Effect of food quality, distance and height on thoracic temperature in the stingless bee Melipona panamica
Division of Biological Sciences, Section of Ecology, Behavior, and Evolution, University of California San Diego, MC#0116, 9500 Gilman Drive, La Jolla, CA 92093-0116, USA
* Author for correspondence (e-mail: jnieh{at}ucsd.edu)
Accepted 14 August 2005
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Summary |
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Key words: thermoregulation, thoracic temperature, foraging, recruitment, meliponine, stingless bee, Melipona panamica
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Introduction |
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Several studies have found evidence for thoracic temperature regulation
during honeybee recruitment (Esch,
1960; Stabentheiner,
2001
; Stabentheiner and
Hagmüller, 1991
;
Waddington, 1990
). Honeybees
can regulate their body temperature according to food quality, exhibiting
higher thoracic temperatures after feeding at richer food sources
(Schmaranzer and Stabentheiner,
1988
; Underwood,
1991
). Thoracic temperature positively correlates with the quality
of the food as perceived by sweetness
(Stabentheiner and Hagmüller,
1991
), proximity to the nest
(Esch, 1960
;
Stabentheiner, 1996
) and
nectar flow rate (Farina and Wainselboim,
2001
). Moreover, thoracic temperatures are affected by the status
of the hive (amount of pollen and nectar stores) and are thus tuned to colony
need (Schulz et al., 1998
).
Mechanistically, honeybee thoracic temperature is tied to metabolic
expenditure, which increases with increasing sugar concentration and nectar
flow rate (Moffatt and Nunez,
1997
), and perhaps with forager motivational state
(Balderrama et al., 1992
).
Honeybee thoracic temperature is tied to the thermal stability and the ability
to generate high mechanical power output in flight
(Dudley, 2000
;
Woods et al., 2005
).
To date, no studies have examined whether stingless bees have similar thermal abilities. We therefore hypothesized that food profitability to the colony would significantly affect the temperatures of recruiting meliponine foragers at the feeder and inside the nest.
What little is known about meliponine thermoregulation largely concerns the
regulation of nest temperatures, not individual thermoregulation
(Kerr and Laidlaw, 1956;
Kerr et al., 1967
;
Michener, 1974
;
Roubik, 1989
;
Wille, 1976
;
Zucchi and Sakagami, 1972
).
Preserving sufficiently high brood temperatures is vital, and temperatures can
drop daily and seasonally to suboptimal levels (below 2836°C) for
maintaining brood even in the tropical and semi-tropical regions inhabited by
stingless bees (Engels et al.,
1995
; Roubik and Peralta,
1983
). Meliponine nest thermoregulation is thus widespread. Zucchi
and Sakagami (1972
) measured
elevated brood temperatures relative to other portions of the nest in several
species (Trigona spinipes, Leurotrigona mulleri, Frieseomelitta varia,
Plebeia droryana, Scaptotrigona depilis, M. quadrifasciata anthidiodes
and M. rufiventris; species names as listed by authors). In S.
postica depilis, nest temperatures were also largely independent of
external temperatures (Rosenkranz et al.,
1987
). Roubik and Peralta
(1983
) propose that the brood
area acts as a central heat source for the nest, with immature bees supplying
the majority of heat and dissipating excess through fanning. Temperatures
within the brood area were on average 23°C higher than the region
immediately outside the involucrum, a resin and wax structure covering the
brood area.
Stingless bees can thermoregulate by modifying their nests and generating
heat. Scaptotrigona postica foragers close their entrance funnel
during cold weather (Engels et al.,
1995). Meliponines can also thicken the nest walls to improve
insulation. Engels et al.
