Clarity on Honey Bee Collapse?

Ratnieks, Francis L. W.; Carreck, Norman

doi:10.1126/science.1185563

Cited by 255 publications

(195 citation statements)

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“…Hence, reports on a steady decline in honeybee populations in Europe, USA and Japan in the recent past (for a review see vanEngelsdorp & Meixner, 2010) caused great concern and several studies were initiated to identify the underlying cause. From these studies it became more and more evident that the key players in most of the 'inexplicable' colony losses are pathogens (Ratnieks & Carreck, 2010). Especially, the ectoparasitic mite Varroa destructor in concert with certain pathogenic bee viruses played a major role in the observed colony collapses (Cox-Foster et al, 2007;Genersch et al, 2010; Guzmán-Novoa et al, 2010;Highfield et al, 2009;Siede et al, 2008;vanEngelsdorp, 2008;vanEngelsdorp et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route

Möckel

Gisder

Genersch

2010

Journal of General Virology

161

191

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Recent reports on a steady decline of honeybee colonies in several parts of the world caused great concern. There is a consensus that pathogens are among the key players in this alarming demise of the most important commercial pollinator. One of the pathogens heavily implicated in colony losses is deformed wing virus (DWV). Overt DWV infections manifested as deformed-wing syndrome started to become a threat to honeybees only in the wake of the ectoparasitic mite Varroa destructor, which horizontally transmits DWV. However, a direct causal link between the virus and the symptom 'wing deformity' has not been established yet. To evaluate the impact of different horizontal transmission routes, and especially the role of the mite in the development of overt DWV infections, we performed laboratory infection assays with pupae and adult bees. We could demonstrate that pupae injected with DWV dose-dependently developed overt infections characterized by deformed wings in adult bees, suggesting that DWV, if transmitted to pupae by the mite, is the causative agent of the deformed-wing syndrome. The OID 50 (overt infection dosage) was approximately 2500 genome equivalents. Injecting more than 1¾10 7 DWV genome equivalents into adult bees also resulted in overt infections while the same viral dosage fed to adult bees only resulted in covert infections. Therefore, both infection of adult bees through DWVtransmitting phoretic mites and infection of nurse bees through their cannibalizing DWV-infected pupae might represent possible horizontal transmission routes of DWV. INTRODUCTIONManaged honeybees are indispensable for profitable and sustainable agriculture and for many non-agricultural ecosystems because of the extraordinary pollination service they provide. Hence, reports on a steady decline in honeybee populations in Europe, USA and Japan in the recent past (for a review see vanEngelsdorp & Meixner, 2010) caused great concern and several studies were initiated to identify the underlying cause. From these studies it became more and more evident that the key players in most of the 'inexplicable' colony losses are pathogens (Ratnieks & Carreck, 2010). Especially, the ectoparasitic mite Varroa destructor in concert with certain pathogenic bee viruses played a major role in the observed colony collapses (Cox-Foster et al., 2007;Genersch et al., 2010; Guzmán-Novoa et al., 2010;Highfield et al., 2009;Siede et al., 2008;vanEngelsdorp, 2008;vanEngelsdorp et al., 2009).One of the viruses heavily implicated in colony losses is Deformed wing virus (DWV), a plus-stranded RNA virus belonging to the genus Iflaviridae (Lanzi et al., 2006). DWV normally causes covert infections in honeybees (de Miranda & Fries, 2008;Hails et al., 2008;Yue et al., 2007). Overt DWV infections characterized by the occurrence of visible disease symptoms (deformed wings, bloated and shortened abdomen, and miscolouring) are associated with V. destructor infestation (Ball & Allen, 1988;Bowen-Walker et al., 1999;Martin, 2001;Martin et al., 1998; Santillán-Galicia et...

