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The Bumblebees Scarcity Syndrome: Are heat waves leading to local extinctions of bumblebees (Hymenoptera: Apidae: Bombus)?

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The Bumblebees Scarcity Syndrome: Are heat waves leading to local extinctions of bumblebees (Hymenoptera: Apidae: Bombus)?

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It is now well known that many bumblebee species are threatened in Europe and in N. America. 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 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.
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Ann. soc. entomol. Fr. (n.s.), 2012, 48 (3–4) : 275-280
275
ARTICLE
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: pierre.rasmont@umons.ac.be, stephanie.iserbyt@umons.ac.be
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
situations.
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
2001).
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?
Observations
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
276
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
experimentations.
Discussion
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
Figure 1
Map of the collecting trips of the authors where they experience the Bumblebees Scarcity Syndrom following a heat wave.
e Bumblebee Scarcity Syndrome
277
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
Figure 2
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.
278
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;
INED 2008).
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
Syndrome.
Figure 3
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
279
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
studies.
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).
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Climate warming has been identified as one of the primary factors causing worldwide pollinator declines. One of the most at-risk groups of pollinators is bumble bees (Bombus spp.). Bumble bees are common, widespread, and key pollinators of a wide range of crops and wild plants. Although studies have examined the thermal physiological traits of individual bumble bees to understand how they may be impacted by climate warming, little to no studies have examined how climate warming may impact whole bumble bee colonies both in their ability to thermoregulate their nest for their brood or in their ability to forage for food. Here, we set out to investigate how climate warming will impact bumble bee colonies by affecting these behaviors. To do this, we first measured temperature in simulated nests both above- and belowground as well as air temperature from March to November of 2021 to understand what temperatures bumble bees experience in different environments. To understand how warming may impact nest thermoregulation and foraging, we examined the rates of these behaviors in response to ambient temperature. Our results show that climate warming will give bees more time to forage and require bees nesting both above- and belowground to heat their nests less, but bees nesting aboveground may have to cool their nests at possibly unsustainable levels. It appears that the direct impact of climate warming on bumble bees is overall beneficial, thus climate warming may be driving bumble bee declines through indirect impacts such as host plant phenological mismatches.
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The IUCN Red List of Threatened Species
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Centuries of landscape changes associated with agriculture have dramatically reduced the amount and increased the temporal variability of the floral resources that support key pollinating insects such as bumble bees. Adapting to these novel resource conditions is important to ensure the persistence of bumble bee species. While several species appear to be in decline in modern agricultural landscapes, others have thrived, suggesting adaptation to exploit highly variable floral resources. Bombus impatiens, the common eastern bumble bee, is a prime example of such a species. We designed an experiment to compare how free‐foraging colonies of B. impatiens performed adjacent to areas with either temporally continuous or variable (pulsed) patches of purple tansy (Phacelia tanacetifolia) plantings. We found that colonies in Phacelia landscapes grew faster, had gained more mass, and produced more gynes than did colonies in reference landscapes with no Phacelia. Comparing colony responses between pulsed and continuous flowering resources showed that total mass gain at the end of the experiment was greater with continuous flowering resources. In contrast, colony growth rate and total gyne production were comparable for colonies adjacent to Phacelia plantings that were continuous versus pulsed. While low in statistical replication, given the scale of the experimental manipulation, our experiment shows that although B. impatiens colonies can exploit periods of resource discontinuity and gain mass, these continuously available floral resources appear important for colony growth and benefit gyne production. Landscape supplementation of floral resources reveals that continuously available floral resources provide a greater benefit to bumble bee colony performance (colony mass, gyne production, foraging activity) relative to discontinuous resource availability.
