- Email: [email protected]
Temperature regulation in the nocturnal melolonthine Sparrmannia flava
J. therm. Biol. Vol. 18, No. l, pp. 25-33, 1993
0306-4565]93 $6.00 + 0.00
Printed in Great Britain. All rights reserved
Copyright ~) 1993 Pergamon Press Lid
TEMPERATURE REGULATION IN THE NOCTURNAL MELOLONTHINE SPARRMANNIA FLAVA S. L. CHOWN and C. H. SCHOLTZ Department of Entomology, University of Pretoria, Pretoria 0002, South Africa (Received 18 September 1992; accepted in revised form 7 October 1992)
AbsU'act--1. Sparrmanniaflava Arrow (Coleoptera: Scarabaeidae) regulated thoracic temperature (Tth) during flight at 38.6°C over an ambient temperature (T~) range of 11°C. 2. Tth and wing loading (19.99 Nm -2) were within the range predicted by body mass (0.80 g) based on previous studies of scaling in beetles, although conductance (0.0087 W °C-~) was considerably lower and wingstroke frequency (87 Hz) higher than that previously recorded in beetles of similar mass. 3. The slope of the regression of abdominal temperature (Tab) on Ta, at Tas > 20°C, was > 1, and physiological heat transfer was demonstrated experimentally, suggesting that low conductance necessitates active heat transfer at high Tas. 4. Sparrmannia flava's early-morning, anti-predator strategy involves adaptations which make it an exception to previous generalizations concerning the thermal biology of beetles. Key Word Index: Thermoregulation; wingstroke frequency; morphology; Coleoptera; Sparrmanniaflava
(1981) and others (e.g. Kammer, 1981) to conclude that the ability of endothermic insects to maintain and regulate elevated thoracic temperatures in flight is strongly size-dependent. After examining the relationships between body mass, temperature sensitivity of wing beat frequency and thermal biology of 24 Holarctic beetle species (all weighing < 1 g), Oertli (1989) concluded, however, that body mass per se was less important than wing stroke frequency, in accounting for thermoregulatory precision and thermal sensitivity of wing stroke frequency. Nonetheless, Oertli (1989) found that larger beetles were generally thermoconformers whereas smaller beetles had greater thermoregulatory precision. Although not explicitly addressed in the literature, this discrepancy between Bartholomew and Heinrich's (1978) and Oertli's (1989) findings concerning the relationship between size and thermal biology is apparent in other studies of beetles. Chappell (1984) found that Cotinus texana (ca 1.29 g) maintained its body temperature up to 12°C above ambient while foraging and regulated thoracic temperature during flight, and Morgan (1987) documented a highly developed capacity for thermoregulation during flight and terrestrial activity in rain beetles (Pleocoma spp 0.6-1.7 g). In contrast, Heinrich and McClain (1986) found that despite a well developed capacity for endothermy, Pachnoda sinuata (ca 0.94 g) did not regulate thoracic temperature during flight and maintained body temperature close to ambient while foraging. The same sort of strategy also seems to be
INTRODUCTION
The thermal biology of bradymetabolic animals has been the subject of extensive research over the past two decades (see review in Cossins and Bowler, 1987). Flying insects, in particular, have enjoyed considerable attention, and relationships between the abiotic environment (particularly ambient temperature), body temperatures, morphology, metabolic rate, and wing morphology and stroke frequency, have been thoroughly investigated (see e.g. Casey, 1988, 1989; Heinrich, 1981a; May, 1979, 1981). Most of this work has been conducted on bees (e.g. Casey et al., 1985; Joos et al., 1991; Stone and Willmer, 1989a), flies (e.g. Morgan and Shelley, 1988; Unwin and Corbert, 1984; Willmer, 1982) and moths (e.g. Bartholomew and Casey, 1978; Bartholomew and Epting, 1975; Casey and Joos, 1983; DeVries and Dudley, 1990), while the Coleoptera have enjoyed less attention. Krogh and Zeuthen (1941) first noted endothermy in beetles, and comparative work was initiated by Bartholomew and Casey (1977a, b), Bartholomew and Heinrich (1978) and Heinrich and Bartholomew (1979). As a result of their studies, Bartholomew and Heinrich (1978) suggested that in beetles lighter than 2 g, body temperature is a passive function of the balance between rates of heat production and heat loss, but that in heavier beetles regulatory mechanisms are involved. This finding was in accord with studies of other insects (e.g. Bartholomew and Heinrich, 1973; May, 1976) and led Bartholomew 25
26
S.L. CHOWNand C. H. SCHOLTZ
followed by Trichostetha fascicularis (see Nicolson and Louw, 1980, p. 125 and Fig. 2), although the authors did not address this point. Heinrich (1981b) pointed out that body temperature in insects is determined not only by constraints of size, but also by constraints of insulation, metabolic rate and wing loading, while subsequent studies of moths (Casey and Joos, 1983) and bees (Dyer and Seeley, 1987; Joos et al., 1991; Stone and Willmer, 1989a; Underwood, 1991) have highlighted the influences on body temperature of aerodynamic configuration, phylogeny and the adaptations of a given species to a particular thermal environment. If in moths and bees such a myriad of factors influence the thermal biology of a species, it is likely that this will be the case in the Coleoptera. The difference between Bartholomew and Heinrich's (1978) and Oertli's (1989) findings is a pertinent example, making evident the need for further data on the thermal biology of flying beetles. In this paper, we examine the thermal biology of a nocturnal, melolonthine scarab, Sparrmanniaflava Arrow (Coleoptera: Scarabaeidae) to provide such information. MATERIALS AND METHODS
Study site This study was done during three 10 day visits, in October 1990, October 1991 and January 1992, to Twee Rivieren camp (26°28'S, 30°37'E) in the Kalahari Gemsbok National Park in the northwestern Cape Province of South Africa. Sparrmannia tiara is extremely abundant in the Kalahari Desert and is unique amongst melolonthines because the larvae feed on the dung of medium-sized antelope (Seholtz, 1988). Adults are large, active melolonthines which spend the day below the soil surface, emerging in the evening or early morning to feed on angiosperm foliage.
Body temperature, morphology, wing morphology and wingstroke frequency All beetles were collected at a black light (Bioquip California) which was run from sunset to sunrise. Thoracic (Tth) and abdominal (Tab) temperatures of beetles, knocked to the ground while flying to the light, were measured to the nearest 0.1°C using 40-gauge copper-constantan thermocouples, glued into hypodermic needles, and a Kane--May 457 XP digital thermometer. All measurements were completed within 5-8 s. Ambient temperature (T,) and humidity were monitored continuously using a Novasina thermo-hygrometer and the former checked against T, measured by the dried thermoeouple. The beetles were subsequently weighed to the nearest mg
with a Sauter electronic balance, and abdominal and thoracic masses were also determined. Wing areas were determined by converting the mass of a photocopy of the fight wing to area using a mass-area regression of the paper (Bartholomew and Heinrich, 1978). Wing length was measured from the basal sclerites to the tip of the leading edge using Vernier calipers. Wing loading was determined by dividing the area of the wings by the beetle's wet mass. Aspect ratio was calculated using the formula provided by EUington (1984). A total of 100 beetles was examined. Wingstroke frequency of eight beetles was recorded using an Audio Technica AT9300 directional microphone and Sony TCM-6 portable casette recorder. Wingstroke frequency was obtained from the recordings using a Kikusui 5020A storage oscilloscope.
Conductance and endothermic warm-up Cooling rates were determined using thermocouples (as above) fixed into the thorax of 26 freshlykilled beetles. Of these, ten were unaltered beetles, eight specimens had the thoracic and abdominal pile removed, using a fine scalpel blade and microscissors, and the elytra and wings were removed from eight individuals to simulate the flying posture. The beetles were heated by an incandescent lamp to 40°C and then allowed to cool, in a 40 x 40 x 30 cm insulated plastic container, while Tth and Ta were recorded every 15 s. The experiment was terminated when beetles were within 2°C of the ambient temperature. Thermal conductance was calculated from cooling rates using the methods outlined by Casey and Joos (1983) and Morgan (1987). To determine rates of endothermic warm-up, beetles were kept in sand overnight. On the following evening, thermocouples were implanted in the thorax of these specimens. This usually stimulated warm-up and Tth was recorded at 5 s intervals in eight specimens.
Physiological heat transfer The possibility of heat transfer from thorax to abdomen was investigated using a modification of Chappell's (1982) method. Live specimens were crosspinned to a Styrofoam block with thermocouples inserted into the thorax and abdomen. The thorax was heated by incandescent lamp while the abdomen was shielded using layers of cardboard and reflective foil, and simultaneous measurements of Tth and Tab were taken to a Tth of ca 40°C. The animal was then killed by injection of a drop of ethyl acetate, allowed to cool, and the procedure repeated.
