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Agronomy Journal 95:191-198 (2003)
© 2003 American Society of Agronomy

SEED

Soil Texture Involvement in Germination and Emergence of Buried Weed Seeds

Stefano Benvenuti*

Dipartimento di Agronomia e Gestione dell'Agroecosistema, Università di Pisa, Via S. Michele degli Scalzi 2, 56124 Pisa, Italy

* Corresponding author (sbenve{at}agr.unipi.it)

Received for publication April 3, 2002.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
Laboratory trials were performed to test germination and emergence characteristics of jimsonweed (Datura stramonium L.) seeds buried in 10 different soil types (with or without the control of soil external gas environment) with pronounced sandy or clay texture. The aim of the experiments was to investigate if the physical characteristics of the soils were involved in both buried-seed ecology and emergence dynamics. Germination inhibition due to burial depth was found to be directly proportional to clay content and inversely proportional to sand content. Measurement of soil air permeability showed a close relation between gas exchange potential and depth-mediated germination inhibition. Comparative analysis of the germination response in nonsoil and soil hypoxia suggested that inhibition is caused not so much by hypoxia per se as by the presence of fermenting metabolites that could not easily be eliminated due to decreased respiratory activity. In situ inspection of buried seeds also revealed that the increased time required for emergence in clay soils is primarily due to increased mean germination time rather than greater difficulty in seedling penetration upwards through the soil before emergence. Partial removal of germination inhibition of buried seeds was facilitated by elevated air oxygen availability but only with sandy soils, showing that inhibition is closely linked to soil ability to induce gas exchange with external air. At excessive burial depth (12 cm), seeds exhibited induction of secondary dormancy independent of soil texture. In conclusion, these experiments demonstrated that soil physical properties have a strong effect on buried-seed ecology and consequently on seedbank dynamics in the agroecosystem.

Abbreviations: D50%, burial depth inducing 50% emergence inhibition • MGT, mean germination time


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
THE GROWING AGRONOMIC INTEREST in forecasting (Alm et al., 1993) and modeling (Grundy et al., 1996) seedbank emergence dynamics has led to increasing interest in studies investigating the relations between ecological soil factors and buried weed seed germination and dormancy (Buhler et al., 1997). It is now widely believed that knowledge of the seedbank germination response to climatic (Forcella et al., 1992), ecological (Benvenuti and Macchia, 1997), and agronomic (Froud-Williams et al., 1984) factors is essential to rationalize direct and indirect weed control. Numerous studies have focused on the relations between weed seed germination and various soil characteristics such as light permeability (Benvenuti, 1995), humidity (Forcella, 1993), and temperature (Nusbaum et al., 1985) and also on the interactions responsible for cyclical induction of secondary dormancy (Baskin and Baskin, 1985). In addition, studies have examined the relation between agricultural practices and emergence dynamics both as a function of seed depth distribution in soil (Cousens and Moss, 1990) and of seed ability to emerge from increasing burial depth (Cussans et al., 1996). The latter aspect has also been studied in an ecological perspective to identify the physiological causes that prevent deeply buried seed from germinating; results obtained so far suggest this is partly due to the lack of a light trigger (Benvenuti and Macchia, 1998) and primarily to the limitation on soil gas diffusion (Benvenuti and Macchia, 1995). It is well known that such factors are linked to soil porosity, which in turn is closely linked to soil texture (Radford and Greenwood, 1970), thus making it possible to predict the relative gas diffusion coefficients (Moldrup et al., 2000). Although it has been ascertained that certain types of soil texture limit soil oxygen transport (Refsgaard et al., 1991), to the point of affecting soil microbiological respiration (Sierra and Renault, 1996), this phenomenon has never been examined in relation to weed seed germination and emergence potential.

