Repeatability of standard metabolic rate and gas exchange characteristics in a highly variable cockroach, Perisphaeria sp.
Spatial, Physiological and Conservation Ecology Group, Department of Zoology, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa
* Author for correspondence (e-mail: slchown{at}sun.ac.za).
Accepted 2 September 2003
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Summary |
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Key words: adaptation, body size, discontinuous gas exchange, metabolic rate, variation, cockroach, Perisphaeria sp
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Introduction |
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In insects, the genetic variability and heritability of several
physiological traits have been investigated, mostly in Drosophila
(usually melanogaster) and often in the context of selection
experiments (e.g. Parsons,
1980; Hoffmann and Parsons,
1989a
; Graves et al.,
1992
; Gibbs et al.,
1997
; Gibert et al.,
1998
; Hoffmann et al.,
2003
). Likewise, variation in traits among populations and as a
consequence of acclimation has also been well explored, especially for thermal
tolerance and desiccation resistance
(Hoffmann, 1990
;
Hoffmann et al., 2001
;
Klok and Chown, 2003
). Whilst
these studies provide evidence that adaptation has probably been responsible
for variation in thermal tolerance and desiccation resistance (see also
Chown et al., 2002
), explicit
exploration of the assumptions underlying the hypothesis of adaptation remains
scarce for most traits. This is especially true of metabolic rate and gas
exchange characteristics. The few explicit studies that have been undertaken
have generally demonstrated a metabolic response to laboratory selection for
desiccation resistance in Drosophila melanogaster, which implies that
the conditions for selection must have been met (Hoffmann and Parsons,
1989a
,b
,
1993
;
Gibbs et al., 1997
;
Djawdan et al., 1998
;
Williams et al., 1998
).
Nonetheless, it is widely assumed that among-species and among-population
variation in whole-organism metabolic traits in most insect taxa is adaptive
(for reviews and examples, see Lighton,
1996
; Chown and Gaston,
1999
; Addo-Bediako et al.,
2001
,
2002
;
Gibbs et al., 2003
). Metabolic
rate is of particular significance in this regard. Not only is it thought to
be closely linked to variation in life history characteristics and body size
(Hoffmann and Parsons, 1991
;
Graves et al., 1992
;
Koz
owski and Gawelczyk,
2002
), but variation therein apparently also has a profound
influence on broad-scale variation in diversity
(Allen et al., 2002
).
Adaptive explanations for variation in metabolic rate and the patterns in
exchange underlying oxygen delivery and CO2 removal in insects
generally take two major forms. First, variation in metabolic rate is thought
to take place in response to either dry conditions, when it is reduced to
conserve water, or to short seasons, when it is elevated to enable more rapid
development (for reviews and discussion, see
Chown and Gaston, 1999;
Addo-Bediako et al., 2002
;
Chown, 2002
). Second,
alterations in gas exchange patterns are thought to have taken place to effect
a respiratory water savings under dry conditions. In particular, it has long
been thought that discontinuous gas exchange, which is present in many insect
species at rest (Lighton,
1996
,
1998
), evolved as a means to
limit respiratory water loss and that it continues to serve this major
function (Levy and Schneiderman,
1966
; Kestler,
1985
; Sláma and
Coquillaud, 1992
; Lighton et
al., 1993a
; Duncan et al.,
2002a
). Discontinuous gas exchange is typically cyclic with each
cycle consisting of a Closed (C) period, during which the spiracles are
tightly closed, a Flutter (F) period, during which the spiracles partly open
and close in rapid succession, and an Open (O) period, during which the
spiracles are open (Lighton,
1996
). The principal explanations for the contribution of
discontinuous gas exchange cycles (DGCs) to water economy are that spiracles
are kept closed for a portion (the C-period) of the DGC thus reducing
respiratory water loss to zero, and that a largely convective F-period
restricts outward movement of water
(Kestler, 1985
). Moreover, it
has also been argued that there is adaptive variation in the durations of the
C-, F-, and O-periods to further reduce water loss. That is, a reduced
O-period, and prolonged C- and F-periods are likely to further restrict
respiratory water loss (Lighton,
1990
; Lighton et al.,
1993b
; Davis et al.,
1999
; Bosch et al.,
2000
; Duncan et al.,
2002a
; Duncan,
2003
). Whilst several other hypotheses for the evolution and
maintenance of DGCs have been proposed
(Lighton and Berrigan, 1995
;
Lighton, 1998
;
Bradley, 2000
), these are also
largely adaptive in nature (though for an exception, see
Chown and Holter, 2000
).
