AMER. ZOOL., 32:225-237 (1992)
Biophysical Ecology and Heat Exchange in Insects1
TIMOTHY M. CASEY
Department of Entomology, Cook College, Rutgers University,
New Brunswick, New Jersey 08903
SYNOPSIS. When used with observations of behavior and physiology of animals in known
microclimates, a biophysical approach is a powerful tool for predicting body temperatures
of insects. For ectothermic insects, solution of the energy budget equation and use of operative temperature models have been used to determine the range of temperatures which an
insect can exhibit in a given environment. Knowledge of body temperature has allowed
predictions of when important behaviors are possible in the field, thereby directly relating
biophysical models to fitness parameters of animals. A proper understanding of the physiological mechanism(s) controlling heat exchange is prerequisite to application and interpretation of information obtained using biophysical techniques. For endothermic insects,
physiological regulation of heat exchange forces a more complicated analysis. Evaluation of
thoracic heat exchange alone (aside from indicating whether insects are regulating Tlh) is of
little utility for either quantifying total heat exchange, or evaluating thermoregulatory mechanisms without further information. Further studies of biophysics and physiology of endothermic insects during flight are needed to correct these deficiencies. Application of biophysical techniques has allowed predictions of behavior offlyinginsects based on principles
of heat exchange which cannot be examined directly. Analyses of endothermy of resting
honeybee swarms and hives indicate that these "superorganisms" regulate temperature rather
precisely over a remarkable range of environmental temperature using mechanisms equivalent to those used by resting endothermic vertebrates.
Hegel, 1981; Kingsolver and Moffat, 1982;
Polcyn and Chappell, 1986). For endothermic insects during flight, quantifying the
total heat exchange provides an independent estimate of the metabolic rate of the
insect (Weis-Fogh, 1968). Finally, quantifying heat exchange can allow an accurate
prediction of the insect's body temperature
in the natural environment (Chappell, 1982;
Kingsolver, 1983a). Since many activities
are strongly temperature dependent, such
predictions are useful in explaining observed
activity patterns and evaluating adaptive
strategies.
Heat exchange of insects has often been
analysed using a biophysical approach
(Parry, 1951; Digby, 1955; Church, 1960).
However, most early studies were laboratory based, aimed primarily at examining
mechanisms of heat exchange per se. In more
recent insect studies (Chappell, 1983; Kingsolver, 1983a; Joos et ai, 1988) investigators have applied biophysical techniques
(Porter and Gates, 1969; Bakken and Gates,
1975; Bakken, 1976a, b) to insects in the
field and have broadened the scope of the
questions and produced predictive models.
1
From the Workshop on Biophysical Ecology: Methods, Microclimates, and Models presented at the Annual In this paper I will describe a series of studMeeting of the American Society of Zoologists, 27-30 ies which utilize a biophysical approach to
December 1989, at Boston, Massachusetts.
examine thermal balance of insects. This
225
INTRODUCTION
Body temperature exerts a major influence on the biochemical reaction rates of
organisms, which in turn affects important
performance capabilities such as feeding,
digestion, growth, locomotion and reproduction (Hochachka and Somero, 1984). As
a consequence of their small size, insects
exhibit rapid rates of heat exchange with
their environment and they are able to utilize microclimates not available to larger
animals.
Quantifying heat exchange is valuable
from a variety of perspectives. From a physiological viewpoint, heat budgets are useful
for evaluating the relative importance of a
particular mechanism of heat transfer such
as evaporation (Cooper et ai, 1985), or the
relative amount of heat exchange occurring
in a particular part of the body, in order to
determine its importance as a site of regulation (Hegel and Casey, 1982). Heat budgets also allow a quantitative evaluation of
the effectiveness of various postures for
behavioral thermoregulation (Casey and
226
TIMOTHY M. CASEY
particular group of studies is chosen because
these insects vary dramatically in body temperature, physiology and avenues of heat
exchange. Where possible I will attempt to
describe the significance of these studies to
our understanding of insect thermal ecology.
