VARROA-BEE RELATIONSHIPS -WHAT THEY TELL US ABOUT CONTROLLING VARROA MITES ON THE EUROPEAN HONEY BEE
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1 VARROA-BEE RELATIONSHIPS -WHAT THEY TELL US ABOUT CONTROLLING VARROA MITES ON THE EUROPEAN HONEY BEE Introduction Denis L. Anderson CSIRO Entomology, PO Box 1700, Canberra, ACT 2601 Australia Tel: , Fax , Until recently, only three species of Varroa mites had been recorded: Varroa jacobsoni, V. underwoodi and V. rindereri. Of these, V. jacobsoni had received the most attention from researchers, primarily because it was believed to have switched-host from the Asian bee (Apis cerana) to the European honey bee (A. mellifera) some years ago, then spread to become a serious parasite of A. mellifera worldwide. However, a little over a year ago, mites that had long been referred to as V. jacobsoni were found to be a complex of at least 2, but possibly 5, sibling species. These recent findings, together with others on bee taxonomy and Varroa reproductive behaviour on A. cerana and A. mellifera in Asia, have radically changed our understanding of Varroa/bee relationships. In this paper I briefly summarise these finding, before discussing what they tell us about controlling Varroa mites on A. mellifera worldwide. The key to understanding Varroa taxonomy is to understand the taxonomy of Varroa mites infesting Asian honey bees. All Varroa mites are natural parasites of Asian species of social honey bees. The first Varroa mite described was V. jacobsoni. A.C. Oudemans described it as a new species in 1904 from mites collected by the naturalist Edward Jacobson from Apis cerana colonies at Semarang on the Indonesian island of Java (10). V. underwoodi was next described in 1987 by M. Delfinado-Baker and K. Aggarwal from mites collected from A. cerana colonies in Nepal (8), while V. rindereri was described in 1996 by L.I. De Guzman and M. Delfinado-Baker from mites collected from A. koschevnikovi in Borneo (5). In early 2000, a comprehensive study incorporating mitochondrial (mtdna) sequencing techniques showed that the Varroa mites that had long been referred to as V. jacobsoni, and that were native parasites of A. cerana throughout Asia, were a complex of more than one species (4). Over 20 different genotypes have now been discovered in this species-complex. Most belong to 2 species, a newly defined V. jacobsoni and a newly named V. destructor, while the taxonomic status of a further 4 genotypes in the complex remains unresolved. Each genotype within the complex is currently referred to after the species it belongs to and the locality from which it exists naturally on its native Asian bee host (a strain of A. cerana). For example, a Java genotype of V. jacobsoni is a member of the species, V. jacobsoni, and exists naturally as a parasite of A. cerana in Java. Similarly, a Korea genotype of V. destructor is a member of the species, V. destructor, and exists naturally as a parasite of A. cerana in Korea, and so on (2, 4). Proceedings of the 37 th International Apicultural Congress, 28 October 1 November 2001, Durban, South Africa APIMONDIA 2001 To be referenced as: Proc. 37 th Int. Apic. Congr., 28 Oct 1 Nov 2001, Durban, South Africa ISBN: Produced by: Document Transformation Technologies Organised by: Conference Planners
2 Evidence of co-evolution between Varroa mites and their native Asian bee hosts Recent and past evidence from mtdna sequencing work has clearly demonstrated that the patternof-speciation among different Varroa genotypes infesting different genotypes of A. cerana throughout Asia is mirrored in the pattern-of-speciation among the A. cerana (3, 4, 12, 13). This, together with the well reported complex active defence behaviours that A. cerana direct against Varroa mites (11), infers that A. cerana and Varroa mites have been co-evolving for a long time. A critical piece of information to come from this work has been that particular strains of A. cerana carry their own particular strain of Varroa mite. Hence, Java and Malaysian strains of A. cerana carry Java and Malaysian genotypes of V. jacobsoni respectively, while Korea and Vietnam strains of A. cerana carry Korea and Vietnam genotypes of V. destructor respectively, and so on. Varroa genotypes that infect the European honey bee As mentioned previously, until recently, the Varroa mites that affect A. mellifera worldwide were assumed to be V. jacobsoni (6) However, mtdna sequencing work has now shown unequivocally that the Varroa mites affecting A. mellifera worldwide are V. destructor (2, 4). Only two genotypes of V. destructor are responsible. These are the so-called Korea and Japan/Thailand genotypes of V. destructor. Of the two mites, the Korea genotype has the widest geographical distribution. It affects A. mellifera in the Europe, the UK, Russia, the Mediterranean, the Middle East, Africa, Asia, North and South America, Canada and New Zealand (3, 4). The Japan/Thailand genotype of V. destructor has a more restricted distribution. It affects A. mellifera in Japan, Thailand, North and South America and Canada (4). In the Americas, this mite was initially found only in Brazil, but