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Article

Soil Seed Bank of Alien and Native Cornus (Cornaceae) Taxa in Lithuania: What Determines Seed Density and Vertical Distribution in Soil?

by
Lukas Petrulaitis
*,
Valerijus Rašomavičius
,
Domas Uogintas
and
Zigmantas Gudžinskas
Institute of Botany, Nature Research Centre, Žaliųjų Ežerų Str. 49, 12200 Vilnius, Lithuania
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(6), 488; https://doi.org/10.3390/d14060488
Submission received: 11 May 2022 / Revised: 9 June 2022 / Accepted: 14 June 2022 / Published: 15 June 2022
(This article belongs to the Special Issue Invasive Alien Plant Species: Encroachment Mechanisms, Impact on Soils, Environment and Ecosystem Services)
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Abstract

:
Soil seed banks of alien plant species are sources of propagules that play a crucial role in plant population dynamics. Studies on seed banks of woody alien species are crucial for understanding mechanisms of their encroachment on natural habitats. This study aimed to compare vertical distribution, density and composition of seed banks formed by native Cornus sanguinea subsp. sanguinea and alien C. alba, C. sericea and C. sanguinea subsp. australis in the Southern Hemiboreal zone of Europe. Five sites for each of four taxa were selected for the study, and seeds were sampled using the soil core method (400 samples in two soil layers: the upper, 0–5 cm, and the lower, 5–10 cm). Extracted seeds were tested with tetrazolium chloride stain to assess their viability. Differences in the seed banks among taxa were compared using generalised linear mixed models (GLMM). The GLMM analysis revealed significant differences in soil seed bank densities in the upper soil between the studied taxa (p < 0.001). We found that two of the alien taxa (C. alba and C. sanguinea subsp. australis) formed a much denser seed bank containing more viable seeds than the native Cornus sanguinea subsp. sanguinea. All three alien species contained more viable seeds (from 40.7% to 45.2% in the upper soil layer) than the native C. sanguinea subsp. sanguinea (19.4% in the upper and 18.2% in the lower soil layer). The cover of Cornus and habitat type had no significant effect on the density of the seed bank, according to GLMM. This study supports the hypothesis that seed banks of alien C. alba and C. sanguinea subsp. australis are denser than those of native C. sanguinea subsp. sanguinea. Furthermore, the seed bank of alien taxa contained more viable seeds than the seed bank of C. sanguinea subsp. sanguinea. Results of this study contribute to the understanding of the invasiveness of alien Cornus taxa.

1. Introduction

Seed ecology, and specifically seed bank density and viability of seeds, are important determinants of plant competitive performance [1]. The soil seed bank in various habitats or certain plant species has been recognised as an essential element of plant ecology [2,3,4]. Soil seed banks are important in the conservation and management of endangered and invasive species and the restoration of habitats and plant communities [1,5,6].
Traditionally, a soil seed bank was classified as either transient, containing seeds that remained viable in the soil for less than a year, or persistent, including seeds that remained viable for more than a year [7]. However, the classification of soil seed banks has changed over the years, and the various types of soil seed banks have been defined [8]. The most widely accepted division of seed banks is into transient and persistent seed banks, which are further subdivided into two groups. A soil seed bank consisting of seeds that remain viable in the soil for more than one year, but less than five years, is recognised as a short-term persistent seed bank, whereas seed banks containing seeds that are viable for five or more years are recognised as long-term persistent seed banks [3,8]. The persistence of viable seeds in a soil seed bank depends on species’ biological traits and environmental factors [9,10]. A high number of viable seeds in a seed bank can sustain the longevity and dynamics of a population, providing successful seedling emergence and recruitment [6].
Studies of the soil seed bank of an alien plant species can provide information on the invasiveness of a species in certain areas [11,12]. Masaki et al. [13] emphasised that the formation of persistent long-term seed banks could be advantageous for woody species in terms of colonising disturbed sites, especially for species whose recruitment depends on irregular habitat disturbances. The results of some studies suggest that the seeds of invasive plants tend to be better adjusted for survival in soil compared with native species [14]. Seed banks of invasive woody legumes (Acacia, Cytisus, Genista, etc.) have been studied extensively [1,15,16,17], whereas seed banks of fleshy-fruited woody species received much less attention [18,19,20]. Recent studies have revealed that alien woody plant species form denser soil seed banks in the invaded range than in their native ranges [21]
When seeds reach the soil and enter the seed bank, they gradually lose their germination potential, especially if they are short-lived [22]. Moreover, seeds may be affected by animals and microorganisms, which can influence their viability and survival in soil [23]. The proportions of damaged, intact, non-viable and viable seeds in soil seed banks show the relationship between seed input into the soil seed bank and its depletion [24,25]. On the other hand, the proportion of damaged, non-viable and viable seeds also gives some indication of the type of seed bank [26].
Most fleshy-fruited shrubs, including Cornus L., form transient seed banks [27]. However, studies on C. controversa Hemsl. suggest different patterns of seed persistence, as they remain viable in the soil for up to ten years [13]. Although the seed bank of C. sanguinea has been classified as transient since the seeds were found to be viable for less than a year [3], recent studies have revealed that seeds of this species can remain viable for at least three years under certain storage conditions [28]. Thus, these results suggest that seed banks of C. sanguinea could be treated as short-term persistent. Information on the seed banks of other species of the genus Cornus, including the widespread and invasive C. alba L. and C. sericea L., is almost unavailable [29,30]. In contrast, information on the seed bank of C. sanguinea L. is fragmentary and is typically presented as a secondary output of ecological studies of the overall seed bank in specific habitats [27]. A very dense seed bank of C. sanguinea containing intact seeds was found in Germany; however, the proportion of viable seeds extracted from the soil samples was less than 1% of the total number of intact seeds [5]. Experiments with C. sanguinea from Central and South Europe have given different rates of fresh seed germination, ranging from 53.0% to 90.8% [27,31,32].
As a part of the study of the ecological performance of alien and native Cornus taxa in the Southern Hemiboreal zone of Europe, we aimed to analyse the soil seed bank of four Cornus taxa occurring in Lithuania (C. alba L., C. sericea L., C. sanguinea L. subsp. australis (C.A. Mey.) Jáv. and C. sanguinea L. subsp. sanguinea). In the study area, Cornus sanguinea subsp. sanguinea is native, whereas the other taxa are naturalised aliens [30,33,34]. Studies on the soil seed bank of woody species confirmed that they form denser seed banks in the alien range because of more significant seed production and lower seed predation than in the native range [21]. Therefore, we set out to test the hypothesis that alien Cornus taxa also form a denser seed bank than the native representatives of this genus. This study aimed to compare vertical distribution, density and composition of the seed bank formed by native and alien Cornus in the Southern Hemiboreal zone of Europe. In this study, we addressed the following questions: (a) What is the vertical distribution of seeds in the soil layers? (b) What is the seed density in the soil seed bank, and how does it differ between native and alien Cornus taxa? (c) What is the viability of seeds extracted from the soil seed bank?

