Temperature Regulation, Energy Metabolism and Mate-Searching in Rain Beetles (Pleocoma Spp.), Winter-Active, Endothermic Scarabs (Coleoptera)

Endogenously elevated body temperatures in beetles were first reported more than 40 years ago in Geotrupes stercorarius that were preparing for flight (Krogh & Zeuthen, 1941). The requirement for a high body temperature for flight in many large insects has since been well documented (see Kammer, 1981, for a review). Many neotropical beetles elevate body temperature during terrestrial locomotion (Bartholomew & Casey, 1977a,b). African dung beetles maintain high body temperatures while making and rolling dung balls (Bartholomew & Heinrich, 1978; Heinrich & Bartholomew, 1979). Elephant beetles (Megasoma elephas) respond to reduced ambient temperature by maintaining body temperature at high levels (Morgan & Bartholomew, 1982). Green fig beetles (Cotinis mutabilis) elevate body temperature above ambient temperature while foraging in fruiting trees (Chappell, 1984). In contrast, flower scarabs (Pachynotus sinuata) warm up only prior to flight and maintain body temperature near ambient temperature while foraging even though they have a well developed capacity for endothermic heat production (Heinrich & McClain, 1986).

The genus Pleocoma (family Scarabaeidae) includes approximately 33 species distributed through the coastal ranges and Sierra Nevada of western North America (Linsley, 1938; Hovore, 1977). The larvae feed on plant roots and are sometimes orchard pests. Adult males weigh 0·6-1·7 g, whereas the flightless females weigh 4·0–8·0g. Male rain beetles undertake aerial and terrestrial searches for females at night during the autumn and winter. They are apparently attracted to the female’s burrow by a pheromone (Rivers, 1890; Davis, 1935; Ellertson & Ritcher, 1959). When the males are searching, ambient temperatures range from –1 to 15 °C. There is one report of males flying during a snowstorm (Van Dyke, 1933). Adult rain beetles do not eat and therefore the intense activity of the males depends on energy stored by the larvae prior to metamorphosis. Previous studies indicated that heavybodied insects like these beetles require a high thoracic temperature for flight. However, the earlier studies concerned tropical and temperate species active at relatively warm ambient temperatures. I have examined thermal adaptations and energetics pertinent to activity in the cold.

I studied rain beetles of the following taxa from October to February (1979-1985) during winter rains in the coastal mountains of California: Pleocoma australis Fall, P. puncticollis Rivers, P. badia badia Fall, P. badia hirsuta Davis, P. conjungens Horn and P. linsleyi Hovore. They all have localized distributions at altitudes ranging from 100 to 2400 m in chaparral or montane forest. Although I gathered field data (body temperatures and behaviour) for all of them, I concentrated my field efforts on P. australis, which is abundant in the San Jacinto Mountains. This species is sometimes active during the late afternoon on rainy days making it possible to observe flight behaviour and terrestrial activity. Laboratory measurements (warming and cooling rates, walking speed and metabolic rates) were made only on P. australis. Beetles used in laboratory experiments were stored in airtight vials at 5°C. Laboratory measurements were completed within 2 weeks of capture.

Male Pleocoma were captured with an insect net. Battery powered ultraviolet lights were used to attract flying beetles after dark. Thoracic and abdominal temperatures (T_th and T_ab) were measured with copper-constantan thermocouples (0·03 mm in diameter) threaded through 30-gauge hypodermic needles with the thermocouple junctions glued in place. Beetles were grasped by the legs to minimize hand contact and measurements were completed within 3–6 s. Ambient temperature (T_a) was measured at the site of capture immediately after T_th and T_ab had been measured. Temperatures were read to the nearest 0·1 °C on a Bailey Bat-12 thermocouple thermometer which had been calibrated against a mercury thermometer traceable to the US Bureau of Standards.

