Jon F. Harrison

Responses of terrestrial insects to hypoxia or hyperoxia.

Oxygen is critically important for catabolic ATP generation but is also a dangerous source of reactive oxygen species. Insects respond to short-term exposure to hypoxia or hyperoxia with compensatory changes in spiracular opening and ventilation that reduce variation in internal Po2. Below critical Po2 values (Pc), nitric oxide and hypoxia inducible factor (HIF)-mediated pathways induce long-term responses such as compensatory tracheal growth, suppressed development, and acclimation of ventilation. Pc values are strongly affected by activity and ontogeny, due to changes in the ratio of tracheal conductance to metabolic rate. Although growth rates and development are suppressed by significant hypoxia in all species studied to date, adult body size is only affected in some species. Severe hyperoxia causes major oxidative stress and reduces survival, while moderate hyperoxia increases development times and body sizes in some species by unknown mechanisms.

Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster.

Although higher temperatures strongly stimulate ectothermic metabolic rates, they only slightly increase oxygen diffusion rates and decrease oxygen solubility. Consequently, we predicted that insect gas exchange systems would have more difficulty meeting tissue oxygen demands at higher temperatures. In this study, Drosophila melanogaster were reared from egg to adult in hyperoxic (40%), hypoxic (10%), and normoxic (21%) conditions and in temperatures ranging from 15°–31.5°C to examine the interactive effect of temperature and oxygen on development. Hyperoxia generally increased mass and growth rate at higher rearing temperatures. At lower rearing temperatures, however, hyperoxia had a very small effect on mass, did not affect growth rate, and lengthened time to eclosion. Relative to normoxia, flies reared in hypoxic conditions were generally smaller (mass and thorax length), had longer eclosion times, slower growth rates, and reduced survival. At cooler temperatures, hypoxia had relatively modest or nonsignificant effects on development, while at higher temperatures, the effects of hypoxia were large. These results suggest that higher temperatures reduce oxygen delivery capacity relative to tissue oxygen needs, which may partially explain why ectotherms are smaller when development occurs at higher temperatures.

Development of respiratory function in the American locust Schistocerca americana I. Across-instar effects

SUMMARY We tested the hypothesis that oxygen delivery from the atmosphere to the tissues becomes more difficult as grasshoppers increase in body size throughout development due to increases in tracheal length. If this is true, then older, larger grasshoppers should have smaller safety margins [higher critical oxygen partial pressures (PO2s)] for oxygen delivery than younger, smaller grasshoppers. We exposed grasshoppers of first, third and fifth instars and adults to decreasing levels of atmospheric O2 and measured their ventilatory responses. Contrary to our prediction, we found that larger grasshoppers had critical PO2s eight times lower than juveniles due in part to their threefold lower mass-specific metabolic rates and their ability to quadruple convective gas exchange. Adults more than doubled abdominal pumping frequency and increased tidal volume by 25% as PO2 decreased fourfold, whereas the youngest juveniles showed no such responses. This study indicates that juveniles may be more susceptible to hypoxia in natural situations, such as exposure to high altitude or restricted burrows. Also, larger size is not necessarily correlated with a smaller safety margin for oxygen delivery in insects.

Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism

Recent studies have suggested that Paleozoic hyperoxia enabled animal gigantism, and the subsequent hypoxia drove a reduction in animal size. This evolutionary hypothesis depends on the argument that gas exchange in many invertebrates and skin-breathing vertebrates becomes compromised at large sizes because of distance effects on diffusion. In contrast to vertebrates, which use respiratory and circulatory systems in series, gas exchange in insects is almost exclusively determined by the tracheal system, providing a particularly suitable model to investigate possible limitations of oxygen delivery on size. In this study, we used synchrotron x-ray phase–contrast imaging to visualize the tracheal system and quantify its dimensions in four species of darkling beetles varying in mass by 3 orders of magnitude. We document that, in striking contrast to the pattern observed in vertebrates, larger insects devote a greater fraction of their body to the respiratory system, as tracheal volume scaled with mass1.29. The trend is greatest in the legs; the cross-sectional area of the trachea penetrating the leg orifice scaled with mass1.02, whereas the cross-sectional area of the leg orifice scaled with mass0.77. These trends suggest the space available for tracheae within the leg may ultimately limit the maximum size of extant beetles. Because the size of the tracheal system can be reduced when oxygen supply is increased, hyperoxia, as occurred during late Carboniferous and early Permian, may have facilitated the evolution of giant insects by allowing limbs to reach larger sizes before the tracheal system became limited by spatial constraints.

Achievement of Thermal Stability by Varying Metabolic Heat Production in Flying Honeybees

Thermoregulation of the thorax allows endothermic insects to achieve power outputs during flight that are among the highest in the animal kingdom. Flying endothermic insects, including the honeybee Apis mellifera, are believed to thermoregulate almost exclusively by varying heat loss. Here it is shown that a rise in air temperature from 20° to 40°C causes large decreases in metabolic heat production and wing-beat frequency in honeybees during hovering, agitated, or loaded flight. Thus, variation in heat production may be the primary mechanism for achieving thermal stability in flying honeybees, and this mechanism may occur commonly in endothermic insects.

