Skip to main content
NCBI home page
UKPMC Funders Author Manuscripts logoLink to UKPMC Funders Author Manuscripts
. Author manuscript; available in PMC: 2011 Dec 1.
Published in final edited form as: J Insect Physiol. 2009 Jul 18;55(10):959–966. doi: 10.1016/j.jinsphys.2009.06.012

Thermoregulation of water foraging wasps (Vespula vulgaris and Polistes dominulus)

Helmut Kovac 1,*, Anton Stabentheiner 1,*, Sigurd Schmaranzer 1
PMCID: PMC3227726  EMSID: UKMS32697  PMID: 19589341

Abstract

A comparison of the thermoregulation of water foraging wasps (Vespula vulgaris, Polistes dominulus) under special consideration of ambient temperature and solar radiation was conducted. The body surface temperature of living and dead wasps was measured by infrared thermography under natural conditions in their environment without disturbing the insects’ behaviour. The body temperature of both of them was positively correlated with Ta and solar radiation. At moderate Ta (22–28 °C) the regression lines revealed mean thorax temperatures (Tth) of 35.5–37.5 °C in Vespula, and of 28.6–33.7 °C in Polistes. At high Ta (30–39 °C) Tth was 37.2–40.6 °C in Vespula and 37.0–40.8 °C in Polistes. The thorax temperature excess (Tth–Ta) increased at moderate Ta by 1.9 °C (Vespula) and 4.4 °C (Polistes) per kW−1 m−2. At high Ta it increased by 4.0 °C per kW−1 m−2 in both wasps. A comparison of the living water foraging Vespula and Polistes with dead wasps revealed a great difference in their thermoregulatory behaviour. At moderate Ta (22–28 °C) Vespula exhibited distinct endothermy in contrast to Polistes, which showed only a weak endothermic activity. At high Ta (30–39 °C) Vespula reduced their active heat production, and Polistes were always ectothermic. Both species exhibited an increasing cooling effort with increasing insolation and ambient temperature.

Keywords: Wasp, Thermoregulation, Foraging, Thermography, Water

1. Introduction

The capability of endothermic heat production by means of the thoracic flight muscles has been developed by several insect groups. Flying insects with the ability to elevate their thorax temperature above ambient air temperature can forage with some independence of the thermal environment (Heinrich and Heinrich, 1983). During resource collection, foraging endothermic insects have high energetic costs because flight muscles must achieve a minimum threshold temperature (e.g. Heinrich, 1979; Harrison and Hall, 1993; Harrison et al., 1996; Coelho and Ross, 1996; Kovac and Schmaranzer, 1996; Woods et al., 2005). The foraging strategies of social insects balance the energy expenditure of individual foragers with the net energetic gains to the colony (Seeley et al., 1991). For example, the value of carbohydrates (sucrose concentration) influences foraging behaviour and thermoregulation of bees and wasps. The foragers can minimize thermoregulatory costs during foraging by varying their thorax temperature in response to the carbohydrate content of the food source (Dyer and Seeley, 1987; Schmaranzer and Stabentheiner, 1988; Waddington, 1990; Stabentheiner and Hagmüller, 1991; Underwood, 1991; Kovac and Stabentheiner, 1999; Stabentheiner, 2001; Nieh and Sanchez, 2005; Nieh et al., 2006). Water collection does not provide a gain in energy. At first sight there is just energy expenditure. However, it is nevertheless essential for the survival of the colonies during heat stress. Wasps use water in conjunction with wing fanning for evaporative cooling of the nest (Steiner, 1930; Weyrauch, 1936; Akre, 1982; Greene, 1991) and in this way prevent overheating of the nest that could result in damage to the brood. In addition, they need water for providing their larvae or for processing plant fibre material for nest construction (Jeanne, 1996).

Variation in ambient air temperature can greatly affect the energy expended by foragers to maintain their flight threshold temperature. Thus, some wasps and bees alter their metabolic or activity rates to respond to changes in ambient temperature (Heinrich, 1993). The ability to regulate above ambient temperature and maintain a positive relationship between ambient and body temperature is a form of thermoregulation (Coelho and Ross, 1996).

Beside the ambient air temperature the influence of solar radiation on insect thermoregulation is not negligible. The effect of solar radiation on body temperature has been investigated in the Western honeybee (Heinrich, 1979) and Indian honeybees (Underwood, 1991) and in wasps of the subfamily Vespinae in a small range of ambient temperatures (Stabentheiner et al., 2004). These measurements showed that part of the heat gained from the sun is used to increase the insects’ thorax temperature. Foragers can minimize the thermoregulatory costs and nevertheless keep flight muscle temperature at a high level.

Concerning Central European wasps (Vespidae) two different strategies of individual thermoregulation seem to exist. The members of the subfamily Vespinae are known to have thermoregulatory abilities comparable to those of the honeybee. They are capable of intense endothermy and modulate their body temperature during food collection. They use this ability to keep their body temperature well above the ambient level to increase foraging efficiency (Heinrich, 1984; Stabentheiner and Schmaranzer, 1987; Kovac and Stabentheiner, 1993, 1999; Coelho and Ross, 1996; Eckles et al., 2008) and to regulate the temperature of their nests (Himmer, 1932; Ishay and Ruttner, 1971; Ishay, 1973; Gibo et al., 1974; Makino and Yamane, 1980; Martin, 1988; Klingner et al., 2005; Klingner et al., 2006). In contrast to the Vespinae, very little is known about the individual thermoregulation of the Polistinae. Preliminary measurements suggested that they are not or only weakly endothermic during their foraging trips on natural food sources (Kovac and Stabentheiner, 2001). Water foraging Polistinae have not yet been investigated. The purpose of this study was to give a comprehensive comparison of the thermoregulatory behaviour of Vespinae and Polistinae during water foraging, with special consideration of the influence of the environmental factors ambient air temperature and solar radiation.

