Bombus terrestris

Last updated

Bombus terrestris
Bombus terrestris.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hymenoptera
Family: Apidae
Genus: Bombus
Subgenus: Bombus
Species:
B. terrestris
Binomial name
Bombus terrestris
Synonyms [1]
  • B. africanusVogt in Krüger, 1956
  • B. audax(Harris, 1776)
  • B. canariensisPérez, 1895
  • B. dalmatinusDalla Torre, 1882
  • B. lusitanicusKrüger, 1956
  • B. maderensisKrüger, 1956
  • B. terrestriformisErlandsson, 1979
  • B. xanthopusKriechbaumer, 1870

Bombus terrestris, the buff-tailed bumblebee or large earth bumblebee, is one of the most numerous bumblebee species in Europe. It is one of the main species used in greenhouse pollination, and so can be found in many countries and areas where it is not native, such as Tasmania. [2] Moreover, it is a eusocial insect with an overlap of generations, a division of labour, and cooperative brood care. The queen is monogamous which means she mates with only one male. B. terrestris workers learn flower colours and forage efficiently.

Contents

Taxonomy and phylogenetics

B. terrestris is part of the order Hymenoptera, which is composed of ants, bees, and wasps. The family Apidae specifically consists of bees. It is also part of the subfamily Apinae. There are 14 tribe lineages within Apinae, and B. terrestris is in the bumblebee tribe, Bombini. It is in the genus Bombus , which consists entirely of bumblebees, and the subgenus Bombus sensu stricto. This subgenus contains closely related species such as Bombus affinis , Bombus cryptarum , Bombus franklini , Bombus ignitus , Bombus lucorum , Bombus magnus , Bombus occidentalis , and Bombus terricola . There are nine recognized subspecies: B. terrestris africanus, B. terrestris audax, B. terrestris calabricus, B. terrestris canariensis, B. terrestris dalmatinus, B. terrestris lusitanicus, B. terrestris sassaricus, B. terrestris terrestris and B. terrestris xanthopus, each with a distinctive coloration scheme. [3]

Description and identification

Ventral view of B. terrestris Dunkle Erdhummel (Bombus terrestris) ventral.jpg
Ventral view of B. terrestris

B. terrestris are pollen-storing bees that generally feed and forage on nectar and pollen. [4] The queen is between 20 and 22 mm long, males range from 14 to 16 mm, and workers from 11 to 17 mm. Workers have white-ended abdomens, and look just like workers of the white-tailed bumblebee, B. lucorum , a close relative, apart from the yellowish bands of B. terrestris being darker in direct comparison. The queens of B. terrestris have the namesake buff-white abdomen tip ("tail"); this area is white as in the workers in B. lucorum. [5] B. terrestris is unique compared to other bees in that their caste of workers exhibit a wide variation in worker size, with thorax sizes ranging from 2.3 to 6.9 mm in length and masses ranging from 68 to 754 mg. [4]

Distribution and habitat

B. terrestris is most commonly found throughout Europe and generally occupies temperate climates. Because it can survive in a wide variety of habitats, there are populations in the Near East, the Mediterranean Islands, and Northern Africa as well. [6] Additionally, it has escaped captivity after being introduced as a greenhouse pollinator in countries where it is not native, so this bee is now considered an invasive species in many of these places, including Japan, Chile, Argentina, and Tasmania. [2] [7] [8] Nests are usually found underground, such as in abandoned rodent dens. [7] [9] Colonies form comb-like nest structures with egg cells each containing several eggs. The queen will lay egg cells on top of one another. Colonies produce between 300 and 400 bees on average, with a large variation in the number of workers. [10]

Colony structure

Social castes

Like in most social bees, there are three main social caste divisions in B. terrestris. This ensures a division of labor and efficient colony functioning. Queens become the main female individual to reproduce in a future colony. There is only one per colony. Her sole responsibility is to lay eggs after she founds a nest. This fate is determined for larvae that receive more food, have longer instar stages, and higher levels of juvenile hormone biosynthesis. [11] Workers, an entirely female caste, mainly forage for food, defend the colony, and tend to the growing larvae. They are usually sterile for most of the colony cycle and do not raise their own young. Unlike queens and workers, which develop from fertilized diploid eggs, drones, or male bees, are born from unfertilized, haploid eggs. Drones leave the colony shortly after reaching adulthood to find a mate outside the nest. Mating is their sole role in the colony.

B. terrestris queen Bombus terrestris queen face HC1.jpg
B. terrestris queen

Life cycle

A solitary queen hatched from her abandoned colony initiates the colony cycle when she mates with a male and finds a nest. She will stay in this nest over winter and then will lay a small batch of diploid (female) eggs in the spring. Once these hatch, she tends the larvae, feeding them with nectar and pollen. When the larvae are grown, they pupate, and about two weeks later, the first workers emerge. This is known as the initiation phase of the colony. [10] Workers forage for nectar and pollen for the colony and tend later generations of larvae. The workers are smaller than the queen, and usually die while foraging in the jaws of predators like birds or robberflies. The foraging range and frequency of workers depends on the quality and distribution of available food, but most workers forage within a few hundred meters of their nest. [12]

This first phase can last a variable amount of time in B. terrestris, after which a switch point is reached, and the queen begins to lay some unfertilized eggs, which develop into males. [10] When the male drones emerge from the nest, they do not return, foraging only for themselves. They seek out emerging queens and mate with them. The remaining diploid eggs hatch into larvae that receive extra food and pupate to become new queens. The queen can use pheromones to discourage the workers' inclination to invest more in these larvae, thereby ensuring that not too many become queens. The resolution of this worker/queen conflict can be complex and is discussed below. The colony persists until fall in temperate zones and then workers begin to lay unfertilized eggs that if they mature will become males. At this point, outright aggression among workers and between the queen and workers begins. This is a predictable time point that occurs about 30 days into the colony cycle in very temperate climates. [10]

Usually, the worker-queen conflict will force the queen out and the new workers will become queenless. A "false queen" might take control of the colony for a short period. [13] The newly emerged queens sometimes act as workers and help to raise another brood of queens. During this time they daily leave the nest looking for food, during which time they may mate. Eventually they find a site to dig a "hibernaculum" where they will hibernate until the next spring, when they emerge, seek food — primarily to build up their ovaries — and soon seek a site to found a new nest. (In warmer climates they may skip the hibernation stage.) Almost always the old colony will have died out, and if the site is free of parasites one of the new queens will return and reuse that site.

