Lasioglossum malachurum

Lasioglossum malachurum
Female
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Hymenoptera
Family:	Halictidae
Genus:	Lasioglossum
Subgenus:	Evylaeus
Species:	L. malachurum
Binomial name
Lasioglossum malachurum (Kirby, 1802)

Lasioglossum malachurum is a small European halictid bee.^[1] This species is obligately eusocial, with queens and workers, though the differences between the castes are not nearly as extreme as in honey bees.^[2] Early taxonomists mistakenly assigned the worker females to a different species from the queens. They are small (~1 cm), shiny, mostly black bees with off-white hair bands at the bases of the abdominal segments.^[1] L. malachurum is one of the more extensively studied species in the genus Lasioglossum, also known as sweat bees. Researchers have discovered that the eusocial behavior in colonies of L. malachurum varies significantly dependent upon the region of Europe in which each colony is located.^[3]

Taxonomy & phylogeny

L. malachurum was described by the entomologist William Kirby in 1802. This species of bees fall within the genus Lasioglossum, which is the largest bee genera.^[1] Lasioglossum falls within the family Halictidae, which includes small to midsize bees and is commonly referred to as the sweat bee family because Halictidae are frequently attracted to human perspiration.^[4] L. malachurum falls within the order Hymenoptera, a large order of generally winged insects containing wasps, bees, and ants. One species of lasioglossum that is closely related to the L. malachurum is L. hemichalceum.^[5]

Description

Caste dimorphism

Physical size is a major distinguishing feature between queens and gynes versus female worker bees. Queens consistently demonstrate larger body size than workers. Queens also tend to have worn wings and worn mandibles as a result of higher activity, in addition to greater ovarian development correlating with the reproductive capacity of queens. Queens also generally have abundant fat stores.^[3] This physical dimorphism persists throughout all stages of the life cycle, from pupae to adult. Rarely, queens can be abnormally small to the size of a worker, but abnormally large workers have never been observed in the wild.^[1]

Nest identification

The sweat bee has a simple nesting architecture consisting of a vertical tunnel into the ground ending in a compartment reserved for brood-rearing.^[3] They nest underground, like Lasioglossum zephyrum, but they do not form the same complex structures.^[6] Nest entrances are frequently concealed using scattered foliage.^[7] For L. malachurum, thousands of nests can be found located within a small region in nesting aggregations, which suggests that the bees likely have some sort of identification mechanism for their own specific nests. In fact, nest entrances and brood cell linings are both impregnated with secretions from the Dufour's gland of the bee, which plays a role in nest orientation.^[8] Nests are dug into hard, compact soil and can be sealed from within by the queen using her abdomen. Because nests are dug into hard soil, construction of a nest represents a significant energy expense to a queen, which explains why gynes frequently usurp other nests rather than founding one of their own.^[9] L. malachurum is a Western Palaearctic species and nests can be found across Southern England and the Channel Islands, most of continental Europe, and North Africa.^[10][11]

Distribution & habitat

L. malachurum is found across England, continental Europe, and northern Africa and is therefore capable of inhabiting a broad range of habitats and climates. Differences in the climes of the various habitats can frequently impact the social behavior of L. malachurum within that habitat. The length of summer, for example, can affect the length of the breeding season and thereby impact the number of broods a queen may have. The longer breeding seasons in Southern Europe can also lead to reproductive capacity in worker bees, making L. malachurum in those regions not purely eusocial.^[3] Female workers in southern European colonies of L. malachurum consequently have significantly more developed ovaries than their counterparts in northern European colonies.^[1]

Due to the relatively broad range of nesting habitats that the species resides in, L. malachurum is subject to a myriad of climate-based selective pressures that cause a differential in behavior dependent upon location. Researchers have identified a tendency for L. malachurum in southern European climes to be characterized by more activity and the production of more worker broods prior to the production of a gyne brood, whereas L. malachurum in northern European climes exhibit less activity and only a single worker brood prior to the gyne brood.^[1][12]

Colony cycle

The queens of L. malachurum, following fertilization the previous year, begin to appear in the spring, when plenty of food sources are available to sustain them after the long overwintering period. Although several females usually outwinter in the same burrow with little conflict, they start to act aggressively until a single female is left in possession of the burrow, leaving the evicted females to obtain or excavate burrows of their own.^[1]

Each female in possession of a nest tunnel then begins to build brood cells in short side passages which she excavates to the side of the main passage. Immediately following construction each brood cell is mass-provisioned with a mixture of pollen and nectar in the form of a firm, doughy mass. An egg is laid on each pollen mass and the individual cell sealed by the female. Each egg takes 22 days to develop from an egg to a full adult.^[13] She then goes on to construct more, similar cells containing eggs and pollen masses.^[1] During this time, before the first worker brood has emerged, containing only about five workers, the foundress queen will frequently leave the nest in order to find provisions to build the brood cells of the nest. These nest absences are accompanied by high risk of intraspecific usurpation.^[2] Once the brood is provisioned, the queen will seal the nest synchronously with all other queens in the aggregation, and all above ground activity will cease for three weeks.^[9]

