HEAVY COLONY LOSSES & THE EUROPEAN HONEYBEE (APIS MELLIFERA)

COMPLEX SYNERGISITC RELATIONSHIPS BETWEEN BIOTIC AND ABIOTC FACTORS

Background 100000 1000000

Since 2006, consistently high rates of colony mortality within managed populations of European 100000
10000
honeybees (Apis mellifera) have been observed throughout the world. Historical large scale losses have
10000
occurred but were typically localised within countries and had a limited duration and identifiable cause

Concentration (ppb)

Concentration (ppb)
1000

[1][2]. Prior to 2006, losses of ~15% per year were expected and attributable to a variety of known 1000

factors. These losses are considered manageable, with beekeepers alleviating losses by splitting colonies 100
100
and purchasing queens. 2006 saw the advent of Colony Collapse Disorder (CCD), symptomized by a rapid
10
departure of adult bees from a colony with the hive remaining seemingly undamaged [3]. A definitive 10

cause is yet to be identified, hence the nickname Mary Celeste Syndrome [4]. Cases of CCD have since 1 1
declined, in the U.S. CCD accounted for 60% of colony loss in 2008, and 31.1% in 2013, in initial reports Mean Max Mean Max Mean Max Mean Max
Wax (ppb)
Mean
Pollen (ppb)
Max Mean
Bee (ppb)
Max

Wax (ppb) Pollen (ppb) Bee (ppb)

0.1
for 2014-2015 losses, CCD is not mentioned [5]. Yet the rates of colony mortality have remained high in LD50
LD50

the U.S. (figure 1) and EU (figure 2) with U.S. winter losses alone averaging 28.7% (2007-2015) [6]. Cases Figure 3: Organophosphate coumaphos concentrations found in Figure 4: Systemic neonicotinoid thiacloprid concentrations found
of colony collapse as a result of parasites particularly Varroa destructor, pathogens namely Nosema 259 wax, 350 pollen and 140 bee samples (% with detections wax in 208 wax, 350 pollen and 140 bee samples (% with detections
98.1, pollen 75.4 ,bee 60) (95% (ppb) wax 11555, wax 1.9, pollen 5.4, bee 0) (95% (ppb) wax 0,
ceranae and disease have become prevalent, highlighting the potential compromisation of A. melliferas pollen 730, bee 135) [8]. pollen 5, bee 0) [8].
immune defence system [7]. Complex synergistic relationships between biotic and abiotic stressors are 1000000
10000
hypothesised as the reason for the increased susceptibility and high mortality rates (categorised in Table
1). CCD seems to be an indicator of a much larger problem colony health. 100000
1000
10000

Aim

Concentration (ppb)
Concentration (ppb)
100 1000
To examine if there is a synergistic relationship between the most common causes of colony collapse,
Varroa Destructor and Nosema ceranae, and agrochemicals and miticides found in hives. 100

Methodology 10
10
Primary literature containing information and data relating to declines in Apis mellifera, was sourced and
amalgamated using scientific journal databases such as; ScienceDirect, Web of Science, JSTOR and PLos 1 1
Mean Max Mean Max Mean Max Mean Max Mean Max Mean Max
ONE. Specific search terms used to find academic papers included; Cause of CCD, Effects of CCD, Wax (ppb) Pollen (ppb) Bee (ppb) Wax (ppb) Pollen (ppb) Bee (ppb)

Interactions between pesticides and parasites, IAPV, Nosema etc. Additionally papers by Dennis 0.1 LD50
LD50

vanEnglesdorp, Jeffery Pettis and Elinor Lichtenberg, among others were sought out due to their
Figure 5: Insecticide fipronil concentrations found in 208 wax, 350 Figure 6: Synthetic pyrethroid fluvalinate concentrations found in
involvement with the EPAs taskforce on pollinator decline. pollen, 140 bee samples (% with detections wax 1.4, pollen 0.3, 259 wax, 350 pollen and 140 bee samples (% with detections 98.1
The journal article High Levels of Miticides and Agrochemicals in North American Apiaries: Implications bee 1.4) (95% (ppb) wax 0, pollen 0, bee 0) [8]. wax, 88.3 pollen, 83.6% bee) (95% (ppb) wax 28503, pollen 294,
bee 1623) [8].
for Honey Bee Health provided data regarding concentrations of pesticides found on pollen, wax and
bees within a wide sample of colonies. The article also provided the LD50 for each pesticide, the lethal 100
90
dose at which a 50% mortality rate is achieved [8]. Additionally the report Pesticide exposure in honey
80
CUMULATIVE MORTALITY (%)
bees results in increased levels of the gut pathogen Nosema provided data relating to the interactions
70
between pesticides and pathogens [9].
60
50
50 40
30
45
20
40 10
35 0
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
30 TIME (DAYS)
Total Loss (%)

Control Thiacloprid Fipronil N. ceranae N. ceranae/Thiacloprid N. ceranae/Fipronil

25
Figure 7: Effect of Nosema ceranae infection on honeybee sensitivity to insecticides showing a synergistic relationship. Red line indicates
time of exposure to insecticides [9].
20

