Insect gas exchange patterns: a phylogenetic perspective
Spatial, Physiological and Conservation Ecology Group, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
* Author for correspondence (e-mail: emarais{at}sun.ac.za)
Accepted 12 October 2005
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Summary |
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Key words: adaptation, discontinuous gas exchange, periodic breathing, phylogeny
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Introduction |
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Subsequent investigations cast doubt on this hypothesis, and six competing
explanations have now been formulated to account for the evolution of DGCs
(reviewed in Chown et al., 2005). A prominent feature of virtually all tests
of the competing hypotheses is that they have been based either on
small-scale, manipulative experiments
(Lighton and Berrigan, 1995;
Chown and Holter, 2000
), or
comparative investigations of a few closely related species (e.g.
Lighton, 1991a
;
Duncan et al., 2002
;
Chown and Davis, 2003
). These
approaches have provided many valuable insights into the evolution of insect
gas exchange patterns, and especially the mechanisms underlying them. However,
broader comparative analyses can also be informative. Indeed, Huey and
Kingsolver (1993
) have
cogently argued that a combined approach involving mechanistic investigations,
laboratory selection and comparative methods is essential if an integrated
understanding of the evolution of physiological traits, and their broader
ecological implications, is to be achieved (see also
Kingsolver and Huey, 1998
;
Feder and Mitchell-Olds,
2003
). Moreover, comparative analyses undertaken in a phylogenetic
context can provide useful information on the history of a given trait,
including its origin, whether or not it should be considered adaptive (in the
strict sense, such that natural selection is responsible for its origin and
maintenance; Coddington, 1988
;
Baum and Larson, 1991
), and the
likelihood of repeated and/or convergent evolution
(Brooks and McLennan, 1991
). In
the context of gas exchange patterns, the value of such a phylogeny-based
comparative approach has already been established by Klok et al.
(2002
), who demonstrated that
discontinuous gas exchange probably arose independently at least four times in
the Arthropoda. Nonetheless, no phylogeny-based comparative analysis of the
occurrence of gas exchange patterns, and particularly discontinuous gas
exchange, in insects (which form a monophyletic unit;
Giribet et al., 2001
) has been
undertaken.
This situation at first appears remarkable, given that published
investigations of gas exchange patterns are available for 99 insect species,
and it is known that these patterns vary considerably among, and sometimes
within, species at rest: from continuous, to cyclic, to discontinuous
(Lighton, 1998;
Marais and Chown, 2003
;
Gibbs and Johnson, 2004
).
However, on closer inspection it is clear that there are probably several
reasons why no phylogeny-based analysis has been undertaken, amongst which two
are perhaps most significant. First, there is probably a file-drawer problem
(Csada et al., 1996
), such
that in instances where species do not show discontinuous gas exchange the
data are not published, thus biasing the literature in favour of reports of
discontinuous gas exchange cycles
(Lighton, 1998
;
Chown, 2001
). Second, and
possibly as a consequence of the file-drawer problem, the taxa for which gas
exchange patterns are available is highly skewed towards the holometabolous
insects. Thus, of the approx. 100 insect species for which information on gas
exchange patterns is presently available, 83 are holometabolous, and of these,
44 are Coleoptera. By contrast, the Exopterygota is comparatively
under-represented in the literature, with published information available for
six cockroach species, six termite species, and five species of Orthoptera. No
Apterygotes (Zygentoma and Archaeognatha) have been investigated.
In this paper, we address some of the above problems and provide the first,
phylogeny-based comparative analysis of the distribution of insect gas
exchange patterns at the order level. Whilst we cannot resolve the file-drawer
issue, we comprehensively review patterns documented by the existing
literature, provide information on several exemplar taxa representing orders
of insects that have not previously been investigated (Archaeognatha,
Zygentoma, Ephemeroptera, Odonata, Mantodea, Mantophasmatodea, Phasmatodea,
Dermaptera, Neuroptera and Trichoptera), and add to the data on little studied
groups (Blattodea, Orthoptera, Hemiptera and Diptera). In undertaking this
work we realise that a comprehensive comparative analysis of insect gas
exchange patterns is still some way off. The 118 species included here
represent less than 0.003% of the estimated global insect fauna
(May, 2000). However, because
much of the variation in insect physiological traits is partitioned at higher
taxonomic levels (Chown et al.,
2002
), we begin by using exemplar taxa at the Order level. Thus,
our aim is to provide a working phylogenetic framework within which the
evolution of gas exchange patterns in insects can be discussed. To date, such
a framework has been missing.
