(Varroa Jacobsoni) in Apis Cerana Cerana and Apis Mellifera Ligustica

Original article

Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana cerana and Apis mellifera ligustica

I Fries Wei Huazhen Shi Wei Chen Shu Jin2

1 Department of Entomology, Swedish University of Agricultural Sciences, S-75007 Uppsala, Sweden; 2 Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Xiang Shan, Beijing 100093, China

(Received 15 August 1995; accepted 23 November 1995)

Summary — Varroa mite mortality and mite damage in colonies of Apis cerana cerana Fabr and Apis mellifera ligustica Spin, where mites were added to observation hive bees and to full-sized colonies of both bee species, were studied. The results show grooming behavior in A cerana but the results also indicate that this behavior may be less effective than previously recorded. In A mellifera colonies, phoretic mites were also removed by the bees but less effectively than in A cerana colonies. The proportion of experimentally-added live mites in the debris that were visibly damaged in colonies of A cerana was 30% (n = 115). From A mellifera colonies, 12.5% of the introduced mites had visible injuries caused by the bees (n = 65). The mites recovered from both bee species showed reduced survival rate on bee pupae compared to control mites. Compared to A mellifera, A cerana is more effective in both removing mites and causing mite damage. However, in A mellifera phoretic mites are also removed by the bees, and some of them are injured. Since no reproduction of Varroa mites occurs in worker brood in A cerana, extremely effective grooming behavior may not be needed to explain the tolerance of A cerana to Varroa mite infestations. The results presented demonstrate that more research is needed to evaluate the importance of grooming behavior to Varroa mite tolerance in both A cerana and A mellifera.

Apis mellifera / Apis cerana /grooming behavior / Varroa jacobsoni / tolerance

INTRODUCTION Varroa mite has become widely distributed in A mellifera comparatively recently. In A The parasitic mite Varroa jacobsoni attacks cerana there is a balanced host/parasite both the European honey bee (Apis mellif- relationship in the sense that the mite does era) and the Asian honey bee (Apis cer- not seriously damage or kill the host. Varroa- ana). A cerana is the original host of the tolerant populations of A mellifera are found parasite (Koeniger et al, 1981), while the in South America in hybrids between Euro- pean and African bees (Camazine, 1986; vation hive experiments and full sized colony Engels et al, 1986; Ritter and De Jong, experiments using both A cerana and A mel- 1984) and in A mellifera populations in lifera colonies. We also report on mite dam- Tunisia (Ritter, 1990). However, in most age in naturally infested colonies of both cases A mellifera colonies die if the mite bee species. population is not controlled. The mechanisms behind the tolerance MATERIAL AND METHODS of A cerana to Varroa mite infestations were investigated by Peng et al (1987). They found extensive grooming behavior in A cer- The experiments presented were performed ana that resulted in removal of more than near Beijing during August and September 1994. 99% of mites added to colonies in obser- The bees used were a Chinese strain of A mellifera ligustica and colonies of A cerana cerana vation hives = 0.3% of the (n 270). Only from the mountain area 120 km south of Bei- mites were removed by grooming in colonies jing. of A mellifera = Of 42 mites exam- (n 270). All mites used in the presented experiments ined from the hive bottom of A cerana, were phoretic mites collected from one heavily 73.8% had visible injuries although no mites infested A mellifera colony. Infested bees were from A mellifera were examined. Büchler et shaken into a box with one side covered by a net, al (1992) also compared grooming in A cer- allowing mites to fall through the net. The bees with ana and A mellifera and found successful were shaken in the box the net side up after a small amount of wheat flour. Thereafter mite removal in 75% of the cases in A cer- adding the box was turned with the net side down and the ana = In A 48% of the mites (n 36). mellifera, mites falling from the bees were collected in a were removed by grooming (n = 25). Effec- container. In the laboratory each mite was trans- tive removal of Varroa mites has also been ferred and cleaned, if needed, onto a semi-damp reported from colonies of A cerana japonica piece of cloth and allowed to walk for approxi- (Takeuchi, 1993). mately half an hour. After that the mites were used for inoculation experiments. The mites were Damaged mites can be found on the bot- inoculated on bees or pupae within an hour of tom board in all Varroa-infested A mellifera collection. colonies, and injuries on Varroa mites, probably caused by grooming, have been observed in A mellifera (Ruttner and Hänel, Observation hive experiments 1992) in Europe. Moosbeckhofer (1992) found a correlation significant