The purpose of this study was thus to assess whether and to what extent soil texture characteristics can represent a useful parameter for simulating emergence dynamics of buried weed seeds. Jimsonweed was selected as the experimental system because this annual species forms a persistent seedbank as a consequence of its survival strategy based on seed dormancy and longevity (Reisman-Berman et al., 1991), which makes it one of the most important summer annual weeds.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
General Procedure
Trials were performed at the Seed Research and Testing Station (International Seed Testing Association approved) of the Agronomy Department of Pisa University. Seeds of jimsonweed were harvested in late summer 2000 near Pisa (Tuscany), Italy (43°43' N, 10°24' E). Ripe seeds were cleaned and stored at room temperature in darkness until use in the following spring. Before use, seeds were chilled for 1 mo at 4°C to overcome internal dormancy.

Soils
Various soil types were collected (layer 0–20 cm) by means of a metal probe in different areas of Tuscany. Soils were chosen as a function of granulometric composition, either decidedly sandy [S. Piero (Pisa), Tirrenia (Pisa), Viareggio (Lucca), Orbetello (Grosseto) and S. Rossore (Pisa)] or clay [Asciano (Pisa), Volterra (Pisa), S. Luce (Pisa), Peccioli (Pisa) and Coltano (Pisa)]. Soil samples were then air-dried and crushed with a metal pestle to break up the soil aggregates that are particularly abundant in soils with a clay matrix. Soils were sieved (1-mm metal mesh) before use as substrate for germination and emergence tests. Table 1 shows the chemical–physical characteristics of the soils utilized.


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  		Table 1. Chemical and physical characteristics of the 10 soils used in the experiments.

 
Seedings
Plastic pots were filled gravimetrically with the different soils and packed with a uniform strength to avoid differential resistance to seedling emergence. Seeding depths were 0, 1, 2, 4, 8, or 12 cm. Some of the seeding experiments were performed using stainless steel boxes (10 by 25 cm, with 20-cm depth) equipped with transparent glass windows along the sides to allow inspection of the buried seeds and thereby monitor germination in situ. In other cases, seeds were sown in transparent plastic vials (3 cm diam. and 12 cm high), which could likewise be inspected and could also be inserted into glass jars (1.000 cm3) with hermetic-seal screw tops and equipped with two (entry and exit) taps for supplying and trapping air or pure oxygen.

Buried-Seed Incubation
Seeded pots were placed in climate-controlled cabinets preset to alternating temperatures of 25 and 30°C and to 12 and 12 h (day and night) of photoperiod. Light intensity of 100 µmol m-2 s-1 was produced by cool fluorescent tubes (TLF 20W/33, Philips, Eindhoven, the Netherlands) and measured with a spectroradiometer (Model 1800 LI-COR, Lincoln, NE). During incubation, pots were moistened by subirrigation.

Calculation of Depth of Fifty Percent Emergence Inhibition
For each seeding depth, percentage of depth inhibition was calculated for each soil as a function of unburied seed germination (0% inhibition). Means of inhibition data of each tested soil type were fitted by a polynomial regression that adequately described the biological response of weed seed germination and emergence. These equations gave the soil depths at which emergence rates reached 50% by using a modified x-intercept method (Wiese and Binning, 1987). The intercept between the polynomial regression and the translated x-axis on the selected y-axis for burial depth inducing 50% emergence inhibition (D50%) shows the relative soil depth inhibition for each soil type. The D50% and soil physical characteristics (texture and gas diffusion data) were fitted by linear regressions.

Measurement of Soil Air Permeability
Determinations were conducted by setting up a simple measurement system, as in the diagram shown in Fig. 1, analogous to that described by other authors (Iversen et al., 2001). The flow of gas through porous media is at a low pressure gradient comparable to water flow and follows Darcy's law (Darcy, 1983).



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  		Fig. 1. Diagrammatic representation of the equipment utilized to measure soil diffusion characteristics. For details on the functioning of the system, see Iversen et al. (2001).

 

where q is the specific air flow rate [liter per unit of time (L T-1)], Ka is the air permeability (L2), p is the pressure [volumetric mass per liter per unit of time (M L-1 T-2)], µ is the dynamic gas viscosity (M L-1 T-1) corrected for temperature, and x is the distance (in flow direction) (L). Air permeability of exhumed soil samples (Ka) was calculated by using the following integration of the above equation:

where Q is the volumetric flow rate (L3 T-1), {Delta}P is the pressure difference across the sample (M L-1 T-2), as is the cross-sectional area (L2), and Ls is the length of the sample (L).

