Original article

Interspecific rearing and acceptance of queens between Fabricius, 1793 and Buttel-Reepen, 1906

N Koeniger G Koeniger S Tingek A Kelitu

1 Institut für Bienenkunde (Polytechnische Gesellschaft), Fachbereich Biologie der JW Goethe-Universität Frankfurt aM, Karl-von-Frisch-Weg 2, 61440 Oberursel, Germany; 2 Agricultural Research Station, Lagud Seberang PO Box 197, 89908 Tenom, ,

(Received 19 July 1996; accepted 4 October 1996)

Summary — Artificial queen cells with grafted young worker larvae of Apis cerana and Apis koschevnikovi were simultaneously introduced into queenless colonies of either A cerana and A koschevnikovi. All colonies preferred to rear conspecific larvae. The degree of this larval preference was different: A cerana colonies were more selective than A koschevnikovi colonies against alien larvae. In contrast, the A koschevnikovi colonies destroyed most of the introduced mature A cerana queen cells and killed all the queens that were able to emerge. A long term acceptance of alien queens occurred in A cerana colonies. The A koschevnikovi queens performed successful mating flights from A cerana colonies and the time of mating flights of these queens did not differ from A koschevnikovi queens fly- ing from conspecific colonies. The mated A koschevnikovi queens laid and the emerged bees were successfully reared by the A cerana worker bees. The A cerana host colonies were gradually transformed into A koschevnikovi colonies.

Apis cerana / Apis koschevnikovi / queen / interspecific relation / reproduction

INTRODUCTION ern Apis mellifera L (Ruttner, 1988; Tingek et al, 1988). Further, multivariate morpho- metric resulted in sim- The cavity-nesting bee species Apis analysis phenotypic ilarities between both Asian species that cerana Fabricius, 1793 and Apis confirmed the taxonomic status of A cerana koschevnikovi Buttel-Reepen, 1906 share and A koschevnikovi as related, dis- several common morphological and behav- closely tinct et al, 1989; Rinderer ioral characters such as prolonged radial species (Ruttner et al, vein of the hind wing, pore in the capping 1989). of the brood cell and fanning position Colonies of both species commonly occur with the head towards the colony entrance. in the region of Tenom (Sabah, Malaysia) These characters are not found in the West- which offer a favorable basis for compara- ble experimental research. Recently, the incubator at 34.5 °C (± 1 °C) and a relative humid- exchange of drone brood between colonies ity of about 60-70%. On day 8 we added two to three worker bees to the queen of A cerana and A koschevnikovi resulted in young (conspecific cell) from queenless colonies into each cage mixed of drones from both populations honey together with some candy (mixture of icing sugar bee species. These drones flew at their and A cerana honey) in order to provide the social species-specific mating time regardless of requirements for the survival of the newly hatched whether they were in conspecific or the other queens. A cerana queens emerged on days 9 species’ colonies (Koeniger et al, 1994). and 10. A koschevnikovi queens emerged on days 11 and 12. Whenever no queen cell was suc- The successful reciprocal interspecific cessfully capped the respective series was acceptance of drone brood and drones led excluded from the experiment. us to the question of whether or not exper- imentally exchanged queen larvae and queens of A cerana and A koschevnikovi Acceptance of alien queen cells were reared and accepted by colonies of and queens the other species. Queen cells reared in conspecific colonies were used for this experiment. For introduction of virgin MATERIAL AND METHODS queens we attached one ripe queen cell (1 or 2 days before emergence) to a comb of a queenless nucleus colony with no larvae younger than 8 The experiments were carried out in the apiaries days. We carried out daily inspections in the early of Research Station near Tenom, Agricultural morning hours and the young queen was marked Sabah East (North ), Malaysia during with paint on the thorax. February and March of 1993, 1994 and 1995.

