Cicada Thermoregulation (Hemiptera, Cicadoidea) 455-470 © Biologiezentrum Linz/Austria; Download Unter
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ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Denisia Jahr/Year: 2002 Band/Volume: 0004 Autor(en)/Author(s): Sanborn Allen F. Artikel/Article: Cicada Thermoregulation (Hemiptera, 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 cicadas 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), 455-470 455 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at 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 animal. Animals 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 species (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 enzymes 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, 456 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at 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 xylem 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 perches 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 order 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 457 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Tj, (1.5-2.O°C). In addition, the T^ range of changes of Tj, in Cacama 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.