Review Special Issues

Review on mathematical modeling of honeybee population dynamics


  • Received: 31 August 2021 Accepted: 11 October 2021 Published: 04 November 2021
  • Honeybees have an irreplaceable position in agricultural production and the stabilization of natural ecosystems. Unfortunately, honeybee populations have been declining globally. Parasites, diseases, poor nutrition, pesticides, and climate changes contribute greatly to the global crisis of honeybee colony losses. Mathematical models have been used to provide useful insights on potential factors and important processes for improving the survival rate of colonies. In this review, we present various mathematical tractable models from different aspects: 1) simple bee-only models with features such as age segmentation, food collection, and nutrient absorption; 2) models of bees with other species such as parasites and/or pathogens; and 3) models of bees affected by pesticide exposure. We aim to review those mathematical models to emphasize the power of mathematical modeling in helping us understand honeybee population dynamics and its related ecological communities. We also provide a review of computational models such as VARROAPOP and BEEHAVE that describe the bee population dynamics in environments that include factors such as temperature, rainfall, light, distance and quality of food, and their effects on colony growth and survival. In addition, we propose a future outlook on important directions regarding mathematical modeling of honeybees. We particularly encourage collaborations between mathematicians and biologists so that mathematical models could be more useful through validation with experimental data.

    Citation: Jun Chen, Gloria DeGrandi-Hoffman, Vardayani Ratti, Yun Kang. Review on mathematical modeling of honeybee population dynamics[J]. Mathematical Biosciences and Engineering, 2021, 18(6): 9606-9650. doi: 10.3934/mbe.2021471

    Related Papers:

  • Honeybees have an irreplaceable position in agricultural production and the stabilization of natural ecosystems. Unfortunately, honeybee populations have been declining globally. Parasites, diseases, poor nutrition, pesticides, and climate changes contribute greatly to the global crisis of honeybee colony losses. Mathematical models have been used to provide useful insights on potential factors and important processes for improving the survival rate of colonies. In this review, we present various mathematical tractable models from different aspects: 1) simple bee-only models with features such as age segmentation, food collection, and nutrient absorption; 2) models of bees with other species such as parasites and/or pathogens; and 3) models of bees affected by pesticide exposure. We aim to review those mathematical models to emphasize the power of mathematical modeling in helping us understand honeybee population dynamics and its related ecological communities. We also provide a review of computational models such as VARROAPOP and BEEHAVE that describe the bee population dynamics in environments that include factors such as temperature, rainfall, light, distance and quality of food, and their effects on colony growth and survival. In addition, we propose a future outlook on important directions regarding mathematical modeling of honeybees. We particularly encourage collaborations between mathematicians and biologists so that mathematical models could be more useful through validation with experimental data.



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    [1] K. M. Smith, E. H. Loh, M. K. Rostal, C. M. Zambrana-Torrelio, L. Mendiola, P. Daszak, Pathogens, pests, and economics: drivers of honey bee colony declines and losses, EcoHealth, 10 (2013), 434–445. doi: 10.1007/s10393-013-0870-2
    [2] R. Johnson, Honey Bee Colony Collapse Disorder, CRS Report for Congressional Research Service Washington, Washington, D. C., 2010.
    [3] S. S. Chopra, B. R. Bakshi, V. Khanna, Economic dependence of us industrial sectors on animal-mediated pollination service, Environ. Sci. Technol., 49 (2015), 14 441–14 451. doi: 10.1021/es505828n
    [4] D. vanEngelsdorp, M. D. Meixner, A historical review of managed honey bee populations in europe and the united states and the factors that may affect them, J. Invertebr. Pathol., 103 (2010), S80–S95. doi: 10.1016/j.jip.2009.06.011
