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New Zealand provides an interesting case study of the epidemiology of American foulbrood (AFB) in managed honey bee colonies. There are several reasons for this.
First, the use of antibiotics to control AFB is illegal in New Zealand, and beekeepers have never used oxytetracycline or sulphathiazole in their hive management. Because beekeepers in New Zealand do not use these drugs, clinical symptoms of AFB are not artificially suppressed, and we can therefore get a clearer idea of the "natural" incidence of the disease in managed colonies, and its spread to other colonies, both managed and wild (feral).
Second, New Zealand has accumulated reliable, accurate, long-term information on the incidence of AFB, a situation that doesn't exist in many other beekeeping countries. The information isn't based on estimates, or only on the findings of government inspectors. The information is far more comprehensive because it also includes the AFB findings of the beekeepers themselves.
In New Zealand, all beehives and apiaries are required by law to be registered for disease control purposes (and a hive in each apiary must be marked with the registration number issued to the beekeeper). All apiary information is lodged in a computerised database, and the record contains, amongst other details, a GPS verifiable grid reference identifying the position to within 100m.
Because apiary locations are constantly changing, there is a further legal requirement for beekeepers to update all apiary information on a yearly basis in the form of a computer printout.
At the same time, beekeepers are required to report all findings of AFB in each apiary over the preceding 12 months. While the reporting could never be expected to be 100% accurate, compliance rates by beekeepers are good, and the information they provide allows for the targeting of further inspections.
There is also a further component of AFB information in New Zealand that is similar to that collected in a number of other countries. This information is derived from inspections carried out by government inspectors, either as part of a contracted programme of AFB control with the National Beekeepers' Association (NBA), or as part of other inspection work contracted either by the Ministry of Agriculture's exotic disease surveillance programme, export certification inspections, or other contracted work such as pollination audits. Altogether, these government personnel inspect approximately 10% of the nation's apiaries each year.
Official information on AFB incidence in New Zealand goes back over half a century (Table 1 presents this information for the last 35 years). The historical record shows that a major increase in AFB incidence occurred in the period 1965-90, with incidence increasing 422%, from 0.2% to 1.2% of hives per annum. The increase corresponded with a major increase in hive numbers in New Zealand. Over the same period, beehives increased by 75%, reaching a high of just over 340,000 in 1987.
The most dramatic increase in hives occurred in the late 1970's and early 1980's, as beekeepers enlarged their businesses in response to the pollination demands of kiwifruit, a major New Zealand horticultural crop. Plantings of kiwifruit increased 15 fold during that period, and hives were required for pollination of kiwifruit orchards at a density of 8 hives per hectare, one of the highest hive densities for any crop in the world. In the 1980's, hive numbers increased by 45% in just seven years.
Beekeepers in New Zealand have always contended that a major reason for the dramatic increase in AFB incidence was related to this increase in hive numbers, with new beekeepers coming into the industry with less knowledge about AFB diagnosis and control. They also argue that the rapid splitting of hives to increase numbers, and the practice of evening out hives prior to kiwifruit pollination, which was practiced extensively in the 1980's, both exacerbated the spread of AFB spores.
Whatever the cause, there was a rapid increase in AFB incidence in the period 1985-1991, with AFB hives jumping 130%. Beekeepers argue that the slight lag in this disease increase compared to the increase in hives, which plateaued in 1987, was caused by the time required for AFB infections to develop and for the spores to spread to other hives.
In 1991, a concerted programme was implemented to reduce this AFB incidence. Unlike previous AFB control programmes in New Zealand, which had been paid for by government, and which didn't have any direct supervision from the beekeeping industry, this programme was financed and directed by the NBA. The work itself was carried out by government personnel on contract to the Association, and the performance of these government personnel was strictly controlled by detailed contract specifications.
The programme involved the annual inspection by government apiary officers of 4% of the country's apiaries. It also included an important component of voluntary inspections carried out by NBA members under the direction of government personnel.
These voluntary inspections are commonly referred to in New Zealand as "diseaseathons." The name plays on the popular charity events on television called "telethons." Diseaseathons generally involve commercial beekeepers donating several days of their time in the spring period to inspect hives often belonging to hobbyist beekeepers. In many parts of the country, diseaseathons are now annual events enjoyed by both commercial and hobbyist beekeepers.
