climatic regime is essential to enable conservation
priorities to be set and assist in directing mitigation actions (Santos et al. 2009).

A number of recent studies have considered the effects of observed climatic shifts
on various taxa, and in addition to more general studies such as Parmesan and Yohe
(2003), Root et al. (2003) and Menzel et al. (2006), these include butterflies (Sparks
and Yates 1997; Parmesan et al. 1999; Roy and Sparks 2000; Menéndez et al. 2008),
flowering plants (Sparks et al. 2000) and birds (Sanz 2003; Sergio 2003). More recent
work has used current distributions of European birds (Huntley et al. 2007) and but-
terflies (Schweiger et al. 2008; Schweiger et al. 2012; Settele et al. 2008) to forecast
likely future ranges, and to consider the possible conservation implications of shifts in
distributions.

In addition to work on butterflies, there are increasing numbers of studies on
other insect groups, and these include Odonata (Dingemanse and Kalkmann 2008),
Coleoptera (eg Molina-Montenegro et al. 2009), Diptera (eg Graham-Taylor et al.
2009), invertebrate disease vectors (e.g. Wilson and Mellor 2008) and pest species (e.g.
Hoffmann et al. 2008). Among pollinators, Williams et al. (2007) have assessed. the
vulnerability of three species of bumblebee (Bombus) to extinction by studying climatic
niches that determine their ranges at a regional scale.

The number of large scale multi-taxa studies on insect species other than Lepidop-
tera has been restricted because detailed data on the biology and distribution of most
insects in general, and pollinator species in particular, are available at fine resolutions
for only a few places. Risk of local extinctions can, therefore, be assessed quite accu-
rately given detailed information on local population, habitat size and climatic condi-
tions (e.g. Franzén et al. 2009). However, assessing extinction risks of these species at
the regional, continental or global scale is hampered by lack of appropriate data.

A risk analysis should, ideally, be based on complete data on the species’ distribu-
tion in conjunction with knowledge on both the abiotic requirements (e.g. climate,
geomorphology, soil) and the biotic requirements (e.g. principal forage plants). Then,
using scenarios for changes in climate and land use, a model can be built to predict po-
tential range shifts and extinctions. Some existing studies have based their analyses on a
climate only model (e.g. Huntley et al. 2007; Settele et al. 2008) and others (e.g. Luetolf
et al. 2009) on a habitat only model. A smaller number of studies link both habitat and
climate models (e.g. Santos et al. 2009; Schweiger et al. 2008; 2012).

Assessing continental-scale risks for generalist and specialist pollinating bee species... 3

We make use of one of the few available pollinator datasets for which comprehen-
sive European-scale distribution is currently known: a number of specialist and gener-
alist Colletes bee species, some of which are endemic to Europe. We ask:

1) What are the levels of risk associated with shifts in climatic conditions at loca-
tions where the pollinator species currently occur?

2) Can we predict the current distribution of specialist and generalist pollinator
species at a continental scale based on climate and host plant distribution variables?

3) Is it likely that the ranges of principal forage plants and specialist bees can be-
come uncoupled under climate change with the possible threat of extinction to one or
both species?

4) What are the likely future European distributions of the investigated species
under the projected shifts in climatic conditions?

The aim of our study is to provide a continental-scale assessment of the risk a pol-
linator species is likely to face under future climate change and to determine if special-
ised species are at greater risk as a result of their narrow pollen forage requirements.

