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Honey Bee Colony Losses
Various factors have been considered to be contributing to honey bee losses, and recent investigations have established some of the most important ones, in particular, pests and diseases, bee management, including bee keeping practices and breeding, the change in climatic conditions, agricultural practices, and the use of pesticides. The global picture highlights the ectoparasitic mite Varroa destructor as a major factor in colony loss. Last but not least, microsporidian parasites, mainly Nosema ceranae, also contribute to the problem. Thus, it is obvious that there are many factors affecting honey bee colony losses globally. Increased monitoring and scientific research should throw new light on the factors involved in recent honey bee colony losses.
Managed honey bees are the most important pollinators for many crops and wild flowering species. Many countries worldwide, particularly in the Northern hemisphere, rely on the Western honey bee, Apis mellifera, for commercial pollination of certain crops, but over the recent years there has been an increase in losses in managed honey bee colonies in some regions of the world. Colony collapse disorder (CCD) has been reported for the first time in 2006 in the USA . Although some bee losses have also been reported in China and Japan, published data from various investigations have shown that honey bee colony numbers have been stable for the past ten years in these regions . The global picture has shown that there are no significant honey bee colony losses reported in Africa, Australia and South America. In the Middle East, the high temperatures and droughts in the summer are the main factor leading to colony losses because many plants, which are important sources for bee forage, suffer from heat stress . Another factor aggravating the problem is the lack of comprehensive laws and legislations concerning the importation of bee colonies .
Indeed, bee colony losses are not a new phenomenon, and historical records show that extensive losses were not unusual in the past. Whilst recent problems may give the impression that there has been a massive decline, global research on honey bee colonies has shown that numbers actually increased between 1961 and 2007, mostly in Asia (426%), Africa (130%), South America (86%), and Oceania (39%) . The most significant honey bee colony losses take place during overwintering, as shown by comparisons of colonies going into wintering and surviving the winter. The latter is a symptom of CCD, which has appeared in Europe, causing losses of up to 30% in some countries . It has been difficult to determine a common pattern for the colony losses, but different investigations confirm that it is a phenomenon characteristic of the Western honey bee, while the Asiatic honey bee, present in southern, southeastern, and eastern Asia, appears to be more resistant to various pests and diseases .
2. Role of Pests as Drivers Leading to Honey Bee Colony Losses
To understand the causes underlying the current decrease in honey bee colonies worldwide, it is important to shed light on the key pests and diseases that negatively affect bee health. Honey bees can be affected by various pests and diseases, including mites, different viruses, microsporidia, bacterial infections, and fungi (Ascosphaera apis) (Table 1). Due to the burden of infectious diseases and their agents, honey bee colonies may manifest significant weakness or even death. Only recently have scientists come to understand better the impact of the development and interactions of these pests and diseases.
Table 1. Some honey bee pests and diseases correlated with colony losses.
|Type of Pathogen||Kind of Relationship||References|
|Varroa destructor||Ectoparasitic mite|||
|Acarapis woodi||Tracheal mite|||
|Varroa jacobsoni||Ectoparasitic mite|||
|Tropilaelaps clareae||Ectoparasitic mite|||
|Deformed wing virus A||Viral pathogen|||
|Deformed wing virus B (VDV1)|
|Acute bee paralysis virus|
|Kashmir bee virus|
|Israeli acute paralysis virus|
|Chronic bee paralysis|
|Black queen cell virus|
|Nosema ceranae||Intestinal parasites|||
|Ascosphaera apis||Fungal pathogen|||
|Aethina tumida||Beekeeping pest|||
2.1. Parasitic Mites
Honey bee hives can be a suitable habitat for various mites (Acari), including nonparasitic, omnivorous, pollen-feeding species, and parasites. Out of the different mite species associated with honey bees, Varroa destructor, Acarapis woodi, Varroa jacobsoni and Tropilaelaps clareae are economically significant pests of honey bees, and their infestation may lead to the destruction of the beekeeping industry in many cases . Varroa destructor is the most serious pest of honey bee colonies around the world, as it is an obligate parasite which is able to attack different developmental stages and castes of A. mellifera . It is interesting to note that Varroa mites have been established in New Zealand since 2000, but as of yet, Australia is still Varroa-free . Additionally, in Africa, African honey bees seem to survive despite the presence of Varoa destructor, as do the Africanized honey bees in South America . It is well known that the ectoparasitic mite Varroa destructor switched hosts from Eastern honey bees (Apis cerana) to Western honey bees (Apis mellifera) . Thus, the Western honey bee has shown more susceptibility than Apis cerana. This increased resistance of the Africanized honey bees against V. destructor may be explained with their more aggressive behavior than the Western honey bee . The association of V. destructor with the Western honey bee has led to a significant reduction of honey bee colonies.
