Ken Tan

Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera.

The vespine wasps, Vespa velutina, specialise in hawking honeybee foragers returning to their nests. We studied their behaviour in China using native Apis cerana and introduced A. mellifera colonies. When the wasps are hawking, A. cerana recruits threefold more guard bees to stave off predation than A. mellifera. The former also utilises wing shimmering as a visual pattern disruption mechanism, which is not shown by A. mellifera. A. cerana foragers halve the time of normal flight needed to dart into the nest entrance, while A. mellifera actually slows down in sashaying flight manoeuvres. V. velutina preferentially hawks A. mellifera foragers when both A. mellifera and A. cerana occur in the same apiary. The pace of wasp-hawking was highest in mid-summer but the frequency of hawking wasps was three times higher at A. mellifera colonies than at the A. cerana colonies. The wasps were taking A. mellifera foragers at a frequency eightfold greater than A. cerana foragers. The final hawking success rates of the wasps were about three times higher for A. mellifera foragers than for A. cerana. The relative success of native A. cerana over European A. mellifera in thwarting predation by the wasp V. velutina is interpreted as the result of co-evolution between the Asian wasp and honeybee, respectively.

Population structure and classification of Apis cerana

Multivariate morphometric analyses of Apis cerana Fabricius, 1793 across its full geographical range were performed. Principal components plots did not reveal distinct morphoclusters. Further substructuring of the principal component plots could not initially be derived but only by introducing local labelling did it reveal six main morphoclusters. We apply geographically based common epithets to the morphoclusters and designate them as: as “Northern cerana”, “Himalayan cerana” “Indian plains cerana” “Indochinese cerana” “Philippine cerana” and “Indo-Malayan cerana”. A. cerana naturally occurs in climatic zones ranging from rainforest, savanna, steppe, grasslands and deciduous forest to taiga. The distributions of the morphoclusters are related to these physiographic and climatic factors. The taxonomy of A. cerana is formally revised and synonymous specific and infraspecific names summarized.ZusammenfassungIn diesem Artikel berichten wir über die Ergebnisse einer über das gesamte Verbreitungsgebiet reichenden multivariaten morphometrischen Analyse von Apis cerana und die statistisch definierten Morphokluster und Subklusterpopulationen innerhalb dieser. (1) Morphokluster I, „nördliche cerana“, erstreckt sich vom nördlichen Afghanistan und Pakistan durch das nordwestliche Indien über das südliche Tibet, das nördliche Myanmar, China und dann nordöstlich nach Korea bis zum fernöstlichen Russland und Japan; (2) Morphokluster II, „himalaya cerana“ schließt die Bienen des nördlichen Indien und einige Regionen des südlichen Tibet und Nepal ein. (3) Morphokluster III „indische Ebene cerana“ besiedelt die Ebenen des zentralen und südlichen Indien und Sri Lanka. (4) In Morphokluster IV, „indo-chinesische cerana“ gruppieren sich die Bienen von Myanmar, Nordthailand, Laos und Südvietnam; (5) Morphokluster V „philippinische cerana“ ist auf die Philippinen beschränkt; (6) Morphokluster VI, hier als „indo-malayische cerana“ bezeichnet, erstreckt sich von Südthailand über Malaysia und Indonesien. Wir stellen die Beziehungen der Morphokluster untereinander und ihre geophysikalischen und ökologischen Umgebungen dar und erstellen eine neue Verbreitungskarte auf Grudlage der gesamten über A. cerana publizierten Literatur (Hepburn and Hepburn, 2006). Einige Anmerkungen zu Genfluss und zeitlicher reproduktiver Isolation werden aus Daten zu Schwärmen und Wanderungen abgeleitet.Nach moderner taxonomischer Praxis sind keine der historisch verwendeten “formellen” lateinischen Namen für die Variationen von Apis passend oder legitim. Daher sollten die Namen unter den Nomenklaturregeln ihrer Zeit gültig erstellten Namen sowie auch die übrigen, überwiegend nach 1970 erstellten Namen als Synonyme angesehen werden. Eine detaillierte synonymische Zusammenstellung im standardisierten taxonomischen Format findet sich bei Engel (1999). Als Konsequenz dieser publizierten Synonyme sind Trinomen wie A. c. japonica oder A. c. cerana unter den Regeln der ICZN keine offiziellen Bestandteile der Klassifikation von Apis mehr. Alle früheren Unterarten sind damit außer Gebrauch. Im gleichen Sinne sind Namen der Morphokluster wie „himalaya cerana“ und „indo-malayische cerana“ wie wir sie hier gebrauchen nicht bindend, sie bieten Bienenwissenschaftlern aber eine weitere Möglichkeit, die zusammenhängenden Populationen von A. cerana sinnvoll und biologisch begründet zu unterteilen. Die ICZN Zusamenfassung der Taxonomie für A. cerana ist hier zusammen mit der formellen Synonymie der Unterartnamen und anderen Namen zusammengestellt, wie es von der Nomenklatur gefordert wird.Zuletzt soll angemerkt werden, dass A. cerana in das nordöstliche China, nach der Ambon Insel, Iran und papua-Neuguinea eingeführt wurde. Von dort hat sie Inseln in der Torresstraße besiedelt (Dunn, 1992) und in neuerer Zeit Neubritannien und die Salomoninseln erreicht (Anderson, 2005 — unpubl. data). A. cerana von Papua-Neuguinea sind morphologisch von denen aus Java nicht unterscheidbar. A. cerana wurde darüber hinaus mehrere Male in Darwin, Brisbane und nahe Perth, Australien aufgegriffen.