Measurements were taken on all soils with water content uniformed to the relative field capacity. Data are given as percentage of air permeability compared with that measured on quartz sand (particles about 200–1000 µm) commonly used in the International Seed Testing Association laboratory for emergence tests on various crops.

Hypoxia Germination without Soil
Seeds were placed in uncovered Petri dishes (6 cm diam.) on filter paper (Wathman no. 1, Fisher Scientific, Pittsburgh, PA), which were then inserted into the above-described glass jars connected with the selected hypoxic gas (1, 5, or 10% of O2 mixed with inert N2). Incubation was performed in the same environmental conditions as described earlier for the climate-controlled cabinets. Radicle protrusion was taken to be the criterion for germination.

Seed Respiration Measurements
Oxygen uptake was determined using a Clark-type electrode (oxymeter, Clark-type electrode, Hansatec, Norfolk, England). The oxygen electrode chamber was filled with 2 mL of distilled water. Seeds were added 10 at a time, with a still bar circulating them around the chamber to maintain a stable oxygen gradient across the membrane. The instrument was calibrated with sodium dithionite (NaS2O4), and measurements were taken within a maximum period of 10 min to avoid changes in seed respiratory activity caused by return to normoxic conditions. Data were expressed as nmol of O2 per seed per 10 min.

Mean Germination Time
Inspection of the boxes with transparent panels made it possible to record the time actually taken by buried seeds to achieve germination (radicle protrusion). Thus, despite seed burial, mean germination time (MGT) could be determined by means of the following formula:

where n is number of seeds germinated on day g and N is the total number of germinated seeds. The same formula was used to calculate mean emergence time, considering cotyledon extension as the criterion for successful emergence. Inspection of the boxes also allowed calculation of the time of pre-emergence growth by subtracting MGT from mean emergence time.

Ungerminated Seed Recovery
After the emergence test, soil was removed from pots and washed. A fine metal sieve (400 µm) was used for seed recovery. Ungerminated seeds from each pot (of each soil type) from the burial depth of 12 cm were imbibed on filter paper in Petri dishes and incubated in the same environmental conditions as adopted for the germination tests.

Statistical Analysis
The treatments were replicated three times and each experiment repeated twice. A completely randomized design was adopted. Data were pooled over the two experiments because there was no interaction. After the homogeneity test of variance, arcsine transformation of emergence percentages was necessary. Angular values were subjected to ANOVA using the Student–Newman–Keuls test (p < 0.05 and/or p < 0.01) for separation of means. For each statistical analysis, commercial software (CoHort software, Minneapolis, MN) was used.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSION
 REFERENCES
 
Figure 2A shows jimsonweed seedling emergence as a function of both seed burial at increasing depth (0, 1, 2, 4, 8, and 12 cm) and the type of substrate utilized (sandy or clay soil or quartz sand). Clay soils resulted in the greatest decrease in energy, with a burial depth of 4 cm being sufficient to halve seedling emergence compared with emergence without burial (on the soil surface). Emergence was less affected in sandy soil and even less in pure quartz sand. In the latter case, more than 20% emergence was achieved even from a burial depth of 8 cm. However, in no case was emergence from a burial depth of 12 cm observed. Failed emergence was due almost exclusively to failed germination as suicide germination resulting from exhaustion of seed energy reserves during pre-emergence was detected only in very rare cases (data not shown).



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  		Fig. 2. (A) Effect of increasing soil depth (0, 1, 2, 4, 8, and 12 cm) on seedling emergence. Polynomial regressions (significant for p < 0.01) are given for quartz sand (y = 0.11X3 - 2.08X2 + 1.71X + 85; R2 = 0.98), sandy soils (y = 0.26X3 - 1.85X2 - 12.68X + 85; R2 = 0.98), and clay soils (y = -0.03X3 + 1.59X2 - 21.76X - 0.4; R2 = 0.98). (B) Soil depth inhibition for quartz sand (y = -0.13X3 + 2.43X2 - 2.0X + 0.4; R2 = 0.98), sandy soils (y = -0.16X3 + 2.48X2 + 2.08X - 0.4; R2 = 0.98), and clay soils (y = 0.04X3 + 1.84X2 + 25.04X - 3; R2 = 0.98). D50%, soil depths inducing 50% emergence inhibition.