By the end of May, larvae from the earliest eggs are full grown and start pupation, emerging from their cells by mid-June. For bees in cooler climates with shorter breeding seasons, these adults are all non-reproductive female workers, somewhat smaller than their mother. The original maternal female bee remains within the nest and guards the entrance to the burrow, now acting as a queen while her non-reproductive daughters act as workers; they go out foraging for food and help in the construction of new brood cells, in which the queen lays new eggs.^[1] For bees in warmer climates with longer breeding seasons, some of the female workers have reproductive capacity and can help breed up to two subsequent worker broods before the eventual gyne brood.^[3]

By the beginning of August, males begin to emerge from the final brood of the season. Several days later, reproductive females begin to emerge as well, who are morphologically similar to their queen. During sunny weather, the nest aggregation becomes a lek and the males vie for territory on the ground.^[7] the males mate with the new reproductive females (from both their own and separate nests), although they do not attempt mating with the non-reproductive females. Impregnated females may continue to live in their mothers' nests, although it is thought that they only forage for their own food and do not contribute to the rest of the nest.^[1]

With the arrival of the colder autumn weather the males and non-reproductive females die off, and the impregnated reproductive females go on to spend the winter in diapause and repeat the life cycle the following year. The life cycle is longer, with two successive broods of workers, farther south in Europe where conditions are warmer and the season longer.^[1][12] Soil temperature specifically has been linked to decreasing the overall length of the nesting cycle.^[13] Workers in warmer soil tend to require less time to provision a new brood, possibly because they have more active time each day.^[13]

Behavior

Dominance hierarchies

L. malachurum colonies are monogynous. Although the queen coordinates the workers within the nest, the workers can exert pressures on the queen as well. Because queens frequently are replaced through usurpation and queen turnover, the workers within a nest will be less related to the queen than expected. As such, the workers are less likely to cooperate with the queen based on maximizing their own fitness. In order to get the workers to remain with the nest and continue to aid her own offspring, the queen will often cede reproduction to alien workers.^[2] These workers can produce males or gynes and have high rates of reproduction. They do not, however, overwinter, nor are they morphologically similar to a queen or gyne.^[3] The length of life span for the queens may be a factor that leads to more reproductive workers in southern climes that have longer breeding seasons; in northern climes, where the queen is generally alive for production of gynes, workers are less likely to be reproductive. In southern climes, where the queen frequently does not survive to gyne production, workers are more likely to be reproductive.^[1]

Communication & recognition

Male-Female communication

Communication between male and female L. malachurum is mediated using pheromones.^[2] Virginal queens attract males through a sex hormone that mated queens lack; thus, males are much more attracted to younger queens. The chemical distinctions between the pheromones released by virginal and mated queens are significant in terms of proportions of hydrocarbons and lactones. Whereas isopentenyl esters, unsaturated fatty acids, and hydrocarbons are far more abundant in the chemical makeup of a virginal queen's hormones, the old queen's hormones are more likely to be made up of largely macrocyclic lactones. This chemical distinction between virginal and old females allows males to distinguish between the two and thus exert male choice in sexual partner. They are also capable of discriminating between familiar and unknown queens and will generally be more attracted to queens of a foreign colony. This attraction to foreign queens likely arose as an outbreeding mating strategy, which would increase genetic diversity of the population and decrease the probability that the next generation would be subject to genetic disease.^[8]

Nest recognition

Because L. malachurum generally nests within aggregations of thousands of colonies within a small region, the ability of bees to recognize their own nests is crucial. Outside the entrances to the nest, guards are posted. These guards mark the nest entrances with Dufour's gland secretions in order to create olfactory cues to guide colony specific bees back to the nest. These secretions are largely made up of alkanes and alkenes.^[8] Bees of the species L. malachurum also rely on visual cues and landmarks in order to determine where their nests are, which they establish through orientation flights and continuously update through re-orientation flights.^[14]

Nestmate discrimination

Nestmates are able to identify other nestmates using olfactory cues as well. Chemical similarities, specifically in non-volatile alkenes and alkanes, provide this cue. Notably, the component of discrimination is not based on kinship but on shared nesting site, and individual bees of L. malachurum will not behave differently toward related nestmates and non-related nestmates. In a given nest, the many different compounds mix together to form a gestalt odor that marks all of the members of the nest. This form of scent blending is found commonly among other members of Hymenoptera including certain bees, wasps, and ants. The gestalt bouquet of odors differs significantly in terms of chemical composition in between different nests.^[15]