Methods

Species distribution and climate data

From a dataset containing distribution data on all 59 species of bees in the genus
Colletes occurring in Europe (Kuhlmann, unpublished data) we selected six species for
which there were sufhicient data to cover adequately their entire European ranges (Ap-
pendix A). Three of these are polylectic species, i.e. pollen forage generalists (Colletes
albomaculatus, C. impunctatus, C. nigricans) and three monolectic or narrowly oli-
golectic, i.e. forage specialists (C. anchusae, C. hederae, C. wolfi). Pollen foraging in
Colletes anchusae and C. wolf: is restricted to Cynoglottis barrelieri (Boraginaceae) (Miil-
ler and Kuhlmann 2003; 2008) whereas C. hederae generally restricts its foraging to
Hedera helix (Araliaceae) (Schmidt and Westrich 1993; Bischoff et al. 2005), although
occasionally it will forage for pollen at various Asteraceae if Hedera helix flowers are not
available (Miller and Kuhlmann 2008; Westrich 2008). Distribution records of these
species from the last 125 years (with 61% of data from the last 40 years) across Europe
were collated and transformed into a presence/absence map at 10’ grid resolution. For
the majority of 10’ grid cells, there was no record, but in total, 1,549 or 4.9 % of all
10° grid cells had at least one record for one of the six species. Prevalence of the six
species ranged from 10 to 150 occupied 10’ grid cells (Table 1). We have assumed that
all records represent the current distribution (cf. Williams et al 2007). Although many
areas have had poor coverage, the problem is reduced by mapping at a relatively coarse
10’ resolution. The presence/absence matrix of these 1,549 grid cells was used to build
distribution models of the species.

4 Stuart RM. Roberts et al. / BioRisk 6: I-18 (2011)
Table |. Model specification and model fit. Percent variation of present-day distribution explained and
model fit of distribution models for the six species.

species number of 10’ cells | model Percent variation in distri-
recorded bution explained by model

generalists

C. albomaculatus 110 3157
C. impunctatus 102 64.2

C. nigricans 150 climate 2oal
specialists

C. anchusae 16 climate 44.7

45.5

C. hederae 76 climate 12.0

climate + hostplant 2.2
C. wolft 10 climate 65.0

65.8

Current (1961-1990 average) and future (2041-2050 average, henceforth “2050”)
climate conditions at the same resolution were taken from Mitchell et al. (2004) and
we used the following five climate variables to predict the distribution of our tar-
get species: mean annual temperature, mean minimum temperature of the coldest
months, mean annual precipitation, annual water deficit and growing degree days >
5°C. These variables represent a set of biologically meaningful factors which, given the
lack of detailed knowledge of climate requirements of individual species, aims to cover
the relevant climate conditions for our six species. We restrict our analyses to a low
greenhouse gas emission scenario (B2) which represents a socio-economic storyline fo-
cussing on local and regional solutions to economic and environmental problems and
projects a global average temperature increase by the end of this century of between 1.4
and 3.8°C (IPCC 2007). We use this as a best case scenario of the lowest risk so that
these underpin the minimum conservation action responses.

The known distribution (both historic and current) of the genus Cynoglottis is
mapped in Miller & Kuhlmann (2003) who based the map on a synthesis of various
regional, national and European floras (see references therein). The known distribu-
tion of Hedera helix is mapped by Meusel (1978) modified by Kuhlmann et al. (2007).
All distributions were digitised as shape files in ArcGIS and converted to a presence/
absence grid at the same resolution as the climate grid.

Distribution modelling

Generalised Linear Models (GLMs) with binomial errors and with linear and quad-
ratic terms for all variables were used to predict the current distribution of the Colletes
species. For the generalist species, we predicted their current distributions across Eu-
rope based on all six climate variables, while for the specialist species, we used the six

Assessing continental-scale risks for generalist and specialist pollinating bee species... 5

climate variables plus the host plant distribution as a binary predictor variable. For
all models, we compared the model fit between the full model (including all possible
predictor variables) and the most parsimonious minimal adequate model (including
only the most significant variables retained after stepwise variable selection allowing for
addition and deletion of variables at each step). The difference in model fit between the
two methods was generally small and so we present the outcomes of the full models.
All models and variable selection procedures were performed in S-Plus 6.2. Predictive
power of the full model was assessed by quantifying the percentage of variation in spe-
cies presence/absence explained by the full set of variables (Table 1). We used the mod-
els fitted on the current climate data to predict climatic suitability of the six species
under future (2050) climate conditions. For the three specialist species, we assumed
that the distribution of the host plants will not change substantially between now and
2050 seeing that the species are almost ubiquitous in Europe. Comparing current ob-
served, current modelled and future modelled distributions of the six species allows us
to assess likely shifts in suitable climate space under changing climate conditions. For
each species we compare the local (within a 100 km radius from each observed loca-
tion) and continental-wide change in climatically suitable area between current and
future climate conditions (Fig. 1).

