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Reproductive Biology |
Department of Biology, Queen's University, Kingston, Ontario K7L 3N6 Canada
Received for publication June 1, 2004. Accepted for publication November 17, 2004.
ABSTRACT
To test the hypothesis that increased allocation to reproduction is selected during biological invasion, we compared germination, survival, growth, and reproduction of native vs. introduced populations of the invasive aquatic plant Butomus umbellatus in a common greenhouse environment. Although seedling emergence and establishment did not differ consistently, survival thereafter was twice as high for eight introduced North American than eight native European populations. As predicted, introduced plants were more likely to produce sexual inflorescences and clonal asexual vegetative bulbils, and they invested much more biomass in both reproductive modes. Higher reproductive investment was due to higher proportional allocation of biomass rather than larger plant size. These results are consistent with selection for increased reproduction during range expansion. However, population genetic surveys indicate that recruitment from seed rarely occurs in introduced populations. Hence increased sexual allocation is not an adaptive response to invasion. Although increased clonal reproduction may be advantageous in expanding populations, genetic evidence from introduced populations of B. umbellatus suggests that increased clonal allocation may have arisen via stochastic processes during long-distance transport or a selective filter right at introduction, rather than incremental natural selection during range expansion.
Key Words: adaptation • allocation • biological invasion • clonal reproduction • founder effect • invasive plants • life history • sexual reproduction
Biologists have long recognized that the long-distance movement of species associated with biological invasion may have significant ecological and evolutionary consequences: both for the species in communities being invaded as well as the invasive species themselves (e.g., Elton, 1958
; Baker and Stebbins, 1965
; Mooney and Cleland, 2001
; Sakai et al., 2001
; Lee, 2002
). Renewed interest in the evolutionary consequences of biological invasion has been spurred by growing concern over the negative ecological and economic effects of invasive species (e.g., Mack et al., 2000
; Pimentel et al., 2000
) as well as the possibility that rapid evolutionary change in colonizing populations contributes to invasion success (Bone and Farres, 2001
; Sakai et al., 2001
; Stockwell et al., 2003
). Understanding evolutionary processes operating during invasion may, therefore, aid in the management of invasive species (Ashley et al., 2003
).
Invasive species often seem to be larger or have higher fecundity in their introduced range compared to their native range (Crawley, 1987
; Grosholz and Ruiz, 2003
; but see Thé baud and Simberloff, 2001
). This may be a plastic response to more favorable environmental conditions in the introduced range, resulting from increased resource availability or reduced biotic pressures from competitors or parasites (Keane and Crawley, 2002
; Wolfe, 2002
; but see Agrawal and Kotanen, 2003
; Mitchell and Power, 2003
; Torchin et al., 2003
). However, recent studies suggest that increased size during invasion can have a genetic basis, presumably resulting from natural selection. Most of the experimental work on adaptive evolution during invasion in plants has focused on the hypothesis that reduced pressure from pathogens and herbivores results in selection for the reallocation of resources from defense to functions such as growth and reproduction that enhance the ability of the invasive species to compete in the habitats it is invading ("evolution of increased competitive ability hypothesis," Blossey and Notzöld, 1995
; Adler, 1999
). To date, tests of this hypothesis using several plant species have produced conflicting results. In some studies, plants from introduced populations are larger and/or more fecund than those from native populations (five species: Pritchard, 1960
; Blossey and Notzöld, 1995
; Blossey and Kamil, 1996
; Willis and Blossey, 1999
; Siemann and Rogers, 2001
; Bastlova and Kvet, 2002
; Leger and Rice, 2003
; Blair and Wolfe, 2004
), while others have either not detected a difference between native and introduced plants or have found that native plants outperformed those from introduced populations (eight species: Willis et al., 2000
; van Kleunen and Schmid, 2003
; Vila et al., 2003
; Bossdorf et al., 2004
; DeWalt et al., 2004
; Maron et al., 2004
).
Rapid colonization of new habitats during biological invasion may cause selection on other aspects of morphology or life history that have been largely ignored in recent studies. Both classic life-history theory (Roff, 1992
) and arguments based on metapopulation dynamics (Olivieri and Gouyon, 1997
; Barrett and Pannell, 1999
) suggest that frequent episodes of colonization and population expansion may favor increased proportional allocation of resources to reproduction and dispersal. The fitness pay-off of reproductive effort is probably higher in rapidly growing populations because opportunities for recruitment and juvenile survival are relatively good. Moreover, new populations will tend to be founded by genotypes with relatively high allocation to multiplication and dispersal, thereby selecting for increased reproductive allocation at the metapopulation level (Piquot et al., 1998
). Although results from some studies are consistent with genetic increases in reproductive output associated with invasion (Siemann and Rogers, 2001
; Blair and Wolfe, 2004
), the extent to which this is simply a consequence of increased size vs. a shift in resource allocation has almost never been investigated (Warwick et al., 1987
; DeWalt et al., 2004
).
