(November 29th, 2010) Over the last decade, beekeepers, scientists, environmentalists and politicians have been lamenting the alarming unexplained decline in honey bee populations in Europe and North America. Jeremy Garwood reports on the scientific battle to save the bees … if only we could finally agree on what’s actually killing them!
In Europe and North America, there has been a steady decline in the number of honey bee (Apis mellifera) colonies during the last half century. This is largely due to pesticides and pests. Colony numbers in Europe decreased from over 21 million hives in 1970 to about 15 million in 2007. In the US, the number of honey-producing colonies dropped from a 1947 high of 5.9 million hives to 2.3 million in 2008.
Bee numbers and decline – Bees in crisis
Up until 1980, most US honey bee losses were attributed to the combined toxicity of pesticides (e.g. organochlorine and organophosphorus), then came dramatic losses due to the parasitic bee mites, Acarapis woodi (in 1984) and Varroa destructor (in 1987). However, during the winter of 2006-07, many US beekeepers opened their hives to discover a new phenomenon – the adult bees had quite simply disappeared from the hive, abandoning their food and brood (young bees). US beekeepers reported losing 38% of their bee colonies. Unable to explain what was happening, scientists called it “Colony Collapse Disorder” (CCD). And, in the absence of a clear explanation or cure for CCD, huge losses have continued – 36% during winter 2007-08, 29% in 2008-09 and another 33% last winter.
Since 1990, European beekeepers have also been experiencing sudden failures of honey bee colonies that retrospectively display characteristics similar to CCD. But losses have attained alarming proportions from 2007 to 2008, estimated at 29% in France, up to 40% in Italy, 33% in Denmark, 33% in the UK and even 89% in parts of Spain!
Beekeepers can continue to replace hives and found new bee colonies but it’s costly. So how long can such losses continue before apicultures give up? In 2009, Apimondia, the international beekeeping organisation, warned that the entire European beekeeping industry could disappear in less than ten years!
Disappearing bees, Colony Collapse Disorder and national frontiers
Researchers around the world have been trying to work out what’s killing the bee colonies. In general, CCD is characterised by the rapid loss from a colony of its adult bee population. No dead adult bees are found inside or in close proximity to the colony. At the final stages of collapse, a queen is only attended by a few newly emerged adult bees. These collapsed colonies often have considerable capped brood and food reserves. But in the absence of large numbers of dead bees, analysis of the causes of CCD has proved difficult.
Many factors have been proposed including viruses, bacteria, fungi, parasitic mites, chemical toxins, electromagnetic radiation from mobile phones, genetically modified crop plants, poor nutrition and the general stress of modern bee life. Certain Americans have even suggested a mass bee kidnapping by UFOs. However, one surprising feature of the scientific explanations for global bee deaths is that they tend to follow national boundaries.
Spanish bees and fungi
Between 2003 and 2004, 40% of the bee colonies in Spain died associated with a syndrome of depopulation. Spanish researchers favoured an exploration of likely pathogens because the bee losses occurred throughout Spain, irrespective of the plant cultures and pesticide treatments used. They observed that the quasi-totality of the thousands of samples they obtained were positive for the microsporidium fungus, Nosema. Infections with Nosema apis are known to be correlated with reduced lifespan of individual bees, reduced performance of colonies and increased winter mortality. Ingested Nosema spores germinate in the bees’ ventriculus, causing damage to gut epithelial cells. However, the affected bees did not show the classic symptoms. In 2006, scientists identified a highly virulent form of Nosema cerranae, an Asian species previously unknown in Europe. This pathogen is now considered the principal cause of Spanish bee woes (‘Honeybee colony collapse due to Nosema cerranae in professional apiaries’, M. Higes et al., Envir. Microb. Rep. 1: 110-13). However, other countries have not found the same level of virulence and the occurrence of Nosema cerranae is not inevitably accompanied by the symptoms described by Higes, leading to the suggestion that this might be a regional problem, rather than a global phenomenon.
Belgium bees fight mites
Belgian scientists have concluded that the mortality of their bee colonies is due to the parasitic mite, Varroa destructor. This mite is already recognised as the most detrimental honey bee parasite in the world – beekeepers regularly treat their hives with anti-mite chemicals. Originally a parasite of the Asian bee, Apis cerana, the Varroa mite has spread over 30 years to infest honey bee colonies worldwide – more than 99% of domestic bees in Europe have been potentially infested by the mites. The female mites feed on adult bees but depend on bee brood for reproduction. They feed on the bee’s hemolymph, causing nutritional deficits in the developing bee.
