Microbial Ecology

, Volume 76, Issue 2, pp 482–491 | Cite as

Honey Bee (Apis mellifera) Pollen Foraging Reflects Benefits Dependent on Individual Infection Status

  • Jade A. Ferguson
  • Tobin D. Northfield
  • Lori LachEmail author
Invertebrate Microbiology


Parasites often modify host foraging behavior, for example, by spurring changes to nutrient intake ratios or triggering self-medication. The gut parasite, Nosema ceranae, increases energy needs of the European or Western honey bee (Apis mellifera), but little is known about how infection affects foraging behavior. We used a combination of experiments and observations of caged and free-flying individual bees and hives to determine how N. ceranae affects honey bee foraging behavior. In an experiment with caged bees, we found that infected bees with access to a high-quality pollen were more likely to survive than infected bees with access to a lower quality pollen or no pollen. Non-infected bees showed no difference in survival with pollen quality. We then tested free-flying bees in an arena of artificial flowers and found that pollen foraging bees chose pollen commensurate with their infection status; twice as many infected bees selected the higher quality pollen than the lower quality pollen, while healthy bees showed no preference between pollen types. However, healthy and infected bees visited sucrose and pollen flowers in the same proportions. Among hive-level observations, we found no significant correlations between N. ceranae infection intensity in the hive and the proportion of bees returning with pollen. Our results indicate that N. ceranae-infected bees benefit from increased pollen quality and will selectively forage for higher quality while foraging for pollen, but infection status does not lead to increased pollen foraging at either the individual or hive levels.


Apis mellifera Parasites Nosema ceranae Pollen preference Foraging behavior Hive 



We thank Roy Swenson and Maurice Damon for allowing us to work in their apiaries and sharing their beekeeping knowledge. We thank Georgia Kelly and Sarah Mannel for laboratory assistance and Phillip Adams for assistance in constructing hoarding cages. We are grateful to Dr. Rob Manning for sharing unpublished data on amino acid content of the pollens.


This study was funded by an Australian Research Council Discovery Early Career Research Award (DE130100709) to LL and James Cook University Honours student support to JF.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1147_MOESM1_ESM.docx (22 kb)
ESM 1 (DOCX 22 kb)


