Allodapine Bee Research Articles

Efficiency and effectiveness of native bees and honey bees as pollinators of apples in New South Wales orchards

Relatively little is known about regional variation in the native insects that visit and pollinate apples - a pollination-dependent and economically valuable global crop - in Australia. We undertook three studies on Pink Lady apple crops in two regions of Australia to 1) quantify the amount of apple pollen carried on the bodies of insects; 2) evaluate differences in the amount of apple pollen deposited on the stigmas by different insects (pollinator efficiency); 3) experimentally assess fruit set to ascertain baseline pollination (open treatment), maximum pollination (hand pollination treatment), pollination after a single visit by an insect (single visit treatment) and no insect pollination (closed control); and 4) quantify regional contributions to pollination services provided by each taxon by calculating pollinator effectiveness (efficiency * visitation rate). The most common apple flower visitors included introduced honey bees (Apis mellifera), native meliponine, allodapine, and halictine bees, hoverflies, and beetles. Native stingless bee, Tetragonula carbonaria, foragers carried the most loose apple pollen on their bodies, followed by honey bees, but most individual insects (51.6 %) visiting flowers carried no apple pollen at all. Comparisons at higher taxonomic levels showed that all bees (pooled) carried more apple pollen on their bodies than all non-bee taxa (pooled). In addition, when contacting flower stigmas, bees deposited more pollen per visit than non-bees. The most pollen grains per single contact visit were deposited by native Exoneura bees (x̅ = 231.25), but variation was high (s.e. = 179.75). Irrespective of pollinator identity, pollen deposition from a single visit increased with time spent on the flower. However, across species, the amount of loose body pollen did not predict the quantity deposited; in particular, honey and stingless bees carried more pollen but deposited less than halictine (Lasioglossum) and allodapine (Exoneura) bees. Fruit set experiments confirmed that Pink Lady apples require pollination, because closed controls set zero fruits. Fruit set also required repeated pollinator visits, because flowers restricted to a single insect visit rarely set fruit. Pollination deficits were detected in both study regions, wherein open treatments set fewer fruits than hand-pollination treatments. Pollination services were predominantly provided by honey bees (97 %) in one region (Orange), but in a second region (Bilpin), honey bees (60 %) were complemented strongly by wild stingless bees (35 %). Hence, in Bilpin, native bee pollination services may buffer predicted decreases in honey bee populations, should the Varroa mite become established in Australian agro-environments.

The first contribution to karyotyping of the Australian allodapine bee Exoneura robusta

The Australian allodapine bee, Exoneura robusta, is an important pollinator of native flowering plants in Australian wet forests. In this study, the karyotype of E. robusta is illustrated and described using an air-drying technique. The metaphase analysis of the females revealed a diploid chromosome number of 26 (2n = 26). We then discuss parameters affecting the quality of chromosomal spreads including humidity which is not included or examined in existing insect karyotyping protocols. It is further discussed that this might be a reason why current bee chromosomal preparation protocols cannot be easily adapted to different bee species.

Casteless behaviour in social groups of the bee Exoneurella eremophila

The comparison of social systems, particularly in closely related taxa, can be highly valuable to the understanding of social evolution. While much research has focused on the formation of hierarchies and eusocial organisation, it needs to be remembered that not all social systems are necessarily based on hierarchies. The allodapine bee Exoneurella tridentata is the only eusocial species within the entire subfamily Xylocopinae (Apidae) with discrete queen and worker morphology. Here, we show that a non-eusocial congener, Exoneurella eremophila, is casteless. Nest collection and dissection data show no evidence of hierarchies, and there were no per capita benefits to group nesting in terms of brood production in any collection period. The casteless behaviour exhibited by E. eremophila appears to be common among very diverse lineages of the bee tribe Allodapini, and as such represents an evolutionarily persistent behavioural strategy. We discuss likely ecological factors that may have driven the evolution of species lacking castes and a species with morphologically distinct castes from within a small monophyletic group—genus Exoneurella.

