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Simultaneous Control of Head and Thoracic Temperature by the Green Darner Dragonfly Anax Junius (Odonata: Aeshnidae)

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Simultaneous Control of Head and Thoracic Temperature by the Green Darner Dragonfly Anax Junius (Odonata: Aeshnidae) The Journal of Experimental Biology 198, 2373–2384 (1995) 2373 Printed in Great Britain © The Company of Biologists Limited 1995 SIMULTANEOUS CONTROL OF HEAD AND THORACIC TEMPERATURE BY THE GREEN DARNER DRAGONFLY ANAX JUNIUS (ODONATA: AESHNIDAE) MICHAEL L. MAY Department of Entomology, Cook College, New Jersey Agricultural Experiment Station, Rutgers University, New Brunswick, NJ 08903, USA Accepted 24 July 1995 Summary Anax junius is a large dragonfly that regulates thoracic during unrestrained flight in the field, Th is regulated temperature (Tth) during flight. This species, like several actively by increasing hemolymph circulation from the other intermittently endothermic insects, achieves control warm thorax at low Ta. Concurrent measurements of of Tth at least in part by increasing circulation of abdominal temperature (Tab) confirm that the abdomen is hemolymph to the abdomen at high air temperature (Ta), used as a ‘thermal window’ at Ta>30 ˚C but apparently not thus facilitating heat loss from the thorax. In this paper, I at lower Ta; thus, some additional mechanism(s) must exist demonstrate that heat transfer to the head is also under for regulation of Tth at low Ta. active control, very probably owing to temperature- sensitive alteration of hemolymph circulation. As a result, head temperature (Th) is strikingly elevated above Ta Key words: Anax junius, Anisoptera, body temperature, circulatory during endothermic warm-up and flight. Furthermore, control, dragonfly, green darner, heat exchange, thermoregulation. Introduction Numerous insects regulate Tth (most recently and The primary aim of this study is to investigate the sources comprehensively reviewed by Heinrich, 1993), among them of variation of Th, its mechanism of control and its responses the subject of this paper Anax junius (Drury) (Heinrich and to environmental temperature and internal variables in A. Casey, 1978; May, 1976, 1986, 1991; Polcyn, 1988). Early junius, a large, highly endothermic dragonfly. The results also work on sphinx moths was interpreted as indicating that these call into question, in this case, the standard model of regulation ‘mammal-like’ insects support a high and constant Tth during of Tth exclusively by modulation of heat loss. flight by elevating metabolic rate at low Ta (Heath and Adams, 1965). Heinrich (1970, 1971a,b) showed, however, that flight metabolic rate is independent of Ta, while heat loss is Materials and methods augmented at high Ta via hemolymph flow between the thorax Experimental procedures and abdomen; this has become the standard paradigm for Body temperatures of Anax junius (see Table 1 for endothermic regulation during flight in insects, including definitions and measurement locations) were recorded in still dragonflies (e.g. Heinrich and Casey, 1978; May, 1976). air and over a range of wind speeds in the laboratory using Research has focused on Tth because the thoracic flight 0.0029 (0.005 cm) diameter copper–constantan (Cu–Cn) muscles are both the primary internal source of heat and thermocouples. Output was recorded at 5–15 s intervals (or up themselves functionally sensitive to temperature (e.g. to 60 s for Ta and Tab2 records), on a Honeywell Electronik 112 Josephson, 1981) and because Tth is relatively easy to measure. Multipoint thermocouple recorder. Airflow was controlled Head temperature has attracted much less attention despite its using a small, open-section, open-flow wind-tunnel consisting possible importance in cephalic neural functioning. Heinrich of a 1.5 m length of 7.5 cm diameter plastic pipe and either a (1980a,b) again pioneered the field, showing that honeybees small centrifugal or axial-flow fan, with layers of cheesecloth reduce Th at high Ta by evaporation and consequently reduce acting as diffusers just downstream of the fan. Most Tth by conduction. Regulation of Th has also been reported in experiments were carried out in a walk-in temperature- a moth (Hegel and Casey, 1982) and a carpenter bee (Baird, controlled chamber. 1986), and Th was thought to be elevated but not regulated in Heat exchange coefficients (see Table 1 for definitions) other bees (May and Casey, 1983; Heinrich and Buchmann, were determined for each tagma in dead dragonflies (May, 1986) and a dragonfly (May, 1987). 