(1995
) observed workers
gathering cerumen particles to plaster the glass covering an observation nest
at the low temperature of 15°C. Interestingly, no evidence has been found
that stingless bees use evaporative cooling
(Fletcher and Crewe, 1981
;
Roubik and Peralta, 1983
), a
strategy used by honeybees (Lindauer,
1954
) and wasps (Coelho and
Ross, 1996
). Ventilation appears to be the preferred strategy
(Fletcher and Crewe, 1981
;
Roubik and Peralta, 1983
;
Zucchi and Sakagami, 1972
) and
may be sufficient to cool colonies under most circumstances, given the
well-insulated nest structure (Engels et
al., 1995
; Rosenkranz et al.,
1987
). Ground-nesting African species, Trigona denoiti
and T. gribodoi, decreased phases of inspiration and expiration in
the night when temperatures decreased
(Moritz and Crewe, 1988
) and
Dactylurina staudingeri, opens nest pores with higher temperatures
during the day and closes them during the colder night
(Darchen, 1973
).
In addition to nest modification, bees actively generate heat. Physical
activity can increase meliponine body temperature. Using an infrared
thermometer, de Lourdes and Kerr
(1989) reported that
Melipona compressipes fasciculata workers had elevated thorax
temperatures (1.03.4°C higher) while working as compared to
resting. Trigona (Plebeina) denoiti workers
increased brood area temperatures when the external temperature was dropped
from 31°C to 15.4°C (Fletcher and
Crewe, 1981
). Such thermoregulation demonstrates that many
meliponines can actively modulate their body temperature by generating heat.
This raises the possibility that stingless bee and honeybee foragers share an
ability to regulate their thoracic temperatures with respect to net food
profitability (caloric intake minus caloric expenditure). Thus, the goal of
our study was to determine whether the temperatures of recruiting meliponine
foragers could be affected by sucrose concentration and location.
We focused on a species, Melipona panamica (previously known as
M. eburnea and M. fasciata; D. W. Roubik, personal
communication; Roubik, 1992),
whose foraging recruitment system has been fairly well studied and is known to
specify the three-dimensional location of good food sources to nestmates
(Nieh,
1998a
,b
;
Nieh and Roubik, 1995
,
1998
). Like honeybees,
stingless bees can use optic flow to measure foraging distances
(Esch et al., 2001
;
Hrncir et al., 2003
). Using
mark and recapture studies, Roubik and Aluja
(1983
) estimated the maximum
flight range of this species to be 1.72.1 km on Barro Colorado Island,
Panama. Foragers are intermediate in size for the genus Melipona,
being approximately 1 cm in length, with an average wingspan of 8 mm and an
average unloaded mass of 0.06 g. Roubik and Buchmann
(1984
) report that the average
food load for M. panamica foraging at a 45% sugar solution was
46.2±6.7 µg (sucrose solution density calculated for 29°C;
Bubnik et al., 1995
). Sugar
concentrations of floral nectar loads ranged from 21% to 60% in M.
panamica, and foragers were able to collect even relatively high
viscosity sucrose solutions (70%), performing better at this task than several
other Melipona species (Roubik
and Buchmann, 1984
).
We performed four experiments. The first examined overall body temperature changes in response to sucrose concentration at the feeder and in the nest. The second examined the effect of sucrose concentration on thoracic temperature in detail, and the third and fourth examined the effect of food location (feeder distance and height) on thoracic temperature.
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Materials and methods |
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Feeders and training
We trained individually marked M. panamica foragers to a
grooved-plate feeder (Nieh et al.,
2003) containing a scented sucrose solution (100 µl anise
extract/liter solution; McCormick & Co. Inc., Hunt Valley, MD, USA). Bees
were trained using an anise-scented 0.5 mol l1 sucrose
solution to which they did not recruit. During the experiments, we used
sucrose solutions ranging in concentration from 1.02.5 mol
l1 (von Frisch,
1967
) mounted on a 1 m high tripod. We marked each visiting bee
with an individual combination of paint marks on the distal tip of the
abdomen. At the beginning of experiments on each day, we used the first marked
foragers to arrive (Nieh et al.,
2003
). Foragers were trained to feeder locations south of the
nest, including the 40 m high Lutz canopy tower
(Nieh and Roubik, 1995
)
located 437 m from the nest. All recruited nestmates were captured in
aspirators until the end of each experimental day
(Nieh et al., 2003
), marked on
the abdomen, and then released. The identity of all foragers was verified by
viewing their return to the colony entrance (E and F) or inside the colony
(D). Each day, we used a different set of foragers that had been recruited and
verified on the previous days. Foragers were counted each 15 min and excess
foragers were captured in aspirators and released at the end of the day. Germ
et al. (1997
) recommends that
honeybee thermal studies be avoided in the early morning or later afternoon to
reduce daily climactic variability. Sunrise and sunset times at our field site
were approximately 06:00 h and 18:30 h, respectively, throughout our field
seasons, and we typically conducted experiments between 10:00 h and 15:00 h.