2. Materials and methods

2.1. Animals, field site and measuring conditions

Measuring location was an orchard on a farm in Gschwendt/Austria, middle Europe. On 5 days in 2 different years we investigated wasps (Vespula vulgaris and Polistes dominulus) foraging water on a rainwater barrel. In order not to impair their behaviour during foraging we refrained from marking the individuals. We presume at least about 15–20 water collecting individuals of Vespula and about 5–10 individuals of Polistes to be included in this study. One of the measuring days in August 2003 was one of the hottest days of the year, with ambient air temperatures (Ta) above 30 °C (~30–40 °C). On the other days we had moderate temperatures in the range of ~20–30 °C. In addition to water foragers, Polistine wasps foraging nectar on raspberry and gathering sap on rhubarb, and another Vespine wasp, Dolichovespula saxonica, also foraging nectar on raspberry blossoms were measured for comparison.

2.2. Measurements

The wasps were filmed during their complete foraging stay at the water barrel with an infrared camera (ThermaCam SC2000 NTS, FLIR) without disturbing them. The infrared camera was calibrated periodical by slotting in a self-constructed peltier driven reference source or an AGA1010 reference radiator of known temperature and emissivity (for details of calibration see Stabentheiner and Schmaranzer, 1987; Schmaranzer and Stabentheiner, 1988). Thermographic data were stored digitally with 14 bit resolution on a portable computer (DOLCH Flexpac-400-XG) at a rate of 3–5 frames s−1. Dolichovespula and Polistes foraging nectar and plant sap were measured solely in the shade at a rate of 25 frames s−1 because the infrared camera AGA 782 SW, which we used at that time, was not appropriate for measurements in the sunshine.

To take into consideration the effects of ambient air temperature, solar radiation and air convection on the measurement site, we determined the insects’ operative (environmental) temperature (Te; Bakken, 1976, 1980, 1992; Bishop and Armbruster, 1999). Freshly killed dead wasps (Vespula and Polistes) were fixed with needles on their wings about 1 cm above a wooden board beside the foraging wasps and measured simultaneously with them. During the measurements there were only a few foraging Polistes at the barrel, thus we did not catch and kill any for estimating the Te. We fetched these measurements of the Te at a later time with two individuals of Polistes in comparison with two Vespula to compensate for possible differences of air convection and other micro climatic effects between measurement days (Fig. 1B).

Fig. 1.

Fig. 1

Open in a new tab

Thermograms of living wasps (A) and dead wasps fixed with needles (B) beside the foraging site of the wasps (top: Polistes, bottom: Vespula). (A) At an ambient temperature of 36.1 °C the body surface temperature of the water foraging Vespula on the left was Tthorax = 41.5, Thead = 38.8, Tabdomen = 38.6 °C, and of the Polistes on the right was Tthorax = 39.7, Thead = 36.7, Tabdomen = 38.8 °C. (B) Body temperature of dead Polistes on top left: Tthorax = 29.5, Thead = 26.1, Tabdomen = 27.6 °C; top right: Tthorax = 29.0, Thead = 27.0, Tabdomen = 26.6 °C; dead Vespula on bottom left: Tthorax = 30.9, Thead = 29.3, Tabdomen = 29.3 °C; bottom right: Tthorax = 29.8, Thead = 28.5, Tabdomen = 26.1 °C at an ambient temperature of 21.6 °C. Left-hand rectangle: reference radiator; between wasps: thermocouples for measurement of Ta (their warming by sunlight was compensated for by special calibrations).

The ambient air temperature (Ta) was measured near the foraging and dead wasps with NTC-sensors or thermocouples. The solar radiation was measured with a Dirmhirn-global radiation-pyranometer (range: 0.3–3.3 μm; NP-42, NEO Inc.) or with a global radiation sensor (FLA613-GS mini spezial, AHLBORN) in the immediate vicinity of the insects. The temperature and radiation data were stored every 2 s with ALMEMO data loggers (AHLBORN). During body temperature calculation from the infrared thermograms they were automatically extracted from the logger files.

2.3. Data evaluation and statistics

The temperature of the three body parts, and of the water surface (in close vicinity to the spot where the wasps’ mouthparts were in contact with the wet substrate), was calculated from the infrared thermograms by means of the AGEMA Research software (FLIR) controlled by a self written Excel VBA-macro (Microsoft Corporation). Values of the body temperature during foraging were taken in regular intervals of about 3 s immediately after the landing of the insects until they took off. The surface temperatures of head (Thd), thorax (Tth) and abdomen (Tab) were calculated with an infrared emissivity of 0.97, determined for the honeybee cuticle (Stabentheiner and Schmaranzer, 1987; Schmaranzer and Stabentheiner, 1988; Kovac and Stabentheiner, 1999). Because the ThermaCam works in the long-wave infrared range (7.5–13 μm) the reflected radiation from the wasps’ cuticle produced only a small measurement error (0.2 °C for 1000 Wm−2) which was compensated for. In this way we reached an accuracy of 0.7 °C for the body surface temperature of the wasps at a sensitivity of <0.1 °C.

The gradient between the thorax and the ambient temperature (thorax temperature excess = Tthorax–Ta) is often used as a measure to judge the endothermic capability of insects. In sunshine, however, this is not a reliable measure of the endogenously generated temperature excess. Therefore, we compared the living wasps’ temperature excess of thorax, head and abdomen with that of the dead wasps (operative temperature excess = Δ(Tbody–Ta) [living-dead wasps]).

The relationship between body temperature, temperature excess and Ta or solar radiation was described by simple linear regression and tested with an ANOVA. Data analysis and statistics were conducted using the Statgraphics package (Statistical Graphics Corporation) and ORIGIN software (OriginLab Corporation).

