Risk management in primary apicultural production. Part 1: bee health and disease prevention and associated best practices

Abstract

Prompted by FAO/WHO's and the European Commission's recognition that documents on Good Farming Practices (GFPs) and Good Veterinary Practices (GVPs) in apicultural production are hardly available, part 1 of this contribution provides an update of current apicultural production and associated best practices to ensure animal and public health. Major bee health and disease prevention issues and risk management options at the primary production level are summarised with particular reference to the role of the veterinary practitioner/consultant and the official veterinarian in a control function in the safe production of honey.

Keywords:

• apiculture
• bee health
• bee disease prevention
• GFPs
• GVPs

1. Introduction

Apiculture (beekeeping) is the practice of the management of honey bees in hives, principally for the honey and pollination (ecosystem services). Hives of bees also produce other products such as wax, royal jelly, propolis and pollen. In addition, an important aspect of beekeeping is the production of bees, queens, package bees, etc. The assurance of bee health has recently become of ecological concern with the advent of phenomena such as Colony Collapse Disorder (Berenbaum 2007; EFSA 2008; Hendrikx et al. 2009; Higes et al. 2009; Vanengelsdorp et al. 2009; Neumann and Carreck 2010). As a result, the European Parliament has called upon the Commission ‘to incorporate into its veterinary policy, research into, and actions to tackle bee disease’ (European Parliament 2008). Each Member State funds bee health research to differing degrees, various international research projects are currently being conducted and research priorities from the apicultural production sector have been formulated, both at EU level and in each Member State (e.g. COLOSS (Neumann 2010a), BEE DOC (Bilikova and Simuth 2010; De Graaf 2010; Forsgren 2010; Moritz 2010; Paxton 2010) and STEP (Neumann 2010b) Bee SHOP (Jaffé et al. 2008), ALARM (Grabaum et al. 2006), APENET (Mutinelli et al. 2009)).

The European Rapid Alert System for Food and Feed (RASFF) has in the past few years also substantiated claims that contaminated and hence potentially unsafe honey is still being produced in the European Union and beyond (RASFF 2004, 2005, 2006, 2007, 2008). It is now timely that the veterinary profession is updated on how it can help to improve apicultural performance.

The role of the veterinarian in apiculture has to date been a modest one, because in some countries the responsibility for bee health does not lie with the veterinary authorities. Hence, in many veterinary curricula, bee health and disease prevention (if at all considered important enough to be specifically addressed at the undergraduate level) is usually restricted to basic bee pathology and sometimes covered only as part of the elective study programme. However, in some countries commercial apiculture is significant and beekeepers are increasingly seeking the support of knowledgeable scientists to advise them on disease prevention and treatment, safe honey production and the related legislative aspects. Also, for veterinarians in a control function (‘official veterinarians’ e.g. those affiliated with the competent authorities) a more solid knowledge of beekeeping practices and associated animal and public health issues is necessary to ensure the performance of responsible inspection and auditing exercises. Consequently, postgraduate Diploma courses for veterinarians who professionally have to deal with bee health and honey safety (Apimondia.org 2009) as well as a blog for veterinary experts in honey bee pathologies (Apivet.eu 2009) are now being offered.

Probably the most important role for veterinarians in apiculture is education, because education of beekeepers is crucial in the correct identification of bee diseases, and the correct application of veterinary medicines. In this context, it should be acknowledged that expert beekeepers will play an important role in training and bee health surveillance and here again veterinarians could be part of education programmes.

In this article, an overview of bee health and disease is presented from a preventive veterinary medicine point of view. A further paper (Formato et al. 2011) will deal more specifically with the elaboration of a risk management system for assuring the safety of unprocessed honey, based on Hazard Analysis Critical Control Point (HACCP) principles. The purpose of these companion papers is to update the readership on apicultural essentials and to indicate options for risk management in which they are or might become involved, in their capacity as veterinary practitioner/consultant (e.g. as teacher in courses for beekeepers) or in their function as official veterinarians in the context of European regulations (European Commission 2004a, 2004b; Smulders et al. 2005), so as to contribute to ongoing international efforts to improve bee health and honey safety.

2. The background of beekeeping

In 2008, the European Food Safety Authority (EFSA) published data from a survey which included amongst other elements, the current level of honey production and its geographical distribution across Europe (Figure 1). Although not completely complying with FAOSTAT and EUROSTAT data, said survey identified Spain, Hungary, Germany, Romania and Poland as the top-five largest producers of honey (EFSA 2008). A more recent document [Regulation (EU) No 726/2010] has identified Spain as the country in Europe with the largest bee population (2,459,373 beehives) and estimates the total European bee population at 13,985,091 million beehives (European Commission 2010).

Figure 1. Distribution of average honey production in Europe combining FAOSTAT and EUROSTAT data (reprinted figure with permission from EFSA (2008)).

Annually an approximate 1.2 million tonnes of honey are produced globally, about 400,000 tonnes of which are traded internationally, main exporters being China, Argentina and Mexico. The degree of self sufficiency of the EU is 40–50% (Michaud 2005). Consequently, products marketed in Europe are sometimes mixes of indigenously produced and imported honey (Ortelli et al. 2004).

