Temperature regulation in burying beetles (Nicrophorus spp.: Coleoptera: Silphidae): effects of body size, morphology and environmental temperature
Department of Biological Sciences, Idaho State University, Pocatello, ID 83209-8007, USA
* Author for correspondence (e-mail: merrmeli{at}isu.edu)
Accepted 17 November 2003
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Summary |
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Key words: thermoregulation, body size, body temperature, burying beetle, operative temperature, flight temperature, Nicrophorus spp., Coleoptera
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Introduction |
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The ecology and reproductive behavior of burying beetles (Coleoptera:
Silphidae: Nicrophorus) are well studied
(Eggert and Müller, 1997;
Scott, 1998
;
Smith and Merrick, 2001
);
however, little is known about the thermal ecology of this genus. Burying
beetles must secure an ephemeral resource (in this case, the carcass of a
small vertebrate) to complete their life cycle. Body size and the potential
for increased thermal stability in larger species may play important roles in
securing these resources from both conspecifics and heterospecifics. The
ability to regulate and maintain a thoracic temperature independent of ambient
conditions during and after flight may provide competitive benefits, both in
terms of carcass defense and speed of burial and the ability to search for
carcasses and mates over a wider temperature range, as demonstrated for
Plecoma spp. (Morgan,
1987
). There is also evidence to suggest that there are
differential tolerances to environmental temperatures among
Nicrophorus species (Wilson et
al., 1984
; Trumbo,
1990
; Sikes, 1996
;
Scott, 1998
), which may be
related to factors such as body size, pigmentation or evolutionary history and
may play a role in species distributions and coexistence. Sympatric species
that utilize different thermal and temporal windows for activity have been
shown to coexist in the same habitat types without much direct contact
(Wilson et al., 1984
), and
larger species in northern Europe and northeastern North America have been
shown to be nocturnal (Scott,
1998
).
Regulation of body temperature in Nicrophorus could be
accomplished by behaviors such as basking, posturing and seeking shade (Casey,
1981,
1992
;
Heinrich, 1996
), by regulating
(conserving or losing) heat generated endogenously by flight muscles in the
thorax (Kammer, 1981
;
Heinrich, 1993
,
1996
), altering metabolic rate
or wing beat frequency or a combination of both behavioral and physiological
thermoregulation (Coelho,
2001
). Nicrophorus have been described as "good,
persistent fliers that are capable of covering large distances in a short
period of time" (Eggert and
Müller, 1997
), and members of this genus fall within the size
class of smaller beetles known to regulate their body temperatures during
flight (0.0031.8 g; Chappell,
1984
; Morgan,
1987
; Oertli,
1989
; Chown and Scholtz,
1993
). Smaller beetles like Nicrophorus may rely on high
wing loading and wing beat frequencies, insulation and morphology to
counteract the amount of body heat lost to convection during flight
(Chown and Scholtz, 1993
), as
opposed to passive heat retention as a result of a large body.
We tested whether three Nicrophorus species (N. hybridus, N.
guttula and N. investigator) are able to (1) warm up before
flight via endogenous heat production and (2) regulate body
temperature during and following flight. We further investigated whether wing
loading or body mass affected thermoregulatory ability, as well as whether the
thermal environment influences the daily activity patterns of burying beetles.
We assess thermoregulatory ability using two measures: (1) the relationship
between thoracic temperature during flight and ambient temperature and (2) the
relationship between thoracic temperature during flight and the effective
(operative) temperature of a dead beetle in the flight position (index of
thermoregulatory performance; Bishop and
Armbruster, 1999). Additionally, we describe daily activity
patterns for the three species over two 24-h observation periods and
investigate how these patterns could be explained in part by the thermal
environment that Nicrophorus experiences and by differential
thermoregulatory abilities among species.
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Materials and methods |
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Capture techniques
Beetles were captured in traps consisting of metal cans (17 cm deep, 15.5
cm in diameter) pierced to allow drainage, half-filled with soil and covered
with wire screening formed into a funnel. Each trap was suspended
approximately 40 cm above the ground and baited with fresh chicken and water
added to the soil (Smith and Merrick,
2001).
