Halictine Bees Research Articles

Addendum to: Joseph Vachal (1838-1911): French entomologist and politician (Zootaxa, 3442, 1-52).

A series of recent papers has compiled brief biographies and listed the scientific publications and taxa proposed for a number of bee researchers (Rasmussen et al. 2007; Zuparko 2007; Rasmussen & Ascher 2008; Rasmussen et al. 2009; Rasmussen 2012; Rasmussen et al. 2013). Unfortunately five taxa attributed in the original publication to Vachal were overlooked in the recent review of his taxonomic work (Rasmussen 2012). Whereas these five names for halictine bees appeared with brief Latin descriptions in the publication by Kohl (1905), all other hymenopteran taxa described by Kohl in this paper had descriptions in German. At least one of the halictine names has been attributed to Kohl (Warncke, 1984), but based on the fact that 1) Kohl gave Vachal the authorship (as “J. Vachal n. sp.”) and 2) the five descriptions are in a different language from the taxa described by Kohl in the same paper, these five names should all be referred to Vachal as pointed out by Ebmer (1976). The paper by Kohl (1905) lists all of the Hymenoptera collected from the surroundings of the snow-capped stratovolcano Mount Erciyes (Erciyes Dag, as Erdschias) of Kayseri Province in Turkey, the highest mountain of central Anatolia. Bee localities visited by the expedition include Bos Tepe and Ewlije-Dagh south of Kayseri and Yilanli Dag (as Illany-Dagh) west of Kayseri. “Bussara (vel Bussana)” is not listed in the gazetteer introducing the study or in Penther (1906), but is possible Bursa in northwest Turkey (Ebmer 2000). Thus, Rasmussen (2012) should be amended to reflect that Vachal described 791 new species (not 786). In addition Table 2 listing the collectors of specimens described by Vachal as new taxa should be amended to include: Penther, Arnold (1865–1931): Turkey (Erciyes and vicinity, “Bussara (vel Bussana)?” (probably Bursa)).

Recipe for disruption: multiple recent arrivals of megachilid bees in Pacific archipelagos

When examining how the ecosystems of remote islands have developed, it is important to know the timing of when various elements arrived and whether they then diversified. Our understanding of the histories behind the biodiverse south west Pacific (SWP) archipelagos is limited, and further impeded by the complex geological histories of this region. Previous studies of the SWP short-tongued halictine bee fauna suggest their presence is much younger than the geological ages of these archipelagos, which is surprising given their critical role as pollinators in other terrestrial ecosystems. The long-tongued megachilid bees represent a considerable proportion of the known bee species for the region, yet little is known of their origin. Here we use genetic diversity within mitochondrial DNA to infer the likely ages and origins of megachilid species from Vanuatu, Fiji, and Samoa. Our results indicate a very recent origin for megachilids in the SWP, with many species exhibiting small intraspecific genetic distances. Three species share almost identical haplotypes with specimens from Southeast Asia, suggesting multiple human-aided introductions. Combined with data from recent studies on other bee groups present in the region, our results have broad implications for how the Pacific island biota developed and how we should approach its management.

Diversification of Fijian halictine bees: Insights into a recent island radiation

Although bees form a key pollinator suite for flowering plants, very few studies have examined the evolutionary radiation of non-domesticated bees over human time-scales. This is surprising given the importance of bees for crop pollination and the effect of humans in transforming ecosystems via agriculture. In the Pacific, where the bee fauna appears depauperate, their importance as pollinators is not clear, particularly in Fiji where species diversity is even lower than neighbouring archipelagos. Here we explore the radiation of halictine bees in Fiji using phylogenetic analyses of mtDNA COI sequence data. Our analyses indicate the existence of several ‘deep’ clades whose divergences are close to the crown node, along with a highly derived ‘broom’ clade showing very high haplotype diversity, and mostly limited to low-lying agricultural regions. This derived clade is very abundant, whereas the more basal clades were relatively rare. Although nearly all haplotype diversity in Fijian Homalictus comprises synonymous substitutions, a small number of amino acid changes are associated with the major clades, including the hyper-diverse clade. Analyses of haplotype lineage accumulation show a steep increase in selectively neutral COI haplotypes corresponding to the emergence of this ‘broom’ clade. We explore three possible scenarios for this dramatic increase: (i) a key change in adaptedness to the environment, (ii) a large-scale extinction event, or (iii) a dramatic increase in suitable habitats leading to rapid population expansion. Using estimated mutation rates of mitochondrial DNA in other invertebrates, we argue that Homalictus first colonised the Fijian archipelago in the middle–late Pleistocene, and the rapid accumulation of haplotypes in the hyper-diverse clade occurred in the Holocene, but prior to recorded human presence in the Fijian region. Our results indicate that bees have not been important pollinators of Fijian ecosystems until very recent times. Post-Pleistocene climate change and anthropogenic effects on Fijian ecosystems are likely to have greatly transformed pollinator suites from the conditions when those ecosystems were first being assembled.

