Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud Werner Rath To cite this version: Werner Rath. Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie, Springer Verlag, 1999, 30 (2-3), pp.97-110. hal-00891571 HAL Id: hal-00891571 https://hal.archives-ouvertes.fr/hal-00891571 Submitted on 1 Jan 1999 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Review article Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Werner Rath Department of Horticulture, Faculty of Agricultural Production, Maejo University, Sansai, Chiang Mai, Thailand (Received 20 August 1998; accepted 11 February 1999) Abstract - The research on bee and mite biology over the past 20 years has uncovered numerous details of the A. cerana-V. jacobsoni co-adaptation which are systematically summarized here. A. cerana acquired a high degree of hygienic efficiency with a differentiated set of behavioural traits that we describe in this review in a broad sense to include grooming of mites by adult bees, uncapping and removal of infested brood and entombing of infested brood. Approximately 20 % of the reproducing mite population can be eliminated by entombing of lethally parasitized drone pupae. In their equally effective infesting behaviour the parasites explore the most suitable adult and larval host individuals for safe phoretic positions, the favourable caste and suitable age. A. cerana compel V. jacobsoni to reproduce exclusively on drone brood hosts. This limited reproduction, in combination with char- acteristics of the population dynamics of the host, are key factors which limit mite populations to tol- erable levels. © Inra/DIB/AGIB/Elsevier, Paris Apis cerana / Varroa jacobsoni / co-adaptation 1. INTRODUCTION scientists only after it became a major pest Varroa jacobsoni Oudemans (Acari: Var- on its acquired host, Apis mellifera L., in The research on the life roidae) females were first collected by Europe. early cycle, Jacobson from its host, the Asian honeybee biology and impacts of V. jacobsoni was Apis cerana Fabricius, in the year 1904 in almost exclusively conducted on the new Java, Indonesia, and were subsequently host A. mellifera. However, it appeared that described by the zoologist Oudemans. The a profound understanding of V. jacobsoni bee parasite received increased attention by and the parasite-host relations had to be E-mail: [email protected] based on the original relationship between traits; 2) population-dynamic aspects; and A. cerana and V. jacobsoni. While the early 3) physiological aspects. The use of the word reports from Koeniger et al. [21, 22] attracted ’hygienic’ is used here in the broad sense attention to the original host, the two publi- to include grooming behaviour, the uncap- cations of Peng et al. in 1987 [28, 29] on ping and removal of parasitized brood, and the successful grooming behaviour of the entombing of mites in cells, as opposed A. cerana worker bees were received with to Rothenbuhler’s use of ’hygienic behav- great excitement. The research of Peng [28] iour’ to describe solely the uncapping and nurtured the hope of finding new ways to removal of diseased brood [37]). control V. jacobsoni on A. mellifera. Even as the quantifications of Peng et al. [28] are revised by more recent research [4, 10, 17, 2. HYGIENIC TRAITS OF 30], this first publication on the interaction A. CERANA VERSUS INFESTING between V. jacobsoni and A. cerana is still TRAITS OF V. JACOBSONI substantial and frequently cited. 2.1. The senses of bees and mites The research on the co-adaptations A. cerana and over between V. jacobsoni It is obvious that bees and mites must the 18 remains modest past years compared have elaborate senses to perceive each to the extensive attention to V. on jacobsoni other’s presence in different places and occa- A. as reviewed in 1994 mellifera, e.g. by sions. V. jacobsoni depends on specific Milani Still are data on the [26]. lacking senses to locate its host, to move to phoret- of A. cerana and population dynamics ically safe places on adult bees [14, 32], to V. in their natural area of distribu- jacobsoni find phoretic feeding places and even to dis- tion, and data on the of reproductive biology tinguish between adult bees of different ages V. on drone brood of A. cerana. jacobsoni and physiologic states (on A. mellifera: [6, 7, of the well-studied of the mite Many aspects 24]). The sensory capabilities of V. jacob- behaviour in A. mellifera hosts are almost soni provide it with information that directs unknown from the host A. original cerana; its behaviour to the correct worker or drone e.g. the cognitive abilities and stress-related brood host which allows optimum timing