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1 Department of Biological Sciences, University of Windsor, 401 Sunset Avenue, Windsor, Ontario, Canada N9B 3P4
Received for publication May 29, 1998. Accepted for publication April 20, 1999.
ABSTRACT
Seed mass is considered to be the least plastic component of reproductive yield. Yet, in invasive populations of garlic mustard, Alliaria petiolata, seed mass was highly variable (eightfold among populations, 2.5–7.5 fold within populations, two-threefold within individuals, and 1.4–1.8 fold within fruits). Variation in seed mass among populations explained nearly half of the total variance. Variation among seeds within fruits accounted for a further 25% of variance. Individual seed mass within a plant decreased with increased distance from the main stem, suggesting that access to parental resources limits seed size in a predictable manner. MANOVAs and Roy-Bargmann stepdown analyses revealed significant effects of seed mass, but not seed position (within a fruit or within an infructescence), on an array of subsequent seedling traits. Smaller seeds germinated significantly earlier, and seedlings from small seeds produced their first primary leaves significantly later and grew significantly taller. After accounting for seed mass as a covariate, only one seedling trait, date of first leaf emergence, was affected by seed position in a fruit. Differences in seed mass may therefore affect seedling recruitment via effects on early seedling growth in this weedy species.
Key Words: Alliaria petiolata • Brassicaceae • positional effects • seed mass variation • seed production • seedling traits
Seed mass varies considerably among species in different habitats and different stages of succession (Salisbury, 1942
; Baker, 1972
; Michaels et al., 1988
; but see Kelly, 1996
). Within a species, seed size has long been considered to be the most stable component of reproductive yield (Harper, Lovell, and Moore, 1970
). In theory, stabilizing selection on individual plants to maintain constant seed size should be intense. Empirically, however, studies have detected significant amounts of intraspecific variation in mean seed size between annual cohorts (Obeso, 1993
), between populations of a species (McWilliams, Landers, and Mahlstede, 1968
; Lord, 1994
; McKee and Richards, 1996
), and between individuals within a population (Cavers and Steel, 1984
; Ågren, 1989
; Mehlman, 1993
). Even within plants, seed size may vary considerably among infructescences (Navarro, 1996
; Vaughton and Ramsey, 1997
), fruits within infructescences (Matthies, 1990
; Obeso, 1993
; Stöcklin and Favre, 1994
), and seeds within fruits (Rocha and Stephenson, 1990
; Stöcklin and Favre, 1994
; Yanful and Maun, 1996
; Méndez, 1997
).
A number of hypotheses have been proposed to account for variation in seed size. If resources are limited to any extent, then supplying individual seeds with greater starting capital must come at the expense of another component of reproductive yield. Smith and Fretwell (1974)
suggested that a trade-off between seed number and seed mass should occur where seed number varied with changing resource status, while seed mass remained relatively constant. The existence of variation in seed mass has been attributed to a number of sources. Seed size variation may produce an optimal seed shadow (Janzen, 1977
) or minimize the risk of failure in heterogeneous environments (Venable and Brown, 1988
). Also, variation in seed size might be adaptive if seeds of different sizes differ in genetic quality (Temme, 1986
). Alternatively, seed size variation might be the result of architectural and physiological constraints (McGinley, Temme, and Geber, 1987
; Wolfe, 1992
; Diggle, 1995
), maternal effects (Mazer, 1986
; Roach and Wulff, 1987
; Gutterman, 1992
; Sills and Nienhuis, 1995
), or reduced resource availability throughout the growing season (Cavers and Steel, 1984
; Winn, 1991
).
The availability of seed reserves will likely influence any subsequent seedling establishment. It has been recognized for a long time that seed size can have important effects on seedling traits, including germination (Schaal, 1980
; Weis, 1982
; Zimmerman and Weis, 1983
; Dolan, 1984
), emergence (Stanton, 1984
; Hendrix and Trapp, 1992
; Yanful and Maun, 1996
), survivorship (Schaal, 1980
; Hendrix and Trapp, 1992
), seedling size (Schaal, 1980
; Weis, 1982
), and seedling competitive ability (Black, 1957
; Houssard and Escarré, 1991
). As a result, seed mass may have significant effects on the persistence or invasiveness of a given species in a habitat. However, in many instances differences in early seedling development do not persist into adulthood (Zimmerman and Weis, 1983
; Houssard and Escarré, 1991
; Reich, Oleksyn, and Tjoelker, 1994
). Hence, the variations evident at the earliest points of germination and immediately postgermination may be of greatest significance to initial establishment in a population, but not, necessarily, to survivorship to reproductive maturity.
Our study had three primary objectives. First, we wished to determine the extent of natural seed mass variation in the weedy biennial Alliaria petiolata at sites across a latitudinal transect of a large portion of its adventive range in North America. Secondly, we examined the degree of seed mass variation within and among fruits on plants from each of these sites. Lastly, we wanted to assess whether differences in seed mass influenced seedling traits in this fecund and rapidly spreading weed. Specifically we determined: (1) the extent of geographical variation in seed mass; (2) the partitioning of variance in seed mass within and among fruits, individuals, and populations; (3) the effect of seed position within a fruit and within a plant on seed mass; (4) the effect of the source population on the probability of seed germination; and (5) whether the position of a seed on a plant, controlling for seed mass, affects germination and seedling establishment.
