Effect of Temperature on the Biotic Potential of Honeybee Microsporidia

Martín-Hernández, Raquel; Meana, Aránzazu; García-Palencia, Pilar; Marı́n, P.; Botías, Cristina; Garrido-Bailón, Encarna; Barrios, Laura; Higes, Mariano

doi:10.1128/aem.02908-08

Cited by 175 publications

(145 citation statements)

References 14 publications

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“…Martín-Hernández et al (12) and Higes et al (7) described the higher prevalence of N. ceranaeinfected honeybees in all four seasons, compared with N. apis infection, which is more prevalent in milder seasons such as the spring and autumn. Moreover, Martín-Hernández et al (13) confirmed the different epidemiological patterns between the two species. They found a better adaptation of N. ceranae than N. apis to temperature.…”

supporting

confidence: 51%

High-Level Resistance of Nosema ceranae , a Parasite of the Honeybee, to Temperature and Desiccation

Fenoy

Rueda

Higes³

et al. 2009

Appl Environ Microbiol

101

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Resistance of Nosema ceranae to different exposure conditions has been evaluated by using Sytox green and DAPI (4,6-diamidino-2-phenylindole) to test spore viability. High thermotolerance at 60 and 35°C and resistance to desiccation were observed. However, a significant decrease in viability after freezing and a rapid degeneration of spores maintained at 4°C were also detected.Two Nosema species have been related to pathology in the honeybee: Nosema apis (18) a parasite of Apis mellifera, the western honeybee, and Nosema ceranae (4), a parasite of Apis cerana, the eastern honeybee. Currently, however, N. ceranae is considered an emergent and important parasite of Apis mellifera (4).Over the last few years, an increase in infections by this microsporidian has been detected in several European countries, together with an increase in honeybee colony deaths and a consequent decrease in the production of honey (9). However, it is not clear if N. ceranae infection may be the only factor related to this disorder, since this pathogen has also been found in healthy colonies (14). In Spain, Higes et al. (7,9) have demonstrated the presence of this parasite in honeybee samples from colonies with clear signs of population depletion, relating the colony collapse disorder to N. ceranae. The presence of this microsporidian is not exclusive to Europe, since it has also been described in bee samples collected about a decade ago in the United States (3).The pathology produced by N. ceranae in A. mellifera bees may be higher than that produced by N. apis, showing a rapid autoinfective capacity of the spores to spread the infection among epithelial cells, producing high mortality (6). On the other hand, reduced longevity of caged N. ceranae-infected worker bees compared to bees infected by N. apis has also been found (15).To date, continuous cultures of N. ceranae are not available and there is no effective treatment. For this reason, it is important to study the effects of different exposure conditions, such as time, temperature, and desiccation, on the viability of spores kept in the laboratory for use in the search for new treatments and for development of culture protocols. In addition, as different levels of thermotolerance in the environment and different epidemiological patterns have been described for these microsporidia, available data on resistance of N. apis spores cannot be extrapolated to N. ceranae.Spores. Spores from N. apis and N. ceranae were provided by the experimental apiary of the Regional Apicultural Center in Marchamalo, Spain. Recently collected spores were purified as described previously (8). The spore concentration was determined by counting with a hematocytometer chamber. Two stocks of N. ceranae spores were used (S1 and S2). All studies were carried out at a concentration of 5 ϫ 10 5 spores/ml. The Nosema species was determined by multiplex PCR, which amplifies the 16S rRNA locus (12).Spore treatments. The effects of time, temperature, and desiccation on viability were measured at different points. All ...

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supporting

confidence: 51%

High-Level Resistance of Nosema ceranae , a Parasite of the Honeybee, to Temperature and Desiccation

Fenoy

Rueda

Higes³

et al. 2009

Appl Environ Microbiol

101

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“…Nevertheless, the facts remain that (i) in Spain and Italy N. ceranae nearly replaced N. apis over the past decade (33) and (ii) N. ceranae infections cause severe honeybee colony losses, at least in Spain (28,30,37). Possible reasons for this assertiveness and virulence of N. ceranae are the exceptional biotic potential of N. ceranae at higher temperatures and the spores' tolerance to temperatures as high as 60°C, combined with resistance to desiccation (18,36). On the other hand, N. ceranae spores have been reported to be sensitive to freezing temperatures (18,20).…”

Section: Discussionmentioning

confidence: 99%

“…In the field, N. ceranae causes an unusual form of nosemosis, which led, and still leads, to severe colony losses in Spain (28,37). One explanation for the higher virulence of N. ceranae in the field could be the better adaptation of N. ceranae than of N. apis to elevated temperatures (18,36), indicating that N. ceranae might be a pathogen whose spread and assertiveness could be influenced by climate change.…”

mentioning

confidence: 99%

Five-Year Cohort Study of Nosema spp. in Germany: Does Climate Shape Virulence and Assertiveness of Nosema ceranae ?