Results

Current distributions and suitable climate space

Within the genus Colletes, we have selected six species with a well recorded European
distribution. We were able to explain between 12% (C. hederae) and 65% (C. wolfi)
of the variation in their current distribution with the climate variables chosen here
(Table 1). Overall, our bioclimate models were able to reproduce the observed current
European distribution of our species accurately (Table 1; Fig. la—f). In particular, the
suitable climate space of the two southern European generalist species C. albomaculatus
and C. nigricans, for instance, was captured very well by our models. When modelling
the distribution of the specialist species, including the distribution of the principal
forage plants as an additional predictor, does not improve the model fit of the models.
The percent variation in distribution with the food plants included in the model only
increases very slightly (Table 1). C. impunctatus (Fig. 1b), shows that it occurs in most
of its current suitable climate space, occurring in the clearly defined boreal climatic
area in northern Europe, with a second centre of distribution in the montane region
of the Alps in the south. Colletes hederae, on the other hand, appears to be the species
which has least filled its suitable climatic space (Fig. le). Large areas in Italy, France
and Spain have highly suitable climate but no, or only few, occurrences of the species
have thus far been reported.

Under present-day climate conditions, species with a predominantly Mediterra-
nean distribution are occupying areas with the highest climatic rarity, i.e., the climatic

6 Stuart RM. Roberts et al. / BioRisk 6: 1-18 (2011)

Present-day recorded Present-day modelled 2030 modelled

b c. impunctatus

C C. nigricans

Figure | (a—c). Potential future European distribution of three investigated generalist Colletes species
based on climate. [Present day recorded distribution; present day modelled distribution, and 2050 mod-
elled climatic suitability of a Colletes albomaculatus b C. impunctatus and € C. nigricans]

conditions of the locations where the species is currently found are not found in many
areas elsewhere in Europe. C. nigricans, with a south-western Mediterranean distribu-
tion, has the rarest suitable climate envelope of our six species (Fig. 1c). C. albomac-
ulatus, which exploits suitable climatic space more widely across the Mediterranean
region, extends into south eastern Europe (Fig. 1a).

Future suitable climate space

We calculated the change in climatically suitable area for each species between cur-
rent and future climatic conditions locally (within a 100 km radius) and Europe-

Assessing continental-scale risks for generalist and specialist pollinating bee species... 7

Present-day recorded Present-day modelled 2050 modelled
distribution suitability (climate) suitability (climate)

Present-day modelled 2050
suitability modelled suitability
(climate+hostplant) (climate+hostplant)

d C. anchusae

Present-day recorded Present-day modelled 2050 modelled
distribution suitability ‘aii suitability (climate)

7 2050
ne modelled suitability
(climate+hostplant) (climate+hostplant)

e C. hederae

Figure | (d-e). Potential future European distribution of two investigated specialist Colletes species
based on climate and host plant distribution. [Present day recorded distribution; present day modelled
suitability (climate); present day modelled suitability (climate & hostplant); 2050 modelled suitability
(climate); and 2050 modelled suitability (climate & hostplant) of d Colletes anchusae and e C. hederae]

8 Stuart PM. Roberts et al. / BioRisk 6: 1-18 (2011)

Present-day recorded Present-day modelled 2050 modelled
distribution suitability (climate) suitability (climate)

Present-day modelled 2050
suitability modelled suitability
(climatet+hostplant) (climatet+hostplant)

f Cwolfi

Figure | (f). Potential future European distribution of the specialist Colletes wolfi based on climate and
host plant distribution. [Present day recorded distribution; present day modelled suitability (climate);
present day modelled suitability (climate & hostplant); 2050 modelled suitability (climate); and 2050
modelled suitability (climate & hostplant)]