  1. 1.
    Martin LB, Scheuerlein A, Wikelski M (2003) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc Lond Ser B Biol Sci 270:153CrossRefGoogle Scholar
  2. 2.
    Booth DT, Clayton DH, Block BA (1993) Experimental demonstration of the energetic cost of parasitism in free-ranging hosts. Proc R Soc Lond Ser B Biol Sci 253:125CrossRefGoogle Scholar
  3. 3.
    Shikano I, Cory JS (2016) Altered nutrient intake by baculovirus-challenged insects: self-medication or compensatory feeding? J Invertebr Pathol 139:25–33. CrossRefPubMedGoogle Scholar
  4. 4.
    Stafford-Banks CA, Yang LH, McMunn MS, Ullman DE (2014) Virus infection alters the predatory behavior of an omnivorous vector. Oikos 123:1384–1390. CrossRefGoogle Scholar
  5. 5.
    Jakobsen PJ, Wedekind C (1998) Copepod reaction to odor stimuli influenced by cestode infection. Behav Ecol 9:414–418. CrossRefGoogle Scholar
  6. 6.
    Naug D, Gibbs A (2009) Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 40:595–599. CrossRefGoogle Scholar
  7. 7.
    Lefevre T, Adamo SA, Biron DG, Misse D, Hughes D, Thomas F (2009) Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host-parasite Interactions. In: Webster JP (ed.) Advances in Parasitology. Natural History of Host-Parasite Interactions 68:45–83Google Scholar
  8. 8.
    Thompson SN, Redak RA (2008) Parasitism of an insect Manduca sexta L. alters feeding behaviour and nutrient utilization to influence developmental success of a parasitoid. J Comp Physiol B-Biochem Syst Environ Physiol 178:515–527. CrossRefGoogle Scholar
  9. 9.
    Graham RI, Deacutis JM, Pulpitel T, Ponton F, Simpson SJ, Wilson K (2014) Locusts increase carbohydrate consumption to protect against a fungal biopesticide. J Insect Physiol 69:27–34. CrossRefPubMedGoogle Scholar
  10. 10.
    Abbott J (2014) Self-medication in insects: current evidence and future perspectives. Ecol Entomol 39:273–280. CrossRefGoogle Scholar
  11. 11.
    Povey S, Cotter SC, Simpson SJ, Lee KP, Wilson K (2009) Can the protein costs of bacterial resistance be offset by altered feeding behaviour? J Anim Ecol 78:437–446. CrossRefPubMedGoogle Scholar
  12. 12.
    Povey S, Cotter SC, Simpson SJ, Wilson K (2014) Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects. J Anim Ecol 83:245–255. CrossRefPubMedGoogle Scholar
  13. 13.
    Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc Royal Soc B-Biol Sci 273:823–829. CrossRefGoogle Scholar
  14. 14.
    Huffman MA, Caton JM (2001) Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees. Int J Primatol 22:329–346. CrossRefGoogle Scholar
  15. 15.
    Lefevre T, Roche B, Poulin R, Hurd H, Renaud F, Thomas F (2008) Exploiting host compensatory responses: the ‘must’ of manipulation? Trends Parasitol 24:435–439. CrossRefPubMedGoogle Scholar
  16. 16.
    Karban R, English-Loeb G (1997) Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78:603–611.<0603,TPAHPC>2.0.CO;2
  17. 17.
    Vale PF, Choisy M, Little TJ (2013) Host nutrition alters the variance in parasite transmission potential. Biol Lett 9:20121145. CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Carlsson-Graner U, Thrall PH (2006) The impact of host longevity on disease transmission: host-pathogen dynamics and the evolution of resistance. Evol Ecol Res 8:659–675Google Scholar
  19. 19.
    Poulin R, Maure F (2015) Host manipulation by parasites: a look back before moving forward. Trends Parasitol 31:563–570. CrossRefPubMedGoogle Scholar
  20. 20.
    Thomas F, Rigaud T, Brodeur J (2012) Evolutionary routes leading to host manipulation by parasites. In: Hughes DP, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford University Press, Oxford, pp 16–35CrossRefGoogle Scholar
  21. 21.
    Calderone NW (2012) Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992–2009. Plos One 7(5):e37235.
  22. 22.
    Campbell J, Kessler B, Mayack C, Naug D (2010) Behavioural fever in infected honeybees: parasitic manipulation or coincidental benefit? Parasitology 137:1487–1491. CrossRefPubMedGoogle Scholar
  23. 23.
