Elrike Marais

Discontinuous gas exchange in insects: a clarification of hypotheses and approaches.

Many adult and diapausing pupal insects exchange respiratory gases discontinuously in a three‐phase discontinuous gas exchange cycle (DGC). We summarize the known biophysical characteristics of the DGC and describe current research on the role of convection and diffusion in the DGC, emphasizing control of respiratory water loss. We summarize the main theories for the evolutionary genesis (or, alternatively, nonadaptive genesis) of the DGC: reduction in respiratory water loss (the hygric hypothesis), optimizing gas exchange in hypoxic and hypercapnic environments (the chthonic hypothesis), the hybrid of these two (the chthonic‐hygric hypothesis), reducing the toxic properties of oxygen (the oxidative damage hypothesis), the outcome of interactions between O2 and CO2 control set points (the emergent property hypothesis), and protection against parasitic invaders (the strolling arthropods hypothesis). We describe specific techniques that are being employed to measure respiratory water loss in the presence or absence of the DGC in an attempt to test the hygric hypothesis, such as the hyperoxic switch and H2O/CO2 regression, and summarize specific areas of the field that are likely to be profitable directions for future research.

Insect gas exchange patterns: A phylogenetic perspective

SUMMARY Most investigations of insect gas exchange patterns and the hypotheses proposed to account for their evolution have been based either on small-scale, manipulative experiments, or comparisons of a few closely related species. Despite their potential utility, no explicit, phylogeny-based, broad-scale comparative studies of the evolution of gas exchange in insects have been undertaken. This may be due partly to the preponderance of information for the endopterygotes, and its scarcity for the apterygotes and exopterygotes. Here we undertake such a broad-scale study. Information on gas exchange patterns for the large majority of insects examined to date (eight orders, 99 species) is compiled, and new information on 19 exemplar species from a further ten orders, not previously represented in the literature (Archaeognatha, Zygentoma, Ephemeroptera, Odonata, Mantodea, Mantophasmatodea, Phasmatodea, Dermaptera, Neuroptera, Trichoptera), is provided. These data are then used in a formal, phylogeny-based parsimony analysis of the evolution of gas exchange patterns at the order level. Cyclic gas exchange is likely to be the ancestral gas exchange pattern at rest (recognizing that active individuals typically show continuous gas exchange), and discontinuous gas exchange probably originated independently a minimum of five times in the Insecta.

Evolutionary responses of discontinuous gas exchange in insects

The discontinuous gas-exchange cycles (DGCs) observed in many quiescent insects have been a cause of debate for decades, but no consensus on their evolutionary origin or adaptive significance has been achieved. Nevertheless, three main adaptive hypotheses have emerged: (i) the hygric hypothesis suggests that DGCs reduce respiratory water loss; (ii) the chthonic hypothesis suggests that DGCs facilitate gas exchange during environmental hypoxia, hypercapnia, or both; and (iii) the oxidative-damage hypothesis suggests that DGCs minimize oxidative tissue damage. However, most work conducted to date has been based on single-species investigations or nonphylogenetic comparative analyses of few species, despite calls for a strong-inference, phylogenetic approach. Here, we adopt such an approach by using 76 measurements of 40 wild-caught species to examine macrophysiological variation in DGC duration in insects. Potential patterns of trait variation are first identified on the basis of the explicit a priori predictions of each hypothesis, and the best phylogenetic generalized least-squares fit of the candidate models to the data is selected on the basis of Akaikes information criterion. We find a significant positive relationship between DGC duration and habitat temperature and an important interaction between habitat temperature and precipitation. This result supports the hygric hypothesis. We conclude that the DGCs of insects reduce respiratory water loss while ensuring adequate gas exchange.

Repeatability of standard metabolic rate and gas exchange characteristics in a highly variable cockroach, Perisphaeria sp.

SUMMARY For natural selection to take place several conditions must be met, including consistent variation among individuals. Although this assumption is increasingly being explored in vertebrates, it has rarely been investigated for insect physiological traits, although variation in these traits is usually assumed to be adaptive. We investigated repeatability (r) of metabolic rate and gas exchange characteristics in a highly variable Perisphaeria cockroach species. Although this species shows four distinct gas exchange patterns at rest, metabolic rate (r=0.51) and the bulk of the gas exchange characteristics (r=0.08–0.91, median=0.42) showed high and significant repeatabilities. Repeatabilities were generally lower in those cases where the effects of body size were removed prior to estimation of r. However, we argue that because selection is likely to act on the trait of an animal of a given size, rather than on the residual variation of that trait once size has been accounted for, size correction is inappropriate. Our results provide support for consistency of variation among individuals, which is one of the prerequisites of natural selection that is infrequently tested in insects.

Uncertainty in invasive alien species listing

Lists of invasive alien species (IAS) are essential for preventing, controlling, and reporting on the state of biological invasions. However, these lists suffer from a range of errors, with serious consequences for their use in science, policy, and management. Here we (1) collated and classified errors in IAS listing using a taxonomy of uncertainty; and (2) estimated the size of these errors using data from a completed listing exercise, with the purpose of better understanding, communicating, and dealing with them. Ten errors were identified. Most result from a lack of knowledge or measurement error (epistemic uncertainty), although two were a result of context dependence and vagueness (linguistic uncertainty). Estimates of the size of the effects of these errors were substantial in a number of cases and unknown in others. Most errors, and those with the largest estimated effect, result in underestimates of IAS numbers. However, there are a number of errors where the size and direction of the effect remains poorly understood. The effect of differences in opinion between specialists is potentially large, particularly for data-poor taxa and regions, and does not have a clearly directional or consistent effect on the size and composition of IAS lists. Five tactics emerged as important for reducing uncertainty in IAS lists, and while uncertainty will never be removed entirely, these approaches will significantly improve the transparency, repeatability, and comparability of IAS lists. Understanding the errors and uncertainties that occur during the process of listing invasive species, as well as the potential size and nature of their effects on IAS lists, is key to improving the value of these lists for governments, management agencies, and conservationists. Such understanding is increasingly important given positive trends in biological invasion and the associated risks to biodiversity and biosecurity.

