Abstract

The conservation of insect pollinators is drawing attention because of reported declines in bee species and the ‘ecosystem services’ they provide. This issue has been brought to a head by recent devastating losses of honey bees throughout North America (so called, ‘Colony Collapse Disorder’); yet, we still have little understanding of the cause(s) of bee declines. Wild bumble bees (Bombus spp.) have also suffered serious declines and circumstantial evidence suggests that pathogen ‘spillover’ from commercially reared bumble bees, which are used extensively to pollinate greenhouse crops, is a possible cause. We constructed a spatially explicit model of pathogen spillover in bumble bees and, using laboratory experiments and the literature, estimated parameter values for the spillover of Crithidia bombi, a destructive pathogen commonly found in commercial Bombus. We also monitored wild bumble bee populations near greenhouses for evidence of pathogen spillover, and compared the fit of our model to patterns of C. bombi infection observed in the field. Our model predicts that, during the first three months of spillover, transmission from commercial hives would infect up to 20% of wild bumble bees within 2 km of the greenhouse. However, a travelling wave of disease is predicted to form suddenly, infecting up to 35–100% of wild Bombus, and spread away from the greenhouse at a rate of 2 km/wk. In the field, although we did not observe a large epizootic wave of infection, the prevalences of C. bombi near greenhouses were consistent with our model. Indeed, we found that spillover has allowed C. bombi to invade several wild bumble bee species near greenhouses. Given the available evidence, it is likely that pathogen spillover from commercial bees is contributing to the ongoing decline of wild Bombus in North America. Improved management of domestic bees, for example by reducing their parasite loads and their overlap with wild congeners, could diminish or even eliminate pathogen spillover.

Highlights

  • Pathogen outbreaks often occur when anthropogenic change brings wildlife into increased contact with humans and domestic animals [1,2,3]

  • Pathogen spillover as envisioned in our model requires that infected commercial bumble bees escape from greenhouses and contaminate the local environment with infectious particles

  • In order to test the predictions of our model, we investigated the prevalence of the pathogen C. bombi among bumble bees at varying distances to three industrial-scale greenhouse operations

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Summary

Introduction

Pathogen outbreaks often occur when anthropogenic change brings wildlife into increased contact with humans and domestic animals [1,2,3]. Due to spillover from commercial bees, C. bombi is becoming established in wild bumble bee populations and may be contributing to the recent declines of certain Bombus species. Halving the estimated rate at which C. bombi breaks down on flowers (Figure S1A), or doubling the rate of C. bombi deposition on flowers (Figure S1B) or transmission from flowers (Figure S1C), causes the late-season wave of infection to increase by 4–5 times (from ,20% to ,90%) This implies that, all else being equal, pathogen species that remain in the environment (decay slowly) as durable spores could spread extensively if introduced into wild populations. A five order-of-magnitude change in the diffusion rate of hosts and pathogens increases the peak prevalence of infection by, at most, ,30% (Figure S1E) These sensitivity analyses indicate that for each of our model parameters there is a threshold value below which no wave of infection is predicted

Results
Discussion
Materials and Methods
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