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Section: Introductionmentioning

confidence: 99%

Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route

Möckel

Gisder

Genersch

2010

Journal of General Virology

161

191

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“…In the United States these losses have been also attributed to a complex syndrome, denoted as colony collapse disorder (CCD), the basis of which is still poorly understood (3). A specific causal agent has not yet been identified, but there is a wide consensus on the multifactorial origin of colony losses that are often associated with high infection levels of parasites and/or pathogens (4,5). This indirectly suggests the possible occurrence of reduced immunocompetence in bees challenged by different stress agents.…”

mentioning

confidence: 99%

Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees

Prisco

Cavaliere

Annoscia

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

579

445

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Large-scale losses of honey bee colonies represent a poorly understood problem of global importance. Both biotic and abiotic factors are involved in this phenomenon that is often associated with high loads of parasites and pathogens. A stronger impact of pathogens in honey bees exposed to neonicotinoid insecticides has been reported, but the causal link between insecticide exposure and the possible immune alteration of honey bees remains elusive. Here, we demonstrate that the neonicotinoid insecticide clothianidin negatively modulates NF-κB immune signaling in insects and adversely affects honey bee antiviral defenses controlled by this transcription factor. We have identified in insects a negative modulator of NF-κB activation, which is a leucine-rich repeat protein. Exposure to clothianidin, by enhancing the transcription of the gene encoding this inhibitor, reduces immune defenses and promotes the replication of the deformed wing virus in honey bees bearing covert infections. This honey bee immunosuppression is similarly induced by a different neonicotinoid, imidacloprid, but not by the organophosphate chlorpyriphos, which does not affect NF-κB signaling. The occurrence at sublethal doses of this insecticide-induced viral proliferation suggests that the studied neonicotinoids might have a negative effect at the field level. Our experiments uncover a further level of regulation of the immune response in insects and set the stage for studies on neural modulation of immunity in animals. Furthermore, this study has implications for the conservation of bees, as it will contribute to the definition of more appropriate guidelines for testing chronic or sublethal effects of pesticides used in agriculture.Apis mellifera | DWV | NLR (CLR) | neuroimmunity | toxicology

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“…Indeed, apiculture is facing a major crisis owing to concurrent factors, such as landscape deterioration, agrochemicals, and parasites (2). Honey bee colony losses have been a major problem since the beginning of modern apiculture (3); however, in 2006, the dramatic dimension of this phenomenon attracted public attention and increasing interest in the scientific community.…”

mentioning

confidence: 99%

A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

Prisco

Annoscia

Margiotta

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

220

228

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Honey bee colony losses are triggered by interacting stress factors consistently associated with high loads of parasites and/or pathogens. A wealth of biotic and abiotic stressors are involved in the induction of this complex multifactorial syndrome, with the parasitic mite Varroa destructor and the associated deformed wing virus (DWV) apparently playing key roles. The mechanistic basis underpinning this association and the evolutionary implications remain largely obscure. Here we narrow this research gap by demonstrating that DWV, vectored by the Varroa mite, adversely affects humoral and cellular immune responses by interfering with NF-κB signaling. This immunosuppressive effect of the viral pathogen enhances reproduction of the parasitic mite. Our experimental data uncover an unrecognized mutualistic symbiosis between Varroa and DWV, which perpetuates a loop of reciprocal stimulation with escalating negative effects on honey bee immunity and health. These results largely account for the remarkable importance of this mite-virus interaction in the induction of honey bee colony losses. The discovery of this mutualistic association and the elucidation of the underlying regulatory mechanisms sets the stage for a more insightful analysis of how synergistic stress factors contribute to colony collapse, and for the development of new strategies to alleviate this problem.Apis mellifera | Varroa destructor | deformed wing virus | mutualistic symbiosis | honeybee colony losses

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Clarity on Honey Bee Collapse?

Abstract: The worldwide losses of honey bee colonies continue to puzzle researchers and the beekeeping industry.

Cited by 255 publications

References 9 publications

Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route

Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route

Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees

A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

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