Nonetheless, with the exception of the laboratory selection experiments on
D. melanogaster, there have been few explicit attempts to investigate
the assumptions underlying these claims for adaptation, which have largely
been made on the grounds of comparative studies, of which the majority have
not been undertaken in an explicitly phylogenetic context (for discussion, see
Chown, 2002;
Chown and Gaston, 1999
; for
recent studies, see Davis et al.,
1999
; Duncan and Byrne,
2000
; Addo-Bediako et al.,
2001
; Gibbs et al.,
2003
). Whilst such comparative studies are useful, they are not
without their problems (e.g. Leroi et al.,
1994
), and it is widely accepted that comparative work should be
supported by more explicit investigations of the extent to which selection is
responsible for variation in physiological traits (e.g.
Huey and Kingsolver, 1993
;
Kingsolver and Huey, 1998
). We
therefore undertook this study to investigate the repeatability of metabolic
rate and the characteristics of discontinuous gas exchange cycles in an insect
species that not only exchanges gases intermittently, but also shows
considerable variation in its gas exchange pattern. We reasoned that if these
traits show significant repeatability in this species, then it is likely that
repeatability will be even more pronounced in most other insect species, which
are generally not as variable (see Chown,
2001
).
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Materials and methods |
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Prior to each gas exchange assessment, the individual in question was
starved for 24 h to reduce variability associated with specific dynamic action
(McEvoy, 1984;
Lighton, 1989
;
Duncan et al., 2002b
).
Assessments were made during the day only, in a well-lit room, because we were
concerned only with discontinuous gas exchange and standard metabolic rate.
The species is nocturnal, and at night activity and metabolic rate are high
(Fig. 1A). Assessments were
also made in dry air because under these conditions a discontinuous gas
exchange cycle would seem most likely as a means to conserve water
(Quinlan and Hadley, 1993
;
Duncan et al., 2002b
). Each
individual was weighed (to a resolution of 0.0001 g), using an analytical
balance (Toledo AX504, Mettler, Columbus, OH, USA), and placed into a 5 ml
cuvette kept at 20±0.2°C using a water bath (Grant LTD20,
Cambridge, UK). Air, scrubbed of water (using Drierite, Krugersdorp, South
Africa) and CO2 (using soda lime) was pushed through the cuvette at
a flow rate of 200 ml min-1 (regulated using a Sidetrack Mass Flow
Controller, Monterey, USA) and into a calibrated infrared gas analyzer (Li-Cor
Li7000; Henderson, USA) set in differential mode to measure CO2
production. A Sable Systems (Henderson, USA) AD-1 activity detector was used
to detect any movement of the cockroach in the cuvette during the experiment,
and the output of the detector was fed into the auxillary channel of the
Li7000. The AD-1 presents activity as a value between -5 V and 5 V, where 0 V
is an accurate indication that the specimen is inactive (for more detail, see
www.sablesys.com/ad1.html).
Inspection of several individuals confirmed lack of activity detected by the
AD-1. To avoid the potential influence of pheromones on the behaviour of
individuals, the cuvette was cleaned thoroughly with ethanol after each
experimental trial. Each experimental assessment also lasted for at least 3 h
(for rationale, see Chown,
2001
). The data file generated by the Li7000 software was
exported, via Microsoft Excel, to DATACAN V (Sable Systems), which
was used for initial analysis of the respirometry data (corrected to standard
temperature and pressure).
