Light, allelopathy, and post-mortem invasive impact on native forest understory species

Biological Invasions volume 16, pages1131–1144(2014)Cite this article

Abstract

Extended leaf phenology (early budbreak and/or delayed leaf drop) and allelopathy are potentially key invasion mechanisms in North American deciduous forests. Because extended phenology confers increased access to light energy and allelochemical production is energetically costly, these traits may interact synergistically to determine invader impact. Garlic mustard (Alliaria petiolata) exhibits both traits, and may also exploit high light in open habitats. We manipulated seasonal light availability to examine effects of light on garlic mustard’s growth, allelochemical production, and impact on native species. Invaded and not-invaded woodland microcosms were exposed to three light treatments: shading year-round (‘extended shade’), shading when the local tree canopy was closed (‘natural shade’), and ambient light year-round (‘no-shade’). Regardless of native presence, garlic mustard biomass was highest under natural shade and, due to apparent irradiation damage, lowest under no-shade. Similarly, growth and fruit production of garlic mustard monocultures were reduced in unshaded conditions. Consistent with these results, garlic mustard reduced the growth of native woodland forbs Blephilia hirsuta and Ageratina altissima most under natural shade, suggesting that extended leaf phenology mediates impact on these herbaceous species. However, garlic mustard growth did not predict reduction of whole-community biomass: invasion reduced native community growth most under no-shade, where invader biomass was lowest but allelochemical production was highest. This result may be driven by a ‘post-mortem’ pulse of allelochemicals from decaying garlic mustard tissue. We conclude that extended leaf phenology may mediate garlic mustard’s impact on some native species, and that light and allelopathy may interact to drive invasion.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Anderson RC, Dhillion SS, Kelley TM (1996) Aspects of the ecology of an invasive plant, garlic mustard (Alliaria petiolata), in central Illinois. Restor Ecol 4(2):181–191. doi:10.1111/j.1526-100X.1996.tb00118.x

    Article  Google Scholar 

  2. Anderson RC, Anderson R, Bauer JT, Slater M, Herold J, Baumhardt P, Borowicz V (2010) Effect of removal of garlic mustard (Alliaria petiolata, Brassicaeae) on arbuscular mycorrhizal fungi inoculum potential in forest soils. Open Ecol J 3:41–47. doi:10.2174/1874213001003010041

    Google Scholar 

  3. Barto EK, Antunes PM, Stinson K, Koch AM, Klironomos JN, Cipollini D (2011) Differences in arbuscular mycorrhizal fungal communities associated with sugar maple seedlings in and outside of invaded garlic mustard forest patches. Biol Invasions 13(12):2755–2762. doi:10.1007/s10530-011-9945-6

    Article  Google Scholar 

  4. Burke DJ (2008) Effects of Alliaria petiolata (garlic mustard; Brassicaceae) on mycorrhizal colonization and community structure in three herbaceous plants in a mixed deciduous forest. Am J Bot 95(11):1416–1425. doi:10.3732/ajb.0800184

    PubMed  Article  Google Scholar 

  5. Burns RM, Honkala BH (1990) Silvics of North America, vol 2, Hardwoods. USDA Forest Serv. Agric. Handbook 654, Washington, DC, 877 p

  6. Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89(4):1043–1055

    PubMed  Article  Google Scholar 

  7. Castellano SM, Gorchov DL (2012) Reduced ectomycorrhizae on oak near invasive garlic mustard. Northeast Nat 19(1):1–24

    Article  Google Scholar 

  8. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15(1):22–40. doi:10.1111/J.1472-4642.2008.00521.X

    Article  Google Scholar 

  9. Cavers PB, Heagy MI, Kokron RF (1979) Biology of Canadian weeds. 35. Alliaria petiolata (M. Bieb) Cavara and Grande. Can J Plant Sci 59(1):217–229

    Article  Google Scholar 

  10. Cipollini K, Titus K, Wagner C (2012) Allelopathic effects of invasive species (Alliaria petiolata, Lonicera maackii, Ranunculus ficaria) in the Midwestern United States. Allelopath J 29(1):63–75

