Ann. soc. entomol. Fr. (n.s.), 2012, 48 (3–4) : 275-280
e Bumblebees Scarcity Syndrome: Are heat waves leading to
local extinctions of bumblebees (Hymenoptera: Apidae: Bombus)?
Abstract. It is now well known that many bumblebee species are threatened in Europe and in N.
America. Various hypotheses have b een propo sed to explain this regression. Some of the hypothetical
factors act at a continental level, as the general restructuration of the agriculture toward the use of
synthetic nitrogen fertilisation, in place of leguminous crops. The landscape fragmentation is typically
a local factor the fusion of which also leads to large-scale effects. Since 2002, we observed a great
number of situations where local droughts and heat waves occurred in France, UK, Scandinavia,
Turkey, leading to very strong local reductions of the bumblebee’s fauna. We observed so many local
cases in 2007-2009 that we could hypothesise that a merger of these local effects could lead to a
new general threat. As they are the most exposed to heat waves, the species with a late (summer)
phenology should be the most sensitive to this risk.
Résumé. Le Syndrome de Rareté Anormale des Bourdons : les canicules conduisent-elles à
des extinctions locales des bourdons (Hymenoptera : Apidae : Bombus) ? Il est maintenant
bien connu que beaucoup d’espèces de bourdons sont menacées en Europe et en Amérique du
Nord. Diverses hypothèses ont été proposées pour expliquer ces régressions. Certains facteurs
hypothétiques agissent à l’échelle continentale, par exemple la restructuration générale de l’agriculture.
La fragmentation du paysage est typiquement un facteur local dont la fusion spatiale a des effets sur
de vastes territoires. Depuis 2002, nous avons observé un parallélisme entre des sècheresses locales
ou des canicules et une très forte dépression de la faune de bourdons. Nous avons observé tellement
de cas locaux de 2007 à 2009 (en France, au Royaume-Uni, en Scandinavie et en Turquie) que nous
émettons l’hypothèse qu’une conﬂ uence de ces effets locaux pourrait mener à une nouvelle menace à
l’échelle continentale. Parce qu’elles sont les plus exposées aux canicules, les espèces estivales sont
celles qui pourraient être les plus sensibles à ce risque.
Keywords: Global warming, climate, pollinators, drought, regression.
P R & S I
Laboratoire de Zoologie, Université de Mons (UMons), Place du Parc 23, B-7000 Mons, Belgium
E-mail: email@example.com, firstname.lastname@example.org
Accepté le 3 novembre 2012
It is now well known that many bumblebees species
are threatened in Europe and in N. America (see e.g.
Biesmeijer et al. 2006; Kosior et al. 2007; Williams et
al. 2009; Cameron et al. 2011). Various hypotheses
have been proposed to explain this regression. Some
of the hypothetical factors act at a continental level,
as the general restructuration of the agriculture thanks
to the use of synthetic nitrogen fertilisation in place
of leguminous crops. e landscape fragmentation is
typically a local factor where the spatial merger could
aﬀ ect wide areas. More obscure is the role that climatic
events could play in the fate of the bumblebee’s species.
Recently, we observed an abnormally low number of
bumblebees in several situations. We will discuss here
the potential role played by heat waves to explain these
For the World Meteorological Organisation a heat
wave occurs when during more than ﬁ ve consecutive
days the daily maximum temperature exceeds the
average maximum temperature by 5 °C (Robinson
e IPPC (2007) observed a “quite slow” global
warming (0.74 °C for the passed century). is increase
of the temperature is only a mean and does not take
into account events occurring at local or regional
scales. As an example, from the year 2000 to 2010,
the meteorological station of Le Luc (France, Var)
recorded a mean temperature increase of +0.9 °C, and
a mean decrease of 32% of the yearly precipitations.
However, the generalised use of means to ﬁ gure the
climatic variations blurs the impact of the extreme
meteorological events of short duration like storms,
drought, and heat waves. Is it possible that such events
that are not accounted for by global statistics act on the
fate of the bumblebee’s faunas?
Since 2002, we observed many situations that
we never met before (1979–2001) during our ﬁ eld
trips and samplings. Until the ﬁ rst decade of the 21st
P. R & S. I
century, in most places, it was very common to collect
scores or even hundreds of bumblebees in a day. Since
2002, we sampled several times in regions or places
where the vegetation was obviously overheated. In such
places, we recorded bumblebee densities that were very
abnormally low. In some places where we had observed
or collected lots of bumblebees some years before, after
heat waves, we observed no or very sparse individuals.