Body temperature before, after and during flight
To determine the thermoregulatory ability of Nicrophorus before
and after flight, we conducted a series of flight trials in a 2.44 mx3 m
Weatherport® or in a 1.2 mx1.2m screen tent throughout the season
and over a range of ambient temperatures. Field-caught beetles were used
within 24 h of capture or held in the laboratory and used within two weeks of
capture. We tested a total of 137 beetles, including individuals of both
sexes, of N. hybridus Hatch and Angell (N=53), N.
guttula Motschulsky (N=28) and N. investigator
Zetterstedt (Idaho N=7, Colorado N=49). Although N.
defodiens were collected, no flight information was obtained from this
species.
For each flight trial we randomly selected a beetle from a holding
container and immediately measured both its abdominal and thoracic
temperatures using a 29-gauge hypodermic temperature probe (Model
HYPO-33-1-T-G-60-SMP-M; Omega Engineering Inc., Stamford, CT, USA) and a
digital microprocessor thermometer (Omega Model HH23). Abdominal temperatures
(Tab) were taken by inserting the probe between two
abdominal sclerites, and thoracic temperatures (Tthx) were
taken by inserting the probe into the ventral metathorax. After measuring the
temperatures, a beetle was then placed on the middle of a stick (810 cm
diameter, 0.5 m length) secured at a 45° angle, where it would walk to the
end of the stick and make preparations to fly. After take-off and flights of
24 s duration, the beetle's thoracic and abdominal temperatures were
measured again. We wore gloves while handling the beetles and measurements
were made within 23 s after landing. Because Nicrophorus have
the ability to raise Tthx to a temperature adequate for
flight (2530°C) even on cooler days by basking (M. J. Merrick
and R. J. Smith, personal observation), every captive flight took place in the
absence of direct sunlight, in addition to being sheltered from wind.
The time between the preflight Tthx measurement and actual flight was frequently long, often taking more than 510 min. We were therefore unable to determine when the warming occurred or if the temperature immediately prior to flight was different from the post-flight temperatures, although continuous flight measurements indicate that during flight in the shade, thoracic temperatures remain near the initial flight temperature. We assume that a beetle's Tthx immediately before flight and Tthx measured post-flight were similar since each captive flight was short (<4 s.). During the time prior to flight, we did not observe any shivering, wing vibrations or outward signs of muscle contraction. Beetles spent this time cleaning foretarsae and antennae clubs, in addition to extending and retracting wings from below the elytra.
We recorded the ambient temperature using both a bare thermocouple and the
effective environmental temperature (Te) of a null
temperature model in the flight position (Te flight); a
dead, dry beetle equipped with thermocouples, wings and elytra raised, and
suspended approximately 0.75 m above the ground
(Hertz et al., 1993) after
each short flight. We also measured hourly the operative temperatures of null
temperature models placed in positions that represented other behaviors a
beetle could adopt in response to its thermal environment: (1) on bare ground,
12 cm below the ground surface, and (2) beneath foliage (at the base of
short grasses or under fresh leaves resting upon a soil substrate). Operative
temperatures, also known as Te, take into account the
effects of radiative and convective heat gain and loss in addition to ambient
temperatures on the body temperature of a nonthermoregulating organism
(Bakken, 1992
;
Heinrich, 1993
) and more
closely approximate the thermal environment that beetles actually experience
(Bakken, 1992
;
Bishop and Armbruster, 1999
).
Differences between Te and actual body temperature
(Tb) can indicate some form of thermoregulation by the
animal (i.e. Tb>Te indicates
endogenous heat production or basking).
To address the point raised by Stone and Willmer
(1989a) that some insects
actually warm up upon cessation of flight, which could cause overestimation of
post-flight Tthx measurements, we measured
Tthx continuously for 1012 min after 24 successful
flight trials for N. hybridus (N=4), N. guttula
(N=3) and N. investigator (N=17) individuals to
determine whether beetles are able to regulate an elevated thoracic
temperature after flight. We recorded Tthx in four
tethered N. hybridus individuals during continuous (1239 min)
flights and subsequent cooling to determine whether Tthx
is regulated during longer flights.
Indices of thermoregulation
A regression of post-flight thoracic temperature against ambient
temperature was used as an index of thermoregulatory precision
(Oertli, 1989). Additionally,
we calculated a thermoregulatory performance index for each species. Bishop
and Armbruster (1999
) define
this index as the slope of Tthx against
Te, which indicates how a real beetle regulates its
thoracic temperature in flight compared with a non-regulating, metabolically
inactive one. Differences between Tthx and
Te would then be the result of physiological or behavioral
control of body temperature (Casey,
1992
). A slope equal to or close to one
(Tthx=Ta) is considered evidence for
thermal conformity, whereas slopes close to or approaching zero are evidence
of thermoregulation.