Very few of the studies investigating differences between native and introduced populations have rigorously tested whether observed increases in size, reproductive output or reproductive allocation are of demographic or adaptive significance in introduced populations. In this study, we used a common-environment experiment to test for an evolutionary increase in survival, plant size, sexual reproduction, clonal reproduction, and the allocation of biomass to both reproductive modes in introduced vs. native populations of an aquatic plant, Butomus umbellatus L. (Butomaceae, flowering rush). We then evaluate the adaptive significance of reproductive changes in light of population genetic estimates of the relative success of sexual and clonal reproduction during invasion.
Biological invasion and reproductive variation in Butomus umbellatus
Butomus umbellatus is an emergent, aquatic perennial indigenous to most of mainland Europe, the United Kingdom, Ireland, and temperate western Asia (Tutin et al., 1980
). It was first recorded in North America on the St. Lawrence River in 1897 and spread into eastern Lake Ontario and Lake Champlain over the next 30 years (Marie-Victorin, 1908
; Knowlton, 1923
; Muenscher, 1930
). A second centre of expansion occurred in southwestern Lake Erie, where it was first recorded in 1918, and subsequently spread into Michigan, Ohio, and southwestern Ontario around Lake Erie and into Lake St. Clair by the mid-1900s (Core, 1941
; Gaiser, 1949
; Stuckey, 1968
). The introduced range has since expanded westward and eastward to encompass most states and provinces along the Canada/USA border (White et al., 1993
). The impacts of B. umbellatus have not been formally studied, but the species can dominate the emergent aquatic vegetation under a wide range of ecological conditions (Zenkert, 1960
; Roberts, 1972
), inhibit industrial and recreational uses of shallow waters (Boutwell, 1990
; Les and Mehrhoff, 1999
), and threaten native littoral species like Zizania aquatica (wild rice), an economically important plant (B. Ranta, Ontario Ministry of Natural Resources, personal communication). Its increasingly rapid spread, especially within the Great Lakes region, has earned B. umbellatus the designation of "principal invasive alien" by the Government of Canada (White et al., 1993
).
Like most aquatic plants, B. umbellatus combines sexual reproduction via seed with clonal reproduction. In terms of vegetative growth, individual ramets consist of a monopodial prostrate rhizome that produces thin upright leaves from rhizome meristems (Wilder, 1974
; Lieu, 1979
). Axillary rhizome meristems also form pea-sized vegetative bulbils that function solely in genet multiplication and dispersal and are unambiguously organs of clonal reproduction (see Grace, 1993
). An individual ramet can produce hundreds of clonal bulbils per season (Thompson and Eckert, 2004
; Lui et al., in press
), which readily detach and quickly develop on the water surface or moist soil (C. G. Eckert, personal observation). A rhizome may break into several fragments over winter, but because they are large and rooted in the substrate, the contribution to multiplication and dispersal is probably negligible. Hence, we classify the rhizome as an organ of vegetative growth. Rhizome meristems also form inflorescences, often several per ramet per season, each consisting of an umbel of 20–50 pink flowers on a long, thin stalk. Flowers are fully self-compatible but require insect visitation for pollination and do not spontaneously self-fertilize (Eckert et al., 2000
). Clonal bulbils sometimes form in inflorescences but never in large numbers (i.e., <10 per plant, Lohammar, 1954
; Eckert et al., 2000
; Thompson and Eckert, 2004
).
In both its native and introduced range, B. umbellatus exhibits marked variation in sexual reproduction associated with polyploidy. Diploids (2n = 2x = 26) produce abundant viable seeds (mean > 20 000 seeds/plant/year), whereas triploids (2n = 3x = 39) produce very few or no viable seeds (Krahulcová and Jarolímová, 1993
; Eckert et al., 2000
; Hroudová and Zákravsky, 2003
; Lui et al., in press
). Individual populations almost always consist of only one cytotype (Krahulcová and Jarolímová, 1993
; Lui et al., in press
). There has been a major shift in cytotype frequencies during invasion: from predominant triploids in Europe to predominant diploids in North America (A. Kliber and C. G. Eckert, unpublished manuscript). The dominance of diploids in introduced populations is associated with a marked difference in reproductive allocation between cytotypes. Introduced diploids invest heavily in inflorescences (25% of biomass) and clonal bulbils (38% of biomass, mean = 300 bulbils/plant), whereas introduced triploids invest almost nothing in either reproductive mode, but heavily in a large, sedentary rhizome (Lui et al., in press
).
