Temperature Regulation in Bee- and Wasp-Mimicking Syrphid Flies

Adult syrphid flies (Diptera: Syrphidae) visit flowers to forage for nectar and pollen and to search for mates. Their importance as pollinators is second only to that of bees (Curran, 1934; Kevan & Baker, 1983). Many syrphids are exceptionally accurate visual mimics of aculeate Hymenoptera. Bumblebee mimics are covered with thick pile whereas mimics of vespid wasps and non-mimetic species are glabrous or have relatively sparse pile. In spite of the variety and abundance of Syrphidae, they have not been intensively studied. In particular, the ability of these flies to hermoregulate during activity is poorly understood.

Many bees and wasps foraging at the same flowers as syrphid flies maintain high body temperatures during activity, using metabolically generated heat (Heinrich, 1983; Heinrich & Heinrich, 1983). Their endothermy permits some of them to be active at ambient temperatures near 0°C. At our study site the largest syrphids are the same size as the smallest bumblebees and wasps, whereas the smallest are considerably smaller than any previously studied endothermic hymenopteran. We here examine thermoregulation in a variety of syrphid flies and compare thermoregulation in the flies and their hymenopteran models.

We obtained data on 12 species of syrphids ranging in body mass from 0·05 to 0·33g (see Table 1 for species names). Most were collected near Weld, Maine, while some Crysotoxum sp. were collected near Richmond, Vermont. The flies were studied from May to August 1985, inclusive, with preliminary data collected during the summer of 1983. Bees and wasps were also collected in Weld. The insects were kept in airtight vials and were weighed (±0·001 g) within several hours of capture.

We measured thoracic temperatures (T_th) in the field using a Sensortek microprobe needle thermocouple (Type MT-2911, time constant = 0·025 s, needle diameter = 0·33 mm). Insects were captured with an aerial net in flight or while perched and the couple was inserted into the centre of the thorax. Measurements were made with the insect immobilized in a pocket of netting to avoid hand contact and to reduce handling time (usually 3–5 s). The thermocouple was dried and air temperature (T_a) was measured in the shade near the site of capture immediately after T_th had been measured. Temperatures were read to the nearest 0·1 °C on a Sensortek Bat-12 thermocouple thermometer that had been calibrated against a mercury thermometer traceable to the US Bureau of Standards.

Syrphid flies for measurements of endothermic warm-up were captured during the afternoon and stored individually at 5 °C until they were used the following morning. A thermocouple (0·03 mm in diameter) was inserted through the dorsolateral thoracic cuticle (couple at midthorax) and fixed in place with a drop of melted beeswax. T_a was measured with a temperature-sensitive integrated circuit (LM334) placed near the insect. Outputs of the thermocouple and the T_a sensor were calibrated against a mercury thermometer. Flies with thermocouple implants were returned to the refrigerator until they were quiescent with T_th below the laboratory T_a (12·3–18·0°C), and were then placed on the laboratory bench under an opaque cup. When T_lh approximated T_a the fly was uncovered and T_lh and T_a were recorded at 2-s intervals by a microcomputer. Warm-up was often initiated upon removal of the cup, but some individuals required gentle prodding.

Freshly-killed syrphid flies were implanted with a thoracic thermocouple as above and heated to about 45 °C using an incandescent lamp. Heated flies were quickly moved into a wind tunnel (wind speed = 5·6 ms⁻¹) and T_th and T_a were recorded at 5-s intervals by a microcomputer. In flies and bumblebees where the thorax was covered with pile, cooling rate was measured first with the pile intact and then again after the pile had been scraped from the thorax.

Data are presented as mean ± standard deviation unless otherwise noted. Student’s t-test (significance level = 0·05) was used to test differences between means and the significance of regressions.

It is common practice to express thermoregulatory ability in terms of the slope of the regression of T_th on T_a. A slope not significantly different from zero indicates excellent thermoregulation, whereas a slope not significantly different from one indicates no thermoregulation. Clearly the accuracy of this test depends on how well the data set represents the thermal relationships of the insect. In some of the less common syrphid species we did not obtain significant regressions, presumably owing to small data sets and large amounts of scatter. For these species we give regression statistics but omit regression lines in Figs 1 and 2. For species where we obtained significant regressions the regression lines are included in those figures.