German bees go virally
German researchers have also identified Varroa as their major bee parasite but think an additional problem is that mites are vectors for viral transmission – they infect the bees with bee pathogenic viruses, like ‘acute bee paralysis virus’ (ABPV) and ‘deformed wing virus’ (DWV). A four-year study by the German Bee Monitoring Programme found a significant correlation between colony winter mortality, autumn mite infestation rates, and the loads of both ABPV and DWV.
However, in Germany, they have also noted a weakening over several decades of the bees’ immune defences that render them more susceptible to viral and bacterial infections. In the early 1980s, bee colonies could harbour several thousand mites without dramatic symptoms but now, an autumn infestation rate of 10%, corresponding to 1,000 mites in a colony of 10,000 bees, is considered a critical threshold for the colony’s winter survival (Elke Genersch et al., Appl. Microbiol. Biotechnol. 87: 87-97).
Bacteria beat up British and Swiss bees
In 2007, researchers in Switzerland and the UK reported a dramatic increase in the presence of the bacterial infection, European foulbrood. This is a pathogenic disease caused by the gram-positive bacterium, Melissococcus plutonius. Normally, it is only pathogenic for honey bee larvae not adults, so it seems unlikely to explain CCD. Indeed, European foulbrood hasn’t been considered much of a problem in apiculture since many infected and diseased colonies spontaneously recover from it. But since 2002, this situation seems to have changed in the UK and Switzerland where the infection and re-infection rates have been dramatically increasing.
US forensic science accuses a novel virus
In the US, researchers took a forensic approach to CCD which is causing alarm, with 30 to 90% loss during the winter of 2006 to 2007. The worker bees had disappeared from the hive without trace. Everyone in the apicultural sector was affected – professional and amateur beekeepers, sedentary or migratory, as well as those who avoided chemical treatments by practising bioorganic beekeeping. An inquest could not show any temporal correlation with the utilisation of pesticides.
Diana Cox-Foster at Pennsylvania State University conducted an experiment, transferring healthy colonies into the hives affected by CCD. She found that healthy colonies could only be maintained if the hives had been irradiated first. This led to a hunt for a possible microbial agent using a meta-genomic approach (Science, 2007). The total RNA present in the affected bees was extracted and sequenced in order to identify the totality of biological agents present. Bacteria, fungi and parasites were identified from their ribosomal RNAs; 7 RNA viruses were also identified. Upon comparing CCD RNA samples with healthy colonies, only the presence of a single virus, the Israeli acute paralysis virus (IAPV), appeared to be correlated with CCD. However, this observation did not indicate if the virus was the causal agent or simply a marker of the syndrome. Furthermore, the IAPV symptoms first observed in Israel in 2004 – paralysis, trembling, presence of dead bees around the hive – are not those observed with the American CCD. IAPV has since been detected in bee samples that predate CCD and its role in CCD is now considered to be secondary (vanEngelsdorp, PLoS ONE, 2009).
France and the pesticide polemic
In France, a mysterious disease that decimated bee hives was first reported in 1994. The affected bees had been foraging on sunflowers treated with a new insecticide, ‘Gaucho’ whose active ingredient is imidacloprid, a neonicotinoid that causes insect paralysis and death by activating the postsynaptic nicotinic acetylcholine receptor.
However, Gaucho is not sprayed on growing plants; it is coated on the seeds. As a systemic pesticide, it is absorbed from the seed coating by the germinating plants and remains in the growing plant tissues, providing pest protection throughout the entire growing season. But then, reasoned French beekeepers, if this insecticide can remain active in the plant that long, isn’t it also present in the flower parts visited by the bees, and in the nectar and pollen they feed on?
And so began a long dispute about the toxicity of such pesticides for bees and the need to curtail their use. Politicians have been lobbied by beekeepers, environmental groups and scientists, who have argued for a ban on the use of certain insecticides and the need for further research to clarify the mechanism(s) causing the large-scale death of French bees. Meanwhile, the agrochemical companies that manufacture imidacloprid (Bayer AG), and two other neonicotinoids, clothianidin (again Bayer AG) and thiamethoxam (Syngenta AG) have consistently denied or minimised the possibility that their products are causing bee deaths.
In 1997, heavy bee losses were again observed, prompting an official study into the causes. Although initial research did not find a clear link to imidacloprid, the insecticide’s use on sunflower seeds was officially suspended as a precautionary measure from 1999-2003. Overall, French honey production fell from 110,000 tonnes in 1996 to 50,000 in 1999.