These results suggest that the success of the diploid cytotype in North America is due to its prodigious production of sexual and clonal propagules, especially because shallow-water habitat, and hence opportunity for the recruitment of sexual and clonal propagules, appears abundant in North America, but these habitats are often dredged in Europe to make waterways navigable. Triploids are rare in North America and genetic evidence suggests that triploids but not diploids spread through their sale as ornamentals (J. L. Montague, A. Kliber, and C. G. Eckert, unpublished manuscript). Here, we test the hypothesis that there has been an evolutionary increase in reproductive allocation by diploids associated with invasion of North America.
MATERIALS AND METHODS
Study populations
A survey of 108 populations of B. umbellatus from throughout Europe identified 17 diploid populations, only eight of which were in water shallow enough to allow flowering and subsequent seed production. We sampled all these native diploid populations and compared them to a sample of eight introduced diploid populations from southern Canada and northern USA (Table 1). Both samples represent a large portion of the genetic diversity detected within each region by population genetic surveys (A. Kliber and C. G. Eckert, unpublished manuscript). From each population, we collected a large sample of seed from 6–20 randomly selected maternal plants (mean = 12.5 "families" per population, Table 1). Three introduced and two native populations were sampled in 2000, and five introduced and six native populations were sampled in 2001. Hence we compared growth and reproduction between introduced and native populations in two sequential experiments.
|
; Eckert et al., 2000
). Seeds collected in 2000 and 2001 were sown in July and October 2002, respectively (hereafter experiments 1 and 2, respectively). Each sample of 20 seeds was sown on water-saturated soil in a 5.75-cm pot at 22–25°C, 65–70% humidity and 16 h light/day. Seedlings emerged and established over a 3-mo period and a 2-mo period for experiments 1 and 2, respectively. We individually transplanted established seedlings when they were 1 cm tall to 3-cm plug tray cells and grew them until they were 7 cm tall, after which they were transplanted to 7.5-cm pots, and eventually 10-cm pots if they appeared to be in danger of becoming pot-bound. All plants were harvested just before senescence (
5 mo after first transplant). We used ProMix ‘BX’ growth medium, fertilized plants with low concentrations of 20 : 20 : 20 (N : P : K) water-soluble fertilizer every 3 wk, and kept the soil flooded. Pots were randomly positioned on a single greenhouse bench and repositioned once a month. During the emergence and establishment phase of the experiment, we counted the number of seedlings in each pot once a week and calculated the proportion of seeds emerging as seedlings (emergence = maximum number of seedlings observed during a census/number of seeds sown) and the proportion of these seedlings surviving until first transplant (establishment = number of seedlings surviving until transplant/maximum number of seedlings observed). When there was more than one replicate per family, values were averaged.
Measuring plant size and reproductive allocation
As plants were growing, we removed and counted all senesced leaves. We harvested all surviving plants (except for population MBNM for which we harvested a random subsample of 50 plants), and separated each plant into leaves, rhizome, inflorescences, and clonal rhizome bulbils. Plants in this experiment only rarely produced inflorescence bulbils, hence we did not separate inflorescences into their sexual and clonal components. Each component was then dried at 70°C until constant mass and weighed to 0.01 g. We also counted the number of leaves (both living and senesced), bulbils and inflorescences produced by each plant. Average leaf weight was calculated for each plant and used to estimate the total mass of leaves that senesced throughout the experiment, which was added to the total leaf mass for each plant. We calculated survival from first transplant to harvest, and the amount of dry mass allocated to vegetative growth (leaves plus rhizome), sexual reproduction (inflorescences), and clonal reproduction (rhizome bulbils).
Statistical analyses
We tested for a difference between native and introduced populations in seedling emergence and establishment using a hierarchical analysis of variance (ANOVA) with experiment and region (native vs. introduced) as main fixed effects, and population nested within experiment and region as a random effect. Because this model combined fixed and random effects F tests were performed using restricted maximum-likelihood. Emergence and establishment proportions of individual seed families were arcsine transformed to meet assumptions of ANOVA.
Seedling emergence and establishment were low, so that surviving plants had to be pooled across families and populations within experiments and regions for subsequent analyses. Although this created statistical interdependence among data points, and some populations and families were much better represented than others (see sample sizes in Table 1), all the results obtained from analysis of pooled data were verified by analyses based on population means (not shown), which were statistically independent and relatively balanced.