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Each individual was assessed five times: twice between 07:00 h and 11:00 h,
once between 11:00 h and 14:00 h and twice between 14:00 h and 18:00 h. This
was done because circadian patterns in metabolic rate have been found in other
insect species (Takahashi-Del-Bianco et
al., 1992). Typically, at least 5 days elapsed between each
assessment of an individual, and the order of assessment with regard to time
of day was randomised. The interval between repeated measures is important
because the shorter it is the greater the likelihood that a high repeatability
will be found (Chappell et al.,
1996
; Bech et al.,
1999
). Although we have no data on lifespan for this species, we
have cultured adults for more than a year, and other blaberids are known to
have an adult lifespan of several years
(Scholtz and Holm, 1985
).
Therefore, an interval of at least 5 days is appropriate for this species,
though perhaps biased somewhat in the direction of higher repeatability. The
total time taken for the study was approximately 5 months.
Analyses
Because of the small number of males available, we generally restricted our
analyses of repeatability to females. Somewhat surprisingly, we found four
major patterns of gas exchange, of which three were intermittent and cyclic
(see Results), and the fourth was continuous. Data from the continuous pattern
were excluded because metabolic rate was significantly higher (approximately
twofold) during this pattern of gas exchange than during the others
[repeated-measures analysis of variance (ANOVA), F(3,41)=6.79,
P=0.0008, Tukey's HSD for unequal sample sizes,
Table 1], even though the
individuals were inactive. In consequence, investigations of the repeatability
of gas exchange components were undertaken for each for the three major cyclic
patterns, and across the dataset as a whole. The variables investigated were
duration (s), CO2 volume (µl) and CO2 emission rate
CO2 (µl
h-1) for each period, and mean
CO2 and mean
frequency of the cycles. Where the analyses were done across the three cyclic
patterns, the Flutter period typical of discontinuous gas exchange was
compared with the `Interburst' period associated with the other forms of
cyclic gas exchange. In these cases we also included data for males.
Repeatability (r) was calculated using the intraclass correlation approach
(Berteaux et al., 1996
;
Falconer and Mackay, 1996
),
based on analyses of variance and the equations provided by Lessells and Boag
(1987
). Because variation in
body mass affects variation in metabolic rate and DGC characteristics in
arthropods (Peters, 1983
;
Lighton, 1991
;
Lighton and Fielden, 1995
;
Davis et al., 1999
), and
because there was a reasonable range in the body mass of the specimens we
examined (females: mass 0.3397±0.0184 g, mean ± S.E.M., range
0.17950.4643 g; males: mass 0.2357±0.0425 g, range
0.17930.3189 g) the effects of body size were taken into account in a
second round of repeatability analyses. Usually, to do this the residuals from
the regression of body mass and the characteristic of interest are used
(Berteaux et al., 1996
;
Fournier and Thomas, 1999
).
Here, this was not done. Rather, in all cases, body mass was included as a
covariate in the initial ANOVAs (for rationale, see
Freckleton, 2002
). Where mass
did not explain a significant portion of the variance in the independent
variable, r was not determined including mass as a covariate. Confidence
intervals for r were calculated using the formulae provided by Krebs
(1999
). A significant
repeatability value of 1 indicates that individuals are perfectly consistent
in their performance over time, whereas a non-significant repeatability value,
or one of 0, indicates no consistent variation among individuals. In all cases
a sequential Bonferroni test (
=0.05) was used to correct table-wide
significance values for multiple tests
(Rice, 1989
).
|
To further investigate the likely sources of variation in these traits,
nested (hierarchical) analyses of variance
(Sokal and Rohlf, 1995) were
used. This method allows ready identification of the level at which most
variation can be explained, and has been used for this purpose in several
other studies (Berteaux et al.,
1996
; Chown et al.,
1999
; Addo-Bediako et al.,
2002
). For each of the major gas exchange patterns, variance was
partitioned between error nested within (<) trial<time of
day<individual<gender. Gender was not used as a level of partitioning in
the pulsation pattern because males never showed the pattern. A similar
analysis was also undertaken across all three cyclic gas exchange patterns. In
the case of frequency and mean metabolic rate, the trial level was excluded
because metabolic rate and frequency are calculated across all the cycles,
rather than just for each individual cycle as can be done for the
characteristics of each of the periods. A sequential Bonferroni correction
(
=0.05) was also applied here.
