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Zeitschrift/Journal: Denisia

Jahr/: 2002

Band/Volume: 0004

Autor(en)/Author(s): Sanborn Allen F.

Artikel/Article: Thermoregulation (, Cicadoidea) 455-470 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Cicada Thermoregulation (Hemiptera, Cicadoidea)

A.F. SANBORN

Abstract

A review the mechanisms and ther- moregulatory strategies used by is presented. The behavioral and physiologi- cal processes used to regulate body tempe- rature are discussed. Behavioral strategies include changes in body orientation to the sun, basking, shade-seeking, microclimate selection, vertical migration, using the wings as a parasol, and suspension of activity. The effect of temperature on the biology of cicadas and the strategies used to deal with temperature are discussed. Physiological responses include thermal adaptation, endothermy, and evaporative cooling.

Key words: temperature regulation, endothermy, evaporative cooling, thermal responses.

Denisia 04, zugleich Kataloge des OÖ. Landesmuseums, Neue Folge Nr. 176 (2002), 455-470

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Temperature is a physical parameter of the Temperature has been shown to affect environmental that affects all organisms at the cicadas at all levels, from controlling the rate cellular level through the temperature depen- of neural firing (WAKABAYASHI & HAGIWARA dent nature of chemical reactions. The daily 1953, WAKABAYASHI & IKEDA 1961) or the contraction kinetics of muscles (AlDLEY &. fluctuations in ambient temperature (Ta) can have a significant influence on the activity of WHITE 1969, JOSEPHSON 1981, JOSEPHSON & any terrestrial . have two opti- YOUNG 1979, JOSEPHSON & YOUNG 1985, SANBORN in press) to determining the rate of ons with respect to body temperature (Tu,) development (AZUMA 1976, HARTZELL 1954, and the changing thermal environment: they NAGAMINE and TERUYA 1976), when a popu- lation emerges (HEATH 1968) or even the dis- tribution of the (OHGUSHI 1954, SCHEPL 1986, TOOLSON 1998). Therefore, temperature and the regulation of body tem- perature (Tu,) are as essential in the lives of cicadas as in any other terrestrial animal. Previous studies (HEATH 1967, HEATH 1972, SANBORN et al. 1995a, SANBORN et al. 1995b, SANBORN 1997, SANBORN 2000, SAN- RORN &. MATE 2000) have shown that cicadas must maintain their Tu, within a small range to coordinate reproductive activity, the main purpose of the adult life stage. The daily varia-

tions of Ta are large enough to prevent the passive development of a constant Tu,, but it is not always practical for an organism to delay activity until ambient conditions are favorable while spending the remainder of the day in a thermal shelter. Cicadas, therefore, spend time and energy thermoregulating to permit activity for a significant portion of the day. The strategies used by animals to regulate Tu, can be divided into two major types of res- ponses: behavioral and physiological. A com- mon method of thermoregulation in cicadas is to use behavioral mechanisms to alter the uptake of solar radiation (Heath 1967, HEATH & WILKIN 1970, HEATH et al. 1972, HEATH Figs. 1: can be thermoconformers or thermoregula- 1972, HASTINGS 1989, HASTINGS & TOOLSON Basking Tympanoterpes elegans BERG. tors. A thermoconformer is an animal whose 1991, TOOLSON 1998, SANBORN 2000, Cicadas will bask at low body and/or ambient temperature to elevate body Tu, changes with and is approximately equal to SANBORN & MATE 2000) (Fig. 1). This type of temperature to a range necessary to Ta. Any animal that is a thermoconformer is organism is termed ectothermic because it uses coordinate activity. Cicadas maximize unable to function efficiently physiologically exogenous heat to regulate Tu,. However, the- radiant energy uptake by orienting the greatest body surface area to the over a wide temperature range because enzym- re have been studies (SANBORN et al. 1995a, sun. The dorsal surface is perpendicu- es function most efficiently over a restricted SANBORN et al. 1995b, SANBORN 1997, SAN- lar to the sun in this photograph. temperature range. The alternative strategy BORN 2000) showing cicadas using the physio- that reduces the negative aspect of fluctuating logical mechanisms of endothermy (the gene- Tu, is thermoregulation. An animal that ther- ration of endogenous heat for thermoregulati- moregulates maintains Tu, within a "preferred" on) and evaporative cooling (KASER & temperature range so its are functio- HASTINGS 1981, TOOLSON 1984, TOOLSON ning near optimal levels while the animal is 1985, TOOLSON 1987, TOOLSON & HADLEY active. 1987, HADLEY et al. 1989, HASTINGS 1989,

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STANLEY-SAMUELSON et al. 1990, HADLEY et Similar patterns of movement and exposu- al. 1991, HASTINGS & TOOLSON 1991, re to solar radiation occur in endothermic spe- SANBORN et al. 1992, TOOLSON 1993, TOOLSON cies. Endothermic species use radiant heat et al. 1994) in the field to regulate T^. when it is available to assist in the elevation of Tjj. This behavioral strategy saves the animals Behavioral Responses metabolic energy that can then be used for activity at a time when solar radiation is not All animals use behavioral thermoregula- available (SANBORN et al. 1995a, SANBORN et tion as a first option to regulate T^. Behavi- al. 1995b, SANBORN 2000). This behavior may oral thermoregulation is the quickest and most also potentially increase the life span of the accessible mode of regulation since the effect individual adult since the adults do not recei- is immediate and behavioral temperature ve significant amounts of energy from the regulation does not require changes in cellular fluid on which they feed (CHEUNG & composition or activity to be effective. There- MARSHALL 1973a). fore, it is not surprising that the majority of We had the opportunity to see importance cicadas regulate T^ through behavioral of basking as a means to elevate T(j to a level mechanisms (HEATH 1967, HEATH &. WlLKlN necessary for activity during a partial (about 1970, HEATH et al. 1972, HEATH 1972, 70%) solar eclipse in 1991 (SANBORN & PHIL- HASTINGS 1989, HASTING & TOOLSON 1991, LIPS 1992). Ta decreased by approximately SANBORN et al. 1992, SANBORN et al. 1995a, 1°C during the eclipse but remained at a level SANBORN et al. 1995b, SANBORN 1997, where activity had been recorded previously TOOLSON 1998, SANBORN 2000, SANBORN & in the species active in the habitat (SANBORN MATE 2000). et al. 1992). The cicadas were forced to sus- As stated previously, the majority of cica- pend activity due to a loss of radiant input, das use solar radiation as a mechanism to ele- which is required to maintain an elevated T(j. vate Tjj. Cicadas move from their nocturnal A similar effect has also been reported several feeding locations to where their expo- times with decreased radiation due to cloud sure to the sun will be maximal early in the cover (see references in SANBORN & PHILLIPS morning. Cicadas bask in to keep T^ 199). elevated to a range necessary for activity. A common mechanism used by ectother- Cicadas have been shown to congregate in mic animals to decrease T^ is to decrease the areas where exposure to the sun is greatest radiant heat load. A simple behavior animals (HUDSON 1890, RAMSAY 1959, HEATH 1967, can employ to decrease radiant heat gain is to HEATH & WILKIN 1970, HEATH et al. 1972, move into a shaded location. This strategy is

HEATH 1972, FLEMING 1975, YOUNG 1975, widely used by cicadas exposed to elevated Ta YOUNG 1980, YOUNG 1981, JOERMANN & and radiant energy from the sun to regulate TJL, SCHNEIDER 1987, HASTINGS 1989, HASTINGS (HEATH 1967, HEATH & WILKIN 1970, HEATH & TOOLSON 1991, SANBORN et al. 1992, et al. 1972, HASTINGS, 1989, HASTINGS & TOOLSON 1998, SANBORN 2000, SANBORN & TOOLSON 1991, SANBORN et al. 1992, SAN- MATE 2000). The concentration of animals BORN et al. 1995a, TOOLSON 1998, SANBORN moves within the habitat to stay exposed to 2000, SANBORN & MATE 2000). Cicadas also the sun as the sun moves through the day change the location of activity from the exter- (HEATH 1967, SANBORN et al. 1995a, DURIN nal regions of plants to inner shaded locations