    [5] G. DeGrandi-Hoffman, H. Graham, F. Ahumada, M. Smart, N. Ziolkowski, The economics of honey bee (hymenoptera: Apidae) management and overwintering strategies for colonies used to pollinate almonds, J. Econ. Entomol., 112 (2019), 2524–2533. doi: 10.1093/jee/toz213
    [6] E. Genersch, American foulbrood in honeybees and its causative agent, paenibacillus larvae, J. Invertebr. Pathol., 103 (2010), S10–S19. doi: 10.1016/j.jip.2009.06.015
    [7] E. Guzmán-Novoa, L. Eccles, Y. Calvete, J. Mcgowan, P. G. Kelly, A. Correa-Benítez, Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (apis mellifera) colonies in Ontario, Canada, Apidologie, 41 (2010), 443–450. doi: 10.1051/apido/2009076
    [8] C. Van Dooremalen, L. Gerritsen, B. Cornelissen, J. J. van der Steen, F. van Langevelde, T. Blacquiere, Winter survival of individual honey bees and honey bee colonies depends on level of varroa destructor infestation, PloS One, 7 (2012), e36285. doi: 10.1371/journal.pone.0036285
    [9] A. C. Highfield, A. El Nagar, L. C. Mackinder, L. M. L. Noël, M. J. Hall, S. J. Martin, et al., Deformed wing virus implicated in overwintering honeybee colony losses, Appl. Environ. Microbiol., 75 (2009), 7212–7220. doi: 10.1128/AEM.02227-09
    [10] M. A. Doeke, M. Frazier, C. M. Grozinger, Overwintering honey bees: biology and management, Curr. Opin. Insect Sci., 10 (2015), 185–193. doi: 10.1016/j.cois.2015.05.014
    [11] B. A. Williams, Unique physiology of host-parasite interactions in microsporidia infections, Cell. Microbiol., 11 (2009), 1551–1560. doi: 10.1111/j.1462-5822.2009.01362.x
    [12] R. Martín-Hernández, C. Botías, L. Barrios, A. Martínez-Salvador, A. Meana, C. Mayack, et al., Comparison of the energetic stress associated with experimental nosema ceranae and nosema apis infection of honeybees (apis mellifera), Parasitol. Res., 109 (2011), 605–612. doi: 10.1007/s00436-011-2292-9
    [13] C. Mayack, D. Naug, Energetic stress in the honeybee apis mellifera from nosema ceranae infection, J. Invertebr. Pathol., 100 (2009), 185–188. doi: 10.1016/j.jip.2008.12.001
    [14] L. Paris, H. El Alaoui, F. Delbac, M. Diogon, Effects of the gut parasite nosema ceranae on honey bee physiology and behavior, Curr. Opin. Insect Sci., 26 (2018), 149–154. doi: 10.1016/j.cois.2018.02.017
    [15] F. Sánchez-Bayo, D. Goulson, F. Pennacchio, F. Nazzi, K. Goka, N. Desneux, Are bee diseases linked to pesticides? A brief review, Environ. Int., 89 (2016), 7–11.
    [16] E. D. Pilling, P. C. Jepson, Synergism between ebi fungicides and a pyrethroid insecticide in the honeybee (apis mellifera), Pestic. Sci., 9 (1993), 293–297.
    [17] J. S. Pettis, E. M. Lichtenberg, M. Andree, J. Stitzinger, R. Rose, D. vanEngelsdorp, Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen nosema ceranae, PloS One, 8 (2013), e70182. doi: 10.1371/journal.pone.0070182
    [18] A. Fisher II, G. DeGrandi-Hoffman, B. H. Smith, M. Johnson, O. Kaftanoglu, T. Cogley, et al., Colony field test reveals dramatically higher toxicity of a widely-used mito-toxic fungicide on honey bees (apis mellifera), Environ. Pollut., 269 (2021), 115964. doi: 10.1016/j.envpol.2020.115964
    [19] G. DeGrandi-Hoffman, S. A. Roth, G. Loper, E. Erickson Jr, Beepop: a honeybee population dynamics simulation model, Ecol. Modell., 45 (1989), 133–150. doi: 10.1016/0304-3800(89)90088-4
    [20] M. A. Becher, J. L. Osborne, P. Thorbek, P. J. Kennedy, V. Grimm, Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models, J. Appl. Ecol., 50 (2013), 868–880. doi: 10.1111/1365-2664.12112
    [21] D. S. Khoury, M. R. Myerscough, A. B. Barron, A quantitative model of honey bee colony population dynamics, PloS One, 6 (2011), e18491. doi: 10.1371/journal.pone.0018491
    [22] J. Chen, K. Messan, M. R. Messan, G. DeGrandi-Hoffman, D. Bai, Y. Kang, How to model honeybee population dynamics: stage structure and seasonality, Math. Appl. Sci. Eng., 1 (2020), 91–125.
    [23] B. Dennis, W. P. Kemp, How hives collapse: allee effects, ecological resilience, and the honey bee, PloS One, 11 (2016), e0150055. doi: 10.1371/journal.pone.0150055
    [24] K. Vetharaniam, N. D. Barlow, Modelling biocontrol of Varroa destructor using a benign haplotype as a competitive antagonist, N. Z. J. Ecol., 30 (2006), 87–102.