Microclimate and activity Microclimate experienced by beetles was measured in terms of operative temperature (Te) by mounting
Temperature regulation in S. tiara thermocouple-equipped dried beetles in a flying and foraging posture (see Morgan and Shelly, 1988). To, T, and windspeed (using a conventional cup anemometer) were monitored from sunset to sunrise. The number of beetles arriving at the light was monitored on an hourly basis each night, together with Ta, windspeed and relative humidity (see above).
27 RESULTS
Body temperature, morphology, wing morphology and wingstroke frequency The Tth of S. tiara ranged from 34.5 to 42.4°C (mean = 38.6°C, SD = 1.47, n = 100) at T= ranging from 13.1 to 24.3°C [Fig. I(A), Table l], and the slope of the regression of T,h on T= (Tth = 0.015 Ta + 38.27)
A
4 I ............................................ 0 42 ° ~11
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.................... .
.
.
.
.
.
.
mm
4oh,.
...........................................
,=,
~.~F'"
...... ; ......................................
~_ ~4 L .....
......................
....
'"
..
.........
I
.... I
........ ~ ....
.............................
......
, ....
F 32
13
14
15
16 '
31
17
18
19
20
21
22
23
24
25
Ambient temperature °C
B
~,,~.~.~
13
14
.................. ... ........................
15
16
17
18
19
20
21
22
23
24
25
Ambient temperature °C Fig. 1. Relationship of thoracic (A) and abdominal (B) temperature to ambient air temperature. Equation for the line in (A): Y=0.015 X + 38.27, and in (B): Y=0.811 X+8.19.
28
S.L. CHOWNand C. H. SCHOLTZ
Table 1. Summary statistics for morphological parameters of S. tiara (n = 100) Mean Body mass (g) Thoracic mass (g) Abdominal mass (g) Wing length (ram) Wing area (cm2) Wing loading (Nm -2) Aspect ratio
0.796 0.362 0.376 26.00 3.91 19.99 6.958
SD
Min
0.158 0.486 0.048 0.236 0.129 0.170 1.06 22.7 0.38 2.77 3.611 11.46 0.478 5.577
Max 1.329 0.440 0.840 28.8 5.01 32.17 8.866
was not significantly different from zero (t = 0.448, P = 0.65). The greatest temperature excess recorded was 29.1°C and the lowest 10.9°C (mean = 20.1°C), and a m i n i m u m flight T~h of 34-35°C was estimated from the lowest fright temperatures measured. These are probably slight overestimates because beetles closed their elytra on capture, elevating Tth by 1-2°C. Abdominal temperatures ranged between 14.2 and 30.4°C ( m e a n = 2 3 . 1 4 , S D = 4 . 3 0 , n = 1 0 0 ) [Fig. I(B)] and the slope of the regression of T~b on Ta (Tab = 0.811 Ta + 8.19) was significantly < 1 ( t = - - 4 . 4 1 4 , P <0.001). However, above a T~ of 20°C, the slope of the regression of Tab on T~ (Tab = 1.571 Ta -- 8.78, r 2 = 0.458, n = 55, P < 0.001) was significantly > 1 (t = 2.408, P < 0.05). Summary statistics for size, thoracic mass, abdominal mass, Tth, wing length, area and loading and aspect ratio are provided in Table 1. Both thoracic and abdominal mass accounted for approx. 46% of body mass (30-58% in the former, 31-65% in the latter). Thoracic mass scaled with 0.53 of body
mass and abdominal mass scaled with 1.54 of body mass (Table 2). Thoracic and abdominal mass were not highly correlated indicating that individuals were carrying different loads. Thoracic mass accounted for more of the variance in both wing length and area than did body mass (Table 2), although the reverse was true of wing loading which scaled as body mass °Ts. Significant, but weak relationships between either body mass, thoracic mass or wing loading, and Tth were found. Temperature excess ( T t h - T~) was correlated with wing loading and body mass, but not with thoracic mass. Wingstroke frequency at a T~ of 14°C varied between 78 and 111 Hz (mean = 86.9, SD = 11.3, n = 8). Conductance and endothermic warm-up
Semilogarithmic plots of the cooling data (Tth--Ta) were accurately described by linear regressions (r 2 > 0.982 in all cases), and representative data for beetles with and without elytra and the dense pile are provided in Fig. 2. Conductance varied between 0.0077W °C -~ and 0.0093W °C -l ( m e a n = 0 . 0 0 8 7 W °C -t, n = 10) and there was a significant inverse relationship between mass and conductance (log c o n d u c t a n c e - - - 0 . 3 5 3 log mass - 4 . 9 0 2 , r 2 = 0.428, P < 0.05) in unaltered beetles. Depilation caused a substantial increase in conductance which varied between 0.0158 and 0.0213W °C - l (mean = 0.0191W °C -~, n = 8), and there was a significant relationship between mass and conductance (log conductance = - 0 . 6 5 7 log m a s s - 4 . 2 7 1 ,
Table 2. Relationships between various morphological parameters and body temperature (n = 100) Slope (mean + SE) A. Body mass Thoracic mass Abdominal mass Wing length Wing area Wing loading
-0.895 + -0.650 + 3.283 + 1.413 + 3.173 +
r2
P
0.558 0.909 0.238 0.194 0.749
0.057 + 0.019 0.414 + 0.II0
3.666 + 0.005 3.079+0.035
0.085 0.127
Abdominal mass
1.204 + 0.196
0.205 + 0.203
0.277
Wing length Wing area Wing loading T,h Tth--Ta
0.212 + 0.021 0.465 + 0.054 0.594+0.114 0.085 + 0.027 0.208-1-0.165
3.475 + 0.022 1.836 + 0.056 3.589+0.118 3.738 + 0.028 3.190+0.171
0.509 0.428 0.217 0.093 0.016
0.0001 0.0001 0.0001 0.0001 0.0020 0.2100
C. Wing loading Tth Tth-- T,
0.064 + 0.021 0.601 +0.116
3.460 + 0.063 1.184+0.345
0.087 0.217
0.0030 0.0001
Tth-T a
0.047 0.049 0.019 0.046 0.014
__ S E )
0.015 0.015 0.006 0.014 0.014
Tth
0.527 + 1.538 + 0.102 + 0.221 + 0.779 +
Intercept (mean
0.0001 0.0001 0.0001 0.0001 0.0001 0.0030 0.0001
B. Thoracic mass
The regression equations are in the form log Y = B log mass + A.
Temperature regulation in $. tiara
29
oo !
t-
0
° 8
'
0
'
'
'
'
50
'
'
'
'
~
'
100
'
,
150
,
I
i
,
,
,
200
,
i
250
i
,
i
,
,
300
i
i
,
350
,
,
,
~
,
,
400
,
,
,
450
,
,
500
Time (seconds) Fig. 2. Representative cooling curves for S. tiara: intact (0.654 g) (squares), depilated (0.686 g) (crosses), and with the wings and elytra removed (0.663 g) (stars). 0.586, P = 0.02). Removal of the wings and elytra also caused an increase in conductance which varied between 0.0125W °C-~ and 0.0153W °C-m (mean=0.0138W °C-I, n=8), and a significant relationship between mass and conductance was also found (log conductance -- -0.563 log mass - 4.594, r 2 ---- 0.647, P < 0.05). Endothermic warm-up was linear in all cases and varied between 2.64 and 6.76°C rain -m (mean = 4.67°C rain -1) at To of 25°C. r 2=
Physiological heat transfer Although the method used for artificially elevating Tth was not ideal for maintaining a large gradient in 7", between the abdomen and thorax, a consistent pattern of response to thoracic heating was clear. In live beetles T,b increased rapidly with increasing T~ and was accompanied by vigorous abdominal ventilation movements, whereas in dead beetles T,b increased less rapidly (Fig. 3). In live beetles,
i i/iiiiiii i 0
50
1O0
150
200
250
300
350
400
Tlme (seconds) Fig. 3. Relationship between thoracic and abdominal temperatures (T~ and T~a~)in a beetle subjected to thoracic heating. T~ live (crosses), T~ five (diagonal crosses), T.~ dead (stars).
30
S.L. Cnowr~ and C. H. SCHOLTZ
21
P "!
