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Oecologia (2000) 122:452–458
© Springer-Verlag 2000
Frances D. Duncan · Marcus J. Byrne
Discontinuous gas exchange in dung beetles:
patterns and ecological implications
Received 4 August 1999 / Accepted: 7 October 1999
Abstract This study correlates a distinctive pattern of
external gas exchange, referred to as the discontinuous
gas exchange cycle (DGC), observed in the laboratory,
with habitat associations of five species of telecoprid
dung beetles. The beetles were chosen from a variety of
habitats that would be expected to present different
amounts of water stress. All five species exhibited DGC.
Sisyphus fasciculatus has been recorded only in woodland areas, and does not have strict spiracular control
during its DGC. Anachalcos convexus and Scarabaeus
rusticus are associated with open mesic habitats. Both
species exhibit a distinct DGC, previously found in some
other insect species, but intermediate within this study
group. Sc. flavicornis and Circellium bacchus are typically found in arid regions, and have the most unusual
form of DGC, with spiracular fluttering during the burst
phase. These results support the hypothesis that spiracular fluttering reduces respiratory water loss. From
this study we conclude that the DGC is an ancestral adaptation, most probably as a result of anoxic environments in underground burrows, but that spiracular control is enhanced to reduce respiratory water loss in beetle
species that live in arid habitats.
Key words Telecoprid · Respiration · Discontinuous gas
exchange cycle · Habitat association · Scarabaeinae
F.D. Duncan (✉)
Department of Physiology, Faculty of Health Sciences,
University of the Witwatersrand, 7 York Road,
Parktown 2193, South Africa
e-mail: [email protected]
Fax: +27-11-6432765
M.J. Byrne
Department of Zoology,
Ecophysiological Studies Research Programme,
University of the Witwatersrand,
Johannesburg, Wits 2050, South Africa
Introduction
Recent studies have shown that several adult insect species (e.g. ants: Lighton 1988a, 1990; Lighton and Wehner 1993; beetles: Bartholomew et al. 1985; Lighton
1985, 1988b, 1991a; a mutillid wasp: Duncan and Lighton 1997; and grasshoppers: Hadley 1994), exhibit a
distinctive pattern of external gas exchange referred to
as the discontinuous gas exchange cycle (DGC; for review see Lighton 1994, 1996). Yet, despite its apparently widespread occurrence, the advantages and evolutionary origins of this type of respiration are still under
debate (Lighton and Berrigan 1995; Hadley 1994). As
many of the species that show DGC (sensu Lighton
1996), are from arid regions (e.g. Namib desert dune
ant, Camponotus detritus, Lighton 1990, and Namib
tenebrionid beetles, Bartholomew et al. 1985), it is assumed to be an adaptive behaviour driven by the need to
minimise respiratory water loss. Alternatively, the main
evolutionary force for the origin of DGC may be
chthonic, derived from respiratory constraints in underground conditions characterised by hypercapnia and
hypoxia. Dung beetles exemplify insects in which one
or both of these selection pressures may operate during
their lifespan. This study attempts to correlate observed
behaviours and habitat associations of telecoprid beetles
with DGC parameters measured in the laboratory, and
draw some conclusions about the origin of this behaviour in the Scarabaeinae.
The DGC is a cyclic discontinuity in external gas exchange previously referred to as discontinuous ventilation cycles. This discontinuous gas exchange typically
consists of three phases (Miller 1981; Kestler 1985;
Sláma 1988). In the closed phase the spiracles are shut,
which inhibits respiratory water loss, and negligible external gas exchange takes place. This is followed by the
flutter phase, during which slight opening of the spiracles on an intermittent basis allows some O2 to enter the
tracheoles, but little CO2 or water vapour is lost. Finally,
in the open or ventilation phase, accumulation of CO2
from respiring tissues triggers some or all of the spira-
453
Fig. 1 Distributions of the study species in South Africa and Namibia. Anachalcos convexus, Scarabaeus rusticus, Sc. flavicornis
and Circellium bacchus data from BioMap (SA), supplied by S.
Koch of the Conservation Planning Unit (University of Pretoria,
South Africa); Sisyphus fasciculatus data from Paschalidis (1974)
cles to open widely, resulting in the rapid release of CO2
and water vapour to the atmosphere.