All feeders were kept in the shade, as is normal for foraging in the forest
understory. On a few days, rain limited data acquisition.
Temperature measurements
We measured the temperature of the thorax (Tth), the
ambient air temperature at the feeder (Ta), and the
ambient air temperature inside the nest (Tnest). To
determine thermal conspicuousness, we calculated the difference between the
thorax temperature and the ambient air temperature at the feeder
(Ta; Stone,
1993b
) and inside the nest (
Tnest). We
also calculated
Tctrl, the difference between the
temperature of the trained forager and a randomly chosen bee within 5 cm of
the trained forager. For controls, we only chose bees that were not actively
foraging or engaging in trophallaxis while we measured trained forager
Tth.
We used infrared thermography to measure forager temperatures (method of
Stabentheiner and Schmaranzer,
1987). To measure forager temperatures on the feeder, we recorded
bee temperatures 10 s after they had begun feeding on the feeder or 10 s after
they had returned to the nest. During our observations, all foragers found
nestmates to unload their food to within 10 s. From June through July 2003, we
used a Raytek PhotoTemp MX6 (close-focus model, supplier FLW Inc., San Diego,
California, USA) photographic infrared (IR) thermometer equipped with True
Spot laser sighting to precisely delineate the measured area (spot measurement
size adjustable to the diameter of a M. panamica thorax). From
November through December 2003, we used a Raytek ThermoView Ti30 infrared
imager (FLW Inc.). PhotoTemp MX6 values were directly entered into a Macintosh
iBook computer (supplier UCSD Bookstore, La Jolla, CA, USA) running Microsoft
Excel v.X, and ThermoView Ti30 images were downloaded onto a Sony Vaio laptop
PCGTR1A
(Amazon.com,
USA), running InsideIR v2.0.2. Each time we made a thermographic measurement,
we measured air temperature inside the nest (Tnest) or at
the feeder (Ta) using a Mastech MAS-345 meter (100 cm long
type K thermocouple, copperconstantan, 0.3 mm diameter;
Amazon.com,
USA) placed 1 cm above the nest or feeder substrate and within 4 cm of the
returning foragers. Thermocouple air temperature measurements were highly
stable.
Calibrations
To calibrate our IR sensors, we waited until the internal and external
surface temperatures of a dead bee had equilibrated, inserted a type K
thermocouple into the bee, and then recorded its dorsal thoracic IR
temperature through IR transparent plastic film (BCU Plastics, San Diego, CA,
USA; Polyolefin FDA grade 75 gauge film, catalog #LS-2475; protocol of
Stabentheiner and Hagmüller,
1991). This film is optically transparent, reduced disturbances to
the nest, and facilitates more normal colony thermoregulation. Equipment
emissivity values were then adjusted until both thermocouple and infrared
temperature readings matched. Comparisons of calibrated readings from the
PhotoTemp MX6 and the ThermoView Ti30 showed no differences in the
temperatures measured by these two devices to the limit of equipment readings
(0.1°C). Both sensors were highly stable and, although tested at a variety
of different temperature and humidity levels in the field and in the lab at
the beginning and end of the experiment, exhibited no need for
recalibration.
Experiment 1: Individual thermal profiles
At 11:00 h on 4 days (over 2 weeks), we randomly selected five individuals
from colony D and recorded their temperatures at the feeder and in the nest
for a period of 1 h usingthermographic scans. The feeder was placed 276 m
south of the nest and 1 m above the ground. The same individuals were recorded
at the feeder and the nest during consecutive 1 h intervals (with a break of
15 min to allow equipment transport). We then switched to a different sucrose
concentration and repeated the procedure. The order of low and high sucrose
concentration presentation and the order of first recording at the feeder or
in the nest were alternated each day to control for potential time effects and
new individuals were chosen each day. Ambient air temperatures were measured
as previously described. We used InsideIR v2.0.2 software to measure the
longitudinal thermal profile along the forager's midline, calculating the
average temperature of each body part (head, thorax, abdomen) for statistical
comparisons.
