Size constrains oxygen delivery capacity within but not between bumble bee castes

Rikki M Walter; Joseph P Rinehart; Michael E Dillon; Kendra J Greenlee

doi:10.1016/j.jinsphys.2021.104297

Size constrains oxygen delivery capacity within but not between bumble bee castes

J Insect Physiol. 2021 Oct:134:104297. doi: 10.1016/j.jinsphys.2021.104297. Epub 2021 Aug 14.

Authors

Rikki M Walter¹, Joseph P Rinehart², Michael E Dillon³, Kendra J Greenlee⁴

Affiliations

¹ Department of Biological Sciences, North Dakota State University, Fargo, ND 58108-6050, USA.
² Agricultural Research Service, Insect Genetics and Biochemistry, United States Department of Agriculture, Fargo, ND 58102-2765, USA.
³ Department of Zoology and Physiology and Program in Ecology, University of Wyoming, Laramie, WY 82071, USA.
⁴ Department of Biological Sciences, North Dakota State University, Fargo, ND 58108-6050, USA. Electronic address: kendra.greenlee@ndsu.edu.

PMID: 34403656
DOI: 10.1016/j.jinsphys.2021.104297

Abstract

Bumble bees are eusocial, with distinct worker and queen castes that vary strikingly in size and life-history. The smaller workers rely on energetically-demanding foraging flights to collect resources for rearing brood. Queens can be 3 to 4 times larger than workers, flying only for short periods in fall and again in spring after overwintering underground. These differences between castes in size and life history may be reflected in hypoxia tolerance. When oxygen demand exceeds supply, oxygen delivery to the tissues can be compromised. Previous work revealed hypermetric scaling of tracheal system volume of worker bumble bees (Bombus impatiens); larger workers had much larger tracheal volumes, likely to facilitate oxygen delivery over longer distances. Despite their much larger size, queens had relatively small tracheal volumes, potentially limiting their ability to deliver oxygen and reducing their ability to respond to hypoxia. However, these morphological measurements only indirectly point to differences in respiratory capacity. To directly assess size- and caste-related differences in tolerance to low oxygen, we measured critical PO₂ (P_crit; the ambient oxygen level below which metabolism cannot be maintained) during both rest and flight of worker and queen bumble bees. Queens and workers had similar P_crit values during both rest and flight. However, during flight in oxygen levels near the P_crit, mass-specific metabolic rates declined precipitously with mass both across and within castes, suggesting strong size limitations on oxygen delivery, but only during extreme conditions, when demand is high and supply is low. Together, these data suggest that the comparatively small tracheal systems of queen bumble bees do not limit their ability to deliver oxygen except in extreme conditions; they pay little cost for filling body space with eggs rather than tracheal structures.

Keywords: Critical PO(2); Flight; Hypoxia; Insect; Metabolism; Pollinator.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Bees* / metabolism
Bees* / physiology
Flight, Animal / physiology*
Hypoxia
Oxygen / metabolism*
Respiration
Respiratory Physiological Phenomena

Substances

Oxygen