The syrphids we studied were active at T_a from at least 12·8 to 27·4°C and, over this range, the T_th of four Bombus mimics typically ranged from 25 to 35°C (Fig. 1). Thoracic temperature averaged 9·8–14·6°C above T_a depending on the species. In three of the four species, regressions of T_th on T_a were not significant (Mallota posticata, y = 22·1+0·57x, r² = 0 ·120, N= 12, P = 0 ·33; Criorhina nigriventris, y = 33 ·4 −0 ·24x, r² = 0 ·012, N = 45, P = 0 ·36; Eristalis barda, y = 17·l+0 ·63x, r²= 0 ·260, N = 11, P=0 ·16). In M. bautias, however, a significant regression was obtained (y = 17 ·5+0’86x, r² = 0·511, N = 10, P = 0 ·02) and the slope of the regression relating T_th to T_a was not significantly different from 1 (P = 0 ·65), suggesting that T_th in this species is not actively regulated.

Thoracic temperatures of bumblebee queens and workers (Bombus spp.; presumptive models for the above four syrphids), taken concurrently and at the same locations where the syrphids were studied, averaged 17 ·9±3 ·02°C above T_a (range = 11 ·6–26·5 °C, N=72). Body masses of the bumblebees averaged 0·293 ± 0·127 g (range = 0·050–0·695 g, N = 68).

Thoracic temperatures of four Vespula-mimicking syrphids, one Dolichovespula-mimic and two non-mimetic syrphids, all having little or no thoracic pile, were also elevated (Fig. 2). Thoracic temperatures of these flies averaged 9·9–12·8°C above T_a. The slopes of regressions relating T_lh to T_a for Temnostoma vespiforme and Sericomyia chrysotoxoides (y = 16·2+0·72x, r² = 0·389, N=41, P <0·001 and y = 6·5+l·18x, r² = 0·672, N = 17, P< 0·001, respectively) did not differ signifia cantly from 1 (P=0·06 and P = 0·41, respectively) suggesting that T_th is not regulated in these species. The regression of T_th on T_a was not significant for Eristalis sp. (y = 18·2+0·617x, r² = 0·166,.V = 17, P = 0·13). In both T. alternans and Crysotoxum sp., however, the slopes of the regressions of T_th on T_a were significantly different from 1 (y = 19·0+0·58x, r² = 0·199, N = 43, P = 0·03 and y = 24·7 + 0·3lx, r² = 0·241, V= 32, P< 0·001, respectively) suggesting that T_th is regulated in these species. Regressions were not performed on data for Se. militans and Se. lata due to small sample sizes.

T_th of yellowjacket wasps (Vespula vulgaris; presumptive model for four of the above syrphids) taken concurrently and at the same locations where the syrphids were studied averaged 15·5 ± 5·48°C above T_a (range = 6·5–27·5°C, N = 13). Body masses of the wasps averaged 0·154±0·052g (range = 0·055–0·199g, N=13). Thoracic temperatures of white-faced hornets (Dolichovespula maculata ; presumptive model for one of the above syrphids) averaged 15·5 ±3·46°C above T_a (range = 11–23·5°C, N = 26). Body masses of the hornets averaged 0·291 ± 0·095 g (range = 0·144–0·463g, N = 26).

There were no significant differences in temperature excess (T_th–T_a) correlated with behaviour (e.g. foraging, basking, flight and patrolling, i.e. males searching for females) in the flies we studied. Likewise, there were no significant differences in the temperature excess between pubescent Bombus mimics and glabrous syrphids or between mimetic and non-mimetic syrphids.

Endothermic warm-up was signalled by the onset of periodic abdominal pumping movements. Most flies warmed spontaneously from T_th = T_a (12·3–18·0°C) after initially being gently prodded: warm-up rates ranged from 1·2–5·5°C min⁻¹, and were strongly dependent on body mass (Fig. 4; warm-up rates plotted in this figure were measured at T_a between 15 and 18°C). Some individuals increased T_th only a few degrees while others increased T_th to as high as 15°C above T_a (see, for example, Fig. 3). Warm-up usually ended with a flight attempt, followed by an immediate decline in T_th. The T_th at take-off ranged as follows: Cr. nigriventris, 21·2–27·3°C; M. posticata, 23·5–26·9°C; T. alternans, 18·7–24·l°C; Se. lata, 21·8°C; Sphecomyia vittata, 20·4°C; T. vespiforme, 23·8°C. In some syrphid species (Cr. nigriventris, Se. lata, Sp. vittata, Chrysotoxum sp.) warm-up was accompanied by an audible whining or buzzing; in others (M. posticata, M. bautias, E. barda, T. alternans, T. vespiforme) warm-up was silent. Heinrich & Pantle (1975) noted a correlation between wing movements and noise during warm-up in Syrphus sp. We sometimes noted minute wing movements during audible warm-ups, but the association between wing motion and noise was inconsistent. In any event, it is clear that in many species of syrphids warm-up can be independent of wing movements or noise.