Experiment 2: Effect of sucrose concentration on thoracic temperature at the food source
We examined the effect of sucrose concentration in detail at a feeder
placed 20 m south of the nests, using seven trained foragers per day (6 total
trials, one trial per day). We used all seven sucrose concentrations
(presented in random order) on each day and a new set of foragers each day. We
consecutively used all three colonies in this experiment (four trials per
colony), measuring thoracic temperatures on the feeder with the PhotoTemp
MX6.
Experiment 3: Effect of distance and sucrose concentration on intranidal thoracic temperature
We trained foragers from colony D to feeders placed 25 m, 50 m, 100 m, 150
m, 276 m and 437 m south of the nest over a period of 31 days. Depending on
weather conditions (frequency and duration of rain), we were able to train the
same set of bees to three or four different locations per day. Each day, we
used a new set of five foragers. We measured forager temperatures inside the
nest with the ThermoView Ti30 and report the thoracic temperature.
Experiment 4: Effect of height on intranidal thoracic temperature
We trained foragers from colony D to either the base (1 m high) or the top
(41 m high) of the Lutz canopy tower. We used a different set of five foragers
per trial and conducted one trial per day for a total of 15 trials at the
tower top and seven at the base (fewer trials due to rain). We did not use the
lower 1.0 mol l1 sucrose concentration in this experiment
because the bees would not feed at the 437 m feeder for such a low
concentration, a common effect encountered when using distant feeders
(Jarau et al., 2000;
Nieh, 2004
).
Statistical analyses
We used JMP IN v4.0.4 software for multiple regression, ANOVA,
t-tests and TukeyKramer HSD tests for pairwise comparisons
(Wilkinson, 1996;
Zar, 1984
). We used Statview
v5.0.1 to conduct Sign tests, presenting the results as the ratio of the
number of observations greater than zero to the number of observations less
than zero. Where appropriate, we applied the sequential Bonferroni correction
(Zar, 1984
). Averages are
presented as mean ± 1 S.D.
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Results |
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Experiment 1: Individual thermal profiles
Thermograms reveal that foragers can be much hotter than either the
background (Fig. 1) or other
bees inside the nest (Fig. 1B). As Fig. 2 shows, foragers are
hotter at the head and thorax than at the abdomen, at higher ambient air
temperatures, for 2.5 mol l1 than for 1.0 mol
l1, and at the feeder than in the nest. These four factors
(in order of decreasing effect: body section, air temperature, sucrose
concentration and measurement location) play a significant role in forager
temperatures at the feeder and in the nest. Forager identity (bee no.) has no
significant (NS) effect (ANOVA overall model
F6,233=335.6.1, P<0.0001,
r2=0.90; body section: F2,233=189.3,
P<0.0001; sucrose concentration: F1,233=52.6,
P<0.0001; air temperature: F1,233=128.1,
P<0.0001; measurement location: F1,233=39.6,
P<0.0001; bee no.: F1,233=0.7,
P=0.40; interactions NS). The effect of measurement location is not
surprising given the cooler temperatures inside the nest.
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At both sucrose concentrations and locations, there are significant
differences between the temperatures of different body sections (ANOVA:
F2,5722.3, P<0.0001, interactions NS). The
thorax is hotter than the head and the abdomen in all pairwise comparisons
under all conditions (TukeyKramer HSD, q*=2.5062,
P<0.05). The head is significantly cooler than the thorax and
hotter than the abdomen in all pairwise comparisons in all conditions
(TukeyKramer HSD, q*=2.5062, P<0.05) except when
measured in the nest after returning from 1.0 mol l1 sucrose
solution (no difference between head and abdomen; TukeyKramer HSD,
q*=2.5062, NS). Comparing the distal (painted) tip of the abdomen
with the proximal end of the abdomen reveals no significant difference
(t-test, t79=0.207, P=0.84). Each body
section was 32.2±1.1°C (thorax), 30.1±0.7°C (head) and
29.2±0.7°C (abdomen, N=20) while the bee was on the
feeder.