behaviour of A. cerana, and the behaviour in of reproduction in A. cerana colonies. Apart brood cells, reproductive cycles, phoretic from the sensory capabilities, the mites inter- choice and of the mites. dispersal act with each other during feeding on adult bees and in brood cells (on A. Interspecific co-adaptation is a theoreti- mellifera: Adult female mites are able to cal concept that describes the phenomena [ 15]). recog- nize host bees in close and of a mutual adaptation of two species. The proximity, they react to attach interpretation of observable phenomena as frequently by jumping rapidly themselves to their host. How- co-adaptation is closely connected to the phoretically from some evi- concept of co-evolution which implies the ever, apart experimental dence on A. mellifera hosts and assumption that the ancestors of A. cerana assumptions deduced from observations, there is and V. jacobsoni exerted selective forces on general little information on the one another [34]. The following sections neurophysiology will summarize host and parasite traits that of V. jacobsoni, the qualities of its senses mutually influence their respective fitness and the stimuli that regulate its behaviour to safe successful and and accordingly can be considered as co- phoresy, dispersal effective on A. cerana hosts. adaptive traits. The current knowledge on reproduction the relationship between A. ceranae and A. cerana must also have specific senses V. jacobsoni is grouped here under three to detect mites on its body or in brood cells. categories: 1) hygienic traits versus infesting These specific senses are a prerequisite to pursuing the hygienic actions of grooming, diseased brood than olfactory stimuli. It is the uncapping of cells and the removal of also uncertain whether nursing bees per- infested brood. Most of the neurobiology ceive qualitative information on the condi- of the bees in relation to their perception of tion of sealed bee brood via pheromone sub- the mites is obscure and several observa- stances, which might enable the bees to tions are not congruent. For example, it is recognize healthy or infested, parasitized or common to observe exposed V. jacobsoni dead pupae, and consequently tolerate them females on the thorax of A. cerana workers or reject them. without any grooming reaction by the bees. Nestmates may even touch the exposed 2.2. phoretic mites with their antenna or mouth Grooming of A. cerana parts without any further reaction to the par- V. jacobsoni by asite. Additionally A. cerana are not dis- turbed at all by certain non-parasitic phoretic A. cerana worker bees perform a highly differentiated set of behavioural traits that mites that are almost as large as V. jacobsoni can be summarized as [12]. In southern Thailand, individual A. cer- ’grooming’, ’uncap- ana workers were found with more than ten ping’, ’removing’ and ’entombing’ [19, 21, mites of the non-parasitic pollen-feeding 22, 28, 29, 33]. Neocypholaelaps sp., and the bees did not The grooming action of A. cerana toward show any grooming response (pers. obs.). phoretic V. jacobsoni received much atten- On the other hand, the bees are disturbed tion following a research report by Peng at and react by self grooming or by performing al. [28]. The researchers observed that grooming dances when V. jacobsoni leave A. cerana bees groomed themselves and phoretically safe positions and move around also performed grooming dances to recruit on their hosts. individual or several nestmates to engage Some investigations suggested that olfac- in social grooming. During self grooming, A. cerana bees brush different of their tory senses are important in mite detection, parts In social the nestmates e.g. A. cerana were found to be more sensi- body. grooming, tive in the detection of experimental mites touch the thorax, propodeum and abdomen that originated from another host colony of the infested bee with their antenna, front and mandibula. The action of ([10, 36], conc. adhering scents: [27]. It is legs grooming not known how bees sense that certain is not specifically directed at the phoretic it that distinct areas sealed brood cells are infested with V. jacob- mite; rather, appears are searched The soni, or contaminated with artificially intro- automatically [13, 32]. duced particles [30, 36]. This remarkable grooming activity may cause the parasite to leave the host or the bees succeed in sense, which also occurs in A. mellifera, may induces the uncapping and removal of damaging the mite with their mandibula. microbial-infested and dead sealed brood Most of the damage that A. cerana bees inflict on occurs on of [37, 41, 42].