A more comprehensive overview of apiculture is provided in the following literature: International Bee Research Association (IBRA; www.ibra.org.uk), the beekeeping portal (www.apiculture.com), Danant (1975) or Crane (1990). All these sources include detailed background information and the various technical terms generally used in literature on beekeeping. This first section aims at introducing some essentials.

A population of honeybees (Apis mellifera spp) in a colony includes one queen (with a life span of 3–4 years) which exclusively lays eggs in the cells of the comb. Unfertilised eggs (containing a unique combination of 50% of the queen's genes) develop into haploid ‘drones’ (i.e. male bees which die upon mating or are expelled from the beehive before overwintering). Following one or more nuptial flights the queen establishes herself in the hive and begins laying eggs in the comb, consisting of thousands of hexagonal cells made by worker bees from wax produced in glands on the underside of their abdomen. Hatching of the eggs takes place in 3–4 days, worker bees feed hatched larvae for 5–7 days whereupon they ‘cap’ the cells with a semi-permeable wax membrane allowing the larvae to pupate rendering either virgin queens, worker bees or drones (i.e. after ca. 16, 21 and 24 days after the egg has been laid, respectively). Worker bees have a life cycle of a few weeks in summer and up to several months in areas with extended winter. Approximately, 20 young worker bees, between 6 and 12 days old, feed the queen with ‘royal jelly’ (secreted from the hypopharyngeal glands) allowing her to continually produce eggs (up to 1500 in mid-summer). Cells are used to develop larvae from the eggs the queen has laid (‘brood cells’) whilst other cells serve the purpose of storing honey and pollen.

A colony typically will vary in size from summer (50,000 or more) to winter (5–15,000 individuals). Apiaries (areas containing one or more man-made beehives in which colonies are kept and cared for) may consist of one to (in commercial beekeeping) hundreds of hives.

A diagrammatic presentation of the typical modern beehive is included in Figure 2.

Figure 2. Essential features of the typical modern beehive (reprinted figure with permission from P. Gordon (2004)) (A) Hive stand: Providing clearance from ground level thus avoiding damp, reducing accessibility for intruders (e.g. mice). (B) Entrance block: Denying or reducing bees’ access to hive, in Wintertime equipped with a mouse guard. (C) Floor board: Rest for brood box with entrance allowing access for bees. (D) Brood box: Series of vertically hanging brood frames on which queen can lay eggs and worker bees perform their various tasks (feeding larvae, caring for drones and queen). (E) Queen excluder: Wire construction preventing queen from laying eggs in super; equally impassable for drones. (F) Super: Containing vertically oriented shallower frames for honey storage; in productive years more than one super necessary. (G) Crown board: Insulation board preventing the escape of too much warmth from super. It contains apertures (1) to insert feeder for supplementary feeding, (2) for bee escape (one-way exit: return through this aperture impossible). (H) Roof: Water-proof cover with metal gauze ventilation holes (inaccessible to insects, robber bees and wasps).

In terms of veterinary public health, apiculture is significant as it involves such fields as food safety, environmental hygiene, human nutrition and disease control [(as bees are involved in the transfer of some communicable diseases listed by the World Organisation for Animal Health (OIE; Table 2)].

Bees play a significant role in public health for the following reasons:

1.	because the incorrect use of some veterinary treatments (e.g. acaricides, antibiotics) may lead to residues of these substances being concentrated in honey, which may also be the case for environmental contaminants such as phytotherapeutics, polycyclic aromatic compounds (e.g. benzene and dioxin), heavy metals and radionuclides,
2.	as bees function as ‘monitors’ for the environmental contamination with the above or other substances used in agriculture (Devillers and Delègue 2002; Yazgan et al. 2006),
3.	as honey has been incriminated in cases of infant botulism caused by spores of clostridial toxin producers [(e.g. Clostridium botulinum); See: Formato et al. 2011)],
4.	as after swarming of colonies these may invade houses or buildings,
5.	because at times honeybees may be highly defensive, the more so after hybridisation with imported bee breeds, after which they can develop particular aggressiveness (‘africanized bees’).

3. Bee health and disease prevention

3.1. Good farming practices

Table 1 lists the various hazards encountered in apicultural practice and the associated Good Farming Practices (GFPs, ‘best beekeeping practices’) preventing these. It characterises the hazards in terms of adverse effects on bee health and honey safety, honey quality and production efficiency and qualitatively indicates the severity of these effects. Table 2 specifically summarises the various agents that jeopardise the honeybee's health and the measures to prevent or treat the associated illnesses. Extended reviews on the various bee diseases have recently become available (Journal of Invertebrate Pathology 2010).

Table 1. Analysis of hazards to bee health (BH), honey safety (HS), honey quality (HQ), production efficiency (PE) and the associated Good Farming Practices (GFPs) preventing these.

