sign in sign up
<<
Home , African bee, Varroa destructor

IN AFRICA – A SERIOUS THREAT

Mike Allsopp

ARC-Plant Protection Research Institute, Private Bag X5017, Stellenbosch 7599, South Africa. Tel: ++27 21 8874690; Fax: ++27 21 8875096; Email: [email protected]

INTRODUCTION

The most serious pest or disease of honeybees in the 20th century has undoubtedly been the ectoparasitic , (formerly ). Relatively harmless on its natural host, the Eastern honeybee , the varroa mite has recently crossed onto the Western honeybee Apis mellifera and spread from its Asian origins throughout most of the world. On the commercially important Apis mellifera the varroa mite is no longer a relatively benign pest, and the result in most cases is the death of the honeybee colony. In regions of the world where the varroa mite is well established, such as Europe and the USA, wild honeybee populations have all but disappeared as a result of varroa mortality (Krause & Page 1995; Finley et al. 1996) and commercial is only possible with the liberal use of anti-varroa pesticides.

Varroa destructor was first found in South Africa in August 1997 (Allsopp et al. 1997), the first report of this mite in sub-Saharan Africa. An immediate survey revealed that the mite was common and widespread in both commercial and wild honeybee populations in the Western Cape, but absent from the rest of the country. The South African National Department of Agriculture immediately convened a workshop during which it was concluded, on the basis on international evidence, that there was no prospect of containing the spread of the mite, nor was there a biocontrol agent available that could be used to eliminate varroa. It was accepted that varroa would eventually spread throughout South Africa, and probably throughout sub-Saharan Africa. The time span for this spread in South Africa was estimated to be between 2-7 years (de Jong et al. 1982), with rapid spread in areas of commercial beekeeping activity and more gradual spread elsewhere.

What was less certain is what effect the varroa mite would have on the honeybees of Africa. It is known that the virulence and effect of the mite is significantly affected by environmental factors (Moretto et al. 1991; Marcangeli et al. 1992), and there were also other variables to consider. Most important was the general belief (Medina 1998; Erickson et al. 1998; but see Page 1998) that African honeybees would be tolerant to the varroa mite, and that varroa would have little impact on the of Africa. Recent evidence suggests that at least three different aspects should be considered when estimating the impact of the varroa mite on African honeybees.

1. The general belief that African honeybees, perhaps by virtue of their short post-capping time in brood development which could result in large numbers of unfertilized daughter , their hygienic behaviour (Moretto et al. 1991), and their defensiveness (Moretto et al. 1991), would prevent varroa from increasing to dangerous levels in the colonies, and hence would be tolerant to the presence of the mite. Support for this view comes from data from North Africa where varroa has seemingly been of little importance (Ducos de Lahitte et al. 1998), from Brazil where varroa has not been destructive in Africanized bees (Moretto et al. 1991; Rosenkranz & Engels 1994), and from early work with Cape honeybees (Apis mellifera capensis) which suggested that these bees

Proceedings of the 37th International Apicultural Congress, 28 October – 1 November 2001, Durban, South Africa APIMONDIA 2001 To be referenced as: Proc. 37th Int. Apic. Congr., 28 Oct – 1 Nov 2001, Durban, South Africa ISBN: 0-620-27768-8 Produced by: Document Transformation Technologies Organised by: Conference Planners would be tolerant to varroa (Moritz & Jordan 1992). This view would predict that varroa would spread throughout the African honeybee population, but would be little more than an additional arbitrary pest present in the colonies.

2. It has also been suggested that what has made the Africanized honeybees of tolerant to the varroa mite is not some behavioural attribute of these bees, but rather that there are a number of different species and populations of mite (Anderson 2000), and that the one present in South America is not particularly virulent. This view predicts that if the more virulent strain of mite is present in South Africa, then it will result in the type of destruction witnessed in North America and Europe.