1981). These generalization are true of both as Ta or T^ increase. This is an especially ectothermic (HEATH 1967, HEATH & WlLKlN important strategy in active animals whose 1970, HEATH et al. 1972, HEATH 1972, metabolism would further increase T^. HASTINGS 1989, HASTINGS & TOOLSON 1991, Shade-seeking behavior has been measu- SANBORN et al. 1992, TOOLSON 1998, red directly in the field. HEATH (1967) measu- SANBORN 2000, SANBORN & MATE 2000) and red the Tjj when animals voluntarily moved to endothermic species (SANBORN et al. 1995a, the shade. He demonstrated cicadas moved SANBORN et al. 1995b, SANBORN 2000). from sun to shade over a very narrow range of

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Tj, (1.5-2.O°C). In addition, the T^ range of changes of Tj, in valvata (UHLER) the laboratory shade-seeking response corre- (HEATH et al. 1972). sponded to the maximum T^,s measured in the Changing the orientation of the body can field suggesting a finely tuned response is con- also alter radiant heat uptake if the animal has trolling behavioral changes that regulate T^ differences in the reflective pattern ot diffe- (HEATH 1967). rent parts of the body. Animals such as Caca- Animals can also regulate the amount of ma valvata (HEATH et al. 1972) and Okanagu- radiant heating by changing the orientation o( des graci/is DAMS (SANBORN et al. 1992) have their body to the sun. This will change the a morphological adaptation that assists in decreasing radiant input at elevated Tj,. The ventral surface of these, and many other desert inhabiting species, is white in color (Fig. 3). The difference in coloration between the dor- sal and ventral surfaces facilitates reducing the radiant heat gain when the animals become negatively oriented to the sun as the white ventral surface reflects a greater portion of the radiant heat. Animals from less thermal rigo- mus habitats do not have this type of reflec- tive ventral surface (HEATH 1967, HEATH 1972). The periodical cicada Ma^dcada cassinii (FlSHER) has been shown to adopt an unusual posture at low T., and when the sun is low on the horizon (HEATH 1967). The wings are spread away from the midline exposing a grea- ter area of the black thorax and abdomen to solar radiation. By the late morning, the wings have returned to their usual position, peaked over the midline of the abdomen. This stra- tegy acts to increase the area of the body expo-

sed to radiant heating at low Ta, thus increa-

sing the heating rate. Similarly when T^, Ta or the sun angle is elevated the wings act as a parasol decreasing the radiant heat load and the temperature excess of the animal. There is also some evidence that cicadas use the wings as a shade in a different mannet. Active Magiacada cassinii orient their bodies with the head facing directly away from the Figs. 2: surface area of the body being exposed to the sun in the aftermxin. This behavior permits the wings to "shade" the body and decrease A specimen of Cacama valvata (UHLER) sun which will alter the heat transfer. As Tj, that has partially rotated around its heat uptake (HEATH 1967). . The radiant heat load decreases increases animals can decrease the total surfa- when the animal exposes the lateral ce area exposed to the sun through three main Selection of a specific microhabitat can be body surface to the sun permitting the used in addition to the gross body movements mechanisms: an animal can orient the side of cicada to maintain body temperature associated with shade-seeking behavior. This in the range necessary for activity. Fur- the body to the sun, rotate the body around a was best illustrated by the description of ther increases in body temperature branch (Fig. 2, 3), or face the head into the will stimulate movement into the movements in (DAVIS) sun (HEATH & WILKIN 1970, HEATH et al. shade. associated with Ta (HEATH & WlLKlN 1970). 1972, HEATH 1972, SANBORN et al. 1992, Diceroprocta apache is able to keep T^, below

SANBORN & MATE 2000). Changes in orienta- Ta, in part, by selecting an appropriate tion in the field have been correlated with microclimate.

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Similarly, microhabitat choice is reported Another strategy for dealing with extreme to be responsible for the difference in Tj, temperature is to suspend activity altogether.

recorded in two syntopic species (HASTINGS & Cicadas are torpid at low Tj, and low Ta TOOLSON 1991). Tibken chiricahua DAVIS is (HEATH 1967, HEATH & WILKIN 1970, HEATH reported to exhibit a higher T^ because it is et al. 1971, HEATH et al. 1972, HEATH 1972, active closer to the ground and in less shade. SANBORN et al. 1992, SANBORN 2000, In contrast, T. duryi DAVIS uses more elevated SANBORN & MATE 2000). This torpidity can perches in deeper shade and has an average T^ be a benefit to ectothermic animals in that 3.1°C lower than T. chiricahua. The differen- metabolic rate decreases as T^ decreases. The ces are not due to biophysical factors as T. duryi is the larger of the two species and should, therefore, equilibrate at a higher T^. These differences may be realted to distributi- on of T. chiricahua which would require adap-

tation to warmer Ta and the selection of ele- vated T^s for activity since it lives in warmer habitats (HASTINGS & TOOLSON 1991). Selection of a proper microhabitat is also important for one of the physiological respon- ses to temperature to be effective. The decrea- se in Tj, due to evaporative cooling disappears when the animals are placed in high humidity environments (TOOLSON 1985, TOOLSON 1987, HASTINGS 1989). Selection of an impro- per microhabitat could lead to an ineffective evaporative cooling response. Related to the selection of a particular microclimate is a vertical change in position

with changes in Ta. This is especially well

exemplified by the vertical migrations of only behaviors exhibited at low T^ or Ta are Figs. 3: Okanagodes pracilis (SANBORN et al. 1992). A cicada that has moved to a negative basking, in an effort to elevate Tjy and fee- orientation. This specimen of Dicero- When Ta is less than <40-42°C, O. gracilis is ding. procta eugraphica (DAVIS) has rotated active on low, scrubby plants (Atriplex spp.) on around its perch to decrease the radi- High Tas, combined with the metabolic which they are difficult to find due to cryptic heat load and maintain body tem- heat produced as a byproduct of normal activi- perature in the range necessary for coloration. However, when T., elevates to as ty, could lead to lethal increases in Tj,. When calling behavior. By moving to the much as 50°C during the heat of the day, underside of the perch, the cicada Tas are elevated, calling activity has been exposes a white ventral surface to the O. gtacilis will abandon the low plants for a reported to be inhibited or depressed in sever- sun and the perch en be used for sha- higher perch on plants like Larrea uridentata al species (SwiNTON 1908, TALHOUK 1959, de by the which decreases the (Fig. 4). These elevated perches place the ani- radiant heat gain from the sun. WARD 1967, HEATH & WILKIN 1970, HEATH mals in lower temperature microclimates by etal. 1972, YOUNG 1974, HAHLEY et al. 1991). elevating the animals above the boundary lay- The potential dangers of activity at elevated er. These vertical migrations also facilitate the T„ were described hv HEATH & WiLKIN efficiency of the evaporative cooling response (1970). They calculated that a Diceroprocta in O. gracilis (SANBORN et al. 1992). By apache that initiated flight at a T^ of 43°C decreasing the temperature gradient with a would lose motor control after 20 seconds due vertical migration, O. gracilis decreases the to the metabolic heat produced in flight. A amount of water that must be evaporated to loss of motor control at elevated T,.s would maintain Tj, at a safe level and permits the most likely result in death for these animals as evaporative response to occur for a greater surface temperatures in their habitat can reach time period. 70°C (HEATH & WILKIN 1970).