2. Materials and Methods

2.1. Studied Taxa

Most species in the genus Cornus are well defined and can be easily recognised; however, the taxonomy of several groups of species is still a subject of discussion. The taxonomy of C. alba and C. sericea for a long time has been controversial. In some periods, they have been treated as a single species [35]; C. sericea has been merged with C. alba at the rank of subspecies [36]. However, recent studies have suggested that they are phylogenetically divergent sister species [37,38]. In this study, we accept the later view and treat C. alba and C. sericea as separate species. Cornus sericea is a potentially invasive species that penetrates into natural forests, wetlands and other habitats across Europe [29].
For the soil seed bank studies, we carefully selected populations of unambiguously identified C. alba, C. sericea, Cornus sanguinea subsp. sanguinea and C. sanguinea subsp. australis. Plants were determined according to their morphological characteristics. Cornus alba and C. sericea we distinguished by the shape of seeds. Cornus alba has stones ellipsoid and tapered to a flat base, whereas C. sericea stones are subglobose and rounded at the base [37,39]. Subspecies of the C. sanguinea are easily distinguished by the leaf indumentum. The lower leaf surface of C. sanguinea subsp. sanguinea is covered with simple erect hairs, whereas leaves of C. sanguinea subsp. australis are covered with strongly appressed medifixed hairs [33,40].
The studied taxa of the genus Cornus are shrubs or small trees. Cornus alba is native to the continental regions of temperate and boreal Eurasia and occurs in mesic and wet meadows, on forest edges and shrubby thickets along rivers, and often invades various anthropogenic habitats [33,34]. Cornus sericea originates from North America; in its natural range, it occurs from Alaska to California. It usually occupies relatively moist habitats such as wet meadows, riparian zones, lakeshores, wetlands and swamp alder woodlands, both in native and alien ranges [37,41]. Cornus sanguinea subsp. sanguinea is widely distributed over the temperate regions of Europe, whereas C. sanguinea subsp. australis is native to south-eastern Europe and West Asia [33,40].
Cornus sanguinea subsp. sanguinea and C. sanguinea subsp. australis grow in broadleaved woodlands, along forest margins, and on the slopes of hills and ravines with calcareous soil [27]. However, in the non-native range, C. sanguinea subsp. australis occurs in semi-natural or even anthropogenic habitats, where it later penetrates into natural habitats [30].

2.2. Study Sites

Populations of the Cornus taxa were selected throughout Lithuania depending on their distribution (Figure 1, Table 1). Five populations of each taxon (C. alba, C. sanguinea subsp. australis, C. sanguinea subsp. sanguinea and C. sericea) were selected, giving a total of 20 sites. Stands with a substantial presence of the mature Cornus individuals in the shrub layer (with coverage ranging from 30% to 60%) and occupying at least 50 m2 were selected for the seed bank sampling.
Voucher specimens from the studied populations were collected and deposited at the Herbarium of the Institute of Botany of the Nature Research Centre (BILAS) in Vilnius. As a result, habitat types were identified (applying the third level) and named following the EUNIS Habitat Classification [42] (Table 1).
Most study sites were selected from broadleaved deciduous forest (T1) habitats (10 sites). Five stands occurred in tree-dominated human-made habitats (V6), three in temperate and Mediterranean montane scrub (S3) and two in riverine and fen scrub (S9). For seed bank analysis among habitat types, we grouped seed bank data according to habitat types by higher level, such as scrub (S), forest (T) and vegetated human-made (V) habitats.

2.3. Sampling Procedures

Soil samples for the seed bank analysis at the Cornus sites we collected in late autumn, during October and November of 2019, following a recommendation by Csontos [43], when the fruits had fallen from the plants. Sampling plots were arranged in transects across the Cornus stand (the transect length was 12 m). The sampling plots in the transect were set with 0.5 m gaps, and 20 soil cores (hereafter referred to as samples) were collected using a steel frame with sides 10 × 10 cm and height 10 cm. We carefully removed organic matter (fallen leaves, withered grass, plant debris) from core sampling from each plot surface.
Each collected soil core was divided into two layers (hereafter referred to as subsamples): the upper 0–5 cm and the lower 5–10 cm layer. Collected soil cores were transferred to labelled bags (with an indication of the taxon name, locality and layer) and brought to the laboratory. In the laboratory, the soil samples were slightly shredded to prevent soil clumping and left to dry in opened bags for about three months at ambient temperature (ca. 20 °C).

2.4. Seed Bank Analysis

The dried soil subsamples were crushed by hand, and the seeds were separated using a set of soil sieves (mesh sizes 3, 2, 1 and 0.25 mm). The seeds of the Cornus from each subsample were picked with pincers and placed into separate labelled paper bags. These seeds were later analysed using a binocular microscope and divided into intact seeds (with no visual damage to the shell) and damaged seeds (with visible damage to the shell). Intact and damaged seeds from each subsample were counted. A total of 400 soil samples and 800 subsamples were analysed during this study.

2.5. Tests of Seed Viability

The viability of all intact seeds extracted from the soil seed bank was tested by applying a standard staining method (TTC-test) using a 1% solution of 2,3,5 triphenyl tetrazolium chloride in distilled water [4]. Before testing, seeds were scarified by cutting off the tip of each seed shell with a medicinal scalpel to expose the embryo to enable better and faster TTC solution penetration. Then, scarified seeds were placed into test tubes with TTC solution and kept in the dark at a temperature of 35 °C for 24 h. For an evaluation of the embryo colour, a cross-section of the seed was made. Embryos were considered viable if they had carmine staining; slightly pink or white embryos were supposed to be non-viable [44].

