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Effect of food quality on the body temperature of wasps (Paravespula vulgaris)
Journal of Insect Physiology 45 (1999) 183–190
Effect of food quality on the body temperature of wasps (Paravespula vulgaris) Helmut Kovac, Anton Stabentheiner
*
Institut fu¨r Zoologie, Karl-Franzens-Universita¨t Graz, Universita¨tsplatz 2, A-8010 Graz, Austria Received 21 April 1998; accepted 16 July 1998
Abstract Body surface temperature of individually marked wasps (Paravespula vulgaris, Vespidae, Hymenoptera) was measured by infrared thermography during repeated visits to a feeding bowl without injuring them or disturbing their behavior. Wasps were fed 0.5, 1 and 2 mol/l sucrose solution at two ambient temperatures. Thoracic temperature varied significantly in dependence on food quality (sucrose concentration of solution). At the higher ambient temperatures of 26.1–30.2°C mean thoracic surface temperatures from different experiments were 35.3 and 38.0°C when the wasps took a 0.5 mol/l sucrose solution, 37.0, 38.7 and 38.7°C when they took a 1 mol/l solution, and 39.1°C when they took a 2 mol/l sucrose solution. At the lower ambient temperatures of 17.6–21.0°C thoracic temperatures were lower but the effect of different sucrose concentrations was similar: 34.7°C with a 0.5 mol/l and 36.1°C with a 1 mol/l sucrose solution. The concentration effect amounted to about 10–25% of the whole variability of thorax temperature. By contrast, the temperatures of the head and abdomen did not follow the changes in thorax temperature according to changes in sucrose concentration closely, which suggests that the pattern of haemolymph circulation may have changed after landing, during the wasps’ stay at the feeder. At initial landing at the feeders thoracic temperatures where equal to (three of eight tests) or lower (five of eight tests) than at final departure. The correlation of thorax temperature with food quality probably reflects the wasps’ level of excitement and motivation to collect the food, which allows them to balance energetic investment with profitability of foraging and the needs of flight muscle performance and motility. 1999 Elsevier Science Ltd. All rights reserved. Keywords: Insect; Wasp; Food quality; Thermoregulation; Thermography
1. Introduction Wasps of the subfamily Vespinae are well known for their faculty of thermoregulation. Because of their pronounced capacity for endothermic heat production they are not only able to increase body temperature well above ambient levels (Heinrich, 1984; Coelho and Ross, 1996) but also to regulate the temperature of their nests (Himmer, 1932; Ishay and Ruttner, 1971). Outside the nest they keep thoracic temperature at a high level to ensure proper function of their flight muscles, which allows them to forage at temperatures as low as 4°C (Heinrich, 1984, 1993; Coelho and Ross, 1996). In general, vespine wasps are considered as heterothermic insects which lower thoracic temperature to near ambient levels during periods of rest or little activity and increase * Corresponding author.
it when preparing for flight or during periods of high activity. However, they are not heterothermic in a sense that during periods of high activity they increase thoracic temperature to a certain level. Rather, the level at which they regulate the temperature of their thorax during periods of high activity has been shown to depend on what they are doing: Heinrich (1984) demonstrated that temperatures were in part different in wasps leaving the nest or returning to it, or in attacking animals. Considerable variation of body temperature was also observed by Coelho and Ross (1996). Since only part of the variation can be explained by the effect of ambient temperature or the behavioral situation (Heinrich, 1984; Coelho and Ross, 1996) we suggested that there must be additional factors which influence regulation of body temperature. In several species of the genus Apis it has been demonstrated that food quality (e.g., sugar concentration and foraging distance) is another factor which modulates the thermal behavior
0022–1910/99/$ - see front matter 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 2 - 1 9 1 0 ( 9 8 ) 0 0 1 1 5 - 2
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of honeybees (Stabentheiner and Schmaranzer, 1986; Dyer and Seeley, 1987; Schmaranzer and Stabentheiner, 1988; Waddington, 1990; Stabentheiner and Hagmu¨ller, 1991; Underwood, 1991; Stabentheiner et al., 1995; Stabentheiner, 1996). Unlike the honeybees the Vespinae forage for insects and flesh to rear their larvae. However, they also gather sugared fluids like honeydew produced by aphids, nectar from flowers or sweet syrup from fruits, which makes them easily trainable to artificial sugar sources. In the present paper we investigated the question of whether the sugar content of the food—as a measure of food quality—may act as a modulator of the thermal behavior of wasps.
2. Materials and methods Common yellowjackets (Paravespula vulgaris, Vespidae, Hymenoptera) were trained to visit a feeding place which was protected from wind and solar radiation on three days of August 1989 and 1992 at two levels of ambient temperature (17.6–21.0°C and 26.1–30.2°C). They were marked individually by color dots applied to their abdomen. In a glass jar inverted over a grooved glass base they were offered sucrose solution of 0.5–2 molar concentration which they could gather ad libitum. Three experiments were performed in this manner. Experiment 1 (1989): In the beginning six wasps were offered sucrose solution of 1 mol/l concentration because with this concentration the wasps could be more easily attracted to the feeding bowl than with lower ones. After about 2 h the concentration was lowered to 0.5 mol/l. Experiment 2 (1989): Six wasps were offered 0.5 mol/l solution first and 1 mol/l solution after about 2 h. Experiment 3 (1992): Four wasps were investigated at a location 10 km apart from that of Experiments 1 and 2. They received 1 mol/l sucrose in the beginning, the concentration of which was lowered to 0.5 mol/l after about 1 h. Another hour later the concentration was again increased to 1 mol/l. Towards the end of the experiment the concentration was increased to 2 mol/l. In order to allow undisturbed, simultaneous and repeated measurement of the temperature of different body parts (head, thorax, abdomen) the method of infrared thermography was used (Schmaranzer, 1983; Stabentheiner and Schmaranzer, 1987). With this method it is possible to determine the body surface temperature from the infrared radiation emitted by an insect’s body. The real-time infrared camera (AGA 782 SW) enabled us to monitor temporal changes of body surface temperature and to perform repeated measurements on the same individual. The thermographic scenes were stored on videotape for later analysis. Thermograms were taken from the videotapes in intervals of 3–8 s, depending on whether the wasps were visible in the infrared image and all body parts were in focus. Because of different
durations of stay at the feeding bowl differences in sample sizes occurred for different feeding bouts. The infrared radiation emitted by the wasps was compared with the radiation of an AGA 1010 reference source, which was precision calibrated against a black body radiator of our own construction. The temperature of the black body radiator was kept constant with an accuracy of ⬍ 0.05°C (Stabentheiner and Schmaranzer, 1987). Since the emissivity of the wasp cuticle was not known we used the value of 0.97 determined in honeybees by simultaneous registration of infrared radiation and surface temperature by means of micro thermocouples (diameter of wires: 0.05 mm) to calculate absolute surface temperatures (for details see Stabentheiner and Schmaranzer, 1987). This seemed to be safe because a very similar value of 0.965 was determined in the European cockchafer Melolontha melolontha (diameter of thermocouple wires: 0.012 mm; Stabentheiner, unpublished measurements). In this way, self-written PC software allowed calculation of absolute body surface temperatures with an accuracy of 0.5°C and relative (comparative) measurements to the nearest 0.2°C. Ambient temperature (Ta) was measured beside the feeding bowl by means of a Technoterm 9400 digital thermometer. To test for intra-individual variation caused by changes in sucrose concentration non-parametric statistics were used: Kruskal–Wallis H test and, for comparison between different concentrations, the Kolmogorov–Smirnov test. Inter-individual variability was tested by ANOVA and Scheffe’s test. Statistics are based on evaluated temperature values (n in Tables 1–3).