    [25] S. J. Martin, Ontogenesis of the mite varroa jacobsoni oud. in worker brood of the honeybee Apis mellifera L. under natural conditions, Exp. Appl. Acarol., 18 (1994), 87–100. doi: 10.1007/BF00055033
    [26] S. Martin, A population model for the ectoparasitic mite varroa jacobsoni in honey bee (Apis mellifera) colonies, Ecol. Modell., 109 (1998), 267–281. doi: 10.1016/S0304-3800(98)00059-3
    [27] D. Wilkinson, G. C. Smith, A model of the mite parasite, varroa destructor, on honeybees (Apis mellifera) to investigate parameters important to mite population growth, Ecol. Modell., 148 (2002), 263–275. doi: 10.1016/S0304-3800(01)00440-9
    [28] G. DeGrandi-Hoffman, R. Curry, A mathematical model of varroa mite (varroa destructor anderson and trueman) and honeybee (Apis mellifera L.) population dynamics, Int. J. Acarol., 30 (2004), 259–274. doi: 10.1080/01647950408684393
    [29] K. Messan, M. Rodriguez Messan, J. Chen, G. DeGrandi-Hoffman, Y. Kang, Population dynamics of varroa mite and honeybee: effects of parasitism with age structure and seasonality, Ecol. Modell., 440 (2021), 109359. doi: 10.1016/j.ecolmodel.2020.109359
    [30] D. S. Khoury, A. B. Barron, M. R. Myerscough, Modelling food and population dynamics in honey bee colonies, PloS One, 8 (2013), e59084. doi: 10.1371/journal.pone.0059084
    [31] C. M. Kribs-Zaleta, C. Mitchell, Modeling colony collapse disorder in honeybees as a contagion. Math. Biosci. Eng., 11 (2014), 1275–1294. doi: 10.3934/mbe.2014.11.1275
    [32] C. J. Perry, E. Søvik, M. R. Myerscough, A. B. Barron, Rapid behavioral maturation accelerates failure of stressed honey bee colonies, Proc. Natl. Acad. Sci., 112 (2015), 3427–3432. doi: 10.1073/pnas.1422089112
    [33] M. A. Becher, V. Grimm, P. Thorbek, J. Horn, P. J. Kennedy, J. L. Osborne, Beehave: a systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure, J. Appl. Ecol., 51 (2014), 470–482. doi: 10.1111/1365-2664.12222
    [34] M. Becher, V. Grimm, J. Knapp, J. Horn, G. Twiston-Davies, J. Osborne, Beescout: A model of bee scouting behaviour and a software tool for characterizing nectar/pollen landscapes for beehave, Ecol. Modell., 340 (2016), 126–133. doi: 10.1016/j.ecolmodel.2016.09.013
    [35] S. Allan, K. Slessor, M. Winston, G. King, The influence of age and task specialization on the production and perception of honey bee pheromones, J. Insect Physiol., 33, (1987), 917–922. doi: 10.1016/0022-1910(87)90003-5
    [36] R. E. Page, C. Y. Peng, Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp. Gerontol., 36 (2001), 695–711. doi: 10.1016/S0531-5565(00)00236-9
    [37] M. L. Winston, The Biology of the Honey Bee, Harvard University Press, 1991.
    [38] S. J. Martin, The role of varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach, J. Appl. Ecol., 38 (2001), 1082–1093. doi: 10.1046/j.1365-2664.2001.00662.x
    [39] J. D. Evans, M. Spivak, Socialized medicine: individual and communal disease barriers in honey bees, J. Invertebr. Pathol., 103 (2010), S62–S72. doi: 10.1016/j.jip.2009.06.019
    [40] Y. Kang, K. Blanco, T. Davis, Y. Wang, G. DeGrandi-Hoffman, Disease dynamics of honeybees with varroa destructor as parasite and virus vector, Math. Biosci., 275 (2016), 71–92. doi: 10.1016/j.mbs.2016.02.012
    [41] Y. Kang, R. Clark, M. Makiyama, J. Fewell, Mathematical modeling on obligate mutualism: Interactions between leaf-cutter ants and their fungus garden, J. Theor. Biol., 289 (2011), 116–127. doi: 10.1016/j.jtbi.2011.08.027
    [42] L. A. Real, The kinetics of functional response, Am. Nat., 111 (1977), 289–300. doi: 10.1086/283161
    [43] H. J. Eberl, M. R. Frederick, P. G. Kevan, Importance of brood maintenance terms in simple models of the honeybee-varroa destructor-acute bee paralysis virus complex, Electron. J. Differ. Equations, 19 (2010), 85–98.
    [44] V. Ratti, P. G. Kevan, H. J. Eberl, A mathematical model for population dynamics in honeybee colonies infested with varroa destructor and the acute bee paralysis virus, Can. Appl. Math. Q., 21 (2012), 63–93.