Bayer’s researchers claimed that imidacloprid had no effects on bee health below a concentration of 20 parts per billion (ppb) and that its concentration in the leaves was below 1.5 ppb. They also eventually admitted it was present in the nectar and pollen but that, at such small concentrations, it posed no threat to bees.
In 2001, Luc Belezunces, a bee researcher at INRA (the French agricultural research institute) in Avignon published “Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera” (in Environmental Toxicology and Chemistry). He found that the acute lethal dose of imidacloprid was only 4-40 ng per bee, much less than most other insecticides. However, his big discovery was that the lethal dose from chronic exposure to imidacloprid was 4,000 times less, “Ingesting 1 pg a day was enough to kill a bee within 10 days”, he told INRA magazine (June 2009). “Moreover, imidacloprid degrades into 6 metabolites, some of which are even more toxic.” He said that the capacity to measure very small traces of imidacloprid in pollen now shows that the concentration is in the range of microgrammes per kg of pollen and that this constitutes a risk for bees. “These results shifted classical conceptions and our first publication in 2001, initially commissioned by the Bayer company, was not well received.”
Despite a four-year suspension of imidacloprid use on sunflower seeds, French bee deaths continued. Bayer claimed this was proof that imidacloprid was innocent but beekeepers pointed out that imidacloprid was still being used to treat maize seeds. They also implicated another pesticide, fipronil, which had been used as a substitute for imidacloprid. Fipronil (manufactured by BASF) is a phenylpyrazol that binds GABA receptors, blocking passage of chloride ions causing hyperexcitation of nerves and muscles. The use of fipronil for crop protection was suspended in France in 2003. The restriction on imidacloprid is maintained.
“Bee Mortality and Bee Surveillance in Europe” – What’s really happening?
Faced with such conflicting research reports, no-one seemed capable of providing a clear explanation of bee colony destruction. A big rethink was needed. In 2008, the European Food Safety Authority called for a systematic, Europe-wide analysis of the existing bee surveillance systems, the known data and all scientific publications related to honey bee colony mortality. Coordinated by the French agency for food security (AFSSA), a consortium of seven European bee research institutes presented their findings in 2009 (http://www.efsa.europa.eu/en/scdocs/scdoc/27e.htm).
They found that most of the surveillance systems in the 24 European countries investigated were inadequately poor with a lack of representative data for colony losses at both the country and EU levels and little standardisation of data, “Concerning surveillance procedures and protocols, of the 18 systems stating that they have in place active surveillance procedures, only 6 can be considered as valid active systems able to produce representative figures of the true colony loss situation for the countries in question.”
Moreover, the only commonly used indicator was the “global colony loss rate” during the over-wintering period, which meant that not all aspects of colony losses, for example, during the summer, could be addressed. Although temporal and geographical analyses indicated an important variability in colony losses, “such trends are difficult to interpret considering the wide variation in the quality of the systems that produce these data.”
Based on such dodgy data, it’s perhaps not so surprising to learn that they also found the existing scientific literature to be confusing, “There are many inconsistencies in the ways in which ‘colony losses’ are defined. Up to 17 different definitions for CCD exist in the literature (!). This means that reports may not always be referring to the same phenomenon and this creates confusion when trying to explain the origin of what has been identified in the field. The described pathology is varied, with authors using the same descriptions for different sets of circumstances.”
Some researchers even have strong doubts that anyone can make a valid assessment of colony loss after it’s occurred. In their ‘Historical review of managed honey bee populations in Europe and the United States and the factors that may affect them’ (J. Invert. Pathology 103, Suppl. 1: S80-95), Dennis vanEngelsdorp (Pennsylvania State University) and Doris Meixner (Bieneninstitut, Hessen, Germany) state, “With few exceptions, it is nearly impossible to determine the cause of a honey bee colony death after the fact. If a colony dies during winter, a considerable amount of time may pass before it is noticed by the beekeeper and clues to the cause are usually lost. To definitively determine the cause or causes of mortality in colonies, a priori sampling and analysis of a representative portion of colonies is needed.”
Pest versus Pesticides – Possible Research Bias?
Pesticides are big business. For example, in 2007, sales of Bayer CropScience’s imidacloprid and clothianidin were €587 million and €110 million, respectively. Any decision to restrict the agricultural use of these substances represents a considerable loss of commercial revenue. It should come as no surprise, then, to discover that the agrochemical companies are busy trying to convince decision-makers that their products are beneficial.