3. Results The wasps stayed at the feeding bowl for about 20– 120 s. Feeding was sometimes interrupted by short flights around the bowl, after which the insects resumed foraging (Fig. 1). Fig. 2 shows typical temperature curves of one wasp (from Experiment 3) gathering sucrose solution of different concentrations which did not interrupt its stays. Thorax temperature (Tth) was either kept constant or increased up to 2°C during the insects’ stay at the feeding bowl (Figs. 1 and 2). Especially before take-off a slight increase was often observed. The temperature of the head (Th) mostly decreased after landing and then remained more or less stable during the rest of the stay. Abdominal temperature (Tab) mostly was lowest at landing and increased towards the wasps’ departure (Figs. 1 and 2). 3.1. Experiment 1 Thoracic surface temperature of the wasps ranged from 31.7 to 39.9°C at ambient temperatures (Ta) of
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Table 1 Body surface temperatures of wasps (Paravespula vulgaris) from Experiments 1 and 2 Sucrose Experiment no. concentration (mol/l) Experiment 1
1
0.5
Experiment 2
0.5
1
Tth ⫾ SD (°C) Th ⫾ SD (°C) Tab ⫾ SD (°C) n
Ta ⫾ SD (°C) N
Mean Landing Departure Mean Landing Departure
37.0 36.2 37.5 35.2 35.3 35.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.2 0.8 1.3 1.2 0.6 1.7
31.7 32.7 31.3 31.6 32.6 31.1
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.2 0.7 1.2 0.9 0.6 0.8
28.7 27.9 29.2 29.1 28.6 29.4
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
0.8 0.4 0.6 0.6 0.5 0.4
187 32 32 278 21 21
Mean Landing Departure Mean Landing Departure
34.7 34.0 34.5 36.1 36.0 35.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.3 1.4 1.7 0.7 0.7 0.7
27.5 28.8 26.3 28.9 30.7 27.6
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.5 1.4 1.3 1.6 1.1 0.7
23.6 23.6 24.0 25.6 25.2 25.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
0.7 0.7 0.8 0.6 0.7 0.6
190 11 11 147 16 21
27.5 ⫾ 0.4
33
28.5 ⫾ 0.6
21
18.3 ⫾ 0.4
11
19.9 ⫾ 0.6
22
Sucrose concentrations offered in the displayed order. Indicated are means of thorax (Tth), head (Th) and abdomen (Tab), mean temperatures during initial landing and final departure, ambient air temperature beside the feeding bowl (Ta) with SD, and number of evaluated thermograms (n), values of Ta and stays at the feeder (N).
Table 2 Body surface temperatures of wasps (Paravespula vulgaris) from Experiment 3
Animal
Sucrose concentration (mol/l)
Tth ⫾ SD (°C)
Th ⫾ SD (°C)
Tab ⫾ SD (°C)
Ta ⫾ SD (°C)
n
N
Wasp 1
1 0.5 1a 2
39.9 38.5 39.6 39.8
⫾ ⫾ ⫾ ⫾
0.9 0.7 0.7 1.0
34.0 33.4 32.8 33.5
⫾ ⫾ ⫾ ⫾
0.9 0.8 0.6 0.6
30.7 30.4 30.2 30.2
⫾ ⫾ ⫾ ⫾
0.7 0.5 0.6 1.2
63 94 47 64
29.8 29.6 29.5 29.1
⫾ ⫾ ⫾ ⫾
0.2 0.3 0.1 0.3
11 12 6 6
Wasp 2
1 0.5 1a 2
38.7 38.3 38.4 38.7
⫾ ⫾ ⫾ ⫾
0.7 0.6 0.7 1.0
34.2 33.4 32.6 33.0
⫾ ⫾ ⫾ ⫾
0.9 0.8 0.7 0.6
30.5 30.4 29.8 29.7
⫾ ⫾ ⫾ ⫾
0.9 0.5 0.7 1.1
73 84 45 68
29.8 29.5 29.4 29.0
⫾ ⫾ ⫾ ⫾
0.2 0.2 0.1 0.2
12 10 6 8
Wasp 3
1 0.5 1a 2
38.4 37.9 38.7 39.8
⫾ ⫾ ⫾ ⫾
1.2 0.6 0.8 1.4
34.2 33.4 32.6 32.6
⫾ ⫾ ⫾ ⫾
0.8 0.7 0.6 0.5
30.0 30.0 29.6 29.2
⫾ ⫾ ⫾ ⫾
1.0 0.6 0.5 1.2
74 106 40 37
29.9 29.5 29.5 29.2
⫾ ⫾ ⫾ ⫾
0.2 0.1 0.1 0.4
13 14 6 5
Wasp 4
1 0.5 1a 2
37.8 37.3 37.9 38.2
⫾ ⫾ ⫾ ⫾
1.1 0.9 1.0 1.3
33.5 32.6 31.9 32.2
⫾ ⫾ ⫾ ⫾
0.9 0.8 0.6 0.6
29.9 29.8 29.5 29.4
⫾ ⫾ ⫾ ⫾
0.7 0.7 0.7 0.8
61 76 45 42
29.9 29.6 29.4 29.0
⫾ ⫾ ⫾ ⫾
0.3 0.2 0.1 0.2
10 10 6 7
All wasps
1 0.5 1a 2
38.7 38.0 38.7 39.1
⫾ ⫾ ⫾ ⫾
1.2 0.8 1.0 1.3
34.0 33.2 32.5 32.9
⫹ ⫹ ⫹ ⫹
0.9 0.8 0.7 0.7
30.3 30.1 29.8 29.8
⫹ ⫹ ⫹ ⫹
0.9 0.6 0.7 1.5
271 360 177 211
29.9 29.5 29.5 29.1
⫾ ⫾ ⫾ ⫾
0.2 0.2 0.1 0.3
46 46 24 26
Sucrose concentrations offered in the displayed order (asecond feeding with 1 mol/l). Indicated are means of thorax (Tth), head (Th), abdomen (Tab) and ambient air temperature beside the feeding bowl (Ta) with SD, and number of evaluated thermograms (n), values of Ta and stays at the feeder (N).
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Table 3 Body surface temperatures of all wasps (Paravespula vulgaris) during initial landing and final departure from Experiment 3 Sucrose concentration (mol/l)
Tth ⫾ SD (°C)
Th ⫾ SD (°C)
Tab ⫾ SD (°C)
n
1
Landing Departure
37.6 ⫾ 1.1 39.6 ⫾ 1.0
34.6 ⫾ 0.8 33.8 ⫾ 1.0
29.8 ⫾ 0.9 30.8 ⫾ 0.7
32 41
0.5
Landing Departure
37.4 ⫾ 0.8 38.7 ⫾ 0.7
33.9 ⫾ 0.9 32.8 ⫾ 0.7
29.6 ⫾ 0.6 30.6 ⫾ 0.4
33 44
1a
Landing Departure
37.8 ⫾ 0.9 39.4 ⫾ 0.8
33.2 ⫾ 0.7 32.1 ⫾ 0.7
29.0 ⫾ 0.5 30.3 ⫾ 0.5
21 23
2
Landing Departure
37.4 ⫾ 0.9 40.3 ⫾ 1.1
33.4 ⫾ 0.7 32.8 ⫾ 0.7
28.2 ⫾ 0.7 30.8 ⫾ 0.8
15 25
Sucrose concentrations offered in the displayed order (asecond feeding with 1 mol/l). Indicated are means of thorax (Tth), head (Th), abdomen (Tab) and ambient air temperature beside the feeding bowl (Ta) with SD, and number of evaluated thermograms (n), values of Ta and stays at the feeder (N).
However, despite the decrease in sucrose concentration Th remained at 31.7°C (4.2 and 3.1°C above ambient temperature with 1 and 0.5 molar sucrose solution, respectively), and Tab increased from 28.7°C to 29.1°C (1.2 and 0.6°C above Ta, respectively). Thoracic temperature at the final departure was significantly higher (p ⬍ 0.0001) than at initial landing during 1 molar feeding and showed the same but not significant trend during 0.5 molar feeding (Table 1). Inter-individual variability was confirmed by ANOVA for both 0.5 and 1 molar concentration (p ⬍ 0.001). Referring to both concentrations Tth of all six investigated wasps differed at least from one and a maximum of all five other individuals (p ⬍ 0.05; Scheffe’s test). 3.2. Experiment 2
Fig. 1. Body surface temperature of a wasp which interrupted its stays at the feeding bowl in order to fly around the feeding place while gathering sucrose solutions of different concentrations (Experiment 1). Downward arrows indicate landing, upward arrows indicate take-off. Ta ⫽ ambient air temperature beside the feeding bowl.
