Abstract
Diet has a significant effect on pathogen infections in animals and the consumption of secondary metabolites can either enhance or mitigate infection intensity. Secondary metabolites, which are commonly associated with herbivore defense, are also frequently found in floral nectar. One hypothesized function of this so-called toxic nectar is that it has antimicrobial properties, which may benefit insect pollinators by reducing the intensity of pathogen infections. We tested whether gelsemine, a nectar alkaloid of the bee-pollinated plant Gelsemium sempervirens, could reduce pathogen loads in bumble bees infected with the gut protozoan Crithidia bombi. In our first laboratory experiment, artificially infected bees consumed a daily diet of gelsemine post-infection to simulate continuous ingestion of alkaloid-rich nectar. In the second experiment, bees were inoculated with C. bombi cells that were pre-exposed to gelsemine, simulating the direct effects of nectar alkaloids on pathogen cells that are transmitted at flowers. Gelsemine significantly reduced the fecal intensity of C. bombi 7 days after infection when it was consumed continuously by infected bees, whereas direct exposure of the pathogen to gelsemine showed a non-significant trend toward reduced infection. Lighter pathogen loads may relieve bees from the behavioral impairments associated with the infection, thereby improving their foraging efficiency. If the collection of nectar secondary metabolites by pollinators is done as a means of self-medication, pollinators may selectively maintain secondary metabolites in the nectar of plants in natural populations.
Similar content being viewed by others
References
Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420
Adler LS, Irwin RE (2005) Ecological costs and benefits of defenses in nectar. Ecology 86:2968–2978
Berenbaum MR (1988) Allelochemicals in insect–microbe–plant interactions; agents provocateurs in the coevolutionary arms race. Wiley, New York
Bernays EA, Singer MS (2005) Taste alteration and endoparasites. Nature 436:476
Blau PA, Feeny P, Contardo L, Robson DS (1978) Allylglucosinolate and herbivorous caterpillars—contrast in toxicity and tolerance. Science 200:1296–1298
Blaw ME, Adkisson MA, Levin D, Garriott JC, Tindall RSA (1979) Poisoning with Carolina jessamine (Gelsemium sempervirens [L.] Ait). J Pediatr 94:998–1001
Boppre M, Colegate SM, Edgar JA (2005) Pyrrolizidine alkaloids of Echium vulgare honey found in pure pollen. J Agric Food Chem 53:594–600
Brown MJF, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–427
Brown MJF, Schmid-Hempel R, Schmid-Hempel P (2003) Strong context-dependent virulence in a host–parasite system: reconciling genetic evidence with theory. J Anim Ecol 72:994–1002
Brysch-Herzberg M (2004) Ecology of yeasts in plant-bumblebee mutualism in Central Europe. FEMS Microbiol Ecol 50:87–100
Chapuisat M, Oppliger A, Magliano P, Christe P (2007) Wood ants use resin to protect themselves against pathogens. Proc R Soc Lond B Biol Sci 274:2013–2017
Christe P, Oppliger A, Bancala F, Castella G, Chapuisat M (2003) Evidence for collective medication in ants. Ecol Lett 6:19–22
Clayton DH, Wolfe ND (1993) The adaptive significance of self-medication. Trends Ecol Evol 8:60–63
Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461–467
Cory JS, Hoover K (2006) Plant-mediated effects in insect–pathogen interactions. Trends Ecol Evol 21:278–286
Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582
Despres L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307
Durrer S, Schmid-Hempel P (1994) Shared use of flowers leads to horizontal pathogen transmission. Proc R Soc Lond B Biol Sci 258:299–302
Ehlers BK, Olesen JM (1997) The fruit-wasp route to toxic nectar in Epipactis orchids? Flora 192:223–229
Elliott SE, Irwin RE, Adler LS, Williams NM (2008) The nectar alkaloid, gelsemine, does not affect offspring performance of a native solitary bee, Osmia lignaria (Megachilidae). Ecol Entomol 33:298–304
Freiburghaus F, Kaminsky R, Nkunya MHH, Brun R (1996) Evaluation of African medicinal plants for their in vitro trypanocidal activity. J Ethnopharmacol 55:1–11
Gegear RJ, Otterstatter MC, Thomson JD (2005) Does parasitic infection impair the ability of bumblebees to learn flower-handling techniques? Anim Behav 70:209–215
Gegear RJ, Otterstatter MC, Thomson JD (2006) Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc R Soc Lond B Biol Sci 273:1073–1078
Gegear RJ, Manson JS, Thomson JD (2007) Ecological context influences pollinator deterrence by alkaloids in floral nectar. Ecol Lett 10:375–382
Golonka AM (2002) Nectar-inhabiting microorganisms and the dioecious plant species Silene latifolia. Department of Botany. Duke University, Durham, p 150
Imhoof B, Schmid-Hempel P (1999) Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insect Soc 46:233–238