Mating flights of A koschevnikovi queens Queen rearing from A cerana colonies

For these experiments four colonies of A cerana For observation of mating flights, a glass cov- and four colonies of A koschevnikovi were used ered channel was fitted to the hive entrance which each year. We had new colonies each year. The was closed in front with a queen excluder colonies were kept in small movable frame hives (Koeniger et al, 1994). A queen was released as x 35 x 42 and contained about 0.5 (25 cm) kg soon as she in the channel bees. We removed the and examined for appeared by lifting queen the excluder. After her departure the excluder the presence of queen cells after 8 All queen days. was closed again. Upon return the queen was cells were removed and we made a frame with found on the excluder and carefully inspected for 12-24 artificial queen cells 6 into (diameter mm) a mating sign. Then the excluder was temporar- which we had 48 larvae from grafted young (< h) ily lifted to allow the queen to enter the hive. The worker cells of ’unrelated’ donor colonies. The colonies were observed from 1400 to 1830 hours queen cells were in a sequence of alter- arranged (local time = GMT + 8) during the mating flight nating species, eg, an artificial queen cell with an experiment period. A cerana was followed by an A koschevnikovi larva which was followed by an A cerana larva and so on. The day of grafting was RESULTS defined as day 0. On day 2 we inspected the queen cells for larval acceptance. Cells with larvae had and drawn out accepted prolonged Queen walls (fig 1). The frame was then replaced back rearing into the colony. On day 7 all capped queen cells were removed from the colony. Each queen cell A cerana colonies continuously preferred was placed in a small plastic cage and kept in an to rear conspecific larvae. After 2 days only 32 alien larvae survived as compared to decreased and as a result four A more than twice the number (67) of con- koschevnikovi queens and 42 A cerana specific brood (fig 1). The relation between emerged (table I). When queen cells con- alien and conspecific queen cells further taining larvae of both species were intro- duced into A koschevnikovi host colonies a After day 2 (day 0 = emergence of the similar trend was observed. A koschevnikovi queen), however, the A cerana queen was worker bees also preferred conspecific lar- frequently attacked by A koschevnikovi vae, but their selection in favor of conspecific worker bees by grasping her with the queens was less severe. At the end 30 mandibles. The queen became motionless queens of A cerana were reared and 72 and emitted a clearly audible buzzing sound. conspecific (A koschevnikovi) queens (fig The surrounding workers then froze their 2; table II). motions and the queen slowly retreated. In this stage, however, several queens had lost some hairs with the rims of their wings of alien Acceptance queens already worn off. After day 3, aggressive behavior of A koschevnikovi worker bees In colonies of A koschevnikovi, out of 21 became more intense. A cerana queens introduced sealed queen cells of A cerana were surrounded by biting A koschevnikovi 12 were destroyed and nine young queens worker bees and rarely was a queen able were found at the first inspection. The freshly to retreat after a buzzing signal. The A cer- emerged alien queen moved calmly on the ana queens were held by workers, balled comb and did not cause much attention and heavily injured resulting in death after among the A koschevnikovi worker bees. 5 days (table II). No A cerana queen was On the first day we rarely saw any antago- able to perform mating flights from the A nistic behavior. koschevnikovi host colony. A cerana colonies destroyed nearly 50% 2. The queen moved somewhat restlessly (n = 8) of the alien queen cells before or over the combs and whenever she was during emergence. Some A cerana colonies encountered by antennating or grooming (n = 6) killed the A koschevnikovi queens workers, a short buzzing of the queen would during the first period. The behavior of A cer- ward off each . These queens ana host bees was similar as described performed a full mating flight activity during above for A koschevnikovi. The A cerana which one A koschevnikovi queen got lost workers attacked the young alien queen and (did not return). Three queens