Telecoprid (ball-rolling) dung beetles are abundant in
Southern Africa (Tribe 1976; Doube 1991), and some
species show marked habitat associations with soil type,
vegetation type and dung type (Doube 1983; Osberg and
Hanrahan 1992; Osberg et al. 1993). The ball-rolling
habit is thought to have evolved in response to competition for space beneath dung pats (Bernon 1981), and
saprophagy is considered to be the ancestral condition
within the Scarabaeidae. This type of feeding stimulated
the evolution of the underground nesting behaviour typical of dung beetles, probably to protect the food mass
and create conditions suitable for symbiotic microbial
growth (Cambefort 1991a). Coprophagy emerged later,
in conjunction with the explosive radiation of the mammals at the beginning of the Tertiary (Cambefort 1991b).
Both of these adaptations would have exerted selection
pressure on the Scarabaeidae, to deal with water stress
while foraging for herbivore dung by flight in open
grasslands, and in response to anoxic conditions known
to exist in dung pats (Holter 1991), and assumed to exist
in underground burrows. Telecoprids usually search for
dung by cruise flight (Cambefort and Hanski 1991), flying directly onto the pat, or walking in the last few metres. Ball-making, when the beetles are either immersed
in the dung or exposed to the elements, may take minutes (Tribe 1976), or hours (Osberg 1988). Ball-rolling is
fairly rapid and positively related to body temperature
(Heinrich and Bartholomew 1979), but may still require
hours of exposure to ambient humidities. When not actively foraging, most beetles will spend extended periods
underground. All Afrotropical Scarabaeidae show strong
seasonal activity, usually linked to rainfall (Davis 1995,
1996). What conditions they experience during periods
of inactivity is unknown, but are likely to be anoxic to
some degree, particularly if they overwinter as adults in
a sealed brood ball. Nesting or feeding beetles may only
spend a few days underground, feeding on or shaping a
dung ball. However, females of some species such as Circellium bacchus (Fabricius), may spend extended periods below ground, tending their single brood ball. This
behaviour is likely to reduce water stress, at the cost of
increasing anoxia.
The study beetles were chosen from a variety of habitats that would be expected to present different water
stress. Sisyphus fasciculatus Boheman has a restricted
distribution in wooded areas of the eastern lowveld region, while Anachalcos convexus Boheman and Scarabaeus rusticus Boheman have a broader eastern distribution and can be found associated with open and shaded
habitats (Fig. 1). Both Sc. flavicornis Boheman and C.
bacchus are found in more arid regions. Sc. flavicornis,
typical of the subgenus Scarabaeoulus, is confined largely to the drier north western Cape Province (Tribe 1976),
while C. bacchus is found in a few restricted populations
in the eastern Cape. This may be a relic population of a
larger distribution of this monospecific genus (Ferreira
1972; Chown et al. 1995); however, its apterous condition and large size is an adaptation to more arid habitats
(Klok 1994).
Although dung beetles may date back to the late Mesozoic, their current biogeography reflects more recent
events of the Miocene to Pleistocene epochs, and 5000
years may have been sufficient to develop reproductively
isolated species (Cambefort 1991b). Therefore, it is not
surprising to find taxa of different ages and origins coexisting in the same geographical region. Table 1 shows the
habitat associations and other characteristics of the experimental species, which are distributed between an ancient tribe (Canthonini; two species), an intermediate
tribe (Scarabaeini; two species), and a modern tribe
(Sisyphini; one species). The classification used here is
based on Cambefort (1991a).
Table 1 Phylogenetic and ecological characteristics of the five telecoprid Scarabaeidae considered in this study
Species
Tribe
Antiquity
Flight
Diel activity
Habitat
Sisyphus fasciculatus Boheman
Scarabaeus rusticus Boheman
Anachalcos convexus* Boheman
Scarabaeus flavicornis Boheman
Circellium bacchus* (Fabricius)
Sisyphini
Scarabaeini
Cathonini
Scarabaeini
Cathonini*
New
Intermediate
Old
Intermediate
Old
Yes
Yes
Yes
Yes
No
Diurnal
Diurnal
Nocturnal
Nocturnal
Diurnal
Mesic, shade
Mesic, open
Mesic, open
Arid, open
Arid, open
Genera marked with an asterisk are endemic to the Afrotropical region (Cambefort 1991b)
454
It is hypothesised that if DGC is the ancestral condition in the Scarabaeinae it would have evolved in response to anoxic conditions in either dung pats or burrows, and would be found in all of the tribes examined.