19
15
13 I 7:00
I
I
8:30
t
L
I
10:00
I
I
I
I
11:30
pm
t
I
1:00
I
L
I
I
2:30
t
I
t
4:00
I
I
I
5:30
I
I
7:00
am
Time Fig. 4. Operative temperatures (T=) for S. tiara in a resting and flying position from sunset to sunrise. Ta (squares), Te resting (stars), Tc flying (crosses). the maximum difference between Tab and Ta during heating varied between 46 and 75% (mean---62%, n - 5 ) of the difference between Tth and Ta, significantly different from the 20-59% ( m e a n = 4 3 % , n = 5) value found in dead beetles (Mann-Whitney U-test U = 2.09, P = 0.037). Microclimate and activity Figure 4 shows the variation in Ta and T0 in an individual in the resting position and in one suspended with the wings and elytra removed (flying position). Only after sunrise, when beetle activity has usually ceased, was there a noticeable difference between 7"= and Ta. Windspeed was below 0.3 m s -t. Beetle activity usually commenced after dark between 19:30 h and 20:00 h in October. At this time and until about 02:00 h, beetles arrived at the black light at a rate of 4-7 beetles per hour, but from 03:00 to 04:30 h there was at least a ten-fold increase in activity (30-40 beetles per hour). On one occasion 60 beetles were collected in < 15 rain. Beetles were never found flying when T~ was above 25°C, thus accounting for the absence of beetles flying before 03:00 h in January, but were otherwise active at a variety of temperatures and windspeeds and even during light rain. DISCUSSION
Like other nocturnal insects with high wing loading [e.g. moths (Bartholomew and Heinrich, 1973), beetles (Bartholomew and Casey, 1977a, b) and bees
(Stone and Willmer, 1989a)] endothermic warm-up is required prior to flight in S. tiara, presumably because of the physiological characteristics of beetle muscle (Josephson, 1981). Endothermic heat generation is probably due to isometric contraction of the asynchronous flight muscles, and rate of warm-up was within the range found for similar-sized beetles (Chappell, 1984; Heinrich and McClain, 1986; Nicolson and Louw, 1980; Morgan, 1987). Figure 1 shows that, in flight, S. tiara is a competent thermoregulator, capable of maintaining Tth at approx. 38°C over a ll°C range in ambient temperature, and the slope of Tth on Ta was substantially lower than that predicted by Oertli's (1989) data from other beetles. Tth was within the range found for similar-sized insects with similar wing loadings (see Bartholomew and Heinrich, 1973, 1978; Morgan, 1987), but may have been an overestimate because of inaccuracies associated with the "grab and stab" technique (Stone and Willmer, 1989b). Preliminary observations indicated, however, that on capture, S. tiara shows a brief rise in temperature followed by passive cooling (type b of Stone and Willmer, 1989b), thus reducing the magnitude of the inaccuracy. Because of the similarity of T, and Te found here, temperature excess (Tth--T=) represents an accurate estimate of the physiological offset temperature (see Casey, 1988). In general, scaling of the morphological parameters and body temperature on body mass departed markedly from interspecific scaling studies of bees of similar size and/or wing loading (Casey et al., 1985; Joos et ai., 1991). Body mass explained less of
Temperature regulation in S. tiara
31
Table 3. Relationships between morpholosical parameters and body mass in E. meriana Olivier Slope (Mean + SE)
(Mean + SE)
Intercept
0.144 + 0.089 0.244 + 0.173 0.757 + 0.171
0.824 + 0.014 1.257 + 0.027 - 1.257 + 0.027
r2
P
0.345 0.284 0.797
0.165 0.218 0.007
A. Body mass
Wing length Wing area Wing loading
The regression equations are in the form log Y = B log body mass + A. Data from Casey et al. (1985). the variation in thoracic mass, wing length and wing area in this study, and slopes of the regressions were generally lower, than in interspecific studies of scaling in similar-sized bees (Case), et al., 1985). As with most flying animals (Lighthill, 1977; but see Casey et al., 1985), much of the variation in wing loading in S. tiara was explained by body mass, although wing loading was not a good predictor of flight temperature. Interestingly, an intraspeeific analysis of the data, provided by Casey et al. (1985, Table 1), for Eulaema meriana Olivier, a bee slightly larger than S. tiara, gave results very similar to those found here, although only the regression of wing loading on body mass proved to be significant (Table 3), probably because of the small sample size. In S. tiara, thoracic mass was a better predictor of wing morphology and body temperature than body mass, because individuals varied in the gut-loads they were carrying (determined by dissection). Even so, exponents were either much lower (wing length and area) or higher (wing loading) than those associated with geometric similarity (i.e. wing length and loading= mass v3, wing area=mass:~3). Larger individuals have a relatively greater wing loading than small individuals and consequently a larger temperature excess, despite the fact that Tth is independent of body weight. This departure from geometric similarity indicates that in S. tiara, where body weight more than doubles between the smallest and largest individuals, there are factors (adaptive or developmental) influencing wing development which result in increased power output at a larger body size. Differences between intra- and interspecific scaling of morphometric parameters and body temperature on body mass have been documented elsewhere (e.g. Bartholomew and Heinrich, 1973), but have not been well studied. Wingstroke frequency was similar to that of E. meriana, a bee of similar mass and wing loading (Casey et al., 1985), but was higher than that predicted by Ocrtli (1989) from data on smaller beetles. In S. tiara, the slope of Tth on Ta was also far lower than that found for beetles with similar wingstroke frequency by Oertli (1989). TB 18/1---(2
Conductance was much lower than that previously recorded for other beetles [0.0114W °C-1 in Cotinus texana (Chappell, 1984), 0.0231 W °C -l in Pleocoma (Morgan, 1987), see also Bartholomew and Heinrich (1978)]. Depilation brought conductance within the range found for similar-sized beetles and indicates that the pile facilitates regulation of Tth at low ambient temperatures and during warm-up, particularly when the beeries are feeding and likely to be close to To (see Fig. 4). The contribution of the pile to a decrease in conductance is similar to that found in other hirsute, flying insects (see Church, 1960). With the elytra removed, the glabrous tergites are exposed and air trapped in the subely~ral cavity can no longer provide additional insulation. Although the resulting increase in conductance was not as high as that found in the case of depilation, it probably contributes substantially to cooling at high Tas, particularly during flight (flight speed ___3.9m s -l, unpublished data) when convective heat loss takes place (Church, 1960). Although the slope of the regression of Tab on Ta was < 1, which is indicative of passive cooling (Casey, 1988), the heat transfer experiments showed that live beetles actively dissipate heat from the abdomen. This implies that passive heat loss via the abdominal tergites is sufficient to balance heat production at lower Tas, but that at high Tas active mechanisms are required, a finding supported by a slope of the regression of Tab on Ta > 1 at T,s above 20°C. However, examination of heat transfer over a range of temperatures is required to substantiate this finding. At high Tas, T~ is probably controlled by pumping warm haemolymph from the thorax to the abdomen as is the case in other insects (e.g. Heinrich, 1971, 1976). During the heat transfer experiments, active abdominal pumping, such as that found in sphinx moths and bumble bees was also noted. Dissection of the abdomen of five individuals revealed that the dorsal aorta not only lies directly below the glabrous tergltes, but that it is lined by blind-ending, broad tracheae, which lead directly to the spiracles. This implies that, like Bombus vosnesenskii (Heinrich, 1976), S. tiara makes use of both
32
S.L. CHOWN and C. H. SCHOLTZ
haemolymph and air circulation to prevent thoracic overheating. No counter-current heat exchanger such as that found in bumble bees (Heinrich, 1976) was found, which suggests that the deep pile is adequate for thermoregulation at low T,s. Like other insects which are capable of warm-up at low temperatures (see Stone and Willmer, 1989a), S. tiara appears to be stressed at the relatively low Tas, because beetles were never found flying at Tas above 25°C, although such TaS are characteristic of the early evening from November to February. Physiological heat transfer has not been previously recorded in beetles although it has been thoroughly investigated in moths, flies, bees and dragonflies (Chappell, 1982; Heinrich, 1976; Heinrich and Casey, 1978; Willmer, 1982). During peak activity of S. flava (03:00-04:30 h) very few other insects and virtually no flying beetles are active. In the Kalahari, peak flight activity of the majority of nocturnal beetles is from dusk until about 22:00 h (personal observation). Insectivore activity is usually highest at this time (e.g. Rautenbach et al., 1988) and S.flava proved to be highly palatable when presented to locally common owls (Tyto alba and Otus leucotis) and a mammalian carnivore (Cynictis penicillata). It therefore seems likely that the thermoregulatory ability of S. tiara forms part of a strategy that enables this conspicuous and palatable beetle to feed and mate at a time when the risk of predation is low, but when the energetic cost of warm-up and flight is likely to be high, due to low T~s. This speculation is partly supported by the dearth of S. flava remains, compared to those of other nocturnal scarabs, in owl pellets. Morgan (1987) suggested that the nocturnal activity of Pleocoma also evolved in response to predation. Sparrmannia flava has a wing loading and body temperature similar to those recorded by Bartholomew and Heinrich 0978) for dung-feeding scarabaeids, but a much lower conductance. Therefore, despite the fact that it has a mass well under 2 g, this species shows many traits characteristic of larger beetles, such as an independence of thoracic temperature on body mass or wing loading and a well-developed capacity for thermo~gulation over a range of temperatures. Its low conductance probably also necessitates physiological heat transfer at high temperatures, making it unique amongst beetles examined to date. These traits, undoubtedly associated with the early-morning, anti-predator strategy adopted by S. tiara, make this species an exception to both Bartholomew and Heinrich's (1978) and Oertli's (1989) generalizations. The individualistic nature of the response of species to their environments is being highlighted both in eeophysiological (e.g. Bartholomew, 1987; Dyer and Seeley, 1987;
Underwood, 1991) and community ecological studies (see e.g. Drake, 1990; Roughgarden, 1989), and is evident in this study. We suggest that future studies of the thermal biology of beetles, particularly studies on scaling, should take cognizance of factors such as intraspecific scaling and the importance of thermal environments and individual strategies.