Flies sometimes sustained endothermy beyond the 2–5 min necessary for T_th to reach flight temperature (Fig. 5). One 0·281-g Cr. nigriventris maintained an average T_th–T_a difference of 13·4°C for more than 26min (Fig. 5).

Thermal conductance of Bombus mimics (Cr. nigriventris, M. posticata, M. bautias, E. barda) and Vespula mimics (T. alternans, T. vespiforme) was highly dependent on body mass (Fig. 6), and conductance of Bombus mimics was on the average lower than that of similarly sized Vespula mimics (presumably reflecting the presence of insulating pile in Bombus mimics).

Removal of pile from the thorax of Bombus mimics and Bombus spp. significantly increased thermal conductance (Fig. 7, P<0·01 for all cases). Thermal conductance of Cr. nigriventris increased by an average of 32% after the pile had been removed.

Thermal conductances of the other three Bombus mimics are combined in Fig. 7 because all have similar short, stiff hairs whereas Cr. nigriventris has relatively long hairs. The removal of pile increased thermal conductance of these other Bombus mimics by an average of 30%. Thermal conductance of Bombus queens and workers increased by 25 % under the same conditions after removal of the thoracic pile.

Thermoregulation in flies is of considerable interest because their small size renders them subject to rapid rates of heat exchange while their flight muscles presumably require a high temperature to support their typically high flight speeds. Behavioural thermoregulation tends to be quite important in small, diurnal species. For example, Arctic mosquitoes (Aedes spp.) bask in the parabolic corollas of flowers that provide no nectar (Hocking & Sharplin, 1965). Light-seeking neotropical robber flies and desert robber flies regulate their high body temperatures while foraging largely by microhabitat selection and postural adjustments (Morgan, Shelly &.Kimsey, 1985; K. R. Morgan & T. E. Shelly, in preparation).

Most previous studies of insect endothermy have focused on large moths, bees and beetles. Many dipterans are so small that dependence on metabolically generated heat for thermoregulation has been considered unlikely. In the blowfly (Calliphora), a temperature increase due to endothermy of only 0·75 °C has been measured (Digby, 1955), and thoracic temperature of the sheep blowfly (Phoenicia) remains within 1·5°C of T_a during tethered flight (Yurkiewicz & Smyth, 1966). Nevertheless, some relatively small syrphids (<0·03 g) maintain a high T_th by a combination of shivering and basking while they congregate at leks (Heinrich & Pantle, 1975; Gilbert, 1984), woodland tabanid and pantophthalmid flies (0·9–2·8g) warm endothermically before flight (May, 1976; Bartholomew & Lighton, 1986), and the horse bot-fly (Gasterophilus; 0·03–0·24g) elevates T_th by as much as 12°C in preparation for flight, and it maintains T_th at variable high levels during tethered flight (Humphreys & Reynolds, 1980).

With the exception of Crysotoxum sp., the lekking behaviour observed in Syrphus spp. (Heinrich & Pantle, 1975; Gilbert, 1984) is absent in the flies we studied. High T_th is therefore not a special adaptation of lekking syrphids.

High T_th, is essential for normal activity in the syrphids we studied. It seems that, rather than being a special adaptation for mimicry, the primary importance of high T_th is to permit normal foraging and/or mate searching at low T_a. Nonmimetic syrphids that we studied (Se. lata and Eristalis sp.) maintain T_th at equally high levels during activity. A variety of other non-mimetic Diptera maintain T_th at similar levels during activity, including tachinids (Chappell & Morgan, 1987) and calliphorids and bombyliids (B. Heinrich & K. R. Morgan, unpublished data).

However, high T_th may have been an important preadaptation for the evolution of mimicry in syrphid flies. In addition to physical characteristics of syrphids which are overtly mimetic, much of their inflight behaviour, including the flight tone (Brower & Brower, 1965), closely resembles that of the model. In fact, the mimicry of many of the flies we studied appeared to be most accurate during flight. If high T_th increases flight speed and manoeuvrability in flying insects (see, for example, Heinrich, 1979, 1983 ; Morgan et al. 1985) it may also be important in allowing syrphids to copy the flight behaviour of their highly endothermic models.

