Browsing by Author "Boardman, Leigh"
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- ItemCold tolerance is unaffected by oxygen availability despite changes in anaerobic metabolism(Springer Nature, 2016) Boardman, Leigh; Sørensen, Jesper G.; Koštál, Vladimir; Šimek, Petr; Terblanche, John S.Insect cold tolerance depends on their ability to withstand or repair perturbations in cellular homeostasis caused by low temperature stress. Decreased oxygen availability (hypoxia) can interact with low temperature tolerance, often improving insect survival. One mechanism proposed for such responses is that whole-animal cold tolerance is set by a transition to anaerobic metabolism. Here, we provide a test of this hypothesis in an insect model system (Thaumatotibia leucotreta) by experimental manipulation of oxygen availability while measuring metabolic rate, critical thermal minimum (CTmin), supercooling point and changes in 43 metabolites in moth larvae at three key timepoints (before, during and after chill coma). Furthermore, we determined the critical oxygen partial pressure below which metabolic rate was suppressed (c. 4.5 kPa). Results showed that altering oxygen availability did not affect (non-lethal) CTmin nor (lethal) supercooling point. Metabolomic profiling revealed the upregulation of anaerobic metabolites and alterations in concentrations of citric acid cycle intermediates during and after chill coma exposure. Hypoxia exacerbated the anaerobic metabolite responses induced by low temperatures. These results suggest that cold tolerance of T. leucotreta larvae is not set by oxygen limitation, and that anaerobic metabolism in these larvae may contribute to their ability to survive in necrotic fruit.
- ItemDoes oxygen limit thermal tolerance in arthropods? A critical review of current evidence(Elsevier, 2016) Verbeck, Wilco C. E. P.; Overgaard, Johannes; Ern, Rasmus; Bayley, Mark; Wang, Tobias; Boardman, Leigh; Terblanche, John S.Over the last decade, numerous studies have investigated the role of oxygen in setting thermal tolerance in aquatic animals, and there has been particular focus on arthropods. Arthropods comprise one of the most species-rich taxonomic groups on Earth, and display great diversity in the modes of ventilation, circulation, blood oxygen transport,with representatives living both in water (mainly crustaceans) and on land (mainly insects). The oxygen and capacity limitation of thermal tolerance (OCLTT) hypothesis proposes that the temperature dependent performance curve of animals is shaped by the capacity for oxygen delivery in relation to oxygen demand. If correct, oxygen limitation could provide a mechanistic framework to understand and predict both current and future impacts of rapidly changing climate. In arthropods, most studies testing the OCLTT hypothesis have considered tolerance to thermal extremes. These studies likely operate from the philosophical viewpoint that if the model can predict these critical thermal limits, then it is more likely to also explain loss of performance at less extreme, non-lethal temperatures, for which much less data is available. Nevertheless, the extent to which lethal temperatures are influenced by limitations in oxygen supply remains unresolved. Here we critically evaluate the support and universal applicability for oxygen limitation being involved in lethal temperatures in crustaceans and insects. The relatively few studies investigating the OCLTT hypothesis at low temperature do not support a universal role for oxygen in setting the lower thermal limits in arthropods.With respect to upper thermal limits, the evidence supporting OCLTT is stronger for species relying on underwater gas exchange, while the support for OCLTT in airbreathers is weak. Overall, strongest support was found for increased anaerobic metabolism close to thermal maxima. In contrast, there was only mixed support for the prediction that aerobic scope decreases near critical temperatures, a key feature of the OCLTT hypothesis. In air-breathers, only severe hypoxia (b2 kPa) affected heat tolerance. The discrepancies for heat tolerance between aquatic and terrestrial organisms can to some extent be reconciled by differences in the capacity to increase oxygen transport. As air-breathing arthropods are unlikely to become oxygen limited under normoxia (especially at rest), the oxygen limitation component in OCLTT does not seem to provide sufficient information to explain lethal temperatures. Nevertheless, many animals may simultaneously face hypoxia and thermal extremes and the combination of these potential stressors is particularly relevant for aquatic organisms where hypoxia (and hyperoxia) is more prevalent. In conclusion, whether taxa show oxygen limitation at thermal extremes may be contingent on their capacity to regulate oxygen uptake, which in turn is linked to their respiratory medium (air vs. water). Fruitful directions for future research include testingmultiple predictions of OCLTT in the same species. Additionally, we call for greater research efforts towards studying the role of oxygen in thermal limitation of animal performance at less extreme, sub-lethal temperatures, necessitating studies over longer timescales and evaluating whether oxygen becomes limiting for animals to meet energetic demands associated with feeding, digestion and locomotion.