A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults

Xenobiotics such as the neonicotinoid pesticide, imidacloprid, are used globally, but their effects on native bee species are poorly understood. We studied the effects of sublethal doses of imidacloprid on olfactory learning in the native honey bee species, Apis cerana, an important pollinator of agricultural and native plants throughout Asia. We provide the first evidence that imidacloprid can impair learning in A. cerana workers exposed as adults or as larvae. Adults that ingested a single imidacloprid dose as low as 0.1 ng/bee had significantly reduced olfactory learning acquisition, which was 1.6-fold higher in control bees. Longer-term learning (1-17 h after the last learning trial) was also impaired. Bees exposed as larvae to a total dose of 0.24 ng/bee did not have reduced survival to adulthood. However, these larval-treated bees had significantly impaired olfactory learning when tested as adults: control bees exhibited up to 4.8-fold better short-term learning acquisition, though longer-term learning was not affected. Thus, sublethal cognitive deficits elicited by neonicotinoids on a broad range of native bee species deserve further study.

Imidacloprid Alters Foraging and Decreases Bee Avoidance of Predators

Concern is growing over the effects of neonicotinoid pesticides, which can impair honey bee cognition. We provide the first demonstration that sublethal concentrations of imidacloprid can harm honey bee decision-making about danger by significantly increasing the probability of a bee visiting a dangerous food source. Apis cerana is a native bee that is an important pollinator of agricultural crops and native plants in Asia. When foraging on nectar containing 40 µg/L (34 ppb) imidacloprid, honey bees (Apis cerana) showed no aversion to a feeder with a hornet predator, and 1.8 fold more bees chose the dangerous feeder as compared to control bees. Control bees exhibited significant predator avoidance. We also give the first evidence that foraging by A. cerana workers can be inhibited by sublethal concentrations of the pesticide, imidacloprid, which is widely used in Asia. Compared to bees collecting uncontaminated nectar, 23% fewer foragers returned to collect the nectar with 40 µg/L imidacloprid. Bees that did return respectively collected 46% and 63% less nectar containing 20 µg/L and 40 µg/L imidacloprid. These results suggest that the effects of neonicotinoids on honey bee decision-making and other advanced cognitive functions should be explored. Moreover, research should extend beyond the classic model, the European honey bee (A. mellifera), to other important bee species.

Differences in foraging and broodnest temperature in the honey bees Apis cerana and A. mellifera

This study aims to explore the effect of ambient temperature on foraging the activity of Apis cerana and Apis mellifera colonies. We recorded ambient temperature, the time at which foraging commenced, worker thoracic temperature, and brood nest temperature at the same apiary in Kunming, China. We found that A. cerana start foraging earlier and at lower temperatures than do A. mellifera. A. cerana foraging (departures per minute) also peaked earlier and at lower temperature than did A. mellifera foraging. At the same ambient temperature, departing A. mellifera foragers and workers sampled from the brood nest had a higher thoracic temperature than departing A. cerana foragers and brood nest workers. A. mellifera colonies also maintained their brood nest temperature significantly higher than did A. cerana. Our results suggest that the larger A. mellifera foragers require a higher thoracic temperature to be able to forage.