But could the interests of the pesticide companies be affecting the impartiality of researchers? Bee researchers at the University of Bologna certainly think so.
“Despite the fact that CCD is unanimously considered by scientists to depend on several causes, two camps are now in conflict,” they write in “The puzzle of honey bee losses” (Stefano Maini et al., Bulletin of Insectology 2010, 63:153-60). “On the one side are the environmentalists/beekeepers and on the other pesticide companies and the scientists sponsored by them.”
The Italian researchers explain how they spent years studying the possibility of adopting the honey bee as a bioindicator of environmental pollution in Italy and that their experience suggests that non-scientific factors are influencing the progress of research on honey bee mortality. “We believe that papers published in scientific journals influence politicians and legislators preparing rules regarding prohibition and limitation of pesticide use. Scientific papers that indicate no hazard of pesticides and refuse to discuss data offering contrary opinions on the effect of pesticides on honey bees and other beneficial insects may cause an underestimation of the real damages that agrochemicals inflict on ecosystems.”
They do concede, “It is impossible to ‘demonstrate scientifically’ the direct influence that the pesticide corporations, seed companies and some farm lobbies have on research teams that conduct research on honey bees,” but they provide several examples, where other researchers have been surprisingly certain that pesticides could not possibly be involved in CCD.
For example, in a recent article in Science magazine “Clarity on honey bee collapse?” (Science 327: 152-3), Francis Ratnieks and Norman Carreck (from the UK’s University of Sussex) state, “The consensus seems to be that pests and pathogens are the single most important cause of colony losses” and that imidacloprid, implicated in French bee losses, now “seems unlikely” to be responsible for French bee deaths. Maini wrote a letter to Science, objecting that “many other scientists are concerned about the inappropriate use or even misuse of insecticides” and that by stating the “main cause of bee losses are ‘diseases’ ”, Ratnieks and Carreck “may give the false impression that insecticides can be sprayed” without due attention. Furthermore, their conclusion about imidacloprid and French bee mortality “appears to be a biased opinion and a conflict of interest”, given that it relied on a citation by “a researcher employed by the producer of imidacloprid” (Bayer AG) and it had been chosen from a special issue of the Bulletin of Insectology that presented several other articles with different conclusions concerning imidacloprid. Maini’s letter was swiftly rejected by Science without explanation.
But he had also been in recent conflict with Carreck who, as senior editor of the Journal of Apicultural Research, took six months to reject a critical manuscript written in response to a 2009 paper by Belgian researchers, “Does imidacloprid seed-treated maize have an impact on honey bee mortality?” (B. K. Nguyen et al., J. Economic Entomology 102: 616-23). The latter study had concluded that imidacloprid has no negative impact on honey bees, at least in Belgium (where mites are uniquely to blame). Again, Maini et al. pointed out that Nguyen had selectively cited work by Bayer researchers, while simultaneously ignoring numerous scientific publications reporting lethal and sub-lethal effects of pesticides. Furthermore, the methodology of the Belgian study only looked for effects late in the maize-growing season, despite evidence that complex effects had been detected both before and after this period.
Examples of agrochemical influence have come to light elsewhere. For example, in 2009, it was discovered that the British Beekeepers’ Association (BBKA) was receiving money from Bayer CropScience in return for endorsing its products as “bee-friendly”. In October 2009, the UK minister of the Department for Environment, Food and Rural Affairs, told parliament that, although the Government took the drop in bee numbers “very seriously”, adequate measures were already in place to protect bees against harmful sprays, “There is no evidence that authorised pesticides pose an unacceptable risk.”
However, it has been shown that where UK publicly-funded bee research projects have been co-financed by pesticide companies, there has been a clear tendency to avoid looking at possible pesticide effects. For example, Syngenta, manufacturers of the neonicotinoid pesticide, thiamexotham, contributed 10% towards a £1 million study at Warwick University to investigate the “parasitic diseases caused by the varroa mite” and the “link between these diseases and the quality of pollen and nectar that the bees are feeding on”. When asked by the Guardian newspaper, researcher David Chandler confirmed that this study will not look at any role that pesticides might play in affecting the quality of bee food or the bee’s resistance to these parasitic diseases. Furthermore, Warwick University has started to promote Syngenta, describing the company as helping to “protect the environment and improve health and quality of life”.
