Tarazona de la Mancha, Spain
Tarazona de la Mancha, Spain

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Higes M.,Centro Apicola Regional CAR | Meana A.,Complutense University of Madrid | Bartolome C.,University of Santiago de Compostela | Botias C.,Centro Apicola Regional CAR | Martin-Hernandez R.,Institute Recursos Humanos para la Ciencia y la Tecnologia INCRECYT
Environmental Microbiology Reports | Year: 2013

The worldwide beekeeping sector has been facing a grave threat, with losses up to 100-1000 times greater than those previously reported. Despite the scale of this honey bee mortality, the causes underlying this phenomenon remain unclear, yet they are thought to be multifactorial processes. Nosema ceranae, a microsporidium recently detected in the European bee all over the world, has been implicated in the global phenomenon of colony loss, although its role remains controversial. A review of the current knowledge about this pathogen is presented focussing on discussion related with divergent results, trying to analyse the differences specially based on different methodologies applied and divisive aspects on pathology while considering a biological or veterinarian point of view. For authors, the disease produced by N.ceranae infection cannot be considered a regional problem but rather a global one, as indicated by the wide prevalence of this parasite in multiple hosts. Not only does this type of nosemosis causes a clear pathology on honeybees at both the individual and colony levels, but it also has significant effects on the production of honeybee products. Journal compilation © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd.


Botias C.,Centro Apicola Regional CAR | Martin-Hernandez R.,Centro Apicola Regional CAR | Martin-Hernandez R.,Institute Recursos Humanos Para la Ciencia y la Tecnologia INCRECYT | Garrido-Bailon E.,Centro Apicola Regional CAR | And 5 more authors.
Research in Veterinary Science | Year: 2012

Microsporidiosis caused by infection with Nosema apis or Nosema ceranae has become one of the most widespread diseases of honey bees and can cause important economic losses for beekeepers. Honey can be contaminated by spores of both species and it has been reported as a suitable matrix to study the field prevalence of other honey bee sporulated pathogens. Historical honey sample collections from the CAR laboratory (Centro Apícola Regional) were analyzed by PCR to identify the earliest instance of emergence, and to determine whether the presence of Nosema spp. in honey was linked to the spread of these microsporidia in honey bee apiaries. A total of 240 frozen honey samples were analyzed by PCR and the results compared with rates of Nosema spp. infection in worker bee samples from different years and geographical areas. The presence of Nosema spp. in hive-stored honey from naturally infected honey bee colonies (from an experimental apiary) was also monitored, and although collected honey bees resulted in a more suitable sample to study the presence of microsporidian parasites in the colonies, a high probability of finding Nosema spp. in their hive-stored honey was observed. The first honey sample in which N. ceranae was detected dates back to the year 2000. In subsequent years, the number of samples containing N. ceranae tended to increase, as did the detection of Nosema spp. in adult worker bees. The presence of N. ceranae as early as 2000, long before generalized bee depopulation and colony losses in 2004 may be consistent with a long incubation period for nosemosis type C or related with other unknown factors. The current prevalence of nosemosis, primarily due to N. ceranae, has reached epidemic levels in Spain as confirmed by the analysis of worker honey bees and commercial honey. © 2011 Elsevier Ltd.


Botias C.,Centro Apicola Regional CAR | Martin-Hernandez R.,Centro Apicola Regional CAR | Martin-Hernandez R.,Institute Recursos Humanos para la Ciencia y Tecnologia | Meana A.,Complutense University of Madrid | Higes M.,Centro Apicola Regional CAR
Parasitology Research | Year: 2012

Nosemosis is one of the most widespread of the adult honey bee diseases and causes major economic losses to beekeepers. Two microsporidia have been described infecting honey bees worldwide, Nosema apis and Nosema ceranae, whose seasonality and pathology differ markedly. An increasing prevalence of microsporidian infections in honey bees has been observed worldwide during the last years. Because nosemosis has detrimental effects on both strength and productivity of the infected colonies, an accurate and reliable method to evaluate the presence of Nosema in honey bee colonies is needed. In this study a high degree of variability in the detection of microsporidia depending on the random subsample analyzed was found, suggesting that both sample size and the time of collection (month and day of sampling) notably affect the diagnosis. © Springer-Verlag 2011.