REGULATION OF BODY TEMPERATURE
Control of body temperature requires that
the rates of heat gain from metabolism and
external sources be balanced by the rates of
heat loss to the environment. In general,
radiation and convection represent the
major avenues of heat exchange, except in
insects which are conspicuously endothermic (Parry, 1951; Digby, 1955). Evaporative cooling is not normally employed to
control body temperature although there are
notable exceptions (see Seymour, 1974;
Heinrich, 1980a, b). Several factors, including size, shape, surface area, coloration, and
degree and length of pubescence will affect
the capacity to absorb solar radiation. Convective heat exchange will vary with size,
shape, orientation and surface properties of
the insect. At high wind velocities heat
exchange by forced convection varies with
the square root of the velocity (Digby, 1955;
Chappell, 1982). At low wind velocity (030 cm/sec) free convection effects predominate and convective heat transfer is almost
independent of velocity (Digby, 1955;
Church, I960).
It is often difficult to quantify avenues of
heat exchange because (a) the characterization of the environment is too simple, (b)
the actual thermal properties of the animal
are only approximately known, (c) the
dynamics of" heat transfer within the body
are not known, or (d) the heat exchange
model employed is too simple. Any or all
of these factors may confound analysis of
heat exchange.
Physiologists have examined heat
exchange using Newton's Law of cooling
which indicates that the rate of temperature
change is proportional to a cooling constant
multiplied by the temperature differential
between the body and the environment.
Multiplying the cooling constant by the specific heat of tissue yields the overall heat
transfer coefficient (C) and the rate of heat
loss (dH/dt) is
dH/dt = C(Tb - TJ
A large body of data from cooling curve
studies is available from insects from several taxa (May, 1976; Bartholomew, 1981).
In general, rates of passive cooling and minimal levels of heat transfer coefficient are
strongly, inversely related to body mass and
are generally similar for insects of a given
mass regardless of taxon. However, some
adult insects are heavily insulated (Church,
1960; Heinrich, 1971a) which significantly
reduces their thoracic heat transfer coefficient.
The Newtonian model is an oversimplification because neither the heat transfer
coefficient nor the temperature difference is
well defined in the natural environment
(Tracy, 1972). Heat transfer coefficients will
vary with the characteristics of the environment (such as wind velocity which affects
convective heat transfer). The operative
temperature is also determined by both the
animal and the environment (Bakken and
Gates, 1975; Bakken, 1976a). However,
since radiative, convective and conductive
heat exchange are all approximately linearly
related to a temperature differential (Bakken and Gates, 1975), utilization of this
model under certain circumstances might
be justified (Bakken, 19766).
The environmental temperature surrounding an insect is complex and often difficult to evaluate because of the different
temperature gradients (radiant temperature, air temperature, substrate temperature, etc.). Moreover, temperature and wind
velocity are difficult to measure accurately
in the field because they vary considerably
with distance from the substrate (Fig. 1).
The actual temperature and wind conditions are dependent on the characteristics
of the substrate (size, shape, surface texture)
and may be modified by the insect itself.
For strictly terrestrial insects it is likely that
they are exposed to a range of temperature
and wind conditions as a result of their residence in the environmental boundary layer.
These factors have often limited a quantitative evaluation of heat exchange and often
227
HEAT EXCHANGE OF INSECTS
= • forced
convection
\
/free convection
conduction
FIG. 1. Schematic diagram for avenues of heat exchange of an ectothermic insect on the ground and an
endothermic insect during flight.
investigators studying insect thermoregulation have reported body temperature as a
function of shade air temperature (see
reviews by Heinrich, 1974; Kammer, 1981;
Willmer, 1982; May, 1983; Casey, 1988).
Although these data can demonstrate
whether or not thermoregulation occurs,
they give little insight into the actual heat
exchange processes involved without further information.
Recent studies have utilized operative
temperature models (Bakken, 1976a) to
characterize the range of thermal conditions
available to animals (Anderson etai, 1979;
Chappell, 1982, 1983). The models (usually
dried or freeze-dried insects) match the surface characteristics of the insects including
surface area, texture and coloration. However, to date, the actual surface characteristics of these models have not been rigorously examined. Since the models produce
no heat, their equilibrium temperature will
be determined entirely by the environment,
thus providing a realistic estimate of the
actual environmental conditions faced by
the animal. Differences in temperature
between a live active animal and a dead
model are the result of physiological or
behavioral control of heat exchange. Using
models ("Te thermometers"), it is possible
to map the entire range of thermal conditions available to the insect in a given habitat. The Te approach is powerful because it
integrates the effects of radiation and convection and it reduces the calculations and
assumptions involved in predicting the
thermal environment (Bakken, 1976a).
