Thermoregulation in the cicada Platypedia putnami variety
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Journal of Thermal Biology 27 (2002) 365–369
Thermoregulation in the cicada Platypedia putnami variety
lutea (Homoptera: Tibicinidae) with a test of a
crepitation hypothesis
Allen F. Sanborna,*, Fernando G. Noriegab, Polly K. Phillipsc
a
School of Natural & Health Sciences, Barry University, 11300 NE Second Avenue, Miami Shores, FL 33161-6695, USA
b
Department of Biochemistry, University of Arizona, Biological Science West 513, Tucson, AZ 85721, USA
c
American University of the Caribbean, C/o MEIO, 901 Ponce de Leon Boulevard, Suite 401, Coral Gables, FL 33134, USA
Received 15 October 2001; accepted 4 January 2002
Abstract
1. Measurements of body temperature (Tb ) in the field demonstrate that Platypedia putnami var. lutea Davis regulates
Tb through behavioral mechanisms.
2. Thermal responses (minimum flight temperature 17.31C, maximum voluntary tolerance-temperature 32.51C, and
heat torpor temperature 44.41C) of P. putnami var. lutea are related to the altitude of their habitat.
3. Water loss rates increase with ambient temperature (Ta ). Water loss rates are not significantly different at the
extremes of the active Tb range but increase significantly when exposed to elevated Ta :
4. Acoustic activity was restricted at 6.71C Tb range. This is similar to the lower end of the Tb range for singing
measured in cicada species that produce sound with a timbal mechanism.
5. The use of the wing musculature to produce acoustic signals in P. putnami var. lutea does not increase the Tb range
over which the species can call compared to timbal calls produced by other cicada species. r 2002 Elsevier Science
Ltd. All rights reserved.
Keywords: Thermoregulation; Behavior; Platypedia putnami; Insect
1. Introduction include endothermy (Sanborn et al., 1995a, b; Sanborn,
2000), evaporative cooling (Kaser and Hastings, 1981;
The body temperature (Tb ) of cicadas must remain Hadley et al., 1991; Hastings and Toolson, 1991;
within a specific range in order to coordinate reproduc- Sanborn et al., 1992), and thermal adaptation (Heath,
tive activity (Heath, 1967, 1972). Thermoregulation in 1967; Heath et al., 1971, 1972; Heath and Wilkin, 1970;
cicadas is often accomplished through behavioral Heath, 1972; Sanborn et al., 1992, 1995a, b; Sanborn
mechanisms (Heath, 1967; Heath and Wilkin, 1970; and Phillips, 1996; Sanborn, 2000; Sanborn and Mat!e,
Heath et al., 1972; Heath, 1972; Hastings, 1989; 2000).
Hastings and Toolson, 1991; Sanborn et al., 1992, Most cicadas produce mating calls with a timbal
1995a, b; Sanborn, 2000; Sanborn and Mate! , 2000). mechanism. An alternative form of sound production is
Physiological mechanisms to regulate Tb in cicadas crepitation (Moore, 1966, 1973, 1993; Sanborn and
Phillips, 1999). Crepitating cicadas will snap their wings
*Corresponding author. Tel.: +1-305-899-3219; fax: +1- together, either against their body or against a substrate,
305-899-3225. to produce sound. It has been hypothesized that
E-mail address: asanborn@mail.barry.edu (A.F. Sanborn). crepitation may permit calling activity over a greater
0306-4565/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved.
PII: S 0 3 0 6 - 4 5 6 5 ( 0 2 ) 0 0 0 0 4 - 9366 A.F. Sanborn et al. / Journal of Thermal Biology 27 (2002) 365–369
Tb range than cicadas that use a timbal mechanism to 351C, and 401C. Six males were tested at each water-
produce their mating call (Sanborn and Phillips, 1999). bath temperature.
We investigate thermoregulation in Platypedia putnami Water loss rates were determined by measuring the
var. lutea Davis and test that hypothesis with this work. mass loss of the individuals within the canisters over
time. Specimens were removed from their respective
canisters every 30 min and weighed on a Sartorius
2. Materials and methods electronic scale sensitive to 70.00001 g. All mass loss
was assumed to be water loss.