	Hazard characterisation		Relevance for
Hazard identification	Hazard specification (and adverse effects)	Severity	BH	HS	HQ	PE	Associated GFPs
1. Apiary site	1.1 Areas characterised by intensive agriculture (increased risk of exposure to pesticides and other chemical contaminants; bee welfare)	VS	*	*	*	*	Survey apiary surroundings before establishing apiary, stay informed of changes Notification of any hazardous operations
	1.2 Areas with heavy industry and traffic (increased risk of exposure to heavy metals and other chemical contaminants)	VS	Some times (not in case of heavy metals)	*	*	Some times (not in case of heavy metals)	Survey apiary surroundings before establishing apiary, stay informed of changes
	1.3 Areas with high relative humidity (increased risk of fungal pathologies; bee welfare)	S	*			*	Refrain from apiculture in said areas
2. Hive identification	Absence of individuation codes (makes honey traceability impossible)	S		*	*		Apply unmistakable numerical code for purposes of hive individuation and subsequent documentation; note that in practice honey from hives is blended and extracted together so, at least, honey should be identifiable by apiary
3. Bee source	3.1 Collecting of unhealthy swarms without sanitary intervention (disease transfer, introducing undesirable genes in the apiary through newly acquired drones)	S	*			*	Respect quarantine measures, treatment of swarms against Varroa mite, inspection, monitor pests and disease (e.g. American Foul Brood); check the productivity and resistance to disease
	3.2 Purchasing unhealthy new stocks of bees (disease transfer, introducing undesirable genes in the apiary through newly acquired drones)	S	*	*	*	*	Assure sanitary status through inspection of the bees and of the new frames and combs; respect quarantine measures; select bee provider adhering to GFPs, avoid buying from unregistered apiaries; check the productivity and resistance to illness
4. Hive inspection	4.1 In very cold weather (death of the brood and cold-stress for adults, bee welfare)	S	*			*	Limit inspection during winter time and in inclement weather
	4.2 Wrong inspection interval (spread of pathogens, bee welfare, death)	S	*			*	Inspect regularly (frequency dependent on season)
	4.3 No inspection of weak colonies (spread of pathogens, death, bee welfare)	S	*			*	Conduct thorough inspection especially when colony strength and production are low
	4.4 Refraining from additional testing (spread of pathogens, death, bee welfare)	S	*			*	Confirm visual inspection by laboratory diagnosis of diseases on brood (AFB, EFB) or on adult bees (nosemosis, virosis)
	4.5 Failure to notify relevant organisation of adverse BH event (spread of pathogens, death, bee welfare)	S	*			*	On suspicion of adverse BH event, notify relevant national organisation for BH
	4.6 Poor hygienic procedures (transfer of pathogens from one hive to another in the same apiary or from a different apiary)	VS	*			*	Use of sterilised beekeeping equipment (hive tool, etc.), clean beesuits and disposable gloves
5. Drugs and medicines	5.1 Using unauthorised drugs (risk of administering fatal dosages)	VS	*	*	*		Exclusively apply drugs registered for use in bees
	5.2 Applying drugs with supers in position (risk of honey contamination)	VS		*	*		Remove supers until withdrawal time of drug has expired
	5.3 Wrong application procedures (risk of honey contamination, bee welfare)	VS	*	*	*		Respect instructions and guidelines for drug use
	5.4 Lack of traceability (prevents effective risk management)	VS		*	*		Record drug use in logbook
	5.5 Leaving drug application tools in the hive (risk of residue formation and drug resistance)	VS	*	*	*		Remove all drug application tools from the hive
	5.6 Unsynchronised drug application against Varroa destructor (ineffective pest control, bee welfare)	S	*				Synchronise Varroa control measures in single apiaries and preferably regions
	5.7 Lack of suitable registered medicines classified as POM/VPS (lack of effective and easily available medicines encourages use of illicit drugs and alternative treatments that can harm the colony, the beekeeper and resultant honey)	VS	*	*	*	*	Exclusively apply drugs registered for use in bees
6. Breeding of the queen	Neither assessing the queen's performance nor her age (disabling monitoring of disease resistance, level of queen's productivity, swarming recognition)	M	*			*	Mark the queen with a colour, specific for the year of her introduction in the hive, replace queen every 2 or 3 years (preferably in late Summer), verify the incidence of diseases and the productivity of the hives
7. Winter precautions including hive maintenance	7.1 Insufficient insulation of the hive (cold stress, bee welfare)	S	*			*	In Autumn (but subject to the specific environmental temperatures in of different countries): reduce size of hive entrance, reduce number of frames and replace them by follower boards, cover hive with insulating material (e.g. black tar paper), check integrity of hives, substitute deficient parts
	7.2 Insufficient food stores (jeopardises bee survival, risk of starvation during Winter, bee welfare)	S	*			*	Feed bees over the Winter, depending on the strength of the hive and the quantity of stores in the hive-box
	7.3 Insufficient protection from attack by pests (jeopardises bee colony survival)	S	*	*		*	Colonies need to be protected from attacks from wasps, hornets, woodpeckers, badgers etc.
8. Bee nutrition	8.1 Feeding bees with honey from unknown sources (possible transmission of pathogen (e.g. P. larvae or Nosema spp.) or residues, bee welfare)	VS	*	*	*		Provide candy or glucose/fructose syrup Never use honey from outside the apiary!
	8.2 Not providing enough feed to weak or young colonies (risk of starvation, productivity losses, bee welfare)	S	*			*	Take special care of young or weak colonies during Autumn, Winter and excessively cold or rainy Springs
	8.3 Insufficient pollen and variety of pollen in the area	S	*			*	Ensure apiaries are sited near a wide variety and abundance of flora, especially spring and late summer flora
9. Homogeneity of colonies growth and production within the apiary	Not balancing the bee-population between hives (weak colonies: risk of starvation, diseases and being subject to robbing; strong colonies: risk of swarming and promoting robbing behaviour)	S	*			*	After having monitored their hygienic status, transfer frame from stronger to weaker hives
10. Swarming	Not taking preventive measures (spread of swarms in the environment without sanitary measures, spread of pathogens, bee welfare, depopulation of hive)	S	*			*	Keep colonies at similar strength (see above), adopt genetic selection for queens with low swarming tendency, adopt specific beekeeping technique to prevent swarming (e.g. hive division, providing bees with new honeycomb foundations, etc.) Ensure that hive capacity is sufficient to discourage swarming
11. Queen excluder	Eggs being deposited in combs of supers intended for honey storage (impairs HQ, disease spread through cross-contamination when supers are interchanged between hives in subsequent years)	S	*		*		Adopt use of queen excluder Ensure queen excluder is in good condition and does not have excessive gaps anywhere
12 General bee welfare	Impaired welfare reduces disease resistance and PE (exposure to pathogens, decrease in productivity)	S	*			*	i)At high ambient temperatures in Summer remove entrance restrictions and bottom board (Varroa net to remain in place, ii) Follow proper hive inspection procedures [i.e. not in Winter, at dusk or during inclement weather, (see above), and move steadily and smoothly], iii) Assure a constant quantity of stores, iv) Mow grass and weeds around hives to prevent insect intrusion via plant stalks, and to facilitate bee flights, v) Annually replace ca. one-half of the wax brood frames
13 Improper honey harvesting	13.1 Wrong timing: too early (not allowing optimal ripening and a too high water content)	M			*		Rely on refractrometry for assessment of the honey's water content
	13.2 Wrong timing: too late (prompting bees to relocate honey in brood chamber or leading to robbing behaviour)	M	*			*	Rely on refractometry for assessment of the honey's water content
	13.3 Imprudent use of smoker (leading to sensory changes in honey and risk of honey contamination, bee welfare)	S	*	*	*		Limit use of smoker
	13.4 Allowing contact between supers and the ground, or allowing contact of honey with dust (both possibly resulting in honey being contaminated with Clostridium botulinum spores)	VS		*			Do not place supers on the ground or any contaminated surface, ensure careful transportation of honey from apiary to storage room (i.e. cover supers adequately)
14 Beekeeper skills and training	14.1 Not provided or insufficient (preventing operatives from adhering to good practices (i.e. all the above))	VS	*	*	*	*	Provide (theoretical and practical) education; and document
	14.1 Lack of follow-up training (preventing operatives from keeping abreast of latest views)	S	*	*	*	*	Provide continuing education and document Encourage continuous learning and formal assessment of good practice and theoretical understanding as well as the membership of educational beekeeping groups
Notes: VS (very serious), Jeopardises colony survival and/or HS; S (serious), markedly affects health of bee population; M (moderately serious), affects BH moderately and/or affects PE// HQ. * indicate that the identified hazard has an effect on BH, HS, HQ and PE.