2.2. Honey Bee-Associated Viruses
About 24 honey bee-associated viruses have been identified in the Western honey bee (Apis mellifera) . Some of them generally persist in the bee’s body, without causing a disease or manifestation of any clinical signs. In general, virus infestations were not considered to be a significant problem to honey bee health. On the other hand, some viruses are more virulent and infective, and thus may cause a significant loss in honey bee colonies as well as a decline in honey bees’ health and production . Some viruses show pathogenicity only under certain favorable environmental conditions.
Varroa mites V. destructor are considered to be the main transmitter of many honey bee viruses: deformed wing virus (DWV); acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), and Israeli acute paralysis virus (IAPV) . Furthermore, three viruses in the transmission of which Varroa seems to play no significant role, namely, chronic bee paralysis virus (CBPV), sacbrood virus (SBV), and black queen cell virus (BQCV) are also frequently surveyed . This fact allows to us think that Varroa mites alone are not the (only) cause of honey bee losses. The negative influence of V. destructor results from its role as a viral reservoir and a transmitter of some honey bee-associated viruses ; the mite promotes replication of honey bee viruses like DWV . Due to its feeding behavior, the Varroa mite injects directly viruses in the hemolymph, which has been associated with oral or sexual transmission of these viruses .
Microsporidia are fungal, obligate intracellular parasites, infectious to honey bees. Microsporidia are possibly the smallest single-cell organisms which have a true nucleus. The genus Nosema is a parasitic fungus infecting insects such as honey bees, bumble bees and silkworms. Until now, only two species of microsporidia, namely, Nosema ceranae and Nosema apis, have been reported to parasitize on adult honey bees . In 2017, a new species of Nosema, named Nosema neumanni, in honey bees from Uganda was reported . It has been established that N. apis is specific for the Western honey bee, Apis mellifera L., whilst the Asiatic bee, Apis cerana, harbors N. ceranae . For a long time, it was believed that N. ceranae and N. apis were species-specific. Since the beginning of this millennium (mainly post 2003), many investigations have revealed that N. ceranae has switched hosts and has become the dominant species in many countries . Thus, it has been suggested that N. ceranae is possibly more virulent than N. apis.
3. Anthropogenic Direct Drivers Associated with Honey Bee Colony Decline
In addition to different pest and diseases as direct natural drivers, there are many other drivers named anthropogenic, that lead to colony losses . In many cases it is the interaction of these factors that leads to morbidity and mortality, and colony losses (Table 2).
Table 2. Environmental factors associated with honey bee colony losses.
|Anthropogenic Direct Drivers that Cause Honey Bee Decline||Impact on Honey Bee||References|
|Pesticides||High rate of mortality, alteration of different biological processes|||
|Climate change||Alteration of honey bee behavior, physiology and distribution, induced changes in flora for honey bees vitality|||
|Introduction of alien species||Competition for food resources, decline of indigenous species, alteration of the new habitat|||
|Genetically Modified Organisms (GMOs) crop||Alteration bees foraging behavior|||
|Land use and management||Habitat and forage loss, honey bee and wild bee competition|||
|Bee management||Hybridity of honey bees, migratory pollination|||
|Environmental pollution||Imbalance in homeostasis, weakening of the immune system|||
|Interactions between drivers||In many cases poorly studied|||
Recent investigations have reported an increase in colony losses in some regions and have stimulated investment in more coordinated monitoring of bees and research on the impact of pests and diseases, bee diversity, bee-keeping practices and bee foraging environments on bee vitality. Factors such as land management and environmental conditions further affect the availability and quality of food sources as well as the conditions in the hive. Effective management of bee colonies under changing situations also depends on beekeeping practices and bee selection. All these diverse factors can affect bees’ vitality and ability to overcome pests and diseases.
This entry is adapted from 10.3390/vetsci7040166
- Neumann, P.; Carreck, N.L. Honey bee colony losses. J. Apic. Res. 2010, 49, 1–6.
- Taniguchi, T.; Kita, Y.; Matsumoto, T.; Kimura, K. Honeybee Colony Losses during 2008~2010 Caused by Pesticide Application in Japan. J. Apic. 2012, 27, 15–27.