Reproductive behavior

Mating system

B. terrestris is a singly mating species. Mating with multiple males might provide benefits of genetic variability among the brood, but it does not happen in this or any but the most highly derived social bees. [14] The lack of multiple matings by B. terrestris queens may be partly due to male interference. B. terrestris males plug the female's sexual tract with a sticky secretion during mating, which appears to reduce the female's ability to successfully mate with other males for several days. [15] However honeybee males also plug the female's reproductive tract to no avail; honeybees mate tens of times on one mating flight. While there may be genetic fitness benefits in colony heterogeneity from a polyandrous mating system, bumblebees are also likely to be monandrous due to social constraints, risks associated with multiple matings, and phylogenetic inertia since the ancestral bees are singly mated. Finding multiple mates might be energetically costly and expose the queen to higher predation risks. Additionally, while queens may prefer multiple matings to ensure more genetic variability and viable offspring, workers are more closely related to full sisters than to paternal half sisters. [14] This is due to haplodiploidy in Hymenopteran social insects in which males (drones) are haploid and females (workers and queens) are diploid. This confers greater genetic similarity between sister workers (relatedness of 0.75) than between mother and offspring (relatedness of 0.5), making the relatedness component of kin selection higher between sisters.

Worker egg laying

In addition to the queen, the workers can lay eggs. Since workers do not mate, all of their eggs are haploid and will develop into drones. There are multiple factors that determine whether a worker bee will become reproductively active. Workers born early in the first brood are more likely to become egg layers due to their increased size and age, which allows more time for ovarian development. Workers usually have to be at least 30 days old to become an egg layer. Individuals that spend less time foraging and more time near the queen are also more likely to become reproductive. Lastly, due to intense competition for the opportunity to reproduce, older workers often harass the queen by attacking her and buzzing loudly. Once this point is reached the colony is usually abandoned. [16]

Sex ratios

Due to the variability in the switch point to male production from worker production of B. terrestris colonies, there are varying levels of sex ratios among nests. Early-switching colonies have a much smaller number of future queens compared to males (1:17.4), which may give them a competitive advantage in mating with later emerging queens. Late-switching colonies have fewer males and a more even sex ratio of 1:1:3, thus indicating the queen's control over her colony (she prefers a 1:1 ratio, since she is equally related to both sons and daughters). On the other hand, workers prefer a 3:1 ratio, as they are more related to each other than to their mother. Although early and late switching colonies are usually balanced equally in numbers in the population, the overall demographic in one study was found to be male biased, resulting in an overall sex ratio of 1:4 (female to males). [10] However, most studies show that this balance of bimodal sex determination between early and late-switching colonies creates the queen's preferred 1:1 sex ratio in B. terrestris populations. [17] This is unusual for monogamous social insects, which usually have a 3:1 sex ratio indicative of worker colony control. B. terrestris often does not conform to standard predictions of sex ratios based on evolutionary theory and haplodiploid theory.

Reproductive suppression

Queen suppression

Queen bees can control oogenesis in worker bees by suppressing juvenile hormone (JH) in the workers, which regulates egg development. Among queenless B. terrestris workers, the corpora allata, which secrete JH, was noticeably enlarged compared to queenright workers. JH concentrations were also higher in the hemolymph of queenless workers. This suggests that the presence of a queen is enough to prevent workers from laying eggs, which helps her maintain genetic control over her colony's brood. The mechanism through which the queen induces this behavior is likely through pheromones. [18]

Worker suppression

While the queen controls much of the egg laying and larval development in the colony, it is likely that workers play a much bigger role in controlling egg laying than previously thought. Dominant workers will often inhibit younger workers from laying eggs. [16] [19] Workers have low levels of JH and ovarian development during the early stages of the colony cycle and also after the competition point. Workers introduced into queenright and queenless colonies experience similar levels of inhibition from fellow workers during the competition point, indicating the key role of worker policing of fellow nest mates later in the colony cycle. This suggests that worker reproductive development will be highest between early development and the competition point in the colony. [19]

Kin selection

Queen and worker on Cucurbita pepo flower Courgette bloem met gewone aardhommel (Cucurbita pepo and Bombus terristris).jpg
Queen and worker on Cucurbita pepo flower

Worker-queen conflict

Conflict is expected between the queen and workers over the sex ratio and reproduction of males in the colony, especially in monandrous colonies where workers are more related to their own sons and nephews than to their brothers. [19] In early-switching colonies, workers might start laying eggs when they know it will be in their own genetic interests, perhaps from a cue that indicates the switch point has been reached and the queen is now laying haploid eggs. In late-switching colonies (where the competition point still occurs at the same time in the cycle), workers may start laying eggs when they detect a change in the queen's pheromone that indicate larvae are developing into new queens. [17] Thus, the outcome of this conflict is mediated through the dominance of the queen and the information available to the workers. While it is assumed that queens usually win this conflict, it is still unclear because some studies have indicated that up to 80% of males are produced by workers. [16] These asymmetries in the timing of egg lying and dominance in B. terrestris might explain why it often does not conform to predicted sex ratios and kin-selection hypotheses, although worker bees are more closely related to their nephews (0.375) than to their brothers (0.25) and kinship selection would lead workers to favor their sons over nephews, and nephews over brothers.

Worker-worker conflict

Although B. terrestris workers are most directly in competition with the queen for egg laying opportunities, they will still inhibit their sisters from laying eggs in order to have their own sons. This is beneficial to them because they will share more genes with their own sons (.5) rather than their nephews (.375). [19] However, kin theory states that in monandrous colonies, workers will be most closely related to their sisters (0.75) but are more closely related to their sons (0.50) than to their nephews (0.375) and least of all to their brothers (0.25), and would accordingly devote their resources.