3. Results

Fig. 1A shows a thermogram of water foraging wasps (V. vulgaris and P. dominulus), and Fig. 1B of dead wasps (V. vulgaris and P. dominulus) fixed at the foraging site on a board. Body surface temperature values of head, thorax and abdomen were evaluated from 1509 thermograms for temperature curves of living wasps (Fig. 2), and 1476 thermograms were used for all body parts of dead wasps. In addition, 357 evaluated thermograms of wasps (Dolichovespula saxonica and P. dominulus) foraging nectar on raspberry and plant sap on rhubarb supplied body temperature data for the following analysis. An average foraging stay at medium ambient air temperature (Ta: 20–30 °C) lasted 21 ± 10 (SD) seconds for Vespula (N = 82) and 16 ± 6 s for Polistes (N = 7). ± At high Ta (30–40 °C) Vespula (N = 78) needed 16 ± 4 and Polistes (N = 68) 16 ± 6 s for collecting the water.

Fig. 2.

Fig. 2

Open in a new tab

Temperature curves of thorax, head and abdomen of water foraging Vespula (top) and Polistes (bottom) from arrival till departure at the water barrel.

3.1. Body temperature and ambient temperature

The relation of body temperature and ambient air temperature (Ta) is described with simple linear regressions shown in Fig. 3A–D. For statistical details see Table 1. At medium Ta (20–30 °C) the temperature of the thorax (Tth), head (Thd) and abdomen (Tab) of Vespula and Polistes water foragers was on average always elevated above Ta and increased with Ta. The regressions were always significantly different from 0 (P < 0.05, Table 1). In Vespula the regression line indicated an increase of the mean Tth from 35.5 to 37.5 °C, of the Thd from 29.1 to 34.1 °C, and of the Tab from 26.0 to 31.5 °C. In Polistes the Tth increased from 28.6 to 33.7 °C, the Thd from 25.0 to 30.7 °C and the Tab from 26.8 to 30.8 °C in this range of Ta (20–30 °C). The abundance of foraging Vespula at this Ta was much higher than that of Polistes, which is expressed in a disproportionately higher number of measured foraging stays for the Vespinae (Vespula N = 82, Polistes N = 7).

Fig. 3.

Fig. 3

Open in a new tab

Water temperature and body temperature of Vespinae (Vespula, Dolichovespula) and Polistinae (Polistes) during water collecting and foraging on raspberry and rhubarb in dependence on ambient temperature (Ta) at two different levels of Ta (A and C: 20–30 °C, B and D: 30–40 °C). For number of observations and regression statistics see Table 1.

Table 1.

Equations of regressions, coefficients of regressions (R), number of measurements (N) and probabilities (P) for the water temperature and the body temperature of Vespinae (Vespula, Dolichovespula) and Polistinae (Polistes) during water foraging, and on raspberry and rhubarb in dependence on ambient temperature (Ta) at two levels of Ta (Fig. 3A and C: 20–30 °C, Fig. 3B and D: 30–40 °C).

Ta (°C) Equations R N P
Vespula – water
20–30 Thorax Tth = 27.41175 + 0.36209*Ta 0.20178 522 < 0.0001
Head Thd = 8.39917 + 0.93079*Ta 0.45513 522 < 0.0001
Abdomen Tab = 3.31422 + 1.02167*Ta 0.50668 522 < 0.0001
Water Twater = 7.3329 + 0.67507*Ta 0.54315 181 < 0.0001
30–40 Thorax Tth = 24.29328 + 0.43083*Ta 0.32296 515 < 0.0001
Head Thd = 21.38082 + 0.44313*Ta 0.35296 511 < 0.0001
Abdomen Tab = 16.10936 + 0.59591*Ta 0.48795 515 < 0.0001
Water Twater = 25.54591+ 0.1619*Ta 0.14942 514 < 0.0001
Polistes – water
20–30 Thorax Tth = 1.91764 + 1.1688*Ta 0.42543 30 0.01909
Head Thd = −4.49277 + 1.29297*Ta 0.56875 30 0.00104
Abdomen Tab = 5.58229 + 0.93007*Ta 0.39501 30 0.03074
Water Twater = 4.70129+ 0.83004*Ta 0.64233 28 < 0.0001
30–40 Thorax Tth = 23.47161 + 0.44577*Ta 0.38489 442 < 0.0001
Head Thd = 17.52134 + 0.53413*Ta 0.43880 438 < 0.0001
Abdomen Tab = 19.76665 + 0.51086*Ta 0.53307 440 < 0.0001
Water Twater = 17.83922 + 0.3951*Ta 0.34866 364 < 0.0001
Dolichovespula - raspberry
20–30 Thorax Tth = −1.29307 + 1.28641*Ta 0.85973 74 < 0.0001
Head Thd = −0.7887 + 1.20336*Ta 0.86174 74 < 0.0001
Abdomen Tab = 1.83391 + 1.04714*Ta 0.76102 74 < 0.0001
Polistes – raspberry
20–30 Thorax Tth = −9.79247 + 1.42237*Ta 0.66113 129 < 0.0001
Head Thd = −8.21547 + 1.35957*Ta 0.70978 129 < 0.0001
Abdomen Tab = −5.33647 + 1.24764*Ta 0.69689 129 < 0.0001
Polistes - rhubarb
20–30 Thorax Tth = 38.41846–0.41693*Ta −0.28278 154 0.0004
Head Thd = 38.30495–0.4162*Ta −0.27034 154 0.0007
Abdomen Tab = 40.65034–0.50875*Ta −0.35157 154 < 0.0001
Open in a new tab

In Vespula foraging under warm conditions the Tth increased on average from 37.2 to 40.6 °C as Ta increased from 30 to 40 °C. The Thd increased from 34.7 to 38.2 °C, and the Tab from 34.0 to 38.7 °C, respectively. In Polistes the Tth increased from 37.0 to 40.8 °C, the Thd from 33.7 to 38.2 °C and the Tab from 35.3 to 39.5 °C. The abundance of foraging species was well-balanced at these conditions (Vespula N = 78, Polistes N = 68 measured foraging stays).