Variation in the proportion of plants surviving until harvest, the proportion of plants producing clonal bulbils, and the proportion of plants producing inflorescences were evaluated using a two-way nominal logistic model with experiment and region as main effects. Individual effects were tested using likelihood-ratio 
2 tests. Variation in biomass components was evaluated using a two-way ANOVA with experiment and region as fixed effects. All biomass components were log10-transformed to meet the assumptions of ANOVA.
We quantified the allometric relations between log10-transformed biomass components using model II reduced major-axis regression (Sokal and Rohlf, 1995
). Variation in the coefficient of allometry (ß) between introduced and native plants was evaluated using analysis of covariance (ANCOVA) to test for interactions between the effects of the covariate (a biomass component) and region. All analyses used JMP (version 5, SAS Institute Inc., 2002
). All means are presented ±1 SE unless otherwise indicated.
The purpose of common environment experiments is to expose genetic differentiation among populations by removing the effects of variation in the environments from which the populations came. Our study, as well as almost all previous comparisons of native and introduced populations, used seed collected from natural populations. As a result, nongenetic maternal effects might contribute to variation in plant performance in the common environment (Roach and Wulff, 1987
). Maternal effects are unlikely to complicate our test for genetic differentiation between native and introduced populations for two reasons. First, plants from the native and introduced populations we sampled were growing in similar habitats, so there is no reason to expect a consistent regional difference in the quality of the maternal environment. Second, maternal effects are very unlikely to cause differences in reproductive allocation, especially when those differences are not associated with an average difference in plant size (Roach and Wulff, 1987
), as was the case in our experiment.
RESULTS
Emergence, establishment, survival, and plant size
The proportion of seeds emerging as seedlings and their subsequent establishment was generally low and varied substantially among populations (Fig. 1). Hierarchical ANOVA detected significantly higher establishment for experiment 1 than experiment 2 but did not detect any consistent difference in either emergence or establishment between native and introduced populations (Table 2, both P > 0.2). In contrast, survival from transplant to harvest was consistently much higher for introduced than native populations (Fig. 2; overall proportion surviving: introduced = 0.65, native = 0.25; nominal logistic model: effect of experiment 2 = 0.23, P = 0.62, effect of region 2 = 41.68, P < 0.00001, interaction between experiment and region 2 = 0.41, P = 0.52). The size of surviving plants, in terms of total dry mass, did not differ consistently between introduced and native populations (Fig. 2, Table 3). Although the effects of experiment and region interacted, there was no significant regional difference in total mass for either experiment (both P > 0.43).
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We have demonstrated major differences in plant performance and reproductive allocation between native and introduced populations of B. umbellatus in a common environment. Although seedling emergence and establishment did not differ between regions, introduced plants were more than twice as likely to survive till harvest than native plants. However, the most striking regional differences involved reproductive allocation. Compared to plants from native populations, plants from introduced populations were more likely to produce inflorescences and clonal bulbils, and they invested much more biomass in both modes of reproduction. Thus our results concur with some previous studies of invasive species demonstrating that, when grown in a common environment, plants from introduced populations outperform plants from native populations (Pritchard, 1960
; Blossey and Notzöld, 1995
; Blossey and Kamil, 1996
; Willis and Blossey, 1999
; Siemann and Rogers, 2001
; Bastlova and Kvet, 2002
; Leger and Rice, 2003
; Blair and Wolfe, 2004
). However, the marked reproductive differences between introduced and native populations observed in our study were not a consequence of introduced plants being larger than native plants, as there were no significant differences in the dry mass of surviving plants (see also DeWalt et al., 2004
). Rather, allometric analysis revealed that plants from introduced populations consistently allocated much more biomass to both clonal and sexual reproduction. Patterns of reproductive allocation very similar to those reported here were observed by Lui et al. (in press)
in a previous greenhouse study of eight introduced populations of B. umbellatus, including three of the populations used in the present study.
Although the high mortality during our experiment is likely typical of B. umbellatus in natural populations (Hroudová et al., 1996
; Hroudová and Zákravsky, 2003
), it greatly reduced replication at the family and population levels for later life history stages. Hence plants had to be pooled within regions for analysis. Nevertheless, the reproductive differences among widely sampled populations were large, consistent, and statistically significant using either plant values or population means (see Materials and Methods, Statistical analyses). Hence, we feel it safe to conclude that there is significant genetic differentiation in reproductive allocation between native and introduced populations of B. umbellatus.