Usurpation

Queens frequently can be usurped by intraspecific gynes, because the creation of a new nest is a significant energy investment for gynes.^[9] The probability of a colony usurpation increases steadily as the season progresses, most likely because the probability of a gyne having the time and resources to found a new colony and produce new workers decreases.^[2] The increasing risk of usurpation may play a role in the small worker broods, because the queen ceases foraging and seals her nest in mid-May in order to protect from usurping gynes.^[2] Early nest closure has been favored by pressure from usurpation and has developed into an evolutionarily stable strategy.^[9] It might also explain why queens are highly aggressive toward other conspecific queens.^[2] In confrontations between foundresses and usurping gynes, female size is a significant determinant of outcome because it give the queen or usurper a significant advantage. Although they have a physical advantage in usurpation, larger queens are more likely to found their own nest rather than usurp another.^[9]

Mating behavior

The nest aggregation of thousands of colonies that persists throughout the year becomes a lek mating system on warm summer days in the latter half of the breeding season (July through September). The daily operational sex ratio has far more males than females, which is common in a lek mating system and among other bees.^[7] The lek mating is a system in which a large group of males cluster at sites visited by females for mating.^[16] Males are attracted during mating by a mix of olfactory cues produced in multiple glandular sources from the female. Males will seek out unrelated, unmated females; because females are only receptive for a short period following their emergence, males must seek out and find an unmated gyne before the large number of other males.^[7] Mating can occur either in the female's nest or on flowers. Queens can be polyandrous, but only rarely do they actually mate with multiple males. Most colonies arise from only one queen and one male.^[2]

Aggression

Aggression is commonly seen between conspecifics of all halictid bees; especially between usurper females, drawn out fights can occur that last for nearly a half-hour and result in damage to or loss of limbs and body parts. Guard bees of the L. malachurum species, which are workers that defend the nest, also demonstrate antagonistic behavior toward non-nestmate conspecifics, by orienting their stingers toward the intruders or blocking the entrance to the nest with their abdomens. They are able to discriminate between non-nestmates and nestmates, whom they allow to pass with ease. Foragers, on the other hand, are either unable to discriminate between nestmate conspecifics and non-nestmate conspecifics or are uninterested in pursuing aggression against non-nestmate conspecifics, and therefore exhibit high levels of tolerance toward all conspecifics.^[17]

Pollination

L. malachurum bees are polylectic, meaning that they collect pollen from a broad range of unrelated plant species. Although L. malachurum display opportunism when selecting flowers from which to extract pollen, they will generally narrow their selection of pollen during a given collection period. The species therefore demonstrates floral consistency, and will generally only collect from one pollen source during a given pollen flight. The pollination behavior of L. malachurum may be useful for humans to cultivate and develop, because the bee has been implicated in pollinating species of plants that are commonly used by humans for food and for medication.^[18]

Parasites

L. malachurum colonies are parasitized by the kleptoparasitic species of the genus Sphecodes. The bees of this genus have developed a strategy for invading the nest of host species that involves avoiding interaction with any host individuals. The parasites generally parasitize L. malachurum nests during the early spring when the foundress queens need to leave their nests unattended in order to forage. Other species will enter guarded nests during the second brood cycle and kill the guard as well all other present host individuals, before laying eggs in the brood cells. After oviposition, the parasite will close the brood cells to prevent the host female from returning and replacing the parasite eggs. Because the parasites in the genus Sphecodes parasitize a broad range of other bee species, there are few adaptations to the specific L. malachurum bee colonies.^[19]