Acknowledgements--We thank Dr M. W. Mansell (National Collection of Insects, Pretoria) for assistance in the field, and Professor P. J. Cilliers (Department of Electronical Engineering, University of Pretoria) for assistance with the storage oscilloscope. We are grateful to the Director, National Parks Board for permission to work in the Kalahari Park, and to the Park Warden Mr E. Le Riche for assistance in the Park. This research was supported by grants from the University of Pretoria and the Foundation for Research Development (Pretoria). REFERENCES
Bartholomew G. A. (1981) A matter of size: an examination of endothermy in insects and terrestrial vertebrates. In Insect Thermoregulation (Edited by Heinrich B.), pp. 45-78. Wiley, New York. Bartholomew G. A. (1987) Interspecific comparison as a toot for ecological physiologists. In New Directions in Ecological Physiology (Edited by Feder M. E., Bennett A. F., Burggren W. W. and Huey R. B.), pp. 11-37. Cambridge University Press, Cambridge. Bartholomew G. A. and Casey T. M. (1977a) Endothermy during terrestrial activity in large beetles. Science 195, 882-883. Bartholomew G. A. and Casey T. M. (1977b) Body temperature and oxygen consumption during rest and activity in relation to size in some tropical beetles. J. therm. Biol. 2, 173-176. Bartholomew G. A. and Casey T. M. (1978) Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J. exp. Biol. 76, 11-25. Bartholomew G. A. and Epting R. J. (1975) Allometry of post-flight cooling rates in moths: a comparison with vertebrate homeotherms. J. exp. Biol. 63, 603-613. Bartholomew G. A. and Heinrich B. (1973) A field study of flight temperatures in moths in relation to body weight and wing loading. J. exp. Biol. 58, 123-135. Bartholomew G. A. and Heinrich B. (1978) Endothermy in African dung beetles during flight, ball making, and ball rolling. J. exp. Biol. 73, 65-83. Casey T. M. (1988) Thermoregulation and heat exchange.
Adv. Insect Physiol. 20, 119-146. Casey T. M. (1989) Oxygen consumption during flight. In
Insect Flight (Edited by Goldsworthy (3. J. and Wheeler C. H.), pp.257-272. CRC Press, Boca Raton, Fla. Casey T. M. and Joos B. A. (1983) Morphometries, conductance, thoracic temperature, and flight enetgvtics of noctuid and geometrid moths. Physiol. ZooL ~o, 160-173. Casey T. M., May M. L. and Morgan K. R. (1985) Flight energetics of euglossine bees in relation to morphology and wing stroke frequency. J. exp. Biol. 116,
271-289.
Temperature regulation in S. flava Chappell M. A. (1982) Temperature regulation of carpenter bees (Xylocopa californica) foraging in the Colorado desert of southern California. Physiol. Zool. 55, 267-280. ChappeU M. A. (1984) Thermoregulation and energetics of the green fig beetle (Cotinus texana) during flight and foraging behaviour. Physiol. Zool. 57, 581-589. Church N. S. (1960) Heat loss and the body temperatures of flying insects. II. Heat conduction within the body and its loss by radiation and convection. J. exp. Biol. 37, 186-212. Cossins A. R. and Bowler K. (1987) Temperature Biology of Animals, p. 339. Chapman & Hall, London. DeVries P. J. and Dudley R. (1990) Morphometrics, airspeed, thermoregulation, and lipid reserves of migrating Uraniafulgens (Uraniidae) moths in natural free flight. Physiol. Zool. 63, 235-251. Drake J. A. (1990) Communities as assembled structures: do rules govern pattern? TREE 5, 159-164. Dyer F. C. and Seeley T. D. (1987) Interspecific comparisons of endothermy in honey-bees (Apis): deviations from the expected size-related patterns. J. exp. Biol. 127, 1-26. Ellington C. P. (1984) The aerodynamics of hovering insect flight. II. Morphological parameters. Phil. Trans. R. Soc. Lend. B 305, 17-40. Heinrich B. (1971) Temperature regulation of the sphinx moth, Manduca sexta. II. Regulation of heat loss by control of blood circulation. J. exp. Biol. 54, 153-166. Heinrich B. (1976) Heat exchange in relation to blood flow between thorax and abdomen in bumblebees. J. exp. BioL 64, 561-585. Heinrich B. (1981a) Insect Thermoregulation, p. 304. Wiley, New York. Heinrich B. (1981b) Ecological and evolutionary perspectives. In Insect Thermoregulation (Edited by Heinrich B.), pp. 235-302. Wiley, New York. Heinrich B. and Bartholomew G. A. (1979) Roles of endothermy and size in inter- and intraspecific competition for elephant dung in African dung beetles, Scarabaeus laevistriatus. Physiol. Zool 52, 484--496. Heinrich B. and Casey T. M. (1978) Heat transfer in dragonflies: 'fliers' and 'perchers'. J. exp. Biol. 74, 17-36. Heinrich B. and McClain E. (1986) "Laziness" and hypothermia as a foraging strategy in flower scarabs (Coleoptera: Scarabaeidae). Physiol. Zool. 59, 273-282. Joos B. A., Young P. A. and Casey T. M. (1991) Wingstroke frequency of foraging and hovering bumblebees in relation to morphology and temperature. Physiol. Ent. 16, 191-200. Josephson R. K. (1981) Temperature and the mechanical performance of insect muscle. In Insect Thermoregulation (Edited by Heinrich B.), pp. 19~4. Wiley, New York, Kammer A. E. (1981) Physiological mechanisms of thermoregulation. In Insect Thermoregulation (Edited by Heinrich B.), pp. 115-158. Wiley, New York.
33
Krogh A. and Zeuthen E. (1941) The mechanism of flight preparation in some insects. J. exp. Biol. 18, 1-9. Lighthill J. (1977) Introduction to the scaling of aerial locomotion. In Scale Effects in Animal Locomotion (Edited by Pedley T. J.), pp. 365-404. Academic Press, London. May M. L. (1976) Thermoregulation and adaptation to temperature in dragonflies (Odonata: Anisoptera). Ecol. Monogr. 46, 1-32. May M. L. (1979) Insect thermoregulation. A. Rev. Ent. 24, 313-349. May M. L. (1981) Wingstroke frequency of dragonflies (Odonata: Anisoptera) in relation of temperature and body size. J. comp. Physiol. B. 144, 229-240. Morgan K. R. (1987) Temperature regulation, energy metabolism and mate searching in rain beetles (Pleocoma spp), winter-active, endothermic scarabs (Coleoptera). J. exp. Biol. 128, 107-122. Morgan K. R. and Shelley T. E. (1988) Body temperature regulation in desert robber flies (Diptera: Asilidae). Ecol. Ent. 14, 419-428. Nicolson S. W. and Louw G. N. (1980) Preflight thermogenesis, conductance and thermoregulation in the protea beetle, Trichostetha fascicularis (Scarabaeidae: Cetoniinae). S. Afr. J. Sci. 76, 124-126. Oertli J. J. (1989) Relationship of wing beat frequency and temperature during take-off flight in temperate-zone beetles. J. exp. Biol. 145, 321-338. Rautenbach I. L., Kemp A. C. and Scholtz C. H. (1988) Fluctuations in availability of arthropods correlated with microchiropteran and avian predator activities. Koedoe 31, 77-90. Roughgarden J. (1989) The structure and assembly of communities. In Perspectives in Ecological Theory (Edited by Roughgarden J., May R. M. and Levin S. A.), pp. 203-226. Princeton University Press, Princeton, N.J. Scholtz C. H. (1988) Biology of Sparrmannia tiara Arrow (Coleoptera: Scarabaeidae: Melolonthinae). Coleopts Bull. 42, 57~12. Stone G. N. and Willmer P. G. (1989a) Warm-up rates and body temperatures in bees: the importance of body size, thermal regime and phylogeny. J. exp. Biol. 147, 303-328. Stone G. N. and Willmer P. G, (1989b) Endothermy and temperature regulation in bees: a critique of 'grab and stab' measurement of body temperature. J. exp. Biol. 143, 211-223. Underwood B. A. (1991) Thermoregulation and energetic decision-making by the honeybees Apis cerana, Apis dorsata and Apis laboriosa. J. exp. Biol. 157, 19-34. Unwin D. M. and Corbert S. A. (1984) Wingbeat frequency, temperature and body size in bees and flies. Physiol. Ent. 9, 115-121. Willmer P. G. (1982) Thermoregulatory mechanisms in Sarcophaga. Oecologia 53, 382-385.