The programme also included a significant counselling component, where beekeepers with AFB problems received advice and assistance from trained professional apiculturalists in reducing AFB incidence in their outfits.
Finally, there was also a research programme carried out by Dr. Mark Goodwin and his team at the Ruakura Research Centre in Hamilton, New Zealand. The research concentrated on factors contributing to the spread of AFB, and simplified ways of detected AFB spores in bees and bee products.
By any measure, the programme was an outstanding success. In the seven years it was in existence, reported AFB incidence decreased on average by 12% per annum, reaching a low of 0.3% in 1999. At the same time, the government agency contracted by the NBA to carry out the programme met or exceeded all contract specifications each year, and kept within the budgets set in the yearly contracts.
Questions were raised towards the end of the programme regarding whether the decreases in reported AFB incidence were a true reflection of the actual AFB incidence in New Zealand beehives. It was argued that reports of AFB made by beekeepers could not be trusted, and that there might be other reasons, such as the stigma attached to AFB or export certification requirements, that could cause beekeepers to under-declare their AFB.
A study was therefore carried out comparing the change in AFB incidence reported by beekeepers with the change in AFB incidence found by government inspectors (Table 2). As the table shows, the reduction in AFB incidence found by inspectors closely tracked AFB incidence reported by beekeepers, and in fact decreased at a slightly faster rate.
This was a remarkable finding, since AFB inspections carried out by inspectors were required by contract to target beekeepers and areas with a known history of AFB. One would therefore have thought that if anything, these government inspections would have decreased at a slower rate. The fact that they didn't, and that they followed so closely the trend of beekeeper reports, strongly suggests that the decreasing trend in beekeeper reports of AFB was a real decrease and not simply under-reporting.
The question overseas beekeepers often ask is, "How do New Zealanders control AFB without the use of antibiotic drugs?" There are really no great secrets or complicated systems in the approach, and Dr. Goodwin and I have attempted, as best we can, to tell the story in a book that has recently been published by the NBA (Figure 1). The book is entitled "Elimination of American Foulbrood Without the Use of Drugs: A Practical Manual for Beekeepers", and in 1998 was distributed to beekeepers throughout in New Zealand. The book is now also available internationally from beekeeping booksellers.
Beekeepers in New Zealand eliminate AFB by using routine and constant AFB inspection, managing their beehives in such a way that they reduce the spread of AFB, and destroying colonies that are found to have clinical infections of the disease.
The system operates on a premise many beekeepers seem reluctant to accept, but a premise that beekeepers nevertheless know, deep down, is true. The premise is: most AFB infections in beehives are due to the beekeeping practices that are carried out on those hives.
Once that premise is accepted, it then follows that the incidence of AFB in the beehives can be reduced by changes in those beekeeping practices. If the incidence of AFB in a beekeeper's hives is remaining stable, the war actually isn't being won. In fact, the beekeeper is infecting clean colonies at the same rate that diseased colonies are being found and destroyed. And if the incidence is increasing, then the beekeeper is infecting more colonies than are being found and destroyed.
To alter the situation, the beekeeper can take one or both of the following approaches. First, the number, frequency, intensity and timing of disease inspections can be modified to find more AFB hives earlier. And second, changes can be made in management practices to slow the spread of the disease. An important management practice often used is quarantines.
First to AFB inspections. From my own experiences observing beekeeping around the world I have come to the conclusion that brood inspections are carried out more often and more thoroughly in New Zealand than in some other beekeeping countries.
Beekeepers in New Zealand have been encouraged for many years to inspect all, or almost all, brood frames, whenever they go into a hive, and especially whenever they take anything from a hive, such as brood, honey or boxes, that may immediately or eventually be put on another hive. As an example, it has been observed that beekeepers in New Zealand who have low AFB infection rates also generally inspect their beehives either when or just after they take their honey off.
While at first hearing it may sound contradictory, case studies in New Zealand have also shown that changes in the frequency and thoroughness of inspections can reduce the incidence of AFB. The reason is that more frequent and thorough inspections are likely to pick up AFB infections at an early stage, before they have a chance to produce large numbers of infective spores and before those spores can be spread to other colonies.