Thermoregulation during activity in the syrphids we studied was less effective than in their hymenopteran models, as indicated by comparisons of temperature excess and the degree of independence of T_th and T_a (i.e. the slopes of regression lines relating T_th to T_a). The temperature excesses of bumblebee mimics averaged 3·3–8·l°C below those of Bombus, while those of wasp mimics averaged 2·7–5·6°C below those of Vespula and Dolichovespula, their models. Only in T. alternans and Chrysotoxum sp. did the regressions of T_th on T_a have slopes significantly different from 1 (0·58 and 0·31, respectively), indicating some regulation of T_th. This partial regulation of T_th is similar to the levels of thermoregulation seen in Syrphus sp. (Heinrich & Pantle, 1975) and Syrphus ribesii (Gilbert, 1984). In contrast, Bombus queens and workers achieve almost perfect regulation of T_th (slopes not significantly different from 0) at T_a between 2·5 and 25°C (Heinrich & Heinrich, 1983). Likewise, Vespula and Dolichovespula achieve excellent regulation of T_th at T_a between 5 and 21°C and between 2 and 23°C, respectively (Heinrich, 1983).

There was no apparent relationship between body mass and temperature excess in the syrphid flies we studied (P = 0·59). Likewise, body mass and temperature excess were not significantly related in the bumblebees, yellow-jacket wasps or white-faced hornets (P = 0·22, P = 0·49 and P = 0·25, respectively). The mean body masses of Bombus-mimicking species ranged from 0·115 to 0·207 g, whereas the mean mass of the bumblebees we studied was 0·293 g. Mean body masses of Vespula and Dolichovespula mimics ranged from 0·067 to 0·34g, whereas mean masses of the wasps and hornets were 0·154 and 0·291 g, respectively. Differences in thermoregulatory ability between the flies and their models may result in part from increased rates of heat loss due to the smaller body sizes of the flies although, where the body masses of mimics and models overlapped, the differences in temperature excess were still apparent.

In general, small heterotherms warm up more rapidly than large ones, but previous data relating the rate of endothermic warm-up to body mass in insects have shown either no relationship (Heinrich & Bartholomew, 1971; Heinrich & Casey, 1973; Bartholomew & Epting, 1975) or a weak positive correlation (May, 1976). Our data for maximum rate of warm-up in syrphid flies show a strong positive correlation with body mass (Fig. 4); in contrast to vertebrate heterotherms, small syrphids warm up more slowly than large syrphids.

The capacity for sustained endothermy has been demonstrated in a variety of bees and beetles but only once previously (to a very limited extent) in a fly. In the laboratory, the giant tropical fly (Pantophthalmus tabaninus) alternates between rest and sustained endothermy where T_th remains 1–2°C above T_a, sometimes for more than 30min (Bartholomew & Lighton, 1986). The capacity for sustained endothermy is much more highly developed in syrphids. Three of the syrphid species we studied showed pronounced tendencies to maintain T_th at high and fairly constant levels (Fig. 5). It seems likely to us that further testing would demonstrate that the response is common in larger syrphids because we at no time observed torpid flies during our extensive observations of foraging flies in the field. The syrphids did not show a clear pattern of periodic cycling of T_th during sustained endothermy in the laboratory, such as that seen in beetles (Morgan & Bartholomew, 1982; Morgan, 1987). However, frequent attempts at flight by the flies may have obscured the cycles.

Sustained endothermy may allow the flies to maintain a state of flight readiness during foraging that would not be possible if T_lh were allowed to fall to T_a. A continuously high T_th may also enhance predator avoidance and may enable the flies to assimilate nutrients more rapidly during foraging and/or enhance growth rates of reproductive cells. The high energetic cost of sustained endothermy may be relatively unimportant even in small flies if there is always a ready source of nectar to fuel their endothermy. Unlike social bees, the flies need not expend energy supplies for nest thermoregulation, and they do not store energy supplies for their relatives and/or offspring.

Although the thick pile of Bombus mimics is clearly effective as insulation, the cooling rates and body temperature excesses of these mimics are similar to those of glabrous syrphids. This suggests that the pubescence characteristic of Bombus mimics did not evolve solely as insulation. Unlike bumblebees and honeybees, which obtain much of their pollen during foraging by combing it from their hairs, syrphids are primarily direct feeders (Gilbert, 1981). If this is true for the Bombus mimics we studied, it is unlikely that their pubescence evolved in response to pollen-gathering behaviour, as suggested for Eristalis tenax by Holloway (1976). It seems most likely that the primary importance of pubescence in Bombus mimics is in improving visual mimicry, and that its importance in insulating the thorax is secondary.

We are indebted to C. H. Morgan for much technical assistance, G. S. Waldbauer for identifying the flies, and J. R. B. Lighton for the use of programs for the BBC microcomputer. We also thank M. A. Chappell and an anonymous reviewer for critically reading the manuscript. This study was funded in part by an intramural grant from the University of Vermont.