- Liu, Z.; Chen, C.; Niu, Q.; Qi, W.; Yuan, C.; Su, S.; Liu, S.; Zhang, Y.; Zhang, X.; Ji, T.; et al. Survey results of honey bee (Apis mellifera) colony losses in China (2010–2013). J. Apic. Res. 2016, 55, 29–37.
- Awad, A.M.; Owayss, A.A.; Alqarni, A.S. Performance of two honey bee subspecies during harsh weather and Acacia gerrardii nectar-rich flow. Sci. Agric. 2017, 74, 474–480.
- Al-Ghamdi, A.; Adgaba, N.; Getachew, A.; Tadesse, Y. New approach for determination of an optimum honeybee colony’s carrying capacity based on productivity and nectar secretion potential of bee forage species. Saudi J. Biol. Sci. 2016, 23, 92–100.
- Potts, S.G.; Roberts, S.P.; Dean, R.; Marris, G.; Brown, M.A.; Jones, R.; Neumann, P.; Settele, J. Declines of managed honey bees and beekeepers in Europe. J. Apic. Res. 2010, 49, 15–22.
- Aston, D. Honey bee winter loss survey for England, 2007–2008. J. Apic. Res. 2010, 49, 111–112.
- Topolska, G.; Gajda, A.; Pohorecka, K.; Bober, A.; Kasprzak, S.; Skubida, M.; Semkiw, P. Winter colony losses in Poland. J. Apic. Res. 2010, 49, 126–128.
- Gray, A.; Adjlane, N.; Arab, A.; Ballis, A.; Brusbardis, V.; Charrière, J.D.; Chlebo, R.; Coffey, M.F.; Cornelissen, B.; Amaro da Costa, C.; et al. Honey bee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018–2019, and the effects of a new queen on the risk of colony winter loss. J. Apic. Res. 2020, 59, 744–751.
- Xu, P.; Shi, M.; Chen, X.X. Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. PLoS ONE 2009, 4, e4239.
- Clermont, A.; Pasquali, M.; Eickermann, M.; Kraus, F.; Hoffmann, L.; Beyer, M. Virus status, varroa levels and survival of 20 managed honey bee colonies monitored in Luxembourg between summer 2011 and spring 2013. J. Apic. Sci. 2015, 59, 59–73.
- Mõtus, K.; Raie, A.; Orro, T.; Chauzat, M.-P.; Viltrop, A. Epidemiology, risk factors and varroa mite control in the Estonian honey bee population. J. Apic. Res. 2016, 55, 396–412.
- Garrido-Bailón, E.; Bartolomé, C.; Prieto, L.; Botías, C.; Martínez-Salvador, A.; Meana, A.; Martín-Hernández, R.; Higes, M. The prevalence of Acarapis woodi in Spanish honey bee (Apis mellifera) colonies. Exp. Parasitol. 2012, 132, 530–536.
- Roberts, J.; Anderson, D.; Tay, W. Multiple host shifts by the emerging honeybee parasite, Varroa jacobsoni. Mol. Ecol. 2015, 24, 2379–2391.
- Waghchoure-Camphor, E.S.; Martin, S.J. Population changes of Tropilaelaps clareae mites in Apis mellifera colonies in Pakistan. J. Apic. Res. 2009, 48, 46–49.
- Posada-Florez, F.; Childers, A.K.; Heerman, M.C.; Egekwu, N.I.; Cook, S.C.; Chen, Y.; Evans, J.D.; Ryabov, E.V. Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Sci. Rep. 2019, 9, 12445.
- De Miranda, J.R.; Cordoni, G.; Budge, G. The acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J. Invertebr. Pathol. 2010, 103, S30–S47.
- Toplak, I.; Jamnikar Ciglenečki, U.; Aronstein, K.; Gregorc, A. Chronic bee paralysis virus and Nosema ceranae experimental co-infection of winter honey bee workers (Apis mellifera L.). Viruses 2013, 5, 2282–2297.
- Li, J.; Wang, T.; Evans, J.D.; Rose, R.; Zhao, Y.; Li, Z.; Li, J.; Huang, S.; Heerman, M.; Rodríguez-García, C.; et al. The phylogeny and pathogenesis of Sacbrood virus (SBV) infection in European honey bees, Apis mellifera. Viruses 2019, 11, 61.
- Spurny, R.; Přidal, A.; Pálková, L.; Kiem, H.K.T.; de Miranda, J.R.; Plevka, P. Virion structure of black queen cell virus, a common honeybee pathogen. J. Virol. 2017, 91, e02100-16.