wide. Plotting the two against each other allows us to assess which species are going
to be affected by loss of climatically suitable area locally vs. at the continental scale
(Fig. 2). For instance, for C. impunctatus (generalist), close to 100% of grid cells
with 100 km radius of current occurrences and in Europe as a whole are predicted
to become less climatically suitable for that species in 2050 than they are now. This
species is therefore likely to face difficulties locally where it currently occurs but also
in terms of finding new areas to colonise in Europe. For C. wolf (specialist) on the
other hand, over 70% of grid cells locally are predicted to become climatically less
suitable between now and 2050, where in the rest of Europe only less than 10% of
grid cells in Europe will be less suitable for this species than they are now. This in-
dicates that this species is likely to face difficulties locally, however, if it manages to
disperse and migrate beyond its local environment, there are large areas elsewhere in
Europe that will be climatically suitable in 2050. For the other two specialist species
(C. anchusae, C. hederae), only ca. 20% of grid cells both close to where the species
are currently found and Europe-wide are predicted to become less climatically suit-
able. This indicates that these species should be able to find suitable climatic condi-
tions locally as well as farther afield (Figs 1d—e, 2).

Assessing continental-scale risks for generalist and specialist pollinating bee species... 9

1.0
Greater proportional loss
of climatic suitability A
. 0.8 Fe C. impunctatus
Proportion of grid
cells with
decreasing 0.6
climatic suitability
within Europe
0.4 -
Greater proportional loss
of climatic suitability
0.2 C.hederae Ac nigricans locally
Ez
A C. albomaculatus oe
0.0 1 1 1
0.0 0.2 0.4 0.6 0.8 1.0

Average proportion of grid cells with
decreasing climatic suitability within 100km
radius of current occurrences

Figure 2. Local vs. continental scale change in climatic suitability between current and future climatic
suitability of six Colletes species. For each species, we calculated the average number of grid cells within a
100 km radius that show decreasing climatic suitability for the species between current and future condi-
tions. We also calculated for each species the proportion of grid cells with decreasing climatic suitability
for the species in the whole of Europe. Black squares indicate specialists, grey triangles indicate generalists.
The solid line indicates the 1:1 line.

Discussion

There are threats to all six studied Colletes species under predicted climate change, but
the threats are not related to forage plant specialisation. In general, we predict that the
trends will be towards a decrease in overall range of our species in Europe caused by
a combination of a reduction in suitable climatic space, compounded by an increase
in isolation between climatically suitable areas. The addition of principal forage plant
distribution as an additional predictor, however, does not improve the power of the
models, as the specialist forage plants are very widely distributed across the continent.
This reflects findings by Schweiger et al. (2012) who found that the majority of inves-
tigated butterfly species in Europe are not limited by their larval host plants.

Of the generalist species, those currently showing a predominantly southern Eu-
ropean distribution are predicted to exhibit only relatively minor decreases (C. nig-
ricans) or no decrease in climatically suitable area (C. albomaculatus) under climate
change. Both species, however, are predicted to experience an increase in isolation
of their future suitable climate space. These changes may appear relatively small, but
they represent net changes, and there is a clear movement northwards of the future
climatic space, away from the current centres of distribution. C. nigricans, already well

10 Stuart PM. Roberts et al. / BioRisk 6: 1-18 (2011)

established in the Mediterranean areas of France, may be able to expand into much of
central and northern France along major river valleys. The projected situation in the
drier parts of its current range suggests future significant declines in southern Iberia.
The predicted suitable climatic envelope maps (Fig. la—f) suggest that C. albomacula-
tus looks well positioned to be able to expand into eastern central Europe, and possibly
also in the steppic environments to the north west of the Black Sea (for map of Euro-
pean biogeographic regions see Appendix B). In both cases, expansion of range would
be aided by their ability to exploit a broad diet spectrum.

Colletes impunctatus is a member of the Boreo-Alpine element in the European bee
fauna, and is the generalist species that appears to be under the greatest threat from
projected climate change. The area suitable for this species will be severely reduced in
the Alps (currently a stronghold), and disjunctions will appear in Fennoscandia. These
reductions in area will negatively affect this species.

The two restricted species which are monolectic on Cynoglottis barrelieri, (Colletes
anchusae and C. wolf) appear to be at risk from both a reduction in suitable climatic
space as well as increased isolation (Fig. 1d, f). This is particularly significant for C. an-
chusae, which moves from being a species with a relatively low risk of negative climatic
impacts, to one with a high risk. C. wolf is currently very restricted in range and has a
disjunct bicentric distribution, with centres in central Italy and again in the north of
that country. This study indicates that the northern Italian population is under severe
threat, with the suitable climatic envelope being eliminated by 2050, with distance,
coupled with topography (the Alps and Appenine mountains acting as a dispersal bar-
rier), making colonisation of new areas unlikely.