MATERIALS AND METHODS
Garlic mustard, Alliaria petiolata (M. Bieb.) Cavara and Grande (Brassicaceae), is a biennial herb that is often the dominant herbaceous species in wet forest and floodplain edges (Cavers, Heagy, and Kokron, 1979
). In populations around Windsor, Ontario, seed germination begins in mid-to-late March. First-year plants consist of a rosette of dark-green, reniform-shaped leaves, which persist through the winter. In the spring of their second year, most individuals produce a single raceme in which the opening of small, white flowers proceeds acropetally. Individual flowers remain open for 2–3 d, with most flowers being pollinated on the first day of flower opening (Cruden, McClain, and Shrivastava, 1996
). In southwestern Ontario, the flowering period lasts from 4 to 6 wk. Following fertilization, plants mature numerous two-loculed, linear fruits. Each fruit produces 8–24 ovules, arranged alternately on both sides of a sinus. These ovules maintain a persistent connection to the wall of the ovary, which allowed us to record the position of an ovule or seed within a fruit.
Sampling procedure and fruit standardization
During summer 1994, we sampled 14 populations of A. petiolata along a latitudinal transect of a portion of the species' distribution in central North America (Table 1). Generally, mean temperature, rainfall, and number of frost-free days were least at more northerly latitudes or more continental locations (Table 1). At most populations, the length of all stems as well as the numbers of stems, infructescences, and mature fruits were recorded for each of 100 plants. At population TN-1, garlic mustard plants were scarce, so only 44 plants were assessed. The fully ripened, mature fruits (i.e., those having at least one mature seed) of ten randomly selected plants were harvested from each population for further analysis. Each of these ten individuals was chosen to have a single stem, bearing only one terminal infructescence. These individuals were selected to control for the effect of plant size as a covariate, since size may be highly correlated with reproductive effort in A. petiolata (Aarssen and Taylor, 1992
; Susko, 1998
). The maternal identity and relative position of each mature fruit within an infructescence were recorded at the time of fruit collection. At this time, all mature seeds had ripened completely, but had yet to be shed from the plant. Fruits were left to air-dry in a cool, dry storage cabinet for 4 mo prior to analysis of their contents.
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). The fate and position of each ovule were recorded, starting at the basal end of a fruit (i.e., nearest to the pedicel) and proceeding to the distal tip. Mature seeds were removed from a fruit and weighed individually on a Sartorius Model M3P microbalance (Sartorius Canada Inc., Mississauga, Ontario, Canada) to 0.001 mg. There was a mean number of 16 ovules per fruit, however the total number of ovules per fruit varied significantly among fruits (Susko and Lovett-Doust, 1998
). Thus, to compare the effects of seed position on seed mass among fruits having different numbers of ovules, we standardized ovule position by applying the formula developed by Hossaert and Valéro (1988)
for leguminous fruits. This procedure transformed each of the sampled fruits to a standardized size. The transformation formula was
 |
).
Seed experiment 1
A bulk seed collection from 100 randomly chosen plants was made from each population in our geographic survey. These seeds were used to assess the effects of seed source on germination in an experiment conducted in the winter of 1994–1995. For each population, we placed 40 seeds on a petri plate (9 cm diameter) containing Whatman number 4 filter paper moistened with 10 mL of distilled water. Each treatment was replicated with 20 petri plates. All petri plates were placed in continuous darkness at 4°C. This temperature/light regime was necessary to break dormancy and maximize germination (Baskin and Baskin, 1992
). During this experiment, seeds were exposed to brief periods of light (1–2 min) when germination counts were made. A seed was recorded as germinated when we observed the emergence of the radicle. Observations were made every 3 d, until no further seeds had germinated for a week following the last recorded day of germination (137 d from the start of the experiment). Plates were kept moist as needed. One-way ANOVAs and post hoc Tukey-Kramer tests were used to assess differences in number of days to 50% germination and overall germination frequencies.
Seed experiment 2
Fruits from 12 individuals at site OH-7 were harvested in the field and placed in labeled envelopes. Each of these single-stemmed plants had a single terminal infructescence that had a minimum of 12 mature fruits. Subsequently, each of the seeds within these fruits was weighed individually. These seeds were used to examine the effects of seed position within a plant on seedling traits. For each plant, we divided fruits into three fruit-position classes within the infructescence: base (nearest the base of an infructescence), middle, and tip (nearest the apex). Fruits were assigned to a fruit-position class by dividing the number of fruits present into thirds. For uneven numbers of fruits any "extra" or "missing" fruits were placed into the middle fruit-position class. Four fruits were studied as replicates from each fruit-position class. Each fruit, in turn, was divided into three within-fruit-position classes: base, middle, and tip. Thus, there was a total of nine classes that identified seeds in terms of their position within a plant.
