Apis Mellifera) Mike Goblirsch

Nosema ceranae disease of the honey bee (Apis mellifera) Mike Goblirsch To cite this version: Mike Goblirsch. Nosema ceranae disease of the honey bee (Apis mellifera). Apidologie, 2018, 49 (1), pp.131-150. 10.1007/s13592-017-0535-1. hal-02973408 HAL Id: hal-02973408 https://hal.archives-ouvertes.fr/hal-02973408 Submitted on 21 Oct 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2018) 49:131–150 Review article * INRA, DIB and Springer-Verlag France SAS, 2017 DOI: 10.1007/s13592-017-0535-1 Nosema ceranae disease of the honey bee (Apis mellifera ) Mike GOBLIRSCH Department of Entomology, University of Minnesota, 219 Hodson Hall, 1980 Folwell Ave, St. Paul, MN 55108, USA Received 26 October 2016 – Revised 13 March 2017 – Accepted 26 July 2017 Abstract – The presence of honey bees in our landscapes has long invoked images of vitality, diligence, and cooperation. Unfortunately, the current state of bee health paints a rather different picture. The survival of honey bees, as well as the livelihoods of those who benefit from their labor, is under threat from several detractors to bee health. Exposure to pesticides, poor forage, mite parasites, and pathogens has resulted in high annual death of colonies in the USA, Europe, and other parts of the world. Among the suspects thought to contribute to bee decline, the fungal pathogen, Nosema ceranae , is found at high prevalence in both healthy and declining colonies. Since N. ceranae is thought to be a recent parasite of Apis mellifera , much remains unknown about its pathology at the individual and colony levels, as well as how infection may interact and synergize with other stressors. A review of research conducted on N. ceranae infection is provided. Attention is given to observations on detection of infection, cytopathology, viability and infectivity of spores, and caste-specific effects to survival, development, physiology, and behavior. Research findings showing effects from interactions with pesticides and viruses are also provided. Comparisons are drawn between N. ceranae and what is known about a similar, long-recognized pathogen of A. mellifera , Nosema apis . When possible, suggestions for future research that could broaden understanding of N. ceranae and ultimately improve honey bee health are offered to link observations on individual bee pathology with pathology observed at the colony level. fungal pathogen / Microsporidia / nosemosis / social behavior 1. A NEW NOSEMA N. ceranae has caused reason for concern for managed populations of A. mellifera and potential- In the aftermath of colony collapse disorder, ly other novel bee hosts. Because A. mellifera is surveillance efforts have recorded the presence of considered to be a recent host, it raises questions as a Bnew Nosema ^ traditionally associated with the to the effects this pathogen has on host physiology, Asian honey bee, Apis cerana , in colonies of the behavior, and longevity at the individual, as well as European honey bee, Apis mellifera . The detection colony, level. The goal of this review is to highlight of this new Nosema sp., Nosema ceranae ,asa research findings that have contributed to our un- natural infection of A. mellifera was first reported derstanding of disease caused by N . ceranae .Ad- in Europe in 2006 (Higes et al. 2006). Since then, ditionally, this review is meant to further the dis- there have been regular reports on the incidence of cussion concerning the impact N . ceranae has N . ceranae in A. mellifera and other host species mainly on A. mellifera and how it compares to from many parts of the world, supporting a wide- nosemosis, the disease traditionally associated with spread distribution of this parasite (Klee et al. 2007; Nosema apis , a similar pathogen long recognized Chen et al. 2008). The widespread distribution of to cause infection in A. mellifera (Zander 1909;for an excellent review of nosemosis and N . apis ,the reader is referred to Fries 1993). N. ceranae likely originated with Apis cerana Corresponding author: M. Goblirsch, as its primary host (Fries et al. 1996;Botíasetal. [email protected] 2012). However, archived samples suggest that Manuscript editor: Yves Le Conte N. ceranae had an expanded geographic and host 132 Goblirsch M. range decades before first detection as natural (Cantwell 1970). Nosema spp. spores have a dis- infections of A. mellifera in Spain (Higes et al. tinct size and ovoid morphology that sets them 2006) and the USA (Cox-Foster et al. 2007; apart from other microbes in tissue homogenates Huang et al. 2007). Two studies examining pre- prepared from honey bees. Coupled with served specimens of honey bees by polymerase sampling of specific cohorts, the method chain reaction (PCR) analysis place