Is Colony Collapse Disorder (CCD) caused by new or re-emerging pathogens? This is one hypothesis put forward by US researchers in 2007 and two candidates, the Israeli Acute Paralysis Virus (IAPV) and the microsporidian parasite Nosema ceranae, have received the most mention in the press.
I reviewed the available scientific literature to evaluate the weight of scientific evidence for the role of each pathogen in CCD and found that in terms of both the number of scientific papers and their substantial content the weight of evidence supports Nosema ceranae over IAPV as a cause of CCD, at least in Spain. Additionally, recent research does not support IAPV as a cause of CCD, in either the United States or Europe.
However, despite this evidence, there is a knowledge gap in the literature about the role of Nosema ceranae in CCD in the United States, which may arise from early US research focus on IAPV, the later start on research on IAPV relative to Nosema ceranae, or different causes of CCD in Europe and the United States. More experimental research is required to confirm that Nosema ceranae does, or does not, play a role in CCD in North America.
Until then, the current weight of evidence for a cause-effect link between Nosema ceranae and CCD supports the adoption of precautionary bee-keeping practices that account for it.
Background
Soon after colony collapse disorder (CCD) emerged in 2006, US researchers focused on a suite of hypotheses, one of which was that CCD is caused by new or re-emerging pathogens (see here).
In 2007, a paper in journal Science reported that a relatively new virus, the Israeli Acute Paralysis Virus (IAPV), was associated with observed occurrences of CCD, a finding that not only generated a tremendous amount of press coverage (see here), but some international intrigue as well (see here). As recently as this year, US researchers were still discussing of the role of IAPV in CCD in a general science magazine.
Nosema ceranae, while recognized as an emerging threat to honey bees prior to CCD, was quickly dismissed as a candidate pathogen for CCD by the primary US researchers. Little was written in the general press about Nosema ceranae until early in 2009 when it received its own press boost after a paper was published by Spanish researchers which appeared to convincingly connect it to CCD (see here).
The challenge to the layperson following developments in CCD research is keeping such press reports on scientific research results in perspective. Reporters often rely on press releases prepared by research institutions and may let the researchers themselves place their results in context.
While this is an important part of reporting on science, reporters rarely dig deep enough or follow a particular issue long enough to be able to establish the relative importance of a particular paper for the reader, beyond the immediate research being reported. This is especially the case for a topic as significant, complex and long-lasting as CCD; it is difficult for the interested layperson keep abreast of the research initiatives and findings, many of which are not reported upon in the general press.
The purpose of this analysis, then, is to determine the relative weight of evidence for the role of IAPV and Nosema ceranae as causes of CCD by finding and evaluating the peer-reviewed scientific evidence available for each.
Methods
I used Google Scholar to search the peer-reviewed scientific literature for research papers on both IAPV and Nosema ceranae (search is current up to the date of this posting). For each pathogen, I considered both the number of scientific papers published about it, from its first appearance in the literature until the present, and their substantive nature in relation to CCD. That is, for each pathogen, I considered how directly the observational or experimental evidence reported in the papers supported a cause-effect link between it and CCD.
To make the direct case for a cause-effect link between a particular pathogen and CCD, the research had to show that infection by the pathogen in question caused symptoms of CCD:
1) most adult bees have left and failed to return to the hive leaving the queen behind (uncharacteristic of bee behaviour);
2) colony losses are rapid and occur in large numbers; no dead adult bees are found within or near the hive;
3) delayed honey robbing behaviour from nearby colonies and honey predators (highly unusual); and
4) the few adults found within abandoned colonies are often highly infected with multiple pathogens.
Results
Evidence for a Cause-Effect Link between the Israeli Acute Paralysis Virus (IAPV) and CCD
The first published description of IAPV in the scientific literature is in 2007. Maori et al. (2007) report that following unusually high honey bee colony losses in Israel, they isolated IAPV, a virus closely related to two previously known bee viruses, the kashmir bee virus and acute bee paralysis virus.