Increased group size promotes task specialization in a normally solitary halictine bee

Division of labour is a fundamental property of animal groups; how it is generated and evolves is, therefore, of central importance to sociobiology. Self-organizational models suggest (1) that division of labour can emerge spontaneously at the origin of group living and (2) that increased group size further promotes task specialization. We examined the emergence and scaling of division of labour in an evolutionarily incipient social system: forced associations of the normally solitary halictine bee Lasioglossum (Ctenonomia) NDA-1. A division of labour between nest excavation and guarding arose in pairs and in groups of four bees, with individuals in larger groups exhibiting higher degrees of task specialization. Task differentiation may be facilitated by intrinsic behavioral variability and/or spatial organization. Our results support the hypotheses that division of labour can self-organize at early stages of social evolution and that greater individual specialization is an emergent consequence of increased group size.

Lynchiatilla Casal, 1963 (Hymenoptera: Mutillidae): a new species from Brazil associated with Paroxystoglossa spiloptera Moure (Hymenoptera: Apidae: Halictinae), and notes on other species

Lynchiatilla parana Cambra in Bergamaschi et al., sp. nov. (female and male) from Brazil and the male of Lynchiatilla leguera Casal, 1963 are newly described and illustrated. Lynchiatilla silvai Casal, 1963 is reported for the first time for the state of Paraná, southern Brazil. A key to the males for those species where they are known is given. Specimens of L. parana sp. nov. were observed and collected during 204 hours of fieldwork in a montane Atlantic Forest area, providing behavioral data and implicating the halictine bee Paroxystoglossa spiloptera Moure, 1960 as its probable host. Adult wasps were captured and kept in individual containers for sex-association mating trials in the laboratory. Color and size variation in a population of L. leguera from Jujuy, northern Argentina, are discussed and illustrated.

Little effect of seasonal constraints on population genetic structure in eusocial paper wasps

Climate has long been suggested to affect population genetic structures of eusocial insect societies. For instance, Hamilton [Journal of Theoretical Biology 7 (1964) 17] discusses whether temperate and tropical eusocial insects may show differences in population-level genetic structure and viscosity, and how this might relate to differences in the degree of synchrony in their life cycles or modes of nest founding. Despite the importance of Hamilton's 1964 papers, this specific idea has not been tested in actual populations of wasps, probably due to the paucity of studies on tropical species. Here, we compare colony and population genetic structures in two species of primitively eusocial paper wasps with contrasting ecologies: the tropical species Polistes canadensis and the temperate species P. dominulus. Our results provide important clarifications of Hamilton's discussion. Specifically, we show that the genetic structures of the temperate and tropical species were very similar, indicating that seasonality does not greatly affect population viscosity or inbreeding. For both species, the high genetic differentiation between nests suggests strong selection at the nest level to live with relatives, whereas low population viscosity and low genetic differentiation between nest aggregations might reflect balancing selection to disperse, avoiding competition with relatives. Overall, our study suggests no prevalence of seasonal constraints of the life cycle in affecting the population genetic structure of eusocial paper wasps. These conclusions are likely to apply also to other primitively eusocial insects, such as halictine bees. They also highlight how selection for a kin structure that promotes altruism can override potential effects of ecology in eusocial insects.

Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae)

The halictid bees are excellent models for the study of social evolution because greater social diversity and plasticity are observed in the tribe Halictini than in any other comparable taxonomic group. We examine the evolutionary relationships within the subfamily Halictinae (“sweat bees”) to investigate the origins of social behaviour within the tribe Halictini. We present a new phylogeny of the subfamily Halictinae based on three nuclear genes (elongation factor-1 alpha, wingless, and long-wavelength rhodopsin) and one mitochondrial gene (cytochrome c oxidase 1) sequenced for 206 halictine bees. We use model-based character reconstruction to infer the probability of a shared eusocial ancestor for the genera Halictus and Lasioglossum, the two genera of Halictini which display eusociality. Our results suggest a high probability for a single origin of eusociality for these two genera, contradicting earlier views of separate origins within each taxon. Fossil-calibrated divergence estimates place this ancestor at approximately 35million years ago, about 14million years earlier than previous estimates of eusocial origins in the halictid bees.