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Physiological Responses All cicadas bask at low T^s. The endo- thermic species augment solar heating with Although behavioral thermoregulation metabolic heat production. At dusk or when has several benefits, there are still limitations environmental conditions prevent the use of placed on reproductive activity due to the solar radiation, the endothermic cicadas use limits to changes in T^ through behavior. metabolic heat to become or to remain active. Physiological mechanisms assist behavioral Thus, the endothermic species do not rely on strategies in regulating T^ to a more precise metabolic heat alone to regulate T^. They will level, thus permitting activity over a wider use radiant solar energy to elevate T^ for

range of Tg. There are three main physiologi- activity when it is available (SANBORN et al. cal responses used by cicadas to survive the 1995a, SANBORN 2000). Restriction in the use thermal environment: endothermy, evaporati- of metabolic heat saves energy stores in the ve cooling and thermal responses. cicadas. The energetic expense of behavioral thermoregulation is the cost of transporting Endogenous heat production used specifi- the animal's mass from one location to ano- cally for thermoregulation constitutes the ther or the cost of maintaining a particular definition of endothermy (ANONYMOUS posture which represents a small fraction of 1987). Endogenous heat production with the the energy cost to maintain T^ using metabo- potential for thermoregulation was first shown lic heat (HEATH 1970). in the tropical cicada Fidicina mannifera (FABRICIUS) (BARTHOLOMEW & BARNHARDT The relationship between field temperatu- 1984). When BARTHOLOMEW & BARNHARDT res and the T^ when voluntary endogenous (1984) described endothermy in F. mannifera, heat production ceased in Proarna bergi they stated that the functional significance of (DISTANT) and P. insignis presents further evi- the endogenous heat was problematic. My col- dence that the cicadas are warming to a level leagues and I have begun to investigate endo- necessary for activity. Captive animals gene- thermy in cicadas in order to determine its rally cease warm-up behavior in the same T^ biological significance (SANBORN et al. 1995a, range of those animals active in the field. The SANBORN et al. 1995b, SANBORN 1997, data also illustrate that the animals possess the SANBORN 2000, SANBORN in press). metabolic machinery necessary to raise their T|j to a biologically significant range Diel T|j distribution of endothermic cica- (SANBORN et al. 1995a, SANBORN et al. 1995b, das is similar to that in ectothermic species in SANBORN 2000). Similarly, the mean T^ of that T^ is elevated above Tg during daylight endothermically active winnemanna hours. Endothermic cicadas differ, however, in does not differ significantly from the mean T^ that the T^ of cicadas "active" at dusk or during the day (SANBORN 2000) and the mean when solar energy is unavailable is approxima- peak T^ measured by BARTHOLOMEW & BARN- tely the same as the diurnal distribution of HARDT (1984) during warm-up behavior in T[jS. A distinction between "active" and Fidicina mannifera is similar to the upper ther- "inactive" individuals must be made because moregulatory temperature we determined for

the Tjj of "inactive" animals approximates Tg the species F. torresi BOULARD & MARTINELLI (SANBORN et al. 1995a, SANBORN 2000) as is (which was split out from F. mannifera) found in ectothermic species under these con- (SANBORN et al. 1995a). ditions (HEATH 1967, SANBORN 2000). T^s of Female endothermic cicadas raise Tj^ dur- Guyalna bonaerensis (BERG), gigas ing the chorusing activity of the males. Fema- (OLIVIER), Proarna insignis DISTANT, and le Guyalna bonaerensis with elevated T^s have Tibicen winnemanna (DAVIS) measured in the been observed ovipositing in the rain field show that these cicadas are endothermic. (SANBORN et al. 1995a). Female Tibicen win- Recorded Tj^s were respectively as much as nemanna captured during the species' evening 13.0°C, 12.0°C, 7.4°C, and 12.6°C greater activity period also had elevated Tus

than Ta when solar heating was unavailable to (SANBORN 2000). The females may be requi- the species (SANBORN et al. 1995a, SANBORN red to elevate Tjj for species recognition. et al. 1995b, SANBORN 2000). Female (VRIJER 1984) and

460 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at crickets (WALKER 1957, WALKER 1963, MOORE 1962, HAYASHI 1982, POPOV et al. DOHERTY 1985) have been shown to respond 1985, DUFFELS 1988). These species may well only to the calls produced by males at the be endothermic since the ectothermic dusk same Tu, as the female. Some evidence to sup- singer saundersii (JOSEPHSON &. port a similar temperature dependent recogni- YOUNG 1979) does not exhibit "sing and " tion system in Tibicen winnemanna is that Tu,s behavior (DOOLAN & MACNALLY 1981). of the females observed were within Fidicina mannifera (BARTHOLOMEW & 0.5°C of the males with which they were BARNHARDT 1984) and Tibicen winnemanna copulating (SANBORN 2000). (SANBORN 2000) are capable of endothermi- The heat for thermoregulation is produced cally warming without flight. Non-flapping by the thoracic musculature. The relatively warm-up in F. mannifera was accompanied by large percentage of body mass (35% in cicadas barely perceptible low frequency (1-2 s ) [BARTHOLOMEW & BARNHARDT 1984, wing movements and telescoping of the abdo- SANBORN et al. 1995b]), the high metabolic men at 15-36 cycles min . Non-flapping scope, and the inefficiency of flight all make warm-up was not observed in T. winnemanna the flight musculature an ideal tissue to gene- in the laboratory, but individuals were obser- rate heat for thermoregulation. The extremely ved to progress from a buzzing call to produ- high metabolic rate of insect flight muscles cing a full mating call without changing sin- makes them well suited for heat production ging perches in the field. Since the mean Tu, (BARTHOLOMEW & EPTING 1975). Guyana of a cicada producing the fast song is signifi- bonaerensis, Quesada gigas, Fidicina torresi cantly greater than one producing a buzz (SANBORN et al. 1995a) and Tibicen winne- (SANBORN 1997), the cicadas were capable of (SANBORN 2000) have been observed raising Tu, without flight. Species of Coleop- to use the heat produced in flight to raise Tu, tera, , Diptera, and endothermically. also have been shown to raise Tu, without wing movements (MAY 1976, BARTHOLOMEW Insect flight is a mechanically inefficient & HEINRICH 1978, HEINRICH 1981, CHAPPELL process. Flight is normally assumed to have an & MORGAN 1987). efficiency of 20% (WEIS-FOGH 1972, WEIS- FOGH 1976, CASEY 1981a), but studies of Proama bergi and P. insignis generate meta- several insect species demonstrate that flight bolic heat with shiver-like movements of the efficiency ranges from 3.3-27.5% (WEIS-FOGH wings (SANBORN et al. 1995b) (Fig. 5). The 1972, WEIS-FOGH 1976, CASEY 1981b, amplitude of the wing vibrations is found to ELLINGTON 1984, ELLINGTON 1985, CASEY et change with increasing Tu, in some moth spe- al. 1985). The efficiency of insect flight is thus cies (DORSETT 1962, Kammer 1981) but this much lower than the assumed value of 20% did not occur in these cicadas. The mecha- and as a class have a mean flight effi- nism producing the wing vibrations in the ciency between 10-15%. This means that a cicadas is probably similar to the near syn- significant amount of the energy used in flight chronous activation of wing elevator and (85-90%) is released as heat. depressor muscles described by KAMMER Behavior similar to that observed in the (1970) in the butterfly Danaus plexippus (L.) endothermic cicadas has been described in but this has yet to be shown with electrical many dusk singing cicadas and endothermy recordings in the cicadas. may be a wide spread phenomenon in the There have been diverse functions descri- superfamily Cicadoidea. It has been reported bed for endogenous heat production of insects that Tibicen auletes (GERMAR) and Tibicen reso- (HEINRICH 1993). It has been estimated that nans (WALKER) are active for a greater period an endothermic cicada would use more than of time than environmental conditions should five times as much energy during activity as an permit (ALEXANDER 1960). "Sing and fly" ectothermic animal (SANBORN et al. 1995a). behavior has been described in these and The use of metabolic heat to raise Tu, for many other species active at dusk (DAVIS activity will decrease the life span of animals 1894a, DAVIS 1894b, MATSUMURA 1898, that do not obtain large amounts of energy ANNANDALE 1900, KERSHAW 1903, DAVIS from their food. Since cicadas feed on xylem 1922, DISTANT 1906, ALEXANDER 1956, fluid (CHEUNG & MARSHALL 1973a, WHITE &