Van der Zee R.,Nederlands Centrum Bijenonderzoek NCB | Gomez-Moracho T.,Centro Apicola Regional CAR | Pisa L.,Nederlands Centrum Bijenonderzoek NCB | Sagastume S.,Centro Apicola Regional CAR | And 6 more authors.
Environmental Microbiology Reports | Year: 2014

Infection of honeybees by the microsporidian Nosema ceranae is considered to be one of the factors underlying the increased colony losses and decreased honey production seen in recent years. However, these effects appear to differ in function of the climatic zone, the distinct beekeeping practices and the honeybee species employed. Here, we compared the response of Apis mellifera iberiensis worker bees to experimental infection with field isolates of N.ceranae from an Oceanic climate zone in Northern Europe (Netherlands) and from a Mediterranean region of Southern Europe (Spain). We found a notable but non-significant trend (P=0.097) towards higher honeybee survival for bees infected with N.ceranae from the Netherlands, although no differences were found between the two isolates in terms of anatomopathological lesions in infected ventricular cells or the morphology of the mature and immature stages of the parasite. In addition, the population genetic survey of the N. ceranaePTP3 locus revealed high levels of genetic diversity within each isolate, evidence for meiotic recombination, and no signs of differentiation between the Dutch and Spanish populations. A cross-infection study is needed to further explore the differences in virulence observed between the two N.ceranae populations in field conditions. © 2013 Society for Applied Microbiology and John Wiley & Sons Ltd.


Jara L.,University of Murcia | Cepero A.,Centro Apicola Regional CAR | Garrido-Bailon E.,Centro Apicola Regional CAR | Martin-Hernandez R.,Centro Apicola Regional CAR | And 2 more authors.
Journal of Invertebrate Pathology | Year: 2012

The recent decline in honey bee colonies observed in both European countries and worldwide is of great interest and concern, although the underlying causes remain poorly understood. In recent years, growing evidence has implicated parasites and pathogens in this decline of both the vitality and number of honey bee colonies. The Iberian Peninsula provides an interesting environment in which to study the occurrence of pathogens and parasites in the host honey bee populations due to the presence of two evolutionary lineages in . A. m. iberiensis (Western European [M] or African [A]). . Here, we provide the first evidence linking the population structure of the Iberian honey bee with the prevalence of some of its most important parasites and pathogens: the . Varroa destructor mite and the microsporidia . Nosema apis and . Nosema ceranae. Using data collected in two surveys conducted in 2006 and 2010 in 41 Spanish provinces, the evolutionary lineage and the presence of the three parasitic organisms cited above were analyzed in a total of 228 colonies. In 2006 . N. apis was found in a significantly higher proportion of M lineage honey bees than in the A lineage. However, in 2010 this situation had changed significantly due to a higher prevalence of . N. ceranae. We observed no significant relationships in either year between the distributions of . V. destructor or . N. ceranae and the evolutionary lineage present in . A. m. iberiensis colonies, but the effects of these organisms on the genetic diversity of the honey bee populations need further research. © 2012 Elsevier Inc.


Bernal J.,University of Valladolid | Martin-Hernandez R.,Centro Apicola Regional CAR | Diego J.C.,University of Valladolid | Nozal M.J.,University of Valladolid | And 3 more authors.
Pest Management Science | Year: 2011

Background: There is great concern about the high losses and strong depopulation of honey bee colonies in some areas of Spain. Some beekeepers have suggested that sunflower seeds treated with the insecticide fipronil could be an important factor in causing those losses. Therefore, an in-depth field study has been carried out in two regions of Spain where sunflower production is intense (Cuenca and Andalucía) and where, for some crops and varieties, fipronil has been used as seed insecticide. RESULTS: Samples of adult bees and pollen were analysed for bee pathogens and pesticide residues respectively. Neither fipronil residues nor its metabolites were detected in any of the samples analysed, indicating that short-term or chronic exposure of bees to fipronil and/or its metabolites can be ruled out in the apiaries surveyed. Varroa destructor and Nosema ceranae were found to be very prevalent. CONCLUSION: The combination of the two pathogens could augment the risk of colony death in infected colonies, without fipronil residues exerting a significant effect in the given field conditions. Indeed, in this study the losses observed in apiaries located close to sunflower crops were similar to those in apiaries situated in forested areas with wild vegetation. © 2011 Society of Chemical Industry.


