Skip to main content
SpringerLink
Log in

Herbivory and Time Since Flowering Shape Floral Rewards and Pollinator-Pathogen Interactions

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Herbivory can induce chemical changes throughout plant tissues including flowers, which could affect pollinator-pathogen interactions. Pollen is highly defended compared to nectar, but no study has examined whether herbivory affects pollen chemistry. We assessed the effects of leaf herbivory on nectar and pollen alkaloids in Nicotiana tabacum, and how herbivory-induced changes in nectar and pollen affect pollinator-pathogen interactions. We damaged leaves of Nicotiana tabacum using the specialist herbivore Manduca sexta and compared nicotine and anabasine concentrations in nectar and pollen. We then pooled nectar and pollen by collection periods (within and after one month of flowering), fed them in separate experiments to bumble bees (Bombus impatiens) infected with the gut pathogen Crithidia bombi, and assessed infections after seven days. We did not detect alkaloids in nectar, and leaf damage did not alter the effect of nectar on Crithidia counts. In pollen, herbivory induced higher concentrations of anabasine but not nicotine, and alkaloid concentrations rose and then fell as a function of days since flowering. Bees fed pollen from damaged plants had Crithidia counts 15 times higher than bees fed pollen from undamaged plants, but only when pollen was collected after one month of flowering, indicating that both damage and time since flowering affected interaction outcomes. Within undamaged treatments, bees fed late-collected pollen had Crithidia counts 10 times lower than bees fed early-collected pollen, also indicating the importance of time since flowering. Our results emphasize the role of herbivores in shaping pollen chemistry, with consequences for interactions between pollinators and their pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420

    Google Scholar 

  • Adler LS, Wink M, Distl M, Lentz AJ (2006) Leaf herbivory and nutrients increase nectar alkaloids. Ecol Lett 9:960–967

    PubMed  Google Scholar 

  • Adler LS, Seifert MG, Wink M, Morse GE (2012) Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol Lett 15:1140–1148

    PubMed  Google Scholar 

  • Anthony WE, Palmer-Young EC, Leonard AS, Irwin RE, Adler LS (2015) Testing dose-dependent effects of the nectar alkaloid anabasine on trypanosome parasite loads in adult bumble bees. PLoS One 10:e0142496

    PubMed  PubMed Central  Google Scholar 

  • Arnold SEJ, Peralta Idrovo ME, Lomas Arias LJ, Belmain SR, Stevenson PC (2014) Herbivore defence compounds occur in pollen and reduce bumblebee colony fitness. J Chem Ecol 40:878–881

    PubMed  CAS  Google Scholar 

  • Baracchi D, Brown MJF, Chittka L (2015) Behavioural evidence for self-medication in bumblebees? F1000 Research 4:73

    PubMed  Google Scholar 

  • Barber NA, Adler LS, Bernardo HL (2011) Effects of above- and belowground herbivory on growth, pollination, and reproduction in cucumber. Oecologia 165:377–386

    PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using {lme4}. J Stat Softw 67:1–48

    Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    PubMed  Google Scholar 

  • Brown M, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–427

    Google Scholar 

  • Bruinsma M, Lucas-Barbosa D, ten Broeke CJM, van Dam NM, van Beek TA, Dicke M, van Loon JJA (2014) Folivory affects composition of nectar, floral odor and modifies pollinator behavior. J Chem Ecol 40:39–49

    PubMed  CAS  Google Scholar 

  • Chauta A, Whitehead S, Amaya-Marquez M, Poveda K (2017) Leaf herbivory imposes fitness costs mediated by hummingbird and insect pollinators. PLoS One 12:e0188408

    PubMed  PubMed Central  Google Scholar 

  • Cook D, Manson JS, Gardner DR, Welch KD, Irwin RE (2013) Norditerpene alkaloid concentrations in tissues and floral rewards of larkspurs and impacts on pollinators. Biochem Syst Ecol 48:123–131

    CAS  Google Scholar 

  • Davis JK, Aguirre LA, Barber NA, Stevenson PC, Adler LS (2019) From plant fungi to bee parasites: Mycorrhizae and soil nutrients shape floral chemistry and bee pathogens. Ecology:e02801

  • Detzel A, Wink M (1993) Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:8–18

