Abstract
Plant performance is influenced by both top-down (e.g., herbivores) and bottom-up (e.g., soil nutrients) controls. Research investigating the collective effects of such factors may provide important insight into the success and management of invasive plants. Through a combination of observational and experimental field studies, we examined top-down and bottom-up effects on the growth and reproduction of an invasive plant, Linaria dalmatica. First, we assessed attack levels and impacts of an introduced biocontrol agent, the stem-mining weevil Mecinus janthinus, on L. dalmatica plants across multiple years and sites. Then, we conducted a manipulative experiment to examine the effects of weevil attack, soil nitrogen availability, and interspecific competition on L. dalmatica. We found substantial variations in weevil attack within populations as well as across sites and years. Observational and experimental data showed that increased weevil attack was associated with a reduction in plant biomass and seed production, but only at the highest levels of attack. Nitrogen addition had a strong positive effect on plant performance, with a two-fold increase in biomass and seed production. Clipping neighboring vegetation resulted in no significant effects on L. dalmatica performance, suggesting that plants remained resource limited or continued to experienced belowground competitive effects. Overall, our research indicates that M. janthinus can exert top-down effects on L. dalmatica; however, weevil densities and attack rates observed in this study have not reached sufficient levels to yield effective control. Moreover, bottom-up controls, in particular, soil nitrogen availability, may have a large influence on the success and spread of this invasive plant.
Similar content being viewed by others
References
Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New York
Bigger DS, Marvier MA (1998) How different would a world without herbivory be? A search for generality in ecology. Integr Biol 1:60–66
Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889
Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895
Blumenthal DM (2009) Carbon addition interacts with water availability to reduce invasive forb establishment in a semi-arid grassland. Biol Invasions 11:1281–1290
Blumenthal DM, Norton AP, Seastedt TR (2010) Restoring competitors and natural enemies for long-term control of plant invaders. Rangelands 32:16–20
Borer ET, Halpern BS, Seabloom EW (2006) Asymmetry in community regulation: effects of predators and productivity. Ecology 87:2813–2820
Bowers MD (1991) Iridoid glycosides. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 297–326
Burke IC, Lauenroth WK, Parton WJ (1997) Regional and temporal variation in net primary production and nitrogen mineralization in grasslands. Ecology 78(5):1330–1340
Catford JA, Roland J, Christer N (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15(1):22–40
Daehler CC (2003) Performance comparisons of co-occurring native and alien plants: implications for conservation and restoration. Annu Rev Ecol Syst 34:183–211
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534
De Clerck-Floate R, Harris P (2002) Linaria dalmatica (L.) Miller, Dalmatian toadflax (Scrophulariaceae). In: Mason PG, Huber JT (eds) Biological control programmes in Canada 1981–2000. CABI Publishing, New York, pp 368–374
Duncan CA, Jachetta JJ, Brown ML, Carrithers VF, Clark JK, Ditomaso JM, Lym RG, McDaniel KC, Renz MJ, Rice PM (2004) Assessing the economic, environmental, and societal losses from invasive plants on rangeland and wildlands. Weed Technol 18:1411–1416
Egan FJ, Irwin RE (2008) Evaluation of the field impact of an adventitious herbivore on an invasive plant, yellow toadflax, in Colorado, USA. Plant Ecol 199(1):99–114
Gröger VD, Johne S (1965) Über das vorkommen von peganin in Linaria-Arten. Planta Med 13(2):182–188
Gruner DS, Smith JE, Seabloom EW, Sandin SA, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken MES, Borer ET, Bolker BM (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–755
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
Hairston NG (1960) Community structure, population control, and competition. Am Nat 94:421–425
Hillebrand H, Gruner DS, Borer ET, Bracken MES, Cleland EE, Elser JJ et al (2007) Consumer vs. resource control of producer diversity depends on ecosystem type and producer community structure. Proc Natl Acad Sci USA 104:10904–10909
Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasions and community structure in Californian serpentine grasslands. Ecology 71:478–491
Inderjit, Cadotte MW, Colautti RI (2005) The ecology of biological invasions: past, present and future. In: Inderjit (ed) Invasive plants: ecological and agricultural aspects. Birkhäuser Verlag, Basel, pp 19–44