2.6. Statistical Analyses

For the analysis of the seed density, seed counts per subsample (0.01 m−2) were re-calculated to obtain mean seed density for a square metre of the study site (seeds 1 m−2). The seed bank data from five sites of each studied taxon were pooled to determine differences between taxa and soil layers.
The results of descriptive statistics include mean values and standard deviations (mean ± SD). The normality of the data distribution was evaluated using the Shapiro–Wilk test. Since all of the datasets for the seed banks were non-normally distributed, non-parametric tests were applied. The differences between the sample medians were assessed by applying the Kruskal–Wallis H-test, and Dunn’s z test was used for a post hoc pairwise comparison. The significance level of the statistical tests was set at p < 0.05. Differences in the proportions of intact seeds in the upper and lower soil layers between different taxa were assessed applying the chi-square (χ2) test. Tests and descriptive statistics were performed using PAST 4.06 software [45]. Comparing seed banks of different Cornus species, the generalised linear mixed model (GLMM) was applied. The number of seeds in a seed bank was included as a response variable, the taxon was considered as a fixed factor, while the site, the cover of Cornus and habitat type (at the first level of classification) were considered as random effects in the model. The models were built in R-project environment, version 4.1.1 [46], using glmmADMB package, version 0.8.0 [47].

3. Results

3.1. Vertical Seed Distribution

A total of 1183 seeds, including both intact and damaged seeds, were collected from soil samples at the Cornus alba study sites, 433 seeds at the C. sericea sites, 712 seeds at the C. sanguinea subsp. sanguinea sites and 1547 seeds at the C. sanguinea subsp. australis sites (Table 2). Most of the seeds were concentrated in the upper soil layer (0–5 cm), a trend observed for all taxa and at all study sites, however, with some quantitative differences between the studied taxa. At C. alba and C. sericea sites, 93.3% and 92.8%, respectively, of all seeds were found in the upper soil layer (Table 2), and no significant differences were revealed between these species (χ2 = 0.01, p = 0.93). It should be noted that no seeds were found in the lower soil layer at the Klaipėda site of C. sericea. The proportions of seeds in the upper soil layer at C. sanguinea subsp. sanguinea and C. sanguinea subsp. australis sites were 88.6% and 87.1%, respectively, and no significant differences were found between taxa (χ2 = 0.84, p = 0.36).
The highest percentage of damaged seeds (41.8%) in the upper soil layer was recorded at C. sericea, whereas at C. sanguinea subsp. australis damaged seeds comprised 23.5% of all seeds from this layer (Table 2). In the lower soil layer, the total number of seeds was significantly lower than in the upper soil layer, and a higher percentage of seeds were damaged than in the upper layer. The proportion of damaged seeds for all studied taxa was higher in the lower soil layer, except for C. alba (10.8%).
Most intact seeds were concentrated in the upper soil layer at all study sites (Table 2). However, significant differences were found between taxa concerning the absolute number of intact seeds. For example, at C. alba sites, 782 intact seeds were found in the upper soil layer, whereas at C. sericea sites, 234 intact seeds were found. At the sites of native C. sanguinea subsp. sanguinea, 430 intact seeds were extracted from the upper soil layer subsamples, whereas at C. sanguinea subsp. australis sites, 1030 intact seeds were found in this layer. In the lower layer, the number of intact seeds was low, but it was higher than the number of damaged seeds at the study sites of all taxa except C. sericea (Table 2).

3.2. Seed Bank Density

The highest mean density of seeds in the upper layer was found for C. sanguinea subsp. australis, whereas the lowest mean number of seeds was revealed at C. sericea sites (Figure 2). The same trend was recorded in the lower soil layer. The highest mean density of seeds in the lower soil layer occurred at C. sanguinea subsp. australis sites, whereas the lowest density was at C. sericea sites.
The number of intact seeds and their density in the upper soil layer (0–5 cm) varied greatly between the sites. The highest density of intact seeds in this layer was recorded at C. alba sites, whereas the lowest density of intact seeds was found at C. sericea sites (Table 3). The density of intact seeds at all pooled C. alba sites was significantly higher than at C. sericea sites (Dunn’s z = 7.62, p < 0.001). The largest variation in the mean density of intact seeds in the upper soil layer was recorded at C. sanguinea subsp. australis sites. The density of intact seeds at Cornus sanguinea subsp. australis sites was significantly higher than the density of intact seeds at Cornus sanguinea subsp. sanguinea sites (z = 4.11, p < 0.001). A significant difference in the intact seed density in the upper soil layer was found between all studied taxa by applying the Kruskal–Wallis H test (H = 75.35, p < 0.001). However, a pairwise comparison revealed no differences between C. alba and C. sanguinea subsp. australis sites (z = 1.02, p = 0.306).
The results of GLMM rejected the presumption of the locality effect, but confirmed that the studied taxa have a significant effect on seed bank density (Table 4). However, the density of seeds in the lower soil layer was affected by the locality in the case of Cornus alba and C. sanguinea subsp. australis. The coverage of Cornus taxa has no significant effect on seed bank density in the upper soil layer, but depended on the taxon (Table 5). In the lower soil layer, the density of seeds of Cornus alba and C. sanguinea subsp. australis was affected by the coverage of Cornus, whereas the density of C. sanguinea subsp. sanguinea and C. sericea seeds did not depend on the cover of the individuals.
The number of intact seeds in the lower soil layer (5–10 cm) was less variable (Table 6) than in the upper soil layer (Table 3). The lowest variation in the density of intact seeds was observed between C. sericea sites (Table 6). The density of intact seeds at pooled sites of C. alba was significantly higher than the density at C. sericea sites (z = 4.69, p < 0.001). The highest variation in the mean density of intact seeds in the lower soil layer was observed for the C. sanguinea subsp. australis sites. The density of intact seeds in the lower soil layer at C. sanguinea subsp. sanguinea sites was significantly lower than at C. sanguinea subsp. australis sites (z = 3.08, p = 0.002). Significant differences in the density of intact seeds in the lower soil layer between all studied sites of pooled taxa were found by applying the Kruskal–Wallis H test (H = 23.61, p < 0.001). However, a pairwise comparison revealed no differences between C. alba and C. sanguinea subsp. australis sites (z = 0.86, p = 0.390).
The results of GLMM revealed no significant effect of the habitat type on the seed bank density; however, as in other cases, it reliably depends on the studied taxa (Table 7). Most of intact seeds were detected in vegetated human-made habitats (V), whereas in forests and other wooded land (T), numbers of intact seeds were lower (Table 8).
Analysis of the habitat type effect on the number of intact seeds in the soil seed bank of individual taxa revealed different pattern of relationships. We found that the upper soil layer of C. sanguinea subsp. sanguinea occurring in temperate scrub habitats contains a significantly higher number of seeds than in broadleaved deciduous forest habitats (Dunn’s z = 4.30, p < 0.001). Different tendencies were observed at C. sanguinea subsp. australis sites. No significant differences were found between intact seed number in broadleaved deciduous forest and temperate scrub habitats (z = 1.10, p = 0.27), whereas significant differences in seed number were found between broadleaved deciduous forest and human-made habitats (z = 5.85, p < 0.001), as well as between temperate scrub and human-made (z = 4.50, p < 0.001) habitats. Thus, the number of intact seeds was higher in open or semi-open habitats than in woodland habitats. It was revealed that the pattern of intact seed density in the lower soil layer is the same as that in the upper soil layer (Table 8).