Acute pesticide poisoning in Germany
Insecticides are used to kill, well, insects, so surely they can also kill bees? A recent reminder that pesticides aren’t inoffensive came in SW Germany in 2008, when 11,000 honey bee colonies (around 400 million bees) died due to acute poisoning by another Bayer neonicotinoid insecticide, clothianidin. Germany immediately suspended use of eight neonicotinoid pesticide seed treatment products for oilseed rape and maize. The group, Coalition against Bayer Dangers, brought a legal case against Bayer's Chairman for marketing dangerous pesticides that are causing the death of bees worldwide. "We're suspecting that Bayer submitted flawed studies to play down the risks of pesticide residues in treated plants," said the coalition's lawyer. In its defense, Bayer CropScience blamed defective seed corn batches. They argued that their insecticide was not at fault if used correctly but that in this case it had been incorrectly glued onto maize seeds such that the coating came off as the seeds were sown. The problem was exacerbated by the use of pneumatic sowing machines which generated toxic dust clouds that drifted across the surrounding fields containing flowering plants in bloom, such as fruit trees and dandelions that the bees were feeding on. Yes, the bees were directly poisoned by clothianidin but it should never have been there if Bayer’s handling procedures had been respected.
Unimpressed, Slovenia and Italy soon followed Germany’s lead and banned sales of clothianidin and imidacloprid.
Pesticides accumulate in US hives
Maryann Frazier (Penn State University) decided to take a closer look at the exposure of US bees to pesticide residues (Am. Bee J. 148: 521-3). She found 121 different pesticides and metabolites in 887 wax, pollen, bee and associated hive samples from migratory and stationary beekeepers. These included 16 parent pyrethroids, 13 organophosphates, 4 carbamates, 4 neonicotinoids, 4 insect growth regulators, 3 chlorinated cyclodienes, 3 organochlorines, one formamidine, 8 miscellaneous miticides/insecticides, 2 synergists, 30 fungicides and 17 herbicides. Over 40 pesticides were systemic. There was an average of 6 pesticides per sample. Only one wax sample, 3 pollen samples and 12 bee samples had no detectable pesticides. Overall, pyrethroids and organophosphates dominated total wax and bee residues, followed by fungicides, systemics, carbamates and herbicides, whereas fungicides prevailed in pollen followed by organophosphates, systemics, pyrethroids, carbamates and herbicides. Quite a chemical cocktail!
In 2008, Frazier told the US Congress hearing into the plight of the honey bee, “We are becoming increasingly concerned that pesticides may affect bees at sub-lethal levels, not killing them outright, but rather impairing their behaviors and their abilities to fight off infections.”
Bee genomic insights
The honey bee consortium published the honey bee genome in 2006 (Nature 443: 931-49), announcing some interesting specificities. For a start, “Given the predicted disease pressures in honeybee colonies, the honeybee genome encodes fewer proteins implicated in insect immune pathways when compared to other insect genomes,” suggesting that the bee’s immune system might be more vulnerable to extrinsic factors than other insects.
There have been reports that honey bees are having less success in resisting microbial infections and mite infestations but why are the bee’s immune defenses weakening? A recent study by Yves Le Conte (INRA Avignon) suggests that pesticide exposure can interact with pathogens to harm honey bee health (“Interactions between Nosema microspores and a neonicotinoid weaken honeybees,” Environ. Microbiol. 12: 774-82). Bees treated with imidacloprid while being fed Nosema spores had highest individual mortality rates than those exposed to imidacloprid or Nosema alone. The activity of glucose oxidase, enabling bees to sterilise colony and brood food, was significantly decreased only by the combination of both factors compared with control, Nosema or imidacloprid groups, suggesting a synergistic interaction. “In the long term this could lead to a higher susceptibility of the colony to pathogens.”
Honey bees also have a smaller genetic repertoire for safely metabolising pesticides. “Contact pesticides affect the worker bees whereas residual pesticides accumulate in lipophilic substances, such as wax or pollen lipids, and impact on the developing brood and queen fecundity.” It seems that the size of the major detoxifying gene families is smaller in the honey bee, making it “unusually sensitive to certain pesticides”. Compared with Anopheles and Drosophila, the honeybee has 30–50% fewer genes encoding the carboxylesterase, cytochrome P450 and glutathione S-transferase enzymes that are principally responsible for the metabolism of pesticides. These are the genes where the great majority of metabolic resistance mutations have been found in other species of invertebrates. So, the bees may well take longer to recover from pesticide exposure than the targeted insect pests!