If however, it is a more derived behaviour, then it would
be expected to be found only in the more modern species. If water saving is responsible for DGC patterns in
dung beetles then the species associated with drier habitats would be expected to exhibit the most pronounced
DGC behaviour regardless of their phylogenetic affiliations.
Materials and methods
Organisms
The beetles were collected by means of baited pitfall traps (Doube
and Giller 1990), and housed in 10-l bins half filled with soil, in
an insectary at 25°C with a 14:10 h light:dark cycle. Beetles were
fed fresh cow dung weekly, and survived well for several months
under laboratory conditions. All beetles were tested within
2 months of collection.
Respirometry
A flow-through respirometry system, described by Lighton
(1991b), was used to measure CO2 emission of inactive beetles.
The system employed a Licor CO2 analyser, respirometers of fixed
volume, a computerised data acquisition system and a constant
mass flow rate. Measurements were made on individual beetles
that were initially weighed to ±0.1 mg (Precisa 160A balance).
The incurrent air stream was scrubbed of H2O and CO2 by a Drierite/Ascarite column and a constant flow of 200 ml min–1 (Sierra
Instruments mass flow meter) of air was drawn over individual
beetles for between 30–60 min. Readings of the amount of CO2
produced were taken every 2 s. The beetles were observed to ensure that they remained stationary during sampling. The respirometry chambers ranged in size from 25 ml to 250 ml, depending on
the size of the beetle. All beetles were measured in an incubator
maintained at a temperature of 20°C.
To convert V̇CO2 to metabolic rate (measured in energy units
of W kg–1) the respiratory quotient (RQ) was assumed to be 0.8,
which had been previously determined for Psammodes striatus
(Coleoptera: Tenebrionidae, Lighton 1988b) and S. fasciculatus
(F.D. Duncan, unpublished work). An RQ of 0.8 gives an energy
equivalent of 24.5 J ml–1 CO2 (Schmidt-Nielsen 1980). This value
was used to express metabolic rate in terms of energy.
Statistics
All means are reported with the standard deviation (SD) and sample size (n). Analysis of variance and Tukey’s multiple range test
was used to compare the ventilation characteristics of the dung
beetles (Zar 1984).
Results
Discontinuous gas exchange cycle
The discontinuous ventilation patterns exhibited by the
inactive dung beetles were all markedly different from
each other. Figures 2 and 3 show a typical recording obtained for each species. All five species show a form of
Fig. 2 Recording of CO2 emission in individuals of S. fasciculatus (mass 0.144 g), Sc. rusticus (mass 0.68 g) and A. convexus
(mass 1.156 g)
DGC. S. fasciculatus (Fig. 2), has a long burst phase
with the spiracles open in an uncoordinated fashion. The
spiracles do not appear to shut completely during the
closed phase, which allows some CO2 to be emitted. Although discontinuous CO2 release is seen, the spiracles
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Fig. 3 Recording of CO2 emission in individuals of Sc. flavicornis
(mass, 0.379 g) and C. bacchus (mass, 5.471 g)
do not exhibit the same degree of control shown by the
other beetles in this study. Both Sc. rusticus (Fig. 2), and
A. convexus (Fig. 2), exhibit a well-defined DGC, as
found in some other adult insects. There is a clear burst
phase, followed by a complete closing of the spiracles.
In both traces there are signs of a flutter phase before the
burst phase. Sc. flavicornis (Fig. 3), also exhibits a clear
DGC, but with a distinct closed phase without fluttering
of the spiracles, prior to the burst phase. Fluttering of the
spiracles takes place during the burst phase. The same
type of spiracular fluttering is seen within the burst
phase of C. bacchus (Fig. 3). This fluttering in the burst
phase has not been reported on for any insect DGC so far
studied.