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Materials and methods |
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Experimental investigations
The additional species collected for investigation were chosen based on
Order-level deficiencies in the literature on gas exchange patterns. Adult
individuals of 19 species representing the Archaeognatha (1 sp.), Zygentoma (3
spp.), Ephemeroptera (1 sp.), Odonata (2 spp.), Blattodea (1 sp.), Mantodea (1
sp.), Mantophasmatodea (1 sp.), Phasmatodea (1 sp.), Orthoptera (1 sp.),
Dermaptera (1 sp.), Hemiptera (2 spp.), Neuroptera (1 sp.), Diptera (1 sp.),
Trichoptera (1 sp.) and Lepidoptera (1 sp.) were collected from several
localities in South Africa (Table
1) and returned to the laboratory within 1 week of collection.
Most experiments started within 12 h of the arrival of the insects at the
laboratory because little is known about how long they survive in captivity.
Insects were held in an incubator at 22±1°C (12 h:12 h L:D
photoperiod), with access to water but not to food (with the exception of the
hemipterans, mantophasmatodeans, cockroaches and the stick insects, where food
was provided, but where a period of starvation preceded respirometry), before
their gas exchange patterns were examined. Assessments were made in dry air
for technical reasons and because under these conditions discontinuous gas
exchange would seem most likely as a means to conserve water
(Duncan et al., 2002). Each
individual was weighed using an analytical balance (0.1 mg resolution; Mettler
Toledo AX504, Columbus, OH, USA), and placed into a cuvette kept at
20±0.2°C, using either a water bath (Grant LTD20, Cambridge, UK) or
a temperature-controlled cabinet (Labcon, Johannesburg, South Africa). This
slightly lower temperature was selected because it improved quiescence and
might have also induced discontinuous gas exchange. Previous work
(Chown, 2001
;
Marais and Chown, 2003
)
indicated that gas exchange patterns, whilst repeatable, can be variable
within individuals and species. In consequence, conditions favourable to the
induction of discontinuous gas exchange were used, and particularly
temperatures that are typically lower than mean summer microclimate
temperatures in the region (which range from 24°C at sea level, to
22°C at the highest inland site of collection, with absolute maxima
ranging from 50°C at the sea level site to 53°C at the high altitude
site; see also Botes et al., in
press
).
|
Air, scrubbed of CO2 (using soda lime) and water (using silica
gel and then Drierite®, Xenia, OH, USA) was passed through the cuvette
(see Table 1 for response
times, regulated using a Sidetrak Mass Flow Controller, Monterey, USA) and
into a calibrated infrared gas analyzer (Li-Cor Li7000 or Li-Cor Li6262;
Lincoln, NE, USA) to measure CO2 production. Flow rates and cuvette
sizes varied according to the species and in a manner such that washout was
unlikely to be significant (see Results, and
Lighton, 1991b). A Sable
Systems (Las Vegas, NV, USA) AD-1 activity detector was used to detect any
movement of the individual in the cuvette during the experiment, and the
output of the detector was fed into the auxiliary channel of the Li7000 or
Li6262. The AD-1 registers activity as a value between 5 and +5 V,
where little deviation from the mean indicates that the animal is inactive,
and a large deviation indicates high levels of activity (for detail see
www.sablesys.com/ad1.html).
Each experimental assessment lasted for approximately 2 h, which is typically
sufficient to detect variation in gas exchange traces
(Chown, 2001
) without
dehydrating animals to such an extent that the gas exchange pattern might
switch to continuous, owing to dehydration, as has been found in some species
(Quinlan and Hadley, 1993
;
Chappell and Rogowitz, 2000
).
The data file generated by the Li7000 software was exported, via
Microsoft Excel, to DATACAN V (Sable Systems,), whilst the data stream from
the Li6262 was captured directly using Sable Systems hardware and software.
DATACAN V was used for initial analysis of the respirometry data (corrected to
standard temperature and pressure) for periods of inactivity only.
Traces of rates of CO2 production
(CO2) were categorized as
continuous, cyclic or discontinuous gas exchange by inspection. The DGCs were
readily identified based on the presence of C-periods and F-periods. However,
identification of gas exchange patterns in the absence of the C- and F-periods
is less straightforward. Several statistical approaches were explored for
distinguishing continuous from cycling patterns objectively. These included
spectral analysis and the modification thereof that has been used to identify
population cycles (Cohen et al.,
1998
). Unfortunately, these methods typically did not allow
continuous and cyclic gas exchange to be distinguished, most notably because
even continuous gas exchange has some periodicity. The variance approach
adopted by Williams et al.
