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Effects of Arbuscular Mycorrhizal Fungi on the Exotic Invasive Vine Pale Swallow-Wort (Vincetoxicum rossicum)

Published online by Cambridge University Press:  20 January 2017

Larissa L. Smith
Affiliation:
Department of Crop and Soil Sciences, Cornell University, Ithaca, NY 14853
Antonio DiTommaso*
Affiliation:
Department of Crop and Soil Sciences, Cornell University, Ithaca, NY 14853
Johannes Lehmann
Affiliation:
Department of Crop and Soil Sciences, Cornell University, Ithaca, NY 14853
Sigurdur Greipsson
Affiliation:
Department of Biology and Environmental Sciences, Troy University, Troy, AL 36082
*
Corresponding author's E-mail: ad97@cornell.edu

Abstract

The ability of arbuscular mycorrhizal fungi (AMF) to influence the performance of nonnative invasive plants in their introduced range has received increasing attention. The dependence of the invasive nonnative vine pale swallow-wort on AMF was studied in three greenhouse experiments. The aims of the present work were to (1) determine AMF colonization levels of field-collected pale swallow-wort plants and several co-occurring native and nonnative plant species, (2) evaluate the growth response of pale swallow-wort to different components of the soil microbial community from an infested site, and (3) determine the growth response of pale swallow-wort when grown with a nonlocal AMF species. AMF root colonization was greater in pale swallow-wort (85, 98, and 50% arbuscules, hyphae, and vesicles, respectively) than in leek (72, 80, and 25%), a species that has been frequently used as a predictor of AMF density in soil. Root colonization of pale swallow-wort in the field was also greater than root colonization of common milkweed, a native herbaceous species often co-occurring in the same habitats, as well as two other herbaceous species, Canada goldenrod and blueweed. Survival of pale swallow-wort plants was significantly greater in soil collected underneath dense monospecific stands of pale swallow-wort in a Henderson Harbor, NY, field site than in sterilized soil. After 12 wk, plants grown in sterilized soil had a 33% survival rate, whereas all plants grown in the unamended soil, with an intact microbial community, were alive. Moreover, plants grown in the unamended soil were 130% taller, had 50% more leaves, and had 83% greater total biomass compared with plants grown in sterile soil. Plants grown in soil containing a Glomus intraradices isolate collected in Troy, AL, were 50% shorter and had 15% lower total biomass than plants grown in the unamended New York field soil. These pale swallow-wort seedlings also had a high mycorrhizal dependency of 93%. Plants grown in a sterilized soil that was reamended with an AMF-free microbial wash had significantly lower belowground and total biomass than plants grown in the unamended soil with the resident AMF community. There was a trend of decreasing height and biomass for plants grown in sterile soil relative to the unamended controls treatment. Plants grown in sterilized soil had significantly (28%) greater total biomass than plants reamended with the AMF-free microbial wash. These findings suggest that AMF occurring in invaded habitats have beneficial effects on pale swallow-wort survival and growth.

