The Honey Bee Parasite Nosema ceranae: Transmissible via Food Exchange?

Michael L Smith,Stephen J Martin

doi:10.1371/journal.pone.0043319

Abstract

Nosema ceranae, a newly introduced parasite of the honey bee, Apis mellifera, is contributing to worldwide colony losses. Other Nosema species, such as N. apis, tend to be associated with increased defecation and spread via a fecal-oral pathway, but because N. ceranae does not induce defecation, it may instead be spread via an oral-oral pathway. Cages that separated older infected bees from young uninfected bees were used to test whether N. ceranae can be spread during food exchange. When cages were separated by one screen, food could be passed between the older bees and the young bees, but when separated by two screens, food could not be passed between the two cages. Young uninfected bees were also kept isolated in cages, as a solitary control. After 4 days of exposure to the older bees, and 10 days to incubate infections, young bees were more likely to be infected in the 1-Screen Test treatment vs. the 2-Screen Test treatment (P = 0.0097). Young bees fed by older bees showed a 13-fold increase in mean infection level relative to young bees not fed by older bees (1-Screen Test 40.8%; 2-Screen Test 3.4%; Solo Control 2.8%). Although fecal-oral transmission is still possible in this experimental design, oral-oral infectivity could help explain the rapid spread of N. ceranae worldwide.

Highlights

Nosema ceranae is a parasitic microsporidium that until the 1990s infected only the Asian honey bee, Apis cerana. It was first reported in the European honey bee, Apis mellifera, in Spain in 2006 [1], though later it was found in archived bee samples in the U.S dating back to 1995 [2], and in Uruguay pre-1990 [3]
In the 2-Screen Test, young bees were placed in one cage, and older infected bees were placed in an adjacent cage; the two groups were separated by 1.5 mm mesh screens spaced 0.6 cm apart for the 19 April trials, and 1.0 cm apart for the 11 May trials
Young uninfected bees that were fed by older infected bees developed N. ceranae infections at a level 13-times higher than young uninfected bees unable to feed from older infected bees

Summary

Introduction

Nosema ceranae is a parasitic microsporidium that until the 1990s infected only the Asian honey bee, Apis cerana. Filtering hairs in the bee’s proventriculus act as a one-way valve, preventing spores in the midgut from reaching the crop [15]. These hairs are capable of retaining particles as small as 0.5 mm in diameter [16]; N. ceranae spores measure 4.462.2 mm [17]. If spores are able to pass the proventriculus, and reach the crop, they could be regurgitated to other colony members during food exchange, providing a mechanism for oral-oral transmission. In the 1-Screen cages, food could be passed between infected and uninfected bees, but not in the 2Screen cages These cages reduce the likelihood of fecal-oral transmission, but cannot entirely eliminate the fecal-oral pathway. Post-treatment infection rates would be predicted to be higher in 1-Screen separated bees than in 2-Screen separated bees

Methods

Findings

Discussion