Bees may also be particularly sensitive to the neonicotinoid insecticides. The honey bee possesses 11 nicotinic acetylcholine receptor subunits (the target of this class of insecticide) one more than either the mosquito or the fruit fly (Andrew K. Jones et al., Genome Research 16: 1422-30). Once again, the question is posed – are all insects equally sensitive to pesticides?
Sub-lethal effects are possible
The dispute over the role of pesticides in bee colony loss is increasingly focused on possible ‘sub-lethal’ effects that do not directly kill the bees but instead disrupt their highly organised social and foraging behaviour, contributing to a collapse of the colony’s cohesion.
In CCD, adult bees disappear from the hive – what if the bees got lost while out foraging and simply couldn’t find their way home? Perhaps their ability to find acceptable food was impaired and they died of exhaustion, unable to return until their mission was accomplished? As usual, interpreting animal behaviour can become quite anthropomorphic; however, researchers have been developing quantifiable bee behavioural tests in order to assess the impact of various substances, including pesticides, at sub-lethal concentrations.
This research has already shown that bees have similarities to humans – they both get drunk on ethanol! And we all know that alcohol intoxication can cause behavioural lapses, impairing motor functioning, learning and memory processing. Might bees also be getting “drunk” on pesticides?
Under current legislation, in order to obtain authorisation for marketing and use of their pesticides, manufacturers are only required to determine the lethal effects of their products on pests and other creatures that might be affected. Hence, despite studies that may document sub-lethal pesticide effects on the targeted ‘natural enemies’, only mortality tests are considered when making a choice between several pesticides in an integrated pest management context.
Yet, in contrast to the easily observable direct poisoning of bees (i.e. they drop dead), sub-lethal effects are much more difficult to demonstrate. They may only become apparent after prolonged exposure and affect various life stages. And what is affected? The cell physiology or immune system of individual bees or social organisation with consequences for the colony as a whole, such as learning, behaviour and communication?
The possibility that bees are experiencing sub-lethal behavioural perturbation due to certain neurotoxic insecticides has been tested. For example, imidacloprid, fipronil and deltamethrin (a very popular pyrethroid insecticide no longer patent-protected) have been shown to affect the bees’ ability to detect food and to accurately return to the hive after foraging.
Inhibition of foraging
If the ability to detect food is compromised, an effect on foraging may occur. When landing on a flower, each forager bee is subjected to a conditioning process, where floral cues (smell, colour, shape) are memorised after being associated with a food reward (nectar and pollen). Under laboratory conditions, olfactory learning can be studied using a bioassay based on the conditioning of the proboscis extension reflex (PER) applied to restrained individual bees. By stimulating the antennae with a sucrose solution, the bee extends its proboscis for feeding. This can be used to assess the ‘gustatory threshold to sugary foods’ – the lowest sugar concentration capable of eliciting a PER. But the application of some pesticides, e.g. fipronil at a dose of one ng per bee, strongly reduces bee sensitivity for low-sucrose concentrations, suggesting that pesticide exposure could effectively reduce the capacity of honey bees to detect food sources (A. K. El Hassani et al., Pharmacol. Biochem. Behav. 82: 30-39).
Tunnels, mazes and food direction
Honey bees use visual landmarks to navigate to a food source as well as to accurately communicate to their hive mates the distance and flying directions for reaching it. A bee exposed to pesticide during a foraging trip may incorrectly acquire or integrate visual patterns, causing disorientation and loss. Aside from impairing the orientation behaviour of exposed foragers, insecticides could affect the accuracy of information relayed through the dances of the returning foragers.
For example, to study the effects of deltamethrin, honey bees were trained to forage on an artificial feeder filled with sucrose solution and were then individually marked with coloured number tags. In an insect-proof tunnel with the feeder located eight metres from the hive, deltamethrin altered the homing flight in foragers treated topically with sub-lethal doses. Treated bees flew towards the sun light and took significantly longer to fly back to the hive. This disorientation was attributed to an effect on the storage or retrieval of spatial information (R. Vandame et al., Environ. Toxicol. Chem. 14: 855-60).
In 1998, Marc Colin’s team at INRA-Avignon also observed effects of low ppb concentrations of imidacloprid on honey bees, finding short-term errors in the bees’ flight plans and that, after a few days, exposed bees stopped feeding altogether – their numbers soon dropped sharply compared to the control groups.
