INSECT FLIGHT TAKES OFF
Arizona State University
University of California, Santa Barbara
j.harrison{at}asu.edu
suarez{at}lifesci.ucsb.edu
This 1951 JEB classic paper, written at the dawn of the Golden Age of
biology by Viking physiologists August Krogh and Torkel Weis-Fogh, was a
collaboration between two men at opposite ends of their careers
(Krogh and Weis-Fogh, 1951).
August Krogh, the only comparative respiratory physiologist to earn a Nobel
Prize, mentored Weis-Fogh during the last years of his life, and died before
the publication of this paper. Among biologists, Krogh is most famous for a
concept that is widely applied even today (Editorial, Nature Genetics
34, 345-346, 2003); that
for a large number of problems, nature has provided an animal of choice on
which it can be most easily studied. This was only Torkel Weis-Fogh's third
paper in a series that have all become classics in the fields of flight
physiology and biomechanics. Weis-Fogh (1949) had previously shown that it was
possible to induce locusts to fly for long periods of time on a tether by
stimulating sensilla on the head with a jet of air. The 1951 paper combined
Weis-Fogh's tethered flight technique with August Krogh's expertise in
respirometry to provide the first measures of metabolic rate and respiratory
quotient in a flying locust. Weis-Fogh's research in Krogh's laboratory was
made possible by a grant from London's Anti-Locust Research Center,
demonstrating that then, as today, potential practical benefit can fuel basic
research.
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The composition of metabolic fuels is such that the oxidation of a given
amount of carbohydrate produces the same amount of CO2 as the
O2 consumed, while fat oxidation yields a ratio of CO2
to O2 of 0.7. Thus, the ratio of the steady-state rate of
CO2 production to O2 consumption by animals, i.e. the
respiratory quotient, can be used as an index of the nature of the fuel(s)
used. Another important scientific finding reported in this paper was that,
unlike all prior studies of insect flight, the respiratory quotient of flying
locusts was less than 1, and tended to decline with time in flight. Up to the
publication of this paper, respiratory quotient had only been measured for
bees and fruitflies, which had been shown to utilize carbohydrates as the
primary fuel for flight. This paper provided the first evidence (later
confirmed, by Jutsum and Goldsworthy,
1976) that fat was the primary fuel in long-term locust flight.
Since then, many investigators have used respirometric and biochemical methods
to study temporal changes in fuel use by insects and the diversity of fuel use
among species. The fact that the fuel used to support flight seems to vary
more with phylogenetic history than ecology/life history remains an
understudied problem in this field.
Equally interesting is the, as yet, unresolved finding in this paper of
elevated gas exchange rates for 1-2 h after flight. The study of `oxygen debt'
was popular when this paper was published, and new insights into this topic
continue to emerge (Pinz and Portner,
2003). In the 1951 paper, Krogh and Weis-Fogh referred to this
elevated post-exercise oxygen consumption as `oxygen debt', but suggest that
it is not due to lack of oxygen in the flight muscle. However, subsequent work
has confirmed that flight metabolism is completely aerobic in sustained insect
flight. This elevated post-flight gas exchange is unlikely to be due simply to
passively declining thoracic temperature, which should occur a few minutes
after landing. Are we observing the slow removal of neurohormonal factors
(e.g. octopamine; Orchard et al.,
1993
) that elevate tissue metabolic rates, and perhaps spontaneous
behavior? What portion of these represent the costs of resynthesizing the
fuels catabolized in the previous flight? More than half a century later,
these data could still provide grist for a grant application!
Studies of animal flight continue to address fundamental problems and
remain one of the most vibrant areas of experimental biology. Biomechanists
use high-speed video, physical models and advanced theory to understand how
animals fly and steer (Sherman and
Dickinson, 2004; Usherwood and
Ellington, 2002
); this area now seems poised to provide the
biological inspiration for engineers to design minute flying robots. Muscle
physiologists are now able to go into insect thoraxes to directly measure
stress, strain, frequency and oxygen consumption, allowing the estimation of
power input, output and efficiency of active muscles
(Josephson et al., 2001
).
Pathway flux rates and mitochondrial electron transfer rates in individual
flying insects have been examined to yield insights into how insects achieve
the highest metabolic rates known in the animal kingdom
(Suarez et al., 2000
). A whole
arsenal of molecular techniques is now available to study the flight muscle
contractile machinery as well as membrane ion channels and pumps
(Vigoreaux, 2001
). The
evolution of insect flight itself is being examined
(Marden and Thomas, 2003
). The
great experimental biologists, August Krogh and Torkel Weis-Fogh provided
large shoulders on which many must stand well into the future.
Footnotes
A PDF file of the original paper can be accessed online: http://jeb.biologists.org/cgi/content/full/207/19/3251/DC1
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