Fearful Foragers: Honey Bees Tune Colony and Individual Foraging to Multi-Predator Presence and Food Quality

Fear can have strong ecosystem effects by giving predators a role disproportionate to their actual kill rates. In bees, fear is shown through foragers avoiding dangerous food sites, thereby reducing the fitness of pollinated plants. However, it remains unclear how fear affects pollinators in a complex natural scenario involving multiple predator species and different patch qualities. We studied hornets, Vespa velutina (smaller) and V. tropica (bigger) preying upon the Asian honey bee, Apis cerana in China. Hornets hunted bees on flowers and were attacked by bee colonies. Bees treated the bigger hornet species (which is 4 fold more massive) as more dangerous. It received 4.5 fold more attackers than the smaller hornet species. We tested bee responses to a three-feeder array with different hornet species and varying resource qualities. When all feeders offered 30% sucrose solution (w/w), colony foraging allocation, individual visits, and individual patch residence times were reduced according to the degree of danger. Predator presence reduced foraging visits by 55–79% and residence times by 17–33%. When feeders offered different reward levels (15%, 30%, or 45% sucrose), colony and individual foraging favored higher sugar concentrations. However, when balancing food quality against multiple threats (sweeter food corresponding to higher danger), colonies exhibited greater fear than individuals. Colonies decreased foraging at low and high danger patches. Individuals exhibited less fear and only decreased visits to the high danger patch. Contrasting individual with emergent colony-level effects of fear can thus illuminate how predators shape pollination by social bees.

Mitochondrial DNA diversity of Chinese Apis cerana

DNA sequence diversity in a non-coding portion of the mitochondrial genome was investigated in samples of Apis cerana from 47 locations in China. Nine haplotypes (mitochondrial genotypes) were found: Japan1, Japan2, Korea4, and Cambodia2, which were previously reported from other populations, and Chinal-5, which are new. All nine sequences belong to the Mainland mitochondrial lineage, and none differs from the Japanl haplotype by more than a single base substitution and/or a single insertion/deletion. Japanl is the most common haplotype, making up 39 of 49 sequences. Haplotype diversity was 0.4 (s.d. 0.089) and nucleotide diversity was 0.00569 (s.d. 0.00154). By both measures the Chinese samples were more diverse than those from Japan and Thailand, similar to populations from Pakistan, Burma and Korea, and less diverse than samples from Indochina (Laos-Cambodia-Vietnam).ZusammenfassungObwohl ein großer Anteil des Verbreitungsgebietes von Apis cerana innerhalb von China liegt, wurden dem Studium der geografischen und genetischen Variation dieser Bienen bislang nur wenig Arbeiten gewidmet. Wir präsentieren hier Daten über die Variation von 49 nichtkodierenden mitochondrialen DNA-Sequenzen chinesischer A. cerana von 47 Orten in 16 verschiedenen Provinzen (Abb.l, Tab. I). In diesen Proben wurden neun verschiedene Haplotypen gefunden (Abb. 1, Tab. I). Vier von diesen — Japan1, Japan2, Korea4 und Kambodscha 2 — waren bereits zuvor bekannt, während fünf weitere — Chinal, China2, China3, China4 und China5 — neu waren. Die nichtkodierenden Sequenzen wurden in der Genbank (http://www.ncbi.nlm.nih.gov/) hinterlegt (Zugangsnummern DQ269024 bis DQ269028). Alle gehören der mitochondrialen Festlandslinie an (Smith und Hagen, 1996; Smith et al., 2000), und keine unterscheidet sich von dem Japanl Haplotyp in mehr als einer einzigen Basensubstitution und/oder einer einzigen Insertion oder Deletion.Wir untersuchten die Diversität der Haplotypen oder Nukleotiden mit dem Computerprogramm DnaSP (Rozas et al., 2003), und verglichen die chinesischen Proben mit anderen Populationen vom asiatischen Festland. In den meisten Festlandspopulationen stellt Japan1 den am häufigsten angetroffenen Haplotyp dar (Tab. II). 39 der 49 chinesischen Sequenzen waren Japan1. Japan2 und Korea4 kamen jeweils zweimal vor, die anderen nur einmal. Die Diversität zwischen unseren chinesischen Proben betrug 0.4 (s.d. 0.089), die Diversität der Nukleotide 0.00569 (s.d. 0.00154).In Abb. 2 und 3 wird die Haplotyp- und Nukleotiddiversität der chinesischen Proben mit der anderer asiatischer Festlandpopulationen verglichen. Die Haplotypdiversität innerhalb der thailändischen und japanischen Proben ist extrem gering, mittelmäßig hoch in chinesischen, koreanischen und pakistanischen Proben, und am höchsten in „Indochina“ (Proben aus Laos, Kambodscha und Vietnam) und in Proben aus Burma. Die hohe Diversität in Burma ist teilweise auf das Vorkommen von Bienen des Sundalandhaplotyps zusammen mit Festlandshaplotypen zurückzuführen (vergl. hierzu die Haplotypdiversität in Burma mit und ohne die Sundaland Haplotypen; Abb. 2).Die Nukleotiddiversität zeigt die gleichen Trends in gesteigerter Form. Die Nukleotiddiversität war in Japan und Thailand extrem niedrig, höher in China, Korea und Pakistan, und am höchsten in Indo-china und Burma. Wenn allerdings die Haplotypen der Sundalandlinie aus dem Datenset von Burma entfernt werden (Abb. 3), ist die Nukleotiddiversität zwischen den verbleibenden burmesischen Festlandlinien deutlich vermindert und der von China, Pakistan und Korea ähnlich. Der Ausschluss der Sundalandlinien wirkt sich wegen der relativ großen Sequenzdiversität zwischen Sundalandlinien und Festlandlinien auf die Nukleotiddiversität dramatischer aus als auf die Haplotypdiversität.

