Bombus affinis

Rusty-patched bumblebee
Photo of Bombus affinis queen, lacking the rust colouring of the worker and male.
Conservation status
Critically Endangered  (IUCN 3.1)[1]
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Hymenoptera
Family:	Apidae
Genus:	Bombus
Subgenus:	Bombus
Species:	B. affinis
Binomial name
Bombus affinis Cresson, 1863[2]
The past range of Bombus affinis.

Bombus affinis, commonly known as the rusty patched bumblebee, is a species of bumblebee that is endemic to North America.^[3] Its historical range in North America has been throughout the east and upper Midwest of the United States,^[4] north to in Ontario, Canada,where it is considered a "species at risk",^[5] east to Quebec, south to Georgia, and west to the Dakotas.^[5] Its numbers have declined in 87% of its historical habitat range.^[4] In September 2016, the U.S. Fish and Wildlife Service proposed listing B. affinis for federal protection as an endangered species.^[6]

Members of B. affinis are relatively large in size, and like other species of bumblebees, are known to be eusocial organisms.^[3] Most nests that are constructed by the B. affinis are built underground, and are commonly found in old rodent burrows.^[3] Nests that are created in captivity can house up to 2,100 members, however, they are typically much smaller in the wild.^[3] This species consumes nectar and pollen from a variety of plants, including Abelia grandiflora, Asclepias syriaca, and Linaria.^[3] The colony odor is very similar to that of Bombus terricola, which makes it difficult for predators and parasites to differentiate between the two different species.^[7]

Taxonomy and phylogeny

Bombus affinis is a member of the subfamily Apinae,^[3] and is most closely related phylogenetically to B. franklini, which is another species of bumble bee that is endemic to North America.^[8] The next most closely related species, however, is B. terricola, which is very similar to B. affinis in terms of bodily pheromones.^[7] This similarity allows members of B. affinis to successfully dominate B. terricola workers after usurping their nests.^[7] B. affinis is in the company of nearly 250 other species of bumblebee worldwide that fall within the genus of Bombus,^[3] although only 50 are native to parts of the US and Canada.^[3] Unlike other members of the family apidae, B. affinis workers and queens are characterized by different color patterns, which allow observes to tell them apart.^[9]

Description and identification

Morphology

There are large differences in morphology between both queens and workers, and males and females.^[9] Queens are approximately 20–22 millimetres (0.79–0.87 in) in length and 9–11 millimetres (0.35–0.43 in) in width, which is larger than workers that are typically about 10–16 millimetres (0.39–0.63 in) in length and 6–9 millimetres (0.24–0.35 in) in width.^[9] Both queens and workers have black hair that covers their head, much of their legs, and the bottom of their abdomens.^[9] They also both have completely yellow hair on the majority of their abdomen, except for a small section near the area closest to the rear end of the bee.^[9] Workers have a slight mixing of yellow and black hairs near the base of the wings, which forms a discernible "v" shape, as well as a rust colored patch of hair on the middle portion of the abdomen.^[9] Thus, while workers and queens share similarities in certain aspects of coloration, there are also differences in terms of body size and the presence or absence of rust colored patch of hair.^[9] Regardless of the caste within the colony, all members of B. affinis have significantly shorter tongues than any other species of bumblebee.^[9] Because of its body size and fury appearance, however, this bee is often confused with other species of bumblebee, such as B. citrinus, B. griseocollis, B. perplexus, and B. vagans.

Furthermore, male and female workers of B. affinis also differ in terms of their appearance and body size. Male workers are typically slightly larger than females (13–17.5 millimetres (0.51–0.69 in) in length), and have a few off-white/pale hairs that are present on top of their head.^[9] They also have black hair which will sometimes streak across the top of the abdomen (which is typically yellow).^[9] Finally, males can even have pale yellow hair on the abdomen, as opposed to the normal shade of yellow that is observed in females and queens.^[9]

Nests

Members of B. affinis are known to build their nests underground in locations such as ditches on the side of the road, wetlands, and fields.^[8] However, there are instances where nests are constructed above ground in chunks of grass and dirt, which can be limited by the availability of open grasslands.^[9] An interesting fact about the B. affinis nest is that a nest was once found inside an armchair that was abandoned outside.^[3] When nests are constructed underground though, they are typically located 16–18 inches (410–460 mm) below the surface, and are composed of soft dirt.^[9]

