JEB Classics 177 THE ORIGIN OF George Newport had reported that there is JEB Classics is an occasional THERMOREGULATORY a correlation between activity and elevated column, featuring historic body temperature in a , a bumblebee, publications from The Journal of STUDIES and a (Newport, 1837). After the Experimental Biology. These subject remained fallow for the following articles, written by modern experts 60 years the Russian physicist Perfirij J. in the field, discuss each classic Bachmetjev resurrected the subject when paper’s impact on the field of he identified the same correlation in biology and their own work. A just before the end of the 19th Century PDF of the original paper is (Bachmetjev, 1899). Similarly, Heinz available from the JEB Archive Dotterweich showed specifically that the (http://jeb.biologists.org/). rise in thoracic temperature of sphinx is related to the insects’ flight preparations (Dotterweich, 1928). In Krogh’s own laboratory in Denmark, Marius Nielsen showed that human body temperature also rises during strenuous activity, and is then regulated at a high level corresponding to work output (Nielsen, 1938). Referencing these early, possibly forgotten, classical studies in Krogh and Zeuthen’s 1941 paper brought the neglected topic of to the forefront of the then hot field of respiratory physiology.

Prior to Krogh and Zeuthen’s work, reports Bernd Heinrich writes about August Krogh of insect thermoregulation were mainly and Eric Zeuthen’s 1941 classic paper on s descriptive. However, their 1941 paper was insect thermoregulation entitled ‘The the first to attempt to crack the proverbial mechanism of flight preparation in some black box of the underlying physiological insects’. A copy of the paper can obtained mechanisms. It set the stage for subsequent at c work by reviewing salient points from the http://jeb.biologists.org/cgi/reprint/18/1/1 scant data available on muscle temperature

i and mechanical work of insects prior to Some ‘classic’ papers shine for their sheer flight or while resting. Using brilliance and thoroughness. They put an thermocouples implanted in butterfly end to argument. Others pioneer a new (Vanessa) flight muscles, they

s method that opens up novel directions of demonstrated that wing movements during research, or they focus on a previously both pre-flight shivering and flight, are ignored work and bring it to light. Still associated with a steady rise in muscle others have impact because they draw temperature until temperatures approaching s attention when a big gun stumbles across human body temperature are reached. The an obstacle or exposes a gaping hole in our butterflies were then thrown into the air to knowledge. I believe that the 1941 paper find the muscle temperatures that enabled by August Krogh and Eric Zeuthen does the insects to fly. Krogh and Zeuthen’s a some or all of the above in the area where observation led them to disagree with insect physiology intersects ecological previous observations about insect flight l energetics and thermoregulation. Working temperatures, stating that ‘We cannot together, they examined a butterfly, a subscribe to Dotterweich’s statement that bumblebee, and a beetle, and concluded moths require a definite temperature to be that the temperature of an insect’s flight able to fly. We made a few observations on

C muscle during pre-flight warm-up Catocola sponsa, measuring thoracic determines its maximal rate of work output temperature and then throwing the moths during flight (Krogh and Zeuthen, 1941). I into the air. These observations indicate first read the Krogh and Zeuthen paper in that at muscle temperatures above 25°C the mid 1960’s when I became interested in this species is able to fly’. Although Krogh insect physiology with the aim of and Zeuthen’s statement does not specify

B discerning mechanisms of what temperatures ‘a few’ observations thermoregulation. I think their paper was encompass, nor what a ‘definite’ inspiring, not for any one particular temperature is, it is clear to me that the

E discovery, but rather for their approach. moth can fly at temperatures as low as 25°C and is not restricted to just the However, the concept that flight muscle narrow range of high muscle temperatures

J activity raised body temperature was hardly that they reported for flight in other insects. new, even in 1941. A century earlier Apparently Dotterweich drew incorrect