Each seed was placed at random in an individual well of a tissue culture plate (Falcon 96-well Microtest III Tissue Culture Plates, Canadawide Scientific Ltd., Ottawa, Ontario, Canada) to which 50 µL of distilled water were added. All plates were placed in darkness for cold stratification at 1°C for 70 d. The tissue culture plates were covered with lids during this portion of the experiment. Plates were kept moist as needed. After 70 d (prior to any seed germination), each seed was individually transplanted into a single cell (4 x 4 x 5 cm) of a germination tray (36 cells) filled with a standard commercial soil mixture (Pro-mix BX, Plant Products Co., Brampton, Ontario, Canada). Seedling trays were placed in a Conviron CMP 3244 growth chamber (Controlled Environments Ltd., Winnipeg, Manitoba, Canada), set with a 20°C light (14 h)/10°C dark (10h) germination regime. Seedling trays were monitored daily. Measurements recorded for each seed included time to germination, time to first true leaf emergence, height of the plant at first leaf emergence, and length of the longest cotyledon at first leaf emergence. Seedlings were harvested 30 d after germination. Seedlings were dried to constant mass at 80°C for 3 d, and total plant biomass was determined.
Differences in seed mass among seed-position classes were tested with one-way analysis of variance (ANOVA). We performed univariate analyses of covariance (ANCOVA) with seed mass as the covariate (SYSTAT, 1992
) to test for significant differences among seed-position classes with respect to the seedling traits indicated above. Hence, we attempted to determine whether the position of a seed on a plant had an effect on seedling traits, independent of its actual mass. We also used multivariate analyses of covariance (MANCOVA) with seed mass as the first covariate to determine whether the variability in one or more seedling traits explained any additional variance in another trait. A significant Wilks' Lambda result was followed by stepdown Roy-Bargmann analysis (see Tabachnick and Fidell, 1996
), where the priority of dependent variables was ordered from highest to lowest as: days to germination, days to first leaf emergence, height of the plant, cotyledon size, and seedling biomass. The benefit of using multivariate analyses was protection against Type I error resulting from multiple tests of correlated dependent variables (e.g., days to germination and days to first leaf emergence, cotyledon size, and seedling biomass, etc.). To further avoid inflated Type I error due to multiple MANCOVAs, we assigned a more conservative alpha of 0.01 to each seedling trait, to keep the overall alpha at 0.05 (Tabachnick and Fidell, 1996
). In order to assess the specific effects of seed mass on these measures, seeds were grouped according to mass into three size classes: small (0.8–1.8 mg), medium (1.8–2.8 mg), and large (>2.8 mg). We used both ANOVAs and MANOVAs, followed by stepdown Roy-Bargmann analysis, to determine the effect of seed mass on all seedling traits. Where any analyses indicated significant effects, comparisons were made using post hoc Tukey-Kramer tests.
RESULTS
Variation in components of yield
Most components of reproductive yield varied clinally among geographic regions (Table 2). In general, plants from southern populations were larger and had greater fruit and seed production than those from northern sites (Table 2). Since some plants had multiple flowering stems, we summed the lengths of all stems to generate the total stem length per plant as an estimate of plant size (and reproductive potential). The mean total stem length (range 4.0–553.8 cm) of individuals did not differ significantly among the three southernmost regions, but was significantly smaller in Ontario (Table 2). The mean values for number of stems (range 1–6), infructescences (range 1–23), mature fruits (range 1–321), and seeds (range 7–3672) on an individual all decreased from southern to northern latitudes (Table 2). For garlic mustard individuals at a given site, the number of seeds per plant was estimated by multiplying the respective population's mean number of seeds per fruit by the number of fruits on a specific plant. Unlike most other measures of yield, mean individual seed mass did not decrease with increased latitude. Instead, seed mass was significantly lower in populations nearer the geographic periphery of the species' range (i.e., Tennessee and Ontario) than in the centre (i.e., Kentucky and Ohio; see Table 2). Seeds in fruits from Ohio were significantly larger, followed by those from Kentucky, Tennessee, and Ontario.
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2 = 0.63, P > 0.05). Germination schedules and measures of subsequent seedling size varied among seed-position classes within garlic mustard individuals (Tables 6, 7). Seed mass, number of days to germination, seedling height, cotyledon size, and seedling biomass were all affected by seed position, both among fruits and among seeds within fruits. Seeds from basal fruits weighed more, germinated later, and produced shorter but heavier seedlings than did seeds from fruits nearer to the tip of a plant (Table 6). A similar trend was observed for seeds from different positions within fruits. Seeds from basal positions within fruits weighed more, germinated later, and produced shorter but heavier seedlings than did seeds from nearer to the tips of fruits (Table 6). Date of emergence of the first true leaf did not display any consistent trend across seed-position classes (Table 6). After adjustment had been made for seed mass as a covariate, seedling height, the number of days to germination, and the number of days to first-leaf production all differed significantly among seed-position classes following univariate analysis (Table 7). In a multivariate analysis the combined measures of seedling traits (i.e., days to germination, days to first-leaf emergence, seedling height, cotyledon length, seedling biomass) were significantly related to seed mass and seed-position class (Wilks' Lambda = 0.924, df = 40, 4719, F = 2.157, P < 0.001). Only the number of days to first-leaf emergence differed significantly among seed-position classes following Roy-Bargmann stepdown analysis and adjustment of significance levels (Table 7). In other words, variation in seed mass accounted for the differences among seed-position classes in most seedling traits. Only the date of first-leaf emergence was affected significantly by the position of a seed within a plant irrespective of the seed's mass.