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Results |
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For most of the characteristics examined here, repeatability was significant and large (Fig. 2, Bonferroni correction did not alter significance values appreciably). Within patterns, repeatability tended to be highest, as might be expected, with values for Burst or O-period characteristics generally above 0.3 (with the exception of Burst duration in the Pulsation pattern when mass was included as a covariate). By contrast, Interburst or C-period characteristics tended to have lower repeatabilities (with the significant exception of emission rate, Fig. 2). Across patterns, repeatabilities were also high for the Burst period and somewhat lower for the Interburst period, with emission rate now having the lowest repeatability. This is not surprising because the three patterns differ in the extent to which individuals close their spiracles. In the DGC pattern the spiracles are held closed, whilst this is generally not the case in the other patterns (Fig. 1). There was consistent among-individual variation in metabolic rate (excluding mass: r=0.51 for males and females, 0.48 for females only; including mass r=0.22 for males and females, 0.29 for females only) and frequency (excluding mass: r=0.25 for females only, 0.31 for males and females; including mass: r=0.29 for females only, 0.35 for males and females) (see Supplemental data, Appendix 1A). In general, repeatabilities tended to decline when mass was included as a covariate, but this was not always the case (Supplemental data, Appendix 1B).
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The nested analyses of variance generally bore out our repeatability results (Table 2). Moreover, they provided additional insight into the level at which variation that was not a function of individual identity was partitioned. Thus, it is clear that DGC patterns tended to vary much more between trials (the Trial term in Table 2) than within a given trial (the Error term in Table 2), whilst the converse was true of the Pulsation pattern and, to a lesser extent, of the InterburstBurst pattern. In this context it is important to realize that the error term includes both error and variation between individual cycles in a particular trial. The nested ANOVAs also revealed that there is generally little variation amongst genders in most of the traits examined here. Although this does not appear to be the case when the analyses are undertaken across all three intermittent patterns, this is solely the consequence of the absence of a pulsation pattern in the males.
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Discussion |
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Despite this variety in gas exchange patterns, repeatability values for
metabolic rate, frequency and the other gas exchange characteristics were
generally high and always significant when examined across the three patterns
that were typical of animals at rest with low metabolic rates. These high
repeatabilities were not a consequence of pronounced differences between the
genders, with the notable exception of the absence of a Pulsation pattern in
males. However, the exclusion of body size variation did tend to result in
lower repeatabilities. Although most studies first remove the effects of size
variation before examining repeatability, it might also be argued that this
should not be done. This is most readily demonstrated in the context of
metabolic rate variation. Several models have demonstrated the importance of
metabolic rate for body size evolution (e.g.
Kozowski and Weiner,
1997
), and Koz
owski and Gawelczyk
(2002
) have clearly shown that
the major factors influencing optimal size are the size dependence of
production rate (which is influenced by metabolic rate; see
Sibly and Calow, 1986
) and the
size dependence of mortality rate (which could be influenced by metabolic
rate; see Chown and Gaston,
1999
). Thus, it seems much more likely that selection will act on
the metabolic rate of an animal of a given size than on the residual variation
of that trait once size has been taken into account. McNab
(1999
) arrived at a similar
conclusion, pointing out "...that total units of metabolism are the
ecologically and evolutionary relevant units". This argument can
readily be applied to all of the other traits we examined, and indeed, in our
view, to most other physiological and life history traits.
Therefore, we can conclude that for most of the characteristics we examined
variation among individuals was typically significant, and often considerable.