Social and foraging behavior

Newly emerged workers start out at the bottom of the dominance hierarchy in the social colony. As they age, they move closer to the position of queen. Queen-side workers are often egg layers and interact more frequently with the queen. This social position may pay off later, after the competition point is reached. When the queen is overthrown by the aggression of the workers, the most dominant worker will have the best likelihood of contributing more eggs to the colony brood and will perhaps climb to the position of "false queen." The queen appears to maintain a constant distance of social dominance from her workers at all points in the cycle, suggesting that she is displaced by the sheer number of workers later in the cycle. [13]

Foraging behavior

B. terrestris generally forage on a large variety of flower species. Their highest activity is in the morning, with their peak time being noted at around 7-8 am. This is likely because it gets progressively warmer in the afternoon, and foragers prefer ambient temperatures of around 25 °C during nectar and pollen collection. [20]

Alloethism

B. terrestris bees exhibit alloethism, which is where different sized bees perform different tasks. This kind of behavior can be seen most often in foraging activities. Larger bees are more often found foraging outside the nest and will return to the nest with larger amounts of nectar and pollen. It is possible that larger bees might be able to withstand greater temperature variation, avoid predation, and travel larger distances making them selectively advantageous. Distinct social roles based on morphology might also be beneficial for individuals of the colonies, by making the colony operate more efficiently. Small bees can be reared more cheaply and kept for in-nest tasks, while only some larvae will be fed enough to become large foraging bees. [4]

B. terrestris foraging Bombus terrestris01.jpg
B. terrestris foraging

Food alert

Individuals who return from the nest after a foraging run often recruit other bees in the colony to leave the nest and search for food. In B. terrestris, successful foragers will return to the nest and run around frantically and without a measurable pattern, unlike the ritualized dance of the honeybee. Although the mechanism by which this recruitment strategy functions is unclear, it is hypothesized that running around likely spreads a pheromone that encourages other bees to exit and forage by indicating the location and odor of food nearby. [9] Colonies with lower food stores will often be more responsive to this foraging pheromone. Conversely, in colonies with ample food reserves bees will be less responsive to these pheromones likely to save time and energy from unnecessary foraging. [21]

Homing ability

B. terrestris has an impressive homing range, where bees displaced from their nests can relocate the colony from up to 9.8 km away. However, the return often takes several days, indicating B. terrestris might be utilizing familiar foliage and natural landmarks to find the nest. This may be a tedious process if an individual is outside the conventional foraging range of the nest. [22] Another study indicated that these bees can navigate their way back to the nest from a distance as far away as 13 km (8.1 mi), although most forage within 5 km of their nest. [23] One mark and recapture study found their average foraging distance to be approximately 663 m. [24] Male bees have also been found to have longer flight ranges than worker bees, likely because they move farther away from the nest to find mates. Males have flight distances of anywhere from 2.6 to 9.9 km. If males also contribute to pollination, this might increase previously predicted pollen flow ranges based on worker flight behavior. [25]

Learning

Bumblebees and honey bees are extremely influenced by an innate preference for blue and yellow color. When they have no training, they will often just visit flowers that naturally attract them. However, it is generally thought that bees will learn to visit more nectar rewarding flowers after experience associates the reward with the color of the petals. This has been demonstrated in B. terrestris, where bees trained on artificially colored flowers will pick a similar color to the one they were trained with when tested with an array of flower choices. If individuals were tested with flower colors significantly different than from what they were trained with, they just visited flowers most closely aligned with their innate color preferences. [26] In addition to identifying specific colors for foraging purposes, it has also been shown that young worker bees have to learn complex motor skills in order to efficiently collect nectar and pollen from flowers. These skills might take several days to develop, as memory does not always hold perfectly on a day-to-day basis, sometimes deteriorating overnight. [27] Even within a species, different populations have varying levels of innate blue preference and exhibit intraspecific variation in learning rate during association tasks. This is true of two subspecies of B. terrestris, B. terrestris dalmatinus and B. terrestris audax. [28]

A study suggests that bumblebees can do motivational trade-offs. [29]

Bombus terrestris 00001.png

Limitations on foraging precision

While bees are highly adept at discrimination tasks, they are still limited by the magnitude of difference needed in hue to properly carry out these tests. Error rates of color recognition decrease in B. terrestris when flower pigments are closer together on the color spectrum. This might have damaging effects on pollination efficiency if bees visit different flower species with similar, but distinct colors, which can only be mediated if the flowers have unique shapes. [30]

Social learning

While bees often forage alone, experiments demonstrate that young foragers might learn what flowers provide the most nectar more quickly when foraging with older workers. B. terrestris individuals have a faster learning curve for visiting unfamiliar, yet rewarding flowers, when they can see a conspecific foraging on the same species. [31] The discovery of this type of associative learning is a novel insight into bee behavior and may supplement learning via color reward association.

Parasites and disease

Brood parasites

B. terrestris is parasitized by B. bohemicus , a brood-parasitic Cuckoo bee that invades B. terrestris hives and takes over reproductive dominance from the host queen, laying its own eggs that will be cared for by host workers. [32] Another brood parasite is the bee B. vestalis . Both of these are distributed in various regions of Europe. The difference between B. bohemicus and B. vestalis is that the former parasitizes several bumble bee species while B. vestalis exclusively parasitizes B. terrestris. [33]

Microsporidian parasites

A common microsporidian parasite that infects the gut of various bumblebee species, including B. terrestris, is Nosema bombi . It can cause a creeping disease and is detrimental to the fitness of its bumblebee host. [34] A study by Manlik et al. (2017) showed that N. bombi infection prevalence varies widely over time, and is associated with mitochondrial DNA genotypes in B. terrestris. [35]

Effects of foraging on resistance

Foraging is considered energetically costly and it is possible that individuals that spend more time foraging suffer costs to their overall fitness. For example, B. terrestris is often vulnerable to parasitism by conopid flies in Central Europe, and it has been hypothesized that foragers might suffer higher incidences of parasites due to the increased metabolic costs of flying. This was demonstrated in a population in which foraging workers had significantly lower levels of encapsulation of an experimental parasitic egg when compared to non-foraging workers. This suggests that foragers have compromised immune systems due to increased energetic expenses and might be predisposed to fly parasites. [36]

Effects of polyandry on resistance

While B. terrestris is a singly mating species, a polyandrous system would potentially be beneficial because it would be possible to attain greater genetic variability for resistance against disease. Accordingly, artificially increasing the number of mates a B. terrestris queen obtains through artificial insemination has shown that the increased genetic variability in her offspring confers greater resistance to the most common bumblebee parasite, Crithidia bombi. [14] However, the average reproductive success between one and multiple matings is not linear. Queens that mated once and mated four times had a higher fitness than those that mated twice. [14] This suggests that there might be a fitness barrier to increased matings, which might be why colonies are usually monandrous.