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STREHL 1978), the nutrients available for face, and the partial pressure gradient of water energy conversion are limited. This raises the between the evaporating surface and the sur- question as to why an animal would expend rounding air. The use of evaporative cooling energy stores to become active when it could by insects is a relatively rare occurrence due to use solar radiation during the day and save their relatively small body si:e. Their high sur- metabolic energy. face to volume ratio, and the limitations of Endothermic behavior in cicadas may ser- sufficient water reserves can quickly lead to osmoregulatory problems for insects that ve to increase reproductive fitness in several attempt to use evaporative cooling. PRANGE ways including: uncoupling of reproductive (1996) has provided a fairly recent review of evaporative cooling in insects as a group. The use of evaporative cooling in cicadas was first described by KASER and HASTINGS (1981) in Tibicen duryi. It has since been described in Cacama valvata (TOOLSON 1993), Diceroprocta apa- che (TOOLSON 1985, TOOLSON 1987, TOOLSON & HADLEY 1987, HADLEY et al. 1989, HADLEY et al. 1991), Okanagodes gracilis (SAN- RORN et al. 1992), T. chiricahua (HASTINGS & TOOLSON 1991), T. dealbatus (DAVIS) (TOOLSON 1984, STANLEY-SAMUELSON et al. 1990, TOOLSON et al. 1994), and further descriptions for T. duryi (TOOLSON 1984, HASTINGS 1989, HASTINGS & TOOLSON 1991). All species inhabit environments in which T]., could elevate to lethal levels. Significant evaporative coo- Figs. 4: behavior from possible physiological con- ling has only been described for species that Okanagodes gracilis DAVIS thermoregu- straints of the environment, avoidance of pos- inhabit hot, dry environments even though lating during the warmest portion of the day. Ambient temeprature was sible thermoregulatory problems of midday by they have different phylogenetic histories 48°C when the image was taken. The restricting activity to the cooler portions of (HEATH 1978). An evaporative cooling picture illustrates the combined use of the day, permitting the use of habitats unavai- mechanism was described in a species from a behavioral and physiological strate- warm, humid environment but it was found gies to thermoregulate. The animal is lable to strictly ectothermic animals, helping exhibiting a negative orientation species to avoid predators, optimizing broad- the species had limited evaporative capabili- which shades the body with the cast coverage and sound transmission, or to ties (TOOLSON & TOOLSON 1991). The ability branch and exposes a white ventral to decrease Tj, below T disappears when ani- surface to the sun to reflect more permit avoidance of acoustic interference a solar radiation and decrease heat load. through temporal separation of singing (SAN- mals are placed in a saturated environment The animal has also abandoned the RORN et al. 1995a, SANBORN et al. 1995b, (TCXUSON 1985, TOOLSON 1987, HASTINGS normal host plant for a higher perch 1989). It appears a significant selection pres- which places the animal in a cooler SANBORN 1997, SANBORN 2000). sure in the evolution of evaporative cooling is microclimate. The animal is feeding A second physiological mechanism to to get the water necessary for evapo- the environment inhabited by the species. rative cooling which depresses the regulate T^ is evaporative cooling. Evaporati- body temperature below ambient. on of water represents a potentially significant Cicadas will attempt to use behavioral These activities combine with elevated mechanism for the dissipation of excess heat mechanisms to decrease T^ before evaporati- thermal tolerances permit reproduc- on of water begins (HADLEY et al. 1991, tive activity at a time when other ani- from any organism. The amount of energy lost mals are seeking shelter from the is dependent upon the coefficient of evapora- SANBORN et al. 1992). However, Diceroprocta heat. tion, the surface area of the evaporating sur- apache can maintain Tj, 5°C below Ta

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(TOOLSON 1987) and Okanagodes gracilis can system (TOOLSON &. HAPLEY 1987, HAPLEY et maintain a 6.7°C gradient (SANBORN et al. al. 1989, HADLEY et al. 1991). Death or the 1992) once evaporation begins. Water Kiss injection of NaCN causes a rapid decrease in rates increase as much as 600% during the transcuticular water flux in Diceroprocta apa- evaporative response (TOOLSON & HAPLEY che. The system probably operates by the cou- 1987) with the amount of water loss increa- pling of an actively transported ion across the sing with increasing Ta (HAPLEY et al. 1991). cell membrane of the dermal glands or dermal The onset of evaporative cooling occurs at gland ducts which then causes water to move a thermoreglatory point that is similar to the by osmosis. The water can then evaporate maximum voluntary tole- rance temperature. Evapo- ration begins at a T^ ot 39.2°C in Dkeroprocta apa- che (HAPLEY et al. 1989) which is the same as the maximum voluntary tole- rance temperature determi- ned by HEATH & WILKIN (1970). Evaporative coo- ling in Okanagodes gracilis occurrs at a T^ slightly abo- ve the maximum voluntary' tolerance temperature but this may have been an arti- fact of the experimental procedure (SANBORN et al. 1992). Evaporative cooling begins at lower T^s when animals are well hydrated and have access to food (TOOLSON & HALUEY 1987, HAPLEY et al. 1991) and T^s elevate as water reserves decrease (HASTINGS 1989). Figs. 5: Endogenous heat production in Proarna insignis DISTANT. The images on the left depict an animal at rest with the wings held over the body. The images on the right Water is evaporated through pores in the were taken while the animal was generating heat to elevate body temperature. The cuticle (Fig. 6) (TOOLSON & HAPLEY 1987, wings flatten in the dorso-ventral plane and are vibrated in a shiver-like manner HADLEY et al. 1991, SANBORN et al. 1992). during heat production. The shivering stops when the animals have elevated their body temperature to the range necessary for activity. These pores are located on the thorax and abdomen in both Dkeroprocta apache and Oka- nagodes gracilis. The pore structure and distri- Figs. 6: The dorsal of bution is also similar in the two species. Magi- Okanagodes gracilis cicada tredecim (WALSH & RlLEY), a species DAVIS. The pores are used to evaporate from a higher humidity, lower Ta environ- water to cool the ani- ment, has a limited number of pores and a mal in extreme heat. limited ability to cool evaporatively (TOOL- The individual pores SON & TOOLSON 1991). The main site of eva- are about 7 mm in diameter. porative water loss is the abdomen in D. apa- che (HAPLEY et al. 1989) which would explain the lower abdominal temperatures also obser- ved in Tibken duryi (HASTINGS 1989). The evaporative cooling mechanism appears to be mediated by an active transport

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once it is outside the cuticle. There is a cycli- maintain Tj, less than Ta (KASER & HASTINGS

