Skip to main content
Log in

Direct effects of a biocontrol agent are greater than indirect effects through flower visitors for the alien plant Dalmatian toadflax (Linaria dalmatica: Scrophulariaceae)

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Herbivory and pollination are important determinants of female reproductive success in flowering plants. Plants must interact with herbivores and flower visitors simultaneously and interaction with one may alter the outcome of the interaction with the other. These indirect effects can have dramatic impacts on plant fitness. The purpose of this study was to examine whether the stem-boring weevil Mecinus janthiniformis (Curculionidae: Coleoptera) affects flower visitation rate and seed set of the exotic plant Dalmatian toadflax (Linaria dalmatica (L.) Mill. Scrophulariaceae). We compared the flower production, flower morphology, visitation rate, fruit production, and pollen limitation on Dalmatian toadflax plants with and without larval feeding by M. janthiniformis. Feeding by M. janthiniformis reduced the number of flowers and per plant visitation rate, and there was a significant interaction between herbivory and flower number suggesting that the change in visitation rate was not solely a function of a reduction in flower abundance. Herbivory also had direct negative impacts on the reproductive success of Dalmatian toadflax. Total flower and fruit production decreased by over 30 % in plants attacked by M. janthiniformis. However, plants with M. janthiniformis were not more pollen-limited than those without M. janthiniformis. This suggests that herbivory had primarily direct effects female reproductive success.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  • Alex JF (1962) The taxonomy, history and distription of Linaria dalmatica. Can J Bot 40:295–307

    Article  Google Scholar 

  • Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR et al (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421

    Article  Google Scholar 

  • Barber NA, Adler LS, Theis N, Hazzard RV, Kiers ET (2012) Herbivory reduces plant interaction with above- and belowground antagonists and mutualists. Ecology 93:1560–1570

    Article  PubMed  Google Scholar 

  • Bigger DS, Marvier MA (1998) How different would a world without herbivory be? A search for generality in ecology. Integr Biol 1:60–67

    Article  Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plant: a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Breiter NC, Seastedt TR (2007) Postrelease evaluation of Mecinus janthinus host specificity, a biological control agent for invasive toadflax (Linaria spp.). Weed Sci 55:164–168

    Article  CAS  Google Scholar 

  • Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336

    Article  Google Scholar 

  • Burd M (1994) Bateman principle and plant reproduction—The role of pollen limitation in fruit and seed set. Bot Rev 60:83–139

    Article  Google Scholar 

  • Burkle LA, Irwin RE, Newman DA (2007) Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system. Am J Bot 94:1935–1943

    Article  PubMed  Google Scholar 

  • Campbell DR, Motten AF (1985) The mechanisms of competition for pollination between two forest herbs. Ecology 66:554–563

    Article  Google Scholar 

  • Cariveau DP, Norton AP (2009) Spatially contingent interactions between an exotic and native plant mediated through flower visitors. Oikos 118:107–114

    Article  Google Scholar 

  • Chittka L, Schurkens S (2001) Successful invasion of a floral market—An exotic Asian plant has moved in on Europe’s river-banks by bribing pollinators. Nature 411:653

    Article  CAS  PubMed  Google Scholar 

  • DeClerck-Floate RA, Miller V (2002) Overwintering mortality of and host attack by the stem-boring weevil, Mecinus janthinus Germar, on Dalmatian toadflax (Linaria dalmatica (L.) Mill.) in western Canada. Biol Cont 24:65–74

    Article  Google Scholar 

  • Docherty Z (1982) Self-incompatibility in Linaria. Heredity 49:349–352

    Article  Google Scholar 

  • Goodwillie C, Kalisz S, Ekert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Ann Rev Ecol Evol Sys 35:47–79

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hamback PA (2001) Direct and indirect effects of herbivory: feeding by spittlebugs affects pollinator visitation rates and seedset of Rudbeckia hirta. Ecoscience 8:45–50

    Google Scholar 

  • Herrera CM, Medrano M, Rey PJ, Sánchez-Lafuente AM, García MB, Guitián J, Manzaneda AJ (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc Natl Acad Sci 99:1682–16828

    Article  Google Scholar 

  • Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527

    Article  Google Scholar 

  • Johnson SG, Delph LF, Elderkin CL (1995) The effect of petal-size manipulation on pollen removal, seed set, and insect-visitor behavior in Campanula americana. Oecologia 102:174–179

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology 92:1769–1780

    Article  PubMed  Google Scholar 

  • Lehtila K, Strauss SY (1997) Leaf damage by herbivores affects attractiveness to pollinator in wild radish, Raphanus raphanistrum. Oecologia 111:396–403

    Article  Google Scholar 

  • Littel RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute Inc, Cary 633 pp

    Google Scholar 

  • Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  • Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution, and population growth. Proc R Soc B 273:2575–2584