Immunocompetence

Surprisingly, the immunocompetence, as measured by the ability to encapsulate a novel antigen, does not vary based on the local environment. Experimental studies demonstrate that B. terrestris have equal levels of encapsulation in poor and stable environments. [37] This is unexpected, because immunity should be compromised in conditions where food supply is low in order to save energy. Perhaps encapsulation represents an invariable trait of bumblebees, or immunity is far too complex to characterize solely based on measurements of encapsulation.

Threats from disease

Deformed wing virus (DWV) is normally a honey bee pathogen that results in reduced and crumpled wings, making those individuals inviable. This virus is thought to have spread to B. terrestris, and in 2004, as many as 10% of queen bees bred commercially in Europe were found dead with deformed wings. This was confirmed as DWV when B. terrestris colonies tested positive for the presence of DWV RNA. This could indicate that DWV is a broad range pathogen among bees, or perhaps it has recently been infecting new hosts after transmission from honey bees. [38]

Interactions with other species

Female Bee Moths ( Aphomia sociella ) prefer to lay their eggs in the nests of bumblebees. The A. sociella larvae will then hatch and feed on the eggs, larvae, and pupae left unprotected by the bees, sometimes destroying large parts of the nest as they tunnel throughout looking for food. [39]

Environmental concerns

Invasive species

While native to Europe, B. terrestris has been introduced as a greenhouse pollinator into many foreign ecosystems. The presence of B. terrestris is becoming an ecological concern in many communities in which it is not native. It is classified as an "invasive alien species" in Japan. [40] For example, B. terrestris has a large niche overlap with local Japanese bee species in terms of flower resources and nest sites. B. terrestris queens competing for local underground nest sites are displacing B. hypocrita sapporoensis. However, B. pseudobaicalensis, which visits similar flowers but only forms nests above ground, has not seen a rapid decline in population numbers. [7]

In 2008, the Australian government banned the live import of B. terrestris into Australia on the grounds that it would present a significant risk of becoming a feral species and thereby present a threat to native fauna and flora. [41] In 2004, this bumblebee was classified as a 'Key Threatening Process' by the Scientific Committee of the New South Wales Department of Environment. [42]

This species was introduced to Chile in 1998. It has since crossed into Argentina, and is spreading at about 275 km per year. Its spread has been detrimental to populations of Bombus dahlbomii , which is the only bumblebee species native to southern South America (Patagonia, Southern Chile and Argentina). [43] Bombus terrestris populations facilitated such massive and immediate population decline of Bombus dahlbomii through competition and pathogen introduction/spillover. [43] [44] Bombus ruderatus , a bee previously introduced in 1982, is also seriously affected. The cause is thought to be the parasite Apicystis bombi , an organism carried by the buff-tails, but which has no adverse effect on that species. [45]

Colony development in changing environments

In temperate areas, variable climates and environmental conditions occur during changing seasons. Lack of available food due to these unpredictable circumstances can often negatively affect colony growth, reproduction, and resistance to parasites. In poor environments with limited food, the few workers born are smaller than average. However, it appears that B. terrestris is well adapted to a changing environment, considering colony growth is higher under variable feeding conditions than under stable feeding conditions. Workers and reproductives are also heavier with a variable food supply when compared to stable food availability. This might indicate an adaptive strategy of increased provisioning to save for days it is hard to find food. [37]

Pesticide exposure

In their 2014 study published in Functional Ecology researchers using Radio-Frequency Identification (RFID) tagging technology on the bees, found that a sublethal exposure to either a neonicotinoid (imidacloprid) and/or a pyrethroid (?-cyhalothrin) over a four-week period caused an impairment of the bumblebee's ability to forage. [46] Research published in 2015 showed that bees prefer solutions containing neonicotinoids, even though the consumption of these pesticides caused them to eat less food overall. This work implies that treating flowering crops with such pesticides presents a sizeable hazard to foraging bees. [47]

Human importance

Commercial use

Since 1987, B. terrestris has been bred commercially for use as a pollinator in European greenhouse crops, particularly tomatoes—a task which was previously carried out by human hand. [40] [48] B. terrestris has been commercially reared in New Zealand since the early 1990s, [49] [50] and is now used in at least North Africa, Japan, Korea, and Russia, with the global trade in bumblebee colonies probably exceeding 1 million nests per year. [51] In Korea, however, some have chosen Bombus ignitus over the already established commercial pollinator, Bombus terrestris, for fear of competition or genetic contamination by mating with native bumblebee species. [52] Also, there has been a ban on importing B. terrestris into North America which resulted in higher interest in other species like B. impatiens in North America. [53]

Nonetheless, B. terrestris are key commercial pollinators in Europe, which has driven researchers to investigate the influence of agricultural land on the foraging and survival of this species. Monoculture reduces biodiversity in farmland areas, and likely decreases the number of flowering species bees can forage on. B. terrestris consequently exhibits greater nest growth in suburban areas than in farmland, because local suburban gardens promote more plant diversity for bees to feed from. Agriculture has a profound impact on many bumblebees, and is causing widespread decline in several species. However, B. terrestris is still widespread, likely because it can forage at very long distances, making it less sensitive to changes in biodiversity and the environment. [54]

Related Research Articles

<span class="mw-page-title-main">Bumblebee</span> Genus of insect

A bumblebee is any of over 250 species in the genus Bombus, part of Apidae, one of the bee families. This genus is the only extant group in the tribe Bombini, though a few extinct related genera are known from fossils. They are found primarily in higher altitudes or latitudes in the Northern Hemisphere, although they are also found in South America, where a few lowland tropical species have been identified. European bumblebees have also been introduced to New Zealand and Tasmania. Female bumblebees can sting repeatedly, but generally ignore humans and other animals.