3.3. Seed Viability

After analysing the intact Cornus seeds, we found that viable seeds in the upper soil layer comprised between 8.6% and 80.1% of all intact seeds extracted from this layer at individual sites (Table 3). At C. alba sites, the density of viable seeds in the upper soil layer was lower than the density of non-viable seeds (Figure 3). The density of viable seeds in the seed bank of C. sericea sites was significantly lower than at the sites of other studied taxa. The proportion of viable seeds at the study sites of C. sericea ranged from 27.1% to 63.2% of the total number of intact seeds at the individual sites for this species.
At the sites of the native C. sanguinea subsp. sanguinea, viable seeds comprised from 8.6% to 28.6% of all intact seeds (Table 3). In contrast, at the sites of the alien C. sanguinea subsp. australis, the soil seed bank was significantly denser (z = 5.55, p < 0.001) and contained a higher proportion of viable seeds than at the sites of C. sanguinea subsp. sanguinea (χ2 = 16.97, p < 0.001). Viable seeds in the upper soil layer at the sites of C. sanguinea subsp. australis comprised from 9.1% to 80.1% of all intact seeds. It should be noted that C. sanguinea subsp. australis and C. alba were not significantly different from each other (z = 1.08, p = 0.280) in terms of the density of viable seeds in the upper soil layer.
The number of seeds in the lower soil layer (5–10 cm) was much lower than in the upper layer (0–5 cm). Nevertheless, the lower soil layer contained viable seeds at many study sites (Table 6). At C. alba sites, viable seeds comprised from 40.0% to 63.2% of all intact seeds recorded in this layer. At C. sericea sites, the density of viable seeds in the lower soil layer was significantly lower than at C. alba sites (z = 3.47, p < 0.001). At two sites of C. sericea, Juodlė and Žiežmariai, all intact seeds in the lower soil layer were viable, although their numbers were small.
At the sites of the native C. sanguinea subsp. sanguinea, the density of viable seeds in the lower soil layer was relatively low, and they comprised from 0% to 33.3% of all intact seeds (Table 6). Contrasting results were obtained from the analysis of the soil seed bank in the lower soil layer at the sites of alien C. sanguinea subsp. australis, where viable seeds comprised from 25.0% to 100% of all recorded intact seeds. The density of viable seeds in the lower soil layer was significantly different between C. sanguinea subsp. sanguinea and C. sanguinea subsp. australis (z = 4.62, p < 0.001); however, no significant differences were found between the density of viable seeds at C. sanguinea subsp. sanguinea and C. sericea (z = 0.20, p = 0.838) sites.

4. Discussion

4.1. Vertical Seed Distribution

Analysis of the vertical distribution of seeds of the four studied Cornus taxa in the soil showed that seeds were concentrated in the upper soil layer, with a much lower number of seeds found in the lower layer. The high concentration of seeds in the upper soil layer is characteristic of many plant species [2,21,24]. The biological characteristics of the species determine the vertical distribution of seeds in the soil, primarily seed production, seed shape and size [10,48,49]. In addition, environmental factors such as the mechanical composition of the soil [48], the thickness and nature of the plant debris layer [22], the type of habitat [7] and the activity of small vertebrates, invertebrates and micro-organisms [22,50] also have a significant influence on the distribution of seeds in the soil.
We found that the proportion of seeds in the lower soil layer was higher for C. sanguinea subsp. sanguinea and C. sanguinea subsp. australis than C. alba and C. sericea (Table 2). We assume that the different proportions of seeds in the soil layers were caused by the different shapes of the seeds of the studied Cornus taxa. The influence of seed shape on the depth of penetration into the soil has been confirmed by analysing the seeds of different plant species. It has been confirmed that round seeds of shrub Cytisus multiflorus (L’Hér.) Sweet can penetrate the deeper soil layers more easily since this shape reduces the friction [48]. The seeds of both subspecies of Cornus sanguinea are globular or subglobular, whereas the seeds of C. alba and C. sericea are laterally compressed [51].
At Šilinė and Vilnius sites, the seed banks of C. sanguinea subsp. sanguinea were studied within broadleaved deciduous forest habitats. We found exceedingly small numbers of seeds in the upper soil layer, and intact seeds were absent from the lower soil layer. The thick layer of dead leaves and other plant remnants accumulating in broadleaved forests probably hampered seed penetration to the deeper soil layers. Some authors have also found that the surrounding vegetation influences seed penetration into the soil [22]. The absence of seeds in the lower soil layer at the Klaipėda site of C. sericea was also related to the peculiarities of the habitat. The permanently damp soil of the Alnus glutinosa (L.) Gaertn. stand could, in our opinion, have interfered with the activities of small soil vertebrates and invertebrates, which have a significant influence on seed migration in the soil [22,49,50]. We observed rodent activity at other study sites of Cornus alba and C. sericea with mesic soils.