At medium Ta we also measured Dolichvespula foraging nectar on raspberry (in the shade), and in this case the Tth increased on average from 29.6 to 34.4 °C, the Thd from 28.1 to 32.5 °C and the Tab from 27.0 to 30.8 °C as Ta increased from 24.0 to 27.7 °C (Fig. 3A). The increase of body temperature with Ta was always significant (P < 0.0001, statistical details in Table 1). Comparing the regression lines of Tth of Dolichovespula with Vespula, ANOVA indicated significant differences (intercepts: F-ratio = 358.89, P < 0.00001; slopes: F-ratio = 18.06, P < 0.00001).

In Polistes gathering nectar on raspberry (in the shade) a positive correlation between Ta and body temperature was observed, with Tth increasing from 25.0 to 29.5 °C, Thd from 25.0 to 29.4 °C and Tab from 25.2 to 29.1 °C as Ta increased from 24.5 to 27.6 °C (P < 0.0001, Fig. 3C, statistical details in Table 1). However, Polistes foraging sap on rhubarb (in the shade) revealed a negative correlation between body temperature and increasing ambient temperature. The Tth decreased on average from 28.4 to 27.4 °C, the Thd from 28.2 to 27.3 °C and the Tab from 28.3 to 27.2 °C as Ta increased from 24.2 to 26.5 °C (P < 0.001, Fig. 3C, statistics in Table 1). Comparing the regression lines of Tth of water foraging and nectar gathering Polistes on raspberry revealed no significant differences between slopes (F-ratio = 0.40, P = 0.5270), but significant differences between intercepts (F-ratio = 167.27, P < 0.00001) could be detected. The regression lines of Tth of water foraging and sap gathering Polistes on rhubarb differed significantly in intercepts (F-ratio = 87.26, P < 0.00001) and slopes (F-ratio = 29.19, P < 0.00001; ANOVA).

The median Tth of water foraging Vespula and Polistes (Vespula: 36.5 and 36.7 °C, Polistes: 31.9 and 31.3 °C, respectively; Fig. 4) did not differ between arrival and departure at moderate Ta (P > 0.05). However, at high Ta in both species the Tth decreased significantly from the landing until take off (Vespula: 39.5 and 38.7 °C; P < 0.002; Polistes: 39.7 and 38.1 °C; P < 0.00001, Mann–Whitney/Wilcoxon test).

Fig. 4.

Fig. 4

Open in a new tab

Temperature of thorax, head and abdomen of Vespula (A) and Polistes (B) during arrival (red, left boxes) and departure (blue, right boxes) at the water barrel. Shown in the box plots are median, 25–75 percentile and minimum and maximum (Mann–Whitney/Wilcoxon test: *P < 0.05, **P < 0.01, ***P < 0.001).

The temperature of the collected water was positively correlated with the Ta under all conditions (Fig. 3, statistics in Table 1). The slope of the regression lines, however, was considerably flatter at high Ta (30–40 °C).

3.2. Thorax temperature excess and solar radiation

The Tth of living and dead wasps (Vespula and Polistes) was elevated above Ta at medium ambient temperature, and increased in all cases significantly with solar radiation (Fig. 5A, statistics in Table 2). The thorax temperature excess (Tth–Ta, mean values of regression lines) increased in Vespula from 10.6 to 12.6 °C (1.9 °C per kW−1 m−2), and in Polistes from 4.1 to 8.1 °C (4.4 °C per kW−1 m−2) as solar radiation increased from 35 to 1104 Wm−2 (Ta:20–30 °C). In dead Vespula it increased from 3.2 to 9.6 °C (6.3 °C per kW−1 m−2), and in dead Polistes from 1.8 to 6.2 °C (6.1 °C per kW−1 m−2). Comparing the four linear regressions with each other, with one exception (dead Vespula against dead Polistes), all differed significantly in intercepts and slopes (P < 0.05, statistics in Table 3).

Fig. 5.

Fig. 5

Open in a new tab

Thorax temperature excess (gradient between thorax and ambient temperature = Tth–Ta) of living Vespula and Polistes during water foraging and dead wasps in dependence on solar radiation at two levels of ambient temperature (A: 20–30 °C, B: 30–40 °C). For number of observations and regression statistics see Table 2.

Table 2.

Equations of regressions, coefficients of regressions (R), number of measurements (N) and probabilities (P) for the thorax temperature excess (Tth–Ta)of Vespula and Polistes during water foraging, and of dead wasps in dependence on solar radiation (SolRad) at two different levels of ambient temperatures (Fig. 5A: 20–30 °C. Fig. 5B: 30–40 °C).

Ta (°C) Equations R N P
20–30 Vespula Tth–Ta = 10.5374 + 0.00191*SolRad 0.31775 520 < 0.0001
Polistes Tth–Ta = 3.41373 + 0.00420*SolRad 0.69657 30 < 0.0001
Dead Vespula Tth–Ta = 2.82083 + 0.00610*SolRad 0.79317 366 < 0.0001
Dead Polistes Tth–Ta = 1.54654 + 0.00584*SolRad 0.75599 501 < 0.0001
30–40 Vespula Tth–Ta = 2.38616 + 0.00385*SolRad 0.56460 515 < 0.0001
Polistes Tth–Ta = 1.91603 + 0.00390*SolRad 0.61785 442 < 0.0001
Dead Vespula Tth–Ta = 0.46817 + 0.01045*SolRad 0.94036 110 < 0.0001
Open in a new tab

Table 3.

Comparison of the linear regressions of Table 2 with an ANOVA. For curves see Fig. 5. Right upper parts of the table parts represent F-ratios (P-values) of the regressions’ slopes, and left lower parts F-ratios (P-values) of the regressions’ intercepts.

