Discontinuous gas exchange and the significance of respiratory water loss in scarabaeine beetles
1 Spatial Physiological and Conservation Ecology Group, Department of
Zoology, University of Stellenbosch, Private Bag X1, Matieland 7602, South
Africa
2 Department of Zoology and Entomology, University of Pretoria, Pretoria
0002, South Africa
* Author for correspondence (e-mail: slchown{at}sun.ac.za)
Accepted 9 July 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: gas exchange, desiccation resistance, metabolic rate, scaling, water loss, dung beetle, Scarabaeus
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Several other avenues of investigation seem to confirm the significance of
the contribution of respiratory transpiration to total water loss.
Experimental manipulations in which spiracles are held open artificially
demonstrated that water loss rates increase dramatically if the spiracles are
kept open (Bursell, 1957;
Edney, 1977
, see also
Lighton et al., 1993
). Based
on comparative data and on laboratory selection experiments, numerous studies
have also shown or argued that metabolic rates in species or populations from
dry environments are lower than those in species or populations from more
mesic environments, thus reducing water loss under the xeric conditions
(Juliano, 1986
;
Hoffmann and Parsons, 1989a
;
Gibbs et al., 1997
;
Chown and Gaston, 1999
;
Davis et al., 2000
;
Gibbs, 2002a
;
Gibbs et al., 2003
). In
addition, large-scale comparative studies by Zachariassen and his colleagues
(Zachariassen et al., 1987
;
Zachariassen, 1996
), strongly
suggest that respiratory transpiration must account for a significant
proportion of water lost by arid-environment insects during dehydration, and
have led these authors to conclude that modification of this loss could
represent a significant fitness benefit.
By contrast, in those studies that have examined the proportional
contribution of respiratory transpiration to total water loss, the general
conclusion has been that respiratory water loss is low, contributing 3-15% of
the total, and with little relationship to the environment (mesic or xeric)
occupied by the species in question
(Hadley and Quinlan, 1993;
Lighton et al., 1993
;
Quinlan and Hadley, 1993
;
Quinlan and Lighton, 1999
).
Indeed, Hadley
(1994a
,b
)
pointed out that in the majority of species examined, respiratory water loss
constitutes such a small proportion of total water loss that it `...is
difficult to see how even major changes in its relative contribution would
affect the water status of these animals'. The importance of respiratory
water loss has been questioned by findings that insects subjected to
desiccation stress often abandon discontinuous gas exchange
(Hadley and Quinlan, 1993
;
Quinlan and Hadley, 1993
;
Chappell and Rogowitz, 2000
;
Rourke, 2000
), and that some
species from xeric areas apparently do not exhibit this gas exchange pattern
at all (Lighton and Berrigan,
1995
; Lighton,
1996
). Moreover, several studies have shown that neither a change
in gas exchange pattern nor a reduction in metabolic rate are accompanied by a
reduction in water loss (Djawdan et al.,
1997
; Williams and Bradley,
1998
; Williams et al.,
1998
; Bradley et al.,
1999
; Rourke,
2000
; Shelton and Appel,
2001a
,b
),
and that even substantial changes in metabolic rate might not markedly improve
survival time via water conservation
(Bosch et al., 2000
).
Nevertheless, the view that respiratory water loss forms an important
component of total transpiration continues to permeate the modern literature.
For example, in revisiting the comparative analysis of water loss undertaken
by Zachariassen and his colleagues, Addo-Bediako et al.
(2001) concluded that
respiratory water loss is of considerable importance in xeric insect species,
although they did not find support for reduced metabolic rate as a means by
which a reduction in transpiration might be effected. Similarly, in a
comparative analysis of water balance in Drosophila species from
mesic and xeric habitats, Gibbs et al.
(2003
) concluded that lower
rates of water loss in the xeric species are achieved primarily by reduction
in respiratory losses associated with a reduction in metabolic rate and
activity levels, and improved spiracular control. Based on investigations of
discontinuous gas exchange in beetles, Duncan and Dickman
(2001
) and Duncan et al.
(2002a
) supported the water
conservation hypothesis for the DGC because the other hypotheses seemed not to
apply to the species they investigated (see also
Vogt and Appel, 2000
). Indeed,
Duncan (2003
) went on to
conclude that every facet of the DGC can be altered (presumably in an adaptive
fashion) to effect respiratory water savings. Thus, it is clear that at
present there is little consensus regarding the significance of respiratory
water loss in insect water balance. Whilst many arguments have been raised
against its likely significance, it continues to engender support. This state
of affairs was perhaps best summed up by Quinlan and Lighton
(1999
) who argued that the
`...interrelationships between gas exchange and water balance are still
largely a matter of conjecture'.
