Journal of Natural History

ISSN: 0022-2933 (Print) 1464-5262 (Online) Journal homepage: http://www.tandfonline.com/loi/tnah20

Hitchhiking with the Vikings? The anthropogenic

bumblebee fauna of Iceland – past and present

Oliver E. Prŷs-Jones, Kristján Kristjánsson & Erling Ólafsson

To cite this article: Oliver E. Prŷs-Jones, Kristján Kristjánsson & Erling Ólafsson (2016):
Hitchhiking with the Vikings? The anthropogenic bumblebee fauna of Iceland – past and
present, Journal of Natural History, DOI: 10.1080/00222933.2016.1234655

To link to this article: http://dx.doi.org/10.1080/00222933.2016.1234655

Published online: 11 Oct 2016.

Submit your article to this journal

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at

http://www.tandfonline.com/action/journalInformation?journalCode=tnah20

Download by: [Ryerson University Library] Date: 11 October 2016, At: 14:29
JOURNAL OF NATURAL HISTORY, 2016
http://dx.doi.org/10.1080/00222933.2016.1234655

Hitchhiking with the Vikings? The anthropogenic bumblebee

fauna of Iceland – past and present
a b c
Oliver E. Prŷs-Jones , Kristján Kristjánsson and Erling Ólafsson
a
Independent Researcher, Denbigh, UK; bReykjavik University, Reykjavik, Iceland; cThe Icelandic Institute of
Natural History, Reykjavik, Iceland

ABSTRACT ARTICLE HISTORY

The number of bumblebee species found in Iceland has doubled Received 13 April 2016
from three to six in 35 years. This paper considers the colonisation Accepted 1 September 2016
of Iceland by bumblebees; updates information on Bombus KEYWORDS
(Pyrobombus) jonellus (Kirby), B. (Megabombus) hortorum (L.) and Iceland; bumblebees;
B. (Bombus) lucorum (L.); presents findings for two new colonists, B. distribution; dispersal;
(Pyrobombus) hypnorum (L.) and B. (Thoracobombus) pascuorum colonisation; anthropogenic
(Scopoli); and considers the arrival of another species, B. effects
(Pyrobombus) pratorum (L.), that may have become established.
The context of bumblebee dispersal to remote islands is consid-
ered. Many of the restricted number of insect species that have
colonised North Atlantic islands have done so in association with
man. B. (Bombus) terrestris (L.) has been used as a pollinator in
glasshouses in Iceland since 1994, and it may also have become
naturalised. Barcoding is needed to check the identity of some
specimens. B. jonellus has probably been present for at least
several hundred years; genetic studies should help determine
whether the timescale for its arrival is compatible with an anthro-
pogenic origin. It is suggested that consideration is given to ways
of reducing both unintended introduction of bumblebee species
with cargo, and the release and disease risk of those imported
intentionally for commercial use.

Introduction
Anthropogenic change influences species composition and the environments on which
those species depend. Iceland is remote from continental landmasses and about half its
100,000 km2 are inhospitable lava desert and glaciers. Peripheral areas support most
plant cover, including a limited range of flowering species suitable as food sources for
bumblebees. Thirty-five years have passed since we first considered the composition
and distribution of the bumblebee fauna (Prŷs-Jones et al. 1981); in that time the
number of bumblebee species in Iceland has doubled, resulting in evolving patterns
of distribution and ecological interaction in a new environment. This paper considers
how bumblebees got to Iceland, summarises our knowledge of the species currently

CONTACT Oliver E. Prŷs-Jones [email protected] Independent Researcher, Ysgubor Ystlum, Waen, Bodfari,
Denbigh, LL16 4DE, UK
© 2016 Informa UK Limited, trading as Taylor & Francis Group
2 O. E. PRŶS-JONES ET AL.

known to occur there, and discusses factors influencing their distributions and ecology
in a relatively challenging environment.

Colonisation in context
The last glaciation ‘wiped the slate clean’, covering Iceland with an ice sheet that
reached maximum extent about 18,000 years BP (Hubbard et al. 2006; Clark et al.
2009). As deglaciation progressed in the Northern Hemisphere, Greenland, Iceland and
the Faroe Islands gradually became habitable again, separated from one another and
from Europe and North America by wide expanses of northern sea (Downes 1988).
Species diversity in these islands remains limited, with an absence of endemic species,
reflecting their geographical isolation and the lack of suitable Ice Age refugia for the
survival of most pre-existing organisms (Downes 1988; Buckland et al. 1996; Ingólfsson
2009).

Dispersal and colonisation

Occasional dispersal events between landmasses may be inconspicuous when a species
fails to establish, or when genetic dilution occurs through interbreeding with a closely
related resident population. One cannot distinguish unsuccessful dispersal due to dis-
tance from successful dispersal that does not lead to colonisation – unless one stumbles
across the vagrant individual involved. Absence may not indicate lack of successful
dispersal if a threshold ‘dose’ of immigrants is needed for establishment and this
requirement is not met due to distance from the source. However, where a single
fertilised queen is sufficient to effect colonisation, as is almost certainly the case in
bumblebees, presence or absence can be a good indicator of dispersal range if there are
no issues such as resource availability or genetic dilution through interbreeding.
Bumblebee dispersal has never been studied directly (Lepais et al. 2010); they are
known to travel over open water – notably when weather conditions are settled and
winds are light – and they are able to maintain a consistent heading, at times orientating
into wind (Mikkola 1978, 1984). Queens observed flying across the Gulf of Finland were
probably successful at reaching Estonia from Finland, travelling at least 75 km over
water (Mikkola 1984). In settled conditions, without significant headwind, distances of
80–100 km might be covered in about 3 hours if one assumes a flight speed of the order
of 30 km/hour, as Mikkola (1984) does. Using values for rate of energy consumption in
flight, and excluding reserves of energy in the fat body, a bumblebee carrying 90
microlitres of a 60% sucrose solution should be able to fly for about 3 hours (Corbet
et al. 1995). Within their maximum flight range, the chance of making landfall will bear
some relationship to the proportion of the flight horizon that is land. A long inlet with
parallel coasts may make the Gulf of Finland an ideal situation for successful dispersal
over water. In practice, conditions are seldom ideal and most often variable, especially
out over the North Atlantic. In unsettled weather, flight into wind is a poor means of
maintaining a heading or ‘ground’ speed, reducing effective range. In addition, aspects
of bumblebee biology restrict their ability to make long sea crossings: colonisation
requires a fertilised queen, and these are present only after emergence from hibernation
in spring, and in late summer or autumn, when weather conditions are often poor, and
 JOURNAL OF NATURAL HISTORY 3

new ‘autumn’ queens are heavily laden with crop contents and stores of fat for
hibernation.
In practice, and in contrast to the situation for wind-borne insects, relatively narrow
stretches of sea can be effective barriers to bumblebee dispersal, with a significant
negative correlation found between the percentage of mainland species on an island
and its distance from adjacent mainland (Pekkarinen and Teras 1993). Colonisation is
often taken to have been ‘natural’ (i.e. unaided by man), but this should not be assumed.
While there is likely to be species variation in dispersal range and propensity, there is
direct and indirect evidence that maximum flight range over water probably does not
often exceed 60 km, and may often be considerably less. In Scotland, genetic evidence
from Hebridean island and mainland populations suggests that Bombus jonellus may be
able to cross sea barriers of > 30 km, while in other species, genetic diversity and
differentiation on islands show that distances > 10 km can be a significant barrier to
movement (e.g. Darvill et al. 2006, 2010; Goulson et al. 2011; and see Boff et al. 2014).
Britain and France are 33 km apart at their closest, the Strait of Dover. This is a distance
that seems to have proved a barrier to unassisted colonisation of Britain by some
European bumblebee species, with the possible exception of Bombus pomorum, found
for a short period on the channel coast of Britain, and, perhaps more ambiguously, of
recent colonisation by B. hypnorum. There remains the possibility that for some species,
present on both sides of the Strait of Dover, a degree of natural background cross-
channel movement may be occurring of which we are presently unaware. In New
Zealand, Macfarlane and Gurr (1995) reported B. terrestris, and undetermined bumble-
bees, as present on 23 islands 2.5–30 km offshore (whether any were introduced
intentionally is not known) and absent from seven island groups between 16 and
55 km offshore. In a five-year study, 15 queens of 10 species of true (nonparasitic)
bumblebees were recorded on North Sea and Baltic Sea lightships, up to 30 km offshore
(Haeseler 1974), with three queens caught on the most distant ship from land (one B.
distinguendus and two Bombus hortorum). Over a 36 year period, observers on oil
platforms in the North Sea reported four instances of bumblebees found aboard: two
25 km offshore, one at 31 km and one at 52 km (1979–2015; pers. comm., North Sea Bird
Club). Recent work by Williams et al. (2015) has shown that the third widest oceanic
divide between significant landmasses in the arctic/subarctic, the Bering Strait, at 82 km,
seems to be an effective barrier to those species occurring on either side – which are
genetically distinct although phenotypically cryptic. Even this might not rule out a low
frequency of successful dispersal events across the Strait, evidence for which might be
lost by genetic assimilation through hybridisation with sibling species on the other side
(e.g. see Ings et al. 2010).

