Asymptomatic presence of Nosema spp. in Spanish commercial apiaries

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Abstract

Nosemosis is caused by intracellular parasites (Nosema apis and Nosema ceranae) that infect the midgut epithelial cells in adult honey bees. Recent studies relate N. ceranae to Colony Collapse Disorder and there is some suggestion that Nosema spp., especially N. ceranae, induces high mortality in honey bees, a fact that is considered as a serious threat for colony survival.

604 samples of adult honey bees for Nosema spp. analysis were collected from beekeeping colonies across Spain and were analysed using PCR with capillary electrophoresis. We also monitored 77 Andalusian apiaries for 2 years; the sampled hives were standard healthy colonies, without any special disease symptoms.

We found 100% presence of Nosema spp. in some locations, indicating that this parasite was widespread throughout the country. The two year monitoring indicated that 87% of the hives with Nosema spp. remained viable, with normal honey production and biological development during this period of time. The results of these trials indicated that both N. ceranae and N. apis could be present in these beehives without causing disease symptom and that there is no evidence for the replacement of N. apis by N. ceranae, supporting the hypothesis that nosemosis is not the main reason of the collapse and death of beehives.

Highlights

► Honeybee samples (N = 604) were analysed using PCR with capillary electrophoresis. ► N. apis and N. ceranae are distributed throughout the Spanish territory. ► Both parasites are present in the hives without developing clinical signs of disease. ► There is no evidence for replacement of N. apis by N. ceranae.

Introduction

Nosemosis is a parasitic disease that attacks all adult forms of honey bees: workers, queens and drones (Bailey, 1955, Alaux et al., 2011, Traver and Fell, 2011). The disease is caused by the microsporidia Nosema apis and/or Nosema ceranae (Bailey, 1962, Fries et al., 1996). As a mechanism of infection, microsporidia are mainly characterised by their ability to disperse among their host as spores. Inside the host the spores germinate and the sporoplasm enter the host cell via the polar filament which is injected into the host cell (Kudo, 1954, Fries et al., 1996, Fries et al., 2006, Lee et al., 2008). There are other microsporidia species that can parasites insects (Avery and Anthony, 1983, Bomar et al., 1993), reptiles (Jacobson et al. 1998), birds (Dorrestein and van der Hage, 1999), fishes (Lom and Nilsen, 2003) and mammals (Percy and Barthold, 1993, Wasson and Peper, 2000), including humans (Shadduck et al., 1990, Cali, 1991, Didier, 2005).

Both N. apis and N. ceranae develop inside the epithelial cells of the bee’s ventriculus, interfering with the absorption of proteins (Liu, 1984, Puerta et al., 2001, Chen et al., 2009). Although this parasite is essentially distributed worldwide (Matheson, 1996, Chen et al., 2007, Higes et al., 2007, Klee et al., 2007, Liu et al., 2008, Williams et al., 2008), the virulence of both species is controversial (Paxton, 2010), and it was also suggested that N. ceranae could cause colony collapse (Cox-Foster et al., 2007, Higes et al., 2008, Higes et al., 2009b).

Over the last decade, Colony Collapse Disorder (CCD) is having a massive impact in Spain, with approximately 30% of the Spanish hives being lost in recent years (unofficial data from beekeepers’ associations). Spain has the largest number of beehives (2,300,000 hives) in the European Union, and Andalusia is the Spanish region that has the largest number of hives (442,466 hives). Due to this large amount of beehives, CCD has become more important in this country in which the income of 80% of professional beekeepers (having more than 150 hives) depends heavily on beekeeping (General Register of Livestock Farms. Ministry of the Environment, Rural and Marine Affairs, 2008).

In response to the increasing concern over CCD, we monitored samples of honey bee hives in the main Spanish areas where beekeeping is practised professionally to clarify the role of nosemosis in CCD and to determinate whether N. ceranae causes this disorder.

Section snippets

Sampling

Samples were collected and monitored by the beekeeping technicians of the different livestock organisations and health advisory associations. Each sample consisted of 100 adult bees collected from the outer honey frame of the same hive. The samples were stored in a freezer at −20 °C until analysis.

The hives chosen did not show any clinical symptoms and did not receive any antifungal treatment, but they were treated with authorised Varroa destructor products at least once a year. The hives were

Results and discussion

The survey data from our 2 years of beehive monitoring indicate that all of the samples tested were positive for Nosema spp. (Table 1), that is, the presence of N. apis, N. ceranae or both. Of the monitored hives, 87% remained alive, with normal production during the study. According to the beekeeper’s questionnaire, the main reason for the death of the monitored samples was a V. destructor infestation.

Both N. apis and N. ceranae were present in hives in spring and autumn, sometimes as a

Acknowledgments

The authors would like to thank the Functional Genomic Unit (University of Cordova), Spanish Farming Association (COAG) and M.C. Fernández Perejón for their editing, comments and suggestions. This project was funded by the European Union and Spanish Ministry for the Rural and Marine Environment (MARM) Project API 06-008 “Research into Colony Collapse Disorder (CCD) in Spain. Evaluation of epidemiological, environmental, and feeding factors”.

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