- Vejsnaes, F.; Neilsen, S.L.; Kryger, P. Factors involved in the recent increase in colony losses in Denmark. J. Apic. Res. 2010, 49, 109–110.
- Chemurot, M.; De Smet, L.; Brunain, M.; De Rycke, R.; de Graaf, D.C. Nosema neumanni n. sp. (Microsporidia, Nosematidae), a new microsporidian parasite of honeybees, Apis mellifera in Uganda. Eur. J. Protistol. 2017, 61, 13–19.
- Sarwar, M. Fungal diseases of honey bees (Hymenoptera: Apidae) that induce considerable losses to colonies and protocol for treatment. Int. J. Zool. Stud. 2016, 1, 8–13.
- Neumann, P.; Pettis, J.S.; Schäfer, M.O. Quo vadis Aethina tumida? Biology and control of small hive beetles. Apidologie 2016, 47, 427–466.
- Schäfer, M.O.; Cardaio, I.; Cilia, G.; Cornelissen, B.; Crailsheim, K.; Formato, G.; Lawrence, A.K.; Le Conte, Y.; Mutinelli, F.; Nanetti, A.; et al. How to slow the global spread of small hive beetles, Aethina tumida. Biol. Invasions 2019, 21, 1451–1459.
- Neumann, P.; Spiewok, S.; Pettis, J.; Radloff, S.E.; Spooner-Hart, R.; Hepburn, R. Differences in absconding between African and European honeybee subspecies facilitate invasion success of small hive beetles. Apidologie 2018, 49, 527–537.
- Huang, Q.; Lopez, D.; Evans, J.D. Shared and unique microbes between Small hive beetles (Aethina tumida) and their honey bee hosts. Microbiol. Open 2019, 8, e899.
- Mustafa, S.G.; Spiewok, S.; Duncan, M.; Spooner-Hart, R.; Rosenkranz, P. Susceptibility of small honey bee colonies to invasion by the small hive beetle, Aethina tumida (Coleoptera, Nitidulidae). J. Appl. Entomol. 2014, 138, 547–550.
- Ellis, J.D.; Hepburn, H.R. An ecological digest of the small hive beetle (Aethina tumida), a symbiont in honey bee colonies (Apis mellifera). Insectes Sociaux 2006, 53, 8–19.
- Bernier, M.; Fournier, V.; Eccles, L.; Giovenazzo, P. Control of Aethina tumida (Coleoptera: Nitidulidae) using in-hive traps. Can. Entomol. 2015, 147, 97–108.
- Sammataro, D.; Gerson, U.; Needham, G. Parasitic mites of honey bees: Life history, implications, and impact. Annu. Rev. Entomol. 2000, 45, 519–548.
- Dhooria, M.S. Parasitic Mites on Honeybees. In Fundamentals of Applied Acarology; Springer: Singapore, 2016.
- Shen, M.; Cui, L.; Ostiguy, N.; Cox-Foster, D. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. J. Gen. Virol. 2005, 86, 2281–2289.
- Iwasaki, J.M.; Barratt, B.I.; Lord, J.M.; Mercer, A.R.; Dickinson, K.J. The New Zealand experience of varroa invasion highlights research opportunities for Australia. Ambio 2015, 44, 694–704.
- Strauss, U.; Dietemann, V.; Human, H.; Crewe, R.M.; Pirk, C.W. Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destructor. Parasitology 2016, 143, 374–387.
- Beaurepaire, A.L.; Truong, T.A.; Fajardo, A.C.; Dinh, T.Q.; Cervancia, C.; Moritz, R.F. Host specificity in the honeybee parasitic mite, Varroa spp. in Apis mellifera and Apis cerana. PLoS ONE 2015, 10, e0135103.
- Medina Flores, C.A.; Guzmán Novoa, E.; Hamiduzzaman, M.; Aréchiga Flores, C.F.; López Carlos, M.A. Africanized honey bees (Apis mellifera) have low infestation levels of the mite Varroa destructor in different ecological regions in Mexico. Genet. Mol. Res. 2014, 13, 7282–7293.
- Oddie, M.; Büchler, R.; Dahle, B.; Kovacic, M.; Le Conte, Y.; Locke, B.; de Miranda, J.R.; Mondet, F.; Neumann, P. Rapid parallel evolution overcomes global honey bee parasite. Sci. Rep. 2018, 8, 7704.
- Gisder, S.; Genersch, E. Special issue: Honey bee viruses. Viruses 2015, 7, 5603–5608.
