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Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus Cirsium (Asteraceae)

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Abstract

Previous studies have examined an association between reproductive success and pollination biology of rare versus widespread species through pair-wise comparisons of native and invasive congeners or rare and common congeners. To determine the importance of reproductive success and pollination biology for an invasive thistle, Cirsium vulgare, we compared it in its invaded range to five, co-occurring native Cirsium species that range from rare to common. Native study species include C. fontinale var. fontinale, C. andrewsii, C. brevistylum, C. occidentale, and C. quercetorum. We compared all species’ reproductive success, insect visitation rate and composition, autonomous self-pollination, and level of pollen limitation in multiple populations. Species differed in their reproductive success; the invasive C. vulgare produced more flower heads per plant than most native species. C. vulgare attracted more visitors than its congeners. In addition, reproductive success and insect visitation significantly varied between populations within species, mainly due to aphid infestation in one population of C. occidentale. Unlike the rare species (C. fontinale and andrewsii), C. vulgare did not require a pollinator for high-levels of seed production. The remaining native species set fewer seeds than C. vulgare without a pollinator. However, differences in insect visitation and autonomous self-pollination did not lead to differences in pollen limitation across species or between populations. This result suggests that factors other than pollination biology determine the difference in reproductive success of these species. However, high levels of autonomous self-pollination and generalist insect visitation may allow the invasive C. vulgare to easily establish new populations from low numbers of propagules. Our study provides one contrast that should build towards a larger comparative analysis to examine general patterns in the relationship between reproductive success, pollination biology, rare and invasive species, and our ability to predict biological invasions in introduced species.

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References

  • Aizen MA (2001) Flower sex ratio, pollinator abundance, and the season pollination dynamics of a protandrous plant. Ecology 82:127–144

    Article  Google Scholar 

  • Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281

    Article  PubMed  Google Scholar 

  • Ashman TL, Stanton M (1991) Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72:993–1003

    Article  Google Scholar 

  • Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347–349

    Article  Google Scholar 

  • Banks JA (1980) The reproductive biology of Erythronium propullans Gray and sympatric populations of E. albidum Nutt. (Liliaceae). Bull Torrey Bot Club 107:181–188

    Article  Google Scholar 

  • Barthell JF, Randall JM, Thorp RW, Wenner AM (2001) Promotion of seed set in yellow star-thistle by honey bees: evidence of an invasive mutualism. Ecol Appl 11:1870–1883

    Article  Google Scholar 

  • Baskin JM, Snyder KM, Walck JL, Baskin CC (1997) The comparative autecology of endemic, globally-rare, and geographically-widespread, common plant species: three case studies. Southwest Nat 42:384–399

    Google Scholar 

  • Bell TJ, Bowles M, McBride J, Havens K, Vitt P, McEachern K (2002) Reintroducing Pitcher’s Thistle. Endanger Species Bull 27:14–15

    Google Scholar 

  • Bevill RL, Louda SM (1999) Comparisons of related rare and common species in the study of plant rarity. Conserv Biol 13:493–498

    Article  Google Scholar 

  • Brown B, 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 

  • Bullock JM, Clear Hill B, Silvertown J (1994) Demography of Cirsium vulgare in a grazing experiment. J Ecol 82:101–111

    Article  Google Scholar 

  • Burd M (1994) Bateman’s 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 (2009) The impact of nutrient availability on floral characters and pollination in Ipomopsis aggregata and Linum lewisii. Plant Ecol 203:83–98

    Article  Google Scholar 

  • Burne HM, Yates CJ, Ladd PG (2003) Comparative population structure and reproductive biology of the critically endangered shrub Grevillea althoferorum and two closely related more common congeners. Biol Conserv 114:53–65

    Article  Google Scholar 

  • Burns JH (2006) Relatedness and environment affect traits associated with invasive and noninvasive introduced Commelinaceae. Ecol Appl 16:1367–1376

    Article  PubMed  Google Scholar 

  • California Exotic Pest Council (CalEPPC) (1999) Exotic pest plants of the greatest ecological concern in California, San Juan Capistrano

  • California Native Plant Society (CNPS) (2007) California native plant society’s inventory of rare and endangered plants of California (online edition, v7-07a) http://www.cnps.org/inventory. California Native Plant Society, Sacramento. Accessed Aug 2008

  • Cierjacks A, Rühr NK, Wesche K, Hensen I (2008) Effects of altitude and livestock on the regeneration of two tree line forming Polylepis species in Ecuador. Plant Ecol 194:207–221

    Article  Google Scholar 

  • Clampitt CA (1987) Reproductive biology of Aster curtus (Asteraceae), a Pacific Northwest endemic. Am J Bot 74:941–946

    Article  Google Scholar 

  • Cronquist A (1953) Specimens in European herbaria. Leafl West Bot 7:26

    Google Scholar 

  • Forcella F, Randall JM (1994) Biology of bull thistle, Cirsium vulgare (Savi.) Tenore. Rev Weed Sci 6:29–50