The third specialist species, Colletes hederae (Fig. le), might derive some benefits
from the projected changes in climate. C. hederae is widely distributed in much of
lowland western Europe, and is the most widespread of the specialist species. It is pos-
tulated that the species has expanded from centres south of the Alps with ameliorating
climate (Kuhlmann, unpublished data). C. hederae has undergone a very rapid expan-
sion of range in the last twelve years, reaching The Netherlands in 1997 (Peeters et al.
1999), and both Luxembourg (Feitz 2001) and the UK in 2001 (Cross 2002). The
range has also expanded eastwards across northern Switzerland and southern Germany
(Herrmann 2007) into central Germany (Frommer 2008). The principal forage plant,
Hedera helix, is known to be strongly climate limited. Iversen (1944) demonstrated
that the plant reproduces vegetatively in the northern parts of its range and that flow-
ering is associated with areas of greater warmth. ‘The northern boundaries of flowering
of Hedera helix are likely to move northwards, creating new colonisation opportunities
for Colletes hederae in the future.

We can say with confidence that although projected climate change may, in part,
negatively impact on the studied bee species, it is most unlikely that declining popu-
lations of the most specialised CoJ//etes will cause a serious reduction in pollination
services to the principal forage plants. Waser et al. (1996) demonstrated that specialist
pollinators tend to pollinate generalist plants, and this is certainly the case for Hedera
helix (Ollerton et al. 2007) which attracts a wide range of insect visitors from several

Assessing continental-scale risks for generalist and specialist pollinating bee species... i

orders. No data is available on the species that visit Cynoglottis barrelieri, but the flow-
ers of the related plant Anchusa strigosa are known to attract a diverse assemblage of
long-tongued bees of the genera Eucera and Anthophora in Israel (Kadmon and Shmida
1992) and so it is likely that C. barrelieri also attracts species other than C. anchusae
and C. wolfi as visitors.

One of the possible consequences for both generalist and specialist Co/letes species
under climate change is that future shifts in range and distribution may be accom-
panied by changes in abundance. Colletes are known to support a number species of
brood parasitic bees in the genus Epeolus which specialise on Colletes (Westrich 1989;
Amiet et al. 1999) and future shifts are particularly likely to affect brood parasites,
which need well established host populations to support them. In the case of E. al
pinus, whose host (C. impunctatus (Amiet et al. 1999)) is restricted to boreo-alpine
habitats, these risks are likely to be greater as the host habitats are predicted to dimin-
ish in area. Of our other modelled species, Colletes hederae is cited as a host of Epeolus
cruciger (Kuhlmann et al. 2007), and believed to be a host of E. fallax (P. Westrich pers.
comm.). In populations of C. hederae in northern Italy, Slovenia and southern Swit-
zerland, nests are subject to parasitism by the bee E. cruciger, whereas no parasitism
has been noted away from these core areas (Kuhlmann et al. 2007). Changing climate
appears to have allowed the C. hederae to expand rapidly, without the cleptoparasite
following at present.

Climate change presents a number of challenges for conservation. To the bees
themselves, the plants they visit, and pollination services in general. In order to un-
derstand how climate shifts may affect plants and pollination more generally, a wider
ranging study would be necessary, as this work deals with only 6 species out of an esti-
mated European bee fauna of about 2,250 species (Polaszek 2004). However, given the
likely loss of suitable climatic space and increased isolation of areas for these six species,
it is likely that many other European bees may also be subject to similar increases in
extinction risk under climate change. For effective bee conservation under environ-
mental change, it is necessary to ensure that as the suitable climate envelopes move,
that suitable habitat is available for the bees to exploit. For those bees that are forage
specialists, this will clearly also involve the provision of the specialised forage itself.

