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Insights & Perspectives Commentary Colony Collapse Disorder in context Geoffrey R. Williams1)2)Ã, David R. Tarpy3), Dennis vanEngelsdorp4), Marie-Pierre Chauzat5), Diana L. Cox-Foster4), Keith S. Delaplane6), Peter Neumann7)8), Jeffery S. Pettis9), Richard E. L. Rogers10) and Dave Shutler2) Although most of humanity relies upon in the past, such as the so-called unex- morbidities occurring worldwide. In foods that do not require animal polli- plainable ‘‘Isle of Wight’’ disease in the many cases, these morbidities can be nation , production of 39 of the early 1900s , the magnitude and explained by known parasites or bee- world’s 57 most important monoculture velocity of these recent declines are keeper management issues. One crops still beneﬁts from this ecosystem likely unprecedented. Often in the example is the devastation caused by service . Western honey bees (Apis media (e.g. ‘‘Mobile phones responsible beekeepers’ inability to control mellifera) are undoubtedly the single- for disappearance of honey bee,’’ avail- V. destructor, which not only feeds most valuable animal pollinators to able at www.telegraph.co.uk), and on host haemolymph and weakens agriculture because they can be easily sometimes in the scientiﬁc literature host immunity but also vectors a maintained and transported to pollina- (e.g. ), these losses are inappropri- variety of viruses . In other cases, tor-dependent crops. Yet, despite an ately equated with ‘‘Colony Collapse however, these morbidities are genu- almost 50% increase in world honey Disorder’’ or CCD, which is character- inely unexplainable, including those bee stocks over the last century, bee- ized by the rapid disappearance of attributed to CCD sensu stricto . In keepers have not kept pace with the adult bees from colonies containing recent winters, colony mortality in >300% increase in pollinator-depend- brood and food stores but lacking dam- Europe has averaged $20% (ranging ent crops . This has led to great uncer- aging levels of parasitic Varroa destruc- from 1.8 to 53% among countries), with tainty surrounding the recent large- tor mites or Nosema microsporidians starvation and parasites believed to be scale die-offs of honey bees around . the main contributors (‘‘Proceedings of the world, and has sparked enormous Although, we agree that CCD is the 4th COLOSS Conference, Zagreb, interest from both scientists and the indeed a signiﬁcant cause for concern, Croatia, 3-4 March 2009’’, available general public. we believe that it is imperative to at www.coloss.org/publications). Although sharp regional declines in appropriately place CCD within the Colony mortality during the 2006/ honey bee populations have occurred greater context of other honey bee 2007, 2007/2008, and 2008/2009 win- ters in the US, the only country where CCD has been documented sensu stricto, was 32% , 36% , and 29% , DOI 10.1002/bies.201000075 respectively. During the winter of 2008/2009, $10% of the 2.3 million 1) 9) Department of Biology, Dalhousie University, United States Department of Agriculture, managed honey bee colonies in the US Halifax, NS, Canada Agricultural Research Service, Beltsville, MD, 2) died with ‘‘CCD-like symptoms’’, and US Department of Biology, Acadia University, USA Wolfville, NS, Canada 10) Ecotoxicology, Bayer CropScience, Research beekeepers self-diagnosed CCD as only 3) Department of Entomology, North Carolina Triangle Park, NC, USA the 8th most important contributor to State University, Raleigh, NC, USA 4) Department of Entomology, The Pennsylvania State University, University Park, PA, USA 5) *Corresponding author: French Food Safety Agency (AFSSA), Sophia- Geoffrey R. Williams Antipolis, France * The commentary was produced in a consultatory 6) E-mail: firstname.lastname@example.org Department of Entomology, University of process initiated by Geoffrey R. Williams, and Georgia, Athens, GA, USA involving the other authors. The paper was written 7) Abbreviation: Swiss Bee Research Centre, Agroscope by Geoffrey R. Williams, David R. Tarpy, Dennis Liebefeld-Posieux Research Station ALP, CCD, Colony Collapse Disorder. van Engelsdorp, Keith S. Delaplane and Dave Bern, Switzerland Shutler with contribution of additional ideas and 8) Department of Zoology and Entomology, comments by Marie-Pierre Chauzat, Diana L. Rhodes University, Grahamstown, South Cox-Foster, Peter Neumann, Jeffery S. Pettis and Africa Richard E. L. Rogers. Bioessays 32: 845–846,ß 2010 WILEY Periodicals, Inc. www.bioessays-journal.com 845 G. R. Williams et al. Insights & Perspectives ..... colony mortality, behind starvation, discriminate among types of colony 6. vanEngelsdorp D, Evans JD, Saegerman C, et al. 2009. Colony Collapse Disorder: a queen-related issues, and parasites . mortality occurring worldwide. This will descriptive study. PLoS One 4: e6481. The point is, honey bees die from many permit a more informed and appropriate 7. Rosenkranz P, Aumeier P, Ziegelmann B. Commentary things. We must be careful to not syno- allocation of research efforts into CCD 2010. Biology and control of Varroa destruc- tor. J Invertebr Pathol 103: S96–S119. nymize CCD with all honey bee losses. speciﬁcally and other causes of 8. vanEngelsdorp D, Underwood R, Caron D, There is a growing consensus that mortality in general. et al. 2007. An estimate of managed colony colony mortality is the product of losses in the winter of 2006–2007: a report multiple factors, both known and commissioned by the Apiary Inspectors of America. Am Bee J 147: 599–603. unknown, acting singly or in combi- References 9. vanEngelsdorp D, Hayes J, Underwood nation [11, 12]. Considering the reliance RM, et al. 2008. A survey of honey bee colony that modern agriculture places on hon- 1. Ghazoul J. 2005. Buzziness as usual? losses in the U.S., fall 2007 to spring 2008. Questioning the global pollination crisis. PLoS One 3: e4071. ey bees for pollination, coordinated 10. vanEngelsdorp D, Hayes J, Underwood Trends Ecol Evol 20: 367–73. efforts, such as those of CANPOLIN ` 2. Klein AM, Vaissiere BE, Cane JH, et al. 2007. RM, et al. 2010. A survey of honey bee colony (Canadian Pollination Initiative, Importance of pollinators in changing land- losses in the United States, fall 2008 to spring scapes for world crops. Proc R Soc B-Biol 2009. J Apic Res 49: 7–14. www.uoguelph.ca/canpolin), COLOSS Sci 274: 303–13. 11. Rogers REL, Williams GR. 2007. Honey bee (Prevention of Honeybee Colony 3. Aizen MA, Harder LD. 2009. The global stock health in crisis: what is causing bee mortality? Losses, www.coloss.org), and the US of domesticated honey bees is growing Am Bee J 147: 441. Department of Agriculture’s Areawide slower than agricultural demand for pollina- 12. Neumann P, Carreck NL. 2010. Honey bee tion. Curr Biol 19: 915–8. colony losses. J Apic Res 49: 1–6. and Managed Pollinator CAP 4. Underwood R, vanEngelsdorp D. 2007. 13. Pettis JS, Delaplane KS. 2010. Coordinated (Coordinated Agricultural Project) , Colony collapse disorder: have we seen this responses to honey bee decline in the USA. are urgently needed to understand and before? Bee Culture 35: 13–8. Apidologie 41: 256–63. mitigate these losses. The ﬁrst step in 5. Ratnieks FLW, Carreck NL. 2010. Clarity on honey bee collapse? Science 327: 152–3. these efforts should be to objectively 846 Bioessays 32: 845–846,ß 2010 WILEY Periodicals, Inc.
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