3. A third possibility to consider is that not only are the race of honeybee and the strain of varroa mite important in predicting the outcome of honeybee-mite interactions, but also what viruses are present in the honeybee population (Ball 1997; Bowen-Walker et al. 1998). There is considerable evidence that colonies infected with varroa eventually collapse as a result of secondary infections, and of these, viruses activated by the presence of the mites are most important. The outcome of this scenario is impossible to predict as nothing is known about the honeybee viruses of South Africa.

In both of the last two scenarios it would be predicted that resistance or tolerance in the honeybee population would develop, but only after the collapse of the majority of the population. In such a case the resistance developed could potentially be masked by the use of chemical treatment by beekeepers to sustain susceptible colonies and the resistance might not be expected to spread through the population.

Although it remains to be determined what effect the mite will have on honeybee populations of Africa, the threat was considered to be sufficient to establish a Varroa Working Group comprising of researchers, beekeepers, users of honeybee , and Department of Agriculture officials. This Working Group instituted a Varroa Research Programme to monitor and investigate the mite in South Africa, the preliminary results of which are presented here.

VARROA RESEARCH PROGRAMME

Value of honeybees in South Africa

The value added to crop production by the commercial pollination of honeybees has been estimated to be in the order of R3.2 billion per annum (Table 1). It is also worth noting that this agricultural output sustains some 250 000 jobs. However, and in contrast to the Americas, perhaps the greatest threat of varroa in Africa is to the wild honeybee populations that pollinate as many as 40-70% of indigenous flowering plants. Should South Africa and the rest of Africa suffer the loss of wild bees witnessed in other parts of the world, this could have significant implications for floral conservation and biodiversity.

Source of the varroa

It has been found that the varroa mite, Varroa jacobsoni, that has caused devastation to honeybee populations almost throughout the world for the past thirty years is not a single species, but rather a species complex, consisting of at least 18 types of mite (Anderson 2000). Of these different types and species, only two are able to reproduce on Apis mellifera, and only one, the Korean-Russian type, is responsible for the extreme damage as seen in Europe and the USA (Anderson 2000). This species has been called Varroa destructor, and this is the type found in South Africa (Anderson 2000). Table 1: Estimated value of honeybees in commercial crop pollination in South Africa

Annual Annual Honeybee added Crop Hectares production value value (tons) (R million) (R million)

Deciduous fruit 171 630 2 358 106 3 716.64 1 296.52

Berries 750 4 682 21.82 8.16

Nuts 14 500 6 565 43.90 11.58

Tropical Fruit 114 509 1 391 154 2 103.45 672.70

Grain crops 322 600 402 840 594.96 86.08

Oilseed crops 845 000 1 133 477 969.67 523.80

Vegetables 48 300 892 907 1 172.26 293.95

Seed production ? ? 127.69 102.15

Other ? ? 1 019.85 210.30

TOTALS 1 517 289 7 707 020 9 770.24 3 205.24

Distribution

In 1997 the varroa mite was to be found only in the Western Cape, but as expected the mite has spread rapidly throughout South Africa, almost entirely as a result of migratory beekeeping activities, and is now present in commercial honeybee colonies in all regions. Varroa mites have also spread into the wild honeybee population, including the Kruger National Park, Cape Peninsular National Park, Tsitsikamma National Park and the Cedarberg.

Impact of varroa

The comprehensive monitoring of mite levels and colony condition in >300 commercial colonies belonging to Cape beekeepers indicates that varroa numbers are strongly negatively correlated with colony size, brood production, and pollen storage (Pearson Correlation Coefficients; p = 0.0001) Hence, as varroa numbers in a colony increase, the colony weakens, and often dies.

There is, however, no clear-cut relationship between varroa infestation rate and colony mortality. Many colonies severely infested with varroa mites have not died during the course of the study, and it is still not known how acutely the mites will impact on the honeybee population of South Africa. Comparisons between varroacide-treated and non- treated colonies, however, indicate massive differences in colony survival and productivity, in at least some situations (Table 2).