<i>Bombus ternarius</i> Species of insect

Bombus ternarius, commonly known as the orange-belted bumblebee or tricolored bumblebee, is a yellow, orange and black bumblebee. It is a ground-nesting social insect whose colony cycle lasts only one season, common throughout the northeastern United States and much of Canada. The orange-belted bumblebee forages on Rubus, goldenrods, Vaccinium, and milkweeds found throughout the colony's range. Like many other members of the genus, Bombus ternarius exhibits complex social structure with a reproductive queen caste and a multitude of sister workers with labor such as foraging, nursing, and nest maintenance divided among the subordinates.

<span class="mw-page-title-main">Early bumblebee</span> Species of bee

The early bumblebee or early-nesting bumblebee is a small bumblebee with a wide distribution in most of Europe and parts of Asia. It is very commonly found in the UK and emerges to begin its colony cycle as soon as February which is earlier than most other species, hence its common name. There is even some evidence that the early bumblebee may be able to go through two colony cycles in a year. Like other bumblebees, Bombus pratorum lives in colonies with queen and worker castes. Bombus pratorum queens use aggressive behavior rather than pheromones to maintain dominance over the workers.

<i>Bombus hypnorum</i> Species of bee

The tree bumblebee or new garden bumblebee is a species of bumblebee common in the European continent and parts of Asia. Since the start of the twenty-first century, it has spread to Great Britain. These bumblebees prefer habitats that others do not, allowing them to pollinate flowers in areas that many other species do not get to.

<i>Bombus lapidarius</i> Species of bee

Bombus lapidarius is a species of bumblebee in the subgenus Melanobombus. Commonly known as the red-tailed bumblebee, B. lapidarius can be found throughout much of Central Europe. Known for its distinctive black and red body, this social bee is important in pollination.

<i>Bombus vestalis</i> Species of bee

Bombus vestalis, the vestal cuckoo bumblebee, is a species of cuckoo bumblebee that lives in most of Europe, as well as North Africa and western Asia. It is a brood parasite that takes over the nests of other bee species. Its primary host is Bombus terrestris. After its initial classification as Psithyrus vestalis, this bumblebee recently was reclassified into the genus Bombus, subgenus Psithyrus.

<i>Bombus bohemicus</i> Species of bee

Bombus bohemicus, also known as the gypsy's cuckoo bumblebee, is a species of socially parasitic cuckoo bumblebee found in most of Europe with the exception of the southern Iberian Peninsula and Iceland. B. bohemicus practices inquilinism, or brood parasitism, of other bumblebee species. B. bohemicus is a generalist parasite, successfully invading several species from genus Bombus. The invading queen mimics the host nest's chemical signals, allowing her to assume a reproductively dominant role as well as manipulation of host worker fertility and behavior.

<i>Bombus hortorum</i> Species of bee

Bombus hortorum, the garden bumblebee or small garden bumblebee, is a species of bumblebee found in most of Europe north to 70°N, as well as parts of Asia and New Zealand. It is distinguished from most other bumblebees by its long tongue used for feeding on pollen in deep-flowered plants. Accordingly, this bumblebee mainly visits flowers with deep corollae, such as deadnettles, ground ivy, vetches, clovers, comfrey, foxglove, and thistles. They have a good visual memory, which aids them in navigating the territory close to their habitat and seeking out food sources.

<i>Bombus lucorum</i> Species of bee

Bombus lucorum, the white-tailed bumblebee, is a species of bumblebee, widespread and common throughout Europe. This name has been widely used for a range of nearly identical-looking or cryptic species of bumblebees. In 1983, Scholl and Obrecht even coined the term Bombus lucorum complex to explain the three taxa that cannot be easily differentiated from one another by their appearances. A recent review of all of these species worldwide has helped to clarify its distribution in Europe and northern Asia, almost to the Pacific. B. lucorum reaches the Barents Sea in the North. However, in southern Europe, although found in Greece it is an upland species with its distribution never quite reaching the Mediterranean.

Two-spotted bumble bee Species of bee

The two-spotted bumble bee is a species of social bumble bee found in the eastern half of the United States and the adjacent south-eastern part of Canada. In older literature this bee is often referred to as Bremus bimaculatus, Bremus being a synonym for Bombus. The bee's common name comes from the two yellow spots on its abdomen. Unlike many of the other species of bee in the genus Bombus,B. bimaculatus is not on the decline, but instead is very stable. They are abundant pollinators that forage at a variety of plants.

<i>Bombus vosnesenskii</i> Species of bee

Bombus vosnesenskii, the yellow-faced bumblebee, is a species of bumblebee native to the west coast of North America, where it is distributed from British Columbia to Baja California. It is the most abundant species of bee in this range, and can be found in both urban and agricultural areas. Additionally, B. vosnesenskii is utilized as an important pollinator in commercial agriculture, especially for greenhouse tomatoes. Though the species is not currently experiencing population decline, urbanization has affected its nesting densities, and early emergence of the B. vosnesenskii has been implicated in the increasing lack of bee diversity on the West coast.

<i>Bombus fervidus</i> Species of bee

Bombus fervidus, the golden northern bumble bee or yellow bumblebee, is a species of bumblebee native to North America. It has a yellow-colored abdomen and thorax. Its range includes the North American continent, excluding much of the southern United States, Alaska, and the northern parts of Canada. It is common in cities and farmland, with populations concentrated in the Northeastern part of the United States. It is similar in color and range to its sibling species, Bombus californicus, though sometimes also confused with the American bumblebee or black and gold bumblebee. It has complex behavioral traits, which includes a coordinated nest defense to ward off predators. B. fervidus is an important pollinator, so recent population decline is a particular concern.

<i>Bombus impatiens</i> Species of insect

Bombus impatiens, the common eastern bumblebee, is the most commonly encountered bumblebee across much of eastern North America. They can be found in the Eastern temperate forest region of the eastern United States, southern Canada, and the eastern Great Plains. Because of their great adaptability, they can live in country, suburbs, and even urban cities. This adaptability makes them a great pollinator species, leading to an increase in their commercial use by the greenhouse industry. This increase consequently led to their farther spread outside their previous distribution range. They are considered one of the most important species of pollinator bees in North America.