negative Two colonies of A cerana and one colony of A between the proportion of damaged mites mellifera were used. The addition of mites onto and the population size of the Varroa mite in marked bees followed the procedures described infested colonies. This indicates that groom- by Peng et al (1987) and the observation hives ing behavior expressed as a proportion of used were the same as used by these authors. Ten to mites were added each time to each damaged mites may be a useful parameter forty colony. in selecting for Varroa tolerance. Observations were made of the behavior of The extent and variation of mite damage individual bees and of mites falling from the bees in some A mellifera populations is well doc- to the bottom of the hive. At the hive bottom there umented (Moosbeckhofer, 1992; Wallner, was a white sheet of paper from which the mites 1994). There is, however, no information could be collected after falling. Each fallen mite about the level of mite damage from was examined under a stereo microscope at 63- fold magnification for visible signs of damage. colonies of A cerana infested naturally by One hour after inoculating the mites onto each mite. on the Varroa This paper reports tagged bee, the individual bees were examined for observations of mite damage from obser- the presence or absence of mites. The experiment was repeated twice in one A added to the colonies, were incubated in the same cerana colony, inoculating ten mites each time. way. The survival success of the mites was mea- This colony had one comb and contained approx- sured three times at 24 h intervals. The numbers imately 800 bees. In another A cerana colony the of incubated mites were 26 for A cerana, 41 for A experiment was conducted once, inoculating 40 mellifera and 40 control mites. mites. This colony had three combs and contained approximately 4 500 bees. In the A mellifera observation hive (two combs, approximately RESULTS 3 500 bees) the experiment was repeated twice, with ten and twenty mites respectively. Observation hive experiments Full-sized colonies In the first A cerana colony only six of the 20 mites were Three A cerana colonies and three A mellifera added recovered. Five of these colonies in Langstroth standard hives were mites were found on the bottom of the hive equipped with net bottoms to allow collection of and examined for damage; none had any mites under the colonies. The colonies were mon- visible damage. One mite was found on the itored daily for mite mortality for one month, and bee onto which it had been added. In the all mites from the A cerana and some of the mites second A cerana colony 11 of 40 mites from the A mellifera colonies were examined for added were recovered on the bottom board. mite damage. In the A cerana colonies the bees covered four, five and six combs respectively and Two of the recovered mites had visible dam- in the A mellifera colonies the corresponding num- age probably caused by the bees. No mite bers were 10, 12 and 15 combs. All six experi- was found on the tagged bee onto which it mental colonies were put on stands approximately had been introduced. 50 cm from the ground with the legs of the stands In the A cerana colonies we observed in water containers, to avoid ants or other ani- most of the marked bees out of mals gaining access to the hive debris. (55 60) At the end of the collection period, two colonies instantly performing auto-grooming (’self- after the mite on the bee’s from each bee species were used to investigate cleaning’) placing mites falling from the colonies after introduction of body. The remaining bees all performed mites directly upon the bees on top of or in grooming or appeared disturbed by the pres- between the frames. Forty eight hours after ence of the mite but this behavior was adding mites, possible residual mites were observed several minutes later and may be as an of the and regarded integrated part colony indistinct. After a few minutes some of the the colony was used for further experiments. bees were involved in allo-grooming (’nest- mites were added into each of two A Sixty mate cleaning’) as described by Peng et al cerana colonies and the experiment was repeated (1987). However, we also observed, again in one of these hives using 100 mites. In two clearly at on a a A mellifera colonies 40 mites were added to each least three occasions, mite leaving hive and the experiment was repeated again in marked bee and moving onto another bee. both hives using 100 mites in each hive. Mites Separate observations were also made were collected from under the colonies 15 and where mites could be seen on bees other 30 min, 1,2,3,4,5 and 6 h after the time of than the original mite-receiving bees. It introduction. Each mite which fell the col- during should be noted that it is very difficult to reg- lection was examined under a stereo period ister with the of mites microscope for signs of damage. certainty destiny placed on individual bees. They may move A number of fallen mites from each colony