Sanchez-Hernandez L.,University of Valladolid | Hernandez-Dominguez D.,University of Valladolid | Martin M.T.,University of Valladolid | Nozal M.J.,University of Valladolid | And 2 more authors.
Journal of Chromatography A | Year: 2016

A study was carried out to evaluate the possible presence of thiamethoxam, clothianidin and imidacloprid, as well as the metabolic breakdown products of these three neonicotinoids in pollen and honey obtained from brood chamber combs of honeybee colonies located next to sunflower and maize crops from coated seeds. Samples were analyzed by liquid chromatography coupled to quadrupole-time-of-flight mass spectrometry detector, in combination with accurate mass tools such as diagnostic ions by exact mass, chlorine mass filters, and MS/MS experiments. The presence of thiamethoxam and clothianidin was confirmed in some of the pollen samples analyzed. Moreover, different metabolites of neonicotinoids were tentatively detected in the pollen and honey samples collected. The results suggested that four metabolites were found in the honey samples, while for pollen samples eleven metabolites were identified; among these, five were considered for the first time as metabolic breakdown products in sunflower and maize plants. © 2015 Elsevier B.V..


PubMed | Centro Apicola Regional CAR
Type: Journal Article | Journal: Parasitology research | Year: 2015

Acarapisosis is a disease of the adult honey bee Apis mellifera L., caused by the tracheal mite Acarapis woodi (Rennie), that affects the prothoracic tracheas of worker honey bees. Although it is not usually considered a real problem for honey bee colonies in southern Europe (mainly Spain and Greece), where the majority of professional beekeepers are located in Europe, recent works have reported the constant presence of this mite in this area, making it a potential cofactor for colony losses. In this study, we developed a specific PCR diagnostic tool that improves the techniques used so far and allowed us to confirm the presence of this parasite in Spain, urging the need to monitor its prevalence and implications in the health of the colonies. Indeed, in a total of 635 apiaries analysed, the prevalence of A. woodi in 2010 was 8.3 and 4 % in 2011. The mite is present in bee colonies over time and should not be underestimated as a possible cofactor in the collapse of bee colonies. Additionally, some positive samples were cloned so a genetic analysis on the diversity within A. woodi isolates was also approached. This allowed us to identify different genetic variants within an isolate, even when they were present at low frequencies. And this genetic analysis revealed the existence of a different clade of Acarapis sequences that could represent a new species or subspecies, although more research is required to verify the identity of this novel lineage at genetic and morphological level.


PubMed | Centro Apicola Regional CAR
Type: Journal Article | Journal: Parasitology research | Year: 2014

Nosema apis and Nosema ceranae are microsporidia which present resistant spores for the transmission stage (environmental spores) that play an important role for epidemiology and for laboratory studies of honey bee microsporidiosis. In this study, the long-term longevity of N. apis and N. ceranae spores exposed to 4 C, room temperature (mean 25 C) and 35 C for 6-month long and to -20 C for 10-month long has been assessed by flow cytometry. Storage temperature and the length of storage duration had adverse effects on spore viability of both Nosema spores, with significant differences between the two species. The greatest increase in spore mortality was observed in N. apis spores stored at 33 C (64, 89%) and in N. ceranae spores at -20 C (53.55%) and at 33 C (51.97%). For N. ceranae spores at -20 C, the loss in viability was very quick, getting an increase over 20% just after 6 days of exposure. Results on viability were confirmed by the infectivity tests where the lowest infectivity for N. ceranae was observed with spores stored for 10 months at -20 C (79%; P<0.05) and for N. apis with spores stored at 33 C (71%; P<0.05). For both Nosema species, the best storage temperatures were 25 and 4 C, especially for N. apis that was almost unaffected at those temperatures.


PubMed | University of Valladolid and Centro Apicola Regional CAR
Type: | Journal: Journal of chromatography. A | Year: 2016

A study was carried out to evaluate the possible presence of thiamethoxam, clothianidin and imidacloprid, as well as the metabolic breakdown products of these three neonicotinoids in pollen and honey obtained from brood chamber combs of honeybee colonies located next to sunflower and maize crops from coated seeds. Samples were analyzed by liquid chromatography coupled to quadrupole-time-of-flight mass spectrometry detector, in combination with accurate mass tools such as diagnostic ions by exact mass, chlorine mass filters, and MS/MS experiments. The presence of thiamethoxam and clothianidin was confirmed in some of the pollen samples analyzed. Moreover, different metabolites of neonicotinoids were tentatively detected in the pollen and honey samples collected. The results suggested that four metabolites were found in the honey samples, while for pollen samples eleven metabolites were identified; among these, five were considered for the first time as metabolic breakdown products in sunflower and maize plants.

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