[Cox-Foster and vanEngelsdorp (2009) write that IAPV was first described in 2004 by Ilan Sela of the Hebrew University of Jerusalem; however, I could not find a published paper to support this. It may be referenced in another paper as a personal communication, or just common knowledge in the bee virus research community. Sela is a co-author of Maori et al. 2007].
That same year, Cox-Foster et al. (2007) published a paper in the journal Science reporting an association between the presence of IAPV and dead colonies exhibiting the symptoms of CCD. This research received much press, but though it showed an association between IAPV and CCD, it did not establish a causal link between them (Anderson and East 2008). For example, CCD could have made the bees susceptible to IAPV infection (Cox-Foster and vanEngelsdorp 2009).
A third IAPV paper published in 2007 reported that the virus had been present in honey bees in the United States for a number of years prior to the onset of CCD (Chen and Evans 2007). So, if IAPV was a cause of CCD, something must have changed to make it more virulent. This ‘something’ could be a new strain arising through genetic mutation, or the arrival of a more virulent strain from outside the US.
Papers relevant to IAPV and CCD that have been published since Cox-Foster et al. (2007) include:
- Palacios et al. (2008): found distinct clusters of the IAPV virus in the United States.
- Blanchard et al. (2008): reported the first detection of IAPV in France, but their results were inconclusive about its relationship to observed colony losses.
- Maori et al. (2009): reported that IAPV can be ‘silenced’ by dsRNA ingestion, suggesting a potential future treatment for the virus.
None of these papers strengthen the support for IAPV as a cause CCD, and recent research weakens the link even further. vanEngelsdorp et al. (2009) report that a replication of the work reported by Cox-Foster et al (2007) did not show IAPV was associated with CCD – that is, they were unable to replicate those earlier results, though they found that the prevalence of other viruses was generally comparable to the prior results.
In summary, the published scientific evidence on IAPV to date does not support the hypothesis that IAPV is a cause of CCD, however, the primary US researchers of CCD remain convinced that a virus of some kind lies at the bottom of the mystery: “The growing consensus among researchers is that multiple factors such as poor nutrition and exposure to pesticides can interact to weaken colonies and make them susceptible to a virus mediated collapse.” (Cox-Foster and vanEngelsdorp 2009)
Evidence for a Cause-Effect Link between Nosema ceranae and CCD
Meanwhile, in Europe there is little or no support for IAPV as a cause of CCD, but lots for Nosema ceranae. There CCD is also called Honey Bee Colony Depopulation Syndrome (HBDS) and research into the role of Nosema ceranae in honey bee colony losses has been going on since before the onset of CCD in the United States, with the pathogen gradually becoming the primary suspect.
Nosema ceranae is a microsporidian (fungal) parasite of the Asian honeybee Apis ceranae that is closely related to Nosema apis, a long known pathogen of the European honeybee Apis mellifera. Nosema ceranae is first mentioned in the scientific literature as a parasite of Apis ceranae in 1996 (see Fries et al. 1996), but not long after that it emerges as a pathogen of Apis mellifera being reported first in Taiwan by Huang et al. (2007) (research submitted for publication in 2005) and then in Spain (Higes et al. 2006).
Since then, research on N. ceranae has steadily accumulated with the publication of at least twenty more papers. For this analysis, I focused on a subset of those papers that describe N. ceranae’s spatial distribution, its pattern of temporal emergence, and the experimental evidence of its role in honey bee colony collapse; however, the citations for the other papers are also included at the end of this article for those interested.
Spatial Distribution of Nosema ceranae:
Nosema ceranae is now widespread throughout the world as a pathogen of Apis mellifera. Klee et al. (2007) summarised its global dispersal as of 2006, when it was present in at least 15 countries across the Americas and Caribbean (Brazil, Martinique, Washington DC), Asia (Vietnam, Taiwan), Europe and Near East (Denmark, Finland, France, Germany, Greece, Italy, Serbia, Spain, Sweden, Switzerland). They attributed its rapid long distance dispersal to the transport of infected honey bees by commercial or hobbyist bee keepers.