    Evans JD, Schwarz RS (2011) Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 19:614–620. CrossRefPubMedGoogle Scholar
  24. 24.
    Higes M, Martin-Hernandez R, Botias C, Bailon EG, Gonzalez-Porto AV, Barrios L, del Nozal MJ, Bernal JL, Jimenez JJ, Palencia PG, Meana A (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10:2659–2669. CrossRefPubMedGoogle Scholar
  25. 25.
    Mayack C, Naug D (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100:185–188. CrossRefPubMedGoogle Scholar
  26. 26.
    Eiri DM, Suwannapong G, Endler M, Nieh JC (2015) Nosema ceranae can infect honey bee larvae and reduces subsequent adult longevity. PLoS One 10:e0126330. CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Fries I, Feng F, daSilva A, Slemenda SB, Pieniazek NJ (1996) 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 32:356–365CrossRefGoogle Scholar
  28. 28.
    Higes M, Martin R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92:93–95. CrossRefPubMedGoogle Scholar
  29. 29.
    Chen Y, Evans JD, Smith IB, Pettis JS (2008) 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 97:186–188CrossRefPubMedGoogle Scholar
  30. 30.
    Guerrero-Molina C, Correa-Benitez A, Hamiduzzaman MM, Guzman-Novoa E (2016) Nosema ceranae is an old resident of honey bee (Apis mellifera) colonies in Mexico, causing infection levels of one million spores per bee or higher during summer and fall. J Invertebr Pathol 141:38–40. CrossRefPubMedGoogle Scholar
  31. 31.
    Rangel J, Baum K, Rubink WL, Coulson RN, Johnston JS, Traver BE (2016) Prevalence of Nosema species in a feral honey bee population: a 20-year survey. Apidologie 47:561–571. CrossRefGoogle Scholar
  32. 32.
    Smart MD, Sheppard WS (2012) Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). J Invertebr Pathol 109:148–151. CrossRefPubMedGoogle Scholar
  33. 33.
    Martin-Hernandez R, Botias C, Barrios L, Martinez-Salvador A, Meana A, Mayack C, Higes M (2011) Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitol Res 109:605–612. CrossRefPubMedGoogle Scholar
  34. 34.
    Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
  35. 35.
    Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, Suchail S, Brunet JL, Alaux C (2013) Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS ONE 8(8):e72016.
  36. 36.
    Jack CJ, Uppala SS, Lucas HM, Sagili RR (2016) Effects of pollen dilution on infection of Nosema ceranae in honey bees. J Insect Physiol 87:12–19. CrossRefPubMedGoogle Scholar
  37. 37.
    Mulholland GE, Traver BE, Johnson NG, Fell RDF (2012) Individual variability of Nosema ceranae infections in Apis mellifera colonies. Insects 3:1143–1155CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Fries I, Chauzat MP, Chen YP, Doublet V, Genersch E, Gisder S, Higes M, McMahon DP, Martín-Hernández R, Natsopoulou M, Paxton RJ, Tanner G, Webster TC, Williams GR (2013) Standard methods for Nosema research. J Apic Res 52:1–28CrossRefGoogle Scholar
  39. 39.
    Williams GR, Alaux C, Costa C, Csaki T, Doublet V, Eisenhardt D, Fries I, Kuhn R, McMahon DP, Medrzycki P, Murray TE, Natsopoulou ME, Neumann P, Oliver R, Paxton RJ, Pernal SF, Shutler D, Tanner G, van der Steen JJM, Brodschneider R (2013) Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J Apic Res 52(1):1–36.
  40. 40.
    Somerville DC (2012) Pollen trapping and storage. NSW Department of Primary Industries, PUB11/75[v2], 5.
  41. 41.
    Somerville DC (2005) Fat bees, skinny bees: a manual on honey bee nutrition for beekeepers. Rural Industries Research and Development Corporation, RIRDC Publication No 05/054.
  42. 42.
    Manning R, Harvey M (2002) Fatty acids in honeybee-collected pollens from six endemic Western Australian eucalypts and the possible significance to the Western Australian beekeeping industry. Aust J Exp Agric 42:217–223. CrossRefGoogle Scholar
  43. 43.
    Cantwell GE (1970) Standard methods for counting nosema spores. Am Bee J 110:222–223Google Scholar
  44. 44.
    Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. CrossRefPubMedGoogle Scholar
  45. 45.
    Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  46. 46.
    Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10. CrossRefPubMedGoogle Scholar
  47. 47.
    R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL
  48. 48.
    RStudio Team (2016) RStudio: integrated development for R. RStudio, Inc., Boston. URL
  49. 49.
    Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  50. 50.
    Frias BED, Barbosa CD, Lourenco AP (2016) Pollen nutrition in honey bees (Apis mellifera): impact on adult health. Apidologie 47:15–25. CrossRefGoogle Scholar
  51. 51.
    DeGrandi-Hoffman G, Chen YP (2015) Nutrition, immunity and viral infections in honey bees. Curr Opin Insect Sci 10:170–176. CrossRefPubMedGoogle Scholar
  52. 52.
    Wang H, Zhang SW, Zeng ZJ, Yan WY (2014) Nutrition affects longevity and gene expression in honey bee (Apis mellifera) workers. Apidologie 45:618–625. CrossRefGoogle Scholar
  53. 53.
    Mattila HR, Otis GW (2006) Effects of pollen availability and Nosema infection during the spring on division of labor and survival of worker honey bees (Hymenoptera : Apidae). Environ Entomol 35:708–717CrossRefGoogle Scholar
  54. 54.
    DeGrandi-Hoffman G, Chen YP, Rivera R, Carroll M, Chambers M, Hidalgo G, de Jong EW (2016) Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements. Apidologie 47:186–196. CrossRefGoogle Scholar
  55. 55.
    Schmid-Hempel P, Stauffer HP (1998) Parasites and flower choice of bumblebees. Anim Behav 55:819–825. CrossRefPubMedGoogle Scholar
  56. 56.
    Schmid-Hempel P, Schmid-Hempel R (1990) Endoparasitic larvae of conopid flies alter pollination behavior of bumblebees. Naturwissenschaften 77:450–452. CrossRefGoogle Scholar
  57. 57.
    Shykoff JA, Schmid-Hempel P (1991) Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie 22:117–125CrossRefGoogle Scholar
  58. 58.
    Gherman BI, Denner A, Bobis O, Dezmirean DS, Marghitas LA, Schluns H, Moritz RFA, Erler S (2014) Pathogen-associated self-medication behavior in the honeybee Apis mellifera. Behav Ecol Sociobiol 68:1777–1784. CrossRefGoogle Scholar
  59. 59.
    Simone-Finstrom MD, Spivak M (2012) Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS ONE 7(3): e34601.
  60. 60.
    Erler S, Moritz RFA (2016) Pharmacophagy and pharmacophory: mechanisms of self-medication and disease prevention in the honeybee colony (Apis mellifera). Apidologie 47:389–411. CrossRefGoogle Scholar
  61. 61.
    Koch H, Brown MJF, Stevenson PC (2017) The role of disease in bee foraging ecology. Curr Opin Insect Sci 21:60–67. CrossRefPubMedGoogle Scholar
  62. 62.
    Hendriksma HP, Shafir S (2016) Honey bee foragers balance colony nutritional deficiencies. Behav Ecol Sociobiol 70:509–517. CrossRefGoogle Scholar
  63. 63.
    Nicholls E, de Ibarra NH (2017) Assessment of pollen rewards by foraging bees. Funct Ecol 31:76–87. CrossRefGoogle Scholar
  64. 64.
    Schmidt JO, Thoenes SC, Levin MD (1987) Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Ann Entomol Soc Am 80:176–183. CrossRefGoogle Scholar
  65. 65.
    Anderson DL, Giacon H (1992) Reduced pollen collection by honey bee (Hymenoptera: Apidae) colonies infected with Nosema apis and sacbrood virus. J Econ Entomol 85:47–51CrossRefGoogle Scholar
  66. 66.
    Lach L, Kratz M, Baer B (2015) Parasitized honey bees are less likely to forage and carry less pollen. J Invertebr Pathol 130:64–71. CrossRefPubMedGoogle Scholar
  67. 67.
    Milbrath MO, Xie XB, Huang ZY (2013) Nosema ceranae induced mortality in honey bees (Apis mellifera) depends on infection methods. J Invertebr Pathol 114:42–44. CrossRefPubMedGoogle Scholar
  68. 68.
    Kurze C, Mayack C, Hirche F, Stangl GI, Le Conte Y, Kryger P, Moritz RFA (2016) Nosema spp. infections cause no energetic stress in tolerant honeybees. Parasitol Res 115:2381–2388. CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Centre for Tropical Environmental and Sustainability Science, College of Science and EngineeringJames Cook UniversityCairnsAustralia

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