1976; Heath and Adams, 1969) in still air and at wind speeds 2374 M. L. MAY 21 from 0.25 to 3.5 m s . The model used to calculate heat loss Apparent Cth is little affected by heat exchange with the head from the entire body (see below) requires estimates of the and abdomen (M. L. May, unpublished data) because the latter coefficients that are independent of heat exchange among cool more rapidly and are usually much less massive, so I made tagmata, but apparent values of Ch and Cab calculated from no such correction of Cth values. cooling curves of intact specimens are reduced by contact with Simultaneous effects of wind and radiation on body the massive, insulated thorax (Hegel and Casey, 1982; temperatures of intact, freshly killed specimens were measured Heinrich, 1980b), which remains warmer throughout cooling as described by May (1987). A 650 W lamp was positioned than the head or abdomen. Therefore, in some additional perpendicular to the body axis above the wind-tunnel outlet. specimens, I measured, at 0.5 and 2 m s21, the conductance of Radiation intensity was adjusted to 200 or 800 W m22 by the head and abdomen dissected from the thorax and reattached varying the distance from the lamp to the insect. using small wooden pegs to a dried A. junius thorax to During endothermic warm-up, specimens were shielded duplicate the airflow regime over intact insects but to minimize from room air currents. If warm-up did not begin heat gain from the thorax. These data were used to correct Ch spontaneously, it was induced by pinching the abdomen. Some and Cab values obtained over the full range of wind speeds. individuals were then killed and a 0.25 W, 1 kV resistor was Table 1. Definitions of symbols Symbol Definition Description −1 Cth (min ) External heat exchange Calculated from cooling curves of dead, intact specimens as described in Materials coefficient (thermal and methods conductance) of thorax −1 Ch (min ) External heat exchange Determined as for Cth coefficient (thermal conductance) of head −1 Cab (min ) External heat exchange Determined as for Cth coefficient (thermal conductance) of abdomen −1 Ch* (min ) Corrected heat exchange Determined as for Ch but for head dissected from body, then reattached to a dried coefficient of head thorax as described in Materials and methods −1 Cab* (min ) Corrected heat exchange Determined as for Ch* coefficient of abdomen −1 Eh (min ) Internal heat exchange Calculated as described in text; indicates ease of heat exchange between coefficient of head head and thorax −1 Eab (min ) Internal heat exchange Calculated as described in text; indicates ease of heat exchange between coefficient of abdomen abdomen and thorax Mth (g) Mass of thorax See Materials and methods Mh (g) Mass of head See Materials and methods Mab (g) Mass of abdomen See Materials and methods Rh Temperature excess ratio Calculated as in equation 1, Materials and methods of head Rab Temperature excess ratio Calculated as in equation 1, Materials and methods of abdomen SR (W m−2) Solar radiation intensity See Materials and methods Ta (°C) Air temperature In the laboratory, bare thermocouple junction placed within 10 cm of insect; in the field, with dried probe at site of capture Tth (°C) Thoracic temperature In the laboratory, junction inserted through the left metepisternum to near center of thoracic muscle mass; in the field, probe inserted into thoracic muscles Th (°C) Core head temperature In the laboratory, junction inserted towards center of head about 3 mm beneath the antero-medial margin of the left eye; in the field, probe inserted to near center of head Th′ (°C) Peripheral head temperature In the laboratory, junction running for about 2 mm just beneath the dorsal cornea of the right eye Tab (°C) Abdominal temperature In the laboratory, junction inserted laterally 1-2 mm into base of third abdominal segment; in the field, probe inserted into second or third abdominal segment Tab1 (°C) Basal abdominal temperature As for Tab, laboratory only Tab2 (°C) Distal abdominal temperature Junction inserted laterally about 1 mm into seventh abdominal segment Temperature regulation in a dragonfly 2375 implanted near the center of the flight musculature through the determined by tissue conductivity and by bulk flow of fluids posteroventral thoracic wall. Current was applied from a (for practical purposes, hemolymph). regulated power supply, adjusted to raise Tth to the desired A convenient indicator of the relative magnitudes of Ch and level, and Th and Tab were monitored to measure passive heat Eh (or of Cab and Eab) is Rh (or Rab), the ratio of the temperature exchange within the body. To test the effects of wind excesses of the head (or abdomen) and thorax, for example: movement, the body was supported in front of the wind-tunnel Rh = (Th 2 Ta)/(Tth 2 Ta) . (1) on the stiff resistor leads. Live dragonflies were heated externally with a microscope At thermal equilibrium (May, 1991), lamp focused onto the thoracic dorsum while the head and Rh = Eh/(Eh + Ch) . (2) thorax were shielded with aluminum foil. The wings were firmly taped to the arms of a U-shaped acrylic plate so the body Thus, in still air or during steady forward flight, Rh should be was suspended freely between the arms in front of the wind- independent of Ta unless heat flow from thorax to head changes tunnel; flexion of the abdomen was restricted by a thin wire with Ta. If hemolymph is used to unload excess thoracic heat fastened across the gap. Air speed near the body in this via the head at high Ta, thus increasing Eh, Rh should increase apparatus was nearly the same as in the free stream.
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