26.1–29.1°C. In the initial phase of the experiment— during 1 molar feeding—mean thorax temperature of the individual wasps was in the range of 35.5–37.7°C. When the sucrose concentration was lowered to 0.5 mol/l mean thoracic surface temperatures decreased to 33.4–36.7°C. Average thorax temperature of all animals during 1 molar feeding was 37.0°C. During 0.5 molar feeding it decreased by 1.7°C to 35.3°C (Table 1; p ⬍ 0.0001).
Offering a 0.5 molar solution first and a 1 molar solution afterwards produced similar results with the exception that—according to the lower ambient temperature of 17.6–21.0°C—the temperatures of all body parts were significantly lower (p ⬍ 0.0001). Thoracic surface temperature ranged from 31.5 to 38.0°C. During 0.5 molar feeding mean thorax temperature of the individual wasps ranged from 34.0 to 36.8°C. When the sucrose concentration was increased to 1 mol/l in the second phase of the experiment mean thoracic surface temperatures increased to 35.4 to 37.5°C. Average thorax temperature of all animals was 34.7°C during 0.5 molar and 1.4°C higher (36.1°C) during 1 molar feeding (Table 1; p ⬍ 0.0001). Average Th increased by 1.4°C and Tab increased by 2.0°C. However, the difference of Th and Tab to Ta (9.2 and 10.0°C for Th, and 5.3 and 5.7°C for Tab at both concentrations, respectively) was significantly higher than at the higher Ta in Experiments 1 and 3 (p ⬍ 0.0001). With both concentrations thoracic tem-
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investigated wasps differed from one to three other individuals (p ⬍ 0.05; Scheffe’s test). 3.3. Experiment 3 Thoracic surface temperature ranged from 34.6 to 42.1°C at ambient temperatures of 28.5–30.2°C. The four individuals showed different thoracic temperature levels (Fig. 3a and Table 2). During initial feeding with 1 mol/l sucrose, for instance, mean thorax temperature (averaged over all visits) of wasp no. 1 was calculated as 39.9°C whereas in wasp no. 4 it amounted only to 37.8°C (Table 2). Inter-individual variability could be confirmed by ANOVA for each concentration (p ⬍ 0.0001). Referring to all concentrations in six of 16 cases (four individuals tested in four experimental periods) mean Tth of all four investigated individuals differed from that of all three other wasps, and in 10 cases mean
Fig. 2. Body surface temperature of wasp no. 1 from Table 2 and Fig. 3 which did not interrupt its stays at the feeding bowl while gathering sucrose solutions of different concentrations (Experiment 3). Downward arrows indicate landing, upward arrows indicate take-off. Ta ⫽ ambient air temperature beside the feeding bowl.
perature at final departure was similar to or slightly higher but not significantly different from the temperature at initial landing (Table 1). Inter-individual variability was confirmed by ANOVA for both 1 and 0.5 molar concentration (p ⬍ 0.0001). Referring to both concentrations Tth of four of the six
Fig. 3. Effect of concentration of sucrose solution on thorax surface temperature of the four wasps from Experiment 3. Sucrose concentrations offered in the order indicated in the figure (* marks second feeding with 1 mol/l). Vertical bars indicate SD. (a) Differences between neighboring concentrations were always significant at p ⬍ 0.05 except for the difference between 0.5 mol/l and 1 mol/l* in wasp 2 (Kolmogorov–Smirnov test). (b) Differences between different concentrations significant at p ⬍ 0.0001. For number of measurements, and head, abdominal and ambient temperature see Table 2.
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Tth of each individual differed at least from that of two other wasps (p ⬍ 0.05; Scheffe’s test). Nevertheless, the reaction to changes in sucrose concentration was similar in all four animals (Fig. 3a). When the sucrose concentration was lowered they reacted by a decrease and when it was increased they reacted by an increase of thoracic temperature. Only in one case the temperature difference following an increase from 0.5 to 1 mol/l was not statistically significant (wasp no. 2, Fig. 3a). The average of thoracic temperature of all four wasps (and all visits) was 38.7°C during initial 1 molar feeding, dropped to 38.0°C during 0.5 molar feeding, increased to 38.7°C when the insects were fed 1 molar solution again, and finally increased to 39.1°C during 2 molar feeding (Fig. 3b, Table 2). Final departure temperature was in all cases significantly higher (p ⬍ 0.0001) than initial landing temperature (Table 3). Mean head temperatures ranged from 31.9 to 34.2°C, which was 3.0 to 4.1°C higher than ambient temperature (Table 2). Mean abdominal temperature (29.2–30.7°C) was only slightly above ambient temperature (0.4–0.7°C, Table 2). The temperature of these body parts did not follow the changes of thoracic temperature according to changes in sucrose concentration closely. Rather, their temperature decreased when the concentration was increased from 0.5 mol/l to 1 mol/l again and only during final feeding with 2 mol/l sucrose Th increased slightly in three of the four individuals. Duration of stay averaged to 31, 28 and 46 s at 0.5, 1 and 2 molar concentration, respectively. There was no obvious correlation between sucrose concentration and duration of the stay except for the fact that the wasps stayed about 15–18 s longer at the feeding place during 2 molar as compared with lower concentrations (p ⬍ 0.0001, Kolmogorov–Smirnov test).