Possible mechanisms for thermoregulation
Cooling rates and body size
Cooling rates (deg. min1) were calculated for beetles
representing three species and ranging in mass from 0.11 g to 0.62 g. Beetles
were observed cooling after short flights (N=24) and after artificial
heating (N=13), where live beetles were heated to a
Tthx of 40°C and then allowed to cool. Differences in
cooling rates between size classes indicate the amount of heat retention that
is a result of body size alone. Based on physiological properties alone,
larger beetles should cool more slowly because of a decreased surface area to
volume ratio and higher thermal inertia. Three body size classes were assigned
for all species based on the median body mass ± 25th and 75th
percentiles (small 25th percentile; large
75th percentile; medium
25th75th percentile). Cooling rates of live, artificially heated
beetles (N=13) were determined by placing the 29-gauge hypodermic
thermocouple probe into the lateral metathorax of a beetle that had been
cross-pinned to a Styrofoam block. The beetle was then placed inside a 28
cmx18 cmx18 cm Styrofoam box and heated to 40°C with an
incandescent lamp, then allowed to cool to within 12° of ambient
air temperature while its thoracic temperature was recorded every 30 s.
Cooling rates of live beetles after flight (N=24) were also measured
for 1012 min following flight (see previous section), and the
differences in cooling rates between size classes for post-flight and
artificially heated beetles were compared in a one-way analysis of variance
(ANOVA). For comparisons, cooling rates for artificially heated beetles were
also calculated between the approximate average ambient temperature recorded
for outdoor flights and ambient laboratory temperature.
Insulation
To understand the role that wings, elytra and thoracic pile play in
insulation and maintenance of body temperature, we divided 28 beetles
(representing three species; N. hybridus, N. investigator and N.
guttula) into three groups: (1) no treatment, (2) thoracic pile removed
with a scalpel and (3) wings and elytra removed
(Chown and Scholtz, 1993). We
determined cooling rates for live beetles in the three treatments as above and
compared cooling rates using a one-way ANOVA.
Physiological heat transfer
We employed methods similar to Chown and Scholtz
(1993) and Coelho
(2001
) to determine whether or
not Nicrophorus have the ability to transfer heat produced in the
thorax to the abdomen to regulate Tthx. A live beetle was
cross-pinned to a Styrofoam block, and one thermocouple probe was inserted
into the lateral thorax and another into the abdomen. The head and thorax were
heated with an incandescent lamp while the abdomen was shielded with Styrofoam
wrapped with aluminum foil. Measurements of Tthx and
Tab were taken simultaneously every 30 s until a thoracic
temperature of 40°C was attained. The beetle was then euthanized with an
injection of ethyl acetate and allowed to cool. Once the
Tthx had returned to within 1°C of
Ta, the procedure was repeated for the same individual,
now dead. A total of 12 N. hybridus individuals were used in this
investigation. We used paired t-tests to compare the rates of warm-up
between alive and dead Tthx and Tab,
between alive Tthx and Tab and between
dead Tthx and Tab. If physiologically
mediated heat transfer to the abdomen were occurring, one would expect the
rate of abdominal heating to be higher in the living beetle than the dead
beetle.
Wing loading
We measured wing loading to quantify differences in the amount of power
output required for flight between the species. Species with a higher average
wing loading may produce more excess heat in flight. To calculate wing
loading, one wing was removed at its base from each beetle that flew
successfully (N=137). Each beetle was weighed to the nearest
milligram following flight and temperature measurements. Wing area was
determined in the lab by scanning (Epson 636U scanner) wings taped to graph
paper (five squares per centimeter) into NIH image® software, where we
measured the area of each wing in mm2. Wing loading was calculated
in mg mm2 for each beetle.
Influence of thermal environment on daily activity patterns
To see how daily activity patterns were affected by temperature, two 24-h
field observations were carried out on 28 June and 28 July at the South Bench
site in Idaho. During each 24-h observation period, traps were checked every
23 h during the day and twice during the night (after midnight), and
the number of beetles and species of each was recorded. During daylight hours,
the number of beetles seen flying in the vicinity of the traps was also
recorded. These observations allowed us to estimate the relative beetle
activity at different times of the day.