Atmospheric oxygen level and the evolution of insect body size

Insects are small relative to vertebrates, possibly owing to limitations or costs associated with their blind-ended tracheal respiratory system. The giant insects of the late Palaeozoic occurred when atmospheric PO2 (aPO2) was hyperoxic, supporting a role for oxygen in the evolution of insect body size. The paucity of the insect fossil record and the complex interactions between atmospheric oxygen level, organisms and their communities makes it impossible to definitively accept or reject the historical oxygen-size link, and multiple alternative hypotheses exist. However, a variety of recent empirical findings support a link between oxygen and insect size, including: (i) most insects develop smaller body sizes in hypoxia, and some develop and evolve larger sizes in hyperoxia; (ii) insects developmentally and evolutionarily reduce their proportional investment in the tracheal system when living in higher aPO2, suggesting that there are significant costs associated with tracheal system structure and function; and (iii) larger insects invest more of their body in the tracheal system, potentially leading to greater effects of aPO2 on larger insects. Together, these provide a wealth of plausible mechanisms by which tracheal oxygen delivery may be centrally involved in setting the relatively small size of insects and for hyperoxia-enabled Palaeozoic gigantism.

INTERPRETING REJECTIONS OF THE BENEFICIAL ACCLIMATION HYPOTHESIS: WHEN IS PHYSIOLOGICAL PLASTICITY ADAPTIVE?

Abstract.— Although many studies testing the beneficial acclimation hypothesis have rejected it, what these rejections imply about the adaptive value of physiological change remains unclear. Uncertainty arises because the hypothesis focuses on the relative performance of organisms exposed to one environment versus another, whereas the raw material available to evolution is variation in acclimation responses of individual traits. This mismatch is problematic when organisms are exposed to poor environments. In poor environments, the adaptive or maladaptive value of changes in individual traits may be obscured by long‐term decrements in organismal condition. A better match between the evolutionary pressures shaping acclimation and the tests used to examine them can be achieved by focusing on the fitness consequences of acclimation changes in individual traits.

Real-time phase-contrast x-ray imaging: a new technique for the study of animal form and function

BackgroundDespite advances in imaging techniques, real-time visualization of the structure and dynamics of tissues and organs inside small living animals has remained elusive. Recently, we have been using synchrotron x-rays to visualize the internal anatomy of millimeter-sized opaque, living animals. This technique takes advantage of partially-coherent x-rays and diffraction to enable clear visualization of internal soft tissue not viewable via conventional absorption radiography. However, because higher quality images require greater x-ray fluxes, there exists an inherent tradeoff between image quality and tissue damage.ResultsWe evaluated the tradeoff between image quality and harm to the animal by determining the impact of targeted synchrotron x-rays on insect physiology, behavior and survival. Using 25 keV x-rays at a flux density of 80 μW/mm-2, high quality video-rate images can be obtained without major detrimental effects on the insects for multiple minutes, a duration sufficient for many physiological studies. At this setting, insects do not heat up. Additionally, we demonstrate the range of uses of synchrotron phase-contrast imaging by showing high-resolution images of internal anatomy and observations of labeled food movement during ingestion and digestion.ConclusionSynchrotron x-ray phase contrast imaging has the potential to revolutionize the study of physiology and internal biomechanics in small animals. This is the only generally applicable technique that has the necessary spatial and temporal resolutions, penetrating power, and sensitivity to soft tissue that is required to visualize the internal physiology of living animals on the scale from millimeters to microns.

Heavy Livestock Grazing Promotes Locust Outbreaks by Lowering Plant Nitrogen Content

Locust Heaven Locust outbreaks have severe consequences for agriculture, but the conditions that promote an outbreak are unknown. Cease et al. (p. 467) investigated aspects of the locust diet and found that increased nitrogen content of cereal grasses reduced the size and viability of a herbivorous locust species. This locust prefers low N plants, which result from heavy grazing by livestock and erosion. High-protein plants inhibit locust swarming, which explains why grazed systems are more prone to outbreaks. Current paradigms generally assume that increased plant nitrogen (N) should enhance herbivore performance by relieving protein limitation, increasing herbivorous insect populations. We show, in contrast to this scenario, that host plant N enrichment and high-protein artificial diets decreased the size and viability of Oedaleus asiaticus, a dominant locust of north Asian grasslands. This locust preferred plants with low N content and artificial diets with low protein and high carbohydrate content. Plant N content was lowest and locust abundance highest in heavily livestock-grazed fields where soils were N-depleted, likely due to enhanced erosion. These results suggest that heavy livestock grazing and consequent steppe degradation in the Eurasian grassland promote outbreaks of this locust by reducing plant protein content.

Ecological and Environmental Physiology of Insects

1. Introduction 2. Basic insect functional anatomy and physiological principles 3. Temperature 4. Water 5. Nutrition, growth, and size 6. Oxygen 7. Techniques and applications 8. Conclusions and future directions References Index