Honey Bee (Apis mellifera) Pollen Foraging Reflects Benefits Dependent on Individual Infection Status
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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.
KeywordsApis 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 Rob Manning for sharing unpublished data on amino acid content of the pollens.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.
- 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
- 16.Karban R, English-Loeb G (1997) Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78:603–611. https://doi.org/10.1890/0012-9658(1997)078<0603,TPAHPC>2.0.CO;2
- 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
- 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. https://doi.org/10.1371/journal.pone.0037235
- 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. https://doi.org/10.1111/j.1462-2920.2008.01687.x CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1016/j.jip.2016.11.001 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1007/s00436-011-2292-9 CrossRefPubMedGoogle Scholar
- 34.Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
- 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. https://doi.org/10.1371/journal.pone.0072016
- 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. https://doi.org/10.3896/ibra.1.52.1.04
- 40.Somerville DC (2012) Pollen trapping and storage. NSW Department of Primary Industries, PUB11/75[v2], 5. https://www.dpi.nsw.gov.au/__data/assets/pdf_file/0003/117516/Pollen-trapping-and-Storage.pdf
- 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. http://www.agrifutures.com.au/publications/fat-bees-skinny-bees-a-manual-on-honey-bee-nutrition-for-beekeepers/
- 43.Cantwell GE (1970) Standard methods for counting nosema spores. Am Bee J 110:222–223Google Scholar
- 47.R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL http://www.R-project.org/
- 48.RStudio Team (2016) RStudio: integrated development for R. RStudio, Inc., Boston. URL http://www.rstudio.com/
- 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. https://doi.org/10.1007/s13592-015-0386-6 CrossRefGoogle Scholar
- 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. https://doi.org/10.1371/journal.pone.0034601