If you are lucky enough to come across some, dip your finger in a jar of honey from Pitcairn Island, a remote British Overseas Territory in the South Pacific. Honey is the island’s main export and is highly prized among gourmands. Pure and untainted by pesticides and pollution, it carries delicious subtropical notes of Pitcairn’s flora – passion flowers, mango, guava and rose apple.
It carries a lot more too, if you know how to look. Crack into any pot of honey and you are opening a portal to an entire ecosystem. Honey contains a detailed record of everything the bees that made it encountered during their foraging – not just the flowers that supplied the nectar and pollen, but also other plants, insects, fungi, viruses and larger animals in the environment.
Bees are “passive bioaccumulators”, explains at the University of Western Australia in Perth. As they go about their business, their fuzzy bodies inadvertently collect samples of whatever they come into contact with and these end up in their honey. “It includes everything,” says at the University of Bologna in Italy. “Well, almost everything.”
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żěè¶ĚĘÓƵs are now waking up to the possibility of dipping into that honeypot for sweet morsels of information they currently struggle to obtain. With advanced DNA tools, researchers are using honey to gather data on bee health, the general state of biodiversity in their foraging patch and diseases in the wider environment. It is pinpointing the possible culprits behind the mysterious colony collapse disorder wiping out honeybee hives, helping prevent food fraud and even allowing us to monitor shifts in climate. “It’s a beautiful way to capture all of that,” says Kaur.
Honey has been prized as a luxury foodstuff for millennia: and commercial production is recorded on cuneiform tablets from the Hittite empire.
Today, the apiculture industry produces about 1.8 million tonnes of honey a year and the market is worth around $10 billion.
The vast majority of commercial honey is made by the European honeybee (Apis mellifera), which produces it as a larder for the lean winter months. Foraging workers fly out from the hive to slurp up flower nectar or honeydew, the sugary anal secretions of aphids and other arthropods that feed on plant sap. Once full, the bees return and regurgitate the sweet liquids directly into the mouth of a hive worker, which partially digests it before regurgitating it into the mouth of another hive worker, or into a cell in the honeycomb. Once it is laid down, workers fan the proto-honey with their wings to dehydrate it. Matured honey is sealed up with wax and left for later – or for humans to steal.
Foragers don’t just return with nectar. They also collect pollen in sacs on their legs, which they mix with nectar and saliva and ferment into a substance called bee bread, which provisions the hive with protein. Foraging workers also visit water, soil and other plants to pick up supplies for the hive, including resins to make the propolis, or “bee glue”, which they use to stick the hive together. All these things find their way into honey, awaiting extraction by researchers.
A murky market
The idea that honey contains biological fingerprints of its origins isn’t new. In 1895, a German chemist by the name of Pfister (his forename is lost in the mists of time) and noted that the pollen grains within were diagnostic of where the honey was made. Thus began the science of melissopalynology, the visual analysis of pollen grains in honey to determine its geographical origin.
Melissopalynology can be a useful way to check the provenance of honey, which can significantly affect its market value. Basic honey costs around , while the most highly prized – usually “monoflorals” such as manuka made from the nectar of a single type of flowering plant – fetch . This price differential creates tasty incentives for fraudsters. Some unscrupulous producers attempt to pass off cheap honey as something more rarefied, or bulk out their honey with fillers such as rice molasses or corn syrup.
Melissopalynology can sometimes spot such practices. Chemical assays have also been developed to detect , and that are distinct to a particular location. But none of these techniques has ever been commercialised, says at Tamil Nadu Agricultural University in Coimbatore, India. They also struggle to detect bulking with non-honey sweeteners, which seems rife. In 2016, the European Commission assessed 893 samples from around Europe and found that .
Melissopalynology is also “very tedious to implement, and requires a considerable amount of training”, noted , then at the University of Grenoble in France, in a Furthermore, it can be quite imprecise, as pollen grains from related species are hard for even expert eyes to tell apart and some honeys don’t contain any pollen, either because they are made exclusively from nectar or honeydew, or because the pollen grains are filtered out during processing, sometimes to frustrate the eagle-eyed melissopalynologists.
Around 20 years ago, scientists realised that honey contained another key source of information: DNA. The European Union had recently enacted new regulations designed, among other things, to crack down on food fraud and asked scientists to develop new authentication methods based on DNA. Honey, being one of the foods most subject to fraud, was an obvious choice.
In 2010, Valentini and her team tested two honeys, one from the Pyrenees mountains and another a blend from sources worldwide, and found that within them was just as good as melissopalynology at identifying their origins as well as being quicker, cheaper and requiring less skill.
Also in 2010, a team led by at the Technical University of Berlin, Germany, published the . The researchers developed DNA tests for the pollen of plants commonly visited by honeybees on the French island of Corsica – sweet chestnut, lavender, eucalyptus, rockrose, oak and broom – and showed that these could be used to distinguish Corsican honey from honeys produced in Britain, Germany and Galicia in Spain.
Corsican honey, or Miel de Corse, is a valuable “protected designation of origin” product, meaning that only honey made there can legally be labelled as such, and it fetches a tasty premium as a result.
DNA authentication is now common practice in the honey industry. The technique has since been extended to identify not just pollen, but also organisms in the bees’ environment. In 2021, for example, at the University of Helsinki in Finland showed that honeys produced in Finland, Sweden and Estonia , microbes and fungi. Pollen-free honeydew honey, meanwhile, can be authenticated such as aphids that secreted the dew.
Another layer of authentication can identify the species of bee that produced a honey. Although the vast majority of commercial honey comes from European honeybees, some sought-after honeys are made by other species. A group of tropical and subtropical stingless bees called the meliponines, for example, make honey that costs a pretty penny and so is a target for being faked or adulterated. Ditto honey from the Asian honeybee (Apis cerana) and the giant honeybee (Apis dorsata). Even regional subspecies of A. mellifera , which is found floating around in the sticky stuff, further helping to pinpoint its geographical origin.