    CAS  Google Scholar 

  • du Rand EE, Smit S, Beukes M, Apostolides Z, Pirk CWW, Nicolson SW (2015) Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Sci Rep 5:11779

    PubMed  PubMed Central  Google Scholar 

  • Durrer S, Schmid-Hempel P (1994) Shared use of flowers leads to horizontal pathogen transmission. Proc R Soc Lond B 258:299–302

    Google Scholar 

  • 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 273:1073–1078

    Google Scholar 

  • Halpern SL, Adler LS, Wink M (2010) Leaf herbivory and drought stress affect floral attractive and defensive traits in Nicotiana quadrivalvis. Oecologia 163:961–971

    PubMed  Google Scholar 

  • Harvey JA, van Dam NM, Gols R (2003) Interactions over four trophic levels: Foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72:520–531

    Google Scholar 

  • Heinrich B (1979) Bumblebee economics. Harvard University Press, Cambridge

    Google Scholar 

  • Hoffmeister M, Wittkoepper N, Junker RR (2016) Herbivore-induced changes in flower scent and morphology affect the structure of flower-visitor networks but not plant reproduction. Oikos 125:1241–1249

    Google Scholar 

  • Irwin RE, Cook D, Richardson LL, Manson JS, Gardner DR (2014) Secondary compounds in floral rewards of toxic rangeland plants: Impacts on pollinators. J Agric Food Chem 62:7335–7344

    PubMed  CAS  Google Scholar 

  • Jacobsen DJ, Raguso RA (2018) Lingering effects of herbivory and plant defenses on pollinators. Curr Biol 28:R1164–R1169

    PubMed  CAS  Google Scholar 

  • Jørgensen B (1992) Exponential dispersion models and extensions: A review. Int Stat Rev 60:5–20

    Google Scholar 

  • Kaczorowski RL, Gardener MC, Holtsford TP (2005) Nectar traits in Nicotiana section Alatae (Solanaceae) in relation to floral traits, pollinators, and mating system. Am J Bot 92:1270–1283

    PubMed  Google Scholar 

  • Kaczorowski RL, Koplovich A, Sporer F, Wink M, Markman S (2014) Immediate effects of nectar robbing by Palestine sunbirds (Nectarinia osea) on nectar alkaloid concentrations in tree tobacco (Nicotiana glauca). J Chem Ecol 40:325–330

    PubMed  CAS  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406

    PubMed  Google Scholar 

  • Kessler A, Halitschke R (2009) Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: Predictions and case study. Funct Ecol 23:901–912

    Google Scholar 

  • Koch H, Woodward J, Langat MK, Brown MJF, Stevenson PC (2019) Flagellum removal by a nectar metabolite inhibits infectivity of a bumblebee parasite. Curr Biol 29:3494–3500.e5

    PubMed  CAS  Google Scholar 

  • Krupnick GA, Weis AE, Campbell DR (1999) The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80:125–134

    Google Scholar 

  • Lehtilä K, Strauss SY (1999) Effects of foliar herbivory on male and female reproductive traits of wild radish, Raphanus raphanistrum. Ecology 80:116–124

    Google Scholar 

  • Lenth R (2019) Emmeans: estimated marginal means, aka least-squares means. R package version 1(4):1

    Google Scholar 

  • Lucas-Barbosa D (2016) Integrating studies on plant-pollinator and plant-herbivore interactions. Trends Plant Sci 21:125–133

    PubMed  CAS  Google Scholar 

  • Lüdecke D (2018) Ggeffects: tidy data frames of marginal effects from regression models. R package version 0.12.0

  • Manson JS, Otterstatter MC, Thomson JD (2010) Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162:81–89

    PubMed  Google Scholar 

  • Manson JS, Rasmann S, Halitschke R, Thomson JD, Agrawal AA (2012) Cardenolides in nectar may be more than a consequence of allocation to other plant parts: A phylogenetic study of Asclepias. Funct Ecol 26:1100–1110

    Google Scholar 

  • Mao W, Schuler MA, Berenbaum MR (2013) Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. Proc Natl Acad Sci U S A 110:8842–8846

    PubMed  PubMed Central  CAS  Google Scholar 

  • McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320

    Google Scholar 

  • Merrill GB (1916) Report of the tobacco insect investigations. In: 4th report board commissioners Porto Rico, from 1st July 1914 to 30th June 1915. San Juan, pp 50-52