Whilst reviewing respiratory water loss in insects, Chown
(2002) proposed several ways
in which the current polarization of findings might be overcome. Amongst
these, the most significant included a move away from the use of proportions
for expressing respiratory water loss (see also Packard and Boardman,
1988
,
1999
), the more frequent use
of comparative analyses that involve work on species in which respiratory and
cuticular transpiration can be clearly distinguished, and clear a
priori statements of the null expectation. In the latter case, arguments
regarding the proportional contribution of respiratory loss to total
transpiration, the relationship between metabolic rate and respiratory water
loss rate, and the contribution of variation in components of the DGC to water
conservation can be restated as: (1) variation in respiratory water loss is
unrelated to variation in total water loss, (2) variation in metabolic rate is
unrelated to variation in respiratory water loss rate and (3) there is no
covariation in DGC period characteristics and respiratory water loss. In
general, the alternatives to these null expectations are straightforward,
although in the case of DGC period characteristics there are two,
non-exclusive alternative hypotheses. These are that covariation between C-
and/or F-period duration and water loss rate is negative
(Lighton, 1990
;
Davis et al., 1999
), and/or
that covariation between O-period duration and water loss rate is positive
(Lighton, 1990
;
Duncan et al., 2002a
).
In this study, we examine these three major hypotheses in an analysis of
water loss in five species of Scarabaeus dung beetles that exhibit
discontinuous gas exchange (Davis et al.,
1999). We determine whether there is variation in total water loss
rate across the individuals in our sample, whether respiratory water loss
contributes significantly to this variation, whether metabolic rate and water
loss rate covary, and whether DGC period durations covary with water loss
rate. In doing so our aim is not only to investigate patterns of water loss in
these species, but also to provide an example of the type of analysis that
could be useful for overcoming the stalemate that currently reigns in the
field of respiratory water loss in insects.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Experimental design
Individuals were held at 25°C under a 12 h: 12 h L:D photoperiod for at
least 5 days before respirometry commenced. Individual beetles were starved
for 24-48 h before a trial to avoid excretion during the experiment. Each
individual was weighed prior to and after a trial using a Sartorius R 200 D
digital balance (Epsom, UK), and mean mass was used in data analyses. A single
beetle was placed in the cuvette during the morning (±10:00 h) to allow
it to settle before data measurement over the following night, when diurnal
Scarabaeini are relatively inactive (Davis,
1996,
2002
). The cuvette was placed
inside a water jacket connected to a Grant LTD20 water bath (Cambridge, UK)
that controlled the selected temperature to within ±0.2°C. The
laboratory was maintained in darkness throughout each trial.
Flow-through respirometry based on a Sable Systems (Henderson, Nevada, USA)
turnkey system was used to measure both CO2 and H2O
production (fully described in Davis et al.,
1999,
2000
). Air was passed through
columns of Drierite and soda lime to remove both water vapour and
CO2. The scrubbed air was then passed through an automated
baselining system, the 340 ml cuvette containing the beetle, and a Li-Cor
CO2/H2O Analyzer Model Li 6262 at a flow rate of 150 ml
min-1. Sable Systems DATACAN V software was used for data capture
and analysis, and all measurements were corrected to standard temperature and
pressure.
In each of the five Scarabaeus species, temperature-modulated
changes in the amounts of both CO2 and H2O production
were recorded at 4°C intervals across a temperature range from 16°C to
32°C (with the exception of S. striatus - see
Table 2). Whereas 10 or more
individuals were measured for S. westwoodi and S. rusticus,
fewer individuals were available for the other three species
(Table 2). For each individual,
measurements of CO2 and H2O release were made at 5 s
intervals during an overnight period of 9-10 h commencing at dusk (18:00-19:00
h). Periodic observations during initial respirometry work revealed that DGCs
were indicative of immobile individuals
(Davis et al., 1999), and
therefore provided standardized data for intra- and interspecific comparisons.
Where possible, DGC measurements were only entered into the analysis for data
recorded after the first 4 h, and for each DGC, measurements of both
CO2 and H2O were made over the same range of samples.
Because the DGC periods were less readily discerned in the water vapour trace
than in the CO2 recording, the water vapour data were divided into
O-period and combined Closed/Flutter (CF) period. C-period emission rate of
CO2 was very close to the baseline (see also
Davis et al., 1999
),
suggesting that there is minimal escape of gasses during the C-period,
indicating that CO2 is lost primarily through the spiracles.
However, CF-period
H2O emission
rate was well above the baseline, representing primarily cuticular water
loss.
|
For each individual, at each temperature, mean
CO2, CF-period
duration, O-period duration,
CO2 for the CF
and O periods, CO2 volume for the CF and O periods, the nadir of
H2O for the CF
period (cuticular water loss rate),
H2O for the
O-period (cuticular plus respiratory water loss rate), respiratory water loss
rate (O-period only), total water loss rate
(
H2O), volume of
cuticular water loss, volume of respiratory water loss, total water loss
volume, and proportional contribution of respiratory water loss were
calculated. The data for each individual were generally derived from the mean
data for at least four DGCs (though in some instances fewer DGCs were used),
and in all subsequent analyses these mean values for each individual were used
as the primary data. Although some authors use values from each cycle in a
discontinuous gas exchange of a single individual as primary, independent data
points (e.g. Duncan et al.,
2002a
,b
),
we consider this pseudoreplication and did not do so.