0306-4565]93 $6.00 + 0.00
Printed in Great Britain. All rights reserved
Copyright ~) 1993 Pergamon Press Lid
TEMPERATURE REGULATION IN THE NOCTURNAL MELOLONTHINE SPARRMANNIA FLAVA S. L. CHOWN and C. H. SCHOLTZ Department of Entomology, University of Pretoria, Pretoria 0002, South Africa (Received 18 September 1992; accepted in revised form 7 October 1992)
AbsU'act--1. Sparrmanniaflava Arrow (Coleoptera: Scarabaeidae) regulated thoracic temperature (Tth) during flight at 38.6°C over an ambient temperature (T~) range of 11°C. 2. Tth and wing loading (19.99 Nm -2) were within the range predicted by body mass (0.80 g) based on previous studies of scaling in beetles, although conductance (0.0087 W °C-~) was considerably lower and wingstroke frequency (87 Hz) higher than that previously recorded in beetles of similar mass. 3. The slope of the regression of abdominal temperature (Tab) on Ta, at Tas > 20°C, was > 1, and physiological heat transfer was demonstrated experimentally, suggesting that low conductance necessitates active heat transfer at high Tas. 4. Sparrmannia flava's early-morning, anti-predator strategy involves adaptations which make it an exception to previous generalizations concerning the thermal biology of beetles. Key Word Index: Thermoregulation; wingstroke frequency; morphology; Coleoptera; Sparrmanniaflava
(1981) and others (e.g. Kammer, 1981) to conclude that the ability of endothermic insects to maintain and regulate elevated thoracic temperatures in flight is strongly size-dependent. After examining the relationships between body mass, temperature sensitivity of wing beat frequency and thermal biology of 24 Holarctic beetle species (all weighing < 1 g), Oertli (1989) concluded, however, that body mass per se was less important than wing stroke frequency, in accounting for thermoregulatory precision and thermal sensitivity of wing stroke frequency. Nonetheless, Oertli (1989) found that larger beetles were generally thermoconformers whereas smaller beetles had greater thermoregulatory precision. Although not explicitly addressed in the literature, this discrepancy between Bartholomew and Heinrich's (1978) and Oertli's (1989) findings concerning the relationship between size and thermal biology is apparent in other studies of beetles. Chappell (1984) found that Cotinus texana (ca 1.29 g) maintained its body temperature up to 12°C above ambient while foraging and regulated thoracic temperature during flight, and Morgan (1987) documented a highly developed capacity for thermoregulation during flight and terrestrial activity in rain beetles (Pleocoma spp 0.6-1.7 g). In contrast, Heinrich and McClain (1986) found that despite a well developed capacity for endothermy, Pachnoda sinuata (ca 0.94 g) did not regulate thoracic temperature during flight and maintained body temperature close to ambient while foraging. The same sort of strategy also seems to be
INTRODUCTION
The thermal biology of bradymetabolic animals has been the subject of extensive research over the past two decades (see review in Cossins and Bowler, 1987). Flying insects, in particular, have enjoyed considerable attention, and relationships between the abiotic environment (particularly ambient temperature), body temperatures, morphology, metabolic rate, and wing morphology and stroke frequency, have been thoroughly investigated (see e.g. Casey, 1988, 1989; Heinrich, 1981a; May, 1979, 1981). Most of this work has been conducted on bees (e.g. Casey et al., 1985; Joos et al., 1991; Stone and Willmer, 1989a), flies (e.g. Morgan and Shelley, 1988; Unwin and Corbert, 1984; Willmer, 1982) and moths (e.g. Bartholomew and Casey, 1978; Bartholomew and Epting, 1975; Casey and Joos, 1983; DeVries and Dudley, 1990), while the Coleoptera have enjoyed less attention. Krogh and Zeuthen (1941) first noted endothermy in beetles, and comparative work was initiated by Bartholomew and Casey (1977a, b), Bartholomew and Heinrich (1978) and Heinrich and Bartholomew (1979). As a result of their studies, Bartholomew and Heinrich (1978) suggested that in beetles lighter than 2 g, body temperature is a passive function of the balance between rates of heat production and heat loss, but that in heavier beetles regulatory mechanisms are involved. This finding was in accord with studies of other insects (e.g. Bartholomew and Heinrich, 1973; May, 1976) and led Bartholomew 25
26
S.L. CHOWNand C. H. SCHOLTZ
followed by Trichostetha fascicularis (see Nicolson and Louw, 1980, p. 125 and Fig. 2), although the authors did not address this point. Heinrich (1981b) pointed out that body temperature in insects is determined not only by constraints of size, but also by constraints of insulation, metabolic rate and wing loading, while subsequent studies of moths (Casey and Joos, 1983) and bees (Dyer and Seeley, 1987; Joos et al., 1991; Stone and Willmer, 1989a; Underwood, 1991) have highlighted the influences on body temperature of aerodynamic configuration, phylogeny and the adaptations of a given species to a particular thermal environment. If in moths and bees such a myriad of factors influence the thermal biology of a species, it is likely that this will be the case in the Coleoptera. The difference between Bartholomew and Heinrich's (1978) and Oertli's (1989) findings is a pertinent example, making evident the need for further data on the thermal biology of flying beetles. In this paper, we examine the thermal biology of a nocturnal, melolonthine scarab, Sparrmanniaflava Arrow (Coleoptera: Scarabaeidae) to provide such information. MATERIALS AND METHODS
Study site This study was done during three 10 day visits, in October 1990, October 1991 and January 1992, to Twee Rivieren camp (26°28'S, 30°37'E) in the Kalahari Gemsbok National Park in the northwestern Cape Province of South Africa. Sparrmannia tiara is extremely abundant in the Kalahari Desert and is unique amongst melolonthines because the larvae feed on the dung of medium-sized antelope (Seholtz, 1988). Adults are large, active melolonthines which spend the day below the soil surface, emerging in the evening or early morning to feed on angiosperm foliage.
Body temperature, morphology, wing morphology and wingstroke frequency All beetles were collected at a black light (Bioquip California) which was run from sunset to sunrise. Thoracic (Tth) and abdominal (Tab) temperatures of beetles, knocked to the ground while flying to the light, were measured to the nearest 0.1°C using 40-gauge copper-constantan thermocouples, glued into hypodermic needles, and a Kane--May 457 XP digital thermometer. All measurements were completed within 5-8 s. Ambient temperature (T,) and humidity were monitored continuously using a Novasina thermo-hygrometer and the former checked against T, measured by the dried thermoeouple. The beetles were subsequently weighed to the nearest mg
with a Sauter electronic balance, and abdominal and thoracic masses were also determined. Wing areas were determined by converting the mass of a photocopy of the fight wing to area using a mass-area regression of the paper (Bartholomew and Heinrich, 1978). Wing length was measured from the basal sclerites to the tip of the leading edge using Vernier calipers. Wing loading was determined by dividing the area of the wings by the beetle's wet mass. Aspect ratio was calculated using the formula provided by EUington (1984). A total of 100 beetles was examined. Wingstroke frequency of eight beetles was recorded using an Audio Technica AT9300 directional microphone and Sony TCM-6 portable casette recorder. Wingstroke frequency was obtained from the recordings using a Kikusui 5020A storage oscilloscope.
Conductance and endothermic warm-up Cooling rates were determined using thermocouples (as above) fixed into the thorax of 26 freshlykilled beetles. Of these, ten were unaltered beetles, eight specimens had the thoracic and abdominal pile removed, using a fine scalpel blade and microscissors, and the elytra and wings were removed from eight individuals to simulate the flying posture. The beetles were heated by an incandescent lamp to 40°C and then allowed to cool, in a 40 x 40 x 30 cm insulated plastic container, while Tth and Ta were recorded every 15 s. The experiment was terminated when beetles were within 2°C of the ambient temperature. Thermal conductance was calculated from cooling rates using the methods outlined by Casey and Joos (1983) and Morgan (1987). To determine rates of endothermic warm-up, beetles were kept in sand overnight. On the following evening, thermocouples were implanted in the thorax of these specimens. This usually stimulated warm-up and Tth was recorded at 5 s intervals in eight specimens.
Physiological heat transfer The possibility of heat transfer from thorax to abdomen was investigated using a modification of Chappell's (1982) method. Live specimens were crosspinned to a Styrofoam block with thermocouples inserted into the thorax and abdomen. The thorax was heated by incandescent lamp while the abdomen was shielded using layers of cardboard and reflective foil, and simultaneous measurements of Tth and Tab were taken to a Tth of ca 40°C. The animal was then killed by injection of a drop of ethyl acetate, allowed to cool, and the procedure repeated.