Thermocouples (0·03 mm in diameter) were implanted in the thorax of freshly captured male P. australis. Similarly sized individuals were chosen to avoid size effects. The leads were fixed in position with beeswax and the beetles were placed in an open container at 6–9°C. Endothermic warm-up was induced by rapping the chamber on the bench top and T_th and T_a were recorded by a microcomputer at 0’5-min intervals. Ventilation rate during warm-up was determined visually by counting abdominal contractions.

Cooling rates were determined using freshly killed male P. australis with thoracic thermocouples as described above. Similarly sized individuals were chosen to eliminate size effects. The insects were heated to 42°C using an incandescent lamp and were then allowed to cool while T_th and T_a were recorded at 2-s intervals by a microcomputer. In the first set of experiments, beetles were positioned in walking posture and cooling rate was measured first on the intact animal and then after removal of the wings and elytra. The insects were then positioned in typical flight posture in a laminar-flow wind tunnel and cooling rate was measured at a wind speed of 3·8 ms⁻¹. A second group of beetles was mounted in flight posture and cooling rate was measured at a wind speed of 4·3 m s⁻¹, first with the pile intact and then with the pile removed from the thorax. Thermal conductance (W°C⁻¹) was calculated from cooling rates by assuming a specific heat of 3·4Jg^−loC⁻¹ (May, 1979). Air speeds in the wind tunnel (measured with a hot wire anemometer) were selected to be similar to flight speeds timed in the field.

Walking speed at a T_a of 4°C was measured by timing P. australis males on a 1-m linear track 5 cm wide. Body temperature increased during the trials by no more than 3°C. Accordingly, T_th was measured before and after each trial and averaged to provide an estimate of mean T_th during the trial. The beetles walked spontaneously at all temperatures.

Oxygen consumption of inactive P. australis was measured by placing individuals into airtight 50ml syringes for 30-300 min. Measurements were made between 09.00 and 18.00h in a dark, controlled-temperature room maintained at 5, 15 or 25 °C. The syringes containing beetles were allowed to equilibrate at a given temperature for 2h and were continuously flushed with fresh air (20 ml min⁻¹) until measurements began. At the beginning of a measurement the respirometer was sealed and an initial sample of air was collected. At the end of the measurement period, a 30-ml air sample was transferred through three-way valves from the syringe respirometer to a third syringe. The fractional concentration of oxygen was measured using an infusion pump to push sample gas through a scrubbing train of Ascarite and Drierite and then through the sensor of an Applied Electrochemistry S3A oxygen analyser. Gas volumes were corrected to STPD after accounting for the volume of the beetle.

The during warm-up and sustained endothermy was measured in an opencircuit respirometry system using the instantaneous method of Bartholomew, Vleck & Vleck (1981). The effective volume of the system was 83 ml. T_a averaged 9°C and was controlled to within 1°C with a temperature cabinet. A beetle (P. australis) was placed in a Lucite respirometer chamber through which air was pumped at a rate of 60 ml min⁻¹. A second pump pulled a subsample (30 ml min⁻¹) of the gas leaving the respirometer through a scrubbing train of Ascarite and Drierite and then through the oxygen sensor. T_th, T_ab, T_a and were recorded simultaneously by a microcomputer at 30-to 60-s intervals.

The mating activity of male and female rain beetles was closely synchronized by autumn and winter rains. Male P. australis emerged from underground and were most abundant during light drizzle at dusk and just after dark. In other Pleocoma species, peak male activity occurred during similar weather just before dawn. Males searched for females by flying upwind in a meandering path within 1-2 m of the ground. Flight speeds ranged from hovering to as high as 4·5ms⁻¹. Flying males were wary and often avoided capture by climbing to heights of 5 m or more. Aerial searching ended when the males landed downwind of the female (usually in a burrow and partially covered by soil). Ground searchers appeared agitated and crawled rapidly. Unlike flying beetles they did not seem to orientate to the burrow but instead appeared to search randomly. If they failed to find the burrow they usually took wing and resumed aerial searching. Upon reaching the burrow entrance they began to dig down to the female who was usually several centimetres or more beneath the surface. Often several males were present near an occupied burrow and although they did not fight they clearly interfered with each other in their efforts to reach the female.

