fate of seeds in the soil
Seed survival and seed bank size can depend on seed burial and habitat conditions, seed age and density, seed predation, and on factors, such as herbivory, that affect seed inputs (reviewed in Baskin & Baskin 1998). We were interested in sunflower seed survival under natural conditions when seeds land on the soil surface, as well as the maximum survival that might occur with burial and low predation. For the latter, we felt that the 25-cm burial should represent a high level of seed persistence as predation should be further reduced by the packet. At this depth there was no light penetration, which enhances germination in H. annuus (Baskin & Baskin 1988), and Teo-Sherrill (1996) found no seedlings emerged from seeds of H. annuus buried 12.5–22.5 cm deep. Our seed survival results were often dependent on the year the experiment was established; in buried packets, plots established in 1999 still had, on average, 47% of the seeds remaining after 4 years, while the plots established in 2000 had only 16% of the seeds remaining after just 3 years. As expected, seed persistence on the soil surface was much lower than in the burial plots, given the high probability of germination, exposure to predation and exposure to more variable conditions (potential seed damage due to wetting and drying). Eight per cent of the seeds persisted for 4 years in the plots initiated in 1999 and fewer than 2% for 2 years in the plots set up in 2000.
Replication of the entire experiment in two different years provided surprising results. The observation that seed survival was often lower in the plots established in 2000 compared with those initiated in 1999 (whether considering calendar year or the age of the seeds) cannot be explained by yearly weather variation. The two sets of plots were adjacent to each other and only slightly different in topography (with the 2000 plots slightly lower), but the sites could still differ in abiotic or biotic factors that affect seed survivorship. Alternatively, the seeds used in 2000 may have had inherently lower survivorship than those in the 1999 cohort. Other studies have shown that seeds collected at different times or under different conditions can differ in characteristics that affect germination and dormancy (Cresswell & Grime 1981; Baskin & Baskin 1998; Qaderi et al. 2002). As we had no a priori reason to expect the observed differences in survival between the 1999 and 2000 plots, we lack the data on seed mass or other traits needed to test for seed quality differences.
The presence of litter on the soil surface reduced seed germination (or early survival of seedlings after emergence) in the first year, as has been found for other species (Jutila & Grace 2002) but, surprisingly, had no effect on numbers of viable seed. Litter may have made it more difficult for seeds to germinate while increasing seed predation, thus leading to no difference in numbers of seeds persisting in the soil. We do not understand why seedling numbers were higher in the presence of litter in the second year. However, this result may simply reflect differences in treatments in the number of remaining seeds available for germination; effects of litter on seedling emergence are often reported (e.g. Hamrick & Lee 1987).
Although seed survival data are often presented as log-linear seed-decay curves (see Lonsdale 1988; Rees & Long 1993; Rees 1997 for critiques), many population dynamic models require estimates of yearly seed survival (Kalisz & McPeek 1992, 1993; Jordan et al. 1995). Our study (Tables 1 and 2) highlights both the various ways that yearly seed survival can be estimated and the range of possible values. We agree with Teo-Sherrill (1996) that presenting a single average value across all experiments and years can be misleading. In addition to variation in survival due to year of establishment (plots initiated in 1999 vs. 2000) and environmental effects, an additional reason for heterogeneity in estimates is that seed sieving is destructive, and thus sampling errors are likely because some estimates use data collected in different subplots (Lonsdale 1988). Seed attrition was often reduced in the later years in the study (Figs 1 and 2). Such variation could indicate age-specific survival differences; for example Rees & Long's (1993) review illustrates that a Type III survivorship curve occurs for many composites. However, as noted by Rees (1997), the conditions experienced by the seeds are likely to change over the course of an experiment, making it difficult to test for age-specific survival. In our study, higher survival of seeds in the later years could result from any combination of differences due to age-specific seed mortality, density-dependent seed mortality (as fewer seeds are present in later years) or habitat-specific seed mortality (the habitat changed from tilled soil to a grass/forb mixture). Regardless of the exact cause, these data suggest that seeds that persist for more than 1 year after dispersal often have a greater probability of also persisting to future years.