- Genersch, E.; Aubert, M. Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet. Res. 2010, 41, 54.
- Ramsey, S.D.; Ochoa, R.; Bauchan, G.; Gulbronson, C.; Mowery, J.D.; Cohen, A.; Lim, D.; Joklik, J.; Cicero, J.M.; Ellis, J.D.; et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc. Natl. Acad. Sci. USA 2019, 116, 1792–1801.
- Locke, B. Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 2016, 47, 467–482.
- Tentcheva, D.; Gauthier, L.; Zappulla, N.; Dainat, B.; Cousserans, F.; Colin, M.E.; Bergoin, M. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol. 2004, 70, 7185–7291.
- Nielsen, S.L.; Nicolaisen, M.; Kryger, P. Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie 2008, 39, 310–314.
- Levin, S.; Sela, N.; Chejanovsky, N. Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Sci. Rep. 2016, 6, 37710.
- Francis, R.M.; Nielsen, S.L.; Kryger, P. Patterns of viral infection in honey bee queens. J. Gen. Virol. 2013, 94, 668–676.
- Paris, L.; El Alaoui, H.; Delbac, F.; Diogon, M. Effects of the gut parasite Nosema ceranae on honey bee physiology and behavior. Curr. Opin. Insect. Sci. 2018, 26, 149–154.
- Fries, I.; Feng, F.; Da Silva, A.; Slemenda, S.B.; Pieniazek, N.J. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol. 1996, 32, 356–365.
- Klee, J.; Besana, A.M.; Genersch, E.; Gisder, S.; Nanetti, A.; Tam, D.Q.; Chinh, T.X.; Puerta, F.; Ruz, J.M.; Kryger, P.; et al. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 2007, 96, 1–10.
- Paxton, R.J.; Klee, J.; Korpela, S.; Fries, I. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007, 38, 558–565.
- Chen, Y.P.; Evans, J.D.; Smith, I.B.; Pettis, J.S. Nosema ceranae is a long-present and widespread microsporidean infection of the European honey bee (Apis mellifera) in the United States. J. Invertebr. Pathol. 2008, 97, 186–188.
- Invernizzi, C.; Abud, C.; Tomasco, I.H.; Harriet, J.; Ramallo, G.; Campa, J.; Katz, H.; Gardiol, G.; Mendoza, Y. Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. J. Invertebr. Pathol. 2009, 101, 150–153.
- Stevanovic, J.; Stanimirovic, Z.; Genersch, E.; Kovacevic, S.R.; Ljubenkovic, J.; Radakovic, M.; Aleksic, N. Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie 2011, 42, 49–58.
- Kovács-Hostyánszki, A.; Espíndola, A.; Vanbergen, A.J.; Settele, J.; Kremen, C.; Dicks, L.V. Ecological intensification to mitigate impacts of conventional intensive land use on pollinators and pollination. Ecol. Lett. 2017, 20, 673–689.
- IPBES. The Assessment Report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on Pollinators, Pollination and Food Production; Potts, S.G., Imperatriz-Fonseca, V.L., Ngo, H.T., Eds.; Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services: Bonn, Germany, 2016; p. 552.
- Al Naggar, Y.; Codling, G.; Vogt, A.; Naiem, E.; Mona, M.; Seif, A.; Giesy, J.P. Organophosphorus insecticides in honey, pollen and bees (Apis mellifera L.) and their potential hazard to bee colonies in Egypt. Ecotoxicol. Environ. Saf. 2015, 114, 1–8.
- Piiroinen, S.; Goulson, D. Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honey bees and bumblebees. Proc. Royal Soc. B. 2016, 283, 20160246.
- Schneider, C.W.; Tautz, J.; Gruenewald, B.; Fuchs, S. RFID tracking of sublethal effects of two neonicotinoids insecticides on the foraging behavior of Apis mellifera. PLoS ONE 2012, 7, e30023.
- Goulson, D. Review: An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 2013, 50, 977–987.
- Le Conte, Y.; Navajas, M. Climate change: Impact on honey bee populations and diseases. Rev. Sci. Tech. OIE J. 2008, 27, 499–510.
- Laurino, D.; Lioy, S.; Carisio, L.; Manino, A.; Porporato, M. Vespa velutina: An Alien Driver of Honey Bee Colony Losses. Diversity 2020, 12, 5.