Lack of ovarian skew in an allodapine bee and the evolution of casteless social behaviour

Facultatively social species exhibit varying degrees of reproductive skew that provide valuable insights into the possible evolutionary forces shaping the origins of obligate eusocial colony organisation, wherein the majority of individuals (workers) forgo direct reproduction. Here we report aspects of the nesting biology of a semi-arid population of the allodapine bee Exoneurella setosa, which forms social colonies that lack reproductive hierarchies and are therefore ‘casteless’; an intriguing discovery given that a congeneric eusocial species exhibits the greatest morphological distinction between queen and worker castes in the entire subfamily Xylocopinae (Apidae). Exoneurella setosa exhibited a modal colony size of two females per nest and we analysed nest-mate differentiation in ovarian development, body size and wing wear (a proxy for foraging activity). We then contrasted empirical results with Monte Carlo-simulated colonies to ascertain that multifemale nests lack evidence for reproductive skew. Our results suggest that nest-site limitation is a key driver for eusocial organisation within the Xylocopinae and that the absence of such environmental limitations, combined with minor benefits for group nesting, can select for casteless social organisation.

Sex Ratios in a Socially Parasitic Bee and Implications for Host-Parasite Interactions

Obligate social parasites of Hymenoptera, known as inquilines, have received enormous attention due to the elaborate adaptations they exhibit for exploiting their hosts, and because they have frequently been used to infer sympatric speciation. Their population biology can be difficult to infer as they are both rare and difficult to extract from host nests. Sex allocation has been studied for very few inquilines of social Hymenoptera. Here we report sex ratio patterns in the allodapine bee Inquilina schwarzi, which is an obligate social parasite of another allodapine, Exoneura robusta. We show that the sex ratio of this inquiline varies with its brood number, it is female-biased in the smallest broods, but becomes more even in larger broods, where the population-wide sex ratio is close to parity. We argue that this pattern of bias is consistent with local resource competition, where inquiline females compete to inherit their natal colony. We also argue that extremely female-biased sex ratios of the host species, combined with overall sex ratio parity in the parasite, may help ameliorate disparity in effective population sizes between these two species which are locked in an evolutionary arms race.

Potential pollination maintenance by an exotic allodapine bee under climate change scenarios in the Indo‐Pacific region

AbstractRecent studies suggest an alarming decline in pollinators across many regions of the world due to multiple factors. One potential factor is climate change, which poses both direct and indirect threats to pollinator populations. To help ameliorate the impact of declining populations on the function of ecological and agricultural systems, there is a need to identify species that may adapt to limit the magnitude of this pollination deficit. The South West Pacific has a highly depauperate endemic bee diversity and numerous non‐indigenous species, including honeybees. One allodapine bee, Braunsapis puangensis, has been accidentally introduced to Fiji where it has rapidly spread across multiple islands and become locally abundant. It is a long‐tongued bee, unaffected by honeybee pathogens, and has the potential to become an important crop pollinator. Here, we model the distribution of this species under different climate scenarios to determine how it is likely to respond to future climate change. We show that its distribution is unlikely to contract, but potentially expand with climate warming. These scenarios therefore indicate that the plasticity in B. puangensis populations may allow it to represent an important crop pollinator in this region should honeybee populations decline.

Small effective population sizes of bee social parasites compared to their hosts raise important questions for evolutionary arms race

Social parasitism in insects has raised major questions in evolutionary biology, firstly in terms of adaptations that parasites use to circumvent host defenses and, secondly, in terms of whether social parasites have arisen via allopatric or sympatric speciation. Here, we raise a third and major evolutionary issue: a priori considerations suggest that social parasites have much smaller effective population sizes (Ne) than their hosts, and should therefore have much slower rates of evolution than their hosts. The evolutionary arms race should therefore be weighted in favor of host species, raising the question of how social parasites have been able to persist over evolutionary time? Very few studies, however, have actually estimated the relative sizes of Ne for social insects and their social parasites, and therefore the dimensions of unequal host–parasite evolutionary rates are unknown. Here, we use extensive samples of allodapine bee host species and their inquilines from two localities over multiple years to gage their relative Nes. We show that inquiline species have Nes that are about an order of magnitude lower than their hosts, so explaining the evolutionary persistence of social parasitism poses a major puzzle for evolutionary biology. We propose several hypotheses that may be able to address this puzzle and discuss how they could be evaluated.

Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies

Communal behaviour is a form of social behaviour where two or more females nest together and have no reproductive hierarchies. Communal behaviour has often been regarded as an evolutionary ‘stepping stone’ to more complex forms of sociality involving castes, as well as a social form derived from solitary behaviour with no further evolution towards eusociality. However, recent phylogenetic studies on halictine bees suggest that some instances of communal behaviour are derived from eusociality. Here, we describe social nesting in an allodapine bee, Braunsapis puangensis, which has been introduced to Fiji from southern Asia. We show that this bee has a casteless form of sociality similar to communal organization, but which has been derived from an ancestrally hierarchical social system. This is likely due to a combination of small benefits for social nesting that rapidly saturate as colonies become larger, along with low costs for dispersal. We suggest that casteless forms of sociality have frequently evolved from hierarchical societies across many insect groups, but the analyses required for recognizing such societies are often undeveloped and hampers comparative approaches. Transitions from hierarchical to casteless societies challenge the notion that eusociality is an evolutionary ‘end point’ and we argue that eusociality can, in some cases, be regarded as an evolutionary step towards egalitarian societies. We also suggest that evolutionary periods involving reproductive hierarchies could select for traits that allow individuals to better assess their social environment and subsequently enable lower reproductive skew.

Current status of the introduced allodapine beeBraunsapis puangensis(Hymenoptera: Apidae) in Fiji

During the last 150 years, incursions of non-native species have been prevalent throughout the South West Pacific. The allodapine bee, Braunsapis puangensis (Cockerell) (Xylocopinae: Allodapini), was introduced to Fiji between 1965 and 2003, most likely from India. Until very recently, little was known about its dispersal ability and subsequent geographical spread across Fiji. Our study greatly increases the geographical records of B.puangensis across Viti Levu, Fiji's largest island, as well as surrounding islands including Vanua Levu, Taveuni and Mana Island. We found that B.puangensis is present throughout all major regions of Viti Levu, and it appears to be highly vagile. In Fiji, we only found B.puangensis foraging on introduced plant species, but nesting in both native and introduced plant species. Increased pollination of weedy exotic plants by this bee could increase their abundance in Fiji. Populations of B.puangensis in Fiji require close monitoring to detect environmental effects including spread of invasive weed species and knock-on effects to ecosystem interactions.

Recent introduction of an allodapine bee into Fiji: A new model system for understanding biological invasions by pollinators.

Morphology-based studies have suggested a very depauperate bee fauna for islands in the South West Pacific, and recent genetic studies since have indicated an even smaller endemic fauna with many bee species in this region resulting from human-aided dispersal. These introduced species have the potential to both disrupt native pollinator suites as well as augment crop pollination, but for most species the timings of introduction are unknown. We examined the distribution and nesting biology of the long-tongued bee Braunsapis puangensis that was first recorded from Fiji in 2007. This bee has now become widespread in Fiji and both its local abundance and geographical range are likely to increase dramatically. The impacts of this invasion are potentially enormous for agriculture and native ecosystems, but they also provide opportunities for understanding how social insect species adapt to new environments. We outline the major issues associated with this recent invasion and argue that a long-term monitoring study is needed.

