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Home , Beekeeping, Honey bee

Western College of Veterinary Medicine

Honey biology, and bee diseases

Elemir Simko, DVM, Diplomate ACVP Department of Veterinary Pathology

1 2 Western College of Veterinary Medicine

Honey bee biology, beekeepingIn the landand beeof blind diseases one eyed man is Elemir Simko, DVM, Diplomate ACVP Department of kingVeterinary Pathology

3 2019 WCVM research and teaching group 4 WCVM 2018 WCVM2017 5 Acknowledgements

North American Protection Campaign NAPPC

6 National Geographic Survey

https://www.nationalgeographic.com/animals/2019/05/which-animal-species-would-you-save/7

• 900,000 are known/described (70,000 vertebrate species) • Estimated 2M to 30M total species • Largest biomass • 10 quintillion individual insects alive

• 10,000,000,000,000,000,000 insects 7,300,000,000 people

8 Insects

• 900,000 known species • Social insects ~2% – Colonial – > 50% of insect biomass – –

• Cooperative brood care • Overlapping generations

• Reproductive division of labor 9 Bees (Apis spp.)

• Open area -> single comb – Little honey bee, – Giant honey bee, – A. laboriosa, A. andreniformis • Closed cavity dweling – A. koschevnikovi – A. nigrocincta – A. nuluensis – A. cerana indica Managed for honey – A. mellifera production 10 Apis melifera

• A. mellifera scutellata () • A. mellifera caucasica (Caucasian bee) • A. mellifera melifera (Dark bee) • A. mellifera lingustica () • A. mellifera carnica (Carniolan bee)

11 Honey hunter risking life to extract honey from a dangerous cliff-side

15,000 year old painting - Cave of the Spider in 12 Writen evidnec of beekeeping ~3500 BC “The god Re wept, and the tears from his eyes fell on the ground and turned into a bee. The bee made her and busied herself with the flowers of every plant and so was made and also honey

out of the tears of Re.” tomb ~600BC tomb

13 Pabasa’s https://www.pri.org/stories/2015-12-02/what-we-can-learn-ancient-egyptian-practice-beekeeping

c. 1000 BC, -

King David c. 1010-970 BCE https://news.kehila.org/wp King Solomon c. 970–931 BCE 14 content/uploads/2017/09/jst403cl_telrehovapiary_hdv.jpg ~3,000 years later – still fixed farm hives Skep Beekeeping Roman

Stenjevac -

http://www.camaspostrecord.com/ne ws/2018/feb/15/buzzing-about-bees/ 15 skep = a domed hive made of twisted straw

Lorenzo Langstroth (1810–1895)

Hoffman frame Bees space 3/8 inch16 HB lives in hive Langstroth hive: • Frame • Cover • Inner cover • Honey suppers • (optional) • Brood chamber • Screen bottom board (optional) • Bottom board 17 vs Colonies in

Beekeepers Colonies 12,000 750,000 10,000

8,000 700,000

6,000

4,000 650,000

2,000 600,000 0

2011 2012 2013 2014 2015 2016 18 Common beekeeping operation in SK

Common beekeeping operation in SK, MB, AB

– 4 hives per pallet – 10-12 pallets per yard (40-48 hives per yard) – 3-5 miles distance between yards (2 mile radius intense ) – Most commercial operations in SK, MB, AB : 500 - 5000 hives

19 ~3,000 acres

1 mile 1.6 km 20 Thank you

21 Dr. Sarah Wood WCVM Horticulture Research Apiary 22 Honey Bee Diseases - Etiology

• Environmental • Management • Genetic • Infectious etiology – , , fungi, , • Pests • Poisoning (medications, and toxic plants)

23 Honey Bee Diseases - Diagnosis

• Clinical history obtained from the owner and physical examination of the colony are crucial elements in identifying/diagnosing the cause of the problem • Confirmation of the final diagnosis may require ancillary tests.