Irwin RE, Adler LS, Brody AK (2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85:1503–1511
Isman MB, Duffey SS (1982) Toxicity of tomato phenolic compounds to the fruitworm, Heliothis zea. Entomol Exp Appl 31:370–376
Karban R, English-Loeb G (1997) Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78:603–611
Konig B (1988) The honeybee as pharmacophorus insect. Entomol Gen 14:145–148
Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Soc Lond B Biol Sci 273:823–829
Lipa JJ, Triggiani O (1988) Crithidia bombi sp n. a flagellated parasite of a bumblebee Bombus terrestris L. (Hymenoptera, Apidae). Acta Protozool 27:287–290
Logan A, Ruiz-Gonzalez MX, Brown MJF (2005) The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees. Parasitology 130:637–642
Manson JS, Thomson JD (2009) Post-ingestive effects of nectar alkaloids depend on dominance status of bumble bees. Ecol Entomol 34:421–426
Manson JS, Lachance MA, Thomson JD (2007) Candida gelsemii sp. nov., a yeast of the Metschnikowiaceae clade isolated from nectar of the poisonous Carolina jessamine. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 92:37–42
Marcucci MC (1995) Propolis—chemical composition, biological properties and therapeutic activity. Apidologie 26:83–99
Otterstatter MC, Thomson JD (2006) Within-host dynamics of an intestinal pathogen of bumble bees. Parasitology 133:749–761
Otterstatter MC, Thomson JD (2007) Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 154:411–421
Otterstatter MC, Gegear RJ, Colla SR, Thomson JD (2005) Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behav Ecol Sociobiol 58:383–389
Pascarella JB (2007) Mechanisms of prezygotic reproductive isolation between two sympatric species, Gelsemium rankinii and G. sempervirens (Gelsemiaceae), in the southeastern United States. Am J Bot 94:468–476
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among 3 trophic levels—influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65
Rhoades DF, Bergdahl JC (1981) Adaptive significance of toxic nectar. Am Nat 117:798–803
SAS Institute (2006) SAS/STAT 9.1 user’s guide. SAS Institute, Cary
Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton
Schmid-Hempel P (2001) On the evolutionary ecology of host–parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158
Schmid-Hempel R, Schmid-Hempel P (1991) Endoparasitic flies, pollen-collection by bumblebees and a potential host–parasite conflict. Oecologia 87:227–232
Schmid-Hempel P, Schmid-Hempel R (1993) Transmission of a pathogen in Bombus terrestris, with a note on division-of-labor in social insects. Behav Ecol Sociobiol 33:319–327
Schmid-Hempel P, Stauffer HP (1998) Parasites and flower choice of bumblebees. Anim Behav 55:819–825
Singer MS, Carriere Y, Theuring C, Hartmann T (2004) Disentangling food quality from resistance against parasitoids: diet choice by a generalist caterpillar. Am Nat 164:423–429
Singer MS, Mace KC, Bernays EA (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS One 4:e4796
Slansky F (1992) Allelochemical–nutrient interactions in herbivore nutrient ecology, vol. II. Ecological and evolutionary processes. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites, vol 2, 2nd edn. Academic Press, San Diego, pp 135–176
Stiles B, Paschke JD (1980) Midgut pH in different instars of 3 Aedes mosquito species and the relation between pH and susceptibility of larvae to a nuclear polyhedrosis virus. J Invertebr Pathol 35:58–64
Strauss SY, Whittall JB (2006) Non-pollinator agents of selection on floral traits. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 120–138
Tadmor-Melamed H, Markman S, Arieli A, Distl M, Wink M, Izhaki I (2004) Limited ability of Palestine sunbirds Nectarinia osea to cope with pyridine alkaloids in nectar of tree tobacco Nicotiana glauca. Funct Ecol 18:844–850
Vanetten H, Temporini E, Wasmann C (2001) Phytoalexin (and phytoanticipin) tolerance as a virulence trait: why is it not required by all pathogens? Physiol Mol Plant Pathol 59:83–93
Wink M, Theile V (2002) Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecology 12:29–46
Acknowledgements
We would like to thank Nathan Muchhala and Mario Vallejo-Marín, Richard Karban and two anonymous reviewers for comments on the manuscript. This study was supported by grants from the Natural Sciences and Engineering Research Council. All experiments complied with the current laws of Canada.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Richard Karban.
J. S. Manson and M. C. Otterstatter have contributed equally.
Rights and permissions
About this article
Cite this article
Manson, J.S., Otterstatter, M.C. & Thomson, J.D. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162, 81–89 (2010). https://doi.org/10.1007/s00442-009-1431-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-009-1431-9