Table 2. Bee health (BH) and disease prevention and possible ramifications for unprocessed honey safety and quality – summarised.

	Agent(s)	Principle effects on bees (health)	Prevention/treatment	Potential effects on HS (quality)
Parasites
Varroa mite	V. destructor ^a	Mites feed off bodily fluids, resulting in reduction of bee life expectancy, nervousness, debility of the immune system, Mites possibly carry over viruses^b	Chemical control: – Acrinathrine (Gabon PA92®) – Amitraz (Apivar®, Apiwarol®, Biowar®, Varidol®, Veratraz®) – Coumaphos (Check Mite®, Perizin®) – Cymiazol (Apitol®) – Flumetrin (Bayer flumethrin®, Bayvarol®) – Fluvalinate (Apistan®, Mavrirol®, Gabon PF90®) – Formic acid (Formidol®) – Oxalic acid (Ecoxal®, Oxuvar®) – Thymol (Apiguard®, Apilive var®, Mehpatika solution®, Thymovar®, XY®) Mechanical control, e.g. – Drone brood sacrifice – Powdered sugar dusting – Brood interruption associated with chemicals treatments – Open mesh floors	Improper and untimely use of chemicals during honey production may lead to honey contamination Improper use of chemicals and at high temperatures may result in absconding or brood death
Acarine mites	Acarapis woodii^a	Live and reproduce in bee's trachea, disrupting respiratory functions and introducing viruses	The same treatments as listed for V. destructor; Placing sugar/vegetable shortening mixes (3:1 ratio) on top bars of hives (shortening traces on bees prevent mites from recognising them as young bees) Menthol vaporisation	Improper and untimely use of chemicals during honey production may lead to honey contamination
Wax moth	Galleria mellonella Achroia grisella	Generally infests only weak hives; Moth feeds on wax from brood combs.	Treatment of infested combs with sulphur steam or freezing combs for 24 h (moths thrive at temperatures >30°C) Treating combs off the hive with acetic acid vapour ‘Biological control’ (spraying Bacillus thuringiensis spores B401®)	Improper and untimely use of sulphur or acetic acid may lead to honey contamination
Small hive  beetle	Aethina tumida ^a	Currently not present in the EU At high levels of hives infestation will drive out bee colonies and destroy brood and stored honey	Chemical compounds for application on the ground around the hives: – Benzene hexachloride Permethrin (GardStar®) – Carbaryl – Chlordasol For sanitation of stored combs: – Para dichloro benzene – Acetic acid – Freezing Chemicals to use inside the hive: – Coumaphos (Check Mite®) – Fipronil Natural (plants) compounds: – Thymol – Camphor – Menthol – Eucalypthol Organic acids: – Formic acid (Formidol®) – Oxalic acid (Ecoxal®) – Lactic acid Mechanical trapping using especially designed floors with oil traps, (possibly in combination with the above options).	Improper and untimely use of chemicals during honey production may lead to honey contamination
Tropilaelaps mite	T. clareae ^a T. koenigerum ^a T. mercedesae ^a T. thaii ^a	Currently not present in the EU Mites feed off bodily fluids, reduction of bee life expectancy, nervousness, debility of immune system, possibly carrying over viruses	Chemical control: – Amitraz (Apivar®, Apiwarol®, Biowar®, Varidol®, Veratraz®) – Coumaphos (Check Mite®, Perizin®) – Flumetrin (Bayer flumethrin®, Bayvarol®) – Fluvalinate (Apistan®, Mavrirol®, Gabon PF90®) – Formic acid (Formidol®) – Oxalic acid (Ecoxal®, Oxuvar®) – Thymol (Apiguard®, Apilive var®, Mehpatika solution®, Thymovar®, XY®) Natural compounds (plants): garlic, liquorice, curcuma Mechanical control: brood interruption associated with chemicals treatments. Agent is unable to survive in a broodless colony (e.g. in severe winters)	Improper and untimely use of chemicals during honey production may lead to honey contamination
Bacteria
American foulbrood (AFB)	Paenibacillus larvae spp.^a	Bacteria consume larvae and infection spreads to – and in most cases kills – the colony	Antibiotics (e.g. Oxytetracyclin, Tylosin tartrate and Sulphur drugs); Note that within the EU these substances are NOT registered for use with AFB Beekeeping technique: – shook swarming (i.e. replacing all infected combs of the nest with new ones) or destruction of the family, dependent of the season and the severity of symptoms – Complete burning of infected combs Hive-box disinfection	Illicit (and imprudent) application of antibiotics may lead to residue formation and associated development of antimicrobial resistance. Note that antibiotics are bacteriostats so the infection usually recurs
European Foulbrood (EFB)^a	Melissococcus plutonius, generally in concert with other bacteria: (Paenibacillus alvei, Enterococcus faecalis, Bacillus laterosporus and Achromobacter eurydicae)	‘Opportunistic’disease; agent infests mid gut of infected bee larvae; [Note that in some European countries (e.g. Switzerland) EFB is on the increase]	Antibiotics (e.g. Oxytetracyclin, Tylosin tartrate, Sulphur drugs). Note that in the EU these substances are NOT registered for use except through the cascade procedure for mild infections Beekeeping technique: – shook swarming (i.e. replacement of the all infected combs of the nest with new ones) – in bad cases destruction of the colony and all internal hive parts	Illicit (and imprudent) application of antibiotics may lead to residue formation and associated development of antimicrobial resistance. Note that antibiotics are bacteriostats so the infection usually recurs