Sc. flavicornis showed the longest interval between
burst peaks. However, C. bacchus probably has the longest interval, but individuals of this species remained inactive within the experimental setup for short time periods only. Consequently, it was not possible to get several
CO2 bursts from one beetle. In the few traces obtained
with more than one peak, the interburst interval was
greater than 15 min. In the four other species the DGC
frequency was found to be mass-independent.
The characteristics of these ventilation cycles are
summarized in Table 2. There is slightly less variability
in the emission rate of CO2 in these beetles, shown by
the coefficient of variability (SD/mean), than is generally
found in discontinuously ventilating arthropods (range
2–3, Lighton 1990).
From Table 2 it is clear that the ventilation characteristics of C. bacchus are different from those of the other
beetles species. The rate of CO2 emission (ml mg–1 h–1)
and burst CO2 emission (µl g–1 h–1) are significantly lower than that found in the other study species, and the time
that the spiracles are open (burst length) is significantly
Table 2 Characteristics (mean±SD) of the discontinuous gas exchange cycle (DGC) in telecoprid beetles. The sample size is the
number of beetles measured, each representing the mean of 2–10
measurements. Means in a row followed by the same letter are not
significantly different (P<0.05; ANOVA with Tukey’s multiple
range test)
Species
S. fasiculatus
Sc. rusticus
A. convexus
Sc. flavicornis
C. bacchus
Mass (g)
0.136±0.012
0.564±0.131
1.421±0.35
0.322±0.053
7.285±2.93
n
6
6
5
12
7
Rate of CO2 emission:
V̇CO2 (ml h–1)
V̇CO2 (ml g–1 h–1)
0.038±0.009a
0.276±0.059a
0.092±0.069a
0.152±0.092b
0.156±0.057a
0.111±0.032b
0.049±0.015a
0.157±0.041b
0.407±0.204b
0.051±0.019c
Coefficient of variation
0.77
1.76
1.22
1.35
1.73
Rate of burst CO2 emission:
Burst V̇CO2 (µl g–1)
Burst V̇CO2 (µl g–1 h–1)
32.17±15.20a
404.9±59.4a
7.36±2.34b
323.0±153.9a,b
3.25±0.62b
221.5±0.09 b
31.32±17.34a
270.8±76.9b
37.95±18.67a
80.2±19.8c
Burst length (s)
285±116a
94±34a
59±21a
392±176a
1595±642b
83.96±28.8a
31.2±14.5b
51.8±10.5b
27.9±17.8b
10.8±2.8b
178±87a
140±86a
194±91a
340±257a
2080±1107b
5.00±3.1b,c
4.80±3.1b
6.45±3.6c
3.53±2.2b
1.86±1.4a
12.98±7.0a
–
–
Interburst V̇CO2 (µl
Interburst length (s)
g–1 h–1)
Discontinuous gas exchange cycle:
Frequency (mHz)
2.22±0.8a,b
Period (min)
8.39±3.0a,b
456
Table 3 Standard metabolic rate (mean±SD) of telecoprid beetles
at 20°C. Means with the same letter are not significantly different
(P<0.05; ANOVA with Tukey’s multiple range test)
Species
Mass
(g)
Metabolic
rate
(W kg–1)
S. fasiculatus
Sc. rusticus
A. convexus
Sc. flavicornis
C. bacchus
0.136±0.012
0.564±0.131
1.421±0.35
0.322±0.053
7.285±2.93
1.789±0.38a
0.987±0.60b
0.719±0.21b
1.019±0.27b
0.331±0.1c
longer. Inspection of the values obtained for the other
four species shows that S. fasciculatus and Sc. flavicornis appear to have similar burst characteristics (burst
emission V̇CO2 in µl g–1, and burst length) while Sc.
rusticus and A. convexus have similar burst characteristics.
