A stressful shortness of breath: molting disrupts breathing in the mayfly <i>Cloeon dipterum</i>

Camp, Allison A.; Funk, David H.; Buchwalter, David B.

doi:10.1086/677899

Cited by 33 publications

(26 citation statements)

References 28 publications

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“…A rigorous test of the ODIM hypothesis requires that only growth-stage observations are included in the analysis because oxygen limitation should become apparent during growth, whereas respiration and metabolism may be reduced by other reasons during moulting (cf. Camp et al, 2014) (Figs 2 and 3). The importance of including only growth-stage data in tests of the ODIM hypothesis is highlighted by the sensitivity of conclusions to the inclusion of post-growth data in the final (V) larval instar.…”

Section: Discussionmentioning

confidence: 92%

“…At the cessation of growth, the gut is purged and moulting begins (except in the final instar where the wandering stage begins after gut purging), which results in changes in MR independently of the ODIM mechanism (cf. Camp et al, 2014) (Figs 2 and 3). Therefore, it is necessary to exclude post-growth observations when testing the ODIM hypothesis, as we did here.…”

Section: Discussionmentioning

confidence: 92%

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Do respiratory limitations affect metabolism of insect larvae before moulting: an empirical test at the individual level

Kivelä

Lehmann

Gotthard

2016

Journal of Experimental Biology

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Recent data suggest that oxygen limitation may induce moulting in larval insects. This oxygen-dependent induction of moulting (ODIM) hypothesis stems from the fact that the tracheal respiratory system of insects grows primarily at moults, whereas tissue mass increases massively between moults. This may result in a mismatch between oxygen supply and demand at the end of each larval instar because oxygen demand of growing tissues exceeds the relatively fixed supply capacity of the respiratory system. The ODIM hypothesis predicts that, within larval instars, respiration and metabolic rates of an individual larva first increase with increasing body mass but eventually level off once the supply capacity of the tracheal system starts to constrain metabolism. Here, we provide the first individuallevel test of this key prediction of the ODIM hypothesis. We use a novel methodology where we repeatedly measure respiration and metabolic rates throughout the penultimate-and final-instar larvae in the butterfly Pieris napi. In the penultimate instar, respiration and metabolic rates gradually decelerated along with growth, supporting the ODIM hypothesis. However, respiration and metabolic rates increased linearly during growth in the final instar, contradicting the prediction. Moreover, our data suggest considerable variation among individuals in the association between respiration rate and mass in the final instar. Overall, the results provide partial support for the ODIM hypothesis and suggest that oxygen limitation may emerge gradually within a larval instar. The results also suggest that there may be different moult induction mechanisms in larva-to-larva moults compared with the final metamorphic moult.

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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 92%

Do respiratory limitations affect metabolism of insect larvae before moulting: an empirical test at the individual level

Kivelä

Lehmann

Gotthard

2016

Journal of Experimental Biology

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“…However, our results do suggest that oxygen limitation may indeed play a significant role when N. triangulifer larvae are warmed beyond their ecologically relevant thermal limit up to their acutely tolerated temperatures. It is also possible that the respiratory challenge observed during the molt (Camp et al, 2014) may introduce transient oxygen limitation, which may become more important as larvae age. The field of toxicology has long realized that mechanisms associated with acute and chronic toxicity may be very different.…”

Section: Discussionmentioning

confidence: 99%

“…To examine the effect of temperature on oxygen consumption rates, we used a fiber-optic-based, intermittent flow respirometry system (Loligo Systems, Tjele, Demnark) as described previously (Camp et al, 2014). We examined oxygen consumption in larvae subjected to a thermal ramp of 1°C h −1 , beginning at their rearing temperature of 22.0±1.0°C.…”

Section: Respirometry Experimentsmentioning

confidence: 99%

Physiological responses to short-term thermal stress in mayfly (Neocloeon triangulifer) larvae in relation to upper thermal limits

Kim

Chou

Funk

et al. 2017

Journal of Experimental Biology

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Understanding species' thermal limits and their physiological determinants is critical in light of climate change and other human activities that warm freshwater ecosystems. Here, we ask whether oxygen limitation determines the chronic upper thermal limits in larvae of the mayfly Neocloeon triangulifer, an emerging model for ecological and physiological studies. Our experiments are based on a robust understanding of the upper acute (∼40°C) and chronic thermal limits of this species (>28°C, ≤30°C) derived from full life cycle rearing experiments across temperatures. We tested two related predictions derived from the hypothesis that oxygen limitation sets the chronic upper thermal limits: (1) aerobic scope declines in mayfly larvae as they approach and exceed temperatures that are chronically lethal to larvae; and (2) genes indicative of hypoxia challenge are also responsive in larvae exposed to ecologically relevant thermal limits. Neither prediction held true. We estimated aerobic scope by subtracting measurements of standard oxygen consumption rates from measurements of maximum oxygen consumption rates, the latter of which was obtained by treating with the metabolic uncoupling agent carbonyl cyanide-4-(trifluoromethoxy) pheylhydrazone (FCCP). Aerobic scope was similar in larvae held below and above chronic thermal limits. Genes indicative of oxygen limitation (LDH, EGL-9) were only upregulated under hypoxia or during exposure to temperatures beyond the chronic (and more ecologically relevant) thermal limits of this species (LDH). Our results suggest that the chronic thermal limits of this species are likely not driven by oxygen limitation, but rather are determined by other factors, e.g. bioenergetics costs. We caution against the use of short-term thermal ramping approaches to estimate critical thermal limits (CT max ) in aquatic insects because those temperatures are typically higher than those that occur in nature.

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“…When first formed, the lumen is filled with liquid, but at each larval molt this liquid, along with old cuticular lining, is excreted, a new cuticle is formed, and the lumen is filled with gas (Camp et al, 2014;Snelling et al, 2011). The presence of a mature, gas-filled lumen can be monitored by brightfield microscopy, by which the gas-filled tube contrasts strongly with the surrounding fluid-filled tissues (Fig.…”

Section: Introductionmentioning

confidence: 99%

Intracellular lumen formation in Drosophila proceeds via a novel subcellular compartment

Nikolova

Metzstein

2015

Development

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Cellular tubes have diverse morphologies, including multicellular, unicellular and subcellular architectures. Subcellular tubes are found prominently within the vertebrate vasculature, the insect breathing system and the nematode excretory apparatus, but how such tubes form is poorly understood. To characterize the cellular mechanisms of subcellular tube formation, we have refined methods of high pressure freezing/freeze substitution to prepare Drosophila larvae for transmission electron microscopic (TEM) analysis. Using our methods, we have found that subcellular tube formation may proceed through a previously undescribed multimembrane intermediate composed of vesicles bound within a novel subcellular compartment. We have also developed correlative light/TEM procedures to identify labeled cells in TEM-fixed larval samples. Using this technique, we have found that Vacuolar ATPase (V-ATPase) and the V-ATPase regulator Rabconnectin-3 are required for subcellular tube formation, probably in a step resolving the intermediate compartment into a mature lumen. In general, our ultrastructural analysis methods could be useful for a wide range of cellular investigations in Drosophila larvae.

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A stressful shortness of breath: molting disrupts breathing in the mayfly Cloeon dipterum

Cited by 33 publications

References 28 publications

Do respiratory limitations affect metabolism of insect larvae before moulting: an empirical test at the individual level

Do respiratory limitations affect metabolism of insect larvae before moulting: an empirical test at the individual level

Physiological responses to short-term thermal stress in mayfly (Neocloeon triangulifer) larvae in relation to upper thermal limits

Intracellular lumen formation in Drosophila proceeds via a novel subcellular compartment

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