In N. Finland in July 2003, we observed an
absolute record of 33 °C at the meteorological station
of Utsjoki. In Ankara (Turkey), we recorded extreme
high temperature and drought in July 2007 (38 °C as
maximum at 959 m elevation). In East-Pyrenees, the
meteo-station of Ste-Léocadie (1320 m) recorded the
record temperatures of 33 °C in August 2001 and 2007.
In these regions, we had made abundant sampling some
years before (see e.g. Iserbyt et al. 2008; Rasmont et al.
2009). After these heat waves, we observed no or very
scarce bumblebees. We could roughly evaluate that the
apparent bumblebee’s density decreased from one to
two orders of magnitude.We repeated such experience
(ﬁ g. 1) in East-Turkey (2002, 2011), in the Pyrenees
(2003, 2006, 2007, 2008, 2012), in Middle Norway
(2008), in Central Sweden (2008), and in Scotland
(2009) (ﬁ g. 2). e most extreme cases were in the
Pyrenees (ﬁ g. 2E), in Arctic Finland in 2003 (ﬁ g. 2D),
and in Central Anatolia in 2007 (ﬁ g. 2A).
We propose to name these situations the Bumblebee
Scarcity Syndrome (BSS). is syndrome became
so common during the last years that it considerably
disturbs (or prevents) many ﬁ eld bumblebee
e correlation between the number of several
bumblebee species and climatic parameters in a
mountain biome is presented by Iserbyt & Rasmont
(2012). It shows that most of the studied species are
sensitive to variations of climatic monthly means. To
take into account extreme meteorological events is the
Map of the collecting trips of the authors where they experience the Bumblebees Scarcity Syndrom following a heat wave.
e Bumblebee Scarcity Syndrome
more diﬃ cult, that very frequently, these events barely
modify the climatic means.
e heat wave could aﬀ ect the bumblebee’s fauna
in various ways:
1. e bumblebees could be killed by the heat
when the temperature rises above a lethal threshold.
e upper fatal limit of temperature is generally very
high in most insects (Uvarov, 1931: 17) and it is
Landscapes with overheated vegetation, with the BSS. A, Dried and overheated Astragalus - steppe in Yozgat (Turkey) in 2007; B, Dried and overheated
Sphagnum bog in Flatanger (Norway) in 2008; C, Overheated heath in Brora (Scotland) in 2009; D, Overheated lesser toundra vegetation in Utsjoki, (N-
Finland) in 2003; E, Dried and overheated alpine vegetation with dying Juniperus sibirica Lodd. ex Burgsd. (=J. nana Willd.) in Osséja (France, Pyrénées-
Orientales) in 2012.
P. R & S. I
very unlikely that it could be overtaken, even in the
strongest heat waves. However, the bumblebees are
now known to be endothermic animals (Heinrich
1979, 1993). Several mechanisms of thermoregulation
(e.g. active nest ventilation) may cause a considerable
energy cost (Heinrich 1979, 1993). Most bumblebees
being cold climate animals, their preferendum (sensu
Uvarov, 1931: 54), or “tolerance zone” (sensu Hallman
& Denlinger 1998), spreads over low temperature
intervals. When they undergo temperatures higher
than their preferendum, their energy need for
thermoregulation could pass over their foraging intake.
For Uvarov (1931: 56), “the preferendum is probably
one of the most potent factors inﬂ uencing the ecological
distribution of insects and their movements”.
2. It is very important to notice that not only
the extreme temperatures during the heat wave are
of importance but also its total duration. Following
Hallman & Denlinger (1998), “the insect is capable of
surviving a series of non-lethal lesions, but at certain
point, the lesions accumulate to a critical level and
cause death.” Denlinger & Yocum (1998) show that
“survival curves which plot survival against duration
of high temperature exposure characteristically have a
broad shoulder (little mortality initially), followed by a
high rate of death”. at means that heat waves could
kill with sublethal temperatures (without trespassing
any lethal threshold), if such high but sublethal
temperature persists during a long time. is eﬀ ect is
well known for human (see e.g. Argaud et al. 2007;
3. e heat wave could also kill by water loss, as
heat waves are very generally associated with drought.
4. It could kill by starvation if overheating or
drought aﬀ ects the availability of foraged vegetation.
5. Winter heat waves could also die in waking up
the hibernating queens when no ﬂ ower resources are
available. Without to wake up the queens, winter heat
waves could also increase the soil humidity, resulting in
higher mortality from diseases (fungi, viruses).
When the bumblebees are in the solitary phase of
their life cycle, they could be aﬀ ected by any of these
causes. When the bumblebees are living in colonies,
they beneﬁ t from the underground or at least protected
nest and its relative homeostasis. At this time, they
probably suﬀ er mainly from the low energy intake that
could be caused by lowered plant productivity. Taking
these hypotheses into consideration, the young sexuals
are at higher risk during their solitary phase.
