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

Figures & data

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

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).

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.

[OIE] Office International des Épizooties [Internet]. 2007. Listed diseases; [accessed 2009 Dec 6]. Available from: http://www.oie.int/eng/maladies/old_en_classification2007.htm

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