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Lifetime- and caste-specific changes in flight metabolic rate and muscle biochemistry of honeybees, Apis mellifera

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Abstract

Honeybees, Apis mellifera, who show temporal polyethism, begin their adult life performing tasks inside the hive (hive bees) and then switch to foraging when they are about 2–3 weeks old (foragers). Usually hive tasks require little or no flying, whereas foraging involves flying for several hours a day and carrying heavy loads of nectar and pollen. Flight muscles are particularly plastic organs that can respond to use and disuse, and accordingly it would be expected that adjustments in flight muscle metabolism occur throughout a bee’s life. We thus investigated changes in lifetime flight metabolic rate and flight muscle biochemistry of differently aged hive bees and of foragers with varying foraging experience. Rapid increases in flight metabolic rates early in life coincided with a switch in troponin T isoforms and increases in flight muscle maximal activities (V max) of the enzymes citrate synthase, cytochrome c oxidase, hexokinase, phosphofructokinase, and pyruvate kinase. However, further increases in flight metabolic rate in experienced foragers occurred without additional changes in the in vitro V max of these flight muscle metabolic enzymes. Estimates of in vivo flux (v) compared to maximum flux of each enzyme in vitro (fractional velocity, v/V max) suggest that most enzymes operate at a higher fraction of V max in mature foragers compared to young hive bees. Our results indicate that honeybees develop most of their flight muscle metabolic machinery early in life. Any further increases in flight metabolism with age or foraging experience are most likely achieved by operating metabolic enzymes closer to their maximal flux capacity.

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Abbreviations

CS:

Citrate synthase

COx:

Cytochrome c oxidase

HK:

Hexokinase

PFK:

Phosphofructokinase

PK:

Pyruvate kinase

V max :

Enzyme maximum activity

v :

In vivo pathway flux

v/V max :

Enzyme fractional velocity

\( V_{{{\text{CO}}_{ 2} }} \) :

Rate of carbon dioxide production

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Acknowledgments

The authors would like to thank Paul Kelly and Heather Mattila (University of Guelph), as well as Les Simonffy for generous assistance with bees; Richard Smith (McMaster University), Todd Gillis and Jordan Klaiman (University of Guelph) for technical advice on troponin T, as well as the McMaster Regional Centre for Mass Spectrometry for protein identification. This study was supported by the Natural Sciences and Engineering Research Council of Canada, Canada Foundation for Innovation, and Ontario Innovation Trust to G.B. McClelland and R. Dukas. G.B. McClelland was supported by an Early Researcher Award from the Ontario Ministry of Research and Innovation. M.-P. Schippers was the recipient of an NSERC postgraduate scholarship.

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Authors and Affiliations

  1. Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada

    Marie-Pierre Schippers & Grant B. McClelland

  2. Departments of Psychology, Neuroscience and Behaviour, McMaster University, Hamilton, ON, L8S 4K1, Canada

    Reuven Dukas

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  1. Marie-Pierre Schippers
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  2. Reuven Dukas
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  3. Grant B. McClelland
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Correspondence to Grant B. McClelland.

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Communicated by H. V. Carey.

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Schippers, MP., Dukas, R. & McClelland, G.B. Lifetime- and caste-specific changes in flight metabolic rate and muscle biochemistry of honeybees, Apis mellifera . J Comp Physiol B 180, 45–55 (2010). https://doi.org/10.1007/s00360-009-0386-9

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