Natural vs assisted colonisation

So how far is too far for dispersal over water? Improbable colonisation events do occur,
unassisted by man; nevertheless we should be mindful that Iceland is 280 km from
Greenland (the two islands have no bumblebee species in common), 400 km from the
Faroe Islands (where there were no bumblebees until very recently; Madsen and Jensen
2011), 800 km from Scotland and 950 km from Norway. The latter two distances
represent 26 and 32 hours’ flight time at a flight speed of 30 km/hour, without
4 O. E. PRŶS-JONES ET AL.

headwind; at best 13 and 16 hours in a body of air moving in the same direction at
30 km/hour. Vagrancy patterns in birds reveal that North American species reach Europe
aided by Atlantic depressions travelling north-east in autumn (Lees and Gilroy 2009) –
weather patterns that are likely to present an additional hindrance to westward dispersal
by bumblebees from Europe. And unlike many birds, and a few specialised species of
bees, bumblebees do not continue to fly after dark (e.g. see Burgett and Sukumalanand
2000; Warrant 2008; Somanathan et al. 2008; Reber et al. 2015).
Historically, the sole bumblebee species known from Iceland was B. jonellus (Prŷs-
Jones et al. 1981). No other aculeate hymenopterans (bees, wasps and ants bearing a
sting) are found there (Downes 1988) other than those introduced by man – intention-
ally, in the case of the honeybee, Apis mellifera, (Matthiasson 1934; Kristjánsson 1992) or
accidentally, in the cases of a number of hymenopteran species (Dolichovespula norwe-
gica, Vespula vulgaris, V. rufa, V. germanica, Polistes associus, P. dominulus and Lasius niger
(see Ólafsson 1979). This context makes it seem clear that bumblebee species in Iceland,
including B. jonellus, along with species on many Atlantic (Marcronesian) islands that are
distant from an adjacent landmass (the Azores, Madeira and perhaps even the Canary
Isles), have benefitted from ‘assisted passage’, and become long-distance colonisers
through the medium of man’s activities in the historic and possibly also in the pre-
historic past. In Iceland, the earliest reference to what were probably bumblebees
(‘hunangsflugur’) is found in Guđmundsson (c. 1640; see ‘A chronological bibliography
of bumblebees in Iceland’ an appendix to Prŷs-Jones et al. 1981). It seems plausible, and
perhaps more likely, that B. jonellus ‘hitchhiked’ to Iceland by hibernating in ships’ stores
(such as hay) – possibly those of eighth–early ninth century Irish monks, or more
plausibly with ninth–tenth century Vikings, or later, in mediaeval times – than that it
flew there unaided. The additional possibility of intentional introduction, even at such an
early date, cannot be excluded.
The recent history of Iceland has been dominated by anthropogenic changes (see
Buckland et al. 1998; Streeter et al. 2015). It is thought that 24,000 people arrived in
Iceland over a 20-year period from about 870 (Vésteinsson and McGovern 2012). They
were responsible for drastically modifying the habitat by forest clearance, reducing
cover from 27% to c. 1% by 1950, with accompanying soil erosion – in part due to
the grazing pressures of introduced farm animals. The arrival of cereals and animals was
accompanied by a diverse insect fauna, both synanthropic and incidental (Smith 1995);
while many invertebrate species are thought to have arrived as stowaways in the ballast
and dunnage of Norse ships (Enckell and Rundgren 1988; Sadler 1991).
In the absence of endemic species, human settlement in Iceland has generally
involved addition rather than loss of species. Types of imports arriving by air and sea
were relatively limited until a few decades ago. This probably served to restrict the
number of ‘phoretic’ colonists (species inadvertently introduced by man’s activities).
Dramatic increases in the variety and quantity of imports, particularly since the Second
World War, have been paralleled by increasing numbers of introduced species (see
Hulme 2009), with few controls that might have prevented them. In 1981, we described
the discovery in Iceland of two bumblebee species previously unrecorded there: B.
hortorum and B. lucorum sensu stricto (Prŷs-Jones et al. 1981). Evidence from collections
suggests that B. hortorum established in the 1950s, while B. lucorum was not recorded
before 1979. Both species were first recorded within 10 km of the port in Reykjavik,
 JOURNAL OF NATURAL HISTORY 5

suggesting that a queen or queens probably arrived hibernating in cargo – although,

again, intentional introductions cannot be excluded. Several species of bumblebee that
overwinter in the ground have been found to make use of peat as a site for hibernation
(e.g. B. pratorum, B. lapidarius and B. hortorum, OEP-J pers. obs.), making imported pot
plants one potential source for introductions. So far as we know, B. hypnorum uses
predominantly ‘above ground’ hibernation sites, for example behind bark (OEP-J,
unpub.). It may therefore be imported with timber, particularly that from which the
bark has not been removed; it has also been found to make use of plant compost in
hanging baskets (OEP-J, unpub.). The first records of B. hypnorum in Britain and Iceland
occurred within a few years of each other (2001 and 2008), near ports (Southampton
and Keflavik respectively (Goulson and Williams 2001; Ólafsson 2010)), and are compa-
tible with cargo-associated transport. Horticultural and arboricultural produce has been
suggested as a vector for introduction of a variety of species, such as the white-toothed
shrew to Ireland (Gargan et al. 2016).
An additional colonisation route for new bumblebee species is through escape from
commercial use in glasshouses, where they are used for crop pollination. B. terrestris was
first imported to Iceland for this purpose in 1994, and has become increasingly popular
up to the present time (Kristjánsson and Lárusdóttir 1994; Lárusdóttir 1995; Kristjánsson
2013). Phenotypically B. terrestris can be hard to separate from B. lucorum and further
work is needed to determine whether it is now established in the country (see below).
The anthropogenic environment includes plants: in the last 30 years the invasive alien
perennial herb Lupinus nootkatensis has spread explosively throughout Iceland and now
covers thousands of square kilometres of land. It grows over previously unvegetated
lava fields as well as low-growing native vegetation and presents a real threat, particu-
larly to dwarf shrub heathland vegetation (Magnússon et al. 2003), on which B. jonellus
has traditionally depended for forage. First imported to Iceland in 1885 for use in plant
trials, further seed of the Nootka lupin came from Alaska in 1945, and the species
became naturalised in Iceland Forestry Service sites. Since 1986 it has been cultivated
and sown in land reclamation projects by the Soil Conservation Service (Bjarnason 1946,
1981; Magnússon 2001, 2010). As a nitrogen-fixer, it proves useful for colonising and
stabilising poorly vegetated areas, creating and improving grazing.