Fungi
Microsporidia	Nosema apis Nosema ceranae	Affecting intestinal tracts of adult bees. Symptoms are: – Diarrhoea (N. apis) – Weakness/depopulation and death (N. ceranae and N. apis)	For N. apis and N. ceranae: antibiotics (e.g. fumagillin Fumidil B®); N.B. NOT admitted in the EU except in the UK Requeening Condense the brood nest Give new foundation comb Take care of good fee Ensure apiaries are sited near a wide variety of (especially spring) flora For N. apis: proper apiary exposure (sunny and not too humid) For N. ceranae: unknown	Illicit (and imprudent) application of antibiotics may lead to residue formation and associated development of antimicrobial resistance
Chalkbrood	Ascosphaera apis	Infests guts of larvae and causes death of the larvae Symptoms are chalky deposits (‘mummies’ in cells and on floor of hive)	Improve general hygiene; Proper apiary exposure (sunny and not too humid); Requeening Replace brood combs Natural product: Vita Feed Green®	None
Stonebrood	Aspergillus fumigatus, Aspergillus flavus, Aspergillus niger	Causes mummification of the brood Symptoms are similar to chalk brood but harder ‘mummies’ with greenish tinge	Improve general hygiene; Proper apiary exposure (sunny and not too humid); Requeening Natural product: Vita Feed Green®	None
Viruses
	Main viruses affected bees are: APV, SPV, ArkV, BQCV, BVX, BVY, CBPV, CWV, DWV, EBV, FBV, SBV, IAPV, KBV, Kakugo virus^c	Mainly causing death of bees during their metamorphosis, malformations, reduction of life expectancy	Experimental trials with RNAi Reduction in the number of pests that puncture the exoskeleton of the bee (Varroa, acarine mites, Nosema) reduces the probability of colony loss	None
Other diseases
Chilled brood	Multifactorial; not really a disease, rather series of management flaws	Sudden drop in temperature (e.g. during extended inspection by the beekeeper during winter season by which nurse bees are prevented from clustering on the frame or too few bees to manage the colony in spring)	Open hive on warm days and the hottest part of the day Reduce the number of bees dying in winter by ensuring maximum health of the colony in Autumn	None
Dysentery	Multifactorial	Combination of inability to perform cleansing flights (ambient temperatures too low to allow proper wing muscle functioning) and inadequate food stores (i.e. containing high amount of indigestible matter). Bees are forced to void in the hive Often associated with a Nosema infection	Temperature control (moving hives in-house) Remove honey and replace it by high fructose corn syrup which is practically void of indigestible matter	None
Pesticide losses	Adult bees having collected pollen and nectar from chemically contaminated flowers^d	Some pesticides, when inappropriately applied can be particularly toxic for bees (e.g. neonicotinoids, organophosphates, organoclorurates, pyrethroids, carbamates), cause contaminated pollen and nectar to be introduced and distributed throughout colony and (at too high concentrations) cause bees’ death or severe disorientation disabling them to return to the hive	Proper positioning of hives, staying informed about use of pesticides in immediate surrounding (i.e. at least at 3 kms) of apicultural premises. Correct, timely and approved application of pesticides	Pesticide contamination of honey and other hive products
Colony collapse disorder	Phenomenon poorly understood; multifactorial^d	Worker bees abruptly abandon colony Considered to be a range of problems with varying outcomes	Yet unknown	Pesticide contamination of honey and other hive products
Notes: ^aListed by OIE as communicable diseases (OIE, 2007).
^b Varroa mites carrying viruses have been aetiologically incriminated in colony losses worldwide.
^cAcute bee Paralysis Virus (APV), Slow Paralysis Virus (SPV), Arkansas Virus (ArkV), Black Queen Cell Virus (BQCV), Bee Virus X (BVX), Bee Virus Y (BVY), Chronic Bee Paralysis Virus (CBPV), Cloudy Wing Virus (CWV), Deformed Wing Virus (DWV), Egyptian Bee Virus (EBV), Filamentous Bee Virus (FBV), Sacbrood Virus (SBV), Israel Acute Paralysis Virus (IAPV), Kashmir Bee Virus (KBV), Kakugo virus.
^dPesticides have been primarily incriminated in colony losses. Additional factors have in literature been suggested to contribute aetiologically to colony collapse disorder: (1) environmental stress, (2) malnutrition, (3) pathogens (including the Israel acute paralysis virus), (4) mites, (5) electromagnetic radiation e.g. from cellular phones, (6) genetically modified crops with pest control characteristics such as transgenic maize, (7) poor nutrition due to the use of large areas of monofloral crops.