<i>Bombus ruderatus</i> Species of bee

Bombus ruderatus, the large garden bumblebee or ruderal bumblebee, is a species of long-tongued bumblebee found in Europe and in some parts of northern Africa. This species is the largest bumblebee in Britain and it uses its long face and tongue to pollinate hard-to-reach tubed flowers. Bumblebees are key pollinators in many agricultural ecosystems, which has led to B. ruderatus and other bumblebees being commercially bred and introduced into non-native countries, specifically New Zealand and Chile. Since its introduction in Chile, B. ruderatus has spread into Argentina as well. Population numbers have been declining and it has been placed on the Biodiversity Action Plan to help counteract these declines.

<i>Bombus muscorum</i> Species of bee

Bombus muscorum, commonly known as the large carder bee or moss carder bee, is a species of bumblebee in the family Apidae. The species is found throughout Eurasia in fragmented populations, but is most commonly found in the British Isles. B. muscorum is a eusocial insect. The queen is monandrous, mating with only one male after leaving a mature nest to found its own. Males mate territorially and the species is susceptible to inbreeding and bottlenecks. The species builds its nests on or just under the ground in open grassland and forages very close to the nest. In recent years, populations have significantly declined due to loss of natural habitat. B. muscorum is currently listed as vulnerable in Europe by the European Red List of Bees.

<i>Bombus affinis</i> Species of bee

Bombus affinis, commonly known as the rusty patched bumble bee, is a species of bumblebee endemic to North America. Its historical range in North America has been throughout the east and upper Midwest of the United States, north to Ontario, Canada, where it is considered a "species at risk", east to Quebec, south to Georgia, and west to the Dakotas. Its numbers have declined in 87% of its historical habitat range. On January 10, 2017, the United States Fish and Wildlife Service placed B. affinis on the list of endangered species, making the rusty patched bumblebee the first bee to be added to the list in the continental United States.

<i>Bombus terricola</i> Species of bee

Bombus terricola, the yellow-banded bumblebee, is a species of bee in the genus Bombus. It is native to southern Canada and the east and midwest of the United States. It possesses complex behavioral traits, such as the ability to adapt to a queenless nest, choose which flower to visit, and regulate its temperature to fly during cold weather. It was at one time a common species, but has declined in numbers since the late 1990s, likely due to urban development and parasite infection. It is a good pollinator of wild flowers and crops such as alfalfa, potatoes, raspberries, and cranberries.

Apicystis bombi is a species of parasitic alveolates in the phylum Apicomplexa. It infects bees, especially bumblebees. It is believed to have a cosmopolitan distribution in bumblebees and a sporadic occurrence in honey bees, and causes disease symptoms in nonresistant bee species.

<i>Bombus ignitus</i> Species of bee

Bombus ignitus is a species of bumblebee in the family Apidae. It is mainly distributed in Eastern Asia, commonly found in China, Japan and Korea. It is used in China and Japan commercially as a pollinator. B. ignitus is a eusocial insect with a queen that is monandrous: mating with only one male in the late summer before hibernating until the following spring. It builds its nest out of a mass of pollen and lays its eggs after completion. Due to numerous conflicts between queens and fertile workers, some surviving queens are badly injured, described by some as living corpses.

Bombus hypocrita, also known as the short-tongued bumblebee, is a Japanese bumblebee commonly used in commercial pollination. These short-tongued bumblebees have a proboscis about 7-9mm long, which is folded under their head when flying. Bumblebees are a small fuzzy insect with yellow and black banding along their abdomen. They are round and covered in pile, the hair-like structures that give them their distinct fuzzy appearance.