Species accounts
Large parts of the interior of Iceland are relatively barren lava fields, unsuitable for
bumblebees. Likewise, much of the more vegetated coastal land is used for agricultural
purposes, and here silage production and grazing can restrict bumblebee foraging and
nesting opportunities.
The season during which bumblebees can be active varies somewhat with the
weather from year to year; it is usually about 5 months long, from mid April until the
beginning of October in urban areas, and from early May to mid September in the wider
countryside.
B. hypnorum was discovered in Keflavik in the south-west of Iceland in 2008 (Ólafsson
2010); B. pascuorum in Hveragerdi, also in the south-west, in 2010 (Ólafsson 2010–2013);
while B. pratorum turned up in the extreme east of Iceland, in the town of Eskifjördur,
also in 2010.
6 O. E. PRŶS-JONES ET AL.

Maps presented below are conservative estimates of distribution, based solely on

bees that have been collected, by both the public and researchers. Collection effort is
likely to reflect centres of population and vegetated areas; however, these are also the
areas most suitable for bumblebees. Specimens were curated by Erling Ólafsson, and are
housed in the Icelandic Institute of Natural History, Gardabaer.

Bombus (Pyrobombus) jonellus (Kirby) – ‘Móhumla’ in Icelandic, or

Peat bumblebee. (Known in Britain as the Heath bumblebee.)

Distribution and habitats

Where sheep grazing is not intense, and particularly where fencing excludes it, B. jonellus
has a widespread distribution in the predominant vegetated habitats, namely subarctic
tundra (dwarf shrub heathland vegetation), remnant boreal birch forest and planted
coniferous woods (Figure 1(a)). Birch forest was previously much more extensive, parti-
cularly in the south (Eysteinsson 2009). Conifer plantations are now gradually increasing
in number and often support reasonable numbers of B. jonellus when planted at a
density that allows a ground flora to persist between them. The distribution of B. jonellus
extends to patches of subarctic tundra on the central plateau, most notably where
grazing pressure is low or excluded.

Nesting
B. jonellus is a surface, sub-surface and occasional aerial nester, making use of suitable
insulated sites in vegetation, under stones, and in rock piles, dry stone walls and birds’
nests (both on the ground and in trees). Most nests that have been examined were at
Heiđmörk, near Reykjavik (Sveinsdóttir 1981; Kristjánsson 1983), an ungrazed moorland
study site of predominantly dwarf shrub heathland. Nests were mainly within or just
below the base of surface vegetation and under rocks, and in most cases fine dry plant
stems and roots had been used to form an insulating cover for the nests (Figure 2).
Measurements were made of the depth of the nest from the surface, and, in some cases,
the distance from the nest entrance to the nest itself (Table 1). Fine grasses were
prominent in the covering of all but one of these nests, together with moss and other
plant material. One nest (VII) was in a pine grove, and its covering comprised tougher
plant material, including coarse grass and leaves (probably from willows).
Table 1 gives the impression that nests are often considerably deeper than subsur-
face. This reflects the rocky nature of the ground at this study site, where bees crawled
between large stones to access some nests. Where the ground surface is flatter, the
majority of nests seem to be positioned at or just below the surface (see Figure 2). Birds’
nests are also used. Petersen and Thorstensen (1991) found evidence for the use of nests
of six passerine species, on and above ground level (primarily wren, Troglodytes troglo-
dytes; but also redwing, Turdus iliacus; white wagtail, Monticilla alba; meadow pipit,
Anthus pratensis; redpoll, Acanthis flammea, and snow bunting, Plectrophenax nivalis).

Foraging
Although similar in appearance to B. hortorum, B. jonellus has a short face and tongue,
and consequently forages on a different range of species. Forage plants in Iceland
 JOURNAL OF NATURAL HISTORY 7

Figure 1. Distribution records of bumblebee species in Iceland.

mainly comprise dwarf shrub heathland species such as bilberry (Vaccinium uliginosum
and V. myrtillus), bearberry (Arctotaphylos uva-ursi), common heather (Calluna vulgaris),
thyme (Thymus praecox), species of willow (Salix phylicifolia, S. lanata, S. arctica, S.
herbacea) and wild geranium (Geranium sylvaticum) (see Table 2).
8 O. E. PRŶS-JONES ET AL.

Figure 2. Bombus jonellus nests. The white arrow indicates the unopened nest ball of Nest 1 (made
up of dead plant material surrounding the nesting cavity). Further details for each of these nests are
given in Table 1. (Photos: Oliver Prŷs-Jones.)

Table 1. Details of Bombus jonellus nest sites.

Nest depth from Nest opening
Nest Date surface (cm) to nest (cm) Comments
1 19.07.79 5 10 Immediately below boulder.
2 21.07.79 3 5 Within tussock of surface vegetation.
3 24.07.79 60 c. 80 Between jumbled blocks of lava covered in turf.
4 26.07.79 15 18 Amongst plant roots within loose dry moorland turf.
5 02.08.79 3 10 Directly under small boulder lying on moorland turf.
I 26.06.81 5 - -
II 01.07.81 8 - -
III 10.07.81 13 - -
IV 15.07.81 3 30 Directly under the surface of moss heath. Tunnel alongside a
prominent Vaccinium branch.
V 30.07.81 25 25 Tunnel to nest.
VII 10.08.81 45 - Under dense turf; bees accessed nest via a vertical fissure
between turf and a large rock.
VIII 26.08.81 30 90 Bees walked 50 cm horizontally on rock, then 40 cm vertically,
beside a rock, to a small cavity beneath it.
Nests 1–4 are illustrated in Figure 2. Nest 2 was at Skaftafell; nest 4 was SW of Vifilstađavatn; the others were at
Heiđmörk, near Reykjavik. ‘Nest opening to nest’ indicates the approximate distance a bee had to walk to access the
nestball, where this information was recorded. Nest data: 1–5 OEP-J (pers. obs., 1979), I–VII Sveinsdóttir (1981).

Clearly B. jonellus adapts to local conditions to an extent: in Iceland its predominant

habitat is subarctic tundra, while in continental Europe it can also be found in wooded
mountainous areas (von Hagen and Aichhorn 2003), and in Britain it is closely associated
with heathland and moorland (Benton 2006). It is seldom found foraging in gardens and
urban sites unless these are interspersed with native habitat and flora.
 JOURNAL OF NATURAL HISTORY 9

Table 2. Plant species visited by bumblebees in Iceland (for species for which
there are records), with an indication of probable significance as sources of
forage.
Bumblebee species (Bombus)
Plant species B. jonellus B. hortorum B. lucorum B. hypnorum
Native species
Arctostaphylos uva-ursi **** ****
Vaccinium uliginosum **** ****
Vaccinium myrtilis **** ****
Calluna vulgaris **** ****
Thymus praecox **** ****
Salix spp. **** ****
Geranium sylvaticum **** * **** **
Trifolium repens **** ****
Angelica sylvestris ** **** **
Rhinanthus minor **
Dryas octopetala **
Geum rivale **
Hieracium spp. **
Leontodon autumnale **
Potentilla palustris **
Ranunculus acris * ***
Taraxacum spp. * ***
Rubus saxatilis *
Viola tricolor *
Galium verum *
Armeria maritima *
Bartsia alpina *
Rhinanthus spp. *
Filipendula ulmaria *** **
Introduced species
Lupinus nootkatensis *** * **** **
Lamium spp. * **
Delphinium spp. * ****
Cotoneaster sp. **
Teucrium sp. *
Veronica longifolia *
Angelica archangelica * **** **
Aconitum spp. ****
Aquilegia spp. ****
Symphytum spp. ****
Anchusa azurea **
Silene dioica **
Pulmonaria mollissima **
Lepidum spp. *
Paeonia spp. *
Papaver sp. *
Geum pallidum *
Campanula carnica *
Borago officinalis *
‘Significance as forage’ is a subjective estimate: * = least significant; **** = most significant.
‘Native’ indicates species of long standing, although some may be anthropogenic in origin.
‘Introduced’ refers to species mainly grown as garden plants.