Active sexual reproduction but no sign of genetic diversity in range-edge populations of Vanilla roscheri Rchb. f. (Orchidaceae) in South Africa

In South Africa, the wild leafless Vanilla roscheri Rchb. f. (Orchidaceae) is distributed only on the banks of the Lake Sibaya in KwaZulu-Natal Coastal Forest in the iSimangaliso Wetland Park. It is the southernmost vanilloid orchid on the African continent and a species of high conservation priority with little understanding of its reproductive biology and levels of genetic diversity. Mating systems and pollination ecology of the species were assessed by in situ experiments, in addition to genotyping plants at 16 microsatellite markers. Allogamous but self-compatible, V. roscheri depends on pollinators to achieve sexual reproduction. Its natural fruit set (26.3 %) is the highest reported for a non-spontaneously self-pollinating Vanilla species. It was associated with numerous flower visitors including two female allodapine bees (Allodapula variegata and Allodape rufogastra, Xylocopinae), captured with pollinia stored on the hind legs, and one female anthophorine bee. On the other hand, we report an absence of genetic diversity and homozygosity of the South-African populations of V. roscheri for all the genetic markers. Given the preferential outbreeding, the high natural fruit set and the pollinator/visitor richness of V. roscheri in Sibaya, a high level of genetic diversity was expected, but this was not the case. We detected a counterintuitive situation between the results of reproductive biology and genetics, making sense once the population situation on the margins of the species distribution is included. The null diversity expressed through the homozygous monomorphic markers is a consequence of the range-edge localization of the populations, which may have been subjected to severe bottlenecks (due to long distance colonization or fragmentation) along with inbreeding, in the past. The analysis highlights the complementarity of the approaches for which the implications in terms of conservation of the species in South Africa are discussed.

Allodapine Bees in the Arabian Peninsula (Hymenoptera: Apidae): A New Species ofBraunsapisfrom the Sarawat Mountains, with an Overview of the Arabian Fauna

ABSTRACT An interesting new species of allodapine bee (Xylocopinae: Allodapini: Allodapina) is described and figured from males and females captured in the Sarawat Mountains near al-Baha, representing the first records of the tribe for Saudi Arabia. Braunsapis alqarnii Engel and Michener, new species, is similar to the small species of the genus known from Africa and Madagascar but is distinguished on the basis of several features, most notably the male hind legs and terminalia. Notes are provided on the known allodapine fauna of the Arabian Peninsula, with a key to the species.

The Problems of a Priori Categorisation of Agonism and Cooperation: Circle‐Tube Interactions in Two Allodapine Bees

AbstractCircle‐tube experiments have been widely used to both examine nestmate recognition in social and solitary insects, as well as to characterise interactions in terms of agonism, cooperation, and avoidance. Despite their use in studies of halictid bees, carpenter bees, adrenid bees, and wasps, they have never been used to explore social interactions in the bee tribe Allodapini, where sociality varies widely in terms of complexity. Here, we investigate behaviours displayed within the highly eusocial allodapine Exoneurella tridentata and the facultatively social Exoneura robusta, using a standardised circle‐tube apparatus. We present two broad and important results: (i) Discrimination between nestmates and non‐nestmates is much more strongly expressed in the facultatively social species and (ii) principal components analyses do not indicate suites of behaviours that permit clear interpretations as being agonistic, cooperative, or avoidance. Our first set of results suggests that nestmate recognition is not an essential ability for social species. Our second set of results raise important questions about a priori functional categorisations of behaviours and whether these can be used to reliably classify observed behaviours as either avoidance, cooperation, or aggression. Our analyses highlight the risks of interpreting social insect interactions and call for a more cautious approach.

A new species of the allodapine bee genus <i>Braunsapis</i> from the Central African Republic (Hymenoptera: Apidae)

A new species of the allodapine bee genus Braunsapis Michener (Allodapini: Allodapina) is described and figured from a series of females collected in the Central African Republic. Braunsapis maxschwarzi Engel, new species, is similar to B. paradoxa (Strand) from South Africa, both species sharing the concave dorsal surface of the sixth metasomal tergum and the peculiar bifid apical projection of the sixth metasomal sternum. The new species, however, can be distinguished by the more extensively developed yellow markings of the face, the yellow pronotal lobe, the more shoulder-like posterolateral margins of the sixth tergum [more similar in this regard to B. angolensis (Cockerell) and not greatly produced as in B. paradoxa], and the more erect and prominent dorsal setae of metasomal terga IV–VI, among other traits.

