Halictus rubicundus

Halictus rubicundus
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Hymenoptera
Family:	Halictidae
Genus:	Halictus
Species:	H. rubicundus
Binomial name
Halictus rubicundus (Christ, 1791)

Halictus rubicundus is a species of sweat bee found throughout the Northern Hemisphere. H. rubicundus was introduced into North America from the Old World during one of two main invasions of Halictus subgenera. These invasions likely occurred via the Bering land bridge at times of low sea level during the Pleistocene epoch.^[1]

The species exhibits different social behaviors depending on climate: it is a solitary species in cooler regions, but eusocial in warmer areas. Occasionally, solitary and eusocial colonies appear simultaneously in the same population.^[2] The sweat bees are extensively studied for their variability in social behavior, which has become a model for social plasticity.^[3] This variability has contributed to an understanding of social evolution in behavior.^[3]

Taxonomy and phylogeny

Halictus rubicundus is a species of the order of Hymenoptera and family Halictidae, more commonly known as sweat bees.^[4] This common name comes from their known attraction to perspiration.^[4] This species exhibits polymorphic social behavior that varies with environmental conditions, and other species of the family Halictidae are thought to have similar variability in sociality.^[5] The genus Halictus was described by Latreille in 1804.^[1]

Description and identification

A female on a flower

The family Halictidae is unique and easy to identify by its metallic appearance.^[4] Halictus rubicundus specifically are less metallic, but have white stripes on the bottom of their abdominal segment and yellow-orange legs.^[6] The bee is about 1 cm in body length and brown in color, with fine white bands across the apices of the abdominal segments.^[4] The males are more slender, with longer antennae and yellow markings on the face and legs; they can be distinguished from males of similar species by the absence of an apical hair band on the terminal abdominal segment.^[4] In social populations, females of the first brood, the workers, can be identified because they are slightly smaller than the second brood females, the foundresses.^[7]

Both solitary and eusocial types of the species have nests in southward facing slopes built for the entrance of their burrows. This slope maximizes the heat absorption from the sun, making the nest warmer. The in-ground nests are built in isolated areas, consisting of sand or soil. The nests with a favorable slope were thought to increase foraging efficiency of adults and development of larvae with a stable thermal environment.^[8]

Distribution and habitat

Halictus rubicundus live in multiple locations worldwide, including North America and the UK, mostly in temperate climates. It is believed that the differences in latitude actually contribute to their social behavior.^[8] Those living in more northern geographic locations are often more solitary in behavior than those in southern areas. This difference is widely studied, as it provides insight into the evolutionary social behavior from solitary to social. Nests are haplometrotic, meaning that they are founded by single females. The species lives in burrowed nests in the ground, where there is a constructed slope to provide thermal regulation of the nest.^[8] This regulation is important for the development of both the eggs and the larvae.^[9] Stones or areas of vegetation are usually found near nest entrances, likely because of the heating properties of these objects.^[8] A higher temperature increases the rate at which the larvae reach the threshold to gain the ability to fly.^[9] Therefore, a warmer nest leads to an increased rate of development of the offspring.

The nests can be up to 120 mm deep, and are constructed in a wide range of soil types.^[9] These common bees are well studied for the evolution of their social behavior.^[3] Because social nests produce more offspring than solitary nests, social nests will burrow further into the ground, as the second brood of the social population will be nested beneath the first brood. Females typically nest in dense packs, likely because the nesting females are relatives and demonstrate philopatric behavior.^[8]

Nesting

H. rubicundus burrow among pebbles, dug by a female

Halictus rubicundus is distributed throughout the Holarctic region. There are two nest types, social and solitary. Social populations typically nest in warmer regions, such as Kansas and southern Ontario, while solitary populations nest in cooler regions, such as Scotland and Alaska. In marginal regions, both social and solitary behavior can be found in different nests of the same population. The solitary phenotype is expressed as a response to colder environments because the warm season is not long enough to produce sequential worker and production broods.^[8]

Soil hardness

The nests are burrowed into the ground in loam soil.^[8] Halictus rubicundus has a high tolerance for soil hardness. Soil hardness affects the density of nesting. Females prefer to nest in softer ground as they spend less energy and time excavating the nest. Unlike the similar species Lasioglossum zephyrum^[10] that build nests in close proximity to each other, this sweat bee prefers to spread out. Foundresses will choose to build their nests in patches of softer ground until they reach the critical nearest-neighbor distance of about 50 mm, at which point the close spacing poses a high risk of the nests collapsing. At this point, further foundresses would be forced to build their nests in harder soils where the nests could be built closer together without compromising nest architecture. Foundresses may test the hardness of the soil by biting into the surface or performing a short test dig.^[9]

Temperature

Nest temperature determines egg development and foraging active time of females. As long as temperatures do not reach lethal thresholds, developmental rates of offspring will increase with temperature. Higher temperatures will also increase the thoracic temperature and allow females to fly more rapidly. With increased speed in flight, females are allowed more time for foraging, mating, and excavating nests.