Type
Research Articles
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Andrade, G., Mihara, K. L., Linderman, R. G., and Bethlenfalvay, G. J. 1998. Soil aggregation status and rhizo-bacteria in the mycorrhizosphere. Plant Soil 202:8996.Google Scholar
Bell, G. 2001. Neutral macroecology. Science 293:24132418.Google Scholar
Blossey, B. and Nötzold, R. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol 83:887889.Google Scholar
Bray, S., Kitajima, K., and Sylvia, D. M. 2003. Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecol. Appl 13:565574.Google Scholar
Brundrett, M. 1991. Mycorrhizas in natural ecosystems. Adv. Ecol. Res 21:171313.CrossRefGoogle Scholar
Brundrett, M., Bougher, N., Dell, B., Grove, T., and Malajczuk, N., editors. 1996. Working with Mycorrhizas in Forestry and Agriculture. Canberra, Australia Australian Centre for International Agricultural Research. 374.Google Scholar
Burleigh, S. H., Cavagnaro, T., and Jakobsen, I. 2002. Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J. Exp. Bot 53:15931601.CrossRefGoogle Scholar
Christensen, T. 1998. Swallow-worts. Wildflower Summer 2125.Google Scholar
Daniels, B. A. and Skipper, H. D. 1982. Methods for the recovery and quantitative estimation of propagules from soil. Pages 2935. in Schenck, N. C., editor. Methods and Principles of Mycorrhizal Research. St. Paul, MN The American Phytopathological Society.Google Scholar
Davis, M. A., Grime, J. P., and Thompson, K. 2000. Fluctuating resources in plant communities: a general theory of invasibility. J. Ecol 88:528534.Google Scholar
DiTommaso, A., Lawlor, F. M., and Darbyshire, S. J. 2005. The biology of invasive alien plants in Canada. 2. Cynanchum rossicum (Kleopow) Borhidi (= Vincetoxicum rossicum (Kleopow) Barbar.) and Cynanchum louiseae (L.) Kartesz & Gandhi) (= Vincetoxicum nigrum (L.) Moench.). Can. J. Plant Sci 85:243263.Google Scholar
Eissenstat, D. and Newman, E. 1990. Seedling establishment near large plants: effects of vesicular–arbuscular mycorrhizas on the intensity of plant competition. Funct. Ecol 4:9599.Google Scholar
Facelli, E., Facelli, J. M., Smith, S. E., and McLaughlin, M. J. 1999. Interactive effects of arbuscular mycorrhizal symbiosis, intraspecific competition and resource availability in Trifolium subterraneum cv. Mt. Barker. New Phytol 141:535547.Google Scholar
Fitter, A. H. 2005. Darkness visible: reflections on underground ecology. J. Ecol 93:231243.Google Scholar
Francis, R. and Read, D. J. 1984. Direct transfer of carbon between plants connected by vesicular–arbuscular mycorrhizal mycelium. Nature 307:5356.Google Scholar
Francis, R. and Read, D. J. 1995. Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to the impact on plant community structure. Can. J. Bot 73:13011309.CrossRefGoogle Scholar
Fumanal, B., Plenchette, C., Chauvel, B., and Bretagnolle, F. 2006. Which role can arbuscular mycorrhizal fungi play in the facilitation of Ambrosia artemisiifolia L. invasion in France. Mycorrhiza 17:2535.Google Scholar
Garbaye, J. 1994. Helper bacteria— a new dimension to the mycorrhizal symbiosis. New Phytol 128:197201.Google Scholar
Goodwin, B. J., McAllister, A. J., and Fahrig, L. 1999. Predicting invasiveness of plant species based on biological information. Conserv. Biol. 13 422426.Google Scholar
Greipsson, S. and DiTommaso, A. 2006. Invasive non-native plants alter the occurrence of arbuscular mycorrhizal fungi and benefit from this association. Ecol. Restor 24:236241.Google Scholar
Hallett, S. G. 2006. Dislocation from coevolved relationships: a unifying theory for plant invasion and naturalization. Weed Sci 54:282290.Google Scholar
Hawkes, C. V., Belnap, J., D'Antonio, D., and Firestone, M. K. 2006. Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant Soil 281:369380.Google Scholar
Heap, A. J. and Newman, E. I. 1980. Links between roots by hyphae of vesicular–arbuscular mycorrhizas. New Phytol 85:169171.Google Scholar
Hierro, J. L., Villarreal, D., Özkan, E., Graham, J. M., and Callaway, R. M. 2005. Disturbance facilitates invasion: the effects are stronger abroad than at home. Am. Nat 168:144156.Google Scholar
Howeler, R. H., Cadavid, L. F., and Burckhardt, E. 1982. Response of cassava to VA mycorrhizal inoculation and phosphorus application in greenhouse and field experiments. Plant Soil 69:327339.Google Scholar
[INVAM] International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi 2005. http://invam.caf.wvu.edu/collection/generalinfo/isol_diversity.htm. Accessed: November 7, 2005.Google Scholar
Jin, L., Gu, Y., Xiaom, M., Chen, J., and Li, B. 2004. The history of Solidago canadensis invasion and the development of its mycorrhizal associations in newly-reclaimed land. Funct. Plant Biol 31:971978.Google Scholar
Johnson-Green, P. C., Kenkel, N. C., and Booth, T. 1995. The distribution and phenology of arbuscular mycorrhizae along an inland salinity gradient. Can. J. Bot 73:13181327.Google Scholar
Klironomos, J. N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:6770.Google Scholar
Ladd, D. and Cappuccino, N. 2005. A field study of seed dispersal and seedling performance in the invasive exotic vine Vincetoxicum rossicum . Can. J. Bot 83:11811188.Google Scholar
Lata, H., De Andrade, Z., Schaneberg, B., Bedir, E., Khan, I., and Moraes, R. 2003. Arbuscular mycorrhizal inoculation enhances survival rates and growth of micropropagated plantlets of Echinacea pallida . Planta Med 69:679682.Google ScholarPubMed