to parts of the bee where they cannot be where no visible damage could be seen under or move onto other bees unde- the microscope were incubated at +34 °C on red- observed, eyed pupae from A mellifera. At the same time tected. With the system used, however, the control mites, collected together with the mites mites removed from the bees were likely to be found on the bottom of the hive since The results from the observation hives the flight activity was low. are summarized in table I. In the A mellifera colony, mites were added on two occasions making a total of 30 Full-sized colonies mites. Only 6 of these mites were recovered from the bottom of the hive and examined. None of these had been visibly dam- During one month, only four mites were aged. Only one mite was found on the bee recovered from the bottom of the A cerana onto which it was added. colonies. From one colony no mites were A direct reaction of A mellifera to adding recovered. From the second colony one was and in the third three the mite onto the bee’s body was absent in mite recovered, mites were found. None of these mites had many cases (17 out of 30). Some cases that visible could be interpreted as auto-grooming or injuries (table II). disturbed behavior were observed (13 out of In the three A mellifera colonies, a total of 30) but not the intense grooming dance per- 258 mites falling naturally from the colonies formed by many A cerana bees. No clear were collected in 24 hour intervals (table II). cases of allo-grooming were observed in A Of these mites 26.4% had detectable mellifera. injuries. Of the 258 collected mites, 132 were alive when they were collected. Only ance (dead, light colored) indicated that they 9.1 % of the live mites had detectable were not mites added to the colonies. The injuries. low natural mite mortality in the experimental colonies influence the cal- During the 24 h preceding the first exper- may slightly iments with adding mites, the two A mellifera culations but not the conclusions. The data colonies used had natural mite mortalities on mites collected from full-sized colonies are summarized in table II. of zero and two mites respectively. When the experiment was repeated, the natural In figure 2 the survival success of mites mite mortalities during the 24 h before the fallen from the bees and then incubated on experiment were four mites in each of the pupae is presented. The mite mortality at 24 two colonies used. h post incubation was already significantly than for the control mites incubated Figure 1 presents the cumulative per- higher one hour after collection from the adult centage recovery of all mites added during bees, both A cerana = 6 h for the A cerana and A mellifera for (P < 0.05, χ2 4.72, 1 df) colonies. Of the 115 mites recovered within and A mellifera (P < 0.05, χ2 = 4.91, 1 df). At 48 and 72 h incubation the of 6 h in the A cerana colonies, 34 mites post mortality (29.6%) had visible signs of damage caused the mites from A cerana was significantly than for those collected from A mel- by the bees. Often one or more legs per higher lifera colonies < = 1 df and P mite were missing, but cases where only (P 0.05, χ2 5.5, < = 1 df the pretarsus of one leg was missing were 0.05, χ2 4.4, respectively). also recorded. The proportion of mites recovered from A mellifera colonies within DISCUSSION 6 h was significantly lower than from the A cerana colonies (P < 0.001, χ2 = 45.2, 1 df). Of the 65 mites recovered, eight had been A substantial proportion of mites are dam- visibly damaged by the bees (12.3%). Thus, aged by bees in A mellifera colonies. In this the proportion of damaged mites in the A investigation, 26.4% of all the naturally fallen mellifera colonies was significantly lower mites had injuries while only 9.1 % of fallen than in the A cerana colonies (P < 0.05, χ2 live mites had injuries. This could indicate = 6.9, 1 df). A total of three mites fallen from either that mites die when they become the A mellifera colonies were not consid- injured, or that the bees injure already dead ered in the calculations since their appear- or non-vital mites. A mellifera do injure already dead Varroa mites introduced with between bee species. Thus, the results pre- hatching brood into colonies (Rosenkranz sented here should be interpreted with great et al, in preparation). caution and, rather than demonstrating a Although not evident from the observation specific grooming efficacy in the tested bees, hive experiments, the presented results they indicate that more research is needed. demonstrate that A cerana is more efficient It should also be noted that in this experi- in both removing and damaging live vigorous ment most of the mites dropped from the Varroa mites compared to A mellifera. This colonies within the first few hours after intro- is congruent with earlier studies where duction. This may not reflect natural condi- grooming behavior has been considered tions and it should be emphasized that there (Büchler et al, 1992; Peng et al, 