4.2. Density of the Seed Bank

The study results showed a dense seed bank in the soil at the sites of the studied four Cornus taxa. The density varied between sites of the same taxon as well as between taxa. The highest density of intact seeds in both soil layers was recorded for C. sanguinea subsp. australis, whereas the lowest density was in the soil of C. sericea sites. It is known that a high yield of fruits per individual positively correlates with the seed density in the seed bank [52]. Cornus alba and C. sericea usually flower and yield twice during the growing season [37,53] and can, therefore, be expected to contribute more to the seed bank than C. sanguinea, which tends to flower and yield fruit once a year [27]. Cornus alba and C. sericea also flowered twice during the growing season at the study sites in Lithuania, although the fruit set after the second flowering of C. sericea was poor. This may explain why the seed bank density of the C. sericea was significantly lower than that of C. alba. It has been found that frugivore birds are a factor affecting the density of the seed bank through the removal of fruits [54]. Studies on C. amomum Mill. and C. racemosa Lam. in the native range in North America have shown that their fruits are consumed faster than fruits of non-native Rhamnus cathartica L. and Rosa multiflora Thunb [55]. Fruits of Cornus amomum and C. racemosa share similar morphological traits (shape and colour) with C. alba and C. sericea. We presume that their seed bank density is also affected by the activity of frugivore birds.
By comparing the density of intact seeds in the seed bank of the native C. sanguinea subsp. sanguinea and of the alien C. sanguinea subsp. australis, we found that alien subspecies formed significantly denser seed banks than the native subspecies in both analysed soil layers. Nevertheless, at the Piepaliai and Liūnelis sites of C. sanguinea subsp. sanguinea, the density of intact seeds in the upper soil layer was the same or even higher than at the Šiauliai and Maišiagala sites of C. sanguinea subsp. australis. Habitat characteristics can probably explain these differences in seed density in the soil. At the Piepaliai and Liūnelis sites, C. sanguinea subsp. sanguinea occupied semiopen scrubland (S35) habitats and, therefore, produced higher fruit yield than occurring in broadleaved deciduous forest habitats (T1B and T1E). At the Šiauliai and Maišiagala sites, stands of C. sanguinea subsp. australis were comparatively young and, therefore, produced fewer seeds, though the density and coverage of individuals were almost the same as in C. sanguinea subsp. sanguinea stands.
Data on the density of the soil seed bank of the Cornus species are very limited, making it difficult to compare the data from this study with data from other regions. For example, according to the studies performed in Germany, the density of Cornus sanguinea subsp. sanguinea seeds in the soil range from 10 to 12 seeds m−2 in young mixed scrublands and from 64 to 320 seeds m−2 in mature scrublands and pine stand [27]. However, another study in Germany [5] has found a much higher seed density of intact seeds (1345 seeds m−2), which is significantly higher than what we found in Lithuania. Thus, the seed density of Cornus sanguinea subsp. sanguinea found in this study in most cases is considerably higher than those found in Germany. Still, the available information suggests that the density of the seed bank is strongly influenced by habitat conditions and characteristics of the stand. Unfortunately, we cannot make broader comparisons of the soil seed bank density formed by this subspecies and the other Cornus taxa studied, as we have not found such published data.

4.3. Viable Seeds

The highest density of intact seeds and the density of viable seeds were found at C. sanguinea subsp. australis sites; however, no significant difference was found between the density of viable seeds at its sites and sites of C. alba. The soil seed bank of these taxa contained significantly more viable seeds than alien C. sericea and native C. sanguinea subsp. sanguinea. It should be noted that both the lowest total seed bank density and the lowest density of viable seeds were recorded at the sites of C. sericea. Furthermore, the percentage of viable seeds of C. sericea at the individual study sites ranged from 11.8% to 100%, although the mean density of seeds in the soil was generally low.
Studies on C. sericea in Ireland have revealed a low seed set and absence of seedlings in the invaded habitats [41]. The study’s author supposed that the vegetative spread of C. sericea is the main means of reproduction in the invaded areas. We also suppose that seedlings of C. sericea play a secondary role in the renewal of its stands. In its native distribution area, the reported mean seed density of C. sericea in forest soil samples was low and comprised 26.1 seeds m−2. In addition, it is unclear whether the seeds in the seed bank were viable as they did not germinate under the experimental conditions [56]. Published data on the seed density and viability of C. sericea in the seed bank in the invaded range are absent.
The results of studies on seed viability of the other Cornus taxa are also quite challenging to interpret unambiguously, as the viability of the seeds was assessed by their germination rate. Studies performed in Germany on the viability of C. sanguinea subsp. sanguinea seeds extracted from the seed bank have revealed that only 0.89% of all intact seeds germinate. This study showed that the density of germinating seeds was 12 seeds m−2, in contrast to a total density of intact seeds of 1345 seeds m−2 [5]. Other studies assessing the germination rate of C. sanguinea subsp. sanguinea seeds have shown contrasting results. The germination rate of its seeds is 81.0% in a garden experiment. In contrast, in a different study conducted in Germany, the proportion of viable seeds ranged from 53.0% to 73.0% [27]. An experiment performed by Takos and Efthimiou [31] found a germination rate of 65.0% in the laboratory and 79.0% in field sowing. Germination of fresh C. sanguinea seeds of summer sowing was found to be 85.8% and 90.8% of autumn sowing [32]. The germination rate and viability of seeds extracted from the soil seed bank may differ significantly from the germination rate and viability of freshly collected seeds, as some of the seeds in the soil may be dormant or may have already lost germination because of age [22,57]. In addition, some authors have suggested that germination rates of C. sericea seeds, and possibly seeds of the other related Cornus species, depend on precipitation during seed formation and the origin of the sampled population. In the native distribution area of C. sericea, the germination rates of its seeds varied from 0–2% to 29–31% in 1984 and from 83–91% to 86–91% in the following year [58].
We found that only 19.4% of C. sanguinea subsp. sanguinea seeds extracted from the upper soil layer and 18.2% from the lower soil layer were viable. Thus, the seed viability rate was significantly lower than in other studied taxa and substantially lower than reported viability in other studies [5,27,31].
The seed bank of fleshy-fruited plants, including most Cornus species, is usually classified as transient or short-lived persistent [8,27]. However, some species prefer forest gaps, including representatives of the genus Cornus, forming extensive and long-term seed banks [13,59]. It has been found that seeds of C. controversa remain viable for more than ten years [13]. Thus, it cannot be excluded that the different seed viability observed in our study is also due to the different seed longevity of the taxa studied. Although seeds of C. sanguinea subsp. sanguinea are thought to remain viable for only one or two years and form transient seed banks [27], some studies suggest that they form a short-lived persistent seed bank [28]. As the soil seed bank of the studied Cornus taxa has a significant proportion of damaged and non-viable seeds, this ratio confirms the existence of an equilibrium between seed input into the soil seed bank and its depletion. The results of our study support the suggestion by other authors that they form a short-term persistent seed bank [24,26,27]. We, therefore, believe that the longevity, viability and germinability of the Cornus seeds should be tested in long-term seed burial experiments.
This research showed that the density of the seed bank formed by the studied Cornus taxa varied considerably between the study sites. Still, we also found significant differences in the density of seed banks between taxa. This study supported our hypothesis that most alien Cornus taxa form denser soil seed banks than native C. sanguinea subsp. sanguinea. We found that the seed bank of alien C. alba, C. sericea and C. sanguinea subsp. australis contained more viable seeds than the seed bank of native C. sanguinea subsp. sanguinea. We suppose that high density in a seed bank, especially when made up of viable seeds in the soil, contributes to the rapid spread of alien Cornus taxa in the southern part of the Hemiboreal zone of Europe.