In both Sc. rusticus and A. convexus, a positive correlation between DGC frequency and rate of CO2 emission
( V̇CO2) was found, which implies that V̇CO2 primarily
modulated DGC frequency to accommodate increased
demand for CO2 release. In C. bacchus and Sc. flavicornis, V̇CO2 is positively correlated with the rate of
burst CO2 emission, indicating that V̇CO2 in this case
primarily modulated burst CO2 volumes to accommodate
increased demand for CO2 release. In S. fasciculatus
there was no correlation between V̇CO2 and any ventilation characteristics, implying that the cyclic CO2 release
was not modulated by gas exchange parameters.
Metabolic rate
The standard metabolic rate for each beetle species was
calculated from the mean V̇CO2 of the beetles while exhibiting regular discontinuous ventilation (Table 3). S.
fasciculatus has the highest metabolic rate while C. bacchus has the lowest.
Grouping all the species data we found that there was
a significant negative relationship between metabolic
rate and body mass (metabolic rate=0.69M–0.38, where
M=mass in g, r2=0.72, P<0.001). The relationship between respiratory rate (ml CO2 h–1) and body mass is
CO2=0.11M0.623, where M=mass in g (r2=0.87, P<0.001).
Discussion
Comparison with other insects
The DGC patterns measured in the telecoprid beetles in
this study show both similarities to and differences from
the DGC patterns reported for other insects. Of interest
in this study is the fact that spiracular fluttering occurred
during the open phase in Sc. flavicornis and C. bacchus
(Fig. 3), and not as a separate phase. In agreement with a
study of tenebrionid beetles (Lighton 1991a), DGC fre-
quency was found to be mass independent. The telecoprid beetles differed from each other in their DGC patterns but could basically be divided into three groups
(Table 2).
Sc. rusticus and A. convexus (Fig. 2) have a DGC pattern which appears similar to those found in several ant
species (Duncan and Crewe 1993), a mutillid wasp
(Duncan and Lighton 1997) and other tenebrionid beetles (Bartholomew et al. 1985). The DGC trace has the
three distinct phases: a closed phase, followed by a variable flutter phase, and then a short-duration open phase.
However, in both these species the volume of CO2 emitted per unit mass during the open phase (Table 1; burst
CO2, A. convexus 3.25 µl g–1 and Sc. rusticus 7.36 µl g–1)
is far lower than that reported for other insects. For the
Namib tenebrionid beetles burst V̇CO2 is 15.8 µl g–1 (calculated from Lighton 1991a), in the ant Camponotus
vicinus 21.4 µl g–1 (Lighton 1992), and in the mutillid
wasp, 22.0 µl g–1 (Duncan and Lighton 1997). This could
imply that the hemolymph CO2 buffering capacity of the
tissues of the two dung beetle species is lower than that
found in most insects (Lighton 1994), or that these beetles do not maintain their open phase volumes near the
maximum. This would suggest that there are factors other than hypercapnia which initiate the open phase. In
both species the DGC frequency was modulated by metabolic rate (V̇CO2), to accommodate increased demands
for CO2 release. The modulation of DGC by metabolic
rate has been reported for several other insect species
(Lighton 1994). The open phase CO2 volume and burst
length were unaffected by metabolic rate increase in both
these species. A similar result was found for the mesic
ant, Camponotus vicinus (Lighton 1988a).
The most attenuated form of the DGC cycle is shown
by S. fasciculatus (Fig. 2), which has a long burst phase
and a short, combined closed and flutter phase. An increase in metabolic rate did not affect any of the DGC
parameters. This may imply that the spiracle control is
not as exact in this species compared to other beetles.
The most unusual form of DGC is exhibited by Sc.
flavicornis, and C. bacchus (Fig. 3). The spiracles appear
to flutter during the burst phase, and the possible advantages of this behaviour are discussed in the next section.
In both species there is no discernible pre-burst flutter
phase but a well-defined closed phase. The closed phase
is the longest in C. bacchus. The volume of CO2 emitted
per unit mass during the open phase (Table 2; burst
V̇CO2, Sc. flavicornis 31.32 µl g–1 and C. bacchus
37.95 µl g–1) is far greater than that reported for other insects (15.8–22.0 µl g–1). This implies that their hemolymph has a high CO2 buffering capacity, or that these
beetles maintain their open phase volumes near the maximum. In both these species metabolic rate (V̇CO2) modulated the ventilation rate and rate of CO2 emission during the open phase. The duration of the open phase remained constant even though metabolic rate increased,
and in Sc. flavicornis the volume of the open phase was
not affected, but in C. bacchus it increased with increased metabolic rate. Lighton and Wehner (1993)
457
found that metabolic rate modulated only ventilation rate
in the xeric ant, Cataglyphis bicolor.