Jamieson MA, Bowers MD (2010) Iridoid glycoside variation in the invasive plant Dalmatian toadflax, Linaria dalmatica (Plantaginaceae), and sequestration by the biological control agent, Calophasia lunula. J Chem Ecol 36:70–79
Jamieson MA, Bowers MD (in press) Soil nitrogen availability and herbivore attack influence the chemical defenses of an invasive plant (Linaria dalmatica; Plantaginaceae). Chemoecology. doi:10.1007/s00049-011-0087-1
Jeanneret P, Schroeder C (1992) Biology and host specificity of Mecinus janthinus Germar (Col: Curculionidae), a candidate for the biological control of yellow and Dalmatian toadflax, Linaria vulgaris (L.) Mill. and Linaria dalmatica (L.) Mill. (Scrophulariaceae) in North America. Biocontrol Sci Technol 2:25–34
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 117:164–169
Knochel DG, Seastedt TR (2010) Reconciling contradictory findings of herbivore impacts on the growth and reproduction of spotted knapweed (Centaurea stoebe). Ecol Appl 20:1903–1912
Knochel DG, Monson ND, Seastedt TR (2010) Additive effects of above- and belowground herbivores on the dominance of spotted knapweed (Centaurea stoebe). Oecologia 164:701–712
Lejeune KD, Suding KN, Sturgis S, Scott A, Seastedt TR (2005) Biological control insect use of fertilized and unfertilized diffuse knapweed in a Colorado grassland. Environ Entomol 34:225–234
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences and control. Ecol Appl 10:689–710
McEvoy PB, Rudd NT, Cox CS, Huso M (1993) Disturbance, competition, and herbivory effects on ragwort Senecio jacobaea populations. Ecol Monogr 63:55–75
Myers JH, Bazely D (2003) Ecology and control of introduced plants. Cambridge University Press, Cambridge
Peterson RKD, Sing SE, Weaver DK (2005) Differential physiological responses of Dalmatian toadflax, Linaria dalmatica L. Miller, to injury from two insect biological control agents: implications for decision-making in biological control. Environ Entomol 34:899–905
Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251
Prudic KL, Oliver JC, Bowers MD (2005) Soil nutrient effects on oviposition preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia 143:578–587
Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr 30(3):409–431
Saner MA, Jeanneret P, Mullerscharer H (1994) Interaction among 2 biological-control agents and the developmental stage of their target weed, Dalmatian toadflax, Linaria dalmatica (L) Mill (Scrophulariaceae). Biocontrol Sci Technol 4(2):215–222
Schat M, Sing SE, Peterson RKD, Menalled FD, Weaver DK (2011) Growth inhibition of Dalmatian toadflax, Linaria dalmatica (L.) Miller, in response to herbivory by the biological control agent Mecinus janthinus Germar. J Entomol Sci 46(3):232–246
Seastedt TR, Pyšek P (2011) Mechanisms of invasions in North American and European grasslands. Annu Rev Ecol Evol Syst 42:133–153
Seastedt TR, Suding KN (2007) Biotic constraints on the invasion of diffuse knapweed (Centaurea diffusai) in North American grasslands. Oecologia 151(4):626–636
Seastedt TR, Gregory N, Buckner D (2003) Reduction of diffuse knapweed by biocontrol insects in a Colorado grassland. Weed Sci 51:237–245
Suding KN, LeJeune KD, Seastedt TR (2004) Competitive impacts and responses of an invasive weed: dependencies on nitrogen and phosphorus availability. Oecologia 141:526–535
Van Hezewijk BH, Bourchier RS, De Clerck-Floate RA (2010) Regional-scale impact of the weed biocontrol agent Mecinus janthinus on Dalmatian toadflax (Linaria dalmatica). Biol Control 55(3):197–202
Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478
Wilson LM, Sing SE, Piper GL, Hansen RW, De Clerck-Floate R, MacKinnon DK, Randall C (2005) Biology and biological control of Dalmatian and yellow toadflax. USDA Forest Service, Morgantown, FHTET-05-13
Wise MJ, Abrahamson WG (2007) Effects of resource availability on tolerance of herbivory: a review and assessment of three opposing models. Am Nat 169:443–454
Acknowledgments
Many thanks are due to Sarah Travers, Patrick Travers, Nicole Won, Ariana Calderon, and Hayden Hedman for their assistance in field and laboratory. Manuscript clarity was greatly improved by Janet S. Prevéy, and three anonymous reviewers. We also thank the City of Boulder, Boulder County, and Linda and Sergio Sanabria for use of their land to conduct research. Funding was provided by the Boulder County Open Space and Parks, the US Department of Agriculture NRI CSREES grant number, 2009-55320-05072 and 2009-04893, and the National Science Foundation grants, DEB 0614883 and 0808473.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jamieson, M.A., Knochel, D., Manrique, A. et al. Top-down and bottom-up controls on Dalmatian toadflax (Linaria dalmatica) performance along the Colorado Front Range, USA. Plant Ecol 213, 185–195 (2012). https://doi.org/10.1007/s11258-011-0013-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-011-0013-1