Oecologia

, Volume 146, Issue 3, pp 373–384

Indirect interaction between two native thistles mediated by an invasive exotic floral herbivore

Plant Animal Interactions

Abstract

Spatial and temporal variation in insect floral herbivory is common and often important. Yet, the determinants of such variation remain incompletely understood. Using 12 years of flowering data and 4 years of biweekly insect counts, we evaluated four hypotheses to explain variation in damage by the Eurasian flower head weevil, Rhinocyllus conicus, to the native North American wavyleaf thistle, Cirsium undulatum. The four factors hypothesized to influence weevil impact were variations in climate, weevil abundance, phenological synchrony, and number of flower heads available, either on wavyleaf thistle or on the other cooccurring, acquired native host plant (Platte thistle, Cirsium canescens), or on both. Climate did not contribute significantly to an explanation of variation in R. conicus damage to wavyleaf thistle. However, climate did influence weevil synchrony with wavyleaf flower head initiation, and phenological synchrony was important in determining R. conicus oviposition levels on wavyleaf thistle. The earlier R. conicus was active, the less it oviposited on wavyleaf thistle, even when weevils were abundant. Neither weevil abundance nor availability of wavyleaf flower heads predicted R. conicus egg load. Instead, the strongest predictor of R. conicus egg load on wavyleaf thistle was the availability of flower heads on Platte thistle, the more common, earlier flowering native thistle in the sand prairie. Egg load on wavyleaf thistle decreased as the number of Platte thistle flower heads at a site increased. Thus, wavyleaf thistle experienced associational defense in the presence of flowering by its now declining native congener, Platte thistle. These results demonstrate that prediction of damage to a native plant by an exotic insect may require knowledge of both likely phenological synchrony and total resource availability to the herbivore, including resources provided by other nontarget native species.

Keywords

Associational defense Biocontrol Invasive species Insect herbivory Phenological synchrony 