Since then, Nosema ceranae has been found in Canada (the provinces of Nova Scotia, New Brunswick and Prince Edward Island) and extended its range in the United States (Minnesota) (Williams et al. 2008). It has also been found in Uruguay (Inverrnizzi et al. 2009), Australia (Giersch et al. 2009) and Hungary (Tapaszti et al. 2009).
Temporal Emergence of Nosema ceranae:
Not only does the scientific literature show that Nosema ceranae has become globally distributed, it also shows that it has been infecting Apis mellifera probably since it was first reported in the literature as a parasite of Apis ceranae. Klee et al. (2007) concluded that N. ceranae had jumped to Apis mellifera ‘within the last decade’ (their paper was submitted for publication in October 2006), a finding consistent with the research of Paxton et al. (2007), who reported that Nosema ceranae had been present in Apis mellifera in Europe since at least 1998.
Where it has become established, N. ceranae has gradually displaced N. apis as the most prevalent nosema infection. Martin-Hernandez et al. (2007) found evidence of Nosema ceranae’s growing severity over time in Europe, with the gradual replacement of N. apis by N. ceranae as the most prevalent nosema infection in in bees samples from Spain, Switzerland, France and Germany. Similar results were found in North America by Chen et al. (2008), who reported that N. ceranae had not only been present there for longer than previously thought (since at least 1995), but that by 2007 it was the primary nosema infection of the honey bees they tested.
Experimental Link between Nosema ceranae and CCD
The rapid spread of Nosema ceranae around the globe and its temporal pattern of emergence and intensification coincided with increasing numbers of colony collapses (e.g., Martin-Hernandez et al 2007). Nevertheless, ‘correlation is not causation’, a saying exemplified by the IAPV case above - and further scientific work would be required to establish the cause-effect link between N. ceranae and CCD.
As Klee et al. (2007) remarked, “Analyses of colonies with and without apparent nosema disease combined with experimental infection trials are needed to determine if there is a causal link between Nosema ceranae and colony collapse.” The scientific research into Nosema ceranae gradually provided strong experimental evidence of a cause-link, at least in Europe. Below is a sketch of the key research findings that establish this connection.
First, Fries et al. (2006) confirmed that Nosema ceranae has become established as a naturally recurring and persistent new infection of European honey bees and could no longer be thought of as a sporadic, exotic infection caused only by the importation of bees or bee products.
Second, experimental infection trials demonstrated that not only was Nosema ceranae able to infect and kill Apis mellifera, it was far more pathogenic than its relative Nosema apis (Higes et al. 2007). In fact, it was soon established that the relative risk of bee depopulation observed in colonies with both Nosema species or N. ceranae only was almost 6 times greater than in colonies without such infections (Martin-Hernandez et al. 2007).
Third, Higes et el. (2007) also described a plausible ‘mechanism of collapse’. They found that bees infected with Nosema ceranae died suddenly after a period of infection, which supported a hypothesis that infected bees die away from the hive while foraging, leading to a steady colony depopulation that would only be detected when a hive (i.e. the queen) could not keep up with the disappearance of foragers in the field (i.e. by laying more eggs and producing worker bees). To an observer, say a commercial beekeeper, this would appear to be a sudden loss and thus one of the key symptoms of CCD – colonies found without adult worker bees and no dead bees near the hive.
Fourth, Higes et al. (2008) showed that natural infection of bee colonies by Nosema ceranae could cause colony collapse. Consistent with the hypothesized ‘mechanism of collapse’ of Higes et al. (2007), they found that signs of colony weakness were not observed until the queen could no longer replace the loss of infected worker bees and that the long period asymptomatic N. ceranae infection helped explain the absence of obvious symptoms until colony collapse occurred.
