Short communicationNutritional stress due to habitat loss may explain recent honeybee colony collapses
Introduction
A sudden large decline in the number of honeybees and the associated concern regarding the pollination of food crops has erupted in the public consciousness over the last few years. These so-called colony collapses have taken an appearance of something mysterious because they are most typically characterized by the loss of almost all adult bees from the colony and no dead bees inside or around it. The cause for these colony collapses has attracted a number of disparate hypotheses, including infections from newly introduced pathogens (Oldroyd, 2007). In spite of the obvious fact that disappearance of bees from colonies must involve them flying out of the hive, surprisingly little research has gone into investigating possible mechanistic explanations based on foraging behavior. Given that this ‘disappearing disease’ has been reported on numerous occasions since the 1800s and has been blamed on almost as many different factors (Underwood and van Engelsdorp, 2007), investigating such broader underlying mechanisms might be more worthwhile than looking for unique pathogens or pesticides as possible causative agents.
We have recently shown that bees infected with the protozoan Nosema ceranae have a higher hunger level than uninfected bees, suggesting that they are energetically stressed (Mayack and Naug, 2009, Naug and Gibbs, in press). Such nutritional stress is a general effect of a number of pathogenic infections and we argue that it would make infected bees more inclined to go out on foraging trips. If such infected bees in lower energetic states go out foraging, they are more likely to fail in their efforts to both reach an outside food source as well as return to the colony. For example, infection with tracheal mites has been shown to reduce the metabolic rate of bees flying in hypoxic air, demonstrating that it might constrain activities requiring the highest metabolic rates such as flying in cool weather (Harrison et al., 2001). It is also important to note here that foraging behavior in honeybees is regulated to a large extent by the nutritional status of individuals, independent of the amount of stored food in the colony (Schulz et al., 1998, Toth et al., 2005). Nutritional and energetic stress on individuals due to infection thus provides a possible mechanism for the disappearance of bees from hives that still have intact stores of honey. If nutritional stress on individuals is a major contributor to colony loss, its effects are likely to be felt most severely at times when and places where bees find it difficult to locate suitable forage. I investigated this idea by evaluating the recent land cover change in the United States brought about by increasing urbanization accompanied by the loss of cropland and natural vegetation.
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Materials and methods
The National Resources Inventory (NRI) is a statistical survey of natural resource conditions and trends in the United States that has been conduced since 1982 and 2003 is the latest year for which these data are currently published. Its land cover data consist of mutually exclusive categories such as cropland, rangeland, forest land, developed land, and water areas (NRI, 2003). I used the data for all land types except that for water because the latter is not particularly relevant to the
Results and discussion
NAAS data show that the number of honeybee colonies in the United States has steadily declined for the last 30 years, with large crashes occurring in the 1980s and 1990s (Fig. 1). Data from NRI show that during the same period there has also been a substantial decrease in the total land area devoted to cropland, pastureland and rangeland in the United States with a concurrent increase in the extent of developed land area (Fig. 2). While each land cover type is significantly correlated to the
Acknowledgements
This paper has benefited greatly from discussions with H.S. Arathi, Chris Mayack, Marla Spivak and comments from two anonymous reviewers. The research is supported by a grant from the National Science Foundation, USA.
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