- ItemEffects of within-generation thermal history on the flight performance of Ceratitis capitata : colder is better(The Company of Biologists, 2014-07) Esterhuizen, Nanike; Clusella-Trullas, Susana; Van Daalen, Corne E.; Schoombie, Ruben E.; Boardman, Leigh; Terblanche, John S.The influence of thermal history on temperature-dependent flight performance was investigated in an invasive agricultural pest insect, Ceratitis capitata (Diptera: Tephritidae). Flies were exposed to one of four developmental acclimation temperatures (Tacc: 15, 20, 25, 30°C) during their pupal stage and tested at these temperatures (Ttest) as adults using a full-factorial study design. Major factors influencing flight performance included sex, body mass, Ttest and the interaction between Ttest and Tacc. Successful flight performance increased with increasing Ttest across all acclimation groups (from 10% at 15°C to 77% at 30°C). Although Tacc did not affect flight performance independently, it did have a significant interaction effect with Ttest. Multiple comparisons showed that flies which had been acclimated to 15°C and 20°C performed better than those acclimated to 25°C and 30°C when tested at cold temperatures, but warm-acclimated flies did not outperform cold-acclimated flies at warmer temperatures. This provides partial support for the ‘colder is better’ hypothesis. To explain these results, several flight-related traits were examined to determine whether Tacc influenced flight performance as a consequence of changes in body or wing morphology, whole-animal metabolic rate or cytochrome c oxidase enzyme activity. Although significant effects of Tacc could be detected in several of the traits examined, with an emphasis on sex-related differences, increased flight performance could not be explained solely on the basis of changes in any of these traits. Overall, these results are important for understanding dispersal physiology despite the fact that the mechanisms of acclimation-related changes in flight performance remain unresolved.
- ItemHigh metabolic and water-loss rates in caterpillar aggregations : evidence against the resource-conservation hypothesis(Company of Biologists, 2013) Schoombie, Ruben E.; Boardman, Leigh; Groenewald, Berlize; Glazier, Douglas S.; Van Daalen, Corne E.; Clusella-Trullas, Susana; Terblanche, John S.Several hypotheses have been proposed for explaining animal aggregation, including energy or water conservation. However, these physiological hypotheses have not been well investigated. Here, we report the effects of aggregation on metabolic (Embedded Image) and evaporative water-loss rates (Embedded Image) of the gregarious caterpillar Eutricha capensis, by comparing individuals and groups of individuals (N=10–100). Contrary to findings from previous physiological studies, we did not find an advantage to aggregation: unexpectedly, Embedded Image and Embedded Image did not decrease with increasing group size. Embedded Image and Embedded Image generally remained constant or increased in larger groups relative to individuals. The amount of water lost per unit of CO2 exchanged (Embedded Image: Embedded Image ratio) showed a marked increase in grouped caterpillars, particularly in larger groups. Other benefits of aggregation (e.g. reduced predation or increased growth rates) likely outweigh these potential costs, because individuals of E. capensis aggregate voluntarily despite no obvious energetic or hygric advantage, and other potentially confounding group effects (e.g. increased thermoregulatory advantage or whole-animal activity) are inconsequential. The results of this study provide an important exception to physiological studies reporting enhanced energy or water conservation in animal groups.