cal rate of water loss at higher Ta> which is 1981, HASTINGS 1989) and appears to alter similar to evaporative cooling mechanisms the T(j at which the evaporative response is described for mammals (HADLEY et al. 1989). initiated (HADLEY et al. 1991, SANBORN et al. Prostaglandins have been suggested to 1992, TOOLSON et al. 1994). Okanagodes graci- regulate the control of transcuticular water lis continually feeds during the day even while flux in cicadas (STANLEY-SAMUELSON et al. performing reproductive activities such as sin- 1990, TOOLSON et al. 1994). Blocking the syn- ging and ovipositing (SANBORN et al. 1992) to thesis of prostaglandins prevents the initiation maintain water balance (Fig. 4). Tibicen duryi of the sweating response in Tibicen dealbatus. also feeds during the day (KASER & HASTINGS The results of these experiments suggest a 1981, HASTINGS 1989) but this species sus- complex interaction of chemicals in the pends other activities while it is feeding 20 carbon, polyunsaturated fatty acids and (HASTINGS 1989). arachidonic acid synthesis pathway that regu- A final physiological mechanism cicadas late the sweating response by regulating the employ is adaptation to particular thermal set point for initiation (TOOLSON et al. 1994). environments. An analysis of the thermal res- It appears cicadas that use evaporative ponses for a particular insect can give insights cooling are adapted to survive the loss of a lar- into how the animal is adapted thermally to ge percentage of their total body water during its environment. Early work (HEATH et al. the evaporative cooling response. Mean water 1971, HEATH et al. 1972) suggested the ther- loss rates of 141% h in Diceroprocta apache mal responses of a particular species were rela- (HADLEY et al. 1991), 10.67% h'1 in Tibicen ted to the habitat type and the elevation of duryi, 11.01% h'l in T. chiricahua (HASTINGS the habitat. This relationship has proven to be & TOOLSON 1991), and 9.73% h'1 in Okana- an over simplification as the number of species godes gracilis (SANBORN et al. 1992) with a investigated has increased and endothermy maximum rate of 30-35% h'' in Diceroprocta was discovered. Our further analyses have sug- apache (TOOLSON 1987) have been reported. gested that the thermal responses of cicadas are related to the activity patterns, thermore- Insects in general simply do not have suf- gulatory strategies, and habitat of a particular ficient body water reserves to employ evapora- species. tion as a main mechanism of thermoregulati- on. However, cicadas are an exception in that Three measurements are required to deter- they have access to a water source that other mine the thermal responses of a species organisms in their environment do not. Cica- (HEATH 1967, HEATH & WILKIN 1970, HEATH das feed on xylem fluid (CHEUNG & MARS- et al. 1971, HEATH et al. 1972, HEATH 1972, HALL 1973a) which is mostly water. In fact, SANBORN et al. 1992, SANBORN et al. 1995a, the digestive system of cicadas is modified to SANBORN et al. 1995b, SANBORN & PHILLIPS eliminate the excess water load they get with 1996, SANBORN 1997, SANBORN 2000, SAN- their food (CHEUNG & MARSHALL 1973b, BORN & MATE 2000, SANBORN &. PHILLIPS MARSHALL & CHEUNG 1973, MARSHALL & 2001). The minimum flight temperature CHEUNG 1974, MARSHALL & CHEUNG 1975, (MFT) represents the lowest T^ at which an MARSHALL 1983). Thus, the use of a specific animal is considered fully coordinated. The food source in a dry environment has permit- maximum voluntary tolerance (MVT) or sha- ted certain cicadas to use evaporative cooling de-seeking temperature is a measure of an as a means to regulate T^. This has allowed upper thermoregulatory set point (HEATH the cicadas to remain active in a thermally 1970). The heat torpor temperature (HTT) is stressed environment at times when other ani- the upper T^ limit of coordinated activity and mals, especially their predators, have retreated can represent an ecologically lethal T^ since to thermal shelters due to the excessive heat the animal is unable to prevent further increa- of the environment. ses in T)j. The T^ range of full activity is the Water uptake in evaporatively cooling difference between the MFT and HTT. cicadas has become an integral daily activity. Table 1 is a summary of the reported cicada Access to water is required for the cicadas to temperature responses.

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The MFTs are the most difficult thermal MVT when it is endothermically active. On response to analyze. There is no clear correla- the other extreme are Diceroprocta apache tion between habitat type and MFT. For (HEATH & WILKIN 1970) and Okanagodes gra- example, the desert inhabiting Diceroprocta cilis (SANBORN et al. 1992). These species cinctifera (UHLER) has the second lowest repor- inhabit the Sonoran Desert where Ta can ted MFT (SANBORN &. PHILLIPS 1996). Simi- approach or exceed 50°C. The animals must larly, OUanagana hesperia (UHLER) lives at alti- have elevated thermal tolerances to be active tude (HEATH 1972) but has a higher MFT for a significant portion of the day in their than desert dwelling species (HEATH & WlL- environment. In addition, the elevated MVT

Species Minimum Flight Maximum Heat Torpor Range of Table 1: Temperature Voluntary Full Activity Mean temperature responses (°C) Tolerance reported in the literature for cicadas. Maqicicada cass/n/71 20.9 31.8 43.0 22.1 Endothermic species are marked with Okanaqana hesperia2 22.9 36.3 43.5 20.6 an asterisk(*). Diceroprocta apache3 21.9 39.2 45.6 23.7 Okanaqodes qracilis* 22.7 41.2 48.7 26.0 Cacama valvata-' CamD Verde 23.7 37.3 44.6 20.9 Aqua Fria 24.0 34.9 44.3 20.3 Diceroprocta cinctifera6 17.6 34.0 45.8 28.2 Diceroprocta cinctifera var. limpia6 16.8 34.7 46.0 29.2 Diceroprocta cinctifera var. viridicosta6 16.7 35.3 46.0 29.3 Diceroprocta aurantiaca7 17.7 36.3 46.0 28.3 Diceroprocta delicata7 Northern population 19.8 33.9 46.8 27.0 Southern population 21.4 35.3 46.5 25.1 Diceroprocta olvmpusa8 20.4 37.0 46.7 26.3 Tibicen chloromerus9 19.2 34.4 45.3 26.1 Tibicen winnemanna*9 16.4 32.7 45.6 29.2 1 2 3 Guyalna bonaerensis*™ 16.7 34.6 44.6 27.9 Heath 1967, Heath 1972, Heath and Wilkin 1970, 4Sanborn etal. 1992, 5Heath Fidicina torresi*^0 19.8 32.0 42.0 22.2 et al. 1972, 6Sanborn and Phillips 1996, Quesada qj/qas*10 19.1 33.8 44.9 25.8 7Sanborn and Phillips 2001, 8Sanborn and 11 20.7 9 10 Proarna bero/* 37.6 46.3 25.6 Mate 2000, Sanborn 2000, Sanborn et 11 Proarna /ns/gn;'s* 19.3 36.4 44.0 24.7 al. 1995a, 11Sanborn etal. 1995b.

KIN 1970, SANBORN et al. 1992). It has been also delays the start of the evaporative cooling suggested that the MFT probably relates more response in these species which could be to the physical design of the cicada flight important in maintaining water balance. motor system than to the origin of the cicada HTT is strictly related to the habitat of a (HEATH et al. 1972). My laboratory has now species. The HTT appears to have evolved to found evidence to support this hypothesis. We reflect the maximum thermal load a species have been able to find several morphological might face in a particular environment. It does variables that influence lift that correlate with not appear to be related to the thermoregula- MFT. However, it appears that the environ- tory strategy or behavior of a species (HEATH ment still plays a role in determining what the MFT will be for a particular species. . 1967, HEATH & WILKIN 1970, HEATH et al. 1971, HEATH et al. 1972, HEATH 1972, SAN- The MVT is easier to relate to the habitat BORN et al. 1992, SANBORN et al. 1995a, SAN- than the MFT. There is an increase in MVT as BORN et al. 1995b, SANBORN & PHILLIPS 1996, habitats become warmer. Fidicina wrresi is SANBORN 2000, SANBORN & MATE 2000, SAN- active on the trunks of primary forest trees in BORN & PHILLIPS 2001). the tropics and has the lowest reported MVT (SANBORN et al. 1995a). The limited exposure There are some generalizations that can be to solar radiation due to the canopy means made in the analysis of the thermal responses F. torresi will save energy with a depressed of endothermic species. The endothermic

