The Occasional Hymenoptera: CCD virus transmitted by pollen?

Colony Collapse Disorder (“CCD”) refers to a phenomenon first described in 2006 by which workers of a colony of European honey bees (Apis mellifera) suddenly die off, leaving insufficient brood cover. The bodies of the dead bees, however, are not found in the hive or immediate area. In this disorder the queen remains in the nest, and usually capped brood are present. The disorder has been reported throughout the United States and Western Europe. There have been occasional reports of similar phenomena back to the nineteenth century. See R. Underwood, D. vanEngelsdorp, “Colony Collapse Disorder: have we seen this before?,” 35 Bee Cult. 13–18 (2007), which describes 18 events of sudden colony deaths dated back to 1869. It is not known, however, whether those instances represent the same disorder; in fact, the nature of the currently described disorder is not well understood.

Many causes have been suggested: electromagnetic radiation, climate change, pesticides, modified crops, malnutrition, antibiotics, pesticides, viruses, bacteria and fungus. One odd feature of this phenomenon is that colonies which have died from CCD generally are not attacked by predators  (or at least not for a substantial time), unlike other cases of a dying colony where workers from healthy colonies invade the colony to plunder its stores.

In June 2009 the CCD Steering Committee (a group of 8 federal agencies coordinated by the Department of Agriculture charged by Congress to report on developments) issued its first annual report, based on work among the agencies and 22 universities, and came to the conclusion that the disorder probably involved the combination of several factors acting synergistically. Colony Collapse Disorder Progress Report (June 2009) (pdf file). This conclusion was amplified by an extensive survey of colony die off, undertaken by researchers from Penn State and published in 2009. The authors concluded there was no one single cause identifiable in the cases they studied, but suggested that CCD involves an interaction between pathogens and other stress factors:

“While no single pathogen or parasite was found with sufficient frequency to conclude a single organism was involved in CCD, pathogens seem likely to play a critical (albeit secondary) role. CCD colonies generally had higher virus loads and were co-infected with a greater number of disease agents than control colonies. Elevated virus and Nosema spp. levels potentially explain the symptoms associated with CCD. One possible way honey bees regulate pathogen and parasite loads within a colony is for infected individuals to emigrate from their hive.” Dennis vanEngelsdorp, et al., “Colony Collapse Disorder: A Descriptive Study,” 4 PLoS e6481 (published online August 3, 2009) (open access).

A leading early candidate was the Varroa destructor mite. This parasite lays eggs in capped larvae. The eggs hatch when the larvae emerge and infect other bees. The hemolymph (i.e., blood-like fluid) of adult bees is sucked by the mites for nutrition. This parasitism leaves the bee vulnerable to other infections. In fact, the mite has been found to carry various RNA viruses which infect honey bees. The mite has not been found in all cases of CCD, however.

The same problem applies to attributing the cause to the fungus Nosema ceranae. This single celled parasite has long been known to cause nosemosis, the principal symptoms of which are dysentery and swelling abdomens of workers. Like CCD it usually does not affect the queen. But although it was found in many hives in Pennsylvania and Spain, it does not account for all cases of CCD.

In October 2010 a paper by Jerry J. Bromenshenk of the University of Montana and others reported on the discovery of a new DNA virus in cases of CCD. The paper claimed that the combination of this virus (invertebrate iridescent virus or IIV6) together with Nosema ceranae was found present in all cases of CCD they studied. They found that neither was fatal by itself, but in combination they proved fatal. Jerry J. Bromenshenk, Colin B. Henderson, Charles H. Wick, Michael F. Stanford, Alan W. Zulich, Rabih E. Jabbour, Samir V. Deshpande, Patrick E. McCubbin, Robert A. Seccomb, Phillip M. Welch, Trevor Williams, David R. Firth, Evan Skowronski, Margaret M. Lehmann, Shan L. Bilimoria, Joanna Gress, Kevin W. Wanner, Robert A. Cramer Jr, “Iridovirus and Microsporidian Linked to Honey Bee Colony Decline,” 5 PLoS One e13181 (published online October 6, 2010) (open access). The article was featured in PLoS Hubs, and the New York Times hailed the paper as a “solution” to the CCD “mystery.” See Kirk Johnson, “Scientists and Soldiers Solve A Bee Mystery,” New York Times (October 7, 2010) (log-in required). Fortune Magazine soon thereafter revealed that  Bromenshenk had not disclosed either to the Times or PLoS his conflict-of-interest from funding by a pesticide concern. See Katherine Eban, “What a scientist didn’t tell the New York Times about his study on bee deaths,” Fortune (October 8, 2010). (The PLoS paper now has a disclosure section.) The astonishing thing about Bromenshenk’s conflict is that, according to Fortune, before he had begun receiving funding from the company, he had been an expert witness against the company in a class action suit alleging damage to bees caused by pesticides. He withdrew as a witness and then received the grant. This is simply an astonishing example of a “purchased” expert and ought to be weighed very heavily in examining any study or experiment construction by Bromenshenk. (It also ought to prevent him from being used as an “expert” in any litigation hereafter.) Other authors in the study had other relationships with companies doing business with the federal agency which provided funding for the study. The study in PLoS took no account of pesticides. Of course, the non-disclosed conflict does not disprove the study, but, as we have seen, even in science people tend to see what they want and not what they don’t, and scientists are selected for studies who have certain expectations. Money is perhaps at least as powerful as religion in clouding judgments. The appearance of a problem is heightened when the apparent conflict is not disclosed by the author.