Acknowledgements

We thank the suppliers of bee distribution data across Europe, including the Bees,
Wasps & Ants Recording Society (UK), Wistein Berg (Norway), EIS (Netherlands),
Jaan Luig (Estonia), Vergilijus Monsevicius (Lithuania), Guy Séderman (Finland),
Fritz Gusenleitner (Austria). The authors acknowledge the European Environment
Agency (http://www.eea.europa.eu) for making available their 2005 map of Europe’s
Biogeographical regions with national boundaries.

This study is part of two Europe-wide assessments of the risks associated with pol-
linator loss and its drivers, undertaken within the FP 6 Integrated Project “ALARM”

12 Stuart PM. Roberts et al. / BioRisk 6: 1-18 (2011)

(Assessing LArge scale environmental Risks for biodiversity with tested Methods:
GOCE-CT-2003-506675; www.alarmproject.net; Settele et al. 2005) and the FP 7
Collaborative Project STEP (Status and Trends of European Pollinators; www.step-
project.net; Potts et al. 2011).

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AppendixA

Summary data at 10’ grid cell resolution (UTM WGS84) used for mapping the 6 spe-
cies of Colletes in this study

Abbreviations used:

alb Colletes albomaculatus
anc Colletes anchusae

hed Colletes hederae

imp Colletes impunctatus
nig Colletes nigricans

wol Colletes wolft

For further information on the dataset, contact M. Kuhlmann.

alb

29SNB20 | 29SNB40__ | 29SNB51 30STB32__ | 30STB53
30SUB31 _|30SUB51 | 30SUB60 |30SUB69 | 30SUF08 _ | 30SUF44 30SVA86
30SVC56 | 30SVD63_|30SVG10 | 30SVG42__ | 30SVG80 | 30SVK72_| 30SVK82__| 30SWF09
30SWJ92_ | 30SXG39__ | 30SYH14 30TUM39_| 30TUMS51
30TVK09 | 30TVK39__ | 30TVK47 30TWL64 | 30TXM71 31SED39
31TBE96 | 31TBH77_ |31TCF24__|31TDHS2_ [31TDH87_ |31TEH95 [31TEJ40 _ | 31TFJ54
32SME66 | 32SME69 | 32SME72 32TLP0O | 32TLP10
32TLQ07 |32TPN59 | 32TPP14 33TUF66 | 33T VK28 33TYN17
33UXP35__|33UXQ42_ |34SEF68 |34SEG56 | 34SEH92__[34SFF49 | 34SFF75 _| 34SFF83
34SFG20 | 34SFG56__ | 34SFG57 34SFH29
34SFH60 | 34SFH81 | 34SFJ76 «| 34SGEG1__—- | 34SGG15_ |34SGH26__|34SGH44_| 34SGH52
348GJ03_[348Gy14__-|34TCs18-|34TCTS4 _|34TCT56 [34TELO1 | 34TEL47__ | 34TEMS53
34TEM61 |34TFM90_ | 34TGK34_ |35SKC30___[35SKV43__ | 35SKV61__[35SLB30__| 35SLU09
35SLU98 | 35SLV40 | 35SLV80__[35SMA96_[35SNB27__|35SNC15__[35TNG67_ | 35TNH52
35TPJ27 | 36RYA43__ | 36SUG87_|36SVG59_—- | 36SWG14_|36SXG44_ | 36SXH11 __| 36SXH69
36SXH95_ | 36SXJ84_- | 36TWL53_ | 36TWQ43_[36TWR20_ | 36TWRI1_ [36TXQI5 | 36TXQ28
36TYL30 _|37SBR69 _|37SCE71__[37SED09 _[37SED78__|37SFD01__|37SFD90__|37TCLO2
37TEE37__|37TFEG8 |37TGE16 [37TGE19 |37TGES9 |37TGFI2 |38SLH56 _ | 38SLJ39
38SL]91_ | 38SMG43__ | 38SMH02_ | 38TKK84__|38TMK44_| 38TMK55_ | 39STCo8 _ | 39STD50
ssw sesxvi7 [porta [osvn | |

34TCS18 | 34TDL83__|34TGNO8 | 35TLH39 | 35TLL95 | 35ULP69 | 35ULP79__| 35ULP89
35ULQ25_|35ULQ47_ | 35ULR41 35UMP47_| 36SUG90
36SWG14_ |36SXG41__ | 36SXH47 37SED08
hed