A population of P. putnami var. lutea was sampled Cooling curves were determined by placing a thermo-
during June 1995 and May and June 2001 at Geology couple wire into the dorsal thorax of a freshly killed
View (32122.250 N, 110142.670 W), Mt. Lemmon, Pima cicada. The cicada was warmed with a heat lamp, then
County, Arizona, at an altitude of 1,981 m. Animals suspended in a Styrofoam box which acted as a
captured for laboratory experimentation were placed on controlled radiant environment. Tb was measured with
ice in a cardboard container with a plant sample and the Physitemp BAT-12 thermometer every 15 s for
moist paper towel until the experiments could be 15 min. Cooling curves were analyzed using the proce-
performed during the afternoon or evening of the day dure of Heath and Adams (1969).
of capture. The specimens used for the water-loss studies All statistics are reported as mean7standard deviation.
were collected in the early morning just as the
population became active and brought immediately to
the laboratory to minimize any effect passive dehydra- 3. Results
tion of the specimens would have on the results.
Tb was measured with a Physitemp BAT-12 digital P. putnami var. lutea is a small cicada (303747 mg
thermocouple thermometer with a type MT-29/1 cop- [n ¼ 35] [Sanborn and Phillips, 1999]) that forms
per-constantan 29 gauge hypodermic microprobe accu- aggregations in pointleaf manzanita (Arctostaphylos
rate to 70.11C, which had been calibrated with a pungens) and silverleaf oak (Quercus hypoleucoides).
National Institutes of Standards and Technology They are a classic example of a behavioral thermo-
mercury thermometer. The probe was inserted midway regulator. In the morning or when Ta or Tb was low, the
into the dorsal mesothorax to record deep Tb : Field cicadas migrated to the outer edges of the eastern side of
temperatures were measured after the cicadas were the host plants. Cicadas would even leave the small
collected by hand after the behavior and position of branches (their usual perch) and sit on leaves where it
the cicadas was determined. The animals were immedi- was possible to maximize the uptake of solar radiation.
ately oriented and held by the wing tips in an effort to As Ta and Tb increased, the cicadas would move deeper
decrease heat transfer between the experimenter and the into the shaded portion of the host plants. In the evening
specimen. Tb was stable during measurement for >15 s as Ta and Tb became more difficult to maintain within
while a cicada was being held so that any heat transfer the shaded portions of the plants, the cicadas migrated
during capture should have been minimal. Thermal to the exposed western edges of the plants. In the
responses were determined in the laboratory following evening, active cicadas were found only on the exposed,
the procedures of Heath (1967) and Heath and Wilkin sunny perches of the western side of the host plants.
(1970). All measurements were recorded within 5 s of the Tb ’s were recorded over a Ta range of 18.2–30.21C
animal being captured in the field or performing the (n ¼ 167) and a Tp range of 19.6–32.01C (n ¼ 167).
desired activity in the laboratory. Perch temperature Mean Tb of cicadas was 33.171.491C (n ¼ 167) with a
(Tp ) was measured immediately after Tb was recorded range of 26.7–35.91C. Tb shows a significant relationship
by placing the tip of the thermocouple above the perch as a function of either Ta (ANOVA F ¼ 11:736; df ¼ 1;
where the animal was captured at the approximate 165, Po0:001) (Fig. 1) or Tp (ANOVA F ¼ 24:700;
height of the middle of the thorax (5 mm). Ambient df ¼ 1; 165; Po0:001) (Fig. 2). The slope of the regres-
temperature (Ta ) was measured at a height of about 1 m sion line of Tb as a function of Ta or Tp is significantly
in the shade after Tp was recorded. different than the one (for Tb vs. Ta ; t ¼ 24:39; df ¼
Evaporative water loss was determined using a 165; P50:0001; for Tb vs. Tp ; t ¼ 22:11; df ¼ 165;
modification of techniques described by Edney (1971) P50:0001) suggesting thermoregulation (May, 1985).