ECTOTHERMIC INSECTS
Individual caterpillars are relatively simple to deal with with respect to heat exchange
because they exhibit no significant capacity
for physiological heat transfer, and they
appear to be strictly ectothermic. They also
tend to have a uniform body temperature,
although this has not been systematically
examined. Due to their small size and the
resulting high surface to volume ratio, their
operative temperatures (Te) are usually
within a few degrees of ambient temperature (Sherman and Watt, 1973; Casey,
1976a; Kevan et ai, 1982; Stevenson,
1985a, b; Fields and McNeil, 1988).
Variation in morphology affects the oper-
228
TIMOTHY M. CASEY
ative temperatures of caterpillars. The distribution of the setae on many caterpillars
is such that they increase the effective cross
sectional area of the caterpillar without
retarding rates of radiant heat uptake. The
setae provide selective insulation and reduce
convective heat exchange without affecting
radiative heat gain, resulting in about a two
degree C increase in body temperature compared with caterpillars of equal size without
setae. This effect can be abolished by orientation and postural adjustment (Casey and
Hegel, 1981). While this is a modest increase
in Tb, it reduces the duration of larval development by several days which is undoubtedly beneficial in reducing mortality to
predators and parasitoids. It is significant
that gypsy moths are not diurnally active at
low population densities and tend to avoid
solar radiation (Knapp and Casey, 1986), so
that setae appear to have no ecological significance for thermal balance. However, at
high population densities gypsy moth caterpillars are conspicuously diurnal and routinely bask. Increased Tb causes increased
rates of food intake (Casey, 1976a) as well
as increased digestion rates (Casey et ai,
1988). Under outbreak conditions intraspecific competition is probably of greater significance than predation. Qualitatively similar patterns of setae enhancing body
temperatures have been reported for other
caterpillars (Kevan et ai, 1982; Fields and
McNeil, 1988).
The Eastern tent caterpillar Malacosoma
americanum is unusual compared to most
caterpillars because individuals are highly
gregarious, and during larval development
they spin a tent which provides protection
from predators and parasitoids during inactive periods (Fitzgerald, 1980). Both the
aggregation behavior and the tent itself are
crucial to larval development. Emerging
from their egg cases in early April, they are
among the earliest of spring caterpillars
(Snodgrass, 1924). While such early emergence is advantageous because many predators and parasitoids will not be in abundance until later in the season, the mean air
temperature during April is close to the
developmental threshold for growth (Knapp
and Casey, 1986). Malacosoma regulates Tb
better than any other larval insect thus far
measured (Casey, 1988). Despite their small
size, even second instar larvae, weighing only
tens of milligrams, are capable of maintaining body temperature in excess of 20°C
above air temperature (Knapp and Casey,
1986). By mid May the increased size of the
caterpillars, warmer air temperatures and
thermal properties of the tent put them in
serious danger of overheating.
In conjunction with a series of studies on
the ecology of tent caterpillars, Joos et al.
(1988) undertook a biophysical analysis of
their heat exchange. Our purpose was to
evaluate the thermal significance of posture,
behavior, and the tent under field conditions. In this study we used operative temperature (Te) models of the tent caterpillar,
consisting of freeze dried specimens with
thermocouples implanted in the body cavity. We made 'clumps' of individual caterpillars to evaluate the role of aggregation on
body temperature. To quantify the thermal
distribution throughout the tent, we forced
a colony of caterpillars to build their tent
on a wooden frame with thermocouples
placed on each of the six arms at precise
intervals. Placing the entire apparatus out
into thefieldin Central New Jersey, we positioned operative temperature models at
various locations on the tent and on a small
branch as a control. We also measured solar
radiation and wind velocity during the
experiments. We then brought the tent and
models into the laboratory and allowed them
to equilibrate under a range of radiant and
convective conditions typical for May at this
latitude.