successfully the aggressions increased as the queens mated and started laying eggs 4 days after aged in the colonies. The queens were then the last mating flight (table II). The eggs balled, injured and expelled. In four A cerana hatched and the A cerana workers suc- colonies, however, the aggressive behav- cessfully reared the A koschevnikovi larvae. ior of the A cerana workers towards the With the newly hatching bees the originally A koschevnikovi queen decreased after day ’pure’ A cerana worker bee population became interspecifically mixed. We were colonies was 1743 hours. The period of total not able to systematically observe this tran- flight activity as well as the period of suc- sition until the A cerana workers were com- cessful mating flights did not differ signifi- pletely replaced by A koschevnikovi worker cantly between queens starting from alien bees. Interspecific aggressions at the hive and conspecific colonies (P= 0.83, Wilcoxon entrance or fights between A cerana and Rank Sum W test). A koschevnikovi worker bees during colony inspection were not observed. DISCUSSION

of A koschevnikovi Mating flights Several crossfostering experiments between queens from A cerana A mellifera and A cerana have been con- and A koschevnikovi colonies ducted. Many of these experiments were outlined or discussed by Ruttner (1988). Four A koschevnikovi virgin queens intro- Alien uncapped brood (eggs and larvae) duced into A cerana colonies performed 16 was cannibalized or removed (Dhaliwal and flights which include three flights from which Atwal, 1970). Capped worker brood of A the queen came back with a mating sign. cerana was accepted and hatched in A mel- For comparison, we observed three lifera colonies. The hatched A cerana work- A koschevnikovi virgin queens which started ers were expelled from an A mellifera colony from conspecific colonies. The queen flights (Sakagami, 1959). Young A mellifera worker occurred between 1700 and 1815 hours in bees were accepted in A cerana colonies both types of host colonies (table IV). During and participated in social duties. When the initial period (1700 to 1745 hours) the returning from their first orientation flights, flight duration was average 2.6 ± 1.9 min. however, the A mellifera workers were Successful mating flights (flights from which attacked by A cerana guard bees (Ruttner, the queen returned with mating sign) 1988). Rearing queens from A cerana larvae occurred in a relatively short period of 30 in A mellifera colonies was tried with little min from 1746 till 1815 hours and flight dura- or no success. In the course of numerous tion was 19.1 ± 4.9 min. The median time for grafting experiments with artificial queen the total flight activity of the queens from cells, eight A cerana larvae were accepted A cerana colonies was 1748 hours and the and four of these cells were capped. No median for flights from A koschevnikovi queen, however, emerged and an inspection of the cells after the due time resulted in ally with the age of the queen, and at day 3 very big larvae without any sign of pupation or 4 (after emergence) the queen was (Ruttner, 1988). Inoue (1962) grafted 100 balled, mutilated and finally expelled from larvae of A cerana japonica into queenless the colony. In A mellifera the young queen and broodless A mellifera colonies, and got starts synthesis after emergence only three queens, which were not accepted and an increasing amount of mandibular by the A mellifera colonies in which they (specially 9-keto-(E)-2- emerged. Recently, Pothichot et al (1993) decenoic acid) is produced until a physio- grafted alien larvae in artificial queen cells of logical level is reached at the time of mating A cerana and A mellifera colonies in Thai- flight (Slessor et al, 1990). We assume that land without any success. All alien larvae this pheromone synthesis happens similarly were rejected whereas conspecific larvae in young queens of A cerana and A were reared in a high percentage. koschevnikovi. The observed worker seemed to increase to In this study we grafted queen cells with aggressions parallel conspecific and alien larvae simultaneously an increase of queen pheromones. into either A cerana or A koschevnikovi host According to Plettner et al (1996) the colonies. This technique was employed to blend of the queen’s mandibular give