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Declines of many bumble bee species have raised concerns because of their importance as pollinators and potential harbingers of declines among other insect taxa. At present, bumble bee conservation is predominantly focused on midsummer flower restoration in open habitats. However, a growing body of evidence suggests that forests may play an important role in bumble bee life history. Compared with open habitats, forests and woody edges provide food resources during phenologically distinct periods, are often preferred nesting and overwintering habitats, and can offer favorable abiotic conditions in a changing climate. Future research efforts are needed in order to anticipate how ongoing changes in forests, such as overbrowsing by deer, plant invasions, and shifting canopy demographics, affect the suitability of these habitats for bumble bees. Forested habitats are increasingly appreciated in the life cycles of many bumble bees, and they deserve greater attention from those who wish to understand bumble bee populations and aid in their conservation.
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Even if climates play an evident role in the bumblebees distribution, at the present time, no research has been performed to test whether climatic parameters actually affect their abundance and diversity. For more than one decade (1999–2009), we monitored the bumblebee fauna of a mountain hotspot in the Eastern Pyrenees. We sampled each year, in July, the same hayfield habitat, resulting in the sampling of 28 species. We computed the correlation of the yearly abundance of the main species with several climatic parameters concerning temperature and precipitation. We separated the parameters measured during the bumblebee solitary phase and those measured during their social phase. Bumblebee fauna composition varied significantly over years. In the 13 species considered, the abundance of 9 was correlated with at least one climatic parameter. The lowest abundance of bumblebees was correlated with hot and dry conditions during the month of August the year before sampling (the nuptial time of the founders). The highest overall abundance of bumblebees was observed during the social phase in the rainy months. Across years, climatic parameters seem to have strongly affected the composition of bumblebee fauna. Our results seem to indicate that hot and dry weather represent serious threat for most bumblebee species. The potential effects of Global Warming are discussed: they may cause a severe reduction of the mountain bumblebee diversity.
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Generating credible climate change and extremes projections remains a high-priority challenge, especially since recent observed emissions are above the worst-case scenario. Bias and uncertainty analyses of ensemble simulations from a global earth systems model show increased warming and more intense heat waves combined with greater uncertainty and large regional variability in the 21st century. Global warming trends are statistically validated across ensembles and investigated at regional scales. Observed heat wave intensities in the current decade are larger than worst-case projections. Model projections are relatively insensitive to initial conditions, while uncertainty bounds obtained by comparison with recent observations are wider than ensemble ranges. Increased trends in temperature and heat waves, concurrent with larger uncertainty and variability, suggest greater urgency and complexity of adaptation or mitigation decisions.
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Despite its small area (20.18 km²), the Eyne Valley, (France, E. Pyrenees) is known to be a place of great faunistic and fl oristic diversity. The authors have studied the bumblebee fauna of the valley for six years, gathering more than 5000 detailed observations. They observed 33 species, of the 46 living in continental France. For each species, the distribution and ecological preferences (altitude, vegetation type, CORINE biotopes, fl oral choices) were recorded. Floral resources may be the most important ecological factor. The altitude, the abundance, the diversity of food plants, and the heterogeneity of habitats seem to explain the survival and the coexistence of this great number of species of bumblebees with various ecological affi nities.
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The bumble and cuckooo bees (Hymenoptera: Apidae: Bombini; Bombus spp. and Psithyrus spp., respectively) are important plant pollinators and any decline in numbers or species constitutes a significant threat both to biological diversity and to whole economies. The distribution, status and factors threatening all 60 known taxa (species and subspecies) of Bombini of 11 countries of Western and Central Europe (Belgium, the Netherlands, Luxembourg, Denmark, Germany, Switzerland, Austria, Czech Republic, Slovakia, Hungary, Poland) were assessed from the beginning of the 20th century. The analysis was based on a literature review, unpublished data, personal communications, our own observations, and an expert review. The IUCN Red List categories were used for assessing the threat of extinction. Eighty per cent of taxa were threatened in at least one country of the region, and 30% of taxa were threatened throughout their range in the countries considered. More species went extinct per country in the second than in the first half of the 20th century, and four taxa went extinct in all 11 countries during 1951–2000. Amongst the factors adversely affecting the Bombini anthropogenic factors (particularly those associated with large-scale farming schemes) appear to be of greater importance than natural factors. To halt population declines and species extinctions it will be necessary to preserve aspects of traditional farming practices and for all Bombini to be afforded legal protection in all countries of the region. The implementation of the European Union's Common Agricultural Policy is likely to have the greatest single impact upon pollinators in the near future.
