Scott Debnam

Year of Award

2022

Document Type

Dissertation

Degree Type

Doctor of Philosophy (PhD)

Degree Name

Organismal Biology, Ecology, and Evolution

Department or School/College

Division of Biological Sciences

Committee Chair

Ragan M. Callaway

Commitee Members

Jerry J. Bromenshenk, H. Arthur Woods, Erick Greene, Colin Henderson, Marcelo A. Aizen

Keywords

Apis mellifera, brood temperature, honey use, insect physiology, metabolism, temperature regulation

Abstract

Little is known about the energetic costs to insects of raising young. Honey bees collectively raise young, or brood, through a series of complex behaviors that appear to accelerate and synchronize the timing of brood maturation. These include maintaining the brood nest at warmer and consistent temperatures and the exceptional activity of "heater bees." The temperature at which juvenile insects are raised can profoundly affect their development. Apis mellifera (Honey bees) cope with temperature-dependent development via social behavior that maintains the relatively high and constant temperatures within the nest where the brood are raised. Yet juvenile honey bee development is complex and can be categorized into egg, larvae, pupating juveniles, and pupae.

Honey bees use passive and active behaviors to maintain remarkably constant brood nest temperatures, from 33 to 35°C, across a wide range of ambient temperatures. In addition to these colony-scale behaviors, a small subset of nurse bees behaves as heater bees. Heater bees contract thoracic flight muscles to generate heat, but their thoraxes reach much higher temperatures than other bees responsible for brood care, ranging between 42 and 47°C. Heater bees focus their attention on incubating individual cells by moving among brood cells and regulating the temperatures of individual eggs, larvae, and pupae.

We constructed four sets of experimental hives to explore the developmental temperatures at which each juvenile stage is maintained, the energetic costs of raising juveniles, and the cost of heater bees. One set allowed us to record the temperatures of undisturbed young in the brood nest area established by the colony. The second set was designed to estimate the numerical allocation of individuals to the heater bee task. The third set was intended to contain only brood, which eliminated foraging and allowed us to quantify stored honey use when rearing

juveniles at 10 and 30°C. The final set was used to measure the respiration rates and energy expenditure of individual bees displaying resting, walking, heating, and agitated behavior. We first discovered that instead of simply maintaining brood nest areas at 33-35°C, honey bees provide extraordinarily precise but different temperatures for larvae and pupae. We found that the temperature at which heater bees regulate cells is above the overall average temperature range of the brood nest. Honey bees raised larvae at 36.38±0.02°C, substantially higher and with a narrower range than what has been reported for the brood nest, 33-35°C. Honey bees raised pupae at 35.18±0.04°C, also higher than the reported temperatures for the brood nest.

We further explored brood development by characterizing the developing juveniles' temperature profile throughout their entire 21-day developmental cycle. We found that eggs were maintained at 36.1 ± 0.03°C, larvae at 36.2 ± 0.02°C, pupating juveniles at 35.9 ± 0.03°C, and pupae at 35.8 ± 0.03°C. All stages were significantly different from all other stages, but importantly larvae were only 0.4°C different from pupae. We then conducted another experiment with brood frames without mature bees and in incubators at 34.5°C. Without nurse bees, the temperatures of eggs, larvae, and pupae were 34.4 ± 0.04°C, 34.7 ± 0.05°C, and 34.3 ± 0.04°C, with larvae different from all other stages, and a 0.3°C difference between larvae and pupae. When compared to the 1.2°C in Chapter 1, this 0.3°C difference suggests that heater bees may be a major driver of the differences between pupae and larvae. However, the 0.4°C difference between larvae and pupae in the second experiment reported in chapter 2, vs. the 0.3°C difference, suggests that the larvae themselves may be the major contributor to the temperature difference between the life stages. Either way, our results suggest honey bee development may involve far more precise temperature during the development of juveniles than previously known.

And finally, to determine the cost of maintaining juveniles at these warmer and more consistent temperatures, we compared the honey used by brood-only experimental colonies with whole-colony measurements of honey storage in the literature. We estimated that raising brood costs colonies half of their annual energy budgets stored as honey, or approximately 43.7±0.9 kg·yr-1. We estimated that roughly 2% of colony individuals perform the task of heater bee. Respiration rates of heater bees (19 mW) were more than those of resting bees (8 mW) but similar to those of walking bees (20 mW) and about half of those that were agitated (46 mW). The energetic cost of heating was more than an order of magnitude lower than reported values for the energetic cost of flying. By integrating data from our experimental hives, we estimate that the annual cost of raising brood is quite high; however, we estimate that heater bee behavior and physiology, though extreme, may require only about 7% of the annual honey stored by a colony.

Instead of simply maintaining brood nest areas at 33-35°C, honey bees provide extraordinarily precise but different temperatures for larvae and pupae. We do not know if these differences ultimately affect development, but they suggest that honey bees may exert far more precise control over the temperatures of their juveniles than previously known, which comes at a high cost at the colony level (macroeconomic), but a surprisingly low cost at the individual (microeconomic) heater bee level.

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