Both tables substantiate the validity of taking risk management measures. These have been formulated in the current European legislation (EU Regulation 852/2004) which stipulates that the primary food producer is responsible for ensuring that any food put on the market is safe, which includes: (1) ensuring that primary products are protected against contaminations, having regard to any processing that primary products will subsequently undergo, (2) complying with control of hazards in primary production and associated operations, (3) ensuring that staff handling foodstuffs are in good health and undergo training on health risks, (4) taking adequate measures to keep clean any facilities, equipment, containers, crates, vehicles and vessels used, (5) taking account of the results of any relevant analyses carried out on samples taken from animals or other samples that have importance to human health, (6) using veterinary medicinal products correctly, as required by the relevant legislation, (7) taking appropriate remedial action when informed of problems identified during official controls, (8) keeping and retaining records related to measures put in place to control hazards in an appropriate manner and for an appropriate period, commensurate with the nature and size of the food business and to make relevant information contained in these records available to the competent authority and receiving food business operators on request, and, finally, (9) keeping records on veterinary medicinal products or other treatments administered to the animals, dates of administration and withdrawal periods (European Commission 2004c).

GFPs play an important role in controlling potential health hazards (Sperber et al. 1998) and constitute the foundations upon which a further HACCP plan is to be based (NACMCF 1997). They consist of the described series of practical operations and managerial procedures which are indispensable for the healthy functioning of apiaries. Moreover, the adherence to GFPs in beekeeping activities is highly advantageous to apiary performance, as it improves the health of the hives, increases hive production, decreases medicinal costs and yields a healthier and higher quality honey for the consumer market.

3.2. The veterinarian's role in apiculture – good veterinary practices

Both veterinary practitioners and veterinarians in a control function may play a role in apiculture. In some countries the former are involved in such tasks as controlling the health status of bee hives, advising beekeepers on proper treatment options of the various pathologies (possibly involving laboratory analysis), prescribing veterinary medicines, assisting in the introduction of and adherence to bee health and honey safety assurance systems, providing instructions on how to keep records in log books as stipulated in European legislation and in the training of beekeepers in general.