New Species of Macrocephalic Halictine Bees (Hymenoptera: Halictidae)

Two new species of New World halictine bees (Halictidae: Halictinae) are described and figured with extreme forms of female macrocephalism. Lasioglossum (Evylaeus) xitle sp. nov. (Halictini: Gastrohalictina) from Cráter del Xitle in Mexico City, Mexico and Augochlora (Oxystoglossella) empusa sp. nov. (Augochlorini: Augochlorina) from Madre de Dios, Peru are remarkable for not only their greatly enlarged heads and monstrously developed mandibles, but also for their pronotal modifications (both species), propodeal lamellae (A. empusa), and genal (L. xitle) and hypostomal (A. empusa) protrusions.

New combinations, sex association, behavioural notes and potential host record for two Neotropical species of Pseudomethoca Ashmead, 1896 (Hymenoptera: Mutillidae)

The present paper transfers Mutilla pumila Burmeister, 1854 and Mutilla pergrata Cresson, 1902 to the genus Pseudomethoca Ashmead, and a lectotype is designated for Mutilla pumila. The male of this species, previously known only from the female sex, is described and the female is redescribed and illustrated for the first time. Sex association was based on laboratory mating trials. Field observations in a montane Atlantic forest site in southern Brazil provided us behavioural notes on attempts of parasitism in nests of the halictine bee Dialictus seabrai (Moure, 1956).

Geographic patterns in the distribution of social systems in terrestrial arthropods

The role of ecology in the evolution and maintenance of arthropod sociality has received increasing research attention in recent years. In some organisms, such as halictine bees, polistine wasps, and social spiders, researchers are investigating the environmental factors that may contribute to high levels of variation in the degree of sociality exhibited both among and within species. Within lineages that include only eusocial members, such as ants and termites, studies focus more on identifying extrinsic factors that may contribute to the dramatic variation in colony size, number of queens, and division of labour that is evident across these species. In this review, I propose a comparative approach that seeks to identify environmental factors that may have a common influence across such divergent social arthropod groups. I suggest that seeking common biogeographic patterns in the distribution of social systems or key social traits may help us to identify ecological factors that play a common role in shaping the evolution of sociality across different organisms. I first review previous studies of social gradients that form along latitudinal and altitudinal axes. Within families and within species, many organisms show an increasing degree of sociality at lower latitudes and altitudes. In a smaller number of cases, organisms form larger groups or found nests cooperatively at higher latitudes and altitudes. I then describe several environmental factors that vary consistently along such gradients, including climate variables and abundance of predators, and outline their proposed role in the social systems of terrestrial arthropods. Finally, I map distributions of a social trait against several climatic factors in five case studies to demonstrate how future comparative studies could inform empirical research.

Structure elucidation of some naturally occurring carbonyl compounds upon coupled gas chromatography/mass spectrometry and micro-reactions

Mass spectrometry coupled with gas chromatography is the ideal tool for structure elucidation of minute amounts of target components contained in complex mixtures. Derivatization of these targets and GC/MS analyses of the reaction products may provide decisive information about the parent compound. Removal of oxygen-containing functional groups may be particularly advantageous. Even when the transformation of a target into an appropriate derivative needs several steps, and corresponding reactions furnish low yields, derivatization is useful. Females of the shrimp Crangon crangon contain (S)-3-hydroxydecanoic acid amide and 3-hydroxy-8-methyldecanoic acid amide. Ketones in the desert locust Schistocerca gregaria proved to be 3,7-dimethylheptacosan-2-one and 3,7,15-trimethylheptacosan-2-one. Double bond positions in unsaturated macrocyclic lactones, which occur in halictine bees, can be easily assigned upon GC/MS after the addition of dimethyldisulfide even when they occur as mixtures of isomers.

Trade-Off between Foraging Activity and Infestation by Nest Parasites in the Primitively Eusocial BeeHalictus scabiosae

Diurnal activities ofHalictus scabiosaebees and their nest parasites (major bee-flies, cuckoo wasps, ichneumon wasps,Sphecodesbees, and velvet ants) were investigated at a study site with 159 nests in Eastern Austria. Foraging activity correlated with ambient temperature only before midday and decreased in the afternoon. The activity of nest-infesting parasites increased during the day and correlated with ambient temperature. The match factorfmbetween the ratios of the foraging activities ofH. scabiosaeand the ratios of aspects of morning temperature was assessed on three consecutive days with different weather. The activity patterns of halictine bees and their nest parasites differed: the parasites exhibited only small time windows in which their activities were synchronised with those of their hosts. The bees exhibited an anticyclic behaviour and collected food in times of low parasite pressure and decreased foraging activity when parasite pressure increased.