Microclimate and activity Microclimate experienced by beetles was measured in terms of operative temperature (Te) by mounting
Temperature regulation in S. tiara thermocouple-equipped dried beetles in a flying and foraging posture (see Morgan and Shelly, 1988). To, T, and windspeed (using a conventional cup anemometer) were monitored from sunset to sunrise. The number of beetles arriving at the light was monitored on an hourly basis each night, together with Ta, windspeed and relative humidity (see above).
27 RESULTS
Body temperature, morphology, wing morphology and wingstroke frequency The Tth of S. tiara ranged from 34.5 to 42.4°C (mean = 38.6°C, SD = 1.47, n = 100) at T= ranging from 13.1 to 24.3°C [Fig. I(A), Table l], and the slope of the regression of T,h on T= (Tth = 0.015 Ta + 38.27)
A
4 I ............................................ 0 42 ° ~11
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.................... .
.
.
.
.
.
.
mm
4oh,.
...........................................
,=,
~.~F'"
...... ; ......................................
~_ ~4 L .....
......................
....
'"
..
.........
I
.... I
........ ~ ....
.............................
......
, ....
F 32
13
14
15
16 '
31
17
18
19
20
21
22
23
24
25
Ambient temperature °C
B
~,,~.~.~
13
14
.................. ... ........................
15
16
17
18
19
20
21
22
23
24
25
Ambient temperature °C Fig. 1. Relationship of thoracic (A) and abdominal (B) temperature to ambient air temperature. Equation for the line in (A): Y=0.015 X + 38.27, and in (B): Y=0.811 X+8.19.
28
S.L. CHOWNand C. H. SCHOLTZ
Table 1. Summary statistics for morphological parameters of S. tiara (n = 100) Mean Body mass (g) Thoracic mass (g) Abdominal mass (g) Wing length (ram) Wing area (cm2) Wing loading (Nm -2) Aspect ratio
0.796 0.362 0.376 26.00 3.91 19.99 6.958
SD
Min
0.158 0.486 0.048 0.236 0.129 0.170 1.06 22.7 0.38 2.77 3.611 11.46 0.478 5.577
Max 1.329 0.440 0.840 28.8 5.01 32.17 8.866
was not significantly different from zero (t = 0.448, P = 0.65). The greatest temperature excess recorded was 29.1°C and the lowest 10.9°C (mean = 20.1°C), and a m i n i m u m flight T~h of 34-35°C was estimated from the lowest fright temperatures measured. These are probably slight overestimates because beetles closed their elytra on capture, elevating Tth by 1-2°C. Abdominal temperatures ranged between 14.2 and 30.4°C ( m e a n = 2 3 . 1 4 , S D = 4 . 3 0 , n = 1 0 0 ) [Fig. I(B)] and the slope of the regression of T~b on Ta (Tab = 0.811 Ta + 8.19) was significantly < 1 ( t = - - 4 . 4 1 4 , P <0.001). However, above a T~ of 20°C, the slope of the regression of Tab on T~ (Tab = 1.571 Ta -- 8.78, r 2 = 0.458, n = 55, P < 0.001) was significantly > 1 (t = 2.408, P < 0.05). Summary statistics for size, thoracic mass, abdominal mass, Tth, wing length, area and loading and aspect ratio are provided in Table 1. Both thoracic and abdominal mass accounted for approx. 46% of body mass (30-58% in the former, 31-65% in the latter). Thoracic mass scaled with 0.53 of body
mass and abdominal mass scaled with 1.54 of body mass (Table 2). Thoracic and abdominal mass were not highly correlated indicating that individuals were carrying different loads. Thoracic mass accounted for more of the variance in both wing length and area than did body mass (Table 2), although the reverse was true of wing loading which scaled as body mass °Ts. Significant, but weak relationships between either body mass, thoracic mass or wing loading, and Tth were found. Temperature excess ( T t h - T~) was correlated with wing loading and body mass, but not with thoracic mass. Wingstroke frequency at a T~ of 14°C varied between 78 and 111 Hz (mean = 86.9, SD = 11.3, n = 8). Conductance and endothermic warm-up
Semilogarithmic plots of the cooling data (Tth--Ta) were accurately described by linear regressions (r 2 > 0.982 in all cases), and representative data for beetles with and without elytra and the dense pile are provided in Fig. 2. Conductance varied between 0.0077W °C -~ and 0.0093W °C -l ( m e a n = 0 . 0 0 8 7 W °C -t, n = 10) and there was a significant inverse relationship between mass and conductance (log c o n d u c t a n c e - - - 0 . 3 5 3 log mass - 4 . 9 0 2 , r 2 = 0.428, P < 0.05) in unaltered beetles. Depilation caused a substantial increase in conductance which varied between 0.0158 and 0.0213W °C - l (mean = 0.0191W °C -~, n = 8), and there was a significant relationship between mass and conductance (log conductance = - 0 . 6 5 7 log m a s s - 4 . 2 7 1 ,
Table 2. Relationships between various morphological parameters and body temperature (n = 100) Slope (mean + SE) A. Body mass Thoracic mass Abdominal mass Wing length Wing area Wing loading
-0.895 + -0.650 + 3.283 + 1.413 + 3.173 +
r2
P
0.558 0.909 0.238 0.194 0.749
0.057 + 0.019 0.414 + 0.II0
3.666 + 0.005 3.079+0.035
0.085 0.127
Abdominal mass
1.204 + 0.196
0.205 + 0.203
0.277
Wing length Wing area Wing loading T,h Tth--Ta
0.212 + 0.021 0.465 + 0.054 0.594+0.114 0.085 + 0.027 0.208-1-0.165
3.475 + 0.022 1.836 + 0.056 3.589+0.118 3.738 + 0.028 3.190+0.171
0.509 0.428 0.217 0.093 0.016
0.0001 0.0001 0.0001 0.0001 0.0020 0.2100
C. Wing loading Tth Tth-- T,
0.064 + 0.021 0.601 +0.116
3.460 + 0.063 1.184+0.345
0.087 0.217
0.0030 0.0001
Tth-T a
0.047 0.049 0.019 0.046 0.014
__ S E )
0.015 0.015 0.006 0.014 0.014
Tth
0.527 + 1.538 + 0.102 + 0.221 + 0.779 +
Intercept (mean
0.0001 0.0001 0.0001 0.0001 0.0001 0.0030 0.0001
B. Thoracic mass
The regression equations are in the form log Y = B log mass + A.
Temperature regulation in $. tiara
29
oo !
t-
0
° 8
'
0
'
'
'
'
50
'
'
'
'
~
'
100
'
,
150
,
I
i
,
,
,
200
,
i
250
i
,
i
,
,
300
i
i
,
350
,
,
,
~
,
,
400
,
,
,
450
,
,
500
Time (seconds) Fig. 2. Representative cooling curves for S. tiara: intact (0.654 g) (squares), depilated (0.686 g) (crosses), and with the wings and elytra removed (0.663 g) (stars). 0.586, P = 0.02). Removal of the wings and elytra also caused an increase in conductance which varied between 0.0125W °C-~ and 0.0153W °C-m (mean=0.0138W °C-I, n=8), and a significant relationship between mass and conductance was also found (log conductance -- -0.563 log mass - 4.594, r 2 ---- 0.647, P < 0.05). Endothermic warm-up was linear in all cases and varied between 2.64 and 6.76°C rain -m (mean = 4.67°C rain -1) at To of 25°C. r 2=
Physiological heat transfer Although the method used for artificially elevating Tth was not ideal for maintaining a large gradient in 7", between the abdomen and thorax, a consistent pattern of response to thoracic heating was clear. In live beetles T,b increased rapidly with increasing T~ and was accompanied by vigorous abdominal ventilation movements, whereas in dead beetles T,b increased less rapidly (Fig. 3). In live beetles,
i i/iiiiiii i 0
50
1O0
150
200
250
300
350
400
Tlme (seconds) Fig. 3. Relationship between thoracic and abdominal temperatures (T~ and T~a~)in a beetle subjected to thoracic heating. T~ live (crosses), T~ five (diagonal crosses), T.~ dead (stars).
30
S.L. Cnowr~ and C. H. SCHOLTZ
21
P "!