Most nests of H. rubicundus are south facing and sloped because of this desire for increased temperature in nesting sites. Based on the distribution of this species, facing the south maximizes the period of time sunlight is shining directly on the nest. Sloping substrates increase the surface area of the nest and allow for higher absorption of sunlight. In order to test the temperature of the substrate, females often spend several seconds basking at various points on the ground while searching for nesting sites.^[9]

Soil water content

The water content of the substrate in which foundresses build the nest is highly important. Waterlogging must be avoided by using well-drained soils, which provides another advantage to building in sloping ground. However, there must be an adequate moisture level to prevent desiccation of the brood cells. For this reason, soil samples of the nests of H. rubicundus have a relatively high humidity.^[9]

Colony cycle

H. rubicundus’s annual colony cycle is dependent both on hibernation and mating schedules.^[11] After hibernation during the winter, female foundresses who mated the previous cycle emerge in the spring.^[11] They each create their own nests in late spring, where they rear a single brood.^[11] Females are more likely to build nests where there is a warmer surface temperature, as this indicates a warmer interior of the nest for the offspring to develop more quickly.^[9] The worker bees provide pollen as food to the larvae.^[8] The gyne will continue to forage for 3–5 weeks, after which she will stop provisioning food to the brood cell.^[8] The brood cells are left inactive for 1–2 weeks before the emergence of the first brood. The first brood emerges in mid to late June. Most females emerging from the first brood will stay with their natal nest and act as foraging workers.^[9]

After the first brood emerges, the daughters will collect pollen on which the foundresses will resume laying eggs. Immediately after mating, the females undergo hibernation for the winter again, and the colony cycle begins again.^[8]

Sociality Effects on Colony Cycle

The annual cycle differs slightly for eusocial and solitary bees, in terms of the number of worker bees and foundresses that are born in the broods. For example, in solitary populations, the females’ first brood rears 40% females who are all able to mate before the next hibernation season.^[11] However, in eusocial populations, the emergence from hibernation occurs about a month earlier, and results in a brood with mostly worker females.^[11] Nesting for solitary populations begins between May and June. The absence of a brood of female workers defines this nest type as solitary, so solitary populations produce only one reproductive brood that is provisioned by a gyne. The emergence of this brood is at approximately the same time as the emergence of the second brood in the social colony cycle. Upon emergency, the offspring mate and then females enter hibernation away from the nesting site. As in social colonies, the males and nest foundresses die at the end of the season.^[8]

Behavior

Halictus rubicundus is widely studied for their variability in behavior depending on geographic location. Those in the south are known to exhibit eusocial behavior, while those in the north are known to be solitary.^[12]

Dominance hierarchy

There is a caste-like system in H. rubicundus.^[12] The dominant motherly behavior often drives away the offspring, but oftentimes, female offspring stay despite this aggressive behavior.^[12] These categories are not thought to be genetically specified, but rather decided by mating behaviors and social factors in the first few days of adulthood.^[13] In this hierarchy, there is a foundress, which is a gyne that is always mated and starts their own colony after hibernation each cycle.^[12] She is considered the foundress queen if she is the dominant one in the colony who reproduces. A gyne is any female with the potential to become a nest foundress.^[12] Below that is a non-gyne, which is a female that stays in an existing colony and often does not mate or reproduce.^[12] Within these non-gynes, there are some who are considered replacement queens, which can sometimes take the place of a foundress queen in the colony.^[12] At the bottom of the caste system are the workers, which help maintain the functions of the colony, including foraging.^[12]

Division of labor

The division of labor differs in eusocial and solitary colonies. In eusocial colonies, it is similar to that in other eusocial bees.^[5] In these colonies, the first brood is primarily worker-females, which in turn help the foundress rear her second brood.^[5] The second brood yields gynes and males, which breed to repeat the cycle.^[5] However, in non-eusocial colonies, the first brood yields reproductives, but usually not workers.^[5] The cooperative breeding behavior of worker bees in eusocial colonies benefits them because their actions maintain the colony and the fitness of the queen foundress.^[14] They benefit by helping their mother raise the second brood, according to the kin selection hypothesis.^[14] By assisting with foraging and feeding the larvae, as well as maintaining the proper functioning of the nest and colony, they help the second brood develop and reproduce to pass down the genes they share.^[14] However, in solitary colonies, the offspring do not serve as workers and do not help the mother establish a second brood, but rather go off to try to establish nests of their own.^[14]