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2 = 0.09, P > 0.05). However, overall, smaller seeds germinated earlier (Table 8). The seedlings that resulted from small seeds began leaf production later and grew taller, but had smaller cotyledons and total biomass than did seedlings from larger seeds (Table 8). All seedling traits differed significantly in a univariate context (Table 7). In a multivariate analysis, combined measures of seedling traits were significantly affected by seed-size class (Wilks' Lambda = 0.778, df = 10, 2178, F = 29.202, P < 0.001). All traits except seedling biomass at 30 d differed significantly among seed-size classes, following Roy-Bargmann stepdown analysis and adjustment of significance levels (Table 7).
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Geographical variation
Most components of reproductive yield in mature plants of Alliaria petiolata were significantly greater in populations from southern regions compared with northern ones. Overall, more than three times as many fruits and seeds developed on individuals in Tennessee, compared to Ontario. The size of plants, degree of branching, and extent of fruit and seed production are all likely to be phenotypically plastic responses to temperature, amount of precipitation, and length of growing season in a given geographic region. In a survey of 34 British populations of common reed, Phragmites australis, McKee and Richards (1996)
demonstrated that although seed set was highly variable among sites, southern and western populations tended to have higher seed sets than northern populations. Furthermore, seed set was shown to be associated with climatic conditions (rainfall and temperature statistics) at these sites. In our study, population means for yield components varied considerably, suggesting that plant size may also be influenced by prevailing local environmental conditions, including perhaps, the associated species, aspect, drainage, and soil type. For example, Anderson and Kelley (1995)
found that soil pH affected the sizes of individuals in garlic mustard populations throughout Illinois; plant mass was greatest in the least acidic soils. As a result, these workers suggested that pH may be a factor limiting the spread of garlic mustard in the state.
Several studies have noted clinal patterns of seed mass variation with respect to both altitude (Baker, 1972
; Lord, 1994
) and latitude (McWilliams, Landers, and Mahlstede, 1968
). For instance, Baker (1972)
observed that mean seed mass for a species decreased with increased altitudes in the mountains of California. In the mustard Capsella bursa-pastoris, Hurka and Benneweg (1979)
reported that seed size was associated with climatic conditions in Europe; large seeds were found in adverse climates, while small seeds occurred in milder climates. On the other hand, seed mass did not vary clinally across latitudes in populations of the perennial herb Prunella vulgaris (Winn and Gross, 1993
). Although P. vulgaris seed mass varied to some extent among populations within different geographic regions, when plants from these seeds were grown in a common environment the mass of the resultant seeds did not differ significantly. Thus, Winn and Gross (1993)
concluded that (a) there was no evidence of genetic variation in seed mass and (b) the selection regime for seed mass was likely to be similar across latitudes.
In A. petiolata, seeds from Kentucky and Ohio were significantly larger than seeds from populations at the geographic periphery of the species' range. Furthermore, seeds from Ohio populations consistently germinated earlier and achieved greater overall germination than seeds from the other three regions. Seeds from two Kentucky populations (KY-5 and KY-6) had the lowest total germination and germinated ~2–3 wk later than Ohio seeds even though all of these populations had approximately the same mean seed mass. One possible explanation for these differences in seed mass and germination may involve the variable breeding system of A. petiolata. In a previous study, we noted the presence of more early- and late-aborted ovules and fewer mature seeds within Ohio fruits than in fruits from Tennessee, Kentucky, and Ontario sites (Susko and Lovett-Doust, 1998
). We speculated that the lower number of mature seeds in fruits from Ohio plants may have been the result of higher outcrossing rates than were seen in other populations of this predominantly autogamous species. In a subsequent study, morphometric analyses were performed on the flowers from Ohio and Ontario plants (Susko, 1998
). Both the absolute and relative distances separating stigmas from anthers were shown to be significantly greater in Ohio flowers than in those from Ontario. Previously, reduced stigma-anther separation was shown to be associated with reduced outcrossing in several species (Glover and Barrett, 1986
; Barrett and Shore, 1987
). Hence, such floral differentiation provides circumstantial evidence that Ohio plants may be performing more outcrossing than plants in other regions. Seeds from cross-pollinations often have greater fitness than those produced through selfing (Kalisz, 1989
; Hamilton and Mitchell-Olds, 1994
) and the greater vigor of Ohio seeds in the present study, illustrated by significantly higher overall germination and more rapid germination, may support the speculation that the Ohio seeds are more likely to be the products of outcrossing than are seeds from the other regions.
Among- and within-plant variation
Seed mass differed significantly both among and within plants. Similar to many studies of seed mass variation, the within-plant component of variance exceeded the among-plant component (Thompson, 1984
; Michaels et al., 1988
; McGinley, 1989
; Mehlman, 1993
; Obeso, 1993
; Méndez, 1997
; Vaughton and Ramsey, 1997
). It is likely that the among-plant variation in seed mass is the result of genetic differences among maternal plants, as well as environmental effects. Sources of maternal environmental effects could include microsite differences in temperature, light, water, and nutrient levels (Wulff, 1986a
; Roach and Wulff, 1987
; Gutterman, 1992
; Sills and Nienhuis, 1995
). For example, in the spring-flowering herb Hydrophyllum appendiculatum, plants grown in full sun produced heavier seeds than did plants grown in shade (Wolfe, 1995
). Similarly, in A. petiolata, plants growing in woodland openings produced heavier seeds than did plants in closed woodland habitats (D. Susko, unpublished data). Hence, spatial variability in light intensity in the forest understory may influence seed mass by affecting total available photosynthate to be partitioned among developing seeds. Byers and Quinn (1998)
reported that seed mass was lower in drier habitats at garlic mustard sites in New Jersey, so availability of moisture may also influence seed mass. Future research into among-plant differences in seed mass is needed, since the design of our study did not allow us to separate genetic and environmental components of seed size variation.