We measured the Tthx and Tab of beetles caught flying into a trap, recorded their weight and removed one wing to calculate wing loading (see previous section). Each time that traps were checked or a beetle was seen flying overhead, we recorded the Ta and Te of a beetle in a flight position. Measurements from the other Te models (on bare ground, 12 cm below ground, under foliage) were taken every 23 h during a 24-h observation period.
We also developed a model to predict Tthx for beetles throughout the day. We measured Te throughout an entire day in late July 2001 and then applied these values to the regression equation of Tthx against Te for each species to predict post-flight thoracic temperatures at each Te value. We then used the range of post-flight Tthx actually measured for the three species in flight trials and in the field and compared these ranges to the predicted Tthx throughout the day to estimate windows of possible flight times.
Statistical analyses
All statistical tests were carried out using StatView® 5.0 for
Macintosh. ANOVAs were followed by Fisher's PLSD post-hoc multiple
comparison tests. Paired t-tests were used to determine significant
differences between pairs of measurements taken for individuals and to test if
there were significant differences in Tthx pre- and
post-flight, between Tthx and Tab and
in cooling/warming rates for living vs dead individuals. Simple,
linear regression was used to test whether the relationship between
Tb and Tte or Ta
was significantly different from zero. Mean values, unless otherwise
specified, are reported ±1 S.E.M.
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Results |
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Post-flight temperature excess in the thorax decreased significantly with increasing ambient temperature (slope=0.523, r2=0.303, N=135, P<0.0001). Above approximately 30°C, the temperature excess between Tthx and Ta becomes negative, indicating that beetles lost heat before or during flight, and no energy for warming up is required (Fig. 1). Post-flight Tthx did not differ significantly among species (for all Idaho and Colorado sites; one-way ANOVA, F=0.803, d.f.=2, P=0.4502), and post-hoc comparisons show that there were no significant differences between species.
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Recordings of continuous Tthx measurements for four sustained (>5 min), tethered flights (Fig. 2) show that N. hybridus has the ability to sustain and regulate thoracic temperatures to some degree during long flights and that the length of the flight may be dependent upon ambient temperature, as the longest flight occurred at the lowest Ta. Mean Tthx for the four sustained flights was 31.5±2.6°C compared with a mean Ta of 26.13°C.
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Indices of thermoregulation
Nicrophorus hybridus is significantly larger than N.
guttula (t=5.364, P<0.0001, d.f.=79) and N.
investigator: N. hybridus mean mass=500±20 mg, N.
guttula mean mass=340±20 mg and N. investigator mean
mass=293±10 mg. The slopes of Tthx vs
Ta and Tthx vs Te of
an operative model (thermoregulatory performance index) indicate that N.
hybridus is better able to regulate body temperature prior to and during
short flights compared with N. guttula and N. investigator.
The slope of the regression of Tthx against
Ta for N. hybridus (0.315;
r2=0.227) is much closer to zero than the slopes
calculated for N. guttula (0.771; r2=0.784) and
N. investigator (0.610; r2=0.221) and is also
significantly different from the slopes for these smaller species (N.
hybridus vs N. guttula t=33.853, P<0.0001, d.f.=77; N.
hybridus vs N. investigator t=14.7795, P<0.0001, d.f.=107).
The slopes for Tthx vs Te
(thermoregulatory performance index) were similar to those comparing
Tthx and Ta, and, again, the
regression slope for N. hybridus (0.370;
r2=0.411) is closer to zero than the slopes calculated for
N. guttula (0.636; r2=0.679) and N.
investigator (0.575; r2=0.327) and is also
significantly different from the other two (N. hybridus vs N. guttula
t=19.777, P<0.0001, d.f.=77; N. hybridus vs N.
investigator t=12.059, P<0.0001, d.f.=107)
(Fig. 3).