    [45] V. Ratti, P. G. Kevan, H. J. Eberl, A mathematical model of the honeybee-varroa destructor-acute bee paralysis virus system with seasonal effects, Bull. Math. Biol., 77 (2015), 1493–1520. doi: 10.1007/s11538-015-0093-5
    [46] V. Ratti, P. G. Kevan, H. J. Eberl, A discrete-continuous modeling framework to study the role of swarming in a honeybee-varroa destrutor-virus system, in Mathematical and Computational Approaches in Advancing Modern Science and Engineering, Springer, (2016), 299–308.
    [47] V. Ratti, P. G. Kevan, H. J. Eberl, A mathematical model of forager loss in honeybee colonies infested with varroa destructor and the acute bee paralysis virus, Bull. Math. Biol., 79 (2017), 1218–1253. doi: 10.1007/s11538-017-0281-6
    [48] K. Messan, G. DeGrandi-Hoffman, C. Castillo-Chavez, Y. Kang, Migration effects on population dynamics of the honeybee-mite interactions, Math. Modell. Nat. Phenom., 12 (2017), 84–115. doi: 10.1051/mmnp/201712206
    [49] B. F. Sweeney, Mathematical modeling of honeybee population dynamics, 2019.
    [50] M. R. Messan, R. E. Page Jr, Y. Kang, Effects of vitellogenin in age polyethism and population dynamics of honeybees, Ecol. Modell., 388 (2018), 88–107. doi: 10.1016/j.ecolmodel.2018.09.011
    [51] K. Tomioka, A. Matsumoto, The circadian system in insects: cellular, molecular, and functional organization, Adv. Insect Physiol., 56 (2019), 73–115. doi: 10.1016/bs.aiip.2019.01.001
    [52] R. D. Booton, Y. Iwasa, J. A. Marshall, D. Z. Childs, Stress-mediated allee effects can cause the sudden collapse of honey bee colonies, J. Theor. Biol., 420 (2017), 213–219. doi: 10.1016/j.jtbi.2017.03.009
    [53] T. D. Seeley, Adaptive significance of the age polyethism schedule in honeybee colonies, Behav. Ecol. Sociobiol., 11 (1982), 287–293. doi: 10.1007/BF00299306
    [54] I. Karsai, T. Schmickl, Regulation of task partitioning by a "common stomach" : a model of nest construction in social wasps, Behav. Ecol., 22 (2011), 819–830. doi: 10.1093/beheco/arr060
    [55] T. Schmickl, I. Karsai, How regulation based on a common stomach leads to economic optimization of honeybee foraging, J. Theor. Biol., 389 (2016), 274–286. doi: 10.1016/j.jtbi.2015.10.036
    [56] T. Schmickl, K. Istvan, Resilience of honeybee colonies via common stomach: a model of self-regulation of foraging, PloS One, 12 (2017), e0188004. doi: 10.1371/journal.pone.0188004
    [57] R. Brodschneider, K. Crailsheim, Nutrition and health in honey bees, Apidologie, 41 (2010), 278–294. doi: 10.1051/apido/2010012
    [58] A. L. Hughes, Life-history evolution at the molecular level: adaptive amino acid composition of avian vitellogenins, Proc. R. Soc. B., 282 (2015), 20151105. doi: 10.1098/rspb.2015.1105
    [59] G. V. Amdam, O. Rueppell, M. K. Fondrk, R. E. Page, C. M. Nelson, The nurse's load: early-life exposure to brood-rearing affects behavior and lifespan in honey bees (Apis mellifera), Exp. Gerontol, 44 (2009), 467–471. doi: 10.1016/j.exger.2009.02.013
    [60] G. V. Amdam, S. W. Omholt, The regulatory anatomy of honeybee lifespan, J. Theor. Biol., 216 (2002), 209–228. doi: 10.1006/jtbi.2002.2545
    [61] U. Glavinic, B. Stankovic, V. Draskovic, J. Stevanovic, T. Petrovic, N. Lakic, et al., Dietary amino acid and vitamin complex protects honey bee from immunosuppression caused by nosema ceranae, PLoS One, 12 (2017), e0187726. doi: 10.1371/journal.pone.0187726
    [62] T. Schmickl, K. Crailsheim, Hopomo: A model of honeybee intracolonial population dynamics and resource management, Ecol. Modell., 204 (2007), 219–245. doi: 10.1016/j.ecolmodel.2007.01.001
    [63] G. V. Amdam, S. W. Omholt, The hive bee to forager transition in honeybee colonies: the double repressor hypothesis, J. Theor. Biol., 223 (2003), 451–464. doi: 10.1016/S0022-5193(03)00121-8
    [64] K. R. Guidugli, A. M. Nascimento, G. V. Amdam, A. R. Barchuk, S. Omholt, Z. L. Simões, et al., Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect, FEBS Lett., 579 (2005), 4961–4965. doi: 10.1016/j.febslet.2005.07.085
    [65] G. Amdam, K. Ihle, R. Page, Regulation of honeybee worker (Apis mellifera) life histories by vitellogenin, in Hormones, Brain and Behavior, (2009), 1003–1027.