We therefore focused on thoracic temperatures. There is a significant effect of ambient air temperature on thoracic temperature at the feeder (ANOVA: F1,497=61.1, P<0.0001) and inside the nest (ANOVA: F1,2628=962.2, P<0.0001, Fig. 3).
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(2) Sucrose concentration has a significant positive effect on
Ta (ANOVA: F1,496=253.6,
P<0.0001, r2=0.21). This corresponds to a rise
of 1.4°C in
Ta per 1 mol l1
increase in sucrose concentration at the food source
(Fig. 4). Sucrose concentration
explains 80% of the variance in average
Ta.
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(2) Both distance and sucrose have significant positive effects on
Tnest (ANOVA: overall model,
F2,2146=170.4, P<0.0001,
r2=0.14, sequential Bonferroni correction applied) with
each factor significant (ANOVA: distance, F1,2146=340.8,
P<0.0001; sucrose concentration, F1,2146=11.2,
P<0.0001, interaction NS and thus two-factor model used,
sequential Bonferroni correction applied). Model fit yields a decrease of
0.4°C in
Tnest with each 100 m of distance and
an increase of 0.1°C per 1 mol l1 increase in sucrose
concentration (Fig. 5). The
effect of distance on
Tnest is approximately 30
times greater than that of sucrose concentration. Sucrose concentration
explains 86% of the variance in average
Tnest.
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A closer examination of Fig.
5 suggests a steeper drop in Tnest at distances
greater than 150 m. We therefore divided this data into two sets, 25100
m and 150437 m, focusing upon the 2.5 mol l1 data
because this was collected for the largest range of distances. At the short
distances (25100 m), there is a very slight, but significant negative
correlation between distance and
Tnest (linear
regression, r2=0.04, slope=0.008,
F1,589=26.3, P<0.0001, sequential Bonferroni
correction applied). At greater distances (150437 m), there is also a
significant but slight negative correlation between distance and
Tnest (linear regression,
r2=0.27, slope=0.006,
F1,558=203.1, P<0.0001, sequential Bonferroni
correction applied). The slopes are small for both distance ranges, but
distance accounts for a far larger portion of the variance in
Tnest at the greater distances. This is perhaps not
surprising given that the distance range spanned by the greater distances
(
287 m) is 3.8 times larger than the distance range spanned by the
short distances (
75 m).
(3) With respect to thermal conspicuousness inside the nest, foragers were
individually hotter than the ambient air temperature in the nest
(Tnest) at all sucrose concentrations and distances
(see effect of distance and sucrose on
Tnest in
previous analysis). At distances up to 150 m from the nest,
(
Tnest=5.1±1.2°C, N=789 for 2.5
mol l1 sucrose solution and
Tnest=4.8±1.4°C, N=787 for 1.0
mol l1sucrose solution) and thus there was a slight
difference between
Tnest at the different sucrose
concentrations up to 150 m (ANOVA F1,1574=15.8,
P<0.0001). When the feeder was placed 276 m from the nest, there
was no difference between the average
Tnest at the
different sucrose concentrations (Fig.
5A,
Tnest=4.0°C at both
concentrations).
On average, trained foragers were slightly but significantly hotter than
the control bees at distances close to the nest
(Table 3). Overall, there was
high variance in Tctrl, with maximum positive and
negative differences of 11.2°C and 7.2°C, respectively (taken
from all distances at both sucrose concentrations). At 2.5 mol
l1 sucrose solution, there were significant differences up
to 100 m, but at 1.0 mol l1 sucrose solution the only
significant difference was at 50 m. There was no significant effect of sucrose
concentration on
Tctrl at distances up to 150 m
(ANOVA F1,1574=0.23, P=0.63). The potential trend
of decreasing
Tctrl with increasing distance did
not hold for the base of the canopy tower, located 437 m from the nest
(Table 3).