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Mechanisms for thermoregulation
Cooling rates and body size
Beetles cooling after short flights (mean post-flight
Tthx=30.4°C) cooled at the same rate as beetles that
were artificially heated when artificial cooling rates were calculated from
30.4°C (t=0.275, d.f.=35, P=0.7847). No beetles warmed
up following flight unless flight was initiated while the post-flight
temperatures were being measured, in which case the trial was omitted from the
analysis of cooling rates. Post-flight and artificial cooling rates (from
30.4°C) were then combined, and cooling rates among size classes were
compared. As expected, based on surface area to volume ratios, large beetles
cooled more slowly than small individuals and significantly slower than
medium-sized individuals (one-way ANOVA, F=4.081, d.f.=2
P=0.0261; Fisher's PLSD, large vs medium mean
difference=0.745 deg. min1, P=0.0074).
Beetles in the large size class (N=10) had a mean cooling rate of
1.062±0.121 deg. min1, beetles in the medium
size class (N=21) had a mean cooling rate of
1.807±0.166 deg. min1, and beetles in the
small size class (N=5) had a mean cooling rate of
1.610±0.341 deg. min1. Cooling rates for the
three species following short flights are summarized in
Table 1. Artificial cooling was
only measured for N. investigator and N. guttula.
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Insulation
To determine the importance of the wings, elytra and thoracic pile as
insulation for burying beetles, we compared the cooling rate of individuals
assigned to one of three treatments: intact (I), wings and elytra removed
(WER), and thoracic pile removed (TPR). There was a significant effect of
treatment (F=4.332, P=0.0248, d.f.=2, power=0.696); beetles
with elytra removed cooled significantly faster (mean=0.145 deg.
min1) than intact beetles (mean=0.098 deg.
min1) (Fisher's PLSD, P=0.0110). Beetles with
thoracic pile removed also cooled faster than intact beetles, but only
marginally (Fisher's PLSD, P=0.0655). Because of the small sample
size in each treatment (I, N=14; WER, N=7; TPR,
N=7), we increased the power of the test (=0.10, power=0.816),
which resulted in a significant difference between the cooling rates of intact
beetles compared with those with insulation removed.
Physiological heat transfer
The rate of abdominal warming between living and freshly killed individuals
was not different (paired t=0.989, P=0.3461, d.f.=10),
indicating that living beetles do not actively shunt heat from the thorax to
the abdomen. Live beetle Tthx increased on average 0.451
deg. min1 faster than in dead beetles, but the difference
was not significant (paired t=1.898, P=0.0869, d.f.=10).
Wing loading
Wing loading was significantly different among species, with N.
hybridus (mean=4.61±0.08 mg mm2) and N.
guttula (mean=4.55± 0.13 mg mm2) exhibiting
significantly higher levels of wing loading than those calculated for N.
investigator (mean=3.37±0.09 mg mm2) (one-way
ANOVA, F=58.617, d.f.=2, P<0.0001; Fisher's PLSD, N.
guttula vs N. investigator mean difference= 1.182 mg
mm2, P<0.0001; N. hybridus vs N.
investigator mean difference=1.244 mg mm2,
P<0.0001). There was also a positive relationship between the
post-flight temperature excess (post-flight
TthxTa) and wing loading in
N. hybridus (slope=1.189, r2=0.066,
P=0.06) and N. investigator (slope=0.868,
r2=0.026, P=0.292) but not for N.
guttula (slope=0.04, r2<0.0001,
P=0.924). Wing loading measurements for each species are summarized
in Table 1.
Influence of thermal environment on daily activity patterns
We found four species of burying beetle co-occurring at the two Idaho study
sites: N. hybridis, N. guttula, N. investigator and N.
defodiens. During a 24-h period, beetle activity began in mid-morning and
then peaked in the late afternoon/early evening, when ambient temperatures
were 2030°C. Around mid-day, ambient temperatures ranged from
25°C to 30°C. Although this temperature range is moderate, the
temperature of operative models on the ground surface and suspended
approximately 1 m above the ground in a flight posture often approached lethal
temperatures, especially during periods of full sun (mean lethal temperature
from previous cooling experiments= 46.15±0.6°C, N=8; M. J.
Merrick and R. J. Smith, unpublished data;
Fig. 4).
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The windows of activity time available for flight throughout the day differed among the three species. Based on the amount of time throughout the day that the post-flight Tthx ranges for the three species (N. hybridus, 24.432.7°C; N. guttula, 22.434.5°C; N. investigator, 2138°C) fell within the predicted thoracic flight temperatures (based on the species-specific regression of Tthx vs Te), it appears that N. investigator would have the largest potential window of activity time, followed by N. hybridus and then N. guttula (Fig. 5). This assumes that the post-flight Tthx measured for each species following short flights approximates actual Tthx in the field and that the range of ambient air temperatures within which we collected flight data reflects the range of ambient air temperatures in which these species are active under field conditions.