    [66] B. R. Johnson, Limited flexibility in the temporal caste system of the honey bee, Behav. Ecol. Sociobiol., 58 (2005), 219–226. doi: 10.1007/s00265-005-0949-z
    [67] J. Oettler, A. L. Nachtigal, L. Schrader, Expression of the foraging gene is associated with age polyethism, not task preference, in the ant cardiocondyla obscurior, PLoS One, 10 (2015), e0144699. doi: 10.1371/journal.pone.0144699
    [68] M. Goblirsch, Z. Y. Huang, M. Spivak, Physiological and behavioral changes in honey bees (Apis mellifera) induced by nosema ceranae infection, PLoS One, 8 (2013), e58165. doi: 10.1371/journal.pone.0058165
    [69] L. R. BenVau, J. C. Nieh, Larval honey bees infected with nosema ceranae have increased vitellogenin titers as young adults, Sci. Rep., 7 (2017), 1–8. doi: 10.1038/s41598-016-0028-x
    [70] S. Cremer, S. A. Armitage, P. Schmid-Hempel, Social immunity, Curr. Biol., 17 (2007), R693–R702. doi: 10.1016/j.cub.2007.06.008
    [71] T. Laomettachit, M. Liangruksa, T. Termsaithong, A. Tangthanawatsakul, O. Duangphakdee, A model of infection in honeybee colonies with social immunity, PloS One, 16 (2021), e0247294. doi: 10.1371/journal.pone.0247294
    [72] D. R. Tarpy, T. D. Seeley, Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens, Naturwiss., 93 (2006), 195–199. doi: 10.1007/s00114-006-0091-4
    [73] D. Sammataro, U. Gerson, G. Needham, Parasitic mites of honey bees: life history, implications, and impact, Annu. Rev. Entomol., 45 (2000), 519–548. doi: 10.1146/annurev.ento.45.1.519
    [74] M. Shen, L. Cui, N. Ostiguy, D. L. Cox-Foster, 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., 86 (2005), 2281–2289. doi: 10.1099/vir.0.80824-0
    [75] S. J. Martin, The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach, J. Appl. Ecol., 38 (2001), 1082–1093. doi: 10.1046/j.1365-2664.2001.00662.x
    [76] D. vanEngelsdorp, M. D. Meixner, A historical review of managed honey bee populations in europe and the united states and the factors that may affect them, J. Invertebr. Pathol., 103 (2010), S80–S95. doi: 10.1016/j.jip.2009.06.011
    [77] I. Fries, Nosema apis—a parasite in the honey bee colony, Bee World, 74 (1993), 5–19. doi: 10.1080/0005772X.1993.11099149
    [78] M. Higes, R. Martín, A. Meana, Nosema ceranae, a new microsporidian parasite in honeybees in europe, J. Invertebr. Pathol., 92 (2006), 93–95. doi: 10.1016/j.jip.2006.02.005
    [79] Y. S. Peng, Y. Fang, S. Xu, L. Ge, The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans, J. Invertebr. Pathol., 49 (1987), 54–60. doi: 10.1016/0022-2011(87)90125-X
    [80] S. D. Ramsey, R. Ochoa, G. Bauchan, C. Gulbronson, J. D. Mowery, A. Cohen, et al., Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph, Proc. Natl. Acad. Sci., 116 (2019), 1792–1801. doi: 10.1073/pnas.1818371116
    [81] G. Tantillo, M. Bottaro, A. Di Pinto, V. Martella, P. Di Pinto, V. Terio, Virus infections of honeybees Apis mellifera, Ital. J. Food Saf., 4 (2015), 5364.