  • Moreira X, Castagneyrol B, Abdala-Roberts L, Traveset A (2019) A meta-analysis of herbivore effects on plant attractiveness to pollinators. Ecology 100:UNSP e02707

  • Muth F, Francis JS, Leonard AS (2016) Bees use the taste of pollen to determine which flowers to visit. Biol Lett 12:20160356

    PubMed  PubMed Central  Google Scholar 

  • Nooten SS, Rehan SM (2020) Historical changes in bumble bee body size and range shift of declining species. Biodivers Conserv 29:451–467

    Google Scholar 

  • Ohnmeiss TE, Baldwin IT (2000) Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology 81:1765–1783

    Google Scholar 

  • Palmer-Young EC, Sadd BM, Stevenson PC, Irwin RE, Adler LS (2016) Bumble bee parasite strains vary in resistance to phytochemicals. Sci Rep 6:37087

    PubMed  PubMed Central  CAS  Google Scholar 

  • Palmer-Young EC, Hogeboom A, Kaye AJ, Donnelly D, Andicoechea J, Connon SJ, Weston I, Skyrm K, Irwin RE, Adler LS (2017) Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees. PLoS One 12:e0183729

    PubMed  PubMed Central  Google Scholar 

  • Palmer-Young EC, Farrell IW, Adler LS, Milano NJ, Egan PA, Junker RR, Irwin RE, Stevenson PC (2019) Chemistry of floral rewards: Intra-and interspecific variability of nectar and pollen secondary metabolites across taxa. Ecol Monogr 89:e01335

    Google Scholar 

  • Parachnowitsch AL, Manson JS (2015) The chemical ecology of plant-pollinator interactions: Recent advances and future directions. Curr Opin Insect Sci 8:41–46

    PubMed  Google Scholar 

  • Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2003) Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135:601–605

    PubMed  Google Scholar 

  • Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2005) Effects of decomposers and herbivores on plant performance and aboveground plant-insect interactions. Oikos 108:503–510

    Google Scholar 

  • Quintero C, Bowers MD (2018) Plant and herbivore ontogeny interact to shape the preference, performance and chemical defense of a specialist herbivore. Oecologia 187:401–412

    PubMed  Google Scholar 

  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Richardson LL, Adler LS, Leonard AS, Andicoechea J, Regan KH, Anthony WE, Manson JS, Irwin RE (2015) Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proc R Soc Lond B 282:20142471

    Google Scholar 

  • Rivest S, Forrest JRK (2020) Defence compounds in pollen: Why do they occur and how do they affect the ecology and evolution of bees? New Phytol 225:1053–1064

    PubMed  Google Scholar 

  • Roger N, Michez D, Wattiez R, Sheridan C, Vanderplanck M (2017) Diet effects on bumblebee health. J Insect Physiol 96:128–133

    PubMed  CAS  Google Scholar 

  • Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209

    CAS  Google Scholar 

  • Ruedenauer FA, Spaethe J, Leonhardt SD (2016) Hungry for quality-individual bumblebees forage flexibly to collect high-quality pollen. Behav Ecol Sociobiol 70:1209–1217

    Google Scholar 

  • Rusman Q, Lucas-Barbosa D, Poelman EH (2018) Dealing with mutualists and antagonists: Specificity of plant-mediated interactions between herbivores and flower visitors, and consequences for plant fitness. Funct Ecol 32:1022–1035

    Google Scholar 

  • Rusman Q, Lucas-Barbosa D, Poelman EH, Dicke M (2019) Ecology of plastic flowers. Trends Plant Sci 24:725–740

    PubMed  CAS  Google Scholar 

  • Shykoff JA, Schmid-Hempel P (1991) Incidence and effects of 4 parasites in natural-populations of bumble bees in Switzerland. Apidologie 22:117–125

    Google Scholar 

  • Silva FA, Guirgis A, Thornburg R (2018) Nectar analysis throughout the genus Nicotiana suggests conserved mechanisms of nectar production and biochemical action. Front Plant Sci 9:1100

    PubMed  PubMed Central  Google Scholar 

  • Soler R, Bezemer TM, der Putten V, Wim H, Vet LEM, Harvey JA (2005) Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J Anim Ecol 74:1121–1130