Importantly, Higes et al. (2008) also showed that Nosema ceranae could be isolated from infected bees, used to infect non-infected colonies, that these colonies subsequently collapsed, and that Nosema ceranae could then be isolated from in bees from those colonies. Theses steps follow Koch’s postulates, a key part of the process for establishing a cause-effect link between a candidate pathogen and a disease. The lack of these steps was a key criticism of the conclusions drawn by Cox-Foster et al. (2007) about the link between IAPV and CCD (e.g., Anderson and East 2008).
Fifth and finally, Higes et al. (2009) reported how Nosema ceranae caused colony collapse in two commercial bee operations, the first such case observed under field conditions. In both cases, analyses supported the conclusion that the observed collapse was due to infection by Nosema ceranae. The researchers searched for and did not find other significant pathogens (e.g., IAPV) or pesticides (e.g., neonicotinoids).
The Weight of Scientific Evidence Favours Nosema ceranae over IAPV as a Cause of CCD
The weight of scientific evidence favours Nosema ceranae over IAPV as a cause of CCD. Not only have more scientific papers been published on Nosema ceranae than IAPV (23 vs. 7), but these papers include a series of substantive papers that experimentally establish a causal link between Nosema ceranae and colony collapse in Europe.
This substantive research shows that Nosema ceranae jumped from Apis ceranae, its natural host, to Apis mellifera sometime in the early to mid-1990’s, that it quickly increased its spatial distribution around the world during the same period of time that Europe and other areas in the world saw increasing instances of colony collapse, that it is now a natural pathogen of Apis mellifera, that it is highly pathogenic to Apis mellifera, that experimental infection of Apis mellifera by Nosema ceranae produces colony collapse exhibiting a key symptom of CCD, that this symptom can be accounted for through a plausible biological ‘mechanism of collapse’, and that natural infections cause colony collapse in commercial beekeeping operations under field conditions in the absence of other suspected causes, such IAPV or pesticides.
No comparable body of research exists for IAPV, and in fact scientific support for IAPV as a cause of CCD in the US has recently waned after vanEngelsdorp et al. 2009 failed to replicate the findings of Cox-Foster et al (2007) – that is, IAPV was not correlated with CCD in this new study.
Thus, based on my two performance measures of number of publications and their substantive content, I conclude that there is a greater weight of scientific evidence for Nosema ceranae as a cause of honey bee colony collapse than for IAPV.
There is No Published Evidence that Nosema ceranae causes CCD in the United States
Yet, a problem remains: while scientific support for IAPV as a cause of CCD has declined since 2007, there is currently no published scientific evidence that Nosema ceranae plays a role in CCD in the United States. This could be for several reasons.
First, the early US research into CCD quickly dismissed Nosema ceranae as a culprit after it was not detected at levels considered high enough to cause colony collapse (see Russell 2007 and also Cox-Foster et al. 2007). This could explain why, in their recent Scientific American article about CCD, Cox-Foster and vanEngelsdorp (2009) do not specifically mention of N. ceranae at all, just that two nosema species were found and dismissed as a possible cause of CCD.
This early dismissal of Nosema ceranae by senior and influential researchers may have biased the direction of research and research funding in the US away from N. ceranae and towards IAPV. This may change with more recent US research that found that in some cases N. ceranae was present in levels high enough to cause colony collapse (van Engelsdorp et al. 2009).
Additionally, perhaps the time has come for greater collaboration between European and US scientists on the potential role of Nosema ceranae in North American cases of CCD. It would at least be useful to rule it out through direct experimentation, rather than indirectly through correlation, especially given the substantial scientific support for its role in CCD in Europe.
Second, research on Nosema ceranae in Europe has been going on a lot longer than research on CCD and IAPV in particular, in the North America. The first papers suggesting a role for N. ceranae in colony collapse were published in 2006, based on research completed in 2005 or earlier, while IAPV emerged as a pathogen of concern in 2007. Based on the publication pattern observed for N. ceranae ( 1 paper in 1996, 2 papers in 2006, 5 papers in 2007, 6 papers in 2008, and 8 papers in 2009) perhaps we can expect more substantive papers on the link between IAPV, or some other virus, and CCD over the next few years.