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Discussion |
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Data from four continuous, sustained flights
(Fig. 2) show that N.
hybridus can maintain elevated Tthx over long periods
of flight. Longer flights may be possible at cooler Tas,
suggested by the fact that the longest flight occurred at 28°C, the
coolest Ta measured for any of the continuous flights. It
is possible that smaller species also regulate Tthx during
sustained flight, based on results from Oertli
(1989) where small beetles
(793 mg, Nicrophorus size range=110880 mg) regulated
Tthx during short flights (
5 s) via
temperature-dependent changes in wing beat frequency. Further studies of
continuous flights, including measurements of wingbeat frequencies for the
smaller species (N. guttula, N. investigator) are warranted. Although
continuous flight data obtained for N. hybridus indicate that this
species is able to maintain a relatively constant Tthx
during longer flights, one caveat is that these results do not fully represent
actual flight conditions. Continuous flight data were taken from individuals
flying while supported by a thermocouple probe, and so the
Tthx measurements may not take into account effects of
generating lift and thrust that would occur in free flight. During free
flight, lift and thrust, in addition to heat generated from muscle
contractions, may increase Tthx during longer flights
above measurements of Tthx made in this study, especially
at low wind speeds where less heat is lost via forced convection
(Church, 1960
;
Casey, 1992
). Tethered flights
also do not allow an animal to carry out normal flight behavior and do not
consider the effects of solar radiation during flight
(Casey, 1992
). Field data
indicate that flight activity ceases when solar radiation is most intense
(Fig. 4), and
Te models confirm that activity during these times could
potentially be lethal, so wind speed and solar radiation may limit the degree
to which a beetle can regulate Tthx during actual flights
in the field.
Mechanisms for thermoregulation
Cooling and body size
Because of an inherently lower surface area to volume ratio, larger insects
should be able to regulate and maintain higher temperature excesses because
they cool more slowly and have a higher thermal inertia
(Bartholomew, 1981;
Stone and Willmer, 1989b
).
This is true for Nicrophorus and is evident in the marked difference
in mass and subsequent thermoregulatory ability between N. hybridus, N.
investigator and N. guttula. Similar results have been shown for
other beetles much larger than Nicrophorus (Bartholomew and Casey,
1977a
,b
;
Bartholomew and Heinrich, 1978
)
and for other insects such as desert robber flies
(Morgan and Shelly, 1988
),
where larger species were better thermoregulators.
Data from beetles cooling from flight or from artificial heating provide
evidence that larger beetles may be able to maintain elevated
Tthx longer after flight, which may confer a competitive
advantage once a carcass is located. Because of slower cooling rates, larger
beetles stay warmer longer, which may be one reason why larger beetles tend to
be more successful in competitive interactions
(Otronen, 1988;
Trumbo, 1990
). This would need
to be tested with a series of carcasses in the field, where body temperatures
of individuals arriving at the carcass and later competing for the carcass
were measured, as was done previously for dung beetles arriving at dung piles
(Bartholomew and Heinrich,
1978
). Controlled laboratory experiments in which an individual
beetle is warmed to a temperature that approximates an after-flight
Tthx and is then placed in an arena with a carcass and
other beetles (potential competitors) may be a way to approach this question.
The use of infrared thermocouples is an appealing, non-invasive approach for
obtaining field temperature measurements, allowing for more natural
behavior.
Insulation, wing loading and heat transfer
Wings, elytra and thoracic pile all played a role in slowing heat loss, and
beetles with both wings and elytra removed cooled significantly faster.
Removal of thoracic pile also resulted in faster cooling rates. Other studies
have reported that thoracic pile had no effect on the cooling rates of beetles
(Nicolson and Louw, 1980;
Morgan, 1987
;
Chown and Scholtz, 1993
), but
this does not seem to be the case in Nicrophorus as the cooling rates
of beetles with and without pubescence differed. A difference in cooling rates
with and without pubescence is also the case for desert locusts (Church,
1960b), where the insulating ability of the pubescence was dependent upon its
density, and potentially for Colias butterflies, where it was shown
that fur thickness increased with elevation
(Kingsolver, 1983
).