The T_tb of male Pleocoma during flight ranged from 33·7 to 40·6°C at T_a ranging from 2·4 to 15·0°C (Fig. 1A). On one occasion I observed P. linsleyi males in flight at T_a< – 1°C but was unable to measure T_tb. The slope of the regression of T_tb of flying Pleocoma on T_a was not significantly different from zero (t-test, P – 0·659), suggesting that Pleocoma regulates T_th during flight. The mean flight temperature was 37·6°C (s.D. = 1·56, N= 83). A minimum flight T_th of 34–35°C was estimated from the lowest flight temperatures measured in beetles in the field. One 1·0 g male had a temperature excess (T_th–T_a) of 35·2°C. The T_ab in flight ranged fro m 11·9 to 28·4°C (mean = 16-8, S.D. =4·01, A⁷ =58; Fig. 2). The slope of the regression of T_ab on T_a was not significantly different from 1 (T_ab = 9· 156+0·777T_a; r² = 0·292, N = 54, p= 0·191).

The T_th of male Pleocoma searching on the ground surface for females ranged from 20·7 to 38·1°C (mean = 31·5, S.D. = 4·50, N = 34) at T_a ranging from 3·1 to 15·0°C (Fig. IB). The slope of the regression of T_th of searching males on T_a was not different from zero (t-test, P– 0·395), suggesting that T_th is also regulated during ground searching. The T_ab ranged from 13·3 to 21·5°C (mean = 16·7, S.D. = 2·01, N – 24) and was unrelated to T_a.

Male P. australis were occasionally found in their burrows just prior to the onset of flights. The T_th of six individuals was from 0·9 to 4·3°C higher than ground temperature (which varied from 9·9 to 12·6°C).

The T_th of female Pleocoma (three P. australis and oneP. linsleyi) captured on or below the ground surface while males were flying ranged from 4·3 to 10·9°C and was not different from the temperature of their immediate surroundings. Dissections of P. australis showed that the flight muscles, which are the site of endothermic heat production in males, are absent in females. In females the thorax and abdomen are filled with what appears to be fat.

Male rain beetles were able to initiate endothermic warm-up from a T_th at least as low as 4·0°C. There was considerable variation in rates of warm-up. At T_a between 6 and 9°C, the increase in T_th was relatively linear and averaged 1·4°C min⁻¹(N = 20, range = 0·7–2·1 ). There was no apparent relationship between body mass and warmup rate, but the range of body masses was limited (0·90–1·45 g).

Cooling data (T_th–T_a) linearized by semilogarithmic plotting were accurately described by least squares linear regressions (all r² were greater than 0·997). Representative cooling data for a 1·2-g male are shown in Fig. 3. In the absence of forced convection, the conductance of three male Pleocoma (mean mass l·17g, S.D. = 0·042) averaged 0·0231 W°C⁻¹ (s.D. = 0·0026). During terrestrial activity, the air spaces under the wings and elytra insulate the thorax and abdomen. After removal of the wings and elytra, conductance increased by about 15% to 0·0271 W°C⁻¹ (S.D. =0·0020). At a wind speed of 3-8ms⁻¹ (equivalent to flight speed) conductance averaged 0·0411W°C⁻¹ (s.D. = 0·0119), a 44% increase over conductance of the intact beetle in still air. Although Pleocoma have thoracic pile, cooling rates of males with the pile removed were not significantly different from those of intact beetles.

Walking beetles responded to handling by warming endothermically from T_tb – T_a = 4°C to T_th as high as 34°C. Two or three speed measurements were made on each individual as T_th gradually increased. This method could potentially introduce a training effect in the successive trials. However, the insects walked with very little prompting in all of the trials, suggesting that training effects were unimportant. Walking speed increased exponentially with T_th from a low of 0·22cms’¹ at 7°C to a high of 5·35cms”¹ at 33°C (Fig. 4). The mean Q₁₀ between 6 and 34°C was 2·5. Male rain beetles walked in a coordinated fashion at T_th as low as 2°C, but by maintaining T_th at 34°C they were able to walk more than 12 times faster than at a T_th of 6°C.

