The European Honeybee, Apis mellifera, is important economically not just for honey production but also as a pollinator. A recent DEFRAreport puts honey valuation at between £10-30 million yearly whilst the pollination of agricultural crops is worth around £200m per anum. As such an economically important species it is unsurprising that the recent decline in honeybee numbers has led to serious concern.
Honeybee populations are declining in some areas including the UK. Honeybee numbers decreased by 25% in central Europe between 1985 and 2005 (Potts et al, 2010). A range of interacting factors are thought to be involved including; bad weather, loss of forage, pesticide use, disease and parasitism (Oldroyd, 2007). In the USA the causes behind the dramatic losses of bee colonies, now named Colony Collapse Disorder, are still under investigation. In the winter of 2006-7 it was estimated that 23% of US beekeepers suffered losses of up to 45% of their hives (Cox Foster et al, 2007). In the UK overwinter losses have been attributed to the influence of disease including several viruses, and the ectoparasitic mite Varroa destructor that vectors and ‘activates’ the viruses (Highfield et al, 2009).
It is known that pathogens can have an effect on host behaviour (eg. Roy et al, 2006). Some influence their hosts to increase their own fitness. For example Schistocephalus solidus, a tape worm that infects sticklebacks, causes changes to its intermediate host’s behaviour that make the host more likely to be eaten by birds; the final host for this specie (Barber et al 2005). Other behavioural changes are seen as the host tries to combat infection. Behaviouralfeverin invertebrates for example; used to slow the onset of disease (Roy et al, 2005). Finally some changes may occur as resources are taken up by the pathogen directly or used preferentially by the immune system. It has been shown that the activation of the honeybee immune system causes decreases in learning ability (Mallon et al 2003).
I will examine the effect of several coevolved and non-coevolved pathogens on honeybee learning and foraging behaviour. This will be achieved in the laboratory with proboscis extension reflex conditioning techniques, in flight rooms with flower array studies and in the field by use of the harmonic radar. I will also be utilising molecular techniques to detect the covert viruses many bees carry.
Condistioned Proboscis Extension (CPE):
Proboscis Extension is a reflex action found in many insects, including honeybees. When a bee senses a food source, such as nectar, it will extend its proboscis (or stick out its tongue!) The reflex can be conditioned by use of a similar method to that used by Pavlov when training his dogs to salivate at the sound of a bell (Pavlov, 1927).
First I chill the bees to around 5-10'C. This makes them dopey so that they cannot fly away (or sting me!)
The bees are then fixed in small tubes and allowed to warm up again. In the tubes the bees can move their antennae and extend their proboscises but (normally) cannot escape. (Here are some pictures of my CPE experiments.)
Each bee is placed in a stream of air. After several seconds the clean air is replaced by scented air and sucrose solution is touched to the bees antennae. The bee should then extend its proboscis. If it does it receives a reward; a drink of the sugary water.
After doing this several times the bee should associate the scent with the food and extend its proboscis at just the scent. Some bees can do this after being shown only once!
I can use this experiment to determine the bees' learning ability by recording how many 'training trails' it takes before the bees learn the association.
The experiment can also be used to test the bees' memory by training them and then waiting for varying amounts of time before testing to see if they still remember.
This method is also being used by companies, such as Inscentinel, to train bees to recognise scents such as those found in explosives or drugs so that the bees can be used in much the same way as sniffer dogs!
In 2009 I tested the learning ability of bees ages between 1 and 12 days post emergence as adults. All ages of bees were able to learn the CPE response but older bees were found to learn the response better and were more responsive to the sucrose. I used these results to choose the age of bees to use in experiments in 2010.
In 2010 I compared the learning ability of both nurse and forage bees infected with the fungus Metarhizium anisopliae to uninfected controls. The sick bees were no less abel to learn than the healthy ones! Although they were hungrier!
Rothamsted has the only Harmonic Radar in the world. The radar can be used to follow free flying insects in the field. (eg. Reynolds et al, 2009)
A transponder is fixed to the back of the insect to be tracked. (Here are some pictures of the radar experiments.) The harmonic radar emits a signal that interacts with the transponder to produce a signal of twice the frequency originally emitted. It is this signal which is received and tracked. Thus the radar follows only signals from the transponder and not signals reflected from hedges, walls or other solid objects.
For some reason the occasional combine harvester also shows up! Luckily bees and combine harvesters are easily distinguished!
The summer of 2009 was spent releasing bees into new foraging areas to see how they would explore. This was part of a larger Syngenta project to model honeybee behaviour. I was interested in the difference between sick and healthy bees. So we set up three colonies heavily infested with varroa and the viruses they transmit and three colonies with lower varroa levels who should thus be healthier, and compared bees from each.
Scarily this is my final year so I am currently trying to get everything analysed and written up.
Barber, I., Walker, P., & Svensson, P.A. (2004) "Behavioural responses to simulated avian predation in female three spined sticklebacks: The effect of experimental Schistocephalus solidus infection." Behaviour. 141: 1425-1440.
Cox-Foster, D. L., S. Conlan, et al. (2007) "A metagenomic survey of microbes in honey bee colony collapse disorder." Science. 318: 283-287.
Highfield, A. C., El-Nagar, A., et al. (2009) "Deformed wing virus implicated in overwintering honeybee colony losses." Applied and Environmental Biology. 75 (22): 7212-7220.
Mallon, E. B., Brockmann, A., et al. (2003) "Immune response inhibits associative learning in insects." Proceedings of the Royal Society of London Series B-Biological Sciences. 270(1532): 2471-2473.
Oldroyd, B. P. (2007) "What's killing American honey bees?" PLoS Biol. 5, e168.
Pavlov, I. P. (1927) "Conditioned reflexes." Routledge and Kegan Paul, London.
Potts, S. G., Roberts, S. P. M., et al. (2010) "Declines of managed honey bees and beekeepers in Europe." Journal of apicultural research. 49 (1): 15-22.
Reynolds, A. M., Swain, J. L., et al. (2009) "Honeybees use a Levy flight search strategy and odour-mediated anemotaxis to relocate food sources." Behavioral Ecology and Sociobiology. 64, 115-123.
Roy, H. E., D. C. Steinkraus, et al. (2006) "Bizarre interactions and endgames: Entomopathogenic fungi and their arthropod hosts." Annual Review of Entomology. 51: 331-357
Other useful references:
Aizen, M. A., Harder, L. D. (2009) "The GlobalStock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination." Current Biology. 19, 915-918.
Van Engelsdorp, D., Hayes, J, Jr., et al (2010) "A survey of honey bee colony losses in the United States, fall 2008 to spring 2009." Journal of apicultural research. 49 (1): 7-14
Behrends, A., Scheiner, R. (2009) "Evidence for associative learning in newly emerged honey bees (Apis mellifera)." Animal Cognition. 12, 249-255.
Abramson, C. I., Sanderson, C., et al. (2005) "Development of an ethanol model using social insects: V. Honeybee foraging decisions under the influence of alcohol." Alcohol. 36, 187-193.
Osborne, J. L., Clark, S. J., et al. (1999) "A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar." Journal of Applied Ecology. 36, 519-533.
Reynolds, A. M., Smith, A. D., et al(2007) "Honeybees perform optimalscale-free searching flights when attempting to locate a food source." Journal of Experimental Biology. 210, 3763-3770.