- Determining the Causes - Dr. Diana Cox-Foster Pennsylvania State University

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1 Colony Collapse Disorder - Determining the Causes - Dr. Diana Cox-Foster Pennsylvania State University

2 Honey Bees in US Agriculture and the Colony Collapse Disorder Essential for pollination of over 100 fruit and vegetable crops in the United States Valued at more than $14.6 billion in the U.S. Varroa mites have resulted in a major decrease in managed colonies in last 18 yrs Recent increased death of colonies -- termed Colony Collapse Disorder (CCD)) CCD affects an estimated 1/4 of all US beekeepers, causing 35 to 100% loss of colonies in operations

3 Symptoms of CCD Rapid decline in number of adult bees Queens present with a few young adult bees, lots of larvae/pupae, and abundant food resources No dead adult bees in or outside the colony No robbing by other bees or invasion by pest insects, suggesting presence of a toxin Infection by an extremely large number of different disease organisms in each adult

4 CCD HEALTHY

5 CCD Working Group Goals Identify potential causal factors common to CCD colonies and not associated with strong, healthy bee colonies Determine how these factors can underlie CCD, by experimentally reproducing CCD symptoms Devise preventative measures to disrupt CCD and ensure strong colonies for pollination

6 Preliminary Work on CCD Description of CCD symptoms Examine known pathogens and parasites Document hive conditions Surveys of Beekeepers Collection of samples from both CCD and non-ccd beekeeping operations Agreement to extensively share samples and data

7 What are the known pathogens of honey bees?

8 Danger, danger, lurking everywhere---

9 A bee s encounter with pathogens and parasites Varroa mites Fungal spores Viruses Nosema Bacteria FOOD Tracheal mites

10 Insect Immunity to Pathogens and Wounding Wounding and melanotic encapsulation Midgut Enzymes and antimicrobial peptides Fat Body Ovary Saliva (glucose oxidase) Hemolymph and blood cells

11 Varroa mite parasitizes the developing pupa and reproduces in the brood cell.

12 How do mites impact honeybee health? Increased incidence of diseases following mite introduction Suppress the immune system of bees, even after removal Infected by some bee viruses Vector viruses

13 Increased incidence of chalkbrood fungal disease in PA following varroa introduction Dennis VanEnglesdorp, State Bee Inspector, October 2005

14 Mites affect specific aspects of honeybee immunity Cellular immunity Lack of key enzyme at adult emergence Decreased enzymes needed for killing reaction Increased cell reaction Antimicrobial reaction Decreased production of antimicrobial peptides

15 Viruses and Varroa--- Role in honey bee disease and colony health???? 18 honey bee viruses Most are picornalike viruses Sacbrood bee virus (SBV) Deformed wing virus (DWV) Kashmir bee virus (KBV) Black queen cell virus (BQCV) Acute bee paralysis virus (ABPV)

16 Bee viruses can be latent or persistent and not cause visible symptoms, as seen with deformed wing virus. No mites, normal wings Mites, normal wings Mites, deformed wings Degree of Wing Deformity Y = * X R 2 = Number of Mites with Bee during Development

17 Deformed-winged bees: A combination of mites and microbial interaction to produce high viral levels? DWV RNA relative to Actin mrna E-3 No injection Saline E. coli Saline E. coli Saline E. coli Without mites, Normal Wings With mites, Normal Wings With mites, Deformed Wings

18 Hypothesized interactions- Varroa mites Immune Normal defenses colonies to without bacteria mites are are decreased able to maintain due to immunosuppression immune defenses by mite to bacteria. feeding Bacteria Viruses replicate Viruses following like DWV, mite SBV, and parasitization. KBV may established Through a an persistent unknown infection, mechanism, that may microbe in the case exposure of DWV triggers be positively a large selected increase by in DWV the in bee. particular. Viruses- DWV, SBV and KBV

19 Percent DWV Hive Hive Hive Hive16 13 w 13 d 13 e 14 w 14 d 14 e 15 w 15 d 15 e 16 w 16 d 16 e Virus prevalence increases during the summer, when mites are not controlled Hive (Day of year) 17 w 17 d 17 e Workers Drones Eggs

20 EVIDENCE OF TRANSMISSION ROUTES Queen Bee Eggs Honey, royal jelly, or bee bread Brood food Larvae Pupae TO OTHER COLONIES VIA CONTAMINATED EQUIPMENT (OR HONEY)? Workers Sperm, Seminal fluid Drones Varroa Mites TO OTHER COLONIES?