In its recently issued Terrestrial Animal Health Code, the World Organisation for Animal Health (OIE) has indicated that ‘the permanent official sanitary surveillance of apiaries should be under the authority of the Veterinary Authority’ and should be performed by either representatives of this authority or by those of approved organisations [possibly assisted by specially trained ‘health inspectors or advisers’ (e.g. experienced beekeepers)] (OIE 2009). Among the tasks of the official veterinarians possibly involved are, as specifically proposed by OIE and already partly included in European legislation (European Commission 2004b): (1) annual official visits to apiaries during the most appropriate period of detection of diseases and additional (unexpected) visits to apiaries where breeding or transport operations are carried out for trade or transfer to other regions or any other purpose whereby diseases could be spread, as well as to apiaries located in the vicinity, and, finally, special visits for sanitary surveillance to sectors where breeding apiaries have been approved for export purposes, (2) collecting sampling for purposes of diagnosis of contagious diseases and despatching them to an official laboratory for analysis, the results of which are to be communicated to the Veterinary Authority with the shortest delay [notably, the EFSA (http://www.efsa.europa.eu/en/scdocs/doc/27e.pdf, page 29) has identified the absence of specific laboratory facilities as a critical point regarding the efficiency of the systems of monitoring the causes of bee health problems], and, finally, (3) applying hygiene measures comprising in particular the treatment of colonies of bees, as well as disinfection of the equipment and possibly the destruction of affected or suspect colonies and of the contaminated equipment so as to ensure the rapid eradication of any outbreak of a contagious disease. Additional tasks, as laid down in European and national legislation, include official control of records contained in log books (European Commission 2004b), residue control – as per national residue plans – of all hive products (honey, royal jelly, propolis, pollen), examination of imported bees for exotic pests (e.g. Aethina and Tropilaelaps), of transport documents (e.g. those on hive or family movements, new purchases) and possibly the official veterinarian's involvement in the training of beekeeping personnel.

Although the drug resistance to antibiotics is not widely reported (e.g. in Europe) the development of resistance against pharmaceuticals used in apiculture is a major concern. Examples include drug resistance of major bee pathogens such as Paenibacillus larvae spp [notably against tetracyclines in the USA and Canada where – as opposed to Europe – these substances are registered for use in bees (Flores 2007)] or Varroa [e.g. against Amitraz, fluvalinate and coumaphos (Mutinelli and Baggio 2004]. The fact that, consequentially, some pharmaceuticals for treating bee diseases are showing reduced or no therapeutical efficiency has prompted action plans by local authorities to permit the import of pharmacologically active substances not yet registered in the country where they are to be administered. Pending the registration of some of these pharmaceuticals, and/or legislative changes that would allow beekeepers to reach a suitably qualified person (SQP) status permitting them administration of such drugs, veterinary practitioners are called upon to be available to guide this transitional situation, which obviously is restricted to veterinary ‘Prescription Only Medicines’ (POM-V). This ‘cascade principle’ is widely used across Europe (RCVS 2009a, 2009b; VMD 2009)]. In Part 2 of this article a list of drugs currently authorised in the various EU Member States has been included (Formato et al. 2011).

Of particular significance is the prescription and proper administration of suitable veterinary medicines in apicultural practice. Whereas more general definitions of GVPs (i.e. standards specifying both veterinary ethics, principles of conduct and requirements relating to the quality management of veterinary operations) are available, such as those formulated by FVE (2002), their utility has been challenged as they are too unspecific for purposes of ensuring the responsible use of veterinary drugs (FAO 2001). The use of more topical ‘Good Practices in the use of Veterinary Drugs’ (GPVDs as defined in FAO's procedural manual), has in the past already been suggested, e.g. by Van Miert (1990) who defined GFPs as a more drug-use focused concept, namely: ‘the selective use (in accordance with directions of instructions for users) of veterinary drugs registered by the authorities in those indications in which they are permitted when the diagnosis has been established and in which the problem of residues in foods of animal origin on using these agents has been taken into account’.

Residues of veterinary drugs and other (environmental) contaminants in apicultural products have in Europe over the past few years been systematically monitored and reported through the RASFF. It appears from these reports that residues are still an issue in honey (and in many other food products for that matter), particularly, when imported into the EU from Asia (notably China). Also indigenously produced honey still contains these, albeit in markedly fewer samples (European Commission 2009b). Annually an approximate 50 notifications of antibiotics residues are reported for honey, and significantly more of pesticides (e.g. 180 notifications in 2007) (RASFF 2004, 2005, 2006, 2007). The most recent report (RASFF 2008) indicates that nitrofurane (metabolites) still represent the most notified hazard, that sulphonamide residues are found less than before, and that other substances (notably erythromycin) are on the rise. In the 2008 Commission Staff Working Document on the implementation of national residue monitoring plans in the Member States, it is reported that the noncompliant results for antibacterials dominated in honey (DG SANCO 2009).

