Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles

Most bees are diurnal, with behaviour that is largely visually mediated, but several groups have made evolutionary shifts to nocturnality, despite having apposition compound eyes unsuited to vision in dim light. We compared the anatomy and optics of the apposition eyes and the ocelli of the nocturnal carpenter bee, Xylocopa tranquebarica, with two sympatric species, the strictly diurnal X. leucothorax and the occasionally crepuscular X. tenuiscapa. The ocelli of the nocturnal X. tranquebarica are unusually large (diameter ca. 1 mm) and poorly focussed. Moreover, their apposition eyes show specific visual adaptations for vision in dim light, including large size, large facets and very wide rhabdoms, which together make these eyes 9 times more sensitive than those of X. tenuiscapa and 27 times more sensitive than those of X. leucothorax. These differences in optical sensitivity are surprisingly small considering that X. tranquebarica can fly on moonless nights when background luminance is as low as 10(-5) cd m(-2), implying that this bee must employ additional visual strategies to forage and find its way back to the nest. These strategies may include photoreceptors with longer integration times and higher contrast gains as well as higher neural summation mechanisms for increasing visual reliability in dim light.

Evolutionary Origin and Maintenance of Sociality in the Small Carpenter Bees

Many arthropods exhibit behaviours precursory to social life, including adult longevity, parental care, nest loyalty and mutual tolerance, yet there are few examples of social behaviour in this phylum. The small carpenter bees, genus Ceratina, provide important insights into the early stages of sociality. I described the biology and social behaviour of five facultatively social species which exhibit all of the preadaptations for successful group living, yet present ecological and behavioural characteristics that seemingly disfavour frequent colony formation. These species are socially polymorphic with both / solitary and social nests collected in sympatry. Social colonies consist of two adult females, one contributing both foraging and reproductive effort and the second which remains at the nest as a passive guard. Cooperative nesting provides no overt reproductive benefits over solitary nesting, although brood survival tends to be greater in social colonies. Three main theories explain cooperation among conspecifics: mutual benefit, kin selection and manipulation. Lifetime reproductive success calculations revealed that mutual benefit does not explain social behaviour in this group as social colonies have lower per capita life time reproductive success than solitary nests. Genetic pedigrees constructed from allozyme data indicate that kin selection might contribute to the maintenance of social nesting -, as social colonies consist of full sisters and thus some indirect fitness benefits are inherently bestowed on subordinate females as a result of remaining to help their dominant sister. These data suggest that the origin of sociality in ceratinines has principal costs and the great ecological success of highly eusociallineages occurred well after social origins. Ecological constraints such as resource limitation, unfavourable weather conditions and parasite pressure have long been considered some of the most important selective pressures for the evolution of sociality. I assessed the fitness consequences of these three ecological factors for reproductive success of solitary and social colonies and found that nest sites were not limiting, and the frequency of social nesting was consistent across brood rearing seasons. Local weather varied between seasons but was not correlated with reproductive success. Severe parasitism resulted in low reproductive success and total nest failure in solitary nests. Social colonies had higher reproductive success and were never extirpated by parasites. I suggest that social nesting represents a form of bet-hedging. The high frequency of solitary nests suggests that this is the optimal strategy when parasite pressure is low. However, social colonies have a selective advantage over solitary nesting females during periods of extreme parasite pressure. Finally, the small carpenter bees are recorded from all continents except Antarctica. I constructed the first molecular phylogeny of ceratinine bees based on four gene regions of selected species covering representatives from all continents and ecological regions. Maximum parsimony and Bayesian Inference tree topology and fossil dating support an African origin followed by an Old World invasion and New World radiation. All known Old World ceratinines form social colonies while New World species are largely solitary; thus geography and phylogenetic inertia are likely predictors of social evolution in this genus. This integrative approach not only describes the behaviour of several previously unknown or little-known Ceratina species, bu~ highlights the fact that this is an important, though previously unrecognized, model for studying evolutionary transitions from solitary to social behaviour.

