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

Authors: WALTER, RIKKI - North Dakota State University; Rinehart, Joseph - Joe; DILLON, MICHAEL - University Of Wyoming; GREENLEE, KENDRA - University Of North Dakota

Submitted to: Journal of Insect Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/11/2021
Publication Date: 8/14/2021
Citation: Walter, R.M., Rinehart, J.P., Dillon, M.E., Greenlee, K.J. 2021. Size constrains oxygen delivery capacity within but not between bumble bee castes. Journal of Insect Physiology. 134. Article 104297. https://doi.org/10.1016/j.jinsphys.2021.104297.
DOI: https://doi.org/10.1016/j.jinsphys.2021.104297

Interpretive Summary: Bumble bees live in small colonies where the worker bees are 3-4 times smaller than the queens. The workers regularly forage for food, which requires a large use of energy, and consequentially requires a large tracheal system, which in insects is a structure that delivers oxygen throughout their body since the blood of most insects cannot carry oxygen. Conversely, queens only fly for short periods in the fall and spring, and thus have relatively smaller tracheal systems, with much of their body devoted to egg production. However, negative consequences of a smaller tracheal system, including a reduced tolerance to low oxygen conditions, have been hypothesized, but have yet to be proven. Hence, we determined the lowest level of oxygen concentrations required for workers and queens at rest and during flight. Although these levels would not be encountered under natural conditions, they are an indicator of how the tracheal system performs in an insect. Our results showed that although the lowest tolerated level differed by body size for both worker and queen bees, there was no significant difference in the lowest tolerated level of workers and queens, except under extreme conditions. This suggests that queen bumble bees pay little cost for filling body space with eggs rather than tracheal structures.

Technical 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 hypoxia tolerance. However, these morphological measurements only indirectly point to differences in hypoxia tolerance. To directly assess size- and caste-related differences in tolerance to low oxygen, we measured critical PO2 (Pcrit; 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 Pcrit during both rest and flight. However, during flight in oxygen levels near the Pcrit, 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.