Nicrophorus species vary in the density of thoracic pile and the
actual area covered by the pile (M. J. Merrick and R. J. Smith, personal
observation). Studies to determine if this variation is related to a species'
thermoregulatory ability and distribution would be of great interest.
During flight, Nicrophorus flies with the elytra elevated and
wings extended. With these structures held away from the body, a beetle in
flight probably loses a great deal of endogenous heat by forced convection
(Church, 1960;
Casey, 1992
). Even without air
movement, beetles cooled significantly faster with wings and elytra removed,
which indicates that this is a substantial avenue for heat loss during
flight.
The ability to regulate body temperatures in flight requires that heat be
generated and maintained at cooler ambient air temperatures and dumped at
higher air temperatures. One mechanism for dumping excess heat is to shunt it
to the abdomen, where it dissipates faster because of the large surface area
of the abdomen and increased airflow and convection during fast flight
(Heinrich, 1993,
1996
). This mechanism of heat
transfer is common in large moths (Heinrich,
1993
,
1996
) but it has not been
observed in beetles (Chown and Scholtz,
1993
), Nicrophorus (present study), honeybees (which have
counter-current heat exchangers in the petiole;
Casey, 1992
) or in cicada
killer wasps (Coelho, 2001
).
Although there does not appear to be any physiological mechanism for control
of heat transfer to and from the abdomen, the fact that the abdomen of
Nicrophorus is significantly cooler than the thorax following short
flights means heat can be lost to the abdomen by simple diffusion of hemolymph
from the thorax to the abdomen. This is supported by the observation that
abdomens of living and dead beetles, shielded from a heat source, heated up at
the same rate. Because the abdomen is exposed during flight and contains large
spiracles along its margins, the opportunity for heat to be lost by forced
convection is great. This presents a problem for retaining heat during flights
at cooler temperatures if no mechanism (such as counter-current heat
exchangers) to prevent heat dissipation to the abdomen exists
(Casey, 1992
;
Heinrich, 1996
). Inability to
control heat loss to the abdomen in cooler temperatures may limit the ambient
temperatures at which flight is possible for Nicrophorus.
Higher wing loading increases the amount of heat produced as the flight
muscles do more work to beat faster and maintain lift. Wing loading increased
with body size in Nicrophorus, and wing loading and body mass were
also negatively correlated with the slope of Tthx against
Ta and the index of thermoregulatory performance,
indicating that better thermoregulators had higher wing loading and were
heavier in general. These results are consistent with those found for other
beetles (Oertli, 1989),
noctuid moths (Casey and Joos,
1983
) and bees (Stone and
Willmer, 1989b
; Bishop and
Armbruster, 1999
).
Another mechanism for thermoregulation that may be important in
Nicrophorus includes heat dissipation from the head. Studies on
thermal stability in honeybees (Roberts
and Harrison, 1999), desert carpenter bees
(Chappell, 1982
), dragonflies
(May, 1995
) and cicada killer
wasps (Coelho, 2001
) indicate
that cooling at high temperatures is facilitated by shunting warm hemolymph to
the head, where heat is then dissipated over either a large surface area as in
carpenter bees or via regurgitated fluid (see
Heinrich, 1996
, chapter 6 for
a review). This mechanism for cooling is a possibility for
Nicrophorus, as burying beetles regularly secrete fluid from the
mouth and anus. Because of these secretions, however, water balance becomes
important for burying beetles. Without access to water, beetles in captivity
quickly die (M. J. Merrick and R. J. Smith, personal observation), and
Nicrophorus are not common in hot, dry habitats.
Influence of thermal environment on activity patterns
Nicrophorus species found in southeastern Idaho are highly
influenced by the thermal environment they experience. Operative temperature
models can be used to gauge the thermal environment that an organism is
experiencing and how habitat features such as substrate, orientation and solar
radiation affect body temperatures. High operative temperatures corresponded
to times of inactivity for beetles in the field
(Fig. 4) and, given the wide
fluctuations in operative temperatures, it is clear that microhabitat choice
could influence the body temperature of an individual. Solar radiation is
likely to play a large role in limiting the activity of Nicrophorus
not only in flight but also in terrestrial activity. Nicrophorus
flies at a lower Tthx range (2038°C) than other
diurnal insects that can tolerate high heat loads, such as the hawkmoth
Macroglossum stellatarum
(Herrera, 1992;
Tthx range 3946°C) or cicada killers
(Sphecius speciosus; Coelho,
2001
; Tthx range 3742°C). Members
of Nicrophorus probably cannot tolerate high heat loads imposed by
flying at midday on warm, calm and clear summer days. On windy days, the
window of flight opportunity may widen, as high wind speeds and fast forward
flight increase convective heat loss
(Casey, 1992
). Beetles left on
the ground in direct sunlight quickly die (M. J. Merrick and R. J. Smith,
personal observation) and a pair of beetles tending to a carcass left on bare
soil (where Te rapidly approaches lethal temperatures
around 4546°C) will quickly work together to move the carcass under
vegetation (M. J. Merrick and R. J. Smith, personal observation).