30TXR38_ | 30TYQ02 | 30UVA46 30UWB01 | 30UWB30
30UWB36 | 30UWB40 | 30UWB41_ |30UWB50 | 30UWBS1_ | 30UWB52 30UWB61
30UWB70 |30UWB71 |30UWB72 |30UWB74 |30UWB81 |30UWB82 | 30UWB92_ | 30UWV00
30UWV27_ | 30UWV37_ | 30UWV38 30UWV65_|30UWV97

Assessing continental-scale risks for generalist and specialist pollinating bee species... ues
30UXB42 |31TDGS6 |31TEJ25 |31TEJos |31TFJ06 | 31TE34 | 31TEJ85 | 31TFI95
31TEJ96 [31TFL50 | 31UCS23 31UES58 | 31UFS10
31UFS82 |31UFS83 | 31UFS93 32TKS62 | 32TKS96 32TLS18
32TLS72. | 32TMK49 |32TMS12 |32TMS93 |32TNK35 |32TNM46 |32TNR29_ | 32TPM59
32TPP24 | 32TPS67__| 32TPS75 32UMA23_|32UMAS1
32UMAS2 |32UMAS4 |32UMV39 |32UMV43 |32UMV49 |32UMV62 |33TUGO2 | 33TUK99
33TUL93 |33TUL97 |33TVK76 |33TVLO7 |33TVL14 |33TVL16 |33TVL67 | 33TWG71
imp
32TKQ82 |32TLQ25 |32TLQ47 |32TLR33. | 32TLR58 =| 32TLRS9 =| 32TLR6O =| 32T LR89
32TLS40 |32TLS6O |32TLS61 |32TLS71 |32TLS72 |32TLS8o |32TLS81 | 32TLS82
32TLS83. | 32TLS90 =| 32TLS91 +|32TLS92. «|| 32TMROO |32TMSOO |32TMS04 | 32TMS10
32TMS12__|32TMS21_| 32TMS22 32TMS45__| 32TMS66
32TMS74_ | 32TMS75_ | 32TMS78 32TMS97_ | 32TNS12 32TNS64
32TNS65 |32TNSG7 |32TNS68 |32TNS69 | 32TNS73_ _|32TNS75 | 32TNS76 | 32TNS83
32TNS87_ | 32TNS96_| 32TNS98 32TPS49__ | 32TPS59
32TPT32 | 32VNJ99_— | 32VNP42 33UUA74__| 33UVC10 33UVV78
33VUD71 | 33VWG72 |33VWH24 |33VWH70 |33VWK64 | 33WVN26 |33WWN93 |33WWR88
34UCF46 | 34UDG81_ | 34UDV34 34VDM36_|34VDM37
34VDM45 | 34VDM46_ | 34VDM48 34VEM17__ | 34VEM27 34VEM47
34VEM57_ |34VEM99_ | 34VEQ11 |34VEQ38 |34VER86 |34VEM03. |34VEM06_ | 34VEM09
34VEM13_ |34VEM14_ | 34VEM17 34VFRO8
34WDB85 | 34WDB9S | 34WDV53 34WES10 | 34WET20 35VLG67
35VLG77__|35VLG87_|35VLH56 |35VLH57—-|35VLH59_-| 35VLJ61_—- |35VMHO05._ | 35VMH40
35VMH62_|35VNG45_|35VNH26 35VNJ49
35VNJ68 | 35VNK04_ |35VNK11 |35VNK28 | 35VNK37_ |35VNK39 |[35VNL12_ | 35VNL13
35VNL99_ | 35VPH15 |35VPJ32-|35VPJ33.—« | 35WLM77_|35WLN81 |35WLN88 | 35WLN89
35WLN91 | 35WMM75 |35WMNOS |35WMN21 | 35WMN22 | 35WMN24 |35WNM25 |35WNM32
35WNM72 |35WNN90 [35WNP19 |35WNP91 |35WNS11 |35WPPOG |36VUQ67_ |36VVPO3
46UBU77 |46UBU96 |46UCA84 |46UCA94 |46UDA00 |46UDA12 |46UDA13_ | 46UDA21
46UDA22 | 46UDV87 |46UFA57 |46UFA68 |46UFVos |47TKM94 |47TLH38 |47TPK58
47TPL85 |47UNQ89 |48TUS28 |4sTwulo |4sTxT21 |48Txu40 |4sTxu41 | 48TXxU60
48TXU80 |48TXU81 |48TYU21 |4sUWwU97 |48UXD28 | 48UXU05 |48UXU26 | 48UXU27
48UXU41 |48UXvo0 |49TBP70 | 49UBQ70
nig a a a |
29RMNOO |29RMP40 |29RMP46 |29RNP17 |29RNP89 | 29RNQ72_ |29RNQ85 | 29RPQS6
29RPQ64 |29RQQ02 |29SMC68 |29SMC69 |29SMC87_ | 29sMC88_ | 29SMC89_ | 29SMC97
29SMD87_|29SNA09__ | 29SNB79 29SPB82
29SQD31_ |29TNF70_ | 29TNF78 29TNF95 | 29TPE24 30STB32
30STB99 _|30STC90 | 30SUAS7_|30SUB15__|30SUB69__| 30SUC01 | 30SUD07__| 30SUF06
30SUF44__|30SVC56__ | 30SVF36 30SVG60 | 30SVG80
30SVH43 | 30SVH54__| 30SVJ64 30SVK82_ | 30SWEO09 30SWG00
30SWG77_|30SWG86 |30SWH50 |30SXG05 _|30SXG38__| 30SXG39__|30SYH14__ | 30SYH56
30SYHS7__|30SYJ27__| 30TTL92 30TUM41_ | 30TUM52
30TVK39 | 30TVM48 | 30TWK02 30TXK66
30TXL37. |30TXMO1 |30TXM08 |30TXM98 |30TYL46 |30TYMO1 |30TYN30_ |31SBC48
31SBC59 _|31SCD41_|31TBE77 31TCF18 | 31TCF24
31TCE55 |31TCGoo |31TCGO1 |31TCG34 31TDH69 |31TDH87 |31TEGI7
31TEG28 |31TEHOO |31TEJ11 — |31TEI44 31TFJ54 |31TEJ63 | 31TEJ67
31TFJ69 |31TEJ75 «| 31TFJ76—_—«| 31 TFJ84 31TF]92.-|31TEJ96~—- | 31 TFK62