4. Discussion In our experiments the range of thorax temperatures was 31.7–42.1°C at an ambient temperature (Ta) of 26.1– 30.2°C, and it was 31.5–38.0°C at a Ta of 17.6–21.0°C. Averaging these values for individual wasps over the experiments at each sucrose concentration resulted in mean temperatures of 33.4–39.9°C in the higher and 34.0–37.5°C in the lower range of Ta. Thorax temperature of Vespula vulgaris investigated by means of thermocouples during attacking, returning to and leaving of the nest as estimated from the figures of Heinrich (1984) cover similar ranges in the same ranges of Ta (about 30– 42°C). When returning to the nest wasps of the species Vespula germanica investigated by Coelho and Ross (1996) also showed similar temperatures of 33–40°C at a Ta of 28–30°C but somewhat lower values of 25–35°C at a Ta of 18–20°C. In the present investigation it is shown for the first
time that sucrose concentration (food quality) modulates thorax temperature of foraging wasps in a similar way as was reported in several honeybee species outside the nest (Stabentheiner and Schmaranzer, 1986, 1987; Dyer and Seeley, 1987; Schmaranzer and Stabentheiner, 1988; Waddington, 1990; Underwood, 1991) and inside it (Stabentheiner and Hagmu¨ller, 1991; Stabentheiner et al., 1995; Stabentheiner, 1996). An increase of sucrose concentration from 0.5 to 1 mol/l increased thoracic surface temperature by 1.7°C in Experiment 1, 1.4°C in Experiment 2 and 0.7°C in Experiment 3, which is less than in Apis mellifera foragers where the same difference in concentration caused a difference in thoracic temperature of about 2.5°C (Stabentheiner and Schmaranzer, 1988). In honeybee foragers which had returned to the hive the difference in Tth between these two concentrations was 1.5–2.4°C (Stabentheiner and Hagmu¨ller, 1991; Stabentheiner et al., 1995). Increasing sucrose concentration from 1 to 2 mol/l stimulated the wasps to increase thoracic temperature by only 0.4°C, which was the same as was observed in honeybee foragers inside the hive at a slightly higher Ta of about 32.6°C (Stabentheiner et al., 1995). Probably, in addition to Ta and other factors, the influence of food quality caused part of the high variability of Tth in wasps as was found by Heinrich (1984) and Coelho and Ross (1996). However, it has to be noted that in our experiments the concentration effect (0.5–2 mol/l) explains only about 10– 25% of the whole variability of the wasps’ thoracic temperature. In honeybees it could be shown that thoracic temperature depends not only on energy content (sucrose concentration) of the food but, rather, on the general quality of the food source (i.e., profitability of foraging): bees foraging from distant feeding places exhibited lower thorax temperatures upon their return to the hive than bees foraging in the vicinity of the hive (Stabentheiner, 1996). Since the distance of our feeding places from the wasps’ nests was unknown, and because we did not know whether the wasps came from one or several nests this effect could not be investigated in the present experiments. We suggest that the higher thorax temperature during feeding with the higher concentrated sucrose solutions reflects the wasps’ level of excitement and motivation to collect the offered food in a similar way as was previously observed in honeybees (Schmaranzer and Stabentheiner, 1988; Stabentheiner and Hagmu¨ller, 1991). However, initial landing temperature depended significantly on the sucrose concentration only in Experiments 1 and 2 but not in Experiment 3. Therefore, we cannot conclude from the present experiments that the anticipation of the wasps (which repeatedly visited the feeding bowl) was higher at higher concentration because they remembered the food quality from the last trip, as was
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hypothesized in honeybees (Schmaranzer and Stabentheiner, 1988). With 2 molar concentration the wasps’ stays lasted longer than with lower concentrations (compare Fig. 2), though, according to the high energy content of the food, a high foraging motivation should have stimulated them to gather the solution as fast as possible. Probably the high viscosity of the sucrose solution, which increases exponentially with concentration, decreased sucking speed with the 2 molar solution and this way delayed take-off in a similar way as was reported in honeybees (Waddington, 1990), independent of the wasps’ foraging motivation. The present results raise the question of the biological significance of the modulation of thorax temperature caused by food quality in wasps. Small endothermic animals like wasps have to cope with a high energy loss (Coelho and Ross, 1996) because of their unfavorable volume to surface ratio. Foraging, therefore, should be kept as short as possible to minimize energetic investment. If the food is of a high quality (e.g., contains much sugar) more energy can be invested to harvest it as fast as possible. If energetic gain is small (e.g., sugar content is low) investments are less profitable and body temperature has to be reduced to balance the ratio of gain to costs of foraging. In this case search for alternative food sources becomes more important. It is known that the power output of insect flight muscles correlates positively with flight muscle temperature in a considerable range (Esch, 1976; Coelho, 1991; Marden, 1995). The same might be expected for the thoracic leg muscles (Stabentheiner, 1996). The higher temperature of thoracic flight muscles, therefore, is supposed to allow faster movement, and facilitate take-off and at least the initial phase of flight. Flying honeybees increase energy investment with weight (Wolf et al., 1989). In wasps (Paravespula vulgaris, P. germanica), however, Pflumm (1977) found no difference in load per trip with different concentrations of sucrose solution. This suggests that in the present observations it was not a higher weight which stimulated the wasps to heat their thorax towards final departure to higher levels at higher concentrations. However, further experiments with parallel measurement of body temperature and load per trip at different sucrose concentrations will be needed to solve this question. Infrared thermography allowed analysis of temperature changes not only in the thorax, but also in other body parts. Head temperature (Th), for instance, was usually highest on landing and decreased during the stay (Figs. 1 and 2 and Tables 1–3). We suggest that Th was higher on landing than during the subsequent stay not only because of a higher rate of heat production but also because of an increased haemolymph circulation during the preceding flight to supply the thoracic flight muscles with sufficient energy, which transported a higher
189
amount of heat to the head. During the stay at the feeding bowl an increased haemolymph circulation probably was not necessary. In both head and abdomen changes of food quality (sucrose concentration) had no clear effect on temperature. For example, when the sucrose concentration was increased from 0.5 to 1 mol/l in experiment 3 Th and Tab decreased slightly though Tth increased. Only the subsequent increase of sucrose concentration to 2 mol/l caused a slight increase of Th. Changes in blood circulation after landing and during sucking at the feeder might account for this partial uncoupling of head and abdominal temperature from Tth. The difference between ambient temperature and the mean temperatures of head and abdomen was significantly higher in the lower range of ambient temperatures (compare Experiment 2 with Experiments 1 and 3, Tables 1–3). At the lower ambient temperature the wasps pumped more heat from the thorax to the head and the abdomen. A similar effect was observed in honeybees which were returning to the hive (Cooper et al., 1985) or foraging on flowers (Kovac and Schmaranzer, 1996). This demonstrates again that Paravespula vulgaris is able to change blood circulation if necessary. The purpose of this behavior probably is to keep not only the thorax but also the head and the abdomen at a temperature which ensures optimal conditions for physiological processes and proper function of nervous centers. In conclusion it can be stated that the effect of food quality on body temperature can be found in more endothermic hymenopterans than expected: it is not only restricted to honeybees but is part of the thermoregulatory strategy of at least one species of vespine wasps too. In the wasps and honeybees investigated so far, therefore, “heterothermy” obviously means more than to lower body temperature to ambient levels during rest or activities with low energetic demands and to heat thoracic flight muscles to a certain level before flight or during high activity. Paravespula vulgaris, like honeybees, balance energetic investment with profitability of foraging and the needs of flight muscle performance and motility. Acknowledgements This work was supported by the Austrian Fonds zur Fo¨rderung der Wissenschaftlichen Forschung (FWF) and the Bundesministerium fu¨r Umwelt, Jugend und Familie. Thanks are also due to G. Stabentheiner and R. Kabelac for electronics and software support, and to K. Hagmu¨ller for his support of the work. References Coelho, J.R., 1991. The effect of thorax temperature on force production during tethered flight in honeybee (Apis mellifera) drones, workers, and queens. Physiological Zoology 64, 823–835.
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Coelho, J.R., Ross, A.J., 1996. Body temperature and thermoregulation in two species of yellowjackets, Vespula germanica and V. maculifrons. Journal of Comparative Physiology B166, 68–76. Cooper, P.D., Schaffer, W.M., Buchmann, S.L., 1985. Temperature regulation of honey bees (Apis mellifera) foraging in the Sonoran desert. Journal of Experimental Biology 114, 1–15. Dyer, C.D., Seeley, T.D., 1987. Interspecific comparison of endothermy in honey-bees (Apis): deviations from the expected sizerelated patterns. Journal of Experimental Biology 127, 1–26. Esch, H., 1976. Body temperature and flight performance of honey bees in a servomechanically controlled wind tunnel. Journal of Comparative Physiology 109, 254–277. Heinrich, B., 1984. Strategies of thermoregulation and foraging in two vespid wasps, Dolichovespula maculata and Vespula vulgaris. Journal of Comparative Physiology B154, 175–180. Heinrich, B., 1993. The Hot-blooded Insects: Strategies and Mechanisms of Thermoregulation. Springer, Berlin. Himmer, A., 1932. Die Temperaturverha¨ltnisse bei den sozialen Hymenopteren. Biological Reviews 7, 224–253. Ishay, J., Ruttner, F., 1971. Thermoregulation im Hornissennest. Zeitschrift fu¨r vergleichende Physiologie 72, 423–434. Kovac, H., Schmaranzer, S., 1996. Thermoregulation of honeybees (Apis mellifera) foraging in spring and summer at different plants. Journal of Insect Physiology 42, 1071–1076. Marden, J.H., 1995. Large-scale changes in thermal sensitivity of flight performance during adult maturation in a dragonfly. Journal of Experimental Biology 198, 2095–2102. Pflumm, W., 1977. Welche Gro¨ßen beeinflußen die Menge der von Bienen und Wespen an der Futterquelle aufgenommenen Zuckerlo¨sung. Apidologie 8, 401–411. Schmaranzer, S., 1983. Thermovision bei trinkenden und tanzenden Honigbienen (Apis mellifera carnica). Verhandlungen der Deutschen Zoologischen Gesellschaft 76, 319.