Data analysis
Generalized linear modelling (see
McCullagh and Nelder, 1989;
Quinn and Keough, 2002
) was
used to obtain best-fit models for total
H2O, respiratory
H2O and
cuticular
H2O.
The independent variables included in these models were: (1) treatment
temperature and species identity for total
H2O, to
determine if there is variation in total water loss rate amongst species; (2)
treatment temperature, log10(mass), log10(cuticular
water loss rate), and log10(spiracular water loss rate) for total
H2O, (3)
treatment temperature, log10(mass), log10(CF-period
duration), log10(O-period duration), and log10(mean
CO2) for
respiratory
H2O;
(4) treatment temperature, and log10(mass) for
log10(cuticular
H2O).
In all cases a normal distribution and identity link function were
specified, and the Akaike Information Criterion (AIC) was used to identify the
best subset of explanatory variables. In cases where the AIC was similar for
different subsets of variables, the model with the fewest variables was chosen
(Quinn and Keough, 2002).
These models were run again and Type III likelihood tests were used to confirm
the significance of each variable. Because Davis et al.
(2000
) found that wing status
(flying vs. flightless) explained much of the variation in
CO2 in these
Scarabaeus species (see also
Reinhold, 1999
;
Addo-Bediako et al., 2002
), and
because flightlessness is reputedly a means by which beetles are able to
effect a water savings (Draney,
1993
; Chown et al.,
1998
), the latter (three) analyses were repeated including a dummy
variable for wing status.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
The best-fit model for spiracular water loss rate included CF-period
duration, O-period duration, and
CO2 (AIC=-187.3,
compared to -184.8 for the full model)
(Table 4). When wing status was
considered, the best-fit model included CF-period duration, O-period duration,
CO2 and wing
status (AIC=-189.2). However, CF-period duration was not significant
(
2=2.995, P=0.08). Therefore, the best fit model
included wing status, O-period duration and
CO2
(Table 4). One explanation for
the exclusion of CF-period duration from the model including wing status is
the particularly prolonged duration of the CF period in S.
gariepinus, and to a lesser extent in S. striatus (see
Table 2).
|
In the case of cuticular water loss, mass and treatment temperature
contributed significantly to the model, as did wing status
(Table 5). To obtain an
indication of the scaling of cuticular and respiratory water loss rate, the
relationship between log10(mass) and log10(cuticular
water loss), and log10(mass) and log10(spiracular water
loss) was investigated for measurements made at 20°C (for which most data
were available) using generalized linear models. Cuticular water loss scaled
significantly (P=0.002) as mass0.721±0.234, which
is not significantly different from a value expected from geometric
considerations alone (mass0.667, t(37)=0.231,
P>0.5). Spiracular water loss scaled significantly
(P=0.0009) as mass0.531±0.160, which is also not
significantly different from a value expected from geometric considerations
alone (mass0.667, t(37)=-0.85,
P>0.4). By contrast,
CO2 scaled
significantly (P=0.0001) as mass1.284±0.160.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Perhaps unsurprisingly, both cuticular and respiratory water loss
contributed significantly to total water loss rate, in keeping with much of
the comparative literature on water balance (for reviews, see
Edney, 1977;
Wharton, 1985
;
Hadley, 1994b
;
Addo-Bediako et al., 2001
). In
other words, the first of our null hypotheses was falsified. In these beetles,
variation in respiratory water loss was related to variation in total water
loss.
Variation in spiracular water loss rate was best explained by a combination
of CF-period duration, O-period duration and
CO2. The
estimates for these parameters indicated that decreasing rates of water loss
are associated with an increase in the duration of the CF-period, a decline in
the duration of the O-period, and a decrease in metabolic rate
(Table 4). These results
provide strong support for the hypothesis that alteration of metabolic rate at
rest can be used to effect a change in water loss, as has previously been
suggested by several authors (Barnhart and
McMahon, 1987
; Zachariassen et al.,
1987
,
1988
;
Lighton and Bartholomew, 1988
;
Hoffmann and Parsons, 1989b
;
Chown and Gaston, 1999
).
Therefore, the second of our null hypotheses can be rejected.