Behaviour and life history of a large carpenter bee (Xylocopa virginica) in the northern extent of its range

Large carpenter bees (Hymenoptera: Apidae: Xylocopa) have traditionally been thought of as exhibiting solitary or occasionally communal colony social organization. However, studies have demonstrated more complex fonns of social behaviour in this genus. In this document, I examine elements ofbehaviour and life history in a North American species at the northern extreme of its range. Xylocopa virginica was found to be socially polymorphic with both solitary and meta-social or semi-social nests in the same population. In social nests, there is no apparent benefit from additional females which do not perfonn significant work or guarding. I found that the timing of life-history events varies between years, yet foraging effort only differed in the coldest and wettest year of2004 the study. Finally, I that male X virginica exhibit female defence polygyny, with resident and satellite males. Resident males maintain their territories through greater aggression relative to satellites.

Nestmate recognition in the large carpenter bee, Xylocopa virginica /

Abstract Many species of social insects have the ability to recognize their nestmates. In bees, sociality is maintained by bees that recognize which individuals should be helped and which should be hanned in order to maximize fitness (either inclusive or individual) (Hamilton 1964; Lin and Michener 1972). Since female bees generally lay eggs in a single nest, it is highly likely that bees found cohabitating in the same nest are siblings. According to the kin selection hypothesis, individuals should cooperate and avoid aggression with same sex nestmates (Hamilton 1964). However, in opposite sex pairs that are likely kin, aggression should increase among nestmates as an expression of inbreeding avoidance (Lihoreau et al. 2007). Female bees often guard nest entrances, recognizing and excluding foreign conspecific females that threaten to steal nest resources (Breed and Page 1991). Conversely, males that aggressively guard territories should avoid aggression towards other males that are likely kin (Shellman-Reeve and Gamboa 1984). In order to test whether Xy/ocopa virginica can distinguish nestmates from non-nestmates, circle tube testing arenas were used. Measures of aggression, cooperation and tolerance were evaluated to detennine the presence of nestmate recognition in this species. The results of this study indicate that male and female X virginica have the ability to distinguish nestmates from non-nestmates. Individuals in same sex pairs demonstrated increased pushing, biting, and C-posturing when faced with non-nestmates. Males in same sex pairs also attempted to pass (unsuccessfully) nOIl-nestmates more often than ncstmates, suggesting that this behaviour may be an cxpression of dominancc in males. Increased cooperation exemplified by successful passes was not observed among nestmates. However, incrcased tolerance in the [onn of head-to-head touching was observed for nestmates in female same sex and opposite sex pairs. These results supported the kin selection hypothesis. Moreover, increased tolerance among opposite sex non-nestmates suggested that X virginica do not demonstrate inbreeding avoidance among nestmates. 3 The second part of this study was conducted to establish the presence and extent of drifting, or travelling to different nests, in a Xylocopa virgillica population. Drifting in flying Hymenoptera is reported to be the result of navigation error and guard bees erroneously admitting novel individuals into the nest (Michener 1966). Since bees in this study were individually marked and captured at nest entrances, the locations where individuals were caught allowed me to determine where and how often bees travelled from nest to nest. Ifbees were captured near their home nests, changing nests may have been deliberate or explained by navigational error. However, ifbees were found in nests further away from their homes, this provides stronger evidence that flying towards a novel nest may have been deliberate. Female bees are often faithful to their own nests (Kasuya 1981) and no drifting was expected in female X virginica because they raise brood and contribute to nest maintenance activities. Contrary to females, males were not expected to remain faithful to a single nest. Results showed that many more females drifted than expected and that they were most often recaptured in a single nest, either their home nest or a novel nest. There were some females that were never caught in the same nest twice. In addition, females drifted to further nests when population density was low (in 2007), suggesting they seek out and claim nesting spaces when they are available. Males, as expected, showed the opposite pattern and most males drifted from nest to nest, never recaptured in the same location. This pattern indicates that males may be nesting wherever space is available, or nesting in benches nearest to their territories. This study reveals that both female and male X virginica are capable of nestmate recognition and use this ability in a dynamic environment, where nest membership is not as stable as once thought.

Differential reproductive success in Cassia fistula in different habitants-A case of pollinator limitations?

Differences in flower success patterns in two habitat types that differed drastically with respect to rainfall, tree density and species composition were studied at Mudumalai wildlife sanctuary, India. Observations on phenological patterns of two species, Cassia fistula and Gmelina arborea, were made from April 1988 through June 1990. Quantitative data on flower-fruit ratio, insect visitation rates, pollen grain per stigma and the number of fruits per tree were recorded. Data were also collected on the number of pollen deposited on the stigma after different types of bees visited the flower. The data suggested that only carpenter bees (Xylocopa spp) effect pollination in C. fistula. The differences in fruit-flower ratios were attributed to the differences in insect visitation rates to inflorescences between sites. The low pollen number per stigma and the resultant reduction in reproductive success in C. fistula are attributed to the competing species G. arborea receiving more visitations from pollinators in the wetter site. These results suggest that pollinator limitation is another constraint in reproductive success of plants.