As the heat waves mainly occur during the months
of July and August, the species that are able to complete
their life cycle and to enter diapause before July could
be saved (e.g. B. hypnorum (L.), B. lucorum (L.), B.
pratorum (L.) or B. terrestris (L.)). e species with a
late phenology could be much more aﬀ ected by heat
waves, while they mainly increase their colonies in July
and their sexual behaviour takes place during August. As
examples of very late species, we could give B. confusus
Schenck, B. cullumanus (Kirby), B. distinguendus
Morawitz, B. humilis (Illiger), B. magnus Vogt (ﬁ g.
3A), B. muscorum (L.) (ﬁ g. 3B), B. subterraneus (L.), B.
sylvarum (L.), B. veteranus (Fabricius), (for phenology,
see e.g. Løken 1973; Peeters et al. 1999). As most of
these late species are strongly regressing everywhere in
Europe (see e.g. Kosior et al. 2007; Rasmont & Iserbyt
2010–2012), we could hypothesise that the heat waves
play a role in this regression and that the late species
are the species most sensitive to the Bumblebee Scarcity
Some species with late phenology, likely the most sensible to the BSS. A, Bombus magnus Vogt; B, Bombus muscorum (L.) ssp. liepetterseni Løken.
e Bumblebee Scarcity Syndrome
Edwards & Williams (2004) and Williams et
al. (2009) hypothesise that the food shortage is a
main cause of bumblebee depletion. However, these
authors also pointed out that the bumblebees that
experience the worst regression across Great Britain,
China and Canada are 1) species with narrow climatic
specialisation, 2) species along their climatic edges and
3) species with queens that begin their activity late in
the year. On the contrary, following these authors,
the species that remain the most successful “tend to
be those bumblebee species with broad climatic ranges
that occur away from the edges of their climatic ranges
and that become active early in the season.”
Our opinion is that the heat waves play an obvious
role in the local and temporary extinction of bumble-
bees. We hypothesise that the geographical coalescence
and the repetition year after year of the Bumblebee
Scarcity Syndrome caused by increasingly frequent
heat waves could be a major factor in the regression
of bumblebee species. is factor could strongly aﬀ ect
other insects as already reported long ago by Chaine
(1912, 1919, reported by Uvarov 1931). It also con-
cerns other animals, e.g. McKechnie & Wolf (2010)
found that heat waves induce catastrophic avian mor-
tality while Welbergen et al. (2008) found the same
about ﬂ ying foxes.
As the frequency of the heat waves is expected to
increase dramatically during the 21st century (Meehl
& Tebaldi 2004; Ganguly et al. 2009), a large number
of bumblebee species could be endangered. It urgently
needs to understand how the bumblebees are able to
withstand to high temperatures. eir physiological
limits need to be clearly determined by experimental
Acknowledgements. We thank the Fonds pour la Recherche
Fondamentale et Collective (FRFC) (subvention VARIGEP),
the Fonds National de la Recherche Scientiﬁ que (FNRS) (short
travel grants), the European Commission CORDIS who funded
the researches in the Kevo subarctic research station-LAPBIAT.
We thank the Dr. B. Cederberg (ArtDatabanken, SLU, Uppsala),
the Dr. S. Neuvonen (Kevo LAPBIAT, Turku, Finland) and
the Prof. A.M. Aytekin (University of Hacettepe, Ankara) who
helped us a lot during ﬁ eld trips. We thans two anonymous
referees. We also thank the Mairie d’Eyne (Pyrénées-Orientales)
(A. Bousquet, R. Staats) who supported our collecting trips in
the Pyrenees. is paper is a contribution to the European
Community’s Seventh Framework Programme (FP7/2007-
2013) under grant agreement no 244090, STEP Project (Status
and Trends of European Pollinators, www.step-project.net).
Argaud L., Ferry T., Le Q.-H., Marﬁ si A., Ciorba D., Achache P.,
Ducluzeau R., Robert D. 2007. Short- and Long-term Outcomes of
Heatstroke Following the 2003 Heat Wave in Lyon, France. Archives of
Internal Medicine 167: 2177-2183.
Biesmeijer J. C., Roberts S. P. M., Reemer M., Ohlemüller R., Edwards
M., Peeters T., Schaﬀ ers A. P., Potts S. G., Kleukers R., omas
C. D., Settele J., Kunin W. E. 2006. Parallel Declines in Pollinators
and Insect-Pollinated Plants in Britain and the Netherlands. Science
Cameron S. A., Lozier J. D., Strange J. P., Koch J. B., Cordes N., Solter
L. F., Griswold T. L. 2011. Patterns of widespread decline in North
American bumble bees. PNAS 108(2): 662-667.