Distribution and habitat

B. affinis requires three different types of habitats (each for foraging, nesting, and hibernating)^[8] which are geographically close to one another; making this species particularly vulnerable to extinction.^[8] As previously mentioned, this species is commonly found in the eastern regions of the United States and Southern areas of Canada, including Ontario.^[8] It requires a temperate climate, and can even withstand cold temperatures that most species of bumblebees cannot.^[3] In addition, B. affinis has been found at elevations as high as 1600m.^[3] B. affinis is known to visit a number of sites for foraging, including sand dunes, farmland, and marshes, and wooded areas.^[3] Members will actively forage between the months of April and October, and thus, require flowers to bloom for a lengthy amount of time.^[3] Furthermore, their nesting habitat is often found underground.^[3] B. affinis nests are strikingly similar to other species of bees, which makes them difficult to locate.^[3] However, queen and workers will work together to make individual cells and honey pots out of wax stores.^[10] In terms of their hibernating habitat, little information is known.^[3] It is not thought that B. affinis queens will overwinter, however, they most likely will live underground or burrow into rotting logs during the winter time to survive.^[3] While B. affinis' habitat used to be highly prevalent, there has been a large decline in recent years, possibly due to increased land development and agricultural use.^[8]

Until the 1980s, it was one of the most common species of bumblebee in southern Ontario. Since then, the species has had a drastic decline in number and is now difficult to find in its normal range.^[5] The only locality within Ontario where the rusty-patched bumblebee has been seen in the last five years is Pinery Provincial Park (Lambton County), despite widespread surveys in Ontario.^[5] The Ontario Ministry of Natural Resources has begun a recovery project aimed at protecting the species and critical habitats centered in Pinery Provincial Park.^[5] These threats have been proposed as the cause of population decline: pathogen spillover from other species, pesticide use, and habitat fragmentation and loss.^[5] Surveys from 2001–2008 have located Bombus affinis populations only in Illinois, Iowa, Maryland, and southern Ontario^[4].

Colony cycle

Colony initiation and growth

New colonies are started by B. affinis in the spring and decline in the fall.^[8] Members of this species will actually emerge before most other species of Bombus, and will continue foraging after other species have begun hibernating.^[8] Solitary queens will be the first to emerge and begin searching for a colony, while also collecting nectar and pollen to feed her future brood.^[9] The queen uses sperm she has saved from her mating activities of the previous fall to fertilize her eggs.^[9] Eggs will hatch about four days after fertilization, but will take up to 5 weeks to become completely developed adults depending on temperature and food availability.^[3] In the first few weeks after laying her brood, the queen is solely responsible for feeding her young.^[9] However, shortly afterwards, her female worker offspring will begin collecting food for the colony in preparation for more offspring.^[9] Once the workers are able to become the primary caretakers of the nest, the queen can focus on laying more eggs.^[9] At this point (which is about halfway through the summer) the number of workers will reach an optimal number and the queen will begin producing males and potential queens.^[9] Colony sizes can range anywhere from 50 to approximately 400 individuals, although colonies that are raised in captivity are known to get much larger, having as many members as 2100.^[9]

Colony decline

During this half-way point in the summer, any members with reproductive potential will leave the nest and begin mating.^[3] The number of potential queens that can be produced is heavily reliant on the amount of nectar and pollen that can gathered during this time.^[9] Thus, a shortage of food may result in lesser queen production, and vice versa.^[9] But because solitary queens are the only members of the B. affinis that can initiate new colonies, the success of future colonies is dependent on queen production.^[9] Furthermore, after mating, new queens will rest and enter into diapause, or hibernation for the winter.^[9] Male members and workers will decline as the weather gets colder, and will eventually die when winter comes.^[3] Thus, colonies live for about 4–5 months depending on the environmental conditions.^[3] It is important to note that it is common for queens to die at different times throughout colony production, which can often lead to orphaned colonies.^[11] Queens typically live for about 77 days on average, from the time the colony is created until the time that the queen dies.^[11]