In New Zealand, a major beekeeping management component that has proven successful in eliminating AFB is quarantine. Quarantine involves controlling and recording the movement of materials that have the potential to carry infective levels of disease spores. There are generally two types of quarantine: apiary quarantine and hive quarantine.
Some beekeepers in New Zealand routinely use apiary quarantines when they take their honey off. They mark stacks of supers according to the apiary site, and then either ensure the supers go back on the same apiary the next year, or only release the supers into general use after the apiary has received an all-clear for AFB following several brood inspections the next spring.
Apiary quarantines are used as a matter of routine, rather than just when an outbreak of AFB occurs. They provide a means of ensuring that when an AFB problem is discovered, the disease doesn't spread via beekeeping equipment to other apiaries.
Hive quarantines are more time consuming, but are definitely used by beekeepers when they experience an AFB outbreak in an apiary. In a hive quarantine, hive components associated with an individual hive remain with that hive, or are marked with a number identifying it to that hive so that the components can be returned to the hive the next year. The general rule of thumb for an all-clear release of such a quarantine is one and a half beekeeping seasons following the finding of the last AFB hive in the apiary.
The important thing in such quarantines is to control the movement of materials that actually have the potential to carry infective levels of disease spores, rather than putting emphasis, and dare we say paranoia, on materials and practices that have a much lower potential disease risk.
Dr. Goodwin's research has shown that by far the materials most capable of carrying infective levels of spores are 1) extracted honey supers, which are often taken unknowingly from AFB hives, and then put on clean hives, generally a year later, and 2) frames of brood and honey, which are often moved unknowingly from hives with sub-clinical AFB hives (that is, hives not showing visual symptoms) to clean hives.
Most of the other things beekeepers normally blame for the spread of AFB turn out not to be as significant or widespread as beekeeping practices. Robbing can be an important cause, of course, but it is usually the result of inadequate levels of beehive inspection, which is really just another name for poor beekeeping management practice.
Dr. Goodwin's studies of spore levels on adult bees have also shown that wild (feral) colonies are not a major source of AFB in most situations and areas of New Zealand. This was quite a revelation to beekeepers in our country, who often blamed wild colonies for their AFB woes. Dr. Goodwin's studies showed, however, that wild colonies are at greater risk of being infected with AFB spores from managing colonies, rather than the other way around.
Dr. Goodwin has also shown that drift of bees from AFB hives to healthy hives is not an important factor, and such things as hive tools, smokers and gloves, as well as the soil in front of hives, foundation and queen bees, are all of little consequence as sources of infective levels of AFB spores.
In addition to inspection and management practices, there is a further component of AFB control in New Zealand, which from the evidence seems to have started as a practice in our country, and which has been used there for many years. The technique involves emersion of the woodenware for at least 10 minutes in paraffin wax heated to at least 160degC.
Dr. Goodwin's research has shown that this technique is one of the few effective ways of destroying AFB spores. His work also shows, however, that the time and temperature are very important, because lesser levels of either will leave significant amounts of viable AFB spores remaining.
Most beekeepers in New Zealand sterilise the supers, boxes and lids that are associated with AFB hives. The sterilisation technique is very basic, and can be used by a beekeeper in the yard behind the honey house.
Paraffin wax sterilisation has the added benefit of preserving woodenware against dryrot. It is, however, a dangerous technique if not carried out by a skilled person, and boil-overs of over-heated paraffin can result in fires that can be difficult to bring under control.
The effectiveness of quarantine programmes in reducing and even eliminating AFB in beekeeping outfits in New Zealand is demonstrated in a set of AFB incidence figures kindly provided by Mr. Ian Berry and his sons Peter and John, from Arataki Honey Hawkes Bay in Havelock North, New Zealand (Tables 3 and 4).
Table 3 shows the number of hives found to be infected with AFB in the Hawkes Bay outfit from 1965 to 1999. From the figures it's obvious that the outfit had two significant outbreaks of AFB during that time, the first beginning in 1973, and the second beginning in 1989.