Repeated origins of social parasitism in allodapine bees indicate that the weak form of Emery's rule is widespread, yet sympatric speciation remains highly problematic

The evolutionary origins of social parasitism are very unevenly distributed among ants, bees and wasps, but social parasite lineages are frequently close relatives of their host lineages. Two explanations for these relationships have been proposed: (1) initially, social species are more likely to become parasitic on relatively closely related social species, because they share life history, physiological and behavioural traits that allow successful integration within the host colony; and (2) social parasites have evolved directly from their host lineage via sympatric speciation. Comparative approaches, covering multiple origins and intermediate evolutionary stages, are needed to determine which of these possibilities is more likely. We use molecular phylogenetics to examine multiple origins of parasitism in the bee tribe Allodapini. We identify seven origins resulting in obligate social parasitism (inquilinism), one origin of facultative social parasitism, which was followed by subsequent speciation and where both daughter species remained facultatively parasitic, and one case of frequent facultative heterospecific co-nesting that probably represents incipient social parasitism. All host–parasite lineage pairs show strong phylogenetic affinities, but only the case of facultative heterospecific nesting involves true sister species relationships. Our results are consistent with the range of parasitic relationships that are expected under an allopatric model for the origin of social parasitism, but are highly problematic for a sympatric speciation model. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 320–331.

A single origin of large colony size in allodapine bees suggests a threshold event among 50 million years of evolutionary tinkering

Evolutionary origins of highly eusocial organization involving morphological castes have been very rare, yet these origins have often led to enormous diversification and ecological success. This suggests that once an apparently severe selective barrier to highly eusocial behaviour is overcome, major new adaptive landscapes open up. One would therefore expect a discontinuity in patterns of evolutionary change across this barrier. However, we do not know if highly eusocial organization has evolved incrementally from less complex societies, or if it has involved some kind of evolutionary leap. Our study examines this issue using colony size data from 33 allodapine bee species, with a crown age of ca. 47 Mya. Our species cover all major allodapine clades, and include Exoneurella tridentata, the only known allodapine with morphologically discrete castes. Phylogenetic analyses indicate a strong effect of phylogeny on the evolution of maximum brood size, but the effect of phylogeny on maximum colony size (number of adults) depends on whether E. tridentata is excluded or included in analyses. We found no evidence of punctuational change in maximum colony or brood sizes over the phylogeny as a whole, but colony and brood sizes in E. tridentata fall well beyond variation among the other allodapines. Colony size in E. tridentata therefore represents an evolutionary outcome that does not fit within the kinds of incremental changes found in other allodapines. We propose that E. tridentata indicates the crossing of an important threshold, and this has entailed some very unusual ecological circumstances.

Description of a New Subgenus ofAllodapula(Apidae: Allodapini) Based on Larval Morphology and DNA Sequence Data

Allodapine bees provide unique insights into social evolution because their method of provisioning brood in communal chambers differs from nearly all other social insects except ants. This method of brood rearing in allodapines is associated with the evolution of remarkable larval morphologies. Interestingly, allodapine larval morphology corresponds closely to phylogeny, more so than adult morphology. Here we describe a very unusual form of larval morphology in an African allodapine bee, Compsomelissa zaxantha, and show that this corresponds with phylogenetic analyses of DNA sequence data indicating that this species is much more closely allied with the genus Allodapula, but represents an evolutionary clade that differs strongly from currently described subgenera of Allodapula. We erect a new subgenus, Mhkuze, to contain this species and discuss the implications of this species for understanding the radiation in allodapine larval morphology.

