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.
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
Alex JF (1962) The taxonomy, history and distription of Linaria dalmatica. Can J Bot 40:295–307
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
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
Bigger DS, Marvier MA (1998) How different would a world without herbivory be? A search for generality in ecology. Integr Biol 1:60–67
Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plant: a hypothesis. J Ecol 83:887–889
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
Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336
Burd M (1994) Bateman principle and plant reproduction—The role of pollen limitation in fruit and seed set. Bot Rev 60:83–139
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
Campbell DR, Motten AF (1985) The mechanisms of competition for pollination between two forest herbs. Ecology 66:554–563
Cariveau DP, Norton AP (2009) Spatially contingent interactions between an exotic and native plant mediated through flower visitors. Oikos 118:107–114
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
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
Docherty Z (1982) Self-incompatibility in Linaria. Heredity 49:349–352
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
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
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
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
Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527
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
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology 92:1769–1780
Lehtila K, Strauss SY (1997) Leaf damage by herbivores affects attractiveness to pollinator in wild radish, Raphanus raphanistrum. Oecologia 111:396–403
Littel RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute Inc, Cary 633 pp
Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545
Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution, and population growth. Proc R Soc B 273:2575–2584
McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 12:1351–1365
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
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
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
Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40
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
Newman DA, Thompson JD (2005) Effects of nectar robbing on nectar dynamics and bumblebee foraging strategies in Linaria vulgaris (Scrophulariaceae). Oikos 110:309–320
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
Parker IM (2000) Invasion dynamics of Cytisus scoparius: a matrix model approach. Ecol Appl 10:726–743
Pearson DE, Callaway RM (2003) Indirect effects of host-specifc biological control agents. Trends Ecol Evol 18:456–461
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
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
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
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
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
Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Ann Rev Ecol Evol Sys 35:435–466
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
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
Swope SM, Parker IM (2010) Trait-mediated interaction and lifetime fitness of the invasive plant Centaurea solstitialis. Ecology 91:2284–2293
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
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
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
Vujnovic K, Wein RW (1997) The biology of Canadian weeds. 106. Linaria dalmatica (L.) Mill. Can J Plant Sci 77:483–491
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
Wootton JT (1993) Indirect effects and habitat use in intertidal community—interaction chains and interaction modifications. Am Nat 141:71–89
Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Ann Rev Ecol Evol Sys 25:443–466
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
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-013-0638-1