300- meter distance with less precision than those of their sisters reared at
the two higher temperatures. Subsequent work looked for temperature-
induced effects on the worker bees’ brains, and found that the connections
between neurons in the mushroom bodies—the centers of information
integration in worker bees’ brains—were highest in bees that matured at
the normal brood- nest temperature (34.5°C) and were significantly lower
in bees raised at temperatures just 1°C (less than 2°F) above or below
normal.
The temperature of any living system reflects the relative rates at which
it gains heat and it loses heat, so to understand how a honey bee colony
maintains a stable, and elevated, temperature in its brood nest, we must
examine how it adjusts both its production of heat through metabolism and
its loss of heat through various means, including nest ventilation and evapo-
rative cooling. These processes are the same for managed colonies living in
hives and wild colonies living in trees, but how hard the bees need to work
to heat and cool their nests often differs greatly for the two types of colo-
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Temperature Control 217
Temperature
conversions
32˚
32˚ C = 90˚ F
16˚
24˚ C = 75˚ F
16˚ C = 61˚ F
24˚
7˚
7˚ C = 45˚ F
–12˚ C = 10˚ F
–18˚ C = 0˚ F
–12˚
–18˚
Entrance
10 cm
Fig. 9.1. Isotherms of a winter cluster of honey bees living in Madison, Wis-
consin. Data were collected at 1700 hours on 25 February 1951, from a colony
housed in a Langstroth- type, movable- frame hive that consisted of three
medium- depth hive bodies. The 7°C (45°F) isotherm marks the outer surface
of the bees’ cluster. Note the pocket of relatively warm air in the upper half of
the hive. It is this microenvironment around the cluster that is its direct ther-
mal environment.
nies. As we shall see, colony thermoregulation—in both summer and win-
ter—is generally easier for wild colonies because the thick wooden walls
of their tree- cavity homes provide better insulation than do the thin lum-
ber walls of most hives, and because cracks in the walls of the wild colo-
nies’ homes are filled with propolis, which makes them less drafty. These
differences in insulation and draftiness are important because they strongly
influence the microenvironment inside a colony’s nest cavity, and it is the
temperature inside the nest cavity, not the temperature outside it, that is
the direct thermal environment of a bee colony (Fig. 9.1). Increasing the
insulation and decreasing the draftiness of a nest enclosure slows the heat
flow between the microenvironment of the nest and the macroenviron-
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218 Chapter 9
ment of the world outside. This means that on a day when the air is cold,
a wild colony living inside a well- insulated and well- sealed tree cavity
needs to produce relatively little heat to keep its brood nest warmed to
the ca. 35°C (95°F) set point, because the microenvironment around it is
so well isolated from the cold macroenvironment outside. It also means
that on an extremely hot day, when heat will tend to flow into a colony’s
nest cavity, a wild colony living in a thick- walled tree hollow may need to
do relatively little cooling to prevent its brood nest from overheating,
because the microenvironment inside the nest cavity is so well isolated
from the high temperatures outside.
EVOLUTIONARY ORIGINS OF COLONY
THERMOREGULATION
The ability of a honey colony to maintain a warm microclimate inside its
nest is ultimately derived from the adaptions of honey bees for flight. Being
insects, honey bees fly by flapping their wings—the most energetically
demanding mode of animal locomotion—and the flight muscles of insects
are among the most metabolically active of tissues. A worker bee in flight
expends energy at a rate of about 500 watts/kilogram (230 watts/pound).
In comparison, the maximum power output of an Olympic rower is only
about 20 watts/kilogram (9 watts/pound). Therefore, whenever a bee is
airborne, she not only consumes the energy in her fuel at a prodigious rate,
she also generates a great deal of heat. The efficiency of a bee’s flight ap-
paratus in converting metabolic fuel to mechanical power is about 10–20
percent, so more than 80 percent of the energy expended in flight appears
as heat in the muscles. The rate of heat loss from a worker bee’s hairy tho-
rax is sufficiently low that during sustained flight her thorax temperature
is typically 10°–15°C (18°–27°F) above the ambient temperature.