Within an infructescence, individual seed mass decreased from basal fruits to distal fruits. Furthermore, seed mass decreased within fruits from basal to distal seed positions. Similar patterns of declining seed mass (or size) with increased distance of fruits and seeds from the rachis have been reported often (Hurka and Benneweg, 1979
; Lee and Bazzaz, 1986
; Matthies, 1990
; Obeso, 1993
; see Lee, 1988
, for review). In a previous study, we found that the probability of maturing a seed decreased with increased distance of fruits and seeds from the plant axis or subtending leaves (Susko and Lovett-Doust, 1998
). We suggested that basal fruits within an infructescence and basal seeds within fruits behaved as stronger sinks for limited parental resources, such as nutrients and photosynthate, than did distal fruits and seeds, simply because of their proximity to vascular tissues. Thus, competition for limited resources may influence both the probability of maturing a seed, as well as the mass of those seeds that reach maturity.
Effects of seed position and mass on seedling traits
Lee (1988)
outlined two physiological models to explain fruit and seed production within plants. In both models the production of phytohormones by fruits and seeds mediated their ability to draw on parental resources. If the levels of growth regulators differ with respect to seed position on a plant, irrespective of the size of developing seeds, then perhaps seed position, per se, can affect seedling success. For instance, Wulff (1986a)
found that seed position within fruits of the perennial herb Desmodium paniculatum affected seedling survival. While seeds nearest the pedicel weighed significantly more than distal seeds, seedlings produced by the most distal seeds had a significantly higher probability of survival than did seedlings arising from basal seeds. We found that differences in seed mass, not seed position, accounted for most of the variation in the seedling traits that we studied; the only property that was associated with seed position (controlling for seed mass) was date of first-leaf emergence. Larger seeds from a representative population germinated later and gave rise to seedlings of greater mass than did smaller seeds. Such larger seedlings would presumably have a competitive advantage over smaller seedlings. In a troublesome adventive weed like garlic mustard, any management practice that reduced mean seed mass would likely lower seedling recruitment. Since seedlings in this study were harvested only a month after germination, we do not know whether any initial size differences would have persisted into adulthood. Other studies have shown that early differences in seedling size may disappear over time (e.g., Black, 1957
; Zimmerman and Weis, 1983
; Kromer and Gross, 1987
; Houssard and Escarré, 1991
). Also, it is unclear whether a large seed size would confer advantages to seedlings in the natural habitat of A. petiolata. Stanton (1984)
found in the wild radish, Raphanus raphanistrum, that large seeds, grown in a greenhouse experiment, were more likely to emerge, and produced more flowers as adults, than did small seeds. However, seed size had no effect on final plant size in a subsequent field experiment (Stanton, 1984
).
In a review of previous seed germination studies, Baskin and Baskin (1998)
summarized the effects of seed size on rate of germination and total percentage germination. They found that germination responses depended on the species investigated. Rate and percentage germination could increase, decrease, or remain unaffected by differences in seed size. In general, our study identified several possible advantages of producing small seeds in A. petiolata. Similar to such species as Cakile edentula (Zhang, 1993
) and Erodium brachycarpum (Stamp, 1990
), small seeds germinated earlier than large seeds. Stamp (1990)
attributed the earlier germination of small seeds to their greater access to water as a result of their higher surface to volume ratios. Hence, small seeds imbibed water faster and broke dormancy sooner. A more rapid uptake of water, as well as thinner seed coats, may be responsible for the earlier loss of dormancy in small seeds of A. petiolata. Small seed size may also influence early seedling growth and establishment. Hendrix et al. (1991)
found that the ratio of maximum root length to total leaf area of Pastinaca sativa seedlings was negatively related to seed mass at 10 and 20 d, but not at 30 or 40 d after emergence. These authors suggested that seedlings from small seeds may have a short-lived ability to better tolerate drought conditions, since plants with less leaf area per unit root should transpire less than seedlings from large seeds. In A. petiolata, small seeds produced seedlings that in the early stages of growth grew taller than did the seedlings arising from large seeds, due to the longer hypocotyls of the former. Consequently, early-emerging seedlings from small seeds may have an opportunity to overtop and shade later-emerging seedlings from large seeds, particularly in the dense clumps of even-aged seedlings typically found in garlic mustard populations (Susko, 1998
). In addition, one might expect small seeds to be more likely to emerge from soil burial at greater depths. This finding contrasts with the results of many seed burial studies, where large seeds were more likely to emerge from greater depths than small seeds (Harper and Obeid, 1967
; van der Valk, 1974
; Weller, 1985
; Wulff, 1986b
; Banovetz and Scheiner, 1994
). At present, we do not know why seedlings from small seeds grow taller, although varying phytohormone levels with seed size may be a factor. Like many weedy species, garlic mustard is frequently found at highly disturbed sites, where seed burial may be the norm rather than the exception. Thus, in terms of seed mass and the early stages of establishment in A. petiolata, bigger may not necessarily be better.