The results indicate that, as a consequence of their behavior and the architecture of the tent, caterpillars have a wide
range of operative temperatures at various
locations on the tent (Fig. 2A). A Te model
placed on a branch in full sunshine nearby
the tent achieved a temperature only a few
°C above air temperature while a similar
model placed on the tent surface in full sunshine can be as much as 30°C above air
temperature (Fig. 2A). Clumping together
further increases body temperatures. Compared with individual models, clumps of 5
caterpillars exhibited Tes 6-7°C greater. The
elevated temperatures are due to several
factors. The tent provides a large boundary
229
HEAT EXCHANGE OF INSECTS
layer which should reduce convective heat
loss. Aggregation further decreases the surface to volume ratio and convective heat
exchange, while still allowing radiant heat
uptake. The tent warms several degrees
above air temperature, further enhancing the
Tb of the caterpillars. In addition to allowing
the caterpillars to heat up far above the levels they could achieve without the tent, the
tent provides a range of temperatures which
the caterpillars can utilize by microhabitat
selection. During the middle of the day the
body temperature of caterpillars can differ
by as much as 20°C, depending on their
location on or in the tent (Fig. 2A). This
highly heterogeneous environment allows
the caterpillars to regulate their T b quite precisely (Fig. 2C). It is interesting to note that
the caterpillars feed at routine intervals,
unaffected by the microclimate. Their synchronized behavior insures that a large tent
is constructed due to communal spinning of
silk. Although they routinely feed before
dawn when environmental temperatures are
lowest, behavioral thermoregulation maximizes digestion thereby strongly affecting
growth rates and insuring that the caterpillars have an empty gut when they leave the
tent to feed (Casey et ai, 1988).
Butterflies are a conspicuous diurnal insect
group which require elevated thoracic temperatures for continuous flight (Heinrich,
1974). With a few exceptions these animals
show limited capacity for endothermy. Most
are ectothermic yet control their body temperature by basking. Patterns ofbasking have
been analysed in detail in some groups (see
Kingsolver, 1985, for review) and are characterized by the position of the wings relative to incoming solar radiation. Dorsal,
lateral, body and baskers have several characteristics in common. Their wing bases are
melanized, allowing greater amounts of
radiant heat to be absorbed (Wasserthal,
1975). This heat is transferred to the thorax,
enhancing rates of heating either through
direct conduction, convection or both
(Kingsolver, 1985).
Kingsolver and colleagues produced a
biophysical model of the body temperature
of Colias butterflies. Using laboratory
derived values for radiant absorptivity and
convection coefficients (Kingsolver and
65
~
55
•
45
1K
3
35
25
1
14
Time of
day
15
(hrs)
FIG. 2. Thermal relations of Eastern tent caterpillars
in the field. (A) The range of air temperatures in different locations inside the tent. (B) Operative temperatures (Te) of models placed in various locations (closed
circles = underside of tent (in shade); diamonds = single model on dorsal surface in sunlight; closed triangles
= "clump model" on the same dorsal surface consisting
of five freeze dried caterpillars attached to resemble a
natural caterpillar aggregation; open triangles = a single
caterpillar model placed on a branch away from the
tent. (Q Body temperatures of living caterpillars under
the same environmental conditions utilizing the thermal heterogeneity of the tent microclimate (after Joos
et ai, 1988).
230
TIMOTHY M. CASEY
-c
u se
tt
e
f
!28
a
32
• 24 •
a
g
a 28
E
Skyland
\
1
t •
20 -
24
Montroa*
o
20
IS
11
13
Hour of day
16
13
1 1
Hour of day
1S
1 00
=
20 -
Hour of day
FIG. 3. Predicted and measured body temperatures of Colias philodice eriphyle butterflies in two different
habitats (A and C). Triangles and circles indicate measured basking temperatures of two individual males
throughout the day. Solid line indicates predicted temperature based on heat balance model. Diamonds indicate
air temperature. Dashed lines indicate minimumflighttemperature. Observed levels offlightactivity from two
different habitats (B and D). (Modified from Kingsolver, 1983a)
Moffat, 1982), body temperatures of the
butterflies in the field during basking could
be predicted, based on measured radiation
and convection (Kingsolver, 1983a, b).