Author Contributions

Methodology, L.P., V.R. and Z.G.; investigation, L.P. and Z.G.; data curation, L.P. and D.U.; writing-original draft preparation, L.P. and Z.G.; writing-review and editing, L.P., V.R., D.U. and Z.G.; visualisation, L.P., Z.G. and D.U.; supervision, V.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy concerns.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Location of the Cornus seed bank sampling sites in Lithuania. White dots—C. alba; black dots—C. sericea; black squares—C. sanguinea subsp. australis; white squares—C. sanguinea subsp. sanguinea.
Figure 1. Location of the Cornus seed bank sampling sites in Lithuania. White dots—C. alba; black dots—C. sericea; black squares—C. sanguinea subsp. australis; white squares—C. sanguinea subsp. sanguinea.
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Figure 2. Mean number of the intact Cornus seeds per square metre: (a)—upper layer (0–5 cm); (b)—lower layer (5–10 cm). Whiskers indicate standard deviation. Different letters above the whiskers indicate significant differences (p < 0.05) applying Dunn’s z-test. Abbreviations of taxa: Co_alb—Cornus alba; Co_ser—Cornus sericea; Co_san_san—Cornus sanguinea subsp. sanguinea; Co_san_aus—Cornus sanguinea subsp. australis.
Figure 2. Mean number of the intact Cornus seeds per square metre: (a)—upper layer (0–5 cm); (b)—lower layer (5–10 cm). Whiskers indicate standard deviation. Different letters above the whiskers indicate significant differences (p < 0.05) applying Dunn’s z-test. Abbreviations of taxa: Co_alb—Cornus alba; Co_ser—Cornus sericea; Co_san_san—Cornus sanguinea subsp. sanguinea; Co_san_aus—Cornus sanguinea subsp. australis.
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Figure 3. Ratio of viable (green) and non-viable (blue) seeds in different soil layers. (a)—in the upper layer; (b)—in the lower layer. Abbreviations of taxa: Co_alb—Cornus alba; Co_ser—Cornus sericea; Co_san_san—Cornus sanguinea subsp. sanguinea; Co_san_aus—Cornus sanguinea subsp. australis.
Figure 3. Ratio of viable (green) and non-viable (blue) seeds in different soil layers. (a)—in the upper layer; (b)—in the lower layer. Abbreviations of taxa: Co_alb—Cornus alba; Co_ser—Cornus sericea; Co_san_san—Cornus sanguinea subsp. sanguinea; Co_san_aus—Cornus sanguinea subsp. australis.
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Table
Table 1. List of the study sites of the Cornus soil seed bank in Lithuania, with their administrative position, geographical coordinates and EUNIS habitat types.
Table 1. List of the study sites of the Cornus soil seed bank in Lithuania, with their administrative position, geographical coordinates and EUNIS habitat types.
Site NameAdministrative UnitLongitude (°E)Latitude (°N)EUNIS Habitat Type
Cornus alba
PanevėžysPanevėžys city55.7527024.31168S92
SurgėliaiŠirvintos distr.55.0149624.90851S92
KiemeliaiVilnius distr.54.8570925.01377T1J
TrakaiTrakai distr.54.6563024.90519V64
AlytusAlytus city54.3880624.00010T1J
Cornus sericea
JuodlėKelmė distr.55.8148922.92023T1F
KlaipėdaKlaipėda city55.6586721.23459T12
JurbarkasJurbarkas city55.0817122.72513V64
ŽiežmariaiKaišiadorys distr.54.8156424.44084T1J
DarsūniškisKaišiadorys distr.54.7477824.13509T12
Cornus sanguinea subsp. sanguinea
RaguviškiaiKretinga distr.55.8599521.39046T11
ŠilinėJurbarkas distr.55.0885622.94780T1B
PiepaliaiKaunas distr.55.0742323.78337S35
VilniusVilnius city54.7533125.29198T1E
LiūnelisLazdijai distr.54.1271323.66146S35
Cornus sanguinea subsp. australis
ŠvobiškisPasvalys distr.56.0546324.16271V64
ŠiauliaiŠiauliai city55.9315423.28444S35
KaišiadorysKaišiadorys city54.8709924.43677V64
MaišiagalaVilnius distr.54.8695925.05138T1J
VievisElektrėnai distr.54.7709424.83838V64
Table
Table 2. Total number of seeds in both upper and lower soil layers, number and percentage of intact and damaged as well as viable and non-viable seeds of the studied Cornus taxa in the upper and lower soil layers.
Table 2. Total number of seeds in both upper and lower soil layers, number and percentage of intact and damaged as well as viable and non-viable seeds of the studied Cornus taxa in the upper and lower soil layers.
TaxaC. albaC. sericeaC. sanguinea subsp. sanguineaC. sanguinea subsp. australis
Total number in both layers11834337121547
Upper soil layer (0–5 cm)
Total number of seeds11004026311347
Percentage of the total number of seeds93.392.888.687.1
Number of damaged seeds 318168201317
Percentage of damaged seed in the layer28.941.831.923.5
Number of intact seeds7822344301030
Percentage of intact seed in the layer71.158.268.176.5
Number of viable seeds3189680466