 
In addition, a relation (second-degree equation) was found between depth-mediated inhibition and seed weight (Benvenuti et al., 2001), with germination of very small seeds being almost completely inhibited even at extremely shallow burial depths. This phenomenon appears of notable importance as a survival strategy of population dynamics because it tends to protect a considerable portion of the seedbank against a risky germination that would be unlikely to result in successful emergence. Conditions unfavorable to emergence arise as a consequence of the normal tillage operations performed in an agroecosystem, which tend to distribute the majority of annually produced seeds through the soil profiles (Grundy et al., 1996); thus, seeds germinated from an excessive depth would undergo a heterotrophic stage (during pre-emergence growth) that would be too protracted for their limited energy reserves. This depth-mediated germination inhibition (Fig. 2B), which is well represented by significant (p < 0.01) polynomial regressions, was found to be greatest in clay soils. The D50% was calculated to be as little as 3.2 cm in clay soils. This index rose to 5.3 cm in sandy soils and to 6.1 cm in the case of pure quartz sand. Significant (p < 0.01) linear regressions between clay (Fig. 3A) and sand (Fig. 3B) particle content and D50% revealed that these two soil components had opposite effects in terms of favoring (clay soil content percentage) or inhibiting (sand soil content percentage) depth-mediated inhibition.



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  		Fig. 3. (A) Linear regression (significant for p < 0.01) between clay percentage in clay soils and depth resulting in 50% emergence inhibition. (B) Linear regression (significant for p < 0.01) between sand percentage in sandy soils and depth resulting in 50% emergence inhibition.

 
The results thus indicate that the annual germination and emergence rate of weed seeds in the seedbank is a function not only of climate and biological characteristics of the various species, but also of soil granulometric composition. The relation between active flora and the seedbank is directly proportional to soil sand content. This can have adverse agronomic repercussions in sandy soils due to the tendency of the weed seeds to germinate from a wider range of depths (implying a greater transition to active flora), but it can also have positive effects in that sandy soils are less suited for long-term accumulation of a seedbank. In contrast, soils with a strong clay matrix are characterized by a lower field emergence rate but, conversely, also by a greater tendency to accumulate a persistent seedbank over time.

Although the physiological causes of this different degree of buried-seed germination inhibition have not yet been fully clarified, our data appear to confirm that inhibition is mediated not so much by the actual quantity of oxygen present in the various soil horizons, but by the specific characteristics of soil gas diffusion (Benvenuti and Macchia, 1995). To carry out an in-depth investigation of the ecological and physical causes of this important aspect, we measured soil physical characteristics and analyzed the findings in relation to the above-described emergence data. The significant (p < 0.01) linear regression between D50% and soil air permeability (Fig. 4) confirms that the decrease in germination observed with increasing burial depth was linked to poor gas exchange in the environment surrounding buried seeds. This is a crucial point as germinating seeds produce volatile toxic metabolites resulting from the onset of fermenting metabolism (acetaldehyde, methanol, and acetone; Holm, 1972) insofar as fermentation is possible based on the degree of hypoxia inevitably induced by limited soil oxygen exchange. What this means is that germination inhibition is not directly attributable to pre-existing soil hypoxia but rather to the hypoxic conditions that occur when seed respiration rate increases in consequence of the germination trigger. Thus, during this phase, soil limitations on oxygen replenishment tend to intensify the hypoxia already induced by partial permeability of seed coat to gases (Gutterman et al., 1992). In this regard, it is worth noting that the seed coat (Botha et al., 1992) induces a natural seed fermentation metabolism during the early stages of germination (resulting in ethanol production), even under normoxic conditions, by causing a hypoxic internal atmosphere. Removal of such fermenting metabolites has also been shown to play a crucial role in promoting or inhibiting germination (Norton, 1986). The greater air permeability measured in sandy soils is thus of major importance both in limiting hypoxia phenomena (more rapid oxygen exchange with the soil surface) and in removing germination-inhibiting volatile metabolites. The finding that toxicity arises in a hypoxic atmosphere by triggering fermenting metabolism is further confirmed in studies on maize (Zea mays L.) seeds subjected to flooding (Martin et al., 1991). In this case too, tolerance of hypoxia was enhanced by removal of toxic metabolites.