References

  1. ↑ Williams, Paul H.; Brown, Mark J.F.; Carolan, James C.; An, Jiandong; Goulson, Dave; Aytekin, A. Murat; Best, Lincoln R.; Byvaltsev, Alexandr M.; Cederberg, Björn; Dawson, Robert; Huang, Jiaxing; Ito, Masao; Monfared, Alireza; Raina, Rifat H.; Schmid-Hempel, Paul; Sheffield, Cory S.; Šima, Peter; Xie, Zenghua (March 2012). "Unveiling cryptic species of the bumblebee subgenus worldwide with COI barcodes (Hymenoptera: Apidae)". Systematics and Biodiversity. 10 (1): 21–56. doi: 10.1080/14772000.2012.664574 . hdl: 1893/7328 .
  2. 1 2 Semmens, T.D.; E. Turner & R. Buttermore. (1993). "Bombus terrestris (L.) (Hymenoptera: Apidae) now established in Tasmania". Australian Journal of Entomology. 32 (4): 346. doi: 10.1111/j.1440-6055.1993.tb00598.x .
  3. ↑ Rasmont, Pierre; Coppee, Audrey; Michez, Denis; De Meulemeester, Thibaut (1 January 2008). "An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae)". Annales de la Société Entomologique de France . New Series. 44 (2): 243–250. doi: 10.1080/00379271.2008.10697559 .
  4. 1 2 3 Goulson, Dave; Peat, James; Stout, Jane C.; Tucker, James; Darvill, Ben; Derwent, Lara C.; Hughes, William O.H. (July 2002). "Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?". Animal Behaviour. 64 (1): 123–130. doi:10.1006/anbe.2002.3041. S2CID   3964066.
  5. ↑ Bumblebee species , retrieved 4 October 2014
  6. ↑ Widmer, A.; P. Schmid-Hempel; A. Estoup; A. Scholl (1998). "Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira". Heredity. 81 (5): 563–572. doi:10.1046/j.1365-2540.1998.00407.x. S2CID   19518818.
  7. 1 2 3 Inoue, M.K.; J. Yokoyama & I. Washitani (2008). "Displacement of Japanese native bumblebees by the recently introduced Bombus terrestris (L.) (Hymenoptera: Apidae)". Journal of Insect Conservation. 12 (2): 135–146. doi:10.1007/s10841-007-9071-z. S2CID   33992235.
  8. ↑ Torretta, J.A.; D. Medan & A. H. Abrahamovich (2006). "First record of the invasive bumblebee Bombus terrestris (L.) (Hymenoptera, Apidae) in Argentina". Transactions of the American Entomological Society. 132 (3 & 4): 285–289. doi:10.3157/0002-8320(2006)132[285:frotib]2.0.co;2. S2CID   86087652.
  9. 1 2 Dornhaus, A. & L. Chittka (2001). "Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications". Behavioral Ecology and Sociobiology. 50 (6): 570–576. doi:10.1007/s002650100395. S2CID   46168842.
  10. 1 2 3 4 5 Duchateau, M. J. & H. H. W. Velthuis (1988). "Development and reproductive strategies in Bombus terrestris colonies". Behaviour . 107 (3): 186–207. doi:10.1163/156853988x00340.
  11. ↑ CNAANI, JONATHAN; BORST, DAVID W; HUANG, Z. -Y; ROBINSON, GENE E; HEFETZ, ABRAHAM (1997-04-01). "Caste Determination in Bombus terrestris: Differences in Development and Rates of JH Biosynthesis between Queen and Worker Larvae". Journal of Insect Physiology. 43 (4): 373–381. doi:10.1016/S0022-1910(96)00106-0. PMID   12769899.
  12. ↑ Stephan Wolf & Robin F. A. Moritz (2008). "Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae)". Apidologie . 39 (4): 419–427. doi:10.1051/apido:2008020. S2CID   31080168.
  13. 1 2 van Honk C. & P. Hogeweg (1981). "The ontogeny of the social structure in a captive Bombus terrestris colony". Behavioral Ecology and Sociobiology. 9 (2): 111–119. doi:10.1007/bf00293582. S2CID   39669241.
  14. 1 2 3 4 Baer, B. & P. Schmid-Hempel (2001). "Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris". Evolution. 55 (8): 1639–1643. doi:10.1554/0014-3820(2001)055[1639:ucopfp]2.0.co;2. PMID   11580023.
  15. ↑ Annette Sauter; Mark J. F. Brown; Boris Baer; Paul Schmid-Hempel (2001). "Males of social insects can prevent queens from multiple mating". Proceedings of the Royal Society B . 268 (1475): 1449–1454. doi:10.1098/rspb.2001.1680. PMC   1088762 . PMID   11454287.
  16. 1 2 3 van Honk, C.G.J.; P.F. Roseler; H.H.W. Velthuis; J.C. Hoogeveen (1981). "Factors influencing the egg laying of workers in a captive Bombus terrestris colony". Behavioral Ecology and Sociobiology. 9: 9–14. doi:10.1007/bf00299847. S2CID   40935091.
  17. 1 2 Bourke, A.F.G. & F.L.W. Ratnieks (2001). "Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae)". Proceedings of the Royal Society of London B. 268 (1465): 347–355. doi:10.1098/rspb.2000.1381. PMC   1088613 . PMID   11270430.
  18. ↑ Roseler, P. F. (1977). "Juvenile hormone control of oogenesis in bumblebee workers, B. terrestris". Journal of Insect Physiology. 23 (8): 985–992. doi: 10.1016/0022-1910(77)90126-3 .
  19. 1 2 3 4 Bloch, G. & A. Hefetz (1999). "Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queen right colonies". Behavioral Ecology and Sociobiology. 45 (2): 125–135. doi:10.1007/s002650050546. S2CID   21888119.
  20. ↑ Kwon, Yong Jung; Saeed, Shafqat (2003-01-01). "Effect of temperature on the foraging activity of Bombus terrestris L. (Hymenoptera: Apidae) on greenhouse hot pepper (Capsicum annuum L.)". Applied Entomology and Zoology. 38 (3): 275–280. doi: 10.1303/aez.2003.275 .
  21. ↑ Molet, Mathieu; Chittka, Lars; Stelzer, Ralph J.; Streit, Sebastian; Raine, Nigel E. (October 2008). "Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris". Behavioral Ecology and Sociobiology. 62 (12): 1919–1926. doi:10.1007/s00265-008-0623-3. S2CID   24258041.
  22. ↑ Goulson, D. & J. Stout (2001). "Homing ability of the bumblebee Bombus terrestris (Hymenoptera: Apidae)" (PDF). Apidologie. 32: 105–111. doi: 10.1051/apido:2001115 .
  23. ↑ Louisa Cheung (July 26, 2006). "Homing instinct of bees surprises". BBC News.
  24. ↑ Walther-Hellwig, K. & R. Frankl (2000). "Foraging distances of Bombus muscorum, Bombus lapidarius, and Bombus terrestris (Hymenoptera, Apidae)". Journal of Insect Behavior. 13 (2): 239–46. doi:10.1023/a:1007740315207. S2CID   29303814.
  25. ↑ Kraus, F.B.; S. Wolf; R.F.A. Moritz (2009). "Male flight distance and population substructure in the bumblebee Bombus terrestris". Journal of Animal Ecology. 78 (1): 247–252. doi: 10.1111/j.1365-2656.2008.01479.x . PMID   19120605.
  26. ↑ Gumbert, A (2000). "Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning". Behavioral Ecology and Sociobiology. 48 (1): 36–43. doi:10.1007/s002650000213. S2CID   13664530.