Alloparental care in a solitary bee

Research into the evolutionary origins of sociality in insect colonies is changing emphasis from understanding how eusociality is maintained to how insects transition from solitary to social lifestyles. The pygmy carpenter bees (Ceratina spp.) offer an excellent model for investigating such factors as they have been historically thought of as solitary but have recently been shown to be socially polymorphic, which may indicate that they are currently in a transitive phase. By utilizing behavioural observation and experimental removal protocols, I show that extended parental care, as well as sibling care in Ceratina calcarata plays an important role in offspring development. I found, upon removal of the mother, that specifically produced ‘dwarf’ female offspring take over parental care roles in the nest. The existence of alloparental care and generational overlap suggests that although they are classified as solitary bees, C. calcarata possess the prerequisite behavioural repertoire for sociality.

The Implications of Forager Behaviour for Social Organisation in a Socially Polymorphic Carpenter Bee (Xylocopa virginica)

In social Hymenoptera, the division of labour is a major step in the evolution of sociality. Bees, which express many different kinds of sociality, can be classified according to how individuals share or do not share foraging and reproductive activities (Michener, 1974). The large carpenter bee, Xylocopa virginica, lives in populations with both solitary and social nests. In social nests, reproduction is controlled by the dominant female, who does all of her own foraging and egg-laying, while the subordinates guard the nest only. This study examined foraging behaviour as a way to classify the social hierarchy. Individual females were marked, measured and intensely observed for the foraging season. It was found that a large number of subordinates forage and likely obtain more reproductive fitness than previously thought. The dominance hierarchy is very likely a social queue, in which bees take turns foraging and egg-laying.

Microsatellite loci for the carpenter bee Xylocopa frontalis (Apidae, Xylocopini)

In the present study, a microsatellite-enriched genomic library was constructed and primers for 14 microsatellite loci were designed for Xylocopa frontalis. Twenty unrelated individuals were screened. All loci were polymorphic and the number of alleles per locus ranged from 6 to 17 (x = 10.43). Observed (H-o) and expected (H-e) heterozygosities ranged from 0.350 to 0.950 and 0.674 to 0.898, respectively. All loci were in Hardy-Weinberg equilibrium, except one. The microsatellite loci described in this study will contribute towards general biology studies of X. frontalis, intranidal genetic relationships and nest management for the pollination of passion fruit.

A story about being engaged in research : buzzing bees, small business and Australian unfair dismissal laws

Protection for employees from unfair dismissal (UFD) has been around in Australia under various guises for 30 years or so (Chapman, 2006). Labour standards, and particularly ILO Convention 158 (Convention Concerning Termination of Employment at the Initiative of the Employer 1982), underpin the adoption of a particular form of federal statutory UFD regime which first appeared in the 1993 reforms to the Industrial Relations Act 1998 (Commonwealth). Its existence, however, has not been uncontroversial, and the meaning, operation, scope and remedies have attracted attention over time. In fact, the first reforms to the federal UFD regime were undertaken under the Keating Labor government three months after they were enacted (Chapman, ibid.). Further reforms were made by the incoming Howard Liberal-national coalition government through the Workplace Relations Act 1996 (Commonwealth) (WRA), and arguably these reforms continued down the ‘contraction’ path (ibid.).

Bees at war: Interspecific battles and nest usurpation in stingless bees

We provide the first evidence for interspecific warfare in bees, a spectacular natural phenomenon that involves a series of aerial battles and leads to thousands of fatalities from both attacking and defending colonies. Molecular analysis of fights at a hive of the Australian stingless bee Tetragonula carbonaria revealed that the attack was launched by a related species, Tetragonula hockingsi, which has only recently extended its habitat into southeastern Queensland. Following a succession of attacks by the same T. hockingsi colony over a 4-month period, the defending T. carbonaria colony was defeated and the hive usurped, with the invading colony installing a new queen. We complemented our direct observations with a 5-year study of more than 260 Tetragonula hives and found interspecific hive changes, which were likely to be usurpation events, occurring in 46 hives over this period. We discuss how fighting swarms and hive usurpation fit with theoretical predictions on the evolution of fatal fighting and highlight the many unexplained features of these battles that warrant further study.