20–30 °C Vespula Polistes Dead Vespula Dead Polistes
Vespula 7.24 (P < 0.0073) 145.99 (P < 0.00001)
Polistes 241.25 (P < 0.00001) 6.10 (P < 0.0139)
Dead Vespula 1858.85 (P < 0.00001) 1.95 (P = 0.1624)
Dead Polistes 14.55 (P < 0.0002) 234.78 (P < 000001)
30–40 °C
Vespula 0.10 (P = 0.7511) 123.37 (P < 0.00001)
Polistes 18.62 (P < 0.00001) 32.87 (P < 0.00001)
Dead Vespula 236.14 (P < 0.00001) 111.65 (P < 0.00001)
Dead Polistes 80.71 (P < 0.00001) 237.43 (P < 0.00001)
Open in a new tab

Under very warm conditions the Tth of living and dead wasps was also elevated above Ta (Fig. 5B). The thorax temperature excess increased with increasing solar radiation, the linear regressions being significantly different from 0 (P < 0.0001, Table 2). The gradient between Tth and Ta increased in Vespula from 2.6 to 5.9 °C (4.0 °C per kW−1 m−2), in Polistes from 2.2 to 5.5 °C (4.0 °C per kW−1 m−2) and in dead Vespula from 1.0 to 10.0 °C (10.7 °C per kW−1 m−2) as solar radiation increased from 68 to 907 Wm−2 (Ta: 30–40 °C). We could not conduct measurements on dead Polistes in this range of Ta. Comparing the four linear regressions with an ANOVA revealed no differences between the slopes of living Vespula and Polistes, but significant differences were observed for all other slopes and intercepts (P < 0.00001, statistics in Table 3).

3.3. Endothermic temperature elevation

Fig. 6 gives an overview of the endothermic temperature elevation of Vespula and Polistes at the two ranges of Ta. The thorax temperature excess (Tth–Ta) of the dead wasps reveals the heat gain of the insects from solar radiation. The difference of the regression lines of the thorax temperature excess in Fig. 5 between living and dead wasps therefore yields an indirect measure of the endothermic heat production of the wasps. At moderate Ta, Vespula exhibited a distinct active heat production even at high solar radiation (Fig. 6A). The Polistes, by contrast, were only weakly endothermic (Fig. 6B). The difference of the thorax temperature excess decreased in both species with increasing solar radiation. In Vespula the active heat production of the thoracic muscles had an effect on the head temperature excess (which was positive), but in Polistes the head temperature excess was not elevated above zero. However, the difference of the abdomen temperature excess was negative for both wasps. The reliability of the data of the head and the abdomen is not as good as that of the thorax because their temperature depends more on the angle of incidence of the solar radiation.

Fig. 6.

Fig. 6

Open in a new tab

Difference of the gradient between head, thorax, abdomen and ambient temperature (Tbody–Ta) of living Vespula and Polistes during water foraging, and dead wasps, in dependence on solar radiation at two levels of ambient temperature (A and B: 20–30 °C, C and D: 30–40 °C).

As already observed at moderate Ta, at high Ta the differences of the thorax temperature excesses decreased with increasing solar radiation (Fig. 6C and D). For Vespula, a positive gradient (Tth–Ta live > Tth–Ta dead) was only detectable at solar radiation less than about 300 Wm−2. In Polistes it soon decreased below zero, but not as quickly as in Vespula. This means that Vespula exhibited a stronger cooling effort in the thorax. The curves of the head and the abdomen were always negative, and their slope followed that of the thorax, except for the head of Polistes (Fig. 6C and D).

4. Discussion

4.1. Body temperature and ambient temperature

In water and nectar foraging wasps (exception Polistes on rhubarb in the shade) an obvious positive correlation between body temperature and ambient air temperature was detected (Fig. 3, Table 1). This result is in good accordance with thoracic temperature measurements of foraging Dolichovespula maculata and V. vulgaris (Heinrich, 1984) and of Vespula germanica and Vespula maculifrons returning to their nest (Coelho and Ross, 1996). Comparing the body temperature measurements of these authors in the same ambient temperature range (Ta: 20–30 °C) with ours, the range of the thorax temperature of Vespula was quite similar (Tth = 30–40 °C). Also in this range was the Tth of Paravespula vulgaris foragers gathering sucrose solution on an artificial feeding bowl, with an average Tth of about 35.3–39.1 °C (Kovac and Stabentheiner, 1999). Water collecting honeybees foraging in the shade had similar Tth values, but no obvious dependence on Ta was detected (Schmaranzer, 2000). In our measurements D. saxonica (in the shade) and P. dominulus foraging nectar or water exhibited similar body temperature patterns, but they were noticeably cooler than V. vulgaris. At very warm conditions (Ta: 30–40 °C) the Tth of the Vespula and Polistes was nearly the same and again in good accordance with measurements of Vespula of Coelho and Ross (1996). As the Tth is important for the ability to take off (flight temperature minimum; Esch, 1976; Coelho and Ross, 1996), and in general the activity is strongly affected by the body temperature (Stabentheiner et al., 2003), thermoregulatory capability likely has some importance for the fitness and foraging success of the insects.

The measurements at moderate ambient temperatures revealed the better thermoregulatory capability of Vespula in comparison to Polistes through the higher elevation of all body parts above Ta and the weaker dependence of the Tth on Ta. With increasing Ta the necessity for an active thermoregulation via thoracic heat production was reduced. The elevation of body temperature above Ta decreased and the gradients between thorax and head and abdomen temperature became smaller. This relationship was also observed by Heinrich (1984) and Coelho and Ross (1996) in other wasp species. However, in contrast to Vespula the Polistes exhibited a nearly parallel increase of all body parts with increasing Ta, which means a weaker (or nearly absent) endothermic response to ambience. At high Ta, when the endothermic heat production became less important, the differences between Vespula and Polistes nearly disappeared (Fig. 3).