These results provide strong evidence that one of the conditions for
considering natural selection an important process in the evolution both of
gas exchange traits and standard metabolic rate has been met
(Endler, 1986;
Bech et al., 1999
). They also
provide a line of evidence, independent of that of comparative analyses,
suggesting that variation in these traits among species and populations might
well be adaptive. The only exceptions appeared to be the characteristics of
the Closed period (in DGC) and Interburst period (in the other cyclic
patterns), where repeatability was generally low. Thus, of the gas exchange
characteristics examined, those associated with the Closed and Interburst
periods are least likely to be the subject of selection. This finding is in
keeping with evidence demonstrating that among species with discontinuous gas
exchange cycles it is most often the F- and O-periods that vary in a way
consistent with adaptive change (Lighton,
1988
; Lighton et al.,
1993a
; Bosch et al.,
2000
; Duncan and Byrne,
2000
; Duncan,
2003
; Chown and Davis,
2003
).
To date, no other studies have convincingly demonstrated consistent
among-individual variation in standard metabolic rate and gas exchange
characteristics in insects. Prior to this investigation, repeatability in one
or more of these traits had only been examined on two occasions. Buck and
Keister (1955) reported, but
did not provide the statistics for, analyses of variance, which apparently
revealed that among-individual variation in O-period volume in diapausing moth
pupae was larger than that within individuals, but that several other
characteristics of the DGC showed "about as much variation between
different cycles of a single pupa as between pupae". Much later,
Chappell and Rogowitz (2000
)
reported repeatability of standard metabolic rate and DGC characteristics for
two species of longicorn beetles (see also
Rogowitz and Chappell, 2000
),
but included both species in their analysis without distinguishing them,
factored out body size before the analyses, and considered their
non-significant results a consequence of small sample size. Our work takes
these initial, useful analyses a step further and demonstrates that, in
general, both standard metabolic rate and gas exchange characteristics are
significantly repeatable, so meeting one of the major requirements for
selection.
Although repeatability estimates for physiological traits in insects and
other arthropods are comparatively rare, our data are in keeping with the work
that has been undertaken to date. For example, Chappell and Rogowitz
(2000) found r values in the
range 0.260.57 for DGC characteristics in the longicorn beetles they
examined. Our values for DGC characteristics not only span a broader range,
but unlike theirs were also all significant. This difference is particularly
important in the context of metabolic rate. Their analysis indicated a low and
non-significant repeatability (0.38), whilst ours suggested that repeatability
of metabolic rate was both higher (0.480.51) and significant.
Nonetheless, it should be kept in mind that the inclusion of body mass as a
covariate makes a considerable difference to the value of r in our analysis,
but not to its significance (repeatability declined from 0.51 to 0.21 when the
effects of mass were controlled for). Considering other physiological traits,
in Melanoplus grasshoppers, repeatability of tethered flight duration
varies between 0.6 and 0.7 (Kent and
Rankin, 2001
), whilst in Rhizoglyphus mites,
repeatability of sperm competitive ability is much lower (0.22)
(Radwan, 1998
).
Our repeatability estimates for metabolic rate in Perisphaeria sp.
were also well within the range of values typically found in vertebrates. For
example, repeatability estimates ranged from 0.35 to 0.52 in breeding female
kittiwakes measured over an interval of one year
(Bech et al., 1999) and, in a
variety of small mammals and birds, varied between 0.261 in meadow voles
measured over an interval of 42 days
(Berteaux et al., 1996
) and
0.64 in kittiwakes measured over the course of a single day
(Fyhn et al., 2001
).
In conclusion, we have provided evidence that at least one of the
prerequisites for natural selection for metabolic rate and gas exchange
characteristics in insects is satisfied, and therefore that variation in these
traits might be considered adaptive. Whilst our work does not provide
conclusive evidence for adaptation in these traits, when considered in
conjunction with selection experiments (reviewed in
Gibbs, 1999), and comparative
analyses (reviewed in Chown and Gaston,
1999
), it does make the argument for adaptive variation more
compelling than it has been. In the past, investigations of variation in gas
exchange characteristics in particular have suffered from an unduly
Panglossian approach.
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Acknowledgments |
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Footnotes |
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