Honeybee Colony Losses and Honeybee Health Issues – Recent Scientific Literature and Findings on Causative Factors
Monheim, August 16, 2010 – So far, increased colony losses have recently been reported from Europe, the USA, the Middle East and Japan, but not from South America, Africa and Australia. Apiculture has been in decline in both Europe and the USA over the recent decades, as is shown by the decreasing numbers of managed honey bee colonies in some regions. In the last years the losses of honey bee colonies have received considerable public attention, and the world’s press has been full of eye-catching but often uninformative headlines proclaiming the dramatic demise of the honey bee. “Colony Collapse Disorder” (CCD) in the USA has attracted great attention, and scientists there and in Europe are working hard to provide explanations for these extensive colony losses.
As the result, over the last months, several scientific papers were issued which report the results of studies on honey bee health issues and honey bee colony losses. Some of them do comprehensively deal with the issue of bee health problems as a whole, whereas others focus on particular factors that may be involved in honey bee colony losses. It is obvious that it is widely agreed among most of the scientists who are involved in the investigation of the backgrounds and causative factors of the observed bee health and bee colony mortality issues that the most relevant key factors are diseases and parasites, as individual stressors as well as in combination.
In the following, a short overview is given about some of the most relevant, recent scientific publications dealing with the backgrounds of bee colony losses and their multifactorial origins.
1.) Clearly, bee colony losses are not a new phenomenon, they just gained more attention: van Engelsdorp and Meixner (2009) examined the historical records and showed that occurrences of extensive losses are not unusual. Already almost a century ago, in 1906, beekeepers on the Isle of Wight (England) for instance, noticed that many of their honey bee colonies were dying, with numerous bees crawling from the hive unable to fly. Older records report massive bee colony losses without obvious disease symptoms from Australia in 1872 (Beuhne 1910).
2.) From a global point of view even the impression of massive bee declines is wrong: According to the FAO (2009) the global stocks of honey bee colonies increased by 64% between 1961 and 2007. However, not all regions have experienced gains. Notably, managed colonies decreased in both Europe (26.5%) and North America (49.5%), while large increases were recorded for Asia (426%), Africa (130%), South America (86%), and Oceania (39%).
3.) Even in Europe, there is no consistent trend towards a bee population decline: whereas there is a decline in particular in Northern and Central European countries (which is basically linked to a falling number of beekeepers in these countries), the number of managed bee colonies is even raising in many Southern European Countries (Potts 2010).
4.) In their joint publication which first appeared in June 2009, the Argentinean ecologist Marcelo A. Aizen and the Canadian biologist Lawrence D. Harder came to the conclusion that the number of bee colonies is growing globally. Regional or national setbacks have no appreciable influence on this. The fact that the numbers of colonies are declining in some of the European industrialized countries and in the USA is due in part to the lower economic attractiveness of beekeeping, resulting, for example, from cheap honey imports from third countries, or to the ageing of active beekeepers and their declining numbers. Despite a global increase in the numbers of bee colonies, they will not develop fast enough to keep up with the rapidly growing pollination requirements of worldwide agriculture. According to Aizen and Harder, two essential factors are necessary to counteract this – greater economic attractiveness, and measures to improve bee health. (Aizen, Harder June 2009 and October 2009).
5.) The most comprehensive recent pieces of work on honey bee health issues and honey bee colony losses are the Scientific Report “Bee Mortality and Bee Surveillance in Europe” submitted by an international group of independent bee researchers to the European Agency for Food Safety EFSA in 2009 (Hendrikx et al. 2009), and the Special Issue “Colony Losses” of the Journal of Apicultural Research (Various Authors 2010a). The EFSA report provides an assessment of the bee health surveillance systems in Europe, and an evaluation and analysis of the existing data and publications related to honeybee colony mortality across Europe. The purpose of the document was to provide a review and assessment of existing bee health surveillance systems in Europe, to evaluate the information available about the phenomenon of colony losses and potential causative factors, and to come up with recommendations how to further address this issue on EU level in terms of improvement of surveillance systems and of research activities to further elucidate the topic. About potential causative factors involved in the observed colony losses, the EFSA report comes to the conclusion that “There is a consensus amongst the scientific community that the causes of colony losses in Europe and the United States are likely to be multifactorial”. There are a plenty of potentially involved factors listed like beekeeping and husbandry practices (feeding, migratory beekeeping, treatments and so forth), environmental factors (climate, biodiversity, etc.), chemical factors (plant protection products) or biological agents (Varroa, Nosema, etc.). However, it is pointed out that no involvement of plant protection products has been proven for colony losses or CCD, and that “High concentrations of pesticides have rarely been identified in relation to colony losses in USA and Europe” (only in cases of acute intoxication incidents, which are mostly based on mis-uses of products).