The scaling component of the allometric relationship
between respiratory rate and body mass for all five telecoprid beetle species is lower than that determined by
Lighton (1991a) for ten species of tenebrionid beetles
(0.623 versus 0.858 respectively). This does not conform
with the vertebrate model, but to date there is no evidence that insects in general conform to that model. We
therefore cannot comment on whether these beetles depart from the allometric equation or not. The y-intercept
is similar (0.11; this study, and 0.162; Lighton 1991a),
indicating adaptations of energy metabolism to aridity,
low habitat productivity and unpredictable environments
(Bartholomew et al. 1985).
Ventilatory pattern and habitat
From the above data we can draw some conclusions
about the function of the DGC in relation to habitat. We
propose that in some species the DGC has been altered
to limit respiratory water loss in more arid environments,
and in those habitats where water loss is not consequential, the DGC is under less stringent control. The role of
DGC in reducing respiratory water loss has been postulated in several earlier studies (see Lighton 1996).
The reduction of respiratory water loss is thought to
be as a result of the diffusive loss of CO2 and water vapour being restricted to discrete cyclic events (Miller
1981). Thus the open phase (high respiratory water loss)
of the DGC should be short relative to the interburst
phase (low respiratory water loss). Another method to
reduce respiratory water loss is to increase the flutter
phase duration and shift more of the total CO2 output to
this phase, as water loss rates are lower in the flutter
phase. An increase of CO2 output in the flutter phase was
reported for arid-adapted Namib beetles (Lighton
1991a). Subsequently, Lighton and Garrigan (1995) have
found that due to spiracular fluttering, less water is lost
during the flutter phase than would be the case in the
open phase where there is no spiracular control, even
though the molar rates of CO2 and water loss during the
flutter phase are equivalent. In the ant, Camponotus vicinus, Lighton and Garrigan (1995) found that the rate of
water loss relative to CO2 emission during the open
phase increased approximately fourfold over flutter
phase levels.
The two study species characterised as arid-habitat
specialists are very different in phylogeny, size and diurnal activity (Table 1). We would expect C. bacchus to be
under water stress due to its peculiar life history, showing long periods of activity in the sun, as it walks to find
dung pads, which are a patchy and ephemeral resource.
Klok (1994), showed that the large body size of C. bacchus is effective in improving its desiccation tolerance.
This species is assumed to be a poor competitor against
large, flying telecoprids, and is therefore confined to drier habitats than most of the other large telecoprids (Tribe
1976; Chown et al. 1995). Aptery and reduction of respiratory water loss may be adaptations to this habitat. Our
results show that although this beetle had a significantly
longer open phase than the other species, there was considerable spiracular movement taking place during this
period. There was no observable flutter phase prior to
the burst phase. Thus, if the proposal by Lighton and
Garrigan (1995) that spiracular fluttering reduces water
loss, spiracular movement in the open phase could be
used by this species to achieve the same end. This beetle,
unlike the tenebrionids studied by Lighton (1991a), is
not using a pre-burst flutter phase, but is reducing its water loss in the open phase.
The same type of pronounced spiracular movement in
the open phase was only seen in the other xeric species,
Sc. flavicornis, which although 24 times smaller and
winged, appears to have adopted the same form of respiratory water loss strategy as C. bacchus. There is no distinct pre-burst flutter phase, and the closed phase is longer than the other species measured. Sc. flavicornis is
crepuscular/nocturnal, but this may be due to competition rather than size. Sc. rubripennis Boheman, shares a
similar habitat, but is half the mass of Sc. flavicornis, diurnally active, and desiccation-resistant (Klok 1994). In
arid-adapted telecoprid beetles, reducing respiratory water loss must be important to their overall water budget.