1987; is a need to study to what extent mites are Takeuchi, 1993). However, the damage damaged in A cerana colonies under natural conditions. The few mites collected from caused to the mite population by the grooming behavior reported here is substantially the debris in naturally infested A cerana colonies in this = had no different from some earlier reports (Peng et investigation (n 4) al, 1987). The proportion of mites removed visible damage. from the bees in this investigation is lower in For both bee species in this investiga- A cerana and higher in A mellifera than tion, some mites that fell from the bees, reported by Peng et al (1987). The propor- where no visible physical damage could be tion of damaged mites is also lower in A cer- detected, still seemed to be damaged by ana than previously reported. It should be the bees. The survival rate of control mites pointed out, though, that the observations incubated on pupae was significantly higher of removed mites only refer to mites found than that of the mites fallen from A cerana or on the bottom. In the observation hives A mellifera colonies. This effect could removal of mites from the hives was prob- depend in part on dehydration or other ably limited due to low flight activities. In experimental effects on the fallen mites but the full-sized colonies, however, the possi- the difference demonstrated between bee bility cannot be excluded that some of the species clearly indicate an effect from the introduced mites were thrown out from the bees. Thus, to evaluate the impact of honey colonies and that this behavior may vary bee behavior on the survival of the mites, it is not sufficient to consider only visibly mite tolerance is not demonstrated in this damaged mites. or any other investigation and the groom- behavior alone cannot There may be several explanations for ing probably explain the described discrepancies to earlier obser- mite tolerance in A cerana (Boecking et al, vations. Peng et al (1987), who only worked 1993). In simulations of the population of the Varroa mite in colonies of A with observation hives, considered move- growth the relative of ment of mites from one bee to another as mellifera, importance repro- successful mite removal. From the point of duction in the worker brood is obvious (Fries view of mite tolerance of the colony, mites et al, 1994). These simulation studies indicate if there is no in the need to be removed not only from individual that, reproduction bees but from the colony. Thus, in this inves- worker brood, the need for effective groom- to the mite under control tigation we did not consider change of host ing keep population to be successful removal of mites. The mites may be reduced. Understanding the relative of various factors that con- we registered as having been removed by importance tribute to the Varroa mite tolerance in A cer- the bees were collected from under the bees ana, or in other mite-tolerant bees, in all cases (observation hive experiments honey may be for available and colony experiments). In our observa- important evaluating in A mellifera. In the search for a tion hive experiments we were not able to options solution to the Varroa mite problem see when the mites changed their host in possible in colonies of A mellifera, many cases. through breeding the host-parasite relationship in the origi- Another possible explanation for the nal host of the mite needs to be studied fur- noted differences to earlier studies may be ther. the source of bees. Peng et al (1987) used A cerana from the south of China, while the A cerana bees in this investigation came ACKNOWLEDGMENT from the Beijing area. The source of mites could also influence the results. We used This was the Swedish Coun- only mites collected from adult bees, while study supported by cil for Forestry and Agricultural Research. Peng et al (1987) used both phoretic mites and mites collected from a sealed brood. The full-sized colony experiments Résumé — Étude comparative du com- demonstrate that the studied A cerana portement de toilettage et du nombre colonies were much more effective in injur- d’acariens lésés (Varroa jacobsoni) chez ing and removing mites from the adult bees Apis cerana cerana et Apis mellifera than the A mellifera colonies. However, in ligustica. On a étudié la mortalité de l’aca- this study this behavior is also present in A rien Varroa jacobsoni et ses lésions (prin- mellifera to a substantial degree. The source cipalement la perte ou les lésions d’une ou of mites (A mellifera) may enhance the plusieurs pattes) dans des ruches d’obser- grooming effect in A cerana since odor is vation, auxquelles des varroas avaient été an important cue for detecting mites ajoutés, et dans des colonies entières des (Rosenkranz et al, 1993). There is a need to deux espèces Apis cerana cerana et Apis study a much larger number of colonies with mellifera ligustica. Dans les ruches d’obser- respect to grooming behavior before any vation, des varroas prélevés dans des colo- conclusions