Agricultural production: plan for a sustainable future with honey bees?

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Agricultural production: plan for a sustainable future with honey bees? Robin Crewe and Robin Moritz Social Insects Research Group Department of Zoology and Entomology

Actually a world without honey bees!

Actually we do know what the world looked like without bees

Origins of Bees The early Cretaceous era (145-113 mya) when flowering plants and their associated bees emerged for the first time. Collaboration between evolving flowering plants and early bee species started in the relatively dry regions of Western Gondwana some 120 million years ago

Oldest fossil bee worker stingless bee

Relationship between Fossil bees and contemporary species Vegan ancestral wasp ~40 species ->761 species

Oligocene climates- 34-23 mya cool temperate warm temperat e warm temperate warm temperate ari d ari d ari d tropic al tropic al tropic al ari d ari d warm temperate col d warm temper ate

Types of honey bees Cavity nesting species Open nest species

Honey bee extinction Stars indicate fossil worker bees in amber

Recent radiation of populations

Colony densities per km2 12 Jaffe et al. Cons. Biol 2010

Distribution of Apis cerana

Relationship between Fossil bees and contemporary species Vegan ancestral wasp ~40 species ->761 species

Decline in managed bee colonies?-fao data World Southern Europe Whole Europe Moritz and Erler 2016

Honey production Moritz and Erler 2016

Honey production/colony Moritz and Erler 2016

What is the FAO data NOT telling us? Pollination services do not get measured by national governments-measuring products and not services The number of colonies used in providing pollination services is not recorded. There is no current method for determining what the pollination service deficit will be in the future. Pollination services are a unique national requirement that must be provided locally. Cannot be outsourced!

Provision of Pollination Services Essential for productive industrial agriculture Dependent on reliable supply of managed colonies Dependent on a sustainable source of honey bee colonies

Source of honey bee colonies Either from wild (African, Europe or middle east) or feral populations (Americas, Australia) Influence of beekeepers may be colony multipliers (Europe, North America, Australia/New Zealand) and/or colony harvesters (Africa, Central and South America) Sustainability is dependent on the management of these two kinds of beekeeping strategies

Responsible colony harvesting for industrial farming & rural development Determine the size and fluctuations in the wild population. Variation in relation to climate Determine safe levels of harvesting in various biomes Continuous monitoring of the state of the wild population to adjust harvesting levels.

Estimation of honeybee populations densities Effective population size of social insects is determined by colony density or number of reproductively active queens Finding and counting colonies is very difficult because they are cryptic so alternative estimation methods required Drone trapping through virgin queens and analysis of their offspring. Direct drone trapping with Williams drone traps

KindsTrapping of honey bee colonies William s Trap Drone Wild colonies unmanaged colonies in an area where honey bees are indigenous Managed colonies in apiaries queen breeding Feral colonies colonies escaped from apiaries and living freely 43

South African Biomes

Proposal for a Survey of the South African honey bee populations Get a consortium of the three universities undertaking honey bee research and the ARC to plan and undertaken the work A number of sampling sites in each of the South African biomes will be identified and samples taken 3 times a year for three successive years. The results will provide a rough estimate of the size of the wild honey bee population, its sensitivity to climate variability and its dynamics. Will provide for realistic estimates of the potential for both professional and developmental beekeeping at particular sites.

Acknowledgements

Estimation of honeybee colony Densities using drones & workers Tswalu experiment 47.2 colonies from worker sample 26.5 colonies from drone sample. 5.7 colonies /km2 -drones Sampling area is almost twice as large using workers than drones. Effect of queen mating flights. Both methods suitable for estimating colony densities. Drone trapping gives superior precision. Moritz, Dietemann and Crewe, J. Insect Conservation 12:455-459 (2008).

Temporal variation in colony presence at Ezemvelo Jaffe et al. 2009 Molecular Ecology Temporal dynamics studied in a nature reserve unaffected by the influence of beekeeping activities. 80% of drone contributing queens were replaced in successive 8 month periods. The effect of this high turnover is high genetic diversity, boosting effective population size and hence maintaining genetic diversity.

South African situation Large wild population 10 million colonies, small proportion managed in apiaries Two subspecies Apis mellifera capensis and Apis mellifera scutellata All major honey bee diseases & parasites present Varroa mites Viruses American foulbrood Capensis problem (social parasites)

Kenyan situation Large wild population unknown size, very small proportion managed in apiaries Four subspecies Apis mellifera litorea Apis mellifera scutellata Apis mellifera monticola Apis mellifera yemenitica All major honey bee diseases & parasites present Varroa mites Viruses Nosema

Kenyan situation Muli E, Patch H, Frazier M, Frazier J, Torto B, et al. (2014) PLoS ONE 9(4): e94459.

