Consistent pollen nutritional intake drives bumble bee ( Bombus impatiens) colony growth and reproduction across different habitats

Abstract

Foraging behavior is a critical adaptation by insects to obtain appropriate nutrients from the environment for development and fitness. Bumble bees (Bombus spp.) form annual colonies which must rapidly increase their worker populations to support rearing reproductive individuals before the end of the season. Therefore, colony growth and reproduction should be dependent on the quality and quantity of pollen resources in the surrounding landscape. Our previous research found that B. impatiens foraging preferences to different plant species were shaped by pollen protein:lipid nutritional ratios (P:L), with foragers preferring pollen species with a ~5:1 P:L ratio. In this study, we placed B. impatiens colonies in three different habitats (forest, forest edge, and valley) to determine whether pollen nutritional quality collected by the colonies differed between areas that may differ in resource abundance and diversity. We found that habitat did not influence the collected pollen nutritional quality, with colonies in all three habitats collecting pollen averaging a 4:1 P:L ratio. Furthermore, there was no difference in the nutritional quality of the pollen collected by colonies that successfully reared reproductives and those that did not. We found however, that "nutritional intake," calculated as the colony-level intake rate of nutrient quantities (protein, lipid, and sugar), was strongly related to colony growth and reproductive output. Therefore, we conclude that B. impatiens colony performance is a function of the abundance of nutritionally appropriate floral resources in the surrounding landscape. Because we did not comprehensively evaluate the nutrition provided by the plant communities in each habitat, it remains to be determined how B. impatiens polylectic foraging strategies helps them select among the available pollen nutritional landscape in a variety of plant communities to obtain a balance of key macronutrients.

Keywords: colony development; colony reproduction; foraging preferences; nutritional ecology; pollen quality; pollination.

Figure 1

Field sites of the Bombus impatiens colonies that we deployed in central Pennsylvania. We placed two colonies at each site, facing opposite directions from each other (~E vs. W). The four sites in the Valley were along the field border of Penn State's Russell E. Larson Agricultural Research Center and were in a predominately agricultural landscape with two small residential neighborhoods. The four Edge sites were along the border of the research center and Rothrock State Forest. The Forest sites were placed ~5 m into the forest off Kepler Rd. in Rothrock State Forest. Photograph generated by Google Earth Pro v.7.1.5.1557

Figure 2

Distributions of protein:lipid ratios (P:L) from pollen collected from the corbiculae of individual Bombus impatiens foragers. (a) Distribution of P:L ratios of all individual forager pollen loads collected (N = 297). Bars represent total numbers of corbiculate loads found within a given P:L range. (b) Mean P:L ratios (±SE) of pollen loads for each week of the study by habitat. P:L ratios did not differ between habitats each week yet exhibited a third‐order polynomial distribution over time. The smooth line was added to show the similar trends in pollen nutrition collected by colonies throughout the season in each habitat. Smoother lines are a cubic spline with lambda of 0.1 generated by JMP Pro 13.2.0. Note that protein concentrations of pollen collected by B. impatiens differed by week while lipid concentrations did not, suggesting that P:L ratios were driven by protein concentrations of pollen collected by bumble bees (see Section 2.1, Table 1)

Figure 3

Regression of environmental variables on Bombus impatiens pollen nutrient concentrations. We conducted multiple regression on daily temperatures and time of day on pollen nutrient concentrations (shown as mean ± SE) collected by bumble bees. Protein concentrations of bumble bee‐collected pollen differed by maximum daily temperature and time of day (F _3,98  = 10.93, p < .01, R ²  = .26), while lipid concentrations did not (F _3,89  = 0.44, R ²  = .015) revealing environmental effects on bumble bee collection of pollen protein concentrations and consistent collection of pollen lipid concentrations

Figure 4

Principal component analysis for season‐long colony development, behavior, and nutrition of Bombus impatiens. PCA grouped factors associated with resource abundance and foraging behavior (pollen and nonpollen foraging rates and corbiculate pollen mass) with colony growth and reproduction (maximum biomass and biomass gain, lifetime population, reproductive success, and number of reproductives). Pollen nutrition was not correlated to colony dynamics because it did not differ between colonies (see Section 2.1) and was assigned to a second factor where lipid and sugar concentrations were negatively correlated to protein concentration and P:L ratios

Figure 5

Colony‐level nutritional intake was highly correlated to colony (a) lifetime population and (b) maximum biomass gain. Nutritional intake was calculated as colony‐level average mg lipid, protein, and sugar foraged per hour (see Section 2 for formula)

Figure 6

Nutritional intake positively affected colony reproduction. (a) Nutritional intake (mean ± SE) for lipid, protein, and sugar was higher in colonies that were reproductively “successful,” producing at least one reproductive individual. Asterisks represent statistical difference at p < .05. (b) Nutritional intake of lipid, protein, and sugar was linearly correlated to the number of reproductive individuals produced by “successful” colonies. Nutritional intake was calculated as colony‐level average mg lipid, protein, and sugar foraged per hour (see Section 2 for formula)