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cicadas generally have a lower MFT and a CADE 1975, SOPER et al. 1976, MANGOLD greater T^ range of full activity when compa- 1978, BELL 1979, BUCHLER & CHILDS 1981, red to ectothermic species. The low MFT of SAKALUK & BELWOOD 1984, FOWLER & the endothermic cicadas may be necessary KOCHALKA 1985, TUTTLE et al. 1985, BEL- because of their endothermic activity'. A low WOOD & MORRIS 1987). An increase in cica- MFT permits the cicada to utilize heat produ- da activity with a decrease in bird activity was ced in flight to raise Tj,. If the MFT were ele- also observed in tropical Brazil (Jones 1884). vated, low Ta could possibly inhibit activity The study of cicada thermal biology has (SANBORN et al. 1995a, SANBORN et al. 1995b, led to some interesting insights into tempera- SANBORN 2000). ture effects and thermoregulation in insects. The MVTs of the endothermic species are However, there is always more to learn about variable but generally are lower than those how temperature influences activity in ani- found in ectothermic species even if the habi- mals. We have even applied thermal biology tats are similar (SANBORN et al. 1995a, SAN- to systematics in helping to separate Dicero- BORN et al. 1995b, SANBORN 2000). The MVT procta aurantiaca DAVIS as a distinct species values obtained probably represent a balanced (SANBORN & PHILLIPS 2001). Continued rese- response to the Tas encountered during their arch using integrated methods should attempt activity period and the maximum Ta encoun- to answer more questions about the thermal tered during the day. If the upper ther- biology of this interesting group of insects. moregulatory point were elevated too high, the cicada might be unable to produce suffi- cient heat to become active at dusk. Similarly Zusammenfassung high Tas could prohibit activity if the MVT was depressed any further. Mechanismen und Strategien der Tempe- The HTTs of endothermic species show raturregelung bei Singzikaden werden im the same dependency to the environment as Überblick dargestellt, Verhaltensweisen und the HTT of ectothermic species. This is best physiologische Vorgänge zur Regulation der illustrated in the HTT of the endothermic Körpertemperatur diskutiert. Verhaltenswei- Tibicen uiinnemanna and the syntopic ecto- sen umfassen Lageveränderung des Körpers zur thermic T. chloromerus (WALKER). The HTT Sonne, sonnenbaden, Schatten aufsuchen, of both species are approximately equal even Auswahl günstiger mikroklimatischer Verhält- though the two species have vastly different nisse, Vertikalwanderung, Verwendung der behavioral strategies and thermoregulatory Flügel als "Sonnenschirm" und die Einstellung points (SANBORN 2000). der Aktivität. Die Auswirkungen der Tempe- Elevated thermal tolerances may also be ratur auf die Biologie der Singzikaden und an adaptation to predator avoidance. Dicero- deren Reaktionen auf bestimmte Temperatur- procta apache (HEATH &. WlLKiN 1970) and the verhältnisse werden diskutiert. Physiologi- syntopic species Okanagodes gracilis (SANBORN sche Reaktionen umfassen Temperaturanpas- et al. 1992) have the highest reported thermal sung, Endothermie und Kühlung durch Eva- tolerances in cicadas. Their elevated thermal poration. tolerances permit the species to be active in a habitat when their potential predators must References retreat to a thermal shelter due to the extreme heat. This is an advantage to the cicadas since AIDLEY DJ. & D.C.S. WHITE (1969): Mechanical pro- perties of glycerinated fibers from the tymbal the males produce conspicuous acoustic sig- muscles of a Brazilian cicada. — Jour. Physiol. nals to attract females. By calling when preda- 205: 179. tors are not active, the cicadas should decrea- ALEXANDER R.D. (1956): A comparative study of sound se their pressure since several types production in insects with special reference to the singing Orthoptera and of the of predators have been shown to orient to the eastern United States. — Ph. D. dissertation. The acoustic signals of insects (WALKER 1964, Ohio State University, Columbus, Ohio, 529 pp.

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ALEXANDER R.D. (1960): Sound communication in CHEUNG W.W.K. S A.T. MARSHALL (1973b): Studies on Orthoptera and Cicadidae. — In: LANYON W.E. & water and ion transport in homopteran inserts: W.N. TAVOLGA, Animal sounds and communica- Ultrastrurture and cytochemistry of the cicado- tion. — Amer. Inst. Biol. Sei. Symp. Ser. Publ. 7: id and cercopoid midgut. — Tissue and Cell 5: pp. 38-92. 651. ANNANDALE N. (1900): Observations on the habits and DAVIS W.T. (1894): Staten Island harvest . — natural surroundings of insects made during the Amer. Nat. 28: 363. "Skeat Expedition" to the Malay Peninsula, DAVIS W.T. (1894): Staten Island harvest flies. — Proc. 1899-1900. V. Sounds produced by insects. — Nat. Sei. Assoc. Staten Island 4: 9. Proc. Zool. Soc. London 1900: 859. DAVIS W.T. (1922): An annotated list of the cicadas of ANONYMOUS (1987): Glossary of terms for thermal Virginia with description of a new species. — physiology, second edition. Revised by the com- Jour. N.Y. Ent. Soc. 30: 36. mission for thermal phsiology of the internatio- nal union of physiological sciences. — Pflüg. DISTANT W.L. (1906): Order Rhynchota. Suborder Archiv. Eur. Jour. Physiol. 410: 567. . Fam. Cicadidae. — Insecta Trans- vaaliensia 7: 167. AZUMA S. (1976): Biological studies of the sugar cane DOHERTY J.A. (1985): Temperature coupling and 'tra- cicada, Mogannia minuta MATSUMURA, with de-off' phenomena in the acoustic communica- special reference to its occurence in Okinawa. — tion system of the , Gryllus bimaculatus Bull. Coll. Agric. Ryukyus Univ. 23: 125. DE GEER (Gryllidae). — Jour. Exp. Biol. 114: 17. BARTHOLOMEW G.A. & M.C. BARNHARDT (1984): Tracheal DOOLAN J.M. & R.C. MACNALLY (1981): Spatial dyna- gases, respiratory gas exchange, body tempera- mics and breeding ecology in the cicada, Cysfo- ture and flight in some tropical cicadas. — Jour. soma saundersii: The interaction between distri- Exp. Biol. 111: 131. butions of resources and interspecific behavior. BARTHOLOMEW G.A. & R.G. EPTING (1975): Allometry of — Jour. Anim. Ecol. 50: 925. post-flight cooling rates in moths: A comparison DORSETT D.A. (1962): Preparation for flight by hawk- with vertebrate homeotherms. — Jour. Exp. moths. — Jour. Exp. Biol. 39: 579. Biol. 63: 603. DUFFELS J.P. (1988): The cicadas of the Fiji, Samoa, and BARTHOLOMEW G.A. & B. HEINRICH (1978): Endothermy Tonga Islands, their and biogeogra- in African dung during flight, ball phy (Homoptera, Cicadoidea) with a chapter on making, and ball rolling. — Jour. Exp. Biol. 73: the geological history of the area by A. Ewart. 65. — Entomonograph 10: 1. BELL P.D. (1979): Acoustic attraction of herons by DURIN B. (1981): Inserts Etc.: An anthology of Arthro- crickets. — Jour. N.Y. Ent. Soc. 87: 126. pods featuring a bounty of beetles. — Hudson BELWOOD J.J. & G.K. MORRIS (1987): predation and Hills Press, New York, 108 pp. its influence on calling behavior in neotropical ELLINGTON C.P. (1984): The aerodynamics of hovering katydids. — Science 238: 64. insert flight. VI. Lift and power requirements. — BUCHLER E.R. S S.B. CHILDS (1981): Orientation to Phil. Trans. Roy. Soc. Lond. Ser. B. 305: 145. distant sounds by big brown (Eptescus ELLINGTON C.P. (1985): Power and efficiency of insert fuscus). — Anim. Behav. 29: 428. flight muscle. —Jour. Exp. Biol. 115: 293.