Sucrose foraging wasps exhibited higher thorax temperatures at departure (Kovac and Stabentheiner, 1999) than at arrival, probably to compensate for the loaded weight. This fact was not detected in the water foraging wasps. Obviously it was not necessary for them to compensate for the loaded water with a higher Tth (and thus flight muscle temperature) for proper departure. At high Ta both species even cooled down between landing and take off (Fig. 4). We suggest this to be the result of the reduced endothermic activity and the cooling via the ingested water. At this high Ta the high Tth after flight made cooling indispensable in both species. Water foraging wasps prefer wet spots (wood, moss, algae, etc.) rather than open water surfaces. These spots differed in their local temperature (see Fig. 1A). Fig. 3 shows that the correlation of local water temperature was flatter at high Ta (Table 1) and considerably below Ta. From this observation we suggest that the wasps actively selected cooler spots for the purpose of cooling.

4.2. Thorax temperature excess and operative temperature

The thorax temperature excess (difference between Tth and Ta) allows an assessment of the thermoregulatory performance of insects and a comparison of different species. Digby (1955) investigated the factors affecting the temperature excess of insects in artificial sunlight under laboratory conditions and found the temperature excess to vary directly with the radiation strength. Our measurements with foraging wasps under natural conditions at moderate and high ambient temperatures confirm this result (Fig. 5, Table 2). The gradient between Tth and Ta increased with increasing solar radiation in dead and living wasps. Cena and Clark (1972) and Underwood (1991) described this positive correlation between excess temperature (thorax and abdomen) and solar radiation for honeybees at the hive entrance and upon arrival at a feeder.

In Fig. 6 the differing thermoregulatory behaviour of Vespula and Polistes is expressed by using the operative temperature (Te thermometer; Bakken, 1992) in connection with the thorax temperature excess. We used this parameter (Te) in addition to quantify the insects’ thermoregulatory performance, as the Ta is often an inaccurate measure of the thermal environment experienced by the insects, which is additionally influenced by solar radiation and convective effects of the wind. The positive parts of the curves in Fig. 6 represent correlates of the amount of endothermic heat production by the wasps.

At moderate Ta the thorax temperature excess of Vespula in dependence on solar radiation was clearly above that of dead wasps and of living Polistes (Fig. 5, Table 2), which indicates their good capability of endothermic heat production with the thoracic muscles and their active thermoregulation. However, the temperature gradient of the dead and living Polistes did not differ, which means no or only a weak degree of endothermy (for statistics see Table 3). The values of nectar and sap foraging Polistes (Fig. 3) in the shade confirm this result. At very warm conditions the thermoregulation of Vespula and Polistes became similar, because Vespula reduced endothermic activity, which obviously was not necessary. The dead wasps, both Vespula and Polistes, exhibited a steeper slope of the temperature gradient with dependence on radiation. The fact that they were heated stronger than the living wasps means that the living wasps exhibited active cooling (negative parts of the curves in Fig. 6C and D). The difference between the dead individuals of the two wasp species may result from varying colouration of the body parts, differences in shape or body orientation, or different micro-environmental temperature and convection conditions. This is also valid for the living wasps and remains to be investigated in detail. The body of the living water collecting wasps was probably cooled via the ingested water. Active cooling of the body in wasps by means of water droplets was reported by Coelho and Ross (1996). In addition, cooling via respiration has to be taken into consideration.Fig. 6C and D indicate that the cooling efforts were smaller in Polistes though their body temperatures were below that of Vespula (Fig. 3). We cannot exclude the possibility that at least part of this difference originated from remaining partial endothermic heat production of Vespula even at high Ta.

4.3. Endothermy

Though Vespula and Polistes are similar in size they displayed striking differences in endothermic capability. However, in other insects a positive relationship between thermoregulatory capability and body size (or mass) was observed, e.g. in moths (Bartholomew and Heinrich, 1973), beetles (Bartholomew and Heinrich, 1978), 18 species of Alaskan bees (Bishop and Armbruster, 1999), and also in wasps by Heinrich (1984). In general, small bees initiate flight at lower thoracic temperatures than larger ones. For bees smaller than 15 mg dry mass (<~40 mg living weight), Bishop and Armbruster (1999) detected no appreciable ability to regulate Tth, and their results are largely in agreement with other studies (e.g. Stone, 1993a, b; Stone and Willmer, 1989a, b). Their results also indicate that bees display continuous variation in the degree of endothermy with weight, even in the smallest solitary bees (Bishop and Armbruster, 1999). However, Dyer and Seeley (1987) detected deviations from the expected size-related patterns in foragers of three Asian and the European honeybee species. The smallest species, Apis florea, showed the smallest temperature excess (Tth–Ta), but the intermediate-sized A. cerana and A. mellifera both showed a consistently higher temperature excess than the largest species, A. dorsata. Our two investigated wasp species also seem to be an exception from the rule of the relationship between thermoregulatory capability and size. Although they have a similar body size and mass (Vespula ~57–97 mg and Polistes ~83–111 mg) they nevertheless showed a quite different thermoregulatory performance.

It seems that Polistes reach a comparable success in individual and colony survival without the high energetic investment of Vespula to generate thermal power for a highly elevated Tth. Future experiments are needed to investigate the question of the benefit of the high energetic investment of the Vespine wasps. Possibly it enables them to collect higher quantities of water in a shorter time, while allowing them to maintain the necessary high body temperature for a safe and quick take off (Esch, 1976; Coelho, 1991). A comparison of the thermoregulatory behaviour of these two wasps species shows that survival of similarly sized insects in the same habitat may be ensured by different physiological strategies.

Acknowledgements

Supported by the Austrian Fonds zur Förderung der Wissenschaftlichen Forschung (FWF, P16584-B06, P20802-B16), and the Austrian Bundesministerium für Land- und Forstwirtschaft, Umwelt und Wasserwirtschaft. We greatly appreciate the help with electronics and software by G. Stabentheiner, with data evaluation by M. Ablasser, P. Kirchberger, B. Klug and G. Rauter, and we thank D. L. Denlinger and two anonymous referees for helpful comments.