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Heat waves are a major cause of weather-related deaths. With the current concern for global warming it is reasonable to suppose that they may increase in frequency, severity, duration, or areal extent in the future. However, in the absence of an adequate definition of a heat wave, it is impossible to assess either changes in the past or possible consequences for the future. A set of definitions is proposed here, based on the criteria for Heat stress forecasts developed by the National Weather Service (NWS). Watches or warnings are issued when taresholds of daytime high and nighttime low heat index (H 1) values are exceeded for at least two consecutive days. The heat index is a combination of ambient temperature and humidity that approximates the environmental aspect of the thermal regime of a human body, with the NWS thresholds representing a generalized estimate of the onset of physiological stress. These thresholds cannot be applied directly nationwide. In hot and humid regions, physical, social, and cultural adaptations will require that the thresholds be set higher to ensure that only those events perceived as stressful are identified. In other, cooler, areas the NWS criteria may never be reached even though unusually hot events may be perceived as heat waves. Thus, it is likely that a similar number of perceived heat events will occur in all regions, with the thresholds varying regionally. Hourly H 1 for 178 stations in the coterminous United States was analyzed for the 1951-90 period to determine appropriate threshold criteria. Use of the NWS criteria alone indicated that much of the nation had less than three heat waves per decade, and this value was adopted as the baseline against which to establish suitable thresholds. For all areas, a percentile thresholds approach was tested. Using all available data, daytime high and nighttime low thresholds were established separately for each specific percentile. Heat waves were treated as occuring when conditions exceeded both the daytime high and the nighttime low thresholds of the same percentile for two consecutive days. Several thresholds were tested. For much of the South, 1% thresholds produced appropriate values. Consequently, a heat wave was defined as a period of at least 48 h during which neither the overnight low nor the daytime high H 1 falls below the NWS heat stress thresholds (80° and 105°F, respectively), except at stations for which more than 1% of both the annual high and low H 1 observations exceed these thresholds, in which case the 1% values are used as the heat wave thresholds. As an extension, "hot spells" were similarly defined, but for events falling between the 1% values and NWS thresholds, with "warm spells" occuring between the 2% and 1% values. Again, stations for which the 1% or 2% H 1 values exceed the NWS thresholds were given modified definitions. The preliminary investigation of the timing and location of heat waves resulting from these definitions indicated that they correctly identified major epidemiological events. A tentative climatic comparison also suggests that heat waves are becoming less frequent in the southern and more frequent in the midwestern and eastern parts of the nation.
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Temperature is one of the principal factors delimitating survival and reproduction of insects and mites. Temperature extremes are a cause of significant natural mortality in populations and offer a rich potential that can be exploited for the development of environmentally safe pest management strategies. The omnipresence of temperature stress has resulted in a wealth of physiological and behavioral adaptations that have evolved to ameliorate or avoid the full brunt of high or low environmental temperatures. These range from behaviors as simple as moving in or out of sunlight to increase or decrease body temperature to the more complex social behaviors of honey bees, Apis mellifera, which cluster to preserve warmth during severe cold and use evaporative cooling aided by wing movement to cool the hive during hot weather. Physiologically insects prepare for cold weather in temperate climates by such means as increasing concentrations of cryoprotectants in the hemolymph and arresting development at a certain cold tolerant stage. A series of proteins produced in response to extreme temperatures and other stresses increases tolerance of the organism to further stress. Some ants are able to initiate heat shock protein synthesis in the absence of thermal stress and use that ability to prepare for brief forays into the desert during the hottest part of the day to scavenge for organisms that have succumbed to the heat (Gehring & Wehner 1995). Coleman et al. (1995) discuss the need for integrating molecular function, metabolic cost, and ecological manifestation and variation to better understand the evolutionary significance of heat shock proteins and their