Levine, J. M., Montserra, V., D'Antonio, C. M., Dukes, J. S., Grigulis, K., and Lavorel, S. 2003. Mechanisms underlying the impacts of exotic plant invasions. Proc. R. Soc. Lond. B 270:775781.Google Scholar
Lockwood, J. L., Simberloff, D., McKinney, M. L., and Von Holle, B. 2001. How many, and which plants will invade natural areas. Biol. Invasions 3:18.Google Scholar
Mack, R. N., Simberloff, D., Lonsdale, W. W., Evans, H., Clout, M., and Bazzaz, F. A. 2000. Biotic invasion: causes, epidemiology, global consequences, and control. Ecol. Appl 10:689710.Google Scholar
Marler, M. J., Zabinski, C. A., and Callaway, R. M. 1999. Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:11801186.Google Scholar
McGonigle, T. 1988. A numerical analysis of published field trials with vesicular–arbuscular mycorrhizal fungi. Funct. Ecol 2:472478.Google Scholar
Mooreman, T. and Reeves, F. B. 1979. The role of endomycorrhizae in revegetation practices in the semiarid west. II. A bioassay to determine the effect of land disturbance on endomycorrhizal populations. Am. J. Bot 66:1418.Google Scholar
Mummey, D. L., Rillig, M. C., and Holben, W. E. 2005. Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:8390.Google Scholar
Munkvold, L., Kjøller, R., Vestberg, M., Rosendahl, S., and Jakobsen, I. 2004. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357364.Google Scholar
Newsham, K. K., Fitter, A. H., and Watkinson, A. R. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol. Evol 10:407411.CrossRefGoogle ScholarPubMed
Pedersen, C. T. and Sylvia, D. M. 1996. Mycorrhiza: ecological implications for plant interactions. Pages 195222. in Mukerji, K. G., editor. Concepts in Mycorrhiza. Dordrecht, Netherlands Kluwer.Google Scholar
Perotto, S. and Bonfante, P. 1997. Bacterial associations with mycorrhizal fungi: close and distant friends in the rhizosphere. Trends Microbiol 5:496501.Google Scholar
Phillips, J. M. and Hayman, D. S. 1970. Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc 55:158160.Google Scholar
Reinhart, K. and Callaway, R. 2004. Soil biota facilitate Acer invasions in Europe and North America. Ecol. Appl. 14 17371745.Google Scholar
Richardson, D. M. and Pyšek, P. 2006. Plant invasions: merging the concepts of species invasiveness and community invisibility. Progr. Phys. Geogr 30:409431.CrossRefGoogle Scholar
Sanders, I. R. 1999. No sex please, we're fungi. Nature 399:737739.CrossRefGoogle ScholarPubMed
SAS 2002. SAS User's Guide. Version 9.1. Cary, NC SAS Institute.Google Scholar
Sheeley, S. 1992. The distribution and life history characteristics of swallow-wort (Vincetoxicum rossicum). M.S. thesis. Syracuse, NY State University of New York College of Environmental Sciences and Forestry. 126.Google Scholar
Sheeley, S. E. and Raynal, D. J. 1996. The distribution and status of species of Vincetoxicum in eastern North America. Bull. Torrey Bot. Club 123:148156.Google Scholar
Smith, F. A., Jakobsen, I., and Smith, S. E. 2000. Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula . New Phytol 147:357366.Google Scholar
Smith, L. L., DiTommaso, A., Lehmann, J., and Greipsson, S. 2006. Growth and reproductive potential of the exotic invasive vine Vincetoxicum rossicum in northern New York state. Can. J. Bot 84:17711780.Google Scholar
Smith, S. E., Smith, F. A., and Jakobsen, I. 2004. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511524.Google Scholar
Stinson, K. A., Campbell, S. A., Powell, J. R., Wolfe, B. E., Callaway, R. M., Thelen, G. C., Hallett, S. G., Prati, D., and Klironomos, J. N. 2006. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727731.Google Scholar
Stutz, J. C., Copemanm, R., Martin, C. A., and Morton, J. B. 2000. Patterns of species composition and distribution of arbuscular mycorrhizal fungi in arid regions of southwestern North America and Namibia, Africa. Can. J. Bot 78:237245.Google Scholar
Turnbull, L. A., Crawley, M. J., and Rees, M. 2000. Are plant populations limited? A review of seed sowing experiments. Oikos 88:225238.Google Scholar
Van der Heijden, M. G. A. 2002. Arbuscular mycorrhizal fungi as determinants of plant diversity: in search of underlying mechanisms and general principles. Pages 243265. in Van der Heijden, M. G. M. and Sanders, I., editors. Mycorrhizal Ecology. Berlin, Germany Springer-Verlag.CrossRefGoogle Scholar
Van der Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., and Sanders, I. R. 1998. Mycorrhizal fungal diversity determines plant diversity, ecosystem variability and productivity. Nature 396:6972.Google Scholar
Van der Heijden, M. G. A., Wiemken, A., and Sanders, I. R. 2003. Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plants. New Phytol 157:569578.Google Scholar
West, H. M. 1996. Influence of arbuscular mycorrhizal infection on competition between Holcus lanatus and Dactylis glomerata . J. Ecol 84:429438.Google Scholar
Wilcove, D. S., Rothstein, D., and Dubow, J. 1998. Quantifying threats to imperiled species in the United States. BioScience 48:607615.Google Scholar
Wolfe, B. E. and Klironomos, J. N. 2005. Breaking new ground: soil communities and exotic plant invasion. BioScience 55:477487.Google Scholar
Zobel, M., Moora, M., and Haukioja, E. 1997. Plant coexistence in the interactive environment: arbuscular mycorrhiza should not be out of mind. Oikos 78:202208.Google Scholar