Schmaranzer, S., Stabentheiner, A., 1988. Variability of the thermal behaviour of honeybees on a feeding place. Journal of Comparative Physiology B158, 135–141. Stabentheiner, A., 1996. Effect of foraging distance on the thermal behavior of honeybees during dancing, walking and trophallaxis. Ethology 102, 360–370. Stabentheiner, A., Hagmu¨ller, K., 1991. Sweet food means “hot dancing” in honey bees. Naturwissenschaften 78, 471–473. Stabentheiner, A., Schmaranzer, S., 1986. Thermografie bei Bienen: Ko¨rpertemperaturen am Futterplatz und im “Bienenbart”. Verhandlungen der Deutschen Zoologischen Gesellschaft 79, 417–418. Stabentheiner, A., Schmaranzer, S., 1987. Thermographic determination of body temperatures in honey bees and hornets: calibration and applications. Thermology 2, 563–572. Stabentheiner, A., Schmaranzer, S., 1988. Flight-related thermobiological investigations of honeybees (Apis mellifera carnica). In: Nachtigall, W. (Ed.), BIONA: Report 6, The Flying Honeybee. Akademie der Wissenschaften und Literatur, Mainz and Fischer, Stuttgart, pp. 89–102. Stabentheiner, A., Kovac, H., Hagmu¨ller, K., 1995. Thermal behavior of round and wagtail dancing honeybees. Journal of Comparative Physiology B165, 433–444. Underwood, B.A., 1991. Thermoregulation and energetic decisionmaking by the honeybees Apis cerana, Apis dorsata and Apis laboriosa. Journal of Experimental Biology 157, 19–34. Waddington, K., 1990. Foraging profits and thoracic temperature in honey bees (Apis mellifera). Journal of Comparative Physiology B160, 325–329. Wolf, Th.J., Schmid-Hempel, P., Ellington, C.P., Stevenson, R.D., 1989. Physiological correlates of foraging efforts in honey-bees: oxygen consumption and nectar load. Functional Ecology 3, 417–424.
Effect of food quality on the body temperature of wasps (Paravespula vulgaris) Helmut Kovac, Anton Stabentheiner
*
Institut fu¨r Zoologie, Karl-Franzens-Universita¨t Graz, Universita¨tsplatz 2, A-8010 Graz, Austria Received 21 April 1998; accepted 16 July 1998
Abstract Body surface temperature of individually marked wasps (Paravespula vulgaris, Vespidae, Hymenoptera) was measured by infrared thermography during repeated visits to a feeding bowl without injuring them or disturbing their behavior. Wasps were fed 0.5, 1 and 2 mol/l sucrose solution at two ambient temperatures. Thoracic temperature varied significantly in dependence on food quality (sucrose concentration of solution). At the higher ambient temperatures of 26.1–30.2°C mean thoracic surface temperatures from different experiments were 35.3 and 38.0°C when the wasps took a 0.5 mol/l sucrose solution, 37.0, 38.7 and 38.7°C when they took a 1 mol/l solution, and 39.1°C when they took a 2 mol/l sucrose solution. At the lower ambient temperatures of 17.6–21.0°C thoracic temperatures were lower but the effect of different sucrose concentrations was similar: 34.7°C with a 0.5 mol/l and 36.1°C with a 1 mol/l sucrose solution. The concentration effect amounted to about 10–25% of the whole variability of thorax temperature. By contrast, the temperatures of the head and abdomen did not follow the changes in thorax temperature according to changes in sucrose concentration closely, which suggests that the pattern of haemolymph circulation may have changed after landing, during the wasps’ stay at the feeder. At initial landing at the feeders thoracic temperatures where equal to (three of eight tests) or lower (five of eight tests) than at final departure. The correlation of thorax temperature with food quality probably reflects the wasps’ level of excitement and motivation to collect the food, which allows them to balance energetic investment with profitability of foraging and the needs of flight muscle performance and motility. 1999 Elsevier Science Ltd. All rights reserved. Keywords: Insect; Wasp; Food quality; Thermoregulation; Thermography
1. Introduction Wasps of the subfamily Vespinae are well known for their faculty of thermoregulation. Because of their pronounced capacity for endothermic heat production they are not only able to increase body temperature well above ambient levels (Heinrich, 1984; Coelho and Ross, 1996) but also to regulate the temperature of their nests (Himmer, 1932; Ishay and Ruttner, 1971). Outside the nest they keep thoracic temperature at a high level to ensure proper function of their flight muscles, which allows them to forage at temperatures as low as 4°C (Heinrich, 1984, 1993; Coelho and Ross, 1996). In general, vespine wasps are considered as heterothermic insects which lower thoracic temperature to near ambient levels during periods of rest or little activity and increase * Corresponding author.
it when preparing for flight or during periods of high activity. However, they are not heterothermic in a sense that during periods of high activity they increase thoracic temperature to a certain level. Rather, the level at which they regulate the temperature of their thorax during periods of high activity has been shown to depend on what they are doing: Heinrich (1984) demonstrated that temperatures were in part different in wasps leaving the nest or returning to it, or in attacking animals. Considerable variation of body temperature was also observed by Coelho and Ross (1996). Since only part of the variation can be explained by the effect of ambient temperature or the behavioral situation (Heinrich, 1984; Coelho and Ross, 1996) we suggested that there must be additional factors which influence regulation of body temperature. In several species of the genus Apis it has been demonstrated that food quality (e.g., sugar concentration and foraging distance) is another factor which modulates the thermal behavior
0022–1910/99/$ - see front matter 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 2 - 1 9 1 0 ( 9 8 ) 0 0 1 1 5 - 2
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of honeybees (Stabentheiner and Schmaranzer, 1986; Dyer and Seeley, 1987; Schmaranzer and Stabentheiner, 1988; Waddington, 1990; Stabentheiner and Hagmu¨ller, 1991; Underwood, 1991; Stabentheiner et al., 1995; Stabentheiner, 1996). Unlike the honeybees the Vespinae forage for insects and flesh to rear their larvae. However, they also gather sugared fluids like honeydew produced by aphids, nectar from flowers or sweet syrup from fruits, which makes them easily trainable to artificial sugar sources. In the present paper we investigated the question of whether the sugar content of the food—as a measure of food quality—may act as a modulator of the thermal behavior of wasps.