Thus selection pressure could have acted on the ancestral
DGC to reduce respiratory water loss. It is interesting
that the study beetles use a different mechanism to that
observed in arid-adapted tenebrionid beetles (Lighton
1991a). More studies are needed to find out whether this
behaviour is unique to Scarabaeini, or if it occurs in other Coleoptera.
The other three study species are associated with mesic habitats. A. convexus and Sc. rusticus are active in
open areas and are likely to experience moderate water
stress. Sc. rusticus is diurnally active in in mid-morning
and A. convexus is nocturnal. These two species may
limit their respiratory water loss by the high DGC frequency and short open phase.
Finally, S. fasciculatus will be the least waterstressed, as it is only active in the leaf litter of dense
shade. Its DGC shows a long open phase, with a very
short flutter and closed phase combined. This species
also has the greatest rate of CO2 emission. This suggests
that the selection pressure on spiracle activity has been
relaxed, and that respiratory water loss is not an important component of this species’ water budget.
Conclusion
Where do these findings lead us with regard to our original hypothesis? The DGC pattern is exhibited in all three
tribes examined, from ancient to modern, which suggests
that it is an ancestral adaptation, most probably as a result of anoxic environments associated with saprophagy.
However, the most sophisticated form of spiracular control is seen in two distantly related species in response to
458
a common arid habitat. This offers firm support to the
theory that spiracular fluttering is an adaptive behaviour
to reduce respiratory water loss in insects.
Acknowledgements We would like to thank Astrid Jankielsohn
for collecting Sc. flavicornis and Martin Villet for collecting C.
bacchus. This research was supported by the University of the
Witwatersrand via the Communication and Behaviour Research
Group and by the Foundation for Research and Development.
References
Bartholomew GA, Lighton JRB, Louw GN (1985) Energetics of
locomotion and patterns of respiration in tenebrionid beetles
from the Namib desert. J Comp Physiol B155:155–162
Bernon G (1981) Species abundance and diversity of the Coleoptera component of a South African cow dung community, and
associated insect predators. PhD thesis, University of Bowling
Green, Ohio
Cambefort Y (1991a) From saprophagy to coprophagy. In: Hanski
I, Cambefort Y (eds) Dung beetle ecology. Princeton University Press, Princeton, pp 22–35
Cambefort Y (1991b) Biogeography and evolution. In: Hanski I,
Cambefort Y (eds) Dung beetle ecology. Princeton University
Press, Princeton, pp 51–68
Cambefort Y, Hanski I (1991) Dung beetle population biology. In:
Hanski I, Cambefort Y (eds) Dung beetle ecology. Princeton
University Press, Princeton, pp 36–50
Chown SL, Scholtz CH, Klok CJ, Joubert FJ, Coles KS (1995)
Ecophysiology, range contraction and survival of a geographically restricted African dung beetle (Coleoptera: Scarabaeidae). Funct Ecol 9:30–39
Davis ALV (1995) Daily weather and temporal dynamics in an
Afrotropical dung beetle community (Coleoptera: Scarabaeidae). Acta Ecol 16:641–656
Davis ALV (1996) Seasonal dung beetle activity and dung dispersal in selected South African habitats: implications for pasture
improvement in Australia. Agric Ecosyst Environ 58:157–169
Doube BM (1983) The habitat preference of some bovine dung
beetles (Coleoptera: Scarabaeidae) in Hluhluwe game reserve,
South Africa. Bull Entomol Res 73:357–371
Doube BM (1991) Dung beetles of Southern Africa In: Hanski I,
Cambefort Y (eds) Dung beetle ecology. Princeton University
Press, Princeton, pp 133–155
Doube BM, Giller PS (1990) A comparison of two types of trap
for sampling dung beetle populations (Coleoptera: Scarabaeidae). Bull Entomol Res 80:259–263
Duncan FD, Crewe RM (1993) A comparison of the energetics of
foraging of three species of Leptogenys (Hymenoptera, Formicidae). Physiol Entomol 18:372–378
Duncan FD, Lighton JRB (1997) Discontinuous ventilation and
energetics of locomotion in the desert-dwelling female mutillid wasp, Dasymutilla gloriosa. Physiol Entomol 22:310–315
Ferreira MC (1972) Os Escarabideos de Africa (Sol do Saara).