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Experiment 4: Effect of food height on intranidal thoracic temperature
(1) There is no significant effect of feeder height above the ground on
intranidal thoracic temperature. In the overall model, only nest air
temperature (Tnest) is a significant factor (ANOVA:
overall model, F2,521=304.9, P<0.0001; effect
tests: Tnest, F1,521=569.8,
P<0.0001; height above ground, F1,521=0.1,
P=0.70, interactions NS and thus two-factor model used). (2) There is
also no significant effect of height on Tnest
(ANOVA, F1,629=2.0, P=0.12,
r2=0.003). (3) However, foragers returning from both the
top and the base of the forest canopy were significantly hotter than the
ambient air temperature (Tnest; P<0.0001) and
as compared to control bees inside the nest (P
0.01,
Table 3).
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Discussion |
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Effect of ambient air temperature
As expected for a heterotherm, ambient air temperature had a significant
effect upon forager body temperature at the feeder and inside the nest (Figs
2 and
3), as it does in honeybees
(Schmaranzer and Stabentheiner,
1988), bumblebees (Heinrich,
1993
) and wasps (Kovac and
Stabentheiner, 1999
). The relationship between forager thorax
temperature (Tth) and Tair is
approximately linear in the range of air temperatures that occurred during our
experiments (21.529.5°C; Fig.
3). It is possible that M. panamica foragers regulate
relatively lower and more stable Tth at higher air
temperatures, as suggested by the slight reduction in Tth
values below the regression line at Ta>28°C
(Fig. 3). Further studies at
higher Ta are needed to clarify this point.
Sucrose effect
In general, floral nectars contain from 5% to 80% sugar
(Baker and Baker, 1983),
corresponding to a range of 0.15 mol l1 to 2.3 mol
l1 sucrose concentration
(Bubnik et al., 1995
). Roubik
and Buchmann (1984
) report
that sucrose concentrations of nectar collected by four species of
Melipona in central Panama during the dry season (including M.
panamica colonies studied on Barro Colorado Island) ranged from 0.6 mol
l1 (21%) to 1.8 mol l1 (60%). We used
sucrose concentrations ranging from 1.0 mol l1 to 2.5 mol
l1, with 1.0 mol l1 as the lowest
concentration for which bees reliably foraged up to 276 m from the nest. Due
to competition from natural food sources, relatively high sucrose
concentrations are required to elicit consistent foraging at artificial
feeders, even during periods of relative food dearth
(Nieh, 2004
).
Although we focused on thoracic temperature measurements, it is clear that
foraging at higher sucrose concentrations resulted in elevated thoracic, head
and abdominal temperatures at the feeder and inside the nest
(Fig. 2). With regards to
measurement technique, painting surfaces for improved thermographic
measurements is a standard practice (Wolfe
and Zissis, 1985), and the thin layer of paint applied to the
distal tip of the abdomen did not interfere with temperature measurements (no
significant temperature differences between painted and unpainted abdominal
sections). At the feeder, forager thoracic temperatures were on average higher
by 2.1°C than the head and by 3.0°C than the abdomen. Higher thorax
temperatures relative to the head and abdomen are reported for M.
compressipes fasciculata (de Lourdes
and Kerr, 1989
), foraging honeybees
(Schmaranzer and Stabentheiner,
1988
), bumblebees (Heinrich,
1993
) and wasps (Kovac and
Stabentheiner, 1999
) and are thus common, if not universal, in
flying heterothermic insects (Heinrich,
1993
).
Melipona panamica foragers likely shiver their thoracic flight
muscles to regulate temperature (Fig.
2). Respiratory metabolism (oxygen consumption) increased with
temperature in the meliponines Scaptotrigona postica
(Silva, 1981), T. a.
fiebrigi and T. a. angustula
(Proni and Hebling, 1996
).
Recently, Hrncir et al. (2004
)
have shown that thoracic vibrations produced by recruiting M.
seminigra foragers increase in duration with increasing food quality.