The of resting beetles increased exponentially with body temperature (Fig. 5). The mean Q₁₀ between 5 and 15°C, and between 15 and 25°C was 2-6. Mean body masses of beetles used in these measurements were as follows: 5°C, l·06g, S.D. = 0·218, ;V = 44; 15°C, l·00g, s.D. =0·220, N = 20; 25°C, 0·94g, S.D. =0·113, N = 21.

T_th and usually rose steadily during endothermic warm-up preceding sustained endothermy (Fig. 6). Performance during sustained endothermy varied in duration and in the level at which T_th was maintained. Bouts of sustained endothermy lasted for 0·15-4·17 h. The mean T_th during these bouts ranged from 10·1 to 30·3°C at a T_a of 9·0°C. T_th and during sustained endothermy oscillated with a given cycle in peaking before the corresponding cycle in T_tb (Fig. 6). The magnitude of oscillations in T_th usually ranged from 1 to 3°C. Maximum excursions in T_th during sustained endothermy in 11 beetles were from 1·3 to 6·3°C. Oscillations in T_ab corresponding to those in T_th were sometimes detected but their amplitudes were small. During a warming cycle in one beetle, T_th changed by 6·2°C but T_ab changed by only 0·8°C. Oscillations in were considerably larger than those in T_th. The was often near zero but occasionally rose to as high as T3mlmin⁻¹. The mean during sustained endothermy increased in a linear fashion with the temperature difference between the thorax and ambient air (Fig. 7). The frequency of warming cycles during sustained endothermy also increased with the temperature difference between the thorax and ambient air (Fig. 8).

Ventilatory movements (abdominal contractions) were not observed in resting Pleocoma. The onset of endothermic warm-up was accompanied by periodic abdominal contractions which continued throughout warm-up and sustained endothermy. Ventilation rate increased exponentially (Q₁₀ = 2·2) with the T_th–T_a difference from a low of 20 min⁻¹ at a T_th–T_a of 2·2°C to a high of 112 min⁻¹ at a T_tb–T_a of 22·7 °C (Fig. 9). In one individual, abdominal contractions were noticeably deeper and slower than was typical, although the rate of warm-up was normal.

Despite low environmental temperatures, flying male Pleocoma maintain a T_th similar to that of other endothermic insects of comparable size (e.g. sphinx moths, bees and other scarabs). The temperature excess (as high as 35·2°C) maintained by male Pleocoma during flight is among the greatest yet reported for an insect, even though the thoracic pile is apparently ineffective as insulation. Moths and bees are covered with dense pile which may reduce their thermal conductance by as much as 50 % (Church, 1960a,b). The cooling rate of male Pleocoma in still air averages 44 % more than that of well-insulated sphinx moths of the same body size [0·347 versus 0·195°Cmin⁻¹°C⁻¹ (data for moths taken from Bartholomew & Epting, 1975)].

Among insects, sustained endothermy at low T_a is known in worker honey-bees (Heusner & Roth, 1963; Heusner & Stussi, 1964; Southwick & Mugaas, 1971; Cayhill & Lustic, 1976), incubating queen bumble-bees (Heinrich, 1974a) and in the scarab beetle Megasoma elephas (Morgan & Bartholomew, 1982). Whereas Pleocoma usually walks steadily during warm-up and sustained endothermy, Megasoma is stationary. Otherwise, the patterns of body temperature regulation in Pleocoma and Megasoma are qualitatively similar. However, Pleocoma and Megasoma differ markedly in the temperature-dependence of their ability to initiate endothermic warm-up. Megasoma was incapable of initiating the endothermic response if T_th fell below about 18°C. In contrast, Pleocoma was able to initiate warm-up at a T_th below 4°C. In tropical flower scarabs (Pachynotus sinuata), the temperature threshold for endothermic warm-up is about 20°C (Heinrich & McClain, 1986).