Most comparisons of introduced and native populations implicitly or explicitly interpret increased vigor of plants from introduced populations in terms of evolutionary change in resource allocation. Usually, the enhanced survival and growth of introduced plants is viewed as a result of reduced allocation of resources to defensive chemistry and/or morphology as predicted by the "evolution of increased competitive ability (EICA) hypothesis" (Blossey and Notzöld, 1995
). Our observations of increased plant survival and reproductive output are consistent with the EICA hypothesis. However, further work is required to show that this is associated with reduced allocation to defense (Willis et al., 1999
; Siemann and Rogers, 2001
; Blair and Wolfe, 2004
) and increased vulnerability to herbivores (see also Daehler and Strong, 1997
; but see Willis et al., 1999
; Siemann and Rogers, 2003
).
How did increased sexual and clonal reproduction evolve during invasion?
The prodigious production of both sexual and clonal propagules of diploid B. umbellatus invading North America compared to diploid populations from the native range is consistent with the hypothesis that increased allocation to reproduction is favored during episodes of rapid range expansion both within populations, due to particularly good opportunities for recruitment (Roff, 1992
), and at the metapopulation level, because genotypes founding new populations may tend to be from lineages with high allocation to multiplication and dispersal (Olivieri and Gouyon, 1997
; Piquot et al., 1998
; Barrett and Pannell, 1999
). This interpretation is further supported by reproductive and distributional differences between the diploid and triploid B. umbellatus invading North America. Invading diploids have a high capacity for multiplication and dispersal through both sexual and clonal reproduction and they also predominate in North America, whereas North American triploids are relatively rare, are sexually sterile, and allocate almost nothing to clonal reproduction (Lui et al., in press
).
We can more critically evaluate this interpretation in light of large-scale surveys of the genetic structure of native and introduced populations of B. umbellatus (Eckert et al., 2003
; A. Kliber and C. G. Eckert, unpublished manuscript). There are three main findings germane to the interpretation of our results: (1) There has been a severe founder effect during the colonization of North America. (2) Genotypic diversity within and among introduced diploid populations is extremely low. Almost all diploid plants in North America express the same multilocus genotype. (3) Genotypic diversity and other indices of sexual recruitment do not differ between sexually fertile diploid and sexually sterile triploid populations in North America. The last two results suggest that, even though introduced diploid populations produce abundant viable seed, plants are rarely recruited from seed in introduced populations. This is consistent with the poor seedling survival we observed as well as the possibility that seed progeny compete with much more rapidly developing progeny from clonal bulbils during establishment (Lui et al., in press
). A lack of evidence for sexual recruitment casts serious doubt on the interpretation that increased sexual reproduction has been selected in introduced populations during colonization.
Population-genetic data suggest that the spread of B. umbellatus in North America is mediated by clonal bulbils. Hence, increased allocation to clonal reproduction, which typifies plants from introduced diploid populations, might have been selected during colonization. However, the lack of evidence for sexual recruitment further suggests that increased clonal multiplication has probably not arisen via incremental natural selection acting on recombinational genetic variation during range expansion in North America. Moreover, invading diploids allocate substantially to both reproductive modes, even though seed seems to be of little functional significance in North America, and the investment of resources in seed reduces the ability of individual plants to make clonal bulbils (Thompson and Eckert, 2004
). Moreover, quantitative genetic analysis of introduced B. umbellatus has not revealed any genetic correlation between reproductive modes that would cause selection for increased clonal allocation to necessarily increase sexual allocation (Thompson and Eckert, 2004
).
Genetic evidence for a severe founder effect during the introduction of B. umbellatus to North America raises the possibility that the differences we observed between native and introduced populations are a byproduct of stochastic processes during long-distance transport. Several high-profile invasive plants appear to have experienced changes in reproductive mode due to founder effect altering allele frequencies at major loci controlling the sexual system (e.g., dioecious Elodea Canadensis, Sculthorpe, 1967
; tristylous Eichhornia crassipes, Barrett and Forno, 1982
), although this possibility has rarely been tested with data from genetic markers (but see Hollingsworth and Bailey, 2000
). Alternatively, increased survival and reproductive allocation in introduced populations of B. umbellatus may be the product of a strong selective filter operating right at introduction. Most long-distance species introductions (>90%) appear to fail at the outset (Williamson and Fitter, 1996
), and it has been suggested that, for any given species, establishment in the adventive range may be contingent on the introduction of a genotype(s) with particular characteristics that allow it to spread where others have gone extinct (Mack et al., 2000
; Simons, 2003
). Unlike recurrent natural selection, a selective filter may not yield well-optimized phenotypes, especially if there have been relatively few introductions. As a result, the diploid B. umbellatus invading North America allocates heavily to both reproductive modes, even though only clonal reproduction is of any functional significance. Unfortunately, unpredictable interactions between selective and stochastic forces at introduction will make the selective filter hypothesis difficult to test in any general way.