19
15
13 I 7:00
I
I
8:30
t
L
I
10:00
I
I
I
I
11:30
pm
t
I
1:00
I
L
I
I
2:30
t
I
t
4:00
I
I
I
5:30
I
I
7:00
am
Time Fig. 4. Operative temperatures (T=) for S. tiara in a resting and flying position from sunset to sunrise. Ta (squares), Te resting (stars), Tc flying (crosses). the maximum difference between Tab and Ta during heating varied between 46 and 75% (mean---62%, n - 5 ) of the difference between Tth and Ta, significantly different from the 20-59% ( m e a n = 4 3 % , n = 5) value found in dead beetles (Mann-Whitney U-test U = 2.09, P = 0.037). Microclimate and activity Figure 4 shows the variation in Ta and T0 in an individual in the resting position and in one suspended with the wings and elytra removed (flying position). Only after sunrise, when beetle activity has usually ceased, was there a noticeable difference between 7"= and Ta. Windspeed was below 0.3 m s -t. Beetle activity usually commenced after dark between 19:30 h and 20:00 h in October. At this time and until about 02:00 h, beetles arrived at the black light at a rate of 4-7 beetles per hour, but from 03:00 to 04:30 h there was at least a ten-fold increase in activity (30-40 beetles per hour). On one occasion 60 beetles were collected in < 15 rain. Beetles were never found flying when T~ was above 25°C, thus accounting for the absence of beetles flying before 03:00 h in January, but were otherwise active at a variety of temperatures and windspeeds and even during light rain. DISCUSSION
Like other nocturnal insects with high wing loading [e.g. moths (Bartholomew and Heinrich, 1973), beetles (Bartholomew and Casey, 1977a, b) and bees
(Stone and Willmer, 1989a)] endothermic warm-up is required prior to flight in S. tiara, presumably because of the physiological characteristics of beetle muscle (Josephson, 1981). Endothermic heat generation is probably due to isometric contraction of the asynchronous flight muscles, and rate of warm-up was within the range found for similar-sized beetles (Chappell, 1984; Heinrich and McClain, 1986; Nicolson and Louw, 1980; Morgan, 1987). Figure 1 shows that, in flight, S. tiara is a competent thermoregulator, capable of maintaining Tth at approx. 38°C over a ll°C range in ambient temperature, and the slope of Tth on Ta was substantially lower than that predicted by Oertli's (1989) data from other beetles. Tth was within the range found for similar-sized insects with similar wing loadings (see Bartholomew and Heinrich, 1973, 1978; Morgan, 1987), but may have been an overestimate because of inaccuracies associated with the "grab and stab" technique (Stone and Willmer, 1989b). Preliminary observations indicated, however, that on capture, S. tiara shows a brief rise in temperature followed by passive cooling (type b of Stone and Willmer, 1989b), thus reducing the magnitude of the inaccuracy. Because of the similarity of T, and Te found here, temperature excess (Tth--T=) represents an accurate estimate of the physiological offset temperature (see Casey, 1988). In general, scaling of the morphological parameters and body temperature on body mass departed markedly from interspecific scaling studies of bees of similar size and/or wing loading (Casey et al., 1985; Joos et ai., 1991). Body mass explained less of
Temperature regulation in S. tiara
31
Table 3. Relationships between morpholosical parameters and body mass in E. meriana Olivier Slope (Mean + SE)
(Mean + SE)
Intercept
0.144 + 0.089 0.244 + 0.173 0.757 + 0.171
0.824 + 0.014 1.257 + 0.027 - 1.257 + 0.027
r2
P
0.345 0.284 0.797
0.165 0.218 0.007
A. Body mass
Wing length Wing area Wing loading
The regression equations are in the form log Y = B log body mass + A. Data from Casey et al. (1985). the variation in thoracic mass, wing length and wing area in this study, and slopes of the regressions were generally lower, than in interspecific studies of scaling in similar-sized bees (Case), et al., 1985). As with most flying animals (Lighthill, 1977; but see Casey et al., 1985), much of the variation in wing loading in S. tiara was explained by body mass, although wing loading was not a good predictor of flight temperature. Interestingly, an intraspeeific analysis of the data, provided by Casey et al. (1985, Table 1), for Eulaema meriana Olivier, a bee slightly larger than S. tiara, gave results very similar to those found here, although only the regression of wing loading on body mass proved to be significant (Table 3), probably because of the small sample size. In S. tiara, thoracic mass was a better predictor of wing morphology and body temperature than body mass, because individuals varied in the gut-loads they were carrying (determined by dissection). Even so, exponents were either much lower (wing length and area) or higher (wing loading) than those associated with geometric similarity (i.e. wing length and loading= mass v3, wing area=mass:~3). Larger individuals have a relatively greater wing loading than small individuals and consequently a larger temperature excess, despite the fact that Tth is independent of body weight. This departure from geometric similarity indicates that in S. tiara, where body weight more than doubles between the smallest and largest individuals, there are factors (adaptive or developmental) influencing wing development which result in increased power output at a larger body size. Differences between intra- and interspecific scaling of morphometric parameters and body temperature on body mass have been documented elsewhere (e.g. Bartholomew and Heinrich, 1973), but have not been well studied. Wingstroke frequency was similar to that of E. meriana, a bee of similar mass and wing loading (Casey et al., 1985), but was higher than that predicted by Ocrtli (1989) from data on smaller beetles. In S. tiara, the slope of Tth on Ta was also far lower than that found for beetles with similar wingstroke frequency by Oertli (1989). TB 18/1---(2
Conductance was much lower than that previously recorded for other beetles [0.0114W °C-1 in Cotinus texana (Chappell, 1984), 0.0231 W °C -l in Pleocoma (Morgan, 1987), see also Bartholomew and Heinrich (1978)]. Depilation brought conductance within the range found for similar-sized beetles and indicates that the pile facilitates regulation of Tth at low ambient temperatures and during warm-up, particularly when the beeries are feeding and likely to be close to To (see Fig. 4). The contribution of the pile to a decrease in conductance is similar to that found in other hirsute, flying insects (see Church, 1960). With the elytra removed, the glabrous tergites are exposed and air trapped in the subely~ral cavity can no longer provide additional insulation. Although the resulting increase in conductance was not as high as that found in the case of depilation, it probably contributes substantially to cooling at high Tas, particularly during flight (flight speed ___3.9m s -l, unpublished data) when convective heat loss takes place (Church, 1960). Although the slope of the regression of Tab on Ta was < 1, which is indicative of passive cooling (Casey, 1988), the heat transfer experiments showed that live beetles actively dissipate heat from the abdomen. This implies that passive heat loss via the abdominal tergites is sufficient to balance heat production at lower Tas, but that at high Tas active mechanisms are required, a finding supported by a slope of the regression of Tab on Ta > 1 at T,s above 20°C. However, examination of heat transfer over a range of temperatures is required to substantiate this finding. At high Tas, T~ is probably controlled by pumping warm haemolymph from the thorax to the abdomen as is the case in other insects (e.g. Heinrich, 1971, 1976). During the heat transfer experiments, active abdominal pumping, such as that found in sphinx moths and bumble bees was also noted. Dissection of the abdomen of five individuals revealed that the dorsal aorta not only lies directly below the glabrous tergltes, but that it is lined by blind-ending, broad tracheae, which lead directly to the spiracles. This implies that, like Bombus vosnesenskii (Heinrich, 1976), S. tiara makes use of both
32
S.L. CHOWN and C. H. SCHOLTZ
haemolymph and air circulation to prevent thoracic overheating. No counter-current heat exchanger such as that found in bumble bees (Heinrich, 1976) was found, which suggests that the deep pile is adequate for thermoregulation at low T,s. Like other insects which are capable of warm-up at low temperatures (see Stone and Willmer, 1989a), S. tiara appears to be stressed at the relatively low Tas, because beetles were never found flying at Tas above 25°C, although such TaS are characteristic of the early evening from November to February. Physiological heat transfer has not been previously recorded in beetles although it has been thoroughly investigated in moths, flies, bees and dragonflies (Chappell, 1982; Heinrich, 1976; Heinrich and Casey, 1978; Willmer, 1982). During peak activity of S. flava (03:00-04:30 h) very few other insects and virtually no flying beetles are active. In the Kalahari, peak flight activity of the majority of nocturnal beetles is from dusk until about 22:00 h (personal observation). Insectivore activity is usually highest at this time (e.g. Rautenbach et al., 1988) and S.flava proved to be highly palatable when presented to locally common owls (Tyto alba and Otus leucotis) and a mammalian carnivore (Cynictis penicillata). It therefore seems likely that the thermoregulatory ability of S. tiara forms part of a strategy that enables this conspicuous and palatable beetle to feed and mate at a time when the risk of predation is low, but when the energetic cost of warm-up and flight is likely to be high, due to low T~s. This speculation is partly supported by the dearth of S. flava remains, compared to those of other nocturnal scarabs, in owl pellets. Morgan (1987) suggested that the nocturnal activity of Pleocoma also evolved in response to predation. Sparrmannia flava has a wing loading and body temperature similar to those recorded by Bartholomew and Heinrich 0978) for dung-feeding scarabaeids, but a much lower conductance. Therefore, despite the fact that it has a mass well under 2 g, this species shows many traits characteristic of larger beetles, such as an independence of thoracic temperature on body mass or wing loading and a well-developed capacity for thermo~gulation over a range of temperatures. Its low conductance probably also necessitates physiological heat transfer at high temperatures, making it unique amongst beetles examined to date. These traits, undoubtedly associated with the early-morning, anti-predator strategy adopted by S. tiara, make this species an exception to both Bartholomew and Heinrich's (1978) and Oertli's (1989) generalizations. The individualistic nature of the response of species to their environments is being highlighted both in eeophysiological (e.g. Bartholomew, 1987; Dyer and Seeley, 1987;
Underwood, 1991) and community ecological studies (see e.g. Drake, 1990; Roughgarden, 1989), and is evident in this study. We suggest that future studies of the thermal biology of beetles, particularly studies on scaling, should take cognizance of factors such as intraspecific scaling and the importance of thermal environments and individual strategies.