FOOTNOTES
1 The authors thank Jon Lovett-Doust, Paul Cavers, Jerry Baskin, Mike Weis, and an anonymous reviewer for valuable discussion and criticism of the manuscript. This work was supported by an NSERC Research Grant to LLD, and an NSERC Postgraduate Scholarship to DJS. 
2 Current address: Department of Crop Science, North Carolina State University, Raleigh, North Carolina 27695-7620.
3 Author for correspondence (b87{at}uwindsor.ca
).
LITERATURE CITED
Aarssen, L. W., and D. R. Taylor. 1992 Fecundity allocation in herbaceous plants.Oikos 65: 225–232. [CrossRef][ISI]
Ågren, J. 1989 Seed size and number in Rubus chamaemorus: between-habitat variation, and effects of defoliation and supplemental pollination. Journal of Ecology 77: 1080–1092. [CrossRef]
Anderson, R. C., and T. M. Kelley. 1995 Growth of garlic mustard (Alliaria petiolata) in native soils of different acidity. Transactions of the Illinois State Academy of Science 88: 91–96.
Baker, H. G. 1972 Seed weight in relation to environmental conditions in California. Ecology 53: 997–1010. [CrossRef][ISI]
Bannovetz, S. J., and S. M. Scheiner. 1994 The effects of seed mass on the seed ecology of Coreopsis lanceolata. American Midland Naturalist 131: 65–74.
Barrett, S. C. H., and J. S. Shore. 1987 Variation and evolution of breeding systems in the Turnera ulmifolia L. Complex (Turneraceae). Evolution 41: 340–354. [CrossRef][ISI]
Baskin, C. C., and J. M. Baskin. 1998 Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, New York, New York, USA.
Baskin, J. M., and C. C. Baskin. 1992 Seed germination biology of the weedy biennial Alliaria petiolata. Natural Areas Journal 12: 191–197.
Black, J. N. 1957 Seed size as a factor in the growth of subterranean clover (Trifolium subterraneum L.) under spaced and sward conditions. Australian Journal of Agricultural Research 8: 335–351. [CrossRef]
Byers, D. L., and J. A. Quinn. 1998 Demographic variation in Alliaria petiolata (Brassicaceae) in four contrasting habitats. Journal of the Torrey Botanical Society 125: 138–149. [CrossRef][ISI]
Cavers, P. B., M. I. Heagy, and R. F. Kokron. 1979 The biology of Canadian weeds. 35. Alliaria petiolata (M. Bieb.) Cavara and Grande. Canadian Journal of Plant Science 59: 217–229. [ISI]
———, and M. G. Steel. 1984 Patterns of change in seed weight over time on individual plants. American Naturalist 124: 324–335. [CrossRef][ISI]
Cruden, R. W., A. M. McClain, and G. P. Shrivastava. 1996 Pollination biology and breeding system of Alliaria petiolata (Brassicaceae). Bulletin of the Torrey Botanical Club 123: 273–280. [CrossRef][ISI]
Diggle, P. K. 1995 Architectural effects and interpretation of patterns of fruit and seed development. Annual Review of Ecology and Systematics 26: 531–552. [CrossRef][ISI]
Dolan, R. W. 1984 The effect of seed size and maternal source on individual size in a population of Ludwigia leptocarpa (Onagraceae). American Journal of Botany 71: 1302–1307. [CrossRef][ISI]
Glover, D. E., and S. C. H. Barrett. 1986 Variation in the mating system of Eichhornia paniculata (Spreng.) Solms (Pontederiaceae). Evolution 40: 1122–1131. [CrossRef][ISI]
Gutterman, Y. 1992 Maternal effects on seeds during development. In M. Fenner [ed.], Seeds: the ecology of regeneration in plant communities, 27–59. CAB International, Wallingford, UK.
Hamilton, M. B., and T. Mitchell-Olds. 1994 The mating system and relative performance of selfed and outcrossed progeny in Arabis fecunda (Brassicaceae). American Journal of Botany 81: 1252–1256. [CrossRef][ISI]
Harper, J. L., P. H. Lovell, and K. G. Moore. 1970 The shapes and sizes of seeds. Annual Review of Ecology and Systematics 1: 327–356.
———, and M. Obeid. 1967 Influence of seed size and depth of sowing on the establishment and growth of varieties of fiber and oil seed flax. Crop Science 7: 527–532.