15 Results
10 H0 : There is no synergistic relationship between N. ceranae and pesticides within Apis
5 mellifera, leading to no increase in mortality rates.
Ha: There is a synergistic relationship between N. ceranae and pesticides within Apis
0
2006-2007 2007-2008 2008-2009 2009-2010 2010-2011 2011-2012 2012-2013 2013-2014 2014-2015 2015-2016 mellifera, leading to increased mortality rates.
Acceptable Winter Loss Total Winter Loss Total Annual Loss Linear (Total Winter Loss) Linear (Total Annual Loss)
Data shows that the cumulative mortality of samples infected with N. ceranae is highly
Figure 1: Total US managed honey bee colony loss estimates [10] (survey data) showing that winter losses (typically associated with CCD) are declining, annual
losses are increasing (Varroa destructor and Nosema ceranae losses typically occur in the summer swarming phase) indicating that the main cause of colony significant (p=<0.05) compared to the control sample (t=1.71 p=0.007). Cumulative
mortality has shifted. mortality of the control compared to samples treated with sublethal levels of
insecticides were found to be insignificant, p=>0.05 (Thiacloprid t=1.6, p=0.39), (Fipronil
t=1.6 p=0.34). Samples infected with N. ceranae and then exposed to sublethal doses of
pesticides were significant compared to the control, (N. ceranae/Thiacloprid: t=1.7,
p=0.001) (N. ceranae/Fipronil: t=1.7, p=0.002).
Colonies subjected to both N. ceranae and pesticides had a higher cumulative mortality
than those infected with just N. ceranae, indicating a synergistic relationship (fig. 7).
Data from N. ceranae/Thiacloprid compared to N. ceranae tested close to the margin of
statistical significance (t=1.7, p=0.06). Comparisons between the N. ceranae/Fipronil
and N. ceranae infected samples, indicated a significant (p=<0.05) relationship (t=1.7,
p= 0.04) thus we can accept Ha.

Discussion
Fluvalinate (fig. 4) and coumaphos (fig.3) are both chemicals used in the treatment of
Varroa, and thus were expected to be found in high concentration. However levels
exceeding the LD50 suggest they are being overused. Both these Miticides have been
shown to exhibit clear non lethal effects including altering the growth and behavioural
characteristics of the queen bee [12]. Although contamination by systemics thiacloprid
Figure 2: Map of reported colony mortality (%) using data generated by COLOSS, obtained by and fipronil was not widespread their sub lethal effects in relation to N. ceranae were
surveys sent to beekeepers. In red 2006-2007 losses, in black 2007-2008 [11] clearly demonstrated (fig. 7). It is likely that other agrochemicals have a similar effect in
weakening the bees resistance to pathogens. And this has led, or at least part led, to the
Table 1: Driving forces of honeybee population instabilities increase in colony mortality in the summer months.
Habitat degradation Agrochemicals Conclusion
Pathogens Parasites Although much of the data regarding numbers of colonies is sporadic and only began in
Invasive species Genetic homogeneity 2006, there are clear trends indicating an increase in mortality (fig. 1 + 2). The scientific
Pollution Malnutrition consensus is that stressors are interacting in a variety of ways to impact colony health.
Agricultural practices Climate change TED talk: A plea for bees. By leading
scientist Dr. Dennis vanEnglesdorp
Thereby causing a reduction in Apis melliferas ability to combat parasitic, pathogenic
and viral threats. With high losses comes increased cost for beekeepers, and many have
References become unable to sustain their operations. If we cannot prevent these losses or
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[2] vanEngelsdorp, D., & Meixner, M. D. (2010). 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, 80-95.
[3] vanEngelsdorp D, E. J. (2009). Colony Collapse Disorder: A Descriptive Study. Pennsylvania: PLoS ONE.
alleviate the costs associated with them, then the profession will likely die out. whilst
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humanity will likely be able to adapt to the changes associated with a loss in pollination,
Wasps are
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protection/colony-collapse-disorder
[6] Steinhauer, N., Rennich, K., Wilson, M., Caron, D., Lengerich, E., Pettis, J., & Vanengelsdorp, D. (2014). A national survey of managed honey bee 20122013 annual colony losses
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[7] Evans, J. D., Aronstein, K., Chen, Y. P., Hetru, C., Imler, J. L., Jiang, H., . . . Hultmark, D. (2006, October). Immune pathways and defence mechanisms in honey bees Apis mellifera.
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[8]Mullin, C. A., Frazier, M., Frazier, J. L., Ashcraft, S., & Simonds, R. (2010). High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee
Pollinators are canaries in the coal mine, and their disappearance is a referendum on
better
Health. PLoS ONE.
[9] Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Vigus, B., & Brunet, J.-L. (2011). Exposure to Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of
Honeybees Previously Infected by Nosema ceranae. Tulane: PLoS ONE.
[10]Steinhauer, N., Rennich, K., Caron, D. M., Delaplane, K., Rangel, J., Rose, R., . . . vanEngelsdorp, D. (2016). Colony Loss 2015-2016: Preliminary Results. USDA NIFA.
the state of our environment, a reminder of the brilliant and frightening
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Journal Economic Entomology , 28-36.
interdependence of our ecosystem. Dr. Dennis vanEnglesdorp [13].
[13] vanEnglesdorp, D. (2008, December). A plea for bees: transcript. Retrieved from TED.