Reproductive suppression

Similar to other social insects, egg laying by B. affinis workers is suppressed by the presence of a dominant queen that is capable of reproducing.^[10] The queen's position as a dominant member or leader of the colony is made known through both pheromones and behavioral patterns.^[10] However, it is strictly the presence of specific pheromones that suppress gonadotropic hormones in B. affinis workers, leading to suppressed reproductive potential.^[10] Recent studies have revealed that there is variability in dominance signals both between certain species, and also between subspecies or subgenera.^[10] For example, in B. terrestris colonies, it is presence or absence of abdominal glands rather than pheromones that dictates the dominance of the queen.^[10] In the absence of a fecund queen, aggression and violence between workers increases quickly.^[10] In addition, ovarian weight is significantly lower in colonies where the queen is present than when she is removed.^[10]

It was previously thought that Bombus bohemicus (an obligate brood parasite of B. affinis) also played a role in suppressing ovarian development in B. affinis, however, it has recently been discovered that this is not the case^[10]. Members of the Psithyrus genus will often maul other members of the host colony, which indirectly decreases the number of eggs laid in the host colony.^[10] B. bohemicus does not demonstrate this behavior, and actually has worse chances of survival in nests where there is not a dominant queen present, due to increased aggression by B. affinis members.^[10] However, it is important to note that while ovarian development is not impacted by the presence of B. bohemicus, overall reproductive success is decreased due to consumption of the host eggs and larval ejection.^[10]

Kin selection

Genetic relatedness

Genetic relatedness within the B. affinis species varies depending on the relationship.^[11] Because members are haplodiploid making males haploid and females diploid, so genetic relatedness is asymmetrical, causing workers to be more closely related to their sisters than their brothers.^[11] B. affinis workers share a correlation coefficient (or variable indicating the strength of the relatedness/ degree of relatedness) of r = 0.75 with full sisters but only r = 0.25 for full brothers.^[12] In addition, workers are also much more closely related to their sons than their own brothers, and even more so than their nephews.^[11] The r value is likely greater than 0.5 for sons.^[12] While it is advantageous for ratio of males to queens to be 1:1 normally, this asymmetry in genetic relatedness results in much conflict between the queen and the workers.^[11] Thus, all members who are workers should demonstrate favor for a predominantly female population (if the queen is the major egg layer in the colony).^[11]

Worker/queen conflict

Differences in genetic relatedness can result in conflict between the B. affinis queen and workers.^[11] This conflict can manifest itself in one of two ways - either through a skewed sex ratio with the absence of any physical aggression, or through direct contact in which one member will act violently towards another member to inhibit reproductive success.^[11] Should aggression manifest itself as skewed sex ratios, the ratio of male to female offspring varies depending on the contribution from queens and workers.^[11] For example, if there is no worker contribution, the ratio will be 1:3 (males to females), however, if contribution is solely from workers, then the ratio be far closer to 1:1.^[11] However, should the aggression manifest itself as violent behaviors, they will often be directed toward a member's brood, through actions such as larval ejection.^[11] This larval ejection is often associated with the degradation of group cohesion, and typically occurs at a late stage in colony development.^[11] It can also be the result of workers attempt to lay their own eggs, independently of the queen.^[11]

Interaction with other species

Parasites

B. affinis is parasitized most extensively by a separate species of bee, Bombus bohemicus, which is an obligate brood parasite.^[7] B. bohemicus will end hibernation shortly after B. affinis, and search for their established nests, however, the exact mechanism is unknown.^[7] It is thought that female members of B. bohemicus are able to locate the host nests by identifying the odor from a distance—without ever having physical contact with the nest or regions that were utilized by workers.^[7] By flying low to the ground and searching carefully (even by looking near leaves and debris), B. bohemicus may first locate the entrance of a B. affinis nest, and then verify their findings via odor identification.^[7] After invading the nest, however, the B. bohemicus will live alongside the queen and the workers, and will also attempt to rear their own brood (who must be raised with host workers' help).^[11] Because larger nests tend to have more workers defending the nest, B. bohemicus often invades smaller nests, which forces it to occupy smaller nests for larger periods of time^[11] B. bohemicus is uniquely found in the nests of B. affinis and B. terricola, where it is usually tolerated if unnoticed. However, B. affinis has been known to exhibit oophagy (or consumption of non-host eggs), larval ejection, and ejection of the parasite in response to parasite presence.^[11] Should B. bohemicus make a mistake in invading the nests of other species, they will be attacked by the queen, whose violent actions often end in their death.^[7]