It was unfortunately not feasible to carry out the seed survival study at the Clinton site, or the field experiment at KSR. We can note, however, that other studies of dormancy in wild sunflower seeds are roughly comparable with ours. For example, Teo-Sherill's (1996) report of 20% survival after 2.5 years for seeds of H. annuus buried 2.5–22.5 cm is similar to our 2000 results, although the two studies differ in both exact burial depth and in the presence of a mesh barrier in our studies. Similarly, our results are generally consistent with Toole & Brown's (1946) summary of Duvel's experiment, which reports that, depending on burial depth, 45–67% of seeds of H. annuus survived for 1 year. One report, the Burnside et al. (1981) buried seed experiment (at 23 cm depth), which revealed only 1–2% annual germination of wild sunflower, does differ greatly from our study. However, as Teo-Sherrill (1996) suggested, the low germination reported by Burnside et al. (1981) is misleading as tetrazolium tests of viability were not performed on exhumed seeds and seeds were tested in November (at a time when they would be intrinsically dormant). It is interesting that Burnside et al. (1996) found that 3% of the seeds from a 20-cm depth could germinate after 17 years of burial, suggesting that some seeds can persist for many years. However, the methodology used was the same as in the earlier study, complicating interpretations.
contribution of previous year's seed vs. the older seed bank to numbers of plants present
Seed fate studies, like those described above, show how long seeds persist but do not provide information on the ecological significance of seed bank survival for plant population biology. By comparing numbers of plants in manipulated sites where the previous year's seeds were, or were not, allowed to disperse, the role of the seed bank in the population may be inferred. From Table 3, we estimate that approximately 23% of the seedlings under the seed dispersal plants have their origins in the seed bank (an average of 41 seedlings are found in April even without seed dispersal and are likely to be among the 179 at sites with seed dispersal). Numbers of seedlings changed from April to May, with an unexpected decrease in the numbers found in plots without seed dispersal and increases in numbers in plots with seed dispersal, such that only a 10.4% seed bank contribution would be estimated from the May data. Our estimates of seed bank contributions are roughly consistent with the average number of seeds sieved from the soil at the site. For example, a mean of 41 seedlings from the seed bank would suggest 25% emergence for the estimated average of 163 seeds present in the 1-m radius area; this is of the same order of magnitude as emergence percentages found at the KSR site. However, the small number of seeds sampled in the soil and the fact that soil seed banks often have a patchy distribution (Benoit et al. 1992) makes it difficult to interpret estimates of average seeds per square cm of soil.
In contrast to our expectations, we found that soil disturbance had no significant effect on our results. Most likely, the relatively low vegetation cover at the site (bare soil was easily visible) reduced the impact of our manipulation. However, the presence or absence of seed dispersal in the previous year did alter the numbers of sunflowers at local sites. Specifically, prevention of seed dispersal, on average, reduced total numbers of seedlings, mature plants and subsequent heads at the local sites. The largest treatment effect was found for seedling counts, with a substantially reduced effect on number of mature plants and head production. The most likely explanation for this reduction in treatment effects with plant development is the presence of density-dependent processes and the considerable plasticity of H. annuus growth. As shown in Fig. 3, plots with high numbers of seedlings did not necessarily produce correspondingly more mature plants and heads, as compared with plots with fewer seedlings. Thus, at low-density seedling sites (usually without seed dispersal from the previous year), plants had, on average, a greater probability of summer survival and greater average head production on a per plant basis, relative to high-density seedling sites.
Results of the study at the Clinton site could have been quite different in a site with more ground cover. In that case, the presence or absence of a disturbance treatment is likely to have determined whether seed emerged from the seed bank. Unfortunately, we rarely know the vertical distribution of seeds in the soil, which has a large effect on how disturbance regimes are likely to affect seedling emergence from the seed bank (Mohler 1993). Further, plants at our sites in 2000 produced large numbers of heads; a similar study with smaller plants could have led to different results, as density dependence might be less pronounced at lower seed densities.
Our results are consistent with those from studies of annual plants that persist despite reproductive failure the previous year (Baskin & Baskin 1975, 1980). Recovery from the seed bank can be dramatic: a population of Sedum pulchellum that resulted from a seed bank had a density of 5.6 plants dm−2 (Baskin & Baskin 1980) and germination of buried seed produced a population of the annual Isanthus brachiatus comparable in size with those found in nearby habitats where seed production had occurred the previous year (Baskin & Baskin 1975). Rogers & Hartnett (2001) found seed rain to be of low importance in seedling recruitment in a tallgrass prairie. In contrast, seed dispersal was very important and seed bank contributions were negligible in two other grassland studies (Bullock et al. 1994; Edwards & Crawley 1999a). Peart (1989) estimated that, for the grass Vulpia bromoides, only 3% of the seedlings were a result of recruitment from the seed bank.
