The influence of mid-continent agricultural land use on the health and survival of commercially managed honey bee (Apis mellifera L.) colonies

Abstract

Commercial honey bee colonies were assessed in six apiaries that varied in their land use composition, in the Prairie Pothole Region of North Dakota over three years, 2010-2013. All colonies were transported to California to pollinate almonds each fall and were transported back to North Dakota each spring. The goal of the study was to determine the factors that most influenced, and thus predicted, annual survival of colonies in the different apiaries from summer through the following spring. The factors were grouped into three levels of analysis: 1) land use surrounding the North Dakota summer apiaries, including floral availability and pesticide exposure; 2) colony-level measures of population size, pollen and honey stores, queen status, and presence and prevalence of parasites and diseases; and 3) individual bee-level measures of nutritional physiology and immunity in 7-day old nurse bees collected from healthy colonies within each apiary. Results indicated that the area of uncultivated land (including CRP lands, pasture, grassland, flowering trees and shrubs, fallow land, hayland, and ditches) exerted a significant positive influence on the annual proportion of colonies surviving among apiaries. At the colony level, the amount of brood (pupae) in September and the mean pollen (g) collected per day over the summer correlated with higher annual survival. Higher Varroa destructor mite infestation levels in September were associated with reduced overwinter survival. Individual bee measures positively influencing survival included the expression level of vitellogenin in September and abdominal lipid stores in August. The expression level of lysozyme-2 in September was related to decreased apiary survival. A final, integrated model, incorporating all of the significant factors across the three levels, revealed that all, except Varroa levels, remained significant as predictors of annual colony survival within apiaries. Varroa was actively and effectively controlled by the collaborating beekeeper; thus in this study was not an overall contributor to colony mortality. This is the first study to quantify the impact and importance of pollen nutrition; i.e., "pollen flow" from the level of landscape to the individual-bee, to the health and survivorship of colonies. The most significant predictors of health and survivorship across all three levels of analysis were all related to nutrition - beginning with abundant flowers located overwhelmingly in uncultivated lands. More and/or better forage led to greater honey production and pollen collection which in turn led to greater nutritional stores in individual bees, and an overall decreased immune response. The presence of quality and abundant forage surrounding summering locations support healthy, robust, and most importantly, surviving, colonies of honey bees.