DNA testing has also been trialled as a way to monitor the health of colonies, flagging up the presence of including varroa mites, which are the most damaging pest of A. mellifera worldwide, according to Fontanesi. The mites eat the flesh of bees, are vectors for infectious diseases such as deformed wing virus and have been implicated in colony collapse disorder. The presence of varroa is currently detected by laborious on-the-ground monitoring, but testing honey when it is harvested would be much more efficient. Kaur says she is trying to persuade the authorities in Western Australia, which is currently varroa-free, to set up a honey-based surveillance system.
DNA revelations
Honey contains DNA traces of the bees’ gut microbiome too, . The microbes play an essential role in the health of the insects and their hives. Disturbances to the microbiome, which have been linked to the use of certain pesticides, make bees more vulnerable to and increase their overall mortality rates. Bees also have a microbiome on the surface of their body and the hive as a whole harbours beneficial microbes in the honeycombs, the brood combs where the queen lays her eggs and in the bee glue. All are vulnerable to disturbances and could be monitored via honey, says Kaur.
It isn’t just bee health that we can learn about. DNA analysis has been used to detect and the presence of invasive plant pests in the bees’ environment. Bee bread is another information-rich source about their wider environment. It, too, has been used to monitor plant species and detect the presence of pathogens and invasive species. Bees also transport pesticides and pollutants into the hive and deposit them in the honey, from where they can be .
The most common DNA authentication technique applied to honey and pollen is called barcoding, which can identify stretches of DNA, or “barcodes”, unique to a species in samples containing a jumble of genetic material. But DNA barcoding has limitations. It can only identify barcodes that the researchers choose to load into their assay. “You only know what you know,” says Kaur. “If there is something new, you don’t know it.”
Enter metagenomics (aka next-generation sequencing), which reveals all the DNA in a sample – called environmental DNA or eDNA – and then runs the results against databases of known genomes. If an organism in the sample is in a database, metagenomics should spot it.
Similar limitations apply: if an organism in the honey hasn’t been sequenced it won’t be identified. But the databases are growing all the time and the sequence information from honey can be rerun as often as required. “The same data could be blasted against the databases again six months later,” says Kaur. “Metagenomics is the way to go for sure.”
The technique is opening up whole new vistas in honey and pollen analysis. In 2018, Fontanesi and his colleagues and found DNA from a vast range of organisms. These included the bees themselves, their associated microbes and pathogens, the plants and sapsuckers they forage from and pretty much everything else in their environment. They even picked up the DNA of the beekeepers. “You get a lot of DNA information,” says Fontanesi. “It can be used to obtain an overall picture of the colony ecosystem and of the landscapes from which honeybees take their nutrients.”
Colony collapse
This proof-of-concept study suggested numerous applications for honey metagenomics. It could, for example, help researchers monitor the health of colonies in more depth than barcoding. In particular, it could finally get to the bottom of colony collapse disorder. The syndrome is a threat to the viability of commercial beekeeping and to the pollination services that are vital to agriculture and natural ecosystems. The ratio of bees to crops is already in decline, largely due to economic pressures: over the past 50 years, production of pollination-dependent food has tripled, but . Colony collapse disorder threatens to worsen this shortage.
Various culprits have been suggested for colony collapse disorder besides varroa mites. They include other pathogens, pesticides and disturbances to the bee and hive microbiomes. Honeys from collapsed colonies could help researchers work out which of these factors matter the most.
Metagenomics has also been trialled as a way to gather useful but hard-to-obtain information from pollen. A team led by at Brock University in Canada collected samples of bee bread and pollen-coated forager bees from inside commercial beehives on blueberry farms in the country. The researchers not only detected the previously unknown presence of 10 bee viruses, but also spotted , suggesting that bees can also be used as an early warning system for agricultural diseases.
A more ambitious proposal is to use honey for to supplement or replace traditional sampling by fieldworkers on the ground. This classic data-gathering method faces numerous challenges, says Fontanesi, including high costs, the difficulty of getting comprehensive information and problems reaching remote places. As a result, there is a long-standing “critical shortage of biodiversity data”, he says.
In addition, traditional biodiversity monitoring captures very little information on microbes, which are vital to the functioning of ecosystems and are increasingly recognised as being threatened by the same pressures that are wiping out larger organisms.
All of these limitations can be overcome by delegating the task to bees. An individual worker forages an area within a radius of and can take a dozen or more trips per day, visiting a wide variety of habitats as it collects nectar, pollen, water and resin. A colony can contain up to 16,000 foraging bees, meaning they are able to gather quantities of data that scientists using traditional sampling methods can only dream of.
“Honeybee colonies are unique, large-scale biomonitoring tools that can provide insights into the status of ecosystems,” says at the Alexander Fleming Biomedical Sciences Research Center in Vari, Greece. She and her colleagues recently applied and showed that it could identify what plants the bees were foraging from, the contents of their gut microbiome and the presence of pathogens in the hive, including varroa.
It is still early days for honey metagenomics, but there are sweet dreams. Fontanesi and his colleagues have established a biobank of honey samples going back 25 years, mostly from Italy, from which they are extracting as much information as they can. It could, for example, be used to track how the climate has shifted by looking at the changes in pollen profiles.
The grand vision is to establish a network of honey monitoring sites to collect and collate environmental information that is currently lacking. That hasn’t happened yet, but there is a growing buzz around the concept, says Kaur. “I think it’s a brilliant idea. Hopefully, everybody will come together and join hands and minds and make it happen.”
Graham Lawton is a staff writer at żěè¶ĚĘÓƵ