For example, in their recent article in the popular science magazine Scientific American, Cox-Foster and vanEngelsdorp (2009) describe an experiment in which honey bees were experimentally infected with IAPV and then exhibited symptoms consistent with CCD 1-2 weeks later. While this is consistent with the hypothesis that that IAPV causes CCD, they also observed colonies infected with IAPV that did not collapse, and in fact, some of them even managed to rid themselves of the virus. (While this information is interesting, it was not reported in a peer-reviewed journal, thus I did not consider it in the weight of evidence analysis.)
Third, it is important to remember that CCD is not a ‘thing’, but a collection of symptoms. It is possible these symptoms may arise from multiple causes and that CCD in North America may result from a different set of factors than colony collapse in Europe. This ‘multiple factor’ hypothesis is also one of the contenders brought forward during the early days of CCD, and as noted earlier, seems to be where some US researchers are beginning to focus.
In the meantime, the overwhelming weight of scientific evidence for the cause-effect link between Nosema ceranae and colony collapse in Europe, as well as the presence of N. ceranae in North America, supports the adoption of precautionary beekeeping practices. In fact, some professional beekeepers already manage their operations under the assumption that N. ceranae is the primary culprit in colony collapse (Vass 2009).
Next post CCD post: Pesticides and CCD. Cheers.
References for This Post:
Anderson, D. and I.J. East. 2008. The Latest Buzz About Colony Collapse Disorder. Science 8 February 2008: 724c-725c. Letter in response to Cox-Foster et al. 2007.
Blanchard P, Schurr F, Celle O, Cougoule N, Drajnudel P, Thiéry R, Faucon JP, Ribière M. 2008. First detection of Israeli acute paralysis virus (IAPV) in France, a dicistrovirus affecting honeybees (Apis mellifera). Journal of Invertebrate Pathology. July 30, 2008 online
CBC news (April 22, 2009). ``Parasite behind European honeybee colony collapse, researchers say`` (about the Higes et al 2009 paper below)
Cox-Foster, D. and D. vanEngelsdorp. (April 2009). Saving the Honeybee. Scientific American Magazine. See this link – online version: Solving the Mystery of the Vanishing Bees
Cox-Foster, D.L., S. Conlan, E.C. Holmes, G. Palacios, J.D. Evans, N.A. Moran, P. Quan, T. Briese, M. Hornig, D.M. Geiser, V. Martinson, D. vanEngelsdorp, A.L. Kalkstein, A. Drysdale, J. Hui, J. Zhai, L. Cui, S.K. Hutchison, J.F. Simons, M. Egholm, J.S. Pettis and W.I. Lipkin. 2007. A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder. Science 318 (5848): 283 – 287.
Chen, Yanping and J.D. Evans 2007. Historical Presence of Israeli Acute Paralysis Virus in the United States. American Bee Journal (here too)
Chen, Y., J.D. Evans, I.B. Smith and J.S. Pettis. 2008. Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology 97(2): 186-188.
Fries I., R. Martin, A. Meana, P. Garcia-Palencia, M. Higes. 2006. Natural infections of Nosema ceranae in European honey bees. J Apicult Res 45: 230–233.
Fries, I., F. Feng, A. da Silva, S.B. Slemenda, N.J. Pieniazek. 1996. Nosema ceranae n. sp. (Microsporidia, Nosematidae), Morphological and Molecular Characterization of a Microsporidian Parasite of the Asian Honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32(3): 356-365.
Giersch, T., T. Berg, F. Galea and M. Hornitzky. 2009. Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie 40 (2009) 117-123
Higes, M., R. Martín-Hernández, E. Garrido-Bailón, A.V. González-Porto, P. García-Palencia, A.Meana, M.J. del Nozal, R. Mayo and J.L. Bernal. 2009. Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports Volume 1 Issue 2, Pages 110 – 113, Published Online: 16 Feb 2009.