Status and future

Widely distributed in vegetated areas, our subjective impression is that B. jonellus has
become considerably less common over the past 35 years. Land management in
cultivated areas has become more intensive, causing a general reduction in the avail-
ability of forage plants for all bumblebee species. Grazing pressures on the extensive
10 O. E. PRŶS-JONES ET AL.

tracts of ‘common’ land (mainly subarctic tundra) vary widely: where intensive, they
cause a marked reduction in the availability of nectar and pollen sources for any
bumblebee species that are able to live there.
Other potentially deleterious effects on the population of B. jonellus could result from
introduced diseases. Whether B. jonellus in Iceland proves to be of early anthropogenic
origin or a natural coloniser, it has lived in isolation from other bumblebee species for a
prolonged period; it may also have low genetic diversity. As a result, it may be
particularly susceptible to diseases carried by recently colonising bumblebee species.
For example, during a study in 1979 in which queens were dissected, no evidence was
found for the presence of the nematode parasite of bumblebees, Sphaerularia bombi
Dufour (Kristjánsson 1983) – a disease common in many bumblebee populations.
In addition, the competitive environment for B. jonellus will almost certainly have
been fuelled by the spread of B. lucorum throughout the country, as it feeds on a very
similar range of plant species (Table 2, and see below). There is a ‘catch-22’ for B. jonellus:
while grazing suppresses native flowering plants, the exclusion of grazers allows the
introduced Nootka lupin to thrive and overgrow dwarf shrub heathland vegetation. The
lupin therefore shades out important forage plants, such as Vaccinium, on which B.
jonellus has traditionally depended. Although it provides pollen for B. jonellus, its flowers
are more easily triggered by the larger, recently arrived, Bombus lucorum. The implica-
tion is that lupin fuels the developing interspecies competitive environment, and gives
B. lucorum an advantage. Whether this has affected the numbers of B. jonellus is unclear.
Although there are reasons for concern about unchecked spread of the lupin (e.g. see
Hiltbrunner et al. 2014), control of it is a controversial topic: in the wider environment,
and in a wider context, arguments can be made both for and against its presence (see
Benediktsson 2015). Given the invasive nature of the plant, we feel vigilance is required
to prevent further colonisation of the national parks, and to selectively eradicate it from
other areas supporting a significant presence of native vegetation.

Bombus (Pyrobombus) hypnorum (Linnaeus) – ‘Rauðhumla’ in Icelandic,

or Red bumblebee. (Also known as the Tree bumblebee.)

Distribution and habitats

This species was first recorded in 2008 in the south-west, at Keflavik, not far from the
port and the country’s international airport (Ólafsson 2010, 2010–2013). It has since
spread to towns throughout the south-west of the country (Figure 1(b)).

Nesting
Queens are observed from mid-April. B. hypnorum is strongly synanthropic and almost
all nests are positioned above ground in man-made structures (particularly roof spaces
and cavity walls in houses), holes in trees and probably also in cliffs (it has been seen
foraging close to cliffs at Almannagjá Gorge, Thingvellir National Park, but not at other
sites in the park). Given the rarity of suitable tree-based nest sites in Iceland, B. hypnorum
will probably leapfrog from one town to another where these support suitable flowers
for foraging.
 JOURNAL OF NATURAL HISTORY 11

Foraging
The species has a short tongue, of similar length to those of B. jonellus and B. lucorum;
unlike B. lucorum it is not known to perforate the corolla tubes of long tubed flowers in
order to collect nectar. A generalist forager, it makes use of a wide range of flower types
that provide accessible nectar. The list of plants species visited by B. hypnorum in Iceland
(Table 2) is likely to get much longer, and their relative importance as sources of forage
to become clearer, as more observations are made.

Status and future

As a strongly synanthropic species throughout much of its range, having a relatively
short colony cycle, it will probably continue to prosper in Iceland in urban environments.

Bombus (Pyrobombus) pratorum (Linnaeus) – no Icelandic name.

(Known in Britain as the Meadow bumblebee.)

Distribution and habitats

B. pratorum has only been found in the extreme east of the country, where a worker
and male were collected in a garden in the centre of the town of Eskifjördur (Figure 1
(c)). This is within 20 km of Seyðisfjörður, where the ferry arrives from Tórshavn, in
the Faroe Islands – where B. pratorum was also found in 2010 (Madsen and Jensen
2011). The ferry sails from Hirtshals in Denmark to the Faroes, and then on to Iceland,
so it seems likely that B. pratorum has been introduced to both countries from
Denmark.

Nesting
No nests have been found in Iceland. In Britain, B. pratorum is a highly adaptable and
opportunistic in its choice of nesting sites, making use of a wide variety of well insulated
natural and man-made sites, including bird and rodent nests. Most nests are situated on
or above ground (Fussell and Corbet 1992). B. pratorum has a short colony cycle in
Britain, where it is able to undergo a second cycle of colony activity in some years (Prŷs-
Jones and Corbet 2011).

Foraging
Foraging preferences in Iceland have not been determined. Where it was found, in
Eskifjördur, it was foraging on raspberry flowers (leading to more ripe fruit that summer
than ever before!). In Britain, B. pratorum makes use of gardens and the wider country-
side for foraging and nesting, and visits a broad variety of flower types. It has a reason-
ably short tongue, but also a relatively narrow head, making nectar accessible from
slightly deeper corolla flowers than might be anticipated. It does not bite holes in order
to collect nectar, but does make secondary use of those bitten by species such as B.
lucorum and B. terrestris.
12 O. E. PRŶS-JONES ET AL.

Status and future

It would appear that at least one nest produced workers and males in 2010, but it is not
yet clear whether the species has successfully established itself in the country. If it does
so, we anticipate it will do best in urban areas with gardens.

Bombus (Megabombus) hortorum (Linnaeus) – ‘Garðhumla’ in Icelandic, or

Garden bumblebee. (Known in Britain as the Small garden bumblebee.)

Distribution and habitats

In Prŷs-Jones et al. (1981) it was suggested that B. hortorum might be dependent on
introduced plants growing in gardens. Current distribution records continue to support
this view. It is still found mainly in the Reykjavik area and surrounding towns, (Figure 1
(d), cf. fig. 1 in Prŷs-Jones et al. 1981). Failure to spread throughout the country is
probably attributable to a lack of plant species in the Icelandic flora with corolla-tubes
long enough to provide B. hortorum with a reasonably exclusive, and therefore pre-
dictable, supply of nectar.

Nesting
Iceland has a summer short in days but long in hours of daylight. B. hortorum has small
colonies and a short colony cycle (Prŷs-Jones and Corbet 2011), presumably requiring a
high rate of gain of nutrients per unit time in order to allow a rapid switch to the
production of males and queens. The presence of new queens (a number of which were
covered in mites) collecting pollen loads at the end of July 2015 (Figure 3) makes an
attempt at a second cycle of reproductive activity within a season a possibility – even in
2015, which had an unusually cold summer; a second cycle of colony activity seems to

Figure 3. New queens of Bombus hortorum foraging for nectar and pollen on Aconitum sp., Botanic
Gardens, Reykjavik, 30 July 2015. Note mites near the wing bases (centre), and the long tongue
(right). (Photos: Oliver Prŷs-Jones.)
 JOURNAL OF NATURAL HISTORY 13

occur in parts of Britain in some years (Prŷs-Jones 1982; Prŷs-Jones and Corbet 2011). As
yet there is no information on the location of nest sites in Iceland.

Foraging
B. hortorum has a very long tongue relative to other species in Iceland (Figure 3). Sources
of nectar, and to a lesser extent pollen, include a range of garden flowers possessing
long corolla-tubes, such as Aconitum (see Figure 3), Delphinium and Aquilegia species
(Table 2). Pollen-collecting individuals of B. hortorum make some use of open-flowered
species, such as poppies and peonies (Table 2); however, the majority of pollen is
collected together with nectar (Prŷs-Jones 1982), and consequently derives from flowers
with long corolla tubes.

Status and future

Given its restricted distribution in a man-made environment, the future of B. hortorum is
heavily dependent on continued availability of exotic long corolla flowers in gardens.
The native flora on its own is probably too restricted in terms of floral morphology, and
therefore nectar availability, for B. hortorum to co-exist with shorter tongued species.

Bombus (Thoracobombus) pascuorum (Scopoli) – ‘Ryđhumla’ in Icelandic, or

Rusty bumblebee. (Known in Britain as the Common carder-bee.)