has since spread to other parts of South and North America and Canada. While the detection of this mite in Brazil seemed incongruous at first, it was found to correlate with reports that Varroa first appeared in Brazil following the introduction of European honey bees from Japan in 1971 (7). Reproductive behaviours of different Varroa mites on different bees An interesting finding that came from the recent Varroa taxonomy work was that their appeared to be genetic isolation between the Varroa genotypes that infested A. cerana and A. mellifera at different localities throughout Asia. For instance, when Varroa mites were randomly sampled from both species of bee in Vietnam, only the Vietnam genotype of V. destructor was found on the indigenous A. cerana, while the introduced A. mellifera were only carrying the Korea genotype of V. destructor, the common genotype that affects A. mellifera in other parts of the world. Likewise, on the northern Philippine island of Luzon, only the taxonomically unresolved Luzon 2 genotype was found on the indigenous A. cerana, whereas the introduced A. mellifera were only carrying the Korea genotype of V. destructor (4). Recent studies have indicated that this isolation between sympatric Varroa genotypes in Vietnam and the Philippines is at least partly due to the inability of the Varroa genotypes infesting the indigenous A. ceranas to reproduce on A. mellifera (3, 9). Genetic isolation between sympatric Varroa genotypes in Asia has been best studied on the Indonesian island of Java. There, the indigenous Asian bee (A. cerana javana) is parasitised by the Java stain of V. jacobsoni (VJ -J), and the introduced A. mellifera is only parasitised by the Korea strain of V. destructor (VD -K). Genetic isolation between the two mite genotypes in Java is 100%
3 The isolation is maintained because: (a) Female VD-K do not spread from the A. mellifera colonies into the A. cerana javana colonies (the reasons for this are not known) (4); (b) Female VJ-J spread at low levels from the A. cerana javana colonies (where they reproduce only on drone brood) into nearby A. mellifera colonies. They then proceed to enter drone and worker brood cells that are in the process of being capped. However, they do not go on to lay eggs or produce offspring (oogenesis is not activated). Instead, the invading female mites remain inside the cells with the developing bee brood and eventually emerge from the cells without offspring with the emerging bees (1). What Varroa-bee relationships tell us about finding a cure for Varroa mites on the European honey bee Recent findings have shown that there are many more Varroa mites than first thought (2, 4). However, all female mites of the different V. jacobsoni and V. destructor genotypes, as well as the females of the current unresolved Varroa mites, and also females of V. underwoodi, show similar reproductive behaviour on their respective indigenous strains of Asian bee (nothing is known about V. rindereri). That is, the female mites can only reproduce on drone brood, not worker brood (3). To reproduce, these females enter drone brood cells just prior to the cells being capped. They immediately move to the bottom of the cells and become buried upside-down in the remaining brood food. They are subsequently released from the food when the bee larvae finish eating. Then, after the bee larvae stretch out in their cells and complete their final larval moults, the female mites proceed to lay eggs and produce offspring (oogenesis is activated). In all cases, the first mite offspring are males, while the remaining offspring are females. These offspring develop into adults through the bee pupation stage. Males are the first to develop into adults and immediately proceed to mate with their sisters. New females, together with the mother mites, are released from the cells with the emerging drone bees. The adult males remain and die within the cells. When there are no drone brood cells available for invasion, mother mites will invade worker cells at the precapping stage. However, they do not go on to lay eggs or offspring (oogenesis is not activated). Instead, they feed and excrete on the developing worker bee pupae until being released from the cells with the emerging worker bees. This behaviour of the different Varroa genotypes, of only reproducing on drone brood of their native host bee, is a major reason why they appear relatively harmless to their native hosts. It is now known that all genotypes of V. jacobsoni and V. underwoodi lack the ability to reproduce on A. mellifera brood. Nevertheless, females of these genotypes will still attempt to reproduce on that bee if given the opportunity. For instance, if A. mellifera colonies are introduced into the vicinity where these genotypes are present on their native bee hosts, they will invade the A. mellifera colonies at low levels and enter brood cells that are in the stage of being capped. They then proceed to show the same elaborate pre-reproductive behaviour that they show on their native bee hosts. However, they do not go on to produce eggs or offspring on either the worker or drone A. mellifera broods (oogenesis is not activated) (1, 3). At the present time, only 2 of the 6 genotypes of V. destructor are known to be capable of reproducing on A. mellifera (4). These are the Korea and Japan/Thailand genotypes of V. destructor. However, these 2 genotypes do recognise A. mellifera brood in the same way they recognise the brood of their indigenous Asian bee hosts (the Korea and Japan/Thailand strains of A. cerana), because they can reproduce on both the drone and worker cells of A. mellifera but only on the drone brood of their Asian bee hosts. This raises the question of why oogenesis is not activated when the other genotypes of V. destructor (and indeed all other Varroa mites) invade A. mellifera brood cells. Most likely, oogenesis in all these mites is activated by Juvenile Hormone III (JH III). Recent studies in Java have indicated that the component that Varroa mites need to activate JH III
4 is a host (bee) component and is obtained within a 72 hour period after the mites enter bee brood cells. This component is likely to be the same or very similar in all Varroa mites, as it has to eventually activate JH III. It may differ in different bees by being present in different concentrations, or released in slightly different time frames. Finding this component of the oogenesis activation process may enable the development of lines of A. mellifera that are totally resistant to the Korea and Japan/Thailand genotypes of V. destructor. Indeed it may explain some of the tolerance that A. mellifera is now showing to V. destructor in different parts of the world (see Dr Ritter s paper in this session). Conclusion Studies are now underway to understand the process that activates Varroa oogenesis. Such information could lead to an innovative cure for the Varroa problem on A. mellifera. This work has been made possible by the recent clarification of Varroa taxonomy, which, in turn, has led to some astonishing new observations on Varroa reproductive behaviour on different bees. These recent developments are extremely exciting and emphasises the value of studying a pest on its native host species. References 1. Anderson, D.L. (1994). Non-reproduction of Varroa jacobsoni in Apis mellifera colonies in Papua New Guinea and Indonesia. Apidologie, 25: Anderson, D.L. (2000). Variation in the parasitic bee mite Varroa jacobsoni Oud. Apidologie, 31: Anderson, D.L. (2001). Unpublished data. 4. Anderson, D.L. and Trueman, J.W.H. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology, 24: De Guzman, L.I. and Delfinado-Baker, M. (1996). A new species of Varroa (Acari: Varroidae) associated with Apis koschevnikovi (Apidae: Hymenoptera) in Borneo. International Journal of Acarology, 22: De Guzman, L.I. and Rinderer, T.E. (1999). Identification and comparison of Varroa species infesting honey bees. Apidologie, 30: De Jong, D.D., Morse, R.A. and Eickwort, G.C. (1982). Mite pests of honey bees. Annual Review of Entomology, 27: Delfinado-Baker, M. and Aggarwal, K. (1987). A new Varroa (Acari: Varroidae) from the nest of Apis cerana (Apidae). International Journal of Acarology, 13: Fuchs, S., Long, L.T. and Anderson, D.L. (2000). A scientific note on the genetic distinctness of Varroa mites on Apis mellifera L. and on Apis cerana Fabr. in North Vietnam. Apidologie, 31: Oudemans, A.C. (1904). Note VIII. On a new genus and species of parasitic acari. Notes Leyden Museum, 24: Rath, W. (1999). Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie, 30: Smith, D.R. and Hagen, R.H. (1996). The biogeography of Apis cerana as revealed by mitochondrial DNA sequence data. Journal of the Kansas Entomological Society, 69: Smith, D.R. Villafuerte, L. Otis, G. and Palmer, M.R. (2000). Biogeography of Apis cerana F. and A. nigrocincta Smith: insights from mtdna studies. Apidologie, 31:
5 VARROA-BEE RELATIONSHIPS -WHAT THEY TELL US ABOUT CONTROLLING VARROA MITES ON THE EUROPEAN HONEY BEE Denis L. Anderson CSIRO Entomology, PO Box 1700, Canberra, ACT 2601 Australia Tel: , Fax , CV of Dr Denis Anderson Dr Anderson is a Principal Research Scientist at the Commonwealth Scientific and Industrial Research Organization (CSIRO) in Australia. Since completing his PhD in bee virology almost 20 years ago, he has continued to work in the area of bee pathology. He has worked on various bee disease problems in Australia and other countries and published widely on most bee pathogens, including viruses, protozoa, fungi, bacteria and mites. For the past 10 years his research has been particularly focussed on Varroa mites. This research culminated in him renaming the mite that affects Apis mellifera worldwide as Varroa destructor. That finding, which was first presented at Apimondia 99 in Vancouver, Canada, before being published early last year in the scientific journal Experimental and Applied Acarology, has received critical acclaim and several awards. Dr Anderson s current research is directed at developing novel control methods for Varroa destructor and another bee mite Tropilaelaps clareae. He is also currently writing a book on Varroa mites, which will be published early in the new year.
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