THE JOURNAL OF EXPERIMENTAL BIOLOGY JEB Classics 178 generalizations about temperature during insect pre-flight warm-up is unlikely potentials and wing muscle contractions regulation, extrapolating from sphinx to be an adaptation for the discharge of that would translate to wing movements. moths to other moths. nervous impulses from the ganglia to the These incorrect assumptions stimulated my muscles. Instead, they state that it is own work when I realised that bees achieve Next the team extended their observations ‘required to allow the muscular engine to impressive temperature increases without of flight muscle temperature into the develop the energy expenditure for flight’. moving their wings, and it eventually bumblebee Bombus horti and found that This, a major point of their paper, became apparent that the wing muscles are the bumblebee’s temperatures paralleled established the framework and a trajectory in tetanus during warm-up (Kammer and those of the butterfly; the thoracic muscles of subsequent insect thermoregulation Heinrich, 1974). Numerous subsequent heated up to at least 30°C before flight. studies for those that followed their lead studies over the next half century revealed Measurements of the insect’s abdominal into physiology. To my knowledge, the fascinating mechanisms of muscle function temperature showed that it was only authors themselves did not proceed further and morphological adaptations for damping slightly elevated, enhancing the team’s in this area, possibly because of the war: thoracic and wing vibrations during warm- point that the flight muscles are indeed the there is a note at the end of the paper, up (Esch et al., 1991) and that ‘warm-up’ source of the body heat, and that the action which states that ‘Owing to war conditions, plays a role in a variety of other of warming-up permits high energy the authors have been unable to submit physiological phenomena besides flight expenditure during flight. corrected proofs prior to publication’. preparation, including brood incubation and colony defense. Krogh and Zeuthen also Krogh and Zeuthen’s final observations in While the paper clearly laid out the essential implied that abdominal temperature is their 1941 paper focused on the large role of thermoregulation in flight, the passive, with thoracic heat simply diffusing (weighing in at almost one gram) authors also enunciated several apparent into the abdomen, setting up another lamellicorn beetle, Geotrupes stercorarius. enigmas that would concern many of the strawman that stimulated subsequent Large ‘pump’ their abdomen prior researchers who followed in their wake. For research that ultimately yielded to flight, and since beetles show no example, why do some insects require a breakthroughs in our understanding of externally-visible motion of the wings or high muscle temperature in order to fly, insect thermoregulation, behavior and social elytra prior to flight, it was presumed that while others do not? Krogh and Zeuthen ecology (reviewed in Heinrich, 1993; they did so in order to raise the oxygen assumed (an assumption that held for the Heinrich, 1996). concentration of the tracheal system. next 30 years) that the maximum flight However, Krogh and Zeuthen’s electrical temperature achieved is only that which the Their short (it would fit into 4 or 5 pages recordings from the flight muscles showed insect spends valuable energy to achieve. in JEB’s current format) paper’s main neural spiking activity as the beetle Since all the work was done with highly influence, I believe, arose not only from warmed up; the flight muscles were active restrained animals, not free-flying ones, the clear and incisive insights it provided even though the wings did not move. That there was never any suggestion that some through simple direct observations, but also is, these insects, which appeared to fly insects might produce heat in excess of their from the unknowns (and interesting without prior shivering, were indeed flight requirements. In their attempt to mistakes) it highlighted. It also emphasises exercising their flight muscles, and since explain this enigma of variable flight the little that was known about insect working muscles require vigorous gas temperatures, Krogh and Zeuthen merely thermoregulation in 1941, most of which exchange, that explained the abdominal suggested that those insects requiring high had been buried in the literature for up to a pumping. It was this observation of muscle temperatures are ‘bad flyers’ and century. ‘invisible’ muscle activity in particular that those who fly at lower temperatures ‘good I found the most intriguing, because it flyers’. It would nowadays be a bit of a Ironically, although the paper by Krogh showed that much was still hidden and stretch to characterize sphinx moths and and Zeuthen focused on muscle unknown. bees as ‘bad’ flyers. Undoubtedly, many physiology, the last paragraph introduced a subsequent studies on the aerodynamics of way of connecting the muscle temperature For me, one of the most provocative insect flight owe at least some of their of the animal with practical estimates of its aspects of Krogh and Zeuthen’s paper was inspiration to Krogh and Zeuthen’s claim energy input and expenditure. For me, that their use of the insects’ cooling curves to about the bumblebee’s ineptitude. I was observation culminated in field studies that estimate energy expenditure, measurements personally inspired to instigate numerous revealed the ecological and evolutionary relationships between bees and flowers and which are still considered virtually studies to determine what body temperatures stimulated me to write the book impossible in free-living animals. When insects flew with and why some had evolved Bumblebee Economics (Heinrich, 1979), their insects stopped exercising they cooled to fly with a low but others with a high which encompassed the enigmas first rapidly to their initial body temperatures, thoracic temperature, all of which ultimately hinted at in this classic paper and the and from the cooling curve Krogh and provided insights into the evolution of insights they subsequently inspired. Zeuthen calculated the insects’ energy thermoregulation (Heinrich, 1977). expenditures, compared them with insect’s 10.1242/jeb.000679 metabolic rate calculated from measured The authors also made mistakes. They rates of carbon dioxide production, and incorrectly posited from their electrical Bernd Heinrich found ‘satisfactory agreement’. recordings from bumblebee flight muscles University of Vermont Furthermore, they converted metabolic that the muscles of these bees generated a [email protected] rates to the caloric intake from sugar vibration frequency of 100·Hz during collected from flowers that was required to shivering (vs 20·Hz for Vanessa butterfly support the insects in pre-flight flight muscle). They had apparently References preparation. assumed that the bee was shivering only Bachmetjev, P. J. (1899). Ueber die when it moved its wings to buzz, making Temperaturen der Insekten nach Beobachtungen Given their simple calculations, Krogh and the ‘reasonable’ assumption that there is a in Bulgarien. Z. Wiss. Zool. 66, 521-604. Zeuthen concluded that the heating process one-to-one correlation between action Dotterweich, H. (1928). Beitrage zur

THE JOURNAL OF EXPERIMENTAL BIOLOGY JEB Classics 179 Nervenphysiologie den Insekten. Zool. Jahrbuch. Heinrich, B. (1993). The Hot-blooded Insects: mechanism of flight preparation in some insects. Abteil. Allgemeine Zoolog. Tiere 44, 399-450. Mechanisms and Evolution of Thermoregulation. J. Exp. Biol. 18, 1-10. Esch, H., Goller, F. and Heinrich, B. (1991). Cambridge, MA: Harvard University Press. Newport, G. (1837). On the temperature of How do bees shiver? Naturwissenschaften. 78, Heinrich, B. (1996). The Thermal Warriors: insects, and its connexion with the functions of 325-328. Strategies of Insect Survival. Cambridge, MA: respiration and circulation in this class of Heinrich, B. (1977). Why have some animals Harvard University Press. invertebrate animals. Phil. Trans. R. Soc. Lond. evolved to regulate a high body temperature? Kammer, A. E. and Heinrich, B. (1974). 127, 259-338. Am. Naturalist 111, 626-640. Metabolic rates related to muscle activity in Nielsen, M. (1938). Die Regulierung der Heinrich, B. (1979). Bumblebee Economics. bumblebees. J. Exp. Biol. 61, 219-227. Koerpertemperatur bei Muskelarbeit. Skand. Cambridge, MA: Harvard University Press. Krogh, A. and Zeuthen, E. (1941). The Archiv Physiol. 79, 193-230.

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