Non-shivering thermogenesis in asynchronous flight muscles of bumblebees? Comparative studies on males of Bombus terrestris, Xylocopa sulcatipes and Acherontia atropos

Surholt, Bernhard; Greive, Heinrich; Baal, Thomas; Bertsch, Andreas

doi:10.1016/0300-9629(90)90116-a

Cited by 20 publications

(13 citation statements)

References 16 publications

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“…The glucose and hexose monophosphate were then isolated from the tissues and 3H and 14C radioactivities were measured (Surholt and Newsholme, 1983). Surholt et al (1990) argue that NST exists in B. terrestris queens because (1) they produce more heat than do Xylocopa bees, (2) no thoracic vibrations art detected in B. terrestris whereas thoracic vibrations are detected in a moth and in Xylocopa, and (3) high biochemical cycling rates have been found in bumblebee muscle. In marked contrast to Clark et al (1973a), who report a shutdown of cycling during flight in bumblebees, Surholt and Newsholme (1983) report a marked increase of cycling in flight in the large (2.3 g) death's-head hawkmoth Acherontia atropos.…”

Section: Bumblebees Out In the Coldmentioning

confidence: 99%

“…Nevertheless, since the thesis of NST for bumblebees is accepted as gospel truth in the general literature and since numerous biochemically oriented publications almost to the present day Surholt et al, 1990) claim that bumblebees can produce heat to elevate Tthx without shivering, it is unfortunately necessary to discuss the topic even though it is not relevant to any insect, as far as we know. Nonshivering thermogenesis, by definition, implies the absence of muscle contractions, either twitches or tetanus resulting from multiple electrical stimulation of the muscles.…”

Section: Bumblebees Out In the Coldmentioning

confidence: 99%

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The Hot-Blooded Insects

Heinrich¹

1993

321

144

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Section: Bumblebees Out In the Coldmentioning

confidence: 99%

Section: Bumblebees Out In the Coldmentioning

confidence: 99%

The Hot-Blooded Insects

Heinrich¹

1993

321

144

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“…In these muscles motor neuron spikes are at a much lower frequency than, and are not one-to-one with (i.e., are asynchronous with, although n:m phase locking can be present, Heide, 1979) the muscle contractions, with the ratio between spikes and muscle contractions ranging from 1:5-1:20 (Pringle, 1949;Roeder, 1951;Wilson and Wyman, 1963;Nachtigall and Wilson, 1967;Bastian and Esch, 1970). Another difference between these and synchronous muscles is that they contract only 3-4%, as opposed to the 8-15% commonly observed in insect muscle (Surholt et al, 1990;Gilmour and Ellington, 1993;Chan and Dickinson, 1996).…”

Section: Unique Properties Due To Acto-myosin Interaction 2: Asynchromentioning

confidence: 99%

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

Hooper

Hobbs

Thuma

2008

Progress in Neurobiology

131

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This is the second in a series of canonical reviews on invertebrate muscle. We cover here thin and thick filament structure, the molecular basis of force generation and its regulation, and two special properties of some invertebrate muscle, catch and asynchronous muscle. Invertebrate thin filaments resemble vertebrate thin filaments, although helix structure and tropomyosin arrangement show small differences. Invertebrate thick filaments, alternatively, are very different from vertebrate striated thick filaments and show great variation within invertebrates. Part of this diversity stems from variation in paramyosin content, which is greatly increased in very large diameter invertebrate thick filaments. Other of it arises from relatively small changes in filament backbone structure, which results in filaments with grossly similar myosin head placements (rotating crowns of heads every 14.5 nm) but large changes in detail (distances between heads in azimuthal registration varying from three to thousands of crowns). The lever arm basis of force generation is common to both vetebrates and invertebrates, and in some invertebrates this process is understood on the near atomic level. Invertebrate actomyosin is both thin (tropomyosin:troponin) and thick (primarily via direct Ca ++ binding to myosin) filament regulated, and most invertebrate muscles are dually regulated. These mechanisms are well understood on the molecular level, but the behavioral utility of dual regulation is less so. The phosphorylation state of the thick filament associated giant protein, twitchin, has been recently shown to be the molecular basis of catch. The molecular basis of the stretch activation underlying asynchronous muscle activity, however, remains unresolved.

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“…Bumblebees, such as the burrowing bumblebee ( Bombus terrestris ), undergo pre-flight thermogenesis to facilitate flight at low temperatures 1–4 . While this is well established, the mechanisms mediating pre-flight thermogenesis are not fully understood.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial glycerol 3-phosphate facilitates bumblebee pre-flight thermogenesis

Masson

Hedges

Devaux

et al. 2017

Sci Rep

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Bumblebees (Bombus terrestris) fly at low ambient temperatures where other insects cannot, and to do so they must pre-warm their flight muscles. While some have proposed mechanisms, none fully explain how pre-flight thermogenesis occurs. Here, we present a novel hypothesis based on the less studied mitochondrial glycerol 3-phosphate dehydrogenase pathway (mGPDH). Using calorimetry, and high resolution respirometry coupled with fluorimetry, we report substrate oxidation by mGPDH in permeabilised flight muscles operates, in vitro, at a high flux, even in the absence of ADP. This may be facilitated by an endogenous, mGPDH-mediated uncoupling of mitochondria. This uncoupling increases ETS activity, which results in increased heat release. Furthermore, passive regulation of this mechanism is achieved via dampened temperature sensitivity of mGPDH relative to other respiratory pathways, and subsequent consumption of its substrate, glycerol 3-phosphate (G3P), at low temperatures. Mitochondrial GPDH may therefore facilitate pre-flight thermogenesis through poor mitochondrial coupling. We calculate this can occur at a sufficient rate to warm flight muscles until shivering commences, and until flight muscle function is adequate for bumblebees to fly in the cold.

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Non-shivering thermogenesis in asynchronous flight muscles of bumblebees? Comparative studies on males of Bombus terrestris, Xylocopa sulcatipes and Acherontia atropos

Cited by 20 publications

References 16 publications

The Hot-Blooded Insects

The Hot-Blooded Insects

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

Mitochondrial glycerol 3-phosphate facilitates bumblebee pre-flight thermogenesis

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