N. ceranae in developed by Cantwell (1970) can provide infor- the USA as early as 1975 (Traver and Fell 2015). mationontheproportioninfectedagainstaspe- Samples collected in Finland between 1986 and cific parameter (e.g., proportion of infected for- 2006 showed that samples from as early as 1998 agers). Although visualizing Nosema spp. spores were positive for N. ceranae (Paxton et al. 2007). under a microscope is relatively straightforward, Likewise, archived material revealed that samples and some skilled technicians may be able to dis- from as early as 1993 from Italy (Ferroglio et al. cern between spores of N . apis and N . ceranae 2013), 1994 from Canada (Currie et al. 2010), and by eye, positive identification to species is com- 1995 from Mexico (Guerrero-Molina et al. 2016) plicated by the fact that both species cause single were positive for N. ceranae . Moreover, one sam- or mixed infections in A. cerana and A. mellifera ple of A. mellifera from Uruguay collected prior (Chen et al. 2009;ForsgrenandFries2010; to 1990 was positive for N . ceranae by PCR Milbrath et al. 2015). Evidence suggests that in- (Invernizzi et al. 2009). In addition, Africanized fections with N . ceranae are now more prevalent drones collected in Brazil in 1979 had presence of in some regions where N . apis had historically spores by microscopy and were positive for been the only species present (Klee et al. 2007; N. ceranae by PCR (Teixeira et al. 2013). Clark Martín-Hernández et al. 2012; Emsen et al. 2016); (1980) described a second microsporidian in bees therefore, failure to diagnose a mixed infection is from southeastern USA; however, it is unlikely to likely if the infection is skewed heavily toward have been N. ceranae due to the presence of a one species. Mixed infections that are skewed in single nucleus instead of the diplonucleus charac- favor of a single species point to the need for a teristic of spores in this species. reliable detection method specific to the level of Although the timing of N . ceranae ’sintroduc- species. Progress has been made using fluorescent tion as a pathogen of A. mellifera is uncertain, it dyes incorporated with microscopic techniques. may have coincided with the spread of the mite For example, the fluorescent brightener, parasite, Varroa destructor.Asthemovementof calcofluor white, has been shown to bind to chitin A. mellifera colonies into and out of regions in the cell wall of mature N . ceranae spores where A. cerana is endemic lead to the introduc- (Snow 2016). Since immature spores lack chitin, tion of the V. destructor as a parasite of this method is useful for localization studies of A. mellifera , the interactions of these bee species mature spores within cells, but it cannot differen- may also have permitted the simultaneous acqui- tiate between species (Snow 2016). Other detec- sition and spread of N . ceranae . One question tion markers, such as labeled antibodies that remains unanswered: if N . ceranae has been (Aronstein et al. 2013), are needed to discern present in colonies of A. mellifera for several species and life stages. Species-specific antibodies decades, why has it only recently been considered could be applied toward the development of field as a factor in the decline of A. mellifera and only assays permitting rapid diagnosis. in some regions? Alternatively, PCR amplification of genes encoding ribosomal RNA (rRNA) that are highly 2. DETECTION AND DIAGNOSIS conserved within a species but variable between species has the potential to increase specificity The first step in understanding the effects of N . and sensitivity of detection and quantification ceranae is the ability to detect and diagnose this (Chen et al. 2009;Carlettoetal.2013; but see pathogen. Diagnosis of Nosema spp. infection Ptaszyńska et al. 2014 on loop-mediated isother- can be determined by viewing and counting mal amplification). One study compared the spec- spores with a hemocytometer under magnification ificity and sensitivity of microscopy to real-time Nosema ceranae disease of the honey bee (Apis mellifera ) 133 PCR and showed that the former failed to identify et al. 1997), there is no evidence of transovarial N. ceranae spores in 50% of samples that tested transmission from an infected queen to her eggs positive by PCR (Traver and Fell 2011a). This (Roberts et al. 2015). The lack of vertical trans- finding may demonstrate a disparity between spe- mission may result from tissue tropism restricting cies in the production of spores, where N. ceranae the pathogen to infection within midgut epithelial may not be as prolific as N. apis (Martín- cells or from immune defenses in semen (Peng Hernández et al. 2009; Mulholland et al. 2012). et al.

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