    Article  PubMed Central  PubMed  Google Scholar 

  • McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 12:1351–1365

    Article  Google Scholar 

  • Mitchell RJ, Karron JD, Holmquist KG, Bell JM (2004) The influence of Mimulus ringens floral display size on pollinator visitation patterns. Func Ecol 18:116–124

    Article  Google Scholar 

  • Morales CL, Travest A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett 12:716–728

    Article  PubMed  Google Scholar 

  • Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilbert GS, Maron JL, Parker IM, Power AG, Torchin ME, Vázquez DP (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029

    Article  PubMed  Google Scholar 

  • Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40

    Google Scholar 

  • Naug D, Arathi HS (2007) Receiver bias for exaggerated signals in honeybees and its implications for the evolution of floral displays. Biol Lett 3:635–637

    Article  PubMed Central  PubMed  Google Scholar 

  • Newman DA, Thompson JD (2005) Effects of nectar robbing on nectar dynamics and bumblebee foraging strategies in Linaria vulgaris (Scrophulariaceae). Oikos 110:309–320

    Article  Google Scholar 

  • Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Google Scholar 

  • Parker IM (2000) Invasion dynamics of Cytisus scoparius: a matrix model approach. Ecol Appl 10:726–743

    Article  Google Scholar 

  • Pearson DE, Callaway RM (2003) Indirect effects of host-specifc biological control agents. Trends Ecol Evol 18:456–461

    Article  Google Scholar 

  • 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 34:899–990

    Article  Google Scholar 

  • Robocker WC (1974) The history, ecology, and control of Dalmatian toadflax. Washington Agricultural Experimental Station Bulletin #1330, Pullman, WA

  • Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56:293–312

    Article  CAS  PubMed  Google Scholar 

  • Schaeffer RN, Manson JS, Irwin RE (2013) Effects of abiotic factors on species interactions on estimates of male function: a meta-analysis. Ecol Lett 16:399–408

    Article  PubMed  Google Scholar 

  • Schat M, Sing SE, Peterson RKD, Menallend 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 46:232–246

    Google Scholar 

  • Sing SE, Peterson RKD, Weaver DK, Hansen RW, Markin GP (2005) A retrospective analysis of known and potential risks associated with exotic toadflax-feeding insects. Biol Cont 35:276–287

    Article  Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Ann Rev Ecol Evol Sys 35:435–466

    Article  Google Scholar 

  • Strauss SY, Conner JK, Rush SL (1996) Foliar herbivory affects floral characters and plant attractiveness to pollinators: implications for male and female plant fitness. Am Nat 147:1098–1107

    Article  Google Scholar 

  • Strauss SY, Conner JK, Lehtilä KP (2001) Effects of foliar herbivory by insects on the fitness of Raphanus raphanistrum: damage can increase male fitness. Am Nat 158:496–504

    Article  CAS  PubMed  Google Scholar 

  • Swope SM, Parker IM (2010) Trait-mediated interaction and lifetime fitness of the invasive plant Centaurea solstitialis. Ecology 91:2284–2293

    Article  PubMed  Google Scholar 

  • Swope SM, Parker IM (2012) Complex interaction among biocontrol agents, pollinators, and an invasive weed: a structural equation modeling approach. Ecol Appl 22:2122–2134

    Article  PubMed  Google Scholar 

  • Toveški I, Caldara R, Jović J, Hernández-Vera G, Baviera C, Gassman A, Emerson B (2011) Morphological, molecular, and biological evidence reveal two cryptic species in Mecinus janthinus Germar (Coleoptera, Curculionidae), a successful biological control agent of Dalmatian toadflax, Linaria dalmatica (Lamiales, Plantaginaceae). Syst Entomol 35:741–753

    Google Scholar 

  • 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 55:197–202

    Article  Google Scholar 

  • Vujnovic K, Wein RW (1997) The biology of Canadian weeds. 106. Linaria dalmatica (L.) Mill. Can J Plant Sci 77:483–491

    Article  Google Scholar 

  • Whitson TD, Burrill LC, Dewey SA, Cudney DW, Nelson BE, Lee RD, Parker R (2002) Dalmatian toadflax, Linaria dalmatica L. In: Whitson TD (ed) Weeds of the west. Western Society of Weed Science Press, Jackson, pp 540–541

    Google Scholar 

  • Wootton JT (1993) Indirect effects and habitat use in intertidal community—interaction chains and interaction modifications. Am Nat 141:71–89

    Article  Google Scholar 

  • Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Ann Rev Ecol Evol Sys 25:443–466

    Article  Google Scholar 

Download references

Acknowledgments

We thank J. Hardin and K. Jacobi for help in the field. A Brody, C Brown, B Kondratieff, and D. Naug provided invaluable comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel P. Cariveau.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cariveau, D.P., Norton, A.P. Direct effects of a biocontrol agent are greater than indirect effects through flower visitors for the alien plant Dalmatian toadflax (Linaria dalmatica: Scrophulariaceae). Biol Invasions 16, 1951–1960 (2014). https://doi.org/10.1007/s10530-013-0638-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0638-1

Keywords

Navigation