- Moritz, R.F.; Haddad, N.; Bataieneh, A.; Shalmon, B.; Hefetz, A. Invasion of the dwarf honeybee Apis florea into the near East. Biol. Invasions 2010, 12, 1093–1099.
- Brittain, C.; Williams, N.; Kremen, C.; Klein, A.M. Synergistic effects of non-Apis bees and honey bees for pollination services. Proc. Royal Soc. B 2013, 280, 20122767.
- Kenis, M.; Auger-Rozenberg, M.A.; Roques, A.; Timms, L.; Péré, C.; Cock, M.J.; Settele, J.; Augustin, S.; Lopez-Vaamonde, C. Ecological effects of invasive alien insects. Biol. Invasions 2009, 11, 21–45.
- Han, P.; Niu, C.; Lei, C.-L.; Cui, J.-J.; Desneux, N. Quantification of toxins in a Cry1Ac + CpTI cotton cultivar and its potential effects on the honey bee Apis mellifera L. Ecotoxicology 2010, 19, 1452–1459.
- Durant, J.L.; Otto, C.R. Feeling the sting? Addressing land-use changes can mitigate bee declines. Land Use Policy 2019, 87, 104005.
- Andrews, E. To save the bees or not to save the bees: Honey bee health in the Anthropocene. Agric. Hum. Values 2019, 36, 891–902.
- Dolezal, A.G.; Toth, A.L. Feedbacks between nutrition and disease in honey bee health. Curr. Opin. Insect. Sci. 2018, 26, 114–119.
- Brodschneider, R.; Crailsheim, K. Nutrition and health in honey bees. Apidologie 2010, 41, 278–294.
- Melicher, D.; Wilson, E.S.; Bowsher, J.H.; Peterson, S.S.; Yocum, G.D.; Rinehart, J.P. Long-Distance Transportation Causes Temperature Stress in the Honey Bee, Apis mellifera (Hymenoptera: Apidae). Environ. Entomol. 2019, 48, 691–701.
- Strachecka, A.; Gryzińska, M.; Krauze, M. The influence of environmental pollution on the protective proteolytic barrier of the honey bee Apis mellifera mellifera. Pol. J. Environ. Stud. 2010, 19, 855–859.
- Goulson, D.; Nicholls, E.; Botías, C.; Rotheray, E.L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015, 347, 1255957.
- Giannini, T.C.; Boff, S.; Cordeiro, G.D.; Cartolano, E.A.; Veiga, A.K.; Imperatriz-Fonseca, V.L.; Saraiva, A.M. Crop pollinators in Brazil: A review of reported interactions. Apidologie 2015, 46, 209–223.
- Kerr, J.T.; Pindar, A.; Galpern, P.; Packer, L.; Potts, S.G.; Roberts, S.M.; Rasmont, P.; Schweiger, O.; Colla, S.R.; Richardson, L.L.; et al. Climate change impacts on bumblebees converge across continents. Science 2015, 349, 177–180.
- Aufauvre, J.; Biron, D.G.; Vidau, C.; Fontbonne, R.; Roudel, M.; Diogon, M.; Viguès, B.; Belzunces, L.P.; Delbac, F.; Blot, N. Parasite-insecticide interactions: A case study of Nosema ceranae and fipronil synergy on honeybee. Sci. Rep. 2012, 2, 326.
- Doublet, V.; Labarussias, M.; de Miranda, J.R.; Moritz, R.F.; Paxton, R.J. Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ. Microbiol. 2015, 17, 969–983.
- Retschnig, G.; Neumann, P.; Williams, G.R. Thiacloprid–Nosema ceranae interactions in honey bees: Host survivorship but not parasite reproduction is dependent on pesticide dose. J. Invertebr. Pathol. 2014, 118, 18–19.
- Paoli, P.P.; Donley, D.; Stabler, D.; Saseendranath, A.; Nicolson, S.W.; Simpson, S.J.; Wright, G.A. Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age. Amino Acids 2014, 46, 1449–1458.
- Barber, N.A.; Soper Gorden, N.L. How do belowground organisms influence plant–pollinator interactions? J. Plant Ecol. 2015, 8, 1–11.
- Hladun, K.R.; Parker, D.R.; Tran, K.D.; Trumble, J.T. Effects of selenium accumulation on phytotoxicity, herbivory, and pollination ecology in radish (Raphanus sativus L.). Environ. Pollut. 2013, 172, 70–75.
- Vanbergen, A.J.; Initiative, T.I.P. Threats to an ecosystem service: Pressures on pollinators. Front. Ecol. Environ. 2013, 11, 251–259.