Long-Term Temporal Trends of Nosema spp. Infection Prevalence in Northeast Germany: Continuous Spread of Nosema ceranae, an Emerging Pathogen of Honey Bees (Apis mellifera), but No General Replacement of Nosema apis.

Sebastian Gisder,Lennart L Horchler,Vivian Schüler,Detlef Groth,Elke Genersch

doi:10.3389/fcimb.2017.00301

Sebastian Gisder, Lennart L Horchler + Show 3 more

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https://doi.org/10.3389/fcimb.2017.00301

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Abstract

The Western honey bee (Apis mellifera) is widely used as commercial pollinator in worldwide agriculture and, therefore, plays an important role in global food security. Among the parasites and pathogens threatening health and survival of honey bees are two species of microsporidia, Nosema apis and Nosema ceranae. Nosema ceranae is considered an emerging pathogen of the Western honey bee. Reports on the spread of N. ceranae suggested that this presumably highly virulent species is replacing its more benign congener N. apis in the global A. mellifera population. We here present a 12 year longitudinal cohort study on the prevalence of N. apis and N. ceranae in Northeast Germany. Between 2005 and 2016, a cohort of about 230 honey bee colonies originating from 23 apiaries was sampled twice a year (spring and autumn) resulting in a total of 5,600 bee samples which were subjected to microscopic and molecular analysis for determining the presence of infections with N. apis or/and N. ceranae. Throughout the entire study period, both N. apis- and N. ceranae-infections could be diagnosed within the cohort. Logistic regression analysis of the prevalence data demonstrated a significant increase of N. ceranae-infections over the last 12 years, both in autumn (reflecting the development during the summer) and in spring (reflecting the development over winter) samples. Cell culture experiments confirmed that N. ceranae has a higher proliferative potential than N. apis at 27° and 33°C potentially explaining the increase in N. ceranae prevalence during summer. In autumn, characterized by generally low infection prevalence, this increase was accompanied by a significant decrease in N. apis-infection prevalence. In contrast, in spring, the season with a higher prevalence of infection, no significant decrease of N. apis infections despite a significant increase in N. ceranae infections could be observed. Therefore, our data do not support a general advantage of N. ceranae over N. apis and an overall replacement of N. apis by N. ceranae in the studied honey bee population.

Highlights

The Western honey bee Apis mellifera is a valuable generalist pollinator for many flowering plants in both natural and agricultural ecosystems
The huge data set on Nosema spp.-infection prevalence in Northeast Germany, which was generated during the 12 year longitudinal cohort study, provided a unique opportunity for a comprehensive analysis of the spread and success of Nosema spp., and especially of N. ceranae, in a restricted honey bee population
Molecular species differentiation of all Nosema spp.-positive samples enabled analysing the seasonality of N. apis, N. ceranae, and co-infections (Table 1)

Summary

Introduction

The Western honey bee Apis mellifera is a valuable generalist pollinator for many flowering plants in both natural and agricultural ecosystems. The cultivation of pollinator-dependent crops is expanding all over the world; there is an increasing demand for insect pollination in worldwide agriculture (Aizen et al, 2008, 2009; Aizen and Harder, 2009). This demand is partially met by a globally increasing number of managed honey bee colonies (Aizen et al, 2008, 2009; Moritz and Erler, 2016), increasing problems with honey bee health resulting in severe honey bee colony losses pose a serious threat to human food security. Among the pathogens studied and discussed in this context are two microsporidian parasites, Nosema apis (N. apis) and N. ceranae, (Cox-Foster et al, 2007; Higes et al, 2008; Genersch, 2010) which infect adult honey bees (Bailey, 1955)

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