Distribution, habitats and foraging

First discovered in 2010, at Hveragerdi, in the south-west of the country, it is now also
encountered in the north, around Akureyri (Figure 1(e)). These areas are 280 km apart
and the species may have arrived in them independently rather than spreading from
one to the other; it has not been recorded at sites in between. Interestingly, Hveragerdi
is a centre of greenhouse horticulture using geothermal heat, and it is possible that B.
pascuorum arrived there with imported plants.

Nesting
No nests have yet been found in Iceland. Elsewhere it is an invariable surface-nester,
utilising grass tussocks and dense surface vegetation, and so it may do best in agricul-
tural and coastal areas.

Foraging
B. pascuorum has a longish tongue. Foraging preferences are yet to be determined in
Iceland; from experience in other countries it is anticipated that it will make use of
elements of the native flora as well as some garden plants.

Status and future

B. pascuorum seems to have become established in two small cultivated areas of south-
west and north central Iceland. Given that in Britain it has the longest colony cycle (Prŷs-
Jones and Corbet 2011), it will be interesting to see whether day length in Iceland
compensates sufficiently to ensure its persistence in a short season.
14 O. E. PRŶS-JONES ET AL.

Bombus (Bombus) lucorum (Linnaeus) – ‘Húshumla’ in Icelandic, or

House bumblebee. (Known in Britain as the Small earth or
White-tailed bumblebee.)

Distribution and habitats

B. lucorum was first found in the capital, Reykjavik, in 1979. The last 35 years have seen a
massive expansion in its distribution (Figure 1(f)), as anticipated in Prŷs-Jones et al.
(1981), based on its foraging preferences and nesting habits in other areas. It has spread
throughout the lowlands and up to the edges of the central plateau. Subarctic tundra
and its associated flora are similar to the conditions found in much of its northern
Palearctic range, and it is doing well in this environment. In contrast to B. jonellus, it also
makes use of gardens and cultivated areas where these support suitable forage plants,
such as clovers and lupins. At lower latitudes it is a relatively long-cycle species; never-
theless, it manages to reproduce successfully in Iceland, so the long daylight hours of
summer seem to provide ample compensation for a short season. Spring queens appear
in numbers from about 20 April, and autumn queens are observed into October. It may
now be commoner than B. jonellus over much of the country, and has probably
benefitted disproportionately from the spread of the Nootka lupin. B. lucorum foragers
appear to work lupin flowers with greater ease than the smaller and weaker foragers of
B. jonellus.

Nesting
In other countries, B. lucorum nests are predominantly underground. This is also true of
those nests that have been found in Iceland. Nesting places include man-made sites
under buildings and sheds, in contrast to B. jonellus.

Foraging
B. lucorum has a short tongue and can bite holes in the corollas of long tubed flowers,
where these are available, and collect nectar. In common with B. jonellus, the majority of
individuals forage in subarctic dwarf shrub heathland. Unlike B. jonellus, and in common
with B. hortorum, it is also found in urban environments; here it forages in gardens and
visits a wide range of short corolla and open flower types that provide nectar, pollen or
both.

Status and future

B. lucorum is part of a complex of sibling species, including B. cryptarum and B. magnus,
that are morphologically similar and difficult or impossible to distinguish reliably on that
basis (Bertsch et al. 2004; Murray et al. 2008; Carolan et al. 2012; Williams et al. 2012;
Scriven et al. 2016). So far, only a single Icelandic specimen has been barcoded as a
check on identity (Williams et al. 2012), and this should be borne in mind when
considering the distribution map (Figure 1(f)). As each distribution record is associated
with a specimen, additional work should help determine whether or not B. cryptarum, B.
magnus, and B. terrestris (see below) are also present.
 JOURNAL OF NATURAL HISTORY 15

Bombus (Bombus) terrestris (Linnaeus) – no Icelandic name. (Known in

Britain as the Large earth or Buff-tailed bumblebee.)

A temporary import licence was granted in 1994 for a project, funded by the Royal
Veterinary and Agriculture University, Denmark, the State Horticultural School in Iceland
and the Icelandic Student Innovation Fund, using colonies of B. terrestris from producers
in Belgium (Biobest N.V.) and the Netherlands (Koppert B.V.), for pollination of tomatoes.
Relicensing has continued because of improved fruit production demonstrated by that
study. Colonies are currently housed in glasshouses for the pollination of tomatoes,
strawberries, raspberries and peppers.
The situation was reviewed recently (Kristjánsson 2013). Around 800–900 colo-
nies are currently imported to Iceland annually, and about 70–80% are used in the
south of the country. Regulations drawn up for the initial study in 1994 were aimed
at preventing the escape of fertilised queens that could become naturalised and
introduce diseases. However, the required monitoring controls (to exclude parasites
and diseases in imported colonies, and on biosecurity in greenhouses) have not
been undertaken; the system currently relies too heavily on self-regulation. Given
the incidence of diseases in nests of B. terrestris imported to Britain (Graystock et al.
2013), there should be considerable scepticism that Iceland has avoided this
problem: it is highly likely that a variety of bumblebee diseases have been, and
continue to be, introduced unwittingly. As the escape of even a single fertilised
queen is probably sufficient to allow a viable naturalised population to develop, it
seems almost certain that B. terrestris will become part of the Iceland fauna very
soon, if it has not already done so. Along with queens, imported diseases are likely
to have spread beyond the confines of greenhouses. What effects they will have, or
are having, on the long-established B. jonellus population are uncertain, but they
are likely to be detrimental (see Otterstatter and Thomson 2008; Murray et al. 2013;
Schmid-Hempel et al. 2014). It seems unlikely that any set of regulations, however
stringently applied, will prevent the naturalisation of an organism that can become
established by the release of a single fertilised queen. The most sensible precau-
tion, for biosecurity purposes, would be to produce colonies solely from Icelandic
queens of currently established species (ironically, by now this may include B.
terrestris).
The official government license is for B. terrestris, and does not specify a subspecies.
Customs declarations by the producers mention B. terrestris (Koppert) and Bombus sp.
(Biobest). Both the producers and the import company tell us that the species used is B.
terrestris terrestris. Currently, there are no independent checks on either the species or
subspecies being used.
B. terrestris (subspecies terrestris) is very similar in appearance to B. lucorum.
Queens are on average somewhat larger than those of B. lucorum, although natural
variation makes this an unreliable character for identification. Examination of col-
lections in the Icelandic Institute of Natural History in 2015 revealed a number of
queens that are large for B. lucorum; closer examination of these, including barcod-
ing, is desirable.
16 O. E. PRŶS-JONES ET AL.