and Sanborn et al. (1992). Individual specimens were The thermal responses determined in the laboratory
placed in plastic film canisters above 5 g of calcium were as follows: minimum flight tempera-
sulfate (Drierite) to produce an approximate 0% tureF17.371.601C (n ¼ 31), maximum voluntary tol-
humidity environment. The specimens were separated erance temperatureF32.572.241C (n ¼ 26), and heat
from the calcium sulfate by a screen. The canisters were torporF44.471.641C (n ¼ 31). Two animals were
placed in water baths that maintained water temperature observed moving from sun to shade in the field. Their
within 70.11C. Animals were tested at 20.51C, 29.61C, Tb ’s were 35.01C and 35.11C similar to upper maximumA.F. Sanborn et al. / Journal of Thermal Biology 27 (2002) 365–369 367
40 y = 30.174 + 0.122x r = 0.258 25
35 20
Body Temperature ( C)
o
30 15
Number
25 10
Tb = Ta
20
5
15
15 20 25 30 35 40 0
. . . . . . .
29 30 31 32 33 34 35 36
Ambient Temperature ( oC) o
Crepitating Body Temperature ( C)
Fig. 1. Tb as a function of Ta in P. putnami var. lutea. The slope
of the regression is significantly different from the one Fig. 3. Distribution of crepitating P. putnami var. lutea Tb ’s.
suggesting thermoregulation. The mean Tb for the population of P. putnami var. lutea is
33.11C. The mean maximum voluntary tolerance temperature is
32.51C.
40 y = 28.373 + 0.182x r = 0.361
35 at 29.61C (Po0:05) and the rate of water loss at 39.91C
Body Temperature (o C)
is significantly greater than at 35.01C (Po0:05) since the
CIE. ranges do not overlap the slope of the comparative
30
regression (Sokal and Rohlf, 1995).
Freshly killed P. putnami var. lutea passively cool at a
25 rate of 0.40770.03241C min11C gradient1 (n ¼ 4).
Crepitating cicadas had a Tb of 33.071.341C
(n ¼ 50). This value is not significantly different from
T =T
20 b a the mean Tb value determined for the population
(t ¼ 0:4257; df ¼ 215; P ¼ 0:6646) or from the max-
imum voluntary tolerance temperature determined in
15
15 20 25 30 35 40 the laboratory (t ¼ 1:213; df ¼ 74; P ¼ 0:8855). The
o range of Tb ’s in crepitating cicadas was 29.2–35.91C.
Perch Temperature ( C) The distribution of crepitation Tb ’s is shown in Fig. 3.
Fig. 2. Tb as a function of Tp in P. putnami var. lutea. The
slope of the regression is significantly different from the one
suggesting thermoregulation. 4. Discussion
P. putnami var. lutea follows the basic thermoregula-
voluntary tolerance temperatures determined in the tory pattern in cicadasFbehavioral heliothermy. They
laboratory. will alter their exposure to the sun through gross body
Water loss rates increased with increasing Ta : movements in one location or through movements from
Average mass loss was 1.27% h1 at 20.61C (95% CIE the edge of their host plants to deep shade within the
1.046–1.489% h1), 3.28% h1 at 29.61C (95% CIE host plant and back again. They have been shown to use
2.817–3.746% h1), 3.77% h1 at 35.01C (95% microclimates effectively in maintaining Tb at a range
CIE 3.185–4.365% h1), and 6.05% h1 at 39.91C suitable to maintain activity. This mechanism of
(95% CIE 5.646–6.454% h1). The water loss rates at thermoregulation has been shown to be common in
the extremes of the Tb range for activity (29.61C and cicadas (see summary in Sanborn, 1998, 2000; Sanborn
35.01C) do not differ significantly (P > 0:05) since the and Mat!e, 2000).