2. Materials and methods Common yellowjackets (Paravespula vulgaris, Vespidae, Hymenoptera) were trained to visit a feeding place which was protected from wind and solar radiation on three days of August 1989 and 1992 at two levels of ambient temperature (17.6–21.0°C and 26.1–30.2°C). They were marked individually by color dots applied to their abdomen. In a glass jar inverted over a grooved glass base they were offered sucrose solution of 0.5–2 molar concentration which they could gather ad libitum. Three experiments were performed in this manner. Experiment 1 (1989): In the beginning six wasps were offered sucrose solution of 1 mol/l concentration because with this concentration the wasps could be more easily attracted to the feeding bowl than with lower ones. After about 2 h the concentration was lowered to 0.5 mol/l. Experiment 2 (1989): Six wasps were offered 0.5 mol/l solution first and 1 mol/l solution after about 2 h. Experiment 3 (1992): Four wasps were investigated at a location 10 km apart from that of Experiments 1 and 2. They received 1 mol/l sucrose in the beginning, the concentration of which was lowered to 0.5 mol/l after about 1 h. Another hour later the concentration was again increased to 1 mol/l. Towards the end of the experiment the concentration was increased to 2 mol/l. In order to allow undisturbed, simultaneous and repeated measurement of the temperature of different body parts (head, thorax, abdomen) the method of infrared thermography was used (Schmaranzer, 1983; Stabentheiner and Schmaranzer, 1987). With this method it is possible to determine the body surface temperature from the infrared radiation emitted by an insect’s body. The real-time infrared camera (AGA 782 SW) enabled us to monitor temporal changes of body surface temperature and to perform repeated measurements on the same individual. The thermographic scenes were stored on videotape for later analysis. Thermograms were taken from the videotapes in intervals of 3–8 s, depending on whether the wasps were visible in the infrared image and all body parts were in focus. Because of different
durations of stay at the feeding bowl differences in sample sizes occurred for different feeding bouts. The infrared radiation emitted by the wasps was compared with the radiation of an AGA 1010 reference source, which was precision calibrated against a black body radiator of our own construction. The temperature of the black body radiator was kept constant with an accuracy of ⬍ 0.05°C (Stabentheiner and Schmaranzer, 1987). Since the emissivity of the wasp cuticle was not known we used the value of 0.97 determined in honeybees by simultaneous registration of infrared radiation and surface temperature by means of micro thermocouples (diameter of wires: 0.05 mm) to calculate absolute surface temperatures (for details see Stabentheiner and Schmaranzer, 1987). This seemed to be safe because a very similar value of 0.965 was determined in the European cockchafer Melolontha melolontha (diameter of thermocouple wires: 0.012 mm; Stabentheiner, unpublished measurements). In this way, self-written PC software allowed calculation of absolute body surface temperatures with an accuracy of 0.5°C and relative (comparative) measurements to the nearest 0.2°C. Ambient temperature (Ta) was measured beside the feeding bowl by means of a Technoterm 9400 digital thermometer. To test for intra-individual variation caused by changes in sucrose concentration non-parametric statistics were used: Kruskal–Wallis H test and, for comparison between different concentrations, the Kolmogorov–Smirnov test. Inter-individual variability was tested by ANOVA and Scheffe’s test. Statistics are based on evaluated temperature values (n in Tables 1–3).
3. Results The wasps stayed at the feeding bowl for about 20– 120 s. Feeding was sometimes interrupted by short flights around the bowl, after which the insects resumed foraging (Fig. 1). Fig. 2 shows typical temperature curves of one wasp (from Experiment 3) gathering sucrose solution of different concentrations which did not interrupt its stays. Thorax temperature (Tth) was either kept constant or increased up to 2°C during the insects’ stay at the feeding bowl (Figs. 1 and 2). Especially before take-off a slight increase was often observed. The temperature of the head (Th) mostly decreased after landing and then remained more or less stable during the rest of the stay. Abdominal temperature (Tab) mostly was lowest at landing and increased towards the wasps’ departure (Figs. 1 and 2). 3.1. Experiment 1 Thoracic surface temperature of the wasps ranged from 31.7 to 39.9°C at ambient temperatures (Ta) of
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Table 1 Body surface temperatures of wasps (Paravespula vulgaris) from Experiments 1 and 2 Sucrose Experiment no. concentration (mol/l) Experiment 1
1
0.5
Experiment 2
0.5
1
Tth ⫾ SD (°C) Th ⫾ SD (°C) Tab ⫾ SD (°C) n
Ta ⫾ SD (°C) N
Mean Landing Departure Mean Landing Departure
37.0 36.2 37.5 35.2 35.3 35.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.2 0.8 1.3 1.2 0.6 1.7
31.7 32.7 31.3 31.6 32.6 31.1
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.2 0.7 1.2 0.9 0.6 0.8
28.7 27.9 29.2 29.1 28.6 29.4
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
0.8 0.4 0.6 0.6 0.5 0.4
187 32 32 278 21 21
Mean Landing Departure Mean Landing Departure
34.7 34.0 34.5 36.1 36.0 35.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.3 1.4 1.7 0.7 0.7 0.7
27.5 28.8 26.3 28.9 30.7 27.6
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
1.5 1.4 1.3 1.6 1.1 0.7
23.6 23.6 24.0 25.6 25.2 25.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾
0.7 0.7 0.8 0.6 0.7 0.6
190 11 11 147 16 21
27.5 ⫾ 0.4
33
28.5 ⫾ 0.6
21
18.3 ⫾ 0.4
11
19.9 ⫾ 0.6
22
Sucrose concentrations offered in the displayed order. Indicated are means of thorax (Tth), head (Th) and abdomen (Tab), mean temperatures during initial landing and final departure, ambient air temperature beside the feeding bowl (Ta) with SD, and number of evaluated thermograms (n), values of Ta and stays at the feeder (N).
Table 2 Body surface temperatures of wasps (Paravespula vulgaris) from Experiment 3
Animal
Sucrose concentration (mol/l)
Tth ⫾ SD (°C)
Th ⫾ SD (°C)
Tab ⫾ SD (°C)
Ta ⫾ SD (°C)
n
N
Wasp 1
1 0.5 1a 2
39.9 38.5 39.6 39.8
⫾ ⫾ ⫾ ⫾
0.9 0.7 0.7 1.0
34.0 33.4 32.8 33.5
⫾ ⫾ ⫾ ⫾
0.9 0.8 0.6 0.6
30.7 30.4 30.2 30.2
⫾ ⫾ ⫾ ⫾
0.7 0.5 0.6 1.2
63 94 47 64
29.8 29.6 29.5 29.1
⫾ ⫾ ⫾ ⫾
0.2 0.3 0.1 0.3
11 12 6 6
Wasp 2
1 0.5 1a 2
38.7 38.3 38.4 38.7
⫾ ⫾ ⫾ ⫾
0.7 0.6 0.7 1.0
34.2 33.4 32.6 33.0
⫾ ⫾ ⫾ ⫾
0.9 0.8 0.7 0.6
30.5 30.4 29.8 29.7
⫾ ⫾ ⫾ ⫾
0.9 0.5 0.7 1.1
73 84 45 68
29.8 29.5 29.4 29.0
⫾ ⫾ ⫾ ⫾
0.2 0.2 0.1 0.2
12 10 6 8
Wasp 3
1 0.5 1a 2
38.4 37.9 38.7 39.8
⫾ ⫾ ⫾ ⫾
1.2 0.6 0.8 1.4
34.2 33.4 32.6 32.6
⫾ ⫾ ⫾ ⫾
0.8 0.7 0.6 0.5
30.0 30.0 29.6 29.2
⫾ ⫾ ⫾ ⫾
1.0 0.6 0.5 1.2
74 106 40 37
29.9 29.5 29.5 29.2
⫾ ⫾ ⫾ ⫾
0.2 0.1 0.1 0.4
13 14 6 5
Wasp 4
1 0.5 1a 2
37.8 37.3 37.9 38.2
⫾ ⫾ ⫾ ⫾
1.1 0.9 1.0 1.3
33.5 32.6 31.9 32.2
⫾ ⫾ ⫾ ⫾
0.9 0.8 0.6 0.6
29.9 29.8 29.5 29.4
⫾ ⫾ ⫾ ⫾
0.7 0.7 0.7 0.8
61 76 45 42
29.9 29.6 29.4 29.0
⫾ ⫾ ⫾ ⫾
0.3 0.2 0.1 0.2
10 10 6 7
All wasps
1 0.5 1a 2
38.7 38.0 38.7 39.1
⫾ ⫾ ⫾ ⫾
1.2 0.8 1.0 1.3
34.0 33.2 32.5 32.9
⫹ ⫹ ⫹ ⫹
0.9 0.8 0.7 0.7
30.3 30.1 29.8 29.8
⫹ ⫹ ⫹ ⫹
0.9 0.6 0.7 1.5
271 360 177 211
29.9 29.5 29.5 29.1
⫾ ⫾ ⫾ ⫾
0.2 0.2 0.1 0.3
46 46 24 26
Sucrose concentrations offered in the displayed order (asecond feeding with 1 mol/l). Indicated are means of thorax (Tth), head (Th), abdomen (Tab) and ambient air temperature beside the feeding bowl (Ta) with SD, and number of evaluated thermograms (n), values of Ta and stays at the feeder (N).