Wasp Hawking Induces Endothermic Heat Production in Guard Bees

Abstract When vespine wasps, Vespa velutina Lepeletier (Hymenoptera: Vespidae), hawk (capture) bees at their nest entrances alerted and poised guards of Apis cerana cerana F. and Apis mellifera ligustica Spinola (Hymenoptera: Apidae) have average thoracic temperatures slightly above 24° C. Many additional worker bees of A. cerana, but not A. mellifera, are recruited to augment the guard bee cohort and begin wing-shimmering and body-rocking, and the average thoracic temperature rises to 29.8 ± 1.6° C. If the wasps persist hawking, about 30 guard bees of A. cerana that have raised their thoracic temperatures to 31.4 ± 0.9° C strike out at a wasp and form a ball around it. Within about three minutes the core temperature of the heat-balling A. cerana guard bees reaches about 46° C, which is above the lethal limit of the wasps, which are therefore killed. Although guard bees of A. mellifera do not exhibit the serial behavioural and physiological changes of A. cerana, they may also heat-ball hawking wasps. Here, the differences in the sequence of changes in the behaviour and temperature during “resting” and “heat-balling” by A. cerana and A. mellifera are reported.

Dancing to different tunes: heterospecific deciphering of the honeybee waggle dance

Although the structure of the dance language is very similar among species of honeybees, communication of the distance component of the message varies both intraspecifically and interspecifically. However, it is not known whether different honeybee species would attend interspecific waggle dances and, if so, whether they can decipher such dances. Using mixed-species colonies of Apis cerana and Apis mellifera, we show that, despite internal differences in the structure of the waggle dances of foragers, both species attend, and act on the information encoded in each other’s waggle dances but with limited accuracy. These observations indicate that direction and distance communication pre-date speciation in honeybees.

Giant Asian honeybees use olfactory eavesdropping to detect and avoid ant predators

Pollinators provide a key ecosystem service that can be influenced by predation and predator avoidance. However, it was unclear whether pollinators can avoid predators by eavesdropping, intercepting predator signals. Using a natural species assemblage, we show that a bee can eavesdrop on and avoid the trail pheromone of a sympatric ant, while foraging on a native plant. The giant Asian honeybee, Apis dorsata, avoided Calliandra haematocephala inflorescences with live weaver ants, Oecophylla smaragdina. Although few foraging bees were attacked, ants killed the bee in almost a third of attacks. Ant presence alone significantly reduced bee floral visits. Bees showed nearly equal avoidance of live ants and trail pheromone extracts, demonstrating that olfactory eavesdropping alone can elicit full avoidance. We then used GC-MS to analyse compounds deposited by ants walking and laying trail pheromone. The most abundant compounds were all trail pheromone components. However, bees did not avoid the most abundant and conspicuous trail pheromone compound, heneicosane. Foragers may instead detect a mixture of different trail pheromone compounds. Our results contribute to a growing understanding of how public information about predators and competitors can shape food webs, and show that pollinators can tap into the private signals of predators and use this information to their advantage.