Two New Halictine Bees in Miocene Amber from the Dominican Republic (Hymenoptera, Halictidae)

Two new halictine bees (Halictidae: Halictinae) are described and fifrom females preserved in Early Miocene (Burdigalian) amber from the Dominican Republic. Oligochlora semirugosa sp. n. (Augochlorini) is similar to O. micheneri Engel but diff ers in the shape of the pronotal dorsolateral angle, the partially rugulose gena (entirely imbricate in the latter species), and the sculpturing of the face, mesosoma, and metasomal terga. Nesagapostemon moronei gen. n. sp. n. (Caenohalictini) resembles Eickwortapis in the absence of carinae bordering the dorsal horizontal surface of the propodeum while having the vertical posterior surface encircled. Th e genus diff ers from Eickwortapis in the much larger and more robust body size (nearly twice as large), the non-slanting and shorter horizontal surface of the propodeum, sculpturing, and pilosity of the hind legs. A second specimen of O. grimaldii Engel is recorded and a provisional key to halictid bees in Dominican amber is provided.

Case 3476DialictusRobertson, 1902 andEvylaeusRobertson, 1902 (Insecta, Hymenoptera): proposed precedence overHemihalictusCockerell, 1897,SudilaCameron, 1898 andSphecodogastraAshmead, 1899

Abstract. The purpose of this petition, under Articles 23.9.3 and 81.2.3 of the Code, is to give the widely used halictine bee generic names Dialictus and Evylaeus, both proposed by Robertson in 1902, precedence over the rarely used but older names Hemihalictus Cockerell, 1897, Sudila Cameron, 1898 and Sphecodogastra Ashmead, 1899 whenever these names are considered to be synonyms. This proposal is intended to best conserve the standard usage of these names.

Emergence and Consequences of Division of Labor in Associations of Normally Solitary Sweat Bees

AbstractDivision of labor is a pervasive feature of animal societies, but little is known about the causes or consequences of division of labor in non‐eusocial cooperative groups. We tested whether division of labor self‐organizes in an incipient social system: artificially induced nesting associations of the normally solitary sweat bee Lasioglossum (Ctenonomia) NDA‐1 (Hymenoptera: Halictidae). We quantified task performance and construction output by females nesting either alone or with a conspecific. Within pairs, a division of labor repeatedly arose in which one individual specialized on excavation and pushing/tamping while her nestmate guarded the nest entrance. Task specialization could not be attributed to variation in overall activity, and the degree of behavioral differentiation was greater than would be expected due to random variation, indicating that division of labor was an emergent phenomenon generated in part by social dynamics. Excavation specialists did not incur a survival cost, in contrast to previous findings for ant foundress associations. Paired individuals performed more per capita guarding, and pairs collectively excavated deeper nests than single bees – potential early advantages of social nesting in halictine bees.

Subsociality in halictine bees

To look for the occurrence and the significance of brood care in social evolution, I reared six eusocial halictine bee species in laboratory cages enabling the observation of intranest behaviour: Lasioglossum (Evylaeus) laticeps, L. (E.) pauxillum, L. (E.) nigripes, L. (E.) euboeensis, Halictus (Halictus) scabiosae and L. (E.) fulvicorne. All of them were subsocial, each mother caring for her brood. Brood cells were sealed after oviposition with earthen plugs; they were then reopened, visited and closed again. These observations plus the reports in the literature on eleven eusocial species indicate that seventeen species of eusocial halictine bees provide parental care, i.e. are subsocial. Brood care, subsociality, is strongly associated with eusociality. To study reversal from eusociality to subsociality, I have reared the non-eusocial form of two species within which there are or have been eusocial forms: Halictus (H.) rubicundus and Lasioglossum (E.) fratellum. They are secondarily solitary, having lost worker brood. However, both species still show brood care. This suggests that in transitions to eusociality, brood care antedated eusociality. To further examine this issue I reared two truly solitary species that are not derived from eusocial ancestors: Lasioglossum (E.) villosulum and L. (L.) quadrinotatum. Unlike secondarily solitary species, females of both these species close their brood cells after oviposition and ignore their progeny thereafter. This association strongly suggests that the subsocial route with maternal brood care is the route to eusociality in halictine bees.