The 1973 outbreak was the result of the purchase of used honey supers from another outfit with an unknown AFB status. Clearly, the other outfit had an AFB problem, and that problem was transferred to the Arataki Hawkes Bay hives by way of those supers. Because the supers were put on a number of Arataki hives before their disease status was determined, the outbreak could not be easily quarantined, and it took the Berry's a further 6 years to bring AFB incidence down to negligible levels.
The second outbreak, in 1989, was the result of Arataki Hawkes Bay purchasing a beekeeping outfit as a going concern. The outfit had an AFB problem, but the Berry's quarantined that outfit, and as a result the infection did not spread to other Arataki Hawkes Bay hives. The infection was therefore brought under control more quickly.
The most important point the figures illustrate, however, is that it is possible using search and destroy inspections, hive and apiary quarantines, and beehive component sterilisation, to successfully eradicate the disease, or at least to operate an outfit within the internationally accepted veterinary standard for "disease freedom" of 0.2% of animals per herd per annum. Arataki Hawkes Bay achieved that in 27 of the last 34 years, and in the each of the last 10 years (Table 4).
Now before readers dismiss the evidence presented in this case study as not being possible in large, commercial, migratory beekeeping enterprises, I need to point out that Ian Berry and his sons together run some 7000 colonies. They put a considerable number of those hives into apple and kiwifruit pollination in the Hawkes Bay region of New Zealand, in close proximity to other pollination hives belonging to a range of other beekeepers. The Berry's also move many of their hives to chase several honey flows.
Over the last four years, in those 7000 hives, the Berry's have not recorded a single AFB hive.
The National Beekeepers' Association in New Zealand has recently embarked down a new road in relation to AFB control. In 1998, the New Zealand government replaced existing AFB control legislation with a Pest Management Strategy (PMS), and gave over responsibility for control programme policy and delivery to the Association. Government continues to maintain an auditing role to ensure the objectives of the PMS are met and legal powers are not abused, but it is the Association's responsibility, through its contractors, and with income levied from beekeepers, to run the programme effectively.
Beekeepers in New Zealand have set themselves an especially challenging goal in their AFB PMS. The goal is to eliminate AFB in managed colonies in New Zealand. The primary objective is to reduce AFB incidence by an average of 10% per year, with an incidence no greater than 0.1% at the end of the second term of the strategy in 2008.
Beekeepers, professional apiculturalists and beekeeping scientists in New Zealand believe that elimination of AFB is possible in our country both because we have a relatively small population of honey bee colonies (estimated to be 400,000 including wild colonies), and because the importation into New Zealand of additional colonies and other materials capable of carrying AFB is strictly controlled. Needless to say, in both cases it greatly helps that New Zealand is an island nation very much isolated from other major beekeeping countries in the world.
At the same time, the chances of AFB elimination are also enhanced in New Zealand by the current low incidence of the disease, and its relatively low infectivity.
Finally, beekeepers believe that AFB can be eliminated in New Zealand because some beekeepers there have already shown that elimination from their own outfits is possible. The argument goes that if beekeepers with very large hive holdings like Ian Berry and his sons can eliminate AFB from their outfits, there is no reason why every beekeeper in New Zealand shouldn't be able to do the same.
Is AFB elimination in a country possible? The next 10 years will tell the story. On the one hand, the track record of AFB control in New Zealand, as well as the success of beekeepers like Ian Berry in eliminating AFB, are excellent portents for the future.
On the other hand, the new PMS structure puts the AFB control programme squarely under the influence of the political processes of the beekeeping industry in New Zealand. A great friend and colleague, the late Ted Roberts, often used to remark to me in his wonderful Welsh accent, "There are some things that are too important for politics, and disease control is one of them."
It is my strongly held view that members of the NBA must continue to insist on a positive commitment to the programme and its objectives from their industry leaders, as well as proper financing of the programme budget, if the goal of the AFB PMS is to be achieved. Put another way, the will of the NBA must match the will of beekeepers like Ian Berry and his sons if AFB is going to be eliminated in New Zealand.
(Note: Incidence equals the number of AFB hives reported divided by the total number of registered beehives)
(Note: The internationally accepted veterinary standard for disease freedom is 0.2% of animals per herd per annum)
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