References

  1. Akre RD. Social Wasps. In: Hermann H, editor. Social Insects. Vol. 4. Academic; New York: 1982. pp. 1–105.pp. 385 [Google Scholar]
  2. Bakken GS. A heat transfer analysis of animals: unifying concepts and the application of metabolism chamber data to field ecology. Journal of Theoretical Biology. 1976;60:337–384. doi: 10.1016/0022-5193(76)90063-1. [DOI] [PubMed] [Google Scholar]
  3. Bakken GS. The use of standard operative temperature in the study of the thermal energetics of birds. Physiological Zoology. 1980;53:108–119. [Google Scholar]
  4. Bakken GS. Measurement and application of operative and standard operative temperatures in ecology. American Zoologist. 1992;32:194–216. [Google Scholar]
  5. Bartholomew GA, Heinrich B. A field study of flight temperatures in moths in relation to body weight and wing loading. Journal of Experimental Biology. 1973;58:123–135. [Google Scholar]
  6. Bartholomew GA, Heinrich B. Endothermy in African dung beetles during flight, ball making, and ball rolling. Journal of Experimental Biology. 1978;73:65–83. [Google Scholar]
  7. Bishop JA, Armbruster WS. Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology. Functional Ecology. 1999;13:711–724. [Google Scholar]
  8. Cena K, Clark JA. Effect of solar radiation on temperatures of working honey bees. Nature. 1972;236:222–223. doi: 10.1038/newbio236222a0. [DOI] [PubMed] [Google Scholar]
  9. Coelho JR. Heat transfer and body temperature in honey bee (Hymenoptera: Apidae) drones and workers. Environmental Entomology. 1991;20:1627–1635. [Google Scholar]
  10. Coelho JR, Ross AJ. Body temperature and thermoregulation in two species of yellowjackets, Vespula germanica and V. maculifrons. Journal of Comparative Physiology B. 1996;166:68–76. [Google Scholar]
  11. Digby PSB. Factors affecting the temperature excess of insects in sunshine. Journal of Experimental Biology. 1955;32:279–298. [Google Scholar]
  12. Dyer CD, Seeley TD. Interspecific comparison of endothermy in honeybees (Apis): deviations from the expected size-related patterns. Journal of Experimental Biology. 1987;127:1–26. [Google Scholar]
  13. Eckles MA, Wilson EE, Holway DA, Nieh JC. Yellowjackets (Vespula pensylvanica) thermoregulate in response to changes in protein concentration. Naturwissenschaften. 2008;95:787–792. doi: 10.1007/s00114-008-0384-x. [DOI] [PubMed] [Google Scholar]
  14. Esch H. Body temperature and flight performance of honey bees in a servomechanically controlled wind tunnel. Journal of Comparative Physiology. 1976;109:265–277. [Google Scholar]
  15. Gibo DL, Yarascavitch RM, Dew HE. Thermoregulation in colonies of Vespula arenaria and Vespula maculata (Hymenoptera: Vespidae) under normal conditions and under cold stress. Canadian Entomologist. 1974;106:503–507. [Google Scholar]
  16. Greene A. Dolichovespula and Vespula. In: Ross KG, Matthews RW, editors. The Social Biology of Wasps. XVII + 678P. Cornell University Press; Ithaca, New York, USA; London, England, UK. Illus. Maps: 1991. pp. 263–306. [Google Scholar]
  17. Harrison JF, Hall HG. African-European honeybee hybrids have low intermediate metabolic capacities. Nature. 1993;363:258–260. [Google Scholar]
  18. Harrison JF, Fewell JH, Roberts SP, Hall HG. Achievement of thermal stability by varying metabolic heat production in flying honeybees. Science. 1996;274:88–90. doi: 10.1126/science.274.5284.88. [DOI] [PubMed] [Google Scholar]
  19. Heinrich B. Thermoregulation of African and European honeybees during foraging, attack, and hive exits and returns. Journal of Experimental Biology. 1979;80:217–229. [Google Scholar]
  20. Heinrich B. Strategies of thermoregulation and foraging in two vespid wasps, Dolichovespula maculata and Vespula vulgaris. Journal of Comparative Physiology B. 1984;154:175–180. [Google Scholar]
  21. Heinrich B. The Hot-Blooded Insects. Springer-Verlag Berlin Heidelberg; London Paris: 1993. [Google Scholar]
  22. Heinrich B, Heinrich MJE. Size and caste in temperature regulation by bumblebees. Physiological Zoology. 1983;56:552–562. [Google Scholar]
  23. Himmer A. Die Temperaturverhältnisse bei den sozialen Hymenopteren. Biological Reviews. 1932;7:224–253. [Google Scholar]
  24. Ishay JS. Thermoregulation by social wasps: behavior and pheromones. Transactions of the New York Acadademy of Science. 1973;35:447–462. doi: 10.1111/j.2164-0947.1973.tb01518.x. [DOI] [PubMed] [Google Scholar]
  25. Ishay J, Ruttner F. Thermoregulation im Hornissennest. Zeitschrift für vergleichende Physiologie. 1971;72:423–434. [Google Scholar]
  26. Jeanne RL. Regulation of nest construction behavior in Polybia occidentalis. Animal Behaviour. 1996;52:473–488. [Google Scholar]
  27. Klingner R, Richter K, Schmolz E, Keller B. The role of moisture in the nest thermoregulation of social wasps. Naturwissenschaften. 2005;92:427–430. doi: 10.1007/s00114-005-0012-y. [DOI] [PubMed] [Google Scholar]
  28. Klingner R, Richter K, Schmolz E. Strategies of social wasps for thermal homeostasis in light paper nests. Journal of Thermal Biology. 2006;31:599–604. [Google Scholar]