should be made concerning its nies d’A mellifera ont été introduits sur des relative importance for Varroa mite toler- abeilles marquées, selon le protocole de ance in A cerana or A mellifera. The rela- Peng et al (1987). Trente varroas ont été tive importance of this behavior for Varroa ajoutés aux colonies d’A mellifera et 60 à celles d’A cerana. Les varroas éliminés par lifera. Puisque V jacobsoni ne se reproduit les abeilles et tombés sur le plancher de la pas dans le couvain d’ouvrières d’A cerana, ruche dans l’heure suivant l’introduction ont la grande efficacité du comportement de été récoltés et leurs lésions étudiées. La toilettage mentionnée auparavant n’est peut- présence de varroas sur les abeilles mar- être pas nécessaire pour expliquer la tolé- quées a été recherchée une heure après rance d’A cerana aux infestations par V leur introduction. Dans les colonies entières, jacobsoni. Nos résultats montrent que des les varroas, prélevés dans des colonies de recherches complémentaires sont néces- mellifera, ont été introduits directement au- saires pour comprendre l’importance du dessus des abeilles sur les barettes supé- comportement de toilettage dans la tolé- rieures (en tout 280 dans les colonies de rance à Varroa, aussi bien chez A cerana mellifera et 220 dans celles de cerana). Les que chez A mellifera. varroas tombés des abeilles ont été récoltés sous les fonds grillagés des ruches 15 Apis mellifera / Apis cerana / comporte- minutes, 30 minutes, 1, 2, 3, 4, 5 et 6 heures ment toilettage / Varroa jacobsoni / sen- après leur introduction. Leurs lésions ont sibilité résistance été étudiées. Les résultats montrent l’exis- tence chez A cerana d’un comportement de toilettage, mais il n’est pas aussi efficace Zusammenfassung — Putzverhalten und que précédemment décrit. Dans les ruches beschädigte Milben (Varroa jacobsoni) d’observation d’A cerana, le comportement bei Apis cerana cerana und Apis melli- de toilettage décrit par Peng et al (1987) a fera ligustica . Mortalität und Verletzungen été observé, mais il est clair également que (meist ein oder mehrere Biene verletzt oder certains varroas changent simplement fehlend) von Varroa wurden an Völkern von d’hôte lorsque que survient le toilettage. Apis cerana cerana und Apis mellifera ligus- D’après les observations, 27 % seulement tica untersucht. Hierzu wurden die unter- des varroas introduits (16 sur 60) ont été suchte Milben zu normalen Bienenvölkern éliminés par les abeilles en 1 heure. Sur les und zu Beobachtungsstöcken zugesetzt. In varroas éliminés, seuls deux (12,5 %) ont den mit A mellifera und A cerana besetzten été visiblement lésés par les abeilles. Sur Beobachtungsstöcken wurden phoretische les 30 varroas introduits sur les abeilles A Milben aus Völkern von A mellifera ent- mellifera, six ont été éliminés par elles et sprechend den Methoden von Peng et al retrouvés sur le plancher (20 %). Aucun (1987) auf gekennzeichnete Bienenarbeite- d’entre eux ne présentaient de lésion. Dans rinnen aufgebracht. Bei A mellifera wurden les colonies entières d’A mellifera, les var- 30, bei A cerana 60 Milben zugesetzt. Die roas ont également été éliminés par les innerhalb der folgenden Stunde von den Bie- abeilles mais de façon bien moins efficace nen entfernten Milben wurden vom Beuten- que dans les colonies d’A cerana. La pro- boden aufgesammelt und auf Verletzungen portion de varroas vivants retrouvés dans untersucht. Die gekennzeichneten Bienen les débris dans les 6 heures suivant l’intro- wurden nach dieser Stunde auf Milbenbe- duction et présentant visiblement des lésions fall untersucht. In den normalen Bienenvöl- a été de 30 % (n = 115) dans les colonies kern beider Bienenarten wurden die eben- d’A cerana et de 12 % (n = 65) dans les falls von A mellifera abgesammelten Milben colonies d’A mellifera. Comparée à A mel- direkt auf die auf den Oberträgern der lifera, A cerana est plus efficace pour se Waben sitzenden Arbeiterinnen aufgesetzt. débarrasser des acariens et leur causer des Die herunterfallenden Milben wurden 0,25, lésions. Néanmoins, ces deux comporte- 0,5, 1, 2, 3, 4 und 6 Stunden nach Einsetzen ments sont également présents chez A mel- der Milben unterhalb eines Drahtgitters im Beutenboden eingesammelt. Alle diese Mil- REFERENCES ben wurden auf Beschädigungen untersucht. wurden 280 Milben in Völker von Insgesamt Boecking O, Rath W, Drescher W (1993) Grooming and A mellifera und 220 in Völker von A cerana removal behavior - strategies of Apis mellifera and eingesetzt. Die Ergebnisse zeigen zwar Apis cerana against Varroa jacobsoni. Am Bee J einen deutlichen Effekt des Putzverhaltens 133, 117-119 bei A cerana, allerdings deuten sie darauf Büchler R, Drescher W, Tornier I (1992) Grooming behaviour of mellifera and hin, daß dieser wesentlich ist als Apis cerana, Apis Apis geringer dorsata and its effect on the parasitic mites Varroa früher berichtet. Das von Peng et al (1987) jacobsoni and Tropilaelaps clareae. 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