larvae equal chances of being accepted pheromones is distinctly different among and reared. As expected there was a strong the several species of the genus Apis (data tendency for preference of conspecific larvae on mandible gland pheromones of A in both species. This tendency, however, was koschevnikovi have yet to be established). stronger in A cerana colonies which reared Therefore, one reason for the host worker significantly fewer alien queens than A bees’ aggression might be due to the koschevnikovi colonies (P < 0.1, Chi2 = 7.24). increasingly wrong blend of pheromones As regards the acceptance of a young alien emitted by the introduced alien queen. A koschevnikovi colonies were more queen, The reactions of A cerana host colonies selective. All A cerana queens were elimi- to young A koschevnikovi queens were not nated the A koschevnikovi worker bees. by consistent. In six colonies the young A The reaction of the queen to aggression koschevnikovi queens were attacked and of alien workers was characterized by a killed. In four colonies, however, the initial buzzing sound. With A mellifera, the virgin antagonistic behavior of the A cerana work- queen emits piping sounds which results in ers ceased allowing the development of the a sudden freezing of the worker’s move- A koschevnikovi queen to sexual maturity ments (Hamman, 1957; Michelsen et al, and performance of successful mating 1986). We observed a freezing reaction of flights. The A koschevnikovi queens then the A koschevnikovi workers to the A cerana started oviposition and the eggs hatched queen buzzing and a similar reaction of A and were successfully reared by the A cer- cerana workers to the A koschevnikovi ana host workers. This observation was queen. Apparently, the interspecific acous- rather unexpected since A cerana colonies tic communication between queen and work- rejected nearly all A koschevnikovi queen ers was successful. This observation cor- cells. In the latter experiments, the bees roborates the findings of Otis et al (1995), had the choice between alien and conspe- indicating that the queen piping of A cerana cific larvae, whereas after accepting the A A was and koschevnikovi similar but signi- koschevnikovi queen only A koschevnikovi different to A mellifera. ficantly eggs and worker larvae were available. Fur- The aggressive behavior, however, ther, we cannot exclude that the criteria for towards the alien queen increased gradu- acceptance are different for worker brood. Eventually more and more A koschevnikovi Koeniger and Koeniger, 1991; Fuchs et al, workers emerged and the A cerana work- 1996). It will be of a great interest to extend ers were replaced. Though the biological crossfostering experiments to Apis nuluensis, situation of this experiment is not typical for the recently described, third cavity-dwelling Apis, it has some similarities with a com- species of Borneo (Tingek et al, 1996). mon phenomenon in other social , bumble bees, ants or social wasps where an alien queen starts repro- ACKNOWLEDGMENTS duction and converts the host colony to her own species (Wilson, 1971). In nearly all We acknowledge support and assistance of JA these cases a close systematic relatedness Yaacob, director of Agriculture Sabah, PP Kee, between both species, the queen’s and the assistant director (research branch), D Simin, in ARS Tenom. S species of host colony, seems to be a func- officer charge Sheppard (WSU, and S Fuchs tional Pullman, USA) (IfB, Oberursel) gave requirement. valuable advice and contributed to the improve- The mating flight data of A koschevnikovi ment of earlier versions of the manuscript. queens flying from conspecific or A cerana colonies did not reveal systematic differ- et inter- ences. Therefore we conclude that the Résumé — Élevage acceptation de reines entre cerana queens followed their own internal clock. spécifiques Apis Similarly, crossfostered drones of A Fabricius, 1793 et Apis koschevnikovi 1906. inter- koschevnikovi and A cerana flew at their Buttel-Reepen, L’acceptation species specific mating time (Koeniger et al, spécifique réciproque du couvain de mâles 1994). Generally, the time of the mating flight et de mâles adultes d’A cerana et d’A koschevnikovi la de savoir seems to depend on the individual’s (drone pose question s’il en est de même les larves de reines or