Diet

B. affinis consumes the nectar and pollen of a variety of nototrobic plant species, including the Lobelia siphilitica, Linaria vulgaris, and Antirrhinum majus.^[13] Dicentra cucullaria, a type of flowering plant, is particularly dependent on members of the B. affinis for sexual reproduction.^[14] In fact, the flower structure and mechanism by which it is pollinated indicate that it is adapted for foragers such as B. affinis, which can separate the outer and inner petals of the flower.^[14] Members will then use their front legs to expose the stigma, stamen, and anthers.^[14] Shortly afterwards, they will sweep pollen in a forward stroke by utilizing their middle legs, before leaving the flower to return to the colony with the pollen.^[13] In this way, the D. cucullaria is pollinated as the bees move from plant to plant, and the B. affinis meets its dietary needs.^[13] This pollen foraging behavior is strikingly similar to bees of the genus Apis.^[14] Species of the Apis variety are lighter in weight though, making it slightly more difficult to gain access.^[13]

Disease

B. affinis is susceptible to a certain species of protozoa, known as Apicystis bombi.^[15] This pathogen impacts about 3% of all Bombus affinis, and is particularly prevalent in Ontario, Canada.^[15] A. bombi first infects the gut of its host, then spreads this infection to the rest of the body.^[16] While its transmission is not well understood, A. bombi causes multiple negative impacts, including increased death of worker bees, and the prevention of formation of new colonies.^[16] It also limits ovarian development of queens, and reduces their lifespans.^[16] Its thought that this disease was introduced to North America by commercial B. terrestris in the early in early 2005 or 2006 when members invaded northern Patagonia, Argentina from Europe.^[15] A. bombi rarely impacts bees occupying Europe (only about 6-8% show signs of infection), however, for European bees living in Patagonia, incidence of infection is closer to about 50% in certain species.^[16] Because of this, there is great concern by conservation experts that A. bombi may be detrimental to several bumblebee species, including B. affinis.^[16]

Importance in agriculture

B. affinis is important to the agricultural industry.^[9] It is known that members of this species pollinate up to 65 different species of plants, and is the primary pollinator of key dietary crops, such as cranberries, plums, apples, onions, and alfalfa.^[3] These crops are important for day-to-day consumption by humans, but are also vital to sustaining other birds and mammals that feed on their fruit.^[3] Plants pollinated by B. affinis (such as Aralia and Spiraea) are used medicinally by aboriginal peoples of Canada known as the First Nations.^[3] Thus, the recent decline of B. affinis could have far reaching affects on ecosystems, economic stability, and cultural traditions.^[3]

In 2008 it was reported that three recent events had led to the decline of B. affinis' agricultural role: pathogen spillover, pesticide use, and habitat loss.^[8] Many bumblebees that are used in commercial businesses harbor harmful parasites that can impact nearby wild populations of B. affinis.^[8] This often has lethal effects, and has led to the decline of B. terricola and B. impatiens, the common eastern bumblebee, as well.^[8] Aside from pathogen spillover, however, novel pesticides also impact populations of B. affinis.^[8] Neonicotinoids in particular are pesticides that are toxic to bees, however, they are commonly used for pest control on crops and turf.^[8] Because B. affinis nests are built underground, they are uniquely susceptible to this pesticide's use on turf.^[9] Lastly, increases in urbanization and industrialization have meant the loss of native habitats.^[8] While other species such as B. bimaculatus, the two-spotted bumble bee, have adapted well to urban environments, B. affinis has not.^[8] It is not known, however, whether or not the reduction of native food plants in particular has impacted B. affinis^[8].