References

  1. Aizen MA, Patterson WA (1995) Leaf phenology and herbivory along a temperature gradient: a spatial test of the phenological window hypothesis. J Veg Sci 6:543–550CrossRefGoogle Scholar
  2. Angulo-Sandoval P, Aide TM (2000) Seasonal variation in leaf characteristics and food selection by larval noctuids on an evergreen Mediterranean shrub. Acta Oecol 21:257–265CrossRefGoogle Scholar
  3. Atsatt PR, O’Dowd DJ (1976) Plant defense guilds. Science 193:24–29PubMedCrossRefGoogle Scholar
  4. Bevill RL, Louda SM, Stanforth LM. (1999) Protection from natural enemies in managing rare plant species. Cons Biol 13:1323–1331CrossRefGoogle Scholar
  5. Bleed A, Flowerday C (1989) An Atlas of the Sand Hills. Resource Atlas no. 5. University of Nebraska, Institute of Agriculture and Natural Resources, Lincoln, NEGoogle Scholar
  6. Chaneton EJ, Bonsall MB (2000) Enemy-mediated apparent competition: empirical patterns and the evidence. Oikos 88:380–394CrossRefGoogle Scholar
  7. Crawley MJ (1983) Herbivory: the dynamics of animal-plant interactions. University of California Press, BerkeleyGoogle Scholar
  8. Crawley MJ (1992) Seed predators and plant population dynamics. In: Fenner M, (ed) Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford, UK, pp 157–192Google Scholar
  9. Gassmann A, Louda SM (2001) Rhinocyllus conicus: initial evaluation and subsequent ecological impacts in North America. In Wajnberg E, Scott JK, Quimby PC, (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, CABI International, Wallingford, Oxon, UK, pp 147–183Google Scholar
  10. Great Plains Flora Association (1986) Flora of the Great Plains. University Press of Kansas, Lawrence, KSGoogle Scholar
  11. Hails RS, Crawley MJ (1991) The population dynamics of an alien insect: Andricus quercuscalicis (Hymenoptera: Cynipidae). J Anim Ecol 60:545–562CrossRefGoogle Scholar
  12. Hamback PA, Beckerman AP (2003) Herbivory and plant resource competition: a review of two interacting interactions. Oikos 101:26–37CrossRefGoogle Scholar
  13. Holt RD (1977) Predation, apparent competition and the structure of prey communities. Theor Popul Biol 12:197–229CrossRefPubMedGoogle Scholar
  14. Holt RD, Hochberg ME (2001) Indirect interactions, community modules and biological control: a theoretical perspective. In: Wajnberg E, Scott JK, Quimby PC, (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, pp 13–37Google Scholar
  15. Hunter AF, Elkinton J (2000) Effects of synchrony with host plant on populations of spring-feeding Lepidopteran. Ecology 81:1248–1261CrossRefGoogle Scholar
  16. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492CrossRefGoogle Scholar
  17. Kelly CA, Dyer RJ (2002) Demographic consequences of inflorescence-feeding insects for Liatris cylindracea, an iteroparous perennial. Oecologia 132:350–360CrossRefGoogle Scholar
  18. Kerslake JE, Hartley SE (1997) Phenology of winter moth feeding on common heather: effects of source population and experimental manipulation of hatch dates. J Anim Ecol 66:375–385CrossRefGoogle Scholar
  19. Koenig WD, Knops JMH (2000) Patterns of annual seed production by northern hemisphere trees: a global perspective. Am Nat 155:59–69CrossRefPubMedGoogle Scholar
  20. Lamp WO, McCarty MK (1981) Biology and ecology of Platte thistle (Cirsium canescens). Weed Sci 29:686–692Google Scholar
  21. Leimu R, Syrjanen K, Ehrlen J, Lehtila KP (2002) Pre-dispersal seed predation in Primula veris: among-population variation in damage intensity and selection on flower number. Oecologia 133:510–516CrossRefGoogle Scholar
  22. Louda SM (1982a). Distribution ecology: Variation in plant recruitment in relation to insect seed predation. Ecol Monogr 52:25–41CrossRefGoogle Scholar
  23. Louda SM (1982b). Limitation of the recruitment of the shrub Haplopappus squarrosus (Asteraceae) by flower- and seed-feeding insects. J Ecol 70:43–53CrossRefGoogle Scholar
  24. Louda SM (1983) Seed predation and seedling mortality in the recruitment of a shrub, Haplopappus venetus (Asteraceae), along a climatic gradient. Ecology 64:511–521CrossRefGoogle Scholar
  25. Louda SM (1989) Differential predation pressure: a general mechanism for structuring plant communities along complex environmental gradients? Trends Ecol Evol 4:158–159CrossRefGoogle Scholar
  26. Louda SM (1998) Population growth of Rhinocyllus conicus (Coleoptera: Curculionidae) on two species of native thistles in prairie. Environ Entomol 27:834–841Google Scholar
  27. Louda SM (2000) Negative ecological effects of the musk thistle biocontrol agent, Rhinocyllus conicus Fröl. In: Follet PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer, Boston, pp 215–243Google Scholar
  28. Louda SM, Arnett AE (2000) Predicting non-target ecological effects of biological control agents: evidence from Rhinocyllus conicus. In: Spencer NR (ed) Proceedings of the 10th international symposium on the biological control of weeds. Montana State University, Bozeman, pp 551–567Google Scholar
  29. Louda SM, Potvin MA (1995) Effect of inflorescence-feeding insects in the demography and lifetime fitness of a native plant. Ecology 76:229–245CrossRefGoogle Scholar
  30. Louda SM, Rodman JE (1996) Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, bittercress). J Ecol 84:229–238CrossRefGoogle Scholar
  31. Louda SM, Dixon PM, Huntly NJ (1987) Herbivory in sun and shade at a natural meadow-woodland ecotone in the Rocky Mountains. Vegetation 72:141–149Google Scholar
  32. Louda, SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science (USA) 277: 1088–1090Google Scholar
  33. Louda SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090CrossRefGoogle Scholar
  34. Louda SM, Arnett AE, Rand TA, Russell FL (2003) Invasiveness of some biological control insects challenges adequacy of ecological risk assessment and regulation. Cons Biol 17:1–11CrossRefGoogle Scholar
  35. Maron JL, Combs JK, Louda SM (2002) Insect herbivory on thistles: congruent interaction strengths in coastal vs. continental dunes. Ecology 83:3382–3392Google Scholar
  36. Mopper S, Simberloff D (1995) Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76:1233–1241CrossRefGoogle Scholar
  37. Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Ann Rev Ecol Syst 16:264–271CrossRefGoogle Scholar
  38. Rodriguez J, Jordano D, Fernandez Haeger J (1994) Spatial heterogeneity in a butterfly-host plant interaction. J Anim Ecol 63:31–38CrossRefGoogle Scholar
  39. Rose KA, Louda SM, Rees M (2005) Demographic and evolutionary impacts of native and invasive insect herbivores on Cirsium canescens. Ecology 86:453–465CrossRefGoogle Scholar
  40. Russell FL, Louda SM (2004) Phenological synchrony affects interaction strength of an exotic weevil with Platte Thistle, a native hostplant. Oecologia 139:525–534CrossRefPubMedGoogle Scholar
  41. Smith TJ III (1987) Seed predation in relation to tree dominance and distribution in mangrove forests. Ecology 68:266–273CrossRefGoogle Scholar
  42. Smith LM, Kok LT (1985) Influence of temperature on the development and mortality of immature Rhinocyllus conicus (Coleoptera: Curculionidae). Environ Entomol 14:629–633Google Scholar
  43. Smith LM, Kok LT (1987) Influence of temperature on oviposition, quiescence, and mortality of Rhinocyllus conicus (Coleoptera: Curculionidae). Environ Entomol 16:971–974Google Scholar
  44. Solbreck C, Sillen-Tullberg B (1986) Seed production and seed predation in a patchy and time-varying environment. Dynamics of a milkweed-tephritid fly system. Oecologia 71:51–58CrossRefGoogle Scholar
  45. Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321–346CrossRefGoogle Scholar
  46. Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New YorkGoogle Scholar
  47. Tauber MJ, Tauber CA, Nyrop JP, Villani MG (1998) Moisture, a vital but neglected factor in the seasonal ecology of insects: hypotheses and tests of mechanisms. Environ Entomol 27:523–530Google Scholar
  48. Vandermeer J (1989) The ecology of intercropping. Cambridge University Press, CambridgeGoogle Scholar
  49. Zwölfer H, Harris P (1984) Biology and host specificity of Rhinocyllus conicus (Froel.) (Col., Curculionidae), a successful agent for biocontrol of the thistle, Carduus nutans L. Z Angew Entomol 97:36–62Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of Nebraska-LincolnLincolnUSA
  2. 2.Department of Biological SciencesWichita State UniversityWichitaUSA

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