Intra-individual variation allows an explicit test of the hygric hypothesis for discontinuous gas exchange in insects
Caroline M. Williams
Shannon L. Pelini
Jessica J. Hellmann
Brent J. Sinclair
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Intra-individual variation
allows an explicit test of
the hygric hypothesis for
discontinuous gas
exchange in insects
Caroline M. Williams1, Shannon L. Pelini2,,
Jessica J. Hellmann2 and Brent J. Sinclair1,*
1Department of Biology, University of Western Ontario, London,
ON N6A 5B7, Canada
2Department of Biological Sciences, University of Notre Dame,
Notre Dame, IN 46556, USA
*Author for correspondence ().
Present address: Harvard Forest, Harvard University, Petersham,
MA 01366, USA
The hygric hypothesis postulates that insect
discontinuous gas exchange cycles (DGCs) are an
adaptation that reduces respiratory water loss
(RWL), but evidence is lacking for reduction of
water loss by insects expressing DGCs under
normal ecological conditions. Larvae of Erynnis
propertius (Lepidoptera: Hesperiidae) naturally
switch between DGCs and continuous gas
exchange (CGE), allowing flow-through
respirometry comparisons of water loss between the
two modes. Water loss was lower during DGCs
than CGE, both between individuals using
different patterns and within individuals using both
patterns. The hygric cost of gas exchange (water
loss associated with carbon dioxide release) and
the contribution of respiratory to total water
loss were lower during DGCs. Metabolic rate
did not differ between DGCs and CGE. Thus,
DGCs reduce RWL in E. propertius, which is
consistent with the suggestion that water loss
reduction could account for the evolutionary
origin and/or maintenance of DGCs in insects.
1. INTRODUCTION
Discontinuous gas exchange cycles (DGCs) have
evolved independently at least five times in insects
(Marais et al. 2005). The evolutionary pressures that
lead to DGCs are debated (Chown et al. 2006).
DGCs consist of three phases: closed phase during
which spiracles are closed and there is no external
gas exchange; flutter phase where spiracles rapidly
open and close, allowing bulk inflow of air, and open
phase where spiracles are open to allow unrestricted
gas exchange (Chown et al. 2006).
Three main adaptive hypotheses have been
proposed to explain the origin and maintenance of
DGCs (Chown et al. 2006). The hygric hypothesis
contends that DGCs have evolved to limit respiratory
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2009.0803 or via http://rsbl.royalsocietypublishing.org.
water loss (RWL) by maximizing the time that the
spiracles are closed, and minimizing water efflux due
to bulk inward convection in the F-phase (Chown
et al. 2006). The chthonic hygric hypothesis
(Lighton & Berrigan 1995) states that DGCs
originated in insects inhabiting hypoxic and hypercapnic
(primarily underground) environments to increase O2
and CO2 diffusion gradients, with coincidental water
savings. The oxidative damage hypothesis (Hetz &
Bradley 2005) suggests that DGCs minimize oxidative
damage during periods of low metabolic demand, by
maintaining low tracheal PO2 while retaining delivery
capacity during periods of high metabolic demand
(e.g. flight).
Here, we focus on the water retention benefits of
DGCs, primarily addressing the hygric hypothesis.
We note the difficulty in distinguishing the hygric
and chthonic hygric hypotheses based on water loss,
but the hygric hypothesis may be rejected
independently of the chthonic and oxidative damage
hypotheses since CO2 and O2 partial pressures are
central to the latter (Chown et al. 2006). The hygric
hypothesis predicts that (i) water lost per CO2 released
will be lower for insects using DGCs (see also Lighton &
Turner 2008) and (ii) DGCs will decrease RWL.
Measurement of water loss within DGCs shows that
RWL is greater when the spiracles are open (see
Chown 2002). DGCs are longer in species from xeric
environments (White et al. 2007), while cyclic and
continuous patterns are more prevalent in mesic
habitats (Marais et al. 2005). RWL was lower in individual
ants that did not express DGCs; however, those
individuals also had lower metabolic rates (Gibbs &
Johnson 2004). Manipulation of environmental
variables can force insects to abandon DGCs (e.g.
Lighton & Turner 2008; Terblanche et al. 2008), but
to our knowledge there have been no comparisons of
RWL in individuals that use both DGCs and
continuous gas exchange (CGE) under ecologically relevant
conditions.
Erynnis propertius (Lepidoptera: Hesperiidae)
overwinter as quiescent late-instar larvae in rolls of dry
oak leaves (Prior et al. 2009). Quiescent larvae
probably experience desiccation during the overwintering
period as no feeding occurs. Under benign conditions,
individuals use both DGCs and CGE, allowing a direct
comparison of water loss rates both between an (...truncated)