The main functions of thermoregulation during flight are to ensure that the flight muscles produce adequate power, while preventing overheating of the thorax (Heinrich, 1974b). Pleocoma clearly regulates T_tb during flight, but the mechanism of regulation is unclear. If, like other insects, Pleocoma has a constant flight at all T_a values, thermoregulation must be accomplished behaviourally (by varying flight duration) or physiologically (by evaporating water or adjusting thermal conductance). At present, only honey-bees are known to use evaporative cooling which they accomplish by regurgitating a droplet of honeycrop fluid onto their tongue (Heinrich, 1979). This mechanism is not possible in Pleocoma because the adults have no mouth. A variety of insects control T_th by pumping warm haemolymph from the thorax to the abdomen which acts as a heat exchanger (e.g. see Heinrich, 1970, 1971, 1976; Heinrich & Casey, 1978; Chappell, 1982; Willmer, 1982; Morgan, Shelly & Kimsey, 1985). However, there is no evidence that Pleocoma or any other beetle controls T_th in this manner (e.g. see Bartholomew & Heinrich, 1978; Chappell, 1984; Heinrich & McClain, 1986). Although T_ab was greater than T_a in flying Pleocoma (Fig. 2), there is no indication that this situation arises other than from passive heat transfer from the thorax to the abdomen. Although much heat is produced by the flight muscles of Pleocoma during flight, the T_a is always below 15 °C so that heat loss is rapid. Regulation of T_th in flying rain beetles may depend on intermittent flight. However, I have no field observations which support or refute this idea. It is noteworthy in this regard that flower scarabs (Pachynotus sinuata) also show no evidence of active heat transfer to the abdomen and suspend flight when T_th exceeds 41 °C (Heinrich & McClain, 1986).

Variation in heat production is the primary mechanism for control of T_th during sustained terrestrial endothermy in Pleocoma. Males maintained T_tb at a fairly constant high level by initiating heat production whenever T_th fell below an apparent lower temperature set point (Fig. 6). They responded to the increased rate of heat loss at greater T_tb –T_a differences by increasing the frequency of heating cycles (Fig. 8).

Male rain beetles showed distinct ectothermic and endothermic patterns of in the laboratory. When allowed to rest quietly the beetles had a low that increased in a regular fashion with temperature between 5 and 25°C (Fig. 5). The of inactive males at 25 °C is similar to that of the green fig beetle (Cotinis mutabilis), another temperate scarab of about the same size (Chappell, 1984). In contrast, above 25°C, or when disturbed at low T_a, beetles began walking, increased to as high as 1·3 ml min⁻¹ and often maintained body temperature considerably above T_a by periodic heat production. The maximum during these intervals of heat production was as much as 13 times the minimum (Fig. 6).

The energy cost of walking in beetles is small relative to the cost of maintaining a temperature excess during sustained endothermy (Bartholomew & Casey, 1977b). Therefore, despite the differences in behaviour between endothermic Pleocoma and Megasoma (rain beetles walked while elephant beetles remained stationary), the energy costs of sustained endothermy can be compared to examine the influence of body size. On a per gram basis, of Pleocoma and Megasoma increases in a linear fashion with the T_th–T_a difference (Fig. 10A). However, the slope of the regression of on the T_th–T_a difference is 1·91 inPleocoma and only 0·30 m Megasoma. At a T_th–T_a difference of 20 °C Pleocoma uses almost six times more energy on a per gram basis (35·36 versus 6·25 ml O₂g⁻¹ h⁻¹). In contrast, Pleocoma uses only one quarter as much on a whole animal basis to maintain the same T_th–T_a difference (39·42 versus 139·38 ml O₂g⁻¹ h⁻¹ ; Fig. 10B). These relationships suggest, paradoxically, that for an endothermic insect in a cold environment where energy stores are slow to accumulate or cannot be replenished there is, within limits, an energetic advantage to being smaller. Despite its more rapid heat loss, an insect the size of male Pleocoma can remain endothermic on a given amount of energy for a longer time than can a larger insect. That energy stores accumulate slowly in Pleocoma is apparent from the extended duration of the larval period. Pleocoma larvae that have been studied moult once per year and pupation is preceded by 9–13 larval instars (Ellertson, 1958). To my knowledge, no other scarab is known to have more than three larval instars.