Another approach intended to simulate learning of complex routes under field conditions measures the orientation performance of bees in a complex maze. This relies on associative learning to fly through a maze according to the presence or absence of a visual cue with the reward of sugar solution at the end. Using this experimental set-up, researchers found that foragers receiving one ppb fipronil performed less well than those in control groups. In parallel, the percentage of bees that did not find the goal within five minutes of entering the maze increased dramatically when exposed to fipronil (34% and 4% in exposed and control groups, respectively) (Axel Decourtye et al., Julius-Kühn-Archiv 423: 75-83).
Consequences of bee crisis for plant pollination
“If the bee disappeared off the surface of the globe then man would only have four years of life left. No more bees, no more pollination, no more plants, no more animals, no more man. – Einstein”. Perhaps you’ve already seen this alarming quote. There is in fact dispute as to whether Albert Einstein ever thought, let alone had much to say about bees. Nevertheless, projections of world food production without bee pollination are causing consternation.
To recapitulate high school biology for jaded molecular biologists, pollination is the process by which pollen grains, which contain the male gametes, are transferred in plants, thereby enabling fertilization and sexual reproduction. Bees are the major type of pollinator in ecosystems that contain flowering plants. Since plants are the primary food source for animals, the reduction or possible disappearance of bees could pose problems to both plant and animal biodiversity and to big chunks of our agricultural food supply.
Besides the domesticated honey bee, there are some 20,000 species of wild bee out there and relatively little is known about how their populations are changing with modern agricultural practices. But what is known isn’t positive – large declines in the diversity and numbers of wild bees have been observed in Europe over the last three decades. Traditionally, pollination in Europe has relied on the unmanaged activities of wild bees, for example, field beans in Europe are pollinated largely by longer-tongued bumble bee species, such as Bombus pascuorum, without which yields are poor.
If both domestic and native bees disappeared, there would be a catastrophic collapse in the pollination system. Animal-mediated pollination contributes to the sexual reproduction of over 90% of the approximately 250,000 species of modern angiosperms and many agricultural crops rely to some degree on pollinators for setting the seeds or fruits that we consume, or the seeds we sow or breed.
The EU estimates that honey bees play a key role in production of over 80 million tonnes of EU food each year – 160 kg of food per EU citizen! It has been estimated that the economic value of insect pollination to agriculture in the EU and USA/Canada is around €14 billion each.
However, relying on the natural distribution of wild bees and honey producers is uncertain. Therefore, many countries have developed contract pollination by honey bees. In fact, this has become essential where there are huge monocultures of food crops that cannot support wild bee populations – these areas become barren or even toxic for bees when the bloom is finished.
Professional honey bee beekeepers have become migratory, moving their bee colonies to seasonally varying high-demand areas of pollination – up to 40,000 km annually in the US (apples, pears and cherries in the NW, citrus and vegetables in Florida, blueberries in Maine, etc.). Pollination of large monocultures requires the concentration of very high populations of bees at bloom. The largest managed pollination event in the world is in Californian almond orchards, where 50% of all US honey bees (>1 million hives!) are trucked to the almond orchards each spring.
Growth of honey bee populations is artificially stimulated for pollination events by feeding artificial diets of sucrose or high fructose corn syrup and artificial protein diets. Could nutritional and environmental stress associated with such a modern bee’s nomadic lifestyle also be a contributory factor in CCD?
Scale of the pollination threat?
Honey bee pollination increases the edible yield of 46 of the world’s leading 115 food crop species, including apples, citrus, tomatoes, sunflowers, rapeseed and soy, while a further ten crops gain following pollination by other species of bee and insect. Without honey bees, food yield for some dependent crops would fall 90%. Around 35% of the human diet is thought to benefit from pollination. Globally, the value of insect pollination has been estimated at €153 billion – 10% of the total value of agricultural production. So, although mankind would not die if honey bees became extinct, our diet would change radically!
But some analysts maintain that the scale of the crisis is exaggerated: it’s not ‘global’. The disaster is limited to Europe and North America, said Argentinian, Marcelo Aizen. In fact, bees elsewhere are doing very well. In 2007, there were an estimated 72.6 million managed honey bee colonies worldwide. Despite bee colony declines since 1961 in both Europe (-27%) and North America (-50%), honey production has increased globally (to > 1 million tonnes) due to large increases in managed bee colonies in Asia (+426%), Africa (+130%), South America (+86%) and Oceania (+39%).