The experimental methods used to estimate seed bank vs. seed rain contributions under field conditions have potential drawbacks. For example, Peart (1989) estimated seed bank contributions by counting the number of grass seedlings appearing in seed exclosures that prevented seed fall. For some species, seedling establishment was higher in the exclosure than in the surrounding area, suggesting artifactual effects of exclosures may have inadvertently increased seedling emergence. In our study, it is possible that long-distance seed dispersal may have accounted for some of the seedlings emerging in sites where we clipped all the heads off the plants. In other studies seed bank contributions are determined by comparing numbers of seedlings in control sites with those in sites where field soil is either sterilized or replaced with other soil that lacks seeds (Bullock et al. 1994; Edwards & Crawley 1999a; Rogers & Hartnett 2001). In such studies, it is possible that the control and experimental treatments may have different seed germination conditions. However, there are many advantages to using natural seed banks and natural seed dispersal. It is difficult to create realistic experimental seed banks because the spatial patchiness and seed density are rarely known, and natural seed rain from plants is likely to lead to different seed dispersal patterns than treatments where seed is sown by researchers.
Data on seed bank size can be useful for interpretations of field experiments. In Edwards and Crawley's (1999a) study, for example, virtually all seedling recruitment was a result of recent seed dispersal. The fact that the community composition of the seed bank was unrelated to the established vegetation reinforces their conclusions. On a population level, Cabin & Marshall (2000) and Cabin et al. (2000) concluded that high seed production of the above-ground plants of a desert annual did not necessarily lead to a large number of seeds entering the seed bank, and that seed bank size was more related to the time between seed inputs into the seed bank and to seed survival rather than to the actual seed production at a particular time. In our study, we did take soil samples. However, in retrospect, they were inadequate to provide a detailed view of seed bank size, presumably because of the patchy nature of seeds in the soil. Given the difficulty of sieving large quantities of seeds, there are advantages to considering Naylor's (1972) mark-recapture technique for evaluating the contribution of recently produced seeds vs. buried seeds to numbers of seedlings.
In most studies of the role of the seed bank, collection of data is stopped after plants reach the seedling stage (e.g. Putwain et al. 1968; Peart 1989; Bullock et al. 1994; Edwards & Crawley 1999a; Rogers & Hartnett 2001). However, the contribution of seeds from the seed bank to numbers of seedlings and their contribution to the final reproductive output of the patch may not be the same. For example, because of density-dependent processes, our study showed a much larger effect of recent seed production on numbers of seedlings in the spring than on head production the following fall. Similar results have occurred in studies of herbivore and pathogen effects on plants. For instance, several studies have shown a strong effect of seedling pathogens or seed predators on numbers of seedling (Edwards & Crawley 1999b; Alexander & Mihail 2000; Cummings & Alexander 2002). However, in these same studies, the effect of the presence of the seed consumers on reproductive output of the patch is much less than expected based on their effects on seedling numbers. Instead, the low-density plant populations that occur in treatments with the seed consumer have reduced intraspecific competition and thus greater per-capita seed production than in treatments without the seed consumer.
In addition to field experiments examining the contribution of the seed bank to numbers of plants in a population (like at our Clinton site), a powerful approach is to create population models that explore the effect of the seed bank. Studies of the variability in seed survival under different conditions, like at the KSR site, are important for parameter estimation in such models. An excellent example is the work by Kalisz (1991) and Kalisz & McPeek (1992, 1993) who incorporated experimental data on seed bank persistence into demographic models of the herbaceous plant Collinsia verna. Simulated populations with a seed bank (compared with those without) grew faster and had an increased time to extinction coupled with a decreased likelihood of extinction. A community-level study (Stöcklin & Fischer 1999), where species with long-lived seeds had a lower probability of extinction in grassland remnants followed for 35 years, supported their findings. Kalisz & McPeek's (1993) results depended on the degree of predictability of environmental regimes. For sunflowers in the Great Plains, yearly variation in the abiotic environment and in population size is common. For example, numbers of sunflowers in western Nebraska vary greatly between years, presumably as a result of variation in environmental conditions (240 100 plants were found on a 28-km roadside survey in 2001; only 6720 were found on the same route in 2002, a year with an extreme drought; D. Pilson, unpublished data). Seed banks are likely to contribute to the persistence of the species in such variable environments.