Simultaneous measurements of thermocouple implanted models verified the predicted
temperatures to within 1.5-2.0cC. Because
flight in these butterflies is limited to body
temperatures between 30 and 40°C (Watt,
1968, 1969), the model was used to predict
the cumulative flight activity (KFAT) for a
butterfly based on microclimatic measurements and a predictive climate space model
(Porter and Gates, 1969). This "flight space"
model accurately predicted the times when
the animals were flight ready based on a
biophysical model predicting body temperatures (Fig. 3). Although these predictions
were based on basking butterflies and the
avenues of heat exchange for flying animals
differs markedly from that of resting animals (see below), these predictions closely
matched observedflighttimes of Colias butterflies. A detailed examination of heat
exchange duringflightin Colias (Tsuji et al,
1986) demonstrated that Tth during flight
was about 2°C lower than that of butterflies
basking within the vegetation (away from
the wind) and about 2°C higher than those
for basking butterflies at the top of the vegetation. In contrast to the basking condition, Colias during flight are somewhat
endothermic as a consequence of metabolic
heat production associated with the flight
effort as is typical of small moths during
flight (Bartholomew and Heinrich, 1973;
Casey, 1980).
Examining butterflies along an altitudinal
gradient, Kingsolver (19836) demonstrated
that butterfly fecundity in certain habitats
HEAT EXCHANGE OF INSECTS
was directly associated with KFAT. KFAT,
in turn, was related to body temperatures
which varied as microclimates vary with
altitude. Further studies examined 'optimal' phenotypes by manipulating the major
morphological variables in the climate space
model and compared these findings with
measured values for the phenotypic characters along an altitudinal gradient (Kingsolver and Watt, 1983). The results indicate
significant differences between the measured values as a function of altitude and
close agreement between their predicted
optima and the measured values.
Taken together, the data indicate that
Colias butterflies are strongly dependent
upon weather conditions for flight which in
turn, may have important consequences for
their fecundity and realized reproduction.
They also demonstrate that local populations adapt to the prevailing weather conditions both in space and in time. Application of a biophysical model of heat
exchange thus provides important information about the population biology of these
butterflies. These data have important
implications for the flight characteristics of
Colias as well. Given their small size, high
sensitivity to weather conditions, and the
importance of flight to their reproductive
biology, these butterflies may exhibit strong
selection for physiological and biochemical
characteristics of the flight motor. Polymorphic genotypes of the glycolytic gene
locus phosphoglucose isomerase (PGI) vary
in transient and maximal rates of fuel supply to flight muscle, causing different genotypes to differ in their ability to initiate and
sustain flight at suboptimal temperatures.
Depending on prevailing weather conditions this advantage may enhance mating
success for the favored genotype by as much
as 50% (Watt, 1985).
ENDOTHERMY DURING FLIGHT
A lumped parameter analysis has routinely been used to analyse heat exchange
of insects. This approach characterizes heat
exchange with a single internal temperature
and a single heat transfer coefficient. While
this analysis may be appropriate for certain
situations, it is of limited utility when analysing heat exchange of flying insects. The
231
situation in a flying insect is much more
complicated because the source of heat production is local (only in the thorax). The
thorax of endothermic insects is often highly
insulated either with scales (moths, bees) or
internally with tracheal sacs (dragonflies) (see
May, 1983, for review). The head and abdomen complicate the picture because these
differ in size, insulation, surface to volume
ratio, and each has been shown to represent
a site of considerable variability in heat
transfer via blood circulation. Consequently, data from these three regions are
needed to produce a quantitative estimate
of heat exchange. The equation characterizing heat exchange of aflyinginsect at steady
state would be:
dH/dt = Cth(Tth - T
+ C h (T h -
Cab(Tab - Te(ab))
+ E + Po
where C,h, Cab, and Ch represent the heat
transfer coefficients of the thorax, abdomen
and head, Tth, Tab and Th represent their
respective temperatures during flight and
Te(th)> Te(ab) and Tc(h) represent the operative
temperatures of these body parts under the
same environmental conditions, E represents the rate of evaporative cooling and P o
represents the portion of the metabolic rate
which is used by the animal to overcome
aerodynamic and inertial drag forces. Using
the above equation, several authors have
compared estimates of total heat loss with
directly measured aerobic metabolism
(Casey, 1980, 1981; May and Casey, 1983;
Hegel and Casey, 1982). For animals which
are endothermic but which do not regulate
T,h, calculated rates of heat loss are generally
similar to measured rates of heat production
(Weis-Fogh, 1968; Casey, 1980).