In the context of the relationship between metabolic rate and total water
loss rate, it is important to note that total rates of water loss measured
here differed from gravimetric estimates made for two of the species for which
data are available (see Klok,
1994). This suggests that comparisons between studies using
short-term water loss rate measurements and those undertaken over longer-term
periods (e.g. Zachariassen et al.,
1987
,
1988
;
Zachariassen, 1996
;
Addo-Bediako et al., 2001
) must
be made with caution. Nonetheless, in the context of these kinds of
comparative analysis of water loss and metabolic rate, it is important to note
that in these Scarabaeus species, the relationship between the
residuals of each of the log(rate)-log(mass) relationships (see
Addo-Bediako et al., 2001
) was
positive (r2=0.97, P=0.014). This finding
provides evidence that the relationship between log(metabolic rate) and
log(water loss rate) was not simply a function of the covariation of both
variables with body mass. The same result was obtained in a multiple
regression with water loss rate and both mass and metabolic rate as
independent variables, as recommended by Freckleton
(2002
). That is, metabolic
rate was retained as a significant term (partial correlation t=4.3,
P<0.05). Indeed, although larger body size has frequently been
identified as an important means by which insects in general
(Schoener and Janzen, 1968
;
Remmert, 1981
;
Lighton et al., 1994
;
Le Lagadec et al., 1998
; but
see also Gibbs and Matzkin,
2001
; Chown and Klok,
2003
; Gibbs et al.,
2003
), and dung beetles in particular
(Chown et al., 1995
), might
alter their responses to environmental water availability, it did not enter
most of our models as a significant term. Clearly, both cuticular and
spiracular water loss rates scale with body mass, but, especially in the
latter case, body mass is much less important in explaining variation than are
other factors. Moreover, it should be kept in mind that body size can affect
desiccation resistance not only via variation in water loss rates,
but also via variation in water content
(Lighton et al., 1994
;
Chown et al., 1995
).
The inclusion of CF-period and O-period durations in the best-fit model for
spiracular water loss also suggests that modifications in the pattern of gas
exchange might be important for altering water loss rates. That is, our third
hypothesis has also been rejected. Whilst it has long been suspected that
there is covariation between gas exchange patterns and water loss rates
(Lighton, 1988a,
1990
,
1991
;
Lighton et al., 1993
;
Davis et al., 1999
;
Bosch et al., 2000
;
Duncan and Dickman, 2001
;
Duncan et al., 2002a
), few
studies have examined the relationships between DGC characteristics and
spiracular water loss (for exceptions, see
Lighton, 1992
;
Lighton et al., 1993
;
Quinlan and Lighton, 1999
).
For the most part, inferences concerning the importance of modulation of
either CF-period or O-period duration for altering spiracular water loss are
based on measurements of
CO2 only (e.g.
Bosch et al., 2000
;
Duncan, 2003
), and then rarely
involving investigations of more than one or two species (though for
exceptions, see Lighton, 1991
;
Davis et al., 1999
;
Duncan and Byrne, 2000
). By
contrast, our results provide explicit support for the idea that modulation of
DGC characteristics and metabolic rate can be used to alter water loss rate.
Moreover, these changes are in a direction that is consistent with a response
to changes in environmental water availability. That is, species from more
arid areas have lower metabolic rates, shorter O-periods and longer
CF-periods. Whilst we cannot conclude that these changes are adaptive, mostly
because the two wingless species are more closely related to each other than
they are to any of the other species (for further discussion, see
Davis et al., 2000
), our
results suggest that this is likely to be the case. In other words, the data
provide support for the proposition that by reducing the period for which
spiracles remain open, and by prolonging the duration of the closed and
flutter periods, species showing DGC can reduce respiratory water loss.
Although the contribution of the F-period to water savings hinges on whether
gas exchange takes place predominantly by convection or diffusion
(Lighton, 1988b
;
Lighton and Garrigan, 1995
;
Lighton, 1996
), it seems
likely that there would be substantial convective airflow in the F-period in
these species, because this has been found in other dung beetle species
(Chown and Holter, 2000
;
Duncan and Byrne, 2000
).
Nonetheless, the exclusion of CF-period duration from the model including wing
status suggests that alteration of CF-period duration might only be a response
to very arid conditions, rather than one found in all species, whereas all
species might modulate water loss via changes in O-period duration.
Prolonged CF-period durations in other beetle species from extremely arid
areas (Bosch et al., 2000
;
Duncan and Byrne, 2000
;
Duncan et al., 2002a
) provide
support for this contention.
Although body mass was excluded from the model used to explain respiratory
water loss, we undertook two additional analyses to investigate the scaling of
both cuticular and spiracular water loss, because scaling of these variables
has long been of interest in water balance physiology
(Kestler, 1985;
Nagy and Peterson, 1988
;
Lighton and Feener Jr, 1989
;
Lighton et al., 1994
;
Lehmann et al., 2000
).
Although several estimates of the scaling of overall water loss have been
made, ranging from 0.484 to 0.943 (Nagy
and Peterson, 1988
;
Zachariassen et al., 1988
;
Chown, 1993
;
Lighton et al., 1994
),
consensus scaling equations for respiratory and cuticular water loss in
insects have not been derived (Edney,
1977
; Arlian and Veselica,
1979
; Peters,
1983
; Wharton,
1985
; Hadley,
1994b
). In part, this must be a consequence of the difficulty of
distinguishing respiratory and cuticular water loss, and the problems of
catabolism when water loss is measured gravimetrically (for a discussion, see
Nicolson, 1980
;
Edney, 1982
;
Addo-Bediako et al., 2001
). By
contrast, the measurements of respiratory and cuticular transpiration made
here are not confounded by these problems. The scaling exponent of 0.721 for
cuticular water loss did not differ from an expectation of 0.67 based on
geometric considerations alone (as is the case for overall water flux in the
Drosophila species examined by
Lehmann et al., 2000
). This
finding does not provide support for Kestler's hypothesis
(Kestler, 1985
) that cuticular
water loss should scale as mass0.33. Kestler
(1985
) argued that because
cuticular thickness scales as mass0.33, cuticular water loss should
scale similarly. The fact that our findings and those of Lehmann et al.