CADE W. (1975): Acoustically orienting : fly FLEMING C.A. (1975): Adaptive radiation in New Zea- phonotaxis to cricket song. — Science 190: land cicadas. — Proc. Amer. Phil. Soc. 119: 298. 1312. FOWLER H.G. & J.N. KOCHALKA (1985): New record of CASEY T.M. (1981a): Energetics and thermoregulation Euphasiopteryx depleta (Diptera: ) of Malacosoma americanum (Lepidoptera: from Paraguay: Attraction to broadcast calls of Lasiocampidae) during hovering flight. — Scapteriscus acletus (Orthoptera: Gryllotalpi- Physiol. Zool. 54: 362. dae). — Florida Entomol. 68: 225. HADLEY N.F., QUINLAN M.C. & M.L. KENNEDY (1991): Eva- CASEY T.M. (1981b): A comparison of mechanical and porative cooling in the desert cicada: thermal energetics estimates of flight cost for hovering efficiency and water/metabolic costs. — Jour. sphinx moths. — Jour. Exp. Biol. 91: 117. Exp. Biol. 159: 269. CASEY T.M., MAY M.L. & K.R. MORGAN (1985): Flight HADLEY, N.F., TOOLSON E.C. & M.C. QUINLAN (1989): energetics of Euglossine in relation to mor- Regional differences in cuticular permeability in phology and wing stroke frequency. — Jour. the desert cicada Diceroprocta apache: Implica- Exp. Biol. 116:271. tions for evaporative cooling. — Jour. Exp. Biol. CHAPPELL M.A. & K.R. MORGAN (1987): Temperature 141: 219. regulation, endothermy, resting metabolism, HARTZELL A. (1954): Periodical cicada. — Contrib. and flight energetics of Tachnid flies {Nowickia Boyce Thompson Inst. 17: 375. sp.). — Physiol. Zool. 60: 550. HASTINGS J.M. (1989): Thermoregulation in the CHEUNG W.W.K. S A.T. MARSHALL (1973a): Water and dog-day cicada Tibicen duryi (Homoptera: ion regulation in cicadas in relation to xylem Cicadidae). — Trans. Kentucky Acad. Sei. 50: feeding. — Jour. Insect Physiol. 19: 1801. 145.

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HASTINGS J.M. & E.C. TOOLSON (1991): Thermoregulati- KAMMER A.E. (1970): Thoracic temperature, shivering, on and activity patterns of 2 syntopic cicadas, and flight in the monarch butterfly, Danaus Tibicen chiricahua and T. duryi (Homoptera, plexippus (L). — Zeit. f. Vergl. Physiol. 68: 334. Cicadidae), in central New Mexico. — Oecologia KAMMER A.E. (1981): Physiological mechanisms of 85: 513. thermoregulation. — In: HEINRICH B., Insect HAYASHI M. (1982): Notes on the distribution of Cica- thermoregulation, John Wiley & Sons, New didae (Insecta, Homoptera) in the Fuji-Hakone- York, pp. 115-158. Izu area. — Mem. Nat. Sei. Mus., Tokyo 15: 187. KASER S.A. & J. HASTINGS (1981): Thermal physiology of HEATH J.E. (1967): Temperature responses of the the cicada Tibicen duryi. — Amer. Zool. 21: periodical "17-year" cicada, Magicicada Cassini 1016. (Homoptera, Cicadidae). — Amer. Midi. Nat. 77: KERSHAW J.C. (1903): A naturalist's notes from . 64. — Field Nat. Quart. 2: 233. HEATH J.E. (1968): Thermal synchronization of emer- MANGOLD J.R. (1978): Attraction of Euphasiopteryx gence in periodical "17-year" cicadas (Homop- ochracea, Corethrella sp. and gryllids to broad- tera, Cicadidae, Magicicada). — Amer. Midi. cast songs of the southern mole cricket. — Nat. 80: 440. Florida Entomol. 61: 57. HEATH J.E. (1970): Behavioral regulation of body tem- perature in poikilotherms. — Physiologist 13: MARSHALL A.T. (1983): X-ray microanalysis of the filter 399. chamber of the cicada, australasiae DON.: A water-shunting epithelial complex. — HEATH J.E., HANAGAN J.L, WILKIN P.J. & M.S. HEATH Cell and Tissue Res. 231: 215. (1971): Adaptation of the thermal responses of insects. — Amer. Zool. 11: 147. MARSHALL A.T. & W.W.K. CHEUNG (1973): Studies on water and ion transport in homopteran insects: HEATH J.E. & P.J. WILKIN (1970): Temperature respon- infrastructure and cytochemistry of the cicado- ses of the desert cicada, Diceroprocta apache id and cercopoid malpighian tubules and filter (Homoptera, Cicadidae). — Physiol. Zool. 43: chamber. — Tissue & Cell 6: 153. 145. MARSHALL A.T. & W.W.K. CHEUNG (1974): Studies on HEATH J.E., WILKIN P.J. & M.S. HEATH (1972): Tempera- water and ion transport in homopteran insects: ture responses of the cactus dodger, Cacama Ultrastructure and cytochemistry of the cicado- valvata (Homoptera, Cicadidae). — Physiol. id and cercopoid hindgut. — Tissue 8 Cell 5: Zool. 45: 238. 671. HEATH M.S. (1972): Temperature requirements of the MARSHALL A.T. & W.W.K. CHEUNG (1975): Ionic balance cicada striatipes beameri: A study of Homoptera in relation to feeding site and from Flagstaff, Arizona. — Plateau 45: 31. plant composition. — Entomol. Exp. Appl. HEATH M.S. (1978): Genera of American cicadas north 18: 117. of Mexico. — Ph. D. dissertation, University of MATSUMURA S. (1898): A summary of Japanese Cicadi- Florida, Gainesville, 231 pp. dae with description of a new species. — Ann. Zool. Jap. 2: 1. HEINRICH B. (1981): Temperature regulation during locomotion in insects. — In: HERRIED C.F. & C.R. MAY M.L. (1976): Warming rates as a function of FOURTNER, Locomotion and energetics in Arthro- body size in periodic endotherms. — Jour. pods, Plenum Press, New York, pp. 391-417. Comp. Physiol. 111B: 55.

HEINRICH B. (1993): The hot-blooded insects. — MOORE T.E. (1962): Acoustical behavior of the cicada Harvard University Press, Cambridge, 601 pp. Fidicina pronoe (WALKER) (Homoptera: Cicadi- dae). — Ohio Jour. Sei. 62: 113. HUDSON G.V. (1890): On the Cicadidae. — Trans. Proc. New Zealand Inst. 23: 49. NAGAMINE M. & R. TERUYA (1976): Life history of Mogannia iwasakii MATSUMURA. — Bull. Okinawa JOERMANN G. S H. SCHNEIDER (1987): The songs of four Agric. Exp. Sta. 2: 15. species of cicada in Yugoslavia (Homoptera: OHGUSHI R. (1954): Preliminary study on a cicada com- Cicadidae). — Zool. Anz. 219: 283. munity at Mt. Nakatsumine. — KontyCl 21: 10. JONES E.D. (1884): In the tropics. — Naturalist (2)9: POPOV A.V., ARONOV I.B. & M.V. SERGEEVA (1985): 125. Calling songs and hearing in cicadas from Sovi- JOSEPHSON R.K. (1981): Temperature and the mecha- et Central Asia. — Jour. Evol. Biochem. Physiol. nical performance of insect muscle. — In: 21: 288. Heinrich B., Insect thermoregulation, John PRANGE H.D. (1996): Evaporative cooling in insects. — Wiley & Sons, New York, pp. 19-44. Jour. Insect Physiol. 42: 493.

JOSEPHSON R.K. & D. YOUNG (1979): Body temperature RAMSAY G.W. (1959): Notes on the ecology of some and singing in the bladder cicada, Cystosoma cicadas in the Wellington District. — New Zea- saundersii. — Jour. Exp. Biol. 80: 69. land Entomol. 2: 29.

JOSEPHSON R.K. & D. YOUNG (1985): A synchronous ins- SAKALUK S.K. & J.J. BELWOOD (1984): Gecko phonotaxis ect muscle with an operating frequency greater to cricket song: a case of satellite predation. — than 500 Hz. — Jour. Exp. Biol. 118: 185. Anim. Behav. 32: 659.

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SANBORM A.F. (1997): Body temperature and the acou- TALHOUK A.S. (1959): The grapevine cicada stic behavior of the cicada Tibicen winnemanna Chloropsalta viridissima (WALKER) (Homoptera- (Homoptera: Cicadidae). — Jour. Insect Behav. Cicadidae). — Proc. Int. Cong. Crop Protect., 10: 257. Hamburg 1: 799.