Table 2: Comparison between varroacide-treated and control colonies in the Western Cape and Kwazulu-Natal (KZN)

Treatment Colonies Control Colonies

Original Surviving Average Original Surviving Average number of colonies number of colonies honey colonies after 6 production colonies after 6 production months in months in surviving surviving colonies colonies

Western 22 21 13.6kg 20 7 2.8kg Cape

KZN 14 13 22.9kg 10 0 0.0kg

In colonies that have not succumbed to the mite in the short-term, tremendous (as much as 95%) levels of brood mortality are being found, resulting in the gradual collapse of these colonies. In the early stages of varroa infestation in a region, colonies with as many as 50 phoretic mites per 100 bees are not uncommon. This represents some 30 000 mites in large colonies, and clearly indicates that the prediction of scenario 1 (above), that certain behavioural attributes of African honeybees would limit varroa population growth in African honeybee colonies, is not taking place. However, after three years of varroa mites having been present in a region, mite numbers are greatly reduced. Whether this is because of mite-tolerance developing in the bees, or because the colonies are too weak and with such high levels of brood mortality that they can no longer sustain mite population growth, remains to be determined.

It remains too early to draw firm conclusions as regards the impact of the varroa mite on African honeybees. Clearly, a large percentage of colonies are succumbing to the mite, but only time will tell if honeybee population collapse of the scale witnessed in Europe and North America occurs in Africa.

Effect on Pollination Efficiency

A 14% reduction in pollination efficiency was found in colonies that were heavily varroa- infested, in contrast to varroa-free control colonies (Table 3), in the pollination of pumpkins. This was despite there being more foraging activity in the varroa-infected colonies, perhaps in an effort to compensate for the reduced efficiency of foraging workers. These results need to be confirmed on other crop types for general significance.

Secondary Diseases

Colonies infested with large numbers of varroa mites are exhibiting additional problems with other diseases and pests. Poor brood patterns are common in these colonies. Small hive beetles, chalkbrood and Braula coeca all appear to be greatly increased in varroa- infected colonies. Chalkbrood, which was previously almost unreported in South Africa, is now widespread and almost ubiquitous. In addition, at least two viruses ( and Acute Paralysis Virus) have been found to be contributing to honeybee and colony mortality in varroa-infested colonies. There appears to be no correlation between varroa mite levels and levels of tracheal mites in African honeybee colonies, and tracheal mites remain uncommon. Table 3: A comparison of the pollination efficacy between varroa-free and varroa-infested honeybee colonies, using pumpkins in Cape Town.

Average Varroa Average number Pollination load (mites per 100 of returning efficacy as bees) foragers in two percentage “fruit” minutes set Treatment colonies 0.15 37.4 74% (n=6)

Control colonies 19.41 53.1 60% (n=6)

Colony collapse in the formerly Apis mellifera scutellata regions of the country is extremely rapid, probably due to the combined contributions of the varroa mite and the Cape Honeybee Problem (Allsopp 1992). The relative importance of these two factors, however, must still be determined.

Chemical control

Synthetic varroacides have been found to be extremely effective in the control of mites (>98%) whilst alternative chemical controls (e.g. formic acid) have been found to be less effective (70% control). Two commercial varroacides (Bayvarol and Apivar) have been registered for use in South Africa. Most beekeepers, who originally were against the use of any chemicals in their colonies for the control of varroa, are now using some varroacide to protect their colonies. Wild honeybees can obviously not be treated with varroacides, and there is great concern amongst beekeepers that the catching of honeybee swarms, the lifeblood of their industry, is on the wane.

Mite Reproduction

Varroa mites are found to successfully reproduce in both worker brood and brood in Cape honeybees, with mites being found in 6% of worker cells and 24% of drone cells (sample size 22 000 cells; Table 4). The reproductive rate in worker brood is calculated to be 1.4 (that is, 0.4 daughter mites produced per cell), and 1.9 in drone brood. Most significantly, in 56% of varroa-infected cells with emerging worker bees, only one mature mite is present. That is, reproduction has not been successfully completed, either because the short post-capping period of Cape bees has prevented completion of the mite reproductive cycle, because of male mite mortality, or because the foundress was infertile. In the case of drones emerging from varroa-infested cells, 27% of these cells have only one mature mite present, which can only be due to infertile foundresses.