6.) The special issue of the Journal of Apicultural Research dealing with the topic of honey bee colony losses contains 31 articles dealing with the recently observed phenomenon of in many regions occurring honeybee colony losses. The articles describe the current status in different countries and investigate different putative causal factors. As the key causative factor involved in the currently reported colony losses, the vast majority of authors sees the parasitic mite Varroa destructor (or, respectively, insufficient Varroa treatment and the increasing resistance of the mite against varroacides). However, most authors agree that the problem is not caused by Varroa alone, and assume a multi- factorial origin of the colony losses. Other involved factors are a multitude of diseases and parasites (their relative importance is controversially debated), hive management and beekeeping practices, climatic factors, queen health issues, nutritional problems, loss of genetic diversity, and environmental factors like the structure of modern agricultural landscapes. Pesticides are listed by some authors as a potentially contributing factor, although there is very few concrete evidence of their involvement as a causal factor in most of the articles, some even rule them out as causes of increased mortality in their reported case examples. Overall, it can be summarized that the researchers contributing to the special issue of the Journal of Apicultural Research in their vast majority do not see pesticides as a key factor causing the observed colony losses, most of them do not even consider them a particularly relevant factor at all. In no case, pesticides were proven to be involved in colony losses as a general or key causal factor, with the exception of some references to incidents (e.g. potential dust exposure) or mis-use (e.g. off-label sprays in orchards).
7.) In 2008, the French Agency for Food Safety AFSSA conducted a comprehensive survey on weakening, collapse and mortality of bee colonies in France (revised version in 2009). The researchers elaborated a plenty of potential causative factors involved in colony mortalities. As main cause of bee health problems, pathogens and parasites are identified: “The Varroa destructor mite and the relatively ineffective methods available to control this pathogen appear to be a major risk factor for winter mortality in honey bee colonies. Other biological pathogens, such as some viruses (CBPV), Nosema sp., Paenibacillus larvae, etc., also play a role in the increasing mortality rate observed in certain apiaries.” Influence of pesticides on bee mortality is particularly seen in cases where products are mis-used and incorrectly applied. The scientists found no evidence substantiating “the hypothesis that chronic exposure of bee colonies to some of these products may play a direct or adjuvant role with respect to certain known biological pathogens.”
8.) Another recent overview article was published by Ratnieks and Carreck (2010) in the renowned scientific journal Science. In this article, potential causative factors of bee colony mortality and colony collapse are introduced and briefly discussed. Among the key findings, the following conclusions are of relevance: “Although full explanations for these losses are still debatable, the consensus seems to be that pests and pathogens are the single most important cause of colony losses.”, and “After 10 years of research, it seems unlikely that imidacloprid was responsible for the French bee deaths […].” This reasoning is in line with the majority of all studies published on this question over the last ten years.
9.) A further important publication reporting the results of a large-scale long-term bee health monitoring project, the German Bee Monitoring, is Genersch et al. (2010a). The authors present a four-year study involving more than 1200 bee colonies from about 120 apiaries all over Germany which were monitored for the entire study period for their health and survival in connection with all factors that may potentially affect bee health. Concurrently, the monitored hives were surveyed for residues of plant protection products. About causes of bee colony mortality, the authors conclude: “The main cause of overwintering problems was undoubtedly infestation with the ectoparasitic mite Varroa destructor followed by viral infections. The infestation with Varroa destructor in fall clearly revealed the highest relation with winter losses of honey bee colonies.” Residue detects did not correlate with poor colony development and colony mortality, and there was no significant difference in overwintering success between apiaries with no residues of plant protection products in the bee bread and those with higher amounts of residues. A particular focus of the monitoring was on Neonicotinoids. Nevertheless, there were hardly any findings of these compounds, although many of the monitored colonies were exposed to crops which are typically treated with these products (e.g. oilseed rape).
10.) In another recent review paper on current threats to honey bees and beekeeping (Genersch 2010), the conclusion is: “Although the phenomenon “decline of honey bees” is far from being finally solved, consensus exists that pests and pathogens are the single most important cause of otherwise inexplicable colony losses.” and “It is clear that several biological and environmental factors acting alone or in combination have the potential to cause premature colony mortality by adversely affecting colony health and lifespan. Among these factors, certain honey bee diseases and parasites have been shown to play a significant role in increased honey bee colony mortality and in the described colony losses.”