Gisder

Hedtke

Möckel

et al. 2010

Appl Environ Microbiol

207

265

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Nosema ceranae and Nosema apis are two fungal pathogens belonging to the phylum Microsporidia and infecting the European honeybee, Apis mellifera. Recent studies have suggested that N. ceranae is more virulent than N. apis both at the individual insect level and at the colony level. Severe colony losses could be attributed to N. ceranae infections, and an unusual form of nosemosis is caused by this pathogen. In the present study, data from a 5-year cohort study of the prevalence of Nosema spp. in Germany, involving about 220 honeybee colonies and a total of 1,997 samples collected from these colonies each spring and autumn and analyzed via species-specific PCR-restriction fragment length polymorphism (RFLP), are described. Statistical analysis of the data revealed no relation between colony mortality and detectable levels of infection with N. ceranae or N. apis. In addition, N. apis is still more prevalent than N. ceranae in the cohort of the German bee population that was analyzed. A possible explanation for these findings could be the marked decrease in spore germination that was observed after even a short exposure to low temperatures (؉4°C) for N. ceranae only. Reduced or inhibited N. ceranae spore germination at low temperatures should hamper the infectivity and spread of this pathogen in climatic regions characterized by a rather cold winter season.

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“…The higher proportion of immature stages of N. ceranae (70%) than of N. apis (50%) in a comparative study of infected honey bees (Martin-Hernandez et al, 2009) indicated that there are clear differences in the total number of parasites inside the gut. As such, the real number of affected cells in bees cannot be accurately evaluated through the total spore count.…”

Section: 2mentioning

confidence: 99%

Interaction between pesticides and other factors in effects on bees

Thompson

2012

EFS3

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Bees are important pollinators of both managed crops and wild flora. An overview of the interactions between pesticides and other factors in effects on bees considered: 1) The importance of the different exposure routes in relation to the overall exposure of bees to pesticides; 2) Multiple exposure to pesticides (including substances used in bee medication) and potential additive and cumulative effects; and 3) Interactions between diseases and susceptibility of bees to pesticides. Nectar foraging bees are likely to experienced highest exposure to both sprayed and systemic seed and soil treatments compounds followed by nurse and brood-attending bees. In both cases the major contribution to exposure was contaminated nectar with direct overspray playing a significant role in exposure. However, there are a variety of other routes (and other bee species) where there is currently insufficient data to fully total exposure: There are a large number of studies that have investigated the interactions between pesticides in bees. By far the majority have related to the interactions involving EBI fungicides and can be related to their inhibition of P450. The scale of the synergy is shown to be dose and season-dependent in acute exposures but there are few data relating to the effect of time between exposures, the effect of route of exposure or on chronic exposure effects at realistic exposure levels. There are a wide range of factors which affect the immunocompetence of bees including diet quality, pest and diseases. Although there are a limited number of laboratory based studies which suggest effects of a pesticide on disease susceptibility there is no clear evidence from field-based studies that exposure of colonies to pesticides results in increased susceptibility to disease or that there is a link between colony loss due to disease and pesticide residues in monitoring studies. KEY WORDSHoneybees, bumble bees, pesticides, disease, mixtures, synergism DISCLAIMERThe present document has been produced and adopted by the bodies identified above as author. This task has been carried out exclusively by the author(s) in the context of a contract between the European Food Safety Authority and the author, awarded following a tender procedure. The present document is published complying with the transparency principle to which the Authority is subject. It may not be considered as an output adopted by the Authority. The European food Safety Authority reserves its rights, view and position as regards the issues addressed and the conclusions reached in the present document, without prejudice to the rights of the authors. The present document has been produced and adopted by the bodies identified above as author. This task has been carried out exclusively by the author in the context of a contract between the European Food Safety Authority and the author awarded following a tender procedure. The present document is published complying with the transparency principle to which the Authority is subject. It may not be considered as...

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Effect of Temperature on the Biotic Potential of Honeybee Microsporidia

Cited by 175 publications

References 14 publications

High-Level Resistance of Nosema ceranae , a Parasite of the Honeybee, to Temperature and Desiccation

High-Level Resistance of Nosema ceranae , a Parasite of the Honeybee, to Temperature and Desiccation

Five-Year Cohort Study of Nosema spp. in Germany: Does Climate Shape Virulence and Assertiveness of Nosema ceranae ?

Interaction between pesticides and other factors in effects on bees

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