    [82] G. DeGrandi-Hoffman, Y. Chen, Nutrition, immunity and viral infections in honey bees, Curr. Opin. Insect Sci., 10 (2015), 170–176. doi: 10.1016/j.cois.2015.05.007
    [83] J. Carrillo-Tripp, B. C. Bonning, W. A. Miller, Challenges associated with research on rna viruses of insects, Curr. Opin. Insect Sci., 8 (2015), 62–68. doi: 10.1016/j.cois.2014.11.002
    [84] J. R. De Miranda, E. Genersch, Deformed wing virus, J. Invertebr. Pathol., 103 (2010), S48–S61. doi: 10.1016/j.jip.2009.06.012
    [85] G. DeGrandi-Hoffman, V. Corby-Harris, Y. Chen, H. Graham, M. Chambers, E. W. DeJong, et al., Can supplementary pollen feeding reduce varroa mite and virus levels and improve honey bee colony survival? Exp. Appl. Acarol., 82 (2020), 455–473. doi: 10.1007/s10493-020-00562-7
    [86] F. Mondet, J. R. de Miranda, A. Kretzschmar, Y. Le Conte, A. R. Mercer, On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite varroa destructor, PLoS Pathog., 10 (2014), e1004323. doi: 10.1371/journal.ppat.1004323
    [87] E. Genersch, W. Von Der Ohe, H. Kaatz, A. Schroeder, C. Otten, R. Büchler, et al., The german bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies, Apidologie, 41 (2010), 332–352. doi: 10.1051/apido/2010014
    [88] M. Betti, L. Wahl, M. Zamir, Age structure is critical to the population dynamics and survival of honeybee colonies, R. Soc. Open Sci., 3 (2016), 160444. doi: 10.1098/rsos.160444
    [89] M. I. Betti, L. M. Wahl, M. Zamir, Effects of infection on honey bee population dynamics: a model, PloS One, 9 (2014), e110237. doi: 10.1371/journal.pone.0110237
    [90] Y. P. Chen, R. Siede, Honey bee viruses, Adv. Virus Res., 70 (2007), 33–80.
    [91] P. A. Moore, M. E. Wilson, J. A. Skinner, Honey bee viruses, the deadly varroa mite associates, Bee Health, 19 (2015), 2015.
    [92] D. J. Sumpter, S. J. Martin, The dynamics of virus epidemics in varroa-infested honey bee colonies, J. Anim. Ecol., 73 (2004), 51–63. doi: 10.1111/j.1365-2656.2004.00776.x
    [93] A. Dénes, M. A. Ibrahim, Global dynamics of a mathematical model for a honeybee colony infested by virus-carrying varroa mites, J. Appl. Math. Comput., 61 (2019), 349–371. doi: 10.1007/s12190-019-01250-5
    [94] B. Dainat, J. D. Evans, Y. P. Chen, L. Gauthier, P. Neumann, Dead or alive: deformed wing virus and varroa destructor reduce the life span of winter honeybees, Appl. Environ. Microbiol., 78 (2012), 981–987. doi: 10.1128/AEM.06537-11
    [95] H. Hansen, C. J. Brødsgaard, American foulbrood: a review of its biology, diagnosis and control, Bee World, 80 (1999), 5–23. doi: 10.1080/0005772X.1999.11099415
    [96] S. J. Martin, A. C. Highfield, L. Brettell, E. M. Villalobos, G. E. Budge, M. Powell, et al., Global honey bee viral landscape altered by a parasitic mite, Science, 336 (2012), 1304–1306. doi: 10.1126/science.1220941
    [97] J. Devillers, In Silico Bees, CRC Press, 2014.
    [98] M. Henry, M. Beguin, F. Requier, O. Rollin, J. F. Odoux, P. Aupinel, et al., A common pesticide decreases foraging success and survival in honey bees, Science, 336 (2012), 348–350. doi: 10.1126/science.1215039
    [99] N. F. Britton, K. J. White, The effect of covert and overt infections on disease dynamics in honey-bee colonies, Bull. Math. Biol., 83 (2021), 1–23.
    [100] S. Datta, J. C. Bull, G. E. Budge, M. J. Keeling, Modelling the spread of american foulbrood in honeybees, J. R. Soc. Interface, 10 (2013), 20130650. doi: 10.1098/rsif.2013.0650
    [101] E. O. Jatulan, J. F. Rabajante, C. G. B. Banaay, A. C. Fajardo Jr, E. C. Jose, A mathematical model of intra-colony spread of american foulbrood in european honeybees (Apis mellifera L.), PLoS One, 10 (2017), e0143805.