For endothermic insects which regulate
Tth physiologically during continuous flight
such as moths (Heinrich, 1970; Casey,
19766, 1981; Hegel and Casey, 1982) and
bees flying in shade in a tropical rainforest
(May and Casey, 1983) heat budgets show
reasonable agreement at low ambient temperatures and become progressively less
reliable as ambient temperatures increase.
Figure 4a shows body temperatures of the
sphinx moth, Manduca sexta, during continuous hovering flight and Figure 4B an
evaluation of heat exchange. At Ta of 24°C,
232
TIMOTHY M. CASEY
Thorax
50
160
40
120
S? 30
20
Evaporation
10
20
30
Air temperature (°C)
15
20
25
30
Ambient temperature (0C)
FIG. 4. (A) Regional body temperatures and (B) rates of heat exchange of the sphinx moth, Manduca sexta,
during continuous hovering flight over a range of air temperatures in the laboratory (i.e., with no significant
external radiant heating). (Modified from Hegel and Casey, 1982)
heat loss from the thorax accounts for only using this approach or that assumptions used
about 30% of the measured heat production in calculations are inadequate and therefore
and at high Ta it is less than 20% above heat exchange is not being appropriately
33°C (Hegel and Casey, 1982). Heat loss estimated.
from the head of this species is a substantial
A possible explanation for this inaccuracy
portion of the total heat production at low is suggested by empirical data for heat transTas; more than 1.5 times either evaporative fer of dragonflies (May, 1976; Heinrich and
or abdominal heat loss. However, as Ta Casey, 1978). Large "flier" dragonflies such
increases, the contribution of the head to as Anax juneus are capable of transferring
total heat loss decreases to less than half the large quantities of heat from thorax to abdoevaporative heat loss and less than 25% of men by haemolymph circulation. If haethe abdominal heat loss. In contrast, molymph flow between these two regions is
although the temperature of the abdomen interrupted, or the dorsal vessel is ligated,
is only slightly elevated above Ta, due to its the temperature distribution of an exterlarge mass and high heat transfer coefficient nally heated living dragonfly becomes
(Heinrich, 1971a), total heat loss from the essentially the same as a dead one. The
abdomen accounts for almost 40% of the abdominal temperatures which are usually
total heat production at high Ta. At most recorded are based on a single grab and stab
Tas abdominal heat loss exceeds that of the measurement and may not correctly charhead and at high Ta it is considerably greater acterize heat exchange between the abdothan thoracic heat loss as well. A previous men and the environment because the temheat budget for hovering sphinx moths perature at different points of the abdomen
which did not examine the heat exchange may vary considerably (Heinrich, 1971 b\ see
of the head (Casey, 19766) accounted for also Heinrich and Casey, 1978).
only 69, 64 and 63% of measured heat proThe abdomen is not the only site used as
duction at Tas of 15, 23 and 32°C, respeca
thermal
window. Honeybees are morphotively. Thus, accounting for heat exchange
logically
prevented
from shunting large
of the head provides a more accurate picquantities
of
heat
to
the abdomen due to
ture. However, it is significant that heat proloops
in
the
dorsal
vessel
which guarantee
duction does not equal heat loss at the highthat
a
counter
current
exchanger
retains heat
est air temperatures in either of the sphinx
in
the
thorax.
Honeybees
are
high
tempermoth budgets or for Euglossine bees flying
,
thoracic
temature
specialists.