But Aizen admitted in 2009, that further analysis showed there were other pollination problems on the horizon (‘The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination’, Current Biology 19: 915-18). Basically, between 1961 and 2006, global agriculture’s dependence on pollinators has increased by 50% and 62% in the developed and developing world, respectively – a rate that has increased far more than the global number of managed honey bee colonies. Aizen reckons that if demand for such crops is maintained, there will be a consequent reduction in yields due to a lack of bee pollination. One way of compensating would be to plant more land with pollinator-dependent crops – 42% more in the developing world.
However, Aizen is assuming that the current unexplained problem of honey bee loss in Europe and the US doesn’t start spreading to the rest of the world. Something that remains to be seen!
CCD – still anybody’s guess?
So, are we closer to understanding why honey bee colonies are collapsing? The recent consensus isn’t very encouraging. An overview of CCD published in PloS One proclaimed itself to be “the first comprehensive survey of CCD-affected bee populations that suggests CCD involves an interaction between pathogens and other stress factors” (‘Colony Collapse Disorder: A Descriptive Study’, Dennis vanEngelsdorp et al., PloS One vol. 4(8): e6481). They concluded that CCD must be multifactorial and complex since, “Of 61 quantified variables (including adult bee physiology, pathogen loads, and pesticide levels), no single measure emerged as a most-likely cause of CCD. Bees in CCD colonies had higher pathogen loads and were co-infected with a greater number of pathogens than control populations, suggesting either an increased exposure to pathogens or a reduced resistance of bees toward pathogens.”
In other words, we still don’t really know what’s happening but bees are likely to continue disappearing in large numbers and with inevitable consequences for plant pollination.
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Info-Box The Honey Bee Chain - Which is the Weakest Link?Honey bees, Apis mellifera, live in colonies whose numbers vary according to season. A colony of domestic bees counts between 40,000 and 60,000 individuals during summer, of which 10,000 are forager bees that will gather enough nectar (a sugar-rich liquid produced by flowers) to form honey reserves for the hive over winter. During winter, colony numbers fall to around 10,000. Each colony is composed of three castes of adult bee – a queen, workers and males. It also contains the eggs, the larvae and nymphs. The Queen, the only fertile female in the colony, is unique. Only the Queen lays the eggs that ensure the continuation of the colony. The workers, non-reproductive females, represent the majority of the population. Their activity varies during their life – nurses, cleaners, wax-secretors, foraging pollen collectors and honey producers. Their numbers assure the thermal regulation of the colony. The males, several hundred, participate in the fertilisation of virgin females, present in temperate regions from April to September. The natural cycle of the colony is annual and it depends strongly upon the available vegetation in the environment. There are four successive phases. The queen starts laying eggs at the beginning of spring (up to 2,000 a day), before foraging flights start. The first larvae are fed with the reserve of pollen from the previous summer, which has been transformed into a mush by the nurse bees. The colony gradually develops; the queen laying more eggs as young bees are born that will be able to nurse new larvae. Foraging is coordinated. When a forager bee finds food it returns to the hive and dances on the comb. The precise movements of her dance communicate to the other bees the flight direction and distance to the source of nectar. Bees exhibit other complex behaviour, e.g. they build combs with perfectly hexagonal and regular cells, keep the hive clean, regulate the temperature and humidity of the hive, assess the qualities of a home for a new swarm, visually memorize the surroundings of the hive and protect the hive against predators. The survival of the hive depends on the integrity of these behaviour patterns. Towards the end of spring, when the population has reached its maximum, swarming occurs – the Queen leaves the hive with some of the workers to found a new colony nearby. A new Queen hatches in the original colony to replace the old Queen who left with the swarm. At the end of summer, the colony produces workers who will pass through the winter. These individuals will live longer, several months, than the summer pollinators, who have produced the honey stores on which the health of the over-wintering individuals is dependent during the cold season. During winter, the population is reduced to a few thousand workers around the Queen and lives on the reserves accumulated during the summer. And Beekeepers… The honey bee has been actively cultivated for its honey for at least 5,000 years. During the winter, the hives remain sealed and the bees don't leave the hive. Bees usually remerge from the hive in April, depending on the region and the weather. This is the moment when the beekeeper opens the hive for the first time since the autumn and verifies the state of the colony (or its demise), taking the opportunity to apply treatments against mites. During summer, the hives are moved and placed to be near particular flowering plants or as part of a pollination service. Honey is extracted and hives may be divided to generate more colonies. In autumn, there is a further treatment against mites for the winter. Each hive is weighed and fed with sugar substitutes to compensate for the removed honey. Hive entries are reduced in size to protect the bees from visitors and cold winds. |
Cartoon: © Roman Dekan - Fotolia.com