Higes, M., Raquel Martín-Hernández, Cristina Botías, Encarna Garrido Bailón, Amelia V. González-Porto, Laura Barrios, M. Jesús del Nozal, José L. Bernal, Juan J. Jiménez, Pilar García Palencia and Aránzazu Meana. 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, doi:10.1111/j.1462-2920.2008.01687.x
Higes, M., P. García-Palencia, R. Martín-Hernández and A. Meana. 2007. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology 94(3), March 2007, Pages 211-217
Higes, M., R. Martína and A. Meana. 2006. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology 92(2): 93-95, June 2006. doi:10.1016/j.jip.2006.02.005
Huang, W., J. Jiang, Y. Chen and C. Wang. 2007. A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38 (2007) 30-37, DOI: 10.1051/apido:2006054
Invernizzi, C. , C. Abud, I.H. Tomasco, J. Harriet, G. Ramallo, J. Campá, H. Katz, G. Gardiol and Y. Mendoza. 2009. Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. Journal of Invertebrate Pathology, 101(2): 150-153, June 2009.
Klee, J., A.M. Besana, E. Genersch, S. Gisder, A. Nanetti, D.Q. Tam, T.X. Chinh, F. Puerta, J.M. Ruz, P. Kryger, D. Message, F. Hatjina, S. Korpela, I. Fries and R.J. Paxton. 2007. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology Volume 96, Issue 1, September 2007, Pages 1-10
Maori, E., N. Paldi, S. Shafir, H. Kalev, E. Tsur, E. Glick and I. Sela. 2009. IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion. Insect Molecular Biology 18(1): 55 – 60, Published Online: 19 Jan 2009.
Maori, E., S. Lavi, R. Mozes-Koch, Y. Gantman, Y. Peretz, O. Edelbaum, E. Tanne and I. Sela. 2007. Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination. J Gen Virol 88 (2007), 3428-3438; DOI 10.1099/vir.0.83284-0.
Martín-Hernández, R., A. Meana, L. Prieto, A.M. Salvador, E. Garrido-Bailón and M. Higes. 2007. Outcome of Colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73(20): 6331-6338
Paxton, R.J., J. Klee, S. Korpela and I. Fries. 2007. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38:558-565, DOI: 10.1051/apido:2007037.
Palacios, G. et al. 2008. Genetic Analysis of Israel Acute Paralysis Virus: Distinct Clusters Are Circulating in the United States. Journal of Virology, July 2008, p. 6209-6217, Vol. 82, No. 13 doi:10.1128/JVI.00251-08
Russell, S. (April 25, 2007). “UCSF scientist tracks down suspect in honeybee deaths” San Francisco Chronicle
Tapaszti, Z., P. Forgách, C. Kővágó, L. Békési, T. Bakonyi, M. Rusvai. 2009. First detection and dominance of Nosema ceranae in Hungarian honeybee colonies. Acta Veterinaria Hungarica 57(3): 383-388, September 2009, DOI 10.1556/AVet.57.2009.3.4. Online Date Monday, July 27, 2009
vanEngelsdorp, D., J.D. Evans, C. Saegerman, C. Mullin, E. Haubruge, B.K. Nguyen, M. Frazier, J. Frazier, D. Cox-Foster, Y. Chen, R. Underwood, D.R. Tarpy, J.S. Pettis. 2009. Colony Collapse Disorder: A Descriptive Study. PLoS ONE 4(8): e6481. doi:10.1371/journal.pone.0006481 (Received: March 6, 2009; Accepted: June 29, 2009; Published: August 3, 2009)
Vass, Keith. (July 20, 2009). Bees are back as scientists uncover cause of colony collapse disorder. Saanich News.