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  		Fig. 4. Linear regression (significant for p < 0.01) between soil depth resulting in 50% emergence inhibition and soil gas diffusion (as percentage of quartz sand). Measurements were taken at field capacity water content.

 
Figure 5A shows germination percentage and time required for germination with increasing hypoxia when seeds were incubated outside of the soil environment. It can be observed that only when decidedly elevated levels of hypoxia were reached (below 5% O2) did hypoxia per se impede or cause a noticeable slowing of germination (increase in MGT). When air oxygen levels were roughly halved (10%), germination was reduced by no more than about 15%. Because soil O2 concentration reaches these levels only in exceptional circumstances (prolonged flooding) (Drew, 1990), it is clear that this cannot be the cause of buried-seed germination inhibition.



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  		Fig. 5. (A) Germination and relative mean germination time (MGT) as a function of oxygen content (21, 10, 5, 1, 0.5 and 0%) in the seed incubation environment. (B) Seed respiration (after 3 d of incubation) at the various levels of oxygen availability. In both graphs, vertical bars indicate standard errors of the means.

 
Figure 5B shows seed respiration under increasing levels of hypoxia. It can be observed that oxygen concentration is directly proportional to seed respiration; thus, 50% reduction in O2 concentration resulted in almost 50% decrease in incubated seed respiration. More severe levels of hypoxia were associated with greater reduction in oxygen consumption. The above-described slowing of germination can thus be attributed to a decrease in the seed respiration rate. It is also evident that part of the seed energy metabolism during pregermination derives from the onset of the fermenting mechanism (Richard et al., 1994), whose target as final electron acceptor is represented by the organic compounds (i.e., volatile metabolites), which once formed, are then responsible for germination inhibition. Thus, in a nonsoil environment (soil surface), hypoxia seems to cause only limited reduction in germination because conditions for removal of toxic metabolites springing from fermentation processes are nonlimiting.

In soil, on the other hand, the sudden increase in oxygen consumption by germinating seed together with the limited potential for gaseous exchange creates a hypoxic environment in the immediate surroundings of the seed. Thus, Fig. 6A shows that the time required for buried-seed germination increased not only as a function of burial depth, but also as a function of the physiological characteristics of the two soil typologies studied. By inspecting the buried seeds through the transparent panels, it was observed that delayed seedling emergence was due not so much to the difficulty of penetrating upwards through the substrates before emergence (linear penetration, Fig. 6B), but rather to the development of a gaseous environment whose degree of hypoxia was a function of soil gas permeability.



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  		Fig. 6. (A) Mean germination time (MGT) observed at different burial depths in sandy or clay soil. Means are followed by relative standard errors. Significance levels (*p < 0.05, **p < 0.01) of the mean differences are shown at the top of the graph. Polynomial regressions are indicated. (B) Linear regressions (significant for p < 0.01) between seedling pre-emergence time and burial depths for both clay and sandy soils. In both graphs, vertical bars indicate standard errors of the means.

 
In agreement with this interpretation, the increase in time required for germination was well fitted by significant (p < 0.01) second-degree polynomial regressions. In other words, the MGT data suggest that the different characteristics of gas diffusion of the two soil types induced a degree of hypoxia proportional to their potential to promote oxygen exchange with the soil surface. The degree of temporary hypoxia (during germination) induced an increase in MGT similar to that observed in the nonsoil germination tests. It is worth pointing out that similar results were observed in clay-coated seeds of sweet pepper (Capsicum annuum L.) (Sachs et al., 1981), whose germination speed depends on the physical characteristics of pellet coating and the related properties of seed coat permeability to oxygen.