There is no evidence for predetermined morphological or physiological differences in caste for H. rubicundus. The differentiation into different castes is based on behavior. Females that do not mate immediately after emergence become workers or replacement queens while the others become gynes.^[13] Another factor that may dictate the role of a female is the relative abundance of males to newly emerged females. There will be a higher percentage of gynes relative to non-gynes when there are an abundance of males.^[2]

Mating behavior

Unlike other bee species that mate in the air, mating in H. rubicundus occurs on the ground in and around the nest aggregation. Males hover around their natal nest and wait to encounter females that are entering or leaving a surrounding nest.^[8] After mating, females enter a dormant state, diapause, and restart the cycle the following spring.^[13]

In this species, there are foundresses, gynes, non-gynes (who can be replacement queens), and worker females. The foundresses are those who are virtually guaranteed to mate before the winter hibernation begins.^[12] The gynes and non-gynes are distinct groups, as gynes are likely to mate and become foundresses, while non-gynes are not.^[12] However, it is theorized that male abundance could possibly play into this distinction early in life.^[12] If there is an abundance of males, a virgin female could mate early in life, before diapause, and make a caste switch into being a gyne.^[12] If she is left unmated, however, she will likely stay a non-gyne.^[12] This caste-determination occurs in the first few days of the female's life, and depends highly on male availability.^[12] The first brood that a foundress has usually rears gynes, non-gynes, and some males.^[12] The second brood has gynes and males only.^[12] Halictus rubicundus is one of the first species discovered to have first broods with both gynes and non-gynes.^[12] It was previously thought that the non-gynes were all produced in the first brood and the gynes in the second brood.^[12]

Nest-site fidelity

Nest-site fidelity may be due to one of three reasons.

1. Philopatry is the tendency for adult bees to nest near parental nest. Returning to the natal nest is beneficial because the nest must have been successful enough to produce adults for one year, so it is assumed to be in good enough condition to raise another brood. This prevents H. rubicundus from taking the risk of settling in a failing nest.
2. Habitat learning describes the process through which females recognize characteristics of the nest from which she came and chooses to nest in similar conditions. Although this is different from philopatry in that she will not purposely choose to be near her previous nest and will make selections based on environmental factors, the nest the female chooses will often still be near her original nest.
3. Social facilitation may influence the nesting location chosen by a female because the benefits of nesting close to other bees may outweigh the costs of finding a new location with a suitable substrate.^[9]

Gregarious nesting

Dense nesting tendencies of H. rubicundus are most likely due to the following three factors:

1. There is a limited amount of suitable substrate in which the bees can build their nests, so they must build many nests packed tightly together without compromising the structural integrity of the nest.
2. As mentioned earlier, philopatry is an important factor in maintaining an aggregation. The search for a new nesting site requires a lot of resources, so females will likely limit their dispersal and stay near their natal nest sites.
3. Hymenopteran and dipteran species may attach the ground nest of H. rubicundus. Although it would seem that aggregation of nesting would increase the mortality due to parasitism as they would be more conspicuous, it is likely that there is a dilution effect that reduce mortality by parasitism.^[9]

Kin selection

Genetic relatedness within colonies

Depending on the geographic location of the colony and its behavior, genetic relatedness within the colonies differs once again. In colonies in the north that exhibit solitary behavior, the genetic relatedness is different because the first brood does not yield worker bees who help the mother raise the following brood.^[14] Therefore, there are no workers to help the mother and each of the gynes goes to establish its own nest, which means the colonies are not genetically related.^[8] In colonies that are established further south, where they practice eusocial behavior, they are genetically related within the colonies. For example, the first brood, which yields several workers, helps the foundress in her colony.^[12] The first brood therefore stays in the colony, and is directly genetically related to the mother by half, and helps to raise the second brood, which is also related to them by half.^[5]

Genetic relatedness among colonies of different behaviors

There are colonies both of eusocial and solitary behavior that have been studied for environmental differences and genetics. It has been shown that there is a stronger link of genetic relatedness between two colonies with similar behavioral patterns, than those of closer geographic distance and different social behaviors.^[5] This does not necessarily mean that social behavior is governed by certain genes, but it could be linked to certain genetic lineages that are more suited for certain environments.^[5] Although there is much more studying that must be done on the correlation between genetics and the environment and social behavior, it has been recorded that there is some sort of link between the three parameters.^[5] Evolutionary characteristics are involved in the crosslink between the northern populations of H. rubicundus having more solitary behavior, and the southern populations being eusocial.^[5] It is a possibility, however, than this link was brought on by environmental control of sociality, rather than a purely genetic standpoint.^[5]