Flight activity appears to be restricted to ambient temperatures between
approximately 14°C and 36°C, which would, at higher elevations,
restrict flight to primarily a diurnal activity. If thermal tolerances for
flight and terrestrial activity are determined for a species, one might be
able to predict areas where nocturnal flight is possible, based on the mean
nighttime temperature for a given habitat and the thermoregulatory abilities
of the species being studied. This information could also allow for predicting
where a species is distributed geographically (in latitude and elevation) and
what habitat types it might utilize. For example, Nicrophorus nigrita
is a burying beetle that occurs along the Pacific coast of North America but
lacks dorsal maculations on the elytra (i.e. it is completely black). Sikes
(1996) found that this beetle
is not active during the middle of the day and that it preferred to locate and
bury carcasses in "moist, cool, redwood-forested canyons". Perhaps
because of its dark pigmentation, this species cannot tolerate high incident
sunlight, or higher operative temperatures, leading one to predict that it
would live in a shady habitat or have crepuscular or nocturnal activity
patterns. Conversely, this species' black pigmentation may be selectively
advantageous for heating up faster in cooler environments.
Temperatures that are restrictive to flight are not necessarily restrictive to other activity, and temperatures restrictive to flight in one species may not restrict flight in another. In the present study, N. investigator flew over a wider range of ambient air temperatures than the other two species, and elevated Tthx on average 7.3°C above ambient. Since most of the N. investigator individuals documented in this study came from Colorado (higher elevations, cooler daily temperatures), this population may be able to tolerate a wider range of environmental temperatures. Beetles were also observed beneath carcasses and walking near them or in baited traps at night and at dawn (temperatures between 12°C and 15°C), with a mean Tthx excess of approximately 4.5°C.
Predictions of potential flight times for the three species (Fig. 5) show that the largest species (N. hybridus) and the species with the widest thermal tolerance (N. investigator) may be able to be active longer throughout the day compared with N. guttula. These predictions for activity times are based on the range of ambient temperatures recorded following each flight during flight trials but do not consider how well each species is able to regulate its body temperature during flights throughout the day. N. investigator may have the widest `window' of possible activity times but may not be able to fly for very long before it becomes too cool or too hot to maintain flight. By contrast, because N. hybridus can regulate its body temperature better, it may be able to fly for longer periods throughout the day. For a beetle that must fly in search of carcasses for food and reproduction, the capability for sustained flights might increase an individual's chances of finding the rare carcass resource and thus their subsequent fitness.
This study incorporates body temperature data, thermal profiles of various
microhabitats and actual observations of animal activity in the field to show
that (1) burying beetle activity is influenced by environmental temperatures,
(2) burying beetles have the ability to elevate thoracic temperatures prior to
flight and (3) thermoregulation during flight is influenced by body mass,
morphological features such as wing loading and insulation. We provide a
preliminary framework for predicting and testing hypotheses about burying
beetle activity times and distributions based on thermal tolerances and
thermoregulatory ability. Body size has been shown to influence competitive
outcomes (Otronen, 1988;
Trumbo, 1990
), speed of
carcass burial (Smith et. al.
2001
) and reproductive success
(Trumbo, 1990
) in burying
beetles and we show here that it also influences thermoregulatory ability,
which may help to further explain these observed relationships between body
size and fitness. We suggest that additional studies examining the
relationships between body size, morphology and thermoregulatory ability and
determining thermal tolerances and how these relate to distributions and
activity times among different species of burying beetles will advance our
current understanding of species distributions, niche partitioning among
sympatric species and the relationship between body size and reproductive
success.
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References |
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