At
low
T
a
in shade (May and Casey, 1983). These data
perature
essentially
follows
the
ambient
suggest that there is either a major site of
heat exchange not being taken into account temperature (that is, the bees are endothermically elevating Tlh but they exhibit rela-
HEAT EXCHANGE OF INSECTS
tively poor thermoregulation). At high temperatures however, they exhibit close control
of Tth and this control is mediated by high
rates of blood borne heat from the thorax
to the head and by massive rates of evaporative cooling to keep head temperature
low, thereby maintaining a thermal gradient
from thorax to head (Heinrich, 1980a, b).
Although the head temperature is close to
the environmental temperature, high rates
of heat exchange occur via evaporation.
Thus, the magnitude and significance of the
head as a site of heat exchange varies dramatically in different species. In order to
produce an accurate heat budget investigators must not only measure temperatures
and heat transfer coefficients but also be
aware of the physiological processes used
by the species of interest. Moreover, without knowing about the evaporative cooling
mechanism of the head, simple evaluation
of temperature and heat transfer coefficient
data from the three body regions of honeybees would yield inaccurate estimates of
heat production.
The endothermic species mentioned
above are advantageous to analyse because
their physiology has been examined in detail
and their flight metabolism has also been
measured providing an independent estimate of the rate of heat production. In many
cases heat production during free flight can
not be obtained and thermal conditions in
their environment are far more complex
than in a laboratory controlled temperature
room. Discrepancies exist between laboratory data and field data for regional body
temperatures of the same species. Heinrich
(1976) demonstrated that bumblebees regulate their rates of heat loss during continuous flight by controlling the circulation
between the thorax and the abdomen. In
the laboratory, the abdominal temperature
excess increases with increasing Ta which is
consistent with the mechanism proposed.
However, abdominal temperatures of bumblebees in the field do not show the same
relationship and in fact usually show a slope
of one or less on a plot of Tab vs. Ta (Heinrich, 1972). Similar relationships have been
reported for dragonflies (May, 1987; D. Polcyn, personal communication), Euglossine
bees (May and Casey, 1983) and carpenter
233
bees(Chappell, 1982; Baird, 1986; Heinrich
and Buchmann, 1986). These data are not
consistent with the hypothesis that heat
transfer to the abdomen is the mechanism
of thermoregulation unless the reported values for abdominal temperature are not an
accurate biophysical representation. At
present we are forced to conclude that this
technique for quantifying energy expenditure is still rather approximate. Further
studies are needed particularly on the magnitude and control of the evaporative component of the energy budget.
Since oxygen consumption does not vary
with temperature during continuous hovering flight (see Casey, 1989, for review) the
general consensus is that thermoregulation
during flight must occur by regulation of
heat loss (Heinrich, 1974; Kammer, 1981).
However, laboratory studies do not allow
insects to display normal flight behavior and
in most cases heat budgets are available only
for hovering animals. For strongly flying
diurnal insects such as dragonflies and bumblebees, solar radiation further complicates
the picture. It is clear that small insects elevate their temperatures while basking prior
to flight and in fact, need to be well above
ambient in order for their muscles to produce sufficient lift to remain airborne (Heinrich, 1974). High heat loads should occur
from both internally generated heat (e.g.,
bumblebees can produce a thoracic temperature excess of 30°C above Ta in the laboratory) and exogenous heating. Carpenter
bees fly throughout the day in deserts of the
southwestern United States, despite high
ambient temperatures and intense solar
radiation, maintaining thoracic temperatures between 39 and 46°C over a T a range
from 20-40°C. Solar radiation has a large
effect on Tth, but only at low wind speeds.
Operative temperatures for bees in full sunlight are about 10°C above air temperature,
but they drop to about 2°C above Ta at moderate wind speeds (Chappell, 1982). Hovering flight is only possible for relatively
short periods due to the combination of high
exogenous and endogenous heating. In order
to remain airborne the bees alternate hovering with fast forward flight. Using a combination of biophysical and physiological
measurements, Chappell (1982) produced
234
TIMOTHY M. CASEY
60 _,
I
i.
20.