Discussion
Many of the restricted number of insect species that have colonised North Atlantic
islands have done so by association with man during the past 1200 years (Downes 1988;
Dugmore et al. 2005). It is reasonable to conclude that all of the bumblebee species now
found in Iceland have also arrived as phoretic travellers with man.
B. jonellus is currently found all along the Atlantic fringe of Europe and was probably
present here over the historic and prehistoric period during which colonisation of
Iceland occurred. It is likely to have been on Iceland in late medieval times on the
basis that Guđmundsson (c. 1640; also see Prŷs-Jones et al. 1981) describes the presence
of ‘hunangsflugur’ (honeyflies) – the traditional Icelandic name for a bumblebee. This
species has a short colony cycle and is thought to be able to produce a second colony
cycle in favourable years (Meidell 1968). Consequently, new queens – along with those
of most species of the subgenus Pyrobombus – seek hibernation/aestivation sites earlier
in the season than many other species. This would make B. jonellus a good candidate as
a ‘hitchhiker’ during the short season of favourable weather (May to August) during
which sailings to Iceland took place historically (Horváth et al. 2011). Genetic studies of
B. jonellus should establish, with more certainty, when and from where the original
colonisation event occurred; and allow us to assess the compatibility of the findings with
an anthropogenic origin in the historic or prehistoric past.
Anthropogenic introductions to Iceland continue at an accelerating rate, and parallel
events on other island groups (Table 3). Historically there were no records of bumble-
bees on the Faroe Islands, apart from a single individual of B. lapponicus found in 1887
(see Madsen and Jensen 2011), and none were found in 1988 (OEP-J, pers. obs.).
Recently, the island group gained two species – B. lucorum1 in 2007 and B. pratorum
in 2010 (Madsen and Jensen 2011). Jensen and Madsen (2013) mention the finding of a
large white-tailed bumblebee in a box of garden plants imported by ship from Scotland.
Likewise, B. terrestris was found on the Shetland Islands for the first time in 2012
(Macdonald and Harvey 2014) and on the Orkneys in 2014 (Prŷs-Jones and Williams
2015). B. pratorum and B. monticola reached Ireland in the latter part of the last century,
and B. hypnorum was recorded for the first time in Britain in 2001 (Goulson and Williams
2001). Goulson (2010) speculated that the subgenus Pyrobombus – to which these latter
three species belong – may be atypically dispersive, on the basis that genetic evidence
from the Hebridean islands and mainland Scottish populations showed that B. jonellus is
able to cross sea-barriers in excess of 30 km. Unassisted dispersal over such distances
may certainly occur; however, the fact that all of the species mentioned above reached
previously uncolonised islands over a relatively brief period makes unassisted dispersal
over water improbable: if they were able to so without assistance, why hadn’t they done
so previously? Untangling colonisation histories is a challenge, and it should always
include consideration of the possible involvement of man. The same arguments apply to
the bumblebee faunas of the Macronesian islands (Azores, Madeira and Canary Islands).
Ancient human-related colonisation of Madeira by bumblebees has also been suggested
recently by Lecocq et al. (2016).
Anthropogenic introductions of bumblebee species are likely to continue unless
positive efforts are made to limit them (see Reade et al. 2015). Apart from direct effects
of exploitative competition for food and habitat, introduced bumblebees bring the
Table 3. Recent colonisation events by Bombus species.
Location Species First recorded Established? Information source
Iceland B. hortorum 1959 ✓ Prŷs-Jones et al. (1981)
B. lucorum 1979 ✓ Prŷs-Jones et al. (1981)
B. hypnorum 2008 ✓ Ólafsson (2010); this paper
B. pascuorum 2010 ✓ Ólafsson (2010–2013); this paper
B. pratorum 2010 ? This paper
Mainland Britain B. hypnorum 2001 ✓ Goulson and Williams (2001)
Shetland Islands B. terrestris 2012 ✓ Macdonald and Harvey (2014)
Orkney Islands B. terrestris 2014 ✓ Prŷs-Jones and Williams (2015)
Fair Isle B. terrestris 2012 ?✗ Prŷs-Jones and Williams (2015)
B. ‘magnus’ 2014 ? Prŷs-Jones and Williams (2015)
Faroe Islands B. ‘lucorum’ 2007 ✓ Madsen and Jensen (2011); Jensen and Madsen (2013)
B. pratorum 2010 ✓ Madsen and Jensen (2011); Jensen and Madsen (2013)
Rakiura (Stewart Island) New Zealand B. hortorum 2014 ✓ Donovan (2015)
Isle of Man B. hypnorum 2015 ? BWARS record (2016 B. hypnorum distribution map)
Republic of Ireland B. hypnorum 2016 ? Bee Watch Ireland Facebook page (confirmed from photo)
Inverted commas indicate instances where barcoding is needed as a check on identity.
JOURNAL OF NATURAL HISTORY
17
18 O. E. PRŶS-JONES ET AL.

likelihood of disease (Colla et al. 2006; Graystock et al. 2013; Murray et al. 2013; Schmid-
Hempel et al. 2014; Brown et al. 2016). Iceland’s ecosystem has developed in unusual
isolation and much of its interest and uniqueness resides in this fact (Gillespie 2007).
Colonising species are likely to alter the pollination services received by native and
introduced plant species and lead to changes in Icelandic plant communities.
To limit the potential for introducing further bumblebee species, and their dis-
eases, it is proposed that government licencing requirements should ensure that the
necessary checks are undertaken to exclude parasites and diseases in imported
colonies, promote good biosecurity practices in greenhouses (Kristjánsson 2013),
and verify which species and subspecies are being imported. Parasite and disease
screening protocols should be adopted, such as those used by Brown et al. (2016). As
most if not all introduced bumblebee species in Iceland have probably arrived in
freight, it would be worth investigating measures aimed at reducing the risk of
accidental importation of queens hibernating in cargo (such as the compost of potted
plants).
Ideally, bumblebee colonies used for pollination in glasshouses should derive from
queens of Icelandic provenance. If checks reveal that B. terrestris has not yet colonised
Iceland, it might be prudent to prevent it happening in future by considering switching
to the use of an already naturalised species, such as B. lucorum.

Acknowledgements
We are most grateful to Dr Paul Williams, Natural History Museum, London, for confirming the
identity of a specimen as B. lucorum by barcoding, and to Dr Sally Corbet and Dr Robert Prŷs-Jones
for comments on the manuscript.

Disclosure statement
No potential conflict of interest was reported by the authors.

Geolocation information

Almannagjá Gorge 64.2750°N 21.1016°W

Akureyri 65.6856°N 18.1116°W
Eskifjörður 65.0709°N 14.0095°W
Garðabær 64.0742°N 21.9061°W
Heiðmörk 64.0660°N 21.7666°W
Hveragerði 63.9975°N 21.1942°W
Keflavík 63.9779°N 22.5852°W
Reykjavík 64.1283°N 21.8229°W
Seyðisfjörður 65.2589°N 14.0046°W

Note
1. As B. lucorum it is part of a sibling species complex, this identification must presumably be
considered provisional.
 JOURNAL OF NATURAL HISTORY 19

ORCID
Oliver E. Prŷs-Jones http://orcid.org/0000-0002-1045-0422
Kristján Kristjánsson http://orcid.org/0000-0002-1899-5937
Erling Ólafsson http://orcid.org/0000-0002-4729-0098

References
Benediktsson K. 2015. Floral hazards: nootka lupin in Iceland and the complex politics of invasive
life. Geografiska Annaler. Series B Human Geography. 97:139–154. doi:10.1111/geob.12070
Benton T. 2006. Bumblebees. The natural history and identification of the species found in Britain.
The New Naturalist Library. London: Collins.
Bertsch A, Schweer H, Titze A. 2004. Discrimination of the bumblebee species Bombus lucorum, B.
cryptarum and B. magnus by morphological characters and male labial gland secretions.
Beiträge zur Entomologie. 54:365–386.
Bjarnason H. 1946. Alaskaför haustið 1945 [A trip to Alaska autumn 1945]. Ársrit Skógræktarfélags
Íslands [Yearbook of the Icelandic Forestry Association]. 13:5–48.
Bjarnason H. 1981. Lúpínan frá Alaska [Lupin from Alaska]. Lesbók Morgunblaðsins, 33 tbl. 3.
október: 6–7.
Boff S, Soro A, Paxton RJ, Alves-dos-Santos I. 2014. Island isolation reduces genetic diversity and
connectivity but does not significantly elevate diploid male production in a neotropical orchid
bee. Conserv Genet. 15:1123–1135.
Brown MJF, Sainsbury AW, Vaughan-Higgins RJ, Measures GH, Jones CM, Gammans N. 2016.
Bringing back a healthy buzz? Invertebrate parasites and reintroductions - a case study in
bumblebees. EcoHealth. doi:10.1007/s10393-015-1093-5
Buckland PC, Dugmore AJ, Sadler JP. 1998. Paleoecological evidence for human impact on the
north Atlantic islands. Proceedings of the 2nd Symposium, Fauna and Flora of the Atlantic
Islands. Boletim do Museu Municipal do Funchal (História Natural), Suppl. 5:89–108.
Buckland PC, Sadler JP, Smith RF. 1996. Contrasting patterns of polar biogeography: north and
south in Atlantic island biota. Proceedings of the 1st Symposium, Fauna and Flora of the
Atlantic Islands. Boletim do Museu Municipal do Funchal (História Natural). Suppl. 4:145–174.
Burgett DM, Sukumalanand P. 2000. Flight activity of Xylocopa (Nyctomelitta) tranquebarica: a
night flying carpenter bee (Hymenoptera: Apidae). J Apicultural Res. 39:75–83.
Carolan JC, Murray TE, Ú F, Crossley J, Schmidt H, Cederberg B, McNally L, Paxton RJ, Williams PH,
Brown MJF. 2012. Colour patterns do not diagnose species: quantitative evaluation of a DNA
barcoded cryptic bumblebee complex. PLoS One. 7:e29251.
Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, Marshall
McCabe A. 2009. The Last Glacial Maximum. Science. 325:710–714.
Colla SR, Otterstatter MC, Gegear RJ, Thomson JD. 2006. Plight of the bumble bee: pathogen
spillover from commercial to wild populations. Biol Conserv. 129:461–467.
Corbet SA, Saville NM, Fussell M, Prŷs-Jones OE, Unwin DM. 1995. The competition box: a graphical
aid to forecasting pollinator performance. J Appl Ecol. 32:707–719.
Darvill B, Ellis JS, Lye GC, Goulson D. 2006. Population structure and inbreeding in a rare and
declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol Ecol. 15:601–611.
Darvill B, O’Connor S, Lye GC, Waters J, Lepais O, Goulson D. 2010. Cryptic differences in dispersal
lead to differential sensitivity to habitat fragmentation in two bumblebee species. Mol Ecol.
19:53–63.
Donovan BJ. 2015. Occurrence of Bombus hortorum (L.) (Hymenoptera, Apoidea) on Rakiura
(Stewart Island). Weta. 49:8–11.
Downes JA. 1988. The post-glacial colonization of the north Atlantic islands. Memoirs Entomol Soc
Can. 120:55–92.
20 O. E. PRŶS-JONES ET AL.