(2000
) do not support this
hypothesis is perhaps not unexpected given that it is not only cuticular
thickness that determines water loss rates
(Gibbs et al., 1991
; Gibbs,
1998
,
2002b
;
Rourke, 2000
). Spiracular
water loss had a somewhat lower scaling exponent (0.531), although it did not
differ from 0.67 either. According to Kestler
(1985
), in a purely
diffusion-based system, respiratory water loss should scale as
mass0.33, whereas in a convection based system it should scale as
mass1.0. The intermediate value obtained here suggests that both
diffusive and convective water loss take place in these species.
In conclusion, we have rejected all three of our null hypotheses, thereby
providing considerable support for previous contentions that modulation of
respiratory water loss is important for water balance in insects. Moreover,
our results also provide direct, comparative evidence that in species with
discontinuous gas exchange cycles, alterations in both metabolic rate and gas
exchange pattern contribute to changes in respiratory water loss. Therefore,
our work not only provides direct evidence for several theoretically appealing
but empirically poorly supported ideas, but also joins a growing body of
evidence (e.g. Lehmann, 2001;
Gibbs et al., 2003
)
demonstrating that respiratory water loss cannot be discounted in
investigations of insect water balance. In the context of discontinuous gas
exchange cycles it also suggests that hypotheses for the origin and
maintenance of these cycles, which are predicated on water savings (the hygric
and chthonic genesis hypotheses; see
Lighton and Berrigan, 1995
;
Lighton, 1996
,
1998
), should not be discarded
just yet.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Addo-Bediako, A., Chown, S. L. and Gaston, K. J. (2001). Revisiting water loss in insects: a large scale view. J. Insect Physiol. 47,1377 -1388.[CrossRef][Medline]
Addo-Bediako, A., Chown, S. L. and Gaston, K. J. (2002). Metabolic cold adaptation in insects: a large-scale perspective. Funct. Ecol. 16,332 -338.[CrossRef]
Arlian, L. G. and Veselica, M. M. (1979). Water balance in insects and mites. Comp. Biochem. Physiol. 64A,191 -200.[CrossRef]
Barnhart, M. C. and McMahon, B. R. (1987). Discontinuous carbon dioxide release and metabolic depression in dormant land snails. J. Exp. Biol. 128,123 -138.
Bosch, M., Chown, S. L. and Scholtz, C. H. (2000). Discontinuous gas exchange and water loss in the keratin beetle Omorgus radula: further evidence against the water conservation hypothesis? Physiol. Entomol. 24,309 -314.[CrossRef]
Bradley, T. J., Williams, A. E. and Rose, M. R. (1999). Physiological responses to selection for desiccation resistance in Drosophila melanogaster. Am. Zool. 39,337 -345.
Burkett, B. N. and Schneiderman, H. A. (1974). Discontinuous respiration in insects at low temperatures: intratracheal pressure changes and spiracular valve behavior. Biol. Bull. 147,294 -310.[Medline]
Bursell, E. (1957). The effects of humidity on the activity of tsetse flies. J. Exp. Biol. 32, 42-51.
Chappell, M. A. and Rogowitz, G. L. (2000).
Mass, temperature and metabolic effects on discontinuous gas exchange cycles
in Eucalyptus-boring beetles (Coleoptera: Cerambycidae).
J. Exp. Biol. 203,3809
-3820.
Chown, S. L. (1993). Desiccation resistance in six sub-Antarctic weevils (Coleoptera: Curculionidae): humidity as an abiotic factor influencing assemblage structure. Funct. Ecol. 7, 318-325.
Chown, S. L. (2002). Respiratory water loss in insects. Comp. Biochem. Physiol. 133A,791 -804.
Chown, S. L. and Gaston, K. J. (1999). Exploring links between physiology and ecology at macro scales: the role of respiratory metabolism in insects. Biol. Rev. 74, 87-120.[CrossRef]
Chown, S. L. and Holter, P. (2000).
Discontinuous gas exchange cycles in Aphodius fossor (Scarabaeidae):
a test of hypotheses concerning origins and mechanisms. J. Exp.
Biol. 203,397
-403.
Chown, S. L. and Klok, C. J. (2003). Water balance characteristics respond to changes in body size in sub-Antarctic weevils. Physiol. Biochem. Zool., in press.