Nectar robbing

Unlike other species of bees, B. affinis queens harvest nectar via "nectar spur perforation" or "nectar robbing".^[14] This unique harvesting behavior is accomplished through a number of maneuvers.^[14] A B. affinis queen must first hang inverted from the edges of the inner petals (occasionally using a neighboring flower to steady herself).^[14] After squeezing her head in the space between the inner and outer petals, and using her front legs to push the inner petal forward, she will perforate the inner petal to gain easy access to the spur.^[14] Because B. affinis has a relatively short tongue,^[9] this enables them to have easy access to the spurs, where nectar is abundant (Other species of bee, such as B. fervidus have much longer tongues, which allows them to gather nectar via the flower's primary opening).^[14] After gathering the nectar, the queen then rotates her head, sweeps pollen from her legs, and leaves.^[14] This behavior does not affect plant fertility, nor does it prevent cross pollination from taking place (as evidenced by the presence of fruit on plants with perforated spurs).^[14]

See also

• List of bumblebee species

References

1. Bombus affinis, IUCN
2. "Bombus affinis". Biolib.cz. Retrieved 18 Sep 2013.
3. Canada, Government of Canada, Environment. "COSEWIC Assessment and Status Report on the Rusty–patched Bumble Bee Bombus affinis in Canada – 2010 - Species at Risk Public Registry". registrelep-sararegistry.gc.ca. Retrieved 2015-10-11.
4. Rusty-patched Bumblebee, Xerces Society
5. "Rusty-patched Bumblebee (Bombus affinis) in Ontario Ontario Recovery Strategy Series" (PDF). Recovery strategy prepared under the Endangered Species Act, 2007. Ministry of Natural Resources. 2011. Retrieved 8 August 2012.
6. Zuckerman, Laura (September 22, 2016). "Rusty patched bumble bee proposed for U.S. endangered species status". Reuters. Retrieved September 26, 2016.
7. "Recognition of Host Nest Odour by the Bumblebee Social Parasite Psithyrus ashtoni (Hymenoptera: Apidae) on JSTOR". JSTOR 25009392.
8. Colla, Sheila R.; Packer, Laurence (2008-02-08). "Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson". Biodiversity and Conservation. 17 (6): 1379–1391. doi:10.1007/s10531-008-9340-5. ISSN 0960-3115.
9. Evans, Elaine. "Status Review of Three Formerly Common Species of Bumble Bee in the Subgenus Bombus" (PDF). The Xerces Society for Invertebrate Conservation. The Xerces Society for Invertebrate Conservation. Retrieved 10 October 2015.
10. "Inability of the Social Parasite Psithyrus ashtoni to Suppress Ovarian Development in Workers of Bombus affinis (Hymenoptera: Apidae) on JSTOR". JSTOR 25084374.
11. "Queen-worker conflict and social parasitism in bumble bees (Hymenoptera: Apidae)". Animal Behaviour. 35: 1026–1036. doi:10.1016/S0003-3472(87)80159-8. Retrieved 2015-10-13.
12. Gadagkar, Raghavendra (1991-04-01). "On testing the role of genetic asymmetries created by haplodiploidy in the evolution of eusociality in the Hymenoptera". Journal of Genetics. 70 (1): 1–31. doi:10.1007/BF02923575. ISSN 0022-1333.
13. "Pollen-Foraging Behavior of Bombus in Relation to Pollination of Nototribic Flowers on JSTOR". JSTOR 2440764.
14. Macior, Lazarus Walter (1970-01-01). "The Pollination Ecology of Dicentra cucullaria". American Journal of Botany. 57 (1): 6–11. doi:10.2307/2440374. JSTOR 2440374.
15. Jepsen, Sarina, et al. "Petition to List the Rusty Patched Bumble Bee Bombis Affinis (Cresson, 1863) as an Endangered Species Under the U.S. Endangered Species Act." The Xerces Society for Invertebrate Conservation, 31 Jan 2013. PDF File. 12 Oct 2015.http://www.xerces.org/wp-content/uploads/2013/01/Bombus-affinis-petition.pdf
16. "Newsletter of the BumbleBee Specialist Group" (PDF). Bumblebee Conservator. 2014.