———, and E. J. Trapp. 1992 Population demography of Pastinaca sativa (Apiaceae): effects of seed mass on emergence, survival, and recruitment. American Journal of Botany 79: 365–375. [CrossRef][ISI]
Hendrix, S. D., E. Nielsen, T. Nielsen, and M. Schutt. 1991 Are seedlings from small seeds always inferior to seedlings from large seeds? Effects of seed biomass on seedling growth in Pastinaca sativa L. New Phytologist 119: 299–305. [CrossRef][ISI]
Hossaert, M., and M. Valéro. 1988 Effect of ovule position in the pod on patterns of seed formation in two species of Lathyrus (Leguminosae: Papilionoideae). American Journal of Botany 75: 1714–1731. [CrossRef][ISI]
Houssard, C., and J. Escarré. 1991 The effects of seed weight on growth and competitive ability of Rumex acetosella from two successional old-fields. Oecologia 86: 236–242. [CrossRef][ISI]
Hurka, H., and M. Benneweg. 1979 Patterns of seed size variation in populations of the common weed Capsella bursa-pastoris (Brassicaceae). Biologisches Zentralblatt 98: 699–709. [ISI]
Janzen, D. H. 1977 Variation in seed size within a crop of a Costa Rican Mucuna andreana (Leguminosae). American Journal of Botany 64: 347–349. [CrossRef][ISI]
Kalisz, S. 1989 Fitness consequences of mating system, seed weight, and emergence date in a winter annual, Collinsia verna. Evolution 43: 1263–1272.
Kelly, C. K. 1996 Seed mass, habitat conditions and taxonomic relatedness: a re-analysis of Salisbury (1974). New Phytologist 135: 169–174. [CrossRef][ISI]
Kromer, M., and K. L. Gross. 1987 Seed mass, genotype, and density effects on growth and yield of Oenothera biennis L. Oecologia 73: 207–212. [CrossRef][ISI]
Lee, T. D. 1988 Patterns of fruit and seed production. In J. Lovett-Doust and L. Lovett-Doust [eds.], Plant reproductive ecology: patterns and strategies, 179–202. Oxford University Press, New York, New York, USA.
———, and F. A. Bazzaz. 1986 Maternal regulation of fecundity: non-random ovule abortion in Cassia fasciculata Michx. Oecologia 68: 459–465. [CrossRef][ISI]
Lord, J. M. 1994 Variation in Festuca novae-zelandiae (Hack.) Cockayne germination behaviour with altitude of seed source. New Zealand Journal of Botany 32: 227–235. [ISI]
Matthews, G. J., and R. Morrow, Jr. 1985 Canada and the World, an Atlas Resource. Prentice-Hall Canada Inc., Scarborough, Ontario, Canada.
Matthies, D. 1990 Plasticity of reproductive components at different stages of development in the annual plant Thlaspi arvense L. Oecologia 83: 105–116. [CrossRef][ISI]
Mazer, S. J. 1986 Parental effects upon components of seed development and seed yield in Raphanus raphanistrum: implications for natural and sexual selection. Evolution 41: 355–371. [CrossRef][ISI]
McGinley, M. A. 1989 Within and among plant variation in seed mass and pappus size in Tragopogon dubious. Canadian Journal of Botany 67: 1298–1304.
———, D. H. Temme, and M. A. Geber. 1987 Parental investment in offspring in variable environments: theoretical and empirical considerations. American Naturalist 130: 370–398. [CrossRef][ISI]
McKee, J., and A. J. Richards. 1996 Variation in seed production and germinability in common reed (Phragmites australis) in Britain and France with respect to climate. New Phytologist 133: 233–243. [CrossRef][ISI]
McWilliams, E. L., R. Q. Landers, and J. P. Mahlstede. 1968 Variation in seed weight and germination in populations of Amaranthus retroflexus L. Ecology 49: 290–296. [CrossRef][ISI]
Mehlman, D. W. 1993 Seed size and packaging variation in Baptisia lanceolata (Fabaceae). American Journal of Botany 80: 735–742. [CrossRef][ISI]
Méndez, M. 1997 Sources of variation in seed mass in Arum italicum. International Journal of Plant Sciences 158: 298–305.
Michaels, H. J., M. F. Willson, B. Benner, R. I. Bertin, A. P. Hartgerink, T. D. Lee, and S. Rice. 1988 Seed size variation: magnitude, distribution, and ecological correlates. Evolutionary Ecology 2: 157–166. [CrossRef]
Navarro, L. 1996 Fruit-set and seed weight variation in Anthyllis vulneraria subsp. vulgaris (Fabaceae). Plant Systematics and Evolution 201: 139–148. [CrossRef][ISI]
NOAA. 1974 Climate of the States, vol. 1, Eastern States. Officials of the National Oceanic and Atmospheric Administration, U.S. Department of Commerce. Water Information Center, Port Washington, New York, New York, USA.
Obeso, J. R. 1993 Seed mass variation in the perennial herb Asphodelus albus: sources of variation and position effect. Oecologia 93: 571–575. [CrossRef][ISI]
Reich, P. B., J. Oleksyn, and M. G. Tjoelker. 1994 Seed mass effects on germination and growth of diverse European Scots pine populations. Canadian Journal of Forest Research 24:306–320.
Roach, D. A., and R. D. Wulff. 1987 Maternal effects in plants. Annual Review of Ecology and Systematics 18: 209–235.
Rocha, O. J., and A. G. Stephenson. 1990 Effect of ovule position on seed production, seed weight, and progeny performance in Phaseolus coccineus L. (Leguminosae). American Journal of Botany 77: 1320–1329. [CrossRef][ISI]
Salisbury, E. J. 1942 The reproductive capacity of plants. G. Bell and Sons, London, UK.
