The mechanics of nectar offloading in the bumblebee Bombus terrestris and implications for optimal concentrations during nectar foraging

Abstract

Nectar is a common reward provided by plants for pollinators. More concentrated nectar is more rewarding, but also more viscous, and hence more time-consuming to drink. Consequently, theory predicts an optimum concentration for maximizing energy uptake rate, dependent on the mechanics of feeding. For social pollinators such as bumblebees, another important but little-studied aspect of foraging is nectar offloading upon return to the nest. Studying the bumblebee Bombus terrestris, we found that the relationship between viscosity (µ) and volumetric transfer rates (Q) of sucrose solutions differed between drinking and offloading. For drinking, Q ∝ µ^-0.180, in good agreement with previous work. Although offloading was quicker than drinking, offloading rate decreased faster with viscosity, with Q ∝ µ^-0.502, consistent with constraints imposed by fluid flow through a tube. The difference in mechanics between drinking and offloading nectar leads to a conflict in the optimum concentration for maximizing energy transfer rates. Building a model of foraging energetics, we show that including offloading lowers the maximum rate of energy return to the nest and reduces the concentration which maximizes this rate by around 3%. Using our model, we show that published values of preferred nectar sugar concentrations suggest that bumblebees maximize the overall energy return rather than the instantaneous energy uptake during drinking.

Keywords: flow rate; honeypots; nectar; offloading; sucrose; viscosity.

Figure 1.

The experimental set-up for recording drinking and offloading rates. (Online version in colour.)

Figure 2.

Boxplots of mean sucrose transfer rates for B. terrestris bumblebees during drinking and offloading of sucrose solution of 35%, 50% and 65% w/w, expressed as volumetric and energy transfer rates. n = 10 bees per concentration; each observation (bee) is the mean of 10 foraging bouts. Boxes are interquartile ranges, thick lines are medians and crosses indicate overall means. The open circles are outliers. (a) Volumetric drinking rate, (b) volumetric offloading rate, (c) energy uptake rate, (d) energy offloading rate.

Figure 3.

Boxplots of the time spent on activities other than drinking or offloading sucrose solution during foraging behaviour. (a) Extra foraging time, i.e. the time in the flight arena not directly spent drinking. (b) Extra colony time, i.e. the time in the nest not spent offloading. n = 10 bees per concentration; each observation is the mean of 10 foraging bouts per bee. Boxplots as in figure 2.

Figure 4.

The relationship between sucrose concentration and foraging efficiency. (a) Data (circles: drinking, and crosses: offloading) and fitted models (lines) of volumetric flow rate versus viscosity for drinking and offloading of sucrose solutions. The slope for drinking, −0.180 [95% CI: −0.211, −0.148], was less steep than that for offloading, −0.502 [−0.590, −0.413]. (b) Modelled relationships for relative instantaneous energy transfer versus concentration for drinking and offloading, using the fitted (slope) parameters from (a), and assuming an air temperature of 23°C for drinking, and abdominal temperature of 27°C for offloading. These relationships give optimum concentrations for maximizing energy transfer rates of 55% for drinking and 36% for offloading. (c) The mean (±95% CI) time spent transferring 35, 50 and 65% w/w sucrose solution. The ratio of time spent drinking to offloading is approximately 17 : 1, 11 : 1 and 6 : 1 for 35, 50 and 65% sucrose solution, respectively. n = 10 bees per concentration, each observation is the mean of 10 foraging bouts per bee. (Online version in colour.)

Figure 5.

Overall energetic models for a complete foraging bout, calculated for total flight times of 100 s and 900 s and assuming a nectar (sucrose solution) load of 105 µl and bee mass of 163 mg. The rate of energy return to the nest is maximized at a sucrose concentration of 65% for a foraging bout with a flight time of 100 s and 74% for a flight time of 900 s (solid lines). The effect of excluding the viscosity dependence of sucrose offloading is illustrated by the dashed line; this is also for a flight time of 100 s but with a fixed offloading time across all concentrations and raises the concentration at which the rate of energy return is maximized to 68%. (Online version in colour.)