• Understanding the normal development of a healthy colony of bees – bee biology and beekeeping • Disturbance of normal colony development is an indication that there is a problem 24 Paul Kelly http://www.uoguelph.ca/honeybee/videos.shtml Dr. Keith S. Delaplane https://bee-health.extension.org/honey-bees-and-beekeeping-a- year-in-the-life-of-an-apiary/ 25 1cm 2cm All activities in hive 5 months (winter) 6 weeks (summer) 20,000 21 days Diploid (32 Worker – 80,000 chr ) HoneyBee Castes 1cm 3 months Die after mating 300 24 days Haploid (16 2cm – 1000 chr ) Egg & PheromonesEgg 3 1 16 days Diploid (32 - 5 years 1cm 2cm Queen chr ) 26

http://bit.ly/2kHoGiQ

Development of honey bees

http://www.everythingabout.net/article s/biology/animals/arthropods/insects/d evelopment_of_the_honey_bee.shtml Egg Prepupa

27 The first 21 days of a bee’s life - Anand Varma

https://www.youtube.com/watch?v=6-tqiaPoS2U

28 Reproduction

Swarming - Overcrowded hive - Drawn out queen cups (bottom of the frame) - Old queen will swarm

http://bit.ly/2nLupTr

http://bit.ly/2nbYVte

https://www.mybeeline.co/en/p/swarming-bees- http://bit.ly/2nc6bFM whats-it-all-about-and-why-do-they-do-it 29 15-17km 7.5km 2-3km 50% mating 50% mating Mating trivia - First 2 weeks of life - Mate in flight - Drones die - ~12-17 drones - stored in for life Jensen et al, 2005 30 Commercial queen rearing

Selecting and grafting Growing queens Introducing new queen

http://bit.ly/2oXeaTF

http://bit.ly/2nUZsNE

31 Dr. Ivanna32 Kozii

Overwinter mortality

http://www.capabees.com/shared/2016/07/2017

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Transmission of disease within a colony transmission

• Thousands of bees with biological Horizontal behavior that requires close interaction – Trophallaxis – Direct contact (e.g. spread) – Housekeeping duties (e.g. removal of dead

brood and adult bees, nursing of brood) transmission

• In addition, there are certain pathogens Vertical (e.g. viruses) that can be transmitted from queen to progeny.

34 Transmission of disease between colonies

Natural transmission • drones and workers drifting • foragers from different colonies on same crops • queens mating with infected drones • colony swarming • foragers robbing weak, infected or dead colonies

35 Transmission of disease between colonies

Robbing • Special behavior of foragers that find an unprotected honey that is “robbed” and brought back into their hive • This behavior intensifies at the end of summer when there is ↓ and ↑ foraging bees • Unprotected stores of honey: dead or weak colonies due to various diseases, hence the “robber” bees become contaminated and bring infectious pathogens back to their hives • Extremely important to remove dead-out colonies from the apiary and, if infectious disease is identified, destroy or disinfect equipment (frames, comb, etc.) • Robbing is not restricted to colonies in the same yard, but it can occur anywhere within the ~5 km (flight radius of forager bees) 36 https://beeinformed.org/2011/09/22/houston-we-have-a-problem/ 37 Transmission of disease between colonies

Anthropogenic transmission of diseases • Extremely important! • Contaminated fomites and equipment: beekeepers can spread diseases from hive to hive or yard to yard in same operation • Sale/purchase: Disease outbreaks occur due to the sale/purchase of contaminated equipment or infected bees among beekeepers • Trade: National and international trade of potentially infected bees and products (e.g. packaged honey bees, queens, semen, honey, etc.) -> a major contributor to the global spread of pathogens during the last several decades, in spite of best intensions, strict regulations and high quality inspections. • Migratory beekeeping practices also contribute significantly to transmission of diseases among colonies and dispersal of pathogens over wide geographical areas. 38 http://www.beeculture.com/tag/migratory-beekeeping/ 39 Migratory in USA

• Almonds in – 1.24 M acres = 5K km2 (PEI=55K km2) – 2 week bloom period – 1.7 M hives (85% of USA commercial hives) • in Washington • Sunflowers in South Dacota • , cherries, avocado, blueberry, etc

40 Pollination in Canada

• 75,000 colonies pollinate canola (AB) • 50,000 colonies pollinate blueberries in British Colombia, but 90,000 is needed • 35,000 colonies pollinate blueberries in Atlantic Canada • 15,000 colonies pollinate tree fruit (BC and ON)

41 Beekeeping: Seasonal Cycle

42 Summer

Spring Fall

Winter

43 Honey Bee Diseases

http://www.honeycouncil.ca/images2/pdfs/B MP_manual_-_Les_Eccles_Pub_22920_- http://www.capabees.com/ _FINAL_-_low-res_web_-_English.pdf 44 Disease symptoms

• Adult bee mortality • Dysentery • Paralysis • Wing deformities • Loss of production • Brood appearance