These data indicate the presence of a large (>27%) percentage of infertile mites in the population. These infertile mites are likely to result from incomplete mite reproduction due to the shortened post-capping period found in worker brood of Cape honeybees. The extremely large numbers of varroa mites found in Cape honeybees (>30 000 in some colonies) indicates however, that although the short post-capping period of Cape bees must limit mite population growth to some extent, it is insufficient to prevent mite levels increasing to lethal levels. These data also indicate that the general presence of drone brood in African honeybee colonies for much of the year is crucial to mite population growth. Table 4: Reproduction of Varroa destructor in Cape honeybees

White-Eye White-Eye Emerging Emerging Worker Pupae Drone Pupae Worker Brood Drone Brood

Cells Examined 8846 3283 6104 1118

Cells with 5.98% 24.0% 4.83% 33.81% Varroa (0.0 – 42.55) (0.0 – 74.87) (0.0 – 49.33) (0.0 – 84.72)

Number of 1.24 1.83 1.74 3.48 Adult Mites per (0 – 4) (0 – 10) (0 – 6) (0 – 21) Infested Cell

Cells with Only 85% 73% 56% 27% a Single Adult Mite

Hygienic behaviour

A small population of selected Cape honeybee colonies have been tested for hygienic behaviour, as a possible basis for resistance to mites (Spivak & Gilliam 1998) and hence the basis for selection and breeding of varroa resistant Cape honeybees. Hygienic behaviour in these colonies has been found to be extremely variable, both between colonies, and with time, but Cape honeybee colonies all appear to be more hygienic than are European colonies (Spivak & Gilliam 1998) with 100% of dead brood being removed in 48 hours in this unselected population. This hygienic trait, however, seemed ineffectual against varroa mite infestation, and all but 2 of the 20 colonies died within 18 months. At present, there seems to be little correlation between the hygienic behaviour of Cape honeybees and their tolerance to varroa mites and natural resistance to the mites does not appear to be a common trait.

CONCLUSIONS

South Africa has the varroa mite that has caused widespread collapse of honeybee colonies throughout the world, and nothing has emerged during the Varroa Research Programme to suggest that the South African situation will be any different. The mite has spread all over the country, including the wild honeybee population, and can be expected to be found in all honeybee colonies in a matter of only a few years. Severe colony damage and loss is being witnessed due to the mite and associated secondary diseases. The presence of the varroa mite in Africa clearly represents a severe threat to the beekeeping industry, to agriculture dependent on honeybees for commercial pollination, to the wild honeybee population, and to the conservation of indigenous flora relying on honeybees for pollination. Only time will tell how severe the threat is.

Left to their own devices African honeybees may be able to accommodate the mite as they appear to have done with other honeybee diseases. It would be expected that large numbers of African honeybee colonies would collapse and die as a result of varroa, both in the wild and managed bee populations, but thereafter, resistance to the mite is expected to develop rapidly in these populations. As only varroa-resistant bees would produce swarms and drones, the resistance would rapidly spread through the population and simply allowing natural selection to take its course should result in African honeybees becoming tolerant to the varroa mite. The economic demand for commercial honeybee colonies will, however, dictate that beekeepers will treat colonies with varroacides should honeybee losses become considerable. This will artificially sustain the susceptible honeybee population, and will prevent the development and spread of a naturally-selected varroa- resistant population.

Hence, a comprehensive response to the varroa threat is required, involving Integrated Pest Management (IPM) strategies, further research, and regional, governmental and legal strategic actions. Included in this strategy are:

1. The development of mechanisms or legislation for the regional control and rotation of varroacides with different modes of action, to guard against the development of resistance in the mite population and to preserve adequate chemical control.

2. The development of guidelines for the use of non-regulated chemical products presently being used against the varroa mite.

3. Mechanisms to ensure the responsible use of chemical measures.

4. The development of cultural (non-chemical) control measures against varroa, to supplement chemical control.

5. The active development of natural resistance to the varroa mite in the wild honeybee population, by restricting the use of chemical control in certain regions, to facilitate the development of tolerance by natural selection.