(1997
) is also unsuitable
because it does not take temporal autocorrelation into account. In
consequence, any comparison of variances between species would be confounded.
Nonetheless, it is essential that some objective criterion has to be developed
to allow traces to be classified or distinguished in a repeatable manner.
Therefore, we developed a simple, alternative convention based on the
principle of the presence of regular bursts. We assumed that when a line is
drawn through the centre of the
CO2 trace a cyclic trace
should have fewer data points above this line than below it. By contrast, more
continuous traces should show the converse. We applied this convention to the
traces we recorded by adhering to the following steps. First, subtract the
minimum point of the time series that has to be analysed from all the data
points. Second, shift the data series down by 50% to ensure that the zero line
passes through the centre of the trace. Third, calculate the percentage of
data points that lie above the zero line. We adopted a conservative approach
here and assumed that if the percentage of data points above the zero line was
<30% the trace was cyclic, whilst if the percentage was >30% the trace
was more likely to be continuous (Fig.
1). This technique is sensitive to traces that show drift and/or
outliers (e.g. electronic glitches, baseline measurements) in the time series
that result in artificial minima or maxima. However, such errors can routinely
be corrected using modern analytical software. Although it might be argued
that an alternative set of criteria should be used, the approach we adopted
makes any decision on cyclic vs continuous traces explicit,
repeatable, and more objective than simple inspection. Here, once this method
had been applied to the traces, summary statistics for the data were
calculated, based on the approach to cyclic and discontinuous gas exchange
patterns adopted by Marais and Chown
(2003
).
|
Analyses
Based on the data from the literature and the data generated in this study
we assigned gas exchange patterns (continuous, cyclic and discontinuous) to
all of the insect orders that have been investigated to date, and these were
plotted onto the phylogeny of the orders provided by Gullan and Cranston
(2005). In those orders where
species showed different gas exchange patterns, or where a single species
showed more than one pattern, all gas exchange patterns were listed. A formal
parsimony analysis (see Brooks and
McLennan, 1991
) was undertaken and used to assess the likely
evolution of gas exchange patterns [see Scholtz and Chown
(1995
) for use of this
approach to investigate the evolution of scarabaeoid diets]. In cases where
both unknown patterns (orders not yet investigated) and known patterns were
present on shallower nodes, preference was given to the known patterns at the
deeper nodes. It should be noted that although the tree provided by Gullan and
Cranston (2005
) indicates some
controversy in interpretation of the branching patterns, it was not presented
with likelihood values for these alternatives. Therefore, a single parsimony
analysis for one character (gas exchange pattern, with three states) based on
the given tree was undertaken. Adopting the same approach with the consensus
phylogeny presented by Grimaldi and Engel
(2005
) did not change our
conclusions.
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Results |
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Our own investigations added 19 species to the list of those that have been
investigated, and importantly most of these were Exopterygotes or Apterygotes:
groups that have enjoyed little attention to date
(Fig. 2). In a few instances,
sample sizes were low, but sufficient to indicate which kinds of gas exchange
patterns were present. In these instances repeated measures of the individuals
at hand were also undertaken (for rationale, see
McNab, 2003). Likewise,
although the response-time of one of our designs was slow (280 ml cuvette with
150 ml flow rate, to accommodate dragonflies), in none of the cases did
Z-transformations (Bartholomew et
al., 1981
), using empirically derived response-time information
from the experimental set-ups (Table
1), suggest that evidence for a lack of spiracle closure was a
consequence of the experimental design. Moreover, the empirically derived
times were well within those that would be typical of the majority of
published studies, based on the cuvette sizes and flow rates reported in those
studies (e.g. Lighton, 1990
;
Harrison et al., 1991
;
Duncan and Lighton, 1997
).
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Discussion |
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Whilst the comparative analysis does indicate which gas exchange
characteristics are basal, it does not clearly resolve the reason(s) for the
origin and/or maintenance of discontinuous gas exchange. Nonetheless,
examination of the data (supplementary material, Appendix 1;
Table 2) reveals several
interesting patterns to the presence and absence of DGCs. There is no clear
pattern of association between DGCs and subterranean vs
non-subterranean lifestyles (2=1.08, P=0.30).