Chown, S. L., Pistorius, P. A. and Scholtz, C. H. (1998). Morphological correlates of flightlessness in southern African Scarabaeinae (Coleoptera: Scarabaeidae): Testing a condition of the water conservation hypothesis. Can. J. Zool. 76,1123 -1133.[CrossRef]
Chown, S. L., Scholtz, C. H., Klok, C. J., Joubert, F. J. and Coles, K. (1995). Ecophysiology, range contraction and survival of a geographically restricted African dung beetle (Coleoptera: Scarabaeidae). Funct. Ecol. 9, 30-39.
Davis, A. L. V. (1996). Diel and seasonal community dynamics in an assemblage of coprophagous, Afrotropical, dung beetles (Coleoptera: Scarabaeidae s. str., Aphodiidae, and Staphylinidae: Oxytelinae). J. Afr. Zool. 110,291 -308.
Davis, A. L. V. (2002). Dung beetle diversity in South Africa: influential factors, conservation status, data inadequacies and survey design. Afr. Entomol. 10, 53-65.
Davis, A. L. V., Chown, S. L., McGeoch, M. A. and Scholtz, C. H. (2000). A comparative analysis of metabolic rate in six Scarabaeus species (Coleoptera: Scarabaeidae) from southern Africa: further caveats when inferring adaptation. J. Insect Physiol. 46,553 -562.[CrossRef][Medline]
Davis, A. L. V., Chown, S. L. and Scholtz, C. H. (1999). Discontinuous gas-exchange cycles in Scarabaeus dung beetles (Coleoptera: Scarabaeidae): Mass-scaling and temperature dependence. Physiol. Biochem. Zool. 72,555 -565.[CrossRef][Medline]
Davis, A. L. V., Scholtz, C. H. and Philips, T. K. (2002). Historical biogeography of scarabaeine dung beetles. J. Biogeog. 29,1217 -1256.[CrossRef]
Djawdan, M., Rose, M. E. and Bradley, T. J. (1997). Does selection for stress resistance lower metabolic rate? Ecology 78,828 -837.
Draney, M. L. (1993). The subelytral cavity of desert tenebrionids. Florida Entomol. 76,539 -548.
Duncan, F. D. (2003). The role of the subelytral cavity in a tenebrionid beetle, Onymacris multistriata (Tenebrionidae: Adesmiini). J. Insect Physiol. 49,339 -346.[CrossRef][Medline]
Duncan, F. D. and Byrne, M. J. (2000). Discontinuous gas exchange in dung beetles: patterns and ecological implications. Oecologia 122,452 -458.[CrossRef]
Duncan, F. D. and Dickman, C. R. (2001). Respiratory patterns and metabolism in tenebrionid and carabid beetles from the Simpson Desert, Australia. Oecologia 129,509 -517.
Duncan, F. D., Krasnov, B. and McMaster, M.
(2002a). Metabolic rate and respiratory gas-exhange patterns in
tenebrionid beetles from the Negev Highlands, Israel. J. Exp.
Biol. 205,791
-798.
Duncan, F. D., Krasnov, B. and McMaster, M. (2002b). Novel case of a tenebrionid beetle using discontinuous gas exchange cycle when dehydrated. Physiol. Entomol. 27, 79-83.[CrossRef]
Edney, E. B. (1977). Water Balance in Land Arthropods. Berlin: Springer.
Edney, E. B. (1982). The truth about saturation deficiency - an historical perspective. J. Exp. Zool. 222,205 -214.
Freckleton, R. P. (2002). On the misuse of residuals in ecology: regression of residuals vs. multiple regression. J. Anim. Ecol. 71,542 -545.[CrossRef]
Gibbs, A., Fukuzato, F. and Matzkin, L. M.
(2003). Evolution of water conservation mechanisms in
Drosophila. J. Exp. Biol.
206,1183
-1192.
Gibbs, A. G. (1998). Water-proofing properties of cuticular lipids. Am. Zool. 38,471 -482.
Gibbs, A. G. (2002a). Water balance in desert Drosophila: lessons from non-charismatic microfauna. Comp. Biochem. Physiol. 133A,781 -789.
Gibbs, A. G. (2002b). Lipid melting and cuticular permeability: new insights into an old problem. J. Insect Physiol. 48,391 -400.[CrossRef][Medline]
Gibbs, A. G., Chippindale, A. K. and Rose, M. R.
(1997). Physiological mechanisms of evolved desiccation
resistance in Drosophila melanogaster. J. Exp.
Biol. 200,1821
-1832.
Gibbs, A. G. and Matzkin, L. M. (2001).
Evolution of water balance in the genus Drosophila. J.
Exp. Biol. 204,2331
-2338.
Gibbs, A. G., Mousseau, T. A. and Crowe, J. H. (1991). Genetic and acclimatory variation in biophysical properties of insect cuticle lipids. Proc. Nat. Acad. Sci. USA 88,7257 -7260.[Abstract]
Hadley, N. F. (1994a). Ventilatory patterns and respiratory transpiration in adult terrestrial insects. Physiol. Zool. 67,175 -189.