CIE. values overlap the slope of the other regression. The thermal responses of P. putnami var. lutea are
The rate of water loss at 20.61C is significantly less than related to the habitat in which the species lives. The368 A.F. Sanborn et al. / Journal of Thermal Biology 27 (2002) 365–369
minimum flight temperature is similar to species that the maximum voluntary tolerance temperature. The
inhabit cooler environments such as Okanagana hesperia maximum voluntary tolerance temperature is an upper
(Uhler) (Heath, 1972) and Magicicada cassinii (Fisher) thermoregulatory set-point (Heath, 1970) and many
(Heath, 1967) although minimum flight temperature is cicadas sing at Tb ’s below the maximum voluntary
difficult to relate strictly to habitat (Sanborn, 1998). The tolerance temperature (Heath, 1967; Heath and Wilkin,
maximum voluntary tolerance temperature and heat 1970; Heath et al., 1972; Sanborn et al., 1992, 1995a, b;
torpor temperature are similar to species that inhabit Sanborn and Mat!e, 2000; Sanborn, 2000, but see for
cooler environments such as O. hesperia (Heath, 1972) exceptions).
and M. cassinii (Heath, 1967). The maximum voluntary P. putnami var. lutea exhibited acoustic behavior over
tolerance and heat torpor temperature are less than the a Tb 6.71C range. The Tb range for crepitating is similar
values reported for other desert species (Heath et al., to the Tb range reported for singing in the ectothermic
1972; Sanborn and Phillips, 1996). The values for all the cicadas O. hesperia (2.81C, Heath, 1972), C. valvata
thermal tolerances in P. putnami var. lutea are less than (9.51C, Heath et al., 1972), M. cassinii (6.81C, Heath,
the values reported for Cacama valvata (Uhler) (Heath 1967), O. gracilis (4.91C, Sanborn et al., 1992),
et al., 1972) and Okanagodes gracilis Davis (Sanborn Diceroprocta apache (Davis) (4.81C, Heath and Wilkin,
et al., 1992) both of which are found at lower altitudes 1970), Diceroprocta olympusa (Walker) (5.81C, Sanborn
around Mt. Lemmon. The thermal responses of P. and Mat!e, 2000) and Tibicen chloromerus (Walker)
putnami var. lutea illustrate adaptation to an altitudin- (8.11C, Sanborn, 2000). The range for acoustic activity
ally based cooler habitat. in P. putnami var. lutea is less than the total range of
The rate of water loss increases in P. putnami var. acoustic activity in the endothermic cicadas Guyalna
lutea as Ta increases. The rate of water loss is bonaerensis (Berg) (11.21C, Sanborn et al., 1995b),
approximately constant over the active range of Tb : It Proarna bergi (Distant) (3.61C, Sanborn et al., 1995a),
appears that P. putnami var. lutea can evaporatively cool P. insignis Distant (3.61C, Sanborn et al., 1995a) and
at higher Ta s but the ability to cool evaporatively Tibicen winnemanna (Davis) (13.21C, Sanborn, 1997,
appears to be limited. In contrast to most desert cicadas 2000). Therefore, these data do not support the
(Kaser and Hastings, 1981; Hastings, 1989; Hastings hypothesis that crepitation can permit acoustic activity
and Toolson, 1991; Hadley et al., 1991; Sanborn et al., over a greater Tb range than a timbal system. It appears
1992), P. putnami var. lutea actually loses a lower that the acoustic activity for reproduction is restricted
percentage of body mass per hour than does Magicicada by temperature in cicadas regardless of the type of sound
tredecim (Walsh and Riley), a species from a warm, generating system employed.
humid environment (Toolson and Toolson, 1991). The
pattern of water loss with increasing temperature
contrasts with the results of a similar experiment on O.
gracilis where water loss rates decreased with increasing Acknowledgements
Ta until after the thermoregulatory point was reached
when the species began to cool evaporatively (Sanborn Jeremy Montague provided valuable assistance with
et al., 1992). the statistical analysis. AFS was supported by NIH-
The rate at which P. putnami var. lutea passively cool MBRSRISE, Barry University (GM59244-01A1) and
is similar to other small cicadas (Sanborn et al., 1992). Sr. John Karen Frei of Barry University.
The cooling rate is related predictably to the size of the
species (Heath and Wilkin, 1970; Heath et al., 1972;
Sanborn et al., 1995a, b; Sanborn, 2000).
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