    [102] Y. Chen, J. D. Evans, I. B. Smith, J. S. Pettis, Nosema ceranae is a long-present and wide-spread microsporidian infection of the european honey bee (Apis mellifera) in the united states, J. Invertebr. Pathol., 97 (2008), 186–188. doi: 10.1016/j.jip.2007.07.010
    [103] L. Bailey, Honey bee pathology, Annu. Rev. Entomol., 13 (1968), 191–212. doi: 10.1146/annurev.en.13.010168.001203
    [104] M. Goblirsch, Nosema ceranae disease of the honey bee (Apis mellifera), Apidologie, 49 (2018), 131–150. doi: 10.1007/s13592-017-0535-1
    [105] S. L. Gage, C. Kramer, S. Calle, M. Carroll, M. Heien, G. DeGrandi-Hoffman, Nosema ceranae parasitism impacts olfactory learning and memory and neurochemistry in honey bees (apis mellifera), J. Exp. Biol., 221 (2018).
    [106] W. F. Huang, L. F. Solter, Comparative development and tissue tropism of nosema apis and nosema ceranae, J. Invertebr. Pathol., 113 (2013), 35–41. doi: 10.1016/j.jip.2013.01.001
    [107] A. Petric, E. Guzman-Novoa, H. J. Eberl, A mathematical model for the interplay of nosema infection and forager losses in honey bee colonies, J. Biol. Dyn., (2016), 1–31.
    [108] N. Muhammad, H. J. Eberl, Two routes of transmission for nosema infections in a honeybee population model with polyethism and time-periodic parameters can lead to drastically different qualitative model behavior, Commun. Nonlinear Sci. Numer. Simul., 84 (2020), 105207. doi: 10.1016/j.cnsns.2020.105207
    [109] M. E. Natsopoulou, D. P. McMahon, V. Doublet, J. Bryden, R. J. Paxton, Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease, Proc. R. Soc. B, 282 (2015), 20141896. doi: 10.1098/rspb.2014.1896
    [110] J. R. Comper, H. J. Eberl, Mathematical modelling of population and food storage dynamics in a honey bee colony infected with nosema ceranae, Heliyon, 6 (2020), e04599. doi: 10.1016/j.heliyon.2020.e04599
    [111] C. A. Mullin, M. Frazier, J. L. Frazier, S. Ashcraft, R. Simonds, J. S. Pettis, et al., High levels of miticides and agrochemicals in north american apiaries: implications for honey bee health, PloS One, 5 (2010), e9754. doi: 10.1371/journal.pone.0009754
    [112] P. Magal, G. Webb, Y. Wu, An environmental model of honey bee colony collapse due to pesticide contamination, Bull. Math. Biol., 81 (2019), 4908–4931. doi: 10.1007/s11538-019-00662-5
    [113] P. Magal, G. F. Webb, Y. Wu, A spatial model of honey bee colony collapse due to pesticide contamination of foraging bees, J. Math. Biol., 80 (2020), 2363–2393. doi: 10.1007/s00285-020-01498-7
    [114] J. C. Rumkee, M. A. Becher, P. Thorbek, P. J. Kennedy, J. L. Osborne, Predicting honeybee colony failure: using the beehave model to simulate colony responses to pesticides, Environ. Sci. Technol., 49 (2015), 12 879–12 887. doi: 10.1021/acs.est.5b03593
    [115] O. Rueppell, R. Linford, P. Gardner, J. Coleman, K. Fine, Aging and demographic plasticity in response to experimental age structures in honeybees (Apis mellifera L.), Behav. Ecol. Sociobiol., 62 (2008), 1621–1631. doi: 10.1007/s00265-008-0591-7
    [116] D. De Jong, P. H. De Jong, Longevity of africanized honey bees (hymenoptera: Apidae) infested by varroa jacobsoni (parasitiformes: Varroidae), J. Econ. Entomol., 76 (1983), 766–768. doi: 10.1093/jee/76.4.766
    [117] H. Kovac, K. Crailsheim, Lifespan of apis mellifera carnica pollm. infested by varroa jacobsoni oud. in relation to season and extent of infestation, J. Apic. Res., 27 (1988), 230–238. doi: 10.1080/00218839.1988.11100808
    [118] G. DeGrandi-Hoffman, F. Ahumada, V. Zazueta, M. Chambers, G. Hidalgo, E. W. Dejong, Population growth of varroa destructor (acari: Varroidae) in honey bee colonies is affected by the number of foragers with mites, Exp. Appl. Acarol., 69 (2016), 21–34. doi: 10.1007/s10493-016-0022-9
    [119] G. DeGrandi-Hoffman, F. Ahumada, H. Graham, Are dispersal mechanisms changing the host-parasite relationship and increasing the virulence of varroa destructor (mesostigmata: Varroidae) in managed honey bee (hymenoptera: Apidae) colonies? Environ. Entomol., 46 (2017), 737–746. doi: 10.1093/ee/nvx077