We see, therefore, that in honey bees an elevated thorax temperature is
an inevitable consequence of flight, but what is critical for understanding
the origins of the colony thermoregulation abilities of honey bees is the
fact that an elevated thorax temperature has become essential for their
flight. Workers must maintain a thorax temperature above about 27°C
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Temperature Control 219
(81°F) to be able to fly. Flight muscles cooler than this simply cannot gen-
erate the high wingbeat frequency and power output per stroke needed
for takeoff and flight. This high minimum thorax temperature for flight
reflects two “design” constraints on the bees’ flight- muscle enzymes: 1)
they must withstand the high thoracic temperature produced by flight, but
2) when built with sufficiently strong intramolecular bonds to resist deg-
radation at high temperatures, they are too rigid to operate efficiently at
low temperatures. So, when honey bees evolved flight muscles adapted to
high temperatures, they also evolved the ability to conduct preflight warm-
ups of these muscles, without which they would remain grounded at tem-
peratures below 27°C (81°F). Bees warm up their flight muscles by simul-
taneously activating the wing- levator and the wing- depressor muscles in
the thorax. This causes these muscles to contract isometrically, which pro-
duces much heat but few or no wing vibrations.
This preflight warm- up behavior evidently set the stage for the evolu-
tion of nest thermoregulation by honey bees, since they use the same
mechanism of isometric muscle contractions for warming their flight
muscles and for heating their brood combs. Recordings of the thorax tem-
peratures of foragers preparing to leave on foraging flights and of nurse
bees heating cells of capped brood show identical patterns of a 2°–3°C
(4°–5°F) per minute rise in thorax temperature. And in both settings the
wings of a bee warming herself remain motionless, folded over her abdo-
men. Sometimes the bees that are heating brood stand perfectly still while
pressing their thoraces onto the caps of cells containing pupae, but other
times they enter empty cells amidst cel
ls of sealed brood and then remain
in them for up to 30 minutes with their thoraces heated to 41°C (106°F),
to warm the pupae in the adjacent cells (Fig. 9.2).
The colony- level thermoregulation abilities of Apis mellifera evolved in
tandem with the evolution of this bee’s social life. In part, honey bee colo-
nies gained their sophisticated control of nest temperature when they
evolved into large groups, simply because a group has a greater capacity
for heat production than an individual. After all, a colony of 15,000 bees
can generate heat some 15,000 times more powerfully than can a single
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220 Chapter 9
C
37.9
37.3
B
36.6
F
36.1
D
35.5
34.8
A
34.3
E
33.7
33.0
Fig. 9.2. Thermogram taken with an infrared camera of worker bees on a comb
containing capped brood cells and empty cells. Capped cells appear gray with
no outline; empty cells are recognized by the hexagonal shape of their rims.
A: worker with hot (ca. 38°C/100°F) thorax that is about to enter an empty cell
adjacent to three sealed brood cells. B: worker that has just left the warm (ca.
37°C/98°F) open cell in the center of the image. C and D: workers not producing
heat; each has a cool thorax. E and F: cells containing workers producing heat; in each, the cell interior glows around the dark silhouette of the cool abdomen of
the heater bee within the cell.
bee. A second advantage in thermoregulation enjoyed by groups relative
to individuals is reduced heat loss per individual, especially when the
group’s members crowd together into a tight cluster. The surface area of
an isolated worker honey bee—a cylinder 14 millimeters (0.55 inch) long
and 4 millimeters (0.16 inch) in diameter—is about 3.8 square centime-
ters (0.6 square inches), but the surface area of 15,000 bees, when con-
tracted into a dense cluster 18 centimeters (7 inches) in diameter, is only
about 1,000 square centimeters (155 square inches). So, when a bee is
huddling in a cluster, her effective surface area is reduced to only 0.067
square centimeters (0.01 square inches), some 60 times smaller than when
she is standing alone.
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Temperature Control 221
BENEFITS OF TEMPERATURE CONTROL
Honey bee colonies benefit greatly from being able to both cool and heat
themselves. With thousands of bees crowded together inside a nest cavity
that has only one rather small entrance opening, a strong colony faces a
risk of disastrous overheating when the temperature outside the nest cav-
ity rises above about 30°C (86°F) and stays there all day. Sustained tem-
peratures over 37°C (99°F) inside a nest will disrupt larval metamorpho-
sis. Also, if the temperature inside a nest rises above 40°C (104°F), then
the beeswax combs can soften dangerously, and those laden with honey
can collapse. Moreover, the adult bees can survive only a few hours at
temperatures of 45°–50°C (113°–122°F), which is just 10°–15°C (18°–
27°F) above their optimum temperature for full activity (35°C/95°F). In
contrast, honey bees can survive indefinitely at 15°C (59°F). This shows
that worker bees, like most organisms, possess a narrower range of heat
tolerance above their optimum than below it. The low tolerance of high
temperatures by honey bees reflects the fact that they have not evolved
enzymes more stable than are normally necessary. This makes sense,
because an enzyme that would be stable at temperatures far above this
bee’s normal range would be too rigid to function efficiently at its usual
temperatures.