SANBORN A.F. (2000): Comparative thermoregulation TOOLSON E.C. (1984): Interindividual variation in epi- of sympatric endothermic and ectothermic cica- cuticular hydrocarbon composition and water das (Homoptera: Cicadidae: Tibicen winneman- loss rates of the cicada, Tibicen dealbatus na and Tibicen chloromerus). — Jour. Comp. (Homoptera: Cicadidae). — Physiol. Zool. 57: Physiol. 186A: 551. 550.

SANBORN A.F. (2001): Timbal muscle physiology in the TOOLSON E.C. (1985): Evaporative cooling in the endothermic cicada Tibicen winnemanna desert cicada, Diceroprocta apache. — Amer. (Homoptera: Cicadidae). — Comp. Biochem. Zool. 25: 144A. Physiol. : in press. TOOLSON E.C. (1987): Water profligacy as an adap- SANBORN A.F., HEATH J.E. & M.S. HEATH (1992): Ther- tation to hot deserts. Water loss rates and eva- moregulation and evaporative cooling in the porative cooling in the Sonoran Desert cicada, cicada Okanagodes gracilis (Homoptera: Cicadi- Diceroprocta apache (Homoptera: Cicadidae). dae). — Comp. Biochem. Physiol. 102A: 751. — Physiol. Zool. 60: 379.

SANBORN A.F., HEATH J.E., HEATH M.S. & F.G. NORIEGA TOOLSON E.C. (1993): In the Sonoran Desert cicadas (1995b): Thermoregulation by endogenous heat court, mate, and waste water. — Nat. Hist. 102: production in two South American grass dwel- 37. ling cicadas (Homoptera: Cicadidae: Proarna). — Florida Entomol. 78: 319. Toolson E.C. (1998): Comparative thermal physiolo- gical ecology of syntopic populations of Cacama SANBORN A.F., HEATH M.S., HEATH J.E. & F.G. NORIEGA valvata and Tibicen bifidus (Homoptera: Cicadi- (1995a): Diurnal activity, temperature responses dae): Modeling fitness consequences of tempe- and endothermy in three South American cica- rature variation. — Amer. Zool. 38: 568. das (Homoptera: Cicadidae: Dorisiana bonae- rensis, Quesada gigas, and Fidicina mannifera). TOOLSON E.C, ASHBY P.D., HOWARD R.W. & D.W. STANLEY- — Jour. Thermal Biol. 20: 451. SAMUELSON (1994): Eicosanoids mediate control of thermoregulatory sweating in the cicada, SANBORN A.F. S S. MATE (2000): Thermoregulation and Tibicen dealbatus (Insecta: Homoptera). — Jour. the effect of body temperature on call temporal Comp. Physiol. 164B: 278. parameters in the cicada Diceroprocta olympu- sa (Homoptera: Cicadidae). — Comp. Biochem. TOOLSON E.C. & N.F. HADLEY (1987): Energy-dependent Physiol. 125A: 141. facilitation of transcuticular water flux contri- butes to evaporative cooling in the Sonoran SANBORN A.F. & P.K. PHILLIPS (1992): Observations on Desert cicada, Diceroprocta apache (Homop- the effect of a partial solar eclipse on calling in tera: Cicadidae). — Jour. Exp. Biol. 131: 439. some desert cicadas (Homoptera: Cicadidae). — Florida Entomol. 75: 285. TOOLSON E.C. & E.K. TOOLSON (1991): Evaporative cooling and endothermy in the 13-year periodi- SANBORN A.F. & P.K. PHILLIPS (1996): Thermal responses cal cicada, (Homoptera, of the Diceroprocta cinctifera species group Cicadidae). — Jour. Comp. Physiol. 161B: 109. (Homoptera: Cicadidae). — Southwestern Nat. 41: 136. TUTTLE M.D., RYAN M.J. & J. BELWOOD (1985): Acousti- cal resource partitioning by two species of SANBORN A.F. & P.K. PHILLIPS (2001): Re-evaluation of phyllostomatid bats (Trachops cirrhosus and the Diceroprocta delicata species complex Tonatia silvicola). — Anim. Behav. 33: 1369. (Homoptera: Cicadidae). — Ann. Ent. Soc. Amer. 94: in press. VRIJER P.W.F. de (1984): Variability in calling signals of SCHEDL V.W. (1986): Zur Verbreitung, Biologie und the pellucida (F.) (Homop- Ökologie der Singzikaden von Istrien und dem tera: ) in relation to temperature, angrenzenden Küstenland (Homoptera: and consequences for species recognition Cicadidae und Tibicinidae). — Zool. Jahr. Abt. f. during distant communication. — Netherlands Syst. Ökol. Geog. Tiere 113: 1. Jour. Zool. 34: 388.

SOPER R.S., SMITH L.F.R. & A.J. DELYZER (1976): Epizoo- WAKABAYASHI T. & S. HAGIWARA (1953): Mechanical and tiology of levispora in an isolated electrical events in the main sound muscle of population of Okanagana rimosa. — Ann. Ent. cicada. — Jap. Jour. Physiol. 3: 249. Soc. Amer. 69: 275. WAKABAYASHI T. & K. IKEDA (1961): Interrelation

STANLEY-SAMUELSON D.W., HOWARD R.W. & E.C. TOOLSON between action potential and miniture electri- (1990): Phospholipid fatty acid composition and cal oscillation in the tymbal muscle of the arachidonic acid uptake and metabolism by the cicada. — Jap. Jour. Physiol. 11: 585. cicada Tibicen dealbatus (Homoptera: Cicadi- WALKER T.J. (1957): Specificity in the response of dae). — Comp. Biochem. Physiol. 97B: 285. female tree crickets (Orthoptera, Gryllidae, SWINTON A.H. (1908): The vocal and instrumental Oecanthinae) to calling songs of the males. — music of insects. — Zoologist (4th Ser.) 12: 376. Ann. Ent. Soc. Amer. 50: 626.

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WALKER T.J. (1963): The taxonomy and calling songs of United States tree crickets (Orthoptera: Gryllidae: Oecanthinae). II. The nigricornis group of the genus Oecanthus. — Ann. Ent. Soc. Amer. 56: 772.

WALKER T.J. (1964): Experimental demonstration of a cat locating Orthoptera prey by the prey's calling song. — Florida Entomol. 47: 163.

WARD G.M. (1967): Close to nature. — Victorian Nat. 84: 360.

WEIS-FOGH T. (1972): Energetics of hovering in hummingbirds and Drosophila. — Jour. Exp. Biol. 56: 79.

WEIS-FOGH T. (1976): Energetics and aerodynamics of flapping flight: a synthesis. — In: RAINEY R.C, Ins- ect flight, Wiley Publishing, New York, pp. 48-72.

WHITE J. & C. STREHL (1978): Xylem feeding by peri- odical cicada nymphs on tree roots. — Ecol. Entomol. 3: 323.

YOUNG A.M. (1974): The population biology of neotropical cicadas. III. Behavioral of in Costa Rican grasslands. — Ent. News 85: 239.

YOUNG A.M. (1975): The population biology of neotropical cicadas. I. Emergence of Procollina and in a mountain forest. — Bio- tropica 7: 248.

YOUNG A.M. (1980): Observations on the aggregation of adult cicadas (Homoptera: Cicadidae) in tropical forests. — Can. Jour. Zool. 58: 711.

YOUNG A.M. (1981): Notes on seasonality and habitat associations of tropical cicadas (Homoptera: Cicadidae) in premontane and montane tropical moist forest in Costa Rica. — Jour. N.Y. Ent. Soc. 89: 123.

Address of the author:

Dr. Allen F. SANBORN School of Natural & Health Scien- ces, Barry University, 11300 NE Second Avenue, Miami Shores, FL 33161-6695, USA.

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