Dugmore AJ, Church MJ, Buckland PC, Edwards KJ, Lawson IT, McGovern TH, Panagiotakopulu E,
Simpson IA, Skidmore P, Sveinbjarnardóttir G. 2005. The Norse landnám on the North Atlantic
islands: an environmental impact assessment. Polar Record. 41:21–37.
Enckell PH, Rundgren S. 1988. Anthropochorous earthworms (Lumbricidae) as indicators of aban-
doned settlements in the Faroe Islands. J Archaeol Sci. 15:439–451.
Eysteinsson T. 2009. Forestry in a treeless land 2009. Iceland Forest Service, Miðvangi 2-4, IS-700,
Egilsstaðir, Iceland.
Fussell M, Corbet SA. 1992. The nesting places of some British bumble bees. J Apicultural Res.
31:32–41.
Gargan LM, Cornette R, Yearsley JM, Montgomery WI, Paupério J, Alves PC, Butler F, Pascal M,
Tresset A, Herrel A, et al. 2016. Molecular and morphological insights into the origin of the
invasive greater white-toothed shrew (Crocidura russula) in Ireland. Biol Invasions. 18:857–871.
Gillespie RG. 2007. Oceanic Islands: models of diversity. In: Levin SA, editor. Encyclopedia of
biodiversity. Oxford: Elsevier; p. 1–13.
Goulson D. 2010. Bumblebees. Behaviour, ecology, and conservation. Oxford Biology. Oxford:
Oxford University Press. 317 p.
Goulson D, Kaden JC, Lepais O, Lye GC, Darvill B. 2011. Population structure, dispersal and
colonization history of the garden bumblebee Bombus hortorum in the Western Isles of
Scotland. Conserv Genet. 12:867–879.
Goulson D, Williams PH. 2001. Bombus hypnorum (Hymenoptera: Apidae), a new British bumble-
bee? Br J Entomol Nat Hist. 14:129–131.
Graystock P, Yates K, Evison SEF, Darvill B, Goulson D, Hughes WHO. 2013. The Trojan hives:
pollinator pathogens, imported and distributed in bumblebee colonies. J Appl Ecol. 50:1207–
1215.
Guđmundsson J. c1640. From ‘Jon Gudmundsson and his Natural History of Iceland’. Hermannsson
H. 1924. Islandica (An annual relating to Iceland and the Fiske Icelandic Collection in Cornell
University Library) 15 (p. 21 ‘hunangsflugur’). Ithaca (NY): Cornell University Library.
Haeseler V. 1974. Aculeate Hymenopteren über Nord- und Ostsee nach Untersuchungen auf
Feuerschiffen [An investigation of the aculeate Hymenoptera from lightships on the North
and Baltic seas]. Entomologica Scandinavica. 5:123–136.
Hiltbrunner E, Aerts R, Bühlmann T, Huss-Danell K, Magnusson B, Myrold DD, Reed SC, Sigurdsson
BD, Körner C. 2014. Ecological consequences of the expansion of N2-fixing plants in cold
biomes. Oecologia. 176:11–24.
Horváth G, Barta A, Pomozi I, Suhai B, Hegedüs R, Åkesson S, Meyer-Rochow B, Wehner R. 2011. On
the trail of Vikings with polarized skylight: experimental study of the atmospheric optical
prerequisites allowing polarimetric navigation by Viking seafarers. Phil Trans R Soc B.
366:772–782.
Hubbard A, Sugden D, Dugmore A, Norddahl H, Pétursson HG. 2006. A modelling insight into the
Icelandic last glacial maximum ice sheet. Quarternary Sci Rev. 25:2283–2296.
Hulme PE. 2009. Trade, transport and trouble: managing invasive species pathways in an era of
globalization. J Appl Ecol. 46:10–18.
Ings TC, N L I, Chittka L, Rasmont P. 2010. A failed invasion? Commercially introduced pollinators in
Southern France. Apidologie. 41:1–13.
Ingólfsson A. 2009. A marine refugium in Iceland during the last glacial maximum: fact or fiction?
Zoologica Scripta. 38:663–665.
Jensen J-K, Madsen HB. 2013. To arter af humlebier yngler på Færøerne (Hymenoptera, Apidae).
[Two species of Bumblebees breed on the Faroe Islands (Hymenoptera, Apidae)]. Entomologiske
Meddelelser. 81:1–14.
Kristjánsson K. 1983. Liffræði Hunangsflugna á Íslandi [The biology of Icelandic bumblebees (Hym.,
Apidae)] [BSc Honours thesis]. Reykjavik: Department of Biology, University of Iceland. 67 p.
Kristjánsson K. 1992. Honingbier og vilde bier i Island [Honey bees and wild bees in Iceland].
Tidsskrift for Biavl. 1:10–16.
Kristjánsson K. 2013. Álitsgerđ um innflutning á hunangsflugum (Bombus spp.) til Íslands [Opinion
on the importation of bumblebees (Bombus spp.) to Iceland]. A report prepared at the request
 JOURNAL OF NATURAL HISTORY 21