Samson, D. A., and K. S. Werk. 1986 Size-dependent effects in the analysis of reproductive effort in plants. American Naturalist 127: 667–680. [CrossRef][ISI]
SAS. 1985 SAS user's guide: statistics, version 6. SAS Institute, Cary, North Carolina, USA.
Schaal, B. A. 1980 Reproductive capacity and seed size in Lupinus texensis. American Journal of Botany 67: 703–709.
Sills, G. R., and J. Nienhuis. 1995 Maternal phenotypic effects due to soil nutrient levels and sink removal in Arabidopsis thaliana (Brassicaceae). American Journal of Botany 82: 491–494. [CrossRef][ISI]
Smith, C. C., and S. D. Fretwell. 1974 The optimal balance between size and number of offspring. American Naturalist 108: 499–506. [CrossRef][ISI]
Stamp, N. E. 1990 Production and effect of seed size in a grassland annual (Erodium brachycarpum, Geraniaceae). American Journal of Botany 77: 874–882. [CrossRef][ISI]
Stanton, M. L. 1984 Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 65: 1105–1112. [CrossRef][ISI]
Stöcklin, J., and P. Favre. 1994 Effects of plant size and morphological constraints on variation in reproductive components in two related species of Epilobium. Journal of Ecology 82: 735–746.
Susko, D. J. 1998 The ovule ecology of garlic mustard, Alliaria petiolata (Brassicaceae), and other mustard species. Ph.D. dissertation, Department of Biological Sciences, University of Windsor, Windsor, Ontario, Canada.
———, and L. Lovett-Doust. 1998 Variable patterns of seed maturation and abortion in Alliaria petiolata (Brassicaceae). Canadian Journal of Botany 76:1677–1686.
SYSTAT. 1992 Statistics, version 5 edition. SYSTAT, Evanston, Illinois, USA.
Tabachnick, B. G., and L. S. Fidell. 1996 Using multivariate statistics, 3rd ed.. HarperCollins College Publishers, New York, New York, USA.
Temme, D. H. 1986 Seed size variability: a consequence of variable genetic quality among offspring? Evolution 40: 414–417. [CrossRef][ISI]
Thompson, J. N. 1984 Variation among individual seed masses in Lomatium grayi (Umbelliferae) under controlled conditions: magnitude and partitioning of the variance. Ecology 65: 626–631. [CrossRef][ISI]
van der Valk, A. G. 1974 Environmental factors controlling the distribution of forbs on coastal foredunes in Cape Hatteras National Seashore. Canadian Journal of Botany 52: 1057–1073. [CrossRef]
Vaughton, G., and M. Ramsey. 1997 Seed mass variation in the shrub Banksia spinulosa (Proteaceae): resource constraints and pollen source effects. International Journal of Plant Sciences 158: 424–431. [CrossRef]
Venable, D. L., and J. S. Brown. 1988 The selective interactions of dispersal, dormancy and seed size as adaptations for reducing risk in variable environments. American Naturalist 131: 360–384. [CrossRef][ISI]
Weis, I. M. 1982 The effects of propagule size on germination and seedling growth in Mirabilis hirsuta. Canadian Journal of Botany 60: 1868–1874.
Weller, S. G. 1985 Establishment of Lithospermum caroliniense on sand dunes: the role of nutlet mass. Ecology 66: 1893–1901. [CrossRef][ISI]
Winn, A. A. 1991 Proximate and ultimate sources of within-individual variation in seed mass in Prunella vulgaris (Lamiaceae). American Journal of Botany 78: 838–844. [CrossRef][ISI]
———, and K. L. Gross. 1993 Latitudinal variation in seed weight and flower number in Prunella vulgaris. Oecologia 93: 55–62.
Wolfe, L. 1992 Why does the size of reproductive structures decline through time in Hydrophyllum appendiculatum (Hydrophyllaceae)? Developmental constraints vs. resource limitation. American Journal of Botany 79: 1286–1290. [CrossRef][ISI]
———. 1995 The genetics and ecology of seed size variation in a biennial plant, Hydrophyllum appendiculatum (Hydrophyllaceae). Oecologia 101: 343–352. [CrossRef][ISI]
Wulff, R. D. 1986a Seed size variation in Desmodium paniculatum I. Factors affecting seed size. Journal of Ecology 74: 87–97. [CrossRef]
———. 1986b Seed size variation in Desmodium paniculatum II. Effects on seedling growth and physiological performance. Journal of Ecology 74: 99–114. [CrossRef][ISI]
Yanful, M., and M. A. Maun. 1996 Effects of burial of seeds and seedlings from different seed sizes on the emergence and growth of Strophostyles helvola. Canadian Journal of Botany 74: 1322–1330.
Zhang, J. 1993 Seed dimorphism in relation to germination and growth of Cakile edentula. Canadian Journal of Botany 71: 1231–1235.
Zimmerman, J. K., and I. M. Weis. 1983 Fruit size variation and its effects on germination and seedling growth in Xanthium strumarium. Canadian Journal of Botany 61: 2309–2315.
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= 0.01 are indicated with an asterisk. The results of Tukey-Kramer tests (within columns) are indicated by different superscripts where values differ significantly at P < 0.05