Biology of a nocturnal bee, Megalopta atra (Hymenoptera: Halictidae; Augochlorini), from the Panamanian highlands

Bees of the genus Megalopta have gained attention as a result of their social nesting and nocturnal foraging. Seventeen nests of Meglaopta atra from the highlands of Chiriqui Province, Panama, were collected at the end of the dry season when brood rearing is expected to be at its peak. Most nests contained single females; within multifemale nests only one female possessed enlarged ovarioles, although some non‐reproductive individuals were inseminated. In two of these nests reproductive individuals were clearly larger in body size than nestmates, but body size variation and macrocephaly were equivalent to those found in other Neotropical augochlorines. There was no evidence of a non‐reproductive worker‐like caste and multifemale nests did not appear to be more productive than solitary nests, which may represent pre‐reproductive assemblages. Megalopta atra appears to be isolated by altitude from co‐geners common in Panama, this is discussed in comparison with temperate halictine bees, in which environmental clines separate solitary from social populations.

Division of labour and socially induced changes in response thresholds in associations of solitary halictine bees

Division of labour is a recurrent property of social groups. Among the different models proposed to explain the origin of division of labour, response-threshold models have garnered strong theoretical and empirical support. These models postulate that task specialization can arise spontaneously from interindividual variation in thresholds for responding to task-associated stimuli. Consequently, individuals with lower thresholds for a given task are more likely to become specialists. Self-reinforcement models expand this hypothesis by proposing that the successful performance of a task lowers an individual's threshold, increasing the probability that it will perform that task again. Although an important component of many models of division of labour, self-reinforcement can be difficult to test in real-world contexts. Here, we asked whether social experience modulates the individual response thresholds of normally solitary individuals. We focused on task performance during the early stages of nest construction in forced associations of the normally solitary halictine bee Lasioglossum (Ctenonomia) NDA-1. Within each pair, a strong behavioural asymmetry arose, with one bee specializing in excavation and her nestmate specializing in guarding the nest entrance. Individual performance of excavation by each bee was compared before and after being paired with a conspecific. After experiencing a social environment, individuals substantially increased their excavation performance. However, bees excavating more frequently in groups did not excavate differentially more afterwards, as would be predicted by self-reinforcement. The social context experienced by bees seems to promote behavioural differentiation leading to task specialization and to modulate response thresholds for excavation.

Hybridization and asymmetric introgression between Rhododendron eriocarpum and R. indicum on Yakushima Island, southwest Japan

We examined natural hybridization between two morphologically and ecologically divergent species on Yakushima Island-the light-purple flowered Rhododendron eriocarpum native to seaside habitats and the red flowered R. indicum native to riverside habitats. By investigation of morphological traits and amplified fragment length polymorphisms (AFLP) we found that hybrid individuals morphologically and genetically intermediate between the two species grow mainly in the seaside areas of the island. The degree of morphological and genetic variation was different among the seaside hybrid populations. Although most pollinator species were exclusive to one of the two flower color groups, the halictine bees of Lasioglossum were observed in both the color types. The crucial interspecific incompatibility after pollination has not been previously described. Geographic distance between the populations is likely to be an important primary factor in bringing about natural hybridization and determining the degree of introgression between R. eriocarpum and R. indicum. The fact that hybrids occur mostly in the seaside area on Yakushima Island indicates that asymmetrical introgression occurs from R. indicum to R. eriocarpum. Alternatively, strong habitat-mediated selection from recurrent floods may prevent the hybrids from colonizing riverside habitats.

Nesting Biology and Social Behavior of Xenochlora Bees (Hymenoptera: Halictidae: Augochlorini) from Perú

Abstract The augochlorine (Halictidae) bee genus Xenochlora is the diurnal sister group to the nocturnal Megalopta, both of which are stem-nesting halictid bees. Here we present notes on the nesting biology and social behavior in four nests of Xenochlora nigrofemorata and one nest of X. ianthina from Madre de Dios, Peru. All nests contained multiple females and dissections of X. nigrofemorata indicated within nest reproductive differentiation among females that is associated with body size. Size variation among females is conspicuous and a variety of morphometrics are examined to document it. A genal index is used to describe cephalic variation, and results are compared with seven other halictine bees. All morphometrics were investigated for measurement error. Nests of Xenochlora appear to be founded by single females and multifemale nests clearly exhibit parasocial behavior and we hypothesize that they temporally switch between semisocial, eusocial and possibly communal phases.