45 Excellent pattern Spotty ‘shotgun’ pattern

46 Differential diagnoses for ‘shotgun’ brood

• Varro • Tracheal mite • • Chalk brood • • European foulbrood • Sacbrood • Failing queen • Inbreeding • Inadequate nutrient supply (spring)

47 Differential diagnoses for ‘shotgun’ brood

• Varro mite • Tracheal mite • Nosema • Chalk brood • American foulbrood • European foulbrood • Sacbrood • Failing queen • Inbreeding • Inadequate nutrient supply (spring)

48 American Foulbrood

49 larvae Gr+ Vegetative and spore forms

https://www.semanticscholar.org/paper/Radiation-inactivation-of-Paenibacillus-larvae- and-Guzman-Cervancia/18ffd32df292051042c6c47107f99c395b4319c8/figure/4 50 AFB Spores

• Survive over 35 years • Withstand –Boiling water – Many disinfectants • Present widespread in many operations

51 American Foulbrood

• The most devastating brood disease of HB • Highly contagious and develop very rapidly resulting in death of colony • Only young larvae (<48hr) are susceptible

Egg Larva Pupa

52 American Foulbrood - Pathogenesis

• Young larvae ingest bacterial spores – Infective dose < 10 spores • Spores germinate in midgut • Proliferation of vegetative bacteria that completely fill the lumen of the gut • Penetration of bacteria through the midgut epithelium • Invasion of the haemocoel – fatal septicemia • Death during late larval or pre-pupal stage 53 American Foulbrood - Pathogenesis

• Initially, infected larva/prepupa turns from a pearly white to brown color • Decay of larval tissue and bacteria generates consistency detectible by ‘ropiness’ test • Desiccation forms a dry, dark brown “scale” – Each scale contains in excess of 2 billion spores – Spores are infective for decades (like Anthrax)

54 "Spotty" brood pattern

Spotty brood pattern Healthy brood pattern

http://www.afb.org.nz/visual-symptoms-of55-afb Normal stages

Egg Young larva Old larva Old larva being capped

Pre-pupa Young pupa Old pupa Imago

http://www.afb.org.nz/identifying-scale 56

Holes in cell cappings normal vs. AFB

Normal

scale -

Cell capping in being sealed Healthy cell capping Hole in capping -> emerging bee AFB

57 - Dark sunken cell capping AFB - cell capping with a hole chewed in it http://www.afb.org.nz/identifying Normal stages vs AFB

Pre-pupa Young pupa Old pupa Imago

Normal AFB

Pre-pupa Young pupa Scales Pupal scale http://www.afb.org.nz/identifying-scale w. proboscis58 Ropiness test of American foulbrood

‘Ropiness’ test

http://www.afb.org.nz/visual-symptoms-of59-afb Identifying scale of American foulbrood

http://www.afb.org.nz/visual-symptoms-of-afb

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bee predators bees/nggallery/honey bee diseases/page/1/image/american pupal

https://agdev.anr.udel.edu/maarec/honey 60

http://www.moraybeedino saurs.co.uk/diseases.html AFB – Lab diagnosis

• Sample suspected cells with swab or cut out a comb (20x20 cm) containing the infected cells • Send samples on ice-pack to lab: e.g. The National Bee Diagnostic Centre, Beaverlodge, AB https://www.thenbdc.ca/about-us-0

61 AFB – Definitive diagnosis

• Demonstration of disease in hive – affected prepupae and pupae, scales, etc • Demonstration of pathogen by microbiological test (culture of PCR)

62 AFB – Lab diagnosis

• Demonstration of disease in hive – affected prepupae and pupae • Demonstration of pathogen by microbiological test

Nota bene: Many colonies can be found to contain spores but not diseased larvae or pupae These colonies are considered to bee contaminated by AFB spores but not affected by AFB disease

63 Blackleg in cattle

http://www.umthunywa.co.zw/wp-content/uploads/2016/03/black-leg.jpg

Diagnosis: - Lesions - Pathogen: - C. chauvoei 64 AFB – Therapy and Prevention (Integrated Management)

• – Exclude contaminated feed (honey) and equipment – Do not introduce comb/frames in apiary – During dearth discourages robbing (provide feed) • Regular replacement of brood frames with new frames (brood frame cycles of 3-5 yrs – recommended) • Genetic selection for improved resistance to AFB – Re-queening with hygienic behavior genetics • Monitoring and early detection