Anti-staphylococcal activity of C-methyl flavanones from propolis of Australian stingless bees (Tetragonula carbonaria) and fruit resins of Corymbia torelliana (Myrtaceae)

Propolis of Australian stingless bees (Tetragonula carbonaria, Meliponini) originating from Corymbia torelliana (Myrtaceae) fruit resins was tested for its antimicrobial activities as well as its flavonoid contents. This study aimed at the isolation, structural elucidation and antibacterial testing of flavanones of C. torelliana fruit resins that are incorporated into stingless bee propolis. Flavanones of this study were elucidated by spectroscopic and spectrometric methods including UV, 1D and 2D NMR, EI-MS, ESI-MS and HR-MS. The results indicated known C-methylated flavanones namely, 1 (2S)-cryptostrobin, its regioisomer 2 (2S)- stroboponin, 3 (2S)- cryptostrobin 7-methyl ether, and 6 (2S)- desmethoxymatteucinol, and known flavanones 4 (2S)- pinostrobin and 5 (2S)- pinocembrin as markers for C. torelliana fruit resins and one propolis type. Ethanolic preparations of propolis were shown to be active against Staphylococcus aureus (ATCC 25923) and to a lesser extent against Pseudomonas aeruginosa (ATCC 27853). C. torelliana flavanones inhibited the growth of S. aureus therefore contributing to the antibacterial effects observed for Australian stingless bee propolis extracts.

Standard yet unusual mechanisms of long-distance dispersal: Seed dispersal of Corymbia torelliana by bees

Mellitochory, seed dispersal by bees, has been implicated in long-distance dispersal of the tropical rain forest tree, Corymbia torelliana (Myrtaceae). We examined natural and introduced populations of C. torelliana for 4 years to determine the species of bees that disperse seeds, and the extent and distance of seed dispersal. The mechanism of seed dispersal by bees was also investigated, including fruit traits that promote dispersal, foraging behaviour of bees at fruits, and the fate of seeds. The fruit structure of C. torelliana, with seed presented in a resin reward, is a unique trait that promotes seed dispersal by bees and often results in long-distance dispersal. We discovered that a guild of four species of stingless bees, Trigona carbonaria, T. clypearis, T. sapiens, and T. hockingsi, dispersed seeds of C. torelliana in its natural range. More than half of the nests found within 250 m of fruiting trees had evidence of seed transport. Seeds were transported minimum distances of 20-220 m by bees. Approximately 88% of seeds were dispersed by gravity but almost all fruits retained one or two seeds embedded in resin for bee dispersal. Bee foraging for resin peaked immediately after fruit opening and corresponded to a peak of seed dispersal at the hive. There were strong correlations between numbers of seeds brought in and taken out of each hive by bees (r = 0.753-0.992, P < 0.05), and germination rates were 95 ± 5%. These results showed that bee-transported seeds were effectively dispersed outside of the hive soon after release from fruits. Seed dispersal by bees is a non-standard dispersal mechanism for C. torelliana, as most seeds are dispersed by gravity before bees can enter fruits. However, many C. torelliana seeds are dispersed by bees, since seeds are retained in almost all fruits, and all of these are dispersed by bees.

Warfare in stingless bees

Bees are well known for being industrious pollinators. Some species, however, have taken to invading the nests of other colonies to steal food, nest material or the nest site itself. Despite the potential mortality costs due to fighting with an aggressive opponent, the prospects of a large bounty can be worth the risk. In this review, we aim to bring together current knowledge on intercolony fighting with a view to better understand the evolution of warfare in bees and identify avenues for future research. A review of literature reveals that at least 60 species of stingless bees are involved in heterospecific conflicts, either as attacking or victim colonies. The threat of invasion has led to the evolution of architectural, behavioural and morphological adaptations, such as narrow entrance tunnels, mud balls to block the entrance, decoy nests that direct invaders away from the brood chamber, fighting swarms, and soldiers that are skilled at immobilising attackers. Little is known about how victim colonies are selected, but a phylogenetically controlled analysis suggests that the notorious robber bee Lestrimelitta preferentially attacks colonies of species with more concentrated honey. Warfare among bees poses many interesting questions, including why species differ so greatly in their response to attacks and how these alternative strategies of obtaining food or new nest sites have evolved.