Likewise, both winged and wingless species show DGCs (
2=0.17,
P=0.68), despite their apparently different oxygen demands
(Reinhold, 1999
;
Addo-Bediako et al., 2002
),
which should mean greater threat of oxidative damage (see
Hetz and Bradley, 2005
) in
flying species at rest because of their highly developed tracheal system that
should mean enhanced oxygen access to tissues
(Chapman, 1998
). However,
associations between DGCs and xeric environments (
2=9.26,
P=0.002), as might be predicted from the hygric hypothesis
(Lighton, 1998
;
Chown and Nicolson, 2004
),
were found. These preliminary analyses broadly suggest that cyclic and
continuous gas exchange at rest are more likely in mesic than in xeric
environments, than are DGCs, but that DGCs can evolve in both kinds of
environments. However, the data have a strong phylogenetic signal such that
DGCs are restricted to a few families. If these analyses are repeated within
orders (Coleoptera, Hymenoptera, Lepidoptera, Orthoptera) or families
(Tenebrionidae, Scarabaeidae, Formicidae) that have sufficiently large sample
sizes, in what is essentially then a phylogenetically nested approach to
examining these associations (see Harvey
and Pagel, 1991
), none of the associations are significant
(
2, P>0.07 in all cases). Thus, the overall result
does not appear to be strongly biased by a single taxon. However, such an
approach does not adequately exclude phylogenetic signal
(Garland et al., 2005
), and
does not make full use of the potentially available environmental data. To
this end, conversion of the environmental data to a continuous, rather than
categorical form, a phylogeny at the species level for the 118 species that
have been studied, and a phylogenetic generalized least-squares analysis
(Grafen, 1989
) is required.
Such work is now underway (C. L. White, S. L. Chown and others, unpublished
data).
In the few studies where a tally has been kept of individuals showing DGCs
vs other gas exchange patterns (e.g.
Gibbs and Johnson, 2004), one
of the predictions of the emergent property hypothesis also seems to be
supported. That is, DGCs should emerge whenever the gas exchange system has
little demand placed on it, but that this might vary given initial conditions
(Chown and Holter, 2000
).
Where there is variation in gas exchange patterns (see also
Table 2), considerable
variation among individuals in gas exchange pattern has been found. Therefore,
DGCs might be an emergent property of the interacting CO2 and
O2 setpoints, although it is not clear why DGCs emerge in only a
few orders. In consequence, there is good reason to undertake modelling work
of interactions between the CO2 and O2 setpoints, in the
context of knowledge of gas exchange regulation (reviewed in
Chown and Nicolson, 2004
), as
well as to examine and, just as importantly, to report variation in gas
exchange patterns within and between individuals (for additional discussion,
see Lighton, 1998
;
Chown, 2001
).
Another striking outcome of this phylogeny-based analysis of insect gas
exchange patterns is that, despite a wide range of studies, undertaken over
many years, nothing remains known of gas exchange in 12 of the 30 insect
orders, and that of the remaining orders, only the Coleoptera and Hymenoptera
have had investigations undertaken on more than ten species. The same is true
of the Arthropoda as a whole, where gas exchange investigations of terrestrial
groups are restricted to only a handful of species (see e.g.
Lighton et al., 1993;
Lighton and Fielden, 1996
;
Lighton, 2002
;
Lighton and Joos, 2002
;
Klok et al., 2002
;
Terblanche et al., 2004
). This
bias in the data does not mean that a clear understanding of the mechanisms
underlying gas exchange, and particularly discontinuous gas exchange, is not
emerging (reviewed by in Lighton,
1996
,
1998
;
Chown and Nicolson, 2004
).
However, it does suggest that investigations of the reasons for the origin and
maintenance of particular forms of gas exchange, in other words their likely
adaptive value, will be constrained, at least from a comparative perspective,
by the absence of appropriate information. To some extent this is true also of
comparisons at the species level where, to date, not a single comparative
analysis, in the strict phylogenetically independent sense (see
Harvey and Pagel, 1991
), or
using a parsimony style approach (see
Brooks and McLennan, 1991
), has
been undertaken for a multi-species monophyletic unit. In addition, laboratory
selection experiments investigating the response of gas exchange patterns to
different conditions have been restricted to a few Drosophila species
and then only under conditions of starvation and desiccation
(Gibbs et al., 1997
; Williams
et al., 1997
,
2004
).
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Acknowledgments |
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Footnotes |
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