The legislation on the use of antimicrobial substances in apiculture varies considerably among countries (Mutinelli and Rademacher 2002; Mutinelli 2006). For instance, in the US and Canada antibiotic use is authorised in beekeeping. However – whereas in the EU drugs such as streptomycin, tetracyclines and sulphonamides are regarded as safe for use in farm animals and Maximum Residue Levels (MRLs, i.e. the maximum concentrations of residue considered as not presenting a hazard for the consumer or the manufacturing process) have been set for their occurrence in beef, lamb and pork (often in several hundred ppb) – the EU prohibits the use of antibiotics in apiculture. This is largely explained by the fact that the pharmaceutical industry considers apiculture to be a niche market and consequently has not invested in collecting and submitting data to the European Medicines Evaluation Agency (EMEA) with a view to obtain marketing authorisation (Martin 2003; Mutinelli 2006). Because of their bacteriostatic nature [antibiotics merely temporarily mask the severity of bee diseases caused by microbial pests (American foulbrood, AFB; European Foulbrood, EFB; and nosemosis) rather than eliminate the responsible agents], it is also often argued that it would be wiser to refrain from – instead of trying to regulate (and therefore justify) the use of antibiotics in apiculture. Incidentally, some European Member States apply the cascade principle to permit the use of antibiotics by authorised officers of the competent authorities.

In Directive 96/23/EC there are no MRLs set for honey (European Commission 1996), so the mandatory monitoring programmes for residues in honey as required in this Directive focuses on residues of veterinary medicinal products and environmental contaminants. However, it should be noted that MRLs have now been set for certain plant protection agents in various products (including honey), a summary of which has been listed by DG SANCO (2010). Non compliant levels in honey of the following substances (that have also been used for plant protection) have been reported: streptomycin, pyrethroids, organochlorine compounds and organophosphates (EFSA 2008). In the absence of MRLs and because many third countries use antibiotics in apiculture, the EU has recently (as per (EC) 470/2009) opened the possibility of extrapolating MRLs from one species/commodity to others (including honey) and will hence allow Member States to import honey from third countries, provided so-called ‘Minimum Required Performance Limits’ (MRPLs) that serve as ‘Reference Points for Action’ (RPA, i.e. concentrations technically detectable in a food control laboratory based on decision limits as defined in Commission Decision 2002/657/EC) are not exceeded, certain administrative procedures are followed (possibly including informing Commission services) and defined sampling procedures are complied with (European Commission 2009c). Currently, the only MRPL established is that for Chloramphenicol (0.3 µg/kg) (European Commission 2009c). Several analytical procedures for assessing antimicrobial residue levels in honey have been described in the past few years (e.g. Edder et al. 2002; Ortelli et al. 2004; Martinez Vidal et al. 2009).

However, the prevalence of residues of antimicrobial agents is not an exclusive problem of third countries. For instance, whereas analyses of antimicrobial residues in honey of different origin by Edder et al. (2002) and Reybroeck (2003) indicated that the residue problem is not restricted to a certain geographical area of origin of the honey (except for chloramphenicol exclusively found in honey produced in China) their data also prove that in many, including EU, countries different veterinary products (streptomycins, tetracyclines and sulphonamides) are used and sometimes simultaneously. Incidentally, antimicrobial residues in honey do not appear to be necessarily the result of illegal application in apiculture. For instance, Brasse (2001) reports low concentrations (<20 µg/kg) in fruit honey from nectar collected in pear orchards since the blossoms are sometimes sprayed with streptomycin preparations like Fructosin® or Plantomycin® for the treatment of fire blight (Erwinia amylovora). It has also been suggested that such low concentrations found in honey of African origin (notably from Zambia) are ‘natural’ and result from the natural occurrence of Streptomyces in the environment (Bradbear 2005).

Such and other observations have prompted FAO/WHO's Codex Alimentarius Commission to issue a circular letter requesting information ‘on veterinary drugs registered across the world, to provide data on honey consumption, considering both direct and indirect honey intake, and to also provide information regarding the existence of Good Veterinary Practice (GVP) in honey production’ (FAO/WHO 2009). The European Commission has recently acknowledged that there are indeed hardly if any publications on GVPs applied to beekeeping activities (European Commission 2009a). By this article, the authors hope to have contributed to remedying this situation.

4. Conclusions

Adhering to GFPs in beekeeping represents the foundation upon which bee health assurance and disease prevention should be based and it is a prerequisite for introducing additional risk management measures. European legislation (European Commission 2004a, 2004b) holds the beekeeper primarily accountable for the assurance of the safety of honey and other apicultural products. In their efforts they are supported by consultants, in most European countries including veterinary practitioners, for assisting them in keeping their bee colonies healthy, production efficiency up to standards and for assuring the safety and quality of the raw products supplied to the processing industry. To this end, beekeepers should also be able to rely on veterinarians adhering to more clearly formulated GVPs. It is timely that the veterinary profession recognises the role it should and could play in assuring bee health and honey safety. Consequently, establishments for veterinary education (at least those in countries where apiculture is significant) are well-advised to pay more attention to including in their curricula all relevant elements, so as to prevent their graduates from being rightfully criticised for their relative incompetence in this area of animal production.

Only provided both GFPs and GVPs are respected, are further risk management measures according to a systematically elaborated and implemented HACCP system for primary apicultural production meaningful and effective. The latter will be dealt with in Part 2 of this article (Formato et al. 2011).

Acknowledgements

Dr Jane Richardson (EFSA, Parma, Italy) and Dr Ivor Davis (past President of the British Beekeeping Association) are gratefully acknowledged for their useful comments on this study.