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

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.

Nosema ceranae in Apis mellifera: a 12 years postdetection perspective

“…Accordingly, the apparent global advantage of N. ceranae appears not to be due to differences in spore production or infectivity (as shown by Milbrath et al ., ). The replacement of N. apis by N. ceranae is unlikely to occur due to a competitive advantage for within‐host spore production (Martín‐Hernández et al ., ; Gisder et al ., ).…”

“…However, the levels of N. ceranae (percentage of bees infected) vary over time with very high levels from the end of summer up to spring and the maximum during winter in Spain (Higes et al, 2008a). These profile can be influenced by some undetermined factors since the higher levels were reported in summer in Canada , in March in Serbia (Stevanovic et al, 2013) or in spring (reflecting the development over winter) in Germany (Gisder et al, 2017). Also, N. ceranae can multiply at higher temperatures, displaying a greater biotic potential than N. apis Higes et al, 2010b;Gisder et al, 2017).…”

“…These profile can be influenced by some undetermined factors since the higher levels were reported in summer in Canada , in March in Serbia (Stevanovic et al, 2013) or in spring (reflecting the development over winter) in Germany (Gisder et al, 2017). Also, N. ceranae can multiply at higher temperatures, displaying a greater biotic potential than N. apis Higes et al, 2010b;Gisder et al, 2017). Indeed, their spores are tolerant to temperatures as high as 608C and they can survive desiccation (Fenoy et al, 2009;Martín-Hern andez et al, 2009).…”

. Study of Nosema spp. in the Tomsk region, Siberia: co-infection is widespread in honeybee colonies

“…The virulence of the parasite, as well as the role and effect of N. ceranae infection in bee colonies has been controversially discussed. Some authors have defined a moderate virulence of parasite N. ceranae similar as that of N. apis, for example in French and German bees (Forsgren & Fries, 2010;Fries, 2010;Gisder et al, 2010Gisder et al, , 2017. In other reports, N. ceranae was characterized as a parasite with high virulence and may have caused large bee colony losses in the countries of the Mediterranean, e.g.…”

Microscopic and Molecular Detection of Nosema ceranae in Honeybee Apis mellifera L. from Romania Status on pathogen worldwide distribution

“…For instance, in the western parts, such as the region of Romanian Banat, where the three counties analyzed in this study are located, the climate is milder and has Mediterranean influences. Among other factors, the climatic conditions of the studied area may justify some of the similarities of prevalence, predominance and clinical impact of N. ceranae in colonies of A. mellifera bees that are characteristic of nosemosis reported in Mediterranean countries Gisder et al, 2017).…”