To obtain further confirmation of the hypothesis put forward here, seeds were buried (laterally, to allow in situ inspection) in purpose-designed transparent vials and subjected to diversified availability of external oxygen (air or 100% oxygen). This made it possible to determine whether the difference in gas diffusion potential between the various soils plays a role in promoting oxygen exchange in the microenvironment surrounding buried seeds. Figure 7 illustrates in situ germination of seed buried at D50% (3.2 cm in clay soils and 5.3 cm in sandy soils). In clay soils (Fig. 7A), the limited potential for gas diffusion prevented buried seeds from drawing on the elevated external availability of oxygen. In contrast (Fig. 7B), greater air permeability in sandy soil seems to be primarily responsible for partial removal of depth-mediated inhibition. Thus, in conditions of elevated external oxygen availability, in situ germination in sandy soil rose significantly (p < 0.05) from 50 to almost 80%.



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  		Fig. 7. In situ germination percentage (in transparent vials) in both (A) clay and (B) sandy soils in the presence of soil external air or oxygen. In both soil types, the relative seeding depth was selected at which previous experiment has showed soil depths inducing 50% emergence inhibition. Vertical bars indicate standard errors of the means. Means followed by the same letter do not differ at p < 0.05 according to the Student–Newman–Keuls LSD test.

 
Figure 8 shows seed germination following depth-mediated inhibition in both soil typologies tested. The elevated germination (roughly 80%) displayed by control seeds (before burial) decreased significantly (p < 0.05) to roughly 15% after burial in deep layers of the two soil types. In both cases, seeds recovered after burial showed elevated dormancy independently of the soil type used for seed incubation. This induction of secondary dormancy was observed in a previous study and attributed to anaerobiosis (or pronounced hypoxia) of the seed incubation environment (Benvenuti and Macchia, 1995). In the present case, however, it is evident that the hypoxia conditions responsible for dormancy induction are due to deep burial independent of gas diffusion. In other words, seed burial at elevated depth results in an analogous ecological situation (probably on account of saturation of the factor inducing seed dormancy) independent of soil physical characteristics.



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  		Fig. 8. Germination percentage before (control) and after deep burial (12 cm) in both clay and sandy soils. Vertical bars indicate standard errors of the means. Means followed by the same letter do not differ at p < 0.05 according to the Student–Newman–Keuls LSD test.

 

   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
REFERENCES
 
The experiments confirmed the necessity to correlate weed seedling emergence with soil properties for a correct interpretation of weed seedling performance. The possibility of integrating agronomic knowledge with the ecophysiology of the seedbank is crucial for prediction of seedling emergence dynamics; in particular, this is of considerable advantage in agricultural systems designed according to the principle of safeguarding the environment, which need to maximize the efficacy and timeliness of direct and indirect weed control measures (Oriade and Forcella, 1999). In this regard, it is important to note that indirect weed control mechanisms based on so-called false seedings may be invalidated by the fact that soils with a pronounced clay matrix impede germination of buried seeds and induce seed dormancy. The data of the present study demonstrate that clay soils can represent the ideal pedologic conditions for accumulation of an elevated persistent seedbank. The lower degree of macroporosity and consequently gas diffusion correlated with such soils (Moldrup et al., 2000) also appears to limit in situ oxygen availability, known to be closely linked to the characteristic of seed longevity (Hendry, 1993), which is in any case, markedly elevated in many species (Burnside et al., 1996).

The above-described impediments to soil gas exchange and consequently seedbank germination could be enhanced by the tendency towards soil compaction. In clod-forming soils, weed seeds are contained inside the clods (Pareja et al., 1985) where they remain dormant until the clods and aggregates are broken up into smaller units (Terpestra, 1995). Tillage techniques used for seedbed preparation are therefore likely to play a crucial role in modulating the level of weed seed germination and consequently the weed development dynamics. Future studies on the involvement of additional ecological factors in seedbank germination and of potential synergies among such factors will hopefully lead to more precise models of weed dynamics, permitting optimization of crop defense mechanisms designed to assure a rational balance between crop production and environmental safeguards.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 





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