queen) internal clock in the genus Apis. pour et les reines adultes de ces deux espèces. Thus the isolation mecha- reproductive Dans des colonies orphelines d’A cerana nism of is based on sympatric Apis species et d’A koschevnikovi on a introduit des cel- individual behavior of the sexual castes lules royales artificielles renfermant de (Koeniger et al, 1988, 1996). jeunes larves soit de la même espèce, soit Our experiments did not reveal a general de l’autres espèce. Les deux espèces and uniform, species-specific pattern: A cer- d’abeilles mellifères ont préféré élever les ana colonies rejected more A koschevnikovi larves de leur propre espèce. Les colonies larvae grafted in queen cells but accepted d’A cerana, en particulier, ont constamment more A koschevnikovi queens. Neverthe- choisi les larves de leur espèce (fig 1) : less the interspecific transfer and accep- seules quatre reines d’A koschevnikovi ont tance of queen cells and queens between été élevées, alors que 42 reines d’A cerana A cerana and A koschevnikovi was more ont émergé pendant la même période successful than the exchange between A (tableau Ia). La sélection par les colonies mellifera and A cerana. Assuming that a d’A koschevnikovi a été moins sévère closer relationship between an alien queen (fig 2) : 30 reines d’A cerana et 72 reines and a host colony favors acceptance, our d’A koschevnikovi ont été élevées results were in line with the current taxon- (tableau Ib). Pour tester l’acceptation des omy of the cavity-dwelling Apis species, reines, des cellules royales mûres (1 à 2 j which gives A cerana and A koschevnikovi avant l’émergence) ont été introduites dans positions close to each other whereas A mel- des colonies orphelines de l’autre espèce lifera is more distant to both Asian species et - à condition que les ouvrières n’aient (Rinderer et al, 1989; Ruttner et al, 1989; pas détruit la cellule royale - Ia jeune reine a émergé dans la colonie étrangère. Sur Zusammenfassung — Interspezifische 18 cellules royales d’A cerana introduites Aufzucht und Annahme von Königinnen dans des colonies d’A koschevnikovi, nous zwischen den Arten Apis cerana Fabri- avons trouvé dix jeunes reines d’A cerana cius, 1793 und Apis koschevnikovi But- (huit cellules royales ont été détruites). Les tel-Reepen , 1906. Künstliche Königinnen- reines étrangères fraîchement écloses n’ont zellen mit jungen Arbeiterinnenlarven der pas beaucoup attiré l’attention des ouvrières eigenen und der fremden Art wurden wei- le premier jour mais, plus tard, elles ont été sellosen Völkern von A cerana bzw. constamment entourées par des ouvrières A koschevnikovi angeboten. Beide Honig- qui les mordaient et elles sont mortes par bienenarten zogen bevorzugt Larven der emballement (tableau II). Les colonies eigenen Art auf. Insbesondere wählten d’A cerana ont détruit à un stade précoce A cerana-Völker deutlich mehr konspezifi- presque 50 % des cellules royales étran- sche Larven (Abb 1); im Ergebnis wurden gères . Dans six colonies d’A cerana, les nur 4 Königinnen von A koschevnikovi auf- reines d’A koschevnikovi ont été tuées au gezogen, während in der gleichen Zeit 42 cours des premiers jours. Mais dans quatre A cerana-Königinnen schlüpften (TabelleI colonies d’A cerana le comportement agres- a). Die gegen fremde Königinnen gerich- sif des ouvrières envers la reine étrangère a tete Wahl von A koschevnikovi-Völkern war diminué au bout de deux jours. Une reine weniger streng (Abb 2). Bis zum Ende die- d’A koschevnikovi n’est pas rentrée de son ses Experiments wurden 30 Königinnen von vol de fécondation. Trois reines se sont A cerana und 72 der konspezifischen accouplées et ont commencé à pondre A koschevnikovi-Königinnen aufgezogen quatre jours après le dernier vol de fécon- (Tabelle I b). Um die Annahme fremder dation (tableau II). Les œufs ont éclos et Königinnen zu untersuchen, wurden reife les ouvrières d’A cerana ont élevé avec suc- Königinnenzellen in weisellose Völker ein- cès le couvain d’A koschevnikovi. Les gesetzt. Falls die Zellen nicht von den Arbei- ouvrières d’A koschevnikovi récemment terinnen zerstört wurden, schlüpften die jun- écloses ont rendu la population d’ouvrières gen Königinnen in den artfremden Völkern. de la colonie d’A cerana graduellement hété- Aus den 18 in A koschevnikovi-Völker ein- rospécifique jusqu’à ce que les