Pheromone recognition

Halictid bees have a gland known as the Dufour’s gland that extends throughout the abdomen. It is found primarily in female Hymenoptera. The Dufour’s gland, which is associated with the sting structure, secretes fluids that are important for socioecological functioning.^[15] In H. rubicundus, the Dufour’s gland produces pheromones that may aid females in recognizing brood cells as well as other individuals in the nest.^[9]

Costs and benefits of sociality

In each different environment, there have been adaptations to minimize the costs and maximize the benefits of their social behavior. In bees with solitary behavior, the cold environments have likely allowed for this behavior because of shorter breeding seasons.^[11] Having shorter growing seasons would degrade the possibility of having a second brood in the same season, which changes the behavior of the worker bees.^[11] There would be no benefit to the worker bees to stay with the mother and help her maintain the colony, as she would not be able to produce another brood that season, so there would be kinship selection benefits. Instead, the first brood in a colony of solitary behavior consists of many gynes, which are potential foundresses, who must mate before the short season is over in order to establish their own colony the following year.^[11] On the other end of the spectrum, the populations that exhibit eusocial behavior had completely different costs and benefits to their sociality. As discussed in the section about genetic relatedness, there are benefits to worker bee behaviors in eusocial colonies, as workers are related to the foundress and the next brood.^[14] Thus, by kin selection, it is beneficial to the workers who cannot mate to help the mother reproduce a healthy second brood that can then pass on half of the same genes they share. However, it is costly to the workers to be in this social environment because they cannot reproduce themselves and directly pass down the genes that they have. In both situations, however, it is more beneficial to exhibit the certain social behavior that they do, than to find an alternative strategy of sociality.

Sex ratio in different colonies

Social colony

In the social colony where there are two broods in one cycle, there are different sex ratios for each brood.^[8] The first brood will contain 75–100% females to provide plenty of workers for the nest to help the mother produce a second brood.^[7] The second brood is slightly male-biased, resulting in a sex ratio of about 60% males. The products of the second brood will act as reproductives (both the males and females).^[8]

Solitary colony

In solitary populations, nesting begins later and only one brood is produced.^[7] The brood has a sex ratio made up of 60% males, similar to that of the second brood in social colonies. This brood is also produced at about the same time that the second brood is produced in social populations so that the colony cycle ends at about the same time.^[8]

Sex ratio effects on sociality

Male abundance and ability to mate have a major effect on deciding the social behavior of a non-gyne versus gyne bee. Therefore, the sex ratio is important to consider. Warmer temperatures for the first brood of a foundress in the spring leads to a higher ratio of male to female offspring.^[2] The best predictor for a female's fate in being a gyne or a non-gyne depends on the male abundance in proportion to virgin females.^[2] This sex ratio is affected by temperature and photoperiod of the male egg production.^[2] One hypothesis suggests that this male bias largely decides the demographic of the colony or population, which influences the sociality that is seen in that population, whether it be largely populated by gynes who go off to create their own nests, or non-gynes who stick around to stay in their nesting colony with their foundress.^[2]

Hierarchy conflict

There is a social caste system in the H. rubicundus species that is affected not solely by genetics, but behaviors in the first few days of adult life. In studying these bees however, it was found that foundresses were never worker bees, and only about five percent of all foundresses ever carry pollen.^[13] The future foundresses were observed leaving the nest within a few days of their adulthood.^[13] Males do not overwinter, so they must find a mate before the female hibernates for the winter.^[13] Because there is no predetermined physiological change in the females that decide what level in the caste system they will be, it can be inferred that this is determined by behavioral conditions.^[13] Therefore, this hierarchy is established by the solitary or eusocial behavior that the population exhibits and the foundress's control over the behavior of its broods. The females must actively seek a mate within the first few days of its life if it wants to leave it's mother's nest and have a life as a gyne and potential foundress.^[13]

Body size as a result of temperature

Temperature affects the size of offspring in Halictus rubicundus, but there are two hypotheses that offer explanations as to why such is the case:

• At optimum temperatures, the maximum offspring size will be produced. Smaller sizes will be the result of both higher and lower temperatures based on differing stresses. So varying conditions around one optimum temperature will lead to different offspring sizes.
• Extreme temperatures may reduce flowering and therefore have an indirect effect on cell provisioning. If temperatures are lower than optimum, lower flowers will be produced and fewer resources will be available to increase growth of offspring.^[8]

Parasites

Halictus rubicundus are parasitized by other hymenopteran species. Although it would seem as though nesting in dense groups would draw attention to aggregations and increase mortality by parasitism, such is not observed to be the case. Because the sweat bees nest densely, it can be assumed that there is a large dilution effect that proportionally decreases mortality rates by parasites.^[9]

References

External links

• Media related to Halictus rubicundus at Wikimedia Commons