Where and when natural selection may have taken place is unknown for most cases of apparently adaptive changes during invasion. Although most workers have assumed that selection has arisen from conditions encountered during spread in the adventive range (e.g., Leger and Rice, 2003
), there is usually little evidence to support this (but see Daehler and Strong, 1997
; Siemann and Rogers, 2001
; Maron et al., 2004
). The role that stochastic processes might have played in influencing selection during colonization has also been largely neglected (Eckert et al., 1996
). Based on the discussion presented here, closer integration of experimental analyses of geographical trait variation with large-scale population-genetic surveys is likely to provide a better understanding of the evolutionary consequences of biological invasion.
FOOTNOTES
1 The authors thank Agnes Kliber, Keiko Lui, Anna Mayer, Barbara Ozimec, and Faye Thompson for sampling natural populations in Europe and North America; Eva Bruni, Dale Kristensen, Tracy-Lynn Reside, and Sarah Yakimowski for help in the greenhouse; Shelley Arnott for helpful suggestions; Alison Derry, Jill Hamilton, Jessica Montague, Karen Samis, and Sarah Yakimowski for comments on the manuscript; and the Natural Sciences and Engineering Research Council of Canada for a discovery grant to CGE. 
2 Author for correspondence (phone: 613-533-6158; fax: 613-533-6617; eckertc{at}biology.queensu.ca
)
LITERATURE CITED
Adler F. R 1999 The balance of terror: an alternative mechanism for competitive trade-offs and its implications for invading species. American Naturalist 154: 497-509[CrossRef][Medline]
Agrawal A. A P. M Kotanen 2003 Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecology Letters 6: 712-715[CrossRef][ISI]
Ashley M. V M. F Willson O. R. W Pergams D. J O'Dowd S. M Gende J. S Brown 2003 Evolutionarily enlightened management. Biological Conservation 111: 115-123[CrossRef][ISI]
Baker H. G G. L Stebbins 1965 The genetics of colonizing species. Academic Press, New York, New York, USA
Barrett S. C. H I. W Forno 1982 Style morph distribution in New World populations of Eichhornia crassipes (Mart.) Solms-Laubach (water hyacinth). Aquatic Botany 13: 299-306[CrossRef][ISI]
Barrett S. C. H J. R Pannell 1999 Metapopulation dynamics and mating-system evolution in plants. In P. M. Hollingsworth, R. M. Bateman, and R. J. Gornall [eds.], Molecular systematics and plant evolution, 74–100. Taylor & Francis, London, UK
Bastlova D J Kvet 2002 Differences in dry weight partitioning and flowering phenology between native and non-native plants of purple loosestrife (Lythrum salicaria L). Flora 197: 332-340[ISI]
Blair A. C L. M Wolfe 2004 Evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85: 3035-3042[CrossRef][ISI]
Blossey B R Notzöld 1995 Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology 83: 887-889[CrossRef]
Blossey B J Kamil 1996 Is the superior competitive ability of invasive plants a result of changes in biomass allocation patterns?. Bulletin of the Ecological Society of America 77: (Supplement) 41
Bone E A Farres 2001 Trends and rates of microevolution in plants. Genetica 112: 165-182
Bossdorf O D Prati H Auge B Schmid 2004 Reduced competitive ability in an invasive plant. Ecology Letters 7: 346-353[CrossRef][ISI]
Boutwell J. E 1990 Flowering-rush: a plant worth watching. Aquatics 12: 8-11
Core E. L 1941 Butomus umbellatus in America. Ohio Journal of Science 41: 79-85
Crawley M. J 1987 What makes a community invasible?. In A. J. Gray, M. J. Crawley, and P. J. Edwards [eds.], Colonization, succession and stability, 429–453. Blackwell Scientific, Oxford, UK
Daehler C. C D. R Strong 1997 Reduced herbivore resistance in introduced smooth cordgrass (Spartina alterniflora) after a century of herbivore-free growth. Oecologia 110: 99-108[CrossRef][ISI]
DeWalt S. J J. S Denslow J. L Hamrick 2004 Biomass allocation, growth, and photosynthesis of genotypes from native and introduced ranges of the tropical shrub Clidemia hirta. Oecologia 138: 521-531[CrossRef][ISI][Medline]
Eckert C. G D Manicacci S. C. H Barrett 1996 Genetic drift and founder effect in native vs. introduced populations of an invading plant, Lythrum salicaria (Lythraceae). Evolution 50: 1512-1519[CrossRef][ISI]