    Google Scholar 

  • Fritz-Sheridan JK (1988) Reproductive biology of Erythronium grandiflorum varieties grandiflorum and candidum (Liliaceae). Am J Bot 75:1–14

    Article  Google Scholar 

  • Gaston KJ, Kunin WE (1997) Rare-common differences: an overview. In: Kunin WE, Gaston KJ (eds) The biology of rarity: causes and consequences of rare-common differences. Chapman & Hall, London, pp 12–29

    Google Scholar 

  • Harmon-Threatt AN, Burns JH, Shemyakina LA, Knight TM (2009) Breeding system and pollination ecology of introduced plants compared to their native relatives. Am J Bot 96:1544–1550

    Article  Google Scholar 

  • Heimann B, Cussans GW (1996) The importance of seeds and sexual reproduction in the population biology of Cirsium arvense—a literature review. Weed Res 36:493–503

    Article  Google Scholar 

  • Hirao AS, Kameyama Y, Ohara M, Isagi Y, Kudo G (2006) Seasonal changes in pollinator activity influence pollen dispersal and seed production of the alpine shrub Rhododendron aureum (Ericaceae). Mol Ecol 15:1165–1173

    Article  PubMed  CAS  Google Scholar 

  • Johnston WR, Proctor J (1981) Growth of serpentine and nonserpentine races of Festuca rubra in solutions simulating the chemical conditions in a toxic serpentine soil. J Ecol 69:855–889

    Article  CAS  Google Scholar 

  • Karron JD (1987) A comparison of levels of genetic polymorphism and self-compatibility in geographically restricted and widespread plant congeners. Evol Ecol 1:47–58

    Article  Google Scholar 

  • Karron JD (1989) Breeding systems and levels of inbreeding depression in geographically restricted and widespread species of Astragalus (Fabaceae). Am J Bot 76:331–340

    Article  Google Scholar 

  • Kaye TN (1999) From flowering to dispersal: Reproductive ecology of an endemic plant, Astragalus australis var. olympicus (Fabaceae). Am J Bot 86:1248–1256

    Article  PubMed  Google Scholar 

  • Keddy CJ, Keddy PA (1984) Reproductive biology and habitat of Cirsium pitcheri. Mich Bot 23:57–67

    Google Scholar 

  • Kelch DG, Baldwin BG (2003) Phylogeny and ecological radiation of New World thistles (Cirsium, Cardueae–Compositae) based on ITS and ETS rDNA sequence data. Mol Ecol 12:141–151

    Article  PubMed  CAS  Google Scholar 

  • Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DF, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497

    Article  Google Scholar 

  • Kunin WE, Gaston KJ (1993) The biology of rarity: patterns, causes and consequences. Trends Ecol Evol 8:298–301

    Article  PubMed  CAS  Google Scholar 

  • Lalonde RG, Roitberg BD (1989) Resource limitation and offspring size and number trade-offs in Cirsium arvense (Asteraceae). Am J Bot 76:1107–1113

    Article  Google Scholar 

  • Lalonde RG, Roitberg BD (1994) Mating system, life history, and reproduction in Canada thistle (Cirsium arvense; Asteraceae). Am J Bot 81:21–28

    Article  Google Scholar 

  • Lavergne S, Thompson JD, Garnier E, Debussche M (2004) The biology and ecology of narrow endemic and widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos 107:505–518

    Article  Google Scholar 

  • Lavergne SM, Debussche M, Thompson JD (2005) Limitations on reproductive success in endemic Aquilegia viscosa (Ranunculaceae) relative to its widespread congener Aquilegia vulgaris: the interplay of herbivory and pollination. Oecologia 142:212–220

    Article  PubMed  Google Scholar 

  • Louda SV, Potvin MA (1995) Effect of inflorescence-feeding insects on the demography and lifetime fitness of a native plant. Ecology 76:229–245

    Article  Google Scholar 

  • Maron JL, Combs JK, Louda SV (2002) Convergent demographic effects of insect attack on related thistles in coastal vs. continental dunes. Ecology 83:3382–3392

    Article  Google Scholar 

  • Masters GJ, Jones TH, Rogers M (2001) Host-plant mediated effects of root herbivory on insect seed predators and their parasitoids. Oecologia 127:246–250

    Article  Google Scholar 

  • Mehrhoff LA III (1983) Pollination in the genus Isotria (Orchidaceae). Am J Bot 79:1444–1453

    Article  Google Scholar 

  • Michaux B (1989) Reproductive and vegetative biology of Cirsium vulgare (Savi) Ten. (Compositae: Cynareae). N Z J Bot 27:401–414

    Google Scholar 

  • Mitich LW (1998) Bull Thistle, Cirsium vulgare. Weed Technol 12:761–763

    Google Scholar 

  • Münzbergová Z (2005) Determinants of species rarity: population growth rates of species sharing the same habitat. Am J Bot 92:1987–1994