Number of non-viable seeds464138350564
Lower soil layer (5–10 cm)
Total number of seeds833181200
Percentage of the total number of seeds6.87.211.412.9
Number of intact seeds741044117
Percentage of intact seed in the layer89.238.754.358.5
Number of damaged seeds 9193783
Percentage of damaged seed in the layer10.861.345.741.5
Number of viable seeds396852
Number of non-viable seeds3543665
Table
Table 3. Mean density of intact, viable and non-viable seeds (mean ± SD) per 1 m−2 and percentage of viable and non-viable seeds in the upper soil layer (0–5 cm) of individual sites and all sites pooled of the studied Cornus taxa. Different lower-case and capital letters denote statistically significant differences between the means among the sites and taxa, respectively, applying Dunn’s post hoc test.
Table 3. Mean density of intact, viable and non-viable seeds (mean ± SD) per 1 m−2 and percentage of viable and non-viable seeds in the upper soil layer (0–5 cm) of individual sites and all sites pooled of the studied Cornus taxa. Different lower-case and capital letters denote statistically significant differences between the means among the sites and taxa, respectively, applying Dunn’s post hoc test.
Site NameIntact SeedsViable SeedsNon-Viable SeedsViable Seeds (%)Non-Viable Seeds (%)
Cornus alba
Panevėžys1095 ± 480 a430 ± 267 a665 ± 283 a39.360.7
Surgėliai555 ± 361 b250 ± 191 ab305 ± 199 b45.055.0
Kiemeliai590 ± 346 b185 ± 224 b405 ± 246 b31.468.6
Trakai415 ± 308 b185 ± 182 b230 ± 210 b44.655.4
Alytus1255 ± 857 a540 ± 554 a715 ± 434 a43.057.0
All sites pooled782 ± 601 A318 ± 348 A464 ± 348 A40.759.3
Cornus sericea
Juodlė240 ± 330 a65 ± 79 abc175 ± 268 a27.172.9
Klaipėda285 ± 323 a180 ± 248 ab105 ± 124 a63.236.8
Jurbarkas255 ± 161 a30 ± 56 ac225 ± 126 b11.888.2
Žiežmariai150 ± 105 a80 ± 87 abc70 ± 78 a53.346.7
Darsūniškis240 ± 266 a125 ± 122 b115 ± 174 a52.147.9
All sites pooled234 ± 252 B96 ± 147 B138 ± 177 B41.059.0
Cornus sanguinea subsp. sanguinea
Raguviškiai825 ± 795 a215 ± 347 a610 ± 500 a26.173.9
Šilinė120 ± 161 b15 ± 36 b105 ± 143 b12.587.5
Piepaliai615 ± 453 a105 ± 156 ac510 ± 356 a17.182.9
Vilnius70 ± 117 b20 ± 51 b50 ± 81 b28.671.4
Liūnelis525 ± 265 a45 ± 59 bc480 ± 238 a8.691.4
All sites pooled431 ± 517 C80 ± 197 B351 ± 386 C18.681.4
Cornus sanguinea subsp. australis
Švobiškis2280 ± 1248 a585 ± 408 a1695 ± 998 a25.774.3
Šiauliai345 ± 268 bd170 ± 149 b175 ± 176 bd49.350.7
Kaišiadorys605 ± 309 c1390 ± 1810 a345 ± 269 ac80.119.9
Maišiagala185 ± 193 b130 ± 152 bc55 ± 74 d70.329.7
Vievis1735 ± 1912 cd55 ± 112 c550 ± 291 e9.190.9
All sites pooled1030 ± 1315 A466 ± 978 A564 ± 769 AC45.254.8
Table
Table 4. GLMM results for the intact seed density in the upper (0–5 cm) and lower (5–10 cm) soil layers. Taxa were considered as a fixed effect (f), whereas locality was considered as a random effect (r). SE—standard error; SD—standard deviation.
Table 4. GLMM results for the intact seed density in the upper (0–5 cm) and lower (5–10 cm) soil layers. Taxa were considered as a fixed effect (f), whereas locality was considered as a random effect (r). SE—standard error; SD—standard deviation.
EffectsEstimateSEz-Valuep-ValueVarianceSD
Upper layer
f C. alba1.9660.2986.60<0.001
f C. sericea 0.8200.3032.71<0.01
f C. sanguinea subsp. sanguinea1.0790.3043.55<0.001
f C. sanguinea subsp. australis1.8390.2996.15<0.001
r Locality 0.4360.660
Lower layer
f C. alba−0.4400.458−0.960.336
f C. sericea−2.3650.546−4.33<0.001
f C. sanguinea subsp. sanguinea−1.4950.515−2.90<0.001
f C. sanguinea subsp. australis−0.4140.468−0.890.376
r Locality 0.9610.980
Table
Table 5. GLMM results for the intact seed density in the upper (0–5 cm) and lower (5–10 cm) soil layers. Taxa were considered as a fixed effect (f) and the cover of Cornus was considered as a random effect (r). SE—standard error; SD—standard deviation.
Table 5. GLMM results for the intact seed density in the upper (0–5 cm) and lower (5–10 cm) soil layers. Taxa were considered as a fixed effect (f) and the cover of Cornus was considered as a random effect (r). SE—standard error; SD—standard deviation.
EffectsEstimateSEz-Valuep-ValueVarianceSD
Upper layer
f C. alba1.9390.2418.04<0.001
f C. sericea0.6500.2522.59<0.01
f C. sanguinea subsp. sanguinea1.2240.2435.04<0.001
f C. sanguinea subsp. australis1.9880.2428.22<0.001
r Cornus cover 0.2790.528
Lower layer
f C. alba−0.3990.498−0.800.423
f C. sericea−1.1670.573−2.82<0.01
f C. sanguinea subsp. sanguinea−1.3130.519−2.530.011
f C. sanguinea subsp. australis 0.6610.5041.310.190
r Cornus cover 1.1271.062
Table