Eckert C. G B Massonnet J. J Thomas 2000 Variation in sexual and clonal reproduction among introduced populations of flowering rush, Butomus umbellatus (Butomaceae). Canadian Journal of Botany 78: 437-446[CrossRef][ISI]
Eckert C. G K Lui K Bronson P Corradini A Bruneau 2003 Population genetic consequences of extreme variation in sexual and clonal reproduction in an aquatic plant. Molecular Ecology 12: 331-344[CrossRef][Medline]
Elton C 1958 The ecology of invasions by plants and animals. Methuen, London, UK
Gaiser L. O 1949 Further distribution of Butomus umbellatus in the Great Lakes region. Rhodora 51: 385-390
Grace J. B 1993 The adaptive significance of clonal reproduction in angiosperms: an aquatic perspective. Aquatic Botany 44: 159-180
Grosholz E. D G. M Ruiz 2003 Biological invasions drive size increases in marine and estuarine invertebrates. Ecology Letters 6: 700-705[CrossRef][ISI]
Hollingsworth M. L J. P Bailey 2000 Evidence for massive clonal growth in the invasive weed Fallopia japonica (Japanese Knotweed). Botanical Journal of the Linnean Society 133: 463-472[CrossRef]
Hroudová Z A Krahulcová P Zákravsky V Jarolímová 1996 The biology of Butomus umbellatus in shallow waters with fluctuating water level. Hydrobiologia 340: 27-30[CrossRef][ISI]
Hroudová Z P Zákravsky 2003 Germination responses of diploid Butomus umbellatus to light, temperature and flooding. Flora 198: 37-44[ISI]
Keane R. M M. J Crawley 2002 Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17: 164-170
Knowlton C. H 1923 Butomus umbellatus on the St. Lawrence River. Rhodora 25: 220-221
Krahulcová A V Jarolímová 1993 Ecology of two cytotypes of Butomus umbellatus I. Karyology and breeding. Folia Geobotanica et Phytotaxonomica 28: 385-411
Lee C. E 2002 Evolutionary genetics of invasive species. Trends in Ecology & Evolution 17: 386-391[CrossRef][ISI]
Leger E. A K. J Rice 2003 Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecology Letters 6: 257-264[CrossRef][ISI]
Les D. H L. J Mehrhoff 1999 Introduction of nonindiginous aquatic vascular plants in southern New England: a historical perspective. Biological Invasions 1: 281-300[CrossRef]
Lieu S. M 1979 Growth forms in the Alismatales. II. Two rhizomatous species: Sagittaria lancifolia and Butomus umbellatus. Canadian Journal of Botany 63: 175-182
Lohammar G 1954 Bulbils in the inflorescences of Butomus umbellatus. Svensk Botanisk Tidskrift 48: 485-488
Lui K F. L Thompson C. G Eckert In press Causes and consequences of extreme variation in reproductive strategy among invasive populations of a clonal aquatic plant, Butomus umbellatus (Butomaceae). Biological Invasions
Mack R. N D Simberloff W. M Lonsdale H Evans 2000 Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689-710[CrossRef][ISI]
Marie-Victorin F 1908 Addition á la flore d'Amerique. Naturaliste Canadien 34: 65-67
Maron J. L M Vila R Bommarco S Elmendorf P Beardsley 2004 Rapid evolution of an invasive plant. Ecological Monographs 74: 261-280[CrossRef][ISI]
Mitchell C. E A. G Power 2003 Release of invasive plants from fungal and viral pathogens. Nature 421: 625-627[CrossRef][Medline]
Mooney H. A E. E Cleland 2001 The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences, USA 98: 5446-5451
Muenscher W. C 1930 Butomus umbellatus in the Lake Champlain basin. Rhodora 32: 19-20
Muenscher W. C 1936 Storage and germination of seeds of aquatic plants. Cornell University Agricultural Station, Ithaca, New York, USA
Olivieri I P.-H Gouyon 1997 Evolution of migration rate and other traits. In I. A. Hanski and M. A. Gilpin [eds.], Metatpopulation biology. Ecology, genetics and evolution, 293–323. Academic Press, San Diego, California, USA
Pimentel D L Lach R Zuniga D Morrison 2000 Environmental and economic costs of nonindigenous species in the USA. Bioscience 50: 53-64[CrossRef][ISI]
Piquot Y D Petit M Valero J Cuguen P deLaguerie P Vernet 1998 Variation in sexual and asexual reproduction among young and old populations of the perennial macrophyte Sparganium erectum. Oikos 82: 139-148[CrossRef][ISI]