Biogeographical origins and diversification of the exoneurine allodapine bees of Australia (Hymenoptera, Apidae)

Aim Early diversification of allodapine bees occurred in Africa c. 50 Ma. They are most abundant in sub-Saharan Africa and Australia, and one of the oldest phylogenetic divergences in the tribe involves a split between an African + Malagasy clade and an Australian clade. The historical biogeographical scenario for this has been highly problematic, entailing an Eocene dispersal from Africa to Australia, followed by an unresolved, and apparently rapid, set of bifurcations leading to the Australian ‘exoneurine’ genera. Here we use an expanded taxon set of Australian species to explore the timing and historical biogeography of the exoneurine radiation. Location Australia, Africa, Madagascar. Methods One nuclear gene (F2 copy of elongation factor 1α) and two mitochondrial genes (cytochrome c oxidase subunit I and cytochrome b) were sequenced for 33 Australian exoneurine species from all five genera found on the continent, as well as for an additional 37 species from all non-parasitic genera in the remainder of the tribe. We used Bayesian inference analyses to study phylogenetic topology and penalized likelihood analyses to infer key dates of divergence within the tribe. We also used lineage-through-time (LTT) analyses and Bayesian analyses to explore the tempo of radiations and biogeographical history of the exoneurines. Results Results from the phylogenetic analyses were congruent with previous studies, indicating a single colonization event c. 34 Ma, too late for Gondwanan vicariance models, and too early for a Laurasian dispersal route. In contrast to earlier studies, we show that this colonization event did not result in an ancient rapid radiation. However, LTT patterns indicated a rapid radiation of the temperate-adapted genera Exoneura and Brevineura, but not of the xeric-adapted genus Exoneurella, from 10 to 6 Ma. Main conclusions Our results indicate a trans-oceanic dispersal event from Africa to Australia, most likely via Antarctica, with an accelerated diversification of temperate-adapted lineages during the major Late Miocene event referred to as the ‘Hill Gap’. This is the first study to link radiations in Australian bee faunal elements to changing climate, and differs from many other plant and insect phylogenetic studies by showing increased radiation of temperate clades, rather than xeric clades, with increasing aridification of Australia.

The evolution of eusociality in allodapine bees: workers began by waiting

Understanding how sterile worker castes in social insects first evolved is one of the supreme puzzles in social evolution. Here, we show that in the bee tribe Allodapini, the earliest societies did not entail a foraging worker caste, but instead comprised females sharing a nest with supersedure of dominance. Subordinates delayed foraging until they became reproductively active, whereupon they provided food for their own brood as well as for those of previously dominant females. The earliest allodapine societies are, therefore, not consistent with an 'evo-devo' paradigm, where decoupling of foraging and reproductive tasks is proposed as a key early step in social evolution. Important features of these ancestral societies were insurance benefits for dominants, headstart benefits for subordinates and direct reproduction for both. The two lineages where morphologically distinct foraging worker castes evolved both occur in ecosystems with severe constraints on independent nesting and where brood rearing periods are very seasonally restricted. These conditions would have strongly curtailed dispersal options and increased the likelihood that dominance supersedure occurred after brood rearing opportunities were largely degraded. The origins of foraging castes, therefore, represented a shift towards assured fitness gains by subordinates, mediated by the dual constraints of social hierarchies and environmental harshness.

Native pollen thieves reduce the reproductive success of a hermaphroditic plant, Aloe maculata

Pollen is unique among floral rewards in functioning as both a carrier of gametes and an attractant and nutritious resource for floral visitors. Animals that collect pollen without pollinating (pollen thieves) could reduce siring success of thieved plants and cause pollen limitation of seed set at the population level; however, such impacts on plant reproduction have not been demonstrated experimentally. To test these effects we added hives of native honey bees (Apis mellifera scutellata) to populations of a primarily bird-pollinated plant, Aloe maculata, in eastern South Africa. In field and aviary trials, bee addition increased pollen removal from anthers but decreased pollen deposition on stigmas, and so reduced both male and female pollination components. Further, total seed production decreased with hive addition in the aviary experiment and in three of four field populations, indicating that population-level pollen theft can also compromise reproductive success. In the field, naturally occurring allodapine bees also seemed to act as pollen thieves, outweighing the effect of honey bee hive addition at one of the four aloe populations. Our results highlight the importance of social bees as pollen thieves, even of plants that have evolved in their presence, and the role of dichogamy in promoting pollen theft. Given the commonness of both social bees and dichogamy, pollen theft is likely a much more common influence on floral ecology and evolution than suggested by the sparse literature.