65 AFB – Therapy and Prevention (Integrated Pest Management)

• Eradication: – AFB-infected colonies and equipment are burned – Radiation could also be considered – This is the only option in some EU counties • Anything less than above is only control and prevention but not eradication

66 AFB – Therapy and Prevention (Integrated Pest Management)

Chemical control in Canada and the USA • Antibiotics in honey bees are permissible for metaphylaxis • AB reduced the threat of AFB for several decades – We became over-dependent on ABs • AB do not kill AFB spores, but prevent the growth and multiplication of the vegetative form of the bacteria • Oxytetracycline used for metaphylaxis [mix 3.5 kg powder shugar with 454g OXY (55mg/g) and give 32g/colony 3 times (4-5 day apart) during spring and fall] • 4-week withdrawal period before honey flow 67 Administration of therapy – AB + powder sugar

mussel

68 AFB – Therapy and Prevention (Integrated Pest Management)

• Some strains of P. larvae became resistant (rAFB) to oxytetracycline • For r-AFB, tylosin (Tylan Soluble®) can be administered in Canada and the USA – Greater potential for tylosin residues to carry-over into honey than with OXY – 4-week withdrawal period before honey flow • Lincomycin was recently registered for bees in Canada

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- predators 70https://agdev.anr.udel.edu/maarec/honey European Foulbrood

• Melissococcus plutonius (M. pluton and Strep pluton) • Brood disease as AFB, but usually not fatal • Self-limiting disease – Usually apparent shortly after a strong nectar flow • High proportion of larvae to nursing bees • Larval starvation – bacteria in GIT compete for nutrition – Followed by spontaneous recovery as the nectar flow continues, if the colony is full-sized and the level of disease is low to moderate

71 EFB - Diagnosis

• Healthy larvae are pearly-white and curled in a “C” shape • Early stages EFB-killed larvae: – “C” shape or occ. twisted, but yellow in color – Visible white tracheal system – Chalky-white midgut from bacteria – EFB-killed larvae are rarely capped (unlike AFB) – Do not readily rope

72 EFB – brown brood color

http://mastersons.net/beekeeping/beekeeping_info/diseases-parasites-and-pests/

73 http://articles.extension.org/pages/23693/european-foulbrood:-a-bacterial-disease-affecting-honey-bee-brood EFB – Lab Diagnosis by culture

• Sampling for laboratory diagnosis – important to include live larvae, newly-killed larvae and scale • Only the live infected larvae will contain pure M. plutonius bacterial culture • Dead larvae, in contrast, contain a confusing array of secondary bacteria that can make a definitive diagnosis challenging

74 https://beeinformed.org/2013/04/05/europea n-foulbrood-efb-identification/

M. Plutonius with Melissococcus plutonius secondary bacteria

75 AFB vs EFB

AFB EFB Death After capping Before capping Dead larva, scale Fat brown scale along lower “C”-shaped scale at base of sides of the cells cell or corkscrew-shaped from base to opening of cell Removal of scale Difficult - fragile Easy - rubbery Cappings Perforated with small holes, Uncapped sunken and greasy Smell Putrid “fish-like” odour May smell ‘sour’ due to secondary bacteria ‘Ropiness’ test Positive Negative – unless due to secondary bacteria -> “pseudoropines” Outcome Fatal – colony dies Usually self-limitting

76 EFB – Therapy and Prevention (Integrated Pest Management)

• Management - prevent inadequate larval feeding – Provide feed during shortage or moving • Regular replacement of brood frames with new frames (brood frame cycles of 3-5 yrs – recommended) • Genetic selection for improving resistance to EFB – Re-queening with hygienic behavior genetics • Physical – ‘Shaking’ technique – Weak EFB colonies with > 50% of dead larvae should

be burned 77 EFB – Therapy and Prevention (Integrated Pest Management)

• Chemical treatment with OXY is effective • Preventive treatment with OXY of AFB controls also EFB • Tylosin is not effective against EFB

78

• Microsporidia receive little attention in veterinary medical curriculum • Parasites of rabbits and fish • Severe disease and death in immunocompromised humans

79 Encephalitozoon cuniculi

80 Microsporidia in bees - Nosema

• Disease of adult bees usually associated with stress • Oral-fecal infection – epithelial cells of midgut are affected resulting in dysentery

81 Nosema

• N. apis - important parasite in temperate climates – Long winters and few cleansing flight opportunities • N. ceranae – jumped from Asian honey bee ( into Apis mellifera) – Present in Canada but reported to cause bigger problems in regions with warmer climates – It seems that N. ceranae is spreding and replacing N. apis also in Canada – More studies are needed