Acknowledgements--We thank Dr M. W. Mansell (National Collection of Insects, Pretoria) for assistance in the field, and Professor P. J. Cilliers (Department of Electronical Engineering, University of Pretoria) for assistance with the storage oscilloscope. We are grateful to the Director, National Parks Board for permission to work in the Kalahari Park, and to the Park Warden Mr E. Le Riche for assistance in the Park. This research was supported by grants from the University of Pretoria and the Foundation for Research Development (Pretoria). REFERENCES
Bartholomew G. A. (1981) A matter of size: an examination of endothermy in insects and terrestrial vertebrates. In Insect Thermoregulation (Edited by Heinrich B.), pp. 45-78. Wiley, New York. Bartholomew G. A. (1987) Interspecific comparison as a toot for ecological physiologists. In New Directions in Ecological Physiology (Edited by Feder M. E., Bennett A. F., Burggren W. W. and Huey R. B.), pp. 11-37. Cambridge University Press, Cambridge. Bartholomew G. A. and Casey T. M. (1977a) Endothermy during terrestrial activity in large beetles. Science 195, 882-883. Bartholomew G. A. and Casey T. M. (1977b) Body temperature and oxygen consumption during rest and activity in relation to size in some tropical beetles. J. therm. Biol. 2, 173-176. Bartholomew G. A. and Casey T. M. (1978) Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J. exp. Biol. 76, 11-25. Bartholomew G. A. and Epting R. J. (1975) Allometry of post-flight cooling rates in moths: a comparison with vertebrate homeotherms. J. exp. Biol. 63, 603-613. Bartholomew G. A. and Heinrich B. (1973) A field study of flight temperatures in moths in relation to body weight and wing loading. J. exp. Biol. 58, 123-135. Bartholomew G. A. and Heinrich B. (1978) Endothermy in African dung beetles during flight, ball making, and ball rolling. J. exp. Biol. 73, 65-83. Casey T. M. (1988) Thermoregulation and heat exchange.
Adv. Insect Physiol. 20, 119-146. Casey T. M. (1989) Oxygen consumption during flight. In
Insect Flight (Edited by Goldsworthy (3. J. and Wheeler C. H.), pp.257-272. CRC Press, Boca Raton, Fla. Casey T. M. and Joos B. A. (1983) Morphometries, conductance, thoracic temperature, and flight enetgvtics of noctuid and geometrid moths. Physiol. ZooL ~o, 160-173. Casey T. M., May M. L. and Morgan K. R. (1985) Flight energetics of euglossine bees in relation to morphology and wing stroke frequency. J. exp. Biol. 116,
271-289.
Temperature regulation in S. flava Chappell M. A. (1982) Temperature regulation of carpenter bees (Xylocopa californica) foraging in the Colorado desert of southern California. Physiol. Zool. 55, 267-280. ChappeU M. A. (1984) Thermoregulation and energetics of the green fig beetle (Cotinus texana) during flight and foraging behaviour. Physiol. Zool. 57, 581-589. Church N. S. (1960) Heat loss and the body temperatures of flying insects. II. Heat conduction within the body and its loss by radiation and convection. J. exp. Biol. 37, 186-212. Cossins A. R. and Bowler K. (1987) Temperature Biology of Animals, p. 339. Chapman & Hall, London. DeVries P. J. and Dudley R. (1990) Morphometrics, airspeed, thermoregulation, and lipid reserves of migrating Uraniafulgens (Uraniidae) moths in natural free flight. Physiol. Zool. 63, 235-251. Drake J. A. (1990) Communities as assembled structures: do rules govern pattern? TREE 5, 159-164. Dyer F. C. and Seeley T. D. (1987) Interspecific comparisons of endothermy in honey-bees (Apis): deviations from the expected size-related patterns. J. exp. Biol. 127, 1-26. Ellington C. P. (1984) The aerodynamics of hovering insect flight. II. Morphological parameters. Phil. Trans. R. Soc. Lend. B 305, 17-40. Heinrich B. (1971) Temperature regulation of the sphinx moth, Manduca sexta. II. Regulation of heat loss by control of blood circulation. J. exp. Biol. 54, 153-166. Heinrich B. (1976) Heat exchange in relation to blood flow between thorax and abdomen in bumblebees. J. exp. BioL 64, 561-585. Heinrich B. (1981a) Insect Thermoregulation, p. 304. Wiley, New York. Heinrich B. (1981b) Ecological and evolutionary perspectives. In Insect Thermoregulation (Edited by Heinrich B.), pp. 235-302. Wiley, New York. Heinrich B. and Bartholomew G. A. (1979) Roles of endothermy and size in inter- and intraspecific competition for elephant dung in African dung beetles, Scarabaeus laevistriatus. Physiol. Zool 52, 484--496. Heinrich B. and Casey T. M. (1978) Heat transfer in dragonflies: 'fliers' and 'perchers'. J. exp. Biol. 74, 17-36. Heinrich B. and McClain E. (1986) "Laziness" and hypothermia as a foraging strategy in flower scarabs (Coleoptera: Scarabaeidae). Physiol. Zool. 59, 273-282. Joos B. A., Young P. A. and Casey T. M. (1991) Wingstroke frequency of foraging and hovering bumblebees in relation to morphology and temperature. Physiol. Ent. 16, 191-200. Josephson R. K. (1981) Temperature and the mechanical performance of insect muscle. In Insect Thermoregulation (Edited by Heinrich B.), pp. 19~4. Wiley, New York, Kammer A. E. (1981) Physiological mechanisms of thermoregulation. In Insect Thermoregulation (Edited by Heinrich B.), pp. 115-158. Wiley, New York.
33
Krogh A. and Zeuthen E. (1941) The mechanism of flight preparation in some insects. J. exp. Biol. 18, 1-9. Lighthill J. (1977) Introduction to the scaling of aerial locomotion. In Scale Effects in Animal Locomotion (Edited by Pedley T. J.), pp. 365-404. Academic Press, London. May M. L. (1976) Thermoregulation and adaptation to temperature in dragonflies (Odonata: Anisoptera). Ecol. Monogr. 46, 1-32. May M. L. (1979) Insect thermoregulation. A. Rev. Ent. 24, 313-349. May M. L. (1981) Wingstroke frequency of dragonflies (Odonata: Anisoptera) in relation of temperature and body size. J. comp. Physiol. B. 144, 229-240. Morgan K. R. (1987) Temperature regulation, energy metabolism and mate searching in rain beetles (Pleocoma spp), winter-active, endothermic scarabs (Coleoptera). J. exp. Biol. 128, 107-122. Morgan K. R. and Shelley T. E. (1988) Body temperature regulation in desert robber flies (Diptera: Asilidae). Ecol. Ent. 14, 419-428. Nicolson S. W. and Louw G. N. (1980) Preflight thermogenesis, conductance and thermoregulation in the protea beetle, Trichostetha fascicularis (Scarabaeidae: Cetoniinae). S. Afr. J. Sci. 76, 124-126. Oertli J. J. (1989) Relationship of wing beat frequency and temperature during take-off flight in temperate-zone beetles. J. exp. Biol. 145, 321-338. Rautenbach I. L., Kemp A. C. and Scholtz C. H. (1988) Fluctuations in availability of arthropods correlated with microchiropteran and avian predator activities. Koedoe 31, 77-90. Roughgarden J. (1989) The structure and assembly of communities. In Perspectives in Ecological Theory (Edited by Roughgarden J., May R. M. and Levin S. A.), pp. 203-226. Princeton University Press, Princeton, N.J. Scholtz C. H. (1988) Biology of Sparrmannia tiara Arrow (Coleoptera: Scarabaeidae: Melolonthinae). Coleopts Bull. 42, 57~12. Stone G. N. and Willmer P. G. (1989a) Warm-up rates and body temperatures in bees: the importance of body size, thermal regime and phylogeny. J. exp. Biol. 147, 303-328. Stone G. N. and Willmer P. G, (1989b) Endothermy and temperature regulation in bees: a critique of 'grab and stab' measurement of body temperature. J. exp. Biol. 143, 211-223. Underwood B. A. (1991) Thermoregulation and energetic decision-making by the honeybees Apis cerana, Apis dorsata and Apis laboriosa. J. exp. Biol. 157, 19-34. Unwin D. M. and Corbert S. A. (1984) Wingbeat frequency, temperature and body size in bees and flies. Physiol. Ent. 9, 115-121. Willmer P. G. (1982) Thermoregulatory mechanisms in Sarcophaga. Oecologia 53, 382-385.