- ItemInteractions between controlled atmospheres and low temperature tolerance : a review of biochemical mechanisms(Frontiers Media, 2011-12-02) Boardman, Leigh; Sorensen, Jesper Givskov; Johnson, Shelley A.; Terblanche, John S.Controlled atmosphere treatments using carbon dioxide, oxygen, and/or nitrogen, together with controlled temperature and humidity, form an important method for post-harvest sterilization against insect-infested fruit. However, in insects, the cross tolerance and biochemical interactions between the various stresses of modified gas conditions and low temperature may either elicit or block standard stress responses which can potentiate (or limit) lethal low temperature exposure. Thus, the success of such treatments is sometimes erratic and does not always result in the desired pest mortality. This review focuses on the biochemical modes of action whereby controlled atmospheres affect insects low temperature tolerance, making them more (or occasionally, less) susceptible to cold sterilization. Insights into the integrated biochemical modes of action may be used together with the pests’ low temperature tolerance physiology to determine which treatments may be of value in post-harvest sterilization.
- ItemOxygen safety margins set thermal limits in an insect model system(The Company of Biologists, 2015-03) Boardman, Leigh; Terblanche, John S.A mismatch between oxygen availability and metabolic demand may constrain thermal tolerance. While considerable support for this idea has been found in marine organisms, results from insects are equivocal and raise the possibility that mode of gas exchange, oxygen safety margins and the physico-chemical properties of the gas medium influence heat tolerance estimates. Here, we examined critical thermal maximum (CTmax) and aerobic scope under altered oxygen supply and in two life stages that varied in metabolic demand in Bombyx mori (Lepidoptera: Bombycidae). We also systematically examined the influence of changes in gas properties on CTmax. Larvae have a lower oxygen safety margin (higher critical oxygen partial pressure at which metabolism is suppressed relative to metabolic demand) and significantly higher CTmax under normoxia than pupae (53°C vs 50°C). Larvae, but not pupae, were oxygen limited with hypoxia (2.5 kPa) decreasing CTmax significantly from 53 to 51°C. Humidifying hypoxic air relieved the oxygen limitation effect on CTmax in larvae, whereas variation in other gas properties did not affect CTmax. Our data suggest that oxygen safety margins set thermal limits in air-breathing invertebrates and the magnitude of this effect potentially reconciles differences in oxygen limitation effects on thermal tolerance found among diverse taxa to date.
- ItemPhysiological mechanisms of dehydration tolerance contribute to the invasion potential of ceratitis capitata (Wiedemann) (Diptera: Tephritidae) relative to its less widely distributed congeners(BioMed Central, 2016) Weldon, Christopher W.; Boardman, Leigh; Marlin, Danica; Terblanche, John S.Background: The Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) is a highly invasive species now with an almost cosmopolitan distribution. Two other damaging, polyphagous and closely-related species, the marula fruit fly, Ceratitis cosyra (Walker), and the Natal fly, Ceratitis rosa Karsch, are not established outside of sub-Saharan Africa. In this study, adult water balance traits and nutritional body composition were measured in all three species at different temperatures and levels of relative humidity to determine whether tolerance of water stress may partially explain their distribution. Results: Adult C. capitata exhibited higher desiccation resistance than C. rosa but not C. cosyra. Desiccation resistance of C. capitata was associated with lower rates of water loss under hot and dry conditions, higher dehydration tolerance, and higher lipid reserves that were catabolised during water stress. In comparison with C. capitata, C. cosyra and C. rosa lost water at significantly higher rates under hot, dry conditions, and did not catabolise lipids or other sources of metabolic water during water stress. Conclusions: These results suggest that adult physiological traits permitting higher tolerance of water stress play a role in the success of C. capitata, particularly relative to C. rosa. The distribution of C. cosyra is likely determined by the interaction of temperature with water stress, as well as the availability of suitable hosts for larval development.