Rev Entomol Moçambique 11:5–1088
Hadley NF (1994) Ventilatory patterns and respiratory transpiration in adult terrestrial insects. Physiol Zool 67:175–189
Heinrich B, Bartholomew GA (1979) Roles of endothermy and
size in inter- and intraspecific competition for elephant dung
in an African dung beetle, Scarabaeus laevistriatus. Physiol
Zool 52:489–496
Holter P (1991) Concentrations of oxygen, carbon dioxide and
methane in the air within dung pads. Pedobiologia 35:281–386
Kestler A (1985) Respiration and respiratory water loss. In: Hoffmann KH (ed) Environmental physiology and biochemistry of
insects. Springer, Berlin, pp 137–183
Klok CJ (1994) Dessication resistance in dung-feeding Scarabaeinae. MSc dissertation, University of Pretoria
Lighton JRB (1985) Minimum cost of transport and ventilatory
patterns in three African beetles. Physiol Zool 58:390–399
Lighton JRB (1988a) Discontinuous ventilation in a small insect,
the formicine ant Camponotus vicinus. J Exp Biol 134:363–
376
Lighton JRB (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 JRB (1990) Slow discontinuous ventilation in the Namib
dune-sea ant, Camponotus detritus (Hymenoptera, Formicidae). J Exp Biol 151:71–82
Lighton JRB (1991a) Ventilation in namib desert tenebrionid beetles: mass scaling and evidence of a novel quantized flutterphase. J Exp Biol 159:249–268
Lighton JRB (1991b) Measurements on insects. In: Payne PA (ed)
Concise encyclopaedia on biological and biomedical measurement systems. Pergamon, Oxford, pp 201–208
Lighton JRB (1992) Direct measurement of mass loss during discontinuous ventilation in two species of ants. J Exp Biol 173:
289–293
Lighton JRB (1994) Discontinuous ventilation in terrestrial insects. Physiol Zool 67:142–162
Lighton JRB (1996) Discontinuous gas exchange in insects. Annu
Rev Entomol 41:309–324
Lighton JRB, Berrigan D (1995) Questioning paradigms: caste
specific ventilation in harvester ants, Messor pergandei and M.
julianus (Hymenoptera: Formicidae). J Exp Biol 198:521–530
Lighton JRB, Garrigan D (1995) Ant breathing: testing regulation
and mechanism hypotheses with hypoxia. J Exp Biol 198:
1613–1620
Lighton JRB, Wehner R (1993) Ventilation and respiratory metabolism in the thermophilic desert ant, Cataglyphis bicolor (Hymenoptera, Formicidae). J Comp Physiol B 163:11–17
Miller PL (1981) Ventilation in active and inactive insects. In:
Herreid CF, Fourtner CR (eds) Locomotion and energetics in
arthropods. Plenum, New York, pp 367–390
Osberg D (1988) The influence of soil type on the potential distribution of two species of Scarabaeine dung beetle. MSc dissertation, University of the Witwatersrand, Johannesburg
Osberg DC, Hanrahan SA (1992) The spatial distribution of Allogymnopleurus thalassinus Klug and A. consocius Peringuey
(Coleoptera: Scarabaeidae) in an area of mixed soil types in
South Africa. J Entomol Soc S Afr 55:85–92
Osberg DC, Doube BM, Hanrahan SA (1993) Habitat specificity
in African dung beetles: the effect of soil type on dung burial
by two species of ball-rolling dung beetles (Coleoptera Scarabaeidae). Trop Zool 6:243–251
Paschalidis KM (1974) The genus Sisyphus Latr. (Coleoptera:
Scarabaeidae) in southern Africa. MSc dissertation, Rhodes
University, Grahamstown, South Africa
Schmidt-Nielsen K (1980) Animal physiology: adaptation and environment, 2nd edn. Cambridge University Press, Cambridge
Sláma K (1988) A new look at insect respiration. Woods Hole
Oceanogr Inst Biol Bull 175:289–300
Tribe GD (1976) The ecology and ethology of ball-rolling dung
beetles (Coleoptera: Scarabaeidae). MSc dissertation, University of Natal, Pietermaritzburg
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, New
Jersey