Pritchard T 1960 Race formation in weedy species with special reference to Euphorbia cyparissias L. and Hypericum perforatum L. In J. L. Harper [ed.], The biology of weeds: a symposium of the British Ecological Society, 61–66. Blackwell Scientific, Oxford, UK
Roach D. A R. D Wulff 1987 Maternal effects in plants. Annual Review of Ecology and Systematics 18: 209-235
Roberts M. L 1972 Butomus umbellatus in the Mississippi watershed. Castanea 37: 83-85
Roff D. A 1992 The evolution of life histories. Chapman & Hall, New York, New York, USA
Sakai A. K F. W Allendorf J. S Holt D. M Lodge J Molofsky K. A With S Baughman R. J Cabin J. E Cohen N. C Ellstrand D. E McCauley P O'Neil I. M Parker J. N Thompson S. G Weller 2001 The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305-332
SAS Institute, Inc. 2002 JMP user's guide, version 5.0. SAS Institute, Inc., Cary, North Carolina, USA
Sculthorpe C. D 1967 The biology of aquatic vascular plants. Edward Arnold, London, UK
Siemann E W. E Rogers 2001 Genetic differences in growth of an invasive tree species. Ecology Letters 4: 514-518[CrossRef][ISI]
Siemann E W. E Rogers 2003 Reduced resistance of invasive varieties of the alien tree Sapium sebiferum to a generalist herbivore. Oecologia 135: 451-457[ISI][Medline]
Simons A. M 2003 Invasive aliens and sampling bias. Ecology Letters 6: 278-280[CrossRef][ISI]
Sokal R. R F. J Rohlf 1995 Biometry, 3rd ed. W. H. Freeman and Company, New York, New York, USA
Stockwell C. A A. P Hendry M. T Kinnison 2003 Contemporary evolution meets conservation biology. Trends in Ecology & Evolution 18: 94-101[CrossRef][ISI]
Stuckey R. L 1968 Distributional history of Butomus umbellatus (flowering rush) in western Lake Erie and Lake St. Clair region. Michigan Botanist 7: 134-142
Thébaud C D Simberloff 2001 Are plants really larger in their introduced ranges?. American Naturalist 157: 231-236[CrossRef][ISI]
Thompson F. L C. G Eckert 2004 Trade-offs between sexual and clonal reproduction in an aquatic plant: experimental manipulations vs. phenotypic correlations. Journal of Evolutionary Biology 17: 581-592[CrossRef][ISI][Medline]
Torchin M. E K. D Lafferty A. P Dobson V. J McKenzie A. M Kuris 2003 Introduced species and their missing parasites. Nature 421: 628-630[CrossRef][Medline]
Tutin T. G V. H Heywood N. A Burgess D. M Moore D. H Valentine S. M Walters D. A Webb 1980 Flora Europea. Cambridge University Press, Cambridge, UK
van Kleunen M B Schmid 2003 No evidence for an evolutionary increased competitive ability in an invasive plant. Ecology 84: 2816-2823[CrossRef][ISI]
Vila M A Gomez J. L Maron 2003 Are alien plants more competitive than their native conspecifics? A test using Hypericum perforatum L. Oecologia 137: 211-215[CrossRef][ISI][Medline]
Warwick S. I B. K Thompson L. D Black 1987 Genetic variation in Canadian and European populations of the colonizing weed species Apera spica-venti. New Phytologist 106: 301-317[CrossRef][ISI]
White D. J E Haber C Keddy 1993 Invasive plants of natural habitats in Canada. Canadian Wildlife Service, Environment Canada, Ottawa, Canada
Wilder G. J 1974 Symmetry and development of Butomus umbellatus (Butomaceae) and Limnocharis flava (Limnocharitaceae). American Journal of Botany 61: 379-394[CrossRef][ISI]
Williamson M A Fitter 1996 The varying success of invaders. Ecology 77: 1661-1666[CrossRef][ISI]
Willis A. J B Blossey 1999 Benign environments do not explain the increased vigour of non-indigenous plants: a cross-continental transplant experiment. Biocontrol Science and Technology 9: 567-577[CrossRef][ISI]
Willis A. J M. B Thomas J. H Lawton 1999 Is the increased vigour of invasive weeds explained by a trade-off between growth and herbivore resistance?. Oecologia 120: 632-640[CrossRef][ISI]
Willis A. J J Memmott R. I Forrester 2000 Is there evidence for the post-invasion evolution of increased size among invasive plant species?. Ecology Letters 3: 275-283[CrossRef][ISI]
Wolfe L. M 2002 Why alien invaders succeed: support for the escape-from-enemy hypothesis. American Naturalist 160: 705-711[CrossRef][ISI]
Zenkert C. A 1960 The Old-World flowering rush: an attractive and aggressive immigrant. Science on the March 40: 71-75
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20 seeds from each of 6–20 (mean = 12.5) maternal seed families per population (see 