  29. Kovac H, Schmaranzer S. Thermoregulation of honeybees (Apis mellifera) foraging in spring and summer at different plants. Journal of Insect Physiology. 1996;42:1071–1076. [Google Scholar]
  30. Kovac H, Stabentheiner A. Körpertemperaturen frei beweglicher Wespen an einem Futterplatz bei wiederholten Sammelflügen. Mitteilungen der deutschen Gesellschaft für allgemeine und angewandte Entomologie. 1993;8:741–744. [Google Scholar]
  31. Kovac H, Stabentheiner A. Effect of food quality on the body temperature of wasps (Paravespula vulgaris) Journal of Insect Physiology. 1999;45:183–190. doi: 10.1016/s0022-1910(98)00115-2. [DOI] [PubMed] [Google Scholar]
  32. Kovac H, Stabentheiner A. A comparison of body temperatures of honeybees and wasps foraging on raspberry and rhubarb. In: Menzel R, Rademacher E, editors. Proceedings of the 2001 Berlin Meeting of the European Sections of the IUSSI; Berlin. 2001. p. 194. ISBN 3-901864-01-7. [Google Scholar]
  33. Makino S, Yamane S. Heat production by the foundress of Vespa simillima, with description of its embryo nest (Hymenoptera: Vespidae) Insecta Matsumurana. 1980;19:89–101. [Google Scholar]
  34. Martin SJ. Thermoregulation in Vespa simillima xanthoptera (Hymenoptera, Vespidae) Kontyu. 1988;56:674–677. [Google Scholar]
  35. Nieh JC, Sanchez D. Effect of food quality, distance and height on thoracic temperature in 343 the stingless bee, Melipona panamica. Journal of Experimental Biology. 2005;208:3933–3943. doi: 10.1242/jeb.01792. [DOI] [PubMed] [Google Scholar]
  36. Nieh JC, Leon A, Cameron S, Vandame R. Hot bumble bees at good food: thoracic temperature of feeding Bombus wilmattae foragers is tuned to sugar concentration. Journal of Experimental Biology. 2006;209:4185–4192. doi: 10.1242/jeb.02528. [DOI] [PubMed] [Google Scholar]
  37. Schmaranzer S. Thermoregulation of water collecting honeybees (Apis mellifera) Journal of Insect Physiology. 2000;46:1187–1194. doi: 10.1016/s0022-1910(00)00039-1. [DOI] [PubMed] [Google Scholar]
  38. Schmaranzer S, Stabentheiner A. Variability of the thermal behaviour of honeybees on a feeding place. Journal of Comparative Physiology B. 1988;158:135–141. [Google Scholar]
  39. Seeley TD, Camazine S, Sneyd J. Collective decision-making in honey bees – how colonies choose among nectar sources. Behavioral Ecology and Sociobiology. 1991;28:277–290. [Google Scholar]
  40. Stabentheiner A. Thermoregulation of dancing bees: thoracic temperature of pollen and nectar foragers in relation to profitability of foraging and colony need. Journal of Insect Physiology. 2001;47:385–392. doi: 10.1016/s0022-1910(00)00132-3. [DOI] [PubMed] [Google Scholar]
  41. Stabentheiner A, Hagmüller K. Sweet food means ‘hot dancing’ in honey bees. Naturwissenschaften. 1991;78:471–473. [Google Scholar]
  42. Stabentheiner A, Schmaranzer S. Thermographic determination of body temperatures in honey bees and hornets: calibration and applications. Thermology. 1987;2:563–572. [Google Scholar]
  43. Stabentheiner A, Vollmann J, Kovac H, Crailsheim K. Oxygen consumption and body temperature of active and resting honeybees. Journal of Insect Physiology. 2003;49:881–889. doi: 10.1016/S0022-1910(03)00148-3. [DOI] [PubMed] [Google Scholar]
  44. Stabentheiner A, Kovac H, Schmaranzer S. Der Einfluss der Sonnenstrahlung auf die Körpertemperatur Wasser sammelnder Wespen (Paravespula germanica) Mitteilungen der deutschen Gesellschaft für allgemeine und angewandte Entomologie. 2004;14:451–454. [Google Scholar]
  45. Steiner A. Die Temperaturregulierung im Nest der Feldwepe (Polistes gallica var. biglumis L.) Zeitschrift für vergleichende Physiologie. 1930;11:461–502. [Google Scholar]
  46. Stone GN. Endothermy in the solitary bee Anthophora plumipes: Independent measures of thermoregulatory ability, costs of warm-up and the role of body size. Journal of Experimental Biology. 1993a;174:299–320. [Google Scholar]
  47. Stone GN. Thermoregulation in four species of tropical solitary bees: the roles of size, sex, and altitude. Journal of Comparative Physiology B. 1993b;163:317–326. [Google Scholar]
  48. Stone GN, Willmer PG. Endothermy and temperature regulation in bees: a critique of ‘grab and stab’ measurement of body temperature. Journal of Experimental Biology. 1989a;143:211–223. [Google Scholar]
  49. Stone GN, Willmer PG. Warm-up rates and body temperatures in bees: the importance of body size, thermal regime and phylogeny. Journal of Experimental Biology. 1989b;147:303–328. [Google Scholar]
  50. Underwood B. Thermoregulation and energetic decisionmaking by the honeybees Apis cerana, Apis dorsata and Apis laboriosa. Journal of Experimental Biology. 1991;157:19–34. [Google Scholar]
  51. Weyrauch W. Das Verhalten sozialer Wespen bei Nestüberhitzung. Zeitschrift für vergleichende Physiologie. 1936;23:51–63. [Google Scholar]
  52. Waddington KD. Foraging profits and thoracic temperatures of honey bees (Apis mellifera) Journal of Comparative Physiology B. 1990;160:325–329. [Google Scholar]
  53. Woods WA, Heinrich B, Stevenson RD. Honeybee flight metabolic rate: does it depend upon air temperature? Journal of Experimental Biology. 2005;208:1161–1173. doi: 10.1242/jeb.01510. [DOI] [PubMed] [Google Scholar]

RESOURCES