Table 6. Mean density of intact, viable and non-viable seeds (mean ± SD) per 1 m−2 and percentage of viable and non-viable seeds in the lower soil layer (5–10 cm) of individual sites and all sites pooled of the studied Cornus taxa. Different lower-case and capital letters denote statistically significant differences between the means among the sites and taxa, respectively, applying Dunn’s post hoc test.
Table 6. Mean density of intact, viable and non-viable seeds (mean ± SD) per 1 m−2 and percentage of viable and non-viable seeds in the lower soil layer (5–10 cm) of individual sites and all sites pooled of the studied Cornus taxa. Different lower-case and capital letters denote statistically significant differences between the means among the sites and taxa, respectively, applying Dunn’s post hoc test.
Site NameIntact SeedsViable SeedsNon-Viable SeedsViable Seeds (%)Non-Viable Seeds (%)
Cornus alba
Panevėžys25 ± 64 a10 ± 31 a15 ± 49 a40.060.0
Surgėliai50 ± 100 ab25 ± 64 a25 ± 44 ab50.050.0
Kiemeliai90 ± 129 a40 ± 82 a50 ± 76 ab44.455.6
Trakai110 ± 137 b60 ± 109 a50 ± 61 b54.545.5
Alytus95 ± 123 b60 ± 109 a35 ± 49 ab63.236.8
All sites pooled74 ± 116 A39 ± 84 A35 ± 56 A52.747.3
Cornus sericea
Juodlė10 ± 31 a10 ± 31 a0 a1000
Klaipėda0 a0 a0 a00
Jurbarkas15 ± 67 a5 ± 22 a10 ± 44 a33.366.7
Žiežmariai10 ± 30 a10 ± 30 a0 a1000
Darsūniškis15 ± 37 a5 ± 22 a10 ± 31 a33.366.7
All sites pooled10 ± 43 B6 ± 24 B4 ± 24 B60.040.0
Cornus sanguinea subsp. sanguinea
Raguviškiai125 ± 141 a30 ± 57 a95 ± 94 a24.076.0
Šilinė0b0 b0 b00
Piepaliai15 ± 37 b5 ± 22 b10 ± 31 b33.366.7
Vilnius5 ± 22 b0 b5 ± 22 b0100
Liūnelis75 ± 107 a5 ± 22 b70 ± 103 a6.793.3
All sites pooled44 ± 94 C8 ± 31 B36 ± 75 A18.281.8
Cornus sanguinea subsp. australis
Švobiškis315 ± 287 a95 ± 94 a220 ± 238 a30.269.8
Šiauliai35 ± 59 b35 ± 59 bc0 b1000
Kaišiadorys170 ± 210 c110 ± 174 ab60 ± 88 c64.735.3
Maišiagala5 ± 22 bd5 ± 22 c0b1000
Vievis60 ± 114 a15 ± 37 c45 ± 115 bc25.075.0
All sites pooled117 ± 201 A52 ± 102 A65 ± 147 A44.455.6
Table
Table 7. GLMM results for the intact seed density in the upper (0–5 cm) soil layer. Taxa were considered as a fixed effect (f) and the habitat type was considered as a random effect (r). SE—standard error; SD—standard deviation.
Table 7. GLMM results for the intact seed density in the upper (0–5 cm) soil layer. Taxa were considered as a fixed effect (f) and the habitat type was considered as a random effect (r). SE—standard error; SD—standard deviation.
EffectsEstimateSEz-Valuep-ValueVarianceSD
Upper layer
f C. alba2.0140.14613.81<0.001
f C. sericea0.9900.1556.38<0.001
f C. sanguinea subsp. sanguinea1.5450.15010.33<0.001
f C. sanguinea subsp. australis 1.9710.14613.53<0.001
r Habitat type 0.05790.2407
Table
Table 8. Number of intact seeds of Cornus taxa in different habitats in the upper (0–5 cm) and lower (5–10 cm) soil layer. Different letters indicate significant differences (p < 0.05) applying Dunn’s post hoc z-test. S—Heathlands, scrub and tundra; T—Forests and other wooded land; V—Vegetated human-made habitats.
Table 8. Number of intact seeds of Cornus taxa in different habitats in the upper (0–5 cm) and lower (5–10 cm) soil layer. Different letters indicate significant differences (p < 0.05) applying Dunn’s post hoc z-test. S—Heathlands, scrub and tundra; T—Forests and other wooded land; V—Vegetated human-made habitats.
TaxaScrub (S)Forest (T)Human-Made (V)
Upper layer
C. alba825 ± 500 a923 ± 728 a415 ± 308 b
C. sericea–229 ± 271 a255 ± 161 a
C. sanguinea subsp. sanguinea570 ± 369 a337 ± 193 b–
C. sanguinea subsp. australis345 ± 268 a185 ± 193 a1540 ± 1485 b
Lower layer
C. alba38 ± 84 a93 ± 125 b110 ± 137 b
C. sericea–10 ± 34 a20 ± 70 a
C. sanguinea subsp. sanguinea45 ± 85 a43 ± 100 a–
C. sanguinea subsp. australis35 ± 59 a5 ± 22 a182 ± 237 b
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Petrulaitis, L.; Rašomavičius, V.; Uogintas, D.; Gudžinskas, Z. Soil Seed Bank of Alien and Native Cornus (Cornaceae) Taxa in Lithuania: What Determines Seed Density and Vertical Distribution in Soil? Diversity 2022, 14, 488. https://doi.org/10.3390/d14060488

AMA Style

Petrulaitis L, Rašomavičius V, Uogintas D, Gudžinskas Z. Soil Seed Bank of Alien and Native Cornus (Cornaceae) Taxa in Lithuania: What Determines Seed Density and Vertical Distribution in Soil? Diversity. 2022; 14(6):488. https://doi.org/10.3390/d14060488

Chicago/Turabian Style

Petrulaitis, Lukas, Valerijus Rašomavičius, Domas Uogintas, and Zigmantas Gudžinskas. 2022. "Soil Seed Bank of Alien and Native Cornus (Cornaceae) Taxa in Lithuania: What Determines Seed Density and Vertical Distribution in Soil?" Diversity 14, no. 6: 488. https://doi.org/10.3390/d14060488

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