  27. ↑ Raine, N.E. & L. Chittka (2007). "Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris)". Naturwissenschaften. 94 (6): 459–464. Bibcode:2007NW.....94..459R. doi:10.1007/s00114-006-0184-0. PMID   17149583. S2CID   22912889.
  28. ↑ Ings, Thomas C.; Raine, Nigel E.; Chittka, Lars (2009-06-01). "A Population Comparison of the Strength and Persistence of Innate Colour Preference and Learning Speed in the Bumblebee Bombus terrestris". Behavioral Ecology and Sociobiology. 63 (8): 1207–1218. doi:10.1007/s00265-009-0731-8. JSTOR   40295468. S2CID   31332225.
  29. ↑ Morell, Virginia (2022-07-26). "Bees may feel pain". www.science.org. Retrieved 2022-09-07.
  30. ↑ Dyer, A.G. & L. Chittka (2004). "Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study". Journal of Comparative Physiology A. 190 (2): 105–114. doi:10.1007/s00359-003-0475-2. PMID   14652688. S2CID   22066483.
  31. ↑ Leadbeater, E. & L. Chittka (2007). "The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris)". Behavioral Ecology and Sociobiology. 61 (11): 1789–1796. doi:10.1007/s00265-007-0412-4. S2CID   569654.
  32. ↑ Kreuter, Kirsten; Bunk, Elfi; Lückemeyer, Anna; Twele, Robert; Francke, Wittko; Ayasse, Manfred (March 2012). "How the social parasitic bumblebee Bombus bohemicus sneaks into power of reproduction". Behavioral Ecology and Sociobiology. 66 (3): 475–486. doi:10.1007/s00265-011-1294-z. S2CID   7124725.
  33. ↑ Kreuter, Kirsten; Twele, Robert; Francke, Wittko; Ayasse, Manfred (August 2010). "Specialist Bombus vestalis and generalist Bombus bohemicus use different odour cues to find their host Bombus terrestris". Animal Behaviour. 80 (2): 297–302. doi:10.1016/j.anbehav.2010.05.010. S2CID   140212119.
  34. ↑ Paul Schmid-Hempel (1998). "Parasites in Social Insects" Princeton University Press.
  35. ↑ Oliver Manlik; Regula Schmid-Hempel & Paul Schmid-Hempel (2017). "Parasite infection of specific host genotypes relates to changes in prevalence in two natural populations of bumblebees". Infection, Genetics and Evolution . 56: 125–132. doi:10.1016/j.meegid.2017.11.019. PMID   29155285.
  36. ↑ König, Cornelia; Schmid-Hempel, Paul (22 May 1995). "Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L". Proceedings of the Royal Society of London. Series B: Biological Sciences. 260 (1358): 225–227. Bibcode:1995RSPSB.260..225K. doi:10.1098/rspb.1995.0084. S2CID   73560782.
  37. 1 2 Schmid-Hempel, R. & P. Schmid-Hempel (1998). "Colony performance and immunocompetence of a social insect, B. terrestris, in poor and variable environments". Functional Ecology. 22: 22–30. doi: 10.1046/j.1365-2435.1998.00153.x .
  38. ↑ Genersch, E.; C. Yue; I. Fries; J. R. de Miranda (2006). "Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities". Journal of Insect Pathology. 91 (1): 61–63. doi:10.1016/j.jip.2005.10.002. PMID   16300785.
  39. ↑ Gambino, Parker (1995). "Dolichovespula (Hymenoptera: Vespidae), Hosts of Aphomia sociella (L.) (Lepidoptera: Pyralidae)". Journal of the New York Entomological Society. 103 (2): 165–169. JSTOR   25010152.
  40. 1 2 Matsumura, Chizuru; Yokoyama, Jun; Washitani, Izumi (2004). "Invasion status and potential ecological impacts of an invasive alien bumblebee, Bombus terrestris L.(Hymenoptera: Apidae) naturalized in Southern Hokkaido, Japan" (PDF). Global Environmental Research. 8 (1): 51–66. NAID   10015248943.
  41. ↑ "Bumblebee rejected for live import". Australian Government. 26 October 2008. Retrieved 1 January 2009.
  42. ↑ Paul Adam (February 2004). "Introduction of the large earth bumblebee, Bombus terrestris - key threatening process listing". NSW Government. Retrieved 1 January 2009.
  43. 1 2 Polidori, C; Nieves-Aldrey, JL (2014). "Comparative flight morphology in queens of invasive and native Patagonian bumblebees (Hymenoptera: Bombus)". Comptes Rendus Biologies. 338 (2): 126–33. doi:10.1016/j.crvi.2014.11.001. hdl: 10261/118107 . PMID   25499798. S2CID   21990979.
  44. ↑ Arbetman, Marina; Meeus, Ivan; Morales, Carolina (2006). "Alien parasite hitchhikes to Patagonia on invasive bumblebee" (PDF). Biological Invasions. 8 (1): 489–494. doi:10.1007/s10530-012-0311-0. S2CID   18481707. Archived from the original (PDF) on 2017-01-09. Retrieved 2015-11-05.
  45. ↑ Goulson, Dave (2013). "Argentinian invasion!". Buzzword. 21: 17–18.
  46. ↑ Gill, Richard J.; Raine, Nigel E. (7 July 2014). "Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure". Functional Ecology. 28 (6): 1459–1471. doi: 10.1111/1365-2435.12292 .
  47. ↑ Kessler, Sébastien C.; Tiedeken, Erin Jo; Simcock, Kerry L.; Derveau, Sophie; Mitchell, Jessica; Softley, Samantha; Radcliffe, Amy; Stout, Jane C.; Wright, Geraldine A. (7 May 2015). "Bees prefer foods containing neonicotinoid pesticides". Nature. 521 (7550): 74–76. Bibcode:2015Natur.521...74K. doi:10.1038/nature14414. PMC   4772122 . PMID   25901684.
  48. ↑ Anon. "Pollination". Koppert. Koppert B.V. Retrieved 18 September 2011.
  49. ↑ Velthuis, H. H. W.; van Doorn, A. (2004). "The breeding, commercialization and economic value of bumblebees". In Freitas, Breno M.; Pereira, Júlio Otávio P. (eds.). Solitary Bees: Conservation, Rearing and Management for Pollination. Imprensa Universitária. pp. 135–149. ISBN   978-85-7485-049-8.
  50. ↑ "Biobees - Bumblebee Biology". Archived from the original on 2012-02-11.
  51. ↑ Dave Goulson (2010). "Bumblebees. Behaviour, Ecology and Conservation" Oxford University Press.
  52. ↑ Yoon, Hyung Joo; Kim, Sam Eun; Kim, Young Soo (2002). "Temperature and humidity favorable for colony development of the indoor-reared bumblebee, Bombus ignitus". Applied Entomology and Zoology. 37 (3): 419–423. doi: 10.1303/aez.2002.419 .
  53. ↑ Goulson, Dave (2010). Bumblebees: Behaviour, Ecology, and Conservation. OUP Oxford. ISBN   978-0-19-955306-8.[ page needed ]
  54. ↑ Goulson, D.; Hughes, W.; Derwent, L.; Stout, J. (January 2002). "Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats". Oecologia. 130 (2): 267–273. Bibcode:2002Oecol.130..267G. doi:10.1007/s004420100803. PMID   28547150. S2CID   655322.

Further reading

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.