ouvrières gebrachten A cerana-Königinnenzellen fan- d’A cerana soient toutes remplacées par den wir 10 junge A cerana-Königinnen; 8 der des ouvrières d’A koschevnikovi. Les vols de Zellen waren zerstört worden. Am ersten fécondation des reines d’A koschevnikovi Tag wurden die frischgeschlüpften Köni- ont eu lieu entre 17 h et 18 h 15 (tableau III). ginnen der fremden Art von den A koschev- L’heure moyenne des vols de reines des nikovi-Königinnen kaum beachtet. Später colonies d’A cerana s’est située à 17 h 48, waren diese Königinnen jedoch beständig celle des reines des colonies d’A koschev- von Arbeiterinnen umgeben, die sie bissen nikovi à 17 h 43. Il n’y a pas eu de diffé- und einknäulten bis diese starben. Die rence significative entre les reines s’envolant A koschevnikovi-Völker wiesen damit alle de colonies étrangères et celles s’envolant eingeführten artfremden Königinnen zurück de colonies de la même espèce en ce qui (Tabelle II). Die A cerana-Völker zerstörten concerne l’activité totale de vol et la durée ebenfalls nahezu 50% der Königinnenzel- des vols de fécondation réussis (p = 0,83, len bereits in einem frühen Stadium. In 6 Wilcoxon Rank Sum W test). A cerana-Völkern wurden die A koschevni- kovi-Königinnen während der ersten Tage Apis cerana / Apis koschevnikovi / rela- getötet. In 4 der A cerana-Völker liess das tion interspécifique / acceptation reine / aggressive Verhalten der Arbeiterinnen élevage reine / reproduction gegen die A koschevnikovi Königinnen dagegen nach 2 Tagen nach. Eine der species specific mating times. Insectes Soc 41, 73- 78 A koschevnikovi-Königinnen kehrte von ihrem Paarungsflug nicht zurück. Drei der Koeniger N, Koeniger G (1991) An evolutionary approach to mating behaviour and drone copulatory organs in Königinnen paarten sich erfolgreich und Apis. Apidologie 22, 581-590 vier nach dem letzten Paa- begannen Tage Koeniger N, Koeniger G, Gries M, Tingek S, Kelitu A rungsflug mit der Eiablage (Tabelle II). Nach (1996) Reproductive isolation of Apis nuluensis dem Schlupf der Maden wurde die (Tingek, Koeniger and Koeniger, 1996) by species- specific mating time. Apidologie 27, 353-360 A koschevnikovi-Brut erfolgreich von den A cerana-Arbeiterinnen Nach Koeniger N, Koeniger G, Tingek S, Mardan M, Rinderer aufgezogen. TE (1988) Reproductive isolation by different time of dem Schlupf der A koschevnikovi-Arbeite- drone flight between Apis cerana Fabricius, 1793 rinnen war die Arbeiterinnenpopulation and Apis vechti (Maa, 1953). Apidologie 19, 103-106 zunächst heterospezifisch zusammenge- Michelsen A, Kirchner WH, Andersen BB, Lindauer M setzt bis alle A cerana-Arbeiterinnen durch (1986) The tooting and quacking vibration signals of the queens: a quantitative analysis. A koschevnikovi-Arbeiterinnen ersetzt waren J Comp Pysiol A 158, 605-611 Die der (Tabelle II). Paarungsflüge Otis GW, Patton K, Tingek S (1995) Piping by queens of A koschevnikovi-Königinnen fanden zwi- Apis cerana (Fabricius 1793) and Apis koschevnikovi schen 17.00 und 18.15 statt (Tabelle III). (Buttel-Reepen 1906). Apidologie 26, 61-65 Der Median der Ausflugzeiten von Königin- Pothichot S, Wongsiri S, Dietz A (1993) Attempts in queen rearing of Apis cerana larvae in Apis mellifera nen aus A cerana-Völkern war 17.48, der colonies and Apis mellifera larvae in Apis cerana aus A koschevnikovi-Völkern 17.43. Zwi- colonies. In: Asian Apiculture. Proc 1st Int Cont Asian schen den aus Völkern der eigenen oder Honey Bees and Bee . Bangkok, , der fremden Art ausfliegenden Königinnen Wicwas Press, Cheshire, CT, USA, 112-117 bestanden keine Unterschiede Plettner E, Otis GW, Wimalaratne PDC, Winston ML, signifikanten Slessor KN, Pankiw T, Punchihewa PWK (1996) in der gesamten Flugaktivität oder des Zeit- Species- and caste-determined mandibular gland raums der erfolgreichen Paarungsflüge signals in honey bees (Apis). J Chem Ecol (in press) (P= 3D0.83, Wilcoxon Rangsummen Test). Rinderer TE, Koeniger N, Tingek S, Mardan M, Koeniger G (1989) A morphological comparison of the cavity bees of Borneo koschevnikovi koschevnikovi / Inter- dwelling honey Apis Apis cerana / Apis (Buttel-Reepen 1906) and Apis cerana (Fabricius spezifische Beziehung / Königin / Fort- 1793). Apidologie 20, 405-411 pflanzung Ruttner F (1988) Biogeography and of Hon- eybees. 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