11.) In a large-scale study on hundred apiaries in Spain, correlations between hive depopulation and putative causal factors involved in bee colony losses were investigated. No correlation was found between colony health status and residues of plant protection products (among them Imidacloprid) on the one hand and the occurrence of the Israeli Acute Paralysis virus on the other hand (Garrido-Bailón et al. 2010).
12.) Finally, another comprehensive work on honeybee health issues was published in a Supplement Volume of the Journal of Invertebrate Pathology (Various Authors 2010b). As expressed in the preface of the volume: “Perhaps most importantly, honeybees are attacked by parasitic mites (Varroa destructor, Acarapis woodi, Tropilaelaps spp.), fungi (Nosema spp., Ascosphaera apis), bacteria (Paenibacillus larvae, Melissococcus plutonius), numerous viruses, and scavengers (from beetles and mice to bears) during any life stage.” (Genersch et al 2010b).
13.) This is in line with the findings published by Johnson, Berenbaum et al. (2009): in a study investigating gene expression in the guts of bees of CCD colonies in comparison to healthy colonies, they found no elevated expression of pesticide response genes, but unusual ribosomal RNA fragments that were conspicuously more abundant in the guts of CCD bees. The presence of these fragments is interpreted as a possible consequence of infections with viruses that affect translation processes.
References
AFSSA (2009): Weakening, collapse and mortality of bee colonies. http://www.afssa.fr/Documents/SANT-Ra-MortaliteAbeillesEN.pdf: 222 pp.
Aizen, M. and Harder, L. (2009): The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination, Current Biology, vol 19, No 11, 1-4,
Aizen, M. and Harder, L. (2009): The truth about the disappearing honeybees, http://www.newscientist.com/article/mg20427316.800-the-truth-about-thedisappearing- honeybees.html
Beuhne, R. (1910): Bee mortality. Journal of the Department of Agriculture of Victoria, Australia 8: 149-151
Hendrikx, P., M.-P. Chauzat, M. Debin, P. Neumann, I. Fries, W. Ritter, M. Brown, F. Mutinelli, Y. Le Conte & A. Gregorc (2009) : Scientific Report Submitted to EFSA : Bee Mortality and Bee Surveillance in Europe. https://secure.fera.defra.gov.uk/beebase/downloadNews.cfm?id=54: 217 pp.
FAO (2009). ProdSTAT Database. Food and Agriculture Organization of the United Nations. Available at http://faostat.fao.org/default.aspx
Garrido-Bailón, E., R. Martín-Hernández, J. Bernal, J. L. Bernal, A. Martínez-Salvador, L. Barrios, A. Meana & M. Higes (2010): Short communication. The detection of Israeli Acute Paralysis virus (IAPV), fipronil and imidacloprid in professional apiaries are not related with massive honey bee colony loss in Spain. Spanish Journal of Agricultural Research 8: 658-661
Genersch, E. (2010): Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology 87:87–97 Genersch, E., W. von der Ohe, H. Kaatz, A. Schroeder, Ch. Otten, R. Büchler, S. Berg,
W. Ritter, W. Mühlen, S. Gisder, M. Meixner, G. Liebig & P. Rosenkranz (2010a):
The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie DOI: 10.1051/apido/2010014: 21 pp.
Genersch, E., J. D. Evans & I. Fries (2010b): Honey bee disease overview. Journal of Invertebrate Pathology 103: S2–S4
Johnson, R.M., J.D. Evans, G.E. Robinson & M.R. Berenbaum (2009): Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). PNAS 106: 14790–14795
Neumann, P. & N.L. Carreck (2010): Honey bee colony losses. Journal of Apicultural Research 49: 1-6
Potts, S.G., S.P.M. Roberts, R. Dean, G. Marris, M.A. Brown, R. Jones, P. Neumann & J. Settele (2010): Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research 49: 15-22
Ratnieks, F.L.W. & N.L. Carreck (2010): Clarity on Honey Bee Collapse? Science 327: 151-152
Van Engelsdorp, D. & M.D. Meixner (2009): A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology 103: S80–S95
Various Authors (2010a): Colony Losses. Special Issue of the Journal of Apicultural Research 49: 1-139
Various Authors (2010b): Bee Diseases. Supplement Volume of the Journal of Invertebrate Pathology 103: S1-S132
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