    Google Scholar 

  11. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88(3):528–534

    Article  Google Scholar 

  12. Engelhardt MJ, Anderson RC (2011) Phenological niche separation of an invasive species Alliaria petiolata. J Torrey Bot Soc 138(4):418–433

    Article  Google Scholar 

  13. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485(7398):359–362

    PubMed  Article  CAS  Google Scholar 

  14. Gurevitch J, Fox GA, Wardle GM, Inderjit, Taub D (2011) Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol Lett 14(4):407–418. doi:10.1111/j.1461-0248.2011.01594.x

    PubMed  Article  CAS  Google Scholar 

  15. Harrington RA, Brown BJ, Reich PB (1989) Ecophysiology of exotic and native shrubs in southern Wisconsin. 1. Relationship of leaf characteristics, resource availability, and phenology to seasonal patterns of carbon gain. Oecologia 80(3):356–367. doi:10.1007/bf00379037

    Article  Google Scholar 

  16. Klionsky SM, Amatangelo KL, Waller DM (2011) Above- and belowground impacts of European buckthorn (Rhamnus cathartica) on four native forbs. Restor Ecol 19(6):728–737. doi:10.1111/j.1526-100X.2010.00727.x

    Article  Google Scholar 

  17. Lankau R (2008) A chemical trait creates a genetic trade-off between intra- and interspecific competitive ability. Ecology 89(5):1181–1187. doi:10.1890/07-1541.1

    PubMed  Article  Google Scholar 

  18. Lankau R (2010) Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol Invasions 12(7):2059–2068. doi:10.1007/S10530-009-9608-Z

    Article  Google Scholar 

  19. Lankau RA (2012) Interpopulation variation in allelopathic traits informs restoration of invaded landscapes. Evol Appl 5(3):270–282. doi:10.1111/j.1752-4571.2011.00218.x

    PubMed Central  Article  Google Scholar 

  20. Lankau RA, Nuzzo V, Spyreas G, Davis AS (2009) Evolutionary limits ameliorate the negative impact of an invasive plant. Proc Natl Acad Sci USA 106(36):15362–15367. doi:10.1073/Pnas.0905446106

    PubMed Central  PubMed  Article  Google Scholar 

  21. MacDougall AS, Gilbert B, Levine JM (2009) Plant invasions and the niche. J Ecol 97(4):609–615. doi:10.1111/j.1365-2745.2009.01514.x

    Article  Google Scholar 

  22. McEwan RW, Birchfield MK, Schoergendorfer A, Arthur MA (2009) Leaf phenology and freeze tolerance of the invasive shrub Amur honeysuckle and potential native competitors. J Torrey Bot Soc 136(2):212–220

    Article  Google Scholar 

  23. Meekins JF, McCarthy BC (2000) Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability. J Ecol 88(3):447–463

    Article  Google Scholar 

  24. Meekins JF, McCarthy BC (2001) Effect of environmental variation on the invasive success of a nonindigenous forest herb. Ecol Appl 11(5):1336–1348. doi:10.2307/3060924

    Article  Google Scholar 

  25. Moles AT, Flores-Moreno H, Bonser SP, Warton DI, Helm A, Warman L, Eldridge DJ, Jurado E, Hemmings FA, Reich PB, Cavender-Bares J, Seabloom EW, Mayfield MM, Sheil D, Djietror JC, Peri PL, Enrico L, Cabido MR, Setterfield SA, Lehmann CER, Thomson FJ (2012) Invasions: the trail behind, the path ahead, and a test of a disturbing idea. J Ecol 100(1):116–127. doi:10.1111/j.1365-2745.2011.01915.x

    Article  Google Scholar 

  26. Muller C (2009) The role of glucosinolates in plant invasiveness. Phytochem Rev 8(1):227–242. doi:10.1007/S11101-008-9115-3