Such vibrations may also have an effect upon thoracic temperature. The
mechanism of heat production has not been elucidated in stingless bees, but in
all endothermic insects investigated, muscle warm-up occurs through
contractions of opposing sets of thoracic flight muscles (shivering) or
via substrate cycling of a pair of enzymes
(Newsholme and Crabtree, 1973
;
Stone and Willmer, 1989
). In
bumblebees and honeybees, close relatives of stingless bees
(Cameron and Mardulyn, 2001
),
contractions of thoracic flight muscles, particularly the dorsoventral muscle
fibers, were most associated with flight warm-up
(Esch and Goller, 1991
).
Location effect
There is no significant effect of height on Tth inside
the nest. However, we found a significant effect of distance on
Tth that is 2030 times greater than that of sucrose
concentration. Thus Tth decreases rapidly with increasing
distance of the food source from the nest. A similar result is reported for
honeybees (Stabentheiner,
2001). At distances greater than 150 m (the maximum distance at
which a significant difference was found between 1.0 mol l1
and 2.5 mol l1 sucrose source), there is evidently little
effect of sucrose concentration on M. panamica
Tth (Fig.
5A). The flight range of M. panamica on Barro Colorado
Island, Panama, is approximately 2.12.4 km
(Roubik and Aluja, 1983
).
Conspicuousness and potential signalling
In honeybees, it remains unclear whether thoracic temperature regulation
acts as signal. Germ et al.
(1997) reported finding no
correlation between honeybee recruitment rates and dancing temperature and
thus concluded that thermal information was unlikely to be a primary source of
information about food quality. Seeley and Towne
(1992
) found no evidence that
recruiters dancing for a better food source attracted more dance followers
than those dancing for a poorer food source. Moreover, the variation in
temperature can be quite significant, particularly given the ambient
temperature, and even for a fixed food quality in honeybees
(Schmaranzer and Stabentheiner,
1988
).
Stingless bees can detect changes in nest temperature, as shown by the
heating experiments of Engels et al.
(1995) and observations of
foragers closing and opening nest pores in response to changing air
temperatures (Darchen, 1973
).
The thermal sensitivity of stingless bees has not been measured, but may be
similar to that of honeybees, which is approximately 0.25°C (true
sensitivity may be higher; Heran,
1952
). Our foragers were hotter than nest air temperatures in the
food unloading area at all distances tested. All foragers, whether returning
from 2.5 mol l1 or 1.0 mol l1 food, were
hotter than ambient air temperatures (Fig.
5A). However, evidence for their thermal conspicuousness relative
to control bees was limited (average
Tctrl no
greater than 0.7°C and then only for distances close to the nest, <150
m). At 150 m and 276 m,
Tctrl was negative
(Table 3). There is high
variance in
Tctrl (average of 0.1±2°C),
as expected given that bees were randomly chosen. This may account for the
higher than expected
Tctrl at 437 m. Control bees,
although inactive foragers at the time of temperature measurement, may have
just completed foraging at good natural food sources during those trials.
Thus, we found thermal differences based upon the net food quality (Figs
4 and
5), but these differences seem
unlikely to play a signaling role given their low level of conspicuousness.
Based upon these data, M. panamica forager temperature would only
provide information about recruiter proximity if nestmates were quite
sensitive to small differences in temperature, and then only for high quality
food sources close to the nest.
The phenomenon of increasing thoracic temperature with increasing sucrose
concentration is thus widespread among the Hymenoptera. For example, the wasp
Paravespula vulgaris also exhibits significantly higher thorax
temperature for higher sucrose solution concentrations
(Kovac and Stabentheiner,
1999). This ability may be linked to flight physiology, because
the large flight muscles can serve as excellent heat generators through
shivering thermogenesis and because these muscles must attain a minimum
temperature to achieve flight (Coelho,
1991
; Dudley,
2000
; Esch and Goller,
1991
; Harrison and Fewell,
2002
; Woods et al.,
2005
). Thus, one function of increasing thoracic temperature may
be to maintain readiness for high mechanical power production in immediate
take-off. We therefore predict that all members of the Apidae will exhibit a
similar response of increased thoracic temperature when feeding at
increasingly concentrated sucrose solutions.
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Acknowledgments |
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References |
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