    Article  Google Scholar 

  • Murray BR, Thrall RH, Lepschi BJ (2002) Relating species rarity to life history in plants of eastern Australia. Evol Ecol Res 4:937–950

    Google Scholar 

  • Muth NZ, Pigliucci M (2006) Traits of invasives reconsidered: Phenotypic comparisons of introduced invasive and introduced noninvasive plant species within two closely related clades. Am J Bot 93:188–196

    Article  Google Scholar 

  • Ohashi K, Yahara T (1998) Effects of variation in flower number on pollinator visits in Cirsium purpuratum (Asteraceae). Am J Bot 85:219–224

    Article  Google Scholar 

  • Palmisano S, Fox LR (1997) Effects of mammal and insect herbivory on population dynamics of a native Californian thistle, Cirsium occidentale. Oecologia 111:413–421

    Article  Google Scholar 

  • Pavlik BM (2003) Plants that protect ecosystems: a survey from California. Biodivers Conserv 12:717–729

    Article  Google Scholar 

  • Powell KI, Knight TM (2009) Effects of nutrient addition and competition on biomass of five Cirsium species (Asteraceae), including a serpentine endemic. Int J Plant Sci 170:918–925

    Article  Google Scholar 

  • Pufal G, Mayer C, Porembski S, Jürgens N (2008) Factors affecting fruit set in Aizoaceae species of the Succulent Karoo. Basic Appl Ecol 9:401–409

    Article  Google Scholar 

  • Purdy BG, Bayer RJ, MacDonald SE (1994) Genetic variation, breeding system evolution, and conservation of the narrow sand dune endemic Stellaria arenicola and the widespread S. longipes (Caryophyllaceae). Am J Bot 81:904–911

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rabinowitz D, Rapp JK (1981) Dispersal abilities of seven sparse and common grasses from a Missouri Prairie. Am J Bot 68:616–624

    Article  Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions-the role of mutualisms. Biol Rev 75:65–93

    Article  PubMed  CAS  Google Scholar 

  • Rose KE, Louda SV, Rees M (2005) Demographic and evolutionary impacts of native and invasive herbivores on Cirsium canescens. Ecology 86:453–465

    Article  Google Scholar 

  • Rymer PD, Whelan RJ, Ayre DJ, Weston PH, Russel KG (2005) Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae). Biol Conserv 123:521–532

    Article  Google Scholar 

  • SPSS (2004) SPSS for Windows. Version 12.0.1. SPSS, Chicago

    Google Scholar 

  • Tenhumberg B, Louda SM, Eckberg JO, Takahashi M (2008) Monte-Carlo analysis of parameter uncertainty in matrix models of the weed Cirsium vulgare. J Appl Ecol 45:438–447

    Article  Google Scholar 

  • University and Jepson Herbaria (2006) Specimen Management for California Herbaria (SMASCH) database. Available via University of California, Berkeley. http://ucjeps.berkeley.edu/db/smasch/. Accessed 13 Sep 2009

  • van Kleunen M, Johnson SD (2007) Effects of self-compatibility on the distribution range of invasive European plant in North America. Conserv Biol 21:1537–1544

    PubMed  Google Scholar 

  • van Leeuwen BH (1981) The role of pollination in the population biology of the monocarpic species Cirsium palustre and Cirsium vulgare. Oecologia 51:28–32

    Article  Google Scholar 

  • Vanparys V, Meerts P, Jacquemart A-L (2008) Plant-pollinator interactions: comparison between an invasive and a native congeneric species. Acta Oecol 34:361–369

    Article  Google Scholar 

  • Young AG, Brown AHD (1998) Comparative analysis of the mating system of the rare woodland shrub Daviesia suaveolens and its common congener D. mimosoides. Heredity 80:374–381

    Article  Google Scholar 

  • Young HJ, Young TP (1992) Alternative outcomes of natural and experimental high pollen loads. Ecology 73:639–647

    Article  Google Scholar 

  • Young AS, Chang SM, Sharitz RR (2007) Reproductive ecology of a federally endangered legume, Baptisia arachnifera, and its more widespread congener, B. lanceolata (Fabaceae). Am J Bot 94:228–236

    Article  Google Scholar 

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Acknowledgments

We thank A. Banai and E. Dangremond for assistance with field work, N. Griffin for assistance with statistical analyses, E. Pardini for assistance with figures, the Knight Lab, M. Cadotte, J. Chase, K. Havens, R. Mitchell, and anonymous reviewers for comments on the manuscript, and J. Hernandez for assistance with insect pollinator identifications. We thank PRNS staff, especially J. Rodgers, B. Becker and E. Hamingson for logistical support. Funding was provided by a Howard Hughes Medical Institute Research Fellowship awarded to KIP, The Pacific Coast Science and Learning Center, and the Environmental Studies Program at Washington University.

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Correspondence to Kristin I. Powell.

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Powell, K.I., Krakos, K.N. & Knight, T.M. Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus Cirsium (Asteraceae). Biol Invasions 13, 905–917 (2011). https://doi.org/10.1007/s10530-010-9878-5

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