The terrestrial dominance of insects is attributed mainly to
their ability, amongst other adaptations, to resist desiccation
through their respiratory systems (Villani et al., 1999).
However, despite many years of investigation (Wigglesworth,
1965), there is still uncertaintity as to exactly how gas and
water move through this system of spiracular openings and
tracheae (Wasserthal, 1996). Cockroaches and locusts pass
inspired air from the anterior spiracles, through longitudinal
trunks that connect the segmental tracheae and out through the
more posterior abdominal spiracles, generating a flow of fresh
air through the body (Miller, 1982). Lepidopteran pupae show
similar patterns of respiration (Schneiderman, 1960), and some
species may be able to control the actions of individual
spiracles (Slama, 1988, 1999).
Retrograde respiratory airflow is presumed to be typical for
all insects (Hadley, 1994; Lighton, 1996), and expelling air
into a sealed space below the elytra is assumed to be an
adaptation, found in many species of wingless beetle
(Cloudsley-Thompson, 1964; Ahearn, 1970; Draney, 1993), to
an arid habitat. Because the cavity maintains its air at a high
humidity, water loss during respiration should be reduced
because the tracheae will not be exposed to dry air. However,
the validity of this hypothesis requires an anterior-to-posterior
flow of respiratory gases through the body and differential
control of the spiracles, neither of which has previously been
demonstrated in these insects (Hadley, 1994).
Spiracular control appears to be most precise in insects that
inhabit dry environments, where they limit water loss by
opening their spiracles for only limited periods during a
discontinuous gas-exchange cycle (DGC) (for reviews, see
Kestler, 1985; Lighton, 1994, 1996; Wasserthal, 1996). The
DGC is a cyclic discontinuity in external gas exchange that
typically consists of three periods (Miller, 1981; Kestler,
1985). There is a closed (C) period, during which the spiracles
are shut, preventing both respiratory water loss and gas
exchange. Oxygen levels in the tracheae drop, while CO
2
is
largely buffered in the tissues and haemolymph. This is
followed by the flutter (F) period, during which slight,
intermittent opening of the spiracles allows some normoxic O
2
uptake through the spiracles by diffusion and convection, but
little CO
2
or water vapour is lost. The final period, the CO
2
burst (B) period, is triggered when the accumulation of CO
2
from respiring tissues causes some or all of the spiracles to
open widely. Rapid unloading of CO
2
should minimise the
time that the spiracles are open and therefore reduce water
vapour loss. However, the role of the DGC as a water-saving
2489 The Journal of Experimental Biology 205, 2489–2497 (2002)
Printed in Great Britain © The Company of Biologists Limited 2002
JEB4059
The sealed subelytral cavity of many flightless beetle
species is widely acknowledged to be an adaptation to
water saving in arid-habitat species. However, this
hypothesis relies on the acceptance of two largely untested
assumptions: (i) that the movement of respiratory gases is
unidirectional from anterior to posterior and (ii) that the
coordinated action of the spiracles directs this flow. We
tested these assumptions by simultaneously measuring
CO
2
and O
2
exchange at the anterior mesothorax,
independently of gas exchange in the posterior body,
which included the subelytral cavity, of a large apterous
beetle, Circellium bacchus. Flow-through respirometry
revealed a marked discontinuous gas-exchange cycle
(DGC) pattern from the anterior half of the body. Very
little CO
2
was released from the posterior body, where the
DGC was not apparent. Labelled air was shown to flow
forwards from the posterior to the anterior body.
Individual sampling from the mesothoracic spiracles
revealed that the right mesothoracic spiracle, lying outside
the elytral cavity, is the primary route for respiratory gas
exchange in C. bacchus at rest. This discovery necessitates
a reassessment of the currently assumed role of the
subelytral cavity in water conservation and is, to our
knowledge, the first demonstration of forward airflow
associated with the unilateral use of a single thoracic
spiracle for respiration in an insect.
Key words: Circellium bacchus, discontinuous gas exchange cycle,
respiration, spiracle, Scarabaeidae, dung beetle, subelytral cavity.
Summary
Introduction
Respiratory airflow in a wingless dung beetle
Frances D. Duncan
1,
* and Marcus J. Byrne
2
1
School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown 2193,
South Africa and
2
Ecophysiological Studies Research Programme, School of Animal, Plant and Environmental
Sciences, University of the Witwatersrand, Johannesburg, Wits 2050, South Africa
*e-mail: duncanfd@physiology.wits.ac.za
Accepted 8 May 2002