82 Nosemosis

• Infected colonies – Poor winter survival – Poor build up in spring – Diarrhea – Hypopharyngeal glands -> reduced brood food – Queen supersedure <- reduced feeding by nurse bees – Reduced nectar and collection

83

Nosemosis - Dysentery

http://kanat.jsc.vsc.edu/stud ent/lees/maincontent.htm

http://mainebeekeepers.org/information- for-beekeepers/when-disaster-strikes/

https://lookfordiagnosis.com/mesh_in fo.php?term=nosema&lang=1 84 Nosema – Diagnosis Determination of # of spores by haemocytometer > 1M spores per bee -> clinically significant

85 N. apis – Therapy and Prevention (Integrated Pest Management)

• Overwintering hives – strong populations – vigorous queens – adequate food (pollen and sugar syrup or honey) – well insulated facing south to promote cleansing flights – Supplemental feeding with high quality feed in spring • Regular replacement of brood frames with new frames (brood frame cycles of 3-5 yrs – recommended)

86 N. apis – Therapy and Prevention (Integrated Pest Management)

• Antibiotic treatment is recommended if infection exceeds 1 million of spores per bee • Fumagillin - B – remains to be an over-counter drug – No effect on spores but suppresses fungal growth – Administered in sugar syrup (avoid heat and UV light)

87 PARASITIC MITES

• ~ 100 non-parasitic harmless species of mites – feed on detritus, pollen or hive products • 3 parasitic mites cause major economic loses – destructor • 1987 – came to North America – Tracheal mite () • 1984 found in the USA – spread by migratory beekeepers – Tropilaelaps mite (Tropilaelaps spp.) in .

88 Varroa

89 Varroa

• 1904 V. jacobsoni identified on A. cerana • ~1940 V. destructor infected A. mellifera • 1970’s – 1980’s – • 1987 – came to North America • 1995 – entire North America except Newfoundland • 2000 - • is without Varroa

90 Varroa - Life Cycle

Phoretic stage • Adult female mite is attached to adult bees and feed between abdominal segments • During winter, almost all Varroa mites are in phoretic stage, because there is little brood

Reproductive stage • Female moves into brood cell to reproduce • When brood is abundant, 70-80% of the mites are in brood cells. 91 92 Clinical signs of varroosis

• Spotty brood • Weak colony • Secondary infections • Poor production • Colony collapse and loss due to direct action of mites, viruses and other diseases secondary to immunosuppression

93 Damaged brood in collapsing colony

due to Varroa

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94 Varroa - Diagnosis

• Examination of: – Debris – screened bottom board – Brood – esp. drone – Sample of adult bees • The above exams will indicate positive or negative – Presence or absence – not very useful – All hives in Canada except Newfoundland are: positive • It is a parasitic disease! • Number of parasites needed to determine clinical significance (Haemonchosis , Coccidiosis etc) 95 Quantitative diagnosis

• Mite infestation rate - determine % of infestation – Alcohol Varroa wash – Sticky bottom boards used to correlate natural mite fall (NMF) with infestation rate

96 Determination of the level of infestation Varroa drop Varroa wash

97 Varroa Thresholds and Therapy “Rule of Thumb” •Less than 1% O.K. •More than 3% therapy needed (unless it is “phoretic season”) •1-3% depends on timing

98 Control of Varroa (Integrated Pest Management)

• Impossible to eradicate • Objective is to lower Varroa below economic risk threshold • Strong colonies -> limit robbing and drifting • Genetic selection • Biological/mechanical control • Chemical treatment: – Synthetic chemicals – Natural organic acids

– Essential oils 99 Varroa – Therapy and Prevention (Integrated Pest Management)

Synthetic chemicals/medications Chemical class Chemical name Trade name Pyrethroid Fluvalinate Apistan® Bayvarol®

Organo- phosphate Coumaphos CheckMite+, Perizin®

Amadine Amitraz Apivar® Pyrazole “METl” Fenpyroximate Hivastan TM acaricides

100 Varroa – Therapy and Prevention (Integrated Pest Management)

Synthetic chemicals/medications Chemical class Chemical name Trade name Pyrethroid Fluvalinate Apistan® Bayvarol®