Beneficial acclimation and the Bogert effect

Few studies have examined the extent to which phenotypic plasticity in a given trait might be influenced by behavioural responses to an environmental cue. Regulatory behaviour might eliminate environmental variation such that little selection for physiological change would take place. Here, to test this Bogert effect on acclimation, we use two life-stages of a kelp fly that inhabit the same habitat, but differ profoundly in their behaviour. We predicted that when denied opportunities for behavioural regulation, mobile, though brachypterous adults would show a performance advantage in most thermal environments following acclimation to their preferred temperature(s). By contrast, in the less mobile larvae, that have a broader thermal preference, beneficial acclimation would be more evident. Ordered factor anova with orthogonal polynomial contrasts revealed that adults recovered faster from chill coma following any one of six short-term temperature treatments if they had been acclimated at low temperature, whilst larvae showed beneficial acclimation.

Life stage-related differences in hardening and acclimation of thermal tolerance traits in the kelp fly, Paractora dreuxi (Diptera, Helcomyzidae).

It is widely appreciated that physiological tolerances differ between life stages. However, few studies have examined stage-related differences in acclimation and hardening. In addition, the behavioural responses involved in determining the form and extent of the short-term phenotypic response are rarely considered. Here, we investigate life stage differences in the acclimation and hardening responses of the survival of a standard heat shock (SHS) and standard low temperature (or cold) shock (SCS), and the crystallization temperature (or supercooling point, SCP) of adults and larvae of the sub-Antarctic kelp fly, Paractora dreuxi. These stages live in the same habitat, but differ substantially in their mobility and thus environmental temperatures experienced. Results showed that neither acclimation nor hardening affected the lower lethal limits in larvae or adults. Adults showed an increase in survival of upper lethal limits after low temperature acclimation, whilst larvae showed a consistent lack of response. The acclimationxhardening interaction significantly affected the SCP in adults, but no response to either acclimation or hardening was found in the larvae. This study further demonstrates the complexities of thermal tolerance responses in P. dreuxi.

Control of discontinuous gas exchange in Samia cynthia: effects of atmospheric oxygen, carbon dioxide and moisture.

SUMMARY The evolution of discontinuous gas exchange (DGE) in insects is highly controversial. Adaptive hypotheses which have obtained experimental support include a water savings mechanism for living in dry environments (hygric hypothesis), a reduction in oxidative damage due to a high-performance oxygen delivery system (oxidative damage hypothesis), and the need for steep intratracheal partial pressure gradients to exchange gases under the hypercapnic and/or hypoxic conditions potentially encountered in subterranean environments (chthonic hypothesis). However, few experimental studies have simultaneously assessed multiple competing hypotheses within a strong inference framework. Here, we present such a study at the species level for a diapausing moth pupa, Samia cynthia. Switching gas conditions from controlled normoxic, normocapnic and intermediate humidity to either high or low oxygen, high or low moisture, elevated carbon dioxide, or some combination of these, revealed that DGE was abandoned under all conditions except high oxygen, and high or low gas moisture levels. Thus, support is found for the oxidative damage hypothesis when scored as maintenance of DGE. Modulation of DGE under either dry or hyperoxic conditions suggested strong support for the oxidative damage hypothesis and some limited support for the hygric hypothesis. Therefore, this study demonstrates that the DGE can be maintained and modulated in response to several environmental variables. Further investigation is required using a strong-inference, experimental approach across a range of species from different habitats to determine how widespread the support for the oxidative damage hypothesis might be.

Reactive oxygen species production and discontinuous gas exchange in insects

While biochemical mechanisms are typically used by animals to reduce oxidative damage, insects are suspected to employ a higher organizational level, discontinuous gas exchange mechanism to do so. Using a combination of real-time, flow-through respirometry and live-cell fluorescence microscopy, we show that spiracular control associated with the discontinuous gas exchange cycle (DGC) in Samia cynthia pupae is related to reactive oxygen species (ROS). Hyperoxia fails to increase mean ROS production, although minima are elevated above normoxic levels. Furthermore, a negative relationship between mean and mean ROS production indicates that higher ROS production is generally associated with lower . Our results, therefore, suggest a possible signalling role for ROS in DGC, rather than supporting the idea that DGC acts to reduce oxidative damage by regulating ROS production.

Scaling of gas exchange cycle frequency in insects.

Previously, it has been suggested that insect gas exchange cycle frequency (fC) is mass independent, making insects different from most other animals where periods typically scale as mass−0.25. However, the claim for insects is based on studies of only a few closely related taxa encompassing a relatively small size range. Moreover, it is not known whether the type of gas exchange pattern (discontinuous versus cyclic) influences the fC–mass scaling relationship. Here, we analyse a large database to examine interspecific fC–mass scaling. In addition, we investigate the effect of mode of gas exchange on the fC–scaling relationship using both conventional and phylogenetically independent approaches. Cycle frequency is scaled as mass−0.280 (when accounting for phylogeneticnon-independence and gas exchange pattern), which did not differ significantly from mass−0.25. The slope of the fC–mass relationship was shallower with a significantly lower intercept for the species showing discontinuous gas exchange than for those showing the cyclic pattern, probably due to lower metabolic rates in the former. Insects therefore appear no different from other animals insofar as the scaling of gas exchange fC is concerned, although gas exchange fC may scale in distinct ways for different patterns.