Hadley, N. F. (1994b). Water Relations of Terrestrial Arthropods. San Diego: Academic Press.
Hadley, N. F. and Quinlan, M. C. (1993).
Discontinuous carbon dioxide release in the eastern lubber grasshopper
Romalea guttata and its effect on respiratory transpiration.
J. Exp. Biol. 177,169
-180.
Hoffmann, A. A. and Parsons, P. A. (1989a). An integrated approach to environmental stress tolerance and life history variation. Desiccation tolerance in Drosophila. Biol. J. Linn. Soc. 37,117 -136.
Hoffmann, A. A. and Parsons, P. A. (1989b).
Selection for increased desiccation resistance in Drosophila
melanogaster: Additive genetic control and correlated responses for other
stresses. Genetics 122,837
-845.
Juliano, S. A. (1986). Resistance to desiccation and starvation of two species of Brachinus (Coleoptera: Carabidae) from southeastern Arizona. Can. J. Zool. 64, 73-80.
Kestler, P. (1985). Respiration and respiratory water loss. In Environmental Physiology and Biochemistry of Insects (ed. K. H. Hoffmann), pp.137 -186. Berlin: Springer.
Klok, C. J. (1994). Desiccation resistance in dung-feeding Scarabaeinae. MSc thesis, University of Pretoria.
Klok, C. J., Mercer, R. D. and Chown, S. L.
(2002). Discontinuous gas exchange in centipedes and its
convergent evolution in tracheated arthropods. J. Exp.
Biol. 205,1031
-1036.
Le Lagadec, M. D., Chown, S. L. and Scholtz, C. H. (1998). Desiccation resistance and water balance in southern African keratin beetles (Coleoptera, Trogidae): the influence of body size, habitat and phylogeny. J. Comp. Physiol. B 168,112 -122.[CrossRef]
Lehmann, F.-O. (2001). Matching spiracle
opening to metabolic need during flight in Drosophila.
Science 294,1926
-1929.
Lehmann, F.-O., Dickinson, M. H. and Staunton, J.
(2000). The scaling of carbon dioxide release and respiratory
water loss in flying fruit flies (Drosophila spp.). J.
Exp. Biol. 203,1613
-1624.
Levy, R. I. and Schneiderman, H. A. (1966). Discontinuous respiration in insects - IV. Changes in intratracheal pressure during the respiratory cycle of silkworm pupae. J. Insect Physiol. 12,465 -492.[Medline]
Lighton, J. R. B. (1988a). Discontinuous CO2 emission in a small insect, the formicine ant Camponotus vicinus. J. Exp. Biol. 134,363 -376.
Lighton, J. R. B. (1988b). Simultaneous measurement of oxygen uptake and carbon dioxide emission during discontinuous ventilation in the tok-tok beetle, Psammodes striatus. J. Insect Physiol. 34,361 -367.
Lighton, J. R. B. (1990). Slow discontinuous ventilation in the Namib dune-sea ant Camponotus detritus (Hymenoptera, Formicidae). J. Exp. Biol. 151, 71-82.
Lighton, J. R. B. (1991). Ventilation in Namib desert tenebrionid beetles: mass scaling and evidence of a novel quantized flutter-phase. J. Exp. Biol. 159,249 -268.
Lighton, J. R. B. (1992). Direct measurement of
mass loss during discontinuous ventilation in two species of ants.
J. Exp. Biol. 173,289
-293.
Lighton, J. R. B. (1994). Discontinuous ventilation in terrestrial insects. Physiol. Zool. 67,142 -162.
Lighton, J. R. B. (1996). Discontinuous gas exchange in insects. Annu. Rev. Entomol. 41,309 -324.[CrossRef][Medline]
Lighton, J. R. B. (1998). Notes from the underground: towards ultimate hypotheses of cyclic, discontinuous gas-exchange in tracheate arthropods. Am. Zool. 38,483 -491.
Lighton, J. R. B. and Bartholomew, G. A. (1988). Standard energy metabolism of a desert harvester ant, Pogonomyrmex rugosus: effects of temperature, body mass, group size, and humidity. Proc. Natl. Acad. Sci. USA 85,4765 -4769.[Abstract]
Lighton, J. R. B. and Berrigan, D. (1995). Questioning paradigms: caste-specific ventilation in harvester ants, Messor pergandei and M. julianus (Hymenoptera: Formicidae). J. Exp. Biol. 198,521 -530.[Medline]
Lighton, J. R. B. and Feener, D. H., Jr (1989). Water-loss rate and cuticular permeability in foragers of the desert ant Pogonomyrmex rugosus. Physiol. Zool. 62,1232 -1256.
Lighton, J. R. B. and Garrigan, D. (1995). Ant breathing: Testing regulation and mechanism hypotheses with hypoxia. J. Exp. Biol. 198,1613 -1620.[Medline]
Lighton, J. R. B., Garrigan, D. A., Duncan, F. D. and Johnson,
R. A. (1993). Spiracular control of respiratory water loss in
female alates of the harvester ant Pogonomyrmex rugosus.