References

1. Wyman, L.M.; Richards, M.H. (27 January 2003). "Colony social organization of Lasioglossum malachurum Kirby (Hymenoptera, Halictidae) in southern Greece" (PDF). Insectes Sociaux 50: 201–211. doi:10.1007/s00040-003-0647-7. Retrieved 26 September 2015.
2. Paxton, Robert J.; Ayasse, Manfred; Field, Jeremy; Soro, Antonella (2002-11-01). "Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee, Lasioglossum malachurum, as revealed by microsatellites". Molecular Ecology 11 (11): 2405–2416. doi:10.1046/j.1365-294X.2002.01620.x. ISSN 1365-294X.
3. Richards, Miriam H (2000-01-01). "Evidence for geographic variation in colony social organization in an obligately social sweat bee, Lasioglossum malachurum Kirby (Hymenoptera; Halictidae)". Canadian Journal of Zoology 78 (7): 1259–1266. doi:10.1139/z00-064.
4. "Sweat Bees". Missouri Department of Conservation.
5. Danforth, Bryan N.; Eardley, Connal; Packer, Laurence; Walker, Kenneth; Pauly, Alain; Randrianambinintsoa, Fano José (2008-01-01). "Phylogeny of Halictidae with an emphasis on endemic African Halictinae". Apidologie 39 (1): 86–101. doi:10.1051/apido:2008002. ISSN 0044-8435.
6. Batra, Suzanne W. T. (1964-06-01). "Behavior of the social bee,Lasioglossum zephyrum, within the nest (Hymenoptera: Halictidæ)". Insectes Sociaux 11 (2): 159–185. doi:10.1007/BF02222935. ISSN 0020-1812.
7. Ayasse, Manfred; Engels, Wolf; Lübke, Gunter; Taghizadeh, Timo; Francke, Wittko (1999-02-01). "Mating expenditures reduced via female sex pheromone modulation in the primitively eusocial halictine bee, Lasioglossum (Evylaeus) malachurum (Hymenoptera: Halictidae)". Behavioral Ecology and Sociobiology 45 (2): 95–106. doi:10.1007/s002650050543. ISSN 0340-5443.
8. Ayasse, M.; Engels, W.; Hefetz, A.; Tengö, J.; Lübke, G.; Francke, W. (1993-03-01). "Ontogenetic patterns of volatiles identified in Dufour's gland extracts from queens and workers of the primitively eusocial halictine bee,Lasioglossum malachmum (Hymenoptera: Halictidae)". Insectes Sociaux 40 (1): 41–58. doi:10.1007/BF01338831. ISSN 0020-1812.
9. Zobel, Marion U.; Paxton, Robert J. (2006-10-25). "Is big the best? Queen size, usurpation and nest closure in a primitively eusocial sweat bee (Lasioglossum malachurum)". Behavioral Ecology and Sociobiology 61 (3): 435–447. doi:10.1007/s00265-006-0271-4. ISSN 0340-5443.
10. "Lasioglossum malachurum (Kirby, 1802) | BWARS". www.bwars.com. Retrieved 2015-09-26.
11. "Lasioglossum malachurum -- Discover Life". www.discoverlife.org. Retrieved 2015-09-26.
12. Soro, A.; Ayasse, M.; Zobel, M. U.; Paxton, R. J. (2008-10-25). "Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum". Insectes Sociaux 56 (1): 55–63. doi:10.1007/s00040-008-1037-y. ISSN 0020-1812.
13. Weissel, N.; Mitesser, O.; Liebig, J.; Poethke, H.-J.; Strohm, E. (2006-11-09). "The influence of soil temperature on the nesting cycle of the halictid bee Lasioglossum malachurum". Insectes Sociaux 53 (4): 390–398. doi:10.1007/s00040-005-0884-7. ISSN 0020-1812.
14. Brünnert, U.; Kelber, A.; Zeil, J. (1994-09-01). "Ground-nesting bees determine the location of their nest relative to a landmark by other than angular size cues". Journal of Comparative Physiology A 175 (3): 363–369. doi:10.1007/BF00192995. ISSN 0340-7594.
15. Soro, Antonella; Ayasse, Manfred; Zobel, Marion U.; Paxton, Robert J. (2010-10-22). "Kin discriminators in the eusocial sweat bee Lasioglossum malachurum: the reliability of cuticular and Dufour’s gland odours". Behavioral Ecology and Sociobiology 65 (4): 641–653. doi:10.1007/s00265-010-1066-1. ISSN 0340-5443.
16. Beehler, Bruce; Foster, Mercedes (February 1988). "Hotshots, Hotspots, and Female Preference in the Organization of Lek Mating System". The American Naturalist 131 (2): 203–219. doi:10.1086/284786.
17. Polidori, Carlo; Borruso, Luigimaria (2011-06-19). "Socially peaceful: foragers of the eusocial bee Lasioglossum malachurum are not aggressive against non-nestmates in circle-tube arenas". acta ethologica 15 (1): 15–23. doi:10.1007/s10211-011-0103-z. ISSN 0873-9749.
18. Polidori, Carlo; Rubichi, Alice; Barbieri, Valeria; Trombino, Luca; Donegana, Marta (11 December 2009). "Floral Resources and Nesting Requirements of the Ground-Nesting Social Bee, Lasioglossum malachurum (Hymenoptera: Halictidae), in a Mediterranean Semiagricultural Landscape". Psyche 2010: 1–11. doi:10.1155/2010/851947. Retrieved 26 September 2015.
19. Sick, M.; Ayasse, M.; Tengö, J.; Engels, W.; Lübke, G.; Francke, W. (1994-01-01). "Host-parasite relationships in six species of Sphecodes bees and their halictid hosts: Nest intrusion, intranidal behavior, and Dufour's gland volatiles (Hymenoptera: Halictidae)". Journal of Insect Behavior 7 (1): 101–117. doi:10.1007/BF01989830. ISSN 0892-7553.