The adaptive significance of avoiding nest overheating is obvious, but
what selective forces favored the evolution of nest warming? The main ben-
efit during the warm months is probably acceleration of brood develop-
ment. Speedy brood development enables rapid colony growth, which is
valuable whenever a colony’s population has dropped sharply, such as at the
end of winter, after swarming, and following heavy mortality from preda-
tion. Significant deceleration of brood development occurs when brood is
cooled just slightly. Vern G. Milum found, for example, that brood located
on the perimeter of a colony’s brood nest, where the temperature averaged
about 31.5°C (89°F), required 22–24 days between egg laying and adult
emergence, whereas brood in the nest center, where it was about 3°C
(4.5°F) warmer, required only 20–22 days to complete development.
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222 Chapter 9
In addition to fostering rapid colony growth, the elevated temperature
of a colony’s brood nest helps it cope with disease. Work done by Anna
Maurizio, in the 1930s, showed that chalkbrood, a disease of honey bee
larvae caused by the fungus Ascosphaera apis, is blocked if a colony keeps its
larvae warm (at 35°C/95°F), but that letting the larvae cool to 30°C
(86°F) for just a few hours is all that is needed for a successful infection of
these larvae by this fungus. Recently, Phil Starks and colleagues have shown
that honey bee colonies have a brood- comb fever response when exposed
to chalkbrood spores. Specifically, colonies that were fed a 50 percent
sugar solution containing ground sporulating chalkbrood mummies—
dead larvae covered with the fruiting bodies of the fungus—raised their
brood- comb temperatures by nearly 0.6°C (1.0°F) (Fig. 9.3). Given that
the normal range of the brood- comb temperature is just 2°C, from 34°C
to 36°C (93°F to 97°F), a 0.6°C increase is a sizable elevation, and it ap-
pears to have been effective in preventing infection. None of the colonies
that were fed the spores acquired the disease. Honey bee colonies also
suffer from at least 15 viral and two bacterial diseases, but the effects of
high brood- comb temperature on a colony’s vulnerability to viral and bac-
terial infections remain unknown. Studies with other insect viruses have
found that they do not cause infections when their hosts are reared at
temperatures like those found in the brood nest of a honey bee colony, so
the elevated temperatures found in honey bee colonies may provide resis-
tance to viral diseases, too.
Of course, another important benefit of the honey bee colony’s ability
to create a warm microclimate within its nest is greater resistance to cold
temperatures out in the general environment. Through its advanced tech-
niques of social thermoregulation, Apis mellifera has greatly expanded its
thermal niche, living today in geographic locations where colonies would
otherwise perish over winter. As was discussed in chapter 6, the honey bee
is basically a tropical insect that has expanded its range into cold- temperate
regions through various adaptations, especially its ability to maintain a
warm cluster throughout long, freezing winters.
See
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Temperature Control 223
0.3
0.2
0.1
ference (˚C)
–0.1
mperature dif –0.2
Te
–0.3
Post-
Prefeed
Feed
Treatment
treatment
Fig. 9.3. Differences between observed and expected temperatures in the center
of the brood comb in three small colonies living in two- frame observation hives,
on days when they were fed sugar syrup that was pure (Feed interval) or con-
tained chalkbrood ( Ascosphaera apis) spores (Treatment interval), and on days
before (Prefeed) and after (Post- treatment) the feeding. Brood- comb tempera-
tures decreased during the Feed period, because some bees left the brood comb
to collect the sugar syrup. Despite the cooling effect of feeding, the colonies had
relatively high brood- comb temperatures when the sugar syrup was inoculated
with chalkbrood spores.
WARMING THE COLONY
The primary problem in thermoregulation that is faced by a honey bee
colony living in a place with long, cold winters is that of staying warmer
than the surrounding environment. As mentioned already, the internal
temperature that a colony strives to maintain varies depending on whether
it is or is not rearing brood. If it is, then the brood- nest region is kept at
34°–36°C (93°–97°F). If it is not rearing brood, then it turns down its
thermostat and maintains its core temperature above about 18°C (64°F)
and its mantle temperatures above about 8°C (46°F). These two tempera-
tures are critical lower limits. Bees chilled below about 18°C (64°F) can-
not generate the neuronal activity that is needed to activate their flight
muscles to produce more heat, and bees cooled below about 8°C (46°F)
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224 Chapter 9
become immobilized and enter a sort of chill coma. Whether a bee sur-
vives such hypothermia depends on its duration; chilling to 10°C (50°F)
or colder kills most bees within 48 hours.
A colony maintains a suitably warm microclimate inside the part of its
nest that it occupies—the combs that it covers—by controlling the rates
of heat production within and heat loss from this region. Figure 9.4 de-
picts the ways that a colony in a winter cluster loses heat to the environ-
The Lives of Bees Page 27