Chaine J. 1912. Inﬂ uence des fortes chaleurs sur certains insectes parasites
des végétaux. Comptes-rendus de l‘Académie des Sciences, Paris 154:
Chaine J. 1919. Destruction du puceron du rosier par les grandes chaleurs
de l‘été. Bull. Soc. Etudes vulg. zool. agric. 18: 23-25.
Denlinger D. L., Yocum G. D. 1998. Physiology of Heat Sensitivity, p.
7-54 in: Hallman G. J., Denlinger D. L. 1998 (eds.) Temperature
Sensitivity in Insects and Application in Integrated Pest Management.
Westview Press, Boulder, Colorado, 311 p.
Edwards M., Williams P. H. 2004. Where have all the bumblebees gone,
and could they ever return? British Wildlife June 2004: 305-312.
Ganguly A. R., Steinhaeuser K., Erickson III D. J., Branstetter M.,
Parish E. S., Singh N., Drake J. B., Buja L. 2009. Higher trends
but larger uncertainty and geographic variability in 21st century
temperature and heat waves. PNAS 106: 15555-15559.
Hallman J., Denlinger D. L. 1998. Introduction: Temperature Sensitivity
and Integrated Pest Management, p. 1-6 in: Hallman G. J., Denlinger
D. L. 1998 (eds.) Temperature Sensitivity in Insects and Application in
Integrated Pest Management. Westview Press, Boulder, Colorado, 311 p.
Heinrich B. 1979. Bumblebee economics. Harvard University Press,
Cambridge, 246 p, 2 pls.
Heinrich B. 1993. e Hot-Blooded Insects. Harvard University Press,
INED 2008. e August 2003 hotwave in France. Institut National
d’Etudes Démographique, http://www.ined.fr/en/everything_about_
2003_france/ (accessed 1.IX.2010).
IPPC 2007. Assessment Report: Climate Change 2007. http://www.ipcc.ch/
pdf/assessment-report/ar4/syr/ar4_syr.pdf (accessed 2.IX.2010).
Iserbyt S., Durieux E.-A., Rasmont P. 2008. e remarkable diversity
of bumblebees (Hymenoptera: Apidae: Bombus) in the Eyne Valley
(France, Pyrénées-Orientales). Annales de la Société entomologique de
France (n.s.) 44(2) : 211-241.
Iserbyt S., Rasmont P. 2012. e eﬀ ect of climatic variation on abun-
dance and diversity of bumblebees: a ten years survey in a mountain
hot spot. Annales de la Société entomologique de France (N.S.) 48(3-4):
Kosior A., Celary W., Olejniczak P., Fijał J., Król W., Solarz W.,
Płonka P. 2007. e decline of the bumble bees and cuckoo bees
(Hymenoptera: Apidae: Bombini) of Western and Central Europe.
Oryx 41(11): 79-88.
Løken A. 1973. Studies on Scandinavian Bumble Bees (Hymenoptera,
Apidae). Norsk entomologisk Tidsskrift 20(1): 1-218.
McKechnie A. E., Wolf B. O. 2010. Climate change increases the
likelihood of catastrophic avian mortality events during extreme heat
waves. Biology Letters 6: 253-256
Meehl G. A., Tebaldi C 2004. More Intense, More Frequent, and Longer
Lasting Heat Waves in the 21st Century. Science 305(5686): 994-997.
Peeters T. M. J., Raemakers I. P., Smit J. 1999. Voorlopige atlas van de
Nederlandse bijen (Apidae). European Invertebrate Survey Nederland,
Leiden, 230 p.
P. R & S. I
Rasmont P., Aytekin A. M., Kaftanoğlu O., Flagothier D. 2009.
e bumblebees of Turkey. Atlas Hymenoptera, Mons, Gembloux.
Rasmont P., Iserbyt S. 2010–2012. Atlas of the European Bees: genus
Bombus. STEP Project, Atlas Hymenoptera, Mons, Gembloux.
Robinson P. J. 2001. On the Deﬁ nition of a Heat Wave. Journal of Applied
Meteorology 40: 762-775.
Uvarov B. P. 1931. Insects and climate. Transactions of the Entomological
Society of London 79: 1-232.
Welbergen J. A, Klose S. M., Markus N., Eby P. 2008. Climate change
and the eﬀ ects of temperature extremes on Australian ﬂ ying-foxes.
Proceedings of the Royal Society, B. Biological Sciences 275: 419-425.
Williams P., Colla S., Xie Z. 2009. Bumblebee Vulnerability: Common
Correlates of Winners and Losers across ree Continents. Conservation
Biology 23(4): 931-940.