-80
-60
-40
-20
0
Environmental Temperature (°C)
20
40
FIG. 5. Oxygen consumption of colonies of honeybees
over a range of ambient temperatures (Modified from
Southwick, 1988)
the first flight space model for an endothermic diurnal insect. Based on calculated heat
loads and heating rates, Chappell (1982)
postulates that varying flight performance
allows the bees to prevent overheating by
altering convective heat exchange. Increases
in metabolic heat production are probably
relatively low compared to increases in convective heat exchange (Ellington et ai, 1990).
Increased thoracic heat loss at higher flight
speeds may also be enhanced by increased
heat loss from the abdomen (Chappell, 1982)
or from the head (Heinrich and Buchmann,
1986), or both.
Recent data by Polcyn (1988) for dragonflies suggests that they may be forced to
fly at midday to remain cool. Thoracic temperatures of dragonflies during flight are
actually lower than operative temperatures
of stationary models, suggesting that the
increases in convective cooling override the
increased flight metabolism and solar radiation. Moreover, both "percher" and "flier"
species exhibit continuous flight at high
temperatures although the former apparently can not regulate heat exchange between
thorax and abdomen (May, 1976; Heinrich
and Casey, 1978). These data suggest that
behavioral control of flight speed represents
an important mechanism for thermoregulation.
HIVES AND SWARMS
Honeybees are the most effective thermoregulators of the social insects (reviewed
by Seeley and Heinrich, 1981). These
"superorganisms" display an amazingly
sophisticated thermoregulatory control. In
a wonderful study on honeybee swarms
Heinrich (1981) thoroughly evaluated thermoregulation of swarms. He demonstrated
that the swarm expands and contracts to
manipulate its rate of heat loss over a very
wide range of ambient temperatures. This
regulation of heat loss is equivalent to the
mechanisms employed by endothermic vertebrate in the thermal neutral zone.
Southwick (1988) examined energy
metabolism in clusters of bees over an
ambient temperature range from 30 -80°C. The bees exhibited a 25°C thermoneutral zone which extended to — 10°C.
Below Ta of - 10°C the bees exhibited a linear increase in metabolism to about — 60°C
when metabolism may have peaked (Fig. 5).
Resting energy metabolism for various sized
clusters conforms almost precisely with the
resting metabolism vs. body mass data for
mammals.
Cooling rates of swarms and clusters are
strongly size dependent (Heinrich, 1981;
Southwick, 1985). The calculated heat
transfer coefficient of these groups is about
the same as that predicted for resting mammals over an equivalent size range (Southwick, 1985).
SUMMARY AND CONCLUSIONS
The thermal biology of insects is fundamental to all their physiological functions
and important aspects of their ecology
including growth, mating and reproduction.
The study of insect thermoregulation has
matured. In the process the field has proceeded from descriptive studies to quantitative evaluations of heat exchange. Biophysical analysis has been useful in
unraveling problems at several levels of biological organization. The utility of this
method for evaluating mechanisms of heat
exchange has been appreciated since the
pioneering work of Parry (1951) and Digby
(1955). More recent studies have moved
from the laboratory to the field providing a
better appreciation for the complexity and
importance of microclimate to insect thermal biology. In the process the nature of the
questions has changed from mechanistic
analysis of heat exchange to questions related
to ecological and evolutionary consequences of heat exchange. Studies of the
HEAT EXCHANGE OF INSECTS
biophysical ecology of insects coupled with
careful behavioral studies and physiological
experiments are providing new understanding of the adaptations of insects which cannot be determined from laboratory studies.
Although general patterns are clear, the
staggering diversity of insects suggests that
new adaptations remain to be discovered.
Biophysical analysis should remain an
important tool in the arsenal of insect physiologists and ecologists.
ACKNOWLEDGMENTS
I thank Drs. Jim Spotila and Mike
O'Connor for inviting me to present a paper
in this symposium. Although I am an "aficionado" of the approach, I normally would
not consider myself a biophysical ecologist
(indeed, if asked for details I would tell a
student to go read some papers by several
of the participants of this symposium).
Nonetheless, I am happy to bear witness to
the power and the utility of biophysical
methods for examining biological questions. Financial support to the author from
the National Science Foundation
(#DCB8802443) and the New Jersey Agricultural Experiment Station (MacintireStennis project 08337) is gratefully
acknowledged.
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