J. Exp. Biol. 179,233
-244.
Lighton, J. R. B., Quinlan, M. C. and Feener, D. H., Jr (1994). Is bigger better? Water balance in the polymorphic desert harvester ant Messor pergandei. Physiol. Entomol. 19,325 -334.
Loveridge, J. P. (1968). The control of water loss in Locusta migratoria migratorioides R. & F. II. Water loss through the spiracles. J. Exp. Biol. 49, 15-29.
McCullagh, P. and Nelder, J. A. (1989). Generalized Linear Models. London: Chapman and Hall.
Nagy, K. A. and Peterson, C. C. (1988). Scaling of water flux rate in animals. Univ. Californ. Publ. Zool. 120,1 -172.
Nicolson, S. W. (1980). Water balance and osmoregulation in Onymacris plana, a tenebrionid beetle from the Namib Desert. J. Insect Physiol. 26,315 -320.
Packard, G. C. and Boardman, T. J. (1988). The misuse of ratios, indices, and percentages in ecophysiological research. Physiol. Zool. 61,1 -9.
Packard, G. C. and Boardman, T. J. (1999). The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comp. Biochem. Physiol. 122A,37 -44.
Peters, R. H. (1983). The Ecological Implications of Body Size. Cambridge: Cambridge University Press.
Quinlan, M. C. and Hadley, N. F. (1993). Gas exchange, ventilatory patterns, and water loss in two lubber grasshoppers: quantifying cuticular and respiratory transpiration. Physiol. Zool. 66,628 -642.
Quinlan, M. C. and Lighton, J. R. B. (1999). Respiratory physiology and water relations of three species of Pogonomyrmex harvester ants (Hymenoptera: Formicidae). Physiol. Entomol. 24,293 -302.[CrossRef]
Quinn, G. P. and Keough, M. J. (2002). Experimental Design and Data Analysis for Ecologists. Cambridge: Cambridge University Press.
Reinhold, K. (1999). Energetically costly behaviour and the evolution of resting metabolic rate in insects. Funct. Ecol. 13,217 -224.[CrossRef]
Remmert, H. (1981). Body size of terrestrial arthropods and biomass of their populations in relation to the abiotic parameters of their milieu. Oecologia 50, 12-13.
Rourke, B. C. (2000). Geographic and
altitudinal variation in water balance and metabolic rate in a California
grasshopper, Melanoplus sanguinipes. J. Exp.
Biol. 203,2699
-2712.
Schoener, T. W. and Janzen, D. H. (1968). Notes on environmental determinants of tropical versus temperate insect size patterns. Am. Nat. 102,227 -224.
Scholtz, C. H. (1989). Unique foraging behaviour in Pachysoma: an adaptation to arid conditions. J. Arid Environ. 16,305 -313.
Shelton, T. G. and Appel, A. G. (2001a). Carbon dioxide release in Coptotermes formosanus Shiraki and Reticulitermes flavipes (Kollar): effects of caste, mass, and movement. J. Insect Physiol. 47,213 -224.[CrossRef][Medline]
Shelton, T. G. and Appel, A. G. (2001b). Cyclic CO2 release and water loss in alates of the eastern subterranean termite (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Amer. 94,420 -426.
Vogt, J. T. and Appel, A. G. (2000). Discontinuous gas exchange in the fire ant, Solenopsis invicta Buren: caste differences and temperature effects. J. Insect Physiol. 46,403 -416.[CrossRef][Medline]
Wharton, G. W. (1985). Water balance of insects. In Comparative Insect Biochemistry, Physiology and Pharmacology, vol. 4 (ed. G. A. Kerkut and L. I. Gilbert), pp. 565-601. Oxford: Pergamon Press.
Williams, A. E. and Bradley, T. J. (1998). The
effect of respiratory pattern on water loss in desiccation-resistant
Drosophila melanogaster. J. Exp. Biol.
201,2953
-2959.
Williams, A. E., Rose, M. R. and Bradley, T. J.
(1998). Using laboratory selection for desiccation resistance to
examine the relationship between respiratory pattern and water loss in
insects. J. Exp. Biol.
201,2945
-2952.
Zachariassen, K. E. (1996). The water conserving physiological compromise of desert insects. Eur. J. Entomol. 93,359 -367.
Zachariassen, K. E., Andersen, J., Kamau, J. M. Z. and Maloiy, G. M. O. (1988). Water loss in insects from arid and humid habitats in East Africa. Acta Entomol. Bohemoslov. 85, 81-93.
Zachariassen, K. E., Anderson, J., Maloiy, G. M. O. and Kamau, J. M. Z. (1987). Transpiratory water loss and metabolism of beetles from arid areas in East Africa. Comp. Biochem. Physiol. 86A,403 -408.[CrossRef]
Zera, A. J. and Denno, R. F. (1997). Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42,207 -231.[CrossRef]