18 Stuart RM. Roberts et al. / BioRisk 6: I-18 (2011)

31TFK65 | 31TFL46 | 31TGJ21__|32SMD78_ [32SMF78__[32TKN88_ [32TKP74 __| 32TKP95
32TKS62 [32TLNO8 | 32TLP10 32TLP27__| 32TLP28

32TLP33. | 32TLP43. (| 32TLP75 32TLQ03 | 32T LR66 32TLS51

32TLS71 |32TLS72__-|32TLS81 [| 32TLS82_—_-[32TLS83_ | 32TLS91_—[32TLS92__ | 32TLS93

32TLT40__ | 32TMM80 | 32TMN71 32TMS02__ | 32TMS03
32TMS12_|32TMS22__|32TNK45__|32TNK57_[32TNM13_[32TNN22_ [32TNQ81_|33SUC10
33SWB08 | 33SWB28 |33SXD29 | 33TTG93 | 33TUF66 | 33TULI4 |33TUL56 | 33TUL87
33TUL93 | 33TVF32__|33TVG06__|33TVK39__[33TVK76 | 33TWG74 |33TXF90 | 33TXJ11

33TXJ21 | 34SEF99

wol

32TMQ21_| 32TMQ23_ | 32TMQ24_[32TMQ42_ [33TTH66 | 33TUG88 | 33TUG92_ | 33TUG98
33TUHOS |33TUHO6 |33TvGo2 | | | | |

Appendix B

Indicative map of the European biogeographical regions, 2005 (baseline map: OEEA,
Copenhagen, 2007).

| Indicative map of the
European blogeographical

regions, 2005

Alpine
Anatediain

Artic

ALLaritic

Black sia
Boreal
Continental
Macaronesia
Mediterranean
Pannenian

Sheppic
Outside data

CRORREORORE

Baseline map ©@ EEA,
Copenhagen, 2007