Although I was unable to measure the energy cost of flight in Pleocoma, it may be calculated from thermal conductance measured at a wind speed equivalent to flight speed. A 1·2-g P. australis flying with T_th–T_a = 30·5°C (the average for this species) has an estimated metabolic rate of 1·5W. The metabolic rate of a 1·2-g sphinx moth in flight is 0·5 W (Bartholomew & Casey, 1978). Assuming that one-tenth to one-quarter of the body mass of Pleocoma is stored fat used for flight, the maximum estimated flight duration should range from 0·9 to 2·2 h ( 1 g fat = 39·7 kJ).

The larval life history adaptations of rain beetles allow for gradual accumulation of energy from relatively non-nutritious food until adequate stores are available for pupation and mating activity. The large size of female Pleocoma has presumably evolved because females are free from constraints on weight placed by flight, and because by being larger they can produce more eggs. The adult life history of male Pleocoma allows for energy conservation until conditions are appropriate for mating, and then energy stores are expended in an all-or-nothing effort when conditions are optimum for mating success.

In view of the high energy cost of activity and the fact that adult Pleocoma do not eat, it is hardly surprising that a male is active for only a few days and that the activity of males and females is closely synchronized. Females must have some indication when to burrow to the surface and disperse pheromone if the males are to find them. In western North America, seasonal rainfall (which occurs during the late autumn and winter) may be the only available environmental stimulus that is precise enough to synchronize mating activity. However, it is unclear whether Pleocoma responds directly to the rain or to some associated stimulus (e.g. falling barometric pressure).

Although endothermy in Pleocoma is energetically costly, it releases the beetles from physiological constraints on activity that would otherwise be imposed by low T_a. As in many other large insects a high T_th is required for flight in Pleocoma. Flight is clearly important during the initial phase of mate-searching when males must search a large area to locate a female. The presence of many males at a single female’s burrow suggests that intermale competition is keen during the terrestrial phase of the search. As many as nine males have been excavated from the burrow of a single female, many having been damaged by the persistent digging efforts of males arriving later (Davis, 1935; Ellertson, 1956). Sustained endothermy increases the speed of terrestrial locomotion in male Pleocoma. Presumably it enhances the efficiency of terrestrial searching for the female and ultimately enhances mating success.

Male rain beetles are highly vulnerable to vertebrate predators during aboveground activity (reviewed in Ellertson, 1958). The problem is acute in daylight when even flying beetles are easily caught by birds. It seems likely that natural selection has favoured crepuscular and nocturnal activity to avoid visual predators. Even at night, active males are noisy and are vulnerable to foxes, coyotes and owls. The ability to locate a female quickly and thus reduce the amount of time spent on the ground surface, and to initiate flight on demand to avoid terrestrial predators, may be important additional advantages of endothermy.

I am indebted to George Bartholomew for help in numerous aspects of this study. Frank Hovore provided much important assistance throughout. I thank David Bradford, George Bryce, Mark Chappell, Art Evans, Beth Flint, Bruce Gill, David Goldstein, Cathy Morgan, Diane Petrula and Todd Shelly for help while collecting beetles. I also wish to acknowledge Albert Bennett, Mark Chappell, Michael Greenfield, Henry Hespenheide and two anonymous reviewers for critically reading the manuscript. I thank John Lighton for the use of programs for the BBC microcomputer. Support was provided by a Dissertation Improvement Grant from the National Science Foundation (DEB-8023917), from Patent Fund Grants administered by UCLA, and by an NSF grant to George Bartholomew (DEB-8103513).