Williams, G.R., A.B.A. Shafer, R.E.L. Rogers, D. Shutler and D.T. Stewart. 2008a. First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. Journal of Invertebrate Pathology 97(2): 189-192 (February 2008), doi:10.1016/j.jip.2007.08.005.
Other IAPV and Nosema ceranae references of interest:
Antúnez, K., R. Martín-Hernández, L. Prieto, A. Meana, P. Zunino and M. Higes. 2009. Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology, doi:10.1111/j.1462-2920.2009.01953.x
Cornman, R.S., Y.P. Chen, M.C. Schatz, C. Street, Y. Zhao, B. Desany, M. Egholm, S. Hutchison, J.S.
Pettis, W.I. Lipkin and J.D. Evans. 2009. Genomic Analyses of the Microsporidian Nosema ceranae, an Emergent Pathogen of Honey Bees. PLoS Pathog. 2009 June; 5(6): e1000466. Published online 2009 June 5. doi: 10.1371/journal.ppat.1000466.
Hayley, J. (July 19, 2007). Asian Parasite Killing Western Bees. Planet Ark.
M. Higes, R. Martín-Hernández, P. García-Palencia, P. Marín and A. Meana. 2009. Horizontal transmission of Nosema ceranae (Microsporidia) from worker honeybees to queens (Apis mellifera). Environmental Microbiology Reports, doi:10.1111/j.1758-2229.2009.00052.x.
Higes, M., Raquel Martı´n-Herna´ndez, Encarna Garrido-Bailo´n, Pilar Garcı´a-Palencia, Ara´nzazu Meana. 2008. Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. Journal of Invertebrate Pathology 97 (2008) 76–78.
Maori, E., Tanne, E. & Sela, I. 2007. Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes. Virology 362, 342–349. {cited by Cox-Foster et al 2007 as paper that says IAPV first reported in 2004}
Maori, E., E. Tanne and I. Sela. 2007. Corrigendum to “Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes” Virology 362: 342–349. Virology 368(1), 10 November 2007, Page 218.
Mayack, C. and D. Naug. 2009. Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology 100(3): 185-188.
Pajuelo, A.G., C. Torres, F.J.O. Bermejo. 2008. Colony losses: A double blind trial on the influence of supplementary protein nutrition and preventative treatment with fumagillin against Nosema ceranae. J Apicult Res 47: 84–86.
Williams, G. R., Michelle A. Sampson, Dave Shutler and Richard E.L. Rogers. 2008. Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? Journal of Invertebrate Pathology Volume 99, Issue 3, November 2008, Pages 342-344 doi:10.1016/j.jip.2008.04.005
“The copyright of the article ‘Honey Bee Colony Collapse Disorder (CCD) VII: IAPV, Nosema ceranae, and CCD’ on ‘What’s Your Ecotype?’ is owned by Ian Parnell. Permission to republish ‘Honey Bee Colony Collapse Disorder (CCD) VII: IAPV, Nosema ceranae, and CCD’ in print or online must be granted by the author in writing.”
Previous posts about CCD:
Honey Bee Colony Collapse Disorder (CCD) I: Should we really be surprised? (May 28, 2007)
Honey Bee Colony Collapse Disorder (CCD) II: What’s causing it? (May 30, 2007)
Green Grazing: Water, Flying Food, Ground-level Ozone, Farmland Biodiversity and Colony Collapse Disorder (July 28, 2007)
Green Grazing: SUDS, Biodiversity Stuff, More About Bees, African Agriculture, and Satellite Fish (August 2, 2007)
Honey Bee Colony Collapse Disorder (CCD) III: The Power of the Press Release (September 28, 2007)
Honey bee Colony Collapse Disorder (CCD) IV: IAPV, CCD, Australian Bees and the Silence of the Press (March 27, 2008)
Honey Bee Colony Collapse Disorder (CCD) V: Trends in Reporting and Research (June 12, 2009)
Honey Bee Colony Collapse Disorder (CCD) VI: The Global Status of CCD (July 10, 2009).