    Google Scholar 

  • Solt ML, Dawson RF, Christman DR (1960) Biosynthesis of anabasine and of nicotine by excised root cultures of Nicotiana glauca. Plant Physiol 35:887–894

    PubMed  PubMed Central  CAS  Google Scholar 

  • Stevenson PC (2019) For antagonists and mutualists: The paradox of insect toxic secondary metabolites in nectar and pollen. Phytochem Rev

  • Stevenson PC, Nicolson SW, Wright GA (2017) Plant secondary metabolites in nectar: Impacts on pollinators and ecological functions. Funct Ecol 31:65–75

    Google Scholar 

  • Thorburn LP, Adler LS, Irwin RE, Palmer-Young EC (2015) Variable effects of nicotine, anabasine, and their interactions on parasitized bumble bees. F1000 Research 4:880

    PubMed  Google Scholar 

  • Thornburg RW, Carter C, Powell A, Mittler R, Rizhsky L, Horner HT (2003) A major function of the tobacco floral nectary is defense against microbial attack. Plant Syst Evol 238:211–218

    Google Scholar 

  • Tiedeken EJ, Egan PA, Stevenson PC, Wright GA, Brown MJF, Power EF, Farrell I, Matthews SM, Stout JC (2016) Nectar chemistry modulates the impact of an invasive plant on native pollinators. Funct Ecol 30:885–893

    Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. R package version 3(2):1

    Google Scholar 

  • Zangerl AR, Rutledge CE (1996) The probability of attack and patterns of constitutive and induced defense: A test of optimal defense theory. Am Nat 147:599–608

    Google Scholar 

  • Zhang Y (2013) Likelihood-based and bayesian methods for tweedie compound poisson linear mixed models. R package version 0.7–8

Download references

Acknowledgements

We thank E. Stone, E. Amponsah, B. Joyce, R. Pasquale, G. Cox, L. Cleary and E. Palmer-Young for help with data collection and thoughtful feedback, the UMass Amherst Quantitative Statistics Group for feedback on statistical analyses, Biobest (Ontario, Canada) for donating bumble bee colonies, and J. van Wyk, R. Malfi, M. Hanusch and three anonymous reviewers for providing constructive comments on the manuscript. This work was funded by the PGAV Destinations Pollinator Research grant, the IMSD/NEAGEP First-Year Pre-Doctoral Fellowship (NIH 25 GM099649), the Lotta M. Crabtree Fellowship, the National Science Foundation Graduate Research Fellowship (NSF 1451512; 1938059), and the National Science Foundation and Austrian Science Fund GROW Program (NSF 1938059; FWF GRW 7-B) to LAA, the Torrey Plant Biology Fellowship to JKD and NIH 1 R01 GM1220 62-01 to LSA.

Author information

Authors and Affiliations

  1. Department of Biology, University of Massachusetts, Amherst, MA, 01003, USA

    Luis A. Aguirre & Lynn S. Adler

  2. Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA, 01003, USA

    Luis A. Aguirre

  3. Department of Entomology, Cornell University, Ithaca, NY, 14850, USA

    Julie K. Davis

  4. Jodrell Laboratory, Royal Botanic Gardens, Kew, Surrey, TW9 3AB, UK

    Philip C. Stevenson

  5. Natural Resources Institute, University of Greenwich, Chatham, Kent, ME4 4TB, UK

    Philip C. Stevenson

Authors
  1. Luis A. Aguirre
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julie K. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philip C. Stevenson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lynn S. Adler
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The study design was devised by LAA and LSA. LAA and JKD carried out the experiments. PCS undertook the chemical analysis. LAA conducted the statistical analyses and wrote the manuscript. All authors contributed critically to the manuscript and approved the final manuscript.

Corresponding author

Correspondence to Luis A. Aguirre.

Electronic supplementary material

ESM 1

(DOCX 19166 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aguirre, L.A., Davis, J.K., Stevenson, P.C. et al. Herbivory and Time Since Flowering Shape Floral Rewards and Pollinator-Pathogen Interactions. J Chem Ecol 46, 978–986 (2020). https://doi.org/10.1007/s10886-020-01213-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-020-01213-2

Keywords

Search

Navigation