    [120] A. C. Kuan, G. DeGrandi-Hoffman, R. J. Curry, K. V. Garber, A. R. Kanarek, M. N. Snyder, et al., Sensitivity analyses for simulating pesticide impacts on honey bee colonies, Ecol. Modell, 376 (2018), 15–27. doi: 10.1016/j.ecolmodel.2018.02.008
    [121] F. Abi-Akar, A. Schmolke, C. Roy, N. Galic, S. Hinarejos, Simulating honey bee large-scale colony feeding studies using the beehave model? Part ii: analysis of overwintering outcomes, Environ. Toxicol. Chem., 39 (2020), 2286–2297. doi: 10.1002/etc.4844
    [122] M. Switanek, K. Crailsheim, H. Truhetz, R. Brodschneider, Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate, Sci. Total Environ., 579 (2017), 1581–1587. doi: 10.1016/j.scitotenv.2016.11.178
    [123] P. Thorbek, P. J. Campbell, P. J. Sweeney, H. M. Thompson, Using beehave to explore pesticide protection goals for european honeybee (Apis melifera L.) worker losses at different forage qualities, Environ. Toxicol. Chem., 36 (2017), 254–264. doi: 10.1002/etc.3504
    [124] M. A. Becher, G. Twiston-Davies, T. D. Penny, D. Goulson, E. L. Rotheray, J. L. Osborne, Bumble-beehave: a systems model for exploring multifactorial causes of bumblebee decline at individual, colony, population and community level, J. Appl. Ecol., 55 (2018), 2790–2801. doi: 10.1111/1365-2664.13165
    [125] M. Calovi, C. M. Grozinger, D. A. Miller, S. C. Goslee, Summer weather conditions influence winter survival of honey bees (Apis mellifera) in the northeastern united states, Sci. Rep., 11 (2021), 1–12. doi: 10.1038/s41598-020-79139-8
    [126] B. Dainat, P. Neumann, Clinical signs of deformed wing virus infection are predictive markers for honey bee colony losses, J. Invertebr. Pathol., 112 (2013), 278–280. doi: 10.1016/j.jip.2012.12.009
    [127] J. D. Evans, C. Saegerman, C. Mullin, E. Haubruge, B. K. Nguyen, M. Frazier, et al., Colony collapse disorder: a descriptive study, PloS One, 4 (2009), e6481. doi: 10.1371/journal.pone.0006481
    [128] G. DeGrandi-Hoffman, F. Ahumada, R. Curry, G. Probasco, L. Schantz, Population growth of varroa destructor (acari: Varroidae) in commercial honey bee colonies treated with beta plant acids, Exp. Appl. Acarol., 64 (2014), 171–186. doi: 10.1007/s10493-014-9821-z
    [129] J. L. Harris, A population model and its application to the study of honey bee colonies, IRE Trans. Circuit Theory, 2 (1980), 44–49.
    [130] C. A. Halsch, A. M. Shapiro, J. A. Fordyce, C. C. Nice, J. H. Thorne, D. P. Waetjen, et al., Insects and recent climate change, Proc. Natl. Acad. Sci., 118 (2021), e2002543117. doi: 10.1073/pnas.2002543117
    [131] F. Bodenheimer, Studies in animal populations. ii. seasonal population-trends of the honey-bee, Q. Rev. Biol., 12 (1937), 406–425. doi: 10.1086/394540
    [132] B. Castellanos-Potenciano, F. Gallardo-López, G. Diaz-Padilla, A. Pérez-Vázquez, C. Landeros-Sánchez, et al., Spatio-temporal mobility of apiculture affected by the climate change in the beekeeping of the gulf of Mexico, Appl. Ecol. Environ. Res., 15 (2017), 163–175.
    [133] Y. Le Conte, M. Navajas, Climate change: impact on honey bee populations and diseases, Rev. Sci. Tech., 27 (2008), 499–510.
    [134] M. K. Crone, C. M. Grozinger, Pollen protein and lipid content influence resilience to insecticides in honey bees (apis mellifera), J. Exp. Biol., 224 (2021), jeb242040. doi: 10.1242/jeb.242040
    [135] A. C. Velásquez, C. D. M. Castroverde, S. Y. He, Plant-pathogen warfare under changing climate conditions, Curr. Biol., 28 (2018), R619–R634. doi: 10.1016/j.cub.2018.03.054
    [136] P. D. Noyes, M. K. McElwee, H. D. Miller, B. W. Clark, L. A. Van Tiem, K. C. Walcott, et al., The toxicology of climate change: environmental contaminants in a warming world, Environ. Int., 35 (2009), 971–986, 2009. doi: 10.1016/j.envint.2009.02.006
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