of the Icelandic Ministry of Industry and Innovation, dated 23 Dec 2013 Available from: https://
www.researchgate.net/publication/298411113_Import_of_bumblebees_Bombus_spp_to_
Iceland_for_pollination_in_greenhauses
Kristjánsson K, Lárusdóttir G. 1994. Frævun tómatplantna (Lycopersicon esculentum Mill.) í
íslenskum gróðurhúsum með hunangsflugum (Bombus sp.) [Pollination of tomato plants
(Lycopersicon esculentum Mill.) in Icelandic greenhouses using bumblebees (Bombus sp.)].
Research report. 20 p. Icelandic. Available from: https://www.researchgate.net/publication/
308624479_Pollination_of_tomato_plants_Lycopersicon_esculentum_Mill_in_Icelandic_green
houses_using_bumblebees_Bombus_sp__In_Icelandic
Lárusdóttir G. 1995. Notkun hunangsflugna (Bombus sp.) við frævun tomatplantna (Lycopersicon
esculentum) í gróðurhúsum á Íslandi [Use of bumblebees (Bombus sp.) to pollinate tomato
plants (Lycopersicon esculentum) in greenhouses in Iceland.] [B.Sc. thesis]. Reykjavik: Department
of Biology, University of Iceland. 70 p.
Lecocq T, Coppée A, Michez D, Brasero N, Rasplus J-Y, Valterova I, Rasmont P. 2016. The alien’s
identity: consequences of taxonomic status for the international bumblebee trade regulations.
Biol Conserv. 195:169–176.
Lees AC, Gilroy JJ. 2009. Vagrancy mechanisms in passerines and near-passerines. In: Slack R,
editor. Rare birds, where and when: an analysis of status and distribution in Britain and Ireland.
Vol. 1. Sandgrouse to New World Orioles. York: Rare Bird Books.
Lepais O, Darvill B, O’Connor S, Osborne JL, Sanderson RA, Cussans J, Goffe L, Goulson D. 2010.
Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol
Ecol. 19:819–831.
Macdonald MA, Harvey PV. 2014. Buff-tailed bumblebee Bombus terrestris in Shetland. BWARS
Newsletter Autumn issue. p. 20–22.
Macfarlane RP, Gurr L. 1995. Distribution of bumble bees in New Zealand. New Zeal Entomol.
18:29–36.
Madsen HB, Jensen J-K. 2011. Humlebier på Færøerne (Hymenoptera, Apidae) [Bumblebees on the
Faroes Islands (Hymenoptera, Apidae)]. Entomologiske Meddelelser. 79:19–26.
Magnússon B. 2001. Vegetation succession in areas colonized by the introduced Nootka Lupin
(Lupinus nootkatensis) in Iceland. In: Biological diversity in Iceland. National Report to the
Convention on Biological Diversity, Ministry for the Environment and Icelandic Institute of
Natural History. Available from: https://www.cbd.int/doc/world/is/is-nr-01-en.pdf
Magnússon B. 2010. NOBANIS – invasive alien species fact sheet – Lupinus nootkatensis. – from:
online database of the European network on invasive alien species – NOBANIS. Available from:
https://www.nobanis.org/fact-sheets/
Magnússon B, Magnússon SH, Sigurđsson BD. 2003. Áhrif alaskalúpínu á gróðurfar [Effects of
Alaska lupin on vegetation]. Náttúrufræðingurinn. 71:98–111.
Matthiasson S. 1934. Býflugnarækt á Islandi.[Beekeeping in Iceland]. Náttúrufræðingurinn. 4:93–96.
Meidell O. 1968. Bombus jonellus (Kirby) (Hym., Apidae) has two generations in a season. Norsk
entomologisk Tidsskrift. 14:31–32.
Mikkola K. 1978. Spring migrations of wasps and bumble bees on the southern coast of Finland
(Hymenoptera, Vespidae and Apidae). Annales Entomologici Fennici. 44:10–26.
Mikkola K. 1984. Migration of wasp and bumble bee queens across the Gulf of Finland
(Hymenoptera; Vespidae and Apidae). Notulae Entomologicae. 64:125–128.
Murray TE, Coffey MF, Kehoe E, Horgan FG. 2013. Pathogen prevalence in commercially reared
bumble bees and evidence of spillover in conspecific populations. Biol Conserv. 159:269–276.
Murray TE, Fitzpatrick U, Brown MJF, Paxton RJ. 2008. Cryptic species diversity in a widespread
bumble bee complex revealed using mitochondrial DNA RFLPs. Conserv Genet. 9:653–666.
Ólafsson E. 1979. Um geitunga (Hymenoptera, Vespidae) og skyldar gaddvespur á Íslandi [About
wasps (Hymenoptera, Vespidae) and related insects in Iceland.]. Náttúrufræđingurinn, Reykjavik.
49:27–40.
Ólafsson E. 2010. Rauðhumla - athyglisverður nýr landnemi 19.5.2010 [The Red bumblebee -
interesting new settlers]. News from the Icelandic Institute of Natural History. Available from:
http://www.ni.is/frettir/nr/1246
22 O. E. PRŶS-JONES ET AL.

Ólafsson E. 2010–2013. Rauðhumla - Bombus hypnorum (Linnaeus, 1758). Available from: http://
www.ni.is/poddur/gardur/poddur/nr/1244
Otterstatter MC, Thomson JD. 2008. Does pathogen spillover from commercially reared bumble
bees threaten wild pollinators? PloS One. 3:e2771.
Pekkarinen A, Teras I. 1993. Zoogeography of Bombus and Psithyrus in northwestern Europe
(Hymenoptera, Apidae). Annales Zoologici Fennici. 30:187–208.
Petersen A, Thorstensen S. 1991. Hunangsflugnabú í hreiðrum spörfugla [Bumblebee Bombus
jonellus (Kirby) colonies in passerine nests.]. Bliki. 10:1–10.
Prŷs-Jones OE. 1982. Ecological studies of foraging and life history in bumblebees [PhD disserta-
tion]. Department of Applied Biology, University of Cambridge.
Prŷs-Jones OE, Corbet SA. 2011. Bumblebees. Naturalists’ Handbooks No. 6. 3rd ed. Exeter: Pelagic
Publishing.
Prŷs-Jones OE, Ólafsson E, Kristjánsson K. 1981. The Icelandic bumble bee fauna and its distribu-
tional ecology. J Apicultural Res. 20:189–197.
Prŷs-Jones OE, Williams PH. 2015. New bumblebee records for Orkney and Fair Isle. BWARS
Newsletter Spring issue. p. 14–16. Available from: https://www.researchgate.net/publication/
280092849_New_bumblebee_records_for_Orkney_and_Fair_Isle
Reade C, Thorp R, Goka K, Wasbauer M, McKenna M. 2015. Invisible compromises: global business,
local ecosystems, and the commercial bumble bee trade. Organ Environ. 28:436–457.
Reber T, Vähäkainu A, Baird E, Weckström M, Warrant E, Dacke M. 2015. Effect of light intensity on
flight control and temporal properties of photoreceptors in bumblebees. J Exp Biol. 218:1339–
1346.
Sadler J. 1991. Beetles, boats and biogeography. Insect invaders of the North Atlantic. Acta
Archaeologica. 61:199–211.
Schmid-Hempel R, Eckhardt M, Goulson D, Heinzmann D, Lange C, Plischuk S, Escudero LR, Salathé
R, Scriven JJ, Schmid-Hempel P. 2014. The invasion of southern South America by imported
bumblebees and associated parasites. J Anim Ecol. 83:823–837.
Scriven JJ, Whitehorn PR, Goulson D, Tinsley MC. 2016. Niche partitioning in a sympatric cryptic
species complex. Ecol Evol. 6:1328–1339.
Smith KP. 1995. Landnám: the settlement of Iceland in archeological and historical perspective.
World Archeol. 26:3 ‘Colonization of Islands’ 319–347.
Somanathan H, Borges RM, Warrant EJ, Kelber A. 2008. Visual ecology of Indian carpenter bees I:
light intensities and flight activity. J Comp Physiol. 194:97–107.
Streeter R, Dugmore AJ, Lawson IT, Erlendsson E, Edwards KJ. 2015. The onset of the palaeoan-
thropocene in Iceland: changes in complex natural systems. Holocene. 25:1662–1675.
Sveinsdóttir B 1981. Bú hunangsflugna í Heiðmörk 1981 [Bumblebee nests in Heidmork 1981] [BSc
thesis]. Reykjavik: Department of Biology, University of Iceland. 46 p.
Vésteinsson O, McGovern TH. 2012. The peopling of Iceland. Norwegian Archaeol Review. 45:206–218.
von Hagen E, Aichhorn A. 2003. Hummeln. Nottuln: Fauna Verlag.
Warrant E. 2008. Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. J Exp
Biol. 211:1737–1746.
Williams PH, Brown MJF, Carolan JC, An J-D, Goulson D, Aytekin AM, Best LR, Byvaltsev AM,
Cederberg B, Dawson R, et al. 2012. Unveiling cryptic species of the bumblebee subgenus
Bombus s. str. world-wide with COI barcodes (Hymenoptera: Apidae). Syst Biodivers. 10:21–56.
Williams PH, Byvaltsev AM, Cederberg B, Berezin MV, Ødegaard F, Rasmussen C, Richardson LL,
Huang J, Sheffield CS, Williams ST. 2015. Genes suggest ancestral colour polymorphisms are
shared across morphologically cryptic species in Arctic bumblebees. PLoS One. 10:e0144544.