Organo- phosphate Coumaphos CheckMite+, Perizin®

Amadine Amitraz Apivar® Pyrazole “METl” Fenpyroximate Hivastan TM acaricides

101 Effective lives of synthetic miticides in North America

Coumaphos

Modified from http://scientificbeekeeping.com/the-varroa-problem-part-1/

102 Varroa – Therapy and Prevention (Integrated Pest Management)

Organic Acids Formic Acid 65%Formic Acid, MAQS Oxalic Acid Mite Wipes Lactic Acid Mite Away Hop Beta Acid Lactic acid Hop Guard TM

Essential Oils Thymol Thymovar® Apiguard® Menthol Eucalyptol Eucalyptol Wintergreen Camphor Wintergreen Camphor

103 CCD –

• Pesticides? • Pathogens? • Environment? • Reduced genetic variabitlity? • Multifactorial? – most likely

Marla Spivak: Why bees are disappearing

https://www.youtube.com/watch?v=dY7iATJVCso

104 http://scientificbeekeeping.com/the-varroa-problem-part-1/

105 Will honey bees be extinct?

Most likely not in foreseeable future.

However, the current North American commercial beekeeping practices may be extinct in the near future. If this happens, commercial pollination services will be compromised severely. 106 Three quarters of the leading global food crops and one third of the total global production volume are dependent upon animal pollination [Klein 2007]. Animal-pollinated crops contribute the majority of the available essential micronutrients (e.g. dietary vitamin A, C, and E, and a large portion of the minerals) to the human diet; accordingly, micronutrient deficiencies together with overall decrease of food availability could have a potentially drastic effect on human nutrition and public health if animal pollination is jeopardized [Eilers 2011, Chaplin-Kramer 2014].

107 The WCVM Honey Bee Lab 2018

Dr. Sarah Wood Jocelyne Chalifour Dr. Ivana Kozii Sarah Barnsley Dr. Roman Koziy Crystani Folkes Dr. Ihor Dvylyuk Roney Silva Dr. Ihor Moshynskyy Leland Guillemin Dr. Colby Klein Claudia Olivas Dr. Igor Medici De Matos Esther Derksen Dr. Zabrodski Dr. Claire J. Rensburg Dr. Mohsen Sharafi Dr. Maddy Friesen 108 Questions?

109 Deformed wing Overview • First identified: https://goo.gl/tG5z1g • Japanese , 1991 • Prevalence • Up to 100% world wide • Developmental stages affected • Egg, larvae, pupae, adults • Vector • Varroa mites

110 Chalkbrood

• Stress-related fungal disease <- Ascophaera apis • Infects honey bee larvae and occ. pupae • Common but usually does not cause significant losses unless there are: – right conditions – stressed colonies • Easy identification • Chalkbrood spores can remain viable for years • Chemical Control – none in Canada and USA

111 Chockbrood – Therapy and Prevention (Integrated Pest Management)

• Management – prevent adverse hive conditions (cooling and moisture) – Strengthen weak colonies – control other diseases or parasites (e.g. Varroa) – Burn combs containing many chalkbrood mummies • Genetic selection for hygienic behaviors • Regular replacement of brood frames with new frames (brood frame cycles of 3-5 yrs – recommended) • Chemical Control – none in Canada and USA

112 Chalkbrood

http://www.sabio.org.za/?page_id=14 http://www.omafra.gov.on.c a/english/food/inspection/b ees/chalkbrood.htm113 Choakbrood

http://www.omafra.gov.on.ca/english/food/inspection/bees/chalkbrood.htm 114 Varroa – Therapy and Prevention (Integrated Pest Management)

• Genetic selection for improving resistance to Varroa • Hygienic behavior • Grooming behavior • Interrupting the reproduction of mites • Removal and freezing of capped drone brood • Screened bottom boards

115 Better color graph

116

Hygienic behavior 80

https://beeinformed.org/author/katie- 117 lee/page/5/ Varroa – Therapy and Prevention (Integrated Pest Management)

• Genetic selection for improving resistance to Varroa • Hygienic behavior • Grooming behavior

• 1:30 to 5:30 https://www.youtube.com/watch?v=xSGa9DKraGA&ebc=ANyPxKo1wQImwTvJwU qzzGaDB8RmC4GPRqb6YZD4WSOP41FqUU-8nb5L6- 9v7pOc0y3coIsApV3ld1a4qvxGevLqyk8Yn0mlTA

118 Destruction of drone brood

https://beeinformed.org/author/katie- 119 lee/page/5/ Baers etc

120