21 How does the combination of mites and chemical stress impact viruses in honey bees?

22 Date Treatment date Coumaphos Mite Drop / Day Threshold - 50 mites/day Formic Pad WV Fume Board Untreated

23 % BQCV Infection Airport Apiary 0 Week 2 Week 10 Week Chemical mite controls differentially affect viral infections-- Suppression of DWV versus Activation of BQCV 0 Untreated WV Fume Board Formic Pad Coumaphos

24 What type of pathogens do we know CCD bees have?

25 Photo by Dennis vanengelsdorp

26 Photo by Dennis vanengelsdorp

27 Working Hypotheses for potential causes of CCD Are new or reemerging pathogens responsible for CCD? Are environmental chemicals impacting bees and triggering CCD? Is a combination of stresses weakening bee colonies and allowing stressrelated pathogens to cause final collapse?

28 Breeding New Genetic Strains of Honey Bees Need for increased genetic resistance to diseases and the impacts of parasites

29 Do we need to be worried about the causal agents of CCD impacting other insect pollinators?

30 SBV DWV HIVE 5 HIVE 46 A B C A B C A single cell of bee bread can have virus present Other Bee Bread Cells w/ DWV HIVE 5 HIVE 46 HIVE 43 in single layers of different colored pollen Hive(Chi Square 1.493, p = ); Color of Pollen (Chi Square=1.452,p = )

31 DWV is NOT associated with a particular color of pollen 50 Percent DWV Black/Brown Brown Light brown Yellow Pollen Color Color of Pollen (Chi Square=1.452,p = )

32 When is the pollen becoming contaminated by the bee viruses?

33 Honey bee viruses --- pollen vs. pollen foragers Pollen DWV SBV DWV- H/Th1 Pollen baskets collected with pollen foragers; foragers either immediately frozen or held 24 hrs with food/h 2 O RNA extracted from pollen and foragers separated into Head/Th1 and Th2,3/Abdomen; RT-PCR performed for DWV, SBV, actin Pollen Foragers DWV- Th/Ab SBV- H/Th1 SBV- Th/Ab Actin- H/Th1 Actin- Th/Ab Retained 24hrs 0 hrs Pollen- DWV 5/12 positive 3/5 from DWV- foragers SBV 11/12 positive Foragers W/positive pollen 0/12 with DWV infection associated with salivary glands (SG) in H/Th1 sample 1/12 with SBV assoc. with SG W/O positive pollen Lack of DWV in pollen of heavily infected H/Th1 of forager

34 Transmission of viruses among pollinators??? Apis mellifera Flowering Plants?? Queen Bee Honey (royal jelly or bee Brood bread) food Eggs Larvae Pupae Bombus or other pollinators Worke rs (Seminal fluid?) Drone s Varroa Mites

35 Deformed wing virus in bumblebees -- can it be acquired from honey bees? Genersch E., Yue C., Fries I., and de Miranda J.R. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. Journal of Invertebrate Pathology 91 (2006) 61 63

36 Penn State University Colony Collapse Disorder Working Group Pennsylvania Department of Agriculture USDA-ARS, Bee Research Laboratory, Beltsville, MD Columbia University and Northeast Biodefense Center Florida Department of Agriculture and Consumer Services North Carolina State University University of Illinois, Champaign-Urbana University of Delaware Additional Research Bee Alert Technologies, Inc., Montana and affiliates

37 Summary Extensive collaboration among researchers of diverse expertises and affiliations Federal, State, and Land-Grant University research targeting real-world problems Cooperative Extension providing the bridge between the research community and the beekeepers and those dependent on pollination Challenges in unraveling the causes of CCD Critical need for prevention to ensure the health of bees (and all insect pollinators) and the pollination industry

38 Questions?