Key behavioural traits of African Honey bees Migratory swarms resulting from seasonal abundance of food Absconding in response to disease/disturbance Faster generation times and smaller colonies

Drone trapping by queens

Estimation of honeybee colony Densities using Drones http://www.nature.com/scitable/resource?action=showfullim... Figure 1 : Sex determination in hymenoptera. Genotypes and sexual fate under the system of complementary sex determination found in many hymenopteran species (ants, bees, wasps, sawflies). Males derive from unfertilized eggs and have only one sex determination allele (marked by different colored bars). Fertilized eggs with two different sex-determining alleles (heterozygous) develop into females. Diploid males arise from fertilized eggs that are homozygous for the same sex-determining allele. These diploid males arise most commonly under inbreeding conditions in which the father has an allele in common with the mother. 2009 Nature Education All rights reserved.

Estimation of honeybee colony Densities in Germany & SA African populations 12.4 17.6 colonies/ km2 analysis of drones European populations 2.4-3.2 colonies/ km2 analysis of workers 1. Ezemvelo, 2 Leeufontein and 3 Suikerbosrand Mortiz et al. J. Insect Conservation 11, 391-397 (2007)

Temporal variation in colony presence at Evemvelo Jaffe et al. Molecular Ecology 11: 1511-1522 (2009)

Colony losses in South Afrcia Absconding 52% Vandalism 46% Honey badgers & ants 30% Capensis social parasite 26% Fire 28%

Floods Vandalism Veld fires Floods & veldfires Removal of forage trees

Conclusions Beekeepers in South Africa colony losses are largely not attributable to diseases, pesticides or parasites Losses are caused by behaviour of the bees and the actions of beekeepers Absconding which is not a loss to the population of colonies capensis social parasite specific to SA Losses made up from trapping colonies from wild population of honeybees as opposed to breeding of colonies as in Europe.

Future More extensive honeybee surveys across SA to determine colony densities on a finer scale Long term monitoring of these sites to determine the effects of Changes in land utilization Harvesting of honeybee populations by beekeepers Effects of diseases Effects of pesticides

Average percentages of colony losses 50 Scutellata 45 Capensis 40 Overall colony losse s % 35 30 25 20 15 10 5 0 2009/2010 2010/2011 2011/2012 Losses scutellata > capensis 2012/2013

Effect of migrating (2011/2012 2012/2013) 60 Migration Stationary Hobby/SM 50 colony losse s % Commercial 40 30 20 10 0 Scutellata Capensis Overall Significant for A. m. scutellata and for A. m. capensis different responses to queen loss.

Honeybadgers Monkeys

Kinds of honey bee colonies Wild colonies unmanaged colonies in an area where honey bees are indigenous Managed colonies in apiaries queen breeding, management of colonies, pollination Feral colonies colonies escaped from apiaries and living freely.

Potts et al 2010 Status: 2010 Neumann & Carreck 2010

Parasitic Cape honey bee worker in scutellata colony 47

Primary cause of losses Absconding 52% Vandalism 46% Honey badgers & ants 30% Capensis social parasite 26% Fire 28%

Distribution of South African subspecies of honeybees scutellata capensis 49 Vaudo et al. J Insect Cons. 2012

Origin of Cape worker social parasitism 50

Development of a single family of social parasites 51

Effect on colony survival of beekeeping activites 52

Capensis infestation of Colonies 53

Conflict over Reproduction 54

Conflict over Reproduction Complete sterility of workers in eusocial 55 colonies is rare Conflict over reproduction between: Queens & workers Workers for chance to reproduce Workers over rearing of brood Apparent harmony is a consequence of temporary resolution of conflicts When relationships amongst individuals are disturbed then strong conflict emerges

Capensis worker reproduction Workers rarely reproduce in presence of own queens Workers reproduce lay diploid eggs that produce females mainly workers In own colony - leads to laying worker headed colonies In other colonies: capensis self social parasitism scutellata - social parasitism and colony loss 56

COLOSS Network Monitoring Pests & & Diagnosis Pathgens Working Group Monitoring and Diagnosis investigating colony losses Standardised protocol for collecting data - allow for comparisons