    Article  CAS  Google Scholar 

  27. Myers CV, Anderson RC (2003) Seasonal variation in photosynthetic rates influences success of an invasive plant, garlic mustard (Alliaria petiolata). Am Midl Nat 150(2):231–245. doi:10.1674/0003-0031(2003)150[0231:svipri]2.0.co;2

    Article  Google Scholar 

  28. Myers CV, Anderson RC, Byers DL (2005) Influence of shading on the growth and leaf photosynthesis of the invasive non-indigenous plant garlic mustard [Alliaria petiolata (M. Bieb) Cavara and Grande] grown under simulated late-winter to mid-spring conditions. J Torrey Bot Soc 132(1):1–10

    Article  Google Scholar 

  29. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team TRC (2009) nlme: linear and nonlinear mixed effects models. R Package version 3.1-96 edn.

  30. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  31. Roberts KJ, Anderson RC (2001) Effect of garlic mustard Alliaria petiolata (Beib. Cavara & Grande) extracts on plants and arbuscular mycorrhizal (AM) fungi. Am Midl Nat 146(1):146–152. doi:10.1674/0003-0031(2001)146[0146:eogmap]2.0.co;2

    Article  Google Scholar 

  32. Rodgers VL, Stinson KA, Finzi AC (2008) Ready or not, garlic mustard is moving in: Alliaria petiolata as a member of eastern North American forests. Bioscience 58(5):426–436. doi:10.1641/B580510

    Article  Google Scholar 

  33. Schreiner RP, Koide RT (1993) Mustards, mustard oils and mycorrhizas. New Phytol 123(1):107–113

    Article  CAS  Google Scholar 

  34. Small CJ, McCarthy BC (2002) Effects of simulated post-harvest light availability and soil compaction on deciduous forest herbs. Can J For Res 32(10):1753–1762. doi:10.1139/x02-099

    Article  Google Scholar 

  35. Smith LM (2013) Extended leaf phenology in deciduous forest invaders: mechanisms of impact on native communities. J Veg Sci. doi:10.1111/jvs.12087

    Google Scholar 

  36. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4(5):727–731. doi:10.1371/journal.pbio.0040140

    Article  CAS  Google Scholar 

  37. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17(6):278–285. doi:10.1016/s0169-5347(02)02483-7

    Article  Google Scholar 

  38. Tholen JT, Shifeng S, Truscott RJW (1989) The thymol method for glucosinolate determination. J Sci Food Agric 49(2):157–165

    Article  CAS  Google Scholar 

  39. Vaughn SF, Berhow MA (1999) Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). J Chem Ecol 25(11):2495–2504. doi:10.1023/a:1020874124645

    Article  CAS  Google Scholar 

  40. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2009) gplots: various R programming tools for plotting data. R package version 2.7.3.

  41. Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J Ecol 96(4):777–783. doi:10.1111/j.1365-2745.2008.01389.x

    Article  Google Scholar 

  42. Xu CY, Griffin KL, Schuster WSF (2007) Leaf phenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154(1):11–21. doi:10.1007/s00442-007-0807-y

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

This project was supported by the Indiana University Department of Biology and by a grant from the Indiana Academy of Sciences. Thanks to Stephanie Dickinson of the Indiana Statistical Consulting Center for assistance with statistical analysis. Thanks to Therese Burkhard and Gerald Smith for assistance with field work, and to the Indiana University Greenhouse staff for watering plants throughout the duration of the experiment.

Author information

Affiliations

  1. Indiana University, 1001 E Third Street, Bloomington, IN, 47405, USA

    Lauren M. Smith & Heather L. Reynolds

Authors
  1. Lauren M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heather L. Reynolds
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lauren M. Smith.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Smith, L.M., Reynolds, H.L. Light, allelopathy, and post-mortem invasive impact on native forest understory species. Biol Invasions 16, 1131–1144 (2014). https://doi.org/10.1007/s10530-013-0567-z

Download citation

Keywords

  • Species invasion
  • Garlic mustard
  • Leaf phenology
  • Allelopathy
  • Gap dynamics