However the results turn out on further efforts to duplicate them, one problem that appears on its face is that like the explanation that Nocema alone causes CCD, it seems to fail because Nocema was not found in all cases of CCD surveyed by the researches in the vanEngelsdorp study. So for the moment we’ll leave that conclusion until it is duplicated by others.

A study published last month by Penn State researches, while not attempting to ascribe a cause to CCD, came to interesting conclusions about the spread of RNA viruses among honey bees and other species. The paper provides evidence that transmission of RNA viruses takes place through pollen transfer and that this provides a mechanism for transfer of the viruses between species. Rajwinder Singh, Abby L. Levitt, Edwin G. Rajotte,Edward C. Holmes, Nancy Ostiguy, Dennis vanEngelsdorp, W. Ian Lipkin, Claude W. dePamphilis, Amy L. Toth, Diana L. Cox-Foster, “RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-Apis Hymenopteran Species,” 5 PLoS ONE e14357 (open access).

Honey bee carrying pollen in a pollen sac

By using reverse transcriptase-PCR the researchers were able to isolate certain viruses known to infect honeybees in pollen collected from forager bees. These viruses–deformed wing virus (DWV), sacbrood virus (SBV) and black queen cell virus (BQCV)–are positive sense, single-stranded RNA viruses. Like other similar viruses (such as polio) these viruses are able to infect a variety of tissue, and can be found in glandular secretions of worker bees and bee feces. It was known that these viruses could be transferred vertically, i.e., from infected queens and drones to offspring. This study, however, is the first to show a route of horizontal infection–via pollen.

Click on image to enlarge.

The study showed that some pollen particles contained these viruses, while the forager carrying it did not. You can see from a figure from the study the relative frequencies of the various viruses in the foragers and the pollen pellets analyzed. The inference to be drawn from this fact is that pollen carried back to a hive  by an uninfected forager can be the source for virus infection in the hive.

A field experiment demonstrated that viruses detected in bee bread (stored pollen) and honey were infectious. Moreover field samples showed that 11 non-Apis pollen-gatherers were infected with the 3 viruses mentioned above or Kashmir bee virus (KBV) and Israeli acute paralysis virus (IAPV). The species were three common bumble bee species (Bombus impatiensB. vagans, B. ternarius), the eastern carpenter bee (Xylocopa virginica), the small carpenter bee (Ceratina dupla), a sweat bee (Augochlora pura), mining bees (Andrena sp.), a yellow jacket (Vespula vulgaris), paper wasps (Polistes metricus, P. fuscatus) and sand wasp (Bembix sp.). That these species were infected via pollen is suggested by the fact that IAPV was detected only in non-Apis pollin-collectors found near the apiaries of honey bees with IAPV (in observations in Pennsylvania and New York). A table showing the presence of viruses in non-Apis pollen collectors found in the study can be seen here.

The researches experimentally showed that one of the viruses, IAPV, could be transferred from honey bees to bumble bees via pollen. They observed in a greenhouse that bumble bees did not feed from a sugar solution that honey bees fed from. So in 2008 they introduced two infection free strains of honey bees and bumble bees. IAPV infected sugar solution was introduced. Within a week the bumble bees were infected. In 2009 the reverse was proved. Infected bumble bees were introduced and within 10 days one of the three honey bee hives was infected. When a different strain of IAPV was introduced in the sugar water, within a week all three bumble bee hives were infected.

All of this amounts to very strong evidence that certain honey bee viruses are transmitted intra- and inter-species by pollen collection. Needless to say, the inter-species spread of viruses that might be implicated in CCD is a worrisome development. The implications go beyond the commercial losses of honey producers. To the extent that plants depend on pollinators susceptible to decimation by such viruses are at risk as well. A wider ecological disaster is possible.

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