Honey Bee Colony Losses Winter 2012-13 Country Losses Algeria Austria Bosnia and Herzegovina Croatia Denmark Estonia Finland Germany Ireland Israel Italy (Veneto region) Latvia Netherlands Norway Poland Scotland Slovakia Sweden 13.45 17.2 6.18 9.52 20.91 25.53 17.02 15.39 37.08 5.9 12.2 19.65 13.71 18.15 18.11 31.06 9.13 22.62 losses 31% (USA) and 34% (UK)

Global perspective Losses remain greater than beekeepers consider acceptable (2013 COLOSS press release) Explanations remain elusive Several possible causative factors: both alone and in combination pesticides, poor nutrition, beekeeping management practices, pests and diseases,

2011/2012 Questionnaire: Colony losses in South Africa Limited knowledge about colony losses Aim of questionnaires to quantify colony losses identify potential causes and threats collect comparable data - standardised protocol

Added for country specific situation Which of the following reasons would you give for your colony losses? How many colonies were lost to this reason? Yes/ No Absconding Bad beekeeping Bad weather / lack of forage/ drought Capensis bees Diseases Fire Honey badger / ants Insecticides / poisoning Pollination stress Small hive beetles Vandalism / theft # Colonies

Diseases and parasites present Varroa Small hive beetle Wax moth European foul brood American foul brood Nosema apis Chalkbrood Viruses

capensis social parasite Remains a major problem in scutellata area problem can be overcome using good beekeeping practices Increasing number of colony losses

Crop effects Reported losses not significantly different from no losses 50 LOSSES (%) 40 30 20 10 0 Yes No

Significantly more colony losses on these crops 60 LOSSES (%) 50 40 30 Yes No 20 10 0 Apples/Cherries Eucalyptus Onions Sunflowers

South African situation Large wild population -14-18 million managed colonies (small proportion) Two subspecies Apis mellifera capensis A. m. scutellata All major honey bee diseases & parasites present Varroa mites American foulbrood Capensis problem

Bad beekeeping practises Unsafe apiary sites

Perceived causes 2009/2011 small hive beetle Varroa Absconding (loss to beekeepers not bee population) chalkbrood Capensis social parasite 2011/2013 Vandalism & Absconding ants Bad weather & honey badger fire Capensis social parasite

Colony losses-south African data? Thousands of colonies 80000 70000 60000 50000 40000 30000 20000 10000 0 Years FAO data SOUTH AFRICA

Trend After 20 years still a major problem in Scutellata areas beekeeping practices to blame problem in the Cape to a lesser degree? Number of colony losses increasing? Catching more infested swarms Is it wise to consider the wild bee population as an inexhaustible resource for restocking?

Average colony losses 35 28.6 30 Losses (%) 25 20 20.6 15 10 5 0 2009/2010 2010/2011 Higher losses with scutellata (29.1%) than capensis (17.9%)

Effect of migrating (combined data) 40 35 35.5 Losses (%) 30 25 20 17.2 15 10 5 0 Migratory beekeepers Stationary beekeepers Only significant for beekeepers using A. m. scutellata, but not A. m. capensis, in their operations

Effect of migrating (2009/2010 2010/2011) Only significant for A. m. scutellata, not for A. m. capensis

Crop effects No significant differences between losses

Losses significantly higher on these crops

Wild honeybees can buffer some losses, but they also make an epidemic disease a serious ecological and economical issue if they came to be threatened

Questionnaire Results will be published in JAR All participants will be updated Information on losses: romee.van.der.zee@beemonitoring.org US http:// beeinformed.org/2013/05/winter-loss-survey-20122013 UK http:// www.bbka.org.uk/files/pressreleases/bbka_release _winter_survival_survey_13_june_2013_1371062171

Questionnaire developed over 3 years 20 countries part of this group All questions well thought through

Fact or fiction? Global decline in honey bee numbers (managed & feral colonies) great concern received attention Exceptional colony losses not unusual Multiple records over 100 years early 1900s Isle of Wight 90% of bees lost 1910 Australia lost 59% of colonies 1915-1917 USA and Canada 2002-2003 Sweden, Germany 2006-2007 USA No definite cause, only speculation An event or part of a cycle of disappearance? RSA loss to beekeepers not bee population

RESULTS Biggest problem is the return rate 2013 data from 19 European countries 15000 beekeepers and 280 000 colonies USA 6,287 beekeepers managing 599,610 colonies, (22.9%) RSA for both seasons 95 beekeepers and 23 355 colonies (4%)

4 35 3 5 3 1 4 27 http://www.southafrica.to/provinces/rsa_by_provinces.jpg