ACKNOWLEDGEMENTS

The help of beekeepers and ARC-PPRI staff in Stellenbosch, as well as the financial assistance of the National Department of Agriculture, the Deciduous Fruit Producers’ Trust, the South African Subtropical Fruit Growers’ Association, and the Western Cape Beekeepers Association, is gratefully acknowledged.

REFERENCES

ALLSOPP, M H (1992) The capensis calamity. South Journal, 63: 76-78. ALLSOPP, M H; GOVAN, V; DAVISON, S (1997) Bee health report: Varroa in South Africa. Bee World, 78: 171-174. ANDERSON, D L (2000) Variation in the parasitic bee mite Varroa jacobsoni Oud. Apidologie, 31: 281-292. BALL, B (1997) Varroa and viruses. In: Munn, P; Jones, R (eds) Varroa! Fight the Mite. International Bee Research Association; pp 11-15. BOWEN-WALKER P L; MARTIN S J; GUNN A (1998). The transmission of between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsonii Oud. Journal of Invertebrate Pathology, 60, 1-7. DE JONG, D; MORSE, R A; EICKWORT, G C (1982) Mite pests of honey bees. Annual Review of Entomology 27: 229-252. DUCOS DE LAHITTE J; KEFUSS J; RITTER W; VANPOUKE J (1998) Testing Apis mellifera intermissa from Tunisia for Varroa jacobsoni tolerance in France. Apidologie 29: 267-269. ERICKSON E H; ATMOWIDJOJO A H; HINES L (1998) Can we produce varroa-tolerant honey bees in the United States? American Bee Journal 138: 828-832. FINLEY, J; CAMAZINE, S; FRAZIER, M (1996) The epidemic of colony losses during the 1995-1996 season. American Bee Journal 136: 805-808. KRAUS, B; PAGE R E Jr (1995) Population growth of Varroa jacobsoni Oud in Mediterranean climates in California. Apidologie 26: 149-157. MARCANGELI, J A; EGUARAS, M J; FERNANDEZ, N A (1992) Reproduction of Varroa jacobsoni (: : Varroidae) in temperate climates of Argentina. Apidologie 23: 57-50. MEDINA L M (1998) Frequency and infestation levels of the mite Varroa jacobsoni Oud. in managed honey bee (Apis mellifera L.) colonies in Yucatan, Mexico. American Bee Journal 138: 125-127. MORETTO, G; GONÇALVES, L S; DE JONG, D; BICHUETTE, M Z (1991) The effects of climate and bee race on Varroa jacobsoni Oud infestations in Brazil. Apidologie 22: 197-203. MORITZ R F A; JORDAN M (1992) Selection of resistance against Varroa jacobsoni across caste and sex in the honeybee (Apis mellifera L., : ). Experimental & Applied Acarology 16: 345-353. PAGE R E (1998) Varroa mite impacts spread and beekeeping. California Agriculture 52: 9-12. ROSENKRANZ, P; ENGELS, W (1994) Infertility of Varroa jacobsoni females after invasion into Apis mellifera worker brood as a tolerance factor against varroatosis. Apidologie 25: 402-411. SPIVAK M; GILLIAM M (1998) Hygienic behaviour of honeybees and its application for control of brood diseases and varroa. Bee World 79: 169-186. VARROA IN AFRICA – A SERIOUS THREAT

Mike Allsopp

ARC-Plant Protection Research Institute, Private Bag X5017, Stellenbosch 7599, South Africa. Tel: ++27 21 8874690; Fax: ++27 21 8875096; Email: [email protected]

Biography: – Mike Allsopp

Works in the Honeybee Section of Plant Protection Research Institute of Agricultural Research Council; worked at Stellenbosch section since 1991; in that time heavily involved in research into the Capensis Problem, and also the Varroa Mite; since 1998, the chief researcher in the South African Varroa Research Programme. Also the Editor of the South African Bee Journal.