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Federal Register / Vol. 86, No. 161 / Tuesday, August 24, 2021 / Rules and Regulations
and parasites are widespread generalists in the host genus, but affect species differently according to host susceptibility and tolerance to infection Kissinger et al. 2011, p. 221; Malfi and Roulston 2014, p. 18. The host species life history plays a role in the virulence of a given pathogen; for instance, parasites may have relatively smaller effects on species with shorter colony life cycles and smaller colony sizes Rutrecht and Brown 2009, entire.
Pathogen spillover is a process whereby parasites and pathogens spread from commercial bee colonies to native bee populations Colla et al. 2006, p.
461; Otterstatter and Thompson 2008, p.
1. The decline of certain Bombus species from the mid-1990s to present, particularly species in the subgenus Bombus sensu stricto including Franklins bumble bee, was contemporaneous with the collapse of commercially bred western bumble bee raised primarily to pollinate greenhouse tomato and sweet pepper crops beginning in the late 1980s Szabo et al. 2012, pp. 232233. This collapse was attributed to infections of Nosema bombi.
Nosema bombi has been detected in native bumble bees in North America, and has been found to be a part of the natural pathogen load. The fungus has been reported in Canada since the 1940s Cordes et al. 2011, p. 7 and appears to have a broad host range in North American Kissinger et al. 2011, p. 222.
Infections of the pathogen primarily occur in the malpighian tubules small excretory or water regulating glands, but also in fat bodies, nerve cells, and sometimes the trachea Macfarlane et al.
1995. Bombus colonies can appear to be healthy but still carry N. bombi and transmit it to other colonies, most likely when spores are fed to larvae and then infected adults drift into non-natal colonies Service 2018a, p. 25.
While we have no evidence of direct effects of a virulent strain of N. bombi on the Franklins bumble bee, N. bombi has been detected in closely related species in the range of the Franklins bumble bee. Furthermore, N. bombi infections in rare species like the Franklins bumble bee are more frequent, are more severe, and seem to affect a higher percentage of individuals of the species Cameron et al. 2011, entire; Cordes et al. 2011, p. 2.
The effect of pathogens on bumble bees varies from mild to severe Macfarlane et al. 1995; Rutrecht et al.
2007, p. 1719; Otti and Schmid-Hempel 2008, p. 577. Bumble bees infected with Nosema bombi may have crippled wings, and queens may have distended abdomens and be unable to mate Otti
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and Schmid-Hempel 2007, pp. 122
123. Malfi and Roulston 2014, p. 24
found that N. bombi infections are more frequent and more severe in rare species, and the species with the highest percentages of infected individuals were rare species. Furthermore, the effects of pathogen infection on bumble bees may be amplified by other influence factors.
Nutritional stress may compromise the ability of bumble bees to survive parasitic infections, as evidenced by a significant difference in mortality in bumble bees on a restricted diet compared to well-fed bees infected with C. bombi Brown et al. 2000, pp. 424
425.
A virulent strain of Nosema bombi from the buff-tailed bumble bee Bombus terrestris may have spread to the eastern bumble bee B. impatiens and western bumble bee from Europe. In the mid-1990s, companies shipped queen eastern and western bumble bees to Europe for their development into colonies to use in commercial pollination services. When the colonies had reached sufficient size, they were shipped back to the United States and deployed in industrial greenhouse operations in California, primarily to pollinate tomatoes and peppers. The colonies may have picked up N. bombi prior to their shipment back into the United States, and once in this country, the commercially reared colonies may have spread the virulent strain to wild populations of Franklins bumble bee Xerces Society and Thorp 2010, p. 14.
In work partially funded by the Service, the University of Illinois conducted surveys for parasites and pathogens in bumble bee populations of the Pacific Northwest and Midwest between 2005
and 2009. The goal was to assess Bombus populations for presence and prevalence of pathogens, particularly microsporidia, in an effort to provide baseline data to assess disease as a potential factor in the decline of the Franklins bumble bee, western bumble bee, and American bumble bee B.
pensylvanicus Solter et al. 2010, p. 1.
The highest prevalence of N. bombi was found in western bumble bee, with 26
percent of collected individuals infected. Crithidia bombi infections of western bumble bee were 2.8 percent overall Solter et al. 2010, pp. 34; no Franklins bumble bees were collected during the study. However, Mt.
Ashland, Oregon, was one of only three sites in the Pacific Northwest study area where N. bombi infections were found in multiple Bombus species the indiscriminate cuckoo bumble bee B.
insularis and black-notched bumble bee B. bifarius Solter et al. 2010, pp. 3

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4. Although Cordes et al. 2011, p. 7
found a new allele in N. bombi, the recent study by Cameron et al. 2016
found no evidence of an exotic strain of N. bombi.
In summary, known pathogens occur within the historical range of the Franklins bumble bee, and we have evidence of several pathogens infecting closely related species within that range that have also likely affected the Franklins bumble bee. Although we have no direct evidence of pathogens playing a role in the decline of the Franklins bumble bee, the disappearance of the Franklins bumble bee occurred soon after a period of potential exposure to introduced pathogens, particularly N. bombi, which is known to have a more severe impact on rare species like the Franklins bumble bee. Decline of other closely related pollinators has been associated with these pathogens, and it is highly likely pathogens have had some negative influence on the resiliency of Franklins bumble bee populations.
Pesticide Use Exposure to pesticides can occur to bumble bees from direct spray or drift, or from gathering or consuming contaminated nectar or pollen Johansen and Mayer 1990; Morandin et al. 2005, p. 619. Lethal and sublethal effects on bumble bee eggs, larvae, and adults have been documented for many different pesticides under various scenarios Service 2018a, p. 28. Documented sublethal effects to individual bumble bees and colonies include reduced or no male production, reduced or no egg hatch, reduced queen production, reduced queen longevity, reduced colony weight gain, reduced brood size, reduced feeding, impaired ovary development, and an increased number of foragers or foraging trips or duration interpreted as risky behaviors Service 2018a, p. 28. Bumble bee habitat can also be impacted by pesticides due to changes in vegetation and the removal or reduction of flowers needed to provide consistent sources of pollen, nectar, and nesting material Service 2018a, p. 28. Declines in bumble bees in parts of Europe have been at least partially attributed to the use of pesticides Williams 1986, p. 54; Kosior et al. 2007, p. 81.
Although the use of land for agricultural purposes has traditionally involved the use of pesticides and other products toxic to bees, one particular class of insecticides known as neonicotinoids have been strongly implicated in the decline of honey bees Apis spp. worldwide, and implicated in the decline of several Bombus
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