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Table 3 Body surface temperatures of all wasps (Paravespula vulgaris) during initial landing and final departure from Experiment 3 Sucrose concentration (mol/l)
Tth ⫾ SD (°C)
Th ⫾ SD (°C)
Tab ⫾ SD (°C)
n
1
Landing Departure
37.6 ⫾ 1.1 39.6 ⫾ 1.0
34.6 ⫾ 0.8 33.8 ⫾ 1.0
29.8 ⫾ 0.9 30.8 ⫾ 0.7
32 41
0.5
Landing Departure
37.4 ⫾ 0.8 38.7 ⫾ 0.7
33.9 ⫾ 0.9 32.8 ⫾ 0.7
29.6 ⫾ 0.6 30.6 ⫾ 0.4
33 44
1a
Landing Departure
37.8 ⫾ 0.9 39.4 ⫾ 0.8
33.2 ⫾ 0.7 32.1 ⫾ 0.7
29.0 ⫾ 0.5 30.3 ⫾ 0.5
21 23
2
Landing Departure
37.4 ⫾ 0.9 40.3 ⫾ 1.1
33.4 ⫾ 0.7 32.8 ⫾ 0.7
28.2 ⫾ 0.7 30.8 ⫾ 0.8
15 25
Sucrose concentrations offered in the displayed order (asecond feeding with 1 mol/l). Indicated are means of thorax (Tth), head (Th), abdomen (Tab) and ambient air temperature beside the feeding bowl (Ta) with SD, and number of evaluated thermograms (n), values of Ta and stays at the feeder (N).
However, despite the decrease in sucrose concentration Th remained at 31.7°C (4.2 and 3.1°C above ambient temperature with 1 and 0.5 molar sucrose solution, respectively), and Tab increased from 28.7°C to 29.1°C (1.2 and 0.6°C above Ta, respectively). Thoracic temperature at the final departure was significantly higher (p ⬍ 0.0001) than at initial landing during 1 molar feeding and showed the same but not significant trend during 0.5 molar feeding (Table 1). Inter-individual variability was confirmed by ANOVA for both 0.5 and 1 molar concentration (p ⬍ 0.001). Referring to both concentrations Tth of all six investigated wasps differed at least from one and a maximum of all five other individuals (p ⬍ 0.05; Scheffe’s test). 3.2. Experiment 2
Fig. 1. Body surface temperature of a wasp which interrupted its stays at the feeding bowl in order to fly around the feeding place while gathering sucrose solutions of different concentrations (Experiment 1). Downward arrows indicate landing, upward arrows indicate take-off. Ta ⫽ ambient air temperature beside the feeding bowl.
26.1–29.1°C. In the initial phase of the experiment— during 1 molar feeding—mean thorax temperature of the individual wasps was in the range of 35.5–37.7°C. When the sucrose concentration was lowered to 0.5 mol/l mean thoracic surface temperatures decreased to 33.4–36.7°C. Average thorax temperature of all animals during 1 molar feeding was 37.0°C. During 0.5 molar feeding it decreased by 1.7°C to 35.3°C (Table 1; p ⬍ 0.0001).
Offering a 0.5 molar solution first and a 1 molar solution afterwards produced similar results with the exception that—according to the lower ambient temperature of 17.6–21.0°C—the temperatures of all body parts were significantly lower (p ⬍ 0.0001). Thoracic surface temperature ranged from 31.5 to 38.0°C. During 0.5 molar feeding mean thorax temperature of the individual wasps ranged from 34.0 to 36.8°C. When the sucrose concentration was increased to 1 mol/l in the second phase of the experiment mean thoracic surface temperatures increased to 35.4 to 37.5°C. Average thorax temperature of all animals was 34.7°C during 0.5 molar and 1.4°C higher (36.1°C) during 1 molar feeding (Table 1; p ⬍ 0.0001). Average Th increased by 1.4°C and Tab increased by 2.0°C. However, the difference of Th and Tab to Ta (9.2 and 10.0°C for Th, and 5.3 and 5.7°C for Tab at both concentrations, respectively) was significantly higher than at the higher Ta in Experiments 1 and 3 (p ⬍ 0.0001). With both concentrations thoracic tem-
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investigated wasps differed from one to three other individuals (p ⬍ 0.05; Scheffe’s test). 3.3. Experiment 3 Thoracic surface temperature ranged from 34.6 to 42.1°C at ambient temperatures of 28.5–30.2°C. The four individuals showed different thoracic temperature levels (Fig. 3a and Table 2). During initial feeding with 1 mol/l sucrose, for instance, mean thorax temperature (averaged over all visits) of wasp no. 1 was calculated as 39.9°C whereas in wasp no. 4 it amounted only to 37.8°C (Table 2). Inter-individual variability could be confirmed by ANOVA for each concentration (p ⬍ 0.0001). Referring to all concentrations in six of 16 cases (four individuals tested in four experimental periods) mean Tth of all four investigated individuals differed from that of all three other wasps, and in 10 cases mean
Fig. 2. Body surface temperature of wasp no. 1 from Table 2 and Fig. 3 which did not interrupt its stays at the feeding bowl while gathering sucrose solutions of different concentrations (Experiment 3). Downward arrows indicate landing, upward arrows indicate take-off. Ta ⫽ ambient air temperature beside the feeding bowl.
perature at final departure was similar to or slightly higher but not significantly different from the temperature at initial landing (Table 1). Inter-individual variability was confirmed by ANOVA for both 1 and 0.5 molar concentration (p ⬍ 0.0001). Referring to both concentrations Tth of four of the six
Fig. 3. Effect of concentration of sucrose solution on thorax surface temperature of the four wasps from Experiment 3. Sucrose concentrations offered in the order indicated in the figure (* marks second feeding with 1 mol/l). Vertical bars indicate SD. (a) Differences between neighboring concentrations were always significant at p ⬍ 0.05 except for the difference between 0.5 mol/l and 1 mol/l* in wasp 2 (Kolmogorov–Smirnov test). (b) Differences between different concentrations significant at p ⬍ 0.0001. For number of measurements, and head, abdominal and ambient temperature see Table 2.
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Tth of each individual differed at least from that of two other wasps (p ⬍ 0.05; Scheffe’s test). Nevertheless, the reaction to changes in sucrose concentration was similar in all four animals (Fig. 3a). When the sucrose concentration was lowered they reacted by a decrease and when it was increased they reacted by an increase of thoracic temperature. Only in one case the temperature difference following an increase from 0.5 to 1 mol/l was not statistically significant (wasp no. 2, Fig. 3a). The average of thoracic temperature of all four wasps (and all visits) was 38.7°C during initial 1 molar feeding, dropped to 38.0°C during 0.5 molar feeding, increased to 38.7°C when the insects were fed 1 molar solution again, and finally increased to 39.1°C during 2 molar feeding (Fig. 3b, Table 2). Final departure temperature was in all cases significantly higher (p ⬍ 0.0001) than initial landing temperature (Table 3). Mean head temperatures ranged from 31.9 to 34.2°C, which was 3.0 to 4.1°C higher than ambient temperature (Table 2). Mean abdominal temperature (29.2–30.7°C) was only slightly above ambient temperature (0.4–0.7°C, Table 2). The temperature of these body parts did not follow the changes of thoracic temperature according to changes in sucrose concentration closely. Rather, their temperature decreased when the concentration was increased from 0.5 mol/l to 1 mol/l again and only during final feeding with 2 mol/l sucrose Th increased slightly in three of the four individuals. Duration of stay averaged to 31, 28 and 46 s at 0.5, 1 and 2 molar concentration, respectively. There was no obvious correlation between sucrose concentration and duration of the stay except for the fact that the wasps stayed about 15–18 s longer at the feeding place during 2 molar as compared with lower concentrations (p ⬍ 0.0001, Kolmogorov–Smirnov test).
4. Discussion In our experiments the range of thorax temperatures was 31.7–42.1°C at an ambient temperature (Ta) of 26.1– 30.2°C, and it was 31.5–38.0°C at a Ta of 17.6–21.0°C. Averaging these values for individual wasps over the experiments at each sucrose concentration resulted in mean temperatures of 33.4–39.9°C in the higher and 34.0–37.5°C in the lower range of Ta. Thorax temperature of Vespula vulgaris investigated by means of thermocouples during attacking, returning to and leaving of the nest as estimated from the figures of Heinrich (1984) cover similar ranges in the same ranges of Ta (about 30– 42°C). When returning to the nest wasps of the species Vespula germanica investigated by Coelho and Ross (1996) also showed similar temperatures of 33–40°C at a Ta of 28–30°C but somewhat lower values of 25–35°C at a Ta of 18–20°C. In the present investigation it is shown for the first
time that sucrose concentration (food quality) modulates thorax temperature of foraging wasps in a similar way as was reported in several honeybee species outside the nest (Stabentheiner and Schmaranzer, 1986, 1987; Dyer and Seeley, 1987; Schmaranzer and Stabentheiner, 1988; Waddington, 1990; Underwood, 1991) and inside it (Stabentheiner and Hagmu¨ller, 1991; Stabentheiner et al., 1995; Stabentheiner, 1996). An increase of sucrose concentration from 0.5 to 1 mol/l increased thoracic surface temperature by 1.7°C in Experiment 1, 1.4°C in Experiment 2 and 0.7°C in Experiment 3, which is less than in Apis mellifera foragers where the same difference in concentration caused a difference in thoracic temperature of about 2.5°C (Stabentheiner and Schmaranzer, 1988). In honeybee foragers which had returned to the hive the difference in Tth between these two concentrations was 1.5–2.4°C (Stabentheiner and Hagmu¨ller, 1991; Stabentheiner et al., 1995). Increasing sucrose concentration from 1 to 2 mol/l stimulated the wasps to increase thoracic temperature by only 0.4°C, which was the same as was observed in honeybee foragers inside the hive at a slightly higher Ta of about 32.6°C (Stabentheiner et al., 1995). Probably, in addition to Ta and other factors, the influence of food quality caused part of the high variability of Tth in wasps as was found by Heinrich (1984) and Coelho and Ross (1996). However, it has to be noted that in our experiments the concentration effect (0.5–2 mol/l) explains only about 10– 25% of the whole variability of the wasps’ thoracic temperature. In honeybees it could be shown that thoracic temperature depends not only on energy content (sucrose concentration) of the food but, rather, on the general quality of the food source (i.e., profitability of foraging): bees foraging from distant feeding places exhibited lower thorax temperatures upon their return to the hive than bees foraging in the vicinity of the hive (Stabentheiner, 1996). Since the distance of our feeding places from the wasps’ nests was unknown, and because we did not know whether the wasps came from one or several nests this effect could not be investigated in the present experiments. We suggest that the higher thorax temperature during feeding with the higher concentrated sucrose solutions reflects the wasps’ level of excitement and motivation to collect the offered food in a similar way as was previously observed in honeybees (Schmaranzer and Stabentheiner, 1988; Stabentheiner and Hagmu¨ller, 1991). However, initial landing temperature depended significantly on the sucrose concentration only in Experiments 1 and 2 but not in Experiment 3. Therefore, we cannot conclude from the present experiments that the anticipation of the wasps (which repeatedly visited the feeding bowl) was higher at higher concentration because they remembered the food quality from the last trip, as was
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hypothesized in honeybees (Schmaranzer and Stabentheiner, 1988). With 2 molar concentration the wasps’ stays lasted longer than with lower concentrations (compare Fig. 2), though, according to the high energy content of the food, a high foraging motivation should have stimulated them to gather the solution as fast as possible. Probably the high viscosity of the sucrose solution, which increases exponentially with concentration, decreased sucking speed with the 2 molar solution and this way delayed take-off in a similar way as was reported in honeybees (Waddington, 1990), independent of the wasps’ foraging motivation. The present results raise the question of the biological significance of the modulation of thorax temperature caused by food quality in wasps. Small endothermic animals like wasps have to cope with a high energy loss (Coelho and Ross, 1996) because of their unfavorable volume to surface ratio. Foraging, therefore, should be kept as short as possible to minimize energetic investment. If the food is of a high quality (e.g., contains much sugar) more energy can be invested to harvest it as fast as possible. If energetic gain is small (e.g., sugar content is low) investments are less profitable and body temperature has to be reduced to balance the ratio of gain to costs of foraging. In this case search for alternative food sources becomes more important. It is known that the power output of insect flight muscles correlates positively with flight muscle temperature in a considerable range (Esch, 1976; Coelho, 1991; Marden, 1995). The same might be expected for the thoracic leg muscles (Stabentheiner, 1996). The higher temperature of thoracic flight muscles, therefore, is supposed to allow faster movement, and facilitate take-off and at least the initial phase of flight. Flying honeybees increase energy investment with weight (Wolf et al., 1989). In wasps (Paravespula vulgaris, P. germanica), however, Pflumm (1977) found no difference in load per trip with different concentrations of sucrose solution. This suggests that in the present observations it was not a higher weight which stimulated the wasps to heat their thorax towards final departure to higher levels at higher concentrations. However, further experiments with parallel measurement of body temperature and load per trip at different sucrose concentrations will be needed to solve this question. Infrared thermography allowed analysis of temperature changes not only in the thorax, but also in other body parts. Head temperature (Th), for instance, was usually highest on landing and decreased during the stay (Figs. 1 and 2 and Tables 1–3). We suggest that Th was higher on landing than during the subsequent stay not only because of a higher rate of heat production but also because of an increased haemolymph circulation during the preceding flight to supply the thoracic flight muscles with sufficient energy, which transported a higher
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amount of heat to the head. During the stay at the feeding bowl an increased haemolymph circulation probably was not necessary. In both head and abdomen changes of food quality (sucrose concentration) had no clear effect on temperature. For example, when the sucrose concentration was increased from 0.5 to 1 mol/l in experiment 3 Th and Tab decreased slightly though Tth increased. Only the subsequent increase of sucrose concentration to 2 mol/l caused a slight increase of Th. Changes in blood circulation after landing and during sucking at the feeder might account for this partial uncoupling of head and abdominal temperature from Tth. The difference between ambient temperature and the mean temperatures of head and abdomen was significantly higher in the lower range of ambient temperatures (compare Experiment 2 with Experiments 1 and 3, Tables 1–3). At the lower ambient temperature the wasps pumped more heat from the thorax to the head and the abdomen. A similar effect was observed in honeybees which were returning to the hive (Cooper et al., 1985) or foraging on flowers (Kovac and Schmaranzer, 1996). This demonstrates again that Paravespula vulgaris is able to change blood circulation if necessary. The purpose of this behavior probably is to keep not only the thorax but also the head and the abdomen at a temperature which ensures optimal conditions for physiological processes and proper function of nervous centers. In conclusion it can be stated that the effect of food quality on body temperature can be found in more endothermic hymenopterans than expected: it is not only restricted to honeybees but is part of the thermoregulatory strategy of at least one species of vespine wasps too. In the wasps and honeybees investigated so far, therefore, “heterothermy” obviously means more than to lower body temperature to ambient levels during rest or activities with low energetic demands and to heat thoracic flight muscles to a certain level before flight or during high activity. Paravespula vulgaris, like honeybees, balance energetic investment with profitability of foraging and the needs of flight muscle performance and motility. Acknowledgements This work was supported by the Austrian Fonds zur Fo¨rderung der Wissenschaftlichen Forschung (FWF) and the Bundesministerium fu¨r Umwelt, Jugend und Familie. Thanks are also due to G. Stabentheiner and R. Kabelac for electronics and software support, and to K. Hagmu¨ller for his support of the work. References Coelho, J.R., 1991. The effect of thorax temperature on force production during tethered flight in honeybee (Apis mellifera) drones, workers, and queens. Physiological Zoology 64, 823–835.
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